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Table 1. 
Distribution of TNM Stage
Distribution of TNM Stage
Table 2. 
Patient Demographics by Age
Patient Demographics by Age
Table 3. 
Summary of Treatment*
Summary of Treatment*
Table 4. 
Survival Rates According to Tumor Size and Stage
Survival Rates According to Tumor Size and Stage
1.
Whicker  JHDeSanto  LWDevine  KD Surgical treatment of squamous cell carcinoma of the base of tongue. Laryngoscope.1972;82:1853-1860.
2.
Schleuning  AJSummers  GW Carcinoma of the tongue: review of 220 cases. Laryngoscope.1972;82:1446-1454.
3.
Riley  RWFee  WEGoffinet  DCox  RGoode  RL Squamous cell carcinoma of the base of the tongue. Otolaryngol Head Neck Surg.1983;91:143-150.
4.
Barrs  DMDeSanto  LWO'Fallon  WM Squamous cell carcinoma of the tonsil and tongue-base region. Arch Otolaryngol.1979;105:479-485.
5.
Thawley  SESimpson  JRMarks  JEPerez  CAOgura  JH Preoperative irradiation and surgery for carcinoma of the base of the tongue. Ann Otol Rhinol Laryngol.1983;92:485-490.
6.
Zelefsky  MJHarrison  LBArmstrong  JG Long-term treatment results of postoperative radiation therapy for advanced stage oropharyngeal carcinoma. Cancer.1992;70:2388-2395.
7.
Machtay  MPerch  SMarkiewicz  D  et al Combined surgery and postoperative radiotherapy for carcinoma of the base of tongue: analysis of treatment outcome and prognostic value of margin status. Head Neck.1997;19:494-499.
8.
Nisi  KWFoote  RLBonner  JAMcCaffrey  TV Adjuvant radiotherapy for squamous cell carcinoma of tongue base: improved local-regional disease control compared with surgery alone. Int J Radiat Oncol Biol Phys.1998;41:371-377.
9.
Moore  DMCalcaterra  TC Cancer of the tongue base treated by a transpharyngeal approach. Ann Otol Rhinol Laryngol.1990;99:300-303.
10.
Zeitels  SMVaughan  CWToomy  JM A precision technique for suprahyoid pharyngotomy. Laryngoscope.1991;101:565-566.
11.
Zeitels  SMVaughan  CWRuh  S Suprahyoid pharyngotomy for oropharynx cancer including the tongue base. Arch Otolaryngol Head Neck Surg.1991;117:757-760.
12.
Weber  PCJohnson  JTMyers  EN The suprahyoid approach for squamous cell carcinoma of the base of the tongue. Laryngoscope.1992;102:637-640.
13.
Civantos  FWenig  BL Transhyoid resection of tongue base and tonsil tumors. Otolaryngol Head Neck Surg.1994;111:59-62.
14.
Nasri  SOh  YCalcaterra  TC Transpharyngeal approach to base of tongue tumors: a comparative study. Laryngoscope.1996;106:945-950.
15.
Callery  CDSpiro  RHStrong  EW Changing trends in the management of squamous carcinoma of the tongue. Am J Surg.1984;148:449-454.
16.
Schechter  GLSly  DERoper  AL  et al Set-back tongue flap for carcinoma of the tongue base. Arch Otolaryngol.1980;106:668-671.
17.
Kaylie  DMStevens Jr  KRKang  MYCohen  JIWax  MKAndersen  PE External beam radiation followed by planned neck dissection and brachytherapy for base of tongue squamous cell carcinoma. Laryngoscope.2000;110:1633-1636.
18.
Wanebo  HJChougule  PAkerley  WL  et al Preoperative chemoradiation coupled with aggressive resection as needed ensures near total control in advanced head and neck cancer. Am J Surg.1997;174:518-522.
19.
Lee  HJZelefsky  MJKraus  DH  et al Long-term regional control after radiation therapy and neck dissection for base of tongue carcinoma. Int J Radiat Oncol Biol Phys.1997;38:995-1000.
20.
Robbins  KTFontanesi  JWong  FSH  et al A novel organ preservation protocol for advanced carcinoma of the larynx and pharynx. Arch Otolaryngol Head Neck Surg.1996;122:853-857.
21.
Hinerman  RWParsons  JTMendenhall  WMStringer  SPCassisi  NJMillion  RR External beam irradiation alone or combined with neck dissection for base of tongue carcinoma: an alternative to primary surgery. Laryngoscope.1994;104:1466-1470.
22.
Horwitz  EMFrazier  AJMartinez  AA  et al Excellent functional outcome in patients with squamous cell carcinoma of the base of tongue treated with external irradiation and interstitial iodine 125 boost. Cancer.1996;78:948-957.
23.
Moore  GJParsons  JTMendenhall  WM Quality of life outcomes after primary radiotherapy for squamous cell carcinoma of the base of tongue. Int J Radiat Oncol Biol Phys.1996;36:351-354.
24.
Harrison  LBZelefsky  MJArmstrong  JGCarper  EGaynor  JJSessions  RB Performance status after treatment for squamous cell cancer of the base of tongue: a comparison of primary radiation therapy versus primary surgery. Int J Radiat Oncol Biol Phys.1994;30:953-957.
25.
Mendenhall  WMStringer  SPAmdur  RJHinerman  RWMoore-Higgs  GJCassisi  NJ Is radiation therapy a preferred alternative to surgery for squamous cell carcinoma of the base of tongue? J Clin Oncol.2000;18:35-42.
26.
Blassingame  CD The suprahyoid approach to surgical lesions at the base of the tongue. Ann Otol Rhinol Laryngol.1952;61:483-489.
27.
Huet  PC Note sur les voies d'acces de la base de la langue. Congre Soc Fr Otorhinolaryngol.1946;65:47-52.
28.
Rethi  A A new method of transverse pharyngotomy. J Laryngol Otol.1948;62:440-460.
29.
American Joint Committee on Cancer AJCC Cancer Staging Handbook. 5th ed. Philadelphia, Pa: Lippincott-Raven Publishers; 1998:38-39.
30.
Freeman  DEMendenhall  WMParsons  JTMillion  RR Does neck stage influence local control in squamous cell carcinomas of the head and neck? Int J Radiat Oncol Biol Phys.1992;23:733-736.
31.
Richard  JMSancho-Garnier  HMicheau  CSaravane  DCachin  Y Prognostic factors in cervical lymph node metastasis in upper respiratory and digestive tract carcinomas: study of 1,713 cases during a 15-year period. Laryngoscope.1987;97:97-101.
Original Article
September 2002

