Microbiological Hazards and Their Control
1.5 Foodborne Illness: Etiologic Agents and Contaminants .1 Bacteria.1 Bacteria
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Practice for Eggs and Egg Products” (CAC 2007b), “Guidelines on the Application of General Principles of Food Hygiene to the Control of Listeria monocytogenes in Ready-to-Eat Foods” (CAC 2007c),
“Code of Hygienic Practice for Powdered Formulae for Infants and Young Children” (CAC 2008b),
“Guidelines on the Application of General Principles of Food Hygiene to the Control of Pathogenic Vibrio Species in Seafood” (CAC 2010), “Guidelines for the Control of Campylobacter and Salmonella in Chicken Meat” (CAC 2011), “Guidelines on the Application of General Principles of Food Hygiene to the Control of Viruses in Food” (CAC 2012), “Principles and Guidelines for the Establishment and Application of Microbiological Criteria Related to Foods” (CAC 2013a), “Guidelines for the Control of Taenia saginata in Meat of Domestic Cattle” (CAC 2014) and “Guidelines for the Control of Trichinella spp. in Meat of Suidae” (CAC 2015). As an “international non-governmental observer (INGO)” to CCFH, ICMSF has played an active role in the development of these international standards.
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In recent years, the incidence of disease caused by thermophilic Campylobacter spp. has increased prominently in many industrialized countries (Friedman 2004). For instance, Campylobacter is the second most common bacterial cause for hospitalization associated with foodborne illness in the U.S. (Scallan et al. 2011a), and it is the leading bacterium responsible for infectious intestinal illness in the U.K. (Tam et al. 2012). Outbreaks of campylobacteriosis are rare, with most cases being sporadic and commonly attributed to undercooked poultry or cross-contamination from raw poultry. Other foods, untreated water, and raw milk also have been implicated (Altekruse et al. 1999).
In countries where raw fish is an important part of the diet, disease caused by Vibrio parahaemo-lyticus is frequent. Occasional outbreaks occur in western countries, but there the vehicle of transmis-sion is usually processed rather than raw seafoods. Notably, consumption of raw oysters contaminated with Vibrio vulnificus pose significant concern for immunocompromised individuals. Vibrio cholerae is endemic in many tropical countries, and water plays a major role in the epidemiology of cholera.
Shigella spp. also represent an important public health problem in many developing countries and cause significant illness in developed countries. Cases of shigellosis reported in developed countries are often associated with travelling, food handlers, and day care centers. Because the reservoir of Shigella spp. is restricted to humans, the source of infection is food or water contaminated by human carriers.
Disease caused by Yersinia enterocolitica and Yersinia pseudotuberculosis occurs worldwide and has been primarily associated with the consumption of raw or undercooked pork and produce held at refrigeration temperatures for extended periods.
Escherichia coli strains are a common part of normal microbial flora of animals, including humans.
Most strains are harmless, but some cause diarrhea. Strains carrying particularly virulent properties have emerged as a serious hazard, with consumption of even low numbers of these organisms bearing a risk for life-threatening illness. During the last three decades, enterohaemorrhagic E. coli (EHEC), producing verocytotoxins (VTs), also called Shiga toxins (STs), have emerged as a serious foodborne hazard. Many different serotypes of E. coli produce VTs or STs. Initially, most human outbreaks of EHEC were due to E. coli O157:H7, although serogroup O111 is the most common cause of illness in Australia. Human illness has now been associated with many verocytotoxin-producing serotypes of E. coli, with serotypes O157, O26, O45, O103, O111, O121, and O145 being responsible for some 90% of illnesses. Human cases of EHEC were initially associated with consumption of undercooked ground beef (Bell et al. 1994) and, occasionally, unpasteurized milk. However, fresh fruits and vege-tables contaminated with EHECs are being implicated in a growing proportion of outbreaks (Sivapalasingam et al. 2004; Mahon et al. 1997; EFSA 2007; FAO/WHO 2008b; Lynch et al. 2009;
Mathusa et al. 2010; Beutin and Martin 2012; Soon et al. 2013; Olaimat and Holley 2012). Outbreaks have also been traced to unpasteurized apple juice (“apple cider” in the U.S.), yogurt, fermented sau-sage, water, and contact with farm animals (Doyle et al. 1997; Mathusa et al. 2010). Of particular note is the major outbreak in Europe involving Shiga toxin-producing E.coli (STEC) O104:H4 present in fenugreek spouts (Beutin and Martin 2012; EFSA 2012; Soon et al. 2012), with this strain also shar-ing virulence characteristics with enteroaggregative E.coli (EAEC).
