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New criteria for inflammatory back pain in patients with chronic back pain: a real
patient exercise by experts from the Assessment of SpondyloArthritis international
Society (ASAS)
Sieper, J.; Van der Heijde, D.M.; Landewe, RB; Brandt, J.; Burgos-Vagas, R.; Collantes-
Estevez, E.; Dijkmans, B.A.C.; Dougados, M.; Khan, M.M.; Leirisalo-Repo, M; van der
Linden, S.C.; Maksymowych, W.P.; Mielants, H.; Olivieri, I.; Rudwaleit, M.
published in
Annals of the Rheumatic Diseases
2009
DOI (link to publisher)
10.1136/ard.2008.101501
document version
Publisher's PDF, also known as Version of record
Link to publication in VU Research Portal
citation for published version (APA)
Sieper, J., Van der Heijde, D. M., Landewe, RB., Brandt, J., Burgos-Vagas, R., Collantes-Estevez, E., Dijkmans,
B. A. C., Dougados, M., Khan, M. M., Leirisalo-Repo, M., van der Linden, S. C., Maksymowych, W. P., Mielants,
H., Olivieri, I., & Rudwaleit, M. (2009). New criteria for inflammatory back pain in patients with chronic back pain:
a real patient exercise by experts from the Assessment of SpondyloArthritis international Society (ASAS). Annals
of the Rheumatic Diseases, 68(6), 784-788. https://doi.org/10.1136/ard.2008.101501
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New criteria for inflammatory back pain in patients
with chronic back pain: a real patient exercise by
experts from the Assessment of SpondyloArthritis
international Society (ASAS)
J Sieper,
1
D van der Heijde,
2
R Landewe´,
3
J Brandt,
4
R Burgos-Vagas,
5
E Collantes-
Estevez,
6
B Dijkmans,
7
M Dougados,
8
M A Khan,
9
M Leirisalo-Repo,
10
S van der
Linden,
3
W P Maksymowych,
11
H Mielants,
12
I Olivieri,
13
M Rudwaleit
1
1
Rheumatology, Medizinische
Klinik I, Charite´ – Campus
Benjamin Franklin, Berlin,
Germany;
2
Leiden University
Medical Center, Leiden, The
Netherlands;
3
Maastricht
University Medical Center,
Maastricht, The Netherlands;
4
Rheumatology Private Practice,
Berlin, Germany;
5
Rheumatology
Department, Hospital General de
Mexico, Universidad Nacional
Autonoma de Mexico, University
of Mexico City, Mexico City,
Mexico;
6
University of Co´rdoba,
Co´rdoba, Spain;
7
VU Medical
Centre, Amsterdam, The
Netherlands;
8
Hospital Cochin,
Paris, France;
9
Case Western
Reserve University, MetroHealth
Medical Center, Cleveland, Ohio,
USA;
10
University Central
Hospital, Helsinki, Finland;
11
University of Alberta,
Edmonton, Alberta, Canada;
12
University Hospital, Ghent,
Belgium;
13
Ospedale San Carlo,
Potenza, Italy
Correspondence to:
Dr M Rudwaleit, Charite´–
Universita¨tsmedizin Berlin,
Campus Benjamin Franklin,
Rheumatologie, Medizinische
Klinik I, Hindenburgdamm 30,
12203 Berlin, Germany; martin.
rudwaleit@charite.de
Accepted 14 December 2008
Published Online First
15 January 2009
ABSTRACT
Objective: Inflammatory back pain (IBP) is an important
clinical symptom in patients with axial spondyloarthritis
(SpA), and relevant for classification and diagnosis. In the
present report, a new approach for the development of
IBP classification criteria is discussed.
Methods: Rheumatologists (n = 13) who are experts in
SpA took part in a 2-day international workshop to
investigate 20 patients with back pain and possible SpA.
Each expert documented the presence/absence of clinical
parameters typical for IBP, and judged whether IBP was
considered present or absent based on the received
information. This expert judgement was used as the
dependent variable in a logistic regression analysis in
order to identify those individual IBP parameters that
contributed best to a diagnosis of IBP. The new set of IBP
criteria was validated in a separate cohort of patients
(n = 648).
