Rheumatology Advance Access originally published online on July 16, 2003
Rheumatology 2003; 42: 1398-1403
© 2003 British Society for Rheumatology
Diagnostic points and possible origin of osteomyelitis in synovitis, acne, pustulosis, hyperostosis and osteitis (SAPHO) syndrome: a radiographic study of 77 mandibular osteomyelitis cases
Y. Suei,
A. Taguchi and
K. Tanimoto1
Department of Oral and Maxillofacial Radiology, Hiroshima University Dental Hospital and 1Department of Oral and Maxillofacial Radiology, Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima, Japan.
Correspondence to:
Y. Suei, Department of Oral and Maxillofacial Radiology, Hiroshima University Dental Hospital, 1-2-3, Kasumi, Minami-ku, Hiroshima 734-8553, Japan. E-mail: suei{at}hiroshima-u.ac.jp
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Abstract
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Objectives. To find diagnostic points and to identify the origin
of osteomyelitis in synovitis, acne, pustulosis, hyperostosis
and osteitis (SAPHO) syndrome.
Methods. Fifty-two patients with mandibular suppurative osteomyelitis and 25 patients with mandibular osteomyelitis in SAPHO syndrome were included in the study. Radiographic patterns of the lesion, types of periosteal reaction and the presence of external bone resorption and bone enlargement were investigated in each case and compared between the two entities.
Results. Suppurative osteomyelitis demonstrated an osteolytic pattern and a lamellated type of periosteal reaction, whereas SAPHO syndrome revealed a mixed-pattern, solid-type periosteal reaction, external bone resorption and bone enlargement.
Conclusions. Radiographic examination is suggested to be convenient and a useful diagnostic method of differentiating osteomyelitis in SAPHO syndrome from suppurative osteomyelitis. The periosteum is suspected to be the original site of osteomyelitic lesions in SAPHO syndrome.
KEY WORDS: Radiology, Bone diseases, Hyperostosis, Bone resorption.
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Introduction
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Except for special and unusual types, osteomyelitis can be conveniently
divided into two groups: osteomyelitis caused by bacterial infection
and osteomyelitis of unknown aetiology [
1]. Because many appellations
have been proposed, we select the terms ‘suppurative osteomyelitis’
and ‘synovitis, acne, pustulosis, hyperostosis and osteitis
syndrome’ (SAPHO syndrome) to represent the entities in
each group. SAPHO syndrome is a clinical entity combining osteomyelitis,
arthritis and skin disease (palmoplantar pustulosis, pustular
psoriasis or severe acne) [
2]. As shown in
Table 1, combinations
of these manifestations lead to a diagnosis. However, a single
bone may be symptomatic and skin disease does not always occur
simultaneously with bone/joint lesions [
3–
5]. In cases
with only one symptomatic bone, diagnosis is difficult and the
lesion is often confused with suppurative osteomyelitis because
of the similarity of the clinicopathological findings [
2]. Patients
often receive long-term administration of antibiotics combined
with surgery, such as saucerisation, decortication and partial
resection of the affected bones, which are usually less effective
and cannot cure the disease [
6–
8]. Conservative and expectant
treatments are recommended for osteomyelitis in SAPHO syndrome
[
9–
15]. Because pain may be severe and continue for several
years, early diagnosis is of great importance in preventing
unnecessary procedures and selecting an effective treatment.
Radiographic examination is a convenient and non-invasive method
of evaluating the osteomyelitic lesion. We performed a radiographic
study to find possible diagnostic points for osteomyelitis in
SAPHO syndrome.
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Methods
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The patients consisted of 52 with mandibular suppurative osteomyelitis
and 25 with mandibular osteomyelitis of SAPHO syndrome. In suppurative
osteomyelitis cases, the male:female ratio was 33:19 and the
mean age was 52.3 yr (range 11–79 yr), and in SAPHO syndrome
cases the corresponding values were 9:16 and 40.5 yr (13–72
yr). In all cases, the presence of osteomyelitis was confirmed
by the clinical findings of pain and/or swelling and radiographic
evidence of osteomyelitis (osteolytic and/or osteosclerotic
change with variable amounts of periosteal reaction). Histological
examination was performed in 39 suppurative osteomyelitis cases
and in 16 SAPHO syndrome cases, and a non-specific inflammatory
condition was confirmed. In cases without biopsy, the possibility
of other lesions, such as malignancies, was rejected by complete
resolution of the symptoms in suppurative osteomyelitis cases
and by follow-up for more than 3 yr in SAPHO syndrome cases.
