Editorial Type: Oncology
 | 
Online Publication Date: 01 Nov 2008

Retrospective Evaluation of Lingual Tumors in 42 Dogs: 1999–2005

DVM,
DVM, Diplomate ACVS,
DVM, MVSc, Diplomate ACVP, and
DVM, PhD, Diplomate ACVIM (Oncology)
Article Category: Other
Page Range: 308 – 319
DOI: 10.5326/0440308
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In this retrospective study of 42 cases of lingual tumors in dogs, 27 (64%) were malignant, and 15 (36%) were benign. Median survival time for dogs with benign tumors was >1607 days, compared to 286 days for malignant tumors. Prognostic factors significantly associated with increased survival included complete histological margins (P=0.036), smaller tumor size (P=0.003), and benign tumor type (P=0.011). Smaller tumors were more likely to be completely resected (P=0.008) and were less likely to recur (P=0.001). Partial or subtotal glossectomies were performed in 13 cases. Short-term morbidity associated with glossectomy included ptyalism and dehiscence. Long-term morbidity included minor changes in eating and drinking habits.

Introduction

Lingual tumors are an important subset of oral neoplasms to define because of the specific implications involved with their treatment, the diversity in tumor type, and their varying prognoses.1,2 In previous studies, histological diagnoses of lingual neoplasms in dogs included but were not limited to squamous cell carcinoma, melanoma, squamous papilloma, plasmacytoma, granular cell tumor, and mast cell tumor.1,2 Limited data are available regarding outcomes for these tumors following treatment. Little documentation is present in the literature discussing function following partial and total glossectomies in dogs. In a recent study, five of five dogs receiving subtotal to total glossectomies had successful outcomes, although hypersalivation was noted in one case, and most dogs had long-term changes in eating and drinking habits.3

In humans, total glossectomy is controversial because of perceptions of unacceptable morbidity associated with loss of intelligible speech and independent oral alimentation. However, total glossectomy resulted in >90% success rate for satisfactory deglutition following surgery in three independent studies.46 Intelligible speech was preserved in 57% to 100% of cases of total glossectomy with laryngeal preservation.46

This study was conducted to determine distribution of tumor types, identify prognostic indicators, evaluate treatment options, document complications, and measure outcomes associated with the treatment of lingual tumors in dogs.

Materials and Methods

The histopathology database of the Animal Medical Center was searched for canine lingual tumors submitted over a 7-year period, from January 1999 to October 2005. Diagnoses were obtained from surgical biopsy or necropsy samples, and all slides were reviewed by one pathologist (Monette). All cases included in the study had a complete medical record and histological slides available for review. Data collected from the medical record included signalment, body weight, clinical signs associated with the tumor, clinical stage, size and location of the tumor, histopathological diagnosis, extent of glossectomy if surgery was performed, surgical margin width, whether a surgical lasera was used, and complications associated with treatment. Additional information collected included placement of feeding tubes, duration of hospital stay, achievement of complete histological margins, use of chemotherapy and radiation as adjunctive therapies, time to recurrence, and date of death if applicable.

Radiation therapy when utilized was delivered via a cobalt 60 teletherapy unit.b Postoperative complications occurring <2 weeks from the time of surgery were considered to be short term. Long-term complications occurred or persisted >2 weeks postoperatively. Recurrence was defined as gross local recurrence noted on physical examination by a veterinarian or at necropsy; regional or distant lymph node metastases confirmed with cytology or histopathology; or distant metastases seen on radiographs, ultrasound, computed tomography, magnetic resonance imaging, or at necropsy. Referring veterinarians and owners were contacted for additional information to complete the medical record.

Tumors were grouped into categories based on tumor area for analysis. Categories were as follows: small tumors were <1 cm2; intermediate tumors were 1 to 4 cm2; large tumors were >4 cm2. Tumors that could not be grouped into size categories because of a diffuse distribution of disease or inadequate documentation in the medical record were excluded from tumor area analysis.

Surgical cases were categorized by the amount of tongue removed surgically, patterned on the scheme developed by Dvorak et al.3 Categories in this study included incisional biopsy, marginal excision, partial glossectomy, subtotal glossectomy, near-total glossectomy, and total glossectomy. Cases with marginal excision had a minimal amount of normal tongue resected along with the mass. Partial glossectomy is defined as full-thickness resection of any portion of the free tongue rostral to the frenulum. Subtotal glossectomy involves resection of the free tongue and a portion of tongue caudal to the frenulum. Resection of =75% of the tongue constitutes a near-total glossectomy. A total glossectomy is excision of the entire tongue.3

Animals with incisional biopsies only were not considered to have had curative intent surgeries and were therefore excluded from all survival and disease-free interval (DFI) data. Mass location on the tongue was ascertained from the records and recorded as dorsal, ventral, or full thickness; left, right, or central; and root, apex, or body.

