Seroprevalence and Associated Risk Factors of Hepatitis B and C among Inmates of Port Harcourt Maximum Security Custodial Centre ()
1. Introduction
Prisoners worldwide form a sizeable portion of the most at-risk populations and are recognized for the increased level of infectious diseases such as Hepatitis B (HBV) and Hepatitis C (HCV) which affect both inmates and prison staff; these rates surpass those in the general population [1] . Long-term confinement in an environment with a high risk of overcrowding, poor nutrition, a dearth of medical treatment, and homosexuality is the norm for prisoners [2] [3] . Thus, prisoners are susceptible to infectious diseases and, after release from these correctional facilities, might go on to spread the infections in their communities spread the disease in their communities.
Inmates often come from marginalized populations, such as injecting drug users (IDUs) and persons with high-risk sexual behaviours (including sex workers), who are already at an increased risk for these infections (Niveau, 2006 [4] ), which all contribute to a high risk of transmission and prevalence of viruses such as HBV, and HCV [5] . Risky behaviours, such as homosexuality, injecting drug use and sharing sharp objects amongst others, contribute to the spread of these infections [6] . Female inmates are abused sexually by prisoners and non-prisoners. They also have problems with the availability of sexual and reproductive health needs thereby exposing them to infections. It has been further documented that in many prisons studied, people in prisons often exchange hygiene products, food, and personal items for sex [7] . Further compounding the situation is inadequate training for prison staff as well as poor medical and social services.
Africa, particularly Sub-Saharan Africa, is distinguished by a poor criminal justice and legal system, which harms the prison system - overcrowding, and mixing of un-sentenced and convicted persons [8] . Moreover, no particular health initiatives are addressing the prevention and spread of HBV infection in Nigerian prisons. The lack of HBV screening and vaccination of inmates has led to asymptomatic carriers fuelling the infection transmission chain through high-risk behaviours and practices [9] .
Viral Hepatitis B is a devastating disease and a major global health problem and is an important cause of mortality globally [10] . Globally, about 296 million have chronic infections and become carriers of the virus, and there are over four million acute clinical cases of HBV every year [11] . Complications of chronic HBV infection such as chronic hepatitis, cirrhosis, and hepatocellular carcinoma accounted for an estimated 820,000 deaths in 2019 [11] . Despite the availability of a safe and efficient vaccine, Nigeria remains highly endemic for HBV infection. Likewise, an HBV seroprevalence of 12.2% was documented in the first Hepatitis B national survey among asymptomatic Nigerians [12] . Although some inmates had acquired HBV infection before incarceration, there are also growing shreds of evidence through prospective cohort studies of ongoing HBV infection transmission among inmates.
The Hepatitis C virus (HCV) represents one of the most prevalent forms of bloodborne viruses among prisoners [13] . Acute and chronic hepatitis, which can range in intensity from a minor condition to a severe, life-long condition including liver cirrhosis and cancer, can both be brought on by the hepatitis C virus. Around 1.5 million new cases of the hepatitis C virus are reported each year, with an estimated 58 million individuals worldwide carrying the illness, approximately 290,000 people died from hepatitis C, majorly from cirrhosis and hepatocellular carcinoma (primary liver cancer). HBV and HCV all have similar modes of transmission; however, HCV has low sexual transmission. HBV is transmitted in the same way as: by contact with the blood or body fluids of an infected person. However, HBV is 10 times more infectious than HCV. The most efficient mode of transmission of HCV is direct percutaneous exposure to infectious blood [14] .
Prisoners have a greater incidence of blood-borne diseases in many nations. Results from a study showed that the overall prevalence of hepatitis B in prisoners was 5.17%. The highest prevalence, that is, 13.14%, was observed in Africa. According to the World Health Organization (WHO) classification, the highest prevalence, that is, 5.04%, was observed in the Western Pacific region. The results showed that the overall occurrence of hepatitis C in prisoners was 13.22% [11] . The highest prevalence, that is, 26.4%, was observed in Australia. According to the WHO classification, the highest prevalence of hepatitis C, that is, 24.26%, was observed in the Southeast Asia region [15] .
