A 13-year-old neutered male Abyssinian cat was evaluated by its primary care veterinarian because of multiple scab lesions over the distal aspect of the right forelimb that hemorrhaged after grooming. The lesions had persisted for several weeks and were attributed to trauma from regular rough play with the family dog. The physical examination identified generalized edema of the right forelimb distal to the elbow joint, with multifocal sanguineous crusting lesions confined to the craniomedial aspect of the distal part of the antebrachium. Hemorrhage from one of these lesions was described as continuous and spurting and required direct pressure, skin sutures, and a bandage to achieve hemostasis. A pulsatile mass of soft tissue consistency was detected over the cranial aspect of the right elbow joint. No comorbidities were identified during the physical examination. A CBC revealed a mild regenerative anemia (Hct, 23% [reference range, 24% to 45%]; hemoglobin concentration, 69 g/L [reference range, 80 to 150 g/L], reticulocyte count, 77 × 109 cells/L [reference range, < 60 × 109 cells/L]), and results of coagulation tests, urinalysis, and radiographic examination of the right forelimb did not suggest an underlying etiopathogenesis for the lesions.
Over the following 6 weeks, the integument lesions and edema persisted without detectable improvement or deterioration. Episodes of hemorrhage frequently followed grooming. Antimicrobial treatments (amoxicillin–clavulanic acida [16.9 mg/kg {7.7 mg/lb}, PO, q 12 h] and clindamycin hydrochlorideb [3.4 mg/kg {1.5 mg/lb}, PO, q 24 h]) and a steroid-antihistamine combinationc (prednisolone–chlorphe-niramine maleate [0.34 mg/kg {0.15 mg/lb}, PO, q 24 h]) were prescribed with no obvious improvement in clinical signs. Further diagnostic testing included a repeated CBC, serum biochemical analysis, and testing for FIV and FeLV. The results were unremarkable. A biopsy sample of affected skin distal to the mass was obtained and submitted to a veterinary pathology laboratory. On histologic examination, the dermis was found to contain numerous cross sections and tangential sections of disorganized small arteries with thickened tunica muscularis (Figure 1). Focally, extensive erosion of the epidermis with replacement by serocellular coagulum was identified. The remaining epidermis in the sample was moderately hyperplastic. The dermis was multifocally fibrotic with microhemorrhage containing numerous mast cells, eosinophils, and neutrophils. These dermatologic alterations reflected atypical dermal hemodynamics, hypertension, and secondary inflammation. An AVF was identified by the veterinary pathologist as a potential cause for the histologic findings.
Photomicrograph of a skin biopsy sample from a region superficial and distal to a pulsatile subcutaneous soft tissue mass proximal to the right elbow joint in a 13-year-old Abyssinian cat. The cat had sanguineous crusting skin lesions with intermittent episodes of hemorrhage on the craniomedial aspect of the right antebrachium. Biopsy was performed approximately 9 weeks after the reported onset of skin lesions. The epidermis is located at the top right of the image. Notice the dysplastic and tortuous arterial structures (asterisks) with markedly thickened tunica media. Arrows indicate dermal arteries with normal tunica media thickness. H&E stain; bar = 200 μm.
Citation: Journal of the American Veterinary Medical Association 254, 3; 10.2460/javma.254.3.393
Owing to the cat's poor response to treatment, a veterinarian specializing in feline medicine was consulted. Amputation of the affected forelimb or referral for advanced imaging was offered. The cat was subsequently referred to Massey University Veterinary Teaching Hospital for advanced imaging and surgical consultation.
On physical examination at the teaching hospital, the cat was ambulatory without detectable lameness. Diffuse pitting edema encompassed the right forelimb distal to the elbow joint, with multifocal, 3- to 4-mm-diameter sanguineous crusting lesions distributed throughout the skin over craniomedial regions of the antebrachium, carpus, and digits. A subcutaneous, fixed, pulsatile mass (approx 0.8 × 2.5 cm) was noted over the proximal craniolateral aspect of the right elbow joint; on palpation, a thrill was detected directly over the structure. An audible bruit was auscultated at the location of the palpable thrill. No scar or evidence of previous trauma was found at the site. The right prescapular lymph node was deemed mildly enlarged on palpation. No other clinically important abnormalities were identified on physical examination.
