Intussusception associated with congenital lymphangioma in a dog

Abstract

A 12-week-old intact male golden retriever dog was referred to our clinic with a history of recurrent diarrhea and rectal prolapse and because of a suspected intussusception. An abdominal ultrasound was conducted to confirm the suspicion of an intussusception. An exploratory laparotomy identified a jejuno-ileo-cecal-colic intussusception that was manually reduced. A 3-centimeter, abnormal cystic lesion was noted to be arising from the mesentery of the distal jejunum and ileum, just orad to the cecum. The cystic lesion and associated intestinal segment were resected, and the histopathologic diagnosis was consistent with a mesenteric lymphatic malformation. To the authors’ knowledge, this is the first report of a mesenteric lymphatic malformation associated with intussusception in a dog.

Key clinical message:

Our findings suggest that mesenteric lymphatic malformations should be considered when cystic structures are associated with intussusceptions in young dogs.

CASE DESCRIPTION

A 12-week-old intact male golden retriever dog was presented to our clinic because of recurrent diarrhea. The dog had a rectal prolapse, presumed to be secondary to chronic diarrhea. The prolapse was manually reduced with topical application of 50% dextrose and secured with a purse-string suture. Metronidazole was prescribed at a dosage of 9.4 mg/kg, PO, q12h. The dog was returned for purse-string suture removal 6 d after placement. Clinical signs included continuation of mucoid diarrhea and new onset of lethargy and weight loss. Abdominal palpation revealed a tube-like, thickened structure that was suspected to be an intestinal intussusception. One lateral abdominal radiograph showed diffusely dilated small-intestinal loops, and a focal ultrasound of the intestinal tract supported the suspicion of intussusception. The dog was subsequently referred for further assessment.

Initial physical examination findings included slightly tacky mucous membranes and a firm, tubular structure palpated in the caudal-dorsal abdomen. The same tubular structure could be palpated on a rectal examination, resulting in a pain response when the structure was manipulated. The remainder of the physical examination was within normal limits.

Based on the dog’s history and physical examination findings, differential diagnoses included intussusception (1), intestinal foreign body (1), congenital abnormality [such as congenital intestinal stenosis (2) or congenital peritoneal bands (3)], inguinal hernia (4), or intra-abdominal mass (3). Diagnostic test recommendations included a CBC, serum biochemistry panel, baseline cortisol, cobalamin, trypsin-like immunoreactivity, pancreatic lipase immunoreactivity, folate, fecal flotation, parvovirus SNAP test, 3-view abdominal radiography, and abdominal ultrasound.

The CBC showed leukocytosis (19.3 × 10⁹/L; RI: 5.4 to 14.3 × 10⁹/L), low hemoglobin (121 g/L; RI: 135 to 198 g/L), low hematocrit (0.346 L/L; RI: 0.40 to 0.56 L/L), low mean cell volume (61.0 fL; RI: 64 to 75 fL), low mean cell hemoglobin concentration (21.2 pg; RI: 22 to 25 pg), and thrombocytosis (688 × 10⁹/L; RI: 218 to 470 × 10⁹/L). The serum biochemistry showed hyperphosphatemia (2.42 mmol/L; RI: 0.94 to 2.13 mmol/L), hyperglycemia (6.8 mmol/L; RI: 3.3 to 6.1 mmol/L), and hypoglobulinemia (16 g/L; RI: 23 to 52 g/L). These findings were most likely a result of systemic inflammation and the young age of the dog. Baseline cortisol was elevated (335 nmol/L; RI: 14 to 180 nmol/L), ruling out Addison’s as a cause for the gastrointestinal signs. Cobalamin was on the low end of the reference interval (333 ng/L; RI: 251 to 908 ng/L) and trypsin-like immunoreactivity was within normal limits (39.4 μg/L; RI: 5.7 to 45.2 μg/L). This combination of results was consistent with distal small intestinal disease or dysbiosis and less indicative of exocrine pancreatic insufficiency. Pancreatic-like immunoreactivity was within the normal reference interval (< 30 μg/L; RI: ≤ 200 μg/L), and thus pancreatitis was considered less likely. Folate was within the normal reference interval (18.1 μg/L; RI: 7.7 to 24.4 μg/L). A fecal float was negative for parasites and a parvovirus SNAP test was negative.

