Zoonoses are infectious diseases that are transmissible from animals (i.e. non-humans) to man. Humans may acquire zoonotic infections through a number of routes, including food, water, direct contact and insect vectors. Transmission of certain diseases through food remains an important cause of illness in both developing and developed countries .
The recent Bovine Spongiform Encephalopathy (BSE) and Foot and Mouth Disease (FMD) crises in Europe and the Avian Influenza crisis in Asia have heightened public concerns over the safety of foods of animal origin. In some cases, the mere presence of disease in herds or flocks of food-producing animals is perceived by consumers as a risk that undermines their confidence in derived food products. However, the risks for human health associated with some of these diseases may be negligible or non-existent, as will be explained in this review.
In industrialized countries, potential risks associated with foodborne pathogens are minimised through stringent animal health control measures. Diseased animals cannot be used to produce human food. For instance, milk from cows with an udder infection cannot be sold or delivered to the dairy plant. Animals arriving at the abattoir to be slaughtered are first inspected for signs of clinical illness before they enter the premises. Throughout the slaughter process, meat inspection procedures are carried out by trained personnel to identify signs of disease in the carcass. Needless to say, any deviation from normality leads to rejection of the carcass for further use.
Some zoonotic pathogens may, however, cause little or no disease in their animal hosts and, unfortunately, these unapparent infections (carrier states) are more difficult to detect, either on farm or at slaughterhouse level. Many of these pathogens reside in the intestinal tract of healthy animals and may spread through faecal contamination of the environment and products such as meat, milk or eggs. Small amounts of intestinal contents may contaminate milk during milking, the carcass at slaughter and the egg during laying. The risk associated with this type of contamination is minimised where proper food hygiene is applied throughout the entire food chain from production, through processing to preparation at home.
This review discusses some of the main animal diseases of importance that may affect man and the risks of contracting the disease via the food chain.
Salmonellosis is the disease caused by one of the many serotypes of the bacterium, Salmonella enterica. It is one of the most common causes of bacterial foodborne illness worldwide, second only to campylobacteriosis [2,3,4]. All species, including humans, may be infected by Salmonella bacteria, which live in the intestine and may be shed in faeces. However, Salmonella can survive and multiply very well outside the intestinal tract, which makes eradication impossible. Moreover, faecal contamination of carcasses, milk and eggs cannot be completely prevented.
In animals, the disease may manifest as one or more of three major syndromes: septicaemia, acute enteritis and chronic enteritis. Some serotypes of Salmonella, such as S. Choleraesuis in pigs, S. Dublin in cattle and S. Pullorum in poultry, can cause severe disease in animals, but livestock can also be carriers without showing clinical signs of infection. The most common serotypes involved in human foodborne illness are S. Enteritidis and S. Typhimurium, but these often cause only mild, if any, disease in livestock.
In humans, salmonellosis causes fever, headache, nausea, vomiting, abdominal cramps and diarrhoea. Symptoms usually develop within 12-72 hours after ingestion, and last for 4-7 days. Most cases are self-limiting, but severe cases require hospitalisation, and may be fatal. The more severe cases are associated with septicaemia, when the organism spreads, via the blood stream, to other body sites. Particularly vulnerable groups include the elderly, infants and people with impaired immune systems. Some people may become carriers following infection and in some cases, there may be long term complications, such as reactive arthritis. ‘Typhoid fever’ is caused by S. Typhi, which only infects humans and is not spread by animals.
Food sources of animal origin include poultry and other meats, eggs and raw milk. However, infection may also be acquired from vegetables that have been irrigated with, or washed in, contaminated water. Although the organism can survive at refrigeration temperatures, it is destroyed by proper cooking and pasteurisation. Cooked foods may, however, be cross-contaminated by raw foods or other unhygienic practices.
Poultry and eggs are particularly high risk foods. Egg-associated salmonellosis is usually transmitted through faecal contamination of the shell, but S. Enteritidis may, rarely, also infect the ovaries of apparently healthy chickens and contaminate their eggs before the shells are formed.
Control measures and voluntary codes of practice for the control of Salmonella are implemented at national and European levels. Compulsory measures are currently in place through EU regulations to control S. Typhimurium and S. Enteritidis in breeding poultry flocks, and these are due to be extended to other groups of poultry and other species .
Humans that are carriers may inadvertently spread infection if they handle food without washing their hands after using the toilet. Direct contact with infected animals, including pets, can also be a source of infection. Reptiles are particularly likely to harbour Salmonella and hands should always be washed after handling pets e.g. reptiles.
Campylobacter jejuni was identified in the early 1980’s as an important enteric pathogen in humans . Prior to this, the organism was thought to be a minor animal pathogen, causing abortion and enteritis in cattle and sheep. Other Campylobacter species are occasionally involved in human disease, including Campylobacter coli. The organism is widespread in the intestines of most warm blooded animals, including cattle, sheep and poultry, and survives particularly well in birds. It rarely causes disease in livestock, although a significant number may be asymptomatic carriers.
