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   Table of Contents  
ORIGINAL ARTICLE
Year : 2023  |  Volume : 14  |  Issue : 1  |  Page : 84-92  

Age- and gender-related radiological changes of the cervical spine: A study with largest magnetic resonance imaging database of 5672 consecutive patients


1 Department of Neurosurgery, Karadeniz Technical University, Trabzon, Turkey
2 Department of Radiology, Kecioren Training and Research Hospital, Ankara, Turkey
3 Department of Neurosurgery, Medical Faculty, Recep Tayyip Erdogan University, Rize, Turkey
4 Department of Pediatric Neurology, Medical Faculty, Karadeniz Technical University, Trabzon, Turkey

Date of Submission02-Feb-2023
Date of Acceptance20-Feb-2023
Date of Web Publication13-Mar-2023

Correspondence Address:
Ayhan Kanat
Department of Neurosurgery, Medical Faculty, Recep Tayyip Erdogan University, 53100, Merkez Rize
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcvjs.jcvjs_9_23

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   Abstract 


Background: The morphological features of the cervical spine are an essential issue. This retrospective study aimed to investigate the structural and radiological changes in the cervical spine.
Materials and Methods: A total of 250 patients with neck pain but no apparent cervical pathology were selected from a database of 5672 consecutive patients undergoing magnetic resonance imaging (MRI). MRIs were directly examined for cervical disc degeneration. These include Pfirrmann grade (Pg/C), cervical lordosis angle (A/CL), Atlantodental distance (ADD), the thickness of transverse ligament (T/TL), and position of cerebellar tonsils (P/CT). The measurements were taken at the positions of T1- and T2-weighted sagittal and axial MRIs. To evaluate the results, patients were divided into seven age groups (10–19, 20–29, 30–39, 40–49, 50–59, 60–69, 70, and over).
Results: In terms of ADD (mm), T/TL (mm), and P/CT (mm), there was no significant difference among age groups (P > 0.05). However, in terms of A/CL (degree) values, a statistically significant difference was observed among age groups (P < 0.05).
Conclusions: Intervertebral disc degeneration was more severe in males than in females as age increased. For both genders, cervical lordosis, decreased significantly as age increased. T/TL, ADD, and P/CT did not significantly differ with age. The present study indicates that structural and radiological changes are possible reasons for cervical pain at advanced ages.

Keywords: Age, cervical spine, gender, radiology


How to cite this article:
Guvercin AR, Arslan E, Hacifazlioglu C, Kanat A, Arslan EA, Yazar U. Age- and gender-related radiological changes of the cervical spine: A study with largest magnetic resonance imaging database of 5672 consecutive patients. J Craniovert Jun Spine 2023;14:84-92

How to cite this URL:
Guvercin AR, Arslan E, Hacifazlioglu C, Kanat A, Arslan EA, Yazar U. Age- and gender-related radiological changes of the cervical spine: A study with largest magnetic resonance imaging database of 5672 consecutive patients. J Craniovert Jun Spine [serial online] 2023 [cited 2023 Mar 25];14:84-92. Available from: https://www.jcvjs.com/text.asp?2023/14/1/84/371574




