a b s t r a c t

Introduction: The US Preventive services Task Force recommends one-time screening of the 1945-1965 birth cohort (baby boomers) for hepatitis C (HCV) infection. New York State legislation mandates screening of baby boomers for HCV in most patient care settings except the emergency department (ED). This cross-sectional study explores baby boomer knowledge of HCV, prevalence of HCV infection, and linkage to care from a large urban ED. Method: Patients participated in a researcher-administered structured interview and were offered an HCV screening test. If HCV antibody reactive, a follow-up clinic appointment was made within 6 weeks. Reminder telephone calls were made a week before the appointment. Attendance at the follow-up appointment was considered successful linkage to care.

Results: A total of 915 eligible patients were approached between October 21, 2014, and July 13, 2015. A total of 427 patients participated in the structured interview; 383 agreed to an HCV rapid test. Prevalence of HCV antibody re- activity was 7.3%. Four patients were successfully linked to care. General knowledge about HCV was fair. Misconcep- tions about transmission were apparent. Beliefs that “if someone is infected with HCV they will most likely carry the virus all their lives unless treated” and that “someone with hepatitis can look and feel fine” were significantly asso- ciated with agreement to testing.

Conclusions: Better linkage to care is needed to justify HCV screening in the 1945-1965 birth cohort in this particular ED setting. Linkage to care from the ED is challenging but can potentially be improved with specific measures includ- ing simplified screening algorithms and supportive resources.

(C) 2015

Introduction

Approximately 3.2 million individuals in the United States are chronically infected with hepatitis C virus (HCV) [1]. Of those with chronic infection, 20% to 30% will develop cirrhosis over 20 to 30 years if untreated [2,3]. Since 2007, deaths from HCV infection have exceeded deaths from HIV infection in the United States [4]. There has beena par- adigm shift in treatment options for HCV infection with direct acting an- tivirals that now make cure the realistic goal for most patients with chronic HCV infection [5].

? Sources of support: This was an unfunded study. OraQuick Hepatitis C Virus Rapid An- tibody Test kits were provided free of charge by Orasure Technologies, Inc.

* Corresponding author at: Infectious Disease Office, NYU School of Medicine, 462 First Ave, NBV-16S 5-13, New York, NY 10016. Tel.: +1 347 255 7853; fax: +1 212 263 7389.

E-mail address: [email protected] (W.E. Allison).

Since August 2012, the 1945-1965 birth cohort (baby boomers) have been targeted by the Centers for Disease Control and Prevention (CDC) for HCV screening for numerous reasons, including high overall HCV prevalence estimated at 3.3%, the highest prevalence of HCV infection in the non-Hispanic black population, and a lower number needed to screen to prevent 1 HCV-related death compared to other age-based co- horts, for example, 1945 to 1970 [6]. More than three-quarters (77%) of all adult HCV infections in the United States are found within the 1945- 1965 birth cohort, but 60% of those infected with HCV in this age group are unaware of their status. According to prediction models, targeted screening within this population will identify more than 800 000 new cases and avoid 120 000 deaths [6-8].

The US Preventive Services Task Force supported the CDC recom- mendation of 1-time screening of baby boomers in June 2013 with a grade B recommendation. Together, these recommendations are funda- mental to achieving HCV prevention goals and directing a national focus on clinical preventive services that can optimize HCV diagnosis and linkage to care and treatment. On January 1, 2014, New York State

http://dx.doi.org/10.1016/j.ajem.2015.12.072

0735-6757/(C) 2015

mandated by law screening for HCV of all baby boomers receiving inpa- tient and primary care services at hospitals and all patients receiving primary care services from physicians, physician assistants, and nurse practitioners regardless of setting. Notably, the mandate excludes the emergency department (ED), although HCV screening for baby boomers in this setting is encouraged [9].

