Work package 2: evaluation of an NHS prison screening programme for active tuberculosis, and survey of latent tuberculosis infection and blood-borne virus prevalence in prisoners

Our study findings relating to hepatitis C in prisoners have previously been published.39

Background/rationale

Prison populations are at an increased risk of infectious diseases including tuberculosis and blood-borne viruses.40 In London, a large continued outbreak of drug-resistant tuberculosis has had many cases that are linked to imprisonment and substance misuse,41 and research using a mobile radiographic unit for intermittent screening in prisons found a rate of tuberculosis of > 208.4 per 100,000 prisoners.3 Prisons have disproportionally large numbers of people who are infected with HIV,42 involved in substance misuse,42–44 homeless,45 and with known clinical and social risk factors for infection and progression to active disease. Prisoners with tuberculosis are also more likely to have infectious pulmonary disease, drug resistance and poor treatment outcomes.46 The prevalence of HIV and hepatitis C among prisoners is also higher than in the general population, and prisoners are among the most vulnerable population to contract hepatitis B virus (HBV) in the UK.47 In the UK, unlinked anonymous blood-borne virus monitoring showed that 10.1% of those in specialist drug services and 9.4% of those in prisons tested positive for hepatitis C, compared with 2.2% overall in primary care in 2013.48 Of all hepatitis C diagnoses, 90% are associated with injecting drug use, and 40% of those who are injecting drugs are estimated to be living with hepatitis C infection.49 The prevalence of HIV in those injecting drugs remains low, at 1.1%, and HBV prevalence has been continuously decreasing (now 17%). This has been attributed to the HBV vaccination programme in specialist drug services and in prisons, where 75% of individuals report having received HBV vaccination.

The National Institute for Health and Care Excellence recommends that prisons and immigration removal centres should have a tuberculosis liaison lead and a tuberculosis policy that is developed in conjunction with tuberculosis services and Public Health England. In prisons with Department of Health and Social Care-funded static digital radiographic facilities for tuberculosis screening, all new prisoners, detainees and transfers should have a chest radiograph within 48 hours of arrival unless they have had a chest radiograph in the last 6 months.33

In addition, NICE advises that prisons in high-incidence areas, or which receive prisoners from high-incidence areas, offer latent tuberculosis screening [interferon gamma release assay (using IGRA)] to prisoners who are aged < 35 years and in regular contact with support services, and where continued support is provided on release, including directly observed preventative treatment (DOPT).33

This part of the guidance has not been widely implemented. Little is known about the prevalence of latent tuberculosis infection in prisons. No such studies have been conducted in the UK, although a Cochrane Review found that the average incidence rate of latent tuberculosis infection in prisons in Brazil and the USA was 26.4 times that of the general population.40 The co-infection rate with latent tuberculosis infection and blood-borne viruses also needs to be established because of the potentially increased risk of hepatotoxicity in the treatment of latent tuberculosis infection with pre-existing liver disease. Furthermore, DOT is currently provided to, on average, only 60% of eligible patients (in London) with active tuberculosis,50 and the impact on health-care services of adding DOPT for prisoners who are released on preventative treatment needs to be assessed.

This study aimed to evaluate the effectiveness of a new prison radiographic screening programme using a teleradiology network of static digital radiographic units to reduce the risk from tuberculosis in prisons, and to determine the prevalence of latent tuberculosis infection and co-infection with blood-borne viruses as well as outcomes of referrals for onward care.

Methods

The primary objectives were to evaluate the effectiveness of a new prison radiographic screening programme using a teleradiology network of static digital radiographic units to reduce the risk from tuberculosis to those in prisons, and to determine the prevalence of latent tuberculosis, HIV, hepatitis B and hepatitis C infection among prisoners in London, with clinical outcomes recorded for participants referred to health-care services. Secondary objectives were to determine interobserver reliability for the interpretation of chest radiographs, and the prevalence of co-infection with latent tuberculosis, HIV, and hepatitis B and hepatitis C in prisoners in London and how this varied according to demographics and lifestyle risk factors such as alcohol and drug use.

Study design

This was an evaluation of a chest radiographic tuberculosis screening programme, and a survey of infection with latent tuberculosis, hepatitis B, hepatitis C and HIV among participants who had undergone chest radiographic screening. The study was conducted over a 6-month period between 7 January 2013 and 28 June 2013.

Ethics approval was obtained from the Offender Health and East of England – Essex National Research Ethics Service (committee number 10/H0302/51).

