179 J Anat. Soc. India 50(2) 179-183 (2001) Anomalous Origin Of The Middle Meningeal Artery—A Review. Manjunath, K.Y. Department of Anatomy, St. John’s Medical College, Bangalore - 560 034 Abstract. Middle meningeal artery (MMA) is the largest and most important of the arteries supplying the meninges. It is usually a branch of the first part of maxillary artery. However other sources of its origin have been described in literature viz : third part of maxillary artery, ophthalmic artery, persistent stapedial artery, internal carotid artery, basilar artery and rarely ascending pharyngeal artery. These anomalous origins of MzMA are of clinical significance in cases of fractures of the squamous and petrous temporal bone, and in surgical interventions involving Vidian nerve or the ligation of the middle meningeal artery. Literature on the incidence of the variations of the origin of the MMA and their embryological basis is reviewed here. Key words : Dural vascularization, Arterial variations, skull, Head injuries. Introduction : middle meningeal artery (OMMA). Earliest The middle meningeal artery (MMA) is the cases of the OMMA were reported by Curnow largest of the several meningeal arteries; it is also (1874) and Zuckerkandl (1976) (cited by Royle by far the most important branch of the maxillary and Motson- 1973; McLennan, Rosenbaum artery as it is a frequent source of haemorrhage and Haughton-1974) after injury to the skull. The MMA is usually a branch 4. Rarely MMA may arise as a branch of the of the first part of the maxillary artery. Other sources persistent stapedial artery (PSA). The PSA is of its origin and course have been described in the usually a branch of the intrapetrous portion of literature. These variations are of clinical the internal carotid artery, enters the tympanic significance in fractures of the squamous and cavity through its floor and passes through the petrous parts of the temporal bones and surgical obturator foramen of the stapes. For a short interventions involving the nerve of the pterygoid distance it is enclosed in a bony canal over the canal and maxillary artery (Klisovic, Sikic and promontary and enters the facial canal, and Krmpotic-Nemanic 1993). emerges in to the middle cranial fossa under the dura and gives off the middle meningeal Sources of anomalous origin of the MMA : branch (Altman 1947). The MMA of stapedial 1. In the absence of foramen spinosum the MMA origin is called the stapedial middle meningeal may enter the middle cranial fossa through the artery (SMMA). The first case of PSA was foramen ovale along with the mandibular described by Hyrtl in 1836 (McLennan et al nerve (Bartlett 1902 ; Chandler and Derezinski 1974). 1935). 5. The MMA can also originate from prepetrous 2. The MMA may arise as a branch of the third and suprasellar portion (extradural portion of part of the maxillary artery (sphenomaxillary the carotid siphon) of the internal carotid portion) and enter, the middle cranial fossa artery. (Newton and Potts 1974, Dilenge and through the lateral end of the superior orbital Ascherl 1980). fissure (SOF) (Toida 1934; Low 1946). 6. The MMA may also arise as a branch of the 3. The MMA may partially (i.e. only the anterior intra cavernous portion (juxtasellar) of the branch) or completely arise from the internal carotid artery (Newton and Potts ophthalmic artery. Under such circumstances it 1974, Tran-Dinh and Jayasinghe 1983). passes through the lateral end of the SOF or a 7. Some authors have reported anomalous origin foramen in the greater wing of the sphenoid of MMA from the basilar artery (Seeger and (foramen meningo-orbitale). The MMA of Hemmer 1976 ; Waga, Okada, Yamamoto ophthalmic origin is known as the ophthalmic 1978; Katz Wisoff, Zimmerman 1981). J. Anat. Soc. India 50(2) 179-183 (2001) 180 Middle Meningeal Artery 8. A rarest instance of MMA arising from the Origin of the MMA from the pertrous segment of the ascendig pharyngeal artery also has been internal carotid artery : reported (Moret, Lasjaunias, Vignaud, Doyon The basis of this anomaly is persistence 1978). (failure of involution) of the embryonic stapedial With the advent of the angiographic technique artery. This artery has been the subject of numerous more and more cases of anomalous origin of the anatomic dissections (Hyrtl 1936 ; Alexander 1849; MMA are being reported in the literature. Brock 1922 cited by Marion, Hinojosa, Khan 