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Journal of Viral Hepatitis, 2012, 19, e163e169
Examining hepatitis c virus testing practices in primary care
C. V. Almario,1 M. Vega,2 S. B. Trooskin3 and V. J. Navarro2
Department of Internal Medicine, Hospital of the
University of Pennsylvania; Division of Gastroenterology and Hepatology, Department of Internal Medicine, Thomas Jefferson University Hospital; and
Division of Infectious Diseases, Department of Internal Medicine, Hospital of the University of Pennsylvania; Philadelphia, PA, USA
Received July 2011; accepted for publication August 2011
SUMMARY. Prior studies found that hepatitis C virus (HCV)
risk assessment and testing in primary care clinics were
suboptimal. We aimed to determine the actual HCV testing
rate among patients with HCV risk factors and to identify
variables predictive of testing. In order to do so, we performed a prospective cohort study among patients seen in
four urban primary care clinics. At the initial visit, patients
were given a questionnaire that listed HCV risk factors and
they were instructed to check ÔyesÕ or ÔnoÕ if they did or did
not have a risk factor, respectively. Patients then handed
this questionnaire to their physician during their initial visit.
Among those who acknowledged having a HCV risk factor
via the questionnaire, we determined the subsequent HCV
testing rate and calculated adjusted odds ratios (aOR) with
95% confidence intervals (CI) to identify variables predictive
Hepatitis C virus (HCV) is the most common bloodborne
infection in the United States, as 3.2 million individuals are
chronically infected nationwide . Furthermore, 40% of
chronic liver disease is related to HCV, and HCV-associated
end-stage liver disease is the most frequent indication for
liver transplantation . Given the significant morbidity and
mortality associated with HCV, the Centers for Disease
Control and Prevention (CDC) , National Institutes of
Health (NIH) , and American Association for the Study of
Abbreviations: AASLD, American Association for the Study of Liver
Diseases; aOR, adjusted odds ratio; CDC, Centers for Disease Control
and Prevention; CI, confidence interval; COPD, chronic obstructive
pulmonary disease; HCV, hepatitis C virus; HIV, human immunodeficiency virus; NIH, National Institutes of Health; OR, odds ratio;
PCP, primary care physician.
Correspondence: Victor J. Navarro, MD, Division of Gastroenterology
and Hepatology, Department of Internal Medicine, Thomas Jefferson
University Hospital, 132 South 10th Street, Suite 480 Main Building, Philadelphia, PA 19107, USA.
2011 Blackwell Publishing Ltd
of testing. Of the 578 individuals who acknowledged having
a HCV risk factor via the questionnaire, only 8% (46/578)
were tested for HCV within 2 months of their initial visit.
Among those tested, 11% (5/46) had a positive HCV antibody test result. The only variable predictive of HCV testing
after adjusting for confounders was having a specific HCV
risk factor identified and documented in the chart by physicians [16% (26/159) vs 5% (20/419); aOR 4.5, 95% CI
2.19.5]. In summary, 92% of patients with a HCV risk
factor were not tested for HCV in the primary care setting,
and efforts to improve such rates are clearly warranted.
Keywords: hepatitis C virus testing, medical comorbidities,
primary care practice.
Liver Diseases (AASLD)  all recommend HCV testing for
persons at high risk. However, previous studies, most of
which were survey based, showed that HCV risk assessment
and testing in primary care settings were suboptimal .
Shehab et al.  noted that among primary care physicians
(PCPs) surveyed nationwide, only 59% asked all patients
about HCV risk factors. A retrospective chart review by
Trooskin et al.  revealed that PCPs documented a history
(positive or negative) of intravenous drug use and blood
transfusion prior to 1992 for 12% and 2% of patients,
respectively. Furthermore, they also found that of those who
admitted intravenous drug use, only 55% were subsequently
tested for HCV .
Patient care in primary care settings has become
increasingly complex. While the time physicians spent with
patients has increased over the years [12,13], the number of
clinical items addressed per visit also increased . Yet, the
increase in the number of addressed clinical diagnoses
outpaced the increase in visit duration, thereby leading to a
decrease in the amount of time devoted to each clinical item
. Given the increased demands placed on PCPs along
with the fact that most prior studies that examined HCV
testing practices were survey based, we aimed to perform a
C. V. Almario et al.
prospective cohort study to determine the actual rate of HCV
testing among primary care patients with a HCV risk factor
and to identify factors predictive of testing.
MATERIALS AND METHODS
We performed a prospective cohort study among patients
seen at four urban primary care clinics in Philadelphia,
Pennsylvania, from October 2004 to June 2005. Two clinics
were university-based primary care practices (an internal
medicine practice and a family medicine practice) at Thomas
Jefferson University Hospital, while the other two clinics
were federally qualified community health clinics. Each of
the four primary care clinics served a unique population.
