Pediatric Radiology
Juvenile Ankylosing Spondylitis 1 Paul Kleinman, M.D.,2 Marcos RlveUs, M.D., Robert Schneider, M.D., and Jeremy J. Kaye, M.D. 3 The clinical histories and radiographs of 28 patients with ankylosing spondylitis were reviewed. Symptoms developed before the age of 17 in all cases. Juvenile ankylosing spondylitis affected youths in their early teens, who presented most commonly with appendicular joint complaints rather than low back pain. The disease was progressive, with the characteristic changes of ankylosing spondylitis eventually occurring in the spine and sacroiliac joints, frequently accompanied by widespread and severe changes in the appendicular joints. HLA B 27 antigen was present in 8 of the 9 patients tested. Thorough clinical, radiographic, and laboratory examination should prevent confusion with juvenile rheumatoid arthritis. INDEX TERMS: Arthritis, rheumatoid • Spine, ankylosis, arthritis (Skeletal system, ankylosing spondylitis, 4[8].740; Spine, ankylosing spondylitis, 3[0].740)
Radiology 125:775-780, December 1977
A
NKYLOSING spondylitis
(AS) is a well-recognized form of arthritis which produces characteristic findings in the sacroiliac joints, spine, and, less frequently, the appendicular joints in young and middle-aged adults. In the past, children and adolescents with early clinical and radiological features of AS have mistakenly been thought to have juvenile rheumatoid arthritis (JRA) (1-3), and it is only recently that the juvenile form of ankylosing spondylitis (JAS) has been fully appreciated (4-11). We wish to report the radiological findings in 28 cases of JAS followed at the Hospital for Special Surgery. The features which allow differentiation of this entity from JRA are discussed and the appendicular joint changes, which are a more prominent feature of the juvenile form, are stressed.
TABLE I:
K
CLINICALLY INVOLVED EXTRASPINAL JOINTS IN
Joint
28 PATIENTS WITH JAS
No. of Cases 22
Hip Shoulder Elbow Wrist Knee Ankle Foot Temporomarfdibular
11 4 4 14 8 8 4
findings of bilateral erosions, sclerosis, or fusion of the sacroiliac joints (12). Patients with psoriasis, Reiter's disease, and infectious arthritis were excluded. All patients had radiographs of the sacroiliac joints and lumbar spine, and also the remainder of the spine when symptoms were present there. Radiographs of symptomatic appendicular joints were obtained in most cases. In addition to routine laboratory studies, latex fixation tests were performed in all cases. HLA typing was carried out in 9 cases and HLA B 27 antigen was found to be present in 8. The most frequent erroneous diagnosis was JRA; several other patients were initially diagnosed as having rheumatic fever, Osgood-Schlatter disease, synovitis, or "growing pains."
MATERIAL AND METHODS
Twenty-eight patients (24 boys and 4 girls) with JAS were studied. Clinical records and available radiographs were reviewed systematically. Except for one 5-year-old boy, all patients were between 10·and 16 years of age (mean, 12 yr.) when symptoms were first noted. The average age at the time of correct diagnosis was 19 years. Twenty-three patients presented with complaints involving the appendicular joints. Fourteen had hip pain alone, 4 had hip pain plus back pain, and 4 had knee or ankle pain alone. Five patients had only back pain at first. Twenty-five patients (89 %) exhibited appendicular joint manifestations during the course of their disease. The distribution of involved joints is shown in TABLE I. Nine patients showed evidence of polyarticular disease, 10 showed oligoarticular symptoms, and 6 had monoarticular manifestations. The diagnosis was based on (a) a clinical history of low back pain and stiffness, unrelieved by rest and lasting for more than three months, and (b) radiological
Radiological Findings Spine: The sacroiliac joints were abnormal In all cases. Changes were always bilateral, sometimes asymmetric when first seen, but uniformly symmetrical In advanced cases. The earliest signs were indistinct joint margins and subchondral sclerosis. The joint space often appeared widened due to erosions at first; but with progression, narrowing developed and led to ankylosis (Figs. 1-3). Fusion occurred in 12 patients and was usually related to the duration of the illness.
