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Prevalence of Campylobacter spp. in poultry and poultry meat in Germany
International Journal of Food Microbiology 51 (1999) 187–190 www.elsevier.nl / locate / ijfoodmicro
Short communication
Prevalence of Campylobacter spp. in poultry and poultry meat in Germany Viktoria Atanassova*, Christian Ring Veterinary University Hannover, Centre for Food Sciences, Department of Food Hygiene and Microbiology, Bischofsholer Damm 15, 30173 Hannover, Germany Received 15 March 1999; accepted 2 August 1999
Abstract Of 509 samples from poultry flocks, 209 isolates (41.1%) were Campylobacter positive. The number of positive cases in broiler carcasses was 45.9%. Of 52 pheasants investigated, 25.9% were Campylobacter positive. Campylobacter jejuni was isolated from 86 (42.0%) poultry flock samples, 47 (43%) broiler samples and 15 (28%) wild pheasant samples. C. coli was found at a rate of 1.2% in poultry flocks, 13% in broilers and 21% in pheasants. 1999 Elsevier Science B.V. All rights reserved. Keywords: Campylobacter; C. jejuni; C. coli; Poultry; Poultry meat
1. Introduction Results of studies on clinical Campylobacter cases in humans show a growing tendency (De Boer and Hahne, 1990; Jones et al., 1991a and b). In several European countries, Campylobacter pathogenic to man have been isolated more frequently than Salmonella (Humphrey et al., 1993; Bryan and Doyle, 1995). Tokumaru et al. (1991) reported that in Japan more Campylobacter than Salmonella are detected during the slaughter and cutting processes. In Germany, campylobacteriosis is the second most frequent cause of gastrointestinal infections *Corresponding author. Tel.: 1 49-511-856-7517; fax: 1 49511-856-7678.
(Dedie` et al., 1993). Campylobacter enteritis is a disease mainly taken up with food. In contrast to other bacterial enteritis agents, an increase of Campylobacter populations in foodstuffs is unlikely. Important sources of infection are inadequately heated poultry meat, poultry liver and cross-contamination of foodstuff through lack of kitchen hygiene (Skirrow, 1982; Skirrow and Blaser, 1992; Oosterom, 1994). From the food hygiene point of view, poultry thus plays an important role in the transmission of Campylobacter to man. In fresh poultry meat, the rate of contamination is 0–100% (Hood et al., 1988; Jones et al., 1991a and b; Karib and Seeger, 1994; Lee et al., 1994). Campylobacter was isolated mainly from the skin, the neck skin and the breast musculature, with
0168-1605 / 99 / $ – see front matter 1999 Elsevier Science B.V. All rights reserved. PII: S0168-1605( 99 )00120-8
188
V. Atanassova, C. Ring / International Journal of Food Microbiology 51 (1999) 187 – 190
bacterial counts of 1.5 3 10 3 –1.5 3 10 6 KbE / g per animal (Hood et al.,1988; Humphrey et al., 1993). Poultry offal (liver, heart and stomach) can generally also be contaminated with Campylobacter. Christopher et al. (1982) reported that 50% of investigated livers were contaminated with Campylobacter. During the slaughter process, damage to the intestinal tract can lead to direct contamination. Contamination can also occur indirectly through air, since during both defeathering and evisceration up to 10 4 KbE / m 3 have been demonstrated (Oosterom et al., 1983; Jones et al., 1991a and b).
2. Materials and Methods
2.1. Poultry and pheasant samples In a study in Germany during a period of three years (1995–1997), samples were obtained from 12 poultry flocks, 2 poultry slaughter plants, as well as from 52 hunted pheasants and investigated for the presence of Campylobacter. The investigations were carried out in the periods November to December. From poultry flocks, which were three-weeks-old, smear samples were taken from five randomly chosen animals one week prior to slaughter, and after slaughter or post-mortem investigation, a caecal and a liver sample were also taken. In slaughter plants, samples were taken from the skin, liver and the neck of slaughtered broilers. From the pheasants, samples were taken from the skin, caecum and liver.
