Skip to main content
Top
Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Reactive case detection of Plasmodium falciparum in western Kenya highlands: effective in identifying additional cases, yet limited effect on transmission

Authors: Ebenezer K. Aidoo, Yaw A. Afrane, Maxwell Gesuge Machani, Winnie Chebore, Bernard Walter Lawson, Harrysone Atieli, Simon Kariuki, Ming-Chieh Lee, Cristian Koepfli, Guofa Zhou, Andrew K. Githeko, Guiyun Yan

Published in: Malaria Journal | Issue 1/2018

Login to get access

Abstract

Background

Identifying asymptomatic reservoirs of malaria parasites using index cases as entry points into the community is potentially a cost-effective way towards achieving malaria elimination.

Methods

Within 1 year, 1430 confirmed malaria cases were identified in Marani hospital, western Kenya. Fifty cases were followed up, and 108 index case household members and 612 neighbours within a 100 m radius were screened. As controls, samples were collected from 510 individuals matched with index cases and located at a distance of ≥ 500 m from them. Infections were diagnosed by microscopy and PCR while simultaneously collecting malaria vectors indoor using pyrethrum spray catches.

Results

In the index case and neighbour households, the prevalence of infection was approximately twice as high as in control households (by PCR: index cases households: 28.9%, neighbours: 25.3%, matched controls: 12.9%). In index case households, the indoor vector density (Anopheles gambiae and Anopheles funestus) was higher (0.46 female/house/night) than in neighbouring (0.31 f/h/n) and control houses (0.29 f/h/n).

