{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,20]],"date-time":"2026-03-20T12:04:22Z","timestamp":1774008262619,"version":"3.50.1"},"reference-count":27,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T00:00:00Z","timestamp":1623628800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T00:00:00Z","timestamp":1623628800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Infect Dis"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background<\/jats:title>\n                <jats:p>Cholera has been present and recurring in Zambia since 1977. However, there is a paucity of data on genetic relatedness and diversity of the <jats:italic>Vibrio cholerae<\/jats:italic> isolates responsible for these outbreaks. Understanding whether the outbreaks are seeded from existing local isolates or if the outbreaks represent separate transmission events can inform public health decisions.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>Seventy-two <jats:italic>V. cholerae<\/jats:italic> isolates from outbreaks in 2009\/2010, 2016, and 2017\/2018 in Zambia were characterized using multilocus variable number tandem repeat analysis (MLVA) and whole genome sequencing (WGS). The isolates had eight distinct MLVA genotypes that clustered into three MLVA clonal complexes (CCs). Each CC contained isolates from only one outbreak. The results from WGS revealed both clustered and dispersed single nucleotide variants. The genetic relatedness of isolates based on WGS was consistent with the MLVA, each CC was a distinct genetic lineage and had nearest neighbors from other East African countries. In Lusaka, isolates from the same outbreak were more closely related to themselves and isolates from other countries than to isolates from other outbreaks in other years.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>Our observations are consistent with i) the presence of random mutation and alternative mechanisms of nucleotide variation, and ii) three separate transmission events of <jats:italic>V. cholerae<\/jats:italic> into Lusaka, Zambia. We suggest that locally, case-area targeted invention strategies and regionally, well-coordinated plans be in place to effectively control future cholera outbreaks.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s12879-021-06259-5","type":"journal-article","created":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T10:03:03Z","timestamp":1623664983000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["Three transmission events of Vibrio cholerae O1 into Lusaka, Zambia"],"prefix":"10.1186","volume":"21","author":[{"given":"John","family":"Mwaba","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amanda K.","family":"Debes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kelsey N.","family":"Murt","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Patrick","family":"Shea","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Michelo","family":"Simuyandi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natasha","family":"Laban","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katayi","family":"Kazimbaya","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Caroline","family":"Chisenga","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shan","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mathieu","family":"Almeida","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jacquelyn S.","family":"Meisel","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aaron","family":"Shibemba","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Timothy","family":"Kantenga","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Victor","family":"Mukonka","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Geoffrey","family":"Kwenda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"David A.","family":"Sack","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Roma","family":"Chilengi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"O. Colin","family":"Stine","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,6,14]]},"reference":[{"key":"6259_CR1","volume-title":"CHOLERA