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Incidence of Listeria spp. and Salmonella spp. in horsemeat for human consumption
International Journal of Food Microbiology 62 (2000) 161–164 www.elsevier.nl / locate / ijfoodmicro
Short communication
Incidence of Listeria spp. and Salmonella spp. in horsemeat for human consumption Magda A. de Assis, Maria Teresa Destro, Bernadette D. G. M. Franco, Mariza Landgraf* ˜ Experimental, Universidade de Sao ˜ Paulo, Av. Prof. Lineu Prestes, 580 BL. 14, Departamento de Alimentos e Nutric¸ao ˜ Paulo, SP, Brazil 05508 -900 Sao Received 1 September 1999; received in revised form 14 March 2000; accepted 31 July 2000
Abstract The incidence of Salmonella spp., Listeria spp. and Listeria monocytogenes in horsemeat for human consumption was investigated. One-hundred and twenty-one samples of frozen horsemeat collected from two Brazilian abattoirs were analysed over a period of 1 year. Twenty-two samples (18.2%) were positive for Listeria spp. with nine (7.4%) containing L. monocytogenes. None of the samples harbored Salmonella spp. 2000 Elsevier Science B.V. All rights reserved. Keywords: Listeria spp.; Listeria monocytogenes; Salmonella spp.; Horsemeat
1. Introduction The international food trade has been increasing in recent years. There is a huge variety of products being commercialized between countries and Brazil has the potential to be one of the largest food exporters, especially where red meat is concerned. Red meat is usually thought of as cattle or swine meat, but other animal species, such as horses, are also included. The consumption of horsemeat in Brazil is very low when compared with beef and pork, however approximately 110,000 animals were slaughtered in 1996. Almost all horsemeat (10,000 tonnes per year, the equivalent of US$12 million) is *Corresponding author. Tel.: 1 55-11-3818-7999; fax: 1 5511-815-4410. E-mail address: [email protected] (M. Landgraf).
directed to international markets, mainly European countries. It is recognized that muscle tissues of healthy animals are, in general, free of microorganisms. However, they can become contaminated during the slaughtering and dressing steps through contact of the carcasses with hide, hooves, manure, soil, and contents of the viscera, if they are punctured. If the slaughterhouse does not apply Good Manufacture Practices, and does not have Standard Sanitary Operation Procedures, other sources of contamination can exist, such as equipment, clothing, hands of personnel, etc. The importance of meat and meat products as vehicles for pathogens is well known worldwide. Pathogens such as Salmonella, Escherichia coli O157:H7, Listeria monocytogenes, Clostridium perfringens, amongst others, are not infrequent in meat
0168-1605 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S0168-1605( 00 )00404-9
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M. A. de Assis et al. / International Journal of Food Microbiology 62 (2000) 161 – 164
and meat products, and have been linked to foodborne diseases (Bell et al., 1994; Bonvet et al., 1986; CDC, 1994, 1995; Jacquet et al., 1995; McLauchlin et al., 1991; Palmer and Rowe, 1986). This study reports the incidence of Listeria spp. and Salmonella spp. in horsemeat for human consumption, with special reference to L. monocytogenes.
2. Materials and methods
2.1. Samples Frozen packs of horsemeat chunks from two different slaughterhouses were brought to the laboratory on ice and were kept at 48C to thaw. Each sample comprised seven to 14, 500 g sample units taken at random from each lot. The meat was finely sliced and portions of 50 g were taken from each sample unit and composited; 50 and 25 g analytical units were analysed for Salmonella and Listeria, respectively.
2.2. Listeria detection The methodology for the detection of L. monocytogenes was according to Warburton et al. (1991). Analytical units of 25 g of horsemeat were homogenized in 225 ml of Listeria Enrichment Broth (LEB)UVM1 formulation (Oxoid, England) and incubated at 308C for 24–48 h. At 24 and 48 h, 0.1 ml of the primary enrichment was transferred to 10 ml of modified Fraser Broth (Oxoid) and incubated at 358C for 24–26 h. The broth was subcultured onto PALCAM agar (Oxoid), LPM agar (Oxoid) and modified Oxford agar (MOX) (Oxoid). LPM plates were incubated at 308C for 24–48 h and PALCAM and MOX plates at 358C for 24–48 h. The plates were then examined for typical colonies. Five typical colonies from each medium were subcultured to Trypticase soy agar (Difco, Detroit, MI, USA) plus 0.6% yeast extract (Difco) and incubated at 308C for 24 h. Colonies showing a blue-gray or blue-green colour under transillumination were submitted for further characterization using the API Listeria ´ (bioMerieux, France).
