Skip to main content
Top
Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Research

The relationship between Plasmodium infection, anaemia and nutritional status in asymptomatic children aged under five years living in stable transmission zones in Kinshasa, Democratic Republic of Congo

Authors: Vivi Maketa, Hypolite Muhindo Mavoko, Raquel Inocêncio da Luz, Josué Zanga, Joachim Lubiba, Albert Kalonji, Pascal Lutumba, Jean-Pierre Van geertruyden

Published in: Malaria Journal | Issue 1/2015

Login to get access

Abstract

Background

Malaria is preventable and treatable when recommended interventions are properly implemented. Thus, diagnosis and treatment focus on symptomatic individuals while asymptomatic Plasmodium infection (PI) plays a role in the sustainability of the transmission and may also have an impact on the morbidity of the disease in terms of anaemia, nutritional status and even cognitive development of children. The objective of this study was to assess PI prevalence and its relationship with known morbidity factors in a vulnerable but asymptomatic stratum of the population.

Methods

A simple random sample, household survey in asymptomatic children under the age of five was conducted from April to September 2012 in two health areas of the health zone of Mont Ngafula 1, Kinshasa, Democratic Republic of Congo.

Results

The PI prevalence were 30.9% (95% CI: 26.5-35.9) and 14.3% (95% CI: 10.5-18.1) in Cité Pumbu and Kindele health areas, respectively, (OR: 2.7; p <0.001). All were Plasmodium falciparum infected and 4% were co-infected with Plasmodium malariae. In Cité Pumbu and Kindele, the prevalence of anaemia (haemoglobin <11 g/dL) was 61.6% (95% CI: 56.6-66.5) and 39.3% (95% CI: 34.0-44.6), respectively, (OR: 2.5; p <0.001). The health area of Cité Pumbu had 32% (95% CI: 27.5-37.0) of chronic malnutrition (HAZ score ≤ −2SD) compared to 5.1% (95% CI: 2.8-7.6) in Kindele. PI was predictor factor for anaemia (aOR: 3.5, p =0.01) and within infected children, there was an inverse relationship between parasite density and haemoglobin level (β = −5*10−5, p <0.001). Age older than 12 months (aOR: 3.8, p = 0.01), presence of anaemia (aOR: 3.4, p =0.001), chronic malnutrition (aOR: 1.8, p = 0.01), having a single parent/guardian (aOR: 1.6, p =0.04), and the non-use of insecticide-treated nets (aOR: 1.7, p = 0.04) were all predictors for PI in the overall population.

