Proyecto académico sin fines de lucro, desarrollado bajo la iniciativa de acceso abierto

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1 Red de Revistas Científicas de América Latina, el Caribe, España y Portugal Sistema de Información Científica Stojanac, Nenad; Stevanevi, Ognjen; Potkonjak, Aleksandar; Savi, Božidar; Stani, Ivan; Vraar, Vuk Importance of Breeding Pigs in the Spread of Salmonella on Farms Acta Scientiae Veterinariae, vol. 42, núm. 1, enero, 2014, pp. 1-8 Universidade Federal do Rio Grande do Sul Porto Alegre, Brasil Disponible en: Acta Scientiae Veterinariae, ISSN (Versión impresa): ActaSciVet@ufrgs.br Universidade Federal do Rio Grande do Sul Brasil Cómo citar? Número completo Más información del artículo Página de la revista Proyecto académico sin fines de lucro, desarrollado bajo la iniciativa de acceso abierto

2 Acta Scientiae Veterinariae, : RESEARCH ARTICLE Pub ISSN Importance of Breeding Pigs in the Spread of Salmonella on Farms Nenad Stojanac 1, Ognjen Stevančević 1, Aleksandar Potkonjak 1, Božidar Savić 2, Ivan Stančić1 & Vuk Vračar 1 ABSTRACT Background: Pigs infected with Salmonella represent a high risk for contamination and cross-contamination of carcasses with Salmonella from feces, tonsils and mesenteric lymph nodes, which occurs on the slaughter line. The environment itself represents a potential source of infection, as it is Salmonella infection of other individuals in the herd (sows, boars, piglets, fattener pigs). One of the leading sources of infection is contaminated feed for pigs, or its ingredients. If an infection occurs at any stage and category of production, those individual animals can become a potential source of infection for all others on farm. Materials, Methods & Results: This study examines the importance of breeding categories of pigs in the spread of salmonellosis in piglets and fattener pigs on seven farrow-to-finish farms in Serbia. From each farm, 30 sows, 121 boars and 90 piglets were tested from the weaning to the time of dispatch to the slaughterhouse. Pigs were examined for the presence of Salmonella-specific antibodies in blood sera and the presence of Salmonella in feces. Pigs feed on the farms were also examined for the presence of Salmonella. The identification of serotypes was conducted according to the Kauffmann-White scheme. For antimicrobial sensitivity and resistance testing, isolates were tested by disc diffusion against a panel of 11 antimicrobials. The numbers of pigs with at least one positive faecal isolation and with at least one positive serological result were evaluated descriptively. The McNemar test was used to compare the number of shedding pigs and the number of seropositive pigs at different time points. The statistical significance of differences between means was at the level of P < Overall, 60.0% of sows were seropositive, and this was significantly higher (P < 0.05) than the seropositivity of the boars. In addition, isolation of Salmonella from feces of sows was more common than from boars. Seroprevalence ranged from 0 to 90% in fattener pigs. Salmonella Typhimurium and Salmonella Derby were the most prevalent serovars, representing 69.77% and 19.77% of isolates serotyped, respectively. Antimicrobial sensitivity and resistance testing was carried out on 88 Salmonella isolates. Discussion: As it is well known that pigs are get easily infected orally with Salmonella and contaminated environments such as feed and litter direct contact between pigs are thought the main source of infection. When compared to higher number of seropositive animals, low number of Salmonella positive feed samples and feces positive animals show the lower correlation between the presence of Salmonella antibodies and Salmonella isolation in the current study. In addition, results obtained from this study shows there may be low correlation between serology and culture test results and low number of culture positivity can originate from latently infected animals or lower sensitivity of the culture methods. On farrow-to-finish farms in Serbia, because sows, boars and fatteners are kept together on the same farm, and for that reason sows and boars may play an important role in the transmission of Salmonella. Among the positive samples, Salmonella Typhimurium and Salmonella Derby represented 89.54% of all isolates. The percentage of Salmonella isolates sensitive to amoxicillin and ceftriaxone exceeded 75%, and sensitive to penicillin was seen in 58%. The antimicrobials showing resistance in this study are similar to those in reports from other authors, in particular the high rate of resistance to tetracyclines, streptomycin, neomycin and doxycycline. The results show that the farms with high prevalences of Salmonella in sows also had a higher prevalence of Salmonella in fattener pigs; this would lead to higher risk of contamination of carcasses. Sows may spend up to 10 years on farms and can be a continuous source of Salmonella infection. Keywords: breeding pigs, feed, prevalence, Salmonella. Received: 04 November 2013 Accepted: 24 March 2014 Published: 28 April Department of Veterinary Medicine, Faculty of Agriculture, University of Novi Sad, Novi Sad, Republic of Serbia. 2 Institute of Veterinary Medicine Belgrade, Belgrade, Serbia. CORRESPONDENCE: N. Stojanac [stojanac.n@gmail.com - Fax: +381 (21) ]. Department of Veterinary Medicine, Faculty of Agriculture, University of Novi Sad, Trg Dositelja Obradovića 8, Novi Sad, Republic of Serbia. 1

