Anthropological Science
Online ISSN : 1348-8570
Print ISSN : 0918-7960
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Brief Communication
The relationship between jugular foramen asymmetry and superior sagittal venous sinus laterality
GEORGE J. DIASVIVEK PERUMALCHRIS SMITHJON CORNWALL
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2014 Volume 122 Issue 2 Pages 115-120

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Abstract

The reason for asymmetry of the jugular foramen (JF) size is unclear, with previous suggestions including that handedness may influence development of a larger JF on the ipsilateral side of handedness. Intracranial venous asymmetry has not previously been considered in relation to JF size. We aim to investigate if the asymmetry of the superior sagittal venous sinus (SSVS) drainage is related to JF size. Two hundred and forty-five skulls from collections in Otago, New Zealand (Indian skulls) and Coimbra, Portgual (European skulls) were assessed for JF size and SSVS laterality. Data were analysed to determine relationships between the variables JF symmetry, side of drainage of SSVS (laterality), location of the skull collection, and sex using chi-squared and proportion tests (P < 0.05). Two hundred and forty skulls were included in the final analysis (140 Otago, 100 Coimbra). A significant relationship was seen between larger JF and SSVS laterality, with ipsilateral SSVS laterality and larger JF more frequent (54.6%). Differences were noted between location: Otago had significantly more right-sided combinations (66.4% vs. 38%), Coimbra had significantly more that were equal-sided (10% vs. 4.3%). JF size was significantly different across the samples: a larger right JF was more frequent (60%). There were also significant differences between location: Otago showed a higher incidence of larger, right JF (74.3% vs. 40%), while Coimbra had more that were equal (34% vs. 5.7%). Drainage side of SSVS was different across, but not between, skull locations; sex had no effect on any variable. The findings demonstrate an association between the ipsilateral SSVS drainage laterality and a larger JF, and support previous findings of asymmetry in JF size. Further investigations are necessary using imaging techniques to explore the nature of the association between JF asymmetry and SSVS drainage laterality.

Introduction

Handedness has been, and remains, a subject of interest for anthropologists because of the influence of handedness on culture. The subject of handedness has been widely investigated in many different fields, including how handedness may affect evolutionary trends in fossil remains of endocranial shape (Balzeau et al., 2012) or the relationship between genes and culture (Laland, 2008). Bilateral asymmetry of jugular foramen (JF) size in the skull has been of interest to anthropologists because of a suggested relationship between handedness and asymmetry of these structures (Hrdlicka, 1915; Glassman and Bass, 1986; Glassman and Dana, 1992; Adams et al., 1997). The cause of this observed JF asymmetry has been proposed as being a relationship between JF size and handedness (Adams et al., 1997) or as the ‘pulsations of the right atrium’ (Hrdlicka, 1915; Neuroangio.org) being responsible for the larger JF. Early hypotheses suggested that increased use of the dominant upper limb would increase the mass of musculature of that limb and create a backpressure in the venous system leading to dilation of the sigmoid sinus on the ipsilateral side, resulting in the widening of the foramen (Hrdlicka, 1915). This theory has been supported by the association of hand dominance with increased JF size through examination of patients undergoing cranial computed tomography (Adams et al., 1997); however, it has also been challenged by the findings of two autopsy studies that found no association between handedness and JF size (Glassman and Bass, 1986; Glassman and Dana, 1992). Even though the suggestion of a relationship between handedness and JF size has been critically refuted, little anatomical data exists to suggest an alternative theory for the observed asymmetry in JF size and determination of hand preference from the examination of human bones remains controversial (Iscan, 1998; Blackburn and Knusel, 2006; Jaskulska, 2009).

The morphometry of the JF has been examined previously, with a positive correlation described between large skull volume and large JF (Wysocki et al., 2006; Adejuwon et al., 2011). It is generally accepted that JF size is mostly asymmetrical, with the right JF larger in two-thirds of cases (Figure 1) (Navsa and Kramer, 1998; Hussain Saheb et al., 2010; Hossain et al., 2012); however, the reason for this asymmetry is unclear (Wysocki et al., 2006). Complete absence of the foramen on either side is not reported although a complete unilateral absence of sigmoid sinus with a large inferior petrosal sinus has been previously described (Laff, 1930). A few case studies have described narrowing of the left foramen in pathological cases (Nayak, 2008; Rastogi and Budhiraja, 2010), though this does not explain the asymmetry in JF size observed in the general population.

Figure 1

Jugular foramen asymmetry in a single skull: (A) posterior and superior view; (B) inferior and anterior view. JF, jugular foramen; FM, foramen magnum; OC, occipital condyle.

