Introduction

An esophageal stricture is a pathologic narrowing of the esophageal lumen. Acquired esophageal strictures are caused by substantial injury to the esophageal lining and subsequent esophagitis extending into its submucosal or muscular layers (Venker-van Haagen et al., 2013; Marks, 2017). As the esophageal lining undergoes normal repair, scarring or fibrous connective tissue formation narrows the luminal diameter of the esophagus (Venker-van Haagen et al., 2013; Marks, 2017). Causes of esophageal injury and esophagitis in animals include gastroesophageal reflux, trauma (e.g., foreign bodies), chemical injuries (e.g., caustic substances or medications), or iatrogenic damage during endoscopy or surgery (Venker-van Haagen et al., 2013; Marks, 2017). Other causes of esophageal narrowing described in domestic mammals include congenital esophageal stenosis, a persistent right aortic arch, and intraluminal or extraluminal mass lesions such as neoplasia or abscesses (Venker-van Haagen et al., 2013; Marks, 2017).

The esophagus is arguably the most unique part of a sea turtle’s gastrointestinal tract and is lined with large, pointed, conical papillae covered by keratinized epithelium (Boylan et al., 2017). The keratinized papillae are found in all sea turtle species and life stages and serve to trap prey when the muscular esophagus contracts to expel excess seawater (Bjorndal, 1985). Esophageal injury in sea turtles is often the result of anthropogenic traumatic injuries, including esophagitis, abscessation, and fistulation secondary to fishing hooks and gear during incidental capture or accidental ingestion (Orós et al., 2004). This report describes an esophageal stricture with complete occlusion in a stranded juvenile green sea turtle (Chelonia mydas) suspected to be acquired secondary to prior unknown trauma and includes the turtle’s clinical presentation, computed tomography assessment, attempted treatment with endoscopic bouginage and surgical resection, and posmortem evaluation.

Case Report

In December 2022, a 2.3-kg juvenile female green sea turtle was rescued after stranding near Hatteras, North Carolina, USA, during a period of sea turtle cold-stunning. On admission to rehabilitation at the Sea Turtle Assistance and Rehabilitation (STAR) Center at the North Carolina Aquarium on Roanoke Island (Manteo, NC, USA), a physical exam found severe emaciation, a healing wound to the left ventral neck, bilateral conjunctival injuries, abnormal buoyancy, small barnacles covering 90% of its carapace, and a cloacal temperature of 12.8°C. Point-of-care diagnostics found mild anemia (packed cell volume, 22%; reported range, 26.4–42%; Bolten and Bjorndal, 1992), hypoproteinemia (total solids, 2.0 g/dl; reported range, 2.5–4.4 g/dl; Anderson et al., 2011), hyponatremia (139.6 mmol/L; reported range, 157–183 mmol/L; Bolten and Bjorndal, 1992), hypochloremia (87.6 mmol/L; reported range, 100–130 mmol/L; Bolten and Bjorndal, 1992), and ionized hypocalcemia (0.59 mmol/L; reported range, 0.87–1.24 mmol/L; Anderson et al., 2011). The turtle was treated with 20 ml/kg lactated Ringer’s solution (ICU Medical, Inc., San Clemente, CA, USA) SC and 50 mg/kg calcium gluconate (Covetrus, Inc., Portland, ME, USA) SC on admission, followed by 20 mg/kg ceftazidime (Sagent Pharmaceuticals, Raleigh, NC, USA) IM every 72 h for 30 days and topical ciprofloxacin ophthalmic solution USP 0.3% (Sandoz, Inc., West Princeton, NJ, USA) applied to both eyes every 12 h for 10 days. After a few weeks, staff reported the turtle was anorexic and losing weight. Given the high volume of stranded cold-stunned sea turtles admitted to the STAR Center, the turtle was transferred to the Karen Beasley Sea Turtle Rescue and Rehabilitation Center (KBSTRRC, Surf City, NC, USA) for further individualized care.

While at KBSTRRC, staff reported the turtle had persistent abnormal buoyancy and was dysphagic. Re-evaluation in mid-January 2023 found persistent emaciation, healing neck and conjunctival injuries, static mild anemia (packed cell volume, 20%; reported range, 26.4–42%; Bolten and Bjorndal, 1992), and hypoproteinemia (total protein, 1.8 g/dl; reported range, 2.5–4.4 g/dl; Anderson et al., 2011) characterized by hypoalbuminemia (0.8 g/dl; reported range, 0.6–2.1 g/dl; Bolten and Bjorndal, 1992). Previously observed electrolyte abnormalities had resolved. Whole-body radiographs revealed reduced volume to the lateral margin of the left lung, suggestive of pneumonia; consequently, treatment with 20 mg/kg ceftazidime IM every 72 h was continued. In late January, staff reported the turtle had persistent dysphagia. The turtle appeared to take longer to eat than conspecifics undergoing similar rehabilitation, could only ingest small pieces of fish, and would frequently and forcefully spout water and bits of fish from its nares while eating. In mid-February, a tube feeding was attempted, given ongoing dysphagia; however, the authors could not pass multiple sizes of red rubber catheters or a metal gavage tube, raising the suspicion of a cranial esophageal stricture. The turtle was referred to the North Carolina State University’s Veterinary Teaching Hospital (Raleigh, NC, USA) for further evaluation of a suspected cranial esophageal stricture via advanced imaging and endoscopy.

At the North Carolina State University’s Veterinary Teaching Hospital in late February, the turtle was anesthetized with 4 mg/kg ketamine (Covetrus, Inc.) and 20 μg/kg dexmedetomidine (Covetrus, Inc.) IV in the left dorsal cervical sinus. The turtle was intubated with a 2.5-mm uncuffed endotracheal tube, and anesthesia was maintained with 0–3% sevoflurane (Dechra Veterinary Products, Overland Park, KS, USA) with manual intermittent positive pressure ventilation. A head and neck CT without contrast was performed with a 64-slice scanner (SOMATOM Sensation 64, Siemens, Berlin, Germany) and found multifocal pockets of subcutaneous gas cranial to the shoulder bilaterally consistent with repeated subcutaneous fluid administration, but no evidence of an esophageal foreign body or intraluminal and extraluminal masses. Similarly, a focal ultrasound examination of the cervical region confirmed the lack of obvious esophageal compression or obstruction. Following computed tomography (CT) and ultrasonography, esophagoscopy was performed with 2.7- and 7.8-mm-diameter rigid and flexible endoscopes, respectively, as described previously (Pressler et al., 2003). Neither endoscope could advance past the caudal pharynx or proximal esophagus—the cranial esophagus appeared to be a blind-ended pouch. A guide wire was passed to puncture into what was expected to be the distal or aboral esophagus. Two sizes of bougie were introduced to widen the hole, and a flexible endoscope was passed. Once insufflated, no keratinized papillae were observed, indicating the endoscope was within the subcutaneous cervical fascia and an iatrogenic esophageal perforation had been created.

The turtle underwent an esophagotomy to repair the esophageal perforation and better confirm the esophageal stricture. The turtle was placed in dorsal recumbency, and the ventral neck was aseptically prepared and draped. Using sharp dissection, a longitudinal incision was made the length of the ventral neck with a #15 scalpel blade. The muscle layers were bluntly dissected, gently retracting the trachea to the left side to observe the esophagus. Two stay sutures were placed in the esophagus, and a longitudinal incision was made with a #15 scalpel blade. A 16 Fr red rubber catheter was first passed antegrade to the stomach and then retrograde to the point of resistance in the aboral esophagus. A second 16 Fr red rubber catheter was passed through the oral cavity caudally. An esophageal stricture was identified approximately 3 cm caudal to the oropharynx and was palpably firm and thickened (Fig. 1). The esophagus was slowly opened with a #15 scalpel blade cranially toward the esophageal stricture. The iatrogenic esophageal perforation was visualized laterally to the stricture, and the esophagus was completely occluded, with normal papillated mucosa covering both blind ends, separated by approximately 5 mm scar tissue. Because of its debilitated condition, unfavorable anatomic location for surgical resection, and insufficient tissue for anastomosis, it was elected to euthanize the turtle. While anesthetized, 1 ml of pentobarbital (EUTHASOL®, Virbac, Carros, France) was administered intracardiac through the plastron; cessation of a heartbeat was confirmed via Doppler ultrasound for 5 min. The turtle was submitted for necropsy and histopathologic evaluation.

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A necropsy confirmed an esophageal stricture and occlusion (Fig. 2). The occlusion was located approximately 3 cm aboral to the oropharynx on gross examination. The esophageal wall was circumferentially expanded by fibrous connective tissue up to 5 mm thick. The surrounding soft tissues to the left side of the esophageal stricture were mottled dark red to purple. Other pathologic changes noted on gross postmortem exam included concavity of the plastron, diffuse serous atrophy of fat, and muscle atrophy, all supportive of prolonged emaciation. A moderate number of metazoan parasites (likely trypanorhynch cestodes) were encysted along the serosal surface of multiple organs. Histopathology revealed the esophageal stricture was comprised of marked focal fibrosis with edema and mild perivascular lymphoplasmacytic inflammation; the etiology of the focal esophageal fibrosis was not evident histologically. Other incidental findings included multifocal granulomas throughout the spleen and liver with intralesional bacteria as well as granulomas within the pectoral muscle and mesentery associated with the aforementioned metazoan parasites.

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Discussion

This case report describes an esophageal stricture with complete occlusion in a sea turtle, a rare and severe esophageal disease. Given the age class and size of the turtle, the authors suspect the esophageal stricture was acquired secondary to prior unknown trauma and less likely progressive congenital stenosis. The inciting esophageal injury may have been related to the healing wound on the turtle’s left ventral neck on admission to rehabilitation. The turtle would not have been releasable without veterinary intervention, given its dysphagia and progressive emaciation. If the endoscopic or surgical intervention had been successful, the turtle’s prognosis would still have been guarded, and the turtle might still have been nonreleasable and required a modified long-term diet under managed care as a permanent resident. In domestic feline and canine patients, esophageal strictures carry a fair-to-guarded prognosis (Venker-van Haagen et al., 2013).

In hindsight, the water and masticated fish forcefully spouted from the turtle’s nares while eating was likely regurgitation, which along with dysphagia, are classic signs of esophageal strictures in domestic animals (Marks, 2017). Pneumonia documented in mid-January observed on whole-body radiographs was likely secondary to dysphagia and aspiration pneumonia, although other etiologies, including cold-stunning (Stockman et al., 2013), cannot be ruled out. Although not a factor in the present case, gastroesophageal reflux associated with anesthesia is reportedly the most common cause of esophageal strictures in domestic canine and feline patients (Pearson et al., 1978; Galatos and Raptopoulos, 1995a, 1995b; Wilson et al., 2006). Of the diagnostic modalities employed, esophagoscopy proved to be a rapid, minimally invasive method to diagnose the turtle’s esophageal stricture. In domestic animals, esophagoscopy is also useful in determining an esophageal stricture’s length and luminal diameter, as well as any concurrent esophagitis (Venker-van Haagen et al., 2013).

Once diagnosed, therapeutic goals for esophageal strictures are to widen intraluminal narrowing, protect the esophageal lining from additional injury, and eliminate or mitigate any inciting cause. Endoscopic-guided mechanical dilation of esophageal strictures by using balloon catheters or bougienage is preferred in domestic canine, feline, and equine patients (Bissett et al., 2009; Prutton et al., 2015) and was pursued initially in this case with the expectation the turtle may have required multiple dilatations. Surgical resection of esophageal strictures is possible but suboptimal in domestic animals (Venker-van Haagen et al., 2013); in the present case, resection was not possible due to anatomical location and insufficient tissue for anastomosis. Placement of an esophageal stent or indwelling balloon dilating esophagostomy tube show promise as novel interventions in domestic canine and feline patients (Lam et al., 2013; Tan et al., 2018), but their application in sea turtles would only be possible in permanent residents under managed care.

Intestinal and cloacal strictures have been previously reported in green sea turtles undergoing rehabilitation or under long-term managed care (Boylan et al., 2017). The etiologies of the strictures were unknown in most cases, although one was associated with an intestinal leiomyoma (Helmick et al., 2000; Erlacher-Reid et al., 2013). Why green sea turtles are overrepresented in the literature (albeit sparsely) for sea turtle gastrointestinal strictures is unclear. Intestinal strictures in green sea turtles could result from a combination of intestinal hypomotility or ileus and species-specific anatomic adaptations (e.g., hindgut fermentation, proportionally longer gastrointestinal tract), which may predispose to intestinal damage or obstruction (Erlacher-Reid et al., 2013). Esophageal stricture in sea turtles would more likely be a severe sequela of anthropogenic esophageal injury, which could range from esophagitis following fishing hook or gear ingestion to complete transection by a boat strike or penetrating wound (e.g., gaff or stingray spine).

In light of the present case, esophageal stricture should be considered a differential for sea turtles undergoing rehabilitation and exhibiting progressive weight loss, dysphagia, or regurgitation. If an esophageal stricture is suspected in a sea turtle, radiography with positive contrast media or CT may be helpful but potentially inconclusive. Esophagoscopy is likely the best modality for diagnosing and potentially mechanically dilating an esophageal stricture in sea turtles, although surgical exploration may be required to confirm a diagnosis. Similar to domestic species, an esophageal stricture in a sea turtle carries a guarded prognosis for long-term survival and release.