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Appendix C
Partners In Health White Paper—Stemming the Tide of Multidrug-Resistant Tuberculosis: Major Barriers to Addressing the Growing Epidemic
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Addressing the Threat of Drug-Resistant Tuberculosis: A Realistic Assessment of the Challenge - Workshop Summary
STEMMING THE TIDE OF MULTIDRUG-RESISTANT TUBERCULOSIS:
MAJOR BARRIERS TO ADDRESSING THE GROWING EPIDEMIC
A WHITE PAPER FOR THE INSTITUTE OF MEDICINE OF THE NATIONAL ACADEMIES
HARVARD MEDICAL SCHOOL
■
PARTNERS IN HEALTH
■
FRANÇOIS–XAVIER BAGNOUD CENTER FOR HEALTH AND HUMAN RIGHTS
■
BRIGHAM AND WOMEN’S HOSPITAL
November 2008
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AUTHORS
Lead Authors
Salmaan Keshavjee
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital/
Partners In Health
Kwonjune Seung
Division of Global Health Equity, Brigham and Women’s Hospital/
Partners In Health
Contributing Authors
Rajesh Gupta
Stanford University School of Medicine
Tom Nicholson
Partners In Health
Julie Rosenberg Talbot
Division of Global Health Equity, Brigham and Women’s Hospital
Chris Vanderwarker
University of Washington
Paul Zintl
Partners In Health/
Department of Global Health and Social Medicine, Harvard Medical School
Other Contributors:
Mercedes Becerra
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital
Paul Farmer
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital/
Partners In Health
Jennifer Furin
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital/
Partners In Health
Stephen Hallisey
Department of Global Health Equity, Brigham and Women’s Hospital
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Amy Judd
Division of Global Health Equity, Brigham and Women’s Hospital
Kathryn Kempton
Partners In Health
David Kim
Division of Global Health Equity, Brigham and Women’s Hospital
Jim Yong Kim
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital/
Harvard School of Public Health/
François–Xavier Bagnoud Center For Health And Human Rights/
Partners In Health
Carole Mitnick
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital
Joia Mukherjee
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital/
Partners In Health
Edward Nardell
Harvard School of Public Health/
Division of Global Health Equity, Brigham and Women’s Hospital
Catherine Oettinger
Partners In Health
Sonya Shin
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital
Valerie Varco
Division of Global Health Equity, Brigham and Women’s Hospital
Rebecca Weintraub
Department of Global Health and Social Medicine, Harvard Medical School/
Division of Global Health Equity, Brigham and Women’s Hospital
In-depth Interviews
Shalala Akhmedova
Coordinator, International Committee of Red Cross (Azerbaijan)
Peter Cegielski
Unites States Centers for Disease Control and Prevention
Agnes Gebhard
KNCV Tuberculosis Foundation
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Ogtay Gozalov
Regional Tuberculosis Control Program, South Caucasus, Azerbaijan
Mark Harrington
Treatment Action Group
Phil Hopewell
University of California San Francisco
Vaira Leimane
WHO Collaborating Centre for Research and Training in Management of MDR-TB (Latvia)
Joël Keravec
Management Sciences for Health/Brazil
Laura Jacobus
Jacobus Pharmaceutical Co., Inc.
Moses Joloba
National Tuberculosis Program, Uganda
Fabienne Jouberton
Global Fund to fight AIDS, Tuberculosis and Malaria
Robert Matiru
Global Drug Facility, STOP TB Partnership
Fuad Mirzayev
World Health Organization
Pierre-Yves Norval
World Health Organization
Madhukar Pai
McGill University
C. N. Paramasivan
Foundation for Innovative New Diagnostics
Dmitri Pashkeevich
Office of the Special Representative of the WHO Director-General in Russia
Trevor Peters
Clinton Foundation
Alexei Prorekhin
Partners In Health, Russia
Steven Reynolds
Unites States Centers for Disease Control and Prevention--Uganda
John Ridderhof
Unites States Centers for Disease Control and Prevention
William Rodriguez
Brigham and Women’s Hospital/Harvard Medical School
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Tamara Russell
Eli Lilly Global Manufacturing
Nina Schwalbe
Global Alliance for Vaccines and Immunization
Alex Sloutsky
Massachusetts State Laboratory Institute/University of Massachusetts
Thelma Tupasi
Tropical Disease Foundation, the Philippines
Karin Weyer
World Health Organization
Abigail Wright
World Health Organization
Acknowledgement of Support
Jaime Bayona
Socios En Salud
Ernesto Jaramillo
World Health Organization
Kitty Lambregts
KNCV Tuberculosis Foundation
Oksana Ponomarenko
Partners In Health, Russia
Mario Raviglione
World Health Organization
Peter Stephens
IMS Health
The authors would like to thank the many other colleagues who participated in numerous discussions on the topics covered in this document over the last year.
