Major Glossectomy in Dogs: A Case Series and Proposed Classification System
Major resections of the tongue have not been commonly performed in animals because of concerns about the unfavorable postoperative effects of diminished lingual function. Five dogs were retrospectively reviewed to determine prehensile function and quality of life after glossectomies. Examinations were performed 1 week to 8 years after glossectomy, and owner interviews were conducted 10 months to 8 years after the surgery. All five dogs had acceptable and functional outcomes. Based on these five cases, glossectomy was well tolerated by dogs and may be a viable treatment option for aggressive tongue tumors and other conditions that render the tongue unsalvageable.
Introduction
Glossectomy, or amputation of any portion of the tongue, has rarely been reported in the veterinary literature. Most published reports have described partial glossectomies.1–3 A classification system for glossectomies has not been established in the veterinary literature. The classification system used in humans is divided into partial, subtotal, near total, and total glossectomies.4 A partial glossectomy is defined as excision or amputation of any portion or all of the oral (free) tongue rostral to the frenulum. A subtotal glossectomy involves the entire free tongue and a portion of the genioglossus, the geniohyoid muscles, or both, caudal to the frenulum. A near total glossectomy refers to resection of ≥75% of the entire tongue. Amputation or excision of the entire tongue is defined as a total glossectomy. In people, partial glossectomies are considered minor glossectomies, while subtotal, near total, and total glossectomies are categorized as major glossectomies. In the study reported here, the authors have applied this classification system to five cases of major glossectomies in dogs. The purpose of this retrospective study is to describe the first report of near total and total glossectomies in dogs and to review the outcomes of those cases.
Case Reports
Case No. 1
A 3-year-old, spayed female miniature schnauzer was presented with a 3-day history of dysphagia and inappetence. Oral examination revealed a 3-cm, soft, mobile mass located on the ventral tongue surrounding the frenulum. The dog had been evaluated 6 months earlier for a similar soft-tissue mass in the same location, which responded to amoxicillina (18.5 mg/kg per os [PO] q 12 hours). The histopathological diagnosis at that time was pyogranulomatous glossitis.
A complete blood count (CBC) and serum biochemical analysis were performed, and the only abnormal results were a leukocytosis (24.5 × 103/μL; reference range, 6.0 to 17.0 × 103/μL) and mature neutrophilia (21.3 × 103/μL; reference range, 3.0 to 11.5 × 103/μL). An enzyme-linked immunoassay (ELISA) occult heartworm test was negative. Skull radiographs revealed a soft-tissue swelling ventral to the mandible and hyoid apparatus. There were no bony abnormalities noted. Fine-needle aspirates were performed of the mass, and the cytological interpretation was chronic pyogranulomatous inflammation.
The dog was subsequently admitted to the hospital for surgical exploration and excision of the pyogranulomatous mass. At surgery, a ventral midline dermal incision was made in the intermandibular space. En bloc excisions of the mass and any associated fistulous tracts were performed along with excision of portions of the mylohyoideus, geniohyoideus, hyoglossus, and genioglossus muscles. The frenulum was reattached to the ventral oral mucosa. The surgical site was packed with saline-moistened, sterile gauze sponges, and a positional bandage was placed. The positional bandage or tie-over dressing utilized umbilical tape laced through suture loops surrounding the wound to secure the bandage material. The surgical site was left to heal by second intention. Both a tracheostomy tube and a percutaneous endoscopic gastrotomy (PEG) tube were placed. The histopathological diagnosis was glossitis and granulation tissue. Tissue cultures grew Corynebacterium spp. susceptible to amoxicillin,a which was administered for 14 days (16 mg/kg PO q 12 hours).
Resection of the intermandibular tissue resulted in vascular compromise to the oral tongue. By 4 days after surgery, there was a clear line of demarcation between viable and nonviable glossal tissue. On the fifth day, the necrotic portion of the tongue, compromising the rostral 60%, was manually removed without surgical intervention. With 40% of the tongue remaining, this was classified as a subtotal glossectomy. The tracheostomy tube was also removed at this time. The dog was discharged from the hospital 1 week after surgery. Delayed primary closure of the ventral intermandibular incision was performed 2 weeks after the initial surgery, at which time it was noted that the dog had developed a soft-tissue, fluid-filled swelling at the caudal lateral aspect of the tongue. Cytological evaluation using a modified Giemsa-Wright stain indicated this swelling was a salivary mucocele.
