Annex 6

Objective 6: Veterinary and Human Disease Risks

Contents

1. Hazard Identification & Characterisation 21.1 Livestock Diseases 21.2 Bacteria 21.3 Common Foodborne Bacteria 21.4 Other Bacteria 31.5 Viruses 41.6 Parasites 61.7 Prion Diseases 71.8 Mycotoxins 71.9 Heat Treatment 82. Disease Risk Assessment 9References 10

Table 1. Potential Food waste-borne Infectious Disease Agents of Ruminants, Pigs and Poultry.

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Table 2. Disease Risks from pathogens of Ruminants, Pigs and Poultry contaminating Food waste.

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1. Hazard Identification & Characterisation

Food waste containing meat or meat products can be a potential source of infection from a range of bacteria (including antimicrobial-resistant strains which may also be able to transfer resistance genes to new hosts) viruses, and parasites. Contaminated foods can also lead to exposure to various toxins. Whilst prion diseases would also pose a serious risk from food waste, there is stringent legislation in force requiring the removal and disposal of Specified Risk Material (SRM) at the abattoir prior to entering the food chain. The feeding of food waste to livestock has therefore been implicated as a means of international transmission of major exotic livestock diseases, and of the spread of these diseases within infected countries.

1.1 Livestock Diseases

Bacterial, viral and parasitic disease agents of livestock considered in the risk assessment are listed in Table 1. As bacterial identification and classification are constantly changing, the terminology used in this report will follow the classification based on the International Code of Nomenclature of Bacteria system wherever possible. The system of virus classification referred to throughout is that used by the Foodborne Viruses in Europe network (FBVE) joint electronic database to (www.rivm.nl/bnwww) (Koopmans et al., 2003). For parasites the system of classification is that used by standard parasitological texts (Taylor Coop and Wall 2007). Many of the listed agents are also zoonotic.

1.2 Bacteria

Many bacteria can cause foodborne illness in humans and disease in animals. In the UK, Campylobacter, Salmonella, Escherichia coli and Clostridium are the commonest bacterial causes of foodborne infection in humans. In addition to disease caused by direct bacterial infection, some foodborne illnesses are caused by exotoxins which are excreted as the bacteria grow, and they can cause illness even when the microbes that produced them have been killed.

1.3 Common Foodborne Bacteria

Campylobacter jejuni is recognized as one of the main causes of bacterial foodborne disease in humans in many countries, with poultry an important source of infection (Hermans et al 2012). While C. jejuni is the commonest species found in poultry it is not considered to be pathogenic in poultry, unless co-infections with other pathogenic organisms are present. C. coli frequently infects pigs (Thakur and Gebreyes, 2005), and can cause foodborne disease in humans (Humphrey et al., 2007). C. fetus is a cause of spontaneous abortions in cattle and sheep, as well as an opportunistic pathogen in humans. The common route of transmission is by the ingestion of contaminated food or water, and the eating of raw meat, particularly poultry in humans. Infection in calves produces diarrhoea, sometimes bloody, mainly in young animals.

Salmonella infections are zoonotic and can be transferred between humans and animals. Current nomenclature suggests that Salmonella consists of two species - S. enterica and S. bongori, with six subspecies; however, traditional nomenclature is still commonly used by specialists in microbiology. Many infections are due to ingestion of contaminated food. Thus food is an important infection route for enteritic Salmonella including those that are resistant to antimicrobials (European Food Safety Authority, 2006). Antimicrobial-resistant Salmonella causing foodborne human disease are well documented. Implicated foods are typically beef, pork, poultry, dairy products, but also eggs and fresh produce.

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Virulent strains of Escherichia coli (enteropathogenic [EPEC], enterohaemorrhagic [EHEC] and enterotoxigenic [ETEC] strains) can cause gastroenteritis, urinary tract infections, and neonatal meningitis. Infections with multi-resistant E. coli are an important public health problem. Transmission of pathogenic E. coli often occurs via the faecal-oral route. Common routes of transmission include unhygienic food preparation, and a range of food products have been associated with E. coli outbreaks. Dairy and beef cattle are primary reservoirs of E. coli O157:H7 and can carry it asymptomatically and shed it in their faeces. Enteric colibacillosis is a common disease of young calves and piglets caused by colonisation of the small intestine by enterotoxigenic strains of E. coli.

Clostridia are a group of obligate anaerobic bacteria consisting of around 100 species that include common free-living bacteria as well as important pathogens in animals and humans. Clostridia are motile bacteria that are ubiquitous in nature and are especially prevalent in soil and decomposing plant material. Some species are normal inhabitants of the intestines and, after the death of the animal, rapidly invade the blood and tissues playing a major role in decomposition of the carcass. Pathogenic clostridia affecting cattle and sheep have been divided into three main groups. Neurotrophic clostridia include C. tetani and C. botulinum, which produce powerful neurotoxins giving rise to the diseases tetanus and botulism respectively. Histotoxic clostridia produce exotoxins that cause local tissue necrosis and systemic toxaemia. Examples include C. chauvoei, the major cause of blackleg; C. novyi type B, which causes black disease; C. septicum which causes malignant oedema and braxy; C. haemolyticum (C. novyi type D), which causes bacillary haemaglobinuria; and C. sordelli which causes gas gangrene. Enterotoxic clostridia include C. perfringens type D, which causes pulpy kidney disease; C. perfringens type C, which causes struck; and C. perfringens type B, which causes lamb dysentery.

C. difficile is a commensal bacterium of the human intestine but has become increasingly important as a cause of antibiotic-associated diarrhoea in humans. Foodborne transmission of C. difficile has been suggested as a possible source of human infections, but evidence to confirm this is incomplete.

Listeria are Gram-positive, non-spore forming bacteria, which can be often be found in the environment of farms (Nightingale et al., 2004) and food processing plants (Chasseignaux et al., 2002). There are several species, most of which cause opportunistic infections in humans. The most significant pathogen is L. monocytogenes. Infection by this agent can cause several symptoms including meningitis and endocarditis, and complications of pregnancy (Farber and Peterkin, 1991) L. monocytogenes has been isolated from cattle, sheep, goats and poultry (Gray and Killinger, 1961). A survey performed in the UK in 2003 of 2981 samples of modified-atmosphere-packed and vacuum-packed cooked ready-to-eat meats sold at retail found that 1 % contained L. monocytogenes at levels >102 cfu per gram (Sagoo et al., 2007), and a later UK survey of speciality meats sold at retail found several samples containing similar levels (Gormley et al., 2010).

