The potential of pregnant women as a sentinel population for malaria surveillance

Nina C Brunner, Frank Chacky, Renata Mandike, Ally Mohamed, Manuela Runge, Sumaiyya G Thawer, Amanda Ross, Penelope Vounatsou, Christian Lengeler, Fabrizio Molteni, Manuel W Hetzel, Nina C Brunner, Frank Chacky, Renata Mandike, Ally Mohamed, Manuela Runge, Sumaiyya G Thawer, Amanda Ross, Penelope Vounatsou, Christian Lengeler, Fabrizio Molteni, Manuel W Hetzel

Abstract

Background: With increasing spatial heterogeneity of malaria transmission and a shift of the disease burden towards older children and adults, pregnant women attending antenatal care (ANC) have been proposed as a pragmatic sentinel population for malaria surveillance. However, the representativeness of routine ANC malaria test-positivity and its relationship with prevalence in other population subgroups are yet to be investigated.

Methods: Monthly ANC malaria test-positivity data from all Tanzanian health facilities for January 2014 to May 2016 was compared to prevalence data from the School Malaria Parasitaemia Survey 2015, the Malaria Indicator Survey (MIS) 2015/16, the Malaria Atlas Project 2015, and a Bayesian model fitted to MIS data. Linear regression was used to describe the difference between malaria test-positivity in pregnant women and respective comparison groups as a function of ANC test-positivity and potential covariates.

Results: The relationship between ANC test-positivity and survey prevalence in children follows spatially and biologically meaningful patterns. However, the uncertainty of the relationship was substantial, particularly in areas with high or perennial transmission. In comparison, modelled data estimated higher prevalence in children at low transmission intensities and lower prevalence at higher transmission intensities.

Conclusions: Pregnant women attending ANC are a pragmatic sentinel population to assess heterogeneity and trends in malaria prevalence in Tanzania. Yet, since ANC malaria test-positivity cannot be used to directly predict the prevalence in other population subgroups, complementary community-level measurements remain highly relevant.

Keywords: Malaria; Malaria elimination; Pregnant women; Surveillance.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
District test-positivity difference SMPS − ANC against ANC malaria test-positivity with regression line and 95% limits of agreement, normalized for ITN use in school children. a Districts with seasonal malaria transmission, by district type. b Districts with perennial malaria transmission, by district type
Fig. 2
Fig. 2
Regional test-positivity difference MIS − ANC against ANC malaria test-positivity with regression line and 95% limits of agreement
Fig. 3
Fig. 3
District test-positivity difference MAP − ANC against ANC malaria test-positivity with regression line and 95% limits of agreement
Fig. 4
Fig. 4
District test-positivity difference BGM − ANC against ANC malaria test-positivity with regression line and 95% limits of agreement. a Districts with seasonal malaria transmission, by district type. b Districts with perennial malaria transmission, by district type