Conclusion

PI in asymptomatic children was correlated with anaemia and chronic malnutrition and was thus a harmful condition in the study population. Malaria control initiatives should not only focus on treatment of symptomatic infections but also take into consideration asymptomatic but infected children.
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO. World malaria report 2013. Geneva: World Health Organization; 2013. WHO. World malaria report 2013. Geneva: World Health Organization; 2013.
2.
go back to reference Douamba Z, Bisseye C, Djigma FW, Compaore TR, Bazie VJ, Pietra V, et al. Asymptomatic malaria correlates with anaemia in pregnant women at Ouagadougou, Burkina Faso. J Biomed Biotechnol. 2012;2012:198317.CrossRefPubMedCentralPubMed Douamba Z, Bisseye C, Djigma FW, Compaore TR, Bazie VJ, Pietra V, et al. Asymptomatic malaria correlates with anaemia in pregnant women at Ouagadougou, Burkina Faso. J Biomed Biotechnol. 2012;2012:198317.CrossRefPubMedCentralPubMed
4.
go back to reference Isah AY, Amanabo MA, Ekele BA. Prevalence of malaria parasitemia amongst asymptomatic pregnant women attending a Nigerian teaching hospital. Ann Afr Med. 2011;10:171–4.CrossRefPubMed Isah AY, Amanabo MA, Ekele BA. Prevalence of malaria parasitemia amongst asymptomatic pregnant women attending a Nigerian teaching hospital. Ann Afr Med. 2011;10:171–4.CrossRefPubMed
6.
go back to reference Noland GS, Ayodo G, Abuya J, Hodges JS, Rolfes MA, John CC. Decreased prevalence of anemia in highland areas of low malaria transmission after a 1-year interruption of transmission. Clin Infect Dis. 2012;54:178–84.CrossRefPubMedCentralPubMed Noland GS, Ayodo G, Abuya J, Hodges JS, Rolfes MA, John CC. Decreased prevalence of anemia in highland areas of low malaria transmission after a 1-year interruption of transmission. Clin Infect Dis. 2012;54:178–84.CrossRefPubMedCentralPubMed
7.
go back to reference Sharp PT, Harvey P. Malaria and growth stunting in young children of the highlands of Papua New Guinea. P N G Med J. 1980;23:132–40.PubMed Sharp PT, Harvey P. Malaria and growth stunting in young children of the highlands of Papua New Guinea. P N G Med J. 1980;23:132–40.PubMed
8.
go back to reference Crowell V, Briet OJ, Hardy D, Chitnis N, Maire N, Di PA, et al. Modelling the cost-effectiveness of mass screening and treatment for reducing Plasmodium falciparum malaria burden. Malar J. 2013;12:4.CrossRefPubMedCentralPubMed Crowell V, Briet OJ, Hardy D, Chitnis N, Maire N, Di PA, et al. Modelling the cost-effectiveness of mass screening and treatment for reducing Plasmodium falciparum malaria burden. Malar J. 2013;12:4.CrossRefPubMedCentralPubMed
11.
go back to reference D’Acremont V, Lengeler C, Mshinda H, Mtasiwa D, Tanner M, Genton B. Time to move from presumptive malaria treatment to laboratory-confirmed diagnosis and treatment in African children with fever. PLoS Med. 2009;6:e252.CrossRefPubMedCentralPubMed D’Acremont V, Lengeler C, Mshinda H, Mtasiwa D, Tanner M, Genton B. Time to move from presumptive malaria treatment to laboratory-confirmed diagnosis and treatment in African children with fever. PLoS Med. 2009;6:e252.CrossRefPubMedCentralPubMed
12.
go back to reference English M, Reyburn H, Goodman C, Snow RW. Abandoning presumptive antimalarial treatment for febrile children aged less than five years–a case of running before we can walk? PLoS Med. 2009;6:e1000015.CrossRefPubMed English M, Reyburn H, Goodman C, Snow RW. Abandoning presumptive antimalarial treatment for febrile children aged less than five years–a case of running before we can walk? PLoS Med. 2009;6:e1000015.CrossRefPubMed
13.
go back to reference Gerstl S, Dunkley S, Mukhtar A, De SM, Baker S, Maikere J. Assessment of two malaria rapid diagnostic tests in children under five years of age, with follow-up of false-positive pLDH test results, in a hyperendemic falciparum malaria area, Sierra Leone. Malar J. 2010;9:28.CrossRefPubMedCentralPubMed Gerstl S, Dunkley S, Mukhtar A, De SM, Baker S, Maikere J. Assessment of two malaria rapid diagnostic tests in children under five years of age, with follow-up of false-positive pLDH test results, in a hyperendemic falciparum malaria area, Sierra Leone. Malar J. 2010;9:28.CrossRefPubMedCentralPubMed
14.
go back to reference WHO. Guidelines for the treatment of malaria. Geneva: World Health Organization; 2010. WHO. Guidelines for the treatment of malaria. Geneva: World Health Organization; 2010.
