Abstract
Background:
Hepatitis B virus (HBV) infection is endemic in West Africa. There has been a significant increase in the Bronx West African (WA) community. To achieve HBV elimination, vaccination of non-immune individuals is important. Unfortunately, vaccine uptake in immigrant populations is at this time very limited.
Methods:
An educational program was conducted by medical providers of WA origin in collaboration with local faith-based organizations, after which free HBV screening was offered. Non-immune individuals were initially recommended to contact their medical provider or referred to the Department of Health for vaccination. Beginning in 2021, the program offered vaccination. A questionnaire including reasons for vaccination in the program was offered.
Findings:
Among the first 500 individuals screened, 34.6 % required vaccination. Among those screened before program vaccine availability, 72.2 % initiated the vaccination series, with 38.2 % obtaining it at an outside setting and 34 % returning when available through the program. Among patients screened after program vaccine availability, 92.1 % initiated the series. Of those receiving vaccination in the program and completing the questionnaire, 70.7 % had access to care but chose vaccination by the program because of the trust instilled by WA personnel.
Interpretation:
Our findings demonstrate the effectiveness of integrating vaccination into an HBV screening program for an immigrant population. It emphasizes the importance of timeliness and cultural sensitivity.
1. Introduction
Hepatitis B virus (HBV) infection is endemic in West Africa where it poses a significant public health burden. Its prevalence can be as high as 14.5 % in certain regions [1–3]. Hepatocellular carcinoma (HCC) is the leading cause of cancer-related mortality among men in multiple West African (WA) countries, and HBV is its main etiologic agent [4]. HBV vaccination programs in other endemic areas, including programs targeting the early vaccination of infants have been successful at decreasing rates of HBV-related complications such as cirrhosis and HCC [5–7]. A universal vaccination program in Taiwan starting in 1984 led to a significant decrease in HBV burden and HCC over the subsequent 30 years [6]. Unfortunately, coverage for routine childhood vaccination against hepatitis B is only 72 % for West Africa, significantly below the 90 % global target, and birth dose vaccination which is required to prevent vertical transmission has a coverage of only 10 %. In addition, adult coverage is only 18 % in the WHO African Region compared to global coverage of 45 % [8,9]. HBV awareness and vaccination rates in West Africa, unfortunately, remain low. Only 32.0 % of respondents were aware of the existence of the HBV vaccine in a random survey in Nigeria, and only 21.2 % had received at least one dose [10,11]. Recently, the United States Center for Disease Control and the United States Preventative Task Force recommended that all adults older than 18 be screened at least once, and people who are at increased risk, including those born in regions with HBV infection prevalence of ≥ 2 %, be screened periodically [12,13]. Because self-reported vaccination among adults >19 years in the United States was reported to be only 30 %, HBV vaccination was recommended for all adults ages 19–59 without evidence of immunity and adults ≥60 with risk factors for HBV as a component of viral hepatitis elimination efforts [14].
The West African population of the Bronx, New York, as defined by the WHO as individuals from seventeen countries, (Algeria, Benin, Berkina Faso, Cape Verde, Cote d’lvoire, Ghana, Guinea, Guinea-Bissau, Liberia, Mauritania, Niger, Nigeria, Senegal, Sierra Leone, The Gambia, Togo, and Mali) has significantly increased in recent years. From 2017 to 2021, approximately 46,600 people of West African origin immigrated to the Bronx [15,16]. In the 2022 census, Africans (predominantly from West Africa) comprised 11 % of the non-citizen residents and 10.7 % of all naturalized citizens in the Bronx [17]. Screening and subsequent vaccination for HBV in the immigrant West African community is currently limited. In a survey of 919 African immigrants in NYC, 56.6 % were HBV non-immune, and only 10.9 % had evidence of prior HBV vaccination [18]. Possible barriers to vaccination that have been proposed include cost, lack of insurance coverage and integration in the United States healthcare system, limited disease awareness, lack of English proficiency, cultural beliefs surrounding Western medicine, and stigma surrounding HBV [19–21].
We previously reported our success in motivating screening for HBV in Bronx West African immigrants through a culturally sensitive educational program held in conjunction with faith-based organizations [20]. We titled our efforts the Starfish Program based on the parable adapted from Loren Eiseley’s The Star Thrower which emphasizes the value of every individual. In 2021 the Program expanded its scope to include free HBV vaccination for non-immune individuals. In this report, we present the effectiveness of integrating HBV vaccination within a screening program targeting a West African immigrant population.
