# Diagnosis challenges in inception cohorts in axial spondyloarthritis: the case of the French national DESIR cohort

Anna Molto, Chris Serrand, Sandrine Alonso, Francis Berenbaum, Pascal Claudepierre, Bernard Combe, Laure Gossec, Adeline Ruyssen-Witrand, Alain Saraux, Daniel Wendling, et al.

► To cite this version:

Anna Molto, Chris Serrand, Sandrine Alonso, Francis Berenbaum, Pascal Claudepierre, et al. Diag-nosis challenges in inception cohorts in axial spondyloarthritis: the case of the French national DESIR cohort. RMD Open, 2024, 10 (3), pp.e004484. 10.1136/rmdopen-2024-004484. hal-04679093

HAL Id: hal-04679093

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Distributed under a Creative Commons Attribution 4.0 International License
Diagnosis challenges in inception cohorts in axial spondyloarthritis: the case of
the French national DESIR cohort

1. http://orcid.org/0000-0003-2246-1986Anna Molto1,2,

2. Chris Serrand3,

3. Sandrine Alonso3,

4. http://orcid.org/0000-0001-8252-7815Francis Berenbaum4,5,

5. http://orcid.org/0000-0003-1911-0544Pascal Claudepierre6,7,

6. http://orcid.org/0000-0003-4002-1861Bernard Combe8,

7. http://orcid.org/0000-0002-4528-310XLaure Gossec9,10,

8. Adeline Ruyssen-Witrand11,

9. http://orcid.org/0000-0002-8454-7067Alain Saraux12,

10. http://orcid.org/0000-0002-4687-5780Daniel Wendling13,

11. Thierry Lequerre14 and

12. http://orcid.org/0000-0003-3009-6229Maxime Dougados15

1. Correspondence to Dr Anna Molto; anna.molto@aphp.fr

Abstract

**Background** Inception cohorts aim to describe chronic diseases from diagnosis and over years of follow-up. Axial spondyloarthritis (axSpA) diagnosis might be challenging during the first years of the disease. Thus, identifying the features that will be associated with a confirmed diagnosis over time is key.

**Objectives** To assess the frequency and the predisposing factors for a change of an initial diagnosis in an inception axSpA cohort.

**Methods** DESIR is an ongoing national multicentre inception axSpA cohort with currently 12.5 years of follow-up. At the entry visit and confirmed at each visit, the diagnosis of axSpA was based on the opinion of the treating rheumatologist. Follow-up was interrupted in case of a change in this initial diagnosis. Multiple imputation was used to estimate the probability of a change in the initial diagnosis of axSpA for each patient lost to follow-up. Factors predisposing to an unchanged diagnosis of axSpA were then assessed using a multivariate logistic regression model on the imputed data sets.

**Results** Of the 708 patients included, over 10 years of follow-up, 45 (6.4%) were excluded due to a diagnosis change and 300 (42.4%) patients were lost to follow-up. Based on the imputation of these 300 patients, a change in their initial axSpA diagnosis was estimated in 42 (14.0%). Factors predisposing to an unchanged initial axSpA diagnosis during follow-up were (ORs (95% CIs)): radiographic sacroiliitis: 17.0 (4.1 to 71.0); psoriasis: 5.3 (2.0 to 14.3); CRP≥6 mg/L: 2.7 (1.3 to 5.3); good NSAID response: 2.5 (1.5 to 4.2); HLA B27+: 2.0 (1.3 to 3.3); anterior chest wall pain: 2.0 (1.2 to 3.3) and female sex: 1.9 (1.2 to 3.0).
**Conclusion** These data suggest that a change in diagnosis in recent onset axSpA exists, but is not frequent, and is less likely to occur in the presence of objective features at baseline.

WHAT IS ALREADY KNOWN ON THIS TOPIC

* Conventional disease description typically involves cross-sectional studies and retrospective analyses, often conducted in specialised centres, resulting in a bias towards more severe cases. This has led to a portrayal of axial spondyloarthritis (axSpA) as having a severe and poor prognosis, which can be distressing for newly diagnosed patients.

WHAT THIS STUDY ADDS

* This study, using data from the DESIR cohort, reveals that the diagnosis of axSpA can change in approximately 10% of cases over 10 years. It also shows that using classification criteria at baseline in such cohorts may exclude many patients, as a significant number will only meet the criteria during follow-up.

HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY

* Our findings suggest that including patients based on the treating physician's diagnosis in inception cohorts, despite its risk of changes, is a more inclusive approach. These data suggest that a change in diagnosis in recent onset axSpA exists, but is not frequent, and is less likely to occur in the presence of objective features at baseline.

Introduction

The conventional approach to describing a disease involves assessing the patient's condition at a specific point in time (eg, cross-sectional studies) and retrospectively examining its clinical features and natural history. However, these studies are typically conducted in specialised centres with expertise in the disease, resulting in a bias of capturing patients with more severe and refractory cases. The findings from these analyses are typically reported in traditional textbooks¹ and serve as the standard description or presentation of the disease for the medical community, including medical students. In the field of axial spondyloarthritis (axSpA), such studies have portrayed a rather severe and poor prognosis,² and this description can be distressing for patients who have recently received a diagnosis and are concerned about their long-term prognosis.

However, an alternative approach based on data from inception cohorts³ is now emerging. Inception cohorts involve the long-term prospective follow-up of patients who have been recently diagnosed with a disease.⁴,⁵ The advantage of these cohorts is that the data collected over time better reflect the long-term prognosis of patients encountered in everyday clinical practice. For instance, in rheumatoid arthritis, the 10-year outcomes of patients with recent-onset
synovitis suggestive of rheumatoid arthritis were found to be quite favourable,
with a significant proportion of patients maintaining an acceptable status
without any disability.⁶ Such information is reassuring for patients who have
recently received a diagnosis.

Some inception cohorts, namely for early RA, have used classification criteria
as their inclusion criteria,⁷,⁸ but more often, patients are rather included
according to the diagnosis from the treating rheumatologist.³,⁹ The reason for
this lies in the fact that classification criteria are usually very specific at the
cost of a lower sensitivity in particular at early stages of the disease.
Conversely, the use of the rheumatologist’s diagnosis as entry criteria is
considered more sensitive at the cost of a lower specificity. In clinical practice,
the initial diagnosis of axSpA has been reported to be challenging and can
change after several months or years of follow-up; thus, it seems crucial to be
able to identify the baseline features that will be associated with a consistent
diagnosis over time.

Given these preliminary considerations, we seized the opportunity provided by
the DESIR cohort, which followed patients with recent onset (axial
inflammatory symptoms for less than 3 years) axSpA for 10 years, to evaluate
(a) the frequency and the baseline predisposing factors of a change in the
entry visit initial diagnosis and (b) the impact of conducting a cohort based on
classification versus diagnostic criteria in this cohort.

## Patients: methods

### Patients

The DESIR cohort (NCT01648907) is currently ongoing and has been
previously described.¹⁰,¹¹ Briefly, consecutive patients aged 18–50 with
inflammatory back pain and a duration of ≥3 months and <3 years were
included in 25 centres in France if the treating rheumatologist considered the
symptoms highly suggestive of axSpA (a score ≥5 on a scale from 0 to 10,
where 0 indicated ‘not suggestive’ and 10 indicated ‘very suggestive’).
Between December 2007 and April 2010, 708 patients were included.

The investigators were asked to maintain all enrolled patients in the cohort
during the first 2 years of follow-up. Starting at year 2 and during all
subsequent visits up to year 10, the investigators had the opportunity to
exclude patients from the cohort if they were convinced that another diagnosis
than axSpA could explain the symptoms observed.

A detailed description of the study protocol is available on the DESIR website
(https://www.lacohortedesir.fr/: desir in English).

The research proposal for this particular analysis was approved in January
2022 by the scientific committee of the DESIR cohort. Patients were not
involved in the design, conduct, reporting or dissemination plans of our
research.

### Data collected
At baseline, the following variables were collected: demographics (age, gender), socioprofessional status, HLA B27 antigen and symptom duration.

During all visits (semiannually during the first 2 years and annually thereafter), the following variables were collected:

* Items to check if the patients fulfilled the axSpA criteria (Amor¹² and ASAS¹³).

* Past or present anterior chest wall pain (including date of onset and exact localisation since disease onset).

