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Current IssueEditorial BoardOnline First ArticlesArchive

Research Article

volume 54 issue 10 (october 2020) : 1265-1271,   Doi: 10.18805/ijar.B-3883

Characterization of Escherichia coli Isolated from Bovine Subclinical Mastitis for Virulence Genes, Phylogenetic Groups and ESBL Production

S
S.M. Nalband
R
R.P. Kolhe
P
P.D. Deshpande
S
S.N. Jadhav
D
D.G. Gandhale
D
D.M. Muglikar
S
S.R. Kolhe
S
S.S. Bhave
U
U.V. Jagtap
C
C.V. Dhandore
1Department of Veterinary Public Health, KNP College of Veterinary Science Shirwal, Satara-412 801, Maharashtra, India.
Cite article:- Nalband S.M., Kolhe R.P., Deshpande P.D., Jadhav S.N., Gandhale D.G., Muglikar D.M., Kolhe S.R., Bhave S.S., Jagtap U.V., Dhandore C.V. (2020). Characterization of Escherichia coli Isolated from Bovine Subclinical Mastitis for Virulence Genes, Phylogenetic Groups and ESBL Production. Indian Journal of Animal Research. 54(10): 1265-1271. doi: 10.18805/ijar.B-3883.

ABSTRACT

Pathogenic E. coli associated with bovine mastitis are least studied group of microbes in India. Thus an investigation was carried out to know the occurrence of bovine subclinical mastitis and E. coli at different dairy farms. E. coli strains isolated from clinical and environmental samples were screened for virulent genes namely, eae, bfpA, iapH, aggR, elt, est, stx1/stx2; phylogenetic groups and for ESBL production. Findings revealed high prevalence of subclinical mastitis (45%). E. coli strains were isolated from milk, udder, milking machine, floor swabs, etc. Out of 81 E. coli, 38 (46.91%) were ESBL producers. The virulent genes in single or in combination were detected in 55 strains and eae gene was predominant (43.20%). The stx1/stx2 were detected in 2.47% samples. E. coli isolates fall under phylogenetic groups B1 (58.18%), A (23.63%) and D (18.18%). Phylogenetic group B2 was not detected. Dairy cattle could act as a reservoir of ESBL type diarrheagenic E. coli. 

