ORIGINAL ARTICLE:
CASE SERIES
Atlo-epistropheal
involvement in oligoarthritis subset of Juvenile Idiopathic Arthritis (JIA):
observation of five cases.
A. Salmaso, A. Lurati, B. Teruzzi, G.
De Marco, M. Gattinara, I. Pontikaki, V. Gerloni and F. Fantini.
Pediatric Rheumatology Unit
Gaetano Pini Institute, Milano,
Italy.
Key words: oligoarticular JIA,
cervical spine, atlo-epistropheal, atlanto-axial, subluxation
Contact:
A. Salmaso MD
Email: ale.salmaso@email.it
Tel +390258296789
Fax +390258296293
Abstract
Cervical spine
involvement is not unusual in rheumatoid arthritis in adults and in
polyarticular and systemic juvenile idiopathic arthritis (JIA). Cervical spine
involvement, particularly atlo-epistropheal (also known as atlo-oxoid or
atlanto-axial) involvement, has not been reported commonly in either the
persistent or extended form of oligoarticular JIA. We report five cases of
children with oligoarticular JIA who developed atlo-epistropheal involvement
and discuss the anatomy, clinical characteristics, and imaging findings in this
syndrome. Though this problem is uncommon, clinicians should be aware of the
possibility of atlo-epistropheal disease in oligoarticular JIA subtypes.
Introduction
Cervical
spine disease is relatively common in rheumatoid arthritis in adults and
systemic onset and polyarticular JIA. [1-2] It usually is a sign of significant
polyarthritis. It can be quite painful and lead to cervical spine fusion with
loss of range of motion of the neck and even cervical spine instability with
neurologic compromise. [3-7] Oligoarticular JIA children have been thought to
have little risk of this involvement, particularly atlo-epistropheal disease. (Editor’s note: atlo-epistropheal is
identical to atlo-oxoid or atlanto-axial, i.e., denoting the joint between the
atlas and axis vertebrae, C1-C2.) We present 5 cases of children with
oligoarticular disease who developed very severe atlo-epistropheal disease, one
with neurological sequelae.
Patients and methods
We enrolled
patients affected by oligoarticular JIA, either persistent or extended, that
are or have been followed at our center (47.8% and 8.6% respectively, of 683
patients affected by JIA). A total of 60 patients affected by JIA extended
oligoarthritis and 327 affected by JIA persistent oligoarthritis were evaluated
with a standard X-ray of the cervical spine during full flexion and extension
of the neck. The mean age at onset of JIA was 5 years (range 2 to 14
years). Lateral view cervical spine
radiographs (in flexion and extension) were taken using a tube-to-plane
distance of 150 cm.
A diagnosis of
anterior atlantoaxial subluxation (aAAS) was made if the distance between the anterior
aspect of the dens and the posterior aspect of the anterior arch of the atlas
was greater than 3 mm. We used the 3 mm distance of Sharp and Pursner [3]
rather than the 4 mm distance suggested by Locke [15] due to the older age of
our patients at the time of our study. A CT or
Results
We report 5
patients with the oligoarthritis form of JIA (2 extended oligoarthritis; 3
persistent oligoarthritis) who have atlo-epistropheal involvement. All patients
were rheumatoid factor and anti-cyclic citullinate peptide antibodies negative;
3/5 patients were antinuclear antibody positive. One patient developed anterior
chronic uveitis. No other causes were found for these neck problems other than
JIA. Table 1 describes the 5 cases below.
|
Table I. 5 Oligoarticular JIA patients with atlo-epistropheal
involvement |
|||||||
|
Patients
# 1-5
in this
case
series |
Subtype JIA |
Age onset JIA |
Age at time of study |
Sex |
Clinical symptoms and signs
of arthritis |
Radiographic changes |
Narrowing spinal canal with or without neurological changes |
|
1 |
OE |
2 yrs |
11 yrs |
F |
P and LOF |
ST and anterior subluxation |
NO |
|
2 |
OE |
8 yrs |
11 yrs |
F |
P LOF |
ST |
YES papilledema spinal cord compression |
|
3 |
OP |
8 yrs |
11 yrs |
F |
LOF only |
erosions and dens dislocation |
NO |
|
4 |
OP |
2 yrs |
24 yrs |
F |
P LOF |
erosions and dens dislocation |
NO |
|
5 |
OP |
3 yrs |
34 years |
M |
none |
erosions and ST |
NO |
OE = oligo extended
OP = oligo persistent
P = pain
LOF = loss of function
ST = synovial thickening
Patient 1 is a 11
year old girl (onset age: 2 years) with radiological evidence of anterior
atlo-epistropheal subluxation caused by the presence of synovial thickening,
leading to pain and loss of function (LOF) of cervical spine. The spinal canal
diameter had no signs of narrowing. Patient 2 is a 11 year old girl (onset age:
8 years) with radiological evidence of synovial thickening between the dens and
the atlas anterior arch. There was pain and limitation of motion (LOM) of the
cervical spine. Spinal cord compression was present with concomitant bilateral
papilledema. There was no other sign of increased intracranial pressure.
