Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 11, Number 9—September 2005
Research

Malaria Attributable to the HIV-1 Epidemic, Sub-Saharan Africa

Eline L. Korenromp*†Comments to Author , Brian G. Williams*, Sake J. de Vlas†, Eleanor Gouws‡, Charles F. Gilks*, Peter D. Ghys‡, and Bernard L. Nahlen*
Author affiliations: *World Health Organization, Geneva, Switzerland; †Erasmus University Medical Center, Rotterdam, the Netherlands; ‡Joint United Nations Programme on HIV/AIDS, Geneva, Switzerland

Main Article

Table 3

Univariate sensitivity analyses of HIV-1 impact on malaria incidence and deaths, sub-Saharan Africa, 2004*

Scenario % increase in malaria incidence due to HIV (minimum and maximum)† % increase in malaria deaths due to HIV (minimum and maximum)†
Default scenario: see Tables 1 and 2. 1.3 (0.20–28)† 4.9 (0.65–114)†
Weaker effect of HIV-1 on malaria incidence: RR = 1.0 at CD4 >500/μL, RR = 2.0 at CD4 200–499/μL, and RR = 4.0 at CD4 <200/μL. 0.8 (0.11–16) 4.4 (0.60–90)
Stronger effect of HIV-1 on malaria incidence: RR = 1.5 at CD4 >500/μL, RR = 4.0 at CD4 200–499/μL, and RR = 8.0 at CD4 <200/μL. 2.2 (0.33–47) 5.7 (0.73–153)
Weaker effect of HIV-1 on malaria mortality (all groups): RR = 1.5 at CD4 >500/μL, RR = 2.0 at CD4 200–499/μL, and RR = 4.0 at CD4 <200/μL. n.a. 2.4 (0.30–59)‡
Weaker effect of HIV-1 on mortality in children <5 y in areas of high malaria transmission specifically, analogous to the comparatively weak effect of HIV-1 on incidence in this group: RR = 1.5 at CD4 >500/μL, RR = 2.0 at CD4 200–499/μL, and RR = 5.0 at CD4 <200/μL. n.a. 3.7 (0.45–114)
Stronger effect of HIV-1 on malaria mortality (all groups): RR = 3.0 at CD4 >500/μL, RR = 6.0 at CD4 200–499/μL, RR = 12.0 at CD4 <200/μL. n.a. 6.9 (0.92–157)§
Stronger decrease with age in malaria incidence: RRs compared to <5 y of 0.30 for 5–14y and 0.05 for >15 y in high malaria transmission areas, and 0.60 for 5–14 y and 0.10 for >15 y for areas of low and unstable malaria transmission including southern African countries. 1.0 (0.13–15) 4.0 (0.45– 59)
No decrease with age in malaria incidence at any malaria transmission intensity. 4.4 (0.54–37) 12.5 (1.5–153)
Stronger decrease with age in malaria CFR: 1.2% in <5 y at all malaria transmission intensities, 0.8% in >5 y at low and unstable transmission, 0.15% in >5 y at high transmission. n.a. 4.0 (0.53–107)
No decrease with age in malaria CFR at any transmission intensity. n.a. 5.7 (0.77–114)
HIV-1 increases malaria incidence also in children <5 y in areas of high malaria transmission. 2.0 (0.26–28) 5.9 (0.78–114)
CD4 count decline during HIV-1 infection: 1,000–100/μL¶ 1.0 (0.15–21) 3.7 (0.50–82)
CD4 count decline during HIV-1 infection: 700–0/μL# 1.7 (0.24–35) 6.2 (0.81–151)
No urban/rural difference in the malaria incidence rate 1.4 (0.20–28) 5.3 (0.67–114)
Lower HIV prevalence in adults: lower bound country estimates by UNAIDS/WHO** 0.9 (0.08–27) 3.2 (0.28–108)
Higher HIV prevalence in adults: upper bound country estimates by UNAIDS/WHO** 2.2 (0.37–29) 8.0 (1.2–121)
Lower HIV prevalence in children <14 y: lower bound country estimates by UNAIDS/WHO†† 1.3 (0.20–27) 3.9 (0.47–111)
Higher HIV prevalence in children <14 y: upper bound country estimates by UNAIDS/WHO†† 1.5 (0.23–29) 6.8 (1.08–119)