The JF is located in the base of articulated skull, immediately posterior to the carotid canal. It is reported as the most complex foramen of the skull base, both containing and surrounded by important neurovascular structures. Anatomically, the JF is commonly divided into three compartments. The anterior compartment transmits the inferior petrosal sinus and the glossopharyngeal (IX) cranial nerve, the middle the vagus (X) and the accessory (XI) cranial nerves, and the posterior compartment contains the sigmoid sinus, the meningeal branches of occipital and ascending pharyngeal arteries, and small emissary veins (Standring, 2008) (Figure 2). The overall arrangement is that the cranial nerves are medial to the internal jugular vein (Caldemeyer et al., 1997); the JF transmits the termination of sigmoid sinus that continues as the internal jugular vein from the superior jugular bulb at the jugular fossa (Standring, 2008).

Figure 2

Schematic drawing of the contents of the right jugular foramen, as viewed from above.

The reason for the observed asymmetry in JF size has not been examined in relation to other asymmetrical venous structures inside the skull. Venous structures are of interest as the junction of the sigmoid sinus with the internal jugular vein occupies the largest portion of cross-sectional area in the JF, indicating the potential for a relationship to exist between asymmetrical venous structures inside the skull. One of the most common intracranial venous asymmetries is the lateral passage of the largest dural venous sinus, the superior sagittal venous sinus (SSVS). The majority of forebrain superficial veins drain into the SSVS (Beards et al., 1998; Brockman et al., 2012); it is located in the sagittal plane at the superior border of the falx cerebri running anterior to posterior from the crista galli of ethmoid bone to termination in the transverse sinus (Figure 3). The SSVS is described as terminating in (draining into) the right transverse sinus in the majority of individuals (Browning, 1953; Ayanzen et al., 2000; Alper et al., 2004); the transverse sinus then passes anterolaterally to become the sigmoid sinus, then turning medially and passing anteriorly to enter the JF and become the internal jugular vein.

Figure 3

Anterior and superior view of the internal surface of the occipital bone from a skull with a horizontal craniotomy showing the groove for the superior sagittal and transverse sinuses. SSS, groove for superior sagittal venous sinus; TS, groove for transverse sinus; IOP, internal occipital protuberance.

Interestingly, the transverse sinuses are often of unequal size and sometimes one is absent (Beards et al., 1998; Ayanzen et al., 2000; Alper et al., 2004). It has also been noted that the transverse sinus with the more direct connection to the SSVS is larger (Mas et al., 1990); it is therefore plausible that the higher volume of cerebral venous drainage via SSVS connection to a larger transverse sinus may consequently necessitate a larger JF on the ipsilateral side. This would suggest that a larger JF could be related to the side of drainage of the SSVS. Identifying the location of the SSVS in human skulls is possible as a visible and palpable groove apparent on the internal surface of the frontal, parietal and occipital bones in relation to the sagittal suture. In addition, the side of drainage is clearly visible on the inner surface of the occipital bone adjacent to internal occipital protuberance. Similarly, the relative capacity of the JF is easily identified through observation. This study aims to examine the relationship between the side of drainage of the SSVS and the size of the JF in order to provide a possible anatomical explanation for the asymmetry in JF size in humans.

Methods

The bony landmarks corresponding to the JF and SSVS were examined in 245 dry adult skulls. The skulls were obtained from two different locations: Indian skulls were accessed from the Department of Anatomy Museum, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand (n = 145), and European skulls from the International Exchange Collection from the Anthropology Museum in the University of Coimbra, Portugal (n = 100). The Coimbra collection contained information including sex; the sex of the Otago collection had been predetermined by biological anthropologists using sex-specific morphological characteristics such as orbit shape, supraorbital ridge, zygomatic and temporal lines, and external occipital protuberance morphology. Exclusion criteria were any evidence of trauma or other lesions (e.g. disease). Institutional ethical approvals were obtained for the study.

The Otago skulls had horizontal craniotomies (Figure 3) and were assessed by direct observation and palpation. The Coimbra skulls were intact and the intracranial features were observed and palpated through the foramen magnum. Measurement protocols were derived from the methodology of Adams et al. (1997); morphometric data was not recorded.

Two experienced anatomists (G.D., V.P.) examined the skulls and agreement was made regarding two assessment measures. First, the termination of the SSVS and its continuity into a transverse sinus was recorded. This was determined by palpating the groove for SSVS and noting which side of the skull the groove lay relative to the vertical crest superior to the internal occipital protuberance; a demarcation was prominent to indicate its presence. The side of SSVS drainage was recorded as the right side, the left side, on both sides equally, or both sides but unequally. Second, the size of the JF was observed at the inferior opening and note was made of the maximum aperture being on the left, the right, or equal.