Conclusions

Screening index case households and neighbours approximately doubles the chance to detect asymptomatic infections compared to randomly selected households. However, even if all cases were followed up, only a small proportion (˂ 10%) of the asymptomatic reservoir in the population would have been identified. Control programmes need to weigh the increased chance to find cases around index cases vs. the logistical challenges to target this subgroup within the population.
Literature
1.
go back to reference WHO, UNICEF. Achieving the malaria MDG target: reversing the incidence of malaria 2000–2015. Geneva: World Health Organization; 2015. WHO, UNICEF. Achieving the malaria MDG target: reversing the incidence of malaria 2000–2015. Geneva: World Health Organization; 2015.
2.
go back to reference Ohrt C, Roberts KW, Sturrock HJ, Wegbreit J, Lee BY, Gosling RD. Information systems to support surveillance for malaria elimination. Am J Trop Med Hyg. 2015;93:145–52.CrossRefPubMedPubMedCentral Ohrt C, Roberts KW, Sturrock HJ, Wegbreit J, Lee BY, Gosling RD. Information systems to support surveillance for malaria elimination. Am J Trop Med Hyg. 2015;93:145–52.CrossRefPubMedPubMedCentral
3.
go back to reference RBM. Global malaria action plan. Geneva: Roll Back Malaria; 2011. RBM. Global malaria action plan. Geneva: Roll Back Malaria; 2011.
4.
go back to reference Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6(5):e20318.CrossRefPubMedPubMedCentral Zhou G, Afrane YA, Vardo-Zalik AM, Atieli H, Zhong D, Wamae P, et al. Changing patterns of malaria epidemiology between 2002 and 2010 in Western Kenya: the fall and rise of malaria. PLoS ONE. 2011;6(5):e20318.CrossRefPubMedPubMedCentral
5.
go back to reference Zhou G, Lee MC, Githeko AK, Atieli HE, Yan G. Insecticide-treated net campaign and malaria transmission in Western Kenya: 2003–2015. Front Public Health. 2016;4:153.CrossRefPubMedPubMedCentral Zhou G, Lee MC, Githeko AK, Atieli HE, Yan G. Insecticide-treated net campaign and malaria transmission in Western Kenya: 2003–2015. Front Public Health. 2016;4:153.CrossRefPubMedPubMedCentral
6.
go back to reference 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 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
7.
go back to reference Karl S, Gurarie D, Zimmerman PA, King CH, St Pierre TG, Davis TM. A submicroscopic gametocyte reservoir can sustain malaria transmission. PLoS ONE. 2011;6:e20805.CrossRefPubMedPubMedCentral Karl S, Gurarie D, Zimmerman PA, King CH, St Pierre TG, Davis TM. A submicroscopic gametocyte reservoir can sustain malaria transmission. PLoS ONE. 2011;6:e20805.CrossRefPubMedPubMedCentral
8.
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.CrossRefPubMedPubMedCentral 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
9.
go back to reference Roberts DR, Vanzie E, Rejmankova E, Masuoka P, Andre R. Use of remote sensing and geographic information systems to target malaria control measures in Belize, Central America. Washington: Scope Malaria Research and Policy; 1999. Roberts DR, Vanzie E, Rejmankova E, Masuoka P, Andre R. Use of remote sensing and geographic information systems to target malaria control measures in Belize, Central America. Washington: Scope Malaria Research and Policy; 1999.
10.
go back to reference Mogeni P, Williams TN, Omedo I, Kimani D, Ngoi JM, Mwacharo J, et al. Detecting malaria hotspots: a comparison of rapid diagnostic test, microscopy, and polymerase chain reaction. J Infect Dis. 2017;216:1091–8.CrossRefPubMed Mogeni P, Williams TN, Omedo I, Kimani D, Ngoi JM, Mwacharo J, et al. Detecting malaria hotspots: a comparison of rapid diagnostic test, microscopy, and polymerase chain reaction. J Infect Dis. 2017;216:1091–8.CrossRefPubMed
11.
go back to reference Parker DM, Landier J, Seidlein L, Dondorp A, White L, Hanboonkunupakarn B, et al. Limitations of malaria reactive case detection in an area of low and unstable transmission on the Myanmar-Thailand border. Malar J. 2016;15:571.CrossRefPubMedPubMedCentral Parker DM, Landier J, Seidlein L, Dondorp A, White L, Hanboonkunupakarn B, et al. Limitations of malaria reactive case detection in an area of low and unstable transmission on the Myanmar-Thailand border. Malar J. 2016;15:571.CrossRefPubMedPubMedCentral
12.
go back to reference WHO. Disease surveillance for malaria elimination: an operational manual. Geneva: World Health Organization; 2012. WHO. Disease surveillance for malaria elimination: an operational manual. Geneva: World Health Organization; 2012.
13.
go back to reference Moonen B, Cohen JM, Snow RW, Slutsker L, Drakeley C, Smith DL, et al. Operational strategies to achieve and maintain malaria elimination. Lancet. 2010;376:1592–603.CrossRefPubMedPubMedCentral Moonen B, Cohen JM, Snow RW, Slutsker L, Drakeley C, Smith DL, et al. Operational strategies to achieve and maintain malaria elimination. Lancet. 2010;376:1592–603.CrossRefPubMedPubMedCentral
14.
go back to reference Searle KM, Shields T, Hamapumbu H, Kobayashi T, Mharakurwa S, Thuma PE, et al. Efficiency of household reactive case detection for malaria in rural Southern Zambia: simulations based on cross-sectional surveys from two epidemiological settings. PLoS ONE. 2013;8:e70972.CrossRefPubMedPubMedCentral Searle KM, Shields T, Hamapumbu H, Kobayashi T, Mharakurwa S, Thuma PE, et al. Efficiency of household reactive case detection for malaria in rural Southern Zambia: simulations based on cross-sectional surveys from two epidemiological settings. PLoS ONE. 2013;8:e70972.CrossRefPubMedPubMedCentral
