114 006 Section1

Red Meat and
Processed Meat
volume 114
This publication represents the views and expert

opinions of an IARC Working Group on the
Evaluation of Carcinogenic Risks to Humans,
which met in Lyon, 6–13 October 2015
LYON, FRANCE - 2018
iarc monographs
oN the evaluation
of carcinogenic risks
to humans
1. EXPOSURE DATA
1.1 Identification of the agents by-products such as blood. It is also important

to distinguish between industrial processing
The focus of this Monograph is the consump- and household preparations. As there is a huge
tion of red meat and processed meat. These terms variety of processed meat products, it is difficult
are defined below. to sort them into categories (Santarelli et al.,
2008). However, based on recommendations by
1.1.1 Red meat the Food and Agriculture Organization of the
United Nations (FAO) (Heinz & Hautzinger,
Red meat refers to fresh unprocessed
2007), different groups of industrial processed
mammalian muscle meat (e.g. beef, veal, pork,
meats can be proposed.
lamb, mutton, horse, or goat meat), which
may be minced or frozen, and is usually (a) Cured meat pieces
consumed cooked.
Examples of cured meat include raw beef, raw
ham, cooked beef, cooked ham, corned beef, and
1.1.2 Offal bacon.
Mammalian offal refers to the internal Curing is a process by which the meat is
organs and entrails of a butchered animal (e.g. treated with a small amount of salt (sodium
scrotum, small intestine, heart, brain, kidney, chloride, NaCl, with or without potassium chlo-
liver, thymus, pancreas, testicle, tongue, tripe, or ride, KCl), with or without nitrate or nitrite salts.
stomach) consumed as such. Mammalian offal Curing enhances shelf-life by preserving and
is considered to be a specific food category in preventing the spoilage of meat. Cured meat cuts
food consumption surveys (FAO, 2015); however, are made of entire pieces of muscle meat and can
mammalian offal is reported together with red be subdivided into two groups: cured raw meats
meat in some epidemiological studies. and cured cooked meats (Pearson & Gillett,
1996; Heinz & Hautzinger, 2007; Honikel, 2010).
1.1.3 Processed meat Cured raw meats are consumed uncooked. They
do not undergo any heat treatment during prod-
Processed meat refers to any meat that has uction, which involves curing, fermentation,
been transformed through one or several of the and ripening in controlled conditions to make
following processes: salting, curing, fermenta- the meats palatable. For cured cooked meats, the
tion, smoking, or other processes to enhance raw muscle meat is always cured and then under-
flavour or improve preservation. Most processed goes treatment to achieve the desired palatability
meats are made from pork or beef, but may also (Heinz & Hautzinger, 2007).
include other red meats, poultry, offal, or meat
37
IARC MONOGRAPHS – 114
(b) Fresh industrial processed meat products (d) Fermented sausages

Examples of fresh industrial processed meat Examples of fermented sausages include
products include sausage and kebab. salami, chorizo, pepperoni, and traditional Asian
These products are mixtures composed of products such as nem.
comminuted muscle meat and animal fat in Fermented sausages are uncooked meat prod-
varying proportions. Products are salted only, ucts, and consist of coarse mixtures of lean meats
not cured. Non-meat ingredients are added in and fatty tissues combined with salt, nitrite
smaller quantities for improvement of flavour and (curing agent), sugar, spices, and other non-meat
binding, or in larger quantities for volume exten- ingredients packed into casings. Their charac-
sion (reducing costs). All meat and non-meat teristic properties (flavour, firm texture, and red
ingredients are mixed when raw. If the fresh curing colour) originate from the fermentation
meat mixture is packed into casings, the product process. Short or long ripening phases, combined
is defined as sausage. Heat treatment is applied with moisture reduction, are necessary to develop
immediately before consumption to make the the typical flavour and texture of the final product.
products palatable (Heinz & Hautzinger, 2007). The fermented sausages are not subjected to any
[The Working Group noted that a hamburger heat treatment during processing and, in most
is considered as belonging to this category of cases, are distributed and consumed raw (Heinz
processed meat when fat, salt, or other addi- & Hautzinger, 2007).
tives are added to the hamburger meat, but is
considered as red meat when it contains minced (e) Dried meat
beef only.] Examples of dried meat include dried meat
strips or flat pieces.
(c) Precooked ready-to-eat products Drying, or drying in combination with
Examples of precooked ready-to-eat products smoking, is practised all over the world and
include frankfurter, mortadella, liver sausage, is probably the most ancient method of meat
blood sausage, canned corned beef, and liver preservation.
pâté. Dried meat products result from dehydration
These products are prepared from muscle or drying of lean meat in natural or artificial
meat, fat, and other edible meat by-products conditions (Zukál & Incze, 2010). Pieces of lean
(blood and liver) or non-meat ingredients. These meat without adherent fat are cut to a specific
products are processed raw through commi- uniform shape that permits the gradual and equal
nuting and mixing. Sometimes the raw meat drying of whole batches of meat. Salt, nitrite,
material can be precooked before it is ground and sugar may be added to the meat before the
or chopped, and other ingredients are added. drying process. Many of the nutritional prop-
The resulting mixture is portioned and then erties of meat, particularly the protein content,
submitted to heat treatment to induce protein remain unchanged through drying. Common
coagulation. This leads to the typical firm, elastic dried meat products are beef jerky from the USA,
texture of precooked ready-to-eat products, as biltong from South Africa, and tasajo from South
well as a desired palatability and a certain degree America (Heinz & Hautzinger, 2007).
of bacterial stability (Heinz & Hautzinger, 2007). Meat may be smoked raw or after salting,
marinating, cooking, or other treatments. There
are many types of smoking, leading to prod-
ucts with very different sensory properties and
38
Red meat and processed meat
shelf-lives. Warm or cold smoking can be used. value of meat is also significantly affected by
Warm smoking is carried out at temperatures of the livestock production system (Lorenzo et al.,
23–45 °C. Cold smoking is carried out at temper- 2010, 2014).
atures of 12–25 °C and is used in the manufac-
(i) Protein
turing of raw fermented sausages made from
cured meats. Red meat contains 20–25 g of protein
Drying and smoking are used to improve the per 100 g. The proteins are highly digestible
shelf-life and organoleptic properties of meat (94%) and provide all essential amino acids
products. In developing countries such as Africa, (lysine, threonine, methionine, phenylalanine,
where extending shelf-life is the priority, drying tryptophan, leucine, isoleucine, and valine)
is the most used process. In parallel with simple (Williams, 2007).
drying, west Africa has refined the hot smoking (ii) Fat
process to further improve shelf-life through the Red meat is also a source of fatty acids. Fat
preservative and antibacterial effects of smoke in red meat is subcutaneous, intramuscular,
substances. To lower the cost of meat products, or intermuscular, and the composition will
African countries have also developed tradi- vary according to the animal’s age, sex, breed,
tional products consisting of mixtures of meat and diet, as well as the cut of meat (Wood &
and vegetables. Central and southern American Enser, 1997). For example, the amount of fat in
countries have adapted European meat raw cattle longissimus muscle can range from
processing techniques for local meat products, 0.59% to 16%, depending on the breed (Barnes
especially for barbecuing (e.g. chorizo criollo or et al., 2012). Fat in meat includes SFAs, mono-
morcilla) (Heinz & Hautzinger, 2007). unsaturated fatty acids (MUFAs), and PUFAs.
The typical fatty acid composition of fat in beef
1.2 Meat composition is reported to be 46.5, 48.9, and 4.59 g per 100
g of total fatty acids for SFAs, MUFAs, and
1.2.1 Red meat PUFAs, respectively. While these proportions
(a) Main components are similar in all red meats, exact amounts
depend on the type of meat (Givens, 2005). The
The animal carcass consists of muscle, main SFAs present in red meat are palmitic
connective tissue, fat and bone, and about 75% acid and stearic acid, and the main MUFA is
water, depending on the species, breed, size, oleic acid. Red meat also contains n-3 PUFAs,
and age. For a given species, the muscle is rela- such as α‑linolenic acid, and n-6 PUFAs, such
tively constant in composition (Table 1.1). Red as linoleic acid. The animal’s diet strongly
meat contains high biological value proteins influences PUFA levels in meat. For example,
and essential micronutrients, including vita- meat from foals raised by extensive production
mins and minerals (Table 1.2; Williams, 2007). systems on wood pastures has higher levels of
The composition of the meat varies based on the n-3 PUFAs than meat from foals fed concen-
animal species, sex, age, and diet, as well as the trate (Lorenzo et al., 2010, 2014). The last cate-
climate and activity during its growth (Lorenzo gory of fat found in the red meat of ruminants
et al., 2010). Total nitrogen, fat, and iron levels is conjugated linoleic acids, the levels of which
increase as the animal approaches maturity. In also depend on feeding practices (Wood et al.,
addition, the ratio of polyunsaturated fatty acids 1999; Givens, 2005).
(PUFAs) to saturated fatty acids (SFAs) decreases
with the maturity of the animal. The nutritional
39
Table 1.1 Chemical composition of typical mammalian muscle (red meat) for consumption
Main component Constituents Wet weight (%)
Water 75.00
Protein 19.00
Myofibrillar: 11.50
Myosin 5.50
Actin 2.50
Connectin 0.90
Nebulin (N2 line protein) 0.30
Tropomyosins 0.60
Troponins, C, I and T 0.60
α,β,γ Actinins 0.50
Myomesin (M-line protein) and C proteins 0.20
Desmin, filamin, F- and I-proteins, etc. 0.40
Sarcoplasmic: 5.50
Glyceraldehyde phosphate dehydrogenase 1.20
Aldolase 0.60
Creatine kinase 0.50
Other glycolytic enzymes 2.20
Myoglobin 0.20
Haemoglobin and other unspecified extracellular proteins 0.60
Connective tissue and organelles: 2.00
Collagen 1.00
Elastin 0.05
Mitochondrial etc. (including cytochrome c and insoluble enzymes) 0.95
Lipid 2.50
Neutral lipid; phospholipids; fatty acids; fat-soluble substances 2.50
Carbohydrate 1.20
Lactic acid 0.90
Glucose-6-phosphate 0.15
Glycogen 0.10
Glucose, traces of other glycolytic intermediates 0.05
Miscellaneous, soluble non-protein substances 2.30
Nitrogenous: 1.65
Creatinine 0.55
Inosine monophosphate 0.30
Di- and tri-phosphopyridine nucleotides 0.10
Amino acids 0.35
Carnosine, anserine 0.35
Inorganic: 0.65
Total soluble phosphorus 0.20
Potassium 0.35
Sodium 0.05
Magnesium 0.02
Calcium, zinc, trace metals 0.03
Vitamins
Various fat- and water soluble vitamins Minute
This table was published in Lawrie’s Meat Science 6th edition, Lawrie (1998), Page No. 59, Copyright Elsevier (1998)
40
Table 1.2 Average nutrient composition (per 100 g) of the lean component of red meat
Nutrient Beef Veal Lamb Mutton

Moisture (g) 73.1 74.8 72.9 73.2
Protein (g) 23.2 24.8 21.9 21.5
Fat (g) 2.8 1.5 4.7 4.0
Energy (kj) 498 477 546 514
Cholesterol (mg) 50 51 66 66
Thiamin (mg) 0.04 0.06 0.12 0.16
Riboflavin (mg) 0.18 0.20 0.23 0.25
Niacin (mg) 5.0 16.0 5.2 8.0
Vitamin B6 (mg) 0.52 0.8 0.10 0.8
Vitamin B12 (μg) 2.5 1.6 0.96 2.8
Pantothenic acid (mg) 0.35 1.50 0.74 1.33
Vitamin A (μg) < 5 < 5 8.6 7.8
Beta-carotene (μg) 10 < 5 < 5 < 5
Alpha-tocopherol (mg) 0.63 0.50 0.44 0.20
Sodium (mg) 51 51 69 71
Potassium (mg) 363 362 344 365
Calcium (mg) 4.5 6.5 7.2 6.6
Iron (mg) 1.8 1.1 2.0 3.3
Zinc (mg) 4.6 4.2 4.5 3.9
Magnesium (mg) 25 26 28 28
Phosphorus (mg) 215 260 194 290
Copper (mg) 0.12 0.08 0.12 0.22
Selenium (μg) 17 < 10 14 < 10
Adapted from Williams (2007). Nutrition & Dietetics, John Wiley & Sons
(iii) Vitamins (iv) Minerals

The only natural source of vitamin B12 is in Red meat is one of the richest sources of
food derived from animal products. Red meat minerals such as iron or zinc, and has a higher
is a rich source of B vitamins such as B6, B12, mineral bioavailability than plant products
niacin, and thiamine (Gille & Schmid, 2015). For (Williams, 2007). For example, 100 g of lean
example, 100 g of lean beef meat will provide beef meat will provide approximatively 1.8 mg
2.5 µg of vitamin B12, corresponding to 79% of of iron and 4.6 mg of zinc, corresponding to
the recommended dietary intake for this nutrient. approximately 14% and 42%, respectively, of the
The older the animal, the richer its meat will be recommended dietary intake for these nutri-
in B vitamins (Williams, 2007). Pork contains ents (Williams, 2007). Red meat is also a good
a high level of thiamine compared with other source of selenium. For example, 100 g of lean
meats (Bender, 1992). While the concentration of beef meat will provide about 17 µg of selenium,
vitamin E in red meat is low, it is higher in fattier corresponding to approximately 26% of the
cuts of meat. Vitamin A and folate are found at recommended dietary intake for this nutrient
higher levels in liver than in lean muscle meat (Williams, 2007).
(Bender, 1992).
41
(v) Creatine antibiotics (chlorotetracycline and oxytetracy-

Creatine levels in skeletal muscle average cline) is increasingly discouraged and regulated.
350 mg per 100 g of red meat (Purchas & Irradiation is permitted in the USA, but it can
Busboom, 2005; Williams, 2007). Cooking of the induce free radical formation (Isam et al., 2007).
muscle meat transforms creatine into creatinine Freezing of red meat results in little to no loss of
through non-enzymatic conversion. Creatine nutrients, apart from vitamin E, which is oxidized.
and creatinine in meat are critical precursors in Proteins remain unchanged during frozen storage,
the formation of heterocyclic aromatic amines but fats are susceptible to changes from oxidation.
(HAAs) (Skog et al., 1998, 2000). Pork meat, which is richer in unsaturated fatty
acids than other red meats, is the most suscep-
(b) Effect of slaughtering and storage post tible to these changes. Once meat is defrosted, the
mortem juices containing soluble proteins, vitamins, and
Preslaughter handling of the animal can have minerals are lost (Rahman, 2007).
an impact on the composition and quality of the (c) Chemical contaminants and residues
meat. For example, stressed or fatigued animals
have depleted glycogen. Before slaughtering, Residues of drugs (e.g. antibiotics and
animals are usually stunned and then exsanguin- hormones), pesticides, and agricultural chemi-
ated. Blood is drained from the carcass, leading cals can be found in meat and meat products (e.g.
to a loss of oxygen and a depletion of adenosine as a result of exposure of the animals to chemi-
triphosphate, as well as the combination of the cals used on buildings, grazing areas, and crops)
proteins actin and myosin to form actinomyosin (Fig. 1.1; Engel et al., 2015). Additionally, several
to cause muscle contraction. After slaughtering, hundred substances may be used to treat animals,
glycogen is converted to lactic acid, and pH to preserve animal health, and to improve animal
levels fall to approximately 5.5 over a period of production, including antimicrobial agents, anti-
24–36 hours and can have an impact on microbial coccidial agents, anthelmintics, steroids, anti-in-
content (Lawrie, 1998; Lawrie & Ledward, 2006). flammatory agents, tranquillizers, vasodilators,
A major safety concern in meat production analgesics, and anaesthetics (FDA, 2005).
and storage is bacterial contamination. Although (i) Veterinary drugs
muscle is usually sterile, bacterial contamination Veterinary drugs given to animals are strictly
from gastrointestinal contents and butchering regulated in most developed countries (FDA,
instruments is common. Bacterial contamination 2005), and maximum residue limits (MLRs) have
is minimized by low temperatures, low tempera- been established for some of these drugs by the
tures and packaging in a controlled atmosphere. Codex Alimentarius.
Minced and comminuted meats with larger
surface areas may be more likely to become Antibiotics: In the European Union (EU), the
contaminated than large cuts of meat (Lawrie, only antibiotics allowed as feed additives are
1998; Lawrie & Ledward, 2006). Physical and coccidiostats and histomonostats (European
chemical methods, such as spray washing with Commission, 2003), as other antibiotics, espe-
hot water, can be used for microbial decontami- cially if they are also used for humans, could
nation. Water may be chlorinated and combined induce antimicrobial resistance in consumers
with weak organic acids, phosphates, hydrogen (Chattopadhyay, 2014). Cooking procedures
peroxide, or ozone to improve antimicrobial degrade the residues of several antibacterial
activities. Improving hygiene levels by means of drugs, depending on the amount of heat
42
treatment involved, principally cooking time These contaminants, which are mainly
and temperature (Heshmati, 2015). produced by industrial processes, are ubiquitous
Hormones: In several countries, such as in foods of animal origin, and accumulate in the
the USA, the use of hormones, including fatty tissues of animals and humans (Larsen,
testosterone propionate, estradiol, estradiol 2006; IARC, 2012a, 2016). Food, including meat,
benzoate, and progesterone, and compounds remains the primary source of human exposure
that display a high affinity for human hormone to these contaminants in the general population
receptors are approved for food animal (IARC, 2012a, 2016).
production. This raises concerns because (iv) Brominated flame retardants
these hormones, or their biologically active
Brominated flame retardants (BFRs) are
metabolites, may accumulate in edible tissues,
widely used in plastic materials, textiles, electric
potentially exposing consumers (Nachman &
and electronic equipment, and of construction
Smith, 2015). Cooking reduces, but does not
materials for livestock buildings. There are five
eliminate, the potential for dietary exposure
classes of BFRs: polybrominated diphenyl ethers
to hormones, such as estradiol, in ground beef
(PBDEs), hexabromocyclododecanes (HBCDs),
(Braekevelt et al., 2011). Table 1.3 lists the
tetrabromobisphenol A, and other phenols, poly-
amounts of steroid hormones ingested via the
brominated biphenyls (PBBs) (IARC, 2016), and
diet from hormone-treated or non–hormone-
unclassified BFRs (ANSES, 2011, 2012; IARC,
treated animals, and the amounts of these
2016). The persistence of BFRs in the environment
hormones produced daily in the human body.
is a public health concern (AFSSA, 2005; ANSES,
[The Working Group noted that the ingestion
2011; EPA, 2010). The main source of human
of estradiol, progesterone, and testosterone
exposure to BFRs is the consumption of fish and
from meat appears to be minor relative to
meat products (Lyche et al., 2015). Studies have
what is biosynthesized in humans (Table 1.3).]
shown that the cooking process and, to a greater
Environmental and phytosanitary contami- extent, the type of meat item influence levels of
nants can also occur in meat products. PDBEs.
(ii) Pesticide residues (v) Polycyclic aromatic hydrocarbons
Pesticide residues used for phytosanitary Polycyclic aromatic hydrocarbons (PAHs) can
treatments may be present in meat products. be generated in the environment or during the
Animals consume plants treated with pesti- processing of foods; this is discussed further in
cides or contaminated by persistent pesti- Section 1.2.3(a)(iii). PAHs are closely monitored
cides in the environment. However, vegetable by health agencies in developed countries (IARC
consumption remains by far the main dietary 2010a; Schroeder, 2010). Furthermore, PAH levels
source of human exposure to pesticides can increase depending on cooking conditions.
(Kan & Meijer, 2007). (vi) Heavy metals
(iii) Dioxins and dioxin-like products Contamination by heavy metals such as
Dioxins and dioxin-like products are divided cadmium, lead, arsenic, or mercury largely
into three groups: polychlorinated dibenzodi- occurs from industrial wastes (IARC, 2012b).
oxins (PCDDs), polychlorinated dibenzofurans Meat consumption is a significant source
(PCDFs), and polychlorinated biphenyls (PCBs) of human exposure to lead and cadmium
(see Fig. 1.1). (Kan & Meijer, 2007).
43
Table 1.3 Comparison of the amounts of steroid hormones produced daily in the human body
and ingested via the diet from hormone-treated animals
Hormone Total daily production (µg/day) Residue in muscle (µg/kg) (Paris et al., 2006) Ingested amount via
(JECFA, 2000; EFSA, 2007) intake of muscle from
Non-treated animals Treated animals treated animalsa (µg/day)
Estradiol < 14 (prepubertal boys) 0.003–0.035 0.011–0.28 0.0033–0.084

10–24 (prepubertal girls)
27–68 (adult men)
30–470 (adult women)
Progesterone 150–250 (prepubertal children) 0.0–0.9 0.23–0.77 0.069–0.231
416–750 (adult men,
premenopausal women)
Testosterone 30–100 (prepubertal children) 0.006–0.029 0.031–0.36 0.0093–0.108
210–480 (adult female)
2100–6900 (adult male)
Calculated according to an intake of 300 g/day of muscle
a
Reprinted from Jeong et al. (2010) © 2010 The Korean Society of Toxicology. License: CC BY-NC 3.0
(vii) Mycotoxins fat, a wide range of non-meat substances are

Mycotoxins, metabolites produced by used in processed meat products (Bender,
mould, are toxic and may be carcinogenic to 1992; Heinz & Hautzinger, 2007; Toldrá, 2010;
animals and humans. Livestock contamination Weiss et al., 2010).
by mycotoxins occurs via their diet, and human (i) Non-meat ingredients of animal origin
exposure results from consumption of contam- Although not commonly applied, non-meat
inated livestock. However, cereals and oil seeds ingredients of animal origin may be used to
are the main sources of human exposure to improve water binding and prevent fat separa-
mycotoxins (FDA, 2008; Marroquín-Cardona tion during heat treatment. Some of these ingre-
et al., 2014). Mycotoxin residues accumulate dients can also be considered as meat extenders.
in the blood, liver, and kidney, and, to a lesser The most commonly used non-meat ingredients
degree, in muscle-derived meat products (Kan of animal origin are milk caseinate; whole milk
& Meijer, 2007). Mycotoxins, such as afla- or non-fat, dried milk; gelatine; blood plasma;
toxin, are not destroyed by normal industrial eggs; and transglutaminase (Sun & Holley, 2011).
processing or cooking since they are heat-stable
(Awadt et al., 2012). (ii) Ingredients of plant origin
Spices are predominantly functional ingredi-
1.2.2 Processed meat ents, and are used in small quantities to provide
or add flavour and taste to meat products. The
(a) Ingredients most commonly used ingredients of plant origin
There are three major reasons for processing are isolated soy protein (≤ 90% protein) and wheat
meat: reduction in microbial contamination, gluten (≤ 80% protein). The most common ingre-
production of attractive products, and reduc- dients used as fillers (if rich in carbohydrate) or
tion of waste by reconstitution of muscle meat meat extenders (if rich in protein) are soy flour
scraps or offal. Therefore, along with the main or concentrate, cereal flour or cereals, starches,
components, which are meat and animal breadcrumbs, vegetables, and fruits (Asgar et al.,
44
Fig. 1.1 Examples of environmental micropollutants potentially found in red and processed

meats
Cln
Cln
O
Cl O Cl
Clm
Clm
Cl O Cl
2,3,7,8-Tetrachlorodibenzo-p-dioxin Polychlorinated dibenzofuran Polychlorinated biphenyls

(TCDD) (PCDFs) (PCBs)
Cl
Brn Brm
O Cl Cl
Cl Cl
Cl
Polybrominated diphenyl ethers Benzo[a]pyrene Lindane
(PBDEs) (BaP) (pesticide)
Adapted from Meat Science, Volume 109, E. Engel, J. Ratel, J. Bouhlel, C. Planche, M. Meurillon, Novel approaches to improving the chemical
safety of the meat chain towards toxicants, Pages No. 75–85, Copyright (2015), with permission from Elsevier (Engel et al., 2015)
2010). Several plant derivatives can also be used flavour; and food colourings. Chemical additives
as fat replacers, antioxidants, or antimicrobials have exclusively functional properties. They are
(Hygreeva et al., 2014). used in small amounts, usually below 1%, with
nitrate as low as 0.05% and with only salt in the
(iii) Chemical substances used as additives
range of 2% (≤ 4% in some fermented dried prod-
There are a limited number of chemical ucts) (Heinz & Hautzinger, 2007).
substances allowed for meat processing, as the
substances need to be safe for consumers and (b) Processing methods
improve the quality of the final product. The most Standard technical processing methods for
commonly used substances are salt (NaCl or NaCl meat products, such as cutting, comminuting,
plus KCl) for taste, impact on meat proteins, and mixing, tumbling, or stuffing, are an important
shelf-life; nitrate and nitrite for curing, colour, part of the manufacturing process (Heinz &
flavour, and shelf-life; ascorbic acid for acceler- Hautzinger, 2007). However, as these processes
ated curing; phosphates for protein structuring do not influence the formation of potentially
and water binding; chemical preservatives for carcinogenic process-induced toxicants, they
shelf-life; antioxidants for flavour and shelf-life; will not be further detailed in this section.
monosodium glutamate for enhancement of
45
Microbial inactivation can be achieved by to form dehydroascorbate, and thus prevents the
“sous vide”, a method whereby foods are vacu- oxidation of nitrite to nitrate. Ascorbate is also
um-packaged and then slow-cooked (tempera- added to reduce the formation of nitrosamines.
ture, 55–60 °C), as well as by cooking, canning Ascorbate, together with nitrite and salt, has an
(temperature, up to 121 °C), irradiation (chilled effective antimicrobial effect, particularly against
temperature, 0–4 °C), and high-pressure Clostridium botulinum (Honikel, 2010; Sindelar
processing (300–600 MPa). Microbial inactiva- & Milkowski, 2012). Citric acid or sodium citrate
tion can also be achieved by the addition of arti- may replace up to half of either form of the ascor-
ficial preservatives such as nitrate or nitrite, weak bate/erythorbate reductants, but may not be used
organic acids, and/or salt or sugar. Canning is without the reductants (Sindelar et al., 2010).
probably the most efficient meat preservation Nitrite addition is strictly regulated by inter-
method, as it ensures the destruction of path- national standards, and the amount allowed in
ogens and food spoilage microorganisms, and cured meat is decreasing (see Section 1.5).
allows foods to be easily handled and trans- (ii) Smoking
ported (Guerrero Legarreta, 2010).
The most common approaches to retard lipid Smoking refers to the exposure of meat
oxidation, a major limiting factor in the shelf- to the smoke of burning wood (Sikorski &
life of dehydrated muscle tissue, is the addition Kalakowski, 2010). Many cured products are
of antioxidants and the use of appropriate pack- also smoked, or contain soluble components of
aging techniques (Rahman, 2007). wood smoke, mainly to add flavour and increase
Chemical processing methods essentially shelf-life. Smoking gives meat a brown colour.
include curing, smoking, and fermentation. It changes its flavour and improves its pres-
ervation, as smoke contains a wide variety of
(i) Curing polyphenolic compounds as well as aldehydes
Meat curing, in the narrow sense, is the and carboxylic acids, which have antimicrobial
addition of salt (NaCl or NaCl plus KCl), with properties. Smoking can be done at different
or without nitrate or nitrite, during the manu- temperatures, depending on the end product
facturing of meat products. Nitrate and nitrite (Sikorski & Kalakowski, 2010). However, wood
are not used as sole curing agents. Each is always pyrolysis may be hazardous, as the process is
applied with salt. In meat products, the concentra- difficult to control and can lead to the gener-
tions of nitrate and nitrite are usually in the range ation of PAHs. Modifications to traditional
of 100–200 mg/kg, while salt is 2000 mg/kg or wood pyrolysis processes are being studied to
more. Salt lowers the water activity and enhances reduce the production and deposition of PAHs
food safety. Salt also changes the protein struc- in processed meat (Roseiro et al., 2011; Ledesma
tures in meat. Nitrate and nitrite support the et al., 2014). An alternative is to use liquid smoke
safety action of salt, and improve the appearance flavouring solutions produced from different
and flavour. Nitrate must undergo reduction to wood products, under specific pyrolysis condi-
nitrite to be effective. During the curing process, tions and as per extraction protocols aimed at
myoglobin is converted to nitrosomyoglobin, strongly reducing the concentration of PAHs
resulting in the characteristic cured meat colour (Sikorski & Kalakowski, 2010).
(EFSA, 2003; Honikel, 2008, 2010). Over the past
few decades, ascorbic acid or its salt, ascorbate
(e.g. isoascorbate or erythorbate), has been used in
cured meat batters. Ascorbate reacts with oxygen
46
(iii) Fermentation of fat. The method has an impact on the forma-

