This article was downloaded by: [University of Nebraska, Lincoln] On: 21 October 2014, At: 03:19 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Veterinary Quarterly Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tveq20
Occurrence of Salmonella in swine in the Latium Region (central Italy) from 1980 to 1989: A retrospective study a
a
a
a
a
G. Di Guardo , G. Fontanelli , G. Panfili , R. Condoleo , L. De Grossi , A. M. a
Brozzi & A. I. Bozzano
a
a
Instituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana , Via Appia Nuova, Rome, 1411–00178, Italy Published online: 01 Nov 2011.
To cite this article: G. Di Guardo , G. Fontanelli , G. Panfili , R. Condoleo , L. De Grossi , A. M. Brozzi & A. I. Bozzano (1992) Occurrence of Salmonella in swine in the Latium Region (central Italy) from 1980 to 1989: A retrospective study, Veterinary Quarterly, 14:2, 62-65, DOI: 10.1080/01652176.1992.9694331 To link to this article: http://dx.doi.org/10.1080/01652176.1992.9694331
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
abnormalities in slaughtered pigs. Vet Quarterly 1990; 12: 146-51. , 33. Statistical Analysis Systems (SAS). SAS Institute Inc., Cary, NC, USA Statistics and Basics User's Guides (1985). 34. Tie len MJM. Incidence and the prevention by animal care of lung and liver
38. Tumbleson ME, Schmidt DA and Scholl E. Hematology and clinical
affections of fattening pigs. PhD-thesis, Agric. University Wageningen, The Netherlands, 1974: 141 pp. 35. Tie len MJM and Elbers ARW. Experiences with Integrated Chain Control for pig production in the Netherlands. Proc 6th Int Congr on Anim Hygiene, 14-17 June 1988, Skara, Sweden. Ed. Ekesbo I. Vol.I.: 227-31. 36. Tolling KT. Age dependent variation of serum creatine kinase isoenzyme levels in pigs. J Vet Med (A) 1982; 29: 420-8.
39. Ubaldi A. Biochemical parameters of pigs in intensive breeding. In:
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
37. Travnicek L and Mandel L. Haematology of conventional and germfree miniature Minnasota piglets. II. Serum proteins and immunoglobulins. Z Versuchstierk 1982; 24: 308-17.
chemistry. In 'Diseases of Swine'. Eds. Leman AD, Straw B, Glock RD, Mengeling WL, Penny RHC and Scholl E. Iowa State University Press, Ames, Iowa, USA, 1988: 27-44.
'Research and results in Clinical Chemistry of Domestic Animals'. Ed. Sommer, H., Institute of Anatomy and Physiology, Bonn,Germany, 1983:
307-16. 40. Willeberg P, Gerbola MA, Kirkegaard Petersen B, and Andersen JB. The
Danish Pig Health Scheme
:
Nationwide Computer-based Abattoir
Surveillance and follow-up at the Herd Level. Prey Vet Med 1984;3:79-91. 41. Wilson GDA, Harvey DG, and Snook CR. A review of factors affecting blood biochemistry in the pig. Br Vet J 1972; 128: 596-609.
OCCURRENCE OF SALMONELLA IN SWINE IN THE LATIUM REGION (CENTRAL ITALY) FROM 1980 TO 1989: A RETROSPECTIVE STUDY G. Di Guardo, G. Fontanelli, G. Panfili, R. Condoleo, L. De Grossi, A. M. Brozzi, and A. I. Bozzano1 Veterinary Quarterly 1992; 14: 62-5
SUMMARY An extensive survey was carried out on 849 biological samples (dead animals, organs and viscera, faeces, and rectal swabs) from pigs in the Latium Region (Central Italy) throughout the years 1980-1989. In total 46 of the samples (5.4%) were found to be bacteriologically positive for salmonellae. Among dead
animals, typical gross lesions were observed in 6 clinically infected animals.
As far as serotypes are concerned 11 different ones were isolated with a predominance of Salmonella typhimurium (26.1%), S. anatum (21.7%), S. bovis-morbificans (15.2%), and S. heidelberg (10.8%). According to Kauffmann-White's classi-
fication scheme, 39.1% of the isolated strains belonged to serogroup B, 13% to serogroup C 1, 17.4% tot serogroup C2, 6.5% to serogroup D, and 23.9% to serogroup El.
In conclusion, the authors speculate that the relatively low Salmonella isolation frequency (5.4%) reported in this study was not dependent upon the cultural procedures used since different enrichment and plating methods were used, but rather upon the great number of rural-type herds which were investigated over the decade compared to industrial-type herds. Otherfactors such
as stress conditions, which are particularly pronounced in
industrial-type herds, and overall climatic situations, which tend
to be characterised by warm, dry and long summers in the Latium Region, are also considered in this respect. INTRODUCTION
Salmonella infections rank among the most important causes of bacterial enteritis in humans, in spite of a generally accepted underreporting, amounting up to 95% in some countries (20). At present, salmonellosis is considered, along with campylobacteri-' osis, one of the two most prevalent reported foodborne zoonoses I
Instituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana, Via Appia Nuova, I411-00178-Rome, Italy.
62
in developed countries (22), being mainly related to the consumption of contaminated meat and other foodstuffs of animal origin (18). In this regard, pork meat and pork meatbased products are frequent sources of Salmonella infection in man (22). Animals are known to play a major role as hosts and vectors of a
variety of zoonotic Salmonella serotypes, which are often asymptomatically carried by them (22). Carrier status frequently occurs in poultry and pigs, with special reference to industrial breeding and production plants (6). In particular, swine can often carry Salmonella in both the intestinal tract and the mesenteric lymph nodes (15). Modern slaughter procedures potentially involve many risks of
both direct and cross-contamination of carcasses and meat surfaces. Cross contamination with pathogenic bacteria (i.e. Salmonella) during slaughter is much more pronounced with pork and poultry carcasses than with beef and sheep carcasses
(23). In modern slaughter lines, Salmonella contamination and crosscontamination of pig carcasses, as well as of the surrounding
environment and slaughter equipment, can especially occur during the evisceration process if this is not carried out properly (22). Surface contamination is further spread during the subsequent chilling, portioning, packaging, and distribution of the meat or meat products. The aim of the present work was to evaluate retrospectively the prevalence and distribution of Salmonella among.pigs reared in
the Latium Region (Central Italy), comparing our data with those previously obtained by other investigators. For this purpose, data were obtained from our Institute's diagnostic
laboratories from 1980 to 1989. Briefly, our Institute (Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana) is a public health organisation placed under the official control of
THEVETERINARYQU ARTERLY, VOL
1
4, No. 2, APRI
L
,
1
992
the Regional Authority. There are nine other such Institutes nationally, each of them being in charge of one, two or three of
were then cultured in TSI-agar at 37° C for 24 h and finally identified and serotyped by using routine biochemical and
the 20 Italian Regions. Our Institute covers Latium and
seroagglutination techniques.
