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Home , Lacrimal artery, Middle meningeal artery, Ophthalmic artery

Okajimas Folia Anat. Jpn., 72(2-3): 163-176, August, 1995

Classification of the Ophthalmic that Arises from the in Japanese Adults

By

Kazuyuki SHIMADA, Yasumi KANEKO, Iwao SATO, Hiromitsu EZURE and Gen MURAKAMI

Department of Anatomy, Showa University, School of Medicine, Tokyo, Japan Department of Anatomy, Nippon Dental University, School of Dentistry at Tokyo, Tokyo, Japan Department of Anatomy, Sapporo Medical University, School of Medicine, Sapporo, Japan

-Received for Publication, July 4, 1995-

Key Words: Gross anatomy, Middle meningeal artery, Orbital branch, Meningo-orbital foramen

Summary: In a study of Japanese adults, we found that the orbital branch (OB) passing through the frequently anastomosed with the or the (12/20). However, the OB passing through the meningo-orbital foramen (mof) only associationaly anastomosed with branches of the ophthalmic artery (4/79). Further- more, the OB in the , excluding the as previously reported. We examined 116 cases in which the OB passed through the mof in 129 adult Japanese cadavers (45.0% in 258 sides). The OB passing through the mof was always distributed to the periorbital region and the area that it supplied was limited to the periorbita in about half of those cases. In another half of the cases (58/116), the area supplied included the lacrimal gland.

The ophthalmic artery in the orbital branch arising cadavers (74 males and 55 females) to determine the from the middle meningeal artery has been described course of the orbital branch and the nerve of the previously (Zuckerkandl, 1876; Meyer, 1887; Lang supply to the orbital area from the middle meningeal and Wachsmuth, 1979; Hollinshead, 1982). More- artery, passing through the mof. In 75 of 129 cadavers, over, the orbital branch (0B) has been considered polyvinyl acetate was injected from the common to be an important souse of blood for the orbital carotid artery in order to allow us to identify the contents and named the accessory ophthalmic artery small twigs that extended through the superior by Gillian (1961). The course of the OB is, however, orbital fissure. In preliminary observations, initially, controversial, it has been proposed to pass exchisively the whole brain was removed and the through the superior orbital fissure (Duke-Elder and was carefully removed with forceps from the inner Wyber, 1961; Doxanas and Anderson, 1984) or surface of the anterior cranial fossa to the middle mainly through the meningo-orbital foramen (mof; cranial fossa. After treatment, we found the OB of Fig. 1; Kopsch, 1955; Lasjaunias, 1981; Ducasse the middle meningeal artery if it was located at the et al., 1985). In this present study, we examined the roof of the orbit. If present such branches were course passing through the mof, of the ophthalmic carefully dissected out and recorded photographically artery branch in the orbit and classified the course and by drawing each case. into four types according to the area supplied. The extend of supply by the ophthalmic artery reveals an important problem in the surgical treatment of the Results base of orbit. Types of entry of the orbital branch of the ophthalmic artery arising from the middle meningeal artery into Materials and Methods the orbit (Fig. 2). Seventy-five injected cadavers (150 sides) were We examined 258 sides of 129 adult Japanese examined. The orbital branch (0B) of the middle

Address correspondence to Kazuyuki Shimada D.D.S., Ph H .D., Department of Anatomy, Showa University School of Medicine , 1-5-S atanodai, Shinagawa-ku, Tokyo 142, Japan.

