Occurrence of Escherichia coli and Pasteurella multocida in Layer Chickens in Bangladesh with Special Reference to Colistin and Quinolone Resistance

Articles in Press

Document Type : Original Paper

Authors

1 Livestock Extension officer (LDDP), Upazilla Livestock Office and Veterinary Hospital, Lohagara- 4396, Chattogram, Bangladesh.

2 Department of Animal Nutrition, Faculty of Veterinary, Animal and Biomedical Sciences, Khulna Agricultural University, Khulna-9202, Bangladesh.

3 Veterinary Surgeon, Upazilla Livestock Office and Veterinary Hospital, Dighalia- 9220, Khulna, Bangladesh.

4 Department of Microbiology and Veterinary Public Health, Faculty of Veterinary Medicine, Chattogram Veterinary and Animal Sciences University, Chattogram, Bangladesh.

5 Department of Microbiology and Public Health, Faculty of Veterinary, Animal and Biomedical Sciences, Khulna Agricultural University, Khulna-9202

6 Department of Veterinary Microbiology, West Bengal University of Animal and Fishery Sciences, 37, K.B. Sarani, Belgachia, Kolkata, West Bengal, India.

Abstract

Pasteurella multocida and Escherichia coli are two important gram-negative bacterial pathogens causing septicemia and are responsible for high morbidity and mortality in poultry with economic losses. To investigate the occurrence of these two pathogens in layer chickens, a cross-sectional study was conducted with liver samples of affected layers (n=100) from July 2018 to November 2018. P. multocida and E. coli were isolated using conventional bacteriological methods and the isolates were confirmed by polymerase chain reaction using species-specific primers. The E. coli isolates obtained were subsequently investigated to determine their susceptibility to different antimicrobials by disc diffusion method.  The minimum inhibitory concentration (MIC) of colistin in E. coli isolates showing phenotypical resistance to colistin was detected using the broth microdilution method. PCR further characterized isolates displaying resistance to colistin and ciprofloxacin.  The occurrence of E. coli in layers was 35% (95% Confidence Interval 26.4 – 44.8%). No P. multocida was confirmed in the samples collected. All E. coli isolates showed phenotypical resistance to ampicillin, ciprofloxacin, sulfamethoxazole-trimethoprim, and tetracycline while 22.9% and 62.9% isolates displayed resistance to colistin and ciprofloxacin, respectively. All isolates were found to be multi-drug resistant. The minimum inhibitory concentration of colistin in E. coli isolates ranged from 8 to 128µg/mL, and 3 out of 8 colistin-resistant E. coli isolates harbored the mcr-1 gene. All ciprofloxacin-resistant isolates contained the gyrA gene. About 94% and 14% of isolates harbored gyrB and parC genes, respectively. The study highlights the circulation of colistin and ciprofloxacin-resistant E. coli in layers in Chattogram, Bangladesh.

