{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,16]],"date-time":"2026-06-16T16:09:34Z","timestamp":1781626174204,"version":"3.54.5"},"reference-count":27,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,8,3]],"date-time":"2020-08-03T00:00:00Z","timestamp":1596412800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,8,3]],"date-time":"2020-08-03T00:00:00Z","timestamp":1596412800000},"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":["Malar J"],"published-print":{"date-parts":[[2020,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>At the beginning of 2019, a sudden surge of malaria cases was observed in the district of Riaba, Bioko Island. Between January and April, confirmed malaria cases increased 3.8-fold compared to the same period in 2018. Concurrently, anopheline human biting rate (HBR) increased 2.1-fold. During the outbreak, 82.2% of the district population was tested for malaria with a rapid diagnostic test; 37.2% of those tested had a detectable infection and were treated according to national guidelines. Vector control interventions, including indoor residual spraying and larval source management were scaled-up. After the interventions, the number of confirmed cases decreased by 70% and the overall parasite prevalence in the communities by 43.8%. Observed prevalence in a follow up malaria indicator survey, however, was significantly higher than elsewhere on the island, and higher than in previous years. There was no significant reduction in HBR, which remained high for the rest of the year. The surge was attributed to various factors, chiefly increased rainfall and a large number of anthropogenic anopheline breeding sites created by construction works. This case study highlights the need for sustained vector control interventions and multi-sector participation, particularly in malaria control and elimination settings with persistently high local malaria receptivity.<\/jats:p>","DOI":"10.1186\/s12936-020-03347-w","type":"journal-article","created":{"date-parts":[[2020,8,3]],"date-time":"2020-08-03T07:06:13Z","timestamp":1596438373000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Malaria outbreak in Riaba district, Bioko Island: lessons learned"],"prefix":"10.1186","volume":"19","author":[{"given":"Carlos A.","family":"Guerra","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Godwin","family":"Fuseini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olivier Tresor","family":"Donfack","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jordan M.","family":"Smith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Teresa Ayingono","family":"Ondo Mifumu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gninoussa","family":"Akadiri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Delicias Esono Mba","family":"Eyang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Consuelo Oki","family":"Eburi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liberato","family":"Motobe Vaz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victor Mba","family":"Micha","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leonor Ada","family":"Okenve","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher R.","family":"Janes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ramona Mba","family":"Andeme","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matilde Riloha","family":"Rivas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wonder P.","family":"Phiri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michel A.","family":"Slotman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David L.","family":"Smith","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4430-4781","authenticated-orcid":false,"given":"Guillermo A.","family":"Garc\u00eda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,8,3]]},"reference":[{"key":"3347_CR1","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1186\/s12936-018-2213-9","volume":"17","author":"J Cook","year":"2018","unstructured":"Cook J, Hergott D, Phiri W, Rivas MR, Bradley J, Segura L, et al. Trends in parasite prevalence following 13\u00a0years of malaria interventions on Bioko Island, Equatorial Guinea: 2004\u20132016. Malar J. 2018;17:62.","journal-title":"Malar J."},{"key":"3347_CR2","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1603\/0022-2585-41.2.158","volume":"41","author":"J Cano","year":"2004","unstructured":"Cano J, Berzosa PJ, Roche J, Rubio JM, Moyano E, Guerra-Neira A, et al. Malaria vectors in the Bioko Island (Equatorial Guinea): estimation of vector dynamics and transmission intensities. J Med Entomol. 2004;41:158\u201361.","journal-title":"J Med Entomol"},{"key":"3347_CR3","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/S0035-9203(00)90246-3","volume":"94","author":"SI Hay","year":"2000","unstructured":"Hay SI, Rogers DJ, Toomer JF, Snow RW. Annual Plasmodium falciparum entomological inoculation rates (EIR) across Africa: literature survey, internet access and review. Trans R Soc Trop Med Hyg. 2000;94:113\u201327.","journal-title":"Trans R Soc Trop Med Hyg"},{"key":"3347_CR4","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1186\/1475-2875-8-19","volume":"8","author":"LA Kelly-Hope","year":"2009","unstructured":"Kelly-Hope LA, McKenzie FE. The multiplicity of malaria transmission: a review of entomological inoculation rate measurements and methods across sub-Saharan Africa. Malar J. 2009;8:19.","journal-title":"Malar J."