REFERENCES

  1. Abebe, R., Hatiya, H., Abera, M., Megersa, B., Asmare, K. (2016). Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at Hawassa milk shed, South Ethiopia. BMC Veterinary Research. 12: 270. DOI: 10.1186/s12917-016-0905-3.
  2. Ali, T., Ur Rahman, S., Zhang, L., Shahid, M., Zhang, S., Liu, G., Gao, J., Han, B. (2016). ESBL-Producing Escherichia coli from cows suffering mastitis in China contain clinical class 1 integrons with CTX-M linked to ISCR1. Frontiers in Microbiology. 7: 1931.DOI:10.3389/fmicb.2016.01931.
  3. Aranda, K.R.S., Fabbricotti, S.H.,Fagundes Neto, U., Scaletsky, I.C.A. (2007). Single multiplex assay to identify simultaneously enteropathogenic, enteroaggregative, enterotoxigenic, enteroinvasive and Shiga toxin-producing Escherichia coli strains in Brazilian children. FEMS Microbiology Letters. 267: 145-150.
  4. Bandyopadhyay, S., Samanta, I., Bhattacharyya, D., Nanda, P.K., Kar, D., Chowdhury, J., Dandapat, P., Das, A.K., et al. (2015). Co-infection of methicillin-resistant Staphylococcus epidermidis, methicillin-resistant Staphylococcus aureus and extended spectrum â-lactamase producing Escherichia coli in bovine mastitis - Three cases reported from India. Vet Quarterly. 35: 56-61. 
  5. Bangar, Y.C., Singh, B., Dohare, A.K., Verma, M.R. (2015). A systematic review and meta-analysis of prevalence of subclinical mastitis in dairy cows in India. Tropical Animal    Health and Production. 47: 291-297.
  6. Blum, SE., Heller, E.D., Sela, S., Elad, D., Edery, N.,Leitner, G. (2015). Genomic and phenomic study of mammary pathogenic Escherichia coli. PLoS ONE. 10: e0136387.
  7. Caine, L.A., Nwodo, U.U., Okoh, A.I., Ndip, R.N., Green, E. (2014). Occurrence of virulence genes associated with diarrheagenic Escherichia coli isolated from raw cow’s milk from two commercial dairy farms in the eastern cape province, South Africa. International Journal of Environmental Research and Public Health. 11: 11950-11963.
  8. Clermont, O., Bonacorsi, S., Bingen, E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology. 66: 4555-4558.
  9. Clinical and Laboratory Standards Institute (CLSI) (2014). Performance Standards for Antimicrobial Susceptibility Testing (27th Edn.) CLSI supplement M100, Wayne, Pennsylvania, USA, pp. 32-40.
  10. Das, A., Guha, C., Biswas, U., Jana, P.S., Chatterjee, A., Samanta, I. (2017). Detection of emerging antibiotic resistance in bacteria isolated from subclinical mastitis in cattle in West Bengal. Veterinary World. 10: 517-520. 
  11. Dubal, Z.B., Rahman, H., Pal, P., Kumar, A., Pradhan, K. (2010). Characterization and antimicrobial sensitivity of the pathogens isolated from bovine mastitis with special reference to Escherichia coli and Staphylococcus spp. Indian Journal of Animal Sciences. 80: 1163-1167. 
  12. Fernandes, J.B., Zanardo, L.G., Galvão, N.N., Carvalho, I.A., Nero, L.A., Moreira, M.A. (2011). Escherichia coli from clinical mastitis: serotypes and virulence factors. Journal of Veterinary Diagnostic Investigation. 23: 1146-1152.
  13. Ghatak, S., Sinha, A., Sen, A., Guha, C., Ahuja, A., Bhattacharjee, U., Das, S., Pradhan, N.R., Puro, K., Jana, C., et al. (2013). Detection of New Delhi metallo-beta-lactamase and extended-spectrum beta-lactamase genes in Escherichia coli isolated from mastitic milk samples. Transboundary and Emerging Diseases. 60: 385-389. 
  14. Gomes, F., Saavedra, M.J., Henriques, M. (2016). Bovine mastitis disease/pathogenicity: evidence of the potential role of microbial biofilms. Pathogens and Disease. 74: ftw006. DOI: 10.1093/femspd/ftw006.
  15. Guler, L., Gunduz, K. (2007). Virulence properties of E. coli isolated from clinical bovine mastitis. Turkish Journal of Veterinary and Animal Sciences. 31: 361-365.
  16. Hiitiö, H., Vakkamäki, J., Simojokim H., Autio, T., Junnila, J., Pelkonen, S., Pyörälä, S. (2017). Prevalence of subclinical mastitis in Finnish dairy cows: changes during recent decades and impact of cow and herd factors. Acta Veterinaria Scandinavica. 59: 22. DOI: 10.1186/s13028-017-0288-x.
  17. Houser, B.A., Donaldson, S.C.,Padte, R., Sawant,A.A., Deb, C., Roy,C., Jayarao, B.M. (2008).Assessment of phenotypic and genotypic diversity of Escherichia coli shed by healthy lactating dairy cattle. Foodborne Pathogens and Disease. 5: 41-51.
  18. Kaipainen, T., Pohjanvirta, T., Shpigel, N.Y., Shwimmer, A , A., Pyörälä, S., Pelkonen, S. (2002). Virulence factors of Escherichia coli isolated from bovine clinical mastitis. Veterinary Microbiology. 85:37-46.
  19. Kempf, F., Loux,V., Germon, P. (2015). Genome sequences of two bovine mastitis-causing Escherichia coli strains. Genome Announcements 3: e00259-15. DOI:10.1128/genomeA.00259-15.
  20. Lamey, A.E., Ammar, A.M., Zaki, E.R., Khairy, N., Moshref, B.S., Refai, M.K. (2013). Virulence factorsof Escherichia coli isolated from recurrent cases of clinical and subclinical mastitis in buffaloes. International Journal of Microbiology Research. 4: 86-94.
  21. Leimbach, A., Poehlein, A., Vollmers, J., Görlich, D., Daniel, R., Dobrindt, U. (2017). No evidence for a bovine mastitis Escherichia coli pathotype. BMC Genomics. 18: 359. DOI: 10.1186/    s12864-017-3739-x.
  22. Lira, W.M., Macedo, C., Marin, J.M. (2004). The incidence of Shiga toxin-producing Escherichia coli in cattle with mastitis in Brazil. Journal of Applied Microbiology. 97: 861-866.
  23. Milanov, D.,Pruniæ, B., Velhner, M., Todoroviæ, D., Polaèek, V. (2015). Investigation of biofilm formation and phylogenetic typing of Escherichia coli strains isolated from milk of cows with mastitis. Acta Veterinaria-Beograd. 65: 202-216.
  24. Momtaz, H., Dehkordi, F.S., Taktaz, T., Rezvani, A., Yarali, S. (2012). Shiga toxin producing Escherichia coli isolated from bovine mastitic milk: Serogroups, virulence factors and antibiotic resistance properties. Scientific World Journal. : 618709. DOI: 10.1100/2012/618709.
  25. Odenthal, S., Akineden, O., Usleber, E. (2016). Extended-spectrum â-lactamaseproducing Enterobacteriaceae in bulk tank milk from German dairy farms. International Journal of Food Microbiology. 238: 72-78. 
  26. Rangel, P., Marin, J.M. (2009). Analysis of Escherichia coli isolated from bovine mastitic milk. Pesquisa Veterinaria Brasileira. 29: 363-368.
  27. Roussel, P., Porcherie, A., Répérant-Ferter, M., Cunha, P., Gitton, C., Rainard, P., Germon, P. (2017). Escherichia coli mastitis strains: In vitro phenotypes and severity of infection in vivo. PLoS ONE. 12: e0178285. DOI: 10.1371/journal.pone.0178285.
  28. Sharma, P. A., Chhabra, R., Sindhu, N. (2012). Prevalence of sub clinical mastitis in cows: its etiology and antibiogram. Indian Journal of Animal Research. 46: 348-353.
  29. Suojala, L., Pohjanvirta, T., Simojoki, H., Myllyniemi, A.L., Pitkälä, A., Pelkonen, S., Pyörälä, S. (2011). Phylogeny, virulence factors and antimicrobial susceptibility of Escherichia coli isolated in clinical bovine mastitis. Veterinary Microbiology. 147: 383-388.
  30. Tark, D.S., Moon, D.C., Kang, H.Y., Kim, S.R., Nam, H.M., Lee, H.S., Jung, S.C., Lim, S.K. (2017). Antimicrobial susceptibility and characterization of extended-spectrum â-lactamases in Escherichia coli isolated from bovine mastitic milk in South Korea from 2012 to 2015. Journal of Dairy Science. 100: 3463-3469.
  31. Tavakoli, M.H., Pourtaghi, H. (2017). Molecular detection of virulence genes and multi-drug resistance patterns in Escherichia coli (STEC) in clinical bovine mastitis: Alborz province, Iran. Iranian Journal of Veterinary Research.18: 208-211.
     
