Graefes Arch Clin Exp Ophthalmol

DOI 10.1007/s00417-014-2772-6

INFLAMMATORY DISORDERS

Acute anterior uveitis and undiagnosed spondyloarthritis:

usefulness of Berlin criteria
Jean Wach & Delphine Maucort-Boulch & Laurent Kodjikian &
Jean Iwaz & Christiane Broussolle & Pascal Sève

Received: 18 March 2014 / Revised: 15 July 2014 / Accepted: 5 August 2014

# Springer-Verlag Berlin Heidelberg 2014

Abstract and the ASAS classification criteria for spondyloarthritis were

Purpose Inflammatory back pain, the main symptom in
spondyloarthritis, is defined by the presence of two or more
positive responses among the four items of Berlin Criteria.
This study assesses the value of these criteria in detecting
previously undiagnosed spondyloarthritis after an episode of
acute anterior uveitis.
Methods Records of patients addressed for etiological diag-
nosis after an acute anterior uveitis (April 2006 to November
2013) were retrospectively analysed. Patient characteristics,
the presence of back pain, Berlin Criteria, the final diagnosis,
Preliminary results of this study were presented during the 66th congress
of the French Society of Internal Medicine (Nice, December 2012) and
during the 119th congress of the French Society of Ophthalmology (Paris,
May 2013)
J. Wach : D. Maucort-Boulch : L. Kodjikian : J. Iwaz :
C. Broussolle : P. Sève
Université Claude Bernard Lyon I, Lyon, France
J. Wach
Rheumatology Department, Centre Hospitalier Lyon-Sud, Hospices
Civils de Lyon, Pierre-Bénite, France
D. Maucort-Boulch : J. Iwaz
Service de Biostatistique, Hospices Civils de Lyon, Lyon, France
D. Maucort-Boulch : J. Iwaz
CNRS, UMR5558, Laboratoire de Biométrie et Biologie Evolutive,
Equipe Biostatistique-Santé, 69100 Villeurbanne, France
L. Kodjikian
Ophthalmology Department, Hôpital de la Croix-Rousse, Hospices
Civils de Lyon, Lyon, France
C. Broussolle : P. Sève (*)
Internal Medicine Department, Hôpital de la Croix-Rousse, Hospices
Civils de Lyon, 103 Grande Rue de la Croix-Rousse, 69317, Lyon
Cedex 04, France
e-mail: pascal.seve@chu-lyon.fr
collected and analysed.
Results The study included 102 patients (59.8 % women).
The mean age was 44.5 years. Uveitis cases were mainly
unilateral (73.5 %) and recurrent (58.8 %). Twenty-one pa-
tients had some type of spondyloarthritis, 20 fulfilling retro-
spectively the ASAS criteria. Back pain with at least two
positive items from Berlin Criteria was 61.9 % sensitive and
97.5 % specific in diagnosing spondyloarthritis. Considering
only one positive item increased the sensitivity (90.5 %) but
decreased the specificity (91.4 %).
Conclusions Acute anterior uveitis may be the key symptom
that reveals a formerly undiagnosed spondyloarthritis. A re-
ferral to a rheumatologist should be considered in presence of
back pain, even without fulfilment of the classical definition
with Berlin Criteria.
Keywords Anterior uveitis . Spondylarthropathies . Back
pain . Diagnosis
Introduction
Uveitis includes a large range of aetiologies, which may each
require a specific treatment. The diagnostic strategy is thus
essential; it is usually guided by the anatomic localisation of
the inflammation and also by potential associated signs [1, 2].
Still, a large proportion of uveitis cases remains idiopathic.
Spondyloarthritis (SpA) is the most frequent systemic dis-
ease associated with anterior uveitis [3]. Inversely, uveitis is
the most frequent non-rheumatologic symptom among pa-
tients with SpA; it affects approximately one third of them
[4, 5]. In this population, uveitis is classically anterior
(90.5 %), acute (88.7 %), unilateral (87.3 %), and, in half of
the patients, recurrent [4].