Long-term Survival Outcome in Transhyoid Resection of Base of Tongue Squamous Cell Carcinoma

Author Affiliations

From the Division of Head and Neck Surgery, UCLA School of Medicine, Los Angeles, Calif.

Arch Otolaryngol Head Neck Surg. 2002;128(9):1067-1070. doi:10.1001/archotol.128.9.1067
Abstract

Background  The transhyoid approach for the resection of squamous cell carcinoma (SCC) of the base of the tongue continues to evolve and remains controversial. We previously reported that the functional outcome of this operation is superior to that of the traditional transmandibular approaches.

Objective  To report our long-term survival rates for T1, T2, and select T3 SCCs of the base of the tongue using the transhyoid approach.

Patients and Methods  Twenty-eight patients with SCC of the base of the tongue were treated using a transhyoid approach at the University of California, Los Angeles, Medical Center between 1981 and 1998.

Results  All 28 patients underwent simultaneous neck dissection, and 27 patients underwent postoperative radiation therapy. The majority of the patients had advanced stage III or IV SCC. Twenty-five of the 28 patients had clear margins in the final pathologic specimen. The overall 3- and 5-year patient survival rates were 88.5% and 80.0%, respectively. Tumor-specific 5-year survival rates were 80.0%, 84.6%, and 50.0% for T1, T2, and T3 tumors, respectively. Stage-specific 5-year survival rates were 60.0%, 100.0%, and 80.0% for stages II, III, and IV, respectively.

