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Published in: Gut Pathogens 1/2023

Open Access 01-12-2023 | Aztreonam | Research

Vibrio cholerae O1 associated with recent endemic cholera shows temporal changes in serotype, genotype, and drug-resistance patterns in Bangladesh

Authors: Fatema Tuz Jubyda, Kazi Sumaita Nahar, Indrajeet Barman, Fatema-Tuz Johura, Mohammad Tarequl Islam, Marzia Sultana, Wali Ullah, Jarin Tasnim, Sahitya Ranjan Biswas, Md Mamun Monir, Christine Marie George, Andrew Camilli, Niyaz Ahmed, Allen G. Ross, John D. Clemens, Munirul Alam

Published in: Gut Pathogens | Issue 1/2023

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Abstract

Background

Despite the advancement in our understanding of cholera and its etiological agent, Vibrio cholerae, the prevention and treatment of the disease are often hindered due to rapid changes in drug response pattern, serotype, and the major genomic islands namely, the CTX-prophage, and related genetic characteristics. In the present study, V. cholerae (n = 172) associated with endemic cholera in Dhaka during the years 2015–2021 were analyzed for major phenotypic and genetic characteristics, including drug resistance patterns.

Results

Results revealed that the V. cholerae strains belonged to serogroup O1 biotype El Tor carrying El Tor -specific genes rtxC, tcpA El Tor, and hlyA El Tor, but possessed classical-biotype cholera toxin. Serotypes of V. cholerae strains differed temporally in predominance with Inaba during 2015–2017, and again in 2020–2021, while Ogawa was the predominant serotype in 2018–2019. Also, ctxB1 was predominant in V. cholerae associated with cholera during 2015–2017, while ctxB7 was predominant in 2018, and in the subsequent years, as observed until 2021. V. cholerae strains differed in their antibiotic resistance pattern with a majority (97%) being multi-drug resistant (MDR) and belonging to six sub-groups. Notably, one of these MDR strains was resistant to eleven of the eighteen antibiotics tested, with resistance to fourth-generation cephalosporin (cefepime), and aztreonam. This extreme drug resistant (XDR) strain carried resistance-related genes namely, extended-spectrum β-lactamases (ESBL), blaOXA-1 and blaPER-3.

