Epidemiology and Infectivity of Plasmodium falciparum and Plasmodium vivax Gametocytes in Relation to Malaria Control and Elimination

Clinical Microbiology Reviews - Tập 24 Số 2 - Trang 377-410 - 2011
Teun Bousema1, Chris Drakeley1
1Department of Immunology & Infection, London School of Hygiene and Tropical Medicine, London W1CE 7HT, United Kingdom

Tóm tắt

SUMMARYMalaria remains a major cause of morbidity and mortality in the tropics, withPlasmodium falciparumresponsible for the majority of the disease burden andP. vivaxbeing the geographically most widely distributed cause of malaria. Gametocytes are the sexual-stage parasites that infectAnophelesmosquitoes and mediate the onward transmission of the disease. Gametocytes are poorly studied despite this crucial role, but with a recent resurgence of interest in malaria elimination, the study of gametocytes is in vogue. This review highlights the current state of knowledge with regard to the development and longevity ofP. falciparumandP. vivaxgametocytes in the human host and the factors influencing their distribution within endemic populations. The evidence for immune responses, antimalarial drugs, and drug resistance influencing infectiousness to mosquitoes is reviewed. We discuss how the application of molecular techniques has led to the identification of submicroscopic gametocyte carriage and to a reassessment of the human infectious reservoir. These components are drawn together to show how control measures that aim to reduce malaria transmission, such as mass drug administration and a transmission-blocking vaccine, might better be deployed.

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Tài liệu tham khảo

10.1086/340638

10.1126/science.1132338

10.1016/S0140-6736(03)15162-8

10.4269/ajtmh.2000.63.199

10.1111/j.1365-2958.2007.05904.x

10.1016/0166-6851(95)02491-3

10.1016/j.trstmh.2005.04.021

Alves F. P. . 2005. Asymptomatic carriers of Plasmodium spp . as infection source for malaria vector mosquitoes in the Brazilian Amazon. J. Med. Entomol. 42:777–779.

. 1887. Haematozoa of malaria. Br. Med. J. 1887:960–961.

10.1016/S0140-6736(07)61609-2

10.1016/S0140-6736(09)61258-7

10.1128/IAI.73.11.7375-7380.2005

10.1086/425015

10.1086/432011

10.4269/ajtmh.1998.59.582

10.1016/S0166-6851(98)00175-3

10.1088/1748-6041/3/3/034007

10.1016/j.pt.2008.08.001

10.1371/journal.pone.0007459

10.1128/CMR.00008-09

10.4269/ajtmh.1991.44.183

10.1016/j.pt.2010.08.005

10.1016/j.molbiopara.2010.03.019

10.1017/S0031182000068219

10.1186/1475-2875-8-S1-S8

10.1371/journal.pmed.0020330

10.1086/587645

10.1016/j.actatropica.2005.04.014

10.1084/jem.174.5.1203

10.1186/1475-2875-4-15

10.4269/ajtmh.1998.59.823

10.1016/j.ijpara.2010.04.010

10.1186/1475-2875-5-104

10.1371/journal.pmed.1000304

10.4269/ajtmh.2009.81.366

10.4269/ajtmh.2006.75.610

10.1371/journal.pmed.0040309

10.1038/32667

10.1017/S0031182097008895

Birku Y. Mekonnen E. Bjorkman A. Wolday D. . 2002. Delayed clearance of Plasmodium falciparum in patients with human immunodeficiency virus co-infection treated with artemisinin. Ethiop. Med. J. 40(Suppl. 1):17–26.

10.1080/00034983.2000.11813562

10.1016/j.vaccine.2009.06.069

10.1016/j.vaccine.2010.06.100

10.1186/1475-2875-5-15

10.1016/j.pt.2005.08.012

10.1080/00034983.1991.11812580

10.4269/ajtmh.1993.48.700

Boudin C. Robert V. Verhave J. P. Carnevale P. Ambroise-Thomas P. . 1991. Plasmodium falciparum and P. malariae epidemiology in a West African village. Bull. World Health Organ. 69:199–205.

