Diagnostic delay in a French cohort of Crohn's disease patients

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Journal of Crohn's and Colitis (2014) xx, xxx–xxx

CROHNS-00954; No of Pages 6

Diagnostic delay in a French cohort ofCrohn's disease patients
Stéphane Nahona,⁎, Pierre Lahmekb, Bruno Lesgourguesa,Cécile Poupardin a, Stanislas Chaussadec,Laurent Peyrin-Biroulet d, Vered Abitbol c
a Division of Gastroenterology and Hepatology, GHI Le Raincy-Montfermeil, Montfermeil, Franceb Hopital Emile Roux, Limeil-Brevannes, Francec Division of Gastroenterology and Hepatology, Hopital Cochin, Paris, Franced Division of Gastroenterology and Hepatology, Inserm U954, University of Nancy, Nancy, France

Received 17 November 2013; received in revised form 25 January 2014; accepted 27 January 2014

⁎ Corresponding author at: Service d'hLeclerc, 93370 Montfermeil, France. Te

E-mail addresses: snahon@ch-mont

1873-9946/$ - see front matter © 2014http://dx.doi.org/10.1016/j.crohns.20

Please cite this article as: Nahon S, edx.doi.org/10.1016/j.crohns.2014.01

KEYWORDSCrohn's disease;Diagnostic delay;Socioeconomic deprivation

Abstract

Diagnostic delay is frequent in Crohn's disease (CD) and may partly depend on socioeconomicstatus. The aim of this study was to determine the diagnostic delay and to identify associatedrisk factors, including socioeconomic deprivation in a French cohort of CD patients.
Methods: Medical and socioeconomic characteristics of all consecutive CD patients followed in 2referral centers between September 2002 and July 2012 were prospectively recorded using anelectronic database. Diagnostic delay was defined as the time period (months) from the firstsymptom onset to CD diagnosis. A long diagnostic delay was defined by the upper quartile of thistime period. Univariate and multivariate analyses were performed to identify the baselinecharacteristics of patients associated with a long diagnostic delay.Results: Three hundred and sixty-four patients with CD (mean age = 29.2 ± 12.6 years, 40.8%men) were analyzed. Median diagnostic delay was 5 months, and a long diagnostic delay wasmore than 12 months. Fifty-six patients (15.3%) had perianal lesions, and 28 patients (8.6%) hadcomplicated disease at diagnosis. None of the following factors were associated with a longdiagnostic delay: age, gender, CD location and behavior, marital and educational, languageunderstanding, geographic origin and socioeconomic deprivation score measured by the EPICESscore.Conclusion: In this French referral center-based cohort of CD patients, the median diagnosticdelay was 5 months. None of the baseline characteristics of the CD, including socioeconomicdeprivation, influenced diagnostic delay in this cohort.© 2014 European Crohn's and Colitis Organisation. Published by Elsevier B.V. All rights reserved.
épatogastroentérologie, Groupel.: +33 1 41 70 81 21; fax: +33 1fermeil.fr, snahon@club-intern

European Crohn's and Colitis14.01.023

t al, Diagnostic delay in a Fren.023

Hospitalier Intercommunal Le Raincy-Montfermeil, 10 avenue du Général41 70 81 94.et.fr (S. Nahon).

Organisation. Published by Elsevier B.V. All rights reserved.

ch cohort of Crohn's disease patients, J Crohns Colitis (2014), http://

mailto:[email protected]

mailto:[email protected]

http://dx.doi.org/10.1016/j.crohns.2014.01.023

http://dx.doi.org/



2 S. Nahon et al.

1. Introduction gangrenosum), disease location and phenotype according to

Crohn's disease (CD) is a chronic and disabling conditionleading to irreversible bowel damage over time. Due tounspecific symptoms and limited test accuracies, a diagnos-tic delay is frequent in CD. In the Swiss inflammatory boweldisease (IBD) cohort, the median diagnostic delay was9 months.1 Whether this result can be extrapolated toother countries such as France is unknown as this maydepend on the health care system.