2.3. Salmonella detection The presence of Salmonella spp. was evaluated according to the following method modified from Flowers et al. (1992). Analytical units of 50 g taken from composited samples were homogenized with 450 ml of buffered peptone water and incubated at 378C for 24 h. Aliquots of 1.0 and 0.1 ml were transferred to Selenite Cystine Broth (SC, Difco) and to Tetrathionate Broth (TT, Difco), respectively. SC tubes were incubated in a dry incubator at 378C and TT in a water bath at 438C, both for 24 h. The broths were streaked onto Hektoen enteric, Brilliant green and Rambach agar plates and incubated at 358C for 24 h. Typical colonies were transferred to Triple sugar iron agar (Difco) and to Lysine iron agar (Difco). Strains exhibiting typical reactions were ´ submitted to API 20 E (bioMerieux) and to serological tests with polyvalent O and H antisera (Probac, Brazil).
3. Results and discussion Twenty-two (18.2%) horsemeat samples out of the 121 samples tested were positive for Listeria spp., with nine (7.4%) identified as L. monocytogenes. Surveys of the microbiological quality of horsemeat are not common, especially when Listeria monocytogenes is considered. The only survey done reported on the recovery of Listeria spp., but not L. monocytogenes, from five of 19 horsemeat samples (26.3%) (Maini et al., 1989). The incidence of Listeria spp. and L. monocytogenes in this study is, in general, lower than that reported for other red meat and meat products. However, it is difficult to compare the results obtained by different researchers since the animal species are different. The incidence of L. monocytogenes in red meat and meat products in Brazil has been studied. Destro et al. (1991) detected the bacterium in 65% of ground beef, 82.4% of frankfurters and 80% of fresh Brazilian pork sausage comprising 75.4% of all samples analysed. L. innocua was recovered from 84.2%, L. seeligeri from 1.8%, L. welshimeri from 3.5% and L. murrayi from 1.8% of samples. Serafini and Nunes (1991) isolated Listeria spp. from 75% of meat products (fresh pork sausage, thermo-processed
M. A. de Assis et al. / International Journal of Food Microbiology 62 (2000) 161 – 164
´ analysed and L. liver, ham and chicken pates) monocytogenes was isolated just from fresh Brazilian pork sausage (11.9%). Mesquita (1991) detected Listeria spp. in 48% of raw beef striploin samples analysed. However, only 2% contained L. monocytogenes. In Australia, Ibrahim and Macrae (1991) reported the presence of Listeria spp. in 34% of raw beef samples, 40% of raw lamb, 30% of raw pork and 2.6% of raw milk samples. L. monocytogenes was detected only in flesh food. Vanderline et al. (1998) found L. monocytogenes in 0.59% of samples obtained from beef carcasses processed for export markets. Jay (1996) revealed that, from 1971 to 1994, the prevalence of L. monocytogenes in raw and processed meats was variable, with 16% of products being positive. Fresh meats tend to contain , 100 cfu / g, while processed meat and poultry products contain the highest numbers (1.9 3 10 5 cfu / g in chicken roll). L. monocytogenes was detected in 2% of pork samples and 22% of beef samples during a survey to assess the contamination of carcasses at the end of the slaughtering process in Belgium (Korsak et al., 1998). Loncarevic et al. (1994), analysing 496 samples of meat, lymph nodes, process water and swabs from different locations in an abattoir for cattle and pigs, in Bosnia and Hercegovina, found L. monocytogenes in two of 10 beef meat samples, five of 50 pigmeat samples and one of 21 lymph nodes of pigs. Weber et al. (1995), studying fecal samples of several domestic and companion animals, found L. monocytogenes in 4.8% of the samples (400) of horse origin and a higher incidence of this species in cattle (33.3%). Pathogens other than L. monocytogenes have been found in horsemeat by some authors (Monteverde et al., 1969; Quevedo et al., 1973). Anderson and Lee (1976) isolated Salmonella from 26.6% of horsemeat samples collected from an American horsemeatpacking plant under federal inspection. Similar results were reported by Gonzales et al. (1996), who detected Salmonella spp. in 20% of horse muscle samples studied. However, during our survey, none of the samples harboured Salmonella spp. It is safe to imply that, in these two abattoirs, good manufacturing practices were applied. When viscera
163
are not punctured and hygienic principles are followed, the absence of enteric pathogens in raw meats is expected. On the other hand, due to the ubiquitous nature of this microorganism, the presence of Listeria spp. in raw products is hard, if not impossible, to control, even when GMPs are applied. The presence of L. monocytogenes in horsemeat should be considered carefully since consumers who potentially undercook the product may be at risk of illness. Also of concern is the fact that hosemeat can be used to prepare ready-to-eat products such as ‘Bresaola’, a typical Italian raw cured product. Cross-contamination at different levels during the handling of this meat must also be considered.
