Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-22T12:27:14.019Z Has data issue: false hasContentIssue false
  • English
  • Français

Risk factors for gametocyte carriage in uncomplicated falciparum malaria in children

Published online by Cambridge University Press:  23 August 2004

A. SOWUNMI ,
B. A. FATEYE ,
A. A. ADEDEJI ,
F. A. FEHINTOLA  and
T. C. HAPPI
A. SOWUNMI
Affiliation:
Department of Pharmacology and Therapeutics and Institute for Medical Research and Training, University of Ibadan, Ibadan, Nigeria
B. A. FATEYE
Affiliation:
Department of Pharmacology and Therapeutics and Institute for Medical Research and Training, University of Ibadan, Ibadan, Nigeria
A. A. ADEDEJI
Affiliation:
Department of Pharmacology and Therapeutics and Institute for Medical Research and Training, University of Ibadan, Ibadan, Nigeria
F. A. FEHINTOLA
Affiliation:
Department of Pharmacology and Therapeutics and Institute for Medical Research and Training, University of Ibadan, Ibadan, Nigeria
T. C. HAPPI
Affiliation:
Department of Pharmacology and Therapeutics and Institute for Medical Research and Training, University of Ibadan, Ibadan, Nigeria
Get access Rights & Permissions [Opens in a new window]

Abstract

The risk factors associated with gametocytaemia at presentation and after treatment with different antimalarial drug regimens were evaluated in 767 children enrolled prospectively in 5 antimalarial drug trials between July 1996 and December 2002 in a hyperendemic area of southwestern Nigeria. The children were assigned to one of 6 treatment groups: chloroquine (CQ) only; pyrimethamine-sulfadoxine (PS) only; amodiaquine (AQ) only; CQ combined with chlorpheniramine (CQCP); or PS combined with CQ (CQPS) or AQ (AQPS). At enrolment, 115 (15%) of 767 children were gametocyte carriers. During follow-up, 15·6% of all patients (i.e. 120 patients) developed patent gametocytaemia, which in 85% (102 patients) had developed by day 7 following treatment. In a multiple regression model, 4 factors were found to be independent risk factors for the presence of gametocytaemia at enrolment: male gender (adjusted odds ratio [AOR]=0·55, 95% confidence interval [CI] 0·36–0·83, P=0·005), absence of fever (AOR=1·61, 95% CI 1·05–2·5, P=0·03), duration of illness >3 days (AOR=1·57, 95% CI 1·0–2·4, P=0·047), and asexual parasite densities less than 5000/μl (AOR=0·42, 95% CI 0·24–0·73, P=0·002). The presence of patent gametocytaemia at enrolment (AOR=0·04, 95% CI 0·02–0·07, P<0·001) and recrudescence of asexual parasites within 14 days were associated with the presence of gametocytaemia 7 or 14 days after enrolment (AOR=0·5, 95% CI 0·3–0·8, P=0·007). Delay in the time taken to clear the initial parasitaemia (>2 days) was associated with increased risk of subsequent gametocyte carriage. These findings may have implications for malaria control efforts in sub-Saharan Africa where control of the disease depends almost entirely on chemotherapy.

