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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
TABLE OF CONTENTS
Summary and keywords 123
Introduction 123
Material and methods 124Pig 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 130
Figures 131
Tables 132
References 135
*Corresponding authorAddress: National Veterinary Institute, SVA, 751 89 Uppsala, SwedenE-mail: [email protected].: +46 18 67 40 00Fax: +46 18 30 91 62
123
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
SUMMARY
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.
INTRODUCTION
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 by
co-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 induced
experimentally 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.
MATERIAL AND METHODS
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 with
Mycoplasma 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 75.000
semen-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) and
Finland (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).
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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 recorded whenever a herd has been suspectedor confirmed of having PMWS, or declared freefrom PMWS. Additionally the presence of anyother significant disease on these farms has beendocumented as has the clinical effect of grouptreatment with antibiotics, when applied.
Efforts made to control PMWS in affectedherdsThe overall strategy to control PMWS in Swedenhas been to perform strict age segregated systemswith hygienic measures between consecutivebatches of pigs and to avoid overcrowding. Theserecommendations essentially prompt the owners ofaffected farms to apply rearing proceduresintroduced on a large scale into the Swedish pigindustry because of the ban of growth promotersin 1986. They are fairly similar to those used byothers (38), and the efforts to decrease the effectsof PMWS have been based on combating otherinfectious diseases and improve management andhygiene (56). This includes a ban on remixing ofpigs at weaning, a ban of downloading of pigs toconsecutive batches of weaners and washing anddisinfecting between consecutive batches. Whene-ver practical, weaning on farms is not performedunder five weeks age. After visiting PMWS-affected herds, people (including veterinarians)may only visit other herds after a 12 hour intervaland must have showered and changed clothes com-pletely (56).
Criterions for declaring herds previouslyPMWS-positive or negative at the herd levelHerds previously diagnosed as PMWS-positivemay be declared free from the disease at herd levelif they regain the productivity they had before thedisease outbreak. The losses post weaning in termsof runts, culled and dead piglets must remain atthe pre-PMWS level for at least four monthsbefore it is possible to declare any herd officiallyfree from the disease. However, herds do notautomatically get declared free from PMWS ifthey fulfil these criteria. If the herd veterinarianhas any doubts whatsoever, the herd will remainas PMWS-positive (see figure 3).
RESULTS
Number of herds positive for PMWS duringthe first three years with the diseaseThe first year with PMWS in Sweden haspreviously been described in detail (62). Aprogeny test station established in March 2002 andlocated several kilometres from the closest pigherd was declared positive for PMWS inDecember 2003. At this time the total prevalenceof poor performing pigs at the test station was4.1%. One year later, 16 herds in four countieshad been declared PMWS positive (Figures 1 and2). A majority of the cases (12 out of 16 = 75 %)were diagnosed in the county of Sickle (Figure 2;county A). One of the PMWS herds was aLandrace nucleus herd that sold pigs to 64 pigletproducing herds and to two sow pools. It isnotable that 55 of the 64 piglet producing herdsstill were free from PMWS by the last ofDecember 2006. Further, 36 out of the totally 42satellite herds in the two sow pools were aslo freefrom PMWS at that time.
During the second year (2005) of the disease inSweden, another 25 herds were declared PMWSpositive, resulting in a two-year-accumulated totalof 41 positive herds, and the disease was presentin 7 counties of Sweden (Figures 1 and 2). Thedisease was still dominating in Sickle with 58% ofthe accumulated cases, but by year two the diseasewas also evident in Hal land (Figure 2, county F;15% of the cases) and ostergotland (Figure 2,county D; 12% of the cases).
During the third year (2006), 82 new herds weredeclared PMWS positive, leading to a three-year-accumulated total of 123 cases (Figure 1). VästraGötaland (Figure 2, county G) which had its firstcase of PMWS during the second half of 2005now had 24 accumulated cases of PMWS. Thedisease continued to spread northbound by the endof year three PMWS was present in 10 counties,including one of the- northern counties (Figure 2,Table 1).
