Skip to main content
Top
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Malaria risk factor assessment using active and passive surveillance data from Aceh Besar, Indonesia, a low endemic, malaria elimination setting with Plasmodium knowlesi, Plasmodium vivax, and Plasmodium falciparum

Authors: Herdiana Herdiana, Chris Cotter, Farah N. Coutrier, Iska Zarlinda, Brittany W. Zelman, Yusrifar Kharisma Tirta, Bryan Greenhouse, Roly D. Gosling, Peter Baker, Maxine Whittaker, Michelle S. Hsiang

Published in: Malaria Journal | Issue 1/2016

Login to get access

Abstract

Background

As malaria transmission declines, it becomes more geographically focused and more likely due to asymptomatic and non-falciparum infections. To inform malaria elimination planning in the context of this changing epidemiology, local assessments on the risk factors for malaria infection are necessary, yet challenging due to the low number of malaria cases.

Methods

A population-based, cross-sectional study was performed using passive and active surveillance data collected in Aceh Besar District, Indonesia from 2014 to 2015. Malaria infection was defined as symptomatic polymerase chain reaction (PCR)-confirmed infection in index cases reported from health facilities, and asymptomatic or symptomatic PCR-confirmed infection identified in reactive case detection (RACD). Potential risk factors for any infection, species-specific infection, or secondary-case detection in RACD were assessed through questionnaires and evaluated for associations.

Results

Nineteen Plasmodium knowlesi, 12 Plasmodium vivax and six Plasmodium falciparum cases were identified passively, and 1495 community members screened in RACD, of which six secondary cases were detected (one P. knowlesi, three P. vivax, and two P. falciparum, with four being asymptomatic). Compared to non-infected subjects screened in RACD, cases identified through passive or active surveillance were more likely to be male (AOR 12.5, 95 % CI 3.0–52.1), adult (AOR 14.0, 95 % CI 2.2–89.6 for age 16–45 years compared to <15 years), have visited the forest in the previous month for any reason (AOR 5.6, 95 % CI 1.3–24.2), and have a workplace near or in the forest and requiring overnight stays (AOR 7.9, 95 % CI 1.6–39.7 compared to workplace not near or in the forest). Comparing subjects with infections of different species, differences were observed in sub-district of residence and other demographic and behavioural factors. Among subjects screened in RACD, cases compared to non-cases were more likely to be febrile and reside within 100 m of the index case.

