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Extraoral surgical correction of lingual entrapment in a Chinese goose (Anser cygnoides).

Abstract: An adult female Chinese goose (Anser cygnoides) presented with a ventral displacement of the hyoid apparatus, associated with distension of the intermandibular sublingual space and of the gular skin, causing difficulties with prehension and deglutition of food and water. Physical examination revealed that the tongue was able to move normally and could be replaced into a normal anatomical position by external compression of the distended ventral intermandibular region. A mild hypoalbuminemia was the only remarkable finding of the biochemistry panel. Radiographs and computed tomography scan of the head and neck regions confirmed a normal hyoid apparatus. An extraoral surgical reconstruction of the distended intermandibular skin was performed: the excess skin was incised and resected and the margins of the incision were sutured with appropriate tissue tension to obtain a good apposition and prevent ventral displacement of the hyoid apparatus. Postoperative complication included airway obstruction by a large amount of respiratory secretions, which were successfully aspirated from the trachea. A supportive elastic bandage was placed at the level of the beak commissure during the following 24 hours in order to reduce downward pressure on the suture line and minimize the risk of dehiscence of the suture. The goose resumed eating within 4 hours following the surgery and oxygen supplementation was discontinued after 24 hours. Respiration was assessed as normal and the tongue remained permanently in normal position. The lingual entrapment did not recur during the following 18 months.

Key words: lingual entrapment, hyoid apparatus, computed tomography, avian, Chinese goose, Anser cygnoides

Case Report

A 3.3 kg adult female Chinese goose (Anser cygnoides) was referred to the William R. Pritchard Veterinary Medical Teaching Hospital of the University of California Davis (Davis, CA, USA) for evaluation of an abnormal ventral intermandibular distension causing difficulties with prehension and deglutition of food and water. The goose was adopted from a shelter 2 years previously by the owners and its exact age was unknown. It was kept in an outdoor enclosure lined with solid rubber floor mats covered with hay bedding. A 120 x 180 cm kennel with a solid roof and a kiddie pool were provided. The diet consisted of waterfowl pellets (Mazuri, Purina, St Louis, MO, USA) and a variety of vegetables, including lettuce and broccoli. The goose had been boarded for 2 days, 2.5 months before presentation. The exact diet offered during the boarding period was unknown. Results of a preboard examination including a complete blood count (CBC) and plasma biochemical panel, were unremarkable. No abnormalities with regards to the tongue mobility, appearance of the gular region, or behavior of the patient were observed at that time.

[FIGURE 1 OMITTED]

About 2 weeks after boarding, the owners observed the bird violently shaking its head and regurgitating its food. The referring veterinarian reported discomfort on palpation of the caudal intermandibular region, with no obvious visible lesions on the beak, oropharyngeal mucosa, or tongue. Treatments prescribed were sucralfate (Carafate, Marion Merrell Dow Inc, Kansas City, MO, USA; 100 mg/kg PO ql2h x 4 d) and cephalexin (150 mg/kg PO ql2h x 7 d). No improvement was noticed during the following week, and the patient was readmitted to the referring veterinarian for a contrast-enhanced digestive study. The radiographs showed a normal upper gastrointestinal tract, but multifocal small ulcerative lesions were noted under the tongue at that time. Treatments prescribed were carprofen (Rimadyl, Pfizer Animal Health, New York, NY, USA; 4 mg/kg PO ql2h x 14 d), ceftiofur hydrochloride (Excenel, Pfizer Animal Health, New York, NY, USA; 11 mg/kg PO ql2h x 5 d), tramadol (Ultram 50 mg tablet, Janssen Raritan, NJ, USA; 7 mg/kg PO q12h x 14 d), and midazolam (0.6 mg/kg IM q24h x 11 d). Despite a transitory improvement, the goose continued to shake its head and regurgitate its food. Its appetite began to decrease, and the owners noticed that the goose was unable to groom. After 3 weeks of treatment, a 10% weight loss was noticed. Vitamin A (Radiance, Zhejiang, China; 2 400 IU/kg PO q24h x 15 d) and gavage feeding at home with pellets slurry were prescribed. A month after the initial discomfort was noticed, ventral displacement of the hyoid apparatus, associated with distension of the intermandibular sublingual space and of the gular skin, were observed on oral examination. The owners began tube feeding the bird in the crop for 4 days, and then started replacing the tongue into its normal position by applying manual pressure to the distended ventral intermandibular region. Once the tongue was in normal position, the goose was able to feed for a few seconds.

