Commentary: Evaluating the tuberculosis burden in prisoners in Pakistan

Mary C White

University of California, San Francisco, 2 Koret Way, Box 0608, San Francisco, CA 94143–0608 USA. E-mail: mcwhite{at}itsa.ucsf.edu

It is well recognized that correctional facilities worldwide are settings in which tuberculosis (TB) prevalence, and transmission, are high. In this issue of the International Journal of Epidemiology, Hussain et al. describe the prevalence of latent TB infection (LTBI) in a random sample of prisoners from five prisons in the North West Frontier Province, Pakistan.1 In this cross-sectional design, the authors provide an interesting glimpse of the burden of infection in this population.

The authors found that 48% of the prisoners were tuberculin skin test (TST) positive, using a conservative evaluation of skin test results: >=15 mm induration was interpreted as positive for those with history of BCG vaccination, ascertained by evidence of a scar. The authors accurately note that this would underestimate those with true LTBI who may have received BCG only in infancy;2 however, this would result in false positives if vaccine was given in later years but without scar development.3 The primary limitation of these cross-sectional data, the measurement of the number of prisoners with new and existing LTBI at the same time, is compounded by the lack of information on what proportion of the prison population has active TB. The sample size, 6% of prisoners (n = 425), was too small to allow reliable estimates of active TB if these 48% had been followed up to determine if any had active TB.

The authors make three overall conclusions on the basis of their data: first, that the prevalence of LTBI is alarmingly high in this prison population; second, that conditions in the prisons suggest transmission of TB within the facility; and thirdly that infection control measures need to be taken in prisons (to diagnose people with TB) that will reduce transmission. Each conclusion might benefit from review in the context of the work and recommendations of others.


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The World Health Organization (WHO) Global Surveillance and Monitoring Project estimates the TB incidence in Pakistan is 181 per 100 000, with an estimated 40% of the population infected with TB.4 The authors’ finding that 48% of this prison population is positive for TB infection is statistically different from the estimated population prevalence of 40% (95% CI for the point estimate of 48% is 43.3–52.7%, P = 0.0009, StatsDirect v.2.2.9, Cheshire, UK). However, prisoner populations are well documented as disproportionately coming from marginalized subgroups, including the poor, substance abusers, ethnic minorities, and the mentally ill, who are at higher risk of TB than the general population. Therefore the finding that LTBI prevalence is 48% in a setting that houses those at increased risk of TB is not surprising, given the 40% estimated prevalence in the overall population.

The authors compare their results with those found by Martin Sanchez et al., who reported prevalence of 55% in a Spanish prison,5 and with Koo et al., who reported 30% prevalence from a California prison.6 In both comparison settings the relatively high prevalence of LTBI among prisoners in countries with low population incidence of TB can be explained in part by co-infection with human immunodeficiency virus (HIV).7 Perhaps more relevant is their comparison with the work of Adib et al., whose survey of all jails in Lebanon demonstrated LTBI prevalence of 45%.8 While HIV rates are not known for Pakistan, the authors cite a study among 3441 male prisoners in Sindh, Pakistan, in whom 1 was HIV-positive,9 and are appropriately cautious in concluding that their findings are in a mostly HIV-negative population. Therefore the authors are correct in their assessment that the high prevalence of TB infection in this prison population may lead to a significant public health crisis for prisons in the future, in the event that HIV co-infection becomes more prevalent in Pakistan.


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Among the factors found by the authors to be significantly associated with LTBI were older age (>42 years), length of incarceration (>2 years), and size of prison accommodation (<=60 ft2). With the exception of the apparent categorization of age into quartiles, there is no explanation for the categories selected for incarceration length or size of prison accommodation; it would have been helpful to understand why, for example, 60 ft2 was selected as the cut-off to indicate higher risk rather than examining this as a continuous variable. In a highly endemic country, age is likely a surrogate for increased lifetime opportunity for exposure, and there is no way to ascertain when or where infection occurred without evidence of prior negative TST to document conversion.

