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Clinical and Experimental Rheumatology 2009; 27: 691-694.
Paediatric rheumatology
Tarsitis as an initial manifestation of juvenile
spondyloarthropathy
C. Álvarez-Madrid1, R. Merino1, J. De Inocencio2, J. García-Consuegra1
1Paediatric Rheumatology Unit, University Hospital La Paz, Madrid, and 2CS Jazmin and
University Hospital La Paz Foundation for Biomedical Research, Madrid, Spain.
Abstract
Objective
The aim of this study was to determine the frequency of tarsitis as one of the first symptoms of juvenile
spondyloarthropathy (JSpA) and to analyze whether patients with tarsitis at onset differ from those without it.
Methods
A retrospective chart review was performed, from January 1996 to September 2007, at a paediatric rheumatology unit
of a tertiary university hospital.
Results
Tarsitis was detected in one-third of the children diagnosed with JSpA. They had fever and received antibiotics due to a
suspected infection more frequently than those without tarsitis. Inflammatory low back pain was extremely unusual among
these patients.
Conclusion
There were some differences between children diagnosed with JSpA initially affected with tarsitis and those without it.
Patients with tarsitis as one of the first symptoms were often misdiagnosed as soft tissue infections.
Key words
Tarsitis, juvenile spondyloarthropathy, children, tarsus, juvenile idiopathic arthritis
692
PAEDIATRIC RHEUMATOLOGY Tarsitis as a form of juvenile spondyloarthropathy onset / C. Álvarez-Madrid et al.
Carla Álvarez-Madrid, MD
Rosa Merino, MD, PhD
Jaime De Inocencio, MD, PhD
Julia García-Consuegra, MD, PhD
Please address correspondence and
reprint requests to:
Dr R. Merino
Paediatric Rheumatology Unit,
University Hospital La Paz
Po de la Castellana 261
28046 Madrid, Spain.
E-mail: merino.hulp@salud.madrid.org
Received on August 11, 2008; accepted in
revised form on March 4, 2009.
© Copyright CLINICAL AND
EXPERIMENTAL RHEUMATOLOGY 2009.
Competing interests: none declared.
Introduction
Juvenile spondyloarthropathy (JSpA)
often begins as asymmetric, peripheral
arthritis of the lower limbs and enthesi-
tis without axial involvement, in con-
trast to what is observed in adults (1,
2). Tarsitis can appear during the initial
stages of the disease. Tarsitis is defined
as foot inflammation from the ankle to
the metatarsophalangeal joints. Tarsal
involvement related to JSpA was first
described by Burgos-Vargas et al. (3,
4). The acute phase is characterized
by diffuse inflammation of tarsal soft
tissues which can be shown by various
imaging techniques, but it should be
suspected from clinical data. If the in-
flammation persists, the structures may
become damaged leading to fusion of
the tarsal bones. This evolution has
been named ankylosing tarsitis.
The aims of this study were to determine
the frequency of tarsitis as one of the
first symptoms of JSpA and to analyze
whether JSpA patients with tarsitis at
that time differed from those without it.
Patients and methods
A retrospective chart review was per-
formed on all patients diagnosed with
JSpA at the paediatric rheumatology
unit of a tertiary university hospital in
Madrid. According to the Unit Registry
between January 1996 and September
2007 3,995 new cases were evaluated.
Of those, 283 (7%) corresponded to in-
flammatory chronic arthritis being 37
of them diagnosed with JSpA.
The patients were classified according
to the European Spondyloarthropathy
Study Group (ESSG) criteria (5). Sub-
sequently, the enthesitis related arthritis
criteria of the International League of
Associations for Rheumatology (ILAR)
(6) were applied.
Variables collected from the begin-
ning of the symptoms until diagnosis of
JSpA included demographic data, clini-
cal manifestations (tarsitis, arthritis of
other joints, enthesitis, dactylitis, lum-
bar/sacroiliac pain, fever and adminis-
tration of antibiotics due to suspected
infection), laboratory findings (eryth-
rosedimentation rate and HLA-B27 sta-
tus) and imaging studies (radiographs,
bone scans and magnetic resonance im-
aging [MRI]) of the tarsus and pelvis.
