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Drivers of tuberculosis epidemics: The role of risk factors and social determinants
Knut Lonnroth*, Ernesto Jaramillo, Brian G. Williams, Christopher Dye, Mario Raviglione
World Health Organization, Geneva, Switzerland
a r t i c l e i n f o
a b s t r a c t
Article history:
Available online 23 April 2009
The main thrust of the World Health Organizations global tuberculosis (TB) control strategy is to ensure
effective and equitable delivery of quality assured diagnosis and treatment of TB. Options for including
preventive efforts have not yet been fully considered. This paper presents a narrative review of the
historical and recent progress in TB control and the role of TB risk factors and social determinants. The
review was conducted with a view to assess the prospects of effectively controlling TB under the current
strategy, and the potential to increase epidemiological impact through additional preventive interventions. The review suggests that, while the current strategy is effective in curing patients and saving lives,
the epidemiological impact has so far been less than predicted. In order to reach long-term epidemiological targets for global TB control, additional interventions to reduce peoples vulnerability for TB may
therefore be required. Risk factors that seem to be of importance at the population level include poor
living and working conditions associated with high risk of TB transmission, and factors that impair the
hosts defence against TB infection and disease, such as HIV infection, malnutrition, smoking, diabetes,
alcohol abuse, and indoor air pollution. Preventive interventions may target these factors directly or via
their underlying social determinants. The identication of risk groups also helps to target strategies for
early detection of people in need of TB treatment. More research is needed on the suitability, feasibility
and cost-effectiveness of these intervention options.
2009 Elsevier Ltd. All rights reserved.
Keywords:
Tuberculosis
Disease control
Social determinants
Risk factors
Review
Epidemiology
WHO
Introduction
The Commission on Social Determinants for Health (CSDH), set
up by the World Health Organization (WHO) in 2005, has
attempted to revitalize the debate and actions to improve health
through addressing the causes of the causes of ill health. The
commission has developed action frameworks in several elds to
address the social determinants of health including early childhood
development, globalization, urbanisation, employment conditions,
social exclusion, etc. A key message from the CSDH is that public
health achievements will largely depend on actions outside the
health care sector (CSDH, 2008).
The work of the commission builds on a long social medicine
tradition, from Virchow and the public health oriented social and
environmental interventions that he and others inspired from the
mid-19th century onwards (Rosen, 1974), through the social model
of health adopted by WHO in the late 1940s (Chisholm, 1948), to the
Health for All concept in the 1970s (WHO, 1978). It has not always
been easy to keep the social medicine concepts and action
* Corresponding author. World Health Organization, Stop TB Department, 20
Avenue Appia, CH-1211 Geneva, Switzerland. Tel.: 41 22 7911628, fax: 41 22
7914199.
E-mail address: lonnrothk@who.int (K. Lonnroth).
0277-9536/$ see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.socscimed.2009.03.041
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Findings
History of TB epidemiology and social change in industrialized
countries
Epidemiological TB data before the 20th century is imprecise.
However, some broad trends have been identied with a reasonable level of certainty. The conventional wisdom is that the incidence of TB increased in industrialized countries in the 17th to 18th
centuries, peaking at different times in different places from the
middle of the 1700s in Great Britain to the beginning of the 1900s in
Japan. From these trends, a temporal association has been suggested between increased TB incidence and rapid industrialization
and urbanisation. TB rates were often particularly high in urban
areas. A plausible explanation is that transmission increased due to
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Deaths/million/year
2000
1500
First anti-TB
drug available
1000
500
World War 1
0
1900
1920
World War 2
1940
1960
1980
Fig. 2. Decline in TB mortality in England and Wales, and its association in time with
the two World Wars, and the introduction of chemotherapy against TB.
Incidence/1 million/yr
10000
1000
100
10
Elimination -16%/yr
Global Plan -6%/yr
Current trajectory -1%/yr
1
2000
2010
2020
2030
2040
2050
Year
Fig. 3. Scenarios for the trend of global TB incidence 20072050, based on: (a)
extrapolation of current rate of decline (1% per year); (b) predicted decline with full
implementation of the Global Plan to Stop TB 20062015 (6% per year); and (c)
desired trend for reaching the TB elimination target by 2050 (16% per year).
