Correlation Between the Ossification of Nuchal Ligament and Clinical

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provided by Elsevier - Publisher Connector Kaohsiung Journal of Medical Sciences (2012) 28, 538e544

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ORIGINAL ARTICLE Correlation between the ossiﬁcation of nuchal ligament and clinical cervical disorders

Yu-Lin Tsai a, Ming-Cheng Weng a, Tien-Wen Chen a, Yi-Lun Hsieh c, Chia-Shin Chen a,b,c, Mao-Hsiung Huang a,b,c,*

a Department of Physical Medicine and Rehabilitation, Kaohsiung Medical University Hospital, Kaohsiung, Taiwan b Facility of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan c Graduate Institute of Neuroscience, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan

Received 30 May 2011; accepted 10 August 2011 Available online 28 August 2012

KEYWORDS Abstract This is a correlation analysis between severity of the ossification of the nuchal Cervical spine; ligament (ONL) and clinical cervical disorders including neck dysfunction, cervical malalign- Neural foramen; ment, and morphologic changes of the cervical neural foramen (CNF). The clinical effects of Nuchal ligament; ONL on active range of motion (AROM) of neck, cervical radiculopathy, abnormal cervical Ossification curvature, and the degree of CNF stenosis in patients with painful neck stiffness are investigated. Studies have investigated the predisposing factors to cervical dysfunction and degenerative disorders; however, few studies have examined the influence of the ONL on neck function and cervical spine. A total of 31 participants with painful neck stiffness were recruited. They accepted measurement of cervical AROM and serial cervical radiographs at anterioreposterior view, lateral view, and bilateral oblique views. Parameters of radiographs measurement included cervical lordotic curve, and cross-sectional areas (CSA) of the ONL and CNF (C2eC3, C4eC5, C5eC6, and C6eC7 levels). The ratio of CSA of the lower CNF (C4eC5, C5eC6, C6eC7) to CSA of the upper CNF (C2eC3) was used as a CNF stenosis ratio. The correlations of ONL size, neck symptoms, cervical AROM, lordotic curve, and CNF stenosis ratio were analyzed. More than half of all patients were positive in cervical root signs and prone to have larger ONL. Neck AROM of all participants was significantly belownormalaverageinalldirections,and a moderate negative association was found between the ONL CSA and AROM in flexioneextension. Most patients had moderate loss of cervical lordotic curve despite there being no significant correlation between ONL CSA and cervical curvature. Moreover, CNF stenosis ratio significantly negatively correlated with

* Corresponding author. Department of Physical Medicine and Rehabilitation, Kaohsiung Medical University Hospital, 100 Tzyou 1st Road, Kaohsiung 807, Taiwan. E-mail address: [email protected] (M.-H. Huang).

ONL CSA. Patients with larger ONL had more severe cervical radiculopathy, more stiffness in ﬂexioneextension direction, more complex degenerative change of spine, and worse CNF stenosis. Copyright ª 2012, Elsevier Taiwan LLC. All rights reserved.

