Hepatitis B virus (HBV) infection is estimated to account for 300 million chronic infections and 1 million deaths each year (World Health Organization, 2021). The global burden of HBV infection is unevenly distributed, with particularly high prevalence in some populations in Africa and South East Asia (Cooke et al., 2019). Likewise, HBV is not experienced equally across society, with a disproportionate prevalence and impact on marginalised and deprived populations, whose needs are poorly met by existing healthcare research, services, interventions and policies (O’Hara et al., 2017; Figure 1A). The ‘inclusion health’ agenda focuses on these populations, setting out to identify and address health and social inequities, for example barriers to accessing mainstream healthcare services (Royal College of Physicians, 2022; Aldridge et al., 2018). These groups include, but are not limited to, migrants in vulnerable situations, people experiencing homelessness (PEH), individuals with substance use disorders, commercial sex workers (CSW), incarcerated individuals, and Roma and Traveller communities (Royal College of Physicians, 2022).

Figure 1

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Viral hepatitis is recognised as a global health priority within the United Nations Sustainable Development Goals 2030 (SDG30). These underpin ambitious targets including 90% HBV vaccine coverage, reducing new chronic infections and new infections by 90% and attributable mortality by 65% (Cooke et al., 2019). Vaccination against HBV, including universal birth dose administration, is a key elimination strategy and is estimated to have prevented 310 million cases of HBV infection between 1990 and 2020 (Cooke et al., 2019, de Villiers et al., 2021). However, birth dose vaccine implementation has been slow in reaching the most vulnerable populations, while a three-dose vaccine schedule remains a challenge (de Villiers et al., 2021). Lack of education and awareness, inadequate living conditions, lack of access to healthcare services, and poverty and stigma among marginalised populations create a permissive environment for HBV transmission. Chronic HBV infection usually remains asymptomatic until late complications (liver fibrosis, cirrhosis, and hepatocellular carcinoma (HCC)). Silent infection, in combination with barriers to testing in the most affected populations, explains why only an estimated 10% of those living with HBV infection are diagnosed (O’Hara et al., 2017).

There is no cure for HBV, but antivirals (nucleos(t)ide analogue agents) can suppress viral replication. Based on international treatment guidelines, only a minority of those with chronic infection are eligible for treatment, and a small proportion of these can actually access consistent therapy (McNaughton et al., 2021). Risk stratification requires consistent surveillance (including clinical review, imaging and laboratory tests), but this can feel burdensome and irrelevant for some people living with asymptomatic infection and/or those who do not meet treatment criteria (Mofokeng, 2021, Adjei et al., 2019). Moreover, HBV receives only a fraction of global research funding allocated to major infectious diseases. For example, in 2022, projected US funding for HIV research is 20-fold greater than for HBV, despite the lower number of people living with HIV infection (National institutes of health, 2022). Therefore, HBV remains a major public health threat, with 1.5 million new infections each year and more annual deaths than malaria or HIV (O’Hara et al., 2017, Graber-Stiehl, 2018).

An advocate with lived experience of HBV infection described the HBV community as ‘the forgotten people’, a description that is also pertinent to inclusion health populations (Matthews et al., 2022a, Aldridge et al., 2018). These exclusions may lead to an increased risk of HBV infection, are amplified by HBV infection, and lead to greater morbidity and mortality as a result of inadequate access to care. In resource-limited settings, where the burden of HBV infection is greatest, the inequities are amplified.

We have collated evidence for the impact of HBV in some of these marginalised populations globally, assimilating data and identifying knowledge gaps in order to inform the HBV agenda in inclusion health. Addressing the complex intersection of social exclusion and HBV infection is essential to support progress towards global elimination goals.

Enhancing HBV within the Inclusion Health Agenda: The next steps

In this section, we consider how the current evidence informs policy and practical strategies to advance prevention, diagnosis, clinical care and treatment for people living with HBV infection in groups who have been under-served to date.

Close the data gap

There are clear SDG30 goals for HBV, but it is impossible to determine the nature and magnitude of the challenge, benchmark progress, or deploy appropriate interventions without accurate epidemiological data. European Centre for Disease Prevention and Control report major data gaps, now exacerbated by the Covid-19 pandemic, with the worst impact in high-burden (often low income) settings, hampering progress towards elimination (Pley et al., 2021). Good quality HBV data for inclusion health populations are lacking, mostly reporting from small, independent, cross sectional seroprevalence studies (summarised in Table 2). Unified, transparent data collection will require increased awareness, advocacy, funding and research, with coordination between organisations (e.g. World Health Organization, United States Centers for Disease Control and Prevention, European Centre for Disease Prevention and Control) to help standardise and strengthen approaches. Crucially, evidence is needed to underpin solution-based methods rather than simply describing problems (Luchenski et al., 2018; Siersbaek et al., 2021).