Factors associated with diagnostic delay in CD are poorlyknown. In the Swiss IBD cohort, age b40 years and ileallocation were associated with diagnostic delay.1 A recentEuropean study showed that the rates of death and poorerself-assessments of health were substantially higher ingroups of lower socioeconomic status.2,3 The impact ofsocioeconomic deprivation on diagnostic delay is unknown ininflammatory bowel disease (IBD).4 The concept of earlytreatment to avoid later complications and the need forsurgery in CD, aligned to rheumatoid arthritis treatments, isgaining momentum.5–7 The identification of factors associ-ated with diagnostic delay may allow earlier therapeuticintervention that could changed the course of CD asdemonstrated by mucosal healing rates in the SONIC trial.8

The aim of this study was therefore to determine thediagnostic delay and to identify associated risk factors inFrench patients with IBD.

2. Patients and methods

All consecutive CD patients followed in two referral centers[Groupe Hospitalier Le Raincy-Montfermeil (suburbs of Paris)and Hopital Cochin (Paris)] were invited to participate in aprospective cohort after they gave informed consent.Clinical and socioeconomic characteristics of all consecutiveCD patients between September 2002 and November 2012were prospectively recorded using an electronic database(FileMaker Pro V 9.0).

2.1. Definition of diagnostic delay

Diagnostic delay was defined as the time period (months)from the first symptom onset to establishment of CDdiagnosis by the gastroenterologist. All consecutive patientsdiagnosed in our hospitals were asked about their symptomonset, and their diagnostic delay was recorded at diagnosis.In patients with CD diagnosis made elsewhere, diagnosticdelay was calculated on the base of patient's interview andthe medical chart.

Similarly to Vavricka et al.,1 we defined “a long diagnosticdelay” as the upper quartile of this time period.

2.2. Data collected

The following sociodemographic and characteristics of CDdata were collected: age, gender, marital, education andemployment status, family history of IBD, symptoms atdiagnosis (and the most relevant of them), extraintestinalmanifestation (peripheral arthritis, ankylosing spondylitis,aphthous stomatitis, uveitis, erythema nodosa, pyoderma

Please cite this article as: Nahon S, et al, Diagnostic delay in a Frenchdx.doi.org/10.1016/j.crohns.2014.01.023

Montreal classification, anoperineal lesions.Socioeconomic deprivation was assessed using the “Eval-

uation de la Précarité et des Inégalités de santé dans lesCentres d'Examens de Santé” (Evaluation of Precarity andInequalities in Health Examination Centers [EPICES]) scorecomputed on the basis of individual conditions of depriva-tion.6,9,10 The questions of the EPICES score are listed inAppendix A. The EPICES score was used as a quantitative oras a dichotomous variable with the EPICES median consid-ered as the cutoff value to divide the population into twosubgroups: the less deprived with a score of 30.17 and themore deprived with a score of N30.17. The questionnairewas administered since 2006 to all new diagnosis of CD. Forpatients diagnosed before 2006, the questionnaire wasadministered retrospectively.

We also collected birth country (France, Europe, NorthAfrica and others) as well as language understanding (poorversus good, according to the quality of the rephrasing bythe patient) assessed by gastroenterologists (SN, VA).

2.3. Statistical analysis

Analyses were conducted with long diagnosis delay as theprimary dependent variable. Variables were coded bothcategorically (sex, CD location, anoperineal lesion, etc.) andcontinuously (age, diagnostic delay, EPICES score, etc). Datawere expressed as mean ± standard deviation or as medianand range.