Keywords

gametocyte carriagechildrenrisk factorsNigeria
Type
Research Article
Information
Parasitology , Volume 129 , Issue 3 , September 2004 , pp. 255 - 262
Copyright
© 2004 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AKIM, N. I. J., DRAKELEY, C., KINGO, T., SIMON, B., SENKORO, K. & SAUERWEIN, R. W. ( 2000). Dynamics of Plasmodium falciparum gametocytaemia in symptomatic patients in an area of intense perennial transmission in Tanzania. American Journal of Tropical Medicine and Hygiene 63, 199–203.CrossRefGoogle Scholar
ANON. ( 1994). Epi Info Version 6. A Word Processing Data Base and Statistics Program for Public Health on IBM-compatible Microcomputers. Atlanta, GA: Centers for Disease Control and Prevention.
BONNET, S., GOUAGNA, L. C., PAUL, R. E., SAFEUKUI, I., MEUNIER, J.-Y. & BOUDIN, C. ( 2003). Estimation of malaria transmission from humans in two neighbouring villages in south Cameroon: evaluation and comparison of several indices. Transactions of the Royal Society of Tropical Medicine and Hygiene 97, 53–59.CrossRefGoogle Scholar
BUCKLING, A., RANFORD-CARTWRIGHT, L. C., MILES, A. & READ, A. F. ( 1999). Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology 118, 339–346.CrossRefGoogle Scholar
BUTCHER, G. A. ( 1997). Antimalarial drugs and the mosquito transmission of Plasmodium. International Journal for Parasitology 27, 975–987.CrossRefGoogle Scholar
CARTER, P. & MILLER, L. H. ( 1979). Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bulletin of the World Health Organization 57 (Suppl. 1), 37–52.Google Scholar
CARTER, R. & GRAVES, P. M. ( 1988). Gametocytes. In Malaria: Principles and Practice of Malariology, vol. 1 ( ed. Wernsdorfer, W. H. & McGregor, I.), pp. 253–306. Churchill Livingstone, Edinburgh.
EZEILO, G. C. ( 1971). Neutropenia in Africans. Tropical and Geographical Medicine 23, 264–267.Google Scholar
FALADE, C. O., SALAKO, L. A., SOWUNMI, A., ODUOLA, A. M. J. & LARCIER, P. ( 1997). Comparative efficacy of chloroquine, halofantrine and sulphadoxine-pyrimethamine in treatment of acute uncomplicated falciparum malaria in Nigerian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 58–62.CrossRefGoogle Scholar
GITHEKO, A. K., BRANDLING-BENNET, A. D., BEIER, M., ATIELI, F., OWAGA, M. & COLLINS, F. H. ( 1992). The reservoir of Plasmodium falciparum malaria in a holoendemic area of Western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 355–358.CrossRefGoogle Scholar
GRIFFIN, J. E. & WILSON, J. D. ( 1991). Disorders of the testis. In Harrison's: Principles of Internal Medicine, vol. 2 (ed. Wilson, J. D., Braunwald, E., Isselbacher, K. J., Peterdorsf, R. G., Martin, J. B., Fauci, A. S. & Root, R. K.), pp. 1765–1776. McGraw-Hill, New York.
HANDUNNETTI, S. M., GUNEWARDENA, D. M., PATHIRANA, P. P. S. L., EKANAYAKE, K., WEERASINGHE, S. & MENDIS, K. N. ( 1996). Features of recrudescent chloroquine-resistant Plasmodium falciparum infections confer a survival advantage on parasites and have implications for disease control. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 563–567.CrossRefGoogle Scholar
HOGH, B., GAMAGE-MENDIS, A., BUTCHER, G. A., THOMPSON, R., BEGTRUP, K., MENDIS, C., ENOSSE, S. M., DGEDGE, M., BARRETO, J., ELING, W. & SINDEN, R. E. ( 1998). The differing impact of chloroquine and pyrimethamine/sulfadoxine upon the infectivity of malaria species to mosquito vector. American Journal of Tropical Medicine and Hygiene 58, 176–182.CrossRefGoogle Scholar
LINGNAU, A., MARGOS, G., MAIER, W. A. & SEITZ, H. M. ( 1993). The effects of hormones on the gametocytogenesis of Plasmodium falciparum in vitro. Applied Parasitology 34, 153–160.Google Scholar