Results: Five parameters best explained IBP according to
the experts. These were: (1) improvement with exercise
(odds ratio (OR) 23.1); (2) pain at night (OR 20.4); (3)
insidious onset (OR 12.7); (4) age at onset ,40 years
(OR 9.9); and (5) no improvement with rest (OR 7.7). If at
least four out of these five parameters were fulfilled, the
criteria had a sensitivity of 77.0% and specificity of 91.7%
in the patients participating in the workshop, and 79.6%
and 72.4%, respectively, in the validation cohort.
Conclusion: This new approach with real patients
defines a set of IBP definition criteria using overall expert
judgement on IBP as the gold standard. The IBP experts’
criteria are robust, easy to apply and have good face
validity.
Chronic back pain is the leading symptom in
patients with axial spondyloarthritis (SpA) includ-
ing patients with ankylosing spondylitis (AS).
12
In
order to clinically differentiate back pain caused by
inflammation of the sacroiliac joints/lower spine
from other causes, attempts have been made to
describe and to define clinical criteria for this
specific kind of back pain, which has been termed
inflammatory back pain (IBP).
3–6
The following
clinical features have been proposed to be used in
different sets of criteria: (i) ‘‘back pain starting at
an age of less than 40 or 45 years’’, because the
disease usually starts in the third decade of life and
an onset after 45 years of age is exceptional;
7
(ii)
‘‘chronic back pain for longer than 3 months’’,
because acute back pain due to non-inflammatory
reasons is very commonly acute in onset and is
often self-limiting;
8
(iii) ‘‘insidious onset’’, because
mechanically caused back pain including disc
herniation or sciatica, for example, is frequently
of acute onset; (iv) ‘‘morning stiffness’’ (normally
of the low back); and (v) ‘‘improvement with
exercise, but not with rest’’ (either as single items
or in combinations as one item). Morning stiffness
of the affected musculoskeletal sites and improve-
ment with exercise are symptoms indicating
musculoskeletal inflammation, which are also
characteristic for other inflammatory rheumatic
diseases such as rheumatoid arthritis and poly-
myalgia rheumatica, although at different loca-
tions in these disease entities; (vi) ‘‘pain at night
(with improvement upon getting up)’’ results from
worsening of symptoms when patients are at
rest—a concept similar to that of morning stiff-
ness; and (vii) ‘‘alternating buttock pain’’, which
likely indicates active inflammation of the sacroi-
liac joints fluctuating from one side to the other,
but which has never been defined according to
temporal characteristics.
The Calin criteria
4
are the first and most
frequently used set of criteria for IBP, and they
have been utilised in the European
Spondyloarthropathy Study Group (ESSG) cri-
teria.
9
Modified definitions of IBP have been used
in the modified New York criteria for AS,
10
and also
in the Amor criteria for SpA.
11
. More recently, a
new set of criteria for IBP have been proposed
(Berlin criteria), based on a study in 101 patients
with AS and 112 control patients with mechanical
low back pain.
6
In general, criteria for IBP were
either derived from studies comparing patients
with AS with patients having back pain of other
(most often mechanical) origin, or from the
experience of single experts. Although IBP is
regarded as a typical clinical symptom for axial
SpA, its sensitivity and specificity with respect to
diagnosis of axial SpA does not exceed 80%.
4–6 12–15
Notwithstanding these limitations, the symptom
of IBP has been successfully used as a screening
parameter for axial SpA in young patients with
chronic low back pain seen by primary care
physicians or orthopaedists.
16
The Assessment of Spondyloarthritis Interna-
tional Society (ASAS) had started an international
project in 2004 to develop new classification
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criteria for axial and peripheral SpA. As part of this project,
international SpA experts met in Berlin in a real patient exercise
to personally investigate patients with possible SpA (via medical
history and physical examination). This exercise was under-
taken because it was felt that the patient–investigator interac-
tion was of pivotal importance since interpretation of
information elicited from patients is not only content depen-
dent but also investigator dependent. The experts had to make a
decision whether they consider the patients suffering from
inflammatory back pain or not, without knowledge about the
final diagnosis (SpA or no SpA). This set-up gave us the unique
opportunity to use the judgement of the expert(s) on the
presence or absence of IBP (and not on the diagnosis of SpA) as
the gold standard, and to statistically derive an optimal set of
IBP classification criteria referred to as ‘‘IBP according to
experts’’.
