Osseous Variations of the Hypoglossal Canal Area Published: 2009.03.01 Authors’ Contribution: Georgios K

Home , Hypoglossal canal, Jugular tubercle

Received: 2008.01.08 Accepted: 2008.03.31 Osseous variations of the hypoglossal canal area Published: 2009.03.01 Authors’ Contribution: Georgios K. Paraskevas1ADE, Parmenion P. Tsitsopoulos2BEF, A Study Design Basileios Papaziogas1AC, Panagiotis Kitsoulis1CD, Soﬁ a Spanidou1D, B Data Collection 2 C Statistical Analysis Philippos Tsitsopoulos AD D Data Interpretation E Manuscript Preparation 1 Department of Human Anatomy, Aristotle University of Thessaloniki, Thessaloniki, Greece F Literature Search 2 Department of Neurosurgery, Hippokration General Hospital, Aristotle University of Thessaloniki, Thessaloniki, G Funds Collection Greece

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Summary

Background: The hypoglossal canal is a paired bone passage running from the posterior cranial fossa to the na- sopharyngeal carotid space. Hyperostotic variations of this structure have been described. Material/Methods: One hundred sixteen adult cadaveric dried skull specimens were analyzed. Several canal features, dimensions, and distances relative to constant and reliable landmarks were recorded. Results: One osseous spur in the inner or outer orifi ce of the canal was present in 18.10% of specimens (42/232). Two or more osseous spurs were evident in 0.86% of specimens (2/232). However, complete osseous bridging, in the outer or inner part of the canal, was evident in 19.83% of specimens (46/232). Osseous bridging extending through the entire course of the canal was visible in 1.72% of the specimens (4/232). The mean lateral length of the canal was 10.22 mm, the mean medial length was 8.93 mm, the mean transverse and vertical diameters of the internal orifi ce were 7.44 mm and 4.42 mm, respectively, and the mean transverse and vertical diameters of the external orifi ce were 6.15 mm and 3.91 mm, respectively. The mean inclination of single hypoglossal canals was 42.3° and 32.4° on the right and left side, respectively. Conclusions: A detailed and accurate evaluation of the hypoglossal canal topographic anatomy with regard to specifi c, standard osseous landmarks was performed. Additional data with respect to several morphologic features of the hypoglossal canal area also was obtained. Results of this study provide important information that will enable effective and reliable surgical intervention in the area of the hypoglossal canal.

key words: hypoglossal canal • anatomy • morphology • surgical approaches • skull base • jugular tubercle

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Author’s address: Georgios Paraskevas, Department of Human Anatomy, Aristotle University Medical School, P.C: 54124, P.O. Box: 300, Thessaloniki, Greece, e-mail: [email protected]

Current Contents/Clinical Medicine • IF(2007)=1.607 • Index Medicus/MEDLINE • EMBASE/Excerpta Medica • Chemical Abstracts • Index Copernicus BR75 Basic Research Med Sci Monit, 2009; 15(3): BR75-83