Three weeks after the initial surgery, this dog was eating and drinking without assistance. At that time, the PEG tube was removed. Follow-up evaluation of this animal occurred regularly over an 8-year period. The owners reported that the dog ate dry dog food by throwing her head back to assist in swallowing the kibble. The dog continued to have a difficult time with soft or canned food, as it tended to lodge in her intermandibular space. The dog drank water by sucking it directly out of the bowl or by filling her mouth and elevating her muzzle.
Case No. 2
A 10-year-old, intact male wolf hybrid was referred for evaluation of a recurring squamous cell carcinoma (SCC) of the tongue. The mass was initially located in the middle left third of the tongue and involved the frenulum. It was excised 6 months earlier via partial glossectomy. Submandibular lymphadenectomy was also performed for staging, and thoracic radiographs revealed no evidence of pulmonary metastasis at that time. The histopathological diagnosis was lingual SCC with apparently clean surgical margins and submandibular lymph node metastasis. The dog was treated with mitoxantroneb (5 mg/m2 intravenously [IV] q 30 days) and cyclophosphamidec (150 mg/m2 IV q 30 days) for 3 months following the initial surgery.
At presentation, there was a 1 cm-diameter mass at the edge of the previous incision and a 3 mm-diameter mass immediately rostral to it, both on the left side of the tongue. Results of a CBC and serum biochemical analysis were within reference ranges. Thoracic radiographs revealed no evidence of pulmonary metastasis. The masses were excised using an elliptical incision that included margins 1-cm rostrally and caudally, and 0.5-cm medial the masses. The medial extent of the incision was the lingual midline. The left lingual artery was ligated with 5-0 polydioxanone suture.d The squamous epithelium was apposed using 4-0 polydioxanone in a simple interrupted pattern. Approximately 20% of the tongue was excised. The histopathological diagnosis was SCC, with clean surgical margins. At the time of discharge, the rostral third of the tongue was slightly gray in color and cool to the touch.
When the dog was returned to the hospital 5 days after surgery, the rostral third of the tongue was necrotic. Results of a CBC and serum biochemical analysis were within reference ranges. The dog was anesthetized, and the rostral third of the tongue was excised with a scalpel blade. The lingual epithelium was closed with 4-0 polydioxanone in a simple continuous pattern. After this second surgery, only 50% of the tongue remained, classifying it as a subtotal glossectomy. Within 24 hours of the second surgery, the dog was lapping foode and water without difficulty. He was discharged from the hospital 2 days after surgery.
Ten months after the last surgery, there was no evidence of local recurrence of the SCC and no evidence of pulmonary metastasis on thoracic radiographs. The owners reported that the dog was having no difficulty eating his normal diet or drinking water. Subsequently, the dog was lost to follow-up.
Case No. 3
A 5-year-old, castrated male Labrador retriever was referred for evaluation of a recurring tongue mass. The original histopathological diagnosis was granulomatous inflammation with no evidence of neoplasia. The mass was excised and had recurred four times in the previous 3 years. The last excision was performed 3 months earlier, at which time 1-cm margins of apparently normal tissue were taken. The histopathological diagnosis at the last excision was neurofibrosarcoma with no evidence of neoplastic cells at the surgical margins.
At presentation, there was a 1 cm-diameter mass on the right dorsal tongue approximately 10 cm rostral to the epiglottis [Figure 1]. Results of a CBC and serum biochemical analysis were within reference ranges, and thoracic radiographs showed no evidence of metastatic disease. The submandibular lymph nodes were evaluated via ultrasound and appeared normal. Cytology of these lymph nodes following fine-needle aspiration revealed no evidence of metastasis. Magnetic resonance imaging (MRI) was performed to determine the extent of the tongue lesion. The MRI showed the mass to be predominately right-sided with extension across the midline. The mass extended caudally approximately 2 cm beyond the grossly visible tumor. There was nonuniform contrast enhancement of the mass.
