Atlanto-Axial Involvement in Rheumatoid Arthritis

ORİJİNAL ARAŞTIRMA
Atlanto-Axial Involvement in
Rheumatoid Arthritis
Anıl GÜVENÇ,a
Korhan Barış BAYRAM,a
Serpil BAL,a
Hikmet KOÇYİĞİT,a
Alev GÜRGAN,a
Melda APAYDINb
Clinics of
a
Physical Medicine and Rehabilitation,
b
Radiology,
Atatürk Research and Training Hospital,
İzmir
Geliş Tarihi/Received: 15.05.2013
Kabul Tarihi/Accepted: 17.05.2013
Yazışma Adresi/Correspondence:
Korhan Barış BAYRAM
Atatürk Research and Training Hospital,
Clinic of Physical Medicine and
Rehabilitation, İzmir,
TÜRKİYE/TURKEY
[email protected]
ABSTRACT Objective: The aim of this retrospective study was to compare the clinical and laboratory findings, functional status and health related quality of life in rheumatoid arthritis (RA) patients with and without atlanto-axial subluxation (AAS). Material and Methods: Thirty five patients
who were diagnosed with RA, who had clinical signs and symptoms related to AAS, and had magnetic resonance imaging (MRI) of atlanto-axial joint, were included into the study. The hospital
records and results of MRI scans were investigated, retrospectively. Results: Fifteen (42.8 %) of 35
RA patients had AAS. The patients were divided into two groups according to the presence of AAS.
When we compare the two groups by means of treatment duration, corticosteroid use, and presence of extra-articular involvement, the differences were statistically significant. These results can
be interpreted as the involvement of atlanto-axial joint had no impact on general well-being of patients; however it is closely related with the cumulative destruction caused by the disease. Conclusion: Therefore, early diagnosis of AAS in RA patients is very important. In order to decide the
type of treatment or to predict the prognosis of disease, being aware of signs and symptoms of AAS
and even early investigation with MRI can be supportive.
Key Words: Arthritis, rheumatoid; atlanto-axial joint; magnetic resonance imaging
ÖZET Amaç: Bu retrospektif çalışmanın amacı atlantoaksiyel subluksasyonu (AAS) olan ve olmayan
romatoid artritli (RA) hastaların klinik ve laboratuar bulguları, fonksiyonel durumları ve yaşam
kalitelerini karşılaştırmaktır. Gereç ve Yöntemler: Çalışmaya RA tanısı almış, AAS varlığı ile ilişkili semptom ve bulguları olan ve atlantoaksiyel ekleme yönelik manyetik rezonans görüntüleme
(MRG) yapılmış toplam 35 hasta dahil edildi. Hastaların hastane dosyaları ve MRG raporları retrospektif olarak incelendi. Bulgular: Klinik semptom ve bulguları olan ve atlantoaksiyel MRG incelemeleri yapılmış toplam 35 olgunun 15’inde (%42,8) AAS saptandı. Hastalar AAS saptanan ve
saptanmayan olmak üzere 2 gruba ayrıldı ve her iki grup karşılaştırıldığında AAS saptanan grupta
hastalık süresi, tedavi süresi, kortikosteroid kullanımı ve ekstraartiküler tutulumun istatistiksel
olarak anlamlı oranda farklı olduğu saptandı. Bu sonuçlar RA’da atlantoaksiyel eklem tutulumunun
hastanın güncel iyilik halinden daha çok hastalığın neden olduğu kümülatif yıkımla ilişkili
olduğunu düşündürmektedir. Sonuç: Bundan dolayı RA’lı hastalarda AAS’nin erken dönemde tanısı
önem taşır. Uyarıcı semptom ve bulguların bilinmesi ve uygun hastalarda MRG incelemesinin yapılması tedavi seçimi ve prognoz tayini açısından yardımcı olabilir.