Campylobacter is now considered the most common bacterial cause of gastroenteritis in humans throughout the world . In humans, infection causes fever, headache and general malaise, followed by abdominal pain and profuse, often bloody, diarrhoea. The incubation period is typically 3-6 days, but may be as long as 10 days, and the illness can last from two days to two weeks. In most patients, the disease is self-limiting and cases recover without specific treatment. In patients with compromised immune systems, however, infection can result in life-threatening septicaemia. Children and elderly patients may also be more severely affected. Complications occur in a small number of cases (2-10%) and include reactive arthritis or a form of paralysis known as ‘Guillain-Barré Syndrome’. These complications usually resolve within a few months.
Transmission of Campylobacter to humans can occur via contaminated raw or undercooked poultry and meat, unpasteurised milk and untreated water. The organism is particularly common on poultry carcasses, and poultry meat is thought to be an important vehicle for infection. Contact with infected pets can also be a source of infection.
Relatively small number of bacteria are required to cause illness in humans, which can result from a single drop of juice from raw chicken meat . The bacteria are readily destroyed on cooking and during the pasteurisation process and freezing reduces the numbers on food. The organism does not readily grow in foods and, moreover, needs ‘warmer’ temperatures for multiplication. Hygiene in food storage and preparation is important for preventing disease, as is thorough cooking of poultry products and pasteurisation of milk, in particular.
Listeriosis is the disease caused by the bacterium Listeria monocytogenes, although other species of Listeria may very rarely be involved. The organism is ubiquitous in the environment and is found throughout the world.
In healthy adult humans, infection does not result in significant disease, but severe illness may occur in the unborn child, infants, the elderly and people with compromised immune systems. The incubation period is variable from 3-21 days depending on the clinical form. Symptoms range from a mild flu-like condition to severe, life-threatening disease characterised by meningitis and septicaemia. Pregnant women are about 20 times more likely than other healthy adults to become infected, with about one third of Listeria cases occurring in pregnant women . Although their own symptoms may be mild, infections can lead to miscarriages, stillbirths, premature delivery or infection of the newborn child.
Of the farm animals, cattle, sheep, goats and, rarely, pigs, are the most commonly affected. In these species, infection causes encephalitis, septicaemia, abortion and kerato-conjunctivitis. L. monocytogenes can also found in healthy animals. In most cases, listeriosis is foodborne but transmission to humans can occasionally occur through direct contact with infected animals.
Because Listeria is widespread in the environment, even in households, it may be transferred to food from a variety of sources. L. monocytogenes is destroyed by cooking and pasteurisation, but contamination of prepared foods can occur after processing and before packaging. Unlike some other foodborne pathogens, the organism grows at low temperatures, and can often be found in refrigerators. Typically, listeriosis in humans is associated with consumption of prepared, ready-to-eat foods that have an extended shelf life and are stored in chilled environment. Soft cheeses, meat pâtés and other delicatessen meat products, in particular, have been sources of infection and should be avoided by pregnant women and other at-risk individuals.
Tuberculosis (TB) is a serious disease of humans and many animals (including birds) that is caused by different species of Mycobacterium. Most cases of human TB are caused by Mycobacterium tuberculosis, which primarily affects humans. The disease in cattle is caused by M. bovis, but this organism can also affect other species, including humans. Birds may be affected by M. avium, which can also infect mammalian species. M. avium does not normally cause disease in humans unless the individual is immunocompromised, as in Acquired Immunodeficiency Syndrome (AIDS).
The disease is characterised by the formation of caseous ‘tubercles’ in various organs of the body. In humans, TB most commonly affects the lungs (pulmonary TB) causing chronic coughing, spitting of blood, fever, nights sweats and weight loss. In some cases, infection may spread to other organs, including the central nervous system, lymph nodes, bones and joints. Many individuals may be infected without showing signs of disease, but the infection lies dormant and may be activated in later years when the immune system is weakened.
Similarly, in cattle, TB usually affects the lungs but may also spread to other organs, including the udder. In the early stages of disease, affected animals may not show signs of clinical disease.
Transmission of the organism is via exhaled air and in excretions and secretions. Today, the main source of TB in humans is other humans infected with M. tuberculosis . During the 1930’s, however, many cattle were infected with M. bovis, and this was a significant cause of TB in humans. The organism spread readily to humans via raw milk, although direct contact with infected animals and person-to-person contact have also been implicated.
The incidence of human M. bovis infections dropped markedly with the introduction of milk pasteurisation and compulsory eradication programmes in cattle. In many European countries these measures have, for 30 years or more, prevented many cases of TB. In the UK, for example, less than 1% of all confirmed tuberculosis cases are due to M. bovis . However, these can usually be attributed to infections acquired abroad, or to reactivation of dormant infections in elderly people who were probably infected before the mandatory pasteurisation of market milk .
