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Malaria Journal
Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Risk factors for asymptomatic malaria infections from seasonal cross-sectional surveys along the China–Myanmar border

Authors: Yan Zhao, Jie Zeng, Yonghong Zhao, Qingyang Liu, Yang He, Jiaqi Zhang, Zhaoqing Yang, Qi Fan, Qinghui Wang, Liwang Cui, Yaming Cao

Published in: Malaria Journal | Issue 1/2018

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Abstract

Background

Border malaria, a shared phenomenon in the Greater Mekong Sub-region of Southeast Asia, is a major obstacle for regional malaria elimination. Along the China–Myanmar border, an additional problem arose as a result of the settlement of internally displaced people (IDP) in the border region. Since asymptomatic malaria significantly impacts transmission dynamics, assessment of the prevalence, dynamics and risk factors of asymptomatic malaria infections is necessary.

Methods

Cross-sectional surveys were carried out in 3 seasons (March and April, July and November) and 2 sites (villages and IDP camps) in 2015. A total of 1680 finger-prick blood samples were collected and used for parasite detection by microscopy and nested RT-PCR (nRT-PCR). Logistic regression models were used to explore the risk factors associated with asymptomatic malaria at individual and household levels.

Results

The prevalence of asymptomatic Plasmodium infections was 23.3% by nRT-PCR, significantly higher than that detected by microscopy (1.5%). The proportions of Plasmodium vivax, Plasmodium falciparum and mixed-species infections were 89.6, 8.1 and 2.3%, respectively. Asymptomatic infections showed obvious seasonality with higher prevalence in the rainy season. Logistic regression analysis identified males and school children (≤ 15 years) as the high-risk populations. Vector-based interventions, including bed net and indoor residual spray, were found to have significant impacts on asymptomatic Plasmodium infections, with non-users of these measures carrying much higher risks of infection. In addition, individuals living in poorly constructed households or farther away from clinics were more prone to asymptomatic infections.