Fermentation refers to a low-energy, biolog- tion of carcinogenic compounds such as HAAs
ical acidulation (by cultured or wild microor- or PAHs (Skog et al., 1998; Giri et al., 2015). At
ganisms) and preservation method that results low temperatures (around 100 °C), steaming,
in a distinctive flavour and palatability, colour, boiling, or stewing generate much lower levels of
and tenderness, as well as in enhanced micro- these carcinogenic compounds. For baking and
biological safety. Since this process involves roasting, temperatures are higher (up to 200 °C),
microorganisms, it is influenced by many envi- but as there is limited direct contact with a hot
ronmental factors, including raw meat quality, surface, the formation of these carcinogenic
sanitation, time, temperature, and humidity, all compounds is also low (Rohrmann et al., 2002).
of which need to be strictly controlled during Barbecuing, grilling, and pan-frying expose
production. The reduction of pH and the lowering meat products to high temperatures, and to
of water activity are microbial hurdles that aid a hot surface or to direct flame, and thus can
in producing a safe product. Both natural and produce an appreciable level of these carcino-
controlled fermentation processes involve lactic genic compounds (American Institute for Cancer
acid bacteria. Fermented sausages often have a Research/World Cancer Research Fund, 1997;
long storage life, due to added salt, nitrate, and/or Sinha et al., 1998a, b).
nitrite, and a low pH, due to lactic acid produc-
(a) Red meat
tion by bacteria in the early stages of storage and
later stages of drying (Ockermann & Basu, 2010). This part of the section focuses on the toxi-
cants found in red meat that are mostly produced
1.2.3 Changes in meat composition due to by certain heating and cooking conditions.
cooking methods (i) N-Nitroso compounds
Cooking can have a positive and negative N-Nitroso compounds (NOCs) are mainly
impact on food quality. Cooking is important formed endogenously in human organisms. No
to inactivate pathogenic microorganisms, and data report their formation in red meat during
improve palatability and digestibility (Santé- heat treatment; they are mainly considered
Lhoutellier et al., 2008; Bax et al., 2012, 2013). processed meat toxicants (see Section 1.2.3(b)(i)).
Generally, cooking reduces, but does not (ii) Heterocyclic aromatic amines
eliminate, meat contaminants such as hormones, HAAs are a family of heat-induced food toxi-
antibiotics, chemicals (e.g. PCBs, PCDFs, and cants that were discovered about 30 years ago by
PCDDs), or metals (e.g. arsenic, cadmium, Professor Sugimura. Currently, about 25 HAAs
mercury, and lead) (Hori et al., 2005; Perelló have been identified in cooked meat, fish, and
et al., 2008; Perelló et al., 2010; Braekevelt et al., poultry products (Sugimura et al., 2004), as well
2011; Zeitoun & Ahmed, 2011; Heshmati, 2015). as in cigarette smoke and diesel exhaust (Manabe
Furthermore, cooking can lead to the production et al., 1991). HAAs can be divided into two distinct
of potential carcinogens. families: aminoimidazoazaarenes and carbo-
The different cooking methods used to lines or pyrolytic HAAs (Fig. 1.2 and Table 1.5).
prepare red and processed meat may have Aminoimidazoazaarenes are formed by Maillard
varying influences on the production of potential reaction (a chemical reaction between amino
carcinogens (Table 1.4). Cooking methods differ acids, creatine/creatinine, and sugars), whereas
based on cooking temperature, direct or indirect carbolines and pyrolytic HAAs are formed at
contact with the heating source (flame), and use
47
Table 1.4 Definition of cooking methodsa
Cooking methodb Definition

Baked Cooked by dry heat in an oven, covered or uncovered, no additional fat used for cooking
Barbecued Cooked on grill bars over burning charcoal, wood or gas
Battered and baked Covered by batter (flour, milk, and egg mixture) and baked
Battered and fried Covered by batter (flour, milk, and egg mixture) and fried
Boiled Cooked in boiling liquid
Breaded and baked Covered by an outer layer of breadcrumbs and baked
Breaded and fried Covered by an outer layer of breadcrumbs and fried
Breaded and griddled Covered by an outer layer of breadcrumbs and griddled
Coated and fried Covered by an outer layer and fried: includes battered and fried, breaded and fried, in flour and fried
Deep fried Cooked in hot fat or oil by immersing the food entirely
Fried Generic descriptor for cooked in heated fat, usually over a direct source of heat
Griddled Cooked on a heated flat metal surface over a source of direct heat; a little fat or oil may be used to
grease the metal surface
Grilled Cooked rapidly without moisture, on grill bars under or over intense direct heat, no fat used
In flour and fried Covered by an outer layer of flour and fried
Microwaved Cooked or reheated in a microwave oven; no fat used
Poached Cooked by dropping in boiling liquid
Reheated Made hot; no liquid nor fat is added
Roasted Cooked by dry heat in an oven or over a fire
Shallow fried Cooked in a shallow layer of heated fat
Steamed Cooked by steam, in pressure cooker or cooked suspended above boiling water
Stewed Cooked by boiling or simmering in liquid contained in an enclosed vessel; the food is cooked over a
low heat for a long period of time
Stir fried/sautéed Cooked by frying food over high heat, by stirring constantly to avoid sticking
Toasted Cooked with direct heat until the surface of the food is browned
a Definitions based on the EPIC Study, Rohrmann et al. (2002)
b Cooking method is defined as the preparation of meat items just before consumption
Adapted by permission from Macmillan Publishers Ltd: Rohrmann et al. (2002). Cooking of meat and fish in Europe--results from the
European Prospective Investigation into Cancer and Nutrition (EPIC). European Journal of Clinical Nutrition, Volume 56, issue 12, pages
1216–1230, copyright (2002)
elevated temperatures (Murkovic, 2004). The meats are given in Table 1.6. The concentrations
main source of human exposure to HAAs is via of HAAs are highly variable. For a comprehen-
cooked proteinaceous foods; however, the levels sive review, see Alaejos & Afonso (2011). A series
of HAAs are highly dependent on the type of of linear tricyclic ring HAAs containing the
meat, cooking time, and cooking temperature, 2-amino-1-methylimidazo[4,5-g]quinoxaline
and generally increase with the level of “done- (IgQx) skeleton are formed in cooked meats at
ness” (Skog et al., 2000). concentrations that are relatively high compared
The cooking method also influences HAA with the concentrations of their angular tricyclic
formation; it has been shown that high-temper- ring isomers or related HAAs (Ni et al., 2008),
ature methods (pan-frying, grilling, and barbe- such as 2-amino-3,8-dimethylimidazo[4,5-f]
cuing) cause the highest HAA concentrations, quinoxaline (MeIQx) and PhIP, which are known
especially for 2-amino-1-methyl-6-phenylimida- experimental animal carcinogens and potential
zo[4,5-b]pyridine (PhIP) (Alaejos & Afonso, 2011). human carcinogens (IARC, 1993). The toxicolog-
The concentrations of HAAs in different cooked ical properties of these recently discovered IgQx
48
Fig. 1.2 Structures of heterocyclic aromatic amines found in cooked red and/or processed meats
Principal aminoimidazoazaarenes found in red and processed meats
NH 2 NH 2
N N
CH 3
N R3 N N CH 3
CH 3 N
NH 2
N R R2 N R1 N N
R = H (IQ) R 1 , R 2 = H, R 3 = Me (8-MeIQx) PhIP
R = Me (MeIQ) R 1 , R 3 = Me, R 2 = H (4,8-DiMeIQx)
Principal pyrolytic HAAs found in red and processed meats
H3C H3C
N N
NH 2 NH 2
N N
CH 3 N N CH 3 N
N
H H H H
Harman Norharman Trp-P-1 Trp-P-2
NH 2 CH 3
N
N N N NH 2
H H
AC MeAC
The full chemical names of these compounds are given in Table 1.5
HAA, heterocyclic aromatic amines
Reprinted from Cancer Science, Volume 95, Takashi Sugimura, Keiji Wakabayashi, Hitoshi Nakagama, Minako Nagao, Heterocyclic amines:
Mutagens/carcinogens produced during cooking of meat and fish, Pages No. 290–299, Copyright (2004), with permission from John Wiley & Sons
(Sugimura et al., 2004)
derivatives warrant further investigation and moiety in the limitation of HAA formation – via
assessment. their scavenging capacity for reactive radicals
Some methods to decrease the levels of involved in the HAA mechanism of formation
HAAs in cooked meats have been described. For (Balogh et al., 2000; Vitaglione & Fogliano, 2004;
example, microwave pretreatment followed by Gibis & Weiss, 2010, 2012). Other compounds,
disposal of the resulting liquid before frying of such as organosulfur compounds, contained
hamburger patties reduces the formation of some in garlic or onion, have also been shown to
aminoimidazoazaarenes (Felton et al., 1992). have an inhibitory effect on HAA formation
Various studies have also emphasized the role of (Shin et al., 2002).
added antioxidants with phenolic or polyphenolic
49
Table 1.5 Chemical names of heterocyclic aromatic amines potentially found in cooked red and
processed meats
Common abbreviation Full name

IQ 2-amino-3-methylimidazo[4,5-f ]quinoline
MeIQ 2-amino-3,4-dimethylimidazo[4,5-f ]quinoline
IQx 2-amino-3-methylimidazo[4,5-f ]quinoxaline
MeIQx 2-amino-3,8-dimethylimidazo[4,5-f ]quinoxaline
4,8-DiMeIQx 2-amino-3,4,8-trimethylimidazo[4,5-f ]quinoxaline
7,8-DiMeIQx 2-amino-3,7,8-trimethylimidazo[4,5-f ]quinoxaline
4-CH2OH-8-MeIQx 2-amino-4-hydroxymethyl-3,8-dimethylimidazo[4,5-f ]quinoxaline
PhIP 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine
4′-hydroxy-PhIP 2-amino-6-(4-hydroxyphenyl)-1-methylimidazo[4,5-b] pyridine
Trp-P-1 3-amino-1,4-dimethyl-5H-pyrido[4,3-b]indole
Trp-P-2 3-amino-1-methyl-5H-pyrido[4,3-b]indole
AαC 2-amino-9H-pyrido[2,3-b]indole
MeAαC 2-amino-3-methyl-9H-pyrido[2,3-b]indole
Glu-P-1 2-amino-6-methyldipyrido[1,2-a:3′2′-d]imidazole
Glu-P-2 2-aminodipyridol[1,2-a:3′2′-d]imidazole
Harman 1-methyl-9H-pyrido[3,4-b]indole
Norharman 9H-pyrido[3,4-b]indole
IgQx 2-amino-1-methylimidazo[4,5-g]quinoxaline
Note: the chemical structure of some of these compounds is given in Fig. 1.2
Adapted with permission from Sugimura et al. (2004) and Alaejos & Afonso (2011)
(iii) Polycyclic aromatic hydrocarbons produced. This may be related to the pyrolysis
The main source of non-occupational human of fat, which drips onto the heat source (Mottier
exposure, for non-smoking individuals, is food et al., 2000).
consumption (Kazerouni et al., 2001). PAHs Heat treatment of red and processed meat can
can be formed by pyrolysis of organic materials, also produce other toxicants, such as acrylamide
direct contact of fat with a flame, or incomplete (Tareke et al., 2002) and N-methylacrylamide
combustion of charcoal, so they are present in (Yaylayan et al., 2004).
grilled meats (Chen & Lin, 1997; Alomirah (iv) Iron
et al., 2011). More than 30 PAHs have been iden- Iron is a trace element essential for human
tified; among them is benzo[a]pyrene (BaP), health that can be found in foods of animal and
which is classified as a Group 1 human carcin- plant origin. In food, iron can be found in two
ogen (IARC, 2012a). The main PAHs found in forms: haem iron and non-haem iron. Haem iron,
processed meats are presented in Fig. 1.3 and which is more bioavailable than non-haem iron,
Table 1.7. Representative concentrations of PAHs is only found in animal products (Schonfeldt &
in different processed meat samples are given in Hall, 2011). Haem iron is contained in myoglobin
Table 1.8. and haemoglobin, whereas non-haem iron is
By avoiding the direct contact of meat with associated with small molecules such as phos-
a flame, PAH levels can be lowered. The amount phate, ascorbate, or free amino acids to form
of fat can also influence PAH levels. The more salts. The amount of iron in meat, and the ratio
fat that is contained in meat, the more PAHs are between haem and non-haem iron, depends on
50
Table 1.6 Concentrations of heterocyclic aromatic amines in different cooked meats
Cooked meat Concentrations of HAAs (ng/g)

IQ MeIQ 8-MeIQx 4,8-DiMeIQx PhIP Trp-P-1 Trp-P-2 Harman Norharman AαC
Minced beef ND–12 ND–8 ND–7 ND–3 ND–34 ND to ND–2 ND–28 ND–30 ND–21
(fried, grilled, < 1.45
and barbecued)
Beef (roasted ND to ND to ND–17.5 ND–3.4 ND–32.4 ND–0.01 ND ND–240a ND–205b ND–0.11
and oven- < 0.2 < 0.2
broiled)
Beef extract ND–75 ND–10 ND–38 ND–6 ND–10 ND–13 ND–14 NQ–377 NQ–94 NQ to < 8.1
(products
commercially
cooked)
Lamb (grilled < 0.1 < 0.1 ND–3 ND–2 ND–11b ND–1 < 0.3 ND–7 ND–9 ND–0.5
and fried)
Pork (grilled ND–7 ND–11 ND–21 ND–28 ND–32 ND–1 ND–5 ND–25a ND–51a ND–3
and fried)
Sausage (fried, ND–5 ND–2 ND–5 ND–3 ND–6 ND–1 ND–2 ND–3 ND–10 <0.03
roasted, and
barbecued)
Bacon (fried) ND–11 ND–2 ND–27 ND–9 ND–106b 0.6 < 0.29 ND–33 ND–60 NQ to < 0.5
Pan scrapings < 2 29–63 4–15 83–144 3–77
from different
meats
a The highest levels of harman and norharman were found in commercially roasted beef (Khan et al., 2008)
b A study in the Republic of Korea reported very high concentrations of PhIP (258 ng/g), harman (990 ng/g), and norharman (413 ng/g) in griddled pork loin, and of PhIP (168 ng/g) in
griddled bacon (Back et al., 2009)

4,8-DiMeIQx, 2-amino-3,4,8-trimethylimidazo[4,5-f ]quinoxaline; 8-MeIQx, 2-amino-3,8-dimethylimidazo[4,5-f ]quinoxaline; AɑC, 2-amino-9H-pyrido[2,3-b]indole; HAA,
heterocyclic aromatic amines; harman, 1-methyl-9H-pyrido[3,4-b]indole; IQ, 2-amino-3-methylimidazo[4,5-f ]quinoline; MeIQ, 2-amino-3,4-dimethylimidazo[4,5-f ]quinoline; ND,
not detected; norharman, 9H-pyrido[3,4-b]indole; NQ, not quantified; PhIP, 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine; Trp-P-1, 3-amino-1,4-dimethyl-5H-pyrido[4,3-b]
indole; Trp-P-2, 3-amino-1-methyl-5H-pyrido[4,3-b]indole
Table compiled using data from the review of Alaejos & Afonso (2011), indicating the lowest and highest values found for the different HAAs in different heat-processed meats
51
Fig. 1.3 Structures of polycyclic aromatic hydrocarbons found in red and/or processed meats
Benzo[a]pyrene Chrysene Benz[a]anthracene Benzo[b]fluoranthene
the species and the type of muscle (Lombardi- protein and lipid content show the highest
Boccia et al., 2002; Table 1.9). Red meat contains AGEP levels, probably due to the large quan-
more total iron and haem iron than white meat. tity of free radicals released via the various
Beef, lamb, and horse meat are richer in haem lipid peroxidation reactions that catalyse the
iron and total iron than pork meat. The age of the formation of AGEPs during the cooking of
animal is also important in iron intake, as older meat products. AGEP formation depends on
animals contain more iron. During cooking, temperature, method, and duration of heating.
part of haem iron is converted to non-haem The higher the cooking temperature, the more
iron, depending on the cooking parameters, AGEPs are formed in red and processed meat.
such as time and temperature (Lombardi- Different studies have shown that oven-frying
Boccia et al., 2002; Purchas & Busboom, 2005; produces more AGEPs than deep-frying, and
Purchas et al., 2006). broiling produces more AGEPs than roasting.
(v) Advanced glycation end products Boiling produces less AGEPs (Goldberg et al.,
2004; Chen & Smith, 2015). Cooking duration
Advanced glycation end products (AGEPs) are seems to be less important than the temperature
heat-induced food toxicants, which are protein- and method, as shown in Table 1.10.
bound Maillard reaction products. AGEPs consti-
tute a group of heterogeneous moieties produced (vi) N-Glycolylneuraminic acid
endogenously from the non-enzymatic glycation Sialic acids are a family of sugars with a
of proteins, lipids, and nucleic acids (Krause et al., nine-carbon sugar acid. N-Glycolylneuraminic
2003; Goldberg et al., 2004). They are present in acid (Neu5Gc) (Fig. 1.4) is one of the most
several heated foods, such as canned foods and common sialic acids and is found in almost all
meat products (Goldberg et al., 2004; Uribarri mammals. Humans are genetically deficient in
et al., 2010). The formation of AGEPs is part of Neu5Gc production and instead metabolically
the normal metabolism, but if their levels are very accumulate it from dietary sources, particu-
high in tissues and in the circulation, they can larly red meat and milk products. However,
become pathogenic. Carboxymethyllysine is one metabolically accumulated dietary Neu5Gc
of the best-characterized AGEP compounds, and results in the production of circulating anti-
is frequently used as a marker of AGEP forma- Neu5Gc antibodies, leading to chronic local
tion in food. In meat products, carboxymethyl- inflammation (Hedlund et al., 2008). It has been
lysine ranges from 0.01 to 6.87 mg per 100 g of shown that the amount of Neu5Gc is high in red
food (mean, 0.86), and in meat dishes, it ranges meats compared with other dietary sources, with
from 0.10 to 42.39 mg per 100 g of food (mean, beef being the most Neu5Gc-enriched compared
2.42) (Hull et al., 2012). AGEP levels depend on with other red meats (Tangvoranuntakul et al.,
red meat composition (Goldberg et al., 2004; 2003; Samraj et al., 2015; Table 1.11).
Chen & Smith, 2015). Indeed, foods high in
52
Fig. 1.4 Structure of N-glycolylneuraminic representative processed meats are given in

acid (Neu5Gc) Table 1.13.
HO A recent study detected N-nitrosamines
O in dry fermented sausages; only NPIP and
HO N-nitrosomorpholine (NMOR) were detected
O OH in a high number of samples (n = 101; 22% and
O 28%, respectively). When N-nitrosamines were
N OH detected, their total amount remained below
H H 5.5 µg/kg, with only one exception at 14 µg/kg
OH
HO (De Mey et al., 2014).
The addition of sodium ascorbate to meat,
OH
and to a lesser extent NaCl, was shown to
decrease N-nitrosamine levels (e.g. NDMA and
NDEA) in processed meat. On the contrary,
(b) Processed meat baking processes increased N-nitrosamine
levels (Rywotycki, 2007). [The Working Group
Processed meat can contain additional toxi- noted that since the levels of nitrate and nitrite
cants, apart from the heat toxicants described allowed in cured products are being lowered in
for red meat. The addition of nitrate and nitrite many countries, a decrease in NOC formation is
generates NOCs, and smoking can generate expected compared with previous decades.]
PAHs.
(ii) Polycyclic aromatic hydrocarbons
(i) N-Nitroso compounds
Traditional commercial smoking techniques,
Processed meat products can be contami- in which smoke from incomplete wood burning
nated with NOCs such as N-nitrosamines, which comes into direct contact with the product,
result from the reaction between a nitrosating can lead to significant contamination by PAHs
agent, originating from nitrite or smoke, and a if the process is not adequately monitored.
secondary amine, derived from protein and lipid Temperature, time, humidity, type of smoke
degradation (Preussmann & Stewart, 1984; De used, and even the design of the smokehouse are
Mey et al., 2015). N-Nitrosamine production is crucial parameters in controlling PAH formation
dependent on reaction conditions (e.g. low pH (EFSA, 2008; Roseiro et al., 2011). The concentra-
and high temperature), and on meat composition tions of selected PAHs in different smoked meats
and processing (e.g. ageing, ripening, fermen- are given in Table 1.8.
tation, smoking, heat treatment, and storage) PAHs have also been found in dry fermented
(Stadler & Lineback, 2009; Sindelar &Milkowski, sausages in Portugal. The concentrations
2012; De Mey et al., 2015). NOCs can also be of chrysene, benzo[a]anthracene, BaP, and
formed endogenously after consumption of red benzo[a]fluoranthene were 5.1–38.11, 8–32.9,
or processed meat (Santarelli et al., 2008). 1.2–6.6, and 0.63–7.4 µg/kg dry matter, respec-
The most commonly found N-nitrosamines tively (Roseiro et al., 2011).
in processed meat are N-nitrosodimethylamine The use of liquid smoke flavouring might
(NDMA), N-nitrosodiethylamine (NDEA), reduce PAH levels in commercially smoked meat
N-nitrosopiperidine (NPIP), and N-nitroso products (EFSA, 2008).
pyrrolidine (NPYR) (Fig. 1.5; Table 1.12). The
concentrations of some of these NOCs in
53
Fig. 1.5 Structures of N-nitroso compounds commonly found in processed meats
N O
N O N N
N N N O
H3C N H3C
CH 3 H3C O
NDMA NDEA NPIP NPYR
The full chemical names of these compounds are given in Table 1.12
1.3 Exposure via food intake (a) Per capita consumption from economic
surveys
1.3.1 Data description
The per capita consumption is calculated
Consumption for a given food depends on as follows: national production figures plus
two parameters: size of the portion and frequency imports, minus exports, divided by the total
of eating. In addition, the overall dietary pattern number of individuals in the population. The
is based on types of foods consumed, which average values are collected by the Food and
depends on socioeconomic factors (e.g. age, Agriculture Organization of the United Nations
ethnicity, geographical origin, religion, level Statistical Databases (FAOSTAT) (FAO, 2015)
of education, and income). As a result of these on a yearly basis, and may provide a superior
difficulties, food consumption can be estimated estimate of long-term consumption. However,
using two different techniques: per capita studies the per capita data underestimate the true
and individual surveys, which can, respectively, consumption of food items, as less than 100%
underestimate or overestimate long-term dietary of the population are consumers, and the whole
exposures. population is used to calculate the data. On the
Food consumption results can also be gener- contrary, for food items consumed by 100% of
ated using household budget surveys, which the population, the data correctly account for
correspond to per capita estimates at the house- both the amount consumed and the frequency
hold level. However, as the data for household of consumption. Based on the FAO per capita
budget surveys are weak, they will not be further data, the World Health Organization (WHO)
considered in this Monograph. generated the Global Environment Monitoring
In epidemiological studies, food frequency System (GEMS) cluster diets (WHO, 2015a)
questionnaires (FFQs) are typically used for using a mathematical technique to group coun-
ranking subjects according to food or nutrient tries with similar dietary patterns (Sy et al.,
intake, rather than for estimating absolute levels 2013). Consumption values were calculated for
of intake (Beaton, 1994; Kushi, 1994; Sempos each cluster as the average consumption of the
et al., 1999). These questionnaires are further food commodity in each country of the cluster.
discussed in Section 1.4.1. The range of values was therefore narrower than
those for FAO national per capita consumption.
54
Table 1.7 Polycyclic aromatic hydrocarbons cited in this Monograph
Common name (name used in this volume) CAS registry No.

