Abstract
We sought to determine the prevalence of HCV infection and identify factors associated with HCV infection among clients presenting to community-based health settings in Hawai‘i from 2010–2013. An earlier report on this study population covered the period from December 2002 through May 2010. Since 2010, the HCV screening inclusion criteria have been relaxed, and the program has greatly expanded. Clients from 26 community-based sites were administered questionnaires, and were screened for HCV antibodies from January 2010 through April 2013 (N = 8,588). Univariate and multivariate logistic regression analyses were performed. HCV antibody prevalence was 5.9% compared with 11.9% from 2002–2010. Persons aged 45–65 years had the highest HCV antibody prevalence (8.4%) compared with all other age groups. Significant independent variables associated with HCV antibody prevalence were injection drug use, blood transfusion before July 1992, and having an HCV-infected sexual partner. While characteristics associated with HCV infection remained essentially unchanged from those identified in the earlier analysis, the expansion of screening sites and less restrictive inclusion criteria led to a much larger study population and a concurrent decrease in overall HCV antibody prevalence. However, while the highest age-specific prevalence remained the same for both screening periods, the prevalence among younger persons (< 30 years old) doubled (from 2.4% to 4.7%). By expanding the HCV screening program and relaxing the inclusion criteria, a greater number of HCV-infected persons and a greater proportion of younger persons with HCV infection were identified while still maintaining a focus on at-risk individuals.
Introduction
As the most common chronic blood borne pathogen in the United States, the hepatitis C virus (HCV) is a leading cause of liver disease and accounts for more than one-third of all liver transplants.1 Approximately 1.3% of the US population is chronically infected, and without treatment, about half will develop cirrhosis or hepatocellular carcinoma (HCC).2
HCV is transmitted primarily via blood-to-blood contact, with the largest risk factor in the United States being injection drug use (IDU).1 Another established risk factor is having a blood transfusion before July 1992 when blood screening programs were implemented.1 Recently, sexual contact with an HCV-infected partner has been recognized as a risk factor for specific populations including HIV-infected men who have sex with men (MSM).4 Unlike hepatitis A and B, there is no vaccine for HCV, though new and effective treatments are being developed. In December 2013, the Food and Drug Administration approved a new drug, sofosbuvir, which showed high rates (up to 90%) of sustained virologic response.5,6 As chronic infection is often asymptomatic, most infected individuals are unaware and therefore do not seek treatment.
In recent years, there has been a 3-fold increase in HCC incidence, of which about 50% is related to HCV infection decades earlier.1 Approximately 75% of HCV-infected individuals in the United States were born between1945–1965. The high prevalence in this birth cohort is attributed to high rates of IDU in the 1970s–80s and the risk from blood transfusions before 1992.1 Most of these individuals no longer engage in risk-related behavior and have not been tested for HCV. As HCV infection can take decades to present symptoms, the burden is now becoming increasingly apparent.7 The Centers for Disease Control and Prevention (CDC) as well as the US Preventive Services Task Force (USPSTF) recently recognized the importance of screening this age group and amended its recommendations for risk-based HCV testing to include one-time screening for all individuals born between 1945 and 1965.7,8
There has been increasing evidence of an epidemic of HCV infection among younger individuals, especially those who inject drugs. In Massachusetts, an increase in newly reported HCV cases among injection drug users aged 15–24 years was observed from 2002–2009.9 Similar findings have been observed in New York among individuals under 30 years old.10 Increasing rates of HCV infection in this younger cohort require attention and have implications on screening and intervention priorities. Several studies on HCV prevalence have been done in Hawai‘i, but most focused on specific populations—men of Japanese ancestry with HCC,11 HIV-infected patients,12 residents of a homeless shelter,13 and Pacific Islander patients with HCC.14 A population-based case-control study was also conducted to investigate HCV risk factors.15
Since 2002, the Hawai‘i State Department of Health (HDOH) Adult Viral Hepatitis Prevention Program has offered risk-based HCV antibody testing based on CDC recommendations,1,16 and has concurrently collected demographic and behavioral/blood exposure data on all persons screened through the program. In 2010, Porter, et al, conducted a study to determine the prevalence of HCV antibody in Hawai‘i and identify characteristics associated with HCV infection among screening program clients. The study analyzed data from December 2002–May 2010, when the program included 23 test sites, and employed strict screening criteria for the majority of that time period. They found an HCV antibody prevalence of 11.8%.17
Since January 2010, the program expanded to include the HIV/AIDS Early Intervention Services (HEIS) program, which offers HCV antibody testing at substance abuse treatment centers statewide. Clients at HEIS sites account for over 40% of all testing. The purpose of this study was to assess the impact of test site expansion on HCV prevalence estimates as well as demographic and behavioral/blood exposure associations with HCV infection from January 2010–April 2013 using Porter, et al,'s findings as a reference.
