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Volume 7, Issue 10

Phylogenetic and antimicrobial drug resistance analysis of O1 isolates from Ghana Open Access

Abstract

We investigated the evolution, phylogeny and antimicrobial resistance of O1 isolates (VCO1) from Ghana. Outbreak and environmental sources of VCO1 were characterized, whole-genome sequenced and compared to globally available seventh pandemic (7P) strains of at SNP resolution. Final analyses included 636 isolates. Novel Ghanaian isolates clustered into three distinct clades (clades 1, 2 and 3) in wave 3 of the 7P lineage. The closest relatives of our novel Ghanaian isolates were from Benin, Cameroon, Togo, Niger and Nigeria. All novel Ghanaian isolates were multi-drug resistant. Environmental isolates clustered into clade 2, despite being isolated years later, showing the possibility of persistence and re-emergence of older clades. A lag phase of several years from estimated introduction to reported cases suggests pathogen persistence in the absence of reported cholera cases. These results highlight the importance of deeper surveillance for understanding transmission routes between bordering countries and planning tailored vaccination campaigns in an effort to eradicate cholera.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): antibiotic resistance , cholera , outbreak , pandemic , phylogeny and West Africa
Funding
This study was supported by the:
  • NIHR Cambridge Biomedical Research Centre and AMR Research Capital Funding Scheme (Award NIHR200640)
    • Principle Award Recipient: GordonDougan
  • NIHR Cambridge Biomedical Research Centre and AMR Research Capital Funding Scheme (Award NIHR200640)
    • Principle Award Recipient: AnkurMutreja
  • Cambridge Africa Partnership for Research Excellence (CAPREx)
    • Principle Award Recipient: JaphethA. Opintan
  • Medical Research Council
    • Principle Award Recipient: RobertC Will
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-10-29
2024-04-26
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References

  1. World Health Organization WHO Fact Sheet: Cholera. World Health Organization - Fact Sheets ; 2021 https://www.who.int/news-room/fact-sheets/detail/cholera
  2. Azman AS, Rudolph KE, Cummings DAT, Lessler J. The incubation period of cholera: a systematic review. J Infect 2013; 66:432–438 [View Article] [PubMed]
     [Google Scholar]
  3. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB. Cholera. Lancet 2012; 379:2466–2476 [View Article] [PubMed]
     [Google Scholar]
  4. Vezzulli L, Colwell RR, Pruzzo C. Ocean warming and spread of pathogenic vibrios in the aquatic environment. Microb Ecol 2013; 65:817–825 [View Article] [PubMed]
     [Google Scholar]
  5. World Health Organization Global Health Atlas. https://www.who.int/data/gho/indicator-metadata-registry/imr-details/42 accessed 2021
  6. Rebaudet S, Sudre B, Faucher B, Piarroux R. Cholera in coastal Africa: a systematic review of its heterogeneous environmental determinants. J Infect Dis 2013; 208:S98–S106 [View Article]
     [Google Scholar]
  7. Ghana Health Service Ghana Health Service Annual Report for 2014; 2014 https://www.ghanahealthservice.org/downloads/Ghana_Health_Service_2014_Annual_Report.pdf accessed 02 Sep 2020
  8. Blake P. Historical perspectives on pandemic cholera. In Wachsmuth I, Blake P, Olsvik Ø. eds Vibrio cholerae and Cholera: Molecular to Global Perspectives Washington, DC: ASM Press; 1994 pp 293–295
     [Google Scholar]
  9. Dziejman M, Balon E, Boyd D, Fraser CM, Heidelberg JF et al. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease. Proc Natl Acad Sci USA 2002; 99:1556–1561 [View Article] [PubMed]
     [Google Scholar]
  10. Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011; 477:462–465 [View Article] [PubMed]
     [Google Scholar]
  11. Rahaman MH, Islam T, Colwell RR, Alam M. Molecular tools in understanding the evolution of Vibrio cholerae . Front Microbiol 2015; 6:1040 [View Article] [PubMed]
     [Google Scholar]
  12. Colwell RR. Global climate and infectious disease: the cholera paradigm. Science 1996; 274:2025–2031 [View Article] [PubMed]
     [Google Scholar]
