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Age-Specific Global Prevalence of Hepatitis B, Hepatitis C, HIV, and Tuberculosis Among Incarcerated People: A Systematic Review

  • Stuart A. Kinner
    Correspondence
    Address correspondence to: Stuart A. Kinner, Ph.D., Centre for Adolescent Health, Murdoch Children's Research Institute, Flemington Rd., Parkville, VIC 3052, Australia. (S.A. Kinner).
    Affiliations
    Centre for Adolescent Health, Murdoch Children's Research Institute, Parkville, Victoria, Australia

    Melbourne School of Population and Global Health, University of Melbourne, Carlton, Victoria, Australia

    Mater Research Institute-UQ, University of Queensland, South Brisbane, Queensland, Australia

    School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia

    Griffith Criminology Institute, Griffith University, Mt Gravatt, Queensland, Australia
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  • Kathryn Snow
    Affiliations
    Melbourne School of Population and Global Health, University of Melbourne, Carlton, Victoria, Australia

    Centre for International Child Health, Department of Paediatrics, University of Melbourne, Royal Children's Hospital, Parkville, Victoria, Australia
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  • Andrea L. Wirtz
    Affiliations
    Center for Public Health and Human Rights, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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  • Frederick L. Altice
    Affiliations
    Section of Infectious Diseases, Yale University School of Medicine and Public Health, New Haven, Connecticut
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  • Chris Beyrer
    Affiliations
    Center for Public Health and Human Rights, Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland
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  • Kate Dolan
    Affiliations
    Program of International Research and Training, National Drug and Alcohol Research Centre, University of New South Wales, Sydney, New South Wales, Australia
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      Abstract

      Purpose

      This study aims to compare the global prevalence of hepatitis B, hepatitis C, HIV, and tuberculosis in incarcerated adolescents and young adults (AYAs) and older prisoners.

      Methods

      This study is a systematic review and meta-analysis of studies reporting the age-specific prevalence of each infection in prisoners. We grouped age-specific prevalence estimates into three overlapping age categories: AYA prisoners (<25 years), older prisoners (≥25 years), and mixed category (spanning age 25 years). We used random effects meta-analysis to estimate the relative risk (RR) of each infection in AYAs versus older prisoners.

      Results

      Among 72 studies, there was marked heterogeneity in prevalence estimates among AYA prisoners for all infections: hepatitis B (.4%–25.2%), hepatitis C (.0%–70.6%), HIV (.0%–15.8%), and active tuberculosis (.0%–3.7%). The pooled prevalence of HIV (RR = .39, 95% confidence interval .29–.53, I2 = 79.2%) and hepatitis C (RR = .51, 95% confidence interval .33–.78, I2 = 97.8%) was lower in AYAs than in older prisoners.

      Conclusions

      The prevalence of HIV and hepatitis C is lower in AYA prisoners than in older prisoners. Despite lower prevalence, acquisition begins early among incarcerated populations. There is an urgent need for targeted, age-appropriate prevention, treatment, and harm reduction measures in and beyond custodial settings to reduce the incidence of infection in these extremely vulnerable young people.

