Almejas 3
Almejas 3
Almejas 3
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and
environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published
by nonprofit societies, associations, museums, institutions, and presses.
Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of
BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.
Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries
or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research
libraries, and research funders in the common goal of maximizing access to critical research.
Journal of Shellfish Research, Vol. 37, No. 4, 695–708, 2018.
ABSTRACT The Nutrient Database for Standard Reference published by the U.S.D.A. describes molluscan shellfish as an
excellent source of vitamin B12, omega-3 fatty acids, choline, iron, selenium, and zinc. Edible molluscs consist primarily of
mussels, clams, scallops, and oysters and are naturally low in carbohydrate, as well as total and saturated fat. With regard to
omega-3 fatty acids, iron, selenium, and zinc, the nutrient value of some shellfish is superior to land-based protein sources, such as
beef, chicken, and pork. Unfortunately, adverse human health considerations need to be noted because of naturally occurring
pathogens, particularly Vibrio species, and algal toxins (brevetoxin, saxitoxin, and domoic acid) that may be present in these
shellfish, as well as fecal-associated viruses (hepatitis A and norovirus) and bacteria (Salmonella) as a consequence of
contamination of shellfish harvest sites. Other environmental contaminants (mercury, methylmercury, and polychlorinated
biphenyls) may bioaccumulate in molluscan shellfish tissues as part of their filter feeding behavior and have potential health
implications. Cooking molluscan shellfish greatly reduces the risk of foodborne infections and increases the nutrient value because
of water loss; however, some vitamins are destroyed by cooking and natural toxins and environmental contaminants are not
always eliminated by normal cooking temperatures. Coastal monitoring of water quality and postharvest processing of some
products should help mitigate risks associated with shellfish consumption and promote a safer, nutrient-rich product.
KEY WORDS: food safety, minerals, molluscan shellfish, nutrition, omega-3 fatty acids, vitamins
695
696 WRIGHT ET AL.
Water
Protein
Carbohydrates
Source: USDA National Nutrient Database for Standard Reference, Release 28. The default age–sex group reference is a male age of 31–50 years based on a 2,200-calorie per day diet. <dl, below
detection limit of assay; NR, not reported by USDAÕs full report. ‘‘Excellent sources’’ based on DV are displayed in bold.
* Significantly higher fat, saturated fat, and 18:2, likely because of fatty acid profile of frying oil.
697
698 WRIGHT ET AL.
consisting of three fatty acids connected to a glycerol backbone. For example, the shorthand notation for DHA is 24:6w3, which
Fat contains 9 kcal/g, which is substantially a higher energy describes the fatty acid as having 24 carbons with six double
value than that of carbohydrates or proteins (both 4 kcal/g). bonds beginning at the third carbon counted from the methyl
Although often disparaged because of its caloric value, dietary (or omega) end. Figure 2 diagrams the fatty acid nomenclature
fat is essential for biological membranes, contributes to the by the omega system. In addition, it is important to understand
transport and absorption of fat-soluble vitamins, and is in- how the human body uses fatty acids. When fats are consumed
volved with many more vital functions related to human met- as a mixture of triglycerides, pancreatic lipase liberates free fatty
abolic activity. The American Heart Association recommends acids that enter the bloodstream. In different cellular com-
consuming 25%–35% of total calories from fat (AHA 2018). partments, mainly in microsomes, fatty acids undergo a series of
By definition, saturated fats contain no double bonds in their elongation with carbon atoms and desaturation by double bond
carbon chains and are typically solid at room temperature addition through a cascade mediated by specific metabolic
(25°C). Most fatty acids in land-based plant and animal tissues elongases and desaturases that convert fatty acids in the body.
are 16- or 18-carbon long fatty acids with zero to three double The position of the first set of double bonds connected from the
bonds. From a nutritional standpoint, the only fatty acids essential methyl (or w/omega) end of the molecule remains unchanged.
for human health are linoleic (18:2w6) and linolenic (18:3w3) acids In other words, an omega-3 fatty acid will remain an omega-3
because mammals lack the enzymes necessary to desaturate fatty fatty acid of different carbon chain lengths and level of satu-
acids beyond the C-9 position in the fatty acidÕs carbon chain (Berg ration after being converted in human metabolic pathways.
et al. 2002). The American Heart Association (2015) suggests This explains why linoleic (18:2w6) and linolenic (18:3w3) fatty
that the amount of saturated fatty acids in a healthy diet should acids are considered essential to human health. Linoleic acid
not exceed 10% of total calories of your daily dietary intake and undergoes carbon chain elongation and addition of double
that trans-fatty acids should be avoided because of the risk as- bonds to form arachadonic acid (20:4w6), which is involved
sociated with heart disease and stroke (AHA 2015). with prostaglandin and hormone formation.
As shown in Table 1, raw or steamed molluscan shellfish are Figure 3 describes the enzymatic cascade in the human body
considered low in fat (0.96–4.5 g per 100 g serving) as compared for the formation of omega-6 and omega-3 fatty acids. Un-
with broiled or roasted land-based meats (3.6–18.7 g). They are fortunately, the metabolic conversion of omega-3 fatty acids in
also notably lower in saturated fats (<1 g) compared with the body is not very efficient. For example, typically less than
chicken, pork, or beef (1–7.3), although cooking methods such 15% of linoleic acid (18:2w6) is metabolically converted to
as breading and frying will greatly increase the fat content DHA (22:6w3) (NIH-ODS 2016). Therefore, direct consump-
(USDA 2015). Fatty acid composition is also striking and tion of dietary EPA and DHA are thought to have the greatest
comprises an abundant nutrient database for researchers to omega-3–related impact on human health. Long chain omega-3
compare seafood species (Rittenschober et al. 2013). As dis- fats, such as DHA and EPA, are thought to lower the incidence
cussed in the following paragraphs, the omega-3 fatty acids in of cardiovascular disease, atrial fibrillation, telomere shorten-
particular are lacking in beef, pork, and poultry but are in ing, and metabolic syndrome in humans (Farzaneh-Far et al.
abundant in both fish and shellfish. 2010, Baik et al. 2010, Nielsen et al. 2012, Lund 2013). Beneficial
observations related to dietary omega-3 consumption and car-
Omega-3 Fatty Acids and Human Health diovascular disease may be due to reduced blood platelet re-
activity, reduced plasma viscosity, and the reduced production
In the early 1980s, several studies concluded that native of cytokines. Docosahexaenoic acid makes up approximately
populations in Greenland and Japan were less susceptible to 90% of the omega-3 fatty acids in the gray matter of the brain
heart attacks compared with those in North America (Bang & (Weiser et al. 2016). The human brain consumes 20% of the
Dyerberg 1980, Kagawa et al. 1982). It was postulated that their bodyÕs overall energy consumption, although only weighing two
diet of cold water seafood, even though high in fat, was the percent of the average human body weight (Bradbury 2011).
major reason for this phenomenon. The relationship of seafood Nutritionally speaking, FDA recommends adequate intake
consumption to human health was further investigated over the levels for dietary omega-3 fatty acids at 1.6 g for males and 1.1 g
next 20 y, as studies attempted to define the reason behind the for females. Beef, chicken, and pork contain very little omega-3
suspected health benefits in populations that consumed mostly fatty acids. Thus, seafood is an essential dietary source of these
seafood. Results indicated that omega-3 fatty acid consumption nutrients. The 2015–2020 United States Department of Agriculture
was the main dietary contributor to increased cardiovascular
health in the native population in Greenland and Japan. Fur-
ther studies have indicated that omega-3 fatty acids have car-
dioprotective and potent anti-inflammatory effects in the
human body (OÕKeefe & Harris 2000).