The organism is destroyed by heat and there is no risk from pasteurised milk. The risk of contracting bovine TB from meat is extremely small, particularly as the organism is killed readily on cooking, and no cases have ever been recorded.
To control TB in cattle, a system of testing and routine meat inspection is undertaken according to EU legislation [8,9]. Infected animals are slaughtered and cattle may not be moved from farms where TB is diagnosed. Austria, Denmark, Germany, Luxembourg, Finland, the Netherlands, Norway and Sweden are currently designated by the EU as being officially free of bovine TB .
Brucellosis is an infectious disease caused by the various species of the bacterium Brucella. The organism affects cattle, sheep, goats, deer, elk, pigs, dogs and many other species, including humans. Brucella organisms persist within the host’s own cells, where they are protected from the animal’s immune response and can give rise to chronic, recurrent infections.
In animals, brucellosis is primarily a disease of the reproductive tract, causing abortion, retained placenta and impaired fertility. Brucella abortus causes brucellosis in cattle (‘Bang’s Disease’, contagious abortion, infectious abortion) although it may also infect other species including humans. B. melitensis causes brucellosis primarily in sheep and goats.
In humans, B. abortus causes ‘undulant fever’ whereas B. melitensis causes the slightly more severe ‘Malta fever’. Symptoms of acute brucellosis are flu-like, including fever, sweats, headache, back pains and physical weakness. Infections usually become chronic, causing recurrent fever, fatigue and joint pain.
Humans may be infected through eating contaminated food or drink or through close contact with an infected animal when the organism may be inhaled or acquired via skin wounds. Most cases occur following consumption of contaminated raw milk or dairy products.
Areas of Europe that are currently listed as high risk for brucellosis include the ‘Mediterranean Basin’ (Portugal, Spain, Southern France, Italy, Greece, Turkey, North Africa) and Eastern Europe [12,13]. It also occurs in South and Central America, the Caribbean, Africa, Asia and the Middle East. Consumption of ‘village cheeses’ in these areas may pose a risk.
EU legislation provides for continued monitoring of areas designated officially free of B. melitensis through annual testing, and places restrictions on sheep and goats that are moved into the area. Currently, officially free regions include the UK, Ireland, Germany, Belgium, Luxembourg, Netherlands, Sweden, Denmark, Finland and parts of France, Italy, Spain and Portugal .
Control measures for B. abortus in cattle include eradication schemes in a number of European countries. The UK, for example, is currently brucellosis-free and operates a national surveillance scheme in which bulk milk samples from dairy herds are tested monthly and blood samples from other breeding cattle are tested every two years. In addition, all cases of abortion or premature birth in cattle are tested for brucellosis and checks are carried out on all imported females after they calve for the first time in the UK.
Pathogenic E. coli
Escherichia coli is a common bacterium that is found as part of the normal flora in the intestines of all warm-blooded animals, including humans. There are many strains of E. coli, and most do not cause disease. However, some strains can result in serious illness in both man and animals. The presence of high numbers of E. coli in raw food or water may be a sign of faecal contamination by humans or animals, but does not cause illness in most cases. E. coli multiplies readily wherever the temperature, humidity and nutrients are favourable.
Pathogenic strains cause gastroenteritis or more serious forms of disease, and are generally grouped according to their mechanism of virulence. Of the five groups, enterotoxigenic strains of E. coli (ETEC) are the major cause of bacterial diarrhoea in developing countries and of ‘traveller’s diarrhoea’ in developed countries . These organisms cause disease by producing toxins that stimulate the lining of the intestines to secrete fluid, resulting in profuse, watery diarrhoea. Most cases recover with fluids alone, particularly oral rehydration solutions, although a number may require antibiotic treatment.
Enterohaemorragic E. coli (EHEC) is a highly pathogenic group of E. coli that has emerged in recent years. The most widely recognised serotype is E. coli O157:H7. This serotype causes symptoms that range from mild diarrhoea to severe abdominal cramps and bloody diarrhoea (haemorrhagic colitis). In some cases, infection can lead to more serious complications including haemolytic uraemic syndrome (HUS) in which the rapid destruction of red blood cells (causing anaemia and spontaneous bleeding) results in kidney failure and, occasionally, neurological signs. Young children and the elderly are the most vulnerable groups and in these patients, infection has proved fatal in a small percentage of cases.
Enterohaemorrhagic E. coli are usually transmitted by contaminated, undercooked minced (ground) beef, but other foods such as sprouts, lettuce and apple juice have also been vectors . Large outbreaks have been caused by contaminated water. If a carcass is contaminated, the organism can be thoroughly mixed in when the meat is minced (ground), resulting in the contamination of a large quantity of meat. Indeed, E. coli O157:H7 was first identified in the USA following an outbreak caused by eating contaminated hamburgers from a fast food outlet . Raw milk has also been a source of infection, resulting from contamination of the milk by faecal material on the udder or on milking equipment. Transmission can also occur through direct contact with infected people or animal carriers, or through contact with contaminated land. It should be reiterated that the animals that carry and excrete EHEC are asymptomatic and are thus not identified on farm or during meat inspection.
