Abdominal Lipomatosis with Secondary Self-Strangulation of Masses in an Adult Rhesus Macaque (Macaca mulatta)

Abstract

An 10-y-old, intact male rhesus macaque (Macaca mulatta) presented for bilateral scrotal swelling and a distended abdomen. A soft mass in the left upper quadrant of the abdomen was palpated. A barium study did not reveal any gastrointestinal abnormalities. Exploratory laparotomy revealed a large (1.25 kg, 15.0 × 13.0 × 9.5 cm), red and tan, soft, circumscribed, spherical mass within the greater omentum and 10 to 20 smaller (diameter, 1 to 4 cm), soft to firm masses in the mesentery and greater omentum. The resected mass was a self-strangulating abdominal lipoma, a pedunculated neoplasm composed of white adipocytes arising from peritoneal adipose tissue undergoing secondary coagulation necrosis after strangulation of the blood supply due to twisting of the mass around the peduncle. The smaller masses were histologically consistent with simple or self-strangulating pedunculated abdominal lipomas. The macaque presented again 9 mo later with a firm, 5.0-cm mass in the midabdomen, with intestinal displacement visible on radiographs. Given this animal's medical history and questionable prognosis, euthanasia was elected. Necropsy revealed numerous, multifocal to coalescing, 1.0- to 15.0-cm, pale tan to yellow, circumscribed, soft to firm, spherical to ellipsoid, pedunculated masses that were scattered throughout the mesentery, greater omentum, lesser omentum, and serosal surfaces of the gastrointestinal tract. All of the masses were pedunculated abdominal lipomas, and most demonstrated coagulation necrosis due to self-strangulation of the blood supply. To our knowledge, this report is the first to describe abdominal lipomatosis with secondary self-strangulation of masses in a rhesus macaque.

Lipomas have been reported frequently in veterinary medicine as benign subcutaneous neoplasms in canines¹⁶ or as pedunculated peritoneal masses with the potential to cause intestinal strangulation in geriatric horses.⁶ Abdominal lipomatosis (multiple abdominal lipomas) in humans and dogs had been reported only rarely and have been accompanied by clinical signs of abdominal distention with or without secondary gastrointestinal complications.¹⁶ Lipomas of the skin of nonhuman primates have affected a patas monkey, an African green monkey, rhesus macaques, and chimpanzees. Lipomas within the peritoneal cavity have been diagnosed rarely in nonhuman primates. Reported cases include an omental lipoma in a mona monkey and an adrenal lipoma in a hamadryas baboon.¹⁴ Here we report the clinical signs, postmortem examination, and histopathologic features of abdominal lipomatosis in a rhesus macaque (Macaca mulatta).

Case Report

An approximately 10-y-old intact male, captive-bred rhesus macaque presented for abdominal distention and bilateral scrotal swelling. The animal was individually housed indoors at an AAALAC-accredited facility in accordance with the Animal Welfare Act¹ and the Guide for the Care and Use of Laboratory Animals.¹⁰ Historically, the macaque consistently tested negative for Macacine herpesvirus 1, SIV, simian retrovirus, and tuberculosis. He was enrolled in an IACUC-approved neuroscience research study and had a cranial implant in place for more than 5 y. This macaque previously was diagnosed with a low-grade myxosarcoma on the right stifle that successfully resolved surgically. At the time of initial presentation, the animal was receiving buprenorphine (0.005 mg/kg IM) for analgesia after adjustment of his cranial implant 2 d earlier.

At presentation (day 0), a routine visual assessment revealed moderate abdominal distention and bilateral scrotal swelling. No other abnormalities were noted, and the macaque was alert, exhibiting normal behavior with normal food and fluid intake, and had normal production of urine and feces. Differential diagnoses for abdominal distention included decreased gastrointestinal peristalsis (due to opioid administration) and neoplasia. Buprenorphine was continued as needed for pain, and due to the drug's potential negative effect on gastrointestinal motility, the macaque was placed on metoclopramide (0.2 mg/kg IM every 12 h).

The animal's clinical condition remained stable, with no regression of the abdominal distention noted by day 4; therefore, the macaque was sedated with ketamine (2.0 mg/kg) and dexmedetomidine (0.04 mg/kg) for a full examination. An abdominal mass approximately 15.0 cm in diameter was palpated in the upper left quadrant. Bilateral scrotal swelling continued to be present.