Anahtar Kelimeler: Artrit, romatoid; atlanto-aksiyel eklem; manyetik rezonans görüntüleme
Romatol Tıp Rehab 2014;25(1):8-14
Copyright © 2014 by
Türk Tıbbi Rehabilitasyon Kurumu Derneği
8
heumatoid arthritis (RA) is a disease; which is encountered all over
the world without known etiology. It is a chronic, inflammatory
and systemic disease, which involves primarily peripheral synovial
joints symmetrically, but it can also develop lesions in other tissues and orTurkiye Klinikleri
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ATLANTO-AXIAL INVOLVEMENT IN RHEUMATOID ARTHRITIS
gans.1 Cervical vertebra involvement is frequent in
Ra, which is the most important reason of head and
neck aches. RA is known to be an inflammatory
arthritis, which involves cervical vertebra most frequently.2 Atlanto-axial area is the mostly affected
region in the cervical vertebra. Since atlanto-axial
subluxation (AAS) is the most common type of instability in RA cases with cervical vertebra involvement, it is reported at different rates ranging
between 19-70% in trials.3-5 In AAS, various clinical pictures ranging from occipito-cervical pain and
minimal movement limitations to prominent neurological problems and even sudden death can be
observed. This feature of the disease is not commonly known, and in addition to this, atlanto-axial joint involvement is diagnosed very lately in the
majority of patients, which are diagnosed at the
cord compression stage and when related neurological injuries have developed. Mortality is reported
to be increased 8 times higher in RA patients with
AAS in respect to the patients without AAS.6 Magnetic resonance imagining (MRI) technique is generally preferred to evaluate AAS presence in RA
patients. MRI is preferred especially because it can
show extradural diseases, canal abnormalities and
visualize pannus; it does not contain ionized radiation and provides basic information even in the
absence of compression.7
In this retrospective study, we aimed to compare clinical and laboratory findings, quality of life and functional states in RA patients with and
without AAS involvement, which is diagnosed by
MRI.
MATERIAL AND METHODS
Patients diagnosed with RA according to American
College of Rheumatology (ACR) criteria (1988),8
who have been followed up for 36 months at our
clinics, and had medical records of clinical evaluation forms, were included into the study. These patients were examined for atlanto-axial subluxation
due to their clinical symptoms and signs by MRI,
and their records were investigated retrospectively.
Standard recorded data related to sociodemographic, disease durations, presence of concomitant
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diseases, medical treatments and morning stiffness
of patients were evaluated. Moreover, concomitantly recorded data about disease activity score
(Disease Activity Score-28, DAS-28),9 health assessment questionnaire (HAQ),10 short form-36 (SF-36)
scale11 and Steinbrocker functional classification12
were also used.
DAS-28 evaluates clinical activity of RA, and
the score is composed by the calculation of number
of swollen joints (NSJ) and number of tender joints
(NTJ) in 28-evaluated joints; ESR and patient’s global evaluation [visual analogue scale (VAS), 0-100
mm].9
In standard HAQ, there are 8 categories; dressing, standing up, eating, walking, hygiene, liftingpicking up, grasping and other activities. It is made
up of 20 questions. Answers are evaluated on 4-point scale:10
0: easily can perform
1: can perform with mild difficulty
2: can perform with quite difficulty
3: cannot perform
SF-36 scale investigates 8 dimensions of health
status in 36 items, like physical function, role limitations (related to physical and emotional problems), social function, mental health, vitality
(energy), pain and general health perception. Scale is a self-assessment scale.11
Steinbrocker functional classification evaluates patients by dividing them into 4 functional classes. These are:12
Class 1: Individual can perform all activities
without difficulty.
Class 2: Although there is sometimes discomfort in one or more joints, patient can perform normal activities at a satisfactory level.
Class 3: Patient can perform common work or
can perform very small part or none of self-care activities.
Class 4: Patient is not at a great extend or totally successful in activities, bed-ridden or wheelchair ridden and can perform very small part or
none of self-care activities.
9
Anıl GÜVENÇ et al.
Laboratory data of patients including serum Creactive protein (CRP), rheumatoid factor (RF),
erythrocyte sedimentation rate (ESR) and hemogram were evaluated.
MRI examinations of atlanto-axial joints of all
patients were performed by head coil imaging (1.5
tesla Philips). Following T1 weighted spin echo
imagining without contrast, T2 weighted gradient
echo images were obtained. Anterior AAS was defined as the distance between interior surface of atlas anterior arch and odontoid process was 2.5 mm
or more.6,13,14 Posterior AAS diagnostic criteria was
defined as loss of the median atlantoaxial distance,15 whereas lateral AAS diagnostic criteria was
defined as shifting of odontoid process more than 2
mm to the left or right at the plane, which was perpendicular to the midline that was joining anterior and posterior arches of atlas.16,17 Previous
atlantoaxial joint MRI results of patients were evaluated retrospectively by a radiologist, who was independent from the clinical signs. Presence of any
of the conditions; anterior, posterior or lateral AAS,
was accepted as AAS.
STATISTICAL ANALYSIS
SPSS (Statistical Package for Social Sciences) for
Windows 16.0 program was used for statistical
analysis. While evaluating study results, in addition to descriptive statistical methods (mean, standard deviation), normally distributed parameters in
quantitative data were compared between groups
by independent Sample t test. Qualitative data were compared by Fisher’s Chi Square test. Results
were evaluated at 95% confidence interval and
with the significance level of p<0.05.
