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Research Article

volume 52 issue 11 (november 2018) : 1635-1641,   Doi: 10.18805/ijar.B-3414

Molecular Characterization of Listeria monocytogenes in white meat samples from Punjab, India

S
Simranpreet Kaur
R
Randhir Singh
M
Mandeep Kaur Sran
J
J.P.S. Gill
1School of Public Health and Zoonoses, College of Veterinary Sciences, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana-141 004, Punjab, India
Cite article:- Kaur Simranpreet, Singh Randhir, Sran Kaur Mandeep, Gill J.P.S. (2017). Molecular Characterization of Listeria monocytogenes in white meat samples from Punjab, India. Indian Journal of Animal Research. 52(11): 1635-1641. doi: 10.18805/ijar.B-3414.

ABSTRACT

A study was undertaken to assess the prevalence of Listeria monocytogenes in white meats in the Punjab, India. A total of 335 samples including 115 samples of chicken, 75 samples of pork and 145 samples of fish were collected from retail outlets. Isolation of the pathogen was done by selective enrichment in University of Vermont Medium I and II and plating onto PALCAM agar. The recovered Listeria isolates were subjected to in-vitro pathogenicity assays and multiplex PCR targeting virulence-associated genes (prfA, plcA, actA, hlyA and iap) of L. monocytogenes. A total of thirty one (31) L. monocytogenes strains were isolated from meat samples with the prevalence of L. monocytogenes as 9.2%. Maximum prevalence was seen in fish (19.3%) followed by chicken (1.7%) and pork (1.3%). All isolates recovered from the study exhibited pathogenicity in in-vitro pathogenicity assays as well as possessed all the virulence related genes. Thus, the presence of pathogenic strains of L. monocytogenes in white meats with a prevalence of 9.2% appeared to be a cause for concern with profound public health implications.

