study the vascular anatomy ofthe superficial temporal, posterior ... carotid arteries and internal jugular veins were isolated and cannulated with ... were also cannulatedposterior to the mastoid processes. ... deep branch close to bone (Fig. 1).
Arun K. Gadre, M.D.,* Michael J. O'Leary, M.D.,t Rizkalla Zakhary, Ph.D.,t Fred H. Linthicum, Jr., M.D.,§ and William F House, M.D.II
The Lateral Skull Base: A
Vascular Perspective
with
Clinical Implications
Surgery of the skull base continues to expand rapidly. Lesions once considered inoperable can now be readily resected, often in an en block manner, due to advances in anesthesia, imaging techniques, and innovative surgical approaches. However, prolonged operating time in a field compromised by prior surgery, radiotherapy, or recurrent tumor is fraught with complications. Additionally, large surgical defects increase the need for reconstructive options. These factors have spurred renewed interest in the vascular anatomy of the lateral skull base. Of the many techniques available for vascular casting, we used methyl methacrylate in cadaver specimens to study the vascular anatomy of the superficial temporal, posterior auricular, and occipital arterial systems. We studied the layers of the scalp and patterns of blood supply to the cranial skeleton and soft tissues.
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MATERIALS AND METHODS Several techniques are available to study the vascular anatomy. In 1672, Jan Swammerdam developed a method for casting the vasculature with wax.1 For the next 3 centuries, investigators used various casting techniques to
improve their understanding of the human vasculature. Their success was limited, and the casts were difficult to reproduce. Spalteholz produced casts of transparent plastic in 1911.2 In the 1940s, wider availability of polymer technology promoted more sophistication in the casting of blood vessels. Batson3 reported the use of methyl methacrylate to study venous networks in the nasal mucosa. Tompsett1 4 described the use of unsaturated polyester resins for corro-
Skull Base Surgery, Volume 1, Number 2, April 1991 *Research Fellow, House Ear Institute, Los Angeles; Assistant Clinical Professor of Anatomy, University of Southern California School of Dentistry, Los Angeles, California; tClinical Fellow (1989-90), House Ear Clinic, Los Angeles, California; Commander, Medical Corps, United States Navy; *Associate Professor of Anatomy, University of Southern California School of Dentistry, Los Angeles, California; *Director of Morphology Laboratories, House Ear Institute, Los Angeles; Clinical Professor of Otolaryngology, University of Southern California School of Medicine, Los Angeles, California; and "lHearing Associates, Newport Beach, California Study was supported by the House Ear Institute, an affiliate of the University of Southern California School of Medicine; by the University of Southern California School of Dentistry; and by National Institutes of Health grant no. S07 RR05303-27 Reprint requests: Dr. Gadre, House Ear Institute, 2100 West Third Street, Los Angeles, CA 90057 Copyright X) 1991 by Thieme Medical Publishers, Inc., 381 Park Avenue South, New York, NY 10016. All rights reserved.
LATERAL SKULL BASE-GADRE ET AL
sion casting. Of the many materials now available for vascular casting, we found that methyl methacrylate has advantages: it produces detailed casts down to the level of capillaries, it keeps its shape, and it allows further study of the specimen with a scanning electron microscope. The technique of Hill and McKinney5 was followed with minor modifications.
Preparation of Specimens We used six unembalmed human specimens. Decapitation was performed at the root of the neck. The common carotid arteries and internal jugular veins were isolated and cannulated with plastic tubing. To clear the vessels of blood clots, we used a hand-held syringe filled with normal saline (2 liters) followed by 300 ml of pH-A (Champion Co., Springfield, OH), which is a hemolyzing detergent. To ensure vessel clearance, we immersed the specimens for 24 hours in a mixture of equal volumes of normal saline and detergent. Each vessel was again flushed with normal saline until the return was clear. The specimens were dehydrated by flushing the vessels with methanol and immersing them overnight in a methanol bath. Acetone was infused into each vessel for 10 to 15 minutes to further enhance dehydration of the distal vasculature and to permit better capillary filling with the monomer. Methanol and acetone also helped to preserve the specimens without loss of "fresh cadaver" qualities.
