Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-05T10:05:55.606Z Has data issue: false hasContentIssue false
  • English
  • Français

Sex ratio of Plasmodium falciparum gametocytes in inhabitants of Dielmo, Senegal

Published online by Cambridge University Press:  09 October 2003

V. ROBERT ,
C. S. SOKHNA ,
C. ROGIER ,
F. ARIEY  and
J.-F. TRAPE
V. ROBERT
Affiliation:
Institut de Recherche pour le Développement, UR Paludisme Afro-Tropical, B.P. 1386, Dakar, Sénégal Institut Pasteur de Madagascar, Groupe de Recherche sur le Paludisme, B.P. 1274, Antananarivo, Madagascar
C. S. SOKHNA
Affiliation:
Institut de Recherche pour le Développement, UR Paludisme Afro-Tropical, B.P. 1386, Dakar, Sénégal
C. ROGIER
Affiliation:
Institut de Médecine Tropicale du Service de Santé des Armées, Le Pharo, 13998 Marseille-Armées, France
F. ARIEY
Affiliation:
Institut Pasteur de Madagascar, Groupe de Recherche sur le Paludisme, B.P. 1274, Antananarivo, Madagascar
J.-F. TRAPE
Affiliation:
Institut de Recherche pour le Développement, UR Paludisme Afro-Tropical, B.P. 1386, Dakar, Sénégal
Get access Rights & Permissions [Opens in a new window]

Abstract

An epidemiological survey was conducted during a 4-month period of intense malaria transmission in Dielmo, a holoendemic Senegalese village. Two thick blood smears per inhabitant were collected weekly. The sex ratio of Plasmodium falciparum gametocytes (gamete precursors) was studied in 50 gametocyte carriers. All age classes were represented (mean 19·7 years; range: 2 months–75 years); 42 (84%) of them did not receive antimalarial treatment. Overall 668 thick smears were examined until 100 gametocytes had been counted or for 40 min. A total of 11 204 gametocytes were observed with a mean sex ratio of 0·346 (95% CI 0·317–0·374), i.e. 2·89 females per 1 male. Among the 284 thick smears in which at least 10 gametocytes were observed, the mean percentage of male gametocytes was 27·8%, with a range of 0–82%. Great variability was observed between gametocyte carriers and also between thick smears from the same gametocyte carrier. A multivariate analysis was performed which highlighted the fact that only 2 variables had a significant effect on the sex ratio. Anaemia was associated with an increased percentage of males (Prevalence Rate Ratio [PPR] of male gametocytes was multiplied by 1·65 if haematocrit rate <32%) and a wave of gametocytes was associated with an increased percentage of female gametocytes (PRR was multiplied by 0·48 during the peak of gametocytaemia and for the 2 weeks following this peak). The variables without significant effect on sex ratio were: age, sex, clinical status and sickle cell trait status of the gametocyte carrier, density of asexual parasites, quinine treatment, and gametocyte density (when taking account of its waves). These results are discussed in regard of possible differential production, mortality or sequestration of one gametocyte sex and selective advantages for the transmission of parasites.

Keywords

Plasmodium falciparumgametocytesex ratiomalaria transmissionholoendemy
Type
Research Article
Information
Parasitology , Volume 127 , Issue 1 , July 2003 , pp. 1 - 8
Copyright
2003 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