},{"key":"3347_CR5","doi-asserted-by":"publisher","first-page":"219","DOI":"10.4269\/ajtmh.2006.75.219","volume":"75","author":"PE Okello","year":"2006","unstructured":"Okello PE, Van Bortel WIM, Byaruhanga AM, Correwyn A, Roelants P, Talisuna A, et al. Variation in malaria transmission intensity in seven sites throughout Uganda. Am J Trop Med Hyg. 2006;75:219\u201325.","journal-title":"Am J Trop Med Hyg"},{"key":"3347_CR6","doi-asserted-by":"publisher","first-page":"246","DOI":"10.11646\/zootaxa.3619.3.2","volume":"3619","author":"M Coetzee","year":"2013","unstructured":"Coetzee M, Hunt RH, Wilkerson R, Della Torre A, Coulibaly MB, Besansky NJ. Anopheles coluzzii and Anopheles amharicus, new members of the Anopheles gambiae complex. Zootaxa. 2013;3619:246\u201374.","journal-title":"Zootaxa."},{"key":"3347_CR7","doi-asserted-by":"publisher","first-page":"253","DOI":"10.1186\/1756-3305-5-253","volume":"5","author":"HJ Overgaard","year":"2012","unstructured":"Overgaard HJ, Reddy VP, Abaga S, Matias A, Reddy MR, Kulkarni V, et al. Malaria transmission after five years of vector control on Bioko Island, Equatorial Guinea. Parasit Vectors. 2012;5:253.","journal-title":"Parasit Vectors."},{"key":"3347_CR8","doi-asserted-by":"publisher","first-page":"184","DOI":"10.1186\/1475-2875-10-184","volume":"10","author":"MR Reddy","year":"2011","unstructured":"Reddy MR, Overgaard HJ, Abaga S, Reddy VP, Caccone A, Kiszewski AE, et al. Outdoor host seeking behaviour of Anopheles gambiae mosquitoes following initiation of malaria vector control on Bioko Island, Equatorial Guinea. Malar J. 2011;10:184.","journal-title":"Malar J."},{"key":"3347_CR9","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1111\/eva.12094","volume":"6","author":"TK Hodges","year":"2013","unstructured":"Hodges TK, Athrey G, Deitz KC, Overgaard HJ, Matias A, Caccone A, et al. Large fluctuations in the effective population size of the malaria mosquito Anopheles gambiae s.s. during vector control cycle. Evol Appl. 2013;6:1171\u201383.","journal-title":"Evol Appl"},{"key":"3347_CR10","doi-asserted-by":"publisher","first-page":"170","DOI":"10.1186\/s12936-015-0679-2","volume":"14","author":"J Bradley","year":"2015","unstructured":"Bradley J, Lines J, Fuseini G, Schwabe C, Monti F, Slotman M, et al. Outdoor biting by Anopheles mosquitoes on Bioko Island does not currently impact on malaria control. Malar J. 2015;14:170.","journal-title":"Malar J."},{"key":"3347_CR11","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1046\/j.1365-2915.2002.00393.x","volume":"16","author":"C Fanello","year":"2002","unstructured":"Fanello C, Santolamazza F, della Torre A. Simultaneous identification of species and molecular forms of the Anopheles gambiae complex by PCR-RFLP. Med Vet Entomol. 2002;16:461\u20134.","journal-title":"Med Vet Entomol"},{"key":"3347_CR12","doi-asserted-by":"publisher","first-page":"503","DOI":"10.4269\/ajtmh.2002.66.503","volume":"66","author":"B Morassin","year":"2002","unstructured":"Morassin B, Fabre R, Berry A, Magnaval JF. One year\u2019s experience with the polymerase chain reaction as a routine method for the diagnosis of imported malaria. Am J Trop Med Hyg. 2002;66:503\u20138.","journal-title":"Am J Trop Med Hyg"},{"key":"3347_CR13","doi-asserted-by":"publisher","first-page":"1071","DOI":"10.1093\/jme\/tjz025","volume":"56","author":"G Fuseini","year":"2019","unstructured":"Fuseini G, Nguema RN, Phiri WP, Donfack OT, Cortes C, Von Fricken ME, et al. Increased biting rate of insecticide-resistant Culex mosquitoes and community adherence to IRS for malaria control in urban Malabo, Bioko Island, Equatorial Guinea. J Med Entomol. 2019;56:1071\u20137.","journal-title":"J Med Entomol."},{"key":"3347_CR14","doi-asserted-by":"publisher","first-page":"3808","DOI":"10.1182\/blood-2011-08-371062","volume":"119","author":"L Gong","year":"2012","unstructured":"Gong L, Maiteki-Sebuguzi C, Rosenthal PJ, Hubbard AE, Drakeley CJ, Dorsey G, et al. Evidence for both innate and acquired mechanisms of protection from Plasmodium falciparum in children with sickle cell trait. Blood. 2012;119:3808\u201314.","journal-title":"Blood"},{"key":"3347_CR15","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1186\/s12936-017-1778-z","volume":"16","author":"M Maziarz","year":"2017","unstructured":"Maziarz M, Kinyera T, Otim I, Kagwa P, Nabalende H, Legason ID, et al. Age and geographic patterns of Plasmodium falciparum malaria infection in a representative sample of children living in Burkitt lymphoma-endemic areas of northern Uganda. Malar J. 2017;16:124.","journal-title":"Malar J."},{"key":"3347_CR16","doi-asserted-by":"publisher","first-page":"1373","DOI":"10.1038\/s41467-017-01352-3","volume":"8","author":"JD Challenger","year":"2017","unstructured":"Challenger JD, Bruxvoort K, Ghani AC, Okell LC. Assessing the impact of imperfect adherence to artemether-lumefantrine on malaria treatment outcomes using within-host modelling. Nat Commun. 2017;8:1373.","journal-title":"Nat Commun."