In February to April in 2006 (year 3), the SwedishAnimal Health Service made an inventory of pigproducers in the PMWS non affected region northof Stockholm (Figure 2, counties J and K). Intotal, 9 piglet producing or integrated herds withmore than 160 sows and 6 satellites belonging totwo different sow pools were scrutinised. Necrop-sies were performed on 63 pigs aged 9-14 weeks
from these 15 apparently healthy herds. The crite-
rions for PMWS was fulfilled in 5 individual pigs
emanating from two herds. One month later, one
of these herds was suspected of having PMWS at
the herd level and later declared PMWS positive
with a merged incidence of runts, culled and dead
piglets of 4.5% post weaning. The other herd has
not, to date, been declared PMWS positive at the
herd level although it is now 15 months since the
investigation was performed (34). None of the pig
herds north of Stockholm, first diagnosed as
having PMWS in 2006, had any contact with herds
previously diagnosed as PMWS positive in other
parts of Sweden. However, the herd in the north
had purchased pigs from a multiplying herd
suspected of having PMWS in 2004 but never
diagnosed as PMWS at the herd level (8).
PMWS in relation to geographic area of
SwedenAs mentioned above PMWS has spread fromSouth to North in Sweden. More than 40% of the
accumulated cases of PMWS have been diagnosed
in Sickle (Figure 2, county A). However, it should
be noted that although the disease in Sweden
appears to have spread from there, 30% of thedomestic sows in Sweden are located in Sickle.
Table 1 shows the relative risk of being affected
by PMWS during the first three years of theoutbreak of disease in Sweden with PMWS corre-
lated to county and number of sows. Herds in
counties with high density of sows and affected
early by PMWS still have a high risk ratio, but the
increased speed in spread of disease is also
elucidated in other counties with many sows.PMWS was not diagnosed in Västra Götaland until
the end of 2005, but the odds ratio to be diagnosed
with PMWS in that county was higher than 1 by
the end of 2006. The high risk ratio obtained in
Värmland might be slightly misleading. This
county has comparably few sows and three of the
five PMWS positive herds were satellites in the
same sow pool. As seen in Table 1, the losses
induced by PMWS are fairly similar all over
Sweden.
Losses over timeIn the three years from the initial herd case of
PMWS was detected in Sweden the disease has
spread around the country, and it has been
possible to examine and document the losses due
to PMWS over time. As seen in Table 2, the
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overall percentage of runts, culled and dead pigsin affected herds has been 7.4 ± 3.2 % at the timepoint when the herds were diagnosed for PMWS.Although differences in losses between individualherds have been observed, the mean losses haveremained at the same level over time.When applying the criteria outlined within thePCVD research program of the sixth framework ofEU (67), 4% corresponds to the minor lossesduring the minimal losses during the post weaningperiod required for PMWS at the herd level inSweden. It should be noted that 1 out of the 24(4%) and 7 out of the 82 (9%) herds diagnosed forPMWS at the herd level during 2005 and 2006,respectively, had losses below this level during thepost weaning period when reported (range1-3.3%).
Herd categoriesIn Sweden, PMWS is more frequently diagnosedin sow pool satellites and integrated herds than inother production systems (Table 3). Furthermore,PMWS is more frequently diagnosed in herdsproducing breeding stock than in piglet producingherds. Fattening herds have only rarely beenofficially considered positive for PMWS. Thelosses due to PMWS in the different categories ofherds have been similar (Table 3).
Correlation to herd sizePMWS was diagnosed three times more often inherds with more than 100 sows compared to herdswith 50-100 sows, which in turn had PMWS 20times more frequently than herds with less than 50sows (Table 4). No obvious differences betweendifferent size segments above 100 sows wererecorded. However, the number of herds inSweden with more than 500 sows is limited.Only 6 specialised fattening herds have beenofficially declared PMWS positive at the herdlevel. They all had more than 500 stalls (n=721;5/721=0.8%), and their sizes ranged from 600 to5,000 stalls.
PMWS in sow pool satellitesThe production cycles of the 42 sow pool satellitesdiagnosed as PMWS-positive is shown in detail inTable 5. As seen in that table, PMWS has beendiagnosed more frequently in herds withintensified systems than in satellites performing theinitial production cycle of 16 weeks.
Satellites with 16 weeks between consecutive
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batches of farrowing sows empty themselvescompletely between every batch. It is notable thatonly one of these satellites has been declaredPMWS positive (Table 5).
