Infection

, Volume 42, Issue 2, pp 281–294

TB and HIV in the Central African region: current knowledge and knowledge gaps

  • S. Janssen
  • M. A. M. Huson
  • S. Bélard
  • S. Stolp
  • N. Kapata
  • M. Bates
  • M. van Vugt
  • M. P. Grobusch
Review

Abstract

Purpose

Reliable and comprehensive data on the HIV/AIDS and TB co-pandemics from Central Africa remain scarce. This systematic review provides a comprehensive overview on current and past research activities in the region and provides a basis for future research work to close knowledge gaps.

Methods

The scientific literature was searched for publications meeting the following search terms: “tuberculosis” or “HIV” or “acquired immunodeficiency syndrome”, combined with “Central Africa”, or the names of individual countries within the region. Original studies, reviews and case series were included, and a selection of relevant articles was made.

Results

Most research in the field of HIV and TB has been conducted in Cameroon, where the epidemics have been described fairly well. The Democratic Republic of Congo ranked second on the amount of publications, despite the civil wars over the past several decades. Very little has been published on HIV and TB in the other countries, possibly due to the poor infrastructure of health care systems, lack of scientific capacity building or shortage of laboratory equipment.

Conclusions

Despite the relatively high burden of HIV and TB in the Central African region, the amount of research activities on these topics is limited. A better understanding of the co-epidemics in this region is urgently needed. The occurrence of opportunistic infections, treatment complications and drug resistance in TB and HIV need to be better described; the failure of public health systems needs to be understood, and research infrastructure needs to be developed. Only then will it be possible to turn the tide against the HIV and TB epidemics in this region.

