Research
Early Identification and Linkage to Care of Foreign-Born People with Chronic Hepatitis B Virus Infection, Multnomah County, Oregon, 2012–2014 Jaime Walters, MPHa Amy Sullivan, PhD, MPHb
ABSTRACT Objective. Hepatitis B virus (HBV) infection is a global health concern, with a large proportion of high-risk individuals unaware of their infection status. People born in countries with medium to high endemicity of HBV should be tested and linked to care. We describe a program that improved identification and linkage to care for refugees and immigrants at the Multnomah County Health Department in Oregon. Methods. We instituted outreach clinics and community referrals and expanded refugee screening to identify foreign-born people at risk for HBV. We obtained data from electronic health records and electronic laboratory reporting, including patient demographics, hepatitis B testing variables, vaccination history, and—for positive cases—risk-factor and linkage-to-care data. All results were entered into an Internet-based data collection tool. For this analysis, we only used results for testing performed from October 2012 through June 2014. Results. We screened 2,087 foreign-born people for HBV infection and identified 77 (4%) people with positive results. HBV infection prevalence varied by site, with 7% of HBV-positive people identified through the outreach and voucher program and 3% identified through refugee screening. Of the 77 people testing positive for HBV, 72 (94%) were successfully linked to care, of whom 68 (94%) attended their first follow-up visit. Conclusion. Implementation of a culturally competent screening program among immigrants and refugees in Multnomah County improved case finding and subsequent linkage to care.
Multnomah County Health Department, Community Epidemiology Services, Portland, OR
a
Multnomah County Health Department, Communicable Disease Services, Portland, OR
b
Address correspondence to: Jaime Walters, MPH, Multnomah County Health Department, Community Epidemiology Services, 426 SW Stark St., 3rd Fl., Portland, OR 97204; tel. 503-988-3406; e-mail . ©2016 Association of Schools and Programs of Public Health
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An estimated 350 million people worldwide are infected with the hepatitis B virus (HBV), resulting in 600,000 annual deaths.1,2 In the United States, more than 2 million people may be chronically infected, although three-quarters of them may not be aware of their infection status, thereby increasing their likelihood of passing the disease to others.3 People infected with HBV may have a self-limiting infection, where they eliminate the virus and have immunity from subsequent reinfection, or may progress to chronic infection that could lead to complications such as cirrhosis, liver failure, and hepatocellular carcinoma.4,5 Although the incidence of acute HBV infection is decreasing, about 43,000 new infections are identified each year in the United States, making early screening and referral to care imperative.5,6 A safe and effective vaccine for HBV prevention has been available in most higher-income countries since the 1980s.7,8 Additionally, the morbidity and mortality associated with HBV infection can be reduced by screening individuals at high risk for infection and by offering appropriately timed antiviral therapy.4,5 However, with the rise in international migration, the number of high-risk immigrants and refugees coming from countries of intermediate and high hepatitis B prevalence has increased substantially.9 HBV-associated sequelae (e.g., cirrhosis and hepatocellular carcinoma) are serious problems in these groups.10,11 Hepatitis B surface antigen (HBsAg) is a marker of chronic infection. Since 2008, the Centers for Disease Control and Prevention (CDC) has recommended that all people in the United States born in geographic regions with HBsAg prevalence $2% (e.g., Asia, Africa, Eastern Europe, the Middle East, and Pacific Islands) be tested for HBsAg and that those infected are linked to medical care and preventive services.5 This group includes immigrants, refugees, asylees, and internationally adopted children born in these areas, regardless of past vaccination status. In 2012, the CDC Division of Viral Hepatitis awarded funds to nine sites through the Prevention and Public Health Fund to implement these recommendations. The Multnomah County Health Department (MCHD) Communicable Disease Services (CDS) was one of these nine grantees (HBV only) in CDC’s Hepatitis Treatment and Linkage to Care (HepTLC) initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. (Other jurisdictions did similar work for hepatitis C.) To increase HBV outreach, testing, and linkage to care of foreign-born people, MCHD expanded HBV testing through the
Refugee Medical Assistance (RMA) program and implemented a culturally and linguistically appropriate, community-based referral mechanism. Linkage to care included referral to a primary care provider or specialist for further evaluation, monitoring, and possible treatment of chronic HBV infection. We describe a HepTLC program that improved case finding and subsequent referrals to improve health outcomes for refugees and immigrants in our jurisdiction. METHODS MCHD is Oregon’s largest local public health agency and safety-net provider serving the Portland metropolitan area, which comprises 1,641,036 residents (43% of the state population) and the majority of Oregon’s newly arriving refugees. Expanded refugee screening MCHD operates the RMA program to provide comprehensive health screenings to nearly all of Oregon’s newly arrived refugees (about 1,000 per year). Screening involves a general examination, including nutritional history, immunizations, an emotional distress screening, and laboratory testing for malaria, lead toxicity, parasites, sexually transmitted infections, and tuberculosis. Previously, the RMA program screened about 30% of these refugees (i.e., primarily women of childbearing age) for HBV. Under the Prevention and Public Health Fund program, and augmented with additional grant funding in the second year, CDS staff members supported the RMA program by expanding protocols for HBV testing to include all incoming refugees and coordinated follow-up for RMA clients who screened positive for HBV. A grant-funded community health specialist linked HBsAg-positive refugees to care. For insured people, linkage to care included linkage to the client’s primary care home; for uninsured people, linkage included referral to other clinics or resources. Community referrals The CDS program partnered with local organizations serving foreign-born people to expand HBV testing in two ways. First, a voucher system was created to refer clients from partner organizations to our CDS clinic for free testing. Second, testing was performed at onsite clinics (e.g., apartment complexes and refugee and immigrant organizations) to reach the target populations where they lived, worked, and prayed. This method also helped overcome perceived barriers to testing, such as transportation issues.