As components of the criminal justice system, prisons are anticipated to hold approximately 11 million individuals globally, including 70,797 inmates in Nigeria as of December 2021 [16] . In Nasarawa State, the prevalence of HBV and HCV were determined to be 23.0% and 12.3%, respectively [17] . Similar research was undertaken on inmates in Sokoto, Nigeria; HBV and HCV seroprevalence rates were 11.1% and 4.0%, respectively [18] . Approximately 29.6% frequency of Hepatitis C infection was detected in Calabar Prison, Cross Rivers state [19] . The frequency of HBsAg among Kuje prison inmates in Nigeria was estimated to be 13.7% in a recent study [9] . Multilevel risk factors have been substantially ascribed to the increased incidence and prevalence of various diseases in jails. Individual risk behaviours such as unprotected sexual activity and the sharing of injecting equipment are included. Despite the fact that these harmful behaviours are rigorously prohibited by the authorities in correctional facilities, some of them persist [20] .
The prison population is not static, as inmates are being incarcerated and some gaining freedom, posing a public health concern to not just the population within the prison, but also to those outside as they associate with society upon release. It becomes significant to continually study the prevalence of these infectious diseases, offering opportunities for intervention and policy changes; hence the need for this study which investigated the seroprevalence of HBV and HCV as well as the risk factors associated with these viral infections among inmates.
2. Materials/Methods
2.1. Study Design
The study was conducted from July to December 2022 using a cross-sectional design with multi-stage sampling. Prior to further categorization, inmates were separated into their respective sexes. Males were designated random numbers for systematic random sampling, while females, who were significantly fewer in number than males, were selected from all qualified candidates. The sample interval was set to 5 and the initial number was selected at random.
2.2. Study Area
The research was conducted at the Port Harcourt Maximum Security Custodial Centre in the Port Harcourt City Council Area of Rivers State, Nigeria. In the course of the study, the number of inmates was approximately 4,000 as new inmates were taken into custody or released. The entire area encompasses roughly 109 square kilometres of land. The institution accommodates inmates with a variety of criminal backgrounds, including those awaiting trial, those convicted, and those sentenced to death [21] . It is a correctional facility for both male and female offenders, with approximately 85% of its capacity designated for male prisoners and 15% for their female counterparts [22] .
2.3. Study Population and Sample Size Determination
The study population comprised inmates in the Port Harcourt Maximum Security Custodial Centre, Port Harcourt. These groups of individuals are faced with many challenges, including overcrowding, poor conditions, and limited access to healthcare services, which can contribute to the spread of infectious diseases. The sample size was calculated based on the expected prevalence of HBV infection among Kuje prison inmates in Nigeria as reported by Dan-Nwafor et al. (2021) [9] which revealed a prevalence of 13.7% was used to calculate the minimum sample size as follows.
Using the formula by Naing et al. (2006) [23]
(1)
where;
n = minimum sample size;
Z = standard deviation corresponding to 95% confidence level set at 1.96;
p = proportion = 13.7% = 0.137;
q = 1 − p = 0.863;
d = desired precision, 5% (0.05).
Therefore,
However, an additional 18 subjects (10%) were recruited to account for anticipated drop-out or missing data while carrying out the study. Therefore, a total of 200 subjects were enrolled in the study.
2.4. Inclusion and Exclusion Criteria
Consenting inmates were recruited, while those who were absent at the time of sampling or refused consent were excluded.
2.5. Data Collection
In gathering sociodemographic and behavioural information, participating inmates were interviewed and administered a structured questionnaire. There were a total of 28 items with 9 of those items being in the sociodemographic information section while 19 items were contained in the behavioural risks section. The questionnaire was adapted from previous research with a similar study design [19] .
In order to preserve anonymity, names were omitted from the questionnaire and serial numbers were used instead to track subjects and findings. For further coupling of the outcome and subject, the serial number on each questionnaire was replicated on the sample bottle.
2.6. Specimen Collection
Five millilitres (5 ml) of blood were collected from each subject and dispensed into a sterile plain container and allowed to clot. The serum obtained was used for serological diagnosis of HbsAg and HCV antibodies.