The spectrum of SpA comprises classically: ankylosing
spondylitis (AS), psoriatic arthritis, spondyloarthritis associ-
ated with inflammatory bowel disease, reactive arthritis, and
undifferentiated SpA (i.e., a presentation with typical features
of SpA but no criteria for one of the previous four subtypes)
[6–8]. SpA is thus one of the most common rheumatic dis-
eases, with an estimated prevalence of 0.5–1.9 % [9].
AS, the leading disease of this spectrum, may evolve into
functional disability, mainly because of a restricted mobility of
the axial skeleton. The diagnosis of AS is often made 8–11
years after the onset of the symptoms [9]. Indeed, rheumato-
logic symptoms such as back pain or arthralgia may often be
overlooked as non-specific. Furthermore, the Modified New
York Criteria for AS require an unequivocal radiographic
sacroiliitis, which often appears late in the course of the
disease. AS and undifferentiated SpA with predominant axial
involvement but without radiographic sacroiliitis are now
considered as the same disease entity but at different stages
of development, and are referred to as axial SpA [9, 10]. New
classification criteria published by the Assessment of
SpondyloArthritis International Society (ASAS) in 2009 were
developed to enable an earlier diagnosis of SpA [11] and,
consequently, allow earlier initiation of an effective treatment
mainly based on physiotherapy and NSAIDs, plus, if neces-
sary, anti-TNF therapy. The expected outcomes are a reduced
disease burden and a lower risk of disability.
Since uveitis may be the first notable specific clinical
manifestation [12–14], ophthalmologists can play a central
role in diagnosing SpA. However, the subgroup of patients
that should be referred to a rheumatologist or have an ad-
vanced diagnostic investigation, such as a MRI of the pelvis,
remains to be determined.
Inflammatory back pain (IBP), defined (in opposition
to mechanical back pain) as back pain associated with
axial SpA, is the leading rheumatologic symptom of
SpA. Several sets of criteria for IBP were proposed for
detecting patients affected by SpA among patients with
chronic back pain, because no single parameter was found
sufficient. According to Berlin Criteria, IBP is defined by
at least two positive responses among four items: 1)
morning stiffness >30 min of duration, 2) improvement
in back pain with exercise but not with rest, 3) awakening
because of back pain during the second half of the night
only, and 4) alternating buttock pain [15].
In a cohort of patients with anterior uveitis, a recent
study has reported an important prevalence (46.8 %) of
self-reported IBP as defined by Berlin Criteria [16]. In the
subgroup of 25 patients that underwent a rheumatologic
assessment, the classification of IBP was 92 % sensitive
and 67 % specific for the diagnosis of AS or of undiffer-
entiated SpA. The objective of present study was thus to
evaluate the ability of Berlin Criteria to recognize undiag-
nosed SpA in a population of acute anterior uveitis.
Graefes Arch Clin Exp Ophthalmol
Materials and methods
Patients
This retrospective chart review considered for inclusion pa-
tients with non-granulomatous acute anterior uveitis (accord-
ing to the SUN classification) [1], sent for diagnosis to the
Department of Internal Medicine at Croix-Rousse Hospital
(Lyon, France) between April 2006 and September 2013.
The study excluded all patients with former diagnosis of
SpA. The ethical review board of the University of Lyon
approved the study; informed consent was not required.
Clinical assessment
At the initial visit, a face-to-face interview followed by a
physical examination was conducted. Each patient report
was retrospectively reviewed for demographic data (age at
initial visit, sex, ethnic group), ophthalmologic characteristics
(laterality, recurrence, associated features), final diagnosis,
history of chronic back pain, and Berlin Criteria for IBP in
patients with chronic back pain. The ASAS classification
criteria for SpA were also retrospectively checked.
Whenever available, biologic (search for HLA-B27 antigen)
and radiographic data (conventional radiograph and/or MRI
of the pelvis) were also examined.
Statistical analysis
SpA and non-SpA patient characteristics were compared
using Mann and Whitney tests for continuous variables and
Pearson’s Chi-squared tests for categorical variables.
To evaluate the statistical performance of back pain in
diagnosing SpA (pain alone or in association with various
numbers of Berlin Criteria), the analysis estimated the sensi-
tivity, specificity, positive and negative likelihood ratio of pain
alone and each pain-criteria association.
Tests with a p-value less than 5 % were considered as
significant. The analyses were performed with R software
(version 2.15, http://cran.r-project.org/).
Results
Among the 102 patients with acute anterior uveitis included in
this study, 21 were finally diagnosed with some type of SpA:
ten AS, nine undifferentiated SpA, one psoriatic arthritis, and
one SpA associated with inflammatory bowel disease. The
other diagnoses were HLA-B27-associated uveitis (n=23),
ulcerative colitis (n=2), sarcoidosis (n=5), Parry–Romberg
syndrome (n=1), cryopyrinopathy (n=1), giant cell arteritis
Graefes Arch Clin Exp Ophthalmol