Tuscany. The most important functions of such Institutes are
animal health care (diagnostic and research activity on the epidemiology, aetiology, pathogenesis, and prophylaxis of transmissible animal diseases) and the hygienic control of all foodstuffs of animal origin and livestock feed.
Swine breeding in Italy is mostly concentrated in northern regions (especially Lombardia and Emilia-Romagna, Piemonte and Veneto), being generally of less importance in the rest of the
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
country. In northern Italy, rearing and production systems are predominantly of the intensive and of the industrial type. Unlike the above-mentioned regions, swine breeding is a minor item in our regional livestock production, where it is mainly organised on a 'traditional' or 'rural' basis. The majority of the few existing industrial herds in Latium are located in Latina province, where the most important pork meat production and processing plants are. In this respect, it should be underlined that pork meat production, processing and consump-
tion in the Latium Region are mostly dependent upon extraregional and extra-national import activities. In consideration of the small swine population and of the lack of specific surveys on Salmonella occurrence in pigs of our region,
we addressed our investigation to a 10-year period, trying to cover the entire territory of our specific region. For a better understanding of the data presented here, we make reference to Salmonella contamination when dealing with inanimate materials, and to Salmonella colonisation and infection in healthy and diseased animals, respectively.
RESULTS
Salmonellae were detected in 12 out of the 180 herds investigated (6.6%) (Table 1), with 46 strains isolated from the
849 (5.4%) biological samples examined. In more detail, 20 Salmonella isolates were obtained from dead animals (9.3%), 4 from organs and viscera (2%), 9 from faecal samples (7.7%), and
13 from rectal swabs (4.1%) (Table 2). According to Kauffmann-White's classification scheme, these strains belonged to
the following serogroups: 39.1% to serogroup B, 13% to serogroup CI, 17.4% to serogroup C2, 6.5% to serogroup DI, and 23.9% to serogroup El. Table 2. Biological materials examined and Salmonella spp. strains isolated
from pigs in the Latium Region from 1980 tot 1989. Biological materials
Number of samples
Dead animals Organs and viscera
Salmonella spp. strains (%) 20 (9.3%)
Rectal swabs
215 200 117 317
Total
849
46 (5.4%)
Faeces
4 (2 %) 9 (7.7%) 13 (4.1%)
Salmonella typhimurium was the most frequently detected serotype, followed by S. anatum, S. bovis-morbificans, S. heidelberg, S. infantis, S. cholerae-suis, S. panama, S. augusten-
borg, S. fayed, S. enteritidis, S. oxford (Table 3). S. bovis-
MATERIALS AND METHODS
Our investigation was carried out on a total of 849 biological samples: 215 young and adult animals, referred to our Institute for necropsy; 200 abdominal (stomach, intestinal tract, mesenteric lymph nodes, liver, spleen, kidneys) and thoracic (lungs, heart) organs and viscera samples collected by local veterinarians from dead animals at their respective sties; 117 faecal samples and 317 rectal swabs collected in herd from living animals for routine parasitological and bacteriological examina-
tions. These were collected from 180 farms, 160 being of the rural and 20 of the industrial type (Table 1).
morbificans was isolated from faecal samples of seven animals from one single industrial herd in Rome province in 1985 (Table 4b). S. typhimurium was the serotype most frequently isolated
from the liver, the gastrointestinal tract and the mesenteric lymph nodes of pigs (4.2%). The serotypes predominantly recovered from single organs and viscera, from faecal samples
and rectal swabs were S. anatum (1.5% of the examined samples), S. bovis-morbificans (6% of the cultured faecal Table 3. Salmonella serotypes isolated from pigs in the Latium Region from
1980 tot 1989.
Once necropsy was performed, fresh tissue samples were collected and subsequently submitted to histopathological and microbiological examinations. For Salmonella isolation, superficial swabs were made and the
Serogroups
Serotypes
Positive
% Values of
Salmonella
samples (%)
serotype on isolated strains
following procedure was used: pre-enrichment in bufferedpeptone water at 37° C for 24 h; selective enrichment in MullerKauffmann broth at 43° C for 24 h and in selenite broth at 37° C for 24 h; culture in desoxycholate-citrate-agar, McConkey-agar,
SS-agar, and brilliant green agar at 37° C for 24 h. Colonies Table 1. Rural-and industrial-type herds checked in each single province of the Latium Region and their respective Salmonella spp. isolation values from
B
(39.1%)
CI
Ruraltype herds
Positive rural herds
Industrialtype herds
Rome Latina Frosinone Rieti Viterbo
101
8
12
Total
160
63
23
5 2
1
14
Positive industrial herds
9
THE VETER
I
26.1 10.8
5 (0.6%) 1 (0.1%)
2.2
(13.%)
3 (0.3%) 2 (0.2%) 1 (0.1%)
6.5 4.3 2.2
C2 (17.4%)
S. bovis-morbificans S. fayed
7 (0.8%) 1 (0.1%)
15.2 2.2
DI
S. panama S. enteritidis
2 (0.2%) 1 (0.1%)
4.3 2.2
El (23.9%)
S. anatum S. oxford
10 (1.2%) 1 (0.1%)
21.7 2.2
Totaal
11
46 (5.4%)
1
1
13
9
12 (1.4%)
S. infantis S. cholerae-suis" S. augustenborg
1980 tot 1989. Provinces
S. typhimurium S. heidelberg NI(*)
'1
1
20
3
() non-identified (**) var. america; var. kunzendorf
NARYQUARTERLY, VOL
1
4
,
No
.
2
,
APR
I
L
,
1
9
92
Tabel 4a. Salmonella serotypes isolated from different biological material (dead animals, organs and viscera) from pigs in the Latium Region from 1980
to 1989.
