Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Malaria Journal
Published in: Malaria Journal 1/2019

Open Access 01-12-2019 | Plasmodium Falciparum | Review

Biology of Plasmodium falciparum gametocyte sex ratio and implications in malaria parasite transmission

Authors: Noëlie Béré Henry, Samuel Sindié Sermé, Giulia Siciliano, Salif Sombié, Amidou Diarra, N’fale Sagnon, Alfred S. Traoré, Sodiomon Bienvenu Sirima, Issiaka Soulama, Pietro Alano

Published in: Malaria Journal | Issue 1/2019

Login to get access

Abstract

While significant advances have been made in understanding Plasmodium falciparum gametocyte biology and its relationship with malaria parasite transmission, the gametocyte sex ratio contribution to this process still remains a relevant research question. The present review discusses the biology of sex determination in P. falciparum, the underlying host and parasite factors, the sex specific susceptibility to drugs, the effect of sex ratio dynamics on malaria parasite transmission and the development of gametocyte sex specific diagnosis tools. Despite the inherent differences across several studies and approaches, the emerging picture highlights a potentially relevant contribution of the P. falciparum gametocyte sex ratio in the modulation of malaria parasite transmission. The increasing availability of molecular methods to measure gametocyte sex ratio will enable evaluation of important parameters, such as the impact of drug treatment on gametocyte sex ratio in vitro and in vivo as well as the changes of gametocyte sex ratios in natural infections, key steps towards elucidating how these parameters affect parasite infectiousness to the mosquito vectors.
Footnotes
1
While this manuscript was in preparation, the topic of this review was covered by an excellent review by Tadesse et al. [103].
 