BABIKER, H. A., RANFORD-CARTWRIGHT, L. C. & WALLIKER, D. (1999). The epidemiology of multiple Plasmodium falciparum infections. 3. Genetic structure and dynamics of Plasmodium falciparum infections in the Kilombero region of Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 93 (Suppl. 1), S1/11–S1/14.Google Scholar
BOYD, M. F., STRATMAN-THOMAS, W. F. & KITCHEN, S. F. (1935). On the relative susceptibility of Anopheles quadrimaculatus to Plasmodium vivax and Plasmodium falciparum. American Journal of Tropical Medicine and Hygiene 15, 485–493.CrossRefGoogle Scholar
BURKOT, T., WILLIAMS, J. L. & SCHNEIDER, I. (1984). Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 339–341.CrossRefGoogle Scholar
BURKOT, T., GRAVES, P. M., PARU, R., BATTISTUTTA, D., BARNES, A. & SAUL, A. (1988). Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. American Journal of Tropical Medicine and Hygiene 39, 135–144.CrossRefGoogle Scholar
CAMERON, A. C. & TREVEDI, P. K. (1998). Regression Analysis of Count Data. Cambridge University Press, Cambridge.CrossRef
CARTER, R. & GRAVES, P. M. (1988). Gametocytes. In Malaria. Principles and Practice of Malariology (ed. Wernsdorfer, W. H. & McGregor, I.), pp. 1–59. Churchill Livingstone, Edinburgh, Scotland.
CONTAMIN, H., FANDEUR, T., ROGIER, C., BONNEFOY, S., KONATE, L., TRAPE, J. F. & MERCEREAU-PUIJALON, O. (1995). Different genetic characteristics of Plasmodium falciparum isolates collected during successive clinical malaria episodes in Senegalese children. American Journal of Tropical Medicine and Hygiene 54, 632–643.Google Scholar
DAUBERSIES, P., SALLENAVES-SALES, S., MAGNE, S., TRAPE, J.-F., CONTAMIN, H., FANDEUR, T., ROGIER, C., MERCEREAU-PUIJALON, O. & DRUILHE, P. (1996). Rapid turnover of Plasmodium falciparum populations in asymptomatic individuals living in a high transmission area. American Journal of Tropical Medicine and Hygiene 54, 18–26.CrossRefGoogle Scholar
FARNERT, A., SNOUNOU, G., ROOTH, I. & BJORKMAN, A. (1997). Daily dynamics of Plasmodium falciparum subpopulations in asymptomatic children in a holoendemic area. American Journal of Tropical Medicine and Hygiene 56, 538–547.CrossRefGoogle Scholar
FONDJO, E., ROBERT, V., LE GOFF, G., TOTO, J. C. & CARNEVALE, P. (1992). Le paludisme urbain à Yaoundé, Cameroun. 2. Etude entomologique dans deux quartiers peu urbanisés. Bulletin de la Société de Pathologie Exotique 85, 57–63.Google Scholar
FONTENILLE, D., LOCHOUARN, L., DIAGNE, N., SOKHNA, C. S., LEMASSON, J.-J., DIATTA, M., KONATE, L., FAYE, F., ROGIER, C. & TRAPE, J.-F. (1997). High annual and seasonal variations in malaria transmission by anophelines and vector species composition in Dielmo, a holoendemic area in Senegal. American Journal of Tropical Medicine and Hygiene 56, 247–253.CrossRefGoogle Scholar
JAMES, S. P. (1931). Some general results of a study of induced malaria in England. Transactions of the Royal Society of Tropical Medicine and Hygiene 24, 477–538.CrossRefGoogle Scholar
KONATE, L., ZWETYANGA, J., ROGIER, C., BISCHOFF, E., FONTENILLE, D., TALL, A., SPIEGEL, A., TRAPE, J.-F. & MERCEREAU-PUIJALON, O. (1999). The epidemiology of multiple Plasmodium falciparum infections. 5. Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, S1/21–S2/28.Google Scholar
LAVERAN, A. (1880). Note sur un nouveau parasite trouvé dans le sang de plusieurs malades atteints de fièvre palustre. Bulletin de l'Académie Nationale de Médecine (Paris) 9, 1235.Google Scholar
MANGA, L., ROBERT, V., MESSI, J., DESFONTAINE, M. & CARNEVALE, P. (1992). Le paludisme urbain à Yaoundé, Cameroun. 1. Etude entomologique dans deux quartiers centraux. Mémoire de la Société Royale Belge d'Entomologie 35, 155–162.Google Scholar