A recent study in an urban ED in Alabama, USA, showed high accept- ability of HCV testing (88%) and high prevalence (11%) of HCV antibody reactivity among 2323 baby boomers offered opt-out testing [10]. Of HCV antibody-reactive patients, 88.2% had confirmatory HCV RNA poly- merase chain reaction testing performed and chronic HCV infection was confirmed in 68%. In that study, slightly more than half of patients (54%) identified with chronic HCV infection attended a follow-up appoint- ment with a liver specialist for care. Another recent study tested 2028 adults (18 years of age or older) for HCV antibody in an urban ED setting in California, USA [11]. This study found an overall prevalence of HCV antibody of 10.3%. However, among baby boomers, the prevalence was higher at 13.7%. In addition, overall, 180 (67%) of 267 had confirma- tory RNA testing with chronic HCV infection confirmed in 126 (70%) of

180. Forty-five percent of those with chronic HCV infection received a

clinic appointment, and the attendance rate was 24% (30/126).

In light of the exclusion of mandatory testing for HCV infection in EDs from New York State legislation and the potential for high preva- lence of unrecognized infection as noted in other urban EDs, our study aimed to ascertain the Level of knowledge about HCV infection among baby boomers, prevalence of HCV antibody reactivity, and the effective- ness of linkage to definitive care among patients presenting to a large public, urban ED in New York City.

Methods

Study setting and population

This was a cross-sectional study at Bellevue Hospital Center (BHC), the oldest continually operating hospital in the United States with a commitment to health care provision regardless of the ability to pay. El- igible study participants consisted of patients born between 1945 and 1965 presenting to BHC ED for care. Exclusion criteria for participation were as follows: (1) refusal to participate when approached; (2) refusal or inability to sign a consent form; (2) an individual triaged as category 1 or 2, who by definition had a life-threatening emergency that preclud- ed study involvement; (3) inability to successfully negotiate use of a telephone interpreter, for example, due to hearing difficulties; (4) a pre- senting complaint that could be categorized as a mental health prob- lem; and (5) individuals in New York City Police Department or Department of Corrections custody.

The institutional review board of BHC and the affiliated New York University Langone Medical Center approved the study. All subjects underwent an informed consent process and were provided with a study information sheet and the CDC information sheet on HCV testing in baby boomers. Participants were able to withdraw from the study at any time for any reason.

Study protocol

Recruitment occurred in 4-hour blocks of time from 8 AM to 8 PM on all days of the week between October 21, 2014, and July 13, 2015. A maximum of 4 recruitment blocks occurred per day, and patient recruit- ment within each block was capped at 10 patients. At the beginning of each recruitment block, a list of all the adult patients in the ED was generated, and every second patient who fulfilled the inclusion criteria was selected starting with longest length of stay in the ED. Two hours into each 4-hour block, the patient list was reprinted, and the random- ization scheme was repeated excluding patients approached during the preceding 2 hours. If all patients were approached before the end of 2 hours, a second frame of alternate patients fitting the inclusion

criteria was generated using the same print out, starting with the next eligible patient.

Eligible consenting patients took part in a researcher-administered questionnaire at the end of which they were offered an HCV antibody rapid test. Telephone interpreters were used as needed. Participation in the study ended if a patient declined the test or had a nonreactive HCV antibody rapid test. Patients with a reactive HCV antibody test were counseled appropriately, and a clinic appointment was offered within 28 days of the test result, if possible and if not the next available appointment beyond 28 days. Patients were contacted a week before their appointment and were offered an alternative date and time if they were unable to attend. Attendance at this first clinic appointment was interpreted as successful initial linkage to care. Nonattendance at the appointment resulted in a follow-up telephone call to ascertain if care had been obtained elsewhere and, if not, to offer a second appoint- ment. Follow-up to confirm attendance at a second-offered appoint- ment was not performed as part of this study protocol.

