Microbiolspec - MTBP 0019 2016

Food-to-Humans
Bacterial Transmission
PATRÍCIA ANTUNES,1 CARLA NOVAIS,2 and LUÍSA PEIXE2
1
Faculdade de Ciências da Nutrição e Alimentação, Universidade do Porto, Porto, Portugal
2
Faculdade de Farmácia, Universidade do Porto, Porto, Portugal
ABSTRACT Microorganisms vehiculated by food might benefit has been an increase in knowledge on gut bacterial
health, cause minimal change within the equilibrium of the host genera and species commonly affected by diet, as well
microbial community or be associated with foodborne diseases.
as evidence suggesting that the intestinal microbiome
In this chapter we will focus on human pathogenic bacteria for
which food is conclusively demonstrated as their transmission
plays an important role in modulating the risk of sev-
mode to human. We will describe the impact of foodborne eral chronic diseases (e.g., inflammatory bowel dis-
diseases in public health, the reservoirs of foodborne pathogens ease, obesity, type 2 diabetes, cardiovascular disease,
(the environment, human and animals), the main bacterial and cancer) (1–3). Nevertheless, comprehensive infor-
pathogens and food vehicles causing human diseases, and the mation about the types of diet that transmit bacteria
drivers for the transmission of foodborne diseases related to the implicated in those diseases, as well as environmental
food-chain, host or bacteria features. The implication of and host factors favoring their colonization, remains
food-chain (foodborne pathogens and commensals) in the
scarce. Notwithstanding, food as a transmission mode
transmission of resistance to antibiotics relevant to the
treatment of human infections is also evidenced. The multiplicity for microorganisms reaching humans is extensively
and interplay of drivers related to intensification, diversification characterized for different pathogenic bacteria, the en-
and globalization of food production, consumer health status, vironment, animals, and humans being their main res-
preferences, lifestyles or behaviors, and bacteria adaptation to ervoirs (Fig. 1) and the fecal-oral route their main
different challenges (stress tolerance and antimicrobial transmission route (4–6). A triad including a contami-
resistance) from farm to human, make the prevention of nated food item, a susceptible human host, and bacte-
bacteria-food-human transmission a modern and continuous
rial pathogens able to survive and multiply in specific
challenge. A global One Health approach is mandatory to better
understand and minimize the transmission pathways of human
environmental conditions must be present for the oc-
pathogens, including multidrug-resistant pathogens and currence of a foodborne disease. Nevertheless, trans-
commensals, through food-chain. mission of typical foodborne pathogens can also occur
more rarely by alternative transmission modes, as by
INTRODUCTION
Food is considered one of the main environmental driv-
ers shaping the human microbiota across the life span. Received: 9 March 2018, Accepted: 27 December 2019,
Published: 16 January 2020
Microorganisms vehiculated by food can be related to Editors: Fernando Baquero, Hospital Ramón y Cajal (IRYCIS), Madrid,
a variety of scenarios, including those benefiting health Spain; Emilio Bouza, Hospital Ramón y Cajal (IRYCIS), Madrid, Spain;
(e.g., stimulation of host antibodies, release of chemicals J.A. Gutiérrez-Fuentes, Complutensis University, Madrid, Spain, and
Teresa M. Coque, Hospital Ramón y Cajal (IRYCIS), Madrid, Spain
to stimulate the health of the overall system, or inhibi- Citation: Antunes P, Novais C, Peixe L. 2020. Food-to-humans
tion of pathogen development), those causing minimal bacterial transmission. Microbiol Spectrum 8 (1):MTBP-0019-2016.
change within the equilibrium of the host microbial doi:10.1128/microbiolspec.MTBP-0019-2016.
Correspondence: Luísa Peixe, lpeixe@ff.up.pt
community, and those that are pathogenic or have been
© 2020 American Society for Microbiology. All rights reserved.
associated with gut-host dysbiosis (1–3). Recently there
ASMscience.org/MicrobiolSpectrum 1
Antunes et al.
FIGURE 1 Reservoirs of the main pathogenic and potentially beneficial bacteria trans-
mitted from food to humans.
direct contact of humans with infected animals or be- enterica serovar Typhi) are associated with systemic
tween humans (7). clinical symptoms and more-severe clinical outcomes,
In general, bacterial pathogens cause foodborne dis- even in individuals without risk factors (6).
eases by three mechanisms: ingestion of preformed tox- In this review, we will focus on pathogenic bacteria
ins in foods (intoxication; e.g., Staphylococcus aureus), for which food is conclusively demonstrated as their
production of toxins within the gastrointestinal tract transmission mode to humans. The impact of foodborne
following ingestion of pathogens (food toxicoinfection; diseases on public health, different scenarios evidencing
e.g., Clostridium perfringens), or invasion of the intes- relevant drivers for bacterial pathogen transmission, and
tinal epithelial cells (infection; e.g., Salmonella) (6). Most the implication of the food chain in the widespread re-
foodborne bacterial pathogens are often associated sistance to antibiotics that is critical to the treatment of
with a self-limiting gastroenteritis syndrome with nau- human infections will be presented.
sea, vomiting, diarrhea, abdominal pain, and sometimes
fever. Nevertheless, such bacteria might also cause se-
vere illness with extraintestinal infections, postinfec- FOODBORNE DISEASES AND
tion sequelae, and even death, especially in individuals PUBLIC HEALTH
in high-risk groups (infants, young children, the el- The first global estimates of foodborne diseases by the
derly, and immunocompromised patients). Few bacterial World Health Organization (WHO) indicate that about
pathogens (e.g., Clostridium botulinum and Salmonella 1 in 10 people (600 million) around the world is sick-
2 ASMscience.org/MicrobiolSpectrum
Food-to-Humans Bacterial Transmission
ened after eating contaminated food each year, with In recent decades, the epidemiology of foodborne
420,000 deaths reported (8). The global burden of outbreaks changed from acute and local to diffuse and
foodborne diseases has been measured in disability- widespread (e.g., geographically dispersed in many
adjusted life years (DALYs), which more fully capture places at once), mostly due to production intensifica-
disease symptoms and severity. In 2010, DALYs data tion and wide distribution of food (20–22). This chal-
showed the loss of 33 million healthy life years, most lenge spurred the development of rapid and more
among children <5 years of age and in low-income sensitive molecular methods for foodborne pathogen
countries (African and Southeast Asian regions) (8). The surveillance, such as whole-genome sequencing (WGS).
most frequent causes of foodborne disease worldwide It became crucial not only to rapidly identify the re-
are bacterial pathogens, the most important being the sponsible pathogen (classical and newly emergent ones)
zoonotic Campylobacter and nontyphoidal Salmonella and source of origin (including the contexts that led to
(NTS) (8). Certain diseases, such as those caused by food contamination) but also to identify new or unsus-
NTS, are a public health concern across all regions of the pected transmission routes and to support public health
world, in high- and low-income countries alike. Other interventions in global food markets (23, 24). For ex-
diseases, such as typhoid fever, foodborne cholera, and ample, WGS has been applied to source attribution of
those caused by pathogenic Escherichia coli, are much campylobacteriosis (25, 26), outbreak investigations of
more common in low-income countries, while Cam- salmonellosis (10, 18, 21, 27) and listeriosis (19, 28),
pylobacter is an important pathogen in high-income as well as to differentiating persistent contamination by
countries (8). Besides the direct impact of foodborne Listeria monocytogenes from reintroduction in food-
diseases in human health, they also have health care, associated environments (29). Beyond high-resolution
economic, and welfare costs, as in the case of the United subtyping, WGS could also allow characterization of
Kingdom and the United States, where available data foodborne pathogen virulence markers (linked to greater
estimated a cost of £1.5 billion and of $14 billion, re- pathogenicity) and stress tolerance as well as antimi-
spectively (9, 10). crobial resistance prediction, both features important
Currently, most human infections have a zoonotic to microbial risk assessment (23, 24). For example, in
origin, and ∼75% of new and emerging pathogens 2011, Shiga toxin-producing E. coli (STEC) O104:H4
originated from animals, including the foodborne ones caused one of the largest foodborne outbreaks of recent
(11). Transmission starts from the original habitat (the history, with >3,000 cases of infection and >40 deaths
animal reservoir) to the food, along the complex farm-to- reported, in multiple European countries and North
table pathway. Maintenance of a reservoir of zoonotic America. Within a week, WGS revealed that the un-
foodborne pathogens is favored by their transmission usually virulent outbreak strain belonged to a distinct
within the food animals and on-farm production envi- group of enteroaggregative E. coli that had acquired the
ronment, through diverse routes (e.g., contaminated feed combination of genes coding for Shiga toxin 2, anti-
and water, humans, rodents, and flies) (12). microbial resistance, and other virulence factors (30).
