Open Access
Research (Published online: 01-10-2016)
7. Prevalence and multidrug resistance pattern of Salmonella isolated from resident wild birds of Bangladesh
Abdullah Al Faruq, Mohammad Mahmudul Hassan, Mohammad Mejbah Uddin, Mohammad Lutfur Rahman, Tofazzal Md. Rakib, Mahabub Alam and Ariful Islam
International Journal of One Health, 2: 35-41

Abdullah Al Faruq: Department of Anatomy and Histology, Faculty of Veterinary Medicine, Chittagong Veterinary and Animal Sciences University, Chittagong 4225, Bangladesh.
Mohammad Mahmudul Hassan: Department of Physiology, Biochemistry and Pharmacology, Faculty of Veterinary Medicine, Chittagong Veterinary and Animal Sciences University, Chittagong 4225, Bangladesh.
Mohammad Mejbah Uddin: Department of Anatomy and Histology, Faculty of Veterinary Medicine, Chittagong Veterinary and Animal Sciences University, Chittagong 4225, Bangladesh.
Mohammad Lutfur Rahman: Department of Anatomy and Histology, Faculty of Veterinary Medicine, Chittagong Veterinary and Animal Sciences University, Chittagong 4225, Bangladesh.
Tofazzal Md. Rakib: Department of Pathology and Parasitology, Faculty of Veterinary Medicine, Chittagong Veterinary and Animal Sciences University, Chittagong 4225, Bangladesh.
Mahabub Alam: Department of Animal Science and Nutrition, Faculty of Veterinary Medicine, Chittagong Veterinary and Animal Sciences University, Chittagong 4225, Bangladesh.
Ariful Islam: EcoHealth Alliance, New York, NY, USA; Institute of Epidemiology, Disease Control and Research (IEDCR), Mohakhali 1212, Bangladesh.

doi: 10.14202/IJOH.2016.35-41

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Article history: Received: 05-08-2016, Accepted: 19-09-2016, Published online: 01-10-2016

Corresponding author: Mohammad Mahmudul Hassan


Citation: Faruq AA, Hassan MM, Uddin MM, Rahman ML, Rakib TM, Alam M, Islam A. Prevalence and multidrug resistance pattern of Salmonella isolated from resident wild birds of Bangladesh. Int J One Health 2016;2:35-41.

Aim: Salmonellosis is one of the most common zoonotic diseases, and the presence of antimicrobial resistant Salmonella in wild birds is global public health threat. Throughout the last decades, multidrug resistance of Salmonella spp. has increased, particularly in developing countries. Therefore, a cross-sectional study was conducted to investigate the prevalence of Salmonella spp. and antimicrobial resistance pattern against Salmonella spp. from two species of resident wild birds namely house crow (Corvus splendens) and Asian pied starling (Gracupica contra).

Materials and Methods: Samples were collected from cloacal swabs of house crows and Asian pied starling for isolating Salmonella spp. (bacteriological culture methods) followed by antimicrobial susceptibility testing (disk diffusion method) against Salmonella spp. isolates during March to December 2014.

Results: The prevalence of Salmonella in Asian pied starling and house crows were 67% and 65%, respectively. Within the category of samples from different species, the variation in prevalence was not varied significantly (p>0.05). Isolated Salmonella spp. was tested for resistance to six different antimicrobial agents. Among six antimicrobial tested, 100% resistance were found to penicillin, oxacillin, and clindamycin followed by erythromycin (50-93%), kanamycin (7-20%), and cephalothin (30-67%) from both species of birds. Kanamycin remained sensitive in (70-73%), cephalothin (26-70%), and erythromycin appeared to be (0-30%) sensitive against Salmonella spp. isolates. Isolated Salmonella spp. was multidrug resistant up to three of the six antimicrobials tested.

Conclusion: It can be said that the rational use of antimicrobials needs to be adopted in the treatment of disease for livestock, poultry, and human of Bangladesh to limit the emergence of drug resistance to Salmonella spp.

Keywords: antimicrobial, prevalence, resistance, resident wild birds, Salmonella.


1. Akkina JE, Hogue AT, Angulo FJ, Johnson R, Petersen KE, Saini PK, et al. Epidemiologic aspects, control, and importance of multiple-drug resistant Salmonella Typhimurium DT104 in the United States. J Am Vet Med Assoc 1999;214:790-8. [PubMed]

2. Steve Yan S, Pendrak ML, Abela-Ridder B, Punderson JW, Fedorko DP, Foley SL. An overview of Salmonella typing: Public health perspectives. Clin Appl Immunol Rev 2004;4:189-204. [Crossref]

3. Uddin M, Ahmed S, Hassan M, Khan S, Mamun M. Prevalence of poultry diseases at Narsingdi, Bangladesh. Int J BioRes 2010;1:09-13.