15.
go back to reference Doumbia SO, Ndiaye D, Koita OA, Diakite M, Nwakanma D, Coulibaly M, et al. Improving malaria control in West Africa: interruption of transmission as a paradigm shift. Acta Trop. 2012;121:175–83.CrossRefPubMedCentralPubMed Doumbia SO, Ndiaye D, Koita OA, Diakite M, Nwakanma D, Coulibaly M, et al. Improving malaria control in West Africa: interruption of transmission as a paradigm shift. Acta Trop. 2012;121:175–83.CrossRefPubMedCentralPubMed
16.
go back to reference Dunyo S, Milligan P, Edwards T, Sutherland C, Targett G, Pinder M. Gametocytaemia after drug treatment of asymptomatic Plasmodium falciparum. PLoS Clin Trials. 2006;1:e20.CrossRefPubMedCentralPubMed Dunyo S, Milligan P, Edwards T, Sutherland C, Targett G, Pinder M. Gametocytaemia after drug treatment of asymptomatic Plasmodium falciparum. PLoS Clin Trials. 2006;1:e20.CrossRefPubMedCentralPubMed
17.
go back to reference Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:e1000324.CrossRefPubMedCentralPubMed Griffin JT, Hollingsworth TD, Okell LC, Churcher TS, White M, Hinsley W, et al. Reducing Plasmodium falciparum malaria transmission in Africa: a model-based evaluation of intervention strategies. PLoS Med. 2010;7:e1000324.CrossRefPubMedCentralPubMed
18.
go back to reference Kern SE, Tiono AB, Makanga M, Gbadoé AD, Premji Z, Gaye O, et al. Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar J. 2011;10:210.CrossRefPubMedCentralPubMed Kern SE, Tiono AB, Makanga M, Gbadoé AD, Premji Z, Gaye O, et al. Community screening and treatment of asymptomatic carriers of Plasmodium falciparum with artemether-lumefantrine to reduce malaria disease burden: a modelling and simulation analysis. Malar J. 2011;10:210.CrossRefPubMedCentralPubMed
19.
go back to reference Vafa M, Troye-Blomberg M, Anchang J, Garcia A, Migot-Nabias F. Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malar J. 2008;7:17.CrossRefPubMedCentralPubMed Vafa M, Troye-Blomberg M, Anchang J, Garcia A, Migot-Nabias F. Multiplicity of Plasmodium falciparum infection in asymptomatic children in Senegal: relation to transmission, age and erythrocyte variants. Malar J. 2008;7:17.CrossRefPubMedCentralPubMed
20.
go back to reference Caulfield LE, Richard SA, Black RE. Undernutrition as an underlying cause of malaria morbidity and mortality in children less than five years old. Am J Trop Med Hyg. 2004;71(2 Suppl):55–63.PubMed Caulfield LE, Richard SA, Black RE. Undernutrition as an underlying cause of malaria morbidity and mortality in children less than five years old. Am J Trop Med Hyg. 2004;71(2 Suppl):55–63.PubMed
21.
go back to reference Jeremiah ZA, Uko EK. Childhood asymptomatic malaria and nutritional status among Port Harcourt children. East Afr J Public Health. 2007;4:55–8.PubMed Jeremiah ZA, Uko EK. Childhood asymptomatic malaria and nutritional status among Port Harcourt children. East Afr J Public Health. 2007;4:55–8.PubMed
22.
go back to reference Ministère du Plan avec la collaboration du Ministère de la Santé: Enquête Démographique de Santé RDC 2007. Kinshasa: République Démocratique du Congo; 2008. Ministère du Plan avec la collaboration du Ministère de la Santé: Enquête Démographique de Santé RDC 2007. Kinshasa: République Démocratique du Congo; 2008.
23.
go back to reference Angus BJ, Chotivanich K, Udomsangpetch R, White NJ. In vivo removal of malaria parasites from red blood cells without their destruction in acute falciparum malaria. Blood. 1997;90:2037–40.PubMed Angus BJ, Chotivanich K, Udomsangpetch R, White NJ. In vivo removal of malaria parasites from red blood cells without their destruction in acute falciparum malaria. Blood. 1997;90:2037–40.PubMed
24.
go back to reference Clark IA, Chaudhri G. Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. Br J Haematol. 1988;70:99–103.CrossRefPubMed Clark IA, Chaudhri G. Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. Br J Haematol. 1988;70:99–103.CrossRefPubMed
25.
go back to reference Davis TM, Krishna S, Looareesuwan S, Supanaranond W, Pukrittayakamee S, Attatamsoonthorn K, et al. Erythrocyte sequestration and anemia in severe falciparum malaria. Analysis of acute changes in venous hematocrit using a simple mathematical model. J Clin Invest. 1990;86:793–800.CrossRefPubMedCentralPubMed Davis TM, Krishna S, Looareesuwan S, Supanaranond W, Pukrittayakamee S, Attatamsoonthorn K, et al. Erythrocyte sequestration and anemia in severe falciparum malaria. Analysis of acute changes in venous hematocrit using a simple mathematical model. J Clin Invest. 1990;86:793–800.CrossRefPubMedCentralPubMed