Almost all type of foods (vehicles of transmission) can Despite the promising application of WGS to improve
be contaminated by foodborne pathogens. Neverthe- foodborne pathogen surveillance, the use of standard-
less, certain vehicles pose a greater threat than others, ized methods that can be practiced among routine lab-
being classified as high-risk foods. They include raw oratories remains a challenge, namely, the selection of
or undercooked foods of animal origin (meat, poultry, standardized analytical tools as well as epidemiologic
eggs, fish, and milk) and, more recently, fresh produce interpretation of WGS data (23, 24).
(including leafy vegetables and sprouts) (13, 14). Also,
food constituted with multiple ingredients and with a
high level of handler manipulation has a greater poten- DRIVERS OF FOOD-TO-HUMAN BACTERIAL
tial to be associated with foodborne diseases (13). Some PATHOGENIC TRANSMISSION
food types are considered unexpected vehicles of path- Several drivers have been identified to promote the in-
ogens by the nature of the food matrices preventing crease of food-to-human bacterial pathogenic transmis-
microorganism multiplication, such as peanut butter, sion and foodborne diseases worldwide by leading to the
caramel apples, peppers, and chocolate. However, such introduction and amplification of pathogens along the
food vehicles have been recently associated with large complex farm-to-human pathway (31–37). This section
outbreaks, sometimes in wide geographic regions (15– will address the driving factors promoting such events
19). associated with the features of bacterial pathogens, the
Antunes et al.
FIGURE 2 Factors that drive transmission of pathogenic bacteria from food to humans.
food chain, and the human host (Fig. 2). Diverse ex- resulting in new opportunities for pathogen transmis-
amples of transmission scenarios involving those drivers sion to humans, particularly of zoonotic agents (e.g.,
will be given. Salmonella and Campylobacter). The increased demand
for food due to worldwide population growth contrib-
Drivers Related to the Food Chain uted to the growth of industrial-scale production sys-
Changes in the food chain, involving intensive and large- tems, including intensification of animal production plus
scale production and distribution, climate change, and agriculture and large-scale food processing and distri-
globalization of food and live animal suppliers, are con- bution (31, 33).
sidered particularly significant drivers for the emergence Intensive livestock practices with high animal densi-
of foodborne diseases (34, 36). ties promote persistence and dissemination of zoonotic
pathogens in food animals and farm production envi-
Transmission Scenarios Related ronments, leading to the maintenance of a reservoir of
to Intensive and Large-Scale Food foodborne pathogens directly transmitted to foods of
Production and Distribution animal origin and indirectly to fresh produce (12). This
Shifts in food production, processing, and distribution is illustrated by pandemic S. enterica serovar Enter-
during the last several decades have contributed to the itidis in the 1980s and ’90s, mostly attributed to in-
increased risk and complexity of foodborne diseases, tensive production of eggs/broilers, which was later
overcome with successful control programs, including intoxication from milk products in Japan resulted in
adequate biosecurity measures (38). More recently, in >10,000 cases, the contamination point being a pro-
the European Union, contamination in the large turkey duction line valve of a major dairy-products processing
production chain was associated with a large outbreak plant in Osaka that became contaminated with staphy-
of S. enterica serovar Stanley (39). Also, in the case of lococcal enterotoxin type A (51). Recently, a 2017–2018
Campylobacter it was shown that the major contami- outbreak in the European Union due to contaminated
nation source of chicken meat was at the large produc- infant formula from a French dairy company with
tion rearing farm (40). More recently, changing farming S. enterica serovar Agona led to the recall of >10 million
practices for free-range and organic animal production boxes from multiple countries (52). A 2-year (2015–
(allowing outdoor access for farm animals) have raised 2016) contaminated food-processing environment re-
new questions about food safety, as this type of pro- sulted in a deadly L. monocytogenes outbreak linked to
duction is also associated with several hazards, including bagged salads (33 cases and 4 deaths in the United States
Campylobacter and Salmonella (41). and Canada) (53). One example of a contaminated food
The intensification of vegetable and fruit production ingredient affecting multiple products was the large
has been also associated with several risks related to the outbreak (714 cases and 9 deaths in 46 states in the
use of unsafe irrigation water and manure, poor worker United States) of S. enterica serovar Typhimurium linked
hygiene, inadequate pest control, and improper cleaning to peanut products from a plant evidencing diverse
of sanitizing or harvest equipment and utensils, among possibilities of pathogen transmission (e.g., rodent-
others (42). It has been shown that organic agriculture accessible entryways, an unsealed air-handling system,
practices related to seed production (e.g., contaminated and rain leakage into peanut storage areas) to food (17).
irrigation water and/or manure) have contributed to There are also comprehensive published examples of
identification of sprouted seeds as a high-risk food for food safety failures (e.g., ignored positive tests of mi-
STEC and Salmonella (43). In the United States, un- crobiological hazards, falsification of food safety docu-
sanitary conditions identified in one farm and processing ments, inadequate controls to prevent contamination
operations environment (failure in sanitizing and fruit and kill bacteria, and insufficient cleaning and sanitation)
precooling; ineffective cleaning due to inadequate fa- that led to large outbreaks and deaths from foodborne
cilities and equipment design) resulted in contamina- diseases, demonstrating that maintaining a food safety
tion of cantaloupes with diverse L. monocytogenes culture within the entire organization is crucial (55).
strains, leading to a large and fatal outbreak (147 cases,
33 deaths, and 1 miscarriage) (22, 44). Other foodborne Transmission Scenarios Related to
outbreaks associated with fruits and vegetables through Globalization of the Food Supply
contact with surface or irrigation water have been re- A growing international food trade resulting in the ex-
ported and recently revised (45). port and import of contaminated farm animals, food
Besides production practices, climate change also can products (e.g., vegetables, fruit, seeds, meat and poultry,
impact crops, food animals, and the growth and survival and ethnic foods), and single meals containing ingre-
of pathogens, as well as exposure and transmission dients from multiple regions is contributing to changing
pathways of foodborne diseases (46, 47). Climate trends in foodborne diseases. Most of the food products
changes potentially enhance the ability of pathogens to consumed in developed countries are produced on in-
survive and persist in soil, crops, and water, increasing dustrial scale, being also increasingly imported (not
the probability of their transmission thorough water, grown or produced locally) due to changing consumer
seafood, or vegetables (46, 48–50). demand for a wide diversity of foods and fresh pro-
The complexity of the food chain due to industrial- duce year-round (33, 56). However, import from other
scale production systems can also increase the risk of countries includes those with lower food safety stan-
foodborne outbreaks, with some occurring during long dards (e.g., lacking meat processing plant inspections) or
periods of time (51–54). A simple failure in a single without appropriate food production and processing
industrial-scale production resulting from contamina- safety practices (e.g., untreated human/animal manure,
tion with pathogens during food processing (e.g., from contaminated water, or untreated wastewater sewage)
the environment, surface, or food ingredients) can result (33, 42). In the European Union, the most-imported
in distribution of contaminated food batches to millions food categories in 2016 were fruits and nuts among
of consumers, affecting their health in different locations vegetable products and fish, crustaceans, and aquatic
at the same time. In 2000, a massive outbreak of food invertebrates among animal products (57), as occurs in
Antunes et al.