1 From the Departments of Radiology (P.K., R.S., J.J.K.) and Medicine (M.R.) of The Hospital for Special Surgery, affiliated with New York Hospital-Comell University Medical College, New York, N. Y. Presented at the Sixty-second Scientific Assembly and Annual Meeting of the Radiological Society of North America, Chicago, 111., Nov. 14-19, 1976. 2 Present address: Bethesda Naval Hospital, Bethesda, Md. 3 Present address: Vanderbilt University Medical College, Nashville, Tenn. sjh
775
776
PAUL KLEINMAN AND OTHERS
Fig. 1. Anteroposterior radiograph of the pelvis of a 16-year-old boy shows sclerosis and erosions around the sacroiliac joints. There is circumferential narrowing of the left hip jo int space , with mild proliferative changes at the junction of the femoral head and neck . This patient first had hip pain at 12 years of age.
Fig. 3.
December 1977
Fig. 2. Anteroposterior radiograph of the pelvis of a 30-year-old man who presented with clinical symptoms of hip pain at 13 years of age. There is severe narrowing of the hip joints bilaterally, with prominent proliferative changes at the junction of the femoral head and neck and fusion of the sacroiliac joint.
35-year-old woman with fusion of the sacroiliac joints and hip joints bilaterally.
The most recent roentgenographic examinations showed spine abnormalities in 20 cases. The earliest changes were related to reactive sclerosis of the vertebral end plates, with " shining corners" progressing to squaring of the vertebral bodies (Fig. 4). Syndesmophytes and apophyseal joint fusion were seen in 13 cases (Figs. 5 and 6) and atlanto-occipital fusion in 1. Spine manifestations characteristically progressed cephalad from the lumbar region, and changes were never observed in the cervical or dorsal spine without lumbar involvement. Appendicular Joints: There was a striking incidence of appendicular joint involvement. The hips were most commonly involved, followed by the knees, shoulders, and distal joints. Demineralization, soft-tissue swelling, and synovitis were commonly present along with joint pain, but several years often elapsed before prominent bony changes became evident radiographically .
Fig. 4. Same patient as in Figure 3. Lateral radiograph of the lumbar spine shows " squaring" of the vertebral bodies with loss of concavity anteriorly. The apophyseal joints are fused. The patient presented with hip pain at 16 years of age and low back pain developed at the age of 17.
Pediatric Vol. 125
JUVENILE ANKYLOSING SPONDYLITIS
777
Radiology
Fig. 5. Anteroposterior radiograph of the lumbar spine in this 31-year-old man shows osteoporosis, fusion of the apophyseal joints, and asymmetric syndesmophyte formation . The latter was seen in several patients, none of whom had evidence of Reiter's disease or psoriatic arthritis.
The hips were radiographically abnormal in 17 cases (Figs. 1-3). The earliest change was periarticular demineralization, followed by joint-space narrowing. In more advanced cases, subchondral sclerosis and erosions of the articular surface of the femoral heads occurred. Varying degrees of proliferative changes were noted about the joint margins. A typical finding was a ring of proliferative change at the junction of the femoral head and neck (Figs. 1 and 2). The findings were "generally bilateral but usually asymmetric. Bilateral hip fusion was noted in 3 cases (Fig. 3). Periosteal new bone formation and cortical irregularity were common about the trochanters, ischia, and lateral iliac margins. The knees were frequently involved. Early changes consisted of demineralization, joint-space narrowing, and marginal erosions (Fig. 7). With progression, irregularity of the articular surfaces, subchondral sclerosis, and mild proliferative changes were noted. As in the hips, the findings were generally bilateral but asymmetric. In advanced cases, joint contractures developed, and in one case osseous fusion occurred (Fig. 8). The changes involving the shoulders were bilateral but
Fig. 6. Fusion of the apophyseal joints and anter ior subligamentous ossification can be seen in the cervical spine of this 30-year-old man. cervical spine involvement was less frequent and occurred later than involvement of the lumbar spine In this series of patients.
generally asymmetric. Mild to moderate joint-space narrowing and demineralization were usually present. Marginal erosions were noted, most commonly in the region of the greater tuberosities, varying from several millimeters to 2 cm. In advanced cases, erosions and sclerosis of the articular surfaces were present (Fig. 9). Two patients had high-riding humeral heads and faceting of the undersurface of the acromion processes, indicating chronic rotator-cuff degeneration. One patient had bilateral elbow effusions but no bony changes. Changes in the ankles and feet were usually symmetrical and consisted of moderate demineralization and diffuse joint-space narrowing. Bilateral subtalar joint fusions
778
PAUL KLEINMAN AND OTHERS
December 1977
Fig. 8. In this 26-year-old man, there Is solid bony fusion of the knee joint 10 years after the onset of symptoms.
