Foot-and-mouth disease

Not to be confused with hand, foot and mouth disease.
Foot-and-mouth disease
Ruptured oral blister in diseased cow.
Classification and external resources
Specialty infectious disease
ICD-10 B08.8 (ILDS B08.820)
ICD-9-CM 078.4
DiseasesDB 31707
MeSH D005536

Foot-and-mouth disease or hoof-and-mouth disease (Aphthae epizooticae) is an infectious and sometimes fatal viral disease that affects cloven-hoofed animals, including domestic and wild bovids.[1][2] The virus causes a high fever for approximately two to six days, followed by blisters inside the mouth and on the feet that may rupture and cause lameness.

Foot-and-mouth disease (FMD) has severe implications for animal farming, since it is highly infectious and can be spread by infected animals through aerosols, through contact with contaminated farming equipment, vehicles, clothing, or feed, and by domestic and wild predators.[3] Its containment demands considerable efforts in vaccination, strict monitoring, trade restrictions, and quarantines, and occasionally the killing of animals.

Susceptible animals include cattle, water buffalo, sheep, goats, pigs,[4][5] antelope, deer, and bison. It has also been known to infect hedgehogs and elephants;[3][6] llamas and alpacas may develop mild symptoms, but are resistant to the disease and do not pass it on to others of the same species.[3] In laboratory experiments, mice, rats, and chickens have been successfully infected by artificial means, but they are not believed to contract the disease under natural conditions.[3] Humans are very rarely infected.

The virus responsible for the disease is a picornavirus, the prototypic member of the genus Aphthovirus. Infection occurs when the virus particle is taken into a cell of the host. The cell is then forced to manufacture thousands of copies of the virus, and eventually bursts, releasing the new particles in the blood. The virus is genetically highly variable,[7] which limits the effectiveness of vaccination.

History

The cause of FMD was first shown to be viral in 1897 by Friedrich Loeffler. He passed the blood of an infected animal through a Chamberland filter and found the collected fluid could still cause the disease in healthy animals.

FMD occurs throughout much of the world, and while some countries have been free of FMD for some time, its wide host range and rapid spread represent cause for international concern. After World War II, the disease was widely distributed throughout the world. In 1996, endemic areas included Asia, Africa, and parts of South America; as of August 2007, Chile is disease-free,[8] and Uruguay and Argentina have not had an outbreak since 2001. In May 2014, the FAO informed that Bolivia, Colombia, Ecuador and Peru were "just one step away" from eradication;[9] North America and Australia have been free of FMD for many years. New Zealand has never had a case of foot-and-mouth disease.[10] Most European countries have been recognized as disease-free, and countries belonging to the European Union have stopped FMD vaccination.

However, in 2001, a serious outbreak of FMD in Britain resulted in the slaughter of many animals, the postponing of the general election for a month, and the cancellation of many sporting events and leisure activities, such as the Isle of Man TT. Due to strict government policies on sale of livestock, disinfection of all persons leaving and entering farms, and the cancellation of large events likely to be attended by farmers, a potentially economically disastrous epizootic was avoided in the Republic of Ireland, with just one case recorded in Proleek, Co. Louth. In August 2007, FMD was found at two farms in Surrey, England. All livestock were culled and a quarantine erected over the area. Two other suspected outbreaks have occurred since, although these seem now not to be related to FMD. The only reported case in 2010 was a false alarm from GIS Alex Baker, as proven false by the Florida Farm and Agricultural Department, and the confirmed quarantine/slaughter of cattle and pigs was reported from Miyazaki Prefecture in Japan in June after three cows tested positive. A total of some 270,000 cattle have been ordered slaughtered following the disease's outbreak.

