The bacteriological quality of goat and ovine milk
Abstract
This study concentrates on information concerning the microbiological hazards that can be present in raw milk from animal species other than cows. A total of 54 (23 of ovine and 31 of goat) bulk tank milk samples from 10 farms in the Czech Republic were collected in years 2013 - 2014. The sampling was done at regular time intervals during the whole year, with five to eight samples collected from each of the 10 dairy farms involved in the study. All milk samples were collected into sterile sampling bottles and transported in a cooler sampling case to the laboratory for immediate examination. Farms were randomly selected to cover the whole area of the Czech Republic. The prevalence and characteristic of Escherichia coli, Staphylococcus aureus, Salmonella spp., Campylobacter spp. and Listeria monocytogenes was studied. Raw cow's milk can be contaminated by E. coli intramammarily during clinical or subclinical mastitis and either directly through animal feces or indirectly during milk collection through farm employees or the milking equipment. E. coli was detected in 90.3% of the goat milk and 95.7% of the ovine milk samples. The genes encoding Shiga toxins 1 and 2- (stx1, stx2) were not detected and no STEC was identified. The Eae was the detected in 3 (4.6%) isolates. S. aureus was detected in 9 (29.0%) samples of goat milk and 8 (34.8%) samples of ovine milk. A total 12 (57.1%) enterotoxin positive S. aureus were obtained; 6 (28.6%) were positive for the production of sec encoding enterotoxin SEC; in 4 (19.0%) isolates the gene seh was detected; 2 (9.5%) isolates were proven positive for seg (4.8%) and combination seg and sei (4.8%). The presence of MRSA was not detected in the tested samples in our study. L. monocytogenes was detected in 1 (3.2%) samples of goat milk and 1 (4.3%) samples of ovine milk. The serotype (1/2a, 1/2b) was detected in our study. Campylobacter spp. and Salmonella spp. were not isolated from any of the samples. These results form the basis for determining the microbiological quality standards for goat and ovine milk.
References
Aras, Z., Aydinb, I., Kav, K. 2012. Isolation of methicillin-resistant Staphylococcus aureus from caprine mastitis cases. Small Ruminant Research. vol. 102, no. 1, p. 68-73. http://dx.doi.org/10.1016/j.smallrumres.2011.08.014
Argudín, M. A., Mendoza, M. C., Rodicio, M. R. 2010. Food Poisoning and Staphylococcus aureus enterotoxins. Toxins. vol. 2, no. 7, p. 1751-1773. http://dx.doi.org/10.3390/toxins2071751 PMid:22069659
Blanco, M., Blanco, J. E., Mora, A., Dahbi, G., Alonso, M. P., Gonzalez, E. A., Bernardez, M. I., Blanco, J. 2004. Serotypes, virulence genes and intimin types of Shiga toxin (Verotoxin)-producing Escherichia coli isolates from cattle in Spain: identification of a new intimin variant gene (eae-ζ). J. Clin. Microbiol., vol. 42, no. 2, p. 645-651. http://dx.doi.org/10.1128/JCM.42.2.645-651.2004 PMid:14766831
Cody, S. H., Abbott, S. L., Marfin, A. A., Schulz, B., Wagner, P., Robbins, K., Mohle-Boetani, J. C., Vugia, D. J. 1999. Two outbreaks of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Northern California. JAMA. vol. 281, no. 19, p. 1805-1810. http://dx.doi.org/10.1001/jama.281.19.1805 PMid:10340367
Claeys, W. L., Cardoen, S., Daube, G., De Block, J., Dewettinck, K., Dierick, K., et al. 2013. Raw or heated cow milk consumption: review of risks and benefits. Food Control, vol. 31, p. 251-262. http://dx.doi.org/10.1016/j.foodcont.2012.09.035
Dahmen, S., Metayer, V., Gay, E., Madec, J. Y., Haenni, M. 2013. Characterization of extended-spectrum beta-lactamase (ESBL)-carrying plasmids and clones of Enterobacteriaceae causing cattle mastitis in France. Vet. Microbiol., vol. 162, no. 2-4, p. 793-799. http://dx.doi.org/10.1016/j.vetmic.2012.10.015 PMid:23127568
De Buyser, M. L., Dufour, B., Maire, M., Lafarge, V. 2001. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int. J. Food Microbiol. vol. 67, p. 1-17. http://dx.doi.org/10.1016/S0168-1605(01)00443-3
Desmarchelier, P., Fegan, N. 2011. Pathogens in milk: Escherichia coli. Encyclopedia of dairy sciences, 2nd ed. Academic Press, London, p. 60-66. http://dx.doi.org/10.1016/B978-0-12-374407-4.00393-9
Doumith, M., Buchrieser, C., Glaser, P., Jacquet, C., Martin, P. 2004. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J. Clin. Microbiol., vol. 42, no. 8, p. 3819-3822. http://dx.doi.org/10.1128/JCM.42.8.3819-3822.2004 PMid:15297538
Fagan, P. K., Hornitzky, M. A., Bettelheim, K. A., Djordjevic, S. P. 1999. Detection of shiga-like toxin (stx1 and stx2), intimin (eaeA), and enterohemorrhagic Escherichia coli (EHEC) hemolysin (EHEC hlyA) genes in animal feces by multiplex PCR. App. Environ. Microbiol., vol. 65, p. 868-872. PMid:9925634
Harrington, P., Archer, J., Davis, J. P., Croft, D. R., Varma, J. K., EIC officers. 2002. Outbreak of Campylobacter jejuni infections associated with drinking unpasteurized milk procured through a cow-leasing program-Wisconsin, Morbidity and Mortality Weekly Report. vol. 51, p. 548-549.