RESULTS
A total of 35 patients were included into the study.
Demographic and clinic characteristics of patients
are shown in Table 1. RA patients were evaluated
for symptoms and signs, which might be related to
atlanto-axial joint (Table 2). None of patients had
trauma or surgical intervention history for the atlanto-axial joint. AAS was diagnosed in 15 out of
35 cases (42.8%).
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ATLANTO-AXIAL INVOLVEMENT IN RHEUMATOID ARTHRITIS
TABLE 1: Some demographic and
clinical characteristics of patients.
n=35
Age (year) (mean±SD)
54.5 ± 11.3
Gender F/M (%)
Disease duration (month) (mean± SD)
Treatment duration (months) (meant±SD)
NSAIDs use (%)
29/6 (82.9/17.1)
111.1 ± 89.4
65.8 ± 51.5
31 (88.5)
Corticosteroid use (%)
24 (68.5)
DMARD use (%)
31 (88.5)
Biological agent use (%)
6 (17.1)
Extra-articular involvement (%)
10 (28.5)
Systemic disease (%)
15 (42.8)
Rheumatoid Factor (%)
29 (82.8%)
Morning stiffness (minute) (mean±SD)
80,1 ± 42.2
NTJ (mean±SD)
15.8 ± 12.9
HAQ (mean±SD)
2.2 ± 0.7
NSJ (mean±SD)
DAS-28 (mean±SD)
6.6 ± 8.9
5.7 ± 1.5
Steinbrocker functional classification, n (%)
Class 1
5 (14.3)
Class 2
23 (65.7)
Class 4
0 (0)
Class 3
7 (20)
NSAIDs: Non-steroidal anti-inflammatory drugs; NSJ: Number of Swollen Joints;
NTJ: Number of Tender Joints; DAS-28: Disease Activity Score;
HAQ: Health Assessment Questionnaire.
TABLE 2: Symptoms and signs related to atlantoaxial
subluxation in patients with Rheumatoid Arthritis.
Occipito-cervical pain
Hoarseness
Dysphagia
Incontinence
Diplopia
n (%)
19 (54.3)
0 (0)
0 (0)
0 (0)
3 (8.5)
Vertigo
10 (28.6)
Neck-ache
29 (82.9)
Tinnitus
Limitations in neck movements
Lhermitte’s sign
Fatigue
Sensational disorders
DTR changes
Cerebellar signs
11 (31.4)
24 (68.6)
15 (42.9)
1 (2.9)
11 (31.5)
0 (0)
0 (0)
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TABLE 3: Comparisons of demographic characteristics,
clinical and laboratory findings of rheumatoid arthritis patients with and without atlanto-axial subluxations.
AAS (+)
AAS(-)
(mean±SD)
(mean±SD)
(n=15)
Age (years)
55.1±9.1
RA Duration (months)
160.1±97.9
Treatment Duration
87.4±57.3
Duration of morning stiffness (minute)
Physician’s Evaluation of Disease Progression
Self Evaluation of Disease Progression
Number of Swollen Joints
91.7±40.2
5.20±1.1
(n=20)
74.3±62.5 0.007
71.5±42.5 0.165
49.6±41
0.029
3.1±1.2
0.009
3.9±1.3
4.2±1.0
6.1±9.4
P*
54.0±12.9 0.774
0.007
6.9±8.8
0.807
5.7±1.5
0.928
Number of Tender Joints
14.3±11.7
16.9±13.9 0.569
ESR
42.9±27.6
38.5±20.8 0.591
Hemoglobin
12.5±1.3
12.3±1.3
DAS-28
5.7±1.5
CRP
25.7±28.6
18.1±25.1 0.411
0.557
*independent sample t test; p<0.05
TABLE 4: Comparisons of clinical signs and symptoms
of rheumatoid arthritis patients with and without
atlanto-axial subluxation.
Symptoms and Signs
AAS (+) n (%)
AAS (-) n (%)
Neck-ache
14 (93.3)
15 (75.0)
Tinnitus
9 (60.0)
2 (10.0)
Limitations in neck movements
13 (86.7)
11 (55.0)
9 (60.0)
2 (10.0)
Occipito-cervical pain
Vertigo
Diplopia
Lhermitte’s sign
Sensational disorders
Muscle weakness
13 (86.7)
8 (53.3)
0 (100)
13 (86.7)
1 (6.7)
6 (30.0)
2 (10.0)
3 (20.0)
2 (10.0)
0 (100)
P*
0.002
0.207
0.007
0.002
0.070
0.047
0.001
0.003
0.429
*Fisher’s Chi Square test; p<0.05.