1.4 Other Bacteria

A range of other bacteria found in livestock have the potential for foodborne transmission and are summarised in Table 1.

The spore-forming bacterium Bacillus anthracis, the causative agent of anthrax, commonly infects wild and domesticated herbivorous mammals. The disease is endemic but sporadic in the UK and can be spread by consumption of contaminated meat and meat products. Anthrax spores can survive for very long periods of time in the environment.

Bacillus cereus is a facultative anaerobic bacterium associated with food poisoning in humans. The food poisoning is a result of ingesting heat-stable enterotoxins produced by the

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bacterium. B. cereus is widespread in the soil and can contaminate such foods as herbs, spices, milk and vegetables. Spores of this organism are heat-resistant and can survive cooking, and a broad range of cooked or processed foods have been associated with infection including vegetables and meats, boiled or fried rice, soups, ice cream, herbs and spices.

Methicillin-resistant S. aureus (MRSA) is recognised as a zoonotic agent following detection in various companion and food-producing animals, including horses, dogs, cats, pigs, cattle, chickens, rabbits and birds. A particular MRSA strain (NT “non-typeable”) has increasingly been isolated from pigs and pig farmers. A recent Dutch study showed that MRSA can be detected at very low concentrations (<10 cfu/g) in unheated meats from various domestic animals and poultry (de Boer et al., 2009). A UK study conducted between 2006 and 2007 (Food Standards Agency Report B18018) indicated that approximately 8 % of red meat produced and sold at retail in the UK was contaminated with S. aureus; no information is available on whether these harboured antibiotic resistance determinants however. Another UK study found MRSA in bulk milk (Garcia-Alvarez et al., 2011).

Mycobacterium bovis is a slow-growing, aerobic bacterium and the causative agent of tuberculosis in cattle (bovine TB). M. bovis may be transmitted to humans via infected milk, although it can also spread via aerosol droplets. Human infections are rare, mostly due to pasteurisation killing any bacteria in infected milk. Cattle are randomly tested for the disease and immediately culled if infected, and depending on the lesions found at meat inspection, the whole carcase is either condemned, or an infected organ or part of the carcase declared unfit for human consumption.

Mycobacterium avium subsp. paratuberculosis is the aetiological agent of ruminant paratuberculosis, commonly referred to as Johne’s disease. The disease is characterised by a chronic granulomatous ileocolitis that ultimately terminates in diarrhoea, weight loss, debilitation, and death. In recent years, there has been an interest in the possible association of paratuberculosis and human Crohn’s disease. M. avium subsp. paratuberculosis may also enter the milk by faecal contamination and is more thermo-tolerant than Mycobacterium bovis and may still remain viable following pasteurisation.

1.5 Viruses

There are a number of viruses that are foodborne, or have the potential to be foodborne to humans and also be transmitted to animals. Viral infections are common causes of food poisoning in humans in developed countries. Several major economically important disease outbreaks in livestock, notably Foot and Mouth Disease and Classical Swine Fever, have occurred by feeding food waste containing meat or meat products. The UK operates strict controls over the import of meat and meat products primarily to guard against the introduction of animal diseases. A ban on swill feeding introduced in May 2001 (now included in the Animal By-Products Regulations) was also put into place following the outbreak of FMD in the UK in 2001.

Foot and Mouth Disease (FMD) is an acute infectious disease, causing fever, followed by the development of blisters, chiefly in the mouth and feet cloven-hoofed animals, in particular cattle, sheep, pigs, goats and deer, although other ruminants including deer and camelids can also be affected.

Swine Vesicular Disease, which first occurred in the UK in 1972, has identical symptoms to Foot and Mouth disease. SVD is an acute, contagious viral disease characterized by fever and vesicles with subsequent ulcers in the mouth and on the snout, feet, and teats. The pathogen is relatively resistant to heat, and can persist for a long time in salted, dried, and smoked meat products. The disease can be introduced into a pig herd by feeding food waste

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containing infected meat scraps, by bringing in infected animals, or by direct contact with infected faeces. Classical swine fever (CSF) is a highly contagious disease of pigs and wild boar. CSF is primarily spread by direct contact or by contact with fomites contaminated with virus. CSF virus can survive in meat and pig products for many months.

African swine fever (ASF) is a serious viral disease of pigs, endemic in Africa. The African swine fever virus (ASFV) is highly contagious, and can spread very rapidly in pig populations by direct or indirect contact.

In poultry several economically important diseases have the potential for foodborne transmission. Newcastle disease (ND) is a contagious disease affecting many domestic and wild avian species. Its effects are most notable in domestic poultry due to their high susceptibility and the potential for severe impacts of an epizootic on the poultry industries. It is endemic to many countries but is absent from the UK. ND is spread primarily through direct contact between healthy birds and the bodily discharges of infected birds. NDV can survive for several weeks on birds' feathers, manure, and other materials and can survive indefinitely in frozen material.

Avian influenza (avian flu or bird flu) refers to influenza caused by viruses adapted to birds. Of the greatest concern is highly pathogenic avian influenza (HPAI). All known viruses that cause influenza in birds belong to the Influenzavirus A genus. All subtypes (but not all strains of all subtypes) of influenza A virus are adapted to birds, although some subtypes are adapted to multiple hosts such that subtypes H7N7 and H5N1 are able to infect humans (Koopmans et al., 2004; Yuen et al., 1998).

The highly pathogenic influenza A virus subtype H5N1 is an emerging avian influenza virus that has been causing global concern as a potential pandemic threat. H5N1 has killed millions of poultry in a growing number of countries throughout Asia, Europe and Africa. Most human infections with avian flu are a result of either handling dead infected birds or from contact with infected fluids. Infectious H5N1 avian influenza virus has been grown from duck meat and the consumption of duck blood has resulted in the infection of humans (Tumpe et al., 2002). This has raised the question if foodborne introduction could be one of the routes by which new viral diseases can enter the human population, although to date there is no evidence that the AI viruses can be transmitted through poultry products or eggs (http://www.efsa.europa.eu/en/topics/topic/avianflu.htm).

There exists a range of endemic viruses that could potentially spread through the feeding of unprocessed food waste. These are also listed in Table 1, and associated risks are summarised in Table 2.

