Distensible superficial venous orbital malformations involving the lower eyelid in two horses

Gareth D. Trope The Equine Centre, Veterinary Clinic and Hospital, University of Melbourne, Werribee, VIC 3030, Australia

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Catherine M. Steel The Equine Centre, Veterinary Clinic and Hospital, University of Melbourne, Werribee, VIC 3030, Australia

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John R. Bowers Equine Concepts, PO Box 36, Mount Martha, VIC 3934, Australia

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Leah A. Bradbury The Equine Centre, Veterinary Clinic and Hospital, University of Melbourne, Werribee, VIC 3030, Australia

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Priscilla J. Hodge Department of Pathology, University of Melbourne, Werribee, VIC 3030, Australia

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David J. Maggs Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616

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Abstract

Case Description—2 horses were examined because of vascular masses involving the lower eyelid.

Clinical Findings—Both horses had a unilateral, fluctuant mass involving the lower eyelid. For horse 1, the mass had been present since birth and had slowly increased in size over time. The mass also changed in size in response to various environmental stimuli, alterations in the position of the horse's head, and digital obstruction of superficial vessels adjacent to the mass. Horse 2 was brought to the hospital for euthanasia, and no historical or antemor-tem data were available. A combination of contrast angiography, Doppler ultrasonography, surgical exploration, and blood gas analysis (horse 1) and postmortem and histologic examination (horse 2) were used to determine that the masses consisted of non-neoplastic distended venous channels with anastomoses to the inferior lateral palpebral and angularis oculi veins (both horses) as well as the facial vein (horse 2). Histologic examination (horse 2) revealed large, endothelial cell-lined, blood-filled spaces within the deep dermis consistent with a distensible superficial venous orbital malformation.

Treatment and Outcome—Horse 1 underwent surgical exploration and ligation of the vascular malformation. Six months after surgery, the mass was markedly reduced in size, and size of the mass was static regardless of head position or environmental stimuli.

Clinical Relevance—Thorough preoperative planning with Doppler ultrasonography, contrast angiography, and blood gas analysis is recommended when attempting surgical correction of these malformations in horses. Surgical ligation can result in a successful cosmetic and functional outcome.

Abstract

Case Description—2 horses were examined because of vascular masses involving the lower eyelid.

Clinical Findings—Both horses had a unilateral, fluctuant mass involving the lower eyelid. For horse 1, the mass had been present since birth and had slowly increased in size over time. The mass also changed in size in response to various environmental stimuli, alterations in the position of the horse's head, and digital obstruction of superficial vessels adjacent to the mass. Horse 2 was brought to the hospital for euthanasia, and no historical or antemor-tem data were available. A combination of contrast angiography, Doppler ultrasonography, surgical exploration, and blood gas analysis (horse 1) and postmortem and histologic examination (horse 2) were used to determine that the masses consisted of non-neoplastic distended venous channels with anastomoses to the inferior lateral palpebral and angularis oculi veins (both horses) as well as the facial vein (horse 2). Histologic examination (horse 2) revealed large, endothelial cell-lined, blood-filled spaces within the deep dermis consistent with a distensible superficial venous orbital malformation.

Treatment and Outcome—Horse 1 underwent surgical exploration and ligation of the vascular malformation. Six months after surgery, the mass was markedly reduced in size, and size of the mass was static regardless of head position or environmental stimuli.

Clinical Relevance—Thorough preoperative planning with Doppler ultrasonography, contrast angiography, and blood gas analysis is recommended when attempting surgical correction of these malformations in horses. Surgical ligation can result in a successful cosmetic and functional outcome.

