Hepatitis B virus and HIV coinfection among adults residing in Cameroon: A systematic review and meta-analysis of prevalence studies

Hepatitis B virus and HIV coinfection among adults residing in Cameroon: A systematic review and meta-analysis of prevalence studies

Infection, Disease & Health (2018) 23, 170e178 Available online at www.sciencedirect.com ScienceDirect journal homepage: http://www.journals.elsevie...

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Infection, Disease & Health (2018) 23, 170e178

Available online at www.sciencedirect.com

ScienceDirect journal homepage: http://www.journals.elsevier.com/infectiondisease-and-health/

Systematic Review

Hepatitis B virus and HIV coinfection among adults residing in Cameroon: A systematic review and meta-analysis of prevalence studies ´ Nkeck c, Anderson Ngouo c, Jean Joel Bigna a,b,*, Jan Rene Ulrich Flore Nyaga c, Jean Jacques Noubiap d a

Department of Epidemiology and Public Health, Centre Pasteur of Cameroon, Yaounde´, Cameroon Faculty of Medicine, University of Paris Sud XI, Le Kremlin-Biceˆtre, France c Department of Internal Medicine, Faculty of Medicine and Biomedical Sciences, University of Yaounde´ I, Yaounde´, Cameroon d Department of Medicine, Groote Schuur Hospital and University of Cape Town, Cape Town, South Africa b

Received 18 December 2017; received in revised form 21 February 2018; accepted 23 February 2018

KEYWORDS HIV; Hepatitis B; Meta-analysis; Systematic review; Cameroon; Africa

Abstract Background: This systematic review and meta-analysis was conducted to determine the prevalence of hepatitis B virus (HBV) and human immunodeficiency virus (HIV) coinfection among adults in Cameroon. Methods: We searched PubMed, EMBASE, Web of Science, Global Index Medicus, and Africa Journal Online with no language restriction to identify articles published from Jan 1996 until Dec 2017. We considered observational studies conducted in apparently healthy populations (pregnant women, blood donors, and general population). We used a random-effects model to pool data. Results: We included 24 studies (23,295 participants) from seven of the ten regions in Cameroon. Four, 20, and no studies had low, moderate, and high risk of bias respectively. The overall HBV-HIV coinfection prevalence was 0.8% (95%CI 0.5e1.0; 11 studies). The overall HBV prevalence in people with HIV was 12.9% (95%CI 9.7e16.5; 20 studies). The HBV prevalence in people with HIV was significantly higher in rural compared to urban. No study reported the prevalence of HIV infection in people with HBV. Conclusions: Although we found a low prevalence of HIV-HBV coinfection in Cameroon, this study presented a high HBV prevalence in people with HIV. Effective strategies to interrupt the transmission of HBV are required, especially among people with HIV infection in rural areas. ª 2018 Australasian College for Infection Prevention and Control. Published by Elsevier B.V. All rights reserved.

* Corresponding author. Department of Epidemiology and Public Health, Centre Pasteur of Cameroon. P.O. Box 1274, Yaounde ´, Cameroon. E-mail addresses: [email protected] (J.J. Bigna), [email protected] (J.R. Nkeck), [email protected] (A. Ngouo), [email protected] (U.F. Nyaga), [email protected] (J.J. Noubiap). https://doi.org/10.1016/j.idh.2018.02.006 2468-0451/ª 2018 Australasian College for Infection Prevention and Control. Published by Elsevier B.V. All rights reserved.

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171

Highlights  This is first review and meta-analysis on hepatitis B virus (HBV) and HIV co-infection in Cameroon.  Not all regions in Cameroon were represented making it difficult to generalize the findings of this review.  All sources of heterogeneity of prevalence estimates were not identified.  This study suggests a high prevalence of HBV infection in people with HIV, especially in rural areas.  Effective strategies to interrupt the transmission of HIV and HBV are required.

