2. M. Rotily et al.
elements converge: there is a clear need for knowledge concern- had had more than two. Among those who had not had a positive
ing the screening practices of GPs and factors underlying the screen during the last 12 months, 55% had not prescribed a
decision to prescribe screening tests. screening test during the 4 preceding weeks. Of those who had
had a positive screening test for at least one patient during the last
For human immunodeficiency virus (HIV) infection, it has
12 months, 29% had not prescribed a screening test during the 4
been demonstrated that patient knowledge, attitude toward and
preceding weeks. Conversely, among the GPs who had had
perception of the disease as well as personal behavior patterns
positive tests for more than 2 patients during the last 12 months,
are closely related to screening and management practices [16].
15% had not prescribed a test during the 4 preceding weeks,
There is however little data in the literature pertaining to these
28% had prescribed one or two and 58% had prescribed more
questions in HCV [17, 18]. It has been demonstrated in dialysis
than two (P < 0.0001).
patients, that systematic screening for hepatitis C is a widespread
but diversely implemented practice [19]. The purpose of our study Factors associated with screening practices are presented in
was to describe the knowledge, opinions and practical attitude of table I. GPs who were under 40 years of age, who practiced in
general practitioners in France concerning hepatitis C screening the Bouches-du-Rhône department, who had a mixed practice
and to identify characteristic features associated with regular (private-salary), who saw more than 20 patients per day, who
prescription of screening tests by these general practitioners. had tested themselves for HCV, who never practiced acupunc-
ture, and who proposed HIV screening tests were the GPs who
more frequently prescribed HCV screening tests. GPs who had
provided care for at least one drug abuser during the preceding
Material and methods 4 weeks prescribed HCV tests more often than those who had not.
Inversely, GPs who feared they would be penalized due to HCV
The study population was composed of general practitioners with screening tests appeared to prescribe such tests less often. Finally,
private practices in the French departments of Alpes-Maritimes, Vaucluse, there was no significant relationship between counseling use of
and Bouches-du-Rhône. A random sample was taken from the telephone condoms and prescription of HCV screening tests (table I).
book lists for general practice and general medicine orientation home-
opathy and/or acupuncture (n = 4102). Potential risk factors leading to HCV screening tests are
presented in table II. Tests were proposed to two groups of
Questionnaires were prepared by a panel of hepatitis C experts and
by general practitioners, taking into account the recommendations of the
patients in priority: intravenous drug abusers and HIV-infected
legal authorities and the guidelines developed during the conferences on patients. However, 9% and 7% of the GPs stated they do not
hepatitis C held in 1997 and 1999 [20-22]. Intravenous and pernasal propose tests for these categories of patients respectively; 39%
drug abuse, blood transfusion before 1991, and history of penal stated they never or rarely propose HCV screening tests for
incarceration were considered in 1999 to be the principal risk factors for pernasal drug abuseres. For patients who had had a blood
HCV infection in addition to the following risk groups: patients with even transfusion before 1991, who had either elevated ALT levels, or
moderately elevated transaminase levels, patients infected by the hepati-
tis B virus or the HIV, sexual partners of an HCV carrier. We widened our
were known to have hepatitis B virus infection, 14% to 19% of the
search for other possible factors of transmission which are not recom- GPs proposed HCV screening tests occasionally or never. For
mended by the conferences for routine practice, notably history of surgery patients with a history of major surgery or endoscopy, 60% and
or endoscopy. One hundred one closed-choice items were tested in a 74% of the GPs respectively proposed tests occasionally or never.
pilot phase conducted with the participation of 5 GPs working outside the Practices concerning search for risk factors, e.g. regular or
geographic region of the study. Six trained female inquirers then occasional intravenous drug use, blood transfusion, history of
conducted phone interviews with the GPs in the study population between
May and June 1999. On average, the interviews lasted 13 minutes. Each
major surgery or endoscopy, are also presented in table II. A
phone number was called 6 times between 9 a.m. and 7 p.m. at different search for risk factors at consultation was not significantly
hours and different days. Among the 609 GPs in the random sample, correlated with prescription of HCV screening tests during the 4
12% were not within the target population (no medical practice, retired, weeks preceding the study.
