Orbit, 2015; 34(4): 212–215 ! Informa Healthcare USA, Inc. ISSN: 0167-6830 print / 1744-5108 online DOI: 10.3109/01676830.2015.1029137

ORIGINAL ARTICLE

Orbital Branch of the Infraorbital Artery: Further Characterization of an Important Surgical Landmark Avni V. Patel1,2, Alia Rashid1,3, Frederick A. Jakobiec1,3, Daniel R. Lefebvre1,2, and Michael K. Yoon1,2

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1

Department of Ophthalmology, Harvard Medical School, Boston, Massachusetts, USA, 2Ophthalmic Plastic Surgery, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA, and 3David G. Cogan Laboratory of Ophthalmic Pathology, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts, USA

ABSTRACT The orbital branch of the infraorbital artery, a key vascular structure that is not universally noted in orbital textbooks and atlases, is clinically significant, since injury to it can result in perioperative hemorrhage. We conducted a cadaver dissection to document its presence, measure its location, and evaluate it histopathologically. It was present in 8 of 9 orbits and was a mean distance of 16.6 mm (range 10–23) from the inferior orbital rim. In half of the specimens, there were 2 separate structures seen. Histopathology confirmed these structures to be neurovascular bundles. Keywords: Infraorbital artery, operative complications, orbital anatomy, orbital branch, orbital vasculature

INTRODUCTION

study is to further characterize the orbital branch of the infraorbital artery through cadaver dissections and histopathologic examination.

Variability in anatomy is well known to occur and is present in nearly all anatomic structures. Vascular variations appear to be the most likely to be encountered, and have been documented in the orbit since the 19th century.1,2 In extensive representations of the orbital vascular network in various textbooks and atlases of orbital anatomy, the orbital branch of the infraorbital artery is rarely mentioned.3–6 The infraorbital artery, arising from the maxillary artery and part of the external carotid circulation, travels through the infraorbital canal along the floor of the orbit. It exits out the infraorbital foramen as a neurovascular bundle with branches of the trigeminal nerve. In some individuals, this artery gives off an orbital branch. As described in a few recent case reports, failure to identify the orbital branch of the infraorbital artery may result in perioperative hemorrhage, and if unrecognized, may result in vision loss from uncontrolled bleeding.7–9 The purpose of this

MATERIALS AND METHODS Prior to the study, the Massachusetts Eye and Ear Infirmary Institutional Review Board reviewed and waived approval as no identifiable living subjects were involved. Donated cadaver heads were dissected. The brief histories of each cadaver (age, sex, cause of death) did not include any orbital disease or trauma. Each cadaver head was dissected bilaterally via a transconjunctival subperiosteal approach. Data recorded included the presence or absence of the artery, the distance from the orbital rim, the presence of associated structures (veins, nerves), and the end target of the artery. In several orbits, a portion of the artery was biopsied and sent for histopathologic evaluation.

Received 22 July 2014; Revised 22 December 2014; Accepted 9 March 2015; Published online 2 June 2015 Correspondence: Michael K. Yoon, Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, MA 02114, USA. Tel: 617-573-5550. Fax: 617-573-5525. E-mail: [email protected]

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Orbital Branch of the Infraorbital Artery

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RESULTS A total of 9 orbits of 5 cadavers were included. In one orbit (subject 3), the right orbit had evidence of previous trauma and was excluded. Coincidentally, all of the cadavers were female (4 Caucasian and 1 Asian) with a mean age of 65 years (range 40–82). The orbital branch of the infraorbital artery was found in 8 of the 9 orbits. The distance to the bony orbital floor foramen from the inferior orbital rim ranged from 10 to 23 mm with a mean distance of 16.6 mm (see Table 1). This foramen was centered on the infraorbital canal. In 4 of 8 orbits with these structures present, two separate structures were identified (Figure 1A). Overall, there was variability in the size of these structures with the largest being several times larger in diameter than the smallest (Figure 1B). In 3 orbits, where relatively large arteries were present, dissection revealed the vessel’s course anteriorly through the orbital fat with terminal branches heading to the origin of the inferior oblique muscle and continuation to the lacrimal sac. Also, in one large vessel, lissamine green tinged saline was injected into TABLE 1. Subject demographics and artery location. Patient age (years) 57 82 69 70 40 Mean: 65

Sex

Ethnicity

F F F F F

White White White White Asian

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the artery with a 30 gauge needle to help visualize the course of the artery (Figure 1C and 1D). After the injection of lissamine green, no identifiable connection between the orbital branch of the infraorbital artery and muscular branches of the ophthalmic artery could be seen.

