Skip to main content
Top
Published in: Malaria Journal 1/2014

Open Access 01-12-2014 | Research

Anti-sporozoite antibodies as alternative markers for malaria transmission intensity estimation

Authors: Kwadwo A Kusi, Samuel Bosomprah, Daniel Dodoo, Eric Kyei-Baafour, Emmanuel K Dickson, Daniel Mensah, Evelina Angov, Sheetij Dutta, Martha Sedegah, Kwadwo A Koram

Published in: Malaria Journal | Issue 1/2014

Login to get access

Abstract

Background

Reported malaria cases continue to decline globally, and this has been attributed to strategic implementation of multiple malaria control tools. Gains made would however need to be sustained through continuous monitoring to ensure malaria elimination and eradication. Entomological inoculation rate (EIR) is currently the standard tool for transmission monitoring but this is not sensitive enough, especially in areas of very low transmission. Transmission estimation models based on seroconversion rates (λ) of antibodies to Plasmodium falciparum blood stage antigens are gaining relevance. Estimates of λ, which is the measure of transmission intensity, correlate with EIR but are limited by long-term persistence of antibodies to blood stage antigens. Seroprevalence of antibodies to sporozoite antigens may be better alternatives since these antigens usually have shorter immune exposure times. The aim of this study was to develop transmission estimation models based on the seroprevalence of antibodies to two P. falciparum sporozoite antigens (CSP, CelTOS) and compare with models based on the classical blood stage antigen AMA1.

Methods

Antibody levels in archived plasma from three cross-sectional surveys conducted in 2009 in a low transmission area of Southern Ghana were assessed by indirect ELISA. Seroprevalence of antibodies against CSP, CelTOS and AMA1 were fitted to reversible catalytic models to estimate λ and corresponding seroreversion rates (ρ) for each antibody.

Results

Of the three models developed, the anti-CSP model predicted a 13-fold decrease in λ four years prior to the time of sampling (2009). Anti-AMA1 antibodies formed at a four-fold greater rate compared to that of anti-CelTOS antibodies, and anti-CSP antibodies during the period of decreased λ. In contrast, anti-AMA1 antibodies decayed at a five-fold slower rate relative to that of anti-CSP antibodies while anti-AMA1 and anti-CelTOS antibody decay rates were not significantly different. Anti-CSP antibodies were relatively short-lived as they formed at an 11.6-fold slower rate relative to their decay during the period of decreased λ.

