Evaluation of Angular Parameters of Craniocervical Junction and Establishing Their Relevance in the Diagnosis of Basilar Invagination

Abstract

Background

The craniocervical junction (CCJ), composed of the atlas, axis, and occipital bone, is a critical anatomical consideration incorporating vital osseoligamentous and neurovascular structures. Basilar invagination (BI) is one of the most common CCJ anomalies. Elaborative research has been done on different linear craniometric parameters for diagnosing BI, but the role of the angular craniometric parameters is still under research. This study aims to describe a detailed analysis of the angular craniometric parameters in the population of the northern part of India. We also aim to describe the different angular craniometric parameters that are useful in establishing the diagnosis of BI.

Methods

A total of 49 patients who underwent surgery for BI and met the criteria for the required bony landmarks used in the angular craniometric analysis were included in this study. Angular craniometric analysis was also performed for 120 controls who were screened for head and spine injuries following trauma, and subsequent scans showed no sign of radiological abnormalities.

Results

In this study, 49 patients were analyzed, who underwent surgery for BI, of which 67.35% (n = 33) patients were males and 32.65% (n = 16) were females. The values of Boogard's angle (BgA) greater than 145 degrees and foramen magnum angle (FMA) greater than 18 degrees were highly diagnostic of BI, with 99.41 and 100% diagnostic accuracies, respectively. Similarly, the value of the tentorial twinning line angle (TtwA) less than 31.9 degrees was highly diagnostic of BI with diagnostic accuracy of 78.11%. The diagnostic accuracy of the combination of TtwA with BgA (91.12%) and with FMA (91.72%) was higher than that of TtwA alone.

Conclusion

FMA and BgA have excellent diagnostic accuracy for BI. TtwA can also be used for establishing the diagnosis of BI in the congenital occipital bone anomalies and comparison of preoperative and postoperative measurements following the surgical procedure like foramen magnum decompression.

Keywords

craniocervical junction - basilar invagination - Boogard's angle - foramen magnum angle - tentorial twinning line angle

Introduction

The craniocervical junction (CCJ), composed of the atlas, axis, and occipital bone, is a critical anatomical consideration incorporating vital osseoligamentous and neurovascular structures. The foramen magnum (FM) is the largest opening of the occipital bone through which these neurovascular structures pass.[1] The bony anatomy of the CCJ region is extremely complex and associated with enormous diversity in its morphology. The CCJ is affected by numerous congenital anomalies that can cause life-threatening neurovascular deficits. The diagnosis of CCJ pathologies is primarily based on interpretation of different radiological parameters. Evaluation of imaging modalities have increased the diagnostic accuracy of the CCJ pathologies. Basilar invagination (BI) is one of the most common CCJ anomalies.[2] [3] The diagnosis of BI is based on various linear and angular radiological craniometric parameters.[4] [5] [6] [7] [8] [9] [10] Elaborative researches have been made on different linear craniometric parameters for diagnosing BI, but the role of angular craniometric parameters is still under research. Various angles have been studied that are utilized in the evaluation of CCJ anomalies, but significant data regarding their diagnostic value remain inconspicuous.[8] [11] [12] [13] Since cranial angles have immense potential to influence angular geometry of the CCJ and, in turn, the whole of vertebral column, it is of paramount importance to have fundamental knowledge of angular craniometric parameters of the posterior cranial fossa (PCF), FM, and CCJ regions. The human skull differs in its morphology due to environmental, racial, and sexual differences.[14] [15] Interpretation of all the angular craniometric parameters heavily relies on normal reference values in healthy individuals, which vary enormously in different populations due to morphological variations of the skull, selection of different landmarks in craniometric analysis, and imaging modalities. Thus, we need a detailed analysis of the angular craniometric parameters of the PCF, FM, and CCJ regions in a healthy population, which can serve as a reference value. India is a vast country with huge geographical variations. Since there is no such study of angular craniometric parameters in the northern part of India, this study aims to describe a detailed analysis of the angular craniometric parameters in the population of the northern part of India. This study also describes different angular craniometric parameters that are useful in establishing the diagnosis of BI. FM decompression involves the removal of some part of the occipital bone, so postoperatively, these conventional parameters become irrelevant for comparison with preoperative measurements. This study also defines such angular craniometric parameters that remain constant despite any surgical procedure.