Benz[a]anthracene 56-55-3
Benzo[b]fluoranthene 205-99-2
Benzo[j]fluoranthene 205-82-3
Benzo[k]fluoranthene 207-08-9
Benzo[c]fluorene 205-12-9
Benzo[ghi]perylene 191-24-2
Benzo[a]pyrene 50-32-8
Chrysene 218-01-9
Cyclopenta[cd]pyrene 27208-37-3
Dibenz[a,h]anthracene 53-70-3
Indeno[1,2,3-cd]pyrene 193-39-5
Dibenzo[a,e]pyrene 192-65-4
Dibenzo[a,h]pyrene 189-64-0
Dibenzo[a,i]pyrene 189-55-9
Dibenzo[a,l]pyrene 191-30-0
Indeno[1,2,3-cd]pyrene 193-39-5
5-Methylchrysene 3697-24-3
Note: the chemical structure of some of these compounds is given in Fig. 1.3
(b) Individual food consumption data of meat (i.e. Asia, 86 g/day; Africa, 51 g/day)
Individual food consumption data are gener- (FAO, 2015).
ated from surveys based on recall or recording of In the European Prospective Investigation
daily consumption over 1–7 days. This method into Cancer and Nutrition (EPIC) study,
allows the distribution of consumption across surveys not representative of the national popu-
a population and the consumption of high lation were conducted in 10 European coun-
consumers to be estimated. The method over- tries. Food consumption was estimated based
estimates long-term consumption by extrapo- on one 24-hour dietary recall (Linseisen et al.,
lating data collected over a short period of time 2002). This study concluded that for total meat,
(Tran et al., 2004; IPCS, 2009). the lowest mean consumption in Europe was
observed in Greece (47 g/day for women and 79
g/day for men), and the highest mean consump-
1.3.2 Results tion was observed in Spain (124 g/day for women
(a) Total meat consumption and 234 g/day for men) (Linseisen et al., 2002).
According to FAOSTAT, from 2003 to 2011,
For total per capita meat consumption meat consumption increased in all regions,
worldwide in 2011, important differences were but most significantly in Asia (16%) and in
observed between regions consuming high Africa (20%). These figures were for both red
quantities of meat (i.e. Oceania, 318 g/day; and poultry meats, and for both processed and
north America, 315 g/day; south America, 215 unprocessed meats (FAO, 2015).
g/day; Europe, 208 g/day; central America, 148
g/day) and regions consuming low quantities
55
Table 1.8 Concentration levels (μg/kg) of selected polycyclic aromatic hydrocarbon in samples of
white, red, and processed meat
PAH Cooking/ Beef Pork Chicken

processing method
Range Mean Range Mean Range Mean
Benzo[k]fluoranthene (BkF) Smoked 1.03–3.35 2.57 0.65–4.69 2.96 1.13–4.01 3.54
Grilled 0.35–2.04 1.87 0.22–3.56 1.37 < 0.10–1.95 1.29
Boiled < 0.10–1.81 1.09 0.36–1.45 1.01 0.12–1.54 1.19
Unprocessed ND ND ND ND ND ND
Benzo[a]pyrene (BaP) Smoked < 0.10–5.43 5.34 0.50–10.02 1.28 < 0.10–5.91 2.91
Grilled 0.17–2.93 2.74 0.21–5.73 1.75 0.48–3.73 1.82
Boiled 0.27–1.30 0.87 0.17–1.45 0.94 < 0.10–1.66 0.99
Unprocessed 1.71–2.42 0.34 ND ND ND ND
Indeno[123-cd]pyrene (IP) Smoked 1.82–27.59 5.10 8.81–31.11 5.29 1.40–7.17 1.39
Grilled 1.34–8.48 0.62 1.65–8.59 4.01 1.07–3.42 0.61
Boiled 0.41–1.22 0.54 0.54–1.81 0.97 0.34–1.19 0.45
Unprocessed 1.32–7.86 3.16 0.27–3.06 1.73 0.21–1.08 0.45
Benzo[ghi]perylene (BghiP) Smoked < 0.30–2.55 1.42 < 0.30–3.18 1.09 0.88–3.41 2.68
Grilled 0.61–1.64 1.50 0.78–2.66 1.84 < 0.30–2.56 1.34
Boiled 0.36–1.19 0.82 < 0.30–1.62 0.93 < 0.30–1.87 1.12
Unprocessed ND ND ND ND ND ND
Adapted from Food chemistry, Volume 156, Olatunji et al. (2014). Determination of polycyclic aromatic hydrocarbons [PAHs] in processed meat
products using gas chromatography – Flame ionization detector, Pages No. 296–300, Copyright (2014), with permission from Elsevier
(b) Association between consumption of red principal component analysis for food clustering
meat and consumption of other foods (Zetlaoui et al., 2011). Based on this approach,
Food categories are not independent in regard and its application in the FAO per capita data
to consumption. In the field of nutrition, nutrient set (i.e. 415 food products in 179 countries), 30
intake is estimated by combining consump- consumption systems leading to 17 cluster diets
tion data with food nutrient composition data- have been described (Sy et al., 2013). According
bases. Thereafter, homogeneous subgroups of to this publication, the consumption of pork
consumers with comparable nutrient intakes meat seemed to be associated with the consump-
(dietary patterns) are identified by using clas- tion of barley beer, poultry meat, wheat flour, and
sical statistical clustering techniques (Pryer et al., refined sugar. The consumption of cattle meat
2001; Hu, 2002). The association between food seemed to be associated with cow milk and wheat
categories can also be observed by using prin- flour (Sy et al., 2013).
cipal component analysis. For example, intake (c) Red meat consumption
of processed meat was associated with intake
of French fries, sweets, cakes, desserts, snacks, According to FAOSTAT in 2011, the cumu-
and alcoholic beverages (Fung et al., 2003; Dixon lated mean per capita consumption of beef,
et al., 2004; Kesse et al., 2006). mutton, goat, and pig meat was 30, 60, 130, 140,
Whereas clustering is based on nutrient and 200 g/day, respectively, for Africa, Asia,
intake, it is very difficult to a posteriori identify America, Europe, and Oceania (FAO, 2015).
foods that contribute by a majority to a given From the WHO/GEMS clusters, the average
dietary pattern. Zetlaoui et al. proposed the use of
56
Table 1.9 Total iron and percentage of haem iron in raw and cooked meat
Meats Total iron (mg/100 g) % Haem iron % Loss

Raw Cooked Raw Cooked
Red meat
Beef
Sirloin 2.07 3.59 83 74 11
Fillet 2.35 3.38 90 85 6
Roasted beef 2.04 3.74 87 84 3
Topside 1.93 2.88 87 66 24
Mean 2.09 3.39 87 78 11
Veal
Fillet 0.85 1.58 84 83 1
Lamb
Chop 2.23 3.20 75 70 7
Horse
Fillet 2.21 3.03 79 71 11
Pork
Loin 0.36 0.46 56 46 18
Chump chop 0.49 0.79 66 69 (+4)
Mean 0.42 0.64 62 61 7
White meat
Chicken
Breast 0.40 0.58 30 28 7
Leg (thigh) 0.70 1.34 30 22 27
Leg (lower part) 0.63 1.20 46 35 24
Wing 0.63 0.92 44 25 43
Mean 0.59 1.01 38 28 28
Turkey
Breast 0.50 0.79 28 27 4
Leg (thigh) 0.99 1.46 50 39 22
Leg (lower part) 0.88 1.51 49 38 22
Mean 0.79 1.25 42 35 18
Adapted from Lombardi-Boccia et al. (2002)
total red meat consumption ranged from 15 to of red meat worldwide ranged from 23 g/day
147 g/day (WHO, 2013). (2.6–28 g/day) for the first quintile to 84 g/day
In a systematic assessment, the Global Burden (71–138 g/day) for the fifth quintile (Imamura
of Diseases Nutrition and Chronic Diseases et al., 2015).
Expert Group (NutriCoDE) evaluated the global Individual food consumption surveys provide
consumption of key dietary items (foods and the distribution of consumption for consumers
nutrients) by region, nation, age, and sex in 1990 only (i.e. high percentiles of consumption as well
and 2010 (Imamura et al., 2015). Consumption as percentages of consumers by country) (FAO/
data were evaluated from 325 surveys (71.7% WHO, 2015; FCID, 2015). Worldwide detailed data
nationally representative) covering 88.7% of on red meat consumption (g/kg bw per day) are
the global adult population. According to the presented in Table 1.14 and Table 1.15 for adults
analysis, the median of mean consumption and children, respectively.
57
Table 1.10 Advanced glycation end product content in red meat, processed meat, and chickena
Meat Cooking/processing method Advanced glycation end product (kU/110 g)
Beef Raw 707

Roast 6 071
Steak, raw 800
Steak, broiled 7 479
Steak, grilled 4 min 7 416
Steak, microwaved, 6 min 2 687
Steak, pan fried w/olive oil 10 058
Steak, strips, 450°F, 15 min 6 851
Steak, strips, stir fried with 1 T canola oil, 15 min 9 522
Steak, strips, stir fried without oil, 7 min 6 973
Stewed 2 443
Frankfurter, boiled in water, 212° F, 7 min 7 484
Frankfurter, broiled 450°F, 5 min 11 270
Ground, 20% fat, pan/cover 5 527
Hamburger patty, olive oil 180°F, 6 min 2 639
Meatball, potted (cooked in liquid), 1 h 4 300
Meatball, w/sauce 2 852
Meatloaf, crust off, 45 min 1 862
Pork Bacon, fried 5 min no added oil 91 577
Bacon, microwaved, 2 slices, 3 min 9 023
Ham, deli, smoked 2 349
Liverwurst 633
Chop, pan fried, 7 min 4 752
Ribs, roasted 4 430
Roast (Chinese take-out) 3 544
Sausage, beef and pork links, pan fried 5 426
Sausage, Italian, raw 1 861
Sausage, Italian, barbecued 4 839
Sausage, pork links, microwaved, 1 min 5 943
Lamb Leg, raw 826
Leg, boiled, 30 min 1 218
Leg, broiled, 450°F, 30 min 2 431
Leg, microwave, 5 min 1 029
Veal Stewed 2 858
Chicken Ground, white meat, raw 877
Meatball, potted (cooked in liquid) 1 h 1 501
Potted (cooked in liquid) with onion and water 3 329
Roasted 6 020
Skin, back of thigh, roasted then barbecued 18 520
Glycation end product content based on carboxymethyllysine content
a
Adapted from Journal of the American Dietetic Association, Volume 110, issue 6, Jaime Uribarri, Sandra Woodruff, Susan Goodman, Weijing
Cai, Xue Chen, Renata Pyzik, Angie Yong, Gary E. Striker, Helen Vlassara, Advanced Glycation End Products in Foods and a Practical Guide to
Their Reduction in the Diet, Pages No. 911-916.e12, Copyright (2010), with permission from Elsevier (Uribarri et al., 2010)
58
The EPIC study concluded that red meat

Table 1.11 Content of N-glycolylneuraminic consumption ranged from 24 to 57 g/day for
acid in red or processed meat, raw or cooked
women and from 40 to 121 g/day for men based
under different conditions
on 24-hour recall (Linseisen et al., 2002).
Meat Neu5Gc content (µg/g)
(ii) Americas
Ground beef 25
Beef steak (raw) 134
Few representative national surveys were
Beef steak (baked) 210
available for the Americas. In the USA (FCID,
Beef steak (boiled) 231 2015), the mean consumption of total red meat
Beef steak (fried) 199 was 86 g/day for adult consumers and 242 g/day
Ground lamb 14 at the 95th percentile for the same population
Lamb steak (raw) 57 (72% consumers). For children aged between
Lamb steak (baked) 50 1 and < 3 years, mean consumption was 31 g/
Lamb steak (boiled) 47
day and 89 g/day at the 95th percentile (62%
Lamb steak (fried) 19
Ground pork 19
consumers). For children aged between 3 and
Pork chop (raw) 25 16 years, mean consumption was 60 g/day and
Pork chop (baked) 40 176 g/day at the 95th percentile (71% consumers)
Pork chop (boiled) 36 (FCID, 2015). Similarly, in Brazil, the mean
Pork chop (fried) 29 consumption of beef was 92 g/day for the general
Pork bratwurst 11 population and 232 g/day at the 95th percen-
Pork bacon 7
tile for the same population (69% consumers).
Neu5Gc, N-glycolylneuraminic acid
From Samraj et al. (2015), with permission of the editor
No data were available for children in Brazil,
and no data were available for other countries
(i) Europe in Latin America. However, according to the
GEMS Cluster diets, the dietary patterns in this
The European Food Safety Authority (EFSA)
region seemed homogeneous (FAO/WHO, 2015;
collected in a harmonized way the results from
Table 1.14 and Table 1.15).
national food consumption surveys of more
than 20 member states of the EU. The median (iii) Africa
of mean meat consumption for adults was Data were scarce and incomplete for Africa.
35 g/day, ranging from about 10 g/day Fortunately, individual food consumption
(Sweden) to 110 g/day (Austria). At the 95th surveys were performed for adult women and
percentile, meat consumption ranged from children in Burkina Faso and Uganda. In these
20 g/day (Sweden, 21% of consumers) to 237 g/ two countries, the percentage of consumers of
day (Austria, 88% of consumers). Similar results red meat was less than 5% of the population.
were found for adolescents, both in terms of However, for these adult consumers, the mean
amount consumed and percentage of the popu- consumption was between 23 and 90 g/day, and
lation that are consumers. For infants and consumption at the 95th percentile was between
toddlers, the median of mean meat consumption 28 and 147 g/day. For children, the percentage
was about 50 g/day, ranging from 20 to 80 g/day, of consumers of red meat was below 4% of this
and the percentage of consumers ranged from population. Similarly, compared with adults,
about 5% (the Netherlands) to 100% (Germany). consumption for child consumers was close to
At the 95th percentile, the meat consumption that observed in developed countries, with a mean
ranged from 40 g/day (the Netherlands) to about between 13 and 62 g/day, and a high consumption
190 g/day (Belgium) (EFSA, 2011).
59
Table 1.12 N-Nitroso compounds commonly found in processed meat
Common abbreviation Full name CAS registry No.

NMDA N-Nitrosodimethylamine 62-75-9
NDEA N-Nitrosodiethylamine 55-18-5
NPIP N-Nitrosopiperidine 100-75-4
NPYR N-Nitrosopyrrolidine 930-55-2
NDBA N-Nitrosodi-n-butylamine 924-16-3
– N-Nitrosomethylethylamine 10595-95-6
– N-Nitrosoproline 7519-36-0
– N-Nitrosohydroxyproline 30310-80-6
NMOR N-Nitrosomorpholine 59-89-2
CAS, Chemical Abstracts Service
The chemical structure of some of these compounds is given in Fig. 1.5
at the 95th percentile of between 22 and (Zhai et al., 2009). For Chinese children, the
69 g/day. It is therefore likely that the difference mean consumption of pork was 51 g/day, and
in the per capita consumption (four to five times consumption of pork at the 95th percentile was
lower in Africa than in Europe) was mainly due to 142 g/day. Beef was consumed by less than 10% of
a lower number of consumers rather than to large the Chinese population, with a mean consump-
differences in the dietary patterns of consumers tion of 46 g/day and consumption at the 95th
(FAO/WHO, 2015; Table 1.14 and Table 1.15). percentile for consumers of 130 g/day. For
children, the mean consumption of beef was
(iv) Middle East and north Africa
32 g/day, and consumption of beef at the
Intake of red meat in countries of the Middle 95th percentile was 85 g/day. These figures were
East and north Africa was estimated in 2010 close to those reported in the Americas and
to range from 200 g/week (Afghanistan) to Europe (FAO/WHO, 2015; Table 1.15).
700 g/week (Algeria and United Arab Emirates) Similarly, in the Republic of Korea, the
(Afshin et al., 2015). consumption of pork for adults was 76 g/day,
(v) Asia and consumption of pork at the 95th percentile
Food consumption surveys were available was 253 g/day (44% of consumers). For children,
from Bangladesh, China, Japan, the Philippines, the mean consumption of pork was 30 g/day,
the Republic of Korea, and Thailand. In Asia, and consumption of pork at the 95th percentile
the main types of red meat consumed were was 95 g/day. Finally, in the Philippines, for one
pork and beef (FAO/WHO, 2015). In China, third of the population, the mean consumption
the predominant red meat consumed was pork, of pork for children was 75 g/day, and consump-
with 63% of consumers, a mean consumption of tion of pork at the 95th percentile was 208 g/day
84 g/day, and consumption at the 95th percentile (33% of consumers). On the contrary, in Japan,
of 224 g/day for adult consumers only (Table 1.14). beef and pork were consumed by a wide range
Based on three consecutive 24-hour recalls, of consumers (i.e. 89% and 99% of the popu-
a prospective study of 5000 adults from 4280 lation, respectively). The mean consumption
households in nine provinces showed an increase and consumption at the 97.5th percentile for
in average consumption of pork of 20% (52 vs consumers only were 53 and 83 g/day, respec-
62 g/day per person) from 1989 to 2004 tively, i.e. about half of the consumption in north
60
Table 1.13 Major sources of dietary N-nitrosamines in processed meats
Processed meat Concentration of nitrosamines (µg/kg)

NDMA NDEA NPYR NPIP
Bacon fried ND–30 ND–1 ND–200 ND–1
Cured meats ND–4 ND–4 ND–25 ND–2
Smoked meats ND–3 ND–7.9 ND–0.1 ND–0.1
Sausages
Frankfurter ND–84 – – –
Mettwurst + + ND–105 ND–60
Liver sausage ND–35 ND–25 ND–80 –
Salami ND–80 – – –
Bologna – ND–25 ND–105 –
+, detected but not quantitated; –, not reported; ND, not detected; NDMA, N-nitrosodimethylamine; NDEA, N-nitrosodiethylamine; NPIP,
N-nitrosopiperidine; NPYR, N-nitrosopyrrolidine
From: Nitrates, nitrites and N‐nitrosocompounds: A review of the occurrence in food and diet and the toxicological implications, R. Walker, Food
Additives & Contaminants, 1990, reprinted by permission of Taylor & Francis (Taylor & Francis Ltd, http://www.tandfonline.com) (Walker, 1990)
America or in China. In Thailand, the percentage a mean consumption that for consumers only
of pork meat consumers was 89%, with a mean ranged from 13 to 70 g/day, and a consumption
consumption of 23 g/day. In Bangladesh, the at the 97.5th percentile that ranged from 83 to
percentage of red meat consumers was less than 257 g/day (FAO/WHO, 2015; Table 1.15).
10%. The mean consumption for consumers was In summary, for most countries (e.g.
between 10 and 23 g/day, and the consump- Australia, central and southern Europe, China,
tion at the 95th percentile was between 25 and the Philippines, the Republic of Korea, and the
77 g/day (FAO/WHO, 2015; Table 1.14 and USA), the mean consumption of red meat for
Table 1.15). consumers only was around 50–100 g/day, and
high consumption was around 200–300 g/day.
(iv) Oceania
The percentage of meat consumers seemed to
The 2008/09 New Zealand Adult Nutrition be proportional to the income or the level of
Survey (University of Otago and Ministry of development. In other words, the distribution
Health, 2011) estimated the mean consumption of meat consumption was fairly similar among
of beef and veal to be 180 g/day, and consump- consumers in these countries. Therefore, anal-
tion of beef and veal at the 90th percentile to be ysis of per capita data only may give the wrong
397 g/day for consumers only. The same survey perception of the levels of consumption. In some
estimated the mean consumption of lamb and countries (e.g. Japan, northern Europe, and
mutton to be 137 g/day, and consumption of lamb Thailand), the consumption of red meat was low,
and mutton at the 90th percentile to be 275 g/day. despite a percentage of consumers of about 90%,
For these two food categories, the percentage of probably due to substitution with fish and other
consumers was 24% for beef and veal meat, and seafoods. Finally, in less-industrialized countries
7% for lamb and goat meat (Parnell et al., 2012). for which data were available (e.g. Bangladesh,
Data on the consumption of pork, as well as the Burkina Faso, and Uganda), the percentage of
total red meat consumption, were not available consumers was below 10%, probably due to
for adults. For Australia, data on consumption the high price of red meat. It should be noted
were only available for children. They showed that, in these countries, the mean and high
61
62

Table 1.14 Worldwide consumption of red meat in adults
Age class Country Survey Meat type No. of No. of Percentage Consumers, Consumers, Consumers,
subjects consumers of Mean STD P975
consumers (g/bw per (g/bw per (g/bw per
day) day) day)
Adult Bangladesh Harvest_2007/8 Beef and other bovines 474 39 8.23% 0.4 0.3 0.9
women meat
Adult Bangladesh Harvest_2007/8 Goat and other caprines 474 9 1.90% 0.5 0.7 2.0
women
Adults Belgium Diet_National_2004 Beef and other bovines 1304 449 34.43% 0.9 0.7 2.5
meat
Adults Belgium Diet_National_2004 Horse and other equines 1304 16 1.23% 1.1 0.7 2.6
Adults Belgium Diet_National_2004 Meat from mammals 1304 9 0.69% 0.7 0.3 1.1
other than marine
mammals, NES
Adults Belgium Diet_National_2004 Pork and other porcines 1304 273 20.94% 0.9 0.5 2.3
Adults Belgium Diet_National_2004 Sheep and other ovines 1304 84 6.44% 0.9 0.5 2.1
General Brazil Brazilian Institute Beef and other bovines 34 003 23 320 68.58% 1.4 1.2 4.4
population of Geography and meat
Statistics
General Brazil Brazilian Institute Goat and other caprines 34 003 194 0.57% 1.8 1.2 4.8
population of Geography and
Statistics
General Brazil Brazilian Institute Meat from mammals 34 003 2071 6.09% 1.0 0.9 3.5
population of Geography and other than marine
Statistics mammals, NES
General Brazil Brazilian Institute Pork and other porcines 34 003 2577 7.58% 1.8 1.7 6.3
Statistics
General Brazil Brazilian Institute Sheep and other ovines 34 003 136 0.40% 1.5 1.1 4.8
Statistics
Adult Burkina Harvest_2010 Beef and other bovines 287 7 2.44% 0.4 0.1 0.5
women Faso meat
Adult Burkina Harvest_2010 Goat and other caprines 287 7 2.44% 0.7 0.5 1.5
women Faso
Adult Burkina Harvest_2010 Meat from mammals 287 3 1.05% 1.7 0.5 2.2
women Faso other than marine
mammals, NES
Table 1.14 (continued)
day) day) day)
Adult Burkina Harvest_2010 Pork and other porcines 287 11 3.83% 0.8 0.5 1.8
women Faso
Adult Burkina Harvest_2010 Sheep and other ovines 287 4 1.39% 0.9 0.3 1.2
women Faso
General China 2002 China Nutrition Beef and other bovines 65 359 5278 8.08% 0.9 0.9 3.2
population and Health Survey meat
General China 2002 China Nutrition Horse and other equines 65 359 66 0.10% 2.1 4.0 10.4
population and Health Survey
General China 2002 China Nutrition Meat from mammals 65 359 635 0.97% 1.2 1.2 4.6
population and Health Survey other than marine
mammals, NES
General China 2002 China Nutrition Pork and other porcines 65 359 41 283 63.16% 1.6 1.4 5.3
General China 2002 China Nutrition Sheep and other ovines 65 359 3690 5.65% 1.2 1.2 4.3
Adults Czech SISP04 Beef and other bovines 1666 514 30.85% 0.8 0.6 2.2
Republic meat
Adults Czech SISP04 Pork and other porcines 1666 694 41.66% 1.1 0.7 2.9
Republic
Adults Denmark Danish_Dietary_ Beef and other bovines 2822 2780 98.51% 0.5 0.4 1.4
Survey meat
Adults Denmark Danish_Dietary_ Pork and other porcines 2822 2750 97.45% 0.6 0.5 1.8
Survey

Adults Denmark Danish_Dietary_ Sheep and other ovines 2822 187 6.63% 0.4 0.2 1.0
Survey
Adults Finland FINDIET_2007 Beef and other bovines 1575 695 44.13% 0.6 0.5 2.0
meat
Adults Finland FINDIET_2007 Pork and other porcines 1575 431 27.37% 0.7 0.6 2.4
Adults Finland FINDIET_2007 Sheep and other ovines 1575 62 3.94% 0.6 0.6 1.8
Adults France INCA2 Beef and other bovines 2276 2002 87.96% 0.7 0.5 1.8
meat
Adults France INCA2 Horse and other equines 2276 52 2.28% 0.3 0.2 0.8
Adults France INCA2 Meat from mammals 2276 825 36.25% 0.1 0.2 0.5
other than marine
mammals, NES
63
64

day) day) day)
Adults France INCA2 Pork and other porcines 2276 1154 50.70% 0.3 0.3 1.1
Adults France INCA2 Sheep and other ovines 2276 627 27.55% 0.2 0.2 0.7
Adults Hungary National_Repr_Surv Beef and other bovines 1074 382 35.57% 0.3 0.3 1.1
meat
Adults Hungary National_Repr_Surv Pork and other porcines 1074 860 80.07% 0.9 0.6 2.6
Adults Hungary National_Repr_Surv Sheep and other ovines 1074 8 0.74% 0.5 0.2 0.8
Adults Ireland NSIFCS Beef and other bovines 958 761 79.44% 0.7 0.6 2.0
meat
Adults Ireland NSIFCS Pork and other porcines 958 427 44.57% 0.5 0.4 1.5
Adults Ireland NSIFCS Sheep and other ovines 958 361 37.68% 0.4 0.3 1.4
Adults Italy INRAN_ Beef and other bovines 2313 1698 73.41% 0.8 0.6 2.3
SCAI_2005_06 meat
Adults Italy INRAN_ Goat and other caprines 2313 3 0.13% 0.6 0.2 0.8
SCAI_2005_06
Adults Italy INRAN_ Horse and other equines 2313 57 2.46% 0.7 0.4 1.5
SCAI_2005_06
Adults Italy INRAN_ Pork and other porcines 2313 735 31.78% 0.6 0.5 1.8
SCAI_2005_06
Adults Italy INRAN_ Sheep and other ovines 2313 71 3.07% 0.6 0.8 1.4
SCAI_2005_06
General Japan DSFFQ _FI Beef and other bovines 2711 2406 88.75% 0.3 0.3 1.0
population meat
General Japan DSFFQ _FI Meat from mammals 2711 112 4.13% 0.2 0.1 0.7
population other than marine
mammals, NES
General Japan DSFFQ _FI Pork and other porcines 2711 2691 99.26% 0.6 0.4 1.5
population
Adults Latvia EFSA_TEST Beef and other bovines 1306 66 5.05% 0.8 0.6 2.7
meat
Adults Latvia EFSA_TEST Goat and other caprines 1306 1 0.08% 0.7 0.7
Adults Latvia EFSA_TEST Meat from mammals 1306 20 1.53% 0.7 0.4 1.7
other than marine
mammals, NES
Adults Latvia EFSA_TEST Pork and other porcines 1306 796 60.95% 1.2 0.9 3.5
day) day) day)
Adults Latvia EFSA_TEST Sheep and other ovines 1306 5 0.38% 0.8 0.3 1.3
Adults Netherlands DNFCS_2003 Beef and other bovines 750 180 24.00% 1.0 0.6 2.5
meat
Adults Netherlands DNFCS_2003 Horse and other equines 750 2 0.27% 0.2 0.1 0.3
Adults Netherlands DNFCS_2003 Pork and other porcines 750 309 41.20% 1.2 0.9 3.8
Adults Netherlands DNFCS_2003 Sheep and other ovines 750 30 4.00% 1.2 0.9 4.1
General Republic of KNHNES Beef and other bovines 9391 3141 33.45% 0.9 1.2 4.1
population Korea meat
General Republic of KNHNES Pork and other porcines 9391 4124 43.91% 1.4 1.8 6.3
population Korea
Adults Spain AESAN_FIAB Beef and other bovines 981 680 69.32% 1.1 0.7 2.8
meat
Adults Spain AESAN Beef and other bovines 410 176 42.93% 1.2 0.8 3.2
meat
Adults Spain AESAN_FIAB Goat and other caprines 981 3 0.31% 1.1 0.2 1.3
Adults Spain AESAN_FIAB Pork and other porcines 981 366 37.31% 1.0 0.7 3.0
Adults Spain AESAN Pork and other porcines 410 129 31.46% 1.0 0.6 2.4
Adults Spain AESAN_FIAB Sheep and other ovines 981 102 10.40% 1.0 0.5 2.3
Adults Spain AESAN Sheep and other ovines 410 18 4.39% 1.1 0.9 3.8
Adults Sweden Riksmaten_1997_98 Beef and other bovines 1210 590 48.76% 0.3 0.2 0.9
meat
Adults Sweden Riksmaten_1997_98 Horse and other equines 1210 8 0.66% 0.1 0.1 0.5

Adults Sweden Riksmaten_1997_98 Pork and other porcines 1210 699 57.77% 0.4 0.2 1.0
Adults Sweden Riksmaten_1997_98 Sheep and other ovines 1210 32 2.64% 0.2 0.2 1.0
General Thailand FCDT Beef and other bovines 16 383 7880 48.10% 0.1
population meat
General Thailand FCDT Pork and other porcines 16 383 14 646 89.40% 0.4
population
Adult Uganda Harvest_2007 Beef and other bovines 176 8 4.55% 1.2 0.8 2.8
women meat
Adult Uganda Harvest_2007 Goat and other caprines 176 2 1.14% 1.2 0.7 1.7
women
Adults United NDNS Beef and other bovines 1724 1349 78.25% 0.4 0.3 1.1
Kingdom meat
65
66

day) day) day)
Adults United NDNS Pork and other porcines 1724 535 31.03% 0.3 0.2 0.9
Kingdom
Adults United NDNS Sheep and other ovines 1724 434 25.17% 0.3 0.2 0.8
Kingdom
Adults USA FCID-WWEIA data Total red meat 31 484 23 825 75.67% 1.1 3.06*
over 16 for years 2005–2010
years
General USA FCID-WWEIA data Total red meat 49 343 35 752 72.46% 1.2 3.59*
population for years 2005–2010
General USA FCID-WWEIA data Sheep meat 49 343 2518 5.10% 0.1 0.56*
General USA FCID-WWEIA data Goat meat 49 343 35 0.07% 1.9 5.8*
General USA FCID-WWEIA data Pork meat 49 343 26 256 53.21% 0.55 2.04*
General USA FCID-WWEIA data Beef meat 49 343 29 788 60.37% 0.96 3.08*
* 95th percentile
NES, not elsewhere specified
Data on USA from FCID (2015): What We Eat In America – Food Commodity Intake Database 2005–10, United States Environmental Protection Agency – Office of Pesticide Programs
© University of Maryland 2012 – 2016. Available from: http://fcid.foodrisk.org/percentiles.php
Data for other countries from FAO/WHO (2015): the FAO/WHO Chronic individual food consumption database – Summary statistics (CIFOCOss), © Copyright World Health
Organization (WHO), 2016. All Rights Reserved. Available from: http://www.who.int/foodsafety/databases/en/
Table 1.15 Worldwide consumption of red meat in children
subjects consumers of mean STD (g/bw P975 (g/bw
consumers consumption per day) per day)
(g/bw per
day)
Adolescents Belgium Diet_National_2004 Beef and other bovines 584 175 29.97% 1.0 0.7 2.5
meat
Adolescents Belgium Diet_National_2004 Horse and other equines 584 6 1.03% 1.3 0.4 1.9
Adolescents Belgium Diet_National_2004 Meat from mammals 584 11 1.88% 0.7 0.4 1.7
other than marine
mammals, NES
Adolescents Belgium Diet_National_2004 Pork and other porcines 584 121 20.72% 1.1 0.7 3.1
Adolescents Belgium Diet_National_2004 Sheep and other ovines 584 43 7.36% 1.0 0.7 2.8
Adolescents Cyprus Childhealth Beef and other bovines 303 18 5.94% 0.6 0.2 0.9
meat
Adolescents Cyprus Childhealth Pork and other porcines 303 154 50.83% 1.1 0.6 2.8
Adolescents Cyprus Childhealth Sheep and other ovines 303 12 3.96% 0.8 0.4 1.8
Adolescents Czech SISP04 Beef and other bovines 298 97 32.55% 1.2 0.8 3.1
Republic meat
Adolescents Czech SISP04 Pork and other porcines 298 125 41.95% 1.4 0.8 3.2
Republic
Adolescents Denmark Danish Dietary Beef and other bovines 479 478 99.79% 0.7 0.5 2.0
Survey meat
Adolescents Denmark Danish_Dietary_ Pork and other porcines 479 472 98.54% 0.7 0.5 2.0
Survey
Adolescents Denmark Danish_Dietary_ Sheep and other ovines 479 21 4.38% 0.5 0.3 1.3