*N.A., not applicable; CFR, malaria case-fatality rate; RR, relative risk; UNAIDS, Joint United Nations Programme on HIV/AIDS/WHO.
†Continental total. In none of the scenarios did the ranking of countries in magnitude of HIV impact change appreciably. Across all scenarios, the minimum and maximum increases (in brackets) were always in Senegal or Mauritania, and in Botswana, respectively. An exception was the scenarios of lower HIV prevalence in adults, for which the lowest malaria impacts would be in Sierra Leone and Somalia.
‡The overall relative risk for malaria mortality due to HIV-1 in stable HIV-1 epidemics is now 2.1, i.e., does no longer fit the observed value of ≈4 (see Methods, Malaria mortality and Effect of HIV).
§The overall relative risk for malaria mortality due to HIV-1 in stable HIV-1 epidemics is now 5.7, i.e., does no longer fit the observed value of ≈4 (see Methods, Malaria death and effect of HIV).
¶As in Western populations (25).
#To allow for a possible initial drop in CD4 immediately upon infection, i.e., still before seroconversion.
**Cross-country median lowerbound estimate of HIV prevalence in adults 2.7%; cross-country median upperbound HIV prevalence estimate 8.8% (compared to default point estimate of 4.8%).
††Cross-country median lowerbound estimate of HIV prevalence in children <14 years of 0.2%; cross-country median upperbound HIV prevalence estimate 1.1% (compared to default point estimate of 0.5%).

