Factors associated with malaria parasitemia, anemia and serological responses in a spectrum of epidemiological settings in Uganda

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Yeka, Adoke ^a,c   Nankabirwa, Joaniter ^b,c   Mpimbaza, Arthur ^b,c   Kigozi, Ruth ^c   Arinaitwe, Emmanuel ^c   Drakeley, Chris ^d   Greenhouse, Bryan ^e   Kamya, Moses R ^b,c   Dorsey, Grant ^e   Staedke, Sarah G ^c,d  

^a MAKERERE UNIVERSITY SCHOOL OF PUBLIC HEALTH   (Uganda)

^b MAKERERE UNIVERSITY COLLEGE OF HEALTH SCIENCES   (Uganda)

^c INFECTIOUS DISEASES RESEARCH COLLABORATION   (Uganda)

^d LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APICAL MEMBRANE ANTIGEN 1; HEMOGLOBIN; MEROZOITE SURFACE PROTEIN 1; APICAL MEMBRANE ANTIGEN I, PLASMODIUM; MEMBRANE PROTEIN; PARASITE ANTIGEN; PROTOZOAL PROTEIN;

ADULT; ANEMIA; ANTIBODY RESPONSE; ARTICLE; CHILD; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; FEMALE; GEOGRAPHIC DISTRIBUTION; HUMAN; INFECTION RATE; MAJOR CLINICAL STUDY; MALARIA; MALE; PARASITE PREVALENCE; PARASITEMIA; PLASMODIUM FALCIPARUM; RISK ASSESSMENT; RISK FACTOR; RURAL AREA; SEROCONVERSION; SEROLOGY; UGANDA; ADOLESCENT; COMPLICATION; IMMUNOLOGY; MALARIA, FALCIPARUM; MIDDLE AGED; PHYSIOLOGY; PREVALENCE; QUESTIONNAIRE; YOUNG ADULT;

PLASMODIUM FALCIPARUM;

ADOLESCENT; ADULT; ANEMIA; ANTIGENS, PROTOZOAN; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; MALARIA, FALCIPARUM; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PARASITEMIA; PLASMODIUM FALCIPARUM; PREVALENCE; PROTOZOAN PROTEINS; SEROLOGIC TESTS; SURVEYS AND QUESTIONNAIRES; UGANDA; YOUNG ADULT;

EID: 84929497623     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118901     Document Type: Article

References (45)

