Drug Resistance Surveillance in Resource-Poor Settings: Current Methods and Considerations for TB, HIV, and Malaria

Bethany L. Hedt Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts; Department of Global Health and Social Medicine, Harvard Medical School, Boston, Massachusetts; Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Global Health Equity, Brigham and Women's Hospital, Boston, Massachusetts; Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts

Search for other papers by Bethany L. Hedt in
Current site
Google Scholar
PubMed
Close
,
Miriam K. Laufer Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts; Department of Global Health and Social Medicine, Harvard Medical School, Boston, Massachusetts; Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Global Health Equity, Brigham and Women's Hospital, Boston, Massachusetts; Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts

Search for other papers by Miriam K. Laufer in
Current site
Google Scholar
PubMed
Close
, and
Ted Cohen Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts; Department of Global Health and Social Medicine, Harvard Medical School, Boston, Massachusetts; Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Division of Global Health Equity, Brigham and Women's Hospital, Boston, Massachusetts; Department of Epidemiology, Harvard School of Public Health, Boston, Massachusetts

Search for other papers by Ted Cohen in
Current site
Google Scholar
PubMed
Close
Restricted access

In resource-constrained environments, monitoring the occurrence of tuberculosis (TB), human immunodeficiency virus (HIV), or malaria resistant to the limited number of available drugs is essential for national treatment program success. Countries with limited resources and technical capacity rely on survey designs and methods that are simple and easily integrated into routine clinical activities to minimize the impact on overburdened clinics. This paper reviews the most commonly used methods for drug-resistance surveillance of TB, HIV, and malaria and discusses the strengths and limitations of these different strategies.

Author Notes

*Address correspondence to Bethany L. Hedt, Harvard School of Public Health, 677 Huntington Ave., Boston, MA 02115. E-mail: bethhedt@gmail.com

Financial support: B.L.H. received support from National Institutes of Health Grant T32 AI007358. M.K.L. received support from National Institutes of Health Grants K23AI059316 and R34AI079315 and the Doris Duke Charitable Foundation. T.C. received support from National Institutes of Health Grant U54 GM088558.

Authors' addresses: Bethany L. Hedt, Department of Biostatistics, Harvard School of Public Health, Boston, MA, and Department of Global Health and Social Medicine, Harvard Medical School, Boston, MA, E-mail: bhedt@hsph.harvard.edu. Miriam K. Laufer, Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, MD, E-mail: mlaufer@medicine.umaryland.edu. Ted Cohen, Division of Global Health Equity, Brigham and Women's Hospital, Boston, MA and Department of Epidemiology, Harvard School of Public Health, Boston, MA, E-mail: tcohen@hsph.harvard.edu.

  • 1.

    Roll Back Malaria, 2008. Executive Summary: The Global Malaria Action Plan. Available at: http://rbm.who.int/gmap/0-5.pdf. Accessed October 6, 2009.

  • 2.

    The Joint United Nations Programme on HIV/AIDS (UNAIDS), 2008. '08 Report on the Global AIDS Epidemic. Available at: http://data.unaids.org/pub/GlobalReport/2008/jc1510_2008globalreport_en.pdf. Accessed October 6, 2009.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    World Health Organization, 2008. World Malaria Report 2008. Available at: http://apps.who.int/malaria/wmr2008/malaria2008.pdf. Accessed October 6, 2009.

  • 4.

    World Health Organization, 2008. Global Tuberculosis Control 2008: Surveillance, Financing and Planning. Available at: http://www.who.int/tb/publications/global_report/2008/. Accessed October 6, 2009.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    UNAIDS, 2009. 2008 UNAIDS Annual Report: Towards Universal Access. Available at: http://data.unaids.org/pub/Report/2009/jc1736_2008_annual_report_en.pdf. Accessed October 6, 2009.

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

    Bennett DE, Bertagnolio S, Sutherland D, Gilks CF, 2008. The World Health Organization's global strategy for prevention and assessment of HIV Drug resistance. Antivir Ther 13 (Suppl 2): 1–13.

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

    Bennett DE, Myatt M, Bertagnolio S, Sutherland D, Gilks CF, 2008. Recommendations for surveillance of transmitted drug resistance in countries scaling up antiretroviral treatment. Antivir Ther 13 (Suppl 2): 25–36.

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

    Jordan MR, Bennett DE, Bertagnolio S, Gilks CF, Sutherland D, 2008. World Health Organization surveys to monitor HIV Drug resistance prevention and associated factors in sentinel antiretroviral treatment sites. Antivir Ther 13 (Suppl 2): 15–23.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    World Health Organization, 2008. HIV Drug Resistance Early Warning Indicators: World Health Organization Indicators to Monitor HIV Drug Resistance Prevention at Antiretroviral Treatment Sites. Geneva, Switzerland: World Health Organization.