Active case finding

Active targeted screening efforts are an important step towards HBV elimination (European Centre for Disease Prevention and Control, 2021; Lemoine et al., 2015). Availability of point-of-care hepatitis B surface antigen tests enable community-based diagnosis, although global efforts are needed to prioritise regular supply in resource-constrained settings (Lemoine et al., 2015). For migrants, community-based testing strategies are effective, with highest uptake in programmes with endorsement from the local community (European Centre for Disease Prevention and Control, 2018; Robotin and George, 2014). Outreach screening is equally important in other inclusion health populations, for example, PEH and PWID (Box 1). Such outreach screening services have been shown to be feasible and acceptable (O’Carroll et al., 2017, Carr et al., 2014), and can also be incorporated into other services (e.g. drug harm reduction programmes).

Box 1

Case studies of inclusion health interventions.

1. RESPOND (Farrant et al., 2022): RESPOND is a team from University College London Hospitals in the London borough of Camden, providing rapid access community based integrated screening and care planning for asylum seekers. It was formed to accommodate the needs of the rising number of people seeking asylum in temporary accommodation at the beginning of the Covid-19 pandemic. The aim is to provide a multi-disciplinary, comprehensive assessment and formulate an integrated migrant health plan, an electronic document that outlines the key issues for each family member. This document remains with the family, and is copied to the primary healthcare provider, thus removing the need for repeated assessments after each short notice relocation.

2. Find & Treat (University College London Hospitals NHS Foundation Trust, 2013): University College London Hospitals Find & Treat are a specialist outreach team working alongside over 200 NHS and third sector front-line services to tackle TB and blood borne viruses among PEH, PWID, migrants in vulnerable situations or people who have been in prison. The team is multidisciplinary, consisting of people with lived experience working as peer advocates, nurse specialists, social and outreach workers, radiographers, and doctors with primary/secondary care expertise. They use state of the art point of care diagnostics within outreach vans to help overcome barriers in access to care among socially excluded populations.

3. ‘Gypsy & Traveller Exchange’ (Leeds gate, 2022): An example of a successful programme of raising awareness is this programme, led by community members and working in partnership with local services, supported by funding from charitable organisations and local government. Their strategy is to identify community members (or ‘gatekeepers’) who are trusted to facilitate communication with healthcare services, lead cultural awareness training for healthcare workers and provide community outreach and dedicated services for Roma and Traveller populations (McFadden et al., 2018; Condon et al., 2019; Carr et al., 2014). Similar approaches could be successful in other populations to provide education and support.

4. ‘One Stop Liver Shop’ (Hla et al., 2020): The Aboriginal population in the Northern Territory has the highest prevalence of HBV in Australia (6.08% compared to the Non-Indigenous population 1.56%). The ‘One Stop Liver Shop’ was developed iteratively with a very remote Aboriginal community (>500 km from the nearest tertiary hospital in Darwin). It is made up of a specialist doctor, community based Aboriginal Health Practitioner, a sonographer and clinical nurse specialist. They use a portable ultrasound scan, a FibroSan for transient elastography and a mobile device to use the ‘Hep B Story App’, a mobile application using the relevant local language. Visits occur 4 times per year. Due to this initiative, 88% of those aware of their diagnosis were engaged in care and 16% were on treatment.

All pregnant women should be screened for HBV, and healthcare professionals should consider opportunistically offering HBV screening in high-risk groups accessing services (World Health Organization, 2020; Centers for Disease Control and Prevention, 2022). There should also be a move to integrate routine hepatitis screening into high-risk healthcare settings, for example TB, sexual health and HIV services. The European Centre for Disease Prevention and Control (ECDC) recommends universal screening in emergency departments in areas where HBV prevalence exceeds 2%, however, evidence suggests that universal emergency department screening is cost effective even at lower prevalence (>0.25%) and therefore the United Kingdom is currently implementing this policy (Williams et al., 2020b, Nebbia et al., 2022).

Multiple studies have demonstrated cost-effectiveness of HBV screening in a variety of different scenarios, including community-based outreach and low prevalence settings (Su et al., 2022, Xiao et al., 2020, Toy et al., 2022, Nayagam et al., 2016, Tordrup et al., 2020, Hutton et al., 2022, Wright et al., 2018). This is largely due to averting high costs associated with decompensated cirrhosis, HCC and liver transplantation.