Conclusions

These features of anti-CSP antibodies can be exploited for the development of models for predicting seasonal, short-term changes in transmission intensity in malaria-endemic areas, especially as the elimination phase of malaria control is approached.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO: World malaria report. 2012, Geneva, Switzerland: WHO Press, World Health Organization WHO: World malaria report. 2012, Geneva, Switzerland: WHO Press, World Health Organization
2.
go back to reference Endeshaw T, Gebre T, Ngondi J, Graves PM, Shargie EB, Ejigsemahu Y, Ayele B, Yohannes G, Teferi T, Messele A, Zerihun M, Genet A, Mosher AW, Emerson PM, Richards FO: Evaluation of light microscopy and rapid diagnostic test for the detection of malaria under operational field conditions: a household survey in Ethiopia. Malar J. 2008, 7: 118-PubMedCentralCrossRefPubMed Endeshaw T, Gebre T, Ngondi J, Graves PM, Shargie EB, Ejigsemahu Y, Ayele B, Yohannes G, Teferi T, Messele A, Zerihun M, Genet A, Mosher AW, Emerson PM, Richards FO: Evaluation of light microscopy and rapid diagnostic test for the detection of malaria under operational field conditions: a household survey in Ethiopia. Malar J. 2008, 7: 118-PubMedCentralCrossRefPubMed
3.
go back to reference Oesterholt MJ, Bousema JT, Mwerinde OK, Harris C, Lushino P, Masokoto A, Mwerinde H, Mosha FW, Drakeley CJ: Spatial and temporal variation in malaria transmission in a low endemicity area in northern Tanzania. Malar J. 2006, 5: 98-PubMedCentralCrossRefPubMed Oesterholt MJ, Bousema JT, Mwerinde OK, Harris C, Lushino P, Masokoto A, Mwerinde H, Mosha FW, Drakeley CJ: Spatial and temporal variation in malaria transmission in a low endemicity area in northern Tanzania. Malar J. 2006, 5: 98-PubMedCentralCrossRefPubMed
4.
go back to reference Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, Lopes D, Lines J, Mshinda H, Lengeler C, Armstrong SJ, Tanner M, Alonso P: An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003, 8: 767-774.CrossRefPubMed Drakeley C, Schellenberg D, Kihonda J, Sousa CA, Arez AP, Lopes D, Lines J, Mshinda H, Lengeler C, Armstrong SJ, Tanner M, Alonso P: An estimation of the entomological inoculation rate for Ifakara: a semi-urban area in a region of intense malaria transmission in Tanzania. Trop Med Int Health. 2003, 8: 767-774.CrossRefPubMed
5.
go back to reference Mbogo CM, Mwangangi JM, Nzovu J, Gu W, Yan G, Gunter JT, Swalm C, Keating J, Regens JL, Shililu JI, Githure JI, Beier JC: Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg. 2003, 68: 734-742.PubMed Mbogo CM, Mwangangi JM, Nzovu J, Gu W, Yan G, Gunter JT, Swalm C, Keating J, Regens JL, Shililu JI, Githure JI, Beier JC: Spatial and temporal heterogeneity of Anopheles mosquitoes and Plasmodium falciparum transmission along the Kenyan coast. Am J Trop Med Hyg. 2003, 68: 734-742.PubMed
6.
go back to reference Corran P, Coleman P, Riley E, Drakeley C: Serology: a robust indicator of malaria transmission intensity?. Trends Parasitol. 2007, 23: 575-582.CrossRefPubMed Corran P, Coleman P, Riley E, Drakeley C: Serology: a robust indicator of malaria transmission intensity?. Trends Parasitol. 2007, 23: 575-582.CrossRefPubMed
7.
go back to reference O’Meara WP, Collins WE, McKenzie FE: Parasite prevalence: a static measure of dynamic infections. Am J Trop Med Hyg. 2007, 77: 246-249.PubMedCentralPubMed O’Meara WP, Collins WE, McKenzie FE: Parasite prevalence: a static measure of dynamic infections. Am J Trop Med Hyg. 2007, 77: 246-249.PubMedCentralPubMed
8.