References Anderson, G.D., Lee, D.R., 1976. Salmonella in horses: a source of contamination of horsemeat in packing plant under Federal Inspection. Appl. Environ. Microbiol. 31, 661–663. Bell, B.P., Goldoft, M., Griffin, P.M., Davis, M.A., Gordon, D.C., Tarr, P.I., Bartleson, C.A., Lewis, J.H., Barrett, T.J., Wells, J.G., Baron, R., Kobayashi, J., 1994. A multistate outbreak of Escherichia coli O157:H7 associated to bloody diarrhea and hemolytic uremic syndrome from hamburgers. J. Am. Med. Assoc. 272, 1349–1353. Bonvet, E., Jestin, C., Ancelle, R., 1986. Importance of exported cases of salmonelloses in the revelation of an epidemic. In: Proceedings of the Second World Congress of Foodborne and Intoxications, Institute of Veterinary Medicine, Berlin, p. 303. Centers for Disease Control and Prevention, 1994. Clostridium perfringens associated with corned beef served at St. Patrick’s Day meals; Ohio and Virginia, 1993. Morbid. Mortal. Weekly Rep. 43, 137–144. Centers for Disease Control and Prevention, 1995. Escherichia coli O157:H7 outbreak linked to commercially distributed dry-cured salami — Washington and California, 1994. Morbid. Mortal. Weekly Rep. 44, 157–160. Destro, M.T., Serrano, A.M., Kabuki, D.Y., 1991. Isolation of Listeria species from some Brazilian meat and dairy products. Food Control 2, 110–112. Flowers, R.S., D’Aoust, J.Y., Andrews, W.H., Bailey, J.S., 1992. Salmonella. In: Vanderzant, C.A., Splittstoesser, D.F. (Eds.), Compendium of Methods for the Microbiological Examination of Foods, 3rd Edition. APHA, pp. 371–422. Gonzales, S., Birman, E., Yaafaar, M., Pavan, M., Silvestre, A., ´ de Salmonella sp en musculo equino. In: XV 1996. Deteccion ˆ ´ Congresso Panamericano de Ciencias Veterinarias, Campo Grande, MS, Brasil, p. 208, poster 1425. Ibrahim, A., Macrae, I.C., 1991. Incidence of Aeromonas and Listeria spp. in red meat and milk samples in Brisbane, Australia. Int. J. Food Microbiol. 12, 263–270. Jacquet, C., Catimel, B., Brosch, R., Bruchieser, C., Dehaumont, P., Goulet, V., Lepoutre, V., Veit, P., Rocourt, J., 1995. In-
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M. A. de Assis et al. / International Journal of Food Microbiology 62 (2000) 161 – 164
vestigations related to the epidemic strain involved in the French listeriosis outbreak in 1992. Appl. Environ. Microbiol. 61, 2242–2246. Jay, J.M., 1996. Prevalence of Listeria spp. in meat and poultry products. Food Control 7, 209–214. Korsak, N., Daube, G., Ghafir, Y., Chaded, A., Jolly, S., Vindevogel, H., 1998. An efficient sampling technique used to detect four foodborne pathogens on pork and beef carcasses in nine Belgian abattoirs. J. Food Prot. 61, 535–541. Loncarevic, S., Milanovic, A., Caklovica, F., Tham, W., Danielsson-Tham, M.L., 1994. Occurrence of Listeria species in an abattoir for cattle and pigs in Bosnia and Hercegovina. Acta Vet. Scand. 35, 11–15. Maini, P., Gaini, R., Piva, I., Zampino, L., Bicocchi, R., Bucci, G., 1989. Listeria spp. and enteric pathogens in raw meat: a survey in the Ferrara area. Boll. Ist. Sieroter. Milan 68, 42–44. McLauchlin, J., Hall, S.M., Velani, S.K., Gilbert, R.J., 1991. Human listerioses and pate — a possible association. Br. Med. J. 303, 773–775. Mesquita, A.J., 1991. Bacteria of the genus Listeria in meat and residual water of washing carcasses in a frigorific abattoir and ´ In: bovine minced meat commercialized in Goiania city, Goias. XXIV World Veterinarian Congress, p. 76, 4.5.3, Abstracts, Rio de Janeiro, Brazil. ´ Monteverde, J.J., Simeone, D.H., Moran, N., Hermida, C.A.,