(n=1), Behcet’s disease (n=1), and idiopathic anterior uveitis
(n=47).
The patients’ clinical characteristics are presented in
Table 1. The mean age at uveitis onset was 44.5 years (range:
16–86). The patients were mostly women (59.8 %) and
Caucasian (81.4 %). Anterior uveitis was unilateral in
73.5 % of the cases, and recurrent in 58.8 %. None of the
studied variables, especially the ocular characteristics, were
found to be statistically significantly different between SpA
and non-SpA patients.
Among the 21 patients with SpA, 20 fulfilled retrospec-
tively the ASAS classification criteria for SpA (19 for axial
SpA and one for peripheral SpA). The 21th patient had no
back pain but a unilateral buttock pain with radiographic
sacroiliitis. Sixteen were HLA-B27-positive.
Thirty-nine patients reported chronic back pain: 19 SpA
and 20 non SpA (Table 2). Nineteen of the 20 patients with
chronic back pain but without SpA were tested for HLA B27,
and only two were positive.
A radiograph of the pelvis was performed in 54 patients: 18
of the 21 SpA patients, 14 of the 20 non SpA patients suffering
from chronic back pain, and 22 of the 61 non SpA patients
without chronic back pain. Defined sacroiliitis (≥stage 2 bi-
lateral or≥stage 3 unilateral) was only observed in the SpA
group (ten patients). Six of the eight SpA patients with normal
radiograph underwent a MRI of the pelvis, and five had pre-
radiographic active sacroiliitis on MRI (i.e., bone oedema)
that confirmed the diagnosis of SpA. The latter had pre-
radiographic erosions as sequela of previous sacroiliitis with-
out defined active lesions. Of the three SpA patients without
any available radiograph, one had a computed tomography
showing sequela of sacroiliitis, another an MRI showing
active sacroiliitis, and the last had peripheral SpA.
The statistical parameters associated with the use of Berlin
Criteria at different thresholds for the diagnosis of SpA are
summarized in Table 2. The presence of back pain alone had
90.5 % sensitivity and 75.3 % specificity. The conventional
threshold (i.e., back pain plus a minimum of two positive
Berlin Criteria items) increased the specificity up to 97.5 %
but decreased the sensitivity down to 61.9 %. The use of back
pain plus only one positive item had intermediate performance
values: 90.5 % sensitivity and 91.4 % specificity. The ROC
curve is shown in Fig. 1. The area under the ROC curve was
0.92 (95 % CI: 0.84–1).
Discussion
The main purpose of the present study was to assess the ability
of Berlin Criteria to detect undiagnosed SpA in a population
of acute anterior uveitis, which represent here 20.6 % of all
patients. Classically, IBP is defined by at least two positive
Berlin items [15], but the present results suggest that this
threshold should be lowered in patients with anterior uveitis
because, as suggested by the ROC-curve analysis, back pain
plus only one positive item had the most interesting balance
between sensitivity (90.5 %) and specificity (91.4 %) in
diagnosing SpA patients with a high probability. In addition,
positive and negative likelihood ratios (10.47 and 0.10 respec-
tively) illustrate the relevance of this threshold. Chronic back
pain alone had also a high sensitivity (90.5 %) but a lower
specificity (75.3 %).

Table 1 Characteristics of the

patients Characteristics Patients (n=102) SpA (n=21) Non-SpA (n=81) P-value

General, n (%)
Mean [SD*] age (years) 44.5 [15.0] 41.2 [13.0] 45.3 [15.5] 0.31
Sex
Females 61 (59.8) 14 (66.7) 47 (58.0) 0.62
Males 41 (40.2) 7 (33.3) 34 (42.0)
Race
Caucasian 83 (81.4) 19 (90.5) 64 (79.0) 0.75
Black 5 (4.9) 1 (4.8) 4 (4.9)
North-African 12 (11.8) 1 (4.8) 11 (13.6)
Asian 2 (2.0) 0 2 (2.5)
Ophthalmologic, n (%)
Unilateral involvement 75 (73.5) 18 (85.7) 57 (70.4) 0.18
Recurrence 60 (58.8) 12 (57.1) 48 (59.3) 1
Elevated IOP 11 (10.8) 3 (14.3) 8 (9.9) 0.69
Synechia 17 (16.7) 5 (23.8) 12 (14.8) 0.335
IOP intraocular pressure, SpA Hypopion 8 (7.8) 0 (0) 8 (9.9) 0.20
spondyloarthritis
Vitritis 10 (9.8) 2 (9.5) 8 (9.9) 1
* SD: standard deviation
 Graefes Arch Clin Exp Ophthalmol