MASWOSWE, S. M., PETERS, W. & WARHURST, D. C. ( 1985). Corticosteroid stimulation of the growth of Plasmodium falciparum gametocytes in vitro. Annals of Tropical Medicine and Parasitology 79, 607–616.CrossRefGoogle Scholar
MONS, B. ( 1985). Induction of sexual differentiation in malaria. Parasitology Today 1, 87–89.CrossRefGoogle Scholar
NACHER, M., SINGHASIVANON, P., SILACHAMROON, U., TREEPRASERTSUK, S., KRUDSOOD, S., GAY, F., MAZIER, D. & LOOARESUWAN, S. ( 2002). Association of helminth infections with increased gametocyte carriage during mild falciparum malaria in Thailand. American Journal of Tropical Medicine and Hygiene 65, 644–647.Google Scholar
PRICE, R. N., NOSTEN, F., LUXEMBURGER, C., TER KUILE, F. O., PAIPHUN, L., CHONGSUPHAJAISIDDHI, T. & WHITE, N. J. ( 1996). Effects of artemisinin derivatives on malaria transmissibility. Lancet 347, 1654–1658.CrossRefGoogle Scholar
PRICE, R., NOSTEN, F., SIMPSON, J. A., LUXEMBURGER, C., PAIPHUN, L., TER KUILE, F., VAN VUGT, M., CHONGSUPHAJAISIDDHI, T. & WHITE, N. J. ( 1999). Risk factors for gametocyte carriage in uncomplicated falciparum malaria. American Journal of Tropical Medicine and Hygiene 60, 1019–1023.CrossRefGoogle Scholar
ROBERT, V., MOLEZ, J-F. & TRAPE, J-F. ( 1996). Short report: gametocytes, chloroquine pressure, and the relative parasite survival advantage of resistant strains of falciparum malaria in West Africa. American Journal of Tropical Medicine and Hygiene 55, 350–351.CrossRefGoogle Scholar
ROBERT, V., AWONO-AMBENE, H. P., LE HESRAN, J-Y. & TRAPE, J-F. ( 2000). Gametocytaemia and infectivity to mosquitoes of patients with uncomplicated Plasmodium falciparum malaria attacks treated with chloroquine or sulfadoxine-pyrimethamine. American Journal of Tropical Medicine and Hygiene 62, 210–216.CrossRefGoogle Scholar
SALAKO, L. A., AJAYI, F. O., SOWUNMI, A. & WALKER, O. ( 1990). Malaria in Nigeria: a revisit. Annals of Tropical Medicine and Parasitology 84, 435–445.CrossRefGoogle Scholar
SHAPER, A. G. & LEWIS, P. ( 1971). Genetic neutropenia in people of African origin. Lancet ii, 1021–1023.CrossRefGoogle Scholar
SINDEN, R. E., CANNING, E. U., BRAY, R. S. & SMALLEY, M. E. ( 1978). Gametocyte and gamete development in Plasmodium falciparum. Proceedings of the Royal Society of London, Series B 201, 375–399.CrossRefGoogle Scholar
SMALLEY, M. E. ( 1976). Plasmodium falciparum gametocytogenesis in vitro. Nature, London 264, 271–272.CrossRefGoogle Scholar
SMALLEY, M. E., BROWN, J. & BASSETT, N. M. ( 1981). The rate of production of Plasmodium falciparum gametocytes during natural infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 318–319.CrossRefGoogle Scholar
SOWUNMI, A. ( 2002). A randomized comparison of chloroquine, amodiaquine and their combination with pyrimethamine-sulfadoxine in the treatment of acute, uncomplicated, Plasmodium falciparum malaria in children. Annals of Tropical Medicine and Parasitology 96, 227–238.CrossRefGoogle Scholar
SOWUNMI, A. ( 2003). A randomized comparison of chloroquine and chloroqunie plus ketotifen, in the treatment of acute, uncomplicated, Plasmodium falciparum malaria in children. Annals of Tropical Medicine and Parasitology 97, 103–117.CrossRefGoogle Scholar
SOWUNMI, A., AKINDELE, J. A. & BALOGUN, M. A. ( 1995). Leukocyte counts in falciparum malaria in African children from an endemic area. African Journal of Medicine and Medical Sciences 24, 145–149.Google Scholar
SOWUNMI, A. & FATEYE, B. A. ( 2003 a). Asymptomatic, recrudescent, chloroquine-resistant, Plasmodium falciparum infections in Nigerian children: clinical and parasitological characteristics and implications for transmission of drug-resistant infections. Annals of Tropical Medicine and Parasitology 97, 469–479.Google Scholar