Keywords

HIV Tuberculosis Central Africa 

References

  1. 1.
  2. 2.
    John MA, Menezes CN, Chita G, Sanne I, Grobusch MP. High tuberculosis and HIV coinfection rate, Johannesburg. Emerg Infect Dis. 2007;13:795–6.PubMedPubMedCentralGoogle Scholar
  3. 3.
    World Health Organization (WHO). Global tuberculosis report 2013. 2013. http://www.who.int/tb/publications/global_report/en/.
  4. 4.
    Dheda K, Shean K, Zumla A, Badri M, Streicher EM, Page-Shipp L, et al. Early treatment outcomes and HIV status of patients with extensively drug-resistant tuberculosis in South Africa: a retrospective cohort study. Lancet. 2010;375:1798–807.PubMedGoogle Scholar
  5. 5.
    Gandhi NR, Moll A, Sturm AW, Pawinski R, Govender T, Lalloo U, et al. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet. 2006;368:1575–80.PubMedGoogle Scholar
  6. 6.
    Grobusch MP. Drug-resistant and extensively drug-resistant tuberculosis in southern Africa. Curr Opin Pulm Med. 2010;16:180–5.PubMedGoogle Scholar
  7. 7.
    Fonjungo PN, Mpoudi EN, Torimiro JN, Alemnji GA, Eno LT, Nkengasong JN, et al. Presence of diverse human immunodeficiency virus type 1 viral variants in Cameroon. AIDS Res Hum Retroviruses. 2000;16:1319–24.PubMedGoogle Scholar
  8. 8.
    Parris GE. Mechanism and history of evolution of symbiotic HIV strains into lethal pandemic strains: the key event may have been a 1927 trial of pamaquine in Leopoldville (Kinshasa), Congo. Med Hypotheses. 2007;69:838–48.PubMedGoogle Scholar
  9. 9.
    Strickland GT. An epidemic of hepatitis C virus infection while treating endemic infectious diseases in Equatorial Africa more than a half century ago: did it also jump-start the AIDS pandemic? Clin Infect Dis. 2010;51:785–7.PubMedGoogle Scholar
  10. 10.
    Vangroenweghe D. The earliest cases of human immunodeficiency virus type 1 group M in Congo-Kinshasa, Rwanda and Burundi and the origin of acquired immune deficiency syndrome. Philos Trans R Soc Lond B Biol Sci. 2001;356:923–5.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Worobey M, Gemmel M, Teuwen DE, Haselkorn T, Kunstman K, Bunce M, et al. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature. 2008;455:661–4.PubMedPubMedCentralGoogle Scholar
  12. 12.
    UNAIDS. UNAIDS report on the global AIDS epidemic 2010. 2010. http://www.unaids.org/globalreport/global_report.htm.
  13. 13.
    World Health Organization (WHO). Multidrug and extensively drug-resistant TB (M/XDR-TB): 2010 global report on surveillance and response. 2010. http://whqlibdoc.who.int/publications/2010/9789241599191_eng.pdf.
  14. 14.
    Abubakar I, Zignol M, Falzon D, Raviglione M, Ditiu L, Masham S, et al. Drug-resistant tuberculosis: time for visionary political leadership. Lancet Infect Dis. 2013;13:529–39.PubMedGoogle Scholar
  15. 15.
    Sibanda EN, Stanczuk G, Kasolo F. HIV/AIDS in Central Africa: pathogenesis, immunological and medical issues. Int Arch Allergy Immunol. 2003;132:183–95.PubMedGoogle Scholar
  16. 16.
    Aghokeng AF, Kouanfack C, Laurent C, Ebong E, Atem-Tambe A, Butel C, et al. Scale-up of antiretroviral treatment in sub-Saharan Africa is accompanied by increasing HIV-1 drug resistance mutations in drug-naive patients. AIDS. 2011;25:2183–8.PubMedGoogle Scholar
  17. 17.
    Mauch V, Weil D, Munim A, Boillot F, Coninx R, Huseynova S, et al. Structure and management of tuberculosis control programs in fragile states—Afghanistan, DR Congo, Haiti, Somalia. Health Policy. 2010;96:118–27.PubMedGoogle Scholar
  18. 18.
    Mbuagbaw J, Eyong I, Alemnji G, Mpoudi N, Same-Ekobo A. Patterns of skin manifestations and their relationships with CD4 counts among HIV/AIDS patients in Cameroon. Int J Dermatol. 2006;45:280–4.Google Scholar
  19. 19.
    Mbanya DN, Zebaze R, Minkoulou EM, Binam F, Koulla S, Obounou A. Clinical and epidemiologic trends in HIV/AIDS patients in a hospital setting of Yaounde, Cameroon: a 6-year perspective. Int J Infect Dis. 2002;6:134–8.PubMedGoogle Scholar
  20. 20.
    Nyambi P, Zekeng L, Kenfack H, Tongo M, Nanfack A, Nkombe I, et al. HIV infection in rural villages of Cameroon. J Acquir Immune Defic Syndr. 2002;31:506–13.PubMedGoogle Scholar
  21. 21.
    Sieleunou I, Souleymanou M, Schönenberger AM, Menten J, Boelaert M. Determinants of survival in AIDS patients on antiretroviral therapy in a rural centre in the Far-North Province, Cameroon. Trop Med Int Health. 2009;14:36–43.PubMedGoogle Scholar
  22. 22.
    Lydié N, Robinson NJ, Ferry B, Akam E, De Loenzien M, Abega S; Study Group on Heterogeneity of HIV Epidemics in African Cities. Mobility, sexual behavior, and HIV infection in an urban population in Cameroon. J Acquir Immune Defic Syndr. 2004;35:67–74.PubMedGoogle Scholar
  23. 23.
    Noeske J, Kuaban C, Cunin P. Are smear-positive pulmonary tuberculosis patients a ‘sentinel’ population for the HIV epidemic in Cameroon? Int J Tuberc Lung Dis. 2004;8:346–51.PubMedGoogle Scholar
  24. 24.
    Noeske J, Ndi N, Mbondi S. Controlling tuberculosis in prisons against confinement conditions: a lost case? Experience from Cameroon. Int J Tuberc Lung Dis. 2011;15:223–7.PubMedGoogle Scholar
  25. 25.
    Basaras M, Santamaría A, Sarsa M, Gutiérrez E, de Olano Y, Cisterna R. Seroprevalence of hepatitis B and C, and human immunodeficiency type 1 viruses in a rural population from the Republic of Equatorial Guinea. Trans R Soc Trop Med Hyg. 1999;93:250–2.PubMedGoogle Scholar
