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Commentary |

Tuberculosis, Vulnerability, and Access to Quality Care

Philip C. Hopewell, MD; Madhukar Pai, MD, PhD
[+] Author Affiliations

Author Affiliations: Division of Pulmonary and Critical Care Medicine, Francis J. Curry National Tuberculosis Center, San Francisco General Hospital, University of California, San Francisco (Drs Hopewell and Pai); and Division of Epidemiology, School of Public Health, University of California, Berkeley (Dr Pai).

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JAMA. 2005;293(22):2790-2793. doi:10.1001/jama.293.22.2790
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As with most infectious diseases, tuberculosis (TB) is not randomly distributed; it thrives in specific groups and under specific conditions in association with identified and unidentified factors that confer vulnerability to the disease. Available information on the association between TB and the many known conditions and circumstances that influence vulnerability to the disease has been reviewed recently and is summarized in the Article .1 2 These conditions and circumstances mainly include 3 broad categories of factors: individual biological factors (eg, immunodeficiency states), social and economic circumstances (eg, crowding, poverty, poor nutrition), and environmental and institutional factors (eg, silica dust, poor ventilation).

BOX. FACTORS THAT INCREASE VULNERABILITY TO TUBERCULOSIS*

Individual Level: Biological and Disease-Related Factors

  • Age

  • Sex ratio

  • Pregnancy

  • Genetic influences on infection or disease vulnerability

  • Interaction with other conditions (eg, human immunodeficiency virus infection)

Household and Community Level: Social and Economic Factors

  • Gender

  • Poverty

  • Poor nutrition

  • Crowding

  • Livelihoods and occupation

  • Illness conceptualization and lack of knowledge

Macro Level: Environmental and Institutional Factors

  • Physical environment (eg, climate, silica dust, indoor air pollution, smoking)

  • Migration

  • Increased drug resistance

  • Inappropriate, delay of, or lack of screening and case detection

  • Treatment delays

  • Poor-quality care

  • Health care system and status of any reform

*Adapted from Bates et al.1 2

Among the biological factors, human immunodeficiency virus (HIV) infection is perhaps the most potent. In the report by Grant and colleagues3 in this issue of JAMA, 2 biological factors, HIV infection and exposure to silica dust, have been superimposed in South African gold miners to set the stage for an extraordinarily high incidence of tuberculosis: 11.9 cases per 100 person-years of observation before implementing a program of treatment with isoniazid and 9.0 cases per 100 person-years after the intervention. Two social factors, incarceration and homelessness, are also discussed in this issue of JAMA. The study by Drobniewski and coworkers4 illustrates the importance of social and institutional factors, such as incarceration, in creating conditions favorable for the transmission of drug-resistant TB. In addition, the report by Haddad and associates5 describing TB among homeless persons in the United States reinforces the point that social circumstances play an important role in determining vulnerability to TB. All 3 studies also illustrate the high degree to which social and biological factors interact in individuals.

The traditional framework for conceptualizing vulnerability to tuberculosis involves partitioning the factors into those that influence the likelihood of acquisition of infection with Mycobacterium tuberculosis and those that influence the host-immune response to the infection. Not included in this 2-component conceptual model, however, is the vulnerability of individuals to severe consequences of TB, including prolonged disability and death, and the vulnerability of communities to ongoing spread of infection, sometimes with drug-resistant organisms, because of a lack of access to appropriate and effective care for diagnosis, treatment, and prevention of TB. Any person anywhere in the world who is unable to access quality health care should be considered vulnerable to TB. Likewise, any community with no or inadequate access to appropriate diagnostic and treatment services for TB is a vulnerable community.

Appropriate and effective care for TB is not complicated in most instances. Current TB care and control strategies are relatively simple and generally quite effective. The DOTS (directly observed therapy, short course) strategy, described in the article by Dye and colleagues6 in this issue of JAMA, when appropriately implemented, has been shown in many countries (most recently and effectively in Peru and China) to reduce the incidence and prevalence of tuberculosis.7 8 Dye and associates6 clearly describe the achievements of the DOTS strategy but also indicate the shortcomings and present some of the reasons why current goals of reducing TB incidence, prevalence, and mortality are not being met. As public health TB control programs implement the DOTS strategy more widely, it is becoming apparent that the lack of access to effective care is one of the main factors limiting global TB control.