Univariate and multivariate analysis were performed tocompare the baseline characteristics of the group of patientswith long diagnosis delay to the others for the followingdata: age, gender, age at diagnosis, family history of IBD,extraintestinal manifestations, past history of appendecto-my, most relevant symptom, complications at diagnosis(occlusion, abscess, peritonitis), CD location and CD pheno-type, marital status, education, language understanding,birth country, geographic origin and EPICES score (ascore N 30.17 defined deprivation). The disease was classi-fied as of a disabling and/or severe disease when at leasttwo of the following disabling predictors defined byBeaugerie et al.11 were observed at diagnosis: age below40 years, active perianal disease and need for oral steroids.

For these analyses, we used Student's t test and ANOVAfor continuous data and the chi-square test or Fisher's exacttest for categorical data. Significant variables resulting fromunivariate analyses (P ≤ 0.20) were processed in a stepwisemultivariate model. Individual odds ratio (OR) and their 95%confidence intervals (CI) were computed for each variable. Atwo-tailed P value b0.05 was considered statisticallysignificant. Statistical analysis was performed by SPSSsoftware (version 18.0).

3. Results

3.1. Patient's characteristics at diagnosis

During the study period, the cohort comprised 390 patientswith Crohn's disease. A total of 364 patients with CD (40.8%men) were analyzed. Two hundred and forty-three patients(67%) had their CD diagnosis made in one of the two referral

cohort of Crohn's disease patients, J Crohns Colitis (2014), http://



3Diagnostic delay in a French cohort of Crohn's disease patients

centers (Montfermeil or Cochin Hospital). The meanage at diagnosis was 29.6 ± 13.1 years. Sociodemographicand clinical characteristics of the population at diagnosisaccording to diagnostic delay are presented in Table 1. CDlocation and phenotype are presented in Table 2. Most of thepatients had ileal location [L1, n = 132 (41.4%)], followed byileocolonic (L3, n = 107 33.5%) and colonic (L2, n = 80, 25.1%)location. One hundred and seventy-five patients (56.3%) hadnon-stricturing and non-penetrating behavior (B1), 92 (29.6%)had stricturing behavior (B2), and 44 (14.1%) had penetratingbehavior (B3) at diagnosis. Fifty-six patients (15.3%) hadperianal lesions at diagnostic, and 28 patients (7.7%) hadcomplications revealing CD (occlusion n = 22, intra-abdominalabscess n = 5, peritonitis n = 1).

3.2. Socioeconomic status

Sixty-two percent of the patients were active workers.Fifty-seven percent had high school graduation or higher.Sixty-six percent were married or in a couple.

Twenty-nine percent of the patients were deprived(EPICES score N 30.17). The EPICES score was not statisti-cally different between the two-referral centers (31% vs.25%, respectively; OR = 1.39, CI = 95% 0.84–2.30, p b 0.2).Twenty-two patients had poor language understanding.

3.3. Diagnostic delay

The median diagnostic delay was 5 months.2–12 Earlydiagnosis (first quartile) corresponded to a period below2 months from first symptoms to CD diagnosis. Late diagnosis(third quartile) was more than 12 months after the onset ofsymptoms.

3.4. Factors associated with a long diagnostic delay

None of the following factors were associated with a longdiagnostic delay: age at diagnosis, gender, family historyof IBD, CD location and behavior, past history of appendec-tomy, extra-intestinal manifestations, year of diagnosis,marital status, education, language understanding, birth

Table 1 Sociodemographic and clinical characteristics of the po

Total sample Delay b 12

Number of patients (data available) 364 275Sex ratio M/F (n = 364) 149/215 114/161Age (mean ± SD) 29.7 ± 13.9A1 b17 years 40 34 (12.3%)A2 (17–39 years) 267 197 (71.7%)A3 (N40 years) 57 44 (16%)Family history of IBD (344) 82 66 (24%)Active smoking (358) 110 83 (30%)Extraintestinal manifestations (341) 22 18 (5.6%)Past history of appendectomy (346) 104 72 (26.2%)Predominant symptomDiarrhea 169 127 (46.2%)Abdominal pain 69 57 (20.7%)Rectal bleeding 40 30 (10.9%)


country, geographic origin and socioeconomic deprivation(EPICES) score (Tables 1–3).