Introduction

Setting

Human immunodeficiency virus (HIV) and hepatitis B virus (HBV) infections exact a high burden worldwide. Both viral infections are implicated in the occurrence of chronic diseases, cancer, and death, and none of them can be overthrown with the use of current antiretroviral therapies [1]. On one hand, there were approximately 36.7 million people living with HIV at the end of 2016 with 1.8 million people being newly infected globally. It was reported that in 2016 70% of all HIV infections and two third of new HIV infections occurred in Africa [2]. On the other hand, it is estimated that more than 257 million people are infected with HBV globally with most of them living in low- and middle-income countries like Cameroon [3,4]. About 1 million people die every year of viral hepatitis related complications, mostly including liver cancer and cirrhosis [5,6]. Indeed, 50e80% of primary liver cancers result from infection with HBV [7]. The morbidity and mortality is increased in the case of HIVHBV coinfection compared in a case of HIV or HIB infection alone [1]. To curb the burden of both diseases, the World Health Organization (WHO) launched global programs with the aim to reduce by 90% the number of new cases of hepatitis B, reduce by 65% the number of hepatitis B-related deaths, and treat 80% of eligible people infected with hepatitis B virus by 2030 [8]. In parallel, United Joint Nations Programme on HIV/AIDS (UNAIDS) launched the 95e95e95 targets; the aim is to diagnose 95% of all HIV-positive individuals, provide antiretroviral therapy (ART) for 95% of those diagnosed, and achieve viral suppression for 95% of those treated by 2030 [9]. In order to achieve these goals, policy makers at national level should be informed and have good quality epidemiological data on HBV-HIV coinfection to implement efficient strategies. Therefore, this systematic review and meta-analysis was conducted to determine (1) the prevalence of HIV infection in adults living HBV, (2) the prevalence of HBV infection in adults living with HIV, (3) and the prevalence of HIV/HBV coinfection in apparently healthy adults residing in Cameroon.

Cameroon is a country situated in Central Africa slightly above the equator. It covers a surface area of 475,650 km2 divided into 10 administrative regions: Adamawa, Centre, East, Far-North, Littoral, North, North-West, South, SouthWest, and West. Cameroon counted 23.44 million inhabitants in 2016 [11]. The HBV universal immunisation programme was introduced in Cameroon for children born in 2005 or later and it is free of charge for this population. Beside this programme, the vaccine is not free of charge for the general population and for children born before 2005. The prevalence estimates of HBV infection in Cameroon are 7.1%, 9.8%, and 10.5% in general population, pregnant women, and blood donors respectively [12]. The prevalence of HIV in adults aged 15e49 years was 3.8% in 2016 [13].

Eligibility criteria for considering studies for the review - Type of population: apparently healthy individuals from the general population, pregnant women, or blood donors aged 15 years or more and residing in Cameroon. We excluded studies conducted in Cameroonian populations residing outside Cameroon. - Types of outcomes: prevalence of HIV infection among people living with HBV, prevalence of HBV infection among people living with HIV, and prevalence of HIV and HBV coinfection. HBV infection should have been diagnosed based on the presence of hepatitis B surface antigen. - Types of studies: cross-sectional studies, cross sectional analysis of baseline data of cohort studies, and each group of case-control studies when cross sectional analysis was considered. We excluded case series, reviews, commentaries, and editorials. - Other criteria. We considered studies regardless language of publication and studies conducted after 1996. In case of duplicates, the most comprehensive and upto-date version of the original study was used.

Methods Search strategy to identify relevant studies The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines served as template for reporting this review [10].

We searched PubMed, EMBASE, Web of Science, Africa Journal Online, Global Index Medicus, Health Sciences

172 and Diseases (the biomedical journal of the Faculty of Medicine and Biomedical Sciences, University of Yaounde ´ 1, Cameroon), National Institute of Statistics, Cameroon (http://www.statistics-cameroon.org/), and National AIDS Control Committee, Cameroon (http://www.cnls.cm/) to identify relevant articles published from Jan 1st, 1996 to December 1st, 2017. We focused on the last 20 years to have contemporaneous estimates. Used as medical subheadings terms and text words, the following terms and their variants were included in the search strategy: “HIV”, “AIDS”, “hepatitis B”, “HBV”, and “Cameroon”. The search strategy conducted in PubMed is shown in Additional Table 1. This search strategy was adapted to suit other databases. The last search was conducted on December 1st, 2017. We manually searched the reference list of all relevant articles and reviews to identify additional articles.

Studies selection Two investigators (JJB and JJN) independently screened titles and abstracts of records found for eligibility. These investigators further independently assessed the full text of each study for eligibility, and consensually retained studies to be included. Disagreement was solved by consensus. We used a screening guide to ensure that the selection criteria were reliably applied by all investigators.