Differential diagnoses for scrotal swelling include vascular outflow obstruction caused by the mass, hypoproteinemia due to hepatic amyloidosis, displacement of mesenteric fat into the scrotal cavity, and displacement of the other mesenteric lipomas into the scrotal cavity by the largest mass, as well as heart failure, Chagas disease, and renal failure. Vascular outflow obstruction and hypoproteinemia were unlikely, because edema would have been more generalized. Chagas disease, heart failure, and renal failure are inconsistent with previous history, clinical signs, and blood work. The scrotal enlargement most likely was caused by displacement of mesenteric lipomas or mesenteric fat into the scrotal cavity.

Radiographs revealed a large, radiopaque abdominal mass of unknown origin that caused a mass effect and displaced the gastrointestinal tract dorsally and to the right lateral aspect of the abdomen (Figure 1). Contrast radiographs confirmed that the gastrointestinal tract was not obstructed. Abdominal ultrasonography was performed, but the source of the mass could not be determined. A fine-needle aspirate was not performed because of concern that this mass was splenic in origin and that postaspiration hemorrhage could result. CBC analysis revealed a mild, microcytic, hypochromic anemia that likely was an anemia of chronic disease or caused by inflammation due to the presence of the chronic cranial implant. The serum chemistry panel revealed an increased GGT, decreased albumin, and increased globulins, suggestive of subclinical amyloidosis. An exploratory laparotomy was elected to determine the origin of the mass and to excise it if possible.

Figure 1.

(A) Left lateral and (B) ventrodorsal abdominal radiographs. A large, radiopaque, soft tissue mass is present in the ventral abdomen (white circle), with displacement of the intestines.

A midline laparotomy revealed the presence of a large (diameter, approximately 15.0 cm), well-encapsulated, moderately vascularized mass with a narrow, twisted peduncle that was wrapped within the greater omentum. Ligatures of 3-0 polyglactin 910 were placed around the peduncle of the mass, and the mass was removed without complication. Another 10 to 20 similar but smaller (diameter, 1.0 to 4.0 cm) nodules were present within the mesentery and greater omentum (Figure 2); approximately 10 of these masses were excised also. The liver was enlarged and pale, with rounded edges and a waxy appearance, suggestive of hepatic amyloidosis. Therefore, a liver biopsy was taken at this time. The macaque received buprenorphine (0.005 mg/kg IM every 12 h for 72 h) and recovered from surgery without complications. Abdominal distention and scrotal swelling resolved postoperatively.

Figure 2.

Intraoperative view of the abdomen. Many, multifocal, pale tan, soft, round nodules (white arrows) are scattered throughout the mesentery and greater omentum.

The masses subsequently were examined by a veterinary pathologist. The largest greater omental mass was an extensive (weight, 1.25 kg; dimensions, 15.0 × 13.0 × 9.5 cm), red and tan, soft, well-circumscribed, spherical, pedunculated tumor (Figure 3). The cut surfaces bulged on sectioning and revealed dark-red areas (hemorrhage) and dark, dull-yellow areas (necrosis). Except for their size, the smaller nodular masses all appeared similar to the largest mass. Impression smears made from the smaller nodular masses were oily and glistening. Wright–Giemsa and new methylene blue staining revealed them to be of low cellularity with scattered, rare, foamy, lipid-laden macrophages and plasma cells, along with scattered fibroblasts.

Figure 3.

Gross photographs of the largest mass resected from the greater omentum. The mass is an extensive (1.25 kg, 15.0 × 13.0 × 9.5 cm), red and tan, soft, well-circumscribed, spherical tumor that is twisted around its pedicle (white arrow), resulting in self-strangulation with secondary hemorrhage and necrosis.

Histologic evaluation revealed all of the masses to be similarly nodular, encapsulated, well-circumscribed, and expansile tumors consisting of sheets of relatively monotonous cells (Figure 4). The cells resembled white adipocytes that otherwise appeared histologically normal (that is, large, ovoid to polygonal cells containing single or few, clear, ovoid, intracytoplasmic vacuoles that displaced the nuclei to the periphery of the cell). A variable amount of secondary mixed inflammatory infiltrate was noted throughout the masses. Large areas of the tumors (often within the central portions) displayed coagulation necrosis, characterized by hypereosinophilia and karyolysis of tumor cells and inflammatory cells (Figure 4). There was also evidence of acute and chronic hemorrhage. According to these characteristics, a histologic diagnosis of self-strangulating abdominal lipomatosis was made. Liver biopsy confirmed the presence of hepatic amyloidosis.