Patient 3 is a 11
year old girl (onset age: 8 years) with radiological evidence of erosions and
vertical dislocation of the dens. Only loss of function of the cervical spine
was present and there was no pain. No neurologic involvement was detected.
Patient 4 is a 24 year old girl (onset age: 2 years) with radiological evidence
of erosions and vertical dislocation of the dens. She also had neck pain and
LOM of the cervical spine. No sign of neurological involvement was found.
Patient 5 is a 34 year old man (onset age of JIA: 3 years) with radiological
evidence of erosions of the dens and the presence of synovial thickening in the
atlo-epistropheal junction. He had no neck pain or LOF. His spinal canal was
without signs of compression.
Discussion
Anatomy
Human cervical spine consists of seven vertebrae C1 - C7. The two most
cranial vertebrae have special architectural design and the other five share a
similar structure. In this small area between the skull and first thoracic
vertebra, there are 16 serially arranged apophyseal synovial joints, 12
uncovertebral joints and six intervertebral discs (Figure 1).
Figure 1
Atlo-epistropheal (atlanto-axial) anatomy by a anterior-posterior view
The most cranial vertebrae “atlas” is a solid bone ring with two lateral
pillars for the apophyseal joints. It carries the skull by two ellipsoid
shaped joints, which allows only flexion and extension movement. The second
vertebrae “axis” has a special structure called “odontoid process” (or dens),
which rises perpendicularly from midbody, acting as an eccentric pivot around
which the atlas rotates. The odontoid process has articulation in the anterior
surface with the anterior arch of atlas and in the posterior surface with the
transversal ligament. In addition, the axis comprises two apophyseal joints
with atlas and two with the third vertebra. Approximately 50% of head rotation
occurs in the atlantoaxial joints and 85% of the whole head and neck movement
in the skull-atlas-axis complex.
The odontoid
process is fixed to the anterior arch of atlas by a strong transverse ligament.
It allows rotational movement but prevents the atlas from slipping forward when
the head is in flexion. In addition, the odontoid process is attached to the
occipital bone by an apical and two alar ligaments, which increases the
stability of both atlanto-occipital and atlantoaxial joints.. The junction of
medulla oblongata and spinal cord is at the level of the odontoid process.
The third to the seventh cervical vvertebrae all consist of body, pedicles, laminae, vertebral arches, and
spinous process. The most important ligaments connecting vertebral bodies
together are the anterior and posterior longitudinal ligaments, which continue
as membrane-like structures to the occipital bone [Figure 2]. The laminae of
vertebrae are connected together by ligamenta flava.
Figure 2.
atlo-epistropheal anatomy in cross-section
Symptoms and signs
Neck pain is a common symptom in atlo-epistropheal arthritis in
rheumatoid arthritis (RA) in adults, regardless of the findings in cervical
spine radiographs (Figure 3). [1] However, neck pain is non-specific. It is
also the most common and earliest manifestation of other cervical spine
disorders involving any cervical vertebrae including chronic arthritis. [1-2] In addition to neck region, pain caused by cervical
spine destruction may be experienced in occipital, retroorbital or temporal
areas. [3] It is also important to bear in mind that subluxations of the
cervical spine do not necessary cause pain or other symptoms. In a study by
Mathews, two-thirds of patients with anterior atlantoaxial subluxation (aAAS)
(atlanto-axial or atlo-epistropheal subluxation) did not have neck pain. [4]
Moreover, Collins et al. reported that 50% of the patients with cervical spine
instability were asymptomatic. [5]
Figure 3. An
lateral view showing an atlantoepistropheal pannus due to chronic arthritis
Complications
Patients with
severe cervical spine disorders may present symptoms and signs caused by
compression of the spinal cord, cervical nerve roots or cranial nerves. [6] In
addition, penetration of the odontoid process through the foramen magnum may
cause the compression of brain stem and even sudden death. [7] Neurological
symptoms and signs have been reported to correlate poorly with the degree of
atlantoaxial instability. [8, 4, 9-10] An
Figure 4:
An
The primary radiological examinations of the cervical spine in patients
with RA are plain radiographs. The standard cervical spine radiographs
include anteroposterior, odontoid, lateral and oblique projections. In the
majority of rheumatological units, lateral view radiographs are taken during
full flexion and extension of the neck.