  26. 26.
    Tudó G, González-Martín J, Obama R, Rodríguez JM, Franco JR, Espasa M, et al. Molecular epidemiology of tuberculosis in the Bata and Malabo districts of Equatorial Guinea. Int J Tuberc Lung Dis. 2004;8:1458–63.PubMedGoogle Scholar
  27. 27.
    Charpentier C, Koyalta D, Ndinaromtan M, Tchobkréo B, Jenabian MA, Day N, et al. Distribution of HIV-1 and HSV-2 epidemics in Chad revealing HSV-2 hot-spot in regions of high-risk HIV spread. J Infect Dev Ctries. 2011;5:64–7.PubMedPubMedCentralGoogle Scholar
  28. 28.
    Wyss K, Hutton G, N’Diekhor Y. Costs attributable to AIDS at household level in Chad. AIDS Care. 2004;16:808–16.PubMedGoogle Scholar
  29. 29.
    Daugla DM, Daoud S, Tanner M, Zinsstag J, Schelling E. Morbidity patterns in three nomadic communities in Chari-Baguirmi and Kanem, Chad. Med Trop (Mars). 2004;64:469–73.Google Scholar
  30. 30.
    Schelling E, Daoud S, Daugla DM, Diallo P, Tanner M, Zinsstag J. Morbidity and nutrition patterns of three nomadic pastoralist communities of Chad. Acta Trop. 2005;95:16–25.PubMedGoogle Scholar
  31. 31.
    Médecins Sans Frontières. Central African Republic: a state of silent crisis. 2011. http://www.msf.org.uk/sites/uk/files/a_state_of_silent_crisis_en_0.pdf.
  32. 32.
    Nouvel LX, Kassa-Kelembho E, Dos Vultos T, Zandanga G, Rauzier J, Lafoz C, et al. Multidrug-resistant Mycobacterium tuberculosis, Bangui, Central African Republic. Emerg Infect Dis. 2006;12:1454–6.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Garin B, Glaziou P, Kassa-Kelembho E, Yassibanda S, Mbelesso P, Morvan J. High mortality rates among patients with tuberculosis in Bangui, Central African Republic. Lancet. 1997;350:1298.PubMedGoogle Scholar
  34. 34.
    Mbendi Nlombi C, Longo-Mbenza B, Mbendi Nsukini S, Muyembe Tamfum JJ, Situakibanza Nanituma H, Vangu Ngoma D. Prevalence of HIV and HBs antigen in blood donors. Residual risk of contamination in blood recipients in East Kinshasa, Democratic Republic of the Congo. Med Trop (Mars). 2001;61:139–42.Google Scholar
  35. 35.
    Kim AA, Malele F, Kaiser R, Mama N, Kinkela T, Mantshumba JC, et al. HIV infection among internally displaced women and women residing in river populations along the Congo River, Democratic Republic of Congo. AIDS Behav. 2009;13:914–20.PubMedGoogle Scholar
  36. 36.
    Bernal MC, Galán MI, Ocete MD, Leyva A, García F, García-Valdecasas J, et al. A seroepidemiological study of human immunodeficiency virus infection in northeast Zaire. Infection. 1994;22:174–7.PubMedGoogle Scholar
  37. 37.
    Laga M, Manoka A, Kivuvu M, Malele B, Tuliza M, Nzila N, et al. Non-ulcerative sexually transmitted diseases as risk factors for HIV-1 transmission in women: results from a cohort study. AIDS. 1993;7:95–102.PubMedGoogle Scholar
  38. 38.
    Laga M, Alary M, Nzila N, Manoka AT, Tuliza M, Behets F, et al. Condom promotion, sexually transmitted diseases treatment, and declining incidence of HIV-1 infection in female Zairian sex workers. Lancet. 1994;344:246–8.PubMedGoogle Scholar
  39. 39.
    Mwandagalirwa K, Jackson EF, McClamroch K, Bollinger R, Ryder RW, Weir SS. Local differences in human immunodeficiency virus prevalence: a comparison of social venue patrons, antenatal patients, and sexually transmitted infection patients in eastern kinshasa. Sex Transm Dis. 2009;36:406–12.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Nelson AM, Perriëns JH, Kapita B, Okonda L, Lusamuno N, Kalengayi MR, et al. A clinical and pathological comparison of the WHO and CDC case definitions for AIDS in Kinshasa, Zaïre: is passive surveillance valid? AIDS. 1993;7:1241–5.PubMedGoogle Scholar
  41. 41.
    Tshikuka Mulumba JG, Atua Matindii B, Kilauzi AL, Mengema B, Mafuta J, Eloko Eya Matangelo G, et al. Severity of outcomes associated to types of HIV coinfection with TB and malaria in a setting where the three pandemics overlap. J Community Health. 2012;37:1234–8.PubMedGoogle Scholar
  42. 42.
    Thea DM, St Louis ME, Atido U, Kanjinga K, Kembo B, Matondo M, et al. A prospective study of diarrhea and HIV-1 infection among 429 Zairian infants. N Engl J Med. 1993;329:1696–702.PubMedGoogle Scholar
  43. 43.
    Van Rie A, Mupuala A, Dow A. Impact of the HIV/AIDS epidemic on the neurodevelopment of preschool-aged children in Kinshasa, Democratic Republic of the Congo. Pediatrics. 2008;122:e123–8.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Ryder RW, Batter V, Kaseka N, Behets F, Sequeira D, M’Boly E, et al. Effect of HIV-1 infection on tuberculosis and fertility in a large workforce in Kinshasa, Democratic Republic of the Congo. AIDS Patient Care STDS. 2000;14:297–304.PubMedGoogle Scholar
  45. 45.
    Henegar C, Behets F, Vanden Driessche K, Tabala M, Bahati E, Bola V, et al. Mortality among tuberculosis patients in the Democratic Republic of Congo. Int J Tuberc Lung Dis. 2012;16:1199–204.PubMedGoogle Scholar
  46. 46.
    Edmonds A, Lusiama J, Napravnik S, Kitetele F, Van Rie A, Behets F. Anti-retroviral therapy reduces incident tuberculosis in HIV-infected children. Int J Epidemiol. 2009;38:1612–21.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Klausner JD, Ryder RW, Baende E, Lelo U, Williame JC, Ngamboli K, et al. Mycobacterium tuberculosis in household contacts of human immunodeficiency virus type 1-seropositive patients with active pulmonary tuberculosis in Kinshasa, Zaire. J Infect Dis. 1993;168:106–11.PubMedGoogle Scholar
