A Patient-Centered Hepatitis B Virus (HBV) Educational Intervention Improves HBV Care Among Underserved Safety-Net Populations

Abstract

Goals:

To evaluate the impact of a prospective patient-centered hepatitis B virus (HBV) educational intervention on improving HBV care.

Background:

Improving patients’ HBV knowledge has the potential to improve adherence to HBV monitoring and management, particularly among underserved safety-net populations.

Methods:

Consecutive chronic HBV adults at a single-center safety-net liver clinic were recruited from July 2017 to July 2018 to evaluate the impact of an in-person, language concordant formal HBV educational intervention on improvements in HBV knowledge and HBV management: appropriate HBV clinic follow-up (≥ 1 visit/year), HBV laboratory monitoring (≥ 1 HBV viral load and alanine aminotransferase test/year), hepatocellular carcinoma surveillance (≥ 1 liver imaging test/year among eligible patients), and HBV treatment among treatment eligible patients. HBV knowledge and management were assessed before and after the intervention and compared with age-matched and sex-matched HBV controls who did not receive an education.

Results:

Among 102 patients with chronic HBV (54.9% men; mean age, 52.0±13.8), HBV education improved HBV knowledge scores by 25% (P<0.001), HBV clinic follow-up from 25.5% to 81.4% (P<0.001), HBV laboratory monitoring from 62.8% to 77.5% (P=0.02), and appropriate HBV treatment from 71.5% to 98.5% (P<0.001). Compared with 102 HBV controls, receiving HBV education was associated with higher rates of HBV clinic follow-up (81.4% vs. 39.2%; odds ratio, 7.02; 95% confidence interval, 3.64–13.56; P<0.001) and appropriate HBV laboratory monitoring (77.5% vs. 42.2%; odds ratio, 4.94, 95% confidence interval, 2.64–9.24; P<0.001).

Conclusion:

A formal, in-person, language concordant educational intervention leads to significant improvements in HBV knowledge, resulting in improved HBV monitoring and appropriate HBV treatment.

Chronic hepatitis B virus infection (HBV) is a leading cause of morbidity and mortality with over 290 million chronically infected worldwide and nearly 2 million chronically infected in the United States.^1,2 Patients with chronic HBV have significant lifetime risks of developing liver-related complications, with up to 40% developing acute HBV exacerbation, cirrhosis, or hepatocellular carcinoma (HCC).^3,4 Early identification of chronic HBV allows for appropriate initiation of therapy to reduce disease progression, reduce the risk of HCC, and improve survival.⁵ Despite established guidelines for the management of chronic HBV, liver disease monitoring, initiation of therapies, and adherence to best practices in HBV care remain suboptimal in various health care settings including safety-net systems.^6–14 For example, a recent study evaluating HBV and HCC screening practices among Asian populations in San Francisco’s safety-net health care system demonstrated only 76% of providers screened >50% of their Asian patients for HBV and 79% of providers screened for HCC among their Asian patients with HBV.¹⁵ Another survey study of primary care providers across different practice settings observed that 42% performed HBV screening in >50% of at-risk patients, 49% provided HBV vaccination in >50% of eligible patients; appropriate laboratory monitoring of patients with HBV every 6 to 12 months was noted to be 79% for alanine aminotransferase testing and 67% for HBV viral load, whereas only 49% performed appropriate HCC surveillance.¹⁴

Many ethnic minorities including Asians and African Americans utilize safety-net hospitals, and these underserved populations are at high risk for health care disparities and barriers to optimal HBV and HCC care.^8,12,15 Although provider-specific factors are an important component of engaging patients into appropriate HBV monitoring and management,^6,15–17 patient-specific factors (in addition to health care system factors) also play a significant role influencing HBV care. These factors include health care access, HBV knowledge and beliefs, attitudes and perceived barriers towards HBV, and are likely to be especially important among underserved populations that mainly comprise ethnic minorities and those with limited English language fluency, lower socioeconomic status, and education levels, all factors that may impact the ability to follow provider recommendations. Data on patient-centered HBV educational interventions are limited overall and especially among underserved populations. The ability to identify specific factors contributing to suboptimal HBV monitoring and management provides opportunities to develop targeted educational interventions to address these barriers to improve patient outcomes. To address these gaps in knowledge, we aimed to prospectively assess the impact of a formal patient educational intervention on improving HBV knowledge and improving HBV monitoring and treatment among underserved patients with chronic HBV at an urban safety-net health system.

