https://orcid.org/0000-0002-3100-3584
Abstract
Background
People who experience incarceration are at increased risk of asthma and have a higher prevalence of risk factors associated with asthma-related mortality. However, there has been little research on the relationship between asthma and mortality in people released from prison.
Objectives
This study examined the association between asthma and all-cause and cause-specific mortality, and estimated the increased risk of asthma-related mortality among adults released from prison compared to the age- and sex-matched general population.
Design
We used data from a nested case-control sample (N = 1658) within a retrospective cohort study of all adults released from prisons in Queensland, Australia, from 1994 to 2007 (N = 42015). Deaths were identified using linkage to national mortality records. Nested study cases were sampled from deaths, with a matched control from the cohort. We examined medical and case management records to identify risk factors potentially associated with mortality. Asthma-related mortality in the cohort was compared to that of the matched general population of Queensland.
Results
People released from prison were more likely than their age and sex matched general population counterparts to have an asthma-related death (HR = 3.32 95%CI:2.14-5.16). Those who had been identified as having asthma in prison had increased odds of mortality from all-cause (OR = 1.86 95%CI:1.40-2.47), drug-related (OR = 2.5 95%CI:1.40-4.46), cardiovascular-related (OR = 3.2 95%CI:1.57-6.51), and respiratory-related (OR = 3.30 95%CI:1.63-6.70).
Conclusion
Among people exposed to incarceration, those with asthma are at elevated risk of death after release from custody. Improved management of respiratory disease in this population may contribute to reducing their high rate of preventable mortality.
Introduction
Asthma is one of the most prevalent chronic illnesses, with approximately 241 million people worldwide with the disease (Citation1). Australia has the highest reported prevalence of adult asthma (Citation2), with an estimated 10.8% (2.5 million) people (Citation3) diagnosed. Internationally, the prevalence of asthma is higher in marginalized sub-populations, including people who experience incarceration: A cross-sectional study of jail and prison inmates in the United States found that they had significantly higher risk (OR = 1.41, 95%CI 1.28-1.56) of having been diagnosed with asthma than the matched general population (Citation4). In a recent cross-sectional study of prison receptions in Australia, 22% reported having been diagnosed with asthma (Citation5).
According to the Global Burden of Disease study (Citation1), approximately 400 000 people died from asthma worldwide in 2015, equating to a rate of approximately 5.6 deaths per 100 000 persons. For the same year in Australia, the mortality rate 7.0 deaths per 100 000 persons (N = 1678) where asthma was identified as a contributing cause of death (Citation6). An inquiry into asthma in the United Kingdom reported that mortality due to asthma was preventable in two thirds of cases (Citation7), and a cross-sectional survey of Australian adults (Citation8) reported that potentially 45% of persons with asthma were not adequately controlling their symptoms, with 10% making at least one emergency department visit within a year prior to the survey.
People who experience incarceration suffer disproportionately from poor physical and mental health, and are more likely to smoke tobacco, have a history of high-risk alcohol consumption, and use illicit drugs (Citation9), which are all risk factors for mortality among asthma sufferers (Citation10). The scientific literature makes note of the elevated prevalence of asthma among people in prison, however no studies to date have quantified the association between asthma and mortality in this population.
A study on deaths of incarcerated males in England and Wales (Citation11) observed a non-significant (SMR = 1.17; 95%CI 0.68-2.01) increase in risk of asthma related death, however that study’s follow-up was restricted to time in prison where the individual’s health would be monitored and treatment would be more readily available than in the community.
The aim of this study was to examine the association between asthma and mortality in people released from prison, while controlling for other risk factors. We examined mortality associated with asthma as well as all-cause, drug-related, cardiovascular, and respiratory disease related mortality. A secondary aim was to compare the rate of asthma-related mortality in people released from prison, to that in the general population, adjusting for age and sex.
Methods
The MARC study is a retrospective cohort of all persons released from an adult correctional facility in Queensland, Australia, during the period 1 January 1994 to 31 December 2007. Correctional records for these 42 015 persons and their 87 090 releases to community during the study period were linked with the National Death Index (NDI), to identify deaths up to 31 December 2008. The probabilistic linkage was performed using name, sex, date of birth, last known state of residence, and date last known alive. All known aliases were included in the linkage process because this has been shown to improve sensitivity, without adversely affecting specificity (Citation12,Citation13).
From correctional records we obtained information on marital status, most serious offense, security classification, history of drug-related conviction, and the dates on which correctional staff documented any perceived risk of self-harm. Correctional records also included all dates of imprisonment and release, and the dates of any community-based orders, during follow-up. From the NDI we obtained information on date of death, state of death registration, year of death registration, and causes of death. Cause of death was coded using a single ICD-9 (International Statistical Classification of Diseases and Related Health Problems) code for deaths registered prior to 1997, and up to fifteen ICD-10 codes for deaths registered from 1997 to 2007.
Deaths in custody (N = 46) were removed from the cohort analysis, however any person time contributed while in community was retained. The ICD codes were grouped into logical categories of major causes of death (Citation14), with an additional asthma-related group (ICD-9: 493, ICD-10: J45-J46).
