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Antibiotic resistance pattern among the Salmonella isolated from human, animal and meat in India

Abstract

The present study was conducted to study the antibiotic resistance pattern among nontyphoidal Salmonella isolated from human, animal and meat. A total of 37 Salmonella strains isolated from clinical cases (human and animal) and meat during 2008–2009 belonging to 12 serovars were screened for their antimicrobial resistance pattern using 25 antimicrobial agents falling under 12 different antibiotic classes. All the Salmonella isolates tested showed multiple drug resistance varying from 5.40% to 100% with 16 of the 25 antibiotics tested. None of the isolates were sensitive to erythromycin and metronidazole. Resistance was also observed against clindamycin (94.59%), ampicillin (86.49%), co-trimoxazole (48.65%), colistin (45.94%), nalidixic acid (35.10%), amoxyclave (18.90%), cephalexin, meropenem, tobramycin, nitrofurantoin, tetracycline, amoxicillin (8.10% each), sparfloxacin and streptomycin (5.40% each). Isolates from clinical cases of animals were resistant to as many as 16 antibiotics, whereas isolates from human clinical cases and meat were resistant to 9 and 14 antibiotics, respectively. Overall, 19 resistotypes were recorded. Analysis of multiple antibiotic resistance index (MARI) indicated that clinical isolates from animals had higher MARI (0.25) as compared to isolates from food (0.22) and human (0.21). Among the different serotypes studied for antibiogram, Paratyhi B isolates, showed resistance to three to 13 antibiotics, whereas Typhimurium strains were resistant to four to seven antibiotics. Widespread multidrug resistance among the isolates from human, animal and meat was observed. Some of the uncommon serotypes exhibited higher resistance rate. Considerable changes in the resistance pattern were also noted. An interesting finding was the reemergence of sensitivity to some of the old antibiotics (chloromphenicol, tetracycline).

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References

  • Achla, P., Grover, S.S., Bhatia, R. and Khare, S., 2005. Sensitivity index of antimicrobial agents as a simple solution for multidrug resistance in Salmonella Typhi. Indian Journal of Medical Research, 121, 185–193.

    PubMed  CAS  Google Scholar 

  • Agarwal, R.K., Bhilegaonkar, K.N., Singh, D.K., Kumar, Ashok and Rathore, R.S., 2003. Laboratory manual for the isolation and identification of foodborne pathogen. (Indian Veterinary Research Institute, Bareilly).

    Google Scholar 

  • Agarwal, R.K., Kapoor, K.N., Verma, J.C. and Bachhil, V.N., Singh, B.R., Kumar, A., Sachan, N., Singh, D.K. and Malik, S.V.S., 1999. First report and some properties of Salmonella Stockholm in India, Indian Journal of Comparative Microbiology Immunology and Infectious Diseases, 20, 50–52.

    Google Scholar 

  • Antony, B., Scaria, B., Dias, M. and Pinto, H., 2009. Salmonella wien from gastroenteritis cases encountered in Mangalore, India: A report of 10 cases and review of the literature. Indian Journal of Medical Science, 63, 195–197.

    Article  Google Scholar 

  • Ashtiani, M.T., Monajemzadeh, M., Kashi, L., 2009. Trends in antimicrobial resistance of fecal Shigella and Salmonella isolates in Tehran, Iran. Indian Journal of Pathology and Microbiology, 52, 52–55.

    Article  Google Scholar 

  • Boonmar, S., Markvichitr, K., Chaunchom, S., Chanda, C., Bangtrakulnonth, A., Pornrunangwong, S., Yamamoto, S., Suzuki, D., Kozawa, K., Kimura, H. and Morita Y., (2008). Salmonella prevalence in slaughtered buffaloes and pigs and antimicrobial susceptibility of isolates in Vientiane, Lao People's Democratic Republic. Journal of Veterinary Medical Science, 70, 1345–1348.

    PubMed  Article  Google Scholar 

  • Braoudaki, M. and Hilton, A.C., 2005. Mechanisms of resistance in Salmonella enterica adapted to erythromycin, benzalkonium chloride and triclosan. International Journal of Antimicrobial Agents, 25, 31–37.

    PubMed  Article  CAS  Google Scholar 

  • Cabrera, R., Ruiz, J., Marco, F., Oliveira, I., Arroyo, M., Aladueña, A., Usera, M.A., De Anta, M.T.J., Gascón, J. and Vila, J., 2004. Mechanism of resistance to several antimicrobial agents in Salmonella clinical isolates causing traveler's diarrhea. Antimicrobial Agents and Chemotherapy, 48, 3934–3939.