Introduction degeneration, and malalignment. The hypotheses for this experimental work were as follows: (1) the severity of ONL Nuchal ligament (NL) is an intervertebral syndesmosis would correlate to prevalence of cervical radiculopathy; (2) which spans the cervical spine and is firmly attached to the the severity of ONL would also correlate to degree of neck external occipital protuberance and to the spinous process stiffness; (3) more degeneration of cervical spine would of C7. It is typically described as a bilaminar fibroelastic coexist with ONL; and (4) worse intervertebral foramen intermuscular septum interposed between the paired narrowing would also coexist with larger ONL. groups of four muscles (rhomboideus minor, serratus posterior, splenius capitis, and trapezius) of the cervico- Materials and methods nuchal region [1e3]. Due to its anatomical and histological characteristics, NL is a reliable landmark widely used as Participants a means to assure a midline orientation. Some reports have demonstrated that NL is important for maintaining the Patients with chronic neck pain and stiffness were recruited lordotic alignment of the cervical spine and stabilizing the from the Rehabilitation Department of Kaohsiung Medical head during movement of the cervical spine [4e6]. University Hospital. All participants were screened by Furthermore, compromise or dysfunction of the NL may be routine physical examination and received serial plain one of the factors that predispose a patient to progressive radiographies of the cervical spine. The inclusion criteria kyphosis or localized junctional deformity [7,8], and NL were (1) painful neck stiffness for more than 2 months, and dysfunction may worsen cervical spine stability and align- (2) ONL recognized according to cervical plain films. The ment [9]. exclusion criteria were recent history of cervical trauma Ossification of the nuchal ligament (ONL) is a radio- (less than 2 months), cervical fracture (neither traumatic opaque formation in the soft tissues behind the spinous nor degenerated), rheumatoid cervical spondylopathy, processes of the cervical spine. Clinically, it is usually central nervous system disorders, spinal cord injury, and asymptomatic but is more often observed in Asian patients, any history of cervical spinal surgery. who are over 40 and are radiographed for some clinical Thirty-three participants (15 men and 16 women), with reason, such as pain or stiffness in neck, head, upper arms, a mean age of 58.5Æ8.3 years (range: 42e77 years) and or upper back [10,11]. Prior reports have variously inter- a mean duration of cervical symptoms of 4.8Æ3.7 months preted the ONL as calcareous bursitis, calcinosis circum- (range: 2 monthse1 years) were enrolled into the study. All scripta ligamenti nuchae, heterotopic development of the participants gave informed consent for the study, and the secondary nucleus of the spinous process of C6, or myositis protocol was approved by the Ethics Review Committee of ossificans circumscripta. Scapinelli [12] reported that the Kaohsiung Medical University. ONL is a true sesamoid bone which is generated from a slow, gradual substitution of a calcified fibrocartilage, and is similar to those commonly found in some tendons of Physical examination limbs. The formation of ONL may occur as a result of NL Spurling’s test, a specific physical examination maneuver in trauma, or, more frequently, may be related to chronic diagnosing acute cervical radiculopathy, was done for overload in NL [13e15]. Some investigators have proposed screening radiculopathy. Other tests for cervical root irri- that the ONL may be one of the spinal ligament ossification tation, such as the foraminal compression test, neck syndromes such as ossification of the ligamentum flavum, distraction, shoulder abduction test, and Valsalva’s ossification of the anterior longitudinal ligament, or ossifi- maneuver, were also carried out. Any one of these tests cation of the posterior longitudinal ligament [11,16,17]. (except Spurling’s test) being positive would be defined as Therefore, being similar to the ossification of other spinal positive in “other cervical root sign.” ligaments, ONL may be a coexisting disorder or may be a risk factor of other cervical degenerative diseases. Neck range of motion measurement However, unlike the ossification of other spinal ligaments, studies demonstrating the characteristics and the clinical To measure cervical active range of motion (AROM), the significance of ONL are limited [11,15,18]. The effect of the patients were instructed to sit on a chair in an upright ONL on patients’ symptoms and cervical function is still position and perform some neck warm-up exercises before unclear. measurement. Using a universal goniometer, the examiner The purpose of the present study was to investigate the measured cervical AROM in flexioneextension, lateral relationship of ONL size to the severity of cervical disorder bending, and lateral rotation three times. Then, the mean including decreasing range of motion, radiculopathy, spinal values of the three repeated measurements of total 540 Y.-L. Tsai et al.

ﬂexioneextension, lateral bending, and lateral rotation correlation coefﬁcient values (0.71e0.82), indicating good were calculated and recorded. to excellent agreement for both intra- and inter-rater All these clinical measurements were performed by one comparisons [29]. of the authors, a rehabilitation physician who was blinded to information concerning the patients’ radiographs. Statistical analysis