2.7. Assay Procedure
Serum samples were used for the assays. The HBV and HCV assays were performed using serum immunochromatographic rapid diagnostic tests (RDTs) for HBV (HbsAg) and HCV (Anti-HCV) by ACON laboratories incorporated, USA. The serological protocol is a qualitative immunoassay detection of hepatitis B surface antigen and IgG antibodies of hepatitis C virus in the sample serum respectively.
2.8. Data Analysis
The obtained data were entered and cleaned using Microsoft Excel and subsequently exported to Graph Pad Prism version 9 for statistical analysis. Descriptive and inferential statistics were conducted with the level of significance set at p < 0.05 with a 95% confidence interval.
2.9. Ethical Considerations
Subjects were duly informed about the study's aim before providing informed consent, with an emphasis on maintaining data confidentiality. The investigation was conducted in accordance with global ethical standards.
3. Results
A total of 200 inmates were involved in this study with a mean age of 33.23. The majority of them were between the ages of 21 - 30 (43.5%) and 31 - 40 years (36.5%). About 69% of inmates were males while 31% were females. Among the studied inmates, the majority were single (72.5%), 60% of the participant had completed their secondary school education and 54% of the inmates were self-employed. Christians were preponderant against other religions (94%), and then 26 inmates (13%) had previous incarceration. The majority of the inmates have been in the prison between 1 - 3 years (44%) as shown in Figure 1(a) and Figure 1(b) below.
The seroprevalence of Hepatitis B and Hepatitis C among the inmates in the current study were 4% and 3.5% respectively with no cases of co-infections reported as shown in Figure 2.
In the current study inmates aged between 21 - 30 years (4.6%) and those aged between 31 - 40 years (5.5%) had a higher prevalence of HBV than other age groups, a higher prevalence was also reported among male subjects (5.8%) as well as among single subjects (4.8%), those in monogamous marriages had a higher prevalence (2%) than their polygamous counterparts. Stratification by the level of education revealed that inmates with at least a primary education had a higher prevalence of HBV (9.3%). Unemployed subjects had a higher prevalence of HBV infection (7.1%) followed by those in private employment (6.3%). Christians in the study had a higher prevalence of HBV (4.3%) than inmates affiliated with other religious practices. Previously incarcerated inmates had a lower HBV infection (3.8%) than those without previous incarceration (4%). Inmates who have been incarcerated between 1 - 3 years had a higher prevalence of HBV infection (8%) than those with less than a year in prison (2.2%) and those incarcerated for over 4 years. However, it was observed that the age, sex, marital status, type of marriage, level of education, occupation, religion, previous incarceration and duration of current incarceration of the inmates were not significantly associated with the seropositivity of HBV infection (p > 0.05) as evident in Table 1.
As regards risky behaviours associated with HBV infection, blood oath-taking
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Figure 1. The sociodemographic distribution of the sampled inmates.
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Figure 2. The seroprevalence of Hepatitis B and Hepatitis C infection.
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Table 1. Prevalence of Hepatitis B and sociodemographic risk factors of inmates.
*Statistical significance p < 0.05.
was significantly associated with HBV infection (p = 0.0036) in the current study, with inmates with a history of blood oath-taking being 6.7 times more likely to be infected with HBV than those who had never taken blood oaths. An HBV prevalence of 13.8% was reported amongst inmates who had taken blood oaths. There was also a significant association between HBV infection and history of surgery (p = 0.0426) as 11.1% of inmates with a history of surgery were positive for HBV. Inmates with a history of surgery were 4.2 times more likely to be infected with HBV than those without a surgical history. A higher prevalence of HBV infection was reported among inmates with a history of alcohol use (4.8%), those with a body piercing (7.5%), inmates with a tattoo (4.6%), inmates with a history of illicit drug use (5.2%), those who share personal belongings (5.7%) and sharp objects with other inmates (5.5%), however, these risky behaviours were not found to be significantly associated with HBV infection. A higher prevalence of HBV infection was also found among inmates with multiple sex partners (5.2%), inmates having sex with non-marital partners (4.7%), inmates with 6 - 10 lifetime sexual partners (9.8%), inmates engaged in homosexuality (8.3%), those involved in transactional sex (4.8%) as well as those with a history of sexually transmitted infections (6.3%); these risky behaviours were also not found to be significantly associated with HBV infection (p > 0.05) as shown in Table 2.