Conclusions  The advantages of the transhyoid approach to SCC of the base of the tongue in conjunction with neck dissection and postoperative radiation therapy include excellent long-term patient survival, improved swallowing and speech function, outstanding tumor exposure, and minimal cosmetic deformity.

SQUAMOUS CELL carcinoma (SCC) of the base of the tongue (BOT) has been associated with a poor prognosis and relatively low 5-year survival rates.14 This type of tumor has been traditionally treated with combined therapy, including surgical resection and radiation therapy.58 Historically, the preferred surgical approaches for BOT SCC have included translabial composite resection or a mandibulotomy (midline or lateral). These approaches were thought to provide the widest possible exposure to the BOT. The transmandibular methods can cause significant secondary morbidity, including lip and chin scars, malocclusion, compromised deglutition, chronic aspiration, and altered speech articulation. As a result, mandible-sparing procedures or primary radiation therapy is now advocated by most centers in the management of BOT tumors.925 One of the best mandbile-sparing procedures is the transhyoid approach, which is the most common surgical alternative for limited, accessible tumors.914

In Blassingame's26 1952 article, he noted that in 1826 Vidal di Cassis was the first to propose a method to gain access to the BOT through the anterior pharyngeal wall. In 1895, Jeremitsch became the first surgeon to use this approach in a practical manner.26 In 1946, Huet27 reintroduced the transhyoid approach for removing BOT tumors, and in 1948, Rethi28 described this method for accessing the lingual thyroid. Despite Blassingame's classic thesis, this approach did not become widely accepted owing to the concern of blindly approaching the deep margin of the BOT and preepiglottic space. In 1990, Moore and Calcaterra9 reported the successful resection of BOT tumors using a modified version of the transhyoid approach. Subsequently, Zeitels et al,10,11 Weber et al,12 and Civantos and Wenig13 also described their excellent results with this method. These authors concluded that the transhyoid approach provides exact anatomical entry with wide exposure of the BOT, while avoiding injury to key neurovascular structures.

At our institution, we treat small to intermediate-sized BOT tumors with combined therapy consisting of a transhyoid surgical excision, neck dissection, and, when appropriate, postoperative radiation therapy. We previously demonstrated that patients who underwent transhyoid resection of BOT tumors had significantly better speech and swallowing functions, with less aspiration, than patients who underwent transmandibular resection.14 In the current study, we present the long-term survival data in cases involving primary surgical excision of BOT SCC with this method and compare the results with those of primary radiotherapy.

PATIENTS AND METHODS

A retrospective chart review was performed in all cases involving patients who were treated for BOT SCC at the University of California, Los Angeles, Medical Center between 1981 and 1998. Twenty-eight patients with BOT SCC were treated with transhyoid surgical resection. All patients underwent preoperative laryngoscopy and advanced imaging studies (ie, computed tomography and/or magnetic resonance imaging) to evaluate the surgical feasibility of the tumor. The patients' disease was staged according to the most recent recommendations of the American Joint Committee on Cancer.29 The operative technique that is used at our institution has been previously described.9 All patients underwent simultaneous ipsilateral or bilateral neck dissections, and the majority also underwent postoperative radiation therapy.

The life table method was used to calculate actual 3- and 5-year survival data. There was no significant delay from diagnosis to surgical treatment in any case. Vital and tumor status at the end of the follow-up period was available either from patient records or from the Central Tumor Registry at the University of California, Los Angeles.