Conclusion

In this setting, risk of malaria infection in index and RACD identified cases was associated with forest exposure, particularly overnights in the forest for work. In low-transmission settings, utilization of data available through routine passive and active surveillance can support efforts to target individuals at high risk.
Literature
3.
go back to reference Cotter C, Sturrock HJW, 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 Cotter C, Sturrock HJW, 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
4.
go back to reference Snow RW, Marsh K. New insights into the epidemiology of malaria relevant for disease control. Br Med Bull. 1998;54:293–309.CrossRefPubMed Snow RW, Marsh K. New insights into the epidemiology of malaria relevant for disease control. Br Med Bull. 1998;54:293–309.CrossRefPubMed
5.
go back to reference 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:e617–28.CrossRefPubMedPubMedCentral 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:e617–28.CrossRefPubMedPubMedCentral
6.
go back to reference Worrall E, Basu S, Hanson K. Is malaria a disease of poverty? A review of the literature. Trop Med Int Health. 2005;10:1047–59.CrossRefPubMed Worrall E, Basu S, Hanson K. Is malaria a disease of poverty? A review of the literature. Trop Med Int Health. 2005;10:1047–59.CrossRefPubMed
7.
go back to reference Zoungrana A, Chou Y-J, Pu C. Socioeconomic and environment determinants as predictors of severe malaria in children under 5 years of age admitted in two hospitals in Koudougou district, Burkina Faso: a cross sectional study. Acta Trop. 2014;139:109–14.CrossRefPubMed Zoungrana A, Chou Y-J, Pu C. Socioeconomic and environment determinants as predictors of severe malaria in children under 5 years of age admitted in two hospitals in Koudougou district, Burkina Faso: a cross sectional study. Acta Trop. 2014;139:109–14.CrossRefPubMed
8.
go back to reference 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 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
9.
go back to reference Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, et al. Community-wide effects of permethrin-treated bed nets on child mortality and morbidity in western Kenya. Am J Trop Med Hyg. 2003;68(4 Suppl):121–7.PubMed Hawley WA, Phillips-Howard PA, ter Kuile FO, Terlouw DJ, Vulule JM, Ombok M, et al. Community-wide effects of permethrin-treated bed nets on child mortality and morbidity in western Kenya. Am J Trop Med Hyg. 2003;68(4 Suppl):121–7.PubMed
10.
go back to reference Littrell M, Sow GD, Ngom A, Ba M, Mboup BM, Dieye Y, et al. Case investigation and reactive case detection for malaria elimination in northern Senegal. Malar J. 2013;12:331.CrossRefPubMedPubMedCentral Littrell M, Sow GD, Ngom A, Ba M, Mboup BM, Dieye Y, et al. Case investigation and reactive case detection for malaria elimination in northern Senegal. Malar J. 2013;12:331.CrossRefPubMedPubMedCentral
11.
go back to reference Liu Y, Hsiang MS, Zhou H, Wang W, Cao Y, Gosling RD, et al. Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu Province, 2001–2011. Malar J. 2014;13:29.CrossRefPubMedPubMedCentral Liu Y, Hsiang MS, Zhou H, Wang W, Cao Y, Gosling RD, et al. Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu Province, 2001–2011. Malar J. 2014;13:29.CrossRefPubMedPubMedCentral
12.
go back to reference Hsiang MS, Hwang J, Kunene S, Drakeley C, Kandula D, Novotny J, et al. Surveillance for malaria elimination in Swaziland: a national cross-sectional study using pooled PCR and serology. PLoS One. 2012;7:e29550.CrossRefPubMedPubMedCentral Hsiang MS, Hwang J, Kunene S, Drakeley C, Kandula D, Novotny J, et al. Surveillance for malaria elimination in Swaziland: a national cross-sectional study using pooled PCR and serology. PLoS One. 2012;7:e29550.CrossRefPubMedPubMedCentral
14.
go back to reference Gueye CS, Sanders KC, Galappaththy GNL, Rundi C, Tobgay T, Sovannaroth S, et al. Active case detection for malaria elimination: a survey among Asia Pacific countries. Malar J. 2013;12:358.CrossRef Gueye CS, Sanders KC, Galappaththy GNL, Rundi C, Tobgay T, Sovannaroth S, et al. Active case detection for malaria elimination: a survey among Asia Pacific countries. Malar J. 2013;12:358.CrossRef
16.
