{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T23:01:34Z","timestamp":1791068494427,"version":"4.1.0"},"reference-count":70,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,9,29]],"date-time":"2021-09-29T00:00:00Z","timestamp":1632873600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Med."],"abstract":"<jats:p>Successful malaria control interventions, mostly based on the training of health workers, distribution of insecticide-treated nets, and spraying, decrease malaria incidence; however, when these interventions are interrupted, a resurgence may occur. In the Peruvian Amazon, after discontinuing the control activities implemented by the PAMAFRO project (2006\u20132010)-a Global Fund-sponsored project for the strengthening of malaria control and surveillance in multiple countries in Latin America\u2013 malaria cases re-emerged dramatically. In parallel, meteorological factors determine the conditions suitable for the development, reproduction, and survival of mosquito vectors and parasites. This study hypothesized that interruption of malaria interventions may have modified the meteorological-malaria relationships over time (i.e., temporal changes in the dose-response between meteorological variables and malaria incidence). In this panel data analysis, we assessed the extent that relationships between meteorological variables and malaria changed temporally using data of monthly malaria incidence due to <jats:italic>Plasmodium vivax<\/jats:italic> or <jats:italic>P. falciparum<\/jats:italic> in Loreto, Peru (2000\u20132017). Generalized additive models were used to explore how the effects of meteorological variables changed in magnitude before, during, and after the PAMAFRO intervention. We found that once the PAMAFRO intervention had been interrupted, the estimated effects (dose-response) of meteorological variables on incidence rates decreased for both malaria parasite species. However, these fitted effect estimates did not reach their baseline levels (before the PAMAFRO period); variations of time-varying slopes between 0.45 and 2.07 times were observed after the PAMAFRO intervention. We also reported significant heterogeneity in the geographical distributions of malaria, parasite species, and meteorological variables. High malaria transmission occurred consistently in the northwestern provinces of Loreto Department. Since the end of the PAMAFRO period, a higher effect of precipitation and actual evapotranspiration was described on <jats:italic>P. falciparum<\/jats:italic> compared to <jats:italic>P. vivax<\/jats:italic>. The effect of temperature on malaria was greater over a shorter time (1-month lag or less), compared with precipitation and actual evapotranspiration (12-month lag). These findings demonstrate the importance of sustained malaria control efforts since interruption may enhance the links between meteorological factors and malaria. Our results also emphasize the importance of considering the time-varying effect of meteorological factors on malaria incidence to tailor control interventions, especially to better manage the current and future climate change crisis.<\/jats:p>","DOI":"10.3389\/fmed.2021.721515","type":"journal-article","created":{"date-parts":[[2021,9,29]],"date-time":"2021-09-29T04:45:58Z","timestamp":1632890758000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":15,"title":["Time-Varying Effects of Meteorological Variables on Malaria Epidemiology in the Context of Interrupted Control Efforts in the Amazon Rainforest, 2000\u20132017"],"prefix":"10.3389","volume":"8","author":[{"given":"Gabriel","family":"Carrasco-Escobar","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jazmin","family":"Qquellon","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diego","family":"Villa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renato","family":"Cava","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alejandro","family":"Llanos-Cuentas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tarik","family":"Benmarhnia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,9,29]]},"reference":[{"key":"B1","unstructured":"World Malaria Report 20202020"},{"key":"B2","unstructured":"Bolet\u00edn Epidemiol\u00f3gico del Per\u00fa - SE 422019"},{"key":"B3","doi-asserted-by":"publisher","first-page":"40350","DOI":"10.1038\/srep40350","article-title":"Spatio-temporal analysis of malaria incidence in the Peruvian Amazon Region between 2002 and 2013","volume":"7","author":"Soto-Calle","year":"2017","journal-title":"Sci