Shape and Size of the Transverse Foramina in Japanese. Kunihiko KIMURA, Masayoshi KONISHI and HU Sheng Yu

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1 Okajimas Foria Anat. Jpn. 62 (2): , August 1985 Shape and Size of the Transverse Foramina in Japanese By Kunihiko KIMURA, Masayoshi KONISHI and HU Sheng Yu Department of Anatomy, National Defense Medical College 3-2 Tokorozawa, Saitama 359, Japan Department of Human Anatomy Wuhan Physical Culture Institute Hankow, Hupeh, China -Received for Publication, Feb. 12, Key words : Transverse foramen, cervical vertebra, Japanese, Chinese, Indians Summary: The present paper aims to describe accurately the shape and size of the transverse foramina in all the cervical vertebrae based on 50 male and 50 female Japanese skeletons. An elliptical shape (about 54%) occurred most frequently, followed by a round shape (about 14%) in all the vertebrae except C2s (superior aspect) and C6. Double foramina (about 11%) were found most frequently in C6 and decreased progressively above and below that level. The main axis of the foramen generally took an anteromedial direction in C1, a frontal direction in C3 05, and an anterolateral direction in C7. The axis changes its direction strikingly at two points, namely from anteromedial to anterolateral between C7 and C6, and from frontal to anterolateral in the foramen of C2, cranialward. The transverse foramina were significantly greater in males than in females, and on the left side in more than half cases. Its value was largest in C1, followed by C2 and C6, and smallest in C7, though it increased gradually from C3 to C6. Almost identical data were observed in Japanese, Chinese and Indian vertebrae. The transverse foramen (foramen transversarium) pierces the transverse process of all the cervical vertebrae, and usually transmits the vertebral artery and vein, accompanied with a plexus of sympathetic nerves. The foramen may be absent in C7 and, when present, frequently does not transmit the vertebral artery. The artery usually first penetrates the transverse foramen of C6 and runs cranialward through the transverse foramina of the other cervical vertebrae to the base of the skull. In 104 African Blacks and Europeans, Argenson et al. (1980) found that initial penetration of the artery was seen in 89.1% at C6, in 6.0% at C5, in 3.5% at C7, in 1.3% at C4 and in 0.1% at C3. In 550 cadavers, Anson and McVay (1971) observed that there are no differences between the right and left vertebral arteries for their level of penetration, the right artery entering the transverse foramen in 90% at C6, 6.9% at C5, 2.0% at C7 and 0.9% at C4, and the left artery in 89.9%, 6.2%, 3.4% and 0.6%, respectively. The artery is situated in the center of the foramen, surrounded by the vertebral vein or veins and a sympathetic plexus (Argenson et al., 1980). While forming a dense plexus around the vertebral artery, the vertebral vein descends through the transverse foramina of the cervical vertebrae and emerges from the transverse foramen of C6 or C7. Address: Dr. Kunihiko Kimura, Department of Anatomy, National Defense Medical College, 3-2 Tokorozawa, Saitama 359, Japan 123

124 K. Kimura et a/. The venous trunk of the vertebro-transverse sinus (Louis and Argenson, 1962) usually occupies the antero-external portion of the foramen (Argenson et al., 1980).

