Risk from Staphylococcus aureus in informally marketed raw cow milk
Article Sidebar
Main Article Content
Abstract
This study aimed to investigate the presence of Staphylococcus spp. and Staphylococcus aureus in raw cow milk samples taken from peddlers of five regions in Bulgaria. The results showed that all 44 samples tested were positive for Staphylococcus spp. All isolates were tested for coagulase production and subjected to PCR analysis. PCR amplification of 16S rRNA and nuc genes found the presence of Staphylococcus aureus in 23 (52.3%) of a total of 44 raw milk samples. The number of Staphylococcus spp. ranged from 3x102 to 1.08x106 cfu/ml, and that of Staphylococcus aureus from 1.5x102 to 3.19x105 cfu/ml. It is concluded that control over the hygiene of handling and processing raw milk is essential for its safety.
Article Details
References
Asao T., Kumeda Y., Kawai T., Shibata H., Oda H., Haruki K., Nakazawa H., Kozaki S. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiology and Infection, 2003, 130(1): 33-40.
Balaban N., Rasooly A. Staphylococcal enterotoxins. International Journal of Food Microbiology, 2000, 61(1): 1-10. https://doi.org/10.1016/S0168-1605(00)00377-9
Bergdoll M. Staphylococcus aureus. In: Foodborne Bacterial Pathogens (M. P. Doyle Ed.). CRC Press, Taylor & Francis Group. 1989, pp. 463-523, ISBN 10: 0824778669, ISBN 13: 9780824778668.
Brakstad O., Aasbakk K., Maeland J. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. Journal of Clinical Microbiology, 1992, 30(7): 1654-1660.
De Buyser M., Dufour B., Maire M., Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. International Journal of Food Microbiology, 2001, 67(1-2): 1-17. https://doi.org/10.1016/S0168-1605(01)00443-3
Donkor E., Aning K., Quaye J. Bacterial contaminations of informally marketed raw milk in Ghana. Ghana Medical Journal, 2007, 41(2): 58-61.
Doss A., Vijayasanthi M. Isolation and prevalence of Staphylococcus aureus from raw bovine milk samples in and around Thoothukudi District, Tamilnadu. International Journal of BioSciences and Technology, 2016, 9(4): 24-26.
El-Leboudy A., Amer A., El-Mohsen S. Detection of some pathogenic organisms from dairy farm milk. Alexandria Journal of Veterinary Sciences, 2015, 44(1): 111-118. http://dx.doi.org/10.5455/ajvs.47762
Fadaei A. Bacteriological quality of raw cow milk in Shahrekord, Iran. Veterinary World, 2014, 7(4): 240-243. http://dx.doi.org/10.14202/vetworld.2014.240-243
Gucukoglu A., Kevenk T., Uyanik T., Cadirci O., Terzi G., Alisarli M. Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. Journal of Food Science, 2012, 77(11): 620-623. https://doi.org/10.1111/j.1750-3841.2012.02954.x
Hill B., Smythe B., Lindsay D., Shepherd J. Microbiology of raw milk in New Zealand. International Journal of Food Microbiology, 2012, 157(2): 305-308. https://doi.org/10.1016/j.ijfoodmicro.2012.03.031
ISO 6888-1:1999. 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.
Jablonski L., Bohach G. Staphylococcus aureus. In: Food Microbiology: Fundamentals and Frontiers (M. P. Doyle, L. R. Beuchat, T. J Montville Eds.). Washington, DC: American Society for Microbiology Press. 1997, pp. 353-375, ISBN 10: 1555811175, ISBN 13: 9781555811174.