´ de alimentos. VI Colombino, M.M., 1969. Microbiologıa ´ ´ Salmonelas en carne y ganglios linfaticos de equinos recien sacrificados. Bacteriologia de agua y liquidos residuales. Rev. Fac. Agronomia y Veterinaria 17, 57–60. Palmer, S.R., Rowe, B., 1986. Trends in Salmonella infections. Public Health Lab. Serv. Microbiol. Dig. 3, 18–21. ´ ´ Quevedo, F.D., Dobosch, D., Gonzalez, E., 1973. Contaminacion de carne equina con salmonelas: un estudio ecologico. I. Equinos portadores. Gaceta Vet. 35, 119–123. Serafini, A., Nunes, I., 1991. Isolation of Listeria monocytogenes from fresh pork sausages and liver, ham and chicken pates, in Goiania, Goias, Brazil. In: XXIV World Veterinarian Congress, p. 76, 4.5.3, Abstracts, Rio de Janeiro, Brazil. Vanderline, P.B., Shay, B., Murray, J., 1998. Microbiological quality of Australian beef carcass meat and frozen bulk packed beef. J. Food Prot. 61, 437–443. Warburton, D.W., Farber, J.M., Babiuk, T., 1991. Isolation of Listeria from all food and environmental samples. In: Compendium of Analytical Methods — Laboratory Procedures of Microbiological Analysis of Foods. Health and Welfare, Vol. 3. Polyscience. Weber, A., Potel, J., Schafer-Schimidt, R., Prell, A., Datzmann, C., 1995. Studies on the occurrence of Listeria monocytogenes in fecal samples of domestic and companion animals. Zbl. Hyg. Umweltmed. 198, 117–123.
Short communication
Incidence of Listeria spp. and Salmonella spp. in horsemeat for human consumption Magda A. de Assis, Maria Teresa Destro, Bernadette D. G. M. Franco, Mariza Landgraf* ˜ Experimental, Universidade de Sao ˜ Paulo, Av. Prof. Lineu Prestes, 580 BL. 14, Departamento de Alimentos e Nutric¸ao ˜ Paulo, SP, Brazil 05508 -900 Sao Received 1 September 1999; received in revised form 14 March 2000; accepted 31 July 2000
Abstract The incidence of Salmonella spp., Listeria spp. and Listeria monocytogenes in horsemeat for human consumption was investigated. One-hundred and twenty-one samples of frozen horsemeat collected from two Brazilian abattoirs were analysed over a period of 1 year. Twenty-two samples (18.2%) were positive for Listeria spp. with nine (7.4%) containing L. monocytogenes. None of the samples harbored Salmonella spp. 2000 Elsevier Science B.V. All rights reserved. Keywords: Listeria spp.; Listeria monocytogenes; Salmonella spp.; Horsemeat
1. Introduction The international food trade has been increasing in recent years. There is a huge variety of products being commercialized between countries and Brazil has the potential to be one of the largest food exporters, especially where red meat is concerned. Red meat is usually thought of as cattle or swine meat, but other animal species, such as horses, are also included. The consumption of horsemeat in Brazil is very low when compared with beef and pork, however approximately 110,000 animals were slaughtered in 1996. Almost all horsemeat (10,000 tonnes per year, the equivalent of US$12 million) is *Corresponding author. Tel.: 1 55-11-3818-7999; fax: 1 5511-815-4410. E-mail address: [email protected] (M. Landgraf).
