Laboratory decision-making during the classical swine fever epidemic of 1997-1998 in The Netherlands

The National Reference Laboratory for classical swine fever (CSF) virus in the Netherlands examined more than two million samples for CSF virus or serum antibody during the CSF epizootic of 1997–1998. The immense amount of samples and the prevalence of border disease (BD) virus and bovine viral diarrhoea (BVD) virus infections in Dutch pig herds necessitated the diagnostic efforts of the laboratory to be focused on generating CSF specific test results throughout the eradication campaign.

Detection of 82% of the 429 outbreaks was achieved through the combined use of a direct immunofluorescence and peroxidase assay (FAT/IPA) with samples (tonsils) collected from clinically-suspected pigs. This suggests that in the majority of the outbreaks, the pigs had clinical signs that were recognised by the farmer and/or veterinarians, indicating the presence of CSF virus in a pig herd. A positive diagnosis of 74% of all the tissue samples (tonsils) collected at infected pig holdings was established by FAT. More than 140,000 heparinised blood samples were examined by virus isolation, resulting in the detection of 4.5% of the infected herds. CSF virus was isolated in approximately 29% of all the blood samples collected from pigs at infected or suspected farms.

Several serological surveys — each done within a different framework — led to the detection of 13.5% of the total number of outbreaks. The detection of CSF virus antibody in serum was carried out by semi-automated blocking ELISA. Approximately 28.5% of the sera which reacted in the ELISA were classified as CSF virus-neutralising antibody positive and 26.5% as positive for other pestiviruses following the virus neutralisation test (VNT).

We concluded that two of the CSF laboratory diagnostic methods described were determinative in the eradication campaign: first, the FAT for the screening of diseased pigs; and second, the ELISA and VNT when millions of predominantly healthy pigs needed to be screened for the presence of CSF serum antibody. Decision-making on the basis of results generated by either method can, however, be seriously hindered when samples are examined from pig herds with a high prevalence of non-CSF pestiviruses.     

The classical swine fever epidemic 1997-1998 in The Netherlands: descriptive epidemiology

The objective of this paper is to describe the severe epidemic of classical swine fever (CSF) in The Netherlands in 1997–1998 under a policy of non-vaccination, intensive surveillance, pre-emptive slaughter and stamping out in an area which has one of the highest pig and herd densities in Europe.

The primary outbreak was detected on 4 February 1997 on a mixed sow and finishing pig herd. A total of 429 outbreaks was observed during the epidemic, and approximately 700 000 pigs from these herds were slaughtered. Among these outbreaks were two artificial insemination centres, which resulted in a CSF-suspect declaration of 1680 pig herds (mainly located in the southern part of The Netherlands). The time between introduction of CSF virus (CSFV) into the country and diagnosis of CSF in the primary outbreak was estimated to be approximately 6 weeks. It is presumed that CSFV was spread from The Netherlands to Italy and Spain via shipment of infected piglets in the beginning of February 1997, before the establishment of a total stand-still of transportation. In June 1997, CSFV is presumed to be introduced into Belgium from The Netherlands.

Pre-emptive slaughter of herds that had been in contact with infected herds or were located in close vicinity of infected herds, was carried out around the first two outbreaks. However, this policy was not further exercised till mid-April 1997, when pre-emptive slaughter became a standard operational procedure for the rest of the epidemic. In total, 1286 pig herds were pre-emptively slaughtered. (approximately 1.1 million pigs). A total of 44 outbreaks (10%) was detected via pre-emptive slaughter.

When there were clinical signs, the observed symptoms in infected herds were mainly atypical: fever, apathy, ataxia or a combination of these signs. In 322 out of 429 outbreaks (75%), detection was bases on clinical signs observed: 32% was detected by the farmer, 25% by the veterinary practitioner, 10% of the outbreaks by tracing teams and 8% by screening teams of the veterinary authorities. In 76% of the outbreaks detected by clinical signs, the farmer reported to have seen clinical symptoms for less than 1 week before diagnosis, in 22% for 1–4 weeks before diagnosis, and in 4 herds (1%) the farmer reported to have seen clinical symptoms for more than 4 weeks before diagnosis.