the United States, where most seafood and a moiety of convenient ready-to-eat (RTE) (e.g., pre-prepared meals,
fruits are imported (56). Both types of foodstuffs have ready-washed fruit and vegetables, and quick-cook
been reported in developed regions as presenting an in- sauces), and healthy foods (e.g., those with less salt),
creased association with foodborne disease outbreaks in known to be associated with higher foodborne pathogen
recent years (13, 14, 27, 56, 58). contamination, constitutes a driving factor in the emer-
In addition, the trade of live animals and food-animal gence of foodborne diseases. One of the major exam-
products has also been implicated in the transmission ples is the increasing consumption of fresh produce due
of foodborne pathogens to humans. In Europe, this to health concerns, which have been frequently associ-
is exemplified by contaminated products resulting in ated with foodborne outbreaks linked to leafy green
multicountry foodborne outbreaks, as the 2017–2018 vegetables (e.g., spinach and lettuce), sprouts, and fruits
S. Enteritidis outbreak linked to eggs (table eggs and (e.g., melons and papayas) in developed countries (56,
consumed raw in some recipes) from Poland, with its 66).
origin in egg-packing centers and laying-hen farms (59). The increasing trend of consumption of uncooked
Recently, poultry products imported from Brazil, one or undercooked food of animal origin (e.g., meat and
of the biggest exporters, have been linked to the spread poultry, fish, seafood-and-meat recipes, and raw milk)
of epidemic clones of an uncommon and multidrug- and convenience foods like RTE also potentiate trans-
resistant (MDR) S. enterica serotype, S. Heidelberg, into mission of foodborne pathogenic bacteria (34). For ex-
European countries (60, 61). Aquaculture practices ap- ample, consumption of raw milk, in which interest is
plied in seafood and fish production in many exporting growing in the European Union, was identified as clearly
countries, mostly in Asia (e.g., integrated fish-pig farms associated with transmission of human disease caused
in Southeast Asia), are also related to food contamina- by Campylobacter, Salmonella, and STEC (67). More-
tion by pathogens (33, 62). For example, using a novel over, the increasing consumption of minimally processed
combination of WGS analysis and geographic metadata foods with extended shelf lives, such as refrigerated or
to create a transmission network, it was possible to trace frozen RTE products, was proposed as a possible factor
the origin of a U.S. outbreak of S. enterica serovar in the promotion of human listeriosis in Europe (68).
Bareilly to scraped tuna imported from a fishery facility Also, several cases and outbreaks of Vibrio parahae-
in India (10). molyticus infections have been reported in European
Recent studies showed that illegal importation of countries, associated with higher consumption of raw
food-animal products (including bush meat and live- and undercooked fish and shellfish (including imported)
stock meat) from Africa to Europe through airport pas- in recent years coupled with an increase in the number of
sengers’ luggage was commonly verified, some of those susceptible individuals consuming seafood products and
illegal food items being contaminated with foodborne with warming of marine waters as a result of global
pathogens such as NTS, suggesting a potential public climatic change (50, 69, 70).
health risk by a neglected route of transmission (63, 64). Besides consumer demand for specific food products,
Also, uncontrolled entry of foodstuffs into the European the new generation of active consumers frequently eat
Union (including from the black market at the EU bor- out of the home, being more exposed to transmission of
der) have been recently reported as a neglected route of foodborne pathogens by contaminated food prepared in
potential methicillin-resistant S. aureus (MRSA) trans- public places. According to the European Food Safety
mission (65). Authority (EFSA), in the European Union almost half of
foodborne outbreaks occurred in food service estab-
Drivers Related to the Host lishments (13). Eating out exposes consumers to food-
Changes in consumer demands for foods, lifestyles, and handler behaviors, whose food safety practices (e.g.,
behaviors related to food safety as well as the increasing personal hygiene to avoid microbial spread, proper food
proportion of vulnerable human host groups can also handling to avoid cross-contamination, and efficient
increase exposure to bacterial pathogens and suscepti- cooking and storage temperatures to avoid microbial
bility to infectious diseases (33, 34, 36). growth) are crucial to prevent transmission of food-
borne pathogenic bacteria to humans. A recent report
Transmission Scenarios Related to Changes studying EU salmonellosis cases associated with ca-
in Consumer Lifestyles and Risk Behaviors tering facilities over a 15-year period identified food-
In recent decades, consumer demand for more-diverse handler behaviors (e.g., cross-contamination between
(e.g., tropical products, fruits and vegetables year-round), heat-treated foods and raw materials or improperly
cleaned food-contact surfaces) as potential risk factors summer activities (picnics, barbecues, and summer fes-
(71). Also, it was shown that food risk behaviors (e.g., tivals), the increased risk of cross-contamination and
serving chicken at barbecues when unsure it was fully lack of personal hygiene together with the difficulty of
cooked—a Campylobacter risk factor) in U.K. kitchens keeping food at safe temperatures coincides with peaks
were widely prevalent among chefs and catering stu- of some foodborne infections (47).
dents and the public (72).
Consumers have more opportunities to travel today, Transmission Scenarios Related
positioning travel and tourism as driving forces con- to Host Risk Population
tributing to exposure to contaminated food (73, 74). For In recent decades, the worldwide increase of vulnerable
example, an international outbreak of S. Heidelberg people, particularly the elderly and the immunocom-
associated with in-flight catering meals affected 25 people promised (e.g., due to cancer, transplant interventions,
of 5 nationalities (74). In addition, food tourism creates AIDS, diabetes, liver or kidney disease, and malnutri-
more opportunities for consumers to be exposed to tion), contributed to more-effective transmission of
pathogenic bacteria by consumption of traditional food particular pathogens to a wide number of susceptible
recipes or exotic cuisine (75). This was illustrated by the hosts. Around 15 to 20% of people of developed coun-
association of Peruvian goat cheese (often made with tries, such as the United Kingdom and United States,
unpasteurized milk) with brucellosis (11) and reptile meal belong to this group, with increased vulnerability re-
with salmonellosis (75). Migration may also change food sulting in development of foodborne disease by a lower
preparation behaviors and consumption habits (34). This infectious dose than typically expected or in diseases
was the case with an outbreak of listeriosis among with increased severity (79). L. monocytogenes is rec-
Mexican immigrants (mostly affecting pregnant women) ognized as one of the main foodborne pathogens with
in the United States as the result of consumption of illicit, great impact in vulnerable groups. In a recent EFSA re-
noncommercial, homemade, Mexican-style cheese pro- port, the only clearly identified risk factor for the in-
duced from contaminated raw milk sold to unlicensed creasing trend in cases of listeriosis in the European
cheese makers by a local dairy (76). Union was the increase in the elderly population (68). In
However, it is of note that a large number of food- France, patients with chronic lymphocytic leukemia had
borne outbreaks occur in the home/domestic kitchen a listeriosis incidence >1,000 times greater than that of
(13). Such events are mostly associated with poor food- the population with no risk factors (80), and low in-
handling behaviors, such as inadequate time-temperature fectious doses of Listeria associated with milkshakes
control, cross-contamination, poor personal hygiene, affected only hospitalized patients in the United States
insufficient cleaning, and using food from unsafe sources (81). The elderly was the group most likely to die after
(6, 77). It was noted that unsafe practices (including infection with STEC, and children <5 years old develop
those related to storage time and temperatures) are not more-severe infections (82). Infant botulism is associated
uncommon with elderly people (>10% of the persons with honey consumption and with the growth of Clos-
studied), one of the risk group consumers, having a tridium botulinum and neurotoxin production in the gut
potential impact on the human listeriosis risk (68). In of infants <1 year old (83). It was also demonstrated that
addition, it was recently reported that the temperatures in patients with chronic liver diseases (cirrhosis), ele-
in EU domestic refrigerators are high (ranging from −8 vated serum iron levels, or immunodeficiency, Vibrio
to −4 to 11 to 21°C), which could potentiate L. mono- vulnificus causes frequently rapid fatal septicemia,
cytogenes growth (68). Also questionable is the proper mostly associated with previous consumption of raw
use of home cooking or reheating methods like micro- oysters (84, 85). The wide use of antacids (particularly
wave and other emerging cooking machines (“cooking proton pump inhibitors) or constipating drugs (e.g.,
robots”). For example, the use of ready-to-cook antipsychotics) by people whether or not they are in the
products for microwave preparation before consump- vulnerable groups might also increase susceptibility to
tion could be a risk if the temperatures are not sufficient foodborne diseases, at least during a transitional period
to kill pathogens like Salmonella (33, 34). This is illus- (79, 86). There is evidence that patients with hypo-
trated by an outbreak of Salmonella possibly related to chlorhydria or achlorhydria or who have been treated
failures in the microwave cooking of frozen, not-ready- with proton pump inhibitors or H2 receptor antagonists
to-eat, microwaveable foods due to misinterpretation are more susceptible to Campylobacter, E. coli O157:
of the product’s cooking label instructions and/or un- H7, L. monocytogenes, Salmonella, Shigella, and Vibrio
familiarity with the oven’s wattage (78). Also, during cholerae than healthy persons (79, 87–89). The increas-
Antunes et al.
