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Research Article

volume 53 issue 7 (july 2019) : 918-925,   Doi: 10.18805/ijar.B-3602

Risk factors for antimicrobial resistance in Escherichia coli isolates from poultry in Haryana

S
S. Kumar
R
R. Gupta
1Department of Veterinary Public Health and Epidemiology, College of Veterinary Sciences, Lala Lajpat Rai University of Veterinary and Animal Sciences, Hisar-125 004, Haryana, India.
Cite article:- Kumar S., Gupta R. (2019). Risk factors for antimicrobial resistance in Escherichia coli isolates from poultry in Haryana. Indian Journal of Animal Research. 53(7): 918-925. doi: 10.18805/ijar.B-3602.

ABSTRACT

Colibacillosis is a disease of severe economic significance to all poultry producers worldwide, characterized by a diverse array of lesions. Due to enormous exploitation of antibiotics in broilers, an increased number of resistant bacterial strains have developed in recent years. 106 E. coli strains were collected from broilers suffering from colibacillosis. The resistance to different classes of antimicrobials was determined. The presence of integrons was determined by Polymerase Chain Reaction (PCR). All the statistical analyses were carried out using STATA™. All the isolates were multidrug resistance (MDR), i.e. resistant to at least one agent in three or more antimicrobial categories. 37 (34.90%) isolates were found positive for Class 1 integrons. There was significant difference in carriage of integrons in different phylogentic groups, p=0.001, however, there was no difference among different serotypes for carriage of integrons. Significant difference was observed for resistance towards co-trimoxazole (p=0.002), piperacillin (p=0.034) and ciprofloxacin (p=0.046) in Class 1 integron carrying isolates and Class 1 integron negative isolates. Significant difference was observed for resistance towards ceftriaxone (p=0.004) and cefotaxime (p=0.027) in relation to phylogenetic groups. Also, significant difference was observed among different serotypes for resistance towards co-trimoxazole (p=0.001), gentamicin (p=0.005) and kanamycin (p=0.041).