The views expressed in this document are solely those of the authors and are not meant to represent the position of any individual who was interviewed or gave support to this project, nor the Institute of Medicine, Harvard Medical School, Partners In Health, the François-Xavier Bagnoud Center for Health Human Rights or Brigham and Women’s Hospital.
Cover Photo: Open Society Institute/Pep Bonet
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TABLE OF CONTENTS
EXECUTIVE SUMMARY
1
SPECIFIC RECOMMENDATIONS:
2
GLOSSARY OF TERMS:
4
Section I: THE PROBLEM OF DRUG-RESISTANT TUBERCULOSIS
5
1 Introduction
5
2 A General Framework for Understanding Barriers to MDR-TB Scale-up
9
Section II: DIAGNOSIS OF MDR-TB
11
1 Introduction
11
1.1 The inadequacies of sputum smear microscopy
11
1.2 Expanding Laboratory Capacity
12
2 The Anatomy of a Laboratory Network
14
2.1 TB laboratory networks
14
2.2 Third-party laboratories
16
2.3 Drug resistance surveillance (DRS)
16
2.4 Capacity gap
18
2.5 Financing gap
19
3 Laboratory Capacity Building
20
3.1 Fragmented organization and a poorly defined role in TB control
22
3.2 Laboratory technical assistance
22
3.3 Human resources
24
3.4 The referral network
26
3.5 Data management
27
3.6 Quality assurance
27
3.7 Lessons learned from the experiences of Peru and Lesotho
30
4 New TB Technologies and the Need for Point-of-Care Testing
31
5 Recommendations
33
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Section III: MDR-TB DRUG SUPPLY
35
1 Introduction
35
2 The GLC Initiative: Actors and Responsibilities
36
2.1 The Green Light Committee (GLC)
36
2.2 The Global Drug Facility (GDF)
38
2.3 Procurement agent
39
2.4 The WHO Essential Drugs Monitoring (EDM) prequalification system
40
2.5 UNITAID
40
3 The GLC Initiative: Institutional Barriers
43
3.1 Single procurement agent, the GDF, and transparency
43
3.2 Prequalification of second-line anti-TB drugs has been slow at WHO
44
4 Drug Supply and Engagement of Drug Manufacturers in MDR-TB Response
49
4.1 MDR-TB projects working outside the GLC initiative
49
4.2 Available drug supply through GLC initiative
51
4.3 Incentives and disincentives for entry into the second-line anti-TB drug market
52
4.4 New therapies for MDR-TB
54
4.5 Governmental health authorities and high quality second-line drugs
56
4.6 Manufacturers in high-burden countries
56
5 Redefining the Paradigm of the GLC Mechanism
58
6 Recommendations
60
Section IV: MDR-TB TREATMENT DELIVERY
62
1 Introduction
62
2 Shifting the Paradigm From “Pilot” Projects to an Integrated Strategy
63
3 Addressing the MDR-TB Treatment Implementation Gap
65
4 Expanding Models of Care
68
4.1 Community-based models for MDR-TB treatment
68
4.2 Participation of the private sector
72
4.3 Transmission control
73
5 Recommendations
76
Section V: References
78
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EXECUTIVE SUMMARY
Every year nearly 500,000 people worldwide fall ill from newly-acquired disease caused by multidrug-resistant tuberculosis (MDR-TB), adding to an estimated global burden of at least 1.5 million prevalent cases. This infectious disease is spread through the air and is caused by strains of Mycobacterium tuberculosis that are resistant to the two most effective first-line anti-tuberculosis drugs. Before they die from the disease, people infected with MDR-TB often transmit the mycobacterium to others. More ominously, tuberculosis strains now deemed extensively drug-resistant (XDR-TB) threaten the progress made to date in the treatment of resistant disease and necessitate an urgent call to action. Though aggressive treatment with second-line drugs has yielded a range of positive outcomes for patients with XDR-TB, the widespread emergence of totally drug-resistant strains (TDR-TB) would return us to the preantibiotic era.