Statistical Analysis

For statistical analyses, median survival times and DFI were calculated by use of Kaplan-Meier life table analysis. Cases without curative intent surgeries were excluded from survival and DFI data. Curative intent was defined as a marginal or wide excision for benign tumors and a wide excision for malignant tumors. Median survival time was defined as the time from the original diagnosis until death. This starting point for survival time was selected in order to determine survival following initial diagnosis rather than survival time following treatment. Dogs alive at the end of the study or dogs that died of a disease process other than the lingual tumor were censored from survival analysis. Disease-free interval was defined as time from the definitive surgical procedure until recurrence. Dogs without documented recurrence of the tumor were censored from DFI analysis.

Variables studied for association with survival and DFI included breed, sex, tumor size, location on tongue, category of tumor (benign or malignant), histopathological diagnosis, chemotherapy administered (yes or no), radiation therapy administered (yes or no), extent of glossectomy, use of surgical laser, postoperative ptyalism, other surgical complications, complete histological margins (yes or no), and recurrence. Logrank testing was used for delineation of significance between categorical subpopulations. Values of P≤0.05 were considered significant. The continuous variables of age and weight were evaluated for association with categorical variables using analysis of variance (ANOVA) testing. Univariate Cox proportional hazard regression model analyses were performed to evaluate whether variables were associated with survival time and as a screen for multivariate analyses. Variables with values of P≤0.2 in the univariate analysis were included in the stepwise multivariate model. Categorical variables were evaluated for associations with chi-square (χ2) analysis and with the Fisher exact test when there were five or less in a cell on χ2 testing. Computer software was used to perform all statistical analyses.c

Results

Forty-two cases of lingual neoplasia were identified that met the criteria for inclusion in this study. Twenty-eight (67%) of 42 dogs with lingual tumors were male, and 14 (33%) of 42 were female. Four of the males were intact, and one of the females was of unknown neuter status. All other dogs were neutered. Median age at diagnosis was 10.5 years (range 1.8 to 13.9 years). Mixed-breed dogs (n=11) were most commonly affected. The most common breeds affected were the golden retriever (n=4), Labrador retriever (n=4), and chow chow (n=3). Breeds with two dogs represented included German shepherd dog, miniature poodle, and standard poodle. Breeds with one dog represented included Boston terrier, Jack Russell terrier, Alaskan malamute, Maltese, Old English sheepdog, Pembroke Welsh corgi, Pomeranian, Rhodesian ridgeback, Samoyed, Scottish terrier, Shiba Inu, shih tzu, West Highland white terrier, and Yorkshire terrier. Median body weight of affected dogs was 21.8 kg (range 3.6 to 48.2 kg). Statistical analysis revealed no significant findings relating to sex, neuter status, breed, or body weight.

Lingual tumors (n=15) in this study were most often incidental findings. In another 12 dogs, the owner noted a mass on the tongue, but no clinical signs were attributed to the mass. Clinical signs referable to the tumor were halitosis (n=5), hypersalivation (n=4), oral hemorrhage (n=3), difficulty with prehension or swallowing (n=2), decreased appetite (n=2), and weight loss (n=1).

Dorsoventral tumor location could be ascertained from the records in 39 of 42 cases; lateral location was determined in 23 of 42 cases; and rostrocaudal location was determined in 32 of 42 cases. No significant associations were found, but several trends were noted. For melanomas, eight of 11 were dorsally located, and eight of 11 were located caudally in the body or root of the tongue. No melanomas were located at the apex of the tongue. All five plasmacytomas were located dorsally. Three of four granular cell tumors were found on the ventral aspect of the tongue. No trends were noted for squamous cell carcinoma or papilloma. Other tumor types had three or less individuals represented.

Twenty-one tumors were grouped in the small size category (<1 cm2), eight were in the intermediate category (1 to 4 cm2), and eight were in the large category (>4 cm2). Five tumors could not be evaluated by size. Four of these could not be categorized due to unclear information regarding size in the medical record. The remaining tumor was diffuse in distribution. Using univariate analysis, dogs with larger tumors were 12.8 to 18.5 times more likely to die of their diseases (P=0.003) [Table 1] and 9.62 times more likely to have local or distant recurrence than dogs with smaller tumors (P=0.002; 95% confidence interval [CI] 2.70 to 34.5). None of these variables were identified for prognostic importance on stepwise multivariate analysis of DFI or survival. A significant inverse association was found between increased tumor size and the achievement of complete histological margins (P=0.008) [Table 2]. Increased tumor size had a significant positive association with increased recurrence (P=0.001). In addition, dogs with larger tumors were less likely to have curative intent surgeries (P <0.001).