On presentation to the University of California Davis, the goose was bright and well hydrated and had a decreased body condition score of 3/9. Mild pododermatitis was noticed bilaterally with firm fibrous swellings of the proximal interphalangeal joint of the second digit. No pain was elicited on palpation of the periarticular proliferative lesions. The tongue was deviated ventrally, enclosed within the previously described distended ventral intermandibular sublingual space. This external distension of the soft tissues measured 2.5 cm in height and was associated with mild dermal erythema (Fig 1). The tip of the tongue appeared rounded and shortened. However, its was able to move the tongue appropriately when it was replaced into a normal anatomical position by external compression of the distended ventral gular skin. When offered waterfowl pellets soaked in water, the goose appeared interested and attempted to ingest them and repeatedly raised its head and engaging in exaggerated swallowing motions but unable to swallow. When offered water, the goose would submerge its beak and move it rapidly from side to side, then raise its head and thrust it back and forth with little water successfully swallowed. A 20-cm long, 3-cm wide band of elastic bandage (Vetrap, 3M, St Paul, MN, USA) was cut, and a 2-cm diameter hole was created 2 cm from an extremity of the bandage where the frontal knob was placed to prevent the bandage from slipping rostrally. The bandage was positioned around the head, just caudal to the commissure of the beak ventrolaterally. This bandage compressed the distended intermandibular sublingual tissue and reduced the hyoid apparatus into normal position, while still allowing the bird to open its beak because of the elasticity of the Vetrap bandage. After placing the bandage, the bird was able to drink water normally and to retrieve and swallow pellets both floating in water and placed on the ground. A complete neurologic examination did not reveal any neurologic deficit.

[FIGURE 2 OMITTED]

Differential diagnoses considered for the observed submandibular lingual entrapment were a skeletal abnormality of the hyoid apparatus (including luxation or fracture) or a muscular or a neurologic dysfunction. The hyoid apparatus of the Chinese goose is composed of a single entoglossal bone, paired rostral basibranchial bones, an urohyal bone, paired ceratobranchial bones, and paired epibranchial bones. (1-3) A fracture of any of these bones was a possibility. Possible muscular injuries were a tear, straining, overstretching, or elongation of the hyobranchial apparatus, including the branchiomandibularis muscle (tongue protractor), cricohyoideus muscle (tongue retractor), stylohyoideus muscle (retracting and raising the tongue), ceratoglossus muscle, hypoglossus muscle (lateral movements of the tongue), intermandibularis muscle, serpiohyoideus muscle, interceratobranchialis muscle, mesoglossus muscle, or genioglossus muscle. (1,4,5) A multifocal muscular disease or a neurologic problem were considered less likely due to the normal movements of the tongue and normal deglutition once the bandage was placed. However, a dysfunction of the trigeminal nerve, whose mandibular branch innervates the mylohyoideus muscles, (5) or a dysfunction of the hypoglossal nerve which innervates, among others, the cricohyoideus, ceratoglossus muscle, and hypoglossus muscles (5) were considered in the differential diagnosis.

