Fitting Health Care to People: Understanding and Adapting to the Epidemiology and Health Literacy of People Affected by Viral Hepatitis from Culturally and Linguistically Diverse Migrant Backgrounds

This study explored the epidemiology and health literacy of people affected by viral hepatitis (VH) from migrant culturally and linguistically diverse (CALD) backgrounds attending a community-based general practitioner and specialty hepatology shared-care (HEPREACH) clinic in Brisbane, Australia. Patient-reported data on health literacy and clinical information from adult patients (n = 66) of CALD background recruited from the liver clinic were analyzed. Health literacy was assessed using a 5-question, 12-point scale. Variance weighted multiple linear regression was used to identify factors associated with knowledge about VH. About three-quarters of patients (74.2%) were diagnosed with hepatitis B. The median knowledge score was 7.8 (interquartile range [IQR] 6‒9). One in five patients did not understand the infective nature of VH, 30.3% did not understand mother-to-child transmission risk, and 30–40% of patients thought activities such as kissing, sharing food or mosquito bites could spread VH. Only 6% of patients understood the risk of liver cancer and the need for regular screening. Higher educational level (secondary, β = 4.8, p < 0.0001 or tertiary, β = 8.1, p < 0.0001 vs. primary) was associated with better knowledge, and transition through a refugee camp (vs. not, β = − 1.2, p = 0.028) and country of diagnosis (overseas vs. Australia, β = − 1.9, p = 0.016) were associated with poorer knowledge. Country of origin, refugee status and opportunities for tertiary education impact patients’ understanding of VH. Ensuring delivery of culturally appropriate care and education is critical to improve knowledge, reduce misconceptions to improve care and outcomes for VH in CALD migrant communities.


Introduction
In Australia, hepatitis B virus (HBV) and hepatitis C burden is borne mostly from immigrants born in intermediate and high HBV prevalence countries [1,2] such as in Asia (57%) and Africa (35%) [3]. The highest prevalence rates of HBV are observed in migrants born in Cambodia (8.6%), Taiwan (8.1%), Vietnam (7.5%), China (6.8%), and Tonga (6.5%) [4]. Immigrants from high HCV prevalence countries have a higher prevalence rate of hepatitis C virus (HCV) infection compared with persons born in Australia, reflecting the contribution of the country of origin [5][6][7].
Health literacy is the ability of persons to obtain, understand, and use health information in a way that benefits their health [8]. The health literacy framework includes two major conceptual models: the multidimensional nature of health literacy and the presence of individual and health system level factors that interact and determine the level of health literacy [9]. Health literacy is thus defined and understood beyond the individual ability, and includes the interaction between individual skills required to obtaining and using health information and the social factors that determine how individuals understand and use this information [10]. Individual attributes including age, gender, ethnicity are enablers to health literacy [11]. Social systems including community members, healthcare providers, culture, and people who provide health education interact with individual factors and determine the extent to which people develop health behavior [9,11].
Health literacy has several dimensions including the accessibility of information, obtaining information, understanding health information and the utilization of health information to engage in and use health services [12,13]. Health literacy frameworks depict the relationship between the dimensions of health literacy and health outcomes in the context of individual and external factors. Individual level factors (age, gender, education) and factors external to the individual (family situation, cultural influence, societal interaction, availability and use of media) determine how individuals obtain, understand and utilize health information for health decision making to bring better health outcomes [14]. Understanding health information is significantly associated with individuals age, being immigrant, living alone, lower educational level and poor socio-economic status measured as low income [15][16][17]. Factors associated with engagement with healthcare providers include age, being of immigrant origin, low educational level, and low income [15,17,18]. Self-efficacy, which is defined as one's judgement of the ability to perform an action, is a critical factor to the realization of understanding health information into an individual's health decision making, including their engagement in healthcare [19]. Self-efficacy is, therefore, a mediator between knowledge about health and the realization of a person's knowledge in to health behavior [11]. Perceived risk of disease is an important determinant of health literacy [17]. A study by Enjezab et al. found participants' perceived risk of disease was significantly associated with the accessibility dimension of health literacy [20].
Immigrants have low health literacy about viral hepatitis (VH) including key aspects of prevention and transmission methods [21][22][23]. Health literacy of people from culturally and linguistically diverse (CALD) backgrounds may be influenced by language barriers, access to health information including digital media, and their healthcare uptakes [23,24]. Immigrants often face challenges of cultural integration and may have a lack of understanding the health system. Low rate of utilization of healthcare system due to poor integration may influence their health literacy [17]. Health information is mostly received from healthcare workers and migrants may miss such an opportunity to access health information, which determines their health literacy [25]. Many countries may not have CALD migrantspecific resources for health information and contributes to the low health literacy in this population group [26].
Health literacy is a key determinant of healthcare utilization and health outcomes [27]. Health literacy has a substantial impact on health inequalities in immigrant populations [10]. Low level of health literacy in CALD migrants is often associated with difficulties in access and processing health information, which may lead to poorer engagement in healthcare systems and poorer utilization of services [18]. There is a strong relationship between health literacy and utilization of healthcare, which is also determined by cultural differences in immigrants [21]. Australia has a universal health care system that allows for subsidized HBV assessment and treatment, though barriers still exist for migrant CALD peoples.
The World Health Organization has identified VH elimination targets, which include a 65% reduction in hepatitisrelated mortality and a 90% reduction in new infections by 2030 [28][29][30]. Without a firm understanding of how VH impacts and is understood by people from CALD backgrounds-including risks of transmission and need for follow-up, successful control of VH will be unattainable. Ensuring health systems meet patients' needs rather than patients "fitted" into the health system, is critical to engaging these vulnerable migrant CALD people. The success of such an effort depends partly on patients' knowledge of VH and their healthcare uptake.
Few studies describe the knowledge of VH in persons with chronic HBV, particularly health literacy about VH in people from CALD backgrounds. We reported the epidemiology of HBV and HCV in migrant communities in Australia and determined their knowledge of VH.