In 19 cases, the initial diagnosis was obtained by incisional biopsy. Biopsy samples obtained from a marginal excision provided the diagnosis in another 18 cases. Aspiration cytology of the mass was performed prior to partial glossectomy in one case. In four cases, partial glossectomies were performed without previous tissue diagnosis. In all cases of marginal excision, a previous biopsy had not been performed. For eight of the 13 partial and subtotal glossectomies, incisional biopsy had been performed previously. The diagnoses for incisional and definitive biopsy samples were in agreement in all cases. In the one case with preoperative aspiration cytology, the initial diagnosis of plasma cell tumor did not agree with the histological diagnosis of fibrosarcoma. Prior to treatment, 26 and seven cases were staged with thoracic radiographs and abdominal ultrasound, respectively. Regional lymph node aspirates were obtained in 10 cases. No cases were found to have metastases at the time of initial treatment.

Of the 42 tumors, 27 (64%) were considered malignant, and 15 (36%) were benign. The most common malignant tumors were melanoma (n=11; 26%) and squamous cell carcinoma (n=7; 17%). Other malignant tumors noted were epitheliotropic T-cell lymphoma (n=3), adenocarcinoma (n=2), fibrosarcoma (n=1), liposarcoma (n=1), peripheral nerve sheath tumor (n=1), and hemangiosarcoma (n=1). Benign tumors diagnosed most commonly included plasmacytoma (n=5; 12%), granular cell tumor (n=4; 10%), and squamous papilloma (n=4; 10%). Other benign tumors included fibroma (n=1) and infiltrative lipoma (n=1) [Table 3].

Glossectomies were performed in 13 of 42 cases; this included 12 partial glossectomies and one subtotal glossectomy. In cases of glossectomy, surgical margins were noted in 11 of 13 cases. A range of 3 mm to 2 cm of grossly normal tissue was taken around the tumor in these cases. The median surgical margin width was 1 cm. In three of four cases with <1 cm surgical margins, complete histological margins were noted in just one case. Complete histological margins were obtained in all seven glossectomy cases with a surgical margin of ≥1 cm. Median follow-up time for glossectomy cases was 301 days (range 47 to 1075 days). Median hospital stay for partial and subtotal glossectomy cases was 2 days (range 1 to 6 days). An esophagostomy tube was placed at the time of surgery in one case of squamous cell carcinoma that received radiation therapy following surgery. The feeding tube was maintained throughout the course of radiation therapy and for 3 weeks afterward. Six of seven dogs with glossectomies (for which data were available) were eating well by mouth 3 days following surgery when hand fed; this included the dog with the esophagostomy tube.

Recommendations given to owners postoperatively were not standardized, but they commonly included hand-feeding meatballs for 2 weeks and offering water in a deep bowl. Six dogs with glossectomies had adequate information in the medical record for their appetites to be assessed at the 2-week recheck. All six of these dogs were eating without assistance at that time.

Curative intent surgeries were performed in 31 cases, including all glossectomies and marginal excisions of benign lingual tumors. Complete histological margins were obtained in 21 of 31 cases. Of these 21 cases, 11 were dogs with malignant neoplasia. Achievement of complete histological margins was significantly associated with increased survival (P=0.025) [Figure 1; Table 4] and DFI (P=0.008). Cases without complete histological margins were 3.58 times more likely to die of their disease than those with complete histological margins (P=0.036; 95% CI 1.09 to 11.7). These cases were also 3.07 times more likely to have local or distant recurrence (P=0.023; 95% CI 1.16 to 8.10). None of these variables were identified for prognostic importance on stepwise multivariate analysis of DFI or survival. Recurrence was more likely in those cases not having complete histological margins (P=0.025). Dogs with larger tumors were less likely to have complete histological margins at the time of initial resection (P=0.008). Interestingly, cases in which a surgical laser was used in the initial resection had an increased probability of complete histological margins (P=0.034). Not unexpectedly, dogs with curative intent surgeries had an increased likelihood of complete histological margins (P=0.004).