2.2. Isolation and identification of Campylobacter Culturing was done by the Campylobacter-Enrichment-Bouillon No.2 (Oxoid No. CM 67) and Preston Campylobacter Selective Agar (PA, Oxoid CM 689). Each of them were supplemented with 5% (v / v)
saponine-lysed horse blood and Campylobacter Selective Supplement (Oxoid No.SR 1 117). The samples in Campylobacter Enrichment Bouillon were incubated for 24h at 378C and 24h at 428C; the culture was streaked onto a PA plate, which was incubated for 48h at 378C and 428C in a microaerobic environment. From each positive agar plate, one typical Campylobacter colony was subcultured and tested for Gram-staining, motility, production of oxidase and catalase and hippurate hydrolysis. All Campylobacter strains were frozen at 2 708C in Brain Heart Infusion (Difco 0037-17-8) with 17% (v / v) glycerol, awaiting biochemical tests (api Campy Ref 20890, ` bio Merieux). The Campylobacter isolates were also serotyped according to the Penner method (Penner and Hennessy, 1980).
3. Results and discussion The results of demonstrating the presence of Campylobacter in poultry flocks, slaughtered broilers and wild pheasants are shown in Table 1. Out of a total of 509 samples taken from poultry flocks, 209 isolates could be classified as Campylobacter. From 111 broiler samples, 51 (45.9%) were Campylobacter positive, and from 52 wild pheasants, 14 (25.9%) were positive. Campylobacter jejuni biotype II was the most frequent isolate from wild pheasants (69.5%) and from broilers (46.0%). C. jejuni biotype I was predominant in isolates from poultry flocks (54.5%). Campylobacter coli most frequently was isolated (1.2%) from poultry flocks. In the group of other Campylobacter spp. we identified Campylobacter sputorum subsp. faecalis, Campylobacter cryaerophila and Campylobacter upsaliensis. The detection rate in three-week-old cockerels (41.4%) and in slaughtered broilers (45.9%) is
Table 1 Campylobacter in poultry production Sample source
No. of samples analysed
Campylobacter positive isolates
Campylobacter positive (%)
Poultry flocks Broilers Wild pheasants
509 111 52
209 51 14
41.4 45.9 25.9
V. Atanassova, C. Ring / International Journal of Food Microbiology 51 (1999) 187 – 190
similar to data from the UK and Northern Ireland, with 41% Campylobacter positive poultry meat (Bryan and Doyle, 1995; Madden et al., 1996; Bolton, 1996). Sources of contamination and routes of infection with Campylobacter are important for poultry fattening units. Transmission of Campylobacter from egg to chick is not typical (Doyle, 1984; Baker et al., 1987). Infection and horizontal transmissions from one living animal to the other are of particular significance for the rate of detection of Campylobacter in poultry production. Very few infected animals can be the source of infection for the whole herd (Shanker et al., 1990). Because of the widespread use of air-conditioning in pens, with optimal temperatures and humidity, seasonal influences on the spread of Campylobacter in production units hardly play a role. Where the inside climate cannot be standardised throughout the year, a higher incidence of Campylobacter is observed in May and October (Doyle, 1984; Arwana, 1987; Wallance et al., 1997). Investigations at poultry slaughtering plants showed that there are many opportunities for contamination of carcasses (Oosterom et al., 1983; Jones et al., 1991a and b). The slaughtering plant is an important station for contamination with Campylobacter, as can be seen from the observation that the rate of isolation from carcasses is several times higher than from animals entering plants (Hartog and De Boer, 1982; Izat et al., 1988; Jones et al., 1991a and b). Our results from 111 slaughtered broilers found positive for Campylobacter (45.9%) correspond to results in literature (Park et al., 1981; Oosterom et al., 1983; Lee et al., 1994). It is well known that higher isolation rates (71%) are found during warm seasons than during the winter (Ziegler, 1993). Our investigations were carried out from November to December, thus this is a further reason for relatively low isolation rates as compared to investigations carried out in summer. In wild birds, Campylobacter has been demonstrated mainly in geese, wading birds, seagulls and ¨ mallard (Glunder, 1988). Out of 52 shot pheasants we investigated, Campylobacter were isolated from 14 (25.9%). When different animal species are compared, Campylobacter jejuni is most the frequently found in
189
poultry (Gonzales and Abuxapqui, 1989; Oosterom et al., 1994). Isolation rates of C. jejuni of up to 100% have been found in freshly slaughtered chickens and turkeys (Acuff et al., 1986; Berndtson et al., 1992; Lee et al., 1994). Our results on the detection of C. jejuni in poultry flocks, slaughtered broilers and shot pheasants are in agreement with results from other EU countries (Christopher et al., 1982; Hood et al., 1988; Shanker et al., 1990; Smith, 1995). The occurence of C. coli in poultry flocks (1.21%) and in slaughtered broilers (13.04%) is lower than in data from Northern Ireland. In our trials, only a low percentage of C. coli was detected, which is in agreement with studies in other countries (Dedie` et al., 1993; Humphrey et al., 1993).