directed to international markets, mainly European countries. It is recognized that muscle tissues of healthy animals are, in general, free of microorganisms. However, they can become contaminated during the slaughtering and dressing steps through contact of the carcasses with hide, hooves, manure, soil, and contents of the viscera, if they are punctured. If the slaughterhouse does not apply Good Manufacture Practices, and does not have Standard Sanitary Operation Procedures, other sources of contamination can exist, such as equipment, clothing, hands of personnel, etc. The importance of meat and meat products as vehicles for pathogens is well known worldwide. Pathogens such as Salmonella, Escherichia coli O157:H7, Listeria monocytogenes, Clostridium perfringens, amongst others, are not infrequent in meat
0168-1605 / 00 / $ – see front matter 2000 Elsevier Science B.V. All rights reserved. PII: S0168-1605( 00 )00404-9
162
M. A. de Assis et al. / International Journal of Food Microbiology 62 (2000) 161 – 164
and meat products, and have been linked to foodborne diseases (Bell et al., 1994; Bonvet et al., 1986; CDC, 1994, 1995; Jacquet et al., 1995; McLauchlin et al., 1991; Palmer and Rowe, 1986). This study reports the incidence of Listeria spp. and Salmonella spp. in horsemeat for human consumption, with special reference to L. monocytogenes.
2. Materials and methods
2.1. Samples Frozen packs of horsemeat chunks from two different slaughterhouses were brought to the laboratory on ice and were kept at 48C to thaw. Each sample comprised seven to 14, 500 g sample units taken at random from each lot. The meat was finely sliced and portions of 50 g were taken from each sample unit and composited; 50 and 25 g analytical units were analysed for Salmonella and Listeria, respectively.
2.2. Listeria detection The methodology for the detection of L. monocytogenes was according to Warburton et al. (1991). Analytical units of 25 g of horsemeat were homogenized in 225 ml of Listeria Enrichment Broth (LEB)UVM1 formulation (Oxoid, England) and incubated at 308C for 24–48 h. At 24 and 48 h, 0.1 ml of the primary enrichment was transferred to 10 ml of modified Fraser Broth (Oxoid) and incubated at 358C for 24–26 h. The broth was subcultured onto PALCAM agar (Oxoid), LPM agar (Oxoid) and modified Oxford agar (MOX) (Oxoid). LPM plates were incubated at 308C for 24–48 h and PALCAM and MOX plates at 358C for 24–48 h. The plates were then examined for typical colonies. Five typical colonies from each medium were subcultured to Trypticase soy agar (Difco, Detroit, MI, USA) plus 0.6% yeast extract (Difco) and incubated at 308C for 24 h. Colonies showing a blue-gray or blue-green colour under transillumination were submitted for further characterization using the API Listeria ´ (bioMerieux, France).
2.3. Salmonella detection The presence of Salmonella spp. was evaluated according to the following method modified from Flowers et al. (1992). Analytical units of 50 g taken from composited samples were homogenized with 450 ml of buffered peptone water and incubated at 378C for 24 h. Aliquots of 1.0 and 0.1 ml were transferred to Selenite Cystine Broth (SC, Difco) and to Tetrathionate Broth (TT, Difco), respectively. SC tubes were incubated in a dry incubator at 378C and TT in a water bath at 438C, both for 24 h. The broths were streaked onto Hektoen enteric, Brilliant green and Rambach agar plates and incubated at 358C for 24 h. Typical colonies were transferred to Triple sugar iron agar (Difco) and to Lysine iron agar (Difco). Strains exhibiting typical reactions were ´ submitted to API 20 E (bioMerieux) and to serological tests with polyvalent O and H antisera (Probac, Brazil).
