Factors related to screening of hepatitis C virus in generalmedicine

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.

SUMMARYDespite the high prevalence of hepatitis C in France (≈ 1.2%), a large proportion of people infected with hepatitis C virus (HCV) are not knownaware 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 HCVscreening 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 bloodtransfusion, and identification of risk factors among patients were not satisfactory. Multivariate analysis showed that certain characteristics ingeneral 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 humanimmunodeficiency virus tests (odds-ratio: 5.55). Other characteristics such as awareness of the course of hepatitis C and health care were alsoassociated 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 andinvestigation of risk factors among patients are not satisfactory among South-eastern French general practitioners. Although HCV screening andhealth care must be improved among intravenous drug users, hepatitis C should not be considered as a disease of injecting drug users only bygeneral practitioners and the population. Efforts should be made so that hepatitis C is recognized as a global public health issue, and training ofgeneral 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 onwww.e2med.com/gcb). Gastroenterol Clin Biol 2002;26:261-9.

An estimated 550,000 persons are infected by the hepatitis Cvirus (HCV) in France [1]. This estimate is based on cross-sectional surveys performed in 1994 which have not beenrenewed since that time. One survey population included womenterminating their pregnancy in the Provence-Alpes-Côte d’Azurand Ile-de-France regions of France [2] and another includedsubjects who voluntarily attended health center consultations [3].With a prevalence of about 1.2% in the French population, HCVis considered to be a real cause of rising mortality due tohepatocellular carcinoma [4]. Retrospective models predicts thatwithout treatment, mortality due to hepatocellular carcinomarelated to HCV infection will continue to rise up through 2020.The annual rise should be expected to reach 150% in men and200% in women [5]. It is also known that progression to cirrhosisis strongly correlated with sex and age. Therapeutic progress,notably with the interferon-ribavirine combination [6, 7] and useof pegylated interferon, allows hope for a significant reduction inmorbidity and mortality. In addition, we were able to demon-strate that screening for HCV infection would lead to cost-effectiveness ratios quite comparable with those accepted forother diseases [8]. With the advent of new treatments, hepatitis

C screening, initially justified to limit the number of new cases,has become a central issue in the anti-hepatitis C campaign.

The current estimate of de novo diagnoses (6000 casesannually including 3500 to 5000 treated patients), as establishedin 1994, contrasts strongly with the estimated number of infectedpersons (550,000) [9]. Several arguments can be put forward toexplain this discordance between the estimated number ofpersons infected by the HCV and the number of patients surveyedand treated. The number of persons actually infected could beoverestimated. Many people have already benefited from treat-ment while others have not been treated, for reasons related tothe clinical patterns or to contraindications. A significant propor-tion of HCV-infected persons are unaware of their serology status[3, 10-12]. Several hypotheses may be advanced to help explaininadequacies in screening. Patients can underestimate the gravityof the disease, fearing the results of complementary tests, or havelittle confidence in current treatments [13]. There is also thequestion of proximity. Here general practitioners (GPs) play acrucial role in screening for infection [14]. Data on hepatitis Cserology obtained in public and private laboratories in theProvence-Alpes-Côte-d’Azur region of France where tests arereimbursed by the national social security, show that GPs play animportant role in HCV screening in this geographic region. In2000, 50% of the prescriptions for HCV serology executed inProvence-Alpes-Côte-d’Azur were written by GPs [15]. All these

Tirés à part : M. ROTILY, INSERM U379, 23 rue Stanislas Torrents,13006 Marseille.E-mail: rotily@marseille.inserm.fr

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

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elements converge: there is a clear need for knowledge concern-ing the screening practices of GPs and factors underlying thedecision to prescribe screening tests.

For human immunodeficiency virus (HIV) infection, it hasbeen demonstrated that patient knowledge, attitude toward andperception of the disease as well as personal behavior patternsare closely related to screening and management practices [16].There is however little data in the literature pertaining to thesequestions in HCV [17, 18]. It has been demonstrated in dialysispatients, that systematic screening for hepatitis C is a widespreadbut diversely implemented practice [19]. The purpose of our studywas to describe the knowledge, opinions and practical attitude ofgeneral practitioners in France concerning hepatitis C screeningand to identify characteristic features associated with regularprescription of screening tests by these general practitioners.

Material and methods

The study population was composed of general practitioners withprivate practices in the French departments of Alpes-Maritimes, Vaucluse,and Bouches-du-Rhône. A random sample was taken from the telephonebook lists for general practice and general medicine orientation home-opathy and/or acupuncture (n = 4102).