PMWS in Sweden and factors other thanPCV2At least one additional disease scenario ofsignificance than PMWS was recorded in 45 of the123 herds (37%) diagnosed as PMWS positive.These diseases were dominated by Lawsoniaintracelluralis (n=22, 18%), followed by respira-tory infections induced by either Mycoplasmahyopneumoniae or Actinobacillus pleuropneumo-niae (n=12, 10%). Eight herds (6%) were affec-ted by Brachyspira spp and another 8 herds (6%)suffered from E. coli-related diseases (postweaning diarrhoea or oedema disease). Highamounts of mycotoxins were found in the feed ofone affected herd.
In general, production was good in the PMWSpositive herds, and no other disease was regardedas significant in the remaining 78 herds that werePMWS positive. However, it should be noted thatmanagement errors were recorded in all affectedherds. They varied from obvious to scarcelydetectable errors, but they were always there.
Effect of treatments with antimicrobials inherds suspected for PMWSGroup treatment with oral antibiotics was used in73 of the 123 PMWS positive herds (Table 6). In33 of these 73 herds, diseases other than PMWSwere diagnosed and judged to be of significantimpact (Lawsonia intracelluralis in 18 herds,Respiratory problems induced by Mycoplasma hyo-pneumoniae or Actinobacillus pleuropneumoniae in9 herds, E. coil-related diseases in terms of postweaning diarrhoea or oedema disease in 8 herds,and Brachyspira pilosicoli in 4 herds - 6 of theherds had two of these diagnoses). The clinicaleffect of oral antibiotic treatments was judged asgood or at least observable in 26 out of these 33herds (79%). In contrast, group treatments wereunsuccessful in 26 out of 40 herds (65%) withoutother significant problems than PMWS (p <0.001,Fischers exact test).
Whenever an individual pig fulfil the demands ofPMWS at necropsy the herd becomes a suspectedherd case of the disease. To date, 52 herds withindividual pigs diagnosed as PMWS positive have
not progressed to diagnosis of PMWS at a herdlevel. On these herds, losses during the postweaning period decreased from a mean incidenceof runts, culled and dead pigs of 5.2±3.8% atsuspicion to 2.0+1.2% when confirmed PMWS-negative (p <0.001, t-test; Table 7). In all 52herds, corrections in management were performed.Group treatments with antibiotics were effective in27 out of 30 of these herds (Table 6) that also hadother problems (Lawsonia intracelluralis; n = 13,respiratory problems; n=8, E. co/i-related disea-ses; n=8, Brachyspira pilosicoli; n=5, or Isospo-ra suis; n=1).
Number of PMWS positive herds laterdeclared free from the diseaseThe criterions applied to regain freedom fromdisease includes a "normal production" during thepost weaning period for at least four months, andpigs sold to fattening enterprises should notdevelop PMWS in these enterprises. Due to thelatter, piglet producers deemed for PMWS thathave regained a fair production since long maystill be officially considered as PMWS positive, aselucidated by Figure 3. However, the exactnumber of such herds is unknown, because thesystematic collection of data at a national level hasonly included losses when herds have beensuspected, deemed or declared free from PMWS.
By the early 2007, 30 out of a total of 123 herds(25%) positive for PMWS prior to 2007 hadofficially been declared free from the disease atherd level. When declared free, the mergedincidence of runts, culled and dead pigs in theseherds had decreased from 7.3 + 27% to 2.3 +1.2% (p < 0.001, t-test), which corresponded tothe production pre-PMWS (Table 7).
DISCUSSION
This manuscript outlines the development ofPMWS from an exotic disease in Sweden to anendemic disease over a three-year period. Thisoccurred despite early recognition and diagnose ofthe index case in 2003, and the substantial effortsof the Swedish authorities and the producers tocombat the disease. The disease has spread fromthe south of Sweden to the north. The spread ofthe disease was initially slow, but accelerated asthe number of infected herds increased. As PMWSis a contagious disease (30) this might indicateincreasing difficulties to separate pigs from healthy
129
herds from PMWS-affected herds during transpor-
tations. The losses due to PMWS in Sweden have
been low in comparison to what has been reported
from elsewhere and also fairly constant over time.
