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Research Article

volume 52 issue 7 (july 2018) : 1048-1052,   Doi: 10.18805/ijar.B-3311

Molecular detection of enterotoxigenic Staphylococcus aureus isolated from mutton marketed in retail outlets of Chennai, India

S
S. Wilfred Ruban
R
R. Narendra Babu
J
J.J. Abraham Robinson
S
Senthil Kumar
T
T.M.A.P. Kumarasamy
K
K. Porteen
P
P. Raja
1Department of Livestock Products Technology, Veterinary College, Hassan- 573 202, Karnataka, India.
Cite article:- Ruban Wilfred S., Babu Narendra R., Robinson Abraham J.J., Kumar Senthil, Kumarasamy T.M.A.P., Porteen K., Raja P. (2017). Molecular detection of enterotoxigenic Staphylococcus aureus isolated from mutton marketed in retail outlets of Chennai, India. Indian Journal of Animal Research. 52(7): 1048-1052. doi: 10.18805/ijar.B-3311.

ABSTRACT

The present study was aimed at detection of enterotoxigenic S. aureus in mutton marketed in retail outlets of Chennai. A total of 120 meat samples were collected from across Chennai for isolation of S. aureus and it was observed that 66.28 per cent of the samples were contaminated with S. aureus. The S. aureus count in mutton samples ranged from 1.8 x 102 to 4.9 x 104 CFU/ g with an overall average of 1.30 x 104 CFU/ g. All the isolates presumptively identified as S. aureus biochemically, amplified 181 bp product specific for nuc gene by PCR, which is species specific marker for S. aureus. Enterotoxin gene profiles (multiplex PCR) results revealed that 70.17 percent of the isolates were enterotoxigenic carrying only six genes (seb, sed, seg, seh, sei and sej) either alone or in combination, whereas none of these isolates harbored sea, sec and see. It was clear that seb (72.5 %) was the predominant enterotoxin gene followed by seg and sei, seh, sej and sed. Six different toxin gene profiles were exhibited by different isolates and majority of the isolates (55 %) carried two or more genes as compared to only one toxin gene. 

