
==== Front
Spine (Phila Pa 1976)
Spine (Phila Pa 1976)
BRS
Spine
0362-2436
1528-1159
Lippincott Williams & Wilkins Hagerstown, MD

38288666
SPINE166938
10.1097/BRS.0000000000004944
00007
3
Cervical Spine
Imaging Characteristics of Nonrheumatoid Arthritis Patients With Retro-odontoid Pseudotumor
A Multicenter Case-control Study
Kawabata Soya MD afb_kawabata@yahoo.co.jp

Kuroshima Kohei MD bkohei_kuroshima@yahoo.co.jp

Kawaguchi Koki MD k-kawaguchi@med.mie-u.ac.jp
c
Takegami Norihiko MD cn-takegami@med.mie-u.ac.jp

Yurube Takashi MD btakayuru@med.kobe-u.ac.jp

Michikawa Takehiro MD dtakehiro.michikawa@med.toho-u.ac.jp

Akeda Koji MD ck_akeda@clin.medic.mie-u.ac.jp

Kakutani Kenichiro MD bkenkakutani@gmail.com

Fujita Nobuyuki MD anfujita2007@yahoo.co.jp

a Department of Orthopaedic Surgery, Fujita Health University, School of Medicine, Toyoake, Aichi, Japan
b Department of Orthopaedic Surgery, Kobe University Graduate School of Medicine, Kobe, Japan
c Department of Orthopaedic Surgery, Graduate School of Medicine, Mie University, Tsu, Japan
d Department of Environmental and Occupational Health, School of Medicine, Toho University, Tokyo, Japan
Address correspondence and reprint requests to Nobuyuki Fujita, MD, Department of Orthopaedic Surgery, School of Medicine, Fujita Health University, 1-98 Dengakugakubo, Kutsukake-cho, Toyoake, Aichi 470-1192, Japan; E-mail: nfujita2007@gmail.com
1 10 2024
30 1 2024
49 19 E315E321
8 11 2023
19 1 2024
© 2024 The Author(s). Published by Wolters Kluwer Health, Inc.
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. http://creativecommons.org/licenses/by-nc-nd/4.0/

Study design.

Multicenter case-control study.

Objective.

To identify imaging characteristics of the cervical spine in patients with retro-odontoid pseudotumor (ROP) without rheumatoid arthritis (RA) and determine the pathogenesis of ROP.

Background.

ROP results from proliferative changes in the soft tissue of the atlantoaxial junction surrounding the region of the transverse ligament, and is commonly seen in RA patients. However, the pathogenesis of ROP caused by mechanical instability of the upper cervical spine in patients without RA is yet to be explained.

Materials and Methods.

We collected imaging data [preoperative radiographs, magnetic resonance imaging (MRI), and computed tomography (CT)] of patients who underwent surgery between April 2011 and March 2022 at the three university hospitals for ROP (cases) and cervical spondylotic myelopathy (as age, sex, and institution matched controls). The two groups were compared for different parameters on cervical dynamic radiographs, MRI, and CT.

Results.

The ROP group consisted of 42 patients, and the control group comprised 168 patients. C2–C7 range of motion was significantly smaller in the ROP group (25.8 ± 2.6°) compared with the control group (33.0 ± 1.0°). C2–C7 sagittal vertical axis was significantly larger in the ROP group than the control group (39.3 ± 3.6 vs. 32.2 ± 1.3 mm). MRI and CT assessment showed progressive degeneration at all intervertebral levels in the ROP group. A significant positive correlation was observed between the thickness of the soft tissue posterior to the dental process and the atlantodental interval in the flexion position (r = 0.501).

Conclusions.

The development of ROP was associated with degeneration of facet joints and intervertebral disks in the middle and lower cervical spine. Our findings suggest that decreased mobility of the middle and lower cervical spine may cause instability in the upper cervical spine, leading to the formation of ROP.