   Introduction Top


A thorough understanding of anatomy is necessary for practicing medicine.[1] The human spinal column has a complex anatomy with variations in the anatomy and measurements at each vertebral level. A healthy population has a wide range of spinal curvatures, especially in the cervical spine.[2] The existence of reciprocal lordotic and kyphotic concord between the cervical, thoracic, and lumbar curvatures has long been established, however,[3] due to its effect on the quality of life and association with disability indices, assessing global sagittal balance in patients with spinal abnormalities has acquired prominence.[4] In the case of spinal diseases, a thorough understanding of the pathophysiology is crucial.[5] Structural deformity or neural compression can occur in patients with cervical deformity.[6] As our knowledge of the subject grows, it has become increasingly clear that healthy individuals exhibit a wide range of spinal curvatures, particularly in the cervical spine.[3] The cervical spine is very intricate, with complexities enabling adequate cranial support[3] and an impressively broad range of motion (ROM).[7] Chronic cervical pain is an important issue, and it has a direct impact on quality of life, days off work, and healthcare costs. There is a correlation between cervical sagittal parameters and neck pain. Understanding the pathogenesis of neck discomfort is crucial to providing effective and affordable management because it affects 5% of patients and is frequently present in those who have sagittal balance problems.[4] As the degeneration develops, the spine's degenerative alterations steadily worsen its alignment and functionality and may lead to major disability and neurologic compromise. Degenerative disorders of the cervical spine have become increasingly common over the last decades. The cervical vertebra column bears the cranial weight,[8] and the morphological features of the cervical spine are important for the normal ROM. Therefore, optimal alignment of the cervical spine is crucial. Cervical spine pathologies can result in loss of focal cervical lordosis and disc height.[9],[10] During axial impact compression of the cervical spine, degeneration may be dependent on age-related changes in the cervical spine. Regarding the increased cervical spine pathologies in the aging population, it is necessary to determine the age- and sex-related structural and radiological changes in the cervical spine. As the proportion of the elderly population grows over time, more individuals with spine problems will likely present secondary to degenerative cervical spine pathologies. Recent years have been characterized by great technological and clinical development in spine surgery. Physiological movements of the cervical spine have been studied in various studies.[11] Radiology plays an important role in evaluating and diagnosing various cervical spine-related pathologies. Currently, noninvasive morphologic evaluation of the cervical spine is often made through computed tomography and magnetic resonance imaging (MRI). The particular biomechanics of the upper cervical spine require to guarantee the best possible surgical approach. We investigated cervical disc degeneration according to Pfirrmann grade (Pg/C), cervical lordosis angle (A/CL), atlantodental distance (ADD), the thickness of transverse ligament (T/TL), and cerebellar tonsil position (P/CT) for individuals of each gender and age group and attempted to clarify these age-related changes using data from MRIs of over 250 patients selected from a database of 5672 consecutive patients.


   Materials and Methods Top


A total of 250 patients without any specific symptoms related to cervical pathology were randomly selected from a database of 5672 consecutive patients who underwent MRIs. The selected patients had not had a cervical pathology in the past such as traumas in childhood. Ethical approval for this study was obtained (Approval number and date: B.10.4.İSM.4.06.68.49/March 13, 2013), with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Magnetic resonance imaging protocols

MRIs were performed with the precision spinal cord 1.5 Tesla system (signage HDxt, GEHC). Standard MRI protocols, including sagittal and axial T1A and T2A fast spin-echo sequences, were applied. Author CH assessed the magnetic resonance (MR) images.

Magnetic resonance imaging evaluation

The discoveries have changed the practice of neurosurgery,[12] but advancements in MR technology can be used to understand the nature of the spinal disorder.[13] Many radiographic parameters have been used to assess spinal misalignment. The Pfirrmann classification has been widely utilized as a classification system for cervical disc degeneration on MRI, despite being first developed as a classification for lumbar disc degeneration. In this study, the measurement of Pg/C, A/CL, ADD, T/TL, and P/CT, MRIs were directly evaluated by an experienced radiologist blinded to patients' clinical and demographic characteristics. The measurements for Pg/C, A/CL, ADD, T/TL, and P/CT were taken at the positions of T1- and T2-weighted sagittal and T2-weighted axial MRIs [Figure 1]. Cobb's method for measuring A/CL was used. A/CLs were measured by joining perpendiculars to lines drawn parallel to the lower endplates of C2 and C7.
Figure 1: The measurements were taken at the positions of T1-and T2-weighted sagittal MRI images. MRI: Magnetic resonance imaging