METHODS
In all, 13 international rheumatologists (all listed as coauthors
of this manuscript) from 9 countries in Europe and North
America who are considered experts in AS/SpA, are full
members of ASAS and who participate in the development of
new ASAS classification criteria for axial SpA met during a 2-
day workshop in Berlin. They obtained clinical history and
performed physical examination of 20 patients with chronic
back pain and suspected axial SpA. The experts had to make a
decision whether they considered the patients to be suffering
from IBP or not, without knowledge about the final diagnosis
(SpA or no SpA). All patients had presented previously to the
Rheumatology outpatient clinic of the Charite´ (Campus
Benjamin Franklin, Berlin, Germany) for diagnostic work-up
and were selected by the local organising rheumatologists (MR,
JS) who themselves did not assess patients in this workshop.
The 13 ASAS experts were divided into 4 groups: 3 groups of 3
experts and 1 group of 4 experts. During the 2 days each group
of experts interviewed and examined 10 patients with help of an
interpreter (6 patients on day 1, 4 patients on day 2; 1 expert
participated only on day 2, and, therefore examined only 4
patients). Each expert independently documented the presence
or absence of a given clinical symptom, a manifestation and a
laboratory or imaging finding. Crosstalk between experts and
discussion or interpretation of findings within the group of
experts was not allowed.
In addition to gender, age and duration of back pain, the
following clinical history items that are related to IBP were
assessed in a yes/no fashion: (1) age at onset ,40 years, (2)
duration of back pain .3 months, (3) insidious onset, (4)
morning stiffness of the back, (5) improvement with exercise,
(6) improvement with rest, (7) alternating buttock pain and (8)
pain at night with improvement upon getting out of bed. In
addition, each ASAS expert had to judge whether IBP was
present or absent in a given patient after taking the clinical
history.
Information on other clinical, laboratory and imaging
features was also collected by the experts as part of the
project to develop new classification criteria for SpA (data not
presented here). Importantly, IBP features including the
overall judgement on the presence of IBP were documented
prior to the assessment of other manifestations including the
physical examination, and prior to looking at radiographs and
MRIs, so that the expert IBP judgement was based solely on
the set of eight IBP questions and not on diagnosis, thereby
reducing possible bias.
Workshop patients
All patients had chronic back pain of unknown origin and, in
the opinion of the local rheumatologists, had clinical features
compatible with spondyloarthritis. According to the assess-
ments and judgements of the local rheumatologists 16/20
patients fulfilled the ESSG classification criteria,
9
and 8/20 had 6
or more (range 7–12) Amor points (reflecting definite SpA)
while a further 7/20 patients had 5 Amor points (reflecting
probable SpA).
11
Four patients did not fulfil the ESSG or the
Amor (6 points) criteria. Further demographic and clinical data
are shown in table 1. The study was approved by the local
ethical committee and informed consent was obtained from all
patients.
Validation study
The ‘‘IBP according to experts’’ criteria, which evolved from this
workshop, were validated in the international ASAS study on
new classification criteria for axial SpA. Similar to the expert
meeting in Berlin, individual IBP parameters as well as the
overall judgement on the presence of IBP were assessed by the
local rheumatologist in patients with chronic back pain of
unclear origin and onset of back pain ,45 years of age (n = 648,
mean age 33.6 years, male gender 44.5%, diagnosis of axial SpA
60.2%).