go back to reference Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, Amran J, Noor AM, Snow RW, Drakeley C: Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerg Infect Dis. 2010, 16: 392-399.PubMedCentralCrossRefPubMed Bousema T, Youssef RM, Cook J, Cox J, Alegana VA, Amran J, Noor AM, Snow RW, Drakeley C: Serologic markers for detecting malaria in areas of low endemicity, Somalia, 2008. Emerg Infect Dis. 2010, 16: 392-399.PubMedCentralCrossRefPubMed
9.
go back to reference Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya WM, Lemnge MM, Cox J, Reyburn H, Riley EM: Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005, 102: 5108-5113.PubMedCentralCrossRefPubMed Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, Malima R, Lusingu J, Manjurano A, Nkya WM, Lemnge MM, Cox J, Reyburn H, Riley EM: Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005, 102: 5108-5113.PubMedCentralCrossRefPubMed
10.
go back to reference Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, Masika P, Mosha J, Bousema T, Shekalaghe S, Cook J, Corran P, Ghani A, Riley EM, Drakeley C: Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS ONE. 2009, 4: e6083-PubMedCentralCrossRefPubMed Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, Masika P, Mosha J, Bousema T, Shekalaghe S, Cook J, Corran P, Ghani A, Riley EM, Drakeley C: Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS ONE. 2009, 4: e6083-PubMedCentralCrossRefPubMed
11.
go back to reference Braga EM, Carvalho LH, Fontes CJ, Krettli AU: Low cellular response in vitro among subjects with long-term exposure to malaria transmission in Brazilian endemic areas. Am J Trop Med Hyg. 2002, 66: 299-303.PubMed Braga EM, Carvalho LH, Fontes CJ, Krettli AU: Low cellular response in vitro among subjects with long-term exposure to malaria transmission in Brazilian endemic areas. Am J Trop Med Hyg. 2002, 66: 299-303.PubMed
12.
go back to reference Morais CG, Soares IS, Carvalho LH, Fontes CJ, Krettli AU, Braga EM: Antibodies to Plasmodium vivax apical membrane antigen 1: persistence and correlation with malaria transmission intensity. Am J Trop Med Hyg. 2006, 75: 582-587.PubMed Morais CG, Soares IS, Carvalho LH, Fontes CJ, Krettli AU, Braga EM: Antibodies to Plasmodium vivax apical membrane antigen 1: persistence and correlation with malaria transmission intensity. Am J Trop Med Hyg. 2006, 75: 582-587.PubMed
13.
go back to reference Druilhe P, Pradier O, Marc JP, Miltgen F, Mazier D, Parent G: Levels of antibodies to Plasmodium falciparum sporozoite surface antigens reflect malaria transmission rates and are persistent in the absence of reinfection. Infect Immun. 1986, 53: 393-397.PubMedCentralPubMed Druilhe P, Pradier O, Marc JP, Miltgen F, Mazier D, Parent G: Levels of antibodies to Plasmodium falciparum sporozoite surface antigens reflect malaria transmission rates and are persistent in the absence of reinfection. Infect Immun. 1986, 53: 393-397.PubMedCentralPubMed
14.
go back to reference Doolan DL, Southwood S, Freilich DA, Sidney J, Graber NL, Shatney L, Bebris L, Florens L, Dobano C, Witney AA, Appella E, Hoffman SL, Yates JR, Carucci DJ, Sette A: Identification of Plasmodium falciparum antigens by antigenic analysis of genomic and proteomic data. Proc Natl Acad Sci U S A. 2003, 100: 9952-9957.PubMedCentralCrossRefPubMed Doolan DL, Southwood S, Freilich DA, Sidney J, Graber NL, Shatney L, Bebris L, Florens L, Dobano C, Witney AA, Appella E, Hoffman SL, Yates JR, Carucci DJ, Sette A: Identification of Plasmodium falciparum antigens by antigenic analysis of genomic and proteomic data. Proc Natl Acad Sci U S A. 2003, 100: 9952-9957.PubMedCentralCrossRefPubMed
15.