      Keywords

      Implications and Contribution
      Preventing incident HIV and hepatitis C infection in incarcerated adolescents and young adults will require both age-appropriate prevention, treatment, and harm reduction efforts in custodial settings, and increased investment in age-appropriate, evidence-based transitional programs to support continuity of health care between prison and community.
      The world prison population is growing at a rate in excess of general population growth and is currently at least 10.35 million, with several-fold more transitioning through these settings every year [
      • Walmsley R.
      World prison population list.
      ]. The age structure of this population at the global level is unknown, but in countries where data are publicly available, young people (aged <25 years) are markedly overrepresented [
      • van Dooren K.
      • Kinner S.A.
      • Forsyth S.
      Risk of death for young ex-prisoners in the year following release from adult prison.
      ,
      • Avery A.
      • Kinner S.A.
      A robust estimate of the number and characteristics of persons released from prison in Australia.
      ,
      • Carson E.A.
      • Anderson E.
      Prisoners in 2015.
      ] and, because they are typically incarcerated for shorter periods of time than their older counterparts, they tend to cycle through custodial settings more rapidly and thus form an even larger proportion of the “churn” through these settings [
      • Avery A.
      • Kinner S.A.
      A robust estimate of the number and characteristics of persons released from prison in Australia.
      ]. Global data on detained adolescents are not available; however, it is evident that millions of adolescents and young adults (AYAs) cycle through custodial settings every year. The vast majority of these—greater than 90% in most countries where data are available—are male [
      • Carson E.A.
      • Anderson E.
      Prisoners in 2015.
      ,
      • AIHW
      Youth justice in Australia 2014-15.
      ,
      • UK Ministry of Justice
      Prison population bulletin: Weekly 3 March 2017.
      ].
      Age cutoffs for determining whether AYAs are incarcerated in juvenile justice facilities or adult prisons differ between countries, and some countries do not have a separate juvenile justice system. In the U.S., there is a further distinction between prisons (for sentences of more than 1 year) and jails (for persons awaiting trial or sentencing, or sentenced to less than 1 year). In the interests of brevity, throughout this manuscript we use the terms “prison” or “custodial setting” to describe all of these facilities, and “prisoners” to describe the people held in these facilities.
      There is a high prevalence of HIV, viral hepatitis, and tuberculosis (TB) in prisoners compared with the corresponding non-incarcerated population. A recent systematic review estimated that the global prevalence of infection among prisoners was 4.8% for hepatitis B virus (HBV), 15.1% for hepatitis C virus (HCV), 3.8% for HIV, and 2.8% for active TB [
      • Dolan K.
      • Wirtz A.
      • Moazen B.
      • et al.
      Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees.
      ]. Prevalence estimates in that study were disaggregated by sex but not by age. The concentration of infectious disease among prisoners produces an imperative to both treat those infected and prevent transmission of infection to those at risk.
      Young people in custodial settings are distinguished by a high prevalence of complex health-related needs, substance use, and sexual risk behaviour, typically set against a backdrop of trauma and entrenched social disadvantage including low education, unemployment and poverty, and increased risk of homelessness [
      • van Dooren K.
      • Kinner S.A.
      • Richards A.
      Complex health-related needs among young, soon-to-be released prisoners.
      ,
      • Kinner S.A.
      • Degenhardt L.
      • Coffey C.
      • et al.
      Complex health needs in the youth justice system: A survey of community-based and custodial offenders.
      ,
      • Golzari M.
      • Hunt S.J.
      • Anoshiravani A.
      The health status of youth in juvenile detention facilities.
      ,
      • Teplin L.A.
      • Elkington K.S.
      • McClelland G.M.
      • et al.
      Major mental disorders, substance use disorders, comorbidity, and HIV-AIDS risk behaviors in juvenile detainees.
      ,
      • Pettit B.
      • Western B.
      Mass imprisonment and the life course: Race and class inequality in U.S. incarceration.
      ]. Studies of the prevalence of infectious disease in these incarcerated young people have never been synthesized, but there is good reason to suspect that the prevalence of infection in prisoners will vary according to age. In the general population, chronic viral hepatitis and HIV prevalence are higher in older age groups, as a result of both increased time spent at risk of infection and time spent at risk before the introduction of control measures in the 1990s and 2000s [
      • Mohd Hanafiah K.
      • Groeger J.
      • Flaxman A.D.
      • et al.
      Global epidemiology of hepatitis C virus infection: New estimates of age-specific antibody to HCV seroprevalence.
      ,
      • Ott J.J.
      • Stevens G.A.
      • Groeger J.
      • et al.
      Global epidemiology of hepatitis B virus infection: New estimates of age-specific HBsAg seroprevalence and endemicity.
      ,
      • Murray C.J.L.
      • Ortblad K.F.
      • Guinovart C.
      • et al.
      Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013.
      ]. With improvements in treatment, those who are HIV infected are living longer, further contributing to higher HIV prevalence among older aged populations [
      • Murray C.J.L.
      • Ortblad K.F.
      • Guinovart C.
      • et al.
      Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990–2013: a systematic analysis for the Global Burden of Disease Study 2013.
      ]. The prevalence of TB in the general population also varies with age, as a function of both the intensity of transmission and the age structure of societies [
      • Mori T.
      • Leung C.C.
      Tuberculosis in the global aging population.
      ]. In endemic settings, TB prevalence is generally lower among AYAs than among adults in middle age and the elderly [
      • Onozaki I.
      • Law I.
      • Sismanidis C.
      • et al.
      National tuberculosis prevalence surveys in Asia, 1990–2012: An overview of results and lessons learned.
      ], whereas in high-income countries, the age-related epidemiology of TB is tied to age-specific patterns of migration [
      • Mori T.
      • Leung C.C.
      Tuberculosis in the global aging population.
      ].
      However, prisoners are not representative of the populations from which they are drawn, and are distinguished by both a relatively high prevalence of risk behaviors for bloodborne infection (e.g., injection drug use, unprotected sex, unsterile body modification practices) [
      • Kinner S.A.
      • Jenkinson R.
      • Gouillou M.
      • et al.
      High-risk drug-use practices among a large sample of Australian prisoners.
      ,
      • Hellard M.E.
      • Hocking J.S.
      • Crofts N.
      The prevalence and the risk behaviours associated with the transmission of hepatitis C virus in Australian correctional facilities.
      ,
      • Kinner S.A.
      • Winter R.
      • Saxton K.
      A longitudinal study of health outcomes for people released from prison in Fiji: The HIP-Fiji project.
      ] and comparatively poor access to vaccination, harm reduction, and other preventive measures [
      • Jürgens R.
      • Ball A.
      • Verster A.
      Interventions to reduce HIV transmission related to injecting drug use in prison.
      ,
      • Zurhold H.
      • Stöver H.
      Evidence of effectiveness of harm reduction measures in prisons: Systematic review.
      ]. Few prison settings provide adequate access to infection control measures such as sterile injecting and tattooing equipment, or condoms, and outbreaks of infection in prison settings have been documented [
      • Dolan K.
      • Wirtz A.
      • Moazen B.
      • et al.
      Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees.
      ,
      • Jürgens R.
      • Ball A.
      • Verster A.
      Interventions to reduce HIV transmission related to injecting drug use in prison.
      ,
      • Taylor A.
      • Goldberg D.
      • Emslie J.
      • et al.
      Outbreak of HIV infection in a Scottish prison.
      ]. There is some evidence that these risk behaviors are more prevalent among young and male prisoners [
      • Kinner S.A.
      • Jenkinson R.
      • Gouillou M.
      • et al.
      High-risk drug-use practices among a large sample of Australian prisoners.
      ,
      • AIHW
      The health of Australia's prisoners 2015.
      ], such that one might expect the incidence of bloodborne infections to be particularly high among young, incarcerated men. This reality is an outcome of the criminalization of substance use globally [
      • Csete J.
      • Kamarulzaman A.
      • Kazatchkine M.
      • et al.
      Public health and international drug policy.
      ].
      Furthermore, among people who inject drugs, hepatitis C seroconversion typically occurs within a few years of initiating injecting [
      • Maher L.
      • Li J.
      • Jalaludin B.
      • et al.
      High hepatitis C incidence in new injecting drug users: A policy failure?.
      ,
      • Hagan H.
      • Thiede H.
      • Des Jarlais D.C.
      Hepatitis C virus infection among injection drug users: Survival analysis of time to seroconversion.
      ], such that the prevalence of this infection may be similar in young and older prisoners, given the high prevalence of drug injection in prisoners [
      • Kinner S.A.
      • Jenkinson R.
      • Gouillou M.
      • et al.
      High-risk drug-use practices among a large sample of Australian prisoners.
      ]. In fact, some studies have reported a higher prevalence of HCV in young prisoners than in older prisoners [
      • Hellard M.E.
      • Hocking J.S.
      • Crofts N.
      The prevalence and the risk behaviours associated with the transmission of hepatitis C virus in Australian correctional facilities.
      ], although others find that despite a higher prevalence of bloodborne virus (BBV) risk behaviors in young prisoners, the prevalence of HCV infection is lower, suggesting a possibly brief window for preventive intervention [
      • van Dooren K.
      • Kinner S.A.
      • Hellard M.
      A comparison of risk factors for hepatitis C among young and older adult prisoners.
      ].
      Prisons are also high-risk congregate settings that, particularly in the absence of routine screening, treatment, and infection control, are conducive to TB transmission [
      • Baussano I.
      • Williams B.G.
      • Nunn P.
      • et al.
      Tuberculosis incidence in prisons: A systematic review.
      ]. This risk is further elevated in immunocompromised individuals, such as those living with HIV [
      • Corbett E.L.
      • Marston B.
      • Churchyard G.J.
      • et al.
      Tuberculosis in sub-Saharan Africa: Opportunities, challenges, and change in the era of antiretroviral treatment.
      ]. Given evidence that adolescents are at higher risk of progression to active TB after exposure than are adults [
      • Comstock G.W.
      • Woolpert S.F.
      Preventive treatment of untreated, nonactive tuberculosis in an Eskimo population.
      ], incarcerated youth may likewise be at comparatively elevated risk of incident TB infection. Whether or not this translates into a higher prevalence of TB infection among young people in prison settings remains unclear.