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Data sources For incoming refugees screened through RMA, data were available through the electronic health record (EHR). Encounter data for refugee screening visits were obtained electronically. For the outreach and voucher programs, CDS was the referring provider, so all data needed were collected and housed at MCHD (i.e., paper files). Because HBV is a reportable condition in Oregon, cases could also be identified via electronic laboratory reporting. Laboratory reports are automatically downloaded into the Oregon Public Health Epidemiologists’ User System (Orpheus). Public health nurses review reports coming in through electronic laboratory reporting, and investigations are initiated according to state-determined guidelines. Data collection All data (i.e., from EHR, Orpheus, or otherwise) collected as part of HepTLC were entered into an Internet-based data collection tool called EvaluationWeb®.12 This system, provided by CDC to all HepTLC sites and operated by a contracting data coordination
center, was intended for monitoring and evaluation purposes only. Information collected included patient demographics (i.e., age, sex, birth year, country of origin, race/ethnicity, and health insurance status), HBV testing variables (i.e., test date, test result, and laboratory type), whether and when the patient received test results, and if a vaccination history for either HBV or hepatitis A existed. For HBsAg-positive patients, risk-factor information, patient education provided (e.g., alcohol education), linkage to care (i.e., how the patient was linked to care, follow-up appointment date, and whether the patient attended that appointment), and if and what date the patient was reported to surveillance were also collected. Patients self-reported attendance at follow-up appointments. All patients were assigned a unique client identification that contained no protected health information. The data coordination center reviewed data monthly for accuracy, and monthly calls were conducted with the center’s technical specialist. We performed all data analyses using SAS® version 9.3.13
Table 1. Characteristics of foreign-born people with hepatitis B virus infection identified during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a by hepatitis B surface antigen result, Multnomah County, Oregon, October 2012–June 2014
Characteristic Total Sex Male Female Age, in years ,18 18–49 $50 Region of origind,e East Asia and the Pacific Sub-Saharan Africa Eastern Europe and Central Asia South Asia Middle East and North Africa Latin America and Caribbean Health insurance status Yes No/don’t know
Total number tested (percent of total)b
Number testing positive for hepatitis B surface antigen (percent of positive)
Proportion testing positive within group (percentage)
2,087 (100)
77 (100)
4
1,089 (52) 998 (48)
46 (60) 31 (40)
4 3
407 (19) 1,190 (57) 490 (24)
8 (10) 47 (61) 22 (29)
2 4 5
36 27 4 5 5 0
(47) (35) (5) (6) (6) (0)
6 7 6 2 1 0
62 (81) 15 (19)
3 6
P-valuec
0.176
0.105
,0.001 613 410 72 240 470 268
(30) (20) (3) (12) (23) (13)
0.046 1,833 (88) 254 (12)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. b
Percentages may not total to 100 because of rounding.
P-value from Pearson’s χ2 test assessing the significance of differences across groups within characteristics
c
d
World Bank country classification
Excludes 14 people unable to be categorized (i.e., missing, don’t know, or declined) with negative hepatitis B surface antigen results
e
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Table 2. Number and percentage of foreign-born people tested for hepatitis B virus infection, testing positive, and linked to care during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a Multnomah County, Oregon, October 2012–June 2014 Site Total Refugee screeningc Voucher/outreachd
Number tested (percent)
Number testing positiveb (percent)
Number linked to care (percent of those testing positive)
2,087 (100) 1,533 (73) 554 (27)
77 (4) 41 (3) 36 (6)
72 (94) 39 (95) 33 (92)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. b
Statistically significant at p,0.001
Clients who were tested for hepatitis B as part of their comprehensive health screening as incoming refugees
c
Clients who were tested for hepatitis B by returning coupons/vouchers to the Multnomah County Communicable Disease Services clinic or who were tested at outreach sites, including apartment complexes or community centers
d
RESULTS From October 2012 through June 2014, 2,087 people were tested for HBV infection (Table 1). We observed no difference between HBsAg test result and sex or age group (p50.176 and p50.105, respectively). Region of origin was significantly associated with test result (p,0.001). People who tested positive for HBsAg were disproportionately and predominantly from East Asia and the Pacific (6% and 47%, respectively) and subSaharan Africa (7% and 35%, respectively). Individuals without health insurance were twice as likely to screen positive for HBsAg compared with individuals who had health insurance. Of the 2,087 individuals screened, 73% were tested via the refugee screening program, and 27% were tested at outreach clinics or through CDS (Table 2).
A total of 77 people (4%) were positive for HBV infection. Prevalence varied by test site, with 36 (7%) positive results at outreach or CDS clinics and 41 (3%) positive results at refugee screenings (p,0.001). Of the 77 HBV-positive individuals, 72 (94%) were successfully linked to care, 70 (97%) of whom saw a primary care physician. Sixty-eight (94%) individuals attended their first appointment (Table 3). Among those not linked to care, one refused, one moved out of state, and three could not be located. Linkage to care was highest from referrals for refugee screening. All patients were seen for follow-up within 90 days of their positive test (median 5 30, maximum 5 84). All cases were reported to surveillance. A total of 477 individuals who tested HBsAg negative were also hepatitis B core antibody (anti-HBc) p ositive,
Table 3. Test results, counseling, and mechanism for linkage to care for foreign-born people tested for hepatitis B virus infection during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a Multnomah County, Oregon, October 2012–June 2014 Total N (percent)
Variable Number of people tested for hepatitis B virus infection (percent) Number testing positive (percent of tested) Number given results (percent) Number counseled (percent) Number linked to care (percent) Number referred to primary care/set up appointment with primary care physician (percent) Number set up appointment with specialist (percent) Number attended first appointment (percent)
2,087 77 75 75 72 70
(100) (4) (97) (97) (94) (97)
2 (3) 68 (94)
Refugee screeningb N (percent) 1,533 41 41 41 39 37
(73) (3) (100) (100) (95) (95)
2 (5) 38 (97)
Voucher/outreach screeningc N (percent) 554 36 34 34 33 33
(27) (6) (94) (94) (92) (100)
0 (0) 30 (91)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014.