Despite the availability of highly effective therapy for many years and a concerted worldwide effort to improve access to the diagnostic and treatment interventions embodied in the DOTS strategy, a large number of individuals in developing countries with TB, or who have symptoms that might be caused by the disease, fail to get adequate services. In 2003, only about 45% of the estimated total number of individuals with sputum smear–positive TB were detected and reported.9 This is especially concerning given that the estimated number of individuals with positive sputum smears probably represents no more than half of all prevalent individuals with TB (ie, all forms, including individuals with sputum smear–positive and sputum smear–negative pulmonary TB and extrapulmonary TB).9 More than 80% of individuals diagnosed as having TB were treated successfully in DOTS programs.6 ,9 Thus, effective treatment for TB, while an important concern, is less of a challenge than appropriate case detection and access to effective treatment.

Not much is known about the large number of cases of TB that are not managed under DOTS programs. Some are probably well managed but the available evidence suggests that, at least in the private sector, this is not the case. Evidence from studies from around the world show that delays in diagnosis, delays in treatment, deviations from standard TB management practices, irrational and harmful practices, variability in the quality of TB care, and inadequate efforts to support patients and improve treatment adherence continue to plague global TB control efforts.

A recent global situation assessment conducted by the World Health Organization (WHO) suggests that delays in diagnosis are common,10 and perhaps more common than delays in seeking care, although both are important.11 The WHO assessment and other studies indicate that physicians, in particular those who work in the private health care sector, often deviate from standard, internationally recommended TB management practices.10 ,12 These include underuse of sputum microscopy and overreliance on radiography for diagnosis, use of inappropriate drug regimens, incorrect combinations of drugs, and inaccurate dosages for the wrong duration.10 ,12 19 These findings highlight flaws in the system of care that lead to lack of access to appropriate services or substandard care to populations that are most vulnerable to TB and are least able to bear the consequences of such systemic failures.

An effort to address the issue of quality of care for individuals with TB, mainly in the private sector, is the development of international standards for TB care. This effort is being led by a consortium of organizations concerned with global TB care and control (American Thoracic Society, US Centers for Disease Control and Prevention, Dutch Tuberculosis Foundation, International Union Against Tuberculosis and Lung Disease, and WHO). A fundamental premise that underlies plans for these standards is that all clinicians who undertake treatment of patients with TB must recognize that they are assuming an important public health function that entails responsibility to the community as well as to the individual patients in their care.

Despite many differences among countries in economic conditions, health care systems, and epidemiological circumstances and among health care professionals, the basic principles of care for persons with or suspected of having TB are the same worldwide. Consequently, the fundamental approaches to TB care can be described in a set of essential standards that can be used in all areas and by all health care sectors—national TB control programs, other public sector agencies, and private health care clinics. Engagement of all clinicians to deliver a high standard of TB care for all patients is essential to protect the health of communities and to restore the health of individuals with the disease, while preventing TB in their families and others with whom they come into contact.

Prompt and accurate diagnosis and effective treatment are not only essential for good patient care, they are the key elements in the public health response to TB and are the cornerstone of TB control. Good care for individuals with TB is unquestionably in the best interest of the wider community. Community contributions to TB care and control are increasingly important in raising public awareness of the disease, providing treatment support, reducing the stigma associated with TB infection, and demanding adherence to a high standard of TB care.20 The community should expect that standards of care will be provided and will be met. Substandard care will likely result in poor patient outcomes, continued infectiousness with transmission of the infection to other community members, and, perhaps, generation and propagation of drug resistance.

In accordance with the DOTS strategy, the standards should address the basic elements of diagnosis and treatment of TB with a series of straightforward statements that are backed by evidence. The intent is to secure a broad base of endorsements—national governments, national TB programs, professional medical and nursing societies, academic institutions, nongovernmental organizations that provide medical care, and HIV-focused organizations—to use the standards to create peer pressure for clinicians to conform to the principles, as well as to serve as the basis for preservice and inservice training.

The areas to be addressed by the standards include identification of persons who should be evaluated for TB, bacteriological confirmation of the diagnosis in all persons with suspected TB, use of drug regimens of proven effectiveness, provision of treatment support and supervision, appropriate HIV counseling and testing under defined epidemiological circumstances, consideration of antiretroviral treatment for patients with HIV infection who have TB, evaluation of all patients with TB infection for the possibility of drug resistance, and required reporting of all cases to the relevant public health authority. A set of standards is only a tool, and having a tool does not guarantee that the job will be done correctly. However, with proper use and broad-based support, the standards could be a useful means of improving the quality of care for TB.