Suppuration or a quick response to antibiotic treatment was
a diagnostic point for suppurative osteomyelitis. In 11 of 25
SAPHO syndrome patients, diagnosis was obtained on the basis
of diagnostic criteria (
Table 1). In the remaining 14 patients,
whose symptomatic site was the mandible alone, the lesion revealed
recurrent bouts of symptoms without suppuration, continuing
for more than 6 months despite long-term antibiotic therapy,
and the diagnosis was diffuse sclerosing osteomyelitis of the
mandible (DSOM) [
16]. DSOM was recognized recently as a mandibular
manifestation of SAPHO syndrome [
2,
17,
18].
The type of radiographic examination in each patient was determined by the physician in charge according to the site of the lesion, the patient's condition and the facilities which could be used at the time of examination. Panoramic and intra-oral radiographs were taken in all cases. A postero-anterior projection was taken when the lesion involved the ramus of the mandible. CT examination was performed in 28 suppurative osteomyelitis cases and in 13 SAPHO syndrome cases. Using all radiographs obtained at the initial examination and during the follow-up period, various findings, such as osteolysis, osteosclerosis and periosteal reaction, and their extents and relationships, were carefully observed. Finally, the radiographic type of the lesion was evaluated by classifying it as showing an osteolytic pattern or a mixed pattern [19]. The osteolytic pattern was characterized by bone resorption with no or a small amount of osteosclerosis. The mixed pattern was a diffuse bone abnormality in which osteosclerosis and osteolysis were intermingled, which was often accompanied by extensive cortical bone resorption. Periosteal reaction was assessed and classified into three types: lamellated, solid and mixed [16, 20]. The lamellated type was a lamellar radio-opacity separated by a radiolucent zone from the underlying cortex or periosteal new bone. The solid type was an even, uniform, radio-opaque appearance on the cortex. When both types were observed, it was evaluated as the mixed type. The presence of other findings previously reported in osteomyelitis cases, such as external bone resorption and bone enlargement, was also investigated.
In this study, ethical approval and informed patient consent were not obtained because all of our data had been obtained during the treatments for the patients and there was no identifiable data.
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Results
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Radiographic findings in suppurative
osteomyelitis cases
Bone resorption was the main feature and radiographs showed
an osteolytic pattern (
Fig. 1). Sclerotic change was slight
and did not progress during the course. On CT images, osteolytic
lesions in the bone were continuous, not scattered, and perforated
the cortical bone. The margin of resorbed cortical bone was
relatively well defined, and the density of the remaining cortical
bone was almost normal (
Fig. 2). Slight sclerotic change was
observed at the cancellous part around the osteolytic lesion.
Periosteal reaction was confirmed in 25 cases on conventional
radiographs and in seven cases on CT images. In most cases it
was the lamellated type and was related to the cortical bone
perforation (
Fig. 3, Table 2).
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FIG. 1. Cropped panoramic radiograph of suppurative osteomyelitis at the right mandible. Osteolytic change is observed from around the molar tooth roots to the body of the mandible (arrows).
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FIG. 2. Axial CT image (bone window) through the mandibular body affected by suppurative osteomyelitis. Osteolytic lesion perforates the cortical plate (white arrow). Slight sclerotic change (black arrows) is observed around the osteolytic lesion. The density of the remaining cortical bone is almost normal.
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FIG. 3. Lamellated-type periosteal reaction (short arrows) and cortical bone perforation (long arrow) observed in a case of suppurative osteomyelitis.
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TABLE 2. Number of patients with each radiographic type of periosteal reaction observed on conventional radiographs and CT images
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Radiographic findings in SAPHO
syndrome cases
Abnormal findings were more diffuse and extensive compared with
those of suppurative osteomyelitis. Resorption of cortical and
trabecular bone, sclerosis of cancellous bone and periosteal
reaction spread to a wide area (
Fig. 4). In two cases, the mandibular
bone was totally involved by the lesion during the late stage.
Osteolytic change was prominent during the early stage as well
as at the time or site of flare-up of the symptoms. Sclerotic
change advanced gradually during the course of the disease and
the osteolytic lesion became diminished and restricted to relatively
small areas. A radiographic mixed pattern was typically observed
during the late stage (
Fig. 5). On CT images, the density was
often identical among the parts of the resorbed cortical bone,
sclerotic cancellous bone and periosteal reaction. Low-density
areas (osteolytic lesions) were scattered within them (
Figs 6 and
7). A periosteal reaction was observed in 21 cases on
conventional radiographs and in nine on CT scans. It was more
prominent during the early stage and was of the solid type in
most cases. (
Table 2,
Figs 6 and
7). External bone resorption
was confirmed in four cases at the time of the initial examination
and in 13 during follow-up. When this finding was confirmed,
the symptoms had already been present for more than 1 yr in
all cases but one. It was usually seen on panoramic radiographs
at a location between the inferior border of the mandibular
body and the posterior border of the mandibular ramus (
Fig. 8).
Bone enlargement was confirmed in three cases on CT images.