Rep"},{"key":"B4","doi-asserted-by":"publisher","first-page":"133","DOI":"10.4269\/ajtmh.16-0268","article-title":"Epidemiology of Plasmodium vivax malaria in Peru","volume":"95","author":"Rosas-Aguirre","year":"2016","journal-title":"Am J Trop Med Hyg"},{"key":"B5","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1186\/1475-2875-8-142","article-title":"The spatial and temporal patterns of falciparum and vivax malaria in Peru: 1994\u20132006","volume":"8","author":"Chowell","year":"2009","journal-title":"Malar J"},{"key":"B6","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1590\/S1726-46342011000200009","article-title":"Long-lasting insecticide - treated bednet ownership, retention and usage one year after their distribution in Loreto, Peru","volume":"28","author":"Rosas-Aguirre","year":"2011","journal-title":"Rev Peru Med Exp Salud Publica"},{"key":"B7","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1590\/S1726-46342010000400008","article-title":"Use of standardized blood smear slide sets for competency assessment in the malaria microscopic diagnosis in the Peruvian Amazon","volume":"27","author":"Rosas-Aguirre","year":"2010","journal-title":"Rev Peru Med Exp Salud Publica"},{"key":"B8","unstructured":"Rosas-AguirreA\n          Understanding transmission dynamics for malaria control and elimination in peru [Doctoral Dissertation]2015"},{"key":"B9","doi-asserted-by":"publisher","first-page":"e0137458","DOI":"10.1371\/journal.pone.0137458","article-title":"Hotspots of malaria transmission in the Peruvian amazon: rapid assessment through a parasitological and serological survey","volume":"10","author":"Rosas-Aguirre","year":"2015","journal-title":"PLoS ONE"},{"key":"B10","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1186\/s13071-016-1693-0","article-title":"The relative contribution of climate variability and vector control coverage to changes in malaria parasite prevalence in Zambia 2006\u20132012","volume":"9","author":"Bennett","year":"2016","journal-title":"Parasit Vectors"},{"key":"B11","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1186\/1475-2875-10-46","article-title":"Reductions in malaria and anaemia case and death burden at hospitals following scale-up of malaria control in Zanzibar, 1999\u20132008","volume":"10","author":"Aregawi","year":"2011","journal-title":"Malar J"},{"key":"B12","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/j.actatropica.2011.06.012","article-title":"Malaria epidemiology and control in Southern Africa","volume":"121","author":"Mharakurwa","year":"2012","journal-title":"Acta Trop"},{"key":"B13","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1186\/s12879-020-05086-4","article-title":"Resurgence risk for malaria, and the characterization of a recent outbreak in an Amazonian border area between French Guiana and Brazil","volume":"20","author":"Mosnier","year":"2020","journal-title":"BMC Infect Dis"},{"key":"B14","doi-asserted-by":"publisher","first-page":"135","DOI":"10.3389\/fenvs.2020.00135","article-title":"The relative role of climate variation and control interventions on malaria elimination efforts in El Oro, Ecuador: a modeling study","volume":"8","author":"Fletcher","year":"2020","journal-title":"Front Environ Sci"},{"key":"B15","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1186\/s40249-018-0460-1","article-title":"Climate drivers of vector-borne diseases in Africa and their relevance to control programmes","volume":"7","author":"Thomson","year":"2018","journal-title":"Infect Dis Poverty"},{"key":"B16","doi-asserted-by":"publisher","first-page":"a025601","DOI":"10.1101\/cshperspect.a025601","article-title":"Malaria transmission and prospects for malaria eradication: the role of the environment","volume":"7","author":"Castro","year":"2017","journal-title":"Cold Spring Harb Perspect Med"},{"key":"B17","doi-asserted-by":"publisher","first-page":"110038","DOI":"10.1016\/j.envres.2020.110038","article-title":"Environmental drivers, climate change and emergent diseases transmitted by mosquitoes and their vectors in southern Europe: a systematic review","volume":"191","author":"Brugueras","year":"2020","journal-title":"Environ Res"},{"key":"B18","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1186\/s13071-015-1053-5","article-title":"Larval and adult environmental temperatures influence the adult reproductive traits of Anopheles gambiae s.s","volume":"8","author":"Christiansen-Jucht","year":"2015","journal-title":"Parasit Vect"},{"key":"B19","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1186\/1475-2875-11-271","article-title":"Modeling