Revisiting Anterior Atlantoaxial Subluxation with Overlooked Information on MR Images

S.-C. Hung; H.-M. Wu; W.-Y. Guo

摘要

BACKGROUND AND PURPOSE: The ADI is the imaging diagnostic clue to AAA subluxation of the cervical spine. Some MR imaging findings other than abnormal ADI relate to AAA subluxation. However, their relationship is not yet clarified. The present study elucidates the role of MR imaging by employing these previously overlooked findings. MATERIALS AND METHODS: This study enrolled 40 patients with AAA subluxation and 20 non-AAA subluxation patients as controls. All MR imaging was performed with supine neutral positioning. The morphology of the dens, bilateral facet joints, and surrounding ligaments, as well as the alignment of the anterior atlantoaxial joint, the spinolaminar line, and the intramedullary signal intensity, were assessed. This investigation statistically analyzed the difference among these groups. RESULTS: Thirty-eight percent (15 of 40) of patients with AAA subluxation showed nAAA. There was no significant difference between the groups of AAA with normal and abnormal ADI except that more peridental pannus was seen in the latter group. More dens erosion (P = .022), tilting of anterior atlantoaxial joint (P = .022), peridental effusion (P 2 mm). Statistical Analysis In patients with nAAA subluxation, the sensitivity and specificity of each individual MR imaging sign were calculated. Chi-square and Fisher exact tests were used to compare nAAA with aAAA subluxation, as well as nAAA subluxation with the control group, having P value set at <0.05. A combination of criteria that optimized sensitivity and specificity for the diagnosis of nAAA subluxation were also developed retrospectively. Results The study consisted of consecutive 43 patients with AAA subluxation who received MR imaging within a 3-month timeframe between 2004 and 2007. Three of them with the following conditions were excluded: one 75-year-old man with C2 fracture, one 9-year-old boy with incomplete ossification of the odontoid process, and one 42-year-man with different MR protocols. Consequently, the study group enrolled 40 patients (16 men, 24 women; age, 26–90 years; mean, 64.7 ± 12.9 years). The diagnoses of these patients consisted of rheumatoid arthritis (n = 11, 28%), ankylosing spondylitis (n = 1), trauma (n = 7), degenerative change (n = 19), and idiopathic or inconclusive (n = 2). Twenty-five of 40 patients (62%) (11 men, 14 women; age, 26–90 years; mean, 64.7 years) were diagnosed with aAAA subluxation with the ADI ranging from 3.1 to 9.5 mm (mean, 5.6 mm). The other 15 (5 men and 10 women) out of 40 patients (38%) were diagnosed with nAAA subluxation with a diagnoses of rheumatoid arthritis in 6, ankylosing spondylitis in 1, trauma in 2, and degenerative or idiopathic changes in 6. For the control group, the diagnoses included trauma (n = 2), degenerative changes (n = 16), and inconclusive (n = 2). Tables 1 and 2 summarize all MR imaging findings. View this table: [in this window] [in a new window] Table 2: Comparison of MR imaging findings of nAAA subluxation patients (n = 15) and the control group (n = 20) Peridental pannus was found in 88% of aAAA subluxation patients, abnormal spinolaminar line in 92%, and anterior atlantoaxial ligament change in 48% of the patients. These frequencies were greater than those for these conditions in the nAAA subluxation group (Table 1). Dens erosion, tilting of the atlantoaxial joint, and peridental effusion were observed, respectively, in 47%, 47%, and 40% of nAAA subluxation patients, which were significantly higher than in the control