  48. 48.
    Le Coeur S, Halembokaka G, Khlat M, Brouard N, Purhuence F, M’Pelé P, et al. Impact of AIDS on adult mortality: a morgue-based study in Pointe-Noire, Republic of Congo. AIDS. 2005;19:1683–7.PubMedGoogle Scholar
  49. 49.
    Pictet G, Le Coeur S, M’Pelé P, Brouard N, Lallemant M. Contribution of AIDS to the general mortality in Central Africa: evidence from a morgue-based study in Brazzaville, Congo. AIDS. 1998;12:2217–23.PubMedGoogle Scholar
  50. 50.
    Mabiala-Babela JR, M’Pemba Loufoua AB, Mouko A, Senga P. Pulmonary tuberculosis in infants in Brazzaville, Congo. A review of 117 cases. Med Trop (Mars). 2008;68:167–72.Google Scholar
  51. 51.
    Mabiala-Babela JR, Makosso E, Senga P. Retrospective study of 61 cases of multifocal tuberculosis in children in Brazzaville, Congo. Med Trop (Mars). 2008;68:41–4.Google Scholar
  52. 52.
    Mpemba Loufoua-Lemay AB, Nzingoula S. Peritoneal tuberculosis in children at the University Hospital Center of Brazzaville: 35 cases. Arch Pediatr. 2003;10:356–7.PubMedGoogle Scholar
  53. 53.
    M’Pemba Loufoua-Lemay AB, Youndouka JM, Pambou B, Nzingoula S. Child tuberculosis at the teaching hospital of Brazzaville from 1995 to 2003. Bull Soc Pathol Exot. 2008;101:303–7.PubMedGoogle Scholar
  54. 54.
    M’Boussa J, Yokolo D, Pereira B, Ebata-Mongo S. A flare-up of tuberculosis due to war in Congo Brazzaville. Int J Tuberc Lung Dis. 2002;6:475–8.PubMedGoogle Scholar
  55. 55.
    M’Pemba Loufoua Lemay AB, Mabiala Babela JR, Bantsimba T, Nzingoula S. Tuberculosis and HIV/AIDS co-infection in children: experience carried out in paediatric service of the teaching Hospital of Brazzaville, Republic of Congo (1995–2004). Bull Soc Pathol Exot. 2007;100:51–2.PubMedGoogle Scholar
  56. 56.
    Tevi-Benissan C, Okome M, Makuwa M, Nkoume MN, Lansoud-Soukate J, Georges A, et al. HIV-2 infection and HIV-1/HIV-2 dual reactivity in patients with and without AIDS-related symptoms in Gabon. Emerg Infect Dis. 1998;4:130–1.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Mounanga M, Revangue BS. HIV-1 seroprevalence in pregnant women in Libreville (Gabon). J Gynecol Obstet Biol Reprod (Paris). 1993;22:509–12.Google Scholar
  58. 58.
    Caron M, Lekana-Douki SE, Makuwa M, Obiang-Ndong GP, Biba O, Nkoghé D, et al. Prevalence, genetic diversity and antiretroviral drugs resistance-associated mutations among untreated HIV-1-infected pregnant women in Gabon, Central Africa. BMC Infect Dis. 2012;12:64.PubMedPubMedCentralGoogle Scholar
  59. 59.
    Bertherat E, Georges-Courbot MC, Nabias R, Georges AJ, Renaut A. Seroprevalence of four sexually transmitted diseases in a semi-urban population of Gabon. Int J STD AIDS. 1998;9:31–6.PubMedGoogle Scholar
  60. 60.
    Schrijvers D, Delaporte E, Peeters M, Dupont A, Meheus A. Seroprevalence of retroviral infection in women with different fertility statuses in Gabon, western equatorial Africa. J Acquir Immune Defic Syndr. 1991;4:468–70.PubMedGoogle Scholar
  61. 61.
    Mvé MT, Bisvigou U, Barry NC, Ondo CE, Nkoghe D. Reasons for stopping and restarting tuberculosis treatment in Libreville (Gabon). Sante. 2010;20:31–4.PubMedGoogle Scholar
  62. 62.
    Nkoghe D, Toung Mve M, Nnegue S, Okome Nkoume M, Iba BJ, Hypolite J, et al. HIV seroprevalence among tuberculosis patients in Nkembo Hospital, Libreville, Gabon. Short note. Bull Soc Pathol Exot. 2005;98:121–2.PubMedGoogle Scholar
  63. 63.
    Mouba JF, Miloundja J, Mimbila-Mayi M, Ndjenkam FT, N’zouba L. Cervical lymph node tuberculosis in Libreville: epidemiology, diagnosis, and therapy. Sante. 2011;21:165–8.PubMedGoogle Scholar
  64. 64.
    Kombila DU, Moussavou-Kombila JB, Grobusch MP, Lell B. Clinical and laboratory features of tuberculosis within a hospital population in Libreville, Gabon. Infection. 2013;41:737–9.PubMedGoogle Scholar
  65. 65.
    Mbopi-Kéou FX, Dempouo Djomassi L, Monebenimp F. Study of factors related to adherence to antiretroviral therapy among patients followed at HIV/AIDS Unit in the District Hospital of Dschang, Cameroon. Pan Afr Med J. 2012;12:55.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Ebana Mvogo C, Ellong A, Bella AL, Luma H, Achu Joko H. Ocular complications of HIV/AIDS in Cameroon: is there is any correlation with the level of CD4 lymphocytes count? Bull Soc Belge Ophtalmol. 2007;305:7–12.PubMedGoogle Scholar
  67. 67.
    Ibara JR, Itoua C, Gathse A, Obengui, Gassaye D, Nkoua JL, et al. Acquired immunodeficiency syndrome in elderly persons in a tropical zone. Apropos of 175 cases in the Congo. Bull Soc Pathol Exot. 2002;95:100–2.PubMedGoogle Scholar
  68. 68.
    Okome Nkoumou MM, Okome Essima R, Obiang Ndong GP, Okome Miame F. Clinical and laboratory findings in HIV-infected patients at the Jeanne Ebori Foundation in Libreville, Gabon (2002–2005). Med Trop (Mars). 2007;67:357–62.Google Scholar
  69. 69.
    Kuaban C, Fotsin JG, Koulla-Shiro S, Ekono MR, Hagbe P. Lower lung field tuberculosis in Yaounde, Cameroon. Cent Afr J Med. 1996;42:62–5.PubMedGoogle Scholar
  70. 70.
    Kuaban C, Koulla-Shiro S, Lekama Assiene T, Hagbe P. Tuberculosis screening of patient contacts in 1993 and 1994 in Yaounde, Cameroon. Med Trop (Mars). 1996;56:156–8.Google Scholar