Conclusion

The observed temporal switching of serotypes, as well as the ctxB genotype, and the emergence of MDR/XDR V. cholerae and their association with endemic cholera in Dhaka underscore the need for routine monitoring of the pathogen for proper patient management.
Literature
2.
go back to reference Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature. 2011;477(7365):462–5.CrossRefPubMedPubMedCentral Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature. 2011;477(7365):462–5.CrossRefPubMedPubMedCentral
4.
go back to reference Safa A, Nair GB, Kong RYC. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol. 2010;18(1):46–54.CrossRefPubMed Safa A, Nair GB, Kong RYC. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol. 2010;18(1):46–54.CrossRefPubMed
7.
go back to reference Ghosh P, Naha A, Pazhani GP, Ramamurthy T, Mukhopadhyay AK. Genetic traits of Vibrio cholerae O1 haitian isolates that are absent in contemporary strains from Kolkata India. PLoS ONE. 2014;9(11):112973.CrossRef Ghosh P, Naha A, Pazhani GP, Ramamurthy T, Mukhopadhyay AK. Genetic traits of Vibrio cholerae O1 haitian isolates that are absent in contemporary strains from Kolkata India. PLoS ONE. 2014;9(11):112973.CrossRef
8.
go back to reference Kumar P, Mishra DK, Deshmukh DG, Jain M, Zade AM, Ingole KV, et al. Vibrio cholerae O1 Ogawa El Tor strains with the ctxB7 allele driving cholera outbreaks in south-western India in 2012. Infect Genet Evol. 2014;1(25):93–6.CrossRef Kumar P, Mishra DK, Deshmukh DG, Jain M, Zade AM, Ingole KV, et al. Vibrio cholerae O1 Ogawa El Tor strains with the ctxB7 allele driving cholera outbreaks in south-western India in 2012. Infect Genet Evol. 2014;1(25):93–6.CrossRef
9.
go back to reference Rashid MU, Rashed SM, Islam T, Johura FT, Watanabe H, Ohnishi M, et al. CtxB1 outcompetes CtxB7 in Vibrio cholerae O1 Bangladesh. J Med Microbiol. 2016;65(1):101–3.CrossRefPubMed Rashid MU, Rashed SM, Islam T, Johura FT, Watanabe H, Ohnishi M, et al. CtxB1 outcompetes CtxB7 in Vibrio cholerae O1 Bangladesh. J Med Microbiol. 2016;65(1):101–3.CrossRefPubMed
10.
go back to reference Rashed SM, Mannan SB, Johura tuz F, Tarequl Islam M, Sadique A, Watanabe H, et al. Genetic characteristics of drug-resistant Vibrio cholerae O1 causing endemic cholera in Dhaka, 2006–2011. J Med Microbiol. 2012;61(PART12):1736–45.CrossRefPubMedPubMedCentral Rashed SM, Mannan SB, Johura tuz F, Tarequl Islam M, Sadique A, Watanabe H, et al. Genetic characteristics of drug-resistant Vibrio cholerae O1 causing endemic cholera in Dhaka, 2006–2011. J Med Microbiol. 2012;61(PART12):1736–45.CrossRefPubMedPubMedCentral
11.
go back to reference Karlsson SL, Thomson N, Mutreja A, Connor T, Sur D, Ali M, et al. Retrospective analysis of serotype switching of Vibrio cholerae O1 in a cholera endemic region shows it is a non-random process. PLoS Negl Trop Dis. 2016;10:10.CrossRef Karlsson SL, Thomson N, Mutreja A, Connor T, Sur D, Ali M, et al. Retrospective analysis of serotype switching of Vibrio cholerae O1 in a cholera endemic region shows it is a non-random process. PLoS Negl Trop Dis. 2016;10:10.CrossRef
12.
go back to reference Baddam R, Sarker N, Ahmed D, Mazumder R, Abdullah A, Morshed R, et al. Genome dynamics of Vibrio cholerae isolates linked to seasonal outbreaks of cholera in Dhaka Bangladesh. MBio. 2020;11:1.CrossRef Baddam R, Sarker N, Ahmed D, Mazumder R, Abdullah A, Morshed R, et al. Genome dynamics of Vibrio cholerae isolates linked to seasonal outbreaks of cholera in Dhaka Bangladesh. MBio. 2020;11:1.CrossRef
13.
go back to reference LeGault KN, Hays SG, Angermeyer A, McKitterick AC, Johura FT, Sultana M, et al. Temporal shifts in antibiotic resistance elements govern phage-pathogen conflicts. Science. 2021;373(6554):1–29.CrossRef LeGault KN, Hays SG, Angermeyer A, McKitterick AC, Johura FT, Sultana M, et al. Temporal shifts in antibiotic resistance elements govern phage-pathogen conflicts. Science. 2021;373(6554):1–29.CrossRef
