The Risk of COVID-19 Infection in Prisons and Prevention Strategies: A Systematic Review and a New Strategic Protocol of Prevention

Health risks within prisons are well known and have worsened with the 2019 coronavirus pandemic (COVID-19), becoming a public health emergency. To date, there are more than 10 million inmates in the world; in most cases, conditions are bad and health care is scarce. A SARS-CoV-2 outbreak inside a prison is extremely rapid. The aim of this systematic review was to analyze all possible prevention techniques to reduce the risk of COVID-19 related infection within prisons. A systematic review of the literature was performed according to the PRISMA guidelines. Scopus, Web of Science, PubMed, and Google Scholar were used as search engines from 1 January 2020 to 1 November 2021 to evaluate the prevention of COVID-19 in prisoners. A total of 1757 articles were collected. Of them, 486 duplicates were removed. A total of 1250 articles did not meet the inclusion criteria. In conclusion, 21 articles were included in the present systematic review. From this analysis, it emerged that the most common COVID-19 prevention methods were the screening of the entire population (prisoners and workers) inside the prison through swab analysis and the reduction in overcrowding in prisons. Few studies concerned the prevention of COVID-19 infection through vaccination and the implementation of quarantine. To our knowledge, this is the first systematic review that evaluates the prevention of COVID-19 within jails and the real effectiveness of all possible methods used and published in the literature. Finally, a very useful strategic protocol is provided to reduce the incidence of infection and to control and manage COVID-19 in prisons.


Introduction
Health risks inside prisons, particularly in overcrowded and under-resourced ones, are well known. However, with the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic in 2019 (COVID-19), they became a public health emergency [1]. To date, in fact, there are more than 10 million prisoners around the world; in most cases, the conditions are bad and health care is poor [2]. The spacing in the cells is difficult to manage. Failure to control infection in prisons would also pose a risk to the general population. Furthermore, the increase in restrictions inside prisons could lead to a worsening of prisoners' human rights [3]. In the pandemic period, the risk of infection within prisons has been strictly related to different factors such as overcrowding, level of education, and medical and environmental conditions [4]. It is wrong to think that, since the detainees are already in isolation from the rest of the world, the hazard of COVID-19 infection is lower [5]. In fact, the general population believes that because prisons are a closed environment and

Results
Of the 21 studies included, most were observational cohort studies (40%) and ecological studies (35%), and the rest were retrospective cohort and cross-sectional studies. In most cases (60%), the studies were conducted in prisons in the United States of America (USA), with the rest in Central South America (Brazil, Guatemala, Mexico) and in Europe, such as United Kingdom (UK), Italy, and Ireland. The most common COVID-19 prevention methods were the screening of the entire population (prisoners and workers) inside the prison through swab analysis and the reduction of overcrowding in prisons. In particular, the overcrowding of prisons was guaranteed through the regulated release of prisoners with minor offenses, the reduction of visits to inmates, the reduction of prison transfers, and the decrease in the number of people inside the cell. Few studies concerned the prevention of COVID-19 infection through vaccination and the implementation of quarantine. A study conducted in Italy used both the serological test for the detection of IgM and IgG of COVID-19 and the analysis of throat swabs [23].
Regulated release worked best in overcrowded prisons to reduce the risk of infection. Reinhart, E. et al. [35] claimed that controlled decarceration reduced the infection rate by eight times in overcrowded prisons, while the use of masks reduced the infection rate by

Results
Of the 21 studies included, most were observational cohort studies (40%) and ecological studies (35%), and the rest were retrospective cohort and cross-sectional studies. In most cases (60%), the studies were conducted in prisons in the United States of America (USA), with the rest in Central South America (Brazil, Guatemala, Mexico) and in Europe, such as United Kingdom (UK), Italy, and Ireland. The most common COVID-19 prevention methods were the screening of the entire population (prisoners and workers) inside the prison through swab analysis and the reduction of overcrowding in prisons. In particular, the overcrowding of prisons was guaranteed through the regulated release of prisoners with minor offenses, the reduction of visits to inmates, the reduction of prison transfers, and the decrease in the number of people inside the cell. Few studies concerned the prevention of COVID-19 infection through vaccination and the implementation of quarantine. A study conducted in Italy used both the serological test for the detection of IgM and IgG of COVID-19 and the analysis of throat swabs [23].
