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Table of Contents    
ORIGINAL ARTICLE
Year : 2018  |  Volume : 66  |  Issue : 5  |  Page : 1394-1399

Ossification of posterior longitudinal ligament and fluorosis


1 Department of Neurosurgery, Nizam's Institute of Medical Sciences, Hyderabad, Telangana, India
2 Department of Neurosurgery, Apollo Hospital, Hyderabad, Telangana, India

Date of Web Publication17-Sep-2018

Correspondence Address:
Dr. Vijaya Saradhi Mudumba
Department of Neurosurgery, Nizam's Institute of Medical Sciences, Hyderabad - 500 082, Telangana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.241343

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 » Abstract 

Objective: Ossification of posterior longitudinal ligament (OPLL) is a progressive disease that causes spinal canal compromise and serious neurological sequelae in advanced cases. The incidence of OPLL in the Asiatic population is 2%–3%, but the incidence is more in the background of fluorosis. Our aim was to study the association of OPLL with fluorosis by comparing urine fluoride levels and to study the types of OPLL.
Materials and Methods: Thirty consecutive patients with OPLL, observed on cervical skiagram, and confirmed by the computed tomography (CT) of the cervical spine, underwent a 24-h urine fluoride level assessment by the ion-selective electrode method. Due consent of all the patients was obtained and the data was collected. Thirty patients with a normal cervical radiograph were taken as a control group and their 24-h urine fluoride levels were compared with the test group. The 24-h urine fluoride level above 1.6 mg/L was taken as the diagnostic parameter of fluorosis. Imaging analysis of the study group focused on the subtype of OPLL, the mass occupying ratio, the sagittal cervical angle, the signs of dural penetration, and the spinal levels involved. Urinary fluoride levels were correlated with the presence of OPLL and different types of OPLL.
Results: Of the 30 patients with OPLL, 25 were males and 5 were females. The most common presentation was myelopathy. Continuous type of OPLL was seen in 11 (36.6%), segmental in 8 (26.6%), focal in 5 (16.6%), and mixed variant in 6 (20%) patients. 24-h urinary fluoride levels ranged from 0.26 mg/L to 12.2 mg/L. 18 (60%) of the patients in the study group were found to have urinary fluoride levels above 1.6 mg/L and only 1 patient (4%) of the control group had the urine fluoride level >1.6 mg/L. This difference was statistically significant. Patients with continuous and mixed types of OPLL had a higher mean urine fluoride level than those with a segmental and focal type of OPLL. The continuous variant of OPLL had a statistically significant occupancy ratio when compared to the other three variants, and the high mass occupancy ratio of the OPLL was directly associated with the presence of dural penetration.
Conclusion: Fluorosis is associated with a higher incidence of OPLL. Higher urinary fluoride levels correlate with the severe forms of OPLL.


Keywords: Fluorosis, myelopathy, OPLL, types of ossified posterior longitudinal ligament, urinary fluoride level
Key Message: On correlating the urinary fluoride levels with the presence of OPLL and different types of OPLL, it was observed that continuous and mixed types of OPLL were associated with a higher mean fluoride level than those with a segmental and focal type of OPLL. The continuous variant of OPLL had a statistically significant occupancy ratio within the spinal canal when compared to the other three variants, resulting in a greater dural penetration. Thus, the more severe forms of OPLL manifested in patients with a higher urinary fluoride level. In patients with cervical OPLL due to fluorosis, cervical kyphosis was found to rarely occur.


How to cite this article:
Reddy K V, Mudumba VS, Tokala IM, Reddy D R. Ossification of posterior longitudinal ligament and fluorosis. Neurol India 2018;66:1394-9

How to cite this URL:
Reddy K V, Mudumba VS, Tokala IM, Reddy D R. Ossification of posterior longitudinal ligament and fluorosis. Neurol India [serial online] 2018 [cited 2018 Oct 23];66:1394-9. Available from: http://www.neurologyindia.com/text.asp?2018/66/5/1394/241343