Three-view abdominal radiographs were taken as the original radiographs consisted of a single radiographic view. Radiographs showed a moderate volume of soft-tissue opacity intermixed with small gas foci and mineral opacities within a distended right caudal abdominal intestinal segment, as well as numerous other gas-distended intestinal segments in the left cranial abdomen (Figures 1, 2). There was a moderate volume of stippled, semi-structured content visible in one of the distended loops in the ventral abdomen. There was a generalized loss of abdominal serosal detail, which could have been due to either free fluid in the peritoneum or the young age of the animal. A mechanical intestinal obstruction was diagnosed, with foreign body obstruction or intussusception being the top considerations.

FIGURE 1.

Right lateral radiographic image of the dog’s abdomen with the cranial aspect to the left and the caudal aspect to the right. The radiograph shows numerous gas-distended intestinal segments and a moderate volume of stippled, semi-structured content visible in one of the distended loops in the ventral abdomen. There is further content dorsally, presumed to be in the colon. There is also a generalized loss of abdominal serosal detail.

FIGURE 2.

Ventrodorsal radiographic image of the dog’s abdomen with the cranial aspect at the top and the caudal aspect at the bottom. The radiograph shows numerous gas-distended small intestinal segments with an additional intestinal segment, in the right caudodorsal abdomen, containing structured content interspersed with small gas foci and mineral opacities. This was presumed to be the descending colon, displaced into the right abdomen.

Abdominal ultrasound showed mild peritoneal effusion in the cranial abdomen, and moderate gas distension of the stomach and multiple loops of the small intestine. In one segment of the distended small intestine in the middle abdomen, there was a multilayered appearance to the wall, also known as a “multiple concentric ring sign” or a “target lesion.” This appearance was consistent with an intussusception and was thought to be associated with either the jejunum or the ileum, based on ultrasound examination. There was detectable vascular flow in the mesenteric fat within the intussusceptum as well as surrounding mild steatitis. There were multiple septate-appearing anechoic structures within the intussusception that were reported to have the appearance of a cyst (Figures 3, 4). These structures all measured < 5 cm in diameter, with oblong, multiseptate appearances. None of the cyst-like structures identified had detectable vascular flow, and at the time of the ultrasound, they were attributed to a cyst-like mesenteric lymph node or other unknown etiology. Based on the imaging findings, an exploratory laparotomy was recommended.

FIGURE 3.

A transverse abdominal ultrasound image of the dog’s small intestine, showing an oblong, multiseptate-appearing, anechoic structure within the intussusception, which has the appearance of a cyst. This structure measures 3.83 × 1.12 cm.

FIGURE 4.

A transverse abdominal ultrasound image of the dog’s small intestine, showing an oblong, multiseptate-appearing, anechoic structure within the intussusception, which has the appearance of a cyst. This structure measures 4.79 × 1.22 cm.

The dog was premedicated with fentanyl (5 μg/kg, IV). Anesthesia was induced with alfaxalone (2 mg/kg, IV), to effect. The dog was intubated and anesthesia was maintained with isoflurane, with the dog on a mechanical ventilator. A fentanyl constant-rate infusion (CRI) (5 μg/kg per hour, IV) was continued for its minimum alveolar concentration-reduction and analgesic properties. Cefazolin (22 mg/kg, IV) was administered as a perioperative antibiotic. Glycopyrrolate (2.5 to 5 μg/kg, IV) was administered as needed for treatment of bradycardia, and a dobutamine CRI (5 μg/kg per hour, IV) was required for management of systemic hypotension.

Exploratory laparotomy revealed a mild to moderate volume of clear peritoneal effusion and a sample was collected for bacterial culture and cytological analysis. A 20-centimeter jejuno-ileo-ceco-colic intussusception was noted. There was moderate dilation of the orad section of the jejunum. The intussusception was manually reduced and ~15 cm of grossly abnormal distal jejunum and ileum, including the now reduced intussusception and ending just orad to the cecum, was observed. Adhesions attached the abnormal small intestinal segments into the abnormal U-shape, with a 3-centimeter, fluid-filled cyst-like structure noted within the adhesions. The dilated orad section of the jejunum tapered sharply into this U-shape, and intestinal contents did not pass easily through this junction. The abnormal segment of small intestine was resected, preserving the ileocecocolic junction. A jejunal-to-distal ileal end-to-end anastomosis was conducted using 4-0 PDS suture material in a simple interrupted pattern. A leak test was negative. Gloves and instruments were changed before lavaging and closing the abdomen in a routine, 3-layer closure.