Literature
1.
WHO. World malaria report 2017. Geneva: World Health Organization; 2017.
2.
Programme RBM. The global malaria action plan for a malaria free world. Geneva: World Health Organization; 2008.
3.
4.
Boudin C, Robert V. Plasmodium falciparum: épidiométrie de la transmission homme-moustique et de l’infection chez le vecteur. Bull Soc Pathol Exot. 2003;96:335–40.PubMed
5.
Hawking F, Wilson ME, Gammage K. Evidence for cyclic development and short-lived maturity in the gametocytes of Plasmodium falciparum. Trans R Soc Trop Med Hyg. 1971;65:549–59.PubMedCrossRef
6.
Smalley ME, Abdalla S, Brown J. The distribution of Plasmodium falciparum in the peripheral blood and bone marrow of Gambian children. Trans R Soc Trop Med Hyg. 1981;75:103–5.PubMedCrossRef
7.
Smalley ME, Sinden RE. Plasmodium falciparum gametocytes: their longevity and infectivity. Parasitology. 1977;74:1–8.PubMedCrossRef
8.
Robert V, Boudin C. Biologie de la transmission homme-moustique du Plasmodium. Bull Soc Pathol Exot. 2003;96:6–20.PubMed
9.
Lensen A, Bril A, van de Vegte M, van Gemert GJ, Eling W, Sauerwein R. Plasmodium falciparum: infectivity of cultured, synchronized gametocytes to mosquitoes. Exp Parasitol. 1999;91:101–3.PubMedCrossRef
10.
11.
Carter LM, Kafsack BFC, Llinάs M, Mideo N, Pollitt LC, Reece SE. Stress and sex in malaria parasites: why does commitment vary? Evol Med Public Health. 2013;2013:135–47.PubMedPubMedCentralCrossRef
12.
Price R, Nosten F, Simpson JA, Luxemburger C, Phaipun L, ter Kuile F, et al. Risk factors for gametocyte carriage in uncomplicated falciparum malaria. Am J Trop Med Hyg. 1999;60:1019–23.PubMedCrossRef
13.
Drakeley CJ, Secka I, Correa S, Greenwood BM, Targett GA. Host haematological factors influencing the transmission of Plasmodium falciparum gametocytes to Anopheles gambiae s.s. mosquitoes. Trop Med Int Health. 1999;4:131–8.PubMedCrossRef
14.
Gbotosho GO, Sowunmi A, Okuboyejo TM, Happi CT, Michael OS, Folarin OA, et al. Plasmodium falciparum gametocyte carriage, emergence, clearance and population sex ratios in anaemic and non-anaemic malarious children. Mem Inst Oswaldo Cruz. 2011;106:562–9.PubMedCrossRef
15.
16.
Ono T, Nakai T, Nakabayashi T. Induction of gametocytogenesis in Plasmodium falciparum by the culture supernatant of hybridoma cells producing anti-P. falciparum antibody. Biken J. 1986;29:77–81.PubMed
17.
Talman AM, Paul RE, Sokhna CS, Domarle O, Ariey F, Trape JF, Robert V. Influence of chemotherapy on the Plasmodium gametocyte sex ratio of mice and humans. Am J Trop Med Hyg. 2004;71:739–44.PubMedCrossRef
18.
Sowunmi A, Fateye BA. Plasmodium falciparum gametocytaemia in Nigerian children: before, during and after treatment with antimalarial drugs. Trop Med Int Health. 2003;8:783–92.PubMedCrossRef
19.
Peatey CL, Skinner-Adams TS, Dixon MW, McCarthy JS, Gardiner DL, Trenholme KR. Effect of antimalarial drugs on Plasmodium falciparum gametocytes. J Infect Dis. 2009;200:1518–21.PubMedCrossRef
20.
Vardo-Zalik AM, Schall JJ. Clonal diversity alters the infection dynamics of a malaria parasite (Plasmodium mexicanum) in its vertebrate host. Ecology. 2009;90:29–36.CrossRef
21.
Bousema JT, Drakeley CJ, Mens PF, Arens T, Houben R, Omar SA, et al. Increased Plasmodium falciparum gametocyte production in mixed infections with P. malariae. Am J Trop Med Hyg. 2008;78:442–8.PubMedCrossRef
22.
McKenzie FE, Jeffery GM, Collins WE. Plasmodium malariae infection boosts Plasmodium falciparum gametocyte production. Am J Trop Med Hyg. 2002;67:411–4.PubMedPubMedCentralCrossRef