Ossification of posterior longitudinal ligament (OPLL) is a progressive disease that causes spinal canal compromise and serious neurological sequelae in advanced cases.[1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21] First described by Key in 1938, it was not until 1960 that OPLL was truly recognized following Tsukimoto's careful autopsy description.[22] A disease that characteristically occurs in the Asiatic population, its prevalence rate is estimated to be 2%–3%.[8],[23],[24],[25],[26],[27] The disease is significantly different from cervical spondylotic myelopathy, a disease more common in non-Asians.[26] Although the cause of OPLL has been debated, fluoride intoxication, diabetes mellitus, growth hormone imbalance, recurrent minor trauma, abnormal calcium metabolism, and infection have been suggested.[22] Fluoride is an important factor in bone mineralization.[25],[26],[27],[28],[29],[30],[31] An optimum intake of fluoride imparts protection against dental caries; however, excessive fluoride intake may cause fluoride intoxication, which is also known as fluorosis.[25] In the fluorotic zones, there is an increase in the number of cases of myelopathy due to cervical OPLL, and therefore, this entity is the cause of major concern. This study was an endeavour to find a correlation between the increased incidence of OPLL when associated with fluorosis. The various types of OPLL encountered were also correlated with the urinary fluoride level.


 » Materials and Methods Top


This is a cross-sectional observational study conducted between 2013 and 2015 at the Nizam's Institute of Medical Sciences, Hyderabad, India. The study group included 30 consecutive patients with symptomatic OPLL. The patient demographics, presenting symptoms, Nurick grading, and radiological characteristics were studied. A group of 30 patients with a normal cervical radiograph were selected as the control group. The 24-h urinary fluoride estimation was carried out in both the groups and the results were compared.

All the patients were enrolled in the study with their due consent and all the data were tabulated for reference.

The institutional ethical committee approval was taken. The ethical committee approval number of 256 was given for the study and a ‘no objection' certificate for publication was given.

Radiological assessment

Cervical X-ray, computed tomography (CT) scan, and magnetic resonance imaging were used to confirm the diagnosis of OPLL [Figure 1]. OPLL was classified as continuous, segmental, mixed and focal variants according to the classification proposed by Japanese Ministry of Public Health and Welfare.[19] The cervical curvature was measured by the Cobb's method. The C2–7 Cobb's angle was measured from the inferior C-2 endplate to the superior C-7 endplate.[5] Cervical spines with Cobb's angle >10° were classified as lordotic, those within the range −5° to 10° as straight, and those < −5° as kyphotic.[16] Mass occupying ratio (percentage of the spinal cord occupied by the OPLL) and signs of dural penetrance were also studied.
Figure 1: Cervical CT scan sagittal image showing the continuous type of OPLL and the X--ray anteroposterior view of the forearm showing ossification of the interosseous membrane

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Diagnosis of fluorosis

Urinary fluoride levels are the best indicators of fluoride intake. Since fluoride excretion is not constant throughout the day, 24-h samples of urine are more reliable than random or morning samples for estimation of fluoride content.[17],[18] Both the study and control group underwent a 24-h urinary fluoride level estimation and the results were compared. The urinary fluoride estimation was done by the ion-selective electrode method using Orion 4-Star Plus pH/ISE benchtop meter equipment, and a value >1.6 mg/L was considered as being diagnostic of fluorosis.[26] X-ray anteroposterior view of the forearm was done in the study group for identification of ossification of the interosseous membrane [Figure 1].[21]

Statistical methods

Descriptive and inferential statistical analyses were performed. The results on continuous measurements were presented as mean ± standard deviation (with the range being minimum–maximum) and results on categorical measurements were presented in numbers (and their percentages). The significance was assessed at 5% level of significance.

Analysis of variance was used to assess the significance of the study parameters between three or more groups of patients; chi-square/Fisher's exact test was used to assess the significance of the study parameters on a categorical scale between two or more groups.