Setting

The setting was a male London prison with a static digital radiographic facility for tuberculosis screening. The operational capacity was 1200 prisoners, and there was a high turnover rate. The radiography machine was situated on the admissions wing, where most prisoners, with the exception of substance misusers, initially stay when they arrive in the prison, and it was used for routine radiography but not for tuberculosis screening. To assist the start of the tuberculosis screening programme, three alternating radiographers from the local NHS trust were engaged to perform radiography. The screening was conducted as 3-hour sessions 5 days per week, either in the morning or in the afternoon.

Participants for evaluation of chest radiographic screening

All new prisoners who had not had a chest radiograph in the last 6 months were eligible to participate. Other prisoners on the admissions wing were asked when possible. New prisoners arrived in the evening, and some were screened on arrival. Most new prisoners were identified from the daily admissions lists the following day. Those located on the admissions wing who were available and agreed to be screened were escorted to the radiography room by the study team. Prisoners on the substance misuse wing had to be escorted to the radiography room by a prison officer. Other prisoners were approached and offered radiography by the study team when possible.

Participants for evaluation of survey of latent tuberculosis infection and blood-borne viruses

All prisoners who had received a chest radiograph with the tuberculosis screening programme were eligible to participate in the latent tuberculosis infection/blood-borne virus screening. Following the radiography, interest in participating was noted on the radiography list. Prisoners located on the admissions wing were consented and screened immediately, when possible, or encouraged to present themselves to the study clinic during free-flow (free time). The study team also knocked on cell doors on the admissions wing and on the substance misuse wing and requested that officers unlock the cells of interested prisoners to allow them to participate. Some participants were booked into a weekly phlebotomy clinic and were escorted by prison officers.

Evaluation of chest radiographic screening

Chest radiographs were reviewed by a team of radiologists at a local NHS trust, which did not use a standard approach for reporting or categorising radiographs. Reports were e-mailed to the prison health-care medical administrator within 24 hours, printed out by the medical secretary at the prison and given to the general practitioner (GP) for review. A list of all chest radiographs with results that were indicated as negative (i.e. no abnormality detected) or positive (i.e. abnormality detected) was also sent to the research team on a monthly basis. Those prisoners with radiographs that were reported or interpreted by the prison GP as needing follow-up were offered appointments in the prison GP clinic, or were referred for advice or review as decided by the GP.

Individual consent was not sought for the study evaluating the NHS radiographic programme because anonymised data were provided for analysis. For prisoners with an abnormal chest radiograph who required follow-up, additional data on outcomes and actions taken by the prison health-care team while the individuals were inmates were provided.

As part of the evaluation of the chest radiographic tuberculosis screening and to facilitate the classification of chest radiographs, a second reading of all chest radiographs was subsequently performed by an independent consultant chest physician with extensive experience in chest radiographic screening. No clinical information was available and the reviewer was blinded to previous reports and repeat chest radiography. All personal identifiers were removed for the second reading and radiographs were reviewed using the prisoner number and XRIS (radiography) number only. The chest radiographs were categorised using the American Thoracic Society (ATS) classification system, with abnormalities defined as typically associated with active or inactive tuberculosis. This classification is currently used for the reporting of chest radiographs by the pan-London Find&Treat mobile radiographic unit tuberculosis screening service.

The reports from the second reading were then compared with the initial reports to assess interobserver reliability. A list of chest radiographs initially reported as normal or not requiring follow-up but subsequently thought to be suggestive of active tuberculosis by the second reader was sent to the prison health service with template letters to participants and their GPs requesting a medical review to exclude active tuberculosis. Participants with previous consent from the latent tuberculosis infection screening were referred directly to NHS health services by the study team when possible. The participants were also referred to the Find&Treat tuberculosis outreach service to encourage attendance.

Survey of latent tuberculosis infection and blood-borne viruses

All prisoners who had received a chest radiograph were approached to test for latent tuberculosis infection and blood-borne viruses. Informed consent was requested and, if provided, a questionnaire with sociodemographic information and self-reported risk factors for tuberculosis was completed by a study nurse. These were developed in conjunction with prisoners, and piloted and modified at the start of the study following feedback from participants. Data collected included self-reported age, country of birth, history and length of imprisonment, current and past history of substance misuse, smoking and homelessness. Those with a planned release date within 2 weeks of the screening were asked to provide contact details in the community. A whole venous blood sample was then collected for latent tuberculosis (QuantiFERON-TB Gold In-Tube gamma interferon releasing assay), HIV-1 and HIV-2 antibodies, hepatitis C (HCV-IgG, HCV-RNA) and hepatitis B (HBsAg, anti-HBs, anti-HBc – see work package 1 for further details). A phlebotomy clinic was run weekly for consented prisoners where a blood sample could not be taken on the day, and, as needed, on the substance misuse wing to maximise uptake. A link was set up with the prison information technology system and latent tuberculosis and blood-borne virus results were fed into the prisoner’s medical record. Results were also sent to the study team via e-mail. Positive blood-borne virus results were telephoned through directly to the study team by the virology department. Positive results were given in person to prisoners within 2 weeks by the study team for latent tuberculosis infection, or by the prison GP for blood-borne viruses, together with a letter explaining the results. Negative results were fed back only on request.