Fig: 7. There are marginal erosions of the medial femoral condyle and tibial plateau and proliferative changes at the proximal tibiofibular Joint. Clinical symptoms developed In the knees at 12 years of age In this 19-year-old youth.
Fig. 10. Lateral radiograph of the foot of a 16-year-old boy shows fusion of the posterior subtalar joint. A large bony spur is present on the plantar aspect of the calcaneus .
Fig. 9. The lateral aspect of the humeral head is eroded (arrows). This 16-year-old boy had involvement of several other appendicular joints and had presented initially with knee and ankle pain at 11 years of age.
occurred in 2 patients (Fig. 10). Erosions were infrequent; when present, they involved the metatarsal heads. Calcaneal spurs were commonly observed. The hands and 'w rists were strikingly abnormal in 3 pa-
tients (Fig. 11). In 2, symmetrical destruction of the distal ulna and extensive erosion of the radius at the distal radioulnar jo int were noted . Additional findings included joint-space narrowing and erosions of the metacarpal heads and phalanges. Metatarsophalangeal joint subluxation and ulnar deviation occurred in one case. DISCUSSION
Since Scott's description of childhood-onset ankylosing spondylitis in 1942 (13), a pattern of clinical and radiographic manifestations has emerged (4-10). The clinical, laboratory, and radiological features of JAS , AS, JRA, and RA are listed in TABLES II and III.
JUVENILE ANKYLOSING SPONDYLITIS
Vol. 125
TABLE
II:
JAS
RA
JRA
AS
Usually Young adult Usually >10yr. Female Female Male
Juvenile Ankylosing Spondylitis 1 Paul Kleinman, M.D.,2 Marcos RlveUs, M.D., Robert Schneider, M.D., and Jeremy J. Kaye, M.D. 3 The clinical histories and radiographs of 28 patients with ankylosing spondylitis were reviewed. Symptoms developed before the age of 17 in all cases. Juvenile ankylosing spondylitis affected youths in their early teens, who presented most commonly with appendicular joint complaints rather than low back pain. The disease was progressive, with the characteristic changes of ankylosing spondylitis eventually occurring in the spine and sacroiliac joints, frequently accompanied by widespread and severe changes in the appendicular joints. HLA B 27 antigen was present in 8 of the 9 patients tested. Thorough clinical, radiographic, and laboratory examination should prevent confusion with juvenile rheumatoid arthritis. INDEX TERMS: Arthritis, rheumatoid • Spine, ankylosis, arthritis (Skeletal system, ankylosing spondylitis, 4[8].740; Spine, ankylosing spondylitis, 3[0].740)
Radiology 125:775-780, December 1977
A
NKYLOSING spondylitis
(AS) is a well-recognized form of arthritis which produces characteristic findings in the sacroiliac joints, spine, and, less frequently, the appendicular joints in young and middle-aged adults. In the past, children and adolescents with early clinical and radiological features of AS have mistakenly been thought to have juvenile rheumatoid arthritis (JRA) (1-3), and it is only recently that the juvenile form of ankylosing spondylitis (JAS) has been fully appreciated (4-11). We wish to report the radiological findings in 28 cases of JAS followed at the Hospital for Special Surgery. The features which allow differentiation of this entity from JRA are discussed and the appendicular joint changes, which are a more prominent feature of the juvenile form, are stressed.