go back to reference Kaiser K, Matuschewski K, Camargo N, Ross J, Kappe SH: Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Mol Microbiol. 2004, 51: 1221-1232.CrossRefPubMed Kaiser K, Matuschewski K, Camargo N, Ross J, Kappe SH: Differential transcriptome profiling identifies Plasmodium genes encoding pre-erythrocytic stage-specific proteins. Mol Microbiol. 2004, 51: 1221-1232.CrossRefPubMed
16.
go back to reference Kariu T, Ishino T, Yano K, Chinzei Y, Yuda M: CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol. 2006, 59: 1369-1379.CrossRefPubMed Kariu T, Ishino T, Yano K, Chinzei Y, Yuda M: CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Mol Microbiol. 2006, 59: 1369-1379.CrossRefPubMed
17.
go back to reference Porter MD, Nicki J, Pool CD, DeBot M, Illam RM, Brando C, Bozick B, De La Vega P, Angra D, Spaccapelo R, Crisanti A, Murphy JR, Bennett JW, Schwenk RJ, Ockenhouse CF, Dutta S: Transgenic parasites stably expressing full-length Plasmodium falciparum circumsporozoite protein as a model for vaccine down-selection in mice using sterile protection as an endpoint. Clin Vaccine Immunol. 2013, 20: 803-810.PubMedCentralCrossRefPubMed Porter MD, Nicki J, Pool CD, DeBot M, Illam RM, Brando C, Bozick B, De La Vega P, Angra D, Spaccapelo R, Crisanti A, Murphy JR, Bennett JW, Schwenk RJ, Ockenhouse CF, Dutta S: Transgenic parasites stably expressing full-length Plasmodium falciparum circumsporozoite protein as a model for vaccine down-selection in mice using sterile protection as an endpoint. Clin Vaccine Immunol. 2013, 20: 803-810.PubMedCentralCrossRefPubMed
18.
go back to reference Bergmann-Leitner ES, Mease RM, De La Vega P, Savranskaya T, Polhemus M, Ockenhouse C, Angov E: Immunization with pre-erythrocytic antigen CelTOS from Plasmodium falciparum elicits cross-species protection against heterologous challenge with Plasmodium berghei. PLoS ONE. 2010, 5: e12294-PubMedCentralCrossRefPubMed Bergmann-Leitner ES, Mease RM, De La Vega P, Savranskaya T, Polhemus M, Ockenhouse C, Angov E: Immunization with pre-erythrocytic antigen CelTOS from Plasmodium falciparum elicits cross-species protection against heterologous challenge with Plasmodium berghei. PLoS ONE. 2010, 5: e12294-PubMedCentralCrossRefPubMed
19.
go back to reference Dutta S, Ware LA, Barbosa A, Ockenhouse CF, Lanar DE: Purification, characterization, and immunogenicity of a disulfide cross-linked Plasmodium vivax vaccine candidate antigen, merozoite surface protein 1, expressed in Escherichia coli. Infect Immun. 2001, 69: 5464-5470.PubMedCentralCrossRefPubMed Dutta S, Ware LA, Barbosa A, Ockenhouse CF, Lanar DE: Purification, characterization, and immunogenicity of a disulfide cross-linked Plasmodium vivax vaccine candidate antigen, merozoite surface protein 1, expressed in Escherichia coli. Infect Immun. 2001, 69: 5464-5470.PubMedCentralCrossRefPubMed
20.
go back to reference Dutta S, Sullivan JS, Grady KK, Haynes JD, Komisar J, Batchelor AH, Soisson L, Diggs CL, Heppner DG, Lanar DE, Collins WE, Barnwell JW: High antibody titer against apical membrane antigen-1 is required to protect against malaria in the Aotus model. PLoS ONE. 2009, 4: e8138-PubMedCentralCrossRefPubMed Dutta S, Sullivan JS, Grady KK, Haynes JD, Komisar J, Batchelor AH, Soisson L, Diggs CL, Heppner DG, Lanar DE, Collins WE, Barnwell JW: High antibody titer against apical membrane antigen-1 is required to protect against malaria in the Aotus model. PLoS ONE. 2009, 4: e8138-PubMedCentralCrossRefPubMed
21.
go back to reference Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, Cox J, Abeku T, Bousema T, Ghani AC, Drakeley C, Riley E: Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008, 7: 195-PubMedCentralCrossRefPubMed Corran PH, Cook J, Lynch C, Leendertse H, Manjurano A, Griffin J, Cox J, Abeku T, Bousema T, Ghani AC, Drakeley C, Riley E: Dried blood spots as a source of anti-malarial antibodies for epidemiological studies. Malar J. 2008, 7: 195-PubMedCentralCrossRefPubMed