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Computer software tools, which included rulers, were used to measure the position of the tonsils by drawing a line from the Basion to the Opisthion (Basion-Opisthion reference line). The position of the tonsils was measured by drawing a perpendicular line from the inferior point of the tonsils to the Basion-Opisthion reference line. Values measured above from the foramen magnum were recorded with “−,” measurements below the foramen magnum were recorded with “+,” and cerebellar tonsils at the foramen magnum level were recorded with 0 values [Figure 1] and [Figure 2].
Figure 2: Shows a T2-weighted axial MRI. The position of the cerebellar tonsils was measured relative to the level of the foramen magnum. Values measured above the foramen magnum were recorded with “−,” measurements below the foramen magnum were recorded with “+,” and cerebellar tonsils at the foramen magnum level were recorded with 0 values. Pg/C: Pfirrmann grade, A/CL: cervical lordosis angle, ADD: Atlantodental distance, T/TL: Thickness of transverse ligament, P/CT: Cerebellar tonsil position relative to the foramen magnum

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Statistical analysis

The data obtained in this study were evaluated using the SPSS 20.0 software (SPSS Inc. Chicago, Illinois 60606-6307 U.S.A). Data frequency and percentage distributions were presented. After a normality test, during the examination of the differences between the groups, a Mann–Whitney U-test was applied to variables distributed nonnormally in binary groups. For nonnormally distributed variables with more than two groups, a Kruskal–Wallis H-test with a Bonferroni correction was used.

When examining the differences between groups, a significance level of 0.05 was preferred. If the significance level was P < 0.05, it was determined that a significant difference existed between the groups. If the significance level was P > 0.05, it was determined that the difference between the groups was not statistically significant.


   Results Top


Evaluation of findings in terms of gender groups

T/TL, ADD, and P/CT did not significantly differ with age (P > 0.05), but the increase in cervical changes with age was greater in females than in males [Table 1]. However, in terms of Pg/C2-3, Pg/C3-4, Pg/C4-5, Pg/C5-6, Pg/C6-7, and A/CL (degree) values, statistically, significant differences between the gender groups were identified (P < 0.05). Pg/C2-3, Pg/C3-4, Pg/C4-5, Pg/C5-6, and Pg/C6-7 were significantly higher in males than in females whereas A/CL (degree) values were significantly higher in females than in males [Table 1] and [Table 2]. [Figure 3] shows the higher values of A/CL in females and males according to the ages of patients.
Table 1: Pfirrmann grade 2-3, pfirrmann grade 3-4, pfirrmann grade 4-5, pfirrmann grade 5-6, pfirrmann grade 6-7, atlanta dental distance (mm), thickness of transverse ligament (mm), position of cerebellar tonsils (mm) and cervical lordosis angle (degree) values and statistical findings between the gender groups

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Table 2: Pfirrmann grade/C2-3, pfirrmann grade/C3-4, pfirrmann grade/C4-5, pfirrmann grade/C5-6, pfirrmann grade/C6-7 values among the age groups

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Figure 3: The higher values of cervical lordosis angles in females and males according to the ages of patients are shown

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Evaluation of intervertebral disc degeneration among age groups

In terms of Pg/C2-3 values, a statistically significant difference was observed between age groups (P < 0.05). Pg/C2-3 values in the 10–19 years of age groups were significantly lower than in other age groups. Pg/C2-3 values in the 20–29 years of age group were significantly lower than in the 40–49, 50–59, 60–69, and 70 and over age groups. Pg/C2-3 values in the 30–39 years of age group were significantly lower than in the age groups of 50–59, 60–69, and 70 and overage. Pg/C2-3 values in the 40–49 years of age groups were significantly lower than in the 50–59, 60–69, and 70 and above age groups [Supplementary Table 1]. In terms of Pg/C3-4 values, a statistically significant difference existed between age groups (P < 0.05). Pg/C3-4 values in the 10–19 years age group were significantly lower than in other age groups. Pg/C3-4 values in the 20–29 years of age group were significantly lower than in the 40–49, 50–49, 60–69, and 70 and over age groups. Pg/C3-4 values in the 30–39 years of age group were significantly lower than in the 50–59, 60–69, and 70 and above age groups. Pg/C3-4 values in the 40–49 years of age group were significantly lower than in the 50–59, 60–69, and 70 and above age groups.