      Incarcerated youth: a global health priority

      The comparatively high prevalence of infection and associated risk behavior in prisoners makes effective prevention with this population—virtually all of whom return to the community—a public health priority [
      • Samuel M.C.
      • Doherty P.M.
      • Bulterys M.
      • et al.
      Association between heroin use, needle sharing and tattoos received in prison with hepatitis B and C positivity among street-recruited injecting drug users in New Mexico, USA.
      ]. To the extent that the prevalence of infection is lower in young prisoners than in older prisoners, the opportunity and imperative for prevention with these young people is proportionately greater. This notion of disproportionate benefit (the so-called triple dividend) was highlighted recently by the Lancet Standing Commission on Adolescent Health and Wellbeing, which both identified incarcerated adolescents as a highly vulnerable group, and identified a critical need for better data on the health of adolescents, particularly vulnerable adolescents [
      • Patton G.C.
      • Sawyer S.M.
      • Santelli J.S.
      • et al.
      Our future: A Lancet commission on adolescent health and wellbeing.
      ,
      • Patton G.C.
      • Sawyer S.M.
      • Ross D.A.
      • et al.
      From advocacy to action in global adolescent health.
      ]. Similarly, both the World Health Organization (WHO) and the United Nations have identified prisoners as a key population for HIV and viral hepatitis responses, and highlighted that young people often constitute an especially vulnerable subgroup of prisoners [
      • WHO
      Consolidated guidelines on HIV prevention, diagnosis, treatment and care for key populations.
      ,
      • United Nations
      United Nations standard minimum rules for the treatment of prisoners (the Mandela Rules).
      ].
      Through systematic review and meta-analysis, the aims of this study were to (1) compare the prevalence of hepatitis B, hepatitis C, HIV, and TB in incarcerated AYAs (aged <25 years) versus older prisoners (aged ≥25 years); and (2) compare the prevalence of each infection in incarcerated AYA males versus females. We hypothesized that there would be an age gradient in the prevalence of all infections, although this gradient would be less steep for HBV, given that vertical transmission is the key driver of HBV infection in many settings [
      • Perz J.F.
      • Armstrong G.L.
      • Farrington L.A.
      • et al.
      The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide.
      ].

      Methods

      This study involves re-analysis of data collected for a systematic review of HBV, HCV, HIV, and TB prevalence in prisoners, published previously [
      • Dolan K.
      • Wirtz A.
      • Moazen B.
      • et al.
      Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees.
      ]. The authors of the original review systematically searched the peer-reviewed and gray literature for studies published between January 1, 2005 and November 30, 2015, reporting biologically confirmed estimates of each infection. Literature searches were supplemented by requests to relevant government agencies and researchers in the field. From more than 11,000 publications identified during the initial search and call for reports, 299 articles were identified that met the inclusion criteria and provided biologic estimates of at least one of the above infections. For each included study, the authors extracted information about the location, facility type, sample size, diagnostic method, overall prevalence, and prevalence by gender and at-risk subpopulation, where reported. The authors of the original paper did not extract age-specific prevalence estimates. Full details of the original search strategy are provided in Supplementary Appendix S1.
      For the present study, we extracted age-specific data from all papers reporting age-specific prevalence for HBV infection (HBsAg), HCV seropositivity or infection (HCV-Ab or HCV-RNA), HIV infection (HIV-Ab), or active TB. Articles that did not provide any age-specific prevalence data were excluded. For the purposes of comparison, we collapsed extracted prevalence data into three age groups: AYAs (aged <25 years), older prisoners (aged ≥25 years), and mixed age groups (containing both young and older prisoners, e.g., age 20–30 years).
      To assess the relative prevalence of each condition among AYA and older prisoners, we used random effects logistic regression, which accounts for interstudy variation, and incorporated inverse double arcsine square root to calculate the pooled relative risk (RR) estimates. The meta-analysis was restricted to studies reporting infectious disease estimates for both AYA and older prisoners. Prevalence estimates for the mixed age group were excluded from these analyses. Heterogeneity was assessed using the I2 statistic, which describes the percentage of variation between studies that is due to heterogeneity rather than chance. In sensitivity analyses, we excluded studies of selected, high-risk samples from the meta-analysis. All analyses were conducted in StatsDirect version 3 (StatsDirect Ltd, Cheshire, UK).