Rethinking prevention strategies

A safe, effective vaccine against HBV has been available since 1982, and remains a key tool for the elimination of viral hepatitis (World Health Organization, 2017). The WHO has recommended a universal birth dose HBV vaccination since 2009, irrespective of the mother’s serological status, but coverage was still only 42% globally and 17% in the WHO African Region by 2021 (World Health Organization, 2022a). Modelling suggests that scaling up of a timely birth dose vaccine to >90% by 2030 would result in immediate reduction of chronic HBV incidence, and 710,000 fewer deaths in those born between 2020–2030, globally (de Villiers et al., 2021). This strategy would be a particularly important public health intervention for future inclusion health populations, in whom catch-up three-dose adult vaccination is challenging and may not be cost-effective.

While catch-up adult vaccination is not advocated at a general population level, opportunities for providing vaccination to high-risk adults must still be explored and developed, optimising approaches to deliver a three-dose schedule alongside education, proactive antenatal and sexual healthcare, and other health interventions (Box 2).

Box 2

Example methods of increasing HBV vaccination coverage among high-risk groups

1. Universal HBV vaccination in prisons in Scotland (Palmateer et al., 2018).

   • Following prison-related outbreaks of acute HBV among PWID, HBV vaccination for all prisoners was introduced in 1999.

   • Among recent-onset PWID in Glasgow, vaccine uptake increased from 16% in 1993 to 59% in 2009–2014 (p<0.001).

   • HBsAg prevalence 0.3% among people who commenced injecting drugs in the decade since universal vaccination induced, compared to 9% globally.

   • Vaccination is associated with 40% reduced odds of ever having HBV (aOR = 0.6, 95% CI 0.37–0.97).

2. HBV-COMSAVA (Community Screening and Vaccination in Africans) Study, Barcelona, Spain (Picchio et al., 2021).

   • Pop-up clinics at west African migrant faith-based and community organisations.

   • Individuals offered a rapid HBsAg diagnostic test and a dried blood sample for analysing HBV viral load and co-infection with hepatitis D virus.

   • If HBsAg +, same day referral to specialist with expedited referral process which did not require prior appointment.

   • If susceptible, offered HBV vaccine in situ at return appointment (‘return-date slip’ reminder given at first appointment).

   • 70% were susceptible to HBV, 74% returned to receive results and 86% of those who returned accepted vaccination.

3. Sex-worker outreach, Ghent, Belgium (Mak et al., 2003)

   • A medical doctor and social nurse visited the workplaces of sex-workers, discussed professional risks, handed out prevention materials and offered free STI screening (Chlamydia, gonorrhoea, syphilis, HIV), a cervical smear and free HBV vaccination.

   • Psychological and legal programs related to sex work could also be discussed and anonymity guaranteed.

   • Over two-thirds of susceptible sex-workers completed an accelerated HBV vaccination schedule (over 2 months), compared to less than half if given over 6 months.

   • Only 7% were vaccinated in existing services.

Given the slow and heterogenous uptake of birth dose vaccination, and challenges associated with catch-up vaccination of inclusion health populations, other prevention strategies need urgent consideration. For example, the ‘Test and Treat’ strategy which aims to suppress the reservoir of virus in the population (McNaughton et al., 2019). According to current guidelines, only 25–35% of adults with CHB are eligible for treatment, leaving the majority at risk of both longer term complications (relevant to the individual) and the potential for transmission (relevant to populations) (McNaughton et al., 2021). HBV/HIV co-infected individuals may have a treatment advantage, reflecting the benefits of greater access to early and consistent antiviral treatment compared to mono-infected individuals (Maponga et al., 2020). Potential risks should be considered: toxicity and side effects, requirement for monitoring, potential for drug resistance, limited gains from treating well people and the cost of drug and potential diversion of healthcare resources (McNaughton et al., 2021). Further research is required to assess the efficacy, feasibility and acceptability of wider treatment roll out.

Designing inclusive HBV healthcare

Once diagnosed, HBV requires long-term surveillance. However, current models of healthcare fail to provide adequate continuity for inclusion health populations, and innovative solutions are needed. Interventions to reduce the burden of vaccine-preventable infections among migrants can be classified based on the individual, community, provider and system (Charania et al., 2020). This framework can be applied to all inclusion health populations (Box 2, Figure 2).

Figure 2

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Developing holistic approaches

Inclusion health populations face many challenges; therefore, the HBV agenda must not operate in a silo. Integrated infectious disease screening can be cost-effective and an efficient use of resources. An example is the World Health Organization’s ‘triple elimination initiative’ which encourages countries to simultaneously commit to elimination of mother-to-child transmission of HIV, syphilis and HBV (World Health Organization, 2022b). This approach has been demonstrated to reduce disease transmission rates, staff and patient time, and overall programme cost (Zhang et al., 2019).