163 164 K. Shimada et al. meningeal artery, passing through the superior classified into four types and the incidence of each orbital fissure (sof), was found in 4.7% of cases was as follows (Fig. 4 and Table 1): type 1, the area (7 sides; type a). The OB passing through the supplied by the OB was limited to the periorbita meningo-orbital foramen (mof) was found in 44.0% (46.6%, 54 of 116 cases); type 2, the OB supplied of cases (66 sides; type b). Moreover, both types the lacrimal gland in the absence of the usual lacrimal were found together in 8.7% (13 sides; Fig. 2; artery (32.8%, 38 of 116 cases); type 3, the OB type c). However, in 9 of 13 cases (of type c), the OB mainly supplied the lacrimal gland together with the passed through the mof and finally supplied the usual lacrimal artery (17.2%, 20 of 116 cases); Type periorbital region. The OB passing through the sof 4, the OB anastomosed with the ophthalmic artery frequently anastomosed with the proximal portion of or the lacrimal artery at the base of the orbit (3.4% , the lacrimal artery or the ophthalmic artery (in 12 of 4 of 116 cases). Details of each type are described 20 cases of type a and type c; Fig. 3). In 5 of in 20 below. cases (of type a and type c), the OB passed through Type 1 (Fig. 5). After passing thought the canal, the sof and supplied the lacrimal gland without the the OB ran frontally to the periorbita of the upper usual lacrimal artery from the ophthalmic artery. In wall of the orbit for 10-20 mm. The OB was then only 2 of 20 cases, the OB passed through the sof and ramified into fine small twigs and supplied the peri- supplied the periorbital region. orbita, in the front of which the branch of the posterior ethmoidal artery and the deep temporal The orbital branch passing through the meningo- artery terminated. orbital foramen. Type 2 (Fig. 6). The supply to the periorbita was The OB was often observed passing through the also observed, as in type 1. After ramification at the mof (45.0% , 116 of 258 cases). In such cases, the periorbita, the OB travel toward the lacrimal gland. OB issued from the frontal branch of the middle Beyond the fronto-zygomatic suture area, the OB meningeal artery beneath the posterior edge of the followed a tortuous or straight course along the lesser wing of the sphenoidal bone. The mof was . Some twigs supplied to orbital fat usually located at the spheno-frontal suture or the and the lateral rectus. The OB entered the lateral frontal bone or the greater wing of the sphenoidal and inferior portion of the lacrimal gland. After bone in the apex of the orbit within a range of 10 — supplying the lacrimal gland, the OB was often 20 mm lateral to the sof, as shown in Figure 1. finally distributed to the upper (15.5% ; 9 of 58 The average length of the so-called Hyrtl canal cases from type 2 and type 3). (Lasjaunias, 1981) was 5-10 mm. The canal ran Type 3 (Fig. 7). In this type, the lacrimal artery almost straight in the dorsi-ventral direction and passed through the mof, as described in type 2 (the was found near the sof. In other cases, the canal was so-called meningo-lacrimal artery in Lasjaunias, located almost at the anterior part of the frontal 1981), and it was observed together with the usual bone, at a distance from the sof. This tortuous canal lacrimal artery which extends from the ophthalmic was about 20 mm in length. The OB passing through artery. the mof always supplied the inferior and lateral part Type 4 (Fig. 8). In 3 cases of this type, the OB of the periorbita. The distribution of the OB was anastomosed with the most proximal portion of the

Table 1. Classification of the orbital branch that passes through the meningo- orbital foramen