Survey
Adolescents France INCA2 Beef and other bovines 973 912 93.73% 0.9 0.6 2.4
meat
Adolescents France INCA2 Horse and other equines 973 21 2.16% 0.5 0.3 1.6
Adolescents France INCA2 Meat from mammals 973 424 43.58% 0.2 0.2 1.0
other than marine
mammals, NES
Adolescents France INCA2 Pork and other porcines 973 482 49.54% 0.4 0.3 1.2
Adolescents France INCA2 Sheep and other ovines 973 257 26.41% 0.3 0.3 0.8
Adolescents Italy INRAN_ Beef and other bovines 247 204 82.59% 1.2 0.9 3.2
SCAI_2005_06 meat
67
68

(g/bw per
day)
Adolescents Italy INRAN_ Horse and other equines 247 8 3.24% 0.8 0.3 1.4
SCAI_2005_06
Adolescents Italy INRAN_ Pork and other porcines 247 81 32.79% 0.8 0.7 2.5
SCAI_2005_06
Adolescents Italy INRAN_ Sheep and other ovines 247 2 0.81% 0.7 0.2 0.9
SCAI_2005_06
Adolescents Latvia EFSA_TEST Beef and other bovines 470 16 3.40% 0.9 0.6 2.3
meat
Adolescents Latvia EFSA_TEST Meat from mammals 470 4 0.85% 0.5 0.1 0.5
other than marine
mammals, NES
Adolescents Latvia EFSA_TEST Pork and other porcines 470 263 55.96% 1.4 1.1 4.1
Adolescents Spain AESAN_FIAB Beef and other bovines 86 62 72.09% 1.4 1.0 4.5
meat
Adolescents Spain NUT_INK05 Beef and other bovines 651 294 45.16% 1.7 1.1 4.8
meat
Adolescents Spain NUT_INK05 Goat and other caprines 651 2 0.31% 1.3 0.5 1.6
Adolescents Spain enKid Horse and other equines 209 2 0.96% 1.0 0.2 1.2
Adolescents Spain NUT_INK05 Horse and other equines 651 1 0.15% 1.3 1.3
Adolescents Spain enKid Meat from mammals 209 69 33.01% 1.5 0.9 3.9
other than marine
mammals, NES
Adolescents Spain AESAN_FIAB Pork and other porcines 86 42 48.84% 1.0 0.6 2.0
Adolescents Spain enKid Pork and other porcines 209 60 28.71% 1.2 0.8 3.3
Adolescents Spain NUT_INK05 Pork and other porcines 651 212 32.57% 1.1 0.7 3.3
Adolescents Spain AESAN_FIAB Sheep and other ovines 86 4 4.65% 1.3 0.6 2.0
Adolescents Spain enKid Sheep and other ovines 209 11 5.26% 1.9 2.3 8.5
Adolescents Spain NUT_INK05 Sheep and other ovines 651 29 4.45% 1.3 0.7 3.8
Adolescents Sweden NFA Beef and other bovines 1018 542 53.24% 0.5 0.4 1.7
meat
Adolescents Sweden NFA Horse and other equines 1018 9 0.88% 0.3 0.3 0.9
Adolescents Sweden NFA Pork and other porcines 1018 286 28.09% 0.8 0.5 2.0
Adolescents Sweden NFA Sheep and other ovines 1018 6 0.59% 0.8 0.8 2.4
(g/bw per
day)
Children Bangladesh Harvest_2007/8 Beef and other bovines 555 41 7.39% 1.0 0.8 3.0
meat
Children Bangladesh Harvest_2007/8 Goat and other caprines 555 12 2.16% 0.9 0.7 2.1
Children Burkina Harvest_2010 Beef and other bovines 288 7 2.43% 0.9 0.6 1.5
Faso meat
Children Burkina Harvest_2010 Goat and other caprines 288 6 2.08% 1.8 1.0 3.3
Faso
Children Burkina Harvest_2010 Meat from mammals 288 3 1.04% 4.8 3.6 8.0
Faso other than marine
mammals, NES
Children Burkina Harvest_2010 Pork and other porcines 288 10 3.47% 2.2 1.6 5.7
Faso
Children Burkina Harvest_2010 Sheep and other ovines 288 3 1.04% 1.9 0.9 2.8
Faso
Children China 2002 China Nutrition Beef and other bovines 2784 171 6.14% 2.0 1.7 6.7
and Health Survey meat
Children China 2002 China Nutrition Horse and other equines 2784 7 0.25% 7.6 10.4 30.9
and Health Survey
Children China 2002 China Nutrition Meat from mammals 2784 27 0.97% 2.6 2.6 10.6
and Health Survey other than marine
mammals, NES
Children China 2002 China Nutrition Pork and other porcines 2784 1703 61.17% 3.3 2.7 10.5

and Health Survey
Children China 2002 China Nutrition Sheep and other ovines 2784 119 4.27% 2.8 2.9 10.3
and Health Survey
Children Japan DSFFQ _FI Beef and other bovines 71 66 92.96% 0.5 0.4 1.3
meat
Children Japan DSFFQ _FI Meat from mammals 71 1 1.41% 0.1
other than marine
mammals, NES
Children Japan DSFFQ _FI Pork and other porcines 71 71 100.00% 1.3 0.8 3.7
Children Philippines Harvest_2003 Beef and other bovines 1205 61 5.06% 1.3 0.8 2.8
meat
69
70

(g/bw per
day)
Children Philippines Harvest_2003 Meat from mammals 1205 22 1.83% 1.4 0.9 3.1
other than marine
mammals, NES
Children Philippines Harvest_2003 Pork and other porcines 1205 395 32.78% 1.4 1.5 5.2
Children Republic of KNHNES Beef and other bovines 654 255 38.99% 1.1 1.3 4.9
Korea meat
Children Republic of KNHNES Pork and other porcines 654 329 50.31% 1.9 2.0 6.5
Korea
Children Australia 2007 ANCNPAS Beef and other bovines 4487 3898 86.87% 1.8 1.9 6.8
(2-16 yrs) meat
Children Australia 2007 ANCNPAS Pork and other porcines 4487 3594 80.10% 0.9 1.2 4.1
(2-16 yrs)
Children Australia 2007 ANCNPAS Sheep and other ovines 4487 2479 55.25% 0.6 1.1 4.0
(2-16 yrs)
Children Australia 2007 ANCNPAS Beef and other bovines 1463 1226 83.80% 2.3 2.1 8.4
(2-6 yrs) meat
Children Australia 2007 ANCNPAS Pork and other porcines 1463 1114 76.14% 1.3 1.4 5.1
(2-6 yrs)
Children Australia 2007 ANCNPAS Sheep and other ovines 1463 741 50.65% 0.7 1.2 4.4
(2-6 yrs)
Infants Bulgaria NUTRICHILD Beef and other bovines 860 89 10.35% 2.7 1.6 7.8
meat
Infants Bulgaria NUTRICHILD Pork and other porcines 860 9 1.05% 2.3 2.2 7.3
Infants Bulgaria NUTRICHILD Sheep and other ovines 860 2 0.23% 2.4 1.0 3.1
Infants Italy INRAN_ Beef and other bovines 16 1 6.25% 3.8 3.8
SCAI_2005_06 meat
Infants Italy INRAN_ Pork and other porcines 16 1 6.25% 1.0 1.0
SCAI_2005_06
Infants Italy INRAN_ Sheep and other ovines 16 1 6.25% 1.3 1.3
SCAI_2005_06
Other Belgium Regional_Flanders Meat from mammals 625 16 2.56% 1.2 0.8 3.3
children other than marine
mammals, nes
(g/bw per
day)
Other Belgium Regional_Flanders Sheep and other ovines 625 10 1.60% 1.4 0.6 2.3
children
Other Belgium Regional_Flanders Beef and other bovines 625 185 29.60% 1.4 0.8 3.1
children meat
Other Belgium Regional_Flanders Horse and other equines 625 8 1.28% 1.3 0.6 2.2
children
Other Belgium Regional_Flanders Pork and other porcines 625 121 19.36% 1.2 0.7 3.1
children
Other Bulgaria NUTRICHILD Beef and other bovines 433 276 63.74% 2.6 1.8 7.2
children meat
Other Bulgaria NUTRICHILD Pork and other porcines 433 37 8.55% 1.9 1.2 6.2
children
Other Bulgaria NUTRICHILD Sheep and other ovines 433 8 1.85% 1.8 1.2 3.2
children
Other Czech SISP04 Beef and other bovines 389 125 32.13% 1.7 1.2 4.5
children Republic meat
Other Czech SISP04 Pork and other porcines 389 121 31.11% 2.0 1.3 5.8
children Republic
Other Denmark Danish_Dietary_ Beef and other bovines 490 482 98.37% 0.9 0.6 2.3
children Survey meat
Other Denmark Danish_Dietary_ Pork and other porcines 490 480 97.96% 1.1 0.8 3.0
children Survey

Other Denmark Danish_Dietary_ Sheep and other ovines 490 25 5.10% 0.6 0.3 1.3
children Survey
Other Finland DIPP Beef and other bovines 933 634 67.95% 1.4 1.1 4.6
children meat
Other Finland STRIP Beef and other bovines 250 81 32.40% 0.8 0.6 2.1
children meat
Other Finland DIPP Pork and other porcines 933 373 39.98% 1.0 1.2 3.8
children
Other Finland STRIP Pork and other porcines 250 64 25.60% 0.8 0.6 2.4
children
Other Finland DIPP Sheep and other ovines 933 23 2.47% 0.6 0.4 1.5
children
71
72

(g/bw per
day)
Other Finland STRIP Sheep and other ovines 250 4 1.60% 1.0 1.1 2.6
children
Other France INCA2 Beef and other bovines 482 440 91.29% 1.5 1.0 3.9
children meat
Other France INCA2 Horse and other equines 482 9 1.87% 0.7 0.2 1.1
children
Other France INCA2 Meat from mammals 482 175 36.31% 0.2 0.4 1.7
mammals, NES
Other France INCA2 Pork and other porcines 482 227 47.10% 0.7 0.5 1.8
children
Other France INCA2 Sheep and other ovines 482 130 26.97% 0.4 0.3 1.4
children
Other Greece Regional_Crete Beef and other bovines 839 24 2.86% 1.3 0.8 3.1
children meat
Other Greece Regional_Crete Goat and other caprines 839 23 2.74% 1.5 0.8 3.5
children
Other Greece Regional_Crete Meat from mammals 839 54 6.44% 1.5 0.9 3.8
mammals, NES
Other Greece Regional_Crete Pork and other porcines 839 288 34.33% 1.7 0.9 3.9
children
Other Greece Regional_Crete Sheep and other ovines 839 149 17.76% 1.3 0.7 3.7
children
Other Italy INRAN_ Beef and other bovines 193 151 78.24% 2.0 1.4 6.0
children SCAI_2005_06 meat
Other Italy INRAN_ Horse and other equines 193 1 0.52% 1.7 1.7
children SCAI_2005_06
Other Italy INRAN_ Pork and other porcines 193 71 36.79% 1.2 0.9 3.2
Other Italy INRAN_ Sheep and other ovines 193 4 2.07% 1.0 0.7 1.9
Other Latvia EFSA_TEST Beef and other bovines 189 6 3.17% 1.2 0.3 1.8
children meat
(g/bw per
day)
Other Latvia EFSA_TEST Meat from mammals 189 2 1.06% 1.4 0.7 1.9
mammals, NES
Other Latvia EFSA_TEST Pork and other porcines 189 105 55.56% 1.6 1.1 4.5
children
Other Netherlands VCP_kids Beef and other bovines 957 255 26.65% 1.2 1.0 3.4
children meat
Other Netherlands VCP_kids Horse and other equines 957 2 0.21% 0.3 0.1 0.4
children
Other Netherlands VCP_kids Pork and other porcines 957 167 17.45% 1.1 0.8 3.0
children
Other Netherlands VCP_kids Sheep and other ovines 957 10 1.04% 0.6 0.3 1.3
children
Other Spain NUT_INK05 Beef and other bovines 399 155 38.85% 2.3 1.4 6.1
children meat
Other Spain enKid Horse and other equines 156 1 0.64% 3.9 3.9
children
Other Spain NUT_INK05 Horse and other equines 399 2 0.50% 3.1 1.3 4.1
children
Other Spain enKid Meat from mammals 156 44 28.21% 2.4 1.4 6.4
mammals, NES

Other Spain enKid Pork and other porcines 156 32 20.51% 1.8 1.0 4.6
children
Other Spain NUT_INK05 Pork and other porcines 399 124 31.08% 1.5 0.9 3.7
children
Other Spain enKid Sheep and other ovines 156 5 3.21% 2.7 1.0 3.8
children
Other Spain NUT_INK05 Sheep and other ovines 399 12 3.01% 1.9 1.2 4.9
children
Other Sweden NFA Beef and other bovines 1473 826 56.08% 0.6 0.5 1.9
children meat
Other Sweden NFA Horse and other equines 1473 15 1.02% 0.2 0.2 0.7
children
73
74

(g/bw per
day)
Other Sweden NFA Pork and other porcines 1473 536 36.39% 0.9 0.7 2.7
children
Other Sweden NFA Sheep and other ovines 1473 15 1.02% 0.6 0.4 1.7
children
Toddlers Belgium Regional_Flanders Beef and other bovines 36 12 33.33% 1.4 0.8 3.0
meat
Toddlers Belgium Regional_Flanders Meat from mammals 36 2 5.56% 1.8 0.7 2.3
other than marine
mammals, NES
Toddlers Belgium Regional_Flanders Horse and other equines 36 1 2.78% 5.0 5.0
Toddlers Belgium Regional_Flanders Pork and other porcines 36 11 30.56% 2.1 2.0 7.3
Toddlers Bulgaria NUTRICHILD Beef and other bovines 428 229 53.50% 2.8 2.0 7.5
meat
Toddlers Bulgaria NUTRICHILD Pork and other porcines 428 26 6.07% 1.6 1.2 5.5
Toddlers Bulgaria NUTRICHILD Sheep and other ovines 428 11 2.57% 1.6 1.0 4.0
Toddlers Finland DIPP Beef and other bovines 497 406 81.69% 2.0 1.6 6.4
meat
Toddlers Finland DIPP Pork and other porcines 497 326 65.59% 1.4 1.4 4.8
Toddlers Finland DIPP Sheep and other ovines 497 26 5.23% 1.0 0.8 4.5
Toddlers Italy INRAN_ Beef and other bovines 36 20 55.56% 2.4 1.6 6.3
SCAI_2005_06 meat
Toddlers Italy INRAN_ Pork and other porcines 36 7 19.44% 0.6 0.2 1.1
SCAI_2005_06
Toddlers Italy INRAN_ Sheep and other ovines 36 2 5.56% 1.6 0.7 2.1
SCAI_2005_06
Toddlers Netherlands VCP_kids Beef and other bovines 322 84 26.09% 1.4 1.2 4.8
meat
Toddlers Netherlands VCP_kids Pork and other porcines 322 47 14.60% 1.2 1.1 4.0
Toddlers Netherlands VCP_kids Sheep and other ovines 322 1 0.31% 1.0 1.0
Toddlers Spain enKid Meat from mammals 17 3 17.65% 3.6 0.5 4.1
other than marine
mammals, NES
Toddlers Spain enKid Sheep and other ovines 17 2 11.76% 1.1 0.5 1.4
(g/bw per
day)
Children USA FCID-WWEIA data Total red meat 5338 2451 45.92% 2.4 7.04
(1–3 yrs) for years 2005–2010
Children USA FCID-WWEIA data Total red meat 12 521 9605 76.71% 1.7 4.98
(3–16 yrs) for years 2005–2010
Data on USA from FCID (2015): What We Eat In America - Food Commodity Intake Database 2005-10, U.S. Environmental Protection Agency - Office of Pesticide Programs ©
University of Maryland 2012 – 2016. Available from: http://fcid.foodrisk.org/percentiles.php

75
consumption for consumers were up to 90 and to 34 g/day (26–76 g/day) for the fifth quintile
150 g/day, respectively (FAO/WHO, 2015; (Imamura et al., 2015).
Table 1.14, Table 1.15). These levels of consumption of processed
meat were consistent with those in Japan, where
(d) Offal consumption the percentage of consumers was about 97%,
The per capita consumption of mammalian the mean consumption was 14 g/day, and the
offal worldwide was generally lower than 10 g/day consumption at the 95th percentile was 34 g/day
per person, except for Australia and European (FAO/WHO, 2015; Table 1.16). On the contrary, in
countries, where the highest levels (15 g/day per China, the percentage of consumers of processed
person) were reported by GEMS clusters diets meat was about 2–3.8% of the total population;
(WHO, 2013). From National food consumption however, for this group, the mean consumption
surveys, high mean consumption for consumers and the consumption at the 95th percentile were
only was reported for a limited proportion of the 66 and 182 g/day, respectively (FAO/WHO, 2015;
population. For example, in Brazil, the average Table 1.16). Based on three consecutive 24-hour
consumption of mammalian offal in the general recalls, a prospective study of 5000 adults from
population was 84 g/day per person for 3.5% of 4280 households in nine provinces showed
consumers (FAO/WHO, 2015). In Germany, the that the average processed meat consumption
mean consumption of cattle offal for adults was increased by three-fold (5 vs 15 g/day per person)
53 g/day per person for 0.3% of consumers. In from 1989 to 2004 (Zhai et al., 2009).
China, the consumption of mammalian offal by Intake of processed meat in countries of the
the general population was 44 g/day per person Middle East and north Africa was estimated
for 3.5% of consumers. It should be noted that in 2010 to range from 2.5 g/day (Palestine) to
high consumers can eat up to about 260 g/day per 6.7 g/day (United Arab Emirates) (Afshin et al.,
person of mammalian offal (Brazil), and in such 2015).
situations, offal was a likely substitute for other In New Zealand, the mean consumption
meat products (FAO/WHO, 2015). of sausages and processed meat was 110 g/day
for women and 142 g/day for men. At the 90th
(e) Processed meat consumption percentile, the consumption reached 212 g/day for
The consumption of processed meat is more women and 300 g/day for men. In addition, the
difficult to estimate than that of red meat, as it is percentage of consumers older than 15 years was
a heterogeneous food group with different defini- about 16% of the population (Parnell et al., 2012).
tions across countries. Detailed worldwide data In Brazil, the percentage of consumers of
on processed meat consumption (g/kg bw per processed meat was about 27% of the total popula-
day) are presented in Table 1.16 and Table 1.17 for tion; however, for this group, the mean consump-
adults and children, respectively. tion and the consumption at the 95th percentile
According to the per capita data collected by were 33 and 94 g/day, respectively (FAO/WHO,
FAOSTAT, the total processed meat consump- 2015; Table 1.16).
tion was between 0 and 33 g/day (FAO/WHO, In the USA, detailed results were available
2015). Based on the GEMS cluster diets, the total for processed meat from game, beef, goat, and
processed meat consumption ranged from less pork. Interestingly, the percentage of consumers
than 1 to 18 g/day (WHO, 2013). ranged from 0.07% (processed goat meat) to 65%
In the NutriCoDE study, the median of mean (processed beef meat), but the mean consumption
consumption of processed meat ranged from ranged from 42 to 99 g/day, and the consumption
3.9 g/day (1.8–5.1 g/day) for the first quintile
76
Table 1.16 Worldwide consumption of processed meat in adults
Age class Country Survey Meat type No. of No. of Percentage of Consumers, Consumers, Consumers,
subjects consumers consumers mean STD (g/bw P975 (g/bw
consumption per day) per day)
(g/bw per day)
General Brazil Brazilian Institute Processed meat and 34 003 334 0.98% 0.6 0.6 2.1
population of Geography and meat products, NES
Statistics
Statistics
Statistics
Statistics
Statistics
Statistics
General China 2002 China Nutrition Processed meat and 65 359 1430 2.19% 1.2 1.1 4.2
population and Health Survey meat products, NES
General China 2002 China Nutrition Processed meat and 65 359 2483 3.80% 0.9 1.3 2.7
population and Health Survey meat products, NES
General Japan DSFFQ _FI Processed meat and 2711 2642 97.45% 0.3 0.2 0.8

population meat products, NES
General Japan DSFFQ _FI Processed meat and 2711 24 0.89% 0.0 0.0
population meat products, NES
Adults Belgium Diet_National_2004 Processed meat and 1304 956 73.31% 0.8 0.7 2.7
meat products, NES
Adults Czech SISP04 Processed meat and 1666 1427 85.65% 1.2 1.0 3.9
Republic meat products, NES
Adults Denmark Danish Dietary Processed meat and 2822 2800 99.22% 0.4 0.3 1.3
Survey meat products, NES
Adults Finland FINDIET_2007 Processed meat and 1575 1188 75.43% 0.7 0.7 2.9
meat products, NES
77
78

subjects consumers consumers mean STD (g/bw P975 (g/bw
(g/bw per day)
Adults France INCA2 Processed meat and 2276 2167 95.21% 0.6 0.4 1.6
meat products, NES
Adults Hungary National_Repr_Surv Processed meat and 1074 1003 93.39% 1.1 0.8 3.0
meat products, NES
Adults Ireland NSIFCS Processed meat and 958 906 94.57% 0.8 0.6 2.1
meat products, NES
Adults Italy INRAN_ Processed meat and 2313 1921 83.05% 0.5 0.4 1.6
SCAI_2005_06 meat products, NES
Adults Latvia EFSA_TEST Processed meat and 1306 868 66.46% 0.9 0.7 2.8
meat products, NES
Adults Netherlands DNFCS_2003 Processed meat and 750 618 82.40% 0.7 0.6 2.4
meat products, NES
Adults Spain AESAN Processed meat and 410 334 81.46% 0.9 0.7 2.5
meat products, NES
Adults Spain AESAN_FIAB Processed meat and 981 908 92.56% 0.8 0.6 2.5
meat products, NES
Adults Sweden Riksmaten_1997_98 Processed meat and 1210 1147 94.79% 0.7 0.4 1.6
meat products, NES
Adults United NDNS Processed meat and 1724 1492 86.54% 0.5 0.4 1.4
Kingdom meat products, NES
Data on USA from FCID (2015): What We Eat In America – Food Commodity Intake Database 2005–10, US. Environmental Protection Agency – Office of Pesticide Programs ©
University of Maryland 2012 – 2016. Available from: http://fcid.foodrisk.org/percentiles.php
Table 1.17 Worldwide consumption of processed meat in children
subjects consumers consumers Mean STD (g/bw P975 (g/bw
(g/bw per
day)
Adolescents Belgium Diet_National_2004 Processed meat and 584 413 70.72% 0.8 0.7 2.7
meat products, NES
Adolescents Cyprus Child health Processed meat and 303 183 60.40% 0.4 0.3 1.1
meat products, NES
Adolescents Czech SISP04 Processed meat and 298 274 91.95% 1.4 1.2 4.6
Republic meat products, NES
Adolescents Denmark Danish Dietary Processed meat and 479 477 99.58% 0.6 0.5 2.0
Survey meat products, NES
Adolescents France INCA2 Processed meat and 973 950 97.64% 0.7 0.5 2.2
meat products, NES
Adolescents Italy INRAN_ Processed meat and 247 216 87.45% 0.8 0.6 2.2
Adolescents Latvia EFSA_TEST Processed meat and 470 333 70.85% 1.2 1.0 3.7
meat products, NES
Adolescents Spain enKid Processed meat and 209 190 90.91% 1.6 1.3 5.3
meat products, NES
Adolescents Spain AESAN_FIAB Processed meat and 86 81 94.19% 1.0 0.7 2.7
meat products, NES
Adolescents Spain NUT_INK05 Processed meat and 651 574 88.17% 1.1 0.9 3.4
meat products, NES
Adolescents Sweden NFA Processed meat and 1018 918 90.18% 1.0 0.8 2.5
meat products, NES

Children China 2002 China Processed meat and 2784 78 2.80% 2.2 1.5 6.8
Nutrition and meat products, NES
Health Survey
Children China 2002 China Processed meat and 2784 78 2.80% 2.2 6.3 8.9
Nutrition and meat products, NES
Health Survey
Children Japan DSFFQ _FI Processed meat and 71 71 100.00% 0.8 0.6 2.6
meat products, NES
Infants Bulgaria NUTRICHILD Processed meat and 860 33 3.84% 2.1 1.3 6.3
meat products, NES
Infants Italy INRAN_ Processed meat and 16 1 6.25% 1.5 1.5
79
80

(g/bw per
day)
Other Belgium Regional Flanders Processed meat and 625 468 74.88% 1.5 1.3 4.7
children meat products, NES
Other Bulgaria NUTRICHILD Processed meat and 433 261 60.28% 1.9 1.6 5.7
Other Czech SISP04 Processed meat and 389 314 80.72% 1.6 1.4 5.5
children Republic meat products, NES
Other Denmark Danish Dietary Processed meat and 490 488 99.59% 1.3 0.9 4.0
children Survey meat products, NES
Other Finland STRIP Processed meat and 250 218 87.20% 1.3 1.0 3.9
Other Finland DIPP Processed meat and 933 825 88.42% 1.8 1.6 6.1
Other France INCA2 Processed meat and 482 465 96.47% 1.3 0.9 3.5
Other Greece Regional Crete Processed meat and 839 327 38.97% 0.5 0.5 1.8
Other Italy INRAN_ Processed meat and 193 157 81.35% 1.2 1.0 4.0
children SCAI_2005_06 meat products, NES
Other Latvia EFSA_TEST Processed meat and 189 113 59.79% 1.8 1.6 6.4
Other Netherlands VCP kids Processed meat and 957 748 78.16% 1.6 1.2 4.5
Other Spain enKid Processed meat and 156 138 88.46% 2.2 1.5 6.5
Other Spain NUT_INK05 Processed meat and 399 357 89.47% 1.7 1.2 4.5
Other Sweden NFA Processed meat and 1473 1379 93.62% 1.5 1.1 4.3
Toddlers Belgium Regional Flanders Processed meat and 36 24 66.67% 1.9 1.2 5.7
meat products, NES
Toddlers Bulgaria NUTRICHILD Processed meat and 428 164 38.32% 2.0 1.5 5.2
meat products, NES
(g/bw per
day)
Toddlers Finland DIPP Processed meat and 497 142 28.57% 1.5 1.6 5.5
meat products, NES
Toddlers Italy INRAN_ Processed meat and 36 22 61.11% 1.6 1.2 5.6
Toddlers Netherlands VCP kids Processed meat and 322 254 78.88% 1.8 1.6 6.5
meat products, NES
Toddlers Spain enKid Processed meat and 17 13 76.47% 2.7 1.8 6.9
meat products, NES
Data on USA from FCID (2015): What We Eat In America – Food Commodity Intake Database 2005–10, United States Environmental Protection Agency – Office of Pesticide Programs
© University of Maryland 2012 – 2016. Available from: http://fcid.foodrisk.org/percentiles.php