group, which had 0%, 10%, and 0%, respectively. An abnormal spinolaminar line was identified in 47% and focal myelopathy in 33% of the nAAA subluxation patients, but neither was found in the control group. No significant difference was found for peridental pannus formation or for signal intensity abnormalities within the anterior atlantoaxial ligament and apical ligament. Discussion Excessive movement between atlas and axis characterizes anterior atlantoaxial instability. At present, dynamic plain radiographs are the criterion standard in diagnosing AAA subluxation. The atlas slips abnormally forward during flexion because of laxity or rupture of the transverse and alar ligaments. The atlas slips backward when the cervical spine is in the neutral or extension positions. A few studies have reported MR imaging findings of AAA subluxation,8,9 but none has focused on the diagnostic implications of abnormalities in the associated structures or suggested a method to improve the false-negative diagnostic rate in nAAA subluxation patients. To our knowledge, this study is the first attempt to do so. Routinely cervical spine MR imaging is performed with supine and neutral positioning. With this positioning, gravity pulls the subluxated atlas backward and downgrades the severity of disease on MR images. In our study, x-ray radiographs with neutral positioning yielded a 28% (11 of 40) false-negative diagnostic rate, while MR imaging with supine neutral positioning produced a 38% (15 of 40) false-negative rate. To our knowledge, there is no report discussing the false-negative rate and sensitivity of dynamic radiography in assessing AAA subluxation. Dynamic MR imaging provides additional information over the routine neutral-positioning scan.8,9 However, it is time-consuming and impractical for daily imaging practice. Additionally, the lengthy scanning time may increase the risk of procedure-related cord compression; also, the false-negative rate of dynamic MR imaging was reported to be as high as 17%.9 Involvement of the atlantoaxial joint, including the peridental pannus, peridental effusion, and dens erosion, are frequently observed in AAA subluxation.10 Inflammation of the synovial lining of the bursae and articular capsule leads to pannus proliferation, followed by destruction of the cartilage and the subchondral bones and, finally, instability. In our series, there was no significant difference regarding pannus proliferation between the nAAA subluxation group and the control group. A possible explanation for this finding is that pannus formation usually reflects a reactive response to chronic inflammatory or degenerative disease. Pannus without associated bony erosion or ligamentous tear at the early disease stage does not lead to AAA subluxation. The subsequent bony erosion and increased synovial effusion represent arthritis that is more advanced. Additionally, instability of the anterior atlantoaxial joint results in negative pressure within the joint space that pulls in more interstitial fluid. Peridental effusion and dens erosion did achieve statistical significance in our study. Based on the biomechanics,11 there is no limitation to sagittal rotation of the atlantoaxial joint. That is, the atlas is free to rotate during flexion/extension until the posterior arch hits the occiput or the neural arch of C2. This means tilting of the atlantoaxial joint can be a normal finding during flexion and extension movements. However, tilting of the anterior atlantoaxial joint in the neutral position was seen in nearly half of the nAAA subluxation patients but was seen in none of the control