Clients who were tested for hepatitis B as part of their comprehensive health screening as incoming refugees
b
Clients who were tested for hepatitis B by returning coupons/vouchers to the Multnomah County Communicable Disease Services clinic or who were tested at outreach sites, including apartment complexes or community centers c
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Table 4. Hepatitis B core antibody result by hepatitis B surface antigen result in foreign-born people tested for hepatitis B virus infection during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a Multnomah County, Oregon, October 2012–June 2014 Hepatitis B surface antigen test Hepatitis B core antibody result Total Positive Negative Indeterminate
Total number tested (percent)b 2,087 552 1,534 1
Number testing positive (percent)
(100) (26) (74) (,1)
77 75 2 0
(4) (97) (3) (0)
Number testing negative (percent)b 2,010 477 1,532 1
(96) (24) (76) (,1)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. b
Percentages may not total to 100 because of rounding.
indicating a past, cleared infection and immunity (Table 4). Of these 477 individuals, 286 (60%) were from East Asia and the Pacific, 91 (19%) were from sub-Saharan Africa, and the remaining 97 (20%) were from South Asia, Middle East and North Africa, Latin America and Caribbean, and Eastern Europe and Central Asia. Individuals identified via the HepTLC initiative had very few risk factors for HBV infection aside from their country of origin. None of the 77 HBsAg-positive people reported past injection drug use, human immunodeficiency virus positivity, or, in males, male sexual partners. Seven people (9%) were ever a household contact to a person with known HBV (five in the previous 12 months), and three (4%) reported multiple sexual partners (i.e., .1 sexual partner in a six-month period). DISCUSSION Screening of 2,087 foreign-born people through refugee screening or community referrals revealed 77 cases of chronic HBV infection that might otherwise have gone undetected. The majority of people testing HBsAg positive were from regions with the highest HBV prevalence (East Asia and the Pacific and subSaharan Africa). Consistent with one of the goals of the HepTLC initiative (i.e., to increase awareness of HBV infection status for people from intermediate and high HBV-endemic countries and help them obtain linkage to medical care), nearly all people found to be infected with HBV were informed of their test results, given appropriate posttest counseling, and linked to care. Our jurisdiction’s percentage of people linked to care was higher than the linkage-to-care rate of two other larger sites (i.e., New York, New York, and San Diego, California) and consistent with a site of similar size already using refugee screening (i.e.,
Minneapolis-St. Paul, Minnesota).10 Linkage to care was most successful through refugee screening, where incoming people were eligible to receive eight months of health benefits through the state Medicaid program. Only one individual screened through this mechanism refused to be linked to care. Outreach clinics were also successful at linking patients to care. However, as in the New York and San Diego study sites, following up with these individuals proved challenging.10 We found that compared with people identified through refugee screening, more people reached via outreach lacked health insurance. Only two people were found to be positive through direct referrals to CDS, but one could not be located. Both of the patients testing positive from CDS lacked health insurance, making collaborations with other community groups and organizations serving foreign-born populations essential for successful linkage to care. We identified a higher prevalence of chronically infected clients from outreach than through refugee screening. This finding was unexpected but could be explained by variations in refugees from particular countries of origin, which vary from year to year. In 2013, the majority of refugees in Multnomah County came from the Middle East and North Africa, where HBV prevalence is lower than in other regions.14 In 2014, the number of refugees to Multnomah County from sub-Saharan Africa increased, especially from the Democratic Republic of Congo, which has experienced ongoing conflict.15 Concomitantly, HBsAg positivity in refugees increased significantly from 2% in 2012–2013 to 4% in 2014 (p50.02). We found a sizeable proportion of all people tested who were HBsAg negative and anti-HBc positive. This combination is typically indicative of past infection and shows immunity from further infection.4,16 As might be expected, immunity to HBV was highest
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in those regions with the highest seroprevalence of chronic HBV infection (i.e., East Asia and the Pacific and sub-Saharan Africa). The percentage of people immune to HBV infection was lower in lowerseroprevalence regions (e.g., South Asia, Middle East, and North Africa). A recent meta-analysis showed an overall pooled seroprevalence of HBsAg of 9.6 (range: 8.2–11.1); in East Asians and Pacific Islanders, the seroprevalence rose to 13.2 (range: 12.0–14.4).4 Regardless, the seroprevalence estimates mirrored the chronic HBV prevalence in those regions. Even in refugees from lower seroprevalence countries, other studies have shown that screening for chronic HBV infection is cost effective, even at prevalence as low as 0.3%.3,4,17 An additional test, antibody to hepatitis B surface antigen (anti-HBs), can determine immunity from past vaccination (or prior infection, if anti-HBc is not ordered at the same time). Of 2,010 people who tested negative for HBsAg, 1,532 (76%) were found to be susceptible to HBV infection. These individuals