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Cervical spondylitis in rheumatoid disease
Case Reports Cervical
Spondylitis
in Rheumatoid
A Comment on Neurologic
Significance
WILLIAM MARTEL, Ann Arbor,
Disease*
and Pathogenesis
M.D
Michigan
Involvement of the cervical spine in rheumatoid arthritis can lead to neurologic complications which may go unrecognized in the presence of severe arthritic disease. Described herein is a patient in whom quadriparesis developed gradually and in whom the effects of the vertebral lesions were documented by arteriography and myelogof thorough roentgenologic evaluation of these patients is raphy ; the importance emphasized. Theories as to the pathogenesis of the vertebral lesions are discussed, including the oossibilitv that a “neuronathic effect” may be more important in this disease ;kan has been rkalized.
T
HE
cervical
spine
rheumatoid
is frequently
disease?
and
chronic
affected
ization she experienced occasional episodes of faintness, particularly on arising in the morning, and for several days she had low backache and numbness of the posterior aspect of her right thigh. She noted progressive muscular weakness for several montlis, particularly in her upper extremities, which had been attributed to the arthritis. Occasionally. there was numbness and tingling in her extremities on bending her head forward. Th e patient had been followed at The university of Michigan Medical Center since 1939. She had severe destructive arthritis which progressively involved most of her joints. There were numerous subcutaneous rheumatoid nodules. She had received steroid therapy intermittently for several years and underwent a joint biopsy in 1960 which led to a diagnosis of “rheumatoid synovitis.” Roentgenologic examination of the cervical spine, performrd as part of a roentgenologic survey (I was attempting to gauge the prevalence of spinal involvement in rheumatoid disease), disclosed atlas subluxation and narrowing of the intervertebral discs between the second and third and sixth and seventh cervical vertebrae (Fig. 1). ‘The antrroposterior diameter of the spinal canal in Aexion at thr l~rl 01 the first cervical vertebra was 15 mm. ‘l’hes~ lesions were apparently asymptomatic. Re-examination in 1963, at which time the patient was also eysentially asymptomatic neurologically, showc~l further su tAuxation of the atlas and destruction of the vrrtrbral rndplates and apophyseal joints of the ttlirtl, fourth.
in
vertebral
[ 1-51. This and may be fatal [S]. Described herein is a patient with severe rheumatoid disease in whom progressive cervical involvement over a period of several years led to quadriparesis. The true nature of the patient’s symptoms was not realized at first. It was only after a review of serial roentgenograins, obtained over a six year interval, that the significance of the patient’s clinical manifestations hecame apparent. Furthermore, the effects of thca vrrtcbral lesions were clearly documented preoperativrly by vertebral arteriography and rnyclography. subluxation
is
complication
commonly
is
often
present
insidious
CASE
REPORT
iifty-four year old white woman (H.K. 524652) who had progressively severe rheumatoid arthritis for twenty-seven years complained of falling down on two separate occasions during the week prior to her hospitalization in November 1966. These episodes were unassociated with vertigo, visual deficit or unconsciousness and she attributed her difficulty to a “buckling of the kneeq.” During the two weeks prior to hospitalA
4 A synonym tinguished
from
for rheumatoid ankylosing
* From the Department March vo,..
arthritis,
to be
dis-
spondylitis,
of Radiology,
The University
of Michigan,
16, 1967. 44,
MARCH
1968
441
.\nn :\rbor, Michigan.
Malkuscript
rc-wived
442
Cervical
Spondylitis
in Rheumatoid
Disease-A4artel
2B
2A
FIG. 1. Cervical spine, 1960. The dislocation of the atlas is evident in the flexion position only. The atlanto-odontoid interval measures 9 mm. in flexion and the anteroposterior diameter of the spinal canal is 15 mm. at the level of the first cervical vertebra. The discs between the second and third and the sixth and seventh cervical vertebrae are reduced in height and there are small anterior osteophytes. FIG. 2. Cervical spine, 1963. A, slight flexion. B, midline laminagram. The atlanto-odontoid interval now measures 13 mm. and the diameter of the spinal canal at the first cervical vertebra is 11 mm. There is extensive destruction of the vertebral end-plates at the fourth and seventh cervical vertebrae. Note the slight malalignment at these levels and the erosions of the apophyseal joints at the third and fourth cervical vertebrae. FIG. 3. Cervical spine, 1966. Flexion. The intervertebral discs between the third and fourth and sixth and seventh cervical vertebrae have been destroyed and there is considerable bone loss particularly between the third and fourth cervical vertebrae with resultant vertical shortening of the spinal canal. The atlas is not fused and the spinal canal at the first cervical vertebra still measures 11 mm. Note the resorption of the discs between the third and fourth, fourth and fifth and sixth and seventh cervical vertebrae, with apposition and apparent partial fusion of the vertebral bodies.