RESULTS

The age range of the patients was 40 to 78 years (average age, 56 years). Twenty-one patients were men and 7 were women. The median follow-up period was 52 months (range of follow-up, 15-112 months). Twenty-six of 28 patients had T1 or T2 tumors (Table 1 and Table 2). Two patients had T3 tumors. A large proportion of the patients' disease was categorized into American Joint Committee on Cancer stage III or IV disease as a result of the high incidence of regional nodal metastasis. No patient's disease was categorized as stage I even though there were 7 T1 tumors. Of the 28 patients, 25 (89%) had clear margins in the final pathologic specimen (Table 3). Twenty-four of the 28 patients underwent primary closure. Seven patients underwent regional or distant microvascular flap reconstruction (ie, pectoralis myocutaneous flap or radial forearm free flap).

The overall 3- and 5-year survival rates with this treatment method were 88.5% and 80.0%, respectively. The respective tumor-specific (TNM) 3- and 5-year survival rates were 85.7% and 80.0% (T1), 84.2% and 84.6% (T2), and 50.0% and 50.0% (T3). The respective stage-specific 3- and 5-year survival rates were 80.0% and 60.0% (stage II), 100% and 100% (stage III), and 86.7% and 80.0% (stage IV). Table 4 summarizes our survival results.

COMMENT

Tonsillar and BOT tumors are the most common oropharyngeal malignancies. The latter have a more aggressive biologic behavior than the former, primarily because of their propensity for submucosal extension and metastatic potential. However, with proper patient selection using advanced radiologic imaging techniques and careful clinical evaluation, therapies can be individualized to maximize control rates. In this series, we have shown that the respective overall 3- and 5-year survival rates of selected, small to intermediate-sized BOT tumors treated with a transhyoid resection (in conjunction with neck dissection and radiation therapy) were 88.5% and 80.0%. The respective tumor-specific 5-year survival rates were 80.0%, 84.6%, and 50.0% for T1, T2, and T3 tumors. These results are comparable to those in previous reports by Weber et al,12 who also examined the control rates using transhyoid resection of T1 and T2 tumors in conjunction with postoperative radiation therapy. Although, their follow-up period was relatively short, they did not see any recurrence in 13 patients who were treated in this manner.

The majority of T1 and T2 lesions in the current study were classified as stage III and IV tumors because of the high incidence of locoregional nodal metastases. Historically, stage III and IV BOT tumors have been associated with poor outcome. Nevertheless, we found that aggressive combination therapy resulted in excellent long-term survival for patients with these advanced-stage tumors. It has also been our experience, as with others, that the biologic behavior of BOT SCC is governed by the size and depth of the tumor rather than the nodal stage and that locoregional metastases do not significantly impair survival.30,31 In an elegant study, Freeman et al30 reviewed 607 cases of head and neck SCC to determine this relationship. They showed that there was no significant correlation between neck stage and primary tumor control on univariate and multivariate analysis.

Our institution previously demonstrated that the transhyoid resection of BOT tumors results in significantly lower morbidity than do the transmandibular methods. Nasri et al14 compared the patients who were treated with the transhyoid approach with those who were treated with composite resection or mandibulotomy. In their study, they did not see any significant difference between the 2 groups in disease-free survival, status of surgical margins, recurrences, or operative complications. However, they did observe significantly superior postoperative speech and swallowing function in the transhyoid group. Civantos and Wenig13 conducted a similar comparison. They also saw no difference in surgical margins and local recurrence but did detect a significantly higher number of serious complications in the transmandibular group. Zeitels et al11 also evaluated 15 patients who had mostly T3 and T4 BOT tumors that were resected via a transoral-transhyoid method. All patients had primary closure and clear margins in the final pathologic specimen, similar to the present study. None of the patients had problems with aspiration, and all patients resumed an oral diet within 3 weeks. Their only complication was a pharyngocutaneous fistula, which resolved with conservative measures.

