HIV and hepatitis B virus co-infection in Mozambique: Policy review and health professionals’ knowledge and practices

Vanda dos Muchangos; Lucia Chambal; Charlotta Nilsson; Esperança Sevene

doi:10.1371/journal.pone.0301305

Abstract

Background

Human Immunodeficiency Virus (HIV) and Hepatitis B Virus (HBV) co-infection is a public health problem affecting 2.7 million worldwide. In Mozambique, the prevalence of this co-infection is 9.1%, calling for specific policies on prevention, diagnosis and adequate management in health facilities caring for HIV patients. This study aimed to review the existing policies and to assess the knowledge and practices of health professionals about HIV/HBV co-infection.

Methods

A document and literature review to describe the existing policies and guidelines on HIV/HBV co-infection in Mozambique was performed. Key informants were contacted to clarify or add information. Health Professionals who care for HIV-positive patients in four health centers in Maputo City, the capital of Mozambique, responded to a questionnaire on knowledge and practices about this co-infection. Qualitative analysis was done to identify main themes using content analysis. Descriptive statistics of socio-demographic, knowledge and practice variables was presented using the SPSS Program version 20 and bivariate analysis was applied to describe the association between variables.

Results

Twenty-one policy documents were found, and five key informants were interviewed. Fifty-two participants answered the questionnaire. Only one policy document explicitly referred to HIV/HBV co-infection treatment. Most Health Professionals (96%) were aware of HIV/HBV co-infection. Although the only existing policy is on the treatment, few (33%) referenced antiretroviral formulations containing Tenofovir and Lamivudine. Only 29% of Health Professionals reported screening HIV patients for HBV and 21% practiced HIV/HBV co-infection counselling. No statistically significant differences were found when relating the socio-demographic variables with knowledge and practices.

Conclusion

Policy documents relating to prevention, diagnosis and clinical management of HIV/HBV co-infection were rare or absent. Health Professionals had little knowledge about HIV/HBV co-infection. Defining adequate policies and training of Health Professionals may help increase awareness, increase counselling of patients for disease prevention, diagnosis and proper management of HIV/HBV co-infected patients.

Citation: dos Muchangos V, Chambal L, Nilsson C, Sevene E (2024) HIV and hepatitis B virus co-infection in Mozambique: Policy review and health professionals’ knowledge and practices. PLoS ONE 19(8): e0301305. https://doi.org/10.1371/journal.pone.0301305

Editor: Isabelle Chemin, Centre de Recherche en Cancerologie de Lyon, FRANCE

Received: March 14, 2024; Accepted: August 2, 2024; Published: August 20, 2024

Copyright: © 2024 dos Muchangos et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: This work was funded by a grant from the Swedish International Development Cooperation Agency, Sida to the Eduardo Mondlane University for a research-training program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

According to UNAIDS (2023), around 39 million people globally were living with human immunodeficiency virus (HIV) in 2022 of which 37.5 million were adults and 1.5 million children. Fifty-three % of all people living with HIV (PLWH) were women and girls [1, 2]. Eastern and southern Africa remains the region most heavily affected by HIV, with 20.6 million PLWH—54% of all PLWH [3]. In Mozambique, the HIV prevalence is 13.2% [4].

With the introduction of specific policies, including policies for access to care and antiretroviral treatment, the average life expectancy of PLWH has been increasing. With increasing longevity, there is an increase in morbidity and mortality associated with other pathologies in patients with HIV, including hepatitis B virus infection (HBV) [5, 6]. In 2019, 296 million people were living with chronic hepatitis B worldwide [7], with a higher prevalence of chronic HBV infection and higher rates of HBV-associated hepatocellular carcinoma (HCC) in sub-Saharan Africa [8, 9]. Studies have shown a HBV infection prevalence in Mozambique at 10.6% [10, 11] and 12.2% [11]. HBV can lead to chronic infection with progression to liver cirrhosis, HCC, liver failure, and death, and the patients with chronic infection become carriers and transmitters of HBV infection [12].

HBV and HIV share the same transmission routes, which include (a) exposure of mucous membranes or non-intact skin to contaminated blood and body fluids (saliva, semen, vaginal fluids), (b) contact with exudates from lesions and contaminated surfaces, (c) interpersonal contact through sharing contaminated objects (needles, syringes, toothbrushes, razors), and (d) mother-to-child transmission. HBV represents a growing cause of mortality and morbidity in HIV co-infected patients, including patients on ART [13, 14].

HIV infection negatively affects the natural course of HBV-induced hepatitis [15]. Co-infected patients are less likely to resolve the acute HBV infection spontaneously, have a higher risk of progression to liver complications with fibrosis [16] and tend to develop cirrhosis and HCC in less time compared to HBV mono-infected patients [17]. Other consequences of HIV/HBV co-infection include reduced response to treatment, cross-drug resistance to HIV and HBV, and increased risk of drug hepatotoxicity [18, 19].

According to the 2021 WHO Global progress report on HIV, viral hepatitis and sexually transmitted infections, in 2015 2.7 million people were co-infected with HIV and hepatitis B virus, and of these, 1.9 million (69% of all cases) lived in sub-Saharan African countries [7, 20]. The prevalence of HIV/HBV co-infection in Mozambique in 2015 was 9.1% [21]. A study of HCC patients at Maputo Central Hospital showed a prevalence of HBV and HIV of 56.1% and 18.6%, respectively [22], highlighting the importance of integrating HBV testing in providing care and attention to HIV-positive patients. This approach would benefit from the infrastructure of HIV care, and it would improve co-infected patients’ health conditions and treatment and reduce morbidity and mortality resulting from co-infection [21].

WHO recommends HBsAg testing to all groups considered at high risk for HBV, including HIV-positive patients, relatives and sexual contacts of patients with HBV, men who have sex with men, sex workers, and prisoners. This recommendation is critical to ensure that non-immune risk groups are vaccinated. It also recommends that HBsAg-positive individuals be referred to evaluate other markers of hepatitis B and staging liver disease for adequate care. The WHO also recommends that if treatment is needed as per HIV or HBV parameters, the ART regimen should contain at least two drugs active against HIV and HBV. The ART regimen would preferably include Tenofovir (TDF) and Emtricitabine (FTC) or Lamivudine (3TC) [23].

To implement the WHO recommendations, Health Professionals (HP) must be guided by clear policies or guidelines [22, 24, 25], have adequate training and have knowledge about the management of this co-infection to adjust their practices. Lack of knowledge about HBV and inappropriate practices were described in low- and middle-income countries [26, 27] and high-income countries [28]. In Mozambique, there is little information on policies for prevention and management of co-infected patients. This study aimed to review the existing policies and to assess the knowledge and practices of health professionals about HIV/HBV co-infection.

Materials and methods

Study design and settings

The study took place from January to May 2019 using mixed methods with qualitative and quantitative approaches. First, a document and literature review to describe the existing policies and guidelines on HIV/HBV co-infection was performed. Second, key informants were in-depth interviewed to complement, clarify or add information. After the policy review, a cross-sectional study was carried out. HPs who care for HIV-positive patients in four health centers (HC) in Maputo City, the capital of Mozambique, responded to a semi-structured questionnaire on knowledge and practices about HIV and HBV co-infection.