3. Results and discussion Twenty-two (18.2%) horsemeat samples out of the 121 samples tested were positive for Listeria spp., with nine (7.4%) identified as L. monocytogenes. Surveys of the microbiological quality of horsemeat are not common, especially when Listeria monocytogenes is considered. The only survey done reported on the recovery of Listeria spp., but not L. monocytogenes, from five of 19 horsemeat samples (26.3%) (Maini et al., 1989). The incidence of Listeria spp. and L. monocytogenes in this study is, in general, lower than that reported for other red meat and meat products. However, it is difficult to compare the results obtained by different researchers since the animal species are different. The incidence of L. monocytogenes in red meat and meat products in Brazil has been studied. Destro et al. (1991) detected the bacterium in 65% of ground beef, 82.4% of frankfurters and 80% of fresh Brazilian pork sausage comprising 75.4% of all samples analysed. L. innocua was recovered from 84.2%, L. seeligeri from 1.8%, L. welshimeri from 3.5% and L. murrayi from 1.8% of samples. Serafini and Nunes (1991) isolated Listeria spp. from 75% of meat products (fresh pork sausage, thermo-processed
M. A. de Assis et al. / International Journal of Food Microbiology 62 (2000) 161 – 164
´ analysed and L. liver, ham and chicken pates) monocytogenes was isolated just from fresh Brazilian pork sausage (11.9%). Mesquita (1991) detected Listeria spp. in 48% of raw beef striploin samples analysed. However, only 2% contained L. monocytogenes. In Australia, Ibrahim and Macrae (1991) reported the presence of Listeria spp. in 34% of raw beef samples, 40% of raw lamb, 30% of raw pork and 2.6% of raw milk samples. L. monocytogenes was detected only in flesh food. Vanderline et al. (1998) found L. monocytogenes in 0.59% of samples obtained from beef carcasses processed for export markets. Jay (1996) revealed that, from 1971 to 1994, the prevalence of L. monocytogenes in raw and processed meats was variable, with 16% of products being positive. Fresh meats tend to contain , 100 cfu / g, while processed meat and poultry products contain the highest numbers (1.9 3 10 5 cfu / g in chicken roll). L. monocytogenes was detected in 2% of pork samples and 22% of beef samples during a survey to assess the contamination of carcasses at the end of the slaughtering process in Belgium (Korsak et al., 1998). Loncarevic et al. (1994), analysing 496 samples of meat, lymph nodes, process water and swabs from different locations in an abattoir for cattle and pigs, in Bosnia and Hercegovina, found L. monocytogenes in two of 10 beef meat samples, five of 50 pigmeat samples and one of 21 lymph nodes of pigs. Weber et al. (1995), studying fecal samples of several domestic and companion animals, found L. monocytogenes in 4.8% of the samples (400) of horse origin and a higher incidence of this species in cattle (33.3%). Pathogens other than L. monocytogenes have been found in horsemeat by some authors (Monteverde et al., 1969; Quevedo et al., 1973). Anderson and Lee (1976) isolated Salmonella from 26.6% of horsemeat samples collected from an American horsemeatpacking plant under federal inspection. Similar results were reported by Gonzales et al. (1996), who detected Salmonella spp. in 20% of horse muscle samples studied. However, during our survey, none of the samples harboured Salmonella spp. It is safe to imply that, in these two abattoirs, good manufacturing practices were applied. When viscera
163
are not punctured and hygienic principles are followed, the absence of enteric pathogens in raw meats is expected. On the other hand, due to the ubiquitous nature of this microorganism, the presence of Listeria spp. in raw products is hard, if not impossible, to control, even when GMPs are applied. The presence of L. monocytogenes in horsemeat should be considered carefully since consumers who potentially undercook the product may be at risk of illness. Also of concern is the fact that hosemeat can be used to prepare ready-to-eat products such as ‘Bresaola’, a typical Italian raw cured product. Cross-contamination at different levels during the handling of this meat must also be considered.