could benefit from HBV immunization. Refugees often come to the United States with missing or incomplete vaccination records, and, without testing for anti-HBs, it is possible that vaccination could be offered to people already immune to infection. As such, refugees at high risk for HBV infection are offered vaccine during RMA screening when both surface antigen and core antibody are negative, and no additional testing (e.g., anti-HBs) is performed. However, at CDS, clients are tested for anti-HBs before being offered vaccine. This testing algorithm may result in considerable cost savings. Although the vaccine itself is free to clients in high-risk populations, MCHD pays any associated administrative fees (i.e., nursing fee, injection fee), which cost about $22. This cost can triple if a person needs up to three doses of vaccine. The anti-HBs test only costs about $8. A recent cost-effectiveness analysis of hepatitis B testing strategies in Canadian immigrants found that screening was a reasonably cost-effective approach because vaccinating the entire immigrant cohort would produce a small relative decrease in morbidity and mortality from new chronic infections that might occur. Furthermore, vaccinating adults is less effective than vaccinating children because the risk of chronic disease after initial acute infection is highest in the youngest age groups.8 Culturally and linguistically competent strategies were needed at all levels of intervention to successfully implement the HepTLC project. Furthermore, educating health-care practitioners on the public health implications of HBV infection and high-risk groups is necessary. In a recent study, only 49% of primary care providers considered HBV infection to be “somewhat
important” and were less aware of the risks of being a child born to immigrant parents.18 Limitations This analysis was subject to at least three limitations. First, presence of a positive HBsAg was used to indicate chronic infection. New acute infections can also show HBsAg positivity. However, most immigrants from intermediate to high HBV-endemic countries acquired their infections in early childhood, so chronic disease was more likely the case.4,16 Second, attendance at the first follow-up medical appointment was self-reported. Some patients may have misreported their attendance. However, for MCHD clients, appointment status was verified in the EHR. Third, in rare cases, some clients may already have been aware of their HBV status. However, the community health specialist checked each new case in the state communicable disease reporting database, so there was minimal chance of duplicative case entry. CONCLUSION Screening activities increased the number of people aware of their HBV infection status, and more than 90% of chronically infected patients were linked to care through this demonstration project. Efforts to more carefully monitor future medical care, including treatment, are warranted because ongoing medical care is imperative for effective management of HBV.10,19,20 Future research is needed to assess the long-term impact of the current investigation and similar programs on morbidity and mortality. Ultimately, identifying, screening, counseling, and linking infected individuals to care will reduce the morbidity and mortality associated with HBV infection. The work presented here is an evaluation of our testing guidelines and informs our public health practice. Review by an institutional review board was not required.
REFERENCES 1. Goldstein ST, Zhou F, Hadler SC, Bell BP, Mast EE, Margolis HS. A mathematical model to estimate global hepatitis B disease burden and vaccination impact. Int J Epidemiol 2005;34:1329-39. 2. Ott JJ, Ullrich A, Mascarenhas M, Stevens GA. Global cancer incidence and mortality caused by behavior and infection. J Public Health (Oxf) 2011;33:223-33. 3. Eckman MH, Kaiser TE, Sherman KE. The cost-effectiveness of screening for chronic hepatitis B infection in the United States. Clin Infect Dis 2011;52:1294-306. 4. Rossi C, Shrier I, Marshall L, Cnossen S, Schwartzman K, Klein MB, et al. Seroprevalence of chronic hepatitis B virus infection and prior immunity in immigrants and refugees: a systematic review and meta-analysis. PLoS One 2012;7:e44611. 5. Weinbaum CM, Williams I, Mast EE, Wang SA, Finelli L, Waskely A, et al. Recommendations for identification and public health man-
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6. 7. 8.
9. 10.
11. 12. 13.
agement of persons with chronic hepatitis B virus infection. MMWR Recomm Rep 2008;57(RR-8):1-20. Daniels D, Grytdal S, Wasley A. Surveillance for acute viral hepatitis—United States, 2007. MMWR Surveill Summ 2009;58(3):1-27. Kao JH, Chen DS. Global control of hepatitis B virus infection. Lancet 2002;2:395-403. Rossi C, Schwartzman K, Oxlade O, Klein MB, Greenaway C. Hepatitis B screening and vaccination strategies for newly arrived adult Canadian immigrants and refugees: a cost-effectiveness analysis. PLoS One 2013;8:e78548. Ott JJ, Stevens GA, Groeger J, Wiersma ST. Global epidemiology of hepatitis B virus infection: new estimates of age-specific HBsAg seroprevalence and endemicity. Vaccine 2012;30:2212-9. Beckett GA, Ramirez G, Vanderhoff A, Nichols K, Chute SM, Wyles DL, et al. Early identification and linkage to care of persons with chronic hepatitis B virus infection—three U.S. sites, 2012–2014. MMWR Morb Mortal Wkly Rep 2014;63(18):399-401. Mitchell T, Armstrong GL, Hu DJ, Wasley A, Painter JA. The increasing burden of imported chronic hepatitis B—United States, 1974–2008. PLoS One 2011;6:e27717. Luther Consulting, LLC. EvaluationWeb®: Version 5. Carmel (IN): Luther Consulting, LLC; 2013. SAS Institute, Inc. SAS®: Version 9.3 for Windows. Cary (NC): SAS Institute, Inc.; 2011.