REFERENCES

  1. Alzubaidy, Z.M., Kakey, S.I. and Ali, J.F. (2013). Isolation and identification of Listeria monocytogenes by PCR from some food sources in Erbil city. Euphrates Journal of Agricultural Science, 5: 14-26.
  2. Barbuddhe, S.B., Swain, B.K., Chakurkar, E.B. and Sundaram, R.N.S. (2003). Microbial quality of poultry meat with special reference to Listeria monocytogenes. Indian Journal of Poultry Science, 38: 305-307.
  3. Beak, S.Y., Lim, S.Y., Lee, D.H., Min, K.H. and Kim, C.M. (2000). Incidence and characterization of Listeria monocytogenes from domestic and imported foods in Korea. Journal of Food Protection, 63: 186-189. 
  4. Ben Embarek, P.K. (1994). Presence, detection and growth of Listeria monocytogenes in seafoods: a review. International Journal of Food Microbiology, 23: 17-34.
  5. Courtieu, A L. (1991). Latest news on Listeriosis. Comparative Immunology Microbiology and Infectious Diseases, 14: 1-7. 
  6. Dhand, N.K. and Khatkar, M.S. (2014). Statulator: An online statistical calculator. Sample Size Calculator for Estimating a Single Proportion. http://statulator. com/SampleSize/ss1P.html#sthash.yIfR2aV7.dpuf
  7. Doijad, S.P., Vaidya, V., Garg, S., Kalekar, S., Rodrigues, J., D’Costa, D., Bhosle, S.N. and Barbuddhe, S.B. (2010). Isolation and Characterization of Listeria Species from Raw and Processed Meats. Journal of Veterinary Public Health, 8: 83-88.
  8. Fallah, A.A., Siavash Saei-Dehkordi, S., Rahnama, M., Tahmasby, H. and Mahzounieh, M. (2012). Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control, 28: 327-332.
  9. Farber, J.M. and Peterkin, P.I. (1991). Listeria monocytogenes, a food borne pathogen. Microbiological Reviews, 55: 476-571.
  10. Furrer, B., Candrian, U., Hoefelein, C. and Luethy, J. (1991). Detection and identification of Listeria monocytogenes in cooked sausage products and in milk by in-vitro amplification of haemolysin gene fragments. Journal of Applied Bacteriology, 70: 372-379.
  11. Germini, A., Masola, A., Carnevali, P. and Marchelli, R. (2009). Simultaneous detection of Escherichia coli O175:H7, Salmonella spp., and Listeria monocytogenes by multiplex PCR. Food Control, 20: 733-738.
  12. Jallewar, P.K., Kalorey, D.R., Kurkure, N.V., Pande, V.V. and Barbuddhe, S.B. (2007). Genotypic characterization of Listeria spp. isolated from fresh water fish. International Journal of Food Microbiology, 114: 120-123.
  13. Jemmi, T. and Stephan, R. (2006). Listeria monocytogenes: food-borne pathogen and hygiene indicator. Revue scientifique et technique (International Office of Epizootics), 25: 571- 580.
  14. Kaur, S., Malik, S.V.S., Vaidya, V.M. and Barbuddhe, S.B. (2007). Listeria monocytogenes in spontaneous abortions in humans and its detection by multiplex PCR. Journal of Applied Microbiology, 103: 1889- 1896.
  15. Khan, J.A., Rathore, R.S., Khan, S. and Ahmad, I. (2013). In vitro detection of pathogenic Listeria monocytogenes from food sources by conventional, molecular and cell culture method. Brazilian Journal of Microbiology, 44: 751-758.
  16. Kwiatek, K. (2004). Occurrence of Listeria monocytogenes in selected food of animal origin. Bulletin of the Veterinary Institute in Pulawy, 48: 269-272.
  17. Leimeister-Wachter, M., Domann, E. and Chakraborty, T. (1991). Detection of a gene encoding a phosahatidylinositol-specific phospholipase C that is coordinately expressed with listeriolysin in Listeria monocytogenes. Molecular Microbiology, 5: 361–366.
  18. McClain, D. and Lee, W.H. (1988). Development of USDA-FSIS method for isolation of Listeria monocytogenes from raw meat and poultry. Journal of the Association of Official Analytical Chemists, 71: 660-663.
  19. Molla, B., Yilma, R. and Alemayehu, D. (2004). Listeria monocytogenes and other Listeria species in retail meat and milk products in Addis Ababa, Ethiopia. The Ethiopian Journal of Health Development, 18: 208-212.
  20. Momtaz, H. and Yadollahi, S. (2013). Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Momtaz Yadollahi Diagnostic Pathology, 8: 149.