Confronting MDR-TB is a core goal stated in the WHO’s Global Plan to Stop TB: 2006-2015. Under the original plan, at least 800,000 people with active MDR-TB were to be treated by 2015. A subsequent revision, reflecting the concern over XDR-TB, made a more ambitious call for universal access to treatment for all active MDR-TB patients; this will require the treatment of nearly 1.6 million patients by 2015. At present, only ten percent of new MDR-TB cases are treated each year, and less than two percent are receiving verifiable, quality-assured, second-line anti-TB drugs through WHO’s Green Light Committee (GLC) mechanism. Preventing the further emergence of strains of tuberculosis with broad-spectrum resistance—including those resistant to all first- and second-line anti-tuberculosis drugs—is dependent upon identifying and addressing barriers to effective diagnosis and treatment of drug-resistant tuberculosis without delay.
While multidrug-resistant strains of tuberculosis may have first emerged from inadequate treatment and control programs in the recent past, continued spread of this airborne pathogen is directly affected by the following barriers to large-scale, effective treatment delivery:
Exceedingly limited capacity to rapidly diagnose drug-resistant TB. True point-of-care testing is practically nonexistent, especially in the areas with the highest tuberculosis burden.
Limited supply of quality-assured second-line anti-tuberculosis drugs. The current supply is insufficient, even for the estimated two percent of MDR-TB patients being treated through the GLC mechanism. This is exacerbated by limited demand for quality-assured second-line anti-tuberculosis drugs in countries with high burdens of MDR-TB. These countries are using local manufacturers who often do not meet quality-assurance standards as defined by the WHO.
Ambiguous messaging about the importance of integration of MDR-TB into national tuberculosis control programs, perpetuated by a “pilot-program” mentality that has not been encouraging a push for universal access.
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Inadequate mechanisms for delivering technical assistance to countries in a manner that sufficiently addresses the need and builds local capacity to effectively and safely treat and manage MDR-TB.
Lack of focus on interrupting transmission of the tuberculosis bacilli in congregate settings both in the community and in institutions such as hospitals, clinics, and prisons.
This paper provides several recommendations to facilitate the expansion of global treatment and prevention of multidrug-resistant tuberculosis. These include: promoting universal access to treatment as part of national tuberculosis control programs; improving and expanding laboratory capacity, including rapid point-of-service testing; reforming the current procurement system to ensure an adequate and accessible supply of quality-assured second-line drugs; providing ongoing, on-site technical assistance; and expanding the delivery of ambulatory-based MDR-TB treatment. It also includes recommendations concerning the development of effective transmission-control programs in resource-limited settings.
SPECIFIC RECOMMENDATIONS:
Diagnostics
Sustainable funding from bilateral and multilateral donors must be increased to support construction of in-country drug-sensitivity testing/rapid-testing laboratories and ongoing external quality assessments by supranational reference laboratories.
Creation of a system of long-term on-site technical assistance would help countries build and/or rapidly expand their capacity to perform mycobacterial culture, DST, and rapid molecular genetic tests for drug-resistant tuberculosis.
In-country laboratory networks for: specimen transport, data management, and certification and coordination of private laboratories need improvement.
Use of excess laboratory capacity for mycobacterial culture and drug-susceptibility testing in wealthy nations should be encouraged while laboratories are being built in poorer regions.
Priority must be given to research on—and funding for—the immediate development and rapid deployment of point-of-care testing for drug-susceptible and drug-resistant tuberculosis.
