Genotypic analyses and antimicrobial resistance profiles of Campylobacter jejuni from crows (Corvidae) of United States and India reflect their respective local antibiotic burdens.

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    • Source:
      Publisher: Oxford University Press Country of Publication: England NLM ID: 9706280 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2672 (Electronic) Linking ISSN: 13645072 NLM ISO Abbreviation: J Appl Microbiol Subsets: MEDLINE
    • Publication Information:
      Publication: 2022- : Oxford : Oxford University Press
      Original Publication: Oxford : Published for the Society for Applied Bacteriology by Blackwell Science, c1997-
    • Subject Terms:
    • Abstract:
      Aim: The study examined the hypothesis that crow-borne Campylobacter can function as environmental reservoirs and indicators of antibiotic resistance (AR) determinants circulating in a human population.
      Methods and Results: Two species of crows from Washington (WA), United States, and Kolkata, India, respectively, were examined for their ability to carry antibiotic resistant Campylobacter. Campylobacter jejuni was the only species isolated by selective agar plating from crow faecal samples. Disk diffusion method used to compare the AR profile of the isolates showed tetracycline (TET) resistance to be the most prevalent (27%) among WA isolates, followed by ciprofloxacin (CIP; 24%). Among Kolkata isolates, nalidixic acid resistance was most common (36%), followed by CIP (27%). The AR profile demonstrated by crow isolates of WA reflects those reported by the US National Antimicrobial Resistance Monitoring System for human isolates (2007-2011), where resistance to TET was most prevalent (≈45%), followed by quinolones (≈24%). The Kolkata crow isolates reflected the AR profile of human clinical isolates from India, where 97% resistance was shown to quinolones, followed by TET (18%). Multilocus sequence typing of 37 isolates, including 11 water isolates from the crow roost area, showed 24 different sequence types (STs). Seventeen of these were previously found in wild birds, 2 in human diarrhoea, 4 in poultry and 8 in environmental water. One isolate was found in both water and faeces, though from different sites within WA.
      Conclusions: The results indicate that crows most likely acquire the AR from anthropogenic sources. Although they are colonized by specific STs, rarely isolated from humans, they can facilitate the spread of AR.
      Significance and Impact of the Study: By studying two areas in different continents, this research demonstrates that Campylobacter borne by crows can function as environmental reservoirs and indicators of AR determinants that circulate in a human population. This information will be of importance to scientists from the medical and poultry industries.
      (© 2021 Society for Applied Microbiology.)
    • References:
      Aarestrup, F., McDermot, P.F. & Wegener, H.C. (2008) Transmission of antibiotic resistance from food animals to humans. Washington DC: ASM Press.
      Alfredson, D.A. & Korolik, V. (2005) Isolation and expression of a novel molecular class D beta-lactamase, OXA-61, from Campylobacter jejuni. Antimicrobial Agents and Chemotherapy, 49, 2515-2518.
      Atterby, C., Börjesson, S., Ny, S., Järhult, J.D., Byfors, S. & Bonnedahl, J. (2017) ESBL-producing Escherichia coli in Swedish gulls-A case of environmental pollution from humans? PLoS One, 12, e0190380.
      Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S. et al. (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19, 455-477.
      Benskin, C.M., Wilson, K., Jones, K. & Hartley, I.R. (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biological Reviews of the Cambridge Philosophical Society, 84, 349-373.
      Bortolaia, V., Kaas, R.S., Ruppe, E., Roberts, M.C., Schwarz, S., Cattoir, V. et al. (2020) ResFinder 4.0 for predictions of phenotypes from genotypes. Journal of Antimicrobial Chemotherapy, 75, 3491-3500.
      Caldwell, D.B., Wang, Y. & Lin, J. (2008) Development, stability, and molecular mechanisms of macrolide resistance in Campylobacter jejuni. Antimicrobial Agents and Chemotherapy, 52, 3947-3954.