The municipality of Maputo is the largest city in Mozambique and the country’s administrative, political, economic and cultural capital, with a population of 1 101 170 according to the National population Census of 2017 [29]. It is divided into seven Municipal Districts: Ka’Mpfumo, Nlhamankulu, Ka’Maxakeni, Ka’Mubukwana, Ka’Mavhota, Ka’Tembe and Ka’Nyaka, where the health centers are located. The most populous district is Ka’Mavhota, with just over a quarter of the city’s total population, followed by the Nlhamankulu district, with just under a quarter. The prevalence of HIV in Maputo City is 16% [4]. Maputo City has 31 HCs that serve PLWH distributed over the city’s seven districts. Five HCs were selected based on the number of HIV patients on antiretroviral treatment. The Mavalane HC is located in Ka’Mavhota district, Alto-Maé HC in Ka’Mpfumo, Polana Caniço and 1° de Maio HCs in Ka’Maxakeni. In these HCs, the services for PLWH are organized into adult outpatient clinics, maternal and child health clinics that include care for pregnant women and HIV-positive children, and counselling services for HIV testing and treatment.

In 2001, Mozambique approved the Norms of Organization of the National Health Service for the care and treatment of people living with HIV/AIDS, the guiding principles for the treatment of patients with HIV/AIDS infection, and the respective Technical Guides for the prevention and treatment of HIV infection. The National Program for the Control of HIV/AIDS is the entity of the National Health System (SNS) responsible for managing HIV-related health services.

Study population and tools

The key informants were heads of relevant programs and institutions involved in the health policy development process in the country, the National Blood Service, Blood Bank, National Directorate of Pharmacy, National Program for the Control of STIs-HIV/AIDS and Hepatitis, and the Immunization Program. For the interview, a script with systematized questions was used to identify documents that refer to policies and regulations regarding the prevention, diagnosis and treatment of HBV-infection in HIV-positive patients. The script contained a section with identification and socio-demographic data, questions regarding the type of policy document, the year of publication, key information regarding prevention, diagnosis and treatment, issuing authority and the document’s source (S1 File).

The HPs were medical doctors (general practitioners), medical technicians (general medicine technicians), nurses (with medium and higher training in nursing) and counselors (with basic training in counselling for testing and treatment of HIV patients and HIV testing) in service for more than six months in HIV-positive patient care. They worked in outpatient clinics for chronic illness, maternal and child health care, prenatal consultation, counselling and testing. They were selected because were involved in the WHO cascade to cure viral hepatitis B and C framework used in this study. Care is given in three levels: first, the counsellors provide counselling for HIV prevention, testing, treatment and adherence; second, the nurses carry out testing for diagnosis, counselling and follow-up of the patient’s treatment; third, the medical technicians and medical doctors make the diagnosis, prescribe the medicines, follow-up the patient’s treatment and reinforce prevention measures and treatment adherence. Specific training is given to the health professionals to implement these guidelines. Participants were selected for convenience according to the distribution and operation of services for HIV-positive patients in the four health units.

Each participant answered a semi-structured questionnaire divided into five-sections, including sociodemographic characteristics, HBV and HIV/HBV co-infection knowledge and practices regarding handling patients with HIV/HBV co-infection, and participant vaccination status (S2 File). The questions were closed with one open option at the end to include any additional information from the participant. The questions were revised to adapt to the participants’ comprehension based on a pre-test.

Data collection

For the desk review, relevant official documents from the Ministry of Health (MoH) were reviewed. The documents were obtained through the government portal and MoH website, using keywords: Hepatitis B, HIV/hepatitis B co-infection, policy, norm, Mozambique, and some documents were provided in physical or electronic format by key informants. The literature review was done electronically using PubMed, Google Academic and Hinari databases. For the search, the words Mozambique with hepatitis B, HIV/HBV co-infection, policies, norms and HIV/HBV co-infection with policies and norms were cross-referenced. Each document was reviewed in a systematized manner, and documents in Portuguese or English were included from the period of January 1977 to February 2019. Only articles available in the full text were reviewed. After the literature search, all abstracts were extracted and screened. The relevant papers and the documents obtained via key informants and desk review were included in this study (PRISMA diagram). After explaining the study procedure and respecting confidentiality and privacy, all participants voluntarily gave written informed consent. Key informants were approached by the principal investigator at their working sectors to conduct a 30 minutes interview focused on the existing policies for the prevention, diagnosis and treatment of HIV and HBV co-infected patients. It included information regarding the documents found in the desk review, the capture of other relevant documents and clarification of possible points of divergence from the information reviewed.

The researcher interviewed HPs for approximately 45–60 minutes at the participants’ most convenient time without workload. The questionnaires were in Portuguese, the local national language.

Data management and analysis

The policy documents were organized according to type, year and document source, key information regarding policies on HBV prevention, diagnosis and treatment in HIV co-infected patients. Policy documents from the MoH and articles were reviewed to describe policies. Each document was reviewed in a systematized manner to identify the type of document, the name and year of publication, and key policy information for the prevention, diagnosis and management of hepatitis in HIV/HBV co-infected patients.

A content analysis of the policy documents regarding the prevention, diagnosis and management of HIV/HBV co-infection was performed. The content of the documents was transcribed to Excel, where they were tabulated according to the predefined themes for describing policies on prevention, diagnosis and treatment of HIV/HBV co-infection patients. The analysis theme was based on the WHO "Monitoring and Evaluation of Viral Hepatitis B and C" Framework [14] for eliminating viral hepatitis as a public health threat by 2030, which describes the ten core indicators for monitoring and evaluation of viral hepatitis B and C. It includes indicators related to the cascade for a cure, such as prevention, testing, diagnosis, treatment, and cure (outputs and outcomes).

New themes that emerged were added to the document table. For Knowledge and practices about HIV and HBV co-infection among health professionals’ data were collected in a questionnaire paper form and then entered into a database on Open Data Kit (ODK) [30] in a tablet. After cleaning, the data were imported into the Scientific Package for Health Sciences (SPSS) Program in version 20 for analysis.

To ensure data quality, a daily review of each questionnaire was carried out to assess their consistency and completeness. All out-of-bounds values were reviewed and corrected. This review was carried out during the data collection process and after entering the data. A descriptive analysis of the socio-demographic, knowledge and practice variables was presented. Given the relevance of some questions, a bivariate analysis of the association between the knowledge and practice variables and the socio-demographic variables (gender, professional experience, profession) was carried out using the Pearson Chi-square test (X²) using a 5% statistical significance level to see if the response was different according to socio-demographic characteristics.

Results

Policy review

Forty documents were identified, 36 resulting from the document and literature review and four provided by key informants. Twenty-one policy documents were included in the study, 17 national and four international. Nineteen documents were excluded because they were not related to HIV and HBV co-infection policies and were not related to Mozambique. We found ordinances, decrees, strategic plans, treatment guides, and resolutions. Fig 1 presents the the document review diagram adapted from Moher D, 2009.

Download:

Fig 1. Document review diagram.

Source: adapted from Prism Diagram. Moher D, 2009.

https://doi.org/10.1371/journal.pone.0301305.g001

The documents were established from 1977 and 2019 by the Ministry of Health, Government of Mozambique and WHO, with key information regarding prevention, diagnosis and treatment of HBV in HIV patients (S1 Table).

A key informant from each of the five sectors of origin of the documents was interviewed, namely, from the Blood Bank, National Directorate of Pharmacy, National Program for the Control of STIs-HIV/AIDS and Hepatitis, Immunization Program, and National Blood Service. The key informants were heads of the program or their representatives with an average length of service of 14 years (5 to 27 years). The median age of the five respondents was 44 years, of which three were women.