Acknowledgements This work was financially supported by Boehringer Ingelheim Fonds Germany.
References Acuff, G.R., Vanderzant, C., Hanna, M.O., Ehlers, J.G., Golan, F.A., Gardner, F.A., 1986. Prevalence of Campylobacter jejuni in turkey carcass processing and further processing of turkey products. J. Food Prot. 49, 712–717. Arwana, A.A., 1987. Untersuchungen zum Vorkommen von ¨ Campylobacter jejuni und Campylobacter coli in Huhnerund ¨ Schlachtfleisch und zum Verhalten der Keime Gegenuber ¨ verschiedenen Umwelteinflussen. Vet. Med. Diss., HU Berlin. Baker, R.C., Paredes, M.D., Qureshi, R.A., 1987. Prevalence of Campylobacter jejuni in eggs and poultry meat in New York State. Poultry Sci. 66, 1766–1770. Bolton, F.J., Fox, A.J., Gibson, J., Madden, R.J., Moore, J.E., Moran, L., Murphy, P., Owen, R.J., Pennington, T.H., Stanley, T., Thomson-Carter, F., Wareing, D.R.A., Wilson, T., 1996. A multi-centre study of methods for sub-typing Campylobacter jejuni. In: Newell, D.G., Ketley, J.M., Feldmann, R.A. (Eds.), Campylobacter, Helicobacter, and Related Organisms, Plenum, New York, pp. 187–189. Berndtson, E., Tivemo, M., Engvall, A., 1992. Distribution and numbers of Campylobacter in newly slaughtered broiler chickens and hens. Int. J. Food Microbiol. 15, 54–60. Bryan, F.L., Doyle, M.P., 1995. Health risks and consequences of Salmonella and Campylobacter jejuni in raw poultry. J. Food Protect. 58, 326–344. Christopher, F.M., Smith, G.C., Vanderzant, C., 1982. Examination of poultry giblets, raw milk and meat for Campylobacter fetus subsp. jejuni. J. Food Protect. 45, 260–262.
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V. Atanassova, C. Ring / International Journal of Food Microbiology 51 (1999) 187 – 190
` M., 1990. Cross-contamination with CamDe Boer, E., Hahne, pylobacter jejuni and Salmonella spp from raw chicken products during food preparation. J. Food Protect. 53, 1067– 1068. ` K., Bockemuhl, ¨ J., Kuhn, ¨ Dedie, H., Volkmer, K.-J., Weinke, U.T., 1993. Campylobacteriosen. In: Bakterielle Zoonosen Bei Tier und Mensch, Ferdinand Enke Verlag, Stuttgart, pp. 49–65. Doyle, M.P., 1984. Association of Campylobacter jejuni with laying hens and eggs. Appl. Environ. Microbiol. 47, 313–320. ¨ Glunder, G., 1988. Charakterisierung von Campylobacter spp. ¨ ¨ ¨ Aus Wildvogeln, Berl. Munch. Tierarztl. Wochenschr. 102, 49–52. Gonzales, V.A., Abuxapqui, J.J.F., 1989. Poultry as Campylobacter jejuni and Campylobacter coli contamination source. Rev. Lat. Amer. Microbiol. 31, 271–273. Hartog, B., De Boer, J.B., 1982. Campylobacter jejuni in poultry products from retail outlets and in poultry slaughterhouse. In: Newell, D.G. (Ed.), Campylobacter: Epidemiology, Pathogenesis and Biochemistry, MTP Press Ltd, Lancaster, p. 270. Hood, A.M., Pearson, A.D., Shahamt, M., 1988. The extent of surface contamination of retailed chickens with Campylobacter jejuni serogroups. Epidemiol. Infect. 100 (1), 17–25. Humphrey, T.J., Henley, A., Lanning, U.D.G., 1993. The colonization of broiler chickens with Campylobacter jejuni: some epidemiologocal investigations. Epidemiol. Infect. 110, 601– 607. Izat, A.L., Gardner, F.A., Denton, J.H., Golan, F.A., 1988. Incidence and level of Campylobacter jejuni in broiler processing. Poultry. Sci 67 (11), 1568–1572. Jones, D.M., Sutcliffe, E.M., Curry, A., 1991a. Recovery of viable but non-culturable Campylobacter jejuni. J. Gen. Microbiol. 137, 2477–2482. Jones, F.T., Axtell, R.C., Rives, D.V., Schneideler, S.E., Tarver, Jr. F.R., Walker, R.L., Wineland, M.J., 1991b. A survey of Campylobacter jejuni contamination in modern broiler production and processing system. J. Food Prot. 54, 259–262. Karib, H., Seeger, H., 1994. Presence of Yersinia and Campylobacter spp. in foods. Fleischwirtsch. 74 (10), 1104–1106. Lee, C.-Y., Tai, C.L., Lin, S.-C., Chien, U.Y.-T., 1994. Occurence of plasmids and tetracycline resistence among Campylobacter jejuni and Campylobacter coli isolated from whole market chickens and clinical samples. Int. J. Food Microbiol. 24, 161–170.