Key words:

retro-odontoid pseudotumor
upper cervical spine
atlantoaxial subluxation
OPEN-ACCESSTRUE
STATUSONLINE-ONLY
==== Body
pmcSpinal surgery is often performed to treat various cervical spine diseases, such as degenerative myelopathy, radiculopathy, disk herniation, and the ossification of the posterior longitudinal ligament.1 In the cervical spine, surgical interventions are more commonly performed for the middle and lower cervical spine and rarely involve the occipital bone and upper cervical spine. Previously, arthrodesis for atlantoaxial subluxation in rheumatoid arthritis (RA) was a relatively frequent surgery of the upper cervical spine; however, with the introduction of biological agents for RA, the need for surgical management in the upper cervical spine of RA patients has significantly reduced.2 Meanwhile, the incidence of retro-odontoid pseudotumor (ROP) is increasing within the aging population.3,4

At present, the diagnosis of ROP is primarily based on magnetic resonance imaging (MRI), with substantial evidence supporting its use in diagnosis.5 On the basis of etiology and MRI findings, ROP is classified into three types.6 Type 1 is the most common variety and is identified as hypointense or isointense lesions on T1-weighted images and heterogeneous lesions in T2-weighted imaging caused by atlantoaxial subluxation. Type 2 has MRI findings similar to type 1 and reportedly results from cervical ankylosis, ossification of the anterior longitudinal ligament (OALL), or spondylosis of the cervical spine. MRI findings of type 3 include hypointense or isointense signals in T1-weighted lesions and hypointense C2–C3 disk herniation contiguous with the retro-odontoid space on T2-weighted images. As a compressive lesion of the upper cervical spine, this lesion may cause quadriplegia, gait disturbance, and respiratory disorders; therefore, surgical treatment is warranted in most cases where the symptoms progress. Common surgical options include C1 laminectomy without fusion3,7 and fixation with implants.4,8–10 In patients with RA, the development of ROP at the atlantoaxial junction is caused not only by instability of the upper cervical spine but also by pannus formation, an inflammatory granulation process seen in RA.11 While upper cervical spine instability is considered the primary cause of ROP formation in non-RA patients, the detailed pathogenesis remains unclear.12 Thus, we conducted a case-control study to analyze the imaging characteristics of the cervical spine in non-RA patients with ROP across various imaging modalities to understand the pathogenesis of ROP.

MATERIALS AND METHODS

Patients

In this case-control study, we included all adult patients who underwent surgery for a diagnosis of ROP (cases, ROP group) between April 2011 and March 2022 at the three university hospitals. Patients diagnosed with RA patients were excluded. In addition, patients who underwent surgery for cervical spondylotic myelopathy (CSM) at the same three hospitals during the selected period were included as controls. The control subjects were individually matched to the cases for age, sex, and hospital to obtain a case-to-control ratio of 1:4.

Outcome Measures

For all participants, the C2–C7 angle, C1–C2 angle, and atlantodental interval (ADI) were measured on preoperative cervical dynamic radiographs (Fig. 1). The C2–C7 angle was defined as the angle between the tangent lines of the lower endplates of C2 and C7 vertebral body. The C1–C2 angle was defined as the angle between the tangent line connecting the lower end of the C1 anterior and posterior arch and the tangent line of the lower endplate of the C2 vertebra. ADI was defined as the distance between the posterior surface of the atlas and the front surface of the odontoid. The range of motion (ROM) of C2–C7 and C1–C2 segment was defined as the difference between flexion and extension. In addition, the C2–C7 sagittal vertical axis (SVA), the C1 sagittal inner diameter, and the presence of the atlas hypoplasia (C1 sagittal inner diameter of ≤29 mm)12 were evaluated on cervical spine radiographs in the neutral position (Fig. 1). The C2–C7 SVA was defined as the distance between the posterior superior corner of C7 and the vertical line from the center of the C2 vertebra.13 The C1 sagittal inner diameter was measured from the posterior surface of the anterior arch and the anterior surface of the posterior arch. We also evaluated the presence of atlantoaxial subluxation (AAS) on cervical radiographs, which was defined as ADI >3 mm in flexion position and not fixed in dynamic flexion and extension.14 Next, the degree of facet joint degeneration and intervertebral disk degeneration in the C2/3 to C6/7 segments were evaluated on computed tomography (CT) and MRI, respectively. Facet joint degeneration on CT imaging was classified as grade I: normal, grade II: the presence of degenerative changes, such as narrowing of joint space, cyst formation, and small osteophytes without joint hypertrophy, grade III: facet joint hypertrophy due to large osteophytes without fusion, and grade IV: bony fusion of the facet joint.15 Likewise, disk degeneration on MRI was classified as grade 0: normal disk, grade 1: mild degeneration, grade 2: moderate degeneration with disk bulging, and grade 3: disk height lower than 25%.16 In addition, the thickness of the soft tissue posterior to the dental process was mesured on sagittal T1-weighted MRI (Fig. 2) according to previous reports.12,17 Finally, correlation coefficients with the ADI in flexion position were calculated for all patients.