Transportation lorries played a major role in the transmission of CSFV before the primary outbreak was diagnosed. It is estimated that approximately 39 herds were already infected before the first measures of the eradication campaign came into force.

After the first measures to stop the spread of CSFV had been implemented, the distribution of the most likely routes of transmission markedly changed. In most outbreaks, a neighbourhood infection was indicated.

Basically, there were two reasons for this catastrophe. Firstly, there was the extent of the period between introduction of the virus in the region and detection of the first outbreak. As a result, CSFV had opportunities to spread from one herd to another during this period. Secondly, the measures initially taken did not prove sufficient in the swine- and herd-dense region involved.     

The 1997-1998 classical swine fever epidemic in The Netherlands--a survival analysis

The aim of this analysis was to characterise the temporal pattern of infection during the 1997/98 classical swine fever (CSF) epidemic in The Netherlands and hence identify and quantify risk factors for infection in different enterprise types and areas. Survival analysis and Cox proportional hazards regression were used to describe the epidemic. Substantial differences in temporal survival patterns (herd breakdown rate) were found between areas where different control policies operated. Factors with a significant influence on the infection hazard of individual herds included: sow numbers as a percentage of total sows and fatteners (HR = 3.38 for mixed herds (0.1–60% sows) vs. fattening herds (0% sows) and HR = 2.74 for breeding herds (60–100% sows) vs. fattening herds), the number of ‘transport contacts per month’ (>0.3 vs. <0.3; HR = 4.11), pig density (pigs/km²) in the area (HR_{1000 pigs} 1.48) and herd size (HR_{100 pigs} = 1.01).

Pre-emptive slaughter in an area appeared to be associated with lower subsequent disease levels. Higher frequency of transport contacts for welfare slaughter during the epidemic, however, well regulated and controlled, was associated with a substantially higher risk of becoming infected. The positive association of a higher pig density with CSF indicates the potential importance of local spread as a factor in disease transmission and emphasizes that dilution of the pig population can contribute to reduction in CSF occurrence. This analysis suggests however, that if pre-emptive slaughter can promptly be applied effectively in an area after initial diagnosis, pig density is then not a significant factor. Mixed and breeding herds had a higher probability of becoming infected than fattening herds, possibly due to different types and frequencies of inter-herd contacts. These contacts continue to some extent during the epidemic, despite the standstill of animal movements.     

Transmission of classical swine fever virus within herds during the 1997-1998 epidemic in The Netherlands

In this paper, we describe the transmission of Classical Swine Fever virus (CSF virus) within herds during the 1997–1998 epidemic in the Netherlands. In seven herds where the infection started among individually housed breeding stock, all breeding pigs had been tested for antibodies to CSF virus shortly before depopulation. Based upon these data, the transmission of CSF virus between pigs was described as exponential growth in time with a parameter r, that was estimated at 0.108 (95% confidence interval (95% CI) 0.060–0.156). The accompanying per-generation transmission (expressed as the basic reproduction ratio, R₀) was estimated at 2.9. Based upon this characterisation, a calculation method was derived with which serological findings at depopulation can be used to calculate the period in which the virus was with a certain probability introduced into that breeding stock. This model was used to estimate the period when the virus had been introduced into 34 herds where the infection started in the breeding section. Of these herds, only a single contact with a herd previously infected had been traced. However, in contrast with the seven previously mentioned herds, only a sample of the breeding pigs had been tested before depopulation (as was the common procedure during the epidemic). The observed number of days between the single contact with an infected herd and the day of sampling of these 34 herds fitted well in the model. Thus, we concluded that the model and transmission parameter was in agreement with the transmission between breeding pigs in these herds.