Keywords

References

Bauer A, Kirby W, Sherris JC & Turck M. 1966. Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45(4_ts): 493-496.
Biswas P, Uddin G, Barua H, Roy K, Biswas D, Ahad A & Debnath N. 2006. Causes of loss of Sonali chickens on smallholder households in Bangladesh. Preventive Veterinary Medicine, 76(3-4): 185-195. DOI: 10.1016/j.prevetmed.2006.05.001
Borowiak M, Fischer J, Hammerl JA, Hendriksen RS, Szabo I & Malorny B. 2017. Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. Journal of Antimicrobial Chemotherapy, 72(12): 3317-3324. DOI: 10.1093/jac/dkx327
Boyen F, Vangroenweghe F, Butaye P, De Graef E, Castryck F, Heylen P, Vanrobaeys M & Haesebrouck F. 2010. Disk prediffusion is a reliable method for testing colistin susceptibility in porcine E. coli strains. Veterinary Microbiology, 144(3-4): 359-362. DOI: 10.1016/j.vetmic.2010.01.010
Casino P, López A, Peiró S, Terrones I, Agustí G, Terlevich D, Asensio D, Marqués AM & Piqué N. 2023. Use of Blood Powder (Ground and Irradiated) for the Manufacture of Chocolate Agar. International Journal of Molecular Sciences, 24(9): 7965. DOI: 10.3390/ijms24097965
Chen J & Griffiths M. 1998. PCR differentiation of Escherichia coli from other Gram‐negative bacteria using primers derived from the nucleotide sequences flanking the gene encoding the universal stress protein. Letters in applied microbiology, 27(6): 369-371. DOI: 10.1046/j.1472-765X.1998.00445.x
Darabpour E, Bavi AP, Motamedi H & Nejad SMS. 2011. Antibacterial activity of different parts of Peganum harmala L. growing in Iran against multi-drug resistant bacteria. EXCLI journal, 10: 252.
Elghandour M, Tan Z, Abu Hafsa S, Adegbeye M, Greiner R, Ugbogu E, Cedillo Monroy J & Salem A. 2020. Saccharomyces cerevisiae as a probiotic feed additive to non and pseudo‐ruminant feeding: a review. Journal of applied microbiology, 128(3): 658-674. DOI: 10.1111/jam.14416
Epizootics IOo. 2007. The global strategy for prevention and control of H5N1 highly pathogenic avian influenza. Food & Agriculture Org.
Ewers C, Janssen T & Wieler LH. 2003. Avian pathogenic Escherichia coli (APEC). Berliner und Munchener tierarztliche Wochenschrift, 116(9-10): 381-395.
Fossum O, Jansson DS, Etterlin PE & Vågsholm I. 2009. Causes of mortality in laying hens in different housing systems in 2001 to 2004. Acta Veterinaria Scandinavica, 51(1): 1-9. DOI: 10.1186/1751-0147-51-3
Gales AC, Jones RN & Sader HS. 2011. Contemporary activity of colistin and polymyxin B against a worldwide collection of Gram-negative pathogens: results from the SENTRY Antimicrobial Surveillance Program (2006–09). Journal of Antimicrobial Chemotherapy, 66(9): 2070-2074. DOI: 10.1093/jac/dkr239
Ghafur A, Shankar C, GnanaSoundari P, Venkatesan M, Mani D, Thirunarayanan M & Veeraraghavan B. 2019. Detection of chromosomal and plasmid-mediated mechanisms of colistin resistance in Escherichia coli and Klebsiella pneumoniae from Indian food samples. Journal of Global Antimicrobial Resistance, 16:  48-52. DOI: 10.1016/j.jgar.2018.09.005
Goetting V, Lee K & Tell L. 2011. Pharmacokinetics of veterinary drugs in laying hens and residues in eggs: a review of the literature. Journal of veterinary pharmacology and therapeutics, 34(6): 521-556. DOI: 10.1111/j.1365-2885.2011.01287.x
Haque MH, Sarker S, Islam MS, Islam MA, Karim MR, Kayesh MEH, Shiddiky MJ & Anwer MS. 2020. Sustainable antibiotic-free broiler meat production: Current trends, challenges, and possibilities in a developing country perspective. Biology, 9(11): 411. DOI: 10.3390/biology9110411
Harper M, Boyce JD & Adler B. 2006. Pasteurella multocida pathogenesis: 125 years after Pasteur. FEMS Microbiology Letters, 265(1): 1-10. DOI: 10.1111/j.1574-6968.2006.00442.x
Heijnen L & Medema G. 2006. Quantitative detection of E. coli, E. coli O157 and other shiga toxin producing E. coli in water samples using a culture method combined with real-time PCR. Journal of Water and Health, 4(4): 487-498. DOI: 10.2166/wh.2006.0032
Hosain MZ, Kabir SL & Kamal MM. 2021. Antimicrobial uses for livestock production in developing countries. Veterinary World, 14(1): 210. 10.14202/vetworld.2021.210-221
Hossain M, Meher, M & Afrin M. 2017. Epidemiological investigation of Pasteurella multocida infection in poultry in Gazipur district of Bangladesh. Bangladesh Journal of Veterinary Medicine, 15(2): 91-95.
Hou J, Long X, Wang X, Li L, Mao D, Luo Y & Ren H. 2023. Global trend of antimicrobial resistance in common bacterial pathogens in response to antibiotic consumption. Journal of Hazardous Materials, 442: 130042. DOI: 10.1016/j.jhazmat.2022.130042
Humphries RM, Ambler J, Mitchell SL, Castanheira M, Dingle T, Hindler JA, Koeth L & Sei K. 2018. CLSI methods development and standardization working group best practices for evaluation of antimicrobial susceptibility tests. Journal of Clinical Microbiology, 56(4).  DOI: 10.1128/jcm. 01934-01917