The number of organisms required to cause disease is thought to be relatively small . Thorough cooking is required to kill the organism, and minced beef should not be eaten if it is still pink. Beef burgers, for example should be cooked to a minimum internal temperature of 70ºC for two minutes.
Foodborne yersiniosis is usually caused by the bacterium Yersinia enterocolitica, although Yersinia pseudotuberculosis may occasionally be involved . The organism occurs in the digestive tract of animals and in the environment, but not all strains are harmful. Strains of Y. enterocolitica that are most likely to cause illness in humans are found most commonly in pigs but have also been isolated from cattle, sheep and poultry. Although Y. enterocolitica can cause enteritis in piglets and lambs, most infections in animals are clinically silent.
Yersiniosis in humans is most common in young children and is characterised by acute diarrhoea, fever, abdominal pain and vomiting. In older children and adults the disease can mimic appendicitis, with fever and right-sided abdominal pain being the predominant signs. Rarely, infection can lead to complications including reactive arthritis or a skin condition called erythema nodosum, but most cases are self-limiting.
Most cases of yersiniosis occur after eating or handling contaminated meat, particularly raw or undercooked pork products. Unpasteurised milk or untreated water that is contaminated can also pose a risk. Children may be infected through cross contamination of their toys, bottles or pacifiers by carers after handling contaminated food. Prevention is dependent on scrupulous hygiene measures in food preparation and storage, and avoiding consumption of raw meat, unpasteurised milk or untreated water.
Anthrax has been recognised as an infectious disease of people and animals for centuries. In nineteenth century Europe, 20-30% of sheep and cattle died of anthrax each year. Today, anthrax still exists in most countries of sub-Sahelian Africa and Asia, South and Central America, the Caribbean, some Southern and Eastern European countries and the Middle East . In other countries, the disease may occur sporadically.
The anthrax organism is a spore-forming bacterium, Bacillus anthracis. Spores form when the organism is exposed to air and, being very resistant, they can survive for decades in soil. Animals are infected when they are exposed to spores by inhalation, ingestion or via the skin.
Anthrax can affect most species, including humans, but is most commonly seen in cattle and sheep, sometimes, pigs. In cattle and sheep, the disease is usually rapidly fatal and affected animals may be found dead without prior clinical signs. The course of the disease tends to be slightly longer in pigs and horses, which may show swelling of the head and neck, although the disease is usually fatal. Where anthrax is suspected, the carcass is not opened, to prevent the anthrax bacilli forming spores on exposure to air. In cattle, anthrax is always considered a possible cause of unexplained sudden death and a blood smear is always carried out to investigate that possibility. Affected carcasses must be disposed of in an approved manner, usually by incineration.
In humans, there are three forms of the disease: • Cutaneous anthrax when the spore enters the skin via a cut or abrasion. This is the most common form, accounting for 95% of human cases worldwide. Skin infections start as a raised itchy lump and develop into blisters then ulcers with a characteristic black centre. • Pulmonary or inhalation anthrax acquired from breathing in spores. Symptoms are initially flu-like, but progress to severe breathing difficulties and shock after 2-6 days. • Gastrointestinal anthrax when spores are consumed in contaminated food, usually undercooked meat from an infected animal. This form of anthrax is extremely rare but, when it occurs, results in severe acute gastroenteritis.
Cutaneous anthrax is milder than the other two forms of disease and can be treated effectively with antibiotics. If untreated, however, the disease can be fatal in approximately 20% of cases. Although inhalation and intestinal anthrax are often fatal, recovery is possible if antibiotic treatment is initiated prior to or immediately after the onset of symptoms. An effective vaccine is available for both humans and animals in at-risk areas.
Humans usually contract anthrax through occupational exposure to the tissues or products, such as skins or wool, of infected animals. In Europe and North America, cases of human anthrax are rare and usually result from contact with imported animal products from countries where the disease is endemic .
Foot and Mouth Disease Foot and Mouth Disease (FMD) is caused by a virus and is one of the most contagious diseases of animals. It affects mainly cloven-hoofed animals, particularly cattle, sheep, goats, pigs and deer, although other animals including elephants, hedgehogs and rats are also susceptible. Foot and Mouth Disease is endemic in parts of Asia, Africa, the Middle East and South America . In disease-free areas, sporadic outbreaks may occur.
The disease causes the formation of vesicles (blisters), mainly in the mouth and on the feet. Vesicles subsequently rupture leaving painful erosions. The disease is rarely fatal, although it can cause sudden death in very young animals. After infection, there may be a drop in milk yield, which can be permanent and chronic lameness. Economic losses as a result of the disease can be very severe, so disease-free areas employ stringent precautions to prevent import of the virus, and measures to eradicate the disease if it occurs.