Study Design and Setting
The Hepatology Research Education and Clinical Outreach (HEPREACH) study is a prospective cohort study of patients of CALD backgrounds diagnosed with VH. The study took place in two clinics in Brisbane, Beaudesert Road Surgery and Inala Primary Care, where migrant communities with a high prevalence of HBV and HCV live. HEPREACH is an innovative model of care for liver disease that reorients the tertiary specialist hepatology services into the community and offers an opportunity for CALD communities to overcome barriers to access to tertiary hospital-based care, integrating general practitioner and specialty nurses into the teams caring for patients [31]. This baseline survey is conducted on the first HEPREACH clinic appointment of patients. Patients were recruited during January 2018 and February 2020.

Study Participants
The study included adults of CALD backgrounds including refugees ≥ 18 years) with a diagnosis of HBV, HCV or both. Patients were identified through a General Practitioner (GP) clinic audit. We excluded patients with decompensated liver cirrhosis and those either assessed for or undergone liver transplantation. Eligible patients were offered appointments to the HEPREACH clinics within the GP practice and written informed consent was obtained. The clinical care of patients at the HEPREACH clinic continued irrespective of participation in the study.

Data Collection
Eligible patients attended a liver clinic where they were seen by a multidisciplinary team including a hepatologist (liver specialist), a specialist hepatitis nurse and a GP with a special interest in VH. Trained research assistants with extensive experience in interviewing CALD communities were employed by the HEPREACH project and conducted the face-to-face interviews with patients after patients completed a HEPREACH clinic visit. Prior to conducting the interview, each participant is asked for the language of their preference. Interpreters were used for interviews with patients who preferred to be interviewed in other languages than English. Information on the date of birth, gender, country of birth, and ethnicity was collected using a structured questionnaire on the date of the first HEPREACH clinic visit. VH literacy data were gathered using a questionnaire using a 5-question 12-point scale.
HBV status was determined by HBV virology test including HBsAg, HBcAg, HBsAb, HBeAg, HBeAb, and HBV viral load. HCV status, genotypes, subtypes, and viral load were determined using the HCV genotype test.