A25-year-old 515-kg (1,133-lb) Thoroughbred gelding (horse 1) used for general-purpose riding was examined at the University of Melbourne Equine Centre for a mass and a laceration, both involving the lower right eyelid. The mass had been present from birth, and the owner reported that its size had been static until 15 years of age but then had increased very slowly over the past 10 years. The eyelid laceration had occurred 3 weeks prior to examination. The horse had received no previous treatment for either lesion. Physical examination revealed that the horse was in good body condition, and results of physical examination were unremarkable other than the presence of marked facial asymmetry as a result of a tortuous, fluctuant, right eyelid mass (Figure 1). Medially, the mass appeared confluent with the angularis oculi vein, which was distended. The mass extended laterally adjacent to the lower eyelid from the medial canthus to approximately 5 cm lateral to the lateral canthus, where it appeared to merge with the transverse facial vein or one of its branches (ie, the inferior lateral palpebral vein). The position ranged from between 1 and 10 mm ventral to the eyelid margin. Although the length of the mass did not change, the diameter changed with certain stimuli. For example, the mass approximately doubled or tripled in diameter when the horse's head was lowered and decreased in diameter by approximately half when the head was raised. There was a similar but smaller change in size associated with environmental stimulation. The mass was largest after the horse was unloaded and placed in a stall. It then gradually reduced to about half the original size as the horse became calmer. The mass could also be caused to enlarge by application of firm digital pressure to obstruct the an-gularis oculi vein. Additionally, digital pressure intended to obstruct the lateral aspect of the vascular mass lateral to the lateral canthus of the eye caused partial collapse of the mass. At no time during the physical examination (ie, at rest, during any manipulations, or from any viewing angle) was the mass pulsatile.

Ophthalmic examination revealed that both eyes were open; no signs of ocular discomfort were evident. Upper eyelid carriage was symmetric OU; however, there was moderate to marked lower eyelid ectropion OD as a result of the mass and laceration. There was no ocular discharge, facial staining, or resting anisocoria. For both eyes, direct and consensual pupillary light reflexes were brisk and complete, menace responses and dazzle and palpebral reflexes were complete, and globe position and movements were normal. Both globes ret-ropulsed normally, and both bony orbits had no palpable abnormalities. The patient behaved as if sighted. Following sedation of the horse with detomidine (10 μg/kg [4.5 μg/lb], IV) and SC infusion of 2 mL of mepi-vacaine adjacent to the auriculopalpebral nerve OU, both eyes were examined by use of diffuse and focal light, slit-lamp biomicroscopy, and monocular indirect and direct ophthalmoscopy. Slit-lamp biomicroscopy was performed before and after pupil dilation. Oph-thalmoscopy was performed after pupil dilation. Both pupils dilated readily following 2 topical applications of 0.5% tropicamide ophthalmic solution.

In addition to the lower eyelid mass OD, there was a small melanotic dermal mass approximately midway along the upper eyelid about 2 to 4 mm dorsal to the eyelid margin (Figure 1). This mass was circular, approximately 2 mm in diameter, and raised < 1 mm. There was a partially healed and cicatrized laceration approximately centrally located on the lower eyelid. This was approximately 10 mm long and left a defect about 5 mm wide at the eyelid margin. It did not result in trichiasis. The upper and lower eyelids and third eyelid were otherwise grossly normal. There was no conjunctival or episcleral hyperemia and no chemosis. The precorneal tear film appeared adequate, and the cornea was clear. The sclera and corneoscleral limbus appeared normal, and the iridocorneal angle was visible and grossly normal laterally and medially. The anterior chamber was clear and deep; no flare or cells were detected. The iris and corpora nigra appeared normal. The lens was brunescent and had 3 to 4 microscopic punctate anterior cortical cataracts. The vitreous was unremarkable. Fundic examination after pupil dilation revealed 2 to 3 scattered tiny punctate regions of melanin migration interpreted as chorioretinal scars (bullet-hole lesions). The optic nerve head and retinal vasculature appeared normal. No abnormalities were detected OS other than lenticular brunescence, 3 to 4 punctate anterior cortical cataracts, and 2 to 3 scattered tiny punctate regions of melanin migration that were interpreted as chorioretinal scars. The intraocular pressure (measured after sedation of the horse and application of auriculopalpebral nerve blocks OU) was 18 mm Hg OS and 19 mm Hg OD. Neither cornea retained fluorescein stain. Fluorescein was not detected at either nasal opening within the first 5 minutes after topical application of fluorescein to each conjunctival fornix. Tentative clinical diagnoses included senile lenticular changes and chorioretinal scars OU, a solitary dermal mass involving the upper eyelid, chronic lower eyelid laceration, and a vascular mass or anomaly involving the lower eyelid OD.

