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Research Article|Articles in Press, 100077

Screening for Hepatitis C Among Community Health Center Patients by Ethnicity and Language Preference

Open AccessPublished:February 03, 2023DOI:https://doi.org/10.1016/j.focus.2023.100077

      Highlights

      • Hepatitis C virus related liver disease is a leading cause of death among Latinos.
      • Community health centers serve high proportion of Latinos and an important setting.
      • Latino-English preferred patients had lower HCV screening rates versus other groups.
      • Understanding of how language preference impacts screening disparities is needed.

      ABSTRACT

      Introduction

      Hepatitis C Virus (HCV) is associated with high morbidity and mortality—chronic liver disease is a leading cause of death among Latinos in the United States. Screening for HCV in community health center (CHC) settings, who serve disproportionate percentage of Latinos, is essential to eradication. We assessed HCV screening disparities in adults served by CHCs by ethnicity and language preference.

      Methods

      This was an observational cohort study spanning 2013-2017 of adults born 1945-1965 in the ADVANCE EHR dataset. Our exposure of interest was race/ethnicity and language preference (non-Hispanic white, Latino-English preferred, Latino-Spanish preferred). Our primary outcome was the relative hazard of HCV screening, estimated using multivariate Cox proportional hazards regression.

      Results

      A total of 182,002 patients met study criteria and included 60% non-Hispanic whites, 29% Latino-Spanish preferred, and 11% Latino-English preferred. In total, 9% received HCV screening and 2.4% were diagnosed with HCV. Latino-English preferred patients had lower rates of screening compared to both non-Hispanic whites and Latino-Spanish preferred (5.5% vs 9.4% vs 9.6%). Compared to non-Hispanic whites, Latino-English preferred had lower hazards of HCV screening (aHR=0.56, 95% CI 0.44-0.72) and Latino-Spanish preferred had similar hazards of HCV screening (aHR=1.11, 95% CI 0.88-1.41).

      Conclusions

      We found that in a large CHC network, adult Latinos who preferred English had lower hazards of HCV screening compared to non-Hispanic whites, while Latinos who preferred Spanish had similar hazards of screening as non-Hispanic whites. Overall prevalence of HCV screening was low. Further work on the role of language preference in HCV screening is needed to better equip primary care providers to provide this recommended preventive service in culturally relevant ways.

      Keywords

      INTRODUCTION

      Hepatitis C virus (HCV) affects 2.4 million people in the United States and new HCV infections have tripled in recent years, 1 conjointly with the opioid crisis and rise of injection drug related infections. HCV is associated with high morbidity and mortality2, 3 impacting Latino populations disproportionately. 4-6 Chronic liver disease is a leading cause of death among Latinos in the United States (US), and Latinos experience a higher rate of HCV related deaths than non-Hispanic whites (6.8 vs 4.5 per 100,000). 7 Published studies report screening in Latino populations remains low, and multiple barriers exist for HCV screening. 6,8,9 The role of Spanish-language preference on health care utilization and outcomes compared to English preference varies by setting and service. 10-13 Community health center (CHC) settings are key to HCV screening efforts as many older, low-income Latino patients receive care in CHCs. 14
      Prior studies have identified disparities in HCV screening rates through surveys15,16 or registry data which may be subject to underreporting. Electronic health records (EHR) may provide additional details of screening disparities and opportunities to target interventions along the HCV treatment cascade; however, most studies using EHR data are limited to local settings, and few examine language preference. 8,9,17 Using a multi-state EHR dataset of CHCs, we evaluated whether there were differences in HCV screening rates between non-Hispanic white, Latino-English language-preferring, and Latino-Spanish language-preferring adults.

      METHODS

      Study Population

      We performed a retrospective cohort study of Latino and non-Hispanic white adults who were seen at CHCs between 2013-2017 in the ADVANCE (Accelerating Data Value Across a National Community Health Center Network) clinical data research network in 21 states. 18 Queries and data tables for analyses were standardized in the PCORnet common data model version 3.1 from the ADVANCE data warehouse, which includes specific deduplication protocols. We defined the eligible population as patients born between 1945-1965 (thus meeting the USPSTF 2013 guideline) whose first encounter in the CHC network occurred during the observation period beginning 2013, when the HCV screening policy was updated. Observation spanned from first visit until screening or censoring (death or end of study period). We excluded patients with an existing HCV diagnosis (diagnosis codes: ICD 070.41, 070.44, 070.51, 070.54, 070.70, 070.71, B17.10, B17.11, B18.2, B19.20, B19.21) at observation start.