10.1111/j.0141-9838.2004.00689.x

10.1084/jem.182.2.409

10.1111/j.1365-3024.2007.00948.x

10.4269/ajtmh.2008.78.442

10.2174/156652406776055140

10.1186/1475-2875-3-18

10.1046/j.1365-3156.2003.01047.x

10.4269/ajtmh.2006.74.425

10.1086/503051

10.1086/652456

10.1186/1475-2875-9-136

10.1371/journal.pone.0014114

10.1016/j.ijpara.2010.09.008

10.3201/eid1603.090732

10.4269/ajtmh.1937.s1-17.253

Boyd M. F. Stratman-Thomas W. K. Muench H. . 1935. The occurrence of gametocytes of Plasmodium vivax during the primary attack. Am. J. Trop. Med. Hyg. 16:133–138.

10.1186/1475-2875-4-27

10.1016/0020-7519(76)90025-4

Brewer G. J. Zarafonetis C. J. . 1967. The haemolytic effect of various regimens of primaquine with chloroquine in American Negroes with G6PD deficiency and the lack of an effect of various antimalarial suppressive agents on erythrocyte metabolism. Bull. World Health Organ. 36:303–308.

10.1111/j.1550-7408.1982.tb05432.x

10.1016/S0166-6851(99)00201-7

10.1017/S0031182000061199

10.1016/0166-6851(94)90111-2

10.1016/j.parint.2010.05.008

10.1006/expr.1999.4429

10.1017/S0031182099003960

10.1098/rspb.2001.1808

10.1371/journal.pctr.0010007

Burgess R. W. Bray R. S. . 1961. The effect of a single dose of primaquine on the gametocytes, gametogony and sporogony of Laverania falciparum . Bull. World Health Organ. 24:451–456.

10.1016/0035-9203(84)90114-7

10.1016/S0020-7519(97)00079-9

10.1016/j.ijpara.2009.11.006

10.1007/BF00418523

10.1038/nature01099

10.1038/263057a0

Carter R. Graves P. M. . 1988. Gametocytes, p. 253–306. In Wernsdorfer W. H. McGregor I. A. (ed.), Malaria: principles and practice of malariology. Churchill Livingstone, Edinburgh, United Kingdom.

10.1016/0014-4894(89)90182-3

10.1084/jem.169.1.135

Carter R. Mendis K. N. Roberts D. . 2000. Spatial targeting of interventions against malaria. Bull. World Health Organ. 78:1401–1411.

Carter R. Miller L. H. . 1979. Evidence for environmental modulation of gametocytogenesis in Plasmodium falciparum in continuous culture. Bull. World Health Organ. 57(Suppl. 1):37–52.

10.1016/S0140-6736(08)61654-2

10.2307/3281273

10.1016/0166-6851(94)90020-5

10.4049/jimmunol.0901331

Chardome M. Janssen P. J. . 1952. Enquête sur l'incidence malarienne par la method dermique dans la region de Lubilash (Congo Belge). Ann. Soc. Belge Med. Trop. 32:209–211.

Charoenlarp P. Areekul S. Harinasuta T. Sirivorasarn P. . 1972. The haemolytic effect of a single dose of 45 mg of primaquine in G-6-PD deficient Thais. J. Med. Assoc. Thai. 55:631–638.

10.1111/j.1365-3156.2004.01217.x

10.1128/CMR.13.3.439

10.1016/j.vaccine.2010.04.036

10.1128/AAC.01472-05

10.1371/journal.pone.0006352

Colbourne M. J . 1956. The effect of prolonged examination of bloodfilms on the parasite rate. West Afr. Med. J. 5:26–30.

10.4269/ajtmh.1990.42.196

10.4269/ajtmh.1992.46.169

10.1603/0022-2585-41.2.201

10.1016/S0166-6851(01)00278-X

10.1371/journal.pone.0005318

Covell G. Coatney G. R. Field J. W. Singh J. . 1955. Chemotherapy of malaria. Monogr. Ser. World Health Organ. 27:1–123.

