Association

of Diffuse

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Calcification

and Ossification

DONALD

Diffuse

ossifying

idiopathic

diathesis

Idiopathic

RESNICK,1

skeletal

JOSE

hyperostosis

in middle-aged

JR.,1

CHARLES

Is a common

and elderly

patients

malities

in this

hyperostosis (DISH) by bone proliferation The most characteristic

condition

are

ligamentous

Case

results.

work

June 30, 1978; was supported

D. Resnick I

Department

of Radiology,

spine,

including

0 1978 American

began

and

C. VINT3

as a tingling

progressed

sensation

to

involve

on the

the

ankle,

physical

and

examination

pronounced muscle

outlined

herpes

zos-

restriction of motion of the and decreased pain and

atrophy

calcification

and

ossification

along

the

anterior

aspect

of the entire vertebral column (fig. iA), bony excrescences about the pelvis, and panaacetabular osteophytes. Prominent calcification and ossification of the posterior longitudinal liga-

ment was noted

calcification

in the cervical

naphy

demonstrated

canal

was not examined.

was that involvement

Lumbar

abnormalities;

The final

that they were accentuated Case

spine (fig. iB).

no significant

neurobogic evaluation related to nerve root

myebog-

the

impression

cervical

after

extensive

the symptoms were probably in the lumbosacral spine, and

by the presence

of herpes

zoster.

2

A 57-year-old which

white

included

man had a complicated

pulmonary

coccidioidomycosis,

resection

adult-onset

medical

for a granuboma

diabetes

history related

mellitus,

type

to

IV hy-

perlipoproteinemia, hypertension, and a hydrocele of the left testicle. His current evaluation at the Hospital of Scripps Clinic for increasing pain and stiffness in the neck and lower back for several years revealed marked restriction of motion of the cervical

of

spine

motion

lordosis

with

paraspinous

in the

lumbar

muscle

spine

was also evident.

with

spasm.

Some

flattening

Laboratory

restriction

of the

examination

lumbar

was unre-

markable.

Radiographic

evaluation

outlined

findings

of DISH, including

new bone formation along the antenolatenal aspect vertebral column, paraacetabular bony excrescences, joint

osteophytosis,

including

and

ment

2A

(figs.

patellar

of the

ossification and

computed

tomography

appropriate

physical

2B)

Radiography

cervical

spine

of the

posterior

longitudinal

further

documented

on

was referred

for

which

(fig.

hyperostosis.

of the entire sacroiliac

was

outlined

2C). The patient

exuberant

liga-

therapy.

3

A 64-year-old

Reports

and

tomography

calcification

Case

white

man was seen at the Hospital

of Scripps

of low back and lower extremity pain for about 13 years which had required lower lumbar laminectomy for , ‘three slipped discs.” Additional musculoskeletal complaints were numbness and tingling of both thighs, pain and stiffness because

no. 7406.

of the Picker Foundation. University

of California

School

of Medicine,

Veterans

California 92161 . Address reprint requests to D. Resnick. a Department of Internal Medicine, Hospital of Scripps Clinic, San Diego, 3 Department of Radiology, Hospital of Scripps Clinic, San Diego, California Am J Roentgenol

VINTON

in the left lower extremity. Laboratory evaluation was unremarkable , although nonspecific electromyographic altenations were apparent in the left leg. Radiographic examination revealed the findings of DISH,

is a comin axial abnor-

accepted after revision August 28, 1978. in part by Veterans Administration grant

foot

Ligament

sensation

man was evaluated at the Hospital of of left lower extremity pain and weak-

is a Picker Scholar

left

The present

cervical

1

Received

The pain

the

ten on the left buttock,

Clinic

A 71-year-old white Scripps Clinic because

This

of

AND

and

knee, hip, and left buttock. An extensive neunologic and onthopedic evaluation 4 years prior to the current evaluation included myebography and electromyography with inconclusive