HISTOPATHOLOGIC DESCRIPTION Five specimens were studied histopathologically with hematoxylin and eosin, Masson trichrome, and elastic stains. In three of the specimens, both arteries and veins had been included in the excision. The Masson trichrome stain revealed a thicker, red-staining muscularis in the arteries. Additionally, the elastic stain demonstrated a prominent elastic lamina in the arteries which was absent in the veins. In two specimens small nerve units enveloped in their fibrous perineuria were identified and stained pale pink with the trichrome method rather than bright red characteristic of smooth muscle vascular mural cells (Figure 2).

DISCUSSION

Right orbit (mm)

Left orbit (mm)

10 16, 21 Excluded (trauma) Absent 19 Mean: 16.6

11 15, 17 17, 23 15 19, 16

The present study examined the orbital branch of the infraorbital artery. We found that this structure penetrated the orbital floor a mean distance of 16.6 mm (10 – 23) from the inferior orbital rim. Our findings were similar to Rubin et al.,8 who found a mean distance of 14.4 mm10–14 in their study of intraoperative findings. Given the known orbital

FIGURE 1. Images of the gross dissection of the orbital branch of the infraorbital artery demonstrate variability in the structure and course of the artery highlighted with the use of lissamine green. (A) A double structure; (B) a large structure; (C) a large artery prior to the injection of lissamine green; (D) a large artery after the injection of lissamine green demonstrating the course of the artery. !

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FIGURE 2. Histopathologic identification of the neurovascular bundle as demonstrated by H&E, elastic, and Masson-trichrome stains. (A) The orbital arterial branch (a) of the infraorbital artery is accompanied by a smaller vein (v). The arrows point to small peripheral nerve units in the vicinity of the vessels. (B) The Masson trichrome stain highlights the red muscularis of the orbital artery (a) outside of which is blue collagen of the adventitia. The adjacent vein (v) displays an inconspicuous muscularis. (C) The Elastic stain reveals a well-developed, uninterrupted elastic lamina in the artery (a), whereas the vein (v) lacks an elastica.

watershed zones between the internal and external carotid circulations, the observed course of the terminal branches of the artery during our dissection, and previous descriptions of the artery,4,5 there is likely shared vascularity to the areas around the inferior oblique and lacrimal sac. Histopathologic examination was essential in verifying that these specimens were indeed neurovascular bundles with the presence of arteries, veins, and nerves. This finding thus classifies this structure as a perforating infraorbital bundle, similar to other neurovascular bundles of the orbit (e.g., zygomatico-temporal bundle). The orbital branch of the infraorbital artery is not frequently discussed, even in orbital anatomy texts and atlases. We reviewed eleven orbital anatomy texts4,5,10–18 and found that the orbital branch of the infraorbital artery was mentioned in only three of them: Gray’s textbook of anatomy as well as the

Rootman and Dutton atlases of orbital anatomy. Of these eleven atlases, three others discuss the infraorbital artery but fail to mention the orbital branch(es) that arise from it. In 1932, Whitnall described the infraorbital artery laying above and medial to the nerve and giving rise to branches serving the inferior oblique muscle, orbital fat, and anteriorly serving the lower eyelid and lacrimal sac.6 Hayreh then described in 1963 orbital branches of the infraorbital artery from its course in the infraorbital groove. He described the orbital branches as supplying the soft tissue of the orbital floor, lacrimal sac, nasolacrimal duct, and supplying small divisions to the inferior rectus, superior oblique and orbicularis muscles.3 Bergen, in a 1981 review article on the vasculature of the orbit, cited both Whitnall and Hayreh in regards to the infraorbital artery supply to the inferior rectus, inferior oblique, and lacrimal sac, without naming the orbital branch of the infraorbital artery.19 Both the Orbit