10.1017/S0031182000084985

10.1016/S0166-6851(98)00040-1

10.1073/pnas.90.17.8292

10.1111/j.1365-2958.2007.06039.x

10.1046/j.1365-3156.2001.00723.x

Dern R. J. Beutler E. Alving A. S. . 1954. The hemolytic effect of primaquine. II. The natural course of the hemolytic anemia and the mechanism of its self-limited character. J. Lab. Clin. Med. 44:171–176.

10.1186/1475-2875-7-248

10.1073/pnas.0702239104

10.1016/j.pt.2008.01.004

10.1038/nrmicro2331

10.1128/CMR.00025-08

10.4269/ajtmh.2000.62.686

10.1001/jama.297.20.2210

10.1016/S1473-3099(10)70079-7

Dowling M. A. Shute G. T. . 1966. A comparative study of thick and thin blood films in the diagnosis of scanty malaria parasitaemia. Bull. World Health Organ. 34:249–267.

10.1016/j.pt.2006.07.001

10.1016/S0035-9203(00)90056-7

10.1111/j.1365-3024.2005.00818.x

10.1086/429669

10.1016/0166-6851(96)02718-1

10.1111/j.0141-9838.2004.00696.x

10.1080/00034983.2000.11813555

10.1046/j.1365-3156.2003.01169.x

10.1017/S0031182098002601

10.1046/j.1365-3156.1999.00361.x

10.1128/iai.65.3.1109-1113.1997

10.1371/journal.pctr.0010020

10.1016/S0166-6851(00)00205-X

10.1016/S0169-4758(99)01608-7

Reference deleted.

Reference deleted.

10.1016/S0035-9203(01)90016-1

10.1111/j.1365-2958.2006.05284.x

10.1016/j.molbiopara.2005.05.010

10.1046/j.1365-2958.2002.02986.x

10.1371/journal.pone.0001311

Elzaki S. G. Gadalla N. B. H. Mansour F. A. Mukhtar E. A. El-Sayed B. B. . 2006. The impact of clearance of the dry season sub-patent parasitaemia on the prevalence of Plasmodium falciparum in Eastern Sudan, abstr. 1172. Abstr. ICOPA XI Conf., Glasgow, United Kingdom.

Enevold A . 2006. The influence of genetic innate resistance and acquired immunity on drug treatment outcome of uncomplicated Plasmodium falciparum malaria in Tanzania. Parassitologia 48:547–551.

10.4269/ajtmh.2006.74.944

10.1016/j.trstmh.2006.06.010

10.1016/S0264-410X(03)00265-2

10.1186/1475-2875-6-80

Faye B. . 2010. Efficacy and tolerability of artesunate-amodiaquine (Camoquin Plus) versus artemether-lumefantrine (Coartem) against uncomplicated Plasmodium falciparum malaria: multisite trial in Senegal and Ivory Coast. Trop. Med. Int. Health 15:608–613.

10.4269/ajtmh.2000.62.291

10.1038/nature01107

10.1097/00002030-200105040-00010

10.4269/ajtmh.1991.45.479

10.1111/j.1365-3024.1992.tb00013.x

10.1051/parasite/2007142135

10.1016/j.molbiopara.2004.12.010

10.1038/nature01097

10.1016/S0001-706X(00)00174-1

10.2307/3284196

George J. N. Sears D. A. McCurdy P. R. Conrad M. E. . 1967. Primaquine sensitivity in Caucasians: hemolytic reactions induced by primaquine in G-6-PD deficient subjects. J. Lab. Clin. Med. 70:80–93.