15.
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
16.
go back to reference 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(5):e63830.CrossRefPubMedPubMedCentral 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(5):e63830.CrossRefPubMedPubMedCentral
17.
go back to reference Fontoura PS, Finco BF, Lima NF, de Carvalho JF Jr, Vinetz JM, Castro MC, et al. Reactive case detection for Plasmodium vivax malaria elimination in Rural Amazonia. PLoS Negl Trop Dis. 2016;10(12):e0005221.CrossRefPubMedPubMedCentral Fontoura PS, Finco BF, Lima NF, de Carvalho JF Jr, Vinetz JM, Castro MC, et al. Reactive case detection for Plasmodium vivax malaria elimination in Rural Amazonia. PLoS Negl Trop Dis. 2016;10(12):e0005221.CrossRefPubMedPubMedCentral
18.
go back to reference Lawpoolsri S, Chavez IF, Yimsamran S, Puangsa-Art S, Thanyavanich N, Maneeboonyang W, et al. The impact of human reservoir of malaria at a community-level on individual malaria occurrence in a low malaria transmission setting along the Thai-Myanmar border. Malar J. 2010;9:143.CrossRefPubMedPubMedCentral Lawpoolsri S, Chavez IF, Yimsamran S, Puangsa-Art S, Thanyavanich N, Maneeboonyang W, et al. The impact of human reservoir of malaria at a community-level on individual malaria occurrence in a low malaria transmission setting along the Thai-Myanmar border. Malar J. 2010;9:143.CrossRefPubMedPubMedCentral
19.
go back to reference Ghebreyesus TA, Haile M, Witten KH, Getachew A, Yohannes M, Lindsay SW, et al. Household risk factors for malaria among children in the Ethiopian highlands. Trans R Soc Trop Med Hyg. 2000;94:17–21.CrossRefPubMed Ghebreyesus TA, Haile M, Witten KH, Getachew A, Yohannes M, Lindsay SW, et al. Household risk factors for malaria among children in the Ethiopian highlands. Trans R Soc Trop Med Hyg. 2000;94:17–21.CrossRefPubMed
20.
go back to reference Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9(1):e1001165.CrossRefPubMedPubMedCentral Bousema T, Griffin JT, Sauerwein RW, Smith DL, Churcher TS, Takken W, et al. Hitting hotspots: spatial targeting of malaria for control and elimination. PLoS Med. 2012;9(1):e1001165.CrossRefPubMedPubMedCentral
21.
go back to reference Lalah JO, Muendo BM, Getenga ZM. The dissipation of hexazinone in tropical soils under semi-controlled field conditions in Kenya. J Environ Sci Health. 2009;44:690–6.CrossRef Lalah JO, Muendo BM, Getenga ZM. The dissipation of hexazinone in tropical soils under semi-controlled field conditions in Kenya. J Environ Sci Health. 2009;44:690–6.CrossRef
22.
go back to reference Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G. Plasmodium falciparum spatial analysis, Western Kenya highlands. Emerg Infect Dis. 2005;11:1571–7.CrossRefPubMedPubMedCentral Munyekenye OG, Githeko AK, Zhou G, Mushinzimana E, Minakawa N, Yan G. Plasmodium falciparum spatial analysis, Western Kenya highlands. Emerg Infect Dis. 2005;11:1571–7.CrossRefPubMedPubMedCentral
23.
go back to reference Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.CrossRefPubMedPubMedCentral Ototo EN, Mbugi JP, Wanjala CL, Zhou G, Githeko AK, Yan G. Surveillance of malaria vector population density and biting behaviour in western Kenya. Malar J. 2015;14:244.CrossRefPubMedPubMedCentral
24.
go back to reference WHO. Manual on practical entomology in malaria: methods and techniques part II. Geneva: World Health Organization; 1975. WHO. Manual on practical entomology in malaria: methods and techniques part II. Geneva: World Health Organization; 1975.
25.
go back to reference Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). South Afr Instit Med Res. 1968;54:1–343. Gillies MT, De Meillon B. The Anophelinae of Africa south of the Sahara (Ethiopian zoogeographical region). South Afr Instit Med Res. 1968;54:1–343.
26.
go back to reference Detinova T. Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. WHO Monograph Series. 1962;47:13–191.PubMed Detinova T. Age-grouping methods in Diptera of medical importance with special reference to some vectors of malaria. WHO Monograph Series. 1962;47:13–191.PubMed
27.
go back to reference Apinjoh T, Mbunwe E, Yafi C, Besingi R, Awah N, Anchang-Kimbi J, et al. Febrile status, malaria parasitaemia and gastrointestinal helminthiasis in school children resident at different altitudes. Trop Med Int Health. 2007;12:165. Apinjoh T, Mbunwe E, Yafi C, Besingi R, Awah N, Anchang-Kimbi J, et al. Febrile status, malaria parasitaemia and gastrointestinal helminthiasis in school children resident at different altitudes. Trop Med Int Health. 2007;12:165.
28.
go back to reference WHO. Basic malaria microscopy. 2nd ed. Geneva: World Health Organization; 2010. WHO. Basic malaria microscopy. 2nd ed. Geneva: World Health Organization; 2010.
29.
go back to reference Kain KC, Lanar DE. Determination of genetic variation within Plasmodium falciparum by using enzymatically amplified DNA from filter paper disks impregnated with whole blood. J Clin Microbiol. 1991;29:1171–4.PubMedPubMedCentral Kain KC, Lanar DE. Determination of genetic variation within Plasmodium falciparum by using enzymatically amplified DNA from filter paper disks impregnated with whole blood. J Clin Microbiol. 1991;29:1171–4.PubMedPubMedCentral