Figure 1—
Figure 1—

Lateral view of the right eye and periocular tissues of a horse (horse 1) examined because of a laceration (arrow) and large mass involving the lower right eyelid and a small dermal mass approximately midway along the upper eyelid (arrowhead).

Citation: Journal of the American Veterinary Medical Association 237, 8; 10.2460/javma.237.8.943

After discussion with the owner, the horse was anesthetized for surgical correction of the eyelid laceration and further investigation of the vascular mass on the right lower eyelid. A 14-gauge, 5.25-inch IV cathetera was placed into the right jugular vein, and procaine penicillin (22 mg/kg [10 mg/lb], IM), gentamicin (6.6 mg/kg [3 mg/lb], IV), phenylbutazone (4.4 mg/kg [2 mg/lb], IV), and tetanus toxoid and antitoxin were administered. The horse was premedicated with acepromazine (0.03 mg/kg [0.014 mg/lb], IV) and romifidine (80 μg/kg [36 μg/lb], IV), and anesthesia was induced with ketamine (2.2 mg/kg [1 mg/lb], IV) and diazepam (0.05 mg/kg [0.023 mg/lb], IV) and maintained with isoflurane in oxygen following orotracheal intubation with a 24-mm-diameter endotracheal tube. Monitoring throughout the procedure consisted of pulse oximetry, direct arterial blood pressure measurement, capnography, end-tidal gas monitoring,b and blood gas analysis.c Mean arterial pressure was > 70 mm Hg throughout the procedure.

The horse was positioned in left lateral recumbency, and the surgical site was prepared aseptically. Blood samples were simultaneously collected from the dorsal metatarsal artery, cephalic vein, and eyelid mass into 3 heparinized syringes,d and the pH, Pco2, and Po2 were immediately analyzed.c When compared with Pvco2 and Pvo2 (59.1 and 297.8 mm Hg, respectively), and Paco2 and Pao2 (59.3 and 473.2 mm Hg, respectively), values for Pco2 and Po2 from blood drawn from the vascular mass (60.3 and 223.4 mm Hg, respectively) indicated that the mass likely contained venous blood and, therefore, was most likely a vascular anomaly. To facilitate contrast angiography, a 2-cm skin incision was made directly over the right transverse facial vein lateral to the lateral canthus of the eye, and the vein was identified and dissected free from surrounding soft tissue. Two ligatures of 3-0 poliglecaprone 25 were placed around the vein, and an 18-gauge, 5-cm IV cathetere was inserted into the vein and retained in place with preplaced ligatures. No change in the appearance of the mass was observed when the ligatures were tightened. Approximately 50 mL of iodinated contrast agentf was injected into the transverse facial vein via the catheter. On 2 occasions, skull radiographs were obtained during and immediately following injection of the contrast agent; however, no contrast was observed within the mass at any time.

