1921
Volume 71, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

species, the etiologic agents of malaria, are obligatory sexual organisms. Gametocytes, the precursors of gametes, are responsible for parasite transmission from human to mosquito. The sex ratio of gametocytes has been shown to have consequences for the success of this shift from vertebrate host to insect vector. We attempted to document the effect of chemotherapy on the sex ratio of two different species: in children from endemic area with uncomplicated malaria treated with chloroquine (CQ) or sulfadoxine-pyrimethamine (SP), and in mice treated with CQ or untreated. The studies involved 53 patients without gametocytes at day 0 (13 CQ and 40 SP) followed for 14 days, and 15 mice (10 CQ and 5 controls) followed for five days. During the course of infection, a positive correlation was observed between the time of the length of infection and the proportion of male gametocytes in both species. No effects of treatment (CQ versus SP for or CQ versus controls for ) on the gametocyte sex ratio were found for either species. This indicates that parasites do not respond to chemotherapy by altering their sex allocation strategy, even though, in the case of , they apparently increase their overall investment in sexual stages. This suggests that malaria parasite species respond to different environmental cues for their sex differentiation and sex determination.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.2004.71.739
2004-12-01
2017-09-23
Loading full text...

Full text loading...

/deliver/fulltext/14761645/71/6/0700739.html?itemId=/content/journals/10.4269/ajtmh.2004.71.739&mimeType=html&fmt=ahah

