Uterine Adenocarcinoma with Abdominal Metastases in an Ovariohysterectomised Cat

Abstract

Surgical findings An adenocarcinoma of the uterine stump with abdominal metastases is described in a 12.5-year-old incompletely ovariohysterectomised domestic shorthair cat. At the time of presentation, the adenocarcinoma had metastasised to the right perirenal lymph node, the abdominal aorta and the right ureter, resulting in the formation of a large cystic structure. This had compressed and displaced surrounding structures, including the abdominal vena cava and the right kidney, and formed multiple adhesions to the body wall and adjacent abdominal structures. Metastatic extension to the aorta had resulted in its regression into a 2 mm diameter non-pulsatile vessel.

Practical relevance Only one case of uterine adenocarcinoma has previously been reported in an ovariohysterectomised cat. As such, this represents a very unusual and severe complication following an incomplete ovariohysterectomy. Invasion of the tumour tissue into surrounding structures created further complications.

Case report

A 12.5-year-old female neutered domestic short-hair (DSH) cat was presented to the University of Glasgow Small Animal Hospital with severe pain and abdominal distension, weight loss, lethargy and persistent signs of oestrus.

History

Signs of oestrus had persisted in the cat despite two attempted ovariohysterectomies. The first was a routine neutering procedure performed at a rescue shelter prior to homing, with the second operation performed when signs of oestrus persisted after the cat had been homed. A third surgery, performed 8 months prior to referral, resulted in the identification and removal of a cystic right ovary. At this time a fluid-filled uterus was also identified, as was a fluid-filled structure near the right kidney; however, no attempt was made to remove these structures.

Two months before referral the cat again started showing signs of oestrus, which persisted despite an injection of proligestone (Delvosteron; Intervet). Subsequent measurement revealed a serum oestradiol concentration in excess of 200 pmol/l, suggesting the presence of functional ovarian tissue. (For males, and females in anoestrus, serum oestradiol concentration should be undetectable, <10 pmol/l.)

Findings on referral

Clinical examination was limited due to poor patient compliance, but marked abdominal enlargement was noted. Abdominal ultrasonography demonstrated a large mid-abdominal mass with many complex cystic cavities. The contents of the cysts were highly echogenic. The uterine body was grossly distended (approximately 1 cm diameter) and contained echogenic fluid. The owners declined any further intervention at this time and a recheck was scheduled for the following week.

Emergency presentation

The cat re-presented as an emergency 48 h later, as she had been increasingly dull, lethargic and inappetent since her previous examination. She had urinated only a small amount, and had not passed faeces.

On examination, she was severely painful over the abdomen and caudal thorax, and would not tolerate any handling over these areas. Her heart rate and peripheral pulses were strong, but almost of a water-hammer type, suggesting above-normal pressure of contraction. The respiratory rate was within normal limits. Given the history, and previous identification of extensive intra-abdominal cystic lesions, exploratory abdominal surgery was recommended as ultrasound-guided aspiration or biopsy was considered unlikely to yield a diagnostic sample.

Pre-anesthetic tests indicated a moderate anaemia (packed cell volume 20%, reference interval [RI] 30–45%). Electrolytes, urea (9.0 mmol/l, RI 5.7–12.9), creatinine (95 mmol/l, RI 71–212) and clotting times were within normal limits. Blood lactate was 1.3 mmol/l (normal <2.5 mmol/l).

Exploratory coeliotomy

On exploratory coeliotomy, performed via a standard xiphoid—pelvic brim incision, a large multilobed cystic mass was identified occupying almost the entire abdominal cavity (Fig 1). The bladder was sitting immediately caudo ventral to the mass, together with a distended uterine body containing purulent material.

The vena cava was displaced to the left side of the abdomen, had become incorporated within the wall of the cystic mass, and was tortuously kinked due to multiple points of adhesion. The right kidney was also to the left of midline, and was adhesed to the cranial aspect of the cystic mass. The proximal right ureter was visualised running into the mass, and terminating within it. The distal right ureter was identified leaving the mass and was followed to the trigone to confirm its provenance. The mass contained approximately 1 litre of fluid, which biochemical analysis subsequently confirmed to have urea (9.3 mmol/l) and creatinine (101 μmol/l) levels higher than the serum levels. This is consistent with extravasated urine that has been contained and partially resorbed.

The left ureter was identified and traced intact from the trigone to the left kidney.

The mass was carefully and progressively dissected free of the vena cava, left kidney and renal vessels, and left ureter. Multiple adhesions between the body wall and the mass were transected. At this point a thin tubular structure, approximately 2–2.5 mm in diameter, was identified running within the left side of the cystic mass, which further evaluation confirmed to be the abdominal aorta (Fig 2). The aortic constriction extended from adjacent to the diaphragm to the caudal abdomen, where the vessel terminated in a hard mass of fibrous tissue immediately beside the uterine body. The vena cava also joined this fibrous area, and here a ballooning of the vessel walls could be seen.

FIG 1

Drainage of the cystic mass confirmed that it was a urinoma

FIG 2

Fibrous remnant of the abdominal aorta, approximately 2 mm in diameter

FIG 3

Histopathology of uterine adenocarcinoma. The single arrow indicates the papillary projections into the lumen, and the double arrow identifies the necrotic debris within the lumen. (inset) The dilated endometrial glands lined with tumour cells

Unfortunately, at this point in the surgery the cat suffered a full cardiorespiratory arrest and resuscitation was unsuccessful.