No specific policy related to HIV/HBV co-infection was found, and recommendations concerning these diseases were in documents related to other policies. The majority of policies were linked to hepatitis B prevention. The biosafety policies were present in different documents, and it has “Safe Injections” through observation of all procedures associated with the preparation of injections, the use of disposable syringes and needles and the proper disposal of material used in the injection. “Blood safety” for the prevention of blood-borne infections for a donation, which includes testing for four infections (HIV, HBV/HCV, Syphilis) and selection of low-risk donors based on a questionnaire, was also legislated (Table 1). A key informant stated that:

“…for all blood-borne diseases, not just Hepatitis B, the first filter is a selection through a questionnaire with exclusion questions for those who have risk factors or risk behaviours for the transmission of Hepatitis B in this case…”(Key informant I)

Download:

Table 1. Existing policies regarding prevention, diagnosis and treatment of hepatitis B.

https://doi.org/10.1371/journal.pone.0301305.t001

In 2006, the MoH introduced the HBV vaccine, which is administered to children under one year of age as part of a pentavalent vaccine (Diphtheria, Pertussis, Tetanus, Hepatitis B and Hib) at month 2, month 3 and month 4 of age. In 2009, MoH recommended vaccination against HBV for adults, adolescents and pregnant women who were victims of rape. In 2014, the guidelines were updated to include children after a rape and health professionals after exposure. The HBV vaccine is administered immediately after the event, in the 1st and 6th months, in a total of 3 doses. These policies do not include routine vaccination of risk groups such as health professionals, HIV positive patients, drug users and neonates (Table 1).

“Well, this is a pentavalent vaccine, in addition to Hepatitis B, there are others, DTP, Hepatitis B,… .so it is a conjugate vaccine, so it is not a single Hepatitis B vaccine… we are thinking of giving the vaccine to the Newborn, but it’s still a plan……”(Key informant II)

Regarding the diagnosis of HBV infection, we did not find specific regulations. The 2014 Guide for Antiretroviral and Opportunistic Infections Treatment recommends testing for HBV in victims of rape and health professionals after exposure. The Guide does not refer to the diagnosis of HBV in HIV positive patients or other risk groups (men who have sex with men, sex workers, intravenous drug users) (Table 1). On the other hand, key informants referred to tests performed for screening of blood donors.

"(…) few patients arrive at the Central Hospital (…) If we had routine testing for hepatitis in our public network we would have more patients being followed up, but we don’t, so the Central Hospital will receive those patients who are in the disease phase, they have to be followed up at the Central Hospital and those who are referred from our blood services… What is done is testing in blood banks (…) but in general there is no national strategy for Hepatitis testing…” (Key informant III).

Regarding the treatment of HBV infection, the guide for Antiretroviral and Opportunistic Infections Treatment (2016) recommends that the co-infected patient be treated with a therapeutic line containing HBV active drugs (TDF+3TC+EFV). It also recommends strictly monitoring liver and kidney function avoiding alcohol and traditional medicines consumption due to the risk of hepatotoxicity. The National Drug Formulary of September 2007 indicates combinations with Lamivudine for the Treatment of HIV and chronic HBV infection. Key informants mentioned that only HIV/HBV co-infected patients benefit from treatment:

“These patients end up benefiting from HIV treatment, so we still don’t have a follow-up norm; at the moment, what we are doing here as Ministry of Health, we are preparing our national guide for the screening, diagnosis, treatment of patients with Hepatitis. We have a technical group working on it.” (Key informant III)

Health professionals’ knowledge and practice

For the assessment of knowledge and practices, 52 HPs were interviewed. The mean age was 35 years old (Min 23- Max 58), and 40 (77%) were female. All participants were trained in management of HIV/AIDS, in contrast, only 7 (14%) had received training related to HBV. Seventy-one % of participants reported having received at least one dose of the HBV vaccine. However, only 11 (21%) received all three doses, and only 9 (17%) knew how many doses were needed to provide immunity against the infection. “Table 2” presents the sociodemographic characteristics, vaccination status and distribution of the participants by health facility and training in HBV.

Download:

Table 2. Sociodemographic characteristics, vaccination status and distribution of participants by health facility and training in HBV.

https://doi.org/10.1371/journal.pone.0301305.t002

Knowledge about HBV infection and HIV/HBV co-infection.

In the evaluation of knowledge, 98% of the participants already had information about HBV infection. Regarding the mode of transmission, 38 (73%) reported shared sharp objects, 25 (48%) participants mentioned sexual contact, 15 (29%) blood transfusion and 10 (19%) mother-to-child transmission. Regarding the prevention methods, 18 (35%) reported using condoms, and only 7 (14%) of the participants mentioned vaccination to prevent HBV. None of the medical technicians or counselors described the vaccine as a means of prevention.

Regarding diagnosis, only 8 (15%) described that the HBsAg marker is used to screen for HBV.

Regarding treatment, 12 (33%) have information that hepatitis B is treatable; of these, 5 (14%) medical doctors, 5 (14%) medical technician and 2 (5%) nurses described that Tenofovir (TDF) is the drug indicated for the treatment of HBV infection. No medical technician described TDF as the drug indicated for the treatment of HBV infection. In the group of doctors, 2 (25%) said they did not know about the drug indicated for the treatment of HBV infection. In the group of nurses, only one reported that TDF is the drug indicated for the treatment of HBV infection. Counselors were excluded from this analysis, as they do not receive training on treatment modalities.

Regarding knowledge about HBV and HIV co-infection, 50 (96%) of the participants reported knowing that HBV and HIV can exist in the same patient. Only 12 (33%) knew about HBV complications in the co-infected patient (Cirrhosis 11, hepatocellular carcinoma 6, Chronic Hepatitis 2 and Hepatotoxicity to ARVs 1) (Table 3). Only 12 (33%) of the participants knew about HBV treatment in patients with HIV and the therapeutic lines indicated for its treatment (it includes two active drugs, Tenofovir and Lamivudine). Counsellors were once again excluded. “Table 3” presents the Knowledge about Hepatitis B and HIV/HBV co-infection.

Download:

Table 3. Knowledge about hepatitis B infection and HIV/HBV co-infection.

https://doi.org/10.1371/journal.pone.0301305.t003

Knowledge about HIV and HBV co-infection according to sociodemographic characteristics.

We did not find an association between knowing whether HIV and HBV can exist in the same patient and gender (p = 0.412), profession (p = 0.197) or professional experience (p = 0.269). However, we found an association between knowledge about complications and profession (p = 0.001), where medical doctors had more knowledge. It was observed that there was an association between knowing that there is HBV treatment in patients with HIV and the professional category (p = 0.009), where medical doctors and medical technicians had more knowledge. This association was not observed with gender (p = 0.433) and professional experience (p = 0.345).”S2 Table”. Counsellors were excluded from this analysis as they do not treat patients.

Practices of health professionals in relation to the handling of co-infected patients

Only 15 (29%) of the participants reported screening for HBV in patients with HIV; 6 (11%) of the nurses, 4 (8%) of the medical doctors, 4 (8%) of the medical technicians and 1 (2%) of the counsellors. Only 11 (21%) reported having counselled on prevention of transmission of HBV; 4 (8%) medical doctors, 4 (8%) nurses, and 3 (5%) medical technicians. No Counsellor reported counselling to prevent the transmission of HBV infection in HIV positive patients. Only 9 (17%) provide counselling on risk behaviors (alcohol consumption, use of traditional medicine, use of intravenous drugs, use of condoms and sharing of syringes) as per the policy recommendation; 4 (8%) medical doctors, 3 (5%) medical technicians and 2 (4%) nurses. None of the counsellors reported counselling about risky behaviors. About what signs to look for in the patient with co-infection, the majority of participants 25 (48%) referred to jaundice. Only 4 (8%) participants mentioned having treated patients with hepatitis B “Table 4”.