2 124 K. Kimura et a/. The venous trunk of the vertebro-transverse sinus (Louis and Argenson, 1962) usually occupies the antero-external portion of the foramen (Argenson et al., 1980). The contents of the transverse foramen seem to influence greatly its size and shape. Variations of the foramen could be useful for estimating variations of the vessels and accompanying nerve structures (Taitz et al., 1978). Therefore, the study of the transverse foramina of the cervical vertebrae could serve for a more accurate interpretation of radiographs, angiograms and CAT scans. Observations on the size and shape of the transverse foramina of all the cervical vertebrae have been made by Francis (1955) in Whites and Blacks, Jaen (1974) in Mexicans, Taitz et al. (1978) in Indians and Hu (1983) in Chinese. In addition, De Boeck et al. (1984) reported a radioanatomical study of the accessory transverse foramen in 156 isolated vertebrae. For Japanese vertebrae, only one publication, on the atlas (Muraki, 1961), has been found. The present paper aims to describe accurately the shape and size of the transverse foramina in all the cervical vertebrae in Japanese, and also to examine differences between males and females and between the right and left sides, as well as between some populations, namely, Japanese, Chinese and Indians. General descriptions were mainly made on the data of Japanese vertebrae, because of small samples of females in both Indian and Chinese skeletons, and lack of data on tribial origins in the former and absence of data for C7 in the latter. Material and Methods The transverse foramina of the first to the seventh cervical vertebrae (C1 C7) of 50 male and 50 female Japanese skeletons in the Department of Anatomy, Yokohama City University School of Medicine, and those of 62 male and 18 female Asian Indian skeletons in the Department of Anatomy, National Defense Medical College, were observed and measured by Kimura and Konishi. The latter had been imported from' India for teaching purposes. In addition the first six cervical vertebrae (C1 C6) of 66 male and 34 female Northeastern Chinese skeletons were examined by Hu at the Department of Human Anatomy, Wuhan Physical Institute in Hankow, China. The transverse foramina were studied from below, the inferior surface of the body of the vertebra facing the examiner. However, for only the second vervical vertebra (axis, C2), both the superior (C2s) and inferior (C20 openings of the transverse foramen were studied separately, because of their different features. As shown in Fig. 1, the transverse foramen was classified into seven types based on shapes; type A round, type B elliptical, type C triangle, type D square, type E double foramina, type F irregular or unclassifiable and type G absent foramen, and also into five types based on direction of the maximum (main) diameter; type I multiaxial as in type A and in some of type E, type II sagittal, type III frontal, type IV oblique anteromedially and type V oblique anterolaterally. The maximal, minimal, sagittal and transverse diameters were directly measured for both the right and left transverse foramen of the vertebra with a pair of sliding calipers accurate to 0.05 mm (Fig. 2). In the case of double foramina (type E), only the main large foramen was measured. An index of the minimum to the maximum diameter (coefficient of roundness, CR), proposed by Taitz et al. (1978), and a modulus of size (the sum of both diameters) were calculated for each foramen. According to the CR, the foramen was classified into brachymorph (more than 85), mesomorph (between 75 and 85) and dolichomorph (less than 75).

3 Shape and Size of Transverse Foramina 125 Fig. 1. Seven (a-g) and five (I-V) types of the transverse foramen of the cervical vertebrae based on its shape and direction of the main axis Fig..2. Measurements of the transverse foramen. Results 1: sagittal diameter, 2: transverse diameter, 3: maximal diameter, 4: minimal diameter. Shape: Table 1 shows incidences of seven shape types of the transverse foramen in Cl to C7 in the Japanese series, for each side and each sex separately. There were no significant differences for incidences of the seven types between the right and left sides of each vertebra, except C2s and C6 in females, and between males and females for each vertebra, except C2s, C2i and C7, at the level of 5% on the basis of the chisquare test. In general, type B (ellipitical) occurred more frequently (about 61%), followed by type A (round) (18%), than other types in each cervical vertebra, except for C2s and C6, in both sexes. The C2s showed more frequently types B (about 50%) and A (36.5%), and the C6 types E (about 41%), A (31.5%) and B (23.5%), than the others. Types C (triangle) and D (square) appeared somewhat more frequently in males (5.0% for type C and 5.6% for type D) than in females (3.25% and 3.0% for each type). Type E (double foramina) occurred at almost the same frequency (about 11%) in both sexes, and mostly (about 96%) in the lower three vertebrae: about 25% in C5, 46% in C6 and 26% in C7. Types F (unclassifiable) (0.38% in only males) and G (absent) (1.3% in both sexes) scarcely appeared in the samples. The foramen of C7 was absent in 1.0% in males and 60% in females. According to the shape of the transverse foramen, the cervical vertebrae could be rouhgly classified into upper (C1-4) and lower (C5-7) groups. Types A-D occurred in over 97% of the transverse foramina in the upper cervical group and in 57% to 77% in the lower. While, type E appeared almost totally in the lower three (about 96%) or four (98%) vertebrae. Direction of the main axis: Table 2 presents incidences of five types according to the direction of the maximal diameter of the transverse foramen in each cervical vertebra of the Japanese series. Regardless of sex, the main types occurred in the following order of frequency in each cervical vertebra: types V (about 61%), 11 (18% and 1(14%) in Cl; types I (36%), V (28%) and 11 (18%) in C2s; types IV (46%), I (29%) and III (19%) in C2i; types III (68%), I (14%), IV (11%) and V (9%) in C3; types III (66%), V (24%) and I (9%) in C4; types III (46%), V (28%) and 1 (21%) In C5; types I (39%), III (27%), V (25%) and IV (7%) in C6; and types IV (83%) and III (12 ) in C7. Size: Table 3 gives the means and standard deviations of the maximal, minimal, sagittal and transverse diameters, and the modu-