REFERENCES

  1. Ahmed, A.M., Shimamoto, T., Shimamoto, T. (2013). Molecular characterization of multidrug-resistant avian pathogenic Escherichia coli isolated from septicemic broilers. International Journal of Medical Microbiology , 303: 475-483.
  2. Bass, L., Liebert, C.A., Lee, M.D., Saummers, A.O., White, D.G., Thayer, S.G., Maurer, J.J. (1999). Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance in avian Esherichia coli. Antimicrobial Agents and Chemotherapy, 43: 2925–2929.
  3. Bauer, A.W., Kirby, W.M., Sherris, J.C., Turck, M. (1966). Antibiotic susceptibility testing by standardized single disk method. American Journal of Clinical Pathology, 45: 493-496.
  4. Butaye, P., Devriese, L.A., Haesebrouck, F. (2003). Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clinical Microbiology Reviews, 16: 175-188.
  5. Clermont, O., Bonacorsi, S., Bingen, E. (2000). Rapid and simple determination of the Esherichia coli phylogenetic group. Applied and Environmental Microbiology, 66: 4555–4558.
  6. Delannoy, S., Beutin, L., Mariani-Kurkdjian, P., Fleiss, A., Bonacorsi, S., Fach, P. (2017). The Escherichia coli serogroup O1 and O2 lipopolysaccharides are encoded by multiple O-antigen gene clusters. Frontiers in Cellular and Infection Microbiology, 7: 30.
  7. Edwards, R. and Ewing, W.N. (1972). Identification of Enterobacteriaceae. 3rd ed., Burgess Publishing Co., Minnesota.
  8. Fabrega, A., Madurga, S., Giralt, E., Vila, J. (2009). Mechanism of action of and resistance to quinolones. Microbial Biotechnology, 2: 40-61.
  9. Giufre, M., Graziani, C., Accogli, M., Luzzi, I., Busani, L., Cerquetti, M. (2012). Escherichia coli of human and avian origin: detection of clonal groups associated with fluoroquinolone and multidrug resistance in Italy. Journal of Antimicrobial Chemotherapy, 67: 860-867.
  10. Jakobsen, L., Spangholm, D.J., Pedersen, K., Jensen, L.B., Emborg, H.D., Agerso, Y., et al. (2010). Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Esherichia coli isolates from community dwelling humans and UTI patients. International Journal of Food Microbiology, 142: 264–272.
  11. Johnson, J.R., Gajewski, A., Lesse, A.J., Russo, T.A. (2003). Extraintestinal pathogenic Escherichia coli as a cause of invasive nonurinary infections. Journal of Clinical Microbiology, 41: 5798–5802.
  12. Kang, M.S., Kim, A., Jung, B.Y., Her, M., Jeong, W., Cho, Y.M., Oh, J.Y., Lee, Y.J, Kwon J.H., Kwon, Y.K. (2010). Characterization of antimicrobial resistance of recent Salmonella enterica serovar Gallinarum isolates from chickens in South Korea. Avian Pathology, 39: 201-205.
  13. Kar, D., Bandyopadhyay, S., Bhattacharyya, D., Samanta, I., Mahanti, A., Nanda, P.K., Mondal, B., et al. (2015). Molecular and phylogenetic characterization of multidrug resistant extended spectrum beta-lactamase producing Esherichia coli isolated from poultry and cattle in Odisha, India. Infection, Genetics and Evolution, 29: 82-90.
  14. Kaushik, P., Anjay, Kumari, S., Bharti,S.K., Dayal, S. (2014). Isolation and prevalence of Salmonella from chicken meat and cattle milk collected from local markets of Patna, India. Veterinary World, 7: 62-65.
  15. Kim, T.E., Jeong, Y.W., Cho, S.H., Kim, S.J., Kwon, H.J. (2007). Chronological study of antibiotic resistances and their relevant genes in Korean avian pathogenic Esherichia coli isolates. Journal of Clinical Microbiology, 45: 3309-3315.
  16. Klein, N.C. and Cunha, B.A. (1995). Third-generation cephalosporins. Medical Clinics of North America, 79: 705-719.
  17. Levesque, C., Piche, L., Larose, C., Roy, P.H. (1995). PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrobial Agents and Chemotherapy, 39: 185-191.
  18. Marchant, M., Vinue, L., Torres, C., Moreno, M.A. (2013). Change of integrons over time in Esherichia coli isolates recovered from healthy pigs and chickens. Veterinary Microbiology, 163 (1-2): 124-132.
  19. Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas M.E., Giske, C.G., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18: 268-281.
  20. Mohamadi, E., Alizade, H., Askari, N., Salehi, M., Porjafarian, M., Ghanbarpour, R. (2015). Antibiotic resistance profile in relation to phylogenetic background in Escherichia coli isolated from fecal samples of healthy ostrich. International Journal of Enteric Pathogens, 3: e25366.
  21. Nelson, M.L. and Levy S.B. (2011). The history of the tetracyclines. Annals of New York Academy of Sciences, 1241: 17-32.
  22. Oosterik, L.H., Peeters, L., Muruku, I., Goddeeris, B.M., Butaye, P. (2014). Susceptibility of avian pathogenic Esherichia coli from laying hens in Belgium to antibiotics and disinfectants and integron prevalence. Avian Diseases, 58(2): 271-278.
  23. Piccirillo, A., Giovanardi, G., Dotto, G., Grilli, C., Montesissa, C., Boldrin, C., et al. (2014). Antimicrobial resistance and class 1 and 2 integrons in Esherichia coli from meat turkeys in Northern Italy. Avian Pathology, 14: 396-405. 
  24. Skurnik, D., Menach, A.L., Zurakowski, D., Mazel, D., Courvalin, P., Denamur, E., Andremont, A., Ruimy, R. (2005). Integron-    associated antibiotic resistance and phylogenetic grouping of Escherichia coli isolates from healthy subjects free of recent antibiotic exposure. Antimicrobial Agents and Chemotherapy, 49: 3062-3065.
  25. Suzuki, M., Yamada, K., Nagao, M., Aoki, E., Matsumoto, M., Hirayama,T., Yamamoto, H., et al. (2011). Antimicrobial ointments and methicillin-resistant Staphylococcus aureus USA300. Emerging Infectious Diseases, 17: 1917-1920.
  26. White, P.A., Mciver, C.J., Rawlinson, W.D. (2001). Integrons and gene cassettes in the Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 45(9): 2658-2661.
  27. Wright, G.D. (2010). Antibiotic resistance in the environment: A link to the clinic? Current Opinions in Microbiology, 13: 589–594.
  28. Yang, H., Chen, S., White, D.G., Zhao, S., McDermott, P., Walker, R., Meng, J. (2004). Characterization of multiple-antimicrobial-    resistant Escherichia coli isolates from diseased chickens and swine in China. Journal of Clinical Microbiology, 42: 3483-    3489. 
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Indian Journal of Animal Research
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    Research Article

    volume 53 issue 7 (july 2019) : 918-925,   Doi: 10.18805/ijar.B-3602

    Risk factors for antimicrobial resistance in Escherichia coli isolates from poultry in Haryana

    S
    S. Kumar
    R
    R. Gupta
    1Department of Veterinary Public Health and Epidemiology, College of Veterinary Sciences, Lala Lajpat Rai University of Veterinary and Animal Sciences, Hisar-125 004, Haryana, India.
    Cite article:- Kumar S., Gupta R. (2019). Risk factors for antimicrobial resistance in Escherichia coli isolates from poultry in Haryana. Indian Journal of Animal Research. 53(7): 918-925. doi: 10.18805/ijar.B-3602.