Download:

Table 4. Practices of health professionals regarding HBV and HIV co-infection.

https://doi.org/10.1371/journal.pone.0301305.t004

Health professionals’ practices and sociodemographic characteristics

No statistically significant relationship was found between screening HIV patients for HBV and gender (p = 0.288), professional category (0.076) and professional experience (0.056). We found an association between counselling for prevention and professional categories (p = 0.028); 4 (36%) medical doctors and 4 (36%) nurses reported giving advice. It was also found that there was a statistically significant relationship between profession and counselling on risk factors (p = 0.009), where 4 (44%) were medical doctors, 3 (33%) medical technicians, and 2 (22%) nurses “S3 Table”.

Discussion

This study was the first carried out in Mozambique on policy review and assessment of the knowledge and practices of health professionals on HIV/HBV co-infection. We did not find studies on health professionals’ knowledge and practices concerning HIV/HBV co-infection. Additionally, we did not find policy documents specific for HIV/HBV co-infection; some guidelines were found in other policies. Most recommendations were related to the prevention of infections. Prevention measures and screening strategies for specific groups were not found, including health professionals, HIV positive patients, or other risk groups (men who have sex with men, sex workers, and intravenous drug users). The current prevention strategy is to vaccinate children under one year of age (under the Expanded Program on Vaccination) without including neonates for the prevention of HBV transmission from mother to child. Screening could help identify those who need treatment and those who would benefit from vaccination. A study in the United States has shown that strategies to screen and treat or vaccinate are cost-effective in reducing the burden of hepatitis B virus among high-prevalence populations [31].

Diagnosed HIV/HBV co-infected patients would benefit from specific guidelines on monitoring for early detection of complications and referral to a high-level facility with a specialist. The policy should be accompanied by health professionals’ awareness, training and engagement to adhere to the guidelines. Studies have described low compliance with hepatocellular carcinoma screening in HIV/HBV co-infected patients, resulting in late management [24, 25]. Only one policy explicitly referred to HIV/HBV co-infection. This was a policy about the use of drugs active against HBV and HIV, a recommendation aligned with the international guidelines [32].

These results are similar to those found in a study carried out in Ethiopia [33], which revealed a lack of treatment policies and strategies for testing, diagnosis and treatment of hepatitis B. A study in Ghana [34] showed that despite the high prevalence of co-infection (12.3%), there were no policies regarding prevention, testing for HBV, or patient management in newly diagnosed HIV-positive patients. There is a need to formulate policies and identify at-risk groups who can benefit from testing, care, and treatment.

The assessment of knowledge and practices involved different categories of health professionals. We included medical doctors, medical technicians, nurses, and counsellors, as they play a critical role in the HIV/HBV co-infected care chain. Although they can intervene in any step, counsellors are more involved with prevention, nurses with screening and medical doctors and technicians with diagnosis, treatment and follow-up. Most health professionals were aware of the coexistence of HIV and HBV co-infection. When asked about transmission, preventions, diagnosis, treatment, and cure, the knowledge was insufficient. Except for a few parameters, there were no differences among all categories of health professionals participating in the study. Most professionals failed to indicate vaccinations as a preventive measure. These findings are similar to studies in India and Malawi, where health professionals had poor knowledge towards HIV/AIDS, HBV and HCV and the need for education on preventing HBV was recommended [35]. It is essential that health professionals know about transmission and prevention measures for HIV/HBV co-infection, not only to counselling their patients but also to protect themselves from the risk of being infected while caring for a patient.

Diagnosing HBV infection through testing for the Hepatitis B Surface Antigen (HBsAg) was also an area of insufficient knowledge. However, there were differences between medical doctors and medical technicians who stood out compared to nurses and counselors. The better performance of medical doctors and medical technicians is expected due to their training in the diagnosis. This result is similar to that reported by Ahmad et al. [36], who showed that knowledge was associated with the professional category. Studies have described HBsAg detection as an accurate test to use in primary care not only for the diagnosis but also for patient monitoring [37, 38].

The study also showed insufficient knowledge about treatment for hepatitis B in HIV co-infected patient. Although they were better than the others, the two categories responsible for treating the patient did not perform well (7 out of 17 medical doctors and technicians did not respond correctly). Few health professionals knew the complications of HBV infection in patients with HIV. A study in Ghana to assess the prevalence of HBV in HIV patients [39] showed that health professionals had insufficient knowledge regarding handling patients with HIV/HBV co-infection, indicating the need for regular training of health professionals about hepatitis B. This lack of knowledge of health professionals can lead to the loss of opportunities for preventing, diagnosing and treating hepatitis B in the co-infected patient.

WHO [23] recommends testing for HBV in all newly diagnosed HIV-positive patients, Hepatitis B vaccination for those who are seronegative for HBV, appropriate treatment of HIV/HBV co-infected and follow-up with control of the degree of liver damage for diagnosis of cirrhosis or hepatocellular carcinoma.

Less than a third of the health professionals reported having provided counselling to prevent the transmission of infection and risk reduction. Counsellors are expected to do so, given their HIV patient care chain role. The lack of training on HIV/HBV co-infection can contribute to these malpractices. Health professionals are also not routinely screening HIV patients for HBV infection. The absence of clear guidelines and training may be a factor that impedes these activities. The cascade of care for HIV positive patients in Mozambique is well defined, with high adherence from the health professionals indicating that clear guidelines embedded in HIV care would help to improve co-infected patient care.

In the study, about 71% of health professionals had received at least one dose of the HBV vaccine. Still, only 17% know how many doses are needed to protect against infection. It shows a lack of knowledge among health professionals about the risk of HBV infection, HBV vaccine, and the importance of being fully vaccinated given the high risk of contracting the infection. We did not find a policy that recommends health professionals to be vaccinated except in case of accidental exposure. The absence of guidelines can also play a role in health professional’s vaccine uptake. WHO recommends HBV vaccination to all healthcare professionals to prevent HBV transmission in the health care unit. These results do not differ from those found in other countries in the sub-Saharan region, such as Ethiopia, Nigeria [40] and Saudi Arabia [41]. Despite health professionals being aware of the vaccine, very few are vaccinated, with low vaccination rates for Hepatitis B in health professionals with even lower rates in the administration of the three doses of the vaccine.

Taking into account the WHO recommended framework of "Monitoring and Evaluation of Viral Hepatitis B and C" for the elimination of viral hepatitis as a public health threat by 2030 [17, 42]; this study focused on the issue related to facilitating factors that consisted of analyzing existing policies and norms for the handling of patients co-infected with HIV/HBV and evaluating an important factor that can affect the cascade of cure, which is the knowledge and practices of health professionals in relation to handling HIV/HBV co-infection. It was observed that there are gaps in the definition of specific policies for co-infected patients and in monitoring the cascade for cure.

Study limitation

The Health Centers included in the study are not representative of the whole country. The number of participants in the study is small and the fact that it included counsellors may have led to the observed limitation in knowledge. An analysis stratified by group was carried out to minimize this limitation. The results relating to the analysis of knowledge according to socio-demographic characteristics should be interpreted with caution given that the number of participants was low and these results were presented as a supplemental tables (S2 and S3 Tables).