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Table 2. Prevalence of Hepatitis B and behavioural risk factors of inmates.
*Statistical significance p < 0.05.
Inmates aged between 21 - 30 years (4.6%) and those aged between 31-40 years (2.7%) had a higher prevalence of HCV than other age groups, a higher prevalence was also reported among male subjects (5.7%) as well as among married subjects (5.9%), those in monogamous marriages had a higher prevalence (6.1%) than their polygamous counterparts. Stratification by the level of education revealed that inmates with at least a secondary education had a higher prevalence of HCV (5%). Privately employed subjects had a higher prevalence of HCV infection (6.3%) followed by those self-employed (3.7%). Christians in the study had a higher prevalence of HCV (3.2%) than inmates affiliated with other religious practices. Previously incarcerated inmates had a slightly higher prevalence of HCV infection (3.8%) than those without previous incarceration (3.4%). Inmates who have been incarcerated between 1 - 3 years had a higher prevalence of HCV infection (6.8%) than those with less than a year in prison (2.2%) and those incarcerated for over 4 years. However, the current study did not significantly associate the age, sex, marital status, type of marriage, level of education, occupation, religion, previous incarceration and duration of current incarceration of the inmates with the seropositivity of HCV infection (p > 0.05) as shown in Table 3.
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Table 3. Prevalence of Hepatitis C and behavioural risk factors of inmates.
*Statistical significance p < 0.05.
The study observed a significant association between blood oath-taking and HCV infection (p = 0.031) with inmates with a history of blood oath-taking being 4.8 times more likely to be infected with HCV than those who had never taken blood oaths. An HCV prevalence of 10.3% was reported among inmates with a history of blood oath. A significant association was also reported between HCV infection and illicit drug use (p = 0.0449) with inmates involved in illicit drug use being 6.7 times more likely to be infected with HCV than those not involved in illicit drug use. The prevalence of HCV among inmates who engage in illicit drug use was 6.2%. Additionally, sex with non-marital partners was found to be a significant association with the prevalence of HCV infection (p = 0.0457), with 5.4% of inmates who have had sexual intercourse with non-marital partners testing positive for HCV; the odds of being infected with HCV among inmates involved in sex with non-marital partners were found to be infinitely higher than those not involved in such sexual practice. Additionally, a higher prevalence of HCV infection was reported among inmates with a history of alcohol use (4.1%), those who shave hair locally (5%), inmates with a tattoo (4.3%), those who share personal belongings (4.9%) and sharp objects with other inmates (5.5%), however, these risky behaviours were not found to be significantly associated with HCV infection. A higher prevalence of HCV infection was also found among inmates with multiple sex partners (5.4%), inmates having sex with non-marital partners (4.7%), inmates with 6 - 10 lifetime sexual partners (9.8%), inmates engaged in homosexuality (4.2%), those involved in transactional sex (4.8%) as well as those with a history of sexually transmitted infections (6.3%); these risky behaviours were also not found to be significantly associated with HCV infection (p > 0.05) as shown in Table 4.
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Table 4. Prevalence of Hepatitis C and behavioural risk factors of inmates.
*Statistical significance p < 0.05.
4. Discussion
The seroprevalence of HBV infection in the current study was 4% among inmates in Port Harcourt. This observation is attributable to risky behaviours practised by the inmates such as sharing sharp objects etc. The seroprevalence from this study was observed to be relatively lower than those reported by similar studies such as the prevalence observed in Kuje prison (13.7%) [9] , 12.2% reported in a national survey among the healthy population in Nigeria [12] , 23% recorded in Nasarawa prison [17] , 11.1% observed in Sokoto prison [18] , 18% in Taraba state [24] as well as the findings in Ghana with a prevalence of 17.4% [25] . Our findings were comparable to those observed in a Pakistani study which yielded a prevalence of 5.9% [26] , as well as the 6% prevalence reported in Ethiopia [27] . On the contrary, the prevalence recorded by this study is higher than a study in Iran which recorded 1.2% [28] .