Biological materials
Serogroups
Serotypes
(%)
B (55%)
dead animals (215)
S. typhimurium S. heidelberg
NI (9 CI (20%)
S. cholerae-suis ** S. infantis S. augustenborg S. anatum S. oxford S. infantis S.anatum
El (25%)
Organs and Viscrea (200)
Positive samples
CI (25%) El (75%)
9 (4.2%) 1 (0.5%) 1 (0.5%) 2 (0.9%) 1 (0.5%) 1 (0.5%) 4 (1.9%) 1 (0.5%) 1 (0.5%) 3 (1.5%)
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
(*) non-identified (**) var. america; var. kunzendotf
DISCUSSION In our investigation, salmonellae were isolated from 5.4% of all examined samples. In this respect, it should be emphasised that a
wide range of detection rates has been observed by several authors, both in reared and regularly slaughtered pigs, with a peak incidence of 84% isolation from the mesenteric lymph nodes and caecal contents of sows slaughtered in Minnesota (19), counterbalanced by a 0.5% detection rate from faeces of extensively bred swine in Yugoslavia (12). An isolation frequency (5.32%) similar to that observed in our study has been reported for pig cadavers, internal organs, rectal
swabs, feed and washings of swine sties in Bulgaria (14). Obviously, geographical and meteorological factors, breeding systems, type of feed, animals' age and category, sampling and collection methods, along with culture techniques, can remarkably affect the isolation rate of salmonellae from material. Our relatively low Salmonella isolation frequency presumably did not depend on the cultural procedures used, since different enrichment and plating methods were used, but depended rather
upon the great number of rural-type herds compared to Tabel 4b. Salmonella serotypes isolated from different biological material (faeces, rectal swabs) from pigs in the Latium Region from 1980 to 1989.
industrial-type herds investigated in this 10-year period.
In this respect, it should be stressed that, within the many documented Salmonella transmission pathways (18), differen-
Biological materials
serogroups
Faeces
B (22.2%) C2 (77.8%)
S. typhimurium S. bovis-morbificans
2 (1.7%) 7 ( 6%)
B (38.5%)
S. typhimurium S. heidelberg
1 (0.3%) 4 (1.3%)
CI (7.7%)
S. infantis S. fayed S. panama S. enteritidis S. anatum
1 (0.3%) 1 (0.3%) 2 (0.6%) 1 (0.3%) 3 (0.9%)
(117)
Rectal Swabs (317)
serotypes
positive samples (%)
C2 (7.7%)
DI (23.1%) El (23,1%)
materials), and S. heidelberg (1.3% of the analysed rectal swabs)
(Tables 4a and 4b). Only 6 out of the 20 diagnosed Salmonella colonisations in dead animals were clinical infections, all occurring in piglets of 2 months or younger, and were caused by S. cholerae-suis (var. kunzendorj) and S. typhimurium, which were isolated from specific lesions. These included haemorrhage and hyperplasia of
different lymph nodes (particularly the mesenteric and the hepatic ones), catarrhal, haemorrhagic or diphtheroid enterocolitis, rectal stricuture (S. typhimurium-infected swine), focal or
diffuse lobular or interstitial pneumonia and, more rarely, fibrino-haemorrphagic pleuro-pericarditis. Histologically, thrombosis (disseminated intravascular coagulation) and vasculitis were frequently observed in the gut, liver, spleen, kidneys and lungs of affected animals, a number of which also showed more or less prominent interalveolar and endoalveolar flogosis in their lungs. Several piglets had variably sized haemorrhagic and necrotic foci in their liver and spleen, where more or less marked interstitial cell infiltrates, sometimes associated with fibrous thickening of interlobular septa, were occasionally seen. The main intestinal lesions included diphtheretic caecitis, colitis and, more rarely, ileitis and 'botton ulcers', while a more or less pronounced hyperplasia was often present in some lymph nodes (mesenteric and hepatic lymph nodes). No other pathogens of parasitic, bacterial, mycoplasmal, mycotic or viral nature were recovered from the animals.
64
ces seem to exist between traditional- and industrial-type piggeries and animal reservoirs such as insects, rodents, birds (poultry, pigeons, etc.), with poor hygienic and environmental conditions (temperature, humidity, etc.) being of major importance in the former rather than in the latter ones. In industrial herds, where animal movements are usually more frequent, a
number of stress conditions tend to act simultaneously, in combination with each other and with a multitude of different epidemiological factors, in facilitating Salmonella intestinal colonisation and subsequent faecal excretion. As demonstrated previously, specific transmission cycles can be
established in this way (7). In our case, poor standards of hygiene were observed in many of the rural-type herds under investigation, where industrial feed and forced ventilation were not used, and where other animal species (poultry, pigeons, cats, dogs, etc.) often lived in close cohabition with the swine. Insects, rodents and wild birds were frequently noted within such herds, where no adequate disinfections were periodically carried out. It is worth mentioning that the importance of vermin, rodents and
wild birds in maintaining specific Salmonella transmission cycles, together with the prevalence of a limited number of serotypes in a certain area, has been repeatedly emphasised (7, 17, 18). Another factor affecting our relatively low Salmonella detection
rate is presumably the overall climatic and environmental conditions in the Latium Region, which are characterised by warm, dry and long summers, with a generally low humidity throughout the year. Our data, indicating a prevalence of S. typhimurium-associated infection and colonisation cases over those caused by different serotypes, are quite in accordance with several investigations
carried out worldwide by different authors (4, 5, 10, 13). However, they differ considerably in relation to S. derby, which was never isolated in our survey despite its frequent occurrence in swine (3, 8, 19) and pork products (2, 9). In our study, S. cholerae-suis was isolated only twice, one strain belonging to the kunzendorf(monophasic variety) and the other one to the america type (biphasic variety); such a relatively low frequency seems to be in accordance with other investigations from different parts of the world (5, 19).
THE V E T E R I N A R Y Q U A R T E R L Y
,
VOL
1
4, No
.
2
,
A PR
I
L
,
1
992
As far as S. anatum, S. panama, S. heidelberg, S. infantis, and S. bovis-morbificans are concerned, their relatively large diffusion among pigs is well known; the remaining serotypes isolated by
5. Choi WP, Lee HS, and Yeo SG, et al. Epizootiological study of Salmonella infection in piggeries. I. Distribution, occurrence, serovars and biovars. Kor J Vet Res 1986; 26: 49-59. 6. Edel W, Kampelmacher EH. Epidemiological studies on Salmonella in a certain area ('Walcheren Project'). II. Salmonella in the mesenteric lymph nodes and rectal contents of normal pigs. Zbl Bakt Hyg, I Abt Orig 1976; A236: 74-82. 7. Edel W, Van Schothorst M, and Van Leusden FM, et al. Epidemiological
us (S. augustenborg, S. fayed, S. enteritidis, S. oxford), were rarely encountered, in accordance with other authors (4, 10, 13). Interestingly, we isolated S. enteritidis, an emerging serotype causing severe foodborne infections in man (11, 18), only once. With reference to gross and histological lesions, our data seem in agreement with those reported in the veterinary literature, both
studies on Salmonella in a certain area ('Walcheren Project'). III. The presence of Salmonella in man, insects, seagulls, and in food, choppingblock scrapings from butcher's shops, effluents of sewage treatment plants and drains of butcher's shops. Zbl Bakt Hyg, I Abt Orig 1978; A242: 468-
in relation to the diseased animals' age and to their causative serotypes (S. cholerae-suis, var. kunzendorf and S. typhimurium) (1).