* Disease activity and severity parameters, including BASDAI (Bath Akylosing Spondylitis Disease Activity Index),¹⁴ ASDAS (Axial Spondyloarthritis Disease Activity Score),¹⁵ CRP (C-reactive Protein) and BASFI Bath Akylosing Spondylitis Functional Index).¹⁶

* Impact of the disease on the daily life of the patients, including ASAS HI (ASAS Health Index)¹⁷ and SF-36 (Short form Questionnaire 36).¹⁸

* Extrapspinal manifestations of the disease, including synovitis, dactylitis and enthesitis.

* Extramusculoskeletal manifestations of the disease, including psoriasis, uveitis and inflammatory bowel disease.

* Main comorbidities, including severe gastrointestinal events, hypertension, major atherosclerotic cardiovascular events, diabetes, cancer and infection (tuberculosis and other severe infections).

* Pharmacological treatment modalities, including NSAID (Non-steroidal Anti-inflammatory drugs) intake according to the ASAS-NSAID scoring system,¹⁹ conventional synthetic and targeted DMARDs Disease-modifying antirheumatic drugs).

* Requirement for surgical treatment modalities, including total hip replacement due to coxitis and spinal vertebrotomy.

* Socioprofessional status, including the number of days of sick leave and pension of invalidity,

## Statistical analysis

### Studied populations

This study includes three populations: 'confirmed', referring to patients who had a full 10-year follow-up with no change in diagnosis; 'other diagnosis', referring to patients who were excluded from the cohort due to a documented change in diagnosis during the follow-up (after year 2, as per protocol); and 'lost to follow-up', referring to patients who were lost at some point during the 10-year follow-up.

It is important to note that some patients classified as 'lost to follow-up' may have been lost due to a diagnosis change that could not be documented in the cohort, which may undermine the representativeness of estimates and
introduce selection biases when the factors affecting follow-up are associated
with outcomes.

To overcome this, multiple imputation by fully conditional specification was
performed and the probability of each ‘lost to follow-up’ patient being excluded
because of ‘other diagnosis’ was estimated.²⁰ Baseline clinical, biological and
radiological characteristics, as well as potential changes in baseline diagnosis
and the 10-year outcomes, were used to create 10 imputed datasets. To
estimate the proportion of lost to follow-up patients who would have been
excluded because of a ‘other diagnosis’, we arbitrarily chose to retain patients
who were classified as such in at least 7 out of the 10 imputation sets.

Characteristics of the patients at year 10 based on their status (‘confirmed’, ‘lost to follow-up’ and ‘other diagnoses’) are described. Quantitative variables are presented with their mean and SD or median with IQR, and qualitative variables with their frequency and associated proportions.

Furthermore, the probability of being lost to follow-up at each visit was
estimated by Kaplan-Meier survival curves.

Predisposing factors of a change in the baseline diagnosis of axSpA

In this analysis, the change in baseline diagnosis was defined as the
dependent variable, and all parameters collected at baseline were considered
independent variables. Variables were analysed through univariate and then
multivariate logistic regression on imputed datasets, and the results were
aggregated according to Rubin's rules.²⁰ Factors with a p value less than 0.20
in the univariate analysis were retained for the multivariate analysis. In the
multivariate analysis, a step-by-step backward selection was performed until
only significant factors remained. This process was repeated for the 10
imputed datasets, and variables that remained in at least 8 of the 10 models
(and not datasets) were included in the final aggregated model. The ORs with
their 95% CIs are presented.

Diagnosis versus classification criteria

The number and proportion of patients fulfilling at baseline the following axSpA
classification criteria: (Amor¹² and ASAS¹³ criteria) as well as the number and
proportion of patients fulfilling such criteria after 10 years of follow-up were
calculated in the ‘confirmed’ population.

All statistical analyses were performed by using SAS enterprise guide V.7.1
software.

Results

Patients and study course

The flow chart of the patients is summarised in figure 1. Of the 708 enrolled
patients, 45 were excluded from the cohort due to a change in the baseline
diagnosis by their treating rheumatologist. These 45 patients represent 6.4%
of the entire cohort and 12.4% of the number of patients who reached the 10-
year follow-up (ie, ‘confirmed’ patients). The diagnoses justifying the exclusion
of the patients from the cohort were as follows: mechanical back pain (n=30), fibromyalgia (n=13), a non-axSpA undifferentiated inflammatory rheumatic disease (n=1) and no information (n=1). During the 10-year follow-up period, three patients died due to the following causes: suicide (n=1), colorectal cancer (n=1) and cardiac arrest (n=1).

