Guerra CA, Snow RW, Hay SI, 2006. Mapping the global extent of malaria in 2005. Trends Parasitol 22: 353–358.
Mendis K, Sina BJ, Marchesini P, Carter R, 2001. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64: 97–106.
Baird JK, 2007. Neglect of Plasmodium vivax malaria. Trends Parasitol 23: 533–539.
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.
Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW, 2004. The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 4: 327–336.
Duarte EC, Gyorkos TW, Pang L, Abrahamowicz M, 2004. Epidemiology of malaria in a hypoendemic Brazilian Amazon migrant population: a cohort study. Am J Trop Med Hyg 70: 229–237.
Pan American Health Organization, Health Information and Analysis, 2008. Health Situation in the Americas: Basic Indicators 2008. Washington, DC.
Flores-Mendoza C, Fernandez R, Escobedo-Vargas KS, Vela-Perez Q, Schoeler GB, 2004. Natural Plasmodium infections in Anopheles darlingi and Anopheles benarrochi (Diptera: Culicidae) from eastern Peru. J Med Entomol 41: 489–494.
Schoeler GB, Flores-Mendoza C, Fernandez R, Davila JR, Zyzak M, 2003. Geographical distribution of Anopheles darlingi in the Amazon Basin region of Peru. J Am Mosq Control Assoc 19: 286–296.
Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Ronca 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.
Branch OH, Takala S, Kariuki S, Nahlen BL, Kolczak M, Hawley W, Lal AA, 2001. Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun 69: 7783–7792.
Roshanravan B, Kari E, Gilman RH, Cabrera L, Lee E, Metcalfe J, Calderon M, Lescano AG, Montenegro SH, Calampa C, Vinetz JM, 2003. Endemic malaria in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 69: 45–52.
Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA, 2006. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg 74: 3–11.
Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, Nandy A, Guthmann JP, Nosten F, Carlton J, Looareesuwan S, Nair S, Sudimack D, Day NP, Anderson TJ, White NJ, 2007. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis 195: 927–933.
Srivastava HC, Sharma SK, Bhatt RM, Sharma VP, 1996. Studies on Plasmodium vivax relapse pattern in Kheda district, Gujarat. Indian J Malariol 33: 173–179.
Craig AA, Kain KC, 1996. Molecular analysis of strains of Plasmodium vivax from paired primary and relapse infections. J Infect Dis 174: 373–379.
Cui L, Escalante AA, Imwong M, Snounou G, 2003. The genetic diversity of Plasmodium vivax populations. Trends Parasitol 19: 220–226.
Bruce MC, Galinski MR, Barnwell JW, Snounou G, Day KP, 1999. Polymorphism at the merozoite surface protein-3alpha locus of Plasmodium vivax: global and local diversity. Am J Trop Med Hyg 61: 518–525.
Feng X, Carlton JM, Joy DA, Mu J, Furuya T, Suh BB, Wang Y, Barnwell JW, Su XZ, 2003. Single-nucleotide polymorphisms and genome diversity in Plasmodium vivax. Proc Natl Acad Sci USA 100: 8502–8507.
Gomez JC, McNamara DT, Bockarie MJ, Baird JK, Carlton JM, Zimmerman PA, 2003. Identification of a polymorphic Plasmodium vivax microsatellite marker. Am J Trop Med Hyg 69: 377–379.
Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, King CL, Kawamoto F, Hartl DL, Wirth DF, 2008. Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene 410: 105–112.
Nyachieo A, van Overmeir C, Laurent T, Dujardin JC, D'Alessandro U, 2005. Plasmodium falciparum genotyping by microsatellites as a method to distinguish between recrudescent and new infections. Am J Trop Med Hyg 73: 210–213.
Kosek M, Yori P, Gilman RH, Calderon M, Zimic M, Chuquiyauri R, Jeri C, Pinedo V, Matthias MA, Llanos-Cuentas A, Vinetz JM, 2012. High degree of Plasmodium vivax diversity in the Peruvian Amazon demonstrated by tandem repeat polymorphism analysis. Am J Trop Med Hyg 86: 580–586.
Kirchgatter K, del Portillo HA, 1998. Molecular analysis of Plasmodium vivax relapses using the MSP1 molecule as a genetic marker. J Infect Dis 177: 511–515.