TABLE I:
K
CLINICALLY INVOLVED EXTRASPINAL JOINTS IN
Joint
28 PATIENTS WITH JAS
No. of Cases 22
Hip Shoulder Elbow Wrist Knee Ankle Foot Temporomarfdibular
11 4 4 14 8 8 4
findings of bilateral erosions, sclerosis, or fusion of the sacroiliac joints (12). Patients with psoriasis, Reiter's disease, and infectious arthritis were excluded. All patients had radiographs of the sacroiliac joints and lumbar spine, and also the remainder of the spine when symptoms were present there. Radiographs of symptomatic appendicular joints were obtained in most cases. In addition to routine laboratory studies, latex fixation tests were performed in all cases. HLA typing was carried out in 9 cases and HLA B 27 antigen was found to be present in 8. The most frequent erroneous diagnosis was JRA; several other patients were initially diagnosed as having rheumatic fever, Osgood-Schlatter disease, synovitis, or "growing pains."
MATERIAL AND METHODS
Twenty-eight patients (24 boys and 4 girls) with JAS were studied. Clinical records and available radiographs were reviewed systematically. Except for one 5-year-old boy, all patients were between 10·and 16 years of age (mean, 12 yr.) when symptoms were first noted. The average age at the time of correct diagnosis was 19 years. Twenty-three patients presented with complaints involving the appendicular joints. Fourteen had hip pain alone, 4 had hip pain plus back pain, and 4 had knee or ankle pain alone. Five patients had only back pain at first. Twenty-five patients (89 %) exhibited appendicular joint manifestations during the course of their disease. The distribution of involved joints is shown in TABLE I. Nine patients showed evidence of polyarticular disease, 10 showed oligoarticular symptoms, and 6 had monoarticular manifestations. The diagnosis was based on (a) a clinical history of low back pain and stiffness, unrelieved by rest and lasting for more than three months, and (b) radiological
Radiological Findings Spine: The sacroiliac joints were abnormal In all cases. Changes were always bilateral, sometimes asymmetric when first seen, but uniformly symmetrical In advanced cases. The earliest signs were indistinct joint margins and subchondral sclerosis. The joint space often appeared widened due to erosions at first; but with progression, narrowing developed and led to ankylosis (Figs. 1-3). Fusion occurred in 12 patients and was usually related to the duration of the illness.
1 From the Departments of Radiology (P.K., R.S., J.J.K.) and Medicine (M.R.) of The Hospital for Special Surgery, affiliated with New York Hospital-Comell University Medical College, New York, N. Y. Presented at the Sixty-second Scientific Assembly and Annual Meeting of the Radiological Society of North America, Chicago, 111., Nov. 14-19, 1976. 2 Present address: Bethesda Naval Hospital, Bethesda, Md. 3 Present address: Vanderbilt University Medical College, Nashville, Tenn. sjh
775
776
PAUL KLEINMAN AND OTHERS
Fig. 1. Anteroposterior radiograph of the pelvis of a 16-year-old boy shows sclerosis and erosions around the sacroiliac joints. There is circumferential narrowing of the left hip jo int space , with mild proliferative changes at the junction of the femoral head and neck . This patient first had hip pain at 12 years of age.
Fig. 3.
December 1977
Fig. 2. Anteroposterior radiograph of the pelvis of a 30-year-old man who presented with clinical symptoms of hip pain at 13 years of age. There is severe narrowing of the hip joints bilaterally, with prominent proliferative changes at the junction of the femoral head and neck and fusion of the sacroiliac joint.
35-year-old woman with fusion of the sacroiliac joints and hip joints bilaterally.
The most recent roentgenographic examinations showed spine abnormalities in 20 cases. The earliest changes were related to reactive sclerosis of the vertebral end plates, with " shining corners" progressing to squaring of the vertebral bodies (Fig. 4). Syndesmophytes and apophyseal joint fusion were seen in 13 cases (Figs. 5 and 6) and atlanto-occipital fusion in 1. Spine manifestations characteristically progressed cephalad from the lumbar region, and changes were never observed in the cervical or dorsal spine without lumbar involvement. Appendicular Joints: There was a striking incidence of appendicular joint involvement. The hips were most commonly involved, followed by the knees, shoulders, and distal joints. Demineralization, soft-tissue swelling, and synovitis were commonly present along with joint pain, but several years often elapsed before prominent bony changes became evident radiographically .
