ATLANTO-AXIAL TUBERCULOSIS IN ADULTS

ROBERT LIFESO

From King Faisal Specialist Hospital and Research Centre, Riyadh

Twelve adult patients with confirmed tuberculosis of the atlanto-axial spine are presented and a
classification proposed. Stage I has minimal ligamentous or bone destruction and no displacement of Cl on
C2; the suggested freatment is transoral biopsy and decompression followed by an orthosis. Stage II has
ligamentous disruption and minimal bone destruction but anterior displacement of Cl on C2; treatment
involves transoral biopsy and decompression, reduction by halo traction, then a posterior C1-2 fusion.
Stage III has marked ligamentous and bone destruction with displacement ofCl forward on C2; the suggested
treatment is transoral biopsy and decompression, reduction by halo fraction, then fusion from the occiput to
C2 or C3.
One patient died before treatment started; all the others have gone on to solid union with resolution of
any neurological deficit. There has been no evidence of reactivation ofdisease over an average follow-up of 36
months.

At the beginning of this century tuberculosis was the This present report is a personal experience of
leading cause of death in western society (Leff, Lester confirmed tuberculosis of the atlanto-axial region in 12
and Addington 1979). Despite a dramatic decrease in its adults.
incidence, tuberculosis still causes death in the United
States, and in much ofthe world (Mitchell 1967). In 1977
MATERIALS AND METHODS
30 000 cases of tuberculosis were documented in the
United States alone, with a 10% fatality rate (Leff et al. Between June 1978 and June 1984, 250 patients with
1979). From 1971 to 1977 the incidence per 100000 tuberculous spondylitis were treated by the author at the
population in the United States felt only to 13.9 from 15.8 King Faisal Specialist Hospital and Research Centre in
(Center for Disease Control 1979). Riyadh, Saudi Arabia. Twelve patients with primary
Although the incidence of tuberculosis in the West involvement of the atlanto-axial region form the basis of
is stabilising, pockets of disease still remain among the this report. There were eight females and four males. The
socio-economically disadvantaged and among recent average age at presentation was 34.3 years (range 14 to 65
immigrants from geographical areas where the disease is years). All patients were skeletally mature and there was
endemic. The movement of large numbers of people no difference in average age between males and females.
from such areas will undoubtedly increase the incidence All patients were treated personally and followed up by
of tuberculosis in more developed countries. the author; the average follow-up was 36 months (range
When treated adequately tuberculosis is curable in 24 to 48 months).
almost all patients. Unfortunately many doctors now The average duration of symptoms prior to referral
consider the disease to have been eradicated and tend to was 10.8 months (range 2 to 24 months); three patients
ignore it in differential diagnosis. had been on antituberculous drugs, three in cervical
Tuberculosis of the atlanto-axial region is certainly traction for between three and nine weeks, one had
rare (Martin 1970); its reported incidence in China undergone incision of a tuberculous abscess of the elbow
(Wang 1981) was only 15 cases out of a total of 5393 and one patient had required nasogastric tube feeding
patients with tuberculosis spondylitis. Fang in Hong because of recurrent episodes of aspiration. No patient
Kong (Fang, Leong and Fang 1983) reported six patients had had spinal surgery.
with atlanto-axial tuberculosis, only two of whom were On presentation all patients underwent a standar-
over the age of 16 years. dised investigation including a complete blood count,
erythrocyte sedimentation rate (Westergren method),
SMAC 20 (sequential multiphasic analysis of chemistry),
R. Lifeso, MD, FRCS(C), FACS, Chief, Orthopaedic Surgery
Department ofSurgery, King Faisal Specialist Hospital, Riyadh 11211, Mantoux tuberculin skin testing, and sputum cultures for
Saudi Arabia. tuberculosis. Radiographs of the chest, of specific spinal
© 1987 British Editorial Society of Bone and Joint Surgery lesions, and of other suspected skeletal sites, were
030l-620X/87/2056 $2.00
performed. Special studies, including technetium-99m

VOL. 69-B, NO. 2, MARCH 1987 183

184 R. LIFESO

Fig. 1 Fig. 2 Fig. 3

Figure 1 - Stage I disease in a 58-year-old woman with a seven-month history ofcervical spine
only abnormality pain. The
on this radiograph is the
retropharyngeal abscess (arrow). There is no evidence of bone destruction or displacement. Figure 2 - Lateral tomogram 26 months later; no
treatment had been given in the interim and there is now total destruction ofthe odontoid and body ofCl (Stage III disease). Figure 3 - CT scan
showing lateral dislocation of Cl on C2 with a large retropharyngeal abscess (arrow).