      Measures

      Outcome: We defined our primary outcome as relative hazard of HCV screening test during the study period. We also determined the prevalence of a new HCV diagnosis during the study period by noting whether the individual had a new HCV diagnosis code after observation start.
      Independent variable: Our primary independent variable was a composite of three mutually exclusive ethnicity and language preference groups: non-Hispanic white, Latino-Spanish language preferred, Latino-English language preferred. Ethnicity and language were based on patient self-reported clinic registration data.
      Covariates: We adjusted for the following potential confounders: age, sex, insurance status at visits during the study period (all public; all private; public and private; no insurance), substance use disorder from encounters and diagnosis ICD9/10 codes excluding tobacco and nicotine, type I or II diabetes diagnosis (to indicate obtaining periodic bloodwork), and number of primary care visits during the study period (proxy for general healthcare utilization).

      Statistical Analysis

      We conducted descriptive analyses of patient characteristics overall and by ethnicity/language groups including prevalence of HCV screening and HCV diagnosis. For our outcome, we used Cox proportional hazards models to estimate covariate-adjusted hazard ratios (aHR) of receipt of HCV screening between ethnic-language groups. We used a proportional hazards approach because we were interested in whether there were differences in time to screening in addition to hazards of screening. Of the 180,053 observations used in the final model, 165,540 were censored at recorded death, end of study period, or date of disenrollment; 1,662 had a recorded death date before receipt of screening. Non-Hispanic white patients were considered referent group and robust standard errors were estimated to account for clustering of patients within clinics. Analyses were conducted using Stata version 15 and R version 4.1.3 with two-sided testing and type I error set at 5%. This study was approved by the Institutional Review Board of Oregon Health & Science University.

      RESULTS

      There were 182,002 eligible patients across 21 states. The average age was 61.9 years (SD 3.89), with 54% female sex. Patients were predominantly non-Hispanic white (60.2%), with 28.8% Latino-Spanish preferred and 11.0% Latino-English preferred (see Table 1).
      Table 1Description of the ADVANCE sample by race, language preference
      No. (%)
      Ethnicity/Language Groups
      OverallNon-Hispanic whiteLatino: Preferring EnglishLatino: Preferring Spanish
      Characteristic(n=182002)(n=109368)(n=19982)(n=52382)
      Age at first

