HIV-hepatitis co-infection in a rural community in Northern Nigeria
Oluwaseyitan Andrew Adesegun1,2,&, Olabiyi Hezekiah Olaniran3, Emmanuel Bamidele4, Joseph Nicholas Inyang1, Michael Adegbe1, Tolulope Oyinloluwa Binuyo5, Osaze Ehioghae2, Oluwafunmilola Adeyemi6, Oyekunle Oyebisi7, Akolade Olukorede Idowu2,8, Oluwafemi Ajose9
1General Hospital, Garaku, Nasarawa State, Nigeria, 2Benjamin Carson (Snr.) School of Medicine, Babcock University, Ilishan-Remo, Ogun State, Nigeria, 3Federal Medical Centre, Keffi, Nasarawa State, Nigeria, 4Department of Community Medicine, Babcock University Teaching Hospital, Ilishan-Remo, Ogun State, Nigeria, 5Oyo State Ministry of Health, Ibadan, Oyo State, Nigeria, 6College of Medicine, University of Ibadan, Ibadan, Oyo State, Nigeria, 7Department of Internal Medicine, Olabisi Onabanjo University Teaching Hospital, Sagamu, Ogun State, Nigeria, 8Department of Internal Medicine, Babcock University Teaching Hopital, Ilishan-Remo, Ogun State, Nigeria, 9School of Public Health, University of South Wales, Wales, United Kingdom
Oluwaseyitan Andrew Adesegun, General Hospital, Garaku, Nasarawa State, Nigeria
HIV, hepatitis B and hepatitis C pose a public health challenge in sub-Saharan
Africa and there are only few studies on co-infection of these viruses
done in rural areas in Northern Nigeria. This study provides a rural
perspective on HIV-hepatitis co-infection in a Northern Nigerian community.
this cross-sectional study was carried out amongst
people living with HIV/AIDS (PLWHA) in a rural community hospital over a three-month period. Socio-demographic data and other relevant information were obtained from the participants and case notes using an interviewer-administered questionnaire. Hepatitis B surface antigen and antibody to Hepatitis C virus were assayed from serum using enzyme-linked immunosorbent assay (ELISA) kits developed by LabACON®. Chi-square test was used to compare categorical variables and logistic regression modelling was used to determine correlates of co-infection in the population.
a total of 281 individuals participated in the study. The prevalence of Hepatitis B co-infection, Hepatitis C co-infection and triple infection was 6.0%, 14.6% and 1.1% respectively. Using Chi-square test, none of the socio-demographic characteristics, WHO Clinical Stage, viral suppression had significant association with Hepatitis B co-infection, however marital status was significantly associated with Hepatitis C co-infection and level of education was significantly associated with triple infection (p < 0.05). Logistic regression modelling generated no significant results.
co-infection of viral hepatitis (particularly Hepatitis C) in PLWHA is common in rural Northern Nigeria, and significant correlates include lack of formal education and being married. There is need for provider-initiated routine counselling and screening of PLWHA for viral hepatitis, with adequate follow-up and treatment of co-infected individuals and Hepatitis B vaccination for those without co-infection.
Human Immunodeficiency Virus (HIV) infection and chronic viral hepatitis
(Hepatitis B and C virus infection) are global health problems that
are of concern particularly to the African people, as the prevalence
chronic illnesses remain high in the continent, particularly the sub-Saharan
region [1-3]. About 37 million individuals are infected
with HIV globally, out of which 5-20% are also co-infected with Hepatitis
B virus (HBV) . Chronic viral hepatitis affects about
70 million people in Africa (60 million with Hepatitis B and 10 million
with Hepatitis C) . Co-infection of any of these
hepatotropic viruses with HIV hastens the progression of liver disease
in these patients [6,7].
Nigeria, a country with a population of about 200 million people
is known to have the second highest prevalence of HIV/AIDS in the
world, recently pegged at 1.4% in 2019, an improvement from previous
The prevalence of HBV infection in Nigeria is between 12.2-14%,
while the prevalence of Hepatitis C virus (HCV) infection ranges
from 2.8 to 24.2%
amongst adults from different sub-regions of the country [9-12].