In terms of Pg/C4-5 values, statistically significant differences between age groups were observed (P < 0.05). Pg/C4-5 values in the 10–19 years of age group were significantly lower than in other age groups. Pg/C4-5 values in the 20–29 years of age group were significantly lower than in the 40–49, 50–49, 60–69, and 70 and over age groups. Pg/C4-5 values in the 30–39 years of age group were significantly lower than in the 50–59, 60–69, and 70 and above age groups. Pg/C4-5 values in the 40–49 years of age group were significantly lower than in the 50–59, 60–69, and 70 and above age groups.

In terms of Pg/C5-6 values, there was a statistically significant difference between age groups (P < 0.05). Pg/C5-6 values in the 10–19 years of age group were significantly lower than in the other age groups. Pg/C5-6 values in the 20–29 years of age group were significantly lower than in the 40–49, 50–49, 60–69, and 70 and over age groups. Pg/C5-6 values in the 30–39 years of age group were significantly lower than in the 50–59, 60–69, and 70 and above age groups. Pg/C5-6 values in the 40–49 years of age groups were significantly lower than in 50–59, 60–69, and 70 and above age groups.

Finally, in terms of Pg/C6-7 values, a statistically significant difference between age groups was observed (P < 0.05). Pg/C6-7 values in the 10–19 years of age groups were significantly lower than in the other age groups. Pg/C6-7 values in 20–29 years of age groups were significantly lower than in the 40–49, 50–49, 60–69, and 70 and over age groups. Pg/C6-7 values in the 30–39 years of age group were significantly lower than in 40–49, 50–59, 60–69, and 70 and above age groups. Pg/C6-7 values in the 40–49 years of age groups were significantly lower than in the 50–59, 60–69, and 70 and above age groups [Table 2].

Evaluation of other findings among age groups

In terms of ADD (mm), T/TL (mm), and P/CT (mm), statistically significant differences between the age groups were observed (P < 0.05). There was a statistically significant difference between the age groups in terms of A/CL (degree) (P = 0.012). A/CL (degree) values in the 30–39 years of age group were significantly higher than in the 50–59 years of age group [Supplementary Table 1] and [Figure 3]. As shown in Figure 3, the histogram shows the differences in A/CL between females and males according to aging.


   Discussion Top


Key results

The main finding of this study is that lordosis decreases with age and disc degeneration worsens with age. To the best of our knowledge, this large cross-sectional study of a total of 250 patients without any specific symptoms related to cervical pathology from a database of 5672 consecutive patients who underwent MRI examinations is the first time reporting. MRI data of 250 people without clinical symptoms or neurological deficits were also assessed. Those patients have had only cervical pain. This degeneration is more common in males than in females as age increases [Table 1]. As shown in Figure 3, the histogram shows the differences in A/CL between females and males according to aging. The main finding of this study is that lordosis decreases with age and disc degeneration worsens with age. These results also indirectly prove that neck pain is more common in males than in females. Morphological characteristics are important to the diagnosis of cervical biomechanical abnormalities. This study indicates that lordosis decreases with age and that disc degeneration worsens with age. This degeneration is more common in males than in females as age increases. The structural and radiological changes found in this study are therefore possible reasons for cervical pain in older adults.

