Prevalence of and risk factors associated with Mycobacterium tuberculosis infection in prisoners, North West Frontier Province, Pakistan

Hamid Hussain, Saeed Akhtar and Debra Nanan

Division of Epidemiology & Biostatistics, Department of Community Health Sciences, The Aga Khan University, Stadium Road, Karachi 74800, Pakistan.

Saeed Akhtar. E-mail: saeed.akhtar{at}aku.edu


    Abstract
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Background This cross-sectional study was conducted to assess the prevalence of and identify factors associated with latent Mycobacterium tuberculosis (MTB) infection in prisoners of North West Frontier Province (NWFP).

Methods A stratified random sampling technique was used to select a sample of 425 from a total of 6607 male prisoners aged 18–60 years from the five central prisons of NWFP, Pakistan (Peshawar, Dera Ismail Khan, Haripur, Kohat, and Mardan). The selected inmates were interviewed using a structured pre-tested questionnaire; a Mantoux tuberculin skin test (TST) was also performed. Latent MTB infection status of the prisoner was determined by the size of the induration of the TST in the presence/absence of a previous BCG scar.

Results Overall prevalence of latent MTB infection among prisoners was 48% (204/425). Using multiple logistic regression, a prisoner’s age, educational level, smoking status, duration of current incarceration, and average accommodation area of 60 ft2 or less in prison barracks were found to be statistically significant (P < 0.05) predictors of latent MTB infection.

Conclusion The high prevalence of latent MTB infection as assessed by TST in prisoners requires immediate steps be taken to identify and confirm MTB infection, and to treat and counsel those found to be positive in this setting. Efforts to halt MTB transmission in prisons should include: routine screening of prisoners on entry using sputum smear and TST for diagnosis of tuberculosis (TB) and latent MTB infection, respectively. The isolation and treatment of TB positive prisoners and chemo-prophylactic treatment of TST positives, reduction of overcrowding, education regarding the harmful effects of smoking, and intensive monitoring of those serving longer prison terms may help reduce the MTB transmission in this setting and in the community at large.


Keywords Cross-sectional study, Mycobacterium tuberculosis, tuberculosis, tuberculin skin test, overcrowding, prisoners, Pakistan

Accepted 22 May 2003

Tuberculosis (TB) is a chronic, infectious disease caused by Mycobacterium tuberculosis (MTB).1,2 Currently, TB is the leading cause of mortality among infectious diseases worldwide, and 95% of TB cases and 98% of deaths due to TB occur in developing countries.3–6 Due to the inadequacy of disease surveillance in Pakistan, it is not possible to present exact data for TB incidence and TB-related mortality. However, based on the results of ad hoc surveys, and using an estimated annual cumulative incidence of TB of 171 cases per 100 000, Pakistan has been ranked as one of the top 22 developing countries afflicted by the current TB epidemic7 (World Health Organization [WHO], 2001 data). High-risk groups for MTB infection in Pakistan, like other developing countries, may include people with human immunodeficiency virus (HIV)/AIDS, people with diabetes or cancer, the malnourished, those living with someone who has active TB, poor and indigent people, residents of homeless shelters, and present or former prisoners.8

Prisoners constitute a high risk group for acquisition of MTB infection and development of TB compared with the general population due to the overcrowding, closed living conditions, insufficient ventilation, generally low socioeconomic status, poor nutrition, and poor health of prison inmates.8–13 There is increasing recognition that the high risk of MTB infection in prison settings poses a problem not only for those imprisoned but also for society at large.14 Prisoners are often highly mobile, circulating within the prison system, and they may be released after some time. Transmission of MTB in prisons is also particularly dangerous as it often involves resistant strains.15,16 Thus, effective MTB infection control in prisons is necessary to protect the well-being of both prisoners and the wider community. Currently there are no available data on prevalence of MTB infection in the prisons of Pakistan. This study estimates the prevalence of latent MTB infection among prisoners in North West Frontier Province (NWFP), Pakistan, and examines factors associated with latent MTB infection in a Pakistani prison setting.