26.
go back to reference Dondorp AM, Angus BJ, Chotivanich K, Silamut K, Ruangveerayuth R, Hardeman MR, et al. Red blood cell deformability as a predictor of anemia in severe falciparum malaria. Am J Trop Med Hyg. 1999;60:733–7.PubMed Dondorp AM, Angus BJ, Chotivanich K, Silamut K, Ruangveerayuth R, Hardeman MR, et al. Red blood cell deformability as a predictor of anemia in severe falciparum malaria. Am J Trop Med Hyg. 1999;60:733–7.PubMed
27.
go back to reference el Hassan AM, Saeed AM, Fandrey J, Jelkmann W. Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur J Haematol. 1997;59:299–304.CrossRefPubMed el Hassan AM, Saeed AM, Fandrey J, Jelkmann W. Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur J Haematol. 1997;59:299–304.CrossRefPubMed
29.
go back to reference Menendez C, Kahigwa E, Hirt R, Vounatsou P, Aponte JJ, Font F, et al. Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet. 1997;350:844–50.CrossRefPubMed Menendez C, Kahigwa E, Hirt R, Vounatsou P, Aponte JJ, Font F, et al. Randomised placebo-controlled trial of iron supplementation and malaria chemoprophylaxis for prevention of severe anaemia and malaria in Tanzanian infants. Lancet. 1997;350:844–50.CrossRefPubMed
30.
go back to reference Phillips RE, Pasvol G. Anaemia of Plasmodium falciparum malaria. Baillieres Clin Haematol. 1992;5:315–30.CrossRefPubMed Phillips RE, Pasvol G. Anaemia of Plasmodium falciparum malaria. Baillieres Clin Haematol. 1992;5:315–30.CrossRefPubMed
31.
go back to reference Van den Ende J. Recurrence of blackwater fever: triggering of relapses by different antimalarials. Trop Med Int Health. 1998;3:632–9.CrossRefPubMed Van den Ende J. Recurrence of blackwater fever: triggering of relapses by different antimalarials. Trop Med Int Health. 1998;3:632–9.CrossRefPubMed
32.
go back to reference Crookston BT, Alder SC, Boakye I, Merrill RM, Amuasi JH, Porucznik CA, et al. Exploring the relationship between chronic undernutrition and asymptomatic malaria in Ghanaian children. Malar J. 2010;9:39.CrossRefPubMedCentralPubMed Crookston BT, Alder SC, Boakye I, Merrill RM, Amuasi JH, Porucznik CA, et al. Exploring the relationship between chronic undernutrition and asymptomatic malaria in Ghanaian children. Malar J. 2010;9:39.CrossRefPubMedCentralPubMed
33.
go back to reference Deen JL, Walraven GE, von Seidlein L. Increased risk for malaria in chronically malnourished children under 5 years of age in rural Gambia. J Trop Pediatr. 2002;48:78–83.CrossRefPubMed Deen JL, Walraven GE, von Seidlein L. Increased risk for malaria in chronically malnourished children under 5 years of age in rural Gambia. J Trop Pediatr. 2002;48:78–83.CrossRefPubMed
34.
go back to reference Ehrhardt S, Burchard GD, Mantel C, Cramer JP, Kaiser S, Kubo M, et al. Malaria, anemia, and malnutrition in african children–defining intervention priorities. J Infect Dis. 2006;194:108–14.CrossRefPubMed Ehrhardt S, Burchard GD, Mantel C, Cramer JP, Kaiser S, Kubo M, et al. Malaria, anemia, and malnutrition in african children–defining intervention priorities. J Infect Dis. 2006;194:108–14.CrossRefPubMed
35.
go back to reference Shankar AH. Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000;182 Suppl 1:S37–53.CrossRefPubMed Shankar AH. Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000;182 Suppl 1:S37–53.CrossRefPubMed
36.
go back to reference Takakura M, Uza M, Sasaki Y, Nagahama N, Phommpida S, Bounyadeth S, et al. The relationship between anthropometric indicators of nutritional status and malaria infection among youths in Khammouane Province, Lao PDR. Southeast Asian J Trop Med Public Health. 2001;32:262–7.PubMed Takakura M, Uza M, Sasaki Y, Nagahama N, Phommpida S, Bounyadeth S, et al. The relationship between anthropometric indicators of nutritional status and malaria infection among youths in Khammouane Province, Lao PDR. Southeast Asian J Trop Med Public Health. 2001;32:262–7.PubMed
37.
38.