Under general anesthesia, the cat was placed in sternal recumbency with its forelimbs extended for nonselective contrast-enhanced CT angiography of both forelimbs. Iodinated contrast mediumd (880 mg of I/kg [400 mg of I/lb]) was administered into the right medial saphenous vein via a 22-gauge IV catheter with a firm push by hand. Two sequences were performede approximately 5 and 30 seconds after the initiation of contrast medium administration. Three-dimensional rendering was used to investigate vascularity of the mass and to identify associated supplying and draining vessels.
An extensive network of dilatated and tortuous vessels was visualized on the cranial aspect of the right forelimb proximal and medial to the elbow joint, consistent with the location of the cephalic and median cubital veins (Figure 2). A large aberrant vessel was identified diverging from the distended brachial artery just proximal to the supracondylar foramen, through which a vessel considered to be an extension of the brachial artery coursed. This anomalous vessel was noted coursing caudodistally around the distomedial aspect of the humerus in close association with the brachial vein. From this location, the vessel emerged, extending in a convoluted path consistent with that of the median cubital vein, to join the cephalic vein at the level of the elbow joint. An AVF was thought to be present within this medial vascular bundle involving the median cubital vein, brachial vein, and brachial artery. However, because of the chronicity of the condition and the substantial alterations in vascular anatomy, it proved impossible to determine the precise location of the AVF within the visible vascular derangements. The distal aspect of the cephalic vein was dilatated and had a tortuous course with multiple small vessels extending from it into surrounding subcutaneous tissue, consistent with venous arterialization.
Results of contrast-enhanced CT angiography of the cat in Figure 1 with 3-D reconstruction. In the craniomedial-caudolateral oblique view of the right forelimb, the presumed origin of the AVF branches from the brachial artery proximal to its course through the supracondylar foramen (arrow). The dilatated and tortuous nature of the median cubital vein (asterisk) is visualized in addition to secondary changes associated with the brachial artery and vein (single dagger) and cephalic vein (double dagger), which was thought to be arterialized. In the lateromedial view of the patient's left forelimb, the vascular anatomy is depicted to enable comparison. The brachial artery and vein (single dagger), cephalic vein (double dagger), and median cubital vein (asterisk) are labeled for reference. L = Left. R = Right.
Citation: Journal of the American Veterinary Medical Association 254, 3; 10.2460/javma.254.3.393
The proximal region of the affected forelimb was clipped of hair and aseptically prepared for surgery. An approximately 6-cm skin incision was made on the craniolateral aspect of the limb. The incision was centered approximately 1.5 cm lateral to the palpable AVF to avoid iatrogenic trauma to the vascular structure. The subcutaneous tissue was bluntly dissected away from the AVF. An attempt to isolate the arteriovenous communication was ineffective owing to the presence of dense fibrous tissue. Considering the potential risks of severe hemorrhage and disruption of the arterial supply to the distal limb, the surgeon (AJW) chose to isolate and ligate the large venous structure coursing from the AVF distally over the cranial aspect of the antebrachium. This was suspected to be the arterialized cephalic vein. Approximately 1.5 cm distal to the AVF, the vessel was isolated from the surrounding dense fibrous tissue by means of blunt dissection. Once this part of the vein was dissected free, a hemostat was applied to create a crush mark for seating the ligature. Following removal of the hemostat, the vessel was ligated with 2–0 polypropylene without transection. The subcutaneous tissue was closed with 4–0 poliglecaprone 25 in a simple continuous pattern, and the skin was closed with 4–0 poliglecaprone 25 in a continuous intradermal pattern.
After surgery, a thrill and bruit were detected as previously described dorsal to the structure, suggesting continued flow through the AVF. The cat recovered uneventfully from general anesthesia. Buprenorphinef (0.02 mg/kg [0.009 mg/lb]) was administered SC, followed by transmucosal administration every 8 hours. The cat was hospitalized for observation for 4 days after surgery. Mild postoperative swelling at the surgical site and persistent edema were noted, but no other abnormalities were detected. The cat was discharged from the hospital on the fifth day, and the owners were advised to restrict its activity and to schedule a recheck examination with the primary care veterinarian. At the time of discharge, no obvious reduction in limb edema was seen.
On follow-up, the owner reported that the diffuse limb swelling had progressively resolved within 5 days after the cat was discharged from the hospital, and all superficial skin lesions had healed within 2 weeks after surgery. No new lesions or episodes of hemorrhage occurred following surgery.