SOWUNMI, A. & FATEYE, B. A. ( 2003 b). Plasmodium falciparum gametocytaemia in Nigerian children: before, during and after treatment with antimalarial drugs. Tropical Medicine and International Health 8, 783–792.Google Scholar
SOWUNMI, A. & FATEYE, B. A. ( 2003 c). Gametocyte sex ratios in children with asymptomatic, recrudescent, pyrimethamine-sulfadoxine-resistant, Plasmodium falciparum malaria. Annals of Tropical Medicine and Parasitology 97, 671–682.Google Scholar
SOWUNMI, A., ODUOLA, A. M. J., OGUNDAHUNSI, O. A. T. & SALAKO, L. A. ( 1998 a). Comparative efficacy of chloroquine plus chlorpheniramine and pyrimethamine-sulphadoxine in acute uncomplicated falciparum malaria in Nigerian children. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 77–81.Google Scholar
SOWUNMI, A., ODUOLA, A. M. J., OGUNDAHUNSI, O. A. T. & SALAKO, L. A. ( 1998 b). Enhancement of the antimalarial effect of chloroquine by chlorpheniramine in vivo. Tropical Medicine and International Health 3, 177–183.Google Scholar
SPSS ( 1999). SPSS for Windows Release 10.01 (Standard Version). SPSS Inc, Chicago, IL, USA.
SUTHERLAND, C. J., ALLOUECHE, A., CURTIS, J., DRAKELEY, C. J., ORD, R., DURAISINGH, M., GREENWOOD, B. M., WARHURST, D. C. & TARGETT, G. A. T. ( 2002). Gambian children successfully treated with chloroquine can harbor and transmit Plasmodium falciparum gametocytes carrying resistant genes. American Journal of Tropical Medicine and Hygiene 67, 575–585.Google Scholar
TCHUINKAM, T., MULDER, B., DECHERING, K., STOFFELS, H., VERHAVE, J. P., COT, M., CARNEVALE, P., MEUWISSEN, J. E. H. T. & ROBERT, V. ( 1993). Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Tropical Medicine and Parasitology 44, 271–276.Google Scholar
THOMSON, D. ( 1911). I. A research into the production, life and death of crescents in malignant tertian malaria, in treated and untreated cases, by an enumerative method. Annals of Tropical Medicine and Parasitology 5, 57–82.Google Scholar
TRAPE, J.-F., PISON, G., PREZIOSI, M.-P., ENEL, C., DU LOU, A. D., DELAUNAY, V., SAMB, B., LAGARDE, E., MOLEZ, J.-F. & SIMONDON, F. ( 1998). Impact of chloroquine resistance on malaria mortality. Life Sciences 321, 689–697.CrossRefGoogle Scholar
TRAPE, J-F. ( 2001). The public health impact of chloroquine resistance in Africa. American Journal of Tropical Medicine and Hygiene 64 (Suppl.), 12–17.CrossRefGoogle Scholar
VON SEIDLEIN, L., DRAKELEY, C., GREENWOOD, B., WALRAVEN, G. & TARGETT, G. ( 2001). Risk factors for gametocyte carriage in Gambian children. American Journal of Tropical Medicine and Hygiene 65, 523–526.CrossRefGoogle Scholar
WHITE, N. J. ( 1997). Assessment of the pharmacodynamic properties of antimalarial drugs in vivo. Antimicrobial Agents and Chemotherapy 41, 1413–1422.Google Scholar
WILKINSON, R. N., NOEYPATIMANONDH, S. & GOULD, D. J. ( 1976). Infectivity of falciparum malaria patients for anopheline mosquitoes before and after chloroquine treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 306–307.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION ( 1973). Chemotherapy of Malaria and Resistance to Antimalarials. Technical Report Series No. 529. WHO, Geneva.
WORLD HEALTH ORGANIZATION ( 2000). Severe falciparum malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 94 (Suppl. 1).CrossRef
WORLD HEALTH ORGANIZATION ( 2001 a). The Use of Antimalarial Drugs. Report of a WHO Informal Consultation. Document WHO/CDS/RBM/2001.33. WHO, Geneva.
WORLD HEALTH ORGANIZATION ( 2001 b). The Use of Antimalarial Drugs. Report of a WHO Informal Consultation. Document WHO/CDS/RBM/2001.35. WHO, Geneva.