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

    World Health Organization, 2009. Methods for Surveillance of Antimalarial Drug Efficacy. Available at: http://apps.who.int/malaria/docs/drugresistance/Protocol2009.pdf. Accessed October 7, 2009.

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

    World Health Organization, 2009. Guidelines for Surveillance of Drug Resistance in Tuberculosis, 4th ed. Available at: http://whqlibdoc.who.int/publications/2009/9789241598675_eng.pdf. Accessed March 31, 2010.

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

    World Health Organization, 2003. Treatment of Tuberculosis: Guidelines for National Treatment Programs. Available at: http://whqlibdoc.who.int/hq/2003/WHO_CDS_TB_2003.313_eng.pdf. Accessed March 1, 2010.

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

    World Health Organization, 2006. The Global Plan to Stop TB 2006–2015: Actions for Life, Towards a World Free of Tuberculosis. Available at: http://www.stoptb.org/globalplan/assets/documents/GlobalPlanFinal.pdf. Accessed March 1, 2010.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Shafer RW, Rhee S, Pillay D, Miller V, Sandstrom P, Schapiro JM, Kuritzkes DR, Bennett D, 2007. HIV-1 protease and reverse transcriptase mutations for drug resistance surveillance. AIDS 21: 215–223.

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

    Bennett DE, Camacho RJ, Otelea D, Kuritzkes DR, Fleury H, Kiuchi M, Heneine W, Kantor R, Jordan MR, Schapiro JM, Vandamme AM, Sandstrom P, Boucher CAB, van de Vijver D, Rhee S, Liu TF, Pillay D, Shafer RW, 2009. Drug resistance mutations for surveillance of transmitted HIV-1 drug-resistance: 2009 update. PLoS One 4: e4274.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Myatt M, Bennett DE, 2008. A novel sequential sampling technique for the surveillance of transmitted HIV drug resistance by cross-sectional survey for use in low resource settings. Antivir Ther 13 (Suppl 2): 37–48.

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

    World Health Organization, 2006. Guidelines for the Treatment of Malaria. Available at: http://whqlibdoc.who.int/publications/2006/9241546948_eng_full.pdf. Accessed March 1, 2010.

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

    Djimde AA, Duombo OK, Traore O, Guindo AB, Kayentao K, Diourte Y, Niare-Doumbo S, Coulibaly D, Kone AK, Cissoko Y, Tekete M, Fofana B, Dicko A, Diallo DA, Wellems TW, Kwiatkowski D, Plowe CV, 2003. Clearance of drug-resistant parasites as a model for protective immunity in Plasmodium falciparum malaria. Am J Trop Med Hyg 69: 558–563.

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

    Koepfli C, Mueller I, Marfurt J, Goroti M, Sie A, Oa O et al., 2009. Evaluation of Plasmodium vivax genotyping markers for molecular monitoring in clinical trials. J Infect Dis 199: 1074–1080.

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

    Wells TNC, Alonso PL, Gutteridge WE, 2009. New medicines to improve control and contribute to the eradication of malaria. Natl Rev 8: 879–891.

  • 21.