A second 2-cm skin incision was made directly over the angularis oculi vein of the right eye, and the vein was ligated with 3-0 poliglecaprone 25. Again, no change in the appearance of the mass was observed following ligation of the angularis oculi vein. Ligatures placed around the transverse facial and angularis oculi veins were left in place in an attempt to reduce blood flow to the mass, to aid identification of other vessels supplying the mass, and to reduce the overall size of the mass for cosmesis. In a further attempt to localize and ligate the blood supply of this mass, a skin incision was made over the ventral margin of the mass approximately midway between the lateral and medial canthi of the eye. The mass was immediately subjacent to and intimately associated with the dermis, such that it was impossible to dissect it free. Numerous vessels potentially anastomosing with the mass were identified and ligated with 2-0 poliglecaprone 25; however, no reduction in mass size was observed. Therefore, all skin incisions were closed with 2-0 polypropylene in a simple interrupted pattern. The eyelid laceration was then débrided until wound edges were bleeding and was sutured closed with a standard 2-layer eyelid margin closure pattern. The subcutaneous and subcon-junctival tissues were closed with a horizontal mattress pattern with 4-0 polydioxanone. The skin was apposed with a figure eight suture pattern of 4-0 polypropylene. The horse recovered from anesthesia without complications. Postoperatively, the horse received procaine penicillin (22 mg/kg, IM) twice daily for 5 days and phenylbutazone (2.2 mg/kg, PO) twice daily for 7 days and then once daily for an additional 14 days. Topical ophthalmic antimicrobial ointment (neomycin, polymyxin, and bacitracin) was applied to the right eye twice daily for 10 days.

There was no obvious immediate postoperative change in the appearance of the mass. Therefore, ultrasonographic examination with a variable-frequency (7-to 12-MHz) linear transducerg and color flow Doppler ultrasonography were performed 2 and 6 days after surgery. No blood flow was detected within the mass on either occasion. However, the mass lumen was filled with hyperechoic, heterogeneous soft tissue consistent with a thrombus (Figure 2). Multiple small vessels superficial to the facial crest appeared to communicate with the mass caudally and ventrally. The communicating vessels could not be traced further ventrally or to their connections with deeper vascular structures. At the time the horse was discharged from the hospital 6 days after surgery, the mass was smaller than at the time of initial examination and was no longer fluctuant. In addition, changes in the horse's head position no longer altered the size of the mass. The eyelid laceration remained well apposed. Skin sutures were removed 14 days after surgery. Recheck examinations conducted 3 and 6 months postoperatively revealed that the dermal mass on the upper eyelid was unchanged, the lower eyelid laceration had completely healed, and the lower eyelid mass was notably smaller, such that the lower eyelid was resting normally on the cornea (Figure 3).

Figure 2—
Figure 2—

Ultrasonographic appearance of the lower eyelid mass in the horse in Figure 1 obtained 2 days after surgical exploration of the area. Notice the region of the mass containing a thrombus (dotted line). Color flow Doppler ultrasonography (evident as red and blue regions) revealed blood flow through an anastomosis leading to the thrombosed region of the mass.

Citation: Journal of the American Veterinary Medical Association 237, 8; 10.2460/javma.237.8.943

Figure 3—
Figure 3—

Lateral (A) and frontal (B) views of the horse in Figure 1 approximately 6 months after surgical exploration of the lower right eyelid mass. Notice that the mass is reduced in size, the lower eyelid laceration has healed, and there is good apposition of the lower right eyelid with the globe. The small dermal mass involving the upper eyelid appears unchanged (arrowhead).

Citation: Journal of the American Veterinary Medical Association 237, 8; 10.2460/javma.237.8.943

A 24-year-old Thoroughbred gelding (horse 2) was brought to the University of Melbourne Equine Centre hospital for euthanasia because of chronic weight loss and diarrhea. The horse had a mass involving the right lower eyelid that appeared similar to the lower eyelid mass described for horse 1 (Figure 4). No historical data were available, and a thorough ophthalmic examination of the horse was not performed. However, postmortem examination revealed that the mass consisted of a tortuous vascular structure closely apposed to the dermis. The mass appeared to extend between the inferior lateral palpebral vein at the lateral canthus and the angularis oculi vein at the medial canthus. Additionally, a thin-walled blood vessel extended between the mass and the facial vein near the junction of the facial vein with the transverse facial venous sinus and deep facial venous sinus (Figure 5). No communication between the eyelid mass and the transverse facial venous sinus was evident at the caudal extent of the lateral canthus of the eye. A sample of the mass and closely apposed skin was placed in 10% formalin solution and processed for histologic examination. Microscopic examination of the mass revealed large blood-filled spaces within the deep dermis adjacent to sinus hairs (vibrissae) but deep to adnexal and glandular structures (Figure 6). The largest of these blood-filled spaces was 3.5 × 2.5 mm; all were lined by a single layer of endothelial cells. Thrombi were not seen in these blood-filled spaces.