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Indian Journal of Animal Research
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    Research Article

    volume 54 issue 10 (october 2020) : 1265-1271,   Doi: 10.18805/ijar.B-3883

    Characterization of Escherichia coli Isolated from Bovine Subclinical Mastitis for Virulence Genes, Phylogenetic Groups and ESBL Production

    S
    S.M. Nalband
    R
    R.P. Kolhe
    P
    P.D. Deshpande
    S
    S.N. Jadhav
    D
    D.G. Gandhale
    D
    D.M. Muglikar
    S
    S.R. Kolhe
    S
    S.S. Bhave
    U
    U.V. Jagtap
    C
    C.V. Dhandore
    1Department of Veterinary Public Health, KNP College of Veterinary Science Shirwal, Satara-412 801, Maharashtra, India.
    Cite article:- Nalband S.M., Kolhe R.P., Deshpande P.D., Jadhav S.N., Gandhale D.G., Muglikar D.M., Kolhe S.R., Bhave S.S., Jagtap U.V., Dhandore C.V. (2020). Characterization of Escherichia coli Isolated from Bovine Subclinical Mastitis for Virulence Genes, Phylogenetic Groups and ESBL Production. Indian Journal of Animal Research. 54(10): 1265-1271. doi: 10.18805/ijar.B-3883.

    ABSTRACT

    Pathogenic E. coli associated with bovine mastitis are least studied group of microbes in India. Thus an investigation was carried out to know the occurrence of bovine subclinical mastitis and E. coli at different dairy farms. E. coli strains isolated from clinical and environmental samples were screened for virulent genes namely, eae, bfpA, iapH, aggR, elt, est, stx1/stx2; phylogenetic groups and for ESBL production. Findings revealed high prevalence of subclinical mastitis (45%). E. coli strains were isolated from milk, udder, milking machine, floor swabs, etc. Out of 81 E. coli, 38 (46.91%) were ESBL producers. The virulent genes in single or in combination were detected in 55 strains and eae gene was predominant (43.20%). The stx1/stx2 were detected in 2.47% samples. E. coli isolates fall under phylogenetic groups B1 (58.18%), A (23.63%) and D (18.18%). Phylogenetic group B2 was not detected. Dairy cattle could act as a reservoir of ESBL type diarrheagenic E. coli. 