Because of the limited sample size and because it was usually unknown in which specific pen the infection started, we were unable to estimate transmission parameters for weaned piglets and finishing pigs from the data collected during the epidemic. However, from the results of controlled experiments in which R₀ was estimated as 81 between weaned piglets and 14 between heavy finishing pigs (Laevens et al., 1998a. Vet. Quart. 20, 41–45; Laevens et al., 1999. Ph.D. Thesis), we constructed a simple model to describe the transmission of CSF virus in compartments (rooms) housing finishing pigs and weaned piglets. From the number of pens per compartment, the number of pigs per pen, the numbers of pigs tested for antibodies to CSF virus and the distribution of the seropositive pigs in the compartment, this model gives again a period in which the virus most probably entered the herd. Using the findings in 41 herds where the infection started in the section of the finishers or weaned piglets of the age of 8 weeks or older, and of which only a single contact with a herd previously infected was known, there was no reason to reject the model. Thus, we concluded that the transmission between weaned piglets and finishing pigs during the epidemic was not significantly different from the transmission observed in the experiments.     

The 1997-1998 epidemic of classical swine fever in the Netherlands

In 1997, the pig husbandry in the Netherlands was struck by a severe epidemic of classical swine fever (CSF). During this epidemic 429 CSF-infected herds were depopulated and approximately 1300 herds were slaughtered pre-emptively. In addition millions of pigs of herds not CSF-infected were killed for welfare reasons (over crowding or overweight). In this paper, we describe the course of the epidemic and the measures that were taken to control it.The first outbreak was detected on 4 February 1997 in the pig dense south-eastern part of the Netherlands. We estimate that CSF virus (CSFV) had already been present in the country by that time for 5-7 weeks and that the virus had been introduced into approximately 39 herds before the eradication campaign started. This campaign consisted of stamping-out infected herds, movement restrictions and efforts to diagnose infected herds as soon as possible. However, despite these measures the rate at which new outbreaks were detected continued to rise. The epidemic faded out only upon the implementation of additional measures such as rapid pre-emptive slaughter of herds in contact with or located near infected herds, increased hygienic measures, biweekly screening of all herds by veterinary practitioners, and reduction of the transportation movements for welfare reasons. The last infected herd was depopulated on 6 March 1998.     

Cost-effectiveness of measures to prevent classical swine fever introduction into The Netherlands

Recent history has demonstrated that classical swine fever (CSF) epidemics can incur high economic losses, especially for exporting countries that have densely populated pig areas and apply a strategy of non-vaccination, such as The Netherlands. Introduction of CSF virus (CSFV) remains a continuing threat to the pig production sector in The Netherlands. Reducing the annual probability of CSFV introduction (P_CSFV) by preventive measures is therefore of utmost importance. The choice of preventive measures depends not only on the achieved reduction of the annual P_CSFV, but also on the expenditures required for implementing these measures. The objective of this study was to explore the cost-effectiveness of tactical measures aimed at the prevention of CSFV introduction into The Netherlands. For this purpose for each measure (i) model calculations were performed with a scenario tree model for CSFV introduction and (ii) its annual cost was estimated. The cost-effectiveness was then determined as the reduction of the annual P_CSFV achieved by each preventive measure (ΔP) divided by the annual cost of implementing that measure (ΔC). The measures analysed reduce the P_CSFV caused by import or export of pigs. Results showed that separation of national and international transport of pigs is the most cost-effective measure, especially when risk aversion is assumed. Although testing piglets and breeding pigs by a quick and reliable PCR also had a high cost-effectiveness ratio, this measure is not attractive due to the high cost per pig imported. Besides, implementing such a measure is not allowed under current EU law, as it is trade restrictive.     

Quantification of the transmission of classical swine fever virus between herds during the 1997-1998 epidemic in The Netherlands

In this study, we describe a method to quantify the transmission of Classical Swine Fever Virus (CSFV) between herds from data collected during the 1997–1998 epidemic in the Netherlands. From the contacts between infected herds and the serological findings shortly before depopulation, we estimated the week of virus introduction and the length of the period over which the herd emitted virus for each CSFV-infected herd. From these data, we estimated the infection-rate parameter β (the average number of herds infected by one infectious herd during one week) and the herd reproduction ratio, R_h (the average total number of secondary outbreaks caused by one infectious herd, i.e. in its entire infectious period), using a SIR-model for different sets of CSF control measures. When R_h > 1, an epidemic continues to grow. On the other hand, when R_h < 1 an epidemic will fade out.