Nasarawa State, a State in the north-central part of the country
is home to many viruses, as high prevalence rates of HIV, Hepatitis
B and Hepatitis
C have been documented in the State. A recent update by the National
Agency for the Control of AIDS (NACA) placed the State in the top
ten list of States
with the highest prevalence of HIV in Nigeria, with prevalence
rate of 1.9%. Prevalence of Hepatitis B in Nasarawa State ranges
between 7.1% and 13.3%
[13-15], while the prevalence of Hepatitis C has been
quoted at around 13.2% to 24.2% [9,15].
Co-infection of one or more of the Hepatitis viruses with HIV is
not uncommon, as these viruses all share similar routes of transmission
sexual practices, mother-to-child transmission, unsafe blood transfusion,
injection with contaminated sharps in the healthcare setting, traditional
tattooing and scarification to mention a few. Recent studies in
the State have shown HIV-HBV co-infection rates to be about 11%,
while HIV-HCV co-infection
rates were about 13.5% and 5% of the HIV positive individuals had
both HBV and HCV in a particular study . This implies
a higher risk of progression of liver disease to liver cirrhosis
and hepatocellular carcinoma amongst co-infected individuals [16,17].
Studies providing information on the state of HIV-hepatitis co-infection in rural
Nigeria, including the current screening practices for these viruses are lacking.
This study will fill a gap in knowledge on this subject, providing information
relevant for a region with high prevalence rates of HIV, Hepatitis B and Hepatitis
C. This study will also inform hospital practices and policies as regards serological
screening practices in HIV positive individuals who present to the hospital
for medical care. The objectives of this study were to determine the prevalence
of Hepatitis-Hepatitis co-infection (HIV-hepatitis B co-infection, Hepatitis
C co-infection and HIV-Hepatitis B-Hepatitis C co-infection / Triple infection),
and ascertain factors associated with HIV-hepatitis co-infection, as well as
correlates of HIV-hepatitis co-infection among people living with HIV/AIDS
(PLWHA) in a Northern Nigerian community.
the study was carried out in a secondary healthcare centre located in Garaku (General Hospital, Garaku), the local government headquarters of Kokona Local Government Area in Nasarawa State. This hospital, which is the only secondary healthcare facility serving the area, provides healthcare to indigenes of the town, as well as other smaller villages in the local government. The hospital provides care to PLWHA in collaboration with the Institute of Human Virology Nigeria (IHVN), Garaku, by running an anti-retroviral therapy (ART) clinic, providing HIV Voluntary Counselling and Testing (VCT), Provider-initiated testing, treatment and follow-up, and management of complications.
the target population for this study was all HIV positive individuals who presented to the ART clinic during the study period, who were not known to have Hepatitis B or Hepatitis C, and had not been screened for Hepatitis B and Hepatitis C in the last 6 months. All those who had been previously diagnosed with Hepatitis B or Hepatitis C, or who had been screened for any of two viruses within the last 6 months were excluded.
the study was a descriptive cross-sectional study, carried out over a three-month
period, from December 2019 to February 2020. Data was obtained from
the participants and from their case notes using an interviewer-administered
which was applied by trained research assistants. The age, gender,
occupation (grouped according to the International Standard Classification
, level of education, marital status, viral suppression
(HIV RNA <1000 copies per millilitre)  and current
WHO clinical stage were obtained and documented. Blood samples (5
millilitres) were obtained by venepuncture from the antecubital fossa and
separate serum from packed cells. Hepatitis B surface antigen (HBSAg)
and antibody to Hepatitis C virus (anti-HCV) were assayed using enzyme-linked
immunosorbent assay (ELISA) kits developed by LabACON® (Hangzhou Biotest Biotech
Co., Ltd, China). The manufacturer´s instructions on the use of the
kits were strictly adhered to.
Sample size determination:
the minimum sample size was determined using the Kish formula (n = Z2pq/d2, where n = sample size, p = prevalence, q = 1-p, d = absolute precision)  to be approximately 260, after finite population correction, assuming a confidence level of 95% and 5% absolute precision, with a prevalence of 28.4% from a previous study .
a multistage sampling technique was employed. The sample size (260) was divided
into three strata, based on the month of th ART clinic appointments for
the clients (December, January, February), with at least 87 participants
allotted to each stratum.