This is possibly due to the general high health
status of the pig industry. The intention of most
producers in Sweden is to effectuate age
segregated rearing systems, and the herds are free
from certain severe diseases such as PRRS and
AD. It is notable that the PMWS-affected herds in
general had a high productivity prior to PMWS.
However, it is also notable that management errors
in some way have constantly been apparent in the
PMWS-positive herds in Sweden.
From the data obtained to date, the Swedish
authorities have concluded that PMWS probably
did not exist in Sweden prior to the index case,
which was diagnosed in a newly established pig
progeny test station (62). The test station was a
dead end with respect to spread of the disease with
no movements of pigs from this station, however,
the rearing strategy on this station was extreme in
comparison to general Swedish conditions (62). It
is probable that the presence of PCV2 in pigs in
Sweden (65,35,44) and the stressors applied to the
pigs at this new testing station together with the
mixed pathogen load of the nucleus herds was
enough to induce PMWS.
The nucleus herd diagnosed as PMWS positive
four months after the index case at the testing
station (62) may in fact have been the first case of
PMWS in Sweden and it is possible that pigs from
this herd may have triggered the disease at the test
station. Pigs from this herd had the highest
incidence of PMWS at the test station before it
was closed down (9). This nucleus herd mayactually have been the true index case, but with
losses below the level required for herd diagnosis,
and thereby undiagnosed for some time. Perhaps
the disease was first identified at the station
because pigs were subjected to stressors (and
maybe also infections) not present on the nucleus
farm at the test station.
If this was the case, this could also explain why
only 2 out of 66 herds (or out of 108 herds ifincluding the sow pool satellite herds) purchasing
pigs from the nucleus herd were diagnosed for
PMWS during inspections carried out in March2004, and also why another four of them were
declared PMWS positive by December that year
(62). The effect of stressors in potentiating PMWS
on these four farms supplied by the nucleus herd isfurther underlined by the fact that the offspring to150 pregnant gilts of the nucleus herd thatfarrowed offsite in 2004 and were reared in
facilities not regularly used for pig production didnot show any signs of PMWS, and had a mortalityrate post weaning of 0.7% (62).
The effect of newly introduced stressors to
susceptible pigs may also explain why certainfattening herds develop PMWS and other remainhealthy despite the fact that they purchase pigsfrom the same piglet producer (62), and in thiscontext PMWS obviously shares an aetiologynature with atrophic rhinitis (11,65) and swinedysentery (18,23,39,48,49,59). Atrophic rhinitisand swine dysentery are two severe porcine disea-ses whose clinical expressions are dependant oninfection with the causal microbe and other fac-tors, such as other infections and a suboptimalenvironment for development of fulminate clinicaldisease. Seen from this view, more focus shouldbe placed on the conditions in the fattening herdrather than in the piglet producing herd.
Currently the declarations of freedom from PMWSappear to be delayed in Swedish piglet producingherds, despite that the criterions for freedom havebeen fulfilled on some of them. For instance, theherd in Figure 3 was not declared free fromPMWS, because pigs moving from this herd to afattening unit consistently broke down withPMWS. It is debatable as to whether the pigletproducer or the fattening unit should be declaredas PMWS-positive as diseased pigs are only seenon the fattening herd. However, Figure 3 alsoshows the complexity of PMWS. Batch 73unexpectedly revealed losses of 6.6%, sevenmonths since the losses exceeded 4% the last time.
It appears odd that only 6 specialised fatteningherds in Sweden have been officially declaredPMWS positive. Weaners are moved to the fatte-ning herds at around 9-12 weeks of age so certain-ly they can still be affected by PMWS (2,54).However, the focus has been on the pigletproducers. Fattening enterprises buying fromPMWS-affected herds have generally not beendeclared PMWS positive since they empty themsel-ves after each batch. However, more attentionought be paid to the fatteners, not least since thelosses become more pronounced when fatteners areaffected by PMWS. In Sweden, the mortality dueto PMWS is equal in fattening herds to that seen
PCV2 may be shed by semen (26,32), and the useof artificial insemination and importation of semenonto farms has been suggested to be involved inthe spread of PMWS. As artificial inseminationseffectuate over 90% of the matings in Sweden, andsemen from up to six boars may be mixed in eachbatch for production of the terminal breeds (H xY-L or D x Y-L) all herds of importance in thecountry have been constantly exposed to any agentspread through semen since the initial outbreak ofPMWS. A large number of these herds (92% ofthe herds with more than 50 sows) have remainedfree of PMWS. Consequently, there is no evidenceto support the spread of a highly contagious agentin Sweden via semen that is contributing todevelopment and spread of PMWS.
