Abstract

A captive, 10-year-old male Ruwenzori fruit bat (Rousettus lanosus) (0.2 kg) was examined for inability to perch. Physical exam findings included tachypnea, dehydration, and enlarged abdomen. Abdominocentesis was grossly consistent with hemoperitoneum. Medical treatment successfully resolved the initial crisis and lead to clinical improvement over the next four days. Autotransfusion was utilized as part of supportive care without apparent complications. Subsequently, clinical condition declined, and exploratory surgery revealed probable metastatic neoplasia in the abdomen. Histopathology confirmed metastatic pancreatic carcinoma.

Introduction

Hemoperitoneum has been reported in a number of species.^{8,10,11,17,22} In domestic dogs and cats, trauma and neoplasia are the most common causes.⁴ These patients frequently present in circulatory collapse and initial supportive care is undertaken prior to definitive diagnosis. Medical management alone, including intravenous fluids, may be adequate for short-term supportive care and long-term resolution in some cases of traumatic hemoperitoneum. In other cases, surgical intervention is needed for treatment as well as definitive diagnosis.⁴

Autotransfusion of free blood recovered from body cavities is a recognized form of providing oxygen carrying capacity as well as hemodynamic support in veterinary and human medicine.^14,19 Advantages of autotransfusion include blood compatibility, elimination of infectious disease transmission, decreased risk of overhydration, and immediate availability. Potential disadvantages include induction of coagulopathy, dissemination of malignant cells or microemboli, and infusion of a contaminated sample.¹⁹

Pancreatic carcinoma has been identified in a number of animals and may present in a variety of ways, although hemoperitoneum is uncommon.^{1,13,16,18,20,21,23,25} Abdominal organ neoplasia is not commonly described in Chiroptera species.^2,3,5,6,12

Case Report

In 1997, Lincoln Park Zoo acquired the animal of this case as part of a single-sex group. The Ruwenzori fruit bats (Rousettus lanosus) are housed with straw-colored fruit bats (Eidolon helvum), and hyrax (Procavia capensis), in a glass-fronted exhibit. They are maintained under reversed light cycle at 78°F. All bats are bred captively and no additions have been made since acquisition. No major health concerns in the bats have been identified.

This animal was found on the exhibit floor. Physical exam revealed a lethargic animal with a taut, distended abdomen, dehydration (8–10%), cool skin, and mild tachypnea. Clinical condition declined during transportation to the veterinary hospital: mucous membranes became white, dyspnea developed, and abdominal swelling progressed. Percutaneous abdominocentesis removed 1 ml of non-clotting sanguineous fluid with packed cell volume (PCV) 17% and total protein (TP) 3.0 g/dl. Direct and sedimentation cytology of the abdominal fluid was consistent with whole blood (Table 1). Lactated Ringer’s solution with 2.5% dextrose (LRS + 2.5% dextrose, 15 ml/kg SQ) was administered. Whole-body radiographs showed homogenous soft tissue density in the abdomen, normal skeletal structure, and normal thoracic organs. Major considerations for hemoperitoneum included trauma, bleeding abdominal neoplasia, coagulopathy (toxin, liver disease, and thrombocytopenia), and organ torsion (stomach, spleen, or liver lobe).

Table 1. Abdominal fluid analysis for Ruwenzori long-haired fruit bat

The animal showed signs of progressive shock. Isoflurane anesthesia (IsoFlo, Abbott Laboratories, North Chicago, IL, USA) was induced to place an intraosseous (IO) catheter, repeated abdominocentesis, and abdominal ultrasound. The IO catheter was made from a 22-G, 1-inch hypodermic needle inserted into the left proximal radius with the animal in sternal recumbency. LRS + 2.5% dextrose was repeated (15 ml/kg IO) as a bolus, three times intra-procedurally. An autotransfusion was elected due to continued decline despite crystalloid support. A heparinized syringe was used for abdominocentesis to obtain 5 ml of abdominal fluid. Four ml (20 ml/kg) was administered IO; mucous membrane color improved and respiratory and heart rates declined. An additional 4 ml of abdominal fluid was removed and refrigerated. Ultrasound demonstrated free abdominal fluid, normal liver echogenicity, and a rounded mass in the left cranial abdomen. Enrofloxacin (Baytril, Bayer Corp., Shawnee Mission, KS, USA, 4 mg/kg IM) and vitamin K₁ (K-Ject, Burns Veterinary Supply, Inc., Rockville Centre, NY, USA, 2 mg/kg SQ) were provided. The animal was placed in an incubator with ambient temperature of 90°F and was eating later in the day. LRS + 2.5% dextrose was administered at 0.5 ml IO every 2 hours for 10 hours after recovery. Autotransfusion of 3 ml stored blood was repeated 4 hours after initial dose. Oxygen (3 L/min) was delivered into the incubator though an inhalant anesthetic unit.

The patient initially responded well to continued supportive care and was active and eating for three days, although the abdomen remained distended. LRS + 2.5% dextrose was continued IO until the catheter was removed on the third day. Abdominocentesis was repeated on day 2 and 3 (Table 1). Repeated ultrasound exam under anesthesia showed enlarged hepatic vessels and rounded masses of heterogenous echogenicity with occasional hypoechoic centers in the abdomen. Radiographs showed a normal thoracic cavity and loss of detail in the abdomen, although the cavity appeared smaller than on initial radiographs. Oxygen was discontinued on the fourth day.

