The NATWEST/RAC ANNUAL FELLOWSHIP in STRATEGIC DEVELOPMENT OF THE UK PIG INDUSTRY 2nd November 2004 The Disease Status of the UK Pig Industry A paper presented by David Strachan MA VetMB BSc PhD MRCVS SAC Veterinary Services, Aberdeen In Support of Dr Keith Lawrence’s Award under the heading of: To challenge the future approach to managing disease in the UK in an ever changing marketplace

Disease Status

Defining the health or disease status of a national herd, at its most basic level, involves the qualitative description of diseases present within national boundaries. The Organisation Internationale des Epizooties (OIE) requires member states to inform the organisation of the presence of any of a large list of animal diseases relevant to international trade and disease control. The information required is provided by national statutory disease notification and disease surveillance systems which also help to maintain national freedom from exotic diseases. The island statuses of Britain and Ireland afford theoretically, increased opportunities to remain free of endemic diseases that are present on the mainland of Europe. In addition, EU and OlE regulations governing trade in live animals are designed to minimise the risks of disease introduction between signatory states. These controls appear to have been relatively successful; indeed the last two outbreaks of OIE list A diseases in pigs (classical swine fever in 2000 and foot and mouth disease in 2001) are not thought to have been caused by the introduction of infected animals. However, international agreements, health controls, quarantine and testing of incoming livestock are obviously only effective when the infectious agents concerned have been identified. Two of the most devastating pig diseases to affect the industry in the last 20 years (porcine reproductive and respiratory syndrome and post-weaning multisystemic wasting syndrome) appear to have been introduced and spread throughout much of the GB herd before the aetiological agents responsible for the disease had been characterized.

Quantitative description of national endemic disease status is less easy to ascertain. While epidemiological studies can provide estimates of disease prevalence, more accurate descriptions can be provided by comprehensive industry-wide surveys, especially relevant in industries as small as that of the UK. The lack of such up-to-date, detailed information on many of the economically important production limiting diseases in the UK inhibits progress in several areas. 1) Accurate knowledge of national herd health status is essential in estimating the costs of individual diseases to the pig industry. 2) Following on from this, coordinated disease eradication strategies can only be successful if the national, regional and area health statuses are known. 3) Increased understanding of the epidemiology of introduced diseases would be helped by accurate knowledge of the disease status of individual farms. For example, PMWS has never been a notifiable disease in the UK and the epidemiology of the disease is still being elucidated five years after its emergence.

Disease Surveillance

Both the qualitative and the quantitative description of national disease status require a robust disease surveillance system. In the UK, a network of disease surveillance centres is provided by the Veterinary Laboratories Agency (England and Wales), the Scottish Agricultural College (Scotland) and the Department of Agriculture and Rural Development (Northern Ireland). A large proportion of the disease surveillance function carried out by these agencies is so-called “scanning” surveillance and relies on samples submitted by farmers and/or vets for diagnostic testing. While this method of surveillance is useful for detecting new and emerging diseases (such as PMWS), endemic diseases are likely to be under reported by this system. Active or targeted surveillance methods are required to more accurately estimate levels of endemic diseases within animal populations using whole industry or cross-sectional studies.

Essential to both these disease surveillance systems is the requirement for accurate and consistent disease definitions. Both the VLA and SAC disease surveillance laboratories use the same strict criteria for recording diagnoses, the Veterinary Investigation Diagnostic Analysis (VIDA) system. Unfortunately the same stringency is not applied to all other methods or surveys and the results are therefore not always comparable between surveys. The diagnostic tests used are also variable and different surveys may be measuring clinical disease, previous exposure to a pathogen (by serology) or the infection with a pathogen in the possible absence of clinical disease (“carrier state”). For some diseases where only subtypes of a particular aetiological agent are pathogenic, screening for the presence of the agent at the pathogen species level alone may give misleading information on disease status. Inconsistencies in tests used, testing protocols and interpretation, cause confusion and difficulties for producers, their veterinarians and breeding companies alike. In addition, statistically valid sampling procedures must be used in order to provide robust prevalence data. In the absence of an official herd health declaration, as occurs in the Danish Specific Pathogen Free (SPF) system, current and accurate information on the UK herd health status is lacking. If diagnostic and categorisation criteria can be agreed by all interested parties, then such as scheme might help to reduce the frequent confusion over what is and what is not "high health" or "defined high health status" stock. With the current increased focus on pig health in the UK, perhaps the time is right to reexplore the possibility of a national herd health classification scheme.