Hata, E., Katsuda, K., Kobayashi, H., Nishimori, K., Uchida, I., Higashide, M., Ishikawa, E., Sasaki, T., Eguchi, M. 2008. Bacteriological characteristics of Staphylococcus aureus isolates from humans and bulk milk. J. Dairy Sci., vol. 91, p. 564-569. http://dx.doi.org/10.3168/jds.2007-0457 PMid:18218742
Ikeda, T., Tamate, N., Yamaguchi, K., Makino, S. 2005. Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. App. Environ. Microbiol., vol. 71, no. 5, p. 2793-2795. http://dx.doi.org/10.1128/AEM.71.5.2793-2795.2005 PMid:15870376
ISO 16649-1 Microbiology of food and animal feeding stuffs. Horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli. Part 1: Colony-count technique at 44 degrees C using membranes and 5-bromo-4-chloro-3-indolyl beta-D-glucuronide, 2012.
ISO 6888-1 (560089) Microbiology of food and animal feeding stuffs, Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species) Part 1: Technique using Baird-Parker agar medium, 2000.
ISO 6579 (560088) Microbiology of food and animal feeding stuffs, Horizontal method for the detection of Salmonella spp., 2003.
ISO 10272-1 (560126) Microbiology of food and animal feeding stuffs, Horizontal method for detection and enumeration of Campylobacter spp., Part 1: Detection method, 2006.
ISO 11290-1 (560093) Microbiology of food and animal feeding stuffs, Horizontal method for the detection and enumeration of Listeria monocytogenes, Part 1: Detection method, 1999.
Jørgensen, H. J., Mørk, T., Caugant, D. A., Kearns, A., Rørvik, L. M. 2005. Genetic variation among Staphylococcus aureus strains from Norwegian bulk milk. App. Environ. Microbiol., vol. 71, no. 12, p. 8352-8361. http://dx.doi.org/10.1128/AEM.71.12.8352-8361.2005 PMid:16332822
Kalman, M., Szollosi, E., Czermann, B., Zimanyi, M., Szekeres, S. 2000. Milkborne campylobacter infection in Hungary. J. Food Protection. vol. 63, no. 10, p. 1426-1429. PMid:11041145
Kathariou, S. 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. J. Food Prot.. vol. 65, no. 11, p. 1811-1829. PMid:12430709
Lee, J. H., Jeong, J. M., Park, Y. H., Choi, S. S., Kim, Y. H., Chae, J. S., Moon, J. S., Park, H., Kim, S., Eo, S. K. 2004. Evaluation of the methicillin-resistant Staphylococcus aureus (MRSA)-Screen latex agglutination test for detection of MRSA of animal origin. J. Clin. Microbiol., vol. 42, no. 6, p. 2780-2782. http://dx.doi.org/10.1128/JCM.42.6.2780-2782.2004 PMid:15184469
Løvseth, A., Loncarevic, S., Berdal, K. G. 2004. Modified multiplex PCR method for detection of pryrogenic exotoxin genes in staphylococcal isolate. J. Clin. Microbiol., vol. 42, no. 8, p. 3869-3872. http://dx.doi.org/10.1128/JCM.42.8.3869-3872.2004 PMid:15297552
Lyra, D. G., Sousa, F. G., Borges, M. F., Givisiez, P. E., Queiroga, R. C., Souza, E. L., Gebreyes, W. A., Oliveira, C. J. 2013. Enterotoxin-encoding genes in Staphylococcus spp. from bulk goat milk. Foodborne Pathog Dis., vol. 10, no. 2, p. 126-130. http://dx.doi.org/10.1089/fpd.2012.1256 PMid:23441914
Martineau, F., Picard, F. J., Roy, P. H., Ouellette, M., Bergeron, M. G. 1998. Species-Specific and Ubiquitous DNA-Based Assays for Rapid Identification of Staphylococcus aureus. J. Clin. Microbiol., vol. 36, no. 3, p. 618-623. PMid:9508283
Martins, E. A., Leal Germano, P. M. 2011. Listeria monocytogenes in ready-to-eat, sliced, cooked ham and salami products, marketed in the city of São Paulo, Brazil: occurrence, quantification, and serotyping. Food Control., vol. 22, no. 2, p. 297-302. http://dx.doi.org/10.1016/j.foodcont.2010.07.026
McCallum, N., Berger-Bachi, B., Senn, M. M. 2010. Regulation of antibiotic resistance in Staphylococcus aureus. Int J Medical Microbiology, vol. 300, p. 118-129. http://dx.doi.org/10.1016/j.ijmm.2009.08.015
Mork, T., Kvitle, B., Mathisen, T., Jorgensen, H. J. 2010. Bacteriological and molecular investigations of Staphylococcus aureus in dairy goats. Vet. Microbiol., vol. 141, no. 1-2, p. 134-141. http://dx.doi.org/10.1016/j.vetmic.2009.08.019 PMid:19733450
Oliver, S. P., Jayarao, B. M., Almeida, R. A. 2005. Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathogens and Disease, vol. 2, p. 115-129. http://dx.doi.org/10.1089/fpd.2005.2.115.