Questionnaires were prepared by a panel of hepatitis C experts andby general practitioners, taking into account the recommendations of thelegal authorities and the guidelines developed during the conferences onhepatitis C held in 1997 and 1999 [20-22]. Intravenous and pernasaldrug abuse, blood transfusion before 1991, and history of penalincarceration were considered in 1999 to be the principal risk factors forHCV infection in addition to the following risk groups: patients with evenmoderately elevated transaminase levels, patients infected by the hepati-tis B virus or the HIV, sexual partners of an HCV carrier. We widened oursearch for other possible factors of transmission which are not recom-mended by the conferences for routine practice, notably history of surgeryor endoscopy. One hundred one closed-choice items were tested in apilot phase conducted with the participation of 5 GPs working outside thegeographic region of the study. Six trained female inquirers thenconducted phone interviews with the GPs in the study population betweenMay and June 1999. On average, the interviews lasted 13 minutes. Eachphone number was called 6 times between 9 a.m. and 7 p.m. at differenthours and different days. Among the 609 GPs in the random sample,12% were not within the target population (no medical practice, retired,no longer in practice, hospital physician) and 14% could not be reachedby phone. Among the 451 GPs who could be contacted, 68% agreed toparticipate. In all, 317 were interviewed. Sixteen questionnaires wereexcluded because of non-response to more than 25 items or incoherentresponses. The study population retained for analysis thus included 301general practitioners.

The chi-square test was used to test correlations between qualitativevariables. The standardized adjusted residuals method was used toidentify cells contributing significantly to the chi-square test. Odds ratioand 95% confidence intervals were calculated to quantify the power of therelationships between the different variables studied and the prescriptionof a hepatitis C screening test within the last 4 weeks. Confounding factorswere identified with logistic regression using SPSS version 9.0T [23]. Allvariables demonstrating significance at p < 0.20 were retained for theinitial model. The final model was obtained using the step-by-stepdescending method. The fit of the final model was evaluated with theHosmer-Lemershow test. All first order interactions were identified andtested. Outlying residuals exhibiting a distribution beyond 2 standarddeviations were excluded from the final model.

Results

Thirty-nine percent of the GPs had not prescribed a screeningtest during the 4 preceding weeks, 34% had prescribed one ortwo and 27% had prescribed more than two. Thirty-seven percentof the GPs had not ordered a test with a positive result within thelast 12 months, 38% had had one or two positive tests and 25%

had had more than two. Among those who had not had a positivescreen during the last 12 months, 55% had not prescribed ascreening test during the 4 preceding weeks. Of those who hadhad a positive screening test for at least one patient during the last12 months, 29% had not prescribed a screening test during the 4preceding weeks. Conversely, among the GPs who had hadpositive tests for more than 2 patients during the last 12 months,15% had not prescribed a test during the 4 preceding weeks,28% had prescribed one or two and 58% had prescribed morethan two (P < 0.0001).

Factors associated with screening practices are presented intable I. GPs who were under 40 years of age, who practiced inthe Bouches-du-Rhône department, who had a mixed practice(private-salary), who saw more than 20 patients per day, whohad tested themselves for HCV, who never practiced acupunc-ture, and who proposed HIV screening tests were the GPs whomore frequently prescribed HCV screening tests. GPs who hadprovided care for at least one drug abuser during the preceding4 weeks prescribed HCV tests more often than those who had not.Inversely, GPs who feared they would be penalized due to HCVscreening tests appeared to prescribe such tests less often. Finally,there was no significant relationship between counseling use ofcondoms and prescription of HCV screening tests (table I).

Potential risk factors leading to HCV screening tests arepresented in table II. Tests were proposed to two groups ofpatients in priority: intravenous drug abusers and HIV-infectedpatients. However, 9% and 7% of the GPs stated they do notpropose tests for these categories of patients respectively; 39%stated they never or rarely propose HCV screening tests forpernasal drug abuseres. For patients who had had a bloodtransfusion before 1991, who had either elevated ALT levels, orwere known to have hepatitis B virus infection, 14% to 19% of theGPs proposed HCV screening tests occasionally or never. Forpatients with a history of major surgery or endoscopy, 60% and74% of the GPs respectively proposed tests occasionally or never.Practices concerning search for risk factors, e.g. regular oroccasional intravenous drug use, blood transfusion, history ofmajor surgery or endoscopy, are also presented in table II. Asearch for risk factors at consultation was not significantlycorrelated with prescription of HCV screening tests during the 4weeks preceding the study.