Conclusions

Sub-microscopic Plasmodium infections were highly prevalent in the border human populations from IDP camps and surrounding villages. Both individual- and household-level risk factors were identified, which provides useful information for identifying the high-priority populations to implement targeted malaria control.
Literature
1.
WHO. World malaria report 2017. Geneva: World Health Organization; 2017.
2.
Committee WHOMPA, Secretariat. Malaria Policy Advisory Committee to the WHO: conclusions and recommendations of seventh biannual meeting (March 2015). Malar J. 2015;14:295.CrossRef
3.
Marsh K, Forster D, Waruiru C, Mwangi I, Winstanley M, Marsh V, et al. Indicators of life-threatening malaria in African children. N Engl J Med. 1995;332:1399–404.CrossRefPubMed
4.
Imbert P, Gerardin P, Rogier C, Ka AS, Jouvencel P, Brousse V, et al. Severe falciparum malaria in children: a comparative study of 1990 and 2000 WHO criteria for clinical presentation, prognosis and intensive care in Dakar, Senegal. Trans R Soc Trop Med Hyg. 2002;96:278–81.CrossRefPubMed
5.
Tadesse FG, van den Hoogen L, Lanke K, Schildkraut J, Tetteh K, Aseffa A, et al. The shape of the iceberg: quantification of submicroscopic Plasmodium falciparum and Plasmodium vivax parasitaemia and gametocytaemia in five low endemic settings in Ethiopia. Malar J. 2017;16:99.CrossRefPubMedPubMedCentral
6.
Imwong M, Hanchana S, Malleret B, Renia L, Day NP, Dondorp A, et al. High-throughput ultrasensitive molecular techniques for quantifying low-density malaria parasitemias. J Clin Microbiol. 2014;52:3303–9.CrossRefPubMedPubMedCentral
7.
Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med. 2015;12:e1001788.CrossRefPubMedPubMedCentral
8.
Zhao Y, Lv Y, Liu F, Wang Q, Li P, Zhao Z, et al. Comparison of methods for detecting asymptomatic malaria infections in the China–Myanmar border area. Malar J. 2017;16:159.CrossRefPubMedPubMedCentral
9.
Lennon SE, Miranda A, Henao J, Vallejo AF, Perez J, Alvarez A, et al. Malaria elimination challenges in Mesoamerica: evidence of submicroscopic malaria reservoirs in Guatemala. Malar J. 2016;15:441.CrossRefPubMedPubMedCentral
10.
Zoghi S, Mehrizi AA, Raeisi A, Haghdoost AA, Turki H, Safari R, et al. Survey for asymptomatic malaria cases in low transmission settings of Iran under elimination programme. Malar J. 2012;11:126.CrossRefPubMedPubMedCentral
11.
Stresman GH, Baidjoe AY, Stevenson J, Grignard L, Odongo W, Owaga C, et al. Focal screening to identify the subpatent parasite reservoir in an area of low and heterogeneous transmission in the Kenya Highlands. J Infect Dis. 2015;212:1768–77.CrossRefPubMed
12.
Sturrock HJ, 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.CrossRefPubMedPubMedCentral
13.
Tadesse FG, Slater HC, Chali W, Teelen K, Lanke K, Belachew M, et al. The relative contribution of symptomatic and asymptomatic Plasmodium vivax and Plasmodium falciparum infections to the infectious reservoir in a low-endemic setting in Ethiopia. Clin Infect Dis. 2018;66:1883–91.CrossRefPubMed
14.
Lin JT, Saunders DL, Meshnick SR. The role of submicroscopic parasitemia in malaria transmission: what is the evidence? Trends Parasitol. 2014;30:183–90.CrossRefPubMedPubMedCentral
15.
Kiattibutr K, Roobsoong W, Sriwichai P, Saeseu T, Rachaphaew N, Suansomjit C, et al. Infectivity of symptomatic and asymptomatic Plasmodium vivax infections to a Southeast Asian vector, Anopheles dirus. Int J Parasitol. 2017;47:163–70.CrossRefPubMed
16.
Gouagna LC, Ferguson HM, Okech BA, Killeen GF, Kabiru EW, Beier JC, et al. Plasmodium falciparum malaria disease manifestations in humans and transmission to Anopheles gambiae: a field study in Western Kenya. Parasitology. 2004;128:235–43.CrossRefPubMed
17.
Ouedraogo AL, Bastiaens GJ, Tiono AB, Guelbeogo WM, Kobylinski KC, Ouedraogo A, et al. Efficacy and safety of the mosquitocidal drug ivermectin to prevent malaria transmission after treatment: a double-blind, randomized, clinical trial. Clin Infect Dis. 2015;60:357–65.CrossRefPubMed
18.
Schneider P, Bousema JT, Gouagna LC, Otieno S, van de Vegte-Bolmer M, Omar SA, et al. Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007;76:470–4.PubMedCrossRef
19.
Cotter C, Sturrock HJ, Hsiang MS, Liu J, Phillips AA, Hwang J, et al. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet. 2013;382:900–11.CrossRefPubMed
20.
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.CrossRefPubMedPubMedCentral
21.
Cui L, Yan G, Sattabongkot J, Cao Y, Chen B, Chen X, et al. Malaria in the Greater Mekong Subregion: heterogeneity and complexity. Acta Trop. 2012;121:227–39.CrossRefPubMed
22.
23.
Wongsrichanalai C, Sirichaisinthop J, Karwacki JJ, Congpuong K, Miller RS, Pang L, et al. Drug resistant malaria on the Thai-Myanmar and Thai–Cambodian borders. Southeast Asian J Trop Med Public Health. 2001;32:41–9.PubMed
24.