  71. 71.
    Pefura Yone EW, Kuaban C, Simo L. Tuberculous pleural effusion in Yaounde, Cameroon: The influence of HIV infection. Rev Mal Respir. 2011;28:1138–45.PubMedGoogle Scholar
  72. 72.
    Sume GE, Hoshen M, Bita G, Kabore S, Nzima VN. Treatment outcome of TB/HIV positive and negative smear positive pulmonary tuberculosis patients treated using daily self-administered therapy in a Cameroonian district hospital. East Afr Med J. 2009;86:469–75.PubMedGoogle Scholar
  73. 73.
    Kuaban C, Bame R, Mouangue L, Djella S, Yomgni C. Non conversion of sputum smears in new smear positive pulmonary tuberculosis patients in Yaounde, Cameroon. East Afr Med J. 2009;86:219–25.PubMedGoogle Scholar
  74. 74.
    Breton G, Service YB, Kassa-Kelembho E, Mbolidi CD, Minssart P. Tuberculosis and HIV in Bangui, Central African Republic: strong prevalence and management difficulties. Med Trop (Mars). 2002;62:623–6.Google Scholar
  75. 75.
    Chartier L, Leng C, Sire JM, Le Minor O, Saman M, Bercion R, et al. Factors associated with negative direct sputum examination in Asian and African HIV-infected patients with tuberculosis (ANRS 1260). PLoS One. 2011;6:e21212.PubMedPubMedCentralGoogle Scholar
  76. 76.
    Ondounda M, Ilozue C, Mounguengui D, Magne C, Nzenze JR. Clinical and radiological features of tuberculosis during HIV infection in Libreville, Gabon. Med Trop (Mars). 2011;71:253–6.Google Scholar
  77. 77.
    Engohan Alloghe E, Toung Mve M, Ramarojoana S, Iba J, Nkoghe D. Epidemiology of childhood tuberculosis in Libreville, Gabon from 1997 to 2001. Med Trop (Mars). 2006;66:469–71.Google Scholar
  78. 78.
    Cuadros DF, Branscum AJ, García-Ramos G. No evidence of association between HIV-1 and malaria in populations with low HIV-1 prevalence. PLoS One. 2011;6:23458.Google Scholar
  79. 79.
    Roka M, Goñi P, Rubio E, Clavel A. Prevalence of intestinal parasites in HIV-positive patients on the island of Bioko, Equatorial Guinea: its relation to sanitary conditions and socioeconomic factors. Sci Total Environ. 2012;432:404–11.PubMedGoogle Scholar
  80. 80.
    Mbopi-Kéou FX, Grésenguet G, Mayaud P, Weiss HA, Gopal R, Matta M, et al. Interactions between herpes simplex virus type 2 and human immunodeficiency virus type 1 infection in African women: opportunities for intervention. J Infect Dis. 2000;182:1090–6.PubMedGoogle Scholar
  81. 81.
    Mbopi-Kéou FX, Legoff J, Grésenguet G, Si-Mohamed A, Matta M, Mayaud P, et al. Genital shedding of herpes simplex virus-2 DNA and HIV-1 RNA and proviral DNA in HIV-1- and herpes simplex virus-2-coinfected African women. J Acquir Immune Defic Syndr. 2003;33:121–4.PubMedGoogle Scholar
  82. 82.
    Békondi C, Bernede C, Passone N, Minssart P, Kamalo C, Mbolidi D, et al. Primary and opportunistic pathogens associated with meningitis in adults in Bangui, Central African Republic, in relation to human immunodeficiency virus serostatus. Int J Infect Dis. 2006;10:387–95.PubMedGoogle Scholar
  83. 83.
    Modia O’Yandjo A, Foidart JM, Rigo J. Influence of HIV-1 and placental malaria co-infection on newborn biometry and Apgar scores in Kinshasa, Democratic Republic of Congo. J Gynecol Obstet Biol Reprod (Paris). 2011;40:460–4.Google Scholar
  84. 84.
    Perret JL, Moussavou-Kombila JB, Delaporte E, Minko-Mi-Etoua D, Pemba LF, Boguikouma JB, et al. Prevalence of hepatitis B and C virus, HTLV-1 and HIV in type B lymphoproliferative syndromes in Gabon. Bull Soc Pathol Exot. 2003;96:275–8.PubMedGoogle Scholar
  85. 85.
    World Health Organization (WHO). Progress report 2011: Global HIV/AIDS response. 2011. http://www.who.int/hiv/pub/progress_report2011/en/.
  86. 86.
    Jao J, Palmer D, Leus I, Tih P, Baweja M, Klotman M, et al. Prevalence and predictors of proteinuria in HIV-infected and uninfected pregnant women in Cameroon. Nephrol Dial Transplant. 2011;26:3051–3.PubMedGoogle Scholar
  87. 87.
    Nkenfou CN, Lobé EE, Ouwe-Missi-Oukem-Boyer O, Sosso MS, Dambaya B, Gwom LC, et al. Implementation of HIV early infant diagnosis and HIV type 1 RNA viral load determination on dried blood spots in Cameroon: challenges and propositions. AIDS Res Hum Retroviruses. 2012;28:176–81.PubMedGoogle Scholar
  88. 88.
    Torpey K, Kasonde P, Kabaso M, Weaver MA, Bryan G, Mukonka V, et al. Reducing pediatric HIV infection: estimating mother-to-child transmission rates in a program setting in Zambia. J Acquir Immune Defic Syndr. 2010;54:415–22.PubMedGoogle Scholar
  89. 89.
    Kouanda S, Tougri H, Cisse M, Simpore J, Pietra V, Doulougou B, et al. Impact of maternal HAART on the prevention of mother-to-child transmission of HIV: results of an 18-month follow-up study in Ouagadougou, Burkina Faso. AIDS Care. 2010;22:843–50.PubMedGoogle Scholar
  90. 90.
    Namukwaya Z, Mudiope P, Kekitiinwa A, Musoke P, Matovu J, Kayma S, et al. The impact of maternal highly active antiretroviral therapy and short-course combination antiretrovirals for prevention of mother-to-child transmission on early infant infection rates at the Mulago national referral hospital in Kampala, Uganda, January 2007 to May 2009. J Acquir Immune Defic Syndr. 2011;56:69–75.PubMedGoogle Scholar
  91. 91.
    Azcoaga-Lorenzo A, Ferreyra C, Alvarez A, Palma PP, Velilla E, del Amo J. Effectiveness of a PMTCT programme in rural Western Kenya. AIDS Care. 2011;23:274–80.PubMedGoogle Scholar