go back to reference Hendrickse RG, Hasan AH, Olumide LO, Akinkunmi A. Malaria in early childhood. An investigation of five hundred seriously ill children in whom a “clinical” diagnosis of malaria was made on admission to the children’s emergency room at University College Hospital, Ibadan. Ann Trop Med Parasitol. 1971;65:1–20.PubMed Hendrickse RG, Hasan AH, Olumide LO, Akinkunmi A. Malaria in early childhood. An investigation of five hundred seriously ill children in whom a “clinical” diagnosis of malaria was made on admission to the children’s emergency room at University College Hospital, Ibadan. Ann Trop Med Parasitol. 1971;65:1–20.PubMed
39.
go back to reference Ministère de la Sante Publique de la santé. Secrétariat général de la santé Kinshasa.DRC: Rapport 2009 de l’Inspection Provinciale de Kinshasa. Kinshasa: République Démocratique du Congo; 2010. Ministère de la Sante Publique de la santé. Secrétariat général de la santé Kinshasa.DRC: Rapport 2009 de l’Inspection Provinciale de Kinshasa. Kinshasa: République Démocratique du Congo; 2010.
40.
go back to reference Muhindo MH, Nabasumba C, Tinto H, D’Alessandro U, Grobusch MP, Lutumba P, et al. Impact of retreatment with an artemisinin-based combination on malaria incidence and its potential selection of resistant strains: study protocol for a randomized controlled clinical trial. Trials. 2013;14:307.CrossRef Muhindo MH, Nabasumba C, Tinto H, D’Alessandro U, Grobusch MP, Lutumba P, et al. Impact of retreatment with an artemisinin-based combination on malaria incidence and its potential selection of resistant strains: study protocol for a randomized controlled clinical trial. Trials. 2013;14:307.CrossRef
41.
go back to reference Bennett S, Woods T, Liyanage WM, Smith DL. A simplified general method for cluster-sample surveys of health in developing countries. World Health Stat Q. 1991;44:98–106.PubMed Bennett S, Woods T, Liyanage WM, Smith DL. A simplified general method for cluster-sample surveys of health in developing countries. World Health Stat Q. 1991;44:98–106.PubMed
42.
go back to reference Ilombe G, Maketa V, Mavoko HM, da Luz RI, Lutumba P, Van Geertruyden JP. Performance of HRP2-based rapid test in children attending the health centre compared to asymptomatic children in the community. Malar J. 2014;13:308.CrossRefPubMedCentralPubMed Ilombe G, Maketa V, Mavoko HM, da Luz RI, Lutumba P, Van Geertruyden JP. Performance of HRP2-based rapid test in children attending the health centre compared to asymptomatic children in the community. Malar J. 2014;13:308.CrossRefPubMedCentralPubMed
43.
go back to reference WHO. Basic malaria microscopy: Part I Learner’ s guide, Part II tutor’s guide. Geneva: World Health Organization; 1991. WHO. Basic malaria microscopy: Part I Learner’ s guide, Part II tutor’s guide. Geneva: World Health Organization; 1991.
44.
go back to reference WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva: World Health Organization; 2011. WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva: World Health Organization; 2011.
45.
go back to reference Multicentre Growth Reference Study Group WHO. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Geneva: World Health Organization; 2006. Multicentre Growth Reference Study Group WHO. WHO Child Growth Standards: Length/height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: Methods and development. Geneva: World Health Organization; 2006.
46.
go back to reference WHO Multicentre Growth Reference Study Group. WHO Child Growth Standards: Head circumference-for-age, arm circumference-for-age, triceps skinfold-for-age and subscapular skinfold-for-age: Methods and development. Geneva: World Health Organization; 2007. WHO Multicentre Growth Reference Study Group. WHO Child Growth Standards: Head circumference-for-age, arm circumference-for-age, triceps skinfold-for-age and subscapular skinfold-for-age: Methods and development. Geneva: World Health Organization; 2007.
47.
go back to reference Baliraine FN, Afrane YA, Amenya DA, Bonizzoni M, Menge DM, Zhou G, et al. High prevalence of asymptomatic Plasmodium falciparum infections in a highland area of western Kenya: a cohort study. J Infect Dis. 2009;200:66–74.CrossRefPubMedCentralPubMed Baliraine FN, Afrane YA, Amenya DA, Bonizzoni M, Menge DM, Zhou G, et al. High prevalence of asymptomatic Plasmodium falciparum infections in a highland area of western Kenya: a cohort study. J Infect Dis. 2009;200:66–74.CrossRefPubMedCentralPubMed
48.