      Results

      Of 299 publications included in the original study, 72 (24%) included age-specific prevalence estimates and were eligible for inclusion in this review (see Supplementary Figure S1). Consistent with the original study, we identified more age-specific prevalence estimates for HIV (n = 42) and HCV (n = 42) than for HBV (n = 13) or TB (n = 11). Several studies reported age-specific prevalence estimates separately for men and women [
      • Fialho M.
      • Messias M.
      • Page-Shafer K.
      • et al.
      Prevalence and risk of blood-borne and sexually transmitted viral infections in incarcerated youth in Salvador, Brazil: Opportunity and obligation for intervention.
      ,
      • Burek V.
      • Horvat J.
      • Butorac K.
      • et al.
      Viral hepatitis B, C and HIV infection in Croatian prisons.
      ,
      • Harawa N.T.
      • Bingham T.A.
      • Butler Q.R.
      • et al.
      Using arrest charge to screen for undiagnosed HIV infection among new arrestees: A study in Los Angeles County.
      ,
      • Larney S.
      • Mahowald M.K.
      • Scharff N.
      • et al.
      Epidemiology of hepatitis C virus in Pennsylvania state prisons, 2004–2012: limitations of 1945–1965 birth cohort screening in correctional settings.
      ,
      • UNODC
      Rapid assessment of HIV situation in prison settings in Ethiopia: Assessment report.
      ,
      • Viitanen P.
      • Vartiainen H.
      • Aarnio J.
      • et al.
      Hepatitis A, B, C and HIV infections among Finnish female prisoners—Young females a risk group.
      ,
      • Zhang L.
      • Yap L.
      • Reekie J.
      • et al.
      Drug use and HIV infection status of detainees in re-education through labour camps in Guangxi Province, China.
      ,
      • Rosen D.L.
      • Schoenbach V.J.
      • Wohl D.A.
      • et al.
      Characteristics and behaviors associated with HIV infection among inmates in the North Carolina prison system.
      ], and one US study reported separate estimates for jail inmates and prison inmates [
      • Nogueira P.A.
      • Abrahao R.M.
      • Galesi V.M.
      Tuberculosis and latent tuberculosis in prison inmates.
      ]. There were 37 sets of prevalence estimates from studies of exclusively male samples, and 18 sets from exclusively female samples.
      A large proportion of included studies were conducted in the WHO region of the Americas and the European region. No included studies pertaining to HBV, HCV, or HIV were identified from the Southeast Asian region. A small number of studies targeted specific risk groups, most often people who use or inject drugs [
      • van Dooren K.
      • Kinner S.A.
      • Hellard M.
      A comparison of risk factors for hepatitis C among young and older adult prisoners.
      ,
      • Kheirandish P.
      • SeyedAlinaghi S.
      • Jahani M.
      • et al.
      Prevalence and correlates of hepatitis C infection among male injection drug users in detention, Tehran, Iran.
      ,
      • Kheirandish P.
      • Seyedalinaghi S.A.
      • Hosseini M.
      • et al.
      Prevalence and correlates of HIV infection among male injection drug users in detention in Tehran, Iran.
      ,
      • Campollo O.
      • Roman S.
      • Panduro A.
      • et al.
      Non-injection drug use and hepatitis C among drug treatment clients in west central Mexico.
      ,
      • Wang H.
      • Li G.
      • Brown K.
      • et al.
      The characteristics and risk factors for HIV infection among Beijing drug users in different settings.
      ]. One study [
      • Javanbakht M.
      • Murphy R.
      • Harawa N.T.
      • et al.
      Sexually transmitted infections and HIV prevalence among incarcerated men who have sex with men, 2000–2005.
      ] recruited from a dedicated unit for incarcerated men who have sex with men (MSM), and two studies recruited prisoners attending health services while incarcerated [
      • Samuel I.
      • Ritchie D.
      • McDonald C.
      • et al.
      Should we be testing all inmates in young offender institutes for hepatitis C?.
      ,
      • Chigbu L.N.
      • Iroegbu C.U.
      Incidence and spread of Mycobacterium tuberculosis-associated infection among Aba Federal prison inmates in Nigeria.
      ]. Detailed information regarding the included studies can be found in Supplementary Appendix S1 (Tables S1–S4).

      Hepatitis B

      There were 10 published estimates of the age-specific prevalence of HBV infection in prisoners. The prevalence among AYA prisoners was highest in studies conducted in Taiwan (24.5%) and Bulgaria (25.2%), and lowest in two studies from the U.S. (.4%, .7%; Table S1).

      Hepatitis C

      There were 42 sets of age-specific prevalence estimates for hepatitis C infection among incarcerated people, including 28 estimates specific to AYA prisoners (Table S2). The highest prevalence estimates for AYA prisoners came from a study of incarcerated young men who injected drugs in Iran (67.2%), and a study of incarcerated young women in Finland (70.6%).

      HIV

      There were 42 age-specific estimates of HIV prevalence among incarcerated people, including 33 specific to AYA prisoners (Table S3). Observed HIV prevalence was highest among AYA prisoners in Nigeria (13.3%) and Zambia (15.8%), among incarcerated young men who injected drugs in Iran (10.8%), among young MSM entering jail in the U.S. (11.6%), and among young women confined in labor camps in China (13.3%).