2. Materials and methods
2.1. Serologic screening
Beginning in 2017, medical professionals of West African origin (two physicians and one patient navigator with a Master’s in Public Health), conducted educational outreach events at local mosques and churches on the impact of HBV as previously described [20]. At the conclusion of the events, arrangements were made for free HBV screening (hepatitis B surface antigen [HBs Ag] and surface antibody [HBs Ab]) at Montefiore Medical Center. A culturally sensitive educational brochure was also provided which included information on HBV and the benefits of vaccination. At the time of the screening session, event attendees were also given the option to refer family and friends for testing. All participants were provided screening results, and a letter was sent with an explicit interpretation of infection status (active infection, evidence of immunity, nonimmune with recommendation for vaccination). Requirements for a complete evaluation was reviewed by the Program hepatologist with all individuals who tested positive for HBsAg, and transition to care was arranged with the patients’ treating physician, Montefiore Hepatology Program, and municipal hospital clinic based on patient preference and/or insurance status. Subsequent contact with the patients indicated that many were not receiving the appropriate care. Additional funds were obtained, and all individuals are now offered a free comprehensive evaluation that adheres to the 2023 CDC Guidelines [12,22].
2.2. HBV vaccination
Individuals requiring HBV vaccination were initially instructed to contact their primary care providers (PCP) for vaccination or referred to a Department of Health (DOH) facility for those who lacked insurance. In December 2020, philanthropic funds for free vaccination were raised, and all non-immune individuals were offered free vaccination through the Program beginning January 2021. In addition, the individuals determined to require vaccination prior to that time were contacted to determine if vaccination had been performed and offered vaccination if it had not been received. HepB-alum 3-dose HBV vaccine was administered until June 2021 at which time vaccination was switched to the Heplisav-B 2-dose series. Vaccinations were performed without inquiring about insurance status throughout 2021. Beginning in 2022, information regarding insurance status was obtained, and permission was requested to bill insurance if available. In addition, a free blood pressure cuff was offered to all individuals as part of a concomitant hypertension screening program.
2.3. Questionnaire
Beginning January 2022, all individuals undergoing vaccination were invited to complete a questionnaire that collected information regarding demographics (age, gender, country of origin, years in the US), insurance status, evidence of a PCP, and history of a chronic condition that was being managed in the United States. For those obtaining vaccination at the Starfish Program, the reason for vaccination by the Program was also recorded (not integrated into the US healthcare system, PCP did not discuss or recommend, or trust) (Fig. 1). Persons were assigned to “not integrated into the US healthcare system” if they did not have insurance or evidence of ongoing contact with the US healthcare system (no PCP, or absence of a chronic medical condition managed in the US). If an individual was integrated in the US healthcare system but chose to be vaccinated in the Program, they were then subdivided into “PCP did not discuss/recommend” or “trust” based on the questionnaire. The category of “trust” was defined as compliance with vaccination due to the presence and reassurance of the West African Program personnel. The questionnaire was only available in English, but it was administered by a Program member who also spoke both Hausa and Twi for those who needed interpretation. A medical phone interpreter was used for two individuals who spoke French.
Fig. 1.
Assessment of reason for vaccination through Starfish Program Individuals were assigned to “not integrated into the US healthcare system” if they did not have US insurance, PCP, or a chronic medical condition that was managed in the US. Individual who had evidence of integration in the US healthcare system were subdivided into “PCP did not discuss/recommend” or “trust” based on questionnaire response. PCP, Primary Care Physician; HBV, Hepatitis B virus; US, United States; SP, Starfish Program.
An attempt was made to contact all individuals who previously had been identified as requiring vaccination and encouraged to return for completion of the questionnaire, HBV vaccination if not previously performed, and a new hypertension screening program with an incentive of a free blood pressure cuff. Individuals who signed the informed consent and completed the questionnaire were given a $50 gift card for travel related expenses.
2.4. Vaccination compliance
An analysis of the first 500 individuals screened was performed to determine the proportion of those who required HBV vaccination and who initiated and completed the series. If vaccination was received at another location (PCP or other private setting, Department of Health), an attempt was made to corroborate vaccination by reviewing accessible shared electronic medical records (Care Everywhere portal, EPIC®) or by obtaining outside records. Otherwise, a reliable history based on timing and description of a multi-dose series was relied upon with special consideration to differentiate HBV from COVID-19 vaccination. “Refusal” was defined as any individual who did not return for vaccination when offered and did not obtain it elsewhere. Individuals who were screened prior to HBV vaccination offering by the Program and could not be contacted to inform them of its availability were considered “lost to follow-up.” Rates of vaccination attainment through PCP or other private setting, DOH, and the Starfish Program were tabulated.