METHODS

Data Sources

Consecutive adults (age 18 y and older) with chronic HBV (persistence of hepatitis B surface antigen for ≥6 mo) who were being managed at a single-center safety-net liver clinic were recruited from July 1, 2017 to 2018. Our health care system is an urban county health care system that serves as the primary provider of health care for the safety-net population of the city of Oakland and the county of Alameda. Our health care system is ethnically diverse with the majority of the patient population covered by Medicaid-type insurance, which is typical for safety-net health systems. Patients who were unable to provide informed consent or who had medical comorbidities that prevented completion of the survey questionnaire were excluded. Enrolled patients completed an HBV questionnaire before and immediately after the completion of a formal in-person patient educational intervention. The questionnaire construct included assessment of HBV knowledge and patient demographics (age, sex, and race), socioeconomic status (income and education level), insurance status, English language fluency, place of birth, duration of US residency, active substance abuse, active tobacco use, presence of cirrhosis, family history of HBV or liver disease, and history of HBV therapy (Supplementary Table 1, Supplemental Digital Content 1, http://links.lww.com/JCG/A528). HBV knowledge was specifically assessed with 13 questions that were adapted on the basis of the published literature and assessed the patient’s ability to accurately identify situations where HBV is and is not transmitted from one individual to another, ability to identify higher risk of HBV in Chinese individuals versus non-Hispanic white individuals, knowledge that HBV can be treated, knowledge that HBV can cause liver cancer, understanding that treatment can prevent disease progression, and knowledge that untreated HBV can lead to death (Table 1).^18,19 The HBV education was a standardized 20-minute powerpoint presentation given in-person by a single hepatologist in English or the patient’s primary language with the aid of an in-person certified interpreter. The content of the educational intervention included information HBV epidemiology, including the worldwide prevalence, which populations are at highest risk of acquiring chronic HBV, and potential symptoms, dangers, and complications of untreated chronic HBV. The material also included details about modes of HBV transmission, potential avenues from which HBV can be spread from person to person, natural history including disease progression from hepatitis to fibrosis to cirrhosis, the importance of HBV monitoring including clinical follow-up and laboratory monitoring, HBV treatment with antiviral therapy in those that are eligible, and HCC screening among individuals with chronic HBV (Supplementary Table 2, Supplemental Digital Content 1, http://links.lww.com/JCG/A528). The same questionnaire was then administered once more at the next regularly scheduled liver clinic visit for each patient.

TABLE 1.

Questions Assessing Patient’s HBV Knowledge

Questions Assessing HBV Knowledge
Can HBV be transmitted by sharing needles?
Can HBV be transmitted by touching, hugging, or kissing?
Can HBV be transmitted by sharing toothbrushes?
Can HBV be transmitted by being near a person who sneezes?
Can HBV be transmitted by sexual intercourse?
Can HBV be transmitted by sharing food or eating utensils?
Can HBV be transmitted from mother to child during childbirth?
Can HBV be transmitted from one person to another even if you are feeling healthy?
Which of the following patients is most likely to be infected with HBV (White American person, Chinese person, both equally, or I do not know)?
Do you think HBV can be treated?
Do you think that HBV can cause liver cancer?
Can HBV treatment prevent liver problems like cirrhosis or liver cancer?
Do you think people can die from hepatitis B?

HBV indicates hepatitis B virus.

Assessments of HBV knowledge score was on the basis of correct answers to HBV knowledge questions (Table 1), with 1 point for a correct answer and 0 points for incorrect answers, with a total of 13 points possible. Assessments of appropriate HBV monitoring and management included HBV clinic follow-up (≥ 1 visit/year), HBV laboratory monitoring (≥ 1 HBV viral load and alanine aminotransferase test/year), HCC surveillance (≥ 1 liver imaging test/year among eligible patients), and HBV treatment among eligible patients. Assessment of appropriate HBV monitoring and management was additionally evaluated in an HBV control group consisting of 1:1 age (± 5 y) and sex-matched patients with HBV receiving care at the same clinic and who did not receive an educational intervention.