Nested case-control study
In a nested case-control study, trained postgraduate staff coded paper-based prison medical and case management records for a subset of the 2,375 individuals who died between 1994 and 2008, and a matching control for each case selected from the entire cohort (N = 42 015). Controls were matched on sex and Indigenous status, were released within 14 days of the case’s date of first release during follow-up, and had at least the same amount of follow-up time. The control’s follow-up time was truncated to their matching case. Matching did not include age in order to retain age as a measurable risk within this group.
We prioritized the coding of records by placing Indigenous people (N = 489 deaths), non-Indigenous females (N = 164 deaths), and a random selection of non-Indigenous males (N = 481) randomly into the upper half of the order of processing, followed by the remainder of the non-Indigenous males (N = 1,241 deaths) in random order. At the end of the coding period the data consisted of 829 matched pairs, comprising 35% of the total deaths in the cohort, 55% (N = 271) of the deaths in Indigenous people, 74% (N = 121) of deaths in non-Indigenous females, and 25% (N = 437) of deaths in non-Indigenous males.
The case-control data included information on medical treatments and other health-related interventions, general health problems, mental health problems, and supplied medications. These data were entered into a secure database, with a value coded as a flag of that indicator’s presence during the current or a prior incarceration, or while previously in the community. To ensure conservative ascertainment of risk factors, all missing values were coded as “not detected”.
Statistical analysis
Person-time in the community was calculated for each individual, commencing from the date of first release during the follow-up period (1 January 1994) to the end of follow-up (31 December 2008) or death, and excluded any time re-incarcerated during follow-up. We calculated the crude mortality rate and indirectly standardized mortality ratios (Citation15) for asthma-related mortality for the entire cohort, using the Queensland general population as the reference. We used the Australian Bureau of Statistics published mortality (Citation6) and population data (Citation16) for the general population of Queensland to match the prison cohort based on age and sex.
The association between asthma and mortality was investigated in the nested case-control data using a series of multivariable logistic regression models. Risk factors were selected for inclusion in age-adjusted models, based on an examination of the literature for those factors associated with mortality. An additional model was produced using a reduced number of combined risk factors, selected using SAS’s logistic regression stepwise selection (Citation17), which uses a combination of adding and removing covariates to build a model with as many covariates as possible that remain significant (SLSTAY = 0.05) when combined into a single model. Separate models were constructed for all-cause mortality, drug-related mortality, cardio-vascular disease mortality, and respiratory disease-related mortality. Asthma was not modeled as a mortality outcome in the case-control sub-study due to the low number of asthma-related deaths (N = 9) in this subset.
All analyses were carried out using SAS version 9.4 (Citation18).
Results
There were 42 015 people released from Queensland prisons from 1994 to 2007, with a median of 6.8 years and a total of 270 661 years of person-time in the community to 31 December 2008 (). During follow-up there were 2,329 deaths while in the community, of which 20 were identified as being asthma related.
Table 1. Characteristics of the full cohort (all adults released from prisons in Queensland 1994–2007) and the case-control sub-study cohort.
The 1,658 records selected for the case-control sub-study had a higher proportion of females and Indigenous persons when compared to the cohort, due to our sampling methods. The median age was higher in the sub-study, as would be expected when a group is sampled for mortality. Median person-time in community was less in the sub-study, as expected given that we sampled deceased persons and censored follow-up time for controls. The self-harm warning flag occurred less often for participants in the sub-study.
Individuals in the cohort were 3.32 times (95%CI 2.14–5.16) more likely than the age- and sex-matched general population of Queensland to die with asthma as an underlying or contributing cause (). Indigenous participants were 5.92 times (95%CI 2.46–14.3) more likely to die due to asthma-related causes, when compared to the age- and sex-matched general population.
Table 2. Asthma-related mortality (underlying and contributing) the population of adults released from Queensland prisons 1994–2007 standardized to the Queensland general population (Citation1).
Logistic modeling of the case-control sub-study for all-cause mortality () identified 13 risk factors that were significantly associated with all-cause mortality when considered individually, after adjusting for age. The stepwise-reduced model of risk factors retained asthma as a risk factor in each model, suggesting that people with asthma are 60% more likely than those without asthma to die after release from prison after controlling for age, alcohol use, enrollment in non-drug-related interventions while in prison, and having a prison medical record that had general health problems identified as cardiovascular disease, diabetes, blood borne viruses, nervous system disease, or any mental illness.
Table 3. Regression model of all-cause, drug-related, cardiovascular and respiratory disease related mortality in case-control sample of adults released from prisons in Queensland 1994–2007.
Compared to those with no asthma diagnosis, individuals with asthma were at higher risk (OR = 1.89, 95%CI 1.11–3.23) for drug-related mortality after controlling for age, blood-borne viruses, and mental illness. Individuals with asthma were at higher risk (OR = 3.36, 95%CI 1.50–7.56) for cardiovascular-related deaths, after controlling for age, cardiovascular disease, nervous system disease, and mental illness. Individuals with asthma were over 4 times more likely (OR = 4.64, 95%CI 2.24–9.60) to die of respiratory disease-related causes, after controlling for age and mental illness.