sixth and seventh cervical vertebrae. The spinal canal at the level of the first cervical vertebra now measured 11 mm. (Fig. 2). Physical examination both in 1960 and in 1963 showed no definite evidence of a neurologic deficit related to these spinal lesions. In November 1966 physical examination disclosed rather severe muscular weakness and diminished deep pain sensation in the upper extremities compared to the lower ones. There was diminished sensa-
tion to pinprick in both hands, particularly on the left side. Vibration and position discrimination were intact. The deep tendon reflexes were hyperactive and there were bilateral extensor plantar reflexes and positive Hoffman signs. The cranial nerves were intact. Roentgenologic examination of the cervical spine showed no significant increase in the degree of atlas displacement but there was bone loss in the third, fourth and sixth cervical vertebral bodies with miniAMERICAN
JOURNAL
OF
MEDICtNE
C:ervical
Spondylitis
in Rheumatoid
Ikeasc-
dlmrie/
part it rs intact and in the midline.
mal ne\v lrone formation and partial anterior fusion at tlwsc. Arcs (Fig. 3,X). ‘The left atlantoaxial joint was srverel~ eroded and the left lateral masses of the first and second cervical wrtebrae were compressed (compare Fiq. 4B ancl 4.4). In view of these changes and the patient’s symptoms, left vertebral arteriography was performed. l’herc \serc tlvo kinks in the vertebral artcr!-. presumably dare to the foreshortening of the spine I I:&. SA), In addition, there were tvvo areas of stenosis al and jrist I~elow the region of the foramen transvt’rsarium of the second cervical vertebra which were f)robably secondary to the destructive bone and joint lesions (~Fig. SB). Lumbar puncture showed the spinal tluid pressure and protein concentrations to be normal; the Queckenstedt test \vas negative. Myrlography disclosed an ertraclural defect, thought to be dr~c to a herniated intervertebral disc at the junction of the fourth and fifth lumbar vertebrae. There was no obstruction to the passage of pantopaqtw through the cervical subarachnoid space. The transverse diameters of the spinal cord and spinal subarachnoid space at the level of the fifth cervical vertcl,ra were 19 and 31 mm., respectively,* and there was no evidence of syringomyelia or spinal cord atrophy. There \vas a shallow defect anteriorly at the junction of the fifth and sixth cervical vertebrae of uncertain significance, possibly due to a minimally cxtrucled disc or osteophyte, and posteriorly there
were multiple
irregularities
thought
to be due to the
dura and liqamenta fiava (Fig. 6). This exaggerated effect was thought to be due to the redundancy of these tissues secondary to the foreshortening of the spinal canal. The subarachnoid space appeared to * I.ncorrccted
for magnification.
taper at tlie first and ~cconcl cervical \~:~~t~~Or~ic ,jnct measured 10 mm. anteroposteriorly. Sorue 01’ 11~ pantopaque passed into the posterior fossa. Following the application of cervical traction for several tlaysl muscular strength appeared to improve in tile upper extremities. Cervical spirit: films obtained in the operating room while tire l)atient \vas in traction showed considerable diminrrtion in tire clegrec of atlas displacement. The patient nnc~erwrnt laminectomy ancl fusion of thr cervical \pine on November 2.3, 1966. ,Jt the time of surgery in \vas noted that the ligamenta Hava over tire 1011cr cervical spine wcrc slightly thickened and inspecrion of the spinal cord at the level of the fifth ant1 iivtir cervical \,ertebrae suggested to the surgeons that there was “slight spinal cord atrophy ancl pallor‘. ‘l’hcre \vas no gross extrusion of the inter\wtrbral tlisc at t11e junction of the fifth and sixth cervical vertebrae. The patient’s symptoms diminished in the immediate postoperative period. COMMENTS
Nontraurnatic atlas dislocation trlay bc fatal in rheunlatoid arthritis affecting the cervical spine and it is therefore particularly important to recognize the possibility of this complication whenever these patients present unttsual rnusculoskeletal synlptorns. Keurologic evaluation of such syrnptorns is particularly difficult in these patients 1.51. They have crippling joint deforrnities, often with secondary nruscular atrophy, [ 71 may mask and peripheral polyneuropathy symptoms of a central lesion. Furthtrrnore, this
444
Cervical
5A
Spondylitis
in Rheumatoid
Disease-MarteI
5B
6
FIG. 5. Left vertebral arteriogram. A, lateral projection. B, anteroposterior view. There are two kinks in the vertebral artery, presumably due to foreshortening of the spinal canal. In addition, there are two areas of stenosis (arrows), seen best in the anteroposterior view, at and just below the region of the foramen transversarium of the second cervical vertebra. Note the left lateral mass of the first cervical vertebra (retouched) (large arrow). FIG. 6. Cervical myelogram. Lateral projection, patient supine. There is no evidence of syringomyelia or spinal cord atrophy. The transverse diameters of the spinal cord and spinal subarachnoid space at the fifth cervical vertebra are 19 mm. and 31 mm., respectively, which is within normal limits [27]. The anteroposterior diameter of the subarachnoid space at the first cervical vertebra (measured from the ventral aspect of the pantopaque column to the posterior bony margin of the canal) is 10 mm. There is a suggestion of tapering within the pantopaque column (arrow) at the first cervical vertebra. Note the posterior irregularities particularly at the fifth cervical vertebra, probably due to redundant dura and ligamenta flava. A shallow anterior defect at the fifth and sixth cervical vertebrae is of doubtful significance in view of the negative findings at surgery with regard to this site.