REFERENCES

  1. Ayalew, H., Birhanu. A. and Asrade. B.(2013) Review on food safety system: Ethiopian perspective. African J Fd Sci. 7: 431-440.
  2. Bhandare, S.G., Sherikar, A.T., Paturkar, A.M., Waskar. V.S. and Zende. R.J. (2007). A comparison of microbial contamination of sheep/goat carcasses in a modern Indian abattoir and traditional meat shops. Food Control. 18: 854-868.
  3. Bhandare, S., Paturkar, A.M., Waskar. V.S. and Zende. R.J. (2010). Prevalence of microorganisms of hygienic interest in an organized abattoir in Mumbai. Indian J. Infect. Dev. Ctries. 4(7):454-458.
  4. Blaiotta, G., Ercoline, D., Pennacchia, C., Fusco, V., Casaburi, A., Pepe. O.and Villani. F. ( 2004). PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of seG and seL in S. aureus AB-8802. J. Appl. Microbiol. 97:719–730.
  5. Brown, D.F.J., Edwards, D.I., Hawkey, P.M., Morrison, D., Ridgway, G.L., Towner. K.J. and Wren. M.W.D. (2005). Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant staphylococcus aureus (MRSA). J. Antimicro. Chemotherapy. 56(6):1000-08.
  6. Cha, J.O., Lee, J.K., Jung, Y.H., Yoo, J.I., Park, Y.K., Kim. B.S. and Y.S. Lee. (2006). Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J. Appl. Microbiol. 101: 864–871. 
  7. Chiang, Y.C., Chang, L.T, Lin., C.W., Yang. C.Y. and Tsen. H.Y. (2006). PCR primers for the detection of staphylococcal enterotoxins K, L, and M and survey of staphylococcal enterotoxin types in Staphylococcus aureus isolates from food poisoning cases in Taiwan. J Fd Protect..69: 1072–1079.
  8. Demir, C., Aslantas, O., Duran, N., Ocak S. and Ozer. B. (2011). Investigation of toxin genes in Staphylococcus aureus strains isolated in Mustafa Kemal University Hospital. Turk J Med Sci. 41 (2): 343-352.
  9. Endale, B.G. and Hailay. G. (2013). Assessment of bacteriological quality of meat contact surfaces in selected butcher shops of Mekelle city, Ethiopia. J. Environ. and Occupational Sci. 2: 61-66.
  10. Gencay, Y.E., Ayaz. A.D. and Kasýmoglu-Dogru. A. (2010). Enterotoxin gene profiles of Staphylococcus aureus and other Staphylococcal isolates from various foods and food ingredients. Erciyes Universitesi Veteriner Fakultesi Dergisi. 7(2):75–80.
  11. Gundogan, N., Citak, S., Yucel. N. and Devren. A. (2005). A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Sci. 69 (4): 807–810.
  12. Gayathri, T. and Anu. S.A. 2015. Isolation and Characterization of Microorganisms from Raw Meat Obtained from Different Market Places in and Around Chennai. J Pharm Chem Biol Sci. 3(2): 295-301.
  13. Hedge, R., Isloor, S., Nithin Prabhu, K., Shome. B.R., Rathnamma, D., Suryanarayana, V.V.S., Yatiraj, S., Prasad, R., Krishnaveni, C., Sundareshan, N., Akhila, D.S., Gomes. A.R. and Hegde. N.R. ((2013)). Incidence of sub-clinical mastitis and prevalence of major mastitis pathogens in organized farms and unorganized sectors. Ind J. Microbiol. 53(3): 315–320.
  14. Haileselassie, M., Taddele, H.., Adhana. K. and Kalayou. S. (2013). Food safety knowledge and practices of abattoir and butchery shops and the microbial profile of meat in Mekelle City. Asian Pac. J Trop. Biomed. 3: 407-412.
  15. Hu, Y., Meng, J., Shi, C., Hervin. K., Fratamico. P.M. and Shi. X. (2013). Characterization and comparative analysis of a second thermonuclease from Staphylococcus aureus. Microbiol. Res. 168 (3): 174–182.
  16. Hwang, S.U., Kim, S.H., Jang, E.J., Kwon, N.H., Park, Y.K., Koo, H.C., Jung, W.K., Kim. J.M. and Park. Y.H. (2007). Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea. Int. J. Food Microbiol. 117: 99–105.
  17. ISO 6888-1: (1999). Horizontal methods for enumeration of coagulase positive Staphylococci (Stahylococcus aureus and other species). Part 1: Technique using Baird-Parker agar medium. International Organization for Standardization, Geneva, Switzerland.
  18. Lovseth, A., Loncarevic. S. and Berdal. K. (2004). Modified multiplex PCR method for detection of pyrogenic exotoxin genes in staphylococcal isolates. J. Clin. Microbiol. 42: 3869–3872.
  19. Monday, S. and Bohach. G.A. (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J. Clin. Microbiol. 37: 3411–3414.
  20. Normanno, G., Firinub, A., Virgiliob, S., Mulab, G., Dambrosioa, A., Poggiub, A., Decastellic. L. and Mioni. R. (2005). Coagulase-    positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol. 98: 73– 79.
  21. Omoe, K., Ishikawa, M., Shimoda, Y., Hu, D., Ueda. S. and Shinagawa. K. (2002). Detection of seg, seh and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harbouring seg, seh or sei genes. J. Clin. Microbiol. 40: 857–862.
  22. Pal, M. 2001. Epidemiology of staphylococcal food poisoning. Beverage and Food World. 28:11-13.
  23. Ramya, P., Tirupathi Reddy, E., Vijaya Kumar A. and Krishnaiah. N. (2015). A study on microbiological analysis of raw meat. Int. J Institut Pharm Life Sci. 5(4): 1-9.
  24. Rosec, J.P. and Gigaud. O. (2002). Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int. J. Food Microbiol. 77: 61–70.
  25. Schelin, J., Wallin-Carlquist, N., Cohn, M.T., Lindqvist, R., Barker. G.C. and. Radstrom. P (2011). The formation of S. aureus enterotoxin in food environments and advances in risk assessment. Virulence. 2: 580–592.
  26. Sharma, K.P. and U.K. Chattopadhay. 2015. Assessment of Microbial load of raw meat Samples sold in the Open Markets of city of Kolkata. IOSR J Agric Vet Sci. 8(3): 24-27. 
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Indian Journal of Animal Research
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    Research Article

    volume 52 issue 7 (july 2018) : 1048-1052,   Doi: 10.18805/ijar.B-3311

    Molecular detection of enterotoxigenic Staphylococcus aureus isolated from mutton marketed in retail outlets of Chennai, India