80. 8. Jayara BM, Biro G, and Kovacs S, et al Prevalence of Salmonella serotypes
in pigs and evalutation of a rapid presumptive test for detection of
In conclusion, it should be once again stressed that many
Salmonella in pig faeces. Acta Vet Hung 1989; 37: 39-44. 9. Johnston RW, Green SS, and Chiv J, et aL Incidence of Salmonella in fresh pork sausage in 1979 compared with 1969. J Food Sci 1982; 47: 1369-71.
Salmonella transmission routes exist, a great number of which are able to reach humans. This unavoidably raises the need to
10. Lammerding AM, Garcia MM, and Mann ED, et aL Prevalence of
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
implement, simultaneously, several preventive measures in different fields. One possible approach is that related to the
Salmonella and thermophilic Campylobacter in fresh pork, beef veal and poultry in Canada. J Food Prot 1988; 51: 47-52. 11 . Lin F-YC, Morris JG, and Trump D, el aL Investigation of an outbreak of
production of Salmonella-free animals, which has been proven to be profitable in pig fattening, although it does not seem to be feasible under practical circumstances (15, 16). A World Health
Salmonella enteritidis gastroenteritis associated with consumption of eggs in
a restaurant chain in Maryland. Am J Epidemiol 1988; 128: 839-44. 12. Markovic BS, StojkoviC-Atanackovié M, and Popovic M. Salmonella in the faeces and mesenteric lymph nodes of swine under extensive conditions. Veterinarski Glasnik 1985; 39: 811-4.
Organisation report (21) indicates three different lines of defence against Salmonella food-borne infections, namely (a) the production of Salmonella-free-animals, (b) the enforcement of hygiene in the slaughterhouses, and (c) public education on food preparation and storage. Undoubtedly, such concepts are valid on a global scale, since the Salmonella problem is a world problem and it would be a nonsense to face it at a national or,
13. Mc Kinley GA, Fagerberg DJ, and Quarles CL, et al Incidence of salmonellae in fecal samples of production swine and swine at slaughter plants in the United States in 1978. Appl Environ Microbiol 1980; 40: 5626.
14. Minev MK, Iordanov S, and Konov V, et al Etiology of salmonellosis in swine raised commercially. Vet Med Nauki 1987; 24: 26-31. 15. Oosterom J, Van Erne EHW, and Van Schothorst M. Epidemiological
even worse, at a regional or territorial level. This will also imply, as a consequence, that other human foodborne infections caused by pathogens such as Campylobacterjejuni, Yersinia enterocolitica, Listeria monocytogenes, Clostridium bowlinum and E. coli, which share epidemiological similarities with the genus Salmonella, will benefit from these preventive actions, with a more or less evident reduction in the number of cases annually reported in the general population.
studies on Salmonella in a certain area ('Walcheren Project'). V. Studies into the possibility of fattening pigs free from Salmonella. Zbl Bakt Hyg, I Abt
Orig 1982; A252: 490-506.
16. Oosterom J, Notermans S. Further research into the possibility of Salmonella-free fattening and slaughter of pigs. J Hyg 1983; 91: 59-69. 17. Oosterom J. Epidemiological studies on Salmonella and Campylobacter je juni. Vet Quart 1987; 9: 348-55. 18. Oosterom J. Epidemiological studies and proposed preventive measures in the fight against human salmonellosis. Int J Food Microbiol 1991; 12: 4152.
ACKNOWLEDGEMENTS
19. Tay SCK, Robinson RA, and Pullen MM. Salmonella in the mesenteric lymph nodes and cecal contents of slaughtered sows. J Food Prot 1989; 52: 202-3. 20. Todd ECD. Preliminary estimates of costs of foodbome disease in Canada and costs to reduce salmonellosis. J Food Prot 1989; 52: 586-94. 21. World Health Organization (WHO). Report of the WHO/WAVFH roundtable conference on the present status of the Salmonella problem (prevention and control), VP/81.27, Bilthoven, The Netherlands, October 6-10
We wish to thank Dr. Johannes Oosterom, DVM, PhD, Royal Gist-brocades, Research and Development, P. O. Box 1, 2600 MA Delft, The Netherlands, for expert revision of the manuscript.
REFERENCES 1. Barker IK, Dreumel AA van. The Alimentary System. In: Pathology of Domestic Animals, KVF Jubb, PC Kennedy, and N Palmer eds, Vol 2, 3rd ed, Academic Press, Inc, San Diego, California, USA, 1985: 1-237. 2. Banks JG, Board RG. The incidence and level of contamination of British
1980.
22. World Health Organization (WHO). Salmonellosis control: the role of animal and product hygiene. WHO Technical Report Series 774, Geneva,
fresh sausages and ingredients with salmonellas. J Hyg Camb 1983; 90: 21323.
1988; 1-83.
3. Bontempi M, Zavanella M. Salmonella carriers among the normal
23. World Health Organization (WHO). Report of WHO consultation on salmonellosis control in agriculture. WHO/CDS/VPH/90.94, Orvieto,
slaughtered pigs. Giorn Mal Inf Parass 1979; 31: 156-7. 4. Cantoni C, D'Aubert S. Food contamination by salmonellae, particularly in fresh sausages. Industrie Alimentari 1976; 15: 111-22.
Italy, April 9-12 1990.
ERRATA The Veterinary Quarterly 1992; 14(1): 39-40
'Peripartum changes in antibody producing capability of lymphocytes from dairy cows% by II. Nagahata, A. Ogawa, Y. Sanada, II. Noda, and S. Yamamoto.
Page:
Text:
39.
line 3 from top, left column (in summary)
periparturiment
39.
line 9 from bottom, left column
parturition at parturition,
40.
Table I, left column, line 2 from top
ly mphococytes
65
Read:
periparturient ...
parturition, at parturition.... lymphocytes
TI1E VETERINARY QUARTERLY, VOL 1 4 ,.11o.