Statistical Analyses

Overall patient characteristics summarized by mean (or median) for continuous variables and frequency for categorical variables and compared using the Student t test for a continuous and χ² test for categorical variables. In the HBV educational intervention group, additional HBV risk factors and patient characteristics were obtained from responses to the HBV questionnaire. HBV knowledge scores are presented as the median and interquartile range (IQR). Improvements in HBV knowledge scores after educational intervention were assessed using the paired t tests. We further assessed the impact of the educational intervention on improvements in appropriate clinic follow-up, laboratory monitoring, HCC surveillance, and HBV treatment among eligible patients¹ by comparing these parameters before and after completion of the intervention. We additionally compared these parameters of HBV monitoring and management between the postintervention group and an HBV control group that did not receive the HBV educational intervention. Adjusted multivariate logistic regression models evaluated the impact of the HBV educational intervention on the aforementioned parameters of HBV monitoring and management. Variables in the multivariate model were selected a priori and included age, sex, race/ethnicity (Asian vs. non-Asian). We further performed a subset multivariate logistic regression analysis of these same outcomes only among the intervention group and variables selected for inclusion in the final model include age, sex, and variables that demonstrated significance (P<0.10) in the univariate model (Supplementary Table 3, Supplemental Digital Content 1, http://links.lww.com/JCG/A528).

Previous studies of patient HBV knowledge that included questions assessing knowledge of modes of transmission, prevention of infection, contraction, and prognosis reported knowledge scores of about 60% at baseline.²⁰ We hypothesized that our educational intervention would improve HBV knowledge scores by 20% (from 60% to 80%). On the basis of this hypothesized improvement, we estimated a sample size needed of 66 to achieve a power of 0.80 and an alpha of 0.05 using a 1-sided statistical analysis. Our final study population was 102 patients with HBV and 102 age-matched and sex-matched HBV controls. All statistical analyses were performed using STATA (version 14, STATCorp, College Station, Texas, USA). Statistical significance was met with a 2-tailed P-value <0.05. This study was approved by Alameda Health System Institutional Review Board.

RESULTS

Overall, 151 consecutive patients with chronic HBV were recruited for the HBV educational intervention, among which 15 patients declined to participate and 34 patients agreed to participate but did not show up to the actual educational session meeting. A final cohort of 102 patients with chronic HBV received the educational intervention, among which 45.1% were female individuals, mean age was 52.0 ± 13.8, 16.7% non-Asian, and 83.3% Asian. The demographics of the HBV control group were similar in age and sex to the intervention group. Additional information regarding patient characteristics and HBV risk factors was obtained from the intervention group from the HBV questionnaire (Table 2). Notable HBV risk factors included receiving dental care in a foreign country (64.7%), household family member with HBV (53.9%), received acupuncture therapy (40.2%), body tattoos (12.8%), and history of blood transfusions (10.8%) (Table 2).

TABLE 2.

Characteristics and Risk Factors of the HBV Educational Intervention Cohort Assessed by Questionnaire