Jackson E., Erten E., Maddi N., Graham T., Larkin J., Blodgett R., Schlesser J., Reddy R. Detection and enumeration of four foodborne pathogens in raw commingled silo milk in the United States. Journal of Food Protection, 2012, 75(8): 1382-1393. https://doi.org/10.4315/0362-028X.JFP-11-548
Jahan M., Rahman M., Parvej M., Chowdhury S. M., Haque M., Talukder M., Ahmed S. Isolation and characterization of Staphylococcus aureus from raw cow milk in Bangladesh. Journal of Advanced Veterinary and Animal Research, 2014, 2(1): 49-55. http://dx.doi.org/10.5455/javar.2015.b47
Jørgensen H., Mørk T., Rørvik L. The occurrence of Staphylococcus aureus on a farm with small-scale production of raw milk cheese. Journal of Dairy Science, 2005, 88(11): 3810-3817. https://doi.org/10.3168/jds.S0022-0302(05)73066-6
Kalmus P., Kramarenko T., Roasto M., Meremae K., Viltrop A. Quality of raw milk intended for direct consumption in Estonia. Food Control, 2015, 51: 135-139. https://doi.org/10.1016/j.foodcont.2014.11.018
Kamal R., Bayoumi M., Abd El Aal S. MRSA detection in raw milk, some dairy products and hands of dairy workers in Egypt, a mini-survey. Food Control, 2013, 33(1): 49-53. https://doi.org/10.1016/j.foodcont.2013.02.017
Katsuda K., Hata E., Kobayashi H., Kohmoto M., Kawashima K., Tsunemitsu H., Eguchi M. Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Veterinary Microbiology, 2005, 105(3-4): 301-305. https://doi.org/10.1016/j.vetmic.2004.12.004
Kouamé-Sina S., Makita K., Costard S., Grace D., Dadié A., Dje M., Bonfoh B. Hazard identification and exposure assessment for bacterial risk assessment of informally marketed milk in Abidjan, Côte d’Ivoire. Food and Nutrition Bulletin, 2012, 33(4): 223-234. https://doi.org/10.1177/156482651203300402
Lowy F. Staphylococcus aureus infection. The New England Journal of Medicine, 1998, 339(8): 520-532. https://doi.org/10.1056/NEJM199808203390806
Makita K., Desissa F., Teklu A., Zewde G., Grace D. Risk assessment of staphylococcal poisoning due to consumption of informally-marketed milk and home-made yoghurt in Debre Zeit, Ethiopia. International Journal of Food Microbiology, 2012, 153(1-2): 135-141. https://doi.org/10.1016/j.ijfoodmicro.2011.10.028
Meshref A. Bacteriological quality and safety of raw cow's milk and fresh cream. Slovenian Veterinary Research, 2013, 50(1): 21-30.
Monday S., Bohach G. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in Staphylococcal isolates. Journal of Clinical Microbiology, 1999, 37(10): 3411-3414.
Ngasala J., Nonga H., Mtambo M. Assessment of raw milk quality and stakeholders’ awareness on milk-borne health risks in Arusha City and Meru District, Tanzania. Tropical Animal Health and Production, 2015, 47(5): 927-932. https://doi.org/10.1007/s11250-015-0810-y
Normanno G., Firinu A., Virgilio S., Mula G., Dambrosio A., Poggiu A., Decastelli L., Mioni R., Scoot S., Bolzoni G., Di Giannatale E., Salinetti A., La Salandra G., Bartoli M., Zuccon F., Pirino T., Sias S., Parisi A., Quaglia N., Celano G. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology, 2005, 98(1): 73-79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
Pourhassan M., Taravat-Najafabadi A. The spatial distribution of bacterial pathogens in raw milk consumption on Malayer City, Iran. Shiraz E-Medical Journal, 2011, 12(1): 2-10.
Pyz-Łukasik R., Paszkiewicz W., Tatara M., Brodzki P., Bełkot Z. Microbiological quality of milk sold directly from producers to consumers. Journal of Dairy Science, 2015, 98(7): 4294-4301. https://doi.org/10.3168/jds.2014-9187
Roberson J., Fox L., Hancock D., Gay J., Besser T. Sources of intermammary infections from Staphylococcus aureus in dairy heifers at first parturition. Journal of Dairy Science, 1998, 81(3): 687-693. https://doi.org/10.3168/jds.S0022-0302(98)75624-3
Rola J., Korpysa-Dzirba W., Czubkowska A., Osek J.Prevalence of enterotoxin genes and antimicrobial resistance of coagulase-positive staphylococci recovered from raw cow milk. Journal of Dairy Science, 2015, 98(7): 4273-4278. https://doi.org/10.3168/jds.2014-9064
Santos V., Martins H., Rezende I., Barbosa M., Andrade E., Souza S., Campos G., Oliveira P., Sousa D., Da Silva D., Amorim A., Timenetsky J., Cruz M., Yatsuda R., Marques L. Virulence factor profile of Staphylococcus aureus isolated from bovine milk from Brazil. Food and Nutrition Sciences, 2014, 5(15): 1496-1505. http://dx.doi.org/10.4236/fns.2014.515162
Shamila-Syuhada A., Rusul G., Wan-Nadiah W., Chuah L. Prevalence and antibiotics resistance of Staphylococcus aureus isolates isolated from raw milk obtained from small-scale dairy farms in Penang, Malaysia. Pakistan Veterinary Journal, 2016, 36(1): 98-102.