Statistical Analyses
Data were entered into the Research Electronic Data Capture (REDCap) database at the Mater Research Institute and exported to Stata version 15.1 for coding and analysis (Stata Corporation, College Station, Texas, USA). Descriptive statistics were used to present patient demographics, clinical profile and genotypic epidemiology of HBV and HCV.
Patient knowledge regarding VH was computed from 5 knowledge questions adapted from a similar study in Australia by Dahl and colleagues [23], which included understanding and utilization of health information. The knowledge scores range from 0 to 12 points with higher scores indicating better knowledge. The instrument and scoring system are shown in Supplementary Table 1.
Adapted from Dahl et al. [23], we gave one point if a patient answered either of HCV, HBV or cirrhosis for a question asking why the patient comes to the clinic, and one point each for mentioning the liver and cirrhosis, liver damage or hepatocellular carcinoma (HCC) on answering how the liver affects the body. For the prompted modes of transmission, we gave 0.5 points for each of the risk factors if the participant answered yes and another 0.5 points if the patient answered no to the misconceptions. Regarding the reasons for being monitored or treated 1 point was assigned for mentioning low viral load and another one point for mentioning the absence or presence of liver damage. Two points were assigned if a participant mentioned reducing alcohol or eating a healthy diet to improve hepatitis or liver disease. Multivariable linear regression reported in terms of coefficients with associated 95% confidence intervals (CIs) was used to identify factors associated with patient literacy about VH. The variance-weighted least squares method was used as it gives a more precise estimate when the sample is small, and the independent variables are categorical.

Characteristics of the HEPREACH Cohort
The baseline characteristics of the cohort are presented in Table 1. The cohort was predominantly female, (41.5% male and 58.5% females), and the median age was 40.2 years (IQR 32.9-47.6). Most of the cohort (83.3%) members were born overseas such as in Vietnam, Taiwan, China, and African countries. Educational status was very variable, − 14% of respondents had only primary education, while nearly half (47.6%) had tertiary qualifications. Many of the patients had arrived as refugees, with twenty-four (40.0%) patients transiting through a refugee camp, spending a median of 5 years in refugee camps. For more than three-quarters (77.8%) of patients, English was the preferred language.

Epidemiology of Hepatitis B Virus Infection
Forty-nine (74.2%) patients had HBV infection and most of them reported longstanding infection. Vertical transmission (39.1%) was the most prevalent mode of acquisition (18 patients, 39%). Most patients were in the immune control phase (57%) or had resolved infection (13%). Of the 49 patients reviewed, 9 (18.4%) were on treatment ( Table 2).

Epidemiology of Hepatitis C Virus Infection
Eighteen (27.3%) patients were diagnosed with HCV infection. The commonest HCV genotype was genotype 3 (63.6%) and the most prevalent HCV subtype was 3a (62.5%). All patients with G4 HCV infection were born outside of Australia (Fig. 1). Patients had a median of 11 years (IQR 6.5-24.5) of HCV infection. Over half of patients (55%) with HCV infection acquired this through injection drug use (IDU). The majority of persons diagnosed with HCV infection were not treated, and two patients were on treatment ( Table 2).

Prevalence of Liver Fibrosis and Cirrhosis
Six (12.5%) patients had a fibrosis score consistent with advanced liver fibrosis (TE 10-14 kPa and another 6 had cirrhosis based on elastography (TE > 14 kPa) fibrosis score.  Table 2).