3 INTRODUCTION Salmonella causes disease in all categories of pigs, but, except in piglets, it is rarely clinically manifested. Isolation of Salmonella from the feces of asymptomatic infected pigs is difficult, because of the sporadic nature of Salmonella excretion and the relatively small number of these bacteria compared with the total fecal microbiota. For these reasons, serological testing using enzyme-linked immunosorbent assay (ELISA) is the method of choice for the detection of Salmonella-positive individuals and herds. Serological monitoring, i.e. the presence of antibodies specific to Salmonella, is used in many countries around the world classifying herds and is the basis for most Salmonella control programs. Specific class G immunoglobulins (IgG) against Salmonella persist in the animals sera long after infection, so detection indicates previous or current exposure of the individual or herd to Salmonella, but is not necessarily an indicator of current infection [26]. In Serbia, all large pig farms are of the one-site type, within which all production stages are included, namely, reproduction (gilts, sows and boars), production of piglets (farrowing house and nursery) and the production of fattener pigs. If an infection occurs at any stage and category of production, those individual animals can become a potential source of infection for all others on farm. The objectives of this study were to: a) keep track on Salmonella status by serological and bacteriological methods in both individual and all animal categories, b) examine correlation of Salmonella presence on-farm feed for the same animals or animal groups and c) determine the importance of animal categories (sows and boars) and feed as a source of Salmonella infection. MATERIALS AND METHODS Study design and herd selection A longitudinal study was conducted in Serbia from May 2011 to December 2012 in seven large farrow-to-finish herds. The criteria for selection were the size of farms (over 1,000 sows) and the willingness of farmers to cooperate. All farms studied operated on the basis of weekly management. All individual animals were marked with ear tags with a unique number. Technology and work organization was similar on all farms. After insemination, sows remained in the mating pens for 28 days and after a positive pregnancy ultrasound test, they were transferred to the waiting area and remained there until farrowing. Sows and gilts were moved to the farrowing house on day 110 of pregnancy. Lactation lasted for 28 days, after which the sows were transferred back to the mating pens and piglets to the nursery. Piglets stayed in the nursery for 42 days after which they were moved to fattening facilities. Fattening lasted 110 days. In every segment of the production the all in-all out principle was used, and all facilities were cleaned, washed and disinfected after emptying, before being re-populated in 3-4 days. Boars were held in separate facilities. All investigated farms exclusively used for artificial insemination. Sample collection Individual blood, faecal and feed samples were collected from 30 sows at weaning, on each farm. From each sow, three piglets were selected and examined in the coming period. In addition, individual blood, faecal and feed samples were collected from pigs on the following periods: at 25 days old (just prior to weaning), 45 days old (in the nursery), 75 days old (just before leaving the nursery), 100 days old (in the finishing unit), 130 days old (in the finishing unit) and 180 days old (just prior to dispatch for slaughter). Blood and feces of the boars were also taken for examination during the first visit to farms, when samples from sows were also taken. Pig feed was taken from the feeders for each animal category (sows, boars, piglets, fattener pigs). During each visit, by the time of blood and feces samples were collected, feed samples were also taken. Laboratory analysis Faecal and feed samples were collected into sterile containers and transported on ice packs to the laboratory within 2-4 h and cultured immediately. ISO 6579:2002 method was followed. Briefly, each sample was incubated in buffered peptone water (BPW) 1 for 18 h at 37 C (pre-enrichment step). Subsequently, 1 ml of inoculum was transferred to 10 ml of Muller Kauffmann tetrathionate-novobiocin broth (MKTTn) 1, and 0.1 ml was transferred to 10 ml of Rappaport Vassiliadis Broth with soya (RVS) 1, and incubated 24 h at 37 C and 41.5 C, respectively, for each enrichment. Then, both xylose lysine deoxycholate agar (XLDA) 1, and Salmonella Chromogenic agar (SCA) 1, plates were inoculated from RVS broth. Also, both brilliant green agar (BGA) 1, and XLDA plates were inoculated from 2