10.1128/IAI.72.11.6359-6366.2004

10.1016/0035-9203(92)90216-Y

10.1111/j.1365-2915.1993.tb00708.x

10.1179/000349804225003541

10.1186/1471-2334-6-16

10.1038/ng.554

10.1017/S003118200300444X

10.1016/S0035-9203(03)80108-6

10.1016/S0035-9203(99)90082-2

10.1128/IAI.66.1.59-64.1998

10.1371/journal.pone.0001101

10.1016/0035-9203(80)90189-3

10.1017/S003118200005825X

10.1111/j.1365-3024.1988.tb00215.x

10.4269/ajtmh.1984.33.1045

10.1111/j.1365-3156.2007.01993.x

10.1086/596741

10.1016/0035-9203(91)90015-Q

10.1371/journal.pmed.1000324

10.1371/journal.pmed.0050038

10.1371/journal.pntd.0000774

10.1016/S0065-308X(05)62005-2

10.1126/science.959832

10.1126/science.1103717

10.1371/journal.pctr.0010015

10.1128/AAC.48.10.3940-3943.2004

10.1016/j.trstmh.2004.10.003

Han E. T. . 2010. Sequence polymorphisms of Plasmodium vivax ookinete surface proteins (Pvs25 and Pvs28) from clinical isolates in Korea. Trop. Med. Int. Health 9:1072–1076.

10.1128/JCM.02117-06

10.1016/S0035-9203(96)90325-9

10.1086/512677

10.1016/0035-9203(71)90036-8

10.1371/journal.pmed.1000290

10.1016/S0166-6851(00)00191-2

10.1073/pnas.96.8.4563

10.1128/IAI.67.5.2334-2339.1999

10.1017/S0031182099005041

10.1128/iai.65.8.3017-3023.1997

10.4269/ajtmh.2006.75.402

10.1016/S0065-308X(05)61003-2

10.1016/j.cub.2008.03.045

10.1016/j.actatropica.2009.08.005

10.1128/IAI.68.12.6618-6623.2000

10.4269/ajtmh.1998.58.176

10.3346/jkms.2011.26.1.42

10.1186/1475-2875-7-64

10.1186/1475-2875-4-46

10.1016/0035-9203(87)90271-9

10.1016/S0035-9203(31)90068-0

10.4269/ajtmh.1952.1.612

10.4269/ajtmh.1958.7.207

10.4269/ajtmh.1955.4.781

Jeffery G. M. Young M. D. Eyles D. E. . 1956. The treatment of Plasmodium falciparum infection with chloroquine, with a note on infectivity to mosquitoes of primaquine- and pyrimethamine-treated cases. Am. J. Hyg. (London) 64:1–11.

10.1086/498577

10.1371/journal.pctr.0020020

10.1016/S0140-6736(00)03127-5

Kar P. K. Dua V. K. Gupta N. C. Gupta A. Dash A. P. . 2009. Plasmodium falciparum gametocytaemia with chloroquine chemotherapy in persistent malaria in an endemic area of India. Indian J. Med. Res. 129:299–304.

10.1186/1475-2875-7-66

10.1186/1475-2875-8-98

10.1111/j.1365-2249.1992.tb06478.x

10.1038/333074a0

10.1016/j.cell.2005.03.027

10.4269/ajtmh.2010.09-0378

10.1038/220191a0

Klein T. A. Harrison B. A. Grove J. S. Dixon S. V. Andre R. G. . 1986. Correlation of survival rates of Anopheles dirus A (Diptera: Culicidae) with different infection densities of Plasmodium cynomolgi . Bull. World Health Organ. 64:901–907.

10.1590/S0074-02761992000700066

10.4269/ajtmh.1991.44.604

10.4269/ajtmh.1991.45.471

10.4269/ajtmh.2009.80.882

10.1016/0166-6851(93)90158-T

10.1016/j.ijpara.2010.05.004

10.1016/j.vaccine.2003.11.060

10.1073/pnas.0609885104

10.1111/j.1365-3024.1987.tb00511.x

10.1016/0166-6851(84)90124-5

10.1016/0166-6851(85)90032-5

10.1007/BF00930817

10.1016/0169-4758(95)80079-4

10.1016/0140-6736(90)92827-5

10.1371/journal.pbio.0030298

10.1038/nature01111

10.1371/journal.pone.0011358

10.1186/1475-2875-8-159

10.4269/ajtmh.2001.64.247

10.1006/expr.1998.4354

10.1086/515263

10.1016/S0035-9203(96)90464-2

10.1128/iai.65.9.3834-3837.1997

10.1126/science.1087025

10.1001/jama.297.20.2201

10.1086/432552

Lingnau A. Margos G. Maier W. A. Seitz H. M. . 1993. The effects of hormones on the gametocytogenesis of Plasmodium falciparum in vitro. Appl. Parasitol. 34:153–160.