During the phase before the first outbreak was diagnosed and no specific measures had been implemented, β was estimated at 1.09 and R_h at 6.8. In the subsequent phase infected herds were depopulated, movement restrictions were implemented, infected herds were traced forward and backward and the herds in the protection and surveillance zones were clinically inspected by the veterinary authorities (regional screening). This set of measures significantly reduced β to 0.38. However, R_h was 1.3 and thus still >1. Consequently, the number of outbreaks continued to grow. After a number of additional measures were implemented, the value of R_h was reduced to 0.5 and the epidemic came to an end. These measures included pre-emptive slaughter of herds that had been in contact with infected herds or were located near an infected herd, increased hygienic procedures, replacement of transports of pigs for welfare reasons by killing of young piglets and a breeding ban, and regional screening for CSF-infected herds by local veterinary practitioners.     

Classical swine fever in The Netherlands 1997-1998: a description of organisation and measures to eradicate the disease

The central and regional organisation of the campaign to eradicate the CSF epidemic in the Netherlands in 1997/1998 is described. The main instruments used in the campaign were based on stamping-out and movement restrictions specified by the European Union. Additional instruments were used for the first time, namely, pre-emptive culling of contact and neighbouring farms, compartmentalisation of transport, monthly serological screening in established surveillance areas and supervised repopulation of all farms in the former surveillance zone. Two other measures, the killing of very young piglets and a breeding ban were introduced to reduce production in established surveillance zones. Several factors complicated the eradication campaign, for instance, the late detection of the first infection; artificial insemination as a source of infection; the organisation of pig farming in the Netherlands, with its highly concentrated production and dependence on the transport of stock from one unit to another; insufficient rendering capacity; decreasing sensitivity of clinical inspection; and extremely high costs.     

种猪场猪瘟和伪狂犬病净化策略浅析

猪瘟和伪狂犬病作为两种不同类别的重要动物疫病在我国种猪场仍普遍存在,直接或间接影响着种猪行业的健康发展。近年来,随着猪瘟和伪狂犬病的综合防控措施及诊断技术的不断突破与革新,为猪瘟和伪狂犬病的净化工作奠定了基础,同时两病净化作为一项重要项目前已被列入国家中长期动物疫病防治规划。本文结合监测技术同疫病防控,旨为种猪场猪瘟和伪狂犬病的净化提供相适应的技术路线。     

猪瘟诊断方法的研究进展

猪瘟是由猪瘟病毒引起的一种急性、发热性、接触性传染病,可引起各种年龄猪发病。随着对猪瘟病毒研究的深入,猪瘟在一定程度上得到了有效控制。但是近年来,世界各国流行的猪瘟在流行病学、临床症状和病理变化等方面出现了一些新的变化,猪瘟的防控出现了许多新的情况。我国猪瘟的发病率亦呈上升趋势,严重威胁着我国养猪业的发展,给养猪业造成了极大的经济损失。因此,建立准确的实验室诊断方法,对于预防和控制猪瘟有重要意义。本文综述了猪瘟诊断技术方面的研究进展,为猪瘟的及时诊断提供参考。     

Laboratory experience during the classical swine fever virus epizootic in the Netherlands in 1997-1998