Radiographic assessments of the cervical spine All data were analyzed by statistical analyses performed with SPSS statistical software version 12.0 (SPSS Inc., Chi- All participants underwent serial cervical radiographic cago, IL). Statistical significance was attributed to p values images at anterioreposterior, lateral, and bilaterally obli- less than 0.05. Independent t-tests were used to determine que views. These images were optimized for evaluation of the difference of ONL size between the subgroups. Using cervical bony structures and were digitally acquired Pearson’s correlation method, the CSA of ONL was analyzed through a picture archiving and communication system for correlation with neck AROM, cervical lordotic curve, and (PACS). All assessments were performed subsequently using CNF stenosis ratio. In general, a correlation coefficient (r) PACS software. All radiographic assessments and measured of 0e0.25 was considered to show little or no correlation, parameters were listed as follows. First, cervical degen- 0.25e0.50 to show a fair correlation, 0.5e0.75 to show erated changes such as significant degenerative osteoar- a moderate to good correlation, and above 0.75 to show thritis (spondylosis), degenerative disk disease, obvious a good to excellent correlation. uncovertebral osteophyte, and malalignment of cervical spine were recognized and defined by radiologists exam- Results ining the radiographs independently without patient information. Second, cervical lordotic curve at C2eC7 was measured using the modified Cobb method [19,20] and Demographic data and clinical findings Harrison posterior tangent methods [21,22], which have been proposed over the years for measurement of thoracic The demographic data and the descriptive statistics for kyphosis and cervical lordosis from lateral radiographs symptoms, signs, and radiographic findings of the 31 (Figs. 1A and B). Third, cross-sectional areas (CSA) of ONL patients in the study are shown in Table 1. When inclusion and bilateral cervical neural foramen (CNF) at one upper and exclusion criteria were matched, all participants had cervical spine (C2eC3, the least change of CNF in cervical painful neck stiffness and ONL to varying degrees. As for spine) and three lower cervical spines (C4eC5, C5eC6, signs of cervical radiculopathy, more than half of all C6eC7) were measured by one of the authors (another patients had positive findings: 17 (54.8%) patients were rehabilitation physician) who also measured the cervical positive in Spurling’s test, and 18 (58.1%) patients were lordotic curve and knew nothing about the patients’ infor- positive in other root signs (foraminal compression test, mation (Figs. 1C and D). neck distraction, shoulder abduction test, the Valsalva’s Clinical studies have documented that foraminal spon- maneuver). In addition, according to radiographic diag- dylosis and further root compression are highest in the noses confirmed by radiologists, more than half of all lower cervical spine, at C4eC5 through C6eC7 [23e28],so patients had associated cervical disorders: 26 (83.9%) we divided the mean of bilateral three lower CNF CSA patients had spondylosis, 25 (80.6%), had degenerative disk (C4eC5, C5eC6, and C6eC7) by the mean of bilateral disease, and 17 (54.8%) had uncovertebral osteophyte, C2eC3 foramina CSA as a “general CNF stenosis ratio” to except for malalignment of cervical spine (25.8%). More- individualize each patient’s CNF stenosis degree. Moreover, over, means of each neck AROM in this cohort of patients Æ e since most symptomatic CNF narrowing occur unilaterally, were 61.7 11.2 (range: 30 85 ) in total flex- e Æ e we selected the data in the worse side of each patient and ion extension, 66.2 14.4 (range 5 130 ) in total lateral Æ e obtained a “specific CNF stenosis ratio” with the same bending, and 82.2 13.3 (range: 60 120 ) in total method used for general CNF stenosis ratio. rotation.

Reliabilities of radiographic assessments Correlation of cervical root sign and CSA of ONL

Two observers with varying clinical experience reviewed As shown in Table 2, when these 31 patients were divided 10 sets of blinded radiographs (lateral view of cervical into subgroups based on signs of radiculopathy, there were spine), which were randomly selected. To study inter-rater statistically significant differences in the CSA of ONL Z variation of radiographic assessments, they measured the between the subgroups of Spurling’s test (p 0.034) and Z CSA of ONL and C2eC3 CNF, and cervical lordotic curve other cervical root signs (p 0.048). measured using the two methods mentioned above in each set of radiographs three times and recorded the mean Correlation of cervical AROM and CSA of ONL value. To determine intra-rater variation, the second measurement was performed by the same observers blin- As shown in Table 3, a moderate negative association was ded to results of the first measurement, with a 30-minute found between the CSA of ONL and total flexioneextension interval. The intraclass correlation coefficient was calcu- AROM (r Z e0.56, p < 0.01). Also, referencing to normal lated to determine inter- and intra-rater reliability. Each global motion of the cervical spine (total flex- measurement consistently demonstrated high intraclass ioneextension: 100e120, total lateral bending: 80e90, Nuchal ligament ossification and cervicalgia 541

Figure 1. The measurement of X-ray finding of cervical spine. (A) The modified Cobb method on the lateral radiographic views. (B) The posterior tangent method uses the two posterior vertebral body corners at C2 and C7. Measurement of cross-sectional area of (C) ossification of the nuchal ligament (ONL) and (D) cervical neural foramen. total rotation: 130e140) [30, 31], the neck AROM of all Correlation of CSA of ONL with radiographic participants was significantly below the normal average in changes of cervical spine each direction (p < 0.001). This was especially the case e with total flexion extension, in which 25 (80.6%) patients’ As for cervical curvature, there was no significant corre- neck ROM decreased by up to 30% (67.7% in total rotation; lation between ONL size and cervical lordotic curves, as 16.1% in total lateral bending). measured by the modified Cobb method or by the Harrison 542 Y.-L. Tsai et al.