10.1101/gad.1656508

10.1128/IAI.67.4.1688-1693.1999

10.1016/S1097-2765(01)80011-3

10.1016/0035-9203(94)90273-9

10.1186/1475-2875-7-216

10.1016/j.actatropica.2008.05.001

10.1016/S0001-706X(00)00110-8

10.1016/0169-4758(87)90063-9

10.1126/science.1125129

10.1371/journal.ppat.1000767

10.1086/526529

10.1016/j.vaccine.2004.12.019

10.1186/1475-2875-8-12

10.7150/ijbs.1.96

10.1080/00034983.1985.11811968

10.1086/424512

10.1182/blood.V96.9.3231

10.1645/GE-1052R.1

10.4269/ajtmh.2002.67.411

10.1645/0022-3395(2002)088[0521:PVBSD]2.0.CO;2

10.1645/GE-911R.1

McMahon J. E. Marshall T. F. Vaughan J. P. Kolstrup N. . 1979. Tanzania Filariasis Project: a provocative day test with diethylcarbamazine for the detection of microfilariae of nocturnally periodic Wuchereria bancrofti in the blood. Bull. World Health Organ. 57:759–765.

10.1128/IAI.72.11.6597-6602.2004

10.4269/ajtmh.2007.77.438

10.1093/aje/kwf030

Mendis K. . 2009. From malaria control to eradication: the WHO perspective. Trop. Med. Int. Health 14:802–809.

10.1016/S0166-6851(00)00314-5

10.1016/S1473-3099(07)70024-5

10.1186/1475-2875-7-237

10.1016/0014-4894(87)90040-3

10.1016/0035-9203(60)90026-2

10.1016/j.ibmb.2005.02.009

10.1016/0035-9203(58)90036-1

Mitri C. Thiery I. Bourgouin C. Paul R. E. . 2009. Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proc. Biol. Sci. 276:3721–3726.

10.1128/IAI.00306-10

10.4269/ajtmh.2008.78.114

10.1111/j.1365-3156.2005.01427.x

10.1111/j.1365-3156.2005.01471.x

Molineaux L. Gramiccia G. . 1980. The Garki Project. Research on the epidemiology and control of malaria in the Sudan savannah of West Africa. World Health Organization Geneva Switzerland.

10.4269/ajtmh.1980.29.725

Mons B . 1986. Intra erythrocytic differentiation of Plasmodium berghei . Acta Leiden. 54:1–124.

10.1128/CMR.15.1.66-78.2002

10.1016/S0140-6736(10)61269-X

10.1038/ncb1345

10.1093/intimm/7.1.147

10.1016/S1473-3099(09)70177-X

10.1016/0035-9203(54)90067-X

10.4269/ajtmh.1957.6.971

10.1080/00034983.1998.11813355

10.1006/expr.1999.4398

10.1016/S0035-9203(98)91061-6

10.1186/1475-2883-5-8

10.1086/430006

10.1016/j.mehy.2003.11.011

10.1016/S0306-9877(02)00265-7

10.1016/j.trstmh.2003.10.005

10.1179/000349804225003145

10.1128/AAC.48.7.2751-2752.2004

10.4269/ajtmh.2004.71.693

10.1645/0022-3395(2002)088[0097:DHCHAS]2.0.CO;2

10.1016/0014-4894(90)90035-B

10.1084/jem.173.3.523

Naotunne T. S. Karunaweera N. D. Mendis K. N. Carter R. . 1993. Cytokine-mediated inactivation of malarial gametocytes is dependent on the presence of white blood cells and involves reactive nitrogen intermediates. Immunology 78:555–562.