Based on previous studies of the prevalence of latent tuberculosis infection in high-income countries’ prison populations, we expected a minimum of 15% of participants to test positive for latent tuberculosis infection;51–55 therefore, we powered the study to measure a 15% prevalence of latent infection with 95% CIs of 12% to 18%, which required 500 participants.

For participants with a positive IGRA test who were aged < 35 years, a referral was made to the local tuberculosis clinic for prophylactic treatment as per NICE guidance. Those with HIV and latent tuberculosis infection co-infection were referred directly to joint local HIV/tuberculosis services, irrespective of age. Participants with hepatitis B, hepatitis C and HIV infection were referred to local health services depending on existing local arrangements, or asked to contact their GP to make a referral upon their release (hepatitis B and hepatitis C only).

Referral and treatment outcomes for positive cases were collated from local NHS services by study nurses at 1 year post the screening date. All study data were collected on paper forms, and then entered onto Microsoft Excel® (Microsoft Corporation, Redmond, WA, USA) 2010 spreadsheets and Microsoft Access® (Microsoft Corporation, Redmond, WA, USA) databases by the research database manager. The final data set was cleaned by the study statistician. Interobserver reliability between the hospital trust radiology department and the secondary reader for the radiographs was evaluated using Cohen’s kappa statistic. For the latent tuberculosis infection prevalence study, results were analysed using Stata version 13. A descriptive analysis of baseline variables and their association with primary and secondary outcomes was performed. Infection prevalence is presented according to exposure variables, including history of homelessness, history of drug and alcohol use and country of birth.

Results

A total of 1491 chest radiographs were taken for 1484 individuals. There were 3032 new arrivals during the study, of whom 618 (20%) arrived in the substance misuse wing. The overall screening coverage of new prisoners was 43% (1302/3032). The vast majority of radiographs that were taken were from new arrivals (87%), 1242 (84%) were from prisoners on the admission wing, 158 (11%) were from the substance misuse wing and 91 (6%) were from other wings. The total number of active screening days was 112, with an average of 13 radiographs per day.

From the initial reporting by the NHS trust radiology department, 141 out of 1491 (9%) radiographs showed some kind of abnormality (see Figure 3). Ninety-seven (69%) of these were acted on by the prison health-care team, including 29 prisoners (29/141, 20%) who had further investigations for tuberculosis. Of the 29 suspected tuberculosis cases, 15 (52%) had one or more sputum sent off for acid-fast bacillus smear and culture and sensitivity. Of these, two had a positive smear result for acid-fast bacillus; none was culture positive for Mycobacterium tuberculosis but one prisoner started tuberculosis treatment and completed a full course of antibiotics under DOT in the prison (see Figure 3). This translates into a tuberculosis rate of 67 per 100,000 prisoners. Of the other 14 cases, one was referred to the tuberculosis clinic for prophylactic treatment, three were reviewed and discharged by the prison GP, three had a computerised tomography scan (from which two cases did not suggest tuberculosis and were discharged and one case was referred to the chronic obstructive pulmonary disease nurse), three had a history of tuberculosis or atypical tuberculosis and required no action, two were lost to follow-up and two had no interventions initiated.

From the secondary reporting, 56 chest radiographs (49 individuals) were reported as suggestive of active tuberculosis. When compared with the initial reporting, 14 of the 56 radiographs (or 49 individuals) had been identified as suggestive of tuberculosis in both reports and 42 radiographs (or 35 individuals) had not been identified as suggestive of tuberculosis in the initial reporting (Table 5). The NHS trust radiology reporters classified 1.9% of chest radiographs as potentially indicating active tuberculosis, whereas the Find&Treat reporter classified 3.8% as active tuberculosis. The inter-rater reliability for suspicion of active tuberculosis was fair (κ = 0.312, 95% CI 0.181 to 0.442).

A total of 15 of the 35 individuals who had not initially been identified as having concerning radiographs had also consented to and participated in the latent tuberculosis infection screening and were referred to local chest clinics. Of these individuals, six were discharged following a review or repeat chest radiography showing no changes, seven had an unknown outcome and two were lost to follow-up. For the 15 participants who were to be contacted by the prison health-care team, no outcome data were available.