Further, the comparable low risk for spread ofPCV2 via semen has recently been elucidated inScandinavia due to export of semen from Swedento Norway. All doses exported are from individualboars, and they are controlled by real time PCRfor presence of PCV2. So far, ejaculates from 54Swedish boars aged 10 to 24 months have beentested, and PCV2 has not been demonstrated inany of them (to be published). This concurs withresults from a Canadian boar station were PCV2was only demonstrated in 27 out of 903 ejaculates(3%), and never from boars older than 68 weeks(40).
in the post weaning period, but the mean losses foreach dead fattener corresponds to EUR 75 compa-red to EUR 52 for each dead weaner (60).
In Sweden, PMWS may have been under-diagnosed in pure piglet producing herds as only1.6% of these herds have been declared positivefor the disease compared to 8.9% of the integratedherds. Possibly this reflects that the latter categoryrear their own pigs to market weight, and in thissystem PMWS does not interfere with logistics interms of problems to sell the growers to otherherds.
130
The incidence of PMWS in Sweden clearly mat-ches the intensity of the pig production. However,from Table 2 it is evident that very small herdscan also be affected by PMWS, but herds withmore than 100 sows and sow pool satellites withintensified systems are more likely to be diagnosedas PMWS-positive herds. PMWS is seldom diag-nosed in herds with less than 50 sows. This mayexplain the recent finding in Norway, where noevidence of PMWS was found in undersizedweaners from 29 pig herds at necropsies perfor-med in 2006 (41). Traditionally, almost all herdsin Norway have had less than 50 sows and mostherd still have less than 70 sows (36). Interestinglythe two herds that were diagnosed for PMWS inNorway during 2003 and later stamped out inclu-ded a small herd with a long history of healthproblems and a recently established herd with 180sows performing early weaning in a continuousproduction system and suffering from overcrow-ding (10). The herd sizes will certainly notdecrease in Sweden, but it is notable thatPMWS-affected sow pool satellites have regainedhealth by returning to less intensive rearingsystems (61).
Other diseases and microbial infections cancontribute to development of PMWS (52,14,58)and losses due to PMWS on some farms canreduce significantly if these other diseases andinfections are combated successfully (38,62). InSweden, group treatments with oral antibioticshave in general been effective when other diseaseswere present, especially in herds suspected forPMWS but never diagnosed on herd basis. In theseherds, the signs of PMWS faded away as the otherinfections were controlled. In contrast, grouptreatments with antibiotics were never successful ifPMWS was the only diagnose of significance inthe herd.
CONCLUDING REMARKS
It appears from the results generated to date, thatPMWS in Sweden is of indigenous origin, but theauthorities have not determined why the diseaseaffected Sweden when it did, nor why it isspreading. In general there are no clear linksbetween affected herds but it is notable thatwhenever PMWS has been diagnosed on a herdlevel management errors or short to non existingempty time between consecutive batches on thefarms has constantly been noted. Producers inSweden have again Jearned that strict batch wiseproduction with proper empty times between bat-ches is valuable, and that downloading of pigs ispotentially dangerous (38,37,62). The data genera-ted in Sweden shows that piglets weaned at ayounger age are more often affected by PMWSbecause weaning take place at a specific day inbatchwise farrowing systems. This means that theyoungest piglets in a batch will be weaned appro-ximately one week younger than the eldest pigs ofthe batch. Obviously the "immunological window"from weaning until the pigs have gained a suffi-
,
.
cient immune system is of importance when the
ubiquitarious PCV2 is super activated. Could the
fact that piglets are weaned and allocated at
constantly younger ages have had an impact on the
development of PMWS? The modern farmed piglet
is weaned abruptly with an instant switch from
milk to cereals, which leads to a disturbance of the
intestinal flora (25). Further, the weaning age has
decreased, leading to less mature pigs at weaning.