go back to reference Ogutu B, Tiono AB, Makanga M, Premji Z, Gbadoe AD, Ubben D, et al. Treatment of asymptomatic carriers with artemether-lumefantrine: an opportunity to reduce the burden of malaria? Malar J. 2010;9:30.CrossRefPubMedCentralPubMed Ogutu B, Tiono AB, Makanga M, Premji Z, Gbadoe AD, Ubben D, et al. Treatment of asymptomatic carriers with artemether-lumefantrine: an opportunity to reduce the burden of malaria? Malar J. 2010;9:30.CrossRefPubMedCentralPubMed
49.
go back to reference Beavogui AH, Djimde AA, Gregson A, Toure AM, Dao A, Coulibaly B, et al. Low infectivity of Plasmodium falciparum gametocytes to Anopheles gambiae following treatment with sulfadoxine-pyrimethamine in Mali. Int J Parasitol. 2010;40:1213–20.CrossRefPubMedCentralPubMed Beavogui AH, Djimde AA, Gregson A, Toure AM, Dao A, Coulibaly B, et al. Low infectivity of Plasmodium falciparum gametocytes to Anopheles gambiae following treatment with sulfadoxine-pyrimethamine in Mali. Int J Parasitol. 2010;40:1213–20.CrossRefPubMedCentralPubMed
50.
go back to reference Bousema T, Okell L, Shekalaghe S, Griffin JT, Omar S, Sawa P, et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malar J. 2010;9:136.CrossRefPubMedCentralPubMed Bousema T, Okell L, Shekalaghe S, Griffin JT, Omar S, Sawa P, et al. Revisiting the circulation time of Plasmodium falciparum gametocytes: molecular detection methods to estimate the duration of gametocyte carriage and the effect of gametocytocidal drugs. Malar J. 2010;9:136.CrossRefPubMedCentralPubMed
51.
go back to reference McGready R, White NJ, Nosten F. Parasitological efficacy of antimalarials in the treatment and prevention of falciparum malaria in pregnancy 1998 to 2009: a systematic review. BJOG. 2011;118:123–35.CrossRefPubMed McGready R, White NJ, Nosten F. Parasitological efficacy of antimalarials in the treatment and prevention of falciparum malaria in pregnancy 1998 to 2009: a systematic review. BJOG. 2011;118:123–35.CrossRefPubMed
52.
go back to reference Hodel EM, Kabanywanyi AM, Malila A, Zanolari B, Mercier T, Beck HP, et al. Residual antimalarials in malaria patients from Tanzania–implications on drug efficacy assessment and spread of parasite resistance. PLoS One. 2009;4:e8184.CrossRefPubMedCentralPubMed Hodel EM, Kabanywanyi AM, Malila A, Zanolari B, Mercier T, Beck HP, et al. Residual antimalarials in malaria patients from Tanzania–implications on drug efficacy assessment and spread of parasite resistance. PLoS One. 2009;4:e8184.CrossRefPubMedCentralPubMed
53.
go back to reference Amaratunga C, Lopera-Mesa TM, Brittain NJ, Cholera R, Arie T, Fujioka H, et al. A role for fetal hemoglobin and maternal immune IgG in infant resistance to Plasmodium falciparum malaria. PLoS One. 2011;6:e14798.CrossRefPubMedCentralPubMed Amaratunga C, Lopera-Mesa TM, Brittain NJ, Cholera R, Arie T, Fujioka H, et al. A role for fetal hemoglobin and maternal immune IgG in infant resistance to Plasmodium falciparum malaria. PLoS One. 2011;6:e14798.CrossRefPubMedCentralPubMed
55.
go back to reference Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J. 2012;11:435.CrossRefPubMedCentralPubMed Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J. 2012;11:435.CrossRefPubMedCentralPubMed
56.
go back to reference Abdullah S, Adazu K, Masanja H, Diallo D, Hodgson A, Ilboudo-Sanogo E, et al. Patterns of age-specific mortality in children in endemic areas of sub-Saharan Africa. Am J Trop Med Hyg. 2007;77(Suppl):99–105.PubMed Abdullah S, Adazu K, Masanja H, Diallo D, Hodgson A, Ilboudo-Sanogo E, et al. Patterns of age-specific mortality in children in endemic areas of sub-Saharan Africa. Am J Trop Med Hyg. 2007;77(Suppl):99–105.PubMed
57.
go back to reference Ghani AC, Sutherland CJ, Riley EM, Drakeley CJ, Griffin JT, Gosling RD, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS One. 2009;4:e4383.CrossRefPubMedCentralPubMed Ghani AC, Sutherland CJ, Riley EM, Drakeley CJ, Griffin JT, Gosling RD, et al. Loss of population levels of immunity to malaria as a result of exposure-reducing interventions: consequences for interpretation of disease trends. PLoS One. 2009;4:e4383.CrossRefPubMedCentralPubMed
58.
go back to reference Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:29.CrossRefPubMedCentralPubMed Laishram DD, Sutton PL, Nanda N, Sharma VL, Sobti RC, Carlton JM, et al. The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malar J. 2012;11:29.CrossRefPubMedCentralPubMed
59.