},{"key":"3347_CR17","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1186\/1475-2875-13-267","volume":"13","author":"O Minzi","year":"2014","unstructured":"Minzi O, Maige S, Sasi P, Ngasala B. Adherence to artemether-lumefantrine drug combination: a rural community experience 6 years after change of malaria treatment policy in Tanzania. Malar J. 2014;13:267.","journal-title":"Malar J."},{"key":"3347_CR18","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/1475-2875-13-7","volume":"13","author":"K Banek","year":"2014","unstructured":"Banek K, Lalani M, Staedke S, Chandramohan D. Adherence to artemisinin-based combination therapy for the treatment of malaria: a systematic review of the evidence. Malar J. 2014;13:7.","journal-title":"Malar J."},{"key":"3347_CR19","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1186\/1475-2875-6-131","volume":"6","author":"DL Smith","year":"2007","unstructured":"Smith DL, Guerra CA, Snow RW, Hay SI. Standardizing estimates of the Plasmodium falciparum parasite rate. Malar J. 2007;6:131.","journal-title":"Malar J."},{"key":"3347_CR20","volume-title":"Larval source management\u2014a supplementary measure for malaria vector control: an operational manual","author":"WHO","year":"2013","unstructured":"WHO. Larval source management\u2014a supplementary measure for malaria vector control: an operational manual. Geneva: World Health Organization; 2013."},{"key":"3347_CR21","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1186\/s12936-015-0986-7","volume":"14","author":"P Ncogo","year":"2015","unstructured":"Ncogo P, Herrador Z, Romay-Barja M, Garcia-Carrasco E, Nseng G, Berzosa P, et al. Malaria prevalence in Bata district, Equatorial Guinea: a cross-sectional study. Malar J. 2015;14:456.","journal-title":"Malar J."},{"key":"3347_CR22","doi-asserted-by":"publisher","first-page":"2332","DOI":"10.1038\/s41467-019-10339-1","volume":"10","author":"CA Guerra","year":"2019","unstructured":"Guerra CA, Kang SY, Citron DT, Hergott DEB, Perry M, Smith J, et al. Human mobility patterns and malaria importation on Bioko Island. Nat Commun. 2019;10:2332.","journal-title":"Nat Commun."},{"key":"3347_CR23","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1186\/s12936-019-3078-2","volume":"18","author":"CA Guerra","year":"2019","unstructured":"Guerra CA, Citron DT, Garc\u00eda GA, Smith DL. Characterising malaria connectivity using malaria indicator survey data. Malar J. 2019;18:440.","journal-title":"Malar J."},{"key":"3347_CR24","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1186\/s12936-015-0579-5","volume":"14","author":"J Bradley","year":"2015","unstructured":"Bradley J, Monti F, Rehman AM, Schwabe C, Vargas D, Garcia G, et al. Infection importation: a key challenge to malaria elimination on Bioko Island, Equatorial Guinea. Malar J. 2015;14:46.","journal-title":"Malar J."},{"key":"3347_CR25","unstructured":"The Government of Equatorial Guinea, Medical Care Development International. Bioko Island Malaria Control Project & Equatorial Guinea Malaria Vaccine Initiative. Quarterly Progress Report and Annual Review\u2013October\u2013December 2018. MCDI, 2018."},{"key":"3347_CR26","unstructured":"The Government of Equatorial Guinea, Medical Care Development International. The Bioko Island Malaria Elimination Project Annual Malaria Indicator Survey 2019. MCDI, 2019."},{"key":"3347_CR27","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1186\/s12936-016-1286-6","volume":"15","author":"JI Meyers","year":"2016","unstructured":"Meyers JI, Pathikonda S, Popkin-Hall ZR, Medeiros MC, Fuseini G, Matias A, et al. Increasing outdoor host-seeking in Anopheles gambiae over 6\u00a0years of vector control on Bioko Island. Malar J. 2016;15:239.","journal-title":"Malar J."}],"container-title":["Malaria Journal"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12936-020-03347-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s12936-020-03347-w\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s12936-020-03347-w.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,2]],"date-time":"2021-08-02T19:45:23Z","timestamp":1627933523000},"score":1,"resource":{"primary":{"URL":"https:\/\/malariajournal.biomedcentral.com\/articles\/10.1186\/s12936-020-03347-w"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,3]]},"references-count":27,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2020,12]]}},"alternative-id":["3347"],"URL":"https:\/\/doi.org\/10.1186\/s12936-020-03347-w","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-32062\/v1","asserted-by":"object"},{"id-type":"doi","id":"10.21203\/rs.3.rs-32062\/v2","asserted-by":"object"},{"id-type":"doi","id":"10.21203\/rs.3.rs-32062\/v3","asserted-by":"object"}]},"ISSN":["1475-2875"],"issn-type":[{"value":"1475-2875","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,3]]},"assertion":[{"value":"27 May 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"25 July 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 August 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"All surveys conducted on Bioko Island are approved by the ethics committee of the Ministry of Health and Social Welfare of Equatorial Guinea.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"277"}}