15.
go back to reference Pereckaite L, Tatarunas V, Giedraitiene A. Current antimicrobial susceptibility testing for beta-lactamase-producing enterobacteriaceae in clinical settings. J Microbiol Methods. 2018;1(152):154–64.CrossRef Pereckaite L, Tatarunas V, Giedraitiene A. Current antimicrobial susceptibility testing for beta-lactamase-producing enterobacteriaceae in clinical settings. J Microbiol Methods. 2018;1(152):154–64.CrossRef
16.
go back to reference Thungapathra M, Sinha KK, Chaudhuri SR, Garg P, Ramamurthy T, Nair GB, et al. Occurrence of antibiotic resistance gene cassettes. Society. 2002;46(9):2948–55. Thungapathra M, Sinha KK, Chaudhuri SR, Garg P, Ramamurthy T, Nair GB, et al. Occurrence of antibiotic resistance gene cassettes. Society. 2002;46(9):2948–55.
17.
go back to reference Naha A, Pazhani GP, Ganguly M, Ghosh S, Ramamurthy T, Nandy RK, et al. Development and evaluation of a PCR assay for tracking the emergence and dissemination of haitian variant ctxB in Vibrio cholerae O1 strains isolated from Kolkata India. J Clin Microbiol. 2012;50(5):1733–6.CrossRefPubMedPubMedCentral Naha A, Pazhani GP, Ganguly M, Ghosh S, Ramamurthy T, Nandy RK, et al. Development and evaluation of a PCR assay for tracking the emergence and dissemination of haitian variant ctxB in Vibrio cholerae O1 strains isolated from Kolkata India. J Clin Microbiol. 2012;50(5):1733–6.CrossRefPubMedPubMedCentral
18.
go back to reference Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important b-lactamases in enterobacteriaceae. J Antimicrob Chemother. 2010;65(3):490–5.CrossRefPubMed Dallenne C, Da Costa A, Decré D, Favier C, Arlet G. Development of a set of multiplex PCR assays for the detection of genes encoding important b-lactamases in enterobacteriaceae. J Antimicrob Chemother. 2010;65(3):490–5.CrossRefPubMed
20.
go back to reference Bin Kim H, Wang M, Ahmed S, Park CH, LaRocque RC, Faruque ASG, et al. Transferable quinolone resistance in Vibrio cholerae. Antimicrob Agents Chemother. 2010;54(2):799–803.CrossRef Bin Kim H, Wang M, Ahmed S, Park CH, LaRocque RC, Faruque ASG, et al. Transferable quinolone resistance in Vibrio cholerae. Antimicrob Agents Chemother. 2010;54(2):799–803.CrossRef
21.
go back to reference Bin Kim H, Park CH, Kim CJ, Kim E, Jacoby GA, Hooper DC. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 2009;53(2):639–45.CrossRef Bin Kim H, Park CH, Kim CJ, Kim E, Jacoby GA, Hooper DC. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 2009;53(2):639–45.CrossRef
22.
go back to reference Mulvey MR, Grant JM, Plewes K, Roscoe D, Boyd DA. New Delhi metallo-β-lactamase in klebsiella pneumoniae and Escherichia coli Canada. Emerg Infect Dis. 2011;17(1):103–6.CrossRefPubMedPubMedCentral Mulvey MR, Grant JM, Plewes K, Roscoe D, Boyd DA. New Delhi metallo-β-lactamase in klebsiella pneumoniae and Escherichia coli Canada. Emerg Infect Dis. 2011;17(1):103–6.CrossRefPubMedPubMedCentral
23.
go back to reference Monir MM, Islam MT, Mazumder R, Mondal D, Nahar KSSM, et al. Genomic attributes of Vibrio cholerae O1 responsible for 2022 massive cholera outbreak in Bangladesh Res Sq. Basel: Preprint; 2022. Monir MM, Islam MT, Mazumder R, Mondal D, Nahar KSSM, et al. Genomic attributes of Vibrio cholerae O1 responsible for 2022 massive cholera outbreak in Bangladesh Res Sq. Basel: Preprint; 2022.
24.
go back to reference Page AJ, Taylor B, Keane JA. Multilocus sequence typing by blast from de novo assemblies against PubMLST. J Open Source Softw. 2016;1(8):118.CrossRef Page AJ, Taylor B, Keane JA. Multilocus sequence typing by blast from de novo assemblies against PubMLST. J Open Source Softw. 2016;1(8):118.CrossRef
25.