Materials and Methods

This retrospective study was done in the department of neurosurgery at a tertiary care center of northern India, between July 2020 and June 2023. A total of 49 patients, who underwent surgery for BI and met the criteria for required bony landmarks used in angular craniometric analysis, were included in the study. Angular craniometric analysis was also performed for 120 controls who were screened for the head and the spinal injury, and the subsequent scans showed no sign of radiological abnormalities. This study was conducted after getting ethical clearance from the local institutional ethical committee.

Imaging Protocol

A computed tomography (CT) scan was performed (as it was easily available at a low cost) using a 128-slice spiral CT scanner (Discovery Ultra, GE). The rotator time was 0.5 seconds with 120 kVp and 200 mA, the slice thickness was 0.625 mm, the slice interval was 0.625 mm, the field of view was 240 mm × 240 mm, and the matrix size was 512 × 512. Radiological assessment was done in all the patients using reconstructed midsagittal images.

Craniometric Evaluation

We used the following angular craniometric parameters to analyze the PCF, FM, and CCJ region (in degrees; [Fig. 1]):

Fig. 1 Midsagittal reconstructed images of the computed tomography scan of the posterior fossa and the craniocervical junction demonstrating various angular craniometric parameters. (A) Basal angle, angle between line connecting the nasion to the tip of the dorsum sellae and the line extending from the tip of the dorsum sellae to the basion. (B) Boogard's angle, angle between the line connecting the tip of the dorsum sellae to the basion and the line from the basion to the opisthion. (C) Nasion–basion–opisthion, angle between the line connecting the nasion, basion, and opisthion. (D) Foramen magnum angle, angle between Chamberlain's line and McRae's line. (E) Clivo-axial angle, angle between the line connecting the tip of the dorsum sellae to the basion extrapolating inferiorly and line between the inferodorsal portions of the axis to the most superodorsal part of the odontoid process extrapolating superiorly. (F) Clivo-palatal angle, angle between lines connecting the tip of the dorsum sellae to the basion and the basion to the posterior pole of the hard palate. (G) Clivo-odontoid angle, angle formed at the intersection of a line connecting the tip of the dorsum sellae to the basion extrapolating inferiorly and the one along the long axis of the odontoid process. (H) Clivo-supraoccipital angle, angle formed between the intersection of the inferiorly extrapolated lines connecting the tip of the dorsum sellae to the basion and the internal occipital protuberance-opisthion (IOP-O) line to the opisthion. (I) Tentorial slope, angle between the line along the tentorium to the IOP and IOP-O line. (J) Tentorial twinning line angle, angle between the line along the tentorium to the IOP and the twinning line.

• Basal angle (BA): Angle between the line connecting the nasion to the dorsum sellae and the line extending from the tip of the dorsum sellae to the tangential surface of the clivus.

• Boogard's angle (BgA): Angle between the line connecting the tip of the dorsum sellae to the basion and the line from the basion to the opisthion.

• Nasion–basion–opisthion (NBO) angle: Angle between the line connecting the nasion, the basion, and the opisthion.

• FM angle (FMA): Angle between the lines connecting the basion to the opisthion and the tip of the hard palate to the opisthion.

• Clivo-axial angle (CXA): Angle between the line connecting the tip of the dorsum sellae to the basion extrapolating inferiorly and the line between the inferodorsal portions of the axis to the most superodorsal part of the odontoid process extrapolating superiorly.

• Clivo-palatal angle (CPA): Angle between the lines connecting the tip of the dorsum sellae to the basion and the basion to the posterior pole of the hard palate.

• Clivo-odontoid angle (COA): Angle formed between the lines connecting the tip of the dorsum sellae to the basion extrapolating inferiorly and the one along the long axis of the odontoid process.