Oliver, S. P., Boor, K. J., Murphy, S. C., Murinda, S. E. 2009. Food safety hazards associated with consumption of raw milk. Foodborne Pathog Dis., vol. 6, no. 7, p. 793-806. http://dx.doi.org/10.1089/fpd.2009.0302 PMid:19737059
Park, Y., W., Juárez, M., Ramos, M.m Haenlein, G. F. W. 2007. Physico-chemical characterisitcs of goat and sheep milk. Small Ruminant Research, vol. 68, p. 88-113. http://dx.doi.org/10.1016/j.smallrumres.2006.09.013
Poulsen, A. B., Skov, R., Pallesen, L. V. 2003. Detection of methicillin resistance in coagulase-negative staphylococci and in staphylococci directly from simulated blood cultures using the EVIGENE MRSA Detection Kit. J. Antimicrob. Chemother., vol. 51, no. 2, p. 419-421. http://dx.doi.org/10.1093/jac/dkg084 PMid:12562714
Robati, R., Gholami, S. 2013. Estimation of virulence genes of Shiga toxin producing Escherichia coli from juice puraches nd vegetables in Tehran/Iran. Europ. J. Experimental Biology, vol. 3, no. 2, p. 457-462. [cit. 2014-01-15]. Available at: http://pelagiaresearchlibrary.com/european-journal-of-experimental-biology/vol3-iss2/EJEB-2013-3-2-457-462.pdf
Scherrer, D., Corti, S., Muehlher, J. E., Zweifel, C., Stephan, R. 2004. Phenotypic and genotypic characteristics of Staphylococcus aureus isolates from raw bulk-tank samples of goat and sheep. Vet. Microbiol., vol. 101, no. 2, p. 101-107. http://dx.doi.org/10.1016/j.vetmic.2004.03.016 PMid:15172692
Silva, E. R., Carmo, L. S. Silva, N. 2005. Detection of the enterotoxins A, B and C genes in Staphylococcus aureus from goat and bovine mastitis in Brazilian dairy herds. Vet. Microbiol.. vol. 106, no. 1-2, p. 103-107. http://dx.doi.org/10.1016/j.vetmic.2004.12.005 PMid:15737479
Šťástková, Z., Karpíšková, S., Karpíšková, R. 2009. Occurrence of methicillin-resistant strains of Staphylococcus aureus at a goat breeding farm, Veterinarni Medicina, vol. 54, p. 419-426. [cit. 2014-01-10]. Available at: http://www.vri.cz/docs/vetmed/54-9-419.pdf
Thomas, D., Chou, S., Dauwalder, O., Lina, G. 2007. Diversity in Staphylococcus aureus enterotoxins. Chem. Immunol. Allergy, vol. 93, p. 24-41. http://dx.doi.org/10.1159/000100856 PMid:17369698
Vanderhaeghen, W., Cerpentier, T., Adriaensen, C., Vicca, J., Hermans, K., Butaye, P. 2010. Methicillin-resistant Staphylococcus aureus (MRSA) ST 398 associated with clinical and subclinical mastitis in Belgian. Vet. Microbiol., vol. 144, no. 1-2, p. 166-171. http://dx.doi.org/10.1016/j.vetmic.2009.12.044 PMid:20092969
Wani, S. A., Hussain, I., Fayaz, I., Mir, M. A., Nishikawa, Y. 2009. Subtype analysis of stx1, stx2 and eae genes in Shiga toxin-producing Escherichia coli (STEC) and typical and atypical enteropathogenic E. coli (EPEC) from lambs in India. Veterinary Journal, vol. 182, no. 3, p. 489-490. http://dx.doi.org/10.1016/j.tvjl.2008.07.017 PMid:18768338
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