Enlarged parietal foramina: a rare finding in a female Greek skull with unusual multiple Wormian bones and a rich parietal vascular network
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1 Anat Sci Int (2013) 88: DOI /s CASE REPORT Enlarged parietal foramina: a rare finding in a female Greek skull with unusual multiple Wormian bones and a rich parietal vascular network Maria Piagkou Georgia Skotsimara Elpida Repousi George Paraskevas Konstantinos Natsis Received: 8 December 2012 / Accepted: 1 March 2013 / Published online: 31 March 2013 Ó Japanese Association of Anatomists 2013 Abstract Enlarged parietal foramina ([5 mm) is an extremely rare developmental defect of the parietal bone, which is distinguished from the normal small parietal foramina, as genes associated with this entity have been identified, suggesting that it is hereditary in nature. We describe a dry skull of a 35-year-old female, with enlarged parietal foramina symmetrically situated bilaterally, oval in shape, measuring mm (right) and mm (left) in size. The foramina coexisted with multiple Wormian bones in several sites of the skull. On the inner parietal bone surface, the anterior, posterior and lateral foramina s rims carried grooves, which were continuous with the middle meningeal vessels branches, indicating that a rich vascular network existed around the foramina. M. Piagkou G. Skotsimara E. Repousi Department of Anatomy, School of Health, National and Kapodistrian University of Athens, 75 Mikras Asias Street, Goudi, Athens, Greece G. Skotsimara msko59@otenet.gr E. Repousi elpidarepousi@hotmail.com M. Piagkou (&) Department of Anatomy, Faculty of Medicine, University of Athens, 75 Mikras Asias Street, Goudi, Athens, Greece mapian@med.uoa.gr G. Paraskevas K. Natsis Department of Anatomy, Medical School, Aristotle University of Thessaloniki, P.O. Box: 300, Thessaloniki, Greece G. Paraskevas g_paraskevas@yahoo.gr K. Natsis natsis@med.auth.gr These vascular grooves also notched the external table at the margin of the foramina, which suggests a potential communication between the meningeal and the scalp vessels. In addition, this vascular variation should be taken into consideration when performing surgical interventions in the area, because the large vascular supply to the foramina is a possible source of extensive bleeding. Moreover, the interaction of intracranial and extracranial veins and the fact that the blood flows in them in both directions, as they are valveless, could represent a possible pathway for infections to spread in the cranial cavity. Keywords Catlin marks Emissary veins Foramina parietalia permagna Middle meningeal vessels Wormian bones Introduction Small parietal foramina (1 2 mm) are a normal feature and are located close to the midline on the parietal bone; their incidence is % among adults (Reddy et al. 2000). Usually, they contain emissary vessels (Mann et al. 2009), either valveless veins connecting the superior sagittal sinus to occipital veins or arteries providing an anastomosis between the meningeal and the occipital arteries (Robinson 1962; Currarino 1976). The enlarged parietal foramina (EPF) also called foramina parietalia permagna or Catlin marks, measuring [5 mm, represent a very rare calvarial defect with a prevalence of 1 in 15,000 to 1 in 50,000 individuals (Reddy et al. 2000; Kortesis et al. 2003; Wilkie and Mavrogiannis 2012). In contrast with the small parietal foramina, the EPF are a calvarial defect and not simply the enlargement of the normal apertures of the parietal bone. Thus, the EPF and
2 176 M. Piagkou et al. the small parietal foramina represent separate entities (Currarino 1976; Tubbs et al. 2003; Dharwal 2012). EPF occurs more commonly in males than in females (Wuyts et al. 2000;De Heer et al.2003) and their appearance indicates a genetic background, suggesting that they are inherited as an autosomal dominant trait (Ghassibé et al. 2006; Griessenauer et al. 2012; Wilkie and Mavrogiannis 2012). No satisfactory explanation for their etiology and functional significance has been proposed (Reddy et al. 2000). Although they are asymptomatic (Nikolić and Zivković 2012), and discovered mostly accidentally during skull radiography, they have been associated with severe symptoms such as headaches, nausea, vomiting, mental retardation and anomalies such as cleft lips, cleft palate encephaloceles, myelomeningoceles, craniosynostosis, craniofacial dysostosis, multiple exostoses, Duane s syndrome and cortical or vascular malformations of the brain (Currarino 1976; Reddy et al. 2000; Kortesis et al. 2003; Tubbs et al. 2004; Ghassibé et al. 2006). The presence of EPF has also been associated with the risk of penetrating trauma and traumatic intracranial injury (Edwards et al. 2012). In this case, the EPF are associated with the existence of multiple Wormian bones (WB) in unusual sites of the skull and the development of a rich vascular network derived from the middle meningeal vessels surrounding the EPF and eventually passing through them to the area of the extracranial skull. Case report After examination of 240 Greek dry adult human skulls of both sexes (bone collection at the Anatomy s Departments of National and Kapodistrian University of Athens and Aristotle University of