and ossification along the anterolateral aspect of the vertebral bodies with localized osteophytosis. Changes in extraspinal locations are also frequent, including ligament and tendon calcification and ossification, panaarticulan osteophytes, and bony excrescences at sites of ligament and tendon attachment to bone. Alterations along the posterior aspect of the vertebrae are rarely mentioned in this condition. Ossification of the posterior longitudinal ligament of the cervical spine has been reported in a large number of Japanese patients and in a few non-Japanese individuals [4-13]. This ossification, which has a characteristic appearance on radiognaphs, may be associated with cervical myelopathy [4, 5, 7, 8, 10, 12] on produce no symptoms and signs [5, 1 0, 1 1 , 13-1S]. Recently we investigated four patients who demonstnated extensive posterior longitudinal ligament calcification in the cervical spine on initial evaluation. Subsequently, additional nadiognaphs revealed findings of DISH. We present these four patients in detail and describe the incidence of radiographic abnormalities along the posterior aspect of cervical vertebral bodies and intervertebral discs in a large number of patients with DISH. Case

A. ROBINSON,2

dorsum

(DISH)

Longitudinal

ness for 15 years.

char-

acterized by bone proliferation along the anterior aspect of the spine and at extraspinal sites of ligament and tendon attachment to bone. Four patients with DISH revealed extensive calcification and ossification of the posterior longitudinal ligament In the cervical spine. Review of cervical spine radiographs in 74 additIonal patIents with DISH demonstrated bony hyperostosis of the posterior aspect of the vertebrae In 41%, posterior spinal osteophytosis in 34%, and posterior longitudlnal ligament calcification and ossification In 50%. These Ilgamentous findings, which have previously been described almost exclusively In Japanese people, appear to be an additional skeletal manifestation of DISH.

Diffuse idiopathic skeletal mon disorder characterized and extraaxial sites [1-3].

Hyperostosis

of the Posterior

GUERRA,

(DISH)

Skeletal

131 :1049-1053, December Roentgen Ray Society

1978

California

1049

Administration

Hospital,

3350

La Jolla

Village

Drive,

5an

Diego.

92037.

92037. 0361

-803X/78/i

200-i

049

$00.00

1050

RESNICK

ET

AL.

in the

cervical

achilles

tendon

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included

spine,

and

mild

associated

significant

restriction

of

spinous

muscle

spasm

of the

forward

flexion

in the

lumbar

and laboratory

analysis

Radiography nent anterior

spine.

motion,

and

normal

pana-

restriction

Neunologic

of iliolumban

Cervical

spine

and ossification

calcification

(fig.

spine

region,

were within

calcification

excrescences.

ment

cervical

cervical

of

examination

limits.

outlined the changes of DISH, including promispinal new bone formation (fig. 3A), paraacetabu-

Ian osteophytes, bony

discomfort in the region of the “ heel spurs.” Physical findings

with

3B).

The patient

ligaments,

radiography

of the posterior was referred

and pelvic

demonstrated

longitudinal

for physical

liga-

therapy.

Case 4 A-57-yean-old

white

ministration

the

Hospital

neck

for

numbness

several

along

sation 1. A, Flowing calcification and ossification along anteof mid and lower thoracic spine. B, Note calcification and of posterior longitudinal ligament in cervical spine (arrow).

1.-Case

nor aspect ossification

of the

years.

right

Radiography of

arm

along

Cervical Review

of

met

the

of motor

aspect

vertebral

abnormalities

also

Ad-

of motion

noted

of the right

in

pain

arm.

and

Previous

of the

antenolatenal

ulnar

of DISH

aspect

Changes

spine

of

nerve.

with

the

radiographs

in

for

abnormalities

along

the

patients DISH

[2]

posterior

in 55 patients

(74%).

