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Am. J. Trop. Med. Hyg., 73(2), 2005, pp. 312-320
Copyright © 2005 by The American Society of Tropical Medicine and Hygiene

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THE PRESENCE OF PLASMODIUM FALCIPARUM GAMETOCYTES IN HUMAN BLOOD INCREASES THE GRAVIDITY OF ANOPHELES GAMBIAE MOSQUITOES

HEATHER M. FERGUSON*, LOUIS C. GOUAGNA, PETER OBARE, ANDREW F. READ, HAMZA BABIKER, JOHN GITHURE, AND JOHN C. BEIER
Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK; Mbita Point Research & Training Centre, International Centre for Insect Physiology and Ecology, Mbita, Kenya; Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya; Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida

We conducted a field study in an area of endemic malaria transmission in western Kenya to determine whether mosquitoes that feed on gametocyte-infected blood but do not become infected have reduced or enhanced fecundity in comparison to mosquitoes fed on uninfected blood. Fifteen paired membrane-feeding experiments were conducted in which two strains of Anopheles gambiae mosquitoes were simultaneously fed on either Plasmodium falciparum–infected blood from children or uninfected control blood from adults. The presence of noninfecting gametocytes in blood increased the probability that An. gambiae would produce eggs after one blood meal by sixfold (odds ratio for control relative to infected blood group 0.16; 95% CI 0.10–0.23). This result could not be explained by variation in blood meal size or hemoglobin content between hosts. When children cleared their infections, the difference in gravidity between mosquitoes fed on their blood and uninfected adults disappeared, suggesting this phenomenon is due to the presence of Plasmodium gametocytes in blood and not to host-specific factors such as age. This result was observed in two mosquito strains that differ in their innate fecundity, suggesting it may apply generally. To our knowledge, this is the first time that Plasmodium has been implicated as enhancing vector gravidity.

Received May 25, 2004. Accepted for publication February 4, 2005.

Acknowledgments: The authors thank S. Ombonya at the Mbita Health Centre, Suba District, and S. Keruba, S. Orao, and P. Ongele from the Mbita Point Research Training Center of ICIPE for technical assistance. We are extremely grateful to all the volunteers who participated in this study and to the village leaders for their support, assistance, and cooperation. The authors thank D. Nwakanma and F. Kenyon at the University of Edinburgh for assistance with parasite molecular analysis and J. Keating for his comments on this manuscript. This paper is submitted for publication with the permission of the Director, Kenya Medical Research Institute (KEMRI).

Financial support: This study was funded by grants from the Wellcome Trust (068292/Z/01/Z) and from the National Institutes of Health (U19 AI455511 and D43TW01142).

* Address correspondence to Heather M. Ferguson, Ifakara Health Research and Development Centre, P.O. Box 53, Off Mlabani Passage, Ifakara, Tanzania. E-mail: hferguson{at}ifakara.mimcom.net; and Laboratory of Entomology, University of Wageningen, P.O. Box 8031, 6700 EH Wageningen, The Netherlands. E-mail: Heather.Ferguson{at}wur.nl

Authors’ addresses: Heather Ferguson, Ifakara Health Research and Development Centre, P.O. Box 53, Off Mlabani Passage, Ifakara, Tanzania, Fax: 255 23 2625312, E-mail: hferguson{at}ifakara.mimcom.net, and Laboratory of Entomology, University of Wageningen, P.O. Box 8031, 6700 EH Wageningen, The Netherlands, E-mail: Heather.Ferguson{at}wur.nl. Louis C. Gouagna and Peter Obare, International Centre for Insect Physiology and Ecology (ICIPE), Mbita Point Research and Training Centre, Suba District, Western Kenya, c/o P.O. Box 30772, Nairobi, Kenya, Fax: +254 385 2219, E-mail: lgouagna{at}mbita.mimcom.net. Andrew F. Read and Hamza Babiker, Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh, UK, EH9 3JT, Fax: +44 131 650 6564, E-mail: a.read{at}ed.ac.uk.; h.babiker{at}ed.ac.uk. John Githure, Human Health Division, International Centre for Insect Physiology and Ecology, Nairobi, Kenya, Fax: +254 20 860110, E-mail: jgithure{at}icipe.org. John C. Beier, Department of Epidemiology and Public Health, Global Public Health Program, University of Miami, Miami, Florida, Fax: 305 256 1306, E-mail: jbeier{at}med.miami.edu.




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