	Proportion (%)	Frequency (N)
HBV risk factors
History of intravenous drug use	6.9	7
History of sexual encounter with known HBV individual	5.9	6
Household family member with HBV	53.9	55
Body tattoos	12.8	13
Body piercings	7.8	8
History of blood transfusion	10.8	11
History of blood exposure on the job	3.9	4
Received dental care in a foreign country	64.7	66
Received acupuncture therapy	40.2	41
Patient characteristics
Has a primary care provider	88.2	90
Interpreter used	60.8	62
Primary language spoken
Non-English	42.2	43
English	57.8	59
Country of birth
US born	10.8	11
vNon-US born	89.2	91
Marital status
Never married/widowed/divorced/separated	34.4	35
Married/living with partner	65.7	67
Highest level of education completed
None/less than high school	23.5	24
High school graduate/some college	52.9	54
College or higher	23.5	24
Annual household income
< US$30,000	55.9	57
≥ US$30,000	19.6	20
Prefer not to answer/not sure	24.5	25
Years since moving to USA if non-US born
< 20 y	83.6	76
≥ 20 y	15.4	14
Unknown	1.1	1
English fluency
Not at all/minimal	66.7	68
Well/fluently	33.3	34
Uses translator at clinic visit	64.7	66
Help with medical material
Never/rarely	28.4	29
Sometimes	13.7	14
Often/always	54.0	55
Unknown	3.9	4
Self-health assessment
Poor/fair	26.4	27
Good/very good/excellent	61.6	72
Unknown	2.9	3
Employment status
Unemployed/retired	55.0	56
Currently working	42.2	43
Other	2.9	3

HBV indicates hepatitis B virus.

Following the in-person language concordant HBV education, HBV knowledge score increased by 25%, from a median of 8 of 13 (IQR, 6 to 9) to 10 of 13 (IQR, 9 to 10), P<0.001 (Fig. 1). This improvement in HBV knowledge was sustained on the basis of a follow-up assessment (mean, 202 ± 102 d) at the next liver clinic visit (median score, 10; IQR, 10 to 10; P=0.92) (Fig. 1).

FIGURE 1.

Improvements in HBV knowledge score following HBV educational intervention. HBV indicates hepatitis B virus.

In addition to improving HBV knowledge, the proportion of patients with HBV receiving appropriate HBV clinic follow-up improved from 25.5% to 81.4% (P<0.001), and was significantly higher than the HBV control group (39.2% control group vs. 81.4% posteducation group, P<0.001) (Fig. 2A). Proportion of patients with HBV receiving appropriate laboratory monitoring improved from 62.8% to 77.5% (P=0.02), which was significantly higher than the HBV control group (42.2%, P<0.001 for comparison with the postintervention group) (Fig. 2B). The rate of HCC surveillance among eligible patients with HBV also increased from 61.0% to 70.5% (P=0.21), and this was higher than the control group (63.0% control group vs. 70.5% postintervention group, P=0.32), although the differences did not reach statistical significance (Fig. 2C). The proportion of eligible patients with HBV receiving antiviral therapy improved from 71.2% to 98.5% (P<0.001), and although this rate was higher than the control group at 91.8%, it did not reach statistical significance (P=0.09 for comparison with the postintervention group) (Fig. 2D).

FIGURE 2.

Improvements in appropriate clinic follow-up (A), appropriate laboratory monitoring (B), appropriate HCC surveillance (C), and appropriate HBV antiviral therapy (D) following HBV educational intervention. HBV indicates hepatitis B virus; HCC, hepatocellular carcinoma.

On adjusted multivariate logistic regression, the HBV educational intervention was associated with significantly higher odds ratio (OR) of appropriate HBV clinic follow-up (OR, 7.02; 95% confidence interval [CI], 3.64–13.56; P<0.001) and appropriate laboratory monitoring (OR, 4.94; 95% CI, 2.64–9.25; P<0.001). Following HBV education, the odds of appropriate HCC surveillance among eligible patients with HBV was 2-fold higher (OR, 1.98; 95% CI, 0.93–4.21; P=0.076) and the odds of initiating HBV treatment among eligible patients was nearly 6-fold higher (OR, 5.75; 95% CI, 0.60–55.60; P=0.13), but these differences did not reach statistical significance likely because of relatively smaller sample size in each respective cohort as our study was not specifically powered for these secondary outcomes (Table 3). Among the subset of patients with HBV who received the educational intervention, each one-point improvement in knowledge score on the postintervention questionnaire was associated with 105% higher odds of appropriate HBV clinic follow-up (OR, 2.05; 95% CI, 1.21–2.45; P=0.008), 65% higher odds of laboratory monitoring (OR, 1.65; 95% CI, 1.01–2.69; P=0.044), and 91% higher odds of HCC surveillance (OR, 1.91; 95% CI, 1.04–3.50; P=0.036) (Supplementary Table 3, Supplemental Digital Content 1, http://links.lww.com/JCG/A528).