Figure 1 Radiographic image of cervical alignment parameters. Angles are shown in black and distances in white.

Figure 2 Mesurement of the thickness of the soft tissue posterior to the dental process on sagittal T1-weighted MRI. The white line indicates the length to be measured.

Ethics Approval

This study was approved by the institutional ethical review board of each hospital, which approved the opt-out consent method based on the retrospective design of the study. The principles of the Declaration of Helsinki were followed throughout the conduct of the study.

Statistical Analysis

Characteristics of the case and control group patients were compared using the Student t test and χ2 test as appropriate. Pearson correlation coefficient was used to assess the correlation between variables. In addition, we constructed a receiver operating characteristic curve (ROC) and calculated the area under the curve (AUC) to estimate the predicted value of the thickness of the soft tissue posterior to the dental process requiring surgery. The cutoff value was the maximum value of the Youden index (sensitivity + specificity −1). All statistical analyses were performed using IBM SPSS Statistics (version 29.0; IBM, Armonk, NY).

RESULTS

Patient Characteristics

There were 42 patients in the ROP group (27 male and 15 female; mean age = 76.4 ± 1.3 years), and 168 patients in the control group (108 male, 60 female; mean age = 76.6 ± 0.6 years). In the ROP group, 6 patients had a history of posterior cervical decompression and 1 patient had a history of posterior cervical decompression and fixation. On the other hand, in the control group, no patient had previous surgery on the cervical spine.

Radiographic Assessment

Table 1 presents the results of radiographic assessment. Both groups had a comparable C2–C7 lordosis angle in the flexion position; however, it was significantly smaller in the ROP group in the neutral and extension positions. The average C2–C7 ROM was significantly smaller in the ROP group (25.8 ± 2.6°) than in the control group (33.0 ± 1.0°), whereas the C2–C7 SVA was significantly larger in the ROP group compared with the control group (39.3 ± 3.6 mm vs. 32.2 ± 1.3 mm).

TABLE 1 Radiographic Parameters of Cervical Spine

	ROP group	Control group	P	
C2–C7 lordosis (°)	
 Neutral	7.6 ± 2.4	14.6 ± 1.0	0.003	
 Flexion	−8.6 ± 2.1	−7.1 ± 1.1	0.55	
 Extension	17.3 ± 2.4	26.3 ± 1.1	< 0.001	
C2–C7 ROM (°)	25.8 ± 2.6	33.0 ± 1.0	0.01	
C2–C7 SVA (mm)	39.3 ± 3.6	32.2 ± 1.3	0.01	
C1 sagittal inner diameter (mm)	34.6 ± 0.5	35.3 ± 0.3	0.26	
Hypoplasia of the atlas (%)	4.8	3.0	0.564	
C1-2 angle (°)	
 Neutral	28.5 ± 1.3	30.5 ± 0.6	0.12	
 Flexion	21.7 ± 1.3	25.5 ± 0.5	0.002	
 Extension	34.1 ± 1.1	34.1 ± 0.5	0.97	
C1-2 ROM (°)	12.4 ± 0.9	8.5 ± 0.4	< 0.001	
ADI (mm)	
 Neutral	3.8 ± 0.3	1.6 ± 0.1	< 0.001	
 Flexion	5.7 ± 0.4	1.9 ± 0.1	< 0.001	
 Extension	3.0 ± 0.3	1.3 ± 0.1	< 0.001	
ADI between flexion and extension (mm)	2.7 ± 0.4	0.6 ± 0.1	< 0.001	
AAS (%)	76.2	7.1	< 0.001	
AAS indicates atlantoaxial subluxation Student t test or χ2 test; ADI, atlantodental interval; ROM, range of motion; ROP, retro-odontoid pseudotumor; SVA, sagittal vertical axis.