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Fig. 4. Framework for proximate risk factors and upstream determinants of TB.
2245
Blas, E., & Sivasankara, A. K. (Eds.). (2009). Priority public health conditions: From
learning to action on social determinants of health. Geneva: World Health
Organization.
Bobrik, A., Danishes, K., Eroshina, K., & McKee, M. (2005). Prison health in Russia:
the larger picture. Journal of Public Health Policy, 26, 3059.
Borgdorff, M., Floyd, K., & Broekmans, J. F. (2002). Interventions to reduce tuberculosis mortality and transmission in low- and middle-income countries.
Bulletin of WHO, 80, 217227.
Brimnes, N. (2007). Vikings against tuberculosis: The International Tuberculosis
Campaign in India, 19481951. Bulletin of the History of Medicine, 81, 407430.
Buskin, S. E., Gale, J. L., Weiss, N. S., & Nolan, C. M. (1994). Tuberculosis risk factors in
adults in King County, Washington, 1998 through 1990. American Journal of
Public Health, 84, 17501756.
Cegielski, P., & McMurray, D. N. (2004). The relationship between malnutrition and
tuberculosis: evidence from studies in humans and experimental animals. The
International Journal of Tuberculosis and Lung Disease, 8, 286298.
China Tuberculosis Control Collaboration. (2004). The effect of tuberculosis control
in China. Lancet, 364, 417422.
Chisholm, B. (1948). Social medicine. Scientic American, 180, 1115.
Cohen, A., & Mehta, S. (2007). Pollution and tuberculosis: outdoor sources. PLoS
Medicine, 4, e141e143.
Commission on Social Determinants of Health. (2007). Achieving health equity: From
root causes to fair outcomes Commission on Social Determinants of Health
interim statement. Geneva: World Health Organization.
Corbett, E. L., Churchyard, G. J., Clayton, T. C., Williams, B. G., Mulder, D., Hayes, R. J., et
al. (2000). HIV infection and silicosis: the impact of two potent risk factors on the
incidence of mycobacterial disease in South African miners. AIDS, 14, 27592768.
Corbett, E. L., Watt, C. J., Walker, N., Maher, D., Williams, B. G., Raviglione, M. C., et al.
(2003). The growing burden of tuberculosis: global trends and interactions with
the HIV epidemic. Archives of Internal Medicine, 163, 10091021.
CSDH. (2008). Closing the gap in a generation: Health equity through action on the
social determinants of health. Final report of the Commission on Social Determinants of Health. Geneva: World Health Organization.
DArcy Hart. (1932). The value of tuberculin test in man, with special reference to
the intracutaneous test. Medical Research Council Special Series, 164, 5132.
Davies, R., Tocque, K., Bellis, M., Rimmington, T., & Davies, P. (1999). Historical
declines in tuberculosis in England and Wales: improving social conditions or
natural selection? The International Journal of Tuberculosis and Lung Disease, 3,
10511054.
Dye, C., & Floyd, K. (2006). Tuberculosis. In T. Jamison, J. G. Breman, & A. R. Measham
(Eds.), Disease control priorities in developing countries (pp. 289309). WA, DC:
The World Bank.
Dye, C., Garnett, G. P., Sleeman, K., & Williams, B. G. (1998). Prospects for worldwide
tuberculosis control under the WHO DOTS strategy. Directly observed shortcourse therapy. Lancet, 352, 18861891.
Dye, C., Lonnroth, K., Jaramillo, E., Williams, B. G., & Raviglione, M. Determinants of
trends in tuberculosis incidence: an ecologic analysis for 134 countries. Bulletin
of WHO, in press.
Dye, C., Ottmani, S., Laasri, L., & Benchelkh, N. (2007). The decline of tuberculosis
epidemics under chemotherapy: a case study in Morocco. The International
Journal of Tuberculosis and Lung Disease, 11, 12251231.
Fairchild, A., & Oppenheimer, M. (1998). Public health nihilism vs. pragmatism:
history, politics, and the control of tuberculosis. American Journal of Public
Health, 88, 11051117.
FAO. (2006). The state of food insecurity in the world 2006. Rome: Food and Agriculture Organization of the United Nations.