23.
Ouedraogo AL, Schneider P, de Kruijf M, Nebie I, Verhave JP, Cuzin-Ouattara N, et al. Age-dependent distribution of Plasmodium falciparum gametocytes quantified by Pfs25 real-time QT-NASBA in a cross-sectional study in Burkina Faso. Am J Trop Med Hyg. 2007;76:626–30.PubMedCrossRef
24.
Carter R, Graves PM. Gametpcytes. In: Wernsdorfer WH, McGregor IA, editors. Malaria principles and practice of malariology, vol. 1. Churchill Livingstone: Edinburgh; 1988. p. 253–306.
25.
Paul RE, Coulson TN, Raibaud A, Brey PT. Sex determination in malaria parasites. Science. 2000;287:128–31.PubMedCrossRef
26.
27.
Reece SE, Duncan AB, West SA, Read AF. Host cell preference and variable transmission strategies in malaria parasites. Proc Biol Sci. 2005;272:511–7.PubMedPubMedCentralCrossRef
28.
Paul RE, Brey PT, Robert V. Plasmodium sex determination and transmission to mosquitoes. Trends Parasitol. 2002;18:32–8.PubMedCrossRef
29.
Robert V, Sokhna CS, Rogier C, Ariey F, Trape JF. Sex ratio of Plasmodium falciparum gametocytes in inhabitants of Dielmo, Senegal. Parasitology. 2003;127:1–8.PubMedCrossRef
30.
Sowunmi A, Gbotosho GO, Happi CT, Folarin OA, Balogun ST. Population structure of Plasmodium falciparum gametocyte sex ratios in malarious children in an endemic area. Parasitol Int. 2009;58:438–43.PubMedPubMedCentralCrossRef
31.
Sowunmi A, Balogun T, Gbotosho GO, Happi CT, Adedeji AA, Bolaji OM, et al. Activities of artemether-lumefantrine and amodiaquine-sulfalene-pyrimethamine against sexual-stage parasites in falciparum malaria in children. Chemotherapy. 2008;54:201–8.PubMedCrossRef
32.
Stone W, Sawa P, Lanke K, Rijpma S, Oriango R, Nyaurah M, et al. A molecular assay to quantify male and female Plasmodium falciparum gametocytes: results from 2 randomized controlled trials using primaquine for gametocyte clearance. J Infect Dis. 2017;216:457–67.PubMedPubMedCentralCrossRef
33.
Delves MJ, Ruecker A, Straschil U, Lelievre J, Marques S, Lopez-Barragan MJ, et al. Male and female Plasmodium falciparum mature gametocytes show different responses to antimalarial drugs. Antimicrob Agents Chemother. 2013;57:3268–74.PubMedPubMedCentralCrossRef
34.
Dicko A, Roh ME, Diawara H, Mahamar A, Soumare HM, Lanke K, et al. Efficacy and safety of primaquine and methylene blue for prevention of Plasmodium falciparum transmission in Mali: a phase 2, single-blind, randomised controlled trial. Lancet Infect Dis. 2018;18:627–39.PubMedPubMedCentralCrossRef
35.
Paul RE, Brey PT, Robert V. Plasmodium sex determination and transmission to mosquitoes. Trends Parasitol. 2002;18:32–8.PubMedCrossRef
36.
Sharma A, Sharma I, Kogkasuriyachai D, Kumar N. Structure of a gametocyte protein essential for sexual development in Plasmodium falciparum. Nat Struct Biol. 2003;10:197–203.PubMedCrossRef
37.
Carter R, Graves P, Creasey A, Byrne K, Read D, Alano P, et al. Plasmodium falciparum: an abundant stage-specific protein expressed during early gametocyte development. Exp Parasitol. 1989;69:140–9.PubMedCrossRef
38.
Alano P. Plasmodium falciparum gametocytes: still many secrets of a hidden life. Mol Microbiol. 2007;66:291–2.PubMedCrossRef
39.
Lobo CA, Konings RNH, Kumar N. Expression of early gametocyte-stage antigens Pfg27 and Pfs16 in synchronized gametocytes and non-gametocyte producing clones of Plasmodium falciparum. Mol Biochem Parasitol. 1994;68:151–4.PubMedCrossRef
40.
Filarsky M, Fraschka SA, Niederwieser I, Brancucci NMB, Carrington E, Carrio E, et al. GDV1 induces sexual commitment of malaria parasites by antagonizing HP1-dependent gene silencing. Science. 2018;359:1259–63.PubMedPubMedCentralCrossRef
