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Olotu A, Fegan G, Williams TN, Sasi P, Ogada E, Bauni E, Wambua J, Marsh K, Borrmann S, Bejon P, 2010. Defining clinical malaria: the specificity and incidence of endpoints from active and passive surveillance of children in rural Kenya. PLoS One 5: e15569.
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Esemu LF et al. 2019. Case definitions of clinical malaria in children from three health districts in the north region of Cameroon. Biomed Res Int 2019: 9709013. doi: 10.1155/2019/9709013.
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17.
Plucinski MM, Candrinho B, Dimene M, Smith T, Thwing J, Colborn J, Rogier E, Zulliger R, 2020. Estimation of malaria-attributable fever in malaria test-positive febrile outpatients in three provinces of Mozambique, 2018. Am J Trop Med Hyg 102: 151–155.
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Boisier P, Jambou R, Raharimalala L, Roux J, 2002. Relationship between parasite density and fever risk in a community exposed to a low level of malaria transmission in Madagascar highlands. Am J Trop Med Hyg 67: 137–140.
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19.
Afrane YA, Zhou G, Githeko AK, Yan G, 2014. Clinical malaria case definition and malaria attributable fraction in the highlands of western Kenya. Malar J 13: 405.
-
20.
Plucinski MM, Rogier E, Dimbu PR, Fortes F, Halsey ES, Aidoo M, Smith T, 2019. Performance of antigen concentration thresholds for attributing fever to malaria among outpatients in Angola. J Clin Microbiol 57: e01901–18.
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Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ, 2012. Entomological indices of malaria transmission in Chikhwawa district, southern Malawi. Malar J 11: 380.
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Mathanga DP, Tembo AK, Mzilahowa T, Bauleni A, Mtimaukenena K, Taylor TE, Valim C, Walker ED, Wilson ML, 2016. Patterns and determinants of malaria risk in urban and peri-urban areas of Blantyre, Malawi. Malar J 15: 590.
-
23.
Chirombo J, Ceccato P, Lowe R, Terlouw DJ, Thomson MC, Gumbo A, Diggle PJ, Read JM, 2020. Childhood malaria case incidence in Malawi between 2004 and 2017: spatio-temporal modelling of climate and non-climate factors. Malar J 19: 5.
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Kapito-Tembo A, Mathanga D, Bauleni A, Pensulo P, Ali D, Valim C, Taylor TE, Laufer MK, 2020. Prevalence and clinical management of mon-malarial febrile illnesses among outpatients in the era of universal malaria testing in Malawi. Am J Trop Med Hyg 103: 887–893.
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Djallé D, Gody JC, Moyen JM, Tekpa G, Ipero J, Madji N, Breurec S, Manirakiza A, 2014. Performance of Paracheck™-Pf, SD Bioline malaria Ag-Pf and SD Bioline malaria Ag-Pf/pan for diagnosis of falciparum malaria in the Central African Republic. BMC Infect Dis 14: 109.
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Overdiagnosis of Malaria Illness in an Endemic Setting: A Facility-Based Surveillance Study in Malawi
Ingrid Peterson
Ingrid Peterson
Center for Vaccine Development and Global Health, University of Maryland Baltimore, Baltimore, Maryland;
Blantyre Malaria Project, College of Medicine, University of Malawi, Blantyre, Malawi;
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Blantyre Malaria Project, College of Medicine, University of Malawi, Blantyre, Malawi;
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Atupele Kapito-Tembo
Atupele Kapito-Tembo
Malaria Alert Center, College of Medicine, University of Malawi, Blantyre, Malawi;
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Andrew Bauleni
Andrew Bauleni
Malaria Alert Center, College of Medicine, University of Malawi, Blantyre, Malawi;
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Osward Nyirenda
Osward Nyirenda
Blantyre Malaria Project, College of Medicine, University of Malawi, Blantyre, Malawi;
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Paul Pensulo
Paul Pensulo
Blantyre Malaria Project, College of Medicine, University of Malawi, Blantyre, Malawi;
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William Still
William Still
Center for Vaccine Development and Global Health, University of Maryland Baltimore, Baltimore, Maryland;
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Clarissa Valim
Clarissa Valim
Department of Global Health, Boston University School of Public Health, Boston, Massachusetts;
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Lauren Cohee
Lauren Cohee
Center for Vaccine Development and Global Health, University of Maryland Baltimore, Baltimore, Maryland;
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Terrie Taylor
Terrie Taylor
Department of Osteopathic Medical Specialties, College of Osteopathic Medicine, Michigan State University, East Lansing, Michigan
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Don P. Mathanga
Don P. Mathanga
Malaria Alert Center, College of Medicine, University of Malawi, Blantyre, Malawi;
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Miriam K. Laufer
Miriam K. Laufer
Center for Vaccine Development and Global Health, University of Maryland Baltimore, Baltimore, Maryland;
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Abstract.