The original cortex was almost or entirely disrupted, and a
cortex-like radio-opaque zone was probably formed by a periosteal
reaction observed outside the original cortex. The mandibular
bone was enlarged (
Fig. 9). In two cases, the possibility of
establishing bone enlargement was suggested because the density
of periosteal bone was higher than that of resorbed cortical
bone (
Fig. 10).
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FIG. 4. Panoramic radiograph of mandibular osteomyelitis of SAPHO syndrome. Diffuse bone abnormality is observed from the right premolar to the ramus region. Cortical bone is resorbed widely (arrows). The lesion involved the whole body of the mandible at the late stage.
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FIG. 5. Panoramic radiograph of SAPHO syndrome. A long-standing lesion that continued for more than 5 yr reveals the mixed pattern. Spotted osteolyses (arrows) are observed in the sclerotic lesion.
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FIG. 6. CT image of SAPHO syndrome. Diffuse cortical bone resorption and spotted osteolyses (arrows) are observed.
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FIG. 7. CT image of SAPHO syndrome. Solid-type periosteal reaction and extensive cortical bone resorption are seen. Differentiation of cancellous, cortical and periosteal new bone is not clear.
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FIG. 8. Panoramic radiograph of SAPHO syndrome reveals external bone resorption of the left mandible (arrows).
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FIG. 9. CT image of SAPHO syndrome through the level of the mandibular canals (long arrows) shows the enlarged left mandible (short arrows).
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FIG. 10. CT image of SAPHO syndrome. Cortex-like radio-opaque band (short arrows) is more distinct than the resorbed original cortex (long arrows).
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Discussion
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Early diagnosis of SAPHO syndrome is very important in preventing
repeated examination and invasive procedures. In the study by
Hayem
et al. [
10] of 120 SAPHO patients, the mean interval between
the onset of the lesion and the diagnosis was about 9 yr. The
present investigation disclosed characteristic radiographic
findings of the mandibular lesion: these were the mixed pattern,
solid-type periosteal reaction, external bone resorption, and
bone enlargement. In previous studies, these findings were reported
in mandibular osteomyelitis in SAPHO syndrome [
16,
18,
21–
23]
but not in suppurative osteomyelitis. While we studied only
the mandible, these findings apply to the osteomyelitic lesion
of SAPHO syndrome in other bones. Progression of initial osteolyses
to diffuse sclerosis, mixed pattern, bone enlargement with extensive
cortical bone resorption, and solid-type periosteal reaction
have been reported frequently in osteomyelitis in SAPHO syndrome
[
3,
4,
24–
27]. On the other hand, lamellated periosteal
reaction and cortical bone perforation is the characteristic
finding in suppurative osteomyelitis [
20,
28–
30].
We suggest that the original site of osteomyelitis in SAPHO syndrome is not the bone but the periosteum. The following are our hypotheses. Some factors (probably cytokines, such as transforming growth factor, interleukin and tumour necrosis factor) are produced in the inflamed periosteum and irritate the osteoblastic and osteoclastic cells, promoting periosteal bone formation in addition to cortical bone resorption. A large amount of cytokines, such as bone morphogenetic protein, transforming growth factor and insulin-like growth factor, which are stored in the cortical bone matrix [31], is released from the resorbed cortical bone and induces endosteal bone formation. Scattered osteolysis in the sclerotic lesion is probably seen when bone remodelling is not uniform. Periosteal bone formation was prominent at the early stage and external bone resorption was confirmed later. This is explained by the different numbers of osteoblastic and osteoclastic cells. During the early stage, abundant and active osteoblastic cells in the periosteum produce new bone; these cells are derived from stroma cells in the periosteum and are exhausted or severely injured by long-standing inflammation. On the other hand, blood-borne osteoclastic cells continue to be derived from granulocyte–macrophage-committed progenitor cells as long as the inflammation continues. As a result, periosteal bone formation may tend to decelerate and external bone resorption may become prominent during the late stage. Diffuse extensive cortical bone resorption and a high recurrence rate after decortication treatment or partial resection of the affected bone [8, 32, 33] are also compatible with this consideration; the periosteum is the original site of the lesion. If the bone itself or an infection of the bone were the cause of the disease, surgical treatments would be more effective. The direct cause of the periosteal inflammation in SAPHO syndrome cannot be identified at present. It is suggested that the main cause is not a bacterial infection but an allergic reaction or an autoimmune disorder, because corticosteroids are more effective than antibiotics in reducing the symptoms [2]. The present study was based on a radiographic investigation alone. Further studies on the periosteum using histological and immunological techniques are necessary to clarify the aetiology and to explore more effective treatment methods for SAPHO syndrome.
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Conflict of interest
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The authors have declared no conflicts of interest.
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Submitted 24 December 2002;
Accepted 3 April 2003
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Abstract
Introduction