1985; Davies 1967), and has been reported to be observed Embryological basis : by chance, in three occasions during middle ear surgery (Baron 1963; House and Patterson 1964). The available embryologic literature on the While naturally present in adult rodents and some development of the cranial arteries suggests a bats, PSA in man is a rarely reported anomaly, fundamental relationship between the development Rarity of this anomaly can be appreciated by the of the ophthalmic and middle meningeal arteries, fact that House and Patterson (1964) encountered and the embryonic stapedial artery (Dilenge and this anomaly only twice during 8,000 procedures on Ascherl 1980). Knowledge concerning the early the middle ear, whereas, Steffen (1968) noticed only development of the stapedial artery is obscure, but two cases during 10,000 middle ear operations. First however some observations by Tandler (1902), reported by Hyrtl in 1836, only around thirty cases of Evans (1912) and Padget (1948) [summarised from this anomaly have been documented in the past 165 Dilenge and Ascherl 1980] permits some years of its history (see Table 1). Guinto, Garrabrant assumptions (see fig.1): The stapedial artery is and Radcliffe (1972), were the first to report the formed by the union of the remnants of the first angiographic features of PSA. The course of the branchial arch with the hyoid artery. After having PSA has been well documented by Altman (1947). penetrated the ring of the stapes it divides into two When present, it can pose a technical problem definitive divisions : during stapes surgery (Guinto et al 1972). A large PSA has been frequently reported in association 1. A maxillofacial division consisting of an with other anomalies : anencephaly and Paget’s infraorbital and a mandibular branch. disease (Altman 1947); multiple congenital 2. A supra orbital division consisting of branches anomalies (Keleman 1958; Sando, Baker and Black destined to supply the orbit and the intracranial 1972 cited by Marion et al 1985); thalidomide child segment of the MMA. The branches of the (Maran 1965 cited by Marion et al 1985); first arch maxillofacial division are assimilated by the anomaly (Pascual-Castroveijo 1983). developing external carotid artery and forms the maxillary artery (including the extracranial Ophthalmic origin of the MMA (OMMA) : part of the MMA). At this stage the proximal Two separate processes are involved in this part of the stapedial artery involutes, and its anomaly : remnants become the tympanic branches of 1. Failure of the proximal intra orbital and retro the MMA. orbital stapedial branches to involute, so that The supra orbital division of the stapedial the intracranial segment of the MMA remains artery forms in addition to the extraocular intra connected with the intraorbital stapedial orbital arteries, the intracranial segment of the branches. MMA. After the intraorbital branches of the stapedial 2. Defective involution of the maxillofacial artery are assimilated by the ophthalmic artery its division of the stapedial artery so that the proximal intra and retro orbital branches involute extracranial segment of the MMA is never and become resorbed by the intracranial segment of formed. As a result, no connection forms the MMA. between the maxillary artery and the J. Anat. Soc. India 50(2) 179-183 (2001) Manjunath, K.Y. 181 intracranial segment of the MMA (Dilenge and ophthalmic artery has also been described (Newton Ascherl 1980). and Potts 1974). The ophthalmic origin of the MMA is a A large meningeal branch originating from the relatively frequent anomaly. Dilenge and Ascherl lacrimal artery has been observed in angiograms in (1980) found 17 cases of MMA arising from the cases of pterional meningiomas. Such branches are ophthalmic artery among 3.500 cerebral angiograms pathological and serve only as a feeder vessel to examined by them (0.5%). Earliest cases of MMA the tumour in that region (Galligioni, Pallone, arising from the ophthalmic artery have been Bernardi, Iraci 1967). Origin of the MMA from described by Curnow (1874) and Zukerkandl (1876). extradural part of the carotid artery is quite rare (see Royle and Motson (1973) have described a case of table 1). A possible embryologic mechanism relates bilateral origin of the MMA from the ophthalmic in to an aberrant origin of the hyoid artery from the an adult skull of Asiatic origin, which is