4. Discussion

Identifying predictors of diagnostic delay is an importantissue when managing chronic disabling and progressiveconditions such as rheumatoid arthritis and CD. In fact, asrecently observed in the Swiss IBD cohort,12 a diagnosticdelay might be associated with worse long-term outcomes(disability and bowel damage). Accordingly, an earlyintroduction of disease-modifying anti-IBD drugs (DMAIDs)13

should be considered in some CD patients with severedisease and/or poor prognostic factors according to ECCOconsensus.14

In this context, evaluating diagnostic delay and itsassociated factors in CD may have direct implications forour clinical practice; recently, in the Swiss IBD cohort, themedian time to diagnosis of CD was 9 months, and 75% of CDpatients were diagnosed within 24 months.1 Burisch et al.15

reported a median time to diagnosis of 4.6 months in theECCO-Epicom cohort (prospective European cohort of pa-tients with IBD). As the diagnostic delay may be influencedby the health care system, whether these data fromSwitzerland can be extrapolated to other countries isunknown. This study shows a suitable delay betweendiagnosis and first symptoms in patients with CD followedin two referral centers in France. The diagnosis was madewith a median time to diagnosis of 5 months and during thefirst year for 75% of the patients. This is in accordance withthe French population-based cohort EPIMAD, which recordsall incident cases of IBD since 1988 in northern France.16 Inthis cohort, the median interval between first symptoms anddiagnosis was 3 months for the entire period, with asignificant decrease in the proportion of intervals longerthan 9 months, from 28% in 1988–1990 to 22% in 2006–2007(p b 0.0001).16 Seventy-five percent of the patients werediagnosed within 8 months between first symptoms todiagnosis.1

In both the EPIMAD and the Swiss IBD cohorts, there was asignificant difference between CD and UC regarding diag-nostic delay.1,16 In the EPIMAD cohort, the median time to

pulation at diagnosis according to diagnostic delay.

months Delay N 12 months OR CI 95% p

8935/54 1.09 0.67–1.78 0.7229.96 ± 10.6 0.876 (6.7%) 0.5 0.2–1.23 0.1270 (78.6%) Reference – –13 (14.6%) 0.83 0.42–1.63 0.5916 (17.9%) 0.7 0.37–1.28 0.2427 (30.3%) 0.99 0.59–1.67 0.974 (4.5%) 1.49 0.49–4.52 0.4832 (35.9%) 1.44 0.87–2.4 0.16

42 (47.2%) 0.76 0.43–1.37 0.3612 (13.5%) 1.57 0.78–3.16 0.2010 (11.2%) 0.88 0.4–1.92 0.74




Table 2 Characteristics of the disease at diagnosis according to diagnostic delay.

Total sample Delay b 12 months Delay N 12 months OR CI 95% p

Number of patients (data available) 364 275 89CD location 319L1 132 98 (35.6%) 34 (38.2%) Reference – –L2 80 63 (22.9%) 17 (19.1%) 0.78 0.4–1.51 0.45L3 107 82 (29.8%) 25 (28%) 0.18 0.49–1.59 0.67L4 37 26 (9.4%) 11 (12.3%) – – –Anoperineal location 56 34 (12.4%) 22 (24.7%) 0.49 0.27–0.89 0.01Phenotype 311B1 175 138 (50.2%) 37 (41.5%) Reference – –B2 92 67 (24.4%) 25 (28.1%) 1.39 0.78–2.5 0.27B3 44 30 (10.9%) 14 (15.7%) 1.74 0.84–3.61 0.13B2 + B3 136 97 (35.3%) 39 (43.8%) 1.5 0.89–2.52 0.12Disabling disease a 201 153 (66.5%) 48 (58.5%) 1.41 0.84–2.36 0.19a Beaugerie L, Seksik P, Nion-Larmurier I, Gendre JP, Cosnes J. Predictors of Crohn's disease. Gastroenterology 2006; 130: 650–6.