ing numbers of vulnerable populations and their risk of stress protects bacteria during subsequent exposure to
easily acquiring a foodborne disease impose the need for normally lethal conditions, as was described for Sal-
food safety management systems among food suppliers monella adaptation to bile or to acid (115, 116). Diverse
of hospitals, nursing homes, elderly-care homes, schools, Salmonella serotypes (S. Typhimurium, S. Enteritidis,
and day care centers for children (79). S. Newport, and S. Infantis) were cross-protected against
UV irradiation, various sanitizing agents, dry heat, and
Drivers Related to Foodborne bile salts when under desiccation stress (117). Induced
Bacterial Pathogens response after contact with sublethal stress or cross-
Foodborne bacterial pathogens face a variety of adverse protection events can be found in the literature for other
effects or stresses during transmission events from their foodborne pathogens, including V. parahaemolyticus,
reservoirs to the human host. Stressful conditions occur L. monocytogenes, and STEC (112, 118, 119).
from the agriculture level to food processing, storage, Against all the above, it is evident that bacterial stress
distribution, cooking, and within the human host (12, response can be a complex scenario, dependent on the
90–93). Such stresses often co- and/or sequentially occur interplay of microbial-specific features and intrinsic
in the same ecosystem (e.g., application of hurdle tech- (e.g., food matrix), extrinsic (e.g., temperature), or food-
nology in food preservation), during ecosystem transi- processing factors (e.g., hurdle technology). According
tion (e.g., from acid food to acid pH in stomach and bile to the nature of such interactions (e.g., bacterial spe-
salts in animal and human gut), or during infection (e.g., cies, strain type, stress concentrations, one or multiple
high temperature or acidic pH within macrophages), stresses, food components, and competing microbiota in
imposing on bacteria the necessity for ceaseless adapta- the host), different outcomes in bacterial survival, mul-
tion (90, 91, 93–97). tiplication, and persistence in the food chain and human
Bacteria stress responses can be stable or transient. host can occur, with potential implications for food-
Stable phenotypes, for example, associated with genetic borne pathogen transmission dynamics. In fact, the
mutation, can be positively selected and fixed in the ability of bacteria to survive and multiply under the
bacterial population under stressful conditions. A tran- stressful conditions occurring in the food chain might
sient stress response can be associated with differential increase human exposure to a greater number of path-
expression of particular genes and generally occurring ogenic bacterial cells in food (e.g., through higher
while the stress is present. These types of responses pathogen shedding from animal reservoirs, survival of
contribute to protect vital processes, to restore cellular food processing, or persistence in food-processing fa-
homeostasis, to repair the damage, to counteract or cilities) as well as to induced stress strains producing
eliminate the stress agent, and/or to increase the cellular greater amounts of toxins responsible for food poison-
resistance against subsequent stress challenges (96). The ing symptoms or requiring lower infectious doses than
ability to overcome sublethal or normally lethal stressful typically expected (120–125).
conditions was described for such diverse foodborne
pathogens as Campylobacter jejuni (e.g., to oxidative Bacterial Strain Diversity Favoring Pathogen-
stress, osmotic stress, or antibiotics) (98–100), Salmo- Food-Human Transmission Scenarios
nella (e.g., to acid, low water activity, thermal treatment, It is well known that bacteria adapt to environmental
high hydrostatic pressure, metals, or antibiotics) (101– conditions by the acquisition of specific genetic clusters
106), STEC (e.g., to acid, osmotic stress, oxidative stress, through horizontal transfer, genetic recombination, or
or heat) (99, 107, 108), L. monocytogenes (e.g., to acid, mutations as well as by differential expression of regu-
osmotic stress, or disinfectants) (99, 109–111), V. para- latory pathways (126). With the advances of geno-
haemolyticus (e.g. to salt, acid, or cold) (112), Bacillus mic, transcriptomic, and single-cell studies applied to
cereus (e.g. to acid, cold, or reducing atmospheres) (96, foodborne pathogens, it is becoming evident that the
113), and Cronobacter sakazakii (e.g., to heat, osmotic dynamic response of microorganisms to changing envi-
stress, or desiccation) (99, 114), among others, stress ronmental conditions depends on the behavior of indi-
responses being strain dependent, i.e., variable among vidual cells within the bacterial population (127, 128).
members of the same species (90). Moreover, the pres- Thus, it is critical to understand the genetic context,
ence of a particular stress can modulate bacterial re- epigenetic mechanisms, and occurrence of heteroge-
sponse to that stress as well as to other ones, the latter neous behaviors of individual bacteria, as they could
phenomenon denominated stress cross-protection (90, have an impact on the success of food-processing and
91). In fact, preexposure to sublethal levels of a given -preservation strategies, on bacterial persistence within
food facilities, and on the food-to-human transmission MDR and highly virulent STEC O104:H4, linked to
of particular strains (e.g., serotypes or clonal lineages). sprout consumption, a serotype that rarely caused hu-
Some examples illustrate variable features among bac- man infection in the past. WGS revealed an unexpected
teria that potentially contribute to pathogen-food-human genetic context of a hybrid enteroaggregative (EAEC)/
transmission scenarios. enterohemorrhagic (EHEC) E. coli strain, potentially
At the farm level, emergent clinically relevant S. en- supporting the high pathogenicity. The evolution anal-
terica serotype Rissen/ST469 and the European clone of ysis of STEC O104:H4 strains, by the description of the
S. Typhimurium/ST34 or S. enterica serotype 4,[5],12: genome and population structure of the outbreak and
i:-/ST34 of pig origin are more tolerant to toxic con- non-outbreak isolates obtained from sporadic infec-
centrations of copper under anaerobiosis, due to the ge- tions, suggested that outbreak STEC O104:H4 might
netic horizontal acquisition of the sil gene cluster, than have evolved to public health importance from EAEC by
other Salmonella serotypes from the same origin that are exploiting a specific cocktail of mobile genetic elements
less associated with human infections (102). Such data (e.g., prophage with stx2, plasmids carrying CTX-M15
suggest that the widespread use of copper as a feed ad- or aggregative adherence fimbriae, high-pathogenicity
ditive in pigs might contribute to the selection of these island [HPI], among others), underlining the possibility
fitter clones, and consequently to pig meat contamina- of further outbreaks if strains achieve novel combina-
tion and their transmission to humans. tions of mobile genetic elements (136–139).
At food-processing facilities, L. monocytogenes ac- Finally, the heterogeneous behavior of individual cells
quiring the qacH and bcrABC genes had a survival ad- within the bacterial population can differentially evolve
vantage when sublethal concentrations of quaternary to cope with the same stress at different levels, or with
ammonium compounds (QACs) often used in disinfec- changing stresses (104, 115, 140). For example, a het-
tion remained on surfaces due to insufficient rinsing erogeneous and multifactorial response to high pressure
methods (110). QAC tolerance genes were often found in S. enterica was described with respect to both degree
in isolates belonging to clonal lineage II-serotype 1/2a- of inactivation and mechanisms (related to the cell
ST121, the dominant persistent ST type worldwide as- membrane and RpoS regulon) used to overcome it.
sociated with food-processing plants and occasionally Parker et al. (140) showed that outbreak E. coli O157:
isolated from human infections (129–132), as well as in H7 strains isolated from patients and the spinach pro-
lineage I-serotype IVb-ST6 isolates associated with hu- duction environment (all indistinguishable by pulsed-
man meningitis (111). Using a WGS approach combined field gel electrophoresis [PFGE]) differ in their stress
with assays evaluating the ability of L. monocytogenes responses, and that marketed spinach bags carried a
to grow in cold (4°C), salt (6% NaCl, 25°C), and acid mix of both subpopulations. Clinical strains carrying
(pH 5, 25°C), it was found that the bacterial stress re- the mutated rpoS gene were more susceptible to acid,
sponse seems to be related to serotype and clonal com- osmotic shock, or oxidation than environmental ones
plex, among other factors (133). with wild-type rpoS. However, clinical strains had a
At the food cooking level, it was shown that E. coli greater nutrient-scavenging ability, potentially favoring
AW1.7 isolated from commercial beef slaughter plants survival and rapid adaptation of E. coli O157:H7 at
had a D60°C of 71 min, with cell counts reducing by critical points of its transmission cycle from “field to
only <5 log10 CFU g−1 in ground-beef patties cooked to fork.”