Conclusions

The study found inadequate policies for preventing, diagnosing, and managing patients with HIV/HBV co-infection. Knowledge about HIV/HBV co-infection was deficient among health professionals, and few knew that HBV vaccination was an effective way to prevent infection. Notably, very few health professionals were vaccinated against HBV. Defining more specific policies, training the health professionals and monitoring their activity may help increase awareness, counselling for disease prevention, early diagnosis and proper treatment of HIV/HBV co-infected patients, as we observed with HIV care.

Supporting information

S1 Table. Documents related to the existing HIV/Hepatitis B virus co-infection policies.

https://doi.org/10.1371/journal.pone.0301305.s001

(DOCX)

S2 Table. Knowledge about co-infection and sociodemographic characteristics.

https://doi.org/10.1371/journal.pone.0301305.s002

(DOCX)

S3 Table. Practices and sociodemographic characteristics.

https://doi.org/10.1371/journal.pone.0301305.s003

(DOCX)

S1 File. Questionnaire for key informants.

https://doi.org/10.1371/journal.pone.0301305.s004

(DOCX)

S2 File. Questionnaire for health professionals.

https://doi.org/10.1371/journal.pone.0301305.s005

(DOCX)

Acknowledgments

We would like to give special thanks to all the participants who accepted to be part of this study. All health professionals at the health facilities where the study took place for their support and collaboration during data collection. To the local Health Centers of Mavalane, Alto-Maé, 1° de Maio and Polana Caniço, where the data were collected. To the General Hospitals of Mavalane, Polana Caniço and Chamanculo. To Mr. Hélio Martins and Mrs. Luiza Huo for helping with the statistical analysis of the data for this project.