BACKGROUND ed with an electronic goniometer. In cases of a double hypoglossal canal, the inclinations of both canals, the length The hypoglossal canal is a bony canal located in the oc- of the septum in partially divided hypoglossal canals, and cipital bone. It lies in the epiphyseal junction between the the distances between the medial and lateral internal ori- basal portion and the jugular process of the occipital bone fi ces of both canals were also recorded with the use of an [1,2]. Variations of the hypoglossal canal are not uncom- electronic goniometer and an electronic digital caliber. mon. Different types, such as bridging and double canals, Finally, associations of partially and totally divided hypo- have been reported, and several attempts have been made glossal canals with adjacent structures, such as jugular fo- to describe them thoroughly [3,4]. ramen bridging, the posterior condylar canal, and occipital condyle morphology, were registered. Differences were Tumor lesions of the skull base in this area were considered measured and analysed using t-test and the level of signifi - to be inoperable not long ago. The surgical approaches are cance was set at p<0.05. technically demanding and complicated, and removal of the lesions is always problematic. However, the introduction of RESULTS advanced microsurgical tools (high-speed drills, suction-ir- rigation devices, microinstruments, etc) has improved re- Two hundred thirty-two hypoglossal canals were examined section and curability of these lesions [2,5,6]. from a total of 116 skulls. The skulls were from 62 men and 54 women. The position of the hypoglossal canal was con- To identify the exact osseous characteristics and topograph- sistently located in the occipital bone just anterior, inferi- ic relations between the canal and adjacent structures rel- or, and slightly medial to the anterior-inferior edge of the ative to stable and reliable anatomic landmarks, we exam- jugular foramen. The canal extended slightly anteriorly in ined variability in the morphology of the hypoglossal canal an inferior-medial to superior-lateral direction. in a large number of specimens. A second aim of this study was to investigate the association of specifi c canal types with Osseous variations in the hypoglossal canal were identi- neighboring anatomic structures. Clinical aspects regarding fi ed (Table 1). One osseous spur located either in the in- surgical intervention in this area are discussed. ternal or external orifi ce of the canal (type 2) was present in 42 canal specimens (18.10%; Figure 1A). Two or more MATERIAL AND METHODS osseous spurs (type 3) were visible in 2 canal specimens (0.86%; Figure 1B). Complete osseous hypoglossal bridg- One hundred sixteen dried skulls from patients aged 20–80 ing of the internal or external portion of the canal (type years at the time of death were used in this study. The 4) was evident in 46 canal specimens (19.83%; Figure 1C). material examined included skulls from the collection Finally, complete osseous bridging (double canal) extending of the Department of Anatomy of Aristotle University of along the entire canal (type 5) was found in 4 sides (1.72%; Thessaloniki. All skulls were from white patients. Data were Figure 1D). Type 1 corresponds to a single canal according collected from both male and female specimens because to the classifi cation of Hauser and De Stefano [3], and in slight sex differences in the incidence of anterior condylar the present study was found in the majority of specimens canal variations have been reported [7,8]. The occipital (59.49%) (Table 1). bones were checked carefully to ensure that they contained the occipital condyle and that the hypoglossal canals were Measurements of canal inclination in nondouble hypoglos- intact bilaterally. Surrounding bony structures were metic- sal canals relative to the midsagittal plane and the distance ulously identifi ed and preserved. The hypoglossal canals of the center of the internal orifi ce of double hypoglossal were clearly delineated. canals from the midpoint of the condylar portion of the occipital bone are shown in Table 2A and Figure 2. In addition, Several measurements were obtained. First, the exact mor- measurements of canal inclination in cases of divided hypo- phology of the hypoglossal canals was recorded. Dimensions, glossal canals (type 4 and type 5) were obtained (Table 2B). such as the lengths of the lateral and medial walls and the The mean transverse and mean vertical diameters of the in- transverse and vertical diameters of the internal and exter- ternal orifi ce were 7.44 mm and 4.42 mm, respectively (Table nal orifi ces of the canal, were calculated with the aid of an 3A). The mean transverse and mean vertical diameters of the electronic digital caliper. The relative position of the in- external orifi ce were 6.15 mm and 3.91 mm, respectively. In ternal orifi ce of the canal with respect to the adjacent sta- cases of partially and totally divided hypoglossal canals, the ble anatomic landmarks, thus the distance of the internal mean medial length was 9.56 mm, the mean lateral length orifi ce of the canal from the midpoint of the the condylar was 11.64 mm, the mean transverse and vertical diameters portion of the occipital bone, the vertical distance from the of the medial internal orifi ce were 4.51 mm and 5.12 mm, internal orifi ce to the lateral border of the foramen mag- respectively, the mean transverse and vertical diameters of num and to the medial border of the sigmoid sulcus, and the lateral internal orifi ce were 2.71 mm and 2.62 mm, re- the distance to the ipsilateral edge of the transverse diam- spectively, and the mean transverse and vertical diameters eter of the foramen magnum were also measured with an of the external orifi ce were 7.12 mm and 6.51 mm, respec- electronic digital caliper. Similarly, the distance from the tively (Figure 3; Table 3). external orifi ce of the hypoglossal canal to the midpoint of the anterior border of the foramen magnum and the verti- The mean medial length of the canal was 8.93 mm, whereas cal distance of the external orifi ce from the lateral border the mean lateral length was 10.22 mm (Table 3A, Figure 4). of the foramen magnum was registered with the aid of an The mean vertical distance from the center of the internal electronic digital caliper. The inclination of the hypoglos- orifi ce of the canal to the lateral border of the foramen mag- sal canal relative to the midsagittal plane also was record- num was 7.41 mm, to the medial border of the sigmoid sul- BR76 Med Sci Monit, 2009; 15(3): BR75-83 Paraskevas GK et al – Osseous variations of the hypoglossal canal area

Table 1A. Variations in the form of the hypoglossal canal according to Hauser and De Stefano [3]. BR Type Characteristics 1 No traces of division. Simple canal

2 Traces of division. One osseous spur expressed either marginally at the inner or outer orifi ce of the canal or inside it

3 Traces of division. Two or more osseous spurs expressed anywhere along the canal

4 Complete osseous hypoglossal bridging expressed in the internal or external portion of the canal

5 Complete osseous hypoglossal bridging extending along the entire canal

Table 1B. Frequencies and percentages of variations of hypoglossal canal morphology in 116 skulls in the present study.