Preparation and Injection of Methyl Methacrylate Batson's no. 17 anatomic corrosion compound (Polysciences, Rydel, PA) comprises methyl methacrylate monomer, catalyst, promoter, and pigment. We used 30 ml of monomer colored with pigment plus 10 ml of catalyst to thin the monomer and eliminate air bubbles from the mixture plus 10 to 15 drops of promoter. These proportions permitted a time lag between preparation and injection of approximately 15 minutes. Polymerization prevented injection beyond this time. A red mixture (40 to 50 ml) was injected into the common carotid arteries of specimens 1, 2, 3, and 4 (eight sides). In specimens 1 and 2 (four sides), the venous system was also injected with methyl methacrylate stained blue. In specimens 5 and 6 (four sides), the superficial temporal arteries were isolated anterior to the tragi and cannulated distal to the points of origin of the maxillary arteries. In these same specimens, the occipital arteries were also cannulated posterior to the mastoid processes. The superficial temporal and occipital arteries were ligated proximally. Cannulas were then secured high in the external carotid artery, so that the perfusate would selectively enter the posterior auricular and maxillary arteries and their branches. Green, blue, and red methyl methacry-
late solutions were simultaneously injected into the superficial temporal, occipital, and external carotid arteries, respectively. The cut ends of blood vessels were clamped as they filled with methyl methacrylate to prevent loss of resin and to minimize contact with air, which is known to retard surface polymerization. Casts were then cured under water, at room temperature, for 24 hours. Casts of polymerized methyl methacrylate, which faithfully reproduced luminal vascular anatomy, were then studied by one or more methods.
Processing of Specimens Specimen 1 (two sides) was treated with a solution containing sodium sulfate (1 gm) and pancreatin enzyme (2 gm) mixed in a liter of normal saline6 at a pH of 8.5 and a temperature of 37°C.4 Specimens 2 and 3 (four sides) were exposed to larvae of the Dermestidae family,6 which spared casts and bone. Specimen 4 (two sides) was treated with 33% hydrochloric acid, which completely dissolved soft tissue and bone. In specimens 5 and 6 (four sides), with three simultaneous injections each, areas of differential cutaneous staining represented the relative distribution of the posterior auricular, occipital, and superficial temporal arteries. These areas were mapped. Starting at a sagittal incision (with releasing incisions over the eyebrow and occiput), we surgically reflected layers of the scalp to confirm anatomic findings in specimens 1 to 4. The posterior auricular artery flaps were raised and studied. Temporal craniotomies were then performed to study the contribution of the middle meningeal artery to the inner table.
RESU LTS Specimens 1, 2, and 3 demonstrated all named vessels described in standard anatomy texts. In addition, the occipital, posterior auricular, superficial temporal, and facial arteries were consistently accompanied by a smaller, deep branch close to bone (Fig. 1). Specimen 1, subjected to partial enzymatic digestion, showed finer anatomic details. The axial periosteal vessels broke into capillary networks closely adherent to bone. Perforators arising from these capillaries penetrated the outer table of the calvaria. Fine anastomotic vessels joined the superficial and deep systems (Fig. 2). The presence of capillaries in the periosteum was confirmed in the dissected specimens (5 and 6). In specimen 4, the middle meningeal artery was seen supplying the inner table. The deep temporal arteries supplied the outer table and the superficial temporal artery supplied the skin and soft tissues (Fig. 3). The pattern of superficial and deep supply was consistent in the dissected specimens and the periosteal blood
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Figure 1. The general pattern of superficial and deep vessels is a finding common to all named arteries. The straight arrow points to the deep (periosteal) branch of the occipital artery and the curved arrow to a branch of the superficial temporal artery (the deepest temporal artery). This vessel is also seen anastomosing with the posterior deep temporal artery in the temporal fossa.