Clinical signs

Ruptured blisters on the feet of a pig

The incubation period for foot-and-mouth disease virus has a range between one and 12 days.[11][12] The disease is characterized by high fever that declines rapidly after two or three days, blisters inside the mouth that lead to excessive secretion of stringy or foamy saliva and to drooling, and blisters on the feet that may rupture and cause lameness.[4][13] Adult animals may suffer weight loss from which they do not recover for several months, as well as swelling in the testicles of mature males, and in cows, milk production can decline significantly. Though most animals eventually recover from FMD, the disease can lead to myocarditis (inflammation of the heart muscle)[14] and death, especially in newborn animals. Some infected ruminants remain asymptomatic carriers, but they nonetheless carry FMDV and may be able to transmit it to others. Pigs cannot serve as asymptomatic carriers.[15]

Evolution

Of the seven serotypes[16] of this virus, A, C, O, Asia 1, and SAT3 appear to be distinct lineages; SAT 1 and SAT 2 are unresolved clades.[17] The mutation rate of the protein-encoding sequences of strains isolated between 1932 and 2007 has been estimated to be 1.46 × 10−3 substitutions/site/year, a rate similar to that of other RNA viruses. The most recent common ancestor appears to have evolved about 481 years ago (early 16th century). This ancestor then diverged into two clades which have given rise to the extant circulating Euro-Asiatic and South African. This event occurred around 1800.[18] Skyline plot analysis shows a population expansion in the early 20th century, which was then followed by a rapid decline in population size in the late 20th century.

At least seven genotypes of serotype Asia 1 are known.[19]

Transmission

The FMD virus can be transmitted in a number of ways, including close-contact animal-to-animal spread, long-distance aerosol spread and fomites, or inanimate objects, typically fodder and motor vehicles. The clothes and skin of animal handlers such as farmers, standing water, and uncooked food scraps and feed supplements containing infected animal products can harbor the virus, as well. Cows can also catch FMD from the semen of infected bulls. Control measures include quarantine and destruction of infected livestock, and export bans for meat and other animal products to countries not infected with the disease.

Just as humans may spread the disease by carrying the virus on their clothes and bodies, animals that are not susceptible to the disease may still aid in spreading it. This was the case in Canada in 1952, when an outbreak flared up again after dogs had carried off bones from dead animals.[3] Wolves are thought to play a similar role in the former Soviet Union.[20]

Infecting humans

Humans can be infected with foot-and-mouth disease through contact with infected animals, but this is extremely rare. Some cases were caused by laboratory accidents. Because the virus that causes FMD is sensitive to stomach acid, it cannot spread to humans via consumption of infected meat, except in the mouth before the meat is swallowed. In the UK, the last confirmed human case occurred in 1966,[21][22] and only a few other cases have been recorded in countries of continental Europe, Africa, and South America. Symptoms of FMD in humans include malaise, fever, vomiting, red ulcerative lesions (surface-eroding damaged spots) of the oral tissues, and sometimes vesicular lesions (small blisters) of the skin. According to a newspaper report, FMD killed two children in England in 1884, supposedly due to infected milk.[23]

Another viral disease with similar symptoms, hand, foot and mouth disease, occurs more frequently in humans, especially in young children; the cause, Coxsackie A virus, is different from FMDV. Coxsackie viruses belong to the Enteroviruses within the Picornaviridae.

Because FMD rarely infects humans, but spreads rapidly among animals, it is a much greater threat to the agriculture industry than to human health. Farmers around the world can lose huge amounts of money during a foot-and-mouth epizootic, when large numbers of animals are destroyed, and revenues from milk and meat production go down.

Vaccination

Like other viruses, the FMD virus continually evolves and mutates, thus one of the difficulties in vaccinating against it is the huge variation between, and even within, serotypes. There is no cross-protection between serotypes (a vaccine for one serotype will not protect against any others) and in addition, two strains within a given serotype may have nucleotide sequences that differ by as much as 30% for a given gene. This means FMD vaccines must be highly specific to the strain involved. Vaccination only provides temporary immunity that lasts from months to years.

Currently, the World Organisation for Animal Health recognizes countries to be in one of three disease states with regard to FMD: FMD present with or without vaccination, FMD-free with vaccination, and FMD-free without vaccination.[24] Countries designated FMD-free without vaccination have the greatest access to export markets, so many developed nations, including Canada, the United States, and the UK, work hard to maintain their current status. Some countries such as Brazil and Argentina which have large beef exporting industries, practise vaccination in some areas but have other vaccination-free zones.