Fig. 4. Same patient as in Figure 3. Lateral radiograph of the lumbar spine shows " squaring" of the vertebral bodies with loss of concavity anteriorly. The apophyseal joints are fused. The patient presented with hip pain at 16 years of age and low back pain developed at the age of 17.
Pediatric Vol. 125
JUVENILE ANKYLOSING SPONDYLITIS
777
Radiology
Fig. 5. Anteroposterior radiograph of the lumbar spine in this 31-year-old man shows osteoporosis, fusion of the apophyseal joints, and asymmetric syndesmophyte formation . The latter was seen in several patients, none of whom had evidence of Reiter's disease or psoriatic arthritis.
The hips were radiographically abnormal in 17 cases (Figs. 1-3). The earliest change was periarticular demineralization, followed by joint-space narrowing. In more advanced cases, subchondral sclerosis and erosions of the articular surface of the femoral heads occurred. Varying degrees of proliferative changes were noted about the joint margins. A typical finding was a ring of proliferative change at the junction of the femoral head and neck (Figs. 1 and 2). The findings were "generally bilateral but usually asymmetric. Bilateral hip fusion was noted in 3 cases (Fig. 3). Periosteal new bone formation and cortical irregularity were common about the trochanters, ischia, and lateral iliac margins. The knees were frequently involved. Early changes consisted of demineralization, joint-space narrowing, and marginal erosions (Fig. 7). With progression, irregularity of the articular surfaces, subchondral sclerosis, and mild proliferative changes were noted. As in the hips, the findings were generally bilateral but asymmetric. In advanced cases, joint contractures developed, and in one case osseous fusion occurred (Fig. 8). The changes involving the shoulders were bilateral but
Fig. 6. Fusion of the apophyseal joints and anter ior subligamentous ossification can be seen in the cervical spine of this 30-year-old man. cervical spine involvement was less frequent and occurred later than involvement of the lumbar spine In this series of patients.
generally asymmetric. Mild to moderate joint-space narrowing and demineralization were usually present. Marginal erosions were noted, most commonly in the region of the greater tuberosities, varying from several millimeters to 2 cm. In advanced cases, erosions and sclerosis of the articular surfaces were present (Fig. 9). Two patients had high-riding humeral heads and faceting of the undersurface of the acromion processes, indicating chronic rotator-cuff degeneration. One patient had bilateral elbow effusions but no bony changes. Changes in the ankles and feet were usually symmetrical and consisted of moderate demineralization and diffuse joint-space narrowing. Bilateral subtalar joint fusions
778
PAUL KLEINMAN AND OTHERS
December 1977
Fig. 8. In this 26-year-old man, there Is solid bony fusion of the knee joint 10 years after the onset of symptoms.
Fig: 7. There are marginal erosions of the medial femoral condyle and tibial plateau and proliferative changes at the proximal tibiofibular Joint. Clinical symptoms developed In the knees at 12 years of age In this 19-year-old youth.
Fig. 10. Lateral radiograph of the foot of a 16-year-old boy shows fusion of the posterior subtalar joint. A large bony spur is present on the plantar aspect of the calcaneus .
Fig. 9. The lateral aspect of the humeral head is eroded (arrows). This 16-year-old boy had involvement of several other appendicular joints and had presented initially with knee and ankle pain at 11 years of age.
occurred in 2 patients (Fig. 10). Erosions were infrequent; when present, they involved the metatarsal heads. Calcaneal spurs were commonly observed. The hands and 'w rists were strikingly abnormal in 3 pa-
tients (Fig. 11). In 2, symmetrical destruction of the distal ulna and extensive erosion of the radius at the distal radioulnar jo int were noted . Additional findings included joint-space narrowing and erosions of the metacarpal heads and phalanges. Metatarsophalangeal joint subluxation and ulnar deviation occurred in one case. DISCUSSION
Since Scott's description of childhood-onset ankylosing spondylitis in 1942 (13), a pattern of clinical and radiographic manifestations has emerged (4-10). The clinical, laboratory, and radiological features of JAS , AS, JRA, and RA are listed in TABLES II and III.
JUVENILE ANKYLOSING SPONDYLITIS
Vol. 125
TABLE
II:
JAS
RA
JRA
AS
Usually Young adult Usually >10yr. Female Female Male