Hunter P. 2001. OIE manual for standards of diagnostic tests and vaccines, Office International des Epizooties: book review. Journal of the South African Veterinary Association, 72(3): 150-157.
Ievy S, Islam MS, Sobur MA, Talukder M, Rahman MB, Khan MFR & Rahman MT. 2020. Molecular detection of avian pathogenic Escherichia coli (APEC) for the first time in layer farms in Bangladesh and their antibiotic resistance patterns. Microorganisms, 8(7): 1021. DOI: 10.3390/microorganisms8071021
Khaton R, Haider M, Paul P, Das P & Hossain M. 2008. Colibacillosis in commercial chickens in Bangladesh. Bangladesh Veterinarian, 25(1): 17-24.
Kheiri R & Akhtari L. 2016. Antimicrobial resistance and integron gene cassette arrays in commensal Escherichia coli from human and animal sources in IRI. Gut Pathogens, 8(1): 1-10.  DOI: 10.1186/s13099-016-0123-3
Kmeť V & Kmeťová M. 2010. High level of quinolone resistance in Escherichia coli from healthy chicken broilers. Folia Microbiologica, 55: 79-82.
Kumar D. 2019. Prospects and challenges of agro-industry in Bangladesh: An agripreneur view. African Journal of Agricultural Research, 14(31): 1379-1389.
Kwon SG, Cha SY, Choi EJ, Kim B, Song HJ & Jang HK. 2008. Epidemiological prevalence of avian pathogenic Escherichia coli differentiated by multiplex PCR from commercial chickens and hatchery in Korea. Journal of Bacteriology and Virology, 38(4): 179-188.
Liu YY, Wang, Y, Walsh TR, Yi LX, Zhang R, Spencer J, Doi Y, Tian G, Dong B & Huang X. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. The Lancet infectious diseases, 16(2): 161-168. DOI: 10.1016/S1473-3099(15)00424-7
Lutful Kabir S. 2010. Avian colibacillosis and salmonellosis: a closer look at epidemiology, pathogenesis, diagnosis, control and public health concerns. International journal of environmental research and public health, 7(1): 89-114.
Masud AA, Rousham EK, Islam MA, Alam MU, Rahman M, Mamun AA, Sarker S, Asaduzzaman M & Unicomb L. 2020. Drivers of antibiotic use in poultry production in Bangladesh: Dependencies and dynamics of a patron-client relationship. Frontiers in Veterinary Science, 7: 78. DOI: 10.3389/fvets.2020.00078
Mehmood M, Qazi M, Muhammad K, Shahid M, Akram M, Amin F, Gul M & Ali M. 2016. Isolation and molecular characterization of Pasteurella multocida from commercial layer flocks suffering from respiratory syndromes. JAPS: Journal of Animal & Plant Sciences, 26(1): 304-308.
Merchand I & Packer RA. 1967. Veterinary bacteriology and virology. Ames, Iowa: State University Press.
Olarinmoye A, Oladele O, Adediji A, Ntiwunka U & Tayo G. 2013. Antibiograms of avian pathogenic Escherichia coli isolates from commercial layers with colibacillosis in Southwest Nigeria. Malaysian Journal of Microbiology, 9(4): 317-325.
Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, Heck M, Savelkoul P, Vandenbroucke-Grauls C & van der Zwaluw K. 2011. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, The Netherlands. Emerging infectious diseases, 17(7): 1216.
Poirel L, Jayol A & Nordmann P. 2017. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clinical microbiology reviews, 30(2): 557-596.  DOI: 10.1128/cmr.00064-16
Rahman M, Samad M, Rahman M & Kabir S. 2004a. Bacterio-pathological studies on salmonellosis, colibacillosis and pasteurellosis in natural and experimental infections in chickens. Bangladesh Journal of Veterinary Medicine, 2(1): 1-8.  DOI: 10.3329/bjvm.v2i1.1926
Rahman M, Samad M, Rahman M & Kabir S. 2004b. In vitro antibiotic sensitivity and therapeutic efficacy of experimental salmonellosis, colibacillosis and pasteurellosis in broiler chickens. Bangladesh Journal of Veterinary Medicine, 2(2): 99-102.
Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, Guerra B, Malorny B, Borowiak M & Hammerl JA. 2018. Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes.
Eurosurveillance, 23(6): 17-00672. DOI: 10.2807/1560-7917.ES.2018.23.6.17-00672
Reig M & Toldrá F. 2008. Veterinary drug residues in meat: Concerns and rapid methods for detection. Meat Science, 78(1-2): 60-67.
Rosengren LB, Waldner CL & Reid-Smith RJ. 2009. Associations between antimicrobial resistance phenotypes, antimicrobial resistance genes, and virulence genes of fecal Escherichia coli isolates from healthy grow-finish pigs. Applied and Environmental Microbiology, 75(5): 1373-1380. DOI: 10.1128/aem.01253-08
Roshdy H, Abd El-Aziz S & Refai M. 2012. Incidence of E. coli in chickens and ducks in different governorates in Egypt. 1st Conf Anim Health Res Inst Assoc. Cairo,
Sarker MS, Mannan MS, Ali MY, Bayzid M, Ahad A & Bupasha ZB. 2019. Antibiotic resistance of Escherichia coli isolated from broilers sold at live bird markets in Chattogram, Bangladesh. Journal of Advanced Veterinary and Animal Research, 6(3): 272.
Singh R, Remington B, Blackall P & Turni C. 2014. Epidemiology of fowl cholera in free range broilers. Avian diseases, 58(1): 124-128. DOI: 10.1637/10656-090313-Reg.1
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Available Online from 08 December 2024

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