2
,
APRIL, 1 9 9 2
Veterinary Quarterly Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tveq20
Occurrence of Salmonella in swine in the Latium Region (central Italy) from 1980 to 1989: A retrospective study a
a
a
a
a
G. Di Guardo , G. Fontanelli , G. Panfili , R. Condoleo , L. De Grossi , A. M. a
Brozzi & A. I. Bozzano
a
a
Instituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana , Via Appia Nuova, Rome, 1411–00178, Italy Published online: 01 Nov 2011.
To cite this article: G. Di Guardo , G. Fontanelli , G. Panfili , R. Condoleo , L. De Grossi , A. M. Brozzi & A. I. Bozzano (1992) Occurrence of Salmonella in swine in the Latium Region (central Italy) from 1980 to 1989: A retrospective study, Veterinary Quarterly, 14:2, 62-65, DOI: 10.1080/01652176.1992.9694331 To link to this article: http://dx.doi.org/10.1080/01652176.1992.9694331
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
abnormalities in slaughtered pigs. Vet Quarterly 1990; 12: 146-51. , 33. Statistical Analysis Systems (SAS). SAS Institute Inc., Cary, NC, USA Statistics and Basics User's Guides (1985). 34. Tie len MJM. Incidence and the prevention by animal care of lung and liver
38. Tumbleson ME, Schmidt DA and Scholl E. Hematology and clinical
affections of fattening pigs. PhD-thesis, Agric. University Wageningen, The Netherlands, 1974: 141 pp. 35. Tie len MJM and Elbers ARW. Experiences with Integrated Chain Control for pig production in the Netherlands. Proc 6th Int Congr on Anim Hygiene, 14-17 June 1988, Skara, Sweden. Ed. Ekesbo I. Vol.I.: 227-31. 36. Tolling KT. Age dependent variation of serum creatine kinase isoenzyme levels in pigs. J Vet Med (A) 1982; 29: 420-8.
39. Ubaldi A. Biochemical parameters of pigs in intensive breeding. In:
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
37. Travnicek L and Mandel L. Haematology of conventional and germfree miniature Minnasota piglets. II. Serum proteins and immunoglobulins. Z Versuchstierk 1982; 24: 308-17.
chemistry. In 'Diseases of Swine'. Eds. Leman AD, Straw B, Glock RD, Mengeling WL, Penny RHC and Scholl E. Iowa State University Press, Ames, Iowa, USA, 1988: 27-44.
'Research and results in Clinical Chemistry of Domestic Animals'. Ed. Sommer, H., Institute of Anatomy and Physiology, Bonn,Germany, 1983:
307-16. 40. Willeberg P, Gerbola MA, Kirkegaard Petersen B, and Andersen JB. The
Danish Pig Health Scheme
:
Nationwide Computer-based Abattoir
Surveillance and follow-up at the Herd Level. Prey Vet Med 1984;3:79-91. 41. Wilson GDA, Harvey DG, and Snook CR. A review of factors affecting blood biochemistry in the pig. Br Vet J 1972; 128: 596-609.
OCCURRENCE OF SALMONELLA IN SWINE IN THE LATIUM REGION (CENTRAL ITALY) FROM 1980 TO 1989: A RETROSPECTIVE STUDY G. Di Guardo, G. Fontanelli, G. Panfili, R. Condoleo, L. De Grossi, A. M. Brozzi, and A. I. Bozzano1 Veterinary Quarterly 1992; 14: 62-5
SUMMARY An extensive survey was carried out on 849 biological samples (dead animals, organs and viscera, faeces, and rectal swabs) from pigs in the Latium Region (Central Italy) throughout the years 1980-1989. In total 46 of the samples (5.4%) were found to be bacteriologically positive for salmonellae. Among dead
animals, typical gross lesions were observed in 6 clinically infected animals.
As far as serotypes are concerned 11 different ones were isolated with a predominance of Salmonella typhimurium (26.1%), S. anatum (21.7%), S. bovis-morbificans (15.2%), and S. heidelberg (10.8%). According to Kauffmann-White's classi-
fication scheme, 39.1% of the isolated strains belonged to serogroup B, 13% to serogroup C 1, 17.4% tot serogroup C2, 6.5% to serogroup D, and 23.9% to serogroup El.
In conclusion, the authors speculate that the relatively low Salmonella isolation frequency (5.4%) reported in this study was not dependent upon the cultural procedures used since different enrichment and plating methods were used, but rather upon the great number of rural-type herds which were investigated over the decade compared to industrial-type herds. Otherfactors such
as stress conditions, which are particularly pronounced in
industrial-type herds, and overall climatic situations, which tend
to be characterised by warm, dry and long summers in the Latium Region, are also considered in this respect. INTRODUCTION
Salmonella infections rank among the most important causes of bacterial enteritis in humans, in spite of a generally accepted underreporting, amounting up to 95% in some countries (20). At present, salmonellosis is considered, along with campylobacteri-' osis, one of the two most prevalent reported foodborne zoonoses I
Instituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana, Via Appia Nuova, I411-00178-Rome, Italy.
62
in developed countries (22), being mainly related to the consumption of contaminated meat and other foodstuffs of animal origin (18). In this regard, pork meat and pork meatbased products are frequent sources of Salmonella infection in man (22). Animals are known to play a major role as hosts and vectors of a
variety of zoonotic Salmonella serotypes, which are often asymptomatically carried by them (22). Carrier status frequently occurs in poultry and pigs, with special reference to industrial breeding and production plants (6). In particular, swine can often carry Salmonella in both the intestinal tract and the mesenteric lymph nodes (15). Modern slaughter procedures potentially involve many risks of
both direct and cross-contamination of carcasses and meat surfaces. Cross contamination with pathogenic bacteria (i.e. Salmonella) during slaughter is much more pronounced with pork and poultry carcasses than with beef and sheep carcasses
(23). In modern slaughter lines, Salmonella contamination and crosscontamination of pig carcasses, as well as of the surrounding
environment and slaughter equipment, can especially occur during the evisceration process if this is not carried out properly (22). Surface contamination is further spread during the subsequent chilling, portioning, packaging, and distribution of the meat or meat products. The aim of the present work was to evaluate retrospectively the prevalence and distribution of Salmonella among.pigs reared in
the Latium Region (Central Italy), comparing our data with those previously obtained by other investigators. For this purpose, data were obtained from our Institute's diagnostic
laboratories from 1980 to 1989. Briefly, our Institute (Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana) is a public health organisation placed under the official control of
THEVETERINARYQU ARTERLY, VOL
1
4, No. 2, APRI
L
,
1
992
the Regional Authority. There are nine other such Institutes nationally, each of them being in charge of one, two or three of
were then cultured in TSI-agar at 37° C for 24 h and finally identified and serotyped by using routine biochemical and
the 20 Italian Regions. Our Institute covers Latium and
seroagglutination techniques.
