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Ten-year followup study of patients with yersinia arthritis.

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533
TEN-YEAR FOLLOWUP STUDY O F PATIENTS WITH
YERSINIA ARTHRITIS
MARJATTA LEIRISALO-REP0 and HANNU SUORANTA
Eighty-five patients with acute Yersinia arthritis
were seen in followup for a mean of 10 years. During
that time, peripheral joint symptoms occurred frequently (51.8%), but these symptoms were mild
(45.9%). Development of a new reactive arthritis (4.7%)
or chronic arthritis (2.4%) was uncommon. One-third
of the patients experienced low back pain, and one-third
of the patients had radiologic evidence of sacroiliitis.
The presence of sacroiliitis was more frequent in patients with low back pain (46.7%) than in those who did
not have symptoms (21.2%). More patients with
HLA-B27 had low back pain and sacroiliitis, but there
was no association of this genetic factor with the residual
symptoms in peripheral joints.
In a susceptible patient, gastrointestinal and
urogenital infections can trigger a sterile inflammatory
arthritis. The triggering factors include enteric infections caused by Salmonella, Shigella, Campylobacter,
and Yersinia enterocolitica, and urogenital infections
caused by Chlamydia trachomatis (1) and, probably,
Neisseria gonorrhoeae ( 2 ) . Patients with Yersinia arthritis have a typical clinical picture that is common to
other forms of reactive arthritis: inflammatory arthritis
with a predilection for large weight-bearing joints,
From the Second Department of Medicine and the Department of Diagnostic Radiology, Helsinki University Central Hospital,
Helsinki, Finland.
Marjatta Leirisalo-Repo, MD: Consultant in Rheumatology,
Second Department of Medicine; Hannu Suoranta, MD Associate
Professor in Radiology, Department of Diagnostic Radiology.
Address reprint requests to Marjatta Leirisalo-Repo, MD,
Second Department of Medicine, Helsinki University Central Hospital, Haartmaninkatu 4, Helsinki, SF-00290, Finland.
Submitted for publication June 23, 1987; accepted in revised form October 1. 1987.
Arthritis and Rheumatism, Vol. 31, No. 4 (April 1988)
frequent extraarticular inflammatory signs, a 3-5month self-limiting course of acute arthritis, and a high
frequency of HLA-B27 (3).
Although the acute phase of Yersinia arthritis is
self-limiting, the patients may have residual symptoms
for a few years (4-6). The disease was first described
in 1969 (7,8), and the long-term prognosis is therefore
not yet completely known. We report here the 10-year
course of 85 patients with Yersinia arthritis who were
followed up prospectively.
PATIENTS AND METHODS
Patients. A 4-year followup study of 144 patients who
had acute Yersinia arthritis during the years 1968-1978 was
described in 1982 (6). The patients living in the metropolitan
area of Helsinki were followed up prospectively at the
outpatient department of the University Central Hospital.
The mean time since the onset of acute Yersinia arthritis was
10.5 years (range 6.3-16.8) in the patients described here.
Five of the 90 patients who fulfilled the followup time criteria
(minimum 6 years) could not be reached because they had
moved away; the study thus includes 85 patients.
Methods. The diagnosis of Yersinia arthritis was
based on the typical clinical picture of reactive arthritis (9)
and an elevated agglutination antibody titer ( ~ 1 : 1 6 0 )for Y
enterocolitica (type 3 or type 9) or a stool culture positive for
the organism. The followup study included a physical examination of the patient, together with relevant laboratory
tests. A radiologic examination of the lumbosacral spine was
performed on 73 patients (mean 9.8 years since onset of
acute disease, range 5.8-16.1).
