{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,18]],"date-time":"2025-12-18T19:58:19Z","timestamp":1766087899086,"version":"build-2065373602"},"reference-count":54,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2022,5,19]],"date-time":"2022-05-19T00:00:00Z","timestamp":1652918400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>The characteristics of P. vivax recurrent episodes were examined using a centralized secondary source of malaria records in Nicaragua and in the two most affected municipalities in the RACCN. The study of 36,787 malaria cases due to P. vivax or P. falciparum revealed that, nationwide, 3624 patients had at least one recurrent infection. This was achieved by matching names, gender, age, community\/municipality, ethnicity, etc. P. vivax was responsible for 88% of recurrent infections of 25\u2013450 days of latency (51.9% were women and 48.1% were men), and these were assumed to be relapse episodes. Of them, 88.2% and 4.4% occurred in the municipalities of Puerto Cabezas and Rosita, respectively. The proportion of P. vivax patients having presumed relapse episodes rose with elevated transmission rates in both municipalities, reaching 7% in Rosita (2017) and 14.5% in Puerto Cabezas (2018). In both areas, relapse episodes were evident over time and were characterized by the production of a continuous stippling pattern with a slope evolving from one transmission peak to the next. During the dry season, short-latency relapse episodes were more robust, while long-latency ones increased just before the P. vivax transmission season began, with a high proportion of long-latency relapses during this period. The abundance of recurrent P. vivax infections, the wide range of relapse latency lengths, and temporal distribution tended to favor year-round transmission. It is necessary to evaluate compliance with and the effectiveness of primaquine treatment and contemplate the use of an alternative drug, among other actions.<\/jats:p>","DOI":"10.3390\/ijerph19106195","type":"journal-article","created":{"date-parts":[[2022,5,19]],"date-time":"2022-05-19T12:25:57Z","timestamp":1652963157000},"page":"6195","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Recurrent Plasmodium vivax Cases of Both Short and Long Latency Increased with Transmission Intensity and Were Distributed Year-Round in the Most Affected Municipalities of the RACCN, Nicaragua, 2013\u20132018"],"prefix":"10.3390","volume":"19","author":[{"given":"Aida M.","family":"Soto","sequence":"first","affiliation":[{"name":"Centre for Research and Health Studies, National Autonomous University of Nicaragua, Managua 11095, Nicaragua"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2347-5581","authenticated-orcid":false,"given":"Lilia","family":"Gonz\u00e1lez-Cer\u00f3n","sequence":"additional","affiliation":[{"name":"Regional Centre of Research in Public Health, National Institute for Public Health, Tapachula 30700, Chiapas, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Frida","family":"Santill\u00e1n-Valenzuela","sequence":"additional","affiliation":[{"name":"Regional Centre of Research in Public Health, National Institute for Public Health, Tapachula 30700, Chiapas, Mexico"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mar\u00eda E.","family":"Parrales","sequence":"additional","affiliation":[{"name":"Malaria Component, Ministry of Health, Managua 11165, Nicaragua"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alberto","family":"Montoya","sequence":"additional","affiliation":[{"name":"Parasitology Department, National Centre for Diagnosis and Reference, Ministry of Health, Managua 11165, Nicaragua"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"17","DOI":"10.4269\/ajtmh.17-0869","article-title":"Malaria Elimination: Time to Target All Species","volume":"99","author":"Lover","year":"2018","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1186\/1475-2875-13-144","article-title":"Geographical variation in Plasmodium vivax relapse","volume":"13","author":"Battle","year":"2014","journal-title":"Malar. J."},{"key":"ref_3","unstructured":"WHO (2022, May 16). Guidelines for the Treatment of Malaria, Available online: https:\/\/www.ncbi.nlm.nih.gov\/books\/NBK294440\/."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"15","DOI":"10.4269\/ajtmh.16-0141","article-title":"Global Epidemiology of Plasmodium vivax","volume":"95","author":"Howes","year":"2016","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_5","unstructured":"WHO (2022, May 16). Guidelines for Malaria. Available online: https:\/\/apps.who.int\/iris\/handle\/10665\/343751."