an internal 71°C, the temperature considered effective
for bacterial elimination in beef (134). This thermal re- Interplay between Bacterial Strains
sistance was linked to the acquisition of an island termed and Food Matrix Favoring Pathogen-
locus of heat resistance (LHR) present in only 2% of E. Food-Human Transmission Scenarios
coli genomes, including clinical ones (107, 135). These Despite the fact that bacterial strain variability could
data suggest the potential inefficacy of standard thermal determine its transmission success to the human host,
conditions applied in food safety when particular strains the interplay of strains with supporting food matrices
are present. seems to be critical for such an event. Food composition
Uncommon bacterial genotypes occurring through might determine the natural colonization of food with
DNA acquisition and recombination events allied to particular strains (e.g., due to specificities of nutrient
transmission-favorable contexts might also contribute availability), protect foodborne pathogens from being
to the emergence of unusual problems. In 2011 in the eliminated during food processing or during their pas-
European Union, thousands of people were infected by sage into the host gastrointestinal tract (e.g., bacteria
Antunes et al.
can use food molecules to overcome stress), and can Food matrices could have an impact on the global
induce the expression of virulence features or of cross- stress response of particular strains due to the expression
protection regulatory pathways dealing with multiple of stress cross-protection mechanisms, often described in
stresses in particular strains (96). Thus, bacterial stress foodborne pathogens (91, 103, 117, 148). Poimenidou
response stimulated by the food matrix could have et al. (149) found that tomato-habituated L. monocy-
multiple food safety implications, namely, in the effi- togenes under cold temperatures was more tolerant to
cacy of hurdle technology used in bacterial growth con- acid or osmotic stress than that habituated on lettuce,
trol (e.g., combination and sequence of stresses applied) and lettuce-habituated L. monocytogenes was more
(90). Moreover, more opportunities for pathogen-food- tolerant during heat challenge at 60°C compared to
human transmission might arise through the con- tomato-habituated cells. Also, Salmonella resistant to
sumption of new food vehicles associated with market low water activity found in some food types (e.g. flour,
availability of a variety of food products with specific chocolate, cocoa and hazelnut shells, and dried milk)
intrinsic (e.g., different types of lettuce species) or pro- was more thermotolerant (99).
cessing factors (e.g., sublethal salt concentrations or low It has been suggested that food molecules (e.g., spe-
acid content), possibly allowing survival and multi- cific amino acids, carbohydrates, urea, and fatty acids)
plication of specific strains. Some examples illustrate could protect bacteria from stressful conditions (96).
the interplay between bacterial strains and food matri- Using a simulated gastric passage model (pH 2.5; pepsin;
ces that potentially contribute to pathogen-food-human bile salt and enzymes), Aviles et al. (150) showed that a
transmission scenarios. peanut butter outbreak-associated S. enterica serovar
Vegetables constitute variable challenges (based, e.g., Tennessee strain was better able to survive the acid en-
on nutrient availability, solar irradiation, and micro- vironment when vehiculated in peanut butter matrix
biota competition) to foodborne pathogens, which could with low water activity and high fat content than in low-
fit better or worse accordingly with the interplay of fat formulations. Also, Birk et al. (151) showed that
strain type, plant species, or even plant age (141). For S. enterica serovar Dublin was better protected when
example, with the use of whole-transcriptome analysis, some types of proteins (pepsin, ovalbumin, and turkey
Crozier et al. (124) observed plant species-specific met- meat) were included in a simulated gastric digestion
abolic responses (e.g., to acid and nutrient stress) when compared with bovine serum albumin, indicating that
E. coli O157:H7 (Sakai strain associated with a sprout protection could be protein specific. In a different con-
outbreak in Japan) was exposed to lettuce or spinach text, Liu et al. (152) showed that E. coli LTH5807 dif-
extracts as well as to different parts of the same plant fered in thermal resistance when heated to 60°C on
(leafs or roots). Brandl et al. (142) demonstrated that mung bean, radish, or alfalfa seeds (153).
population sizes of E. coli O157:H7 (lettuce-associated Bacterial stress protection by the food matrix seems to
outbreak H1827 clinical strain) and S. enterica serovar be also related to low infectious doses, as in the case of
Thompson (cilantro-associated outbreak RM1987 clin- salmonellosis epidemiological linked to values of the
ical strain) were higher in young romaine lettuce leaves order of 10 to 100 CFU vehiculated by food with low
(enriched in total nitrogen and carbon) than in middle water activity, compared to >105 CFU in other food
leaves harvested from mature lettuce heads, positioning types (103). Another explanation for such low infectious
younger leaves as vehicles of greater risk to transmit doses is that bacteria could be missed by standard mi-
human pathogens. Moreover, several studies found that crobiological food methods, as dehydration could in-
some foodborne pathogens (e.g., Salmonella, E. coli, duce the bacterial filament form (underestimate the true
and L. monocytogenes) have the ability to internal- number of cells) or the viable but nonculturable (VBNC)
ize in vegetables’ edible parts (e.g., tomatoes and let- state (impairing bacterial growth). Filamentous bacteria
tuce), impairing their removal by standard disinfection seem to be more acid or bile resistant and retained their
methods before human consumption (143–146). Thus, virulence in vitro and in vivo in a mouse model (154),
knowing the interaction of specific strains with partic- and cells in the VBNC state were described in some cases
ular vegetables might contribute to predictive modeling to maintain their pathogenic capacity after resuscita-
or risk-based analysis of the potential for microbial tion (103, 155). For example, it was demonstrated that
contamination, colonization, and persistence in different VBNC cells of C. jejuni maintained the ability to adhere
horticultural crops (each day more often associated with to intestinal cells (156) and VBNC cells of E. coli O157:
outbreaks) (147) and to better understanding of the H7 expressed stx1 and stx2 toxin-coding genes and
transmission routes and vehicles of particular strains. produced the toxin (157, 158). The VBNC state was also
described for other foodborne pathogens such as Shi- duration that shedding occurs, resulting in diverse levels
gella spp., Yersinia enterocolitica, Aeromonas spp., of environmental, animal carcass, or vegetable contam-
Brucella spp., and Vibrio spp. (155), being induced by ination, with impact on pathogen transmission dynam-
several stresses occurring in the food matrices and dur- ics (168, 170). On the other hand, the interplay between
ing food processing or storage (155, 159). Considering bacterial genetic evolution and environmental challenges
the large number of foodborne outbreaks described imposed by the specific physiology of each host (e.g.,
without the identification of the etiological agent, im- related to the variable gut environment in different ani-
plicated food vehicle, or reservoir (13), more knowledge mal reservoirs, changing diets, or antimicrobials used in
is needed to clarify how often VBNC bacteria could intensive animal production) might increase bacterial
be involved in undetected pathogen-food-human trans- shedding from particular individuals and drive strains’
mission events. For example, the STEC O104:H4 of the evolution pathways toward specialist (e.g., one host) or
sprout-associated European outbreak in 2011 was never generalist (multiple hosts) lifestyles (5, 168, 171). A se-
isolated from the suspected origin (fenugreek seeds), and lection of generalist strains conducts to greater trans-
it was shown to be able to enter the VNBC state and mission opportunities among a variety of reservoirs and
resuscitate (160). hosts (172). In contrast, specialist strains have fewer
Finally, the components of food matrices or the opportunities to be transmitted but usually cause more
processing factors applied to them might have an impact severe, chronic and asymptomatic infections, with the
on the expression of foodborne pathogen virulence fac- possibility of long periods of host shedding, sometimes
tors. This is the case for enterotoxins produced by undetected (5). Some examples illustrate the interplay of
Staphylococcus spp., B. cereus, or STEC, in which toxin strain-host scenarios potentially contributing to food-
expression seem to be dependent on the interplay be- borne pathogen-food-human transmission.