  13. Dixit SM, Johura FT, Manandhar S, Sadique A, Rajbhandari RM et al. Cholera outbreaks (2012) in three districts of Nepal reveal clonal transmission of multi-drug resistant Vibrio cholerae O1. BMC Infect Dis 2014; 14:392 [View Article] [PubMed]
     [Google Scholar]
  14. Weill F-X, Domman D, Njamkepo E, Tarr C, Rauzier J et al. Genomic history of the seventh pandemic of cholera in Africa. Science 2017; 358:785–789 [View Article] [PubMed]
     [Google Scholar]
  15. Thompson CC, Freitas FS, Marin MA, Fonseca EL, Okeke IN et al. Vibrio cholerae O1 lineages driving cholera outbreaks during seventh cholera pandemic in Ghana. Infect Genet Evol 2011; 11:1951–1956 [View Article] [PubMed]
     [Google Scholar]
  16. Trucksis M, Michalski J, Deng YK, Kaper JB. The Vibrio cholerae genome contains two unique circular chromosomes. Proc Natl Acad Sci USA 1998; 95:14464–14469 [View Article] [PubMed]
     [Google Scholar]
  17. Eibach D, Herrera-León S, Gil H, Hogan B, Ehlkes L et al. Molecular epidemiology and antibiotic susceptibility of Vibrio cholerae associated with a large cholera outbreak in Ghana in 2014. PLoS Negl Trop Dis 2016; 10:e0004751 [View Article] [PubMed]
     [Google Scholar]
  18. Opintan JA, Newman MJ, Nsiah-Poodoh OA, Okeke IN. Vibrio cholerae O1 from Accra, Ghana carrying a class 2 integron and the SXT element. J Antimicrob Chemother 2008; 62:929–933 [View Article] [PubMed]
     [Google Scholar]
  19. Centers for Disease Control and Prevention Integrated Disease Surveillance and Response (IDSR), Global Health Protection and Security; 2010 https://www.cdc.gov/globalhealth/healthprotection/idsr/
  20. Suleman Y. Solid waste disposal and community health implications in Ghana: evidence from Sawaba, Asokore Mampong Municipal Assembly. J Civ Environ Eng 2016; 5:1000202 [View Article]
     [Google Scholar]
  21. Mireku-Gyimah N, Apanga PA, Awoonor-Williams JK. Cyclical cholera outbreaks in Ghana: filth, not myth. Infect Dis Poverty 2018; 7:51 [View Article] [PubMed]
     [Google Scholar]
  22. EPA Standard Analytical Protocol for Vibrio cholerae O1 and O139 in Drinking and Surface Water, EPA 600/R-10/139/October Washington, DC: Environmental Protection Agency; 2010
     [Google Scholar]
  23. CDC Laboratory Methods for the Diagnosis of Vibrio cholerae Atlanta, GA: Centers for Disease Control and Prevention; 2012
     [Google Scholar]
  24. CLSI Performance Standards for Antimicrobial Susceptibility Testing, 27th Informational Supplement, M100-S27 Wayne, PA: Clinical and Laboratory Standards Institute; 2017
     [Google Scholar]
  25. O’Brien TF, Stelling J. WHONET – tracking microbes for patient safety. J Microbiol Immunol Infect 2015; 48:S22 [View Article]
     [Google Scholar]
  26. Ponstingl H, Ning Z. SMALT. Wellcome Sanger Institute; 2010 https://www.sanger.ac.uk/tool/smalt-0/ accessed 11 Sep 2020
  27. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res 2015; 43:e15 [View Article] [PubMed]
     [Google Scholar]
  28. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
     [Google Scholar]
  29. Kalyaanamoorthy S, Minh BQ, Wong TKF, Von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
     [Google Scholar]
  30. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article] [PubMed]
     [Google Scholar]
  31. Rambaut A. FigTree, version 1.4.3; 2009 http://tree.bio.ed.ac.uk/software/figtree accessed 04 May 2020
  32. Tonkin-Hill G, Lees JA, Bentley SD, Frost SDW, Corander J. RhierBAPS: an R implementation of the population clustering algorithm hierBAPS. Wellcome Open Res 2018; 3:93 [View Article] [PubMed]
     [Google Scholar]
  33. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007; 7:214 [View Article] [PubMed]
     [Google Scholar]
  34. Rue Hå, Martino S. Approximate Bayesian inference for hierarchical Gaussian Markov random field models. J Stat Plan Inference 2007; 137:3177–3192 [View Article]
     [Google Scholar]
  35. Rambaut A, Drummond AJ. LogCombiner v1.8.2
  36. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 2018; 67:901–904 [View Article] [PubMed]
     [Google Scholar]
  37. Helfrich P, Rieb E, Abrami G, Lücking A, Mehler A. TREEANNOTATOR: versatile visual annotation of hierarchical text relations. In Proceedings of the Eleventh International Conference on Language Resources and Evaluation 2018