Taherikalani M., Hemati S., Heidarzadi K., Mahdavi Z., Ghanbari F., Mohamadi M., Ghafourian S., Varzi A., Jalilian F., Bogdanovic L., Saki K. Unexpectedly high occurrence of Escherichia coli and Staphylococcus aureus isolates from raw milk in Ilam, Western Iran. Journal of Biological Regulators & Homeostatic Agents, 2015, 29(4): 859-863.
Thaker H., Brahmbhatt M., Nayak J. Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Vet World, 2013, 6(1): 10-113 https://doi.org/10.5455/vetworld.2013.10-13
Wertheim H., Melles D., Vos M., van Leeuwen W., van Belkum A., Verbrugh H., Nouwen J. The role of nasal carriage in Staphylococcus aureus infections. The Lancet Infectious Diseases, 2005, 5(12): 751-762. https://doi.org/10.1016/S1473-3099(05)70295-4
Zhang S., Iandolo J., Stewart G. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiology Letters, 1998, 168(2): 227-233 https://doi.org/10.1111/j.1574-6968.1998.tb13278.x
Balaban N., Rasooly A. Staphylococcal enterotoxins. International Journal of Food Microbiology, 2000, 61(1): 1-10. https://doi.org/10.1016/S0168-1605(00)00377-9
Bergdoll M. Staphylococcus aureus. In: Foodborne Bacterial Pathogens (M. P. Doyle Ed.). CRC Press, Taylor & Francis Group. 1989, pp. 463-523, ISBN 10: 0824778669, ISBN 13: 9780824778668.
Brakstad O., Aasbakk K., Maeland J. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. Journal of Clinical Microbiology, 1992, 30(7): 1654-1660.
De Buyser M., Dufour B., Maire M., Lafarge V. Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. International Journal of Food Microbiology, 2001, 67(1-2): 1-17. https://doi.org/10.1016/S0168-1605(01)00443-3
Donkor E., Aning K., Quaye J. Bacterial contaminations of informally marketed raw milk in Ghana. Ghana Medical Journal, 2007, 41(2): 58-61.
Doss A., Vijayasanthi M. Isolation and prevalence of Staphylococcus aureus from raw bovine milk samples in and around Thoothukudi District, Tamilnadu. International Journal of BioSciences and Technology, 2016, 9(4): 24-26.
El-Leboudy A., Amer A., El-Mohsen S. Detection of some pathogenic organisms from dairy farm milk. Alexandria Journal of Veterinary Sciences, 2015, 44(1): 111-118. http://dx.doi.org/10.5455/ajvs.47762
Fadaei A. Bacteriological quality of raw cow milk in Shahrekord, Iran. Veterinary World, 2014, 7(4): 240-243. http://dx.doi.org/10.14202/vetworld.2014.240-243
Gucukoglu A., Kevenk T., Uyanik T., Cadirci O., Terzi G., Alisarli M. Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. Journal of Food Science, 2012, 77(11): 620-623. https://doi.org/10.1111/j.1750-3841.2012.02954.x
Hill B., Smythe B., Lindsay D., Shepherd J. Microbiology of raw milk in New Zealand. International Journal of Food Microbiology, 2012, 157(2): 305-308. https://doi.org/10.1016/j.ijfoodmicro.2012.03.031
ISO 6888-1:1999. 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.
