Estimation of Malaria-Attributable Fever in Malaria Test–Positive Febrile Outpatients in Three Provinces of Mozambique, 2018

Mateusz M. Plucinski Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
United States President’s Malaria Initiative, Centers for Disease Control and Prevention, Atlanta, Georgia;

Search for other papers by Mateusz M. Plucinski in
Current site
Google Scholar
PubMed
Close
,
Baltazar Candrinho National Malaria Control Program, Ministry of Health, Maputo, Mozambique;

Search for other papers by Baltazar Candrinho in
Current site
Google Scholar
PubMed
Close
,
Mercia Dimene National Malaria Control Program, Ministry of Health, Maputo, Mozambique;

Search for other papers by Mercia Dimene in
Current site
Google Scholar
PubMed
Close
,
Tom Smith Swiss Tropical and Public Health Institute, Basel, Switzerland;
University of Basel, Basel, Switzerland;

Search for other papers by Tom Smith in
Current site
Google Scholar
PubMed
Close
,
Julie Thwing Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;

Search for other papers by Julie Thwing in
Current site
Google Scholar
PubMed
Close
,
James Colborn Clinton Health Access Initiative, Maputo, Mozambique;

Search for other papers by James Colborn in
Current site
Google Scholar
PubMed
Close
,
Eric Rogier Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;

Search for other papers by Eric Rogier in
Current site
Google Scholar
PubMed
Close
, and
Rose Zulliger Malaria Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia;
United States President’s Malaria Initiative, Centers for Disease Control and Prevention, Maputo, Mozambique

Search for other papers by Rose Zulliger in
Current site
Google Scholar
PubMed
Close
Restricted access

Like most malaria-endemic countries, Mozambique relies on tabulation of confirmed malaria test–positive febrile patients to track incidence of malaria. However, this approach is potentially biased by incidental malaria parasitemia in patients with fever of another etiology. We compared pan-Plasmodium aldolase and lactate dehydrogenase and Plasmodium falciparum histidine-rich protein 2 (PfHRP2) antigen concentrations measured using a laboratory bead-based assay of samples collected from 1,712 febrile and afebrile patients of all ages in Maputo, Zambézia, and Cabo Delgado provinces. We used a Bayesian latent class model to estimate the proportion of malaria-attributable fevers in malaria test–positive febrile patients. Depending on the antigen, estimated rates of malaria-attributable fever in malaria test–positive febrile patients were 100% in Maputo, 33–58% in Zambézia, and 63–74% in Cabo Delgado. Our findings indicate that most malaria test–positive febrile patients in the three provinces of Mozambique had a fever that was likely caused by the concurrent malaria infection. Counting malaria test–positive febrile patients for estimation of malaria incidence appears to be appropriate in this setting.

    • Supplemental Materials (PDF 930 KB)

Author Notes

Address correspondence to Mateusz M. Plucinski, Centers for Disease Control and Prevention, Malaria Branch, 1600 Clifton Rd., Atlanta, GA 30329. E-mail: mplucinski@cdc.gov

Authors’ addresses: Mateusz M. Plucinski, Julie Thwing, Eric Rogier, and Rose Zulliger, Malaria Branch, Division of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: mplucinski@cdc.gov, jthwing@cdc.gov, erogier@cdc.gov, and ymr0@cdc.gov. Baltazar Candrinho and Mercia Dimene, National Malaria Control Program, Ministry of Health, Maputo, Mozambique, E-mails: candrinhobaltazar@gmail.com and merciad40@yahoo.com.br. Tom Smith, Swiss Tropical and Public Health Institute, Basel, Switzerland, E-mail: thomas-a.smith@unibas.ch. James Colborn, Clinton Health Access Initiative, Maputo, Mozambique, E-mail: jcolborn.ic@clintonhealthaccess.org.

  • 1.

    Ministério da Saúde–MISAU, Instituto Nacional de Estatística–INE, ICF, 2018. Inquérito de Indicadores de Imunização, Malária e HIV/SIDA em Moçambique–IMASIDA, 2015. Maputo, Moçambique: MISAU/Moçambique, INE, and ICF.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    MISAU, 2017. Normas de Tratamento de Malária em Moçambique. Maputo, Moçambique: DNSP.