Rotaviruses infect a variety of animals, including cattle, pigs, sheep, horses, chickens, dogs and cats and there is evidence for zoonotic transmission (Cook et al., 2004). There are a number of various rotavirus antigenic groups (A-G) and serotypes. In calves for example, Group A rotaviruses are the most prevalent in many countries including the UK and are commonly associated with neonatal calf diarrhoea (Bezek 1994). There are few reported outbreaks of foodborne gastroenteritis due to rotaviruses, although it is likely that contamination of foodstuffs can occur.

Hepatitis E virus causes disease in humans and is widespread in Southeast Asia, northern and central Africa, India, and Central America. Reported symptomatic infection is uncommon in the UK and has generally been attributed to acquisition during foreign travel (Sadler et al. 2006), although it is likely that autochthonous infection does occur (Dalton et al., 2008). It is spread mainly through faecal contamination of water and by food. Domestic animals have been reported as a reservoir for the hepatitis E virus, with some surveys showing infection

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rates exceeding 95% among domestic pigs. Transmission after consumption of wild boar meat and uncooked deer meat has been reported. A link between human hepatitis E cases and hepatitis E virus (HEV) in pig livers, possibly through foodborne transmission of HEV has been suggested (Wichman et al., 2008). HEV has been found in pig populations and in commercial pig livers in several countries; other possible food sources include shellfish (bivalved molluscs). A recent study found HEV in pork sausages sold at retail in the UK (Berto et al., 2012). For taste and other sensory reasons, inadequately cooked pig livers are preferred by some consumers, but the heat treatment thus applied may not be sufficient to inactivate hepatitis E virus. To prevent hepatitis E, food trade and consumers need to cook food thoroughly. Thus for example, with sliced pig liver, depending on thickness and quantity, there is a need to boil at 100°C or stir-fry in hot skillet/wok for at least three to five minutes. Heating to an internal temperature of 90°C for 90 seconds is required for cooking of molluscan shellfish; hence, boil at 100°C until their shells open; boil for additional three to five minutes afterwards. In addition, food trade and consumers are also advised to observe good personal and food hygiene practices. Consumers could ask for thoroughly cooked food when eating out; this is particularly important for high risk populations such as the elderly or pregnant women.

1.6 Parasites

Many types of parasites are foodborne, and humans can become infected following the ingestion of infected or contaminated meat, fish, molluscs, vegetables, fruit, or products derived from these foods. In most cases, parasitic infections are acquired by eating raw or incompletely cooked food, or food that is or poorly preserved. Most, if not all, infections are preventable if the food is cooked sufficiently to destroy the infective stages of the parasite.

Meat from many species of animals has been a recognized source of many zoonotic helminth infections but few are likely to pose a risk from recycled food as they will have been identified and removed during meat inspection. A number of foodborne helminth infections have been reported worldwide but have not been recorded in the UK.

Tapeworm cysts (Taenia and Echinococcus species) are found on occasions and will be removed at meat inspection and as such should not have entered the food chain. Illegally imported food, especially bush meat, which has the potential to carry viable cysts, is only potentially infective to the final host (humans or carnivores) and not to livestock. The possible exception is with Trichinella, where there is a risk from imported meats or meat products, particularly pork, or other pig products such as sausages.

Whilst not occurring in the UK, there are a range of other helminth parasites that are foodborne and found throughout the world. The majority of these infections are commonly associated with cultural and eating habits and occur following the ingestion of infected or contaminated meat, fish, molluscs, vegetables, or fruit, or products derived from these foods. In most cases, parasitic infections are acquired by eating raw or incompletely cooked food, or food that is partially pickled or smoked or poorly preserved. Most, if not all, infections are preventable if the food is prepared sufficiently to destroy the infective stages of the parasite.

There are a number of foodborne protozoal infections that pose a potential risk. Infections with Cryptosporidium species are a significant cause of diarrhoea in humans and also in domesticated animals. Transmission is via a resistant oocyst stage, usually through faecal contamination of water or food, or by direct contact. In humans, foodborne transmission of cryptosporidiosis has been reported following the consumption of certain foods, notably raw sausage, offal, chicken salad, and milk. Evidence suggests that untreated milk, undercooked sausage meat, and offal have been implicated in outbreaks, but heat treatments such as those used for the pasteurization of foods are likely to destroy the oocysts. Toxoplasma gondii has worldwide distribution and differs from other coccidian protozoa in that it shows a

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complete lack of host specificity. Foodborne transmission by the ingestion of tissue cysts in raw or undercooked meat from a variety of livestock and game animals has been well documented as a major source of human infection. Adequate cooking kills the organism, and all meat should be cooked thoroughly before eating. Infections with Cyclospora cayetanensis in man can cause protracted diarrhoea with nausea, and vomiting. Food outbreaks have only been associated with eating fresh fruit.

Giardia duodenalis is a major cause of diarrheal disease. It can be zoonotic, being found in a variety of animal species, including cattle and sheep (Smith et al., 2007). Transmission is via a resistant cyst stage, and the median infectious dose is between 25 and 100 cysts (Rendtorff, 1979). It can contaminate foods via handling by infected persons, and fresh produce can be contaminated at source through irrigation with sewage-contaminated water, or contact with infected animals or their manure (Cook and Lim, 2012). Several outbreaks of giardiasis transmitted by consumption of foods including tripe, salmon and vegetables have been described (Smith et al. 2007).

1.7 Prion Diseases

Prions are proteinaceous transmissible agents that cause abnormal folding of certain brain proteins resulting in brain damage and death (Collins et al. 2004). This is in contrast to all other known infectious agents, which must contain nucleic acids (either DNA, RNA, or both). All known mammalian prion diseases (transmissible spongiform encephalopathies) are caused by the prion protein, PrP and include scrapie, bovine spongiform encephalopathy (BSE), chronic wasting disease (CWD), and Creutzfeldt-Jakob disease (CJD) in humans. (Belay and Schonberger 2005). Although BSE and CJD are not directly related, a variant of CJD, vCJD appears to be caused by the same agent as BSE. Current research suggests that the primary method of infection in animals is through ingestion and that prions may be deposited in the environment through the remains of dead animals and via urine, saliva, and manure (Gough and Maddison 2010). The UK BSE epidemic was thought to be caused by cattle being fed the remains of other cattle in the form of meat and bone meal (MBM), which caused the infectious agent to spread. The cause of BSE is thought to have been caused through the contamination of MBM from sheep with scrapie that were processed in the same slaughterhouse and probably accelerated by the recycling of infected bovine tissues prior to the recognition of BSE. A ban on feeding cattle meat and bone meal to cattle resulted in a significant reduction in cases in the UK. At the abattoir, the brain, spinal cord, trigeminal ganglia, intestines, eyes and tonsils from cows are classified as Specified Risk Material (SRM) and must be disposed of appropriately. Continuing control relies on import control, feeding regulations and surveillance measures.