4 S. Nahon et al.

diagnosis was 3 months for CD patients and 2 months for UCpatients, while in the Swiss IBD cohort, the median time todiagnosis was 9 months for CD and 4 months for UC(p b 0.001). Such discrepancy between CD and UC is likelyexplained by the fact that rectal bleeding in UC patientscauses them to consult their general practitioner orgastroenterologist earlier, whereas symptoms are oftenunspecific in CD. In our study enrolling only CD patients,rectal bleeding was not associated with an earlier diagnosiscompared with other symptoms such as diarrhea or abdom-inal pain.

Interestingly, we did not find any difference betweenpatients with long diagnostic delay (more than 12 months)and those with a shorter delay for the following parameters:CD location, CD behavior, complications (occlusion orabdominal abscesses) and the severity of the disease. In

Table 3 Socioeconomic status according to diagnostic delay.

Total sample Delay b 12 mo

Number of patients 364 275Deprivation 340 255(EPICES score a N30.17) 71 (27.8%)Education status 300 224High school graduation or higher 124 (55.4%)Marital status 326Married or in a couple 160Single 69Separated or divorced 17Employment status 324Working 143 (59.3%)Unemployed or disabled 44 (18.2%)Student 36 (14.9%)Retired 18 (7.4%)Language understanding (poor) 255 12 (6.1%)Birth country 335France 168 (66.9%)Europe 13 (5.2%)North Africa 61 (24.3%)Other 9 (3.6%)a Score of deprivation.


the study by Vavricka et al.,1 ileal location was associatedwith a longer time to diagnosis. The authors explained thisfinding by the fact that ileal location is more frequentlyrevealed by abdominal pain without diarrhea, which can beconfused with irritable bowel syndrome.1 We found a highrate (43.7%) of patients with stricturing or penetratingbehavior at diagnosis when compared to previous re-ports.17,18 This may explain why ileal location, which isknown to be the main site for disease complications, was notassociated with diagnostic delay in our study. Indeed,strictures and fistulas/abscesses are more often symptom-atic and more specific than uncomplicated CD.

In addition, we did not observe that CD patients withextraintestinal manifestation had an earlier diagnosis, asobserved in the Swiss cohort.1,19 Other physicians such asrheumatologists may be not well informed about the

nths Delay N 12 months OR CI 95% p

898527 (31.7%) 0.83 0.49–1.41 0.497647 (61.8%) 0.77 0.45–1.3 0.32

57 Reference19 0.77 0.43–1.4 0.394 0.66 0.21–2.05 0.46

59 (71.1%) Reference12 (14.4) 0.66 0.33–1.34 0.256 (7.2%) 0.4 0.16–1.01 0.056 (7.2%) 0.81 0.31–2.14 0.663 (5.2%) 0.84 0.23–3.08 0.79

51 (60.7%) Reference2 (2.4%) 0.51 0.11–2.32 0.5128 (33.3%) 1.51 0.88–2.61 0.133 (3.6%) 1.1 0.29–4.21 0.89




Questions Coefficient

1. Do you sometimes meet a social worker(welfare worker. educator)?

10.06

2. Do you have a complementary healthinsurance (mutual insurance)?

−11.83

3. Do you live as a couple? −8.284. Are you a homeowner or will you be one in thenear future?

−8.28

5. Are there periods in the month when you havereal financial difficulties to face your needs(food, rent, electricity)?

14.80

6. Have you done any sport activities in the last12 months?

−6.51

7. Have you gone to any shows (cinema,theatre) over the last 12 months?

−7.10

8. Have you gone on holiday over the last12 months?

−7.10

9. Have you seen any family member over thelast six months (other than your parents orchildren)?

−9.47

10. If you have difficulties (financial, family orhealth), is there anyone around you who couldtake you in for a few days?