10.1016/j.ijpara.2004.10.014

10.1080/00034983.1997.11813182

10.1016/j.bcmd.2008.12.005

10.1016/0001-706X(94)90117-1

10.1016/S0140-6736(00)02505-8

10.1016/j.ijpara.2007.07.003

10.1371/journal.pone.0004364

10.1186/1475-2875-5-98

10.1097/00062752-199704020-00012

10.1371/journal.pmed.0050226

10.1186/1475-2875-7-125

10.1086/644781

Okell L. C. . The potential contribution of mass treatment to the control of Plasmodium falciparum malaria. PLoS One, in press.

10.1046/j.1365-3156.2001.00752.x

10.1016/S0140-6736(08)61655-4

10.1016/S1473-3099(10)70096-7

10.1016/0020-7519(90)90118-7

Ono T. Nakai T. Nakabayashi T. . 1986. Induction of gametocytogenesis in Plasmodium falciparum by the culture supernatant of hybridoma cells producing anti-P. falciparum antibody. Biken J. 29:77–81.

10.1006/expr.1993.1062

10.1590/S0074-02762002000800026

10.1186/1475-2875-9-281

10.1371/journal.pone.0008410

10.1016/j.actatropica.2007.09.003

10.4269/ajtmh.2007.76.626

10.1073/pnas.0800459105

10.1371/journal.pone.0002530

10.1017/S0031182005009601

10.1016/j.ijpara.2007.05.009

10.1016/0166-6851(93)90224-L

10.1016/S1471-4922(01)02122-5

10.1126/science.287.5450.128

10.1186/1475-2875-3-39

10.1080/15216540050033078

10.1126/science.7569897

10.1086/644645

10.4269/ajtmh.1988.39.26

10.1186/1475-2875-3-34

10.1371/journal.pone.0003779

10.1017/S0031182099006277

10.1016/S0140-6736(05)66416-1

10.1128/IAI.67.12.6369-6374.1999

10.1017/S0031182000062065

10.1016/0035-9203(87)90172-6

10.1017/S0007485300009834

10.1017/S0031182007003381

10.1111/j.1365-3024.1994.tb00302.x

10.4269/ajtmh.1999.60.1019

10.1016/S0140-6736(96)91488-9

10.1128/AAC.44.6.1680-1685.2000

10.1128/AAC.48.4.1329-1334.2004

10.1016/S0035-9203(01)90027-6

10.4269/ajtmh.2008.79.378

10.1093/infdis/169.4.932

10.1046/j.1365-3156.1997.d01-267.x

10.1111/j.1365-2915.2006.00627.x

Quakyi I. A. . 1987. The 230-kDa gamete surface protein of Plasmodium falciparum is also a target for transmission-blocking antibodies. J. Immunol. 139:4213–4217.

10.1016/j.molbiopara.2009.08.004

10.4269/ajtmh.2002.67.39

10.1128/iai.56.7.1820-1824.1988

10.1017/S003118200007935X

10.1016/S0140-6736(07)60160-3

10.1016/j.trstmh.2006.06.008

10.1111/j.1365-3024.1994.tb00305.x

10.2307/3283117

10.1038/nature06954

Reece S. E. Duncan A. B. West S. A. Read A. F. . 2005. Host cell preference and variable transmission strategies in malaria parasites. Proc. Biol. Sci. 272:511–517.

10.1017/S0031182003004013

Reeve P. A. Toaliu H. Kaneko A. Hall J. J. Ganczakowski M. . 1992. Acute intravascular haemolysis in Vanuatu following a single dose of primaquine in individuals with glucose-6-phosphate dehydrogenase deficiency. J. Trop. Med. Hyg. 95:349–351.