14. Multnomah County Health Department. Analysis of arrivals to Multnomah County, Oregon, electronic disease notification (EDN) system. Portland (OR): Multnomah County Health Department; 2014. 15. Office of the United Nations High Commissioner for Refugees. 2015 UNHCR country operations profile—Democratic Republic of the Congo [cited 2015 Nov 17]. Available from: http://www .unhcr.org/cgi-bin/texis/vtx/page?page549e45c366&submit5GO 16. Mast EE, Weinbaum CM, Fiore AE, Alter MJ, Bell BP, Finelli L, et al. A comprehensive immunization strategy to eliminate transmission of hepatitis B virus infection in the United States: recommendations of the Advisory Committee on Immunization Practices (ACIP) part II: immunization of adults. MMWR Recomm Rep 2006;55(RR-16):1-33. 17. Veldhuijzen IK, Toy M, Hahné SJ, De Wit GA, Schalm SW, de Man RA, et al. Screening and early treatment of migrants for chronic hepatitis B virus infection is cost-effective. Gastroenterology 2010;138:522-30. 18. Said A, Jou JH. Hepatitis B vaccination and screening awareness in primary care practitioners. Hepatitis Res Treat 2014;2014:373212. 19. Lok AS, McMahon BJ. Chronic hepatitis B [published erratum appears in Hepatology 2007;45:1347]. Hepatology 2007;45:507-39. 20. Lok AS, McMahon BJ. Chronic hepatitis B: 2009 update. Hepatology 2009;50:661-2.
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Early Identification and Linkage to Care of Foreign-Born People with Chronic Hepatitis B Virus Infection, Multnomah County, Oregon, 2012–2014 Jaime Walters, MPHa Amy Sullivan, PhD, MPHb
ABSTRACT Objective. Hepatitis B virus (HBV) infection is a global health concern, with a large proportion of high-risk individuals unaware of their infection status. People born in countries with medium to high endemicity of HBV should be tested and linked to care. We describe a program that improved identification and linkage to care for refugees and immigrants at the Multnomah County Health Department in Oregon. Methods. We instituted outreach clinics and community referrals and expanded refugee screening to identify foreign-born people at risk for HBV. We obtained data from electronic health records and electronic laboratory reporting, including patient demographics, hepatitis B testing variables, vaccination history, and—for positive cases—risk-factor and linkage-to-care data. All results were entered into an Internet-based data collection tool. For this analysis, we only used results for testing performed from October 2012 through June 2014. Results. We screened 2,087 foreign-born people for HBV infection and identified 77 (4%) people with positive results. HBV infection prevalence varied by site, with 7% of HBV-positive people identified through the outreach and voucher program and 3% identified through refugee screening. Of the 77 people testing positive for HBV, 72 (94%) were successfully linked to care, of whom 68 (94%) attended their first follow-up visit. Conclusion. Implementation of a culturally competent screening program among immigrants and refugees in Multnomah County improved case finding and subsequent linkage to care.
Multnomah County Health Department, Community Epidemiology Services, Portland, OR
a
Multnomah County Health Department, Communicable Disease Services, Portland, OR
b
Address correspondence to: Jaime Walters, MPH, Multnomah County Health Department, Community Epidemiology Services, 426 SW Stark St., 3rd Fl., Portland, OR 97204; tel. 503-988-3406; e-mail . ©2016 Association of Schools and Programs of Public Health
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An estimated 350 million people worldwide are infected with the hepatitis B virus (HBV), resulting in 600,000 annual deaths.1,2 In the United States, more than 2 million people may be chronically infected, although three-quarters of them may not be aware of their infection status, thereby increasing their likelihood of passing the disease to others.3 People infected with HBV may have a self-limiting infection, where they eliminate the virus and have immunity from subsequent reinfection, or may progress to chronic infection that could lead to complications such as cirrhosis, liver failure, and hepatocellular carcinoma.4,5 Although the incidence of acute HBV infection is decreasing, about 43,000 new infections are identified each year in the United States, making early screening and referral to care imperative.5,6 A safe and effective vaccine for HBV prevention has been available in most higher-income countries since the 1980s.7,8 Additionally, the morbidity and mortality associated with HBV infection can be reduced by screening individuals at high risk for infection and by offering appropriately timed antiviral therapy.4,5 However, with the rise in international migration, the number of high-risk immigrants and refugees coming from countries of intermediate and high hepatitis B prevalence has increased substantially.9 HBV-associated sequelae (e.g., cirrhosis and hepatocellular carcinoma) are serious problems in these groups.10,11 Hepatitis B surface antigen (HBsAg) is a marker of chronic infection. Since 2008, the Centers for Disease Control and Prevention (CDC) has recommended that all people in the United States born in geographic regions with HBsAg prevalence $2% (e.g., Asia, Africa, Eastern Europe, the Middle East, and Pacific Islands) be tested for HBsAg and that those infected are linked to medical care and preventive services.5 This group includes immigrants, refugees, asylees, and internationally adopted children born in these areas, regardless of past vaccination status. In 2012, the CDC Division of Viral Hepatitis awarded funds to nine sites through the Prevention and Public Health Fund to implement these recommendations. The Multnomah County Health Department (MCHD) Communicable Disease Services (CDS) was one of these nine grantees (HBV only) in CDC’s Hepatitis Treatment and Linkage to Care (HepTLC) initiative, which promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. (Other jurisdictions did similar work for hepatitis C.) To increase HBV outreach, testing, and linkage to care of foreign-born people, MCHD expanded HBV testing through the
Refugee Medical Assistance (RMA) program and implemented a culturally and linguistically appropriate, community-based referral mechanism. Linkage to care included referral to a primary care provider or specialist for further evaluation, monitoring, and possible treatment of chronic HBV infection. We describe a HepTLC program that improved case finding and subsequent referrals to improve health outcomes for refugees and immigrants in our jurisdiction. METHODS MCHD is Oregon’s largest local public health agency and safety-net provider serving the Portland metropolitan area, which comprises 1,641,036 residents (43% of the state population) and the majority of Oregon’s newly arriving refugees. Expanded refugee screening MCHD operates the RMA program to provide comprehensive health screenings to nearly all of Oregon’s newly arrived refugees (about 1,000 per year). Screening involves a general examination, including nutritional history, immunizations, an emotional distress screening, and laboratory testing for malaria, lead toxicity, parasites, sexually transmitted infections, and tuberculosis. Previously, the RMA program screened about 30% of these refugees (i.e., primarily women of childbearing age) for HBV. Under the Prevention and Public Health Fund program, and augmented with additional grant funding in the second year, CDS staff members supported the RMA program by expanding protocols for HBV testing to include all incoming refugees and coordinated follow-up for RMA clients who screened positive for HBV. A grant-funded community health specialist linked HBsAg-positive refugees to care. For insured people, linkage to care included linkage to the client’s primary care home; for uninsured people, linkage included referral to other clinics or resources. Community referrals The CDS program partnered with local organizations serving foreign-born people to expand HBV testing in two ways. First, a voucher system was created to refer clients from partner organizations to our CDS clinic for free testing. Second, testing was performed at onsite clinics (e.g., apartment complexes and refugee and immigrant organizations) to reach the target populations where they lived, worked, and prayed. This method also helped overcome perceived barriers to testing, such as transportation issues.