1. World malaria report 2010, World Health Organization, (2010) Available: http://www.who.int/malaria/world-malaria-report-2010/.
2. Aregawi MW, Ali AS, Al-Mafazy AW, Molteni F, Katikiti S, Warsame M, et al. (2011) Reductions in malaria and anaemia case and death burden at hospitals following scale-up of malaria control in Zanzibar, 1999-2008. Malar J 10: 46. 1475-2875-10-46 [pii]; doi: 10.1186/1475-2875-10-46 PMID: 21332989
3. Barnes KI, Durrheim DN, Little F, Jackson A, Mehta U, Allen E, et al. (2005) Effect of artemether-lumefantrine policy and improved vector control on malaria burden in KwaZulu-Natal, South Africa. PLoS Med 2: e330. 05-PLME-RA-0166R2 [pii] doi: 10.1371/journal.pmed.0020330 PMID: 16187798
4. Ceesay SJ, Casals-Pascual C, Erskine J, Anya SE, Duah NO, Fulford AJ, et al. (2008) Changes in malaria indices between 1999 and 2007 in The Gambia: a retrospective analysis. Lancet 372: 1545-1554. doi: 10.1016/S0140-6736(08)61654-2 PMID: 18984187
5. Karema C, Aregawi MW, Rukundo A, Kabayiza A, Mulindahabi M, Fall IS, et al. (2012) Trends in malaria cases, hospital admissions and deaths following scale-up of anti-malarial interventions, 2000-2010, Rwanda. Malar J 11: 236. 1475-2875-11-236 [pii] doi: 10.1186/1475-2875-11-236 PMID: 22823945
6. O'Meara WP, Bejon P, Mwangi TW, Okiro EA, Peshu N, Snow RW, et al. (2008) Effect of a fall in malaria transmission on morbidity and mortality in Kilifi, Kenya. Lancet 372: 1555-1562. S0140-6736(08) 61655-4 [pii] doi: 10.1016/S0140-6736(08)61655-4 PMID: 18984188
7. Otten M, Aregawi M, Were W, Karema C, Medin A, Bekele W, et al. (2009) Initial evidence of reduction of malaria cases and deaths in Rwanda and Ethiopia due to rapid scale-up of malaria prevention and treatment. Malar J 8: 14. 1475-2875-8-14 [pii] doi: 10.1186/1475-2875-8-14 PMID: 19144183
8. O'Meara WP, Mangeni JN, Steketee R, Greenwood B (2010) Changes in the burden of malaria in sub-Saharan Africa. Lancet Infect Dis 10: 545-555. S1473-3099(10)70096-7 [pii] doi: 10.1016/S1473-3099 (10)70096-7 PMID: 20637696
9. Okiro EA, Bitira D, Mbabazi G, Mpimbaza A, Alegana VA, Talisuna AO, et al. (2011) Increasing malaria hospital admissions in Uganda between 1999 and 2009. BMC Med 9: 37. 1741-7015-9-37 [pii] doi: 10. 1186/1741-7015-9-37 PMID: 21486498
10. Talisuna A, Adibaku S, Dorsey G, Kamya MR, Rosenthal PJ (2011) Malaria in Uganda: Challenges to control on the long road to elimination. II. The path forward. Acta Trop. S0001-706X(11)00196-3 [pii] doi: 10.1016/j.actatropica.2011.06.013
11. Yeka A, Gasasira A, Mpimbaza A, Achan J, Nankabirwa J, Nsobya S, et al. (2011) Malaria in Uganda: Challenges to control on the long road to elimination I. Epidemiology and current control efforts. Acta Trop. S0001-706X(11)00061-1 [pii] doi: 10.1016/j.actatropica.2011.03.004
12. World malaria report 2013, World Health Organization (2013) Available: http://www.who.int/entity/malaria/publications/world-malaria-report-2013/report/en/index.html.
13. Uganda Demographic and Health Survey 2011, available at (www.ubos.org/onlinefiles/uploads/ubos/UDHS/UDHS2011.pdf).
14. Uganda Demographic and Health Survey 2006, available at (dhsprogram.com/pubs/pdf/FR194/FR194.pdf).
15. Kigozi R, Baxi SM, Gasasira A, Sserwanga A, Kakeeto S, Nasr S, et al. (2012) Indoor residual spraying of insecticide and malaria morbidity in a high transmission intensity area of Uganda. PLoS One 7: e42857. PONE-D-12-10962 [pii]. doi: 10.1371/journal.pone.0042857 PMID: 22880123
16. Bukirwa H, Yau V, Kigozi R, Filler S, Quick L, Lugemwa M, et al. (2009) Assessing the impact of indoor residual spraying on malaria morbidity using a sentinel site surveillance system in Western Uganda. Am J Trop Med Hyg 81: 611-614. 81/4/611 [pii] doi: 10.4269/ajtmh.2009.09-0126 PMID: 19815875