1.8 Mycotoxins

Mycotoxins are toxic secondary metabolites produced by fungii or moulds that readily colonise crops. Mycotoxins can appear in the food chain as a result of fungal infection of crops, either by being eaten directly by humans or by being used as livestock feed. Mycotoxins greatly resist decomposition or being broken down in digestion, so they remain in the food chain in meat and dairy products and cooking and freezing do not destroy them.Aflatoxins are a type of mycotoxin produced by Aspergillus species. Four different types of aflatoxins are produced, which are B1, B2, G1, and G2. Aflatoxin B1, the most toxic, is a potent carcinogen and has been directly correlated to adverse health effects, such as liver cancer, in many animal species. Aflatoxins are largely associated with commodities produced in the tropics and subtropics, such as cotton, peanuts, spices, pistachios and maize.

Ochratoxins are produced by Penicillium and Aspergillus species. Aspergillus ochraceus is found as a contaminant of a wide range of commodities including beverages such as beer

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and wine. Ochratoxin A is relatively thermostable and is not destroyed by most food processes. It can also pass through the food chain and may be found in meat products, especially pork.

Citrinin is a mycotoxin originally isolated from Penicillium citrinum, but has been found to be produced by a variety of other fungi which are found or used in the production of human foods, such as grain, cheese, sake and red pigments.

Patulin is a toxin produced by a number of fungal species associated with a range of mouldy fruits and vegetables, in particular rotting apples and figs.

Fusarium toxins are produced by over 50 species of Fusarium and infect the grain of developing cereals such as wheat and maize. They include a range of mycotoxins, such as: the fumonisins, which affect the nervous systems of horses; the trichothecenes, which are strongly associated with chronic and fatal toxic effects in animals and humans. Fumonisins are relatively stable to elevated temperatures, and survive a range of cooking processes.

1.9 Heat Treatment

Heat treatment is generally lethal to microorganisms, but each species has its own particular heat tolerance. During pasteurisation for example, the rate of bacterial destruction is logarithmic, and bacteria are killed at a rate that is proportional to the number of organisms present. The process is dependent both on the temperature of exposure and the time required at this temperature to accomplish the desired rate of destruction. Thermal calculations thus involve knowledge of the concentration of microorganisms to be destroyed, the thermal resistance of the target microorganisms, and the temperature time relationship required for destruction of the target organisms. Cooking is the usual way of destroying microbes in food, although the process is neither uniform nor instantaneous. Some microorganisms are more heat-resistant and survive cooking, so as a consequence more stringent time and temperature combinations are required.

Several parameters are used in thermal calculations and define the rate of thermal lethality.

1. The Thermal Death Time (TDT) is the time needed to kill a given number of organisms at a specified temperature.

2. Thermal Death Point (TDP) is defined as the temperature needed to kill a given number of microorganisms in a fixed time – usually 10 minutes.

3. The D-value (Decimal Reduction Time) is the time required to destroy 90 % of the organisms and is a measure of the heat resistance of a microorganism. It is the time in minutes at a given temperature required to destroy 1 log cycle (90%) of the target microorganism.

4. The z-value is the number of degrees (oC or oF) required to change the D value by a factor of ten; z values thus provide information on the destruction rate at different temperatures, allowing for the calculation of equivalent thermal processes at different temperatures.

These thermal destruction parameters assume that the effects of heat on microorganisms are constant and unaffected by the heating rate in the sub-lethal temperature range. Gram-positive bacteria tend to be more heat resistant than Gram-negative bacteria; yeasts and moulds tend to be fairly heat sensitive as are parasites. Compared to bacteria, foodborne viruses are generally more resistant to heat. In addition, persistence of the viruses may be

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different in different food substrates, e.g. hepatitis A virus in bivalve molluscs needs more stringent conditions than the virus in milk for the same level of inactivation. The effects of temperature on the range of microorganisms considered in this risk assessment are shown in Table 2. Wherever possible, D-values are provided for comparison but for a number of organisms, specific heat inactivation data are not available and requires further research.

2. Disease Risk Assessment

A number of pathogenic viruses, bacteria, and parasites are foodborne, or have the potential to be transmitted via food to both livestock and humans. As part of the risk assessment, hazard identification was conducted for those pathogens that may constitute a hazard in food waste and can infect humans and livestock. The complete lists of diseases considered in the risk assessment are provided in Table 1. These represent either diseases endemic to the UK, notifiable, or exotic diseases considered to be zoonotic or of economic importance.

Meat products originating from the UK or from within the EU , which have entered the food chain and been through the appropriate inspection processes, should in theory present little additional risk if re-fed as food waste to animals unless cross-contamination with other foodstuffs or spoiling through poor storage occurs. The greatest risk is through illegally imported meats, and meat products, which could potentially cause outbreaks of exotic animal diseases.

The majority of disease agents are sensitive to temperature and are killed at the higher temperatures that occur during cooking. For many of the identified bacteria, the vegetative forms are killed rapidly at boiling point (100oC). Bacterial spores are common contaminants of food products, and may cause food spoilage or food-borne illness. They are extremely resistant to heat and other preservation treatments in comparison to vegetative cells. The inactivation of spores requires high temperatures and long heating times. Anthrax bacteria, for example, are killed at 92-100oC for 2 hours but the spores are killed at higher temperatures of 140oC for 30 minutes or at 160oC for 8 minutes.

Spores of Bacillus cereus are also heat-resistant and can survive cooking. B. cereus also produces toxins and foods contaminated with the emetic toxin produced by these bacteria need to be heated to (126oC) for more than 90 minutes to destroy the toxin.

Species of clostridia produce a range of toxins including neurotoxins (C. tetani and C. botulinum); exotoxins (C. chauvoei, C. novyi, C. haemolyticum and C. sordelli) and enterotoxins (C. perfringens, C. difficile). Spores and toxins exhibit varying degrees of heat resistance.