More than one-third of the GPs underestimated the amplitudeof the HCV epidemic in France and 18% of them stated they didnot know the magnitude of the epidemic; 74% of the GPsunderestimated the risk of progression from infection to chronichepatitis while 49% and 66%, respectively overestimated the riskof progression from chronic hepatitis to cirrhosis and fromcirrhosis to hepatocellular carcinoma (table III). On univariateanalysis, these levels of knowledge were not or weakly correlatedwith screening practice during the last 4 weeks. Analysis ofadjusted residuals only retained that GPs who estimated the riskof progression from chronic hepatitis to cirrhosis correctlyapparently prescribed screening tests more often than those whoover or under estimated the risk or did not respond to thequestion.

For questions concerning medical management of patientsinfected with the HCV virus, 69% and 95% of GPs respectively feltthat interferon alone or in combination with ribavirine is effective(table IV). Three-quarters of the GPs also felt that adverse effectsassociated with interferon are important and 40% agreed withthe opinion that patients often interrupt interferon treatment andrefuse liver biopsy. In the opinion of a minority of the GPs,patients adhere well to interferon treatment. The GPs had a morenegative opinion concerning patient behavior for liver biopsy,refusal of treatment, and adherence to the prescribed treatmentfor intravenous drug abusers than for the other patients. The rateof non-response for these questions was high. For example, 53%

M. Rotily et al.

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of GPs thought that intravenous drug users often refuse liverbiopsy compared with 39% of patients in general (P < 0.01). Onthe other hand, 61% and 90% respectively agreed with theopinion that active intravenous drug users and users of intrave-nous drug substitutes can adhere to interferon treatment. Half ofthe GPs agreed with the opinion that HCV-infected patientsdrinking three to four glasses of alcoholic beverages daily canadhere to interferon treatment. With one exception, opinionsconcerning medical management of HCV-infected patients werenot correlated with the rate of screening test prescription duringthe last 4 weeks. It was simply noted that GPs in agreement with

the opinion that patients can adhere to interferon treatmentprescribe tests more often (P = 0.06).

The initial multivariate analysis included all factors associatedwith non-prescription of HCV screening tests during the last 4weeks with a 20% statistical threshold. A backward stepwisemodel excluding 4 correctly classified 77% of the predictedvalues, retaining 8 significant and independent variables asso-ciated with the lack of a screening test (table V). These included:GPs aged over 40 years, practice in the Alpes-Maritimes, nodrug users among patients, agreement with the opinion that

Table I. − Number of screening tests offered in the past four weeks in relation to the characteristics of the general practitioner.

Nonen = 116

1-2 testsn = 103

> 2 testsn = 82

Totaln = 301

P

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

Factors related to screening of hepatitis C virus in general medicine

263

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 ofhepatitis C screening tests prescribed in the past 4 weeks, n (%).

Nonen = 116

1-2 testsn = 103

> 2 testsn = 82

Totaln = 301

P

Number of HCV infected persons inFrance

< 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 whowill develop chronic hepatitis

< 60 % 90 (41) 74 (33) 58 (26) 222 0.12

60-80 % (consensus) a 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 chronichepatitis who will develop cirrhosis

< 15 % 26 (41) 23 (37) 14 (22) 63 0.38

15-25 % (consensus) 14 (26)a 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 whowill 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.

M. Rotily et al.

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patients adhere well to interferon prescriptions, poor knowledgeof progression from chronic hepatitis to cirrhosis, few or noprescriptions of HIV screening tests, fear of being penalized forprescribing HCV screening tests.

Discussion

The rate of participation of GPs in this survey (68%) iscomparable but slightly below that observed in early surveys of

GPs conducted in the study region on other topics, particularlyconcerning attitudes and opinions about HIV (80%) [24]. Therecould be several reasons for this difference. First, GPs may bebecoming less willing to participate in telephone interviewsbecause they consider they are being solicited too often. Thislower participation rate could also be related to less concernabout hepatitis C than about other diseases such as AIDS or moreprevalent benign diseases [25]. The participation rate is howevercomparable with those generally observed in national surveys[26, 27]. The social and demographic characteristics of our

Table IV. − Prescription of hepatitis C screening tests in the past 4 weeks in relation to opinions aboutthe treatment of patients infected with hepatitis C virus, n (%).

Nonen = 116

1-2 testsn = 103

> 2 testsn = 82

Totaln = 301

P

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 alcoholicbeverage 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.ap < 0.05 in standardized adjusted residuals analysis.

Factors related to screening of hepatitis C virus in general medicine

265

sample population are similar to those in earlier regional surveys[25, 28].