At surgery, a transverse dorsal incision was made 4 cm from the most caudal aspect of the tongue. A similar incision was made through the epithelium on the ventral surface of the tongue, conserving as much mucosa as possible. The lingual vessels were dissected and ligated. The muscular tissue was excised using electrosurgery. The ventral mucosal edges were apposed to the dorsal tongue epithelium using 3-0 polyglactin 910 suturef in a simple interrupted pattern [Figure 2]. In total, approximately 80% of the tongue was excised, classifying the excision as a near total glossectomy. A PEG tube was placed at the time of surgery. Histopathological diagnosis was neurofibrosarcoma with no evidence of neoplastic cells at the surgical margins.
The dog was eating chilled canned-food meatballs on the second day after surgery. Each meatball was manually dropped into the back of his mouth while holding the muzzle in an elevated position. One week after surgery, the dog was discharged from the hospital. At that time, he was eating orally, with assistance, as well as receiving supplementation via the PEG tube. Eight days after surgery, the dog began sucking water from a bucket. By 3 weeks after surgery, the dog was eating without assistance and the PEG tube was removed.
One year after surgery, the dog developed lameness in his right thoracic limb. Radiography performed by the referring veterinarian showed a lytic bone lesion in the middiaphysis of the ulna. The lesion was suspected to be neoplasia, and the owners elected euthanasia. A biopsy sample was not obtained. Thoracic radiographs at that time were normal, with no evidence of metastatic disease.
The owners of this dog were interviewed by telephone concerning the dog’s postoperative quality of life and lingual function. The dog had no difficulty eating or drinking unassisted within 3 weeks postoperatively. The dog also returned to normal activities 1 month after surgery, and such activities including daily Frisbee catching. He showed no signs of heat intolerance in the summer months.
Case No. 4
A 3-year-old, castrated male Labrador retriever was referred after his tongue became entrapped in a paper shredder. The paper shredder jammed, and in trying to free his tongue, the entire musculature was avulsed from its base. On presentation, the dog was in hypovolemic shock with pale mucous membranes and poor peripheral pulses. Packed cell volume (PCV) was 46% (reference range, 37% to 55%), and total serum protein was 4.0 mg/dL (reference range, 5.4 to 7.1 mg/dL). An IV catheter was placed, and lactated Ringer’s solution was administered at 90 mL/kg during the first hour of treatment.
Upon stabilization, the dog was anesthetized, and the lingual vasculature was identified and ligated. There were no remaining glosseus muscles in the oral cavity, classifying this traumatic avulsion as a total glossectomy [Figure 3]. The remaining ventral mucosa was apposed using 3-0 polyglactin 910 in simple interrupted and simple continuous suture patterns, and a PEG tube was placed. Recovery was uneventful, and the dog was discharged from the hospital 1 week after surgery, at which time he was still being fed through the PEG tube. Two weeks postoperatively, the dog was eating chilled canned-food meatballs orally with assistance and obtaining his daily water requirements orally via a syringe. The PEG tube was removed 3 weeks after the trauma. At that time, oral examination revealed minor incisional dehiscence with granulation tissue [Figure 4]. By 4 weeks after surgery, he was eating dry dog food soaked in water and had learned to suck water from a bucket.
The dog was reevaluated 10 weeks after surgery for hyperptyalism. On oral examination, the ventral mucosa was fully healed, and the owner reported that the dog was eating and drinking without difficulty. The dog was discharged from the hospital with 0.5 mg glycopyrrolateg (0.014 mg/kg PO q 6 to 8 hours); however, there was no response to therapy. The hyperptyalism was presumed to be secondary to an inability to contain the saliva within the oral cavity. It was not believed to result from hypersalivation. Six weeks later, this dog had bilateral sublingual and mandibular sialadenectomy performed in an attempt to control the hyperptyalism. The owner reported by telephone interview 15 months after the traumatic glossectomy that the dog was eating and drinking without assistance and had returned to normal activities, such as Frisbee catching and tug-of-war. The dog continued to have hyperptyalism, although the sialadenectomy had greatly improved the condition.