• Clivo-supraoccipital angle (CSO): Angle formed between the intersection of inferiorly extrapolated lines connecting the dorsum sellae to the basion and the internal occipital protuberance (IOP) to the opisthion.

• Tentorial slope: Angle between the line along the tentorium and the line connecting IOP and the tip of the opisthion.

• Tentorial twinning line angle (TtwA): Angle between the line along the tentorium to the IOP and the line connecting the IOP and the tuberculum sellae.

Statistical Analysis

Data entry was done in the Microsoft excel spreadsheet, and the final analysis was done with the use of Statistical Package for Social Sciences (SPSS) software, IBM, Chicago, United States, version 25.0. The presentation of the categorical variables was done in the form of number and percentages (%). On the other hand, the quantitative data with normal distribution were presented as the means ± standard deviation (SD) and the data with non-normal distribution as median with the 25th and 75th percentiles (interquartile range). Data normality was checked by using Kolmogorov–Smirnov test. Comparisons of the variables that were quantitative and not normally distributed in nature were analyzed using the Mann–Whitney U test (for two groups) and the Kruskal–Wallis test (for more than two groups), and variables that were quantitative and normally distributed in nature were analyzed using independent t-test (for two groups) and ANOVA (for more than two groups).

Univariate analysis and multivariate logistic regression was done to find out the most significant angular craniometric parameters that could establish diagnosis of BI. Receiver operating characteristic (ROC) curves were used to define the cutoff values of angular craniometric parameters, which were found significant on multivariate analysis. Binary logistic regression and ROC curve analyses were used to evaluate the diagnostic efficacy of BgA, FMA, and TtwA when assessed in combinations.

Results

In this study, 49 patients, who underwent surgery for BI, were evaluated, of which 67.35% (n = 33) patients were males and 32.65% (n = 16) were females. The age range of the patients was 18 to 70 years, with a mean age of 34.82 ± 10.52 years. The mean age of the controls was 43.5 ± 14.08 years, with 49.17% (n = 59) males and 50.83% (n = 61) females ([Table 1]).

Table 1 Demographic analysis

Demographic characteristics	Patients with basilar invagination (n = 49)	Control group (n = 120)
18–30	15 (30.61%)	21 (17.50%)
31–40	26 (53.06%)	37 (30.83%)
41–50	5 (10.20%)	20 (16.67%)
51–60	1 (2.04%)	27 (22.50%)
61–70	2 (4.08%)	15 (12.50%)
Mean ± SD	34.82 ± 10.52	43.5 ± 14.08
Female	16 (32.65%)	61 (50.83%)
Male	33 (67.35%)	59 (49.17%)

Abbreviation: SD, standard deviation.

Angular Craniometric Evaluation in Patients with BI and the Control Group

The mean values of the different angular craniometric parameters are given in [Table 2]. On univariate analysis of these parameters, measurements of BA (p < 0.0001), BgA (p < 0.0001), NBO (p < 0.0001), FMA (p < 0.0001), and CSO (p < 0.0001) were significantly higher in patients with BI than the control group. Measurements of CXA (p < 0.0001), CPA (p < 0.0001), COA (p < 0.0001), and TtwA (p < 0.0001) were significantly lower in patients with BI than in the control group. However, values of tentorial slope were higher in patients with BI than in the control group, but it was not significant (p = 0.463).

