Unstable Malaria Transmission in the Southern Peruvian Amazon and Its Association with Gold Mining, Madre de Dios, 2001–2012

Juan F. Sanchez Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru.

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Andres M. Carnero Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru.

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Esteban Rivera Dirección Regional de Salud de Madre de Dios, Ministerio de Salud del Perú, Puerto Maldonado, Peru.

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Luis A. Rosales Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru.

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G. Christian Baldeviano Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru.

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Jorge L. Asencios Dirección Regional de Salud de Madre de Dios, Ministerio de Salud del Perú, Puerto Maldonado, Peru.

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Kimberly A. Edgel Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru.

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Joseph M. Vinetz Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, California.

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Andres G. Lescano Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru.
School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru.

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DOI:
https://doi.org/10.4269/ajtmh.16-0030
Volume/Issue:
Volume 96: Issue 2
Page(s):
304–311
Restricted access
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The reemergence of malaria in the last decade in Madre de Dios, southern Peruvian Amazon basin, was accompanied by ecological, political, and socioeconomic changes related to the proliferation of illegal gold mining. We conducted a secondary analysis of passive malaria surveillance data reported by the health networks in Madre de Dios between 2001 and 2012. We calculated the number of cases of malaria by year, geographic location, intensity of illegal mining activities, and proximity of health facilities to the Peru–Brazil Interoceanic Highway. During 2001–2012, 203,773 febrile cases were identified in Madre de Dios, of which 30,811 (15.1%) were confirmed cases of malaria; all but 10 cases were due to Plasmodium vivax. Cases of malaria rose rapidly between 2004 and 2007, reached 4,469 cases in 2005, and then declined after 2010 to pre-2004 levels. Health facilities located in areas of intense illegal gold mining reported 30-fold more cases than those in non-mining areas (ratio = 31.54, 95% confidence interval [CI] = 19.28, 51.60). Finally, health facilities located > 1 km from the Interoceanic Highway reported significantly more cases than health facilities within this distance (ratio = 16.20, 95% CI = 8.25, 31.80). Transmission of malaria in Madre de Dios is unstable, geographically heterogeneous, and strongly associated with illegal gold mining. These findings highlight the importance of spatially oriented interventions to control malaria in Madre de Dios, as well as the need for research on malaria transmission in illegal gold mining camps.

Author Notes

* Address correspondence to Andres G. Lescano, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Avenida Honorio Delgado 430, Urbanización Ingenieria, San Martin de Porres, Lima, Peru. E-mail: andres.lescano.g@upch.pe
† These authors contributed equally to this work.

Financial support: This study was supported by U19AI089681 from NIAID (JMV) and partially funded by the Armed Forces Health Surveillance Center, Global Emerging Infections Surveillance and Response System (AFHSC/GEIS) of the U.S. Department of Defense. Lescano is sponsored by the training grant 2D43 TW007393 awarded by the Fogarty International Center of the U.S. National Institutes of Health.

Copyright statement: Several authors of this manuscript are military service members or employees of the U.S. Government. This work was prepared as part of their duties. Title 17 U.S.C. § 105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. § 101 defines a U.S. Government work as a work prepared by a military service member or employee of the U.S. Government as part of that person's official duties.

Authors' addresses: Juan F. Sanchez, Andres M. Carnero, Luis A. Rosales, G. Christian Baldeviano, and Kimberly A. Edgel, Department of Parasitology, U.S. Naval Medical Research Unit No. 6 (NAMRU-6), Lima, Peru, E-mails: chiroque@gmail.com, andrescarnero@gmail.com, larhpe@hotmail.com, geralc.baldeviano.fn@mail.mil, and kimberly.a.edgel.mil@mail.mil. Esteban Rivera and Jorge L. Asencios, Dirección Regional de Salud de Madre de Dios, Ministerio de Salud del Perú, Puerto Maldonado, Peru, E-mails: estebanriveracarrera@gmail.com and arjorgeluis@hotmail.com. Joseph M. Vinetz, Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, CA, E-mail: jvinetz@ucsd.edu. Andres G. Lescano, School of Public Health and Administration, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mail: andres.lescano.g@upch.pe.