Figure 4 - Stage
I disease, with a lesion in the
anterior portion
of C2 with no retropharyngeal
abscess. Figure 5 - Lateral radiograph taken at
the time of transoral biopsy shows direct
surgical approach to the entire body of C2.

Fig. 4 Fig. 5

bone scans (six patients), gallium scans (two patients), of whom were unable to walk but had sensory sparing;
myelogram (eight patients), and computed tomographic one of these four died of respiratory arrest within 48
scans (nine patients), were performed as clinically hours of admission (Figs 1 to 3). The fifth patient had
indicated. The diagnosis of tuberculosis was established tetraparesis but was able to walk with assistance.
by positive cultures for Mycobacterium tuberculosis in Fifteen other sites of tuberculous involvement were
nine patients, by a positive acid-fast smear in five identified in the 1 2 patients : other spinal sites in five,
patients, and by histology showing granulomatous other musculoskeletal sites in seven, and soft-tissue
disease in eight patients. Each patient had at least one involvement in three.
positive smear, culture, or histological examination. Classification. All cases were classified into one of three
Clinical presentation. All patients complained of severe stages depending on the radiological appearance
neck pain. Eight presented with severe fixed torticollis, (Table I). Ten patients had a retropharyngeal abscess as
four with twelfth nerve palsy, four had fixed trismus and well as specific spinal lesions (Figs 4 and 5). In Stage I
one each presented with hoarseness, difficulty in disease the ligaments were intact, there was minimal
swallowing, stridor, or lateral nystagmus. No patient had bone destruction and no evidence of anterior
a discharging sinus but one patient did have cervical displacement of Cl on C2. Proximal translocation of the
lymphadenopathy positive on biopsy for Mycobacterium dens occurred in one patient. In Stage II disease, there
tuberculosis. was ligamentous disruption with anterior displacement
Five patients presented with cord involvement, four of Cl on C2 but bone destruction was still minimal ; there

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 ATLANTO-AXIAL TUBERCULOSIS IN ADULTS 185

Table I. Classification, radiographic measurements (mean and range) and treatment of the 12 patients

Displacement Proximal fraaslocation

Number above McRae’s line (mm) Retropharyngeal
of ____________________ soft.tiasue shadow
Stage patients Rotatory Anterior Cl on C2 (mm) Pre-treatine’jt Post.treatment .anterior to C2 (mm) Treatment
I 4 2 subluxated

1.5 (1 to 3) 3.5 (0 to 14) 0.8 (0 to 3) 12 (5 to 22) Cervicothoracic 3

2 normal orthosis
Halo-vest

II 3 3 subluxated 6.0(3to9) 1.3(Oto4) 0 19.0 (16 to 22) Cl-2 fusion 2

Cl-3 fusion

III 5 3 lateral dislocations Impossible to 5.3(Oto9) 0 17.0 (2 to 26) Occ-C2 fusion