Adjunctive therapies included chemotherapy in two cases. One case with adenocarcinoma received an alternating course of three intravenous doses each of carboplatin at 300 mg/m2 and doxorubicin at 30 mg/m2. One case of epitheliotropic T-cell lymphoma received two oral doses of lomustine at 60 mg/m2 and one intramuscular dose of L-asparaginase at 400 IU/kg. Radiation therapy was used in five cases. Hypofractionated treatment protocols were used in two cases of melanoma—each of which received three treatments of 8 Gy given on days 0, 7, and 21. Three cases of squamous cell carcinoma were treated with definitive intent utilizing a standardized fractionation course to deliver a total dose of 48 Gy. Two of these cases received 3.2 Gy fractions for 15 treatments, and the other case received 3 Gy fractions for 16 treatments. The only significant finding regarding use of adjunctive therapies was the association of administration of chemotherapy with increased recurrence (P = 0.006).

Local tumor recurrence was noted in eight (26%) of 31 cases with curative intent surgeries. Seven were in cases of malignancy, including two cases each of melanoma and squamous cell carcinoma. Single cases of adenocarcinoma, epitheliotropic T-cell lymphoma, and hemangiosarcoma also had local recurrence. The benign mass with recurrence was a plasmacytoma that recurred twice, even with complete histological margins. Malignant tumors were more likely to recur (P=0.023). Dogs with curative intent surgeries were less likely to have tumor recurrence (P=0.022). Tumor recurrence was associated with decreased survival (P<0.001). Cases with tumor recurrence were 33.3 times more likely to die of their diseases than cases with no recurrence noted (P=0.001; 95% CI 4.26 to 250.0). An association of decreased survival with tumor recurrence was confirmed with multivariate analysis [Table 1]. Six (14%) of 42 total cases had confirmed distant metastases at the time of death. Five of these were cases of melanoma with pulmonary metastases. One case of adenocarcinoma also had pulmonary metastases. One case of epitheliotropic T-cell lymphoma was confirmed to be multicentric at the time of necropsy. Regional lymph node metastasis without distant metastasis was seen in one case of squamous cell carcinoma.

Of the glossectomy cases, seven (54%) of 13 had short-term complications. Short-term complications occurred within 2 weeks of surgery and included ptyalism (n=5; 38%) and dehiscence (n=3; 23%). All cases of dehiscence had good final outcomes, with one case requiring a revision surgery. In two of the three cases with dehiscence, a surgical laser was used for the original excision.a The laser was used for the definitive procedure in six cases. Long-term complications that occurred or persisted >2 weeks following surgery were documented in three (23%) of 13 cases. Two of these cases had long-term changes in eating and drinking habits. Owners reported these dogs persistently dropped food and dribbled water due to difficulties with prehension and swallowing. One of these cases had a subtotal glossectomy. In the third case, a dog with squamous cell carcinoma and concurrent megaesophagus developed aspiration pneumonia 204 days following glossectomy. This dog was euthanized shortly thereafter because of poor quality of life associated with the pneumonia and recurrence of the tumor.

At the conclusion of this study, 10 cases were alive, 13 were dead as a result of their lingual tumors, and 15 were dead of other causes. All cases dying from their diseases had malignant tumors. Four cases were lost to follow-up. Eight cases received a necropsy. Median time of follow-up for all cases was 245 days (range 0 to 1607 days). Overall median survival time was >1607 days [Figure 2; median not reached], and DFI was 284 days [Figure 3]. Dogs with benign lingual tumors treated with surgical excision had a significantly longer median survival time and DFI when compared to dogs with malignant tumors. Median survival time for dogs with benign tumors was >1607 days (median not reached), compared to the median of 286 days for dogs with malignant tumors (P=0.001) [Figure 4]. Disease-free interval for dogs with benign tumors was also significantly longer at >1607 days (median not reached), compared to 49 days for dogs with malignant tumors (P=0.001) [Figure 5]. Dogs with malignant tumors were 14.7 times more likely to die of their diseases than dogs with benign tumors (P=0.011; 95% CI 1.84 to 111.1) [Table 1] and 7.63 times more likely to have local or distant recurrence (P=0.007; 95% CI 1.74 to 33.3). None of these variables were identified for prognostic importance on stepwise multivariate analysis of DFI or survival. Cases with incisional biopsy alone were excluded from Kaplan-Meier analysis. Median survival time for those cases was 88 days (range 0 to 1142 days).

Kaplan-Meier median survival time for the 11 cases of melanoma was 222 days (range 47 to 840 days) [Table 5]. At the time of death, distant metastases were noted in five of 11 cases. For four of seven cases in which local control was attempted, complete histological margins were achieved. Two of these cases were lost to follow-up at 47 and 91 days. Of the remaining cases, one had tumor excision by the referring veterinarian, with clean but close histological margins. The owner elected no further treatment, and the tumor recurred at 168 days postoperatively; 286 days after surgery, euthanasia was performed. In the remaining case, a subtotal glossectomy was performed. No adjunctive therapy was performed, and the dog was euthanized 840 days postoperatively for reasons unrelated to the melanoma.