Hu Y, Zhou G, Ruan Y, Lee MC, Xu X, Deng S, et al. Seasonal dynamics and microgeographical spatial heterogeneity of malaria along the China–Myanmar border. Acta Trop. 2016;157:12–9.CrossRefPubMedPubMedCentral
25.
Lo E, Zhou G, Oo W, Lee MC, Baum E, Felgner PL, et al. Molecular inference of sources and spreading patterns of Plasmodium falciparum malaria parasites in internally displaced persons settlements in Myanmar–China border area. Infect Genet Evol. 2015;33:189–96.CrossRefPubMedPubMedCentral
26.
Wangdi K, Gatton ML, Kelly GC, Clements AC. Cross-border malaria: a major obstacle for malaria elimination. Adv Parasitol. 2015;89:79–107.CrossRefPubMed
27.
Imwong M, Nguyen TN, Tripura R, Peto TJ, Lee SJ, Lwin KM, et al. The epidemiology of subclinical malaria infections in South-East Asia: findings from cross-sectional surveys in Thailand–Myanmar border areas, Cambodia, and Vietnam. Malar J. 2015;14:381.CrossRefPubMedPubMedCentral
28.
Parker DM, Matthews SA, Yan G, Zhou G, Lee MC, Sirichaisinthop J, et al. Microgeography and molecular epidemiology of malaria at the Thailand–Myanmar border in the malaria pre-elimination phase. Malar J. 2015;14:198.CrossRefPubMedPubMedCentral
29.
Polonsky JA, Ronsse A, Ciglenecki I, Rull M, Porten K. High levels of mortality, malnutrition, and measles, among recently-displaced Somali refugees in Dagahaley camp, Dadaab refugee camp complex, Kenya, 2011. Confl Health. 2013;7:1.CrossRefPubMedPubMedCentral
30.
Turner C, Turner P, Carrara V, Burgoine K, Tha Ler Htoo S, Watthanaworawit W, et al. High rates of pneumonia in children under 2 years of age in a South East Asian refugee population. PLoS ONE. 2013;8:e54026.CrossRefPubMedPubMedCentral
31.
Hershey CL, Doocy S, Anderson J, Haskew C, Spiegel P, Moss WJ. Incidence and risk factors for Malaria, pneumonia and diarrhea in children under 5 in UNHCR refugee camps: a retrospective study. Confl Health. 2011;5:24.CrossRefPubMedPubMedCentral
32.
Zhou G, Lo E, Zhong D, Wang X, Wang Y, Malla S, et al. Impact of interventions on malaria in internally displaced persons along the China–Myanmar border: 2011–2014. Malar J. 2016;15:471.CrossRefPubMedPubMedCentral
33.
Li N, Parker DM, Yang Z, Fan Q, Zhou G, Ai G, et al. Risk factors associated with slide positivity among febrile patients in a conflict zone of north-eastern Myanmar along the China–Myanmar border. Malar J. 2013;12:361.CrossRefPubMedPubMedCentral
34.
Vyas S, Kumaranayake L. Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan. 2006;21:459–68.CrossRefPubMed
35.
Hosmer DW Jr, Lemeshow S, Sturdivant RX. Model-building strategies and methods for logistic regression. Applied logistic regression. New York: Wiley; 2013. p. 89–151.
36.
Grange L, Loucoubar C, Telle O, Tall A, Faye J, Sokhna C, et al. Risk factors for Plasmodium falciparum gametocyte positivity in a longitudinal cohort. PLoS ONE. 2015;10:e0123102.CrossRefPubMedPubMedCentral
37.
Alves FP, Gil LH, Marrelli MT, Ribolla PE, Camargo EP, Da Silva LH. Asymptomatic carriers of Plasmodium spp. as infection source for malaria vector mosquitoes in the Brazilian Amazon. J Med Entomol. 2005;42:777–9.CrossRefPubMed
38.
Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833–40.CrossRefPubMed
39.
Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Jain A, Taghavian O, et al. Common asymptomatic and submicroscopic malaria infections in Western Thailand revealed in longitudinal molecular and serological studies: a challenge to malaria elimination. Malar J. 2016;15:333.CrossRefPubMedPubMedCentral
40.
Durnez L, Pareyn M, Mean V, Kim S, Khim N, Menard D, et al. Identification and characterization of areas of high and low risk for asymptomatic malaria infections at sub-village level in Ratanakiri, Cambodia. Malar J. 2018;17:27.CrossRefPubMedPubMedCentral
41.
Baum E, Sattabongkot J, Sirichaisinthop J, Kiattibutr K, Davies DH, Jain A, et al. Submicroscopic and asymptomatic Plasmodium falciparum and Plasmodium vivax infections are common in western Thailand—molecular and serological evidence. Malar J. 2015;14:95.CrossRefPubMedPubMedCentral
42.
Sumari D, Mugasa J, Selemani M, Shekalaghe S, Mugittu K, Gwakisa P. Prevalence of submicroscopic Plasmodium falciparum infections in asymptomatic children in low transmission settings in Bagamoyo, Tanzania. MWJ. 2016;7:6.
43.
Mvumbi DM, Bobanga TL, Melin P, De Mol P, Kayembe JM, Situakibanza HN, et al. High prevalence of Plasmodium falciparum infection in asymptomatic individuals from the Democratic Republic of the Congo. Malar Res Treat. 2016;2016:5405802.PubMedPubMedCentral
44.
Wang Y, Zhong D, Cui L, Lee MC, Yang Z, Yan G, et al. Population dynamics and community structure of Anopheles mosquitoes along the China–Myanmar border. Parasit Vectors. 2015;8:445.CrossRefPubMedPubMedCentral
45.