    REFERENCES

    1. Abebe, R., Hatiya, H., Abera, M., Megersa, B., Asmare, K. (2016). Bovine mastitis: prevalence, risk factors and isolation of Staphylococcus aureus in dairy herds at Hawassa milk shed, South Ethiopia. BMC Veterinary Research. 12: 270. DOI: 10.1186/s12917-016-0905-3.
    2. Ali, T., Ur Rahman, S., Zhang, L., Shahid, M., Zhang, S., Liu, G., Gao, J., Han, B. (2016). ESBL-Producing Escherichia coli from cows suffering mastitis in China contain clinical class 1 integrons with CTX-M linked to ISCR1. Frontiers in Microbiology. 7: 1931.DOI:10.3389/fmicb.2016.01931.
    3. Aranda, K.R.S., Fabbricotti, S.H.,Fagundes Neto, U., Scaletsky, I.C.A. (2007). Single multiplex assay to identify simultaneously enteropathogenic, enteroaggregative, enterotoxigenic, enteroinvasive and Shiga toxin-producing Escherichia coli strains in Brazilian children. FEMS Microbiology Letters. 267: 145-150.
    4. Bandyopadhyay, S., Samanta, I., Bhattacharyya, D., Nanda, P.K., Kar, D., Chowdhury, J., Dandapat, P., Das, A.K., et al. (2015). Co-infection of methicillin-resistant Staphylococcus epidermidis, methicillin-resistant Staphylococcus aureus and extended spectrum â-lactamase producing Escherichia coli in bovine mastitis - Three cases reported from India. Vet Quarterly. 35: 56-61. 
    5. Bangar, Y.C., Singh, B., Dohare, A.K., Verma, M.R. (2015). A systematic review and meta-analysis of prevalence of subclinical mastitis in dairy cows in India. Tropical Animal    Health and Production. 47: 291-297.
    6. Blum, SE., Heller, E.D., Sela, S., Elad, D., Edery, N.,Leitner, G. (2015). Genomic and phenomic study of mammary pathogenic Escherichia coli. PLoS ONE. 10: e0136387.
    7. Caine, L.A., Nwodo, U.U., Okoh, A.I., Ndip, R.N., Green, E. (2014). Occurrence of virulence genes associated with diarrheagenic Escherichia coli isolated from raw cow’s milk from two commercial dairy farms in the eastern cape province, South Africa. International Journal of Environmental Research and Public Health. 11: 11950-11963.
    8. Clermont, O., Bonacorsi, S., Bingen, E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology. 66: 4555-4558.
    9. Clinical and Laboratory Standards Institute (CLSI) (2014). Performance Standards for Antimicrobial Susceptibility Testing (27th Edn.) CLSI supplement M100, Wayne, Pennsylvania, USA, pp. 32-40.
    10. Das, A., Guha, C., Biswas, U., Jana, P.S., Chatterjee, A., Samanta, I. (2017). Detection of emerging antibiotic resistance in bacteria isolated from subclinical mastitis in cattle in West Bengal. Veterinary World. 10: 517-520. 
    11. Dubal, Z.B., Rahman, H., Pal, P., Kumar, A., Pradhan, K. (2010). Characterization and antimicrobial sensitivity of the pathogens isolated from bovine mastitis with special reference to Escherichia coli and Staphylococcus spp. Indian Journal of Animal Sciences. 80: 1163-1167. 
    12. Fernandes, J.B., Zanardo, L.G., Galvão, N.N., Carvalho, I.A., Nero, L.A., Moreira, M.A. (2011). Escherichia coli from clinical mastitis: serotypes and virulence factors. Journal of Veterinary Diagnostic Investigation. 23: 1146-1152.
    13. Ghatak, S., Sinha, A., Sen, A., Guha, C., Ahuja, A., Bhattacharjee, U., Das, S., Pradhan, N.R., Puro, K., Jana, C., et al. (2013). Detection of New Delhi metallo-beta-lactamase and extended-spectrum beta-lactamase genes in Escherichia coli isolated from mastitic milk samples. Transboundary and Emerging Diseases. 60: 385-389. 
    14. Gomes, F., Saavedra, M.J., Henriques, M. (2016). Bovine mastitis disease/pathogenicity: evidence of the potential role of microbial biofilms. Pathogens and Disease. 74: ftw006. DOI: 10.1093/femspd/ftw006.
    15. Guler, L., Gunduz, K. (2007). Virulence properties of E. coli isolated from clinical bovine mastitis. Turkish Journal of Veterinary and Animal Sciences. 31: 361-365.