In terms of the C1–C2 measurements, the C1 sagittal inner diameter and the percentage of patients with atlas hypoplasia were similar in both groups (Table 1). The ROP group had an average C1–C2 angle of 21.7 ± 1.3° in the flexed position, which was significantly smaller than that of the control group (25.5 ± 0.5°). This allowed an average of 12.4 ± 0.9° of C1–C2 ROM in the ROP group compared with 8.5 ± 0.4° for the control group.

Table 1 also presents the results of the ADI and AAS evaluation. ADI was significantly greater in the ROP group than in the control group in all three positions (flexion, neutral, and extension). Likewise, ADI in flexion and extension was also significantly greater in the ROP group. AAS was present in 76.2% of the ROP group patients compared with only 7.1% in the control group.

MRI and CT Findings

The ROP group showed more progressive disk degeneration in all intervertebral disks on MRI (Table 2) and degenerative changes in the facet joints at all levels (C2/3 to C6/7) in the CT examination (Table 3). Both facet joints and intervertebral disks showed particularly higher degeneration at the C4/5 and C5/6 levels and mild degeneration at the C2/3 level.

TABLE 2 MRI Evaluation of C2/C3-C6/C7 Disk Degeneration

	Grade	P	
1	2	3	
C2/3	
 ROP group	21 (51.2)	16 (39.0)	4 (9.8)	< 0.001	
 Control group	149 (88.7)	17 (10.1)	2 (1.2)		
C3/4	
 ROP group	4 (9.5)	19 (45.2)	19 (45.2)	< 0.001	
 Control group	53 (31.5)	90 (53.6)	25 (14.9)		
C4/5	
 ROP group	4 (9.5)	26 (61.9)	12 (28.6)	< 0.001	
 Control group	47 (28.0)	84 (50.0)	37 (22.0)		
C5/6	
 ROP group	4 (9.5)	19 (45.2)	19 (45.2)	< 0.001	
 Control group	27 (16.1)	98 (58.3)	43 (25.6)		
C6/7	
 ROP group	4 (9.5)	18 (42.9)	20 (47.6)	< 0.001	
 Control group	54 (32.1)	76 (45.2)	38 (22.6)		
χ2 test.

ROP indicate retro-odontoid pseudotumor.

TABLE 3 CT Evaluation of C2/3-C6/C7 Facet Joint Degeneration

	Grade	P	
1	2	3	4	
C2/3	
 ROP group	0 (0)	9 (22.6)	17 (43.0)	14 (35.0)	< 0.001	
 Control group	18 (10.7)	61 (36.3)	79 (47.0)	10 (6.0)		
C3/4	
 ROP group	0 (0)	3 (7.3)	27 (65.9)	11 (26.8)	< 0.001	
 Control group	12 (7.1)	50 (29.8)	100 (59.5)	6 (3.6)		
C4/5	
 ROP group	0 (0)	2 (4.9)	28 (68.3)	11 (26.8)	0.04	
 Control group	9 (5.4)	46 (27.4)	105 (63.0)	8 (4.8)		
C5/6	
 ROP group	0 (0)	6 (14.6)	23 (56.1)	12 (29.3)	0.04	
 Control group	12 (7.1)	90 (53.6)	62 (36.9)	4 (2.4)		
C6/7	
 ROP group	1 (2.4)	14 (34.1)	20 (48.8)	6 (14.6)	< 0.001	
 Control group	12 (7.1)	119 (70.8)	31 (18.5)	6 (3.6)		
χ2 test.