The effect of aging

Aging is a complex biological process.[14] It leads to progressive changes in the spine. A whole host of gross-level neuroanatomical changes take place as we get older.[15] Vertebral joints are important because separate them from the adjacent vertebral bodies. With aging, both these joints and end plates undergo degeneration, and the shapes of the cervical vertebrae may change with aging. In this study, only 13 patients were older than 70 years. Geographic and ethnic variations of the cervical spine may affect the result of this study. We observed the interactive effect of aging in the patient population increased degeneration in all cervical intervertebral discs was observed for both genders with increasing age [Table 2]. Degenerative disc disease is a common disease of the spine.[16] The degeneration with aging may be responsible for changes in the spine. In humans, there are structural problems that relate to age,[17] because their body structures are sensitive to the effect of age and gender.[14] Older patients may have a different course than younger patients. Cervical extensor muscles have an important role the in maintaining the stability of the sagittal plane balance of the cervical spine, but the paraspinal muscle volume is decreased in older patients.[18] There is a relationship between paraspinal muscle volume and disc degeneration. Spinal balance is a necessary element for understanding spinal disease.[17] Symmetric load transmission across the entire spine is important[19] To examine the outcomes of a study, it is necessary to have testable hypotheses.[20] The human body, which appears symmetrical along the midline grossly.[18] is, in fact, asymmetrical both morphologically and physiologically.[19] Normal alignment of the spine depends on structural, muscular, bony, and articular factors.[17] This asymmetry has been explained as the result of differential mechanical loadings,[15] but it leads to side differences in mechanical loadings.[15] Aging affects the sexes differently.[14] In this study, without gender distinction, no statistically significant difference between the groups was observed for ADD, T/TL, and P/CT (P > 0.05) [Supplementary Table 1]. In general, it is accepted that ADD <5 mm is normal for the child age group, and ADD <3 mm is normal for the adult age group. In this study, individuals 10 years and older were evaluated and found that the mean ADD was 1.53 mm (1.36–1.61).

Certain anatomical structures call for detailed study due to their functional importance.[1] Spine anatomy has always been an interesting subject for medical scientists.[11],[21] The degenerative changes in cervical disc MRI are often seen in healthy subjects. Since it enables close examination of the cord and stabilizing ligaments in this region, MRI of the cervical spine is a technology that is increasingly used to assess the cervical cord and ligamentous anatomy.[22] The upper cervical spine is different from the rest of the subaxial cervical spine.[8] This part of the spine not only supports the mass of the head but also possesses the characteristics of the widest ROM related to the rest of the spine.[23] Normal atlantoaxial articulation is responsible for approximately 50% of cervical spine rotation.[24] In the study of Panjabi et al., it was reported on the quantitative anatomy of upper cervical spine ligaments.[25] They measured upper cervical spine ligament lengths and determined that the transverse ligament was 21.9 mm long and the alar ligaments were 10.3 mm long.[25] That study did not report the T/TL in the axial plane. In our study, the average T/TL was 1.98 mm (1.65–2.05). In our study, the P/CT was also measured relative to the level of the foramen magnum. In Chiari malformation, altered cerebrospinal fluid circulation at the foramen magnum prevents instantaneous pressure equilibration between the intracranial and spinal subarachnoid space[26] which depends on cerebellar herniation.[27] According to the measured cerebellar tonsil levels, the mean P/CT was −0.89 mm (−1.86–[−0.36]) for all age groups. Although the mean P/CT in the youngest age group (10–19-year-old) was −1.16 mm, the mean P/CT in the oldest age group (70 and above) was −1.28 mm [Table 3]. Therefore, it can be said that as age increases, the cerebellar tonsil does not progress caudally downward. This result also suggests that the Chiari malformation type I, which is detected through clinical findings in adults and older adults is congenital rather than acquired.
Table 3: Atlanta dental distance (mm), thickness of transverse ligament (mm) and position of cerebellar tonsils (mm), cervical lordosis angle (degree) values and statistical findings among the age groups

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The association between sex and spine disease is an interesting subject. The cervical alignment in female subjects can be lower than that in male subjects. We analyzed the cervical spines of 155 females versus 95 males. In females, A/CL changes with age more than in males. This is an interesting finding, as the (usually) weaker posterior muscular tension band in females could play a role. The cervical degeneration over time concerning gender and age for patients without a discrete history of pathology or trauma. As the current literature is limited on the demographic and longitudinal variations of cervical alignment, this study adds relevant contributions. A question may arise about how the patients were selected since neck pain patients without radiculopathy or myelopathy typically do not undergo MRI. In our country, cervical MRI is routinely requested for all chronic cervical pain.