    S
    S. Wilfred Ruban
    R
    R. Narendra Babu
    J
    J.J. Abraham Robinson
    S
    Senthil Kumar
    T
    T.M.A.P. Kumarasamy
    K
    K. Porteen
    P
    P. Raja
    1Department of Livestock Products Technology, Veterinary College, Hassan- 573 202, Karnataka, India.
    Cite article:- Ruban Wilfred S., Babu Narendra R., Robinson Abraham J.J., Kumar Senthil, Kumarasamy T.M.A.P., Porteen K., Raja P. (2017). Molecular detection of enterotoxigenic Staphylococcus aureus isolated from mutton marketed in retail outlets of Chennai, India. Indian Journal of Animal Research. 52(7): 1048-1052. doi: 10.18805/ijar.B-3311.

    ABSTRACT

    The present study was aimed at detection of enterotoxigenic S. aureus in mutton marketed in retail outlets of Chennai. A total of 120 meat samples were collected from across Chennai for isolation of S. aureus and it was observed that 66.28 per cent of the samples were contaminated with S. aureus. The S. aureus count in mutton samples ranged from 1.8 x 102 to 4.9 x 104 CFU/ g with an overall average of 1.30 x 104 CFU/ g. All the isolates presumptively identified as S. aureus biochemically, amplified 181 bp product specific for nuc gene by PCR, which is species specific marker for S. aureus. Enterotoxin gene profiles (multiplex PCR) results revealed that 70.17 percent of the isolates were enterotoxigenic carrying only six genes (seb, sed, seg, seh, sei and sej) either alone or in combination, whereas none of these isolates harbored sea, sec and see. It was clear that seb (72.5 %) was the predominant enterotoxin gene followed by seg and sei, seh, sej and sed. Six different toxin gene profiles were exhibited by different isolates and majority of the isolates (55 %) carried two or more genes as compared to only one toxin gene. 