Figure 4.

Low magnification photomicrograph of a smaller omental mass. The mass is composed of sheets of white adipocytes surrounded by a thick, fibrous pseudocapsule. Hematoxylin and eosin stain; magnification, 25×.

On day 291, the macaque represented for abdominal distension, scrotal swelling, and mildly loose stool. A physical examination under sedation was performed. An abdominal mass (diameter, approximately 5.0 cm) was palpated in the upper-right quadrant, and scrotal swelling was present. Radiographs revealed possible masses present between lumbar vertebrae L3 and L6 and a second mass between lumbar vertebrae L5 and L6, which displaced the intestinal tract dorsally and to the lateral right aspect of the abdomen. Hepatomegaly was evident. Ultrasonography examination revealed no evidence of intestinal or splenic entrapment within the masses. No involvement of the mass with the kidney, bladder, or liver was noted. An increase in globulins and a decrease in albumin were present on the blood chemistry panel, indicating potential subclinical amyloidosis or chronic inflammation. CBC analysis and other chemistry panel parameters were unremarkable. Given the recurrence of the masses and questionable prognosis, euthanasia was elected.

At necropsy, there were numerous, multifocal to coalescing, circumscribed, pale tan to yellow, soft to firm, pedunculated masses (diameter, 1.0 to 15.0 cm) scattered throughout the entire mesentery, greater omentum, lesser omentum, and serosal surfaces of the stomach, small and large intestines with no evidence of entrapment or strangulation of any portion of the gastrointestinal tract (Figure 5). However, most masses twisted around their respective peduncles, resulting in self-strangulation of the blood supply, with secondary hemorrhage and necrosis within the masses (Figure 6). The liver was pale tan and markedly and diffusely enlarged, with rounded margins and a waxy, firm, but friable texture. All other organs and tissues were within normal gross limits. Histologic examination revealed the masses to be neoplasms composed of white adipocytes (similar to those removed earlier), indicating recurrence of abdominal lipomatosis. A histologic diagnosis of recurrent or persistent strangulating abdominal lipomatosis, concurrent with diffuse hepatic amyloidosis, was made.

Figure 5.

View of the abdomen during necropsy. There are many, multifocal, pale tan, soft, round nodules scattered throughout the mesentery, greater omentum, lesser omentum, and serosal surfaces of the gastrointestinal tract. The mass circled in white is shown in Figure 6. Severe hepatic amyloidosis (white arrows) is also evident.

Figure 6.

Gross photographs of the largest greater omental mass (see Figure 5). The mass is an extensive, 15.0-cm, red and tan, soft, well-circumscribed, spherical tumor that is twisted around its pedicle (white arrow), resulting in self-strangulation with secondary hemorrhage and necrosis.

Discussion

Abdominal lipomatosis is characterized by multiple, benign masses consisting of normal white adipocytes. Neoplasms derived from white adipocytes can be classified according to either location, number of tumors involved, gross or subgross appearance, or microscopic characteristics (Figure 7).^11,12,16,23

Figure 7.

Classification of lipomas, adapted from references 11, 12, 15, and 21.

Peritoneal lipomas have been described commonly in horses and rarely in dogs and humans.^3,6,7,12,16 Benign lipomas arising from the mesentery are a common incidental finding in horses, and pedunculated strangulating lipomas are a common cause of colic in horses undergoing surgery.¹⁵ In horses, these masses may become pedunculated as they enlarge, thus allowing them to move around the abdomen.¹⁵ Due to their mobility, these tumors can become wrapped around intestine, causing intestinal strangulation.^3,8,15 In addition, masses that arise from a location adjacent to the gastrointestinal tract may cause an extraluminal obstruction of the intestines.¹⁵ The average age of horses that are affected by strangulating lipomas is approximately 19.2 y,¹⁵ with the incidence of strangulating lipomas being positively associated with increasing age.^3,6 In one study of 467 geriatric horses that presented at a university hospital, 7% had strangulating lipomas.³ In addition, 44% of the horses with small intestinal lesions in the cited study³ were diagnosed as having a strangulating lipoma.³ Treatment of strangulating lipomas in horses consists of surgical resection of the strangulated intestine and the associated lipoma.¹⁵