Omega-3 fatty acids that are thought to play major roles in
the human health include alpha-linolenic acid, eicosapentaenoic
acid (EPA), and docosahexaenoic acid (DHA). To understand
the nutritional implications of these omega-3 fatty acids, their
chemical structure warrants explanation. The shorthand nu-
meric fatty acid nomenclature rules describe the number of
carbons in the fatty acid chain, followed by the number of
double bonds in the molecule and separated by a colon (:), and Figure 2. Diagram of the linoleic acid molecule to describe nomenclature
then the omega-position of the first carbon from the methyl end. (18:2v6).
NUTRITIONAL AND BACTERIAL COMPOSITION OF MOLLUSCAN SHELLFISH 699
have also reported that oysters and other molluscs are relatively
low in cholesterol (Childs et al. 1987, Nettleton & Exler 1992).
In fact, Childs et al. (1987) observed the impact of three animal
proteins on cholesterol absorption in the body and discovered
that males fed an oyster/clam diet showed lowered choles-
terol adsorption compared with a diet of chicken meat. Eastern
oysters (Crassostrea virginica) have slightly less cholesterol
(30 mg/100 g) compared with Pacific oysters (Crassostrea gigas)
(48 mg/100 g) (Nettleton & Exler 1992). In general, cholesterol
values reported by the USDA National Nutrient Database
showed that molluscs varied with preparation and were highest
in steamed, followed by raw and canned at 56, 28, and 3 mg/100 g,
respectively (see Table 1).
Calcium
(USDA) guidelines suggest that eight ounces (224 g) of seafood
per week or 250 mg/day each of EPA and DHA (500 g total) is a Calcium is the most abundant metal in the human body and
sufficient amount to provide health benefits (USDA 2015). The is essential to bone biogenesis, as deficiencies can cause osteo-
FDA also specifies that the labels of dietary supplements should porosis. It is required for intracellular signaling and neural
exceed a daily intake of EPA and DHA over 2 g. A 3-oz serving transmission. It is also an essential component of the calcium
of salmon cooked provides about 1.6 g omega-3 fatty acids, carbonate shells of molluscan shellfish and, as such, is recruited
whereas a typical 1,000 mg fish oil dietary supplement provides from seawater and deposited at fairly high concentrations in
180 mg EPA and 120 mg DHA (NIH-ODS 2016). their tissues. Levels of calcium in shellfish are 2- to 10-fold
Nutritional recommendations for omega-3 consumption higher than those found in beef, chicken, or pork.
have focused on oily fish, but mussels and oysters can be ex-
cellent sources for total omega-3 fatty acids (Table 1). The types Iron
of fatty acid vary among species, but shellfish contain mostly
EPA and DHA. Scallops contain little of omega-3 fatty acids, The primary metabolic function of iron is the transport of
but oysters can exceed 500 mg for total omega-3 fatty acids. oxygen throughout the body as a complex with hemoglobin and
as a cofactor for electron transport (Eguchi & Saltman 1987).
Cholesterol
Iron deficiency is called anemia, and symptoms include fatigue,
weakness, and difficulty maintaining body temperature (Miller
Clinical investigations over many years have linked choles- 2013). Several enzymes cofactor with iron, especially for oxi-
terol to heart disease and atherosclerosis (Libby et al. 2000). dative phosphorylation in the energy pathway. Dietary iron is
Recent research findings suggest that dietary cholesterol does stored in mammals primarily as a complex with ferritin, a protein
not play as large a role in atherosclerosis as previously thought complex with multiple subunits. Transferrin is the protein that
(Lecerf & de Lorgeril 2008). In addition, the human body re- transports iron within the blood where it is deposited in ferritin
quires cholesterol, which is found in every cell in the body and is for storage at other locations, primarily the liver and muscles.
an important precursor for many vital compounds required for Ascorbic acid (vitamin C) stimulates the synthesis of ferritin and
the normal human body function (Simons & Ikonen 2000). For the absorption of dietary iron (Hallberg et al. 1989).
example, cholesterol is involved in the synthesis of sex hor- United States Department of Agriculture National Nutrient
mones (estrogen and testosterone), growth, and cellular main- Database shows that raw oysters (4.6–5.8 mg/100 g) and mus-
tenance. Approximately 75% of the cholesterol in the human sels (3.95 mg/100 g) are an excellent source of iron (Table 2).
body at any given time is produced primarily by the body itself, Clams (1.62 mg/100 g) contain less iron than oysters but are
in the liver, with the other 25% derived from dietary sources. still a good source according to DV calculations. When cooked,
Overall, molluscan shellfish contain lower levels of cholesterol the amount of available iron actually increases between 65%
than beef, chicken, or pork (Phillips et al. 2012). Researchers and 100%. For example, breaded and fried clams contain the
700 WRIGHT ET AL.
TABLE 2.
Selected mineral content of molluscan shellfish, beef, chicken, and pork and available dietary guidelines for 2015 to 2020.
Source: USDA National Nutrient Database for Standard Reference, Release 28. The default age–sex group reference is a male age of 31–50 years
based on a 2,200-calorie per day diet. <dl, below detection limit of assay; NR, not reported by USDAÕs full report. ‘‘Good sources’’ based on DV are
displayed in italics. ‘‘Excellent sources’’ based on DV are displayed in bold.
highest levels of iron reported (13.91 mg of iron per 100 g Approximately, 25% is involved with muscle function. As it is
sample). Scallops (0.38 mg/100 g) contain less than half the essential to many biochemical mechanisms in the human body,
levels of beef, chicken, and pork, whereas oysters and clams magnesium is an important metabolic mineral (Bergman et al.
contain several times the amount for land-based meats. Farmed 2009). Magnesium is involved with nerve and muscle mainte-
oyster species are reported to have slightly higher iron levels nance and function, supports immunity, healthy heart rate, and
compared with wild caught, although Nettleton did not find any interacts with calcium in bone maintenance and keeps calcium
significant differences in farmed versus wild oysters for any dissolved in blood (Grzebisz 2011). Magnesium is although
nutrient they investigated (Nettleton & Exler 1992). Cooked thought to be involved in blood glucose levels and energy pro-
clams and cooked beef contain similar amounts of iron. duction. Steamed and canned oysters provide a good source of
In some individuals, a genetic abnormality results in over- magnesium. Fried scallops are also a good source of magnesium
absorption of iron and consequently iron overload from a and contain 18 to 58 mg/100 g, while other molluscan shellfish
condition referred to as hemochromatosis. These persons must ranged from 14 to 37 mg/100 g.
avoid iron-rich food and may require chelation therapy or
phlebotomy. Interestingly, persons with hemochromatosis are Manganese
also highly susceptible to fatal Vibrio vulnificus disease. In mice,
iron overload reduced the infectious dose from about 100,000 to Manganese is involved in enzyme function and is even a
theoretically one bacterium (Wright et al. 1981). Thus, consumption component of several enzymes, such as arginase, concanavalin
of raw oysters is particularly a concern to persons with hemo- A, glutamine-synthase, and many others (Horning et al. 2015).
chromatosis and should be avoided. There appears to be a number of roles that manganese plays in
osteoporosis, diabetes, and seizure disorders. In addition, toxic
Magnesium levels of manganese in water have also been reported. The U.S.