Five months after surgical intervention, the cat was reassessed at the teaching hospital. On examination of the right forelimb, no audible bruit, palpable thrill, or superficial lesions were noted. Palpation of the limb did not elicit behavioral signs of discomfort, and no detectable edema was present. A small, firm, soft tissue structure that measured approximately 0.6 × 1.0 cm was palpated approximately 0.5 cm proximal to the level of the elbow joint on the cranial surface of the limb. No abnormalities were identified on blood pressure measurement, thoracic auscultation, or echocardiographic evaluation.
Both forelimbs were reexamined with nonselective contrast-enhanced CT angiography as previously described, and views were compared with an image obtained prior to surgery (Figure 3). The large aggregate of dilatated tortuous vessels was no longer present in the right forelimb. A vascular structure thought to be the cephalic vein ended abruptly in the proximal region of the antebrachium at the site of the surgical ligation. Venous return appeared to occur predominantly through the median and brachial veins. These vessels were considered to be of appropriate size, compared with the vascular structures of the contralateral forelimb in this patient.
Preoperative craniocaudal (A) and follow-up craniocaudal (B) and craniomedial-caudolateral oblique (C) contrast-enhanced CT angiography images of the right forelimb of the cat in Figure 1 with 3-D reconstruction. Follow-up images were obtained at a recheck examination 5 months after surgery. The site of surgical ligation distal to the vascular mass is indicated (arrows). In the postoperative images, the aggregate of previously noted dilatated tortuous vessels is no longer evident. Vascular perfusion of the distal aspect of the antebrachium appeared adequate. See Figure 2 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 254, 3; 10.2460/javma.254.3.393
Discussion
Congenital and acquired AVFs have been described in various locations in dogs and cats. The congenital form of AVF is most commonly reported, and these are typically associated with hepatic and cardiac vasculature following a failure of embryonic structure differentiation.1,2 Less commonly, AVFs are acquired, and these develop predominantly in the extremities.3–10 Acquired peripheral AVFs are typically the result of trauma,3,11 with various sources of vascular injury proposed, including blunt12 and penetrating trauma,13,14 vascular catheterization, extravascular injection of irritant drugs,15 erosion and rupture of an aneurysm, iatrogenic occlusion by en bloc ligation,7,16 and neoplasia.3–5,17 Clinical reports5,7,13,18,19 of peripheral AVFs in cats are infrequent, but proposed causes for these anomalies have included trauma associated with onychectomy7 or bite wounds.7,18 In 1 case, peripheral AVF was associated with a subcutaneous hemangiosarcoma.5 The cause of the AVF in the cat of the present report was undetermined; however, the location was considered consistent with trauma to the brachial artery just proximal to the elbow.
When an AVF forms, blood is preferentially diverted away from a high-resistance capillary bed, shunting into the associated low-pressure venous system. This results in a decrease in arterial pressure sensed proximally by homeostatic arterial baroreceptors.3 Activation of the autonomic, sympathoadrenal, and renin-angiotensin-aldosterone systems can result in increased heart rate and stroke volume, peripheral vasoconstriction, and increased circulating blood volume, respectively.3,20 The magnitude of hemodynamic changes and associated clinical signs appears to be influenced by AVF characteristics including location, size, structure, extent of supplying and draining vasculature, and adequacy of collateral circulation.3,11,12,20–23 Patients with AVFs are predisposed to volume overload, pulmonary hypertension, and high-output cardiac failure, with large centrally located fistulae causing more severe cardiovascular effects.3,11,20,22,24
Peripheral AVFs are associated with various clinical signs reflecting local hypertension, impeded blood flow, and hypoxia.3,24 These clinical signs can include hypertrophy of the affected limb, localized hyperthermia, cellulitis, edema, lameness or other signs of pain, cyanosis, ischemia, superficial integument ulceration, and recurrent hemorrhage.3–5,21,24 Physical examination findings characteristic for AVFs include a palpable thrill, audible bruit, and the detection of a Nicoladoni-Branham sign,3 a vagally induced bradycardia observed on mechanical occlusion of an AVF that is considered to be almost pathognomonic for the condition. A bruit generally results from a disruption of the normal laminar blood flow that causes eddies to occur. Although a thrill and a bruit were identified in in the cat of this report, a Nicoladoni-Branham sign was not detected.
Various imaging methods can be used to detect AVFs; however, contrast-enhanced angiography is considered the most important aid in diagnosis and evaluation of the condition in people and nonhuman animals.3,4,11 In early reports, diagnosis in dogs and cats was made via nonselective2,25 or selective6,7,12,14 contrast-enhanced angiography. This has evolved through fluoroscopic planning and intraoperative studies, CT angiography,26–28 and, more recently, 3-D rendering.8,18 In our patient, 3-D rendering enabled accurate delineation of the lesion, confirmation of the diagnosis, and understanding of the surrounding structures, which aided surgical planning.