Copyright:
© The American Society of Tropical Medicine and Hygiene 2017
Received:
10 Jan 2016
|
Accepted:
29 Sep 2016
|
Published Online:
08 Feb 2017
Cover The American Journal of Tropical Medicine and Hygiene
The American Journal of Tropical Medicine and Hygiene
Print ISSN:
0002-9637
Online ISSN:
1476-1645
  • 1.

    World Health Organization, 2013. World Malaria Report 2013. Geneva, Switzerland: WHO.

  • 2.

    Cohen JM, Smith DL, Cotter C, Ward A, Yamey G, Sabot OJ, Moonen B, 2012. Malaria resurgence: a systematic review and assessment of its causes. Malar J 11: 122.

  • 3.

    Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD, 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413–431.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Sachs J, Malaney P, 2002. The economic and social burden of malaria. Nature 415: 680–685.

  • 5.

    Quintero JP, Siqueira AM, Tobon A, Blair S, Moreno A, Arevalo-Herrera M, Lacerda MV, Valencia SH, 2011. Malaria-related anaemia: a Latin American perspective. Mem Inst Oswaldo Cruz 106 (Suppl 1): 91–104.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Pan American Health Organization, 2011. Malaria in the Americas. Available at: http://www.paho.org/hq/index.php?option=com_docman&task=doc_download&gid=22422&Itemid=270&lang=en. Accessed December 12, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Baird JK, 2007. Neglect of Plasmodium vivax malaria. Trends Parasitol 23: 533–539.

  • 8.

    Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM, 2007. Vivax malaria: neglected and not benign. Am J Trop Med Hyg 77: 79–87.

  • 9.

    Gething PW, Elyazar IR, Moyes CL, Smith DL, Battle KE, Guerra CA, Patil AP, Tatem AJ, Howes RE, Myers MF, George DB, Horby P, Wertheim HF, Price RN, Mueller I, Baird JK, Hay SI, 2012. A long neglected world malaria map: Plasmodium vivax endemicity in 2010. PLoS Negl Trop Dis 6: e1814.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Gething PW, Patil AP, Smith DL, Guerra CA, Elyazar IR, Johnston GL, Tatem AJ, Hay SI, 2011. A new world malaria map: Plasmodium falciparum endemicity in 2010. Malar J 10: 378.

  • 11.

    Ministerio de Salud, 2013. Análisis de Situación de Salud en el Perú. Lima, Peru: Ministerio de Salud del Perú.

  • 12.

    Ministerio de Salud, 2000. The Economic Impact of Malaria in Peru. Lima, Peru: Ministerio de Salud del Peru.

  • 13.

    Griffing SM, Gamboa D, Udhayakumar V, 2013. The history of 20th century malaria control in Peru. Malar J 12: 303.

  • 14.

    Vittor AY, Pan W, Gilman RH, Tielsch J, Glass G, Shields T, Sanchez-Lozano W, Pinedo VV, Salas-Cobos E, Flores S, Patz JA, 2009. Linking deforestation to malaria in the Amazon: characterization of the breeding habitat of the principal malaria vector, Anopheles darlingi. Am J Trop Med Hyg 81: 5–12.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Hahn MB, Gangnon RE, Barcellos C, Asner GP, Patz JA, 2014. Influence of deforestation, logging, and fire on malaria in the Brazilian Amazon. PLoS One 9: e85725.

  • 16.

    de Castro MC, Monte-Mor RL, Sawyer DO, Singer BH, 2006. Malaria risk on the Amazon frontier. Proc Natl Acad Sci USA 103: 2452–2457.

  • 17.