10.1084/jem.158.3.976

10.4269/ajtmh.2000.62.210

10.4269/ajtmh.1996.55.350

10.1016/S0035-9203(96)90408-3

10.1017/S0031182003003299

10.4269/ajtmh.1996.54.111

10.1006/expr.1995.1003

10.1046/j.1365-3024.1996.d01-54.x

10.1128/IAI.68.6.3455-3462.2000

Rupp I. . Malaria parasites form filamentous cell-to-cell connections during reproduction in the mosquito midgut. Cell Res., in press.

10.1371/journal.pone.0002280

10.4269/ajtmh.2003.69.529

10.1017/S0031182000060303

10.4269/ajtmh.2003.69.536

Sattler M. A. . 2005. Habitat characterization and spatial distribution of Anopheles sp . mosquito larvae in Dar es Salaam (Tanzania) during an extended dry period. Malar. J. 4:4.

10.1016/j.micinf.2007.02.011

10.1016/0001-706X(93)90013-2

10.1097/QCO.0b013e3282a95e12

10.1017/S0031182000006818

10.1128/AAC.32.6.793

10.4269/ajtmh.2007.76.470

10.1016/j.ijpara.2006.01.002

10.1016/j.molbiopara.2004.03.018

10.1128/JCM.38.11.4072-4075.2000

Schulemann W . 1932. Synthetic anti-malarial preparations. Proc. R. Soc. Med. 25:897–905.

10.1038/nsb899

10.1016/0020-711X(91)90061-Q

10.1128/EC.00029-06

10.1371/journal.pone.0001023

10.1111/j.1365-3156.2007.01821.x

10.1128/AAC.01135-09

Shutler D. Reece S. E. Mullie A. Billingsley P. F. Read A. F. . 2005. Rodent malaria parasites Plasmodium chabaudi and P. vinckei do not increase their rates of gametocytogenesis in response to mosquito probing. Proc. Biol. Sci. 272:2397–2402.

10.1017/S0031182099006691

10.1016/j.molbiopara.2005.04.015

10.1111/j.1550-7408.1993.tb06109.x

Sinclair D. Zani B. Donegan S. Olliaro P. Garner P. . 2009. Artemisinin-based combination therapy for treating uncomplicated malaria. Cochrane Database Syst. Rev. 2009:CD007483.

10.1017/S0031182000050824

10.1016/j.ijpara.2004.10.005

10.1016/S0065-308X(08)60462-5

10.1016/S0065-308X(08)60033-0

Sinden R. E. Gilles H. M. . 2002. The malaria parasites, p. 8–35. In Warrel D. A. Gilles H. M. (ed.), Essential malariology, 4th ed. Hodder Arnold, London, United Kingdom.

10.1016/0035-9203(76)90096-1

10.1016/0035-9203(77)90149-3

10.1016/0035-9203(81)90019-5

10.1016/0035-9203(81)90348-5

10.1017/S0031182000047478

10.1186/1475-2875-8-87

10.1371/journal.pbio.0050042

10.1016/0092-8674(95)90056-X

10.1016/0001-706X(94)00082-C

Smith T. A. Chitnis N. Briet O. J. Tanner M. . Uses of mosquito-stage transmission-blocking vaccines against Plasmodium falciparum . Trends Parasitol., in press.