Disease Spread

The structure of the UK pig industry has considerable effects on the spread of infectious agents between herds and thus on the disease status of the national herd. Firstly, although the national pig density is relatively low, pig production is concentrated in certain geographical areas of Great Britain with effectively higher pig density (East Anglia and East Yorkshire in particular). This has allowed, and continues to allow, the spread of diseases whose aetiological agents are thought capable of being spread over short distances by aerosol (enzootic pneumonia) or by birds (transmissible gastroenteritis) (Goodwin, 1985; Harris and Alexander, 1999). Secondly, the majority of commercial units purchase replacement stock from a small number of sources that increases the potential for the rapid dissemination of infectious agents throughout large parts of the industry. This has been especially important where ill-defined diseases or diseases of unknown aetiology have been introduced into the country. For example, there is evidence to suggest that PRRS may have originally spread in the UK via animal (Robertson, 1992a) and semen movements (Robertson, 1992b) at a time when diagnostic testing for exposure to PRRS virus was not available.

Endemic Disease Status in the UK herd

Porcine reproductive and respiratory syndrome (PRRS)

Since its arrival in 1991, the disease has spread widely within the UK. Introduction of the infection into units via live animals, semen and area transmission is thought to occur (Mortensen et al. 2002). Detailed recent epidemiological studies are lacking, but diagnostic serological testing by enzyme immunoassay (EIA) in 356 herds in Britain showed the presence of active viral infection in 56% of herds (Richardson, 2004). This was based on serological testing of six pigs from each of five age groups (3-4 weeks, 5-7 weeks, 8-10 weeks, 11-13 weeks and >15 weeks) with over 95% seroprevalence demonstrated in the older age group. The same study suggested some regional variation (35-82%) with lower prevalence among outdoor herds and in areas where outdoor herds predominate. To date there has been no virological or serological evidence that the “US strain” of PRRSv, which has caused severe problems in some European countries, is present in UK pigs (T. Drew, pers. comm.). Seroprevalence is high in most countries where the virus is present (Benfield et al., 1999; Martelli, 2002) although low seroprevalence has been recorded in some European countries without any evidence of clinical outbreaks (Stukelj & Valenèak, 2003). Vaccination is now widespread and although genetic differences between European strains can cause variation in vaccine efficacy, these are less important than the more fundamental genetic differences between the European and American strains (Labarque et al., 2004) Although local spread may continue to cause herd breakdowns in some pig-dense areas, the depopulation/repopulation of herds with widely available PRRS-free stock and the increase in closed herd policies (in some cases combined with vaccination) leading to possible elimination of the virus from breeding herds, may further help to reduce the prevalence in the national herd.

Aujeszky's disease

Aujeszky's disease was eradicated from the UK mainland between 1983 and 1989 but is still present in Northern Ireland. An eradication programme is underway in Northern Ireland and although serological surveys estimate that some herds remain infected, reports of clinical disease are currently rare (S. Kennedy, pers. comm.).

Swine influenza

Oubreaks of swine influenza (SI) occur regularly within the UK herd causing reproductive problems and clinical respiratory disease. Economic losses due to SI in the UK finishing herd alone have previously been estimated at L60m per annum (Kay et al., 1994). In addition, SI virus infection can contribute to porcine respiratory disease complex (PRDC) in combination with other infections. Recent VIDA diagnoses of swine influenza range from between 38 and 9 outbreaks confirmed per year (VIDA 2002). The majority of outbreaks in the recent years have been due to “classic” H1N1 (endemic in the pig population), avian-like H1N1 and human-like H3N2 serotypes. The highly contagious nature of this virus and the variability in clinical manifestation of disease make the current influenza status of the UK herd difficult to ascertain. In most herds, the infection spreads rapidly within all age groups and the virus may disappear from the herd (Easterday and van Reeth, 1999). In some cases however continuous virus circulation may occur (Madec 1985) and may cause annual reappearance of clinical disease (Brown, 2003). The public health aspects of influenza A viruses are well known and there is concern over the possibility of recombination between highly pathogenic avian and human influenza viruses in the porcine host and the zoonotic consequences.