TABLE 3.

Adjusted Multivariate Regression Models Evaluating the Impact of HBV Educational Intervention on HBV Monitoring and Management

Appropriate HBV Clinic Follow-up	Adjusted Odds Ratio	95% Confidence Interval	P
Male (vs. female)	1.13	(0.60–2.15)	0.701
Age	1.01	(0.99–1.03)	0.361
Asian (vs. non-Asian)	1.70	(0.79–3.64)	0.173
Educational Intervention	7.02	(3.64–13.56)	< 0.001
Appropriate HBV laboratory monitoring
Male (vs. female)	0.87	(0.47–1.61)	0.662
Age	1.01	(0.99–1.04)	0.256
Asian (vs. non-Asian)	1.41	(0.68–2.95)	0.357
Educational Intervention	4.94	(2.64–9.25)	< 0.001
Appropriate HCC surveillance*
Male (vs. female)	0.80	(0.39–1.61)	0.524
Age	1.01	(0.98–1.04)	0.46
Asian (vs. non-Asian)	0.82	(0.32–2.14)	0.685
Educational intervention	1.98	(0.93–4.21)	0.076
Appropriate HBV treatment†
Male (vs. female)	1.68	(0.23–12.1)	0.605
Age	0.98	(0.91–1.06)	0.663
Asian (vs. non-Asian)	1.16	(0.12–11.49)	0.896
Educational intervention	5.75	(0.60–55.60)	0.130

^*Among patients with HBV eligible for HCC Surveillance.

^†Among patients with HBV eligible for HBV treatment.

HBV indicates hepatitis B virus; HCC, hepatocellular carcinoma.

DISCUSSION

Among an ethnically diverse safety-net population of adults with chronic HBV, our study demonstrated the ability of a targeted in-person language concordant HBV educational intervention to affect a sustained improvement in patient HBV knowledge. More importantly, this educational intervention and the resulting improved HBV knowledge translated into improvements in key parameters of HBV monitoring and management, including HBV clinic follow-up, HBV laboratory monitoring, HCC surveillance among eligible patients with HBV, and appropriate initiation of HBV antiviral therapy. These observations demonstrate the ability of a patient-centered standardized HBV educational intervention to improve HBV knowledge and HBV monitoring and management, particularly among safety-net settings, which provide care to a large proportion of ethnic minorities at risk for chronic HBV infection.

Previous studies evaluating patient-specific interventions focused primarily on improving HBV knowledge and vaccination rates among noninfected patients who are at risk of chronic HBV. Shah and Abu-Amara²¹ performed a systematic review that included 7 studies evaluating the impact of patient education on HBV outcomes. Although these studies did demonstrate the ability of education to improve HBV knowledge, 2 focused vaccination rates among individuals attending clinic for treatment of sexually transmitted diseases,^22,23 3 focused on patients presenting to substance use disorder clinics to evaluate improvements in HBV testing and knowledge,^24–26 one focused on improvements in HBV vaccination in homeless adults,²⁷ and one focused on improvements in HBV knowledge using an online module and survey among pregnant women.²⁸ A more recent study by Zacharias et al²⁹ evaluated the impact of a community outreach program linked with HBV education on improving HBV knowledge in individuals recruited through a free HBV screening and vaccination program. Knowledge regarding HBV risk factors, potential consequences, and treatment options was poor at baseline but improved following education. Although these previous studies demonstrate the ability to improve HBV knowledge through patient education, they did not specifically focus on patients with chronic HBV infection and thus were unable to assess the impact of education on HBV monitoring and management.