The current understanding of peripheral AVFs in dogs and cats is primarily limited to clinical reports and extrapolation from human medicine. Definitive treatment recommendations for peripheral AVF in small animals have not been established. This report describes the successful surgical management of a peripheral AVF with ligation of the aberrant arterialized vein without resection of the AVF. To the authors’ knowledge, this approach has not been previously described in the veterinary literature. Surgical intervention for a peripheral AVF should aim to disrupt the abnormal hemodynamics through the fistulous structure.4,23 This has historically been achieved in cats through en bloc resection of all associated vascular structures with13 or without5,7 prior occlusion of abnormal vascular structures with cyanoacrylate. When this is not possible, amputation has been considered as a salvage procedure.18,19
Where applicable, successful intravascular embolization provides a minimally invasive method to completely occlude abnormal vascular communications. This method has been described for treatment of AVF prior to resection in a cat13; in that case, complications included the presence of cyanoacrylate in the pulmonary parenchyma, the palmarodistal aspect of the treated limb, and the nonresected antebrachial vasculature. Persistent pyrexia, medial palmar hypoesthesia, and apparent local hypothermia (with the forepaw of the affected limb cool to the touch) were observed after the surgery.13 Furthermore, the cat had evidence of localized irritation with self-trauma to the accessory carpal pad 1 month after surgery and persistent licking of the affected paw reported 1 year later, although no active skin lesions were present.
For the cat of the present report, open surgery was elected after discussions with an interventional radiology physician. It was suggested that embolization might be impossible given the size and nature of the AVF. Surgical ligation of the suspected arterialized cephalic vein distal to the AVF was pursued over ligation of the AVF and en bloc resection of the anomalous vessels because of inability to accurately localize and ligate the AVF directly without risking substantial injury. Specifically, concerns included tearing the AVF and associated vasculature or causing a clinically important compromise of the arterial blood supply to the distal aspect of the limb if brachial blood flow was disrupted. It was reasoned that ligation of the vessel feeding arterial pressure to the venous system would decrease local hypertension, resolve the subsequent integument lesions, and end potentially life-threatening hemorrhagic episodes. It was further considered that the AVF, although still patent, would not lead to further hemodynamic problems alone. Complete resolution of the clinical signs was attained through ligation of the arterialized cephalic vein, and no complications were identified. On follow-up CT angiography 5 months after the procedure, the AVF and the large network of tortuous vessels associated with the AVF were no longer discernible, and the previously identified dermatologic lesions were absent.
The hemodynamic effects of the cephalic ligature on the AVF, proximal vasculature, and cardiovascular system were unknown and potentially problematic in this case. Further arterialization of adjacent vessels of the distal part of the limb was expected. We inferred that ligation of the cephalic vessel altered total vascular resistance and subsequent blood flow through the fistula and proximal vasculature; how ligation distal to the fistula resulted in resolution of the AVF was unknown, although the treatment may have led to thrombus formation more proximally, resulting in AVF occlusion. The treatment option of ligating arterialized venous structures draining an acquired peripheral AVF was successful in the cat of this report and warrants further investigation in cats.
Acknowledgments
Costs associated with hospitalization, general anesthesia, and CT during the follow-up examination period were subsidized by the Massey University Veterinary Teaching Hospital. No third-party funding or support was received in connection with the case or the writing and publication of the manuscript. The authors declare that there were no conflicts of interest.
The opinions expressed in this article are those of the authors and do not necessarily reflect the views of the listed institutions.
ABBREVIATIONS
| AVF | Arteriovenous fistula |
Footnotes
Noroclav, Norbrook Laboratories Ltd, Newry, Northern Ireland.
Antirobe, Zoetis New Zealand Ltd, Auckland, New Zealand.
Prednil, Jurox New Zealand Ltd, Auckland, New Zealand.
Omnipaque, 755 mg/mL (equivalent to 350 mg of I/mL), GE Healthcare Australia Pty Ltd, Parramatta, NSW, Australia.
Philips Brillance workstation 16-slice CT, Philips Healthcare, Markham, ON, Canada.
Temgesic, Reckitt Benckiser Healthcare UK Ltd, Hull, England.
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