Type 1 2 3 4 5 n%n%n%n%n% R/L 64/74 27.59/31.90 20/22 8.62/9.48 1/1 0.43/0.43 28/18 12.07/7.76 3/1 1.29/0.43 T 138 59.49 42 18.10 2 0.86 46 19.83 4 1.72 R – right; L – left; T – total; hypoglossal canal types are according to Hauser and De Stefano [3].

Figure 1. (A) Type 2 hypoglossal canal. One osseous spur is evident in the internal orifi ce of the canal. (B) Type 3 hypoglossal canal. Two bony spurs are visible in the internal orifi ce of the canal. (C) Type 4 hypoglossal canal. Complete osseous bridging in the internal orifi ce of A B the canal. (D) Type 5 hypoglossal canal. Complete osseous bridging extends along the entire canal. Double canal. HC: hypoglossal canal.

C D

cus was 9.28 mm, and the mean distance to the ipsilateral men magnum was in each measurement greater than the edge of the transverse diameter of the foramen magnum corresponding distance on the right side, but there was not was 8.91 mm (Table 4A, Figure 5). The canals were com- statistically signifi cant difference (p<0.05). pletely surrounded by cortical bone in the vast majority of patients (85.78%). Excluding complete septa of type 5 hypoglossal canals and bridges of the internal orifi ce of the hypoglossal canal, we Measuring the distance between the external orifi ce of the found than in most cases (91.38%) the length of the sep- hypoglossal canal and the midpoint of the anterior border tum extended from 40% to 60% of the total length of the of the foramen magnum, we found the mean value on the hypoglossal canal (Table 5A; Figure 5). In addition, we cal- right and the left sides to be 15.48 mm and 15.99 mm, re- culated the distance between the medial and lateral internal spectively (Table 4B). The mean value of the vertical distance orifi ces of the canal and found that the mean value on the of the external orifi ce from the lateral border of the fora- right and the left sides was 3.71 mm and 5.17 mm, respec- men magnum on the right and the left sides was 8.05 mm tively (Table 5B). We also found that a posterior condylar and 8.35 mm, respectively. We recorded that on the left side, canal coexisted in 54% of the examined double hypoglos- the distance between the external orifi ce of the hypoglossal sal canals (type 4 and type 5) (Figure 6A), jugular foramen canal and the midpoint of the anterior border of the fora- bridging existed in 42% of double canals (Figure 6B), and BR77 Basic Research Med Sci Monit, 2009; 15(3): BR75-83

Table 2A. Measurement of non-double hypoglossal canal inclinations and distance of the internal orifi ce of non-double canals from the midpoint of the condylar portion of the occipital bone.

Inclination Distance (grade) (mm) Right Left Mean 42.3 32.4 1.46 SD 5.4 3.6 0.44 Maximum 49.9 37.2 2.08 Figure 2. Inclination of the longitudinal axis of the hypoglossal canal Minimum 35.8 28.1 –0.15 (a) relative to the midsagittal plane (b). Distance from the center of the internal orifi ce of the hypoglossal canal Indicates that the center of the internal orifi ce of the hypoglossal from the midpoint of the condylar portion of the canal (c). canal was found inferior to the midpoint of the condylar portion of the HC – hypoglossal canal; CL – clivus; TB – temporal bone; occipital bone. SD – standard deviation. FM – foramen magnum.

Table 2B. Measurement of inclination of both canals in cases of partially and totally divided hypoglossal canals (types 4 and 5).