Duration of incarceration may represent primary infection within the correctional setting, but those with longer prison time may be members of the cohort of people who spend time in other high-risk areas, such as hospitals or homeless shelters, have substance use, or other cumulative TB risk factors outside prison. The fact that only 19% of prisoners in this sample had been in prison more than 2 years may suggest that prison terms are rather short. However, incarceration >6 months was found to be a risk factor for active TB in prisoners in Botswana, in a similar one-time survey in a prison system without regular screening at entry.10

Inadequate ventilation and enclosed spaces have been shown to be a risk for transmission.11,12 The variable available in this study, size of prison accommodation, is suggestive of crowded conditions conducive to TB transmission, but may also represent the realities of prison life and the relatively low position of the most marginalized people within the facility. Housing in prisons, in particular in countries where resources are scarce, can be influenced by internal hierarchies, making some people further marginalized within the prison system.13 Moreover, the frequent movements of prisoners make the interpretation of this single measurement difficult.

More importantly, however, is the lack of information on any screening or baseline health information that may have been gathered in the prison. The authors note that each prison had a medical consulting unit staffed with a qualified physician, but there is no indication of any screening of prisoners at entry. Hanau-Bercot et al. demonstrated prospectively that prison inmates have higher risk of developing active TB, independent of incarceration. Using restriction fragment length polymorphism analysis of Mycobacterium tuberculosis strains from inmates, they did not show direct transmission within the prison, with the exception of one probable transmission among 93 cases of active TB.14 They concluded, as did Hussain et al. in the current article,1 that accurate determination of transmission within a prison can only be done prospectively. There is considerable evidence of transmission of TB within prison walls; because of limited surveillance for active TB, delayed diagnosis, and high turnover11 those with unrecognized TB become index cases and transmit disease to both prisoners and prison workers.6,15,16 But without data to document conversion from TST negative to positive, or surveillance to detect development of active TB in a previously healthy prisoner or prison worker, the suggestion that the high rate of LTBI is a result of transmission inside the prison cannot be supported.


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The authors suggest that infection control measures will reduce transmission within prisons, a suggestion that in general is supported by the WHO,13 if not by the data in this study. The authors recommend screening at prison entry with sputum smear, and routine TST for latent TB infection. Their recommendations are partly in agreement with guidelines from the WHO, which state that screening for active TB should be done at entry, by chest x-ray and/or symptom review, with confirmation of TB suspects by sputum microscopy.13 WHO guidelines further suggest that a complete screening of the entire prison population should be done to identify prevalent cases, followed by screening at entry to identify new cases, and annual check ups and self-referral to detect missed cases. This is a costly process, but one that will effectively remove the reservoir of prevalent cases from the prison population and actively find new cases that enter the system.

The WHO does not, however, recommend TST or preventive therapy for those found with LTBI in high prevalence countries where effective control of active TB is not in place. Their position is that detecting and adequately treating active TB is the most cost-effective way to control TB, and a programme to find and treat those with LTBI will divert resources from this priority.13 While it is true that the TST can be a valuable epidemiological tool to use as a baseline, against which to measure annual conversions from negative to positive in order to detect transmission within the facility, the primary focus of prison TB control, in particular in settings with limited resources, should be the identification and treatment of prisoners with active TB. As the authors have not described any systematic screening of prisoners at entry for active TB in these Pakistan prisons, one would question the recommendation of routine TST for prisoners in this setting.

Complementing the active case-finding is the need for adequate treatment of those found to have active TB. The relatively short prison terms in this study (52% were in prison less than 1 year) raises the possibility that people will not be incarcerated long enough for adequate treatment, a concern not raised by this paper but one that is critically important for control of the TB epidemic. Treatment by Directly Observed Treatment Shortcourse (DOTS) case management, whether in prison or by linking with community resources, is a crucial step both to cure the individual patient and to minimize development of resistant strains. DOTS, including case detection, fully supervized standard short-course treatment, reliable provision of drugs, effective monitoring of the TB programme, and government/prison commitment to TB control, are the key components to managing TB. These seemingly simple steps are complicated by the need for integration of services, within prison systems as well as with the outside community, to detect and treat cases who come and go from the prison setting to the community.