Since each month (stratum) had 8 clinic days on average, at least 11
participants were randomly selected on each clinic day throughout the
study period, until
the minimum sample size was reached.
Data collection and analysis:
data was entered into the IBM Statistical Package for Social Sciences (SPSS) Version 22 (Chicago, IL, USA) and summary statistics were generated. Chi-square test was used to compare categorical variables, while univariate/multivariate logistic regression was used to model the relationship between socio-demographic variables and HIV-Hepatitis co-infection in the population. Unadjusted odds ratio (OR) and adjusted odds ratio (aOR) were generated for the univariate and multivariate logistic regression models respectively, and their associated 95% confidence intervals computed. Age, gender, level of education, occupation, marital status, WHO clinical stage and viral suppression were used as socio-demographic (independent) variables, while HIV-Hepatitis B co-infection, HIV-Hepatitis C co-infection and HIV-Hepatitis B-Hepatitis C co-infection (triple infection) each served as the dependent variables. Level of significance was set at p < 0.05.
ethical approval was obtained from the ethics review committee of the Federal Medical Centre, Keffi, Nasarawa State, Nigeria, with registration number NHREC/21/12/2012. Written informed consent was obtained from study participants.
Socio-demographic characteristics of respondents:
a total of 281 respondents were sampled, 79.7% of whom were female while 20.3% were male. The mean age of respondents was 37.1±9.5, with the age of respondents ranging between 7 and 68 years. Most respondents (43.8%) were however within the 31-40 age group (Table 1, Table 1 (suite)). Majority of the participants (43.4%) had no prior formal education, whereas 23.5% had primary, 25.3% had secondary and 7.8% had tertiary education. Two hundred and forty four (86.8%) of the respondents were married, while 24 (8.5%) and 13 (4.6%) respondents were single and divorced/separated respectively. The occupations of the respondents are classified in line with the International Standard Classification of Occupations (Table 1, Table 1 (suite)).
HIV status and co-infection with viral hepatitis:
all of the respondents had been previously diagnosed with HIV and commenced on
Highly Active Anti-Retroviral Therapy (HAART). Two hundred and seventy five (97.9%)
of the study participants were in WHO clinical stage 1, while 5 (1.8%) were in
stage 2 and 1 (0.4%) in stage 3. Two hundred and fifty participants (89%) had
achieved HIV viral suppression (defined as viral load <1000 copies per ml) ,
while 11% had not achieved HIV viral suppression, as documented in their case
notes. However, only 224 (80.4%) of the respondents had their most recent viral
load tests done within the last 12 months; 54 (19.2%) had their viral load checked
within the last 24 months while 1 participant´s result was from the last
36 months. Seventeen participants (6.0%) had Hepatitis B co-infection, while
41 participants (14.6%) had Hepatitis C co-infection. Three individuals (1.1%)
had dual co-infection with Hepatitis B and Hepatitis C (triple infection). Our
study also showed that majority of those who had Hepatitis B co-infection, Hepatitis
C co-infection and triple infection were between 31 and 40 years of age, female,
skilled agricultural workers, though the occupation of those with triple infection
was evenly distributed between civil servants, professionals and the unemployed
(Table 2, Table 2 (suite), Table 2 (suite 1)).
While most of the respondents who had Hepatitis B and C co-infection were uneducated,
two-third of those with triple infection had tertiary education. Furthermore,
majority of the respondents with Hepatitis B co-infection, Hepatitis C co-infection
and triple infection were married, in WHO clinical stage 1 and had achieved HIV
viral suppression (Table 2, Table 2 (suite), Table 2 (suite 1)).
There was no statistically significant association between the socio-demographic
characteristics, WHO Clinical Stage, HIV viral suppression and Hepatitis
B co-infection using Chi-square test (p > 0.05) (Table 2, Table 2 (suite), Table 2 (suite 1)). However, marital status was significantly associated with Hepatitis
C co-infection (p < 0.05), as 97.6% of those who had Hepatitis C co-infection
were married (Table 2, Table 2 (suite), Table 2 (suite 1)). Other socio-demographic characteristics, along with WHO clinical
stage and HIV viral suppression had no association with Hepatitis C co-infection
(p > 0.05) (Table 2, Table 2 (suite), Table 2 (suite 1)). Only level of education had a significant association with HIV-Hepatitis
B-Hepatitis C (triple) infection (p < 0.05), amongst all the variables tested
(Table 2, Table 2 (suite), Table 2 (suite 1)) with two-third (66.7%) of those that had triple infection having
tertiary education (Table 2, Table 2 (suite), Table 2 (suite 1)).
