Introduction
The parietal foramen (PF) is located on both sides of the sagittal suture (SS), near the juncture of the parietal bone’s middle and posterior thirds (1). It transmits parietal emissary veins (EV), arteries to the superior sagittal sinus (SSS), one branch of the occipital artery, and an anastomotic artery from the scalp (2-4). Emissary veins connects the SSS to the veins of the scalp. The EV has no valves, allowing blood to flow in both directions and performing crucial tasks, including balancing the internal pressure and providing cerebral congestion (5). A skull’s diploic veins have a significant association with PF, which may serve as a route for spreading infections from the superficial veins of the skull to the dural venous sinuses (1). The ossification of the parietal bone starts in the 7-8th fetal week at ossification centers and lasts until the seventh fetal month. The parietal notch forms as the ossification decelerates significantly along the midline, and the delayed closure of the parietal notch results in several abnormalities (6). The delayed or incomplete ossification process and closed the third fontanel, frequently leave behind variations like obeliac bones, PF, or parietal fissures (7). Therefore, the neurosurgeon must know the location, number, and size of the PF to avoid inadvertent hemorrhage from injury to the parietal EV (5).
However, few studies have analyzed the possible association between PF, SS, and LS (7). The relationship between the SS, LS, and PF might play a role in identifying various ethnicities or populations. Therefore, the current study examined the location, type incidence, diameter of PF, and the relationship between SS and LS in Turkish adult dry skulls.
Materials and Methods
A cross-sectional morphological and morphometrical study of PF was conducted with 166 Turkish adult dry skulls in 2018-2020. The skulls were obtained from the Department of Anatomy, Akdeniz University Faculty of Medicine.
Compliance with Ethical Standards
The current study was approved by the Ethics Committee of the Akdeniz University Faculty of Medicine (approval date: 26.08.2020 and decision number: 596).
Study Design
The numbers (n), incidences (%), diameters (mm), and types of PF were measured bilaterally by an LCD digital caliper (0-150 mm) (Mitutoyo, Japan). The sex and morphology of the skulls were noted. Twenty-one deformed skulls with pathology and fractures were excluded from the study. The current study comprised skulls with precise SS and LS without parietal bone injury. For morphometric analyses, the shortest distances between the PF-SS, PF-LS, inferior border of median PF (MPF) and Lambda were measured (Figure 1). These measurements were repeated twice to provide a precision estimation. The three used precision estimates were calculated as follows to provide intraobserver precision. The technical error of measurement (TEM), the relative TEM (rTEM), and the coefficient of reliability (R) were all used in this research (8-11).
Statistical Analysis
SPSS 25 (IBM, United States) was used for analysis, and p<0.05 was deemed statistically significant for all comparisons. For continuous variables, descriptive statistics included mean standard deviation, standard error of the mean, minimum, and maximum, and for categorical variables, percentages (%). Multiple t-tests were used to compare groups with normal distributions.
Results
The R-values of the variables were close to one, indicating that measurements were achieved with an adequate degree of intra-observer accuracy.
Incidence
The incidence of PF was detected at a rate of 74.6% (right) and 74.7% (left). The incidence of PF was 63.3 in males, this rate was 36.7 in females. The incidences of PF on both sides are presented in Figure 2. Bilateral PF was found in 74.65%, and unilateral PF was present in 55.75% of Turkish dry skulls. The MPF was found on the SS in 33.7% of the skull. Five types of PF (absence, single, double, triple, quadruple, and quintet) were recorded (Figure 3).
Distance
The PF-LS was 39.88±1.99 mm (2.91-104.11 mm) on the left side, while the mean distance between PF-LS was 40.69±1.67 mm (6.03-101.24 mm) on the right side. The mean values of PF-LS and the differences between the sexes are presented in Table 1. Their differences were not significant on both sides (p>0.05). The PF-SS was 12.87±1.25 mm (0.26-85.03 mm) on the left side, and it was 11.95±1.21 mm (0.40-83.36 mm) on the right side. PF-SS values on the left side differ significantly according to sex. This value indicates that PF has an asymmetrical distribution (p=0.010, p<0.05). MPF-L was 45.64±3.34 mm. The MPF also differed significantly by sex (p=0.04, p<0.05). The number of PF and PF-LS values do not differ significantly according to the sex on both sides (Table 2).
Discussion
The incidence of bilateral PF (74.65%) was higher than unilateral PF (55.75%) in Turkish adult dry skulls. The incidence of the MPF (33.7%) was found to be higher than in other studies. A comparison of the findings of our study with other studies in the literature is presented in (Table 3). The incidence of PF varies from 50-80% in various populations (3,5,12). Several variants, including PF, may have a different occurrence according to the demographic, origin, and sex (13).