It is always difficult to achieve a precise assessment ofawareness and opinion among healthcare professionals.Indeed, knowledge of a disease cannot be adequately summa-rized with a few questions during a telephone interview. Theprocess involved is more complex. In a telephone survey, it ishighly unlikely that a good response rate could be maintained ifan excessively large number of questions were asked. Generalpractitioners would also perceive extensive surveys as a test ofknowledge, which would probably lower the participation rate.The four questions concerning the HCV epidemic and the naturalhistory of the disease were designed to reflect both knowledgeand awareness of the hepatitis C epidemic. It would bereasonable to assume that physicians who express a correct oroverestimation of the epidemic and who perceive treatments asbeing effective and well observed by patients would tend topropose screening tests more regularly. Our findings do nothowever provide confirmation of this assumption since evenphysicians who were of the opinion that patients comply withtheir interferon treatment correctly offered HCV screening testsless often. The magnitude of the epidemic, the efficacy oftreatments, and the acceptability of medical management thus donot appear to be determining factors for screening practices, a

finding that would suggest that information campaigns withoverly alarming messages have little impact.

The factors with a determining effect on screening practicesappear to lie elsewhere, perhaps in the identification of riskfactors and most importantly in the method and arguments usedwhen proposing a screening test to a patient. First of all, it wasnoticed that the GPs did not systematically search for risk factorssuch as history of transfusion or drug use. Likewise in offeringscreening tests for patients at risk of HCV infection. Accordingly,19% and 14% respectively never or only occasionally proposedtests for patients with an elevated ALT level or who had prior HBVinfection. On the other hand, screening practices which the 1997consensus conference did not include in their recommendations,i.e. tests for patients with a history of major surgery orendoscopy, were systematically employed by a non-negligiblenumber of GPs. The efficacy of widening screening to includenosocomial risks has not been clearly demonstrated, but theFrench General Direction of Health has published a document forhealthcare workers where nosocomial exposure is placed on thesame level as history of blood transfusion on the list of risk factorsto be identified. The recent action taken by private medicallaboratories has also raised the question of nosocomial contami-nation since 44% of the declared reasons for searching for HCVcontamination involve medical investigations. These results are inagreement with those of recently published French studies [29,30].

The high proportion of general practitioners who never oronly occasionally propose tests for people transfused before1991 could be explained either by insufficient diffusion ofprofessional guidelines, including conference guidelines, or bythe insufficiency of these guidelines themselves. In our question-naire, we asked the 177 GPs who had an Internet access if theywanted to receive the text of the consensus conference. Only 6 ofthem stated they already had the guidelines and 87% asked toreceive them. In addition, we did not observe any significantrelationship between declared search for risk factors and thefrequency of screening test prescriptions. It would be reasonableto assume that physicians who search for risk factors would alsoprescribe screening tests more often. It appears thus thatphysicians have a certain difficulty in proposing a screening testas part of their search for risk factors such as drug use or bloodtransfusion. It is difficult for patients to tell their physician they useor have used intravenous drugs, even occasionally. Likewise, it isdifficult for the physician to search for a history of penalincarceration. GPs may also be unable to identify transfusionepisodes because before 1990 hospitalized patients were notnecessarily informed of blood transfusions performed duringtheir hospital stay. These various factors could explain, in part,the absence of correlation between the search for risk factors andthe frequency of screening test prescription. An additional factorwould be the absence of tracability of blood products prior to1991, explaining the large number of persons currently unawareof their serology status.

The GPs who stated they cared for intravenous drug users hadprescribed more screening tests during the 4 preceding weeksthan the others. Similarly, when asked about their attitudeconcerning proposing screening tests, the GPs stated theypropose tests to intravenous drug users more systematically thanto people who had transfusions before 1991, who had knownHBV infection, or who lived with an HCV-infected person. Thisperception and more favorable attitude about screening druguser is particularly surprising in light of the fact that a majority ofthe GPs stated they believe drug users refuse liver biopsy andinterferon treatment more often than other patients and that theyadhere to prescribed treatments less well. It thus appears thathepatitis C is perceived first of all as a drug-use-related diseasewhich not only stigmatizes drug users, but also leads toinsufficient proposal for screening tests to people with a history of

Table V. − Multivariate analysis of the factors associated with thepractice of hepatitis C screening.