    Materials and Methods
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
A cross-sectional study design was used to estimate the prevalence of latent MTB infection in the five central prisons in NWFP (Peshawar, Dera Ismail Khan, Haripur, Kohat, and Mardan) during July–September 2001. These 5 central prisons are the largest in the province; 15 smaller district-level prisons were excluded as they housed only a small number of ‘under trial’ prisoners for a short duration only. Each central prison has a medical unit staffed by a qualified physician which looks after the health-care needs of prisoners. In case a prisoner requires hospitalization, the facility at the district civil hospital is used. Each central prison was taken as a stratum, and a sample size determined proportional to its population size (number of prisoners). Study subjects were selected from a list constructed by the prison authorities through simple random sampling. The study population comprised male prisoners aged 18–60 years; those who were sentenced to death or in solitary custody were excluded. We also excluded prisoners whose prison term was <=3 months from the date of interview, since the Mantoux tuberculin skin test (TST) detects a reaction on an average 2–10 weeks after infection with MTB and some infected prisoners could be missed (false negative), thus leading to underestimation of prevalence.17 The demographic features of the inmates did not vary significantly between the five prisons. The mean (± standard deviation) duration of incarceration was 3.34 ± 0.91 years. Prisoners were predominately young adult males with mean (± standard deviation) age of 34.76 ± 9.97 years. They were poorly educated as 91% of inmates had formal schooling of <=5 years. These inmates were also a socioeconomically disadvantaged group as 96% of them were unemployed before the beginning of their current sentence. No further reliable epidemiological data on factors like homelessness, substance abuse, which are risk factors for acquiring MTB infection, were available.

A pre-tested structured questionnaire was used to collect data from each prisoner on their age, educational level, smoking status, duration of current incarceration, and the average area (ft2) of accommodation in the prison barrack. Since BCG vaccination is a part of the WHO recommended routine immunization programme for children in Pakistan, the presence of a BCG vaccination scar was taken as an evidence of previous BCG vaccination, as has been done by others.18 To determine the outcome (latent MTB infection positive/negative), TST was performed according to WHO protocol using a freshly prepared 0.1 ml dilution of tuberculin (purified protein derivative (PPD-RT 23) 5 tuberculin units, Connaught Laboratories, Ontario, Canada). The solution was injected intradermally on the flexor aspect of the forearm; the resulting induration was measured after 72 hours by ballpoint pen technique along the long axis of the forearm. Indurations of diameter >=10 mm in BCG unvaccinated prisoners, and >=15 mm in BCG vaccinated prisoners were considered as positive for latent MTB infection; otherwise, the result was considered negative.19,20 We did not consider the specific micro-organism that might have been involved with positive TST, since positive TST can result from infection with atypical mycobacteria as well.21 However, these cross-reactions tend to be smaller than reactions caused by MTB infection.22 Moreover TST is a recommended test for epidemiological studies, where mass screening for exposure to MTB is desired.17 Two male physicians conducted all interviews, and performed and evaluated the Mantoux TST. The study was approved by the Departmental Ethics Review Committee.

Data management and analysis
Data were double-entered using EPI-INFO version 6.04 software. In the descriptive analysis, frequencies, means, standard deviations, and quartiles of study variables were obtained, as appropriate. Using simple logistic regression, an unadjusted odds ratio (OR) and corresponding 95% CI for each independent variable was determined using latent MTB infection status (positive or negative) of the prisoner as the outcome variable. Multiple logistic regression analysis was performed to assess simultaneously the effect of selected risk factors on the dependent variable. The inclusion of variables in the multivariable analysis was based on their biological significance, or those variables from the simple logistic regression analyses with a P <= 0.25.


    Results
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 Abstract
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
During July–September 2002, a total of 6607 prisoners resided in the five central prisons of NWFP. Of these, 425 (6%) were selected for the study: 164/2581 from Peshawar; 83/1297 from Haripur; 90/1390 from Dera Ismail Khan; 54/839 from Kohat; and 34/500 from Mardan. The response rate for both the interview and TST was 100%. Prevalence of latent MTB infection among the different prisons did not vary substantially and ranged from 47% to 49%. The overall prevalence of latent MTB infection in this study population was 48% (204/425).