the role of environmental variables on the population dynamics of the malaria vector Anopheles gambiae sensu stricto","volume":"11","author":"Parham","year":"2012","journal-title":"Malar J"},{"key":"B20","doi-asserted-by":"publisher","first-page":"1146","DOI":"10.1371\/journal.pone.0001146","article-title":"Unexpected high losses of Anopheles gambiae larvae due to rainfall","volume":"2","author":"Paaijmans","year":"2007","journal-title":"PLoS ONE"},{"key":"B21","doi-asserted-by":"publisher","first-page":"7","DOI":"10.1186\/1476-072X-6-7","article-title":"Habitat suitability mapping of Anopheles darlingi in the surroundings of the Manso hydropower plant reservoir, Mato Grosso, Central Brazil","volume":"6","author":"Zeilhofer","year":"2007","journal-title":"Int J Health Geogr"},{"key":"B22","doi-asserted-by":"publisher","first-page":"e0211258","DOI":"10.1371\/journal.pone.0211258","article-title":"Predicting the direct and indirect impacts of climate change on malaria in coastal Kenya","volume":"14","author":"Le","year":"2019","journal-title":"PLoS ONE"},{"key":"B23","first-page":"93","article-title":"Climate, environment and transmission of malaria","volume":"24","author":"Rossati","year":"2016","journal-title":"Infez Med"},{"key":"B24","doi-asserted-by":"publisher","first-page":"5635","DOI":"10.1073\/pnas.0601493103","article-title":"Malaria risk and temperature: influences from global climate change and local land use practices","volume":"103","author":"Patz","year":"2006","journal-title":"Proc Natl Acad Sci USA."},{"key":"B25","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1186\/s12936-015-0630-6","article-title":"Malaria incidence from 2005\u20132013 and its associations with meteorological factors in Guangdong, China","volume":"14","author":"Guo","year":"2015","journal-title":"Malar J"},{"key":"B26","doi-asserted-by":"publisher","first-page":"20160048","DOI":"10.1098\/rspb.2016.0048","article-title":"Variation in relapse frequency and the transmission potential of Plasmodium vivax malaria","volume":"283","author":"White","year":"2016","journal-title":"Proc R Soc B Biol Sci"},{"key":"B27","doi-asserted-by":"publisher","first-page":"244","DOI":"10.1093\/femsle\/fnx244","article-title":"Vector-borne diseases and climate change: a European perspective","volume":"365","author":"Semenza","year":"2018","journal-title":"FEMS Microbiol Lett"},{"key":"B28","doi-asserted-by":"publisher","first-page":"560","DOI":"10.4103\/ijmr.IJMR_933_17","article-title":"Early warning systems for the detection of malaria outbreaks","volume":"146","author":"Maharaj","year":"2017","journal-title":"Indian J Med Res"},{"key":"B29","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1186\/1475-2875-3-44","article-title":"Weather-based prediction of Plasmodium falciparum malaria in epidemic-prone regions of Ethiopia II. Weather-based prediction systems perform comparably to early detection systems in identifying times for interventions","volume":"3","author":"Teklehaimanot","year":"2004","journal-title":"Malar J"},{"key":"B30","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1093\/biostatistics\/kxs052","article-title":"Capturing the time-varying drivers of an epidemic using stochastic dynamical systems","volume":"14","author":"Dureau","year":"2013","journal-title":"Biostatistics"},{"key":"B31","unstructured":"Reporte regional de indicadores sociales del departamento de Loreto2020"},{"key":"B32","unstructured":"Compendio Estad\u00edstico: Loreto 20172017"},{"key":"B33","unstructured":"Poblaci\u00f3n afiliada a alg\u00fan seguro de salud2018"},{"key":"B34","doi-asserted-by":"publisher","first-page":"180","DOI":"10.4269\/ajtmh.13-0547","article-title":"Healthcare access and health beliefs of the indigenous peoples in remote amazonian Peru","volume":"90","author":"Brierley","year":"2014","journal-title":"Am J Trop Med Hyg"},{"key":"B35","doi-asserted-by":"publisher","first-page":"498","DOI":"10.3389\/fpubh.2020.00498","article-title":"Travel time to health facilities as a marker of geographical accessibility across heterogeneous land coverage in Peru","volume":"8","author":"Carrasco-Escobar","year":"2020","journal-title":"Front Public Health"},{"key":"B36","unstructured":"SENAMHI - Loreto2020"},{"key":"B37","unstructured":"Herramientas Para la Vigilancia Epidemiol\u00f3gica2005"},{"key":"B38","unstructured":"Directiva sanitaria N\u00b0 046 - MINSA\/DGE-V.01 de notificaci\u00f3n de enfermedades y eventos sujetos a vigilancia epidemiol\u00f3gica en salud p\u00fablica2013"},{"key":"B39","unstructured":"Manual