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© Masson, Paris, 2001.                                                                                                    Gastroenterol Clin Biol 2001;25:261-269




                          Factors related to screening of hepatitis C virus in general
                              medicine

         Michel ROTILY (1), Sandrine LOUBIÈRE (1), Johanne PRUDHOMME (1, 2), Isabelle PORTAL (3), Albert TRAN (4),
                              Philippe HOFLIGER (6), Dominique VALLA (5), Jean-Paul MOATTI (1)
     (1) INSERM U 379, Marseille ; (2) ORS Provence-Alpes-Côte d’Azur, Marseille, France ; (3) Réseau Hépatite MPAC, Hôpital la Conception, Marseille ;
   (4) Fédération des Maladies Transmissibles, Hôpital de l’Archet, Nice ; (5) Service d’Hépato-gastroentérologie, Hôpital Beaujon, Clichy ; (6) Correspondant
                                                  Régional, Provence-Alpes-Côte d’Azur de l’ANAES, Nice.


SUMMARY
Despite the high prevalence of hepatitis C in France (≈ 1.2%), a large proportion of people infected with hepatitis C virus (HCV) are not known
aware of their status. The objective of this study was to investigate the factors related to screening in general medicine.
Material and methods — Three hundred and one general practitioners were interviewed by phone in South-Eastern France about their HCV
screening practices, knowledge of the epidemic, of the natural course of the disease, and opinions about health care for people infected with HCV.
Results — While general practitioners often offered HCV screening to intravenous drug users, screening for people who had received blood
transfusion, and identification of risk factors among patients were not satisfactory. Multivariate analysis showed that certain characteristics in
general practitioners were negatively and independently related to the frequency of HCV screening, especially: general practitioners older than 40
(odds-ratio: 3.12), general practitioners who did not care for intravenous drug users (odds-ratio: 2.24) and did not prescribe human
immunodeficiency virus tests (odds-ratio: 5.55). Other characteristics such as awareness of the course of hepatitis C and health care were also
associated with HCV screening. Conversely knowledge of the size of the epidemic was not related to better HCV screening practices.
Conclusion — Our study shows that knowledge about the size of the epidemic and the natural history of hepatitis C, HCV screening practices and
investigation of risk factors among patients are not satisfactory among South-eastern French general practitioners. Although HCV screening and
health care must be improved among intravenous drug users, hepatitis C should not be considered as a disease of injecting drug users only by
general practitioners and the population. Efforts should be made so that hepatitis C is recognized as a global public health issue, and training of
general practitioners should be improved to investigate risk factors and offer HCV screening instead of merely dramatizing the situation.




  To cite the present paper, use exclusively the following reference. Rotily M, Loubière S, Prudhomme J, Portal I, Tran A, Hofliger P,
  Valla D, Moatti JP. Facteurs associés à la proposition du dépistage de l’hépatite C en médecine générale (full text in english on
  www.e2med.com/gcb). Gastroenterol Clin Biol 2002;26:261-9.



An estimated 550,000 persons are infected by the hepatitis C                        C screening, initially justified to limit the number of new cases,
virus (HCV) in France [1]. This estimate is based on cross-                         has become a central issue in the anti-hepatitis C campaign.
sectional surveys performed in 1994 which have not been
renewed since that time. One survey population included women                             The current estimate of de novo diagnoses (6000 cases
terminating their pregnancy in the Provence-Alpes-Côte d’Azur                       annually including 3500 to 5000 treated patients), as established
and Ile-de-France regions of France [2] and another included                        in 1994, contrasts strongly with the estimated number of infected
subjects who voluntarily attended health center consultations [3].                  persons (550,000) [9]. Several arguments can be put forward to
With a prevalence of about 1.2% in the French population, HCV                       explain this discordance between the estimated number of
is considered to be a real cause of rising mortality due to                         persons infected by the HCV and the number of patients surveyed
hepatocellular carcinoma [4]. Retrospective models predicts that                    and treated. The number of persons actually infected could be
without treatment, mortality due to hepatocellular carcinoma                        overestimated. Many people have already benefited from treat-
related to HCV infection will continue to rise up through 2020.                     ment while others have not been treated, for reasons related to
The annual rise should be expected to reach 150% in men and                         the clinical patterns or to contraindications. A significant propor-
200% in women [5]. It is also known that progression to cirrhosis                   tion of HCV-infected persons are unaware of their serology status
is strongly correlated with sex and age. Therapeutic progress,                      [3, 10-12]. Several hypotheses may be advanced to help explain
notably with the interferon-ribavirine combination [6, 7] and use                   inadequacies in screening. Patients can underestimate the gravity
of pegylated interferon, allows hope for a significant reduction in                  of the disease, fearing the results of complementary tests, or have
morbidity and mortality. In addition, we were able to demon-                        little confidence in current treatments [13]. There is also the
strate that screening for HCV infection would lead to cost-                         question of proximity. Here general practitioners (GPs) play a
effectiveness ratios quite comparable with those accepted for                       crucial role in screening for infection [14]. Data on hepatitis C
other diseases [8]. With the advent of new treatments, hepatitis                    serology obtained in public and private laboratories in the
                                                                                    Provence-Alpes-Côte-d’Azur region of France where tests are
                                                                                    reimbursed by the national social security, show that GPs play an
Tirés à part : M. ROTILY, INSERM U379, 23 rue Stanislas Torrents,                   important role in HCV screening in this geographic region. In
13006 Marseille.                                                                    2000, 50% of the prescriptions for HCV serology executed in
E-mail: rotily@marseille.inserm.fr                                                  Provence-Alpes-Côte-d’Azur were written by GPs [15]. All these