41.
Brancucci NMB, Bertschi NL, Zhu L, Niederwieser I, Chin WH, Wampfler R, et al. Heterochromatin protein 1 secures survival and transmission of malaria parasites. Cell Host Microbe. 2014;16:165–76.PubMedCrossRef
42.
Tiburcio M, Dixon MW, Looker O, Younis SY, Tilley L, Alano P. Specific expression and export of the Plasmodium falciparum Gametocyte EXported Protein-5 marks the gametocyte ring stage. Malar J. 2015;14:334.PubMedPubMedCentralCrossRef
43.
Painter HJ, Carrasquilla M, Llinas M. Capturing in vivo RNA transcriptional dynamics from the malaria parasite Plasmodium falciparum. Genome Res. 2017;27:1074–86.PubMedPubMedCentralCrossRef
44.
Silvestrini F, Alano P, Williams JL. Commitment to the production of male and female gametocytes in the human malaria parasite Plasmodium falciparum. Parasitology. 2000;121:465–71.PubMedCrossRef
45.
Smith TG, Lourenco P, Carter R, Walliker D, Ranford-Cartwright LC. Commitment to sexual differentiation in the human malaria parasite, Plasmodium falciparum. Parasitology. 2000;121:127–33.PubMedCrossRef
46.
Bruce MC, Baker DA, Alano P, Rogers NC, Graves PM, Targett GA, Carter R. Sequence coding for a sexual stage specific protein of Plasmodium falciparum. Nucleic Acids Res. 1990;18:3637.PubMedPubMedCentralCrossRef
47.
Kafsack BF, Rovira-Graells N, Clark TG, Bancells C, Crowley VM, Campino SG, et al. A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature. 2014;507:248–52.PubMedPubMedCentralCrossRef
48.
Bancells C, Llora-Batlle O, Poran A, Notzel C, Rovira-Graells N, Elemento O, et al. Revisiting the initial steps of sexual development in the malaria parasite Plasmodium falciparum. Nat Microbiol. 2019;4:144–54.PubMedCrossRef
49.
Kent RS, Modrzynska KK, Cameron R, Philip N, Billker O, Waters AP. Inducible developmental reprogramming redefines commitment to sexual development in the malaria parasite Plasmodium berghei. Nat Microbiol. 2018;3:1206–13.PubMedPubMedCentralCrossRef
50.
51.
Khan SM, Franke-Fayard B, Mair GR, Lasonder E, Janse CJ, Mann M, et al. Proteome analysis of separated male and female gametocytes reveals novel sex-specific Plasmodium biology. Cell. 2005;121:675–87.PubMedCrossRef
52.
Lasonder E, Rijpma SR, van Schaijk BCL, Hoeijmakers WAM, Kensche PR, Gresnigt MS, et al. Integrated transcriptomic and proteomic analyses of P. falciparum gametocytes: molecular insight into sex-specific processes and translational repression. Nucleic Acids Res. 2016;44:6087–101.PubMedPubMedCentralCrossRef
53.
Miao J, Chen Z, Wang Z, Shrestha S, Li X, Li R, Cui L. Sex-specific biology of the human malaria parasite revealed from the proteomes of mature male and female gametocytes. Mol Cell Proteomics. 2017;16:537–51.PubMedPubMedCentralCrossRef
54.
Alano P, Read D, Bruce M, Aikawa M, Kaido T, Tegoshi T, et al. COS cell expression cloning of Pfg377, a Plasmodium falciparum gametocyte antigen associated with osmiophilic bodies. Mol Biochem Parasitol. 1995;74:143–56.PubMedCrossRef
55.
de Koning-Ward TF, Olivieri A, Bertuccini L, Hood A, Silvestrini F, Charvalias K, et al. The role of osmiophilic bodies and Pfg377 expression in female gametocyte emergence and mosquito infectivity in the human malaria parasite Plasmodium falciparum. Mol Microbiol. 2008;67:278–90.PubMedCrossRef
56.
Severini C, Silvestrini F, Sannella A, Barca S, Gradoni L, Alano P. The production of the osmiophilic body protein Pfg377 is associated with stage of maturation and sex in Plasmodium falciparum gametocytes. Mol Biochem Parasitol. 1999;100:247–52.PubMedCrossRef