go back to reference van Eijk AM, Ramanathapuram L, Sutton PL, Kanagaraj D, Priya GSL, Ravishankaran S, et al. What is the value of reactive case detection in malaria control? A case-study in India and a systematic review. Malar J. 2016;15:67.CrossRefPubMedPubMedCentral van Eijk AM, Ramanathapuram L, Sutton PL, Kanagaraj D, Priya GSL, Ravishankaran S, et al. What is the value of reactive case detection in malaria control? A case-study in India and a systematic review. Malar J. 2016;15:67.CrossRefPubMedPubMedCentral
17.
go back to reference Hustedt J, Canavati SE, Rang C, Ashton RA, Khim N, Berne L, et al. Reactive case-detection of malaria in Pailin Province, Western Cambodia: lessons from a year-long evaluation in a pre-elimination setting. Malar J. 2016;15:132.CrossRefPubMedPubMedCentral Hustedt J, Canavati SE, Rang C, Ashton RA, Khim N, Berne L, et al. Reactive case-detection of malaria in Pailin Province, Western Cambodia: lessons from a year-long evaluation in a pre-elimination setting. Malar J. 2016;15:132.CrossRefPubMedPubMedCentral
18.
go back to reference WHO. World malaria report 2009. Geneva: World Health Organization; 2009. WHO. World malaria report 2009. Geneva: World Health Organization; 2009.
19.
go back to reference WHO. World malaria report 2015. Geneva: World Health Organization; 2015. WHO. World malaria report 2015. Geneva: World Health Organization; 2015.
20.
go back to reference Surya A. Indonesia gap analysis. In: Asia Pacific malaria elimination network advocacy workshop, Bangkok, Thailand; 2014. Surya A. Indonesia gap analysis. In: Asia Pacific malaria elimination network advocacy workshop, Bangkok, Thailand; 2014.
21.
go back to reference Coutrier F, Cotter C, Tirta Y, Schwartz A, Zarlinda I, Basri H, et al. Serial molecular identification to confirm the presence of Plasmodium knowlesi in Indonesia. In: Poster session presented at: 64th annual meeting of the American society for tropical medicine and hygiene; 2015 Oct 25–29; Philadelphia. Coutrier F, Cotter C, Tirta Y, Schwartz A, Zarlinda I, Basri H, et al. Serial molecular identification to confirm the presence of Plasmodium knowlesi in Indonesia. In: Poster session presented at: 64th annual meeting of the American society for tropical medicine and hygiene; 2015 Oct 25–29; Philadelphia.
22.
go back to reference BPS. Aceh Besar dalam angka 2015 (Aceh Besar in figure 2015). Aceh Besar: Badan Pusat Statistik (Central Bureau of Statistics); 2015. BPS. Aceh Besar dalam angka 2015 (Aceh Besar in figure 2015). Aceh Besar: Badan Pusat Statistik (Central Bureau of Statistics); 2015.
23.
go back to reference BPS. Aceh Besar dalam angka 2012 (Aceh Besar in figure 2012). Aceh Besar: Badan Pusat Statistik (Central Bureau of Statistics); 2012. BPS. Aceh Besar dalam angka 2012 (Aceh Besar in figure 2012). Aceh Besar: Badan Pusat Statistik (Central Bureau of Statistics); 2012.
24.
go back to reference Dinkes Aceh Besar. Profil kesehatan Kabupaten Aceh Besar tahun 2006 (District health profile of Aceh Besar 2006). Kota Jantho: Dinas Kesehatan Kabupaten Aceh Besar (District Health Office of Aceh Besar); 2006. Dinkes Aceh Besar. Profil kesehatan Kabupaten Aceh Besar tahun 2006 (District health profile of Aceh Besar 2006). Kota Jantho: Dinas Kesehatan Kabupaten Aceh Besar (District Health Office of Aceh Besar); 2006.
25.
go back to reference BPS. Aceh Besar dalam angka 2013 (Aceh Besar in figure 2013). Aceh Besar: Badan Pusat Statistik (Central Bureau of Statistics); 2013. BPS. Aceh Besar dalam angka 2013 (Aceh Besar in figure 2013). Aceh Besar: Badan Pusat Statistik (Central Bureau of Statistics); 2013.
26.
go back to reference Dinkes Provinsi Aceh. Panduan lapangan penyelidikan epidemiologi malaria bagi petugas puskesmas dan dinas kesehatan kabupaten/kota (Field manual of epidemiology investigation of malaria for primary health center and district health office staff). Aceh: Dinas Kesehatan Provinsi Aceh (Provincial Health Office of Aceh); 2012. Dinkes Provinsi Aceh. Panduan lapangan penyelidikan epidemiologi malaria bagi petugas puskesmas dan dinas kesehatan kabupaten/kota (Field manual of epidemiology investigation of malaria for primary health center and district health office staff). Aceh: Dinas Kesehatan Provinsi Aceh (Provincial Health Office of Aceh); 2012.
