Arteriovenous Malformation of the Tongue Resulting in Recurrent Severe Hemorrhage in a Young Dog
ABSTRACT
An 8 mo old male entire beagle was presented to the emergency and critical care service following several severe bleeding episodes from the oral cavity. Oral examination revealed a purple, spongy, pulsatile lesion on the rostral two-thirds of the tongue. Computed tomography angiography revealed a severely distended right linguofacial vein with numerous, tortuous branching vessels within the tongue, consistent with an arteriovenous (AV) malformation. A cervical surgical approach was performed, and the right lingual artery was isolated and catheterized. A direct arteriogram confirmed this was the main feeder artery to the lesion, and it was ligated. Although the bleeding episodes initially resolved, a moderate bleeding episode occurred 6 days postoperatively, and a partial glossectomy was performed. Histopathology was consistent with an AV malformation. The dog had a good recovery from surgery and remains free of clinical signs 13 mo later. Following extensive review of the veterinary literature, this is the only reported case of a lingual AV malformation in the dog. Partial glossectomy resulted in resolution of the clinical signs and was well tolerated. Although rare, AV malformations should be considered as a differential diagnosis for spontaneous oropharyngeal bleeding.
Introduction
Vascular malformations are uncommon in all species and are considered a subcategory of vascular anomalies.1,2 Several cases of arteriovenous (AV) malformations and AV fistulae have been described in the veterinary literature.2–12 Treatments reported to date include ligation of the feeding vessel; embolization of the feeding vessel with liquid, glue, or a coil; or surgical resection with or without prior embolization.2–12 The following case report describes an unusual cause of spontaneous oropharyngeal bleeding in a young dog, successfully treated with complete excision of the lesion via partial glossectomy.
Case Report
An 8 mo old male intact 11.4 kg beagle presented to our emergency and critical care service following severe spontaneous bleeding from the oral cavity. A dark area at the rostral edge of his tongue had been noted when he was acquired by the owners at 8 wk of age. The dog had a 5 mo history of minor, spontaneous, self-resolving bleeds from the oral cavity, typically during eating or when chewing on toys. These episodes occurred approximately every 7 to 10 days, would self-resolve within 2 to 3 days, and had been assumed to be caused by teething. On the morning of presentation, the dog had three major bleeds from the oral cavity and collapsed. He was taken to his referring veterinarian where initial diagnostics revealed a packed cell volume (PCV) of 14% and an in-house partial thromboplastin time and activated partial thromboplastin time within normal limits. He was given a 5 mL/kg bolus of crystalloid fluids and referred for further stabilization and investigation. On presentation to our hospital, he was quiet but responsive, with white, tacky mucous membranes. He was tachycardic (heart rate 160 beats per min) with a grade III/VI systolic murmur. A purple/red lesion was noted at the rostral edge of the tongue. His general physical examination was otherwise unremarkable. Point-of-care ultrasound of the thorax and abdomen confirmed no free pleural or abdominal fluid. His PCV was 11% and total solids (TS) 48 g/L. Venous blood gas analysis revealed a hyperlactatemia (lactate 5.5 mmol/L, reference interval: 0.6–2.5 mmol/L). Hematology revealed a decreased red blood cell count (1.53 × 1012/L, reference interval: 5.5–8.5 × 1012/L), decreased hemoglobin (2.5 g/dL, reference interval: 12–18 g/dL), and decreased hematocrit (8.7%, reference interval: 37–55%), with a blood smear indicating marked anemia with strong evidence of regeneration and iron deficiency, consistent with chronic blood loss. Biochemistry revealed a decreased total protein (39.9 g/L, reference interval: 54.9–75.3 g/L), decreased albumin (18.8 g/L, reference interval: 26.3–38.2 g/L), decreased globulin (21.1 g/L, reference interval: 23.4–42.2 g/L), and mildly elevated urea (11.2 mmol/L, reference interval: 3.1–10.1 mmol/L). Angio Detect testa for Angiostrongylus vasorum was negative. SNAP 4Dxb for Ehrlichia canis, Ehrlichia ewingii, Borrelia burgdorferi, Anaplasma phagocytophilum, Anaplasma platys, and Dirofilaria immitis was also negative.
Two 10 mL/kg boluses of a balanced, isotonic crystalloid solution were given over 30 min, and a transfusion of a single unit of canine packed red blood cells (330 mL, 28.9 mL/kg) was administered based on blood type (DEA 1 positive). A further profuse bleeding episode occurred in the hospital several hours after admission and a second unit of packed red blood cells (290 mL, 25.4 mL/kg) was administered, followed by a unit of fresh frozen plasma (120 mL, 10.9 mL/kg). The following morning, the PCV and TS were 14% and 45 g/L, respectively. The dog was anesthetized and examination of the oral cavity revealed a purple, spongy, pulsatile lesion on the rostral two-thirds of the tongue, extending further caudally on the right side (Figure 1). Computed tomography angiography of the head and neck was performed, which showed a severely distended right linguofacial vein, measuring 6 mm as it branched from the jugular vein and 13 mm at its largest diameter at the caudal aspect of the mandible. In contrast, the right linguofacial vein measured 1.2 mm at its largest diameter. Within the tongue, numerous tortuous enlarged vessels were seen (Figure 2). Lymph nodes were within normal size and no other abnormalities were visualized.