81
at the 95th percentile ranged from 152 to 130 pg/kg bw per month at the 50th and 90th
309 g/day (FCID, 2015). percentiles, respectively. The contribution
In Europe, the mean consumption of from meat was estimated to range from 6% in
processed meat for adults was between about Asia to 23% in north America for PCDDs and
10 and 80 g/day. The consumption at the 95th PCDFs, and from 4% in Asia to 55% in north
percentile was up to 200 g/day (EFSA, 2011). America for dioxin-like PCBs (JECFA, 2002).
In the EPIC cohort, the lowest consumption Brominated flame retardants (BFRs): Food
of processed meat was found in Greece, with consumption, especially fish and meat
11 g/day for women and 19 g/day for men. The product consumption, is a major route of
highest consumption of processed meat was human contamination (Lyche et al., 2015).
found in Norway for women (48 g/day) and in For example, higher levels of PBDEs in
Germany for men (89 g/day) (Linseisen et al., humans were found in studies in the USA
2006). where fish were most highly contaminated
[The Working Group noted that despite the (median, 616 pg/g), followed by meat (median,
weaknesses of the data set, it seemed that in 190 pg/g). However, unlike many European
certain countries the consumption of processed countries where fish consumption predom-
meat is similar to the consumption of red meat inates, dietary intake of PBDEs in the USA
for consumers only. However, the percentage of is mostly from meat consumption (Schecter
consumers of processed meat seemed to be much et al., 2008).
smaller, leading to a per capita consumption four Heavy metals: The heavy metals cadmium,
to five times lower than that of red meat.] arsenic, and lead have been classified
(f) Dietary exposure to chemicals in meat as carcinogens by IARC (IARC, 2012a).
For the EU, the European Food Safety
(i) Chemicals in the environment Authority (EFSA) has estimated that average
Several chemicals classified as carcinogens by weekly dietary exposure to cadmium was
the International Agency for Research on Cancer 2.04 µg/kg bw, and at the 95th percentile,
(IARC) are present in the environment and can weekly dietary exposure to cadmium was
contaminate meat through air, water, or animal 3.66 µg/kg bw. Food consumed in larger quan-
feed. They can be generated either from indus- tities had the greatest impact on dietary expo-
trial activities or from microorganisms (IARC, sure to cadmium. This was true for the broad
2010a, b, 2012a, b, 2016). food categories of grains and grain products
Dioxin and dioxin-like compounds: The Joint (26.9%). Meat and edible offal were estimated
FAO/WHO Expert Committee on Food to contribute 7.7% of the total dietary expo-
Additives (JECFA) assessed dioxins and sure (EFSA, 2012). In 2010, JECFA estimated
related compounds in 2002. The dietary that for adults, the mean dietary expo-
exposure estimate, expressed as toxic equiva- sure to cadmium was 2.2–12 μg/kg bw per
lency factors for PCDDs and PCDFs based on month, and high-level dietary exposure to
national data, ranged from 33 to 42 pg/kg bw cadmium was 6.9–12.1 μg/kg bw per month.
per month and from 81 to 100 pg/kg bw For children aged 6 months to 12 years, the
per month at the 50th and 90th percen- mean dietary exposure to cadmium was
tiles, respectively. For coplanar PCBs, the 3.9–20.6 μg/kg bw per month. Meat was
dietary exposure estimate ranged from 9 to not part of the food groups that contributed
47 pg/kg bw per month and from 25 to significantly (40–85%) to the total dietary
82
exposure to cadmium (i.e. rice, wheat, vege- Polycyclic aromatic hydrocarbons (PAHs): In
tables, and molluscs) (JECFA, 2013). 2006, JECFA estimated the dietary exposure
Dietary exposure to inorganic arsenic was to PAHs in 18 countries, including Australia,
last evaluated by JECFA in 2011. The occur- Brazil, New Zealand, and the United
rence of total arsenic in meat ranged from Kingdom. Estimated intake of BaP ranged
0.004 to 0.78 mg/kg, and meat was not a major from < 1 to 2.0 µg/day and from 0.0001 to
contributor to dietary exposure to inorganic 0.005 µg/kg bw per day. For the other nine
arsenic (JECFA, 2011). PAHs, intake ranged from less than 1 to
Lead was last evaluated by JECFA in 2011. ~12 µg/day and from 0.0001 to 0.015 µg/kg bw
Mean dietary exposure to lead ranged from per day (WHO, 2006). Generally, despite high
0.02 to 3 μg/kg bw per day for adults, and concentrations of PAHs, meat and barbecued
from 0.03 to 9 μg/kg bw per day for children. foods were not major contributors to PAH
The contribution of meat and meat products, exposure; however, in the USA, grilled and
including offal, was estimated to be 9% of the barbecued meat was estimated to contribute
total dietary exposure to lead (JECFA, 2013). to 21% of the intake of BaP (WHO, 2006).
Cereals, vegetal oil, animal fat, and vegetal
Mycotoxins: EFSA concluded that carry-over fat contributed up to 60% to the whole food
of aflatoxin, deoxynivalenol, zearalenone, intake of PAHs, as they are major contribu-
and fumonisin to products of animal origin tors by weight to the total diet (Dennis et al.,
was very low (EFSA, 2004a, b, c, 2005c; Kan 1983).
& Meijer, 2007). Accumulation of ochratoxin
A occurred predominantly in the blood, Nitrosamines: The main sources of NOCs in
liver, and kidney. Muscle, milk, and eggs the diet are nitrite-preserved meat products
contained much lower levels of this mycotoxin (Tricker, 1997; Haorah et al., 2001). Haorah
(EFSA, 2004d). et al. (2001) reported a mean concentration
of 5.5 µmol/kg of NOCs in frankfurters, but
(ii) Chemicals from cooking practices only 0.5 µmol/kg of NOCs in fresh meat.
Acrylamide: Acrylamide may occur in
Heterocyclic aromatic amines (HAAs): No meat during cooking (Tareke et al., 2002).
international dietary exposure assessment However, meat has been estimated to be a
was available for HAAs; however, in the EPIC minor contributor, between 0.2% and 2% of
study, dietary exposure to HAAs was esti- total dietary intake (WHO, 2006).
mated in the Heidelberg cohort (Germany)
using a detailed dietary questionnaire
that assessed meat consumption, cooking 1.4 Exposure assessment and
methods, and degree of browning of the
biological markers
respective food items. Results based on total
meat consumption (including poultry meat) 1.4.1 Questionnaires
showed a total median exposure to HAAs
of 30.6 ng/day (13–71.3 ng/day) (Rohrmann A description of the epidemiological studies
et al., 2007). Other studies’ results showed a included in this Monograph, in terms of their
significantly lower dietary exposure to HAAs study design, is provided in Section 2. A review
for Europe (6.1 ng/kg bw per day) (Zimmerli of dietary assessment methodologies used in the
et al., 2001) and the USA (11.0–19.9 ng/kg bw epidemiological studies is beyond the scope of
per day) (Keating & Bogen, 2004). this Monograph (e.g. Thompson & Subar, 2013).
83
The majority of the studies used food frequency a food list for their FFQ using 3-day measured
questionnaires (FFQs) to assess individual food records that could capture 85% or more of
meat intake (including red meat and processed the intake of key nutrients and also food items
meat). FFQs are typically used in epidemio- traditionally consumed by the populations repre-
logical studies to measure usual dietary intake sented in the Multiethnic Cohort Study.
in individuals for several reasons. First, FFQs Many FFQs have been developed and adapted
are a feasible approach in case–control studies, to suit different research questions and popula-
where usual diet must be ascertained retrospec- tions. In the USA, for example, several question-
tively (often from the distant past). Second, in naires are commonly used (and are cited in this
large prospective cohort studies, FFQs can be Monograph), including:
distributed by mail or online to a large number Health Habits and History Questionnaire
of participants; are self-administered (typically); (HHHQ) or Block questionnaire (Block
may be optically scanned, computer-assisted, et al., 1986, 1990; Sobell et al., 1989): This is
or web-based; and are analysed using precoded a semiquantitative food frequency question-
foods/food groups and portion sizes. naire (SQFFQ) originally developed by the
The FFQ approach asks respondents to report National Cancer Institute (NCI). The SQFFQ
their usual frequency of consumption for each collects portion size information; however,
food from a list of foods during a specific period portion sizes are specified as standardized
of time (several months or a year). FFQs are portions or by choosing from a range of
generally used for ranking subjects according portions sizes (e.g. small, medium, or large).
to food or nutrient intake, rather than for esti- The original Block FFQ has been modified,
mating absolute levels of intake. In addition, and is continually updated by researchers to
they are widely used in case–control and cohort suit their research questions and populations.
studies to assess an association between dietary
intake and disease risk (Kushi, 1994; Beaton, Harvard FFQ or Willett questionnaire (Caan
1994; Sempos et al., 1999). et al., 1998; McCann et al., 1999): This
The ability to quantify total dietary intake FFQ was developed at Harvard University.
depends on the number of food items listed in Standard portion size defaults are included
the FFQ, on the level of detail collected within as part of the food items listed, rather than as
the questionnaire, on whether portion sizes for a separate listing.
the foods/food groups are included, and on the NCI Diet History Questionnaire (DHQ): The
timeframe of intake or reference period used. DHQ was designed with an emphasis on
For red meat and processed meat specifically, cognitive ease of use for respondents (Subar
the classifications used to define red meat and et al., 1995, 2001). It is an SQFFQ, which uses
processed meat as a food category also influence an embedded question approach, that was
the calculation of total dietary intake (Block et al. developed by NCI.
1986; Rimm et al., 1992). Definitions of red meat and processed meat as
Although food lists included in FFQs vary a food category varied across the studies included
based on the purpose of the study and the study in this Monograph. Red meat was commonly
population, the appropriateness of the food lists defined as beef, pork, lamb, or a combination
is crucial. The full variability of an individual’s thereof, and processed meat was generally
diet, which includes many foods and mixed defined as meat made largely from pork, beef, or
dishes, cannot be captured by a finite food list. poultry that undergoes methods of preservation,
Ollberding et al. (2012), for example, identified
84
such as curing, smoking, or drying (Santarelli (b) Validation and calibration

et al., 2008). While many studies explicitly The relative validity of an FFQ provides
defined these classifications (Tiemersma et al., information on how well the instrument is
2002; Ferrucci et al., 2009; Cross et al., 2010), measuring what it is intended to measure. This
other studies provided either no description or is completed by comparing intake assessed using
an unclear description of these classifications an FFQ with intake assessed using a reference
(Kato et al., 1997; Järvinen et al., 2001). The method (which is deemed to be superior) in the
level of detail collected by the epidemiological same individuals (e.g. an interviewer-led dietary
studies, in terms of meat intake, varied widely. history or multiple 24-hour recalls). FFQs may
Most studies reported the association between often be validated for their ability to assess total
categories of meat intake labelled “red meat” energy intake in comparison with the doubly
or “processed meat” and cancer risk; however, labelled water technique (Hill & Davies, 2001).
several studies reported results for individual The superior method is often prohibitive for use
red meat items (e.g. beef or pork) (Brink et al., in large epidemiological studies due to partici-
2005; Norat et al., 2005; Sato et al., 2006; Takachi pant burden, or overall cost of administering and
et al., 2011; Egeberg et al., 2013) and/or processed coding the instrument. Calibration studies are
meat items (e.g., hot dogs or bacon). The studies used to calibrate an FFQ to a reference method
that included detailed information on the intake using a regression model. Many of the studies
of specific processed meat items were superior to included in this Monograph used various statis-
those that combined generic items into one food tical methods, employing measurement error
group or one-line items (e.g. “processed meat”), models and energy adjustment to assess the
as the amount of nitrate, nitrite, and haem iron validity of the FFQs and to adjust estimates of the
in processed foods can vary dramatically. relative risks for disease outcomes (Bingham &
(a) Portion size Day, 1997; Kipnis et al., 1997; Carroll et al., 1998;
Hu et al., 1999). For example, in the National
Scientists have used many methods to Institutes of Health – American Association of
improve assessment of portion size in the studies Retired Persons (NIH-AARP) Diet and Health
included in this report. For example, Pietinen Study, the FFQ used was calibrated against two
et al. (1999) included a portion size booklet of non-consecutive 24-hour dietary recalls (Cross
122 photographs of foods, each with three to et al., 2010). In the EPIC study, investigators used
five different portion sizes. In the Canadian a computerized 24-hour dietary recall method to
National Breast Screening Study (CNBSS), Kabat calibrate dietary measurements across countries
et al. (2007) also included photographs of portion and to correct for systematic over- or underes-
sizes to improve portion size assessment. In timation of dietary intake (Norat et al., 2005;
the Finnish Mobile Clinic Health Examination Pala et al., 2009). Tiemersma et al. (2002) vali-
Survey, Järvinen et al. (2001) used plastic food dated their short SQFFQ using a dietary history
models and real foods to help estimate portion method, which is a robust, interviewer-admin-
sizes for their interviewer-assisted FFQ. Dixon istered dietary assessment method. Each study
et al. (2004) also used three-dimensional food included in this Monograph was examined to
models, plastic cups, and spoons to help partic- determine whether the FFQ used to assess red
ipants identify usual serving sizes in the Kaiser meat and processed meat exposure had been
Permanente Medical Care Program in northern validated (see Section 2).
California, USA.
85
(i) Heterocyclic aromatic amines correlation coefficients of HAA intake, assessed

Assessment of dietary HAA intake is chal- using the FFQ and food diaries, were 0.43 (95%
lenging, as HAA concentrations vary greatly confidence interval, CI, 0.30–0.55) for MeIQx
according to cooking technique, temperature, intake and 0.22 (95% CI, 0.07–0.36) for PhIP
cooking time, and meat type (Sinha et al., intake. Deattenuated correlations were 0.60
1995; Knize et al., 1998; Sinha et al., 1998a, b). (95% CI, 0.49–0.69) and 0.36 (95% CI, 0.22–0.49),
Epidemiological studies have tried to overcome respectively (Cantwell et al., 2004). This meat-
these difficulties using surrogate markers of cooking module has been used in the Prostate,
HAA intake, such as method of cooking, surface Lung, Colorectal and Ovarian (PLCO) Cancer
browning, total cooking time, and gravy intake. Screening Trial (Cross et al., 2005), Nurses’
To estimate the intake of these cooked meat Health Study (NHS) (Wu et al., 2010), Health
mutagens, a detailed meat-cooking module was Professionals Follow-Up Study (HPFS), and
developed. The meat-cooking module was a modi- other studies (Cantwell et al., 2004).
fied version of the 1992, 100-item, self-adminis- (ii) Nitrate and nitrite
tered HHHQ to assess usual dietary intake over Dietary assessment of nitrate and nitrite
the past year (Block et al., 1986). An interview- intake was reported by the NIH-AARP Diet and
er-administered questionnaire on meat-cooking Health Study (Dellavalle et al., 2013). The base-
practices was also used to assess the consumption line questionnaire included an FFQ that asked
of 23 meat, poultry, and fish items using a matrix participants about their frequency of consump-
similar to the 100-item HHHQ. The question- tion and portion sizes of 124 food items over the
naire collected information on cooking methods; past 12 months. Intake of each item was assessed
embedded questions assessed how well the meat using 10 predefined categories, ranging from
was cooked. Portion size was estimated as small, “never” to “≥ 2 times per day” for foods, “never”
medium, or large, relative to the standard portion to “≥ 6 times per day” for beverages, and three
size indicated for each food listed in the ques- portion size categories. The FFQ was developed
tionnaire and meat-cooking module. A mutagen and validated by NCI using two 24-hour recalls
database, called Computerized Heterocyclic in a subset of the cohort (Thompson et al., 2008).
Amines Resource for Research in Epidemiology Concentrations of nitrate and nitrite for each
of Disease (CHARRED), developed by NCI/ food item were estimated from the existing body
NIH (NCI, 2017) was used to estimate the intake of scientific literature, as previously described
of mutagenic compounds from cooked meats. (Ward et al., 2003, 2006; Kilfoy et al., 2011). Daily
The CHARRED database estimates the HAA intake of nitrate and nitrite was calculated by
content of commonly consumed meats, based multiplying the frequency of consumption by the
on detailed information about the meat-cooking portion size and the nitrate and nitrite content
methods used and meat-doneness level. The rela- of each food item, and then summing across
tive validity of this meat-cooking module has all food items. Nitrate and nitrite intake from
been measured using multiple food diaries (three animal sources and plant sources was calculated
of four non-consecutive day diaries completed separately. In addition to examining nitrate and
over a 3-month period) as the reference method nitrite intake from all animal sources, intake
(Cantwell et al., 2004). Dietary intake of the from processed meat sources was examined
three most abundant HAAs was considered: separately, as were animal sources excluding
MeIQx, 2-amino-3,4,8-trimethylimidazo[4,5-f] processed meat (this primarily included intake
quinoxaline (4,8-DiMeIQx), and PhIP. Crude
86
from fresh meats, eggs, yogurt, cheese, and other (d) Cohort studies
dairy products). A major strength of cohort studies in nutri-
The nitrate and nitrite content of over 3000 tional epidemiology is their ability to demon-
foods was determined by conducting a review strate a temporal relationship between dietary
of the literature, focusing on Canadian and exposure and cancer risk, as all dietary assess-
USA foods, and by calculating the means of the ments are completed before diagnoses. This limits
published values weighted by the number of difficulties with recall bias and reverse causation.
samples analysed (Ward et al., 2003, 2006; Kilfoy Wei et al. (2004) used a validated, self-ad-
et al., 2011). The nitrate and nitrite values for foods ministered, 61-item SQFFQ at baseline in 87 733
constituting an FFQ line item were combined by women from the NHS and a validated, self-ad-
weighting the food-specific values by sex-specific ministered, 131-item SQFFQ in 46 632 men from
intake amounts from the 1994–1996 Continuing the HPFS. The study had several strengths. For
Survey of Food Intakes by Individuals (CSFII) example, the FFQs used were extensively vali-
(Subar et al., 2000). For example, the nitrate dated and tested for reproducibility using data
content of a line item was calculated using the collected from a subgroup of participants who
weighted average of the nitrate content of the completed two FFQs (1 year apart) and two
included foods, where the weights were deter- 1-week diet records (6 months apart during the
mined by intake amounts from the CSFII, based intervening year). The association between base-
on age group and sex. Daily intake of nitrate line meat intake and cancer risk was assessed in
and nitrite was calculated by multiplying the this study, and red meat intake was clearly defined
frequency of consumption of each line item by as the consumption of beef, pork, or lamb as a
its nitrate or nitrite content and summing over main dish. In addition, in this combined cohort
line items. In addition to calculating nitrate and of women and men, risk estimates were adjusted
nitrite intake from all foods, nitrite intake from using a multivariate model that included impor-
plant, animal, and processed meat sources was tant confounders (age; family history; body mass
calculated separately. index, BMI; physical activity; beef, pork, or lamb
(c) Heterogeneity across studies as a main dish; processed meat; alcohol; calcium;
folate; height; smoking pack-years before aged
There was substantial heterogeneity across 30 years; history of endoscopy; and sex). A limi-
the studies included in this Monograph due to tation of this study was the quantification of red
a variety of factors, such as different methods of meat in servings per day only (i.e. not in g/day).
dietary assessment and/or measurement, defini- In the Physicians’ Health Study (PHS), Chen
tions (e.g. food groups and serving sizes), analyt- et al. (1998) used a nested case–control design to
ical categorizations (e.g. servings/week and assess the relationship between red meat intake
g/day), exposure contrasts (e.g. analytical and colorectal cancer by N-acetyltransferase
cut-points and intake level comparisons), and (NAT) genotype. The study included 212 men
degrees of adjustment for potential confounding who were recruited as part of the Physicians’
factors. Each cohort study included in this Health Study and were subsequently diagnosed
Monograph is described in Section 2. The with colorectal cancer or rectal cancer during
strengths and limitations of the questionnaires 13 years of follow-up and were genotyped via
used in studies included in this Monograph are baseline blood sample, along with 221 controls.
outlined below. At baseline, participants completed an abbre-
viated, self-administered FFQ, which inquired
87
about usual consumption of red meat (beef, of meat, but also was calibrated within this study
pork, or lamb as a main dish, as a mixed dish population using two non-consecutive 24-hour
or sandwich, and as hot dogs), chicken, and fish. dietary recalls. However, there was overlap in the
The abbreviated FFQ used in this study was not definitions of red meat and processed meat, as
validated, but an expanded form of this FFQ was some processed meat items were classified as red
validated among other male health professionals. meat.
There were some limitations to this study, as the In the EPIC study (Norat et al., 2005), dietary
use of an abbreviated FFQ (with fewer food items intake over the 12 months before enrolment was
listed) prevented the adjustment of risk estimates measured by country-specific, validated dietary
for total energy intake. In addition, dietary intake questionnaires (88–266 food items, depending
of processed meat was included with red meat on the country), which were self-administered in
intake, and meat intake was assessed as servings most countries; in Malmö, Sweden, a question-
per day only (i.e. not in g/day). naire combined with a food record was used. A
Dietary assessment in the NIH-AARP Diet second dietary measurement was taken from an
and Health Study was described in detail by 8% random sample of the cohort (36 994 partic-
Cross et al. (2010). The study included approx- ipants) using a computerized 24-hour dietary
imately half a million women and men, each recall method to calibrate dietary measurements
of whom completed a validated, self-adminis- across countries and to correct for systematic
tered, 124-item FFQ at baseline. Approximately over- or underestimation of dietary intake. The
6 months later, cancer-free participants were major strengths of this study were the large vari-
mailed a risk factor questionnaire, which detailed ability in dietary intake across the population
information on meat intake and cooking pref- and the use of a computerized 24-hour dietary
erences. Meat cooking method (grilled/barbe- recall method to calibrate dietary measurements
cued, pan-fried, microwaved, and broiled) and across countries.
doneness level (well done/very well done and In the Alpha-Tocopherol, Beta-Carotene
medium/rare) were used in conjunction with Cancer Prevention (ATBC) Study, researchers
the CHARRED database to estimate the intake used a self-administered, modified dietary
of several HAAs. The FFQ assessed the usual history method to capture usual dietary intake
frequency of consumption and portion size 12 months before recruitment. The dietary
information of foods and drinks over the past history method included 276 food items and a
12 months. All types of beef, pork, and lamb portion size booklet of 122 photographs of foods,
were considered red meat, including bacon, beef, each with 3–5 different portion sizes. Red meat
cold cuts, ham, hamburger, hot dogs, liver, pork, intake was defined as intake of beef, pork, or
sausage, and steak. Processed meat included lamb (Pietinen et al., 1999). A major strength of
bacon, cold cuts (red and white meat), ham, this study was the use of a detailed questionnaire.
luncheon meats (red and white meat), poultry In the Multiethnic Cohort Study, Ollberding
sausage, red meat sausage, and standard hot et al. (2012) assessed diet using a validated
dogs and low-fat hot dogs made from poultry. quantitative FFQ, which included a list of foods
Meats added to complex food mixtures, such as identified from 3-day measured food records, to
pizza, chilli, lasagne, and stew, contributed to capture 85% or more of the intake of key nutri-
the relevant meat type. There were many notable ents and food items traditionally consumed by
strengths to this study. Several of these strengths the populations represented in the cohort. The
were related to the FFQ, which not only contained definition of meat intake was clearly defined as
detailed questions pertaining to the components total meat, red meat, and processed meat. Risk
88
estimates were adjusted for important potential FFQ was not very extensive, and there were no
confounders, including energy intake. This study quantitative data on red meat intake provided.
had many strengths, including a large variability It is also unclear whether intake of red meat
in diet due to the inclusion of multiple ethnicities included processed meat.
and the use of an extensive dietary questionnaire. A study by Tiemersma et al. (2002) in the
The PLCO Cancer Screening Trial (Ferrucci Netherlands examined the association between
et al., 2009) used an NCI DHQ to assess usual meat intake and cancer risk using a nested case–
intake (both frequency and portion size) of 124 control design. A strength of this study was
food items over the past year. The definition of the use of an SQFFQ, which was validated for
red meat (g/day) included bacon, beef, cheese- use through comparison with a dietary history
burger, cold cuts, ham, hamburger, hot dogs, liver, method. A limitation of this study, however, was
pork, sausage, veal, venison, and red meat from that a major source of meat in the population (i.e.
mixed dishes. Processed meat included bacon, a mixture of pork and beef) was not captured by
cold cuts, ham, hot dogs, and sausage. However, the FFQ.
a limitation of this study was the clear overlap in In the Shanghai Women’s Health Study, Lee
the definitions of red meat and processed meat, et al. (2009) assessed dietary intake at base-
as some processed meat items were classified as line using a validated quantitative FFQ, which
red meat. included 19 food items/groups of animal origin.
Flood et al. (2003) used a 62-item NCI A major strength of this study was that the FFQ
Block FFQ in the Breast Cancer Detection was administered by interview.
Demonstration Project (BCDDP) to assess red In the prospective cohort study of 37 112
meat intake in the previous year. A limitation of residents of Melbourne, Australia, English et al.
this study was the combined estimate of exposure (2004) assessed dietary intake using a 124-item
to meat, which included pork, beef, hamburger, FFQ. They also provided a clear definition of
processed meat, and liver, so risk estimates for what they included in terms of fresh red meat
red meat alone or processed meat alone were not (veal, beef, lamb, pork, rabbit, or other game). A
possible. As the cohort was generated based on limitation of this study, however, was that portion
a screening programme, participants may have size was not measured.
changed their dietary habits before baseline, and In the Iowa Women’s Health Study, (Lee et al.,
recorded intake may therefore not have accu- 2005) assessed usual dietary intake over the past
rately reflected long-term intake. year using a validated, 127-item, self-adminis-
Singh & Fraser (1998) assessed dietary intake tered SQFFQ virtually identical to the question-
in the Adventists Health Study cohort using a naire used in the 1984 survey of the NHS (Bostick
self-administered, mailed, 55-item SQFFQ. The et al., 1994). Red meat was defined as beef, pork,
SQFQQ included just six questions regarding red or lamb as a main dish. This study had several
meat intake, defined as current intake of beef or strengths, including assessment of reliability and
pork. A limitation of this study was the relatively accuracy of the FFQ used, which was comparable
short dietary questionnaire in a low-risk popula- to what was observed in the NHS. The exten-
tion, with low red meat consumption. sive FFQ allowed for multivariable adjustment,
In the New York University Women’s Health including age, total energy intake, height, parity,
Study, Kato et al. (1997) assessed red meat intake total vitamin E intake, interaction term vitamin
using a 70-item FFQ, which was slightly modi- E *age, and vitamin A supplement use.
fied from the questionnaire designed by Block
and coworkers (Block et al., 1986). However, the
89
(e) Case–control studies 1.4.2 Biological markers

