Bony Tunnel Formation Associated with the Distal Segment of the Frontal Branch of the Middle Meningeal Artery

Abstract

The knowledge of certain anatomical variations is fundamental and any surgeon who operates without that knowledge may encounter difficulty during surgery. In this context, there is the middle meningeal artery (MMA) which also engenders considerable clinical interest due to its location. The MMA is predominantly periosteal, irrigating the bone and dura mater. It enters the floor of the middle cranial fossa through the foramen spinosum, travels laterally through a middle fossa bony ridge, and curves anteriorly over the upper-greater wing of the sphenoid where it divides into parietal and frontal branches at a variable point. Occasionally, the distal segment of the frontal branch may pass through a bony tunnel of variable size. To the best of our knowledge, there is no evidence in the current literature on the incidence of this rare bony tunnel. Therefore, we decided to investigate the incidence of this bony tunnel in 85 dry skulls of adults (both genders) belonging to the didactic collection of the Human Anatomy Laboratory of the Universidade de Santa Cruz do Sul, Brazil. All the skulls were examined bilaterally for the presence or absence of the bony tunnel associated with the distal segment of the frontal branch of the MMA. Of the 85 skulls analyzed, the bony tunnel was present on the right side in 1.18% and on the left side in 5.88% ( p  = 0 .045 ). Thus, in the studied sample, there was a significant tendency for this bony tunnel to be formed on the left side.

Introduction

Originating from the maxillary artery, the middle meningeal artery (MMA) is predominantly periosteal, irrigating the bone and dura mater. It enters the floor of the middle cranial fossa through the foramen spinosum, travels laterally through a middle fossa bony ridge, and curves anteriorly over the upper-greater wing of the sphenoid where, at a variable point, it divides into the parietal and frontal branches. ^{1 2 3 4 5 6}

The parietal branch of the MMA follows the posterior–superior direction and branches within the posterior aspect of the skull. The frontal branch of the MMA crosses the greater wing of the sphenoid and follows the superior aspect of the sphenoid and then curves posteriorly through the parietal bone toward the apex of the skull. ^{2 3 4 5}

The proximal segment of the frontal branch may be located in a bony tunnel and thus be particularly susceptible in tearing when the skull fractures. ^{4 7 8} In addition, occasionally, the distal segment of the frontal branch may traverse a bony tunnel of variable size. However, the incidence of this intermittent bony tunnel in the distal segment of the frontal branch of MMA is not reported in the literature.

Due to its anatomical peculiarity, the MMA has been described ⁶ as being comparatively exposed in the temporal region which makes it vulnerable to injuries to the outer skull that result in epidural bleeding or the formation of a posttraumatic pseudoaneurysm.

Given that several studies have shown that detailed knowledge of the morphological organization of MMA and of some unusual tunnels in the skull may be very important clinically, ^{4 6 8 9 10 11 12} we decided to investigate the bilateral incidence of the bony tunnel associated with the distal branch segment of the MMA in dried adult human skulls.

Methodology

In this study, 85 dry skulls from adults (both genders) belonging to the didactic collection of the Human Anatomy Laboratory of the University of Santa Cruz do Sul (UNISC), Rio Grande do Sul, Brazil, were analyzed. None of the skulls presented any evidence of bone pathology or deformation. The research ethics committee of UNISC approved this research project (Registration number: 176355).

The skulls were analyzed bilaterally for the presence or otherwise of the bony channel associated with the distal portion of the frontal branch of the MMA ( Fig. 1 ). All statistical analyzes were performed using GraphPad Prism 5.0 software (Graphpad Software, Inc., U.S.A.). The Student's t -test was used for paired samples (a p value of 0.05 or less was considered significant). This test can be used in situations where the variables are dichotomous (0, absence or 1, presence) because the average of these variables is equivalent to the proportion of occurrence of the event of interest (in this case, the occurrence of the tunnel). Tunnel length (mm) was measured with the aid of a digital caliper (DIGIMESS, São Paulo, SP, Brazil).

Fig. 1.

Internal view of the skull ( A ) with emphasis on the bony groove of the distal segment of the frontal branch of the middle meningeal artery ( B ). Image ( B ), the bony tunnel formation (weaker dotted line) can be seen in continuity with the bone sulcus (stronger dotted lines) of the frontal branch of the middle meningeal artery.

Results

The analysis of 85 skulls revealed the bony tunnel was present on the right side in one skull (1.18%; length = 19.3 mm) and on the left side in five skulls (5.88%; length = 25.4 ± 17.5 mm; p  = 0 .045 ). Only one of the analyzed skulls presented the bony tunnel bilaterally. Thus, in the studied sample, there is a tendency for the formation of the bony tunnel associated with the distal segment of the frontal branch of the MMA to be presented on the left side. In our observations, we found no indication of any pathology associated with these anatomical variations.

Discussion

Although many studies have pointed out that the complex embryological development of the MMA may lead to numerous variations, ^{13 14} we failed to find any description in the medical literature that presents data similar to ours and thus could be directly confronted with our results. However, we believe that the explanation for the formation of this intermittent bony tunnel may be related to the embryological association that exists between the skull/dura mater and the MMA.