Appraisal of the risk of bias Risk of bias of included studies was evaluated using an adapted version of the tool developed by Hoy and colleagues [14]. A score of 1 (yes) or 0 (no) was assigned for each item, and scores summed across items to generate an overall quality score that ranged from 0 to 10. Studies were then classified as having a low (8e10), moderate (5e7), or high (0e4) risk of bias. Two investigators (JRN and AN) independently assessed study methodological quality, with disagreements resolved by consensus or arbitration of a third investigator (UFN).

Data extraction and management Four investigators (JJB, JRN, UFN, and AN) extracted the following data: general information (author, year of publication), study characteristics (study design, setting, area, sampling method, period of participants’ recruitment, timing of data collection, region in Cameroon, representativeness of sample), participants characteristics (inclusion and exclusion criteria, mean or median age, age range, proportions of male participants, and disease specific/ profile specific to the study population), and prevalence data (cases and sample size). We conducted a sensitive analysis considering only at low-risk of infection including general population, blood donors, and pregnant women. In the case where prevalence rates or relevant data for estimating them were not available, we contacted the corresponding author of the study to request the missing information. In the absence of response or no availability of full data, we excluded the corresponding study. Disagreements between investigators were resolved through discussion and by consensus.

J.J. Bigna et al.

Data synthesis and analysis Data were analysed using the ‘meta’ packages of the statistical software R (version 3.3.3, The R Foundation for statistical computing, Vienna, Austria). Unadjusted prevalence was calculated based on the information of crude numerators and denominators provided by individual studies. To keep the effect of studies with extremely small or extremely large prevalence estimates on the overall estimate to a minimum, the variance of the study-specific prevalence was stabilized with the Freeman-Tukey double arc-sine transformation before pooling the data with the random-effects meta-analysis model [15]. Symmetry of funnel plots and Egger test was done to assess the presence of publication and selective reporting bias [16]. A p-value < 0.10 was considered indicative of statistically significant publication bias. Heterogeneity across included studies was assessed using the c2 test for heterogeneity with a 5% level of statistical significance [17], and by using the I2 and H statistics for which a value of 50% for I2 was considered to imply substantial heterogeneity [18]. When substantial heterogeneity was detected (p < 0.05), subgroup analyses to investigate the possible sources of heterogeneity were performed. We considered population (general, blood donors, and pregnant women) and areas (urban, rural) as subgroups. Inter-rater agreements between investigators for study inclusion and methodological quality assessment were assessed using Kappa Cohen’s coefficient [19].

Results Study selection In total, 229 records were identified. After elimination of duplicates, screening titles and abstracts, 183 papers were found irrelevant and excluded. Agreement between investigators on abstract selection was high (k Z 0.89). Full texts of the remaining 46 papers were scrutinized for eligibility, among which 22 were excluded. Agreement between investigators on final inclusion was high (k Z 0.96). Overall, 24 studies were found eligible; hence they were included in the meta-analysis (Fig. 1).

Characteristics of included studies Four (16.3%) studies had low, 20 (83.3%) studies had moderate and no study had high risk of bias. All were crosssectional. Twelve studies were conducted in urban areas only, two in rural areas only, and 10 in both areas. All studies were antenatal care or hospital-based. No study was national representative. Twelve were conducted in the Centre Region, five in the South-West Region, two in the North-West Region, two in the Far North Region, two in the Littoral Region, and one simultaneous in five regions (Centre, East, North-West, and South). No study was conducted in Adamawa, North, and West Regions. Eighteen studies were prospective and six were retrospective. Twenty-one studies used consecutive sampling and three did not describe the sampling method. Thirteen studies were conducted in general population, six in blood donors,

Hepatitis B and HIV coinfection in Cameroon

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229 records identified through database searches 105 duplicates excluded

124 records screened on the basis of title and/or abstract 78 records excluded

46 full-text articles assessed for eligibility

22 full-text articles excluded • No prevalence data, n = 18 • Duplicates, n = 3 • Not eligible HBV diagnostic method, n = 1

24 studies included in qualitative synthesis

24 studies included in quantitative synthesis (meta-analysis) Fig. 1

The review process.

and five in pregnant women. The mean/median age varied from 24.4 to 44.0 years (range: 15e94). The proportion of males varied from 0 to 93.7%. Participants were included between 2000 and 2015. Additional Table 2 presents individual characteristics of each included study.

Table 1

Prevalence of HBV-HIV coinfection Table 1 summarizes meta-analyses of prevalence. In total, 23,295 individuals were included (5862 from general population, 15,150 blood donors, and 2283 pregnant women). The

Summary statistics of the prevalence HBV-HIV coinfection in Cameroon.