Main Article

References
  1. Chandramohan  D, Greenwood  BM. Is there an interaction between human immunodeficiency virus and Plasmodium falciparum? Int J Epidemiol. 1998;27:296301. DOIPubMedGoogle Scholar
  2. World Health Organization. Malaria and HIV/AIDS interactions and implications: conclusions of a technical consultation convened by WHO; 2004 23–25 June. Report no.: WHO/HIV/2004.08. Geneva; 2004.
  3. Grimwade  K, French  N, Mbatha  DD, Zungu  DD, Dedicoat  M, Gilks  CF. Childhood malaria in a region of unstable transmission and high human immunodeficiency virus prevalence. Pediatr Infect Dis J. 2003;22:105763. DOIPubMedGoogle Scholar
  4. Grimwade  K, French  N, Mbatha  DD, Zungu  DD, Dedicoat  M, Gilks  CF. HIV infection as a cofactor for severe falciparum malaria in adults living in a region of unstable malaria transmission in South Africa. AIDS. 2004;18:54754. DOIPubMedGoogle Scholar
  5. Chirenda  J, Siziya  S, Tshimanga  M. Association of HIV infection with the development of severe and complicated malaria cases at a rural hospital in Zimbabwe. Cent Afr J Med. 2000;46:59. DOIPubMedGoogle Scholar
  6. Kalyesubula  I, Musoke-Mudido  P, Marum  L, Bagenda  D, Aceng  E, Ndugwa  C, Effects of malaria infection in human immunodeficiency virus type 1-infected Ugandan children. Pediatr Infect Dis J. 1997;16:87681. DOIPubMedGoogle Scholar
  7. Leaver  RJ, Haile  Z, Watters  DA. HIV and cerebral malaria. Trans R Soc Trop Med Hyg. 1990;84:201. DOIPubMedGoogle Scholar
  8. Greenberg  AE, Nsa  W, Ryder  RW, Medi  M, Nzeza  M, Kitadi  N, Plasmodium falciparum malaria and perinatally acquired human immunodeficiency virus type 1 infection in Kinshasa, Zaire. A prospective, longitudinal cohort study of 587 children. N Engl J Med. 1991;325:1059. DOIPubMedGoogle Scholar
  9. Whitworth  J, Morgan  D, Quigley  M, Smith  A, Mayanja  B, Eotu  H, Effect of HIV-1 and increasing immunosuppression on malaria pasitaemia and clinical episodes in adults in rural Uganda: a cohort study. Lancet. 2000;356:10516. DOIPubMedGoogle Scholar
  10. French  N, Nakiyingi  J, Lugada  E, Watera  C, Whitworth  JAG, Gilks  CF. Increasing rates of malarial fever with deteriorating immune status in HIV-1 infected Ugandan adults. AIDS. 2001;15:899906. DOIPubMedGoogle Scholar
  11. Asamoah-Odei  E, Garcia Calleja  JM, Boerma  JT. HIV prevalence and trends in sub-Saharan Africa: no decline and large subregional differences. Lancet. 2004;364:3540. DOIPubMedGoogle Scholar
  12. Korenromp  EL, Williams  BG, Gouws  E, Dye  C, Snow  RW. Measurement of trends in childhood malaria mortality in Africa: an assessment of progress toward targets based on verbal autopsy. Lancet Infect Dis. 2003;3:34958. DOIPubMedGoogle Scholar
  13. Craig  MH, Kleinschmidt  I, le Sueur  D, Sharp  BL. Exploring thirty years of malaria case data in KwaZulu-Natal, South Africa, Part II: the impact of non-climatic factors. Trop Med Int Health. 2004;9:125866. DOIPubMedGoogle Scholar
  14. Tsoka  JM, Sharp  BL, Kleinschmidt  I. Malaria mortality in a high-risk area of South Africa. Presented at Third MIM Pan-American malaria conference: Global advances in malaria research: Evidence-based decision making for malaria control policy. Abstract 528. Arusha, Tanzania, November, 2002.
  15. Sharp  B, van Wyk  P, Sikasote  JB, Banda  P, Kleinschmidt  I. Malaria control by residual insecticide spraying in Chingola and Chililabombwe, Copperbelt Province, Zambia. Trop Med Int Health. 2002;7:7326. DOIPubMedGoogle Scholar
  16. Trape  JF. The public health impact of chloroquine resistance in Africa. Am J Trop Med Hyg. 2001;64:127.PubMedGoogle Scholar
  17. Mouchet  J, Manguin  S, Sircoulon  J, Laventure  S, Faye  O, Onapa  AW, Evolution of malaria in Africa for the past 40 years: impact of climatic and human factors. J Am Mosq Control Assoc. 1998;14:12130.PubMedGoogle Scholar
  18. Kleinschmidt  I, Omumbo  J, Briet  O, van de Giesen  N, Sogoba  N, Mensah  NK, An empirical malaria distribution map for West Africa. Trop Med Int Health. 2001;6:77986. DOIPubMedGoogle Scholar