      Active tuberculosis

      There were 11 published sets of age-specific prevalence estimates for TB among prisoners, of which only 4 contained estimates specific to AYA prisoners (Table S4). Two studies identified no young prisoners with active TB in samples from facilities in Iran [
      • Assefzadeh M.
      • Barghi R.G.
      • Shahidi S.
      Tuberculosis case—Finding and treatment in the central prison of Qazvin province, Islamic Republic of Iran.
      ] and the U.S. [
      • Risser W.L.
      • Smith K.C.
      Tuberculosis in incarcerated youth in Texas.
      ]. In contrast, young prisoners in one facility in Cameroon had a prevalence of active TB of 3.7% [
      • Noeske J.
      • Kuaban C.
      • Amougou G.
      • et al.
      Pulmonary tuberculosis in the Central Prison of Douala, Cameroon.
      ], whereas active TB prevalence among young prisoners in a facility in Bangladesh [
      • Banu S.
      • Hossain A.
      • Uddin M.K.
      • et al.
      Pulmonary tuberculosis and drug resistance in Dhaka central jail, the largest prison in Bangladesh.
      ] was observed at 1.1%.

      Sex differences among incarcerated AYA

      The majority of studies reported on samples comprised both men and women, although men were consistently the majority. There were 18 sets of age-specific prevalence estimates for incarcerated women and 37 sets for incarcerated men, of which 12 pertained specifically to incarcerated young women and 27 to incarcerated young men. The prevalence of chronic HBV infection among incarcerated young men ranged from 1.5% to 10.8%; the one study with an exclusively female sample [
      • Fialho M.
      • Messias M.
      • Page-Shafer K.
      • et al.
      Prevalence and risk of blood-borne and sexually transmitted viral infections in incarcerated youth in Salvador, Brazil: Opportunity and obligation for intervention.
      ] observed a prevalence of 8.3% (Figure S4). The prevalence of HCV infection ranged from 1.0% to 67.2% among incarcerated young men and from 3.4% to 70.6% among incarcerated young women (Figure S5). The prevalence of HIV infection was observed at .0%–13.3% among samples of incarcerated young men and across the same range for incarcerated young women (Figure S6). There were no sex-stratified estimates of the prevalence of active TB among samples of incarcerated youth.

      Relative risk of infection in AYA and older prisoners

      We used random effects logistic regression to assess the relative prevalence of each infection among AYA and older prisoners. Based on data from 25 studies, we estimated that the risk of HIV infection among AYA prisoners was 39% of that among older prisoners (RR = .39, 95% confidence interval .29–.53, I2: 79.2%). Based on data from 15 studies, we estimated that the risk of HCV infection among AYA prisoners was 51% of that among older prisoners (RR = .51, 95% confidence interval .33–.78, I2: 97.8%). Point estimates for HBV and TB (each based on three studies) were also less than one, but were not statistically significant at p < .05 (Table 1, Figure 1, Figure 2, Figure 3, Figure 4). Sensitivity analyses, excluding studies of high-risk samples for HCV (n = 3) and HIV (n = 3), produced similar findings (Table S5, Figures S2 and S3).
      Table 1Relative risk of HBV, HCV, HIV, and TB infection among AYA prisoners (aged <25 years) versus older prisoners (aged ≥25 years)
      ConditionNo. of studiesRR (95% CI)p ValueI2 (95% CI)
      HBV3.87 (.41–1.81).7046.4% (.0%–83.7%)
      HCV15.51 (.33–.78).00297.8% (97.4%–98.1%)
      HIV25.39 (.29–.53)<.00179.2% (69.7%–84.7%)
      TB3.66 (.27–1.63).3776.1% (.0%–90.7%)
      Analyses are restricted to studies reporting infectious disease estimates for both AYA and older populations. Statistical analyses were conducted in StatsDirect 3 using a meta-analysis with random effects that incorporates inverse double arcsine square root to calculate the pooled relative risk estimates. Given the expected heterogeneity between studies, all meta-analyses were performed using random effects models, which account for interstudy variation. Heterogeneity was assessed using the I2 statistic, which describes the percentage of variation between studies that is due to heterogeneity rather than chance.
      AYA =  adolescent and young adult; CI = confidence interval; HCV = hepatitis C virus; HBV = hepatitis B virus; RR = relative risk; TB = tuberculosis.
      Figure 1
      Figure 1HBV in young versus older prisoners (mixed group excluded).
      Figure 2
      Figure 2HCV in young versus older prisoners (mixed group excluded).
      Figure 3
      Figure 3HIV in young versus older prisoners (mixed group excluded).
      Figure 4
      Figure 4TB in young versus older prisoners (mixed group excluded).