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"466","DOI":"10.4269\/ajtmh.1978.27.466","article-title":"Field evaluation of primaquine in the control of Plasmodium vivax","volume":"27","author":"Cedillos","year":"1978","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"581","DOI":"10.4269\/ajtmh.1975.24.581","article-title":"Patterns of Plasmodium vivax recurrence in a high-incidence coastal area of El Salvador, C.A","volume":"24","author":"Mason","year":"1975","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1186\/1756-3305-6-109","article-title":"Molecular and epidemiological characterization of Plasmodium vivax recurrent infections in southern Mexico","volume":"6","author":"Mu","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1186\/s12936-015-0938-2","article-title":"Effectiveness of combined chloroquine and primaquine treatment in 14 days versus intermittent single dose regimen, in an open, non-randomized, clinical trial, to eliminate Plasmodium vivax in southern Mexico","volume":"14","author":"Rodriguez","year":"2015","journal-title":"Malar. J."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"707","DOI":"10.4269\/ajtmh.1972.21.707","article-title":"Studies on the characterization of Plasmodium vivax strains from Central America","volume":"21","author":"Contacos","year":"1972","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_11","unstructured":"WHO (2022, May 16). World Malaria Report. Available online: https:\/\/www.who.int\/teams\/global-malaria-programme\/reports\/world-malaria-report-2021."},{"key":"ref_12","unstructured":"WHO (2022, May 16). World Malaria Report. Available online: https:\/\/www.who.int\/publications\/i\/item\/9789241565721."},{"key":"ref_13","unstructured":"PAHO (2022, May 16). Report on the Situation of Malaria in the Americas. Available online: https:\/\/www3.paho.org\/hq\/index.php?option=com_docman&view=download&category_slug=datos-estadisticos-mapas-8110&alias=48336-situation-of-malaria-in-the-region-of-the-americas-2017-1&Itemid=270&lang=es."},{"key":"ref_14","unstructured":"BANCO MUNDIAL (2022, May 16). Poblaci\u00f3n Total Nicaragua. Available online: https:\/\/datos.bancomundial.org\/indicador\/SP.POP.TOTL?locations=NI."},{"key":"ref_15","unstructured":"Gobierno de Nicaragua (2022, May 16). Perfil Demogr\u00e1fico Nicaragua. Available online: https:\/\/pronicaragua.gob.ni\/media\/publications\/Perfil_Demografico_2020_PWsyOuB.pdf."},{"key":"ref_16","unstructured":"(2022, May 16). Plan Nacional de Nicaragua en el Marco del Plan Mesoamericano Para Mejorar el Control de la Malaria Hacia su Eliminaci\u00f3n. Available online: http:\/\/www.proyectomesoamerica.org:8088\/smsp\/phocadownload\/Institucional\/PlanesNacionales\/PNMalaria\/NIC%20PN%20Malaria.pdf."},{"key":"ref_17","unstructured":"(1996). Biolog\u00eda y Ecolog\u00eda de Anopheles albimanus Wiedemann en Centroam\u00e9rica. Bol. Oficina Sanit. Panam., 121, 32."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1186\/1756-3305-3-72","article-title":"The dominant Anopheles vectors of human malaria in the Americas: Occurrence data, distribution maps and bionomic precis","volume":"3","author":"Sinka","year":"2010","journal-title":"Parasites Vectors"},{"key":"ref_19","unstructured":"Sequeira, M.E.H., Amador, J.J., Domingo, G., Quintanilla, M., and de los Santos, T. (2022, May 16). Malaria in Nicaragua: A Review of Control Status, Trends, and Needs. Available online: https:\/\/path.azureedge.net\/media\/documents\/TS_nicaragua_malaria_rpt.pdf."},{"key":"ref_20","first-page":"605","article-title":"Relationship between malarial parasitaemia and symptoms of the disease: A review of the literature","volume":"22","author":"Covell","year":"1960","journal-title":"Bull. World Health Organ."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4271","DOI":"10.1128\/AAC.48.11.4271-4280.2004","article-title":"In vivo assessment of drug efficacy against Plasmodium falciparum malaria: Duration of follow-up","volume":"48","author":"Stepniewska","year":"2004","journal-title":"Antimicrob. Agents. Chemother."},{"key":"ref_22","first-page":"CD004389","article-title":"Primaquine for preventing relapse in people with Plasmodium vivax malaria treated with chloroquine","volume":"10","author":"Galappaththy","year":"2013","journal-title":"Cochrane Database Syst. Rev."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"133","DOI":"10.2310\/7060.2005.12306","article-title":"Adequate primaquine for vivax malaria","volume":"12","author":"Kitchener","year":"2005","journal-title":"J. Travel. Med."