57.
van Schaijk BCL, van Dijk MR, van de Vegte-Bolmer M, van Gemert G-J, van Dooren MW, Eksi S, et al. Pfs47, paralog of the male fertility factor Pfs48/45, is a female specific surface protein in Plasmodium falciparum. Mol Biochem Parasitol. 2006;149:216–22.PubMedCrossRef
58.
Vermeulen AN, van Deursen J, Brakenhoff RH, Lensen TH, Ponnudurai T, Meuwissen JH. Characterization of Plasmodium falciparum sexual stage antigens and their biosynthesis in synchronised gametocyte cultures. Mol Biochem Parasitol. 1986;20:155–63.PubMedCrossRef
59.
Schneider P, Reece SE, van Schaijk BC, Bousema T, Lanke KH, Meaden CS, et al. Quantification of female and male Plasmodium falciparum gametocytes by reverse transcriptase quantitative PCR. Mol Biochem Parasitol. 2015;199:29–33.PubMedCrossRef
60.
Eksi S, Williamson KC. Male-specific expression of the paralog of malaria transmission-blocking target antigen Pfs230, PfB0400w. Mol Biochem Parasitol. 2002;122:127–30.PubMedCrossRef
61.
Lobo CA, Fujioka H, Aikawa M, Kumar N. Disruption of the Pfg27 locus by homologous recombination leads to loss of the sexual phenotype in P. falciparum. Mol Cell. 1999;3:793–8.PubMedCrossRef
62.
Miao J, Li J, Fan Q, Li X, Cui L. The Puf-family RNA-binding protein PfPuf2 regulates sexual development and sex differentiation in the malaria parasite Plasmodium falciparum. J Cell Sci. 2010;123:1039–49.PubMedPubMedCentralCrossRef
63.
64.
Paul RE, Brockman A, Price RN, Luxemburger C, White NJ, Looareesuwan S, et al. Genetic analysis of Plasmodium falciparum infections on the north-western border of Thailand. Trans R Soc Trop Med Hyg. 1999;93:587–93.PubMedCrossRef
65.
Robert V, Read AF, Essong J, Tchuinkam T, Mulder B, Verhave JP, et al. Effect of gametocyte sex ratio on infectivity of Plasmodium falciparum to Anopheles gambiae. Trans R Soc Trop Med Hyg. 1996;90:621–4.PubMedCrossRef
66.
Talman AM, Paul RE, Sokhna CS, Domarle O, Ariey F, Trape JF, et al. Influence of chemotherapy on the Plasmodium gametocyte sex ratio of mice and humans. Am J Trop Med Hyg. 2004;71:739–44.PubMedCrossRef
67.
Bousema T, Drakeley C. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev. 2011;24:377–410.PubMedPubMedCentralCrossRef
68.
Eksi S, Morahan BJ, Haile Y, Furuya T, Jiang H, Ali O, et al. Plasmodium falciparum gametocyte development 1 (Pfgdv1) and gametocytogenesis early gene identification and commitment to sexual development. PLoS Pathog. 2012;8:e1002964.PubMedPubMedCentralCrossRef
69.
Sowunmi A, Balogun ST, Gbotosho GO, Happi CT. Plasmodium falciparum gametocyte sex ratios in children with acute, symptomatic, uncomplicated infections treated with amodiaquine. Malar J. 2008;7:169.PubMedPubMedCentralCrossRef
70.
Sowunmi A, Balogun ST, Gbotosho GO, Happi CT. Influence of anemia on Plasmodium falciparum gametocyte sex ratios in acutely symptomatic children. Open Trop Med J. 2008;1:13–20.CrossRef
71.
Bousema JT, Drakeley CJ, Mens PF, Arens T, Houben R, Omar SA, et al. Increased Plasmodium falciparum gametocyte production in mixed infections with P. malariae. Am J Trop Med Hyg. 2008;78:442–8.PubMedCrossRef
72.
Sowunmi A, Fateye BA, Adedeji AA, Fehintola FA, Happi TC. Risk factors for gametocyte carriage in uncomplicated falciparum malaria in children. Parasitology. 2004;129:255–62.PubMedCrossRef
73.
74.
Sokhna CS, Trape JF, Robert V. Gametocytaemia in Senegalese children with uncomplicated falciparum malaria treated with chloroquine, amodiaquine or sulfadoxine + pyrimethamine. Parasite. 2001;8:243–50.PubMedCrossRef