In endemic settings where asymptomatic malaria infections are common, malaria infection can complicate fever diagnosis. Factors influencing fever misdiagnosis, including accuracy of malaria rapid diagnostic tests (mRDTs) and the malaria-attributable fraction of fevers (MAF), require further investigation. We conducted facility-based surveillance in Malawi, from January 2012 through December 2013 in settings of high perennial (Chikhwawa), high seasonal (Thoylo), and moderate seasonal (Ndirande) malaria transmission. Consecutive patients presenting to outpatient departments were screened; those with suspected malaria illness were tested by mRDT or routine thick-smear microscopy. Test positivity rates (TPRs), positive predictive value (PPVs) of mRDTs, and MAFs were calculated by site, age, and season. Of 41,471 patients, 10,052 (24.2%) tested positive for malaria. The TPR was significantly greater in Chikhwawa (29.9%; 95% CI, 28.6–30.0) compared with Thyolo (13.2%; 95% CI, 12.5–13.7) and Ndirande (13.1%; 95% CI, 12.2–14.4). The overall PPV was 77.8% (95% CI, 76.8–78.7); it was lowest among infants (69.9%; 95% CI, 65.5–74.2) and highest among school-age children (81.9%; 95% CI, 80.3–83.4). Malaria infection accounted for about 50% of fevers in children younger than 5 years old with microscopy-confirmed Plasmodium falciparum infection, and less than 20% of such fevers in school-age children. Outpatient settings in Malawi had a high burden of malaria illness, but also possible overdiagnosis of malaria illness. Interventions to reduce malaria transmission and rapid testing for other common febrile illness may improve diagnostic clarity among outpatients in malaria endemic settings.
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Author Notes
Financial support: This work was supported by the NIH–National Institute of Allergy and Infectious Diseases (U19AI089683 and K24AI114996). We acknowledge the support of the University of Maryland Baltimore Institute for Clinical and Translational Research.
Authors’ addresses: Ingrid Peterson, Center for Vaccine Development and Global Health, University of Maryland Baltimore, Baltimore, MD, and Blantyre Malaria Project, College of Medicine, University of Malawi, Blantyre, Malawi, E-mail: idpet2@gmail.com. Atupele Kapito-Tembo, Andrew Bauleni, and Don P. Mathanga, Malaria Alert Center, College of Medicine, University of Malawi, Blantyre, Malawi, E-mails: atupelekapito@gmail.com, abauleni@mac.medcol.mw, and dmathang@mac.medcol.mw. Osward Nyirenda and Paul Pensulo, Blantyre Malaria Project, College of Medicine, University of Malawi, Blantyre, Malawi, E-mails: omnyirenda@gmail.com and paulpensulo@gmail.com. William Still, Lauren Cohee, and Miriam K. Laufer, Center for Vaccine Development and Global Health, University of Maryland Baltimore, Baltimore, MD, E-mails: wstill@umaryland.edu, lcohee@som.umaryland.edu, and mlaufer@som.umaryland.edu. Clarissa Valim, Department of Global Health, Boston University School of Public Health, Boston, MA, E-mail: clariss.valim@gmail.com. Terrie Taylor, Department of Osteopathic Medical Specialties, College of Osteopathic Medicine, Michigan State University, East Lansing, MI, E-mail: ttmalawi@msu.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Waitumbi JN, Kuypers J, Anyona SB, Koros JN, Polhemus ME, Gerlach J, Steele M, Englund JA, Neuzil KM, Domingo GJ, 2010. Outpatient upper respiratory tract viral infections in children with malaria symptoms in western Kenya. Am J Trop Med Hyg 83: 1010–1013.
