Julia Österberg

Feed-borne Outbreak of Salmonella Cubana in Swedish Pig Farms: Risk Factors and Factors Affecting the Restriction Period in Infected Farms

In 2003, a feed-borne outbreak of Salmonella Cubana occurred in Sweden as a result of contamination in a feed plant. Salmonella Cubana was detected in 49 out of 77 pig farms having received possibly contaminated feed. In this study, potential risk factors for farms being salmonella positive were examined, and a survival analysis was performed to investigate risk factors affecting the restriction period for salmonella positive farms.The median restriction time for all 49 farms was 17 weeks. An increased risk for farms being salmonella infected (positive in feed and/or faeces) was seen for fattening farms and farms feeding soy. The survival analysis showed that herds with a low level of infection and farms with a high hygiene level had shorter restriction times.This study is unique as it investigates a real outbreak of feed-borne salmonella, where the source of infection was reliably identified, the period of exposure could be defined and data were collected from all exposed farms.SammanfattningSommaren 2003 påvisades en kontamination med Salmonella Cubana i en svensk foderfabrik. Vidare utredning visade att potentiellt smittat foder hade levererats till 77 svinbesättningar.I 49 av de 77 besättningarna kunde S. Cubana isoleras vid provtagningar av svin och/eller fodersystem. Dessa besättningar spärrförklarades och sanerades i enlighet med det svenska salmonellakontrollprogrammet. Denna studie omfattar en riskfaktoranalys och en överlevnadsanalys. Riskfaktorer för att en besättning som mottagit foder från den kontaminerade fabriken infekterats med salmonella undersöktes, respektive faktorer som kan ha påverkat spärrtidens längd på de gårdar som befanns salmonellapositiva. För de 49 drabbade besättningar var medianvärdet för spärrtidens längd 17 veckor. En ökad risk för att ha blivit infekterad med salmonella sågs hos gårdar med slaktsvinsproduktion och hos gårdar som köpt soja från den kontaminerade foderfabriken. Det visades även att gårdar med ett lågt smittryck, samt de med en hög hygiennivå, hade kortare spärrtid. Denna studie är unik då den undersöker ett verkligt utbrott av foderburen salmonella där smittkällan identifierats, exponeringsperioden definierats och data samlats in från samtliga gårdar som fått det potentiellt smittade fodret. .

Effects of a challenge dose of Salmonella Typhimurium or Salmonella Yoruba on the patterns of excretion and antibody responses of pigs

The epidemiology of a feed-associated Salmonella serotype (Salmonella Yoruba) was compared with that of a ‘classical’ serotype (Salmonella Typhimurium) by inoculating pigs aged 10 weeks with 0·65 × 103, 0·65 × 106 or 0·65 × 109 colony-forming units (cfu) of either serotype. The pigs were then monitored for eight weeks with respect to the faecal excretion of Salmonella species and the presence of serum antibodies. Only minor differences were observed between the two serotypes but the dose inoculated had significant effects. The pigs inoculated with 0·65 × 109 cfu shed Salmonella species in faeces constantly for four weeks, and intermittently during the subsequent four weeks; the pigs inoculated with 0·65 × 106 cfu shed Salmonella species intermittently for four weeks, but not for longer, and the pigs inoculated with 0·65 × 103 cfu generally did not excrete Salmonella species. The pigs inoculated with 0·65 × 109 cfu S Typhimurium seroconverted at a high titre within two weeks, the pigs inoculated with 0·65 × 106 cfu seroconverted later and with lower titres of antibodies, and the pigs inoculated with 0·65 × 103 cfu did not seroconvert. A similar pattern was observed with S Yoruba, but the responses were slower and at lower titres.