Assuming an approximate prevalence of 10% of HCV among a popu- lation size of 44 000 unique baby boomers who have a Bellevue Hospital ED visit each year, a sample size of 381 was calculated to assure that the empiric estimate was within 3% of the true prevalence (true prevalence being between 7% and 13% at a 95% Confidence level).

Study instruments and diagnostic testing

The patient questionnaire was developed based on the knowledge of HCV portion of the Hepatitis C Follow-up Survey carried out during the National Health and Nutrition Examination Survey from 2001 to 2008 [12]. An expert panel consisting of 2 infectious disease physicians and 2 emergency medicine physicians assessed the interview scripts for content relevance, language, and structure, and it was piloted on 81 pa- tients. The patient interview consisted of 3 sections: sociodemographic factors, knowledge of HCV, and acceptability of testing. Hepatitis C virus knowledge was ascertained via either a “true or false” or “yes/no/don’t know” response to a series of statements about HCV transmission and health effects. One question about HCV cure was on a 5-point Likert scale (from 1, never, to 5, always). All interview questions were closed except 1 open-ended question asking participants for their reason for a “no” response to a question about whether they would accept an HCV test if it were offered to them.

Testing for HCV antibody was done using the OraQuick HCV Rapid Antibody test (OraSure Technologies, Bethlehem, PA). This test uses fingerstick or venipuncture whole blood giving a result within 20 mi- nutes. It is Food and Drug Administration approved for Point-of-care testing with a sensitivity and specificity equivalent to laboratory tests even when antibody levels are low [13].

Data management and statistical analysis

Data were entered into a Research Electronic Data Capture database hosted by New York University [14]. Research Electronic Data Capture is a secure, Web-based application designed to support data capture for research studies. Data were analyzed in August 2015 using IBM SPSS Version 17 statistical software [15]. Standard descriptive statistics were obtained. The significance of comparisons between groups was assessed using a ?² test or Fisher exact test for small proportions at a significance level of P <= .05. Odds ratios (ORs) and 95% confidence inter- vals (CIs) were used as measures of association. Open responses were analyzed qualitatively to identify common themes emerging from the wording of the responses. Missing data were missing at random and minimal and were, therefore, dealt with by listwise/pairwise deletion.

Results

Between October 21, 2014, and July 13, 2015, 915 eligible patients fulfilling the inclusion criteria were approached. A total of 427 patients

participated in the structured interview with 383 patients agreeing to both the interview and HCV testing and 44 patients agreeing to the in- terview only. This corresponded to 41.9% of eligible patients approached participating in both the interview and HCV testing. Table 1 summa- rized participant characteristics.

Prevalence of HCV antibody reactivity was 7.3% (28/383 patients). Of the 28 HCV antibody-positive patients, 14 were given a follow-up ap- pointment within 28 days as per the study protocol. Seven patients were given appointments within 29 to 38 days due to high clinic vol- umes and lack of provider availability for appointment slots. Of the 7 pa- tients who were not given an appointment, 5 refused an appointment when offered; 1 patient was recruited during the weekend and could not be contacted by telephone on the next weekday to receive an ap- pointment; and for 1 patient, the reason an appointment was not given was not recorded. Of the 5 patients who refused an appointment, 2 preferred to follow-up with their primary care provider, 1 was moving out of state, and 2 were undomiciled and did not provide reasons for re- fusal. Table 2 shows the geographical diversity of regions of birth of non-US-born participants.

Of the 21 patients provided appointments, only 7 patients (19%)

were linked to care. Two had an undetectable HCV RNA and thus no chronic HCV infection, 1 person was started on HCV treatment (12 weeks of ledipasvir/sofosbuvir), and 1 person attended their first ap- pointment but not a subsequent one and at the study conclusion had not commenced treatment. Of the remaining 17 patients who were given an appointment, follow-up telephone calls were possible for 12. It was not possible to contact 5 patients given an appointment–4 of them were undomiciled and had no contact telephone, one of them gave a relative’s contact number and the relative was not in touch with them. Of the 12 patients able to be contacted by telephone, contact was only established with 4 patients despite repeated attempts. Of 4 of these successfully contacted patients, 2 confirmed that they would at- tend their appointment. Of the remaining 2, 1 stated that they would not attend as they were waiting for their health insurance to be ap- proved and 1 stated that they were unlikely to attend as they expected to be incarcerated at the time of the appointment.