Although humans can be affected by FMD, this is extremely rare . When it occurs, the disease in humans is relatively benign. During the large outbreak in the UK in 2001, there were no confirmed cases of transmission of FMD from animals to humans [22,23]. Less than 40 cases of FMD in humans have been confirmed worldwide throughout the last century . Although it is not entirely clear how transmission occurred, these cases are believed to have had close contact with infected animals or to have consumed raw milk. No cases of infection from pasteurised milk or from consuming meat from infected animals have been reported. It is generally agreed that FMD has no implications for the human food chain .
Avian influenza is an infectious, viral disease that causes respiratory, digestive and/or neurological disease in many species of birds. Some species, such as migratory wildfowl, can be asymptomatic carriers, and may represent a natural reservoir of virus .
Avian influenza is caused by Type A strains of the influenza virus. There are a number of different subtypes of influenza that affect birds, some of which cause relatively mild disease whilst others cause a highly contagious, rapidly fatal form of the disease, resulting in severe epidemics. The latter form of the disease is referred to as ‘highly pathogenic avian influenza’ (HPAI), with a mortality rate that can approach 100%. Domestic poultry, including chickens, turkeys, guinea fowl, occasionally ducks and geese, are particularly susceptible to epidemics of rapidly fatal influenza.
Avian influenza viruses normally only infect birds, but can also infect pigs and other mammals. The first documented cases of avian influenza infecting humans occurred in Hong Kong in 1997 . The HPAI strain (H5N1) that was involved caused severe respiratory disease, resulting in six human fatalities. Further spread of the virus was prevented through the rapid destruction of Hong Kong’s entire poultry population. Subsequently, outbreaks in flocks the Netherlands and Hong Kong, involving other avian influenza viruses caused relatively mild disease in humans, although one fatality occurred in the Netherlands. In 2004, cases involving H5N1 strain occurred in humans in Viet Nam and Thailand with more severe consequences and, since then, cases have also been confirmed in Cambodia, Indonesia, China and Turkey .
Although trade restrictions have been imposed on some countries to protect animal health, there is no epidemiological evidence that avian influenza can be transmitted to humans via properly cooked food [25,26,27]. The WHO and other expert bodies, therefore, do not currently consider avian influenza a food safety risk for consumers. Humans have acquired avian influenza infections through close contact with live poultry, not through eating poultry meat.
Infected birds generally die or are slaughtered before they can enter the food chain and any remaining potential risk is reduced to insignificant levels when the meat is processed. Although HPAI virus strains can survive for long periods of time at low temperatures, they are inactivated at temperatures above 70ºC. Poultry meat and eggs that are properly cooked do not pose a risk to consumers.
Trichinellosis, or trichinosis, is a parasitic disease of mammals caused by a nematode worm (roundworm) of the Trichinella genus, mainly Trichinella spiralis. The worm gains entry to the body when larval cysts are eaten in infected muscle meat. Gastric juices break down the tough cysts and release infective larvae, which then invade the small intestinal lining and mature to adults. Adult female worms subsequently release larvae that penetrate the intestinal wall and are distributed throughout the body via blood and lymphatic vessels. Only in skeletal muscles, they form cysts, which can remain viable for several years. The life cycle is perpetuated when the infected muscle is eaten by another host.
Although all mammals are probably susceptible, infection is usually confined to carnivorous species, mainly pigs, dogs, cats, carnivorous game, rodents and humans. Horses may occasionally be infected after eating fodder contaminated by decaying rodents. Most infections in domestic and wild animals go undiagnosed, but heavy infestations can give similar signs to those seen in humans.
In humans, trichinellosis is very variable in the symptoms it causes. Light infections may go unnoticed, whilst heavy infestations can cause severe symptoms and may, occasionally, be fatal. The intestinal phase of infection may be associated with diarrhoea and abdominal pain, whilst the period of larval migration may be associated with fever, sweating, chills, muscle pain, weakness, fatigue and swelling and pain around the eyes. Symptoms are directly or indirectly associated with the damage caused by the larvae penetrating the tissues. Symptoms gradually subside but, occasionally, complications develop when heart, brain or lungs are involved. Rarely, death may result from heart failure.
Human infections are traditionally associated with eating raw or undercooked pork (such as ham or sausage) or wild carnivorous game (including wild boar, bear and seal). However, recent outbreaks in Europe have been linked to eating undercooked horse meat . Current EU regulations dictate that all pig, horse and wild boar meat intended for Community trade must be inspected for the presence of Trichinella according to EU standards. There is no evidence to suggest that Trichinella is currently present in UK pigs or horses, and a recent survey found no evidence of infection in the UK fox population .