4. Mahmud MS, Bari ML, Hossain MA. Prevalence of Salmonella serovars and antimicrobial resistance profiles in poultry of Savar area, Bangladesh. Foodborne Pathog Dis 2011;8:1111-8. [Crossref] [PubMed]

5. Rahman M, Samad M, Rahman M, Kabir S. Bacterio-pathological studies on salmonellosis, colibacillosis and pasteurellosis in natural and experimental infections in chickens. Bangladesh J Vet Med 2004;2:1-8.

6. White DG, Piddock LJ, Maurer JJ, Zhao S, Ricci V, Thayer SG. Characterization of fluoroquinolone resistance among veterinary isolates of avian Escherichia coli. Antimicrob Agents Chemother 2000;44:2897-9. [Crossref] [PubMed] [PMC]

7. Balague C, Vescovi EG. Activation of multiple antibiotic resistance in uropathogenic Escherichia coli strains by aryloxoalcanoic acid compounds. Antimicrob Agents Chemother 2001;45:1815-22. [Crossref] [PubMed] [PMC]

8. Sattar S, Hassan MM, Islam S, Alam M, Faruk M, Chowdhury S, et al. Antibiotic residues in broiler and layer meat in Chittagong District of Bangladesh. Vet World 2014;7:738-43. [Crossref]

9. Hassan MM, Amin KB, Ahaduzzaman M, Alam M, Al Faruk MS, Uddin I. Antimicrobial resistance pattern against E. coli and Salmonella in layer poultry. Res J Vet Pract 2014;2:30-5. [Crossref]

10. Chowdhury S, Hassan MM, Alam M, Sattar S, Bari MS, Saifuddin AK, et al. Antibiotic residues in milk and eggs of commercial and local farms at Chittagong, Bangladesh. Vet World 2015;8:467-71. [Crossref] [PubMed] [PMC]

11. Hassan MM, Ahaduzzaman M, Alam M, Bari MS, Amin KA, Faruq AA. Antimicrobial resistance pattern against E. coli and Salmonella spp. in environmental effluents. Int J Nat Sci 2015;5:52-8. [Crossref]

12. Mahmud T, Hassan MM, Alam M, Khan MM, Bari MS, Islam A. Prevalence and multidrug-resistant pattern of Salmonella from the eggs and egg-storing trays of retail markets of Bangladesh. Int J One Health 2016;2:7-11. [Crossref]

13. Ahaduzzaman M, Hassan MM, Alam M, Islam S, Uddin I. Antimicrobial resistance pattern against Staphylococcus aureus in environmental effluents. Res J Vet Pract 2014;2:13-6. [Crossref]

14. Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, et al. The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis 2013;13:155-65. [Crossref]

15. Tacao M, Correia A, Henriques I. Resistance to broad-spectrum antibiotics in aquatic systems: Anthropogenic activities modulate the dissemination of bla(CTX-M)-like genes. Appl Environ Microbiol 2012;78:4134-40. [Crossref] [PubMed] [PMC]

16. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: Antibiotic resistance genes in natural environments. Nat Rev Microbiol 2010;8:251-9. [Crossref] [PubMed]

17. Reed KD, Meece JK, Henkel JS, Shukla SK. Birds, migration and emerging zoonoses: West nile virus, lyme disease, influenza A and enteropathogens. Clin Med Res 2003;1:5-12. [Crossref] [PubMed] [PMC]

18. CLSI. Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth Informational Suppliment. Vol. 26, 27. Wayne, PA: CLSI; 2007.

19. Wikler MA. Performance Standards for Antimicrobial Susceptibility Testing: Seventeenth Informational Supplement. Wayne, PA: Clinical and Laboratory Standards Institute; 2007.

20. Asagi M, Oka C, Sato G. Isolation of Salmonella Typhimurium var. Copenhagen from crows in the city of Otaru. Nihon Juigaku Zasshi 1976;38:521-2. [Crossref] [PubMed]

21. Snoeyenbos GH, Morin EW, Wetherbee DK. Naturally occurrine Salmonella in "blackbirds" and gulls. Avian Dis 1967;11:642-6. [Crossref] [PubMed]

22. Morishita TY, Aye PP, Ley EC, Harr BS. Survey of pathogens and blood parasites in free-living passerines. Avian Dis 1999;43:549-52. [Crossref] [PubMed]

23. Carlson JC, Franklin AB, Hyatt DR, Pettit SE, Linz GM. The role of starlings in the spread of Salmonella within concentrated animal feeding operations. J Appl Ecol 2011;48:479-86. [Crossref]

24. Zhao S, McDermott PF, White DG, Qaiyumi S, Friedman SL, Abbott JW, et al. Characterization of multidrug resistant Salmonella recovered from diseased animals. Vet Microbiol 2007;123:122-32. [Crossref] [PubMed]

25. Oldfield EC. The road to resistance: Antibiotics as growth promoters for animals. Am J Gastroenterol 2003;98:499. [PubMed]

26. White DG, Zhao S, Sudler R, Ayers S, Friedman S, Chen S, et al. The isolation of antibiotic-resistant Salmonella from retail ground meats. N Engl J Med 2001;345:1147-54. [Crossref] [PubMed]

27. Fluit AC. Towards more virulent and antibiotic-resistant Salmonella? FEMS Immunol Med Microbiol 2005;43:1-11. [Crossref] [PubMed]

28. Prakash B, Krishnappa G, Muniyappa L, Kumar BS. Epidemiological characterization of avian Salmonella enterica serovar infections in India. Int J Poult Sci 2005;4:388-95. [Crossref]

29. Begum K, Reza TA, Haque M, Hossain A, Hassan FK, Hasan SN, et al. Isolation, identification and antibiotic resistance pattern of Salmonella spp. from chicken eggs, intestines and environmental samples. Bangladesh Pharm J 2010;13:23-7.