Right Left Mean 34.8° (A) 16.1° (P) 31.2° (A) 14.8° (P) SD 8.4° (A) 4.9° (P) 7.3° (A) 4.1° (P) Maximum 48° (A) 25° (P) 45° (A) 23° (P) Minimum 19.3° (A) 9° (P) 18° (A) 8.5° (P) A – anterior canal; P – posterior canal1. there was an association with the 8-shaped type of occipital condyle, according to the Naderi et al classifi cation [17], in 52% of double canals (Table 5C; Figure 7). Bilateral osseous variations were found in 32 of 116 skulls (27.59%). Figure 3. Measurement of the lateral (L) and medial (M) lengths and Male skulls showed a slight predilection toward types 3, 4, transverse and vertical diameters of the internal (IO) and and 5 compared with female skulls, not being statistically external (EO) orifi ces of the hypoglossal canal. signifi cant. Partially and totally divided canals were found more frequently in the right side. The right side predilection was found to be statistically signifi cant (p<0.05) We measured the inclinations of both canals in cases of divided double hypoglossal canals, fi nding that the anterior DISCUSSION canal formed a greater angle (almost 2-fold) relative to the midsagittal plane compared to the corresponding angle rel- The foramen hypoglossi, or anterior condylar or hypoglossal ative to the posterior canal in 100% of the cases studied. To canal, extends from the posterior cranial fossa to the naso- our knowledge, this is the fi rst report of these values. pharyngeal carotid space. It is formed by several bony structures: the occipital condyles inferiorly, the sphenoid por- According to Rhoton [10], the hypoglossal canal is locat- tion of the clivus superomedially, and the jugular foramen ed above the middle third of the occipital condyle and ex- and jugular process of the occipital bone laterally [1,9,10]. tends posteriorly to anteriorly and medially to laterally. The Its location is inferior, anterior, and slightly medial to the intracranial end of the hypoglossal canal (small oval) is lo- anteroinferior edge of the jugular bulb [2]. The canal ex- cated approximately 5 mm above the junction of the poste- tends ventrally and laterally at a 45° angle to the sagittal rior and middle third of the occipital condyle and approx- plane [11]. In the present study, we accurately determined imately 8 mm from the posterior edge of the condyle. The the range and mean value of non-double hypoglossal ca- average length of the longest axis of the condyle is 21 mm nal inclination, fi nding a mean angle of 42.3° and 32.4° on [10]. Hadley and Shelton [2] estimated the mean length right and left sides, respectively. Apart from the hypoglos- of the simple hypoglossal canal to be between 7.8 mm and sal nerve, the canal also contains a venous plexus, often a 11.2 mm and the mean breadth to be between 3.8 mm and meningeal branch of the ascending pharyngeal artery and 5 mm. These values are in agreement with the results of an emissary vein draining to the transverse sinus [12–16]. Katsuta et al. [11]. BR78 Med Sci Monit, 2009; 15(3): BR75-83 Paraskevas GK et al – Osseous variations of the hypoglossal canal area

Table 3. Measurement of medial and lateral lengths and diameters of internal and external orifi ces of hypoglossal canals. BR A. Cases of single hypoglossal canals (types 1–3) (n: 182; right: 99; left: 82).

Diameter (mm) Length (mm) Internal orifi ce External orifi ce Lateral Medial Transverse Vertical Transverse Vertical Mean 10.22 8.93 7.44 4.42 6.15 3.91 SD 1.81 1.74 1.40 0.93 1.32 1.12 Maximum 14.34 12.12 10.26 6.45 8.18 5.84 Minimum 6.92 5.85 4.61 3.11 3.64 2.11 SD – standard deviation.

B. Cases of divided hypoglossal canals (types 4 and 5) (n: 50; right: 31; left: 19).

Diameter (mm) Length (mm) Medial internal orifi ce Lateral internal orifi ce External orifi ce Lateral Medial Transverse Vertical Transverse Vertical Transverse Vertical Mean 11.64 9.56 4.51 5.12 2.71 2.62 7.12 6.51 SD 1.41 1.71 0.42 6.23 0.62 0.44 0.51 0.93 Maximum 13.23 11.23 5.38 0.74 3.04 3.15 7.73 7.24 Minimum 9.62 7.84 3.94 5.73 1.84 2.16 6.18 5.65 SD – standard deviation.

attempt to determine the relative position of the internal and the external orifi ces of single hypoglossal canals relative to constant and reliable anatomic landmarks (foramen magnum, condylar portion of the occipital bone, sigmoid sulcus) was made. In regard to the external orifi ce of single hypoglossal canals, we calculated the distance to the midpoint of the anterior border of the foramen magnum and the vertical distance to the lateral border of the foramen magnum. We consider that these measurements of relative location of the 2 orifi ces are reliable because they refer to stable anatomic landmarks, whereas the occipital condyle morphology is variable.