Khusmith S, Tharavanij S, Bunnag D, 1998. Antigenic disparity of Plasmodium vivax causing initial symptoms and causing relapse. Southeast Asian J Trop Med Public Health 29: 519–524.
Pukrittayakamee S, Chantra A, Simpson JA, Vanijanonta S, Clemens R, Looareesuwan S, White NJ, 2000. Therapeutic responses to different antimalarial drugs in vivax malaria. Antimicrob Agents Chemother 44: 1680–1685.
Pukrittayakamee S, Imwong M, Looareesuwan S, White NJ, 2004. Therapeutic responses to antimalarial and antibacterial drugs in vivax malaria. Acta Trop 89: 351–356.
Zakeri S, Barjesteh H, Djadid ND, 2006. Merozoite surface protein-3alpha is a reliable marker for population genetic analysis of Plasmodium vivax. Malar J 5: 53.
Bruce MC, Galinski MR, Barnwell JW, Donnelly CA, Walmsley M, Alpers MP, Walliker D, Day KP, 2000. Genetic diversity and dynamics of Plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121: 257–272.
Leclerc MC, Durand P, Gauthier C, Patot S, Billotte N, Menegon M, Severini C, Ayala FJ, Renaud F, 2004. Meager genetic variability of the human malaria agent Plasmodium vivax. Proc Natl Acad Sci USA 101: 14455–14460.
Chen N, Auliff A, Rieckmann K, Gatton M, Cheng Q, 2007. Relapses of Plasmodium vivax infection result from clonal hypnozoites activated at predetermined intervals. J Infect Dis 195: 934–941.
Collins WE, 2007. Further understanding the nature of relapse of Plasmodium vivax infection. J Infect Dis 195: 919–920.
Galappaththy GN, Omari AA, Tharyan P, 2007. Primaquine for preventing relapses in people with Plasmodium vivax malaria. Cochrane Database Syst Rev CD004389.
Orjuela-Sanchez P, da Silva NS, da Silva-Nunes M, Ferreira MU, 2009. Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia. Am J Trop Med Hyg 81: 961–968.
Solari-Soto Lely, Soto-Tarazona Alonso, Mendoza-Requena Daniel, Llanos-Cuentas Alejandro, 2002. Ensayo clinico del tratamiento de la malaria vivax con esquema acortado de primaquina comparado con el esquema tradicional. Rev Per Soc Med Intern 15: 4.
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To determine the magnitude of Plasmodium vivax relapsing malaria in rural Amazonia, we carried out a study in four sites in northeastern Peru. Polymerase chain reaction-restriction fragment length polymorphism of PvMSP-3α and tandem repeat (TR) markers were compared for their ability to distinguish relapse versus reinfection. Of 1,507 subjects with P. vivax malaria, 354 developed > 1 episode during the study; 97 of 354 (27.5%) were defined as relapse using Pvmsp-3α alone. The addition of TR polymorphism analysis significantly reduced the number of definitively defined relapses to 26 of 354 (7.4%) (P < 0.05). Multivariate logistic regression modeling showed that the probability of having > 1 infection was associated with the following: subjects in Mazan (odds ratio [OR] = 2.56; 95% confidence interval [CI] 1.87, 3.51), 15–44 years of age (OR = 1.49; 95% CI 1.03, 2.15), traveling for job purposes (OR = 1.45; 95%CI 1.03, 2.06), and travel within past month (OR = 1.46; 95% CI 1.0, 2.14). The high discriminatory capacity of the molecular tools shown here is useful for understanding the micro-geography of malaria transmission.
Financial support: This work was supported by the following grants from the United States Public Health Service, National Institutes of Health/National Institute of Allergy and Infectious Diseases: D43TW007120, K24AI068903, R01AI067727, U19AI089681. In addition, we are grateful for guidance and inspiration from Stephanie Brodine, John Weeks, and Richard Garfein, members of Dr. Chuquiyauri's thesis committee in the San Diego State University-University of California San Diego Doctoral Program in Global Health (supported by NIH grant R25TW007500).