Results of logistic regression analyses for the HIV-Hepatitis B co-infection
model, after systematic removal of variables with extremely high or low odds
ratio (unadjusted and adjusted odds ratios) indicated that the generated models
were no different from null models, suggesting that none of the independent
variables were sufficiently correlated with HIV-Hepatitis B co-infection.
A similar finding was obtained when HIV-Hepatitis C and Triple infection were
set as the dependent variable.
The goal of the study was to establish the prevalence and factors
associated with Hepatitis co-infection in a rural population of PLWHA in
Nigeria. It was found that most of the study participants were aged 31-40
years. This finding is in agreement with recent national statistics that
indicate that the burden of HIV infection in Nigeria is highest in individuals
aged 15- 49 years (about 75% of all PLWHA) . More
women (randomly selected) were found to have participated in this study,
which may suggest that more women attended the ART clinic during the study
period. This is generally in keeping with national statistics that reports
over half of PLWHA in Nigeria to be females, in both rural and urban areas
[22-24]. A study conducted in Keffi, a town not far
from the study location also yielded similar male-female distribution, while
another report from a study conducted six years prior, in the same hospital,
confirmed the pattern [14,25].
On another note, this finding may also suggest a higher clinic attendance
and health-seeking behaviour in women, though this was not an objective
of the study and hence was not properly assessed. The above referenced report
by the National Agency for the Control of AIDS (NACA) also shows that females
with HIV had a higher incidence of sexually transmitted infections, a report
which is in tandem with our findings, which showed that females had a proportionately
higher prevalence of Hepatitis B co-infection, Hepatitis C co-infection
and HIV-Hepatitis B-Hepatitis C triple infection [22,24].
Our study shows that more women had Hepatitis B, Hepatitis C and both co-existing
with HIV, which is similar to previous studies conducted in the same region
of Northern Nigeria[14,25]. However,
studies in South-east and Southwest Nigeria found males to be more likely to
have co-infection with the Hepatitis viruses [26,27]. Our
report also shows that the burden of HIV-Hepatitis co-infection is higher in
middle aged individuals than in any other age bracket, especially in those
aged 31-40 years, similar to what was found six years prior in the same study
population . The prevalence of Hepatitis B co-infection,
Hepatitis C co-infection and triple infection was 6%, 14.6% and 1.1% respectively.
This prevalence rate for Hepatitis B co-infection is much less than the 13%
reported in the same community (Garaku) years ago, and the other higher rates
reported in the State, as well as the national average [13-15, 25].
The story is however different for Hepatitis C co-infection rates which are
notably higher than Hepatitis B co-infection both in our study and the above
mentioned Keffi study . Varying co-infection rates
have also been reported in different parts of the country, from 1.9% in Ekiti
and 3% in Ibadan, to 23.5% in Abeokuta [27-29]. Prevalence
of viral hepatitis is generally noted to be comparatively higher in Northern
Nigeria than the Sothern parts of the country . Education
and occupation could be likely drivers of this problem, as most of our respondents
who had co-infection (particularly Hepatitis B and Hepatitis C) were uneducated
agricultural workers, though most of those who had triple infection had tertiary
education. This finding of education affecting co-infection
in general is not alarming, as the study was carried out in a rural community
where lack of formal education is commonplace. It is possible that a lack of
formal education could preclude some individuals from utilizing their clinic
visits to the utmost, by obtaining all needed information from the healthcare
givers. It is also possible for a lack of formal education to favour poor health-seeking
behaviours. This hence suggests the need for healthcare workers, particularly
those caring for PLWHA in rural settings to give voluntary counselling and
screening for Hepatitis B and Hepatitis C to PLWHA.