Median survival time for the seven cases of squamous cell carcinoma was 301 days (range 204 to 496 days) [Table 6]. Local control was achieved in two of four cases in which it was attempted. One of these cases received a marginal excision and was disease free at 345 days postoperatively; however, the dog was lost to follow-up. In the other case, a partial glossectomy was performed. The dog was disease free at last recheck (111 days) in the authors’ hospital and was euthanized at 496 days postoperatively for unknown reasons.

The median survival time for five dogs with plasmacytoma was >1607 days (median not reached). Complete histological margins were not achieved in one case initially, but no gross recurrence was seen at 165 days postoperatively. Another case had complete histological margins but had recurrence at 284 days and again at 581 days postoperatively. After the third excision, the dog was disease free for an additional 508 days before being euthanized for an unrelated reason.

In two of four cases of granular cell tumor, complete initial histological margins were not obtained. However, no local recurrence was noted, and median survival time was >1023 days (median not reached). Two of four cases of squamous papilloma also did not have complete histological margins, but no gross recurrence was seen. Median survival time was >1081 days (median not reached). Two dogs with lingual papilloma were <2 years of age at presentation, while the remaining two were >10 years of age.

Discussion

No significant sex, breed, age, or weight predilections for development of lingual tumors were identified in this study. In the study by Dennis, large-breed dogs (>15 kg) were 2.31 times more likely to be diagnosed with lingual tumors.2 In this study, a lingual tumor was typically an incidental finding, or a dog was presented because the owner noted a mass on the tongue; these circumstances were consistent with those in the study by Beck.1 Other common clinical signs between the two studies were halitosis, ptyalism, and oral hemorrhage.

Tumor location has been previously purported to affect prognosis, although this statement was not supported by published clinical data.7 Dogs with rostral tumor locations were given better prognoses because of the likelihood of earlier detection, more robust vascular and lymphatic channels in the caudal tongue, and the ease of obtaining wider surgical margins.7 No significant associations based on location were seen in this study, although melanoma seemed to have a predilection for the dorsal aspect of the body and root of the tongue.

Tumor size has not been previously reported to affect outcomes in dogs with lingual neoplasia. Categories for tumor area were created based on distribution of tumor sizes seen in this study. The oral tumor size categories used in this study allowed significant findings to be elucidated; such findings may not have been revealed if the broader World Health Organization categories were used.7 Smaller tumors were more likely to be completely excised and were less likely to recur. Also, dogs with smaller tumors were more likely to have curative intent surgeries; this may indicate a negative treatment bias toward larger lingual masses in this study.

The authors recommend incisional biopsy prior to further decision-making for lingual tumors because of the large variation in prognosis between benign and malignant tumors. In this study, marginal excision was commonly successful for control of benign tumors, but it cannot be recommended without previous incisional biopsy. Of seven glossectomy cases with surgical margins =1 cm in this study, complete histological margins were obtained in all seven. Dogs with complete histological margins had longer median survival times and DFIs in this study when compared to dogs that did not have complete margins obtained. Cases with attainment of complete histological margins were 3.58 times less likely to die of their diseases. Cases with recurrence in the present study were 33 times more likely to die of their diseases. Recurrence was more likely with increased tumor size and with malignant tumors. These results reinforce the need for early intervention and incisional biopsy prior to planning definitive therapy in these cases.

For known malignant tumors, appropriate further staging is indicated based on the aggressive behavior of common malignant tumors of the tongue. Specific recommendations cannot be made based on the results of this study, but thoracic radiography, abdominal ultrasound, and sentinel lymph node cytology may be indicated as for staging of other malignant tumors. An earlier report suggests that most lingual masses are malignant.1 In the current study, 64% of tumors were malignant and 36% were benign; these results were similar to those of another study.2 Based on the results of these recent studies, dogs with lingual tumors may have more favorable outcomes than previously suspected.

Use of a carbon dioxide laser in the current study was influenced by the individual surgeon’s preference. One advantage of the laser is control of hemorrhage in the vascular tissue of the tongue. Possible disadvantages of the laser include adverse effects on healing (suggested by the dehiscence of two cases in this study) and negative effects on the pathologist’s ability to interpret surgical margins. In a recent study comparing the use of a carbon dioxide laser to traditional sharp dissection for elevation of skin flaps, surgical wounds created by the laser had significantly less hemorrhage but also demonstrated less tensile strength when compared to wounds created by traditional surgical techniques.8 Increased inflammation and necrosis of tissue edges were also noted with use of the laser in that study.