* Type 1, The area supplied is limited to the periorbita; type 2, supplying to the lacrimal gland without the usual lacrimal artery; type 3, supplying the lacrimal gland with the usual lacrimal artery; type 4, anastomosis with the ophthalmic or the lacrimal artery. Ophthalmic Artery Arising from the Middle Meningeal Artery 165 usual lacrimal artery immediately after the OB had mosed with the lacrimal artery or the ophthalmic passed through the mof. Moreover, in just one case artery only rarely (type 4, 3.4%; 4 of 116 cases). of type 4, the OB passed through the mof to supply However, the OB that passed through the sof fre- the lacrimal gland, the lateral rectus, superior rectus quently anastomosed with the proximal portion of and levator palpebrae superioris muscles. Then the the lacrimal artery or the ophthalmic artery (60.0%, OB travelled along the frontal nerve towards the 12/20 of type a and type c). Moreover, one of four trochlea of the oblique superior muscle to become cases of anastomosis showed a well-developed OB the supratrochleal artery that was distributed the that passed through the mof, supplying to a large frontal portion of the face. The artery running be- part of the orbital contents, as reported by Meyer neath the trochlea and supplying the face was also (1887) and Hiura (1980). However, in the orbital seen as a branch of the ophthalmic artery. A fine artery (Adachi, 1928), the ophthalmic artery arising anastomosis was found between the OB and the from the middle meningeal artery passes through the ophthalmic artery under the rectus superior muscle sof, not through the mof, in the Japanese (Adachi, in the posterior portion of the orbit. 1928), in Negroes (Harvey and Howard, 1945) and We examined each type of blood supply to the in Caucasians (Zuckerkandle, 1876; Bansal, 1961). orbital contents when the OB passed through the The differences in the frequencies of anastomosis mof. The branching and distribution patterns of the and in courses of the orbital artery are summarized ophthalmic artery showed, normal range of variation, below. except for those of the lacrimal artery. It has been proposed that the OB is to derived from the anastomosis between the stapedial artery and the primary ophthalmic artery during develop- Discussion ment (Dilenge and Ascherl, 1980; Padget, 1948). However, the OB passing through the mof always During our observations of 258 sides of cadavers supplied to the periorbital region but rarely anasto- of the Japanese adult, the OB passing through the mosed with the lacrimal artery or the ophthalmic mof was found in about half of cases (45.0% , 116/ artery. Moreover, the frontal branch of the middle 258). Moreover, in half of our cases, the OB that meningeal artery, which extends the OB that passes passed throughthe mof mainly supplied the lacrimal through the mof, often runs in a canal in the gland (58/116). In about half the cases (54/116), frontal bone or the sphenoidal bone (Chandler and however, the area supplied in cases of type 1 was Derezinski, 1935). The canal is located close to the limited to the periorbital region. The OB passing mof at the anterior base of the . The results through the sof was found in fewer cases (13.3% , 20/ suggest that most such cases are derived from a 150 from type a and type c), although this branch meningeal branch of the middle meningeal artery at was described by Lang and Wachsmuth (1979) and an early developmental stage. In this study, the OB Hollinshead (1982). Our results cannot comparted passing through the sof usually anastomosed with the to previous reports about the OB which has not lacrimal artery or the ophthalmic artery (12/20) and been examined including cases of type 1. However, rarely supplied the periorbital region (2/20). There- Ducasse et al. (1985) reported that the OB passed fore, our observations seem to support the hypothesis through the mof and supplied the lacrimal gland (the that the OB passing through the sof originateds meningo-lacrimal artery) in 28.5% of 70 cadavers of developmentally from the anastomosis between the Caucasians examined. Recently, Lang and Kageyama stapedial and primary ophthalmic . (1990) reported that the meningo-lacrimal artery The present study suggests that the OB passing was found in 15.9% of 71 Caucasians cadavers. In through the mof might be clinically important as both previous reports, the incidence corresponds an accessory blood supply to the orbital contents. closely to ours (22.5% , 58/258 from type 2 and During reconstruction of the anterior base of the type 3). skull and the orbit after orbital base (Price The distribution of the OB passing through the et al., 1988; Stiernberg et al., 1987), the OB passing mof varied among cases. The term "meningo- through the mof can easily to be damaged and a lacrimal artery" (Lasjaunias, 1981; Ducasse et al., large part of the blood supply to the orbital contents 1985) cannot always apply to the OB that passes can be lost. Moreover, the OB passing through the through the mof since the area is supplied often mof is thought to become a main feeding artery limited to the periorbita. Many previous reports, of meningiomas in the anterior cranial fossa, as with the exception only of that of Diamond (1991), indicated by Kuru (1957). describe the meningo-lacrimal artery as supplying the periorbita as well as the lacrimal gland. We found that the OB passing through the mof anasto- 166 K. Shimadaet al.