      CDC. (2012) Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet Surveillance Report for 2011 (Final Report). Atlanta, GA: U.S. Department of Health and Human Services, CDC. 2012. http://www.cdc.gov/foodnet/PDFs/2011_annual_report_508c.pdfhttp://www.cdc.gov/foodnet/PDFs/2011_annual_report_508c.pdf.
      Dolejska, M. & Literak, I. (2019) Wildlife is overlooked in the epidemiology of medically important antibiotic-resistant bacteria. Antimicrobial Agents and Chemotherapy, 63(8), e01167-19.
      Du, J., Luo, J., Huang, J., Wang, C., Li, M., Wang, B. et al. (2019) Emergence of genetic diversity and multi-drug resistant Campylobacter jejuni from wild birds in Beijing, China. Frontiers in Microbiology, 10, 2433.
      Engberg, J., Aarestrup, F.M., Taylor, D.E., Gerner-Smidt, P. & Nachamkin, I. (2001) Quinolone and macrolide resistance in Campylobacter jejuni and C. coli: resistance mechanisms and trends in human isolates. Emerging Infectious Diseases, 7, 24-34.
      Ge, B., Wang, F., Sjölund-Karlsson, M. & McDermott, P.F. (2013) Antimicrobial resistance in Campylobacter: susceptibility testing methods and resistance trends. Journal of Microbiol Methods, 95, 57-67.
      Ghosh, R., Uppal, B., Aggarwal, P., Chakravarti, A. & Jha, A.K. (2013) Increasing antimicrobial resistance of Campylobacter jejuni isolated from paediatric diarrhea cases in a tertiary care hospital of New Delhi, India. Journal of Clinical Diagnostic Research, 7, 247-249.
      Gibreel, A., Tracz, D.M., Nonaka, L., Ngo, T.M., Connell, S.R. & Taylor, D.E. (2004) Incidence of antibiotic resistance in Campylobacter jejuni isolated in Alberta, Canada, from 1999 to 2002, with special reference to tet(O)-mediated tetracycline resistance. Antimicrobial Agents and Chemotherapy, 48, 3442-3450.
      Griekspoor, P., Colles, F.M., McCarthy, N.D., Hansbro, P.M., Ashhurst-Smith, C., Olsen, B. et al. (2013) Marked host specificity and lack of phylogeographic population structure of Campylobacter jejuni in wild birds. Molecular Ecology, 22, 1463-1472.
      Griggs, D.J., Peake, L., Johnson, M.M., Ghori, S., Mott, A. & Piddock, L.J. (2009) Beta-lactamase-mediated beta-lactam resistance in Campylobacter species: prevalence of Cj0299 (bla OXA-61) and evidence for a novel beta-Lactamase in C. jejuni. Antimicrobial Agents and Chemotherapy, 53, 3357-3364.
      Guerrant, R.L., van Gilder, T., Steiner, T.S., Thielman, N.M., Slutsker, L., Tauxe, R.V. et al. (2001) Practice guidelines for the management of infectious diarrhea. Clinical Infectious Diseases, 32, 331-351.
      Gupta, A., Nelson, J.M., Barrett, T.J., Tauxe, R.V., Rossiter, S.P., Friedman, C.R. et al. (2004) Antimicrobial resistance among Campylobacter strains, United States, 1997-2001. Emerging Infectious Diseases, 10, 1102-1109.
      Hao, H., Dai, M., Wang, Y., Chen, D. & Yuan, Z. (2010) Quantification of mutated alleles of 23S rRNA in macrolide-resistant Campylobacter by TaqMan real-time polymerase chain reaction. Foodborne Pathogens and Disease, 7, 43-49.
      Hughes, L.A., Bennett, M., Coffey, P., Elliott, J., Jones, T.R., Jones, R.C. et al. (2009) Molecular epidemiology and characterization of Campylobacter spp. isolated from wild bird populations in northern England. Applied and Environment Microbiology, 75, 3007-3015.