probably the internal carotid artery, so that its union with first photographic record of this anomaly. Gabriele remnants of the first branchial arch to form the and Bell (1967) consider their report of three cases stapedial artery either does not occur or occurs with of ophthalmic origin of the MMA as the first out any relation to the level of the stapes (Dilenge arteriographic demonstration of this anomaly. and Ascherl 1980). Instances of partial origin of MMA (only the Only a few cases of the MMA arising from the anterior branch) have been reported previously : basilar artery have been reported (Seeger and Toida (1934) in his study of 192 Chinese skulls Hemmer 1976; Waga et al 1978; Katz et al 1981). found five instances of anterior branch, and only The embryology of this anomaly has not been one instance of the complete stem of the MMA described and is only speculative. Waga et al (1978) originating from the orbit (Low 1946). Chandler and feel that this anomaly is due to an anastomosis Derezinski (1935) in their study of 1200 sides of the between the trigeminal artery and the PSA. skull found only one instance of the anterior branch of the MMA arising from the orbit. Klisovic et al Relationship of the foramen spinosum to the (1993) found 1% incidence of the cases of partial anomalous origin of the MMA : origin of the MMA from the ophthalmic artery in their Absence of the foramen spinosum often study. Embryological basis of this partial origin of accompanies aplasia of the conventional MMA. the MMA from the ophthalmic is, that sometimes the Substitution of the MMA by the OMMA or PSA extracranial segment of the MMA forms normally would also be expected to result in the absence of and unites with the intracranial segment, with only this foramen. A small foramen spinosum suggests partial involution of the retro orbital stapedial hypoplasia of the conventional MMA; under such branches so that some connection with the MMA is circumstances, a second source of the meningeal maintained (Dilenge and Ascheri 1980). Under such blood supply should be sought (McLennan et al a circumstance the anterior branch originates from 1974). McLennan et al (1974) in their examination of the ophthalmic and the posterior from the maxillary 108 dried skulls found only one skull with bilateral artery. According to Falk and Nicholls (1992), the and another with unilateral absence of foramen anterior branch of the MMA of humans is spinosum. Low (1946), Royle and Motson (1973) homologous with the meningeal lacrimal artery of have also noticed bilateral absence of the foramen rhesus monkeys. All three of the homologues,derive spinosum in their report of the anomalous origin of (developmentally) from the ophthalmic artery, and the MMA, from the orbit. The evolution of selective supply the same region of the skull and duramater. and even subselective cerebral angiography, The difference is that the homologous artery is coupled with continued refinement in angiographic usually distinct from the MMA in monkeys and apes, imaging apparatus and substraction technique, has but has become incorporated as the anterior branch permitted remarkable progress in ability to resolve of the MMA in humans. Incidence of the posterior vascular anatomy (Dilenge and Asherl 1980). branch of the MMA alone arising from the Selective catheterisation of branches of the J. Anat. Soc. India 50(2) 179-183 (2001) 182 Middle Meningeal Artery common carotid artery has facilitated the Nos 2, 3, 4, 7, 9, 10, 14 are cited from angiographic demonstration of anomalous origin of Marion et al. - No. 21 the MMA (Mclennan et al 1974). Around fifty cases (b) Intra cavernous part (Juxtasellar) (1) of the MMA of ophthalmic origin have been reported Newton and Potts (1974-c-1) (2) Tran- so far (see Table-I). Dinh & Jayasinghe (1983-c-1) Table 1 (c) Prepetrous & Suprasellar part (1) Newton Case Reports of The Anomalous Origin of The and Potts (1974-c-1) (2) Dilenge and Middle Meningeal Arterty Ascherl (1980-c-1) Source of the anomalous MMA IV. Basilar artery : (1) Altman (1974-b-1) (2) Authors (Year; material observed* no. of cases) Seeger and Hemmer (1976-c-3) (3) Waga, Okada, Yamamoto (1978-c-1) (4) Katz. I. 3rd part of Maxillary artery : (1) Low (1946-a- Wisoff, Zimmerman (1981-b, c-1) I) V. Ascending pharyngeal artery : (1) Moret, II. Ophthalmic artery : (1) Curnow (1874-b-1) (2) Lasjaunias, Vignaud, Doyon (1978-c-1) Zuckerkandl (1876-b-0) (3) Quain (1892-**) ...................... (4) Whitnall (1932-**) (5) Toida (1934-a-5 ant. *Material observed-(a) dry skulls, (b) cadaver/ branch only; I-complete stem) (6) Chandler postmortem dissection/clinical case (c) angiography. and Derezinski (1935 -a-ant. branch only-1) (7) **indicates material observed/number of cases not Bernasconi (1965-**) (8) Gabriele and Bell known. (1967-c-3) (9) Royle and Motson (1973-a-1) (10) Takahashi, Tamakawa, Kishikawa, Unlike the MMA of stapedial origin there have Kowada (1973-c-*0) McLennan, Rosenbaum been no reports of a case of MMA of ophthalmic origin presenting with clinical symptoms. Anomalous and Haughton (1974-a-2; c-5) (12) Dilenge and origin of the MMA from the third part of the Ascherl (1980 -c-17) (13) Nakagawa, Tanabe, maxillary artery or the ophthalmic is of surgical Sato (1982-c-2) interest beause it would be difficult to ligate its main Nos. 1,2 cited from No. 9; Nos. 3. 4. 7 cited trunk, Since it will not be found in its normal place in from No. 8; No-5 from No. 6 comparison to the conventional MMA located in the III. Internal carotid artery : (a) Intrapetrous part floor of the middle cranial fossa, where it would be (stapedial art.) (1) Hyrtl (1936-b-*) (2) within easy access (Low 1946, Klisovic et al 1993). Zuckerkandl (1873-b-*)/3) Alexander (1899-b-* (4) Brock (1922-b-) (5) Altman (1947; 57-b-2) References : (8) Keleman (1958-b-1) (7) Baron (1963-b-1) 1. Altman, F. (1947) : Anomalies of the internal carotid artery and its branches; their embryological and comparative (8) House and Patterson (1964-b-2) (9) anatomical significance. Report of a new case of persistent dePinies,Ongsiako (1964-b-1) (10) Maran stapedial artery. Laryngoscope. 57 (5) : 313- 339. (1965-b-1) 11) Davies (1967-b-1) (12) Steffen 2. Altman, F. (1957): Ear in severe malformations of head ; (1968-b-2) (13) Guinto, Garrabrant, Radcliffe discussion of formal and causal genetic factors. Laryngoscope. 66 (6) : 7- 25. (1972-c-3) (14) Sando, Baker, Black (1972-b/c- 3. Bartlett, W. (1902) : Contribution to the Surgical anatomy of 1) (15) Teal, Rumbaugh, Bergeron, Segall the middle cranial fossa. Annals of Surgery. 36 : 680-702. (1973-C-1) (16) McLennan, Rosenbaum, 4. Curnow, J. (1874) : Two instances of irregular ophthalmic Haughton (1974c-2) (17) Glassock, Dickins, and middle meningeal arteries. Journal of Anatomy and Jackson, Wiet (1980-b-1) (18) Dilenge and Physiology. 8 : 155- 156. Ascherl (1980-c-3) (19) Morano, Horton, 5. Chandler, S. B. and Derezinski, C. F. (1935) : The variations Gabriele (1981-c-1) (20) Pascual-Castroviejo of the middle meningeal artery with in the middle cranial fossa. Anatomical Record. 62 (3) : 309- 320 (1980-b/c-1) (21) Marion, Hinojosa, Khan (1985-b-2) J. Anat. Soc. India 50(2) 179-183 (2001) Manjunath, K.Y. 183 6. Davies, D. G. (1967) : Persistent stapedial artery ; A temporal 23. Nakagawa, T., Tanabe, S., Sato, D. (1982) : Anomalous bone report. Journal of Laryngology and Otology. 81 : 649 - ophthalmic artery-case reports and review of literature. No To 660. Shinkei. 34 (4) : 405 - 13. 7. Dilenge, D., Asherl, G. F. Jr., (1980) : Variations of the 24. Newton, T.H., and Potts, D. G. (Eds): Radiology of the skull ophthalmic and middle meningeal arteries : relation to the and brain, In: Angiography (arteries) Vol 2. The C.V. Mosby embryonic stapedial artery. American journal of Co. St. Louis. p 1261-1269 . (1974) Neuroradiology. 1 : 45 -54. 25. Pascual-Castroviejo- I. (1983) : Persistene of the stapedial 8. Falk, D., and Nicholls, P. (1992) : Meningeal Arteries in artery in a first arch anomaly : a case report. Cleft- Palate rhesus macaques (Macaca mulatta) : implictions for vascular Journal. 20 (2) : 146-50. evolution in anthropoids. American Journal of Physical 26. Rodesch, G. Choi, I.S., Lasjaunias, P. (1991) : Complete Anthropology. 89 : 299-308. persistence of the hyoido-stapedial artery in man. case report. Surgery Radiology Anatomy 13 (1) : 63-65. 9. Gabriele, O. F. and Bell, D. (1967) :Ophthalmic origin of the middle meningeal artery. Radiology. 89 : 841-844. 27. Royle, G., Motson, R. (1973) : Anomalous origin of the middle meningeal artery. Journal of Neurology, Neurosurgery 10. Galligioni., F., Pellone, M., Bernardi, R., Iraci, G. (1967): and Psychiatry. 36: 874- 876. Further observations on the meningeal branch of the lacrimal artery : Four additional cases. American Journal of 28. Seeger, J.F., Hemmer, J.F. (1976) : Persistent basilar I Roentgenology. 