Patient responses to knowledge questions about HCV are shown in Table 3. Most respondents recognized the natural history and complica- tions of HCV. Most respondents recognized the blood-borne risk factors for HCV. Some misconceptions about transmission were apparent. Less than one-third of respondents identified the baby boomer birth cohort as being at greater risk for HCV infection than other age groups. More than half of participants thought that a vaccine exists for HCV. Lack of knowledge about the curability of HCV infection was reflected in the Likert scaled responses to the question “how often do treatments

Table 1

Patient participant characteristics

		n (%)
Sex	Male	249 (58)
	Female	178 (42)
Place of birth	USA	151 (35.3)
	Other	275 (64.4)
	Missing data	1 (0.3)
No. of years in the United States if	0-10 y	52 (19)

born outside the United States 11-20 y 75 (28)

>= 21 y 145 (53)

Education level High school diploma and above 262 (61) No high school diploma or less 164 (38) Missing data 1 (1)

Primary language English 260 (61)

Spanish 128 (30)

Other 138 (32)

Employment Employed 148 (35)

Table 2

Region of birth of non-US-born participants

Region n (%)

Central and South America 152 (55.1)

The Caribbean 32 (11.6)

Sub-Saharan Africa 25 (9.1)

Northern Africa 8 (2.9)

Western Asia 2 (0.7)

Eastern Asia 10 (3.6)

Southern Asia 17 (6.2)

South East Asia 9 (3.1)

Europe 11 (6.2)

CIS 3 (1.1)

Missing data 1 (0.4)

Abbreviations: CIS, Commonwealth of Independent States corresponding to the former Soviet Union.

available today cure hepatitis C” with only 81 (19%) of participants an- swering correctly “most of the time.”

Believing the statement “if someone is infected with hepatitis C virus, they will most likely carry the virus all their lives unless treated” to be true was significantly associated with agreeing to have an HCV rapid test when offered (P = .045; OR, 0.32; 95% CI, 0.11-0.96). Believing the statement “someone with hepatitis can look and feel fine” to be true was also signif- icantly associated with agreeing to have an HCV rapid test when offered (P = .014; OR, 0.24; 95% CI, 0.069-0.80). There was no association with answering any other HCV knowledge question correctly with agreement to have an HCV rapid test. The most common Reasons for refusal to have an HCV screening test included not wanting to have a finger prick, want- ing to leave the ED and already having had an HCV screening test.

Discussion

Our results show a high prevalence of 7.3% of HCV antibody reactiv- ity in the 1945-1965 birth cohort presenting to a large urban public ED. Linkage to care from the ED was poor. Ultimately, only 1 patient was commenced on HCV treatment by the conclusion of the study. Our prev- alence results reflect the findings of others studies (in Alabama and Cal- ifornia) reporting linkage to care following baby boomer screening for HCV in the ED setting [10,11]. However, our linkage to care rates were much lower. A linkage to care rate of greater than 80% has recently been demonstrated with HCV screening in the 1945-1965 birth cohort in the inpatient setting in South Texas [16]. In another recent report, those at risk for HCV infection were screened in 5 Primary care settings in Philadelphia, Pennsylvania, and baby boomers represented 62.6% of those chronically infected with HCV [17]. The linkage to care rate in this ambulatory care setting was 62%. The health care setting may influ- ence the rate of linkage to care, and the ED environment may prove par- ticularly challenging for linking patients to care.