4 MKTTn broth. All the plates were incubated at 37 C for 24 h. Suspected colonies (with black centre and/ or pink from XLDA, pink from BGA or magenta from SHA) were purified on a nutrient agar and confirmed biochemically using API 20E kits 2 and serologically using poly O antiserum 3. The identification of serotypes was conducted according to the Kauffmann-White scheme [22]. For antimicrobial sensitivity and resistance testing, isolates were tested by disc diffusion against a panel of 11 antimicrobials (Table 7). Blood was taken by puncture of the brachiocephalic plexus of the sows, boars and piglets. All blood sera from sows and piglets were frozen, and blood sera (harvested after thawing) were examined for specific IgG antibodies against Salmonella using an indirect ELISA [18]. Statistical analyses Data were entered into an Excel spreadsheet (Microsoft Excel 2010) and imported into Stata (Stata 8 Intercooled for Windows 9x) in which data were analyzed. Descriptive analysis was performed in MiniTab version 14 (MiniTabR14b) and Excel (Microsoft Excel 2010). The numbers of pigs with at least one positive faecal isolation and with at least one positive serological result were evaluated descriptively. The McNemar test was used to compare the number of shedding pigs and the number of seropositive pigs at different time points. The statistical significance of differences between means was at the level of P < RESULTS Serological and bacteriological results in sows In the study, seropositivity was found in all seven farms, with 60.0% overall seropositivity in sows. Percentage of seropositivity was changed from 20% to 90% and farm III was being the lowes as 20% (Table 1). Salmonella was isolated from sow feces in three out of the seven (42.8%) farms. On each of these three farms (I, IV and VII) Salmonella was isolated from the feces of only one sow. The overall Salmonella in feces was 4.3% in all the examined farms in sows. In two out of the seven farms (in farms IV and VII), Salmonella was found in feed samples of sows (Table 1). Serological and bacteriological results in boars In the study, 19 (15.7%) out of 121 boars tested were found seropositive. Seroprevalences ranged from 3 6.7% on farm III to 33.3% on farm I. We found the lowest Salmonella seroprevalance on farm III both in boars and in sows (Tables 1 & 2). The overall seroprevalence in boars on all farms studied was significantly lower (P < 0.05) than the overall seroprevalece of sows on the same farms. In boars, on two (28.6%) out of the seven farms, Salmonella was isolated from feces. On the same farms (I and IV), Salmonella was also found in the sows. Two (1.6%) out of 121 faecal samples tested from boars were positive for Salmonella, which was significantly lower (P < 0.05) than the sow faecal samples (4.3%) of which Salmonella was isolated. Salmonella was not isolated any of feed samples of boars on seven farms (Table 2). Serological and bacteriological results in piglets and fattener pigs On farm III, all tested individual animals during the entire follow-up period (from weaning until sending to slaughterhouse) were seronegative. On the other six farms, the number of seropositive animals increased with the age of animals. On all farms, except farm III, at day 75, at least 6 seropositive pigs were found. The greatest seroprevalence, expressing 90% the animals, was found on farm VII, in fattener pigs before slaughter at 180 days old (Table 3). On farm III, Salmonella was not isolated from feces of any examined animal from the periods of weaning to sending to the slaughterhouse. On the other six farms, at the day of weaning (28 days old) and/or 45 days old, Salmonella was found in the feces of at least one of the tested animals. In the same fattener pigs, at 180 days old (before slaughter), Salmonella was not found in any of faecal samples (Table 4). On four farms tested, Salmonella was found in feed of piglets and fattener pigs. On farms I and IV, Salmonella was isolated from the feed of 100 days old aged fattener pigs, and on farms VI and VII in feed of fattener pigs aged 45 and 75 days (Table 5). Salmonella serovars Serotyping was carried out on 86 Salmonella isolates. The prevalence of all serovars detected is given in Table 6. The most prevalent serotype was Salmonella Typhimurium, which was isolated from the faeces of the sows, boars and pigs. Antimicrobial sensitivity and resistance Antimicrobial sensitivity and resistance testing was carried out on 88 Salmonella isolates. The number of isolates sensitive and resistant to each antimicrobial is shown in Table 7.