Citation: Journal of the American Animal Hospital Association 56, 6; 10.5326/JAAHA-MS-7080
Citation: Journal of the American Animal Hospital Association 56, 6; 10.5326/JAAHA-MS-7080
An AV malformation was diagnosed on the basis of the computed tomography angiography, and options for further treatment were discussed with the owners. These included ligation or embolization of the main feeder artery to the lesion (right lingual artery), right common carotid artery ligation, or partial glossectomy. Given the caudal extent of the lesion, and the dog’s age, the owners elected to attempt ligation of the lingual artery as a first-line treatment. An unknown prognosis with this technique was given to the owners.
The dog was anesthetized and prepared for surgery. He was placed in dorsal recumbency with a sandbag under the nose and neck. The distended right linguofacial vein was easily visualized sitting just under the skin. A ventral approach was made on the right medial aspect of the mandible, from the mid mandible to the mid cervical region. The approach continued on the medial aspect of the severely distended right linguofacial vein. This vein was carefully dissected toward the caudal aspect of the incision to allow its retraction with a silicone vessel loop. The right common carotid artery was isolated with silicone vessel loops at the rostral and caudal aspects of the right lingual artery branch. A 20 G IV catheter was inserted into the lingual artery and contrast fluoroscopy using Iohexolc 300 mgI/mL was performed, confirming this vessel to be the main feeder artery to the malformation. This vessel (the right lingual artery) was ligated with two 3-0 polypropylened and two 3-0 Polydiaxononee sutures. A routine closure was then performed.
The dog recovered well from surgery and initially no bleeding episodes occurred. He was discharged 2 days postoperatively with a 5-day course of oral paracetamol (10 mg/kg q 12 hr), soft food, and monitoring instructions.
Six days postoperatively, a mild amount of bleeding occurred when the dog was found to be chewing his bed, which quickly resolved but led to multiple small bleeds throughout that day. Eleven days postoperatively, a severe oral bleeding episode occurred and the dog was readmitted. On presentation his PCV was 10% and TS 48 g/L. A transfusion of canine packed red blood cells was administered after a cross match had been performed. After discussion with the owners, a partial glossectomy was performed the following day. The patient was anesthetized and placed in sternal recumbency with the maxilla suspended between two drip stands. A V-shaped incision was made in the tongue, removing the grossly abnormal areas; this resulted in removal of approximately two-thirds of the tongue. The dorsal and ventral mucosal edges were apposed with simple interrupted 3-0 Polyglactin 910f sutures (Figure 3).
Citation: Journal of the American Animal Hospital Association 56, 6; 10.5326/JAAHA-MS-7080
The resected tissue was submitted for histological evaluation, and the report indicated an extensive vascular proliferation in the subepithelial stroma, with focal epithelial ulceration and adjacent vascular thrombosis. Microscopic examination confirmed the presence of numerous variably sized, tortuous arterioles and venules, admixed with clusters of capillary vessels, consistent with an AV malformation or, less likely, a hemangioma (Figure 4).
Citation: Journal of the American Animal Hospital Association 56, 6; 10.5326/JAAHA-MS-7080
The dog remained in the hospital for 7 days postoperatively to ensure adaption to eating was sufficient prior to discharge. The partial glossectomy was well tolerated, and at the time of discharge, he was able to eat soft food balls from a raised bowl and drink from a deep bowl. At re-examination 1 mo postoperatively, the dog was reported to be doing well. Eating and drinking abilities had improved with continuation of offering from raised bowls. Halitosis had been noted by the owners, and some tartar was noted on the teeth. The only abnormality reported by the owners was saliva leaking from the oral cavity. No abnormalities were present on general physical examination, and on conscious oral examination, the surgical site had healed well. By 3 mo postoperatively, the owners reported that the dog was eating and drinking well with self-adaption of throwing balls of food into the back of his mouth and swallowing. He was reported to be bright, lively, and back to behaving like a normal puppy, with resolution of the previous saliva leakage. At 13 mo postoperatively, the owner reported no further bleeding episodes and an excellent quality of life.