17. Jagannathan P, Muhindo MK, Kakuru A, Arinaitwe E, Greenhouse B, Tappero J, et al. (2012) Increasing incidence of malaria in children despite insecticide-treated bed nets and prompt anti-malarial therapy in Tororo, Uganda. Malar J 11: 435. 1475-2875-11-435 [pii] doi: 10.1186/1475-2875-11-435 PMID: 23273022
18. Burkot TR, Graves PM (1995) The value of vector-based estimates of malaria transmission. Ann Trop Med Parasitol 89: 125-134. PMID: 7605122
19. Akhwale WS, Lum JK, Kaneko A, Eto H, Obonyo C, Bjorkman A, et al. (2004) Anemia and malaria at different altitudes in the western highlands of Kenya. Acta Trop 91: 167-175. S0001706X04000737 [pii]. doi: 10.1016/j.actatropica.2004.02.010 PMID: 15234666
20. Korenromp EL, Armstrong-Schellenberg JR, Williams BG, Nahlen BL, Snow RW (2004) Impact of malaria control on childhood anaemia in Africa-a quantitative review. Trop Med Int Health 9: 1050-1065. TMI1317 [pii] doi: 10.1111/j.1365-3156.2004.01317.x PMID: 15482397
21. Mathanga DP, Campbell CH Jr., Vanden Eng J, Wolkon A, Bronzan RN, Malenga GJ, et al. (2010) Comparison of anaemia and parasitaemia as indicators of malaria control in household and EPI-health facility surveys in Malawi. Malar J 9: 107. 1475-2875-9-107 [pii] doi: 10.1186/1475-2875-9-107 PMID: 20409342
22. Guerra CA, Hay SI, Lucioparedes LS, Gikandi PW, Tatem AJ, Noor AM, et al. (2007) Assembling a global database of malaria parasite prevalence for the Malaria Atlas Project. Malar J 6: 17. 1475-2875-6-17 [pii] doi: 10.1186/1475-2875-6-17 PMID: 17306022
23. Hay SI, Snow RW (2006) The malaria Atlas Project: developing global maps of malaria risk. PLoS Med 3: e473. 06-PLME-HIA-0393R2 [pii] doi: 10.1371/journal.pmed.0030473 PMID: 17147467
24. Drakeley CJ, Corran PH, Coleman PG, Tongren JE, McDonald SL, Carneiro I, et al. (2005) Estimating medium-and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A 102: 5108-5113. 0408725102 [pii] doi: 10.1073/pnas.0408725102 PMID: 15792998
25. Bretscher MT, Supargiyono S, Wijayanti MA, Nugraheni D, Widyastuti AN, Lobo NF, et al. (2013) Measurement of Plasmodium falciparum transmission intensity using serological cohort data from Indonesian schoolchildren. Malar J 12: 21. 1475-2875-12-21 [pii] doi: 10.1186/1475-2875-12-21 PMID: 23327665
26. Estevez PT, Satoguina J, Nwakanma DC, West S, Conway DJ, Drakeley CJ (2011) Human saliva as a source of anti-malarial antibodies to examine population exposure to Plasmodium falciparum. Malar J 10: 104. 1475-2875-10-104 [pii] doi: 10.1186/1475-2875-10-104 PMID: 21527045
27. Stewart L, Gosling R, Griffin J, Gesase S, Campo J, Hashim R, et al. (2009) Rapid assessment of malaria transmission using age-specific sero-conversion rates. PLoS One 4: e6083. doi: 10.1371/journal. pone.0006083 PMID: 19562032
28. Kilama M, Smith DL, Hutchinson R, Kigozi R, Yeka A, Lavoy G, et al. (2014) Estimating the annual entomological inoculation rate for Plasmodium falciparum transmitted by Anopheles gambiae s.l. using three sampling methods in three sites in Uganda. Malar J 13: 111. 1475-2875-13-111 [pii] doi: 10. 1186/1475-2875-13-111 PMID: 24656206
29. Roll Back Malaria (2010) Saving Lives with Malaria Control: Counting Down to the Millenium Development Goals. Available: http://www.rbm.who.int/ProgressImpactSeries/docs/report3-en.pdf.
30. Corran P, Coleman P, Riley E, Drakeley C (2007) Serology: a robust indicator of malaria transmission intensity? Trends Parasitol 23: 575-582. S1471-4922(07)00277-2 [pii] doi: 10.1016/j.pt.2007.08.023 PMID: 17988945
31. Filmer D, Pritchett LH (2001) Estimating wealth effects without expenditure data-or tears: an application to educational enrollments in states of India. Demography 38: 115-132. PMID: 11227840