Age, sex, and other sociodemographic characteristics were not significantly associated with the HBV infection spread. This is consistent with the study carried out in Pakistan [26] , but not in conformity with the study carried out in North East Ethiopia [28] and Iran [29] .
One of the identified risk factors in this study was a history of blood oath (p = 0.0036). An HBV prevalence of 13.8% was observed among inmates with a history of blood oath with an odds ratio of 3.7. Blood oaths are mostly practised by cultists to show camaraderie and a spirit of unity. The blood oath-taking could take place before incarceration or during incarceration in other for them to be protected in the prison yard. During this ritual, if a member has HBV and engages in a blood oath, all other members involved will be infected with the virus. The findings of this study are similar to the study carried out in Kuje Prison where blood oath-taking was observed in inmates with a prevalence of 5.7% [9] .
A history of surgery was also identified as a risk factor for HBV infection (p = 0.0426). An HBV prevalence of 11.1% was observed among inmates with a history of surgery with an odds ratio of 4.2. Negligence from healthcare workers such as improper sterilization of surgical materials and incorrect screening of blood donors for surgical procedures exposes patients to the hepatitis B virus. This significant risk factor was similarly reported by Kazi and colleagues [26] .
Other risk factors such as a history of illicit drug use, alcohol consumption, blood transfusion, having multiple sexual partners, and homosexuality are factors that can contribute to such prevalence although not significantly associated statistically in this study. However, these other risk factors were found to be significant in similar studies carried out in Iran [28] , Nasarawa State Nigeria [17] , and Ethiopia [27] .
The seroprevalence of HCV in the current study was 3.5%. The prevalence of HCV in this study is relatively lower than in the findings from previous studies in Nigeria such as in Nassarawa State prison (12.3%) [17] , 5.6% in Kuje prison [9] and 29.6% observed in Calabar prison [19] . This large variation is probably due to the population size, difference in assay methods, variation in risk factors among inmates as well as variation in risk behaviours among the different prison populations [30] . When paralleled with international studies, the prevalence is higher than studies from India (1.27%) [31] , West Africa (0.5%) [32] , Turkey (0.5%) [33] and Ethiopia (1.2%) [27] . On the contrary, the prevalence study is lower than studies from Ghana (19.2%) [25] , Brazil (13.6%) [34] , Pakistan (15.2%) [26] , Mexico (4.6%) [35] , Cameroun (4.4%) [36] and Spain (22.7%) [37] . The pragmatic differences in this prevalence could be due to the population size tested, the condition of the prison, high-risk behaviours such as injection drug use, homosexuality, and the screening method could also impact the differences [38] [39] .
The seroprevalence of HBV and HCV was reported only in male subjects, though not statistically significant. This conforms to similar research by Okafor et al. (2021) [19] , where the majority of the males were seropositive but was not statistically significant. Conversely, Poulin and colleagues (2007) [40] had higher values for females than males. In this study, the sociodemographic characteristics were not significantly associated with both viral infections. Kassa et al. (2021) [27] reported a similar trend among prisoners in North East Ethiopia.
A major risk factor significantly associated with the distribution of HCV infection was blood oath taking (p = 0.0301). An HCV prevalence of 10.3% was observed among inmates with a history of blood oath with an odds ratio of 4.8. Blood oath is an unhealthy practice performed by lovers or members of a confraternity to prove loyalty. Introducing unscreened blood into the body is a risk that can subject an individual to a variety of infections, particularly blood-borne infections such as HCV infection. The findings from this study were at variance with the study in Calabar [19] and Pakistan [26] .
Sex with non-marital partners was also identified as a risk factor in the spread of HCV infection (p = 0.0457). An HCV prevalence of 5.4% was observed among inmates who had sex with non-marital partners. It is not surprising that sexual intercourse with a non-marital partner is a major risk for the spread of HCV infection. This is because inmates mostly come from marginalized populations such as injecting drug users, high-risk sexual behaviours, sexual workers, paedophiles kidnappers, cultists and the like. This population is notable for unfaithfulness and behaviour such as rape, prostitution, and molestation. This observation however varied from the studies in the Calabar prison [19] and New Bell Prison [36] .