HIV-HBV Coinfection By population General Blood donors Pregnant women By area Urban Rural Both HBV in HIV By population General Pregnant women By area Urban Rural Both

N N Prevalence studies participants (95%CI)

I2 (95%CI)

H (95%CI)

11

17,893

0.8 (0.5e1.0)

50.5 (0.6e75.0)

1.4 (1.0e2.0) 0.029

0.151

1 6 4

761 15,150 1982

1.2 (0.5e2.1) 0.6 (0.4e1.0) 0.9 (0.5e1.4)

NA 59.7 (0.9e83.6) 0.0 (0.0e84.2)

NA NA 1.6 (1.0e2.5) 0.030 1.0 (1.0e2.5) 0.407

NA 0.710 0.350

6 0 5 13

14,932 NA 2961 5402

0.6 (0-3-1.0) NA 1.0 (0.6e1.4) 12.1 (8.4e16.5)

63.7 (12.1e85.0) NA 0.0 (0.0e63.3) 95.0 (93.0e96.5)

1.7 (1.1e2.6) 0.017 NA NA 1.0 (1.0e1.7) 0.687 4.5 (3.8e5.3) <0.0001

0.621 NA

12 1

5101 301

12.4 (8.3e17.1) 9.3 (6.3e12.9)

95.4 NA

4.4 (3.7e5.3) <0.0001 NA NA

0.715 NA

6 2 5

1389 1685 2328

9.3 (7.0e12.0) 54.2 (0.0e81.7) 1.5 (1.0e2.3) 0.053 13.6 (12.0e15.4) 5.8 1.0 0.303 15.1 (6.1e27.3) 98.1 (97.0e98.7) 7.2 (5.8e8.9) <0.0001

0.803 NA 0.856

P P Egger P heterogeneity test difference

0.282

0.206

0.674 0.259

0.035

NA: not applicable; CI: confidence interval; HIV: human immunodeficiency virus; HBV: hepatitis B virus.

174

J.J. Bigna et al. Events

Study

Total

Events

95%−CI

Weight

Population = Blood donors Ankouane, 2015

58

9024

0.64

[0.49; 0.83]

21.5%

Eboumbou, 2014

0

477

0.00

[0.00; 0.77]

7.0%

Mbanya, 2003

4

252

1.59

[0.43; 4.01]

4.3%

Mbanya, 2005

2

204

0.98

[0.12; 3.50]

3.6%

Noubiap, 2013

6

543

1.10

[0.41; 2.39]

7.6%

36

4650

0.77

[0.54; 1.07]

19.4%

0.63 [0.35; 0.96]

63.4%

Ymele, 2012

Subgroup Prevalence

15150

Heterogeneity: I 2 = 59.7% [0.9%; 83.6%], τ2 = 0.0002, p = 0.0297

Population = General Shevell, 2015

9

Subgroup Prevalence

761

1.18

[0.54; 2.23]

9.5%

761

1.18 [0.52; 2.09]

9.5%

Heterogeneity: not applicable

Population = Pregnant women Fomulu, 2013

7

959

0.73

[0.29; 1.50]

10.9%

Noubiap, 2015

5

325

1.54

[0.50; 3.55]

5.2%

Sone, 2017

2

298

0.67

[0.08; 2.40]

4.9%

Tanjong, 2016

6

400

1.50

[0.55; 3.24]

6.1%

0.95 [0.55; 1.45]

27.1%

Subgroup Prevalence 2

1982 2

Heterogeneity: I = 0% [ 0%; 84.2%], τ = 0, p = 0.4068

Overall prevalence 2

17893

0.77 [0.53; 1.05] 100.0%

2

Heterogeneity: I = 50.2% [0.6%; 75.0%], τ = 0.0002, p = 0.0285

0

Fig. 2

1

2

3

4

Prevalence of HBV-HIV coinfection in apparently healthy population in Cameroon.

prevalence of HBV-HIV coinfection was 0.8% (95%CI 0.5e1.0; range 0.0e1.6%) with no difference between general population, pregnant women and blood donors (Fig. 2 & Table 1). There was no difference between areas (Additional Fig. 1). The prevalence of HBV infection in people with HIV was 12.1% (95%CI 8.4e16.5; range 9.8e16.0%) with no difference between general population and pregnant women (Fig. 3 & Table 1). The prevalence was higher in studies conducted in both areas (15.1%) followed by rural (13.6%) and then urban areas (9.3%) (Additional Fig. 2). There was substantial heterogeneity for all analyses except for HBV-HIV coinfection prevalence in pregnant women and in both areas; and for the prevalence of HBV infection in people with HIV in rural area. Any funnel plot (Additional Figs. 3 and 4) suggested publication bias confirmed by the Egger test (Table 1).