Table 1 Radiographic findings and clinical signs of ONL Discussion patients. The NL is an important structure for cervical spine stability Variable Radiographic Radiculopathy Mean since it may limit flexion and influence muscular activity in diagnosis sign no. (%) ROM () the neck [1,2,4e6,9]. The ONL is one of the spinal ligament no. (%) ossification syndromes related to trauma or chronic over- Spondylosis 26 (83.9) load in NL [11,13,14,16,17], and is may be one of a number Degenerative disk 25 (80.6) of factors that may predispose a patient to progressive disease cervical spine instability and malalignment [7,8]. Uncovertebral 17 (54.8) In the present study, 31 patients with ONL (16 female osteophyte and 15 male), between 42 and 77 years of age, who were Malalignment 8 (25.8) consistent with patients prone to ONL were included Spurling’s test 17 (54.8) [11,15,16]. Among these middle-aged patients with ONL, Other root signs 18 (58.1) more than half were positive for signs of nerve root irrita- Myofascial pain 12 (38.7) tion. Moreover, those patients with positive signs of nerve syndrome root irritation were prone to have larger ONL (negative Total flexione 61.7 Æ 11.2 group: 76.4 Æ 49.22 and 76.3 Æ 37.2 mm2; positive group: extension 113.5 Æ 44.0 and 111.5 Æ 52.6 mm2), which supported our Total lateral 66.2 Æ 14.4 first hypothesis. bending To our understanding, few studies have reported the Total lateral 82.2 Æ 13.3 effect of the ONL on patients’ symptoms and cervical rotation function. Compared with the normal average of neck AROM ONL Z ossification of nuchal ligament; ROM Z range of motion. [30,31], our findings demonstrated that the neck AROM of patients enrolled in this study were all significantly below the normal average in each direction. Greater decreases of AROM by up to 30% were found in total flexioneextension. posterior tangent methods. Regarding the CNF narrowing, In addition, the ONL was mainly related to limitation of significant negative association was found between the neck flexioneextension, which is consistent with previous CSA of ONL and the general CNF stenosis ratio reports [4e6], despite the absence of a significant corre- (r Z e0.427, p < 0.05) and the specific CNF stenosis ratio lation between this and the other directions of cervical (r Z e0.416, p < 0.05). The above data are summarized in AROM. Table 4. Observing the X-ray characteristics of 141 participants with ONL, Luo et al. [15] reported several coexistent disorders including vertebral hyperosteogeny (65.96%), Correlation of CSA of ONL with various radiographic intervertebral space or intervertebral foramen stenosis findings (51.06%), anterior or posterior longitudinal ligament calcification (34.75), and cervical instability (46.81%). Our Correlation between ONL and several radiographic assess- results demonstrated that, except for uncovertebral ments are demonstrated in Table 5. By dividing these 31 osteophyte (54.8%) and malalignment (25.8%), more than patients into subgroups based on radiographic findings, 80% of all ONL patients had associated cervical disorders a significant difference was found in the CSA of ONL including spondylosis (83.9%) and degenerative disk disease between positive and negative groups of uncovertebral (80.6%). Furthermore, there was a significant difference in osteophyte (p Z 0.015). There was no significant difference the CSA of ONL between patients with or without unco- in the CSA of ONL between the two groups of spondylosis, vertebral osteophyte. In addition, there was a trend degenerative disk disease, and malalignment. However, toward greater ONL CSA in patients who simultaneously there was a trend toward greater ONL CSA in those patients have more positive radiographic findings (S3 of 4 cervical having three or more positive radiographic findings (S3 disorders described above). Our third hypothesis could be positive findings), although it was not statistically signifi- supported by the above analysis and the results of previous cant (p Z 0.074). studies.

Table 2 Comparison of CSA of patients with or without cervical root sign. CSA (mm2) tp Positive group (mean Æ SD) Negative group (mean Æ SD) Sign of radiculopathy Spurling’s test 113.5 Æ 44.00 76.4 Æ 49.22 2.22 0.03* Other root signs 111.5 Æ 52.6 76.3 Æ 37.2 2.06 0.04*

*Significant difference between group means (p < 0.05). CSA Z cross-sectional area of ossification of nuchal ligament; SD Z standard deviation. Nuchal ligament ossification and cervicalgia 543