5 Table 1. Distribution and presence of IgG in blood and Salmonella in faecal and feed samples of sows on 7 farrow-to-finish swine farms. Farm Number of blood sera positive Number of faecal samples positive Number of feed samples positive N (%) N (%) N (%) I 24/30 (80.0) 3/30 (10.0) 0/30 (0) II 9/30 (30.0) 0/30 (0.0) 0/30 (0) III 6/30 (20.0) 0/30 (0.0) 0/30 (0) IV 12/30 (40.0) 3/30 (10.0) 3/30 (10) V 24/30 (80.0) 0/30 (0.0) 0/30 (0) VI 24/30 (80.0) 0/30 (10.0) 0/30 (0) VII 27/30 (90.0) 3/30 (20.0) 9/30 (30) Total 126/210 (60.0) 9/210 (4.3) 12/210 (5.7) Table 2. Distribution and presence of IgG in blood and Salmonella in faecal and feed samples of boars on 7 farrow-to-finish swine farms. Farm Number of blood sera positive Number of faecal samples positive Number of feed samples positive N (%) N (%) N (%) I 6/18 (33.3) 1/18 (5.5) 0/18 (0) II 1/10 (10.0) 0/10 (0.0) 0/10 (0) III 2/30 (6.7) 0/30 (0.0) 0/30 (0) IV 2/25 (8.0) 1/25 (4.0) 0/25 (0) V 3/15 (20.0) 0/15 (0.0) 0/15 (0) VI 2/9 (22.2) 0/9 (0.0) 0/9 (0) VII 3/14 (21.4) 0/14 (0.0) 0/14 (0) Total 19/121 (15.7) 2/121 (1.6) 0/121 (0) Table 3. Salmonella seroprevalence estimates provided by blood serum sample collected of pigs on 7 farrow-to-finish swine farms. Age Farm /90 (%) (Days) I II III IV V VI VII 25 3 (3.3) 0 (0.0) 0 (0.0) 6 (6.7) 39 (43.3) 0 (0.0) 12 (13.3) 45 6 (6.7) 0 (0.0) 0 (0.0) 6 (6.7) 45 (50.0) 45 (50.0) 54 (60.0) (16.7) 6 (6.7) 0 (0.0) 6 (6.7) 45 (50.0) 48 (53.3) 63 (70.0) (33.3) 18 (20.0) 0 (0.0) 9 (10.0) 51 (56.7) 48 (53.3) 69 (76.7) (70.0) 18 (20.0) 0 (0.0) 12 (13.3) 54 (60.0) 60 (66.7) 78 (86.7) (80.0) 21 (23.3) 0 (0.0) 18 (20.0) 54 (60.0) 60 (66.7) 81 (90.0) 4

6 Table 4. Distribution Salmonella in faecal samples of pigs on 7 farrow-to-finish swine farms. Age Farm /90 (%) (Days) I II III IV V VI VII (13.3) 0 (0.0) 0 (0.0) 3 (3.3) 9 (10.0) 3 (3.3) 6 (6.7) (13.3) 6 (6.7) 0 (0.0) 3 (3.3) 6 (6.7) 6 (6.7) 6 (6.7) 75 9 (10.0) 3 (3.3) 0 (0.0) 0 (0.0) 6 (6.7) 9 (10.0) 18 (20.0) (10.0) 0 (0.0) 0 (0.0) 6 (6.7) 0 (0.0) 3 (3.3) 15 (16.7) (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 3 (3.3) (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) Table 5. Distribution Salmonella in feed samples of pigs on 7 farrow-to-finish swine farms. Age Farm /10 (%) (Days) I II III IV V VI VII 25 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 45 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (20.0) 1 (10.0) 75 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (10.0) 3 (30.0) (10.0) 0 (0.0) 0 (0.0) 2 (20.0) 0 (0.0) 0 (0.0) 0 (0.0) (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) Table 6. Salmonella serovars isolated from 7 farrow-to-finish swine farms, grouped according breeding pigs. Sows Boars Pigs Total (%) S. Typhimurium (69.77) S. Derby (19.77) S. Infantis (4.65) S. Enteritidis (3.49) S. Livingstone (2.32) Table 7. Number (%) of Salmonella isolates to each antimicrobial tested (n = 88). Antimicrobial Sensitive Intermediate Resistant N (%) N (%) N (%) Amoxicillin 81 (92.0) 4 (4.5) 3 (3.5) Ceftriaxone 77 (87.4) 8 (9.1) 3 (3.5) Enrofloxacin 33 (37.5) 46 (52.3) 9 (10.2) Gentamicin 43 (48.9) 8 (9.1) 37 (42.0) Colistin 7 (7.9) 8 (9.1) 73 (83.0) Neomycin 9 (10.2) 30 (34.1) 49 (55.7) Penicillin 58 (65.9) 18 (20.5) 12 (13.6) Streptomycin 4 (4.5) 11 (12.5) 73 (83.0) Tetracycline 3 (3.5) 6 (6.8) 79 (89.7) Doxycycline 5 (5.7) 16 (18.2) 67 (76.1) Flumequin 34 (38.6) 14 (15.9) 40 (45.5) 5

7 DISCUSSION Humans may often be infected with Salmonella from contaminated carcasses of fattener pigs [3]. For this reason, much research regarding Salmonella detection in pigs has been conducted in fattener pigs [1,4]. All studies have shown that it is necessary to examine all categories of pigs and their premises in terms of Salmonella carriage for complete control and reduction [1,8,26]. As it is well known that pigs are get easily infected orally with Salmonella [25], and contaminated environments such as feed and litter direct contact between pigs are thought the main source of infection. On farrow-to-finish farms in Serbia, because sows, boars and fatteners are kept together on the same farm, and for that reason sows and boars may play an important role in the transmission of Salmonella. In the study, detection of antibodies to