-
2.
Dalrymple U et al. 2019. The contribution of non-malarial febrile illness co-infections to Plasmodium falciparum case counts in health facilities in Sub-Saharan Africa. Malar J 18: 195.
-
3.
Abeku TA, Kristan M, Jones C, Beard J, Mueller DH, Okia M, Rapuoda B, Greenwood B, Cox J, 2008. Determinants of the accuracy of rapid diagnostic tests in malaria case management: evidence from low and moderate transmission settings in the East African highlands. Malar J 7: 202.
-
4.
Mahende C, Ngasala B, Lusingu J, Yong TS, Lushino P, Lemnge M, Mmbando B, Premji Z, 2016. Performance of rapid diagnostic test, blood-film microscopy and PCR for the diagnosis of malaria infection among febrile children from Korogwe District, Tanzania. Malar J 15: 391.
-
5.
Mbabazi P, Hopkins H, Osilo E, Kalungu M, Byakika-Kibwika P, Kamya MR, 2015. Accuracy of two malaria rapid diagnostic tests (RDTs) for initial diagnosis and treatment monitoring in a high transmission setting in Uganda. Am J Trop Med Hyg 92: 530–536.
-
6.
Ranadive N et al. 2017. Limitations of rapid diagnostic testing in patients with suspected malaria: a diagnostic accuracy evaluation from Swaziland, a low-endemicity country aiming for malaria elimination. Clin Infect Dis 64: 1221–1227.
-
7.
Wongsrichanalai C, Barcus MJ, Muth S, Sutamihardja A, Wernsdorfer WH, 2007. A review of malaria diagnostic tools: microscopy and rapid diagnostic test (RDT). Am J Trop Med Hyg 77: 119–127.
-
8.
Dalrymple U, Arambepola R, Gething PW, Cameron E, 2018. How long do rapid diagnostic tests remain positive after anti-malarial treatment? Malar J 17: 228.
-
9.
Tran TM et al. 2013. An intensive longitudinal cohort study of Malian children and adults reveals no evidence of acquired immunity to Plasmodium falciparum infection. Clin Infect Dis 57: 40–47.
-
10.
Ndong IC, Okyere D, Enos JY, Mensah BA, Nyarko A, Abuaku B, Amambua-Ngwa A, Merle CSC, Koram KA, Ahorlu CS, 2019. Prevalence of asymptomatic malaria parasitaemia following mass testing and treatment in Pakro sub-district of Ghana. BMC Public Health 19: 1622.
-
11.
Walldorf JA et al. 2015. School-age children are a reservoir of malaria infection in Malawi. PLoS One 10: e0134061.
-
12.
Baliraine FN, Afrane YA, Amenya DA, Bonizzoni M, Menge DM, Zhou G, Zhong D, Vardo-Zalik AM, Githeko AK, Yan G, 2009. High prevalence of asymptomatic Plasmodium falciparum infections in a highland area of western Kenya: a cohort study. J Infect Dis 200: 66–74.
-
13.
Smith T, Schellenberg JA, Hayes R, 1994. Attributable fraction estimates and case definitions for malaria in endemic areas. Stat Med 13: 2345–2358.
-
14.