disease frequently dictates a sedentary existence which may cause certain neurologic deficits to go undetected. The patient herein described in retrospect probably had significant neurologic symptoms for at least three months prior to her hospitalization. Awareness of what the previous roentgenograms had shown in this case prompted the request for further studies, including vertebral arteriography and myelography, which in turn led to a better evaluation of the patient. Cervical myelopathy and radiculoneuropathy may result from chronic spinal cord or nerve root compression, secondary to vertebral subluxation, or to ischemia [2,8] as a result of narrowing of the vertebral, the anterior or posterior spinal and radicular arteries. Arterial compression may be secondary to vertebral subluxation
or to rheumatoid destruction of the apophyseal joints in view of their proximity to the vertebral arteries. Intervertebral disc extrusion may also be a significant factor. This patient appeared to have such a lesion in the lumbar spine. Cervical nerve root compression by an extruded disc was recently observed in a young adult who had had rheumatoid arthritis with cervical involvement as a child [9]. Any of these three factors may be operative and thorough roentgenologic evaluation in certain cases, including myelography and vertebral angiography, is therefore advisable, particularly prior to surgical correction. A number of these patients with severe vertebral subluxation have had a surprising lack of commensurate neurologic manifestations [5]. This may be related to the slow development of AMERICAN
JOURNAL
OF
MEDICINE
C:er\4cal
Spondylitis
in Kheurnatoicl
IIIC’W I&~ns. allowing an adaptation of thr xpmal cord. or to the frequently associated bone destrllction, lea\,ing nlore rooln for the cord itself I_‘]. On the other hand, this discrepancy may rpfl(.ct tile role of spinal cord ischcmia and the fact that attcnrralion of the arterial supply is not nclccxssarily proportional to the degree of \.ertrhral destruction and sltbluxation. It is of interest lhat in this patient the reduced anteroposterior diameter of the spinal canal at the first cervical vertebra did not change appreciably between 1963 and 1966 but neurologic manifestations first developed in 1966. Perhaps the narrowing of the vertebral artery occurred during this interval in view of the progressive destruction of the adjacent left atlanto-axial joint. Kecently, Turnbull et al. [ 701 questioned whether \,ertebral artery narrowing could result in ischelnia of the spinal cord and emphasized the numerous collateral pathways. Conceivahl>-, in this case the vertical foreshortening of the spinal canal nlay have aggravated an alread) inarginal situation with regard to compressioll of the spinal cord or its arteries. Possibly, such foreshortening may have caused traction 011 the nerve roots or radicular arteries. On the other hand, delayed myelopathy in traumatic and congenital abnormalities of the craniovertebral region has been recognized [II, 721 and? whatever its mechanism, perhaps it occurs in this situation as well. There appears to be a predilection for the cervical spine in rheumatoid disease, the basis for which is not clearly understood. The normally greater mobility of this segment, compared to the rest of thr spine, is probably an important factor. There is some evidence that usage and mechanical stress may enhance the destructive process in the peripheral joints [ 7.3,74]. The cervical inter\rertebral disc spaces are commonly found to be reduced in height at multiple levels [I 41. Osteophytes tend to be absent or small at these sites but this may reflect the inability of the rheumatoid patient to form bone rather than anything specific about the intervertebral disc lesions [75]. One may speculate as to the nature of these lesions inasmuch as cartilaginous joints are not commonly affected in rhcxumatoid disease, although they are frequently involved in ankylosing spondylitis. Perhaps in\~olvement of the diarthrodial apophyseal joints further increases the mobility of the indilidrtal crrlical vertebrae and premature degeneration of the cartilage plates supervenes. If v0
1.
44,
MARCH
1968
l>iseaye
- AZ;lor~~d
-1-i.?i
this is trur. the. \.prtrbral end-plate d(>htr-rlction, such as was present in this patient, Illa> in part be drle to intravertehral disc herniatiolls and represent largely a degencrativr rather I hair an inflarnlnatory process. Parentheticall), tilt, pwscncc of small alnounts of pannus does not nwc+ sarily preclrlde this interprrtation. 111drrcl. rstrusions of disc material into the \-rrt&ral bodies has been observed [!)I and narrowing 01 the intcrvrrtebral disc spaces of the 1ulnba1 spine may be significantly Inore cc~nImon in patients with rheumatoid dlseasc [ /li /r 1. IlO\\-ever, an additional possibility to cxplaill the involvement of these cartilaginous joints slho\lld be taken into account. The t\nco\.ertrbral (Luschka) joints are syno\?al in character and apparently are acquired, inasmuch as the! arc’ not observed in children. Should these joints become affected, their contiguity wit11 the ‘iI,tervertebral discs might lead to destruction of the latter. It is noteworthy in this rcqard that vertebral end-plate erosion of the type illustrated (Fig. 2) is rare in juvenile rhrumatoid arthritis I/9]. Earlv fusion of the cervical apophyseal joints is characteristic of the discasr in children, however, and this lnay confer solne protection to the anterior cartilaginolls joints. Indeed, following such fusion of t lx apophyseal joints, the intervertebral discs characteristicall) become atrophic. A similar sequence illa)’ be observed at isolated cervical levels in adult>, with this disease. It appears that rheumatoid destrllction of the apophyseal joints in adults is often followed by “erosion” of the \-ertcf)ral rndplates at that level, whereas, apophysral ank>-losis is usually associated with atroph!. of tile adjacent intervertebral disc with sparing l)f the vertebral end-plates [ 181. It does not seem unreasonable to speculate that in some people a “neuropathic effect” Ina!’ be operative in addition to the rherrlnatoid process. This could be due to peripheral nruropatlry or to a lesion of the spinal cord [Xl. particularly in view of the destructive cervical spondylitis which may be present. The surgeon’s obser\.ation that the spinal cord appeared slightl) atrophic is of interest but of uncertain siqnificance. The ratio of the transverse diameters of the spinal cord and spinal subarachnoid space as Ineasured on the Inyelogram was within nortllal limits 1271. It is conceivable, howe\,er, that a rnininlal atrophic change may not be dctrctablc 1)) myelography. Although it has not bcrn possible thus far to document clinical cvid(,ncc w sup-
446
Cervical
Spondylitis
port this hypothesis of a neurogenic
in Rheumatoid
basis for
bone resorption in this disease [5], attention should be directed to postmortem examinations of the spinal cord in these subjects.