Disease caused by L. monocytogenes is not frequent, but can be severe, with a high mortality rate in populations at risk, such as infants, pregnant women, and the immunocompromised. The bacterium is ubiquitous and foods implicated in outbreaks range from products made from raw milk, butter, ready-to-eat meat products, surimi, smoked mussels and trout, fruits and vegetables. Two major out-break of listeriosis for instance occurred in Canada in 2008, one major outout-break being linked to ready-to-eat meat cuts and another one to the consumption of cross-contaminated pasteurized milk cheese (Gaulin et al. 2008; PHAC 2008). Two other significant public health events in the U.S. linked to L. monocytogenes were an outbreak of listeriosis attributable to contaminated cantaloupe and milk shakes made from contaminated ice cream (CDC 2012, 2015).
Specific international attention has been given to the safety of food for infants and young children as it relates to the possible presence of Cronobacter spp. (previously referred to as Enterobacter saka-zakii) in powdered formulae (Norberg et al. 2012; Yan et al. 2012). Cronobacter spp. has been
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mented as a rare cause of outbreaks and sporadic cases of neonatal meningitis, necrotizing enterocolitis, and sepsis in infants with a high mortality. They are ubiquitous in nature, and have been found to occur in different food operations as well as in consumer homes (Kandhai et al. 2004). Among infants, those at greatest risk are infants less than 2 months of age, particularly pre-term infants, low birth weight infants (<2500 g), and immunocompromised infants. FAO and WHO have established two international risk assessments on the topic (FAO/WHO 2006b, 2008a). Other than powdered infant formulae, no food source has specifically been epidemiologically linked to disease caused by Cronobacter spp. and therefore the focus of food safety management has been on the potential pres-ence of these pathogens in processing facilities for infant formulae, raw materials and finished products.
Botulism occurs relatively infrequently, but remains a serious concern because of the life-threaten-ing nature of the disease and the impact on trade of the incriminated product type. For many years, commercially processed foods were less frequently involved than home-canned or home-prepared foods, but more recently several commercially prepared products have been implicated. Faulty pro-cessing and/or inappropriate storage temperatures have been the most common reasons for botulism, with home-processed foods and foods mishandled in food service establishments also responsible.
Foods implicated include hot sauce containing jalapeño peppers prepared without adequate heating, potato salad prepared with foil-wrapped baked potatoes previously stored at room temperature, sau-téed onions in butter stored unrefrigerated and then served on a sandwich, tiramisu-mascarpone cheese under-processed canned chili and non-refrigerated carrot juice. With improved refrigerated storage during food distribution and use, Staphylococcus aureus and Clostridium perfringens now cause illness only when there has been temperature abuse. Due to improved refrigeration, however, the shelf-life of many foods has lengthened possibly leading to a new concern that psychrotrophic pathogens may increase to dangerous levels without spoilage being evident to the consumer.
Microorganisms of most concern in this regard are non-proteolytic strains of C. botulinum types B, E, and F, L. monocytogenes and Y. enterocolitica, all of which cause little or no deterioration of the food supporting their growth.
Other foodborne bacterial pathogens include Streptococcus pyogenes, Mycobacterium tuberculosis, Brucella abortus, and Bacillus cereus. An overview of relevant pathogens for a range of food com-modities has been compiled (ICMSF 1998b, 2005).