10.1017/S0031182099006265

10.1128/IAI.71.1.393-400.2003

10.1016/S0140-6736(06)68931-9

10.1016/S1473-3099(10)70187-0

10.1016/0166-6851(93)90077-B

10.1051/parasite/2001083243

10.1186/1475-2875-9-57

10.1186/1475-2875-7-169

10.1590/S0074-02762008000800002

10.1159/000140463

10.1128/AAC.00077-07

10.1051/parasite/2003104363

10.1179/000349803225002381

10.1046/j.1365-3156.2003.01093.x

10.1590/S0074-02762005000400019

10.1017/S0031182004005669

10.4269/ajtmh.2009.09-0394

10.1186/1475-2875-8-297

10.4269/ajtmh.1988.39.337

10.1016/S0140-6736(04)17478-3

10.1186/1475-2875-7-249

10.4269/ajtmh.1986.35.259

10.1111/j.0105-2896.2004.00181.x

10.1016/S0166-6851(01)00225-0

10.1016/j.molbiopara.2009.03.007

10.4269/ajtmh.2002.67.578

10.1371/journal.pmed.0020092

10.1645/0022-3395(2001)087[0928:DOAMFT]2.0.CO;2

10.1086/380468

10.1186/1475-2875-3-24

10.4269/ajtmh.2004.71.739

10.1086/319689

10.1016/0165-2478(88)90148-4

10.1016/S0166-6851(00)00285-1

10.1016/S0169-4758(97)89810-9

10.1017/S0031182001007776

10.2165/00002018-200427010-00003

Tchuinkam T. . 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.

10.1016/S0166-6851(99)00066-3

10.1086/367705

10.1016/S0035-9203(35)90015-3

10.1016/S0035-9203(02)90385-8

10.1093/emboj/20.15.3975

10.4269/ajtmh.1998.59.481

10.1016/j.pt.2005.04.005

10.1111/j.1550-7408.1992.tb01476.x

10.1111/j.1550-7408.1989.tb01079.x

10.1006/expr.1998.4347

10.1126/science.162.3850.273

10.1007/BF03401770

10.1016/S1383-5769(02)00037-5

10.1016/j.pt.2007.09.010

10.1016/j.ejmech.2008.08.011

van den Berghe L. Chardome M. Peel E. . 1952. Supériorité des préparations de scarification du derme sur les préparations de sang périphérique pour le diagnostic de malaria. An. Inst. Med. Trop. 9:553–562.

10.1016/j.trstmh.2005.02.007

10.1017/S0031182004006067

10.1016/j.ijpara.2006.05.004

10.1016/S0035-9203(03)90059-9

10.1016/S0092-8674(01)00199-4

10.1371/journal.ppat.1000853

10.1016/j.pt.2007.08.006

10.1186/1475-2875-7-134

10.1086/507310

10.1016/j.molbiopara.2006.05.015

10.1084/jem.162.5.1460

10.1016/0166-6851(86)90027-7

Vogel G . 2010. The ‘do unto others’ malaria vaccine. Nature 238:847–848.

10.4269/ajtmh.2001.65.523

10.1016/j.pt.2003.08.003

10.1016/S0140-6736(99)10237-X

10.1186/1475-2875-9-147

10.4038/cmj.v47i3.3434

10.1371/journal.pntd.0000653

10.1186/1475-2875-8-212

10.1126/science.1155165

10.1186/1475-2875-7-S1-S8

10.1111/j.1365-3024.2006.00804.x

10.1016/S0140-6736(00)02727-6

10.4269/ajtmh.1999.60.7

10.1046/j.1365-3024.2003.00643.x

10.1016/0166-6851(93)90058-6

10.1016/S0166-6851(96)02621-7

10.1016/0166-6851(95)02507-3

10.1371/journal.pgen.1000882

10.1073/pnas.94.1.338

World Health Organization. 2008. Global malaria control and elimination: report of a technical review. WHO Geneva Switzerland. http://www.who.int/malaria/publications/atoz/9789241596756 .

World Health Organization. 2006. Guidelines for the treatment of malaria. WHO/HTM/MAL/2006.1108. WHO, Geneva, Switzerland.

World Health Organization. 2000. Malaria transmission blocking vaccines: an ideal public good. WHO document number TDR/RBM/MAL/VAC/2000.1. WHO, Geneva, Switzerland.

10.1128/iai.43.2.664-669.1984

10.1371/journal.pone.0002636

10.1073/pnas.0608545103

10.1371/journal.pmed.0020190

10.1371/journal.pone.0002390

10.1016/j.molbiopara.2005.05.007

10.4269/ajtmh.2006.74.568

10.1086/522985

10.1371/journal.pone.0001630

10.1371/journal.pone.0006358