Of the 1484 prisoners screened with a chest radiograph, 595 prisoners were approached by the research team and 88% of them consented to participate in the study. The final analysis included 513 individuals (see Figure 3 for full details).

All participants were male, and the majority were born in the UK (336/513, 66%) and aged 16–39 years (404/513, 79%) (Table 6). Just over half (274/506, 54%) of participants had a history of homelessness, slept rough, sofa surfed, squatted or stayed in a homeless hostel, and 16% (81/513) had slept at a place where people used illicit drugs. The vast majority (408/513, 80%) were current smokers and around one-third (170/513, 31%) had smoked crack cocaine or heroin [with crack cocaine more commonly used (160/513, 31%) than heroin (99/513, 19%)]. Injecting drug use was less frequent (40/513, 8%), and heroin use (39/513, 8%) was higher than crack cocaine use (26/513, 5%). Four per cent of participants (21/513) reported having shared needles.

The estimated overall prevalence of latent tuberculosis infection was 13% (65/513); among this group 5% (3/65) of participants were co-infected with HCV and 6% (4/65) were co-infected with HBV. Univariable analysis demonstrated higher rates of latent tuberculosis infection in non-UK-born participants than in UK-born participants (21.5% vs. 6.3%), and in those aged 30–39 years than in those aged 16–29 years (13.5% vs. 8%).

Thirty-seven participants with a positive IGRA result were eligible for preventative treatment and referred to the local hospital chest clinic. A total of 40.5% (15/37) of participants started preventative treatment, of whom 60% (9/15) completed their treatment course and 40% (6/15) had incomplete treatment. The remaining 22/37 (59.5%) were lost to follow-up or discharged as they did not attend appointments. Prevalence of current hepatitis C was 4% (22 individuals), which in 45% of cases (10/22) was a new infection. None of these individuals was referred to a hepatitis clinic, half (5/10) were seen by a prison or community GP and the other half were lost to follow-up. Of the 12 participants with known hepatitis C infection, the majority (58%) were lost to follow-up or discharged because of non-attendance, and 5 out of 12 (42%) were under medical review by their GP or the hepatitis clinic. None of the 22 participants started hepatitis C treatment.

Prevalence of current hepatitis B was low (2%), and 70% (7/10) of the individuals with current hepatitis B had new or previously unknown infections, of whom 43% were seen by prison GPs or community GPs and 57% were lost to follow-up or discharged because of non-attendance. Of the three individuals with known HBV infection, one was referred to a hepatitis clinic, one was deported before referral and one had no interventions. Sixty-five per cent of all participants had insufficient or no immunity to HBV, and none had HIV infection.

Discussion

Our study of the tuberculosis radiographic screening programme found a tuberculosis rate of 67 per 100,000 prisoners but, as this is based on a single case, CIs are wide. In combination with the high prevalence of latent tuberculosis, and compared with the London rate of 35.5 per 100,000 Londoners,57 this indicates that prisoners remain at high risk of tuberculosis in the UK.

The lack of classification system in the initial reporting meant that radiographs were reported in a variety of ways by the different radiologists from the NHS trust. As a consequence of this, we changed a secondary objective from looking at the outcome of radiographs reported as suggestive of tuberculosis to looking at the outcome of radiographs where investigations for tuberculosis were instigated by the prison.

Prisoners were out of their cells for 3.5 hours per day and screening competed with paid prison work, attending courses that could lead to transfer to a lower-category prison or earlier release on probation, exercise and social visits. Access outside these times was very limited. During lockdown (security alert or staff meetings), no movement among prisoners was allowed, which had a further impact on the screening uptake; this, and restricted operational capacity within the research team, meant that we were unable to approach all eligible participants in the studies. Owing to the study setting, a sampling framework was not possible for recruiting patients, and we used convenience sampling.

We consider that the sample size obtained in both studies was a strength in our research. The prison population is often considered challenging to engage with, and our research nurses had extensive experience of working with prisoners as well as substance misusers. We found that both chest radiography and latent tuberculosis infection/blood-borne virus screening were highly acceptable among prisoners. We were also able to collect individual biological data, including information on self-reported clinical and social risk factors for tuberculosis, on all participants in the latent tuberculosis infection screening. These questionnaires were developed with prisoners, piloted and altered following user feedback at the start of the study. A limitation of the research was that the questionnaires were not validated for risk factors for prisoners. We used robust data collection methods, and obtained a high level of clinical outcome data.