Case No. 5
A 9-year-old, castrated male border collie was referred after entrapping his tongue in a paper shredder. The tongue was completely avulsed at the base, resulting in a traumatic total glossectomy [Figure 5]. The dog was presented in hypovolemic shock with pale mucous membranes, poor peripheral pulses, and tachycardia. He also had hematemesis. The PCV was 29%, and serum total protein was 4.2 mg/dL. An electrocardiogram showed second-degree atrioventricular heart block, which resolved with administration of subcutaneous atropineh (0.04 mg/kg). An IV catheter was placed, and lactated Ringer’s solution was administered at a rate of 90 mL/kg during the first hour of treatment.
Following stabilization, the dog was anesthetized and the lingual vessels were identified and ligated. The remaining ventral mucosa was apposed with a simple continuous suture pattern using 4-0 polyglactin 910, and a PEG tube was placed. Four days after the trauma, the dog was discharged from the hospital. During hospitalization, all nutritional needs were provided through the PEG tube. Once at home, the dog started swallowing chilled canned-food meatballs that the owner would throw to him. The dog had previously been trained for this activity. One week after surgery, the dog was able to pick up canned-food meatballs and would throw his head back to aid in swallowing. Oral fluid requirements were delivered through the PEG tube until 2 weeks after surgery, at which time water was administered via a syringe. The PEG tube was removed 17 days after surgery. Within 1 month, the dog was eating dry dog food placed in water. This dog never learned to suck water into his mouth like the other cases; however, his water requirements were supplied with the food. The dog returned to agility training 1 month after surgery. One year after the trauma, the owners reported that the dog had no evidence of heat intolerance.
Discussion
Functions of the tongue in the dog include food apprehension and swallowing, taste, heat dissipation through panting, vocalization, and grooming. The swallowing mechanism is divided into three phases: oral, pharyngeal, and esophageal.5 The tongue plays a vital role in the oral phase and initiates the pharyngeal phase. After lapping liquid, the canine tongue forms a tubular space with the palate. The dorsum of the tongue then compresses against the palate, forcing the liquid into the oropharynx.6 The tongue then bulges back into the oropharynx, propelling the fluid into the laryngeal pharynx.6 For solid foods, the tongue receives the food and carries it to the caudal mouth for mastication. Once the food has been adequately chewed, the tongue compresses against the palate, forming a food bolus that is then forced into the oropharynx.6
Glossectomy, or amputation of any portion of the tongue, has been used as a surgical treatment for neoplasia of the tongue in humans. Reports of glossectomies in animals are sporadic, with most reports detailing partial or subtotal glossectomy.1026 Only two reports of major glossectomies exist in the veterinary literature. One report described a jaguar that lost all but a small portion of the genioglossus muscle in a cage accident, and one report described a domestic cat that lost 75% of the tongue in a cat fight.78 Both of these animals had an acceptable outcome; however, the domestic cat was euthanized for lack of self-grooming. No reports of near total or total glossectomies in dogs have been published.
To date, a classification system for glossectomies has not been established in animals. The system used by the authors of this report paralleled that used in humans.4 Use of a classification system may provide better standardization for reporting and comparing animal cases.