Regulated release worked best in overcrowded prisons to reduce the risk of infection. Reinhart, E. et al. [35] claimed that controlled decarceration reduced the infection rate by eight times in overcrowded prisons, while the use of masks reduced the infection rate by 2.5%, while the visit ban reduced the infection rate by 1.2%. Brinkley-Rubinstein, L. et al. [30] concluded that inter-prison transfers reduced the risk of COVID-19 infection. Furthermore, the incidence of COVID-19 was lower in prisons where there was an adequate number of prisoners and in those in which detainees were housed in single-cell units [34].
Clarke, M. et al. [26] used the contact tracing team (CTT). Specifically, in cases of a suspected COVID-19 prisoner, the CTT was notified and analyzed all the contacts of this suspected case. All of these prisoners were subjected to both swabs and subsequently quarantine, regardless of the outcome of the swab. If one prisoner had a positive result, the cycle was repeated. If the prisoner was negative, the quarantine continued but the cycle of contact tracing was interrupted.
Obviously, all hygiene measures and the use of PPE were also essential for reducing the hazard of COVID-19 infection.
Finally, all of the included studies stated that the risk of COVID-19 infection in prisons was higher than in the general population, thus, prevention measures were needed to reduce the risk of transmission. In fact, Marquez, N.M. et al. [31] calculated a mortality in 2020 that was 42% higher than that of 2019, of which 80.4% was due to COVID-19. Jiménez, M.C. et al. [25] affirmed that the COVID-19 rate among incarcerated individuals was nearly three times that of the general population of Massachusetts and five times the rate in the United States. Only one study showed the effects of vaccination within prisons. Brinkley-Rubinstein et al. [32] stated that there were few studies evaluating COVID-19 and vaccination in prisons. Specifically, 2380 residents inside the prison (prisoners and staff) who had received at least one dose of vaccine were analyzed. Only 27 had tested positive for SARS-CoV-2, testifying to the vaccine's effectiveness even in the prison population. The authors concluded that the vaccine was an extremely effective tool for the prevention of COVID-19 in prisons. Table 1 summarizes the evidence from this systematic review.

Discussion
The prison population is an extremely vulnerable population [40]. There are 2.3 million people in prisons and juvenile facilities in the USA. It is estimated that in the USA the incarceration rate is equal to 698 prisoners per 100,000 inhabitants (24% of all prisoners worldwide), and the outbreak of COVID-19 made inmates particularly vulnerable [41][42][43]. In Brazil, deaths in jails accounted for 17.5% of all deaths, with a peak in Rio de Janeiro, where it was 28.5%. With the related COVID-19 pandemic, this risk has increased even more, and the Brazilian government has suspended prisoner transfers and prison visits; however, this has not slowed the incidence of the virus [44].
The COVID-19 entry routes into prisons may be different. At the beginning of the pandemic a COVID-19 entry route into prisons came from the external environment. Visitors (e.g., family members) can be a vehicle for transmitting the infection, and visits were prohibited in many countries [45][46][47]. Even the staff (e.g., cleaners, policemen, etc.), for the same reason, can be a vector of infection. In fact, initially, the incidence of COVID-19 is higher among prison staff than among prisoners. However, subsequently, the situation reversed and outbreaks among prisoners were almost unmanageable, resulting in the need for infection prevention measures [48]. In fact, the SARS-CoV-2 epidemic inside a prison is extremely fast; it was estimated that after only 30 days from the start of the pandemic, 7.8% of staff and 5.6% of prisoners were already positive for throat swab for SARS-CoV-2 [49,50]. Shen et al. [51] claims that a positive COVID-19 subject within a cell has a 60% chance of infecting the other resident of the cell. Obviously, if one inmate lives in a dormitory, the other inmate can be infected at the same time, especially considering the poor ventilation inside prisons.
An observational study evaluated the outcome of COVID-19 disease in prisoners compared to the general population. This study showed that inmates were more frequently symptomatic (fever, tachypnea, hypoxemia) and were more commonly admitted to the intensive care unit (ICU) and intubated. Finally, in-hospital mortality was more frequent in prisoners than in the general population [52]. Saloner et al. [53] calculated that the incidence of COVID-19 inside prisons was 5.5 times higher; in some facilities, prisoners had been swab screened for SARS-CoV-2 with a prevalence of 65% of positives for the total number of prisoners. The correlated COVID-19 death rate in prisons was 39 deaths per 100,000 prisoners, while in the general population it was 29 deaths per 100,000 people.
These results are consistent with those of the present systematic review. In fact, Blair, A. [19] tested some Canadian prisoners through swabs by PCR analysis for SARS-CoV-2 and found 29% positives compared with 6% of the general population (non-prisoners); mortality was 0.6%. Marquez et al. [31], on the other hand, through a retrospective cohort study using data reported by the Florida Department of Corrections, stated that, comparing mortality in prisons from 2015 to 2019 with that of 2020, mortality in 2020 was 42% higher, with 80.4% deaths related to COVID-19.