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Figure 2. Capillaries in the periosteum, with anastomotic channels (arrowheads) between the superficial (STA) and deepest (DeTA) temporal arteries. The temporomandibular joint (TMJ) is also depicted.
.W
-
y
'Iw.
Figure 3. Viewing from inside the calvarium, the middle meningeal artery (MMA) deep temporal (DTA) and superficial temporal (STA) arteries are seen. Notice a tuft of capillaries arising from the anterior branch of the middle meningeal artery supplying the inner table and diploe.
LATERAL SKULL BASE-GADRE ET AL
supply was found to be axial. In the scalp, skin and galea were held together by dense fibrofatty tissue. The superficial branch of the superficial temporal artery penetrated this layer about 2 cm above the zygomatic arch to supply the dermis and galea. This artery anastomosed freely with the superficial branches of the posterior auricular and occipital arteries. In dissections of specimens 5 and 6, the periosteum over the frontoparietal region could be split into two distinct layers. The outer layer of periosteum was continuous with the loose areolar tissue that covered the temporal aponeurosis. This innominate fascia had fine blood vessels arising from the superficial temporal artery system (Fig. 4). The inner layer covered and adhered to the outer table to the level of the superior temporal line, where it split to ensheath the temporalis muscle. The lateral layer formed the tough temporal aponeurosis (deep temporal fascia), which was supplied by the middle temporal artery. The medial layer was thin and adhered to the temporalis muscle laterally and the bone of the temporal fossa medially. A vascular arcade in this layer appeared to form an anastomosis between the deep temporal arteries and a fairly constant vessel, which we will call the deepest temporal artery. We are introducing this term to differentiate this vessel from the anterior and posterior deep temporal arteries, which are branches of the maxillary artery. This vessel is the deepest branch of the superficial temporal artery system (Fig. 5) and courses from just anterior to the external auditory canal over the root of the zygoma for 4 to 5 cm. Temporal craniotomies revealed that a branch from the middle meningeal artery entered a nutrient foramen in
R1 .. ry
,
the squama of the temporal bone and supplied the inner table and diploe. When we raised a posterior auricular artery skin flap, as described by Kolhe and Leonard,7 we saw a deeper vessel coursing in the periosteum over the mastoid process. This vessel was the deep branch of the posterior auricular artery (Fig. 6), which supplied the mastoid cortex. On dissection, the venous system generally paralleled the arterial system but its anatomy was more variable. An arteriolar plexus was observed in the infratemporal fossa (Fig. 7). The plexus appeared to arise from the maxillary artery and transverse facial artery.
DISCUSSION Our findings suggest the possibility of development of new reconstructive options in skull base surgery. The challenge in reconstructive skull base surgery is to provide a reliable and permanent means of compartmentalization8 without sacrificing function and appearance. The reconstructive potential of the temporoparietal-galeal system of flaps has not yet been fully realized.9 Recent use of the scalp and calvarial bone for this purpose'O°'l has renewed interest in the anatomy and vascular supply to the lateral skull. Unfortunately, there is little uniformity in the nomenclature of these temporal layers; the same layer is described by various synonyms, and some authors have even questioned the existence of a distinct innominate fascia. 12 We confirmed that the periosteum of the occipital,
.............S
Figure 4. A dissected specimen confirmed the presence of the innominate fascia (I) as being distinct from the temporalis fascia (T). Fine capillaries are seen in the innominate fascia.