McGuinness D, Koram K, Bennett S, Wagner G, Nkrumah F, Riley E, 1998. Clinical case definitions for malaria: clinical malaria associated with very low parasite densities in African infants. Trans R Soc Trop Med Hyg 92: 527–531.
-
15.
Olotu A, Fegan G, Williams TN, Sasi P, Ogada E, Bauni E, Wambua J, Marsh K, Borrmann S, Bejon P, 2010. Defining clinical malaria: the specificity and incidence of endpoints from active and passive surveillance of children in rural Kenya. PLoS One 5: e15569.
-
16.
Esemu LF et al. 2019. Case definitions of clinical malaria in children from three health districts in the north region of Cameroon. Biomed Res Int 2019: 9709013. doi: 10.1155/2019/9709013.
-
17.
Plucinski MM, Candrinho B, Dimene M, Smith T, Thwing J, Colborn J, Rogier E, Zulliger R, 2020. Estimation of malaria-attributable fever in malaria test-positive febrile outpatients in three provinces of Mozambique, 2018. Am J Trop Med Hyg 102: 151–155.
-
18.
Boisier P, Jambou R, Raharimalala L, Roux J, 2002. Relationship between parasite density and fever risk in a community exposed to a low level of malaria transmission in Madagascar highlands. Am J Trop Med Hyg 67: 137–140.
-
19.
Afrane YA, Zhou G, Githeko AK, Yan G, 2014. Clinical malaria case definition and malaria attributable fraction in the highlands of western Kenya. Malar J 13: 405.
-
20.
Plucinski MM, Rogier E, Dimbu PR, Fortes F, Halsey ES, Aidoo M, Smith T, 2019. Performance of antigen concentration thresholds for attributing fever to malaria among outpatients in Angola. J Clin Microbiol 57: e01901–18.
-
21.
Mzilahowa T, Hastings IM, Molyneux ME, McCall PJ, 2012. Entomological indices of malaria transmission in Chikhwawa district, southern Malawi. Malar J 11: 380.
-
22.
Mathanga DP, Tembo AK, Mzilahowa T, Bauleni A, Mtimaukenena K, Taylor TE, Valim C, Walker ED, Wilson ML, 2016. Patterns and determinants of malaria risk in urban and peri-urban areas of Blantyre, Malawi. Malar J 15: 590.
-
23.
Chirombo J, Ceccato P, Lowe R, Terlouw DJ, Thomson MC, Gumbo A, Diggle PJ, Read JM, 2020. Childhood malaria case incidence in Malawi between 2004 and 2017: spatio-temporal modelling of climate and non-climate factors. Malar J 19: 5.
-
24.
Severe Malaria Observatory, n.d. Malaria Prevalence, Cases, Map, Treatment, Risk and Deaths in Malawi. Available at: https://www.severemalaria.org/countries/malawi. Accessed January 15, 2021.
-
25.
Kapito-Tembo A, Mathanga D, Bauleni A, Pensulo P, Ali D, Valim C, Taylor TE, Laufer MK, 2020. Prevalence and clinical management of mon-malarial febrile illnesses among outpatients in the era of universal malaria testing in Malawi. Am J Trop Med Hyg 103: 887–893.
-
26.
Djallé D, Gody JC, Moyen JM, Tekpa G, Ipero J, Madji N, Breurec S, Manirakiza A, 2014. Performance of Paracheck™-Pf, SD Bioline malaria Ag-Pf and SD Bioline malaria Ag-Pf/pan for diagnosis of falciparum malaria in the Central African Republic. BMC Infect Dis 14: 109.
-
27.
Chinkhumba J, Skarbinski J, Chilima B, Campbell C, Ewing V, San Joaquin M, Sande J, Ali D, Mathanga D, 2010. Comparative field performance and adherence to test results of four malaria rapid diagnostic tests among febrile patients more than five years of age in Blantyre, Malawi. Malar J 9: 209.
-
28.
Herson J, 2009. Statistical issues. Herson J, ed. Data and Safety Monitoring Committees in Clinical Trials. Boca Raton, FL: CRC Press, 67–68.