27.
go back to reference Balitbangkes. Riset kesehatan dasar 2013 (Basic health research 2013). Jakarta: Badan Penelitian dan Pengembangan Kesehatan Kementerian Kesehatan RI (National Institute of Health and Research Development); 2013. Balitbangkes. Riset kesehatan dasar 2013 (Basic health research 2013). Jakarta: Badan Penelitian dan Pengembangan Kesehatan Kementerian Kesehatan RI (National Institute of Health and Research Development); 2013.
28.
go back to reference Menteri Kesehatan RI. Peraturan tatalaksana malaria (Management malaria case regulation). In: Permenkes No 5/MENKES/Per/I/2013 (Indonesia KKR editor, vol. Nomor 5 Tahun 2013): Menteri Hukum dan Hak Asasi Manusia (Minister of Law and Human Rights); 2013. Menteri Kesehatan RI. Peraturan tatalaksana malaria (Management malaria case regulation). In: Permenkes No 5/MENKES/Per/I/2013 (Indonesia KKR editor, vol. Nomor 5 Tahun 2013): Menteri Hukum dan Hak Asasi Manusia (Minister of Law and Human Rights); 2013.
29.
go back to reference Ho W. Basic malaria microscopy. Part 1: Learner’s guide. Geneva: World Health Organization; 2010. Ho W. Basic malaria microscopy. Part 1: Learner’s guide. Geneva: World Health Organization; 2010.
30.
go back to reference Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMed Plowe CV, Djimde A, Bouare M, Doumbo O, Wellems TE. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg. 1995;52:565–8.PubMed
31.
go back to reference Aydin-Schmidt B, Xu W, Gonzalez IJ, Polley SD, Bell D, Shakely D, et al. Loop mediated isothermal amplification (LAMP) accurately detects malaria DNA from filter paper blood samples of low density parasitaemias. PLoS One. 2014;9:e103905.CrossRefPubMedPubMedCentral Aydin-Schmidt B, Xu W, Gonzalez IJ, Polley SD, Bell D, Shakely D, et al. Loop mediated isothermal amplification (LAMP) accurately detects malaria DNA from filter paper blood samples of low density parasitaemias. PLoS One. 2014;9:e103905.CrossRefPubMedPubMedCentral
32.
go back to reference Hopkins H, Gonzalez IJ, Polley SD, Angutoko P, Ategeka J, Asiimwe C, et al. Highly sensitive detection of malaria parasitemia in a malaria-endemic setting: performance of a new loop-mediated isothermal amplification kit in a remote clinic in Uganda. J Infect Dis. 2013;208:645–52.CrossRefPubMedPubMedCentral Hopkins H, Gonzalez IJ, Polley SD, Angutoko P, Ategeka J, Asiimwe C, et al. Highly sensitive detection of malaria parasitemia in a malaria-endemic setting: performance of a new loop-mediated isothermal amplification kit in a remote clinic in Uganda. J Infect Dis. 2013;208:645–52.CrossRefPubMedPubMedCentral
33.
go back to reference Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, et al. Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malar J. 2010;9:108.CrossRefPubMedPubMedCentral Steenkeste N, Rogers WO, Okell L, Jeanne I, Incardona S, Duval L, et al. Sub-microscopic malaria cases and mixed malaria infection in a remote area of high malaria endemicity in Rattanakiri province, Cambodia: implication for malaria elimination. Malar J. 2010;9:108.CrossRefPubMedPubMedCentral
34.
go back to reference Hsiang MS, Lin M, Dokomajilar C, Kemere J, Pilcher CD, Dorsey G, et al. PCR-based pooling of dried blood spots for detection of malaria parasites: optimization and application to a cohort of Ugandan children. J Clin Microbiol. 2010;48:3539–43.CrossRefPubMedPubMedCentral Hsiang MS, Lin M, Dokomajilar C, Kemere J, Pilcher CD, Dorsey G, et al. PCR-based pooling of dried blood spots for detection of malaria parasites: optimization and application to a cohort of Ugandan children. J Clin Microbiol. 2010;48:3539–43.CrossRefPubMedPubMedCentral
35.
go back to reference Schwartz A, Baidjoe A, Rosenthal PJ, Dorsey G, Bousema T, Greenhouse B. The effect of storage and extraction methods on amplification of Plasmodium falciparum DNA from dried blood spots. Am J Trop Med Hyg. 2015;92:922–5.CrossRefPubMedPubMedCentral Schwartz A, Baidjoe A, Rosenthal PJ, Dorsey G, Bousema T, Greenhouse B. The effect of storage and extraction methods on amplification of Plasmodium falciparum DNA from dried blood spots. Am J Trop Med Hyg. 2015;92:922–5.CrossRefPubMedPubMedCentral
36.