      Discussion

      This systematic review identified 72 publications reporting age-specific prevalence estimates for hepatitis B, hepatitis C, HIV, and/or TB among prisoners. We hypothesized that the prevalence of each infection would be lower among AYA prisoners than among older prisoners. We found that HIV and HCV—the most prevalent infections in this population, transmitted primarily through drug injection using contaminated injecting equipment (and, in the case of HIV, unsafe sex)—were more prevalent in older prisoners than in AYA prisoners. We observed no statistically significant difference between age groups in the prevalence of either HBV or TB. There was substantial heterogeneity between studies in the prevalence of each infection, consistent with evidence that incarcerated populations both reflect and amplify the prevalence of infection in the surrounding community [
      • Kamarulzaman A.
      • Reid S.E.
      • Schwitters A.
      • et al.
      Prevention of transmission of HIV, hepatitis B virus, hepatitis C virus, and tuberculosis in prisoners.
      ]. Nevertheless, given the high prevalence of infection in incarcerated AYA, effective responses in these settings are critical to the health of young people at the population level, particularly in countries with a high incarceration rate, such as the U.S. [
      • Hammett T.M.
      • Harmon M.P.
      • Rhodes W.
      The burden of infectious disease among inmates of and releases from US correctional facilities, 1997.
      ].
      As both HIV and HCV seroconversion are irreversible, our finding that seroprevalence rose with age is perhaps unsurprising, although at least one study has reported a higher prevalence of HCV infection in younger prisoners [
      • Hellard M.E.
      • Hocking J.S.
      • Crofts N.
      The prevalence and the risk behaviours associated with the transmission of hepatitis C virus in Australian correctional facilities.
      ]. Given mounting evidence of injecting risk behavior [
      • Kinner S.A.
      • Jenkinson R.
      • Gouillou M.
      • et al.
      High-risk drug-use practices among a large sample of Australian prisoners.
      ] and associated incident HIV and HCV infection in prisons [
      • Miller E.R.
      • Bi P.
      • Ryan P.
      Hepatitis C virus infection in South Australian prisoners: Seroprevalence, seroconversion, and risk factors.
      ,
      • Teutsch S.
      • Luciani F.
      • Scheuer N.
      • et al.
      Incidence of primary hepatitis C infection and risk factors for transmission in an Australian prisoner cohort.
      ,
      • Cunningham E.B.
      • Harjarizadeh B.
      • Bretana N.A.
      • et al.
      Ongoing incident hepatitis C virus infection among people with a history of injecting drug use in an Australian prison setting, 2005–2014: The HITS-p study.
      ,
      • Dolan K.A.
      • Wodak A.
      HIV transmission in a prison system in an Australian State.
      ,
      • Taylor A.
      • Goldberg D.
      • Emslie J.
      • et al.
      Outbreak of HIV infection in a Scottish prison.
      ], coupled with inadequate coverage of evidence-based preventive measures such as needle and syringe programs and opioid agonist therapy in these settings [
      • Jürgens R.
      • Ball A.
      • Verster A.
      Interventions to reduce HIV transmission related to injecting drug use in prison.
      ], our findings point to an urgent need to scale up harm and demand reduction measures for incarcerated AYA who inject drugs to prevent another generation of vulnerable young people from acquiring life-threatening, costly infections. In settings where HIV infection is concentrated in MSM, increased access to condoms and pre-exposure prophylaxis, coupled with decriminalization of same-sex behavior, are also important elements of effective prevention [
      • Beyrer C.
      Global prevention of HIV infection for neglected populations: Men who have sex with men.
      ,
      • Jones A.
      • Cremin I.
      • Abdullah F.
      • et al.
      Transformation of HIV from pandemic to low-endemic levels: A public health approach to combination prevention.
      ].
      Because virtually all young prisoners return to the community after a relatively short period of incarceration, and given evidence of rapid relapse to drug injection after release from custody [
      • Winter R.
      • Young J.
      • Stoové M.
      • et al.
      Relapse to injecting drug use following release from prison in Australia.
      ], achieving sustained reductions in infection for these young people will require continuous support during and after their transition back to the community, including through uninterrupted provision of opioid agonist therapy for those who are opioid dependent [
      • Kamarulzaman A.
      • Reid S.E.
      • Schwitters A.
      • et al.
      Prevention of transmission of HIV, hepatitis B virus, hepatitis C virus, and tuberculosis in prisoners.
      ,
      • Larney S.
      Does opioid substitution treatment in prisons reduce injecting-related HIV risk behaviours? A systematic review.
      ,
      • Springer S.A.
      • Qiu J.
      • Saber-Tehrani A.S.
      • et al.
      Retention on buprenorphine is associated with high levels of maximal viral suppression among HIV-infected opioid dependent released prisoners.
      ,
      • Dolan K.A.
      • Shearer J.
      • White B.
      • et al.
      Four-year follow-up of imprisoned male heroin users and methadone treatment: Mortality, re-incarceration and hepatitis C infection.
      ]. Furthermore, given evidence that incarceration precipitates increased injecting risk behavior [
      • Milloy M.-J.S.
      • Buxton J.
      • Wood E.
      • et al.
      Elevated HIV risk behaviour among recently incarcerated injection drug users in a Canadian setting: A longitudinal analysis.
      ] and reduces adherence to ART among those who are HIV positive [
      • Milloy M.J.
      • Kerr T.
      • Buxton J.
      • et al.
      Dose-response effect of incarceration events on nonadherence to HIV antiretroviral therapy among injection drug users.
      ,
      • Westergaard R.P.
      • Kirk G.D.
      • Richesson D.R.
      • et al.
      Incarceration predicts virologic failure for HIV-infected injection drug users receiving antiretroviral therapy.
      ], efforts to minimize the incarceration of at-risk young people are important to preventing the further spread of infection [
      • Csete J.
      • Kamarulzaman A.
      • Kazatchkine M.
      • et al.
      Public health and international drug policy.
      ,
      • Altice F.L.
      • Azbel L.
      • Stone J.
      • et al.
      The perfect storm: Incarceration and the high-risk environment perpetuating transmission of HIV, hepatitis C virus, and tuberculosis in Eastern Europe and Central Asia.