A description of the case–control studies Despite more than 35 years of research, no
included in this Monograph is provided in long-term validated biomarkers of exposure
Section 2. Case–control studies investigating have been employed in molecular epidemi-
the association between meat intake and cancer ology studies to assess the role of genotoxicants
risk are limited, as they assess dietary intake in cooked or processed meat and cancer risk.
after cancer has been diagnosed, which can lead Additionally, other than HAAs, the biomarkers
to recall bias. In addition, patients often change of PAHs or NOCs are not specific to meat, as
their dietary intake due the presence of a solid they may also measure environmental or endog-
tumour to avoid pain or reflux, for example. As a enous exposure.
result, investigators usually ask cases included in [The Working Group noted that short-lived
their studies to recall dietary intake in the period biomarkers, including urinary metabolites
before diagnosis of cancer to capture usual diet and DNA adducts of meat-related genotoxi-
before diagnosis. As a result, case–control studies cants, exist; however, they cannot be used as
are limited due to the measurement error asso- biomarkers of exposure in epidemiological
ciated with dietary intake due to memory recall. studies, and do not belong in this section
Tavani et al. (2000), for example, assessed total (see Section 4 for details).]
red meat intake (beef, veal, and pork) per week The accumulation of PhIP in hair may
2 years before diagnosis, while Chiu et al. (2003) represent the first long-term biomarker of
assessed dietary intake 5 years before diagnosis HAA exposure in cooked meats, although this
in a case–control study in Shanghai. biomarker is a measure of the unmetabolized
In the North Carolina Colon Cancer Study, chemical and not the biologically effective dose.
Butler et al. (2003) assessed usual diet in the Harmonization of the method across laborato-
year before diagnosis for patients, or the year ries is required for validation and implementa-
before the date of selection for controls, using a tion in epidemiological studies.
150-item FFQ, which was a modified version of Recent studies of omnivores have used
the Block questionnaire. However, no informa- metabolomics to identify constituents of meat
tion regarding validation was provided. Red meat in plasma and urine to measure meat consump-
intake was calculated as the sum of hamburger, tion. Metabolomics is still a developing tech-
steak, pork chop, sausage, and bacon intake. nology. It employs liquid chromatography-mass
spectrometry (LC-MS)–based methods to iden-
(f) Conclusion tify the constituents or chemicals present in
As outlined in this section, the question- cooked or processed meat, and may provide reli-
naires used in the cohort and case–control able assessment of dietary habits and patterns of
studies varied in several ways, including in the meat consumption in the future.
methods of dietary assessment and/or measure- Data on the most promising biomarkers
ment, the use of validated/calibrated question- of exposure for red meat and processed meat
naires, the definitions of meat and processed consumption in epidemiological studies are
meat as food groups, the inclusion of serving or summarized in Section 1.4.2(a) and (b).
portion sizes, the ability to assess intake (i.e. in
g/day), and the degree of adjustment for poten-
tial confounding factors.
90
(a) Hair biomarkers less efficiently to hair, and exposure cannot be

Gas chromatography-mass spectrometry assessed with hair (Bessette et al., 2009; Iwasaki
(GC-MS) with negative ion chemical ioniza- et al., 2014).
tion or liquid chromatography-tandem mass There are reports on the measurement by
spectrometry (LC-MS/MS) with triple quadru- GC-NICI/MS of hydroxylated PAHs, including
pole-mass spectrometry (TQ-MS) instruments naphthalene and pyrene, in the hair of subjects
have been employed to measure PhIP in the hair (Schummer et al., 2009; Appenzeller et al., 2012;
of subjects in European countries (Alexander Appenzeller & Tsatsakis, 2012). Using hair to
et al., 2002), Japan (Kobayashi et al., 2005; assess exposure to PAHs through meat consump-
Kobayashi et al., 2007; Iwasaki et al., 2014), and tion is challenging because of the multiple
the USA (Bessette et al., 2009; Turesky et al., sources of exposure to PAHs and the low levels
2013). PhIP was identified in the hair of omni- of hydroxylated PAHs in hair.
vores, but not in the hair of vegetarians (Bessette (b) Urinary and plasma biomarkers
et al., 2009). The binding of PhIP to hair is
strongly driven by melanin content, and binding Targeted approaches have been used to
levels of PhIP in hair should be normalized to measure different procarcinogens, their metab-
melanin content (Bessette et al., 2009; Turesky olites, and DNA adducts in urine. More recently,
et al., 2013). Turesky et al. (2013) observed that, untargeted metabolomics approaches have been
after being fed a semicontrolled diet, levels of used to understand dietary patterns of meat
PhIP in the hair of volunteers increased in an consumption, to strengthen self-administered
exposure-dependent manner. Levels of PhIP in FFQs.
hair were stable over time, varying in two meat (i) Metabolomics: nutrients and secondary or
eaters by less than 24% over a 6-month interval indirect biomarkers
(Turesky et al., 2013). In another study, levels of Plasma and urine from subjects on different
PhIP in the hair of Japanese subjects were corre- diets have been characterized by proton nuclear
lated with grilled/stir-fried meat intake, but not magnetic resonance, GC-MS, and LC-MS tech-
with grilled/stir-fried fish intake (Kobayashi niques, and hundreds of chemicals have been
et al., 2005). Levels of PhIP were further corre- identified (Puiggròs et al., 2011; Hedrick et al.,
lated with dietary HAA intake, according to 2012; Scalbert et al., 2014).
an FFQ (Kobayashi et al., 2007). Since the Correlations were observed among chem-
binding of PhIP to hair is largely influenced ical biomarkers of red meat, shellfish, fish, other
by pigmentation, the biomonitoring of PhIP in food components, multivitamins, and diets, in
an older population with predominantly white plasma (Guertin et al., 2014). Several biomarkers
hair may be difficult. Moreover, because the in urine correlated to meat intake included:
growth cycles of individual hair follicles are creatine, creatinine, carnitine, carnosine, ophi-
asynchronous across the scalp, hair samples dine, 1-methylhistidine, and 1-methylhistidine
should be consistently collected from the same and 3-methylhistidine (Dragsted, 2010; Puiggròs
area of the scalp for comparison of PhIP levels et al., 2011).
in the hair of individuals (Bessette et al., 2009; In a urinary metabolomic study employing
Turesky et al., 2013). Despite these limitations, LC-MS, 3-indoleacetyl-glucuronide, a micro-
biomonitoring of PhIP levels in hair is the first biome metabolite of tryptophan, which is found
biomarker for assessing long-term exposure to at high concentrations in animal protein, was
this cooked meat carcinogen. Other HAAs bind identified, possibly reflecting differences in the
91
protein sources between the diets (Andersen formed during muscle catabolism, thus lack
et al., 2014). Indole propionate was also identified specificity for meat intake. 1-Methylhistidine has
as a potential biomarker of red meat in plasma also been found in the urine of subjects on a fish
(Guertin et al., 2014). Indoles are metabolites diet (Lloyd et al., 2011). Another study reported
of tryptophan that are largely produced by the that the mean urinary levels of 1-methylhisti-
bacterial flora; however, they are not specific to dine and 3-methylhistidine did not differ among
meat, as they are also found in high amounts in 131 colorectal adenoma and control subjects
soya and eggs (Guertin et al., 2014). (P = 0.72) (Cross et al., 2014). Thus, methyl-
histidine may not be a good indicator of meat
(ii) Urinary 1-methylhistidine,
processing conditions, and the levels of methyl-
3-methylhistidine, creatinine, and taurine
histidine present in meat may not correlate to
There were marked differences between the the levels of procarcinogens formed in cooked or
proton nuclear magnetic resonance spectra of processed meat.
high–red meat, low–red meat, and vegetarian To date, there are no chemical markers or
diets, which included elevated urinary levels metabolites of meat constituents that can provide
of creatinine, taurine, carnitine, trimethyl- information on the methods of meat processing
amine-N-oxide, and methylhistidine in the high– and cooking that produce carcinogens.
red meat group. However, the spectral changes
differentiating the low–red meat and vegetarian
groups were subtle. The urinary metabolite 1.5 Regulations and guidelines
trimethylamine-N-oxide, a product formed from
In many countries, the production of red
carnitine by the bacterial microbiota, was associ-
meat and processed meat is subject to stringent
ated with meat intake, but it is also a biomarker
regulations. These regulations are primarily
of fish intake, and may confound the interpreta-
intended to prevent infectious diseases and
tion of meat consumption patterns (Stella et al.,
minimize contamination of the meat prod-
2006).
ucts. Under the auspices of WHO and FAO, the
In another controlled meat-feeding study,
Codex Alimentarius was established to provide
the urinary excretion of creatinine, taurine,
international food standards, guidelines, and
1‑methylhistidine, and 3-methylhistidine was
codes of practice to protect and promote safety,
investigated in individuals who consumed
quality, and fairness in the international food
various amounts of red meat: vegetarian (0 g/
trade (Codex Alimentarius, 2015). The scope of
day), low red meat (60 g/day), medium red meat
standards issued by the Codex Alimentarius is
(120 g/day), and high red meat (420 g/day)
illustrative of standards and regulatory meas-
(Cross et al., 2011). All components demon-
ures typically issued on a national basis for the
strated a significant dose–response relationship,
maintenance of food safety in relation to meat
increasing as red meat intake increased (Ptrend
products (Table 1.18).
< 0.0001). There were significant differences in the
An exhaustive list of all regional and national
mean levels of 1-methylhistidine and 3-methyl-
food authorities is not provided here, but a
histidine across the four dietary intake groups
summary of those operating in Europe and the
(P < 0.01 and P < 0.05, respectively). However,
USA is provided.
taurine and creatinine levels in the vegetarian
EFSA (EFSA, 2015) is the EU risk assessment
and low–red meat intake groups could not be
authority for food and feed safety. For red meat
distinguished (P = 0.95 and P = 0.88, respec-
and processed meat, relevant EFSA panels or units
tively). 3-Methylhistidine and creatinine are
include animal health and welfare, biological
92
Table 1.18 Examples of meat-related food safety standards issued by Codex Alimentarius
Reference Standard Committee Last

modified
CAC/GL 14-1991 Guide for the Microbiological Quality of Spices and Herbs Used in CCPMPP 1991
Processed Meat and Poultry Products
CAC/GL 78-2011 Guidelines for the Control of Campylobacter and Salmonella in Chicken CCFH 2011
Meat
CAC/GL 85-2014 Guidelines for the Control of Taenia saginata in Meat of Domestic Cattle CCFH 2014
CAC/GL 86-2015 Guidelines for the Control of Trichinella spp. in Meat of Suidae CCFH 2015
CAC/GL 87-2016 Guidelines for the Control of Nontyphoidal Salmonella spp. in Beef and CCFH 2016
Pork Meat
CAC/RCP 58-2005 Code of Hygienic Practice for Meat CCMPH 2005
CODEX STAN 89-1981 Standard for Luncheon Meat CCPMPP 2015
CODEX STAN 98-1981 Standard for Cooked Cured Chopped Meat CCPMPP 2015
CCFH, Codex Committee on Food Hygiene; CCMPH, Codex Committee on Meat Hygiene; CCPMPP, Codex Committee on Processed Meat
and Poultry Products
From Codex Alimentarius (2016a)
monitoring, contaminants, and assessment and of other foods and water with enteric pathogens
methodological support. of animal origin (Sofos, 2008).
In the USA, the relevant statutory authority Many countries approach food safety, specif-
for safety in relation to meat products is the United ically in relation to meat production, through
States Department of Agriculture (Department compliance with hazard analysis and critical
of Agriculture, 2015). The United States Food control point (HACCP)-based regulations;
and Drug Administration (FDA) is responsible HACCP is a safety and quality management tool
for regulating chemicals authorized in meat. A (Hudson et al., 1996).
range of guidance documents and regulations
are issued by this administration (FDA, 2015). 1.5.2 Prevention of contamination
(a) Red meat
1.5.1 Prevention of infectious disease
Red meat may contain residues from veter-
The broad issues addressed by food safety inary drugs. These compounds are generally
regulations have been summarized by Henson & regulated at the national level, but 67 of them
Caswell (1999), and include new potential food- are regulated by international standards (i.e.
borne risks, such as bovine spongiform enceph- maximum residue limits, MRLs) established by
alopathy and genetically modified organisms, the Codex Alimentarius (2015). There is currently
as well as recognized risks posed by well-char- no international monitoring of the frequency of
acterized bacteria. The scientific rationale for use of these chemicals.
food safety regulations involves risk assessment, Red meat is usually free of additives.
management, and communication. However, in certain circumstances, colours are
For meat products, the regulations aim to used for certification stamps on the surfaces
decrease contamination by microbial pathogens of fresh cuts of meat, and are indicated in
(e.g. Listeria monocytogenes, Escherichia coli, and the food category system with a notation for
Salmonella) by minimizing cross-contamination “stamping, marking or branding the product”
(Codex Alimentarius, 2016a).
93
Red meat may also contain chemicals present resulting from the processing of meat or from the
in the environment or used in the production further processing of such processed products,
of feed-like pesticide residues. When there so that the cut surface shows that the product
is sufficient scientific information available no longer has the characteristics of fresh meat”
about a chemical, the Joint FAO/WHO Expert (European Commission, 2004).
Committee defines its acceptable daily intake At the international level, there is currently
(ADI), which is the amount of chemical, expressed no active committee of the Codex Alimentarius
based on body weight, that can be ingested over to deal with meat (abolished in 1971) or processed
a lifetime without appreciable health risks. From meat (abolished in 1990), and the international
the ADI, the Codex Alimentarius Commission standards for meat products are established by
establishes an MRL per kilogram of food that is horizontal committees (e.g. committees for food
recommended as being legally acceptable. The additives, contaminants, or pesticide residues).
Codex Alimentarius Commission does not estab- In addition to the chemicals possibly present in
lish an MRL for a chemical if dietary exposure is meat in general, processed meat may contain food
above the ADI. Furthermore, no MRL is estab- additives. However, many of these food additives,
lished if a chemical is assessed to be a genotoxic such as nitrites (80 mg/kg), colouring agents
carcinogen in humans (Codex Alimentarius, such as erythrosine (30 mg/kg), and antioxidants
2015). MRLs have been established by the Codex including butylated hydroxytoluene (100 mg/kg)
Alimentarius for several pesticide residues are regulated by international standards estab-
possibly occurring in meat (Codex Alimentarius, lished by the Codex Alimentarius (2016a).
2016b). Most of these limits were established at
the limit of detection of the analytical method.
Other chemical contaminants present in the References
environment, such as heavy metals or persistent
organic pollutants, may also occur in red meat. Afshin A, Micha R, Khatibzadeh S, Fahimi S, Shi P, Powles
Some of these contaminants are regulated inter- J et al.; 2010 Global Burden of Diseases, Injuries, and
Risk Factors Study: NUTRItrition and ChrOnic
nationally by the Codex Alimentarius. WHO/ Diseases Expert Group (NUTRICODE), and Metabolic
GEMS has collected national monitoring data Risk Factors of ChrOnic Diseases Collaborating Group
on 145 environmental contaminants (WHO, (2015). The impact of dietary habits and metabolic
2015b). Moreover, the Codex Alimentarius risk factors on cardiovascular and diabetes mortality
in countries of the Middle East and North Africa in
has adopted codes of practice to reduce food 2010: a comparative risk assessment analysis. BMJ
and feed contamination by lead (Codex Open, 5(5):e006385. doi:10.1136/bmjopen-2014-006385
Alimentarius, 2004), by dioxin and dioxin-like PMID:25995236
AFSSA (2005). Avis de l’Agence française de sécurité sani-
PCBs (Codex Alimentarius, 2006), and by PAHs taire des aliments relatif à l’évaluation de l’exposition
(Codex Alimentarius, 2009). de la population française aux dioxines, furanes et PCB
de type dioxine. Saisine No.2005-SA-0372. Maisons-
(b) Processed meat Alfort, France: l’Agence française de sécurité sanitaire
des aliments. [French]
National regulations are in place for processed Alaejos MS, Afonso AM (2011). Factors that affect
meat in many countries around the world, e.g. in the content of heterocyclic aromatic amines in
the USA (Office of the Federal Register, 2015). In foods. Comp Rev Food Sci Food Safe, 10(2):52–108.
doi:10.1111/j.1541-4337.2010.00141.x
Europe, the European Parliament and the Council Alexander J, Reistad R, Hegstad S, Frandsen H,
of the EU define a “meat product” in Annex I to Ingebrigtsen K, Paulsen JE et al. (2002). Biomarkers
Regulation (EC) No 853/2004. The annex states of exposure to heterocyclic amines: approaches to
that “meat products” means processed products
94
improve the exposure assessment. Food Chem Toxicol, Balogh Z, Gray JI, Gomaa EA, Booren AM (2000).
40(8):1131–7. doi:10.1016/S0278-6915(02)00053-4 Formation and inhibition of heterocyclic aromatic
PMID:12067575 amines in fried ground beef patties. Food Chem Toxicol,
Alomirah H, Al-Zenki S, Al-Hooti S, Zaghloul S, 38(5):395–401. doi:10.1016/S0278-6915(00)00010-7
Sawaya W, Ahmed N et al. (2011). Concentrations and PMID:10762724
dietary exposure to polycyclic aromatic hydrocarbons Barnes K, Collins T, Dion S, Reynolds H, Riess H, Stanzyk
(PAHs) from grilled and smoked foods. Food Contr, A et al. (2012). Importance of cattle biodiversity and
22(12):2028–35. doi:10.1016/j.foodcont.2011.05.024 its influence on the nutrient composition of beef. Anim
American Institute for Cancer Research/World Cancer Front, 2(4):54–60. doi:10.2527/af.2012-0062
Research Fund (1997). Food, nutrition, and the preven- Bax ML, Aubry L, Ferreira C, Daudin JD, Gatellier P,
tion of cancer: a global perspective. Washington (DC), Rémond D et al. (2012). Cooking temperature is a
USA: American Institute for Cancer Research. key determinant of in vitro meat protein digestion
Andersen MB, Rinnan Å, Manach C, Poulsen SK, Pujos- rate: investigation of underlying mechanisms. J Agric
Guillot E, Larsen TM et al. (2014). Untargeted metab- Food Chem, 60(10):2569–76. doi:10.1021/jf205280y
olomics as a screening tool for estimating compliance PMID:22335241
to a dietary pattern. J Proteome Res, 13(3):1405–18. Bax ML, Buffière C, Hafnaoui N, Gaudichon C, Savary-
doi:10.1021/pr400964s PMID:24444418 Auzeloux I, Dardevet D et al. (2013). Effects of meat
ANSES (2011). Etude de l’alimentation totale française 2 cooking, and of ingested amount, on protein digestion
(EAT 2). Avis de l’ANSES, rapport d’expertise. Résidus speed and entry of residual proteins into the colon: a
de pesticides, additifs, acrylamide, hydrocarbures study in minipigs. PLoS One, 8(4):e61252 doi:10.1371/
aromatiques polycycliques. Maisons-Alfort, France: journal.pone.0061252 PMID:23593443
Agence nationale de sécurité sanitaire de l’alimenta- Beaton GH (1994). Approaches to analysis of dietary data:
tion, de l’environnement et du travail. [French] relationship between planned analyses and choice of
ANSES (2012). Avis de l’Agence nationale de sécurité sani- methodology. Am J Clin Nutr, 59(1):Suppl: 253S–61S.
taire de l’alimentation, de l’environnement et du travail PMID:8279436
relatif aux analyses de retardateurs de flamme bromés Bender A (1992). Meat and meat products in human
(RFB) à mettre en œuvre dans le cadre des prochains nutrition in developing countries. Food & Nutrition
plans de surveillance. Avis de l’Anses - Saisine No. 2010- Paper (Vol. 53). Rome, Italy: Food and Agriculture
SA-0225. Maisons-Alfort, France: Agence nationale de Organization of the United Nations. Available from:
sécurité sanitaire de l’alimentation, de l’environnement http://www.fao.org/docrep/T0562E/T0562E00.HTM
et du travail. [French] Bessette EE, Yasa I, Dunbar D, Wilkens LR, Le Marchand
Appenzeller BM, Mathon C, Schummer C, Alkerwi A, Lair L, Turesky RJ (2009). Biomonitoring of carcinogenic
ML (2012). Simultaneous determination of nicotine and heterocyclic aromatic amines in hair: a validation
PAH metabolites in human hair specimen: a potential study. Chem Res Toxicol, 22(8):1454–63. doi:10.1021/
methodology to assess tobacco smoke contribution in tx900155f PMID:19588936
PAH exposure. Toxicol Lett, 210(2):211–9. doi:10.1016/j. Bingham SA, Day NE (1997). Using biochemical markers
toxlet.2011.11.022 PMID:22155355 to assess the validity of prospective dietary assessment
Appenzeller BM, Tsatsakis AM (2012). Hair analysis for methods and the effect of energy adjustment. Am J Clin
biomonitoring of environmental and occupational Nutr, 65(4):Suppl: 1130S–7S. PMID:9094909
exposure to organic pollutants: state of the art, critical Block G, Hartman AM, Dresser CM, Carroll MD,
review and future needs. Toxicol Lett, 210(2):119–40. Gannon J, Gardner L (1986). A data-based approach to
doi:10.1016/j.toxlet.2011.10.021 PMID:22079616 diet questionnaire design and testing. Am J Epidemiol,
Asgar MA, Fazilah A, Huda N, Bhat R, Karim AA (2010). 124(3):453–69. PMID:3740045
Nonmeat protein alternatives as meat extenders and Block G, Woods M, Potosky A, Clifford C (1990). Validation
meat analogs. Comp Rev Food Sci Food Safe, 9(5):513– of a self-administered diet history questionnaire using
29. doi:10.1111/j.1541-4337.2010.00124.x multiple diet records. J Clin Epidemiol, 43(12):1327–35.
Awadt WA, Ghareeb K, Bohm J (2012). Occurrence, health doi:10.1016/0895-4356(90)90099-B PMID:2254769
risks and methods of analysis for aflatoxins and ochra- Bostick RM, Potter JD, Kushi LH, Sellers TA, Steinmetz
toxin A. J Vet. Anim Sci, 2(1):1–10. KA, McKenzie DR et al. (1994). Sugar, meat, and fat
Back YM, Lee JH, Shin HS, Lee KG (2009). Analysis of intake, and non-dietary risk factors for colon cancer
heterocyclic amines and beta-carbolines by liquid incidence in Iowa women (United States). Cancer
chromatography–mass spectrometry in cooked meats Causes Control, 5(1):38–52. doi:10.1007/BF01830725
commonly consumed in Korea. Food Addit Contam PMID:8123778
Part A Chem Anal Control Expo Risk Assess, 26(3):298– Braekevelt E, Lau BP, Tague B, Popovic S, Tittlemier SA
305. doi:10.1080/02652030802526834 PMID:19680902 (2011). Effect of cooking on concentrations of β-es-
tradiol and metabolites in model matrices and beef.
95
J Agric Food Chem, 59(3):915–20. doi:10.1021/jf103064q Codex Alimentarius (2006). Code of practice for the
PMID:21218831 reduction of dioxin and dioxin-like PCB contam-
Brink M, Weijenberg MP, de Goeij AF, Roemen GM, Lentjes ination in foods and feeds (CAC/RCP 62-2006).
MH, de Bruïne AP et al. (2005). Meat consumption and Rome, Italy: World Health Organization/Food and
K-ras mutations in sporadic colon and rectal cancer in Agriculture Organization of the United Nations.
The Netherlands Cohort Study. Br J Cancer, 92(7):1310– Available from: http://www.codexalimentarius.org/
20. doi:10.1038/sj.bjc.6602491 PMID:15812479 download/standards/10693/CXP_062e.pdf
Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, Codex Alimentarius (2009). Code of practice for the
Gammon MD et al. (2003). Heterocyclic amines, meat reduction of contamination of food with polycy-
intake, and association with colon cancer in a popu- clic aromatic hydrocarbons (PAH) from smoking
lation-based study. Am J Epidemiol, 157(5):434–45. and direct drying processes (CAC/RCP 68-2009).
doi:10.1093/aje/kwf221 PMID:12615608 Rome, Italy: World Health Organization/Food and
Caan BJ, Slattery ML, Potter J, Quesenberry CPJ Jr, Agriculture Organization of the United Nations.
Coates AO, Schaffer DM (1998). Comparison of the Available from: http://www.codexalimentarius.org/
Block and the Willett self-administered semiquan- download/standards/11257/CXP_068e.pdf
titative food frequency questionnaires with an inter- Codex Alimentarius (2015). International food standards.
viewer-administered dietary history. Am J Epidemiol, Maximum residue limits (MRLs) and risk management
148(12):1137–47. doi:10.1093/oxfordjournals.aje. recommendations (RMRs) for residues of veterinary
a009598 PMID:9867257 drugs in foods. CAC/MRL 2-2015. Updated at the 38th
Cantwell M, Mittl B, Curtin J, Carroll R, Potischman Session of the Codex Alimentarius Commission (July
N, Caporaso N et al. (2004). Relative validity of a 2015). Rome, Italy: World Health Organization/Food
food frequency questionnaire with a meat-cooking and Agriculture Organization of the United Nations.
and heterocyclic amine module. Cancer Epidemiol Available from: http://fao.org/input/download/
Biomarkers Prev, 13(2):293–8. doi:10.1158/1055-9965. standards/45/MRL2_2015e.pdf
EPI-270-2 PMID:14973110 Codex Alimentarius (2016a). General standard for
Carroll RJ, Freedman LS, Kipnis V, Li L (1998). A new food additives. Codex STAN 192-1995. Adopted in
class of measurement-error models, with appli- 1995. Revised in 2016. Rome, Italy: World Health
cations to dietary data. Can J Stat, 26(3):467–77. Organization/Food and Agriculture Organization
doi:10.2307/3315770 of the United Nations. Available from: www.fao.org/
Chattopadhyay MK (2014). Use of antibiotics as feed addi- gsfaonline/docs/CXS_192e.pdf
tives: a burning question. Front Microbiol, 5(334):334 Codex Alimentarius (2016b). Pesticide residues in food and
PMID:25071747 feed. Codex pesticides residues in food online database.
Chen BH, Lin YS (1997). Formation of polycyclic aromatic Rome, Italy: World Health Organization/Food and
hydrocarbons during processing of duck meat. J Agric Agriculture Organization of the United Nations. Available
Food Chem, 45(4):1394–403. doi:10.1021/jf9606363 from: http://www.fao.org/fao-who-codexalimentarius/
Chen G, Smith JS (2015). Determination of advanced codex-texts/dbs/pestres/en/
glycation endproducts in cooked meat products. Food Cross AJ, Ferrucci LM, Risch A, Graubard BI, Ward MH,
Chem, 168:190–5. doi:10.1016/j.foodchem.2014.06.081 Park Y et al. (2010). A large prospective study of meat
PMID:25172699 consumption and colorectal cancer risk: an investiga-
Chen J, Stampfer MJ, Hough HL, Garcia-Closas M, Willett tion of potential mechanisms underlying this associa-
WC, Hennekens CH et al. (1998). A prospective study tion. Cancer Res, 70(6):2406–14. doi:10.1158/0008-5472.
of N-acetyltransferase genotype, red meat intake, and CAN-09-3929 PMID:20215514
risk of colorectal cancer. Cancer Res, 58(15):3307–11. Cross AJ, Major JM, Rothman N, Sinha R (2014). Urinary
PMID:9699660 1-methylhistidine and 3-methylhistidine, meat intake,
Chiu BC, Ji BT, Dai Q, Gridley G, McLaughlin JK, Gao YT and colorectal adenoma risk. Eur J Cancer Prev,
et al. (2003). Dietary factors and risk of colon cancer in 23(5):385–90. doi:10.1097/CEJ.0000000000000027
Shanghai, China. Cancer Epidemiol Biomarkers Prev, PMID:24681531
12(3):201–8. PMID:12646508 Cross AJ, Major JM, Sinha R (2011). Urinary biomarkers
Codex Alimentarius (2004). Code of practice for the of meat consumption. Cancer Epidemiol Biomarkers
prevention and reduction of lead contamination in Prev, 20(6):1107–11. doi:10.1158/1055-9965.EPI-11-
foods (CAC/RCP 56-2004). Rome, Italy: World Health 0048 PMID:21527577
Organization/Food and Agriculture Organization Cross AJ, Peters U, Kirsh VA, Andriole GL, Reding D,
of the United Nations. Available from: http://www. Hayes RB et al. (2005). A prospective study of meat and
codexalimentarius.org/download/standards/10099/ meat mutagens and prostate cancer risk. Cancer Res,
CXP_056e.pdf 65(24):11779–84. doi:10.1158/0008-5472.CAN-05-2191
PMID:16357191
96
De Mey E, De Klerck K, De Maere H, Dewulf L, the Commission related to fumonisins as undesirable