4 126 K. Kimura et a/. Table I. Incidences of seven shape types of transverse foramina in Cl to C7 in Japanese. Table 2. Incidences of five types of transverse foramina based on direction of the main axis in Japanese. lus for each cervical vetebra in the Japanese series for each sex and each side separately. The material number of some vertebrae was diminished because of absence (type G). Table 4 shows differences between the right and left sides and sex differences for the means of all measurements based on paired t-test and t-test, respectively. In the table, an asterisk and double asterisks stand for significant differences at the levels of 5% and 1%, respectively. In general, all the diameters and the module of the transverse foramen were significantly larger in males than in females in each vertebra except for C7. Also, on the basis of the module, the transverse foramen was significantly, or arithmetically at least, larger on the left side than on the

5 Shape and Size of Transverse Foramina 127 Table 3. Means and standard deviations of four diameters and the module of the transverse foramen for each cervical vertebra in Japanese. Table 4. Results of paired t-test for differences between the right and left sides, and those of t-test for sex differences, for the means of all measurements of the transverse foramina. right of each vertebra, with a few exceptions, for both sexes. According to differences between the modules on the right and left sides, the vertebra was classified into three groups; R > L, R = L and R < L (Table 5). Table 5 reveals that the transverse foramen is greater on the left side in more than half (50-74%) of the specimens. Regardless of sex and side, the module shows the largest value for C 1, followed by C2i and C6, and the smallest for C7. It decreased gradually cranialward from C6 to C3, and increased again at C2i and Cl. The value was smaller at C2s than at C2i and C3 C6. Discussion The sulcus arteriae vertebral is of the atlas is sometimes converted into a foramen by a delicate bony specule growing from the posterior end of the superior articular