22.
23.
go back to reference Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, Otieno S, Carneiro I, Cox J, Msuya E, Kleinschmidt I, Maxwell C, Greenwood B, Riley E, Sauerwein R, Chandramohan D, Gosling R: Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010, 201: 1764-1774.CrossRefPubMed Bousema T, Drakeley C, Gesase S, Hashim R, Magesa S, Mosha F, Otieno S, Carneiro I, Cox J, Msuya E, Kleinschmidt I, Maxwell C, Greenwood B, Riley E, Sauerwein R, Chandramohan D, Gosling R: Identification of hot spots of malaria transmission for targeted malaria control. J Infect Dis. 2010, 201: 1764-1774.CrossRefPubMed
24.
go back to reference Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, McCarthy J, Vallely A, Drakeley C: Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J. 2010, 9: 169-PubMedCentralCrossRefPubMed Cook J, Reid H, Iavro J, Kuwahata M, Taleo G, Clements A, McCarthy J, Vallely A, Drakeley C: Using serological measures to monitor changes in malaria transmission in Vanuatu. Malar J. 2010, 9: 169-PubMedCentralCrossRefPubMed
25.
go back to reference Wipasa J, Suphavilai C, Okell LC, Cook J, Corran PH, Thaikla K, Liewsaree W, Riley EM, Hafalla JC: Long-lived antibody and B cell memory responses to the human malaria parasites, plasmodium falciparum and plasmodium vivax. PLoS Pathog. 2010, 6: e1000770-PubMedCentralCrossRefPubMed Wipasa J, Suphavilai C, Okell LC, Cook J, Corran PH, Thaikla K, Liewsaree W, Riley EM, Hafalla JC: Long-lived antibody and B cell memory responses to the human malaria parasites, plasmodium falciparum and plasmodium vivax. PLoS Pathog. 2010, 6: e1000770-PubMedCentralCrossRefPubMed
26.
go back to reference Braga EM, Fontes CJ, Krettli AU: Persistence of humoral response against sporozoite and blood-stage malaria antigens 7 years after a brief exposure to Plasmodium vivax. J Infect Dis. 1998, 177: 1132-1135.CrossRefPubMed Braga EM, Fontes CJ, Krettli AU: Persistence of humoral response against sporozoite and blood-stage malaria antigens 7 years after a brief exposure to Plasmodium vivax. J Infect Dis. 1998, 177: 1132-1135.CrossRefPubMed
27.
go back to reference Dodoo D, Hollingdale MR, Anum D, Koram KA, Gyan B, Akanmori BD, Ocran J, Adu-Amankwah S, Geneshan H, Abot E, Legano J, Banania G, Sayo R, Brambilla D, Kumar S, Doolan DL, Rogers WO, Epstein J, Richie TL, Sedegah M: Measuring naturally acquired immune responses to candidate malaria vaccine antigens in Ghanaian adults. Malar J. 2011, 10: 168-PubMedCentralCrossRefPubMed Dodoo D, Hollingdale MR, Anum D, Koram KA, Gyan B, Akanmori BD, Ocran J, Adu-Amankwah S, Geneshan H, Abot E, Legano J, Banania G, Sayo R, Brambilla D, Kumar S, Doolan DL, Rogers WO, Epstein J, Richie TL, Sedegah M: Measuring naturally acquired immune responses to candidate malaria vaccine antigens in Ghanaian adults. Malar J. 2011, 10: 168-PubMedCentralCrossRefPubMed
29.
go back to reference Baird JK: Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today. 1995, 11: 105-111.CrossRefPubMed Baird JK: Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today. 1995, 11: 105-111.CrossRefPubMed
30.