1.5.2 Viruses
Hepatitis A virus (HAV),norovirus (NoV) (formerly known as Small Round Structured Viruses, or SRSVs, or Norwalk/Norwalk-like viruses),and rotavirus are known causes of foodborne illness. As methods of detection have improved and national initiatives on surveillance and ascertainment are being intensified, NoV has been recognized more often as the most important cause of non-bacterial gastroenteritis throughout the world (Caul 2000). Viruses are occasionally involved in large outbreaks (Weltman et al. 1996), but the true extent and importance of viruses in foodborne illness has not been adequately assessed (ACMSF 1995). Studying the burden of foodborne illnesses in the USA, Mead et al. (1999) already estimated that viruses are more important than bacteria and protozoa as a cause of foodborne illness. This was confirmed by more recent data (Scallan et al. 2011a) establishing that norovirus alone is responsible for 58% of illnesses, as compared to 30% in total being caused by the top three bacterial pathogens (i.e., non-typhoidal Salmonella spp., C. perfringens, and Campylobacter spp.). Next to being the leading cause of foodborne illness, NoV was identified as the cause of second highest number of hospitalizations and the fourth highest cause of death (Scallan et al. 2011a).
Surveillance of infectious intestinal illness data from the UK suggest that norovirus, sapovirus and rotavirus are the leading causes there (Tam et al. 2012). In Australia, NoV was identified as the
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leading cause of foodborne illness, accounting for 30% of illnesses (Hall and Kirk 2005). Live bivalve molluscs are often implicated in viral foodborne disease outbreaks (Halliday et al. 1991). A review of food- and waterborne outbreak events due to NoV between 2000 and 2007 revealed that in 42.5% of the cases the food handler was responsible for the outbreak, contaminating sandwiches and catered meals, followed by water (27.5%), bivalve shellfish (17.5%) and fresh produce (12.5%) (Baert et al.
2009). A review of the global burden of disease and of particular viruses of concern determined that NoV and HAV are most frequently involved in foodborne viral infections (FAO/WHO 2008c), based on the symptoms of infection, these viruses can be grouped into those that cause gastroenteritis (NoV, human rotavirus, astroviruses, Aichi virus, Adenoviruses and Sapoviruses), enterically transmitted hepatitis (caused by HAV and Hepatitis E virus, which migrate to the liver, where they manifest dis-ease), and a third group which replicates in the human intestine, but only cause illness after they migrate to other organs such as the central nervous system (Enterovirus).
1.5.3 Protozoa
Foodborne protozoa have also been incriminated in large outbreaks, e.g., Cryptosporidium parvum from apple juice and water (Osewe et al. 1996), and Cyclospora cayetanensis from raspberries, let-tuce, and water (Speer 1997). In immunocompromised persons, diarrhea may be severe, making the illness serious and difficult to treat. Large outbreaks in North America have had a huge impact on international trade in soft fruit and salad vegetables because if present on the initial crop, these proto-zoa are almost impossible to eliminate. Illness due to Toxoplasma gondii is also much more serious in immunocompromised persons and pregnant women. In the USA, T. gondii is an important cause of hospitalization and death in the US (Scallan et al. 2011a) and a major economic burden among the foodborne diseases, due to deaths and life-long impairments of infected infants (Batz et al. 2011).
Sporadic cases of protozoal infection have also been linked to consumption of undercooked meat, primarily pork, and fish products.
1.5.4 Seafood Toxins
Disease caused by histamine and other biogenic amines can arise from several foods, notably scom-broid fish species. In North America, illness attributed to histamine is the second most common dis-ease from fish, excluding shellfish (MMWR 2000).