de procedimientos de laboratorio para el diagn\u00f3stico de malaria2003"},{"key":"B40","unstructured":"Norma t\u00e9cnica de salud para la atenci\u00f3n de la malaria y malaria grave en el Per\u00fa2015"},{"key":"B41","unstructured":"Compartiendo Lecciones Aprendidas2011"},{"key":"B42","doi-asserted-by":"publisher","first-page":"170191","DOI":"10.1038\/sdata.2017.191","article-title":"TerraClimate, a high-resolution global dataset of monthly climate and climatic water balance from 1958-2015","volume":"5","author":"Abatzoglou","year":"2018","journal-title":"Sci Data"},{"key":"B43","doi-asserted-by":"publisher","first-page":"456","DOI":"10.3389\/fpsyg.2017.00456","article-title":"Repeated measures correlation","volume":"8","author":"Bakdash","year":"2017","journal-title":"Front Psychol"},{"key":"B44","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1111\/j.1467-9868.2010.00749.x","article-title":"Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models","volume":"73","author":"Wood","year":"2011","journal-title":"J R Stat Soc Ser B (Statistical Methodol"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1201\/9781315370279","author":"Wood","year":"2017","journal-title":"Generalized Additive Models: An Introduction With R"},{"key":"B46","doi-asserted-by":"publisher","first-page":"27","DOI":"10.4269\/ajtmh.13-0363","article-title":"Implementation of malaria dynamic models in municipality level early warning systems in Colombia. Part I: description of study sites","volume":"91","author":"Ruiz","year":"2014","journal-title":"Am J Trop Med Hyg"},{"key":"B47","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1186\/1475-2875-10-297","article-title":"Determinants of relapse periodicity in Plasmodium vivax malaria","volume":"10","author":"White","year":"2011","journal-title":"Malar J"},{"key":"B48","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1186\/1756-3305-6-357","article-title":"Impact of climate variability on Plasmodium vivax and Plasmodium falciparum malaria in Yunnan Province, China","volume":"6","author":"Bi","year":"2013","journal-title":"Parasit Vectors."},{"key":"B49","doi-asserted-by":"publisher","first-page":"4","DOI":"10.4269\/ajtmh.16-0160","article-title":"Implications of Plasmodium vivax biology for control, elimination, and research","volume":"95","author":"Olliaro","year":"2016","journal-title":"Am J Trop Med Hyg"},{"key":"B50","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1186\/s12936-018-2342-1","article-title":"Microclimate variables of the ambient environment deliver the actual estimates of the extrinsic incubation period of Plasmodium vivax and Plasmodium falciparum: a study from a malaria-endemic urban setting, Chennai in India","volume":"17","author":"Thomas","year":"2018","journal-title":"Malar J"},{"key":"B51","doi-asserted-by":"publisher","first-page":"17882","DOI":"10.1038\/s41598-019-53838-3","article-title":"Malaria predictions based on seasonal climate forecasts in South Africa: a time series distributed lag nonlinear model","volume":"9","author":"Kim","year":"2019","journal-title":"Sci Rep"},{"key":"B52","volume-title":"Essential Malariology","author":"Warrell","year":"2002"},{"key":"B53","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1007\/s10393-017-1307-0","article-title":"Evaluating efficacy of landsat-derived environmental covariates for predicting malaria distribution in rural villages of Vhembe District, South Africa","volume":"15","author":"Malahlela","year":"2018","journal-title":"Ecohealth"},{"key":"B54","doi-asserted-by":"publisher","first-page":"e170","DOI":"10.1017\/S0950268819000608","article-title":"Lag effect of climatic variables on dengue burden in India","volume":"147","author":"Kakarla","year":"2019","journal-title":"Epidemiol Infect"},{"key":"B55","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1007\/s42398-019-00078-w","article-title":"Impact of climate change on agriculture production and its sustainable solutions","volume":"2","author":"Arora","year":"2019","journal-title":"Environ Sustain"},{"key":"B56","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1186\/s13071-015-1033-9","article-title":"Predicting potential ranges of primary malaria vectors and malaria in northern South America based on projected changes in climate, land cover and human population","volume":"8","author":"Alimi","year":"2015","journal-title":"Parasit Vectors"},{"key":"B57","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1186\/s12942-018-0122-3","article-title":"Spatial panorama of malaria prevalence in Africa under