Social distancing is often recommended, but it is almost always difficult to maintain inside prisons. In the absence of recommendations from state governments, many prisons acted independently and were unable to prevent infection, developing outbreaks. According to some authors [54], action should be taken on three levels: macro level by raising the awareness of state governments; medium level through unique protection policies in cities; and at the micro level through the single detention center. The recommendations provided by the Centers for Disease Control and Prevention (CDC) [55] include the administration of mass tests through PCR obtained by means of swabs inside prisons, regardless of the presence of symptoms. The asymptomatic or pre-symptomatic subjects make up 40-45% of the totality of COVID-19 positive prisoners. The same recommendations also include the administration of SARS-CoV-2 PCR-search swabs to staff members at regular intervals, regardless of the presence of symptoms. According to Quan et al. [56], however, releasing ex-inmates can amplify the transmission of SARS-CoV-2 when they pass to the general society. Therefore, viral screening through the use of oral-pharyngeal swabs can detect infected subjects who are in an asymptomatic or pre-symptomatic phase at the time of release. This could be an effective strategy to reduce the contagion. According to an article published in the American Journal of Public Health, the prevention policy within the prison should include several measures such as: early decarceration for minor offenses, improving the ventilation of common spaces and cells, using PPE appropriately, limiting transfers of prisoners to different structures, encouraging sanitation in prisons by improving health care, and providing mental health support [57,58]. However, the early release of prisoners in a pandemic state could cause difficulties for ex-prisoners in their rehabilitation within society. This could lead to a relapse in their delinquency or, for the weaker, frail, and elderly inmates, a sort of abandonment to society [59].
In China and in South Korea, on the other hand, various preventive measures have been adopted to deal with epidemic outbreaks inside prisons. First, they have funding for the purchase of adequate PPE. Second, they saw that many outbreaks originated from the staff and spread among the prisoners, so they set up shift work for the staff. Third, they created several areas for confirmed cases and suspected COVID-19 cases [60,61]. In Australia, on the other hand, the government adopted several bans against the development of epidemic outbreaks: suspension of visits between prisoners; decrease in transfers between different prisons; temperature control for staff at the entrance; introduction of quarantine periods for new prisoners; and creation of isolation hubs for positive prisons [62,63]. Prisons in the Philippines and Pakistan have a serious problem of prison overcrowding, and it is estimated that only 25% of inmates use face masks as PPE, so the Philippine government arranged to use CTTs as a model to prevent outbreaks within prisons [64,65]. In Italy, the Ministry of Justice and Health has implemented the practices of isolating prisoners and prisons from the outside world, and the creation of a sort of CTT for the identification of suspected or confirmed COVID-19 cases. However, this measure dramatically reduced prisoners' human rights and only slightly slowed the progression of COVID-19 within prisons [66,67]. Italy also adopted other types of maneuvers to prevent COVID-19 infection within prisons, such as the possibility of home detention in cases of prisoners with less than 18 months of sentence to serve [68][69][70]. However, the release of prisoners is a highly debated topic: on the one hand, it could reduce overcrowding in prisons, but on the other hand, it would put prisoners on probation who may not have a home to live in. This could lead to an increase in crime. For this reason, some countries have tried to implement hygiene rules inside prisons [71]. In UK prisons, it has been estimated that the isolation of new inmates for 10-14 days systematically reduces the likelihood of new infections within the prison [72]. In Turkey, on the other hand, the prevention strategy is essentially based on the disinfection and decontamination of the prison environment; the suspension of all collective activities; the suspension of education, work, and training activities for prisoners; increase in PPE; 14-day quarantine for new inmates; and isolation of all suspected cases [73]. The Brazilian National Penitentiary also used the same measures, implementing PPE, freeing the elderly with serious chronic disease, reducing the number of inmates inside the cells, and suspending visits inside the prison [74]. Obviously, the situation in the poorest countries is much more serious; in fact, the prisons are almost all overcrowded, PPE is in short supply, and the risk of continuing epidemic outbreaks is extremely high. COVID-19 in these countries' prisons is virtually uncontrollable [75]. According to Brelje et al. [76], to tackle COVID-19 inside prisons, it is necessary to increase the means of screening within these structures. Symptom screening alone could cause a subtle spread of the infection, so it must be supplemented with laboratory techniques (serum and swabs). In addition, fair distribution of all PPE for residents (staff and inmates) should be encouraged. Finally, ensure access to mental health care and support for all prisoners. A case report, on the other hand, reiterates the importance of health care during the COVID-19 pandemic; clinicians should ensure the health of all patients, especially if in prison, as they live in solitude. Specifically, a 73-year-old man with heart failure, chronic kidney failure, and diabetes mellitus was admitted to a hospital near the prison due to COVID-19 related pneumonia. Throughout the hospitalization, the prisoner was intubated and remained chained to the bed; after a few days he died in complete solitude, chained, losing his human rights [77].
