Preemptively planned en bloc resection of an extensive right adrenal pheochromocytoma involving the right hepatic division, caval thrombus and segmental caudal vena cava in a dog with Budd−Chiari‐like syndrome

Abstract Background Surgical resection is the treatment of choice for canine adrenal pheochromocytomas (PHEOs). Information on en bloc resection of adrenal PHEO with tumour thrombus, right hepatic division and segmental caudal vena cava (CVC) running through the adrenal tumour and right hepatic division is limited. Objective To describe the preemptively planned en bloc resection of an extensive right adrenal PHEO involving the right hepatic division, the caval thrombus and the segmental CVC in a dog with Budd−Chiari‐like syndrome (BCLS). Methods A 13‐year‐old castrated male miniature dachshund was referred for surgical treatment due to anorexia, lethargy and severe abdominal distension caused by abundant ascites. Preoperative computed tomography (CT) revealed a large mass in the right adrenal gland with a large caval thrombus obstructing the CVC and hepatic veins, which caused BCLS. Additionally, collateral vessels were formed between the CVC and azygos veins. No findings suggested obvious metastases. Based on CT findings, an en bloc resection of the adrenal tumour with caval thrombus, right hepatic division and segmental CVC was planned. Results The preoperatively planned resection was feasible; the tumour was completely resected grossly. The operation time and total Pringle manoeuvre time were 162 min and 16 min 56 s, respectively. There was no postoperative hindlimb oedema, renal dysfunction, ascites or abdominal distention. The patient's clinical signs, including appetite, fully improved. Hospitalization lasted 16 days. However, the patient died on the 130th postoperative day due to suspected metastases and cachexia. Conclusions Even in case of an extensive infiltration of adrenal PHEO causing BCLS, an en bloc resection might be successfully achieved based on the preoperative CT findings speculating the collateral vessels formed for caudal venous return.


MATERIALS AND METHODS
A 13-year-old castrated male miniature dachshund was brought to an emergency animal clinic with a chief complaint of abdominal distension and appetite loss. An abdominal ultrasound revealed a large mass in the abdominal cavity. The patient was examined at another animal hospital and underwent CT and fine-needle aspiration of the mass, which was suspected to be a malignant epithelial tumour that originated from the right adrenal gland and had severely infiltrated into the surrounding tissues. Approximately 2 weeks later, the patient was referred to our hospital for surgical treatment.
On the first evaluation, the patient had anorexia, asthenia and lethargy, and a general physical examination revealed severe abdominal distension and a body condition score of 2/5. The patient had a body weight of 9.5 kg, a rectal temperature of 38. The day after the first evaluation, the anaemia (PCV 20%) noted on the initial CBC improved after 200 mL fresh whole blood was transfused to a PCV of 29%, and the patient showed increased activity.
There were no neoplastic cells in the sediment smears. An adrenal hormone test was performed as shown in Table 2. The adrenocorticotropic hormone (ACTH) stimulation test was within the normal ranges. In addition, plasma catecholamine fraction, including adrenaline, noradrenaline and dopamine, was not high.
Therefore, we proposed surgical treatment, and the owner then provided consent for en bloc resection of the mass. Five days after the first evaluation, the patient underwent a CT examination, followed by surgery.
Under general anaesthesia, the patient firstly underwent contrast-

F I G U R E 6
The blood vessels and hepatic ducts that flow into the right hepatic division were ligated and resected en bloc. and then, decreased to 4 mmHg after tourniquet 3 was temporarily engaged. Tourniquet 3 was released, and the Pringle manoeuvre was performed by squeezing tourniquet 1. The hepatic arteries, portal branch and hepatic duct in the right hepatic division were en masse ligated and resected using 3-0 coated braided nylon sutures (Surgilon TM ; Medtronic), and then, tourniquet 1 was released to discontinue the Pringle manoeuvre ( Figure 6). Furthermore, the mass was isolated