  • 3.

    Smith T, Schellenberg JA, Hayes R, 1994. Attributable fraction estimates and case definitions for malaria in endemic areas. Stat Med 13: 23452358.

  • 4.

    World Health Organization, 2019. World Malaria Report 2018. Geneva, Switzerland: WHO.

  • 5.

    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.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Vounatsou P, Smith T, Smith A, 1998. Bayesian analysis of two‐component mixture distributions applied to estimating malaria attributable fractions. J R Stat Soc Ser C 47: 575587.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Plucinski MM, Rogier E, Dimbu R, 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: e01901e01918.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Candrinho B et al. 2019. Quality of malaria services offered in public health facilities in three provinces of Mozambique: a cross-sectional study. Malaria J 18: 162.

  • 9.

    Plucinski MM, Candrinho B, Dimene M, Colborn J, Lu A, Nace D, Zulliger R, Rogier E, 2019. Assessing performance of HRP2 antigen detection for malaria diagnosis in Mozambique. J Clin Microbiol 57: e0087519.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    MISAU, INE, 2016. Inquérito de Indicadores de Imunização, Malária e HIV/SIDA em Moçambique (IMASIDA) 2015: Relatório de Indicadores Básicos. Maputo, Moçambique: INE.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Plucinski MM et al. 2018. Screening for pfhrp2/3-deleted Plasmodium falciparum, non-falciparum, and low-density malaria infections by a multiplex antigen assay. J Infect Dis 219: 437447.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Rogier E et al. 2017. Bead based immunoassay allows sub-picogram detection of histidine-rich protein 2 from Plasmodium falciparum and estimates reliability of malaria rapid diagnostic tests. PLoS One 12: e0172139.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Spiegelhalter D, Thomas A, Best N, Lunn D, 2003. WinBUGS Version 1.4. 2003. Robinson Way, Cambridge: MRC Biostatistics Unit, Institute of Public Health.

  • 14.

    World Health Organization, 2016. Malaria Rapid Diagnostic Test Performance: Results of WHO Product Testing of Malaria RDTs: Round 7 (2015–2016). Geneva, Switzerland: WHO.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Barnwell J, 2009. Implications of Parasite Density Thresholds for Product Testing, Lot-Testing and Positive Control Wells. Geneva, Switzerland: WHO, 3941.

  • 16.

    Plucinski MM, McElroy PD, Dimbu PR, Fortes F, Nace D, Halsey ES, Rogier E, 2019. Clearance dynamics of lactate dehydrogenase and aldolase following antimalarial treatment for Plasmodium falciparum infection. Parasit Vectors 12: 293.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Bisoffi Z, Sirima SB, Menten J, Pattaro C, Angheben A, Gobbi F, Tinto H, Lodesani C, Neya B, Gobbo M, 2010. Accuracy of a rapid diagnostic test on the diagnosis of malaria infection and of malaria-attributable fever during low and high transmission season in Burkina Faso. Malaria J 9: 192.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Dicko A, Mantel C, Kouriba B, Sagara I, Thera MA, Doumbia S, Diallo M, Poudiougou B, Diakite M, Doumbo OK, 2005. Season, fever prevalence and pyrogenic threshold for malaria disease definition in an endemic area of Mali. Trop Med Int Health 10: 550556.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Rogier C, Commenges D, Trape J-F, 1996. Evidence for an age-dependent pyrogenic threshold of Plasmodium falciparum parasitemia in highly endemic populations. Am J Trop Med Hyg 54: 613619.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Mutanda AL, Cheruiyot P, Hodges JS, Ayodo G, Odero W, John CC, 2014. Sensitivity of fever for diagnosis of clinical malaria in a Kenyan area of unstable, low malaria transmission. Malar J 13: 163.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 157 152 11
Full Text Views 907 19 2
PDF Downloads 282 13 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save