These

into

types

which

together: (fig. 5). Bony

posterior

of the (fig. 4). was lost

74

criteria

bodies

dep-

vertebral

in DISH

published

be divided

were found hyperostosis the

distribution

nadiculopathy.

calcification and ossification ligament in the cervical spine was recommended, the patient

could

along

Veterans

range

the alterations

the

previously

definite

rosis

patient

Spine

documented

frequently 1 . Bony

The

aspect

along

cervical

our

of the

at the

decreased

demonstrated

bone

column, and extensive posterior longitudinal Although myelography to follow-up.

who

evaluated

and

included M#{233}ni#{232}ne’s disease. Laboratory analysis but electromyognaphy outlined absent sen-

There was no evidence osition

was

pain

the lateral

medical history was unrewarding, Fig.

man for

aspect

three eburnation

of the

or scle-

vertebral

bodies

was apparent in 30 patients (41%). This abnormality was most apparent in the upper cervical vertebrae and produced “highlighting” or “whitening” of the posterior cortex.

2. Osteophytosis. posterior

aspect

Osteophytes of the

patients (34%). They lower cervical region cences,

typically

canal. 3. Posterior ossification. were apparent

vertebral

were

were most frequent where they produced

small,

which

longitudinal Ligamentous in 37

protruding bodies

protruded

ligament

calcification patients (50%).

from noted

the in 25

in the mid and bony excresinto

the

calcification

spinal

and

and ossification These deposits,

particularly frequent in the upper cervical spine, were of variable size, linear in distribution, bumpy in contour, and typically were separated from the subjacent vertebral body by a radiolucency of variable thickness. These three types of radiographic abnormalities were Fig. 2.-Case 2. A, Lateral radiograph ofcervical spine demonstrating extensive calcification and ossification of posterior longitudinal ligament. Observe nadiolucency between radiodense ligament and posterior surface of second cervical vertebral body. B, Tomogram demonstrating calcified and ossified posterior longitudinal ligament. C, CT scan at level of one cervical vertebral body outlining radiodense ligament separated from posterior aspect of vertebral body.

commonly, but not invariably, associated with alterations along the anterior aspect of the cervical spine which included osteophytes and flowing ossification anterior to the vertebral bodies and intervertebral discs. Although

thoracolumbar

changes

were

invariably

present

allowing

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DISH/CALCIFICATION

AND

OSSIFICATION

OF

POSTERIOR

1051

LIGAMENT

the diagnosis of DISH, there was no definite correlation between the extent of abnormality along the posterior aspect of the cervical vertebrae and that in the thoracolumbar region. Discussion

Although

DISH

calcification

and

and

posterior

ossification

longitudinal

have

received

ligament considerable

attention in the medical literature, their possible association has rarely been mentioned. Arlet et al. [16] analyzed 40 patients with cervical myelopathy and noted the frequency of vertebral hypenostosis in these patients. Of the 40 patients, 17 (43%) had both DISH and acquired stenosis of the cervical canal related to bony prolifenation

along

the

posterior

aspect

of the

vertebral

bodies.

The pattern of proliferation included findings similar to those noted in our investigation, such as hyperostosis, osteophytosis, and ligament calcification and ossification. Ono et al. [17] investigated 166 patients with ossification of the posterior longitudinal ligament. Symptoms in these patients, including motor and sensory disturbances in the lower extremity, were particularly prominent when the ossified posterior longitudinal ligament occupied 60% of the sagittal diameter of the cervical spine. Of 160 patients in that report, 71 (44%) demonstrated concomitant hyperostosis on the anterior aspect of the vertebral column. Postmortem examination of two patients with both posterior longitudinal ligament calcification and DISH revealed that the ossification of the posterior longitudinal ligament was particularly prominent in its superficial layer, whereas the unossified deep layer was thickened, creating a radiolucency between the

ossified

ligament

the craniocervical lined proliferation of the

matrix

These which though

findings occurs anterior

cification

within

and

Although

[4-12]. tions,

underlying

vertebral

the

posterior

ossification

and

with

posterior

Parasthesias

may

vary

numbness

from

or tingling

be encountered symptoms

stiffness,

,

pathology

definite

can

longitudinal

may be asymptomatic [13], signs have been associated

including

and

ligament.

coexist

in their

be

ligament

a variety with this intermittent

of sympdisorder sensa-

of several

one or both upper extremities, to extensive anesthesia of the trunk and lower extremities disturbances, such as weakness, incoordination,

pain

At out-

hyperplasia

longitudinal

frequently

differences

patients

stability, may ties. Additional

body.

evaluation

did not document the sequence of events in this condition, but suggested that aland posterior longitudinal ligament cal-

and remarkable noted. ossification toms and

and

junction , histologic of cartilagelike cells

digits

of

and severe [6]. Motor and in-

in upper and lower extremmay include head and neck

urinary

and

rectal

incontinence

and

-

A and B, Lateral and frontal nadiographs of cervical spine demonstrating widespread calcification and ossification of postenor longitudinal ligament (arrows). C and D, Lateral and frontal tomoFig.