Taeniasis is a parasitic disease of humans caused by the tapeworms Taenia saginata (from cattle) or Taenia solium (from pigs). The adult tapeworms are found only in humans, where they attach to the wall of the small intestine and can grow to several metres in length. Egg-containing segments, which are independently motile, are shed by the tapeworm and passed in faeces or migrate through the anus. Infection is usually asymptomatic, but may be associated with diarrhoea, flatulence, abdominal discomfort and weight loss.
For both tapeworms, the intermediate host is infected when they eat material contaminated by infected human sewage. For T. saginata, the intermediate host is cattle, whereas both pigs and humans can act as intermediate hosts for T. solium. Ingested eggs hatch in the intestine and migrate to other tissues where they form small larva-containing vesicles (cysticerci), which may survive for several years. T. saginata cysticerci form only in muscle tissue whereas T. solium cysticerci can form in muscle, liver, lung, brain and other tissues. The condition in which cysticerci are present in muscle or other organs is known as ‘cysticercosis’.
In cattle and pigs, infected individuals may show no obvious clinical signs unless the infestation is severe. In humans with cysticercosis, however, symptoms may be moderate to severe depending on the number and location of the cysticerci. Where cysticerci are present in muscles, patients are frequently asymptomatic although heavy infestations can cause muscle inflammation with swelling and weakness. Severe involvement of heart muscle can lead to heart failure whilst the presence of cysticerci in the brain (neurocysticercosis) can cause seizures and other neurological signs.
EU regulations dictate that carcasses are inspected routinely for the presence of cysticerci . However, light infections may not be detected. Taeniasis (adult tapeworm infection) in humans may thus occur by eating undercooked beef or pig meat that contains viable cysticerci. Tapeworm carriers are the source of infection for human cysticercosis, when poor hygiene measures allow contamination of food, water and other surfaces with T. solium eggs.
Bovine Spongiform Encephalopathy Bovine Spongiform Encephalopathy (BSE) is a transmissible brain disease of cattle, which was first recognised in November 1986 in the UK . In this country, the number of cases grew considerably over the next few years but, following the introduction of protective measures, has been declining steadily since the epidemic peaked in 1993. Since 1989, cases have also been reported in native cattle in a range of other European countries, with most of these occurring in France, Germany, Ireland, Portugal, Spain and Switzerland.
BSE is one of a group of neurological disorders known as Transmissible Spongiform Encephalopathies (TSE), which affect a variety of animal species and humans. These include scrapie in sheep and goats, and Creutzfeldt-Jakob disease in humans. The TSEs are characterised by degeneration of the central nervous system, giving the brain a spongy appearance on microscopic examination. This results in the development of severe neurological signs and is invariably fatal.
In cattle, BSE has a long incubation period of four to five years but death occurs within weeks to months of the onset of clinical signs. The neurological signs associated with BSE include incoordination and behavioural abnormalities, which give rise to its colloquial name, ‘Mad Cow Disease’.
The causal agent of BSE and other TSEs is still a matter of scientific debate, although the weight of evidence points to a protein, named ‘prion’, rather than a microorganism, such as bacteria or viruses [30,31]. The prion theory hypothesises that the agent responsible for BSE and other TSEs is a ‘misfolded’ form of a normal host prion protein, which is found mainly on brain cell membranes. The abnormal prion accumulates in the brain by transforming normal prion proteins adjacent to it, and forms amyloid-like deposits, which are insoluble and eventually cause neuronal death and astrogliosis.
Transmission of the acquired form of the disease usually occurs by ingestion of infective material. The main vector of BSE in cattle is meat and bone meal (MBM) which, at the time BSE was first recognised, was commonly fed to cattle as a recycled protein source. This animal feed may have become contaminated through the incorporation of carcasses of TSE-affected animals, such as sheep with scrapie or cattle with BSE. It is thought that changes in the rendering process used to manufacture MBM, particularly changes in the temperature and pressure applied, may have favoured the survival of the infectious agent in the feed . Although the original source of BSE is still not clear, its rapid spread was almost certainly due to the feeding of contaminated MBM to other cattle.
Creutzfeldt-Jakob Disease (CJD) is one of a number of TSEs that affect humans. This is a rare and fatal condition that occurs sporadically in middle aged and older individuals, causing dementia and progressively severe neurological signs. In 1996, a new form of CJD, called variant CJD (vCJD), was described in the UK . This form differed from classic CJD as it affected younger patients and had a longer duration of illness. It has been shown that vCJD was probably linked to potential dietary exposure to beef products contaminated with infected tissues. More recently, it has been shown that the prion protein that accumulates in the brain of patients with vCJD is similar to that found in cattle with BSE.
A range of protective measures have been introduced throughout the EU, and are under constant review, to minimise the risk of BSE spreading amongst cattle and of infective material entering the human food chain. Suspected cases of BSE are slaughtered and their carcasses incinerated. In the UK, a ban on feeding MBM to ruminants was introduced in 1988 and led to a drastic reduction in the incidence of BSE in cattle [32,33]. Current EU regulations prohibit the feeding of any mammalian protein (MBM and, for example, bloodmeal) to ruminants and the feeding of mammalian MBM to all other farm livestock.