Farmer, P. (1997). Social scientists and the new tuberculosis. Social Science &
Medicine, 44, 347358.
Frieden, T. R., Fujiwara, P. I., Washko, R. M., & Hamburg, M. A. (1995). Tuberculosis in
New York Citydturning the tide. The New England Journal of Medicine, 333,
229233.
Friedman, L. N., Williams, M. T., Singh, T. P., & Frieden, T. R. (1996). Tuberculosis,
AIDS, and death among substance abusers on welfare in New York City. The New
England Journal of Medicine, 334, 828833.
Gilson, L., Doherty, J., Loewenson, R., & Francis, V. (2007). Knowledge network on
health systems WHO Commission on Social Determinants of Health. Final report.
London: Centre for Health Policy.
Gonzalez, E., Armas, L., & Llanes, M. J. (2007). Progress towards tuberculosis elimination in Cuba. The International Journal of Tuberculosis and Lung Disease, 11,
405411.
Grundy, E. (2005). The McKeown debate: time for burial. International Journal of
Epidemiology, 34, 529533.
Hanson, C., Floyd, K., & Weil, D. (2006). Tuberculosis in the poverty alleviation
agenda. In M. Raviglione (Ed.), TB: A comprehensive international approach (pp.
10971114). New York: Informa Healthcare.
Harling, G., Ehrlich, R., & Myer, L. (2008). The social epidemiology of tuberculosis in
South Africa: a multilevel analysis. Social Science & Medicine, 66, 492505.
Hinman, A. R., Judd, J. M., Kolnik, J. P., & Daitch, P. B. (1976). Changing risks in
tuberculosis. American Journal of Epidemiology, 103, 486497.
Holtgrave, D. R., & Crosby, R. A. (2004). Social determinants of tuberculosis case
rates in the United States. American Journal of Preventive Medicine, 26, 159162.
Humphrey, J. H., Nathoo, K. J., & Hargrove, J. W. (2007). HIV-1 and HIV-2 prevalence
and associated risk factors among postnatal women in Harare, Zimbabwe.
Epidemiology and Infection, 135, 933942.
2246
Huong, N. T., Duong, B. D., Co, N. V., Quy, H. T., Tung, L. B., Broekmans, J. F., et al.
(2006). Tuberculosis epidemiology in six provinces of Vietnam after the
introduction of the DOTS strategy. The International Journal of Tuberculosis and
Lung Disease, 10, 963969.
Irwin, N., & Whiting, D. (2008). The social determinants of diabetes and its impact
on human well-being. In E. Blas, & A. K. Sivasankara (Eds.), Priority public health
conditions: From learning to action on social determinants of health. Geneva:
World Health Organization.
IUATLD, & WHO. (2007). A WHO/The Union monograph on TB and tobacco control
Joining efforts to control two related global epidemics. WHO/HTM/TB/2007.390.
Geneva: World Health Organization.
Jaramillo, E. (1999). Encompassing prevention with treatment: the path for a long
lasting control of tuberculosis. Social Science & Medicine, 49, 393404.
Keppel, K. G. (2007). Ten largest racial and ethnic health disparities in the United
States based on healthy people 2010 objectives. American Journal of Epidemiology, 166, 97103.
Kjellstrom, T., Mercado, S., Sattherhwaite, D., McGranaham, G., Friel, S., &
Havemann, K. (2007). Our cities, our health, our future: Acting on social determinants for health equity in urban settings. Report to the WHO Commission on
Social Determinants of Health from the Knowledge Network on urban settings.
Kobe: World Health Organization Kobe Centre.
Labonte, R., Blouin, C., & Chopra, M. (2007). Towards health-equitable globalization:
Rights, regulation and redistribution. Final report to the Commission on Social
Determinants of Health from the Globalization Knowledge Network. Ottawa:
Institute of Population Health.
Laxminarayan, R., Klein, E., Dye, C., Floyd, K., Darley, S., & Adeyi, O. (2007). Economic
benet of tuberculosis control. Policy Research Working Paper 4295. WA: The
World Bank.
Leon, D. A., Chenet, L., Shkolnikov, V. M., Zakharov, S., Shapiro, J., Rakhmanova, G.,
et al. (1997). Huge variation in Russian mortality rates 198494: artefact,
alcohol, or what? Lancet, 350, 383388.