Transmissible gastroenteritis (TGE)

The emergence and spread of porcine respiratory coronavirus in the UK pig population, and the cross protection against TGE that the infection provides (Pensaert and Van Reeth, 1998), is thought to have been the major factor responsible for the decline in incidence of TGE in the UK since the 1980s. Five outbreaks of TGE were recorded in England during the late 1990s (VIDA), and a serological survey of 64 finishing units in East Anglia demonstrated evidence of exposure to the TGE virus in 22% of units (Pritchard et al., 1999). The disease has never been recorded in Scotland. Sporadic outbreaks of porcine epidemic diarrhoea, caused by a coronavirus distinct form TGE virus, are recorded in England, although the infection is not thought to be common in the UK and Europe (Pensaert and Van Reeth, 1998).

Enzootic pneumonia (EP)

Enzootic pneumonia due to Mycoplasma hyopneumoniae infection is considered to be one of the major production limiting diseases worldwide. The prevalence of the disease shows some variation between pig producing areas and the severity of pulmonary disease may be increased by the involvement of viruses such as PRRS and other contributors to PRDC (Halbur et al., 1993) and perhaps more recently by the effects of PMWS. Most recent surveys in the UK have been based on vaccine usage or surveys of herd health declarations and no widespread serological surveys have been carried out in recent years. Abattoir data involving quarterly monitoring of 125 finishing herds in Scotland (representing around 75% of Scottish production) as part of the Wholesome Pigs scheme, have shown that 50% of units have average lung scores consistent with absence of M. hyopneumoniae in the herd (unpublished data). Abattoir monitoring on its own is not a robust method of ascertaining EP-status since other chronic bacterial infections can cause grossly similar lesions and such lesions appear to be more frequent in some herds affected by PMWS. However as one of the methods of monitoring for freedom from disease in defined high health status herds, abattoir monitoring is widely used throughout the industry. Confirmatory testing of suspicious lesions is now frequently performed by polymerase chain reaction (PCR) testing for M. hyopneumoniae-specific DNA.

Progressive atrophic rhinitis

Atrophic rhinitis involving toxigenic strains of Pasteurella multocida (alone or in combination with other agents) is now more frequently referred to as progressive atrophic rhinitis (PAR) to differentiate it from non-progressive atrophic rhinitis (NPAR) caused by toxigenic strains of Bordetella bronchiseptica. Toxigenic B. bronchiseptica is believed to be widespread in the pig population and NPAR is not considered a major production limiting disease. In contrast, PAR can cause poor growth in finishing pigs (Pedersen and Barfod, 1981). Deleterious effects due to PAR on DLWG have been shown to vary markedly between surveys and between units (reviewed by Christensen et al., 1999) but can be as high as 13%. A marked increase in prevalence of PAR was observed during the 1960s and 1970s (Penny and Mullen, 1975) and although some work has suggested that PAR is still spreading between herds in some countries (Glattleider et al., 1996), current evidence in the UK based on use of vaccine in sows (J. Richardson pers. comm.) would tend to suggest that clinical disease is now not widespread. The disease is likely to have declined due to the fact that for some years most breeding stock for sale in the UK has originated from herds subjected to routine monitoring for the presence of PAR. Snout scoring of slaughter pigs has long been used as a method to monitor the PAR status of herds (Penny and Mullen, 1975) but interpretation in the absence of severe lesions is difficult (Goodwin, 1988). Recent development of PCR tests for the detection of toxigenic P. multocida-specific DNA in throat swabs represent a significant advance in diagnosis and monitoring of PAR (Amigot et al., 1998) and such tests are now routinely used by some breeding companies. The current prevalence of PAR in the UK is not known but out of 87 herds in Scotland routinely monitored by abattoir snout scoring, lesions suggestive of PAR were observed in pigs from seven (8.5%) of the herds (unpublished data).

Streptococcus suis

Streptococcus suis infections are responsible for a number of clinical problems, the most serious being meningitis, septicaemia and arthritis. The organism is also frequently involved as a secondary pathogen in complex respiratory disease and more occasionally as a cause of abortion. Of the 34 known serotypes, eighteen (serotypes 1, 2 [& 1/2], 3, 4, 7, 8, 9, 10, 14, 15, 16, 17, 22, 24, 25, 28, 31 and 34) have been isolated from pigs in the UK (Heath et al. 1996, MacLennan et al., 1996). The serotypes most often responsible for primary clinical disease are serotypes 2, 1/2, 14 (or 1/14). Assessment of herd health status with regard to S. suis is usually made on a combination of clinical grounds and bacteriological isolation and typing. No reliable serological tests are currently available. Healthy carriers of S. suis are a frequent finding and bacterial isolation from tonsils is an insensitive method of detection/screening. Molecular techniques for detecting serotypes, subtypes or specific virulence factors in tonsillar swabs may in the future be useful as screening tests (Wisselink, 1999). Serotype 2 became a problem the UK during the 1980s as a cause of meningitis and septicaemia, mainly in weaned pigs, and strains of this serotype are still regarded as the most serious within the industry. Health Controls in breeding companies supplying replacement stock have succeeded in virtually preventing new outbreaks of serotype 2 disease. Serotype 14 emerged as a significant problem during the 1990s manifesting as arthritis and meningitis/septicaemia mainly in unweaned piglets (Heath et al., 1996: MacLennan et al., 1996). Based on VIDA returns, the disease is now widespread throughout the UK industry.