      encounter (mean(SD))
      61.90 (3.89)61.86 (3.92)61.53 (3.84)62.12 (3.85)
      Age group, years
      50-541583 (0.9)1095 (1.0)189 (0.9)299 (0.6)
      55-5963412 (34.8)38546 (35.2)7645 (38.3)17221 (32.9)
      60-6476389 (42.0)45219 (41.2)8376 (41.9)22794 (43.5)
      65-6935729 (19.6)21998 (20.1)3289 (16.5)10442 (19.9)
      70-734889 (2.7)2780 (2.5)483 (2.4)1626 (3.1)
      Female sex98353 (54.0)56546 (51.6)10681 (53.5)31126 (59.4)
      Insurance
      Never Insured35414 (19.5)19087 (17.4)3957 (19.8)12370 (23.6)
      Some Private35764 (19.7)24273 (22.1)3737 (18.7)7754 (14.8)
      Some Public101057 (55.5)59733 (54.5)11196 (56.0)30128 (57.5)
      Some Public and Private9767 (5.4)6545 (6.0)1092 (5.5)2130 (4.1)
      Screened for HCV
      Hepatitis C virus
      16462 (9.0)10342 (9.4)1092 (5.5)5028 (9.6)
      HCV
      Hepatitis C virus
      Diagnosis
      4305 (2.4)3328 (3.0)655 (3.3)322 (0.6)
      SUD
      Substance Use Disorder
      17260 (9.5)13949 (12.7)1966 (9.8)1345 (2.6)
      FPL
      Federal Poverty Level
      <138%99381 (54.6)49546 (45.2)12447 (62.3)37388 (71.4)
      >=138%29388 (16.1)21710 (19.8)2961 (14.8)4717 (9.0)
      Missing53233 (29.2)38382 (35.0)4574 (22.9)10277 (19.6)
      Visits Per Year
      <150566 (27.8)33391 (30.5)5614 (28.1)11561 (22.1)
      1-359350 (32.6)35696 (32.6)6369 (31.9)17285 (33.0)
      3-531110 (17.1)16825 (15.3)3370 (16.9)10915 (20.8)
      5-1027276 (15.0)14645 (13.4)3045 (15.2)9586 (18.3)
      10+13700 (7.5)9081 (8.3)1584 (7.9)3035 (5.8)
      Age At HCV Diagnosis
      50-549 (0.0)8 (0.0)1 (0.0)0 (0.0)
      55-591284 (0.7)939 (0.9)281 (1.4)64 (0.1)
      60-642135 (1.2)1724 (1.6)215 (1.1)196 (0.4)
      65-69761 (0.4)563 (0.5)149 (0.7)49 (0.1)
      70-73116 (0.1)94 (0.1)9 (0.0)13 (0.0)
      Not Diagnosed177697 (97.6)106310 (97.0)19327 (96.7)52060 (99.4)
      a Hepatitis C virus
      b Substance Use Disorder
      c Federal Poverty Level
      In total, 9% had an HCV screening test, and 2.4% were diagnosed with HCV during the study period. In the unadjusted analysis, Latino-English preferred patients had lower rates of HCV screening than non-Hispanic whites and Latino-Spanish preferred (5.5% vs 9.4% vs 9.6%, p<0.001). After adjustment, Latino-English language preferred patients had lower hazards of HCV screening than non-Hispanic whites (aHR=0.56, 95% CI=0.44-0.72), while Latino-Spanish language preferred patients had similar hazards of HCV screening (aHR=1.11, 95% CI=0.88-1.40) (Table 2, Figure 1).
      Table 2Adjusted Relative Hazard of Receipt of Hepatitis C Virus screening test
      Patients included in the time to event analysis were required to have entered the study population during the study period and not have a screening at their first visit.
      Patient GroupHR Estimate (95% CI)
      Adjusted Hazard Ratio
      Adjusted for: age category, female sex, insurance, visits per year, diabetes diagnosis, and substance use disorder
      Latino English Speaking0.56 (0.43, 0.72)
      Latino Spanish Speaking1.11 (0.88, 1.40)
      Non-Hispanic whiteRef
      Unadjusted Hazard RatioLatino English Speaking0.61 (0.47, 0.79)
      Latino Spanish Speaking1.08 (0.81, 1.45)
      Non-Hispanic whiteRef
      1 Patients included in the time to event analysis were required to have entered the study population during the study period and not have a screening at their first visit.
      2 Adjusted for: age category, female sex, insurance, visits per year, diabetes diagnosis, and substance use disorder
      Figure 1:
      Figure 1Kaplan-Meier plots for HCV screening completion by Race/Ethnicity-Language (Non-Hispanic White, Latino-English language preferred, Latino-Spanish language preferred)
      Figure note: The proportion screened at each timepoint is among patients who have not yet been screened or censored.