Multiple orthogonal and oblique radiographs of the skull and ventrodorsal and right lateral whole body radiographs were obtained with the goose sedated with midazolam (0.7 mg/kg IM) and butorphanol (Torbugesic, Fort Dodge Laboratories Inc, Madison NJ, USA; 0.7 mg/kg IM), revealing soft-tissue distension in the intermandibular sublingual region with ventral displacement of the hyoid apparatus (Fig 2). The tongue appeared to be contained within soft tissue ventrally to the mandibles. Radiographs of the neck did not reveal any abnormality. Radiographs of the feet showed bilateral soft-tissue opacities at the level of the proximal interphalangeal joint of the second digit, without involvement of the joint or bones. Because a reducible luxation of the entoglosso-basibranchial joint or a nondisplaced fracture of a ceratobranchial bone (6) could not be ruled out, a computed tomography scan was recommended.

A blood sample was obtained from the right medial tarsometatarsal vein for a CBC and plasma biochemical panel. The CBC results were unremarkable. The results of the plasma biochemical analysis showed a mild hypoalbuminemia (1.4 g/dL; ISIS (7) reference interval 1.6-2.4 g/dL), which was attributed to chronic inflammation or malnutrition associated with the recent weight loss over the last 2 months.

[FIGURE 3 OMITTED]

A computed tomography scan was performed the next day to elucidate the abnormal position of the tongue and hyoid apparatus. The bird was premedicated with midazolam (0.7 mg/kg IM) and butorphanol (0.7 mg/kg IM) for intravenous catheter placement. Anesthesia was then induced with propofol (4.5 mg/kg IV), with additional isoflurane 3% delivered via facemask. The bird was then intubated with a 5-0 mm uncurled endotracheal tube and maintained under isoflurane anesthesia 1%-3% during the procedure by mechanical ventilatation (Bird Mark 7 respirator, Carefusion Corporation, San Diego, CA, USA). Fluids were administered intravenously at a rate of 10 mL/kg/h. Body temperature was maintained with a warming pad, and the bird was monitored using electrocardiogram, end-tidal C[O.sub.2], and pulse oximetry. The computed tomographic images were acquired both with the tongue in a normal anatomic position (by applying sustained pressure to the ventral intermandibular soft tissues during the scan) and with the tongue in the abnormal anatomic position as the bird presented (no compression of the intermandibular soft tissues). Contiguous computed tomographic images were made with 1.3 mm-slice thickness using tube parameters of 120 kV, 79.0 mA on a 16-slice helical scanner (LightSpeedl6, GE, Milwaukee, WI, USA) from rostral to the beak to include the sixth cervical vertebra. Three-dimensional volume rendered models were made to compare the intermandibular and pharyngeal region before and after repositioning. Repositioning of the hyoid apparatus produced variable angulation between the entoglossum and the rostral basibranchial bone without any detectable lesion (Fig 3).

The next day the goose was anesthetized for an extraoral surgical reconstruction of the distended gular skin. The goal of the surgical procedure was to resect the excessively stretched gular skin while reducing the ventral displacement of the hyoid apparatus, to maintain a sustained ventral pressure applied to the hyoid apparatus by the intermandibular sublingual soft tissues, thus keeping the tongue in normal position. The goose was pre-medicated with midazolam (0.7 mg/kg IM), butorphanol (0.7 mg/kg, IM) and glycopyrrolate (Baxter Healthcare Company, Deerfield, IL, USA; 0.01 mg/kg IM). An intravenous catheter was placed on the left tarsometatarsal vein and anesthesia was induced with propofol (9 mg/kg IV) and then maintained with isoflurane 1%-3% delivered via facemask. A slow intravenous injection of cefazolin (20 mg/kg) was administered. The bird was then intubated with a 5-0 mm uncuffed endotracheal tube and a tracheal tube humidifier (Humidi-vent, Mini Agibeck Product, Hudson RCI, Temecula, CA, USA) was connected between the endotracheal tube and the circuit to prevent desiccation of the airways. The goose was monitored using ECG, end-tidal C[O.sub.2], [O.sub.2] saturation, and esophageal temperature. The goose was mechanically ventilated during the procedure to maintain the end-tidal C[O.sub.2] between 36 and 41 mmHg. An arterial catheter was placed in the left ulnar artery, and the arterial blood pressure was monitored every 5 minutes. The feathers were clipped and plucked from the cranial intermandibular region to caudal to the epibranchial bones, and the skin was surgically prepared. The skin was pulled taut, and the outline of the incision (approximately 7 cm x 4 cm) to resect the excess skin was marked with a surgical pen. An incision was made with a #15 scalpel blade through the skin along the markings. Allis tissue forceps were used to apply appropriate tension on the flap, and bipolar radiosurgery was used to incise the skin and dissect the dermis from the underlying connective tissue while ensuring hemostasis. A series of simple interrupted sutures of 3-0 polydioxanone (PDS, Ethicon, Johnson & Johnson Company, Somerville, NJ, USA) were then placed subcutaneously to reduce dead space and reconstruct appropriate tissue tension in the area, followed by superficial subcutaneous reconstruction with 3-0 PDS in a simple continuous pattern. Finally, 3-0 PDS in a simple continuous pattern was placed intradermally to provide skin apposition.