References

  1. Burkot T, Williams JL, Schneider I, 1984. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg 78 : 339–341.
  2. Bruce MC, Alano P, Duthie S, Carter R, 1990. Commitment of the malaria parasite Plasmodium falciparum to sexual and asexual development. Parasitology 100 : 191–200.
  3. Silvestrini F, Alano P, Williams JL, 2000. Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology 121 : 465–471.
  4. Smith TG, Lourenco P, Carter R, Walliker D, Ranford-Cartwright LC, 2000. Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology 121 : 127–133.
  5. West SA, Smith TG, Nee S, Read AF, 2002. Fertility insurance and the sex ratios of malaria and related hemospororin blood parasites. J Parasitol 88 : 258–263.
  6. Paul REL, Brey PT, Robert V, 2002. Plasmodium sex determination and transmission to mosquitoes. Trends Parasitol 18 : 32–38.
  7. Gardner A, Reece SE, West SA, 2003. Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. J Theor Biol 223 : 515–521.
  8. Read AF, Narara A, Nee S, Keymer AE, Day KP, 1992. Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104 : 387–395.
  9. Read AF, Anwar M, Shutler D, Nee S, 1995. Sex allocation and population structure in malaria and related parasitic protozoa. Proc R Soc Lond B Biol Sci 260 : 359–363.
  10. Nee S, West SA, Read AF, 2002. Inbreeding and parasite sex ratios. Proc R Soc Lond B Biol Sci 269 : 755–760.
  11. Charnov EL, 1982. The Theory of Sex Allocation, Princeton, NJ: Princeton University Press.
  12. West SA, Reece SE, Read AF, 2001. Gametocyte sex ratio of malaria and related Apicomplexa (Protozoa) parasites. Trends Parasitol 17 : 525–531.
  13. Gandon S, Mackinnon MJ, Nee S, Read AF, 2001. Imperfect vaccines and the evolution of pathogen virulence. Nature 414 : 751–756.
  14. Carter R, Miller LH, 1979. Environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bull World Health Organ 57 (suppl 1): 37–52.
  15. McKenzie FE, Jeffery GM, Collins WE, 2001. Plasmodium malariae blood-stage dynamics. J Parasitol 87 : 626–637.
  16. McKenzie FE, Jeffery GM, Collins WE, 2002. Plasmodium vivax blood-stage dynamics. J Parasitol 88 : 521–535.
  17. Paul REL, Ariey F, Robert V, 2003. The evolutionary ecology of Plasmodium. Ecol Lett 6 : 866–880.
  18. Gautret P, Coquelin F, Chabaud AG, Landau I, 1997. The production of gametocytes by rodent Plasmodium species in mice during phenylhydrazine induced reticulocytosis. Acta Parasitol 42 : 65–67.
  19. Paul REL, Coulson TN, Raibaud A, Brey PT, 2000. Sex determination in malaria parasites. Science 287 : 128–131.
  20. Trager W, Gill GS, 1992. Enhanced gametocyte formation in young erythrocytes by Plasmodium falciparum in vitro. J Protozool 39 : 429–432.
  21. Drakeley CJ, Secka I, Correa S, Greenwood BM, Targett GA, 1999. Host haematological factors influencing the transmission of Plasmodium falciparum gametocytes to Anopheles gambiae s.s. mosquitoes. Trop Med Int Health 4 : 131–138.
  22. Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, ter Kuile F, van Vugt M, Chongsuphajaisiddhi T, White NJ, 1999. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am J Trop Med Hyg 60 : 1019–1023.
  23. Robert V, Sokhna CS, Rogier C, Ariey F, Trape J-F, 2003. Sex ratio of Plasmodium falciparum in inhabitants of Dielmo, Senegal. Parasitology 127 : 1–8.
  24. Schall JJ, 2000. Transmission success of the malaria parasite Plasmodium mexicanum into its vector: role of gametocyte density and sex ratio. Parasitology 121 : 575–580.
  25. Boyd MF, 1949. Epidemiology: factors related to the definitive host. Boyd MF, ed. Malariology. Philadelphia: W. B. Saunders, 608–697.
  26. Noden BH, Beadle PS, Vaughan JA, Pumpuni CB, Kent MD, Beier JC, 1994. Plasmodium falciparum: the population structure of mature gametocyte cultures has little effect on their innate fertility. Acta Trop 58 : 13–19.
  27. Boyd MF, Stratman-Thoma WK, Kitchen SF, 1935. On the relative susceptibility of Anopheles quadrimaculatus to Plasmodium vivax and Plasmodium falciparum. Am J Trop Med Hyg 15 : 485–493.
  28. Robert V, Read AF, Essong J, Tchuinkam T, Mulder B, Verhave JP, Carnevale P, 1996. Effect of gametocyte sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae. Trans R Soc Trop Med Hyg 90 : 621–624.
  29. Shute PG, Maryon M, 1951. A study of gametocytes in a west African strain of Plasmodium falciparum. Trans R Soc Trop Med Hyg 44 : 421–438.
  30. Smalley ME, Sinden RE, 1977. Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology 74 : 1–8.