The dog recovered well from anesthesia. Postoperative analgesia included a bupivacaine line block (10 mg, periincisional), fentanyl CRI (2 to 3 μg/kg per hour, IV), and gabapentin (12.5 mg/kg, PO, q8h). A B12 injection was administered (2.5 mL, SC) as a supplementation due to the marked reduction in length of ileum following resection.

The dog had variable stool consistency throughout the postoperative period, with occasional episodes of diarrhea and occasional hematochezia. The dog was discharged 2 d after surgery and prescribed gabapentin (12.5 mg/kg, PO, q8h) for analgesia, and fenbendazole (50 mg/kg, PO, q24h) and praziquantel (5 mg/kg, PO, given once) as prophylactic dewormers, despite the negative fecal floatation. At a 2-week follow-up examination, the dog had recovered well and had not experienced a recurrence of clinical signs.

Cytological analysis of free abdominal fluid collected during surgery showed no organisms on Gram stain, and aerobic bacterial culture yielded no bacterial growth. A fasted gastrointestinal panel was submitted postoperatively to measure B12, before administration of the B12 supplementation, and was within normal limits. The resected small intestine (15 to 20 cm in length), containing distal jejunum and ileum, that was adhered together in a U-shape with fibrous tissue and fluid filled cyst-like structures was submitted for histopathologic assessment. Histopathologically, the serosal surfaces of the adjacent segments of small intestine were adhered together by loose fibrous connective tissue containing numerous, variably sized blood and lymphatic vessels and multilocular cystic spaces. The cystic spaces were located in the distal jejunal/ileal area of mesenteric adhesion within the loose fibrous connective tissue. These cystic spaces were lined by attenuated spindloid cells and contained small amounts of clear fluid with multifocal aggregates of fibrin.

The surrounding fibrous connective tissue contained numerous small-caliber blood vessels that were often oriented perpendicularly to the cyst lumen in a granulation tissue-like appearance. The mucosa of the intestinal wall was infiltrated by small numbers of neutrophils, with very small numbers of neutrophils extending into the underlying submucosa. Based on these findings, a final diagnosis of mesenteric intestinal fibrous adhesions with multilocular cystic structures and atypical lymphovascular proliferation was made (5–7). This constellation of findings was considered most likely a mesenteric lymphatic malformation, also known as lymphangioma, and mild neutrophilic enteritis.

DISCUSSION

Treatment of intussusception requires surgical management, in the form of either manual reduction, if the intestines remain viable; or resection and anastomosis, if the intestines are nonviable or manual reduction is not possible (1,8). Histopathologic examination of the excised tissues is warranted to assess underlying disease. In the present case, on histological examination, the site of intussusception involved a distal jejunal/ileal area of mesenteric adhesion with atypical lymphovascular proliferation strongly suggestive of a mesenteric lymphatic malformation (5–7,9,10). A congenital etiology was considered most likely due to the young age of this dog; however, an acquired form of mesenteric lymphangioma could not be definitively ruled out. To the authors’ knowledge, this is the first report of this type of lesion as an etiology or sequelae of a canine intussusception.

The gold standard for diagnosis of an intussusception is abdominal ultrasound; however, CT is recently becoming a more available option (1). In the present case, an intussusception was identified with ultrasonography; however, multiple septate-appearing anechoic structures were also identified within the intussusception, ranging from ~3 to 5 cm in length by ~1 to 2 cm in width. Although rare, similar findings of cystic structures have been identified within intussusceptions in humans (6,7,11). In a human case, a small (diameter: 15 to 20 mm), unilocular cyst with a thin inner rim and posterior enhancement was located within the cecum on ultrasound and confirmed to be an enterogenous cyst (12). In another human case, ultrasonography showed a multilocular cyst measuring 7 cm in diameter and associated with a typical-appearing intussusception (11). Histopathologic examination confirmed the cyst to be a multilocular cystic lymphangioma (11). It is important to note that, although most mesenteric lymphatic malformations appear as anechoic multilocular cystic masses on ultrasound, they can also appear as solid masses, though only in rare instances (9).