2 impossible to assess assess Occ-C3 fusion 2
Death
Halo-vest only

Normal ralues
Anterior displacement: < 3 mm
Retropharyngeal shadow : < 7 mm

was proximal translocation of the odontoid in one case. Gallie-type fusion of C 1-2 was performed using autogen-
In Stage III disease there was marked bone destruction ous bone and a 16-gauge wire passed under the arch of Cl
with complete obliteration of the anterior arch of Cl and, and around the spinous process of C2 ; this was followed
eventually, complete loss of the odontoid process ; these by halo-vest immobilisation for six weeks and then a
cases exhibited marked instability ofthe occipitocervical cervicothoracic orthosis for a further six weeks (Figs 6 to
junction. 8).
Treatment. Treatment was based on the radiological and In Stage III disease, halo traction was used to reduce
clinical findings at presentation. A transoral biopsy of the displacement; this was followed by a posterior fusion
the retropharyngeal soft-tissue abscess was performed from the occiput to C2 or C3 (Figs 9 to 1 1), performed
under general anaesthesia in all cases. Treatment then using parallel burr holes in the posterior occiput,
depended on the stage of the disease. bringing 16 or 1 8-gauge wire through these burr holes
In Stage I disease a cervicothoracic orthosis was and around the spines of C2 and/or C3 and using an
used until stability had been achieved. In one case a halo- autogenous bone graft. Halo-vest immobilisation was
vest was used because ofa 14 mm proximal translocation then used until there was evidence of stability.
of the dens. All patients were treated with standard therapeutic
In Stage II disease, a halo was applied and reduction doses of isoniazid, rifampicin, ethambutol and pyridox-
achieved with gentle traction. When normal realignment me. The doses were: isoniazid 5 to 10 mg/kg to a
had been attained, always within seven days, a posterior maximum of 300 mg per day ; rifampicin 10 to 20 mg/kg

Figure 6 - Lateral CT scan reconstruction in Stage II disease, showing a retropharyngeal soft-tissue abscess, anterior subluxation of the body of
C l(arrow), proximal translocation of the odontoid into the foramen magnum, and the spinal cord tightly compressed by anterior subluxation of
C I . Figure 7 - CT scan showing marked anterior subluxation of Cl forward on the odontoid. The spinal canal is grossly compromised and a large
soft-tissue abscess is seen. Figure 8 - After transoral decompression, halo traction and Gallie Cl-2 fusion, there is good realignment ofthe atlanto-
axial junction.

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 I 86 R. LIFESO

__.‘s
, ,. . ,.-.

Fig. 10 Fig. 11
Total destruction of the anterior arch of Cl, with the odontoid protruding into the foramen magnum above McRae’s line. Figure 10 - Lateral
radiograph taken with the patient in traction following transoral biopsy and seven days’ halo traction. The anterior arch of Cl is missing (arrow)
but excellent alignment has been achieved. Figure 1 1 - Thirty months after fusion from the occiput to C2. Alignment is maintained and the
posterior fusion looks solid. The odontoid tip is still above McRae’s line but there is no neurological impairment.

to a maximum of 600 mg per day ; ethambutol 15 mg/kg Rotatory subluxation was very difficult to measure
to a maximum of 1200 mg per day ; and pyridoxine 25 mg because of fixed torticollis, difficulty in achieving an
per day. All drugs were given in one daily dose. adequate anteroposterior radiograph, and occasionally
Ethambutol was routinely discontinued after three severe bone loss. In general there was increased rotatory
months, the other drugs after 12 months. All patients deformity with increasing bone loss.
completed a standard drug treatment protocol without Six patients underwent technetium-99m bone scans;
modification. in four there was a negative scan in the upper cervical
spine, one scan was positive in this region and one scan
was equivocal. Only two patients had gallium scans, both
RESULTS of which were negative in the upper cervical spine. All
Haematology. The haemoglobin averaged
12. 1 g/dl radiographic lesions were osteolytic and in no patient
(range 9 to 14 g/dl), the white blood cell count
averaged was there evidence of new bone formation or sequestra.
7.0 x l0/l (range 4.7 to 10 x t0/l) and the average All chest radiographs were negative for tuberculosis.
erythrocyte sedimentation rate (Westergren) was 47 mm Clinical results. Four patients presented with Stage I
in the first hour (range 6 to 72 mm). The Mantoux test disease : three were immobilised for three months in a
was positive in all patients. Biochemical analysis did not cervicothoracic orthosis while one was immobilised in a
allow differentiation of tuberculosis from other possible halo-vest ; all were clinically and radiographically stable
disease entities and there was no specific picture to within three months. Three patients presented with
identify tuberculous spondylitis. During the six years of Stage II disease : two underwent a Gatlie-type fusion of
this study, no other aetiology for this pattern of Cl-2 while one patient had a Cl-3 fusion because the
retropharyngeal abscess, bone destruction and spinous process of C2 was small ; after 12 weeks of
displacement was identified in any patient. immobilisation all fusions were solid. Five patients
Positive cultures for Mycobacterium tuberculosis presented with Stage III disease : one died within 48
were obtained in nine patients, five patients had positive hours because of instability and lateral translocation of
acid-fast
granulomatous
fled. Each
smears