2.5. Impact of Starfish Program vaccine availability and incentives on vaccination rate
Individuals requiring vaccination were divided into three cohorts: Cohort A screened prior to the availability of Program vaccination; Cohort B screened in calendar year 2021 when vaccination was available and offered at the time that results were provided; and Cohort C screened in calendar year 2022 when vaccination was offered at the time results were provided and incentives offered (free blood pressure cuff and travel stipend). To determine whether proximity of screening to Program vaccine offering affected vaccination rates, Cohort A was divided into 3 groups. Group 1 was screened before 2020, group 2 from January to June 2020, and group 3 from July to December 2020.
For Cohort A, receipt of vaccination, site (Program versus outside facility), timing relative to availability of Program vaccination and offer of incentives were tabulated. For Cohort B, receipt of vaccination, site, and timing related to offer of incentives were tabulated. For Cohort C, receipt of vaccination and site of vaccination were tabulated.
2.6. Statistical analysis
Demographic information, clinical characteristics, and screening/vaccination data points were tabulated as means and standard deviations or counts and percentages. Data collection was performed using Microsoft Excel. Nominal data was analyzed using Fisher’s exact tests and Chi-Squared tests based on sample size, per current statistical guidelines [23]. Strength of association was assessed using Mean Square Contingency Coefficient (Phi Coefficient) where applicable. All computations were performed using IBM® SPSS® Statistics version 28.0.1.0.
2.7. Institutional review board
Serologic testing was performed as a free clinical service at Montefiore Medical Center. The questionnaire was approved by the Albert Einstein Institutional Review Board, and written informed consent was obtained prior to its completion.
2.8. Role of the funding source
Study sponsors had no role in study design; collection, analysis, or interpretation of data; writing of the report; or the decision to submit the paper for publication.
3. Results
3.1. Serologic screening
Five hundred individuals were screened from October 2018 to April 2022. One-hundred seventy-three (34.6 %) were non-immune. Ninety-seven individuals were in Cohort A, 43 in Cohort B, and 33 in Cohort C.
3.2. HBV vaccination and compliance
Among Cohort A, only 31 (32.0 %) obtained vaccination from a PCP or other private setting and 4 (4.1 %) from a DOH facility at the time of screening when vaccination by the Program was not available, and two individuals obtained vaccination from the military as a requirement for service. Twenty-five (25.8 %) individuals returned for vaccination by the Program in 2021. One individual who was unable to be contacted in 2021 readily returned for vaccination in 2022 when finally reached. Seven (7.2 %) deferred vaccination in 2021 but agreed in 2022 when offered the incentives. Thirteen (13.4 %) refused vaccination, 12 (12.4 %) were lost to follow-up, and 2 (2.1 %) died. In total, 70 individuals (72.2 %) received the first vaccination. Compliance with the series was 88.6 % (Fig. 2). Eight individuals did not complete the series, including 2 individuals who had a reaction to the first injection. There was no significant change in vaccination rates between screening period groups 1, 2, and 3 (75 %, 60 %, 86.7 %, respectively; p = 0.147).
Fig. 2.
Sankey diagram of vaccination status for Cohorts A-C- SP, Starfish Program;
Among Cohort B, 35 (81.4 %) individuals received the first HBV vaccination without an incentive in 2021, significantly more than those in Cohort A who were screened prior to vaccine availability (p < 0.001). Thirty-three (76.7 %) were vaccinated in the Program, and 2 individuals (4.7 %) obtained it from a PCP or other private setting. Three individuals (7.0 %) initially deferred vaccination but returned in 2022 when offered the incentives. Five individuals (11.6 %) declined to return for vaccination, including 2 who relocated from the Bronx immediately after undergoing screening. In total, 88.4 % individuals received the first vaccination. Compliance with the series was 94.7 % (Fig. 2).
Among Cohort C, 32 individuals (97.0 %) received the first vaccination. One (3.0 %) person obtained it from a PCP, and 31 (93.9 %) from the Program. One (3.0 %) individual refused vaccination. Compliance with the series was 90.6 % (Fig. 2).
The median timing between screening and the date of the first dose of the vaccine for the individuals in Cohorts B and C was 8.0 days.
Compliance was compared between participants who received the 3-dose vaccination series and the 2-dose series through the SP (p = 0.118). Twenty-two individuals started the 3-dose series, and 19 (86.36 %) completed the series. Seventy-eight individuals started the 2-dose series, and 75 (96.15 %) completed the series.