go back to reference Ambroise J, Irenge LM, Durant JF, Bearzatto B, Bwire G, Colin Stine O, et al. Backward compatibility of whole genome sequencing data with MLVA typing using a new MLVAtype shiny application for Vibrio cholerae. PLoS ONE. 2019;14(12):1–12.CrossRef Ambroise J, Irenge LM, Durant JF, Bearzatto B, Bwire G, Colin Stine O, et al. Backward compatibility of whole genome sequencing data with MLVA typing using a new MLVAtype shiny application for Vibrio cholerae. PLoS ONE. 2019;14(12):1–12.CrossRef
26.
go back to reference Wu CJ, Chuang YC, Lee MF, Lee CC, Lee HC, Lee NY, et al. Bacteremia due to extended-spectrum-β-lactamase-producing Aeromonas spp. at a medical center in Southern Taiwan. Antimicrob Agents Chemother. 2011;55(12):5813–8.CrossRefPubMedPubMedCentral Wu CJ, Chuang YC, Lee MF, Lee CC, Lee HC, Lee NY, et al. Bacteremia due to extended-spectrum-β-lactamase-producing Aeromonas spp. at a medical center in Southern Taiwan. Antimicrob Agents Chemother. 2011;55(12):5813–8.CrossRefPubMedPubMedCentral
29.
go back to reference Nair GB, Qadri F, Holmgren J, Svennerholm AM, Safa A, Bhuiyan NA, et al. Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. J Clin Microbiol. 2006;44(11):4211–3.CrossRefPubMedPubMedCentral Nair GB, Qadri F, Holmgren J, Svennerholm AM, Safa A, Bhuiyan NA, et al. Cholera due to altered El Tor strains of Vibrio cholerae O1 in Bangladesh. J Clin Microbiol. 2006;44(11):4211–3.CrossRefPubMedPubMedCentral
30.
go back to reference Pal BB, Nayak AK, Nayak SR. Emergence and spread of different ctxB alleles of Vibrio cholerae O1 in Odisha. India Int J Infect Dis. 2021;1(105):730–2.CrossRef Pal BB, Nayak AK, Nayak SR. Emergence and spread of different ctxB alleles of Vibrio cholerae O1 in Odisha. India Int J Infect Dis. 2021;1(105):730–2.CrossRef
31.
go back to reference Satchell KJF, Jones CJ, Wong J, Queen J, Agarwal S, Yildiz FH. Phenotypic analysis reveals that the 2010 haiti cholera epidemic is linked to a hypervirulent strain. Infect Immun. 2016;84(9):2473–81.CrossRefPubMedPubMedCentral Satchell KJF, Jones CJ, Wong J, Queen J, Agarwal S, Yildiz FH. Phenotypic analysis reveals that the 2010 haiti cholera epidemic is linked to a hypervirulent strain. Infect Immun. 2016;84(9):2473–81.CrossRefPubMedPubMedCentral
32.
go back to reference Hossain ZZ, Leekitcharoenphon P, Dalsgaard A, Sultana R, Begum A, Jensen PKM, et al. Comparative genomics of Vibrio cholerae O1 isolated from cholera patients in Bangladesh. Lett Appl Microbiol. 2018;67(4):329–36.CrossRefPubMed Hossain ZZ, Leekitcharoenphon P, Dalsgaard A, Sultana R, Begum A, Jensen PKM, et al. Comparative genomics of Vibrio cholerae O1 isolated from cholera patients in Bangladesh. Lett Appl Microbiol. 2018;67(4):329–36.CrossRefPubMed
33.
go back to reference Ramamurthy T, Mutreja A, Weill FX, Das B, Ghosh A, Nair GB. Revisiting the global epidemiology of cholera in conjuction with the genomics of Vibrio cholerae. Front Public Heal. 2019;7(July):1–10. Ramamurthy T, Mutreja A, Weill FX, Das B, Ghosh A, Nair GB. Revisiting the global epidemiology of cholera in conjuction with the genomics of Vibrio cholerae. Front Public Heal. 2019;7(July):1–10.
34.
go back to reference Smith AM, Weill FX, Njamkepo E, Ngomane HM, Ramalwa N, Sekwadi P, et al. Emergence of Vibrio cholerae o1 sequence type 75, South Africa, 2018–2020. Emerg Infect Dis. 2021;27(11):2927–31.CrossRefPubMedPubMedCentral Smith AM, Weill FX, Njamkepo E, Ngomane HM, Ramalwa N, Sekwadi P, et al. Emergence of Vibrio cholerae o1 sequence type 75, South Africa, 2018–2020. Emerg Infect Dis. 2021;27(11):2927–31.CrossRefPubMedPubMedCentral
37.
go back to reference Alam M, Kasan NA, Sadique A, Bhuiyan NA, Ahmed KU, Nusrin S, et al. Seasonal cholera caused by Vibrio cholerae serogroups O1 and O139 in the coastal aquatic environment of Bangladesh. Appl Environ Microbiol. 2006;72(6):4096–104.CrossRefPubMedPubMedCentral Alam M, Kasan NA, Sadique A, Bhuiyan NA, Ahmed KU, Nusrin S, et al. Seasonal cholera caused by Vibrio cholerae serogroups O1 and O139 in the coastal aquatic environment of Bangladesh. Appl Environ Microbiol. 2006;72(6):4096–104.CrossRefPubMedPubMedCentral