−9.47

11. If you have difficulties (financial, family orhealth), is there anyone around you who couldhelp you financially (material aid such asmoney lending)?

−7.10

Intercept 75.14

5Diagnostic delay in a French cohort of Crohn's disease patients

possibility of having IBD in patients with digestive symptomsin France. This will require further investigation.

Studies have long shown inequalities in access to, andutilization of, healthcare services among patients of minor-ity race and reduced socioeconomic status.2–4 A recentEuropean study showed that the rates of death and poorerself-assessments of health were substantially higher ingroups of lower socioeconomic status.2–4 Because IBD careoften entails frequent visits to gastroenterologists, endoscopicexaminations and disease surveillance, equal access to, andutilization of, necessary services is of vital importance.4

Socioeconomic deprivation, which is associated with lessfrequent and later care, can result in belated diagnosis andtreatment in chronic disease and also in IBD.4,20 Only one studyfocused on the impact of socioeconomic deprivation on delayin diagnosis in IBD patients.21 In this small pediatric study,underinsured subjects had a nearly 4-fold longer delayin diagnosis of IBD than insured subjects.21 This is the firststudy evaluating the impact of socioeconomic deprivation ondiagnostic delay using a validated score of deprivation,namely, the EPICES score.10,11 In our work, socioeconomicdeprivation evaluated by the EPICES score was not associatedwith diagnostic delay in CD. We could also show thatsocioeconomic deprivation does not impact neither diag-nostic delay neither severity of CD in this cohort of FrenchCD patients.10,22

French healthcare is based on a compromise betweenegalitarianism and free market. All citizens are said to beequal, yet choice and competition are fiercely protected.Access to Health care is available to everyone withoutwaiting lists. The French patient pays their doctor's fee andthen claim back 75%–80%. As payment may deter the poorestpeople from seeking care, about 6 million people are exemptin France. Thus, patients with low socioeconomic statushave easy access to health care and treatment.

The main strength of this work is the assessment of thesocioeconomic deprivation by a validated questionnaire(EPICES score),9,10 as it is a major determinant of diagnosticdelay.

A limitation of this study is that in patients with a longhistory of symptoms before diagnosis or with CD diagnosismade outside our hospitals, a recall bias of symptom onset ispossible. It is noteworthy that patients enrolled in this studywere recruited from 2 different centers. The first hospitalis located in the suburbs of Paris (Montfermeil Hospital)and attracts a population of patients expected to bedisadvantaged, while the second hospital located in Paris(Cochin Hospital) attracts a population of less disadvantagedpatients. However, the EPICES score was not statisticallydifferent between the two-referral centers.

In conclusion, in this French cohort of CD patients,diagnostic delay was relatively short, being 5 months. Noneof the baseline characteristics, including socioeconomicdeprivation influenced diagnostic delay in our cohort.

Conflict of interest

All authors have no conflicts of interest or financial tiesrelevant to the manuscript to disclose.

Specific author contributions: (1) study concept anddesign, (2) acquisition of data, (3) analysis and interpretation


of data, (4) drafting of the manuscript, (5) critical revisionof the manuscript for important intellectual content, (6)statistical analysis, (7) technical or material support and(8) study supervision.

Stéphane Nahon: 1, 2, 3, 4 and 8; Pierre Lahmek: 3 and 6;Bruno Lesgourgues: 5 and 7; Cécile Poupardin: 2; StanislasChaussade: 4; Laurent Peyrin-Biroulet: 5; Vered Abitbol: 1,2, 3, 5 and 8.

Appendix A. Questions of the EPICES score andtheir coefficient.


EPICES: Evaluation de la Précarité et des Inégalités de santédans les Centres d'Examen de Santé.

Score calculation: each question coefficient is added tointercept whenever the answer is “yes.” A score equal to0 corresponds to non-deprivation; a score equal to 100corresponds to maximum deprivation.

Questions were translated from French to English.

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Diagnostic delay in a French cohort of Crohn's disease patients