COUNTRY PROFILE: ZAMBIA [Internet]. Lusaka","author":"WHO","year":"2011","unstructured":"WHO. CHOLERA COUNTRY PROFILE: ZAMBIA [Internet]. Lusaka; 2011 [cited 2017 Aug 21]. Available from: http:\/\/www.who.int\/cholera\/countries\/ZambiaCountryProfile2011.pdf?ua=1"},{"issue":"8","key":"6259_CR2","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1111\/tmi.13084","volume":"23","author":"J Mwaba","year":"2018","unstructured":"Mwaba J, Ferreras E, Chizema-Kawesa E, Mwimbe D, Tafirenyika F, Rauzier J, et al. Evaluation of the SD bioline cholera rapid diagnostic test during the 2016 cholera outbreak in Lusaka. Zambia Trop Med Int Heal. 2018;23(8):834\u201340. https:\/\/doi.org\/10.1111\/tmi.13084.","journal-title":"Zambia Trop Med Int Heal"},{"key":"6259_CR3","doi-asserted-by":"crossref","unstructured":"De R, Ghosh JB, Sen Gupta S, Takeda Y, Nair GB. The Role of Vibrio cholerae Genotyping in Africa. J Infect Dis. 2013;208(SUPPL. 1):532-8.","DOI":"10.1093\/infdis\/jit199"},{"issue":"6","key":"6259_CR4","doi-asserted-by":"publisher","first-page":"e0006492","DOI":"10.1371\/journal.pntd.0006492","volume":"12","author":"G Bwire","year":"2018","unstructured":"Bwire G, Sack DA, Almeida M, Li S, Voeglein JB, Debes AK, et al. Molecular characterization of Vibrio cholerae responsible for cholera epidemics in Uganda by PCR, MLVA and WGS. Picardeau M, editor. PLoS Negl Trop Dis. 2018;12(6):e0006492 [cited 2018 Sep 21]. Available from: http:\/\/dx.plos.org\/10.1371\/journal.pntd.0006492.","journal-title":"PLoS Negl Trop Dis"},{"key":"6259_CR5","doi-asserted-by":"crossref","unstructured":"B\u00e9nard AHM, Guenou E, Fookes M, Ateudjieu J, Kasambara W, Siever M, et al. Whole genome sequence of vibrio cholerae directly from dried spotted filter paper. PLoS Negl Trop Dis. 2019;13(5):e0007330.","DOI":"10.1371\/journal.pntd.0007330"},{"issue":"1","key":"6259_CR6","doi-asserted-by":"publisher","first-page":"e0004307","DOI":"10.1371\/journal.pntd.0004307","volume":"10","author":"AK Debes","year":"2016","unstructured":"Debes AK, Ateudjieu J, Guenou E, Lopez AL, Bugayong MP, Retiban PJ, et al. Evaluation in Cameroon of a Novel, Simplified Methodology to Assist Molecular Microbiological Analysis of V. cholerae in Resource-Limited Settings. Ryan ET, editor. PLoS Negl Trop Dis. 2016;10(1):e0004307 [cited 2018 Aug 24]. Available from: http:\/\/dx.plos.org\/10.1371\/journal.pntd.0004307.","journal-title":"PLoS Negl Trop Dis"},{"issue":"17","key":"6259_CR7","doi-asserted-by":"publisher","first-page":"4367","DOI":"10.1128\/JB.00698-10","volume":"192","author":"EA Kendall","year":"2010","unstructured":"Kendall EA, Chowdhury F, Begum Y, Khan AI, Li S, Thierer JH, et al. Relatedness of Vibrio cholerae O1\/O139 isolates from patients and their household contacts, determined by multilocus variable-number tandem-repeat analysis. J Bacteriol. 2010;192(17):4367\u201376 [cited 2018 Aug 26]. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/20585059.","journal-title":"J Bacteriol"},{"key":"6259_CR8","unstructured":"S A. Babraham Bioinformatics - FastQC A Quality Control tool for High Throughput Sequence Data [Internet]. 2010 [cited 2020 Dec 21]. Available from: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/"},{"key":"6259_CR9","doi-asserted-by":"crossref","unstructured":"Chen S, Zhou Y, Chen Y, Gu J. Fastp: An ultra-fast all-in-one FASTQ preprocessor. In: Bioinformatics. Oxford University Press; 2018. p. i884\u201390.","DOI":"10.1093\/bioinformatics\/bty560"},{"issue":"4","key":"6259_CR10","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","volume":"9","author":"B Langmead","year":"2012","unstructured":"Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012 Apr;9(4):357\u20139. https:\/\/doi.org\/10.1038\/nmeth.1923.","journal-title":"Nat Methods"},{"issue":"16","key":"6259_CR11","doi-asserted-by":"publisher","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","volume":"25","author":"H Li","year":"2009","unstructured":"Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment\/map format and SAMtools. Bioinformatics. 