tween toxin type, strain, thermal treatment, and food C. jejuni is a major foodborne human pathogen
matrix, although different studies reported disparate vehiculated mainly by contaminated poultry (13, 173).
data (95, 121, 123,161–167). Thus, the certainty of as- C. jejuni can highly colonize poultry (up to 1010 CFU/g
sessing Staphylococcus or B. cereus food poisoning risk feces), and it is suggested that the high body tempera-
through colony-forming units present in food prod- tures (41 to 45°C) of poultry species, the poultry gut
ucts has been disproven, with the scientific community environment, and the inefficiency of poultry immune
and food business operators aware of the threat arising system activation contribute to the persistent coloniza-
from unforeseeable enterotoxin production under stress tion of the avian gut with thermotolerant and micro-
conditions. aerophilic C. jejuni and, consequently, to its continuous
shedding and transmission to the environment and other
Interplay between Bacterial Strains poultry hosts (173, 174). Also, for STEC O157:H7, in-
and Host Favoring Pathogen-Food-Human dividual host features allied to strain and environmental
Transmission Scenarios factors could determine the level of host colonization
A successful host colonization occurs by the ability of and shedding. Cattle are pointed to as the main reservoir
a pathogen to outcompete and outgrow native host of STEC O157:H7, with some animals classified as
microbiota, mostly in the intestinal tract (97, 168). For “super-shedders” when they release ≥104 CFU/g of fe-
that, foodborne pathogens must survive specific stressful ces (175). Strain specificities (e.g., ability to colonize
conditions (e.g., stomach acid, macrophages, and oxi- the rectal-anal junction of cattle), animal features (e.g.,
dative stress) as well as modulate host microbiota (e.g., composition of the cattle native microbiome), and ani-
changing the equilibrium of particular species), the im- mal age and diet seem to determine whether E. coli
mune system (e.g., inducing inflammatory reactions), O157:H7 can proliferate sufficiently for the host to ob-
and, indirectly, the gut physicochemical environment tain super-shedder status (168, 175–177). The supper-
(e.g., available nutrients and oxygen tension) (95, 97, shedding state or a prolonged release period of bacteria
168, 169). A previous contact with stressful conditions in the feces has also been associated with consump-
in the food chain might allow a preadaptation of the tion of antibiotics with impact on the host microbiota.
pathogen to those similarly occurring in the host, or even This was detected for S. Typhimurium in mouse infec-
increase its virulence due to coregulation of stress and tion models, releasing bacteria on the order of >108
virulence genes (90, 105, 109). After the colonization CFU/g, or in outbreaks of S. Typhimurium from roast
step, foodborne pathogens shedding from their hosts pork, in which antibiotic consumption by patients in-
vary in the amount of bacteria expelled and in the creased the carrier state period (125, 178). Prolonged
Antunes et al.
human symptomatic infections (from weeks to several ANTIMICROBIAL-RESISTANT

years) with other NTS serotypes (S. enterica serovars FOODBORNE BACTERIA TRANSMISSION
Mbandaka, Bredeney, Infantis, and Virchow) have also ALONG THE FOOD CHAIN
been described, with antibiotic consumption also cited Antimicrobial resistance is considered a major global
as one of the factors contributing to their persistence public health issue for humans and animals, and a ma-
(170). jor priority in food safety by a number of entities (the
High host shedding of foodborne pathogen strains European Commission, WHO, and Food and Agriculture
allied to favorable transmission patterns might increase Organization of the United Nations) (182–186). Accord-
opportunities to colonize multiple available hosts (e.g., ing to Centers for Diseases Control and Prevention (CDC)
several animal species), which depend on bacteria mak- estimates, antibiotic-resistant infections caused 23,000
ing rapid adjustments to each new host ecosystem. deaths per year in the United States, and about one of five
However, the high prevalence and wide distribution resistant infections were caused by microorganisms from
of the so-called “generalist clonal lineages” complicates food and animals (185, 187–189). Nevertheless, the con-
source attribution, as in the case of C. jejuni ST21/ST45 tribution of food to the transmission to humans of bac-
clonal complexes isolated from poultry, cattle, and in- teria carrying clinically relevant resistance genes is still
fected humans (172). In spite of this, Sheppard et al. poorly established, including the real enrichment of the
(179) showed that within ST21/ST45 clonal complexes human microbiota with such bacteria and genes.
exist sublineages with host association, determined by Although in recent years great effort has been made
the occurrence of the panBCD genes encoding the vita- by different organizations (e.g., the WHO, EFSA, and
min B5 biosynthesis pathway, more prevalent in cattle CDC) to understand the magnitude and burden of an-
(diet composed of grass with low vitamin B5) isolates timicrobial resistance transmission through the food
than in chicken (diet composed of cereal and grains chain, it remains uncertain at the global level (190). It is
abundant in vitamin B5) ones. The discovery by WGS of particularly underestimated in low- and middle-income
gene loci gained or lost makes genetic elements possible countries where drivers of antimicrobial resistance (e.g.,
targets for source tracking, with the genetic makeup of unregulated farming and food-production practices
a human isolate theoretically helping in the potential concerning food safety and antibiotic use; poor hygienic
identification of the isolate source and of transmission conditions, namely, related to water and sewage; and
food vehicles (180). Generalist and specialist lifestyles human travel and migration) are significant, eventually
could also be related to Salmonella serotypes, with affecting the spread of antimicrobial resistance by the
S. Typhi (specialist serotype) associated with human food chain in a wide geographic area (189, 191). The
reservoirs and infections, and the main emerging S. regular use of antimicrobials in livestock (therapeutic,
Typhimurium and S. Enteritidis (generalist serotypes) metaphylactic, prophylactic, or growth-promoting use)
associated with human infections and colonization of associated with modern intensive food-animal produc-
diverse animals (13, 181). It remains to clarify whether tion has been considered the main driver of the selection
generalism is a stable strategy taking advantage of the of both antibiotic-resistant bacteria and genetic elements
large number of transmission opportunities in agricul- worldwide, with food products (e.g., meat, poultry,
ture or whether it reflects insufficient time for well- eggs, vegetables, and farmed fish) the most relevant
adapted host specialist lineages to have evolved in the transmission mode to humans (186, 188, 189, 192).
recent man-made environment. For example, studies on In fact, new WHO guidelines on the use of medically
S. Typhimurium ST313, causing invasive infections in important antimicrobials in food-producing animals
immunocompromised populations in Africa, point to stressed that antibiotic-resistant bacteria in this sector
the presence of degraded genome capacity in the form were reduced by up to 39% after interventions re-
of pseudogenes and deletions, suggesting evolution from stricting antibiotic use at the farm level (186). How-
a generalist to a specialist lifestyle, with transmission ever, other nonantibiotic compounds with antimicrobial
among humans potentially exerting genomic selection activity and widely used in food-animal production
pressure (181). Understanding the differences of food- (e.g., copper) may also contribute to the selection of
borne pathogen lifestyles is important to establish ef- antibiotic-resistant zoonotic bacteria and to less suc-
fective control measures adapted to the context of cessful intervention scenarios related to reduction of
specific hosts as well as to preview future transmission antibiotic use (101, 102, 188, 193).
scenarios of specific foodborne strains through particu- Antimicrobial-resistant bacteria with human rele-
lar reservoirs and food types. vance include pathogenic zoonotic organisms (e.g.,
Salmonella and Campylobacter) as well as likely com- colonization of humans (Fig. 3) (190, 194). In gen-
mensal zoonotic bacteria (e.g., E. coli and Enterococ- eral, these commensal strains with likely animal origin
cus). Both groups have been recognized as important are widespread in multiple hosts and often partici-
or major contributors to the burden of antimicrobial pate in genetic exchange events with other microorgan-
resistance (188, 192, 194). Antimicrobial-resistant zoo- isms sharing the same ecosystems, making direction of
notic pathogenic bacteria may be associated with more- transmission (e.g., food-human, environment-human, or
prolonged infections; treatment failures as a result of human-human) hard to assess (189, 190).
invasive infections; or the use of last-line antimicrobials For several decades, the contribution of food-animal
for therapy, which are more expensive and/or toxic. reservoirs and food vehicles in the transmission of
Commensal zoonotic bacteria could be reservoirs of antimicrobial-resistant bacteria relevant to human health
clinically relevant antibiotic resistance genes mobilizable has been controversial. However, accumulating evi-
to pathogens and be potentially involved in extra- dence linking livestock production with antimicrobial
intestinal opportunistic infections (e.g., urinary tract or resistance burden in humans has been reported (188–
bloodstream infections) after transmission by food and 190, 192, 195), which we classify in three categories.