38.
go back to reference Alam M, Sultana M, Nair GB, Sack RB, Sack DA, Siddique AK, et al. Toxigenic Vibrio cholerae in the aquatic environment of mathbaria Bangladesh. Appl Environ Microbiol. 2006;72(4):2849–55.CrossRefPubMedPubMedCentral Alam M, Sultana M, Nair GB, Sack RB, Sack DA, Siddique AK, et al. Toxigenic Vibrio cholerae in the aquatic environment of mathbaria Bangladesh. Appl Environ Microbiol. 2006;72(4):2849–55.CrossRefPubMedPubMedCentral
40.
go back to reference Garbern SC, Chu TC, Yang P, Gainey M, Nasrin S, Kanekar S, et al. Clinical and socio-environmental determinants of multidrug-resistant Vibrio cholerae 01 in older children and adults in Bangladesh. Int J Infect Dis. 2021;105:436–41.CrossRefPubMedPubMedCentral Garbern SC, Chu TC, Yang P, Gainey M, Nasrin S, Kanekar S, et al. Clinical and socio-environmental determinants of multidrug-resistant Vibrio cholerae 01 in older children and adults in Bangladesh. Int J Infect Dis. 2021;105:436–41.CrossRefPubMedPubMedCentral
41.
go back to reference Krishna K, Anas A, Kuttan SP, Vijayakumar S, Chekidhenkuzhiyil J, Philomina B, et al. Multiple drug-resistant Vibrio Cholerae responsible for cholera outbreak among migrant domestic workers in Kerala, South India. Multidiscip Digit Publish Inst Proc. 2021;66(1):26. Krishna K, Anas A, Kuttan SP, Vijayakumar S, Chekidhenkuzhiyil J, Philomina B, et al. Multiple drug-resistant Vibrio Cholerae responsible for cholera outbreak among migrant domestic workers in Kerala, South India. Multidiscip Digit Publish Inst Proc. 2021;66(1):26.
42.
go back to reference Parvin I, Shahunja KM, Khan SH, Alam T, Shahrin L, Mahmuda Ackhter M, et al. Changing susceptibility pattern of Vibrio cholerae o1 isolates to commonly used antibiotics in the largest diarrheal disease hospital in Bangladesh during 2000–2018. Am J Trop Med Hyg. 2020;103(2):652–8.CrossRefPubMedPubMedCentral Parvin I, Shahunja KM, Khan SH, Alam T, Shahrin L, Mahmuda Ackhter M, et al. Changing susceptibility pattern of Vibrio cholerae o1 isolates to commonly used antibiotics in the largest diarrheal disease hospital in Bangladesh during 2000–2018. Am J Trop Med Hyg. 2020;103(2):652–8.CrossRefPubMedPubMedCentral
43.
go back to reference Kitaoka M, Miyata ST, Unterweger D, Pukatzki S. Antibiotic resistance mechanisms of Vibrio cholerae. London: Microbiology Society; 2011.CrossRef Kitaoka M, Miyata ST, Unterweger D, Pukatzki S. Antibiotic resistance mechanisms of Vibrio cholerae. London: Microbiology Society; 2011.CrossRef
45.
go back to reference Mandal J, Sangeetha V, Ganesan V, Parveen M, Preethi V, Harish BN, et al. Third-generation cephalosporin-resistant Vibrio cholerae. India Emerg Infect Dis. 2012;18(8):1326–8.PubMed Mandal J, Sangeetha V, Ganesan V, Parveen M, Preethi V, Harish BN, et al. Third-generation cephalosporin-resistant Vibrio cholerae. India Emerg Infect Dis. 2012;18(8):1326–8.PubMed
46.
go back to reference Verma J, Bag S, Saha B, Kumar P, Ghosh TS, Dayal M, et al. Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. Proc Natl Acad Sci USA. 2019;116(13):6226–31.CrossRefPubMedPubMedCentral Verma J, Bag S, Saha B, Kumar P, Ghosh TS, Dayal M, et al. Genomic plasticity associated with antimicrobial resistance in Vibrio cholerae. Proc Natl Acad Sci USA. 2019;116(13):6226–31.CrossRefPubMedPubMedCentral
Metadata
Title
Vibrio cholerae O1 associated with recent endemic cholera shows temporal changes in serotype, genotype, and drug-resistance patterns in Bangladesh
Authors
Fatema Tuz Jubyda
Kazi Sumaita Nahar
Indrajeet Barman
Fatema-Tuz Johura
Mohammad Tarequl Islam
Marzia Sultana
Wali Ullah
Jarin Tasnim
Sahitya Ranjan Biswas
Md Mamun Monir
Christine Marie George
Andrew Camilli
Niyaz Ahmed
Allen G. Ross
John D. Clemens
Munirul Alam
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2023
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-023-00537-0

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