go back to reference Tiono AB, Guelbeogo MW, Sagnon NF, Nebie I, Sirima SB, Mukhopadhyay A, et al. Dynamics of malaria transmission and susceptibility to clinical malaria episodes following treatment of Plasmodium falciparum asymptomatic carriers: results of a cluster-randomized study of community-wide screening and treatment, and a parallel entomology study. BMC Infect Dis. 2013;13:535.CrossRefPubMedCentralPubMed Tiono AB, Guelbeogo MW, Sagnon NF, Nebie I, Sirima SB, Mukhopadhyay A, et al. Dynamics of malaria transmission and susceptibility to clinical malaria episodes following treatment of Plasmodium falciparum asymptomatic carriers: results of a cluster-randomized study of community-wide screening and treatment, and a parallel entomology study. BMC Infect Dis. 2013;13:535.CrossRefPubMedCentralPubMed
60.
go back to reference Askjaer N, Maxwell C, Chambo W, Staalsoe T, Nielsen M, Hviid L, et al. Insecticide-treated bed nets reduce plasma antibody levels and limit the repertoire of antibodies to Plasmodium falciparum variant surface antigens. Clin Diagn Lab Immunol. 2001;8:1289–91.PubMedCentralPubMed Askjaer N, Maxwell C, Chambo W, Staalsoe T, Nielsen M, Hviid L, et al. Insecticide-treated bed nets reduce plasma antibody levels and limit the repertoire of antibodies to Plasmodium falciparum variant surface antigens. Clin Diagn Lab Immunol. 2001;8:1289–91.PubMedCentralPubMed
61.
go back to reference Bull PC, Lowe BS, Kaleli N, Njuga F, Kortok M, Ross A, et al. Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte surface antigens among healthy Kenyan children. J Infect Dis. 2002;185:1688–91.CrossRefPubMed Bull PC, Lowe BS, Kaleli N, Njuga F, Kortok M, Ross A, et al. Plasmodium falciparum infections are associated with agglutinating antibodies to parasite-infected erythrocyte surface antigens among healthy Kenyan children. J Infect Dis. 2002;185:1688–91.CrossRefPubMed
62.
go back to reference Cavanagh DR, Elhassan IM, Roper C, Robinson VJ, Giha H, Holder AA, et al. A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein-1 in an area of unstable malaria in Sudan. J Immunol. 1998;161:347–59.PubMed Cavanagh DR, Elhassan IM, Roper C, Robinson VJ, Giha H, Holder AA, et al. A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein-1 in an area of unstable malaria in Sudan. J Immunol. 1998;161:347–59.PubMed
63.
go back to reference Kobbe R, Hogan B, Adjei S, Klein P, Kreuels B, Loag W, et al. Follow-up survey of children who received sulfadoxine-pyrimethamine for intermittent preventive antimalarial treatment in infants. J Infect Dis. 2011;203:556–60.CrossRefPubMedCentralPubMed Kobbe R, Hogan B, Adjei S, Klein P, Kreuels B, Loag W, et al. Follow-up survey of children who received sulfadoxine-pyrimethamine for intermittent preventive antimalarial treatment in infants. J Infect Dis. 2011;203:556–60.CrossRefPubMedCentralPubMed
64.
go back to reference Rogerson SJ, Wijesinghe RS, Meshnick SR. Host immunity as a determinant of treatment outcome in Plasmodium falciparum malaria. Lancet Infect Dis. 2010;10:51–9.CrossRefPubMed Rogerson SJ, Wijesinghe RS, Meshnick SR. Host immunity as a determinant of treatment outcome in Plasmodium falciparum malaria. Lancet Infect Dis. 2010;10:51–9.CrossRefPubMed
65.
go back to reference D’Alessandro U, Olaleye BO, McGuire W, Langerock P, Bennett S, Aikins MK, et al. Mortality and morbidity from malaria in Gambian children after introduction of an impregnated bednet programme. Lancet. 1995;345:479–83.CrossRefPubMed D’Alessandro U, Olaleye BO, McGuire W, Langerock P, Bennett S, Aikins MK, et al. Mortality and morbidity from malaria in Gambian children after introduction of an impregnated bednet programme. Lancet. 1995;345:479–83.CrossRefPubMed
66.
go back to reference Koram KA, Molyneux ME. When is “malaria” malaria? The different burdens of malaria infection, malaria disease, and malaria-like illnesses. Am J Trop Med Hyg. 2007;77 Suppl 6:1–5.PubMed Koram KA, Molyneux ME. When is “malaria” malaria? The different burdens of malaria infection, malaria disease, and malaria-like illnesses. Am J Trop Med Hyg. 2007;77 Suppl 6:1–5.PubMed
67.
go back to reference Greenwood B. The use of anti-malarial drugs to prevent malaria in the population of malaria-endemic areas. Am J Trop Med Hyg. 2004;70:1–7.PubMed Greenwood B. The use of anti-malarial drugs to prevent malaria in the population of malaria-endemic areas. Am J Trop Med Hyg. 2004;70:1–7.PubMed
68.