},{"key":"ref_24","first-page":"174","article-title":"Primaquine and relapses of Plasmodium vivax. Meta analysis of controlled clinical trials","volume":"18","year":"2015","journal-title":"Rev. Bras. Epidemiol."},{"key":"ref_25","unstructured":"Ministerio de Salud (2022, May 16). Esquema Nacional de Tratamiento de Malaria. Available online: https:\/\/www.paho.org\/es\/documentos\/esquema-nacional-tratamiento-malaria-miniosterio-salud-nicaragua-2014."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"889","DOI":"10.4269\/ajtmh.2009.80.889","article-title":"The participation of secondary clinical episodes in the epidemiology of vivax malaria during pre- and post-implementation of focal control in the state of Oaxaca, Mexico","volume":"80","author":"Rodriguez","year":"2009","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Hurtado, L.A., Rigg, C.A., Calzada, J.E., Dutary, S., Bernal, D., Koo, S.I., and Chaves, L.F. (2018). Population Dynamics of Anopheles albimanus (Diptera: Culicidae) at Ipeti-Guna, a Village in a Region Targeted for Malaria Elimination in Panama. Insects, 9.","DOI":"10.3390\/insects9040164"},{"key":"ref_28","first-page":"168","article-title":"Estimating the relapse risk of Plasmodium vivax in Iran under national chemotherapy scheme using a novel method","volume":"43","author":"Haghdoost","year":"2006","journal-title":"J. Vector. Borne Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1186\/s12936-021-03886-w","article-title":"Development of weight and age-based dosing of daily primaquine for radical cure of vivax malaria","volume":"20","author":"Taylor","year":"2021","journal-title":"Malar. J."},{"key":"ref_30","first-page":"3","article-title":"Primaquine double dose for 7 days is inferior to single-dose treatment for 14 days in preventing Plasmodium vivax recurrent episodes in Suriname","volume":"11","author":"Adhin","year":"2018","journal-title":"Infect. Drug Resist."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"961","DOI":"10.4269\/ajtmh.2009.09-0337","article-title":"Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia","volume":"81","author":"Ferreira","year":"2009","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1403","DOI":"10.1590\/0102-311X00169312","article-title":"Factors associated with recurrent Plasmodium vivax malaria in Porto Velho, Rond\u00f4nia State, Brazil, 2009","volume":"30","author":"Rodrigues","year":"2014","journal-title":"Cad. Saude Publica"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1186\/s12936-019-2644-y","article-title":"Evaluation of Plasmodium vivax malaria recurrence in Brazil","volume":"18","author":"Daher","year":"2019","journal-title":"Malar. J."},{"key":"ref_34","unstructured":"PAHO Malaria Technical Advisory Group (2022, May 16). Strategies to Decrease Relapses in P. vivax Cases. Available online: https:\/\/www3.paho.org\/hq\/index.php?option=com_docman&view=download&slug=malaria-technical-group-session-6-strategy-for-reducing-the-relapses-of-p-vivax-for-the-control-and-elimination-of-malaria-in-the-americas&Itemid=270&lang=es."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/B978-0-12-407826-0.00003-5","article-title":"Natural acquisition of immunity to Plasmodium vivax: Epidemiological observations and potential targets","volume":"81","author":"Mueller","year":"2013","journal-title":"Adv. Parasitol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"997","DOI":"10.4269\/ajtmh.2007.76.997","article-title":"The risk of malarial infections and disease in Papua New Guinean children","volume":"76","author":"Michon","year":"2007","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"642","DOI":"10.4269\/ajtmh.2004.70.642","article-title":"A retrospective examination of reinfection of humans with Plasmodium vivax","volume":"70","author":"Collins","year":"2004","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1590\/S0074-02762008000700007","article-title":"Asymptomatic Plasmodium spp. infection in Tierralta, Colombia","volume":"103","author":"Cucunuba","year":"2008","journal-title":"Mem. Inst. Oswaldo Cruz."