    Wright A, Zignol M, Van Deun A, Falzon D, Gerges SR, Feldman K, Hoffner S, Drobniewski F, Barrera L, van Soolingen D, 2009. Epidemiology of antituberculosis drug resistance 2002–07: an updated analysis of the Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Lancet 373: 1861–1873.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Abegaz WE, Grossman Z, Wolday D, Ram D, Kaplan J, Sibide K, Wuhib T, Ismael S, Nkengasong J, Mekonen T, Berhanu W, Messele T, Lulseged S, Maayan S, Mengitsu Y, 2008. Threshold survey evaluating transmitted HIV drug resistance among public antenatal clinic clients in Addis Ababa, Ethiopia. Antivir Ther 13 (Suppl 2): 89–94.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Hedt BL, Wadonda-Kabondo N, Makombe S, Harries AD, Schouten EJ, Limbambala E, Hochesang M, Aberle-Grasse J, Kamoto K, 2008. Early warning indicators for HIV drug resistance in Malawi. Antivir Ther 13 (Suppl 2): 69–75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Kamoto K, Aberle-Grass J, Malawi HIV Drug Resistance Task Force , 2008. Surveillance of transmitted HIV drug resistance with the World Health Organization threshold survey method in Lilongwe, Malawi. Antivir Ther 13 (Suppl 2): 83–87.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Maphalala G, Okello V, Mndzebele S, Gwebu P, Mulima N, Dlamini S, Nhlabatsi B, Ginindza T, Ghebrenegus Y, Ntilivamunda A, Mwanyumba F, Ledwaba J, Pillay V, Bennett DE, 2008. Surveillance of transmitted HIV drug resistance in the Manzini–Mbabane corridor, Swaziland, in 2006. Antivir Ther 13 (Suppl 2): 95–100.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Nguyen HT, Duc NB, Shrivastava R, Tran TH, Nguyen TA, Thang PH, McNicholl JM, Leelawiwat W, Chonwattana W, Sidibe K, Fujita M, Luu CMT, Kakkar R, Bennett DE, Kaplan J, Cosimi L, Wolfe MI, 2008. HIV drug resistance threshold survey suing specimens from voluntary counseling and testing sites in Hanoi, Vietnam. Antivir Ther 13 (Suppl 2): 115–121.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Pillay V, Ledwaba J, Hunt G, Rakgotho M, Singh B, Makubalo L, Bennett DE, Puren A, Morris L, 2008. Antiretroviral drug resistance surveillance among drug-naive HIV-1–infected individuals in Gauteng Province, South Africa in 2002 and 2004. Antivir Ther 13 (Suppl 2): 101–107.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Sirivichayakul S, Phanuphak P, Pankam T, O-Charoen R, Sutherland D, Ruxrungtham K, 2008. HIV drug resistance transmission threshold survey in Bangkok, Thailand. Antivir Ther 13 (Suppl 2): 109–113.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Somi GR, Kibuka T, Diallo K, Tuhuma T, Bennett DE, Yang C, Kagoma C, Lyamuya EF, Swai RO, Kassim S, 2008. Surveillance of transmitted HIV drug resistance among women attending antenatal clinics in Dar es Salaam, Tanzania. Antivir Ther 13 (Suppl 2): 77–82.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Castillo J, Comegna M, Quijada W, Jauvin V, Pinson P, Masquelier B, Fleury H, Castro E, 2009. Surveillance of HIV type 1 drug among naïve patients from Venezuela. AIDS Res Hum Retroviruses 25: 1329–1333.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Inocencio LA, Pereira AA, Sucupira MC, Fernandez JC, Jorge CP, Souza DF, Fink HT, Diaz RS, Becker IM, Suffert TA, Arruda MB, Macedo O, Simão MBG, Tanuri A, 2009. Brazilian network for HIV drug resistance surveillance: a survey of individuals recently diagnosed with HIV. J Int AIDS Soc 12. doi:10.1186/1758-2652-12-20.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Ndembi N, Lyagoba F, Kushemererma G, Serwanga J, Katongole-Mbidde E, Grosskurth H, Kaleebu P, 2008. Transmitted antiretroviral drug resistance surveillance among new HIV type 1-diagnosed women attending antenatal clinic in Entebbe, Uganda. AIDS Res Hum Retroviruses 24: 889–895.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    World Health Organization, 2009. Global Tuberculosis Control 2008: Epidemiology, Financing and Planning. Available at: http://www.who.int/tb/publications/global_report/2009/en/index.html. Accessed March 1, 2010.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Zhang J, Kang D, Fu J, Sun X, Lin B, Bi Z, Nkengasong JN, Yang C, 2010. Surveillance of transmitted HIV type 1 drug resistance in newly diagnosed HIV type 1-infected patients in Shandong Province, China. AIDS Res Hum Retroviruses 26: 99–103.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Price RN, Dorsey G, Ashley EA, Barnes KI, Baird JK, d'Alessandro U, Guerin PJ, Laufer MK, Naidoo I, Nosten F, Olliaro P, Plowe CV, Ringwald P, Sibley CH, Stepniewska K, White NJ, 2007. World Antimalarial Resistance Network I: clinical efficacy of antimalarial drugs. Malar J 6: 119.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Guerin PJ, Bates SJ, Sibley CH, 2009. Global resistance surveillance: ensuring antimalarial efficacy in the future. Curr Opin Infect Dis 22: 593–600.

  • 37.

    Laufer MK, Djimde AA, Plowe CV, 2007. Monitoring and deterring drug-resistant malaria in the era of combination therapy. Am J Trop Med Hyg 77 (Suppl 6): 160–169.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Cohen T, Hedt BL, Pagano M, 2010. Estimating the magnitude and direction of bias in tuberculosis drug resistance surveys conducted only in the public sector: a simulation study. BMC Public Health 10. doi:10.1186/1471-2458-10-355.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Lillebaek T, Dirksen A, Baess I, Strunge B, Thomsen VO, Andersen AB, 2002. Molecular evidence of the endogenous reactivation of Mycobacterium tuberculosis after 33 years of latent infection. J Infect Dis 185: 401–404.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 373 317 32
Full Text Views 334 18 1
PDF Downloads 121 18 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save