    ABSTRACT

    Colibacillosis is a disease of severe economic significance to all poultry producers worldwide, characterized by a diverse array of lesions. Due to enormous exploitation of antibiotics in broilers, an increased number of resistant bacterial strains have developed in recent years. 106 E. coli strains were collected from broilers suffering from colibacillosis. The resistance to different classes of antimicrobials was determined. The presence of integrons was determined by Polymerase Chain Reaction (PCR). All the statistical analyses were carried out using STATA™. All the isolates were multidrug resistance (MDR), i.e. resistant to at least one agent in three or more antimicrobial categories. 37 (34.90%) isolates were found positive for Class 1 integrons. There was significant difference in carriage of integrons in different phylogentic groups, p=0.001, however, there was no difference among different serotypes for carriage of integrons. Significant difference was observed for resistance towards co-trimoxazole (p=0.002), piperacillin (p=0.034) and ciprofloxacin (p=0.046) in Class 1 integron carrying isolates and Class 1 integron negative isolates. Significant difference was observed for resistance towards ceftriaxone (p=0.004) and cefotaxime (p=0.027) in relation to phylogenetic groups. Also, significant difference was observed among different serotypes for resistance towards co-trimoxazole (p=0.001), gentamicin (p=0.005) and kanamycin (p=0.041).