Tarsitis was defined as inflammation of
the mid-foot causing pain and limping
documented by a physician. Imaging
techniques were consistent with the
clinical profile. Other etiologies such
as trauma or infections were excluded.
To assess tarsal involvement at diagno-
sis the Spondyloarthropathy Tarsal Ra-
diographic Index (SpA-TRI) was ap-
plied categorizing the lesions in a scale
that ranged from 0 (normal) to 4 (bony
ankylosis) (7).
At the last visit, before September
2007, the number of patients diagnosed
with ankylosing spondilytis (AS) or an-
kylosing tarsitis were recorded.
Statistical analyses were performed us-
ing the SPSS 11.0 package. Descriptive
characteristics of variables were repre-
sented as median, mean and standard
deviation or percentages. Comparisons
between groups were done using the
Mann-Whitney U-test for quantitative
variables, and Chi-square and Fisher’s
exact test for qualitative variables. Dif-
ferences were considered significant at
(p<0.05).
Results
During the study period 37 patients
were diagnosed with JSpA. All chil-
dren fulfilled ESSG criteria. However,
only 32 (86%) were allocated to the
ILAR enthesitis related arthritis catego-
ry. Five patients were excluded: three
because of positive family history of
psoriasis in a first-degree relative; one
of these had disease onset at 17.3 years
of age. Another one, a boy, was diag-
nosed with reactive arthritis. Finally a
girl presented unilateral sacroiliitis and
ankle arthritis with no other criteria.
Thirteen out of 37 (35%) patients had
tarsitis as one of the first symptoms. In
three of them unilateral tarsitis was the
only sign of musculoskeletal involve-
ment. Bilateral tarsitis was found in 4
of the other 10 children. Only one (8%)
of the 13 cases with tarsitis at diagno-
sis had lumbar/sacroiliac pain, in con-
trast to 13 of 24 (54%) without tarsitis.
Fever and antibiotic treatment before
JSpA diagnosis were more frequently
recorded among those who started with
tarsal inflammation. The main clinical
and laboratory characteristics of the
series are reported in Table I. At that
693
PAEDIATRIC RHEUMATOLOGY
Tarsitis as a form of juvenile spondyloarthropathy onset / C. Álvarez-Madrid et al.
time none presented uveitis, and all had
negative antinuclear antibodies.
According to the radiographic index
tarsal involvement at diagnosis was
between grades 0 (normal) and 1 (os-
teopenia) in all cases. Gammagraphic
bone scans of the feet performed in 6
patients showed increased uptake of the
isotope (Fig. 1) and MRI carried out in
5 showed signal enhancement of soft
tissues (Fig. 2). Radiographs of sacro-
iliac joints obtained in 12 of 14 children
with inflammatory lumbar/sacroiliac
pain were normal except for one case.
That patient fulfilled diagnostic criteria
for AS at the first visit and conventional
radiography and MRI confirmed the di-
agnosis. He consulted us 5.3 years after
his symptoms began, had no tarsitis,
and later developed Chron’s disease.
At the last visit, after a mean disease
duration of 3.8±2.6 (0.09-11.3), me-
dian 4.3 years, with no differences be-
tween patients with and without tarsitis
(p=0.22), two children fulfilled criteria
for ankylosing spondylitis, after 5 and 9
years of disease duration, before tumor
necrosis factor antagonists were start-
ed. Neither of them presented tarsitis
as an initial symptom. One was the boy
affected by Chrön’s disease mentioned
above. The other was a boy diagnosed
with JSpA in 1996 when he had back
pain and a normal sacroiliac joints x-
ray. Later in 2005 he complained again
of back pain and his x-ray showed
grade 2 bilateral sacroiliitis. Etanercept
was started and his disease has been in-
active since. None of the patients in the
series had developed ankylosing tarsi-
tis by the end of the study.
Discussion
The ESSG criteria have demonstrated
high sensitivity (83.9%) and specificity
(87.5%) for the diagnosis of JSpA (8).