References

1. UNAIDS. THE PATH THAT ENDS AIDS 2023 UNAIDS GLOBAL AIDS UPDATE EXECUTIVE SUMMARY [Internet]. Geneva; 2023. Available from: http://www.wipo.int/amc/en/mediation/rules
- View Article
- Google Scholar
2. UNAIDS. Global HIV statistics [Internet]. 2023 [cited 2024 Jan 20]. Available from: https://www.unaids.org/en/resources/fact-sheet
- View Article
- Google Scholar
3. UNAIDS. UNAIDS DATA 2022 [Internet]. Geneva; 2022 [cited 2024 Jan 20]. Available from: https://www.unaids.org/sites/default/files/media_asset/data-book-2022_en.pdf
- View Article
- Google Scholar
4. MISAU I. Inquérito de Indicadores de Imunização, Malária e HIV/SIDA em Moçambique (IMASIDA).
5. Hoffmann CJ, Thio CL. Clinical implications of HIV and hepatitis B co-infection in Asia and Africa. 2007;7:402–9. pmid:17521593
- View Article
- PubMed/NCBI
- Google Scholar
6. Mena G, García-Basteiro AL, Bayas JM. Hepatitis B and A vaccination in HIV-infected adults: A review. Hum Vaccin Immunother. 2015;11(11):2582–98. pmid:26208678
- View Article
- PubMed/NCBI
- Google Scholar
7. WHO. Global progress report on HIV, viral hepatitis and sexually transmitted infections, 2021 [Internet]. Geneva; 2021 [cited 2024 Jan 20]. Available from: https://www.who.int/publications/i/item/9789240027077
- View Article
- Google Scholar
8. Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol. 2006;44(SUPPL. 1):6–9. pmid:16352363
- View Article
- PubMed/NCBI
- Google Scholar
9. Spearman CW, Afihene M, Ally R, Apica B, Awuku Y, Cunha L, et al. Hepatitis B in sub-Saharan Africa: strategies to achieve the 2030 elimination targets. Lancet Gastroenterol Hepatol. 2017;2(12):900. pmid:29132759
- View Article
- PubMed/NCBI
- Google Scholar
10. Stokx J, Gillet P, De Weggheleire A, Casas EC, Maendaenda R, Beulane AJ, et al. Seroprevalence of transfusion-transmissible infections and evaluation of the pre-donation screening performance at the Provincial Hospital of Tete, Mozambique. BMC Infect Dis. 2011;11(1):141. pmid:21605363
- View Article
- PubMed/NCBI
- Google Scholar
11. Viegas EO, Tembe N, Macovela E, Gonçalves E, Augusto O, Ismael N, et al. Incidence of HIV and the Prevalence of HIV, Hepatitis B and Syphilis among Youths in Maputo, Mozambique: A Cohort Study. PLoS One. 2015;1–15. pmid:25798607
- View Article
- PubMed/NCBI
- Google Scholar
12. Abeje G, Azage M. Hepatitis B vaccine knowledge and vaccination status among health care workers of Bahir Dar City Administration, Northwest Ethiopia: A cross sectional study. BMC Infect Dis. 2015;15(1):1–6. pmid:25637342
- View Article
- PubMed/NCBI
- Google Scholar
13. Muriuki BM, Gicheru MM, Wachira D, Nyamache AK, Khamadi SA. Prevalence of hepatitis B and C viral co-infections among HIV-1 infected individuals in Nairobi, Kenya. BMC Res Notes. 2013;6(1):1. pmid:24016453
- View Article
- PubMed/NCBI
- Google Scholar
14. Sun HY, Sheng WH, Tsai MS, Lee KY, Chang SY, Hung CC. Hepatitis B virus coinfection in human immunodeficiency virus-infected patients: A review. World J Gastroenterol. 2014;20(40):14598–614. pmid:25356024
- View Article
- PubMed/NCBI
- Google Scholar
15. Archampong TNA, Lartey M, Sagoe KW, Obo-Akwa A, Kenu E, Gillani FS, et al. Proportion and factors associated with Hepatitis B viremia in antiretroviral treatment naïve and experienced HIV co-infected Ghanaian patients. BMC Infect Dis. 2016;16(1):1–9.
- View Article
- Google Scholar
16. Badawi MM, Atif MS, Mustafa YY. Systematic review and meta-analysis of HIV, HBV and HCV infection prevalence in Sudan. Virol J. 2018;15(148):1–16. pmid:30253805
- View Article
- PubMed/NCBI
- Google Scholar
17. WHO. Global health sector strategy on viral hepatitis 2016–2021. Global Hepatitis Programme Department of HIV/AIDS [Internet]. 2016 [cited 2019 Oct 20];(June):56. Available from: https://www.who.int/publications/i/item/WHO-HIV-2016.06
18. Deressa T, Damtie D, Fonseca K, Gao S, Abate E, Alemu S, et al. The burden of hepatitis B virus (HBV) infection, genotypes and drug resistance mutations in human immunodeficiency virus-positive patients in Northwest Ethiopia. PLoS One. 2017;12(12):1–11. pmid:29281718
- View Article
- PubMed/NCBI
- Google Scholar
19. Rachel M, Barbara C, Murphy C, Komujuni C, Nyakato P, Ocama P, et al. Uptake of hepatitis B-HIV co-infection screening and management in a resource limited setting. Hepatol Med Policy. 2018;3(1):1–7.
- View Article
- Google Scholar
20. Platt L, French CE, McGowan CR, Sabin K, Gower E, Trickey A, et al. Prevalence and burden of HBV co-infection among people living with HIV: A global systematic review and meta-analysis. J Viral Hepat. 2020;27(3):294–315. pmid:31603999
- View Article
- PubMed/NCBI
- Google Scholar
21. Chambal LM, Samo Gudo E, Carimo A, Corte Real R, Mabunda N, Maueia C, et al. HBV infection in untreated HIV-infected adults in Maputo, Mozambique. PLoS One. 2017;12(7):1–12.
- View Article
- Google Scholar
22. Cunha L, Carrilho C, Bhatt N, Loforte M, Maueia C, Fernandes F, et al. HIV infection in Mozambican patients. Cancer Treat Res Commun. 2019;
- View Article
- Google Scholar
23. WHO. Guideline For The Prevention, Care And Treatment Of Persons With Chronic Hepatitis B Infection. 2015 [cited 2019 Oct 20];(April):124. Available from: https://www.who.int/publications/i/item/9789241549059
- View Article
- Google Scholar
24. Hearn B, Chasan R, Bichoupan K, Suprun M, Bagiella E, Dieterich DT, et al. Low Adherence of HIV providers to practice guidelines for hepatocellular carcinoma screening in HIV/Hepatitis B Coinfection. Clinical Infectious Diseases. 2015;61(11):1742–8. pmid:26240206
- View Article
- PubMed/NCBI
- Google Scholar
25. Willemse S, Smit C, Sogni P, Sarcletti M, Uberti-Foppa C, Wittkop L, et al. Low compliance with hepatocellular carcinoma screening guidelines in hepatitis B/C virus co-infected HIV patients with cirrhosis. J Viral Hepat. 2019;26(10):1224–8. pmid:31136059
- View Article
- PubMed/NCBI
- Google Scholar
26. Peksen Y, Canbaz S, Leblebicioglu H, Sunbul M, Esen S, Sunter AT. Primary care physicians’ approach to diagnosis and treatment of hepatitis B and hepatitis C patients. BMC Gastroenterol. 2004;4:1–6.
- View Article
- Google Scholar
27. Al-Hazmi AH. Knowledge, attitudes and practice of primary health care physicians towards hepatitis B virus in Al-Jouf province, Saudi Arabia. BMC Res Notes. 2014;7(1):1–7. pmid:24885149
- View Article
- PubMed/NCBI
- Google Scholar
28. Upadhyaya N., Chang R., Davis C., Conti M. C., Salinas-Garcia D., & Tang H. Chronic hepatitis B: perceptions in Asian American communities and diagnosis and management practices among primary care physicians. Postgrad Med. 2010;122(5):165–175. pmid:20861600
- View Article
- PubMed/NCBI
- Google Scholar
29. INE. Anuário estatístico 2017- Moçambique. Instituto Nacional de Estatística. Moçambique; 2017.
30. Hartung C, Anokwa Y, Brunette W, Lerer A, Tseng C, Borriello G. Open data kit: Tools to build information services for developing regions. ACM International Conference Proceeding Series. 2010;
- View Article
- Google Scholar
31. Chahal HS, Peters MG, Harris AM, McCabe D, Volberding P, Kahn JG. Cost-effectiveness of Hepatitis B Virus Infection Screening and Treatment or Vaccination in 6 High-risk Populations in the United States. Open Forum Infect Dis. 2019;6(1). pmid:30931346
- View Article
- PubMed/NCBI
- Google Scholar
32. Cheng Zhimeng, Lin Panpan and NC. HBV/HIV Coinfection: Impact on the Development and Clinical Treatment of Liver Diseases. Front Med. 2021;
- View Article
- Google Scholar
33. Shiferaw F, Letebo M, Bane A. Chronic viral hepatitis: policy, regulation, and strategies for its control and elimination in Ethiopia. BMC Public Health. 2016;16(1):1–13.
- View Article
- Google Scholar
34. Agyeman AA, Ofori-Asenso R. Prevalence of HIV and hepatitis B coinfection in Ghana: A systematic review and meta-analysis. AIDS Res Ther. 2016;13(1):1–9. pmid:27190544
- View Article
- PubMed/NCBI
- Google Scholar
35. Mtengezo J, Lee H, Ngoma J, Kim S, Aronowitz T, DeMarco R, et al. Knowledge and attitudes toward HIV, hepatitis B virus, and hepatitis C virus infection among health-care workers in Malawi. Asia Pac J Oncol Nurs. 2016;3(4):344–51. pmid:28083551
- View Article
- PubMed/NCBI
- Google Scholar
36. Ahmad A, Munn Sann L, Abdul Rahman H. Factors associated with knowledge, attitude and practice related to hepatitis B and C among international students of Universiti Putra Malaysia. BMC Public Health. 2016;16(1):1–8. pmid:27443276
- View Article
- PubMed/NCBI
- Google Scholar
37. Veldhuijzen IK, Mostert MC, Niesters HGM, Richardus JH, De Man RA. Accuracy of a referral guideline for patients with chronic hepatitis B in primary care to select patients eligible for evaluation by a specialist. Gut. 2007;56(7):1027–8. pmid:17566039
- View Article
- PubMed/NCBI
- Google Scholar
38. Chan HLY, Thompson A, Martinot-Peignoux M, Piratvisuth T, Cornberg M, Brunetto MR, et al. Hepatitis B surface antigen quantification: Why and how to use it in 2011—A core group report. J Hepatol. 2011;55(5):1121–31. pmid:21718667
- View Article
- PubMed/NCBI
- Google Scholar
39. Kye-Duodu G, Nortey P, Malm K, Nyarko KM, Sackey SO, Ofori S, et al. Prevalence of hepatitis B virus co-infection among HIV-seropositive persons attending antiretroviral clinics in the Eastern Region of Ghana. Pan African Medical Journal. 2016;25(Supp 1):1–6. pmid:28210375
- View Article
- PubMed/NCBI
- Google Scholar
40. Malewezi B, Omer SB, Mwagomba B, Araru T. Protecting health workers from nosocomial Hepatitis B infections: A review of strategies and challenges for implementation of Hepatitis B vaccination among health workers in Sub-Saharan Africa. J Epidemiol Glob Health. 2016;6(4):229–41. pmid:27154428
- View Article
- PubMed/NCBI
- Google Scholar
41. Alshammari TM, Aljofan M, Subaie G, Hussain T. Knowledge, awareness, attitude, and practice of health-care professionals toward hepatitis B disease and vaccination in Saudi Arabia. Hum Vaccin Immunother. 2019;15(12):2816–23. pmid:31226008
- View Article
- PubMed/NCBI
- Google Scholar
42. WHO. Consolidated strategic information Guidelines for viral hepatitis [Internet]. 2019 [cited 2024 Jul 9]. 29 p. Available from: https://www.who.int/publications/i/item/9789241515191
- View Article
- Google Scholar

[ref1] 1. UNAIDS. THE PATH THAT ENDS AIDS 2023 UNAIDS GLOBAL AIDS UPDATE EXECUTIVE SUMMARY [Internet]. Geneva; 2023. Available from: http://www.wipo.int/amc/en/mediation/rules
View Article
Google Scholar

[2] View Article

[3] Google Scholar

[ref2] 2. UNAIDS. Global HIV statistics [Internet]. 2023 [cited 2024 Jan 20]. Available from: https://www.unaids.org/en/resources/fact-sheet
View Article
Google Scholar

[5] View Article

[6] Google Scholar

[ref3] 3. UNAIDS. UNAIDS DATA 2022 [Internet]. Geneva; 2022 [cited 2024 Jan 20]. Available from: https://www.unaids.org/sites/default/files/media_asset/data-book-2022_en.pdf
View Article
Google Scholar

[8] View Article

[9] Google Scholar

[ref4] 4. MISAU I. Inquérito de Indicadores de Imunização, Malária e HIV/SIDA em Moçambique (IMASIDA).