Environmental Protection Agency has a 50 mg/L maximum
The human body contains approximately 25 g of magne- allowable level of magnesium in drinking water (EPA 2018b).
sium. Magnesium is primarily found in bones and makes up Manganese toxicity may result in moderate to severe neuro-
60%–65% of the total magnesium in the body (Grzebisz 2011). logical symptoms to those similar to ParkinsonÕs disease
NUTRITIONAL AND BACTERIAL COMPOSITION OF MOLLUSCAN SHELLFISH 701
(Aschner et al. 2009). Clams, cooked oysters, and mussels are Zinc
either a good or excellent source of dietary manganese. Raw
Zinc is a major contributor to health and nutrition by
Pacific oysters and cooked eastern oysters vary between being
boosting immune function, regulation of aging, atherosclerosis,
ranked good to excellent sources of manganese. Canned clams
and autoimmune diseases (Samman 2007). There may also be
contain moderately low levels of manganese.
other roles zinc plays in cancer, diabetes, AlzheimerÕs disease,
and other age-related conditions (Choy et al. 2002, Samman
Phosphorus
2007, Sandstead 2012, Guan et al. 2015, Maulvault et al. 2015).
Phosphorus is necessary as an essential mineral that is pri- Oysters are very high in zinc. Fresh and canned mussels con-
marily used for growth and repair of human cells and tissues, as tained the highest samples of zinc in a study conducted by
well as healthy energy levels (Bergman et al. 2009, Kraft 2015). Olmedo et al. (2013a). United States Department of Agriculture
Approximately 85% of all the phosphorus in the body is a (Table 2) reported that the zinc concentration in canned eastern
hydroxyapatite complex with calcium, which is responsible for oysters is 91 mg per 100 g of sample, which is 500 times more
bone hardness (Bergman et al. 2009). Vitamin D is required to than the DV for zinc.
absorb phosphorus efficiently by acting as a cofactor for
several human metabolic functions. Nearly all clams, mussels, VITAMINS ASSOCIATED WITH MOLLUSCAN SHELLFISH
and scallops are a good to excellent source of phosphorus. AND HUMAN HEALTH
Raw and steamed scallops are excellent sources of phospho- Daily values for selected vitamin content of molluscan
rus. Phosphorus levels are highest in steamed scallops, but shellfish are shown in Table 3 and are based on the Available
clams and mussels cooked by moist heat also contain excellent Dietary Guidelines (2015 to 2020) from the USDA National
sources of phosphorus. Most molluscan shellfish evaluated in Nutrient Database. These guidelines describe ‘‘good’’ and
this review are a good source of phosphorus, as are nearly all ‘‘excellent’’ amounts for DV, and this terminology is used in the
land-based animals. Pork is an excellent source of phospho- following paragraphs to reflect these guidelines. A ‘‘good’’ nu-
rus, but higher phosphorus values are found in clams and tritional source would contribute 10%–19% of the DV, whereas
scallops. an ‘‘excellent’’ source would provide 20% or higher of a par-
ticular nutrient.
Potassium
TABLE 3.
Selected vitamin content of molluscan shellfish, beef, chicken, and pork and available dietary guidelines for 2015 to 2020.
Source: USDA National Nutrient Database for Standard Reference, Release 28. The default age–sex group reference is a male age of 31–50 years
based on a 2,200-calorie per day diet. <dl, below detection limit of assay; NR, not reported by USDAÕs full report. ‘‘Good sources’’ based on DV are
displayed in italics. ‘‘Excellent sources’’ based on DV are displayed in bold.
Vitamin B3 deficiency can cause nausea, skin and mouth le- foods (NIH-ODS 2018c). Folate is a coenzyme of single carbon
sions, anemia, headaches, and lack of energy (USNLM 2018b). in nucleic acid synthesis and the metabolism of amino acids. It is
Cooked clams, steamed oysters, and cooked mussels are ex- especially important in the conversion of homocysteine to me-
cellent sources of vitamin B3; however, its levels are much lower thionine in the synthesis of methyl donor, S-adenosyl-
than in beef, chicken, and pork. For example, roasted chicken methionine (Bailey et al. 2001). Raw mussels are the only
contains approximately 280% more vitamin B3 than the highest good source of dietary folate among molluscs, whereas oysters
value for molluscan shellfish (steamed Pacific oysters). are notably lacking in this nutrient (0.1–0.2 mg/100 g). Steamed
mussels contain almost double the concentration of folate
Vitamin B12 (Cobalamins) found in raw mussels (76 and 42 mg/100 g, respectively). In
comparison, land-based proteins range from 3 to 11 mg/100 g.
Vitamin B12 is a water-soluble vitamin that is especially
important in DNA synthesis and regulation (Ryan- Choline
Harshman & Aldoori 2008). It is required for proper red
blood cell function, promotes a healthy neurological system, Choline is considered an essential micronutrient and is vital
and plays a role in fatty acid metabolism (NIH-ODS 2018b). for early brain development. It is found in cell membranes as
Amino acid metabolism is also mediated by vitamin B12. Clams part of the headgroup of phospholipids. Although small
and mussels are excellent sources of vitamin B12. Steamed amounts of choline are produced in the liver as phosphatidyl-
clams contain 98.9 mg of vitamin B12, which is more than choline, choline must be obtained from the diet to meet human
double the next highest level in fried clams. Oysters and scallops requirements (Ziesel & da Costa 2009). It is also the precursor
also provide a good source of vitamin B12. for acetylcholine, an important neurotransmitter involved in
memory function and movement and supports cellular meth-
Folate/Folic Acid
ylation reactions, including genomic methylation (Wallace &
Fulgoni 2017). Dietary choline levels tend to be high in canned
Folate is a water-soluble B vitamin that is either naturally clams and oysters cooked under dry heat. Chicken and beef
present (particularly in leafy greens) and/or fortified in some contain good or excellent levels of dietary choline. The choline
NUTRITIONAL AND BACTERIAL COMPOSITION OF MOLLUSCAN SHELLFISH 703
content of oysters and clams are comparable with that of beef fatal. Although this organism is responsible for only 19% or
and chicken. 13% of infections, depending on the reporting source, it causes
greater than 80% of mortality associated with seafood (Newton
MOLLUSCAN SHELLFISH AND SEAFOOD SAFETY et al. 2012). Diarrheal symptoms are rare, but overwhelming
Although nutritional benefits related to consumption of sepsis may follow ingestion of seafood or wound infections that
molluscan shellfish are clearly evident, there are food safety can be fatal within 48 h. The vast majority of persons with
considerations related to these seafood products, particularly foodborne V. vulnificus disease have ingested raw oysters and
when consumed raw. Filter-feeding molluscs can concentrate have some type of underlying condition, such as hemochro-
pathogens and toxins that are detrimental to human health. matosis (iron overload), liver disease, diabetes, and AIDS.
Seafood is responsible overall for less than 7% of illnesses or These persons should avoid consumption of raw oysters and
deaths from foodborne outbreaks in the United States. (Painter also exposure of open wounds to seawater, fish, or shellfish, as
et al. 2013). These data excluded Vibrio vulnificus, which is the their fatality rate exceeds 50% for infected individuals.
leading cause of death from infectious disease related to seafood Vibrio alginolyticus is the third most common cause of vib-
consumption; however, the incidence of disease is rare (124 riosis is the United States. Although this species is considered an
cases in 2014) relative to Salmonella (>million cases/year) emerging foodborne pathogen, it is more commonly implicated
https://www.cdc.gov/nationalsurveillance/pdfs/covis-annual- in wound and ear infections. Symptoms include gastroenteritis
summary-2014-508c.pdf. and occasionally septic shock. Other Vibrio spp. associated with
Seafood safety concerns are largely related to risks associ- consumption of raw shellfish include Vibrio cholerae, but cases
ated with the consumption of raw shellfish. Many of these risks are rare and mostly sporadic, although a small outbreak (n ¼
could be avoided simply by cooking the product; however, a 11) attributed to consumption of raw oysters was reported in
culture of consuming oysters raw dates back to early human 2011 (Onifade et al. 2011).