Direct and indirect transmission of four Salmonella enterica serotypes in pigs

BackgroundFeed-borne spread of Salmonella spp. to pigs has been documented several times in recent years in Sweden. Experiences from the field suggest that feed-associated serotypes might be less transmittable and subsequently easier to eradicate from pig herds than other serotypes more commonly associated to pigs. Four Salmonella serotypes were selected for experimental studies in pigs in order to study transmissibility and compare possible differences between feed-assoociated (S Cubana and S Yoruba) and pig-associated serotypes (S Derby and S Typhimurium).MethodsDirect contact transmission was studied in four groups of pigs formed by six 10-week-old salmonella negative pigs commingled with two fatteners excreting one of the four salmonella serotypes. Indirect transmission was studied by putting six 10-week-old salmonella negative pigs in each of four salmonella contaminated rooms. Each room had previously housed a group of pigs, excreting one of the four selected serotypes.All pigs were monitored for two weeks with respect to the faecal excretion of salmonella and the presence of serum antibodies. At the end of the trial, eight samples from inner tissues and organs were collected from each pig at necropsy.ResultsIn the four direct transmission groups, one pig shed Salmonella (Cubana) at one occasion. At necropsy, S Typhimurium was isolated from one pig.In the indirect transmission groups, two pigs in the Yoruba room and one pig in each of the other rooms were excreting detectable levels of Salmonella once during the study period of two weeks. At necropsy, S Derby was isolated from one of six pigs in the Derby room and S Typhimurium was isolated from four of the six pigs in the Typhimurium room.No significant serological response could be detected in any of the 48 pigs.ConclusionsThese results show that all four selected serotypes were able to be transmitted in at least one of these field-like trials, but the transmission rate was low in all groups and no obvious differences between feed-associated and pig-associated serotypes in the transmission to naïve pigs and their subsequent faecal shedding were revealed. However, the post mortem results indicated a higher detection of S Typhimurium in the ileocecal lymph nodes of pigs introduced into a contaminated environment in comparison with the other three serotypes.

Patterns of excretion and antibody responses of pigs inoculated with Salmonella Derby and Salmonella Cubana.

Groups of six, 10-week-old pigs were inoculated with 0.65 x 103, 0.65 x 106 or 0.65 x 109 colony-forming units (cfu) of Salmonella Cubana or Salmonella Derby and then monitored for eight weeks for the faecal excretion of Salmonella species and the presence of serum antibodies. Eight tissue samples were collected postmortem from each pig and analysed for Salmonella species. In general, the dose had a greater impact on the responses of the pigs than the serovar. However, in the groups inoculated with 0.65 x 106 cfu, S Cubana were excreted only by one pig during the first two days after infection, whereas the pigs inoculated with S Derby all shed the bacteria constantly for two weeks and then intermittently for several weeks. In the low dose groups none of the pigs excreted any detectable salmonella whereas all the pigs in both high dose groups shed salmonella constantly or intermittently throughout the eight weeks. All the 12 pigs inoculated with 0.65 x 106 or 0.65 x 109 cfu of S Derby seroconverted during the study period, whereas all the pigs inoculated with 0.65 x 103 remained seronegative. No serological response could be detected in the three groups of pigs inoculated with S Cubana. In the postmortem samples both serovars were re-isolated from the caecal contents and the colonic tissue, but the other organs and tissues were all negative except for one ileocaecal lymph node from a pig inoculated with 0.65 x 106 cfu of S Derby.

Antibiotic Resistance in Escherichia coli from Pigs in Organic and Conventional Farming in Four European Countries

Organic pig production differs in many ways from conventional production of pigs, e.g., in antibiotic use, herd structure, feeding regimes, access to outdoor areas and space allowance per pig. This study investigated if these differences result in a lower occurrence of antibiotic resistance in organic slaughter pigs in Denmark, France, Italy and Sweden. Samples were taken from the colon content and/or faeces and minimum inhibitory concentrations (MIC) of ten antibiotics were determined in isolates of Escherichia coli. In addition, the proportion of tetracycline (TET) resistant E. coli in colon content and/or faeces from individual pigs was determined. In all four countries the percentage resistance to ampicillin, streptomycin, sulphonamides or trimethoprim was significantly lower in E. coli from organic pigs. In France and Italy, the percentage of isolates resistant to chloramphenicol, ciprofloxacin, nalidixic acid or gentamicin was also significantly lower in the E. coli from organic pigs. Resistance to cefotaxime, was not found in any country. The percentage of E. coli isolates resistant to TET as well as the proportion of TET-resistant E. coli was significantly lower in organic than in conventional pigs, except in Sweden where TET-resistance was equally low in both production types. There were also differences between countries within production type in the percentage resistance to individual antibiotics as well as the proportion of TET-resistant E. coli with lower median proportions in Sweden and Denmark compared to France and Italy. The study shows that in each of the four countries resistance in intestinal E. coli was less common in organic than in conventional pigs, but that there were also large differences in resistance between countries within each production type, indicating that both country- and production-specific factors influence the occurrence of resistance.