[ref5] 5. Hoffmann CJ, Thio CL. Clinical implications of HIV and hepatitis B co-infection in Asia and Africa. 2007;7:402–9. pmid:17521593
View Article
PubMed/NCBI
Google Scholar

[12] View Article

[13] PubMed/NCBI

[14] Google Scholar

[ref6] 6. Mena G, García-Basteiro AL, Bayas JM. Hepatitis B and A vaccination in HIV-infected adults: A review. Hum Vaccin Immunother. 2015;11(11):2582–98. pmid:26208678
View Article
PubMed/NCBI
Google Scholar

[16] View Article

[17] PubMed/NCBI

[18] Google Scholar

[ref7] 7. WHO. Global progress report on HIV, viral hepatitis and sexually transmitted infections, 2021 [Internet]. Geneva; 2021 [cited 2024 Jan 20]. Available from: https://www.who.int/publications/i/item/9789240027077
View Article
Google Scholar

[20] View Article

[21] Google Scholar

[ref8] 8. Alter MJ. Epidemiology of viral hepatitis and HIV co-infection. J Hepatol. 2006;44(SUPPL. 1):6–9. pmid:16352363
View Article
PubMed/NCBI
Google Scholar

[23] View Article

[24] PubMed/NCBI

[25] Google Scholar

[ref9] 9. Spearman CW, Afihene M, Ally R, Apica B, Awuku Y, Cunha L, et al. Hepatitis B in sub-Saharan Africa: strategies to achieve the 2030 elimination targets. Lancet Gastroenterol Hepatol. 2017;2(12):900. pmid:29132759
View Article
PubMed/NCBI
Google Scholar

[27] View Article

[28] PubMed/NCBI

[29] Google Scholar

[ref10] 10. Stokx J, Gillet P, De Weggheleire A, Casas EC, Maendaenda R, Beulane AJ, et al. Seroprevalence of transfusion-transmissible infections and evaluation of the pre-donation screening performance at the Provincial Hospital of Tete, Mozambique. BMC Infect Dis. 2011;11(1):141. pmid:21605363
View Article
PubMed/NCBI
Google Scholar

[31] View Article

[32] PubMed/NCBI

[33] Google Scholar

[ref11] 11. Viegas EO, Tembe N, Macovela E, Gonçalves E, Augusto O, Ismael N, et al. Incidence of HIV and the Prevalence of HIV, Hepatitis B and Syphilis among Youths in Maputo, Mozambique: A Cohort Study. PLoS One. 2015;1–15. pmid:25798607
View Article
PubMed/NCBI
Google Scholar

[35] View Article

[36] PubMed/NCBI

[37] Google Scholar

[ref12] 12. Abeje G, Azage M. Hepatitis B vaccine knowledge and vaccination status among health care workers of Bahir Dar City Administration, Northwest Ethiopia: A cross sectional study. BMC Infect Dis. 2015;15(1):1–6. pmid:25637342
View Article
PubMed/NCBI
Google Scholar

[39] View Article

[40] PubMed/NCBI

[41] Google Scholar

[ref13] 13. Muriuki BM, Gicheru MM, Wachira D, Nyamache AK, Khamadi SA. Prevalence of hepatitis B and C viral co-infections among HIV-1 infected individuals in Nairobi, Kenya. BMC Res Notes. 2013;6(1):1. pmid:24016453
View Article
PubMed/NCBI
Google Scholar

[43] View Article

[44] PubMed/NCBI

[45] Google Scholar

[ref14] 14. Sun HY, Sheng WH, Tsai MS, Lee KY, Chang SY, Hung CC. Hepatitis B virus coinfection in human immunodeficiency virus-infected patients: A review. World J Gastroenterol. 2014;20(40):14598–614. pmid:25356024
View Article
PubMed/NCBI
Google Scholar

[47] View Article

[48] PubMed/NCBI

[49] Google Scholar

[ref15] 15. Archampong TNA, Lartey M, Sagoe KW, Obo-Akwa A, Kenu E, Gillani FS, et al. Proportion and factors associated with Hepatitis B viremia in antiretroviral treatment naïve and experienced HIV co-infected Ghanaian patients. BMC Infect Dis. 2016;16(1):1–9.
View Article
Google Scholar

[51] View Article

[52] Google Scholar

[ref16] 16. Badawi MM, Atif MS, Mustafa YY. Systematic review and meta-analysis of HIV, HBV and HCV infection prevalence in Sudan. Virol J. 2018;15(148):1–16. pmid:30253805
View Article
PubMed/NCBI
Google Scholar

[54] View Article

[55] PubMed/NCBI

[56] Google Scholar

[ref17] 17. WHO. Global health sector strategy on viral hepatitis 2016–2021. Global Hepatitis Programme Department of HIV/AIDS [Internet]. 2016 [cited 2019 Oct 20];(June):56. Available from: https://www.who.int/publications/i/item/WHO-HIV-2016.06

[ref18] 18. Deressa T, Damtie D, Fonseca K, Gao S, Abate E, Alemu S, et al. The burden of hepatitis B virus (HBV) infection, genotypes and drug resistance mutations in human immunodeficiency virus-positive patients in Northwest Ethiopia. PLoS One. 2017;12(12):1–11. pmid:29281718
View Article
PubMed/NCBI
Google Scholar

[59] View Article

[60] PubMed/NCBI

[61] Google Scholar

[ref19] 19. Rachel M, Barbara C, Murphy C, Komujuni C, Nyakato P, Ocama P, et al. Uptake of hepatitis B-HIV co-infection screening and management in a resource limited setting. Hepatol Med Policy. 2018;3(1):1–7.
View Article
Google Scholar

[63] View Article

[64] Google Scholar

[ref20] 20. Platt L, French CE, McGowan CR, Sabin K, Gower E, Trickey A, et al. Prevalence and burden of HBV co-infection among people living with HIV: A global systematic review and meta-analysis. J Viral Hepat. 2020;27(3):294–315. pmid:31603999
View Article
PubMed/NCBI
Google Scholar

[66] View Article

[67] PubMed/NCBI

[68] Google Scholar

[ref21] 21. Chambal LM, Samo Gudo E, Carimo A, Corte Real R, Mabunda N, Maueia C, et al. HBV infection in untreated HIV-infected adults in Maputo, Mozambique. PLoS One. 2017;12(7):1–12.
View Article
Google Scholar

[70] View Article

[71] Google Scholar

[ref22] 22. Cunha L, Carrilho C, Bhatt N, Loforte M, Maueia C, Fernandes F, et al. HIV infection in Mozambican patients. Cancer Treat Res Commun. 2019;
View Article
Google Scholar

[73] View Article

[74] Google Scholar

[ref23] 23. WHO. Guideline For The Prevention, Care And Treatment Of Persons With Chronic Hepatitis B Infection. 2015 [cited 2019 Oct 20];(April):124. Available from: https://www.who.int/publications/i/item/9789241549059
View Article
Google Scholar

[76] View Article

[77] Google Scholar

[ref24] 24. Hearn B, Chasan R, Bichoupan K, Suprun M, Bagiella E, Dieterich DT, et al. Low Adherence of HIV providers to practice guidelines for hepatocellular carcinoma screening in HIV/Hepatitis B Coinfection. Clinical Infectious Diseases. 2015;61(11):1742–8. pmid:26240206
View Article
PubMed/NCBI
Google Scholar