Discussion Although a low prevalence HIV-HBV coinfection in apparently healthy populations in Cameroon was observed, this

study suggests a high prevalence of HBV infection in adult populations with HIV. No study reported the prevalence of HIV infection in people with HBV. The prevalence of HBV infection in people with HIV in our study (12.9%) is in the range of that reported in other parts of Africa and East-Asia and recently reported by a meta-analysis including eight studies in Cameroon [12]. The prevalence of HBV in people with HIV varies from 4.8% to 16.9% in different parts of Africa continent [20e31]. The prevalence of HBV infection in adults with HIV in our review was higher of that reported in Western Europe and North America [31]. We did not find any study reporting on the HBV-HIV coinfection prevalence in apparently healthy populations nor the prevalence of HIV in people with HBV in Africa to make a comparison with our findings. It is well documented that the natural course of HBV infection can be modified in the presence of HIV as well as the course of HIV infection can be modified in the presence of HBV although data are conflicting in the last case. In fact, it has been shown that compared to HBV-mono-infected, people with acute HBV infection in the presence of HIV had lower rate of spontaneous clearance of HBV, higher levels of HBV

Hepatitis B and HIV coinfection in Cameroon

175

Events Total

Study

Events

95%−CI

Weight

Population = .General Ambassa, 2016

12

75

16.00

[ 8.55; 26.28]

6.5%

Feldt, 2013

33

279

11.83

[ 8.28; 16.21]

7.8%

2

80

2.50

[ 0.30; 8.74]

6.6%

Geretti, 2017

54

552

9.78

[ 7.43; 12.57]

8.1%

143

995

14.37

[12.25; 16.71]

8.2%

51

833

6.12

[ 4.59; 7.97]

8.2%

116

455

25.49

[21.55; 29.76]

8.0%

14

169

8.28

[ 4.60; 13.51]

7.4%

168

531

31.64

[27.70; 35.78]

8.0%

Ottop, 2012

16

230

6.96

[ 4.03; 11.05]

7.7%

Salpini, 2016

25

212

11.79

[ 7.78; 16.91]

7.6%

Zoufaly, 2012

87

690

12.61

[10.22; 15.32]

8.1%

12.39 [ 8.33; 17.10]

92.2%

Kouanfack, 2012 Loriette, 2015 Luma, 2016 Magoro, 2016 Mbougoua, 2010 Noubiap, 2015

Subgroup Prevalence

5101

2

2

Heterogeneity: I = 95.4% [93.4%; 96.7%], τ = 0.0126, p < 0.0001

Population = Pregnant women Kfutwah, 2012

28

Subgroup Prevalence

301

9.30

[ 6.27; 13.16]

7.8%

301

9.30 [ 6.26; 12.86]

7.8%

Heterogeneity: not applicable

Overall prevalence

5402

12.14 [ 8.36; 16.51] 100.0%

Heterogeneity: I 2 = 95.0% [93.0%; 96.5%], τ2 = 0.0119, p < 0.0001

5

Fig. 3

10

15

20

25

30

35

Prevalence of HBV infection in people with HIV in Cameroon.

deoxyribonucleic acid load, and lower rate of the proportion of the presence hepatitis B e antigen [32e36]. HIV also increases the risk for developing cirrhosis and end-stage liver disease in the case of HBV coinfection [37e39]. In contrast, data are conflicting about the role of HBV in the course of HIV infection. Indeed, some studies suggest more AIDS defining illness in people with HBV-HIV coinfection [40] while others do not suggest any change in the HIV disease survival and progression [41,42]. Cameroon counts about 14,000,000 of adult inhabitants [13]. With an estimated adult population of 14,000,000 and a prevalence of HBV-HIV of 0.8%, Cameroon has about 100,000 adults co-infected with HIV and HBV. The cost for treatment for HBV infection varies from 11 to 456 USD per month (depending on the presence of the hepatitis B delta virus). The guaranteed minimum wage in Cameroon is 72.5 USD. This suggests that many people in Cameroon cannot afford treatment against HBV. Hence, primary prevention through vaccination appears to be an efficient strategy to interrupt transmission of HBV in people with HIV. Such measures should be accompanied by widespread education campaigns regarding the transmission and infection