A study conducted by the VLA to assess the thermo-stabilities of viruses during composting indicated that parvoviruses (bovine parvovirus (BPV) and porcine parvovirus (PCV)) appear to be the most resistant to heat at 56oC, 60oC and 70oC respectively when considering a 3-log reduction and were the most appropriate markers for ensuring that this reduction can be achieved for viral hazards potentially present in Category 3 ABPs (this conclusion may also be applicable to food waste). The study looked at published decimal reduction times (DRT or D-values), for 20 viruses (adenovirus, astrovirus, avian circoviruses, avian parvovirus blue tongue virus, bovine parvovirus, bovine rotavirus, canine parvovirus, feline calicivirus, foot and mouth disease virus, Hepatitis E virus, infectious bursal disease virus, infectious pancreatic necrosis virus, other calciviruses, other circoviruses, porcine circovirus type 2, porcine parvovirus, rabbit haemorrhagic disease virus, and swine vesicular disease virus) (Defra project SE4401 2011), many of which have been included in this risk-assessment.

All parasites are destroyed by adequate cooking at temperatures >60oC and should present little risk to re-cycled food when processed correctly.

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Transmissible spongiform encephalopathies (Scrapie, BSE, CJD, v-CJD, CWD) are highly resistant to heat and chemical inactivation. In the UK, specified risk materials (SRM) from cattle and sheep do not enter the food chain and are currently disposed of by incineration. It is assumed in this risk assessment that this situation will continue and therefore there should be no additional risk to the feeding of food waste containing meat products to livestock.

Food waste has been fed to domestic animals particularly pigs and poultry, whilst historically, ruminants have been fed meat and bone meal produced from rendered carcasses. The feeding of food waste to pigs is a traditional practice that is still carried out in a number of countries. For example, in New Zealand, legislation requires that any waste containing meat is cooked (100°C for 1 hour). This was the situation in Britain, where swill feeding to pigs was controlled under the Food waste Order 1973, and the subsequent Animal By-Products Order 1999 and its amendments. However, following the outbreak of Foot and Mouth Disease in 2001, the Government prohibited the feeding of catering waste to animals that contained, or had been in contact with animal by-products. This restriction was subsequently reflected by the EU Animal By-Products Regulation and became mandatory in all Member States. Feeding catering waste to farmed livestock is currently not permitted. The Spongiform and Encephalopathy Advisory Committee (SEAC) also recommended that all intra-species recycling should be avoided to prevent the risk of a TSE being spread through recycling in animal feed. These restrictions, amongst others, are implemented under the previous (EC No 1774/2002), and the newly revised (EC No 1069/2009), Animal By-Products Regulations.

If conducted according to prescribed guidelines and stringent supervision and enforcement, then heat-treatment at 100oC for 1 hour is adequate to destroy identified endemic pathogens in the low risk category (Table 2). These organisms have been considered low risk because thermal-inactivation data indicates that a 6-log10 or greater reduction in their numbers would be obtained by this treatment.

Agents in the low to medium-risk category include those spore -forming bacteria (e.g. B. anthracis) which thermal inactivation data indicates that a 6- log10 or greater reduction in their numbers would be obtained by cooking contaminated foods at 100oC for 1 hour, but their ability to form spores confers a higher potential for heat resistance than those agents in the low risk category. Also included in this category are FMDV and SVD, which may not be inactivated if they are located within bone tissue.

Diseases in the medium to high risk category (Table 2) comprise spore -forming bacteria (e.g. C. botulinum) where insufficient information may be available to determine if cooking at 100oC for 1 hour will reduce their numbers in contaminated foods by 6 log10.

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Table 1. Potential Food waste-borne Infectious Disease Agents of Ruminants, Pigs and Poultry.

Group Family Genus Species Disease

Bacteria

Bacillaceae Bacillusanthracis Anthrax in ruminantscereus Enterotoxin -producing bacteria causing food-

poisoning

Brucellaceae Brucella

melitensis All species cause zoonotic brucellosis. B. melitensis infects goats and sheep; B. abortus which infects cattle; B. suis infects pigs and B. ovis infects sheep. All species cause abortion in their respective hosts.

abortusovissuis

Campylobacteraceae Campylobacterjejuni Main cause of foodborne gastroenteritis and

pathogen in poultryfetus Abortion in cattle and sheep

Clostridiaceae Clostridium

chauvoei Blackleg in cattle and sheepnovyi Type B causes black disease in cattle and

sheephaemolyticum (novyi D) Bacillary haemogobinuria in cattle and sheepsepticum Malignant oedema in cattle and sheep, and

braxy in sheepsordelli Gas gangrenebotulinum Botulismtetani Tetanus

Enterobacteriacae

Escherichia coli Enterotoxigenic strains (O157:H7) cause gastroenteritis, nephritis, meningitis etc. Cattle are reservoirs; contamination risks.

Salmonella enterica Many serovars. Includes subspecies Typhimurium found mainly in cattle and Enteridis in poultry, Serovar paratyphi (Paratyphoid) includes S. pullorum in poultry.

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Group Family Genus Species Disease

Bacteria

Mycobacteriaceae Mycobacterium

bovis Important cause of bovine TB and transmitted to humans through milk.

Avium Subsp. paratuberculosis

Found mostly in birds causing avian TB but occasionally also in other animals and in humansCause of Johne’s disease in cattle. Link to Crohn’s disease in humans

StaphylococcaceaeStaphylococcus

pyogenes β haemolytic group causing endocarditis in pigs

agalactiae β haemolytic group causing mastitis in cattlesuis Significant zoonosis found in pigs and other

domestic animalspneumoniae Also known as Pneumococcus an important

cause of meningitis in humans. Infects calves and cattle and a cause of mastitis.

Enterococcus durans ϒ-haemolytic group causing diarrhoea in pigs. Reservoir of vancomysin-resistance.

Listeriaceae Listeria monocytogenes Virulent foodborne pathogen and causes meningo-encephalitis in ruminants

Spirochaetaceae Brachyspira hyodysenteriae Cause of swine dysenteryVibrionaceae Vibrio cholerae Cause of cholera associated with

contaminated water. Other species associated with shellfish.

Erysipelotricidae Erysipelothrix rhusiopathiae Causes erysipelas in animals and erysipeloid in humans

Staphylococcaceae Staphylococcus aureus Range of illnesses from abscesses to pneumonia, meningitis, endocarditis, bacteraemia, and sepsis. MRSA is a zoonotic issue and has been detected in food producing animals including an NT strain in pigs.

