Retrospective evaluation of CT-head scans for the association between posterior atlanto-occipital membrane ossification with  cervicogenic headache and migraine

doi:10.21203/rs.3.rs-1592140/v1

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Retrospective evaluation of CT-head scans for the association between posterior atlanto-occipital membrane ossification with cervicogenic headache and migraine

https://doi.org/10.21203/rs.3.rs-1592140/v1

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Purpose- The objective of the study was to find the prevalence of arcuate foramen and its association with cervicogenic headache and migraine. To study various demographic parameters associated with the anomaly and to correlate the extent of ossification of posterior atlanto-occipital membrane with the severity of symptoms.

Methods- A cross sectional study was done to analyze CT-head scans of patients with cervicogenic headache and migraine for the presence of arcuate foramen. Demographic parameters of the patients were collected from the detailed case report from achieves. The collected data was analyzed using SPSS, a p-value of <0.05 were considered significant.

Results- Arcuate foramen was prevalent in 41.8% of symptomatic patients. No significant association between the incidence of arcuate foramen and age group was found. Incidence is increased incidence among the male patients (61%). Patients who are labourer by occupation showed increased incidence (34.78%). A positive correlation (0.755) was found between the extent of ossification and the severity of clinical symptoms. The foramen was more commonly found on the left side and majority of patients presented with unilateral anomaly (27.27%).

Conclusion- Arcuate foramen is fairly prevalent among the symptomatic patients and is often neglected as an etiologic agent and leads delay in diagnosis and management. It can lead to injury to vertebral artery during screw placement if misidentified as broad posterior arch. Therefore, it must be screened in symptomatic patients and those patients undergoing lateral neck surgery using lateral cephalogram, if detected must be documented on health records of the patient.

Arcuate foramen

migraine

cervicogenic headache

computed tomography

atlanto-occipital membrane

The posterior atlanto-occipital membrane also known as the ligamentum flavum joins the posterior arch of the atlas with the occipital bone. The lateral edges of this membrane lies in close proximity with the 3rd part of vertebral artery [1]. Along with vertebral artery it also circumvents the 1st cranial nerve with venous plexus[2]. The lateral edges of this membrane may ossify which can lead to compression of vertebral artery by formation of a foramen which is known as the ‘arcuate foramen’. The compression of vertebral arteries by arcuate foramen may lead to blood flow disturbances which contributes to the incidence of neurological pathologies like migraine or Barre-Lieou syndrome[3] and clinically presents with the symptoms of headache, nausea, retro-orbital pain, dysphagia, dysphonia or, disturbances in vision[4]. There are several other names used to designate this anomaly like posterior ponticle, ponticulus posticus, posticus ponticus or kimmerle’s anomaly [5].

The patients with the presence of arcuate foramen predominantly presents with the chief complaints of headache, pain in the regions of neck-shoulder and arm, vertigo [6]. A study by Wight et al. reported that there is increased presence of this anomaly in common sufferers of migraine and cervicogenic headache with the odds ratio of 2 to 19:1 providing significant evidence of this association [7].

In radiologic studies, the prevalence of this association is mainly studied either in lateral radiographs or in CT-scans. However, a CT-based study provides more advantage over the lateral cephalograms in that the assessment of the morphology and laterality is more accurate [8]. The presence of this anomaly is not a rare phenomenon as in the western population the prevalence has been reported to be between 5.1% and 37.8% [9].

The exact cause of this anomaly is yet to be established but the probable causes can be congenital, genetic, ossification due to age or external mechanical factors. This anomaly assumes significant importance in the management of patients requiring cervical spine intervention particularly, C1 lateral screw placement in atlas region for the treatment of atlanto-axial instability, if ignored it can lead to vertebral artery injury which can have grave complications[10]. The knowledge of this anomaly is also very important in the diagnosis and management of patients with migraine or headache and the patients presenting with these complaints should be screened radiographically for its presence, as it is often overlooked [11].

Hence, the present study was undertaken to find out the association between posterior atlanto-occipital membrane ossification with cervicogenic headache and migraine by retrospective evaluation of CT-head scans and prevalence of arcuate foramen.

Ethics consideration:-

The study was conducted after obtaining approval from Institutional Ethics Committee; Reference No: GMCJ/IEC Approval/48/2021, Date- 2/6/2021.Strict confidentiality of the data is being maintained.