Adjunctive therapies were used sparingly in these cases; therefore, specific recommendations for their use cannot be made based on the results of this study. However, tumors for which complete surgical margins cannot be attained or those that have a high incidence of local recurrence following definitive surgery, such as melanoma and squamous cell carcinoma, may be good candidates for postoperative radiation therapy. Tumors with a high incidence of distant recurrence may benefit from chemotherapy or other systemic modalities of treatment. Cases receiving chemotherapy were associated with increased recurrence in this study. This finding is probably due to selection bias, since dogs with more aggressive disease processes are more likely to receive chemotherapy and also suffer recurrence.

Major functions of the tongue during eating include formation of a food bolus, keeping the bolus positioned between the teeth during chewing, and moving the bolus into the pharyngeal region just prior to swallowing.9 Other functions of the tongue include grooming and thermoregulation.9 Partial and subtotal glossectomy was well tolerated in the current study, with no complications attributable to major loss of these functions. Short-term complications seen included ptyalism and dehiscence, which were usually self-limiting.

In the current study, two dogs with more aggressive resections had permanent but mild changes in eating and drinking habits. Dogs in the Carpenter study were initially hand-fed preformed boluses of food.10 Water was offered in a deep dish or bucket because of the dogs’ diminished ability to lap fluids. Similar home care recommendations following glossectomy were given for dogs in this study. Four of five dogs with subtotal to total glossectomies in one study were managed with a gastrostomy tube for the first 2 to 3 weeks following surgery.3 All dogs were able to eat, and four of five were able to drink water within 1 month of surgical treatment. One case report described a dog with a self-induced total glossectomy that was managed with a pharyngostomy tube until the dog was able to eat unaided.11 Only one dog in the current study was managed with a feeding tube, but placement of a feeding tube may be necessary with more aggressive resections, such as near-total and total glossectomies. The aspiration pneumonia that developed in one case 204 days after surgery may have been caused by alterations in deglutition caused by the glossectomy, but it was more likely secondary to the concurrent megaesophagus or local tumor recurrence.

Oral melanoma is a locally invasive neoplasm with a strong predilection to metastasize to regional lymph nodes and the lungs.7 Melanoma was the most common diagnosis in this study, as it was in another recent retrospective study.2 Median survival time, which had not been previously reported for lingual melanoma, was 222 days in this study. In the study by Beck, local tumor control was achieved in four of five tumors treated surgically, with survival times of 330 to 1350 days postoperatively.1 In the current study, only two cases had curative intent surgeries with complete margins achieved. One of these cases had local recurrence at 168 days postoperatively. The other case was disease free at 840 days when euthanized for an unrelated reason. The reason for prolonged survival in this case is unclear, but a recent study reports a small subset of oral melanomas that may be less aggressive.12 More than half of the cases of lingual melanoma in this study had metastases at the time of death; results of a previous study are similar.2 Three chow chows were included in the current study, and all were diagnosed with lingual melanoma. In the study by Dennis, chow chows and Chinese shar peis were more likely to develop lingual melanoma than other breeds of dogs.2

Squamous cell carcinoma is overwhelmingly the most common lingual neoplasm in humans, comprising 95% of tumors in one study.13 Squamous cell carcinoma had been previously identified as the most common tumor in dogs, comprising 37% of the total.1 Squamous cell carcinoma was less common in this study and another recent retrospective study.2 Based on the cases presented in this study and previous reports, surgical resection with complete margins may provide a good long-term prognosis for these animals.1,10 Further study is warranted.

Plasmacytomas comprised 12% of all lingual neoplasms in this study, but they were not diagnosed in a previous large review of canine lingual tumors.1 Extramedullary plasmacytoma is typically a benign tumor, with local recurrence and distant metastasis uncommon following primary therapy.14 Lingual plasmacytomas are one subset of this group, comprising 12 (9%) of 136 extramedullary plasmacytomas diagnosed in one review.14 In the same study, no recurrence was seen following initial surgical treatment in 99 (88%) of 112 dogs with a minimum follow-up period of 12 months. The findings in this study were similar, with one in five cases developing local recurrence. Although there is no statistical sex predilection for this tumor, an interesting trend for males to develop lingual plasmacytomas was seen in 11 of 12 dogs in the study by Clark and in all five dogs of the current study.14

Granular cell tumors and canine papillomas are typically benign, and most occur in the oral cavity.15 Each of these tumors represented 10% of cases in the current study, which was comparable to previous studies.1,2 No local or distant recurrence was seen in any of the cases in the current study.