  92. 92.
    Fitzgerald FC, Bekker LG, Kaplan R, Myer L, Lawn SD, Wood R. Mother-to-child transmission of HIV in a community-based antiretroviral clinic in South Africa. S Afr Med J. 2010;100:827–31.PubMedPubMedCentralGoogle Scholar
  93. 93.
    Mirkuzie AH, Hinderaker SG, Sisay MM, Moland KM, Mørkve O. Current status of medication adherence and infant follow up in the prevention of mother to child HIV transmission programme in Addis Ababa: a cohort study. J Int AIDS Soc. 2011;14:50.PubMedPubMedCentralGoogle Scholar
  94. 94.
    Ikechebelu JI, Ugboaja JO, Kalu SO, Ugochukwu EF. The outcome of prevention of mother to child transmission (PMTCT) of HIV infection programme in Nnewi, southeast Nigeria. Niger J Med. 2011;20:421–5.PubMedGoogle Scholar
  95. 95.
    Kouanfack C, Aghokeng AF, Mondain AM, Bourgeois A, Kenfack A, Mpoudi-Ngolé E, et al. Lamivudine-resistant HBV infection in HIV-positive patients receiving antiretroviral therapy in a public routine clinic in Cameroon. Antivir Ther. 2012;17:321–6.PubMedGoogle Scholar
  96. 96.
    Laurent C, Kouanfack C, Laborde-Balen G, Aghokeng AF, Mbougua JB, Boyer S, et al. Monitoring of HIV viral loads, CD4 cell counts, and clinical assessments versus clinical monitoring alone for antiretroviral therapy in rural district hospitals in Cameroon (Stratall ANRS 12110/ESTHER): a randomised non-inferiority trial. Lancet Infect Dis. 2011;11:825–33.PubMedGoogle Scholar
  97. 97.
    Van Rompaey S, Kimfuta J, Kimbondo P, Monn C, Buvé A. Operational assessment of access to ART in rural Africa: the example of Kisantu in Democratic Republic of the Congo. AIDS Care. 2011;23:686–93.PubMedGoogle Scholar
  98. 98.
    Ryder RW, Kamenga C, Jingu M, Mbuyi N, Mbu L, Behets F. Pregnancy and HIV-1 incidence in 178 married couples with discordant HIV-1 serostatus: additional experience at an HIV-1 counselling centre in the Democratic Republic of the Congo. Trop Med Int Health. 2000;5:482–7.PubMedGoogle Scholar
  99. 99.
    Laurent C, Meilo H, Guiard-Schmid JB, Mapouré Y, Noël JM, M’Bangué M, et al. Antiretroviral therapy in public and private routine health care clinics in Cameroon: lessons from the Douala antiretroviral (DARVIR) initiative. Clin Infect Dis. 2005;41:108–11.PubMedGoogle Scholar
  100. 100.
    Marcellin F, Boyer S, Protopopescu C, Dia A, Ongolo-Zogo P, Koulla-Shiro S, et al. Determinants of unplanned antiretroviral treatment interruptions among people living with HIV in Yaoundé, Cameroon (EVAL survey, ANRS 12-116). Trop Med Int Health. 2008;13:1470–8.PubMedGoogle Scholar
  101. 101.
    Billong SC, Fokam J, Nkwescheu AS, Kembou E, Milenge P, Tsomo Z, et al. Early warning indicators for HIV drug resistance in Cameroon during the year 2010. PLoS One. 2012;7:e36777.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Ndziessi G, Boyer S, Kouanfack C, Cohen J, Marcellin F, Moatti JP, et al. Adherence as a predictor of sexual behaviors in people living with HIV/AIDS during the first year of antiretroviral therapy in rural Cameroon: data from Stratall ANRS 12110/ESTHER trial. PLoS One. 2012;7:e36118.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Muko KN, Ngwa VC, Chigang LC, Ngwa IG, Meiburg A, Shu EN. Willingness to pay for treatment with highly active antiretroviral (HAART) drugs: a rural case study in Cameroon. SAHAR J. 2004;1:107–13.Google Scholar
  104. 104.
    Yumo HA, Mbanya D, Kuaban C, Neuhann F. Outcome assessment of a global fund grant for tuberculosis control at the district level in rural Cameroon. Int J Tuberc Lung Dis. 2011;15:352–7.PubMedGoogle Scholar
  105. 105.
    Njozing BN, Edin KE, San Sebastián M, Hurtig AK. Voices from the frontline: counsellors’ perspectives on TB/HIV collaborative activities in the Northwest Region, Cameroon. BMC Health Serv Res. 2011;11:328.PubMedPubMedCentralGoogle Scholar
  106. 106.
    Kuaban C, Bercion R, Jifon G, Cunin P, Blackett KN. Acquired anti-tuberculosis drug resistance in Yaounde, Cameroon. Int J Tuberc Lung Dis. 2000;4:427–32.PubMedGoogle Scholar
  107. 107.
    Mauclère P, Loussert-Ajaka I, Damond F, Fagot P, Souquières S, Monny Lobe M, et al. Serological and virological characterization of HIV-1 group O infection in Cameroon. AIDS. 1997;11:445–53.PubMedGoogle Scholar
  108. 108.
    Yamaguchi J, McArthur CP, Vallari A, Coffey R, Bodelle P, Beyeme M, et al. HIV-1 Group N: evidence of ongoing transmission in Cameroon. AIDS Res Hum Retroviruses. 2006;22:453–7.PubMedGoogle Scholar
  109. 109.
    Brennan CA, Bodelle P, Coffey R, Devare SG, Golden A, Hackett J Jr, et al. The prevalence of diverse HIV-1 strains was stable in Cameroonian blood donors from 1996 to 2004. J Acquir Immune Defic Syndr. 2008;49:432–9.PubMedGoogle Scholar
  110. 110.
    Burda ST, Konings FA, Williams CA, Anyangwe C, Nyambi PN. HIV-1 CRF09_cpx circulates in the North West Province of Cameroon where CRF02_AG infections predominate and recombinant strains are common. AIDS Res Hum Retroviruses. 2004;20:1358–63.PubMedGoogle Scholar
  111. 111.
    Carr JK, Wolfe ND, Torimiro JN, Tamoufe U, Mpoudi-Ngole E, Eyzaguirre L, et al. HIV-1 recombinants with multiple parental strains in low-prevalence, remote regions of Cameroon: evolutionary relics? Retrovirology. 2010;7:39.PubMedPubMedCentralGoogle Scholar
  112. 112.