climate change and interventions scenarios","volume":"17","author":"Moukam Kakmeni","year":"2018","journal-title":"Int J Health Geogr"},{"key":"B58","doi-asserted-by":"publisher","first-page":"e0129869","DOI":"10.1371\/journal.pone.0129869","article-title":"Climate change and spatiotemporal distributions of vector-borne diseases in Nepal - A systematic synthesis of literature","volume":"10","author":"Dhimal","year":"2015","journal-title":"PLoS ONE"},{"key":"B59","doi-asserted-by":"publisher","first-page":"342","DOI":"10.1038\/nature09098","article-title":"Climate change and the global malaria recession","volume":"465","author":"Gething","year":"2010","journal-title":"Nature"},{"key":"B60","doi-asserted-by":"publisher","first-page":"1096","DOI":"10.4081\/jphia.2020.1096","article-title":"Modelling malaria reduction in a highly endemic country: Evidence from household survey, climate, and programme data in Zambia","volume":"11","author":"Nawa","year":"2020","journal-title":"J Public Health Afr"},{"key":"B61","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1186\/1475-2875-11-122","article-title":"Malaria resurgence: a systematic review and assessment of its causes","volume":"11","author":"Cohen","year":"2012","journal-title":"Malar J"},{"key":"B62","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1093\/cid\/cix251","article-title":"Resurgence of malaria following discontinuation of indoor residual spraying of insecticide in an area of Uganda with previously high-transmission intensity","volume":"65","author":"Raouf","year":"2017","journal-title":"Clin Infect Dis"},{"key":"B63","doi-asserted-by":"publisher","first-page":"e149","DOI":"10.1016\/S1473-3099(18)30757-6","article-title":"Venezuela's humanitarian crisis, resurgence of vector-borne diseases, and implications for spillover in the region","volume":"19","author":"Grillet","year":"2019","journal-title":"Lancet Infect Dis"},{"key":"B64","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1186\/s12936-021-03668-4","article-title":"Cross-border malaria in Northern Brazil","volume":"20","author":"Arisco","year":"2021","journal-title":"Malar J"},{"key":"B65","doi-asserted-by":"publisher","first-page":"593","DOI":"10.1186\/s12936-016-1635-5","article-title":"The economics of malaria control and elimination: a systematic review","volume":"15","author":"Shretta","year":"2016","journal-title":"Malar J"},{"key":"B66","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1186\/s12936-017-2019-1","article-title":"Maximizing the impact of malaria funding through allocative efficiency: using the right interventions in the right locations","volume":"16","author":"Scott","year":"2017","journal-title":"Malar J"},{"key":"B67","doi-asserted-by":"publisher","first-page":"238","DOI":"10.3389\/fpubh.2016.00238","article-title":"Effect of deforestation and land use changes on mosquito productivity and development in western Kenya highlands: Implication for malaria risk","volume":"4","author":"Kweka","year":"2016","journal-title":"Front Public Health"},{"key":"B68","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1093\/jme\/tjaa137","article-title":"The effects of high-altitude windborne migration on survival, oviposition, and blood-feeding of the African malaria mosquito, Anopheles gambiae s.l. (Diptera: Culicidae)","volume":"58","author":"Sanogo","year":"2020","journal-title":"J Med Entomol"},{"key":"B69","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1080\/14787210.2019.1693259","article-title":"Asymptomatic malaria in the clinical and public health context","volume":"17","author":"Cheaveau","year":"2019","journal-title":"Expert Rev Anti Infect Ther"},{"key":"B70","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1186\/s12936-018-2197-5","article-title":"Modelling and observing the role of wind in Anopheles population dynamics around a reservoir","volume":"17","author":"Endo","year":"2018","journal-title":"Malar J"}],"container-title":["Frontiers in Medicine"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2021.721515\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,29]],"date-time":"2021-09-29T04:46:25Z","timestamp":1632890785000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2021.721515\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,9,29]]},"references-count":70,"alternative-id":["10.3389\/fmed.2021.721515"],"URL":"https:\/\/doi.org\/10.3389\/fmed.2021.721515","relation":{},"ISSN":["2296-858X"],"issn-type":[{"value":"2296-858X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,9,29]]},"article-number":"721515"}}