[FIGURE 4 OMITTED]

After initial recovery from anesthesia, the goose showed signs of inspiratory distress in ventral recumbency. The patient was reintubated with a 5.0 mm endotracheal tube and reanesthetized with isoflurane. A plug of mucus was visualized approximately 10 cm from the glottis in the trachea. Mucus obstructing the trachea was retrieved with suction. After removing mucus from the trachea, the goose still showed intermittently increased inspiratory effort but these modifications in the breathing pattern were minimal and did not preclude extubation. The goose was therefore extubated, and no recurrence of the tracheal obstruction occurred. The goose was kept in an oxygen chamber and administered meloxicam (Metacam, Boehringer Ingelheim Vetmedica Inc, St Joseph, MO, USA; 0.5 mg/kg SC once), with resolution of the respiratory signs within 24 hours. A bandage made of Vetrap was replaced just caudal to the beak commissure as previously described preoperatively and was maintained in place during the next 24 hours to reduce downward pressure on the suture line and minimize the risk of dehiscence (Fig 4). The goose ate with great appetite the night after surgery. After bandage removal, the tongue remained in normal position and the bird demonstrated normal ability to eat and drink. The goose was discharged with ceftiofur crystalline free acid injections (Excede, Pfizer Animal Health; 50 mg/kg IM q4d x 2 [wk.sup.8]) and meloxicam (0.5 mg/kg SC q12h x 3 wk). Injectable medications were elected due to the potential for oral trauma with oral administration of drugs and owner concerns and preferences. The owners were instructed to feed only soft food, including soaked pellets and finely cut greens, and to gently clean the surgical wound with diluted 0.05% chlorhexidine solution after each meal. Small quantities of food were offered 5 times a day for the 3 following weeks while ensuring the goose was gaining weight at home.

Three weeks after the procedure, the patient was presented for a follow-up appointment. The goose was reported to be doing well at home, with no difficulty eating, drinking, or grooming, and a normal activity level. It had regained 15% of its weight, increasing to 3.8 kg, and no respiratory difficulties were reported. Meloxicam was discontinued at that time. There was no recurrence of the ventral displacement of hyoid apparatus during the next 18 months.