On day 5, the animal declined, was weak and dehydrated. Blood was obtained under inhalant anesthesia for complete blood count (CBC) and serum chemistry evaluation. Abdominocentesis was repeated and the animal improved by afternoon (Table 1). Leukocytosis (15,000/µl) with neutrophilia (12,150/µl) and monocytosis (1,050/µl), anemia (18%), and panhypoproteinemia were present (albumin 2.4 g/dl, globulin 2.0 g/dl, and total protein 4.4 g/dl).¹⁵ Aspartate aminotransferase (AST) was increased at 302 IU/L and total bilirubin was increased at 2.4 g/dl.¹⁵

Clinical condition declined, occasional vomiting developed, and abdominocentesis was repeated seven days after presentation. On the eighth day, exploratory laparotomy was performed to allow definitive diagnosis and possible treatment. An IO catheter was placed in the right radius to supply intraoperative fluid support. LRS + 2.5% dextrose was administered at 0.25 ml IO every 15 minutes (5 ml/kg/h). Prior to surgery, 18 ml of sanguineous fluid was removed by abdominocentesis. After initial incision and removal of approximately 10 ml of abdominal fluid, pulse quality deteriorated. Hetastarch (6% Hetastarch in 0.9% NaCl, Gensia Sicor Pharmaceuticals Inc., Irvine, CA, USA, 5 ml/kg IO) was administered and pulse quality improved. Surgery revealed a lobulated, friable, yellow-white mass (3×2 cm) with ulcerated areas in the cranial left abdomen. Nodules were visible in the liver and by the spleen. The masses bled easily when handled. At 45 minutes into surgery, the patient went into acute respiratory arrest and cardiac arrest rapidly followed. Resuscitation efforts were not pursued.

Full necropsy and histopathology results were obtained. Grossly, two large masses were observed: a 3×3×1 cm mass adjacent to the duodenum and a 2×1×0.8 cm mass in the mesentery adjacent to the spleen. Similar masses of smaller size (generally under 5 mm) were noted throughout the abdominal and thoracic cavities. Histopathologically, the masses were consistent with pancreatic carcinoma. The gall bladder was surrounded by and impinged upon by the carcinoma, bile canaliculi had bile plugs, and ductules had large quantities of bile. The duodenum was also partially constricted by the neoplasia. Final diagnosis was pancreatic carcinoma with multicentric metastases and serosal bleeding.

Discussion

The abdominal fluid accumulation was likely secondary to pancreatic carcinoma hemorrhage, although hemoperitoneum is not commonly reported with this tumor.^{1,13,16,18,20,21,23} Pancreatic carcinoma is frequently aggressive with metastatic disease present at diagnosis, as in this case.^9,18,24 On initial presentation, collapse was believed due to acute hemorrhage. However, given the abdominal fluid volume, it seems plausible that chronic bleeding or ascites was also present. Initially, 9 ml of blood was removed but an estimated 5 ml (minimum) remained in the abdomen. Estimated abdominal fluid volume was approximately 70% of estimated blood volume, so it seems more likely that some chronic accumulation had occurred. Acute hemorrhage is expected to have a PCV close to that of the circulatory system, until compensatory mechanisms can adjust systemic volume, and the initial abdominal fluid PCV was 17%. Though it would have been helpful to obtain baseline bloodwork at the time of presentation, in very small animals, it is difficult to balance the need for monitoring blood parameters with the patient’s need for blood.

Fluid support is critical to helping animals recover from hypovolemic shock by establishing normal blood volume. Initial fluid support was in the form of the crystalloid LRS. Though this is the primary means of increasing vascular volume, an inadequate response was observed. Colloid support is used to increase the colloid osmotic pressure (COP) of the blood. In normal animals, COP is primarily provided by albumin. In disease states, blood protein levels may decrease. The optimal use of crystalloid and colloid support is debated, but colloid support may increase intravascular volume more rapidly and sustainably than crystalloids alone.²⁶ Blood and blood products are natural colloids. If severe anemia has developed, increasing oxygen carrying capacity of the blood is critical. Emergency autotransfusion of blood pooling in a body cavity is one means of achieving this. Due to a clinical assessment of rapidly progressing shock, this animal was auto-transfused despite being unable to clearly establish that the blood obtained was free of contamination. A whole blood transfusion from a conspecific could have been used but was not pursued due to the time delay in getting an animal and unknown risk of transfusion reaction.

Neutrophilic leukocytosis with monocytosis was likely related to stress and chronic inflammation. Panhypoproteinemia in dogs and cats is related to hemorrhagic loss, exudation, protein-losing enteropathy, or malassimilation, and was likely related in this case to hemorrhage and possibly ascites fluid accumulation.⁷ Increased AST in dogs and cats is related to increased hepatocellular permeability or muscle damage.⁷ Muscle damage is associated with creatine kinase (CK) elevations in many species. CK values were normal in this case, supporting a hepatic source of elevated AST. Total bilirubin increase is related to cholestasis or hemolysis.⁷ Bloodwork supported a diagnosis of chronic hemorrhage as well as liver disease with cholestasis or bile duct obstruction.

Exploratory surgery was delayed due to initial clinical improvement with medical management. Traumatic hemoperitoneum can be managed medically. The decision to surgically intervene was made when clinical condition deteriorated and abdominal swelling persisted. This animal did do well throughout a long anesthetic period. Providing presurgical correction of low protein levels and anemia with appropriate fluid administration might have increased stability during surgery even more. Supportive care was rewarding in the short term for this case, despite the severe, underlying disease process. During the clinical course and at necropsy, no indication of adverse reaction to the autotransfusions was noted, despite lack of filtering of the blood. Subjectively, the authors’ opinion is that it did help to stabilize this patient.

Acknowledgments

Special thanks to Joel Pond, CVT (Lincoln Park Zoo), Richard Nye, DVM (Midwest Bird and Exotic Clinic), and Michael Kinsel, DVM, DACVP (University of Illinois Zoo Pathology Program).

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