Table 2 Angular craniometric evaluation of the craniocervical junction region and the posterior cranial fossa (univariate analysis)

Angular craniometric parameters	Patients with basilar invagination (n = 49)	Control group (n = 120)	p-value
Basal angle (degrees)	147.99 ± 2.77	125.92 ± 4.41	< 0.0001[a]
Boogard angle (degrees)	156 ± 2.95	136.89 ± 3.39	< 0.0001[a]
Nasion basion opisthion angle (degrees)	174.87 ± 2.43	169.4 ± 2.01	< 0.0001[a]
Foramen magnum angle (degrees)	29.34 ± 3.97	12.88 ± 1.74	< 0.0001[a]
Clivo-axial angle (degrees)	78.9 ± 8.32	145.58 ± 8.78	< 0.0001[a]
Clivo-palatal angle (degrees)	39.02 ± 5.14	60.1 ± 5.76	< 0.0001[a]
Clivo-odontoid angle (degrees)	91.34 ± 9.2	161.19 ± 9.07	< 0.0001[a]
Clivo-supraoccipital angle (degrees)	86.87 ± 3.74	77.6 ± 4.52	< 0.0001[a]
Tentorial slope (degrees)	89.19 ± 4.67	88.5 ± 5.87	0.463[a]
Tentorial twinning line angle (degrees)	31.91 ± 2.53	34.09 ± 2.12	< 0.0001[a]

^a Independent t-test.

On multivariate logistic regression, measurements of the BgA, FMA, and TtwA were significantly associated with the patients of BI ([Table 3]). The ROC curve was analyzed for all the angular craniometric parameters that were found significant in the multivariate logistic regression to extract the cutoff values of the respective angle for diagnosing BI ([Table 4]). ROC curve analysis of the BgA yielded an area under the curve (AUC) of 0.999 (standard error [SE]: 0.00076; confidence interval [CI]: 0.977–1; p < 0.0001; sensitivity: 100%; specificity: 99.17%) with 99.41% diagnostic accuracy ([Fig. 2]). Similarly for the FMA, the AUC was 1 (SE: 0; CI: 0.978–1; p < 0.0001; sensitivity: 100%; specificity: 100%) and for TtwA, the AUC was 0.737 (SE: 0.0456; CI: 0.663–0.801; p < 0.0001; sensitivity: 53.06%; specificity: 88.33%; [Fig. 3]). ROC curve analysis also identified that values of the BgA greater than 145 degrees and FMA greater than 18 degrees were highly diagnostic of BI. Similarly, the value of the TtwA less than 31.9 degrees was highly diagnostic of BI, with a diagnostic accuracy of 78.11% ([Fig. 4]).

Fig. 2 Receiver operating characteristic curve of Boogard's angle (degrees) for predicting basilar invagination.

Fig. 3 Receiver operating characteristic curve of the foramen magnum angle (degrees) for predicting basilar invagination.

Fig. 4 Receiver operating characteristic curve of the tentorial twinning line angle (degrees) for predicting basilar invagination.

Table 3 Angular craniometric evaluation of the craniocervical junction region and the posterior cranial fossa (multivariate analysis)

Variables	Beta coefficient	Standard error	p-value	Lower bound (95%)	Upper bound (95%)
Basal angle (degrees)	0.004	0.002	0.066	0	0.009
Boogard angle (degrees)	0.008	0.002	0.001	0.003	0.012
Nasion basion opisthion angle (degrees)	0.002	0.004	0.543	–0.005	0.009
Foramen magnum angle (degrees)	0.019	0.002	< 0.0001	0.014	0.023
Clivo-axial angle (degrees)	–0.002	0.004	0.69	–0.009	0.006
Clivo-palatal angle (degrees)	–0.001	0.002	0.408	–0.004	0.002
Clivo-odontoid angle (degrees)	–0.003	0.004	0.358	–0.01	0.004
Clivo-supraoccipital angle (degrees)	0.002	0.002	0.293	–0.002	0.005
Tentorial twinning line angle (degrees)	–0.013	0.003	0.0001	–0.019	–0.006

Table 4 Receiver operating characteristic (ROC) curve analysis of angular craniometric parameters