30. Ahmed M, Rahman M, Mahbub K, Wahiduzzaman M. Characterization of antibiotic resistant Salmonella spp isolated from chicken eggs of Dhaka city. J Sci Res 2010;3:191. [Crossref]

31. Suresh T, Hatha AA, Sreenivasan D, Sangeetha N, Lashmanaperumalsamy P. Prevalence and antimicrobial resistance of Salmonella enteritidis and other salmonellas in the eggs and egg-storing trays from retail markets of Coimbatore, South India. Food Microbiol 2006;23:294-9. [Crossref] [PubMed]

32. McHugh GL, Moellering RC, Hopkins CC, Swartz MN. Salmonella Typhimurium resistant to silver nitrate, chloramphenicol, and ampicillin. Lancet 1975;1:235-40. [Crossref]

33. Roantree RJ, Kuo TT, MacPhee DG. The effect of defined lipopolysaccharide core defects upon antibiotic resistances of Salmonella Typhimurium. J Gen Microbiol 1977;103:223-34. [Crossref] [PubMed]

34. Fu KP, Neu HC. Piperacillin, a new penicillin active against many bacteria resistant to other penicillins. Antimicrob Agents Chemother 1978;13:358-67. [Crossref]

35. Guzman-Blanco M, Casellas JM, Sader HS. Bacterial resistance to antimicrobial agents in Latin America. The giant is awakening. Infect Dis Clin North Am 2000;14:67-81, viii. [Crossref]

36. Nishino K, Nikaido E, Yamaguchi A. Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar Typhimurium. J Bacteriol 2007;189:9066-75. [Crossref] [PubMed] [PMC]

37. Jacobs-Reitsma WF, Koenraad PM, Bolder NM, Mulder RW. In vitro susceptibility of Campylobacter and Salmonella isolates from broilers to quinolones, ampicillin, tetracycline, and erythromycin. Vet Q 1994;16:206-8. [Crossref] [PubMed]

38. Cui S, Ge B, Zheng J, Meng J. Prevalence and antimicrobial resistance of Campylobacter spp. and Salmonella serovars in organic chickens from Maryland retail stores. Appl Environ Microbiol 2005;71:4108-11. [Crossref] [PubMed] [PMC]

39. Groisman EA, Parra-Lopez C, Salcedo M, Lipps CJ, Heffron F. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci U S A 1992;89:11939-43. [Crossref] [PubMed] [PMC]

40. Davis MA, Hancock DD, Besser TE, Rice DH, Gay JM, Gay C, et al. Changes in antimicrobial resistance among Salmonella enterica serovar Typhimurium isolates from humans and cattle in the Northwestern United States, 1982-1997. Emerg Infect Dis 1999;5:802-6. [Crossref] [PubMed] [PMC]

41. Besser TE, Goldoft M, Pritchett LC, Khakhria R, Hancock DD, Rice DH, et al. Multiresistant Salmonella Typhimurium DT104 infections of humans and domestic animals in the Pacific Northwest of the United States. Epidemiol Infect 2000;124:193-200. [Crossref] [PubMed] [PMC]

42. Carattoli A. Plasmid-mediated antimicrobial resistance in Salmonella enterica. Curr Issues Mol Biol 2003;5:113-22. [PubMed]

43. Helmuth R. Antibiotic resistance in Salmonella. Salmonella in Domestic Animals. New York: CABI Publishing; 2000. p. 89-106. [Crossref]

44. Ang JY, Ezike E, Asmar BI. Antibacterial resistance. Indian J Pediatr 2004;71:229-39. [Crossref] [PubMed]

45. Keelara S, Scott HM, Morrow WM, Gebreyes WA, Correa M, Nayak R, et al. Longitudinal study of distributions of similar antimicrobial-resistant Salmonella serovars in pigs and their environment in two distinct swine production systems. Appl Environ Microbiol 2013;79:5167-78. [Crossref] [PubMed] [PMC]

46. Maragkoudakis PA, Mountzouris KC, Psyrras D, Cremonese S, Fischer J, Cantor MD, et al. Functional properties of novel protective lactic acid bacteria and application in raw chicken meat against Listeria monocytogenes and Salmonella enteritidis. Int J Food Microbiol 2009;130:219-26. [Crossref] [PubMed]