Study design:- Observational type of Cross sectional study.

Setting:- Study was carried out in Department of Radiology in Government Medical College, Jalgaon.

Study duration:- The study was conducted from 9th June 2021 to 10th September, 2021. Total study duration was 3 months. Of the total study duration research was done from 9th June, 2021 to 10th of August (2 months) followed by 1 month of report making.

Sample size:- The sample size is calculated by Cochran’s sample size formula i.e. Z²pq/e²; Z value = 1.96, p = it is the estimated proportion of population which has the attribute = 17.2, q = 100 – p = 82.8,

e = the margin of error = 10% Therefore, Z²pq/e² = 54.71 ~ 55

A total of 55 cases will be included in the study.

Inclusion criteria:-

All patients presented with the symptom of chronic headache or migraine in whom the CT scan reports are available are included in the study.

Exclusion criteria:-

Pregnant women.

Patients diagnosed with brain tumour.

Patients suffering from acute sinusitis, meningitis or other inflammatory conditions of brain or its related structures.

Patients with the history of chronic alcoholism.

Sample collection:-

CT-Head scans of the patients with the symptom of cervicogenic headache or migraine satisfying the inclusion criteria were collected from the archives division of the department in the digital format, from the detailed case report available parameters like age, sex and occupation of the patients were recorded.

Instrument used:-Toshiba Alexion 16 slice CT-scanner was used for scanning the patients included in the study.

Scan parameters:-Patients were in supine position with head first during the process of scanning, they were scanned from the vertex of the skull to the 2nd cervical vertebra (C2).

Sample analysis:-

The collected samples were grouped according to their age, gender, occupation (labourer in whom lifting of heavy weighted objects is involved as in farmers, construction workers etc. and non-labourers in whom lifting of heavy objects is not involved).

The recorded samples were scrutinized in Vitrea Workstation LT (Version 4.1.52) for the presence or, absence of arcuate foramen. The samples which presented with arcuate foramen were further evaluated whether the foramen is complete in which a complete bony ring is formed or, incomplete in which there is a defect in the bony ring. The presence of complete/incomplete foramen is taken as a positive finding. The collected samples were divided (on the basis of type of arcuate foramen) into normal in which the foramen was absent, partial/incomplete and complete.

The horizontal and vertical diameter of the complete arcuate foramen was also collected.

To rule out any error which may have occurred during collection, 20 random samples were re-evaluated after one month of initial examination.

The severity of headache was recorded in the detailed case report according to 6-point verbal rating scale (VRS) in which no pain indicated by a score of 0 followed by 1 for mild pain, 2 for moderate pain and 3 for severe pain, 4 for very severe pain and 5 for most severe pain imaginable. The scores were documented for its correlation with the extent of ossification (absent/incomplete/complete).

Of the 55 samples collected the mean age of the patients was 33.4 ± 13.86 years with the range of 7 to 73 years. There were a total of 25(45.4%) male patients and 30(55.6%) female patients.

Statistical tools and methods:-

The collected samples were analyzed in SPSS statistical package (version 25). Descriptive statistics such as mean, standard deviation and percentage were used to present the collected data. Chi-square test was used for determining the significance of difference in incidence of complete and incomplete arcuate foramen between gender groups and different age group, a p-value of < 0.05 were considered significant.

The present study was carried out in the Department of Radiology for the period of 2 months from 9th June, 2021 to 10th August, 2021. A total of 55 CT-Head scans has been included in the study.

Table 1

Age wise and gender wise distribution of the patients (n = 55)
AGE WISE DISTRIBUTION
Age group	No. of patients	Percentages (%)
< 10	1	1.82
10–20	8	14.54
21–30	17	30.90
31–40	14	25.46
41–50	9	16.37
51–60	4	7.27
61–70	1	1.82
71–80	1	1.82
Total	55	100
GENDER WISE DISTRIBUTION
Gender	No. of patients	Percentage (%)
Male	25	45.45
Female	30	54.55
Total	55	100

Table 1 and Fig. 1 shows the age wise and gender wise distribution of patients. Out of the total 55 samples which were studied, the maximum number of patients who presented with the complaint of headache or migraine are present in the age group of 21–30 years (30.90%) followed by in the age group of 31–40 years (25.45%). Gender wise distribution shows females have a higher rate of presentation with headache or migraine as compared to males with 30 females (54.55%) and 25 males (45.45%).