go back to reference Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol. 1993;58:283–92.CrossRefPubMed Snounou G, Viriyakosol S, Jarra W, Thaithong S, Brown KN. Identification of the four human malaria parasite species in field samples by the polymerase chain reaction and detection of a high prevalence of mixed infections. Mol Biochem Parasitol. 1993;58:283–92.CrossRefPubMed
37.
go back to reference Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60:687–92.PubMed Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60:687–92.PubMed
38.
go back to reference Imwong M, Tanomsing N, Pukrittayakamee S, Day NPJ, White NJ, Snounou G. Spurious amplification of a Plasmodium vivax small-subunit RNA gene by use of primers currently used to detect P. knowlesi. J Clin Microbiol. 2009;47:4173–5.CrossRefPubMedPubMedCentral Imwong M, Tanomsing N, Pukrittayakamee S, Day NPJ, White NJ, Snounou G. Spurious amplification of a Plasmodium vivax small-subunit RNA gene by use of primers currently used to detect P. knowlesi. J Clin Microbiol. 2009;47:4173–5.CrossRefPubMedPubMedCentral
39.
go back to reference Hosmer Jr DW, Lemeshow S, Sturdivant RX. Model-building strategies and methods for logistic regression. In: Applied logistic regression. New York: Wiley; 2013. p. 89–151. doi: 10.1002/9781118548387.ch4. Hosmer Jr DW, Lemeshow S, Sturdivant RX. Model-building strategies and methods for logistic regression. In: Applied logistic regression. New York: Wiley; 2013. p. 89–151. doi: 10.​1002/​9781118548387.​ch4.
41.
go back to reference Stoica P, Selen Y, Li J. On information criteria and the generalized likelihood ratio test of model order selection. IEEE Signal Process Lett. 2004;11:794–7.CrossRef Stoica P, Selen Y, Li J. On information criteria and the generalized likelihood ratio test of model order selection. IEEE Signal Process Lett. 2004;11:794–7.CrossRef
42.
go back to reference Howe LD, Hargreaves JR, Huttly SRA. Issues in the construction of wealth indices for the measurement of socio-economic position in low-income countries. Emerg Themes Epidemiol. 2008;5:3.CrossRefPubMedPubMedCentral Howe LD, Hargreaves JR, Huttly SRA. Issues in the construction of wealth indices for the measurement of socio-economic position in low-income countries. Emerg Themes Epidemiol. 2008;5:3.CrossRefPubMedPubMedCentral
43.
44.
go back to reference Sulistyaningsih E, Fitri LE, Löscher T, Berens-Riha N. Diagnostic difficulties with Plasmodium knowlesi infection in humans. Emerg Infect Dis. 2010;16:1033–4.CrossRefPubMedPubMedCentral Sulistyaningsih E, Fitri LE, Löscher T, Berens-Riha N. Diagnostic difficulties with Plasmodium knowlesi infection in humans. Emerg Infect Dis. 2010;16:1033–4.CrossRefPubMedPubMedCentral
45.
go back to reference Lansang MAD, Belizario VY, Bustos MDG, 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 Lansang MAD, Belizario VY, Bustos MDG, 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
46.
go back to reference 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 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
47.
go back to reference Monteiro TH, Chaves Tdo S, Matos HJ, Sofffiatti NF, Guimarães RJ, Guimarães 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 Monteiro TH, Chaves Tdo S, Matos HJ, Sofffiatti NF, Guimarães RJ, Guimarães 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
48.
go back to reference Barbara KA, Sukowati S, Rusmiarto S, Susapto D, Bangs MJ, Kinzer MH. Survey of Anopheles mosquitoes (Diptera: Culicidae) in West Sumba District, Indonesia. Southeast Asian J Trop Med Public Health. 2011;42:71–82.PubMed Barbara KA, Sukowati S, Rusmiarto S, Susapto D, Bangs MJ, Kinzer MH. Survey of Anopheles mosquitoes (Diptera: Culicidae) in West Sumba District, Indonesia. Southeast Asian J Trop Med Public Health. 2011;42:71–82.PubMed
49.
go back to reference Barber BE, William T, Grigg MJ, Yeo TW, Anstey NM. Limitations of microscopy to differentiate Plasmodium species in a region co-endemic for Plasmodium falciparum, Plasmodium vivax and Plasmodium knowlesi. Malar J. 2013;12:8.CrossRefPubMedPubMedCentral Barber BE, William T, Grigg MJ, Yeo TW, Anstey NM. Limitations of microscopy to differentiate Plasmodium species in a region co-endemic for Plasmodium falciparum, Plasmodium vivax and Plasmodium knowlesi. Malar J. 2013;12:8.CrossRefPubMedPubMedCentral