4.-Case

4.

grams better delineating

these

findings.

Fig.

3.-Case

Calcification of second

3.

A, Typical

and ossification and

third

cervical

flowing

ossification

of posterior vertebral

bodies

in thoracic

longitudinal (arrow).

ligament

B, at level

spine.

1052

RESNICK

ET

AL.

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and

senosry

loss

in

case

1

numbness

,

the thigh in case 3, and upper sensory loss in case 4 may have longitudinal spine

of our the

ligament

may

be

patients, of

and

Human

patient with tomography ossification

within

It is apparent bral vical

with

revealed

but

the

extent

al.

[19]

previously

posterior

from

this will

review

that

we have an age-

population, examinations

bony hyperostosis and Posterior longitudinal

tion and ossification these latter changes

DISH

is considered an

incidence

a frequent that

may

and elderly patients [18], the posterior longitudinal regarded

as

findings

calcification ligament almost

and should

confined

of

number

of verte-

analyzed cersex-matched

minor ligament

12%

a

computed extent

review patients

disease reach

canal

ligament.

not and

were not apparent, are indeed associated

only

described

posterior

our brief in elderly

the one

calcifi-

spinal

a great

abnormalities. Although spine radiographs in

some with osteophytosis.

of

longitudinal significant

control spine

not

ligament

reveal

“normal” 20 cervical

with

in

myelopathy in whom the presence and

the

DISH

of

longitudinal

cervical documented

of

evaluation;

tomography

et

tingling

Tomography

adequate

posterior

ossification

impingement.

patients

for

computed

presence

cation

ossification.

necessary

and

extremity numbness and been reiated to posterior

of about yielded

degrees calcifica-

of

suggesting that with DISH. If

in this of

country

middle-aged

ossification no longer to

of be

Japanese

individuals. Fig. 5.-Hyperostosis ond,

third,

dysfunction,

and fourth

and

patients

may

loss

reveal

of posterior cervical

surface

vertebral

of libido.

On physical

muscle

toms

atrophy,

and

signs

are,

in general,

in other disorders of the Our previous investigations not emphasize abnormalities

the

cervical

tients

vertebrae,

with

ligament

DISH ossification,

small

posterior

tosis

[18].

these

and

tions recent

are frequent experience

suggests tion and

fasciculations,

additional

bodies integrity logic

we did

revealed

posterior

along

in with

Some

the the

pres-

DISH

some

and

hyperos-

evaluation that

such

of alteraour here

ligament calcificaspine may become

as deposition aspect

discs leading

pa-

demonstrated

disease. Furthermore, four patients reported

posterior

did of

longitudinal

closer

longitudinal in the cervical

of the

note

who

our with

disorder. is important, the

being

osteophytes

from

and intervertebral of the spinal cord, findings.

others

spine patients

that posterior ossification

bone

nonspecific,

and

cervical

hy-

incidence of and the symp-

spinal canal and cord. of patients with DISH of the posterior aspect

although

It is apparent

extensive in this This observation and

who

REFERENCES

examination,

perreflexia, and sensory loss. The reported these findings has varied considerably, ent

of sec-

bodies.

of

of calcium the

vertebral

may compromise to significant

neurologic

abnormalities

the neuroin

three of these four patients (cases 1 , 3, and 4) may indeed have resulted from such ossification; it is therefore imperative that the radiologist search diligently for these changes. Thus, lower extremity muscle atrophy