Discussion
Vascular malformations are a subcategory of vascular anomalies, with the other major subcategory being neoplastic or neoplastic-like lesions, often called hemangiomas.1,2 Vascular malformations are always present at birth, grow with the individual, and never regress.13 Conversely, hemangiomas are not present at birth, grow rapidly during a proliferative phase, go through a period of stabilization, and then involute.13 Vascular malformations are composed of mature endothelium that does not undergo tumor-like endothelial proliferation. Glucose transporter protein-1 immunostaining has been used in human pathology to differentiate these from hemangiomas.14
Several classification systems have been described in the human literature to categorize a variety of documented vascular malformations. The modified Hamburg classification system is thought to be the most accepted system and considered a primary classification based on whether a malformation is capillary, venous, arterial, lymphatic, or combined vascular.15 Subclassification is then established based on embryological characteristics, with the two major categories being extratruncular and truncular.15 Extratruncular and truncular forms are characterized based on the time at which the defect occurred in embryogenesis; extratruncular lesions arise when developmental arrest occurs in the earlier stage of embryonic life, when the vascular system is in the reticular stage. Truncular forms occur when developmental arrest occurs at the vascular trunk formation period, at a later stage of embryonic development.15 Arteriovenous malformations that are truncular often result in aplasia or obstruction, whereas extratruncular forms are infiltrating.15 Another classification scheme complementary to the endothelial classification system classifies AV malformations based on the identification of their rate of blood flow.16 In that scheme, vascular malformations are classified into low-flow (venous) and high-flow (AV) malformations.16 Although a classification system for vascular malformations in dogs has not been reported, some of the principles of the human classification system can be applied to this case. Based on these, the vascular anomaly seen in the dog described here would be classified as an AV malformation with high flow rates and extratruncular characteristics owing to its infiltrative nature. In humans, the importance of classification lies in the ability to help guide clinical decision making; transcatheter embolization or surgical resection is the treatment of choice for high-flow AV malformations, whereas percutaneous treatment with a sclerosing agent is recommended for low-flow vascular malformations.17
Congenital hepatic AV malformations are the most commonly reported AV malformations in the veterinary literature, but acquired cases secondary to trauma (surgical and other forms) and neoplasia have also been reported.2–12 Treatments reported to date include ligation of the feeding vessel; embolization of the feeding vessel with liquid, glue, or a coil; or surgical resection with or without prior embolization.2–12 Embolization was discussed as a treatment option for this case as it has been successfully performed in veterinary species for treatment of AV malformations.2,3,8,11 Although transcatheter embolization is the treatment of choice for high-flow AV malformations in humans,17 embolization alone has not been found to be curative in certain cases.14 A review of the literature regarding lingual vascular malformations in humans suggests that surgical resection with or without prior transcatheter embolization to reduce intraoperative hemorrhage would be the treatment of choice for the majority of cases.14
In the case reported here, ligation of the lingual artery did not result in medium- or long-term resolution of the clinical signs. This was not completely unexpected because the right and left lingual arteries anastomose throughout the parenchyma of the tongue muscle. Indeed, disruption of flow through one artery has been shown to have no significant effect on blood flow.18 However, surgical resection via partial glossectomy is an invasive surgery and can have a significant impact on quality of life. Given the dog’s young age, the owners elected to try a less invasive option first. Although this did not resolve the symptoms other than in the very short term, partial glossectomy has resulted in a good long-term outcome to date.
AV malformations of the tongue have not been previously reported in veterinary patients. A single case series describing AV hemangiomas in two dogs and one cat reported one case of a lingual hemangioma that was managed by surgical resection.19 The lesions described in that case series were focal masses seen in mature animals. In contrast, the case described here was seen in a very young animal and was much more locally extensive, suggestive of an AV malformation rather than a hemangioma.
Arteriovenous malformations of the tongue are rarely reported in humans and are often compartmentalized into the context of larger head and neck vascular malformations.14 A recent case series describes 11 lingual AV malformations in humans, 4 with evidence of upper neck and mouth involvement and 7 focal lingual masses.14 Presenting clinical signs included sudden enlargement of a previously detected lesion and spontaneous bleeding.14 Age of presentation for the focal AV malformations ranged from 6 mo to 41 yr, with the majority of lesions described as hyperemic and firm with a clear border.14 They were found to have a single feeder lingual artery on angiography in the majority of cases, similar to the one described here, and were all treated with surgical resection of the affected tissue, with only one case having embolization of the feeder vessel preoperatively (in order to reduce intraoperative bleeding).14 The more complex malformations involving the neck and mouth required extensive surgery for removal of the affected tissue, with a mean operating time of 11 hr.14 Two out of four cases experienced recurrence within 2 mo, requiring further surgical intervention.14
Conclusion
Although rare, AV malformations should be considered as a differential diagnosis for spontaneous oropharyngeal bleeding, especially in younger dogs.
The dorsal aspect of the tongue showing the lesion on the rostral two-thirds, extending caudally on the right side.
A dorsal plane 3D volume-rendered computed tomography angiography image of the severely distended right linguofacial vein (*) as it branches from the right external jugular vein (†) and the tortuous branching vessels within the tongue (diamond). The normal left linguofacial vein (arrow) and the internal jugular veins (arrowheads) are labeled.
Image showing the dorsal surface of the tongue following glossectomy as the final sutures are being placed.
Dorsal aspect of the tongue showing increased numbers of variably sized, irregular, blood-containing vascular spaces lined by flat endothelium including arterioles (*), venules (†), and capillaries (‡). Hematoxylin and eosin stain; bar = 50 µm.
Contributor Notes
AV (arteriovenous); PCV (packed cell volume); TS (total solids)