no longer in practice, hospital physician) and 14% could not be reached
by phone. Among the 451 GPs who could be contacted, 68% agreed to More than one-third of the GPs underestimated the amplitude
participate. In all, 317 were interviewed. Sixteen questionnaires were of the HCV epidemic in France and 18% of them stated they did
excluded because of non-response to more than 25 items or incoherent not know the magnitude of the epidemic; 74% of the GPs
responses. The study population retained for analysis thus included 301 underestimated the risk of progression from infection to chronic
general practitioners. hepatitis while 49% and 66%, respectively overestimated the risk
The chi-square test was used to test correlations between qualitative of progression from chronic hepatitis to cirrhosis and from
variables. The standardized adjusted residuals method was used to cirrhosis to hepatocellular carcinoma (table III). On univariate
identify cells contributing significantly to the chi-square test. Odds ratio analysis, these levels of knowledge were not or weakly correlated
and 95% confidence intervals were calculated to quantify the power of the with screening practice during the last 4 weeks. Analysis of
relationships between the different variables studied and the prescription
of a hepatitis C screening test within the last 4 weeks. Confounding factors adjusted residuals only retained that GPs who estimated the risk
were identified with logistic regression using SPSS version 9.0T [23]. All of progression from chronic hepatitis to cirrhosis correctly
variables demonstrating significance at p < 0.20 were retained for the apparently prescribed screening tests more often than those who
initial model. The final model was obtained using the step-by-step over or under estimated the risk or did not respond to the
descending method. The fit of the final model was evaluated with the question.
Hosmer-Lemershow test. All first order interactions were identified and
tested. Outlying residuals exhibiting a distribution beyond 2 standard For questions concerning medical management of patients
deviations were excluded from the final model. infected with the HCV virus, 69% and 95% of GPs respectively felt
that interferon alone or in combination with ribavirine is effective
(table IV). Three-quarters of the GPs also felt that adverse effects
associated with interferon are important and 40% agreed with
Results the opinion that patients often interrupt interferon treatment and
refuse liver biopsy. In the opinion of a minority of the GPs,
Thirty-nine percent of the GPs had not prescribed a screening patients adhere well to interferon treatment. The GPs had a more
test during the 4 preceding weeks, 34% had prescribed one or negative opinion concerning patient behavior for liver biopsy,
two and 27% had prescribed more than two. Thirty-seven percent refusal of treatment, and adherence to the prescribed treatment
of the GPs had not ordered a test with a positive result within the for intravenous drug abusers than for the other patients. The rate
last 12 months, 38% had had one or two positive tests and 25% of non-response for these questions was high. For example, 53%
262
3. Factors related to screening of hepatitis C virus in general medicine
Table I. − Number of screening tests offered in the past four weeks in relation to the characteristics of the general practitioner.