PAUL, R. E. L., BREY, P. T. & ROBERT, V. (2002). Plasmodium sex determination and transmission to mosquitoes. Trends in Parasitology 18, 32–38.CrossRefGoogle Scholar
PAUL, R. E. L., COULSON, T. N., RAIBAUD, A. & BREY, P. T. (2000). Sex determination in malaria parasites. Science 287, 128–131.CrossRefGoogle Scholar
PAUL, R. E. L., PACKER, M. J., WALMSLEY, M., LAGOG, M., RANFORD-CARTWRIGHT, L. C., PARU, R. & DAY, K. P. (1995). Mating patterns in malaria parasite populations of Papua New Guinea. Science 269, 10709–11711.CrossRefGoogle Scholar
PICKERING, J., READ, A. F., GUERRERO, S. & WEST, S. A. (2000). Sex ratio and virulence in two species of lizard malaria parasites. Evolutionary Ecology Research 2, 171–184.Google Scholar
READ, A. F., NARARA, A., NEE, S., KEYMER, A. E. & DAY, K. P. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, 387–395.CrossRefGoogle Scholar
ROBERT, V., READ, A. F., ESSONG, J., TCHUINKAM, T., MULDER, B., VERHAVE, J. P. & CARNEVALE, P. (1996). Effect of gametocyte sex ratio in infectivity of Plasmodium falciparum to Anopheles gambiae. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 621–624.CrossRefGoogle Scholar
SCHALL, J. J. (2000). Transmission success of the malaria Plasmodium maxicanum into its vector: role of gametocyte density and sex ratio. Parasitology 121, 575–580.Google Scholar
SHUTE, P. G. & MARYON, M. (1951). A study of gametocytes in a West African strain of Plasmodium falciparum. Transactions of the Royal Society of Tropical Medicine and Hygiene 44, 421–438.CrossRefGoogle Scholar
SILVESTRINI, F., ALANO, P. & WILLIAMS, J. L. (2000). Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121, 465–471.CrossRefGoogle Scholar
SMALLEY, M. E. & SINDEN, R. E. (1977). Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74, 1–8.CrossRefGoogle Scholar
SMITH, T. G., LOURENÇO, P., CARTER, R., WALLIKER, D. & RANFORD-CARTWRIGHT, L. C. (2000). Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology 121, 127–133.CrossRefGoogle Scholar
TAYLOR, L. H. (1997). Epidemiological and evolutionary consequences of mixed-genotype infections of malaria parasites. Ph.D. thesis, University of Edinburgh, Edinburgh.
TAYLOR, P. J. & HURD, H. (2001). The influence of host haematocrit on the blood feeding success of Anopheles stephensi: implication for enhanced malaria transmission. Parasitology 122, 491–496.CrossRefGoogle Scholar
TRAGER, W., TERSHAKOVEC, M., LYANDVERT, L., STANLEY, H., LANNERS, H. N. & GUBERT, E. (1981). Clones of the malaria parasite Plasmodium falciparum obtained by microscopic selection: their characterisation with regards to knobs, chloroquine sensitivity, and formation of gametocytes. Proceedings of the National Academy of Sciences, USA 78, 6527–6530.CrossRefGoogle Scholar
TRAPE, J.-F., ROGIER, C., KONATE, L., DIAGNE, N., BOUGANALI, H., CANQUE, B., LEGROS, F., BADJI, A., NDIAYE, G., NDIAYE, P., BRAHIMI, K., FAYE, O., DRUILHE, P. & DA SILVA, L. P. (1994). The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. American Journal of Tropical Medicine and Hygiene 51, 123–137.CrossRefGoogle Scholar
WEST, S. A., REECE, S. E. & READ, A. F. (2001). Gametocyte sex ratios of malaria and related apicomplexan (protozoa) parasites. Trends in Parasitology 17, 525–531.CrossRefGoogle Scholar
WEST, S. A., SMITH, T. G., NEE, S. & READ, A. F. (2002). Fertility insurance and the sex ratio of malaria and related hemospororin blood parasites. Journal of Parasitology 88, 258–263.CrossRefGoogle Scholar
ZEGER, S. & LIANG, K. (1986). Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42, 121–130.CrossRefGoogle Scholar