Kristan M, Abeku TA, Beard J, Okia M, Rapuoda B, Sang J, et al. Variations in entomological indices in relation to weather patterns and malaria incidence in East African highlands: implications for epidemic prevention and control. Malar J. 2008;7:231.CrossRefPubMedPubMedCentral
46.
Sturrock HJ, Novotny JM, Kunene S, Dlamini S, Zulu Z, Cohen JM, et al. Reactive case detection for malaria elimination: real-life experience from an ongoing program in Swaziland. PLoS ONE. 2013;8:e63830.CrossRefPubMedPubMedCentral
47.
Lansang MA, Belizario VY, Bustos MD, Saul A, Aguirre A. Risk factors for infection with malaria in a low endemic community in Bataan, the Philippines. Acta Trop. 1997;63:257–65.CrossRefPubMed
48.
Kleinschmidt I, Sharp B. Patterns in age-specific malaria incidence in a population exposed to low levels of malaria transmission intensity. Trop Med Int Health. 2001;6:986–91.CrossRefPubMed
49.
Monteiro TH, Chaves Tdo S, Matos HJ, Sofffiatti NF, Guimaraes RJ, Guimaraes LH, et al. Basic sanitation, socioeconomic conditions, and degree of risk for the presence and maintenance of malaria in a low-transmission area in the Brazilian Amazon. Rev Soc Bras Med Trop. 2015;48:573–9.CrossRefPubMed
50.
Quantick O, Howlett-Shipley R, Roughton S, Ross D. Malaria in British military personnel deployed to Sierra Leone: a case series. J R Army Med Corps. 2017;163:65–7.CrossRefPubMed
51.
Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev Anti Infect Ther. 2013;11:623–39.CrossRefPubMed
52.
53.
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.CrossRefPubMedPubMedCentral
54.
Chourasia MK, Raghavendra K, Bhatt RM, Swain DK, Valecha N, Kleinschmidt I. Burden of asymptomatic malaria among a tribal population in a forested village of central India: a hidden challenge for malaria control in India. Public Health. 2017;147:92–7.CrossRefPubMedPubMedCentral
55.
Coalson JE, Walldorf JA, Cohee LM, Ismail MD, Mathanga D, Cordy RJ, et al. High prevalence of Plasmodium falciparum gametocyte infections in school-age children using molecular detection: patterns and predictors of risk from a cross-sectional study in southern Malawi. Malar J. 2016;15:527.CrossRefPubMedPubMedCentral
56.
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.CrossRefPubMedPubMedCentral
57.
Lin E, Kiniboro B, Gray L, Dobbie S, Robinson L, Laumaea A, et al. Differential patterns of infection and disease with P. falciparum and P. vivax in young Papua New Guinean children. PLoS ONE. 2010;5:e9047.CrossRefPubMedPubMedCentral
58.
Bhatt S, Weiss DJ, Cameron E, Bisanzio D, Mappin B, Dalrymple U, et al. The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature. 2015;526:207–11.CrossRefPubMedPubMedCentral
59.
Mullany LC, Lee CI, Paw P, Shwe Oo EK, Maung C, Kuiper H, et al. The MOM Project: delivering maternal health services among internally displaced populations in eastern Burma. Reprod Health Matters. 2008;16:44–56.CrossRefPubMed
60.
61.
Hiscox A, Khammanithong P, Kaul S, Sananikhom P, Luthi R, Hill N, et al. Risk factors for mosquito house entry in the Lao PDR. PLoS ONE. 2013;8:e62769.CrossRefPubMedPubMedCentral
62.
Lwetoijera DW, Kiware SS, Mageni ZD, Dongus S, Harris C, Devine GJ, et al. A need for better housing to further reduce indoor malaria transmission in areas with high bed net coverage. Parasit Vectors. 2013;6:57.CrossRefPubMedPubMedCentral
63.
Coleman M, Coleman M, Mabaso ML, Mabuza AM, Kok G, Coetzee M, et al. Household and microeconomic factors associated with malaria in Mpumalanga, South Africa. Trans R Soc Trop Med Hyg. 2010;104:143–7.CrossRefPubMed
64.
Liu JX, Bousema T, Zelman B, Gesase S, Hashim R, Maxwell C, et al. Is housing quality associated with malaria incidence among young children and mosquito vector numbers? Evidence from Korogwe, Tanzania. PLoS One. 2014;9:e87358.CrossRefPubMedPubMedCentral
65.
Pinchoff J, Henostroza G, Carter BS, Roberts ST, Hatwiinda S, Hamainza B, et al. Spatial patterns of incident malaria cases and their household contacts in a single clinic catchment area of Chongwe District, Zambia. Malar J. 2015;14:305.CrossRefPubMedPubMedCentral
66.
Hsiang MS, Hwang J, Tao AR, Liu Y, Bennett A, Shanks GD, et al. Mass drug administration for the control and elimination of Plasmodium vivax malaria: an ecological study from Jiangsu province, China. Malar J. 2013;12:383.CrossRefPubMedPubMedCentral
67.
Cao J, Sturrock HJ, Cotter C, Zhou S, Zhou H, Liu Y, et al. Communicating and monitoring surveillance and response activities for malaria elimination: China’s “1-3-7” strategy. PLoS Med. 2014;11:e1001642.CrossRefPubMedPubMedCentral
Metadata
Title
Risk factors for asymptomatic malaria infections from seasonal cross-sectional surveys along the China–Myanmar border
Authors
Yan Zhao
Jie Zeng
Yonghong Zhao
Qingyang Liu
Yang He
Jiaqi Zhang
Zhaoqing Yang
Qi Fan
Qinghui Wang
Liwang Cui
Yaming Cao
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2398-y

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