      ]. Among studies presenting sex-specific estimates, high HIV or HCV seroprevalence was more often observed among young women than young men, consistent with previous findings that incarcerated women have a particularly high prevalence of HIV and HCV infection, driven largely by a higher prevalence of injection drug use and higher rates of unsafe injecting practices, primarily in the context of intimate relationships [
      • Macalino G.E.
      • Hou J.C.
      • Kumar M.S.
      • et al.
      Hepatitis C infection and incarcerated populations.
      ,
      • Tracy D.
      • Hahn J.A.
      • Fuller Lewis C.
      • et al.
      Higher risk of incident hepatitis C virus among young women who inject drugs compared with young men in association with sexual relationships: A prospective analysis from the UFO Study cohort.
      ].
      We found comparatively few studies that reported age-specific prevalence estimates for HBV or TB, and no evidence that the prevalence of these infections was different among incarcerated AYAs and older prisoners. HBV prevalence among incarcerated young people from high HBV prevalence settings is largely determined by control of mother to child transmission at the time they were born, whereas among prisoners from low prevalence countries, HBV prevalence is more likely to reflect transmission via sexual behavior and injecting drug use [
      • Ott J.J.
      • Stevens G.A.
      • Groeger J.
      • et al.
      Global epidemiology of hepatitis B virus infection: New estimates of age-specific HBsAg seroprevalence and endemicity.
      ,
      • Nelson P.K.
      • Mathers B.M.
      • Cowie B.
      • et al.
      Global epidemiology of hepatitis B and hepatitis C in people who inject drugs: Results of systematic reviews.
      ]. The HBV vaccine was introduced in the late 1980s; however, global coverage of the three-dose schedule is currently estimated at 83% and coverage of the birth dose at only 39% [
      • WHO
      Immunization coverage.
      ]. In some settings, the current cohort of incarcerated youth will be fully vaccinated, whereas in countries that have only recently implemented national HBV vaccination programs, it will be some time before fully vaccinated cohorts begin entering the prison system. Free hepatitis B vaccination for all prisoners is recommended as part of the United Nations Office on Drugs and Crime “comprehensive package” for responding to HIV and other infections in prison settings [
      • UNODC
      Policy brief: HIV prevention, treatment and care in prisons and other closed settings: A comprehensive package of interventions.
      ].
      The comparative dearth of studies on HBV among prisoners compared with those on HCV is notable. Although HCV is more common among people who inject drugs due to much lower rates of spontaneous clearance, HBV presents an equal threat to the health of those who do develop chronic infection. In addition, HBV in an adult from an endemic area may represent an infection acquired at birth, which HCV rarely does; thus even a young adult with HBV may have lived with the infection for multiple decades and may be at high risk of progression to advanced liver disease in the near future. The burden of HBV among AYA prisoners, particularly those living in high prevalence countries, merits increased attention. Increased vaccination coverage for young people who experience incarceration, particularly in endemic areas, should be a priority [
      • Kamarulzaman A.
      • Reid S.E.
      • Schwitters A.
      • et al.
      Prevention of transmission of HIV, hepatitis B virus, hepatitis C virus, and tuberculosis in prisoners.
      ].
      Documented TB prevalence among people over the age of 15 years in the general population in endemic countries varies markedly by setting, but is very rarely in excess of 1% of the population [
      • World Health Organization
      Global tuberculosis report.
      ]. The prevalence estimates reported here demonstrate a very substantial burden of disease in prisoners compared with the general public, including among incarcerated youth in the studies from Cameroon [
      • Noeske J.
      • Kuaban C.
      • Amougou G.
      • et al.
      Pulmonary tuberculosis in the Central Prison of Douala, Cameroon.
      ] and Bangladesh [
      • Banu S.
      • Hossain A.
      • Uddin M.K.
      • et al.
      Pulmonary tuberculosis and drug resistance in Dhaka central jail, the largest prison in Bangladesh.
      ]. Although TB prevalence is generally lower among young people in the general population, we found no age gradient in the prevalence of this infection in prison. One possible explanation for this finding is that, whereas BBV infections are often acquired in the community before incarceration, active TB among prisoners will very often reflect recent transmission. In many prison settings, access to diagnosis and treatment for TB is limited, as is capacity to isolate those who are infected. Prison overcrowding is a widespread problem, but is often particularly acute in low- and middle-income countries where TB is endemic [
      • Baussano I.
      • Williams B.G.
      • Nunn P.
      • et al.
      Tuberculosis incidence in prisons: A systematic review.
      ,
      • Simooya O.O.
      Infections in prison in low and middle income countries: Prevalence and prevention strategies.
      ,
      • O'Grady J.
      • Hoelscher M.
      • Atun R.
      • et al.
      Tuberculosis in prisons in sub-Saharan Africa—The need for improved health services, surveillance and control.
      ]. The incarceration of young people in adult prisons is likely to expose them to markedly higher risks of TB infection and disease than they would face in the community [
      • Baussano I.
      • Williams B.G.
      • Nunn P.
      • et al.
      Tuberculosis incidence in prisons: A systematic review.
      ]. Therefore, efforts to prevent the incarceration of young people in these settings—particularly those who are more vulnerable to infection due to HIV-related immunosuppression—may reduce the incidence of TB in vulnerable AYAs.
      Chronic hepatitis, HIV, and TB contribute significantly to the global burden of disease [
      • Kassebaum N.J.
      • Arora M.
      • Barber R.M.
      • et al.
      Global, regional, and national disability-adjusted life-years (DALYs) for 315 diseases and injuries and healthy life expectancy (HALE), 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015.
      ], and typically have profound implications for the life expectancy and life choices of young people who acquire these infections. Obtaining reliable epidemiological data is a first essential step in developing evidence-based responses, and funding them at a scale proportional to need. Our findings add support to calls for more, better, and more consistent data on the health of young people, particularly vulnerable groups such as those exposed to the criminal justice system [
      • Patton G.C.
      • Sawyer S.M.
      • Santelli J.S.
      • et al.
      Our future: A Lancet commission on adolescent health and wellbeing.
      ,
      • WHO
      Consolidated guidelines on HIV prevention, diagnosis, treatment and care for key populations.
      ].