go back to reference Shekalaghe S, Alifrangis M, Mwanziva C, Enevold A, Mwakalinga S, Mkali H, Kavishe R, Manjurano A, Sauerwein R, Drakeley C, Bousema T: Low density parasitaemia, red blood cell polymorphisms and Plasmodium falciparum specific immune responses in a low endemic area in northern Tanzania. BMC Infect Dis. 2009, 9: 69-PubMedCentralCrossRefPubMed Shekalaghe S, Alifrangis M, Mwanziva C, Enevold A, Mwakalinga S, Mkali H, Kavishe R, Manjurano A, Sauerwein R, Drakeley C, Bousema T: Low density parasitaemia, red blood cell polymorphisms and Plasmodium falciparum specific immune responses in a low endemic area in northern Tanzania. BMC Infect Dis. 2009, 9: 69-PubMedCentralCrossRefPubMed
31.
go back to reference Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, Theander TG, Nkya WM, Lemnge MM, Riley EM: Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 2005, 191: 1589-1598.CrossRefPubMed Drakeley CJ, Carneiro I, Reyburn H, Malima R, Lusingu JP, Cox J, Theander TG, Nkya WM, Lemnge MM, Riley EM: Altitude-dependent and -independent variations in Plasmodium falciparum prevalence in northeastern Tanzania. J Infect Dis. 2005, 191: 1589-1598.CrossRefPubMed
32.
go back to reference Campo JJ, Whitman TJ, Freilich D, Burgess TH, Martin GJ, Doolan DL: Toward a surrogate marker of malaria exposure: modeling longitudinal antibody measurements under outbreak conditions. PLoS ONE. 2011, 6: e21826-PubMedCentralCrossRefPubMed Campo JJ, Whitman TJ, Freilich D, Burgess TH, Martin GJ, Doolan DL: Toward a surrogate marker of malaria exposure: modeling longitudinal antibody measurements under outbreak conditions. PLoS ONE. 2011, 6: e21826-PubMedCentralCrossRefPubMed
33.
go back to reference Ramasamy R, Nagendran K, Ramasamy MS: Antibodies to epitopes on merozoite and sporozoite surface antigens as serologic markers of malaria transmission: studies at a site in the dry zone of Sri Lanka. Am J Trop Med Hyg. 1994, 50: 537-547.PubMed Ramasamy R, Nagendran K, Ramasamy MS: Antibodies to epitopes on merozoite and sporozoite surface antigens as serologic markers of malaria transmission: studies at a site in the dry zone of Sri Lanka. Am J Trop Med Hyg. 1994, 50: 537-547.PubMed
34.
go back to reference Webster HK, Gingrich JB, Wongsrichanalai C, Tulyayon S, Suvarnamani A, Sookto P, Permpanich B: Circumsporozoite antibody as a serologic marker of Plasmodium falciparum transmission. Am J Trop Med Hyg. 1992, 47: 489-497.PubMed Webster HK, Gingrich JB, Wongsrichanalai C, Tulyayon S, Suvarnamani A, Sookto P, Permpanich B: Circumsporozoite antibody as a serologic marker of Plasmodium falciparum transmission. Am J Trop Med Hyg. 1992, 47: 489-497.PubMed
35.
go back to reference Afari EA, Appawu M, Dunyo S, Baffoe-Wilmot A, Nkrumah FK: Malaria infection, morbidity and transmission in two ecological zones in Southern Ghana. Afr J Health Sci. 1995, 2: 312-315.PubMed Afari EA, Appawu M, Dunyo S, Baffoe-Wilmot A, Nkrumah FK: Malaria infection, morbidity and transmission in two ecological zones in Southern Ghana. Afr J Health Sci. 1995, 2: 312-315.PubMed
36.
go back to reference Agyepong IA, Ansah E, Gyapong M, Adjei S, Barnish G, Evans D: Strategies to improve adherence to recommended chloroquine treatment regimes: a quasi-experiment in the context of integrated primary health care delivery in Ghana. Soc Sci Med. 2002, 55: 2215-2226.CrossRefPubMed Agyepong IA, Ansah E, Gyapong M, Adjei S, Barnish G, Evans D: Strategies to improve adherence to recommended chloroquine treatment regimes: a quasi-experiment in the context of integrated primary health care delivery in Ghana. Soc Sci Med. 2002, 55: 2215-2226.CrossRefPubMed
37.
go back to reference Agyepong IA, Manderson L: Mosquito avoidance and bed net use in the greater Accra region, Ghana. J Biosoc Sci. 1999, 31: 79-92.CrossRefPubMed Agyepong IA, Manderson L: Mosquito avoidance and bed net use in the greater Accra region, Ghana. J Biosoc Sci. 1999, 31: 79-92.CrossRefPubMed
38.