Acknowledgments 9) Gillian LA. The collateral circulation of the human orbit. Arch. Ophthalmol. 1961; 65:100-110. The authors wish to thank Prof. Noboru Goto 10) Harvey JC and Howard LM. A rare case of anomalous ophthalmic artery in a negro. Anat. Rec. 1945; 92:87-90. (Chairman of Department of Anatomy, Showa 11) Hiura A. An anomalous ophthalmic artery arising from University School of Medicine) and Prof. Tooru the middle meningeal artery. Anat. Anz. 1980; 147: Sato (Chainnan of Department of Anatomy, School 473-476. 12) Hollinshead WH. Anatomy for Surgeons (3rd edition). of Dentistry at Tokyo, Nippon Dental University) Vol. 1., Harper and Row, Philadelphia, pp. 152-153, 1982. for their encouragement to his study. 13) Kopsch FR. Rauber-Kopsch Lehrbuch und Atlas der Anatomie des Menschen (Band 1). Georg Thieme Verlag, Stuttgart, p. 189, 1955. 14) Kuru Y. Meningial branch of the ophthalmic artery. Acta. References Radiol. Diag. 1957; 6:241-251. 15) Lang J and Kageyama I. The ophthalmic artery and 1) Adachi B. Das Arteriensystemder Japaner (Band 1). its branches, measurement and clinical importance. Surg. pp. 103-106,Maruzen, Kyoto, 1928. Radiol. Anat. 1990; 12:83-90. 2) Bansal PC. A case of abnormal ophthalmic arteries, J. 16) Lang J and Wachsmuth W. Lam Praktische Anatomie. Anat. Soc. India. 1961;10:41-42. (Band 1 Teil A). Springer, Berlin, pp. 475-533, 1979. 3) Chandler SR and DerezinskiCF. The variationsof the 17) Lasjaunias PL. Craniofacial and Upper Cervical Arteries. middle meningealartery within the middle cranialfossa. Function, Clinical and Angiographic Aspect. Williams and Anat. Rec. 1935;62:309-319. Wilkins, Baltimore, London, pp. 13-78, 1981. 4) Diamond MK. Homologies of the meningeal-orbital 18) Meyer F. Zur Anatomie der Orbitalarterien. Morph. Jb. arteriesof humans:a reappraisal.J. Anat. 1991; 178:223— 1887; 12:414-418. 241. 19) Padget DH. The development of the cranial arteries in 5) DilengeD and Ascher! GF. Variationsof the ophthalmic the human embryo. Contrib Embryol Carnegie Inst of and middle meningeal arteries: relation to the embryonic Washington 1948; 32:207-261. stapedialartery. Amer.J. Neuroradiol.1980; 1:45-53. 20) Price JC, Loury M, Carson B and Johns ME. The 6) Doxanas MT and Anderson RL. Clinical Orbital pericranial flap for reconstruction of anterior skull base Anatomy.Williams and Wilkins,Baltimore, pp. 160-169, defect. Laryngoscope, 1988; 98:1159-1164. 1984. 21) Stiernberg CM, Bailey BJ, Weiner RL, Kalhoun KH 7) Ducasse A, SengalA, Delattre JF and Flament JB. The and Quinn FB. Reconstruction of the anterior skull base participationof the externalcarotid artery to the orbital following craniofacial resection. Arch Otolaryngol Head vascularization.J. Fr. Ophthalmol.1985; 8:333-339. Neck. Surg. 1987; 113:110-112. 8) Duke-ElderS and WyberKC. Systemof Ophthalmology. 22) Zuckerkandl E. Zur Anatomie der Orbitalarterien. Med. Vol. 2., Henry Kimpton,London, pp. 469-471, 1961. Jahrb. Wien. 1876; 3:343. Ophthalmic Artery Arising from the Middle Meningeal Artery 167 Plate I

Explanation of Figures

Plate I

Fig. 1. The meningo-orbital foramen in the dry skull of a Japanese cadaver. A: Frontal view, B: Posterior view from the internal cranial base. The meningo-orbitalforamina are located at the frontal bone (arrow), the spheno-frontal suture (small arrowhead) or the greater wing of the sphenoidal bone (large arrowhead). The correspondingforamen in the two views is indicated by the same symbol. Abbreviations: AC, anterior cranial fossa; F, hypophysial fossa; 0, . 168 K. Shimada et al.

Plate 11

Plate II

Fig. 2. The middle meningeal artery travelling into the orbit on the right side. A. The orbital branch of the middle meningeal artery comes from the superior orbital fissure (type a): 4.7% (N = 7). B. Type b; the OB comes through the meningo-orbital foramen in directly: 44.0% (N = 66), C. Type c is a mixed case: 8.7% (N = 13). Abbreviations: sof, superior orbital fissure; mof, meningo- orbital foramen. Ophthalmic Artery Arising from the Middle Meningeal Artery 169 Plate HI

Plate III

Fig. 3. The course and distribution of the OB passing through the superior orbital fissure. Examination of 20 cases of the OB passing through the superior orbital fissure (sof) (a case show in Fig. 2A and 2C). A. The branch anastomosis with the lacrimal artery or with the ophthalmic artery: 60.0% (N = 12), B. Supplying the lacrimal gland (Lacr) without the usual lacrimal artery: 25.0% (N = 5), C. Supplying an area limited to the periorbita: 10.0% (N = 2). Abbreviations: anas, anastomosis; po, twigs to periorbita. 170 K. Shimada et al.