go back to reference Sutherland CJ, Drakeley CJ, Schellenberg D. How is childhood development of immunity to Plasmodium falciparum enhanced by certain antimalarial interventions? Malar J. 2007;6:161.CrossRefPubMedCentralPubMed Sutherland CJ, Drakeley CJ, Schellenberg D. How is childhood development of immunity to Plasmodium falciparum enhanced by certain antimalarial interventions? Malar J. 2007;6:161.CrossRefPubMedCentralPubMed
69.
go back to reference Njama-Meya D, Kamya MR, Dorsey G. Asymptomatic parasitaemia as a risk factor for symptomatic malaria in a cohort of Ugandan children. Trop Med Int Health. 2004;9:862–8.CrossRefPubMed Njama-Meya D, Kamya MR, Dorsey G. Asymptomatic parasitaemia as a risk factor for symptomatic malaria in a cohort of Ugandan children. Trop Med Int Health. 2004;9:862–8.CrossRefPubMed
70.
go back to reference Hotez PJ, Molyneux DH. Tropical anemia: one of Africa’s great killers and a rationale for linking malaria and neglected tropical disease control to achieve a common goal. PLoS Negl Trop Dis. 2008;2:e270.CrossRefPubMedCentralPubMed Hotez PJ, Molyneux DH. Tropical anemia: one of Africa’s great killers and a rationale for linking malaria and neglected tropical disease control to achieve a common goal. PLoS Negl Trop Dis. 2008;2:e270.CrossRefPubMedCentralPubMed
71.
go back to reference Stauffer W, Fischer PR. Diagnosis and treatment of malaria in children. Clin Infect Dis. 2003;37:1340–8.CrossRefPubMed Stauffer W, Fischer PR. Diagnosis and treatment of malaria in children. Clin Infect Dis. 2003;37:1340–8.CrossRefPubMed
72.
go back to reference Jaenisch T, Sullivan DJ, Dutta A, Deb S, Ramsan M, Othman MK, et al. Malaria incidence and prevalence on Pemba island before the onset of the successful control intervention on the Zanzibar archipelago. Malar J. 2010;9:32.CrossRefPubMedCentralPubMed Jaenisch T, Sullivan DJ, Dutta A, Deb S, Ramsan M, Othman MK, et al. Malaria incidence and prevalence on Pemba island before the onset of the successful control intervention on the Zanzibar archipelago. Malar J. 2010;9:32.CrossRefPubMedCentralPubMed
73.
go back to reference Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, Mohamed AD, et al. Scaling up malaria control in Zambia: progress and impact 2005–2008. Am J Trop Med Hyg. 2010;83:480–8.CrossRefPubMedCentralPubMed Chizema-Kawesha E, Miller JM, Steketee RW, Mukonka VM, Mukuka C, Mohamed AD, et al. Scaling up malaria control in Zambia: progress and impact 2005–2008. Am J Trop Med Hyg. 2010;83:480–8.CrossRefPubMedCentralPubMed
74.
go back to reference Matangila JR, Lufuluabo J, Ibalanky AL, Inocencio da Luz RA, Lutumba P, Van Geertruyden JP. Asymptomatic Plasmodium falciparum infection is associated with anaemia in pregnancy and can be more cost-effectively detected by rapid diagnostic test than by microscopy in Kinshasa, Democratic Republic of the Congo. Malar J. 2014;13:132.CrossRefPubMedCentralPubMed Matangila JR, Lufuluabo J, Ibalanky AL, Inocencio da Luz RA, Lutumba P, Van Geertruyden JP. Asymptomatic Plasmodium falciparum infection is associated with anaemia in pregnancy and can be more cost-effectively detected by rapid diagnostic test than by microscopy in Kinshasa, Democratic Republic of the Congo. Malar J. 2014;13:132.CrossRefPubMedCentralPubMed
75.
go back to reference Bottius E, Guanzirolli A, Trape JF, Rogier C, Konate L, Druilhe P. Malaria: even more chronic in nature than previously thought; evidence for subpatent parasitaemia detectable by the polymerase chain reaction. Trans R Soc Trop Med Hyg. 1996;90:15–9.CrossRefPubMed Bottius E, Guanzirolli A, Trape JF, Rogier C, Konate L, Druilhe P. Malaria: even more chronic in nature than previously thought; evidence for subpatent parasitaemia detectable by the polymerase chain reaction. Trans R Soc Trop Med Hyg. 1996;90:15–9.CrossRefPubMed
Metadata
Title
The relationship between Plasmodium infection, anaemia and nutritional status in asymptomatic children aged under five years living in stable transmission zones in Kinshasa, Democratic Republic of Congo
Authors
Vivi Maketa
Hypolite Muhindo Mavoko
Raquel Inocêncio da Luz
Josué Zanga
Joachim Lubiba
Albert Kalonji
Pascal Lutumba
Jean-Pierre Van geertruyden
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0595-5

Other articles of this Issue 1/2015

Malaria Journal 1/2015 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 discuss last year's major advances in heart failure and cardiomyopathies.