go back to reference Ansah EK, Gyapong JO, Agyepong IA, Evans DB: Improving adherence to malaria treatment for children: the use of pre-packed chloroquine tablets vs. chloroquine syrup. Trop Med Int Health. 2001, 6: 496-504.CrossRefPubMed Ansah EK, Gyapong JO, Agyepong IA, Evans DB: Improving adherence to malaria treatment for children: the use of pre-packed chloroquine tablets vs. chloroquine syrup. Trop Med Int Health. 2001, 6: 496-504.CrossRefPubMed
39.
go back to reference Ansah EK, Narh-Bana S, Asiamah S, Dzordzordzi V, Biantey K, Dickson K, Gyapong JO, Koram KA, Greenwood BM, Mills A, Whitty CJ: Effect of removing direct payment for health care on utilisation and health outcomes in Ghanaian children: a randomised controlled trial. PLoS Med. 2009, 6: e1000007-PubMedCentralPubMed Ansah EK, Narh-Bana S, Asiamah S, Dzordzordzi V, Biantey K, Dickson K, Gyapong JO, Koram KA, Greenwood BM, Mills A, Whitty CJ: Effect of removing direct payment for health care on utilisation and health outcomes in Ghanaian children: a randomised controlled trial. PLoS Med. 2009, 6: e1000007-PubMedCentralPubMed
40.
go back to reference Chinbuah AM, Gyapong JO, Pagnoni F, Wellington EK, Gyapong M: Feasibility and acceptability of the use of artemether-lumefantrine in the home management of uncomplicated malaria in children 6–59 months old in Ghana. Trop Med Int Health. 2006, 11: 1003-1016.CrossRefPubMed Chinbuah AM, Gyapong JO, Pagnoni F, Wellington EK, Gyapong M: Feasibility and acceptability of the use of artemether-lumefantrine in the home management of uncomplicated malaria in children 6–59 months old in Ghana. Trop Med Int Health. 2006, 11: 1003-1016.CrossRefPubMed
41.
go back to reference Dodowa Health Research Centre: 2008–2009 Biennial report. 2009, 1-40. Dodowa Health Research Centre: 2008–2009 Biennial report. 2009, 1-40.
42.
go back to reference 2012 Ministry of Health, Ghana: Holistic assessment of the health sector programme of work Ghana Ministry of Health. 2013, 1-117. http://www.moh-ghana.org/UploadFiles/Publications/2012%20Holistic%20Assessment%20Report%20ofoe130715062103.pdf, accessed on 12th October 2013. 2012 Ministry of Health, Ghana: Holistic assessment of the health sector programme of work Ghana Ministry of Health. 2013, 1-117. http://​www.​moh-ghana.​org/​UploadFiles/​Publications/​2012%20Holistic%20Assessment%20Report%20ofoe130715062103.pdf, accessed on 12th October 2013.
43.
go back to reference Lindner SE, Swearingen KE, Harupa A, Vaughan AM, Sinnis P, Moritz RL, Kappe SH: Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol Cell Proteomics. 2013, 12: 1127-1143.PubMedCentralCrossRefPubMed Lindner SE, Swearingen KE, Harupa A, Vaughan AM, Sinnis P, Moritz RL, Kappe SH: Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol Cell Proteomics. 2013, 12: 1127-1143.PubMedCentralCrossRefPubMed
Metadata
Title
Anti-sporozoite antibodies as alternative markers for malaria transmission intensity estimation
Authors
Kwadwo A Kusi
Samuel Bosomprah
Daniel Dodoo
Eric Kyei-Baafour
Emmanuel K Dickson
Daniel Mensah
Evelina Angov
Sheetij Dutta
Martha Sedegah
Kwadwo A Koram
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2014
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-13-103

Other articles of this Issue 1/2014

Malaria Journal 1/2014 Go to the issue
Obesity Clinical Trial Summary

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.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

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

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

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

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