6 128 K. Kimura et al. Table 5. Incidences of three groups based on differences of the right and left sides for individual vertebrae. process. Bergman (1967) studied on variations of the atlas based on a survey of the literature and 142 vertebrae, including the transverse-vertical and sagittal foramina and incomplete closure of the transverse foramen. Bergman (1967) observed occurrences of the transverse-vertical foramen, which is formed by an osseous bridge convex upward and laterally, running from the lateroposteior border of the lateral mass of the vertebra to the posterior lamina of the transverse process, the sagittal foramen, which is formed by an osseous arch convex in the posterior-superior direction, running from the posterior end of the superior articular fossa to the base of the posterior arch as far as the posterior boundary of the sulcus of the vertebral artery, and the incomplete closure of the transverse foramen. According to Bergman, the transverse-vertical foramen was found in 0 to 6.8%, the sagittal foramen in 0 to 19.1%, and the incomplete closure of the foramen in 3.6 to 15.2% in some racial populations. For example, these variations were observed in 5.0%, 3.0% and 6.0% in Japanese (Hasebe, 1913) and in 3.5%, 10.5% and 12.0% in Poles (Bergman, 1967), respectively. However, none of these variations was found in the present series. Table 6 shows mean frequencies of seven shape types for the transverse foramina in the upper four, the lower three and all cervical vertebrae, including the C2s, in Japanese, Indians and Chinese, combining both sexes and sides. In the table, types F and G are combined because of their small frequencies. As previously mentioned, the data of C7 are absent in the Chinese sample (marked with an asterisk in the text). Types A D occurred in about 98% and 95% of the transverse foramina in the upper four cervical vertebrae, and about 70% and 54% in the lower three in Japanese and Indians, respectively. These types appeared in about 96% of the upper four and about 69%* of the fifth and sith cervical vertebrae in Chinease. Regardless of different populations, type B (elliptical) occurred more frequently (about 54%), followed by type A (round) (about 14%), than other types in each vertebra, except for C2s and C6. Types C and D Occurred more frequently in males than in females in Japanese. This sex difference was also observed in Chinese, but not in Indians. Type E appeared more frequently in the lower three cervical vertebrae (about 29% in Japanese, 27%* in Chinese and 40% in Indians), especially in C6, than in the upper (about 2.5%, 2.3% and 0.9% in each racial group). Francis (1955) found double foramina in about 29% of C5 and 58% of C6 in 109 male whites, including incompletely double foramina. Francis also mentions that a similar finding was recorded in female whites, and male and female blacks. On the average, Francis (1955) found double foramina in 190 of 1526 foramina (12.5%) in 109 male whites, and Taitz et al. (1978) recorded them in 34 of 480 foramina (7.1%) in Indians. In the present study, type E was found in about 1 1 %of Japanese, about 15.5% of Indians and about 9%* of

7 Shape and Size of Transverse Foramina 129 Table 6. Mean frequencies of seven shape types of the transverse foramina of the upper four, the lower three and all cervical vertebrae in Japanese, Chinese and Indians. Chinese. Accordingly, regardless of sex and populations, it seems that double foramina are generally found in about 7-15% of vertebrae, being most frequently in C6 and decreasing progressively above and below that level. The foramen of C7 was absent in 1.0% in males and 6.0% in females of Japanese, and in 2.7% in males and 2.8%in females of Indians. Some textbooks describe a division of the transverse foramen by a fibrous or bony bridge. For example, Rauber-Kopsch (1940) and Frazer (1965) describe a foramen intratransversarium or subdivided foramen at all levels except in the atlas and axis, the small posterior foramen being for a vein. According to Lutz (1968) and TOndury (1970), the accessory foramen encloses a branch of the vertebral nerve. On the basis of our observations in a few cases during anatomical dissection, a tributary of the vertebral vein or veins passes through the accessory foramen. Fig 3 shows the polygon from the CR index (coefficient of roundness) for the transverse foramen of each cervical vertebra in the male and female Japanese, Chinese and Indian series of the present study, as well as that for the Indian series (combined sexes) reported by Taitz et al. (1973). The dotted area shows mesomorph, categorized by the indices between 75 and 85. The great majority of the transverse foramina falls into the mesomorph category, while the exceptions of dolichomorph for C7 and branchymorph for C2s, C5 and C6, regardless of populations. The direction of the main axis of the transverse foramen at each level is almost identical in the Japanese, Chinese and Indian series. Accordingly, regardless of sex and populations, the following conclusions may be drawn: while the transverse foramen generally takes an anteromedial to a sagittal direction in Cl and C2s, it takes an anterolateral to a frontal directionat C2i. Then, the main axis generally takes a frontal direction in C3 to C6, changing from an anterolateral to an anteromedial direction gradually. It takes an anterolateral direction in most cases (about 83%) in C7 again. That is, the main axis of the transverse foramen changes its direction strikingly at two points, in the transverse foramen C2 and between C7 and C6. It seems that the direction of the transverse foramen corresponds well to the course of the vertebral artery at each level. The transverse foramen is significantly greater in males than in females at each level, except for C7, and on the left side than on the right of individual vertebrae