    Parker BS, Paredes Olortegui M, Peñataro Yori P, Escobedo K, Florin D, Rengifo Pinedo S, Cardenas Greffa R, Capcha Vega L, Rodriguez Ferrucci H, Pan WK, Banda Chavez C, Vinetz JM, Kosek M, 2013. Hyperendemic malaria transmission in areas of occupation-related travel in the Peruvian Amazon. Malar J 12: 178.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Coura JR, Suarez-Mutis M, Ladeia-Andrade S, 2006. A new challenge for malaria control in Brazil: asymptomatic Plasmodium infection–a review. Mem Inst Oswaldo Cruz 101: 229–237.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Asner GP, Llactayo W, Tupayachi R, Luna ER, 2013. Elevated rates of gold mining in the Amazon revealed through high-resolution monitoring. Proc Natl Acad Sci USA 110: 18454–18459.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Swenson JJ, Carter CE, Domec JC, Delgado CI, 2011. Gold mining in the Peruvian Amazon: global prices, deforestation, and mercury imports. PLoS One 6: e18875.

  • 21.

    Cremers L, Kolen J, De Theije M, 2013. Small-scale gold mining in the Amazon. The cases of Bolivia, Brazil, Colombia, Peru and Suriname. Amsterdam, The Netherlands: Centre for Latin American Studies and Documentation, 101.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Breeveld FJ, Vreden SG, Grobusch MP, 2012. History of malaria research and its contribution to the malaria control success in Suriname: a review. Malar J 11: 95.

  • 23.

    Evans L 3rd, Coignez V, Barojas A, Bempong D, Bradby S, Dijiba Y, James M, Bretas G, Adhin M, Ceron N, Hinds-Semple A, Chibwe K, Lukulay P, Pribluda V, 2012. Quality of anti-malarials collected in the private and informal sectors in Guyana and Suriname. Malar J 11: 203.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, Ghani A, Drakeley C, Gosling R, 2012. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med 9: e1001165.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Brack A, Ipenza C, Alvarez J, Sotero V, 2011. Minería Aurífera en Madre de Dios y Contaminación con Mercurio. Una Bomba de Tiempo. Lima, Peru: Ministerio del Ambiente.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Mosquera C, Chavez ML, Pachas VH, Moschella P, 2009. Estudio diagnóstico de la actividad minera artesanal en Madre de Dios. Lima, Peru: Fundación Conservación Internacional.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Guzman J, Nayhua L, 2012. Situación epidemiológica de la Malaria en el Perú. (Hasta la SE N° 52* 2012). Bol Epidemiol, Lima, Peru: Ministerio de Salud del Perú, 888–891.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Dirección General de Epidemiología, 2013. Dirección General de Epidemiología. Reporte Epidemiológico. Available at: http://www.dge.gob.pe/mapas/. Accessed December 10, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Instituto Nacional de Estadística e Informática, 2013. Instituto Nacional de Estadística e Informática. Compendio estadístico del Perú 2013. Available at: http://www.inei.gob.pe/media/MenuRecursivo/publicaciones_digitales/Est/Lib1097/libro.pdf. Accessed December 10, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Oficina General de Epidemiología, 2005. Oficina General de Epidemiología. Protocolos de Vigilancia Epidemiológica. Parte I. Malaria. Available at: http://www.dge.gob.pe/buho/buho_malaria.pdf. Accessed December 11, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Valencia L, 2014. Madre de Dios: ¿Podemos Evitar la Tragedia? Políticas de Ordenamiento de la Minería Aurífera. Lima, Peru: Sociedad Peruana de Derecho Ambiental.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Ministerio de Salud, 2013. Ministerio de Salud. Mapa de Establecimientos de Salud MINSA. Available at: http://www.geominsa.minsa.gob.pe/geominsa/. Accessed December 11, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    MeteoRed, 2013. MeteoRed. Climate in Peru. Available at: http://www.meteored.com.ar/historico/tiempo-en_Puerto+Maldonado-America+Sur-Peru-Madre+de+Dios–1-23133.html. Accessed December 11, 2013.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Ministerio de Energía y Minas, 2014. Ministerio de Energía y Minas. Estadísticas de producción minera. Available at: http://www.minem.gob.pe/_estadisticaSector.php?idSector=1&idCategoria=10. Accessed January 7, 2014.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    World Gold Council, 2014. World Gold Council. Interactive Gold Price Chart and Downloads. Available at: http://www.gold.org/investment/statistics/gold_price_chart/. Accessed January 14, 2014.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Lawless JF, 1987. Negative binomial and mixed Poisson regression. Can J Stat 15: 209–225.