    PubMed  Article  CAS  Google Scholar 

  • Cailhol, J., Lailler, R., Bouvet, P., Vieille, S.L., Gauchard, F., Sanders, P. and Brisabois, A., 2005. Trends in antimicrobial resistance phenotypes in non-typhoid Salmonellae from human and poultry origins in France. Epidemiology and Infection, 134, 171–178.

    Article  Google Scholar 

  • Capoor, M.R., Nair, D., Posti, J., Singhal, S., Deb, M., Aggarwal, P. and Pillai, P., 2009. Minimum inhibitory concentration of carbapenems and tigecycline against Salmonella spp. Journal of Medical Microbiology, 58, 337–341.

    PubMed  Article  CAS  Google Scholar 

  • Cardoso, M.O., Ribeiro, A.R., dos Santos, L.R., Pilotto, F., Moraes, H.L.S., Salle, C. T.P., Rocha, S.L. Silveira and Nascimento, V.P., 2006. Antibiotic resistance in Salmonella Enteritidis isolated from broiler carcasses. Brazilian Journal of Microbiology, 37, 368–371.

    Article  Google Scholar 

  • Dahal, N., 2007. Prevalence and antimicrobial resistance of Salmonella in imported chicken carcasses in Bhutan, (Unpublished MSc Thesis, Chiang mai university and Freie universität, Berlin).

    Google Scholar 

  • Ekwenye, U.N. and Kazi, E., 2007. Investigation of plasmid DNA and antibiotic resistance in some pathogenic organisms. African Journal of Biotechnology, 6, 877–880.

    CAS  Google Scholar 

  • Egorova, S., Timinouni, M., Demartin, M., Granier, S.A., Whichard, J.M. Sangal, V., Fabre, L., Delauné, A., Pardos, M., Millemann, Y., Espié, E., Achtman, M., Grimont, P.A.D. and Weill, F., 2008. Ceftriaxone-resistant Salmonella enterica serotype Newport, France. Emerging Infectious Disease, 14, 954–957.

    Article  CAS  Google Scholar 

  • Farmer, J.J. III., 1995. Enterobacteriaceae: introduction and identification. In: Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C., Yolken, R.H. (eds), Manual of clinical microbiology, (American Society for Microbiology Press. Washington DC) 438–449.

    Google Scholar 

  • Guibourdenche, M., Roggentin, P., Mikoleit, M., Fields, P.I., Bockemu¨ J., Grimont, P. A.D. Weill, F-Xavier., 2010. Supplement 2003e2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Research in Microbiology, 161, 26–29.

    PubMed  Article  Google Scholar 

  • Hall, R.M. 2010. Salmonella genomic islands and antibiotic resistance in Salmonella enterica. Future Microbiology, 5, 1525–1538.

    PubMed  Article  CAS  Google Scholar 

  • Harakeh, S., Yassine, H., Gharios, M., Barbour, E., Hajjar, S., El-fadel, M., Toufeili, I. and Tannous, R., 2005. Isolation, molecular characterization and antimicrobial resistance patterns of Salmonella and Escherichia coli isolates from meat-based fast food in Lebanon. Science of the Total Environment, 341, 33–44.

    PubMed  Article  CAS  Google Scholar 

  • Hoelzer, K., Moreno Switt, A.I. and Wiedmann M., 2011. Animal contact as a source of human non-typhoidal salmonellosis. Veterinary Research, 42, 34.

    PubMed  Article  Google Scholar 

  • Hof, H., Stroder, J., Buisson, J and Royer, R., 1986. Effect of different nitroheterocyclic compounds on aerobic, microaerophilic, and anaerobic bacteria. Antimicrobial Agents and Chemotherapy, 30, 679–683.

    PubMed  CAS  Google Scholar 

  • Hopkins, K.L., Day, M. and Threlfall, E.J., 2008. Plasmid-mediated quinolone resistance in Salmonella enterica, United Kingdom. Emerging Infectious Diseases, 14, 340–342.

    PubMed  Article  Google Scholar 

  • Hung, P.H., Chiu, Y.L. and Hsueh, P.R., 2007. Gas-forming splenic abscess due to Salmonella enterica serotype Enteritidis in a chronically hemodialyzed patient. Journal of Microbiology, Immunology and Infection, 40, 276–278.