The active surveillance of TSEs consists of the removal, at slaughter, of all specified risk materials (SRM) from cattle, sheep and goat carcasses of animals older than one year. SRMs include brain, spinal cord, eyes. The whole intestine in cattle, and the spleen in sheep are removed from all animals regardless of their age. EU regulations also now prohibit the use of mechanically recovered meat from ruminant bones.
In the UK, the risk to consumers has been further reduced by the Over Thirty Month (OTM) rule, in which cattle over thirty months are not permitted to enter the human food chain. No clinical cases have occurred in the UK in cattle under thirty months, and animals below this age are unlikely to contain significant BSE infectivity. This rule is not applicable in other EU countries, where older animals may enter the food chain if a post-mortem test for BSE proves negative.
In January 2006, however, the UK government introduced a replacement of the OTM rule with a system of robust testing for OTM cattle born after July 1996 . This change acknowledges the reduced, very low risk to UK consumers that has been achieved and the effectiveness of other control measures, which will remain in place. The new scheme, known as the Older Cattle Disposal Scheme (OCDS), will bring the UK in line with other EU countries.
Prevention of foodborne infections requires an integrated (‘Farm to Fork’) approach to food production. This involves measures aimed at eradication of zoonotic diseases within the animal population and prevention of contamination at all stages of the food supply chain.
In developed countries, governments have established food safety and sanitary regulations to control zoonoses, which are under continual reassessment. The EU food safety strategy, for example, provides extensive legislation and outlines the responsibilities of both producers and suppliers in ensuring the safety of the food supply . Specific control measures for a number of zoonotic pathogens are discussed in the relevant sections of this review.
EU regulations are amongst the most stringent in the world and cover: • The rejection of animal feed materials that could pose a risk to animal and human health. • Monitoring of disease within the resident animal population and implementation of eradication and control strategies. • Health requirements for animals and animal products imported into or traded within the EU. • Identification and traceability of individual animals. • Animal welfare standards. • Food hygiene standards at critical points throughout the food production process.
The Food and Veterinary Office (FVO), an arm of the European Commission, plays an important role in verifying whether EU food safety regulations are being enforced . A team of about 80 FVO inspectors carry out spot checks at the premises of producers, slaughterhouses or processing plants, both within and outside the EU, to ensure that adequate control and enforcement mechanisms are in place and are effective in practice.
Food safety has a high priority within the food chain, but consumers must also share the responsibility for ensuring food safety within the home because contamination of certain foods cannot be prevented. A few simple procedures should be employed to minimise the risk of foodborne disease, and these may be summarised in accordance with the WHO’s ‘Five Keys to Safer Food’ strategy :
- Wash and dry hands before preparing any food and after handling raw foods, especially raw meat or poultry.
- Ensure that food preparation areas and equipment are clean.
- Ensure that hands are washed after going to the toilet.
- Protect kitchen areas and food from insects, pests and other animals.
- People with gastrointestinal illness, such as vomiting or diarrhoea, should not handle food intended for consumption by others.
Why? – While most microorganisms do not cause disease, dangerous microorganisms are found in soil, water, animals and people. These microorganisms are carried on hands, wiping cloths and utensils, especially chopping boards. The slightest contact can transfer them to food and cause foodborne disease. Examples of zoonotic pathogens that may be transmitted in this way include Salmonella, Campylobacter, EHEC and eggs of the tapeworm, Taenia solium.
Separate raw and cooked food
- Store raw foods (especially meat, poultry and seafood) separately from ready to eat foods to prevent cross contamination.
- Store raw meat and poultry in sealable containers, preferably at the bottom of the fridge, to prevent juices dripping onto ready-to-eat foods.
- Use different knives and chopping boards for preparing raw and ready-to-eat foods.
Why? – Raw food, especially meat, poultry and seafood, and their juices, can contain dangerous microorganisms, such as Salmonella, Campylobacter, Listeria and EHEC, which may be transferred onto other foods during food preparation and storage.
- Ensure that food is cooked thoroughly to the correct temperature.
- Poultry, minced meat products (eg hamburgers and sausages) and rolled joints, in particular, should not be served pink. Ideally, the centre of the food should reach a temperature of 70ºC for at least two minutes.
- Eggs should be cooked until the yolk is firm.
- Soups and stews should be brought to the boil.
- Reheated food should be piping hot before serving and only reheated once.
Why? – Proper cooking kills almost all dangerous microorganisms. Studies have shown that cooking food to a temperature of 70ºC can help ensure that it is safe for consumption. Foods that require special attention include minced meats, rolled roasts, large joints of meat and whole poultry. Although the BSE causative agent is resistant to normal cooking, all other pathogens discussed in this review are destroyed or inactivated at temperatures above 70ºC.