Tuscany. The most important functions of such Institutes are
animal health care (diagnostic and research activity on the epidemiology, aetiology, pathogenesis, and prophylaxis of transmissible animal diseases) and the hygienic control of all foodstuffs of animal origin and livestock feed.
Swine breeding in Italy is mostly concentrated in northern regions (especially Lombardia and Emilia-Romagna, Piemonte and Veneto), being generally of less importance in the rest of the
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
country. In northern Italy, rearing and production systems are predominantly of the intensive and of the industrial type. Unlike the above-mentioned regions, swine breeding is a minor item in our regional livestock production, where it is mainly organised on a 'traditional' or 'rural' basis. The majority of the few existing industrial herds in Latium are located in Latina province, where the most important pork meat production and processing plants are. In this respect, it should be underlined that pork meat production, processing and consump-
tion in the Latium Region are mostly dependent upon extraregional and extra-national import activities. In consideration of the small swine population and of the lack of specific surveys on Salmonella occurrence in pigs of our region,
we addressed our investigation to a 10-year period, trying to cover the entire territory of our specific region. For a better understanding of the data presented here, we make reference to Salmonella contamination when dealing with inanimate materials, and to Salmonella colonisation and infection in healthy and diseased animals, respectively.
RESULTS
Salmonellae were detected in 12 out of the 180 herds investigated (6.6%) (Table 1), with 46 strains isolated from the
849 (5.4%) biological samples examined. In more detail, 20 Salmonella isolates were obtained from dead animals (9.3%), 4 from organs and viscera (2%), 9 from faecal samples (7.7%), and
13 from rectal swabs (4.1%) (Table 2). According to Kauffmann-White's classification scheme, these strains belonged to
the following serogroups: 39.1% to serogroup B, 13% to serogroup CI, 17.4% to serogroup C2, 6.5% to serogroup DI, and 23.9% to serogroup El. Table 2. Biological materials examined and Salmonella spp. strains isolated
from pigs in the Latium Region from 1980 tot 1989. Biological materials
Number of samples
Dead animals Organs and viscera
Salmonella spp. strains (%) 20 (9.3%)
Rectal swabs
215 200 117 317
Total
849
46 (5.4%)
Faeces
4 (2 %) 9 (7.7%) 13 (4.1%)
Salmonella typhimurium was the most frequently detected serotype, followed by S. anatum, S. bovis-morbificans, S. heidelberg, S. infantis, S. cholerae-suis, S. panama, S. augusten-
borg, S. fayed, S. enteritidis, S. oxford (Table 3). S. bovis-
MATERIALS AND METHODS
Our investigation was carried out on a total of 849 biological samples: 215 young and adult animals, referred to our Institute for necropsy; 200 abdominal (stomach, intestinal tract, mesenteric lymph nodes, liver, spleen, kidneys) and thoracic (lungs, heart) organs and viscera samples collected by local veterinarians from dead animals at their respective sties; 117 faecal samples and 317 rectal swabs collected in herd from living animals for routine parasitological and bacteriological examina-
tions. These were collected from 180 farms, 160 being of the rural and 20 of the industrial type (Table 1).
morbificans was isolated from faecal samples of seven animals from one single industrial herd in Rome province in 1985 (Table 4b). S. typhimurium was the serotype most frequently isolated
from the liver, the gastrointestinal tract and the mesenteric lymph nodes of pigs (4.2%). The serotypes predominantly recovered from single organs and viscera, from faecal samples
and rectal swabs were S. anatum (1.5% of the examined samples), S. bovis-morbificans (6% of the cultured faecal Table 3. Salmonella serotypes isolated from pigs in the Latium Region from
1980 tot 1989.
Once necropsy was performed, fresh tissue samples were collected and subsequently submitted to histopathological and microbiological examinations. For Salmonella isolation, superficial swabs were made and the
Serogroups
Serotypes
Positive
% Values of
Salmonella
samples (%)
serotype on isolated strains
following procedure was used: pre-enrichment in bufferedpeptone water at 37° C for 24 h; selective enrichment in MullerKauffmann broth at 43° C for 24 h and in selenite broth at 37° C for 24 h; culture in desoxycholate-citrate-agar, McConkey-agar,
SS-agar, and brilliant green agar at 37° C for 24 h. Colonies Table 1. Rural-and industrial-type herds checked in each single province of the Latium Region and their respective Salmonella spp. isolation values from
B
(39.1%)
CI
Ruraltype herds
Positive rural herds
Industrialtype herds
Rome Latina Frosinone Rieti Viterbo
101
8
12
Total
160
63
23
5 2
1
14
Positive industrial herds
9
THE VETER
I
26.1 10.8
5 (0.6%) 1 (0.1%)
2.2
(13.%)
3 (0.3%) 2 (0.2%) 1 (0.1%)
6.5 4.3 2.2
C2 (17.4%)
S. bovis-morbificans S. fayed
7 (0.8%) 1 (0.1%)
15.2 2.2
DI
S. panama S. enteritidis
2 (0.2%) 1 (0.1%)
4.3 2.2
El (23.9%)
S. anatum S. oxford
10 (1.2%) 1 (0.1%)
21.7 2.2
Totaal
11
46 (5.4%)
1
1
13
9
12 (1.4%)
S. infantis S. cholerae-suis" S. augustenborg
1980 tot 1989. Provinces
S. typhimurium S. heidelberg NI(*)
'1
1
20
3
() non-identified (**) var. america; var. kunzendorf
NARYQUARTERLY, VOL
1
4
,
No
.
2
,
APR
I
L
,
1
9
92
Tabel 4a. Salmonella serotypes isolated from different biological material (dead animals, organs and viscera) from pigs in the Latium Region from 1980
to 1989.