    Google Scholar 

  • Kikuvi, G.M., Ombui, J.N. and Mitema, E.S., 2010. Serotypes and antimicrobial resistance profiles of Salmonella isolates from pigs at slaughter in Kenya. Journal of Infections in Developing Countries, 4, 243–248.

    CAS  Google Scholar 

  • Khan, M.F.R., Rahman, M.B., Khan, M.S.R. and Nazir, M.N.H., 2005. Antibiogram and plasmid profile analysis of isolated poultry Salmonella of Bangladesh. Pakistan Journal of Biological Sciences, 8, 1614–1619.

    Article  CAS  Google Scholar 

  • Kulkarni, R.D., Ajantha, G.S, Shubhada, C. and Jain P., 2009. Isolation of Salmonella enterica serotype Isangi from a suspected case of enteric encephalopathy. Indian Journal of Medical Microbiology, 27, 65–66.

    PubMed  CAS  Google Scholar 

  • Kumar, K., 2009. PCR based detection of zoonotic Salmonella from foods. (Unpublished PhD Thesis, Hemwati Nandan Bahuguna Garhwal Central University, Srinagar, Uttrakhand, India).

    Google Scholar 

  • Lakshmi, V., Ashok, R., Susmita, J. and Shailaja, V.V., 2006. Changing trends in the antibiograms of Salmonella isolates at a tertiary care hospital in Hyderabad. Indian Journal of Medical Microbiology, 24, 45–48.

    PubMed  Article  CAS  Google Scholar 

  • Levings, R.S., Lightfoot, D., Hall, R.M. and Djordjevic, S.P., 2006. Aquariums as reservoirs for multidrug-resistant Salmonella Paratyphi B, Emerging Infectious Diseases, 12, 507–510.

    PubMed  Article  CAS  Google Scholar 

  • Maharjan, M., Joshi, V., Joshi, D.D. and Manandhar, P., 2006. Prevalence of Salmonella species in various raw meat samples of a local market in Kathmandu. Annals of the New York Academy of Science, 1081, 249–256.

    Article  Google Scholar 

  • Mandal, S., Mandal, M.D. and Pal, N.K., 2004. Reduced minimum inhibitory concentration of chloramphenicol for Salmonella enterica serovar Typhi. Indian Journal of Medical Sciences, 58, 16–23.

    PubMed  CAS  Google Scholar 

  • Maripandi, A. and Al-Salamah, A.A., 2010. Multiple-antibiotic resistance and plasmid profiles of Salmonella Enteritidis isolated from retail chicken meats. American Journal of Food Technology, 5, 260–268.

    Article  CAS  Google Scholar 

  • Mohanty, S., Renuka, K., Sood, S., Das, B.K. and Kapil, A., 2006, Antibiogram pattern and seasonality of Salmonella serotypes in a north Indian tertiary care hospital. Epidemiology and Infection, 134, 961–966.

    PubMed  Article  CAS  Google Scholar 

  • Murugkar, H.V., Rahman, H., Kumar, A. and Bhattacharyya, D., 2004. Isolation, phage typing and antibiogram of Salmonella from man and animals in northeastern India. Indian Journal of Medical Research, 122, 237–242.

    Google Scholar 

  • Nikaido, H., 2009. Multidrug resistance in bacteria. Annual Review of Biochemistry, 78, 119–146.

    PubMed  Article  CAS  Google Scholar 

  • Onyango, M.D., Ghebremedhin, B., Waindi, E.N., Kakai, R., Rabsch, W., Tietze, E., König, W. and König, B., 2009. Phenotypic and genotypic analysis of clinical isolates Salmonella serovar Typhimurium in western Kenya. Journal of Infections in Developing countries, 3, 685–694.

    CAS  Google Scholar 

  • Paterson, D.L., 2006. Resistance in Gram-negative bacteria. Enterobacteriaceae, American Journal of Medicine. 119, S20-S28.

    Article  CAS  Google Scholar 

  • Prakash, B., Krishnappa, G., Muniyappa L. and Kumar, B.S., 2005. Epidemiological characterization of avian Salmonella enterica serovar infections in India, International Journal of Poultry Science, 4, 388–395.

    Article  Google Scholar 

  • Prescot, J.F. and Baggot, J.D., 1993. Fluoroquinolones, In: J. F. Prescot and J. D. Baggot (eds), Antimicrobial therapy. In: Veterinary Medicine. 2nd Edn. (Iowa State University Press. Ames) 252–261.