  19. Snow  RW, Craig  MH, Newton  CRJC, Steketee  RW. The public health burden of Plasmodium falciparum malaria in Africa: deriving the numbers. Working Paper 11, Disease Control Priorities Project. In: The Disease Control Priorities Project (DCPP) Working Paper Series. Bethesda (Maryland): Fogarty International Center, National Institutes of Health; 2003.
  20. Robert  V, Macintyre  K, Keating  J, Trape  JF, Duchemin  JB, Warren  M, Malaria transmission in urban sub-Saharan Africa. Am J Trop Med Hyg. 2003;68:16976.PubMedGoogle Scholar
  21. Nájera  JA, Hempel  J. The burden of malaria. Geneva: World Health Organization, Div. of Control of Tropical Disease, Malaria unit; 1996. Report No.: CTD/MAL/96.10.
  22. Improved methods and assumptions for estimation of the HIV/AIDS epidemic and its impact: Recommendations of the UNAIDS Reference Group on Estimates, Modelling and Projections. AIDS. 2002;16:W1–14.PubMedGoogle Scholar
  23. Kelly  P, Zulu  I, Amadi  B, Munkanta  M, Banda  J, Rodrigues  LC, Morbidity and nutritional impairment in relation to CD4 count in a Zambian population with high HIV prevalence. Acta Trop. 2002;83:1518. DOIPubMedGoogle Scholar
  24. Levin  A, Brubaker  G, Shao  JS, Kumby  D, O'Brien  TR, Goedert  JJ, Determination of T-lymphocyte subsets on site in rural Tanzania: results in HIV-1 infected and non-infected individuals. Int J STD AIDS. 1996;7:28891. DOIPubMedGoogle Scholar
  25. Tsegaye  A, Messele  T, Tilahun  T, Hailu  E, Sahlu  T, Doorly  R, Immunohematological reference ranges for adult Ethiopians. Clin Diagn Lab Immunol. 1999;6:4104.PubMedGoogle Scholar
  26. Urassa  W, Bakari  M, Sandstrom  E, Swai  A, Pallangyo  K, Mbena  E, Rate of decline of absolute number and percentage of CD4 T lymphocytes among HIV-1-infected adults in Dar es Salaam, Tanzania. AIDS. 2004;18:4338. DOIPubMedGoogle Scholar
  27. Colebunders  R, Bahwe  Y, Nekwei  W, Ryder  R, Perriens  J, Nsimba  K, Incidence of malaria and efficacy of oral quinine in patients recently infected with human immunodeficiency virus in Kinshasa, Zaire. J Infect. 1990;21:16773. DOIPubMedGoogle Scholar
  28. UNAIDS. Report on the global HIV/AIDS epidemic. Geneva: Joint United Nations Programme on HIV/AIDS (UNAIDS); 2004 June. Report No.: UNAIDS/04.16E.
  29. Beier  JC, Killeen  GF, Githure  JI. Short report: entomologic inoculation rates and Plasmodium falciparum malaria prevalence in Africa. Am J Trop Med Hyg. 1999;61:10913.PubMedGoogle Scholar
  30. United Nations. World population prospects - the 2004 revision population database. New York: United Nations Population Division; 2002.
  31. Taha  TET, Canner  JK, Dallabetta  GA, Chiphangwi  JD, Liomba  G, Wangel  A-M, Childhood malaria parasitaemia and HIV in Malawi. Trans R Soc Trop Med Hyg. 1994;88:1645. DOIPubMedGoogle Scholar
  32. Birku  Y, Mekonnen  E, Bjorkman  A, Wolday  D. Delayed clearance of Plasmodium falciparum in patients with human immunodeficiency virus co-infection treated with artemisinin. Ethiop Med J. 2002;40(Suppl.1):1726.PubMedGoogle Scholar
  33. Kamya  MR, Kigonya  CN, McFarland  W. HIV infection may adversely affect clinical response to chloroquine therapy for uncomplicated malaria in children. AIDS. 2001;15:11878. DOIPubMedGoogle Scholar
  34. Muller  O, Musoke  P, Sen  G, Moser  R. Pediatric HIV-1 disease in a Kampala Hospital. J Trop Pediatr. 1990;36:2836.PubMedGoogle Scholar
  35. Niyongabo  T, Deloron  P, Aubry  P, Ndarugirire  F, Manirakiza  F, Muhirwa  G, Prognostic indicators in adult cerebral malaria: a study in Burundi, an area of high prevalence of HIV infection. Acta Trop. 1994;56:299305. DOIPubMedGoogle Scholar
  36. Declich  S, Clerici  M, Okwey  R, Ouma  J, Ochakachon  R, Francesconi  P, Investigating the association between HIV and malaria in sub-Saharan Africa. In: XIVth International AIDS conference; 2002 July 7–12; Barcelona, Spain; 2002. Abstract number ThPeC7607.
  37. Cohen  C, Karstaedt  A, Govender  N, Thomas  J, Hlatshwayo  D, Dini  L, Increase in severe malaria in HIV-positive adults in South Africa. In: XIVth International AIDS conference; 2002 July 7–12; Barcelona, Spain; 2002. Abstract number ThPeC7602.