Biological materials
Serogroups
Serotypes
(%)
B (55%)
dead animals (215)
S. typhimurium S. heidelberg
NI (9 CI (20%)
S. cholerae-suis ** S. infantis S. augustenborg S. anatum S. oxford S. infantis S.anatum
El (25%)
Organs and Viscrea (200)
Positive samples
CI (25%) El (75%)
9 (4.2%) 1 (0.5%) 1 (0.5%) 2 (0.9%) 1 (0.5%) 1 (0.5%) 4 (1.9%) 1 (0.5%) 1 (0.5%) 3 (1.5%)
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
(*) non-identified (**) var. america; var. kunzendotf
DISCUSSION In our investigation, salmonellae were isolated from 5.4% of all examined samples. In this respect, it should be emphasised that a
wide range of detection rates has been observed by several authors, both in reared and regularly slaughtered pigs, with a peak incidence of 84% isolation from the mesenteric lymph nodes and caecal contents of sows slaughtered in Minnesota (19), counterbalanced by a 0.5% detection rate from faeces of extensively bred swine in Yugoslavia (12). An isolation frequency (5.32%) similar to that observed in our study has been reported for pig cadavers, internal organs, rectal
swabs, feed and washings of swine sties in Bulgaria (14). Obviously, geographical and meteorological factors, breeding systems, type of feed, animals' age and category, sampling and collection methods, along with culture techniques, can remarkably affect the isolation rate of salmonellae from material. Our relatively low Salmonella isolation frequency presumably did not depend on the cultural procedures used, since different enrichment and plating methods were used, but depended rather
upon the great number of rural-type herds compared to Tabel 4b. Salmonella serotypes isolated from different biological material (faeces, rectal swabs) from pigs in the Latium Region from 1980 to 1989.
industrial-type herds investigated in this 10-year period.
In this respect, it should be stressed that, within the many documented Salmonella transmission pathways (18), differen-
Biological materials
serogroups
Faeces
B (22.2%) C2 (77.8%)
S. typhimurium S. bovis-morbificans
2 (1.7%) 7 ( 6%)
B (38.5%)
S. typhimurium S. heidelberg
1 (0.3%) 4 (1.3%)
CI (7.7%)
S. infantis S. fayed S. panama S. enteritidis S. anatum
1 (0.3%) 1 (0.3%) 2 (0.6%) 1 (0.3%) 3 (0.9%)
(117)
Rectal Swabs (317)
serotypes
positive samples (%)
C2 (7.7%)
DI (23.1%) El (23,1%)
materials), and S. heidelberg (1.3% of the analysed rectal swabs)
(Tables 4a and 4b). Only 6 out of the 20 diagnosed Salmonella colonisations in dead animals were clinical infections, all occurring in piglets of 2 months or younger, and were caused by S. cholerae-suis (var. kunzendorj) and S. typhimurium, which were isolated from specific lesions. These included haemorrhage and hyperplasia of
different lymph nodes (particularly the mesenteric and the hepatic ones), catarrhal, haemorrhagic or diphtheroid enterocolitis, rectal stricuture (S. typhimurium-infected swine), focal or
diffuse lobular or interstitial pneumonia and, more rarely, fibrino-haemorrphagic pleuro-pericarditis. Histologically, thrombosis (disseminated intravascular coagulation) and vasculitis were frequently observed in the gut, liver, spleen, kidneys and lungs of affected animals, a number of which also showed more or less prominent interalveolar and endoalveolar flogosis in their lungs. Several piglets had variably sized haemorrhagic and necrotic foci in their liver and spleen, where more or less marked interstitial cell infiltrates, sometimes associated with fibrous thickening of interlobular septa, were occasionally seen. The main intestinal lesions included diphtheretic caecitis, colitis and, more rarely, ileitis and 'botton ulcers', while a more or less pronounced hyperplasia was often present in some lymph nodes (mesenteric and hepatic lymph nodes). No other pathogens of parasitic, bacterial, mycoplasmal, mycotic or viral nature were recovered from the animals.
64
ces seem to exist between traditional- and industrial-type piggeries and animal reservoirs such as insects, rodents, birds (poultry, pigeons, etc.), with poor hygienic and environmental conditions (temperature, humidity, etc.) being of major importance in the former rather than in the latter ones. In industrial herds, where animal movements are usually more frequent, a
number of stress conditions tend to act simultaneously, in combination with each other and with a multitude of different epidemiological factors, in facilitating Salmonella intestinal colonisation and subsequent faecal excretion. As demonstrated previously, specific transmission cycles can be
established in this way (7). In our case, poor standards of hygiene were observed in many of the rural-type herds under investigation, where industrial feed and forced ventilation were not used, and where other animal species (poultry, pigeons, cats, dogs, etc.) often lived in close cohabition with the swine. Insects, rodents and wild birds were frequently noted within such herds, where no adequate disinfections were periodically carried out. It is worth mentioning that the importance of vermin, rodents and
wild birds in maintaining specific Salmonella transmission cycles, together with the prevalence of a limited number of serotypes in a certain area, has been repeatedly emphasised (7, 17, 18). Another factor affecting our relatively low Salmonella detection
rate is presumably the overall climatic and environmental conditions in the Latium Region, which are characterised by warm, dry and long summers, with a generally low humidity throughout the year. Our data, indicating a prevalence of S. typhimurium-associated infection and colonisation cases over those caused by different serotypes, are quite in accordance with several investigations
carried out worldwide by different authors (4, 5, 10, 13). However, they differ considerably in relation to S. derby, which was never isolated in our survey despite its frequent occurrence in swine (3, 8, 19) and pork products (2, 9). In our study, S. cholerae-suis was isolated only twice, one strain belonging to the kunzendorf(monophasic variety) and the other one to the america type (biphasic variety); such a relatively low frequency seems to be in accordance with other investigations from different parts of the world (5, 19).
THE V E T E R I N A R Y Q U A R T E R L Y
,
VOL
1
4, No
.
2
,
A PR
I
L
,
1
992
As far as S. anatum, S. panama, S. heidelberg, S. infantis, and S. bovis-morbificans are concerned, their relatively large diffusion among pigs is well known; the remaining serotypes isolated by
5. Choi WP, Lee HS, and Yeo SG, et al. Epizootiological study of Salmonella infection in piggeries. I. Distribution, occurrence, serovars and biovars. Kor J Vet Res 1986; 26: 49-59. 6. Edel W, Kampelmacher EH. Epidemiological studies on Salmonella in a certain area ('Walcheren Project'). II. Salmonella in the mesenteric lymph nodes and rectal contents of normal pigs. Zbl Bakt Hyg, I Abt Orig 1976; A236: 74-82. 7. Edel W, Van Schothorst M, and Van Leusden FM, et al. Epidemiological
us (S. augustenborg, S. fayed, S. enteritidis, S. oxford), were rarely encountered, in accordance with other authors (4, 10, 13). Interestingly, we isolated S. enteritidis, an emerging serotype causing severe foodborne infections in man (11, 18), only once. With reference to gross and histological lesions, our data seem in agreement with those reported in the veterinary literature, both
studies on Salmonella in a certain area ('Walcheren Project'). III. The presence of Salmonella in man, insects, seagulls, and in food, choppingblock scrapings from butcher's shops, effluents of sewage treatment plants and drains of butcher's shops. Zbl Bakt Hyg, I Abt Orig 1978; A242: 468-
in relation to the diseased animals' age and to their causative serotypes (S. cholerae-suis, var. kunzendorf and S. typhimurium) (1).