3.3. Questionnaire
Ninety-three individuals (53.8 %) completed the questionnaire, including 44 (45.4 %) of Cohort A, 18 (41.9 %) of Cohort B, and 31 (93.9 %) of Cohort C. Mean age was 53 ± 11.9, and 66.7 % were male. Ninety-two (98.9 %) were born in West Africa, including 63 (67.7 %) from Ghana. The mean number of years lived in US was 16.9 ± 9.6.
Among the 26 individuals in Cohort A who were vaccinated in the Program and completed the questionnaire, 22 (84.6 %) were previously integrated into the US healthcare system. Reasons for vaccination by the Program included not being integrated in the US healthcare system (4, 15.4 %), PCP not discussing or recommending HBV vaccination (1, 3.9 %), and trust (21, 80.8 %).
Among the 18 individuals in Cohort B who were vaccinated in the Program and completed the questionnaire, 12 (66.7 %) were previously integrated into the US healthcare system. Reasons for vaccination by the Program included not being integrated in the US healthcare system (6, 33.3 %), PCP not discussing or recommending HBV vaccination (1, 5.6 %), and trust (11, 61.1 %).
Among the 31 individuals in Cohort C who were vaccinated in the Program and completed the questionnaire, 21 (67.7 %) were previously integrated into the US healthcare system. Reasons for vaccination by the Program included not being integrated into the US healthcare system (10, 32.3 %) and trust (21, 67.7 %).
4. Discussion
In this report, we describe the effectiveness of integrating HBV vaccination within a culturally sensitive screening program targeting a West African immigrant population. Of the individuals screened within the first year that the vaccine was offered through the Program, 88.4 % of non-immune individuals received at least one dose. This rate is significantly greater compared to that when vaccination was not available when only 32 % of the individuals that were screened obtained it from their PCP or another private setting, and 4 % from the DOH. During the first year that the vaccine was offered by the Program, 25.8 % of those previously screened readily returned for vaccination. Importantly, 12.4 % were lost to follow-up. An important factor in promoting vaccination by the Program is “trust.” Among participants who were vaccinated in the Program and completed the questionnaire, 53 (70.7 %) were integrated into the US healthcare system yet obtained the vaccine specifically from the Program due to the trust instilled by its West African personnel.
Vaccination rates among immigrant populations are low. Compared to native-born Americans, foreign-born populations consistently have lower rates of vaccination across all major vaccine types, including pneumococcal polysaccharide vaccine (62.6 % vs 40.5 %), tetanus (65.0 % vs 50.6 %); TDAP (15.5 % vs 9.3 %), and human papillomavirus (38.7 % vs 14.7 %) [24]. HBV vaccination presents an additional barrier to compliance as it consists of a multi-dose series. In a study comparing the 3 versus 2-dose HBV series, only 44.7 % and 60.5 % completed vaccination within a year, respectively [25]. When combined, these factors result in dramatically lower HBV vaccination rates in immigrant populations. In a survey of 359 Vietnamese immigrants, only 7.3 % reported having received the HBV vaccination [26]. In a study of 919 sub-Saharan African immigrants in New York City, only 10.9 % demonstrated evidence of prior vaccination [18]. The high vaccination and compliance rates achieved in our Program are striking and are even higher than that of a native-born population.
Insurance coverage and ongoing healthcare utilization have been proposed to be key factors for promoting vaccination in immigrant populations [24]. While these factors are undoubtedly influential, our findings indicate that these are not necessarily the most important ones. Among the individuals screened prior to the availability of Program vaccination, few utilized the option for free vaccination at the DOH. More importantly, 79.0 % of individuals from Cohort A who returned for vaccination and completed the questionnaire had ongoing interaction with the healthcare system and access to vaccination but did not obtain it from their established medical provider. However, they readily returned for vaccination when offered by the Program.
Our results emphasize that trust is an essential component of an outreach program that targets a vulnerable population with significant cultural concerns [27,28]. The majority of individuals (70.7 %) vaccinated by the Program who completed the questionnaire chose to do so because of the trust which was formed through the educational and screening program staffed by West African personnel. In fact, it was not unusual for an individual to explicitly state that the comfort provided by the presence of West African personnel was essential to their decision to undergo screening and vaccination. As an anecdote, several non-immune West African healthcare workers sought out screening so that they could receive vaccination from the Program even though they had access for several years to free and convenient vaccination through their employee health programs. It is important to note the Program vaccinations required additional visits to a hospital site that was in the midst of intensive COVID-19 precautions and not otherwise frequented by the participants; it was not necessarily a more convenient option than vaccination elsewhere.