group. One possible explanation is that instability and weakness of the periarticular structures holds the atlas loose in the neutral position. Whether this finding constitutes an early sign of instability requires further investigation. To our knowledge, no published report discusses this easily overlooked finding. The transverse ligament is recognized as the most important structure that is responsible for atlantoaxial instability.12 Because transverse and alar ligaments are difficult to visualize on sagittal images, this study chose peridental effusion and pannus as indirect signs of abnormalities within these structures, rather than direct inspection and measurement. Other ligamentous supporting structures, including the anterior atlantoaxial ligament and the apical ligament, are relatively ignored and are thought to be clinically insignificant.13 Apical ligament abnormalities (thickening or absence) in both groups were not rare.14 This observation is in agreement with previous reports,12,14 and it reflects the inconsistency of this vestigial structure. The anterior atlantoaxial ligament extends from the anterior midportion of the dens to the inferior aspect of the anterior arch of C1, and prevents hyperextension of the upper cervical spine. The role of the ligament in stabilizing the atlantoaxial joint is thought to be weaker than the transverse and alar ligaments and it provides a secondary support.15 Once the primary ligaments (transverse and alar ligaments) are disrupted, the secondary ligaments are susceptible to injury and stretch with relative ease. This probably explains why the abnormalities of the anterior atlantoaxial ligament were seldom observed in the nAAA subluxation group and the control group but were significantly more frequently seen in the aAAA subluxation group (48%). The tectorial membrane is a strong band of longitudinally oriented fibers, and it is one of the most important ligamentous structures in the craniovertebral junction.16 Its function is to check extension, flexion, and vertical translation. Skull base fracture with partial or complete disruption of the tectorial membrane is associated with instability.16 In our results, there is no significant difference among the study (both the aAAA and nAAA groups) and control groups, probably due to the stronger consistency of the ligament and being less susceptible to pannus erosion or wearing.17 Facet displacement of the lateral atlantoaxial joint has been proposed as a useful sign for diagnosing AAA subluxation by using conventional or 3D CT.18 In our results, a mild trend of facet displacement was observed in the nAAA subluxation group (data not shown) with a modest statistical difference (P = .14). Nevertheless, MR imaging provides more information about the facet joints beyond displacement. Subtle changes of lateral facet joints, such as bony erosion, presence of joint effusion, or joint space widening, were all more frequently observed in the nAAA subluxation group and were useful diagnostic clues in early detection of instability before facet displacement. In patients with nAAA subluxation, cervical compressive myelopathy is caused by 2 mechanisms. One mechanism is intraspinal encroachment of the peridental pannus, which is usually evident on MR images by its abnormal soft tissue signal intensity. The other mechanism is narrowing of the bony spinal canal by a subluxed atlas. Sometimes, this may not be apparent in the neutral position and is only evident during flexion.8 This explains why only 1 patient among the 5 patients with focal myelopathy in the nAAA subluxation group demonstrated