                                                                              261
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
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
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
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
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
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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                                                                                 268

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Factors Related to HCV Screening in French General Practice

  • 1. © Masson, Paris, 2001. Gastroenterol Clin Biol 2001;25:261-269 Factors related to screening of hepatitis C virus in general medicine Michel ROTILY (1), Sandrine LOUBIÈRE (1), Johanne PRUDHOMME (1, 2), Isabelle PORTAL (3), Albert TRAN (4), Philippe HOFLIGER (6), Dominique VALLA (5), Jean-Paul MOATTI (1) (1) INSERM U 379, Marseille ; (2) ORS Provence-Alpes-Côte d’Azur, Marseille, France ; (3) Réseau Hépatite MPAC, Hôpital la Conception, Marseille ; (4) Fédération des Maladies Transmissibles, Hôpital de l’Archet, Nice ; (5) Service d’Hépato-gastroentérologie, Hôpital Beaujon, Clichy ; (6) Correspondant Régional, Provence-Alpes-Côte d’Azur de l’ANAES, Nice. SUMMARY Despite the high prevalence of hepatitis C in France (≈ 1.2%), a large proportion of people infected with hepatitis C virus (HCV) are not known aware of their status. The objective of this study was to investigate the factors related to screening in general medicine. Material and methods — Three hundred and one general practitioners were interviewed by phone in South-Eastern France about their HCV screening practices, knowledge of the epidemic, of the natural course of the disease, and opinions about health care for people infected with HCV. Results — While general practitioners often offered HCV screening to intravenous drug users, screening for people who had received blood transfusion, and identification of risk factors among patients were not satisfactory. Multivariate analysis showed that certain characteristics in general practitioners were negatively and independently related to the frequency of HCV screening, especially: general practitioners older than 40 (odds-ratio: 3.12), general practitioners who did not care for intravenous drug users (odds-ratio: 2.24) and did not prescribe human immunodeficiency virus tests (odds-ratio: 5.55). Other characteristics such as awareness of the course of hepatitis C and health care were also associated with HCV screening. Conversely knowledge of the size of the epidemic was not related to better HCV screening practices. Conclusion — Our study shows that knowledge about the size of the epidemic and the natural history of hepatitis C, HCV screening practices and investigation of risk factors among patients are not satisfactory among South-eastern French general practitioners. Although HCV screening and health care must be improved among intravenous drug users, hepatitis C should not be considered as a disease of injecting drug users only by general practitioners and the population. Efforts should be made so that hepatitis C is recognized as a global public health issue, and training of general practitioners should be improved to investigate risk factors and offer HCV screening instead of merely dramatizing the situation. To cite the present paper, use exclusively the following reference. Rotily M, Loubière S, Prudhomme J, Portal I, Tran A, Hofliger P, Valla D, Moatti JP. Facteurs associés à la proposition du dépistage de l’hépatite C en médecine générale (full text in english on www.e2med.com/gcb). Gastroenterol Clin Biol 2002;26:261-9. An estimated 550,000 persons are infected by the hepatitis C C screening, initially justified to limit the number of new cases, virus (HCV) in France [1]. This estimate is based on cross- has become a central issue in the anti-hepatitis C campaign. sectional surveys performed in 1994 which have not been renewed since that time. One survey population included women The current estimate of de novo diagnoses (6000 cases terminating their pregnancy in the Provence-Alpes-Côte d’Azur annually including 3500 to 5000 treated patients), as established and Ile-de-France regions of France [2] and another included in 1994, contrasts strongly with the estimated number of infected subjects who voluntarily attended health center consultations [3]. persons (550,000) [9]. Several arguments can be put forward to With a prevalence of about 1.2% in the French population, HCV explain this discordance between the estimated number of is considered to be a real cause of rising mortality due to persons infected by the HCV and the number of patients surveyed hepatocellular carcinoma [4]. Retrospective models predicts that and treated. The number of persons actually infected could be without treatment, mortality due to hepatocellular carcinoma overestimated. Many people have already benefited from treat- related to HCV infection will continue to rise up through 2020. ment while others have not been treated, for reasons related to The annual rise should be expected to reach 150% in men and the clinical patterns or to contraindications. A significant propor- 200% in women [5]. It is also known that progression to cirrhosis tion of HCV-infected persons are unaware of their serology status is strongly correlated with sex and age. Therapeutic progress, [3, 10-12]. Several hypotheses may be advanced to help explain notably with the interferon-ribavirine combination [6, 7] and use inadequacies in screening. Patients can underestimate the gravity of pegylated interferon, allows hope for a significant reduction in of the disease, fearing the results of complementary tests, or have morbidity and mortality. In addition, we were able to demon- little confidence in current treatments [13]. There is also the strate that screening for HCV infection would lead to cost- question of proximity. Here general practitioners (GPs) play a effectiveness ratios quite comparable with those accepted for crucial role in screening for infection [14]. Data on hepatitis C other diseases [8]. With the advent of new treatments, hepatitis serology obtained in public and private laboratories in the Provence-Alpes-Côte-d’Azur region of France where tests are reimbursed by the national social security, show that GPs play an Tirés à part : M. ROTILY, INSERM U379, 23 rue Stanislas Torrents, important role in HCV screening in this geographic region. In 13006 Marseille. 2000, 50% of the prescriptions for HCV serology executed in E-mail: rotily@marseille.inserm.fr Provence-Alpes-Côte-d’Azur were written by GPs [15]. All these 261
  • 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- ´ ´ REFERENCES retroviral drugs is based on and adapted to this erroneous evaluation [34]. Unlike the widespread opinion among many practitioners, it has been demonstrated that drug users are often 1. 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