  38. Williams  BG, Dye  C. Antiretroviral drugs for tuberculosis control in the era of HIV/AIDS. Science. 2003;301:15357. DOIPubMedGoogle Scholar
  39. Auvert  B, Males  S, Puren  A, Taljaard  D, Carael  M, Williams  B. Can highly active antiretroviral therapy reduce the spread of HIV? A study in a township of South Africa. J Acquir Immune Defic Syndr. 2004;36:61321. DOIPubMedGoogle Scholar
  40. Morgan  D, Mahe  C, Mayanja  B, Whitworth  JA. Progression to symptomatic disease in people infected with HIV-1 in rural Uganda: prospective cohort study. BMJ. 2002;324:1936. DOIPubMedGoogle Scholar
  41. Mermin  J, Lule  J, Ekwaru  JP, Malamba  S, Downing  R, Ransom  R, Effect of co-trimoxazole prophylaxis on morbidity, mortality, CD4-cell count, and viral load in HIV infection in rural Uganda. Lancet. 2004;364:142834. DOIPubMedGoogle Scholar
  42. Craig  MH, Snow  RW, le Sueur  D. A climate-based distribution model of malaria transmission in sub-Saharan Africa. Parasitol Today. 1999;15:10511. DOIPubMedGoogle Scholar
  43. Muller  O, Moser  R. The clinical and parasitological presentation of Plasmodium falciparum malaria in Uganda is unaffected by HIV-1 infection. Trans R Soc Trop Med Hyg. 1990;84:3368. DOIPubMedGoogle Scholar
  44. Seyler  C, Anglaret  X, Dakoury-Dogbo  N, Messou  E, Toure  S, Danel  C, Medium-term survival, morbidity and immunovirological evolution in HIV-infected adults receiving antiretroviral therapy, Abidjan, Cote d'Ivoire. Antivir Ther. 2003;8:38593.PubMedGoogle Scholar
  45. World Health Organization. UNAIDS, UNICEF. Joint WHO/UNAIDS/UNICEF statement on use of cotrimoxazole as prophylaxis in HIV exposed and HIV infected children. 2004 Nov 22 [cited 2004 Nov 25]; Available from: http://www.who.int/hiv/en/
  46. Anglaret  X, Chene  G, Attia  A, Toure  S, Lafont  S, Combe  P, Early chemoprophylaxis with trimethoprim-sulphamethoxazole for HIV-1 infected adults in Abidjan, Cote d'Ivoire: a randomised trial. Lancet. 1999;353:14638. DOIPubMedGoogle Scholar
  47. Chintu  C, Bhat  GJ, Walker  AS, Mulenga  V, Sinyinza  F, Lishimpi  K, Co-trimoxazole as prophylaxis against opportunistic infections in HIV-infected Zambian children (CHAP): a double-blind randomised placebo-controlled trial. Lancet. 2004;364:186571. DOIPubMedGoogle Scholar
  48. Improved methods and assumptions for estimation of the HIV/AIDS epidemic and its impact: Recommendations of the UNAIDS Reference Group on Estimates, Modelling and Projections. AIDS. 2002;16:W1–14.PubMedGoogle Scholar
  49. Williams  BG, Dye  C. Antiretroviral drugs for tuberculosis control in the era of HIV/AIDS. Science. 2003;301:15357. DOIPubMedGoogle Scholar
  50. Urassa  W, Bakari  M, Sandstrom  E, Swai  A, Pallangyo  K, Mbena  E, Rate of decline of absolute number and percentage of CD4 T lymphocytes among HIV-1-infected adults in Dar es Salaam, Tanzania. AIDS. 2004;18:4338. DOIPubMedGoogle Scholar
  51. Kelly  P, Zulu  I, Amadi  B, Munkanta  M, Banda  J, Rodrigues  LC, Morbidity and nutritional impairment in relation to CD4 count in a Zambian population with high HIV prevalence. Acta Trop. 2002;83:1518. DOIPubMedGoogle Scholar
  52. Levin  A, Brubaker  G, Shao  JS, Kumby  D, O'Brien  TR, Goedert  JJ, Determination of T-lymphocyte subsets on site in rural Tanzania: results in HIV-1 infected and non-infected individuals. Int J STD AIDS. 1996;7:28891. DOIPubMedGoogle Scholar
  53. Tsegaye  A, Messele  T, Tilahun  T, Hailu  E, Sahlu  T, Doorly  R, Immunohematological reference ranges for adult Ethiopians. Clin Diagn Lab Immunol. 1999;6:4104.PubMedGoogle Scholar
  54. Tsegaye  A, Messele  T, Tilahun  T, Hailu  E, Sahlu  T, Doorly  R, Immunohematological reference ranges for adult Ethiopians. Clin Diagn Lab Immunol. 1999;6:4104.PubMedGoogle Scholar
  55. Morgan  D, Mahe  C, Mayanja  B, Okongo  JM, Lubega  R, Whitworth  JA. HIV-1 infection in rural Africa: is there a difference in median time to AIDS and survival compared with that in industrialized countries? AIDS. 2002;16:597603. DOIPubMedGoogle Scholar

Main Article

Page created: April 23, 2012
Page updated: April 23, 2012
Page reviewed: April 23, 2012
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external