Numerical data was recorded using Microsoft Excel (Microsoft Corp., Albuquerque, NM) and analysed using Stata statistical software (StataCorp., College Station, TX); chi-squared tests (test for independence, goodness of fit) and tests for differences in proportion (to determine whether the difference between proportions is significant) with significance at P < 0.05 were used to determine whether correlations existed between drainage laterality of SSVS and the side of the larger JF in the overall population, between skull populations, and between sexes.

Results

In total 240 skulls provided data for inclusion; in five male skulls the location of the SSVS could not be distinguished and the data were removed from the analysis. From the remaining skulls 159 were male, and 81 female. Descriptive data for skull origin, sex, JF size, and SSVS laterality are presented in Table 1.

Table 1 Results of superior sagittal sinus laterality (SSVS) and jugular foramen (JF) side with maximum aperture for Coimbra skulls, Otago skulls, and combined populations.
Group Side SSVS JF
n % n %
Coimbra Female R 26 26 17 17
L 9 9 10 10
Equal 5 5 13 13
Male R 36 36 23 23
L 14 14 16 16
Equal 10 10 21 21
Sub-total 100 100 100 100
Combined sexes R 62 62 40 40
L 23 23 26 26
Equal 15 15 34 34
Total 100 100 100 100
Otago Female R 28 20 30 21.4
L 9 6.4 7 5
Equal 4 2.9 4 2.9
Male R 68 48.6 74 52.9
L 19 13.6 21 15
Equal 12 8.6 4 2.9
Sub-total 140 100 140 100
Combined sexes R 96 68.6 104 74.3
L 28 20 28 20
Equal 16 11.4 8 5.7
Total 140 100 140 100
Combined Female all R 54 22.5 47 19.6
L 18 7.5 17 7.1
Equal 9 3.8 17 7.1
Male all R 104 43.3 97 40.4
L 33 13.8 37 15.4
Equal 22 9 25 10.4
Sub-total 240 100 240 100
Combined sexes all R 158 65.8 144 60
L 51 21.3 54 22.5
Equal 31 12.9 42 17.5
Total 240 100 240 100

Relationship between jugular foramen and superior sagittal sinus

Categorization of results for skull origin, JF size, and SSVS laterality are presented in Table 2. A significant relationship was observed between larger JF size and laterality of the SSVS, with the side of the SSVS positively related to the side of the larger JF. Otago had significantly more right-right combined JF-SSVS than Coimbra (P < 0.01), with a trend observed for Coimbra to have more JF-SSVS combinations that were equal.

Table 2 Results of larger jugular foramen and superior sagittal sinus laterality for Coimbra skulls, Otago skulls, and combined populations. JF, jugular foramen; SSVS, superior sagittal sinus.
Centre Larger JF side SSVS side
SSVS right SSVS left SSVS equal
n % n % n %
Coimbra JF right 38 38 0 0 2 2
JF left 0 0 23 23 3 3
JF equal 24 24 0 0 10 10
Sub total 100 100 100 100 100 100
Otago JF right 93 66.4 5 3.6 6 4.3
JF left 2 1.4 22 15.7 4 2.9
JF equal 1 0.7 1 0.7 6 4.3
Sub total 140 100 140 100 140 100
Combined JF right 131 54.6 5 2.1 8 3.3
JF left 2 0.8 45 18.8 7 2.9
JF equal 25 10.4 1 0.4 16 6.7
Total 240 100 240 100 240 100

Jugular foramen size

JF size was statistically different for the combined study population, a larger right JF being significantly more frequent than either left or equal JF overall. There were significant differences between the two study populations (P < 0.001); with Otago having a significantly higher frequency of larger JF on the right (P < 0.01), and Coimbra having significantly more JF that were equal in size (P < 0.01). There was no difference between sexes for the distribution of JF size.

Superior sagittal sinus laterality

Laterality of the SSVS was significantly different across the study populations (Otago, Coimbra, combined) with SSVS to the right more frequent across all populations. There was no difference in SSVS laterality proportions between study populations. There was no difference between sexes for the distribution of SSVS laterality.

Discussion

Findings from this study demonstrate an association between the laterality of the JF and the SSVS, with a significant relationship between the larger JF and the side on which the SSVS descends intracranially on the occiput. This study details the morphology of bony features on human crania and describes a potential association between two bony landmarks; however, this association by itself does not support causality. This is the first such description of such a relationship, which lends further support to the suggestion that handedness is not related to JF capacity.