Twenty years ago, piglets in Sweden were weaned
at 6-7 weeks of age. Pigs of today may weight 25
125
100
75
50
25
131
kg at the age of eight weeks. Today piglets areweaned at 4-5 weeks of age in Sweden, and evenearlier in many other countries. The offspring tosows in their natural habitat are finally weaned atthe age of four months following a gradual processand adaptation to other feed ingredients than milk(24). Does the P in PMWS really stand for Post-weaning? Taking porcine physiology into accountit should perhaps instead be Pre-weaning, eventhough the pigs are actually weaned.
Accumulated cases of PMWS in Sweden
0 6'
2003Dec 2004Dec 2005Dec 2006Dec
Figure 1. Accumulated cases of PMWS in Sweden from the index case diagno-
sed in December 2003 until last December in 2006, i.e. during the first threeyears with the disease.
2004-12-31n = 16
N
2005-12-31 2006-12-31n = 41 n = 123
Figure 2. Geographical localisation of the accumulated cases of PMWS in Sweden by the end ofthe years 2004, 2005 and 2006. Counties mentioned in Table 1 and in the text are visualised bycapitals in the map to the far left.
_
1
2,
16
14
12
10
8
6
4
2
132
CD CO CDCV CO CO .4-
Batch
rc;CO a-- (30 a- CD a-CD IN- N- CO CO CS) 0)
Figure 3. Batchwise mortality post weaning in the first conventional herd deemed forPMWS in Sweden. The 650 sow herd was established in April 2003 (Batch 1) andfarrowing takes place every second week. The herd was diagnosed for PMWS inJanuary 2004 (Batch 19, arrow), and the figure shows batches weaned from establish-ment until April 2007 (Batch 105). Open symbols show the incidence of culled pigletspost weaning, and filled symbols show the total mortality. The post weaning lossessince January 2005 (Batch 44-105, n=61) is 2.3 + 1.3% and 1.5 ± 0.6% during thelast 12 months (n=26), respectively. However, the herd is still not officially declaredfree from PMWS.
CountyPMWS Sows
Riskratio
Losses(cases) (% of
the cases)% of the
populationMean Range
A Slane 55 43.1 30.8 1.41 7.5 ± 3.2 3 16B Blekinge 1 0.8 1.1 0.73 4.0C Smfiland & Oland 5 4.1 7.9 0.52 6.7 ± 3.4, 4 12D Ostergotland 11 8.9 6.4 1.39 7.5 ± 2.1 4 10E Sodermanland 1 0.8 4.9 0.16 8.0F Halland 20 16.3 11.6 1.41 6.9 ± 2.2 3 10G Västra Götaland 24 19.5 17.9 1.09 7.3 ± 3,9 1 15H Wirmland 5 4.1 2.4 1.71 7.6 ± 2.1 4 10I Närke 2.3J Vastmanland 2 1.6 4.5 0.36 9.8+7.4 4.5 15K Uppland 3.3L Gotland 3.5
Northern counties 1 0.8 3.3 0.24 4.0
Table I. The number of accumulated cases of PMWS during the first three years with the disea-se in Sweden, and the risk ratio for being deemed for PMWS from a geographical point of view.The capitals that precede each county are visualised in the map to the far left in Figure 2.
Number herds deemed Losses post weaning (%)ofMean Range
2003 1 4.1 4.12004 15 8.4 ± 3.3 4 14.62005 25 7.3 ± 2.4 3 12.62006 82 7.2 ± 3.4 1 - 16
Overall 123 7.4 3.2 1 16
Table 2. Overall losses in terms of the merged incidence of runts, culled and dead pigs in herdsat the time point when they were diagnosed positive for PMWS during the first three years withthe disease in Sweden.