75.
Sowunmi A, Balogun ST, Gbotosho GO, Happi CT. Plasmodium falciparum gametocyte sex ratios in symptomatic children treated with antimalarial drugs. Acta Trop. 2009;109:108–17.PubMedCrossRef
76.
Rener J, Carter R, Rosenberg Y, Miller LH. Anti-gamete monoclonal antibodies synergistically block transmission of malaria by preventing fertilization in the mosquito. Proc Natl Acad Sci USA. 1980;77:6797–9.PubMedCrossRef
77.
Carter R, Gwadz RW, Green I. Plasmodium gallinaceum: transmission-blocking immunity in chickens. II. The effect of antigamete antibodies in vitro and in vivo and their elaboration during infection. Exp Parasitol. 1979;47:194–208.PubMedCrossRef
78.
Khan SM, Reece SE, Waters AP, Janse CJ, Kaczanowski S. Why are male malaria parasites in such a rush? Sex-specific evolution and host-parasite interactions. Evol Med Public Health. 2013;2013:3–13.PubMedCrossRef
79.
Reece SE, Drew DR, Gardner A. Sex ratio adjustment and kin discrimination in malaria parasites. Nature. 2008;453:609–14.PubMedCrossRef
80.
Read AF, Anwar M, Shutler D, Nee S. Sex allocation and population structure in malaria and related parasitic protozoa. Proc Biol Sci. 1995;260:359–63.PubMedCrossRef
81.
82.
WHO. Guidelines for the treatment of malaria. 2nd ed. Geneva: World Health Organization; 2010.
83.
Drakeley CJ, Jawara M, Targett GA, Walraven G, Obisike U, Coleman R, et al. Addition of artesunate to chloroquine for treatment of Plasmodium falciparum malaria in Gambian children causes a significant but short-lived reduction in infectiousness for mosquitoes. Trop Med Int Health. 2004;9:53–61.PubMedCrossRef
84.
Okell LC, Drakeley CJ, Ghani AC, Bousema T, Sutherland CJ. Reduction of transmission from malaria patients by artemisinin combination therapies: a pooled analysis of six randomized trials. Malar J. 2008;7:125–38.PubMedPubMedCentralCrossRef
85.
White NJ, Ashley EA, Recht J, Delves MJ, Ruecker A, Smithuis FM, et al. Assessment of therapeutic responses to gametocytocidal drugs in Plasmodium falciparum malaria. Malar J. 2014;13:483.PubMedPubMedCentralCrossRef
86.
Hallett RL, Dunyo S, Ord R, Jawara M, Pinder M, Randall A, et al. Chloroquine/sulphadoxine-pyrimethamine for gambian children with malaria: transmission to mosquitoes of multidrug-resistant Plasmodium falciparum. PLoS Clin Trials. 2006;1:e15.PubMedPubMedCentralCrossRef
87.
Barnes KI, Little F, Mabuza A, Mngomezulu N, Govere J, Durrheim D, et al. Increased gametocytemia after treatment: an early parasitological indicator of emerging sulfadoxine-pyrimethamine resistance in falciparum malaria. J Infect Dis. 2008;197:1605–13.PubMedCrossRef
88.
Mitri C, Thiery I, Bourgouin C, Paul RE. Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proc Biol Sci. 2009;276:3721–6.PubMedPubMedCentralCrossRef
89.
Gbotosho GO, Sowunmi A, Happi CT. Kinetics of Plasmodium falciparum gametocyte sex ratios: application to the evaluation of the potential of antimalarial drugs to influence malaria transmission. Open Trop Med J. 2011;4:33–8.CrossRef
90.
91.
Ouédraogo AL, Bousema T, Schneider P, de Vlas SJ, Ilboudo-Sanogo E, Cuzin-Ouattara N, et al. Substantial contribution of submicroscopical Plasmodium falciparum gametocyte carriage to the infectious reservoir in an area of seasonal transmission. PLoS ONE. 2009;4:e8410.PubMedPubMedCentralCrossRef
92.
Okell LC, Ghani AC, Lyons E, Drakeley CJ. Submicroscopic infection in Plasmodium falciparum-endemic populations: a systematic review and meta-analysis. J Infect Dis. 2009;200:1509–17.PubMedCrossRef