Authors' addresses: Raul Chuquiyauri, ‘Alexander von Humboldt’ Tropical Medicine Institute, Cayetano Heredia Peruvian University, Lima, Peru, E-mail: rachuqui@ucsd.edu. Pablo Peñataro, Margaret Kosek, and Robert H. Gilman, Johns Hopkins Bloomberg School of Public Health, Department of International Health, Division of Global Disease Epidemiology and Control, Baltimore, MD, E-mails: pyori@jhsph.edu, mkosek@jhsph.edu, and rgilman@jhsph.edu. Manuel Fasabi, Maritza Calderon, and Sonia Torres, AB Prisma, Lima, Peru, E-mails: manuelmani1@gmail.com, mmcalderons@yahoo.es, and soniatadimi@yahoo.com. Kimberly C. Brouwer, Division of Global Public Health, School of Medicine, University of California San Diego, La Jolla, CA, E-mail: kbrouwer@ucsd.edu. Joseph M. Vinetz, Division of Infectious Diseases, Department of Medicine, University of California San Diego, La Jolla, CA, E-mail: jvinetz@ucsd.edu.
Guerra CA, Snow RW, Hay SI, 2006. Mapping the global extent of malaria in 2005. Trends Parasitol 22: 353–358.
Mendis K, Sina BJ, Marchesini P, Carter R, 2001. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64: 97–106.
Baird JK, 2007. Neglect of Plasmodium vivax malaria. Trends Parasitol 23: 533–539.
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.
Hay SI, Guerra CA, Tatem AJ, Noor AM, Snow RW, 2004. The global distribution and population at risk of malaria: past, present, and future. Lancet Infect Dis 4: 327–336.
Duarte EC, Gyorkos TW, Pang L, Abrahamowicz M, 2004. Epidemiology of malaria in a hypoendemic Brazilian Amazon migrant population: a cohort study. Am J Trop Med Hyg 70: 229–237.
Pan American Health Organization, Health Information and Analysis, 2008. Health Situation in the Americas: Basic Indicators 2008. Washington, DC.
Flores-Mendoza C, Fernandez R, Escobedo-Vargas KS, Vela-Perez Q, Schoeler GB, 2004. Natural Plasmodium infections in Anopheles darlingi and Anopheles benarrochi (Diptera: Culicidae) from eastern Peru. J Med Entomol 41: 489–494.
Schoeler GB, Flores-Mendoza C, Fernandez R, Davila JR, Zyzak M, 2003. Geographical distribution of Anopheles darlingi in the Amazon Basin region of Peru. J Am Mosq Control Assoc 19: 286–296.
Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Ronca 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.
Branch OH, Takala S, Kariuki S, Nahlen BL, Kolczak M, Hawley W, Lal AA, 2001. Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun 69: 7783–7792.
Roshanravan B, Kari E, Gilman RH, Cabrera L, Lee E, Metcalfe J, Calderon M, Lescano AG, Montenegro SH, Calampa C, Vinetz JM, 2003. Endemic malaria in the Peruvian Amazon region of Iquitos. Am J Trop Med Hyg 69: 45–52.
Vittor AY, Gilman RH, Tielsch J, Glass G, Shields T, Lozano WS, Pinedo-Cancino V, Patz JA, 2006. The effect of deforestation on the human-biting rate of Anopheles darlingi, the primary vector of falciparum malaria in the Peruvian Amazon. Am J Trop Med Hyg 74: 3–11.
Imwong M, Snounou G, Pukrittayakamee S, Tanomsing N, Kim JR, Nandy A, Guthmann JP, Nosten F, Carlton J, Looareesuwan S, Nair S, Sudimack D, Day NP, Anderson TJ, White NJ, 2007. Relapses of Plasmodium vivax infection usually result from activation of heterologous hypnozoites. J Infect Dis 195: 927–933.
Srivastava HC, Sharma SK, Bhatt RM, Sharma VP, 1996. Studies on Plasmodium vivax relapse pattern in Kheda district, Gujarat. Indian J Malariol 33: 173–179.
Craig AA, Kain KC, 1996. Molecular analysis of strains of Plasmodium vivax from paired primary and relapse infections. J Infect Dis 174: 373–379.
Cui L, Escalante AA, Imwong M, Snounou G, 2003. The genetic diversity of Plasmodium vivax populations. Trends Parasitol 19: 220–226.
Bruce MC, Galinski MR, Barnwell JW, Snounou G, Day KP, 1999. Polymorphism at the merozoite surface protein-3alpha locus of Plasmodium vivax: global and local diversity. Am J Trop Med Hyg 61: 518–525.
