Postweaning multisystemic wasting syndrome (PMWS) in Sweden from an exotic to an endemic disease

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    Veterinary Quarterly 2007; 29(4): 122-137

    Postweaning Multisystemic Wasting Syndrome (PMWS) in SwedenFrom an exotic to an endemic disease

    P. Wallgrenl '2'*, K. Bela', C.-J. Ehlorsson3, G. Bergstrom3,M. Lindberg3, C. Fossum4, G.M. Allan5 and J.A. Robertsson3

    'National Veterinary Institute, Uppsala, Sweden2Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden3Swedish Animal Health Service, Johanneshov, Sweden4Department of Molecular Biosciences, Section of Veterinary Immunology and Virology,Swedish University of Agricultural Sciences, Uppsala, Sweden

    5Virology Branch, Agri-food and Biosciences Institute, Veterinary Sciences Division, Stormont,Belfast, United Kingdom


    Summary and keywords 123Introduction 123Material and methods 124

    Pig production in Sweden 124The general health status of the Swedish pig population 124Contact with other pig populations 125PCV2 in Sweden 125Diagnosis of PMWS in Sweden 125Clinical recordings in herds suspected or deemed for PMWS 126Efforts made to control PMWS in affected herds 126Criterions for declaring herds previously PMWS-positive or negative at the herd level 126

    Results 126Number of herds positive for PMWS during the first three years of the disease . 126PMWS in relation to geographic area of Sweden 127Losses over time 127Herd categories 127Correlation to herd size 127PMWS in sow pool satellites 127PMWS in Sweden and factors other than PCV2 128Effect of treatments with antimicrobials in herds suspected for PMWS 128Number of PMWS positive herds later declared free from the disease 128

    Discussion 128

    Concluding remarks 130Figures 131Tables 132

    References 135

    *Corresponding authorAddress: National Veterinary Institute, SVA, 751 89 Uppsala, SwedenE-mail: Per.Wallgren@sva.seTel.: +46 18 67 40 00Fax: +46 18 30 91 62

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    Postweaning Multisystemic Wasting Syndrome (PMWS) in SwedenFrom an exotic to an endemic disease

    P. Wallgren, K. Bela, C.-J. Ehlorsson, G. Bergstrom,M. Lindberg, C. Fossum, G.M. Allan and J.A. Robertsson


    Postweaning multisystemic wasting syndrome (PMWS) is causally associated with porcine circovirus

    type 2 (PCV2) infection of pigs. PCV2 was first demonstrated in Swedish pigs in 1993, although the

    virus was almost certainly present in pigs in the country before that. Despite this, no signs of PMWS

    were observed in pigs of Sweden until the first outbreak was reported in 2003. The accumulated

    number of PMWS-affected herds have increased via 16 (2004) and 41 (2005) to 123 in December 2006.

    Of these herds, 30 (25%) have now been declared free from PMWS. However, a number of other

    herds have had individual pigs that have fulfilled the demands for PMWS at necropsy and 52 of these

    herds have been declared negative on herd basis after treatment for intestinal or respiratory diseases,

    and/or by correcting shortcomings in management of the herd including feed. Thus, individual cases

    of the disease have been observed in around 200 herds by the end of 2006 and PMWS is now regarded

    as an endemic disease in Sweden.The pig population of Sweden is geographically isolated, the density of pigs and the pathogen load in

    the country is low and the use of growth promoters (low dose antibiotics in feed) was prohibited in

    1986. Additionally, the trade of animals in Sweden is organised in a restricted way. Because of these

    factors it is possible to conduct meaningful real-time studies on the transformation of PMWS in

    Sweden from being an exotic to an endemic disease in a three year time scale.

    Initially the PMWS cases were concentrated in the southern part of Sweden, but have gradually

    spread north. The PMWS-positive herds have, in general, had an effective production, but some

    management errors have constantly been observed in affected herds. Physical links between affected

    herds are often missing, and the data generated to date on the PMWS outbreaks in Sweden do not

    suggest an introduction of a new contagious microbe into the country that is responsible for thePMWS outbreaks, nor does PMWS appear to be spread via semen. In Sweden, intensity in rearing,

    disease preventing measures and immaturity of the piglets appear to be important as predisposingfactors to PMWS and, as such, are discussed in this article.

    Keywords: Circovirus; Epidemiology; Mortality; Multifactorial diseases; Pigs; Porcine circovirus type 2

    infections; Postweaning multisystemic wasting syndrome; Semen; Spread; Sweden; Swine disea-

    ses; Transmis-sion; Viral diseases; Wasting.