80. 8. Jayara BM, Biro G, and Kovacs S, et al Prevalence of Salmonella serotypes
in pigs and evalutation of a rapid presumptive test for detection of
In conclusion, it should be once again stressed that many
Salmonella in pig faeces. Acta Vet Hung 1989; 37: 39-44. 9. Johnston RW, Green SS, and Chiv J, et aL Incidence of Salmonella in fresh pork sausage in 1979 compared with 1969. J Food Sci 1982; 47: 1369-71.
Salmonella transmission routes exist, a great number of which are able to reach humans. This unavoidably raises the need to
10. Lammerding AM, Garcia MM, and Mann ED, et aL Prevalence of
Downloaded by [University of Nebraska, Lincoln] at 03:19 21 October 2014
implement, simultaneously, several preventive measures in different fields. One possible approach is that related to the
Salmonella and thermophilic Campylobacter in fresh pork, beef veal and poultry in Canada. J Food Prot 1988; 51: 47-52. 11 . Lin F-YC, Morris JG, and Trump D, el aL Investigation of an outbreak of
production of Salmonella-free animals, which has been proven to be profitable in pig fattening, although it does not seem to be feasible under practical circumstances (15, 16). A World Health
Salmonella enteritidis gastroenteritis associated with consumption of eggs in
a restaurant chain in Maryland. Am J Epidemiol 1988; 128: 839-44. 12. Markovic BS, StojkoviC-Atanackovié M, and Popovic M. Salmonella in the faeces and mesenteric lymph nodes of swine under extensive conditions. Veterinarski Glasnik 1985; 39: 811-4.
Organisation report (21) indicates three different lines of defence against Salmonella food-borne infections, namely (a) the production of Salmonella-free-animals, (b) the enforcement of hygiene in the slaughterhouses, and (c) public education on food preparation and storage. Undoubtedly, such concepts are valid on a global scale, since the Salmonella problem is a world problem and it would be a nonsense to face it at a national or,
13. Mc Kinley GA, Fagerberg DJ, and Quarles CL, et al Incidence of salmonellae in fecal samples of production swine and swine at slaughter plants in the United States in 1978. Appl Environ Microbiol 1980; 40: 5626.
14. Minev MK, Iordanov S, and Konov V, et al Etiology of salmonellosis in swine raised commercially. Vet Med Nauki 1987; 24: 26-31. 15. Oosterom J, Van Erne EHW, and Van Schothorst M. Epidemiological
even worse, at a regional or territorial level. This will also imply, as a consequence, that other human foodborne infections caused by pathogens such as Campylobacterjejuni, Yersinia enterocolitica, Listeria monocytogenes, Clostridium bowlinum and E. coli, which share epidemiological similarities with the genus Salmonella, will benefit from these preventive actions, with a more or less evident reduction in the number of cases annually reported in the general population.
studies on Salmonella in a certain area ('Walcheren Project'). V. Studies into the possibility of fattening pigs free from Salmonella. Zbl Bakt Hyg, I Abt
Orig 1982; A252: 490-506.
16. Oosterom J, Notermans S. Further research into the possibility of Salmonella-free fattening and slaughter of pigs. J Hyg 1983; 91: 59-69. 17. Oosterom J. Epidemiological studies on Salmonella and Campylobacter je juni. Vet Quart 1987; 9: 348-55. 18. Oosterom J. Epidemiological studies and proposed preventive measures in the fight against human salmonellosis. Int J Food Microbiol 1991; 12: 4152.
ACKNOWLEDGEMENTS
19. Tay SCK, Robinson RA, and Pullen MM. Salmonella in the mesenteric lymph nodes and cecal contents of slaughtered sows. J Food Prot 1989; 52: 202-3. 20. Todd ECD. Preliminary estimates of costs of foodbome disease in Canada and costs to reduce salmonellosis. J Food Prot 1989; 52: 586-94. 21. World Health Organization (WHO). Report of the WHO/WAVFH roundtable conference on the present status of the Salmonella problem (prevention and control), VP/81.27, Bilthoven, The Netherlands, October 6-10
We wish to thank Dr. Johannes Oosterom, DVM, PhD, Royal Gist-brocades, Research and Development, P. O. Box 1, 2600 MA Delft, The Netherlands, for expert revision of the manuscript.
REFERENCES 1. Barker IK, Dreumel AA van. The Alimentary System. In: Pathology of Domestic Animals, KVF Jubb, PC Kennedy, and N Palmer eds, Vol 2, 3rd ed, Academic Press, Inc, San Diego, California, USA, 1985: 1-237. 2. Banks JG, Board RG. The incidence and level of contamination of British
1980.
22. World Health Organization (WHO). Salmonellosis control: the role of animal and product hygiene. WHO Technical Report Series 774, Geneva,
fresh sausages and ingredients with salmonellas. J Hyg Camb 1983; 90: 21323.
1988; 1-83.
3. Bontempi M, Zavanella M. Salmonella carriers among the normal
23. World Health Organization (WHO). Report of WHO consultation on salmonellosis control in agriculture. WHO/CDS/VPH/90.94, Orvieto,
slaughtered pigs. Giorn Mal Inf Parass 1979; 31: 156-7. 4. Cantoni C, D'Aubert S. Food contamination by salmonellae, particularly in fresh sausages. Industrie Alimentari 1976; 15: 111-22.
Italy, April 9-12 1990.
ERRATA The Veterinary Quarterly 1992; 14(1): 39-40
'Peripartum changes in antibody producing capability of lymphocytes from dairy cows% by II. Nagahata, A. Ogawa, Y. Sanada, II. Noda, and S. Yamamoto.
Page:
Text:
39.
line 3 from top, left column (in summary)
periparturiment
39.
line 9 from bottom, left column
parturition at parturition,
40.
Table I, left column, line 2 from top
ly mphococytes
65
Read:
periparturient ...
parturition, at parturition.... lymphocytes
TI1E VETERINARY QUARTERLY, VOL 1 4 ,.11o.
2
,
APRIL, 1 9 9 2