Discussion

This adult female Chinese goose was diagnosed with a submandibular lingual entrapment, which was successfully surgically reconstructed. Development of an intermandibular soft-tissue distension has been previously reported in large herbivorous waterfowl. (9) In severe or chronic cases, intermandibular soft tissues can stretch to the point that the tongue slips ventrally and cannot be repositioned by the bird. (10) This condition has been reported anecdotally in a Toulouse goose (Anser anser domesticus), black swans (Cvgnus atratus), cygnets between 2 and 4 months of age, and Australian shelduck (Tadorna tadornoides) due to their tendency to eat more fibrous plant material. (5,10) To the authors' knowledge, this condition has not been previously described in a Chinese goose. The goose tongue is composed of 4 parts rostrally to caudally: apex, body, lingual prominence, and root of the tongue. (11) Grandy corpuscules and Herbst corpusucles are located in the anterior part of the beak skin and form the "bill tip organ." (11) The beak edges contain laminae while the tongue edges contain conical papillae and filiform papillae. (11) The ventral side of the rostral part of the tongue includes a structure called the "lingual nail," which is a hard, well-keratinized epithelial structure that ensheaths the apex of the tongue and is able to stretch and function as a spoon. (11) Four types of food intake have been identified in Anseriformes: grazing, pecking, drinking, and filter feeding. Grazing and pecking are used to grasp solid food items. (11) Pecking starts with grabbing the grains by the tip of the beak. The papillae of the tongue, together with the beak, help to cut the plants before intraoral transport. The apex and the lingual prominence are involved and move to transport the food toward the esophagus. (11) During grazing, the goose uses the lateral rims of the beak to grab the leaves of grass, which are broken off across the lateral filtering lamellae, and swallowed. (11)

A suspected cause of submandibular lingual entrapment is intake of unsuitable forage that forms a sublingual ball of grass. (10,12) When the goose consumes soft, supple greenery, the food is easily broken into short manageable pieces. Longer, dry, or fibrous grass species often require repeated sideways movements to be broken. One hypothesis is that this material may become trapped sublingually. (10) Although in most cases, normal mastication or dabbling in water eventually dislodges the grass ball, occasionally these food items remain entrapped laterally to the frenulum in the intermandibular space for an extended period, stretching the intermandibular skin and leading to further accumulating of debris. (10) Most of the muscular development of the goose tongue is dedicated to dorsal and cranial tongue movement. (6) In most cases of tongue entrapment, the bird does not have the ability to withdraw the tongue from the pouch created in the intermandibular space and to reposition it dorsally because it cannot retract the tongue far enough caudally. (10) Under normal grazing conditions, waterfowl have the opportunity to select grazing material that best suits their dietary needs, which is not always the case in captivity. (10) Dry soybeans and cowpea have been associated with esophageal impaction, (13) but the precise cause of sublingual impaction has not been identified. In the case presented here, a pelleted diet of appropriate quality and a variety of greens were offered by the owners, although the goose had access to hay bedding. Therefore, the cause of the submandibular lingual entrapment remains unknown.

Other differential diagnoses included a skeletal abnormality of the hyoid apparatus and a muscular or neurologic dysfunction. In the reported case of a goose with a fracture of a ceratobranchial bone, the clinical presentation was similar to this case but the bird was able to eat despite the fracture and the swelling was asymmetrical. (6) Radiographs did not enable a complete assessment of the hyoid apparatus in the goose we describe because of superimposition of the tissues. The entoglossal bone of a Chinese goose has a continuation as cartilage reaching as far as half of the apex length (11) and the length of the urohyal bone is as long as the basibranchial bone. (2) This complicated the interpretation of the radiographs.

Therefore, computed tomography was the most useful imaging technique in this case to assess integrity of the hyoid apparatus. Muscular injury of the branchiomandibularis muscle could have resulted in a deficit of the protraction of the tongue. Alternatively a dysfunction of either the cricohyoideus or the stylohyoideus muscles could have impaired tongue retraction. (1,4,5) An isolated dysfunction of other muscles of the hyoid apparatus was considered less likely due to their more secondary role in the rostro-caudal movement of the hyoid apparatus. However, a multifocal muscular disease could not be ruled out initially. A neurologic or neuromuscular dysfunction was not investigated further due to the ability of the goose to move its tongue normally when a bandage was placed on the caudal intermandibular region. A neurologic dysfunction was suspected in other cases of sublingual entrapment (5,10) but has not been demonstrated to the authors' knowledge.