None 1-2 tests > 2 tests Total P
n = 116 n = 103 n = 82 n = 301
Age 0.01
< 40 years 13 (23) 21 (37) 23 (40) 57
≥ 40 years 103 (42) 82 (34) 59 (24) 244
Gender 0.18
Female 36 (46) 26 (33) 16 (21) 78
Male 80 (36) 77 (35) 66 (29) 223
Department of practice 0.009
Bouches du Rhône 58 (33) 73 (42) 43 (25) 174
Alpes Maritimes 40 (47) 23 (27) 23 (27) 86
Vaucluse 18 (44) 7 (17) 16 (39) 41
Type of practice 0.08
Private practice 102 (40) 89 (35) 63 (25) 254
Salary ± private practice 14 (30) 14 (30) 19 (40) 47
Number of consultations per day 0.02
< 20 63 (45) 49 (35) 28 (20) 140
≥ 20 53 (32) 54 (34) 54 (34) 161
Practice includes acupuncture 0.04
Principally or occasionally 19 (49) 16 (41) 4 (10) 39
Never 97 (37) 87 (33) 78 (30) 262
Afraid that ordering screening tests will be penalizing 0.12
Yes 11 (58) 3 (16) 5 (26) 19
No 101 (37) 99 (36) 77 (27) 277
Participation in a hepatitis-HIV network 0.11
Yes 26 (38) 18 (26) 25 (36) 69
No 90 (39) 85 (37) 57 (25) 232
HIV screening test(s) ordered during the last 12 months 0.0001
0-5 33 (67) 12 (25) 4 (8) 49
6-20 51 (38) 58 (43) 27 (20) 136
> 20 32 (28) 33 (28) 51 (44) 116
Number of drug abusers among patients treated during the last 4 weeks 0.0001
At least 1 34 (28) 39 (33) 48 (39) 121
None 82 (46) 64 (36) 34 (18) 180
Personal screening 0.007
No 38 (44) 27 (31) 22 (25) 87
HIV only 44 (49) 29 (33) 16 (18) 89
HCV (with or without HIV) 34 (27) 47 (38) 44 (35) 125
Use of condoms 0.53
Yes 71 (36) 70 (35) 55 (29) 185
No 45 (43) 33 (31) 27 (26) 105
of GPs thought that intravenous drug users often refuse liver the opinion that patients can adhere to interferon treatment
biopsy compared with 39% of patients in general (P < 0.01). On prescribe tests more often (P = 0.06).
the other hand, 61% and 90% respectively agreed with the
opinion that active intravenous drug users and users of intrave- The initial multivariate analysis included all factors associated
nous drug substitutes can adhere to interferon treatment. Half of with non-prescription of HCV screening tests during the last 4
the GPs agreed with the opinion that HCV-infected patients weeks with a 20% statistical threshold. A backward stepwise
drinking three to four glasses of alcoholic beverages daily can model excluding 4 correctly classified 77% of the predicted
adhere to interferon treatment. With one exception, opinions values, retaining 8 significant and independent variables asso-
concerning medical management of HCV-infected patients were ciated with the lack of a screening test (table V). These included:
not correlated with the rate of screening test prescription during GPs aged over 40 years, practice in the Alpes-Maritimes, no
the last 4 weeks. It was simply noted that GPs in agreement with drug users among patients, agreement with the opinion that
263
4. M. Rotily et al.
Table II. − Screening tests prescribed in relation to the various risk factors and identification of risk factors, n (%).
Screening tests proposed for Always Often Occasionally/never Notapplicable
Intravenous drug abuser 233 (85) 18 (6) 24 (9) 26
Pernasal drug abuser 124 (46) 39 (15) 105 (39) 33
Patient transfused before 1991 226 (75) 25 (8) 50 (17) –
Patient transfused after 1990 160 (53) 43 (14) 98 (33) –
Patient with elevated ALAT 214 (71) 31 (10) 56 (19) –
Patient with HBV infection 229 (76) 30 (10) 42 (14) –
Patient with HIV infection 263 (87) 18 (6) 20 (7) –
Sexual partner of an HCV-positive person 228 (76) 25 (8) 48 (16) –
Patient who underwent endoscopy 48 (16) 29 (10) 224 (74) –
Patient with a history of major surgery 75 (25) 44 (15) 182 (60) –
New patient 5 (2) 3 (1) 293 (97) –
Search for risk factors Always Often Occasionally Never
Regular use of intravenous drugs 92 (31) 53 (18) 118 (39) 38 (13)
Occasional use of intravenous drugs 79 (26) 39 (13) 135 (45) 48 (16)
Blood transfusion 176 (59) 58 (19) 50 (17) 17 (6)
Endoscopy 95 (32) 52 (17) 103 (34) 51 (17)
Invasive procedure 102 (34) 51 (17) 86 (29) 62 (21)
Table III. − Knowledge about the hepatitis C epidemic and its natural history in relation to number of
hepatitis C screening tests prescribed in the past 4 weeks, n (%).