Keep food at safe temperatures
- Store perishable foods at the correct temperature.
- Chilled, ready to eat foods must be kept at temperatures below 5ºC (41ºF).
- Hot foods must be kept at temperatures above 60ºC (140ºF) before serving.
- Cool rapidly and refrigerate leftover foods if they are not to be used within 2 hours.
- Food should be cold before placing in the refrigerator, since it may take a while to cool off in the refrigerator and hot food may warm up other foods.
- Do not thaw frozen food at room temperature.
Why? – Microorganisms can multiply very quickly if food is stored at room temperature. By holding at temperatures below 5ºC or above 60ºC, the growth of microorganisms is always slowed down and in most cases stopped, notable exceptions include Listeria, which can still grow at temperatures below 5ºC albeit slowly.
Use safe water and raw materials
- Use safe drinking water to wash and prepare food and make ice.
- Select fresh and wholesome foods.
- Avoid consuming raw meat and unpasteurised milk.
- Wash fruits and vegetables, especially if eaten raw.
- Use produce before the ‘Use by’ or ‘Best before’ date on the packaging.
Why? – Raw materials, including water and ice, may be contaminated with dangerous microorganisms. Toxic chemicals may be formed in damaged and mouldy foods. Care in selection of raw materials and simple measures, such as washing and peeling, may reduce the risk. Contaminated water, for example, has been associated with outbreaks of Salmonella, Campylobacter and EHEC, whilst infections with Salmonella, Campylobacter, Mycobacteria (TB), Brucella and EHEC can be acquired through the consumption of contaminated milk or dairy products that are not pasteurised.
- WHO (updated 2002) Food Safety and Foodborne Illness. Fact sheet 237.
- Allos BM (2002) Campylobacter jejuni Infections: update on emerging issues and trends. Clinical Infectious Diseases 32: 1201-1206
- WHO (updated 2005) Drug-resistant Salmonella. Fact sheet 139.
- WHO (2000) Campylobacter. Fact sheet 255.
- European Commission (29 Sept 2003) Press release IP/03/1306
- CDC (2005) Campylobacter infections.
- CDC (2005) Listeriosis.
- Defra (updated 2005) Bovine TB; What is bovine tuberculosis?
- DEFRA (updated 2005) Bovine TB: Protecting public health from bovine TB (bTB)
- Health Protection Agency (updated 2005) Tuberculosis – Mycobacterium bovis
- Food Safety Authority of Ireland (2005) Report on Zoonoses in Ireland 2002 & 2003
- DEFRA (updated 2005) Disease fact sheet: Brucellosis (Brucella melitensis)
- CDC (updated 2005) Brucellosis (Brucella melitensis, abortus, suis and canis)
- CDC (updated 2005) Enterotoxigenic Escherichia coli (ETEC)
- WHO (updated 2005) Enterohaemorrhagic Escherichia coli (EHEC). Fact sheet 125
- DEFRA (2005) Zoonoses Report UK 2004 PB 10814
- CDC (updated 2005) Escherichia coli O157:H7
- CDC (2005) Yersinia enterocolitica.
- WHO (2001) Anthrax. Fact sheet 264.
- Health Protection Agency (updated 2005) General Information – Anthrax.
- DEFRA (updated 2005) Disease factsheet: Foot-and-mouth disease (FMD)
- DEFRA (2003) Zoonoses Report UK 2001 PB 7995
- DEFRA (2004) Zoonoses Report UK 2002 PB 9248
- WHO (updated 2006) Avian influenza (“bird flu”) – Fact sheet.
- WHO (updated 2005) Avian Influenza: Food safety issues.
- International Food Safety Authorities Network (INFOSAN) Information Note 7/2005 (Rev 1.5 Dec) – Avian Influenza (4 November 2005)
- European Food Safety Authority (EFSA) Press Release (26 Oct 2005). EFSA provides update on avian influenza and food safety.
- EUROPA European Commission (2001) Opinion on Trichinellosis, epidemiology, methods of detection and Trichinella - free pig production
- EUROPA European Commission (2000) Opinion on The control of taeniosis/cysticercosis in man and animals.
- WHO (updated 2002) Bovine spongiform encephalopathy. Fact sheet 113.
- DEFRA (updated 2005) BSE: Science and research – Pathogenesis.
- DEFRA (updated 2004) BSE: Disease control and eradication – Causes of BSE.
- WHO (updated 2002) Variant Ceutzfeld-Jakob Disease. Fact sheet 180.
- DEFRA (updated 2005) BSE: Over Thirty Month (OTM) cattle.
- EUROPA (updated 2005) Overviews of the European Union Activities – Food Safety.
- EUROPA (updated 2006) European Commission – Food and Veterinary Office
- WHO (2004) Five Keys to Safer Food.