Derdelinckx G, Peeters MC et al. (2014). The occurrence substances in animal feed. EFSA J., 235:1–32.
of N-nitrosamines, residual nitrite and biogenic amines EFSA (2007). Opinion of the scientific panel on contamina-
in commercial dry fermented sausages and evaluation tions in the food chain on a request from the European
of their occasional relation. Meat Sci, 96(2 Pt A):821–8. Commission related to hormone residues in bovine
doi:10.1016/j.meatsci.2013.09.010 PMID:24200576 meat and meat products. Palma, Italy: European Food
De Mey E, De Maere H, Paelinck H, Fraeye I (2015). Safety Authority. EFSA J. 510:1–62.
Volatile N-nitrosamines in meat products: potential EFSA (2008). Polycyclic aromatic hydrocarbons in food.
precursors, influence of processing and mitigation Scientific Opinion of the Panel on Contaminants in the
strategies. Crit Rev Food Sci Nutr, 57(13):2909–2923 Food Chain. EFSA J, 724:1–114.
doi:10.1080/10408398.2015.1078769 PMID:26528731 EFSA (2011). The EFSA Comprehensive European Food
Dellavalle CT, Daniel CR, Aschebrook-Kilfoy B, Consumption Database [online database]. Parma,
Hollenbeck AR, Cross AJ, Sinha R et al. (2013). Dietary Italy: European Food Safety Authority. Available from:
intake of nitrate and nitrite and risk of renal cell http://www.efsa.europa.eu/en/food-consumption/
carcinoma in the NIH-AARP Diet and Health Study. comprehensive-database, accessed September 2015
Br J Cancer, 108(1):205–12. doi:10.1038/bjc.2012.522 EFSA (2012). Cadmium dietary exposure in the
PMID:23169285 European population. EFSA J, 10(1):2551. http://dx.doi.
Dennis MJ, Massey RC, McWeeny DJ, Knowles ME, Watson org/10.2903/j.efsa.2012.2551. Available from: www.
D (1983). Analysis of polycyclic aromatic hydrocarbons efsa.europa.eu/efsajournal doi:10.2903/j.efsa.2012.2551
in UK total diets. Food Chem Toxicol, 21(5):569–74. EFSA (2015). European Food Safety Authority [website].
doi:10.1016/0278-6915(83)90142-4 PMID:6686183 Parma, Italy: European Food Safety Authority.
Department of Agriculture (2015). Federal Meat Inspection Available from: http://www.efsa.europa.eu/
Act. Washington (DC), USA: United States Department Egeberg R, Olsen A, Christensen J, Halkjær J, Jakobsen
of Agriculture, Food Safety and Inspection Service. MU, Overvad K et al. (2013). Associations between red
Available from: http://www.fsis.usda.gov/wps/portal/ meat and risks for colon and rectal cancer depend on
fsis/topics/rulemaking/federal-meat-inspection-act the type of red meat consumed. J Nutr, 143(4):464–72.
Dixon LB, Balder HF, Virtanen MJ, Rashidkhani B, doi:10.3945/jn.112.168799 PMID:23427329
Männistö S, Krogh V et al. (2004). Dietary patterns Engel E, Ratel J, Bouhlel J, Planche C, Meurillon M (2015).
associated with colon and rectal cancer: results from Novel approaches to improving the chemical safety of
the Dietary Patterns and Cancer (DIETSCAN) Project. the meat chain towards toxicants. Meat Sci, 109:75–85.
Am J Clin Nutr, 80(4):1003–11. PMID:15447912 doi:10.1016/j.meatsci.2015.05.016 PMID:26043665
Dragsted LO (2010). Biomarkers of meat intake and the English DR, MacInnis RJ, Hodge AM, Hopper JL,
application of nutrigenomics. Meat Sci, 84(2):301–7. Haydon AM, Giles GG (2004). Red meat, chicken,
doi:10.1016/j.meatsci.2009.08.028 PMID:20374789 and fish consumption and risk of colorectal cancer.
EFSA (2003). Opinion of the Scientific Panel on Biological Cancer Epidemiol Biomarkers Prev, 13(9):1509–14.
Hazards on the request from the Commission related PMID:15342453
to the effects of nitrites/nitrates on the microbiological EPA (2010). An exposure assessment of polybromi-
safety of meat products. EFSA J, 14:1–31. nated diphenyl ethers. Report No. EPA/600/R-
EFSA (2004a). Opinion of the Scientific Panel on 08/086F. Washington (DC), USA: National Center for
Contaminants in the Food Chain on a request from Environmental Assessment, Office of Research and
the Commission related to aflatoxin B1 as undesirable Development, United States Environmental Protection
substance in animal feed. EFSA J., 39:1–27. Agency.
EFSA (2004b). Opinion of the Scientific Panel on European Commission (2003). Regulation (EC) No
Contaminants in the Food Chain on a request from 1831/2003 of the European Parliament and of the
the Commission related to deoxynivalenol (DON) as Council of 22 September 2003 on additives for use
undesirable substance in animal feed. EFSA J., 73:1–41. in animal nutrition. Official Journal of the European
EFSA (2004c). Opinion of the Scientific Panel on Union L, 268:29–43.
Contaminants in the Food Chain on a request from European Commission (2004). Regulation (EC) No.
the Commission related to zearalenone as undesirable 853/2004 of the European Parliament and of the
substance in animal feed. EFSA J., 89:1–35. Council of 29 April 2004 laying down specific hygiene
EFSA (2004d). Opinion of the Scientific Panel on rules for food of animal origin. Available from: http://
Contaminants in the Food Chain on a request from the eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:
Commission related to ochratoxin A (OTA) as undesir- L:2004:226:0022:0082:EN:PDF
able substance in animal feed. EFSA J., 101:1–36. FAO (2015). Food Balance. FAOSTAT [online database].
EFSA (2005c). Opinion of the Scientific Panel on Food and Agriculture Organization of the United
Contaminants in the Food Chain on a request from Nations Statistics Division. Rome, Italy: Food and
97
Agriculture Organization of the United Nations. beef patties. Food Chem, 134(2):766–74. doi:10.1016/j.
Available from: http://faostat3.fao.org/browse/FB/*/E, foodchem.2012.02.179 PMID:23107689
accessed 9 July 2015 Gille D, Schmid A (2015). Vitamin B12 in meat and dairy
FAO/WHO (2015). The FAO/WHO Chronic individual products. Nutr Rev, 73(2):106–15. doi:10.1093/nutrit/
food consumption database – summary statistics nuu011 PMID:26024497
(CIFOCOss). Food and Agriculture Organization of the Giri A, Khummueng W, Mercier F, Kondjoyan N,
United Nations/World Health Organization. Available Tournayre P, Meurillon M et al. (2015). Relevance of
from: http://www.who.int/foodsafety/databases/en/ two-dimensional gas chromatography and high reso-
FCID (2015). What we eat in America - Food commodity lution olfactometry for the parallel determination
intake database 2005-10. Commodity consumption of heat-induced toxicants and odorants in cooked
calculator. United States Environmental Protection food. J Chromatogr A, 1388:217–26. doi:10.1016/j.
Agency, Office of Pesticide Programs © University chroma.2015.01.045 PMID:25728653
of Maryland 2012-2016. Available from: http://fcid. Givens DI (2005). The role of animal nutrition in improving
foodrisk.org/percentiles.php the nutritive value of animal-derived foods in rela-
FDA (2005). Subject: Illegal residues in meat, poultry, tion to chronic disease. Proc Nutr Soc, 64(3):395–402.
seafood, and other animal derived foods. Chapter: doi:10.1079/PNS2005448 PMID:16048674
Post-approval monitoring of animal drugs, feeds and Goldberg T, Cai W, Peppa M, Dardaine V, Baliga BS,
devices In: Compliance program guidance manual. Uribarri J et al. (2004). Advanced glycoxidation end
United States Food and Drug Administration. products in commonly consumed foods. J Am Diet
FDA (2008). Subject: Mycotoxins in domestic and Assoc, 104(8):1287–91. doi:10.1016/j.jada.2004.05.214
imported food. Chapter 07: Molecular biology and PMID:15281050
natural toxins. In: Compliance program guidance Guerrero Legarreta I (2010). Canned products and pâté.
manual. United States Food and Drug Administration. In: Toldra F, editor. Handbook of meat processing.
FDA (2015). Guidance and regulation. Washington (DC), Blackwell Publishing. Part 2, Chapter 19; 337–349.
USA: United States Department of Agriculture, Food Available from: http://onlinelibrary.wiley.com/
and Drug Administration. Available from: http://www. doi/10.1002/9780813820897.ch19/summary
fda.gov/Food/GuidanceRegulation Guertin KA, Moore SC, Sampson JN, Huang WY, Xiao Q,
Felton JS, Knize MG, Roper M, Fultz E, Shen NH, Stolzenberg-Solomon RZ et al. (2014). Metabolomics
Turteltaub KW (1992). Chemical analysis, preven- in nutritional epidemiology: identifying metabolites
tion, and low-level dosimetry of heterocyclic amines associated with diet and quantifying their potential
from cooked food. Cancer Res, 52(7):Suppl: 2103s–7s. to uncover diet-disease relations in populations. Am J
PMID:1544148 Clin Nutr, 100(1):208–17. doi:10.3945/ajcn.113.078758
Ferrucci LM, Cross AJ, Graubard BI, Brinton LA, PMID:24740205
McCarty CA, Ziegler RG et al. (2009). Intake of meat, Haorah J, Zhou L, Wang X, Xu G, Mirvish SS (2001).
meat mutagens, and iron and the risk of breast cancer Determination of total N-nitroso compounds and
in the Prostate, Lung, Colorectal, and Ovarian Cancer their precursors in frankfurters, fresh meat, dried
Screening Trial. Br J Cancer, 101(1):178–84. doi:10.1038/ salted fish, sauces, tobacco, and tobacco smoke partic-
sj.bjc.6605118 PMID:19513076 ulates. J Agric Food Chem, 49(12):6068–78. doi:10.1021/
Flood A, Velie EM, Sinha R, Chaterjee N, Lacey JV Jr, jf010602h PMID:11743810
Schairer C et al. (2003). Meat, fat, and their subtypes as Hedlund M, Padler-Karavani V, Varki NM, Varki A (2008).
risk factors for colorectal cancer in a prospective cohort Evidence for a human-specific mechanism for diet
of women. Am J Epidemiol, 158(1):59–68. doi:10.1093/ and antibody-mediated inflammation in carcinoma
aje/kwg099 PMID:12835287 progression. Proc Natl Acad Sci U S A, 105(48):18936–
Fung T, Hu FB, Fuchs C, Giovannucci E, Hunter DJ, 41. doi:10.1073/pnas.0803943105 PMID:19017806
Stampfer MJ et al. (2003). Major dietary patterns and Hedrick VE, Dietrich AM, Estabrooks PA, Savla J, Serrano
the risk of colorectal cancer in women. Arch Intern E, Davy BM (2012). Dietary biomarkers: advances,
Med, 163(3):309–14. doi:10.1001/archinte.163.3.309 limitations and future directions. Nutr J, 11(1):109
PMID:12578511 doi:10.1186/1475-2891-11-109 PMID:23237668
Gibis M, Weiss J (2010). Inhibitory effect of marinades with Heinz G, Hautzinger P (2007). Meat processing technology
hibiscus extract on formation of heterocyclic aromatic for small - to medium - scale producers. Rome, Italy: Food
amines and sensory quality of fried beef patties. Meat and Agriculture Organization of the United Nations.
Sci, 85(4):735–42. doi:10.1016/j.meatsci.2010.03.034 Available from: http://www.fao.org/documents/card/
PMID:20418021 fr/c/fb92d00f-7ff3-593a-a77c-7b19003b2554/
Gibis M, Weiss J (2012). Antioxidant capacity and inhibi- Henson S, Caswell J (1999). Food safety regulation:
tory effect of grape seed and rosemary extract in mari- an overview of contemporary issues. Food Policy,
nades on the formation of heterocyclic amines in fried 24(6):589–603. doi:10.1016/S0306-9192(99)00072-X
98
Heshmati A. (2015). Impact of cooking procedures on Risks Hum, 94:1–448. PMID:21141240. Available from:
antibacterial drug residues in foods: a review. Journal http://monographs.iarc.fr/ENG/Monographs/vol94/
of Food Quality & Hazards Control, 2:33–37. index.php
Hill RJ, Davies PS (2001). The validity of self-reported IARC (2012a). Arsenic, metals, fibres, and dusts. IARC
energy intake as determined using the doubly labelled Monogr Eval Carcinog Risks Hum, 100C:1–499.
water technique. Br J Nutr, 85(4):415–30. doi:10.1079/ PMID:23189751. Available from: http://monographs.
BJN2000281 PMID:11348556 iarc.fr/ENG/Monographs/vol100C/index.php
Honikel KO (2008). The use and control of nitrate and IARC (2012b). Chemical agents and related occupations.
nitrite for the processing of meat products. Meat IARC Monogr Eval Carcinog Risks Hum, 100F:1–599.
Sci, 78(1–2):68–76. doi:10.1016/j.meatsci.2007.05.030 PMID:23189753. Available from: http://monographs.
PMID:22062097 iarc.fr/ENG/Monographs/vol100F/index.php
Honikel KO (2010). Curing. Chapter 6. In: Toldra F, editor. IARC (2016). Polychlorinated biphenyls and polybromi-
Handbook of meat processing. Blackwell Publishing; nated biphenyls. IARC Monogr Eval Carcinog Risks
125–41. doi:10.1002/9780813820897.ch6 Hum, 107:1–502. Available from: http://monographs.
Hori T, Nakagawa R, Tobiishi K, Iida T, Tsutsumi T, iarc.fr/ENG/Monographs/vol107/index.php
Sasaki K et al. (2005). Effects of cooking on concentra- Imamura F, Micha R, Khatibzadeh S, Fahimi S, Shi P,
tions of polychlorinated dibenzo-p-dioxins and related Powles J et al. ; Global Burden of Diseases Nutrition
compounds in fish and meat. J Agric Food Chem, and Chronic Diseases Expert Group (NutriCoDE)
53(22):8820–8. doi:10.1021/jf050978l PMID:16248590 (2015). Dietary quality among men and women in 187
Hu FB (2002). Dietary pattern analysis: a new direc- countries in 1990 and 2010: a systematic assessment.
tion in nutritional epidemiology. Curr Opin Lipidol, Lancet Glob Health, 3(3):e132–42. doi:10.1016/S2214-
13(1):3–9. doi:10.1097/00041433-200202000-00002 109X(14)70381-X PMID:25701991
PMID:11790957 IPCS (2009). Principles and methods for the risk assess-
Hu FB, Stampfer MJ, Rimm E, Ascherio A, Rosner BA, ment of chemicals in food. Environmental Health
Spiegelman D et al. (1999). Dietary fat and coro- Criteria 240. Geneva, Switzerland: International
nary heart disease: a comparison of approaches Programme on Chemical Safety, Food and Agriculture
for adjusting for total energy intake and modeling Organization of the United Nations/World Health
repeated dietary measurements. Am J Epidemiol, Organization. Available from: http://www.who.int/
149(6):531–40. doi:10.1093/oxfordjournals.aje.a009849 foodsafety/publications/chemical-food/en/
PMID:10084242 Isam T, Kadim IT, Mahgoub O (2007). Postharvest handling
Hudson WR, Mead GC, Hinton MH (1996). Relevance of red meat. In: Rahman MS editor. Handbook of food
of abattoir hygiene assessment to microbial contami- preservation. New York, USA: Marcel Dekker; 173.
nation of British beef carcases. Vet Rec, 139(24):587–9. Iwasaki M, Mukai T, Takachi R, Ishihara J, Totsuka
PMID:8981733 Y, Tsugane S (2014). Validity of a self-administered
Hull GLJ, Woodside JV, Ames JM, Cuskelly GJ (2012). food frequency questionnaire in the estimation
Nε-(Carboxymethyl)lysine content of foods commonly of heterocyclic aromatic amines. Cancer Causes
consumed in a Western style diet. Food Chem, Control, 25(8):1015–28. doi:10.1007/s10552-014-0401-7
131(1):170–4. doi:10.1016/j.foodchem.2011.08.055 PMID:24890804
PMID:23017409 Järvinen R, Knekt P, Hakulinen T, Rissanen H, Heliövaara
Hygreeva D, Pandey MC, Radhakrishna K (2014). Potential M (2001). Dietary fat, cholesterol and colorectal cancer
applications of plant based derivatives as fat replacers, in a prospective study. Br J Cancer, 85(3):357–61.
antioxidants and antimicrobials in fresh and processed doi:10.1054/bjoc.2001.1906 PMID:11487265
meat products. Meat Sci, 98(1):47–57. doi:10.1016/j. JECFA (2000). Toxicological evaluation of certain veter-
meatsci.2014.04.006 PMID:24845336 inary drug residues in food: Estradiol-17α, proges-
IARC (1993). Some naturally occurring substances: food terone, and testosterone. Prepared by the Fifty-second
items and constituents, heterocyclic aromatic amines meeting of the Joint FAO/WHO Expert Committee
and mycotoxins. IARC Monogr Eval Carcinog Risks on Food Additives. Geneva, Switzerland: World
Hum, 56:1–599. Available from: http://monographs. Health Organization. WHO Food Additives Series: 43.
iarc.fr/ENG/Monographs/vol56/index.php Available from: http://www.inchem.org/documents/
IARC (2010a). Some non-heterocyclic polycyclic aromatic jecfa/jecmono/v43jec05.htm
hydrocarbons and some related exposures. IARC JECFA (2002). Polychlorinated dibenzodioxins (PCDDs),
Monogr Eval Carcinog Risks Hum, 92:1–853. Available polychlorinated dibenzofurans (PCDFs), and coplanar
from: http://monographs.iarc.fr/ENG/Monographs/ polychlorinated biphenyls (PCBs). Evaluations of
vol92/index.php PMID:21141735 the Joint FAO/WHO Expert Committee on Food
IARC (2010b). Ingested nitrate and nitrite, and cyano- Additives. Geneva, Switzerland: World Health
bacterial peptide toxins. IARC Monogr Eval Carcinog Organization. Available from: http://apps.who.
99
int/food-additives-contaminants-jecfa-database/ Kipnis V, Freedman LS, Brown CC, Hartman AM,

chemical.aspx?chemID=2753 Schatzkin A, Wacholder S (1997). Effect of measurement
JECFA (2011). Acrylamide. In: Safety evaluation of certain error on energy-adjustment models in nutritional epide-
contaminants in food. Prepared by the Seventy-second miology. Am J Epidemiol, 146(10):842–55. doi:10.1093/
meeting of the Joint FAO/WHO Expert Committee on oxfordjournals.aje.a009202 PMID:9384205
Food Additives. WHO Food Additives Series: 63, FAO Knize MG, Brown ED, Salmon CP, Levander OA, Felton
JECFA Monographs 8. JS, Rothman N (1998). Heterocyclic amine content
JECFA (2013). Cadmium. Evaluations of the Joint in restaurant-cooked hamburgers, steaks, ribs and
FAO/WHO Committee on Food Additives. chicken. J. Food Ag. Chem., 46(11):4648–51. doi:10.1021/
Geneva, Switzerland: World Health Organization. jf980639a
Available from: http://apps.who.int/food- Kobayashi M, Hanaoka T, Hashimoto H, Tsugane S (2005).
additives-contaminants-jecfa-database/chemical. 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine
aspx?chemID=1376 (PhIP) level in human hair as biomarkers for dietary
Jeong S-H, Kang D, Lim M-W, Kang CS, Sung HJ (2010). grilled/stir-fried meat and fish intake. Mutat Res,
Risk assessment of growth hormones and antimicrobial 588(2):136–42. doi:10.1016/j.mrgentox.2005.09.008
residues in meat. Toxicol Res, 26(4):301–13. doi:10.5487/ PMID:16289877
TR.2010.26.4.301 PMID:24278538 Kobayashi M, Hanaoka T, Tsugane S (2007). Validity
Kabat GC, Miller AB, Jain M, Rohan TE (2007). A cohort of a self-administered food frequency questionnaire
study of dietary iron and heme iron intake and risk of in the assessment of heterocyclic amine intake using
colorectal cancer in women. Br J Cancer, 97(1):118–22. 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyri-
doi:10.1038/sj.bjc.6603837 PMID:17551493 dine (PhIP) levels in hair. Mutat Res, 630(1–2):14–9.
Kan CA, Meijer GAL (2007). The risk of contamination doi:10.1016/j.mrgentox.2007.02.003 PMID:17392018
of food with toxic substances present in animal feed. Krause R, Knoll K, Henle T (2003). Studies on the forma-
Anim Feed Sci Technol, 133(1–2):84–108. doi:10.1016/j. tion of furosine and pyridosine during acid hydrolysis
anifeedsci.2006.08.005 of different Amadori products of lysine. Eur Food Res
Kato I, Akhmedkhanov A, Koenig K, Toniolo PG, Shore Technol, 216(4):277–83. doi:10.1007/s00217-002-0649-0
RE, Riboli E (1997). Prospective study of diet and Kushi LH (1994). Gaps in epidemiologic research methods:
female colorectal cancer: the New York University design considerations for studies that use food-fre-
Women’s Health Study. Nutr Cancer, 28(3):276–81. quency questionnaires. Am J Clin Nutr, 59(1):Suppl:
doi:10.1080/01635589709514588 PMID:9343837 180S–4S. PMID:8279420
Kazerouni N, Sinha R, Hsu C-H, Greenberg A, Rothman Larsen JC (2006). Risk assessments of polychlorinated
N (2001). Analysis of 200 food items for benzo[a]pyrene dibenzo-p-dioxins, polychlorinated dibenzofu-
and estimation of its intake in an epidemiologic study. rans, and dioFxin-like polychlorinated biphenyls in
Food Chem Toxicol, 39(5):423–36. doi:10.1016/S0278- food. Mol Nutr Food Res, 50(10):885–96. doi:10.1002/
6915(00)00158-7 PMID:11313108 mnfr.200500247 PMID:17009211
Keating GA, Bogen KT (2004). Estimates of heterocy- Lawrie RA (1998). Lawrie’s meat science. Cambridge,
clic amine intake in the US population. J Chromatogr England: Woodhead Publishing Ltd.
B Analyt Technol Biomed Life Sci, 802(1):127–33. Lawrie RA, Ledward DA (2006). Chapter 5: The conversion
doi:10.1016/j.jchromb.2003.10.047 PMID:15036004 of muscle to meat. In: Lawrie RA, editor. Lawrie’s meat
Kesse E, Clavel-Chapelon F, Boutron-Ruault MC (2006). science. Cambridge, England: Woodhead Publishing
Dietary patterns and risk of colorectal tumors: a cohort Ltd.
of French women of the National Education System Ledesma E, Rendueles M, Díaz M (2014). Benzo(a)pyrene
(E3N). Am J Epidemiol, 164(11):1085–93. doi:10.1093/ penetration on a smoked meat product during smoking
aje/kwj324 PMID:16990408 time. Food Addit Contam Part A Chem Anal Control
Khan MR, Busquets R, Santos FJ, Puignou L (2008). Expo Risk Assess, 31(10):1688–98. doi:10.1080/1944004
New method for the analysis of heterocyclic amines 9.2014.949875 PMID:25078362
in meat extracts using pressurised liquid extraction Lee DH, Anderson KE, Folsom AR, Jacobs DR Jr (2005).
and liquid chromatography–tandem mass spectrom- Heme iron, zinc and upper digestive tract cancer: the
etry. J Chromatogr A, 1194(2):155–60. doi:10.1016/j. Iowa Women’s Health Study. Int J Cancer, 117(4):643–7.
chroma.2008.04.058 PMID:18490022 doi:10.1002/ijc.21215 PMID:15929082
Kilfoy BA, Zhang Y, Park Y, Holford TR, Schatzkin A, Lee SA, Shu XO, Yang G, Li H, Gao YT, Zheng W (2009).
Hollenbeck A et al. (2011). Dietary nitrate and nitrite Animal origin foods and colorectal cancer risk: a
and the risk of thyroid cancer in the NIH-AARP report from the Shanghai Women’s Health Study. Nutr
Diet and Health Study. Int J Cancer, 129(1):160–72. Cancer, 61(2):194–205. doi:10.1080/01635580802419780
doi:10.1002/ijc.25650 PMID:20824705 PMID:19235035
100
Linseisen J, Kesse E, Slimani N, Bueno-De-Mesquita HB, coupled to mass spectrometry. J Agric Food Chem,
Ocké MC, Skeie G et al. (2002). Meat consumption in 48(4):1160–6. doi:10.1021/jf991205y PMID:10775366
the European Prospective Investigation into Cancer Murkovic M (2004). Formation of heterocyclic aromatic
and Nutrition (EPIC) cohorts: results from 24-hour amines in model systems. J Chromatogr B Analyt
dietary recalls. Public Health Nutr, 5(6B):6B: 1243–58. Technol Biomed Life Sci, 802(1):3–10. doi:10.1016/j.
doi:10.1079/PHN2002402 PMID:12639230 jchromb.2003.09.026 PMID:15035991
Linseisen J, Rohrmann S, Norat T, Gonzalez CA, Nachman KE, Smith TJ (2015). Hormone use in food
Dorronsoro Iraeta M, Morote Gómez P et al. (2006). animal production: assessing potential dietary expo-
Dietary intake of different types and characteristics sures and breast cancer risk. Curr Environ Health
of processed meat which might be associated with Rep, 2(1):1–14. doi:10.1007/s40572-014-0042-8
cancer risk - results from the 24-hour diet recalls in PMID:26231238
the European Prospective Investigation into Cancer NCI (2017). CHARRED: Computerized Heterocyclic
and Nutrition (EPIC). Public Health Nutr, 9(4):449–64. Amines Resource for Research in Epidemiology of
doi:10.1079/PHN2005861 PMID:16870017 Disease. Bethesda (MD), USA: Division of Cancer
Lloyd AJ, Favé G, Beckmann M, Lin W, Tailliart K, Xie L Epidemiology and Genetics, National Cancer Institute.
et al. (2011). Use of mass spectrometry fingerprinting Available from: http://dceg.cancer.gov/tools/design/
to identify urinary metabolites after consumption of charred
specific foods. Am J Clin Nutr, 94(4):981–91. doi:10.3945/ Ni W, McNaughton L, LeMaster DM, Sinha R, Turesky
ajcn.111.017921 PMID:21865330 RJ (2008). Quantitation of 13 heterocyclic aromatic
Lombardi-Boccia G, Martinez-Dominguez B, Aguzzi amines in cooked beef, pork, and chicken by liquid
A (2002). Total heme and non-heme iron in raw chromatography–electrospray ionization/tandem
and cooked meats. J Food Sci, 67(5):1738–41. mass spectrometry. J Agric Food Chem, 56(1):68–78.
doi:10.1111/j.1365-2621.2002.tb08715.x doi:10.1021/jf072461a PMID:18069786
Lorenzo JM, Crecente S, Franco D, Sarriés MV, Gómez M Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir
(2014). The effect of livestock production system and M et al. (2005). Meat, fish, and colorectal cancer risk:
concentrate level on carcass traits and meat quality of the European Prospective Investigation into Cancer
foals slaughtered at 18 months of age. Animal, 8(3):494– and Nutrition. J Natl Cancer Inst, 97(12):906–16.
503. doi:10.1017/S175173111300236X PMID:24398030 doi:10.1093/jnci/dji164 PMID:15956652
Lorenzo JM, Fuciños C, Purriños L, Franco D (2010). Ockermann HW, Basu L (2010). Chapters 9 and 10:
Intramuscular fatty acid composition of “Galician Fermented meat products: production and consump-
Mountain” foals breed: effect of sex, slaughtered age tion. In: Toldrá F, editor. Handbook of meat processing.
and livestock production system. Meat Sci, 86(3):825– Columbus (OH), USA: The Ohio State University.
31. doi:10.1016/j.meatsci.2010.07.004 PMID:20675062 Office of the Federal Register (2015). Part 319–definitions
Lyche JL, Rosseland C, Berge G, Polder A (2015). Human and standards of identity or composition. Title 9 -
health risk associated with brominated flame-retard- Animals and animal products (9 CFR Part 319). United
ants (BFRs). Environ Int, 74:170–80. doi:10.1016/j. States Code of Federal Regulations. Washington
envint.2014.09.006 PMID:25454234 (DC), USA: United States Government Publishing
Manabe S, Izumikawa S, Asakuno K, Wada O, Kanai Office. Available from: http://www.gpo.gov/fdsys/
Y (1991). Detection of carcinogenic amino-al- pkg/CFR-2015-title9-vol2/xml/CFR-2015-title9-vol2-
pha-carbolines and amino-gamma-carbolines in part319.xml
diesel-exhaust particles. Environ Pollut, 70(3):255–65. Olatunji OS, Fatoki OS, Opeolu BO, Ximba BJ (2014).
doi:10.1016/0269-7491(91)90013-M PMID:15092136 Determination of polycyclic aromatic hydrocarbons
Marroquín-Cardona AG, Johnson NM, Phillips TD, [PAHs] in processed meat products using gas chro-
Hayes AW (2014). Mycotoxins in a changing global matography – flame ionization detector. Food Chem,
environment – a review. Food Chem Toxicol, 69:220– 156:296–300. doi:10.1016/j.foodchem.2014.01.120
30. doi:10.1016/j.fct.2014.04.025 PMID:24769018 PMID:24629971
McCann SE, Marshall JR, Trevisan M, Russell M, Muti P, Ollberding NJ, Wilkens LR, Henderson BE, Kolonel LN,
Markovic N et al. (1999). Recent alcohol intake as esti- Le Marchand L (2012). Meat consumption, heterocy-
mated by the health habits and history questionnaire, clic amines and colorectal cancer risk: the Multiethnic
the Harvard semiquantitative food frequency ques- Cohort Study. Int J Cancer, 131(7):E1125–33. doi:10.1002/
tionnaire, and a more detailed alcohol intake ques- ijc.27546 PMID:22438055
tionnaire. Am J Epidemiol, 150(4):334–40. doi:10.1093/ Pala V, Krogh V, Berrino F, Sieri S, Grioni S, Tjønneland
oxfordjournals.aje.a010012 PMID:10453809 A et al. (2009). Meat, eggs, dairy products, and risk of
Mottier P, Parisod V, Turesky RJ (2000). Quantitative breast cancer in the European Prospective Investigation
determination of polycyclic aromatic hydrocarbons into Cancer and Nutrition (EPIC) cohort. Am J Clin
in barbecued meat sausages by gas chromatography
101
Nutr, 90(3):602–12. doi:10.3945/ajcn.2008.27173 duodenal digestion. Meat Sci, 74(3):443–9. doi:10.1016/j.