None 1-2 tests > 2 tests Total P
n = 116 n = 103 n = 82 n = 301
Number of HCV infected persons in
France
< 400.000 39 (36) 41 (38) 29 (27) 109 0.25
400.000-600.000 (consensus) 38 (41) 32 (34) 23 (25) 93
> 600.000 14 (31) 12 (27) 19 (42) 45
Do not know 25 (46) 18 (33) 11 (24) 54
Proportion of HCV-infected persons who
will develop chronic hepatitis
< 60 % 90 (41) 74 (33) 58 (26) 222 0.12
a
60-80 % (consensus) 14 (45) 12 (39) 31
> 80 % 6 (40) 7 (47) 2 (13) 15
Do not know 15 (46) 8 (24) 10 (30) 33
Proportion of persons with chronic
hepatitis who will develop cirrhosis
< 15 % 26 (41) 23 (37) 14 (22) 63 0.38
a
15-25 % (consensus) 14 (26) 20 (38) 19 (36) 53
> 25 % 57 (39) 50 (34) 39 (27) 146
Do not know 19 (49) 10 (26) 10 (26) 39
Proportion of persons with cirrhosis who
will develop hepatocellular carcinoma
<3% 7 (44) 5 (31) 4 (25) 16 0.97
3-6 % (consensus) 12 (38) 13 (41) 7 (22) 32
>6% 75 (38) 68 (34) 57 (29) 200
Do not know 22 (42) 17 (32) 14 (26) 53
a
p < 0.05 in adjusted residuals analysis.
264
5. Factors related to screening of hepatitis C virus in general medicine
Table IV. − Prescription of hepatitis C screening tests in the past 4 weeks in relation to opinions about
the treatment of patients infected with hepatitis C virus, n (%).
None 1-2 tests > 2 tests Total P
n = 116 n = 103 n = 82 n = 301
Interferon is effective alone
Agree 84 (40) 68 (33) 56 (27) 208 0.58
Do not agree 32 (34) 35 (38) 26 (28) 93
Interferon-ribavirine combination is effective
Agree 112 (39) 98 (34) 77 (27) 287 0.68
Do not agree 4 (28) 5 (36) 5 (36) 14
Interferon produces important adverse effects
Agree 90 (40) 81 (36) 56 (24) 227 0.21
Do not agree 26 (35) 22 (30) 26 (35) 74
Patients often have to interrupt interferon treatments
Agree 45 (37) 48 (40) 28 (23) 121 0.21
Do not agree 71 (39) 55 (31) 54 (30) 180
Patients often refuse liver biopsy
Agree 51 (43) 37 (31) 32 (27) 120 0.47
Do not agree 65 (36) 66 (36) 50 (28) 181
Patients often refuse interferon treatment
Agree 24 (41) 22 (38) 12 (21) 58 0.45
Do not agree 92 (38) 81 (33) 70 (29) 243
Patients observe interferon prescriptions well
Agree 111 (41)a 90 (33) 72 (26) 273 0.06
Do not agree 5 (18) 13 (46) 10 (36) 28
IDU often refuse liver biopsy
Agree 37 (32) 42 (36) 37 (32) 116 0.60
Do not agree 13 25) 19 (36) 20 (39) 52
IDU often refuse interferon therapy
Agree 24 (30) 29 (37) 26 (33) 79 0.88
Do not agree 21 (30) 24 (34) 26 (36) 71
IDU observe interferon prescriptions well
Agree 24 (32) 23 (31) 27 (37) 74 0.53
Do not agree 20 (26) 30 (40) 26 (34) 76
IDU can benefit from interferon
Agree 76 (43) 56 (32) 45 (25) 177 0.07
Do not agree 33 (30) 43 (38) 36 (32) 112
Patients on substitute drugs can benefit from interferon
Agree 98 (38) 89 (35) 71 (28) 258 0.92
Do not agree 12 (41) 9 (31) 8 (28) 29
Patients drinking more than 3-4 glasses of alcoholic
beverage per day can benefit from interferon
Agree 64 (41) 53 (34) 39 (25) 156 0.33
Do not agree 46 (33) 49 (36) 43 (31) 138
IDU: intravenous drug users.