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Group Family Genus Species Disease

Viruses

Asfaviridae Asfivirus African Swine Fever (ASF) Virus

Causes a haemorrhagic fever with high mortality rates in pigs.

Arteriviridae Arterivirus

Porcine Reproductive and Respiratory Syndrome (PRRS) Virus

Causes PPRS, a highly contagious viral disease leading to reproductive failure, respiratory tract illness in young pigs and cyanosis (blue ear pig disease).

Caliciviridae Vesivirus

Vesicular exanthema virus

Produces disease clinically indistinguishable from FMD and SVD. Thought to have arisen from feeding uncooked waste sea food to pigs.

Circoviridae

Circovirus Porcine Multisystemic Wasting Syndrome (PMWS) Virus

Porcine circovirus type 2 causing illness in piglets, loss of body condition, enlarged lymph nodes, dyspnoea, diarrhoea and jaundice.

Gyrovirus Chicken Anaemia (CA) Virus

Causes Infectious Chicken Anaemia with bone marrow atrophy and severe immunosuppression in young chicks.

Coronoviridae Coronovirus

Severe Acute Respiratory Syndrome SARS) Virus

Zoonotic disease (SARS) in humans linked to Chinese markets and bushmeat.

Transmissible Gastroenteritis (TGE) Virus

Highly infectious disease in pigs (TGE) causing vomiting and diarrhoea.

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Group Family Genus Species Disease

Viruses

Flaviviridae Pestivirus

Bovine Viral Diarrhoea (BVD) Virus

Common in cattle and a cause of respiratory disease and acute enteric disorders (BVD or Mucosal Disease)

Border Disease (BD) Virus

Congenital disorder of lambs characterized by low viability, poor conformation, tremor, and an excessively hairy birth coat

Classical Swine Fever (CSF) Virus

Highly contagious disease of pigs and wild boar causing fever, skin lesions, convulsions and death

Hepeviridae Hepevirus Hepatitis E Virus Human infection but found in pigs with reported foodborne transmission from eating uncooked wild boar meat

Herpesviridae

Varicellovirus Suid herpesvirus 1(Pseudorabies virus)

Causes Aujesky’s Disease (Pseudorabies) which may lead to abortion and high mortality in piglets

Lltovirus Gallid herpesvirus 1(Avian herpesvirus 1)

Infection causes inflammation of the trachea and larynx (Avian infectious laryngotracheitis )

OrthomyxoviridaeInfluenzavirus A

Highly Pathogenic Avian Influenza (HPAI) Virus

Avian influenza viruses adapted to birds but includes important subtypes (e.g. H7N7 and H5N1) able to infect humans

Swine Influenza Virus Swine flu leading to respiratory disease and infertility caused by various subtypes (H1N1, H1N2, H2N1, H3N1, H3N2, and H2N3)

Influenzavirus C Swine Influenza (SI) Virus

Also linked to swine flu

Paramyxoviridae

Avulavirus Newcastle Disease (ND) Virus

Several strains causing Newcastle disease, which is a highly contagious bird disease affecting many domestic and wild avian species.

Henipavirus Nipah Virus Bat virus highly contagious in pigs causing respiratory symptoms

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Group Family Genus Species Disease

Viruses

Parvoviridae Parvovirus

Porcine Parvovirus(Porcine Enterovirus)

With porcine enterovirus causes SMEDI (stillbirth, mummification, embryonic death and infertility) in pigs

Bovine Parvovirus Neonatal diarrhoea

Picorniviridae

Apthovirus Foot and Mouth Disease Virus

Foot and mouth disease (FMD) is an acute infectious disease, causing fever, followed by the development of blisters, chiefly in the mouth and feet cloven-hoofed animals, in particular cattle, sheep, pigs, goats, deer

Enterovirus

Swine Vesicular Disease Virus

Causes swine vesicular disease (SVD), which is an acute, contagious viral disease of pigs characterized by fever and vesicles with subsequent ulcers in the mouth and on the snout, feet, and teats.

Porcine Enterovirus With porcine parvovirus causes SMEDI (stillbirth, mummification, embryonic death and infertility) in pigs

Reoviridae

Orbivirus Bluetongue Virus Bluetongue disease or catarrhal fever is a non-contagious, non-zoonotic, insect-borne, viral disease of ruminants, mainly sheep and less frequently cattle, goats and other ruminants.

Rotavirus Bovine RotavirusOvine RotavirusPorcine RotavirusAvian Rotavirus

Rotaviruses infect many species of animals and humans causing diarrhoea notably in young neonates. Zoonotic transmission may occur.

Rhabdoviridae Vesiculovirus Vesicular stomatitis virus

Vector-borne, zoonotic diseases with clinical symptoms identical to FMD - vesicles in the mouth and on the coronary band.

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Group Family Genus Species Disease

Nematodes Trichinellidae Trichinella

spiralis Encapsulated clade or group of species infecting a wide range of animals including humans. Asymptomatic in animals. Human infection with T. spiralis often through ingestion of undercooked pork or game meats.

nativabritovi

Cestodes Taeniidae Taenia

saginata Generally asymptomatic human tapeworm with intermediate host cattle. Metacestodes present in meat and viscera of infected cattle.

solium Generally asymptomatic human tapeworm with intermediate host pigs. Metacestodes present in meat and viscera of infected pigs.

Protozoa

Cryptosporidiidae Cryptosporidium

parvum Diarrhoea in neonatal ruminants and pigs. Important zoonosis causing diarrhoea in humans.

hominis Human species causing diarrhoea in humans but can infect ruminants.

suis Generally asymptomaticbaileyi Respiratory disease in chickensmeleagridis Diarrhoea in turkeys

Eimeriidae Cyclospora

cayetanensisSpp.gondii

Infections can cause protracted diarrhoea, and vomiting in humans. Food outbreaks have only been associated with eating fruit or salads.

Sarcocystiidae

Sarcocystis Infection usually asymptomatic but can occasionally cause severe symptoms in infected animals and occasionally humans. Large number of species with a complex life cycle involving intermediate hosts (ruminants, pigs etc.) and final carnivore hosts (dogs, cats, humans etc)

Toxoplasma Infects all warm blooded animals; important zoonosis and cause of abortion in sheep.

Giardiidae Giardia duodenalis Affects humans causing diarrhoea; also a variety of animal species including cattle and sheep where infections are often asymptomatic

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Table 2. Disease Risks from pathogens of Ruminants, Pigs and Poultry contaminating Food waste.