Several osseous variations in the form of the hypoglossal canal have been described. Five types can be distinguished: type 1, no evidence of division (typical single canal) (65.4%); Figure 4. Mean vertical distance from the center of the internal orifi ce type 2, one osseous spur located either at the inner or outer of the canal to the lateral border of the foramen magnum orifi ce of the canal or inside it (16.1%); type 3, two or more (a) and to the medial border of the sigmoid sulcus (b). Mean osseous spurs along the canal (2.3%); type 4, complete os- distance to the ipsilateral edge of the transverse diameter of seous bridging either in the internal or external portion the foramen magnum (c). CL – clivus; TB – temporal bone; of the canal (13.1%); and type 5, complete osseous bridg- FM – foramen magnum. ing occupying the entire extent of the canal (3.1%) [3]. Divisions of the canal are generally explained by the fusion of 3 or 4 formerly separated vertebrae that are remnants Naderi et al [17] reported that the intracranial orifi ce of of the intervertebral foramina [3]. The canal morphology the hypoglossal canal was found at the junction of the sec- is strongly linked with the process of occipital chondrifi ca- ond and third quarter of the occipital condyle in more than tion at the stage of a 17-mm embryo and the development 55% of specimens. The extracranial orifi ce of the hypoglos- of the hypoglossal nerve. It is the rates and timing of these sal canal was evident in more than 90% of specimens in the conditions and the opposing process of loss of material that fi rst quarter or at the junction of the fi rst and second quar- defi ne the presence and the extent of canal bridging and ter of the hypoglossal canal [17]. In the present study, an subsequent hyperostotic changes [18]. However, there are BR79 Basic Research Med Sci Monit, 2009; 15(3): BR75-83

Table 4A. Measurement of the vertical distance from the internal Table 5A. Measurement of the length of the septum (Ls), length of orifi ce of the hypoglossal canal to the lateral border of the the lateral wall of the double hypoglossal canal (Lw), and foramen magnum (A), to the medial border of the sigmoid the ratio (Ls/Lw; only for mean values). sulcus (B), and to the distance from the internal orifi ce of the canal to the ipsilateral edge of the transverse diameter Length of septum Length of lateral Ls/Lw of the foramen magnum(C). (mm) wall (mm)

Distance A Distance B Distance C Mean 6.31 11.48 0.55 (mm) (mm) (mm) SD 1.58 0.93 Mean 7.41 9.28 8.91 Maximum 8.78 12.41 SD 0.76 1.02 1.13 Minimum 4.06 9.82 Maximum 8.53 10.76 10.63 Simple bridging of the internal orifi ce and complete septa of type 5 Minimum 6.37 8.07 7.41 hypoglossal canals were excluded. SD – standard deviation. SD – standard deviation. Table 5B. Measurement of the distance between the medial and lateral internal orifi ces of the hypoglossal canal (types 4 and 5). Table 4B. Measurement of the distance of the external orifi ce of the hypoglossal canal to the midpoint of the anterior border Right (mm) Left (mm) of the foramen magnum (A) and the vertical distance of the external orifi ce from the lateral border of the foramen Mean 3.71 5.17 magnum (B). SD 2.11 2.82 Distance A (mm) Distance B (mm) Maximum 6.44 8.33 Right Left Right Left Minimum 1.12 2.21 SD – standard deviation. Mean 15.48 15.99 8.05 8.35 SD 0.84 0.72 1.53 0.81 Table 5C. Association of the type 4 and type 5 hypoglossal canals with various forms of the ipsilateral occipital condyle according Maximum 16.66 17.04 10.38 9.45 to the classifi cation of naderi et al. [17]. Minimum 14.32 14.88 6.31 7.48 Type of Occipital Condyle n % SD – standard deviation. 8-shaped 26 52 Oval-shaped 18 36 accounts in which there are 2 bundles of the hypoglossal nerve with 2 foramina, and both bundles pass through the Triangle-shaped 4 8 same foramen. This has been explained by the formation Ring-shaped 2 4 of dura mater that covers the nerve at the opening, not by the fusion of the occipital somites [19].

Other authors have reported the following incidence for each type of hypoglossal canal: Berry and Berry [7] examined 585 skulls and discovered a double hypoglossal canal in 14.6%. Corruccini [20] found an incidence of 8.3% of hypoglossal bridging in 321 skulls. Lillie [21], in 35 male skulls, reported a 62.1% incidence of single canal, a 19.4% incidence of incomplete partially divided canal, and an 18.5% incidence of double canal on the left side, and a 59.2% incidence of single canal, an 18.5% incidence of incomplete partially divided canal, and a 22.3% incidence of double canal on right side. However, Katsuda et al [11] examined 25 skulls and described the following incidence: type 1, 45%; types 2 and 3, 35%; type 4, 15% to 20%; and type 5, 1% to 3%. In the present study, which represented a sample of the Greek popula- tion, the following was found: type 1, 59.49%; type 2, 18.10%; type 3, 0.86%; type 4, 19.83%; and type 5, 1.72%.