  21. Nightingale, K.K., Schukken, Y.H., Nightingale, C.R., Fortes, E.D., Ho, A.J., Her, Z., Grohn, Y.T., McDonough, P.L. and Wiedmann, M. (2004). Ecology and Transmission of Listeria monocytogenes Infecting Ruminants and in the Farm Environment. Applied Environment and Microbiology, 70: 4458-4467.
  22. Notermans, S.H., Dufrenne, J., Wachter, L.M., Domann, E. and Chakraborty, T. (1991). Phosphatidyl inositol-specific phospholipase C activity as a marker to distinguish between pathogenic and non-pathogenic Listeria species. Applied Environment and Microbiology, 57: 2666-2670.
  23. Orsi, R.H., Bakker, H.C.D. and Wiedmann, M. (2011). Listeria monocytogenes lineages: Genomics, evolution, ecology and phenotypic characteristics. International Journal of Medical Microbiology, 301: 79-96.
  24. Pal, A., Labuza, T.P. and Diez-Gonzalez, F. (2008). Evaluating the growth of Listeria monocytogenes in refrigerated ready-to-eat frankfurters: influence of strain, temperature, packaging, lactate and diacetate, and background microflora. Journal of Food    Protection, 71: 1806-1816.
  25. Parihar, V.S., Barbuddhe, S.B., Danielsson-Tham, M.L. and Tham, W. (2008). Isolation and characterization of Listeria species from tropical seafood. Food Control, 19: 566-569.
  26. Paziak-Domanska, B., Boguslawska, E., Wieckowska-Szakiel, M., Kotlowski, R., Rozalska, B., Chmiela, M., Kur, J., Dabrowski, W. and Rudnicka, W. (1999). Evaluation of the API test, Phosphatidylinositol-specific phospholipase C activity and PCR method in identification of Listeria monocytogenes in meat foods. FEMS Microbiology Letters, 171: 209-214.
  27. Rflrvik, M.L., Dominique, A., Caugant, B. and Yndestad, M. (1995). Contamination pattern of Listeria monocytogenes and other Listeria spp. in a salmon slaughterhouse and smoked salmon processing plant. International Journal of Food Microbiology, 25: 19-27.
  28. Rossi, M.L., Paiva, A., Tornese, M., Chianelli, S. and Troncoso, A. (2008). Listeria monocytogenes outbreaks: A review of the routes that favor bacterial presence. Revista Chilena Infectologia, 25: 328-335. 
  29. Schillinger, U., Kaya, M. and Lucke, F.K. (1991). Behaviour of Listeria monocytogenes in meat and its control by a bacteriocin -producing strain of Lactobacillus. Journal of Applied Microbiology, 70: 473-478.
  30. Seeliger, H.P.R. and Jones, D. (1986). Genus Listeria Pirie, 1940, 383, p.1235-1245. In: Sneath, P.M.A., Nair, N.S., Sharpe, M.E., Holt, J.G. (ed.), Bergey’s Manual of Systematic Bacteriology, Vol.2, The Williams and Wilkins Co., Baltimore.
  31. Suarez, M. and Vazquez-Boland J.A. (1999). The bacterial actin nucleator protein actA is involved in epithelial cell invasion by Listeria monocytogenes. PUBMED [Accession No. AF103807].
  32. USDA (United States Department of Agriculture) (1992). Federal Register, 57: 319460- 319467.
  33. Vinothkumar, R., Arunagiri, K. and Sivakumar, T. (2013). Studies on pathogenic Listeria monocytogenes from marine food resources. International Journal of Current Microbiology and Applied Science, 1: 86-93.
  34. Wadud, S., Leon-Velarde, C.G., Larson, N. and Odumeru, J.A. (2010). Evaluation of immunomagnetic separation in combination with ALOA Listeria chromogenic agar for the isolation and identification of Listeria monocytogenes in ready-to-eat foods. Journal of Microbiological Methods, 81: 153-159.
  35. Yadav, M. M., Roy, A., Bhanderi, B. and Joshi, C. (2010). Pheno-genotypic characterization of Listeria monocytogenes from bovine clinical mastitis. Buffalo Bulletin, 29: 29-38.
  36. Yadollahi, S., Momtaz, H., Doudi, M. and Bakhsh, E.J. (2013). The objective of this study was to isolation and characterization of Listeria species and determines Listeria monocytogenes serotypes in fresh fish, shrimp, crab and lobster in Isfahan and Shahrekord. International Journal of Advanced Biological and Biomedical Research, 5: 493-504. 
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Indian Journal of Animal Research
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    Research Article