<figure><img src="image_2.png" /></figure>

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**Figure 1**

Flow chart of 708 patients with recent low back pain considered as having axSpA, over their 10-year follow-up in the Devenir des Spondyloarthrites Récentes (DESIR) cohort. *See the Methods section. We considered a patient as ‘estimated change in the baseline diagnosis’ in case a change in diagnosis was estimated in at least 7 out of the 10 imputed datasets. axSpA, axial spondyloarthritis.

Of the remaining 660 patients, 300 were lost to follow-up during the 10 years with the following estimations: 14.8% (95% CI 12.0% to 17.4%), 25.5% (95% CI 24.0% to 30.8%) and 45.7% (95% CI 41.8% to 49.4%) at the 2-year, 5-year and 10-year visits, respectively (online supplemental figure 1).

Supplemental material
[rmdopen-2024-004484supp001.pdf](rmdopen-2024-004484supp001.pdf)

In at least 7 (out of 10) multiple imputation data sets, 42 patients (5.9% of the entire cohort and 14.0% of the group of patients lost to follow-up) were
imputed as 'other diagnosis' (eg, suspected of a change in the axSpA baseline
diagnosis); considering these imputations, in total 87 patients (45 documented
changes in diagnosis and 42 estimated, according to the multiple imputation
results) (ie, 12.2% of the whole cohort) were estimated to be suffering from a
disease different than axSpA (online supplemental figure 2).

The baseline characteristics of the patients regarding these different
populations are summarised in [table 1].

• [VIEW INLINE](#)

• [VIEW POPUP](#)

**Table 1**

Baseline characteristics of the patients with regard to their status during
the 10-year follow-up period

Predisposing factors of a confirmed baseline diagnosis

Factors predisposing to an unchanged initial axSpA diagnosis during follow-up
were (ORs (95% CIs)): radiographic sacroiliitis: 17.0 (4.1 to 71.0); psoriasis:
5.3 (2.0 to 14.3); CRP≥6 mg/L: 2.7 (1.3 to 5.3); good NSAID response: 2.5 (1.5
to 4.2); HLA B27+: 2.0 (1.3 to 3.3); anterior chest wall pain: 2.0 (1.2 to 3.3) and
female sex: 1.9 (1.2 to 3.0) (table 2).

• [VIEW INLINE](#)

• [VIEW POPUP](#)

**Table 2**

Baseline predisposing factors of a maintained (no change) diagnosis of
axSpA during the 10-year follow-up period (results of the multivariate
analysis on the imputed datasets)

Diagnosis versus classification as entry criteria

The fulfilment of axSpA classification criteria (spondyloarthritis., Amor and ASAS criteria) regarding the patients' status during the 10-year follow-up period was evaluated: 21 (49%) and 16 (36%) out of the 45 patients with a documented change in diagnosis fulfilled the baseline Amor and ASAS criteria, respectively. The proportion of patients fulfilling these criteria in the 'confirmed' population went from 85% to 100% for the Amor criteria and from 68% to 83% for the ASAS criteria from baseline to year 10, respectively.
Discussion

These results provide insights into the pros and cons of selecting inclusion
criteria in an inception cohort. Based on the diagnosis by the treating
physician, there was a risk of changes in the baseline diagnosis over time,
which occurred in approximately 10%–15% of our cohort. Interestingly, when
examining the classification criteria, we observed the following: first, that a
significant proportion of patients whose treating physician changed the
diagnosis over time did actually meet the classification criteria at baseline
(47% and 36% for the Amor and ASAS criteria, respectively); and second, that
the percentage of patients meeting the classification criteria increased during
the 10-year follow-up period, suggesting that enrolling patients based on the
fulfilment of classification criteria would have excluded a significant number of
patients. These data confirm that the inclusion of patients in an inception
cohort should be based on the diagnosis by the treating physician, but the risk
of changes in the baseline diagnosis must be considered in subsequent
analyses and sample size estimations. Furthermore, and from a more clinical
point of view, these findings highlight that despite it has been suggested that
axSpA diagnosis can be challenging, in our cohort the final proportion of
persistent diagnosis over time was very high (ie, more than 85%).