30.
go back to reference Mharakurwa S, Simoloka C, Thuma PE, Shiff CJ, Sullivan DJ. PCR detection of Plasmodium falciparum in human urine and saliva samples. Malar J. 2006;5:103.CrossRefPubMedPubMedCentral Mharakurwa S, Simoloka C, Thuma PE, Shiff CJ, Sullivan DJ. PCR detection of Plasmodium falciparum in human urine and saliva samples. Malar J. 2006;5:103.CrossRefPubMedPubMedCentral
31.
go back to reference Rougemont M, Van SM, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004;42:5636–43.CrossRefPubMedPubMedCentral Rougemont M, Van SM, Sahli R, Hinrikson HP, Bille J, Jaton K. Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004;42:5636–43.CrossRefPubMedPubMedCentral
32.
go back to reference Wirtz RA, Burkot TR, Graves PM, Andre RG. Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol. 1987;24:433–7.CrossRefPubMed Wirtz RA, Burkot TR, Graves PM, Andre RG. Field evaluation of enzyme-linked immunosorbent assays for Plasmodium falciparum and Plasmodium vivax sporozoites in mosquitoes (Diptera: Culicidae) from Papua New Guinea. J Med Entomol. 1987;24:433–7.CrossRefPubMed
33.
go back to reference WHO. Malaria entomology and vector control: learners guide. Trial edition HIV/AIDS, tuberculosis and malaria, roll back malaria. Geneva: World Health Organization; 2003. WHO. Malaria entomology and vector control: learners guide. Trial edition HIV/AIDS, tuberculosis and malaria, roll back malaria. Geneva: World Health Organization; 2003.
34.
go back to reference Smith JL, Auala J, Tambo M, Haindongo E, Katokele S, Uusiku P, et al. Spatial clustering of patent and sub-patent malaria infections in Northern Namibia: implications for surveillance and response strategies for elimination. PLoS ONE. 2017;12(8):e0180845.CrossRefPubMedPubMedCentral Smith JL, Auala J, Tambo M, Haindongo E, Katokele S, Uusiku P, et al. Spatial clustering of patent and sub-patent malaria infections in Northern Namibia: implications for surveillance and response strategies for elimination. PLoS ONE. 2017;12(8):e0180845.CrossRefPubMedPubMedCentral
35.
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
36.
go back to reference Ouedraogo AL, Goncalves BP, Gneme A, Wenger EA, Guelbeogo MW, Ouedraogo A, et al. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis. 2016;213:90–9.CrossRefPubMed Ouedraogo AL, Goncalves BP, Gneme A, Wenger EA, Guelbeogo MW, Ouedraogo A, et al. Dynamics of the human infectious reservoir for malaria determined by mosquito feeding assays and ultrasensitive malaria diagnosis in Burkina Faso. J Infect Dis. 2016;213:90–9.CrossRefPubMed
37.
go back to reference 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.PubMed 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.PubMed
38.
go back to reference Bousema JT, Gouagna LC, Drakeley CJ, Meutsetege AM, Okech BA, Akim IN, et al. Plasmodium falciparum gametocyte carriage in asymptomatic children in Western Kenya. Malar J. 2004;3:18.CrossRefPubMedPubMedCentral Bousema JT, Gouagna LC, Drakeley CJ, Meutsetege AM, Okech BA, Akim IN, et al. Plasmodium falciparum gametocyte carriage in asymptomatic children in Western Kenya. Malar J. 2004;3:18.CrossRefPubMedPubMedCentral
39.
go back to reference Bousema T, Stresman G, Baidjoe AY, Bradley J, Knight P, Stone W, et al. The impact of hotspot-targeted interventions on malaria transmission in Rachuonyo South District in the Western Kenyan highlands: a cluster-randomized controlled trial. PLoS Med. 2016;13(4):e1001993.CrossRefPubMedPubMedCentral Bousema T, Stresman G, Baidjoe AY, Bradley J, Knight P, Stone W, et al. The impact of hotspot-targeted interventions on malaria transmission in Rachuonyo South District in the Western Kenyan highlands: a cluster-randomized controlled trial. PLoS Med. 2016;13(4):e1001993.CrossRefPubMedPubMedCentral
40.
go back to reference Degefa T, Yewhalaw D, Zhou G, Lee MC, Atieli H, Githeko AK, et al. Indoor and outdoor malaria vector surveillance in western Kenya: implications for better understanding of residual transmission. Malar J. 2017;16:443.CrossRefPubMedPubMedCentral Degefa T, Yewhalaw D, Zhou G, Lee MC, Atieli H, Githeko AK, et al. Indoor and outdoor malaria vector surveillance in western Kenya: implications for better understanding of residual transmission. Malar J. 2017;16:443.CrossRefPubMedPubMedCentral
41.
go back to reference Killeen GF. Chitnis N Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis. Malar J. 2014;13:97.CrossRefPubMedPubMedCentral Killeen GF. Chitnis N Potential causes and consequences of behavioural resilience and resistance in malaria vector populations: a mathematical modelling analysis. Malar J. 2014;13:97.CrossRefPubMedPubMedCentral
Metadata
Title
Reactive case detection of Plasmodium falciparum in western Kenya highlands: effective in identifying additional cases, yet limited effect on transmission
Authors
Ebenezer K. Aidoo
Yaw A. Afrane
Maxwell Gesuge Machani
Winnie Chebore
Bernard Walter Lawson
Harrysone Atieli
Simon Kariuki
Ming-Chieh Lee
Cristian Koepfli
Guofa Zhou
Andrew K. Githeko
Guiyun Yan
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/s12936-018-2260-2

Other articles of this Issue 1/2018

Malaria Journal 1/2018 Go to the issue