    REFERENCES

    1. Ayalew, H., Birhanu. A. and Asrade. B.(2013) Review on food safety system: Ethiopian perspective. African J Fd Sci. 7: 431-440.
    2. Bhandare, S.G., Sherikar, A.T., Paturkar, A.M., Waskar. V.S. and Zende. R.J. (2007). A comparison of microbial contamination of sheep/goat carcasses in a modern Indian abattoir and traditional meat shops. Food Control. 18: 854-868.
    3. Bhandare, S., Paturkar, A.M., Waskar. V.S. and Zende. R.J. (2010). Prevalence of microorganisms of hygienic interest in an organized abattoir in Mumbai. Indian J. Infect. Dev. Ctries. 4(7):454-458.
    4. Blaiotta, G., Ercoline, D., Pennacchia, C., Fusco, V., Casaburi, A., Pepe. O.and Villani. F. ( 2004). PCR detection of staphylococcal enterotoxin genes in Staphylococcus spp. strains isolated from meat and dairy products. Evidence for new variants of seG and seL in S. aureus AB-8802. J. Appl. Microbiol. 97:719–730.
    5. Brown, D.F.J., Edwards, D.I., Hawkey, P.M., Morrison, D., Ridgway, G.L., Towner. K.J. and Wren. M.W.D. (2005). Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant staphylococcus aureus (MRSA). J. Antimicro. Chemotherapy. 56(6):1000-08.
    6. Cha, J.O., Lee, J.K., Jung, Y.H., Yoo, J.I., Park, Y.K., Kim. B.S. and Y.S. Lee. (2006). Molecular analysis of Staphylococcus aureus isolates associated with staphylococcal food poisoning in South Korea. J. Appl. Microbiol. 101: 864–871. 
    7. Chiang, Y.C., Chang, L.T, Lin., C.W., Yang. C.Y. and Tsen. H.Y. (2006). PCR primers for the detection of staphylococcal enterotoxins K, L, and M and survey of staphylococcal enterotoxin types in Staphylococcus aureus isolates from food poisoning cases in Taiwan. J Fd Protect..69: 1072–1079.
    8. Demir, C., Aslantas, O., Duran, N., Ocak S. and Ozer. B. (2011). Investigation of toxin genes in Staphylococcus aureus strains isolated in Mustafa Kemal University Hospital. Turk J Med Sci. 41 (2): 343-352.
    9. Endale, B.G. and Hailay. G. (2013). Assessment of bacteriological quality of meat contact surfaces in selected butcher shops of Mekelle city, Ethiopia. J. Environ. and Occupational Sci. 2: 61-66.
    10. Gencay, Y.E., Ayaz. A.D. and Kasýmoglu-Dogru. A. (2010). Enterotoxin gene profiles of Staphylococcus aureus and other Staphylococcal isolates from various foods and food ingredients. Erciyes Universitesi Veteriner Fakultesi Dergisi. 7(2):75–80.
    11. Gundogan, N., Citak, S., Yucel. N. and Devren. A. (2005). A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Sci. 69 (4): 807–810.
    12. Gayathri, T. and Anu. S.A. 2015. Isolation and Characterization of Microorganisms from Raw Meat Obtained from Different Market Places in and Around Chennai. J Pharm Chem Biol Sci. 3(2): 295-301.
    13. Hedge, R., Isloor, S., Nithin Prabhu, K., Shome. B.R., Rathnamma, D., Suryanarayana, V.V.S., Yatiraj, S., Prasad, R., Krishnaveni, C., Sundareshan, N., Akhila, D.S., Gomes. A.R. and Hegde. N.R. ((2013)). Incidence of sub-clinical mastitis and prevalence of major mastitis pathogens in organized farms and unorganized sectors. Ind J. Microbiol. 53(3): 315–320.
    14. Haileselassie, M., Taddele, H.., Adhana. K. and Kalayou. S. (2013). Food safety knowledge and practices of abattoir and butchery shops and the microbial profile of meat in Mekelle City. Asian Pac. J Trop. Biomed. 3: 407-412.
    15. Hu, Y., Meng, J., Shi, C., Hervin. K., Fratamico. P.M. and Shi. X. (2013). Characterization and comparative analysis of a second thermonuclease from Staphylococcus aureus. Microbiol. Res. 168 (3): 174–182.
    16. Hwang, S.U., Kim, S.H., Jang, E.J., Kwon, N.H., Park, Y.K., Koo, H.C., Jung, W.K., Kim. J.M. and Park. Y.H. (2007). Novel multiplex PCR for the detection of the Staphylococcus aureus superantigen and its application to raw meat isolates in Korea. Int. J. Food Microbiol. 117: 99–105.
    17. ISO 6888-1: (1999). Horizontal methods for enumeration of coagulase positive Staphylococci (Stahylococcus aureus and other species). Part 1: Technique using Baird-Parker agar medium. International Organization for Standardization, Geneva, Switzerland.
    18. Lovseth, A., Loncarevic. S. and Berdal. K. (2004). Modified multiplex PCR method for detection of pyrogenic exotoxin genes in staphylococcal isolates. J. Clin. Microbiol. 42: 3869–3872.
    19. Monday, S. and Bohach. G.A. (1999). Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J. Clin. Microbiol. 37: 3411–3414.
    20. Normanno, G., Firinub, A., Virgiliob, S., Mulab, G., Dambrosioa, A., Poggiub, A., Decastellic. L. and Mioni. R. (2005). Coagulase-    positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. Int J Food Microbiol. 98: 73– 79.
    21. Omoe, K., Ishikawa, M., Shimoda, Y., Hu, D., Ueda. S. and Shinagawa. K. (2002). Detection of seg, seh and sei genes in Staphylococcus aureus isolates and determination of the enterotoxin productivities of S. aureus isolates harbouring seg, seh or sei genes. J. Clin. Microbiol. 40: 857–862.
    22. Pal, M. 2001. Epidemiology of staphylococcal food poisoning. Beverage and Food World. 28:11-13.
    23. Ramya, P., Tirupathi Reddy, E., Vijaya Kumar A. and Krishnaiah. N. (2015). A study on microbiological analysis of raw meat. Int. J Institut Pharm Life Sci. 5(4): 1-9.
    24. Rosec, J.P. and Gigaud. O. (2002). Staphylococcal enterotoxin genes of classical and new types detected by PCR in France. Int. J. Food Microbiol. 77: 61–70.
    25. Schelin, J., Wallin-Carlquist, N., Cohn, M.T., Lindqvist, R., Barker. G.C. and. Radstrom. P (2011). The formation of S. aureus enterotoxin in food environments and advances in risk assessment. Virulence. 2: 580–592.
    26. Sharma, K.P. and U.K. Chattopadhay. 2015. Assessment of Microbial load of raw meat Samples sold in the Open Markets of city of Kolkata. IOSR J Agric Vet Sci. 8(3): 24-27. 
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