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Submicroscopic Plasmodium falciparum gametocytemia (< 5,000 gametocytes/mL) is common and may result in mosquito infection. We assessed the relation between gametocyte density and mosquito infection under experimental and field conditions using real-time quantitative nucleic acid sequence-based amplification (QT-NASBA) for gametocyte quantification. Serial dilutions of NF54 P. falciparum gametocytes showed a positive association between gametocyte density and the proportion of infected mosquitoes (ß = 6.1; 95% confidence interval [CI], 2.7–9.6; P = 0.001). Successful infection became unlikely below an estimated density of 250–300 gametocytes/mL. In the field, blood samples of 100 naturally infected children showed a positive association between gametocyte density and oocyst counts in mosquitoes (ß = 0.38; 95% CI, 0.14–0.61; P = 0.002). The relative contribution to malaria transmission was similar for carriers with submicroscopic and microscopic gametocytemia. Our results show that transmission occurs efficiently at submicroscopic gametocyte densities and that carriers harboring submicroscopic gametocytemia constitute a considerable proportion of the human infectious reservoir.
Received May 17, 2006. Accepted for publication October 25, 2006.
Acknowledgments: The authors thank Jolanda Klaassen, Astrid Pouwelsen, Laura Pelser, and Jacqueline van Haalen of Radboud University Nijmegen and Samuel Orao from ICIPE for help with mosquito dissections. The authors thank the community of Mbita and surrounding villages for their cooperation. The authors thank Steve Kaniaru, George Omweri, Nick Makio, Patrick Sawa, Bernard Kapesa, Kenneth Okoth, and Peter Ongele for work in the field.
Financial support: This work was supported by the Technology Foundation STW (Grant NFA6009) and WOTRO (WM 2003-00702).
* Address correspondence to J. Teun Bousema, Department of Medical Microbiology 268, Radboud University, Nijmegen Medical Centre, PO Box 9101, 6500 HB Nijmegen, The Netherlands. E-mail: t.bousema{at}ncmls.ru.nl
The first two authors each contributed equally to this manuscript.
Authors’ addresses: Petra Schneider, Institute of Immunology and Infection Research, University of Edinburgh, Edinburgh, UK, E-mail: Petra.Schneider{at}ed.ac.uk. J. Teun Bousema, Marga van de Vegte-Bolmer, and Robert W. Sauerwein, Department of Medical Microbiology 268, Radboud University Nijmegen Medical Centre, PO Box 9101, 6500 HB, The Netherlands, Telephone: 31-243619515, E-mails: t.bousema{at}ncmls.ru.nl, M.vandeVegte{at}mmb.umcn.nl, and r.sauerwein{at}mmb.umcn.nl. Louis C. Gouagna, Institut de Recherche pour le Développement, 01 PO Box 182, Ouagadougou, Burkina Faso, E-mail: Louis-Clement.Gouagna{at}ird.bf. Silas Otieno, International Centre for Insect Physiology and Ecology, Mbita, PO Box 30772, Nairobi, Kenya, E-mail: silas_otieno{at}yahoo.co.uk. Sabah A. Omar, Kenya Medical Research Institute, PO Box 54840, Nairobi, Kenya, E-mail: OSabah{at}kemri.org.
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