Acknowledgment: I appreciate the support of Ivan F. Duff, M.D., in making this patient available for roentgenologic evaluation. The surgery was performed by Richard C. Schneider, M.D. and Robert W. Bailey, M.D. of the University of Michigan Medical Center. REFERENCES 1. MARTEL, W.
2.
3.
4.
5.
6.
7.
8.
and PAGE, .I. W. Cervical vertebral erosions and subluxations in rheumatoid arthritis and ankylosing spondylitis. Arthritis & Rheumat., 3: 546-556, December 1960. MARTEL, W. The occipito-atlanto-axial joints in rheumatoid arthritis and ankylosing spondylitis. Am J. Roentgenol., 86: 223, 1961. MARTEL, W. Occipito-atlanto-axial joints in rheumatoid arthritis. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Congress Series No. 61, p. 189. Amsterdam, 1963. Excerpta Medica Foundation. SHARP, J. and PURSER, D. W. Spontaneous atlantoaxial dislocation in ankylosing spondylitis and rheumatoid arthritis. Ann. Rheumat. Dis., 20: 47, 1961. MARTEL, W., DUFF, I. F., PRESTON, R. E. and HAYES, J. T. The cervical spine in rheumatoid arthritis; correlation of radiographic and clinical manifestations. (Abstract.) Arthritis & Rheumat., 7: 326 1964. MARTEL, W. and ABELL, M. R. Fatal atlanto-axial luxation in rheumatoid arthritis. Arthritis & Rheumat. 6: 224, 1963. FREUND,H. A., STEINER,G., LEICHTENTRITTB. and PRICE, A. E. Peripheral neuropathy in chronic atrophic arthritis. Am. J. Path., 18: 865, 1942. SCHNEIDER,R. C. and CROSBY, E. C. Vascular insufficiency of brain stem and spinal cord in spinal trauma. Neurology, 9: 643, 1959.
Disease-Martel
9. MARTEL, W. Personal observations. 10. TURNBULL, I. M., BRIEG, A. and HASSLER, 0. Blood supply of the cervical spinal cord in man. A microangiographic cadaver study. J. Neurosurg., 24: 951, 1966. 11. BACHS, A., BARRAQUER-BORDAS,L., BARRAQUERFERRE, L., CANADELL, J. M. and MODELELL, A. Delayed myelopathy following atlanto-axial dislocation by separated odontoid process. Brain, 78: 537, 1955. 12. LIST, C. F. Neurologic syndromes accompanying developmental anomalies of occipital bone, atlas and axis. Arch. Neural., 45: 577, 1941. 13. MARTEL, W., HAYES, J. T. and DUFF, I. F. The pattern of bone erosion in the hand and wrist in rheumatoid arthritis. Radiology, 84: 204, 1965. 14. CASTILLO, B. A. and SCOTT, R. A. Physical activity, cystic erosions and osteoporosis in rheumatoid arthritis. Ann. Rheumat. Dis., 24: 522, 1965. 15. MARTEL, TY. Discussion: Lumbar spine. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Contress Series No. 61, p. 260. Amsterdam, 1963. Excerpta Medica Foundation. 16. LAWRENCE, J. S. and SHARP, J. Lumbar spine. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Congress Series No. 61, p. 239. Amsterdam, 1963. Excerpta Medica Foundation. 17. DE SEZE, S., DEBEYRE, N. and DJIAN, A. Radiological study of the dorso-lumbar spine in rheumatoid arthritis. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Congress Series No. 61, p. 251. Amsterdam, 1963. Excerpta Medica Foundation. 18. MARTEL, W. Further observations on the spine in rheumatoid disease. To be published. 19. MARTEL, W., HOLT J. F. and CASSIDY, J. T. Roentgenologic manifestations of juvenile rheumatoid arthritis. Am. J. Roentgenol., 88: 400, 1962. 20. MARTEL, W., BRODY, G. D. and CASSIDY, J. T. A lesion of the spinal cord in a case of juvenile rheumatoid arthritis. To be published. 21. KHILNANI, M. T. and WOLF, B. S. Transverse diameter of cervical spinal cord on pantopaque myelography. J. Neurosurg., 20: 660, 1963.