    Porcine circovirus type 2 (PCV2) is generally

    accepted as the causal agent of postweaning multi-

    systemic wasting syndrome (PMWS) (2,54), but it

    is also generally accepted that the presence of

    other infectious or non-infectious factors is

    required for the development of the full clinical

    disease (3,4,28,52). PMWS has been experimen-

    tally reproduced in snatch-farrowed colostrum-

    deprived (SFCD) and in gnotobiotic piglets byco-infections with PCV2 and porcine parvovirus

    (PPV) (3,13,52) or porcine reproductive and

    respiratory syndrome virus (PRRSV) (4,17). In

    addition, PMWS has been successfully inducedexperimentally in PCV2 seronegative colostrum

    fed pigs inoculated in the first week of life withPCV2 alone (31) and in PCV2 seropositve pigletsweaned at the age of 12-14 days, inoculated withMycoplasma hyopneumoniae at the age of 4 weeksand with PCV2 at the age of 6 weeks, respectively(46). PMWS has also been reproduced in gnotobi-otic piglets inoculated with PCV2 alone in combi-nation with immunsostimulators (29) or immuno-suppressors (27). Experimental infections ofconventional and in specific pathogen-free (SPF)pigs with tissue homogenates from PMWS-affectedweaners have also induced mild PMWS (7,1). Inthese experiments, all inoculated pigs seroconver-ted to PCV2, but not to any other common virusor bacteria. Transmission of PMWS has also beendemonstrated by mixing healthy weaners with


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    PMWS-affected pigs in previously emptied andcleaned facilities (30).

    PMWS was first observed in a high health herd inCanada in 1991 (6,12). Wasting of weaners wasalso observed in France 1996 (33) and since thenthe disease has spread around the world (2). InScandinavia, PMWS was officially diagnosed forthe first time in Denmark during 2000 and byMarch 2005 PMWS had been reported in 539herds (66). In Norway, PMWS has been diagnosedin two herds during 2003 (10). These herds wereimmediately isolated and finally stamped out (36).To date, PMWS has not been diagnosed in anyother herd in Norway. PMWS has not been diag-nosed in Finland although antibodies to PCV2have been demonstrated in serum from 80% of500 randomly selected fattening pigs collected atslaughter and in all Finish nucleus herds (20). InSweden, PMWS was diagnosed for the first timein December 2003 (62). Since then, the diseasehas spread with an increasing speed in the country.This manuscript aims to describe this spread, andhow PMWS transformed from being an exotic toan endemic disease in Sweden.


    Pig production in SwedenThe Swedish pig industry comprises approximately160,000 sows and around 3.25 million pigs arereared annually to market weight. All pig herds inSweden are health monitored by the SwedishAnimal Health Service, supported by legislation ofthe Swedish Board of Agriculture. Herds withhealth problems are put under restrictions, andPMWS is handled according to strategies develo-ped in co-operation with the producers .and theauthorities. The number of herds in 2003, the lastyear with freedom from PMWS, is used to calcu-late the relative risks of being diagnosed withPMWS. During 2003, 2,483 production sites hou-sed sows out of which 886 had more than 50sows, 427 more than 100 sows, 45 more than 500sows and 22 more than 1,000 sows. Fattening pigswere present at 2,993 sites out of which 721housed more than 500 pigs. Farrow to finish herds(n=418) and Specific Pathogen Free herds (SPF-herds, n=25) are included under both categotiesabove, as well as 30 pure-bred nucleus herds withYorkshire (Y), Landrace (L), Hampshire (H) orDuroc (D) pigs and 70 multiplying herds produ-cing YL-hybrids that sell breeding stock.

    Around 20% of the Swedish pig production takesplace in sow pool systems. In these systems all drysows are kept at a central unit and before farro-wing they are leased by piglet producing unitscalled satellites. Following weaning, the sows arereturned to the central unit for mating. In 2003,there were 30 sow pools with a total of 32,200sows and 284 satellite units. This system is nor-mally performed in cycles of 16 weeks at the satel-lite units. The 16 week cycle is typified by thearrival of pregnant sows at the satellite unit threeweeks prior to farrowing, weaning on this unit at 5weeks of age and return of sows to the central unitbefore the arrival of a subsequent group of sowseight weeks later. Satellites can also run two orfour cycles like this in a parallel system, and ingeneral there is time for adequate hygiene measu-res. However, in recent years some satellite herdshave developed intensified systems with shortercycles with a view to increased production, whichin practise have lead to shortened times for rearingand/or hygiene measures.

    A ban of growth promoters (low dose antibioticsin feed) was effectuated in Sweden in 1986.During the subsequent years intestinal healthproblems of recently weaned piglets increased(51), which necessitated improvements in therearing systems in Swedish herds. Consequently,over 90% of the Swedish pigs are today reared inbatch systems based on age-segregation from birthto slaughter (21). Swedish animal welfare lawdemands an area of 0.17 m2 + (weight in kg/130kg) m2 for growing pigs (42), which correspondsto an area of 0.4 m2 per weaner of 30 kg and 0.94m2 for a market weight pig of 100 kg. This lawalso prohibits weaning before 4 weeks of age, andweaning generally takes place at the age of 4 to 5weeks.