The internal medicine university-based practice provided
care for a population of which 45% were African American.
A majority of the internal medicine patients had private
insurance. For the family medicine university-based practice,
60% of the patients were African American and approximately 50% had private insurance. Regarding the community clinics, one served a predominantly Latino population
(85%), of which approximately 25% were undocumented
immigrants. The second community clinic served a predominantly African American population (70%). The
majority of patients receiving care at the two community
health clinics were either uninsured or covered by a Medicaid Health Maintenance Organization.
Our group previously performed a retrospective chart
review among patients seen in the four clinics described
previously. The aim of the prior study was to examine HCV
risk factor ascertainment, testing and referral for treatment,
with particular attention to the role of race and ethnicity
. For our current prospective study, we focused on
examining HCV testing practices and determining factors
predictive of testing. Participants in our current study included patients, 18 years of age or older, who had not been
seen in the clinic for 5 years or more. Individuals were asked
to participate in the study while they were in the waiting
room, and those who agreed to participate were given a HCV
risk factor questionnaire that listed risk factors for HCV. The
questionnaire asked patients whether they ever had any of
the following: a blood transfusion before 1992, an organ
transplant before 1992, long-term dialysis, a spouse or significant other who was diagnosed with HCV, been in prison
or jail for more than 24 h, worked as a healthcare worker
and accidentally been stuck with a needle, injected recreational drugs even if it was just one time or a tattoo or body
piercing (ear piercing not included). At the bottom of the
questionnaire, participants were instructed to check ÔyesÕ or
ÔnoÕ if they did or did not have any of the above HCV risk
factors, respectively. Those who had a HCV risk factor were
told to simply check ÔyesÕ and to not identify their specific
HCV risk factor on the questionnaire. The questionnaire was
made in duplicate with one copy given to the studyÕs personnel. Patients were instructed to hand the other copy of
the questionnaire to their PCP during their initial visit. Of
note, the HCV risk factor questionnaire did not include any
language prompting the PCP to order HCV testing if the
patient acknowledged having a HCV risk factor via the
The charts of all patients who identified themselves as
having a HCV risk factor on the questionnaire were reviewed
2 months after their initial visit by a team of trained chart
reviewers. Demographics collected included age, sex, race/
ethnicity, primary care clinic setting (university-based vs
community), total number of clinic visits within a 2-month
period after the initial visit, insurance status, highest level of
education and annual income. All pre-existing medical
comorbidities documented in the chart were recorded. Anyone with a known prior diagnosis of HCV was excluded from
the study. We checked to see whether the HCV risk factor
questionnaire was present in the chart and determined
whether physicians identified and documented in the chart
the specific HCV risk factor that each patient possessed. We
also determined whether a HCV antibody test was subsequently performed by searching the chart for a HCV antibody
test result or documentation from the physician clearly stating that the patient was referred for HCV antibody testing.
Statistical tests were performed using SPSS 17.0 (SPSS
Inc., Chicago, IL, USA). StudentÕs t-test and the chi-square
test were used to analyse continuous and categorical variables, respectively. When sample sizes for categorical variables were small, the FisherÕs exact test was used in place of
the chi-square test. A P value <0.05 was considered statistically significant. A binary logistic regression model was used to calculate adjusted odds ratios (aOR) with 95% confidence intervals (CI) to find variables predictive of HCV testing. Variables from univariate analysis with a P < 0.20 were included as covariates in the regression model. This cut-off value was chosen so that we could liberally include variables in the model and therefore assess confounding by more variables. This study was approved by the Institutional Review Board of Thomas Jefferson University Hospital. RESULTS Overall, 1848 individuals from four urban primary care clinics agreed to complete the HCV risk factor questionnaire during their initial primary care visit. Of the 1848 individuals who participated, 658 (36%) acknowledged on the questionnaire that they had a risk factor for HCV. On