populations, as evidenced by the discovery of massive shell
middens that are an archaeological testament to raw oyster Other Bacterial and Viral Pathogens Associated with Seafood
consumption. These mounds of mollusc shells are generally Salmonella enterica infections have been associated with
located either nearshore or underwater and are thought to be molluscan shellfish consumption, and a survey of oysters har-
directly associated with molluscan shellfish consumption in vested from 36 bays in the United States found that 7.4%
villages along coastal areas. Molluscan shellfish were both a harbored the bacterium, primarily from the serogroup Newport
food source and a useful tool, as shell by-product was used for (78%) (Brands et al. 2005). Furthermore, an FDA market
cutting and digging applications (Smith 2015). survey (DePaola et al. 2010) detected Salmonella in oyster
products (1.5%), and this survey also reported the prevalence of
Vibrio Species two viruses most often associated with disease related to shell-
Most of the infectious agents associated with molluscan fish consumption, namely, norovirus (3.9%) and hepatitis A
shellfish safety are naturally occurring in the estuarine and virus (4.4%) (Rippey 1994).
marine environment, although pathogens can be transmitted
through fecal sources of contamination. Vibrio species are the Toxic Algae
primary indigenous pathogens and account for 75% of seafood- Toxic algal blooms present a challenge to the seafood in-
related infectious disease (Scallan et al. 2011). Vibrios are dustry and are particularly concerning for consumption of
present ubiquitously in coastal habitats and comprise the nat- filter-feeding molluscan shellfish that may accumulate these
ural microflora of shellfish. Risk of Vibrio-related diseases has toxins (Basti et al. 2018). The primary toxic species are di-
been shown to increase greatly with warming water tempera- noflagellates, which are classified by their toxic repertoire and
ture, as cases are more prevalent in summer months. Also, include neurotoxic shellfish poisoning (Karenia brevis), para-
warming of coastal waters due to climate change is likely to lytic shellfish poisoning (mixed species, including Alexandrium
contribute to increased disease incidence (Vezzulli et al. 2012). spp.), and diarrhetic shellfish poisoning (Dinophysis and Pro-
The majority of foodborne vibriosis in the United States is rocentrum species). Symptoms range from mild diarrhea to se-
attributed to Vibrio parahaemolyticus, accounting for 45% or rious neurological complications, such as mouth tingling,
54% of cases from 1996 to 2010 based on COVIS or FoodNet, slurred speech, respiratory distress, and paralysis. Species of the
respectively (Newton et al. 2012). This bacterium generally diatom Pseudo-nitzschia cause amnesic shellfish poisoning,
causes a mild diarrhea but is frequently associated with large which can produce short-term memory loss. The ciguatera
outbreaks of disease. CDC estimates 128 cases are not reported toxin-producing Gambierdiscus spp. are more likely associated
for every confirmed illness; thus, this organism is largely re- with fish poisoning from consumption of large fish high in the
sponsible for the estimated 80,000 cases/year of Vibrio in- food chain than they are with shellfish poisoning.
fections in the United States of which 65% are thought to be
foodborne. Disease incidence varies from year to year but is Mercury Poisoning
most common in the Pacific northwest and North Atlantic
states, and V. parahaemolyticus monitoring programs have been Coal-burning power plants are a dominant source of human-
used for disease prediction and guidance for harvest closure in caused mercury emissions in the atmosphere and account for
some areas. ;40% of domestic (5% global) mercury emissions in United
The second most common cause of vibriosis in the United States, remaining as either deposited in the soil and water (25%)
States is Vibrio vulnificus, which produces a much more serious or as a component of the global biogeochemical cycle (75%)
disease that frequently becomes systemic and can be rapidly (EPA 2018a). Marine bacteria (Pseudomonas spp.) convert
704 WRIGHT ET AL.
elemental mercury to methylmercury in aquatic environments and shellfish draw attention to these risks and have been vali-
(Blackmore & Wang 2004, De et al. 2007). As a result, most dated by successful lawsuits against seafood restaurants that
common organic mercury compound found in the environment ensure labels are informative and visible; however, it should be
is a methyl mercury–cysteine complex (Berry & Ralston 2008). noted that unlike other food industry, shellfish suppliers and
Several investigators have researched seleniumÕs role in binding retailers have long maintained a tracking system that tags the
heavy metals (especially mercury), potentially reducing toxicity location and harvest date for all oysters to facilitate trace-back
(Cuvin-Aralar & Furness 1991). Also, selenium compounds, investigations and prevent large outbreaks (Wright et al. 2009,
particularly selenium P, bind mercury to decrease toxicity NSSP 2015).
(Cuvin-Aralar & Furness 1991, Yoneda & Suzuki 1997,
Chapman & Chan 2000, Raymond 2004, Ralston et al. 2008); Post-Harvest Processing
however, severe mercury poisoning after bioaccumulation of To address problems associated with the consumption of
mercury in molluscan shellfish and finfish from dumping of raw molluscan shellfish, the National Shellfish Sanitation Pro-
industrial wastewater may expose pregnant women to mercury gram promoted and, in some cases, mandated harvest time–
or methylmercury and could impact the health of the fetus temperature controls, specific storage parameters, and PHP
(Wooltorton 2002), as there is no effective treatment for meth- methods to reduce the food safety risk. This information is
ylmercury exposure. A recent advisory by the FDA suggests provided in detail at the website for the Interstate Shellfish
that women of childbearing age, especially if breastfeeding or Sanitation Conference (http://www.issc.org/). One method
pregnant, eat two to three servings of fish per week from the commonly used in Europe is depuration or wet storage using
‘‘best choices list’’ (FDA 2017a), which includes clams, oysters, sanitized seawater to ‘‘flush’’ out filter-feeding shellfish (NSSP
and scallops, whereas mussels are not listed in the advisement 2015). Although this method is effective in removing fecal-
document. associated bacteria, Vibrio spp. are not eliminated. PHP
methods now in practice in the United States include thermal
Shellfish Safety Monitoring processing, freezing, irradiation, and high hydrostatic pressure
(Wright et al. 2009, Wright & Schneider 2010). These methods
In general, safety of shellfish in the United States is moni- are generally effective and will reduce levels of Vibrio spp. to the
tored at harvest and is based on water quality standards de- required nondetectable level; however, they all have the disad-
termined by the FDA and the Intestate Shellfish Sanitation vantage of killing the mollusc, and thus require additional
Conference (www.issc.org/home) and described in the National storage and packaging protocols for the product to be served
Shellfish Safety Program Guide (NSSP 2015). Coastal states in as a ‘‘on the half shell.’’