The hypoglossal canal has been described as triple or Figure 5. Measurement of the length of the septum (Ls) and the quadrable in rare cases [19,22]. Poirier and Charpy [23] length of the lateral wall (Lw) of a double hypoglossal canal. BR80 Med Sci Monit, 2009; 15(3): BR75-83 Paraskevas GK et al – Osseous variations of the hypoglossal canal area BR

B A Figure 6. (A) Posterior condylar canal (with a probe in its lumen) coexisting with a double hypoglossal canal. (B) Posterior condylar canal (large arrow) coexisting with jugular foramen bridging (small arrow). HC – hypoglossal canal; FM – foramen magnum; OC – occipital condyle; JF – jugular fossa with jugular foramen.

B A Figure 7. Double hypoglossal canal (A) associated with an 8-shaped type of occipital condyle (B) (arrows). HC – hypoglossal canal, FM – foramen magnum, OC – occipital condyle, JF – jugular fossa with jugular foramen. reported cases in which the canal was divided into 4 parts. glossal canal [25]. Our hypothesis is that a possible distur- This was not confi rmed in the present study. Lillie [21] sug- bance in the process of ossifi cation during occipital bone gests that some of the osseous processes observed in multi- formation may result in the formation of a double hypo- ple canals may represent a secondary ossifi cation in the du- glossal canal, posterior condylar canal, and jugular fora- ral septa extending between the fasciculi of the hypoglossal men bridging. nerve roots rather than remnants of arches of occipital vertebrae. It is also probable that in some cases these divisions We measured, for the fi rst time, the length of the septum, are signifi cant not of division of the nerve, but of vascular excluding the simple bridging of the internal orifi ce and variation. Some of these variations are due to aberrant ves- the complete septum of type 5 hypoglossal canals, fi nding sels and not to division of the nerve. However, the nerve a mean value of 6.31 mm. We studied the possible associa- has also been noted to pass through as 2 separate nerves, tion of type 4 and type 5 hypoglossal canals with the poste- each in a canal of its own [21]. rior condylar canal, jugular foramen bridging, and the morphology of the ipsilateral occipital condyle. We found that The posterior condylar canal appears in approximately 40% the double hypoglossal canals with a relative high frequen- of skulls. It pierces the condylar fossa immediately poste- cy were associated with the posterior condylar canal (54%) rior to the occipital condyle. Occasionally, it transmits an and jugular foramen bridging (42%), whereas 52% of ca- emissary vein, which allows anastomosis of the jugular bulb nals of type 4 and type 5 coexisted ipsilaterally with the 8- or sigmoid sinus with the suboccipital venous plexus [24]. shaped type of occipital condyle, according to the classifi - Jugular foramen bridging, or ponticuli foraminis jugularis, cation of Naderi et al [17]. refers to a bony bridging of the jugular foramen established by contact of the intrajugular process of the temporal bone Although there are differences among races, in most cas- with the bony process of the occipital bone projecting ei- es there is no trace of division of the hypoglossal canal ther from just above or from a site posterior to the hypo- [3,8,21,26]. Several distinct differences between the left BR81 Basic Research Med Sci Monit, 2009; 15(3): BR75-83 and the right sides have been described, with the complete tance of approximately 12 mm. When drilling the upper and incomplete canal division by bony septum to be more posterior portion of the condyle, the posterior condylar frequent on the right side as it is confi rmed by the presenr vein may be a source of bleeding, which can be confused work. In the present study, in type 4 and type 5 hypoglos- with bleeding from the venous plexus of the hypoglossal ca- sal canals, the posterior canal was approximately twice the nal, particularly in canal variants. The jugular tubercle can size of the anterior canal in all specimens studied. It must be identifi ed after exposing the hypoglossal canal [10,31]. be emphasized that the race homogeneity (white caucasian Paracondylar exposure, which provides access mainly to the race) in our work renders our study reliable. posterior margin of the jugular foramen and jugular bulb, can be carried out successfully without drilling of the occip- Tumor lesions in the area of the hypoglossal canal are un- ital condyle [11,32]. The widely used far-lateral transcon- common; however, a detailed knowledge of the anatomy of dylar approach provides exposure to the intracranial and the hypoglossal canal is crucial for the effective treatment of intracanalicular portions of the lesion, although direct ac- the underlying pathology [2,27]. The most frequently report- cess to the hypoglossal canal is not provided, and excision ed tumors in this area are hypoglossal schwannomas, which of extracranial tumor portions requires further neck dissec- arise intracranially and extend through the hypoglossal cation [9,36]. The suboccipital subtonsillar approach allows nal to extracranial spaces [9]. Other diseases involving the for radical tumor removal through a standard craniotomy hypoglossal canal include glomus jugulare tumors, metasta- and allows a direct angle of view without consuming