AMERICAN
JOURNAL
OF
MEDICINE
Spondylitis
in Rheumatoid
A Comment on Neurologic
Significance
WILLIAM MARTEL, Ann Arbor,
Disease*
and Pathogenesis
M.D
Michigan
Involvement of the cervical spine in rheumatoid arthritis can lead to neurologic complications which may go unrecognized in the presence of severe arthritic disease. Described herein is a patient in whom quadriparesis developed gradually and in whom the effects of the vertebral lesions were documented by arteriography and myelogof thorough roentgenologic evaluation of these patients is raphy ; the importance emphasized. Theories as to the pathogenesis of the vertebral lesions are discussed, including the oossibilitv that a “neuronathic effect” may be more important in this disease ;kan has been rkalized.
T
HE
cervical
spine
rheumatoid
is frequently
disease?
and
chronic
affected
ization she experienced occasional episodes of faintness, particularly on arising in the morning, and for several days she had low backache and numbness of the posterior aspect of her right thigh. She noted progressive muscular weakness for several montlis, particularly in her upper extremities, which had been attributed to the arthritis. Occasionally. there was numbness and tingling in her extremities on bending her head forward. Th e patient had been followed at The university of Michigan Medical Center since 1939. She had severe destructive arthritis which progressively involved most of her joints. There were numerous subcutaneous rheumatoid nodules. She had received steroid therapy intermittently for several years and underwent a joint biopsy in 1960 which led to a diagnosis of “rheumatoid synovitis.” Roentgenologic examination of the cervical spine, performrd as part of a roentgenologic survey (I was attempting to gauge the prevalence of spinal involvement in rheumatoid disease), disclosed atlas subluxation and narrowing of the intervertebral discs between the second and third and sixth and seventh cervical vertebrae (Fig. 1). ‘The antrroposterior diameter of the spinal canal in Aexion at thr l~rl 01 the first cervical vertebra was 15 mm. ‘l’hes~ lesions were apparently asymptomatic. Re-examination in 1963, at which time the patient was also eysentially asymptomatic neurologically, showc~l further su tAuxation of the atlas and destruction of the vrrtrbral rndplates and apophyseal joints of the ttlirtl, fourth.
in
vertebral
[ 1-51. This and may be fatal [S]. Described herein is a patient with severe rheumatoid disease in whom progressive cervical involvement over a period of several years led to quadriparesis. The true nature of the patient’s symptoms was not realized at first. It was only after a review of serial roentgenograins, obtained over a six year interval, that the significance of the patient’s clinical manifestations hecame apparent. Furthermore, the effects of thca vrrtcbral lesions were clearly documented preoperativrly by vertebral arteriography and rnyclography. subluxation
is
complication
commonly
is
often
present
insidious
CASE
REPORT
iifty-four year old white woman (H.K. 524652) who had progressively severe rheumatoid arthritis for twenty-seven years complained of falling down on two separate occasions during the week prior to her hospitalization in November 1966. These episodes were unassociated with vertigo, visual deficit or unconsciousness and she attributed her difficulty to a “buckling of the kneeq.” During the two weeks prior to hospitalA
4 A synonym tinguished
from
for rheumatoid ankylosing
* From the Department March vo,..
arthritis,
to be
dis-
spondylitis,
of Radiology,
The University
of Michigan,
16, 1967. 44,
MARCH
1968
441
.\nn :\rbor, Michigan.
Malkuscript
rc-wived
442
Cervical
Spondylitis
in Rheumatoid
Disease-A4artel
2B
2A
FIG. 1. Cervical spine, 1960. The dislocation of the atlas is evident in the flexion position only. The atlanto-odontoid interval measures 9 mm. in flexion and the anteroposterior diameter of the spinal canal is 15 mm. at the level of the first cervical vertebra. The discs between the second and third and the sixth and seventh cervical vertebrae are reduced in height and there are small anterior osteophytes. FIG. 2. Cervical spine, 1963. A, slight flexion. B, midline laminagram. The atlanto-odontoid interval now measures 13 mm. and the diameter of the spinal canal at the first cervical vertebra is 11 mm. There is extensive destruction of the vertebral end-plates at the fourth and seventh cervical vertebrae. Note the slight malalignment at these levels and the erosions of the apophyseal joints at the third and fourth cervical vertebrae. FIG. 3. Cervical spine, 1966. Flexion. The intervertebral discs between the third and fourth and sixth and seventh cervical vertebrae have been destroyed and there is considerable bone loss particularly between the third and fourth cervical vertebrae with resultant vertical shortening of the spinal canal. The atlas is not fused and the spinal canal at the first cervical vertebra still measures 11 mm. Note the resorption of the discs between the third and fourth, fourth and fifth and sixth and seventh cervical vertebrae, with apposition and apparent partial fusion of the vertebral bodies.