The indications to perform a glossectomy include neoplasia; glossitis; traumatic injuries such as lacerations; ulcerations and burns from ingestion of caustic substances; chronic linear foreign bodies; and electrical injuries.26 Tumors of the tongue account for 4% of all oral pharyngeal cancers in dogs.1 Numerous isolated case reports of lingual tumors exist in the veterinary literature.1–3910 However, to date, only one retrospective review of canine tongue tumors has been published.2 The most prevalent tumors in that report, in order of incidence, were the SCC, granular cell myoblastoma, malignant melanoma, and mast cell tumor. Other tumor types reported in the canine tongue include hemangiosarcoma, fibrosarcoma, neurofibrosarcoma, leiomyosarcoma, rhabdomyosarcoma, lipoma, hemangiopericytoma, hemangioma, myxoma, and myeloma.2910 Case no. 3 in this report was diagnosed with a neurofibrosarcoma. In the literature, three individual cases of lingual neurofibrosarcomas have been reported in humans, and one case has been reported in the dog.911
The location of lingual tumors significantly impacts the prognosis in people. Anterior lesions of the tongue in humans are detected earlier (thereby resulting in a better prognosis) than posterior lesions, which generally are found in more advanced stages.12 Beck, et al. reported that 54% of canine tongue tumors were located midline or were bilaterally symmetrical.2 The lingual tumors in Beck’s study were evenly distributed among rostral, middle, and caudal locations. More tumors were reported on the dorsal surface of the tongue than the ventral surface or were diffuse throughout the parenchyma. The location of the tumor within the tongue and the stage of disease did not affect prognosis in those canine cases.2
An association between lingual tumors and other primary tumors has been reported in humans, with 11% to 29% of affected people having a second primary tumor.1213 Sixteen percent of dogs with tongue tumors have had a second primary tumor.2 The reason for such an association has not been determined. In the study reported here, case no. 3 developed a lytic middiaphyseal bone lesion that was suspected to be neoplastic. Since a biopsy or necropsy was not performed, the origin of the lesion was undetermined.
The value of major glossectomies in humans is controversial.141619–2123–25 When performing a partial or subtotal glossectomy in a person, it is recommended that a minimum of 1 cm of normal tissue be excised around the mass.14 Despite attempts at wide excision, 32% to 36% of tongue resections for SCC in people that had clean histopathological margins, developed tumor recurrence at the primary site.1415 In both human and veterinary medicine, radiotherapy and chemotherapy are the most common primary and adjunctive treatments used for tongue tumors.3121321 However, SCC, the most prevalent lingual tumor in both humans and dogs, tends to be poorly responsive to both radiation and chemotherapy.312–1425
In people, the 5-year survival rates for lingual SCC are similar regardless of the therapy chosen.16–21 However, most reports have not compared survival rates based on the modified World Health Organization Tumor Node Metastasis (TNM) classification system.22 In people, a major glossectomy at least offers substantial palliation for the pain associated with lingual tumors.1621 In one report of 80 total glossectomies in humans, most patients did not require postoperative analgesics because of the marked pain relief associated with surgery.23 The candidates for radical resections are generally functionally restricted from the size of the tumor and debilitating pain. Numerous publications have addressed the quality of life in people who have undergone total glossectomies.141618212425 Although a majority of patients did develop comprehensible speech and the ability to eat unassisted, even those who did not still rated their quality of life as good to excellent.21
There are several pre- and postoperative factors that must be considered when performing a glossectomy. Profuse bleeding during surgery of the tongue is common because of the rich vascularity of the organ. Care should be taken to control hemorrhage. Use of electrosurgery, lasers, and/or temporal occlusion of the carotid arteries through a ventral neck incision may be considered to help with hemostasis.26 Development of aspiration pneumonia is one of the most prevalent postoperative complications in humans, with a 10% to 37% occurrence rate.2025 None of the five dogs presented in the study reported here developed clinical aspiration pneumonia. Because of the degree of vascularity within the tongue, healing is rapid and infections are uncommon. Other defense mechanisms of the oral cavity include the tough epithelium of the tongue, the antibacterial properties of saliva, and an aggregation of immunoreactive cells in the supporting connective tissues.27 In most animals, antimicrobials may not be required postoperatively.
For the major glossectomies performed in this study, assistance with feeding was needed postoperatively. Feeding tubes placed by esophagostomy or gastrostomy were also helpful and were necessary in some cases for several weeks to months. For the three dogs in this case series that had near total and total glossectomies, the owners had the best success training the dogs to eat chilled meatballs formed from canned dog food. Once the dogs were able to pick up and swallow a meatball on their own, they were encouraged to drink by placing the meatball in a bowl of water. Owners should be thoroughly educated on the postoperative care before a major glossectomy is performed. The owners of all five dogs in this study indicated that the first postoperative month required much time and effort on their part. All of the owners reported, however, that the experience was probably more traumatic for them than for their pet.