From February 1997 till May 1998 the national reference laboratory for classical swine fever (CSF) in the Netherlands was confronted with millions of samples taken from pigs during an outbreak of CSF in a pig dense region. In a limited period major logistic problems needed to be solved regarding the processing of samples and information at the laboratory facilities.In total over 2.3 million samples were examined by different CSF diagnostic methods. The majority (approximately 2.1 million) of these samples were blood samples which were tested for CSF serum antibody in a semi-automated ELISA. Approximately 166,000 samples were examined for the presence of CSF virus or viral antigen. Automated preparation and testing of blood samples for CSF serum antibody, the obligatory identification and registration system of pig holdings and the computerised laboratory management system made it possible to process the huge amount of samples and information presented in a limited period. The majority of the test results was sent to the veterinary authorities via e-mail or a computerised fax system.Of the 429 outbreaks 82% were detected via a direct immunofluorescence technique performed on cryostat sections of the tonsil. The sampling of clinically suspected pigs ('guided' sampling) for this diagnostic method provided rapid positive and negative results and thus played a paramount role during the eradication campaign. Serological surveys identified 13.5% of the infected pig holdings: such surveys proved very effective in the screening of holdings which were subjected to restrictions (protection or surveillance zones) for many months. Virus isolation performed on different types of samples detected 4. 5% of the infected pig holdings.In conclusion, analysis of data collected in the laboratory and epidemiological analysis should result in an improved eradication plan for the future control of outbreaks of CSF in the Netherlands supported by optimised CSF diagnostic methods.     

泉州市洛江区猪瘟抗体水平检测效果分析

结合实验室每年的检测工作,2013-2014年对洛江区辖区内20个生猪规模养殖场和89个散养户的856份猪血清进行猪瘟疫苗免疫抗体检测。结果表明:洛江区猪瘟疫苗免疫抗体合格率呈现上升趋势,规模场猪瘟疫苗免疫抗体合格率明显高于散养户,免疫2次的抗体合格率明显高于1次。抗体检测工作的开展,对制定科学合理的免疫程序,有效防控猪瘟疫情的发生发挥了积极的作用。     

河源某猪场两种猪瘟疫苗田间免疫效果对比试验

通过在河源某猪场,对不同厂家两种猪瘟疫苗单独使用及混合使用后的的免疫效果对比,得出以下结论：首免和二免均使用猪瘟传代细胞苗免疫的效果最好;首免使用猪瘟脾淋苗,二免使用猪瘟传代细胞苗免疫的效果次之;首免和二免均使用脾淋苗免疫的效果最差。     

A multiplex RT-PCR assay for the rapid and differential diagnosis of classical swine fever and other pestivirus infections

Classical swine fever is a highly contagious viral disease causing severe economic losses in pig production almost worldwide. All pestivirus species can infect pigs, therefore accurate and rapid pestivirus detection and differentiation is of great importance to assure control measures in swine farming. Here we describe the development and evaluation of a novel multiplex, highly sensitive and specific RT-PCR for the simultaneous detection and rapid differentiation between CSFV and other pestivirus infections in swine. The universal and differential detection was based on primers designed to amplify a fragment of the 5′ non-coding genome region for the detection of pestiviruses and a fragment of the NS5B gene for the detection of classical swine fever virus. The assay proved to be specific when different pestivirus strains from swine and ruminants were evaluated. The analytical sensitivity was estimated to be as little as 0.89 TCID₅₀. The assay analysis of 30 tissue homogenate samples from naturally infected and non-CSF infected animals and 40 standard serum samples evaluated as part of two European Inter-laboratory Comparison Tests conducted by the European Community Reference Laboratory, Hanover, Germany proved that the multiplex RT-PCR method provides a rapid, highly sensitive, and cost-effective laboratory diagnosis for classical swine fever and other pestivirus infections in swine.     