Canine oral papillomas are typically benign tumors caused by a papillomavirus. Multiple lesions are usually present; they can be smooth, shiny papules or pedunculated, hyperkeratotic masses.9 Many tumors in young dogs will regress spontaneously in 4 to 8 weeks.7 Interestingly, two dogs in the current study were <2 years of age, and two dogs were >10 years of age.

Weaknesses of this study include limitations inherent to all retrospective studies, including incomplete observations, small numbers of patients in each group, and lack of standard treatment and follow-up protocols. Ideally, all cases would have a necropsy performed to identify cause of death and evaluate true rates of local and distant recurrence. Prospective studies focusing on each common tumor type with standard protocols for surgical and postoperative treatment (including necropsy for all individuals) are indicated.

Conclusion

The outcomes between benign and malignant lingual tumors are different; therefore, obtaining incisional biopsies prior to making definitive surgical recommendations is important. Surgical excision may be curative for benign tumors. Dogs with benign lingual tumors have a significantly longer median survival time and DFI than dogs with malignant tumors. Achievement of complete histological margins is significantly associated with an increased median survival time and DFI. Most complications associated with partial and subtotal glossectomies are minor and self-limiting.

Luxar CO2 laser Model LX-20SI; Luxarcare LLC, Woodinville, WA 98072

Theratron 780; Atomic Energy of Canada, Ltd., Ontario, Canada

Statview statistical software; SAS Institute, Inc., Cary, NC 27513

Table 1 Results of Cox Proportional Hazard Analysis of Risk Factors Affecting Survival in Dogs With Lingual Tumors

          Table 1
Table 2 Summary of Significant Associations Among Variables for Dogs With Lingual Tumors

          Table 2
Table 3 Frequency and Percent of Histological Tumor Type in 42 Cases of Canine Lingual Tumors

          Table 3
Table 4 Results of Univariate Analysis of Prognostic Factors Affecting Survival and Disease-free Interval in Dogs With Lingual Tumors

          Table 4
Table 5 Clinical Data for Cases Diagnosed With Lingual Melanoma

          Table 5
Table 5 (cont′d)

          Table 5
Table 6 Clinical Data for Cases Diagnosed With Lingual Squamous Cell Carcinoma

          Table 6
Figure 1—. Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Surgeries with complete margins (n=21) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Surgeries with incomplete margins (n=10) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. A significant survival advantage for dogs with complete surgical margins was noted (P=0.025).Figure 1—. Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Surgeries with complete margins (n=21) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Surgeries with incomplete margins (n=10) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. A significant survival advantage for dogs with complete surgical margins was noted (P=0.025).Figure 1—. Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Surgeries with complete margins (n=21) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Surgeries with incomplete margins (n=10) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. A significant survival advantage for dogs with complete surgical margins was noted (P=0.025).
Figure 1 Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Surgeries with complete margins (n=21) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Surgeries with incomplete margins (n=10) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. A significant survival advantage for dogs with complete surgical margins was noted (P=0.025).

Citation: Journal of the American Animal Hospital Association 44, 6; 10.5326/0440308

Figure 2—. Kaplan-Meier curve for overall survival in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study.Figure 2—. Kaplan-Meier curve for overall survival in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study.Figure 2—. Kaplan-Meier curve for overall survival in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study.
Figure 2 Kaplan-Meier curve for overall survival in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study.

Citation: Journal of the American Animal Hospital Association 44, 6; 10.5326/0440308

Figure 3—. Kaplan-Meier curve for overall disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study.Figure 3—. Kaplan-Meier curve for overall disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study.Figure 3—. Kaplan-Meier curve for overall disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study.
Figure 3 Kaplan-Meier curve for overall disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study.

Citation: Journal of the American Animal Hospital Association 44, 6; 10.5326/0440308

Figure 4—. Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant tumors (n=17) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. A significant survival advantage for dogs with benign tumors was noted (P=0.001).Figure 4—. Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant tumors (n=17) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. A significant survival advantage for dogs with benign tumors was noted (P=0.001).Figure 4—. Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant tumors (n=17) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. A significant survival advantage for dogs with benign tumors was noted (P=0.001).
Figure 4 Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant tumors (n=17) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. A significant survival advantage for dogs with benign tumors was noted (P=0.001).