Thessaloniki), we describe a dry skull of a female, 35 years old, with bilateral EPF of oval shape (Fig. 1). There were differences between extra and intracranial measurements of the sagittal diameter (SD) and coronal diameter (CD) of the EPF bilaterally. The CD of the right EPF was 9.3 mm extracranially and 8.3 mm intracranially, and SD was 4.5 mm extracranially and 4.6 mm intracranially. The CD of the left EPF was 9.2 mm extracranially and 7.2 mm intracranially, and SD was 4.9 mm extracranially and 5.2 mm intracranially. The distance between the midpoint of the medial EPF s rim and the sagittal suture was found to be 13.5 mm on the right and 14.6 mm on the left side. The distance between the midpoint of the anterior EPF s rim and the coronal suture was 74.9 mm on the right and 70.0 mm on the left side, and the distance between the midpoint of the posterior EPF s rim and the lambdoid suture was 36.5 mm on the right and 40.8 mm on the left side. As far as the sagittal suture is concerned, we observed that the part of it between the EPF was a straight line in Fig. 1 Posterior view of the skull showing the presence of enlarged parietal foramina (EPF) bilaterally contrast to its sections anteriorly and posteriorly to the EPF, which appeared more complex. Mechanical forces in the area of the EPF might result in redistribution of forces in the parietal bone, increasing them near the lambda area and decreasing them in the area between the EPF, resulting in reduced complexity along the sagittal suture (Mann et al. 2009). The EPF coexisted with multiple WB in the lambdoid, coronal, sphenozygomatic, lacrymomaxillary, sphenofrontal and the parietomastoid sutures, in the posterior fontanelle and in the area of the asterion. Two WB were also observed on the frontal bone, intracranially (Figs. 2, 3). The EPF s anterior, posterior and lateral rims were irregular due to the existence of narrow grooves. The majority of the grooves were continuous with the anterior and middle branches of the middle meningeal artery (MMA) bilaterally, as shown by the traces of the meningeal branches on the parietal bone. Especially, we observed the orifice of one anterior MMA s branch responsible for the supply of the anterior one-third of the parietal bone bilaterally and two middle MMA s branches on the right and three on the left side, which supplied the posterior twothirds of the parietal bone. During their course and ramification on the parietal bone, these main branches give additional collateral branches towards the EPF, which eventually surround them. In addition, it is remarkable that the collateral branches anastomose (Fig. 3). From the external view of the skull, the grooves notched the external table at the EPF s margin, and thus it is possible that the intracranial arterial branches converging on the EPF eventually pass through them and emerge extracranially. Unfortunately, the course of these branches after their emergence via the EPF cannot be determined due to the lack of arterial traces on the parietal bone, but it is possible
3 A case of enlarged parietal foramina 177 Fig. 2 The existence of multiple Wormian bones (WB) indicated by arrows and asterisks. a In the left coronal suture, 8 WB. b In the right coronal suture, 9 WB. c In the left sphenozygomatic suture, 2 WB. d In the left lambdoid suture, 2 WB. e In the right lambdoid suture, 6 WB. f In the posterior fontanelle, 1 large WB. g In the left lacrimomaxillary suture, 1 WB. h In the right lacrimomaxillary suture, 1 WB. i Intraorbitally, on the left side, 3 WB 1 in the sphenofrontal and 2 in the sphenozygomatic sutures. j On the right side, 3 WB, 1 in the parietomastoid suture and 2 in the asterion. k Intracranially, 3 WB in the right sphenofrontal suture and 2 WB on the frontal bone on the left side. l Intracranially, on the left side, 5 WB, 1 in the lambdoid suture and 4 in the asterion
4 178 M. Piagkou et al. Discussion Fig. 3 Lateral view of the inside of calvarium and skull base showing the rich vascular supply from the middle meningeal artery (MMA) branches to the EPF. R Right side, L left side, a anterior, m middle, p posterior, ma middle anterior, mm middle median, mp middle posterior MMA s branches that these branches supply blood to extracranial tissues and/or even anastomose with the scalp arteries. Typically, the middle meningeal veins (MMV) accompany the MMA s branches in their grooves (Stallworthy 1932). Therefore, along with the arterial network around the EPF, a venous network draining the adjacent tissues coexists. In addition, MMV s branches also possibly accompany the MMA s branches via the EPF and emerge extracranially, possibly draining into the scalp veins. Communication between the meningeal and diploic veins has been reported previously (O Rahilly 1963). We observed deep grooves created by the diploic veins, intracranially, near the EPF s medial rim. We did not observe any communication between the middle meningeal and the diploic veins. EPF are believed to be variable expressions of a calvarial ossification disorder, which do not derive merely from the enlargement of small parietal foramina (Currarino 1976; Dharwal 2012). Developmentally, the parietal bone s ossification begins during the 7th or 8th fetal week from ossification centers