Lienhardt, C. (2001). From exposure to disease: the role of environmental factors in
susceptibility to and development of tuberculosis. Epidemiologic Review, 23,
288301.
Lin, H., Ezzati, M., & Murray, M. (2007). Tobacco smoke, indoor air pollution and
tuberculosis: a systematic review and meta-analysis. PLoS Medicine, 4, e142.
Lonnroth, K., & Raviglione, M. (2008). Global tuberculosis epidemiology prospects
for control. Seminars in Respiratory & Critical Care Medicine, 29, 481491.
Lonnroth, K., Williams, B. G., Stadlin, S., Jaramillo, E., & Dye, C. (2008). Alcohol use as
risk factor for tuberculosis disease a systematic review. BMC Public Health, 8, 289.
Lonnroth, K., Zignol, M., & Uplekar, M. (2006). Controlling TB in large metropolitan
settings. In M. Raviglione (Ed.), TB: A comprehensive international approach (pp.
10051027). New York: Informa Healthcare.
Lopez De Fede, A., Stewart, J. E., Harris, M. J., & Mayeld-Smith, K. (2008). Tuberculosis in socio-economically deprived neighborhoods: missed opportunities
for prevention. The International Journal of Tuberculosis and Lung Disease, 12,
14251430.
McKeown, T., & Record, R. G. (1962). Reasons for the decline of mortality in England
and Wales during the nineteenth century. Population Studies, 16, 94122.
Menzies, D., Joshi, R., & Pai, M. (2007). Risk of tuberculosis infection and disease
associated with work in health care settings. The International Journal of
Tuberculosis and Lung Disease, 11, 593605.
Mishra, V., Assche, S. B., Greener, R., Vaessen, M., Hong, R., Ghys, P. D., et al. (2007).
HIV infection does not disproportionately affect the poorer in sub-Saharan
Africa. AIDS(Suppl. 7), S17S28.
Mori, M. A., Leonardson, G., & Welty, T. K. (1992). The benets of isoniazid
chemoprophylaxis and risk factors for tuberculosis among Oglala Sioux Indians.
Archives of Internal Medicine, 152, 547550.
Muniyandi, M., Ramachandran, R., Gopi, P. G., Chandrasekaran, V., Subramani, R.,
Sadacharam, K., et al. (2007). The prevalence of tuberculosis in different
economic strata: a community survey from South India. The International
Journal of Tuberculosis and Lung Disease, 11, 10421045.
Navarro, V., Muntaner, C., Borrell, C., Benach, J., Quiroga, A., Rodrguez-Sanz, M., et al.
(2006). Politics and health outcomes. Lancet, 368, 10331037.
Pesut, D. P., Gledovic, Z. B., Grgurevic, A. D., Nagorni-Obradovic, L. M., & Adzic, T. N.
(2008). Tuberculosis incidence in elderly in Serbia: key trends in socioeconomic
transition. Croatian Medical Journal, 49, 807812.
Piot, P., Greener, R., & Russell, S. (2007). Squaring the circle: AIDS, poverty, and
human development. PLoS Medicine, 4, 15711575.
Porter, D. (2006). How did social medicine evolve, and where is it heading? PLoS
Medicine, 3, 16671672.
Porter, J. D. H., & Grange, J. M. (1999). Tuberculosis An interdisciplinary perspective.
London: Imperial College Press.
Prince, M., Patel, V., Saxena, S., Maj, M., Maselko, J., Phillips, M. R., et al. (2007). No
health without mental health. Lancet, 370, 859877.
Raviglione, M. (2007). Infectious diseases and globalization. Rome, Vatican City.
Raviglione, M., & Pio, A. (2002). Evolution of WHO policies for tuberculosis control,
19482001. Lancet, 359, 775780.
Raviglione, M., & Uplekar, M. (2006). The new Stop TB Strategy of WHO. Lancet, 367, 952.
Reidpath, D. (2008). Social determinants of HIV/AIDS. In E. Blas, & A. K. Sivasankara
(Eds.), Priority public health conditions: From learning to action on social determinants of health. Geneva: World Health Organization.
Rhefuess, E. (2006). Fuel for life Household energy and health. Geneva: World
Health Organization.