Table 2

Distribution of patients according to the presence or absence of arcuate foramen(n = 55)
Arcuate foramen	No. of patients	Percentage (%)
Present	23	41.8
Absent	32	58.2
Total	55	100

Analysis of 55 CT-Scans revealed the presence of arcuate foramen on one or both side(s) in 23 patients (41.8%). Thus, the present study found the prevalence of arcuate foramen to be 41.8% among the patients with cervicogenic headache and migraine. (Table 2 and Fig. 2)

Table 3

Age-wise distribution of patients with the presence of arcuate foramen (n = 23)
Age group	No. of patients with arcuate foramen	Percentage (%)	No. of patients without arcuate foramen	Percentage (%)
< 10	0	0	1	3.13
11–20	3	13.64	5	15.62
21–30	5	22.73	12	37.5
31–40	5	22.73	9	28.12
41–50	5	22.73	4	12.5
51–60	3	13.64	1	3.13
61–70	1	4.54	0	0
71–80	1	4.54	0	0
Total	23	100	32	100

The age-wise distribution data indicates that there is increased incidence of arcuate foramen in the age groups of 21–30, 31–40 and 41–50 years with 22.73% each followed by the age groups 11–20 and 51–60 years as shown in Table 3 and Fig. 3. However, no significant association between the incidence of arcuate foramen and age group was found.

Table 4

Comparison of the gender-wise prevalence of arcuate foramen using Chi Square test(n = 23)
Gender	No. of patients with arcuate foramen	Percentage (%)	No. of patients without arcuate foramen	Percentage (%)
Male	14	61	11	34.37
Female	9	39	21	65.63
Total	23	100	32	100
χ2 -3.789 p-value 0.047

Gender-wise distribution of patients with arcuate foramen shown in Table 4 and Fig. 4 showed that there is increased incidence among the male patients with 14 male patients showing the presence of arcuate foramen (61%), while 9 females were found with the presence of arcuate foramen (39%). The difference in incidence between males and females was statistically significant (p-0.047).

Table 5

Comparison of occupation-wise prevalence of arcuate foramen using Chi Square test
Occupation	Present	Percentage (%)	Absent	Percentage (%)
Labourer (n = 10)	8	34.78	2	6.25
Non-labourer (n = 45)	15	65.22	30	93.75
Total	23	100	32	100
χ2–7.323 p-value- 0.009

On analysis of distribution of patients with arcuate foramen according to their occupation as shown in Table 5 and Fig. 5, it is evident that there is increased incidence among the patients who are labourer by occupation (34.78%) as compared to 6.25% patients with absence of arcuate foramen. And the difference observed was statistically significant (p-0.009).

For measuring the intensity of pain, 6-point verbal rating scale (VRS) was used with no pain indicated by a score of 0 followed by 1 for mild pain, 2 for moderate pain and 3 for severe pain, 4 for very severe pain and 5 for most severe pain imaginable.

A positive correlation (0.755) was found between the extent of ossification (absent/incomplete/complete) and the severity of clinical symptoms and it was statistically significant with a p-value < 0.001 as shown in Fig. 6.

Table 6

Dimensions of the complete arcuate foramen found in the study(n = 3)
Diameter (mm)	Complete foramen no.1	Complete foramen no.2	Complete foramen no.3	Mean (mm)
Antero-posterior	8.4	7.4	8.1	7.96
Supero-inferior	4.7	6.5	5.2	5.46

The present study found 3 complete arcuate foramens in total with the mean antero-posterior diameter of 7.96mm (7.4-8.4mm) and mean supero-inferior diameter of 5.46mm (4.7-6.5mm) as shown in Table 6.

Table 7

Prevalence of complete and incomplete arcuate foramen with respect to side
	Absent	Incomplete	Complete	Total
Left side	37(67.27%)	16(29.09%)	2(3.63%)	55
Right side	42(76.63%)	12(21.81%)	1(1.81%)	55

As shown in Table 7 and Fig. 7, there is presence of 18 (16 partial + 2complete) arcuate foramen on the left side while on the right side there are 13 (12 partial + 1 complete) arcuate foramen, depicting a increased incidence on the left side.