Health Literacy About Viral Hepatitis
The overall median score for VH knowledge of patients was 7.8 (IQR 6-9) on a 12-point scale. Two patients had a maximum score of 11.5 points and the other two had a score of 2 points (Fig. 2). One-fifth of patients (21.2%) were unsure of what HBV or HCV was and did not understand the concept of it as an infective agent. Forty percent understood the concept of the virus, and over half perceived it as an external infectious-like entity affecting the liver. Seven (10.8%) patients interviewed thought VH is not transmittable to other persons. Despite most patients having acquired hepatitis vertically, even after prompting, 30% did not recognize perinatal transmission as a risk factor. Most patients were aware of risk factors for the transmission of HBV or HCV such as sexual contact (77.3%), contact with infected blood (86.4%), unclean needles (84.9%), and blood transfusion (83.3%). Many patients felt VH infections could be transmitted by sharing food (21.2.0%), kissing (31.8%), breathing (9.1%), and mosquitoes (37.9%). Importantly, only 6% were aware of the purpose of regular liver cancer surveillance (Table 3).   Table 4 presents the factors associated with VH knowledge score. The higher level of educational attainment was associated with better literacy on hepatitis; compared to patients with primary school, for those with secondary education level the knowledge score was increased by 4.8 (p < 0.0001) and for tertiary education level the score increased by 8.1 (p < 0.0001). Forty percent of patients had been in a refugee camp, and this was significantly associated with lower knowledge scores than those who had not (β = − 1.2, p = 0.028). A diagnosis of VH made outside of Australia had a lower knowledge score by nearly 2 points (β = − 1.9, p = 0.016).