Methods
This study analyzed data from three years of HCV data collection efforts conducted at community-based health settings across the state. The total number of participating sites from January 2010 to April 2013 was 26. HEIS represented four of these sites, and all clients from HEIS sites were offered screening for HCV antibody. Clients presenting to the remaining 22 sites were screened individually and considered at risk for HCV infection if they reported at least one of five risk factors previously identified by the CDC:16 an unsterile tattoo or piercing, blood transfusion before July 1992, exposure to blood, sexual contact with an HCV-infected partner, or IDU.
Clients undergoing HCV testing completed a questionnaire prior to testing. Questionnaires collected information on self-reported age, gender, race/ethnicity, and HCV risk factor history. A unique identifier was assigned to each client to link HCV antibody test results. From January 2010 until April 2011, a paper questionnaire was administered, but starting in May 2011, the questionnaire changed to an electronic form that was used for HCV, as well as HIV and HBV, screening. The electronic questionnaire included more items on HIV risks and sexual history; for demographic items, the new questionnaire grouped Native Hawaiian and Pacific Islander ethnicities together, while the previous questionnaire separated them. The items addressing HCV risk factors were unchanged. Prior to May 2011, questionnaires were completed either by a counselor or client; since May 2011, questionnaires were completed by the counselor conducting the interview. Clients with a negative test but positive history of risk factor exposure were encouraged to return for a repeat test. In our analysis the denominator is the number of tests performed since clients may have had multiple tests within our study period.
HCV antibody testing was performed via whole blood laboratory testing with Home Access® finger-stick blood collection kit or Oraquick® HCV Rapid Antibody Test point-of-care kit. Blood specimens from Home Access® test kits were tested for anti-HCV antibody using an enzyme immunoassay (EIA) (Abbott HCV EIA 2.0 or Ortho HCV EIA 3.0). A positive result was determined by either a positive EIA signal-to-cut-off ratio of 3.8 or greater, or a positive EIA signal-to-cut-off ratio of less than 3.8 and a confirmatory positive Recombinant Immunoblot Assay (RIBA).18 The Oraquick® HCV Rapid Antibody Test provides results within twenty minutes utilizing whole blood specimens via finger-stick. For each test performed, the sensitivity is ≥ 95% and the specificity is ≥ 99%.18,19
Demographic characteristics and behavioral/blood exposure factors were analyzed using chi-square tests. Odds ratios and 95% confidence intervals were calculated for each factor. Univariate and multivariate logistic regression analyses were performed, and analyses were stratified by gender. Univariate analyses were performed using EpiInfo, versions 3.5.1 and 7 (CDC, Atlanta, GA); logistic regression analyses were performed using SAS version 9.3 (SAS Institute, Cary, NC). P-values less than or equal to .05 were considered statistically significant. All tests were 2-tailed. The study was approved by the HDOH institutional review board.
Results
From January 2010 through April 2013, 9,107 tests were conducted; only 7.8% of individuals who were offered testing declined. Of the 9,107 tested, 519 (5.7%) had indeterminate or no reported HCV antibody result and thus were excluded. Of the 8,588 records included in the analysis, 508 (5.9%) had positive HCV antibody results. In regards to data collection, 1,623 results came from the old questionnaire before May 2011, while 6,965 came from the new questionnaire. Along with a unique identifier, 13 HDOH sites used a client identification number (ID) to link clients to their medical records. By comparing these records with client IDs (n = 2,006), we estimate that 2.7% of our population consisted of repeat clients. Among the repeat clients, an estimated 3.7% had a positive test result.