The principal intoxications having a microbiological origin in seafood include paralytic shellfish poisoning (PSP), diarrhetic shellfish poisoning (DSP), neurotoxic shellfish poisoning (NSP), amnesic shellfish poisoning (ASP) (also known as domoic acid poisoning), ciguatera, and scombroid (hista-mine) fish poisoning. PSP, DSP, and NSP are caused by toxins produced by dinoflagellates, and ASP by a diatom. All these diseases typically result from consumption of bivalve molluscs that have been feeding on the toxigenic algae. The toxin(s) causing Ciguatera are derived from toxigenic microalgae growing in and around tropical coral reefs and passed up the marine food chain through herbivorous reef fish to more far-ranging carnivorous species. Humans typically become intoxicated from eating the toxic fish. Histamine or scombroid poisoning is caused by consumption of fish containing high levels of histamine (and other biogenic amines) resulting from histidine dehydrogenase activity of bacteria multiplying on the fish after death. With the exception of histamine and other biogenic amines, toxin accumulation is passive. All the seafood toxins are resistant to heating and, therefore, cannot be destroyed by cooking. They are undetectable organoleptically (ICMSF 1996; Liston 2000;
Whittle and Gallacher 2000).
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1.5.5 Toxigenic Fungi
Mycotoxins are fungal metabolites which when ingested, inhaled or absorbed through the skin, can cause disease or death in man and animals. Although there are many types of toxic metabolites, most are of little concern for humans, either because their toxicity is limited or because they are produced by species that are uncommon in foods. The most important mycotoxins are aflatoxins (B1, B2, G1 and G2), ochratoxin A, fumonisins, deoxynivalenol, zearalenone (Miller 1995) and patulin. These toxins are produced by a few species of fungi from the common genera Aspergillus, Penicillium and Fusarium. These fungi may grow and produce toxins on the crop before harvest or after harvest dur-ing drydur-ing and storage. The production of mycotoxins also depends on a wide variety of agronomic and climate conditions as well as on whether a particular cultivar is grown within the area to which it is adapted (Pitt et al. 2012; Taniwaki and Pitt 2013).
On a global scale, the most important mycotoxins are the aflatoxins that are produced by Aspergillus flavus, A. parasiticus, A. nomius and related species, growing mainly in peanuts, tree nuts, cotton seed and maize. Aflatoxins have a likely involvement in five toxic effects: acute toxicity, liver carcinogenic-ity, growth retardation in children, immunosuppression and liver cirrhosis. Aflatoxins cause primary liver cancer in humans and outbreak cases and deaths related to consumption of food contaminated with aflatoxins have been reported, especially in developing countries (Azziz-Baumgartner et al.
2004; Lewis et al. 2005; Taniwaki and Pitt 2013). Ochratoxin A is a chronic nephrotoxin, affecting kidney function in all animal species tested, and probably has a role in kidney disease in wide areas of Europe. Ochratoxin A is produced by three well defined groups of fungi: firstly, the ochre coloured aspergilli, comprising Aspergillus ochraceus, A. westerdijkiae, A. steynii and a few other related spe-cies; secondly, the black aspergilli, A. carbonarius and common species A. niger, which produces OTA only infrequently; and, thirdly, the Penicillium species, P. verrucosum plus the closely related species P. nordicum (Frisvad et al. 2006; Pitt and Hocking 2009). Another role in human disease is probable for fumonisins, produced by Fusarium verticillioides and F. proliferatum during growth in maize, which have been implicated in human esophageal cancer. It has been shown that some fumoni-sins are also produced by Aspergillus niger, an entirely unexpected source (Frisvad et al. 2007).
Aspergillus niger has usually been regarded as a benign fungus and has been widely used in enzyme production and ingredients for food processing. It holds GRAS (generally regarded as safe) status and is among the most commonly reported from foods. The possibility of co- occurrence of ochratoxin A and fumonisin B2 in foods is of concern (Taniwaki and Pitt 2013). Trichothecene toxins, such as deoxynivalenol and nivalenol produced by Fusarium graminearum and related species in cereals, cause immunosuppresssion and consequently have a potentially important role in reducing disease resistance, which as yet is ill-defined. Zearalenone is an oestrogenic mycotoxin and is produced by the same Fusarium species that produce DON and nivalenol, and generally under the same conditions;
the main sources are maize and small grains. Patulin is produced mainly by Penicillium expansum and P. sclerotigenum and the occurrence of this toxin is related to apple products. Patulin shows neuro-toxic activity for certain animals but in humans, it is still unclear whether there are harmful effects.