101 : 22-27. middle meningeal artery anastomosis. Radiology. 118 : 367- 370 11. Glassock, M. E., Dickins, J. R. E., Jackson, C. G., Wiet, R.J. (1980) : Vascular anomalies of the middle ear. Laryngoscope. 29. Steffen, T. M. (1968), Vascular anomalies of the middle ear. Laryngoscope. 78 : 171 - 197. 90 : 77-88. 30. Takahashi, M., Tamakawa, Y., Kishikawa, T., Kowada, M. 12. Guinto, F., Garrabrant, E. C., Radcliffe, W. B. (1972) : (1973) : Anomalous origin of the middle meningeal artery Radiology of the persistent stapedial artery. Radiology. 105 : from the ophthalmic artery/Embryologic and Clinical 365 - 369 considertion. Nippon-lgku-Hoshasen -Gakki-Zashi. 33 (3) : 13. House, H. P., Patterson, M. E. (1964) : Persistent stapedial 242- 6. artery : report of two cases. Transactions of American 31. Teal, J. S., Rumbaugh, C. L., Bergeron, R. T. and Segall, H. Academy of Ophthalmology Otolaryngology. 68 : 644-646. D. (1973) : Congenital absence of the internal carotid artery 14. Hyrtl, J. (1836) : Neue Beobachtungen aus dem Gebiete der associated with cerebral hemiatrophy, absence of the external menschlichen and Vergleichenden Anatomie. 3. Verber carotid artery, and persistence of the stapedial artery. mehrere im menschen vorkommende analogieen derjenigen American Journal of Reoentgenology. 118 (3): 534-545. arterie entdete. Medizinische Jahrbucher oesterreich states. 32. Toida, N. (1934) : Ueber die endokranischen furchen der 10 : 457-466 cited by Marion et al. (1985). arteria meningea media bie den Chinesen. Journal of Oriental 15. Katz, M., Wisoff, H. S., Zimmerman, R. D. (1981) : Basilar- Medicine. 21 : 13- 15. cited by Chandler and Derezinski. middle meningeal anastomosis associated with a cerebral (1935). aneurysm.Journal of Neurosurgery. 54 : 677-680. 33. Tran-Dinh, H. and Jyasinghe, I. S. (1983). Cavernous origin 16. Kelemen, G. (1958) : Arteria stapedia, in bilateral persistene. of the middle meningeal artery. Journal of Anatomy. 136 : Archives of Otolaryngology. 67 : 668-677. 653. 17. Klisovic, D. Sikic, E. and Krmpotic-Nemanic, J. (1993) : 34. Waga, S., Okada, M. and Yamamoto, Y. (1978) : Basilar Variations of the middle meningeal artery: significance for middle Meningeal arterial anastomosis. case report. Journal surgery and practice.Clinical Anatomy. 6 (5) : 289-294. of Neurosurgery. 49 : 450 ~ 52. 18. Low, F. N. (1946) : An anomalous middle meningeal artery. 35. Zuckerkandl, E. (1873) : Ueber die Arteria stapedia des Anatomical Record. 95 : 347-351. menschen. Monatsschr F Ohrenheilk Laryngorhinol. 7 : 6-7. 19. Morano, G.D., Horton, J.A., Gabriele, O.F. (1981) : cited by Marian et al-1995. Persistent embryologial loop of the internal carotid, middle 36. Zuckerkandl, E. (1876). Zur Anatomie der Orbitalarterien. meningeal and ophthalmic. Radiology. 141 : 409-410. 343-350. Medizinische Jahrbiucher der K Gellschaft der 20. Marion, M., Hinojosa, R., Khan, A.A. (1985) : Persistence of (Artze zu. (Wien) cited by Royleand Motson 1973. the stapedial artery : a histological study. Otolaryngology and Head and Neck Surgery. 93 (3) 292-312. 21. McLennan, J.E., Rosenbaum, A.E., and Haughton, V. M. (1974) : Internal carotid origins of the middle meningeal artery. Neuroradiology. 7 : 265-275. This Article Can be Downloaded / Printed Free from 22. Moret, J., Lasjaunias, P., Vignaud, J., Doyon, D. (1978) : http:\\jasi.net Participation de l’artere meningee moyenne a la vascularisation de al fossa posterieure. Neuroradiology. 16 : 306-7. J. Anat. Soc. India 50(2) 179-183 (2001) Opp. 180 Middle Meningeal Artery Fig I : (1-4) 1- shows the stapedial artery (sta) arising from the internal carotid artery and dividing into, supra orbital (SO) and maxillofacial (MF) divisions. 20mm stage embryo. 2-maxillofacial and middle meningeal arteries (MMA) have been assimilated into external carotid artery (ECA) to form the maxillary artery (MAX); supra orbital division (SD) has united with the ophthalmic artery (OA)- following the involution of the stapedial artery. 3- The middle meningeal artery (mma) being given off by the persistent stapedial artery (sta). 4- The intracranial part of the MMA has become annexed to the ophthalmic artery giving rise of ophthalmic middle menningeal. [based on the descriptions from, Davies 1967; Dilenge and Ascherl-1980; Marion. Hinojosa, Khan-1985].