Reasons cited for restricting export from countries using FMD vaccines include, probably most importantly, routine blood tests relying on antibodies cannot distinguish between an infected and a vaccinated animal,[25] which severely hampers screening of animals used in export products, risking a spread of FMD to importing countries. A widespread preventive vaccination would also conceal the existence of the virus in a country. From there, it could potentially spread to countries without vaccine programs. Lastly, an animal infected shortly after being vaccinated can harbor and spread FMD without showing symptoms itself, hindering containment and culling of sick animals as a remedy.

Many early vaccines used dead samples of FMDV to inoculate animals, but those early vaccines sometimes caused real outbreaks. In the 1970s, scientists discovered that a vaccine could be made using only a single key protein from the virus. The task was to produce enough quantities of the protein to be used in the vaccination. On June 18, 1981, the US government announced the creation of a vaccine targeted against FMD, the world's first genetically engineered vaccine.

The North American FMD Vaccine Bank is housed at the United States Department of Agriculture's Foreign Animal Disease Diagnostic Laboratory at Plum Island Animal Disease Center. The Center, located 1.5 mi (2.4 km) off the coast of Long Island, NY, is the only place in the United States where scientists can conduct research and diagnostic work on highly contagious animal diseases such as FMD. Because of this limitation, US companies working on FMD usually use facilities in other countries where such diseases are endemic.

Epizootics

Foot and Mouth notice; Monmouthshire, Wales, 1869

United States 1870–1929

The US has had nine FMD outbreaks since it was first recognized on the northeastern coast in 1870;[26] the most devastating happened in 1914. It originated from Michigan, but its entry into the stockyards in Chicago turned it into an epizootic. About 3,500 livestock herds were infected across the US, totaling over 170,000 cattle, sheep, and swine. The eradication came at a cost of US$4.5 million, a huge sum of money in 1914.

A 1924 outbreak in California resulted not only in the slaughter of 109,000 farm animals, but also 22,000 deer.

The US had its latest FMD outbreak in Montebello, California, in 1929. This outbreak originated in hogs that had eaten infected meat scraps from a tourist steamship that had stocked meat in Argentina. Over 3,600 animals were slaughtered and the disease was contained in less than a month.[27][28]

United Kingdom 1967

In October 1967, a farmer in Shropshire reported a lame sow, which was later diagnosed with FMD. The source was believed to be remains of legally imported infected lamb from Argentina and Chile. The virus spread and, in total, 442,000 animals were slaughtered and the outbreak had an estimated cost of £370 million.

Taiwan 1997

Taiwan had previous epidemics of FMD in 1913–14 and 1924–29, but had since been spared,[29] and considered itself free of FMD as late as in the 1990s. On the 19th of March 1997, a sow at a farm in Hsinchu Prefecture, Taiwan, was diagnosed with a strain of FMD which only infects swine. Mortality was high, nearing 100% in the infected herd. The cause of the epidemic was not determined, but the farm was near a port city known for its pig-smuggling industry and illegal slaughterhouses. Smuggled swine or contaminated meat are thus likely sources of the disease.

The disease spread fast among swine herds in Taiwan, with 200–300 new farms being infected daily. Causes for this include the high swine density in the area, with up to 6,500 hogs per square mile, feeding of pigs with untreated garbage, and the farms' proximity to slaughterhouses. Other systemic issues, such as lack of laboratory facilities, slow response, and initial lack of a vaccination program, contributed. The farmers allegedly intentionally introduced FMD to their flocks, because the payment offered to farmers for culled swine was at the time higher than their market value.

A complicating factor is the endemic spread of swine vesicular disease (SVD) in Taiwan. The symptoms are indistinguishable from FMD, which may have led to previous misdiagnosing of FMD as SVD. Laboratory analysis was seldom used for diagnosis, and FMD may thus have gone unnoticed for some time.