Salmonella in the majority of sows (60.0%) and isolation of Salmonella from the feces of 9 (4.3%) sows, indicate that sows can be potential source of Salmonella in these herds. While the presence of antibodies specific to Salmonella in sows indicates that they are a potential source of infection. The presence of antibodies is of little importance for colostral immunity, because humoral immunity is less effective against facultative intracellular bacteria including Salmonella [12]. Salmonella can survive within the macrophages, where they cannot be reached by antibodies [30]. Salmonella was isolated from the feed of two of the three sows which were both seropositive and feces-positive. This suggests that the source of infection may be contaminated by feed, as it has been found on search of many other authors [6-8]. When compared to higher number of seropositive animals, low number of Salmonella positive feed samples and feces positive animals show the lower correlation between the presence of Salmonella antibodies and Salmonella isolation in the current study [10,19,23] (Table 1). In addition, results obtained from this study shows there may be low correlation between serology and culture test results and low number of culture positivity can originate from latently infected animals or lower sensitivity of the culture methods. On pig farms in Serbia, boars are always kept under the best conditions, at optimum temperature with the best hygiene, movement of people access, and disinfection by the use of most stringent disinfectants. All of these aforementioned reasons may cause lower Salmonella seroprevalance in boars (15.7%) compared to sows (60.0%), which confirms the literature data that biosecurity measures are essential for the control of Salmonella infection [2]. In two (1.6%) boars, Salmonella was isolated from feces, while 121 feed samples tested were Salmonella-free. The presence of antibodies specific for Salmonella in pigs does not mean that the infection is necessarily active and the pig is carrier of Salmonella, but indicates that it is or was exposed to infection. Clinically, Salmonella is rarely manifested in boars, but when this does occur, it is seen most often in the form of diarrhea [31], usually when the immune system becomes weak as a result of stress or co-infection with other pathogens [9,27,29]. After weaning, piglets become more susceptible to infections with Salmonella, because of their transition to solid feed, changes in the environment, stress and failure of colostral immunity [14,19]. In the current study, isolation of Salmonella had a rising trend from weaning to 75 days, after which it slowed down, but at day 180, when fatteners were sent to slaughter, all samples of feces were free of Salmonella. This was probably due to: the increased resistance of the pigs own immune systems [21]; the use of antibiotics as preventive purposes, which is common on farms in Serbia [5]; and the lower frequency of people in the finishing fattening units [13]. In contrast to the noticeable age-related decline in the number of individuals from which Salmonella was isolated from feces, the number of seropositive individuals increased with age. Studies have shown that individual pigs which had contact with Salmonella and where seroconversion occurred [16], the formation of IgG persisted in the blood at least for 6 months after the infection [24]. Among the positive samples, Salmonella Typhimurium and Salmonella Derby represented 89.54% of all isolates. This date correspond well with studies from many countries [15,17,32]. The percentage of Salmonella isolates sensitive to amoxicillin and ceftriaxone exceeded 75%, and sensitive to penicillin was seen in 58%. The antimicrobials showing resistance in this study are similar to those in reports from other authors, in particular the high rate of resistance to tetracyclines, streptomycin, neomycin and doxycycline [11,20,28]. The results of this study indicate that feed contaminated with Salmonella leads to infection of pigs, which sometimes - as in this study - is impossible to confirm by isolating Salmonella from feces. However, the fact that individual pigs had contact 6