the United States track fecal indicator bacterial (fecal coliforms Alternatively, shellstock can be transferred from estuaries
or Escherichia coli) to determine open and closing of harvest with relatively low salinity (1–10 ppt) and high Vibrio levels
areas. Heavy rainfall can cause nonpoint source pollution and to more off-shore sites with higher salinity and lower Vibrio
may instigate closures. California now monitors Vibrio para- levels. The process is called relaying and has been shown to be
haemolyticus levels that indicate increased risk and precipitate effective in some cases but may not be suitable for all Vibrio
cessation of shellfish harvesting. Some states also monitor di- species, as some (Vibrio parahaemolyticus in particular) has
rectly for toxic algal species. For example, Florida Department higher salinity tolerance. If PHP is used to reduce human
of Environmental Protection does periodic sampling for algal pathogens in molluscan shellfish, the dealer must use the
species and maintains a hot line for reporting blooms (https:// process under a seafood hazard analysis critical control point
floridadep.gov/dear/algal-bloom/content/algal-bloom- plan and validate that it achieves a minimum 3.52 log re-
sampling-results). duction of viable bacteria and reduces the level of Vibrio
Health considerations for Vibrio vulnificus are not addressed vulnificus and V. parahaemolyticus to nondetectable levels
by monitoring, as the organism is found naturally in coastal (Baker 2016). A novel method using a derivative of chitin in
waters and is not a result of fecal contamination. The pres- the form of chitosan microparticles was recently described
ence of V. vulnificus (or other pathogens) does not change the (Fang et al. 2015) and was effective against all the three major
sensory attributes of molluscan shellfish, as these are not pathogenic Vibrio species to achieve the required reductions
spoilage organisms and would be essentially impossible to de- while leaving the oyster viable; however, efficacy of chitosan
tect even in an oyster with high levels of Vibrio spp. by visual for Salmonella was inhibited in the presence of sea salt (Fan
inspection, taste, or smell (Mouzin et al. 1997). Bacterial and et al. 2017).
viral contamination of both raw and cooked seafood during
PHP or storage have been reported and also present risks that Molluscan Shellfish and Cooking
are not prevented by the current system of monitoring (Baker
2016). Fried and steamed oysters are commonly consumed in the
It appears that most of the general public understands that United States, but raw remains the number one method of
there is a certain level of risk when raw oysters are consumed, consumption (Flattery & Bashin 2004). In other countries and
but a survey conducted by the ISSC in 2002 noted that there cultures, clams, mussels, and scallop meats are also frequently
were several health risks that were not well known to raw oyster consumed raw. In the United States, clams, mussels, and scal-
consumers with certain underlying medical conditions, such as lops are mostly prepared by sauteing, frying, broiling, and
diabetes. In addition, some raw oyster consumers have the incorporated in a soup or chowder. The USDA Nutrient Da-
general knowledge that oysters may collect and concentrate tabase for raw oysters, clams, mussels, and scallops (Tables 1–3)
bacteria and virus particles naturally because of the way they compares raw versus preparation by several cooking and/or
feed (Uchida et al. 2017). Warnings on menus serving raw fish preservation methods. The nutritional content for cooked food
NUTRITIONAL AND BACTERIAL COMPOSITION OF MOLLUSCAN SHELLFISH 705
appears to increase after cooking because of water loss. Cooked other off-flavors (Kinsella 1987). There are several positive as-
seafood will lose some level of moisture (even if steamed or pects to frying foods, as it introduces additional flavors, reduces
boiled), resulting in nutrient concentration effects unless ther- moisture, changes in texture, and eliminates pathogenic bacte-
mal degradation or loss from edible tissue. Some B vitamins are ria. A restaurant or food processor commonly change the oil
particularly heat labile (Nettleton & Exler 1992). Domingo enough to minimize any off-flavors that come from the frying
(2016) studied common cooking procedures and their effect on process. It is also unlikely that toxic levels of aldehydes would
levels of environmental contaminants. Results suggest that not be consumed at high enough concentrations to have health
common cooking methods (boiling, frying, grilling, and roast- implications because the consumer would likely not eat it be-
ing) may reduce the level of organic contaminants in the cooked cause of the rancid flavor of the fried seafood.
product because these residues are present in fatty tissues that
melt during cooking and thus are not consumed. CONCLUSIONS
FDA (2017b) described guidelines for cooking molluscan
shellfish to ensure food safety. Unless previously processed, Molluscan shellfish, such as oysters, clams, mussels, and
shellfish are sold live and should be examined before cooking scallops, provide an excellent dietary source of various health-
for open shells that do not close, as product with open shells are related nutrients that may not be available in land-based protein
likely dead. Dead shellfish decompose rapidly, increasing the sources. The commonly consumed products are naturally low in
likelihood of contamination with pathogenic bacteria. To boil fat, saturated fat, and cholesterol, whle providing adequate
molluscan shellfish in the shell, cook until the shells are open amounts of heart-healthy omega-3 fatty acids at levels that meet
and continue boiling for five more minutes. When steaming, do suggested daily intake amounts. Frequent consumption of raw
so until the shells open, then continue for an additional 10 min. or cooked shellfish, particularly oysters and mussels, provides a
If the shellfish do not open during cooking, do not eat them as diet that is rich in EPA and DHA and exceeds levels found in
they may have been dead or injured before cooking. If the oyster beef, chicken, and pork by 200%.
meat is already shucked from the shell, boil for at least 3 min or Health benefits or other attributes that are thought to be
until the edges begin to curl. Deep-fat frying of shucked oysters obtained from eating raw, as compared with cooked, molluscan
(whether breaded or not) should be at an oil temperature of shellfish need to be balanced by potential risks, particularly for
375°F/190°C. Shucked oysters can also be broiled when the individuals with immune deficiency or iron overload conditions
heating sources is approximately 3 inches from the top of the that increase susceptibility to fatal Vibrio vulnificus disease.
oyster for at least 3 min. Cooking essentially eliminates the risk of infectious diseases
Some health-related considerations from consuming fried associated with consumption of raw seafood and increases the
molluscs include increasing the fat concentration from oil up- nutrient composition by virtue of water loss. Although marine
take in the muscle tissue. Also, most fried foods are breaded toxins common to molluscan shellfish will not likely be dena-
which increases carbohydrates, calories, and additional frying tured at normal cooking temperatures, water quality monitor-
oil uptake. Furthermore, frying oil can become oxidized after ing by state regulatory agencies reduces the potential risk for
sufficient use, and oxidized fat consumption is also associated human exposure by mandating closure for suspect harvest
with negative health implications due to formation of toxic al- areas. In addition, molluscan shellfish suppliers can use post-
dehydes (Viau et al. 2016). Soybean oil, canola oil, or frying oil harvest techniques to lower the risk of harmful bacteria, toxins,
blends, commonly used for frying seafood, are also subject to or heavy metals (Greig & Wenzloff 1978, Anacleto et al. 2015,
auto-oxidation after if improperly stored. Volatile off-flavors Baker 2016). Finally, the risk to healthy individuals from
are formed because of accelerated oxidative rancidity during consuming cooked molluscan shellfish is extremely low,
repeated frying that forms aldehydes, ketones, alcohols, car- whereas nutritional benefits are uniquely abundant, especially
boxylic acids, and other organic compounds which are associ- for essential nutrients that should promote good health. Bon
ated with fishy, painty, cardboardy, green, grassy, and many appetit!
LITERATURE CITED
AHA. 2015. American Heart Association (AHA). Trans fat. Accessed Bailey, L. B., S. Moyers & J. F. Gregory. 2001. Folate. In: Bowman,
April 1, 2017. Available at: https://healthyforgood.heart.org/eat- B. & R. Russell, editors. Present knowledge in nutrition. Washington,
smart/articles/trans-fat. DC: International Life Sciences Institute. pp. 278–301.
AHA. 2018. American Heart Association (AHA). Dietary fat recom- Baker, G. L. 2016. Food safety impacts from post-harvest processing
mendations 1957–2015. Accessed April 1, 2017. Available at: https:// procedures of molluscan shellfish. Foods 5:29.
healthyforgood.heart.org/eat-smart/articles/dietary-fats. Bang, H. O. & J. Dyerberg. 1980. Lipid metabolism and ischemic heart
Anacleto, P., A. L. Maulvault, M. L. Nunes, M. L. Carvalho, R. Rosa & disease in Greenland Eskimos. In: Draper, H., editor. Advances in
A. Marques. 2015. Effects of depuration on metal levels and health nutrition research. New York, NY: Plenum Press. pp. 1–22.
status of bivalve molluscs. Food Control 47:493–501. Basti, L., H. Hegaret & S. E. Shumway. 2018. Harmful algal blooms and
Aschner, M., K. M. Erikson, E. Herrero Hernandez & R. Tjalkens. shellfish. In: Shumway, S. E., J. M. Burkholder & S. L. Morton,
2009. Manganese and its role in ParkinsonÕs disease. Neuromuscular editors. Harmful Algal Blooms: A Compendium Desk Reference.