Sharp and Purser [3] measured the distance between the anterior arch of
atlas and the anterior surface of the odontoid process in two lateral view
cervical spine radiographs (flexion and
extension views) taken from a general population and from patients with RA. They
demonstrated that in an adult population more than 3 mm separation is abnormal
and in RA patients a greater than 3 mm finding is likely due to the arthritis.
Hereafter, more than 3 mm anterior atlantoaxial distances have been considered
to indicate aAAS in RA by the majority of the investigators. [11-14] Locke and
colleagues found this distance to be more than 4 mm in normal children. [15]
Boden et al. [16] defined a new radiographic parameter, i.e., the
posterior atlanto-odontoid interval (PADI), which is the distance between the
posterior aspect of the odontoid process and the anterior edge of the posterior
arch of atlas in lateral view cervical spine radiographs. In their study, the
sagittal diameter of the bony spinal canal was the most important predictor of
paralysis and postoperative neurological recovery in patients with aAAS. [16]
Values of 14 mm or less were determined to be critical for the development of irreversible
myelopathic changes.
CT scan has been
particularly valuable in the evaluation of the severity of aAAS. However, after
the development and increase in availability of
Cervical
spine disease in JIA
Cervical spine
involvement in adult rheumatoid arthritis has been described in several studies
[7-10] and constitutes one of the typical expressions of the disease. Juvenile
idiopathic arthritis (JIA) is a systemic disease of childhood affecting
primarily the joints (Durban’s 1997 Criteria). [19] Detailed information on
cervical spine changes in patients with JIA is available in only a few studies.
In patients with JIA, the cervical spine is often affected usually at level of
the interapophyseal joints (often+ starting at C2-C3), leading to pain and
functional limitations (Figure 5).
Figure 5. A lateral radiograph of the cervical spine demonstrating C2-C3
interapophyseal disease in a child with JIA.
Other typical changes
in the cervical spine of systemic and polyarticular JIA children include fusion
of adjacent spinous processes, narrowing of the intervertebral disk, and
atlantoaxial subluxation. [20]
The atlantoaxial
involvement has been considered uncommon
in JIA, with the exception of the RF+ forms (analogue to adult RA). [20-24] It
is important to note that in adult RA and in JIA, sustained rheumatoid
inflammation of the atlantoaxial apophyseal joints causes cartilage
destructions and finally bone erosions leading to atlantoaxial impaction, which
has also been referred to as vertical atlantoaxial subluxation, basilar
invagination, or cranial settling. [6]
In the
oligoarthritis JIA, common findings include large joint arthritis of 4 joints
or less in the first six months (e.g., knee, ankle, wrist, hip) and anterior chronic uveitis that is associated
with a positive antinuclear antibody titer. Only rare cases have been reported
previously of atlantoepistropheal involvement in JIA oligoarticular children.
[20-24] For example, Hensinger et al. reviewed 121 JRA patients in 1986, among
whom were 57 children with pauciarticular subtype. None had signs or symptoms
of cervical spine disease including neck pain or neurological changes and only
one child had roentgenographic involvement. [22] Our experience suggests that
atlo-epistropheal disease including neurological compromise due to subluxation
may occur in children with oligoarticular disease and though unusual in our
population (5/387 or 1.3%), does not appear to be rare and should be watched
for. It suggests that oligoarticular JIA is not always a benign disease.
Conclusions
Atlo-epistropheal arthritis with possibe subluxation has
previously been described in the rheumatoid factor positive JIA group. [19-23] This
report emphasizes that atlo-epistropheal involvement may occur in
oligoarthritis JIA, including in both the extended and the persistent
oligoarticular forms. More studies are necessary to assess the true prevalence
of atlo-epistropheal involvement in different populations of children affected
by JIA. In the meantime, it is important to be vigilant for cervical spine
disease in children with oligoarticular JIA, including regular range of motion
exams of the neck, particularly as the children may not complain of neck pain.
References
1.