Table 2 Statistical performance of back pain, alone or in association with various numbers of Berlin Criteria, for diagnosing SpA

Associations All patients SpA Sensitivity Specificity Positive LR Negative LR

(n=102) (n=21)

Back pain 39 19 90.5 [77.9–100] 75.3 [65.0–84.7] 3.66 0.13

Back pain with≥1 criterion 26 19 90.5 [77.9–100] 91.4 [85.2–94.7] 10.47 0.10
Back pain with≥2 criteria 15 13 61.9 [41.1–82.7] 97.5 [94.1–100] 25.07 0.39
Back pain with≥3 criteria 9 9 42.9 [21.7–64.0] 100 – 0.57
Back pain with 4 criteria 5 5 23.8 [5.6–42.0] 100 – 0.76

Sensitivity and Specificity are expressed in percentages with 95 % confidence intervals. SpA Spondyloarthritis, LR likelihood

Berlin criteria were initially designed to detect SpA among chronic back pain and not only those presenting IBP accord-
the large number of patients with chronic back pain in the ing to the classical definition.
general population [15]. Therefore, it may not be surprising In this study, one fifth of the patients presented an undiag-
that these criteria do not have the same relevance when nosed SpA, which, in agreement with previous studies, con-
applied in the very selective population of anterior uveitis firms that uveitis may be the key symptom that prompts the
patients, which is at higher risk of presenting SpA. Indeed, diagnosis of an unknown SpA [12–14]. In a group of 394
the sensitivity and specificity of anterior uveitis to detect SpA uveitis patients, Fernández-Melón et al. reported 18 % SpA,
patients from patients with other musculoskeletal diseases is among which 41 % newly diagnosed cases after the episode of
estimated at 32 and 95 %, with a positive likelihood ratio of uveitis [12]. No difference in the clinical pattern of uveitis was
6.4 [9]. While the prevalence of SpA in chronic back pain observed between previously diagnosed and undiagnosed
patients is approximately 5 % [9], here almost half of the SpA patients. In another cohort of 514 patients with anterior
patients reporting chronic back pain finally had a diagnostic uveitis, the prevalence of SpA was 22.7 %, with 53 % of
of SpA (Table 2). previously unknown cases [13]. Monnet and al. reported
These results present some contradictions with the study of 77.7 % of SpA cases in 175 patients with HLA-B27-
Chan et al., who recently determined the prevalence of IBP associated uveitis, and found that 64 % of cases were only
according to Berlin Criteria in a population of anterior uveitis diagnosed at the time of uveitis episode [14]. According to the
patients diagnosed between September 2000 and March 2008 latter authors, the first attack of uveitis appears generally after
[16]. Among 141 responders, 66 (46.8 %) were diagnosed by the first rheumatologic symptoms with an average delay of
self-reported questionnaire as having IBP (back pain plus a 7.6±10.5 years. Indeed, in the DESIR cohort of 708 patients
minimum of two positive items). In a sample of 25 patients, with recent IBP (<3 years) suggestive of SpA, 8.5 % had at
whom may not be representative of the studied population
since a higher proportion reported IBP (64 % vs 46.8), the
sensitivity and specificity of Berlin Criteria in diagnosing SpA
were 92 % and 67 % respectively. In contrast, we report here a
prevalence of IBP defined as back pain with≥2 positive Berlin
Criteria items of only 13.9 % and a sensitivity and specificity
in diagnosing SpA of 61.9 % and 97.5 % respectively. This
difference may have several explanations. First, Chan’s study
used self-reported questionnaires, which would have encour-
aged the participation of patients with back pain more than
those who were asymptomatic. Second, it used for each ques-
tion the formulation « do you ever have… », which may have
also increased the number of positive answers because the first
three questions of Berlin Criteria refer to regular rather to
occasional characteristics of the pain. Finally, Chan and al.
included patients at a distance from the episode of uveitis, and
so did not explore the diagnostic value of Berlin Criteria at the
time of first evaluation. Overall, we believe that the present
results extend Chan’s conclusions, and suggest that referral to
a rheumatologist should be considered for every patients with Fig. 1 ROC curve
Graefes Arch Clin Exp Ophthalmol
least one episode of uveitis at the time of inclusion [17]. Sixty-