Integrated infection screening is also recommended in migrants, and in most countries screening tests are offered following a risk assessment (European Centre for Disease Prevention and Control, 2018). Screening is found to be cost-effective, feasible and acceptable, but migrants are a heterogenous group, and services should be culturally appropriate, and accommodate the possibility of fear and stigma surrounding screening and diagnosis (Seedat et al., 2018; Cinardo et al., 2022). In many countries, migrants will undergo pre-entry or port-of-entry screening, missing those who arrive through informal routes (Cinardo et al., 2022). Culturally sensitive outreach services are an important way to reach and screen inclusion health populations (Box 1).

Multi-morbidity is common, for example, incarcerated individuals with HBV have high rates of HIV, HCV and /or TB co-infection (Ahmadi Gharaei et al., 2021; do Nascimento et al., 2020; La Torre et al., 2007), and of substance use and severe mental illness (Kamarulzaman et al., 2016; Fazel and Danesh, 2002). Non-communicable diseases are also prevalent among inclusion health populations (Tweed et al., 2021) for example, PEH have a three-fold elevated risk of cardiovascular disease and cardiovascular mortality compared to non-homeless individuals (Table 2; Al Shakarchi et al., 2020). Moreover, people with co-existing exposures, for example incarceration and substance use, or serious mental illness and substance use, have worse outcomes (Tweed et al., 2021). Diabetes is associated with an increased risk of HBV-associated HCC (hazard ratio 1.36, 95% CI 1.23–1.49)(Campbell et al., 2021). The HBV inclusion health agenda must therefore take a ‘syndemic’ approach, namely to tackle viral hepatitis not as an isolated challenge but recognising its place amongst complex social, physical and mental health challenges and addressing the person as a whole (Mendenhall, 2017; Matthews et al., 2022b).

Prioritising patient and public involvement

HBV infection can result in stigma and discrimination, which is magnified when combined with the experiences of socially excluded groups (Matthews et al., 2022a). Sharing lived experiences builds rapport, trust and equality, helping promote advocacy, build peer support networks, navigate healthcare systems and promote diagnosis and treatment of blood borne infections (Paisi et al., 2022; Crone et al., 2022). There is a long history of peer-led approaches with successful outcomes in HIV, TB and HCV (Story et al., 2020; Øgård-Repål et al., 2023). For example, as part of the HepCare project, people with lived experience of HCV infection were upskilled to become equal members of the healthcare team, providing a cost-effective approach to enhancing diagnosis, linkage to care and treatment success (Ward et al., 2019; Surey et al., 2021; Surey et al., 2019). Importantly, a focus group involving people with lived experience ranked advocacy via peer-led services as the second most important intervention behind stable housing (Luchenski et al., 2018). The success and knowledge gained from this peer-led approach must now be translated to HBV.

Improving awareness, education, and advocacy

Qualitative research from Australia has identified lack of confidence of healthcare professionals and poor communication surrounding HBV (Wallace et al., 2011; Robotin et al., 2021). Sensitive communication around HBV is of heightened importance in populations who already experience discrimination and stigma, and is a particular consideration where certain subjects are culturally taboo (Condon et al., 2019). Engagement requires sensitivity to cultural nuances, including traditional and religious beliefs (Holmstrom, 2019, Carr et al., 2014). Training for healthcare professionals in trauma-informed care would benefit many inclusion health populations who are more likely to have a history of experiencing assault and torture (Emily, 2021). Lack of awareness is present in healthcare professionals as well as in at-risk populations (Cochrane et al., 2016; Bierhoff et al., 2021). A UK survey of primary care practitioners found many did not believe routine testing of HBV in migrants was necessary, and national guidelines were poorly followed (Evlampidou et al., 2016). Interventions to raise HBV awareness in different groups are paramount to inform action for inclusion health populations.

Representative research

Inclusion health populations are often seen as ‘hard to reach’ and may not be viewed as ideal research participants given the possibility of increased loss to follow up and co-morbid conditions. This is further exacerbated in low-resource settings, where there is higher HBV prevalence. There is a striking lack of inclusion health research within Africa, even among global reviews (Table 2). In order to be generalisable and equitable, HBV research needs to be representative of real-world populations and challenges, on a global scale. Performance of new biomarkers, for example hepatitis B core-related antigen, or clinical fibrosis scores, such as APRI and FIB-4, needs to be validated for clinical utility in these populations with overlapping risk factors, multi-morbidity and in varying global populations. While limited treatments currently exist for HBV infection, there is active research into improved treatment and curative therapies; for these to be relevant in populations most affected by HBV, clinical trials must recruit accordingly. Mixed-method approaches should be utilised to understand views and unmet needs of marginalised communities in relation to HBV. The exclusion of inclusion health populations from the current research agenda is likely to further exacerbate inequities when more effective treatments do become available.