17
Data analysis
In total, 124 clinical judgements on IBP were available on the 20
patients from 13 experts (12 experts evaluated 10 patients each,
1 expert 4 patients only). Nine IBP judgements were missing,
and six IBP judgements were excluded from further analysis
because the expert could not decide on the presence or absence
of IBP. The remaining 109 expert judgements on IBP were used
for further analysis. For each patient and each IBP parameter
Table 1 Demographic and clinical data* of patients selected for
Assessment of Spondyloarthritis International Society (ASAS) workshop
Workshop patients (n = 20)
Age (years), mean (SD) 40.8 (10.7)
Male gender, n (%) 8 (40.0)
Duration of back pain (years), mean (SD) 6.9 (6.1)
IBP according to Calin et al, n (%) 15 (75.0)
IBP according to Rudwaleit et al, n (%) 14 (73.7)
Enthesitis of the heel, ever, n (%) 8 (40.0)
Peripheral oligoarthritis, ever, n (%) 6 (30.0)
Acute anterior uveitis, ever, n (%) 0
Dactylitis, ever, n (%) 2 (10.0)
Psoriasis, ever, n (%) 1 (5.0)
Inflammatory bowel disease, ever, n (%) 1 (5.0)
Family history of SpA, n (%) 6 (30.0)
Good response to NSAIDs, n (%) 16 (80.0)
HLA-B27 positive, n (%) 11 (55.0)
Elevated CRP, n (%) 5 (25.0)
Definite radiographic sacroiliitis according to
modified New York criteria, n (%)
3 (15.0)
Active inflammatory lesions on MRI of sacroiliac
joints, n (%)
9 (45.0)
Amor >6 points, n (%){ 8 (40.0)
Amor >5 points, n (%){ 15 (75.0)
ESSG criteria fulfilled, n (%) 16 (80.0)
*All clinical parameters including imaging results as assessed by the local organising
rheumatologist, before patients were seen by the ASAS experts; {6 or more Amor
points defines definite SpA; {5 or more Amor points defines probable or definite SpA.
Amor, Amor criteria
11
for SpA; CRP, C-reactive protein; ESSG, European
Spondyloarthropathy Study Group; HLA, human leukocyte antigen; IBP, inflammatory
back pain; NSAID, non-steroidal anti-inflammatory drug; SpA, spondyloarthritis.
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there were between 4–7 judgements. Concordance among
experts regarding individual IBP items was calculated as
following: first, concordance for a given IBP parameter was
calculated for each patient (expressed as 0–1). Second, the
concordance rates of all patients assessed for a given IBP
parameter were summed and then divided by the number of
patients (n = 20). The x
2
test was used for comparison of
proportions. Stepwise forward and backward logistic regression
analysis was applied to identify IBP parameters, which
independently contribute to IBP with the overall expert
judgement on IBP (present or absent) as binary outcome.
Since the 109 judgements were made by 13 experts and based on
20 patients, the 109 IBP judgements cannot be considered
independent judgements. We therefore also applied a multilevel
approach adjusting for patient dependence (level 1) and expert
dependence (level 2), using generalised estimating equations
(GEE) for binomial outcomes (conditional logistic regression
analysis). In that analysis, IBP judgement was the dependent
variable, and patient and expert were within-subject factors.
RESULTS
IBP was considered to be present in 61 of 109 (56%) expert
judgements. The frequencies of individual IBP parameters in
patients considered to have IBP and patients considered not to
have IBP are shown in fig 1. The concordance among experts
regarding IBP items was fairly high: 0.94 (age of onset), 0.95
(duration of back pain .3 months), 0.83 (insidious onset), 0.84
(pain at night), 0.89 (morning stiffness), 0.77 (improvement
with exercise), 0.72 (no improvement with rest) and 0.86
(alternating buttock pain). The concordance rate regarding the
global judgement on presence or absence of IBP was 0.83.
Logistic regression analysis revealed the following five
parameters to be independently contributory to IBP: (1)
improvement with exercise (odds ratio (OR) 23.1, 95% CI 3.5
to 154.4; p = 0.001), (2) pain at night (OR 20.4, 95% CI 3.5 to
118.8; p = 0.001), (3) insidious onset (OR 12.7, 95% CI 2.9 to
56.4; p = 0.001), (4) age at onset ,40 years (OR 9.9, 95% CI 2.1
to 47.1; p = 0.004) and (5) no improvement with rest (OR 7.7,
95% CI 1.8 to 33.3; p = 0.006). Three parameters were not
independently contributory to IBP: duration of back pain
.3 months (present in 96.6% vs 91.7% of IBP vs no IBP),
alternating buttock pain (present in 41.1% vs 10.9%) and
morning stiffness (present in 78.7% vs 41.7%). GEE analysis,
which adjusts for patient dependency and expert dependency,
revealed the same five parameters and gave almost identical
odds ratios (data not shown). Table 2 shows the five parameters
that independently contribute to IBP according to the ASAS
experts, and which form the new set of ‘‘IBP according to
experts’’ criteria.