patient
and eight had histology
disease. No resistant
had at least
compatible
strains
one positive
were identi-
culture
with

or
the atlas, one patient

vest only, and

,
three
with complete
bodies of Cl C2 and most of C3 was managed
patients
obliteration

underwent
of the
in a halo-
fusion ; all
histology for Mycobacterium tuberculosis. achieved solid bony fusion at between 12 and 16 weeks.
Radiology. A retropharyngeal abscess was seen in all but Patients were not kept in bed but mobilised as soon
two patients (Fig. 4) (Wholey, Bruwer and Baker 1958). as their clinical status allowed, and they were discharged
There was no correlation between the stage of disease on as soon as they were fit enough, all within 17 days of
presentation and the size of the retropharyngeal abscess. admission.
The tip of the dens protruded into the foramen All the patients were rapidly relieved of neurological
magnum in four patients (McRae 1953). There was no symptoms and pain relief was more dramatic after
correlation between neurological impairment and pro- surgical stabilisation. The average time to complete
trusion of the dens. relief from pain in those treated surgically was two

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 ATLANTO-AXIAL TUBERCULOSIS IN ADULTS 187

months, and in those treated medically 4.2 months. There were no complications from posterior fusion,
No patient has shown continuation or reactivation minimal morbidity and all patients rapidly recovered
of disease after completing 12 months’ chemotherapy. normal neurological status. It is a relatively simple
procedure, familiar to most practising orthopaedic
surgeons and leads to very rapid pain relief and a high
DISCUSSION
rate of fusion.
Tuberculosis of the upper cervical spine seems to begin Basing treatment on the radiological progression of
either in the retropharyngeal space with secondary disease and on the amount of soft-tissue and bone
involvement of bone or rarely in the bone itself. With destruction seems logical and is applicable to other non-
progression there is increasing ligamentous involvement tuberculous processes. No pathological process has yet
with minimal osteolytic erosions into the odontoid or into been demonstrated which produced a similar radiologi-
Cl .This allows anterior subluxation of Cl on C2, cal and clinical picture.
increasing rotatory subluxation, and proximal transloca- It is possible that in some instances a formal
tion of the odontoid (Figs 6 to 8). The final stage of the posterior fusion may not be required in patients with
disease involves increased bone destruction (Figs 2, 3, 9 displacement, but in view of the early healing and
and 10) with complete loss of the anterior arch of Cl, stability afforded by fusion, it is recommended that
fractures through the base of the odontoid or the fusion be performed in all such cases.
proximal portion of the body of C2, and eventually Conclusion. Tuberculosis at the atlanto-axial junction is
complete obliteration of the odontoid process. In the probably much more common in adults than has been
most severely affected cases there was complete loss of previously realised. Its effects can be permanent and it
both the odontoid and the anterior arch of Cl with a may even be fatal, but if treated early and adequately it is
grossly unstable articulation between the occiput and C2. curable in almost all cases.
Tuberculosis at the atlanto-axial region may be The classification system devised for this study is
much more common in adults than previously recog- simple and applicable to other conditions affecting the
nised. The spinal cord in this region is at risk either atlanto-axial region.
because of mechanical compression by a tuberculous
abscess or because of instability caused by destruction of
ligamentous structures and bone, allowing atlanto-axial
subluxation and/or upward translocation of the dens.
Any lesion at the atlanto-axial region requires urgent REFERENCES
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