The Pfirrmann disc grade is one intuitive measurement of disc degeneration, but also it has so many limitations to use, such as inter-extra-observed correlation.

Limitations

The retrospective design of the study that involved reviewing patients is a major disadvantage. The patients' ROM measurements related to the cervical spine and age-related changes, instead of prospectively measuring variables of interest, could not be done. The radiological view may have been good, but this does not always show that everything is going well.[24] In this study, the quantified neck pain in the sample population could not be performed. We did not use the Neck Disability Index which is commonly used for patients with cervical pathologies. There have been major changes in medical practice in the last decades,[28] and high technology has been used.[29] Today, radiologic evaluation is an increasingly important role in the diagnosis and management of patients. Significant advances in MRI have occurred[30] and our understanding of spinal disorders has evolved.[31] Moreover, we selected only 250 patients from a database of 5672 patients undergoing MRI. MRI is very sensitive and has specific to tissue disruptions,[17],[32] in the spinal cord but MRI has a disadvantage in the measurement of cervical lordosis. The biggest drawback of this study is that the measurements were done in MR images that were taken in the supine position. There can be some concern (s) about the accuracy of cervical lordosis measured in patients in prone positioning. Some spinal parameters could be evaluated precisely only by MR. For example, sometimes it is difficult to distinguish the posterior edge of the anterior C1 arch and the anterior edge of the odontoid process through MR image, so it could not be confirmed if ADD evaluation is precise. We omitted giving extra radiation to patients using cervical XR. Validity in research refers to how accurately a study answers the study question or the strength of the study conclusions.[8] Here, validity refers to how well the assessment tool measures the underlying outcome of interest.[8] Another limitation is the limited sample size of the study which is a major concern in terms of the statistics sample size[33] because the calculation of sample size is one of the important components of the design of a study. A further detailed study should be performed to argue for causality. If a researcher selects a smaller number of case, it may lead to missing significant differences even if it exists in the population.[34] The search question of this paper was age- and gender-related radiological changes utilizing MRI in the cervical spine. For these purposes, as the authors, we investigated cervical disc degeneration according to Pfirrmann grade (Pg/C), A/CL, ADD, and the T/TL, and cerebellar tonsil position (P/CT) for individuals. Although this was not a natural history study, a total of 250 patients in different age groups with MRI scans who were suffering from neck pain were examined. None of the patients had cervical spine pathology. As the nature of the spine is dynamic, sometimes, it is difficult to depict the pathology with a single conventional imaging modality. Those patients may need dynamic X-rays and/or MRIs for differential diagnosis and decision-making. Four parameters of the study except cervical lordosis can be measured rightly on the MRI, however, measurement of cervical lordosis on MRI is not proper, because MRI is taken in the supine position; however, cervical lordosis must be measured in the standing position.


   Conclusions Top


The main finding of this study is that lordosis decreases with age and disc degeneration worsens with age. This degeneration is more common in males than in females as age increases. In females, A/CL changes with age more than in males. T/TL, ADD, and P/CT were not significantly affected by age. This is novel and interesting information. Intervertebral disc degeneration and cervical spondylosis may cause cervical problems that in turn lead to biochemical and morphological modifications of the cervical spine.[35] The craniovertebral junction and the upper cervical region consisting of anatomical structures from the occipital bone to the C2–C3 intervertebral disc and the embryological, anatomical, and biomechanical properties of these regions are significantly different from the cervical vertebrae located in the subaxial region. Among all patients regardless of gender, the structural and radiological changes found in this study are therefore possible reasons for cervical pain in older adults. Pain may persist or recur despite well-indicated and well-performed disc surgery.[16] The development of pain can be associated with certain alterations in the balance of the spine.[8],[36] Of course, further studies are necessary to assess the reasons for cervical pain in older adults.