Although the impact patient-targeted education on improving HBV monitoring and management has not been well studied, the role of such education on improving outcomes among patients with the hepatitis C virus (HCV) has been previously reported.^19,30 Surjadi et al¹⁹ evaluated 201 patients with chronic HCV who underwent a 2-hour standardized in-person presentation facilitated by a specialized hepatology nurse practitioner that included information on HCV diagnosis, natural history, and treatment. This patient-centered education led to improvements in overall HCV knowledge and translated into higher show rates to liver clinic compared with before the intervention was implemented (64 vs. 39%; P<0.0001). In a follow-up to this study, Lubega et al³⁰ evaluated 118 patients with chronic HCV who received antiviral therapy and demonstrated that patients who received the aforementioned 2-hour patient-centered education had shorter time to initiation of treatment compared with those who did not receive education (median, 136 vs. 284 d; P<0.0001). Furthermore, receipt of HCV education was associated with significantly higher odds of achieving sustained virologic response (OR, 3.0; 95% CI, 1.1–7.9; P=0.03). These findings are in line with our observations that targeted patient education improves disease monitoring and management, likely through improved engagement and adherence to provider recommendations.

Although our current study specifically focused on patient-specific factors, provider-specific factors also play an important role in contributing to appropriate monitoring and management of chronic HBV. Khalili and colleagues identified provider-specific barriers contributing to suboptimal HBV and HCC care among Asian populations and specifically assessed practices with respect to HBV screening and chronic HBV management, HCC surveillance, provider knowledge of HBV and HCC, and attitudes toward (and perceived barriers to) HBV care and HCC surveillance.^6,8,12,15 Thus, comprehensive intervention to improvement HBV care needs to additionally target providers to improve knowledge and awareness of HBV, but also appropriate guideline-based monitoring and management of chronic HBV.

Although our findings provide important data to guide future interventions to improve HBV care, certain limitations should be acknowledged. Given our study cohort consisted of patients receiving care at a single safety-net health system, these findings may not necessarily be generalizable to other practice settings. However, HBV infection disproportionally affects individuals from predominantly immigrant, low income, and underinsured communities^13,31,32 and these individuals mostly rely on safety-net health care resources, and thus understanding mechanisms to improve HBV care among safety-net settings is critical to reducing the disproportionate burden of disease in these populations. A potential limitation of our study is that patients may be utilizing different health systems for care in light of the Affordable Care Act, which may have contributed to an underestimation of follow-up care and monitoring. Nevertheless, our focus on a safety-net HBV cohort is actually a strength compared with other tertiary care settings, given that most patients in safety-net systems are ethnic minorities and may have limited English language fluency, have low socioeconomic status leading to limited health insurance and experience, have known barriers to access to care, thus, unable or unwilling to be seen at other health systems easily.^33,34 Although emergency care might be provided elsewhere, HBV monitoring and management are not usually performed in the acute or emergency settings. Therefore, our study has likely adequately captured HBV outcomes in our cohort. In our study, only the group of patients with HBV who participated in the educational intervention received the questionnaire, and thus, baseline risk factors and characteristics such as educational level, country of birth, and household income were not available for the control cohort given that these data are not readily available for extraction from the medical records. Finally, our study was powered specifically to evaluate changes in HBV knowledge following the educational intervention and not for HBV monitoring and management parameters. Thus, the improvements in HCC surveillance and HBV treatment while higher in the postintervention group compared with both the preintervention and control groups did not reach statistical significance. This is primarily because of the fact that assessment of HCC surveillance and HBV treatment was conducted only in the subset of patients who were eligible for HCC surveillance and HBV treatment, respectively. Thus, given the overall smaller sample size from which to assess changes in HCC surveillance and HBV antiviral treatment, we did not retain adequate power to detect potentially significant effects of the educational intervention. Given that the current study is a non-randomized study, future research should consider a cluster randomized controlled study design with adequate power to not only assess improvements in knowledge but specifically for outcomes such as HCC surveillance and HBV treatment in eligible patients.

In conclusion, among an ethnically diverse safety-net cohort of patients with chronic HBV, a targeted in-person, language concordant formal patient HBV educational intervention achieves a sustained improvement in HBV knowledge after a mean follow-up of over 6 months. This intervention and the resulting improvement in HBV knowledge improved patient adherence to HBV care and directly resulted in improvements in HBV clinic follow-up, HBV laboratory monitoring, HCC surveillance, and appropriate initiation of HBV antiviral therapy, highlighting the importance of addressing patient-specific factors to improve long-term HBV care especially for highly vulnerable populations.