The resulting sensitivities and specificities if >3/5, >4/5, or
all five parameters of the IBP expert criteria were present are
shown in table 3. The best trade-off between sensitivity and
specificity was found if >4/5 were fulfilled. We also compared
in the workshop patients the IBP expert criteria with the Calin
criteria
4
and with the IBP criteria by Rudwaleit et al,
6
using
again the expert opinion on presence or absence of IBP, and not
the diagnosis, as gold standard (table 3).
The new ‘‘IBP according to experts’’ definition was validated
in the international ASAS study on new classification criteria
for axial SpA (table 3). The sensitivity of the ‘‘IBP according to
experts’’ criteria (at least four of the five present) was similar in
the validation study as compared to the workshop patients
(79.6% vs 77.0%), whereas the specificity was somewhat lower
(72.4% vs 91.7%). The performance of the Calin criteria and of
the Berlin criteria in the validation study is also shown in table 3.
DISCUSSION
An unprecedented approach for the development of IBP
definition has been used in this study: firstly, a group of
internationally recognised experts with a longstanding reputa-
tion in the field of SpA and AS met in Berlin and personally
investigated patients with a possible diagnosis of SpA; and
secondly, the single expert’s judgement on whether IBP was
present or absent in a given patient was used as the gold
standard, not the final diagnosis of SpA. This latter aspect
importantly adds to the face validity of the herein proposed
ASAS expert’s IBP criteria.
Figure 1 Frequencies of individual
parameters of inflammatory back pain
(IBP) in patients considered by
Assessment of Spondyloarthritis
International Society (ASAS) experts to
have IBP and considered not to have IBP.
The frequencies of all IBP parameters
except the item ‘‘duration of back pain
.3 months’’ were statistically different
(p,0.05) between patients with and
without IBP.
Table 2 Inflammatory back pain (IBP) parameters, according to experts
Parameter Criteria
1 Age at onset ,40 years
2 Insidious onset
3 Improvement with exercise
4 No improvement with rest
5 Pain at night (with improvement upon getting up)
Sensitivity 77.0% and specificity 91.7% if at least four out of five parameters are
present. Note that sensitivity and specificity refer to the presence of IBP, not to
diagnosis.
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Although for practical reasons the number of experts and the
number of patients was limited in the workshop, 109
judgements on IBP were analysed. The high concordance rate
of the experts of between 0.72 and 0.95 for single IBP
parameters indicates that communication with the patients
was good and any language barrier (which was solved by
independent non-medical interpreters) was not a problem in
this exercise.
The herein presented new criteria for IBP do not reveal major
differences in comparison to other established IBP criteria. This
is not surprising because existing IBP criteria have been applied
all over the world in daily clinical practice for many years and
some of the participating experts have been involved in the
development of the other criteria. In fact, the new criteria
represent some sort of synthesis of existing criteria. The items
‘‘disease onset at an age ,40 years’’, ‘‘insidious onset’’ and
‘‘improvement with exercise’’ also represent three of the five
Calin criteria.
4
Interestingly, ‘‘morning stiffness’’ was substi-
tuted by ‘‘pain at night’’, which describes a somewhat similar
domain. As can be seen from fig 1, ‘‘morning stiffness’’ and
‘‘pain at night’’ were similar in regard to differentiation of IBP
from no IBP, though ‘‘pain at night’’ performed better in the
logistic regression analysis. Morning stiffness is a rather
frequent complaint in patients with any kind of back pain,
especially when the duration of the morning stiffness is not
quantified. The value of morning stiffness as an IBP parameter
seems to be better when there is a differentiation between
,30 min and .30 min, as was recently proposed by the Berlin
criteria,
6
, however, morning stiffness was not quantified in this
workshop.
The item ‘‘no improvement of back pain with rest’’ appeared
to be important to the experts and became part of the new IBP
criteria. In the modified New York criteria for AS
10
IBP was
defined in one single item as morning stiffness, improvement
with exercise but not by rest and symptom duration
.3 months. Additionally, in the Berlin criteria for IBP
‘‘improvement with exercise, but not with rest’’ was used as
one conditional item.