Comparative evaluations of demographic data,
laboratory results and some clinical characteristics
of patients with and without AAS are shown in
Table 3. In our study, when patients with AAS were compared with patients without AAS, disease duration (p=0.007); treatment duration (p=0.029);
corticosteroid use (p=0.009); physician’s assessment
of disease progression (p=0.007) and self-assessment
of disease progression (p=0.009) were all higher in
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the group with AAS. However, there was no significant difference in duration of morning stiffness
(p=0.165), ESR (p=0.591), CRP (p=0.411), DAS-28
(p=0.928), number of tender joints (NTJ) (p=0.569)
and number of swollen joints (NSJ) (p=0.807) between two groups. While extraarticular involvement
was 53.3% in the group with AAS, this rate was
10% in the group without AAS (p=0.007).
When clinical symptoms and signs of patients
related to AAS were compared, signs and symptoms of occipito-cervical pain (p=0.002); tinnitus
(p=0.002); vertigo (0.007); Lhermitte’s sign
(p=0.001); sensational disorders (p=0.003) and limitations in head and neck movements (p=0.047)
were encountered more frequently in the group
with AAS (Table 4).
If distribution of patients is concerned according to Steinbrocker functional classification, number of patients in class I, II, III and IV were 5, 23, 7
and none, respectively. When patients grouped according to Steinbrocker functional classification
were compared in respect to AAS, there was no significant difference between two groups (p>0.05).
There was no difference between two groups in respect to HAQ and SF-36 subscales also (p>0.05).
DISCUSSION
Cervical involvement in RA is first defined at 1890
by Garrod.18 While RA can involve any of the cervical vertebra, it frequently involves the craniocervical region. Like in peripheral joints, it
progresses with synovial inflammation; pannus formation; ligament, cartilage and bone destruction.
Fatality of AAS development was first mentioned
in 1951 by Davis, who reported a sudden death case due to medullary compression.19
AAS development is directly increased with
the disease duration in RA. Wolf et al. reported
that AAS frequency was 13% in the first decade,
whereas this ratio was unchanged in the second decade. However, in the third decade this rate showed a marked increase and reached to 48%.20
Winfield21 and Mathews22 reported that AAS was
developed more frequently in cases at and over 5
years of age. Disease durations were significantly
11
Anıl GÜVENÇ et al.
longer in the patient group with AAS. Similarly,
treatment durations were longer in the group with
AAS. Therefore, it is suggested that this can be caused by longer durations of both disease and treatment in the group with AAS.
On the other hand, it is proposed that AAS is
encountered independently from age and is mostly
observed in males.23 Additionally, advanced age is
considered among risk factors for cervical vertebra
involvement.24 However, there were no significant
differences in age and gender in our study.
There are studies reporting that AAS involvement was frequently encountered in RA cases
using corticosteroids.22,25 Mathews et al.22 reported
that corticosteroid using cases had increased flexion capacity, which might facilitate AAS appearance. As it is commonly known, upper cervical region
involvements are observed in atlanto-axial joints in
inflammatory rheumatological diseases. This condition is closely related to atlanto-axial joint being
the most mobile joint in the cervical region. In our
study, statistically significant difference was only
detected in the steroid users in both groups, when
compared to medical treatments containing disease modifying drugs, non-steroidal anti-inflammatory drugs, and biological agents. This result was
also compliant with the results of Mathews et al.22
The most frequent predictive sign of AAS related to RA is occipito-cervical pain.26,27 Occipitocervical pain has other etiological reasons in
addition to root compression and degenerative arthritis. Especially degenerative arthritis is observed
more frequently with advanced age. Therefore, occipito-cervical pain due to other reasons should be
differentiated. In our study, we defined that occipito-cervical pain was at higher rates in the group
with AAS. In addition to this, we believe that patients with occipito-cervical pain, but without AAS
should also follow up closely, because they are under the risk. When we have investigated the presence of neck ache and AAS, there was no
significant difference between the two groups. The
other accompanying clinical sign in AAS is the limitations in neck movements. In our study, we detected significant limitations in neck movements
in patients with AAS.
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ATLANTO-AXIAL INVOLVEMENT IN RHEUMATOID ARTHRITIS
Cerebellar and spinal cord compressions, nerve root and vascular compressions were found
among neurological signs, which might develop related to AAS. Pellicci et al.28 reported in their study
that despite 80% of cervical region involvements,
only 36% of patients had neurological signs. Also,
they emphasized that 50% of RA patients were clinically asymptomatic, but they were demonstrated
to be instable radiologically There are also difficulties in neurological evaluations of RA patients. Pains that patients experience due to diffuse arthritis,
deformities and muscle atrophies also complicate
neurological examinations. Moreover neuropathies, monoarthritis multiplex and cervical subaxial
subluxations may be encountered. When it is thought that these complications might be present in
patients, it is very difficult to define whether these signs are upper cervical pathologies or not.