Plate IV

Plate IV

Fig. 4. Classification of the types of course and distribution of the orbital branch that passess through the meningo-orbital foramen (mof) (116 cases in 258 sides: 45.0%). Viewed from the right side. A. Type 1, the area Supplied is limited to the periorbita: 46.6% (N = 54); B. type 2, supplying the lacrimal gland (Lacr) without the usual lacrimal artery: 32.8% (N = 38); C. type 3, supplying to the lacrimal gland with the usual lacrimal artery: 17.2% (N = 20); D. type 4, anastomosis with the lacrimal artery or the ophthalmic artery: 3.4% (N = 4). Abbreviations: anas, anastomosis, po, twigs to periorbita Ophthalmic Artery Arising from the Middle Meningeal Artery 171 Plate V

Plate V

Fig. 5. The of case of type 1: The orbital branch passes through the meningo-orbital foramen. Blue resin was injected from the . The orbital branch was cut at the meningo-orbital foramen portion as shown by an arrow. The area supplied in this artery was limited to the periorbita below the lateral part of the roof of the orbit (encompassed by a dotted line). The lacrimal artery is seen also visible below the periorbita (arrowheads). Abbreviations: oc, occulomotor nerve; oph, ophthalmic nerve; opt, ; pe, posterior ethmoidal artery; TM: temporalis muscle, UEL, upper eyelid; ZB, . 172 K. Shimada et al.

Plate VI

Fig. 6. Dissection of a case of type 2 case from the right side. The orbital branch passes through the meningo-orbital foramen (large star). Photograph (A) and the corresponding line drawing (B). The branch supplies the lacrimal gland (LG) and the upper eyelid (UEL) without the usual lacrimal artery. Abbreviations: ae, anterior ethmoidal artery; f: frontal nerve; m, middle meningeal artery; oa, ophthalmic artery; opt, optic nerve; oph, ophthalmic nerve; soy, superior ophthalmic ; LG, lacrimal gland; LPS, levator palpebrae superioris muscle; OS, obliquus superior muscle; RS,'rectus superior muscle; TM, temporalis muscle; UEL, upper eyelid; ZB, zygomatic bone; Arrowheads, the orbital branch; small asterisks, branches to the rectus medialis muscle; small black stars, branches to the rectus inferior muscle; small white stars, branches to the rectus lateralis muscle. Ophthalmic Artery Arising from the Middle Meningeal Artery 173 Plate VI 174 K. Shimada et al.

Plate VII

Fig. 7. Dissection of case of type 3 case from the right side. The orbital branch passes through the meningo-orbital foramen. Photograph (A) and the corresponding line drawing (B). The branch supplies the lacrimal gland (LG) and the upper eyelid (UEL) with the usual lacrimal artery (pink in B). Arrowheads, the orbital branch, large star; meningo-orbital foramen (opened), a, anastomosis between the usual lacrimal artery and the middle meningeal artery (see Fig. 3A). Abbreviations: ae, anterior ethmoidal artery; f, frontal nerve; ic, ; ifo, ; m, middle meningeal artery; noi, nerve to the rectus inferior muscle. oa, ophthalmic artery; oph, ophthalmic nerve; opt, optic nerve; soy, ; LPS, levator palpebrae superioris muscle; 01, obliquus inferior muscle; OS, obliquus superior muscle; RI, rectus inferior muscle; RL, rectus lateralis muscle; RM. rectus medialis muscle; RS, rectus superior muscle; Small white stars, branches to the rectus superior and levator palpebrae superioris muscles. Ophthalmic Artery Arising from the Middle Meningcal Artery 175 Plate VII 176 K. Shimada et al.

Plate Viii

Plate VIII

Fig. 8. Line drawing of a case of type 4 from the left side. The orbital branch (red) passes through the meningo-orbital foramen (large star). The branch supplies to the lacrimal Gland (LG), occular muscles and the skin of the frontal region. The usual lacrimal artery is not found. Abbreviations: a, anastomosis between the ophthalmic artery and the type 4 orbital branch; ac, anterior ethmoidal artery; f, frontal nerve; ic, internal carotid artery; m, middle meningeal artery, oa: ophthalmic artery, opt, optic nerve; oph, ophthalmic nerve; soy, superior ophthalmic vein; LPS, levator palpebrae superioris muscle; OS, obliquus superior muscle; RS, rectus superior muscle.