Table 1 shows demographic associations with HCV antibody positivity among the study population. Gender and age group differences were statistically significant while ethnicity was not. Men had a significantly higher prevalence compared to women and transgender individuals (OR = 1.45, 95% CI: 1.18–1.77, P-value < .001). HCV antibody prevalence was significantly higher for persons aged 45–64 years [8.4%, P-value < .001]. Individuals under 30 years old had an HCV antibody prevalence of 4.7%. While not statistically significant, Native Americans had the highest and Asians the lowest HCV antibody prevalence.
Table 1.
Demographic characteristics and HCV antibody status of participants screened at community-based health settings, Hawai‘i, 2010–2013
| Variables | HCV Antibody Positive (n=508) Number (%) | HCV Antibody Negative (n=8080) Number (%) | Total Tested | P-value |
| Gender | .0023 | |||
| Men | 364 (6.6%) | 5149 (93.4%) | 5513 | |
| Women | 139 (4.7%) | 2795 (95.3%) | 2934 | |
| Transgender | 1 (1.4%) | 69 (98.6%) | 70 | |
| Not Reported | 4 (5.6%) | 67 (94.4%) | 71 | |
| Total | 508 (5.9%) | 8080 (94.1%) | 8588 | |
| Age Group (in years) | < .001 | |||
| 0–13 | 0 (0.0%) | 0 (0.0%) | 0 | |
| 13–14 | 1 (25.0%) | 3 (75.0%) | 4 | |
| 15–19 | 14 (4.9%) | 273 (95.1%) | 287 | |
| 20–24 | 68 (5.1%) | 1275 (94.9%) | 1343 | |
| 25–29 | 68 (4.4%) | 1485 (95.6%) | 1553 | |
| 30–34 | 65 (5.0%) | 1233 (95.0%) | 1298 | |
| 35–39 | 48 (5.0%) | 904 (95%) | 952 | |
| 40–44 | 54 (6.5%) | 774 (93.5%) | 828 | |
| 45–49 | 67 (8.7%) | 700 (91.3%) | 767 | |
| 50–54 | 47 (7.4%) | 584 (92.6%) | 631 | |
| 55–59 | 40 (9.2%) | 397 (90.8%) | 437 | |
| 60–64 | 19 (8.1%) | 217 (91.9%) | 236 | |
| 65 or older | 16 (8.6%) | 169 (91.4%) | 185 | |
| Not Reported | 1 (1.5%) | 66 (98.5%) | 67 | |
| Total | 508 (5.9%) | 8080 (94.1%) | 8588 | |
| Ethnicity* | .200 | |||
| White | 312 (6.4%) | 4540 (93.6%) | 4852 | |
| Asian | 164 (5.4%) | 2883 (94.6%) | 3047 | |
| Black | 19 (5.5%) | 324 (94.5%) | 343 | |
| Hispanic | 49 (5.8%) | 790 (94.2%) | 839 | |
| Native American | 38 (7.7%) | 453 (92.3%) | 491 | |
| Hawaiiana | 204 (5.6%) | 3412 (94.4%) | 3616 | |
| Total | 786 (6.0%) | 12,402 (94.0%) | 13,188 | |
Ethnicity totals exceed 8,588 as categories were not mutually exclusive.
The new questionnaire combined Hawaiian and Pacific Islander together.
Figure 1 shows HCV antibody prevalence and total number of tests by site. HEIS sites conducted a large percent of tests (42.6%), and HCV antibody prevalence at HEIS sites (6.5%) was not significantly different than all other sites.
Figure 1.
HCV Antibody Prevalence and Total Tests Done by Site, January 2010–April 2013
Table 2 shows unadjusted univariate analysis of behavioral/blood exposure factors for HCV infection. IDU was the behavioral/blood factor most strongly associated with HCV antibody prevalence (OR = 2.40, 95% CI: 1.96–2.94, P-value < .001). Exposure to blood showed a significantly inverse association with HCV antibody prevalence (OR = 0.68, 95% CI: 0.54–0.85, P-value = .001). Getting an unsterile tattoo or piercing was not significantly associated with HCV antibody prevalence (OR = 1.02, 95% CI: 0.83–1.26, P-value = .823).