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Author details

1. Emily Martyn

   1. The Francis Crick Institute, London, United Kingdom
   2. London School of Hygiene & Tropical Medicine, London, United Kingdom
   3. Hospital for Tropical Diseases, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom

   Contribution

   Conceptualization, Writing – original draft

   Competing interests

   No competing interests declared

2. Sarah Eisen

   Hospital for Tropical Diseases, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom

   Contribution

   Conceptualization, Writing – review and editing

   Competing interests

   No competing interests declared

3. Nicky Longley

   1. London School of Hygiene & Tropical Medicine, London, United Kingdom
   2. Hospital for Tropical Diseases, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom
   3. Department of Infectious Diseases, University College London Hospitals NHS Foundation Trust, London, United Kingdom

   Contribution

   Conceptualization, Writing – review and editing

   Competing interests

   No competing interests declared

4. Philippa Harris

   Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom

   Contribution

   Conceptualization, Writing – review and editing

   Competing interests

   No competing interests declared

5. Julian Surey

   1. Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom
   2. Institute of Global Health, University College London, London, United Kingdom
   3. Universidad Autonoma de Madrid, Ciudad Universitaria de Cantoblanco, Madrid, Spain

   Contribution

   Conceptualization, Writing – review and editing

   Competing interests

   No competing interests declared

6. James Norman

   Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

7. Michael Brown

   1. London School of Hygiene & Tropical Medicine, London, United Kingdom
   2. Department of Infectious Diseases, University College London Hospitals NHS Foundation Trust, London, United Kingdom
   3. Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom

   Contribution

   Writing – review and editing

   Competing interests

   MB has led local research studies funded by Gilead (an HIV testing study in 2009 or so, and COVID trials 2020-22) and has provided (unfunded) consultancy to Gilead wrt COVID therapeutics

8. Binta Sultan

   1. Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom
   2. Mortimer Market Centre, Central and North London NHS Foundation Trust, London, United Kingdom

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

9. Tongai G Maponga

   Stellenbosch University, Faculty of Medicine and Health Sciences, Tygerberg, South Africa

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

10. Collins Iwuji

    1. Department of Global Health, Brighton and Sussex Medical School, University of Sussex, Brighton, United Kingdom
    2. Africa Health Research Institute, Durban, KwaZulu-Natal, South Africa

    Contribution

    Writing – review and editing

    Competing interests

    CI has received support for conference attendance and research grant paid to his institution from Gilead Sciences Ltd

11. Stuart Flanagan

    Mortimer Market Centre, Central and North London NHS Foundation Trust, London, United Kingdom

    Contribution

    Supervision, Writing – review and editing

    Competing interests

    SF has received travel and conference bursaries from AbbVie, Gilead, Bristol-Myers-Squibb, IMS Health

12. Indrajit Ghosh

    1. Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom
    2. Mortimer Market Centre, Central and North London NHS Foundation Trust, London, United Kingdom

    Contribution

    Conceptualization, Writing – review and editing

    Competing interests

    No competing interests declared

13. Alistair Story

    1. Find & Treat Service, Division of Infection, University College London Hospitals NHS Foundation Trust, London, United Kingdom
    2. Collaborative Centre for Inclusion Health, University College London, London, United Kingdom

    Contribution

    Conceptualization, Supervision, Writing – review and editing

    Contributed equally with

    Philippa C Matthews

    Competing interests

    No competing interests declared

14. Philippa C Matthews

    1. The Francis Crick Institute, London, United Kingdom
    2. Department of Infectious Diseases, University College London Hospitals NHS Foundation Trust, London, United Kingdom
    3. Mortimer Market Centre, Central and North London NHS Foundation Trust, London, United Kingdom
    4. Division of Infection and Immunity, University College London, London, United Kingdom

    Contribution

    Conceptualization, Supervision, Funding acquisition, Visualization, Writing – original draft, Project administration

    Contributed equally with

    Alistair Story

    For correspondence

    philippa.matthews@crick.ac.uk

    Competing interests

    PCM holds a Wellcome Fellowship and NIHR funding, and receives funding to her research team from GSK

    "This ORCID iD identifies the author of this article:" 0000-0002-4036-4269

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