sixth and seventh cervical vertebrae. The spinal canal at the level of the first cervical vertebra now measured 11 mm. (Fig. 2). Physical examination both in 1960 and in 1963 showed no definite evidence of a neurologic deficit related to these spinal lesions. In November 1966 physical examination disclosed rather severe muscular weakness and diminished deep pain sensation in the upper extremities compared to the lower ones. There was diminished sensa-
tion to pinprick in both hands, particularly on the left side. Vibration and position discrimination were intact. The deep tendon reflexes were hyperactive and there were bilateral extensor plantar reflexes and positive Hoffman signs. The cranial nerves were intact. Roentgenologic examination of the cervical spine showed no significant increase in the degree of atlas displacement but there was bone loss in the third, fourth and sixth cervical vertebral bodies with miniAMERICAN
JOURNAL
OF
MEDICtNE
C:ervical
Spondylitis
in Rheumatoid
Ikeasc-
dlmrie/
part it rs intact and in the midline.
mal ne\v lrone formation and partial anterior fusion at tlwsc. Arcs (Fig. 3,X). ‘The left atlantoaxial joint was srverel~ eroded and the left lateral masses of the first and second cervical wrtebrae were compressed (compare Fiq. 4B ancl 4.4). In view of these changes and the patient’s symptoms, left vertebral arteriography was performed. l’herc \serc tlvo kinks in the vertebral artcr!-. presumably dare to the foreshortening of the spine I I:&. SA), In addition, there were tvvo areas of stenosis al and jrist I~elow the region of the foramen transvt’rsarium of the second cervical vertebra which were f)robably secondary to the destructive bone and joint lesions (~Fig. SB). Lumbar puncture showed the spinal tluid pressure and protein concentrations to be normal; the Queckenstedt test \vas negative. Myrlography disclosed an ertraclural defect, thought to be dr~c to a herniated intervertebral disc at the junction of the fourth and fifth lumbar vertebrae. There was no obstruction to the passage of pantopaqtw through the cervical subarachnoid space. The transverse diameters of the spinal cord and spinal subarachnoid space at the level of the fifth cervical vertcl,ra were 19 and 31 mm., respectively,* and there was no evidence of syringomyelia or spinal cord atrophy. There \vas a shallow defect anteriorly at the junction of the fifth and sixth cervical vertebrae of uncertain significance, possibly due to a minimally cxtrucled disc or osteophyte, and posteriorly there
were multiple
irregularities
thought
to be due to the
dura and liqamenta fiava (Fig. 6). This exaggerated effect was thought to be due to the redundancy of these tissues secondary to the foreshortening of the spinal canal. The subarachnoid space appeared to * I.ncorrccted
for magnification.
taper at tlie first and ~cconcl cervical \~:~~t~~Or~ic ,jnct measured 10 mm. anteroposteriorly. Sorue 01’ 11~ pantopaque passed into the posterior fossa. Following the application of cervical traction for several tlaysl muscular strength appeared to improve in tile upper extremities. Cervical spirit: films obtained in the operating room while tire l)atient \vas in traction showed considerable diminrrtion in tire clegrec of atlas displacement. The patient nnc~erwrnt laminectomy ancl fusion of thr cervical \pine on November 2.3, 1966. ,Jt the time of surgery in \vas noted that the ligamenta Hava over tire 1011cr cervical spine wcrc slightly thickened and inspecrion of the spinal cord at the level of the fifth ant1 iivtir cervical \,ertebrae suggested to the surgeons that there was “slight spinal cord atrophy ancl pallor‘. ‘l’hcre \vas no gross extrusion of the inter\wtrbral tlisc at t11e junction of the fifth and sixth cervical vertebrae. The patient’s symptoms diminished in the immediate postoperative period. COMMENTS
Nontraurnatic atlas dislocation trlay bc fatal in rheunlatoid arthritis affecting the cervical spine and it is therefore particularly important to recognize the possibility of this complication whenever these patients present unttsual rnusculoskeletal synlptorns. Keurologic evaluation of such syrnptorns is particularly difficult in these patients 1.51. They have crippling joint deforrnities, often with secondary nruscular atrophy, [ 71 may mask and peripheral polyneuropathy symptoms of a central lesion. Furthtrrnore, this
444
Cervical
5A
Spondylitis
in Rheumatoid
Disease-MarteI
5B
6
FIG. 5. Left vertebral arteriogram. A, lateral projection. B, anteroposterior view. There are two kinks in the vertebral artery, presumably due to foreshortening of the spinal canal. In addition, there are two areas of stenosis (arrows), seen best in the anteroposterior view, at and just below the region of the foramen transversarium of the second cervical vertebra. Note the left lateral mass of the first cervical vertebra (retouched) (large arrow). FIG. 6. Cervical myelogram. Lateral projection, patient supine. There is no evidence of syringomyelia or spinal cord atrophy. The transverse diameters of the spinal cord and spinal subarachnoid space at the fifth cervical vertebra are 19 mm. and 31 mm., respectively, which is within normal limits [27]. The anteroposterior diameter of the subarachnoid space at the first cervical vertebra (measured from the ventral aspect of the pantopaque column to the posterior bony margin of the canal) is 10 mm. There is a suggestion of tapering within the pantopaque column (arrow) at the first cervical vertebra. Note the posterior irregularities particularly at the fifth cervical vertebra, probably due to redundant dura and ligamenta flava. A shallow anterior defect at the fifth and sixth cervical vertebrae is of doubtful significance in view of the negative findings at surgery with regard to this site.