Authors' contribution

All authors read and approved the final version of the manuscript.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Kanat A, Aydin Y. Posterior C1-C2 transarticular screw fixation for atlantoaxial arthrodesis. Neurosurgery 1999;44:687-9.  Back to cited text no. 23
    
24.
Kanat A. Comment on Bunmaprasert et al. Reducible nonunited type II odontoid fracture with atlantoaxial instability: Outcomes of two different fixation techniques. Int. J. Environ. Res. Public Health 2021, 18, 7990. Int J Environ Res Public Health 2022;19:5018.  Back to cited text no. 24
    
25.
Panjabi MM, Oxland TR, Parks EH. Quantitative anatomy of cervical spine ligaments. Part I. Upper cervical spine. J Spinal Disord 1991;4:270-6.  Back to cited text no. 25
    
26.
Yilmaz A, Kanat A, Musluman AM, Colak I, Terzi Y, Kayacı S, et al. When is duraplasty required in the surgical treatment of chiari malformation type I based on tonsillar descending grading scale? World Neurosurg 2011;75:307-13.  Back to cited text no. 26
    
27.
Yolas C, Kanat A. Recrudescence of the syringomyelia after surgery of chiari malformation type 1 with duraplasty. Br J Neurosurg 2020;34:697-700.  Back to cited text no. 27
    
28.
Aydin MD, Kanat A, Aydin A, Aydin A, Demirci T, Ozmen S. Estimating basilar artery upper rupture limit by dangerous alarming diameter of arteries (DADA) following bilateral common carotid artery ligation; a new theorem. Int J Neurosci 2022;132:107-13.  Back to cited text no. 28
    
29.
Kanat A. Wrong-site craniotomy. J Neurosurg 2013;119:1079-80.  Back to cited text no. 29
    
30.
Polat HB, Kanat A, Celiker FB, Tufekci A, Beyazal M, Ardic G, et al. Rationalization of using the MR diffusion imaging in B12 deficiency. Ann Indian Acad Neurol 2020;23:72-7.  Back to cited text no. 30
  [Full text]  
31.
Ozdemir B, Kanat A, Erturk C, Batcik OE, Balik MS, Yazar U, et al. Restoration of anterior vertebral height by short-segment pedicle screw fixation with screwing of fractured vertebra for the treatment of unstable thoracolumbar fractures. World Neurosurg 2017;99:409-17.  Back to cited text no. 31
    
32.
Kanat A, Yazar U, Kazdal H, Sonmez OF. Introducing a new risk factor for lumbar disc herniation in females: Vertical angle of the sacral curvature. J Korean Neurosurg Soc 2012;52:447-51.  Back to cited text no. 32
    
33.
Celiker M, Kanat A, Ozdemir A, Celiker FB, Kazdal H, Ozdemir B, et al. Controversy about the protective role of volume in the frontal sinus after severe head trauma: Larger sinus equates with higher risk of death. Br J Oral Maxillofac Surg 2020;58:314-8.  Back to cited text no. 33
    
34.
Kilic M, Aydin MD, Demirci E, Kilic B, Yilmaz I, Tanriverdi O, et al. Unpublished neuropathologic mechanism behind the muscle weakness/paralysis and gait disturbances induced by sciatic nerve degeneration after spinal subarachnoid hemorrhage: An experimental study. World Neurosurg 2018;119:e1029-34.  Back to cited text no. 34
    
35.
Inan Gezgin MK, Yildirim CH, Altun I, Berkyurek E, Geyik AM, Yildirim K. Microdiscectomy and intervertebral disc replacement for herniation involving fifth and sixth cervical vertebras: Our experience with 53 patients. Sinir Sist Cerrahisi Derg 2015;1:1925.  Back to cited text no. 35
    
36.
Kanat A, Ozdemir B. In reply to the letter to the editor regarding “restoration of anterior vertebral height by short-segment pedicle screw fixation with screwing of fractured vertebra for the treatment of unstable thoracolumbar fractures”. World Neurosurg 2017;101:793.  Back to cited text no. 36
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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