In this study, the data analysed did not identify injection drug use as a risk factor for HCV infection. This practice has been previously reported as a risk factor for HCV infection in earlier studies in prisons in Mexico [35] and Brazil [34] . This is further supported by poor acceptance of this habit since it is not practised openly in the country. Secondly, IDU is not popular when likened to illicit drug use practices observed in Nigerian prisons [17] [19] . As identified by this study, the illicit drug is a major risk factor for the spread of HCV infection (p = 0.0449). An HCV prevalence of 6.2% was observed among inmates with a history of illicit drug use with an odds ratio of 6.7. Smoking of cannabis (hemp and marijuana) and other similar substances, rather than injection are more common substance abuse observed in Nigerian correctional centres.
5. Conclusion
The current study highlights a relatively lower seroprevalence of HBV and HCV among prisoners in Port-Harcourt Maximum Security Custodial Centre in comparison with previous studies in Nigeria. There was no case of HCV-HBV coinfection. The seroprevalence of HBV infection was significantly associated with a history of blood oath and surgery while the seroprevalence of HCV was also significantly associated with a history of blood oath in addition to sex with non-marital partners and illicit drug use. The outcomes of this research call for the enactment of programmed regulation intended for prison facilities like Port Harcourt Maximum Security Custodial Centre. The spread of these viral infections can be further controlled by multifaceted approaches by the prison personnel, administration, and Government. Although the sources of infections are not known with early infection being asymptomatic, the transmission will continue to increase due to poor living conditions and behaviours of the inmates. Therefore, vaccination policies for hepatitis B should be implemented, and access to regular screening and therapy for both HBV and HCV should be available to inmates to decrease the incidence of infection in the prison and the general population upon release of inmates. Inmates should be better enlightened about the use of condoms upon release from prison in addition to mitigating high-risk sexual practices in the prison, personal hygiene supplies, and sterile injection equipment for important medical procedures should be put in place by the management to curb the transmission of Hepatitis B and C.
6. Limitations of the Study
The utilisation of HBsAg and Anti-HCV rapid diagnostic test (RDT) kits (ACON Laboratories) in assaying hepatitis B and C instead of analytical processes based on enzyme-linked immunosorbent assay (ELISA) and polymerase chain reaction (PCR) is a limitation of this study. While HBsAg RDTs are quick, affordable and have very good sensitivity and specificity, they may produce false negatives or false positives, leading to an underestimation or overestimation of the prevalence of hepatitis B virus (HBV) infection in the study population. An HBsAg rapid diagnostic test kit only detects the presence of HBsAg and cannot differentiate between acute and chronic HBV infection or detect other HBV markers such as hepatitis B e antigen (HBeAg) or hepatitis B core antibody (anti-HBc). Anti-HCV RDTs used in this study also have very good sensitivity and specificity in addition to being cost-effective and rapid, the test may also produce false negatives or false positives. Additionally, the test only detects antibodies to HCV and cannot differentiate between acute and chronic HCV infection or detect the presence of HCV RNA. These limitations may affect the accuracy of the prevalence estimates obtained using the test, and a combination of different laboratory tests may be needed for a more accurate diagnosis of HCV infection in prevalence studies like the current study.
Self-reported HBV vaccination status of the inmates was also a limitation of the current study as this approach relies on the accuracy of the participant's memory and may not account for doses that were missed or given incorrectly. Additionally, the timing and completeness of vaccination may vary between individuals and populations, leading to difficulties in making accurate comparisons. Moreover, self-reported vaccination status may not accurately reflect an individual's immune status, as some people may not have developed sufficient immunity despite receiving the recommended vaccine doses. Therefore, relying solely on self-reported vaccination history may lead to an underestimation of the true prevalence of HBV infection and susceptibility in a population.
Acknowledgements
The authors appreciate the participation of the prisoners in this study. We would also want to thank the officials and administrators of the Maximum Security Custodial Centre, Port Harcourt, as well as the Department of Medical Laboratory Science, Rivers State University, Port Harcourt, for their assistance.