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Figure 5. The temporalis muscle (M) has been reflected from the temporal fossa, revealing an anastomosis between the posterior deep and deepest temporal arteries (between arrows). The deepest temporal artery appeared black from a mixture of red and green colors, injected simultaneously into the superficial temporal and maxillary arteries.
frontal, and parietal regions could be split into a more superficial "periosteal" layer continuous inferiorly with the innominate fascia and a deeper "subperiosteal" layer adherent to the bone. 13 We also found that the innominate fascia was supplied by fine vessels that appeared to arise from the superficial temporal artery system. This finding
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implies that the layer is vital and that more layers are locally available for reconstructive purposes. In the region of the zygomatic arch, a fat pad deep to the innominate fascia was also a constant finding. These findings confirmed the concept of a bilayered periosteum proposed by Casanova et al'3 and Psillakis et
Figure 6. The deep branch of the posterior auricular artery supplying the periosteum and lateral surface of the mastoid. The posterior auricular artery and vein are seen in the skin flap.
LATERAL SKULL BASE-GADRE ET AL
varium would have potential advantages as a donor site. Based on our vascular findings, it is conceivable that composite free or pedicled flaps can be fashioned from locally available tissues for reconstructive skull base surgery.
CONCLUSIONS Every named artery in the skull is accompanied consistently by a deeper periosteal branch. The findings of such an extensive, axially based periosteal vascular supply, throughout the calvarium, holds great promise in the Figure 7. Arrowhead points to an arterial plexus in of osteo-subperiosteal flaps for skull base development the infratemporal fossa. reconstruction. In addition an anastomosis was found between the deep temporal artery and the deepest temporal artery in the subperiosteum of the temporal fossa. A al. 14 The existence of a bilayered periosteum has also been previously undescribed arterial plexus was also seen in the confirmed by histologic and electron microscopic exam- infratemporal fossa. The vascular anatomy of the region inations. 15 raises new possibilities for reconstructive options in surOur findings also suggest that the subperiosteum of gery of the skull base. the temporal fossa is a vascularized membrane: an upwardly convex vascular anastomosis is present between the deep temporal arteries and the deepest branch of the REFERENCES superficial temporal artery. This arterial anastomosis suggests the possibility of development of axial-pattern osteosubperiosteal flaps to reconstruct the lateral wall or 1. Tompsett DH: Anatomical Techniques. Edinburgh: E & S Livingstone, 1956 floor of the orbit. 2. Spalteholz W: Uber das Durchsichtigmachen von menschlichen The importance of the deep branch of the posterior und tierischen Praparaten. Leipzig, 1911 auricular artery coursing within the periosteum is its 3. Batson OV: The venous networks of the nasal mucosa. Ann Otol Rhinol Laryngol 63:571-580, 1954 nourishment of cortical bone of the mastoid. One of the 4. Tompsett DH: Anatomical Techniques. Edinburgh: E & S Livingauthors (A.K.G.) has successfully used an anteriorly pedstone, 1970 icled composite osteoperiosteal flap with compact cortical 5. Hill EG Jr, McKinney WM: Vascular anatomy and pathology of the head and neck: Method of corrosion casting. Adv Neurol 30: mastoid bone to reconstruct the posterior canal wall in 191-197, 1981 patients following modified radical mastoidectomies. 6. Hildebrand M: Anatomical Preparations, Berkeley: University of California Press, 1968 The anatomy of the arterial supply to the calvarium has been controversial. 