disease frequently dictates a sedentary existence which may cause certain neurologic deficits to go undetected. The patient herein described in retrospect probably had significant neurologic symptoms for at least three months prior to her hospitalization. Awareness of what the previous roentgenograms had shown in this case prompted the request for further studies, including vertebral arteriography and myelography, which in turn led to a better evaluation of the patient. Cervical myelopathy and radiculoneuropathy may result from chronic spinal cord or nerve root compression, secondary to vertebral subluxation, or to ischemia [2,8] as a result of narrowing of the vertebral, the anterior or posterior spinal and radicular arteries. Arterial compression may be secondary to vertebral subluxation
or to rheumatoid destruction of the apophyseal joints in view of their proximity to the vertebral arteries. Intervertebral disc extrusion may also be a significant factor. This patient appeared to have such a lesion in the lumbar spine. Cervical nerve root compression by an extruded disc was recently observed in a young adult who had had rheumatoid arthritis with cervical involvement as a child [9]. Any of these three factors may be operative and thorough roentgenologic evaluation in certain cases, including myelography and vertebral angiography, is therefore advisable, particularly prior to surgical correction. A number of these patients with severe vertebral subluxation have had a surprising lack of commensurate neurologic manifestations [5]. This may be related to the slow development of AMERICAN
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C:er\4cal
Spondylitis
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IIIC’W I&~ns. allowing an adaptation of thr xpmal cord. or to the frequently associated bone destrllction, lea\,ing nlore rooln for the cord itself I_‘]. On the other hand, this discrepancy may rpfl(.ct tile role of spinal cord ischcmia and the fact that attcnrralion of the arterial supply is not nclccxssarily proportional to the degree of \.ertrhral destruction and sltbluxation. It is of interest lhat in this patient the reduced anteroposterior diameter of the spinal canal at the first cervical vertebra did not change appreciably between 1963 and 1966 but neurologic manifestations first developed in 1966. Perhaps the narrowing of the vertebral artery occurred during this interval in view of the progressive destruction of the adjacent left atlanto-axial joint. Kecently, Turnbull et al. [ 701 questioned whether \,ertebral artery narrowing could result in ischelnia of the spinal cord and emphasized the numerous collateral pathways. Conceivahl>-, in this case the vertical foreshortening of the spinal canal nlay have aggravated an alread) inarginal situation with regard to compressioll of the spinal cord or its arteries. Possibly, such foreshortening may have caused traction 011 the nerve roots or radicular arteries. On the other hand, delayed myelopathy in traumatic and congenital abnormalities of the craniovertebral region has been recognized [II, 721 and? whatever its mechanism, perhaps it occurs in this situation as well. There appears to be a predilection for the cervical spine in rheumatoid disease, the basis for which is not clearly understood. The normally greater mobility of this segment, compared to the rest of thr spine, is probably an important factor. There is some evidence that usage and mechanical stress may enhance the destructive process in the peripheral joints [ 7.3,74]. The cervical inter\rertebral disc spaces are commonly found to be reduced in height at multiple levels [I 41. Osteophytes tend to be absent or small at these sites but this may reflect the inability of the rheumatoid patient to form bone rather than anything specific about the intervertebral disc lesions [75]. One may speculate as to the nature of these lesions inasmuch as cartilaginous joints are not commonly affected in rhcxumatoid disease, although they are frequently involved in ankylosing spondylitis. Perhaps in\~olvement of the diarthrodial apophyseal joints further increases the mobility of the indilidrtal crrlical vertebrae and premature degeneration of the cartilage plates supervenes. If v0
1.
44,
MARCH
1968
l>iseaye
- AZ;lor~~d
-1-i.?i
this is trur. the. \.prtrbral end-plate d(>htr-rlction, such as was present in this patient, Illa> in part be drle to intravertehral disc herniatiolls and represent largely a degencrativr rather I hair an inflarnlnatory process. Parentheticall), tilt, pwscncc of small alnounts of pannus does not nwc+ sarily preclrlde this interprrtation. 111drrcl. rstrusions of disc material into the \-rrt&ral bodies has been observed [!)I and narrowing 01 the intcrvrrtebral disc spaces of the 1ulnba1 spine may be significantly Inore cc~nImon in patients with rheumatoid dlseasc [ /li /r 1. IlO\\-ever, an additional possibility to cxplaill the involvement of these cartilaginous joints slho\lld be taken into account. The t\nco\.ertrbral (Luschka) joints are syno\?al in character and apparently are acquired, inasmuch as the! arc’ not observed in children. Should these joints become affected, their contiguity wit11 the ‘iI,tervertebral discs might lead to destruction of the latter. It is noteworthy in this rcqard that vertebral end-plate erosion of the type illustrated (Fig. 2) is rare in juvenile rhrumatoid arthritis I/9]. Earlv fusion of the cervical apophyseal joints is characteristic of the discasr in children, however, and this lnay confer solne protection to the anterior cartilaginolls joints. Indeed, following such fusion of t lx apophyseal joints, the intervertebral discs characteristicall) become atrophic. A similar sequence illa)’ be observed at isolated cervical levels in adult>, with this disease. It appears that rheumatoid destrllction of the apophyseal joints in adults is often followed by “erosion” of the \-ertcf)ral rndplates at that level, whereas, apophysral ank>-losis is usually associated with atroph!. of tile adjacent intervertebral disc with sparing l)f the vertebral end-plates [ 181. It does not seem unreasonable to speculate that in some people a “neuropathic effect” Ina!’ be operative in addition to the rherrlnatoid process. This could be due to peripheral nruropatlry or to a lesion of the spinal cord [Xl. particularly in view of the destructive cervical spondylitis which may be present. The surgeon’s obser\.ation that the spinal cord appeared slightl) atrophic is of interest but of uncertain siqnificance. The ratio of the transverse diameters of the spinal cord and spinal subarachnoid space as Ineasured on the Inyelogram was within nortllal limits 1271. It is conceivable, howe\,er, that a rnininlal atrophic change may not be dctrctablc 1)) myelography. Although it has not bcrn possible thus far to document clinical cvid(,ncc w sup-
446
Cervical
Spondylitis
port this hypothesis of a neurogenic
in Rheumatoid
basis for
bone resorption in this disease [5], attention should be directed to postmortem examinations of the spinal cord in these subjects.