The type of arcuate foramen (absent/incomplete/complete) are depicted in the figures below.(Figure: − 8–10)

Table 8

Analysis of arcuate foramen laterality in sample population.
Arcuate foramen		No. of patients	Percentage (%)
Present	Unilateral	15	27.27
Present	Bilateral	8	14.54
Absent		32	58.19
Total		55	100

On analysis of patients with the presence of arcuate foramen according to the laterality majority of the patients presented with unilateral arcuate foramen with the percentage of 27.27% while, 14.54% patients showed the presence of bilateral arcuate foramen as shown in Table 8 and Fig. 11.

Prevalence of arcuate foramen and its association with cervicogenic headache and migraine

In present study a total of 55 CT-Head scans from the patients with symptoms of cervicogenic headache and migraine were collected and analyzed for the presence of arcuate foramen, the overall prevalence of arcuate foramen was found to be 41.8%, the values are similar to Sabir et al.[12] who reported a prevalence of 42% in their study in which they investigated 100 patients with migraine. The prevalence varies according to geographical origin of sample population as in Table 1. Munjal et al.[13] reported a prevalence of 56.8% while Geist et al.[14] reported a lower prevalence of 26.2%.

Table 1 :-Comparison of prevalence of arcuate foramen in different studies with the present study

Various studies	Country	Type of study	No. of sujects	Prevalence of arcuate foramen [incomplete + complete] (no. of arcuate foramen)
Kaur et al[55]	India	Cadaveric	67	23.8% (16)
Baeesa et al.[56]	Saudi arabia	CT	453	47.9% (217)
Cederberg et al.[21]	US	X-Ray	255	38.1% (97)
Geist et al.[57]	Taiwan	CT	576	26.2% (151)
Karau et al.[58]	Kenya	Cadaveric	102	53.1% (55)
Munjal et al.[59]	India	X-Ray	620	56.8% (352)
Poplewski et al.[60]	Poland	Cadaveric	250	24% (60)
Sabir et al.[52]	India	X-Ray	100	42% (42)
Sylla et al.[61]	France	Cadaveric	50	36% (18)
Present study	India	CT	55	41.8% (23)

The pooled prevalence of arcuate foramen in general population in India is found to be 22.3%(incomplete 14.7% + complete 7.6%) as reported in a meta-analysis done by Pekala et al[15]. However the present study found a striking 41.8% prevalence of arcuate foramen in patients with cervicogenic headache and migraine which shows that the posterior atlanto-occipital membrane ossification is distinctly associated with cervicogenic headache and migraine.

Age wise incidence of arcuate foramen

The present study reported a higher incidence in age groups after puberty, while there was no case of arcuate foramen reported in less than 10 years of age thus excluding the theory of congenital origin of arcuate foramen while, there were higher number of patients with the presence of arcuate foramen as compared to patients without arcuate foramen in the age group above 40 years which reinstates the theory of ossification as it is a age related process as stated by Pyo et al.[16], Taitz et al.[17] who found that the presence of foramen was prevalent in the age group of 10-30 years and complete arcuate foramen was predominated in age of 30-80 years but, the present study found that there is increase incidence among the age group of 21-50 years. However, no significant association between the incidence of arcuate foramen and age group was found and it was consistent with the findings of Hiroli et al. [18]

Gender wise incidence of arcuate foramen

In terms of incidence by gender different authors has reported different predilections. Some studies report the incidence is more in the male population as reported by Hong et al.[19] in which they found that prevalence in male population was 19.3% while in female population it was 12.8%. On the contrary, in a study conducted by Schilling j et al. [20] showed higher prevalence in female as compared to males. However, the present study found male predominance of 61% and female 39%, the difference was statistically significant (p-0.047).The difference in prevalence could be attributed to difference in origin of sample population and sample distribution.

Prevalence of arcuate foramen by occupation

In the present study out of the total 10 labourers 8 labourers had the presence of arcuate foramen and the overall prevalence was 34.78% as compared to 6.25% patients who didn’t showed the presence of the foramen. The difference of prevalence of arcuate foramen among the labourer and non-labourer groups was statistically significant (p-0.009). This provides substantial evidence for the fact that the formation arcuate foramen may be due to external mechanical factors [17], such as those persons who are involved in regular lifting of heavy weighted objects as stated by a study done by Paraskevas et al. [21] the study also reported that among 176 samples studied they found the presence of arcuate foramen in 37.5% of labourers which is correlates to the findings of present study.