Genus Species Risk* Category (H/M/L/ U)

Details References

Bacillus

anthracis L-M Bacteria are killed at 92-100oC for 2 hours and spores are killed at 140oC for 30 minutes or at 160oC for 8 minutes. Boiling at 100oC or dry heat at 150oC for 10 minutes kills spores.D-value of spores in milk (2% fat) at 80, 85, and 90oC s were 30.09, 9.30, and 3.86 min, respectivelyIn skim milk, log CFU per ml reductions for B. anthracis spores were 0.45 after 90 min at 72 oC, 0.39 after 90 min at 78 oC, and 8.10 after 60 min at 100 oC.

Whitney et al (2003)

Cruz and Montville (2008)

Novak et al. (2005)cereus L-M D-values were in the range of 3.45 min at 60o C to 10.6 min at

56oC in saline. The z-values recorded ranged from 9.3 oC in culture broth to 24o C in whole milk. The inactivation pattern for spores for the same isolates was curvilinear with D-values ranging from 4.4 min at 95oC in whole milk to 19.45 min at 85oC in saline. The z-values for spores ranged from 16.6oC in saline to 38.4o C in whole milk.In skim milk log CFU per ml were 0.39 after 90 min at 72 oC, 0.21 after 60 min at 78 oC, and 7.62 after 60 min at 100 oC.

Shivalingsarj and Mandyam (2010)

Brucella

melitensis U No details available on thermal inactivation.abortus L 63 oC for 30 mins, or 72 oC 15 secs can kill B. abortus Van de Heever et al.

(1982)ovis L No details available on thermal inactivation.suis L 62oC for 30 mins kills 6 log B. suis. Park et al. (1932)

Campylobacter jejuni L 60oC 0.8 min kills 1 log C. jejuni Nguyen et al. (2006)fetus L Inactivated by moist heat (121°C for at least 15 min)

or dry heat (160-170°C for at least 1 hour)http://www.phac-aspc.gc.ca/lab-bio/res/psds-ftss/msds29e-eng.php

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Clostridium

chauvoei U No details availablenovyi U No details availablehaemolyticum M-H Spores of 15 of 18 strains of Clostridium were inactivated by

exposure to moist heat at 90oC for 4 min with D values for linear inactivation varying from 26.6, 8.0, and 4.3 min at 70°C, 80°C, and 90°C, respectively.

Fuentes and Garcia (1980)

septicum U No details availablesordelli M-H D values for C. sordellii ATCC 9714 spores ranged between

175.60 min for D(80) (the D value for spore suspensions treated at 80oC) and 11.22 min for D(95). The thermal resistance (Z) value of spores was 12.59oC.Heat treatments at up to 85oC for 120 min failed to cause a 100-fold destruction in spore populations. By contrast, spore counts were reduced by 2 log(10) within 73 mins and 23 mins at 90oC and 95oC, respectively.

Sipos-Kozma et al. (2010)

botulinum M-H Time-temperature combinations of 90°C for 10 min, 85°C for 36 to 52 min, and 80°C for 129 to 270 mins have been suggested to reduce the number of spores of non-proteolytic C. botulinum by a factor of 106. However, in the absence of additional controlling factors such as chill storage, these heat processes have since been shown to fail in controlling growth and toxin production from 106 spores of non-proteolytic C. botulinum types B, E, and F in meat.20 minutes at 79°C or 5 min at 85°C is recommended as the minimum heat treatment for inactivation of 103 LD50 botulinum toxins per gram of the foods tested.When cooked in rice at 100c for 30 min, inactivation of 3 - 4 log10 could be observed.

Lindstrom et al. (2003)

Woodburn et al. (2006)

Konagaya et al. (2009)

tetani M-H Thermal resistance of spores revealed a biphasic inactivation at lower temperatures with D values for linear inactivation varying from 26.6, 8.0, and 4.3 min at 70 oC, 80 oC, and 90 oC, respectively.

Dixit et al. (2005)

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Escherichia coli L Heating at 60oC from 0.4 to 0.8 min can reduce E. coli O157:H7 in ground meats by 1 log.E. coli O157 was found to survive after 30 min at 55°C, but not after 60 min at 55°C.

Ahmed et al. (1995)

Sahlström et al (2008)

Salmonella enterica L A D-value of 2.20 min was reported for S. typhimurium on chicken meat at 85 oC.D-values of 293, 40.8 and 5.7 min at 50, 55 and 60 oC respectively have been calculated for the relatively heat-resistant Salmonella strain S. senftenberg 775W in liquids.

de Jong et al. (2012)

Mycobacterium

bovis L Meat from partially condemned carcasses of TB reactor cattle may be used for the preparation of meat food products, if heated to a temperature > (76oC (170°F) for >30 minutes. Bacteria are killed when heated to 63°C for 30 minutes or 72°C for 15 seconds.

www.food.gov.uk/multimedia/pdfs/board/fsa010803.pdf

aviumSubsp. paratuberculosis

L Heating at 72oC for 4.2 sec can reduce MAP by 1 log. Foddai et al. (2010)

Staphylococcus aureus L Heating at 66.5oC for 15 secs can reduce S. aureus in milk by > 6 log.

Pearce et al. (2012)

Streptococcus

pyogenes L 82oC (180oF) would provide adequate pasteurization of milk, taking an arbitrary destruction level of 15 D-values

Evans, D.A (1969)

agalactiae L After 4 min of traditional thermal pasteurization treatment in human milk resulted in an 8-log inactivation.

Viazis et al. (2008)

suis L At 60oC S. suis only survived for 10 minutes in water or broth. Clifton-Hadley and Henright (1984)

pneumoniae U No details availableEnterococcus durans L Heat resistance in enterococci is highly variable with D values

extending from 0.3 – 5.1 minutes. Two isolates of E. durans were the most heat-resistant with z-values of 8.7 and 8.8oC.

McAuley et al. (2012)

Listeria monocytogenes L Bacteria present in mussels killed after 17mins at 58oC, and 3mins at 62oC

Bremner andOsborne (1997)

Brachyspira hyodysenteriae U No informationVibrio cholerae Heat resistance of V. cholerae expressed in decimal reduction

values (D) in foods at aw 0.99 and pH = 6.5-7.0, has been reported to be 18 seconds at 72 °C

Mossel et al., (1995).