PMID:19491385 meatsci.2006.03.015 PMID:22063048
Paris A, Andre F, Antignac JP, Le Bizec B, Bonneau M, Rahman MS (2007). Food preservation overview. In:
Briant C et al. (2006). Hormones et promoteurs de Rahman MS, editor. Handbook of food preservation.
croissance en productions animales: de la physiologie New York, USA: Marcel Dekker; 635–66.
à l’évaluation du risque. INRA Prod Anim, 19(3):151– Rimm EB, Giovannucci EL, Stampfer MJ, Colditz GA,
240. [French] Litin LB, Willett WC (1992). Reproducibility and
Parnell WR, Blakey CW, Smith C (2012). Secondary anal- validity of an expanded self-administered semiquan-
ysis of Adult Nutrition Survey 2008/09 for intake of titative food frequency questionnaire among male
Beef and Lamb for the New Zealand population and for health professionals. Am J Epidemiol, 135(10):1114–26,
consumers. Dunedin, New Zealand: LINZ® Nutrition discussion 1127–36. PMID:1632423
and Activity Research Unit, University of Otago, Rohrmann S, Linseisen J, Becker N, Norat T, Sinha R,
Report No.: 2012.138. Skeie G et al. ; European Prospective Investigation into
Pearson AM, Gillett TA (1996). Curing. Chapter 3. In: Cancer and Nutrition (2002). Cooking of meat and fish
Pearson AM, Gillett TA, editors. Processed meats, 3rd in Europe – results from the European Prospective
Edition. Maryland, USA: Aspen Publishers, Inc; 53–78. Investigation into Cancer and Nutrition (EPIC). Eur J
Perelló G, Martí-Cid R, Castell V, Llobet JM, Domingo JL Clin Nutr, 56(12):1216–30. doi:10.1038/sj.ejcn.1601494
(2010). Influence of various cooking processes on the PMID:12494307
concentrations of PCDD/PCDFs, PCBs and PCDEs Rohrmann S, Zoller D, Hermann S, Linseisen J (2007).
in foods. Food Contr, 21(2):178–85. doi:10.1016/j. Intake of heterocyclic aromatic amines from meat
foodcont.2009.05.003 in the European Prospective Investigation into
Perelló G, Martí-Cid R, Llobet JM, Domingo JL (2008). Cancer and Nutrition (EPIC)-Heidelberg cohort. Br
Effects of various cooking processes on the concen- J Nutr, 98(6):1112–5. doi:10.1017/S000711450778145X
trations of arsenic, cadmium, mercury, and lead in PMID:18309547
foods. J Agric Food Chem, 56(23):11262–9. doi:10.1021/ Roseiro LC, Gomes A, Santos C (2011). Influence of
jf802411q PMID:18986150 processing in the prevalence of polycyclic aromatic
Pietinen P, Malila N, Virtanen M, Hartman TJ, Tangrea hydrocarbons in a Portuguese traditional meat product.
JA, Albanes D et al. (1999). Diet and risk of colorectal Food Chem Toxicol, 49(6):1340–5. doi:10.1016/j.
cancer in a cohort of Finnish men. Cancer Causes fct.2011.03.017 PMID:21419819
Control, 10(5):387–96. doi:10.1023/A:1008962219408 Rywotycki R (2007). The effect of baking of various kinds
PMID:10530608 of raw meat from different animal species and meat
Preussmann R, Stewart BW (1984). N-Nitroso carcin- with functional additives on nitrosamine contami-
ogens. In: Searle CE, editor. Chemical carcinogens. nation level. Food Chem, 101(2):540–8. doi:10.1016/j.
Washington (DC), USA: American Chemical Society; foodchem.2006.02.012
643–828. Samraj AN, Pearce OMT, Läubli H, Crittenden AN,
Pryer JA, Nichols R, Elliott P, Thakrar B, Brunner Bergfeld AK, Banda K et al. (2015). A red meat-derived
E, Marmot M (2001). Dietary patterns among a glycan promotes inflammation and cancer progression.
national random sample of British adults. J Epidemiol Proc Natl Acad Sci U S A, 112(2):542–7. doi:10.1073/
Community Health, 55(1):29–37. doi:10.1136/ pnas.1417508112 PMID:25548184
jech.55.1.29 PMID:11112948 Santarelli RL, Pierre F, Corpet DE (2008). Processed meat
Puiggròs F, Solà R, Bladé C, Salvadó MJ, Arola L (2011). and colorectal cancer: a review of epidemiologic and
Nutritional biomarkers and foodomic methodol- experimental evidence. Nutr Cancer, 60(2):131–44.
ogies for qualitative and quantitative analysis of doi:10.1080/01635580701684872 PMID:18444144
bioactive ingredients in dietary intervention studies. Santé-Lhoutellier V, Astruc T, Marinova P, Greve E,
J Chromatogr A, 1218(42):7399–414. doi:10.1016/j. Gatellier P (2008). Effect of meat cooking on physic-
chroma.2011.08.051 PMID:21917262 ochemical state and in vitro digestibility of myofi-
Purchas RW, Busboom JR (2005). The effect of produc- brillar proteins. J Agric Food Chem, 56(4):1488–94.
tion system and age on levels+ of iron, taurine, doi:10.1021/jf072999g PMID:18237130
carnosine, coenzyme Q(10), and creatine in beef Sato Y, Nakaya N, Kuriyama S, Nishino Y, Tsubono Y, Tsuji I
muscles and liver. Meat Sci, 70(4):589–96. doi:10.1016/j. (2006). Meat consumption and risk of colorectal cancer
meatsci.2005.02.008 PMID:22063884 in Japan: the Miyagi Cohort Study. Eur J Cancer Prev,
Purchas RW, Busboom JR, Wilkinson BH (2006). Changes 15(3):211–8. doi:10.1097/01.cej.0000197455.87356.05
in the forms of iron and in concentrations of taurine, PMID:16679863
carnosine, coenzyme Q(10), and creatine in beef longis- Scalbert A, Brennan L, Manach C, Andres-Lacueva C,
simus muscle with cooking and simulated stomach and Dragsted LO, Draper J et al. (2014). The food metab-
olome: a window over dietary exposure. Am J Clin
102
Nutr, 99(6):1286–308. doi:10.3945/ajcn.113.076133 Sinha R, Rothman N, Brown ED, Salmon CP, Knize
PMID:24760973 MG, Swanson CA et al. (1995). High concentrations
Schecter A, Harris TR, Shah N, Musumba A, Päpke of the carcinogen 2-amino-1-methyl-6-phenylim-
O (2008). Brominated flame retardants in US food. idazo-[4,5-b]pyridine (PhIP) occur in chicken but
Mol Nutr Food Res, 52(2):266–72. doi:10.1002/ are dependent on the cooking method. Cancer Res,
mnfr.200700166 PMID:18040989 55(20):4516–9. PMID:7553619
Schonfeldt HC, Hall NG (2011). Determining iron Sinha R, Rothman N, Salmon CP, Knize MG, Brown ED,
bio-availability with a constant heme iron value. Swanson CA et al. (1998b). Heterocyclic amine content
J Food Compos Anal, 24(4–5):738–40. doi:10.1016/j. in beef cooked by different methods to varying degrees
jfca.2011.01.002 of doneness and gravy made from meat drippings. Food
Schroeder H (2010). Les hydrocarbures aromatiques Chem Toxicol, 36(4):279–87.[b] doi:10.1016/S0278-
polycycliques présentent-ils un risque de neurotoxicité 6915(97)00162-2 PMID:9651044
développementale? ANSES Bulletin veille scientifique Skog K, Solyakov A, Jagerstad MI (2000). Effects of
santé environnement travail; 11:83–8. Available from: heating conditions and additives on the formation of
https://www.anses.fr/fr/system/files/BVS-mg-011- heterocyclic amines with reference to amino-carbo-
SCHROEDER.pdf [French] lines in a meat juice model system. Food Chem Toxicol,
Schummer C, Appenzeller BM, Millet M, Wennig R 68(3):299–308. doi:10.1016/S0308-8146(99)00195-8
(2009). Determination of hydroxylated metabolites Skog KI, Johansson MA, Jägerstad MI (1998). Carcinogenic
of polycyclic aromatic hydrocarbons in human hair heterocyclic amines in model systems and cooked
by gas chromatography–negative chemical ionization foods: a review on formation, occurrence and intake.
mass spectrometry. J Chromatogr A, 1216(32):6012–9. Food Chem Toxicol, 36(9–10):879–96. doi:10.1016/
doi:10.1016/j.chroma.2009.05.068 PMID:19577242 S0278-6915(98)00061-1 PMID:9737435
Sempos CT, Liu K, Ernst ND (1999). Food and nutrient Sobell J, Block G, Koslowe P, Tobin J, Andres R (1989).
exposures: what to consider when evaluating epide- Validation of a retrospective questionnaire assessing
miologic evidence. Am J Clin Nutr, 69(6):1330S–8S. diet 10–15 years ago. Am J Epidemiol, 130(1):173–87.
PMID:10357757 PMID:2741904
Shin H-S, Strasburg GM, Gray JI (2002). A model system Sofos JN (2008). Challenges to meat safety in the
study of the inhibition of heterocyclic aromatic 21st century. Meat Sci, 78(1–2):3–13. doi:10.1016/j.
amine formation by organosulfur compounds. J Agric meatsci.2007.07.027 PMID:22062090
Food Chem, 50(26):7684–90. doi:10.1021/jf025707e Stadler RH, Lineback DR (2009). Process-induced food
PMID:12475289 toxicants, occurrence, formation, mitigation and
Sikorski ZE, Kalakowski E (2010). Smoking. In: Toldra health risks. Hoboken (NJ), USA: John Wiley & Sons.
F, editor. Handbook of meat processing. Oxford, UK: Stella C, Beckwith-Hall B, Cloarec O, Holmes E, Lindon
Wiley-Blackwell. doi:10.1002/9780813820897.ch12 JC, Powell J et al. (2006). Susceptibility of human meta-
Sindelar JJ, Milkowski AL (2012). Human safety contro- bolic phenotypes to dietary modulation. J Proteome Res,
versies surrounding nitrate and nitrite in the diet. Nitric 5(10):2780–8. doi:10.1021/pr060265y PMID:17022649
Oxide, 26(4):259–66. doi:10.1016/j.niox.2012.03.011 Subar AF, Midthune D, Kulldorff M, Brown CC,
PMID:22487433 Thompson FE, Kipnis V et al. (2000). Evaluation of
Sindelar JJ, Sebranek JG, Bacus JN (2010). Uncured, natural, alternative approaches to assign nutrient values to
and organic processed meat products. Meat processing food groups in food frequency questionnaires. Am J
technology series. Champaign (IL), USA: American Epidemiol, 152(3):279–86. doi:10.1093/aje/152.3.279
Meat Science Association; 1–42. Available from http:// PMID:10933275
www.lulu.com/shop/jeffrey-sindelar/uncured-natural- Subar AF, Thompson FE, Smith AF, Jobe JB, Ziegler RG,
and-organic-processed-meat-products/paperback/ Potischman N et al. (1995). Improving food frequency
product-12200306.html questionnaires: a qualitative approach using cognitive
Singh PN, Fraser GE (1998). Dietary risk factors for interviewing. J Am Diet Assoc, 95(7):781–8, quiz 789–90.
colon cancer in a low-risk population. Am J Epidemiol, doi:10.1016/S0002-8223(95)00217-0 PMID:7797809
148(8):761–74. doi:10.1093/oxfordjournals.aje.a009697 Subar AF, Ziegler RG, Thompson FE, Johnson CC,
PMID:9786231 Weissfeld JL, Reding D et al.; Prostate, Lung, Colorectal,
Sinha R, Knize MG, Salmon CP, Brown ED, Rhodes D, and Ovarian Cancer Screening Trial Investigators
Felton JS et al. (1998a). Heterocyclic amine content (2001). Is shorter always better? Relative importance
of pork products cooked by different methods and of questionnaire length and cognitive ease on response
to varying degrees of doneness. Food Chem Toxicol, rates and data quality for two dietary questionnaires.
36(4):289–97. doi:10.1016/S0278-6915(97)00159-2 Am J Epidemiol, 153(4):404–9. doi:10.1093/aje/153.4.404
PMID:9651045 PMID:11207159
103
Sugimura T, Wakabayashi K, Nakagama H, Nagao M long-term dietary exposure: a methyl mercury case
(2004). Heterocyclic amines: mutagens/carcinogens study. Risk Anal, 24(1):19–30. doi:10.1111/j.0272-
produced during cooking of meat and fish. Cancer Sci, 4332.2004.00408.x PMID:15027997
95(4):290–9. doi:10.1111/j.1349-7006.2004.tb03205.x Tricker AR (1997). N-Nitroso compounds and man:
PMID:15072585 sources of exposure, endogenous formation and
Sun XD, Holley RA (2011). Factors influencing gel occurrence in body fluids. Eur J Cancer Prev,
formation by myofibrillar proteins in muscle 6(3):226–68. doi:10.1097/00008469-199706000-00003
foods. Comp Rev Food Sci Food Safe, 10(1):33–51. PMID:9306073
doi:10.1111/j.1541-4337.2010.00137.x Turesky RJ, Liu L, Gu D, Yonemori KM, White KK,
Sy MM, Feinberg M, Verger P, Barré T, Clémençon S, Wilkens LR et al. (2013). Biomonitoring the cooked
Crépet A (2013). New approach for the assessment of meat carcinogen 2-amino-1-methyl-6-phenylimida-
cluster diets. Food Chem Toxicol, 52:180–7. doi:10.1016/j. zo[4,5-b]pyridine in hair: impact of exposure, hair
fct.2012.11.005 PMID:23182740 pigmentation, and cytochrome P450 1A2 phenotype.
Takachi R, Tsubono Y, Baba K, Inoue M, Sasazuki S, Cancer Epidemiol Biomarkers Prev, 22(3):356–64.
Iwasaki M et al.; Japan Public Health Center-Based doi:10.1158/1055-9965.EPI-12-1206 PMID:23329727
Prospective Study Group (2011). Red meat intake may University of Otago and Ministry of Health (2011).
increase the risk of colon cancer in Japanese, a popu- Methodology report for the 2008/09 New Zealand
lation with relatively low red meat consumption. Asia Adult Nutrition Survey. Wellington, New Zealand:
Pac J Clin Nutr, 20(4):603–12. PMID:22094846 Ministry of Health. Available from: http://www.
Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki health.govt.nz/system/files/documents/publications/
N, Varki A et al. (2003). Human uptake and incorpo- methodology-report.pdf, accessed August 2015
ration of an immunogenic nonhuman dietary sialic Uribarri J, Woodruff S, Goodman S, Cai W, Chen X,
acid. Proc Natl Acad Sci U S A, 100(21):12045–50. Pyzik R et al. (2010). Advanced glycation end products
doi:10.1073/pnas.2131556100 PMID:14523234 in foods and a practical guide to their reduction in the
Tareke E, Rydberg P, Karlsson P, Eriksson S, Törnqvist diet. J Am Diet Assoc, 110(6):911–16.e12. doi:10.1016/j.
M (2002). Analysis of acrylamide, a carcinogen formed jada.2010.03.018 PMID:20497781
in heated foodstuffs. J Agric Food Chem, 50(17):4998– Vitaglione P, Fogliano V (2004). Use of antioxidants to
5006. doi:10.1021/jf020302f PMID:12166997 minimize the human health risk associated to muta-
Tavani A, La Vecchia C, Gallus S, Lagiou P, Trichopoulos genic/carcinogenic heterocyclic amines in food.
D, Levi F et al. (2000). Red meat intake and cancer risk: J Chromatogr B Analyt Technol Biomed Life Sci,
a study in Italy. Int J Cancer, 86(3):425–8. doi:10.1002/ 802(1):189–99. doi:10.1016/j.jchromb.2003.09.029
(S I C I )10 9 7- 0 21 5 (2 0 0 0 0 5 01) 8 6 : 3 <4 2 5 : : A I D - PMID:15036011
IJC19>3.0.CO;2-S PMID:10760833 Walker R (1990). Nitrates, nitrites and
Thompson FE, Kipnis V, Midthune D, Freedman LS, N-nitrosocompounds: a review of the occurrence in food
Carroll RJ, Subar AF et al. (2008). Performance of a and diet and the toxicological implications. Food Addit
food-frequency questionnaire in the US NIH-AARP Contam, 7(6):717–68. doi:10.1080/02652039009373938
(National Institutes of Health-American Association of PMID:2079111
Retired Persons) Diet and Health Study. Public Health Ward MH, Cantor KP, Riley D, Merkle S, Lynch CF (2003).
Nutr, 11(2):183–95. doi:10.1017/S1368980007000419 Nitrate in public water supplies and risk of bladder
PMID:17610761 cancer. Epidemiology, 14(2):183–90. doi:10.1097/01.
Thompson FE, Subar AF (2013). Dietary assess- EDE.0000050664.28048.DF PMID:12606884
ment methodology. In: Coulston AM, Boushey CJ, Ward MH, Cerhan JR, Colt JS, Hartge P (2006).
Ferruzzi MG, editors. Nutrition in the prevention Risk of non-Hodgkin lymphoma and nitrate and
and treatment of disease. 3rd ed. Elsevier. doi:10.1016/ nitrite from drinking water and diet. Epidemiology,
B978-0-12-391884-0.00001-9 17(4):375–82. doi:10.1097/01.ede.0000219675.79395.9f
Tiemersma EW, Kampman E, Bueno de Mesquita HB, PMID:16699473
Bunschoten A, van Schothorst EM, Kok FJ et al. (2002). Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS,
Meat consumption, cigarette smoking, and genetic Willett WC et al. (2004). Comparison of risk factors
susceptibility in the etiology of colorectal cancer: for colon and rectal cancer. Int J Cancer, 108(3):433–42.
results from a Dutch prospective study. Cancer Causes doi:10.1002/ijc.11540 PMID:14648711
Control, 13(4):383–93. doi:10.1023/A:1015236701054 Weiss J, Gibis M, Schuh V, Salminen H (2010). Advances
PMID:12074508 in ingredient and processing systems for meat and
Toldrá F (2010). Handbook of meat processing. Oxford, meat products. Meat Sci, 86(1):196–213. doi:10.1016/j.
UK: Wiley-Blackwell. doi:10.1002/9780813820897 meatsci.2010.05.008 PMID:20619800
Tran NL, Barraj L, Smith K, Javier A, Burke TA (2004). WHO (2006). Evaluation of certain food contaminants.
Combining food frequency and survey data to quantify Sixty-fourth report of the Joint FAO/WHO Expert
104
Committee on Food Additives. WHO Technical Swiss diet: analytical method, exposure estimation
Report Series No. 930. Geneva, Switzerland: World and risk assessment. Food Addit Contam, 18(6):533–51.
Health Organization. doi:10.1080/02652030119545 PMID:11407752
WHO (2013). GEMS/Food cluster diets - 2012. A part Zukál E, Incze K (2010). Drying. Part 1, Chapter 11. In:
of the FOSCOLLAB platform for food safety data Toldrá F, editor. Handbook of meat processing. Oxford,
and information. Geneva, Switzerland: World Health UK: Wiley-Blackwell; 219–229. Available from: http://
Organization. Available from: https://extranet.who.int/ onlinelibrary.wiley.com/doi/10.1002/9780813820897.
sree/Reports?op=vs&path=/WHO_HQ_Reports/G7/ ch11/summary
PROD/EXT/GEMS_cluster_diets_2012&userid=G7_
ro&password=inetsoft123
WHO (2015a). WHO databases on food safety [online
databases]. Geneva, Switzerland: World Health
Organization. Available from: http://www.who.int/
foodsafety/databases/en/, accessed 9 July 2015
WHO (2015b). GEMS/Food contaminants [online data-
base]. Geneva, Switzerland: Global Environment
Monitoring System - Food Contamination Monitoring
and Assessment Programme, World Health
Organization. Available from: https://extranet.who.int/
gemsfood/Search.aspx
Williams P (2007). Nutritional composi-
tion of red meat. Nutr Diet, 64(s4): S11311–9.
doi:10.1111/j.1747-0080.2007.00197.x
Wood JD, Enser M (1997). Factors influencing fatty acids
in meat and the role of antioxidants in improving meat
quality. Br J Nutr, 78(01):Suppl 1: S49–60. doi:10.1079/
BJN19970134 PMID:9292774
Wood JD, Enser M, Fisher AV, Nute GR, Richardson
RI, Sheard PR (1999). Manipulating meat quality and
composition. Proc Nutr Soc, 58(2):363–70. doi:10.1017/
S0029665199000488 PMID:10466178
Wu K, Sinha R, Holmes MD, Giovannucci E, Willett W, Cho
E (2010). Meat mutagens and breast cancer in postmen-
opausal women – a cohort analysis. Cancer Epidemiol
Biomarkers Prev, 19(5):1301–10. doi:10.1158/1055-9965.
EPI-10-0002 PMID:20447922
Yaylayan VA, Locas CP, Wnorowski A, O’Brien J
(2004). The role of creatine in the generation of
N-methylacrylamide: a new toxicant in cooked meat.
J Agric Food Chem, 52(17):5559–65. doi:10.1021/
jf049421g PMID:15315400
Zeitoun MM, Ahmed SM (2011). Effect of cooking method
on the residues of natural sex steroid hormones in local
and imported meats and meat products in Al-Qassim
region. J Agril Vet Sci, 4(2):83–92.
Zetlaoui M, Feinberg M, Verger P, Clémençon S (2011).
Extraction of food consumption systems by nonneg-
ative matrix factorization (NMF) for the assessment
of food choices. Biometrics, 67(4):1647–58. doi:10.1111/
j.1541-0420.2011.01588.x PMID:21418050
Zhai F, Wang H, Du S, He Y, Wang Z, Ge K et al. (2009).
Prospective study on nutrition transition in China.
Nutr Rev, 67:Suppl 1: S56–61. doi:10.1111/j.1753-
4887.2009.00160.x PMID:19453679
Zimmerli B, Rhyn P, Zoller O, Schlatter J (2001).
Occurrence of heterocyclic aromatic amines in the
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Red Meat and

This publication represents the views and expert

LYON, FRANCE - 2018

1.1 Identification of the agents by-products such as blood. It is also important

(b) Fresh industrial processed meat products (d) Fermented sausages

Nutrient Beef Veal Lamb Mutton

(iii) Vitamins (iv) Minerals

(v) Creatine antibiotics (chlorotetracycline and oxytetracy-

Estradiol < 14 (prepubertal boys) 0.003–0.035 0.011–0.28 0.0033–0.084

(vii) Mycotoxins fat, a wide range of non-meat substances are

Fig. 1.1 Examples of environmental micropollutants potentially found in red and processed

2,3,7,8-Tetrachlorodibenzo-p-dioxin Polychlorinated dibenzofuran Polychlorinated biphenyls

(iii) Fermentation of fat. The method has an impact on the forma-

Table 1.4 Definition of cooking methodsa

Cooking methodb Definition

R = H (IQ) R 1 , R 2 = H, R 3 = Me (8-MeIQx) PhIP

R = Me (MeIQ) R 1 , R 3 = Me, R 2 = H (4,8-DiMeIQx)

Principal pyrolytic HAAs found in red and processed meats

Harman Norharman Trp-P-1 Trp-P-2

Common abbreviation Full name

Cooked meat Concentrations of HAAs (ng/g)

Red meat and processed meat

Benzo[a]pyrene Chrysene Benz[a]anthracene Benzo[b]fluoranthene

Fig. 1.4 Structure of N-glycolylneuraminic representative processed meats are given in

Fig. 1.5 Structures of N-nitroso compounds commonly found in processed meats

NDMA NDEA NPIP NPYR

Table 1.7 Polycyclic aromatic hydrocarbons cited in this Monograph

Common name (name used in this volume) CAS registry No.

PAH Cooking/ Beef Pork Chicken

Meats Total iron (mg/100 g) % Haem iron % Loss

Meat Cooking/processing method Advanced glycation end product (kU/110 g)

Beef Raw 707

The EPIC study concluded that red meat

Table 1.12 N-Nitroso compounds commonly found in processed meat

Common abbreviation Full name CAS registry No.

Table 1.13 Major sources of dietary N-nitrosamines in processed meats

Processed meat Concentration of nitrosamines (µg/kg)

IARC MONOGRAPHS – 114

Red meat and processed meat

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Red meat and processed meat

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Red meat and processed meat

IARC MONOGRAPHS – 114

Red meat and processed meat

IARC MONOGRAPHS – 114

Red meat and processed meat

IARC MONOGRAPHS – 114

Red meat and processed meat

IARC MONOGRAPHS – 114

Red meat and processed meat

Red meat and processed meat

IARC MONOGRAPHS – 114

Red meat and processed meat

IARC MONOGRAPHS – 114

Red meat and processed meat

such as curing, smoking, or drying (Santarelli (b) Validation and calibration

(i) Heterocyclic aromatic amines correlation coefficients of HAA intake, assessed

(e) Case–control studies 1.4.2 Biological markers