dynamics of these viruses. Indeed, studies in Cameroon reported that less than 30% of the general population knew the route of transmission of HBV [43]. In addition, 47e83.2% of healthcare workers have been reported to have a good level of knowledge on HBV infection [44e46]. In Cameroon in 2016, there were 560,000 (90% of them aged more than 15 years) people living with HIV and 32,000 new HIV infections [47]. Only 58% of people living with HIV were aware of their status. Among people knowing their status, only 37% were on antiretroviral treatment. Of those on antiretroviral treatment, only 52% achieved HIV viral suppression [47]. These parameters are far from the 90-9090 objectives [9]. Strategies to interrupt the transmission of HIV and HBV include significant financial resource allocation and logistical support of the health system, communitybased integrated prevention campaign, national homebased, mobile, or self-voluntary HIV and HBV counselling and testing, mobile HIV and HBV antiretroviral treatment distribution [48]. Although it is difficult to implement all these strategies in a weak health system of a developing country [49], however these activities can be integrated into community-based and ongoing mobile activities as a

176 package. For example, mobile ART distribution could be combined with mobile vaccination and antenatal care activities in certain health areas of the country. Context specific strategies to increase linkage to care and adherence to antiretroviral treatment are also needed. These strategies can include using text messages and phone calls for linkage to care [50] and adherence to antiretroviral treatment [51] as demonstrated in randomized controlled trials conducted in the country. Peer supporters, alarms, counselling, and enhanced standard of care can also be considered for adherence to antiretroviral treatment [52]. Rural areas should be prioritized. Strengths of this study include the use a comprehensive search strategy and involvement of two independent investigators in all stages of the review process. In most of analyses, the results of tests for publication bias provided evidence that we were unlikely to have missed studies that could have altered the meta-analysis results. Strong and robust statistical methods were used. Nevertheless, the findings of this review should be interpreted in the light of its limitations. Firstly, there was no national representative study included in this review and data used for this study did not include all regions of the country. We did not find any study conducted in the Adamawa, North, and West Regions of the country. Thus, our data might difficult to generalize at the country-level. Secondly, there were not enough studies for some subgroup comparisons. Therefore, the findings in subgroup analyses should be interpreted with caution. Thirdly, the real prevalence may be lower since data were from studies conducted in healthcare settings. In addition, across studies, screening tools and their diagnostic features are different; this may impact estimates and may be at origin of source of unexplained heterogeneity when pooling data. We were unable to measure the impact of this because information on sensitivity and specificity of diagnostic tools used were not reported in included studies. Nonetheless, to the best of our knowledge, this is the first comprehensive review on the prevalence of HBV-HIV coinfection in Cameroon. It gives a clear overview of the burden of this coinfection in the country, the need for efficient public health interventions to curb the burden of these diseases in the country, and crucial gaps to fill in future research. In the absence of data from a national representative study that requires more logistics and higher cost, having a metaanalysis of several studies in this field provides insights into the epidemiology of HIV and HBV coinfection with little expenditure, although the interpretation should take into account the heterogeneity of the diagnostic tools and populations included in different studies. This can be done in other African countries as has already been done for Ghana [20]. Although we found a low prevalence of the presence of both HIV and HBV in apparently healthy adult populations in Cameroon, this study suggests a high prevalence of HBV in people with HIV. As such, both diseases should be prioritized by policy makers and stakeholders from the health sector. Effective strategies to interrupt the transmission of HIV and HBV are required for the entire population and people living with HIV and/or HBV, especially in rural areas. Studies are needed to determine the prevalence of HIV infection in people living with HBV.

J.J. Bigna et al.

Ethical considerations Not applicable, systematic review.

Authorship statement Conception and design: JJB and JJN. Search strategy: JJB. Study selection: JJB and JJN. Data extraction: JJB, JRN, UFN, and AN. Data synthesis and analysis: JJB. Data interpretation: JJB and JJN. Manuscript drafting: JJB. Manuscript revision: JJN, JRN, UFN, and AN. All authors read and approved the final manuscript.

Conflicts of interest The authors declare that they have no competing interests.

Funding This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Provenance and peer review Not commissioned; externally peer reviewed.

Acknowledgements None.

Appendix A. Supplementary data Supplementary data related to this article can be found at https://doi.org/10.1016/j.idh.2018.02.006.

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