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1415","DOI":"10.1016\/S0140-6736(99)00941-1","article-title":"Symptomless Plasmodium vivax infections in native Amazonians","volume":"353","author":"Camargo","year":"1999","journal-title":"Lancet"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.pt.2014.02.004","article-title":"The role of submicroscopic parasitemia in malaria transmission: What is the evidence?","volume":"30","author":"Lin","year":"2014","journal-title":"Trends. Parasitol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"413","DOI":"10.2174\/138945007780058997","article-title":"Purine nucleoside phosphorylase: A potential target for the development of drugs to treat T-cell- and apicomplexan parasite-mediated diseases","volume":"8","author":"Silva","year":"2007","journal-title":"Curr. Drug Targets"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1016\/j.meegid.2015.08.040","article-title":"Genetic structure of Plasmodium vivax in Nicaragua, a country in the control phase, based on the carboxyl terminal region of the merozoite surface protein-1","volume":"40","author":"Gutierrez","year":"2016","journal-title":"Infect. Genet. Evol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1186\/s12936-017-1905-x","article-title":"Genetic diversity and natural selection of Plasmodium vivax multi-drug resistant gene (pvmdr1) in Mesoamerica","volume":"16","author":"Montoya","year":"2017","journal-title":"Malar. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1093\/cid\/ciq249","article-title":"Plasmodium vivax recurrence following falciparum and mixed species malaria: Risk factors and effect of antimalarial kinetics","volume":"52","author":"Douglas","year":"2011","journal-title":"Clin. Infect. Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1093\/infdis\/jiz052","article-title":"Plasmodium vivax Relapse Rates Following Plasmodium falciparum Malaria Reflect Previous Transmission Intensity","volume":"220","author":"Ashley","year":"2019","journal-title":"J. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.4269\/ajtmh.20-0186","article-title":"Estimating the Proportion of Plasmodium vivax Recurrences Caused by Relapse: A Systematic Review and Meta-Analysis","volume":"103","author":"Commons","year":"2020","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"310","DOI":"10.4269\/ajtmh.2002.66.310","article-title":"A high malaria reinfection rate in children and young adults living under a low entomological inoculation rate in a periurban area of Bamako, Mali","volume":"66","author":"Sagara","year":"2002","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1186\/1475-2875-12-354","article-title":"Genetic structure of Plasmodium falciparum populations across the Honduras-Nicaragua border","volume":"12","author":"Larranaga","year":"2013","journal-title":"Malar. J."},{"key":"ref_49","first-page":"S333","article-title":"Plan to improve malaria control towards its elimination in Mesoamerica","volume":"53","author":"Rodriguez","year":"2011","journal-title":"Salud. Publica Mex."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Balieiro, A.A.S., Siqueira, A.M., Melo, G.C., Monteiro, W.M., Sampaio, V.S., Mueller, I., Lacerda, M.V.G., and Villela, D.A.M. (2021). Short-Time Recurrences of Plasmodium vivax Malaria as a Public Health Proxy for Chloroquine-Resistance Surveillance: A Spatio-Temporal Study in the Brazilian Amazon. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph18105061"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1056\/NEJMoa1710775","article-title":"Tafenoquine versus Primaquine to Prevent Relapse of Plasmodium vivax Malaria","volume":"380","author":"Lacerda","year":"2019","journal-title":"N. Engl. J. Med."},{"key":"ref_52","unstructured":"WHO (2022, May 16). New Opportunities to Prevent Plasmodium vivax Malaria Relapse. Available online: https:\/\/www.who.int\/news\/item\/25-02-2019-new-opportunities-to-prevent-p-vivax-malaria-relapse#:~:text=For%20the%20treatment%20of%20P,a%20full%202%2Dweek%20period."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1186\/1475-2875-13-51","article-title":"Mass primaquine treatment to eliminate vivax malaria: Lessons from the past","volume":"13","author":"Kondrashin","year":"2014","journal-title":"Malar. J."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1186\/s12936-019-2907-7","article-title":"Mass drug administration should be implemented as a tool to accelerate elimination: Against","volume":"18","author":"Mendis","year":"2019","journal-title":"Malar. J."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/10\/6195\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T23:14:55Z","timestamp":1760138095000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/10\/6195"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,19]]},"references-count":54,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["ijerph19106195"],"URL":"https:\/\/doi.org\/10.3390\/ijerph19106195","relation":{},"ISSN":["1660-4601"],"issn-type":[{"type":"electronic","value":"1660-4601"}],"subject":[],"published":{"date-parts":[[2022,5,19]]}}}