The placement of the PF concerning the SS is crucial for neurosurgeons since the EV might rupture during surgery and result in spontaneous bleeding (5,14). The significant differences in the PF-SS on the left side according to sex should be considered in surgery. It was reported that 32% (calvaria) bilateral, and 35% (calvaria) of them unilateral (1). It has been reported that PF is more often unilateral than bilateral, and it was hardly ever multiple or MPF (15). PF was present on the SS in 5% calvaria (1). The mean incidence of bilateral PF was 41.2%, and unilateral PF was 29.9%, as reported in the literature (1). The data of our study was found to be lower than the de Souza et al. (16) (84.3%, Brazil), Mann et al. (7) (85%, Japan), Liu et al. (17) (82.86%, China), Shmarhalov et al. (18) (85.7%, Ukraine); however, it was higher than Boyd (13) (60%, Scotland), Wysocki et al. (12) (60%, Poland), Murlimanju et al. (19) (55.2%, India), Yoshioko et al. (3) (50%, USA) and Berge and Bergman (20) (30%, unilateral, USA). The incidence of MPF was noted by Mann et al. (7) (0.7%) and Naidoo et al. (1) (3.4%), which were conducted in Japanese, and South African populations. It has been reported that PF is greater in the Australian and New Zealand populations than in other ethnicities (13). There were no age or sex differences between the populations according to the distribution, frequency, and size of PF (13). However, this study revealed that the incidence of MPF was higher (33.7%) than in other studies. This difference between findings may be impacted by shifts in ethnicity, population, location, or intervariability in the same population, or by using criteria for determining the PF (18,20).
The relationship between the PF-SS is crucial for neurosurgical approaches because of the possibility of EV rupture during surgery (19). The shortest distance between PF and SS was 12.87±1.25 mm (0.26-85.03 mm) on the left side, and PF-SS was 11.95±1.21 mm (0.40-83.36 mm) on the right side in the current study. However, our findings were higher than those of Naidoo et al. (1) (4.44-18.2 mm; mean: 9.02 mm), Yoshioko et al. (3) (3-12 mm), and Murlimanju et al. (19) (0.5-15 mm), Halagatti and Sagar (2) (6.6 mm) and Shantharam and Manjunath (5) (2-36 mm). Piagkou et al. (21) asserted that PF-SS was 13.5 mm (right) and 14.6 mm (left) and PF-LS was 36.5 mm (right) and 40.8 mm (left). Similarly, it was found to be 39.88±1.99 mm on the left side and 40.69±1.67 mm on the right side in our study. Shantharam and Manjunath (5) reported that PF was located 7-56.1 mm from the Lambda. It was found to be 45.64±3.34 mm (range: 9-100.28 mm), and the MPF also differs significantly by sex (p=0.04, p<0.05). It might be due to the mechanical stresses in the vicinity of the PF over the SS and Lambda (7). The size and symmetry of the PF are significant because they may aid radiologists in diagnosing several pathological impairments (20). Safe radical surgery requires a thorough understanding of the morphological differences in the PF and skull vault (20). Failure to recognize this variance might injure the branches of EV and related arteries that have formed around the PF, leading to excessive intraoperative bleeding and sinus thrombosis (21). The mean size of PF was recorded by Yoshioka et al. (3) (0.4-4.3 mm), Shantharam and Manjunath (5) (0.86-5.57 mm), Mann et al. (7) (1.8-2 mm), Naidoo et al. (1) (0.74-3.08 mm), Berge and Bergman (20) (0.67 mm). Similarly, the mean diameter was 1.7 mm (0.6-2.9 mm) in our study. In the literature, the size of the PF less than 0.5 mm or above 1.5 mm has been reported as a rare condition (7). Boyd (13) reported that PF was equal in size on both sides. In about half the cases mean diameter of PF was ≤0.5 mm, PF was >1-5 mm (7%), and their rest were 1 mm. A large PF was typically not linked to a larger EV and most likely resulted from an ossification deficiency in the parietal bones (13). Moreover, a large PF greater than 5 mm likely suggests an abnormal development of the fetal vascular system that may affect both skull and brain development (22).
Reddy et al. (14) claimed that aberrant vascular evolution with enlarged PF (>5 mm) during the fetal development might affect the development of the brain and skull. It has been reported that enlarged PF (foramina parietal permagna, Catlin marks) coexists with a benign calvarial deficiency with a prevalence of 1 in 15,000 to 1 in 50,000 individuals and numerous Wormian bones (14,21,23). Several reports of enlarged PF have been in conjunction with clinical diseases such as cerebral venous and cortical abnormalities, perineural tumors, and skull fractures (5,13,14). It has been reported that enlarged PF reveals a genetic background and carries an autosomal dominant inheritance (21). Although they are asymptomatic, they have been linked to nausea, multiple exostoses, mental retardation, cleft palate, headaches, encephaloceles, vomiting, myelomeningocele, Duane’s syndrome, straight sinus hypoplasia, the persistence of the median prosencephalic vein and falcine sinus, a dilated vein, vascular or cortical malformations of the brain (14,21). In contrast, it has been claimed that small PF had only a minor hemodynamic role. Moreover, the persistence of the lateral margin of the parietal notch may cause a small PF during the development (21). Wysocki et al. (12) stated that sexual dimorphism in PF according to the size of the PF.