Acknowledgment: I appreciate the support of Ivan F. Duff, M.D., in making this patient available for roentgenologic evaluation. The surgery was performed by Richard C. Schneider, M.D. and Robert W. Bailey, M.D. of the University of Michigan Medical Center. REFERENCES 1. MARTEL, W.
2.
3.
4.
5.
6.
7.
8.
and PAGE, .I. W. Cervical vertebral erosions and subluxations in rheumatoid arthritis and ankylosing spondylitis. Arthritis & Rheumat., 3: 546-556, December 1960. MARTEL, W. The occipito-atlanto-axial joints in rheumatoid arthritis and ankylosing spondylitis. Am J. Roentgenol., 86: 223, 1961. MARTEL, W. Occipito-atlanto-axial joints in rheumatoid arthritis. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Congress Series No. 61, p. 189. Amsterdam, 1963. Excerpta Medica Foundation. SHARP, J. and PURSER, D. W. Spontaneous atlantoaxial dislocation in ankylosing spondylitis and rheumatoid arthritis. Ann. Rheumat. Dis., 20: 47, 1961. MARTEL, W., DUFF, I. F., PRESTON, R. E. and HAYES, J. T. The cervical spine in rheumatoid arthritis; correlation of radiographic and clinical manifestations. (Abstract.) Arthritis & Rheumat., 7: 326 1964. MARTEL, W. and ABELL, M. R. Fatal atlanto-axial luxation in rheumatoid arthritis. Arthritis & Rheumat. 6: 224, 1963. FREUND,H. A., STEINER,G., LEICHTENTRITTB. and PRICE, A. E. Peripheral neuropathy in chronic atrophic arthritis. Am. J. Path., 18: 865, 1942. SCHNEIDER,R. C. and CROSBY, E. C. Vascular insufficiency of brain stem and spinal cord in spinal trauma. Neurology, 9: 643, 1959.
Disease-Martel
9. MARTEL, W. Personal observations. 10. TURNBULL, I. M., BRIEG, A. and HASSLER, 0. Blood supply of the cervical spinal cord in man. A microangiographic cadaver study. J. Neurosurg., 24: 951, 1966. 11. BACHS, A., BARRAQUER-BORDAS,L., BARRAQUERFERRE, L., CANADELL, J. M. and MODELELL, A. Delayed myelopathy following atlanto-axial dislocation by separated odontoid process. Brain, 78: 537, 1955. 12. LIST, C. F. Neurologic syndromes accompanying developmental anomalies of occipital bone, atlas and axis. Arch. Neural., 45: 577, 1941. 13. MARTEL, W., HAYES, J. T. and DUFF, I. F. The pattern of bone erosion in the hand and wrist in rheumatoid arthritis. Radiology, 84: 204, 1965. 14. CASTILLO, B. A. and SCOTT, R. A. Physical activity, cystic erosions and osteoporosis in rheumatoid arthritis. Ann. Rheumat. Dis., 24: 522, 1965. 15. MARTEL, TY. Discussion: Lumbar spine. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Contress Series No. 61, p. 260. Amsterdam, 1963. Excerpta Medica Foundation. 16. LAWRENCE, J. S. and SHARP, J. Lumbar spine. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Congress Series No. 61, p. 239. Amsterdam, 1963. Excerpta Medica Foundation. 17. DE SEZE, S., DEBEYRE, N. and DJIAN, A. Radiological study of the dorso-lumbar spine in rheumatoid arthritis. Radiological aspects of rheumatoid arthritis. In: Proceedings of an International Symposium. International Congress Series No. 61, p. 251. Amsterdam, 1963. Excerpta Medica Foundation. 18. MARTEL, W. Further observations on the spine in rheumatoid disease. To be published. 19. MARTEL, W., HOLT J. F. and CASSIDY, J. T. Roentgenologic manifestations of juvenile rheumatoid arthritis. Am. J. Roentgenol., 88: 400, 1962. 20. MARTEL, W., BRODY, G. D. and CASSIDY, J. T. A lesion of the spinal cord in a case of juvenile rheumatoid arthritis. To be published. 21. KHILNANI, M. T. and WOLF, B. S. Transverse diameter of cervical spinal cord on pantopaque myelography. J. Neurosurg., 20: 660, 1963.
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