Discussion
The aims of our study were to compare the rate of asthma-related mortality in adults released from prison with that in the general population, and to consider asthma as a risk factor for mortality after release from prison. In a cohort of all adults released from prisons in Queensland over a 14-year period, we observed a crude rate of asthma-related death of 7.4 per 100 000 person-years, which was 3.3 times greater than in the general population, after adjusting for age and sex. To our knowledge this is the first study to examine asthma-related mortality in this population.
In a nested case-control study we considered asthma as a risk factor for death after release from prison. After adjusting for confounders, we found that asthma was associated with a 60% increase in the risk of death from any cause. Asthma was also associated with an increased risk of death from specific causes. Adults released from prison with asthma were 1.9 times more likely than those without asthma to die from drug-related causes. Possible explanations for this finding include that cocaine and opioid use are associated with an increased risk of severe asthma attacks (Citation19), and that illicit drug use increases the risk of life-threatening respiratory problems (Citation20). Asthma may also interact with pulmonary dysfunction due to smoking and drug use (Citation21,Citation22), which are highly prevalent among people in prisons in Australia (Citation23).
Adults released from prison with asthma were 3.4 times more likely than those without asthma to die of cardio-vascular related causes. This is likely due to the association between asthma and coronary heart disease (Citation24), although asthma medication has also been linked with cardio-vascular events (Citation25). Unsurprisingly, those with asthma were 4.6 times more likely than those without asthma to die of respiratory-disease related causes, which includes asthma-related deaths. In a model not presented here, we excluded the deaths identified as asthma-related from the respiratory mortality outcome, and found that the risk remained high (OR = 4.1, 95%CI 1.9–8.8), which may indicate that some deaths are not properly classified as asthma-related (Citation26).
Our findings reinforce previous research showing that asthma is a complicating condition that increases mortality from multiple causes (Citation27).
Our study had a few notable limitations. First, we were limited to a small number of deaths for each mortality outcome, and so necessarily reduced the number of covariates entered into the models. The results presented here would benefit from replication in a larger study. Second, we relied on resource-intensive coding of paper-based prison medical records, however correctional health providers in some jurisdictions have adopted electronic medical records, which might permit population-level data linkage and increase power for analyses. Third, our follow-up period ended in 2008, although there is no evidence that rates of asthma in prison have changed since this time, other policy changes may have impacted on mortality outcomes, and there have been large strides in asthma management. In 2014, Queensland Corrective Services adopted a smoke free policy (Citation28) which included smoking cessation support programs; these may have reduced the risks reported here, although there is evidence that the vast majority of people who desist from smoking in prison rapidly relapse upon release from custody (Citation29).
People with asthma are recommended to have a written action plan (Citation30,Citation31) which contains instructions for handling the illness. However, only 28% of Australians with asthma have such an action plan (Citation3). The proportion of people in prison with asthma who have such a plan is unknown. Some prisons in the UK have specialist respiratory care clinics for inmates to be assessed, advised and treated (Citation32). In the United States, one study reported that 26 of 41 correctional institutions had a protocol for the management of asthma, with many of those being out of date or incomplete (Citation33). Improved management of asthma in prisons and, critically, once these medically complex individuals return to the community, has the potential to reduce preventable deaths after release from prison.
Conclusions
People who experience incarceration are more likely to have been diagnosed with asthma, and are at increased risk of asthma-related death after release from prison compared to the general population. Asthma is associated with an increase in the risk of mortality related to conditions that are more prevalent among incarcerated populations, such as drug use and cardiovascular disease. The highly structured nature of correctional settings allows for highly targeted interventions both in custody, and after release (Citation34). Policy makers should take advantage of the public health opportunities presented by correctional settings, to reduce asthma-related morbidity and mortality in this population. Effective asthma interventions, monitoring and management can reduce the risk of preventable death. Prison release policies need to ensure that those individuals identified with asthma are being provided with or directed to potentially life-saving programs.
Acknowledgements
The authors wish to thank Queensland Corrective Services for provision of data and technical assistance, and the Australian Institute of Health and Welfare for assistance with data linkage. The views expressed herein are solely those of the authors, and in no way reflect the views or policies of Queensland Corrective Services. The authors also wish to acknowledge the late Professor Konrad Jamrozik for his contribution to study design. Funding: This study was funded by the Asthma Australia (https://www.asthmaaustralia.org.au) grant no. #2014001807. Study data collection was supported by NHMRC project grant no. 456107. Ethics approval was obtained from the Australian Institute of Health and Welfare, the University of Queensland, Queensland Health and Queensland Corrective Services ethics committees. S.K. was supported by an NHMRC Senior Research Fellowship (GNT1078168). R.A. was supported by an NHMRC Career Development Fellowship L2 (GNT1012485).
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