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109 Featherstone D, Brown, D and R Sanders. Development of the Global Measles Laboratory Network. J Infect Dis, 2003; 187 Suppl 1: S264-9.
110 Cohen GM. Access to diagnostics in support of HIV/AIDS and tuberculosis treatment in developing countries. Aids 2007; 21 Suppl 4: S81-7.
111 Diagnostics for Tuberculosis: Global Demand and Market Potential. World Health Organization: Geneva, 2007.
112 Maher D, Dye C, Floyd K, et al. Planning to improve global health: the next decade of tuberculosis control. Bull World Health Organ 2007. 85(5): p. 341-7.
113 Ridderhof, JC, van Deun, A, Kam, KM, et al., Roles of laboratories and laboratory systems in effective tuberculosis programmes. Bull World Health Organ 2007; 85(5): 354-9.
114 Bates I and K Maitland. Are laboratory services coming of age in sub-Saharan Africa? Clin Infect Dis 2006; 42 (3): 383-4.
115 Muula AS and FC Maseko. Medical laboratory services in Africa deserve more. Clin Infect Dis 2006; 42(10): 1503.
116 Martin R, Hearn TL, Ridderhof J, et al. Implementation of a quality systems approach for laboratory practice in resource-constrained countries. Aids 2005. 19 Suppl 2: p. S59-65.
117 Dukes Hamilton, C, Sterling, TR, Blumberg HM, et al., Extensively drug-resistant tuberculosis: are we learning from history or repeating it? Clin Infect Dis 2007; 45(3): 338-42.
118 Harries AD, Zachariah R, Bergstrom K, et al. Human resources for control of tuberculosis and HIV-associated tuberculosis. Int J Tuberc Lung Dis 2005. 9(2): p. 128-37.
119 Chen, L, Evans, T Anand S, et al. Human resources for health: overcoming the crisis. Lancet 2004; 364(9449): 1984-90.
120 Narasimhan V, Brown H, Pablos-Mendez, A, et al. Responding to the global human resources crisis. Lancet 2004. 363(9419): p. 1469-72.
121 Hanvoravongchai, P. Scaling up health workforces in response to critical shortages. Lancet 2007; 370(9605): 2080-1.
122 Mullan F and S Frehywot. Non-physician clinicians in 47 sub-Saharan African countries. Lancet 2007; 370(9605): 2158-63.
123 Hongoro C and B McPake. How to bridge the gap in human resources for health. Lancet 2004; 364(9443): 1451-6.
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124 Yagui M, Perales MT, Asencios L, et al. Timely diagnosis of MDR-TB under program conditions: is rapid drug susceptibility testing sufficient? Int J Tuberc Lung Dis 2006. 10(8): p. 838-43.
125 Petti, CA, Polage CR, Quinn TC, et al. Laboratory medicine in Africa: a barrier to effective health care. Clin Infect Dis 2006; 42(3): 377-82.
126 Blaya JA and HS Fraser. Development, implementation and preliminary study of a PDA-based tuberculosis result collection system. AMIA Annu Symp Proc 2006: 41-5.
127 Blaya, JA, Shin SS, Yagui MJ, et al. A web-based laboratory information system to improve quality of care of tuberculosis patients in Peru: functional requirements, implementation and usage statistics. BMC Med Inform Decis Mak 2007; 7: 33.
128 Global Tuberculosis Control 2007. Surveillance, Planning, Financing. World Health Organization: Geneva, 2007.
129 Rojpibulstit M, Kanjanakiritamrong J and V Chongsuvivatwong. Patient and health system delays in the diagnosis of tuberculosis in Southern Thailand after health care reform. Int J Tuberc Lung Dis 2006; 10(4):422-428.
130 Lonnroth K, Thuong LM, Linh PD and VK Diwan. Delay and discontinuity—a survey of TB patients’ search of a diagnosis in a diversified health care system. Int J Tuberc Lung Dis 1999; 3:992-1000.
131 Liam CK and BG Tang. Delay in the diagnosis and treatment of pulmonary tuberculosis in patients attending a university teaching hospital. Int J Tuberc Lung Dis 1997; 1:326-332.