  • Sirichote, P., Bangtrakulnonth, A., Tianmanee, K., Unahalekhaka, A., Oulai, A., Chittaphithakchai, P., Kheowrod, W., Hendriksen, R.S., 2010. Serotypes and antimicrobial resistance of Salmonella enterica spp in central Thailand, 2001–2006. Southeast Asian Journal of Tropical Medicine and Public Health. 41, 1405–1415.

    PubMed  CAS  Google Scholar 

  • Shukla, I. and Khan, J.A., 2004. Re-emergence of chloranicol sensitive Salmonella enterica serotype Typhi - a preliminary report. Bionotes, 6, 50.mphe

  • Sorbera, L.A., Del Fresno, N., Castaner, R.M. and Rabasseda, X., 2002. Faropenem daloxate. Drugs of the Future, 27, 223–233.

    Article  CAS  Google Scholar 

  • Su, L-H. and Chiu, C-H., 2007. Salmonella: Clinical importance and evolution of nomenclature. Chang Gung Medicine Journal, 30, 210–219.

    Google Scholar 

  • Stevens, M.P., Humphrey, T.J. and Maskell, D.J., 2009. Molecular insights into farm animal and zoonotic Salmonella infections. Philosophical Transactions of the Royal Society B. 364, 2709–2723.

    Article  CAS  Google Scholar 

  • Tenson, T., Lovmar, M. and Ehrenberg, M., 2003 The Mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome. Journal of Molecular Biology, 330, 1005–1014.

    PubMed  Article  CAS  Google Scholar 

  • Threlfall, E.J., Clifton-Hadley, F.A., Ridley, A.M., Davies, R.H., 2002. Comparison of gyrA mutations, cyclohexane cesistance, and the presence of class I Integrons in Salmonella enterica from farm animals in England and Wales. Journal of Clinical Microbiology, 40, 1481–1486.

    PubMed  Article  Google Scholar 

  • Threlfall, E.J., Fisher, I.S.T., Berghold, C., Gerner-Smidt, P., Tschape, H., Cormican, M., Luzzi, I., Schnieder, F., Wannet, W., Machado, J. and Edwards G., 2003. Antimicrobial drug resistance in isolates of Salmonella enterica from cases of salmonellosis in humans in Europe in 2000: results of international multi-centre surveillance. Eurosurveillance, 8, 41– 45

    PubMed  CAS  Google Scholar 

  • Vila, J., Gascdn, J., Abdalla, S., Gomez, ]., Moveno, A., Covachlin, M. and Jimenez de Anta, M.T., 2006, Antimicrobial Resistance of Nontyphoidal Salmonella Isolates in Traveler's Diarrhea, Journal of Travel Medicine, 2, 45–47.

    Article  Google Scholar 

  • Vo, A.T., van Duijkeren, E., Gaastra, W. and Fluit, A.C., 2010. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS One, 5, e9440.

    PubMed  Article  Google Scholar 

  • White, D.G., Zhao, S. and Sudler, R., 2001. The isolation of antibiotic resistant Salmonella from retail ground meats. New England Journal of Medicine, 345, 1147–1154.

    PubMed  Article  CAS  Google Scholar 

  • Yu, F., Chen, Q., Yu, X., Li, Q., Ding, B., Yang, L., Chen, C., Qin, Z., Parsons, C., Zhang, X., Huang, J., Luo, Y., Wang, L. and Pan J., 2011. High prevalence of extended-spectrum beta lactamases among Salmonella enterica Typhimurium isolates from pediatric patients with diarrhea in China. PLoS One, 6, e16801.

    PubMed  Article  CAS  Google Scholar 

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Acknowledgement

The authors thank the Director, Indian Veterinary Research Institute, Izatnagar, Bareilly, India for providing facilities to carry out this work.

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Correspondence to Rajesh Kumar Agarwal.

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Singh, S., Agarwal, R.K., Tiwari, S.C. et al. Antibiotic resistance pattern among the Salmonella isolated from human, animal and meat in India. Trop Anim Health Prod 44, 665–674 (2012). https://doi.org/10.1007/s11250-011-9953-7

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  • DOI: https://doi.org/10.1007/s11250-011-9953-7

Keywords

  • Antibiogram
  • Clinical isolates
  • Resistance pattern
  • Salmonella
  • Paratyphi B
  • Typhimurium