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Erysipelothrix rhusiopathiae Erysipelothrix cultures are reportedly destroyed byexposure to moist heat at 55°C for 10 min

(Timoney et al., 1988)

Asfivirus ASF Virus L Pig meat products reaching 69oC during processing are unlikely to contain residual virus

McKercher et al (1980)

Arterivirus PRRS Virus U No details availableCaliciviridae Vesivirus U No details available on thermal inactivation.Circovirus PMWS Virus L Infectivity of PCV2 was reduced by approximately 1.6 log by

pasteurization (10 hours at 60oC) and by 0.75 by dry-heat treatment (80o C for 72 hours). PCV2 was additionally almost completely resistant to dry-heat treatment up to 120oC for 30 minutes (mean log infectivity reduction 1.25), although it was more effectively inactivated when the temperature of wet-heat treatment was increased to 80oC (> 3.2 log infectivity reduction)

Welch et al. (2006)

Gyrovirus Chicken Anaemia Virus

L Infectivity of CAV was reduced by approximately 1.4 log by pasteurization (10 hours at 60oC) and by 1.25 log by dry-heat treatment (80 o C for 72 hours). CAV was additionally almost completely resistant to dry-heat treatment up to 120o C for 30 minutes (mean log infectivity reduction 0.6), although it was more effectively inactivated when the temperature of wet-heat treatment was increased to 80oC ( > 3.6 log infectivity reduction)

Welch et al. (2006)

Coronavirus

SARS Virus L Thermal inactivation at 56oC was highly effective in the absence of protein, reducing the virus titre to below detectability. If protein-containing solutions are to be inactivated, heat treatment at 60oC for at least 30 min must be used.

Rabenau et al. (2005)

TGE Virus L No details available on thermal inactivation.

Pestivirus

BVD Virus L No details available on thermal inactivation.BD Virus L No details available on thermal inactivation.Classical Swine F ever Virus

L CSFV was heat inactivated in slurry within 3 min at 60oC Turner et al. (2000)

Varicellovirus Suid herpesvirus 1 (Aujesky’s Disease)

ADV was heat inactivated in slurry within 3 min at 62oC Turner et al. (2000)

Lltovirus Gallid herpesvirus 1 L No thermal inactivation data available.

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Influenzavirus A

HPA Virus L In studies conducted on the thermal inactivation of H5N1 In thigh and breast chicken, the predicted D-values and the upper limits of their 95% prediction intervals for 57 to 61oC were 241.2 and 321.1 s, 146.8 and 195.4 s, 89.3 and 118.9 s, 54.4 and 72.4 s, and 33.1 and 44.0 s. D-values and conservative D-values predicted for higher temperatures were 0.28 and 0.50 s for 70oC; and 0.041 and 0.073 s for 73.9oC.

Thomas and Swayne (2007)

Swine Influenza Virus A

L Virus survival in farm slurry under anaerobic conditions generally ≤1h when heated to 55oC

Botner and Belsham (2011)

Influenzavirus C Swine Influenza Virus C

L No information available

Avulavirus Newcastle Disease Virus

L Linear regression models on the thermal inactivation data for two highly pathogenic, and two low pathogenic strains of AIV and ND predicted that the current USDA-temperature guidelines for cooking chicken meat to achieve a 7-log reduction of Salmonella also would effectively inactivate the AIV and NDV strains tested. Experimentally, the AIV and NDV strains used in this study were effectively inactivated in chicken meat held at 70 or 73.9oC for less than 1 s.

Thomas et al. 2008

Henipavirus Nipah Virus L 56 oC 30 min can inactivate Nipah virus. Daniels et al. (2001)

ParvovirusPorcine Parvovirus L Heat treatment at 70oC for 60 min do not completely inactivate

Porcine parvovirusSahlstrom et al (2008)

Bovine Parvovirus L At least 90oC for 20 minutes for complete inactivation in water. Rehman (1987)Apthovirus FMD Virus L-M FMDV was heat inactivated in slurry within 3 min at 67oC Turner et al. (2000)

EnterovirusSVD Virus L-M Virus suspended in milk was inactivated in two minutes at 60oC Herniman et al. (1973)Porcine Enterovirus (SMEDI)

L No thermal inactivation data available

Orbivirus Blue Tongue Virus L Vector-borne. Below Ph6 bluetongue virus was irreversibly inactivated within 1 minute at 37oC

Svehag et al (1966)

Rotavirus Bovine RotavirusOvine RotavirusPorcine RotavirusAvian Rotavirus

L Heating at 50oC for 30 minutes can result in a 2 log decrease in rotavirus infectivity.

Estes et al., (1979)

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Hepevirus Hepatitis E Virus L HEV in contaminated commercial pig livers can be effectively inactivated if cooked properly, although incubation at 56oC for 1 hour cannot inactivate the virus.

Feagins et al. (2007)

Vesiculovirus Vesicular stomatitis virus

L No thermal inactivation data available

Trichinellaspiralis L The thermal death point of T. spiralis is approximately 57oC.

The USDA requires pork to be cooked for 2 hours at 52.2°C, for 15 min at 55.6°C, and for 1 min at 60°C.

Zimmer et al. (2008)Zimmer et al. (2009)Kotula et al. (1983)

nativa Lbritovi L

Taenia saginata L Macroscopic parasites removed at meat inspection prior to entering the food chain. Risk from imported, uncooked meats. Heating to a temperature of 56°C will inactivate cysticerci. Freezing meats to -4o F for 24 hours also kills tapeworm eggs.

Allen (1947)solium L

Cryptosporidium

parvum LHeating to temperatures greater than 72.4oC for one minute, or greater than 64.2oC for two minutes of a five-minute heating cycle inactivates oocysts.

Fayer (1994); Taylor (2000)

hominis Lsuis Lbaileyi Lmeleagridis L

Cyclospora cayetanensis L Foodborne transmission linked to contaminated fresh produce - fruit and herbs. Oocysts killed by cooking.

Mansfield and Gajadhar (2004)

Sarcocystis spp. L Sarcocysts in the muscles of pigs became non-infective after heating infected pork in small pieces at 60oC for 20 min, 70oC for 15 min and 100oC for 5 min

Saleque et al. (1990)

Toxoplasma gondii L Cooking at 60oC or higher for 3½ minutes or longer renders Toxoplasma cysts non-infectious

Dubey et al. (1990); Taylor (2000)

Giardia duodenalis L The thermal death point for Giardia is 68oC (Myer and Radulescu, (1978)

H = High; M = Low, M = Medium; U = unknown

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