Radiographs made during the acute phase of disease
in 52 of the patients were available for analysis. Radiologic
analysis of the films was performed by one of us (HS),
according to the criteria described by Macrae et a1 (10). The
radiologist did not know the clinical symptoms or the HLA
status of the patient whose films were being read. Radiologic
findings were graded on a scale of 0-4, according to the New
LEIRISALO-REP0 AND SUORANTA
534
Table 1. Extraarticular features during acute Yersinia arthritis in
85 patients
Table 2. Peripheral joint symptoms in 85 patients with previous
Yersiniu arthritis
No. of patients
Feature
Urethritis/pathologic urinalysis
Eye inflammation
Iritis
Conjunctivitis
Episcleritis
Carditis
Erythema nodosum
Maculopapular or pustular skin eruption
Keratoderma blennorrhagicum
Low back pain
(n
23*
3
2
1
6
7
7
2
29
* lncludes 2 patients with hematuria and 1 with proteinuria.
York criteria (11). In the analysis, radiologic evidence of
sacroiliitis was present if there was at least minimal sclerosis, with or without erosions.
Statistical analysis. Chi-square with Yates’ correction
was used to compare differences in the frequency of symptoms and of HLA-B27. Differences in disease duration were
analyzed using the Kolmogorov-Smirnov test (12). Other
comparisons were made using Student’s t-test for unpaired
groups.
RESULTS
The study included 85 patients (39 men and 46
women) who had had acute Yersinia arthritis 6.3-16.8
years previously (mean 10.5). HLA-B27 was present
in 80% of the patients. The sex distribution was equal
in the B27 positive and B27 negative patients. Pertinent medical histories before the acute Yersinia arthritis included rheumatic fever in 4 patients, acute arthritis in 3, established ankylosing spondylitis in 2,
seronegative erosive polyarthritis in 1, and reactive
arthritis caused by Salmonella infantis in 1 . In addition, 1 patient had symptoms of rheumatoid arthritis
for 1 month prior to the Yersinia gastroenteritis that
triggered the reactive arthritis. During the acute Yersinia arthritis, the patients had inflammatory oligoarthritis or polyarthritis that mainly affected the lower
extremities. The duration of the acute phase varied
from < I month to 1 year (mean 3.2 months). In
addition to joint symptoms, extraarticular inflammatory symptoms frequently occurred (Table 1). Six
patients had carditis, with the following manifestations: mitral regurgitation in 3 patients, transient left
atrial enlargement in 1 patient, transient enlargement
of the heart in 1 patient, and pericarditis in 1 patient.
Peripheral joint symptoms. During the followup
period, joint Symptoms occurred frequently, with
51.8% of the patients having some joint symptoms,
Number of symptomatic patients
Transient or mild symptoms
Transient joint pains
Achilles tendinitis
Plantar fasciitis
Transient joint stiffness
Transient joint effusion
Crepitation on movement
Acute symptoms
Acute coxitis
Acute reactive arthritis
Chronic arthritis
Recurrent attacks of Reiter’s
syndrome with progression to
chronic arthritis
Juvenile chronic polyarthritis
Seronegative polyarthritis
Seropositive rheumatoid arthritis
Women
Total
Men
= 39) (n = 46) (n = 85)
17
27
44
8
I
2
2
3
0
9
0
0
2
8
4
17
1
2
4
11
4
0
I
I
3
1
4
1
I
0
0
0
0
2
1
1
2
1
1
which in most cases (39 [88.6%] of the patients with
joint symptoms; 45.9% of all patients) were mild or
transient (Table 2). Transient joint effusion of unknown cause occurred in 12.9% of the patients, but
only 4 patients (4.7%) had a new reactive arthritis
during the followup period. The triggering infections in
these were Salmonella (1 patient), Chlamydia (1
patient), and Yersinia (1 patient). The fourth patient
had acute Reiter’s syndrome of unknown etiology.
Five patients (5.9%) had peripheral chronic
arthritis (Table 2). In 3 of them, the arthritis was
present before onset of the Yersinia arthritis. During
the followup, 1 patient had recurrent attacks of Reiter’s syndrome, which 11 years later, progressed into
chronic Reiter’s syndrome. Only 1 patient had prolonged (5 years) seronegative chronic polyarthritis as a
sequela of Yersinia arthritis. She had a history of
rheumatic fever, with continuous joint symptoms and
erosive arthritis for 2 years. The occurrence of peripheral joint symptoms did not differ between male and
Table 3. Percentage of patients with residual joint symptoms,
according to the presence or absence of HLA-B27
~~
Peripheral transient joint symptoms
Chronic arthritis
Low back Rain
Radiologic’sacroiliitist
~~~~
827 +
(n = 68)
827 (n = 17)
45.6
7.3
41.2
40.7
47.1
0.0
* Chi-square test with Yates’ correction. NS
t In 59 B27+ and
P*
11.8
NS
NS
<0.05
7.1
<0.05
= not significant.