ROP indicate retro-odontoid pseudotumor.

Assessment of the Soft Tissue Posterior to the Dental Process

Table 4 summarizes the results for the soft tissue thickness posterior to the dental process in the study patients. The mean soft tissue thickness in the ROP group was 9.6 ± 0.4 mm compared with 4.3 ± 0.1 mm in the control group (Table 4). Furthermore, a significant positive correlation was observed between the thickness of the soft tissue posterior to the dental process and the ADI in the flexion position (r = 0.501, P <0.001; Fig. 3).

TABLE 4 Thickness of the Soft Tissue Posterior to the Dental Process in Magnetic Resonance Image

	ROP group	Control group	P	
Thickness of the soft tissue posterior to the dental process (mm)	9.6 ± 0.4	4.3 ± 0.1	< 0.001	
Student t test.

ROP indicate retro-odontoid pseudotumor.

Figure 3 A positive linear correlation (r = 0.501, P < 0.001) was observed between the ADI in the flexion position and the thickness of the soft tissue posterior to the dental process. Black circles and solid black circles indicate control and ROP cases, respectively. ADI indicates atlantodental interval; ROP, retro-odontoid pseudotumor.

As per the ROC curve analysis, the optimal cutoff value for the predicted thickness of the soft tissue posterior to the dental process requiring surgery was 6.05 mm with 95.2% sensitivity and 91.4% specificity (AUC = 0.979; 95% CI: 0.96–1.00; Table 5).

TABLE 5 Cut off Value for the Predicted Thickness of the Soft Tissue Posterior to the Dental Process Requiring Surgery

	AUC	Cutoff value (mm)	Sensitivity (%)	Specificity (%)	
Predicted thickness of the soft tissue	0.979 (95% CI = 0.96-1.00)	6.05	95.2	91.4	
AUC indicate area under the curve.

DISCUSSION

To the best of our knowledge, this is the first study to include a large sample of nonrheumatoid ROP patients and evaluate the intervertebral disk and facet joints of the middle and lower cervical spine in these patients. We observed that the development of ROP was associated with degeneration of the facet joints and intervertebral disks in the middle and lower cervical spine, with severe degeneration at the C5/6 level and mild degeneration at C2/3. Presumably, the degeneration can start at C5/6 and progress cephalad to other intervertebral levels. This could cause decreased ROM presenting as limited C2–C7 extension and reduced lordosis angle in C2–C7, resulting in instability of the upper cervical spine. Furthermore, the positive correlation between ADI in the flexion position and the thickness of the soft tissue posterior to the dental process suggests that ROP may develop due to increased ADI associated with C1/2 instability. Takahata et al 12 also reported that decreased ROM in C2–C7 can lead to the development of ROP, which is one of the few reports evaluating radiographically intervertebral degeneration as a cause for limited ROM. Tanaka et al 6 described AAS and cervical ankylosis, OALL, or spondylosis of the cervical spine as different causes of ROP. Meanwhile, our results suggest that a decrease in C2–C7 ROM may lead to AAS as a result.

With the advent of MRI, ROP in three nonrheumatic patients with atlantoaxial instability was first repoeted in 1986.5 At the time, the authors considered chronic mechanical irritation as the cause of ROP development. Eventually, it was reported that a disruption of the ligaments and capsular support structures present at the craniocervical junction can cause atlantoaxial instability.18 In this study, we found a significant correlation between ADI in the flexion position and soft tissue thickness behind the dental process, suggesting that the progressive AAS increases the formation of reactive fibrocartilage masses, which eventually develop into ROP. A synovial joint exists between the transverse ligament and the odontoid, which is the potential region where the inflammatory and repair processes may be repeated. As a result, the possibility of reactive fibrocartilaginous mass enlargement has been reported in this region.19