Med. 11:252–266. New York, NY: John Wiley & Sons, Ltd.
Bacher, A., S. Eberhardt, M. Fischer, K. Kis & G. Richter. 2000. Bio- Berg, J. M., J. L. Tymoczko & L. Stryer. 2002. Membrane-bound en-
synthesis of vitamin B2 (riboflavin). Annu. Rev. Nutr. 20:153–167. zymes generate unsaturated fatty acids. In: Biochemistry, 5th edi-
Baik, I., R. D. Abbott, J. D. Curb & C. Shin. 2010. Intake of fish and n-3 tion. New York, NY: W. H. Freeman. 899 pp.
fatty acids and future risk of metabolic syndrome. J. Am. Diet. Bergman, C., D. Gray-Scott, J. Chen & S. Meacham. 2009. What is next
Assoc. 110:1018–1026. for the dietary reference intakes for bone metabolism related
706 WRIGHT ET AL.
nutrients beyond calcium: phosphorus, magnesium, vitamin D, and Fan, Y., A. Ginn, Z. Ma, M. Kang, K. C. Jeong & A. C. Wright. 2017.
fluoride? Crit. Rev. Food Sci. Nutr. 49:136–144. Application of chitosan microparticles for mitigation of Salmonella
Berry, M. J. & N. V. C. Ralston. 2008. Mercury toxicity and the miti- in agricultural water. J. Appl. Microbiol. 123:1346–1358.
gating role of selenium. Ecohealth 5:456–459. Fang, L., B. Wolmarans, M. Y. Kang, K. C. Jeong & A. C. Wright.
Bi, X., L. House & Z. F. Gao. 2016. Impacts of nutrition information on 2015. Application of chitosan microparticles for reduction of Vibrio
choices of fresh seafood among parents. Mar. Resour. Econ. species in seawater and live oysters (Crassostrea virginica). Appl.
31:355–372. Environ. Microbiol. 81:640–647.
Blackmore, G. & W. Wang. 2004. The transfer of cadmium, mercury, Farzaneh-Far, R., J. Lin, E. S. Epel, W. S. Harris, E. H. Blackburn &
methylmercury, and zinc in an intertidal rocky shore food chain. M. A. Whooley. 2010. Association of marine omega-3 fatty acid
J. Exp. Mar. Biol. Ecol. 307:91–110. levels with telomeric aging in patients with coronary heart disease.
Borghi, L., T. Meschi, F. Amato, A. Briganti, A. Novarini & JAMA 303:250–257.
A. Giannini. 1996. Urinary volume, water and recurrences in idio- FDA. 2011. Food and Drug Administration (FDA). Fish and fishery
pathic calcium nephrolithiasis: a 5-year randomized prospective products hazards and controls guidance, 4th edition. Rockville, MD:
study. J. Urol. 155:839–843. FDA. 468 pp.
Bourre, J. & P. Paquotte. 2008. Seafood (wild and farmed) for the el- FDA. 2017a. Food and Drug Administration (FDA). Eating fish: what
derly: contribution to the dietary intakes of iodine, selenium, DHA pregnant women and parents should know. Accessed January 26,
and vitamins B12 and D. J. Nutr. Health Aging 12:186–192. 2018. Available at: https://www.fda.gov/Food/ResourcesForYou/
Bradbury, J. 2011. Docosahexaenoic acid (DHA): an ancient nutrient Consumers/ucm393070.htm.
for the modern human brain. Nutrients 3:529–554. FDA. 2017b. Food and Drug Administration (FDA). Fresh and frozen
Brands, D. A., A. E. Inman, C. P. Gerba, C. J. Mare, S. J. Billington, seafood: selecting and serving it safely. Accessed February 13, 2018.
L. A. Saif, J. F. Levine & L. A. Joens. 2005. Prevalence of Salmonella Available at: https://www.fda.gov/food/resourcesforyou/
spp. in oysters in the United States. Appl. Environ. Microbiol. consumers/ucm077331.htm.
71:893–897. Flattery, J. & M. Bashin. 2004. A baseline survey of raw oyster con-
Brin, M. 1982. Nutrition and vitamin C. Chemtech 12:428–432. sumers in four states. In: Interstate shellfish sanitation conference–
CDC. 2016. Water and nutrition. Accessed February 13, 2018. Avail- Vibrio vulnificus education. Accessed March 6, 2018. Available at:
able at: https://www.cdc.gov/healthywater/drinking/nutrition/ http://www.issc.org/Data/Sites/1/media/education/BaselineSurvey.
index.html. pdf.
Chapman, L. & H. M. Chan. 2000. The influence of nutrition on Greig, R. & D. Wenzloff. 1978. Metal accumulation and depuration
methylmercury in toxication. Environ. Health Perspect. 108:29–56. by American oyster, Crassostrea-virginica. Bull. Environ. Contam.
Childs, M. T., C. S. Dorsett, A. Failor, L. Roidt & G. S. Omenn. 1987. Toxicol. 20:499–504.
Effects of shellfish consumption on cholesterol absorption in nor- Gribble, M. O., R. Karimi, B. J. Feingold, J. F. Nyland, T. M. OÕHara,
molipidemic men. Metabolism 36:31–35. M. I. Gladyshev & C. Chen. 2016. Mercury, selenium and fish oils in
Choy, C., C. Lam, L. Cheung, C. Briton-Jones, L. Cheung & C. Haines. marine food webs and implications for human health. J. Mar. Biol.
2002. Infertility, blood mercury concentrations and dietary seafood Assoc. U.K. 96:43–59.
consumption: a case-control study. BJOG 109:1121–1125. Grzebisz, W. 2011. Magnesium—food and human health. J. Elem.
Cuvin-Aralar, M. L. & R. W. Furness. 1991. Mercury and selenium 16:299–323.
interaction—a review. Ecotoxicol. Environ Saf. 21:348–364. Guan, S., T. Palermo & J. Meliker. 2015. Seafood intake and blood
De, J., H. R. Dash & S. Das. 2014. Mercury pollution and cadmium in a cohort of adult avid seafood consumers. Int. J. Hyg.
bioremediation—a case study on biosorption by a mercury-resistant Environ. Health 218:147–152.
marine bacterium. In: Das, S., editor. Microbial biodegradation and Hallberg, L., M. Brune & L. Rossander. 1989. The role of vitamin C in
bioremediation. London and Waltham, MA: Elsevier. pp. 137–166. iron absorption. Int. J. Vitam. Nutr. Res. 30:103–108.
De, J., N. Ramaiah, N. B. Bhosle, A. Garg, L. Vardanyan, Herman, J. R. 2015. Protein and the body. Division of Agricultural
V. L. Nagle & K. Fukami. 2007. Potential of mercury-resistant Sciences and Natural Resources, Oklahoma State University. Still-
marine bacteria for detoxification of chemicals of environmental water, OK. Accessed March 4, 2018. Available at: http://pods.dasnr.
concern. Microbes Environ. 224:336–345. okstate.edu/docushare/dsweb/Get/Document-2473/T-3163web.
DePaola, A., J. L. Jones, J. Woods, W. Burkhardt, K. R. Calci, pdf.