Jablonski L., Bohach G. Staphylococcus aureus. In: Food Microbiology: Fundamentals and Frontiers (M. P. Doyle, L. R. Beuchat, T. J Montville Eds.). Washington, DC: American Society for Microbiology Press. 1997, pp. 353-375, ISBN 10: 1555811175, ISBN 13: 9781555811174.
Jackson E., Erten E., Maddi N., Graham T., Larkin J., Blodgett R., Schlesser J., Reddy R. Detection and enumeration of four foodborne pathogens in raw commingled silo milk in the United States. Journal of Food Protection, 2012, 75(8): 1382-1393. https://doi.org/10.4315/0362-028X.JFP-11-548
Jahan M., Rahman M., Parvej M., Chowdhury S. M., Haque M., Talukder M., Ahmed S. Isolation and characterization of Staphylococcus aureus from raw cow milk in Bangladesh. Journal of Advanced Veterinary and Animal Research, 2014, 2(1): 49-55. http://dx.doi.org/10.5455/javar.2015.b47
Jørgensen H., Mørk T., Rørvik L. The occurrence of Staphylococcus aureus on a farm with small-scale production of raw milk cheese. Journal of Dairy Science, 2005, 88(11): 3810-3817. https://doi.org/10.3168/jds.S0022-0302(05)73066-6
Kalmus P., Kramarenko T., Roasto M., Meremae K., Viltrop A. Quality of raw milk intended for direct consumption in Estonia. Food Control, 2015, 51: 135-139. https://doi.org/10.1016/j.foodcont.2014.11.018
Kamal R., Bayoumi M., Abd El Aal S. MRSA detection in raw milk, some dairy products and hands of dairy workers in Egypt, a mini-survey. Food Control, 2013, 33(1): 49-53. https://doi.org/10.1016/j.foodcont.2013.02.017
Katsuda K., Hata E., Kobayashi H., Kohmoto M., Kawashima K., Tsunemitsu H., Eguchi M. Molecular typing of Staphylococcus aureus isolated from bovine mastitic milk on the basis of toxin genes and coagulase gene polymorphisms. Veterinary Microbiology, 2005, 105(3-4): 301-305. https://doi.org/10.1016/j.vetmic.2004.12.004
Kouamé-Sina S., Makita K., Costard S., Grace D., Dadié A., Dje M., Bonfoh B. Hazard identification and exposure assessment for bacterial risk assessment of informally marketed milk in Abidjan, Côte d’Ivoire. Food and Nutrition Bulletin, 2012, 33(4): 223-234. https://doi.org/10.1177/156482651203300402
Lowy F. Staphylococcus aureus infection. The New England Journal of Medicine, 1998, 339(8): 520-532. https://doi.org/10.1056/NEJM199808203390806
Makita K., Desissa F., Teklu A., Zewde G., Grace D. Risk assessment of staphylococcal poisoning due to consumption of informally-marketed milk and home-made yoghurt in Debre Zeit, Ethiopia. International Journal of Food Microbiology, 2012, 153(1-2): 135-141. https://doi.org/10.1016/j.ijfoodmicro.2011.10.028
Meshref A. Bacteriological quality and safety of raw cow's milk and fresh cream. Slovenian Veterinary Research, 2013, 50(1): 21-30.
Monday S., Bohach G. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in Staphylococcal isolates. Journal of Clinical Microbiology, 1999, 37(10): 3411-3414.
Ngasala J., Nonga H., Mtambo M. Assessment of raw milk quality and stakeholders’ awareness on milk-borne health risks in Arusha City and Meru District, Tanzania. Tropical Animal Health and Production, 2015, 47(5): 927-932. https://doi.org/10.1007/s11250-015-0810-y
Normanno G., Firinu A., Virgilio S., Mula G., Dambrosio A., Poggiu A., Decastelli L., Mioni R., Scoot S., Bolzoni G., Di Giannatale E., Salinetti A., La Salandra G., Bartoli M., Zuccon F., Pirino T., Sias S., Parisi A., Quaglia N., Celano G. Coagulase-positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology, 2005, 98(1): 73-79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
Pourhassan M., Taravat-Najafabadi A. The spatial distribution of bacterial pathogens in raw milk consumption on Malayer City, Iran. Shiraz E-Medical Journal, 2011, 12(1): 2-10.