132 Rajeswari R, Chandrasekaran V, Suhadev M, Sivasubramaniam S, Sudha G and G Renu. Factors associated with patient and health system delays in the diagnosis of tuberculosis in South India. Int J Tuberc Lung Dis 2002; 6:789-795.
133 Cheng G, Tolhurst R, Li RZ, et al. Factors affecting delays in tuberculosis diagnosis in rural China: a case study in four counties in Shandong Province. Trop Med Int health 2005; 99:355-362.
134 Lorent N, Mugwaneza P, Mugabekazi J, Gasana M, Van Bastelaere S, Clerinx J, et al. Risk factors for delay in the diagnosis and treatment of tuberculosis at a referral hospital in Rwanda. Int J Tuberc Lung Dis 2008; 12(4):392-396.
135 World Health Organization/International Union Against Tuberculosis and Lung Disease. Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Anti-tuberculosis drug resistance in the world: report no. 4. Geneva, Switzerland: World Health Organization; 2008. Pg 14
136 Summary: Strategic Plans 2006 - 2015 of the Partnership, Working Group and Secretariat (Stop TB) http://www.stoptb.org/globalplan/plan_p3main.asp?p=3
137 The Global MDR-TB & XDR-TB Response Plan 2007-2008. In. Geneva: Stop TB Partnership; 2007. www.stoptb.org/resource_center/assets/documents/Global%20MDR-TB_and_%20XDR-TB_Response%20Plan_2007-08.pdf
138 Mattelli, Migliori, Cirillo, Centis, Girardi, Raviglioni Multi-drug Resistant and Extensively-drug Resistant Mycobacterium Tuberculosis: Epidemiology and Control. Future Drugs, 2007. Pg 865
139 World Health Organization, “Stop TB Partnership delivers treatments for 10 million people in six years” http://www.who.int/mediacentre/news/releases/2007/pr25/en/index.html
140 Interview with GDF, November 2007
141 Request for Proposals for second-line anti-TB Drugs Procurement Agent(s), August, 2006 Available: http://www.stoptb.org/gdf/newsevents/newsarchive.asp
142 Unitaid Homepage http://www.unitaid.eu
143 Unitaid Homepage http://www.unitaid.eu
144 Interviews with GLC representatives
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145 Tropical Disease Foundation, Manila, Philippines. Permission for use of this material was obtained from Dr. Thelma Tupasi.
146 Interviews with GLC-approved project procurement managers
147 WHO list of prequalified medicinal products. http://healthtech.who.int/pq/ Site accessed on August 12, 2008.
148 World Health Organzation. The Global MDR-TB and XDR-TB Response Plan. Geneva, Switzerland: World Health Organization; 2007. WHO/HTM/STB/2007.387.
149 TB infections by country, 2003, WHO estimate
150 Russian Ministry of Health and Social Development 2007
151 Russian Ministry of Health and Social Development 2007
152 From IMS Health, conveyed to the Drug Management Sub-Committee of the Stop TB Partnership, MDR-TB Working Group
153 Keravec J. Implementation of a National Program for TB Drugs Quality Assuaranc in Brazil, Projeto MSH/Rational Pharmaceutical Management Plus Program (RPM Plus) Rio de Janeiro, Brazil 2007.
154 Currently offered through GDF, though not listed on GDF 2006 chart of medications
155 Stop TB Partnership, Global Drug Facility Drugs, Diagnostics, and other TB supplies, list of 2nd line drugs. http://www.stoptb.org/gdf/drugsupply/drugs_available.asp#2nd%20Line%20Drugs
156 Gupta R, Kim JY, Espinal MA, et al. Responding to Market Failures in Tuberculosis Control. Science 2001 Aug 10;293(5532):1049-51.
157 Interview, GDF November 2007
158 Interviews with pharmaceutical industry representatives.
159 From IMS Health, conveyed to the Drug Management Sub-Committee of the Stop TB Partnership, MDR-TB Working Group. Cited with permission from IMS Health and the WHO.