Figure 4—
Figure 4—

Postmortem lateral view of the right eye and periocular tissues of a horse (horse 2) examined because of chronic weight loss. Notice the mass that extends between the transverse facial vein or one of its branches (asterisk) and the angularis oculi vein (arrowhead), both of which appear somewhat distended. Additionally, a subcutaneous vessel can be seen extending rostrally and ventrally from the mass (arrows).

Citation: Journal of the American Veterinary Medical Association 237, 8; 10.2460/javma.237.8.943

Figure 5—
Figure 5—

Diagram of the lower eyelid mass and associated blood vessels of the horse in Figure 4. The mass appeared to extend between the inferior lateral palpebral vein and the angularis oculi vein. Additionally, a thin-walled blood vessel (asterisk) extended between the mass and the facial vein.

Citation: Journal of the American Veterinary Medical Association 237, 8; 10.2460/javma.237.8.943

Figure 6—
Figure 6—

Photomicrograph of a portion of the lower eyelid mass from the horse in Figure 4. Notice the large, partially blood-filled space (arrow) in the dermis adjacent to sinus hairs (vibrissae) beneath adnexal and glandular structures (A). H&E stain; bar = 500 μm. The space is lined by a single layer of endothelial cells (asterisk; B). H&E stain; bar = 50 μm.

Citation: Journal of the American Veterinary Medical Association 237, 8; 10.2460/javma.237.8.943

Discussion

On the basis of physical, ultrasonographic, and his-topathologic findings; results of blood gas analyses; and response to surgery, we believe that the 2 horses described in the present report had superficial venous orbital malformations involving the lower eyelid. In both horses, these malformations most likely originated medially from the angularis oculi vein and laterally from the transverse facial vein or one of its branches (ie, the inferior lateral palpebral vein).

To our knowledge, periocular vascular malformations have been rarely described in the veterinary literature, with prior reports describing orbital varices in 2 dogs1,2 and an iguana.3 In humans, malformations of the angularis oculi vein and of the veins within the orbit have been described, albeit uncommonly.4–9 In human patients, orbital varices have been classified as distensible or nondistensible and as superficial or deep,10 with superficial venous orbital malformations involving the periorbital skin, conjunctiva, or eyelid without extension of the malformation posterior to the equator of the globe and deep venous orbital malformations involving the orbit posterior to the equator of the globe.11,12 On the basis of this classification system, we believe that the masses identified in the horses described in the present report represent distensible, superficial venous orbital malformations.

The pathogenesis of orbital vascular malformations is unclear. Vascular malformations are defined as structural anomalies of blood vessels resulting from errors during embryological development.11 In humans, these occur during the 4th to 10th weeks of gestation. It is believed that the location, distribution, and extent of these lesions are affected by various local physio-chemical or neural influences.11 Depending on hemodynamic flow characteristics, it has been proposed that they be classified as no flow, venous flow, or arterial flow malformations.10 Venous flow malformations (also known as primary varices) can be further classified as distensible or nondistensible. Arterial flow malformations (also known as secondary varices) represent normal veins that have expanded under arterial pressure in the absence of intervening capillary beds that otherwise would dissipate the pressure.10 For horse 1, the owner reported that the malformation had been present since birth, blood gas analysis revealed that it contained venous blood, and postoperative Doppler ultrasonography revealed communication with deeper vascular structures. In horse 2, postmortem examination revealed that the malformation formed an anastomosis between the inferior lateral palpebral vein, an-gularis oculi vein, and facial vein, without any arterial relationship. Taken together, these findings suggest that both horses described in the present report had primary venous malformations that likely arose from anatomic variations resulting in abnormal venous anastomoses.

