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EXPERIMENTAL INFECTION OF THE NEOTROPICAL MALARIA VECTOR ANOPHELES DARLINGI BY HUMAN PATIENT-DERIVED PLASMODIUM VIVAX IN THE PERUVIAN AMAZON

Malaria transmission from humans to mosquitoes is modulated by human host immune factors. Understanding mechanisms by which the human host response may impair parasite infectivity for mosquitoes has direct implications for the development of transmission-blocking vaccines. We hypothesized that despite a low transmission intensity of malaria in the Peruvian Amazon region of Iquitos, transmission-blocking immunity against Plasmodium vivax might be common, given an unexpectedly high proportion of asymptomatic parasitemic individuals in this region. To test this hypothesis, the ability of symptomatic P. vivax malaria patients to experimentally infect wild-caught outbred Anopheles darlingi mosquitoes was tested using the indirect membrane feeding technique. Only half (52/102) of P. vivax parasitemic patients successfully infected mosquitoes. Transmitters were more likely to have gametocytes (OR 6.35, P = 0.003), high parasitemia (OR 3.79, P = 0.024), and, in terms of basic clinical parameters, a slower pulse rate (mean ± SD: 82.3 ± 12.3 versus 88.7 ± 13.5, P = 0.016) than non-transmitters. Log₁₀ gametocytemia and log₁₀ real-time reverse transcriptase Pvs25 PCR quantifying gametocytes were significantly and positively correlated with oocyst counts (correlation coefficient 0.505, R² = 0.26, P = 0.001). These experiments are the first to establish a system of determining transmission patterns in experimental infection of outbred natural neotropical malaria vectors in the Amazon region. Patients with P. vivax inefficiently infect outbred An. darlingi mosquitoes, raising the possibility that some degree of naturally occurring transmission-blocking immunity is present on a population basis in the Peruvian Amazon, an area of low intensity of malaria transmission.

Received March 17, 2006. Accepted for publication June 15, 2006.

Acknowledgments: We are grateful to the Director of the Loreto Department of Health, Carlos Vidal Ore, M.D., for his support on this project. We thank our field team, Dr. Eddy Segura, Sonia Torres Andrade, and Nahir Chuquipiodo, along with the dedicated insectary staff, Victor Lopez, Carlos Tong, and Dario Ramirez; technical assistance in Iquitos from Carlos Pacheco, Flor Pacheco, Silvia Marin Gonzales, and Alex Tenorio Sanchez; helpful guidance from Kailash Patra and Mike Matthias; and participation of patients from the city of Iquitos and the villages of Varillal and Santo Tomas are also appreciated.

Financial support: This study was supported by an ASTMH-Ellison Postdoctoral Fellowship in Tropical Medicine (A.R.B.), NIH institutional training grant T32AI007036 (with which A.R.B. was supported), an IDSA summer scholarship (J.L.), the Baylor Department of International Medicine (J.L.), a Doris Duke Charitable Foundation Innovations in Clinical Research Program grant (J.M.V.), NIH/NIAID grant K24AI068903 (J.M.V.), NIH/NIDA grant K01DA020364 (K.B.), and NIH Fogarty International Center Global Infectious Diseases Training Grant 5D43TW007120 (J.M.V.).

^* Address correspondence to Joseph M. Vinetz, University of California San Diego School of Medicine, Division of Infectious Diseases, Department of Medicine, 9500 Gilman Drive, 0741, George Palade Laboratories/Cellular and Molecular Medicine-West Room 125, La Jolla, CA 92093-0741. E-mail: jvinetz{at}ucsd.edu

Authors’ addresses: Ajay R. Bharti, Kimberly C. Brouwer, Jessica Lin, and Joseph M. Vinetz, University of California San Diego School of Medicine, La Jolla, California, E-mails: abharti{at}ucsd.edu, kbrouwer{at}ucsd.edu, jesstlin{at}gmail.com, and jvinetz{at}ucsd.edu. Raul Chuquiyauri and Alejandro Llanos-Cuentas, Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Lima, Peru, E-mails: raulharo{at}yahoo.com and allanos{at}upch.edu.pe. Jeffrey Stancil, Naval Medical Research Center Detachment, Iquitos, Peru, E-mail: stancil{at}nmrcd.med.navy.mil.

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