Also, during the conduct of these analyses, we encountered the issue of
missing data due to patients being lost to follow-up during the study period. To
address this, we chose to use multiple imputations. This technique has the
advantage of using the full extent of available information and allows to
provide unbiased estimates under the assumption of data missing at random.²¹

²² However, since the results obtained are estimations based on observed
data, they may differ from reality. Moreover, the high number of missing data
and the rarity of some events prevented us from applying this approach to a
few outcomes, particularly those related to disease management during the
study period. Nonetheless, this imputation method is less prone to bias than
complete-case analysis.²³

Not surprisingly, baseline characteristics associated with a change in the
baseline diagnosis mirrored the parameters that have been reported to have a
higher likelihood ratio for diagnosis²⁴: B27 negativity, the absence of
radiographic-structural damage, poor or no response to NSAIDs, the absence
of psoriasis and the absence of anterior chest-wall pain. More intriguing and
unexpected were the association of the female gender with an unchanged
baseline diagnosis.

In summary, these data suggest that a change in diagnosis at the inclusion
visit and the risk of follow-up should be considered in inception cohorts but that
statistical models including multiple imputations could facilitate assessment of
the long-term prognosis of the disease despite these challenges.

Data availability statement
Data are available on reasonable request. The collected materials from DESIR are available for any researcher. The overall description of the cohort and the procedures of the application of a research project are summarised on the website: http://www.lacohortedesir.fr/desir-in-english/.

## Ethics statements

### Patient consent for publication

Consent obtained directly from patient(s).

### Ethics approval

This study involves human participants and DESIR cohort and its ancillary studies were approved by the Comité de Protection des Personnes—île de France IIIEUDRACT reference: 2007-A00608-45CPP, reference: 2457. Participants gave informed consent to participate in the study before taking part.

## Acknowledgments

The DESIR cohort is conducted with Assistance Publique-Hopitaux de Paris (AP-HP, Paris France) as the sponsor and under the umbrella of the French Society of Rheumatology. The DESIR cohort is run with the support of unrestricted grants from (in order of decreasing support) Pfizer France, Biogen, AbbVie, UCB, Lilly, Galapagos, Novartis, MSD, Fresenius and Celltrion HealthCare. We thank the Clinical Research Unit Paris Centre (AP-HP, Paris France), and the Institut national de la santé et de la recherche medicale (Inserm). We also thank the investigators: Pr Maxime Dougados, Pr André Kahan, Dr Julien Wipff and Dr Anna Molto (Paris-Cochin), Pr Olivier Meyer, Pr Philippe Dieudé (Paris-Bichat), Pr Pierre Bourgeois, Pr Laure Gossec (Paris-La Pitie-Salpétriere), Pr Francis Berenbaum (Paris-Saint-Antoine), Pr Pascal Claudepierre (Creteil), Pr Maxime Breban, Pr Maria-Antonietta D'Agostino, Pr Félicie Costantino (Boulogne-Billancourt), Pr Michel De Bandt, Dr Bernadette Saint-Marcoux (Aulnay-sous-Bois), Pr Philippe Goupille (Tours), Pr Jean-François Maillefert (Dijon), Pr Xavier Puechal, Dr Emmanuelle Dernis (Le Mans), Pr Daniel Wendling, Pr Clément Prati (Besançon), Pr Bernard Combe, Pr Cédric Lukas (Montpellier), Pr Liana Euller-Ziegler, Pr Véronique Breuil (Nice), Pr Pascal Richette (Paris Lariboisière), Pr Pierre Lafforgue, Pr Thao Pham (Marseille), Pr Patrice Fardellone, Dr Patrick Boumier, Dr Pauline Lasselin (Amiens), Pr Jean-Michel Ristori, Pr Martin Soubrier, Pr Anne Tournadre (Clermont-Ferrand), Dr Nadia Mehsen (Bordeaux), Pr Damien Loeuille (Nancy), Pr René-Marc Flipo (Lille), Pr Alain Saraux (Brest), Pr Corinne Miceli, Dr Stephan Pavy (Le Kremlin-Bicêtre), Pr Alain Cantagrel, Pr Adeline Ruyssen-Witrand (Toulouse), Pr Olivier Vittecoq, Pr Thierry Lequerre (Rouen).

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