 » Results Top


A total of 30 patients were included in the study group. The patient demographics regarding age, gender, Nurick's grading at presentation, and the OPLL types are depicted in [Figure 2],[Figure 3],[Figure 4],[Figure 5]. Based on the morphology of OPLL, 11 (36.6%) were of the continuous type, 8 (26.6%) of the segmental type, 5 (16.6%) of the mixed type, and 6 (20%) of the focal type. One level disease was present in 4 (13.3%), two levels disease in 2 (6.6%), three levels in 3 (10%), four levels in 5 (16.6%), five levels in 5 (16.6%), and six or more levels in 11 (36.6%) patients. The most common levels involved were C4–C6, with C5 vertebra being the most common level involved.
Figure 2: Male and female patients included in the study

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Figure 3: Age distribution in the study

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Figure 4: Grading of patients with myelopathy

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Figure 5: Morphology of OPLL on plain radiographs

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24-H urinary fluoride levels

In the study group, 18 of 30 (60%) patients had the urine fluoride levels in excess of 1.6 mg/L, which was diagnostic of fluorosis, whereas the control group had only 1 of 30 with urine fluoride levels in excess of 1.6 mg/L. The results were analyzed with Fisher's exact test, and the P value was <0.0001, suggesting a significant and a strong association of OPLL with fluorosis. A subgroup analysis of the urine fluoride levels among different types of OPLL was done [Figure 6] ]. A post hoc analysis had shown a significant difference in the urinary fluoride levels in the continuous type of OPLL when compared with the focal type (P = 0.044) and segmental type (P = 0.46).
Figure 6: Distribution of patients with 24 h fluoride levels

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Sagittal cervical angle

The sagittal cervical angle was measured in the study group using Cobb's method and Surgimap software . The results were compared among different types of OPLL and the difference was not found to be statistically significant. No patient in our group had kyphosis. However, straightening of the cervical spine was seen in 9 (26.6%) patients, a normal lordotic curvature in 12 (40%) patients, and hyperlordosis in 9 (26.6%) patients. The overall mean cervical curvature was 18.9°.

Occupancy ratio

The occupancy ratio (percentage of spinal canal occupied by OPLL) was measured using the Surgimap software. The mean occupancy ratio for the continuous type of OPLL was 54.3, for the mixed type 41.2, for the segmental type 35.1, and for the focal type 31. The overall mean occupancy ratio of OPLL was 42.5. The results were analyzed and a significant difference in the mean occupying ratio was found based on the OPLL type (P = 0.001). Post hoc analysis showed that the continuous type of OPLL had a significant higher occupancy ratio when compared with the focal (P < 0.0001) and segmental (P = 0.002) types.

Dural penetration

Dural penetration on CT scan was significantly different based on the OPLL type. The OPLL type (P < 0.006) and occupancy ratio (P < 0.001) had a direct correlation with the presence of dural penetration. Continuous and mixed types of OPLL with a higher occupancy ratio were associated with dural penetration.


 » Discussion Top


The association of age with OPLL secondary to fluorosis

The ossification of PLL secondary to fluoride intoxication is seen in patients who are beyond the middle age, as the disease severity depends on the quantity of fluoride ingested and the duration of exposure. Shortt et al.,[21] (1937) were of the opinion that a residence of 30–40 years in an endemic area was necessary for the development of a definite picture of skeletal fluorosis. Jolly et al.,[21] (1969) reported that the advanced stage of fluoride intoxication usually resulted from continuous exposure of an individual to 20–80 mg fluoride ion daily over a period of 10–20 years, and such a heavy exposure is associated with at least 10 ppm levels in water supply.[29],[30],[31] Thus, the manifestations of the disease rarely occur in young patients. In 1984, Tsuyama reported the highest incidence of fluoride intoxication among the 50–59 year age group in Japan.[24] Kim et al.,[9] (in the Korea population) and Wu JC et al. 27 (in the Taiwanese population) reported similar findings with the highest incidence in the fifth decade. In this study, the mean age was 52 years, which was similar to the age found in the earlier studies suggesting that an older age correlates with a higher incidence of OPLL.

Gender and fluorotic OPLL

OPLL has been reported to be more common in male patients. Overall, men were more commonly affected than women with the male: female ratio ranging from 1.1 to 3.0 in the previous reports. [8, 12, 15, 27, 28] Hiramatsu and Nobechi [7] reported contrary findings and demonstrated that women were affected three times more than men. This discrepancy can be attributed to their utilization of the institutional data base rather than a population-based data. In our study, the male-to-female ratio was 5:1. This may be attributed to an increased intake of water containing fluoride in males following excessive sweating, as most of our patients were manual labourers.