Histopathology

Histopathology of the uterus (Fig 3) identified a thickened endometrium with papillary projections into the lumen, and irregularly shaped dilated endometrial glands lined with layers of tumour cells. There was extensive necrosis of tumour cells with many glandularspaces and the uterine lumen contained necrotic debris. The tumour cells were columnar with a moderate amount of eosinophilic cytoplasm, a hyperchromatic ovoid and central nucleus, and a prominent, central, deeply eosinophilic nucleolus. There was a moderate degree of anisokaryosis, a large number of multinucleate cells, and one to three mitotic figures per high power field.

Recurrent oestrous cycles are the most common clinical sign of ovarian remnant syndrome; albeit there may be an interval of years between ovariohysterectomy and signs of oestrus.

Neoplastic cells were also identified in the aorta, perirenal tissue and cystic structure. The cells seen within these structures differed from the tumour cells within the uterus as they were polygonal, rather than cuboidal, had more variance in both the shape of the nuclei and number of nucleoli, and demonstrated marked (as opposed to moderate) anisokaryosis and a higher mitotic index (up to eight mitotic figures per high power field). The shared characteristics included the eosinophilic cytoplasm and deeply eosinophilic nucleoli.

These histopathological features are consistent with metastatic spread of the tumour from a primary glandular tumour — most likely from the endometrium of the uterine stump.

Discussion

Uterine neoplasia is rare in the cat, comprising 0.29% of all feline neoplasms in one study. ¹ Overall, uterine leiomyoma and adenocarcinoma have been the most common tumours described in retrospective studies limited to tumours of the feline reproductive system. ^1,2

Uterine tumours are more commonly found in entire female cats, between 4 and 16 years of age. ^1,3–9 Only one case of uterine adenocarcinoma has been reported in an ovariohysterectomised female cat. ¹

The clinical signs in cats with uterine tumours vary but can include abdominal distension, weight loss, anorexia, pain, vaginal bleeding and infertility. ^1,9,10 In this case, the cat was displaying signs of prolonged and recurrent oestrus despite attempted ovariohysterectomy, and had abdominal distension, weight loss and pain.

The persistent signs of oestrus could be attributed to ovarian remnant syndrome (ORS), which refers to the presence of functional ovarian tissue in a previously ovariohysterectomised animal. ^11,12 There is some debate in the literature as to the cause of ORS, with suggested causes falling into two broad categories — anatomical variation and surgical error. Anatomical variants include the presence of an accessory ovary or extension of ovarian tissue into the ovarian ligament, which becomes functional after removal of the ovary. Potential surgical errors include improper clamp placement, dropping of ovarian tissue, and a small surgical incision that limits visualisation. ^12,13 Recurrent oestrous cycles are the most common clinical sign of ORS; albeit there may be an interval of years between ovariohysterectomy and signs of oestrus. ¹¹ Diagnosis is based on history, clinical signs, hormonal assays, vaginal cytology and exploratory surgery.

This report documents a very unusual complication following an incomplete ovariohysterectomy. It is likely that the initial surgery and the inflammation caused by further surgical attempts, as well as hormonal drive from the remaining ovarian tissue, led to the development of uterine neoplasia. Invasion of the tumour tissue into surrounding structures created further complications, which included the formation of a large cystic structure consistent with a urinoma (ie, an accumulation of extravasated urine within a fibrous sac).

Urinomas occur due to persistent urine leakage from a ureter triggering a fibroblastic reaction that acts to contain the urine within the retroperitoneal space. In humans, despite being rare, they have been reported to occur secondarily to trauma (penetrating or blunt) or obstruction (neoplasia and calculi), and following surgery (urogenital, orthopaedic and vascular procedures, and neurosurgery). In the veterinary literature there are only isolated case reports of urinomas, which include three cases in cats following road traffic accidents, ^14–16 and one in a dog following ligation during ovariohysterectomy. ¹⁷

It is likely that, in this cat, the initial surgery and the inflammation caused by further surgical attempts, as well as hormonal drive from the remaining ovarian tissue, led to the development of uterine neoplasia.

To the authors’ knowledge, there have been no previous reports of urinoma formation secondary to neoplasia in feline patients. The other unusual feature of this case was the aortic metastasis, which had led to progressive aortic constriction.

In the case of this cat it is likely that invasion of the right ureter by the tumour led to a slow leakage of urine out of the ureter, producing a urinoma. To the authors’ knowledge, there have been no previous reports of urinoma formation secondary to neoplasia in feline patients. Urinomas have many synonyms, including paraureteral pseudocyst and uriniferous pseudocyst. What is important, however, is that they are differentiated from perinephric pseudocysts, which are fluid-filled sacs surrounding the kidney, usually seen in association with chronic renal failure. ^16,18

The other unusual feature of this case was the aortic metastasis, which had led to progressive aortic constriction and, based on the appearance at surgery, a significantly reduced blood flow. Aortic metastasis has been documented associated with a variety of tumours in people, including colon carcinoma, malignant germ cell testicular tumour and carcinoid tumours. ^19–21 In the main, invasion is reported to the aortic wall, and can be associated with aneurysmal dilation and occasionally spontaneous rupture. By contrast, constriction or progressive occlusion is only infrequently reported. Abdominal aortic, celiac axis and mesenteric arterial occlusion due to neoplastic thrombosis has been recently reported in an elderly woman, associated with a 2-week history of abdominal pain, ²¹ and it may be that the progressive aortic occlusion in the cat in the present report contributed to the abdominal pain that developed prior to surgery.