Since May 1998, seven outbreaks of meningitis and septicaemia involving S. suis serotype 1/2 (reacting to both serotype 1 and serotype 2 antisera) have been recorded in Scottish herds. Traditionally considered of lower intrinsic virulence than serotype 2 isolates, these outbreaks have been generally serious, with mortality rates of up to 3.6% in newly weaned pigs (Strachan et al., 2003).

Several herd problems with S. suis serotype 9 have occurred in the last few years in the UK (Heath and Hunt, 2001) and Eire (P. Spillane, pers. comm.). The clinical presentation appears to be similar to serotype 1 or 1/14 disease with arthritis and meningitis in piglets and recently weaned pigs. The origin of these isolates is not known.

Actinobacillus pleuropneumoniae (APP)

Like many infectious bacterial diseases of pigs, pleuropneumonia due to infection with Actinobacillus pleuropneumoniae has become more important with increased intensification of the industry. Although the disease has been reported in many pig producing countries, as would be expected, the prevalence of the 15 known serotypes shows some geographical variation (Taylor, 1999). Isolates of certain serotypes (e.g. serotypes 1, 5, 9, 10 & 11) are generally believed to have a higher intrinsic virulence than others (e.g. serotype 3) although differences in virulence have also been observed within the same serotype (Brandreth and Smith, 1987). The serotypes most commonly recorded in the British Isles are serotypes 2, 3, 6, 7 & 8 (McDowell and Ball, 1994). Serotype 2 appears to be isolated more frequently in Northern Ireland compared to Britain (McDowell, pers. comm.). Recent studies quantifying the herd prevalence of A. pleuropneumoniae infection and clinical disease due to the organism are lacking. Brandreth and Smith (1985) examining slaughter pigs from 78 herds in eastern England found pleuropneumonia-like lesions in 44 herds (56%). A. pleuropneumoniae was isolated in pigs from 22 of these herds and also in pigs from 4 herds where no pleuropneumonia-like lesions were recorded. It is generally believed that actinobacilli other than APP can cause pleuropneumonia-like lesions (Taylor, 1999) though usually without high mortality. Acute pasteurellosis due to Pasteurella multocida may also resemble pleuropneumonia (Taylor, 1999). The unreliability of slaughter surveillance for APP has driven the development of a serotype-specific serological surveillance system used in the Danish Specific Pathogen Free (SPF) programme (Sorensen, 2001) where serotypes 2, 6, 5 and 12 occur most commonly. Serotype-specific enzyme immunoassays (EIA) are now being developed in Denmark to supercede the original complement fixation tests (CFT). Such tests are not currently available in the UK. PCR tests specific for Apx toxin genes have been developed (Frey et al., 1995, Angen & Jessing, 2004) but are not currently validated for tonsillar swabs in live animals.

Swine dysentery

Infection with Brachyspira hyodysenteriae, causing swine dysentery, is endemic in many pig-producing countries, including the UK. A practitioner survey conducted by Taylor (1984) indicated that 27% of herds were affected with the disease. A more recent survey of 105 producers by Pearce (1999) estimated that swine dysentery was a problem in 10.5% of herds.