The levels of hepatitis C and hepatitis B were lower than expected. This is probably explained by the small number of substance misusers (those with the highest risk of tuberculosis) who participated in the study as a result of the remote location of the chest radiography equipment, which was a prerequisite for the latent tuberculosis infection/blood-borne virus screening.

Many other studies have reported rates of tuberculosis in prisons. In London, sporadic radiographic screening in prisons found a rate of 208 per 100,000 prisoners. A survey from the WHO European region58 found a median notification rate of 232 (range 0–17,808) per 100,000 prisoners. Although the type and timing of screening varied, most countries performed radiographic screening at prison entry.58 The cost-effectiveness of chest radiographic screening for this high-risk population has also been demonstrated.59–61

We are not aware of any published data on tuberculosis and blood-borne virus co-infection among UK prisoners. A study of tuberculosis and blood-borne viruses in a male prison in Pakistan demonstrated higher prevalence of HIV, HBV and hepatitis C (2%, 5.9% and 15.2%, respectively), but also a higher prevalence of illicit drug use and slightly more injecting drug use.62 Other prevalence studies on sexually transmitted infections and blood-borne viruses found rates of hepatitis C between 4.9% and 29.7%, HIV of 0% and 6.6% and HBV of 2.4% and 25.2%.63–65

Other studies on latent tuberculosis infection prevalence in prisons have been carried out in various countries, although, to our knowledge, not in a UK setting. Latent tuberculosis infection rates vary considerably: 17% in the USA,15 40.3–53.3% in Spain,66 48% in Pakistan,67 49% in Brazil and 87.6–88.8% in Malaysia.68,69 Comparisons with our study results are challenging because of the heterogeneity between the studies including the different tests used for latent tuberculosis infection, varying background rates of tuberculosis, prevalence of HIV infection, eligibility criteria and levels of uptake. Chan et al.70 used QuantiFERON IGRA to assess the lifelong effect of bacillus Calmette–Guérin (BCG) vaccination and found a latent tuberculosis infection prevalence of 25% in Taiwan.

We found a continued high rate of active tuberculosis (albeit with wide CIs). Although lower than previous London estimates, this still supports the use of systematic screening for active tuberculosis among prisoners, although how this should be arranged needs further development to maximise uptake including in the most vulnerable groups, such as substance misusers. Funding for training and allocation of prison staff to carry out regular radiographic screening need to be provided, and the timing of radiography considered. Screening prisoners immediately on arrival may maximise uptake before prisoners are allocated to different wings. Another option would be to offer chest radiographic screening as an opt-out part of the ‘next-day’ health screening offered to all new prisoners. For future large-scale tuberculosis chest radiographic screenings in a prison setting, we would recommend using an established classification for the reporting of chest radiographs, such as the American Thoracic Society or the Public Health England pre-departure tuberculosis screening, to enable follow-up, analysis and comparison with other studies.

Our study also demonstrated previously unknown high levels of latent tuberculosis infection and blood-borne virus, as well as low levels of HBV vaccination despite a target vaccination programme. This indicates a high level of unmet need and highlights the inequalities in health seen within this population. The prison setting with DOT facilities provides an excellent opportunity to treat individuals with latent tuberculosis who have social risk factors, such as homelessness and substance misuse, that frequently prevent them from being offered latent tuberculosis infection treatment in the community. However, our study demonstrates extremely poor outcomes across all three infections for those referred to NHS health services following a positive result. This may partly be explained by the nature of prison services: a high and fast turnover of prisoners with limited notice, complicated follow-up and onward referral to local NHS services, and incomplete contact details in health-care records, which meant that some prisoners did not receive their results and missed out on onward care upon release. New and better performance indicators are required to improve patient pathways through the prison; however, improved co-ordination of services and follow-up support in the community is also essential to ensure continued care and treatment completion upon release. Alternative models using multidisciplinary teams and appointment sites acceptable to patients have been trialled for hepatitis C71–73 and have improved outcomes for tuberculosis in London, which has been recognised by NICE.10,26 Further research and health and social care service development are required to improve health outcomes and address the wider determinants of health in this population.

Deviations from the protocol

The planned work had been based on the assumption that the prison would start a routine radiographic screening service; as this did not happen, we provided radiographic resources to the prison to undertake screening. This reduced the numbers going through screening, preventing full evaluation. Owing to the small numbers, the planned linkage to surveillance data was abandoned as only one active tuberculosis case was identified. Participants were recruited into the study of latent tuberculosis infection and blood-borne viruses only if they had undergone radiographic screening, which also limited recruitment.