p < 0.05 in standardized adjusted residuals analysis.
a
patients adhere well to interferon prescriptions, poor knowledge GPs conducted in the study region on other topics, particularly
of progression from chronic hepatitis to cirrhosis, few or no concerning attitudes and opinions about HIV (80%) [24]. There
prescriptions of HIV screening tests, fear of being penalized for could be several reasons for this difference. First, GPs may be
prescribing HCV screening tests. becoming less willing to participate in telephone interviews
because they consider they are being solicited too often. This
lower participation rate could also be related to less concern
about hepatitis C than about other diseases such as AIDS or more
Discussion prevalent benign diseases [25]. The participation rate is however
comparable with those generally observed in national surveys
The rate of participation of GPs in this survey (68%) is [26, 27]. The social and demographic characteristics of our
comparable but slightly below that observed in early surveys of
265
6. M. Rotily et al.
Table V. − Multivariate analysis of the factors associated with the finding that would suggest that information campaigns with
practice of hepatitis C screening. overly alarming messages have little impact.
The factors with a determining effect on screening practices
Odds 95 % CI p appear to lie elsewhere, perhaps in the identification of risk
ratio
factors and most importantly in the method and arguments used
Age when proposing a screening test to a patient. First of all, it was
≤ 40 years Ref noticed that the GPs did not systematically search for risk factors
such as history of transfusion or drug use. Likewise in offering
> 40 years 3.12 [1.39-7.00] 0.006
screening tests for patients at risk of HCV infection. Accordingly,
Department 19% and 14% respectively never or only occasionally proposed
Bouches du Rhône Ref tests for patients with an elevated ALT level or who had prior HBV
Alpes Maritimes 2.05 [1.10-3.84] 0.02
infection. On the other hand, screening practices which the 1997
consensus conference did not include in their recommendations,
Vaucluse 2.00 [0.88-4.53] 0.10 i.e. tests for patients with a history of major surgery or
Drug user seen at consultation during endoscopy, were systematically employed by a non-negligible
the last 4 weeks number of GPs. The efficacy of widening screening to include
At least one Ref nosocomial risks has not been clearly demonstrated, but the
None 2.24 [1.25-4.02] 0.007 French General Direction of Health has published a document for
healthcare workers where nosocomial exposure is placed on the
Patients observe interferon
prescriptions well
same level as history of blood transfusion on the list of risk factors
to be identified. The recent action taken by private medical
Agree Ref laboratories has also raised the question of nosocomial contami-
Do not agree 6.89 [1.50-31.64] 0.01 nation since 44% of the declared reasons for searching for HCV
Knowledge of the course of HCV contamination involve medical investigations. These results are in
infection agreement with those of recently published French studies [29,
Good Ref 30].