spinal canal narrowing. Therefore, suspicion of atlantoaxial joint instability should always be kept in mind once focal high cervical myelopathy is depicted as the only significant finding. This study retrospectively applied optimal diagnostic criteria by using peridental effusion, lateral facet arthropathy, focal myelopathy, and an abnormal spinolaminar line. If the diagnosis of nAAA subluxation were made on the basis of either of these criteria, an optimal calculated sensitivity of 100% and a specificity of 90% could theoretically be achieved in this patient population. This combination of diagnostic criteria also supports the hypothesis that indirect signs of instability must occur in at least 1 of the anchoring points before AAA subluxation develops. Several limitations were present in this study. First, the study population was small, and approximately half of the study group had inflammatory arthritis. The known trend of rheumatoid arthritis to involve the synovial-lining joint and cause pannus formation may lead to a characteristic appearance different from those patients with spondylosis.19 However, in our results, no significant difference was found in the incidence of pannus between the nAAA subluxation and control groups. Second, additional tailored sequences, such as short inversion recovery or fat-saturated T2-weighted imaging, can improve detection of signal intensity in the atlantoaxial joint, craniocervical ligaments, and prevertebral soft tissues,20 and contrast-enhanced study can improve the delineation of pannus or synovitis and differentiate joint effusion and various forms of pannus and depict ancillary findings.21 On top of routine pulse sequences, we added these sequences for rheumatoid arthritis patients or those with other known inflammatory disorders. Because the study group included diverse clinical diagnoses, the short inversion recovery, fat-saturated FSE-T2-weighted, and postcontrast scanning were not used for all patients. Moreover, in some cases the diagnosis of AAA subluxation was not even suspected by the clinicians when they referred patients for MR examinations. Third, although AAA subluxation is the most frequent abnormality of the cervical spine in patients with rheumatoid arthritis, several other abnormalities may also occur in the same patient, including vertical atlantoaxial dislocation (atlantoaxial impaction) and rotatory atlantoaxial subluxation. The contribution of these coexisting instability problems to abnormal MR imaging findings is indisputable and should always be kept in mind. Conclusions MR imaging is a valuable tool for diagnosing atlantoaxial instability and has a sensitivity of 100% and a specificity of 90% based on our proposed diagnostic criteria (peridental effusion, lateral facet arthropathy, focal myelopathy, and an abnormal spinolaminar line). Additionally, MR imaging may provide earlier warning signs of instability that predate the clinical symptoms. Further investigations to confirm both these findings and the diagnostic efficacy of our criteria would be invaluable.

机译：背景与目的：ADI是颈椎AAA半脱位的影像学诊断线索。除了异常 ADI以外的一些MR影像学发现与AAA半脱位有关。但是，它们的关系尚尚不清楚。本研究通过利用这些先前被忽略的发现阐明了 MR成像的作用。材料与方法：本研究招募了40例AAA半脱位和20 非AAA半脱位患者作为对照。所有MR成像均进行仰卧位中性定位。窝，双侧小关节和周围韧带的形态，以及前寰枢关节，棘突的排列，并评估髓内信号强度。本研究从统计学上分析了这些组之间的差异。结果：38例AAA半脱位患者中有38％（40人中有15人）显示nAAA。正常和异常ADI的AAA组的之间没有显着差异，除了在后者组中观察到更多的偶然的pan。牙本质侵蚀（P = .022），前寰枢关节倾斜（P = .022），偶然渗出（P 2 mm）。统计分析在nAAA半脱位患者中，计算每个MR影像征象的敏感性和特异性。卡方检验和Fisher精确检验用于比较nAAA与aAAA半脱位，以及nAAA与半脱位的对照组，具有P 值设置为<0.05。还回顾性地提出了优化灵敏度和特异性以诊断nAAA半脱位的标准。结果该研究由连续的43例患者组成在2004年和2007年之间的3个月内接受MR成像的AAA半脱位。其中三个具有以下条件的患者被排除在外：一个75 1岁的C2骨折男子，1个9岁的男孩的齿突突骨化不完全，以及1个42岁的男孩，其MR规程不同。