Angular craniometric parameters	Boogard's angle (degrees)	Foramen magnum angle (degrees)	Tentorial twinning line angle (degrees)
Area under the ROC curve (AUC)	0.999	1	0.737
Standard error	0.00076	0	0.0456
95% CI	0.977–1.000	0.978–1.000	0.663–0.801
p-value	< 0.0001	< 0.0001	< 0.0001
Cutoff	> 145	> 18	≤31.9
Sensitivity (95% CI)	100% (92.7–100.0%)	100% (92.7–100.0%)	53.06% (38.3–67.5%)
Specificity (95% CI)	99.17% (95.4–100.0%)	100% (97.0–100.0%)	88.33% (81.2–93.5%)
PPV (95% CI)	98% (89.4–99.9%)	100% (92.7–100.0%)	65% (48.3–79.4%)
NPV (95% CI)	100% (96.9–100.0%)	100% (97.0–100.0%)	82.2% (74.5–88.3%)
Diagnostic accuracy	99.41%	100.00%	78.11%

Abbreviations: AUC, area under the curve; CI, confidence interval; NPV, negative predictive value; PPV, positive predictive value.

ROC curve analysis was again done to analyze the combined diagnostic accuracy of the angular craniometric parameters, which were found to be significant in the multivariate logistic regression ([Table 5]). The diagnostic accuracy of the combination of the TtwA with the BgA (91.12%; sensitivity: 100%; specificity: 87.5%; positive predictive value [PPV]: 76.56%; negative predictive value [NPV]: 100%) and with the FMA (91.72%; sensitivity: 100%; specificity: 88.33%; PPV: 77.78%; NPV: 100%) was higher than that of the TtwA alone. Although the diagnostic accuracy of the combination of the BgA and FMA (99.41%; sensitivity: 100%; specificity: 99.17%; PPV: 98%; NPV: 100%) was equal to the BgA alone but lesser than the FMA ([Fig. 5]).

Fig. 5 Sensitivity, specificity, positive predictive value, and negative predictive value of the combination of Boogard's angle (degrees), foramen magnum angle (degrees), and tentorial twinning line angle (degrees) for predicting basilar invagination.

Table 5 Receiver operating characteristic curve of angular craniometric parameters in combinations

Angular craniometric parameters	Boogard's angle and foramen magnum angle	Boogard's angle and tentorial twinning line angle	Foramen magnum angle and tentorial twinning line angle
Sensitivity (95% CI)	100% (92.75–100.00%)	100% (92.75–100.00%)	100% (92.75–100.00%)
Specificity (95% CI)	99.17% (95.44–99.98%)	87.5% (80.22–92.83%)	88.33% (81.20–93.47%)
AUC (95% CI)	1 (0.97–1.00)	0.94 (0.89–0.97)	0.94 (0.89–0.97)
Positive predictive value (95% CI)	98% (89.35–99.95%)	76.56% (64.31–86.25%)	77.78% (65.54–87.28%)
Negative predictive value (95% CI)	100% (96.95–100.00%)	100%(96.55–100.00%)	100% (96.58–100.00%)
Diagnostic accuracy	99.41%	91.12%	91.72%

Abbreviations: AUC, area under the curve; CI, confidence interval.

Discussion

BI is one of the most common CCJ anomalies, which is characterized by the abnormal flattening of the skull base (platybasia) and the rostral migration of the odontoid process through the FM, leading to compression of the cervicomedullary junction. It is often associated with other developmental anomalies of the occipital bone, atlas, and axis.[16] The diagnosis of BI is based on the radiological evaluation of the linear and angular craniometric parameters. This study deals with the angular craniometric parameters; all of them are based on measurements on the reconstructed CT images.