The findings of this systematic review are consistent with other studies. Most of the included studies, in fact, concerned the screening of internal residents (prisoners and staff) of prisons through throat swabs. This method not only allowed the detection of symptomatic positives, but also asymptomatic and pre-symptomatic subjects, blocking potential epidemic outbreaks [19,22,37,38]. Pagano et al. [23] used both PCR swab analysis and serological testing, which were equally effective. Controlled decarceration was a very useful element in reducing the incidence of COVID-19 in prisons. Reinhart et al. [35] stated that controlled decarceration reduced the infection rate by eight times in overcrowded prisons. The use of masks reduced the infection rate by 2.5%, while the visit ban reduced the infection rate by 1.2%. Another effective measure was the CTT [26]: specifically, in cases of a suspected COVID-19 prisoner, the CTT was notified and analyzed all the contacts of this suspected case. All of these prisoners were subjected to both swabs and, subsequently, quarantine, regardless of the outcome of the swab. If a subject was positive, the cycle was repeated. If a subject was negative, quarantine continued but the cycle of contact tracing was interrupted. All studies also analyzed the risk of repercussions of these measures on the mental health of prisoners, confirming a strong concern for this aspect.
To date, there are few studies that analyze the effects of the vaccination campaign inside prisons. Prisons should not be seen in isolation from the global community, but as an integral part. Since the efficacy of the COVID-19 vaccine has been established, and since inmates are a fragile population with high mortality, vaccination should be a priority in prisons. Vaccination, in fact, represents an effective weapon to reduce epidemic outbreaks, morbidity, and related COVID-19 mortality of inmates inside prisons [78,79].
In fact, in the present study, only one study showed the effects of vaccination within prisons. Brinkley-Rubinstein et al. [32] stated that there were few studies evaluating COVID-19 in prisons and vaccination. Specifically, 2380 residents inside the prison (prisoners and staff) who had received at least one dose of the vaccine were analyzed. Only 27 tested positive for SARS-CoV-2, testifying the vaccine's effectiveness even in the prison population. The authors concluded that the vaccine was an extremely effective tool for the prevention of COVID-19 in prisons.
This study is, to date, the first systematic review that highlights the main aspects of COVID-19 in prisons, showing the incidence, morbidity, and mortality within these structures and providing the most important prevention techniques to reduce the risk of infection in prisons. Through this review, a preventive strategy for the risk of contagion is provided through the application of general measures to be implemented in prisons (improvement of environmental hygiene, appropriate use of PPE, release for minor crimes, mass screening, vaccination), and local measures in cases of a positive COVID-19 subject occurring within the prison (Figure 2a,b) [72][73][74]77]. Due to the fragility of people in prison and the precarious clinical condition of many prisoners, COVID-19 vaccination should be a priority in this population [17,80]. However, the vaccination campaign in prisons is still slow and incomplete, and should be encouraged by governments [81][82][83][84][85][86][87][88][89]. COVID-19 vaccination certification, also called "COVID-19 passport" or "Green Pass" (GP), exists in many countries [86,89]. Practically, the use of this certification is used indoors, for traveling, for gyms, and for entering shops-anywhere people gather. The purpose of the GP is to allow access to these places only to those who possess it, in order to limit the spread of COVID-19, an objective that today is still an effective weapon in the battle against SARS-CoV-2 [87].
However, this systematic review shows that the use of the GP in prisons is highly debated and not unique, and visitors to prisons (family members of inmates, lawyers) are not required to show COVID-19 vaccination certification in all countries. Initially, the WHO established that it was necessary to perform a check of the conditions for all visitors inside prisons [7]. In Italy, the government established that all visitors must not show a GP at the entrance to the prison [90]. In New Zealand, on the other hand, from 9 December 2021, all prison visitors aged 12 and over must be fully vaccinated and show their GP upon arrival [91]. In South Australia, the same provision was established in October 2021 Due to the fragility of people in prison and the precarious clinical condition of many prisoners, COVID-19 vaccination should be a priority in this population [17,80]. However, the vaccination campaign in prisons is still slow and incomplete, and should be encouraged by governments [81][82][83][84][85][86][87][88][89]. COVID-19 vaccination certification, also called "COVID-19 passport" or "Green Pass" (GP), exists in many countries [86,89]. Practically, the use of this certification is used indoors, for traveling, for gyms, and for entering shops-anywhere people gather. The purpose of the GP is to allow access to these places only to those who possess it, in order to limit the spread of COVID-19, an objective that today is still an effective weapon in the battle against SARS-CoV-2 [87].