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Data sources For incoming refugees screened through RMA, data were available through the electronic health record (EHR). Encounter data for refugee screening visits were obtained electronically. For the outreach and voucher programs, CDS was the referring provider, so all data needed were collected and housed at MCHD (i.e., paper files). Because HBV is a reportable condition in Oregon, cases could also be identified via electronic laboratory reporting. Laboratory reports are automatically downloaded into the Oregon Public Health Epidemiologists’ User System (Orpheus). Public health nurses review reports coming in through electronic laboratory reporting, and investigations are initiated according to state-determined guidelines. Data collection All data (i.e., from EHR, Orpheus, or otherwise) collected as part of HepTLC were entered into an Internet-based data collection tool called EvaluationWeb®.12 This system, provided by CDC to all HepTLC sites and operated by a contracting data coordination
center, was intended for monitoring and evaluation purposes only. Information collected included patient demographics (i.e., age, sex, birth year, country of origin, race/ethnicity, and health insurance status), HBV testing variables (i.e., test date, test result, and laboratory type), whether and when the patient received test results, and if a vaccination history for either HBV or hepatitis A existed. For HBsAg-positive patients, risk-factor information, patient education provided (e.g., alcohol education), linkage to care (i.e., how the patient was linked to care, follow-up appointment date, and whether the patient attended that appointment), and if and what date the patient was reported to surveillance were also collected. Patients self-reported attendance at follow-up appointments. All patients were assigned a unique client identification that contained no protected health information. The data coordination center reviewed data monthly for accuracy, and monthly calls were conducted with the center’s technical specialist. We performed all data analyses using SAS® version 9.3.13
Table 1. Characteristics of foreign-born people with hepatitis B virus infection identified during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a by hepatitis B surface antigen result, Multnomah County, Oregon, October 2012–June 2014
Characteristic Total Sex Male Female Age, in years ,18 18–49 $50 Region of origind,e East Asia and the Pacific Sub-Saharan Africa Eastern Europe and Central Asia South Asia Middle East and North Africa Latin America and Caribbean Health insurance status Yes No/don’t know
Total number tested (percent of total)b
Number testing positive for hepatitis B surface antigen (percent of positive)
Proportion testing positive within group (percentage)
2,087 (100)
77 (100)
4
1,089 (52) 998 (48)
46 (60) 31 (40)
4 3
407 (19) 1,190 (57) 490 (24)
8 (10) 47 (61) 22 (29)
2 4 5
36 27 4 5 5 0
(47) (35) (5) (6) (6) (0)
6 7 6 2 1 0
62 (81) 15 (19)
3 6
P-valuec
0.176
0.105
,0.001 613 410 72 240 470 268
(30) (20) (3) (12) (23) (13)
0.046 1,833 (88) 254 (12)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. b
Percentages may not total to 100 because of rounding.
P-value from Pearson’s χ2 test assessing the significance of differences across groups within characteristics
c
d
World Bank country classification
Excludes 14 people unable to be categorized (i.e., missing, don’t know, or declined) with negative hepatitis B surface antigen results
e
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Table 2. Number and percentage of foreign-born people tested for hepatitis B virus infection, testing positive, and linked to care during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a Multnomah County, Oregon, October 2012–June 2014 Site Total Refugee screeningc Voucher/outreachd
Number tested (percent)
Number testing positiveb (percent)
Number linked to care (percent of those testing positive)
2,087 (100) 1,533 (73) 554 (27)
77 (4) 41 (3) 36 (6)
72 (94) 39 (95) 33 (92)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. b
Statistically significant at p,0.001
Clients who were tested for hepatitis B as part of their comprehensive health screening as incoming refugees
c
Clients who were tested for hepatitis B by returning coupons/vouchers to the Multnomah County Communicable Disease Services clinic or who were tested at outreach sites, including apartment complexes or community centers
d
RESULTS From October 2012 through June 2014, 2,087 people were tested for HBV infection (Table 1). We observed no difference between HBsAg test result and sex or age group (p50.176 and p50.105, respectively). Region of origin was significantly associated with test result (p,0.001). People who tested positive for HBsAg were disproportionately and predominantly from East Asia and the Pacific (6% and 47%, respectively) and subSaharan Africa (7% and 35%, respectively). Individuals without health insurance were twice as likely to screen positive for HBsAg compared with individuals who had health insurance. Of the 2,087 individuals screened, 73% were tested via the refugee screening program, and 27% were tested at outreach clinics or through CDS (Table 2).