Effects of free-range and confined housing on joint health in a herd of fattening pigs

BackgroundFree-range housing, in which pigs have access to both indoor and outdoor areas, is mandatory in organic pig production in Europe, but little is known about the effects of this housing on joint health in pigs. A high level of joint condemnations at slaughter has been reported in organic free-range pigs in Sweden, compared with pigs raised in conventional confined housing. We hypothesised that biomechanical forces imposed on the joints of pigs that range freely promote the development of osteochondrosis and lead to joint condemnation. We compared the prevalence of osteochondrosis and other joint lesions (e.g. arthritis, traumatic) in the elbow and hock joints of 91 crossbred Hampshire (Yorkshire × Landrace) fattening pigs that were housed in a free-range indoor/outdoor system with that in 45 pigs housed in confined indoor pens.ResultsA larger proportion of free-range than confined pigs had osteochondrosis in the elbow joints (69 vs. 50%, p?<?0.05), and a higher proportion of these joints in free-range pigs showed moderate or severe lesions (33 vs. 16%, p?<?0.05). The free-range pigs also showed a higher prevalence of osteochondrosis in the hock joints (83 vs. 62%, p?<?0.05) and a larger proportion of these joints had moderate or severe lesions (69 vs. 33%, p?<?0.001). At slaughter, 4.2% of the free-range pigs had condemned joints, all of which showed severe osteochondrosis, while no joints of confined pigs were condemned.ConclusionsIn this experiment the prevalence of osteochondrosis in the elbow and the hock was higher, and lesions were more severe, in free-range than in confined pigs, suggesting that free-range housing increases the risk of acquiring osteochondrosis. Increased biomechanical stress to vulnerable joint structures may be the mechanism behind this effect, however more studies are needed to verify these results. This study suggests that modification of housing, and breeding for joints that are more adapted to free-range movement may be needed in free-range pig production. Severe osteochondrosis is a cause of joint condemnation, but the condemnation rate at slaughter underestimates the actual frequency of joint lesions and hence is a poor assessment of joint health.

Risk assessment as a tool for improving external biosecurity at farm level

BackgroundBiosecurity routines at herd level may reduce the probability of introduction of disease into the herd, but some measures may be regarded as expensive and cumbersome for the farmers. Custom-made measures based on individual farm characteristics may aid in improving the actual application of on-farm biosecurity.The aim of the study was to provide a tool for calculating the effects of different biosecurity measures and strategies on the individual farm level.A simple model was developed to assess the risk of disease introduction and the need for biosecurity measures in individual farms. To illustrate the general applicability of the tool, it was applied to theoretical examples of Swedish cattle and pig farms and diseases endemic in those animal species in the EU, in two scenarios with different between-farm contact patterns.ResultsThe model illustrated that the most important factors affecting the risk, and the effect of biosecurity measures such as quarantine routines and protective clothing, were the frequency of between-farm contacts and prevalence of the disease. The risk of introduction as well as the effect of biosecurity measures differed between farm types and disease transmission routes. Adapting contact patterns to mitigate a specific disease risk was as important as biosecurity measures for some farm types, but the largest effect was seen when combining biosecurity measures with more planned contact patterns.ConclusionsThe risk assessment model proved useful for illustrating the risk of introduction of endemic diseases and the mitigating effect of different biosecurity measures on farm level. Model outputs could be used to justify prioritisation of measures or adapting contact patterns. The theoretic exercise of adjusting model inputs and comparing outputs may help veterinary advisors to understand farm-specific risks and motivate farmers to improve biosecurity in their individual farm, as it can be tailored to each farmer’s needs and preferences.

Characterization of Antibiotic Resistance Gene Abundance and Microbiota Composition in Feces of Organic and Conventional Pigs from Four EU Countries

One of the recent trends in animal production is the revival of interest in organic farming. The increased consumer interest in organic animal farming is mainly due to concerns about animal welfare and the use of antibiotics in conventional farming. On the other hand, providing animals with a more natural lifestyle implies their increased exposure to environmental sources of different microorganisms including pathogens. To address these concerns, we determined the abundance of antibiotic resistance and diversity within fecal microbiota in pigs kept under conventional and organic farming systems in Sweden, Denmark, France and Italy. The abundance of sul1, sul2, strA, tet(A), tet(B) and cat antibiotic resistance genes was determined in 468 samples by real-time PCR and the fecal microbiota diversity was characterized in 48 selected samples by pyrosequencing of V3/V4 regions of 16S rRNA. Contrary to our expectations, there were no extensive differences between the abundance of tested antibiotic resistance genes in microbiota originating from organic or conventionally housed pigs within individual countries. There were also no differences in the microbiota composition of organic and conventional pigs. The only significant difference was the difference in the abundance of antibiotic resistance genes in the samples from different countries. Fecal microbiota in the samples originating from southern European countries (Italy, France) exhibited significantly higher antibiotic resistance gene abundance than those from northern parts of Europe (Denmark, Sweden). Therefore, the geographical location of the herd influenced the antibiotic resistance in the fecal microbiota more than farm’s status as organic or conventional.