    volume 52 issue 11 (november 2018) : 1635-1641,   Doi: 10.18805/ijar.B-3414

    Molecular Characterization of Listeria monocytogenes in white meat samples from Punjab, India

    S
    Simranpreet Kaur
    R
    Randhir Singh
    M
    Mandeep Kaur Sran
    J
    J.P.S. Gill
    1School of Public Health and Zoonoses, College of Veterinary Sciences, Guru Angad Dev Veterinary and Animal Sciences University, Ludhiana-141 004, Punjab, India
    Cite article:- Kaur Simranpreet, Singh Randhir, Sran Kaur Mandeep, Gill J.P.S. (2017). Molecular Characterization of Listeria monocytogenes in white meat samples from Punjab, India. Indian Journal of Animal Research. 52(11): 1635-1641. doi: 10.18805/ijar.B-3414.

    ABSTRACT

    A study was undertaken to assess the prevalence of Listeria monocytogenes in white meats in the Punjab, India. A total of 335 samples including 115 samples of chicken, 75 samples of pork and 145 samples of fish were collected from retail outlets. Isolation of the pathogen was done by selective enrichment in University of Vermont Medium I and II and plating onto PALCAM agar. The recovered Listeria isolates were subjected to in-vitro pathogenicity assays and multiplex PCR targeting virulence-associated genes (prfA, plcA, actA, hlyA and iap) of L. monocytogenes. A total of thirty one (31) L. monocytogenes strains were isolated from meat samples with the prevalence of L. monocytogenes as 9.2%. Maximum prevalence was seen in fish (19.3%) followed by chicken (1.7%) and pork (1.3%). All isolates recovered from the study exhibited pathogenicity in in-vitro pathogenicity assays as well as possessed all the virulence related genes. Thus, the presence of pathogenic strains of L. monocytogenes in white meats with a prevalence of 9.2% appeared to be a cause for concern with profound public health implications.