      Iovine, N.M. (2013) Resistance mechanisms in Campylobacter jejuni. Virulence, 4, 230-240.
      Jain, D., Sinha, S., Prasad, K.N. & Pandey, C.M. (2005) Campylobacter species and drug resistance in a north Indian rural community. Transactions of the Royal Society of Tropical Medicine and Hygiene, 99, 207-214.
      Jolley, K.A., Bray, J.E. & Maiden, M.C.J. (2018) Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Research, 3, 124.
      Lachance, N., Gaudreau, C., Lamothe, F. & Larivière, L.A. (1991) Role of the beta-lactamase of Campylobacter jejuni in resistance to beta-lactam agents. Antimicrobial Agents and Chemotherapy, 35, 813-818.
      Li, X.Z., Mehrotra, M., Ghimire, S. & Adewoye, L. (2007) beta-Lactam resistance and beta-lactamases in bacteria of animal origin. Veterinary Microbiology, 121, 197-214.
      Luangtongkum, T., Jeon, B., Han, J., Plummer, P., Logue, C.M. & Zhang, Q. (2009) Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiology, 4, 189-200.
      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 & Infection, 18, 268-281.
      Marotta, F., Garofolo, G., di Marcantonio, L., di Serafino, G., Neri, D., Romantini, R. et al. (2019) Antimicrobial resistance genotypes and phenotypes of Campylobacter jejuni isolated in Italy from humans, birds from wild and urban habitats, and poultry. PLoS One, 14, e0223804.
      Meinersmann, R.J., Berrang, M.E., Bradshaw, J.K., Molina, M., Cosby, D.E., Genzlinger, L.L. et al. (2020) Recovery of thermophilic Campylobacter by three sampling methods from river sites in Northeast Georgia, USA, and their antimicrobial resistance genes. Letters in Applied Microbiology, 71, 102-107.
      Mukherjee, P., Ramamurthy, T., Bhattacharya, M.K., Rajendran, K. & Mukhopadhyay, A.K. (2013) Campylobacter jejuni in hospitalized patients with diarrhea, Kolkata, India. Emerging Infectious Diseases, 19, 1155-1156.
      Neogi, S.B., Islam, M.M., Islam, S.K.S., Akhter, A., Sikder, M.M.H., Yamasaki, S. & et al. (2020) Risk of multi-drug resistant Campylobacter spp. and residual antimicrobials at poultry farms and live bird markets in Bangladesh. BMC Infectious Diseases, 20, 278.
      Obeng, A.S., Rickard, H., Sexton, M., Pang, Y., Peng, H. & Barton, M. (2012) Antimicrobial susceptibilities and resistance genes in Campylobacter strains isolated from poultry and pigs in Australia. Journal of Applied Microbiology, 113, 294-307.
      Reddy, S. & Zishiri, O.T. (2017) Detection and prevalence of antimicrobial resistance genes in Campylobacter spp. isolated from chickens and humans. Onderstepoort Journal of Veterinary Research, 84, e1-e6.
      Ruiz-Palacios, G.M. (2007) The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clinical Infectious Diseases, 44, 701-703.
      Sen, K., Berglund, T., Soares, M.A., Taheri, B., Ma, Y., Khalil, L. et al. (2019) Antibiotic resistance of E. coli isolated from a constructed wetland dominated by a crow roost, with emphasis on ESBL and AmpC containing E. coli. Frontiers in Microbiology, 10, 1034.
      Sen, K., Lu, J., Mukherjee, P., Berglund, T., Varughese, E. & Mukhopadhyay, A.K. (2018) Campylobacter jejuni colonization in the crow gut involves many deletions within the cytolethal distending toxin gene cluster. Applied and Environment Microbiology, 84(6), e01893-17.
      Sen, K., Shepherd, V., Berglund, T., Quintana, A., Puim, S., Tadmori, R. et al. (2020) American crows as carriers of extra intestinal pathogenic E. coli and Avian pathogenic-like E. coli and their potential impact on a constructed wetland. Microorganisms, 8(10), 1595.