2009 Aug;25(16):2078\u20139. https:\/\/doi.org\/10.1093\/bioinformatics\/btp352.","journal-title":"Bioinformatics."},{"issue":"6","key":"6259_CR12","doi-asserted-by":"publisher","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","volume":"26","author":"AR Quinlan","year":"2010","unstructured":"Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics. 2010 Jan 28;26(6):841\u20132. https:\/\/doi.org\/10.1093\/bioinformatics\/btq033.","journal-title":"Bioinformatics."},{"issue":"10","key":"6259_CR13","doi-asserted-by":"publisher","first-page":"714","DOI":"10.1089\/cmb.2013.0084","volume":"20","author":"S Nurk","year":"2013","unstructured":"Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol. 2013 Oct 1;20(10):714\u201337. https:\/\/doi.org\/10.1089\/cmb.2013.0084.","journal-title":"J Comput Biol"},{"issue":"8","key":"6259_CR14","doi-asserted-by":"publisher","first-page":"1072","DOI":"10.1093\/bioinformatics\/btt086","volume":"29","author":"A Gurevich","year":"2013","unstructured":"Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013 Apr 15;29(8):1072\u20135. https:\/\/doi.org\/10.1093\/bioinformatics\/btt086.","journal-title":"Bioinformatics."},{"issue":"11","key":"6259_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s13059-014-0524-x","volume":"15","author":"TJ Treangen","year":"2014","unstructured":"Treangen TJ, Ondov BD, Koren S, Phillippy AM. The harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 2014;15(11):1\u201315.","journal-title":"Genome Biol"},{"key":"6259_CR16","doi-asserted-by":"crossref","unstructured":"Price MN, Dehal PS, Arkin AP. FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One. 2010;10, 5(3):e9490.","DOI":"10.1371\/journal.pone.0009490"},{"issue":"W1","key":"6259_CR17","doi-asserted-by":"publisher","first-page":"W242","DOI":"10.1093\/nar\/gkw290","volume":"44","author":"I Letunic","year":"2016","unstructured":"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 Jul 8;44(W1):W242\u20135. https:\/\/doi.org\/10.1093\/nar\/gkw290.","journal-title":"Nucleic Acids Res"},{"issue":"3","key":"6259_CR18","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","volume":"215","author":"SF Altschul","year":"1990","unstructured":"Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403\u201310. https:\/\/doi.org\/10.1016\/S0022-2836(05)80360-2.","journal-title":"J Mol Biol"},{"issue":"APR","key":"6259_CR19","doi-asserted-by":"publisher","first-page":"901","DOI":"10.3389\/fmicb.2019.00901","volume":"10","author":"YMG Hounmanou","year":"2019","unstructured":"Hounmanou YMG, Leekitcharoenphon P, Hendriksen RS, Dougnon TV, Mdegela RH, Olsen JE, et al. Surveillance and Genomics of Toxigenic Vibrio cholerae O1 From Fish, Phytoplankton and Water in Lake Victoria, Tanzania. Front Microbiol. 2019;10(APR):901 [cited 2020 Dec 21]. Available from: https:\/\/www.frontiersin.org\/article\/10.3389\/fmicb.2019.00901\/full.","journal-title":"Front Microbiol"},{"issue":"12","key":"6259_CR20","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0007934","volume":"13","author":"YMG Hounmanou","year":"2019","unstructured":"Hounmanou YMG, Leekitcharoenphon P, Kudirkiene E, Mdegela RH, Hendriksen RS, Olsen JE, et al. Genomic insights into Vibrio cholerae O1 responsible for cholera epidemics in Tanzania between 1993 and 2017. PLoS Negl Trop Dis. 2019 Dec 23;13(12):e0007934. https:\/\/doi.org\/10.1371\/journal.pntd.0007934.","journal-title":"PLoS Negl Trop Dis"},{"issue":"1","key":"6259_CR21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12879-017-2252-9","volume":"17","author":"Y Kachwamba","year":"2017","unstructured":"Kachwamba Y, Mohammed AA, Lukupulo H, Urio L, Majigo M, Mosha F, et al. Genetic characterization of Vibrio cholerae O1 isolates from outbreaks between 2011 and 2015 in Tanzania. BMC Infect Dis. 2017;17(1):1\u20136.","journal-title":"BMC Infect Dis"},{"issue":"6364","key":"6259_CR22","doi-asserted-by":"publisher","first-page":"785","DOI":"10.1126\/science.aad5901","volume":"358","author":"FX Weill","year":"2017","unstructured":"Weill FX, Domman D, Njamkepo E, Tarr C, Rauzier J, Fawal N, et al. Genomic history of the seventh pandemic of cholera in Africa. Science. 