    Konings FA, Haman GR, Xue Y, Urbanski MM, Hertzmark K, Nanfack A, et al. Genetic analysis of HIV-1 strains in rural eastern Cameroon indicates the evolution of second-generation recombinants to circulating recombinant forms. J Acquir Immune Defic Syndr. 2006;42:331–41.PubMedGoogle Scholar
  113. 113.
    Mboudjeka I, Bikandou B, Zekeng L, Takehisa J, Harada Y, Yamaguchi-Kabata Y, et al. Genetic diversity of HIV-1 group M from Cameroon and Republic of Congo. Arch Virol. 1999;144:2291–311.PubMedGoogle Scholar
  114. 114.
    Ndembi N, Takehisa J, Zekeng L, Kobayashi E, Ngansop C, Songok EM, et al. Genetic diversity of HIV type 1 in rural eastern Cameroon. J Acquir Immune Defic Syndr. 2004;37:1641–50.PubMedGoogle Scholar
  115. 115.
    Ndembi N, Iwamoto S, Ngansop C, Lemey P, Abimiku A, Mbanya D, et al. High frequency of HIV-1 dual infections in Cameroon, West Central Africa. J Acquir Immune Defic Syndr. 2011;57:e25–7.PubMedGoogle Scholar
  116. 116.
    Soares EA, Makamche MF, Siqueira JD, Lumngwena E, Mbuagbaw J, Kaptue L, et al. Molecular diversity and polymerase gene genotypes of HIV-1 among treatment-naïve Cameroonian subjects with advanced disease. J Clin Virol. 2010;48:173–9.PubMedGoogle Scholar
  117. 117.
    Yamaguchi J, Bodelle P, Vallari AS, Coffey R, McArthur CP, Schochetman G, et al. HIV infections in northwestern Cameroon: identification of HIV type 1 group O and dual HIV type 1 group M and group O infections. AIDS Res Hum Retroviruses. 2004;20:944–57.PubMedGoogle Scholar
  118. 118.
    Véras NM, Santoro MM, Gray RR, Tatem AJ, Lo Presti A, Olearo F, et al. Molecular epidemiology of HIV type 1 CRF02_AG in Cameroon and African patients living in Italy. AIDS Res Hum Retroviruses. 2011;27:1173–82.PubMedPubMedCentralGoogle Scholar
  119. 119.
    Faria NR, Suchard MA, Abecasis A, Sousa JD, Ndembi N, Bonfim I, et al. Phylodynamics of the HIV-1 CRF02_AG clade in Cameroon. Infect Genet Evol. 2012;12:453–60.PubMedGoogle Scholar
  120. 120.
    Ortiz M, Sanchez I, Gonzalez MP, León MI, Abeso N, Asumu E, et al. Molecular epidemiology of HIV type 1 subtypes in equatorial guinea. AIDS Res Hum Retroviruses. 2001;17:851–5.PubMedGoogle Scholar
  121. 121.
    Koyalta D, Charpentier C, Beassamda J, Rey E, Si-Mohamed A, Djemadji-Oudjeil N, et al. High frequency of antiretroviral drug resistance among HIV-infected adults receiving first-line highly active antiretroviral therapy in N’Djamena, Chad. Clin Infect Dis. 2009;49:155–9.PubMedGoogle Scholar
  122. 122.
    Vidal N, Koyalta D, Richard V, Lechiche C, Ndinaromtan T, Djimasngar A, et al. High genetic diversity of HIV-1 strains in Chad, West Central Africa. J Acquir Immune Defic Syndr. 2003;33:239–46.PubMedGoogle Scholar
  123. 123.
    Djoko CF, Rimoin AW, Vidal N, Tamoufe U, Wolfe ND, Butel C, et al. High HIV type 1 group M pol diversity and low rate of antiretroviral resistance mutations among the uniformed services in Kinshasa, Democratic Republic of the Congo. AIDS Res Hum Retroviruses. 2011;27:323–9.PubMedPubMedCentralGoogle Scholar
  124. 124.
    Mokili JL, Wade CM, Burns SM, Cutting WA, Bopopi JM, Green SD, et al. Genetic heterogeneity of HIV type 1 subtypes in Kimpese, rural Democratic Republic of Congo. AIDS Res Hum Retroviruses. 1999;15:655–64.PubMedGoogle Scholar
  125. 125.
    Vidal N, Peeters M, Mulanga-Kabeya C, Nzilambi N, Robertson D, Ilunga W, et al. Unprecedented degree of human immunodeficiency virus type 1 (HIV-1) group M genetic diversity in the Democratic Republic of Congo suggests that the HIV-1 pandemic originated in Central Africa. J Virol. 2000;74:10498–507.PubMedPubMedCentralGoogle Scholar
  126. 126.
    Bikandou B, Takehisa J, Mboudjeka I, Ido E, Kuwata T, Miyazaki Y, et al. Genetic subtypes of HIV type 1 in Republic of Congo. AIDS Res Hum Retroviruses. 2000;16:613–9.PubMedGoogle Scholar
  127. 127.
    Candotti D, Tareau C, Barin F, Joberty C, Rosenheim M, M’Pele P, et al. Genetic subtyping and V3 serotyping of HIV type 1 isolates in Congo. AIDS Res Hum Retroviruses. 1999;15:309–14.PubMedGoogle Scholar
  128. 128.
    Niama FR, Toure-Kane C, Vidal N, Obengui P, Bikandou B, Ndoundou Nkodia MY, et al. HIV-1 subtypes and recombinants in the Republic of Congo. Infect Genet Evol. 2006;6:337–43.PubMedGoogle Scholar
  129. 129.
    Caron M, Makuwa M, Souquière S, Descamps D, Brun-Vézinet F, Kazanji M. Human immunodeficiency virus type 1 seroprevalence and antiretroviral drug resistance-associated mutations in miners in Gabon, central Africa. AIDS Res Hum Retroviruses. 2008;24:1225–8.PubMedGoogle Scholar
  130. 130.
    Mintsa-Ndong A, Caron M, Plantier JC, Makuwa M, Le Hello S, Courgnaud V, et al. High HIV Type 1 prevalence and wide genetic diversity with dominance of recombinant strains but low level of antiretroviral drug-resistance mutations in untreated patients in northeast Gabon, Central Africa. AIDS Res Hum Retroviruses. 2009;25:411–8.PubMedGoogle Scholar
  131. 131.
    Burda ST, Viswanath R, Zhao J, Kinge T, Anyangwe C, Tinyami ET, et al. HIV-1 reverse transcriptase drug-resistance mutations in chronically infected individuals receiving or naïve to HAART in Cameroon. J Med Virol. 2010;82:187–96.PubMedPubMedCentralGoogle Scholar
  132. 132.