The following may explain the poor linkage to care in our study. A substantial number of baby boomers with HCV antibody reactivity also had unstable housing and could not be contacted. Besides not hav- ing a telephone, numerous barriers to accessing health care services exist for undomiciled patients, including lack of health insurance and low literacy [18]. Furthermore, we did not immediately test antibody- reactive patients for HCV RNA to confirm the diagnosis. Having this test result pending or known may have influenced patients’ decisions to attend their appointment. This highlights an important component of the care cascade for HCV screening and linkage to care: reflex to HCV RNA testing for all HCV antibody-positive results. This presents ad- ministrative and Logistical challenges at the laboratory level and may not be possible for all institutions.

Given the large proportion of participants who were foreign born, it has to be considered if this may have influenced the study results. There are no

Unemployed/retired/unable to work

275 (64)

published data on the prevalence of HCV infection following screening

specifically in foreign-born baby boomers in the United States or in the

Missing data 4 (1)

1945-1965 birth cohort in the countries of origin of the foreign-born

Table 3 Responses to HCV knowledge questions in patients born 1945 to 1965
	True, n (%)	False, n (%)	Don’t know, n (%)	Missing, n (%)
If someone is infected with HCV, they will most likely carry the virus all their lives unless treated.	261 (61)	56 (13)	110 (26)	0
Hepatitis C can cause the liver to stop working.	298 (70)	26 (6)	103 (24)	0
Hepatitis C can lead to liver cancer.	245 (57)	35 (8)	140 (33)	7 (2)
Someone with hepatitis C can look and feel fine.	267 (62)	78 (18)	80 (19)	2 (1)
You can get hepatitis C by getting a blood transfusion from an infected donor.	331 (78)	32 (7)	61 (14)	3 (1)
You can get hepatitis C by shaking hands with someone who has hepatitis C.	66 (15)	287 (67)	72 (17)	2 (1)
You can get hepatitis C by kissing someone who has hepatitis C.	161 (38)	154 (36)	110 (25)	2 (1)
You can get hepatitis C by having sex with someone who has hepatitis C.	254 (60)	73 (17)	98 (22)	2 (1)
You can get hepatitis C by being born to a woman who had hepatitis C when she gave birth.	250 (59)	56 (13)	119 (27)	2 (1)
You can get hepatitis C by being stuck with a needle or sharp instrument that has hepatitis C infected blood on it.	350 (82)	22 (5)	50 (12)	5 (1)
You can get hepatitis C by working with someone who has hepatitis C.	82 (19)	278 (65)	64 (15)	3 (1)
You can get hepatitis C by sharing needles used for injecting drugs even if only once many years ago.	351 (82)	22 (5)	51 (12)	3 (1)
People born from 1945 to 1965 are more likely to have hepatitis C than people born before or after those years.	133 (31)	117 (28)	172 (40)	5 (1)
There is a vaccine that can be used to prevent people from getting infected with the HCV.	223 (52)	56 (13)	144 (34)	4 (1)
Hepatitis C is curable.	218 (51)	91 (21)	114 (27)	4 (1)
New medications have become available in the past 3 years that have made hepatitis C easier to treat.	282 (66)	19 (4)	122 (29)	4 (1)
Correct responses for each question are indicated in boldface; percentages are rounded to whole numbers.

participants in this study. The high proportion of foreign-born baby boomers in our study is not unexpected given the location of the ED in a city that has a large immigrant population. The geographic location of the place of birth of most participants was in Central and South America (Latin America) and the Caribbean. Data on HCV prevalence in these re- gions are limited, but a recent meta-analysis reported a pooled regional prevalence of HCV antibody in injecting Drug users, noninjecting drug users, men who have sex with men, sex workers, and prison inmates to be 49%, 4%, 3%, 2%, and 12.5%, respectively [19]. Unfortunately, this meta- analysis did not assess HCV seroprevalence in the general population.