time. ses, myelomas, and, rarely, meningiomas [1]. Lesions in this However, this approach is limited to lesions that extend ex- area were believed to be inoperable until recently. They still tracranially and not too far inferiorly [9]. require advanced neurosurgical technique. However, with the advent of microsurgical tools (microinstruments, high- CONCLUSIONS speed drills, special suction devices, etc) and experienced hands, many lesions are now curable [2,5,6]. We confi rmed the not uncommon presence of several osseous variations in the hypoglossal canal. Several canal di- Several approaches have been suggested for the surgical man- mensions were measured, and their relevance to adjacent agement of these lesions. These include the extended pos- structures was assessed. In addition, the inclination of the terolateral approach, the supracondylar approach, the far- hypoglossal canal relative to the midsagittal plane was mea- lateral transcondylar approach, and the midline suboccipital sured. Finally, the coexistence of a double hypoglossal canal subtonsillar approach [2,5,10,11,28–31]. Some of these have with several adjacent areas was evaluated. These data provide managed to improve the angle of exposure by reducing the useful information that will enable safe and successful sur- amount of brain retraction [32]. Potential disadvantages of gical treatments in the area of the hypoglossal canal. these approaches include mainly prolonged operation time and risk of damage to the vertebral artery, jugular bulb, sig- REFERENCES: moid sinus, and several cranial nerves [33]. The hypoglossal canal can be safely and reliably approached using sever- 1. Voyvodic F, Whyte A, Slavotinek J: The hypoglossal canal: Normal MR al landmarks, depending on the selected approach. During enhancement pattern. Am J Neuroradiol, 1995; 16: 1707–10 surgery, important key points are the drilling of the occipi- 2. Hadley K, Shelton C: Infratemporal fossa approach to the hypoglossal canal: Practical landmarks for elusive anatomy. The Laryngoscope, tal condyle, the lateral mass of C1, and extradural drilling of 2004; 114: 1648–51 the jugular tubercle [10,11,34]. Detection of the locations 3. Hauser G, De Stefano GF: Variations in form of the hypoglossal canal. of the internal and external orifi ces of the hypoglossal ca- Am J Phys Anthropol, 1985; 67: 7–11 nal is an important step for lateral skull base approaches. To 4. Bhuller A, Sapudo JR, Choi D et al: Intracranial course and relations avoid hypoglossal nerve injury, the location and morphol- of the hypoglossal nerve. An anatomic study. Surg Radiol Anat, 1998; ogy of the hypoglossal canal should be determined during 20: 109–12 preoperative surgical planning with the aid of neuroimag- 5. Wen HT, Rhoton Al Jr, Katsuda T et al: Microsurgical anatomy of the transcondylar, supracondylar, and paracondylar extensions of the far- ing studies. The clinician, together with the radiologist, lateral approach. J Neurosurg, 1997; 87(4): 555–85 should carefully study and interpret the available imaging 6. Wanebo JE, Chicoine MR: Quantitative analysis of the transcondylar studies to trace possible osseous variations and to clarify the approach to the foramen magnum. Neurosurgery, 2001; 49: 934–43 exact morphologic features in this area. These data can be 7. Berry AC, Berry RJ: Epigenetic variation in the human cranium. J Anat, further studied, evaluated, and confi rmed intraoperative- 1967; 101: 367–79 ly. Failure to identify a pre-existing hypoglossal canal vari- 8. Berry AC: Factors affecting the incidence of nonmetrical skeletal variation may lead to damage of the hypoglossal nerve. Every ants. J Anat, 1975; 120: 519–35 case should be individualized, and careful interpretation of 9. Tatagiba M, Koerbel A, Roser F: The midline subtonsillar approach to the hypoglossal canal: surgical anatomy and clinical application. Acta preoperative imaging can identify the detailed morphology Neurochir (Wien), 2006; 148: 965–69 of this area and thus, help the surgeon choose and under- 10. Rhoton Al Jr: The far-lateral approach and its transcondylar, supracon- take the appropriate procedure [1,2,35]. dylar, and paracondylar extensions. Neurosurgery, 2000; 47(3 Suppl.): S195–209 Especially when performing the far-lateral approach, con- 11. Katsuta T, Matsushima T, Wen HT et al: Trajectory of the hypoglossal nerve in the hypoglossal canal: Signifi cance for the trancondylar ap- dylar drilling is of major signifi cance. This requires a de- proach. Neurol Med Chir (Tokyo), 2000; 40: 206–10 tailed understanding of the relation of the hypoglossal ca- 12. Saleh E, Naguib M, Aristequi M et al: Lower skull base: study with sur- nal to the occipital condyle. The maximum extent of the gical implications. Ann Otol Rhinol Laryngol, 1995; 104: 57–61 upper portion of the occipital condyle that can be drilled 13. Yousry I, Morril B, Schmid UD et al: Detailed anatomy of the intracra- without exposing the hypoglossal canal is the posterior nial segment of the hypoglossal nerve: neurovascular relationships and third of its long axis [10,31]. According to Muthukumar et landmarks on magnetic resonance imaging sequences. J Neurosurg, 2002; 96: 1113–22 al [35] the occipital condyle can be safely drilled for a dis- BR82 Med Sci Monit, 2009; 15(3): BR75-83 Paraskevas GK et al – Osseous variations of the hypoglossal canal area