      Limitations

      This study provided the first comprehensive review of published, age-specific prevalence estimates of bloodborne viral infections and active pulmonary TB among prisoners. The reviewed studies spanned a wide variety of detention settings, including prisons, jails, labor camps, youth detention facilities, and compulsory drug treatment facilities, although remarkably few studies of detained juveniles were identified. Further research on the health status of detained juveniles, particularly in low- and middle-income settings, should be a priority.
      We observed substantial heterogeneity in prevalence estimates between studies; this is to be expected given the diversity of geographical and epidemiological settings of included studies. Strategies for preventing and responding to these infections are likely to differ markedly between settings; however, consideration of these differences was beyond the scope of this review. A large proportion of studies was conducted in upper middle- or high-income countries from the European region and the region of the Americas, and only one study was identified from the Southeast Asian region [
      • Banu S.
      • Hossain A.
      • Uddin M.K.
      • et al.
      Pulmonary tuberculosis and drug resistance in Dhaka central jail, the largest prison in Bangladesh.
      ]. Among the 299 studies identified in the original systematic review [
      • Dolan K.
      • Wirtz A.
      • Moazen B.
      • et al.
      Global burden of HIV, viral hepatitis, and tuberculosis in prisoners and detainees.
      ], those reporting age-disaggregated prevalence estimates were disproportionately from high-income countries (56% of studies with age-disaggregated data vs. 46% of those without). Our findings may not generalize to low-income countries, and further research in these settings is urgently required.
      We also observed significant heterogeneity in estimates of the RR of infection between AYA and older prisoners. As such, our meta-analysis findings should be interpreted with caution, although inspection of forest plots suggests that this heterogeneity is largely a function of variation in the magnitude rather than the direction of RR estimates: in other words, the finding that HCV and HIV infection were less prevalent among AYA was reasonably consistent, although the extent to which the prevalence of infection was lower in young prisoners varied between studies.
      Some studies recruited high-risk samples; however, exclusion of these in sensitivity analyses had minimal impact on our estimates. Other studies may have only or preferentially tested symptomatic individuals; prevalence estimates in these studies may have been inflated. Screening algorithms for TB were inconsistent, with different studies using different combinations of symptom screening, chest x-ray, and microbiologic testing. This is consistent with the greater challenge of mass TB screening due to the absence of a high-performance, gold-standard test. No study attempted to identify patients with extrapulmonary TB, which constitutes more than 30% of disease in some countries [
      • Norbis L.
      • Alagna R.
      • Tortoli E.
      • et al.
      Challenges and perspectives in the diagnosis of extrapulmonary tuberculosis.
      ]—as such, the prevalence estimates for TB presented here will underestimate the true burden of disease. Several studies only provided microbiologic testing to participants who reported TB symptoms, which is known to reduce case detection, as up to 30% of people with pulmonary TB may be asymptomatic [
      • WHO
      Systematic screening for active tuberculosis: Principles and recommendations.
      ].
      The present study was able to include only one in four studies from the original review (i.e., those that included age-disaggregated prevalence estimates) and, among these, heterogeneity in age categories hampered data synthesis. This is a perennial problem for meta-analysis and a well-recognized challenge for research on AYA health [
      • Patton G.C.
      • Sawyer S.M.
      • Santelli J.S.
      • et al.
      Our future: A Lancet commission on adolescent health and wellbeing.
      ,
      • Patton G.C.
      • Coffey C.
      • Cappa C.
      • et al.
      Health of the world's adolescents: A synthesis of internationally comparable data.
      ]. One possible solution for future research is to employ individual patient data meta-analysis, in which primary data are reanalyzed in a coordinated fashion, to increase data harmonization and potentially permit inclusion of additional studies [
      • Riley R.D.
      • Lambert P.C.
      • Abo-Zaid G.
      Meta-analysis of individual participant data: Rationale, conduct, and reporting.
      ].
      In conclusion, the prevalence of HIV and hepatitis C among incarcerated AYAs is high, but lower than among older prisoners. Given the high background prevalence of infection, persistence of BBV risk behaviors, and inadequacy of infection control measures, prisons are extremely high-risk settings for the transmission of infection for these young people. As a primary measure, every effort should be made to reduce incarceration of AYAs, and to prevent incarceration for substance use and substance use disorders [
      • Csete J.
      • Kamarulzaman A.
      • Kazatchkine M.
      • et al.
      Public health and international drug policy.
      ]. The window of opportunity for preventing infection in incarcerated AYA is likely brief and will require both age-appropriate prevention through adoption of evidence-based harm reduction measures and rapid scale-up of in-prison treatment for HIV and HCV, and associated conditions such as opioid dependence and mental disorder [
      • Altice F.L.
      • Azbel L.
      • Stone J.
      • et al.
      The perfect storm: Incarceration and the high-risk environment perpetuating transmission of HIV, hepatitis C virus, and tuberculosis in Eastern Europe and Central Asia.
      ]. There is good evidence for both the effectiveness and the acceptability of these responses, but uptake remains poor in many settings. Given that most AYAs spend a relatively short time in custody before returning to the community, improved continuity of care between prison and community is also essential to reducing the incidence of infection, and associated morbidity and mortality, in these highly vulnerable young people.

      Funding Sources

      This work was supported by grants to the Center for Public Health and Human Rights at Johns Hopkins Bloomberg School of Public Health from the National Institute on Drug Abuse ; the Open Society Foundations ; the United Nations Population Fund ; MAC AIDS ; the Bill and Melinda Gates Foundation ; the Johns Hopkins University Center for AIDS Research , a National Institute of Health (NIH)-funded programme P30AI094189 . S.A.K. receives salary support from NHMRC Senior Research Fellowship APP1078168 . F.L.A. received funding from the National Institutes on Drug Abuse ( R01 DA025943 , R01 DA041271 , R01 DA029910 , R01 DA030768 , R01 DA030762 , and K24 DA017072 ). K.D. is funded by the Australian National Drug and Alcohol Research Centre .

      Appendix. Supplementary Data

      The following is the supplementary data to this article:

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