Table 2.
Univariate analysis of behavioral/blood exposure factors for HCV antibody positivity, among participants screened at community-based health settings, Hawai‘i, 2010–2013
| Variables | HCV Antibody Positive (n=508) Number (%) | HCV Antibody Negative (n=8080) Number (%) | OR (95% CI) | P-value |
| Tattoo or Piercing (Unsterile) | ||||
| Yes | 136 (5.6%) | 2305 (94.4%) | 1.02 (0.83–1.26) | .823 |
| No | 305 (5.4%) | 5293 (94.6%) | 1.00 | — |
| No Data Reported or Unknown | 67 (12.2%) | 482 (87.8%) | — | — |
| Blood Transfusion before July 1992* | ||||
| Yes | 56 (8.2%) | 631 (91.8%) | 1.67 (1.24–2.24) | .001 |
| No | 379 (5.2%) | 6958 (94.8%) | 1.00 | — |
| No Data Reported or Unknown | 56 (17.1%) | 272 (82.9%) | — | — |
| Exposure to Blood (eg, needlestick) | ||||
| Yes | 105 (4.0%) | 2520 (96.0%) | 0.68 (0.54–0.85) | .001 |
| No | 305 (5.8%) | 4938 (94.2%) | 1.00 | — |
| No Data Reported or Unknown | 98 (13.6%) | 622 (86.4%) | — | — |
| HCV-infected Sexual Partner | ||||
| Yes | 98 (6.6%) | 1388 (93.4%) | 1.50 (1.17–1.94) | .002 |
| No | 176 (4.5%) | 3745 (95.5%) | 1.00 | — |
| No Data Reported or Unknown | 234 (7.4%) | 2947 (92.6%) | — | — |
| Injection Drug Use | ||||
| Yes | 144 (11.3%) | 1133 (88.7%) | 2.40 (1.96–2.94) | < .001 |
| No | 363 (5.0%) | 6863 (95.0%) | 1.00 | — |
| No Data Reported or Unknown | 1 (1.2%) | 84 (98.8%) | — | — |
Includes only persons born prior to July 1992
Table 3 shows multivariate logistic regression results when adjusted for all behavioral/blood exposure factors—having an unsterile tattoo or piercing, blood transfusion before July 1992, exposure to blood, sexual contact with an HCV-infected partner, or IDU. All factors except having an unsterile tattoo or piercing were significantly associated with HCV antibody positivity. Having a blood transfusion and IDU demonstrated the strongest association. Gender stratified behavioral/blood exposure factors were also examined (Table 4). For men, IDU, receiving a blood transfusion prior to July 1992, and having an HCV-infected sexual partner were significantly associated with HCV antibody positivity. For women, IDU was significantly associated with HCV antibody positivity (OR = 2.84, 95% CI: 1.61–5.00, P-value <.001), and exposure to blood or needlestick injury had a significant inverse association with HCV antibody positivity (OR = 0.45, 95% CI: 0.24–0.85, P-value = .013). Having an HCV-infected sexual partner (OR = 1.51, 95% CI: 1.10–2.07, P-value = .012) and receiving a blood transfusion prior to July 1992 (OR = 1.92, 95% CI: 1.28–2.89, P-value = .002) were only significant in men.
Table 3.
Multivariate analysisa of behavioral/blood exposure factors for HCV antibody positivity, among participants screened at community-based health settings, Hawai‘i, 2010–2013
| Variables | OR (95% CI) | P-value |
| Tattoo or Piercing (Unsterile) | 1.06 (0.80–1.39) | .700 |
| Blood Transfusion before July 1992 | 1.91 (1.35–2.70) | < .001 |
| Exposure to Blood (eg, needlestick) | 0.66 (0.49–0.89) | .006 |
| HCV-infected Sexual Partner | 1.49 (1.14–1.95) | .004 |
| Injection Drug Use | 1.93 (1.40–2.67) | < .001 |
Each variable in the multivariate analysis is adjusted for all other behavioral/blood exposure variables.
Table 4.