References

    1. WHO . Global Technical Strategy for Malaria 2016–2030. Geneva: World Health Organization; 2015.
    1. Nankabirwa J, Brooker SJ, Clarke SE, Fernando D, Gitonga CW, Schellenberg D, et al. Malaria in school-age children in Africa: an increasingly important challenge. Trop Med Int Health. 2014;19:1294–1309. doi: 10.1111/tmi.12374.
    1. Sserwanga A, Harris JC, Kigozi R, Menon M, Bukirwa H, Gasasira A, et al. Improved malaria case management through the implementation of a health facility-based sentinel site surveillance system in Uganda. PLoS ONE. 2011;6:e16316. doi: 10.1371/journal.pone.0016316.
    1. Yukich JO, Butts J, Miles M, Berhane Y, Nahusenay H, Malone JL, et al. A description of malaria sentinel surveillance: a case study in Oromia Regional State, Ethiopia. Malar J. 2014;13:88. doi: 10.1186/1475-2875-13-88.
    1. Cibulskis RE, Bell D, Christophel E-M, Hii J, Delacollette C, Bakyaita N, et al. Estimating trends in the burden of malaria at country level. Am J Trop Med Hyg. 2007;77:133–137. doi: 10.4269/ajtmh.2007.77.133.
    1. Mayor A, Menendez C, Walker PGT. Targeting pregnant women for malaria surveillance. Trends Parasitol. 2019;35:677–686. doi: 10.1016/j.pt.2019.07.005.
    1. van Eijk AM, Hill J, Noor AM, Snow RW, ter Kuile FO. Prevalence of malaria infection in pregnant women compared with children for tracking malaria transmission in sub-Saharan Africa: a systematic review and meta-analysis. Lancet Glob Health. 2015;3:e617–e628. doi: 10.1016/S2214-109X(15)00049-2.
    1. Hellewell J, Walker P, Ghani A, Rao B, Churcher TS. Using ante-natal clinic prevalence data to monitor temporal changes in malaria incidence in a humanitarian setting in the Democratic Republic of Congo. Malar J. 2018;17:312. doi: 10.1186/s12936-018-2460-9.
    1. Chacky F, Runge M, Rumisha SF, Machafuko P, Chaki P, Massaga JJ, et al. Nationwide school malaria parasitaemia survey in public primary schools, the United Republic of Tanzania. Malar J. 2018;17:452. doi: 10.1186/s12936-018-2601-1.
    1. MoHCDGEC, MoH, NBS, OCGS, ICF. Demographic and health survey and malaria indicator survey (TDHS-MIS) 2015–16. Dar es Salaam, Tanzania, 2016.
    1. Worldpop. United Republic of Tanzania 100 m Population. . Accessed 28 Nov 2016.
    1. MAP. The Malaria Atlas Project. . Accessed 28 Nov 2016.
    1. Ssempiira J, Nambuusi B, Kissa J, Agaba B, Makumbi F, Kasasa S, et al. Geostatistical modelling of malaria indicator survey data to assess the effects of interventions on the geographical distribution of malaria prevalence in children less than 5 years in Uganda. PLoS ONE. 2017;12:e0174948. doi: 10.1371/journal.pone.0174948.
    1. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat Methods Med Res. 1999;8:135–160. doi: 10.1177/096228029900800204.
    1. Pindolia DK, Garcia AJ, Huang Z, Smith DL, Alegana VA, Noor AM, et al. The demographics of human and malaria movement and migration patterns in East Africa. Malar J. 2013;12:397. doi: 10.1186/1475-2875-12-397.
    1. Lowassa A, Mazigo HD, Mahande AM, Mwang’onde BJ, Msangi S, Mahande MJ, et al. Social economic factors and malaria transmission in Lower Moshi, northern Tanzania. Parasit Vectors. 2012;5:129. doi: 10.1186/1756-3305-5-129.
    1. Korenromp E, Mahiané G, Hamilton M, Pretorius C, Cibulskis R, Lauer J, et al. Malaria intervention scale-up in Africa: effectiveness predictions for health programme planning tools, based on dynamic transmission modelling. Malar J. 2016;15:417. doi: 10.1186/s12936-016-1461-9.
    1. Kalanda GC, Hill J, Verhoeff FH, Brabin BJ. Comparative efficacy of chloroquine and sulphadoxine–pyrimethamine in pregnant women and children: a meta-analysis. Trop Med Int Health. 2006;11:569–577. doi: 10.1111/j.1365-3156.2006.01608.x.
    1. Fried M, Muehlenbachs A, Duffy PE. Diagnosing malaria in pregnancy: an update. Expert Rev Anti Infect Ther. 2012;10:1177–1187. doi: 10.1586/eri.12.98.
    1. Trape J-F, Rogier C, Konate L, Diagne N, Bouganali H, Canque B, et al. The Dielmo project: a longitudinal study of natural malaria infection and the mechanisms of protective immunity in a community living in a holoendemic area of Senegal. Am J Trop Med Hyg. 1994;51:123–137. doi: 10.4269/ajtmh.1994.51.123.
    1. Giha HA, Nasr A, Iriemenam NC, Balogun HA, Arnot D, Theander TG, et al. Age-dependent association between IgG2 and IgG3 subclasses to Pf332-C231 antigen and protection from malaria, and induction of protective antibodies by sub-patent malaria infections, in Daraweesh. Vaccine. 2010;28:1732–1739. doi: 10.1016/j.vaccine.2009.12.018.
    1. Baird JK, Purnomo, Basri H, Bangs MJ, Andersen EM, Jones TR, et al. Age-specific prevalence of Plasmodium falciparum among six populations with limited histories of exposure to endemic malaria. Am J Trop Med Hyg. 1993;49:707–719. doi: 10.4269/ajtmh.1993.49.707.
    1. Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri PH, et al. Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. Am J Trop Med Hyg. 1991;45:65–76. doi: 10.4269/ajtmh.1991.45.65.
    1. Baird JK. Host age as a determinant of naturally acquired immunity to Plasmodium falciparum. Parasitol Today. 1995;11:105–111. doi: 10.1016/0169-4758(95)80167-7.
    1. Riley EM, Morris-Jones S, Blackman MJ, Greenwood BM, Holder AA. A longitudinal study of naturally acquired cellular and humoral immune responses to a merozoite surface protein (MSP1) of Plasmodium falciparum in an area of seasonal malaria transmission. Parasite Immunol. 1993;15:513–524. doi: 10.1111/j.1365-3024.1993.tb00639.x.
    1. Früh K, Doumbo O, Müller HM, Koita O, McBride J, Crisanti A, et al. Human antibody response to the major merozoite surface antigen of Plasmodium falciparum is strain specific and short-lived. Infect Immun. 1991;59:1319–1324.
    1. Walldorf JA, Cohee LM, Coalson JE, Bauleni A, Nkanaunena K, Kapito-Tembo A, et al. School-age children are a reservoir of malaria infection in Malawi. PLoS ONE. 2015;10:e0134061. doi: 10.1371/journal.pone.0134061.
    1. Khagayi S, Desai M, Amek N, Were V, Onyango ED, Odero C, et al. Modelling the relationship between malaria prevalence as a measure of transmission and mortality across age groups. Malar J. 2019;18:247. doi: 10.1186/s12936-019-2869-9.
    1. Phalkey RK, Yamamoto S, Awate P, Marx M. Challenges with the implementation of an Integrated Disease Surveillance and Response (IDSR) system: systematic review of the lessons learned. Health Policy Plan. 2015;30:131–143. doi: 10.1093/heapol/czt097.
    1. van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, et al. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009-11. Lancet Infect Dis. 2013;13:1029–1042. doi: 10.1016/S1473-3099(13)70199-3.
    1. Berhan Y, Berhan A. Antenatal care as a means of increasing birth in the health facility and reducing maternal mortality: a systematic review. Ethiopian J Health Sci. 2014;24:93–104. doi: 10.4314/ejhs.v24i0.9S.
    1. Sturrock HJW, Hsiang MS, Cohen JM, Smith DL, Greenhouse B, Bousema T, et al. Targeting asymptomatic malaria infections: active surveillance in control and elimination. PLoS Med. 2013;10:e1001467. doi: 10.1371/journal.pmed.1001467.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다