Of 425 prisoners, 111 (26%) were in the age group 18–26 years, 110 (26%) were >26–34 years, 102 (24%) >34–42 years, and 102 (24%) were >42 years of age. More than half (243 or 57%) had no formal schooling. Prior to the beginning of their current sentences, the number unemployed was 96 (23%), while 320 (75%) worked on a daily wages basis. For current incarceration, 225 (52%) prisoners had been in prison for <1 year, 124 (29%) for 1–2 years, and 81 (19%) had spent >2 years in prison. There were 329 (77%) prisoners housed in barracks wherein mean area per inmate was <=60 ft2 and 96 (23%) had an average area per inmate of >60 ft2 available to them. A BCG vaccination scar was evident only in 72 (16%). Two-hundred (47%) prisoners were currently non-smokers; 122 (29%) reportedly smoked 1–5, 77 (18%) smoked 6–10, and 26 (6%) smoked >10 cigarettes per day. The number of prisoners who shared blankets, towels, or eating utensils were 201 (48%), 177 (42%), and 268 (64%), respectively (Table 1Go).


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Table 1 Characteristics of prisoners as assessed in a cross-sectional study of Mycobacterium tuberculosis infection in five prisons, North West Frontier Province, Pakistan. July–September 2001 (n = 425)
 
Based on the results of the simple logistic regression analyses, the variables included in the multiple logistic regression analysis were age of the prisoner, smoking status, educational level, duration of current incarceration, and average accommodation area of the barrack (Table 2Go). The final multivariable logistic regression model (Table 3Go) showed that prisoners aged >=42 years (adjusted OR = 3.5; 95% CI: 1.9, 6.7), with no formal schooling (adjusted OR = 2.2; 95% CI: 1.4, 3.4), those who have been in the prison for >2 years (adjusted OR = 3.4; 95% CI: 1.8, 6.4), or who have had on an average accommodation area of <=60 ft2 (adjusted OR = 2.8; 95% CI: 1.6, 4.9), or were current smokers were more likely to be TST positive. The multiple logistic regression model was also run including prison location as a fixed effect; the resultant OR did not differ from those obtained when this variable was excluded from the final model (data not shown).


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Table 2 Simple logistic regression analyses of hypothesized factors associated with tuberculin skin test status among prisoners in five prisons studied in a cross-sectional study, North West Frontier Province, Pakistan July–September 2001 (n = 425)
 

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Table 3 Multivariable logistic regression model of factors associated with Mycobacterium tuberculosis infection as assessed by tuberculin skin test in prisoners from five prisons, North West Frontier Province, Pakistan July–September 2001
 

    Discussion
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
This study estimated the prevalence of latent MTB infection in adult male prisoners of NWFP as 48%. The data on the prevalence of latent MTB infection in other prisons of the country were not available for comparison. Also, the data on the resistance pattern of potential mycobacteria that were involved were not available to us. The prevalence of HIV infection in study population was unknown and could not be assessed in the study. An earlier study, however, documented a prevalence of HIV less than 1% in prisoners of Sindh.23 Our findings on the prevalence of latent MTB infection can be compared with those reported from studies of prisons in other countries. The prevalence of MTB infection in prisons in Barcelona was 56%; this relatively high level was associated with high rates of HIV seropositivity and MTB co-infection.24 Prevalence of MTB infection in state prisons was 30% in California,25 and 20% in New York,26 with suspected transmission of infection in both settings.27 These lower rates for infection may be due to a lower prevalence of TB disease in the general US population. In a 1995 survey of prisons in Lebanon, a country similar in its stage of development and health services infrastructure to Pakistan, prevalence of latent MTB infection was found to be 45%.28

In Pakistan, prevalence of latent MTB infection in the general population is assumed to be quite high,29 and as noted earlier, the current cumulative incidence is reported to be 171 per 100 000. At 48%, the prevalence of MTB infection among prisoners seems alarmingly high and warrants immediate action for infection control. The country’s reported HIV prevalence is relatively low,23,30 but it may be an underestimation of the true situation since Pakistan lacks an appropriate disease surveillance system for case detection and reporting. There is, therefore, a potential for rapid transmission in subgroups through high-risk behaviours such as unsafe injections, unprotected sex, and general lack of knowledge of HIV/AIDS.25 The possible threat of HIV transmission in a setting where TB prevalence is already high may result in an explosive epidemic in the near future in Pakistan. In developed countries, TB was on the decline till the 1980s after which the disease became resurgent with the HIV/AIDS epidemic.31