Pellicci PM, Ranawat CS, Tsairis P, Bryan WJ.
prospective study of the progression of rheumatoid arthritis of the
cervical spine. J Bone Joint Surg Am. 1981;63:342-350.
2. Rawlins
BA, Girardi FP, Boachie-Adjei O. Rheumatoid arthritis of the cervical spine
Rhem Dis Clin North Am. 1998;24:55-65.
3. Sharp J
, Purser DW. Spontaneous atlanto-axial dislocation in ankylosing spondylitis
and rheumatoid arthritis. Ann Rheum Dis. 1961;20:47-74.
4. Mathews
JA. Atlanto-axial subluxation in
rheumatoid arthritis. Ann Rheum Dis. 1969;28:260-266.
5. Collins
DN, Barnes CL, Fitzrandolph RL. Cervical spine instability in rheumatoid
patients having total hip or knee arthroplasty. Clin Orthop. 1991;272:127-135.
6.
Santavirta S, Kankaanpaa U, Sandelin J, Laasonen E, Konttinen YT, Slatis
P, et al. Evaluation of patients with
rheumatoid cervical spine. Scan J Rheumatol. 1987;16:9-16.
7.
Mikulowski P, Wollheim FA, Rotmil P, Olsen I. Sudden death in rheumatoid
arthritis with atlanto-axial dislocation. Acta Med Scand. 1975;198:445-451.
8. Conlon
PW, Isdale IC, Rose BS. Rheumatoid arthritis of the cervical spine. An analysis
of 333 cases. Ann Rheum Dis. 1966;25:120-126.
9. Rana NA.
Natural history of atlantoaxial subluxation in rheumatoid arthritis. Spine
1989;14:1054-1056.
10. Floyd
AS, Learmonth ID, Mody G, Meyers OL.
Atlantoaxial instability and neurologic indicators in rheumatoid
arthritis. Clin Orthop. 1989;177-182.
11. Smith
PH, Benn RT Sharp J. Natural history of rheumatoid cervical luxations. Ann
Rheum Dis. 1972;31:431-439.
12. Park
WM, O’Neill M, McCall IW. The radiology of rheumatoid involvement of the
cervical spine. Skeletal Radiol. 1979;4:1-7.
13. Halla
JT, Hardin JG. The spectrum of atlantoaxial facet joint involvement in
rheumatoid arthritis. Arthritis Rheum. 1990;33:325-329.
14. Boden
SD, Dodge LD, Bohlman HH, Rechtine GR. Rheumatoid arthritis of the cervical
spine. J Bone Joint Surg Am. 1993;75:1282-1297.
15. Locke
GR, Gardner JI, Von Epps EF. Atlas-dens interval (
16. Boden SD.
Rheumatoid arthritis of the cervical spine. Spine 1994;19:2275-2280.
17.
Pettersson H, Larsson EM, Holtas S, Cronqvist S, Egund N, Zygmunt S, et al. MR
imaging of the cervical spine in rheumatoid arthritis. Am J Neuroradiol. 1988
May-June;9:573-577.
18.
Reijnierse M, Breedveld FC, Kroon HM, Hansen B, Pope TL, Bloem JL. Are magnetic
resonance flexion views useful in evaluating the cervical spine of patients
with rheumatoid arthritis? Skeletal Radiol. 2000;29:85-89.
19. Petty
RE, Southwood TR, Baum J, Bhettay E, Glass DN, Manners P, et al. Revision of the proposed
classification criteria for juvenile idiopathic arthritis: Durban 1997. J Rheumatol.
1998;25:1991-4.
20. Martel
W, Holt JF, Cassidy JT. Roentgenologic manifestations of juvenile rheumatoid
arthritis. AJR. 1962;88:400-23.
21.
Grokoest AW, Snyder AI , Ragan C. Some aspects of juvenile rheumatoid
arthritis. Bull Rheum Dis. 1957;8:147-8.
22.
Hensinger RN, DeVito PD, Ragsdale CG. Changes in the cervical spine in juvenile
rheumatoid arthritis. J Bone Joint Surg AM. 1986 Feb;68(2):1986-98.
23. Espada
G, Babini JC, Maldonado-Coccoja, Garcia-Mortero O. Radiologic review: The
cervical spine in juvenile rheumatoid arthritis. Semin Arthritis Rheum.
1988;17:185-95.
24. Laiho
K, Savolainen A, Kautiainen H, Kekki P, Kauppi M. The cervical spine in
juvenile chronic arthritis. Spine Journal 2002;2:89-94.