RESULTS
The en bloc resection of the right adrenal mass involving the right hepatic division, caval thrombus and segmental CVC was feasible in this case. The operation time from skin incision to closure was 162 min.   The superior effectiveness of CT in the detection of intravascular infiltrating lesions in canine adrenal tumours has been shown to be as follows: ultrasound exam has a detection sensitivity of 80−100% and specificity of 90−96% (Davis et al., 2012, Kyles et al., 2003, while CT has a detection sensitivity of 92% and specificity of 100% (Schultz et al., 2009). CT may effectively detect collateral circulation due to CVC obstruction. A previous study on healthy dogs reported that 3 weeks after gradual obstruction of the CVC in the cranial region of the renal vein, contrast CT revealed collateral circulation from the renal capsule and the CVC to the lumbar, vertebral and azygos veins (Peacock et al., 2003). In our case, since the collateral circulation returned from the CVC to the azygos vein was created, we considered that the venous return volume could be maintained even with complete CVC obstruction. Based on the CT findings, we could plan an en bloc resection of the right hepatic division, caval thrombus and right adrenal tumour, including a part of the CVC, without the reduction of venous return.
The presence or absence of caval thrombi in canine adrenal tumours is considered a prognostic factor (Massari et al., 2011). PHEO is one of the short-term prognostic factors since intravascular invasion into the CVC is common (Barrera et al., 2013). On the other hand, caval thrombus removal through CVC incision in canine adrenal tumours is not associated with short-term prognosis (Schwartz et al., 2008, Kyles et al., 2003, Herrera et al., 2008. In dogs with caval thrombi, those with intravascular infiltration beyond the hilar region are at least four times more likely to die within a short period than those without (Barrera et al., 2013). It has been recently demonstrated that even dogs with an intravascularly infiltrated caval thrombus beyond the hepatic hilum can survive the perioperative period secondary to skilled anaesthesia management by anaesthesiologists and blood preparations (Lipscomb, 2019). In dogs with adrenal tumours undergoing surgical treatment, the perioperative complication and mortality rates are ≥ 50% (Barthez et al., 1997, Kyles et al., 2003, Mayhew et al., 2019, Knight et al., 2019 and 12−50% (Massari et al., 2011, Schwartz et al., 2008, Barrera et al., 2013, Kyles et al., 2003, Herrera et al., 2008, Mayhew et al., 2019, Knight et al., 2019, respectively. In our case, contrast-enhanced CT suggested poor systemic blood circulation due to caval thrombus. In addition, since our patient also had BCLS, the patient had the potential risk of higher perioperative mortality. When an experienced surgeon performs the appropriate procedure, the presence or absence of a caval thrombus does not significantly affect the perioperative complication/mortality rate (Kyles et al., 2003). Previous reports of en bloc resection, including the CVC for PHEO with intravascular infiltration into the CVC, have reported a good long-term prognosis, with a survival time of 20−49 months (Louvet et al., 2005, Guillaumot et al., 2012. On the other hand, other previous cases of canine PHEO with BCLS have suggested a poor prognosis: one patient died during the perioperative period due to dyspnoea (Kyles et al., 2003), while another underwent euthanasia at the owner's request (Schoeman & Stidworthy, 2001, Rosa et al., 2012. Our case with preoperative BCLS also showed a short survival time (approximately 4 months) after surgery, and the causes of death were suspected to be metastases and cachexia. In our case, BCLS postoperatively disappeared because the resumption of flow through the left and central hepatic divisions likely led to the resolution of the ascites. In addition, the surgical treatment improved the appetite loss and overall condition of the patient for a short postoperative time.
Therefore, en bloc resection of PHEO with caval thrombus causing BCLS should only be considered to improve the quality of life in patients with collateral venous return development.
In conclusion, our report described that preemptively planned en bloc resection of an extensive right adrenal PHEO, involving the right hepatic division, caval thrombus and segmental CVC, was successfully performed based on the preoperative CT findings in the patient, and BCLS resolved after surgery. In the case of CT findings indicating naturally occurring collateral vessels, en bloc resection could be feasible for PHEO patients with extensive infiltration into the CVC, right hepatic division and hepatic vein obstruction.

ETHICS APPROVAL STATEMENT
Informed owner consent of the patient was obtained prior to the first evaluation, and all procedures for the patient were approved by the Ethical Committee of Nihon University Animal Medical Center (accession No. 03-019).