Madden, R.H., Moran, L., Scates, P., 1996. Subtyping of animal and human Campylobacter spp. using RAPD. Lett. Appl. Microbiol. 23, 167–170. Oosterom, J., Notermans, S., Karman, H., Engels, G.B., 1983. Origin and prevalence of Campylobacter jejuni in poultry processing. J. Food Protect. 46, 339–344. Oosterom, J., 1994. Campylobacter jejuni in Foods of Animal Origin, Bilthoven, The Netherlands, Working paper for WHO consultation on epidemiology and control of campylobacteriosis in humans and animals. Park, C.E., Stankiewicz, Z.K., Lovett, J., Hunt, J., 1981. Incidence of Campylobacter jejuni in fresh eviscerated whole market chickens. Can. J. Microbiol. 27, 841–842. Penner, I.L., Hennessy, I.N., 1980. Passive hemagglutination technique for serotyping Campylobacter fetus subsp. jejuni on the basis of soluble heat-stable antigens. Clin. Microbiol. 12, 732–737. Shanker, S., Lee, A., Sorrell, T.C., 1990. Horizontal transmission of Campylobacter jejuni amongst broiler chicks: experimental studies. Epidemiol. Infect. 104, 101–110. Skirrow, M., Blaser, B.M.J., 1992. Clinical and epidemiologic considerations. In: Nachamkin, J., Blaser, M.J., Tompkins, L.S. (Eds.), Campylobacter jejuni: Current Status and Future Trends, Am. Soc. Microbiol, Washington DC, pp. 3–7. Skirrow, M.B., 1982. Campylobacter enteritidis – the first five years. J. Hyg. 89, 175–184. Smith, J.L., 1995. Arthritis, Guillain-Barre` syndrome, and other sequelae of Campylobacter jejuni enteritis. J. Food Protect. 58 (10), 1153–1170. Tokumaru, M., Konuma, H., Umesako, M., Konno, S., Shinagawa, K., 1991. Rates of detection of Salmonella and Campylobacter in meats in response to the sample size and the infection level of such species. Int. J. Food Microbiol. 13 (1), 41–46. Wallace, J.S., Stanley, K.N., Currie, J.E., Diggle, P.I., Jones, K., 1997. Seasonality of thermophilic Campylobacter populations in chickens. J. Appl. Microbiol. 82, 219–224. Ziegler, F., 1993. Ein Beitrag zum Vorkommen von Campylo¨ bacter jejuni und Campylobacter coli in der Huhnermast, ¨ Wien, Veterinarmed. Univ. Diss..