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Orbital Branch of the Infraorbital Artery Rootman et al.4 and Dutton5 atlases are relatively more recent publications that describe branches of the infraorbital artery that can cause substantial bleeding with complications. More recently, there have been a few case reports of postoperative complications resulting from interference with the orbital branch of the infraorbital artery during inferior orbital wall dissection, underscoring the importance of the surgeon’s familiarity with the anatomy of this vessel.8,9 Coulter et al.7 described a patient who experienced significant postoperative hemorrhage after orbital floor fracture repair causing a decrease in vision, swelling around the eye and intense nausea. The orbit was immediately reexplored and the orbital branch of the infraorbital artery, which had previously been cauterized, was causative. Rubin et al.8 also reported a case during which the orbital branch was damaged during surgery resulting in intraoperative hemorrhage and complicated cauterization. Most recently, Hwang et al.9 described postoperative hemorrhage after repair of a medial orbital wall fracture 15 hours after surgery. Immediate drainage and exploration revealed the bleeding branch. The universality of the perforating infraorbital bundle is not clear. We found it present in 8 of 9 orbits. Larger studies can help reveal if surgeons should expect to see this in every case. In addition, the presence of more than one structure (i.e., separate vein and artery) can lead to the cauterization of one, but not the other and can lead to bleeding complications. We emphasize that when operating in the inferior orbit, this neurovascular bundle should be anticipated and properly handled.

DECLARATION OF INTEREST The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

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REFERENCES 1. Zuckerkandl E. Zur Anatomie der Orbitalarterien. Med Jahr 1876;6:343. 2. Meyer F. Zur Anatomie der Orbitalarterien. Morph Jahrb 1887;12:414–458. 3. Hayreh SS. Arteries of the orbit in the human being. Br J Surg 1963;50:938–53. 4. Rootman J, Stewart B, Goldberg RA. Orbital Surgery: A Conceptual Approach. Philadelphia, PA: LippincottRaven, 1995. 5. Dutton JJ. Atlas of Clinical and Surgical Orbital Anatomy: Expert Consult. Philadealphia, PA: Saunders, 2011. 6. Whitnall S. Anatomy of the human orbit and accessory organs of vision. New York: Oxford University Press, 1979. 7. Coulter VL, Holds JB, Anderson RL. Avoiding complications of orbital surgery: the orbital branches of the infraorbital artery. Ophthalmic Surg 1990;21(2):141–3. 8. Rubin PAD, Hatton MP, Bilyk JR. Orbital perforating branch of the infraorbital artery: an important landmark in orbital surgery. Ophthal Plast Reconstr Surg 2005; 21(6):447–9. 9. Hwang K, Kim JH, Kang YH. Orbital hematoma caused by bleeding from orbital branch of the infraorbital artery after reconstruction of an orbital fracture. J Craniofac Surg 2014; 25(2):375–6. 10. Lemke B, Rocca R, Lisman R. Surgery of the Eyelids and Orbit: An Anatomical Approach and Reconstructive Surgery. Norwalk, Conn: Appleton & Lange, 1990. 11. Mausolf F. The Anatomy of the Ocular Adnexa: Guide to Orbital Dissection. Springfield, IL: Thomas, 1975. 12. Keating RF, Stewart WB, Toth BA. An Atlas of Orbitocranial Surgery. Boca Raton, FL: CRC Press, 1999. 13. Yen M. Surgery of the Eyelid, Lacrimal System, and Orbit. New York, NY: Oxford University Press, 2011. 14. Zide BM, Jelks GW. Surgical Anatomy of the Orbit. New York, NY: Raven Press; 1985. 15. Beard C. Anatomy of the orbit: a dissection manual. Birmingham, AL: Aesculapius Pub. Co.; 1977. 16. Wolff E, Bron A, Tripathi R, Tripathi B. Wolff’s Anatomy of the Eye and Orbit. 1997. 17. Doxanas MT, Anderson RL. Clinical Orbital Anatomy. Baltimore, MD: Williams and Wilkins, 1984. 18. Gray H. Anatomy of the Human Body. Philadelphia: Lea & Febiger, 1918. 19. Bergen MP. A literature review of the vascular system in the human orbit. Acta Morphol Neerl Scand 1981; 19(4):273–305.

Orbital Branch of the Infraorbital Artery: Further Characterization of an Important Surgical Landmark.

The orbital branch of the infraorbital artery, a key vascular structure that is not universally noted in orbital textbooks and atlases, is clinically ...
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