因此，研究组招募了40名患者（16名男性，24名女性；年龄26-90岁；平均， 64.7±12.9岁）。这些患者的诊断包括类风湿关节炎（n = 11，28％），强直性脊柱炎（n = 1），创伤（n = 7），退行性改变（ n = 19），特发性或不确定（n = 2）。 25名患者中有25名（62％）（男11例，女14例；年龄26- 90 年；平均64.7年被诊断为AAA半脱位，ADI范围为3.1至9.5 mm（平均5.6 mm）。在 40例患者中的另外15例（5名男性和10名女性）（38％）被诊断为nAAA半脱位，并被诊断为类风湿性关节炎在6例中，强直性脊柱炎在1例中，创伤在2例中，变性或特发性变化在6例中。对于对照组，的诊断包括创伤（n = 2），变性changes （n = 16），并且不确定（n = 2）。表1和2总结了所有MR影像学发现。查看此表：[在此窗口中] [在新窗口中]表2：nAAA半脱位的MR成像结果比较患者（n = 15）和对照组（n = 20），在88％的aAAA半脱位患者中发现了偶然的血管nu，异常的椎弓根线占92％，并且前寰枢椎 48％的患者的韧带改变。这些频率大于nAAA半脱位组（表1）中这些条件的频率。牙本质侵蚀，寰枢关节倾斜和nAAA半脱位患者分别有47％，47％和40％的患者出现了偶然的积液，显着高于患者。对照组分别有0％，10％和0％。在47％的nAAA半脱位患儿中发现了异常的棘柱状线和47％的局灶性脊髓病患者，但在对照组中没有发现。未发现偶然的pan神经元形成或前寰韧带和顶韧带内信号强度异常的显着差异。讨论寰枢椎和轴之间的过度运动是前寰枢椎不稳定的特征。现在，动态平片X片是诊断AAA半脱位的标准标准。由于屈曲或横韧带和翼韧带破裂，寰椎在屈曲过程中异常向前滑动。当颈椎处于中立位置或伸展位置时，地图集会向后滑动。少数研究报告了 AAA半脱位， 8,9 的MR影像学发现，但没有研究集中在相关结构异常的诊断意义上或建议使用方法来提高nAAA 半脱位患者的假阴性诊断率。就我们所知，这项研究是第一个尝试进行的研究。常规颈椎MR成像是在仰卧状态下进行的。通过这种定位，重力将半脱位图谱向后拉，并降低MR图像上疾病的严重性。在我们的研究中，具有中性定位的X射线射线照相能够产生28％（40分之11）的假阴性诊断率，而具有仰卧位中性定位的MR成像会产生^{38％（40分之15）的假阴性率。据我们所知，目前尚无讨论动态放射线照相术在评估AAA半脱位中的假阴性率和敏感性。动态 MR成像提供了常规中性定位扫描的更多信息。 8,9 但是，这很耗时，并且 < / sup>对于日常成像实践不切实际。此外，漫长的扫描时间可能会增加与手术相关的脐带压迫的风险；此外，动态MR成像的假阴性率据报道高达17％。 9 寰枢关节受累包括AAA半脱位常观察到胎盘，偶然的积液和牙本质侵蚀。 10 滑膜随后是软骨和软骨下骨骼的破坏，最后是不稳定。在我们的系列研究中，nAAA半脱位组与对照组之间的神经pan增生没有显着差异（）。此发现的可能的解释是，pan的形成通常反映了对慢性炎症或变性疾病的反应。在疾病早期没有相关骨侵蚀或韧带韧带撕裂的虫不会导致AAA半脱位。随后的骨侵蚀和滑膜积液增多代表关节炎更晚期。此外，前寰枢关节的不稳定性在关节空间内导致负压，从而吸引更多的组织液。偶然的积液和牙本质糜烂确实在我们的研究中达到统计学上的意义。基于生物力学， 11 对矢状面的旋转没有限制。寰枢关节。也就是说，地图集在弯曲/伸展过程中自由旋转，直到后弓击中枕骨或C2的神经弓。这意味着在屈曲和伸展运动中，寰枢关节的倾斜可能是正常现象。但是，在 nAAA半脱位患者的近一半中，可以看到前寰枢关节在中性位置上的倾斜，但是在对照组组。一种可能的解释是，关节周围结构的不稳定性和无力将地图集保持在中性位置。这一发现是否构成了不稳定的早期迹象，需要进一步调查。据我们所知，没有公开的报告讨论了这一容易忽视的发现。横向韧带被认为是导致寰枢椎不稳的最重要的结构。 12 由于在矢状位图像上很难看到横韧带和翼状韧带，因此本研究选择了顺发性积液和 pannus作为这些结构中异常的间接迹象，而不是直接检查和测量。其他韧带的支撑结构，包括前寰枢韧带和心尖韧带，都被相对忽略，并且被认为在临床上无足轻重。两组中的13 根尖韧带异常（sup> （增厚或缺失）并不罕见。 14 此的观察与以前的报道一致， 12，14 和反映了这种残余结构的不一致性。前寰韧带从牙窝的前中部延伸到C1前弓的下侧，并防止上肢过度伸展颈椎。韧带在稳定寰枢关节中的作用应该弱于横向韧带和翼状韧带，并提供了辅助支撑。 sup> 15 一旦初级韧带（横向韧带和翼状韧带）破裂，次级韧带就很容易受到伤害，并随着相对伸展sup>轻松。这可能解释了为什么在nAAA半脱位组和对照组中很少观察到前韧带异常，而在aAAA半脱位组中（48％）。结膜是一条很强的纵向取向的纤维束，是最重要的韧带结构之一。 / sup>在颅骨交界处。 16 其功能是检查的伸展，弯曲和垂直平移。颅底骨折并部分或完全破坏了覆膜与不稳定有关。 16 在我们的结果中，没有 < / sup>研究组（aAAA和nAAA 组）与对照组之间的显着差异，可能是由于韧带的一致性较强，并且对pan的侵蚀较不敏感或佩戴。 17 寰枢椎外侧关节的小平面移位已提出作为诊断AAA半脱位的有用标志通过使用常规或3D CT。 18 在我们的结果中，nAAA半脱位组的观察到了轻度的变化。 / sup>（未显示数据），但统计差异不大（P = .14）。尽管如此，MR成像仍提供了有关小关节的更多信息（位移除外）。在上，更经常观察到侧面小关节的细微变化，例如骨侵蚀，关节积液的存在，或关节间隙扩大。 nAAA半脱位组对于在小平面移位之前的不稳定性的早期检测中提供有用的诊断线索。在nAAA半脱位患者中，颈椎压缩性脊髓病是由2机制。一种机制是偶然神经pan的椎管内侵犯，通常通过其异常的软组织信号强度在MR图像上很明显。的另一种机制是通过半脱位的寰椎使骨脊管狭窄。有时，在中立位置可能不明显，并且在屈曲期间只有明显。 8 这解释了为什么在中只有1名患者 nAAA半脱位组的5例局灶性脊髓病表现为椎管狭窄。因此，一旦将局灶性高度颈椎病描述为唯一的重要发现，就应始终牢记怀疑寰枢椎关节不稳。本研究回顾性应用最佳诊断标准，方法是使用偶然性积液，侧面小关节病，局灶性脊髓病和棘突层异常。如果根据以下任一标准对nAAA半脱位进行诊断，则最佳计算灵敏度为100％，特异性为90理论上可以在该患者人群中达到％。这种诊断标准组合还支持以下假设：至少在1 在AAA半脱位发生之前的固定点。本研究存在一些局限性。首先，研究人口很小，并且研究组中大约一半患有炎性关节炎。类风湿性关节炎涉及滑膜衬里关节并导致血管pan形成的已知趋势可能导致特征性外观不同于脊椎病患者。 19 但是，在我们的研究结果中， nAAA半脱位组和对照组之间of的发生率没有显着的差异。其次，附加的定制序列（例如短反转恢复或脂肪饱和的T2加权成像）可以改善对寰枢关节，颅颈信号强度的检测韧带和椎骨前软组织， 20 和对比增强型研究可以改善血管nu或滑膜炎的轮廓，并且区分关节积液和各种形式的血管nu和 < / sup>描述辅助结果。 21 在常规脉冲序列的基础上，我们将这些序列添加到了类风湿关节炎患者或患有其他已知炎症的患者疾病。由于研究组包括各种临床诊断，因此不使用短反转恢复，脂肪饱和FSE-T2加权和对比后扫描适用于所有患者。此外，在某些情况下，当临床医生将病人转诊给MR检查时，甚至没有怀疑AAA半脱位的诊断。第三，尽管AAA半脱位是类风湿关节炎患者最常见的颈椎异常，同一患者也可能发生其他几种异常，包括垂直寰枢椎脱位（寰枢椎撞击）和旋转寰枢椎半脱位。这些并存的不稳定性问题对异常MR影像学发现的贡献是无可争辩的，应牢记在心。结论MR影像学是一种有价值的工具用于诊断寰枢椎不稳，根据我们提出的诊断标准（偶然渗出，侧面构面），灵敏度为100％，特异性为90％关节病，局灶性脊髓病和异常的Spinolaminar 线）。此外，MR成像可能会在临床症状出现之前就提供不稳定性的早期警告信号。进一步调查，以确认这些发现以及我们标准的诊断性功效将是无价的。 < / sup>}

Revisiting Anterior Atlantoaxial Subluxation with Overlooked Information on MR Images

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