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Hussain et al.1 provide an intriguing view of five prisons in the North West Province of Pakistan, a country ranked by WHO as one of the 22 highest incidence countries for TB.4 The authors have confirmed that prisoners here, as in other places worldwide, are among those with the highest risk for TB. Their work lays the groundwork for prospective studies of this setting where the most vulnerable are housed, where opportunities abound for detection and treatment, yet where the resources are so often limited.


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1 Hussain H, Akhtar S, Nanan D. Prevalence of and risk factors associated with Mycobacterium tuberculosis infection in prisoners, North West Frontier Province, Pakistan. Int J Epidemiol 2003;32:794–99.[Abstract/Free Full Text]

2 Centers for Disease Control and Prevention. Targeted tuberculin testing and treatment of latent tuberculosis infection. MMWR 2000;49(No.RR-6):1–43.[Medline]

3 Menzies D. Tuberculin surveys—why? Int J Tuberc Lung Dis 1998;2:263–64.[ISI][Medline]

4 Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC, for the WHO Global Surveillance and Monitoring Project. Global burden of tuberculosis: Estimated incidence, prevalence, and mortality by country. JAMA 1999;282:677–86.[Abstract/Free Full Text]

5 Martin Sanchez V, Alvarez-Guisasola F, Cayla JA, Alvarez JL. Predictive factors of Mycobacterium tuberculosis infection and pulmonary tuberculosis in prisoners. Int J Epidemiol 1995;24:630–36.[Abstract]

6 Koo DT, Baron RC, Rutherford GW. Transmission of Mycobacterium tuberculosis in a California State Prison, 1991. Am J Public Health 1997;87:279–82.[Abstract]

7 Hammett TM, Harmon MP, Rhodes W. The burden of infectious disease among inmates of and releasees from US correctional facilities, 1997. Am J Public Health 2002;92:1789–94.[Abstract/Free Full Text]

8 Adib SM, Al-Takash H, Al-Hajj C. Tuberculosis in Lebanese jails: prevalence and risk factors. Eur J Epidemiol 1999;15:253–60.[CrossRef][ISI][Medline]

9 Baqi S, Nabi N, Hasan SN et al. HIV antibody seroprevalence and associated risk factors in sex workers, drug users, and prisoners in Sindh, Pakistan. J Acquir Immune Defic Syndr Hum Retrovirol 1998; 18:73–79.[Medline]

10 Centers for Disease Control and Prevention. Rapid assessment of tuberculosis in a large prison system – Botswana, 2002. MMWR 2003; 52(No.12):250–52.[Medline]

11 MacIntyre CR, Kendig N, Kummer L, Birago S, Graham NM, Plant AJ. Unrecognised transmission of tuberculosis in prisons. Eur J Epidemiol 1999;15:705–09.[CrossRef][ISI][Medline]

12 Centers for Disease Control and Prevention. Prevention and control of tuberculosis in correctional facilities: recommendations of the Advisory Council for the Elimination of Tuberculosis. MMWR 1996;45(No.RR-8):1–26.[Medline]

13 World Health Organization. Tuberculosis Control in Prisons: A Manual for Programme Managers. Geneva: WHO, 2000.

14 Hanau-Bercot B, Gremy I, Raskine L et al. A one-year prospective study (1994–1995) for a first evaluation of tuberculosis transmission in French prisons. Int J Tuberc Lung Dis 2000;4:853–59.[ISI][Medline]

15 Jones TF, Craig AS, Valway SE, Woodley CL, Schaffner W. Transmission of tuberculosis in a jail. Ann Intern Med 1999;131: 557–63.[Free Full Text]

16 Valway SE, Richards SB, Kovacovich J, Greifinger RB, Crawford JT, Dooley SW. Outbreak of multi-drug-resistant tuberculosis in a New York State prison, 1991. Am J Epidemiol 1994;140:113–22.[Abstract]





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