1 . Resnick D, Shaul SR, Robins JM: Diffuse idiopathic skeletal hyperostosis (DISH): Forestier’s disease with extraspinal manifestations. Radiology 1 15 : 51 3-524 , 1975 2. Resnick D, Niwayama C: Radiographic and pathologic features of spinal involvement in diffuse idiopathic skeletal hyperostosis (DISH). Radiology 119:559-568, 1976 3. Forestier J, Rotes-Querol J: Senile ankylosing hyperostosis of the spine. Ann Rheum Dis 9 :321-330, 1950 4. Nakanishi T, Mannen T, Toyokura Y. Sakaguchi R, Tsuyama N: Symptomatic ossification of the posterior longitudinal ligament of the cervical spine. Neurology 24:1139-1143, 1974 5. Bakay L, Cares HL, Smith RJ: Ossification in the region of the posterior longitudinal ligament as a cause of cervical myelopathy. J Neurol Neurosurg Psychiatr 33 : 263-268, 1970 6. Takahashi M, Kawanami H, Tomonaga M, Kitamura K: Ossification of the posterior longitudinal ligament. A roentgenologic and clinical investigation. Acta Radio! [Diagn] (Stockh) 13:25-36, 1972 7. Soo YS, Sachdev AS: Calcification in the posterior longitudinal ligament as a cause of cervical myelopathy. Med J Aust 1 :743-744, 1971 8. Op den Orth JO: Die Verkalkung bzw. Verknocherung des Ligamentum Longitudinale Postenius den Halswirbelsaule. Fortschr Geb Roentgenstr Nuk!earmed 1 22 : 442-445 , 197 9, Lagemann VK: Hintere Langsbandverkalkungen kombiniert mit virbelkorperexkavationen. Fortschr Gob Roentgenstr Nuklearmed 116:834-835, 1972 10. Minagi H, Gronner AT: Calcification of the posterior longitudinal ligament: a cause of cervical myelopathy. Am J Roentgeno! 105:365-369, 1969

DISH/CALCIFICATION ii

.

Hiramatsu

Y,

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longitudinal 12.

Nobechi

ligament

T:

Calcification

of

of the spine among

ogy 100:307-312, 1971 Nagashima C: Cervical the posterior longitudinal 660, 1972

posterior Radiol-

due to ossification of J Neurosurg 37:653-

14.

cation of the posterior longitudinal ligament of the cervical spine. J Neurol Sci 19 :375-381 , i973 Yanagi T: Ossification of the posterior longitudinal liga-

A clinical

T, Toyokuna

and

i6.

17.

OF

radiological

Y: Asymptomatic

analysis

ossifi-

of

forty-six

cases. Brain Nerve 22 : 909-921 , 1970 Palacios E, Brackett CE, Leany DJ: Ossification of the posterior longitudinal ligament associated with a herniated intervertebral disc. Radiology 1 00 : 31 3-31 4 , 1971

18.

19.

POSTERIOR

LIGAMENT

1053

Anlet PJ, Pujol M, Buc A, Genaud G, Gaynand M, Latorzeff S: Role de l’hyperostose vertebrale dans es myelopathies cervicales. Rev Rhum Mal Osteoartic 43 : 167-175, 1976 Ono K, Ota H, Tada K, Hamada H, Takaoka K: Ossified posterior longitudinal ligament. A clinicopathologic study. Spine

Nakanishi

15.

Mannen

myelopathy ligament.

the

Japanese.

OSSIFICATION

13.

ment.

T,

AND

2:126-138,

1977

AF, Wiesner KB, Niwayama G, Utsingen PD, Shaul SA: Diffuse idiopathic skeletal hyperostosis (DISH). Ankylosing hyperostosis of Fonestien and RotesQuerol. Semin Arthritis Rheum 7 : i53-i87, 1978 Hyman RA, Merten CW, Liebeskind AL, Naidich JB, Stein HL: Computed tomography in ossification of the posterior longitudinal spinal ligament. Neuroradiology 13 : 227-228, Aesnick

1977

D, Shapiro

Association of diffuse idiopathic skeletal hyperostosis (DISH) and calcification and ossification of the posterior longitudinal ligament.

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