Our findings also highlight the importance of timing in promoting vaccine uptake. Cohort B, which was offered Program vaccination as an option at the time that results were provided, led to a vaccination rate of 88.4 % with only 3 individuals requiring an incentive and none lost to follow-up. In contrast, Cohort A, which was not initially offered vaccination, had a rate of only 72.2 %, and 12 (12.4 %) were lost to follow-up. Interestingly, there was no observed relationship between timing of the educational programming and vaccination rates within Cohort A. Our results emphasize the importance to “strike while the iron is hot” and offer the vaccination at the time of screening while the individual is most cognizant of its importance.
When analyzing the role that incentives play in motivating individuals to obtain vaccination, we found that a slightly greater percentage obtained vaccination when incentives were offered in Cohort C when compared to Program vaccination without an incentive in Cohort B (p = 0.042, Phi- Coefficient = 0.239). Although this difference was significant, the strength of association between implementing Program vaccination and vaccine compliance was stronger (p < 0.001, Phi-coefficient = 0.418 between Cohort A and Cohort B).
There are several limitations to our findings. First, it was assumed that the 12 individuals (12.4 %) who were lost to follow-up were not vaccinated. Completion rate of the questionnaire in Cohorts A and B were relatively low (45.4 % and 41.9 %) as it was only available beginning in 2022, and many individuals vaccinated prior to this time did not return to complete it. This study is observational in nature and does not directly assess causality. It was not possible to verify all vaccinations performed at an outside facility. However, none of these limitations detract from the importance of our findings. An additional limitation was not determining whether HBcAb was present. The screening program was started with very limited funds. It was decided to defer HBcAb testing because (1) the goal was to maximize the identification of the number of HBsAg positive individuals, (2) HBV vaccination was not an initial consideration, and (3) the cost of measurement of HBcAb was disproportionally high compared to the other two measures. As the program expanded, funds were specifically recruited for vaccination. Because at least one vaccine was indicated due to the high-risk population and it was assumed that few would comply with the series, HBcAb testing was not initially performed. After review of this experience, it has since been included in the Program.
Our study presents an effective model for increasing HBV vaccination in a high-risk population by incorporating it in a culturally sensitive screening program. Our findings emphasize the importance of cultural sensitivity, timeliness, and the relatively limited impact of insurance and healthcare integration status. The World Health Organization has recently made the elimination of viral hepatitis by 2030 a key public health initiative. Because HBV is most prevalent in low- and middle-income countries where it is associated with significant stigma, it is imperative to develop effective vaccination programs for these populations. Our study presents a tangible and readily replicable solution which should be able to be adapted to any population and vaccine-preventable disease.
5. Dedication
This paper is dedicated to the memory of Jason Marks. The generosity of his family and friends made this program possible.
Acknowledgments
The authors would like to acknowledge Jin Carrero, LPN and Juliet Silvera, LPN who administered the vaccinations, and Bergan Pharmacy for donation of the blood pressure cuffs to the program.
The authors would like to thank the following funding sources for helping make this program possible:
Gilead Sciences.
Check Hep B Navigation Program funded by the New York Council.
Donations by Friends and Family of Jason Marks and the 41–74 Club of NY.
Funding
Funding provided by Gilead Sciences, Check HepB Navigation Program, friends, and family of Jason Marks, and the 41–74 Club of NY.
Footnotes
CRediT authorship contribution statement
Jessie A. Birnbaum: Conceptualization, Investigation, Methodology, Data curation, Formal analysis, Writing – original draft. Daniel Guttman: Conceptualization, Investigation, Methodology, Data curation, Formal analysis, Writing – original draft. Mugdha Parulekar: Conceptualization, Investigation, Methodology, Data curation, Formal analysis, Writing – original draft. Fatima Omarufilo: Conceptualization, Investigation, Methodology, Data curation. Emmanuel U. Emeasoba: Conceptualization, Investigation, Methodology. Julie Nguyen: Conceptualization, Investigation, Data curation, Writing – original draft. Oluwadara Tokunboh: Conceptualization, Investigation, Data curation, Writing – original draft. Jared Coe: Conceptualization, Investigation, Writing – review & editing. Matthew J. Akiyama: Conceptualization, Investigation, Writing – review & editing. Samuel H. Sigal: Conceptualization, Investigation, Methodology, Data curation, Funding acquisition, Writing – original draft.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Data availability
Data will be made available on request.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Data will be made available on request.