160 Feuer C (2006) Tuberculosis research and development: A critical analysis. Treatment Action Group. Available: http://www.aidsinfonyc.org/tag/tbhiv/tbrandd.pdf. Accessed 7 October 2007
161 Glickman et al. “A Portfolio Model of Drug Development for Tuberculosis” Science. March 3, 2006. pg 1246.
162 Ginsberg, Ann. “Emerging Drugs for Active Tuberculosis” Seminars in Respiratory and Critical Care Medicine. 2008. 29(5)
163 Sacks, Leonard and Behrman, Rachel E. “Developing new drugs for the treatment of drug-resistant tuberculosis: a regulatory perspective” Tuberculosis (2008) 88 Suppl 1.
164 Mitnick CD et al. Randomized trials to optimize treatment of multidrug-resistant tuberculosis. PLoS Med 4(11): e292. doi:10.1371/journal.pmed.0040292
165 Glickman et al. “A Portfolio Model of Drug Development for Tuberculosis” Science. March 3, 2006. pg 1246.
166 Farlow, Letter to Science, February 23, 2007; in response to “A Portfolio Model of Drug Development for Tuberculosis” Science. March 3, 2006. pg 1246.
167 This workshop was convened in Cambridge, Massachusetts, USA on June 10 to 12, 2008, by partners of the MDR-TB Working Group of the Stop-TB Partnership. It was sponsored and organized by: Boston University School of Public Health, International Union Against TB & Lung Disease, KNCV Tuberculosis Foundation, MDR-TB Working Group of the Stop-TB Partnership, Médecins Sans Frontières, Partners In Health/Harvard Medical School, Potts Memorial Foundation, Treatment Action Group, World Health Organization.
168 Sun Q, Santoro MA, Meng Q, et al. Pharmaceutical Policy in China. Health Affairs 2008 Jul-Aug;27(4):1042-50.
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169 PSU Pharma Companiess May be Kept Out of Price Control for Now http://economictimes.indiatimes.com/Economy/PSU_pharma_cos_out_of_price_control/articleshow/3266374.cms
170 Ibid
171 Lilly MDR-TB Partnership Facts http://lillymdr-tb.com/facts.html
172 Interviews with Eli Lilly, Aspen Pharmacare October 2007- January 2008
173 Ibid.
174 Ibid.
175 Ibid.
176 Interviews with Eli Lilly, October 2007
177 Park SK, CT Kim and SD Song. Outcome of chemotherapy in 107 patients with pulmonary tuberculosis resistant to isoniazid and rifampicin. Int J Tuberc Lung Dis 1998. 2:877-884.
178 Telzak EE, Sepkowitz K, Alpert P, et al. Multidrug-resistant tuberculosis in patients in patients without HIV infection. New Engl J Med 1995.333:907-903.
179 Farmer PE, Kim JY, Mitnick CD, et al. Responding to Outbreaks of Multidrug-resistant tuberculosis: Introducing DOTS-Plus. In: Tuberculosis: A comprehensive International Approach, 2nd edition. 2000. Reichman L. and Hershfield ES ed. 447-69 Marcel Dekker, Inc. New York, NY.
180 Leimane V, Riekstina V, Holtz TH, et al. 2005. Clinical outcome of individualised treatment of multidrug-resistant tuberculosis in Latvia: a retrospective cohort study. Lancet 365(9456):318-26.
181 Farmer PE, Furin JJ and SS Shin. Managing multidrug-resistant tuberculosis. Journal of Respiratory Diseases 2000. 21(1), 53-56.
182 World Health Organization (2006). “Opportunities for Global Health Initiatives in the Health System Action Agenda,” Department of Health Policy, Development and Services Evidence and Information for Policy, World Health Organization (WHO) Working Paper No. 4.
183 Coker RJ, Atun RA and M McKee. Health-care system frailties and public health control of communicable disease on the European Union's new eastern border. Lancet 2004. 363(9418):1389-92.
184 See: Global Fund, eleventh board meeting (28-30 September 2005). “Report of the Technical Review Panel and the Secretariat on Round Five Proposals,” <http://www.theglobalfund.org/en/files/about/technical/report/Round_5_TRP_Report.pdf > (accessed 2 Jan 2008).