The TST is recommended by WHO as the standard technique for mass screening of latent MTB infection.32,33 The major advantage of the test is that it can identify latent MTB infection before it develops to the disease stage; additionally, it is relatively inexpensive to perform. While a multitude of TST exist, the Mantoux test is the most quantifiable, and allows the determination of sensitivity and specificity at different cut-off points; we used cut-off points considered to reduce overestimation of infection (positivity). Current guidelines suggest that some degree of tuberculin sensitivity should be attributed to previous BCG vaccination.33 However, the test detects a reaction on the average 2–10 weeks after latent infection with MTB, and some truly infected individuals could have been missed (false negatives), leading to an underestimation of prevalence.17 Also, conditions such as malnutrition, HIV, malignancy, and even active TB can depress the body’s immune response to the tuberculin antigen; such immuno-compromised prisoners with MTB infection may have had false negative readings.

In our study, inmates over 42 years old had significantly elevated adjusted odds of TST positivity, which may represent an increasing risk of reactivation of latent MTB infection with increasing age.34,35 Length of current incarceration was strongly associated with an increased odds of latent MTB infection, and as in other studies,27 this suggests horizontal transmission or reactivation of past MTB infection due to unfavourable environmental conditions inside prisons. The inverse relationship between TST and area of accommodation is not surprising given that overcrowding is known to facilitate MTB transmission.33 In Pakistan, as in most prisons in South Asia, overcrowding and a general deterioration in environmental conditions are serious problems.36 In 1997, all prisons in NWFP housed 9291 prisoners whereas the official capacity was 7098.36 The demonstrated dose–response relationship with current cigarette smoking and tuberculin positivity is consistent with the knowledge that tobacco smoking increases both risk of MTB transmission and development of disease.37 Those with no formal education were also more likely to have MTB infection; lack of formal education may be a proxy for low socioeconomic status.

It was not possible to conduct the questionnaire interviews in strict privacy due to security reasons, and self-reported data, especially to sensitive questions (e.g. household income, occupation) may entail some response bias. Only the average accommodation area in a barrack was determined, and ecological fallacy regarding this variable may be a factor. The study design was cross-sectional, and thus limited to estimating prevalence of infection; incidence, and risk factors associated with MTB transmission in prisons warrant further evaluation using a prospective study design. Only adult male prisoners were included in this study; investigations should be extended to similar types of institutions in the country, and should include women and children.


    Conclusion
 Top
 Abstract
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
The high prevalence of latent MTB infection in NWFP prisons indicates the need to enforce infection control practices in these settings. Environmental controls in prisons including steps for the early diagnosis and appropriate treatment of TB should be instituted. Screening for TB on entry into prison using sputum smear and for latent MTB infection using TST should be done routinely. Steps like isolation and treatment of those who turn out to smear positive and chemo-prophylactic treatment of TST positive prisoners may help reduce the MTB transmission in prisons. The issue of overcrowding in prisons can be partly addressed by building more prisons. Also, an in-prison anti-tobacco campaign would have a number of public health benefits including potential reduction in MTB infection risk.


KEY MESSAGES

  • This study showed a high prevalence of latent Mycobacterium tuberculosis infection in prisoners, who may pose a risk of transmission to the wider community on their release.
  • Screening of inmates at entry to prisons and use of established treatment and control strategies may help reduce the transmission of Mycobacterium tuberculosis.
  • The issue of overcrowding in prisons needs to be addressed as a priority.
  • Future research should examine the effect of these steps.

 


    Acknowledgments
 
We gratefully acknowledge the financial support provided for this study by Health Sciences Academy, Peshawar, NWFP. We also thank the participants and project physicians for their assistance in data collection. We also recognize the co-operation extended to us by the management of prisons during the course of this study.


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 Abstract
 Materials and Methods
 Results
 Discussion
 Conclusion
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