A total of 77 people (4%) were positive for HBV infection. Prevalence varied by test site, with 36 (7%) positive results at outreach or CDS clinics and 41 (3%) positive results at refugee screenings (p,0.001). Of the 77 HBV-positive individuals, 72 (94%) were successfully linked to care, 70 (97%) of whom saw a primary care physician. Sixty-eight (94%) individuals attended their first appointment (Table 3). Among those not linked to care, one refused, one moved out of state, and three could not be located. Linkage to care was highest from referrals for refugee screening. All patients were seen for follow-up within 90 days of their positive test (median 5 30, maximum 5 84). All cases were reported to surveillance. A total of 477 individuals who tested HBsAg negative were also hepatitis B core antibody (anti-HBc) p ositive,
Table 3. Test results, counseling, and mechanism for linkage to care for foreign-born people tested for hepatitis B virus infection during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a Multnomah County, Oregon, October 2012–June 2014 Total N (percent)
Variable Number of people tested for hepatitis B virus infection (percent) Number testing positive (percent of tested) Number given results (percent) Number counseled (percent) Number linked to care (percent) Number referred to primary care/set up appointment with primary care physician (percent) Number set up appointment with specialist (percent) Number attended first appointment (percent)
2,087 77 75 75 72 70
(100) (4) (97) (97) (94) (97)
2 (3) 68 (94)
Refugee screeningb N (percent) 1,533 41 41 41 39 37
(73) (3) (100) (100) (95) (95)
2 (5) 38 (97)
Voucher/outreach screeningc N (percent) 554 36 34 34 33 33
(27) (6) (94) (94) (92) (100)
0 (0) 30 (91)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014.
Clients who were tested for hepatitis B as part of their comprehensive health screening as incoming refugees
b
Clients who were tested for hepatitis B by returning coupons/vouchers to the Multnomah County Communicable Disease Services clinic or who were tested at outreach sites, including apartment complexes or community centers c
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Table 4. Hepatitis B core antibody result by hepatitis B surface antigen result in foreign-born people tested for hepatitis B virus infection during the Hepatitis Testing and Linkage to Care (HepTLC) initiative,a Multnomah County, Oregon, October 2012–June 2014 Hepatitis B surface antigen test Hepatitis B core antibody result Total Positive Negative Indeterminate
Total number tested (percent)b 2,087 552 1,534 1
Number testing positive (percent)
(100) (26) (74) (,1)
77 75 2 0
(4) (97) (3) (0)
Number testing negative (percent)b 2,010 477 1,532 1
(96) (24) (76) (,1)
a HepTLC was a Centers for Disease Control and Prevention initiative that promoted viral hepatitis B and hepatitis C screening, posttest counseling, and linkage to care at 34 U.S. sites during 2012–2014. b
Percentages may not total to 100 because of rounding.
indicating a past, cleared infection and immunity (Table 4). Of these 477 individuals, 286 (60%) were from East Asia and the Pacific, 91 (19%) were from sub-Saharan Africa, and the remaining 97 (20%) were from South Asia, Middle East and North Africa, Latin America and Caribbean, and Eastern Europe and Central Asia. Individuals identified via the HepTLC initiative had very few risk factors for HBV infection aside from their country of origin. None of the 77 HBsAg-positive people reported past injection drug use, human immunodeficiency virus positivity, or, in males, male sexual partners. Seven people (9%) were ever a household contact to a person with known HBV (five in the previous 12 months), and three (4%) reported multiple sexual partners (i.e., .1 sexual partner in a six-month period). DISCUSSION Screening of 2,087 foreign-born people through refugee screening or community referrals revealed 77 cases of chronic HBV infection that might otherwise have gone undetected. The majority of people testing HBsAg positive were from regions with the highest HBV prevalence (East Asia and the Pacific and subSaharan Africa). Consistent with one of the goals of the HepTLC initiative (i.e., to increase awareness of HBV infection status for people from intermediate and high HBV-endemic countries and help them obtain linkage to medical care), nearly all people found to be infected with HBV were informed of their test results, given appropriate posttest counseling, and linked to care. Our jurisdiction’s percentage of people linked to care was higher than the linkage-to-care rate of two other larger sites (i.e., New York, New York, and San Diego, California) and consistent with a site of similar size already using refugee screening (i.e.,
Minneapolis-St. Paul, Minnesota).10 Linkage to care was most successful through refugee screening, where incoming people were eligible to receive eight months of health benefits through the state Medicaid program. Only one individual screened through this mechanism refused to be linked to care. Outreach clinics were also successful at linking patients to care. However, as in the New York and San Diego study sites, following up with these individuals proved challenging.10 We found that compared with people identified through refugee screening, more people reached via outreach lacked health insurance. Only two people were found to be positive through direct referrals to CDS, but one could not be located. Both of the patients testing positive from CDS lacked health insurance, making collaborations with other community groups and organizations serving foreign-born populations essential for successful linkage to care. We identified a higher prevalence of chronically infected clients from outreach than through refugee screening. This finding was unexpected but could be explained by variations in refugees from particular countries of origin, which vary from year to year. In 2013, the majority of refugees in Multnomah County came from the Middle East and North Africa, where HBV prevalence is lower than in other regions.14 In 2014, the number of refugees to Multnomah County from sub-Saharan Africa increased, especially from the Democratic Republic of Congo, which has experienced ongoing conflict.15 Concomitantly, HBsAg positivity in refugees increased significantly from 2% in 2012–2013 to 4% in 2014 (p50.02). We found a sizeable proportion of all people tested who were HBsAg negative and anti-HBc positive. This combination is typically indicative of past infection and shows immunity from further infection.4,16 As might be expected, immunity to HBV was highest