Transmission of classical swine fever virus by artificial insemination during the 1997-1998 epidemic in The Netherlands: a descriptive epidemiological study

In the course of the 1997-1998 CSF epidemic in the Netherlands, two semen collection centres (SCC) became infected. As an eradication strategy for an acute crisis situation, it was concluded that all semen of the boars at the SCCs collected and distributed in the risk period of 28 January to 7 March 1997 was potentially contaminated (suspect semen). As a consequence, a total of 1,680 pig herds, mainly located in the southern part of the Netherlands, were officially declared CSF suspect. The purpose of this study was to investigate whether infection of farms through contaminated semen played a significant role in the CSF epidemic. A total of 123 CSFV infected herds were identified, that had received suspect semen from one or both of the infected SCCs. In 87 out of these 123 infected herds, infection by way of artificial insemination (AI) could be excluded either according to the insemination information or the infection pattern observed. In only 21 herds, infection by way of AI was regarded as possible according to the insemination information and infection pattern. Owing to missing information, no conclusion could be drawn about the possibility of infection of 15 farms by way of AI. Thus, we conclude that at most 36 farms may have been infected through AI during the CSF epidemic in the Netherlands.     

Laboratory findings during the classic swine fever epidemic of 1997-1998

The results of the laboratory tests carried out by the Institute for Animal Science and Health (ID-Lelystad), the Netherlands, on samples collected during the Classical Swine Fever (CSF) epidemic 1997-1998 are summarized in this article. The relevance of the different laboratory tests and various samples collected on the eradication of CSF during an outbreak is evaluated.     

Simulated financial losses of classical swine fever epidemics in the Finnish pig production sector

Rapid structural change and concentration of pig production in regions with most intensive production has raised concerns about whether the risk of large-scale disease losses has increased in Finland. This paper examines the pig industry's losses due to classical swine fever (CSF) epidemics. The work is based on economic and epidemiological models providing insights to the consequences of epidemics to infected and uninfected farms, government and meat processing. The economic analysis was carried out by use of a sector model, which simulated the recovery of pig production, starting from the recognition of the disease in the country and ending at a steady-state market equilibrium about 12 years later. The model explicitly took into account profit-maximising behaviour of producers and the effects of decrease in export demand.

Epidemiological evidence suggests that under the current spatially diversified structure of Finnish pig farming and related industries, the probability of a severe disease epidemic counting dozens of infected farms is small. Even for epidemics considered large in Finland (5–33 infected farms) combined with a major reduction in export demand, the median loss was simulated to be only €19.2 million. The majority of these losses were due to loss of exports corresponding almost 20% of pig meat production in Finland. While the current structure of pig farming in Finland incurs higher production costs than the most intensive structures in Europe, it also seems to decrease the probability of ‘catastrophic’ economic losses. The results suggest that the response of export markets and the number of uninfected farms affected by preventive measures are critical to the magnitude of losses, as they can amplify losses even if only few farms become infected.     

Spatial and stochastic simulation to evaluate the impact of events and control measures on the 1997-1998 classical swine fever epidemic in The Netherlands. II. Comparison of control strategies

Using the spatial, temporal and stochastic simulation model InterCSF, several alternative pre-emptive slaughter strategies that could have been applied in the Dutch Classical Swine Fever (CSF) epidemic of 1997–1998 were evaluated. Furthermore, effects of changes in some disease-spread and disease-control parameters were studied. InterCSF simulates the spread of CSF between farms through local spread and contacts (animals, transport and persons). Disease spread is affected by control measures implemented through different mechanisms (e.g. depopulation of infected farms, pre-emptive slaughter, movement control). The starting point for the evaluation of strategies was a simulated basic scenario, which mimicked the real epidemic. Strategies were compared using epidemiological as well as economic results. Economic results were generated by a separate model (EpiLoss) that calculated the direct losses and consequential losses for farmers and related industries. The comparison of the different alternatives to the basic scenario led to some general conclusions on the Dutch CSF-epidemic. Pre-emptive slaughter seemed to be an effective strategy to reduce the size of an epidemic, if started at an early stage. Economically, pre-emptive slaughter was not as expensive as expected; the resulting smaller size of the epidemic, combined with less welfare slaughter, led to much lower overall losses. Furthermore, although large movement control areas seemed effective in reducing the size of the epidemic, the total losses were relatively high because of subsequent welfare slaughter. If infection probabilities could be reduced, for example by improved biosecurity, the resulting epidemics would be much smaller.