14. Adamczyk M, Bulski T, Sowińska J et al: Trigeminal nerve-artery con- 26. Bastianini A, Guidotti A, Hauser G et al: Variations in the method of tact in people without trigeminal neuralgia: MR study. Med Sci Monit, the division of the hypoglossal canal in Sienese skulls of known age and BR 2007; 13(Suppl.1): 38–43 sex. Acta Anat, 1985; 123: 21–24 15. Paraskevas G, Tsitsopoulos PP, Papaziogas B et al: Persistent primitive 27. Gigis P, Paraskevas G: Neuroanatomy, Central Nervous System, University hypoglossal artery. An incidental autopsy fi nding and its signifi cance Studio Press, Thessaloniki, 1999; 68 in clinical practice. Folia Morphologica (Warz), 2007; 66(2): 143–47 28. Smith PG, Backer RJ, Kletzker GR et al: Surgical management of tran- 16. Mysior M, Stefańczyk L: Doppler ultrasound criteria of physiological fl ow scranial hypoglossal schwannomas. Am J Otol, 1995; 16: 451–56 in asymmetrical vertebral arteries. Med Sci Monit, 2007; 13(Suppl.1): 29. Gilsbach JM, Sure U, Mann W: The supracondylar approach to the jug- 73–77 ular tubercle and hypoglossal canal. Surg Neurol, 1998; 50: 563–70 17. Naderi S, Korman E, Çitak G et al: Morphometric analysis of human 30. Spector S, Anderson GJ, McMenomey SO et al: Quantitative descrip- occipital condyle. Clin Neurol Neurosurg, 2005; 107: 191–99 tion of the far-lateral transcondylar transtubercular approach to the fo- 18. O’Rahilly R, Müller F: The early developement of the hypoglossal nerve ramen magnum and clivus. J Neurosurg, 2000; 92: 824–31 and occipital somites in staged human embryos. Am J Anat, 1984; 169: 31. Sarma S, Sekhar LN, Schessel DA: Nonvestibular schwannomas of the 237–57 brain: a 7-year experience. Neurosurgery, 2002; 50: 437–48 19. Le Double AF: Variations des os du crâne de l’homme. Vigot, Paris, 32. Dowd GC, Zeiller S, Awasthi D: Far lateral transcondylar approach: di- 1903; 67–70 mensional anatomy. Neurosurgery, 1999; 45: 95–100 20. Corruccini RS: An examination of the meaning of cranial discrete traits 33. Spektor S, Anderson GJ, McMenomey SO et al: Quantitative descrip- for human skeletal biological studies. Am J Phys Anthropol, 1974; 40(3): tion of the far-lateral transcondylar approach to the foramen magnum 425–45 and clivus. J Neurosurg, 2000; 92: 824–31 21. Lillie RD: Variations of the canalis hypoglosii. Anat Rec, 1917; 13: 34. Babu RP, Sekhar LN, Wright DC: Extreme lateral transcondylar ap- 131–44 proach: technical improvements and lessons learned. J Neurosurg, 22. Weigner K: Über die assimilation des atlas und über die variationen am 1994; 81: 49–59 os occipitale beim merischen. Anat Hefte, 1991; Bd. 45 35. Muthukumar N, Swminathan R, Venkatesh G et al: A morphometric 23. Poirier P, Charpy A: Traite d’Anatomie Humaine, Paris, 1911; Tome 1 analysis of the foramen magnum region as its relates to the transcon- 24. Keskil S, Gözil R, Galgüner E: Common surgical pitfalls in the skull. dylar approach. Acta Neurochir (Wien), 2006; 147: 889–95 Surg Neurol, 2003; 59: 228–31 36. Ho CL, Derytter MJ: Navigated dorsolateral suboccipital transcondy- 25. Hanihara T, Ishida H: Frequency variations of discrete cranial traits in lar (NADOSTA) approach for treatment of hypoglossal schwannoma. major human populations. III. Hyperostotic variations. J Anat, 2001; Case report and review of the literature. Clin Neurol Neurosurg, 2005; 199: 251–72 107: 236–42

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