Starting neurological symptoms in AAS are generally encountered in the form of sensorial perception disorders. In our study, we also defined
that perception disorders in patients with AAS were significantly at higher rates than in the other
group.
It has also reported that vertebrobasilar insufficiency might be observed due to compressions of
vascular structures in AAS.29 Symptoms and signs
indicative of vertebrobasilar insufficiency may range between mild symptoms like vertigo, tinnitus
and syncope to severe ones like leading to cortical
blindness. In our study, tinnitus, one of the symptoms indicative of vertebrobasilar insufficiency,
was significantly high in the group with AAS. Similarly, other vertebrobasilar insufficiency sign, vertigo, was also higher in the AAS group.
When pyramidal tractus is involved in RA, upper motor neuron signs become marked; like increased deep tendon reflexes, pathological reflexes,
muscle weakness and spasticity. Cord compression
may end up with clinical picture of spastic paraparesis or quadriparesis. However, it is difficult to evaluate tonus, muscle strength and deep tendon
reflexes in RA due to painful joints and deformities, and, as a result, to diagnose myelopathy. In our
study, muscle weakness was detected only in one
out of 35 RA patients (2.8%). Lhermitte’s test,
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ATLANTO-AXIAL INVOLVEMENT IN RHEUMATOID ARTHRITIS
which is employed to diagnose myopathy, was detected higher in the group with AAS. This result has
suggested that patients with positive Lhermitte test
should have detailed investigations and be followed
up closely for the development of myopathy.
When the relationship between disease severity and cervical involvement is investigated in a
study,4 cervical involvement has been more frequently defined in cases with longer disease activation. In our study, there was no significant difference
between the groups in disease activity parameters
like ESR, CRP, NSJ, NTJ and DAS-28 values. We
have thought that efficient treatment to disease activity, which was given during the patient evaluation for atlantoaxial joints, might resulted in this
outcome.
In our study, we detected that results of disease progression evaluations (VAS) of both patients
and physicians were higher in the group with AAS.
VAS evaluations of patients and physicians were
parameters, which were commonly indicating cumulative effects of RA. Although there were significant differences between groups in disease
duration, treatment duration, patient’s and physician’s evaluations of disease progressions in AAS,
there were no significant differences in laboratory
1.
2.
3.
4.
5.
Firestein GS. Rheumatoid arthritis. In: Ruddy
S, Harris ED, Sledge CB, eds. Kelley’s textbook of rheumatology. 6th ed. WB Saunders
Company; 2001. p. 921-66.
Nguyen HV, Ludwig SC, Silber J, Gelb DE,
Anderson PA, Frank L, et al. Rheumatoid
arthritis of the cervical spine. Spine J 2004;
4(3): 329-34.
Boden SD, Dodge LD, Bohlman HH, Rechtine
GR. Rheumatoid arthritis of the cervical spine.
A long-term analysis with predictors of paralysis and recovery. J Bone Joint Surg Am
1993;75(9):1282-97.
Zoli A1, Priolo F, Galossi A, Altomonte L, Di
Gregorio F, Cerase A, et al. Craniocervical
junction involvement in rheumatoid arthritis: a
clinical and radiological study. J Rheumatol
2000; 27(5):1178-82.
Castor WR, Miller JD, Russell AS, Chiu PL,
Grace M, Hanson J. Computed tomography of
the craniocervical junction in rheumatoid
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findings of patient’s current disease activity, like
NSJ, NTJ and DAS-28. This result has indicated that
AAS might be related more to data showing cumulative effects of the disease rather than the data
showing the current status.
Craniocervical junction involvement due to
RA, and related subluxations may cause severe
complications like severe neurological disorders
and sudden death. In order to prevent such a complication of RA, first of all recognition of risk factors and then careful evaluations of them are very
important. Predictive signs and symptoms of atlanto-axial joint involvement, like occipito-cervical
pain, neck ache and limitations of neck movements, should be known and patients should be accurately inquired for them. These clinical signs and
symptoms can also help to identify the patient group that will be investigated radiologically. Although direct radiographic examinations may be
beneficial for pre-investigation, they do not provide detailed information in soft tissue pathologies
and myopathy. Therefore, we believe that MRI examinations can be beneficial in choosing the treatment and for the prognosis in advanced staged RA
patients, who have persistent occipito-cervical pains and neurological deficits.
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