    REFERENCES

    1. Ahmed, A.M., Shimamoto, T., Shimamoto, T. (2013). Molecular characterization of multidrug-resistant avian pathogenic Escherichia coli isolated from septicemic broilers. International Journal of Medical Microbiology , 303: 475-483.
    2. Bass, L., Liebert, C.A., Lee, M.D., Saummers, A.O., White, D.G., Thayer, S.G., Maurer, J.J. (1999). Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance in avian Esherichia coli. Antimicrobial Agents and Chemotherapy, 43: 2925–2929.
    3. Bauer, A.W., Kirby, W.M., Sherris, J.C., Turck, M. (1966). Antibiotic susceptibility testing by standardized single disk method. American Journal of Clinical Pathology, 45: 493-496.
    4. Butaye, P., Devriese, L.A., Haesebrouck, F. (2003). Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clinical Microbiology Reviews, 16: 175-188.
    5. Clermont, O., Bonacorsi, S., Bingen, E. (2000). Rapid and simple determination of the Esherichia coli phylogenetic group. Applied and Environmental Microbiology, 66: 4555–4558.
    6. Delannoy, S., Beutin, L., Mariani-Kurkdjian, P., Fleiss, A., Bonacorsi, S., Fach, P. (2017). The Escherichia coli serogroup O1 and O2 lipopolysaccharides are encoded by multiple O-antigen gene clusters. Frontiers in Cellular and Infection Microbiology, 7: 30.
    7. Edwards, R. and Ewing, W.N. (1972). Identification of Enterobacteriaceae. 3rd ed., Burgess Publishing Co., Minnesota.
    8. Fabrega, A., Madurga, S., Giralt, E., Vila, J. (2009). Mechanism of action of and resistance to quinolones. Microbial Biotechnology, 2: 40-61.
    9. Giufre, M., Graziani, C., Accogli, M., Luzzi, I., Busani, L., Cerquetti, M. (2012). Escherichia coli of human and avian origin: detection of clonal groups associated with fluoroquinolone and multidrug resistance in Italy. Journal of Antimicrobial Chemotherapy, 67: 860-867.
    10. Jakobsen, L., Spangholm, D.J., Pedersen, K., Jensen, L.B., Emborg, H.D., Agerso, Y., et al. (2010). Broiler chickens, broiler chicken meat, pigs and pork as sources of ExPEC related virulence genes and resistance in Esherichia coli isolates from community dwelling humans and UTI patients. International Journal of Food Microbiology, 142: 264–272.
    11. Johnson, J.R., Gajewski, A., Lesse, A.J., Russo, T.A. (2003). Extraintestinal pathogenic Escherichia coli as a cause of invasive nonurinary infections. Journal of Clinical Microbiology, 41: 5798–5802.
    12. Kang, M.S., Kim, A., Jung, B.Y., Her, M., Jeong, W., Cho, Y.M., Oh, J.Y., Lee, Y.J, Kwon J.H., Kwon, Y.K. (2010). Characterization of antimicrobial resistance of recent Salmonella enterica serovar Gallinarum isolates from chickens in South Korea. Avian Pathology, 39: 201-205.
    13. Kar, D., Bandyopadhyay, S., Bhattacharyya, D., Samanta, I., Mahanti, A., Nanda, P.K., Mondal, B., et al. (2015). Molecular and phylogenetic characterization of multidrug resistant extended spectrum beta-lactamase producing Esherichia coli isolated from poultry and cattle in Odisha, India. Infection, Genetics and Evolution, 29: 82-90.
    14. Kaushik, P., Anjay, Kumari, S., Bharti,S.K., Dayal, S. (2014). Isolation and prevalence of Salmonella from chicken meat and cattle milk collected from local markets of Patna, India. Veterinary World, 7: 62-65.
    15. Kim, T.E., Jeong, Y.W., Cho, S.H., Kim, S.J., Kwon, H.J. (2007). Chronological study of antibiotic resistances and their relevant genes in Korean avian pathogenic Esherichia coli isolates. Journal of Clinical Microbiology, 45: 3309-3315.
    16. Klein, N.C. and Cunha, B.A. (1995). Third-generation cephalosporins. Medical Clinics of North America, 79: 705-719.
    17. Levesque, C., Piche, L., Larose, C., Roy, P.H. (1995). PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrobial Agents and Chemotherapy, 39: 185-191.
    18. Marchant, M., Vinue, L., Torres, C., Moreno, M.A. (2013). Change of integrons over time in Esherichia coli isolates recovered from healthy pigs and chickens. Veterinary Microbiology, 163 (1-2): 124-132.
    19. Magiorakos, A.P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas M.E., Giske, C.G., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18: 268-281.
    20. Mohamadi, E., Alizade, H., Askari, N., Salehi, M., Porjafarian, M., Ghanbarpour, R. (2015). Antibiotic resistance profile in relation to phylogenetic background in Escherichia coli isolated from fecal samples of healthy ostrich. International Journal of Enteric Pathogens, 3: e25366.
    21. Nelson, M.L. and Levy S.B. (2011). The history of the tetracyclines. Annals of New York Academy of Sciences, 1241: 17-32.
    22. Oosterik, L.H., Peeters, L., Muruku, I., Goddeeris, B.M., Butaye, P. (2014). Susceptibility of avian pathogenic Esherichia coli from laying hens in Belgium to antibiotics and disinfectants and integron prevalence. Avian Diseases, 58(2): 271-278.
    23. Piccirillo, A., Giovanardi, G., Dotto, G., Grilli, C., Montesissa, C., Boldrin, C., et al. (2014). Antimicrobial resistance and class 1 and 2 integrons in Esherichia coli from meat turkeys in Northern Italy. Avian Pathology, 14: 396-405. 
    24. Skurnik, D., Menach, A.L., Zurakowski, D., Mazel, D., Courvalin, P., Denamur, E., Andremont, A., Ruimy, R. (2005). Integron-    associated antibiotic resistance and phylogenetic grouping of Escherichia coli isolates from healthy subjects free of recent antibiotic exposure. Antimicrobial Agents and Chemotherapy, 49: 3062-3065.
    25. Suzuki, M., Yamada, K., Nagao, M., Aoki, E., Matsumoto, M., Hirayama,T., Yamamoto, H., et al. (2011). Antimicrobial ointments and methicillin-resistant Staphylococcus aureus USA300. Emerging Infectious Diseases, 17: 1917-1920.
    26. White, P.A., Mciver, C.J., Rawlinson, W.D. (2001). Integrons and gene cassettes in the Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 45(9): 2658-2661.
    27. Wright, G.D. (2010). Antibiotic resistance in the environment: A link to the clinic? Current Opinions in Microbiology, 13: 589–594.
    28. Yang, H., Chen, S., White, D.G., Zhao, S., McDermott, P., Walker, R., Meng, J. (2004). Characterization of multiple-antimicrobial-    resistant Escherichia coli isolates from diseased chickens and swine in China. Journal of Clinical Microbiology, 42: 3483-    3489. 
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