    16. Hiitiö, H., Vakkamäki, J., Simojokim H., Autio, T., Junnila, J., Pelkonen, S., Pyörälä, S. (2017). Prevalence of subclinical mastitis in Finnish dairy cows: changes during recent decades and impact of cow and herd factors. Acta Veterinaria Scandinavica. 59: 22. DOI: 10.1186/s13028-017-0288-x.
    17. Houser, B.A., Donaldson, S.C.,Padte, R., Sawant,A.A., Deb, C., Roy,C., Jayarao, B.M. (2008).Assessment of phenotypic and genotypic diversity of Escherichia coli shed by healthy lactating dairy cattle. Foodborne Pathogens and Disease. 5: 41-51.
    18. Kaipainen, T., Pohjanvirta, T., Shpigel, N.Y., Shwimmer, A , A., Pyörälä, S., Pelkonen, S. (2002). Virulence factors of Escherichia coli isolated from bovine clinical mastitis. Veterinary Microbiology. 85:37-46.
    19. Kempf, F., Loux,V., Germon, P. (2015). Genome sequences of two bovine mastitis-causing Escherichia coli strains. Genome Announcements 3: e00259-15. DOI:10.1128/genomeA.00259-15.
    20. Lamey, A.E., Ammar, A.M., Zaki, E.R., Khairy, N., Moshref, B.S., Refai, M.K. (2013). Virulence factorsof Escherichia coli isolated from recurrent cases of clinical and subclinical mastitis in buffaloes. International Journal of Microbiology Research. 4: 86-94.
    21. Leimbach, A., Poehlein, A., Vollmers, J., Görlich, D., Daniel, R., Dobrindt, U. (2017). No evidence for a bovine mastitis Escherichia coli pathotype. BMC Genomics. 18: 359. DOI: 10.1186/    s12864-017-3739-x.
    22. Lira, W.M., Macedo, C., Marin, J.M. (2004). The incidence of Shiga toxin-producing Escherichia coli in cattle with mastitis in Brazil. Journal of Applied Microbiology. 97: 861-866.
    23. Milanov, D.,Pruniæ, B., Velhner, M., Todoroviæ, D., Polaèek, V. (2015). Investigation of biofilm formation and phylogenetic typing of Escherichia coli strains isolated from milk of cows with mastitis. Acta Veterinaria-Beograd. 65: 202-216.
    24. Momtaz, H., Dehkordi, F.S., Taktaz, T., Rezvani, A., Yarali, S. (2012). Shiga toxin producing Escherichia coli isolated from bovine mastitic milk: Serogroups, virulence factors and antibiotic resistance properties. Scientific World Journal. : 618709. DOI: 10.1100/2012/618709.
    25. Odenthal, S., Akineden, O., Usleber, E. (2016). Extended-spectrum â-lactamaseproducing Enterobacteriaceae in bulk tank milk from German dairy farms. International Journal of Food Microbiology. 238: 72-78. 
    26. Rangel, P., Marin, J.M. (2009). Analysis of Escherichia coli isolated from bovine mastitic milk. Pesquisa Veterinaria Brasileira. 29: 363-368.
    27. Roussel, P., Porcherie, A., Répérant-Ferter, M., Cunha, P., Gitton, C., Rainard, P., Germon, P. (2017). Escherichia coli mastitis strains: In vitro phenotypes and severity of infection in vivo. PLoS ONE. 12: e0178285. DOI: 10.1371/journal.pone.0178285.
    28. Sharma, P. A., Chhabra, R., Sindhu, N. (2012). Prevalence of sub clinical mastitis in cows: its etiology and antibiogram. Indian Journal of Animal Research. 46: 348-353.
    29. Suojala, L., Pohjanvirta, T., Simojoki, H., Myllyniemi, A.L., Pitkälä, A., Pelkonen, S., Pyörälä, S. (2011). Phylogeny, virulence factors and antimicrobial susceptibility of Escherichia coli isolated in clinical bovine mastitis. Veterinary Microbiology. 147: 383-388.
    30. Tark, D.S., Moon, D.C., Kang, H.Y., Kim, S.R., Nam, H.M., Lee, H.S., Jung, S.C., Lim, S.K. (2017). Antimicrobial susceptibility and characterization of extended-spectrum â-lactamases in Escherichia coli isolated from bovine mastitic milk in South Korea from 2012 to 2015. Journal of Dairy Science. 100: 3463-3469.
    31. Tavakoli, M.H., Pourtaghi, H. (2017). Molecular detection of virulence genes and multi-drug resistance patterns in Escherichia coli (STEC) in clinical bovine mastitis: Alborz province, Iran. Iranian Journal of Veterinary Research.18: 208-211.
       
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