The third most common geographical place of birth for study partic- ipants was sub-Saharan Africa. Similarly to Latin America, data on HCV prevalence in Africa are sparse. A recent meta-analysis reports on the seroprevalence of HCV in sub-Saharan Africa [20]. This analysis included 213 studies from 33 different countries, and the pooled HCV seropreva- lence across all identified cohorts was 2.98%. There was considerable re- gional variation in HCV seroprevalence ranging from 0.91% in southeast Africa to 6.76% in central Africa. A subanalysis of cohorts defined as low risk (the general population and inpatients and outpatients not at high risk for HCV) had a pooled HCV seroprevalence of 11.87%.

In addition, a study in Texas examined health beliefs and comorbid- ities associated with appointment maintaining behavior in adults with HCV and HIV infection and found that health beliefs, psychiatric illness, and HIV coinfection were independently associated with missed ap- pointments [21]. We did not collect such data, but given cultural differ- ences in health beliefs that can exist, it is possible in our largely immigrant population that health beliefs may have influenced appoint- ment keeping behavior; this warrants further investigation.

This study has limitations. Because the reliability of self-reported data is dependent on the completeness and integrity of participant responses and the quality of responses is affected by participant understanding of the questions asked, a more labor-intensive and time-consuming process of having the questionnaires administered by researchers in an interview format was used [22]. Despite this, some questions were not answered resulting in missing data, although this was minimal. In addition, the ma- jority of recruitment occurred between 8 AM and 8 PM Monday to Friday with limited recruitment at weekends. Characteristics of patients present- ing to the ED vary by time of the day. Not recruiting consistently across days of the week and times of the day may have influenced our results. Fi- nally, this study was conducted in a single institution in a urban public hospital, and so, the findings may not be generalizable to other institu- tional settings such as nonacademic or Rural settings.

Conclusion

The low linkage to care rate in this study does not support targeted screening of the 1945-1965 birth cohort for HCV section in this ED

setting. Although the prevalence of HCV antibody reactivity in baby boomers screened was high, better linkage to care and higher numbers of baby boomers with confirmed chronic HCV infection are needed to justify screening in this ED. Linkage to care must be improved and spe- cific measures to improve linkage to care in this ED warrants further in- vestigation. As was found with screening for HIV infection, we believe that screening for HCV infection in the ED makes an important contribu- tion to achieving chronic HCV infection prevention goals. Moreover, the contribution that EDs can make to public health initiatives including screening for infectious diseases is recognized [23,24]. To successfully contribute, multiple factors will need to be addressed.

The perception of ED providers that such screening is not part of acute care provision was previously encountered with HIV screening in the ED and may be similarly encountered with implementation of HCV screening [25,26]. Health care provider education and ancillary support (eg, dedicated point-of-care testers and care coordinators to as- sist with follow-up) is essential to overcoming this barrier. Previous studies with HIV screening have demonstrated that, with education, ED clinicians acknowledge the importance of screening in the ED as a public health measure; we believe that this will also apply to HCV screening [27,28]. In addition, care coordinators may facilitate linkage to care from the ED setting. Significant financial barriers to HCV screen- ing in the ED setting in the United States exist, particularly the Centers for Medicare and Medicaid Services decision to exclude EDs from reim- bursement for HCV screening [29]. Additional factors to be considered include targeted education to foreign-born groups within the baby boomer cohort to increase knowledge of their risk of HCV and its cur- ability with new drugs and, finally, simplification of HCV screening algo- rithms to include reflex testing for HCV RNA after antibody reactivity.

Acknowledgments

The authors thank Alexander Arispe, Martha Harrison, Sumit Kumar, Samantha Maliha, Carl Preiksaitis, Jonathan Steinberg, and Xiangyu Xie for assistance with HCV point-of-care testing. The authors additionally thank OraSure Technologies, Inc, for provision of OraQuick Hepatitis C Virus Rapid Antibody Test kits free of charge.

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