OPLL and fluorosis

The incidence of OPLL in the Asiatic population has been reported to be between 2%–3% in many previous studies. [8, 10, 16, 23, 24, 27] It has been postulated that the incidence may be more in fluorotic patients, but no study has defined a clear association between OPLL and fluorosis.[6],[14] In this study, of the 30 patients with OPLL, 18 patients had fluorosis, diagnosed by the 24-h urinary fluoride levels ≥1.6 mg/L and an ossification of interosseous membrane of the forearm. Previously, Reddy [17] had published that OPLL is very commonly observed (37 of 80 people) in endemic areas. In this study, we were able to document and strengthen this strong association of OPLL and fluorosis, explaining the reason for an increasing incidence of OPLL in endemic regions.

Fluoride is one of the essential minor elements with a daily requirement of less than or equal to 6 mg/day.[17] Fluorosis is caused by excessive intake of fluoride or its intoxication and was first reported by Feil in 1930.[17] Neurological complications occur in 10% of patients with skeletal fluorosis.[26] Hence, fluorosis should be considered as a potential contributing factor for cervical OPLL, especially in endemic areas.

Type of OPLL and urinary fluoride levels

In this study, we have documented that there was a significant difference in the urinary fluoride levels across different types of OPLL, and fluorosis was associated with more severe forms of OPLL. A higher fluoride intake over a prolonged period coupled with malnutrition, strenuous exercise, and environmental factors predispose to the development of fluorosis and OPLL.[17]. The most common subtype of OPLL was segmental in 39% of the patients according to Epstein.[3] Kalb et al.,[8] found that the most common form of OPLL in fluorotic patients was the segmental variety in 36.4%, followed by the focal variety in 27.3% patients. In this study, the most common type of OPLL was the continuous (36.6%) type followed by the segmental (26.6%) type, the mixed (16.6%) type, and the localized (20%) type. The continuous OPLL had the maximum urinary fluoride levels compared with the segmental OPLL, though in both the groups, the 24-h urinary fluoride levels were high when compared with the normal range. This is the first study in literature demonstrating a direct and strong association of OPLL with the 24-h urine fluoride levels.

The predilection of OPLL to occur in the cervical spine is linked to the mobile nature of the latter.[12] It has been reported that OPLL was absent behind the Klippel–Feil segment, whereas rest of the cervical spine had florid OPLL. Probably the congenitally fused segments sustained less severe strain, and therefore, less degeneration of the posterior longitudinal ligament (PLL) leading to a focal absence of OPLL posterior to the fused contiguous vertebral segments. Thus, the mechanical factors coupled with environmental and genetic factors predispose to OPLL formation. However, the factors contributing to the formation of different types of OPLL are still a mystery. Our study is the first of its kind to suggest that gradation of 24-h urinary fluoride levels was directly related to the severity of OPLL (that is, lower levels of 24-h urinary fluoride levels were related with focal/segmental types of OPLL, and the higher levels of 24-h urinary fluoride levels were associated with the continuous type of OPLL).

Occupancy ratio and OPLL

Imaging of the spine continues to be the most appropriate diagnostic tool. CT scan images were used to measure the percentage of spinal canal occupied by OPLL.[8] The occupancy ratio had no positive correlation with the myelopathy grade, which was also reported by Deshpande et al.[2] It was proposed that the clinical presentation depends not only on the percentage of the canal occupied by the OPLL but also on its effects on the blood supply to the cord. However, a canal stenosis of > 60% due to the presence of the OPLL is associated with a negative surgical outcome according to Kalb et al.,[8] and Saetia et al.[19]

In this study, the difference between the mean occupancy ratio among different types of OPLL was statistically significant. Post hoc analysis had shown that the severe forms of OPLL had a significantly higher occupancy ratio than the focal (P < 0.0001) and segmental (P = 0.002) types. These results were comparable to the results published in the study by Kalb et al.[8] wherein the mixed type of OPLL had a significantly higher occupying ratio than the localized (P = 0.011) or segmental (P = 0.008) types. However, the association between the occupancy ratio and the grade of myelopathy was not statistically significant in the present study.