     [Google Scholar]
  38. Inouye M, Dashnow H, Raven L-. A, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article] [PubMed]
     [Google Scholar]
  39. Lu J. Krakentools; 2021 https://github.com/jenniferlu717/KrakenTools accessed 19 May 2021
  40. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with Kraken 2. Genome Biol 2019; 20:257 [View Article] [PubMed]
     [Google Scholar]
  41. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. Microb Genom 2017; 3:e000131 [View Article] [PubMed]
     [Google Scholar]
  42. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 2009; 25:1968–1969 [View Article] [PubMed]
     [Google Scholar]
  43. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58:212–220 [View Article] [PubMed]
     [Google Scholar]
  44. Harris SR. In_silico_pcr: script to run an in silico PCR for a set of primer pairs on an assembly; 2016 https://github.com/simonrharris/in_silico_pcr accessed 18 Jan 2021
  45. Center for Genomic Epidemiology CholeraeFinder 1.0. https://cge.cbs.dtu.dk/services/CholeraeFinder/ accessed 08 Sep 2020
  46. Moore S, Dongdem AZ, Opare D, Cottavoz P, Fookes M et al. Dynamics of cholera epidemics from Benin to Mauritania. PLoS Negl Trop Dis 2018; 12:e0006379 [View Article] [PubMed]
     [Google Scholar]
  47. Marin MA, Thompson CC, Freitas FS, Fonseca EL, Aboderin AO et al. Cholera outbreaks in Nigeria are associated with multidrug resistant atypical El Tor and non-O1/non-O139 Vibrio cholerae . PLoS Negl Trop Dis 2013; 7:e2049 [View Article] [PubMed]
     [Google Scholar]
  48. Kiiru J, Mutreja A, Mohamed AA, Kimani RW, Mwituria J et al. A study on the geophylogeny of clinical and environmental Vibrio cholerae in Kenya. PLoS One 2013; 8:e74829 [View Article] [PubMed]
     [Google Scholar]
  49. Pena ES, Kakaiuml CG, Bompangueacute D, Toureacute K. Cholera: evolution of epidemiological situation in four French-speaking African Countries from 2004 to 2013. West Afr J Med 2014; 33:245–251 [PubMed]
     [Google Scholar]
  50. Kuma GK, Opintan JA, Sackey S, Nyarko KM, Opare D et al. Antibiotic resistance patterns amongst clinical Vibrio cholerae O1 isolates from Accra, Ghana. Int J Infect Control 2014; 10:i3 [View Article]
     [Google Scholar]
  51. Danso EK, Asare P, Otchere ID, Akyeh LM, Asante-Poku A et al. A molecular and epidemiological study of Vibrio cholerae isolates from cholera outbreaks in southern Ghana. PLoS One 2020; 15:e0236016 [View Article] [PubMed]
     [Google Scholar]
  52. Ceccarelli D, Spagnoletti M, Bacciu D, Cappuccinelli P, Colombo MM. New V. cholerae atypical El Tor variant emerged during the 2006 epidemic outbreak in Angola. BMC Microbiol 2011; 11:130 [View Article] [PubMed]
     [Google Scholar]
  53. Spagnoletti M, Ceccarelli D, Rieux A, Fondi M, Taviani E et al. Acquisition and evolution of SXT-R391 integrative conjugative elements in the seventh-pandemic Vibrio cholerae lineage. mBio 2014; 5:e01356-14 [View Article] [PubMed]
     [Google Scholar]
  54. Rijal N, Acharya J, Adhikari S, Upadhaya BP, Shakya G et al. Changing epidemiology and antimicrobial resistance in Vibrio cholerae: AMR surveillance findings (2006-2016) from Nepal. BMC Infect Dis 2019; 19:801 [View Article] [PubMed]
     [Google Scholar]
  55. Rezaie N, Bakhshi B, Najar-Peerayeh S. Distribution of resistance genetic determinants among Vibrio cholerae isolates of 2012 and 2013 outbreaks in IR Iran. Microb Pathog 2017; 104:12–16 [View Article] [PubMed]
     [Google Scholar]
  56. Kar SK, Pal BB, Khuntia HK, Achary KG, Khuntia CP. Emergence and spread of tetracycline resistant Vibrio cholerae O1 El Tor variant during 2010 cholera epidemic in the tribal areas of Odisha, India. Int J Infect Dis 2015; 33:45–49 [View Article] [PubMed]
     [Google Scholar]
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Phylogenetic and antimicrobial drug resistance analysis of Vibrio cholerae O1 isolates from Ghana
M Gen 7, 000668 (2021); https://doi.org/10.1099/mgen.0.000668
/content/journal/mgen/10.1099/mgen.0.000668
/content/journal/mgen/10.1099/mgen.0.000668
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