      Sheppard, S.K., Colles, F.M., McCarthy, N.D., Strachan, N.J., Ogden, I.D., Forbes, K.J. et al. (2011) Niche segregation and genetic structure of Campylobacter jejuni populations from wild and agricultural host species. Molecular Ecology, 20, 3484-3490.
      Silva, J., Leite, D., Fernandes, M., Mena, C., Gibbs, P. & Teixeira, P. (2011) Campylobacter spp. as a foodborne pathogen: a review. Frontiers in Microbiology, 2(200), 1-12. https://pubmed.ncbi.nlm.nih.gov/21991264.
      Soderlund, R., Skarin, H., Borjesson, S., Sanno, A., Jernberg, T., Aspan, A. et al. (2019) Prevalence and genomic characteristics of zoonotic gastro-intestinal pathogens and ESBL/pAmpC producing Enterobacteriaceae among Swedish corvid birds. Infection Ecology & Epidemiology, 9, 1701399.
      Stone, D., Davis, M., Baker, K., Besser, T., Roopnarine, R. & Sharma, R. (2013) MLST genotypes and antibiotic resistance of Campylobacter spp. isolated from poultry in Grenada. Biomed Research International, 2013, 794643.
      Taff, C.C., Weis, A.M., Wheeler, S., Hinton, M.G., Weimer, B.C., Barker, C.M. et al. (2016) Influence of host ecology and behavior on Campylobacter jejuni prevalence and environmental contamination risk in a synanthropic wild bird species. Applied and Environment Microbiology, 82, 4811-4820.
      Tajada, P., Gomez-Graces, J.L., Alós, J.I., Balas, D. & Cogollos, R. (1996) Antimicrobial susceptibilities of Campylobacter jejuni and Campylobacter coli to 12 beta-lactam agents and combinations with beta-lactamase inhibitors. Antimicrobial Agents and Chemotherapy, 40, 1924-1925.
      Watts, J.L., Shryock, T., Apley, M., Brown, S.D., Gray, J.T., Heine, H., Hunter, R.P., Mevius, D.J., Paich, M. & Silley, P. (2008). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Annapolis MD: Clinical and Laboratory Standards Institute. Approved standard-third edition.
      Weis, A.M., Storey, D.B., Taff, C.C., Townsend, A.K., Huang, B.C., Kong, N.T. et al. (2016) Genomic Comparison of Campylobacter spp. and their potential for zoonotic transmission between birds. Primates, and Livestock, 82, 7165-7175.
      Westerfield, M. (2012) The language of crows. Ashford Press.
      WHO. http://www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf.
      Wilson, D.L., Abner, S.R., Newman, T.C., Mansfield, L.S. & Linz, J.E. (2000) Identification of ciprofloxacin-resistant Campylobacter jejuni by use of a fluorogenic PCR assay. Journal of Clinical Microbiology, 38, 3971-3978.
      Withey, J.C. & Marzluff, J.M. (2005) Dispersal by juvenile American Crows (Corvus brachyrhynchos) influences population dynamics across a gradient of urbanization. The Auk, 122, 205-221.
      Zankari, E., Allesøe, R., Joensen, K.G., Cavaco, L.M., Lund, O. & Aarestrup, F.M. (2017) PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens. Journal of Antimicrobial Chemotherapy, 72, 2764-2768.
    • Grant Information:
      Fulbright Global Fellowship to Keya Sen; King County WaterWorks Program, Washington; University of Washington Bothell Facilities Services , Washington
    • Contributed Indexing:
      Keywords: Campylobacter; antimicrobial; environmental water; genotyping; resistance
    • Accession Number:
      0 (Anti-Bacterial Agents)
    • Publication Date:
      Date Created: 20210714 Date Completed: 20211230 Latest Revision: 20211230
    • Publication Date:
      20221213
    • Accession Number:
      10.1111/jam.15220
    • Accession Number:
      34260789