Citation: Journal of the American Animal Hospital Association 44, 6; 10.5326/0440308

Figure 5—. Kaplan-Meier curve for disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant (n=17) tumors are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study. A significant difference in disease-free interval between the benign and malignant groups was noted (P=0.001).Figure 5—. Kaplan-Meier curve for disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant (n=17) tumors are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study. A significant difference in disease-free interval between the benign and malignant groups was noted (P=0.001).Figure 5—. Kaplan-Meier curve for disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant (n=17) tumors are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study. A significant difference in disease-free interval between the benign and malignant groups was noted (P=0.001).
Figure 5 Kaplan-Meier curve for disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant (n=17) tumors are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study. A significant difference in disease-free interval between the benign and malignant groups was noted (P=0.001).

Citation: Journal of the American Animal Hospital Association 44, 6; 10.5326/0440308

Footnotes

    Doctor Bonczynski’s current address is Animal Specialty Center, 9 Odell Plaza, Yonkers, New York 10701. Doctor Bergman’s current address is Brightheart Veterinary Centers, 80 Business Park Drive, Suite 110, Armonk, New York 10504.

References

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    Dennis MM, Ehrhart N, Duncan CG, et al. Frequency of and risk factors associated with lingual lesions in dogs: 1,196 cases (1995–2004). J Am Vet Med Assoc 2006;228:1533–1537.
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    Dvorak LD, Beaver DP, Ellison GW, et al. Major glossectomy in dogs: a case series and proposed classification system. J Am Anim Hosp Assoc 2004;40:331–337.
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    Bova R, Cheung I, Coman W. Total glossectomy: is it justified? ANZ J Surg 2004;74:134–138.
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    Tiwari R, Karim AB, Greven AJ, et al. Total glossectomy with laryngeal preservation. Arch Otolaryngol Head Neck Surg 1993;119: 945–949.
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    Sultan MR, Coleman JJ. Oncologic and functional considerations of total glossectomy. Am J Surg 1989;158:297–302.
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    Liptak JM, Withrow SJ. Cancer of the gastrointestinal tract. In: Withrow SJ, Vail DM, eds. Small Animal Clinical Oncology. 4th ed. St. Louis: Saunders, 2007:455–510.
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    Mison MB, Steficek B, Lavagnino M, et al. Comparison of the effects of the CO2 surgical laser and conventional surgical techniques on healing and wound tensile strength of skin flaps in the dog. Vet Surg 2003;32:153–160.
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    Lobprise HB, Wiggs RB. Anatomy, diagnosis and management of disorders of the tongue. J Vet Dent 1993;10:16–23.
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    Carpenter LG, Withrow SJ, Powers BE, et al. Squamous cell carcinoma of the tongue in 10 dogs. J Am Anim Hosp Assoc 1993;29: 17–24.
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    Clutton RE, Richards DLS. The management of total tongue avulsion in a dog: a case report. J Small Anim Pract 1987;28:307–310.
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    Spangler WL, Kass PH. The histologic and epidemiologic bases for prognostic considerations in canine melanocytic neoplasia. Vet Pathol 2006;43:136–149.
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    Maddox WA, Sherlock EC, Evans WB. Cancer of the tongue: review of thirteen-year experience—1955–1968. Am Surg 1971;37:624–650.
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    Clark GN, Berg J, Engler SJ, et al. Extramedullary plasmacytomas in dogs: results of surgical excision in 131 cases. J Am Anim Hosp Assoc 1992;28:105–111.
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    Patnaik AK. Histologic and immunohistochemical studies of granular cell tumors in seven dogs, three cats, one horse, and one bird. Vet Pathol 1993;30:176–185.
Copyright: Copyright 2008 by The American Animal Hospital Association 2008
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Figure 1

Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Surgeries with complete margins (n=21) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Surgeries with incomplete margins (n=10) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. A significant survival advantage for dogs with complete surgical margins was noted (P=0.025).


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Figure 2

Kaplan-Meier curve for overall survival in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study.


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Figure 3

Kaplan-Meier curve for overall disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Of these 31 cases, 14 had benign lingual tumors and 17 had malignant lingual tumors. The red circles denote dogs that were censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study.


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Figure 4

Kaplan-Meier survival curve for 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant tumors (n=17) are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Censored cases died of causes other than lingual tumor, or they were alive at the conclusion of this study. A significant survival advantage for dogs with benign tumors was noted (P=0.001).


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Figure 5

Kaplan-Meier curve for disease-free interval in 31 cases of canine lingual tumors with curative intent surgeries. Benign tumors (n=14) are depicted as a blue line, with green circles denoting dogs censored from statistical analysis. Malignant (n=17) tumors are depicted as a red line, with red circles denoting dogs censored from statistical analysis. Cases were censored due to no documented recurrence by the end of this study. A significant difference in disease-free interval between the benign and malignant groups was noted (P=0.001).


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