16,17 We found no major artery 7. Kolhe PS, Leonard AG: The posterior auricular flap: Anatomical studies. Br J Plast Surg 40:562-569, 1987 entering the bone at suture lines. We also found the middle 8. Arden RL, Mathog RH, Thomas LM: Temporalis muscle-galea flap in craniofacial reconstruction. Laryngoscope 97:1336meningeal artery to be the chief vessel penetrating the 1342, 1987 inner table, whereas no major vessels penetrated the outer 9. Panje WR, Morris MR: Refinement in head and neck reconstructable. However, fairly constant, deep branches of the tion: The temporoparietal fascia flap. Presented at the Triological Society, Western Sectional Meeting, Jan 5-7, 1990 named vessels coursed in the subperiosteum. Here they NF, Schramm VL, Sekhar LN: Reconstruction of the cranial broke up into a network of capillaries and perforators that 10. Jones base following tumour resection. Br J Plast Surg 40:155-162, are part of the vascular supply to the outer table, as 1987 suggested by Argenta et al. 18 The prospect of exploiting 11. Rose EH, Norris MS: The versatile temporoparietal fascial flap: Adaptability to a variety of composite defects. Plast Reconstr this vascular distribution for the development of axial Surg 85:224-232, 1990 outer table-subperiosteal pedicled or free flaps needs fur- 12. Abul-Hassan HS, von Drasek Ascher G, Acland RD: Surgical ther study. anatomy and blood supply of the fascial layers of the temporal region. Plast Reconstr Surg 77:17-24, 1986 Experimental studies in rabbits and monkeys seem to 13. Casanova R, Cavalcante D, Grotting JC, Vasconez LO, Psillakis validate the clinical concept that membranous bone grafted JM: Anatomic basis for vascularized outer-table calvarial bone in the craniofacial region undergoes less resorption than flaps. Plast Reconstr Surg 78:300-308, 1986 endochondral bone.'9 Additionally, vascularized mem- 14. Psillakis JM, Grotting JC, Casanova R, Cavalcante D, Vasconez LO: Vascularized outer table calvarial bone flaps. Plast Reconstr branous bone transfers retain their osseous mass to a Surg 78:309-317, 1986 greater degree than comparable nonvascularized bone 15. Habal MB, Maniscalco JE: Observations on the ultrastructure of the pericranium. Ann Plast Surg 6:103-111, 1981 grafts.20-22 If bone can survive with little resorption at an 16. Brookes M: The Blood Supply of Bone, New York: Appletonunfavorable site, vascularized transfers of membranous Century-Crofts, 1971 bone would be an optimal approach.18 Thus, the cal- 17. Cutting CB, McCarthy JG, Berenstein A: Blood supply of the
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18. 19. 20. 21.
upper craniofacial skeleton: The search for composite calvarial bone flaps. Plast Reconstr Surg 74:603-610, 1984 Argenta LC, Friedman RJ, Dingman RO, Duus EC: The versatility of pericranial flaps. Plast Reconstr Surg 76:695-702, 1985 Zins JE, Whitaker LA: Membranous versus endochondral bone: Implications for craniofacial reconstruction. Plast Reconstr Surg 72:778-784, 1983 Canalis RF, Saffouri M, Mirra J, Ward PH: The fate of pedicle osteocutaneous grafts in mandibulo-facial restoration. Laryngoscope 87:895-908, 1977 Canalis RF: Further observation of the fate of pedicle osteo-
22.
cutaneous grafts. Otolaryngol Head Neck Surg 87:763-767, 1979 Antonyshyn 0, Colcleugh RG, Hurst LN, Anderson C: The temporalis myo-osseous flap: An experimental study. Plast Reconstr Surg 77:406-415, 1986
The authors are grateful to Butch Welch for assistance with the figures and to Peggy Nasoordeen and Randolf L. Green for assistance in manuscript preparation.
REVIEWER'S COMMENTS The authors are to be commended. Not only is this study well planned but the article is lucidly written. Furthermore, it is clear that a great deal of hard work was undertaken to produce the analysis of the vascular supply of the lateral skull base, all of which is well supported by the illustrations. The exact relationship of the frontoparietal periosteum to the temporalis fascia and the innominate fascia may have been forgotten by many otologists and certainly it was unknown by this reviewer that the "deepest temporal artery" arises from the superficial temporal system, not from the maxillary artery, as previously believed. The findings of a deep periosteal blood vessel accompanying the named vessels has, as the authors say, implications for reconstructive flaps. It is hoped that the further study of the aspect, already planned, will be carried out.
Paul Fagan, M.D.
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