The swine depopulation was a massive undertaking, with the military contributing substantial manpower. At peak capacity, 200,000 hogs per day were disposed of, mainly by electrocution. Carcasses were disposed of by burning and burial, but burning was avoided in water resource protection areas. In April, industrial incinerators were running around the clock to dispose of the carcasses.

Initially, 40,000 combined vaccine doses for the strains O-1, A-24, and Asia-1 were available and administered to zoo animals and valuable breeding hogs. At the end of March, half a million new doses for O-1 and Asia-1 were made available. On the May 3rd, 13 million doses of O-1 vaccine arrived, and both the March and May shipments were distributed free of charge. With a danger of vaccination crews spreading the disease, only trained farmers were allowed to administer the vaccine under veterinary supervision.

Taiwan had previously been the major exporter of pork to Japan, and among the top 15 pork producers in the world in 1996. During the outbreak, over 3.8 million swine were destroyed at a cost of US$6.9 billion. The Taiwanese pig industry was devastated as a result, and the export market was in ruins.[27] [30] In 2007, Taiwan was considered free of FMD, but was still conducting a vaccination program, which restricts the export of meat from Taiwan.

United Kingdom 2001

The epidemic of foot-and-mouth disease in the United Kingdom in the spring and summer of 2001 was caused by the "Type O pan Asia" strain of the disease.[31] This episode resulted in more than 2,000 cases of the disease in farms throughout the British countryside. Around ten million sheep and cattle were killed in an eventually successful attempt to halt the disease.[32] The County of Cumbria was the worst affected area of the country, with 843 cases. By the time the disease was halted in October 2001, the crisis was estimated to have cost Britain £8 billion ($13 billion) in costs to the agricultural and support industries, and to the outdoor industry. What made this outbreak so serious was the amount of time between infection being present at the first outbreak locus, and the time when countermeasures were put into operation against the disease, such as transport bans and detergent washing of both vehicles and personnel entering livestock areas. The epidemic was probably caused by pigs which had been fed infected rubbish that had not been properly heat-sterilized. Further, the rubbish is believed to have contained remains of infected meat that had been illegally imported to Britain.[33]

China 2005

In April 2005, an Asia-1 strain of FMD appeared in the eastern provinces of Shandong and Jiangsu. During April and May, it spread to suburban Beijing, the northern province of Hebei, and the Xinjiang autonomous region in northwest China. On 13 May, China reported the FMD outbreak to the World Health Organization and the OIE. This was the first time China has publicly admitted to having FMD.[34][35] China is still reporting FMD outbreaks. In 2007, reports filed with the OIE documented new or ongoing outbreaks in the provinces of Gansu, Qinghai and Xinjiang. This included reports of domestic yak showing signs of infection.[36] FMD is endemic in pastoral regions of China from Heilongjiang Province in the northeast to Sichuan Province and the Tibetan Autonomous region in the southwest. Chinese domestic media reports often use a euphemism "Disease Number Five" (五号病 wǔhàobìng) rather than FMD in reports because of the sensitivity of the FMD issue. In March 2010, Southern Rural News (Nanfang Nongcunbao), in an article "Breaking the Hoof and Mouth Disease Taboo", noted that FMD has long been covered up in China by referring to it that way.[37] FMD is also called canker (口疮, literally "mouth ulcers" kǒuchuāng) or hoof jaundice (蹄癀 tíhuáng) in China, so information on FMD in China can be found online using those words as search terms.[38][39] One can find online many provincial orders and regulations on FMD control antedating China's acknowledgment that the disease existed in China, for example Guangxi Zhuang Autonomous Region 1991 regulation on preventing the spread of Disease No.5.[40]

United Kingdom 2007

An infection of foot-and-mouth disease in the United Kingdom was confirmed by the Department for Environment, Food and Rural Affairs, on 3 August 2007, on farmland located in Normandy, Surrey.[41][42] All livestock in the vicinity were culled on 4 August. A nationwide ban on the movement of cattle and pigs was imposed, with a 3-km (1.9-mi) protection zone placed around the outbreak sites and the nearby virus research and vaccine production establishments, together with a 10-km (6.2-mi) increased surveillance zone.[43]