Worthy of note is the fact that a large majority of our respondents with co-infection
were married. This suggests the perpetuation of co-infection within married
couples, and possible transmission to their offspring, more so in a culture
that permits polygamy. This assumption is however subject to confounding by
other variables such as the presence or absence of extramarital sexual relations,
one partner being a chronic carrier prior to marriage and other known risk
factors for HIV, Hepatitis B and Hepatitis C infection. This finding however
raises questions on why there are more married PLWHA who are co-infected.
Interestingly, most of our respondents were in WHO clinical stage 1 and had achieved
viral suppression (< 1000 RNA copies/ml), an acceptable cut-off in the developing
world. This was a noteworthy observation, and is indicative of efforts of the
caregivers in encouraging drug compliance, as well as the patients´ willingness
to adhere to the anti-retroviral medications. It is however not yet common
practice for healthcare providers to request routine viral hepatitis screening
for PLWHA in Nigeria. A similar study in Jos however found that most of their
respondents who had Hepatitis B co-infection and triple infection had higher
HIV RNA loads and had more severe immunosuppression prior to the initiation
of HAART .
Some of the limitations of this study include the fact that we did not evaluate
the presence of risk factors (modes of transmission) for hepatitis B and Hepatitis
C, though this may have aided in the establishment of some associations. We
were also unable to run other viral markers such as Hepatitis B core antigen,
which would have provided further details on the serostatus of the participants,
as it relates to chronic carriage and infectivity. This was due to the limited
resources available for the study.
This study found a higher Hepatitis C co-infection rate relative to Hepatitis B co-infection rate, and a low rate of triple infection. Lack of formal education, as well as being married were significant correlates of triple infection and HIV-Hepatitis C co-infection respectively, from this study. The authors recommend that healthcare providers for PLWHA be aware of the risk of their patients contracting Hepatitis B and Hepatitis C, particularly those living in the Northern part of Nigeria where there is a high prevalence of HIV, Hepatitis B and Hepatitis C, and hence provide annual or biannual routine voluntary counselling and screening for them, to possibly correspond with the routine viral load checks.
What is known about this topic
- It is known that HIV, Hepatitis B and Hepatitis C are prevalent in sub-Saharan Africa, more so in Nigeria, and co-infection of these viruses in an individual is inevitable.
What this study adds
- This study gives a snapshot of the situation in a rural community in Northern Nigeria, where the prevalence of HIV, Hepatitis B and Hepatitis C are known to be high;
- It gives the prevalence rates of co-infection for an entire local government and also identifies significant correlates of Hepatitis B and Hepatitis C co-infection amongst PLWHA in a rural community which include lack of formal education and marital status (being married).
The authors declare no competing interests.
Oluwaseyitan Andrew Adesegun was the principal investigator, involved in the conceptualization, design, implementation of the research protocol and drafting of the manuscript. Olabiyi Hezekiah Olaniran and Emmanuel Bamidele were involved in the design of the study as well as drafting and critical review of the manuscript. Joseph Nicholas Inyang and Michael Adegbe were involved in the implementation of the research protocol as well as review of the manuscript. Tolulope Oyinloluwa Binuyo, Osaze Ehioghae, Oluwafunmilola Adeyemi, Oyekunle Oyebisi, Akolade Olukorede Idowu and Oluwafemi Ajose were instrumental in the critical review of the manuscript, and provided editorial oversight to the project.
All authors read and approved the final version of the manuscript.
The researchers would like to acknowledge the leadership and staff of the Institute of Human Virology Nigeria (IHVN) of General Hospital, Garaku, Nasarawa State, particularly Mrs. Esther Turaki, Mr. Barnabas Michael Yikon, Mr. Francis Alli and Ms. Blessing Haruna for the full show of support as well as technical assistance in actualizing the project. The researchers also acknowledge the hospital administration of General Hospital, Garaku, Nasarawa State, as well as the leadership and staff of the medical laboratory of the hospital for assisting with the sample collection and assays.
1: socio-demographic characteristics of study participants
Table 1 (suite): socio-demographic characteristics of
Table 2: association between socio-demographics and co-infection
Table 2 (suite): association between socio-demographics and co-infection
Table 2 (suite 1): association between socio-demographics and co-infection
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