However, this systematic review shows that the use of the GP in prisons is highly debated and not unique, and visitors to prisons (family members of inmates, lawyers) are not required to show COVID-19 vaccination certification in all countries. Initially, the WHO established that it was necessary to perform a check of the conditions for all visitors inside prisons [7]. In Italy, the government established that all visitors must not show a GP at the entrance to the prison [90]. In New Zealand, on the other hand, from 9 December 2021, all prison visitors aged 12 and over must be fully vaccinated and show their GP upon arrival [91]. In South Australia, the same provision was established in October 2021 [92]. In Ireland, visitors are not required to exhibit the GP, however, the government itself says this decision is under review [93]. In the USA, all visitors must complete a vaccination certification form stating that they are fully vaccinated, or submit a negative COVID-19 test result from an approved test performed within three days before entry [94].
In any case, the crucial role of the GP in the prevention of COVID-19 infection and the promotion of the vaccination campaign is undoubted. However, in the present study, it is shown that not all countries have adopted this measure in prisons, and there is much debate on the subject. This systematic review proposes a new model that is useful to further reduce the risk of COVID-19 outbreaks within prisons, which is based on reducing the risk of transmission of SARS-CoV-2 from outside by visitors. This review involves checking body temperature at the entrance to the prison, filling out a health questionnaire, and checking the GP (Figure 3). In any case, the crucial role of the GP in the prevention of COVID-19 infection and the promotion of the vaccination campaign is undoubted. However, in the present study, it is shown that not all countries have adopted this measure in prisons, and there is much debate on the subject. This systematic review proposes a new model that is useful to further reduce the risk of COVID-19 outbreaks within prisons, which is based on reducing the risk of transmission of SARS-CoV-2 from outside by visitors. This review involves checking body temperature at the entrance to the prison, filling out a health questionnaire, and checking the GP (Figure 3).

Conclusions
The prisoner population is a highly vulnerable population, suffering from high rates of mental disorders, substance abuse disorders, poor medical conditions, old age, poorly

Conclusions
The prisoner population is a highly vulnerable population, suffering from high rates of mental disorders, substance abuse disorders, poor medical conditions, old age, poorly hygienic dormitories, overcrowded facilities, high rate of infectious diseases, morbidity, and mortality [95,96]. Initially, the policy adopted to reduce the transmission of COVID-19 was to quarantine new inmates and the replenishment of PPE. However, these measures have often contributed to worsening the mental health of prisoners, thus, measures that ensure the psychological and physical well-being of this category are needed [97][98][99][100]. In fact, it must always be borne in mind that too strict regulations can cause damage to the mental health of prisoners; therefore, when implementing anti-COVID-19 measures, it is necessary to keep this aspect in mind [101,102]. Prisons should evaluate and create innovative strategies to promote prisoners' mental health, including the establishment of periodic psychological therapies. Prisoners and all health care workers should work closely together to ensure health and infection prevention within these penitentiary facilities and provide adequate follow-up plans and periodic telemedicine appointments [103]. As noted by this systematic review, new studies about the risk of COVID-19 infection in prisons through the Green Pass Policy (GPP) should be encouraged. In fact, by comparing these results with those in which the GPP is not applied, it is possible to verify whether the GPP is effective in reducing the risk of COVID-19 infection in penitentiaries.

Proposed Strategy
As clarified in Figure 2, "general measures" and "local measures" need to be implemented in a prison. General measures are those that should be implemented within a prison, such as the appropriate use of a filtering face piece 2 (FFP2s), an effective vaccination campaign, population screening by swabs and serology for SARS-CoV-2, implementation of safety measures, isolation and quarantine, reduction in the number of prisoners in cells, and improvement of the health and hygiene of all prisoners. By "local measures", we mean those to be implemented in cases of prisoner positivity. In cases of suspected positivity, it is necessary to notify the CTT, then carry out a contact tracing operation and monitoring of symptoms. It is necessary to implement quarantine and a molecular swab for SARS-CoV-2 of all close contacts, together with psychological support. The cycle must be repeated if the result is still positive in the molecular control buffer. Figure 3, on the other hand, clarifies the measures to be implemented for all people who access prisons. It is necessary to perform the following: a body temperature check, a questionnaire on health status, and a check of the COVID-19 vaccination certificate.