Relationship between jugular foramen size and superior sagittal sinus laterality

We found a significant relationship between SSVS drainage laterality and larger JF size with a statistical association found between larger JF and the ipsilateral SSVS groove. Previous examinations of venous asymmetry have shown the right transverse sinus to be larger in 59% of cases (Ayanzen et al., 2000), and the left transverse sinus to be aplastic or hypoplastic in 59% of cases (Alper et al., 2004)— this is congruent with our finding of 54.6% of skulls having a correlation between right-sided SSVS and a larger JF on the right. Significant differences were also observed in the frequency of right SSVS-JF skulls, with Otago skulls having more of this combination than Coimbra. This is most likely explained by the higher number of equal SSVS in the Coimbra population, where a trend was seen for Coimbra to have more equal SSVS-JF skulls. This demonstrates the existence of population differences for these parameters, and these should be taken into account with research that includes different populations of human skulls where JF and SSVS are being examined.

Our results suggest that SSVS laterality and JF size may be related. This is of interest in regards to the potential relationship between JF size and handedness as the SSVS develops in stages throughout gestation (Kopuz et al., 2010) and its laterality is unlikely to be affected by any circumstances post-partum, suggesting that any influence on handedness and JF size would potentially have to be genetic or determined in utero. Statistical evidence in previous work seemsed to support the proposition of the right JF being associated with hand dominance, as right JF are usually larger and most populations are right-handed (Glassman and Dana, 1992; Adams et al., 1997); however, the internal jugular vein, sigmoid and inferior petrosal venous sinuses have no functional relationship with the vessels of the upper limbs and JF capacity is not likely to be affected in this manner.

Jugular foramen size

Results from this study are consistent with findings in other publications, adding to the literature that supports the observation that the right JF is on average larger than the left, and that the proportion of individuals with either larger or equally sized JF may vary between populations. Our results of 60% larger JF on the right side compare favourably with previous recordings of 58.2% (Hossain et al., 2012), 58.6% (Adams et al., 1997), and 64.8% (Hussain Saheb et al., 2010) in Indian, unknown, and Indian skull populations, respectively. Previous findings relating to equal size of JF are also similar to our overall population findings of 17.5%, with congruence between our results and reports of 10.4% (Hussain Saheb et al., 2010), 10.7% (Adams et al., 1997), and 20% (Hossain et al., 2012). However, when we assessed our two populations separately we found a significant variation between the two study groups, with Otago skulls having 5.7% equal JF size and Coimbra 34%. The Coimbra skull proportion of skulls with equal JF size are therefore comparable to the 33.3% reported by Glassman and Dana (1992). This variation between the populations suggests that care should be taken in assuming equal JF sizes in populations where norms have not previously been established.

Superior sagittal sinus laterality

No previous studies have reported on the laterality of the SSVS in human skulls using the methodology in this study. A few studies mention laterality of the SSVS when discussing the laterality of the transverse sinus, to which the SSVS is intimately related (Beards et al., 1998; Ayanzen et al., 2000; Alper et al., 2004). The frequency of approximately 60% in which transverse sinuses are unilaterally hypo- or hyperplasic (Ayanzen et al., 2000; Alper et al., 2004) is in agreement with the frequency of SSVS laterality reported here (65.8%). We found no significant difference in the frequency of SSVS laterality between populations, suggesting that this landmark may be consistent between different populations.

Limitations

Older, post-mortem damaged or well-handled skulls may sometimes be difficult to study effectively given the potential for damage of bony surfaces; however, we only found five skulls where contours did not allow comprehensive analysis to take place. This was mainly due to the faintness of the bony grooves produced by the SSVS and transverse sinuses. Excluding these five skulls from the study data would not have affected the conclusions and statistical analyses. Inter-observer variation was unlikely to have contributed to any bias in the results, as both assessors agreed on study criteria prior to undertaking the assessment and were experienced in this form of osteological examination.

Conclusion

This study describes an association between the laterality of the SSVS and the size of the JF, with a positive relationship between larger JF and the laterality of SSVS passage in the occiput. Other results support previous population data on JF asymmetry, indicating that large JF are more likely to be located on the right side, and that different populations of interest may show different frequencies of morphological features. We also found no difference between sexes within study populations for any feature, or for SSVS laterality between populations. Further studies with imaging techniques such as magnetic resonance venography are required to determine the nature of potential relationships between the laterality of the SSVS and JF size.

Acknowledgments

The authors would like to thank Andrew Gray, biostatistician, for his assistance with the data analysis, and Coimbra University Anthropology Department and University of Otago Department of Anatomy for providing access to the skull collections. The authors declare no conflict of interest.

References
 
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