Pyz-Łukasik R., Paszkiewicz W., Tatara M., Brodzki P., Bełkot Z. Microbiological quality of milk sold directly from producers to consumers. Journal of Dairy Science, 2015, 98(7): 4294-4301. https://doi.org/10.3168/jds.2014-9187
Roberson J., Fox L., Hancock D., Gay J., Besser T. Sources of intermammary infections from Staphylococcus aureus in dairy heifers at first parturition. Journal of Dairy Science, 1998, 81(3): 687-693. https://doi.org/10.3168/jds.S0022-0302(98)75624-3
Rola J., Korpysa-Dzirba W., Czubkowska A., Osek J.Prevalence of enterotoxin genes and antimicrobial resistance of coagulase-positive staphylococci recovered from raw cow milk. Journal of Dairy Science, 2015, 98(7): 4273-4278. https://doi.org/10.3168/jds.2014-9064
Santos V., Martins H., Rezende I., Barbosa M., Andrade E., Souza S., Campos G., Oliveira P., Sousa D., Da Silva D., Amorim A., Timenetsky J., Cruz M., Yatsuda R., Marques L. Virulence factor profile of Staphylococcus aureus isolated from bovine milk from Brazil. Food and Nutrition Sciences, 2014, 5(15): 1496-1505. http://dx.doi.org/10.4236/fns.2014.515162
Shamila-Syuhada A., Rusul G., Wan-Nadiah W., Chuah L. Prevalence and antibiotics resistance of Staphylococcus aureus isolates isolated from raw milk obtained from small-scale dairy farms in Penang, Malaysia. Pakistan Veterinary Journal, 2016, 36(1): 98-102.
Taherikalani M., Hemati S., Heidarzadi K., Mahdavi Z., Ghanbari F., Mohamadi M., Ghafourian S., Varzi A., Jalilian F., Bogdanovic L., Saki K. Unexpectedly high occurrence of Escherichia coli and Staphylococcus aureus isolates from raw milk in Ilam, Western Iran. Journal of Biological Regulators & Homeostatic Agents, 2015, 29(4): 859-863.
Thaker H., Brahmbhatt M., Nayak J. Isolation and identification of Staphylococcus aureus from milk and milk products and their drug resistance patterns in Anand, Gujarat. Vet World, 2013, 6(1): 10-113 https://doi.org/10.5455/vetworld.2013.10-13
Wertheim H., Melles D., Vos M., van Leeuwen W., van Belkum A., Verbrugh H., Nouwen J. The role of nasal carriage in Staphylococcus aureus infections. The Lancet Infectious Diseases, 2005, 5(12): 751-762. https://doi.org/10.1016/S1473-3099(05)70295-4
Zhang S., Iandolo J., Stewart G. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiology Letters, 1998, 168(2): 227-233 https://doi.org/10.1111/j.1574-6968.1998.tb13278.x
This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Open access articles are distributed under the terms and conditions of the Creative Commons Attribution-Share Alike 4.0 International License (CC BY-SA 4.0) license:
https://creativecommons.org/licenses/by-sa/4.0
If you have any questions about the permitted uses of a specific article, please contact us.
Permissions Department of the Academic Publishing House of the UFT Plovdiv
Plovdiv 4002, 26 Maritsa Blvd., Bulgaria
E-mail: editor.in.chief@ijfsab.com
Tel.: +359 (32) 603-802
Fax: +359 32/ 644 102
How to Cite
BANGIEVA, Desislava; RUSEV, Valentin.
Risk from Staphylococcus aureus in informally marketed raw cow milk.
Food Science and Applied Biotechnology, [S.l.], v. 2, n. 1, p. 74-80, mar. 2019.
ISSN 2603-3380.
Available at: <https://www.ijfsab.com/index.php/fsab/article/view/67>. Date accessed: 14 oct. 2024.
doi: https://doi.org/10.30721/fsab2019.v2.i1.67.