  31. Sowunmi A, Fateye BA, 2003. Gametocyte sex ratios in children with asymptomatic, recrudescent, pyrimethamine-sulfadoxine-resistant, Plasmodium falciparum malaria. Ann Trop Med Parasitol 97 : 671–682.
  32. Sowunmi A, Fateye BA, 2003. Changes in Plasmodium falciparum gametocytaemia in children with chloroquine-sensitive asexual infections. Parasite 10 : 363–369.
  33. Sokhna CS, Trape J-F, Robert V, 2001. Gametocytaemia in Senegalese children with uncomplicated falciparum malaria treated with chloroquine, amodiaquine or sulfadoxine + pyremethamine. Parasite 8 : 243–250.
  34. Carter R, Graves PM, 1988. Gametocytes. Wernsdorfer WH, McGregor I, eds. Malaria: Principles and Practice of Malariology. Edinburgh: Churchill Livingstone, 1–59.
  35. Montalvo-Alvarez A, Landau I, Baccam D, Chabaud AG, Ginsburg H, 1988. Experimental modifications of the circadian rhythm of Plasmodium vinckei petteri following cryopreservation: probable resistance of the merozoite to thawing. C R Acad Sci III 307 : 5–10.
  36. Gautret P, Gantier JC, Baccam D, Miltgen F, Saulai M, Chabaud AG, Landau I, 1996. The gametocytes of Plasmodium vinckei petteri, their morphological stages, periodicity and infectivity. Int J Parasitol 26 : 1095–1101.
  37. Garnham PCC, 1966. Malaria Parasites and Other Haemosporidia. Oxford: Blackwell Scientific.
  38. Ramkaran AE, Peters W, 1969. Infectivity of chloroquine resistant Plasmodium berghei to Anopheles stephensi enhanced by chloroquine treatment. Nature 223 : 635–636.
  39. Hogh B, Gamage-Mendis A, Butcher GA, Thompson R, Begtrup K, Mendis C, Enosse SM, Dgedge M, Barreto J, Eling, Sinden RE, 1998. The differing impact of chloroquine and pyrimethamine/sulfadoxine upon the infectivity of malaria species to the mosquito vector. Am J Trop Med Hyg 58 : 176–182.
  40. Buckling AG, Read AF, 1999. The effect of chloroquine treatment on the infectivity of Plasmodium chabaudi gametocytes. Int J Parasitol 29 : 619–625.
  41. Puta C, Manyando C, 1997. Enhanced gametocyte production in Fansidar-treated Plasmodium falciparum malaria patients: implications for malaria transmission control programmes. Trop Med Int Health 2 : 227–229.
  42. von Seidlein L, Jawara M, Coleman R, Doherty T, Walraven G, Targett G, 2001. Parasitaemia and gametocytaemia after treatment with chloroquine, pyrimethamine/sulfadoxine, and pyrimethamine/sulfadoxine combined with artesunate in young Gambians with uncomplicated malaria. Trop Med Int Health 6 : 92–98.
  43. Enosse S, Butcher GA, Margos G, Mendoza J, Sinden RE, Hogh B, 2000. The mosquito transmission of malaria: the effects of atovaquoneproguanil (Malarone) and chloroquine. Trans R Soc Trop Med Hyg 94 : 77–82.
  44. Wilkinson RN, Noeypatimanondh S, Gould DJ, 1976. Infectivity of falciparum malaria patients for anopheline mosquitoes before and after chloroquine treatment. Trans R Soc Trop Med Hyg 70 : 306–307.
  45. Tchuinkam T, Mulder B, Dechering K, Stoffels H, Verhave JP, Cot M, Carnevale P, Meuwissen JH, Robert V, 1993. Experimental infections of Anopheles gambiae with Plasmodium falciparum of naturally infected gametocyte carriers in Cameroon: factors influencing the infectivity to mosquitoes. Trop Med Parasitol 44 : 271–276.
  46. Peters W, Ramkaran AE, 1980. The chemotherapy of rodent malaria, XXXII. The influence of paminobenzoic acid on the transmission of Plasmodium yoelii and P. berghei by Anopheles stephensi. Ann Trop Med Parasitol 74 : 275–282.
  47. Chutmongkonkul M, Maier WA, Seitz HM, 1992. A new model for testing gametocytocidal effects of some antimalarial drugs on Plasmodium falciparum in vitro. Ann Trop Med Parasitol 86 : 207–215.
  48. Gautret P, Landau I, Tailhardat L, Miltgen F, Coquelin F, Voza T, Chabaud AG, Jacquemin JL, 2000. The effects of subcurative doses of chloroquine on Plasmodium vinckei petteri gametocytes and on their infectivity to mosquitoes. Int J Parasitol 30 : 1193–1198.
  49. Ichimori K, Curtis CF, Targett GA, 1990. The effects of chloroquine on the infectivity of chloroquine-sensitive and -resistant populations of Plasmodium yoelii nigeriensis to mosquitoes. Parasitology 100 : 377–381.
  50. Kappes B, Doerig CD, Graeser R, 1999. An overview of Plasmodium protein kinases. Parasitol Today 15 : 449–454.
  51. Reece SE, Duncan AB, West SA, Read AF, 2003. Sex ratios in the rodent malaria parasite, Plasmodium chabaudi. Parasitology 127 : 419–425.
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.2004.71.739
Loading
/content/journals/10.4269/ajtmh.2004.71.739
Loading

Data & Media loading...

  • Received : 08 Mar 2004
  • Accepted : 09 Jun 2004

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error