Halagatti and Sagar (2) reported that the frequency and situation of PF help in knowing the relationship between sinuses and extracranial veins. Their situation is essential for analyzing the injuries of the scalp and surgery (2). It has been reported that PF is positioned at the posterior one-third of the parietal bone (7). It is situated 83 mm anterior to the Inion, 2 cm in front of the Lambda in newborns, and 2-5 cm in front of the Lambda in adults (3,7). It has been reported that PF is found 3.5 cm anterior to the Lambda and on either side of the SS (2). In our study, similar to the others, PF was present on both sides of the SS or unilaterally and it was located in front of Lambda and LS. Yoshioka et al. (3) reported that PF occurred between the middle meningeal and scalp arteries. They reported scalp anastomosis that gives off a small artery via PF to communicate with the same branches of the middle meningeal artery (55%), and 45% had an anastomosis with pericranial artery through PF (3). It has been indicated that the PF and the skull’s diploic veins had a direct relation (13). This association is likely to be crucial in transmitting the infection to the extracranial part of the skull (13). The risk of injury to the SSS or intraoperative blood loss can be reduced by precisely localizing the PF on radiological evaluation and then carefully obstructing the EV (24). The current findings may aid in safe movements around PF that transmit an arterial channel across the scalp and dura mater covering the SSS.
The PF can show variations concerning its type, number, size, and shape (2,3). Circular, oval, slit-like, and enlarged PFs have been described in the literature (7,15).
Circular, oval, slit-like, and enlarged PFs were also detected in our study. The size of the PF and how far away it is from the midline affect the shape of the PF, and differences may be caused by alterations in the ossification process (18). A slit or V-shaped notch caused by a prolonged ossification process behind the parietal bone and especially in the obelion is known as the sub-sagittal suture or third fontonel (6). According to reports, heterozygous mutations of MSX2, an autosomal dominant gene, cause the enlarged PF and contiguous gene deletion syndrome (Potocki-Shaffer syndrome) with oval deformities of parietal bone (25). The PF often has a well-defined border, which aids the radiologist in distinguishing it from other clinical situations such as lytic lesions and burr holes during surgery (5,14). However, in a study, the margins of PF were not regular due to the presence of a small groove close to the PF (21). The variations in PF might be related to the changes in the embryological development of the parietal bone (3).
It has been revealed that knowledge about the prevalence and location of PF may help neurosurgeons modify the procedures to reduce the injury risk of EV and related arteries (1,26). The early fusion of the SS, excessive bone growth, and aberrant fibroblast growth factor (FGF) might cause craniofacial deformity and osteogenic differentiation (7). More than one PF could be explained by a delayed or incomplete ossification process of the parietal bone or third fontanel. In our study, the presence of more than one PF was detected (n=1-5), this indicates a delayed ossification process. PF has implications for bone biomechanics, suture development, reduced tensile stresses, increased compressive stresses, and transfer of infection to the cerebral cavity (2,7). The other hypothesis that ALX4 is a specific gene for the formation of PF in the deletion syndrome is supported by individuals with 11p11.2 deletion who also have bilateral PF (25).
Additionally, enlarged PF has been recorded in Chinese populations; however, only 16% have a potential third locus on 4q21-q23, which are caused by these mutations (21). We can compare the allometric patterns in various populations thanks to epigenetic variants such as PF, which serve as indicators of embryological processes (4). The variations in PF might provide significant insights into the structure of the human genome and advance our knowledge of the causes of congenital diseases.
Study Limitations
The causes of death, pathology, and neurological or congenital disorders of the measured skulls were unclear. Therefore, we could not establish a correlation between our findings and clinical impairments. Despite these limitations, the study has strengths in emphasizing the possible association between PF, SS, and LS in dry skulls and the differences between the sexes. This relationship between them might play a role in identifying various ethnicities and reducing the surgical complications surrounding the PF.
Conclusion
The significant differences in the PF-SS on the left side according to sex should be considered in surgery. Other findings of the study are the presence of more than one PF and its asymmetric distribution in the skull. This might be due to the delayed ossification process or differences in ethnicity.
Ethics
Ethics Committee Approval: The current study was approved by the Ethics Committee of the Akdeniz University Faculty of Medicine (approval date: 26.08.2020 and decision number: 596).
Informed Consent: Not required.
Peer-review: Internally peer-reviewed.
Authorship Contributions
Concept: O.G., E.O., F.B.Y., Design: O.G., E.O., F.B.Y., Data Collection or Processing: O.G., E.O., Analysis or Interpretation: O.G., E.O., Literature Search: O.G., E.O., Writing: O.G., E.O.
Conflict of interest: No conflict of interest was declared by the authors.
Financial Disclosure: The authors declare that this study received no financial support.