More detailed bacteriological studies involving 98 UK units demonstrated that B. hyodysenteriae was present as a primary pathogen in 13% of herds and as part of a mixed infection in 16% of herds (Thomson et al., 2001). Definitive diagnosis has previously depended on the somewhat technically demanding isolation and identification of the organism from faeces. However the advent of PCR tests for Brachyspira species-specific DNA has improved diagnostic capability. It should be noted that “avirulent” isolates of B. hyodysenteriae have been isolated (Lysons et al., 1982). In addition, virulent Brachyspira hyodysenteriae strains producing PCR results consistent with Brachyspira innocens (as the name suggests, an avirulent species) have been detected in four UK herds since 1999 (J. Thomson, pers. comm.). The farms involved had reported clinical signs typical of swine dysentery in grower pigs. Confirmation of the B. hyodysenteriae species identification was achieved by a combination of bacterial culture and a PCR test that detects the TlyA haemolysin gene of B. hyodysenteriae. The current prevalence of this atypical strain of B. hyodysenteriae is under investigation.

For these reasons, a combination of culture (isolation and biochemical identification) and PCR techniques are currently recommended for diagnostic purposes. Serological tests have been used for prevalence studies in the USA (Egan et al., 1983) but such tests were not appropriate for the detection of individual pigs with disease. The development of tests based on other B. hyodysenteriae-specific antigens shows promise (La and Hampson, 2001) but no such tests are available in the UK.

Porcine colonic spirochaetosis

Colonic spirochaetosis or spirochaetal diarrhea has been reported in most major pig-producing countries and was first recognized in the UK by Taylor (1980). The epidemiology of the disease is not fully understood and is complicated by the fact that the causative organism, Brachyspira pilosicoli, can also be isolated from other hosts including birds (Jansson et al. 2001), dogs (Oxberry and Hampson, 2003) and humans (Komer and Gebbers, 2003). In a survey of colitis conducted by Thomson et al. (2001), B. pilosicoli was the most commonly isolated bacterial pathogen and was suggested as the primary agent in 18% of the outbreaks and as part of a mixed infection in a further 24% of herds. As for swine dysentery, diagnosis is based mainly on bacterial culture with biochemical identification and PCR.

Porcine proliferative enteropathy (PPE)

The spectrum of clinical entities now grouped as porcine proliferative enteropathy (porcine intestinal adenomatosis, regional ileitis and haemorrhagic proliferative enteropathy) have a worldwide distribution (McOrist and Gebhart, 1999). A survey of 319 pig farms in England and Scotland (representing around % of the UK herd) in 1998 suggested that 31% of farms had experienced one or more clinical outbreaks of PPE in the previous 3 years (Smith and McOrist, 1998). The causative organism Lawsonia intracellularis is believed to have a very widespread distribution and a serological survey of finishing pigs in the UK and Eire has estimated a seroprevalence of 62% with around 95% of herds having seropositive pigs (Mortimer et al., 2000).

Sarcoptic mange

Infestation with Sarcoptes scabiei var. suis is considered to be the most important ectoparasite of pigs throughout the world and a cause of significant economic loss (Cargill and Dobson, 1979). Recent estimates of prevalence have been based on assessment of popular dermatitis scores in slaughtered pigs, caused by hypersensitivity to the mite (Davies et al., 1991) although an antibody EIA for testing meat juice in slaughtered pigs has recently been developed (Vercruysse et al., 2004). Papular dermatitis surveys have estimated that up to 24% of pigs and 24% of units in England have scores consistent with sarcoptic mange (B. Rice, pers. comm.). A similar herd prevalence of 23% has been estimated in Scottish herds (unpublished data).

Conclusion

The health status of the UK pig industry can be defined in different ways:

1) Are specific diseases present in the UK herd? For most diseases this question is easily answered. The high standard of previous and current scanning surveillance has resulted in detailed knowledge in this area.

2) If a disease is present, how widespread is the disease and where is it? In other words, what is the herd prevalence? Detailed information in this area is lacking as there have been few recent studies concerning the enzootic diseases of major economic importance. An exception to this is the recently introduced Zoonosis Action Plan national Salmonella serology programme which has provided useful information on the prevalence of certain Salmonella spp. in the UK pig herd (although a pathogen of zoonotic interest rather than a major production-limiting disease). 3) What proportion of pigs in the national herd is affected? This would require details not only of the number of herds that were affected but also the disease prevalence within each herd.

Significant advances in disease surveillance systems within the UK pig industry are required before these questions can be fully answered for many of the endemic diseases. High-throughput, and perhaps cheaper, molecular diagnostic tests and the increased use of geographical information systems in disease surveillance may well facilitate such advances. The health status of the UK pig industry will be a dynamically changing picture, influenced by many factors such as changes in world trade, new and emerging diseases and the withdrawal of antibiotic growth promoters but accurate knowledge of the status is essential for its future competitiveness in a global market.

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