Therefore, based on classical embryological description ^{15 16 17 18 19} of the skull/dura mater and the MMA, we will present some aspects that may shed some light on the formation of this intermittent bony tunnel associated to the distal segment of the frontal branch of the MMA:

Skull/Dura Mater

The skull is divided into the neurocranium which is the portion that surrounds the brain and the viscerocranium, the part in which the facial bones develop. The neurocranium itself is subdivided into: (1) the bones of the base (chondrocranium) which undergo endochondral ossification (i.e., they pass through a cartilaginous stage) and (2) those membranous or flat bones which ossify directly and at no stage consist of cartilage.

Developmental landmarks begin with stage XI (2.5 to 4.5 mm CR  =  crown-rump), when the otic plate is visible externally and marks the position of the future temporal bone. During stage XII (3 to 5 mm CR) this plate transforms into a vesicle. Also at this time, the notochord separates from the neural tube in the cranial and cervical areas with the rostral portions of notochord marking the boundary between the future sphenoid and occipital bones. The mesodermal condensations around it, referred as prechordal and parachordal, are destined to differentiate into most major bones in the base of the skull.

The first chondrification begins during stage XVII (11 to 14 mm CR) in both the basiocciput and the body of the sphenoid. This process of chondrification continues rapidly, and by stage XX (18 to 22 mm CR), the hypoglossal nerve passes through a chondrified foramen. This is when the first indication of the dura mater is seen within the skull.

The outermost of the three meninges, the dura mater, consists of a thick membrane composed of dense collagen lined with mesothelium. Although the dura of the spinal canal and the skull is continuous, their relationships to associated structures are quite different. Within the spinal canal, the dura mater is not adherent to the vertebrae or intervertebral discs, so that there are both epidural and subdural spaces. The epidural space is filled with fat and a network of veins, whereas the subdural space is obliterated by the adherence of the two moist membranes, the arachnoid and dura mater. Beginning at the level of the foramen magnum, the dura mater adheres to the periosteum of the skull (another collagen-based connective tissue frequently referred to as the outer layer of the dura mater) which lines the cranial bones. Thus, there is no natural epidural space within the skull but a subdural space exists in the same manner as the spinal canal.

Specifically, Lemire et al ¹⁵ offer an explanation for the difference in relationships between cranial and spinal dura mater. Separation of the spinal dura mater from the perichondrium to form an epidural space is necessary to allow movement within the functional articulations between the vertebrae. Within the skull, there is no functional space and the dura mater can remain adherent to the endocranium.

MMA

At the 4th to 5th weeks (stages XIII and XV, 7–9 mm CR) of gestation, the MMA begins as a dorsal branch of the stapedial artery which arises from the hyoid artery derived from the second branchial arch. After passing through the ring of stapes, it divides into two main branches: the maxillofacial that leaves the cranial cavity through the foramen spinosum, and the supraorbital branch that supplies the orbit and the intracranial segment of the MMA anteriorly. ^{16 19}

At the 7th to 8th weeks (stages XX and XXI, 22–24 mm CR) of gestation, the stapedial artery involutes and the remnants become the tympanic branches of the MMA which retains communication with the supraorbital and maxillofacial divisions. Thus the distal portion of the internal maxillary artery forms and communication with the intracranial components of the stapedial system is established (the internal maxillary branch of the external carotid artery becomes recognizable as the stem of the MMA). The branches of the normal adult MMA include a supraorbital branch to the orbit, as well as smaller branches to the trigeminal ganglion, the petrosal branch, and the superior tympanic artery. ^{17 18 19}

Conclusion

Given the proximity of the skull/dura mater (endocranium) and the MMA in the early embryonic period, any abnormal growth, expansion, or variation of the MMA branches during those developmental stages might lead to the formation of grooves or occasionally tunnels on the inner surface of the skull. Our belief in this principle is based on the fact that Lemire et al ¹⁵ describe that after stage XVI, the changes in the bones of the skull are quite intense, mainly in the regions of fontanelles, which present sites of quite active osteogenesis where osteoblasts are found in abundance.

In addition, the distal bony areas of the distal segment of the frontal branch of the MMA are relatively close to the anterolateral fontanelle which in turn presents intense osteogenic activity. Thus, the inner surface of the skull could rapidly remodel and form tunnels by the action of excessively overhanging branches in the distal segment of the frontal branch of the MMA.

Another aspect that supports this reasoning is the fact that specifically, the parietal and temporal bones that comprise the distribution areas of the frontal branch of the MMA only undergo ossification after the formation of the branches of the MMA ¹¹ and thus these bone areas might easily be shaped according to possible variations in the arterial pattern of the frontal branch of the MMA.

Therefore, this sequential embryological development and the close anatomical proximity between the skull/dura mater and the MMA may explain the mechanism by which this tunnel is formed.

Additionally, we do not currently have a plausible explanation as to why there is a tendency for the bony tunnel associated with the distal segment of the frontal branch of the MMA to form on the left side. However, we believe that future studies using more accurate evaluation procedures, such as computed tomography or other in vivo imaging techniques could be performed to verify the existence of this trend.

Moreover, the skulls used in our study belong to an old collection and unfortunately, data about gender and ethnicity were not available. However, these limitations do not change the main goals and results of our analysis, namely, to provide new information and basic knowledge regarding an important intracranial vessel of considerable clinical interest.

According to Kornieieva et al, ⁶ there is a close correlation between the morphological characteristics of the MMA and the individual shape of the skull. Estimating the shape of the skull offers involved specialists valuable information, helping them predict probable types of variability of the MMA and foresee the possibility of the manipulation and risk of iatrogenic trauma at the early diagnostic stage. This is especially important for emergent patients with acute epidural bleeding requiring prompt lifesaving solutions.