the subsequent chart review 2 months after their initial visit, 58 individuals either had charts with incomplete data or charts that could not be located. We excluded 22 individuals because they had a known prior diagnosis of HCV. Therefore, our study population included 578 patients with a HCV risk factor. Demographic characteristics of the study population are presented in Table 1. Only 46 of 578 (8%) individuals with a HCV risk factor were tested for HCV within 2 months after 2011 Blackwell Publishing Ltd HCV testing in primary care Table 1 Characteristics of the study population e165 Tested for HCV P Variable No (n = 532) Yes (n = 46) Age (years) Sex Male Female Race/ethnicity§ African American Asian Caucasian Latino Other Primary care clinic setting Community University-based Total number of clinic visits Insurance coverage** No Yes HCV risk factor questionnaire present in chart Specific HCV risk factor documented by physician Education levelàà Some high school or less High school degree Undergraduate degree Graduate degree Annual income ($)§§ £15 000 15 00149 999 50 00099 999 100 000 No. of medical comorbidities 3 2 1 0 33.0 ± 12.3 35.8 ± 11.6 0.14* 213 (40) 314 (60) 23 (50) 23 (50) 0.21à 188 (36) 4 (1) 213 (41) 104 (20) 12 (2) 11 (24) 1 (2) 13 (28) 21 (46) 0 (0) <0.01à 194 (37) 338 (64) 1.5 ± 0.8 25 (54) 21 (46) 1.8 ± 0.9 137 (26) 392 (74) 342 (65) 15 (33) 31 (67) 37 (82) 0.02à 133 (25) 26 (57) <0.01à 90 (17) 246 (46) 141 (27) 54 (10) 16 (37) 16 (37) 10 (23) 1 (2) 0.01à 156 (37) 167 (40) 65 (16) 31 (7) 14 (41) 10 (29) 8 (24) 2 (6) 0.50à 30 (6) 58 (11) 123 (23) 321 (60) 6 (13) 6 (13) 12 (26) 22 (48) 0.16à 0.02à <0.01* 0.32à Data are presented as mean ± standard deviation, or n (%). Per cent totals may not equal 100 because of rounding. HCV, hepatitis C virus. *StudentÕs t-test. Not known for five individuals. àChi-square test. §Not known for 11 individuals. Within the 2 months after the initial visit. **Not known for three individuals. Not known for nine individuals. ààNot known for four individuals. §§Not known for 125 individuals. their initial visit. Among those tested, five of 46 (11%) had a positive HCV antibody test result, 39 of 46 (85%) were negative, and two of 46 (4%) had pending results at the time of chart review. When comparing those who were tested for HCV vs those who were not, we found that those tested had a higher proportion of Latinos, were more often seen in the community primary care clinic setting, had more clinic visits during the 2 months after their initial visit and were less educated. 2011 Blackwell Publishing Ltd They were also more likely to have the HCV risk factor questionnaire present in their chart and to have a physician who identified and documented a specific HCV risk factor in the chart. No statistically significant differences were found in regard to age, sex, insurance status, annual income and number of comorbidities. Of the 578 individuals who acknowledged having a HCV risk factor via the questionnaire, only 159 of 578 (28%) had physicians who identified and documented a specific e166 C. V. Almario et al. HCV risk factor in the chart. Twenty-one of 159 (13%) patients had two documented risk factors while 138 of 159 (87%) only had one. Table 2 lists the specific risk factors documented in the chart by physicians and their associated rates of HCV testing. No association was found between HCV testing and the number of identified HCV risk factors, as one of 21 (5%) individuals with two risk factors were tested vs 25 of 138 (18%) of those with one risk factor (P = 0.20). Table 3 presents the rate of HCV testing associated with each medical comorbidity. The only comorbidity with a statistically significant association with HCV testing was hyperlipidemia. All other medical comorbidities were not predictive of HCV testing. Among individuals with 0, 1, 2 or 3 medical comorbidities, the rate of HCV testing was 22 of 343 (6%), 12 of 135 (9%), six of 64 (9%) and six of 36 (17%), respectively (P = 0.16). Table 4 shows the unadjusted and aOR for variables predictive of HCV testing. In our unadjusted analysis, we noted that patients with 3 medical comorbidities were more likely to undergo HCV testing when compared to those without medical comorbidities. However, after adjusting for confounders with a binary logistic regression, no statistically significant difference was seen in HCV testing rates between patients with 0, 1, 2 or 3 medical comorbidities. The only variable that remained predictive of HCV testing after adjusting for confounders was having a physician who identified and documented a specific HCV risk factor in the chart. DISCUSSION The rate of HCV testing among primary care patients with a HCV risk factor was very low, as only 8% underwent HCV HCV risk factor n Tested for HCV