8 with Salmonella was clearly proven in this study by both positive bacteriological and serological findings. Sows are frequently carriers of Salmonella and are source of infection, especially in stressful stages (farrowing and weaning period), while in Serbia, boars are kept in better conditions and attract more attention, and therefore, are less likely to infect other animals on the farm. CONCLUSION Based on this results, we conclude that fattener pigs, living on farms where there are higher seroprevalences of Salmonella in sows, have higher seroprevalence. This indicates that the sows, in addition to feed, are one of the leading sources of Salmonella infections on farms in Serbia. Sows remain in the herd approximately 3 years, although some reside in-herd for up to 10 years, which is substantially longer than the fattener pigs. Therefore, if a sow is a Salmonella carrier, it can remain a potential source of the organism for a long period of time. For these reasons, sows should be given special attention and further research should focus in this direction, all with the aim to reduce Salmonella infections in pigs. SOURCES AND MANUFACTURERS 1 Oxoid, Hampshire, England, UK. 2 BioMérieux, Marcy l Etoile, France. 3 Pro-Lab Diagnostics, Richmond Hill, ON, Canada. Funding. This research was financially supported by the Ministry of Education, Science and Technological Development of the Republic of Serbia, Project No. TR Declaration of interest. The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. REFERENCES 1 Alban L., Baptista F.M., Møgelmose V., Sørensen L.L., Christensen H., Aabo S. & Dahl J Salmonella surveillance and control for finisher pigs and pork in Denmark - A case study. Food Research International. 45(2): Beloeila P.A., Chauvina C., Prouxa K., Fableta C., Madeca F. & Alioumc A Risk factors for Salmonella seroconversion of fattening pigs in farrow-to-finish herds. Veterinary Research. 38(6): Blagojevic B. & Antic D Assessment of potential contribution of official meat inspection and abattoir process hygiene to biological safety assurance of final beef and pork carcasses. Food Control. 36(1): Bolton D.J., Ivory C. & McDowell D A study of Salmonella in pigs from birth to carcass: serotypes, genotypes, antibiotic resistance and virulence profiles. International Journal of Food Microbiology. 160(3): Bonardi S., Bassi L. Brindani F., D Incau M., Barco L., Carra E. & Pongolini S Prevalence, characterization and antimicrobial susceptibility of Salmonella enterica and Yersinia enterocolitica in pigs at slaughter in Italy. International Journal of Food Microbiology. 163(2-3): Callies A., Sander S.J., Verspohl J., Beineke A. & Kamphues J Effect of grinding intensity and feed physical form on in vitro adhesion of Salmonella Typhimurium and mannose residues in intestinal mucus receptors for Salmonellae. Journal of Animal Science. 90(4): Correia-Gomes C., Mendonça D., Vieira-Pinto M. & Niza-Ribeiro J Risk factors for Salmonella spp in Portuguese breeding pigs using a multilevel analysis. Preventive Veterinary Medicine. 108(2-3): De Busser E.V., De Zutter L., Dewulf J., Houf K. & Maes D Salmonella control in live pigs and at slaughter. Veterinary Journal. 196(1): De la Fé Rodríguez P.Y., Martin L.O.M., Muñoz E.C., Imberechts H., Butaye P., Goddeeris B.M. & Cox E Several enteropathogens are circulating in suckling and newly weaned piglets suffering from diarrhea in the province of Villa Clara, Cuba. Tropical Animal Health and Production. 45(1): Farzan A., Friendship R., & Dewey C.E Evaluation of enzyme-linked immunosorbent assay (ELISA) tests and culture for determining Salmonella status of a pig herd. Epidemiology and Infection. 135(2): Graziani C., Busani L., Dionisi A.M., Lucarelli C., Owczarek S., Ricci A., Mancin M., Caprioli A. & Luzzi I Antimicrobial resistance in Salmonella enterica serovar Typhimurium from human and animal sources in Italy. Veterinary Microbiology. 128(3-4): Haesebrouck F., Pasmans F., Chiers K., Maes D., Ducatelle R. & Decostere A Efficacy of vaccines against bacterial diseases in swine: what can we expect? Veterinary Microbiology. 100(3-4): Hoelzer K., Switt A.I.M. & Wiedmann M Animal contact as a source of human non-typhoidal salmonellosis. Veterinary Research. 42: 34. 7

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