93.
Menegon M, Severini C, Sannella A, Paglia MG, Sangare D, Abdel-Wahab A, et al. Genotyping of Plasmodium falciparum gametocytes by reverse transcriptase polymerase chain reaction. Mol Biochem Parasitol. 2000;111:153–61.PubMedCrossRef
94.
95.
Kaslow DC, Syin C, McCutchan TF, Miller LH. Comparison of the primary structure of the 25 kDa ookinete surface antigens of Plasmodium falciparum and Plasmodium gallinaceum reveal six conserved regions. Mol Biochem Parasitol. 1989;33:283–7.PubMedCrossRef
96.
Santolamazza F, Avellino P, Siciliano G, Yao FA, Lombardo F, Ouedraogo JB, et al. Detection of Plasmodium falciparum male and female gametocytes and determination of parasite sex ratio in human endemic populations by novel, cheap and robust RTqPCR assays. Malar J. 2017;16:468.PubMedPubMedCentralCrossRef
97.
Meerstein-Kessel L, Andolina C, Carrio E, Mahamar A, Sawa P, Diawara H, et al. A multiplex assay for the sensitive detection and quantification of male and female Plasmodium falciparum gametocytes. Malar J. 2018;17:441–52.PubMedPubMedCentralCrossRef
98.
Burkot TR, Williams JL, Schneider I. Infectivity to mosquitoes of Plasmodium falciparum clones grown in vitro from the same isolate. Trans R Soc Trop Med Hyg. 1984;78:339–41.PubMedCrossRef
99.
West SA, Smith TG, Nee S, Read AF. Fertility insurance and the sex ratios of malaria and related hemospororin blood parasites. J Parasitol. 2002;88:258–63.PubMedCrossRef
100.
Gardner A, Reece SE, West SA. Even more extreme fertility insurance and the sex ratios of protozoan blood parasites. J Theor Biol. 2003;223:515–21.PubMedCrossRef
101.
Bradley J, Stone W, Da DF, Morlais I, Dicko A, Cohuet A, et al. Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density. Elife. 2018;7:e34463.PubMedPubMedCentralCrossRef
102.
Birkholtz LM, Coetzer TL, Mancama D, Leroy D, Alano P. Discovering new transmission-blocking antimalarial compounds: challenges and opportunities. Trends Parasitol. 2016;32:669–81.PubMedCrossRef
103.
Tadesse FG, Meerstein-Kessel L, Goncalves BP, Drakeley C, Ranford-Cartwright L, Bousema T. Gametocyte sex ratio: the key to understanding Plasmodium falciparum transmission? Trends Parasitol. 2019;35:226–38.PubMedCrossRefPubMedCentral
Metadata
Title
Biology of Plasmodium falciparum gametocyte sex ratio and implications in malaria parasite transmission
Authors
Noëlie Béré Henry
Samuel Sindié Sermé
Giulia Siciliano
Salif Sombié
Amidou Diarra
N’fale Sagnon
Alfred S. Traoré
Sodiomon Bienvenu Sirima
Issiaka Soulama
Pietro Alano
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2019
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-019-2707-0

Other articles of this Issue 1/2019

Malaria Journal 1/2019 Go to the issue

Research

Malaria prevention in the city of Yaoundé: knowledge and practices of urban dwellers

Review

Biology and bionomics of malaria vectors in India: existing information and what more needs to be known for strategizing elimination of malaria

Review

The past, present and future of anti-malarial medicines

Research

Environmental and sociodemographic factors associated with household malaria burden in the Congo

Research

Using sibship reconstructions to understand the relationship between larval habitat productivity and oviposition behaviour in Kenyan Anopheles arabiensis

Research

The development and evaluation of a self-marking unit to estimate malaria vector survival and dispersal distance
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits