History
A 19-year-old 0.45-kg sexually intact female gray-headed flying fox (Pteropus poliocephalus) was presented to the Zoological Medicine Service at the University of Florida because of acute inspiratory dyspnea. The caretakers reported that the bat suddenly developed signs of heavy breathing and foaming at the mouth earlier in the day and that the bat's diet included fresh whole grapes along with other fruit.
On physical examination, the bat was bright and alert but dyspneic and produced copious clear viscous foam from the mouth and nose. Cardiac and pulmonary auscultations were hindered by referred noise from the upper airway. The patient underwent general anesthesia (isoflurane delivered in oxygen by face mask) for radiographic examination (Figure 1).


Right lateral (A) and ventrodorsal (B) whole-body radiographic images of an anesthetized 19-year-old 0.45-kg sexually intact female gray-headed flying fox (Pteropus poliocephalus) evaluated because of acute dyspnea and copious amounts of clear foam produced from the mouth and nose.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471


Right lateral (A) and ventrodorsal (B) whole-body radiographic images of an anesthetized 19-year-old 0.45-kg sexually intact female gray-headed flying fox (Pteropus poliocephalus) evaluated because of acute dyspnea and copious amounts of clear foam produced from the mouth and nose.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471


Right lateral (A) and ventrodorsal (B) whole-body radiographic images of an anesthetized 19-year-old 0.45-kg sexually intact female gray-headed flying fox (Pteropus poliocephalus) evaluated because of acute dyspnea and copious amounts of clear foam produced from the mouth and nose.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471


Right lateral (A) and ventrodorsal (B) whole-body radiographic images of an anesthetized 19-year-old 0.45-kg sexually intact female gray-headed flying fox (Pteropus poliocephalus) evaluated because of acute dyspnea and copious amounts of clear foam produced from the mouth and nose.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471
Right lateral (A) and ventrodorsal (B) whole-body radiographic images of an anesthetized 19-year-old 0.45-kg sexually intact female gray-headed flying fox (Pteropus poliocephalus) evaluated because of acute dyspnea and copious amounts of clear foam produced from the mouth and nose.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471
Radiographic Findings and Interpretation
Radiography revealed a gas-distended esophagus and a round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter) superimposed with the caudal aspect of the intrathoracic portion of the esophagus (Figure 2). The cranial aspect of this mass was outlined by gas and considered to have been in the lumen of the esophagus; however, the caudal extent was not clearly demarcated. The cardiovascular structures, pleural cavity, and pulmonary parenchyma were interpreted as radiographically normal. There was a diffuse lack of peritoneal and retroperitoneal serosal detail, considered a normal variation for the species of bat; however, emaciation was not completely excluded. The gastrointestinal tract had marked, diffuse gas distention, which we attributed to aerophagia secondary to respiratory distress. Other incidental radiographic findings included dental disease (eg, alveolar bone widening of multiple teeth) and degenerative skeletal changes (eg, multifocal intervertebral disk space narrowing, spondylosis deformans, and osteophyte and enthesophyte formation of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints).




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471




Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471
Same images as in Figure 1 (A and B) plus colli-mated right lateral (C) and ventrodorsal (D) thoracic radio-graphic images of the same bat. The esophagus (dotted outline) has diffuse gas distention. A round to ovoid, homogeneously soft tissue opaque mass (approx 1 cm in diameter; asterisks) is superimposed with the caudal aspect of the intrathoracic portion of the esophagus; the cranial aspect of this mass is outlined by gas and considered to occupy the entire esophageal lumen at the site. There is a diffuse lack of peritoneal and retroperitoneal serosal detail, and the gastrointestinal tract has marked gas distention. Dental disease is evident with alveolar bone widening (white arrows) at multiple teeth. Degenerative skeletal changes include multifocal intervertebral disk space narrowing (black arrowheads), spondylosis deformans (black arrows), and osteophyte and enthesophyte formation (white arrowheads) of the right shoulder joint, left hip joint, and bilateral elbow, carpal, and stifle joints.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471
Differential diagnoses for the intraluminal esophageal mass included a foreign body, neoplasia, abscess, granuloma, and hiatal hernia. Given that the clinical signs developed suddenly and that fresh whole fruit was provided in the diet, an esophageal foreign body, such as a grape, was initially the main concern. The bat was anesthetized and intubated, general anesthesia was maintained with isoflurane delivered in oxygen, and esophageal endoscopy was performed (not shown). A highly vascularized soft tissue mass in the caudal aspect of the esophagus occupied most of the esophageal lumen and was suspected to have been a malignant neoplasm.
Treatment and Outcome
The owner elected euthanasia and necropsy for the bat. In the region of the gastroesophageal junction, there was circumferential thickening (approx 2 × 1.8 × 0.3 cm) of the caudal aspect of the intrathoracic portion of the esophagus, consistent with the soft tissue mass seen on radiography and endoscopy. The luminal surface of this esophageal thickening was white-gray and granular (Figure 3).

Necropsy image of the incised, isolated esophagus (E), esophageal mass (arrowheads), and stomach (S) of the bat described in Figure 1, showing the luminal surfaces of each in the region of the gastroesophageal junction. A portion of the liver (L) remains attached and also grossly appears affected by the mass.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471

Necropsy image of the incised, isolated esophagus (E), esophageal mass (arrowheads), and stomach (S) of the bat described in Figure 1, showing the luminal surfaces of each in the region of the gastroesophageal junction. A portion of the liver (L) remains attached and also grossly appears affected by the mass.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471
Necropsy image of the incised, isolated esophagus (E), esophageal mass (arrowheads), and stomach (S) of the bat described in Figure 1, showing the luminal surfaces of each in the region of the gastroesophageal junction. A portion of the liver (L) remains attached and also grossly appears affected by the mass.
Citation: Journal of the American Veterinary Medical Association 259, 5; 10.2460/javma.259.5.471
Results of histologic examination indicated squamous cell carcinoma that had expanded the mucosa of the esophagus, infiltrated the esophageal submucosa and muscularis layers, focally invaded into and through the diaphragm, and superficially invaded into the liver. There were frequent keratin pearls and keratinization of neoplastic cells, 1 to 9 mitotic figures/hpf (400× magnification), and superficial necrosis and bacterial colonization.
Comments
On radiography, the esophageal squamous cell carcinoma in the bat of the present report was large enough to have been recognized as a soft tissue mass. Additionally, esophageal tumors may cause a mass effect, show evidence of mineralization, or potentially not be evident radiographically. The bat's esophagus was also gas-distended cranial to the mass; however, this radiographic finding may not be present in all affected patients. Further characterization of esophageal masses may require additional diagnostic imaging, such as positive-contrast esophagography, CT, and endoscopy. Definitive diagnosis requires cytologic examination, histologic examination, or both.
Esophageal neoplasms reported in gray-headed flying foxes include metastatic carcinoma, fibropapilloma, subcutaneous fibrosarcoma, and rhabdomyoma.1 In dogs and cats, benign or malignant esophageal neoplasia is rare and accounts for < 0.5% of all neoplasia in these species.2
The bat of the present report was 19 years of age; similarly, most affected dogs and cats are older, and there is no predilection for sex or breed. The more commonly reported esophageal neoplasms in dogs and cats include squamous cell carcinoma, leiomyosarcoma, fibrosarcoma, and osteosarcoma.3 Squamous cell carcinoma is common in cats, with the middle third of the esophagus cranial to the thoracic inlet most commonly affected. Except for animals with benign esophageal lesions,3 lymphoma, or low-grade leiomyosarcoma,4 the prognosis for cure or palliation is very poor for dogs and cats with esophageal neoplasia, especially carcinomas, because of poor surgical resection options and high metastatic rates.
In animals with esophageal neoplasia, clinical signs may include weight loss, dysphagia, regurgitation, signs of pain when swallowing, and signs related to aspiration pneumonia. Other clinical findings, such as hypertrophic osteopathy, can be seen with esophageal neoplasms, especially with sarcoma associated with Spirocera lupi.5,6 The bat of the present report had dyspnea, which could have been attributed to an accumulation of saliva in the oral cavity secondary to esophageal obstruction, with these secretions partially obstructing the larynx; however, there was no radiographic or postmortem evidence of aspiration pneumonia. Radiographically, this bat diffusely lacked peritoneal and retroperitoneal serosal detail, which was considered a clinically normal variation for the species; however, emaciation was not completely excluded.
In the bat of the present report, squamous cell carcinoma had invaded the bat's diaphragm and liver, and similar features of neoplastic invasion into adjacent tissues have been described in human medicine.7 The probable explanation for the superficial colonization of bacteria seen on histologic examination of the esophageal tumor in this bat may have represented bacterial translocation secondary to tumor necrosis.
Radiography is a relatively inexpensive, widely available, and fast first-line diagnostic imaging modality that can be used to detect structural abnormalities of the esophagus. In gray-headed flying foxes with a soft tissue opaque mass in the caudal portion of the esophagus, malignant neoplasia should be considered as a differential diagnosis.
References
- 1. ↑
Ladds P. Pathology of Australian native wildlife. Colling-wood, Australia: CSIRO Publishing, 2009;429–456.
- 2. ↑
Ridgway RL, Suter PF. Clinical and radiographic signs in primary and metastatic esophageal neoplasms of the dog. J Am Vet Med Assoc 1979;174:700–704.
- 3. ↑
Hamilton TA, Carpenter JL. Esophageal plasmacytoma in a dog. J Am Vet Med Assoc 1994;204:1210–1211.
- 4. ↑
Farese JP, Bacon NJ, Ehrhart NP, et al. Oesophageal leiomyosarcoma in dogs: surgical management and clinical outcome of four cases. Vet Comp Oncol 2008;6:31–38.
- 5. ↑
Ranen E, Lavy E, Aizenberg I, et al. Spirocercosis-associated esophageal sarcomas in dogs. A retrospective study of 17 cases (1997–2003). Vet Parasitol 2004;119:209–221.
- 6. ↑
Dvir E, Kirberger RM, Mukorera V, et al. Clinical differentiation between dogs with benign and malignant spirocercosis. Vet Parasitol 2008;155:80–88.
- 7. ↑
DeVita VT, Hellman S, Rosenberg SA. Cancer, principles & practice of oncology. 7th ed. Philadelphia, PA: Lippincott, Williams & Wilkins, 2005;713–761.