The only significant complication seen in these five dogs was a single case of hyperptyalism. Hyperptyalism is an uncommon complication in human glossectomy patients. In humans, oral glycopyrrolate given three to four times daily markedly decreases drooling.2829 Glycopyrrolate is a quaternary ammonium compound that penetrates the blood-brain barrier poorly; therefore, it lacks the central nervous system side effects associated with atropine. In humans, glycopyrrolate has a slow and erratic absorption from the gastrointestinal system, but it is a long-lasting antisialagogue even when plasma levels are low.29 The gastrointestinal absorption of glycopyrrolate in dogs is unknown, but case no. 4 in this study had a poor response to oral glycopyrrolate. Other reported treatment options for hyperptyalism include sialadenectomy, salivary duct ligation, or duct diversion. Case no. 4 underwent sialadenectomy of the sublingual and mandibular salivary glands. This surgical therapy was palliative and not curative.
To the authors’ knowledge, reports of near total and total glossectomies in dogs have not been published. Carpenter, et al. reviewed 10 canine cases in which 40% to 60% of the tongue was excised. Although Carpenter, et al. documented acceptable outcomes, they suggested that more aggressive excision of the tongue in dogs may cause unacceptable morbidity.3 In contrast, all five dogs in the study reported here had functional outcomes and adapted to their disability. All owners reported that each of their dogs have had an excellent quality of life after glossectomy, and they had no regrets about their decision to pursue treatment. The only negative issue expressed by four owners was a dislike of the PEG tube. None of these dogs had complications from their feeding tubes. Based on the results of this study, major glossectomy was well tolerated by the dogs.
Aggressive surgical excision of the tongue may result in better survival rates in dogs with lingual cancer. Although relatively uncommon, most lingual tumors are not diagnosed in dogs until they are fairly advanced and therefore are associated with a poor prognosis. Owners often elect euthanasia of these dogs because of an anticipated poor quality of life. Because the number of cases in this study was low, conclusions could not be made regarding the prognosis for tongue tumors treated with surgery versus radiation or chemotherapy; however, glossectomy may be a viable treatment option.
Conclusion
This report showed that a surgical major glossectomy was well tolerated by the five dogs in the study. Based on these results, glossectomy may be considered as a treatment for aggressive tongue tumors and other conditions that render the tongue unsalvageable. In this study, a glossectomy classification system was used that paralleled the one developed in people. This system may be helpful in the standardization and reporting of future cases and in determining prognosis after treatment.
Amoxi tabs; Smith Kline Beecham Pharmaceuticals, Philadelphia, PA
Novantrone; Immunex Co., Seattle, WA
Lyophilized Cytoxan; Bristol-Myers Squibb Co., Princeton, NJ
PDS II; Ethicon, Somerville, NJ
A/D diet; Hill’s Pet Nutrition, Inc., Topeka, KS
Vicryl; Ethicon, Somerville, NJ
Robinul; A. H. Robbins Co., Richmond, VA
Atropine SA; The Butler Co., Columbus, OH
Citation: Journal of the American Animal Hospital Association 40, 4; 10.5326/0400331
Citation: Journal of the American Animal Hospital Association 40, 4; 10.5326/0400331
Citation: Journal of the American Animal Hospital Association 40, 4; 10.5326/0400331
Citation: Journal of the American Animal Hospital Association 40, 4; 10.5326/0400331
Citation: Journal of the American Animal Hospital Association 40, 4; 10.5326/0400331
Preoperative view of a 1 cm-diameter neurofibrosarcoma on the tongue of a 5-year-old, castrated male Labrador retriever (case no. 3).
Preoperative oral view of a 3-year-old, castrated male Labrador retriever (case no. 4) after traumatic total glossectomy.
The tongue of a 9-year-old, castrated male border collie (case no. 5) after traumatic glossectomy secondary to lingual entrapment in a paper shredder.