Treatment of early stage intermandibular distension consists of manually removing the sublingual debris and does not require anesthesia. (9) Preventing grazing for at least 7 to 10 days has also been recommended anecdotally. (9) Some birds may need to be caught and examined every 2 weeks to dislodge entrapped food material in periods of dry weather, due to poor grass quality. (10) Chronic entrapment has been corrected previously by extraoral surgical resection of the stretched, redundant sublingual intermandibular skin (10) or by intraoral resection of the redundant frenulum tissue with a C[O.sub.2] laser associated with a nonabsorbable suture through the mandibular symphysis pulling the tongue rostrally. (5) In one case report, the frenulum was incised rostrocaudally and a monofilament 2-0 nylon suture was placed through the rostral muscular insertion on the ventral surface of the basibranchial bone, then through a hole drilled into the caudal part of the mandibular symphysis. (5) The suture was tightened until the tongue was pulled forward in anatomical position, and the frenulum was closed with absorbable suture. (5) In the case described here, a less-invasive extraoral technique was elected. Placement of an esophagostomy feeding tube after intermandibular skin resection has been proposed to decrease downward pressure on the suture line during feeding. (5) In the goose described here, gavage was not necessary because the bird was eating on its own immediately after surgery. An external bandage was placed for 24 hours after surgery to counteract possible pressure on intermandibular tissue associated with potential vocalization and distress during recovery.

Complications after surgical submandibular skin resection have been described. In an Australian shelduck, the abnormal remodeled shape of the entrapped tongue prevented beak closure after extraoral resection of the stretched sublingual intermandibular skin. (10) The tongue was bent dorsally, forming a hook-like tip that was successfully treated by partial tongue amputation. (10) In the current case, the tongue apex returned to its normal shape and was appropriate for feeding immediately after surgery. The abnormal shape of the rostral end of the tongue on presentation was likely caused by compression toward the mandibular symphysis, since this resolved spontaneously after the procedure. It is unknown if this outcome is due to species-specific differences or if the complicated case in the Australian shelduck was caused by contracture and fibrosis of the tongue secondary to lesion chronicity.

The anesthetic protocol with propofol was chosen to avoid mask induction, which can induce apnea and bradycardia in waterfowl. (14) Rather than being a classic diving response, this condition is a stress response mediated by the trigeminal nerve receptors in the beak and nares. (14) Premedication with midazolam has been shown to decrease this stress response. (14) Inspiratory dyspnea observed during recovery from the second anesthesia could be attributed to accumulation of mucoid secretions in the airways. The use of a tracheal tube humidifier has been reported to decrease mucus plug formation, (15) although this did not prevent mucus accumulation in this case. Premedication with glycopyrrolate may have contributed to this anesthetic complication. Anticholinergic agents reduce pharyngeal and tracheal secretions but also increase their viscosity, which can increase the risk of airway obstruction. (16) Consequently, these agents are recommended only in cases of bradycardia in waterfowl. (16)

In this report we describe the successful surgical management of chronic submandibular lingual entrapment by extraoral resection of the distended cutaneous tissue in the submandibular space. Although possible causes of the condition presented in this goose are mentioned, the cause was not ascertained.

Acknowledgments: The authors thank Delphine Grosset for her contribution to Figure 3's design.

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Claire Grosset, DVM, IPSAV Zoological Medicine, David Sanchez-Migallon Guzman, LV, MS, Dipl ECZM (Avian), Dipl ACZM, Andrew Waymire, DVM, Sarah M. Puchalski, VRSS, DVM, Dipl ACVR, and Michele A. Steffey, DVM, Dipl ACVS

From the Companion Avian and Pet Exotic Service, William R. Pritchard Veterinary Medical Teaching Hospital (Grosset), the Department of Medicine and Epidemiology (Guzman), and the Department of Surgical and Radiological Sciences (Puchalski, Steffey), School of Veterinary Medicine, University of California at Davis, Davis, CA 95616, USA, and the Banfield Pet Hospital, 3220 W Shaw Ave, Fresno, CA 93711, USA (Waymire).
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Author:Grosset, Claire; Guzman, David Sanchez-Migallon; Waymire, Andrew; Puchalski, Sarah M.; Steffey, Mich
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Dec 1, 2013
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