      DISCUSSION

      In a large multi-state cohort of established CHC patients, we found low HCV screening prevalence (9%), but slightly higher than national average HCV diagnosis rates (2.4% vs 1%).16 We also found significant HCV screening disparities by ethnicity and language preference. Our population's HCV screening prevalence is lower than national estimates based on the National Health Interview Survey (17.3% in 2017), 9 and consistent with prior estimates of CHC screening prevalence amongst a smaller network (8.3% of 61,000 eligible). 19 Other studies reveal variability in HCV screening rates in CHCs, 8,9,20 which warrants further investigation.
      We also found that Latinos who preferred Spanish had similar rates and hazards of screening compared to non-Hispanic white, but Latinos who preferred English had lower rates and hazards of HCV screening. This was surprising as we hypothesized that Spanish-preferring Latino patients would have lower screening rates than English-preferring patients, as prior studies have shown with regards to access to health services and utilization, 2,10 HIV prophylaxis awareness, 21 and use of physician services. 22 However, we now have increasing evidence that in our practice- based research network, Spanish-preferring patients often utilize preventive services more than non-Hispanic whites and English-preferring Latinos. 11,12,23 One explanation may be that heightened attention to Spanish preferred patients in CHCs, which have additional community, cultural and language engagement resources, facilitate trust between CHC providers and Spanish speaking patients, leading to increased adherence to screening recommendations, as other screening evaluations in our network suggest. 24,25 Organizational differences in care settings (e.g., variability in support staff such as bilingual navigators) have been shown to explain differences in receipt and understanding screening mammography results across ethnic groups. 26 It's also important to note that these were patients seeking care at CHCs, as opposed to general populations, which might also explain our findings. Further exploration into why English preferring Latinos had lower rates of screening is required.

      Limitations

      There are several limitations of the analyses. Screening as opposed to diagnostic testing for HCV is difficult to ascertain in our dataset. Our definition of screening is subject to misclassification bias if patients received the test outside the EHR network or received the test prior to cohort inception, which we mitigated by limiting the sample to patients whose first visit in the network occurred during the observation period. We also have evidence that the majority of patients seen in our network tend to receive all their care within the network. 27,28 Second, this is an observational study that may be subject to unmeasured confounding. This analysis did not adjust for social determinants of health such as education level, or provider level factors that might explain differences we observed. We also recognize that the USPSTF guidelines have since been updated to include universal screening for all adults29—our findings remind us that expanding screening initiatives without addressing underlying inequities in access to screening and subsequent treatment may worsen disparities in care. 8

      CONCLUSIONS

      In a nationally representative cohort of CHC patients, we found low rates of HCV screening overall, and significant disparities in the hazards of HCV screening by language preference amongst Latinos. Further work examining language preference is needed to better equip primary care providers to implement HCV screening in culturally relevant ways.

      ACKNOWLEDGMENTS

      Acknowledgements: This work was conducted with the Accelerating Data Value Across a National Community Health Center Network (ADVANCE) Clinical Research Network (CRN). OCHIN leads the ADVANCE network in partnership with Health Choice Network, Fenway Health, and Oregon Health & Science University. ADVANCE is funded through the Patient-Centered Outcomes Research Institute (PCORI), contract number RI-OCHIN-01-MC. The research presented in this paper is that of the authors and does not reflect the official policy of the NIH.
      Funding: National Institute on Aging; Grant number: R01AG056337; Recipient: John Heintzman; National Institute on Drug Abuse; Grant number: 1K23DA053390-01A1; Recipient: Brian Chan
      Conflict of Interest Statement: The authors declare that there are no conflicts of interest
      Funding: National Institute on Aging; Grant number: R01AG056337; Recipient: John Heintzman
      National Institute on Drug Abuse; Grant number: 1K23DA053390-01A1; Recipient: Brian Chan
      No financial disclosures were reported by the authors of this paper
      Credit Statement: Brian Chan MD MPH: conceptualization, methodology, formal analysis, investigation, writing – original draft, project administration; David Ezekiel-Herrera MS: conceptualization, methodology, software, data curation, formal analysis, investigation, writing- review & editing, visualization; Steffani R. Bailey PhD: conceptualization, methodology, investigation, writing- review & editing; Miguel Marino PhD: conceptualization, methodology, software, formal analysis, investigation, writing- review & editing, supervision, resources, funding acquisition, project administration; Jennifer A. Lucas PhD, MPH: methodology, formal analysis, data curation, investigation, writing -review & editing, resources, project administration; Sophia Giebultowicz MS: methodology, software, validation, data curation writing-review & editing; Erika Cottrell PhD, MPP: conceptualization, resources, writing-review and editing, supervision, project administration; Joe Carroll MD: conceptualization, methodology, investigation, writing-review & editing; John Heintzman MD MPH: conceptualization, methodology, investigation, writing- review & editing, project administration, resources, supervision, funding acquisition.
      Preliminary results of this work were presented virtually at the California, Hawaii, Northwest Society of General Internal Medicine (SGIM) regional meeting January 2022.