Short communication
Prevalence of Campylobacter spp. in poultry and poultry meat in Germany Viktoria Atanassova*, Christian Ring Veterinary University Hannover, Centre for Food Sciences, Department of Food Hygiene and Microbiology, Bischofsholer Damm 15, 30173 Hannover, Germany Received 15 March 1999; accepted 2 August 1999
Abstract Of 509 samples from poultry flocks, 209 isolates (41.1%) were Campylobacter positive. The number of positive cases in broiler carcasses was 45.9%. Of 52 pheasants investigated, 25.9% were Campylobacter positive. Campylobacter jejuni was isolated from 86 (42.0%) poultry flock samples, 47 (43%) broiler samples and 15 (28%) wild pheasant samples. C. coli was found at a rate of 1.2% in poultry flocks, 13% in broilers and 21% in pheasants. 1999 Elsevier Science B.V. All rights reserved. Keywords: Campylobacter; C. jejuni; C. coli; Poultry; Poultry meat
1. Introduction Results of studies on clinical Campylobacter cases in humans show a growing tendency (De Boer and Hahne, 1990; Jones et al., 1991a and b). In several European countries, Campylobacter pathogenic to man have been isolated more frequently than Salmonella (Humphrey et al., 1993; Bryan and Doyle, 1995). Tokumaru et al. (1991) reported that in Japan more Campylobacter than Salmonella are detected during the slaughter and cutting processes. In Germany, campylobacteriosis is the second most frequent cause of gastrointestinal infections *Corresponding author. Tel.: 1 49-511-856-7517; fax: 1 49511-856-7678.
(Dedie` et al., 1993). Campylobacter enteritis is a disease mainly taken up with food. In contrast to other bacterial enteritis agents, an increase of Campylobacter populations in foodstuffs is unlikely. Important sources of infection are inadequately heated poultry meat, poultry liver and cross-contamination of foodstuff through lack of kitchen hygiene (Skirrow, 1982; Skirrow and Blaser, 1992; Oosterom, 1994). From the food hygiene point of view, poultry thus plays an important role in the transmission of Campylobacter to man. In fresh poultry meat, the rate of contamination is 0–100% (Hood et al., 1988; Jones et al., 1991a and b; Karib and Seeger, 1994; Lee et al., 1994). Campylobacter was isolated mainly from the skin, the neck skin and the breast musculature, with
0168-1605 / 99 / $ – see front matter 1999 Elsevier Science B.V. All rights reserved. PII: S0168-1605( 99 )00120-8
188
V. Atanassova, C. Ring / International Journal of Food Microbiology 51 (1999) 187 – 190
bacterial counts of 1.5 3 10 3 –1.5 3 10 6 KbE / g per animal (Hood et al.,1988; Humphrey et al., 1993). Poultry offal (liver, heart and stomach) can generally also be contaminated with Campylobacter. Christopher et al. (1982) reported that 50% of investigated livers were contaminated with Campylobacter. During the slaughter process, damage to the intestinal tract can lead to direct contamination. Contamination can also occur indirectly through air, since during both defeathering and evisceration up to 10 4 KbE / m 3 have been demonstrated (Oosterom et al., 1983; Jones et al., 1991a and b).
2. Materials and Methods
2.1. Poultry and pheasant samples In a study in Germany during a period of three years (1995–1997), samples were obtained from 12 poultry flocks, 2 poultry slaughter plants, as well as from 52 hunted pheasants and investigated for the presence of Campylobacter. The investigations were carried out in the periods November to December. From poultry flocks, which were three-weeks-old, smear samples were taken from five randomly chosen animals one week prior to slaughter, and after slaughter or post-mortem investigation, a caecal and a liver sample were also taken. In slaughter plants, samples were taken from the skin, liver and the neck of slaughtered broilers. From the pheasants, samples were taken from the skin, caecum and liver.
2.2. Isolation and identification of Campylobacter Culturing was done by the Campylobacter-Enrichment-Bouillon No.2 (Oxoid No. CM 67) and Preston Campylobacter Selective Agar (PA, Oxoid CM 689). Each of them were supplemented with 5% (v / v)
saponine-lysed horse blood and Campylobacter Selective Supplement (Oxoid No.SR 1 117). The samples in Campylobacter Enrichment Bouillon were incubated for 24h at 378C and 24h at 428C; the culture was streaked onto a PA plate, which was incubated for 48h at 378C and 428C in a microaerobic environment. From each positive agar plate, one typical Campylobacter colony was subcultured and tested for Gram-staining, motility, production of oxidase and catalase and hippurate hydrolysis. All Campylobacter strains were frozen at 2 708C in Brain Heart Infusion (Difco 0037-17-8) with 17% (v / v) glycerol, awaiting biochemical tests (api Campy Ref 20890, ` bio Merieux). The Campylobacter isolates were also serotyped according to the Penner method (Penner and Hennessy, 1980).