-
29.
Quakyi IA et al. 2018. Diagnostic capacity, and predictive values of rapid diagnostic tests for accurate diagnosis of Plasmodium falciparum in febrile children in Asante-Akim, Ghana. Malar J 17: 468.
-
30.
Hofmann NE et al. 2019. Diagnostic performance of conventional and ultrasensitive rapid diagnostic tests for malaria in febrile outpatients in Tanzania. J Infect Dis 219: 1490–1498.
-
31.
Osei-Yeboah J, Kwame Norgbe G, Yao Lokpo S, Khadijah Kinansua M, Nettey L, Allotey EA, 2016. Comparative performance evaluation of routine malaria diagnosis at Ho Municipal Hospital. J Parasitol Res 2016: 5837890.
-
32.
Huong NM, Davis TM, Hewitt S, Huong NV, Uyen TT, Nhan DH, le Cong D, 2002. Comparison of three antigen detection methods for diagnosis and therapeutic monitoring of malaria: a field study from southern Vietnam. Trop Med Int Health 7: 304–308.
-
33.
Mwesigwa J et al. 2019. Field performance of the malaria highly sensitive rapid diagnostic test in a setting of varying malaria transmission. Malar J 18: 288.
-
34.
Hopkins H, Bebell L, Kambale W, Dokomajilar C, Rosenthal PJ, Dorsey G, 2008. Rapid diagnostic tests for malaria at sites of varying transmission intensity in Uganda. J Infect Dis 197: 510–518.
-
35.
Mabunda S, Aponte JJ, Tiago A, Alonso P, 2009. A country-wide malaria survey in Mozambique: II. Malaria attributable proportion of fever and establishment of malaria case definition in children across different epidemiological settings. Malar J 8: 74.
-
36.
Smith T, Charlwood JD, Kitua AY, Masanja H, Mwankusye S, Alonso PL, Tanner M, 1998. Relationships of malaria morbidity with exposure to Plasmodium falciparum in young children in a highly endemic area. Am J Trop Med Hyg 59: 252–257.
-
37.
Baird JK, Jones TR, Danudirgo EW, Annis BA, Bangs MJ, Basri H, Purnomo, Masbar S, 1991. Age-dependent acquired protection against Plasmodium falciparum in people having two years exposure to hyperendemic malaria. Am J Trop Med Hyg 45: 65–76.
-
38.
Rogier C, Commenges D, Trape JF, 1996. Evidence for an age-dependent pyrogenic threshold of Plasmodium falciparum parasitemia in highly endemic populations. Am J Trop Med Hyg 54: 613–619.
-
39.
Peterson I et al. 2016. Respiratory virus-associated severe acute respiratory illness and viral clustering in Malawian children in a setting with a high prevalence of HIV infection, malaria, and malnutrition. J Infect Dis 214: 1700–1711.
-
40.
Waitumbi JN, Kuypers J, Anyona SB, Koros JN, Polhemus ME, Gerlach J, Steele M, Englund JA, Neuzil KM, Domingo GJ, 2010. Outpatient upper respiratory tract viral infections in children with malaria symptoms in western Kenya. Am J Trop Med Hyg 83: 1010–1013.
-
41.
Thompson MG et al. 2012. Influenza and malaria coinfection among young children in western Kenya, 2009–2011. J Infect Dis 206: 1674–1684.
-
42.
Worges M, Celone M, Finn T, Chisha Z, Winters A, Winters B, Keating J, Yukich JO, 2019. Malaria case management in Zambia: a cross-sectional health facility survey. Acta Trop 195: 83–89.
-
43.
Derua YA, Ishengoma DR, Rwegoshora RT, Tenu F, Massaga JJ, Mboera LE, Magesa SM, 2011. Users’ and health service providers’ perception on quality of laboratory malaria diagnosis in Tanzania. Malar J 10: 78.
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