Extent of ossification and severity of symptoms

In a study done by Chitroda et al. [22] the presence of symptoms in patients with complete form of arcuate foramen had a higher incidence while, the presence of symptoms was less in patients with incomplete/partial form of arcuate foramen. Present study also found a positive correlation (0.755) between the extent of ossification and severity of clinical symptoms as patients with complete arcuate foramen reported a higher score in 6-point verbal rating scale for the pain caused by headache.

Morphometric analysis of arcuate foramen

On measuring the dimensions of total 3 complete foramen found in the present study the average antero-posterior diameter was 7.96mm which ranged from 7.4mm to 8.4mm while, the supero-inferior diameter ranged from 4.7mm to 6.5mm with mean diameter of 5.46mm. The measurements were similar to a study done by Unur et al. [23] in which incidence of complete arcuate foramen was studied who reported that their mean supero-inferior and antero-posterior diameters were 5.7 mm (3.7-8.5 mm) and 8.1 mm (5.7-10.0 mm).

Buyuk et al. [24] in their radiological analysis using CT in an orthodontic population reported that on left side complete arcuate foramen was found in 8.3% and incomplete foramen was found in 32.6% of patients. While, on the right side complete foramen was found in 7.2% and incomplete foramen was found in 31.6%. The difference in frequency between left and right was statistically not significant. Their study is similar to the present study as it was found that on the left side incomplete foramen was found in 29.09% of cases and complete foramen was found in 3.63%. While, on the right side 21.81% incomplete foramen was found and 1.81% complete foramen was found.

In the present study on the analysis for laterality in the sample population 27.27% presented with unilateral arcuate foramen while, 14.54% presented with bilateral arcuate foramen. In a study by Gupta et al. [25] the prevalence of unilateral arcuate foramen was 9.09% and bilateral foramen was 10.91%. The difference in results may be due to difference in sample selection as the present study only included symptomatic patients.

Limitations

The present study was cross-sectional and retrospective, further studies should include a control group for better proving the association between the arcuate foramen and headache or migraine.
The present study included only 55 samples and was single centric, further studies should be multi-centric involving a large sample size.

ACKNOLEDGEMENT

We are grateful for Indian Council of Medical Science (ICMR) for supporting the study under ICMR-STS 2020.

Ethics approval and consent to participate – The study was conducted after obtaining approval from Institutional Ethics Committee; Reference No: GMCJ/IEC Approval/48/2021, Date- 2/6/2021. As the study was retrospective, consent to participate was not required.

Consent for publication – All authors has agreed to publish the present study.

Availability of data and materials- the study data was recorded in the achieves of the department and was accessed with the permission of head of department.

Competing interests – No competing interests are present.

Funding – No funding has been provided for the present study.

Authors' contributions –

K Sudip:- Protocol development,Data collection and management,Data analysis,Manuscript writing.

UC Patil:- Data analysis, Manuscript editing.

AP Wasadikar:- Data analysis, Manuscript editing.

Acknowledgements - We are grateful for Indian Council of Medical Science (ICMR) for supporting the study under ICMR-Short Term Studentship (STS 2020).

Authors' information

1. Kumar Sudip - M.B.B.S undergraduate student at Government Medical College, Jalgaon, Maharashtra, India. ORCID - 0000-0001-8066-7099

2. Dr. Utkarsh Chandrakant Patil – Assistant professor in Department of Radiology at Government Medical College, Jalgaon, Maharashtra, India.

3. Dr. Anjali Pravinkumar Wasadikar - Associate professor and Head of Department of Radiology at Government Medical College, Jalgaon, Maharashtra, India.

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Retrospective evaluation of CT-head scans for the association between posterior atlanto-occipital membrane ossification with cervicogenic headache and migraine

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Abstract

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Introduction

Methods

Ethics consideration:-

Inclusion criteria:-

Sample collection:-

Sample analysis:-

Statistical tools and methods:-

Results

Discussion

Declarations

References

Additional Declarations

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Version 1