The treatment of BOT SCC remains controversial. Over the past decade, many centers have successfully broadened the indication of primary radiotherapy to include early and advanced BOT tumors.1725 These groups have reported T1 and T2 5-year survival rates of 73% to 96%. Some groups have reported improved outcome with postirradiation interval neck dissection and/or brachytherapy.17,19,21,22,25 Proponents of primary radiation therapy argue that survival outcome and tumor control are comparable to those of surgical resection, while the morbidity associated with primary radiation is significantly less. However, these studies continue to compare the morbidity of primary radiation therapy with that of a traditional, transmandibular surgical approach. Furthermore, it is difficult to critically ascertain the results of primary radiation therapy from the literature, as outcome studies have included postirradiation neck dissection, brachytherapy, and salvage surgery.

In the present study, we report high overall 5-year survival rates in cases of BOT SCC with the use of primary surgical resection via a transhyoid approach, neck dissection, and postoperative radiation therapy. Given the excellent survival benefits and limited functional morbidity, we continue to promote this aggressive combined therapy for small BOT tumors that do not extend anterior to the circumvallate papillae or onto the mandible.

CONCLUSIONS

The advantages of the transhyoid approach to BOT SCC in conjunction with neck dissection and postoperative radiation therapy include excellent long-term patient survival, improved swallowing and speech function, outstanding tumor exposure, and minimal cosmetic deformity.

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Article Information

Accepted for publication February 21, 2002.

This study was presented as a poster at the annual meeting of the American Head and Neck Society, Palm Desert, Calif, May 14-16, 2001.

Corresponding author and reprints: Elliot Abemayor, MD, PhD, Division of Head and Neck Surgery, UCLA School of Medicine, 62-132 CHS, 10833 Le Conte Ave, Los Angeles, CA 90095-1624.