>.
o2
C7,
9v uort,--31ib cc Ao0 0 CO ci§b cc), 9Cb
C511111111,1111111IflarrtrUr5Ibr,o0%. ect:1- Gap.0- (.0
LO
± -
0 0op 0
-
-
-" .1y1
-
-
-
,
133
Category
Within category Deemed herds within category
Deemed(n)
Total Deemed(n) (%)
Sizes Losses(%, mean)
Losses(%, ran
Nucleus ormultipliers
5 100 5.0 100 378 sows 8.4 ± 2.7 5 12
Pigletproducers
32 1,965 1.6 10 1,050 sows 7.4 ± 3.3 4 16
Integrated 37 418 8.9 24 1,100 sows 7.4 ± 3.1 3 15
Fatteningherds
6 2,475 0.2 600 5,000 stalls 6.3 ± 2.3 3 10
Sow poolsatellites
42 284 14.8 35 590 sows* 7.4 ± 3.5 1 15
*Adjusted number of sows based on the number of farrowings per year
Table 3. The percentages of Swedish pig herds diagnosed PMWS positive during the first three years with the disea-
se within different herd categories. Also the losses due to PMWS within the different categories of herds are shown.
Number of sowsHerds within segment
< 501,597
50 - 100459
101 - 500382
501-100023
1000
22
Herds deemed for PMWSPiglet producers 2 9 19 1 1
Integrated herds 1 10 22 2 2
Breeding herds 1 4
TOTAL 3 20 45 3 3
% Deemed 0.2 4.4 11.8 13.0 13.6
Mean losses (%) 5.3 ± 1.5 7.6 ± 3.1 7.7 ± 3.2 6.4 ± 2.3 6.2 ± 3.9
Range for losses (%) 4 - 7 4 - 16 3 - 15 4 8.5 3 10.5
Table 4. The percentages of Swedish sow herds diagnosed as PMWS positive during the first three years with
the disease with respect to size. Also the losses due to PMWS within the different segments are shown.
-
-
134
Weeksbetweenfarrowings
Max theoreticrearing time
to 25 kg
Batchessimultaneouslyat the satellite
Herdswithin
segment
Herdsdeemed % deemed
1 66 84 days 12 3 1 33%2 66 - 84 days 6 7 1 14%3 66 days 4 1 1
6100%
7 77days 2 14 43%
4 84 days 4 35 4 11%5 84 days 5 2 0 0%8 84 days 2 155 26 17%16 84 days 1 66 1 2%
All 284 43 15%
All < 84 days 20 9 45%All 84 days 264 31 12%
Table 5. Rearing strategies for sow pool satellite herds in Sweden diagnosed as PMWS positiveduring the first three years with the disease.
Herd CategoriesEffect of group treatment
SignGood Observable None
Herds diagnosed for PMWS3340
273
12
7
251
(36%)(18%)
(93%)(33%)
147
21
(42%)(18%)
(7%)(33%)
726
1
(21%)(65°))
0
(33%)
p<0.001
p<0.05
With other significant diagnosesNo other diseases recorded
Suspected herds, never deemedWith other significant diagnosesNo other diseases recorded
Table 6. Effect of group treatment with antibiotics in 73 herds diagnosed for PMWS at herd level,and in 30 suspected herds never diagnosed for PMWS at herd level. The table compares effect oftreatment in herds suspected for PMWS alone with the effect in herds also suffering from otherdiseases.
Definition of the herdsLosses post weaning (%)
Range Mean Sigificance
Diagnosed for PMWS (n = 30)When deemed for PMWSWhen declared free
Never deemed for PMWS (n = 52)When suspected for PMWSWhen suspicion was withdrawn
3 15
1 5
0 18
0 6
7.3 ± 2.72.3 + 1.1
5.2 ± 3.82.0 ± 1.2
p<0.001
p<0.001
Table 7. The losses in terms of merged incidence of mortality and runts post weaning in herds whensuspicion finally was withdrawn in comparison to lossess on suspicion or when being deemed.
,
.
-
-
-
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AcknowledgementsThis work includes efforts made by many people apart from the authors. We wish to thank all persons thathave contributed to this work and to all who have allowed us access to information that many times could
be defined as confidential and sensitive. This work was supported by grants from EU, Project No: 513928within the Sixth Framework Programme, from Formas and from the Swedish Farmers Foundation for Agri-
cultural Research. Individual persons within the Swedish Animal Health Service and the National VeterinaryInstitute, SVA also have provided great enthusiasm.
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