Histopathologically, ROP is composed of inflammatory cells and fibrous and granulation tissues.5,20 There is substantial evidence regarding AAS and soft tissue proliferative changes at the atlantoaxial junction associated with RA; however, the need for upper cervical spine surgery has reduced dramatically with advances in the nonsurgical treatment of RA.2 On the other hand, considering the pathogenesis of ROP which primarily involves degenerative changes in surrounding structures, the number of patients with ROP is expected to increase in an aging society. In addition, the idea that global alignment, including the thoracolumbar spine, influences cervical spine alignment is becoming more common and has been corroborated in numerous reports.21,22 An increase in the number of cases with ROP is anticipated in an aging population, which may be triggered by deformities of the thoracolumbar spine; therefore, evaluating the alignment of the entire spine is essential.

The common treatment options for ROP include direct resection,23,24 C1 laminectomy without fusion,3,7 occiput–cervical (O-C) fusion,4,8 and atlantoaxial (C1–C2) arthrodesis.9,10 C1 laminectomy without fusion is considered suitable for patients without upper cervical spine instability, while fixation is recommended in cases of instability.12 Notably, several studies have reported resolution of the ROP after fixation.10,25 However, patients with ROP have a high degree of degeneration of the middle and lower cervical spine, and fixation of the upper cervical spine may result in dysphagia. In particular, a decrease in the O-C2 angle is known to cause dysphagia; hence, caution is advised during fixation.26

There is a lack of definitive diagnostic criteria for ROP. Histologically, a soft tissue proliferative thickness of ≥3 mm is reported to be abnormal,18 with some studies defining ROP thickness as ≥3 mm or ≥5 mm.12,17 Since there are no clinically applicable methods to define ROP size, in this retrospective study, we defined “ROP” cases as patients who underwent upper cervical spine surgery due to ROP and those who had surgery on the middle and lower cervical spine for CSM were categorized as “CSM controls.” Nevertheless, based on our ROC analysis, we propose a 6.05 mm soft tissue thickness posterior to the dental process as the cutoff value for considering surgery in patients with ROP. If the soft tissue thickness exceeds this value, the patient is likely to develop spinal cord compression symptoms, requiring surgery. This value may be helpful in ascertaining surgical indications for ROP.

This study had several limitations. First, although the study was conducted at multiple facilities, ROP is a relatively rare disease, and consequently, the number of cases is limited which may lead to restricted clinical variation. Second, we selected CSM patients who underwent surgery as controls but did not include CSM patients on conservative treatment or adults without cervical diseases. Thus, the cutoff value of around 6 mm for ROP diagnosis in this study may not be generalizable in all contexts. Third, the outcome of each procedure was not evaluated. This was a retrospective study; patients were selected based solely on diagnostic name, and clinical aspects were not evaluated. Furthermore, patients with a history of cervical spine surgery were included only in the ROP group. It is possible that these may have influenced the results of this study. Finally, because this is a cross-sectional study, it is not possible to conclude that degeneration of the middle and lower cervical spine was responsible for the development of ROP. However, the primary objective of this study was to elucidate the pathophysiology of ROP, and despite these limitations, we believe that this study achieved its stated aims.

In conclusion, progressive degeneration of the facet joints and intervertebral disks in the middle and lower cervical spine may lead to chronic instability in the upper cervical spine, which is potentially responsible for ROP formation. In addition, a positive correlation exists between ADI in the flexion position and the thickness of the soft tissue posterior to the dental process, suggesting that ROP may develop due to increased ADI associated with C1/2 instability. This study offers valuable insight into the mechanisms behind the development of ROP.

Key Points

Imaging data of patients who underwent surgery for retro-odontoid pseudotumor (ROP) (42 cases) and cervical spondylotic myelopathy (168 cases as age, sex, and institution matched controls) were evaluated to determine the pathogenesis of ROP.

Development of ROP was associated with degeneration of facet joints and intervertebral disk in the middle and lower cervical spine.

Decreased mobility of the middle and lower cervical spine may cause instability in the upper cervical spine, leading to the formation of ROP.

References

The authors report no conflicts of interest.
==== Refs
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