  • 37.

    Vuong QH, 1989. Likelihood ratio tests for model selection and non-nested hypotheses. Econometrica 57: 307–333.

  • 38.

    Kiszewski AE, Teklehaimanot A, 2004. A review of the clinical and epidemiologic burdens of epidemic malaria. Am J Trop Med Hyg 71: 128–135.

  • 39.

    Vinetz JM, Gilman RH, 2002. Asymptomatic Plasmodium parasitemia and the ecology of malaria transmission. Am J Trop Med Hyg 66: 639–640.

  • 40.

    Vosti SA, 1990. Malaria among gold miners in southern Para, Brazil: estimates of determinants and individual costs. Soc Sci Med 30: 1097–1105.

  • 41.

    Duarte EC, Fontes CJ, 2002. Association between reported annual gold mining extraction and incidence of malaria in Mato Grosso-Brazil, 1985–1996. Rev Soc Bras Med Trop 35: 665–668.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Singer B, Sawyer DO, 1992. Perceived malaria illness reports in mobile populations. Health Policy Plan 7: 40–45.

  • 43.

    Barbieri AF, Sawyer DO, Soares-Filho BS, 2005. Population and land use effects on malaria prevalence in the southern Brazilian Amazon. Hum Ecol 33: 847–874.

  • 44.

    Silva IA, Nyland JF, Gorman A, Perisse A, Ventura AM, Santos EC, Souza JM, Burek CL, Rose NR, Silbergeld EK, 2004. Mercury exposure, malaria, and serum antinuclear/antinucleolar antibodies in Amazon populations in Brazil: a cross-sectional study. Environ Health 3: 11.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Crompton P, Ventura AM, de Souza JM, Santos E, Strickland GT, Silbergeld E, 2002. Assessment of mercury exposure and malaria in a Brazilian Amazon riverine community. Environ Res 90: 69–75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 46.

    Ashe K, 2012. Elevated mercury concentrations in humans of Madre de Dios, Peru. PLoS One 7: e33305.

  • 47.

    Rosales-Rimache JA, Malca NE, Alarcón JJ, Chávez M, Gonzáles MA, 2013. Genotoxic damage among artisanal and small-scale mining workers exposed to mercury. Rev Peru Med Exp Salud Publica 30: 595–600.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 48.

    Olson SH, Gangnon R, Elguero E, Durieux L, Guegan JF, Foley JA, Patz JA, 2009. Links between climate, malaria, and wetlands in the Amazon Basin. Emerg Infect Dis 15: 659–662.

  • 49.

    Aramburú GJ, Ramal AC, Witzig R, 1999. Malaria reemergence in the Peruvian Amazon region. Emerg Infect Dis 5: 209–215.

  • 50.

    Bautista CT, Chan AS, Ryan JR, Calampa C, Roper MH, Hightower AW, Magill AJ, 2006. Epidemiology and spatial analysis of malaria in the northern Peruvian Amazon. Am J Trop Med Hyg 75: 1216–1222.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 51.

    Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, Alvarez E, Perez EJ, Gotuzzo E, 2005. Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J 4: 27.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 52.

    de Castro MC, Sawyer DO, Singer BH, 2007. Spatial patterns of malaria in the Amazon: implications for surveillance and targeted interventions. Health Place 13: 368–380.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 53.

    Barbieri AF, Sawyer DO, 2007. Heterogeneity of malaria prevalence in alluvial gold mining areas in northern Mato Grosso State, Brazil. Cad Saude Publica 23: 2878–2886.

    • PubMed
    • Search Google Scholar
    • Export Citation
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