It is well known that the exclusion sys-
tem of the ILAR criteria does not allow
the classification of all patients (9).
The tendency of JSpA towards males,
with positive HLA-B27 antigen, asym-
metric peripheral arthritis in lower
limbs, enthesitis, and dactylitis has
been previously described (10-12).
The frequency of the spondylarthropa-
thy from the registers of paediatric rheu-
matology clinics is around 10% (13).
In this series, tarsitis was one of the
initial symptoms of JSpA in one-third
(35%) of the patients. According to
other studies up to 71.4% of children
with JSpA developed tarsitis in the first
six months of the disease (14).
At initial stages of JSpA tarsitis should
be suspected by clinical data, and im-
aging techniques should be consistent
with the clinical profile. Tarsal radiog-
raphy helps to exclude osteolitic and
other lesions, whereas bone scan and
Table I. Main characteristics of 37 patients with juvenile spondyloarthropathy at diagnosis,
classified according to the presence or absence of tarsitis.
Values are shown as median, mean ± SD (min-max) and number (percentage)
With tarsitis Without tarsitis p-value
(n=13) (n=24)
Demographic characteristics
Male 9 (69) 17 (71) 0.60
Age at onset (y) 10, 10 ± 4 (3.6-17.3) 9.4, 9.6 ± 2.1 (3.6-14.3) 0.64
Clinical characteristics
Time to diagnosis (y) 0.3, 0.7 ± 0.7 (0.04-2) 0.4, 0.9 ± 1.2 (0.04-5.3) 0.42
Age at diagnosis (y) 10.3, 10.7 ± 4 (3.8-17.7) 10.5, 10.6 ± 2.4 (4-14.7) 0.86
Lower limbs arthritis* 11 (85) 21 (88) 0.58
Asymmetric arthritis 10 (77) 21 (88) 0.34
Enthesitis 7 (54) 11 (46) 0.45
Dactylitis 3 (23) 5 (21) 0.59
Lumbar/sacroiliac pain 1 (8) 13 (54) 0.006
Fever** 6 (46) 4 (17) 0.06
Antibiotic treatment** 6 (46) 1 (4) 0.004
Analytical data
HLA-B27 (+) 11 (85) 21 (88) 0.58
ESR mm/h 56, 56 ± 28 (13-125) 44.5, 45 ± 29 (4-104) 0.26
ESR: Erythrosedimentation rate.
*Predominantly lower limbs arthritis; **Fever and antibiotic treatment before juvenile spondylo-
arthropathy diagnosis.
Fig. 1. Vascular phase of a bone scan demonstrating increased uptake of technetium 99m in soft tis-
sues. It corresponds to a boy diagnosed with juvenile spondyloarthropathy who presented with left
tarsitis as an unique manifestation of the disease.
694
PAEDIATRIC RHEUMATOLOGY Tarsitis as a form of juvenile spondyloarthropathy onset / C. Álvarez-Madrid et al.
MRI reveal the inflammation sites. The
biggest diagnostic challenge is unilater-
al tarsal inflammation and fever with no
other manifestations related to disease.
The present study has significant limi-
tations, as it is a retrospective analysis
with few patients and short disease
duration. It cannot be concluded that
tarsitis is a form of JSpA without sac-
roiliitis nor spondylitis. However, axial
involvement was unfrequent in cases
with tarsitis at disease onset, only 8%,
in contrast to 54% of the children with-
out it. Moreover none of the patients
with tarsitis at diagnosis has developed
axial involvement. However, long-term
studies have shown that JSpA is asso-
ciated with the development of spond-
ylitis and sacroiliitis years after onset
(15), indicating that this is a possible
outcome for those patients.
Despite the limitations of this study
there were some differences between
children diagnosed with JSpA initially
affected with tarsitis and those without
it. In the first group, 46% of the children
had fever and received antibiotic therapy
because of a suspected soft tissue infec-
tion, whereas only 17% of the patients
without tarsitis at onset had fever, and
only 1 (4%) was treated with antibiotics.
This indicates that the diagnosis of JSpA
in children with tarsitis usually requires
the exclusion of an infectious etiology.