three percent of uveitis cases occurred after or at the time of
the first sign of IBP.
Since the anatomic type of uveitis guides the diagnosis
investigations [2], we only included anterior uveitis, which
are far the most frequent type of uveitis in SpA patients [4].
We also logically excluded granulomatous uveitis since they
are exceptionally associated with SpA [2]. The prevalence of
SpA, HLA-B27 associated and idiopathic uveitis is consistent
with previous studies [12, 13, 16].
The clinical pattern of uveitis among patients with SpA in
our study reflects the classical feature: mostly unilateral
(85.7 %) and recurrent (57.1 %) [4, 12, 13]. However, ocular
characteristics do not allow any distinction between SpA and
non-SpA patients (Table 1).
The presence of HLA-B27 may be a common genetic
feature between anterior uveitis and SpA. Among 96 patients
tested, 42.7 % were HLA-B27 positive, as expected [18].
Nonetheless, Linssen and al. suggested that acute anterior
uveitis and AS are associated diseases, even irrespective of
the presence of HLA-B27 [19]. Indeed, in our study, five SpA
patients (23.8 %) were HLA-B27 negative (all SpA patients
having been tested). Thus, screening for SpA should not be
limited to HLA-B27 positive patients.
We observed more women in the SpA group, with a sex
ratio of 0.50 versus 0.72 in the non-SpA group, which may
appear to be in contradiction with the traditional male pre-
dominance in AS. However, it is consistent with the recently
published DESIR cohort which reported 54 % of women in a
population of early IBP according to Berlin or Calin Criteria
[20]. In this cohort, 60 of the 708 IBP patients had a previous
episode of uveitis, and 58.3 % were women [17]. Even if the
influence of gender on extra rheumatologic symptoms among
SpA is still a matter of debate, Zeboulon and al. reported in
their systematic literature review that women with SpA were
more likely to be affected by uveitis than men (33.3 % versus
28.5 %; odds ratio 1.3) [4].
Although the ASAS “IBP according to expert criteria”
were more recently published and are part of the ASAS
classification criteria for SpA [11, 21], we used Berlin
Criteria because they are routinely used in the study
Department since their publication in 2006. Besides, two
items of the ASAS criteria (namely, “type of onset” and
“age at onset”) were not accurate in most patient records.
Furthermore, the ASAS recommends using either Berlin
Criteria or the so-called “according to expert” Criteria for
establishing a diagnosis of IBP [22].
Despite their importance for the diagnosis of SpA in
anterior uveitis patients, the present results have a number
of limitations. First, a referral bias cannot be excluded
because the study department belongs to a major
University hospital. Second, a classification bias may be
suspected because the diagnoses of SpA were made at the
discretion of the physician, but this bias is highly improb-
able, because only two SpA patients did not retrospec-
tively fulfil the currently recommended ASAS criteria for
axial SpA. The first patient presented a unilateral buttock
pain (without real back pain) with radiographic
sacroiliitis, and the other had a peripheral SpA.
However, no patient in the non-SpA group was found to
be positive for the ASAS criteria for axial SpA.
The present results confirm that acute anterior uveitis is
often a presenting symptom of SpA. The classical definition
of IBP according to Berlin Criteria, initially designed to detect
SpA among patients suffering from chronic back pain, seems
to be inadequate in this population. We thus propose that
chronic back pain, even without classical definition of IBP,
should be considered as suggestive of SpA and lead to a
referral to a rheumatologist. Patients with back pain and only
one item of Berlin criteria should be considered to be at high
probability of having SpA and then, have extensive investi-
gation if necessary. This proposition should be further vali-
dated by the results of a prospective study of a well-defined
diagnostic strategy.
Competing interest The authors declare no competing interests.
Financial support Study performed at Hospices Civils de Lyon, Quai
des Célestins, 69288 Lyon Cedex 02, France. No financial support.
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