J. A. Krantz, J. C. Bowers, K. Kasturi, R. H. Byars, E. Jacobs, Horning, K. J., S. W. Caito, K. G. Tipps, A. B. Bowman & M. Aschner.
D. W. Hills & K. Nabe. 2010. Bacterial and viral pathogens in live 2015. Manganese is essential for neuronal health. Annu. Rev. Nutr.
oysters: 2007 United States market survey. Appl. Environ. Microbiol. 35:71–108.
76:2754–2768. Iwamoto, M., T. Ayers, B. E. Mahon & D. L. Swerdlow. 2010. Epi-
Domingo, J. 2016. Nutrients and chemical pollutants in fish and shell- demiology of seafood-associated infections in the United States.
fish. Balancing health benefits and risks of regular fish consumption. Clin. Microbiol. Rev. 23:399–411.
Crit. Rev. Food Sci. Nutr. 56:979–988. Kagawa, Y., M. Nishizawa, M. Suzuki, T. Miyatake, T. Hamamoto,
Dong, F. M. 2001. The nutritional value of shellfish. Washington/ K. Goto, E. Motonaga, H. Izumikawa, H. Hirata & A. Ebihara.
Oregon Sea Grant. Accessed March 5, 2018. Available at: https:// 1982. Eicosapentaenoic acids of serum lipids of Japanese islanders
wsg.washington.edu/wordpress/wp-content/uploads/publications/ with low incidence of cardiovascular diseases. J. Nutr. Sci. Vitami-
Nutritional-Value-of-Shellfish.pdf. nol. (Tokyo) 28:441–453.
Eguchi, L. A. & P. Saltman. 1987. Kinetics and mechanisms of metal Kantor, L. 2016. AmericansÕ seafood consumption below recommen-
reduction by hemoglobin. 1. Reduction of iron (iii) complexes. dations. Washington, DC: United States Department of Agricul-
Inorg. Chem. 26:3665–3669. ture, Economic Research Service. Accessed December 13, 2017.
EPA. 2018a. Environmental Protection Agency (EPA). Mercury in your Available at: https://www.ers.usda.gov/amber-waves/2016/october/
environment. Accessed March 2, 2018. Available at: http://www. americans-seafood-consumption-below-recommendations/.
epa.gov/mercury/about.html. Kinsella, J. E. 1987. Seafoods and fish oils in human health and disease.
EPA. 2018b. Environmental Protection Agency (EPA). Drinking water Components affecting the safety of fish oils. New York, NY: Marcel
regulations and contaminants. Accessed February 13, 2018. Avail- Dekker, Inc. 317 pp.
able at: https://www.epa.gov/dwregdev/drinking-water-regulations- Kopple, J. D. 1975. Evidence that histidine is an essential amino acid in
and-contaminants. normal and chronically uremic man. J. Clin. Invest. 55:881–891.
NUTRITIONAL AND BACTERIAL COMPOSITION OF MOLLUSCAN SHELLFISH 707
Kraft, M. 2015. Phosphorus and calcium: a review for the adult nutri- assessment and mercury-selenium balance. Food Chem. Toxicol.
tion support clinician. Nutr. Clin. Pract. 30:21–33. 62:299–307.
Lecerf, J. M. & M. de Lorgeril. 2008. Dietary cholesterol: from physi- Olmedo, P., A. Pla, A. Hernandez, F. Barbier, L. Ayouni & F. Gil.
ology to cardiovascular risk. Sci. Aliments 28:68–76. 2013b. Determination of toxic elements (mercury, cadmium, lead,
Libby, P., M. Aikawa & U. Schonbeck. 2000. Cholesterol and arthro- tin and arsenic) in fish and shellfish samples. Risk assessment for the
sclerosis. Biochim. Biophys. Acta 1529:299–309. consumers. Environ. Int. 59:63–72.
Lund, E. 2013. Health benefits of seafood; Is it just the fatty acids? Food Onifade, T. J. M., R. Hutchinson, K. Van Zile, D. Bodager, R. Baker &
Chem. 140:413–420. C. Blackmore. 2011. Toxin producing Vibrio cholerae O75 outbreak,
Maulvault, A., P. Anacleto, V. Barbosa, J. Sloth, R. Rasmussen, United States, March to April 2011. Euro Surveill. 16:10–12.
A. Tediosi, M. Fernandez-Tejedor, F. van den Heuvel, M. Kotterman & Painter, J. A., R. M. Hoekstra, T. Ayers, R. V. Tauxe, C. R. Braden,
A. Marques. 2015. Toxic elements and speciation in seafood sam- F. J. Angulo & P. M. Griffin. 2013. Attribution of foodborne ill-
ples from different contaminated sites in Europe. Environ. Res. nesses, hospitalizations, and deaths to food commodities by using
143:72–81. outbreak data, United States, 1998–2008. Emerg. Infect. Dis. 19:407.
Miletic, I., M. Miric, Z. Lalic & S. Sobajic. 1991. Composition of lipids Phillips, K. M., D. M. Ruggio, J. Exler & K. Y. Patterson. 2012. Sterol
and proteins of several species of mollusks, marine and terrestrial, composition of shellfish species commonly consumed in the United
from the Adriatic Sea and Serbia. Food Chem. 41:303–308. States. Food Nutr. Res. 56:10931.
Miller, J. L. 2013. Iron deficiency anemia: a common and curable dis- Pietros, J. M. & M. A. Rice. 2003. The impacts of aquacultured oys-
ease. Cold Spring Harb. Perspect. Med. 3:7. ters, Crassostrea virginica (Gmelin, 1791) on water column nitro-
Morris, M. C., J. Brockman, J. Schneider, Y. Wang, D. A. Bennett, gen and sedimentation: results of a mesocosm study. Aquaculture
C. C. Tagney & O. van de Rest. 2016. Association of seafood con- 220:407–422.
sumption, brain mercury level, and APOE 4 status with brain Prunty, F. & C. Vass. 1943. The assessment of vitamin C nutrition in
neuropathy in older adults. JAMA 315:489–497. man. Biochem. J. 37:623–629.
Mouzin, E., L. Mascola, M. Tormey & D. E. Dassey. 1997. Prevention Ralston, N. V., C. R. Ralston, J. L. Blackwell & L. J. Raymond. 2008.
of Vibrio vulnificus infections—assessment of regulatory educational Dietary and tissue selenium in relation to methylmercury toxicity.
Strategies. JAMA 278:576–578. Neurotoxicology 29:802–811.
Nettleton, J. A. & J. Exler. 1992. Nutrients in wild and farmed fish and Raymond, L. J. 2004. Mercury: selenium interactions and health im-
shellfish. J. Food Sci. 57:257–260. plications. SMDJ 7:72–77.
Newton, A., M. Kendall, D. J. Vugia, O. L. Henao & B. E. Mahon. Rippey, S. R. 1994. Infectious-diseases associated with molluscan
2012. Increasing rates of vibriosis in the United States, 1996–2010: shellfish consumption. Clin. Microbiol. Rev. 7:419.
review of surveillance data from 2 systems. Clin. Infect. Dis. 54: Rittenschober, D., V. Nowak & U. Charrondiere. 2013. Review of
S391–S395. availability of food composition data for fish and shellfish. Food
Nielsen, M. S., A. Gammelmark, T. Madsen, T. Obel, I. Aardestrup & Chem. 141:4303–4310.
E. B. Schmidt. 2012. The effect of low-dose marine n-3 fatty acids on Ryan-Harshman, M. & W. Aldoori. 2008. Vitamin B12 and health. Can.
the biosynthesis of pro-inflammatory 5-lipoxygenase pathway me- Fam. Physician 54:536–541.
tabolites in overweight subjects: a randomized controlled trial. Samman, S. 2007. Zinc. Nutr. Diet. 64:S131–S134.