Poor 6.04 [1.62-22.41] 0.007 The high proportion of general practitioners who never or
only occasionally propose tests for people transfused before
Knowledge of course to cirrhosis
1991 could be explained either by insufficient diffusion of
Good Ref professional guidelines, including conference guidelines, or by
Poor 3.02 [1.32-6.93] 0.009 the insufficiency of these guidelines themselves. In our question-
naire, we asked the 177 GPs who had an Internet access if they
Number of HIV screening tests
prescribed during the last 12 months wanted to receive the text of the consensus conference. Only 6 of
them stated they already had the guidelines and 87% asked to
>5 Ref
receive them. In addition, we did not observe any significant
0-5 5.55 [2.54-12.07] 0.0001 relationship between declared search for risk factors and the
Do you believe prescribing HCV tests frequency of screening test prescriptions. It would be reasonable
will have a penalizing effect? to assume that physicians who search for risk factors would also
No Ref prescribe screening tests more often. It appears thus that
Yes 2.82 [0.94-8.53] 0.07
physicians have a certain difficulty in proposing a screening test
as part of their search for risk factors such as drug use or blood
Ref: reference value = 1 to calculate odds ratio. transfusion. It is difficult for patients to tell their physician they use
or have used intravenous drugs, even occasionally. Likewise, it is
difficult for the physician to search for a history of penal
sample population are similar to those in earlier regional surveys incarceration. GPs may also be unable to identify transfusion
[25, 28]. episodes because before 1990 hospitalized patients were not
It is always difficult to achieve a precise assessment of necessarily informed of blood transfusions performed during
awareness and opinion among healthcare professionals. their hospital stay. These various factors could explain, in part,
Indeed, knowledge of a disease cannot be adequately summa- the absence of correlation between the search for risk factors and
rized with a few questions during a telephone interview. The the frequency of screening test prescription. An additional factor
process involved is more complex. In a telephone survey, it is would be the absence of tracability of blood products prior to
highly unlikely that a good response rate could be maintained if 1991, explaining the large number of persons currently unaware
an excessively large number of questions were asked. General of their serology status.
practitioners would also perceive extensive surveys as a test of The GPs who stated they cared for intravenous drug users had
knowledge, which would probably lower the participation rate. prescribed more screening tests during the 4 preceding weeks
The four questions concerning the HCV epidemic and the natural than the others. Similarly, when asked about their attitude
history of the disease were designed to reflect both knowledge concerning proposing screening tests, the GPs stated they
and awareness of the hepatitis C epidemic. It would be propose tests to intravenous drug users more systematically than
reasonable to assume that physicians who express a correct or to people who had transfusions before 1991, who had known
overestimation of the epidemic and who perceive treatments as HBV infection, or who lived with an HCV-infected person. This
being effective and well observed by patients would tend to perception and more favorable attitude about screening drug
propose screening tests more regularly. Our findings do not user is particularly surprising in light of the fact that a majority of
however provide confirmation of this assumption since even the GPs stated they believe drug users refuse liver biopsy and
physicians who were of the opinion that patients comply with interferon treatment more often than other patients and that they
their interferon treatment correctly offered HCV screening tests adhere to prescribed treatments less well. It thus appears that
less often. The magnitude of the epidemic, the efficacy of hepatitis C is perceived first of all as a drug-use-related disease
treatments, and the acceptability of medical management thus do which not only stigmatizes drug users, but also leads to
not appear to be determining factors for screening practices, a insufficient proposal for screening tests to people with a history of
266
7. Factors related to screening of hepatitis C virus in general medicine
drug transfusion. These findings are in agreement with earlier without dramatizing the disease, although all must be aware of
work where it was demonstrated that intravenous drug users are the importance of this public health problem in France.
more often aware of their serology status than non-users [31] and
that the efficiency of post-transfusion screening is low [32]. ACKNOWLEDGMENTS - This study was conducted with the support of
In a study conducted in the department of Poitou-Charentes, it the Agence Nationale de Recherche on AIDS (convention N° 98137 du
17/12/1998). The authors thank Christian Pradier, members of the
was also shown that fear of biopsy and treatment side effects is
scientific committee (Luc Niel, Marc Bourlière, Denis Ouzan, Stanislas
shared by patients and physicians [33]. Our results emphasize Pol, Danièle Botta-Friedlund), the inquirers (Dominique Braesh,
the high percentage of general practitioners who agree with the Stéphane Berthelot, Christine Carvajal, Christel Durazzi, Carole Joseph,
opinion that drug users refuse liver biopsy and treatment more Marylise Sauze), and Claire Delorme, Joëlle Bussolon, Aude Baudouin,
often and follow their treatment less well than the general and all the general practitioners who took the time to participate in this
population of HCV-infected patients. Work on medical manage- survey.
ment of HIV in drug users has demonstrated that physicians who
care for these patients often retain a poor evaluation of patient
adherence to treatment and that their prescription of anti-
´ ´
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