8 130 K. Kimura et al. Fig. 3. Polygon from the coefficient of roudness (CR index) for the transverse foramen in each cervical vertebra in Japanese, Chinese and Indians in the present series and in Indians reported by Taitz et al. (1973), in more than half the cases at each level. Stopford (1916) found that the vertebral arteries are usually (92%) unequal in size, the left being larger in somewhat more than half of 150 brains, which was also noted by Hardesty et al. (1963) and Epstein (1969). This fits our observations, mentioned above. Regardless of sex, sides and population group, the transverse foramen shows the smallest value at C7 and a remarkably large value at C6. This fits the fact that the vertebral artery initailly penetrates the transverse foramen of C6 in about 90%of cases. Thereafter, the value decreases gradually cranialwards to C3, and increases again at C2 to show the largest value at C 1, where the vertebral artery exist. These differences may be related not only to the size of the contents but also to the mechanical stresses due to movements at each level. Acknowledgements We wish to express our sincere thanks to Dr. Ronald Singer, Department of Anatomy, University of Chicago, for his kind advice in the preparation of the English manuscript. References 1) Argenson, C., J.P. Franck, S. Sylla, H. Dintimille, S. Papasian, and V. di Marino: The vertebral arteries (Segments VI and V2). Anat. Clin. 2 : 29-41, (1980) 2) Anson, B.J., and C.B. McVay: Surgical Anatomy. 5th ed. W.B. Saunders Co., Philadelphia, (1971) 3) Bergman, P. : On the varieties of the atlas in man. Folia Morphol. 28: , (1967) 4) Boeck, M. De, R. Potviliege, F. Roels, and E. De Smedt: The accessory costotransverse foramen: a radioanatomical study. J. Conput. Assist. Tomogr. 8: , (1984) 5) Epstein, B.S.: The Spine. A radiological Philadelphia, (1976)

9 Shape and Size of Transverse Foramina 131 6) Francis, C.C. : Dimensions of the cervical vertebrae. Anat. Rec. 122: , (1955) 7) Frazer, J. E. : Anatomy of the Human Skeleton. 6th ed. J. and A. Churchill, London, (1965) 8) Hardesty, W.H., W.B. Whitacre, J.F. Toole, and H.P. Royster: Studies on the vertebral artery blood flow. Surg. Forum 13: , (1982) 9) Hasebe, K. : Die Wirbelsaule der Japaner. Z. Morph. Anthrop. 15: , (1913) 10) Hu, S.Y. : The morphology of foramen transversarium of cervical vertebrae and cervical spondylosis. Chinese J. Sport Med. 2: 43-45, (1983) (in Chinese) 11) Jaen, E.M.T.: Variedades anatornicas en vertebras de la coleci6n Tlatelolco. Anales del Institutto Nacional de Antropologia Historia, Mexco 52: 71-81, (1974) 12) Louis, R., and C. Argenson: Les veines verte- brales. Travaux Inst. Anat. Marseille 21; 21-25, (1962) 13) Lutz, G., Die Entwicklung des Halssympathicus und des Nerves vertebralis. Z. Ant. Entwicklungsgesch. 127: , (1968) 14) Muraki, T. : An anatomical study of the atlas in the Japanese in Kwanto district. Jikeikai Med. J. 25; , (1962) (in Japanese) 15) Rauber-Kopsch, F. : Lehrbuch und Atlas der Anatomie des Menschen. 16th ed. George Thieme Verlag, (1940) 16) Stophord, J.S.B. : The arteries of the pons and medulla oblongata. J. Anat. Physiol. 50: , (1916) 17) Taitz, C., H. Nathan, and B. Arensburg: Anatomical observations of the foramina transversaria. J. Neurol. Psych. 41: , (1978) 18) TOndury, G. : Angwendte und topographische Anatomie. 4th ed. Georg Thieme Verlag, Leipzig, (1970)

Anatomical observations of the foramina transversaria

Journal of Neurology, Neurosurgery, and PsYchiatry, 1978, 41, 170-176 Anatomical observations of the foramina transversaria C. TAITZ, H. NATHAN, AND B. ARENSBURG From the Department of Anatomy and Anthropology,