    Charpentier C, Gody JC, Tisserand P, Matta M, Fournier J, Mbitikon O, et al. Usefulness of a genotypic resistance test using dried blood spot specimens in African HIV-infected children with virological failure according to the 2010-revised WHO criteria. Arch Virol. 2011;156:1603–6.PubMedGoogle Scholar
  133. 133.
    Ragupathy V, Zhao J, Wood O, Tang S, Lee S, Nyambi P, et al. Identification of new, emerging HIV-1 unique recombinant forms and drug resistant viruses circulating in Cameroon. Virol J. 2011;8:185.PubMedPubMedCentralGoogle Scholar
  134. 134.
    Ceccarelli L, Salpini R, Moudourou S, Cento V, Santoro MM, Fokam J, et al. Characterization of drug resistance mutations in naive and ART-treated patients infected with HIV-1 in Yaounde, Cameroon. J Med Virol. 2012;84:721–7.PubMedGoogle Scholar
  135. 135.
    Fokam J, Salpini R, Santoro MM, Cento V, Perno CF, Colizzi V, et al. Drug resistance among drug-naive and first-line antiretroviral treatment-failing children in Cameroon. Pediatr Infect Dis J. 2011;30:1062–8.PubMedGoogle Scholar
  136. 136.
    Péré H, Charpentier C, Mbelesso P, Dandy M, Matta M, Moussa S, et al. Virological response and resistance profiles after 24 months of first-line antiretroviral treatment in adults living in Bangui, Central African Republic. AIDS Res Hum Retroviruses. 2012;28:315–23.PubMedGoogle Scholar
  137. 137.
    Charpentier C, Gody JC, Tisserand P, Matta M, Péré H, Fournier J, et al. Surveillance of antiretroviral drug resistance mutations in untreated young children living in the Central African Republic. Antivir Ther. 2011;16:1347–50.PubMedGoogle Scholar
  138. 138.
    Charpentier C, Gody JC, Mbitikon O, Moussa S, Matta M, Péré H, et al. Virological response and resistance profiles after 18 to 30 months of first- or second-/third-line antiretroviral treatment: a cross-sectional evaluation in HIV type 1-infected children living in the Central African Republic. AIDS Res Hum Retroviruses. 2012;28:87–94.PubMedGoogle Scholar
  139. 139.
    Vergne L, Malonga-Mouellet G, Mistoul I, Mavoungou R, Mansaray H, Peeters M, et al. Resistance to antiretroviral treatment in Gabon: need for implementation of guidelines on antiretroviral therapy use and HIV-1 drug resistance monitoring in developing countries. J Acquir Immune Defic Syndr. 2002;1:165–8.Google Scholar
  140. 140.
    Assam-Assam JP, Penlap VB, Cho-Ngwa F, Tedom JC, Ane-Anyangwe I, Titanji VP. Mycobacterium tuberculosis complex drug resistance pattern and identification of species causing tuberculosis in the West and Centre regions of Cameroon. BMC Infect Dis. 2011;11:94.PubMedPubMedCentralGoogle Scholar
  141. 141.
    Bercion R, Kuaban C. Initial resistance to antituberculosis drugs in Yaounde, Cameroon in 1995. Int J Tuberc Lung Dis. 1997;1:110–4.PubMedGoogle Scholar
  142. 142.
    Kassa-Kelembho E, Bobossi-Serengbe G, Takeng EC, Nambea-Koisse TB, Yapou F, Talarmin A. Surveillance of drug-resistant childhood tuberculosis in Bangui, Central African Republic. Int J Tuberc Lung Dis. 2004;8:574–8.PubMedGoogle Scholar
  143. 143.
    Diguimbaye C, Hilty M, Ngandolo R, Mahamat HH, Pfyffer GE, Baggi F, et al. Molecular characterization and drug resistance testing of Mycobacterium tuberculosis isolates from Chad. J Clin Microbiol. 2006;44:1575–7.PubMedPubMedCentralGoogle Scholar
  144. 144.
    Abdelhadi O, Ndokaïn J, Ali MM, Friocourt V, Mortier E, Heym B. Drug resistance testing of Mycobacterium tuberculosis isolates from sputum in Chad. Bull Soc Pathol Exot. 2012;105:16–22.PubMedGoogle Scholar
  145. 145.
    Minime-Lingoupou F, Pierre-Audigier C, Kassa-Kélémbho E, Barilone N, Zandanga G, Rauzier J, et al. Rapid identification of multidrug-resistant tuberculosis isolates in treatment failure or relapse patients in Bangui, Central African Republic. Int J Tuberc Lung Dis. 2010;14:782–5.PubMedGoogle Scholar
  146. 146.
    Kabedi MJ, Kashongwe M, Kayembe JM, Mumba Ngoyi D, Mampasi P, Mbaya P, et al. Primary resistance of Mycobacterium tuberculosis to anti-tuberculosis drugs in Kinshasa, (DRC). Bull Soc Pathol Exot. 2007;100:275–6.PubMedGoogle Scholar
  147. 147.
    Mounguengui D, Ondounda M, Mandji Lawson JM, Fabre M, Gaudong L, Mangouka L, et al. Multi-resistant tuberculosis at the hôpital d’instruction des armées de Libreville (Gabon) about 16 cases. Bull Soc Pathol Exot. 2012;105:1–4.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • S. Janssen
    • 1
    • 2
    • 3
    • 4
  • M. A. M. Huson
    • 1
    • 3
  • S. Bélard
    • 1
    • 3
    • 4
  • S. Stolp
    • 1
    • 3
  • N. Kapata
    • 5
    • 6
  • M. Bates
    • 6
    • 7
  • M. van Vugt
    • 1
    • 4
  • M. P. Grobusch
    • 1
    • 2
    • 3
    • 4
  1. 1.Department of Infectious Diseases, Division of Internal Medicine, Center of Tropical Medicine and Travel MedicineAcademic Medical Center, University of AmsterdamAmsterdamThe Netherlands
  2. 2.Institute of Tropical MedicineUniversity of TübingenTübingenGermany
  3. 3.Centre de Recherches Médicales de Lambaréné (CERMEL)LambarénéGabon
  4. 4.Institute of Infectious Diseases and Molecular MedicineUniversity of Cape TownCape TownSouth Africa
  5. 5.National TB and Leprosy Control Program, Ministry of HealthLusakaZambia
  6. 6.UNZA-UCLMS Research & Training ProgrammeUniversity Teaching HospitalLusakaZambia
  7. 7.Department of Infection, Division of Infection and ImmunityUniversity College LondonLondonUK

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