To reduce the vulnerability of individuals to TB, a multipronged approach is essential. Efforts to improve living circumstances, alleviate poverty, minimize crowding, prevent malnutrition, and prevent and treat HIV infection, as well as research and development for new tools, are all critical undertakings. Among these activities should be vigorous efforts to address shortcomings in the quality of care for individuals with TB, an often overlooked reason for increased vulnerability to the disease.

Corresponding Author: Philip C. Hopewell, MD, Division of Pulmonary and Critical Care Medicine, San Francisco General Hospital, University of California, San Francisco, 1001 Potrero Ave, Room 5K1, San Francisco, CA 94110 (phopewell@medsfgh.ucsf.edu).

Financial Disclosures: None reported.

Funding/Support: This work was supported by the National Institutes of Health (NIH), NIH/National Institute of Allergy and Infectious Diseases grant R01 AI 34238, and Fogarty AIDS International Training Program grant 1-D43-TW00003-16.

Role of the Sponsor: These funding sources had no role in the preparation, review, or approval of the manuscript.

Bates I, Fenton C, Gruber J.  et al.  Vulnerability to malaria, tuberculosis, and HIV/AIDS infection and disease, I: determinants operating at individual and household level.  Lancet Infect Dis. 2004;4267-277
PubMed
Bates I, Fenton C, Gruber J.  et al.  Vulnerability to malaria, tuberculosis, and HIV/AIDS infection and disease, II: determinants operating at environmental and institutional level.  Lancet Infect Dis. 2004;4368-375
PubMed
Grant AD, Charalambous S, Fielding KL.  et al.  Effect of routine isoniazid preventive therapy on tuberculosis incidence among HIV-infected men in South Africa: a novel randomized incremental recruitment study.  JAMA. 2005;2932719-2725
Drobniewski F, Balabanova Y, Nikolayevsky V.  et al.  Drug-resistant tuberculosis, clinical virulence, and the dominance of the Beijing strain family in Russia.  JAMA. 2005;2932726-2731
Haddad MB, Wilson TW, Ijaz K, Marks SM, Moore M. Tuberculosis and homelessness in the United States, 1994-2003.  JAMA. 2005;2932762-2766
Dye C, Watt CJ, Bleed DM, Hosseini SM, Raviglione MC. The evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally.  JAMA. 2005;2932767-2775
Suarez PG, Watt CJ, Alarcon E.  et al.  The dynamics of tuberculosis in response to 10 years of intensive control effort in Peru.  J Infect Dis. 2001;184473-478
PubMed
China Tuberculosis Control Collaboration.  The effect of tuberculosis control in China.  Lancet. 2004;364417-422
PubMed
World Health Organization.  Global Tuberculosis Control: Surveillance, Planning, FinancingGeneva, Switzerland: World Health Organization; 2005
World Health Organization.  Involving Private Practitioners in Tuberculosis Control: Issues, Interventions, and Emerging Policy FrameworkGeneva, Switzerland: World Health Organization; 2001
Cheng G, Tolhurst R, Li RZ, Meng QY, Tang S. Factors affecting delays in tuberculosis diagnosis in rural China: a case study in four counties in Shandong Province.  Trans R Soc Trop Med Hyg. 2005;99355-362
PubMed
Uplekar M, Pathania V, Raviglione M. Private practitioners and public health: weak links in tuberculosis control.  Lancet. 2001;358912-916
PubMed
Lonnroth K, Thuong LM, Linh PD, Diwan VK. Delay and discontinuity—a survey of TB patients’ search of a diagnosis in a diversified health care system.  Int J Tuberc Lung Dis. 1999;3992-1000
PubMed
Olle-Goig JE, Cullity JE, Vargas R. A survey of prescribing patterns for tuberculosis treatment amongst doctors in a Bolivian city.  Int J Tuberc Lung Dis. 1999;374-78
PubMed
Prasad R, Nautiyal RG, Mukherji PK, Jain A, Singh K, Ahuja RC. Diagnostic evaluation of pulmonary tuberculosis: what do doctors of modern medicine do in India?  Int J Tuberc Lung Dis. 2003;752-57
PubMed
Shah SK, Sadiq H, Khalil M.  et al.  Do private doctors follow national guidelines for managing pulmonary tuberculosis in Pakistan?  East Mediterr Health J. 2003;9776-788
PubMed
Singla N, Sharma PP, Singla R, Jain RC. Survey of knowledge, attitudes and practices for tuberculosis among general practitioners in Delhi, India.  Int J Tuberc Lung Dis. 1998;2384-389
PubMed
Suleiman BA, Houssein AI, Mehta F, Hinderaker SG. Do doctors in north-western Somalia follow the national guidelines for tuberculosis management?  East Mediterr Health J. 2003;9789-795
PubMed
Uplekar MW, Shepard DS. Treatment of tuberculosis by private general practitioners in India.  Tubercle. 1991;72284-290
PubMed
Hadley M, Maher D. Community involvement in tuberculosis control: lessons from other health care programmes.  Int J Tuberc Lung Dis. 2000;4401-408
PubMed