Histologic examination of orbital vascular malformations in humans reveals dilated irregular veins lined by a single layer of endothelium with or without thrombi.6,8,12 Distensible and nondistensible lesions do not appear to differ in appearance greatly. The histologic findings in horse 2 appeared similar to those reported for similar malformations in people,6,8,12 although the tortuous nature of the vessels was not appreciable in the cross sections reviewed. Although a previous report3 described the histo-logic appearance of an orbital varix in an iguana, we are unaware of any other reports of the histologic appearance of vascular malformations in animals.

In humans and animals with orbital vascular malformations, the diagnosis has been made with a combination of radiography, Doppler ultrasonography, contrast angiography, computed tomography, and magnetic resonance imaging.1–3,13–15 Some of these techniques were also useful in horse 1 in the present report. Contrast an-giography was attempted intraoperatively; however, no contrast was observed within the malformation. This may have been because multiple venous anastomoses within the malformation allowed rapid removal of the contrast material into the circulation or because of inadequate coordination of injection of the contrast agent and radiographic exposure. Fluoroscopy, had it been available, would likely have overcome these limitations. Although postoperative Doppler ultrasonography was useful in horse 1, a preoperative assessment should also have been performed, as it likely would have allowed identification of the numerous anastomoses within the malformation and permitted more extensive pre-operative planning. Likewise, we would recommend that blood gas analysis be conducted preoperatively in patients with vascular anomalies to better characterize their vascular origin.

Treatment of orbital vascular malformations varies depending on the location and degree of distensibility of the malformation.12 Reported methods of treatment include surgical excision via orbitotomy,16 enucleation,3 embolization with silastic liquid4 or microcoils,2,17 carbon dioxide laser ablation,12 and percutaneous alcohol sclerotherapy.12 Treatment of horse 1 in the present report was aimed at reduction in size and weight of the mass so that the eyelid laceration could be corrected and eyelid function and apposition with the globe could be improved. We suspect that after ligation of the vessels supplying the malformation, a decrease in blood flow was achieved that resulted in thrombosis, fibrosis, and ultimately contraction and reduction in size of the mass over the 6 months after surgery. Complete resection was not possible because of the lack of mobile adjacent tissue in the lower eyelid, and many of the alternative treatment modalities were not available. Intraluminal sclerotherapy seemed unlikely to be successful in this horse because of the size, tortuosity, and extent of blood flow through the mass, which likely would have caused marked dilution of any material that was injected and could have caused systemic toxicosis. Therefore, reduction of blood flow within the vascular mass via ligation, thrombosis, and fibrosis was the therapeutic goal in this horse. Although resolution was slow, a cosmetic and functional outcome was achieved.

ABBREVIATIONS

OD

Oculus dexter (right eye) OS Oculus sinister (left eye)

OU

Oculi uterque (both eyes)

a.

Angiocath, Becton Dickinson Infusion Therapy Systems Inc, Sandy, Utah.

b.

Mindray PM 9000, Shenzhen Mindray Bio-Medical Electronics, Shenzhen, China.

c.

ABL 625, Radiometer, Brønshøj, Denmark.

d.

PICO50, Radiometer, Brønshøj, Denmark.

e.

Optiva, Medex Medical Ltd, Rossendale, Lancashire, England.

f.

Omnipaque (240 mg/mL), GE Healthcare Pty Ltd, Rydalmere, NSW, Australia.

g.

Acuson Aspen, Siemens, Munich, Germany.

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