Gender-stratified, multivariate analysisa of behavioral/blood exposure factors for HCV antibody positivity, among participants screened at community-based health settings, Hawai‘i, 2010–2013
| Variables | Men | Women | ||
| OR (95% CI) | P-value | OR (95% CI) | P-value | |
| Tattoo or Piercing (Unsterile) | 0.94(0.68–1.31) | .722 | 1.41(0.84–2.37) | .197 |
| Blood Transfusion before July 1992 | 1.92(1.28–2.89) | .002 | 1.85(0.94–3.65) | .074 |
| Exposure to Blood (eg, needlestick) | 0.74(0.52–1.04) | .084 | 0.45(0.24–0.85) | .013 |
| HCV-infected Sexual Partner | 1.51(1.10–2.07) | .012 | 1.52(0.91–2.56) | .110 |
| Injection Drug Use | 1.70(1.14–2.54) | .009 | 2.84(1.61–5.00) | < .001 |
Each variable in the multivariate analysis is adjusted for all other behavioral/blood exposure variables.
Discussion
HCV antibody prevalence among our tested clients was 5.9%. This is lower than the 11.8% prevalence found by Porter, et al, but still much higher than the 1.6% prevalence estimated for the general US population.1,2 This higher prevalence is expected because, excluding testing at HEIS sites, all clients were identified as having at least one risk factor for HCV infection. Within HEIS sites, 33.2% tested for HCV antibody did not have any risk factors. Thus, HEIS sites captured more clients with no history of risk factors and with a negative HCV antibody result, leading to a lower HCV prevalence compared to the findings of Porter, et al. Even though the previous study was conducted over an eight year period, the study population (3,306) was smaller.17 Inclusion of HEIS sites increased the number of clients receiving HCV antibody testing more than 2-fold in just over three years. While HCV prevalence has been lower in recent years, the increase in testing has effectively identified more HCV antibody positive clients (508) in three years than were identified previously (390) over eight years.17 Increased testing has also been supported by the introduction of the rapid test and electronic questionnaire. However, there are cost challenges in providing treatment for HCV-infected individuals as drug therapy ranges from $70,000 to $170,000,20 and insurance payers may begin to prioritize coverage for treatment based on new recommendations by the American Association for the Study of Liver Disease.21
Persons aged 45–65 years, which includes participants born between 1945–1965, had significantly higher HCV antibody prevalence (8.4%) compared to all other age groups (5.1%), similar to the findings from Porter, et al.17 This is consistent with national findings.8 Recommendations from the USPSTF for one-time screening for individuals born between 1945 and 1965 should ensure that screening tests are covered by most insurance payers under provisions of the Affordable Care Act.8
Changes in the screening protocol and test sites since the study of Porter, et al, led to an increase in the percentage of clients tested who were under 30 years old (from 28% to 37%). These clients had twice the HCV antibody prevalence (4.7%) as those identified in the earlier study period (2.4%).17 While a true increase in HCV prevalence among this younger cohort may have occurred, changes in the screening protocol disallow our ability to make this conclusion. However, an increase may indeed be occurring among younger injection drug users in Hawai‘i, as the statewide syringe exchange program reported an increase of HCV antibody prevalence in its clients under 30 years old, from 18.4% in 2011 to 28.6% in 2012.22 An increase in drug use and sharing of equipment has been observed in other states, and law enforcement data showed the number of heroin initiates annually in the United States increased 1.8 times in 2009 compared to 2002.9
Overall, men had the highest HCV antibody prevalence, followed by women and then transgender individuals. Porter, et al, found the highest prevalence among transgender individuals followed by men and then women.17 The observed difference may be due in part to the small population (0.8%) who identified as transgender in this study. Previous studies observed that men have a higher prevalence of HCV infection than women especially among injection drug users, noting higher lifetime rates of IDU and substance use disorders in men.23 Native Americans had the highest HCV antibody prevalence among ethnic groups, whereas Asians had the lowest. While not significant, this finding is consistent with the most recent CDC surveillance data.24
While all HCV behavioral/blood exposure factors—except for having an unsterile tattoo or piercing—were significantly associated with HCV antibody positivity, the magnitude of the odds ratios were lower than what was found in the previous study. IDU still had the strongest association and was significant for both men and women; however, our OR was much lower than that found by Porter, et al, (1.9 and 13.6, respectively).17 Having a blood transfusion before July 1992 was also significantly associated with HCV antibody positivity, but after gender stratification remained significant for men only.