Prostaglandins Leukot. Essent. Fatty Acids 87:43–48. Sandstead, H. 2012. Zinc nutrition from discovery to global health
NIH-ODS. 2016. National Institutes of Health (NIH)—Office of Di- impact. Adv. Nutr. 3:718–719.
etary Supplements (ODS). Fact sheet for health professionals: Scallan, E., R. M. Hoekstra, F. J. Angulo, R. V. Tauxe, M.-A. Wid-
omega 3 fatty acids. Accessed March 5, 2018. Available at: https:// dowson, S. L. Roy, J. L. Jones & P. M. Griffin. 2011. Foodborne
ods.od.nih.gov/factsheets/Omega3FattyAcids-HealthProfessional/. illness acquired in the United States-major pathogens. Emerg. In-
NIH-ODS. 2018a. National Institutes of Health (NIH)—Office of Di- fect. Dis. 17:7–15.
etary Supplements (ODS). Dietary supplement fact sheet: vitamin Simons, K. & E. Ikonen. 2000. Cell biology—how cells handle choles-
B6. Accessed March 5, 2018. Available at: https://ods.od.nih.gov/ terol. Science 290:1721–1726.
factsheets/VitaminB6-HealthProfessional/. Smith, D. 2015. Oyster: a gastronomic history, New York, NY: Harry
NIH-ODS. 2018b. National Institutes of Health (NIH)—Office of Di- N. Abrams. 256 pp.
etary Supplements (ODS). Fact sheet for health professionals: vi- Sormo, E. G., T. M. Ciesielski, I. B. Overjordet, S. Lierhagen,
tamin B12. Accessed March 5, 2018. Available at: https://ods.od. G. S. Eggen, T. Berg & B. M. Jenssen. 2011. Selenium moderates
nih.gov/factsheets/VitaminB12-HealthProfessional/. mercury toxicity in free-ranging fish. Environ. Sci. Technol. 45:6561–
NIH-ODS. 2018c. National Institutes of Health (NIH)—Office of Di- 6566.
etary Supplements (ODS). Dietary supplement fact sheet: folate. Tsuji, A., T. Nakamura & K. Shibata. 2017. Effects of mild and severe
Accessed March 5, 2018. Available at: https://ods.od.nih.gov/ vitamin B1 deficiencies on the meiotic maturation of mice oocytes.
factsheets/Folate-HealthProfessional/. Nutr. Metab. Insights 10:1–9.
NOAA. 2016. National Oceanic and Atmospheric Administration Uchida, H., C. Roheim & R. Johnston. 2017. Balancing the health risks
(NOAA). Fisheries of the United States 2015. Accessed March 5, and benefits of seafood: how does available guidance affect con-
2018. Available at: https://www.st.nmfs.noaa.gov/Assets/ sumer choices? Am. J. Agric. Econ. 99:1056–1077.
commercial/fus/fus15/documents/FUS2015.pdf. United States Department of Health and Human Service. 2015.
NSSP. 2015. National Shellfish Sanitation Program (NSSP). Guide for 2015–2020 Dietary guidelines for Americans. Appendix 7. Nutri-
the control of molluscan shellfish 2015 revision. Accessed March 5. tional goals for age-sex groups based on dietary reference intakes
Available at: https://www.fda.gov/downloads/Food/ and dietary guidelines recommendations. pp. 97–98. Accessed
GuidanceRegulation/FederalStateFoodPrograms/UCM505093. March 5, 2018. Available at: https://health.gov/dietaryguidelines/
pdf. 2015/resources/2015-2020_Dietary_Guidelines.pdf.
OÕKeefe, J. H. & W. S. Harris. 2000. From Inuit to implementation: USDA. 2015. United States Department of Agriculture (USDA).
omega-3 fatty acids come of age. Mayo Clin. Proc. 75:607–614. 2015–2020 Dietary guidelines. Accessed April 6, 2018. Available at:
Olmedo, P., A. Hernandez, A. Pla, P. Femia, A. Navas-Acien & F. Gil. https://www.choosemyplate.gov/dietary-guidelines.
2013a. Determination of essential elements (copper, manganese, USDA. 2018a. United States Department of Agriculture, Agricultural
selenium and zinc) in fish and shellfish samples. Risk and nutritional Research Service, Nutrient Data Laboratory. USDA National
708 WRIGHT ET AL.
Nutrient Database for Standard Reference. Accessed April 2018. Wallace, T. & V. Fulgoni. 2017. Usual choline intakes are associated
Accessed at: https://ndb.nal.usda.gov/ndb/search/list. with egg and protein food consumption in the United States. Nu-
USDA. 2018b. United States Department of Agriculture (USDA). trients 9:839.
2020–2025 Dietary guidelines for Americans: we want to hear from Weiser, M. J., C. M. Butt & M. H. Mohajeri. 2016. Docosahexaenoic
you. Accessed April 2018. Available at: https://www.usda.gov/ acid and cognition throughout the lifespan. Nutrients 8:99.
media/blog/2018/03/01/2020-2025-dietary-guidelines-americans- Wooltorton, E. 2002. Facts on mercury and fish consumption. CMAJ
we-want-hear-you. 167:897.
USNLM. 2018a. United States National Library of Medicine Wright, A. C., M. D. Danyluk & W. S. Otwell. 2009. Pathogens in raw
(USNLM). Vitamin D. Accessed April 2018. Available at: https:// foods: what the salad bar can learn from the raw bar. Curr. Opin.
www.ncbi.nlm.nih.gov/pubmedhealth/PMHT0001921/. Biotechnol. 20:172–177.
USNLM. 2018b. United States National Library of Medicine Wright, A. C. & K. R. Schneider. 2010. Pathogenic vibrios in seafood.
(USNLM). Accessed April 2018. Available at: https://medlineplus. In: Juneja, V. K. & H. N. Sofos, editors. Pathogens and toxins
gov/druginfo/natural/924.html. in foods: challenges and interventions. Washington, DC: ASM
Venugopal, V. & K. Gopakumar. 2017. Shellfish: nutritive value, health Press. pp. 146–163.
benefits, and consumer safety. Compr. Rev. Food Sci. Food Saf. Wright, A. C., L. M. Simpson & J. D. Oliver. 1981. Role of iron in
16:1219–1242. the pathogenesis of Vibrio vulnificus infections. Infect. Immun.
Vezzulli, L., I. Brettar, E. Pezzati, P. C. Reid, R. R. Colwell, 35:503–507.
M. G. Hofle & C. Pruzzo. 2012. Long-term effects of ocean warming Wylie-Rosett, J., C. J. Segal-Isaacson & A. Segal-Isaacson. 2004. Car-
on the prokaryotic community: evidence from the vibrios. ISME J. bohydrates and increases in obesity: does the type of carbohydrate
6:21–30. make a difference? Obes. Res. 12:124S–129S.
Viau, M., C. Genot, L. Ribourg & A. Meynier. 2016. Amounts of the Yoneda, S. & K. T. Suzuki. 1997. Detoxification of mercury by selenium
reactive aldehydes, malonaldehyde, 4-hydroxy-2-hexenal, and by binding of equimolar Hg-Se complex to a specific plasma protein.
4-hydroxy-2-nonenal in fresh and oxidized edible oils do not nec- Toxicol. Appl. Pharmacol. 143:274–280.
essary reflect their peroxide and anisidine values. Eur. J. Lipid Sci. Ziesel, S. H. & K. A. da Costa. 2009. Choline: an essential nutrient for
Technol. 118:435–444. public health. Nutr. Rev. 67:615–623.