      REFERENCES

      1. Ryerson AB, Schillie S, Barker LK, Kupronis BA, Wester C. Vital Signs: Newly Reported Acute and Chronic Hepatitis C Cases - United States, 2009-2018. MMWR Morbidity and mortality weekly report. Apr 10 2020;69(14):399-404. doi:10.15585/mmwr.mm6914a2
      2. Ly KN, Hughes EM, Jiles RB, Holmberg SD. Rising Mortality Associated With Hepatitis C Virus in the United States, 2003-2013. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America. May 15 2016;62(10):1287-1288. doi:10.1093/cid/ciw111
      3. Chou R, Dana T, Fu R, et al. Screening for Hepatitis C Virus Infection in Adolescents and Adults: Updated Evidence Report and Systematic Review for the US Preventive Services Task Force. JAMA: the journal of the American Medical Association. Mar 2 2020;doi:10.1001/jama.2019.20788
      4. Rodriguez-Torres M. Latinos and chronic hepatitis C: a singular population. Clin Gastroenterol Hepatol. May 2008;6(5):484-90. doi:10.1016/j.cgh.2008.02.036
      5. Rodriguez-Torres M, Jeffers LJ, Sheikh MY, et al. Peginterferon alfa-2a and ribavirin in Latino and non-Latino whites with hepatitis C. The New England journal of medicine. Jan 15 2009;360(3):257-67. doi:10.1056/NEJMoa0805062
      6. Turner BJ, Taylor BS, Hanson J, et al. High priority for hepatitis C screening in safety net hospitals: Results from a prospective cohort of 4582 hospitalized baby boomers. Hepatology. Nov 2015;62(5):1388-95. doi:10.1002/hep.28018
      7. Scaglione S, Kliethermes S, Cao G, et al. The Epidemiology of Cirrhosis in the United States: A Population-based Study. J Clin Gastroenterol. Sep 2015;49(8):690-6. doi:10.1097/mcg.0000000000000208
      8. Kim NJ, Locke CJ, Park H, Magee C, Bacchetti P, Khalili M. Race and Hepatitis C Care Continuum in an Underserved Birth Cohort. J Gen Intern Med. Oct 2019;34(10):2005-2013. doi:10.1007/s11606-018-4649-6
      9. Turner BJ, Rochat A, Lill S, et al. Hepatitis C Virus Screening and Care: Complexity of Implementation in Primary Care Practices Serving Disadvantaged Populations. Ann Intern Med. Dec 17 2019;171(12):865-874. doi:10.7326/M18-3573
      10. DuBard CA, Gizlice Z. Language spoken and differences in health status, access to care, and receipt of preventive services among US Hispanics. American journal of public health. Nov 2008;98(11):2021-8. doi:10.2105/AJPH.2007.119008
      11. Heintzman J, Bailey SR, Cowburn S, Dexter E, Carroll J, Marino M. Pneumococcal Vaccination in Low-Income Latinos: An Unexpected Trend in Oregon Community Health Centers. Journal of health care for the poor and underserved. 2016;27(4):1733-1744. doi:10.1353/hpu.2016.0159
      12. Heintzman JD, Bailey SR, Muench J, Killerby M, Cowburn S, Marino M. Lack of Lipid Screening Disparities in Obese Latino Adults at Health Centers. American journal of preventive medicine. Jun 2017;52(6):805-809. doi:10.1016/j.amepre.2016.12.020
      13. Heintzman J, Hwang J, Quinones AR, et al. Influenza and pneumococcal vaccination delivery in older Hispanic populations in the United States. Journal of the American Geriatrics Society. Dec 2 2021;doi:10.1111/jgs.17589
      14. National Association of Community Health Centers. Community Health Center Chartbook accessed: 1/25/22, https://www.nachc.org/research-and-data/research-fact-sheets-and-infographics/2021-community-health-center-chartbook/
      15. Rosenberg ES, Rosenthal EM, Hall EW, et al. Prevalence of Hepatitis C Virus Infection in US States and the District of Columbia, 2013 to 2016. JAMA Netw Open. Dec 7 2018;1(8):e186371. doi:10.1001/jamanetworkopen.2018.6371