14 B27- patients who were radiographed.
535
YERSZNZA ARTHRITIS
female patients (Table 2), or between those with and
those without HLA-B27 (Table 3).
Spinal symptoms. Low back pain during the
night and early morning, associated with morning
stiffness and improving with exercise, was reported by
35.3% of the patients during the followup period. The
symptoms were more common in HLA-B27 positive
patients (Table 3 ) , but there was no statistically significant difference in the proportion of males (38.5%) and
femaies (32.6%) who had these symptoms.
Radiologic findings. During the acute phase,
21.2% of the patients, including 2 patients with established ankylosing spondylitis, had radiologic evidence
of sacroiliitis. There was only 1 HLA-B27 negative
patient who had sacroiliitis. In films made during the
acute Yersinia arthritis episodes, the presence of sacroiliac changes did not differ significantly between
male and female patients (24.1% versus 17.4%) or
between HLA-B27 positive and negative patients
(21.7% versus 16.7%).
Radiographic examinations during the mean
followup period of 9.8 years (range 5.8-16.1) after
acute Yersinia arthritis detected evidence of sacroiliitis (at least minimal sclerosis) in 35.6% of the
patients (Figure 1). Twenty-four B27 positive patients
had radiographic changes, in contrast with only 1
HLA-B27 negative patient (40.7% versus 7.1%; P <
0.05). Again, there was no statistically significant
difference between male and female patients in this
respect (42.9% versus 26.3%). Five of the patients (1
was HLA-B27 negative) had marginal or lateral syndesmophytes. The radiologic sacroiliitis correlated
positively with the presence of low back pain: 46.7%
of the patients with symptoms at the followup study
had sacroiliitis, compared with 21.2% of the asymptomatic patients (P < 0.05). The radiologic changes
developed or progressed in 17.6% of the patients, but
in many cases, the changes observed during the acute
phase remained the same (Figure 1).
Other inflammatory signs. Two of the 6 patients
with previous carditis had persistent, asymptomatic
mitral regurgitation. Twelve patients (14.1%) had
GRADE OF
SACROlLllTlS
L
A
B
4 1
2
4
6
8
10
12
14
16
0
2
4
6
8
10
12
14
16
FOLLOW- UP TI ME (years)
Figure 1. Radiologic grading of changes in the sacroiliacjoints in patients with Yersinia arthritis, with respect to followup interval.
A, Males. B, Females. One dot represents I radiographic examination of 1 patient. Dots connected with lines represent the
radiographic findings of 1 patient during the followup. Radiographs were graded on a scale of 0-4, according to the New York
criteria ( I I).
536
LEIRISALO-REP0 AND SUORANTA
acute iritis, and 2 patients (2.4%) had conjunctivitis
during the followup interval. All of the 12 patients with
acute iritis were HLA-B27 positive. Urologic inflammatory symptoms (urethritis, dysuria, prostatitis, balanitis, recurrent pyelonephritis, and gonorrhea) had
occurred in 10.6% of the patients, as frequently in B27
positive patients as in B27 negative patients.
Factors determining the long-term prognosis.
The presence of low back pain during acute arthritis
correlated with the presence of low back pain during
the followup period: 86.2% of patients with low back
pain and 33.9% of those without low back pain during
the acute disease had low back pain during the followup period (P< 0.001). At the followup study, 19.2% of
those with low back pain experienced during the acute
phase of Yersinia arthritis had developed radiologic
evidence of sacroiliitis, compared with 40.4% of those
without back pain during the acute disease. The
chance that patients with one or more extraarticular
features of Reiter’s syndrome would have radiologic
evidence of sacroiliitis at the time of the followup
study (36.0%) was similar to that for patients with only
joint symptoms during the acute disease (31.3%).