Discussion
Most patients in the HEPREACH cohort were overseasborn, and two-fifths of patients transitioned through a refugee camp. Patients held many misconceptions related to VH transmission including sharing food, kissing, breathing and mosquitoes as potential transmission risk factors, but many did not realize the risks of transmission from identified risks. Country of hepatitis diagnosis, patient educational level, preferred language of communication, and having stayed in a refugee camp were associated with knowledge of VH. While three-fourths of patients were diagnosed with HBV, less than one-in-five were on treatment. Similarly, only 3 of the 18 persons diagnosed with HCV were treated. All patients with G4 HCV genotype were born outside Australia. Low rate of treatment might be influenced by the inability to utilize health information to improve healthcare seeking behavior because of the low level of health literacy in the study participants [21,27]. Additionally, low treatment rates for both HCV and HBV represent a major deficiency of the health system's ability to serve this community. The low HCV treatment rate in this population may reflect access to care, which could also be influenced by socio-economic, cultural and linguistic factors. A high treatment coverage and success rate in CALD populations is essential to reach HCV elimination targets, given the significant burden of HCV in people from CALD backgrounds [32].
The ethnic diversity and casemix of HBV and HCV is representative of Australia's VH epidemiology, which is strongly influenced by immigration from high-to intermediate-prevalence countries [4,33]. Most migrant patients living with HBV or HCV were born in Vietnam, Liberia, Taiwan, and other countries in the Pacific and African regions, which were known to have a high prevalence of HBV [7]. The longer duration since HBV infection could be due to transitioning through the refugee camp, or other barriers to healthcare such as culture and language. Low levels of understanding of the risks of HCC and the need for regular screening may underlie the higher prevalence of HCC in migrant Australians with HBV, which can occur without progression to cirrhosis (Taye et al. 2019, unpublished). The country of birth for patients with HCV G4 being outside of Australia (one case each from DR Congo and Sudan) is in line with studies that reported the genotypic distribution of HCV is markedly contributed to by immigration [5,34]. The finding suggests the need for consideration of varying genotypes to achieve a high rate of treatment success [5,35].
This study is one of the few that investigated the health literacy of CALD communities about VH. We found the health literacy of migrant people with VH was limited by their educational level, having a history of being a refugee and with non-English speaking language preference. Patients whose diagnosis had been provided before their migrationeither in their country of origin or a transit camp, had a significantly poorer understanding of VH. This may reflect more limited health care resources and expertise in their country of diagnosis, which itself may have been a transit country for the 40% of patients who were refugees.
Our study participants had a low median knowledge score and only two-thirds of patients were able to describe that VH affects the liver. Without knowledge of the implications of VH, particularly hepatocellular carcinoma (HCC) in people of CALD backgrounds is limited and could have an impact on the screening for HCC and HBV treatment uptake [36]. Laboratory and radiologic evidence of cirrhosis and liver damage in these patients were common, indicating the need for early diagnosis and monitoring.
Although most patients acquired HBV vertically, a third of patients did not recognize perinatal transmission as a risk factor. This wide gap in knowledge of vertical transmission has a significant contribution to mother to child transmission of HBV to children born in Australia, making HBV median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score median score  a major health problem in people of CALD background. Expanding knowledge of VH is, therefore, a key element of the approaches to prevent transmission and accelerate elimination [32].
Many patients had misconceptions about the transmission of VH (e.g. Sharing food, kissing, breathing, and mosquito bites). The higher rate of misconceptions held by CALD populations reflects the presence of a wider knowledge gap that must be addressed during follow up visits to prevent the transmission of VH to other family members [23,37,38]. The high proportion of misconceptions in VH patients could contribute to poor diagnosis and treatment uptake rates and may increase patient lost-to-follow-up.
Societal perspectives about VH are variable depending on the education from healthcare providers [39]. Social networks determine the dynamics of transmission for VH and the related perceptions of having VH infections are related to differential treatment-seeking and health outcomes [40]. The disconnection between patient perspectives and experience and assumptions of healthcare providers has implications on the engagement of people living with VH [41]. The social attribution to having hepatitis among the community themselves is crucial to design the type and level of medical and psychosocial support for patients [39].
The knowledge of VH was associated with educational level, staying in a refugee camp and the country of diagnosis. Higher educational level contributes substantially to the ability of CALD migrants to retrieve health information including information from different languages, which is a key pillar in improving health literacy [25]. Better access to information about VH and delivering patient education contributes to the positive behavior that prepares patients to contribute towards the prevention of hepatitis through vaccination, preventing vertical transmission or unsafe injections [42]. In the refugee camps, migrants may not have access to health information and were more likely to have lower health literacy scores. Health information resources at refugee camps are not refugee-specific or may not be available [26]. This implies the importance of VH education and provision of access to health information in refugee camps to prevent infection in migrants and transmission to other communities at the destination country. Migrant people are at-risk group, targeted strategies need to include focused patient education about VH transmission and misconceptions such as multilanguage-focused health information using mobile applications [43].
While this is the largest study that assessed patient literacy to VH in people from CALD backgrounds in Australia, the generalizability of our findings could be limited by the small sample size and the fact that the study population was recruited from two clinics located in areas overpopulated with migrants. The study assessed health literacy in the context of Australia and different ways of understanding and terminologies that might have existed in the countries of birth were not included in the assessment. The duration of stay in Australia before VH diagnosis could not be established because of the variable country of diagnosis for participants. Due to the scope of the data, other dimensions of health literacy such as self-efficacy were not reported in this study. Despite what appear to be significant weaknesses in health literacy and poor treatment rates, it is likely that selection bias from this group of engaged patients understates the situation for many migrant people with VH in the community. Nevertheless, this study identified a clear health literacy gap particularly in the areas of transmission and natural history, which can be used to design CALD-focused patient education strategies to reduce the number of new cases, increase treatment uptake, and reduce stigma and discrimination, pivotal to achieving the VH elimination targets.

Conclusions
A significant health literacy gap exists for migrant CALD people affected by VH. Low rates of VH treatment and relatively high rates of cirrhosis and liver fibrosis were also observed. Such disparities can only be addressed by being targeted and tailored to the needs of migrant people, a group at high risk of VH and vulnerable to poorer health outcomes. In order to meet the needs of these patients and public health elimination objectives, it is critical that health systems adapt to the needs of the people they care for, rather than anticipating equivalent outcomes by forcing CALD migrant patients with VH into a health system that is not designed to fit this purpose. This can be achieved through implementation of culturally appropriate care, multilanguage-focused health information such as by using mobile application, engaging ethnic community organizations in mobilization, and capacity building in the primary care including focused GP training to better manage VH.