and the ossification process is not usually completed until the 7th fetal month. The ossification slows distinctly around the midline, causing the formation of the parietal notch, and this delayed closure produces numerous anomalies (Currarino 1976). EPF arise from one large central defect from ossification failure in both parietal bones (Kortesis et al. 2003). At birth, there is a midline ossification deficit, which, until the 2nd year of life is transformed in two distinct foramina, the EPF, due to the appearance of ossification islets (Currarino 1976). In contrast, small parietal foramina are possibly the result of persistence of the most lateral aspect of the primitive parietal notch rather than an ossification disorder (Wilkie et al. 2000). The fact that EPF and small parietal foramina are separate entities, apart from their different developmental genesis, is also confirmed by the fact that, in one study, the EPF coexisted in a single skull with normal small parietal foramina (Tubbs et al. 2003). In our case, we did not observe the existence of both EPF and normal parietal foramina. EPF are usually inherited as an autosomal dominant trait, which is expressed in all the family s generations with variable penetrance (Griessenauer et al. 2012). This is explained genetically by loss of function mutations in human homeobox genes MSX2 and ALX4 located at 11p11 and 5q34-35, respectively (Ghassibé et al. 2006; Griessenauer et al. 2012). A possible third locus on 4q21- q23 has also been reported in Chinese families. There have also been reported isolated incidences of EPF, but only 16 % of them are due to these mutations (Griessenauer et al. 2012). WB are the result of an ossification disorder and their pathogenesis may be due to environmental and genetic variations (Sanchez-Lara et al. 2007). The MSX1/2 mutations are a pathway of WB appearance (Roybal et al. 2010). Knowing that WB and EPF reflect an ossification disorder and MSX2 mutations probably exist in these entities, the coexistence of WB and EPF may not be an incidental fact, as they may be associated genetically. The incidence of multiple WB observed among the comparative Greek dry skulls was 1.25 % (3/240), indicating that the condition of multiple WB observed in this skull is very rare in our collection, which supports the possible genetic correlation between the EPF and WB in this case.
5 A case of enlarged parietal foramina 179 Previous studies have also reported that vascular anomalies, such as a persistent primitive falcine sinus (Reddy et al. 2000; Fink and Maixner 2006), the persistence of the median prosencephalic vein (Valente et al. 2004; Mavrogiannis et al. 2006), the hypoplasia of the straight sinus (Reddy et al. 2000; Mavrogiannis et al. 2006) and a dilated vein (Ghassibé et al. 2006), coexisted with the EPF defect. In this case report, a remarkable vascular network had developed around the EPF. Stallworthy (1932) is the only author to have observed a vascular variation similar to that seen here. Coexistence of the EPF with this vascular abnormality is of great clinical importance in surgical interventions in the area. In these cases, unawareness of this variation could result in injury of MMA branches developed around the EPF and thus cause extensive and life-threatening hemorrhage intraoperatively. In addition, in patients with this anatomic variation, surgeons may fail to stop MMA bleeding, such as in cases of epidural hematoma in head traumas and aneurysm ruptures, using the technique of ligating the MMA close to the foramen (Bruner and Sherkat 2008). Furthermore, the observation that the intracranial vascular grooves converge on the EPF and notch extracranially at their margin suggests that blood to extracranial tissues may be supplied by MMA branches and that a potential interaction between the meningeal and scalp vascular systems exists. This has great clinical importance as far as the venous interaction is concerned. Considering that these veins are valveless, i.e., the blood flows in both directions, these interacting veins could represent the pathway for the spread of infections into the cranial cavity. In addition, sacrificing these veins may lead to sinus thrombosis (Mortazavi et al. 2012). Conclusion In conclusion, this paper focuses on the simultaneous presence of three distinct anatomic entities; EPF, WB and the rich vascular network surrounding the EPF that passes through them and emerges at the external cranial surface. It also highlights the clinical importance of this vascular anomaly, which implies many risks intraoperatively, especially when the surgeon is unaware of it. Consecutively, a radiological and angiographic control is suggested for patients known to have an EPF genetic background, in order to avoid the risk of extensive bleeding and thrombosis intraoperatively. Last but not least, the possible interaction between the meningeal and scalp veins suggests an additional route for the spread of infection. Acknowledgments This study has not received any funding support. There was no contribution of other colleagues or institutions. Conflict of interest References None. Bruner E, Sherkat S (2008) The middle meningeal artery: from clinics to fossils. 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