Tattoo or body piercing Prior incarceration History of intravenous drug use Blood transfusion before 1992 Healthcare worker with history of accidental exposure Significant other with HCV Long-term kidney dialysis 91/159 (57) 43/159 (27) 19/159 (12) 14/159 (9) 9/159 (6) 9/91 (10) 4/43 (9) 9/19 (47) 1/14 (7) 1/9 (11) 3/159 (2) 1/159 (1) 2/3 (67) 1/1 (100) Table 2 Rate of HCV testing according to HCV risk factor Data are presented as n (%). HCV, hepatitis C virus. Table 3 Rate of HCV testing according to individual medical comorbidities Tested for HCV Medical comorbidity Does not have comorbidity Has comorbidity P Coronary artery disease Hypertension Stroke or seizure disorder Peripheral vascular disease Hyperlipidemia Inflammatory bowel disease Irritable bowel syndrome Gastroesophageal reflux disease Diabetes Thyroid disease COPD or asthma HIV Cancer Psychiatric disorder Arthritis 45/573 40/514 45/566 46/576 36/516 46/573 46/568 42/537 44/562 44/563 39/532 45/572 46/571 40/510 43/550 1/5 (20) 6/64 (9) 1/12 (8) 0/2 (0) 10/62 (16) 0/5 (0) 0/10 (0) 4/41 (10) 2/16 (13) 2/15 (13) 7/46 (15) 1/6 (17) 0/7 (0) 6/68 (9) 3/28 (11) 0.34* 0.66 1.00* 1.00* 0.02* 1.00* 1.00* 0.56* 0.37* 0.34* 0.08* 0.39* 1.00* 0.78 0.48* (8) (8) (8) (8) (7) (8) (8) (8) (8) (8) (7) (8) (8) (8) (8) Data are presented as n (%). HCV, hepatitis C virus; COPD, chronic obstructive pulmonary disease; HIV, human immunodeficiency virus. *FisherÕs exact test. Chi-square test. 2011 Blackwell Publishing Ltd HCV testing in primary care Table 4 Variables predictive of HCV testing Variable Tested for HCV n (%) Unadjusted OR (95% CI) Specific HCV risk factor documented by physician Yes 26/159 (16) 3.9 (2.17.2) No (reference) 20/419 (5) 1 HCV risk factor questionnaire present in chart Yes 37/379 (10) 2.5 (1.15.4) No (reference) 8/190 (4) 1 Primary care clinic setting Community 25/219 (11) 2.1 (1.13.8) University-based 21/359 (6) 1 (reference) No. of medical comorbidities 3 6/36 (17) 2.9 (1.17.8) 2 6/64 (9) 1.5 (0.63.9) 1 12/135 (9) 1.4 (0.73.0) 0 (reference) 22/343 (6) 1 e167 Adjusted OR (95% CI)* 4.5 (2.19.5) 1 1.8 (0.74.5) 1 0.6 (0.21.8) 1 1.7 (0.46.9) 0.9 (0.32.9) 1.3 (0.62.9) 1 HCV, hepatitis C virus; OR, odds ratio; CI, confidence interval. *We used a binary logistic regression model to adjust for age, race/ethnicity, primary care clinic setting (university-based vs community), total number of clinic visits within 2 months of initial visit, HCV risk factor questionnaire presence in chart, documentation of specific HCV risk factor, education level and number of medical comorbidities per individual. Not known for nine individuals. testing. We found that having a specific HCV risk factor identified and documented in the chart by physicians predicted HCV testing. Our study has a number of unique features that differentiate it from prior studies examining HCV testing in primary care settings. Most notable was the prospective design of our study and our focus on actual PCP practices, as we examined individual medical charts. Prior investigators primarily used surveys to study how PCPs identified and managed HCV , but surveys are prone to bias and may not reflect true practices. In fact, our HCV testing rate of 8% is in stark contrast to the 70% of surveyed PCPs who stated that they test all patients with risk factors . This strongly suggests that actual practices differ markedly from surveyed responses. The low rate of HCV testing among our study population was especially surprising given that all PCPs were handed a questionnaire from each patient at the initial visit identifying themselves as having a HCV risk factor. This strongly suggests that HCV testing was not a high priority for PCPs at the initial visit. The low rate may also reflect PCPsÕ unfamiliarity with HCV testing guidelines from national organizations. This is supported by our finding that only 47% and 7% of patients with a history of intravenous drug use and blood transfusion before 1992 were tested for HCV, respectively. These two risk factors are arguably the most important ones for HCV acquisition, and the CDC , NIH , and AASLD  all recommend testing these two cohorts for HCV. Further supporting the idea that PCPs are unfamiliar with HCV testing guidelines was a prior survey 2011 Blackwell Publishing Ltd that found that 42% of PCPs were unaware of the national guidelines regarding HCV testing . Other surveys administered among primary care residents  and family physicians  revealed their insufficient knowledge about HCV testing guidelines and that they often tested for HCV in inappropriate clinical situations. Another unique aspect of our study was our examination of the impact of medical comorbidities on HCV tes ... Purchase answer to see full attachment
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