Traditionally, measurements of the BA were done on plain radiographs, and gradually have been replaced by the updated imaging modalities.[9] [17] Ferreira and Botelho, in their literature review, described that a BA greater 129 degrees is highly diagnostic of platybasia.[18] Presentation of the isolated platybasia is usually asymptomatic,[19] so other different angular craniometric parameters are used to complement the diagnosis of BI. This was evident in our study, as platybasia was significantly associated in the patients with BI but was not diagnostic as concluded in the multivariate analysis. The BgA and NBO angle are the other methods of measuring the flattening of the skull base.[20] [21] [22] [23] [24] Different studies have shown that the BgA is greater in measurement in the patients with BI than in the normal population.[8] [21] [22] [23] Nascimento et al[21] and Baysal et al[22] found that the BgA has the highest diagnostic accuracy among various angular craniometric parameters, with cutoff values for diagnosing BI being greater than 136 degrees and greater than 137.84 degrees, respectively. In this study, the diagnostic cutoff value was greater than 145 degrees, which is higher than the previous studies. The FMA is one of the recently developed angular craniometric parameters to diagnose BI. The mean value of the FMA is usually higher in patients with BI.[25] Nascimento et al identified that an FMA greater than 17 degrees has the optimal diagnostic value regarding BI.[26] In this study, the diagnostic cutoff value for BI was 18 degrees, which is comparable to the previous studies. Other craniometric angles used to complement the diagnosis of BI including the CXA, CPA, COA, and CSO, but the diagnostic accuracies of these parameters remain dubious.[8] [12] [22] [27] [28] [29]

The tentorial slope and TtwA are used to describe the dimensions of the PCF. The tentorium slope is usually decreased in patients with BI.[30] However, in this study, the tentorial slope was slightly greater but not significant. Karagöz et al[23] found that patients with a smaller PCF had lower values of the TtwA than the normal population, but its implication for the diagnosis of BI are not well described in the literature. In this study, the TtwA was significantly lower in the patients with BI, and its value of less than 31.9 degrees was highly diagnostic of BI.

Diagnostic Accuracy of a Combination of Different Angular Craniometric Parameters

Measurements of the BgA and FMA include the identification of the bony landmarks such as the opisthion and basion, which are sometimes not appreciable in the congenital occipital bone anomalies like atlantooccipital assimilation and supraoccipital or basioccipital hypoplasia ([Fig. 6A]). Owing to removal of occipital bone and instrumentation during PCF surgeries, these conventional parameters become irrelevant for comparison with preoperative measurements ([Fig. 6B, C]). Since the TtwA includes identification of the bony landmarks that remain constant in the associated congenital anomalies of the occipital bone or despite any surgical procedure like FM decompression, it can serve as a useful adjunct in such scenarios; however, it carries a lower diagnostic accuracy as concluded in this study. Furthermore, sometimes a single parameter has the tendency to vary in a normal range, so measurement of more than one parameter is necessary to authenticate the results more precisely.[7] [18]

Fig. 6 Midsagittal reconstructed images of the computed tomography scan of the posterior fossa and the craniocervical junction demonstrating (A) atlanto-occipital assimilation (white arrow), which makes it difficult to identify the basion. (B) Preoperative image in which the opisthion is identifiable (white arrow). (C) Postoperative image in which the opisthion in nonidentifiable due to removal of some part and instrumentation (white arrow).

This study shows that the combination of the TtwA and FMA has excellent sensitivity, specificity, and better diagnostic accuracy for BI than the TtwA alone. Therefore, we propose the measurement of the FMA in combination with the TtwA, which lessens the dependency on traditional bony landmarks and improves the diagnostic accuracy of the TtwA for BI. Moreover, the combination of the BgA and FMA has excellent diagnostic accuracy for BI, which is comparable when both the BgA and FMA are evaluated separately. Therefore, this combination can be used to improve the authenticity of results in diagnosing BI where these landmarks are easily identifiable.

Limitations

The retrospective nature of the study, with a small sample size, makes it biased. Lack of assessment of interobserver variability in our study was another limitation. However, the study lays the foundation for further prospective studies regarding the relevance of these parameters in the diagnosis of BI.

Conclusion

Values of the FMA greater than 18 degrees, BgA greater than 145 degrees, and TtwA less than 31.9 degrees are significantly accurate for establishing the diagnosis of BI. The combination the FMA and TtwA can be used to establish the diagnosis of BI more accurately in the conditions where traditional landmarks are not easily identifiable. However, the combination of the BgA and FMA has excellent diagnostic accuracy for BI, where these landmarks are easily identifiable.

Conflict of Interest

None declared.

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Publication History

Article published online:
21 May 2025