    The general health status of the Swedish pigpopulationThe Swedish pig population has a favourablehealth status. Sweden is free from all diseaseslisted by the Office International des Epizooties(01E), including Aujeszky's disease (AD) andporcine reproductive and respiratory syndrome(PRRS), as well as from porcine endemic diar-rhoea (PED) and transmissible gastro-enteritis(TGE). AD was diagnosed in 1963 and eradicatedfrom Sweden in 1996 (50). Additionally, since1984 Salmonella infection is generally diagnosedin less than 5 pig herds per year (43). However,

  • 77 pig herds in the area south of Stockholm were

    subclinically infected with Salmonella cubana

    during 2003, which was spread from a feed plant

    and discovered by the national screening program.

    All these infected herds and the feed plant are now

    free of this infection (47,57). Infections withMycoplasma hyopneumoniae and Actinobacilluspleuropneumoniae are widespread in the conven-

    tional pig population in Sweden, but the influence

    of these diseases has decreased since the 1990ies

    due to the commonly performed age segregated

    production from birth to slaughter (21). However,

    during the recent years problems with Actinobacil-

    lus pleuropneumoniae have increased.

    Purebred and multiplying herds in Sweden are

    affiliated to extended control programs and are

    also declared free from atrophic rhinitis (toxin

    producing strains of Pasteurella multocida),

    Salmonella spp., swine dysentery (Brachyspirahyodysenteriae) and mange (Sarcoptes scabiei).

    Contact with other pig populationsPrior to 2005, transports of pigs from othercountries through Sweden had not taken place.

    Since 2005, transfer breeding stock exported from

    Denmark to the Baltic states and Poland through

    Sweden has occurred. These shipments of pigs are

    declared to emanate from Danish nucleus herds

    free from PRRS (22).

    During 1995-2002, a total of 57 boars wereimported to Sweden, 15 from Finland and 42 from

    Norway. Recently a formal genetic cooperation

    has been established between these three countries,

    resulting in import of 115 Norwegian boars from

    2006 up to June 2007. Further, around 75.000semen-doses have been imported from Norway

    during the last decade. Due to lack of pigs inSweden a total number of 34,000 growers have

    been imported from Norway (n=4,000) andFinland (n=30,000) since 2006, and the number

    of pigs imported corresponds to 85 batches of 400

    pigs. These pigs were imported at 25 kg bodyweight as complete batches and reared to market

    weight without mixing with other pigs (22).

    Norway and Finland have a similar health status as

    Sweden: Pigs are still free from PRRS, and were

    at the time of the exports also free from PMWS,

    although the incidences of PCV2-seropositive pigs

    were high in both countries (20,36).


    PCV2 in SwedenPCV2 infection of pigs has been confirmed aswidespread in Sweden by two serosurveys. In apilot study 288 out of 300 (96%) randomly selec-ted porcine sera contained antibodies to PCV2(35), and in a subsequent study performed in 2000antibodies to PCV2 were demonstrated in 1208 outof 1500 (80.5%) sera collected within the nationalcontrol program for Aujeszky's diseases (44).

    PCV2 infection was first demonstrated in 1993 inSweden in a SPF farrow to finish herd (65). Thisherd was initially set up by caesarean sections in1988 and had been closed since establishment,except for purchase of semen from conventionalboar stations in Sweden. Retrospective testing ofsera collected from this herd revealed that the herdwas PCV2 negative until 1993, when seroconversi-on occurred. The biosecurity procedures for thisherd (64) indicate use of PCV2 contaminatedsemen as the cause of the seroconversion to PCV2.During the period of seroconversion to PCV2 inthe SPF herd exudative epidermitis was diagnosedin two litters, and a transient reduced fertility wasrecorded (65). However, the post weaning mortali-ty in this herd since the introduction of PCV2 isless than 0.1% and PMWS has not been diagnosedin any pig from this herd. However, a PCV2isolate recovered from tissues collected in 1993from a pig in this herd has been successfully usedas an inoculum for experimental reproduction ofPMWS in SFCD piglets in Northern Ireland,Sweden and Denmark (5,19).

    Diagnosis of PMWS in SwedenIn individual pigs, PMWS has been diagnosedusing the internationally accepted criteria ofclinical disease, typical macroscopical andhistological lesions and the presence of anabundance of PCV2 antigen in these lesionsdemonstrated by immunohistochemistry (IHC)(55,54).

    At herd level, diagnosis of PMWS has followedthe criteria outlined within the PCVD researchprogram of the sixth framework of EU (67). InSweden the recommended criterion to diagnosePMWS on herd level corresponds to losses of atleast 4% post weaning. These losses have beendefined as the merged incidence of runts, culledand dead piglets (62).

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    Clinical recordings in herds suspected ordeemed for PMWSThe losses in terms of wasting, culled and deadpigs post weaning have been documented since theonset of PMWS in Sweden. These losses havebeen r...


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