References
1.
Whicker  JHDeSanto  LWDevine  KD Surgical treatment of squamous cell carcinoma of the base of tongue. Laryngoscope.1972;82:1853-1860.
2.
Schleuning  AJSummers  GW Carcinoma of the tongue: review of 220 cases. Laryngoscope.1972;82:1446-1454.
3.
Riley  RWFee  WEGoffinet  DCox  RGoode  RL Squamous cell carcinoma of the base of the tongue. Otolaryngol Head Neck Surg.1983;91:143-150.
4.
Barrs  DMDeSanto  LWO'Fallon  WM Squamous cell carcinoma of the tonsil and tongue-base region. Arch Otolaryngol.1979;105:479-485.
5.
Thawley  SESimpson  JRMarks  JEPerez  CAOgura  JH Preoperative irradiation and surgery for carcinoma of the base of the tongue. Ann Otol Rhinol Laryngol.1983;92:485-490.
6.
Zelefsky  MJHarrison  LBArmstrong  JG Long-term treatment results of postoperative radiation therapy for advanced stage oropharyngeal carcinoma. Cancer.1992;70:2388-2395.
7.
Machtay  MPerch  SMarkiewicz  D  et al Combined surgery and postoperative radiotherapy for carcinoma of the base of tongue: analysis of treatment outcome and prognostic value of margin status. Head Neck.1997;19:494-499.
8.
Nisi  KWFoote  RLBonner  JAMcCaffrey  TV Adjuvant radiotherapy for squamous cell carcinoma of tongue base: improved local-regional disease control compared with surgery alone. Int J Radiat Oncol Biol Phys.1998;41:371-377.
9.
Moore  DMCalcaterra  TC Cancer of the tongue base treated by a transpharyngeal approach. Ann Otol Rhinol Laryngol.1990;99:300-303.
10.
Zeitels  SMVaughan  CWToomy  JM A precision technique for suprahyoid pharyngotomy. Laryngoscope.1991;101:565-566.
11.
Zeitels  SMVaughan  CWRuh  S Suprahyoid pharyngotomy for oropharynx cancer including the tongue base. Arch Otolaryngol Head Neck Surg.1991;117:757-760.
12.
Weber  PCJohnson  JTMyers  EN The suprahyoid approach for squamous cell carcinoma of the base of the tongue. Laryngoscope.1992;102:637-640.
13.
Civantos  FWenig  BL Transhyoid resection of tongue base and tonsil tumors. Otolaryngol Head Neck Surg.1994;111:59-62.
14.
Nasri  SOh  YCalcaterra  TC Transpharyngeal approach to base of tongue tumors: a comparative study. Laryngoscope.1996;106:945-950.
15.
Callery  CDSpiro  RHStrong  EW Changing trends in the management of squamous carcinoma of the tongue. Am J Surg.1984;148:449-454.
16.
Schechter  GLSly  DERoper  AL  et al Set-back tongue flap for carcinoma of the tongue base. Arch Otolaryngol.1980;106:668-671.
17.
Kaylie  DMStevens Jr  KRKang  MYCohen  JIWax  MKAndersen  PE External beam radiation followed by planned neck dissection and brachytherapy for base of tongue squamous cell carcinoma. Laryngoscope.2000;110:1633-1636.
18.
Wanebo  HJChougule  PAkerley  WL  et al Preoperative chemoradiation coupled with aggressive resection as needed ensures near total control in advanced head and neck cancer. Am J Surg.1997;174:518-522.
19.
Lee  HJZelefsky  MJKraus  DH  et al Long-term regional control after radiation therapy and neck dissection for base of tongue carcinoma. Int J Radiat Oncol Biol Phys.1997;38:995-1000.
20.
Robbins  KTFontanesi  JWong  FSH  et al A novel organ preservation protocol for advanced carcinoma of the larynx and pharynx. Arch Otolaryngol Head Neck Surg.1996;122:853-857.
21.
Hinerman  RWParsons  JTMendenhall  WMStringer  SPCassisi  NJMillion  RR External beam irradiation alone or combined with neck dissection for base of tongue carcinoma: an alternative to primary surgery. Laryngoscope.1994;104:1466-1470.
22.
Horwitz  EMFrazier  AJMartinez  AA  et al Excellent functional outcome in patients with squamous cell carcinoma of the base of tongue treated with external irradiation and interstitial iodine 125 boost. Cancer.1996;78:948-957.
23.
Moore  GJParsons  JTMendenhall  WM Quality of life outcomes after primary radiotherapy for squamous cell carcinoma of the base of tongue. Int J Radiat Oncol Biol Phys.1996;36:351-354.
24.
Harrison  LBZelefsky  MJArmstrong  JGCarper  EGaynor  JJSessions  RB Performance status after treatment for squamous cell cancer of the base of tongue: a comparison of primary radiation therapy versus primary surgery. Int J Radiat Oncol Biol Phys.1994;30:953-957.
25.
Mendenhall  WMStringer  SPAmdur  RJHinerman  RWMoore-Higgs  GJCassisi  NJ Is radiation therapy a preferred alternative to surgery for squamous cell carcinoma of the base of tongue? J Clin Oncol.2000;18:35-42.
26.
Blassingame  CD The suprahyoid approach to surgical lesions at the base of the tongue. Ann Otol Rhinol Laryngol.1952;61:483-489.
27.
Huet  PC Note sur les voies d'acces de la base de la langue. Congre Soc Fr Otorhinolaryngol.1946;65:47-52.
28.
Rethi  A A new method of transverse pharyngotomy. J Laryngol Otol.1948;62:440-460.
29.
American Joint Committee on Cancer AJCC Cancer Staging Handbook. 5th ed. Philadelphia, Pa: Lippincott-Raven Publishers; 1998:38-39.
30.
Freeman  DEMendenhall  WMParsons  JTMillion  RR Does neck stage influence local control in squamous cell carcinomas of the head and neck? Int J Radiat Oncol Biol Phys.1992;23:733-736.
31.
Richard  JMSancho-Garnier  HMicheau  CSaravane  DCachin  Y Prognostic factors in cervical lymph node metastasis in upper respiratory and digestive tract carcinomas: study of 1,713 cases during a 15-year period. Laryngoscope.1987;97:97-101.
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