Neither the maximal erythrocyte sedimentation rate,
maximal white blood cell count, maximal Yersinia
antibody titer, nor the duration of the acute arthritis
correlated with the presence of radiologic sacroiliitis at
the followup study. Thus, the presence of HLA-B27
was the only factor among the parameters studied that
could determine the long-term prognosis.
DISCUSSION
Although mild residual symptoms occur in 50%
of the patients with peripheral Yersiniu arthritis, the
prognosis seems to be good. In the present series, only
1 of the 85 patients developed chronic polyarthritis,
which persisted for 5 years; however, this patient had
had erosive arthritis. Another patient had, within 1
month, first the onset of rheumatoid arthritis and then
Yersinia arthritis. The benign course of reactive arthritis has been emphasized by some (13,14), but not all
(5,15-17), authors. The good initial prognosis of reactive arthritis may be changed if there are recurrent
attacks of arthritis. Recurrent attacks of Reiter’s syndrome are common in patients with uroarthritis
(18,19), but occurred infrequently in the present patient series. We have also observed a less favorable
prognosis of peripheral arthritis in patients with Reiter’s disease, compared with patients with Yersiniu
arthritis (20).
A 20-year followup study of another type of
enteroarthritis, that triggered by Shigella infection,
indicated that chronic arthritis developed in 18% of the
patients (17). Some of the discrepancies between the
various results can be explained by different criteria
for selection of patients, by genetic factors, and perhaps, by variations in the triggering infection (urogenital or gastrointestinal). Reactive arthritis is defined
as sterile joint inflammation for which no triggering
factor, either as a living cell or in the form of antigen,
can be detected in the joint (21). However, there is
increasing evidence that Chlamydia trachomatis can
be either isolated (22) or detected by antigen in the
synovial fluid or in the synovium (23). Consequently, a
living or persisting Chlamydia could explain the rapidly progressive symptoms that are occasionally observed in Reiter’s syndrome (13). A reactivation of
persistent chlamydia1 infection in the absence of a new
infective urethritis could also explain at least some of
the recurrences of arthritis that are typical of this
disease (18).
There is no evidence for the persistence or
latency of enteric infections that trigger reactive arthritis, although antigenic material of Yersinia has
been detected in immune complexes in sera (24) or in
synovial fluid (25) from patients with Yersinia arthritis.
The presence of such material correlated with the
prolonged course of the joint symptoms in these
patients, but no relapses were described.
HLA-B27 positive subjects have an increased
risk of developing sacroiliitis. It has been suggested
that as many as 20% of the HLA-B27 positive population (26) or of the relatives of HLA-B27 positive
patients (27) have ankylosing spondylitis. This is consistent with our finding that about 20% of the
HLA-B27 positive patients already had radiologic
evidence of sacroiliitis during the acute Yersinia arthritis. Sacroiliitis has also been observed during the
onset of Reiter’s syndrome; after a mean of 10 years,
a third of the patients had radiologic changes of
sacroiliitis (28). This i s in accordance with the longterm prognosis of Shigella enteroarthritis (17), but
higher (19) and lower (1 8) figures have been reported
for venereal Reiter’s syndrome, in which the progression of sacroiliac changes is very slow (28,29).
Most patients who have Yersinia arthritis continue to have normal sacroiliac joints, and many of
those with sacroiliitis that is present during the acute
disease show no progression of the sacroiliac inflammation. The causal relationship between previous Yersinia arthritis and subsequent sacroiliitis is therefore
YERSINIA ARTHRITIS
still uncertain. The presence of HLA-B27 seems to b e
a major factor contributing to the severity of acute
Yersinia arthritis (6). It also correlates with t h e occurrence of low back pain and radiologic changes of
sacroiliitis after a c u t e arthritis and may be an independent factor determining the long-term prognosis of t h e
patients.
537
16.
17.
18.
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