References Anderson, G.D., Lee, D.R., 1976. Salmonella in horses: a source of contamination of horsemeat in packing plant under Federal Inspection. Appl. Environ. Microbiol. 31, 661–663. Bell, B.P., Goldoft, M., Griffin, P.M., Davis, M.A., Gordon, D.C., Tarr, P.I., Bartleson, C.A., Lewis, J.H., Barrett, T.J., Wells, J.G., Baron, R., Kobayashi, J., 1994. A multistate outbreak of Escherichia coli O157:H7 associated to bloody diarrhea and hemolytic uremic syndrome from hamburgers. J. Am. Med. Assoc. 272, 1349–1353. Bonvet, E., Jestin, C., Ancelle, R., 1986. Importance of exported cases of salmonelloses in the revelation of an epidemic. In: Proceedings of the Second World Congress of Foodborne and Intoxications, Institute of Veterinary Medicine, Berlin, p. 303. Centers for Disease Control and Prevention, 1994. Clostridium perfringens associated with corned beef served at St. Patrick’s Day meals; Ohio and Virginia, 1993. Morbid. Mortal. Weekly Rep. 43, 137–144. Centers for Disease Control and Prevention, 1995. Escherichia coli O157:H7 outbreak linked to commercially distributed dry-cured salami — Washington and California, 1994. Morbid. Mortal. Weekly Rep. 44, 157–160. Destro, M.T., Serrano, A.M., Kabuki, D.Y., 1991. Isolation of Listeria species from some Brazilian meat and dairy products. Food Control 2, 110–112. Flowers, R.S., D’Aoust, J.Y., Andrews, W.H., Bailey, J.S., 1992. Salmonella. In: Vanderzant, C.A., Splittstoesser, D.F. (Eds.), Compendium of Methods for the Microbiological Examination of Foods, 3rd Edition. APHA, pp. 371–422. Gonzales, S., Birman, E., Yaafaar, M., Pavan, M., Silvestre, A., ´ de Salmonella sp en musculo equino. In: XV 1996. Deteccion ˆ ´ Congresso Panamericano de Ciencias Veterinarias, Campo Grande, MS, Brasil, p. 208, poster 1425. Ibrahim, A., Macrae, I.C., 1991. Incidence of Aeromonas and Listeria spp. in red meat and milk samples in Brisbane, Australia. Int. J. Food Microbiol. 12, 263–270. Jacquet, C., Catimel, B., Brosch, R., Bruchieser, C., Dehaumont, P., Goulet, V., Lepoutre, V., Veit, P., Rocourt, J., 1995. In-
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M. A. de Assis et al. / International Journal of Food Microbiology 62 (2000) 161 – 164
vestigations related to the epidemic strain involved in the French listeriosis outbreak in 1992. Appl. Environ. Microbiol. 61, 2242–2246. Jay, J.M., 1996. Prevalence of Listeria spp. in meat and poultry products. Food Control 7, 209–214. Korsak, N., Daube, G., Ghafir, Y., Chaded, A., Jolly, S., Vindevogel, H., 1998. An efficient sampling technique used to detect four foodborne pathogens on pork and beef carcasses in nine Belgian abattoirs. J. Food Prot. 61, 535–541. Loncarevic, S., Milanovic, A., Caklovica, F., Tham, W., Danielsson-Tham, M.L., 1994. Occurrence of Listeria species in an abattoir for cattle and pigs in Bosnia and Hercegovina. Acta Vet. Scand. 35, 11–15. Maini, P., Gaini, R., Piva, I., Zampino, L., Bicocchi, R., Bucci, G., 1989. Listeria spp. and enteric pathogens in raw meat: a survey in the Ferrara area. Boll. Ist. Sieroter. Milan 68, 42–44. McLauchlin, J., Hall, S.M., Velani, S.K., Gilbert, R.J., 1991. Human listerioses and pate — a possible association. Br. Med. J. 303, 773–775. Mesquita, A.J., 1991. Bacteria of the genus Listeria in meat and residual water of washing carcasses in a frigorific abattoir and ´ In: bovine minced meat commercialized in Goiania city, Goias. XXIV World Veterinarian Congress, p. 76, 4.5.3, Abstracts, Rio de Janeiro, Brazil. ´ Monteverde, J.J., Simeone, D.H., Moran, N., Hermida, C.A.,
´ de alimentos. VI Colombino, M.M., 1969. Microbiologıa ´ ´ Salmonelas en carne y ganglios linfaticos de equinos recien sacrificados. Bacteriologia de agua y liquidos residuales. Rev. Fac. Agronomia y Veterinaria 17, 57–60. Palmer, S.R., Rowe, B., 1986. Trends in Salmonella infections. Public Health Lab. Serv. Microbiol. Dig. 3, 18–21. ´ ´ Quevedo, F.D., Dobosch, D., Gonzalez, E., 1973. Contaminacion de carne equina con salmonelas: un estudio ecologico. I. Equinos portadores. Gaceta Vet. 35, 119–123. Serafini, A., Nunes, I., 1991. Isolation of Listeria monocytogenes from fresh pork sausages and liver, ham and chicken pates, in Goiania, Goias, Brazil. In: XXIV World Veterinarian Congress, p. 76, 4.5.3, Abstracts, Rio de Janeiro, Brazil. Vanderline, P.B., Shay, B., Murray, J., 1998. Microbiological quality of Australian beef carcass meat and frozen bulk packed beef. J. Food Prot. 61, 437–443. Warburton, D.W., Farber, J.M., Babiuk, T., 1991. Isolation of Listeria from all food and environmental samples. In: Compendium of Analytical Methods — Laboratory Procedures of Microbiological Analysis of Foods. Health and Welfare, Vol. 3. Polyscience. Weber, A., Potel, J., Schafer-Schimidt, R., Prell, A., Datzmann, C., 1995. Studies on the occurrence of Listeria monocytogenes in fecal samples of domestic and companion animals. Zbl. Hyg. Umweltmed. 198, 117–123.