3. Results and discussion The results of demonstrating the presence of Campylobacter in poultry flocks, slaughtered broilers and wild pheasants are shown in Table 1. Out of a total of 509 samples taken from poultry flocks, 209 isolates could be classified as Campylobacter. From 111 broiler samples, 51 (45.9%) were Campylobacter positive, and from 52 wild pheasants, 14 (25.9%) were positive. Campylobacter jejuni biotype II was the most frequent isolate from wild pheasants (69.5%) and from broilers (46.0%). C. jejuni biotype I was predominant in isolates from poultry flocks (54.5%). Campylobacter coli most frequently was isolated (1.2%) from poultry flocks. In the group of other Campylobacter spp. we identified Campylobacter sputorum subsp. faecalis, Campylobacter cryaerophila and Campylobacter upsaliensis. The detection rate in three-week-old cockerels (41.4%) and in slaughtered broilers (45.9%) is
Table 1 Campylobacter in poultry production Sample source
No. of samples analysed
Campylobacter positive isolates
Campylobacter positive (%)
Poultry flocks Broilers Wild pheasants
509 111 52
209 51 14
41.4 45.9 25.9
V. Atanassova, C. Ring / International Journal of Food Microbiology 51 (1999) 187 – 190
similar to data from the UK and Northern Ireland, with 41% Campylobacter positive poultry meat (Bryan and Doyle, 1995; Madden et al., 1996; Bolton, 1996). Sources of contamination and routes of infection with Campylobacter are important for poultry fattening units. Transmission of Campylobacter from egg to chick is not typical (Doyle, 1984; Baker et al., 1987). Infection and horizontal transmissions from one living animal to the other are of particular significance for the rate of detection of Campylobacter in poultry production. Very few infected animals can be the source of infection for the whole herd (Shanker et al., 1990). Because of the widespread use of air-conditioning in pens, with optimal temperatures and humidity, seasonal influences on the spread of Campylobacter in production units hardly play a role. Where the inside climate cannot be standardised throughout the year, a higher incidence of Campylobacter is observed in May and October (Doyle, 1984; Arwana, 1987; Wallance et al., 1997). Investigations at poultry slaughtering plants showed that there are many opportunities for contamination of carcasses (Oosterom et al., 1983; Jones et al., 1991a and b). The slaughtering plant is an important station for contamination with Campylobacter, as can be seen from the observation that the rate of isolation from carcasses is several times higher than from animals entering plants (Hartog and De Boer, 1982; Izat et al., 1988; Jones et al., 1991a and b). Our results from 111 slaughtered broilers found positive for Campylobacter (45.9%) correspond to results in literature (Park et al., 1981; Oosterom et al., 1983; Lee et al., 1994). It is well known that higher isolation rates (71%) are found during warm seasons than during the winter (Ziegler, 1993). Our investigations were carried out from November to December, thus this is a further reason for relatively low isolation rates as compared to investigations carried out in summer. In wild birds, Campylobacter has been demonstrated mainly in geese, wading birds, seagulls and ¨ mallard (Glunder, 1988). Out of 52 shot pheasants we investigated, Campylobacter were isolated from 14 (25.9%). When different animal species are compared, Campylobacter jejuni is most the frequently found in
189
poultry (Gonzales and Abuxapqui, 1989; Oosterom et al., 1994). Isolation rates of C. jejuni of up to 100% have been found in freshly slaughtered chickens and turkeys (Acuff et al., 1986; Berndtson et al., 1992; Lee et al., 1994). Our results on the detection of C. jejuni in poultry flocks, slaughtered broilers and shot pheasants are in agreement with results from other EU countries (Christopher et al., 1982; Hood et al., 1988; Shanker et al., 1990; Smith, 1995). The occurence of C. coli in poultry flocks (1.21%) and in slaughtered broilers (13.04%) is lower than in data from Northern Ireland. In our trials, only a low percentage of C. coli was detected, which is in agreement with studies in other countries (Dedie` et al., 1993; Humphrey et al., 1993).
Acknowledgements This work was financially supported by Boehringer Ingelheim Fonds Germany.