FIGURE 3 Implications of antibiotic-resistant bacteria transmitted from food to humans.

ABR, antibiotic resistance.
Antunes et al.
Association between the Use of treatment of severe human infections) was commonly
Antimicrobial Agents and the Occurrence detected in Campylobacter and Salmonella from hu-
of Antimicrobial-Resistant Bacteria in mans and poultry. This is illustrated by the high level of
Food-Producing Animals and/or Humans resistance to ciprofloxacin in C. jejuni isolated from
The correlation between antibiotic use and the occur- broilers (69.8%), broiler meat (65.7%), and humans
rence of antimicrobial resistance in bacteria isolated (60.2%). In the case of Salmonella, it was reported that
from the food chain and humans is evident in studies resistance to ciprofloxacin was markedly higher in some
from the last 25 years, including those of zoonotic serotypes commonly associated with poultry (S. Enteri-
pathogens or commensal bacteria. Among the more il- tidis, S. Infantis, and S. enterica serovar Kentucky),
lustrative cases was the consequences of licensing the suggesting a greater contribution of the poultry pro-
fluoroquinolone enrofloxacin for animal use in the duction chain to the human burden (183). Moreover, a
1990s, especially in poultry. It led to increased rates of high prevalence of MDR Salmonella in humans (26%)
ciprofloxacin resistance in S. Typhimurium DT104 re- and poultry meat (broiler, 24,8%; turkey, 30.5%) (in-
covered from animals/food and humans in the United cluding the ampicillin/streptomycin/sulfonamides and
Kingdom (196) and of C. jejuni from humans in the tetracycline resistance [ASSuT] profile) was also de-
United States (197) and from chickens and humans scribed (183). Data from the National Antimicrobial
in The Netherlands (198). More recently, a voluntary Resistance Monitoring System (NARMS) reported an
withdrawal of ceftiofur by poultry producers in Canada increase of S. 4,[5],12:i:- with the ASSuT-MDR pheno-
was correlated with decreasing occurrence of ceftiofur- type in humans, from 43 to 60% between 2014 and
resistant S. Heidelberg (one of the most common sero- 2015, and of 65% in swine from 2015 (206).
types associated with salmonellosis in this country) from In low- and middle-income countries (e.g., in Asia,
both human infections and retail poultry. After rein- African, and Latin America), the rates of antibiotic re-
troduction of ceftiofur 2 years later in poultry produc- sistance, including to clinically relevant antibiotics
tion, an increase in resistance levels in poultry and (ciprofloxacin, extended-spectrum cephalosporins, co-
humans was once more observed (199). Another ex- listin, and carbapenems), are undoubtedly higher than in
ample was the ban of the glycopeptide avoparcin as high-income countries, with food products presenting a
a growth promoter in Europe in the 1990s, which led potential role in its emergence (189). For example, high
to the reduction of vancomycin-resistant Enterococcus levels of Salmonella nonsusceptible to ciprofloxacin
in community settings (producing animals and healthy (15 to 48%) and cephalosporins (38% to ceftriaxone)
humans) (200–203). Evidence on the correlation be- were observed in humans from Asian countries (207,
tween antibiotic consumption and resistance among 208). These data are in agreement with several studies
foodborne pathogens from humans and food-producing documenting a high prevalence of resistance to fluoro-
animals was also corroborated by the last European quinolones (>22.5% to ciprofloxacin) and cephalospo-
Centre for Disease Prevention and Control (ECDC)/ rins (12.5 to >23.4% to ceftriaxone and 26.6% to
EFSA/European Medicines Agency (EMA) joint re- ceftazidime) in Salmonella from poultry meat obtained
port involving univariate/multivariate analysis in almost in South Korea and China (209, 210), as well as in
30 European countries. It demonstrated that resistance E. coli from farmed fish (36.7% reduced susceptibility
to fluoroquinolones in Salmonella and Campylobacter to ciprofloxacin) in China (211). Also, a recent Chinese
and resistance to macrolides in Campylobacter coli from surveillance study revealed high rates of the new
humans were related to the consumption of fluoro- plasmid-mediated colistin resistance gene mcr-1 in di-
quinolones or macrolides, respectively, in animals (204). verse foodborne bacteria recovered from water (71%
Previous findings have also suggested a link between of samples), animal feces (51%), food products (36%,
S. Enteritidis resistance to nitrofurans and their illegal mostly meat), and humans (28% of human subjects
use in food-producing poultry in Portugal (205). surveyed), further supporting the role of the food chain
in the transmission of colistin-resistant bacteria and the
Correlation between Rates of Antibiotic mcr-1 gene to humans (212). However, direct zoonotic
Resistance among Bacteria from Food- transmission of mcr-1 could not be excluded, as stated
Producing Animals, Food, and Humans by the association of colonization of farmers with mcr-
Obtained from Systematic Surveillance Data 1-carrying bacteria with exposure to mcr-1-positive
The 2016 EFSA reported that resistance to widely used chickens from small-scale poultry farms in Vietnam
antimicrobials (including critical ones important for the (213).
The role of low- and middle-income countries as mission of Salmonella, E. coli, and Enterococcus spp.
largely exporters of food to different geographic regions clones from the food chain to humans. It includes studies
of the world, their changing from extensive farming developed in diverse time frames that established such
systems to large-scale ones with a higher use of anti- linkages. Other examples including only mobilization of
biotics due to consumer demand for protein, and the genetic elements are discussed in the paragraphs below.
largely unregulated use of antibiotics in animal pro- In several European countries, multiple clones of
duction suggest that international trade of contaminated pathogenic Salmonella serotypes ESBL producers (e.g.,
breeding animals (e.g., poultry production depends on CTX-M-2, CTX-M-9, and TEM-52) shared between
a pyramid-like breeding system), feed, and meat prod- poultry and human cases have been reported (Table 1).
ucts with antibiotic-resistant foodborne pathogens may A recent example describes an MDR and ESBL-
contribute to the rapid worldwide spread of these bac- producing (CTX-M-1) clone of S. Infantis causing hu-
teria, with impact on human health (214). The last man infections and isolated from poultry (including
DANMAP (Danish Integrated Antimicrobial Resistance meat) in Italy during 2001 and 2014 (Table 1) (219). In
Monitoring and Research Programme) report described Canada, the transmission of S. Heidelberg (one of the
higher levels of extended-spectrum β-lactamase (ESBL)/ top MDR poultry-related serotypes in North America)
AmpC-producing E. coli (56% of samples, including between abattoir, retail poultry, and humans as well
ST131 clone) and ciprofloxacin resistance in C. jejuni as the transmission of a common CMY-2 plasmid
(71% of isolates) from imported broiler meat compared among those strains was suggested (220). Also of con-
with domestically produced broiler meat (23% of the cern is the dissemination of the ciprofloxacin-resistant
samples with ESBL/AmpC-producing E. coli and 22% S. Kentucky ST198 strain (with a reservoir in northern
of C. jejuni isolates with ciprofloxacin resistance) (215). Africa [Egypt]) in Europe and elsewhere since 2010,
Recently, Brazilian imported poultry meat contaminated including that associated with an increasing number of
with extended-spectrum cephalosporin-resistant blaCMY-2- contaminated sources, mainly poultry but also seafood
producing S. Heidelberg (a poultry-related serotype (221). A possible transmission from pork products to
uncommon in Europe) was reported in Europe and in- humans of mcr-1 colistin resistance observed in an MDR
cluded strains with indistinguishable PFGE profiles from and copper-tolerant clinically relevant S. 1,4,[5],12:i:-
epidemic clones with invasive potential that caused out- clonal lineage was suggested in a Portuguese study
breaks in the United States, alerting for potential risk to (222). Other studies also point to the food chain as an
human health (60, 61). The spread of E. coli carry- important reservoir of mcr-1-bearing plasmids trans-
ing blaCMY-2 from flocks of imported broiler parents to mitted among different bacterial clones and species (213,
broiler meat (including potentially human-pathogenic 223) and suggest that mcr-1 first arose in animals before
types), even in a country with no cephalosporin use being transmitted to humans, due to colistin use in food-
(216), suggests that the globalization of trade of food animal production (152). Other descriptions of shared
animals and food products is an important driver of genetic elements include identical oqxAB-carrying plas-
antibiotic resistance spread through the food chain. mids carried by Salmonella and E. coli and identified in
food products and humans, particularly in China (177),
Transmission of Clinically Relevant Antibiotic with a few reports of shared clones (224).