32. Uganda Malaria Control Strategic Plan 2005/6-2009/10. Available: health.go.ug/mcp/index2.html.
33. Desai MR, Terlouw DJ, Kwena AM, Phillips-Howard PA, Kariuki SK, Wannemuehler KA, et al. (2005) Factors associated with hemoglobin concentrations in pre-school children in Western Kenya: crosssectional studies. Am J Trop Med Hyg 72: 47-59. 72/1/47 [pii]. PMID: 15728867
34. Owusu-Agyei S, Fryauff DJ, Chandramohan D, Koram KA, Binka FN, Nkrumah FK, et al. (2002) Characteristics of severe anemia and its association with malaria in young children of the Kassena-Nankana District of northern Ghana. Am J Trop Med Hyg 67: 371-377. PMID: 12452491
35. Reithinger R, Ngondi JM, Graves PM, Hwang J, Getachew A, Jima D (2013) Risk factors for anemia in children under 6 years of age in Ethiopia: analysis of the data from the cross-sectional Malaria Indicator-Survey, 2007. Trans R Soc Trop Med Hyg 107: 769-776. trt096 [pii] doi: 10.1093/trstmh/trt096 PMID: 24218415
36. Premji Z, Hamisi Y, Shiff C, Minjas J, Lubega P, Makwaya C (1995) Anaemia and Plasmodium falciparum infections among young children in an holoendemic area, Bagamoyo, Tanzania. Acta Trop 59: 55-64. 0001706X9400079G [pii]. PMID: 7785526
37. Green HK, Sousa-Figueiredo JC, Basanez MG, Betson M, Kabatereine NB, Fenwick A, et al. (2011) Anaemia in Ugandan preschool-aged children: the relative contribution of intestinal parasites and malaria. Parasitology 138: 1534-1545. S0031182011001016 [pii] doi: 10.1017/S0031182011001016 PMID: 21819635
38. Osterbauer B, Kapisi J, Bigira V, Mwangwa F, Kinara S, Kamya MR, et al. (2012) Factors associated with malaria parasitaemia, malnutrition, and anaemia among HIV-exposed and unexposed Ugandan infants: a cross-sectional survey. Malar J 11: 432. 1475-2875-11-432 [pii] doi: 10.1186/1475-2875-11-432 PMID: 23270614
39. Lusingu JP, Vestergaard LS, Mmbando BP, Drakeley CJ, Jones C, Akida J, et al. (2004) Malaria morbidity and immunity among residents of villages with different Plasmodium falciparum transmission intensity in North-Eastern Tanzania. Malar J 3: 26. 1475-2875-3-26 [pii]. doi: 10.1186/1475-2875-3-26 PMID: 15282030
40. Maxwell CA, Chambo W, Mwaimu M, Magogo F, Carneiro IA, Curtis CF (2003) Variation of malaria transmission and morbidity with altitude in Tanzania and with introduction of alphacypermethrin treated nets. Malar J 2: 28. 1475-2875-2-28 [pii]. doi: 10.1186/1475-2875-2-28 PMID: 14585106
41. Ye Y, Madise N, Ndugwa R, Ochola S, Snow RW (2009) Fever treatment in the absence of malaria transmission in an urban informal settlement in Nairobi, Kenya. Malar J 8: 160. 1475-2875-8-160 [pii] doi: 10.1186/1475-2875-8-160 PMID: 19604369
42. Bejon P, Williams TN, Liljander A, Noor AM, Wambua J, Ogada E, et al. (2010) Stable and unstable malaria hotspots in longitudinal cohort studies in Kenya. PLoS Med 7: e1000304. doi: 10.1371/journal. pmed.1000304 PMID: 20625549
43. Riley E, Wagner G, Roper C (1996) Estimating the force of malaria infection. Parasitol Today 12: 410-411. 0169475896806338 [pii]. PMID: 15275295
44. Supargiyono S, Bretscher MT, Wijayanti MA, Sutanto I, Nugraheni D, Rozqie R, et al. (2013) Seasonal changes in the antibody responses against Plasmodium falciparum merozoite surface antigens in areas of differing malaria endemicity in Indonesia. Malar J 12: 444. 1475-2875-12-444 [pii] doi: 10. 1186/1475-2875-12-444 PMID: 24321092
45. Proietti C, Pettinato DD, Kanoi BN, Ntege E, Crisanti A, Riley EM, et al. (2011) Continuing intense malaria transmission in northern Uganda. Am J Trop Med Hyg 84: 830-837. 84/5/830 [pii] doi: 10.4269/ajtmh.2011.10-0498 PMID: 21540398