2017;358(6364):785\u20139. https:\/\/doi.org\/10.1126\/science.aad5901.","journal-title":"Science"},{"issue":"4","key":"6259_CR23","doi-asserted-by":"publisher","first-page":"e0008227","DOI":"10.1371\/journal.pntd.0008227","volume":"14","author":"J Mwaba","year":"2020","unstructured":"Mwaba J, Debes AK, Shea P, Mukonka V, Chewe O, Chisenga C, et al. Identification of cholera hotspots in Zambia: A spatiotemporal analysis of cholera data from 2008 to 2017. Akullian A, editor. PLoS Negl Trop Dis. 2020;14(4):e0008227 [cited 2020 Sep 21]. Available from: https:\/\/dx.plos.org\/10.1371\/journal.pntd.0008227.","journal-title":"PLoS Negl Trop Dis"},{"issue":"6","key":"6259_CR24","doi-asserted-by":"publisher","first-page":"e0005671","DOI":"10.1371\/journal.pntd.0005671","volume":"11","author":"M Garrine","year":"2017","unstructured":"Garrine M, Mandomando I, Vubil D, Nhampossa T, Acacio S, Li S, et al. Minimal genetic change in Vibrio cholerae in Mozambique over time: Multilocus variable number tandem repeat analysis and whole genome sequencing. PLoS Negl Trop Dis. 2017;11(6):e0005671 [cited 2018 Feb 10]. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/28622368.","journal-title":"PLoS Negl Trop Dis"},{"issue":"5","key":"6259_CR25","doi-asserted-by":"publisher","first-page":"2141","DOI":"10.1073\/pnas.0906355107","volume":"107","author":"R Chayot","year":"2010","unstructured":"Chayot R, Montagne B, Mazel D, Ricchetti M. An end-joining repair mechanism in Escherichia coli. Proc Natl Acad Sci U S A. 2010 Feb 2;107(5):2141\u20136. https:\/\/doi.org\/10.1073\/pnas.0906355107.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"2","key":"6259_CR26","doi-asserted-by":"publisher","first-page":"233","DOI":"10.3201\/eid2202.151175","volume":"22","author":"CM George","year":"2016","unstructured":"George CM, Monira S, Sack DA, Rashid M, Saif-Ur-Rahman KM, Mahmud T, et al. Randomized Controlled Trial of Hospital-Based Hygiene and Water Treatment Intervention (CHoBI7) to Reduce Cholera. Emerg Infect Dis. 2016;22(2):233\u201341 [cited 2019 may 15]. Available from: http:\/\/www.ncbi.nlm.nih.gov\/pubmed\/26811968.","journal-title":"Emerg Infect Dis"},{"key":"6259_CR27","first-page":"8","volume":"1","author":"E Michel","year":"2019","unstructured":"Michel E, Gaudart J, Beaulieu S, Bulit G, Piarroux M, Boncy J, et al. Full title: estimating effectiveness of case-area targeted response interventions against cholera in Haiti. Elife. 2019;1:8.","journal-title":"Elife"}],"container-title":["BMC Infectious Diseases"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12879-021-06259-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12879-021-06259-5\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12879-021-06259-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,6,14]],"date-time":"2021-06-14T10:03:24Z","timestamp":1623665004000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcinfectdis.biomedcentral.com\/articles\/10.1186\/s12879-021-06259-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,6,14]]},"references-count":27,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["6259"],"URL":"https:\/\/doi.org\/10.1186\/s12879-021-06259-5","relation":{},"ISSN":["1471-2334"],"issn-type":[{"value":"1471-2334","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,6,14]]},"assertion":[{"value":"2 February 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 June 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"Ethical approval was granted by the ethical review committee of The University of Zambia Biomedical Research Ethics Committee (UNZABREC- REF NO:003\u201310-17).","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval, consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"570"}}