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Bates I, Fenton C, Gruber J.  et al.  Vulnerability to malaria, tuberculosis, and HIV/AIDS infection and disease, I: determinants operating at individual and household level.  Lancet Infect Dis. 2004;4267-277
PubMed
Bates I, Fenton C, Gruber J.  et al.  Vulnerability to malaria, tuberculosis, and HIV/AIDS infection and disease, II: determinants operating at environmental and institutional level.  Lancet Infect Dis. 2004;4368-375
PubMed
Grant AD, Charalambous S, Fielding KL.  et al.  Effect of routine isoniazid preventive therapy on tuberculosis incidence among HIV-infected men in South Africa: a novel randomized incremental recruitment study.  JAMA. 2005;2932719-2725
Drobniewski F, Balabanova Y, Nikolayevsky V.  et al.  Drug-resistant tuberculosis, clinical virulence, and the dominance of the Beijing strain family in Russia.  JAMA. 2005;2932726-2731
Haddad MB, Wilson TW, Ijaz K, Marks SM, Moore M. Tuberculosis and homelessness in the United States, 1994-2003.  JAMA. 2005;2932762-2766
Dye C, Watt CJ, Bleed DM, Hosseini SM, Raviglione MC. The evolution of tuberculosis control and prospects for reducing tuberculosis incidence, prevalence, and deaths globally.  JAMA. 2005;2932767-2775
Suarez PG, Watt CJ, Alarcon E.  et al.  The dynamics of tuberculosis in response to 10 years of intensive control effort in Peru.  J Infect Dis. 2001;184473-478
PubMed
China Tuberculosis Control Collaboration.  The effect of tuberculosis control in China.  Lancet. 2004;364417-422
PubMed
World Health Organization.  Global Tuberculosis Control: Surveillance, Planning, FinancingGeneva, Switzerland: World Health Organization; 2005
World Health Organization.  Involving Private Practitioners in Tuberculosis Control: Issues, Interventions, and Emerging Policy FrameworkGeneva, Switzerland: World Health Organization; 2001
Cheng G, Tolhurst R, Li RZ, Meng QY, Tang S. Factors affecting delays in tuberculosis diagnosis in rural China: a case study in four counties in Shandong Province.  Trans R Soc Trop Med Hyg. 2005;99355-362
PubMed
Uplekar M, Pathania V, Raviglione M. Private practitioners and public health: weak links in tuberculosis control.  Lancet. 2001;358912-916
PubMed
Lonnroth K, Thuong LM, Linh PD, Diwan VK. Delay and discontinuity—a survey of TB patients’ search of a diagnosis in a diversified health care system.  Int J Tuberc Lung Dis. 1999;3992-1000
PubMed
Olle-Goig JE, Cullity JE, Vargas R. A survey of prescribing patterns for tuberculosis treatment amongst doctors in a Bolivian city.  Int J Tuberc Lung Dis. 1999;374-78
PubMed
Prasad R, Nautiyal RG, Mukherji PK, Jain A, Singh K, Ahuja RC. Diagnostic evaluation of pulmonary tuberculosis: what do doctors of modern medicine do in India?  Int J Tuberc Lung Dis. 2003;752-57
PubMed
Shah SK, Sadiq H, Khalil M.  et al.  Do private doctors follow national guidelines for managing pulmonary tuberculosis in Pakistan?  East Mediterr Health J. 2003;9776-788
PubMed
Singla N, Sharma PP, Singla R, Jain RC. Survey of knowledge, attitudes and practices for tuberculosis among general practitioners in Delhi, India.  Int J Tuberc Lung Dis. 1998;2384-389
PubMed
Suleiman BA, Houssein AI, Mehta F, Hinderaker SG. Do doctors in north-western Somalia follow the national guidelines for tuberculosis management?  East Mediterr Health J. 2003;9789-795
PubMed
Uplekar MW, Shepard DS. Treatment of tuberculosis by private general practitioners in India.  Tubercle. 1991;72284-290
PubMed
Hadley M, Maher D. Community involvement in tuberculosis control: lessons from other health care programmes.  Int J Tuberc Lung Dis. 2000;4401-408
PubMed
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