A lymphatic malformation, also known as lymphangioma, is a congenital malformation of lymphatic tissue (6). This is a rare diagnosis in humans, occurring most commonly in infants and children (6,7,11). These structures are most frequently identified in the neck, head, and oral cavity, but can develop in the abdominal cavity less commonly (5–7,9–11). Within the abdominal cavity, they are often associated with the mesentery (5,9), though this represents < 1% of all lesions (6,7,10). The most common complication associated with mesenteric lymphatic malformations in humans is volvulus; however, there are a few reports of mesenteric lymphatic malformations associated with intussusceptions (6,10). The typical diameter of these cystic lesions ranges from 0.8 to 3.5 cm (6). Regardless of location, the definitive treatment for lymphatic malformations in human medicine is surgical resection, with resection of the associated intestine for intestinal- or mesenteric-located lymphangiomas (6,7).

Lymphangiomas are hypothesized to be caused by a failure of embryologic development of the lymphatics, when primary lymphatic sacs fail to join the lymphatic system, or if acquired inflammation of the lymphatic channels leads to obstruction and subsequent development of a cystic lymphangioma (6). Histopathologically, these lymphatic malformations can be divided into 3 groups: cystic, simple, and cavernous lymphangiomas (6,10). Cystic lymphangiomas are typically lined by flat endothelial cells, dilated lymphatic lacunae, abundant lymphatic lymphocytes, or lymphoid tissue (6,10). Simple lymphangiomas often originate in the skin and histologically consist of small, thin-walled lymphatic spaces (6,10). Cavernous lymphangiomas show some association with normal lymphatic spaces (6,10).

The findings reported herein fit most closely with the congenital cystic lymphangioma classification, based on the clinical presentation, age of the dog, and histopathologic features when compared to the human medical literature. The primary symptoms reported by humans with this condition, when associated with an intussusception, are localized abdominal pain, nausea, and vomiting; however, a single case with symptoms of mucoid, bloody diarrhea was also reported (6,7,10,11). Although the dog did not exhibit abdominal pain, nausea, or vomiting, it did present with mucoid diarrhea. The young age of the human patient with mucoid diarrhea strongly supported a diagnosis of congenital malformation as the underlying cause of the cystic lesion, similar to the case for this dog (10). Furthermore, histopathologic findings in human medicine showed irregular cystic structures with walls composed of smooth muscle cells and fibrocytes, with an inner lining of flat or attenuated endothelium, that resembled the cells that line normal lymphatic vessels (6,7,10). These findings were similar to the histopathologic findings in this dog, with the supporting stroma containing fibrous tissue and variably sized blood and lymphatic vessels and multilocular cystic spaces lined with attenuated spindloid cells.

Cystic lymphangiomas have been reported 7 times in the veterinary literature, with varying histopathologic features and 1 other case associated with the mesentery (13–19). Although the ages of animals in these cases ranged from 7 mo to 8 y, most were < 1 y of age at the time of diagnosis, making a congenital cause more likely (13–19). The single mesenteric-associated case was presented with a history of vomiting, decreased appetite, and abdominal distension. An abdominal CT scan showed a large, lobulated, and smoothly marginated fluid-filled mass with multifocal septations occupying most of the peritoneal space that was centered in the mid-mesentery. An intussusception was not observed in that case and clinical signs were attributed to the space-occupying mass (13). The other reported cases of cystic lymphangiomas included lesions in the retroperitoneum, peritoneum, mammary tissue, ovaries, uterus, urinary bladder, rectum, and metacarpal pads (13–19).

We report the first case of a mesenteric cystic lymphatic malformation associated with an intussusception in a dog. Further research into the prevalence of this condition in dogs is warranted. From the findings of this case report, lymphatic malformations should be considered when cystic structures are associated with intussusceptions in young dogs. CVJ