50.
go back to reference Barber BE, William T, Dhararaj P, Anderios F, Grigg MJ, Yeo TW, et al. Epidemiology of Plasmodium knowlesi malaria in north-east Sabah, Malaysia: family clusters and wide age distribution. Malar J. 2012;11:401.CrossRefPubMedPubMedCentral Barber BE, William T, Dhararaj P, Anderios F, Grigg MJ, Yeo TW, et al. Epidemiology of Plasmodium knowlesi malaria in north-east Sabah, Malaysia: family clusters and wide age distribution. Malar J. 2012;11:401.CrossRefPubMedPubMedCentral
51.
go back to reference Stresman GH, Kamanga A, Moono P, Hamapumbu H, Mharakurwa S, Kobayashi T, et al. A method of active case detection to target reservoirs of asymptomatic malaria and gametocyte carriers in a rural area in Southern Province, Zambia. Malar J. 2010;9:265.PubMedPubMedCentral Stresman GH, Kamanga A, Moono P, Hamapumbu H, Mharakurwa S, Kobayashi T, et al. A method of active case detection to target reservoirs of asymptomatic malaria and gametocyte carriers in a rural area in Southern Province, Zambia. Malar J. 2010;9:265.PubMedPubMedCentral
52.
go back to reference Rulisa S, Kateera F, Bizimana JP, Agaba S, Dukuzumuremyi J, Baas L, et al. Malaria prevalence, spatial clustering and risk factors in a low endemic area of Eastern Rwanda: a cross sectional study. PLoS One. 2013;8:e69443.CrossRefPubMedPubMedCentral Rulisa S, Kateera F, Bizimana JP, Agaba S, Dukuzumuremyi J, Baas L, et al. Malaria prevalence, spatial clustering and risk factors in a low endemic area of Eastern Rwanda: a cross sectional study. PLoS One. 2013;8:e69443.CrossRefPubMedPubMedCentral
53.
go back to reference 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 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
54.
go back to reference Sanders KC, Rundi C, Jelip J, Rashman Y, Smith Gueye C, Gosling RD. Eliminating malaria in Malaysia: the role of partnerships between the public and commercial sectors in Sabah. Malar J. 2014;13:24.CrossRefPubMedPubMedCentral Sanders KC, Rundi C, Jelip J, Rashman Y, Smith Gueye C, Gosling RD. Eliminating malaria in Malaysia: the role of partnerships between the public and commercial sectors in Sabah. Malar J. 2014;13:24.CrossRefPubMedPubMedCentral
55.
go back to reference Guyant P, Canavati SE, Chea N, Ly P, Whittaker MA, Roca-Feltrer A, et al. Malaria and the mobile and migrant population in Cambodia: a population movement framework to inform strategies for malaria control and elimination. Malar J. 2015;14:252.CrossRefPubMedPubMedCentral Guyant P, Canavati SE, Chea N, Ly P, Whittaker MA, Roca-Feltrer A, et al. Malaria and the mobile and migrant population in Cambodia: a population movement framework to inform strategies for malaria control and elimination. Malar J. 2015;14:252.CrossRefPubMedPubMedCentral
56.
go back to reference Webb P, Bain C. Essential epidemiology: an introduction for students and health professionals. Leiden: Cambridge University Press; 2011. Webb P, Bain C. Essential epidemiology: an introduction for students and health professionals. Leiden: Cambridge University Press; 2011.
57.
go back to reference Grigg MJ, William T, Drakeley CJ, Jelip J, von Seidlein L, Barber BE, et al. Factors that are associated with the risk of acquiring Plasmodium knowlesi malaria in Sabah, Malaysia: a case-control study protocol. BMJ Open. 2014;4:e006004.CrossRefPubMedPubMedCentral Grigg MJ, William T, Drakeley CJ, Jelip J, von Seidlein L, Barber BE, et al. Factors that are associated with the risk of acquiring Plasmodium knowlesi malaria in Sabah, Malaysia: a case-control study protocol. BMJ Open. 2014;4:e006004.CrossRefPubMedPubMedCentral
Metadata
Title
Malaria risk factor assessment using active and passive surveillance data from Aceh Besar, Indonesia, a low endemic, malaria elimination setting with Plasmodium knowlesi, Plasmodium vivax, and Plasmodium falciparum
Authors
Herdiana Herdiana
Chris Cotter
Farah N. Coutrier
Iska Zarlinda
Brittany W. Zelman
Yusrifar Kharisma Tirta
Bryan Greenhouse
Roly D. Gosling
Peter Baker
Maxine Whittaker
Michelle S. Hsiang
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1523-z

Other articles of this Issue 1/2016

Malaria Journal 1/2016 Go to the issue