Oddsratio

95 % CI p

Age

≤ 40 years Ref

> 40 years 3.12 [1.39-7.00] 0.006

Department

Bouches du Rhône Ref

Alpes Maritimes 2.05 [1.10-3.84] 0.02

Vaucluse 2.00 [0.88-4.53] 0.10

Drug user seen at consultation duringthe last 4 weeks

At least one Ref

None 2.24 [1.25-4.02] 0.007

Patients observe interferonprescriptions well

Agree Ref

Do not agree 6.89 [1.50-31.64] 0.01

Knowledge of the course of HCVinfection

Good Ref

Poor 6.04 [1.62-22.41] 0.007

Knowledge of course to cirrhosis

Good Ref

Poor 3.02 [1.32-6.93] 0.009

Number of HIV screening testsprescribed during the last 12 months

> 5 Ref

0-5 5.55 [2.54-12.07] 0.0001

Do you believe prescribing HCV testswill have a penalizing effect?

No Ref

Yes 2.82 [0.94-8.53] 0.07

Ref: reference value = 1 to calculate odds ratio.

M. Rotily et al.

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drug transfusion. These findings are in agreement with earlierwork where it was demonstrated that intravenous drug users aremore often aware of their serology status than non-users [31] andthat the efficiency of post-transfusion screening is low [32].

In a study conducted in the department of Poitou-Charentes, itwas also shown that fear of biopsy and treatment side effects isshared by patients and physicians [33]. Our results emphasizethe high percentage of general practitioners who agree with theopinion that drug users refuse liver biopsy and treatment moreoften and follow their treatment less well than the generalpopulation of HCV-infected patients. Work on medical manage-ment of HIV in drug users has demonstrated that physicians whocare for these patients often retain a poor evaluation of patientadherence to treatment and that their prescription of anti-retroviral drugs is based on and adapted to this erroneousevaluation [34]. Unlike the widespread opinion among manypractitioners, it has been demonstrated that drug users are oftencapable of following their prescriptions satisfactorily [35]. Inparticular, adherence to treatment is good in patients givenmethadone or buprenorphine substitutes [36]. It is thus urgent toverify whether the opinion that drug users refuse liver biopsymore often and/or do not adhere well to their interferontreatment is founded or not. It is also important to identify factorsassociated with refusal of liver biopsy and poor therapeuticobservance.

Even after adjustments for confounding factors, the GPs in thisstudy who practice in certain French departments orderedscreening tests more often than their colleagues in other depart-ments in the same region. In an earlier survey on delay in HIVscreening in the region, we had already noted a considerablediscrepancy between access to screening in the different depart-ments [31]. Practices appear to be determined locally, althoughno underlying reasons could be identified. Proximity to auniversity teaching hospital, presence of dynamic preventionnetworks, organization of continuing education programs, andprevention policies implemented by local authorities wouldconstitute potential hypotheses to analyze. Regarding the contri-bution of healthcare networks, the study by Babany et al. [37]conducted in 604 general practitioners demonstrated that morethan 90% did not participate in an HCV network, and mostimportantly that one-third expressed their desire to participate insuch a network in order to have access to better qualityinformation.Our findings argue in favor of the idea that localdisparities in access to health care exist within given regions ofcountries like France where health policy is highly centralized.

We noted a positive correlation between prescription of HIVtests and HCV tests. It appears that general practitioners who arefamiliar with screening procedures are more prone to proposetests for HCV infection. It has been demonstrated, for AIDS, thatcertain social and demographic, as well as personal, character-istics are associated with medical practices and attitudes [24].Our findings demonstrate that younger physicians are morefavorable towards screening for HCV infection and inversely,physicians who fear being penalized because they order screen-ing tests are less prone to prescribe screening.

In summary, this study shows that sustained efforts will berequired to improve general practitioners’ screening practices forHCV in France. The situation could be even less favorable inregions with a lower prevalence of drug use than in southernFrance. A national survey on screening practices of generalpractitioners and specialists working in private practice would bemost useful. Beyond the evident need for reinforced screeningand management of occasional or regular drug abusers, it isessential to combat the opinion among physicians and thegeneral public that HCV infection is limited to this population. Forus, efforts should be placed on better informing physicians onhow best to identify risk factors and propose screening tests

without dramatizing the disease, although all must be aware ofthe importance of this public health problem in France.

ACKNOWLEDGMENTS - This study was conducted with the support ofthe Agence Nationale de Recherche on AIDS (convention N° 98137 du17/12/1998). The authors thank Christian Pradier, members of thescientific committee (Luc Niel, Marc Bourlière, Denis Ouzan, StanislasPol, Danièle Botta-Friedlund), the inquirers (Dominique Braesh,Stéphane Berthelot, Christine Carvajal, Christel Durazzi, Carole Joseph,Marylise Sauze), and Claire Delorme, Joëlle Bussolon, Aude Baudouin,and all the general practitioners who took the time to participate in thissurvey.

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