6
Since ‘‘improvement with exercise’’ and
‘‘no improvement with rest’’ as single items were independently
contributory to IBP according to our analysis we decided to use
them also independently in the new criteria. ‘‘Alternating
buttock pain’’, which is part of the Berlin criteria,
6
was not
independently contributory to IBP and, therefore, was not
included into the new expert criteria. Although ‘‘alternating
buttock pain’’ differentiates well between IBP and no IBP, a
limitation of this item seems to be its rather low prevalence of
around 40%, which was also the case in the previous study,
6
and
which makes this item of limited value in any criteria set.
The duration of ‘‘back pain .3 months’’, an item from the
Calin criteria, did not differentiate between IBP and no IBP
(fig 1). However, this was due to the selection of patients who
were chosen because of chronic low back pain. Thus, nearly all
patients with and without a final diagnosis of SpA had back
pain for longer than 3 months. In general, however, symptom
duration .3 months remains an important entry parameter in
less selected back pain patients before considering SpA as a
possible diagnosis and before assessing IBP.
13
Focussing on
patients with chronic back pain (.3 months) and young onset
in the application of IBP criteria has also been applied in other
studies.
616
Thus, the new IBP criteria are applicable in patients
with chronic low back pain (.3 months) and not necessarily in
patients with acute low back pain.
Using the expert judgment on IBP as the gold standard, the
Berlin criteria had a worse specificity (62.5%) than the Calin
criteria (73%) in the workshop patients, which may be
explained by the fact that two of the four items of the Berlin
criteria could not be accurately assessed in this exercise. These
two items were (a) morning stiffness .30 min (in the present
study morning stiffness was assessed only as yes or no) and (b)
pain at the second half of the night only. In the present study
only pain at night with improvement upon getting up was
assessed, without differentiation between the first and the
second half of the night.
The validation study on ASAS candidate classification criteria
for axial SpA
17
gave us the opportunity to validate the new ‘‘IBP
according to experts’’ criteria. In this large cohort of 648
patients with chronic back pain of unclear origin and age at
onset of back pain ,45 years, the ‘‘IBP according to experts’’
criteria (at least 4/5 present) showed a similar sensitivity of
79.6% (against IBP as gold standard, rather than diagnosis) but a
lower specificity of 72.4% which was still reasonably good. In
this validation study the Calin criteria had a higher sensitivity
Table 3 Sensitivity and specificity of the experts’ criteria for inflammatory back pain (IBP) in comparison
with other IBP criteria in the workshop patients (n = 20 patients) and in the Assessment of Spondyloarthritis
International Society (ASAS) validation study (n = 648 patients) against global expert judgement on presence
or absence of IBP
ASAS workshop* (n = 20 patients) ASAS validation study{ (n = 648 patients)
Sensitivity (%) Specificity (%) Sensitivity (%) Specificity (%)
IBP according to experts:
At least 3/5 present 91.8 56.3 95.1 47.5
At least 4/5 present 77.0 91.7 79.6 72.4
All 5/5 present 41.0 100 38.6 91.9
Calin criteria:{
At least 4/5 present 82.0 73.0 89.9 52.5
Berlin criteria:"
At least 2/4 present 83.6 62.5 70.0 81.4
Note that sensitivity and specificity refer to presence of IBP, not to diagnosis.
*ASAS Workshop patients: in total, 109 judgements on IBP were made by 13 experts in 20 patients; { ASAS validation study: in
total 648 judgements on IBP in 648 patients from 25 centres worldwide were made by the local rheumatologist; {Calin criteria
refers to IBP criteria by Calin et al,
4
which are fulfilled if at least 4 of the following 5 items are present: (1) age at onset ,40 years;
(2) back pain .3 months; (3) insidious onset; (4) associated with morning stiffness; (5) improvement with exercise; "Berlin
criteria refers to IBP criteria by Rudwaleit et al,
6
which are fulfilled if at least 2 of the following 4 items are present: (1) morning
stiffness .30 min; (2) improvement with exercise but not with rest; (3) awakening in the second half of the night because of back
pain; (4) alternating buttock pain.
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