Feng X, Carlton JM, Joy DA, Mu J, Furuya T, Suh BB, Wang Y, Barnwell JW, Su XZ, 2003. Single-nucleotide polymorphisms and genome diversity in Plasmodium vivax. Proc Natl Acad Sci USA 100: 8502–8507.
Gomez JC, McNamara DT, Bockarie MJ, Baird JK, Carlton JM, Zimmerman PA, 2003. Identification of a polymorphic Plasmodium vivax microsatellite marker. Am J Trop Med Hyg 69: 377–379.
Karunaweera ND, Ferreira MU, Munasinghe A, Barnwell JW, Collins WE, King CL, Kawamoto F, Hartl DL, Wirth DF, 2008. Extensive microsatellite diversity in the human malaria parasite Plasmodium vivax. Gene 410: 105–112.
Nyachieo A, van Overmeir C, Laurent T, Dujardin JC, D'Alessandro U, 2005. Plasmodium falciparum genotyping by microsatellites as a method to distinguish between recrudescent and new infections. Am J Trop Med Hyg 73: 210–213.
Kosek M, Yori P, Gilman RH, Calderon M, Zimic M, Chuquiyauri R, Jeri C, Pinedo V, Matthias MA, Llanos-Cuentas A, Vinetz JM, 2012. High degree of Plasmodium vivax diversity in the Peruvian Amazon demonstrated by tandem repeat polymorphism analysis. Am J Trop Med Hyg 86: 580–586.
Kirchgatter K, del Portillo HA, 1998. Molecular analysis of Plasmodium vivax relapses using the MSP1 molecule as a genetic marker. J Infect Dis 177: 511–515.
Khusmith S, Tharavanij S, Bunnag D, 1998. Antigenic disparity of Plasmodium vivax causing initial symptoms and causing relapse. Southeast Asian J Trop Med Public Health 29: 519–524.
Pukrittayakamee S, Chantra A, Simpson JA, Vanijanonta S, Clemens R, Looareesuwan S, White NJ, 2000. Therapeutic responses to different antimalarial drugs in vivax malaria. Antimicrob Agents Chemother 44: 1680–1685.
Pukrittayakamee S, Imwong M, Looareesuwan S, White NJ, 2004. Therapeutic responses to antimalarial and antibacterial drugs in vivax malaria. Acta Trop 89: 351–356.
Zakeri S, Barjesteh H, Djadid ND, 2006. Merozoite surface protein-3alpha is a reliable marker for population genetic analysis of Plasmodium vivax. Malar J 5: 53.
Bruce MC, Galinski MR, Barnwell JW, Donnelly CA, Walmsley M, Alpers MP, Walliker D, Day KP, 2000. Genetic diversity and dynamics of Plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121: 257–272.
Leclerc MC, Durand P, Gauthier C, Patot S, Billotte N, Menegon M, Severini C, Ayala FJ, Renaud F, 2004. Meager genetic variability of the human malaria agent Plasmodium vivax. Proc Natl Acad Sci USA 101: 14455–14460.
Chen N, Auliff A, Rieckmann K, Gatton M, Cheng Q, 2007. Relapses of Plasmodium vivax infection result from clonal hypnozoites activated at predetermined intervals. J Infect Dis 195: 934–941.
Collins WE, 2007. Further understanding the nature of relapse of Plasmodium vivax infection. J Infect Dis 195: 919–920.
Galappaththy GN, Omari AA, Tharyan P, 2007. Primaquine for preventing relapses in people with Plasmodium vivax malaria. Cochrane Database Syst Rev CD004389.
Orjuela-Sanchez P, da Silva NS, da Silva-Nunes M, Ferreira MU, 2009. Recurrent parasitemias and population dynamics of Plasmodium vivax polymorphisms in rural Amazonia. Am J Trop Med Hyg 81: 961–968.
Solari-Soto Lely, Soto-Tarazona Alonso, Mendoza-Requena Daniel, Llanos-Cuentas Alejandro, 2002. Ensayo clinico del tratamiento de la malaria vivax con esquema acortado de primaquina comparado con el esquema tradicional. Rev Per Soc Med Intern 15: 4.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 2714 | 2531 | 42 |
Full Text Views | 334 | 9 | 0 |
PDF Downloads | 104 | 10 | 0 |