Resistance Genes on Mobile Genetic Elements In relation to commensal zoonotic bacteria, evidence
and/or Antibiotic-Resistant Clones of Zoonotic of antibiotic resistance transmission between animals/
Pathogens and Commensal Bacteria from food and humans is harder to establish, with some
Producing Animals and Food to Humans studies reaching different conclusions (195, 225, 226).
Transmission of antibiotic-resistant clones and genetic Those suggesting such transmission through the food
elements between bacteria (pathogens and commensal) chain were based on the detection of common clinically
from the food chain to humans has been described in relevant genes, mobile genetic elements (e.g., plasmids),
recent decades (189, 191, 195, 217, 218). With the and/or clones between food and humans (including
evolution of molecular methods (WGS versus multilocus those associated with infections). For example, trans-
sequence typing [MLST] and PFGE), the accuracy of mission from livestock and/or retail meat to humans
such linkages may be clearer in the near future as data of ESBL and AmpC β-lactamase genes on plasmids (in-
accumulate, by facilitating the identification of new cluding plasmids shared with pathogenic bacteria like
cases as well as confirming or contesting older ones. Salmonella) and/or of E. coli clones has been suggested
Table 1 shows examples illustrating linkage and trans- (195, 218, 226–232). The last DANMAP also reported
16
Antunes et al.
TABLE 1 Antibiotic-resistant pathogens and commensal zoonotic bacteria recovered from food products and humansa
Clinically relevant
Clonality antibiotic resistance Genetic element Food source Country(ies)/
Bacteria approach gene(s) PL – Inc group (human source) year(s) Reference(s)
Salmonella
S. 1,4,[5],12:i:- PFGE MCR-1 PL-X4, HI2 Pork products (clinical cases) Portugal/2011–2015 222
S. Enteritidis PFGE, phage typing ESBL-CTX-M-15 PL – FII Chicken meat, chicken feces, or Korea/2009 245
diseased chicken (clinical cases)
S. Heidelberg WGS-based hqSNV AmpC-CMY-2 PL – I1 Retail poultry, abattoir poultry Canada/2012 220
(clinical cases)
S. Heidelberg PFGE, MLST AmpC-CMY-2 PL – I1, A/C Imported poultry meat (clinical Portugal/2014–2015; 60, 61
cases) The Netherlands/1999–2013
S. Heidelberg PFGE AmpC-CMY-2 PL – I1 Chicken abattoir, chicken retail, Canada/2002–2004 246
bovine and porcine (clinical cases)
S. Indiana PFGE ESBL-CTX-M-65, PL-NR Chicken (clinical cases) China/2009–2013 224
CTX-M-14; PMQR-AAC
(6′)-IB-CR+OQXAB
S. Infantis PFGE, MLST, ESBL-CTX-M-1, PL-I1+P Broiler meat, broiler chickens Italy/2011–2014 219
WGS-based SNP CTX-M-65 (clinical cases)
S. Infantis PFGE ESBL-TEM-52 PL – I1 Poultry (clinical cases) Belgium/2001–2005 247
S. Kentucky PFGE, MLST CipR- Poultry and turkey meat, seafood, Europe, Asia/2000–2013 221
(ST198-X1-SGI1) broilers (clinical cases)
S. Typhimurium PFGE ESBL-CTX-M-2 PL – NR Poultry (clinical cases) Brazil/2003–2004 248
PFGE ESBL-CTX-M-1 PL – N Swine meat (human) Germany/2007 249
S. Virchow PFGE, MLST ESBL-CTX-M-15 PL-HI2 Poultry meat, pig farms (clinical Korea/2012 98
cases)
PFGE ESBL-CTX-M-2 PL – NR Poultry (clinical cases) Belgium-France/2000–2003 250
PFGE ESBL-CTX-M-9 NR Broilers (clinical cases) Spain/2000–2004 251
Escherichia coli
A-ST-10, ST-117 MLST ESBL-diverse Chicken meat, other meats The Netherlands 228
(healthy humans-fecal, and
human blood)
O25:H4-B2-ST131 MLST, PFGE ESBL-CTX-M-9 Chicken meat and avian (human Spain/1993–2010 252
infections)
ASMscience.org/MicrobiolSpectrum
A-ST-10, ST-117 MLST ESBL-CTX-M-1, TEM-52 PL-I1 (ST3, ST7, ST10) Poultry (blood and urine isolates) The Netherlands/2006–2010 230
A, B1, D MLST, AFLP, PFGE ESBL PL Chicken meat (human carrier or The Netherlands/2008–2009 227
blood isolates)
ST38 WGS-based SNP; AmpC-CMY-2 PL-K Chicken meat (clinical isolates- Norway/2012–2014 232
MLST urinary tract infections)
Enterococcus
Enterococcus faecium PFGE aac(6′)-Ie-aph(2″)-Ia NR Poultry carcasses (healthy human Portugal/2001 233
feces)
Enterococcus faecalis PFGE aac(6′)-Ie-aph(2″)-Ia NR Poultry carcasses (healthy human Portugal/2001 233
feces)
PFGE aac(6′)-Ie-aph(2″)-Ia NR Poultry carcasses United States/1998–2000 234
(outpatients’ feces)
PFGE aac(6′)-Ie-aph(2″)-Ia NR Ground pork (healthy United States/1998–2000 234
human feces)
aAbbreviations: AFLP, amplified fragment length polymorphism; hqSNV, high-quality core genome single-nucleotide variant; NR, not reported; NT, plasmids that were not typeable with the scheme used; PL,
plasmid.
the observation of phylogenetically related (WGS-based globalization of food production; consumer health sta-
single-nucleotide polymorphism [SNP]) ST131 blaCMY-2- tus, lifestyles, and behaviors; and bacterial adaptation to
producing E. coli from imported meat and human different challenges from farm to human make the pre-
bloodstream infections in Denmark during 2015-2016, vention of bacteria-food-human transmission a modern
thus suggesting a potential zoonotic link between imported and continuous challenge. To minimize the selection and
broiler meat and severe human infections (215). Among spread of foodborne zoonotic pathogens and commen-
Enterococcus spp. the same clones of a gentamicin- sals, including MDR, it is critical to improve biosecurity
resistant E. faecalis or E. faecium were found in the feces measures from the farm (e.g., high hygiene standards
of healthy humans and in poultry carcasses for human and vaccination) and throughout the food chain (e.g.,
consumption in Portugal (233). Clonal linkage between slaughtering and food processing, food handling, and
poultry or ground pork for human consumption and education of consumers); to control antibiotic use, and
humans was also detected in the United States (234). the live-animal and food trade; as well as to explore
Freitas et al. (235) detected the same MDR, vancomycin- bacterial adaptation mechanisms to food production
resistant E. faecium clone (CC5-PFGE A) in a piggery ecosystems. A global One Health approach is manda-
environment, feces from live and slaughtered swine, tory to better understand and minimize the transmission
healthy human feces, and hospitalized patients, strongly pathways of human pathogens through the food chain
suggesting its transmission across the food chain in (8, 189).
Europe and the United States between 1995 and 2008.
Tn1546-vanA with the same structure and shared by ACKNOWLEDGMENTS
We thank the European Society of Clinical Microbiology and
humans and food animals was also described (236, 237).
Infectious Diseases (ESCMID) Food- and Water-borne Infections
More recently, new alerts of public health threats, Study Group (EFWISG).
but those with indefinable risks for human health, linked
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Food-to-Humans

human symptomatic infections (from weeks to several ANTIMICROBIAL-RESISTANT

FIGURE 3 Implications of antibiotic-resistant bacteria transmitted from food to humans.

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