Sagittal cervical angle

We evaluated the sagittal cervical angle for possible correlation with types of OPLL and found that there was no such correlation. The literature mentions that sagittal cervical angle varies from 11.3° ± 7.0°.[5],[10] The mean cervical angle was 18.9° in this study. Of the 30 patients, 9 had straightening, 12 maintained a normal lordotic curvature, and 9 had a hyperlordotic curvature. No patient in our study group had kyphosis and the same was reported by Fujimori et al.[5] and Lee et al.[11] Probably OPLL offers protection against development of cervical kyphosis.

An increase in kyphosis occurs when there was an existing kyphosis before surgery. However, Lee et al.,[11] have found that postoperative development of kyphosis was varying in different types of OPLL. Segmental OPLL was more often associated with postoperative kyphosis. The reason was the failure of segmental OPLL in providing enough stability to the spinal column to maintain the same preoperative cervical curvature after the laminectomy, when compared with the continuous type of OPLL.

Cho et al.,[1] in their study, where a total laminectomy was performed in patients with OPLL, found that none of their patients had preoperative kyphosis. However, 13 of the 14 patients developed kyphosis after total laminectomy. This may be due to the different definitions of kyphosis used in the study.

In this study, postoperative changes in cervical angle were not assessed, but it remains an area of interest for further study.

Dural penetration in fluorosis

Dural penetration with an OPLL is associated with the risk of postoperative cerebrospinal fluid (CSF) leak. A sagittal CT scan showing a single-layer sign, the “C” sign, or the ‘double-layer' sign, is a good predictor of dural penetration.[20]

Kalb et al.,[8] in their study stated that a high mass occupying ratio of OPLL was directly associated with the presence of dural penetration. Kalb et al.,[8] found signs of dural penetration in 60% and Min et al.,[13] in 30.5% patients, and these signs were more common in nonsegmental OPLL. In our study, signs of dural penetration were evaluated in different types of OPLL. It was found that the sign was present in 12 of 30 (40%) patients, out of whom a continuous form of OPLL was present in 8, and a mixed form of OPLL was present in 3. The continuous and mixed types of OPLL, which have high mass occupancy ratio, are associated with dural penetration. A careful preoperative assessment of the CT scan for dural penetration, especially in the continuous and mixed forms of OPLL, can predict and avoid postoperative complications such as CSF leak during the performance of anterior cervical surgery for removal of the OPLL.


 » Conclusion Top


The incidence of OPLL was found to be more in male patients. The peak incidence of OPLL was noted in the fifth decade. Fluorosis had a significant association with the incidence of OPLL. Higher urinary fluoride levels correlated with the severe forms of OPLL. Cervical kyphosis is rare among patients with cervical OPLL due to fluorosis.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

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Cho WS, Chung CK, Jahng TA, Kim HJ. Post-laminectomy kyphosis in patients with cervical ossification of the posterior longitudinal ligament: Does it cause neurological deterioration? J Korean Neurosurg Soc 2008;43:259-64.  Back to cited text no. 1
    
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Deshpande R, Dinakar I, Reddy SM. Calcified posterior longitudinal ligament and myelopathy. Indian J Orthop 1976;10.  Back to cited text no. 2
    
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Epstein, N. Ossification of the cervical posterior longitudinal ligament: A review. Neurosurg Focus 2002:13:1-10.  Back to cited text no. 3
    
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Fargen KM, CoX JB, Hof DJ. Does ossification of the posterior longitudinal ligament progress after laminoplasty? Radiographic and clinical evidence of ossification of the posterior longitudinal ligament lesion growth and risk factors for late neurological deterioration. J Neurosurg Spine 2012;17:512-24.  Back to cited text no. 4
    
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Hida K, Iwasaki Y, Koyanagi I, Abe H. Bone window computed tomography for detection of dural defect associated with cervical ossified posterior longitudinal ligament. Neurol Med Chir (Tokyo) 1997;37:173-6.  Back to cited text no. 6
    
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Kalb S, Martirosyan NL, Perez-Orribo L, Kalani MY, Theodore N. Analysis of demographics, risk factors, clinical presentation, and surgical treatment modalities for the ossified posterior longitudinal ligament. Neurosurg Focus 2011;30:E11.  Back to cited text no. 8
    
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]



 

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