      16. Hofmeister MG, Rosenthal EM, Barker LK, et al. Estimating Prevalence of Hepatitis C Virus Infection in the United States, 2013-2016. Hepatology. Mar 2019;69(3):1020-1031. doi:10.1002/hep.30297
      17. Geboy AG, Nichols WL, Fernandez SJ, Desale S, Basch P, Fishbein DA. Leveraging the electronic health record to eliminate hepatitis C: Screening in a large integrated healthcare system. PloS one. 2019;14(5):e0216459. doi:10.1371/journal.pone.0216459
      18. DeVoe JE, Gold R, Cottrell E, et al. The ADVANCE network: accelerating data value across a national community health center network. J Am Med Inform Assoc. Jul-Aug 2014;21(4):591-5. doi:10.1136/amiajnl-2014-002744
      19. Cook N, Turse EP, Garcia AS, Hardigan P, Amofah SA. Hepatitis C Virus Infection Screening Within Community Health Centers. J Am Osteopath Assoc. Jan 2016;116(1):6-11. doi:10.7556/jaoa.2016.001
      20. Bian J, Schreiner AD. Population-based screening of hepatitis C virus in the United States. Curr Opin Gastroenterol. May 2019;35(3):177-182. doi:10.1097/MOG.0000000000000520
      21. Mansergh G, Herbst JH, Holman J, Mimiaga MJ. Association of HIV pre-exposure prophylaxis awareness, preferred Spanish (vs. English) language use, and sociodemographic variables among Hispanic/Latino men who have sex with men. Annals of epidemiology. Mar 2019;31:8-10. doi:10.1016/j.annepidem.2019.01.003
      22. Derose KP, Baker DW. Limited English proficiency and Latinos' use of physician services. Medical care research and review: MCRR. Mar 2000;57(1):76-91. doi:10.1177/107755870005700105
      23. Heintzman J, Kaufmann J, Lucas J, et al. Asthma Care Quality, Language, and Ethnicity in a Multi-State Network of Low-Income Children. Journal of the American Board of Family Medicine: JABFM. Sep-Oct 2020;33(5):707-715. doi:10.3122/jabfm.2020.05.190468
      24. White RO, Osborn CY, Gebretsadik T, Kripalani S, Rothman RL. Health literacy, physician trust, and diabetes-related self-care activities in Hispanics with limited resources. Journal of health care for the poor and underserved. Nov 2013;24(4):1756-68. doi:10.1353/hpu.2013.0177
      25. Heintzman JD, Ezekiel-Herrera DN, Quinones AR, et al. Disparities in Colorectal Cancer Screening in Latinos and Non-Hispanic Whites. American journal of preventive medicine. Feb 2022;62(2):203-210. doi:10.1016/j.amepre.2021.07.009
      26. Kenny JD, Karliner LS, Kerlikowske K, Kaplan CP, Fernandez-Lamothe A, Burke NJ. Organization Communication Factors and Abnormal Mammogram Follow-up: a Qualitative Study Among Ethnically Diverse Women Across Three Healthcare Systems. J Gen Intern Med. Oct 2020;35(10):3000-3006. doi:10.1007/s11606-020-05972-2
      27. Huguet N, Kaufmann J, O'Malley J, et al. Using Electronic Health Records in Longitudinal Studies: Estimating Patient Attrition. Medical care. Jun 2020;58 Suppl 6 Suppl 1:S46-S52. doi:10.1097/MLR.0000000000001298
      28. O'Malley JP, O'Keeffe-Rosetti M, Lowe RA, et al. Health Care Utilization Rates After Oregon's 2008 Medicaid Expansion: Within-Group and Between-Group Differences Over Time Among New, Returning, and Continuously Insured Enrollees. Medical care. Nov 2016;54(11):984-991. doi:10.1097/MLR.0000000000000600
      29. Screening for Hepatitis C Virus Infection in Adolescents and Adults: Recommendation Statement. American family physician. Sep 15 2020;102(6):363-366.

      Conflict of Interest Statement

      The authors declare that there are no conflicts of interest
      No financial disclosures were reported by the authors of this paper