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in those regions with the highest seroprevalence of chronic HBV infection (i.e., East Asia and the Pacific and sub-Saharan Africa). The percentage of people immune to HBV infection was lower in lowerseroprevalence regions (e.g., South Asia, Middle East, and North Africa). A recent meta-analysis showed an overall pooled seroprevalence of HBsAg of 9.6 (range: 8.2–11.1); in East Asians and Pacific Islanders, the seroprevalence rose to 13.2 (range: 12.0–14.4).4 Regardless, the seroprevalence estimates mirrored the chronic HBV prevalence in those regions. Even in refugees from lower seroprevalence countries, other studies have shown that screening for chronic HBV infection is cost effective, even at prevalence as low as 0.3%.3,4,17 An additional test, antibody to hepatitis B surface antigen (anti-HBs), can determine immunity from past vaccination (or prior infection, if anti-HBc is not ordered at the same time). Of 2,010 people who tested negative for HBsAg, 1,532 (76%) were found to be susceptible to HBV infection. These individuals could benefit from HBV immunization. Refugees often come to the United States with missing or incomplete vaccination records, and, without testing for anti-HBs, it is possible that vaccination could be offered to people already immune to infection. As such, refugees at high risk for HBV infection are offered vaccine during RMA screening when both surface antigen and core antibody are negative, and no additional testing (e.g., anti-HBs) is performed. However, at CDS, clients are tested for anti-HBs before being offered vaccine. This testing algorithm may result in considerable cost savings. Although the vaccine itself is free to clients in high-risk populations, MCHD pays any associated administrative fees (i.e., nursing fee, injection fee), which cost about $22. This cost can triple if a person needs up to three doses of vaccine. The anti-HBs test only costs about $8. A recent cost-effectiveness analysis of hepatitis B testing strategies in Canadian immigrants found that screening was a reasonably cost-effective approach because vaccinating the entire immigrant cohort would produce a small relative decrease in morbidity and mortality from new chronic infections that might occur. Furthermore, vaccinating adults is less effective than vaccinating children because the risk of chronic disease after initial acute infection is highest in the youngest age groups.8 Culturally and linguistically competent strategies were needed at all levels of intervention to successfully implement the HepTLC project. Furthermore, educating health-care practitioners on the public health implications of HBV infection and high-risk groups is necessary. In a recent study, only 49% of primary care providers considered HBV infection to be “somewhat
important” and were less aware of the risks of being a child born to immigrant parents.18 Limitations This analysis was subject to at least three limitations. First, presence of a positive HBsAg was used to indicate chronic infection. New acute infections can also show HBsAg positivity. However, most immigrants from intermediate to high HBV-endemic countries acquired their infections in early childhood, so chronic disease was more likely the case.4,16 Second, attendance at the first follow-up medical appointment was self-reported. Some patients may have misreported their attendance. However, for MCHD clients, appointment status was verified in the EHR. Third, in rare cases, some clients may already have been aware of their HBV status. However, the community health specialist checked each new case in the state communicable disease reporting database, so there was minimal chance of duplicative case entry. CONCLUSION Screening activities increased the number of people aware of their HBV infection status, and more than 90% of chronically infected patients were linked to care through this demonstration project. Efforts to more carefully monitor future medical care, including treatment, are warranted because ongoing medical care is imperative for effective management of HBV.10,19,20 Future research is needed to assess the long-term impact of the current investigation and similar programs on morbidity and mortality. Ultimately, identifying, screening, counseling, and linking infected individuals to care will reduce the morbidity and mortality associated with HBV infection. The work presented here is an evaluation of our testing guidelines and informs our public health practice. Review by an institutional review board was not required.
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14. Multnomah County Health Department. Analysis of arrivals to Multnomah County, Oregon, electronic disease notification (EDN) system. Portland (OR): Multnomah County Health Department; 2014. 15. Office of the United Nations High Commissioner for Refugees. 2015 UNHCR country operations profile—Democratic Republic of the Congo [cited 2015 Nov 17]. Available from: http://www .unhcr.org/cgi-bin/texis/vtx/page?page549e45c366&submit5GO 16. Mast EE, Weinbaum CM, Fiore AE, Alter MJ, Bell BP, Finelli L, et al. A comprehensive immunization strategy to eliminate transmission of hepatitis B virus infection in the United States: recommendations of the Advisory Committee on Immunization Practices (ACIP) part II: immunization of adults. MMWR Recomm Rep 2006;55(RR-16):1-33. 17. Veldhuijzen IK, Toy M, Hahné SJ, De Wit GA, Schalm SW, de Man RA, et al. Screening and early treatment of migrants for chronic hepatitis B virus infection is cost-effective. Gastroenterology 2010;138:522-30. 18. Said A, Jou JH. Hepatitis B vaccination and screening awareness in primary care practitioners. Hepatitis Res Treat 2014;2014:373212. 19. Lok AS, McMahon BJ. Chronic hepatitis B [published erratum appears in Hepatology 2007;45:1347]. Hepatology 2007;45:507-39. 20. Lok AS, McMahon BJ. Chronic hepatitis B: 2009 update. Hepatology 2009;50:661-2.
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