References Acuff, G.R., Vanderzant, C., Hanna, M.O., Ehlers, J.G., Golan, F.A., Gardner, F.A., 1986. Prevalence of Campylobacter jejuni in turkey carcass processing and further processing of turkey products. J. Food Prot. 49, 712–717. Arwana, A.A., 1987. Untersuchungen zum Vorkommen von ¨ Campylobacter jejuni und Campylobacter coli in Huhnerund ¨ Schlachtfleisch und zum Verhalten der Keime Gegenuber ¨ verschiedenen Umwelteinflussen. Vet. Med. Diss., HU Berlin. Baker, R.C., Paredes, M.D., Qureshi, R.A., 1987. Prevalence of Campylobacter jejuni in eggs and poultry meat in New York State. Poultry Sci. 66, 1766–1770. Bolton, F.J., Fox, A.J., Gibson, J., Madden, R.J., Moore, J.E., Moran, L., Murphy, P., Owen, R.J., Pennington, T.H., Stanley, T., Thomson-Carter, F., Wareing, D.R.A., Wilson, T., 1996. A multi-centre study of methods for sub-typing Campylobacter jejuni. In: Newell, D.G., Ketley, J.M., Feldmann, R.A. (Eds.), Campylobacter, Helicobacter, and Related Organisms, Plenum, New York, pp. 187–189. Berndtson, E., Tivemo, M., Engvall, A., 1992. Distribution and numbers of Campylobacter in newly slaughtered broiler chickens and hens. Int. J. Food Microbiol. 15, 54–60. Bryan, F.L., Doyle, M.P., 1995. Health risks and consequences of Salmonella and Campylobacter jejuni in raw poultry. J. Food Protect. 58, 326–344. Christopher, F.M., Smith, G.C., Vanderzant, C., 1982. Examination of poultry giblets, raw milk and meat for Campylobacter fetus subsp. jejuni. J. Food Protect. 45, 260–262.
190
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` M., 1990. Cross-contamination with CamDe Boer, E., Hahne, pylobacter jejuni and Salmonella spp from raw chicken products during food preparation. J. Food Protect. 53, 1067– 1068. ` K., Bockemuhl, ¨ J., Kuhn, ¨ Dedie, H., Volkmer, K.-J., Weinke, U.T., 1993. Campylobacteriosen. In: Bakterielle Zoonosen Bei Tier und Mensch, Ferdinand Enke Verlag, Stuttgart, pp. 49–65. Doyle, M.P., 1984. Association of Campylobacter jejuni with laying hens and eggs. Appl. Environ. Microbiol. 47, 313–320. ¨ Glunder, G., 1988. Charakterisierung von Campylobacter spp. ¨ ¨ ¨ Aus Wildvogeln, Berl. Munch. Tierarztl. Wochenschr. 102, 49–52. Gonzales, V.A., Abuxapqui, J.J.F., 1989. Poultry as Campylobacter jejuni and Campylobacter coli contamination source. Rev. Lat. Amer. Microbiol. 31, 271–273. Hartog, B., De Boer, J.B., 1982. Campylobacter jejuni in poultry products from retail outlets and in poultry slaughterhouse. In: Newell, D.G. (Ed.), Campylobacter: Epidemiology, Pathogenesis and Biochemistry, MTP Press Ltd, Lancaster, p. 270. Hood, A.M., Pearson, A.D., Shahamt, M., 1988. The extent of surface contamination of retailed chickens with Campylobacter jejuni serogroups. Epidemiol. Infect. 100 (1), 17–25. Humphrey, T.J., Henley, A., Lanning, U.D.G., 1993. The colonization of broiler chickens with Campylobacter jejuni: some epidemiologocal investigations. Epidemiol. Infect. 110, 601– 607. Izat, A.L., Gardner, F.A., Denton, J.H., Golan, F.A., 1988. Incidence and level of Campylobacter jejuni in broiler processing. Poultry. Sci 67 (11), 1568–1572. Jones, D.M., Sutcliffe, E.M., Curry, A., 1991a. Recovery of viable but non-culturable Campylobacter jejuni. J. Gen. Microbiol. 137, 2477–2482. Jones, F.T., Axtell, R.C., Rives, D.V., Schneideler, S.E., Tarver, Jr. F.R., Walker, R.L., Wineland, M.J., 1991b. A survey of Campylobacter jejuni contamination in modern broiler production and processing system. J. Food Prot. 54, 259–262. Karib, H., Seeger, H., 1994. Presence of Yersinia and Campylobacter spp. in foods. Fleischwirtsch. 74 (10), 1104–1106. Lee, C.-Y., Tai, C.L., Lin, S.-C., Chien, U.Y.-T., 1994. Occurence of plasmids and tetracycline resistence among Campylobacter jejuni and Campylobacter coli isolated from whole market chickens and clinical samples. Int. J. Food Microbiol. 24, 161–170.
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