The most common mesenchymal tumors diagnosed in dogs are lipomas.¹⁶ In one retrospective study of 179 cases of canine lipomas, 98% were located subcutaneously. In another study involving 6 cases of canine nonsubcutaneous lipomas, the masses involved the abdominal or thoracic cavities, and all were simple lipomas, with the exception of one case with one mass extending from the umbilical attachment and a second lipoma infiltrating the sheath of the transversus abdominis. Lipomas arising from the abdominal cavity of canines in these cases originated from the retroperitoneal fat, periprostatic fat, urachal remnant, and from an unknown location. Clinical signs in canines with abdominal lipomas usually are attributed to compression of nearby organs and can include abdominal distention, dysuria, or tenesmus. Intrathoracic lipomas may result in coughing or dyspnea. In these cases, surgical resection is performed, with recurrence reported in only one case. Whether the so-called recurrence of this tumor was due to incomplete removal of the original tumor or the generation of a new lipoma from a novel location is unknown.¹⁶

According to the reported human cases, lipomas can arise from the trunk, extremities, abdominal cavity, thoracic cavity, and the intestinal mesentery.^4,12 The actual incidence of lipomas was likely higher than that reported because they tend to be subclinical.⁴ Genetics, obesity, diabetes mellitus, hypercholesterolemia, and traumatic injury are associated with lipomas. In humans, lipomas tend to be soft, slow-growing, moveable, and nonpenetrating in nature and may cause clinical signs if they become very large.⁴ These masses are considered one of the most common submucosal tumors in the gastrointestinal tract, but they usually remain small.¹¹ As with those in dogs, abdominal lipomas in humans can cause abdominal distention, weight loss, abdominal pain, anorexia, and constipation.⁴ Cases of diffuse infiltrating lipomatosis in humans are very rare.¹² Of these cases, approximately 80% occur on the lower extremities; however, the lesion can originate from the thoracic, abdominal, or pelvic cavity as well as the cervical, deltoid, and subcutaneous tissues.^23,25

Lipomas in nonhuman primates have been reported but only rarely have been noted to occur within the abdominal cavity. An omental lipoma in a mona monkey, an adrenal lipoma in a hamadryas baboon, as well as visceral lipomas, and myelolipomas in the mediastinum and pulmonary hilus in 2 lemurs have been reported.¹⁴ Reports of adipose tissue neoplasms in nonhuman primates are sparse and restricted to a few case reports of liposarcoma in a ring-tailed lemur and a galago monkey; a myelolipoma in a potto monkey; and mesenchymal skin and subcutaneous lipomas in macaques, patas monkeys, an African green monkey, guinea baboons, a ring-tailed lemur, and chimpanzees.^9,14,17-19

In addition, biopsies of masses in our population of rhesus macaques have revealed dermal and subcutaneous lipomas. The paucity of the clinical reports of lipomas in macaques may be due to underreporting related to the frequency of lipomas in veterinary medicine and their benign behavior.¹³

Abdominal neoplasias in macaques are a relatively common finding at necropsy. In a multiinstitutional survey, 13% of all tumors involved the gastrointestinal tract,¹⁴ and in aged nonhuman primates, gastrointestinal adenocarcinoma is one of the most common malignant neoplasms diagnosed in macaques.^5,18,21,24 In addition, there are reported cases of gastric and esophageal squamous cell carcinomas, esophageal leiomyomas, gastric and colonic leiomyosarcomas, gastric submucosal fibroma, gastrointestinal lymphoma, gastric adenoma, and gastric stromal tumors in macaques.^2,5,20,22 Benign gastric masses caused by Nochtia nochtii in macaques have also been reported.⁵

To our knowledge, this report is the first description of abdominal lipomatosis in a rhesus macaque. Like those in dogs,¹⁶ this tumor showed clinical signs associated with abdominal distention, and after recurrence, gastrointestinal signs that were likely linked to compression of the intestines. In this case of abdominal lipomatosis in a rhesus macaque, the animal originally demonstrated no clinical signs other than abdominal distention and scrotal swelling. Upon representation for this problem, clinical signs were accompanied by mildly loose stool, which may have been caused by compression of the intestines by the masses and abnormal motility in the gastrointestinal tract. The abdominal lipomas were pedunculated and due to secondary torsion along the peduncles, ischemic necrosis was present within the neoplasms. Whether recurrence of these masses was due to incomplete removal of the original masses or de novo generation of new tumors is unclear. Abdominal lipomatosis should be considered as a differential diagnosis for when presented with a case of abdominal distention in a rhesus macaque.