185 Opportunities for Global Health Initiatives in the Health System Action Agenda, Department of Health Policy, Development and Services Evidence and Information for Policy, World Health Organization (WHO) Working Paper No. 4. 2006.
186 Keshavjee S, Gelmanova I, Pasechnikov A, Mushustin S, Andreev Y, et al. “Treating Multi-Drug Resistant Tuberculosis in Tomsk, Russia: Developing programs that address the linkage between poverty and disease,” Ann N Y Acad Sci. 2007 Oct 22; epub ahead of print.
187 Keshavjee S, Seung K, Satti H, Furin J, Farmer P, Kim JY, Becerra M. Building capacity for multidrug-resistant tuberculosis treatment: health systems strengthening in Lesotho. Innovations 2007 Fall; 2(4):87-106.
188 World Health Organization. 1999. Global Tuberculosis Control, WHO Report 1999. Geneva: World Health Organization.
189 Nardell E. Tuberculosis in homeless, residential care facilities, prisons, nursing homes, and other close communities. Semin Respir Infect 1989.4:206.
190 Moore M, McCray E and I Onorato. Cross matching TB and AIDS registries: TB patients with HIV coinfection, United States, 1993-1994. Publ Health Rep 1999.114:269-77.
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191 Murray J. Tuberculosis and human immunodeficiency virus infections during the 1990s. Bull Int Union Tuberc Lung Dis 1991; 66:21-5.
192 Sumartojo, E. When tuberculosis treatment fails: a social behavioral account of patient adherence. Am Rev Respir Dis 1993. 147:1311-20.
193 World Health Organization/International Union Against Tuberculosis and Lung Disease. Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Anti-tuberculosis drug resistance in the world: report no. 4. Geneva, Switzerland: World Health Organization; 2008.
194 Gupta R, Kim JY, Espinal MA, et al. Responding to market failures in tuberculosis control. Science. 2001; 293: 1048-1051.
195 Nathanson E, Lambregts van Weezenbeek CSW, Rich MR, et al. Multidrug-resistant tuberculosis management in resource limited settings. Emerging Infectious Diseases. 2006; 12(9)1389-1397.
196 Leimane V, Riekstina V, Holtz TH, et al. Clinical outcome of individualised treatment of multidrug-resistant tuberculosis in Latvia: a retrospective cohort study. Lancet. 2005; 365(9456): 318-326.
197 Mitnick C, Bayona J, Palacios E, et al. Community-based treatment for multidrug-resistant tuberculosis in Lima, Peru. New England Journal of Medicine. 2003; 348(2): 119-28.
198 Tupasi T, Gupta R, Quelapio M, et al. Feasibility and cost-effectiveness of treating multidrug-resistant tuberculosis: a cohort study in the Philippines. PLOS Med. 2006; 3(9): e352.
199 World Health Organization/International Union Against Tuberculosis and Lung Disease. Global Project on Anti-Tuberculosis Drug Resistance Surveillance. Anti-tuberculosis drug resistance in the world: report no. 4. Geneva, Switzerland: World Health Organization; 2008.
200 World Health Organzation/Stop TB Partnership. Global Plan to Stop TB: 2006-2015. Geneva, Switzerland: World Health Organization; 2006. WHO/HTM/STB/2006.38.
201 Keshavjee S., Gelmanova I., Pasechnikov A., Mushustin S., Andreev Y., et al. Treating Multi-Drug Resistant Tuberculosis in Tomsk, Russia: Developing programs that address the linkage between poverty and disease. Ann N Y Acad Sci. 2007 Oct 22; epub ahead of print.
202 PEPFAR Homepage. http://www.pepfar.gov/pepfar/press/81964.htm. Accessed November 20, 2008.
203 World Health Organization. Azerbaijan Tuberculosis Profile. In: WHO; 2007.
204 Holley J, Akhundov O, Nolte E. Health care systems in transition: Azerbaijan. In. Edited by WHO Regional Office for Europe on behalf of the European Observatory on Health Systems and Policies. Copenhagen; 2004.