[79] View Article

[80] PubMed/NCBI

[81] Google Scholar

[ref25] 25. Willemse S, Smit C, Sogni P, Sarcletti M, Uberti-Foppa C, Wittkop L, et al. Low compliance with hepatocellular carcinoma screening guidelines in hepatitis B/C virus co-infected HIV patients with cirrhosis. J Viral Hepat. 2019;26(10):1224–8. pmid:31136059
View Article
PubMed/NCBI
Google Scholar

[83] View Article

[84] PubMed/NCBI

[85] Google Scholar

[ref26] 26. Peksen Y, Canbaz S, Leblebicioglu H, Sunbul M, Esen S, Sunter AT. Primary care physicians’ approach to diagnosis and treatment of hepatitis B and hepatitis C patients. BMC Gastroenterol. 2004;4:1–6.
View Article
Google Scholar

[87] View Article

[88] Google Scholar

[ref27] 27. Al-Hazmi AH. Knowledge, attitudes and practice of primary health care physicians towards hepatitis B virus in Al-Jouf province, Saudi Arabia. BMC Res Notes. 2014;7(1):1–7. pmid:24885149
View Article
PubMed/NCBI
Google Scholar

[90] View Article

[91] PubMed/NCBI

[92] Google Scholar

[ref28] 28. Upadhyaya N., Chang R., Davis C., Conti M. C., Salinas-Garcia D., & Tang H. Chronic hepatitis B: perceptions in Asian American communities and diagnosis and management practices among primary care physicians. Postgrad Med. 2010;122(5):165–175. pmid:20861600
View Article
PubMed/NCBI
Google Scholar

[94] View Article

[95] PubMed/NCBI

[96] Google Scholar

[ref29] 29. INE. Anuário estatístico 2017- Moçambique. Instituto Nacional de Estatística. Moçambique; 2017.

[ref30] 30. Hartung C, Anokwa Y, Brunette W, Lerer A, Tseng C, Borriello G. Open data kit: Tools to build information services for developing regions. ACM International Conference Proceeding Series. 2010;
View Article
Google Scholar

[99] View Article

[100] Google Scholar

[ref31] 31. Chahal HS, Peters MG, Harris AM, McCabe D, Volberding P, Kahn JG. Cost-effectiveness of Hepatitis B Virus Infection Screening and Treatment or Vaccination in 6 High-risk Populations in the United States. Open Forum Infect Dis. 2019;6(1). pmid:30931346
View Article
PubMed/NCBI
Google Scholar

[102] View Article

[103] PubMed/NCBI

[104] Google Scholar

[ref32] 32. Cheng Zhimeng, Lin Panpan and NC. HBV/HIV Coinfection: Impact on the Development and Clinical Treatment of Liver Diseases. Front Med. 2021;
View Article
Google Scholar

[106] View Article

[107] Google Scholar

[ref33] 33. Shiferaw F, Letebo M, Bane A. Chronic viral hepatitis: policy, regulation, and strategies for its control and elimination in Ethiopia. BMC Public Health. 2016;16(1):1–13.
View Article
Google Scholar

[109] View Article

[110] Google Scholar

[ref34] 34. Agyeman AA, Ofori-Asenso R. Prevalence of HIV and hepatitis B coinfection in Ghana: A systematic review and meta-analysis. AIDS Res Ther. 2016;13(1):1–9. pmid:27190544
View Article
PubMed/NCBI
Google Scholar

[112] View Article

[113] PubMed/NCBI

[114] Google Scholar

[ref35] 35. Mtengezo J, Lee H, Ngoma J, Kim S, Aronowitz T, DeMarco R, et al. Knowledge and attitudes toward HIV, hepatitis B virus, and hepatitis C virus infection among health-care workers in Malawi. Asia Pac J Oncol Nurs. 2016;3(4):344–51. pmid:28083551
View Article
PubMed/NCBI
Google Scholar

[116] View Article

[117] PubMed/NCBI

[118] Google Scholar

[ref36] 36. Ahmad A, Munn Sann L, Abdul Rahman H. Factors associated with knowledge, attitude and practice related to hepatitis B and C among international students of Universiti Putra Malaysia. BMC Public Health. 2016;16(1):1–8. pmid:27443276
View Article
PubMed/NCBI
Google Scholar

[120] View Article

[121] PubMed/NCBI

[122] Google Scholar

[ref37] 37. Veldhuijzen IK, Mostert MC, Niesters HGM, Richardus JH, De Man RA. Accuracy of a referral guideline for patients with chronic hepatitis B in primary care to select patients eligible for evaluation by a specialist. Gut. 2007;56(7):1027–8. pmid:17566039
View Article
PubMed/NCBI
Google Scholar

[124] View Article

[125] PubMed/NCBI

[126] Google Scholar

[ref38] 38. Chan HLY, Thompson A, Martinot-Peignoux M, Piratvisuth T, Cornberg M, Brunetto MR, et al. Hepatitis B surface antigen quantification: Why and how to use it in 2011—A core group report. J Hepatol. 2011;55(5):1121–31. pmid:21718667
View Article
PubMed/NCBI
Google Scholar

[128] View Article

[129] PubMed/NCBI

[130] Google Scholar

[ref39] 39. Kye-Duodu G, Nortey P, Malm K, Nyarko KM, Sackey SO, Ofori S, et al. Prevalence of hepatitis B virus co-infection among HIV-seropositive persons attending antiretroviral clinics in the Eastern Region of Ghana. Pan African Medical Journal. 2016;25(Supp 1):1–6. pmid:28210375
View Article
PubMed/NCBI
Google Scholar

[132] View Article

[133] PubMed/NCBI

[134] Google Scholar

[ref40] 40. Malewezi B, Omer SB, Mwagomba B, Araru T. Protecting health workers from nosocomial Hepatitis B infections: A review of strategies and challenges for implementation of Hepatitis B vaccination among health workers in Sub-Saharan Africa. J Epidemiol Glob Health. 2016;6(4):229–41. pmid:27154428
View Article
PubMed/NCBI
Google Scholar

[136] View Article

[137] PubMed/NCBI

[138] Google Scholar

[ref41] 41. Alshammari TM, Aljofan M, Subaie G, Hussain T. Knowledge, awareness, attitude, and practice of health-care professionals toward hepatitis B disease and vaccination in Saudi Arabia. Hum Vaccin Immunother. 2019;15(12):2816–23. pmid:31226008
View Article
PubMed/NCBI
Google Scholar

[140] View Article

[141] PubMed/NCBI

[142] Google Scholar

[ref42] 42. WHO. Consolidated strategic information Guidelines for viral hepatitis [Internet]. 2019 [cited 2024 Jul 9]. 29 p. Available from: https://www.who.int/publications/i/item/9789241515191
View Article
Google Scholar

[144] View Article

[145] Google Scholar

Figures

Abstract

Background

Methods

Results

Conclusion

Introduction

Materials and methods

Study design and settings

Study population and tools

Data collection

Data management and analysis

Results

Policy review

Health professionals’ knowledge and practice

Knowledge about HBV infection and HIV/HBV co-infection.

Knowledge about HIV and HBV co-infection according to sociodemographic characteristics.

Practices of health professionals in relation to the handling of co-infected patients

Health professionals’ practices and sociodemographic characteristics

Discussion

Study limitation

Conclusions

Supporting information

S1 Table. Documents related to the existing HIV/Hepatitis B virus co-infection policies.

S2 Table. Knowledge about co-infection and sociodemographic characteristics.

S3 Table. Practices and sociodemographic characteristics.

S1 File. Questionnaire for key informants.

S2 File. Questionnaire for health professionals.

Acknowledgments

References