Table 3 Correlation of CSA and cervical ROM. Table 5 The differences of CSA in patients with various Variable CSA (mm2) p radiographic findings. Coefficients (r) 95% CI Variable CSA (mm2) p Cervical ROM Positive Negative Total flexione À0.56 À0.764 to e0.259 0.001* group group extension Radiographic findings Total lateral À0.06 À0.403 to 0.304 0.76 Spondylosis 97.8 Æ 51.4 91.0 Æ 41.6 0.78 bending DDD 101.2 Æ 52.3 78.2 Æ 31.0 1.03 Total lateral À0.12 À0.454 to 0.246 0.53 UO 115.8 Æ 52.2 73.6 Æ 34.9 0.02* rotation Malalignment 105.6 Æ 53.2 93.7 Æ 93.7 0.56 S3 positive findings 109.4 Æ 54.1 79.2 Æ 36.9 0.07 * Statistically significant (p < 0.05). CSA Z cross-sectional area of ossification of nuchal ligament; * Statistically significant (p < 0.05). ROM Z range of motion; CI Z confidence interval. CSA Z cross-section area of ossification of nuchal ligament; DDD Z degenerative disk disease; UO Z uncovertebral osteophyte. Compared to the prevalence of cervical instability (46.81%) reported in a previous study [15], we only found eight (25.8%) patients to have cervical malalignment as confirmed by radiologists. Referring to the literature [18] analyzed 50 cases of ONL and also reported higher demonstrating normal curve of cervical lordosis and its prevalence of involvement at the lower spinal segments (24% relationship to neck symptoms [32,33], we found that 29 at C5 level, 66% at C6 level, 4% at C7 level) [18]. Our results (93.5%) patients had cervical lordotic curve below normal showed that most ONL developed behind the lower spinal value (30) and 24 (77.4%) patients with cervical curve of segments, from C5 to C7, matching the findings of previous less than 20. This means that most of these ONL patients studies. Moreover, using CNF stenosis ratio to quantify and have abnormal cervical curvature and are prone to suffer individualize the CNF narrowing degree of each patient, the from associated neck complaints. However, we found no present study found a relationship of ONL to coexisting CNF significant effect of the ONL on the derangement of narrowing with a fair to moderate significant correlation, cervical spine. Limitations associated with the measuring which supported our fifth hypothesis. method may be the major reason for this. Although both It has been well documented that degenerative changes the modified Cobb method and the Harrison posterior of the intervertebral disks and nerve root impingement in tangent method are valid and reliable methods in wide use the intervertebral foramen occur most commonly at the e e e [19e22], in terms of fast screening radiographs, they still C5 C6 and C6 C7 spaces [25 27], and more than 80% of have limitations in evaluating complex curves, especially the cervical radiculopathy occurs at the C6 and C7 level when the spine develops an “S” curve. Other instruments, [28]. Lind et al. [34] have also demonstrated that the e complex measuring methods, or a sample consisting of largest intersegmental flexion extension motion occurs e e more participants may be necessary for further between C4 C5 and C5 C6. Chronic trauma or overload investigation. with aging at the lower segments of the cervical spine may As reported by Luo et al. [15], 86 (52.8%) patients had ONL explain the presence of ONL as well as CNF stenosis in this at the C5eC6 level and 38 (23.3%) at the C6eC7 level. Zhou area. However, how to explain the negative correlation between them and whether resolution of either could have a positive effect on the other are interesting questions which warrant further investigation. This study has several strengths, not only in examining Table 4 Correlation of CSA with radiographic changes of the correlation between ONL and neck symptoms and cervical spine. cervical function, but also in quantifying and individualizing Variable CSA (mm2) p personal CNF stenosis degree, and testing the relationship Coefficients 95% CI of the ONL to cervical curvature and CNF stenosis. From (r) plain radiography, we could screen the severity of ONL and CNF stenosis, and discover coexisting cervical degenerated Cervical Curvature disorders. Furthermore, the primary treatment strategy À À MCM 0.18 0.498 to 0.191 0.35 could initially be determined by physicians. À PTM 0.05 0.313 to 0.394 0.81 However, this study also has several limitations. First, CNF stenosis our sample size was too small to examine other factors that G CNF stenosis ratio À0.43 À0.679 to e0.086 0.02* may correlate with incidence or severity of ONL and CNF S CNF stenosis ratio À0.42 À0.671 to e0.072 0.02* stenosis including gender, age, lifestyle, and the course of associated diseases. A comparable group of individuals < * Statistically significant (p 0.05). having neck complaints without ONL, and long-term follow- Z Z CNF cervical neural foramen; CSA cross-sectional area of up are also important considerations for outcome study in ossification of nuchal ligament; G Z general; MCM Z modified these patients. 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