205 Gozalov O. phone interview. In. phone interview ed: Rosenberg, Julie; 2007.
206 Holley J, Akhundov O, Nolte E. Health care systems in transition: Azerbaijan. In. Edited by WHO Regional Office for Europe on behalf of the European Observatory on Health Systems and Policies. Copenhagen; 2004.
207 Coninx R, Pfyffer GE, Mathieu C, Savina D, Debacker M, Jafarov F, et al. Drug-resistant tuberculosis in prisons in Azerbaijan: case study. Bmj 1998,316:1423-1425.
208 Pfyffer GE, Strassle A, van Gorkum T, Portaels F, Rigouts L, Mathieu C, et al. Multidrug-resistant tuberculosis in prison inmates, Azerbaijan. Emerg Infect Dis 2001,7:855-861.
209 World Health Organization. Involving Private Practitioners in Tuberculosis Control: Issues, Interventions, and Emerging Policy Framework. Geneva, World Health Organization, 2001. WHO/CDS/TB/2001.285.
210 Uplekar MW, Rangan S. Private doctors and tuberculosis control in India. Tubercle and Lung Disease. 1993; 74:332-337.
211 Uplekar MW, Juvekar SK, Parande DB, et al. Tuberculosis management in private practice and its implications. Indian Journal of Tuberculosis. 1996; 43: 19-22.
212 Uplekar M, Juvekar S, Morankar S, et al. Tuberculosis patients and practitioners in private clinics in India. International Journal of Tuberculosis and Lung Disease. 1998; 2: 324-329.
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213 Singla N, Sharma PP, Singla R, Jain RC. Survey of knowledge, attitudes and practices for tuberculosis among general practitioners in Delhi, India. International Journal of Tuberculosis and Lung Disease. 1998; 2: 384-389.
214 Kimerling ME, The Russian equation: an evolving paradigm in tuberculosis control. Int J Tuberc Lung Dis 2000. 4(12 Suppl 2): p. S160-7.
215 Willingham FF, Schmitz TL, Contreras M, et al. Hospital control and multidrug-resistant pulmonary tuberculosis in female patients, Lima, Peru. Emerging Infectious Diseases 2001. 7(1): p. 123-127.
216 Gelmanova IY, Keshavjee S, Golubchikova VT, Berezina VI, Strelis AK, Yanova GV, Atwood S, Murray M. Barriers to successful tuberculosis treatment in Tomsk, Russia; non-adherence, default, and the acquisition of multi-drug resistance. Bull WHO Sep; 85(9): 703–711.
217 Li X, Zhang Y, Shen X, Shen G, Gui X, Sun B, Mei J, Deriemer K, Small PM, Gao Q. Transmission of drug-resistant tuberculosis among treated patients in Shanghai, China. J Infect Dis 2007 Mar 15: 195(6):864–9.
218 Wells CD, Cegielski JP, Nelson LJ, et al. HIV infection and mutlidrug-resistant tuberculosis--the perfect storm. The Journal of Infectious Diseases 2007. 196(supplement 1): p. S86-S107.
219 Basu S, Andrews JR, Poolman EM, et al. Prevention of nosocomial transmission of extensively drug-resistant tuberculosis in rural South African district hospitals: an epidemiological modeling study. Lancet, 2007. 370(9597): p. 1500-7.
220 Excerpted from: Keshavjee S, Seung K, Satti H, Furin J, Farmer P, Kim JY, Becerra M. Building capacity for multidrug-resistant tuberculosis treatment: health systems strengthening in Lesotho. Innovations. 2007 Fall; 2(4):87-106.
221 See: World Health Organization (2007) “WHO Report: Global Tuberculosis Control: Africa.” <http://www.who.int/tb/publications/global_report/2007/pdf/afr.pdf> (accessed 6 Jan 2008).
222 See: World Health Organization (September 2005). “Summary Country Profile for HIV/AIDS Treatment Scale-up: Lesotho.” http://www.who.int/hiv/HIVCP_LSO.pdf> (accessed 6 Jan 2008).
223 Ministry of Health and Social Welfare, Government of Lesotho, 2006
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