    REFERENCES

    1. Alzubaidy, Z.M., Kakey, S.I. and Ali, J.F. (2013). Isolation and identification of Listeria monocytogenes by PCR from some food sources in Erbil city. Euphrates Journal of Agricultural Science, 5: 14-26.
    2. Barbuddhe, S.B., Swain, B.K., Chakurkar, E.B. and Sundaram, R.N.S. (2003). Microbial quality of poultry meat with special reference to Listeria monocytogenes. Indian Journal of Poultry Science, 38: 305-307.
    3. Beak, S.Y., Lim, S.Y., Lee, D.H., Min, K.H. and Kim, C.M. (2000). Incidence and characterization of Listeria monocytogenes from domestic and imported foods in Korea. Journal of Food Protection, 63: 186-189. 
    4. Ben Embarek, P.K. (1994). Presence, detection and growth of Listeria monocytogenes in seafoods: a review. International Journal of Food Microbiology, 23: 17-34.
    5. Courtieu, A L. (1991). Latest news on Listeriosis. Comparative Immunology Microbiology and Infectious Diseases, 14: 1-7. 
    6. Dhand, N.K. and Khatkar, M.S. (2014). Statulator: An online statistical calculator. Sample Size Calculator for Estimating a Single Proportion. http://statulator. com/SampleSize/ss1P.html#sthash.yIfR2aV7.dpuf
    7. Doijad, S.P., Vaidya, V., Garg, S., Kalekar, S., Rodrigues, J., D’Costa, D., Bhosle, S.N. and Barbuddhe, S.B. (2010). Isolation and Characterization of Listeria Species from Raw and Processed Meats. Journal of Veterinary Public Health, 8: 83-88.
    8. Fallah, A.A., Siavash Saei-Dehkordi, S., Rahnama, M., Tahmasby, H. and Mahzounieh, M. (2012). Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control, 28: 327-332.
    9. Farber, J.M. and Peterkin, P.I. (1991). Listeria monocytogenes, a food borne pathogen. Microbiological Reviews, 55: 476-571.
    10. Furrer, B., Candrian, U., Hoefelein, C. and Luethy, J. (1991). Detection and identification of Listeria monocytogenes in cooked sausage products and in milk by in-vitro amplification of haemolysin gene fragments. Journal of Applied Bacteriology, 70: 372-379.
    11. Germini, A., Masola, A., Carnevali, P. and Marchelli, R. (2009). Simultaneous detection of Escherichia coli O175:H7, Salmonella spp., and Listeria monocytogenes by multiplex PCR. Food Control, 20: 733-738.
    12. Jallewar, P.K., Kalorey, D.R., Kurkure, N.V., Pande, V.V. and Barbuddhe, S.B. (2007). Genotypic characterization of Listeria spp. isolated from fresh water fish. International Journal of Food Microbiology, 114: 120-123.
    13. Jemmi, T. and Stephan, R. (2006). Listeria monocytogenes: food-borne pathogen and hygiene indicator. Revue scientifique et technique (International Office of Epizootics), 25: 571- 580.
    14. Kaur, S., Malik, S.V.S., Vaidya, V.M. and Barbuddhe, S.B. (2007). Listeria monocytogenes in spontaneous abortions in humans and its detection by multiplex PCR. Journal of Applied Microbiology, 103: 1889- 1896.
    15. Khan, J.A., Rathore, R.S., Khan, S. and Ahmad, I. (2013). In vitro detection of pathogenic Listeria monocytogenes from food sources by conventional, molecular and cell culture method. Brazilian Journal of Microbiology, 44: 751-758.
    16. Kwiatek, K. (2004). Occurrence of Listeria monocytogenes in selected food of animal origin. Bulletin of the Veterinary Institute in Pulawy, 48: 269-272.
    17. Leimeister-Wachter, M., Domann, E. and Chakraborty, T. (1991). Detection of a gene encoding a phosahatidylinositol-specific phospholipase C that is coordinately expressed with listeriolysin in Listeria monocytogenes. Molecular Microbiology, 5: 361–366.
    18. McClain, D. and Lee, W.H. (1988). Development of USDA-FSIS method for isolation of Listeria monocytogenes from raw meat and poultry. Journal of the Association of Official Analytical Chemists, 71: 660-663.
    19. Molla, B., Yilma, R. and Alemayehu, D. (2004). Listeria monocytogenes and other Listeria species in retail meat and milk products in Addis Ababa, Ethiopia. The Ethiopian Journal of Health Development, 18: 208-212.
    20. Momtaz, H. and Yadollahi, S. (2013). Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Momtaz Yadollahi Diagnostic Pathology, 8: 149.
    21. Nightingale, K.K., Schukken, Y.H., Nightingale, C.R., Fortes, E.D., Ho, A.J., Her, Z., Grohn, Y.T., McDonough, P.L. and Wiedmann, M. (2004). Ecology and Transmission of Listeria monocytogenes Infecting Ruminants and in the Farm Environment. Applied Environment and Microbiology, 70: 4458-4467.
    22. Notermans, S.H., Dufrenne, J., Wachter, L.M., Domann, E. and Chakraborty, T. (1991). Phosphatidyl inositol-specific phospholipase C activity as a marker to distinguish between pathogenic and non-pathogenic Listeria species. Applied Environment and Microbiology, 57: 2666-2670.
    23. Orsi, R.H., Bakker, H.C.D. and Wiedmann, M. (2011). Listeria monocytogenes lineages: Genomics, evolution, ecology and phenotypic characteristics. International Journal of Medical Microbiology, 301: 79-96.
    24. Pal, A., Labuza, T.P. and Diez-Gonzalez, F. (2008). Evaluating the growth of Listeria monocytogenes in refrigerated ready-to-eat frankfurters: influence of strain, temperature, packaging, lactate and diacetate, and background microflora. Journal of Food    Protection, 71: 1806-1816.
    25. Parihar, V.S., Barbuddhe, S.B., Danielsson-Tham, M.L. and Tham, W. (2008). Isolation and characterization of Listeria species from tropical seafood. Food Control, 19: 566-569.
    26. Paziak-Domanska, B., Boguslawska, E., Wieckowska-Szakiel, M., Kotlowski, R., Rozalska, B., Chmiela, M., Kur, J., Dabrowski, W. and Rudnicka, W. (1999). Evaluation of the API test, Phosphatidylinositol-specific phospholipase C activity and PCR method in identification of Listeria monocytogenes in meat foods. FEMS Microbiology Letters, 171: 209-214.
    27. Rflrvik, M.L., Dominique, A., Caugant, B. and Yndestad, M. (1995). Contamination pattern of Listeria monocytogenes and other Listeria spp. in a salmon slaughterhouse and smoked salmon processing plant. International Journal of Food Microbiology, 25: 19-27.
    28. Rossi, M.L., Paiva, A., Tornese, M., Chianelli, S. and Troncoso, A. (2008). Listeria monocytogenes outbreaks: A review of the routes that favor bacterial presence. Revista Chilena Infectologia, 25: 328-335. 
    29. Schillinger, U., Kaya, M. and Lucke, F.K. (1991). Behaviour of Listeria monocytogenes in meat and its control by a bacteriocin -producing strain of Lactobacillus. Journal of Applied Microbiology, 70: 473-478.
    30. Seeliger, H.P.R. and Jones, D. (1986). Genus Listeria Pirie, 1940, 383, p.1235-1245. In: Sneath, P.M.A., Nair, N.S., Sharpe, M.E., Holt, J.G. (ed.), Bergey’s Manual of Systematic Bacteriology, Vol.2, The Williams and Wilkins Co., Baltimore.
    31. Suarez, M. and Vazquez-Boland J.A. (1999). The bacterial actin nucleator protein actA is involved in epithelial cell invasion by Listeria monocytogenes. PUBMED [Accession No. AF103807].
    32. USDA (United States Department of Agriculture) (1992). Federal Register, 57: 319460- 319467.
    33. Vinothkumar, R., Arunagiri, K. and Sivakumar, T. (2013). Studies on pathogenic Listeria monocytogenes from marine food resources. International Journal of Current Microbiology and Applied Science, 1: 86-93.
    34. Wadud, S., Leon-Velarde, C.G., Larson, N. and Odumeru, J.A. (2010). Evaluation of immunomagnetic separation in combination with ALOA Listeria chromogenic agar for the isolation and identification of Listeria monocytogenes in ready-to-eat foods. Journal of Microbiological Methods, 81: 153-159.
    35. Yadav, M. M., Roy, A., Bhanderi, B. and Joshi, C. (2010). Pheno-genotypic characterization of Listeria monocytogenes from bovine clinical mastitis. Buffalo Bulletin, 29: 29-38.
    36. Yadollahi, S., Momtaz, H., Doudi, M. and Bakhsh, E.J. (2013). The objective of this study was to isolation and characterization of Listeria species and determines Listeria monocytogenes serotypes in fresh fish, shrimp, crab and lobster in Isfahan and Shahrekord. International Journal of Advanced Biological and Biomedical Research, 5: 493-504. 
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