On 4 August, the strain of the virus was identified as a "01 BFS67-like" virus, one linked to vaccines and not normally found in animals, and isolated in the 1967 outbreak.[44] The same strain was used at the nearby Institute for Animal Health and Merial Animal Health Ltd at Pirbright, 2.5 miles (4.0 km) away, which is an American/French owned research facility, and was identified as a possible source of infection.[45]

On 12 September, a new outbreak of the disease was confirmed in Egham, Surrey, 19 km (12 mi) from the original outbreak,[46] with a second case being confirmed on a nearby farm on 14 September.[47]

These outbreaks caused a cull of all at-risk animals in the area surrounding Egham, including two farms near to the famous four-star hotel Great Fosters. These outbreaks also caused the closure of Windsor Great Park due to the park containing deer; the park remained closed for three months. On 19 September 2007, a suspected case of FMD was found in Solihull, where a temporary control zone was set up by Defra.

Japan and Korea 2010–2011

In April 2010, a report of three incursions of FMD in Japan and South Korea led the United Nations Food and Agriculture Organization (FAO) to issue a call for increased global surveillance. Japan veterinary authorities confirmed an outbreak of type O FMD virus, currently more common in Asian countries where FMD is endemic.

South Korea was hit by the rarer type A FMD in January, and then suffered type O infection in April.[48] The most serious case of foot-and-mouth outbreak in South Korea's history started in November 2010 in pig farms in Andong city of Gyeongsangbuk-do, and has since spread in the country rapidly.[49][50] More than 100 cases of the disease have been confirmed in the country so far,[49] and in January 2011, South Korean officials started a mass cull of approximately 12%, or around three million in total, of the entire domestic pig population, and 107,000 of three million cattle of the country to halt the outbreak.[49]

On 10 Feb 2011, North Korea reported an outbreak affecting pigs in the region around Pyongyang, by then ongoing since at least December 2010. Efforts to control the outbreak have been hampered by illicit sales of infected meat.[51]

Bulgaria 2011

The outbreak was recognised when a wild boar was shot, which had crossed the Bulgarian-Turkish border near the village of Kosti, Burgas Province, in the Strandzha Mountains.[52] The necropsy uncovered foot-and mouth disease.[52] After this, 37 infected animals were discovered in the village of Kosti, and all susceptible animals there were culled. Burgas Province and seven other neighboring provinces declared a quarantine zone.[53]

On 14 January, a further outbreak was discovered in the neighboring village of Rezovo,[52] thought to have been carried by a Turkish cattle herd. On 17 January, the presence of the disease was confirmed.[52] The Bulgarian authorities ordered culling of all susceptible livestock in Rezovo.[54] Compensation for the losses in the two villages has been promised.[52]

On 31 January, a third focus of infection was discovered in the southeastern Bulgarian village of Gramatikovo. On 25 March, two new outbreaks were discovered in the villages of Granichar and Kirovo.[55]

Economic and ethical issues

Epidemics of FMD have resulted in the slaughter of millions of animals, despite this being a frequently nonfatal disease for adult animals (2–5% mortality), though young animals can have a high mortality.[56] The Taiwan outbreak that only affected pigs also showed a high mortality for adults. The destruction of animals is primarily to halt further spread, as growth and milk production may be permanently affected, even in animals that have recovered. Due to international efforts to eradicate the disease, infection would also lead to trade bans being imposed on affected countries. Critics of current policies to cull infected herds argue that the financial imperative needs to be balanced against the killing of many animals,[57] especially when a significant proportion of infected animals, most notably those producing milk, would recover from infection and live normal lives, albeit with reduced milk production. On the ethical side, one must also consider FMD is a painful disease for the affected animals.[58] The vesicles/blisters are painful in themselves, and restrict both eating and movement. Through ruptured blisters, the animal is at risk from secondary bacterial infections [58] and, in some cases, permanent disability.

See also

References

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