This diagnostic dilemma may also be
faced when confronting a patient with
monoarthritis of the knee, ankle or hip,
although the anatomy of those joints al-
lows the clinician to obtain synovial
fluid to make the correct diagnosis.
In summary, patients with JSpA and tar-
sitis as one of the first symptoms were
often misdiagnosed with infections and
the evidence of axial involvement was
low in them.
References
1. MARKS SH, BARNETT M, CALIN A: A case-
control study of juvenile- and adult-onset an-
kylosing spondylitis. J Rheumatol 1982; 9:
739-41.
2. BURGOS-VARGAS R, PETTY RE: Juvenile an-
kylosing spondylitis. Rheum Dis Clin North
Am 1992; 18: 123-42.
3. BURGOS-VARGAS R: Contribuciones de la reu-
matología mexicana al área de las espondiloar-
tropatías. Rev Mex Reumat 2002; 17: 141-52.
4. BURGOS-VARGAS R, PACHECO-TENA C, VÁZ-
QUEZ-MELLADO J: Juvenile-onset spondylo-
arthropathies. Rheum Dis Clin North Am
1997; 23: 569-98.
5. DOUGADOS M, VAN DER LINDEN S, JUHLIN
R et al.: The European Spondylarthropathy
Study Group preliminary criteria for the
classification of spondylarthropathy. Arthri-
tis Rheum 1991; 34: 1218-27.
6. PETTY RE, SOUTHWOOD TR, MANNERS P et
al.: International League of Associations for
Rheumatology Classification of juvenile idio-
pathic arthritis: second revision, Edmonton,
2001. J Rheumatol 2004; 31: 390-2.
7. PACHECO-TENA C, LONDOÑO JD, CAZARÍN-
BARRIENTOS J et al.: Development of a ra-
diographic index to assess the tarsal involve-
ment in patients with spondyloarthropathies.
Ann Rheum Dis 2002; 61: 330-4.
8. KASAPÇOPUR Ö, DEMIRLI N, ÖZDOĞAN H
et al.: Evaluation of classification criteria
for juvenile-onset spondyloarthropathies.
Rheumatol Int 2005; 25: 414-8.
9. MERINO R, DE INOCENCIO J, GARCÍA-
CONSUEGRA J: Evaluation of revised Inter-
national League of Associations for Rheu-
matology Classification Criteria for juvenile
idiopathic arthritis in Spanish children (Ed-
monton 2001). J Rheumatol 2005; 32: 559-
61.
10. ZOCHLING J, BRANDT J, BRAUN J: The cur-
rent concept of spondyloarthritis with special
emphasis on undifferentiated spondyloarthri-
tis. Rheumatology 2005; 44: 1483-91.
11. AGGARWAL A, HISSARIA P, MISRA R: Juven-
ile ankylosing spondylitis – is it the same dis-
ease as adult ankylosing spondylitis? Rheu-
matol Int 2005; 25: 94-6.
12. GENSLER L, DAVIS JC: Recognition and
treatment of juvenile-onset spondyloarthritis.
Curr Opin Rheumatol 2006; 18: 507-11.
13. PRUTKI M, TAMBIC BUKOVAC L, JELUSIC
M, POTOCKI K, KRALIK M, MALCIC I: Retro-
spective study of juvenile spondylarthropa-
thies in Croatia over the last 11 years. Clin
Exp Rheumatol 2008; 26: 693-9.
14. BURGOS-VARGAS R, VÁZQUEZ-MELLADO J:
The early clinical recognition of juvenile-
onset ankylosing spondylitis and its differ-
entiation from juvenile rheumatoid arthritis.
Arthritis Rheum 1995; 38: 835-44.
15. FLATØ B, HOFFMANN-VOLD AM, REIFF A,
FØRRE Ø, LIEN G, VINJE O: Long-term out-
come and prognostic factors in enthesitis-re-
lated arthritis: a case-control study. Arthritis
Rheum 2006; 54: 3573-82.
Fig. 2. MRI of the foot of the same boy with tarsitis represented in Figure 1. The cross-section and
lateral view show gadolinium signal enhancement of soft tissues.