Having an HCV-infected sexual partner was significantly associated with HCV antibody positivity but after gender stratification, remained significant only among men; similar to findings from the earlier Hawai‘i study. While the risk of HCV transmission through sexual contact is believed to be low, this could represent an important risk for MSM.25 Recent evidence has shown increasing incidence of HCV infection for MSM who are also HIV infected.25
Having an unsterile tattoo or piercing was not significantly associated with HCV antibody positivity. Of note, the CDC classifies individuals with a history of tattooing or piercing as “persons for whom routine testing is of uncertain need.”26 Needlestick injury was found to have a significant inverse association with HCV antibody positivity, and it remained significant for women only after gender stratification. Porter, et al, showed similar magnitudes of association. It is possible that being a healthcare worker may have confounded the results. A previous study looking at blood exposures and HCV infection among emergency responders found that these workers had a high rate of blood exposures, but HCV infection was not significantly associated with blood exposure.27 Another study found a protective effect among healthcare workers when socioeconomic and environmental factors were not taken into account and these may also have confounded our results.28
While iatrogenic transmission is the leading cause of HCV infection globally and accounts for the majority of cases in Egypt, the country with the highest HCV infection prevalence, 29,30 iatrogenic transmission is not considered a major population-based risk factor for HCV infection in the United States, where injection drug use has consistently been identified as the leading risk factor for past and current HCV infection.7,29,31
This study has several limitations. The population was not randomly selected, hence selection bias may have occurred. Our results therefore may be considered anecdotal and are not generalizable to the population at-large. Secondly, this study only detected the presence of HCV antibodies, which indicates previous exposure to HCV, not necessarily active infection. Still, 50%–80% of antibody positive individuals are chronically infected.2 Also, some repeat clients were considered separate participants for analytic purposes. However, the estimated percentage of repeat clients was low at 2.7%, with only 3.7% of those clients having a positive test result. This is similar to the study of Porter, et al, that estimated 4.0% repeat clients with 1.5% of repeat clients having positive test results.17 Finally, 5.7% of the questionnaires collected were excluded due to missing or inconclusive HCV antibody test results.
Missing information could have lowered the power of the analysis. However, demographic questions had over 95% completion, and the completion of behavioral/blood exposure factor questions ranged from 86.3% (HCV-infected sexual partner) to 98.6% (IDU). An analysis was done for the study population who answered all five behavioral/blood exposure factor questions. The findings were similar to the total study population's results; therefore missing information seems not to have significantly impacted the results. Also, our behavioral/blood exposure multivariate analysis was not adjusted for age or ethnicity, which may have confounded our results.
Changes to the questionnaire after April 2011 may also have affected the results. Having the counselor complete the new questionnaire resulted in greater completion rates and less missing information. However, this change in survey instrument and interview style presents potential for information and mode biases since clients may be less inclined to reveal their behavioral history to a counselor. Also, changes to the ethnic categories between questionnaires could make ethnic comparisons problematic.
Conclusion
Our study shows that a relaxed screening protocol, leading to expanded screening for HCV, has effectively increased the number of clients tested while still remaining concentrated on a relatively high prevalence population. While the behavioral/blood exposure factor associations found were lower in magnitude than those identified by Porter, et al, they are consistent with national findings. Use of the rapid test and electronic questionnaire has supported expanded testing by improving the ease, costs, and completeness of HDOH's screening efforts. Questions on referral and linkage to care were added to the HDOH questionnaire after our study was completed. Hopefully they will provide more insight on HCV treatment in Hawai‘i. Meanwhile, clinicians should continue to identify patients at risk for HCV, such as IDU, and offer screening to individuals born between 1945 and 1965 to ensure appropriate testing and treatment.
Acknowledgements
We gratefully acknowledge Jeremy Porter for data analysis and guidance, and Peter Whiticar, STD/AIDS Prevention Branch, Hawai‘i State Department of Health, for program support. We also acknowledge the staff of all the community-based health agencies included in this report for their participation.
Conflict of Interest
None of the authors identify a conflict of interest.
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