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Figure 1.
The staging system reported by Shin et al (stage 0, no invasion; stage I, invasion limited to the external perichondrium; stage II, invasion between the rings or destroyed the cartilage; stage III, invasion extending through or between the cartilage into the lamina propria of tracheal mucosa; stage IV, tracheal mucosal invasion). The top half shows the epithelium, and the bottom half shows the adventitia.

The staging system reported by Shin et al19 (stage 0, no invasion; stage I, invasion limited to the external perichondrium; stage II, invasion between the rings or destroyed the cartilage; stage III, invasion extending through or between the cartilage into the lamina propria of tracheal mucosa; stage IV, tracheal mucosal invasion). The top half shows the epithelium, and the bottom half shows the adventitia.

Figure 2.
Typical bronchoscopic findings at each stage. A and B, stage I; C and D, stage II; E through J, stage III; and K and L, stage IV. The arrows show the invaded areas.

Typical bronchoscopic findings at each stage. A and B, stage I; C and D, stage II; E through J, stage III; and K and L, stage IV. The arrows show the invaded areas.

Demographics, Tumor Stage, Surgical Procedures Performed, and Bronchoscopic Findings of 16 Patients With Laryngotracheal Invasion*
Demographics, Tumor Stage, Surgical Procedures Performed, and Bronchoscopic Findings of 16 Patients With Laryngotracheal Invasion*
1.
McConahey  WMHay  IDWoolner  LBvanHeerden  JATaylor  WF Papillary thyroid cancer treated at the Mayo Clinic, 1946 through 1970: initial manifestations, pathologic findings, therapy, and outcome. Mayo Clin Proc. 1986;61978- 996Article
2.
Ishihara  TKobayashi  KKikuchi  KKato  RKawamura  MIto  K Surgical treatment of advanced thyroid carcinoma invading the trachea. J Thorac Cardiovasc Surg. 1991;102717- 720
3.
Hay  IDBergstralh  EJGoellner  JREbersold  JRGrant  CS Predicting outcome in papillary thyroid carcinoma: development of a reliable prognostic scoring system in a cohort of 1779 patients surgically treated at one institution during 1940 through 1989. Surgery. 1993;1141050- 1058
4.
Dean  DSHay  ID Prognostic indicators in differentiated thyroid carcinoma. Cancer Control. 2000;7229- 239
5.
Tovi  FGoldstein  J Locally aggressive differentiated thyroid carcinoma. J Surg Oncol. 1985;2999- 104Article
6.
Czaja  JMMcCaffrey  TV The surgical management of laryngotracheal invasion by well-differentiated papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg. 1997;123484- 490Article
7.
McCaffrey  TVBergstralh  EJHay  ID Locally invasive papillary thyroid carcinoma: 1940-1990. Head Neck. 1994;16165- 172Article
8.
Nakao  KMiyata  MIzukura  MMonden  YMaeda  MKawashima  Y Radical operation for thyroid carcinoma invading the trachea. Arch Surg. 1984;1191046- 1049Article
9.
Bayles  SWKingdom  TTCarlson  GW Management of thyroid carcinoma invading the aerodigestive tract. Laryngoscope. 1998;1081402- 1407Article
10.
Segal  KAbraham  ALevy  RSchindel  J Carcinomas of the thyroid gland invading larynx and trachea. Clin Otolaryngol. 1984;921- 25
11.
Nishida  TNakao  KHamaji  M Differentiated thyroid carcinoma with airway invasion: indication for tracheal resection based on the extent of cancer invasion. J Thorac Cardiovasc Surg. 1997;11484- 92Article
12.
Ballantyne  AJ Resections of the upper aerodigestive tract for locally invasive thyroid cancer. Am J Surg. 1994;168636- 639Article
13.
Yang  CCLee  CHWang  LSHuang  BSHsu  WHHuang  MH Resectional treatment for thyroid cancer with tracheal invasion: a long-term follow-up study. Arch Surg. 2000;135704- 707Article
14.
Fujimoto  YObara  TIto  Y  et al.  Aggressive surgical approach for locally invasive papillary carcinoma of the thyroid in patients over forty-five years of age. Surgery. 1986;1001098- 1107
15.
Ishihara  TYamazaki  SKobayashi  K  et al.  Resection of the trachea infiltrated by thyroid carcinoma. Ann Surg. 1982;195496- 500Article
16.
McCaffrey  JC Evaluation and treatment of aerodigestive tract invasion by well-differentiated thyroid carcinoma. Cancer Control. 2000;7246- 252
17.
McCaffrey  TVLipton  RJ Thyroid carcinoma invading the upper aerodigestive system. Laryngoscope. 1990;100824- 830Article
18.
Park  CSSuh  KWMin  JS Cartilage-shaving procedure for the control of tracheal cartilage invasion by thyroid carcinoma. Head Neck. 1993;15289- 291Article
19.
Shin  DHMark  EJSuen  HCGrillo  HC Pathologic staging of papillary carcinoma of the thyroid with airway invasion based on the anatomic manner of extension to the trachea: a clinicopathologic study based on 22 patients who underwent thyroidectomy and airway resection. Hum Pathol. 1993;24866- 870Article
20.
Friedman  MDanielzadeh  JACaldarelli  DD Treatment of patients with carcinoma of the thyroid invading the airway. Arch Otolaryngol Head Neck Surg. 1994;1201377- 1381Article
21.
Akslen  LAHaldorsen  TThoresen  SOGlattre  E Survival and causes of death in thyroid cancer: a population-based study of 2479 cases from Norway. Cancer Res. 1991;511234- 1241
22.
Talpos  GB Tracheal and laryngeal resections for differentiated thyroid cancer. Am Surg. 1999;65754- 760
23.
Batsakis  JG Laryngeal involvement by thyroid disease. Ann Otol Rhinol Laryngol. 1987;96718- 719
24.
Ebihara  MEbihara  SKishimoto  S  et al.  Surgical treatment of differentiated thyroid cancer with tracheal invasion [in Japanese]. Nippon Jibiinkoka Gakkai Kaiho. 1998;1011406- 1411Article
25.
Melliere  DJBen Yahia  NEBecquemin  JPLange  FBoulahdour  H Thyroid carcinoma with tracheal or esophageal involvement: limited or maximal surgery? Surgery. 1993;113166- 172
26.
Britto  EShah  SParikh  DMRao  RS Laryngotracheal invasion by well-differentiated thyroid cancer: diagnosis and management. J Surg Oncol. 1990;4425- 31Article
27.
Grillo  HCSuen  HCMathisen  DJWain  JC Resectional management of thyroid carcinoma invading the airway. Ann Thorac Surg. 1992;543- 10Article
28.
Choi  TKSiu  KFLam  KHWong  J Bronchoscopy and carcinoma of the esophagus, II: carcinoma of the esophagus with tracheobronchial involvement. Am J Surg. 1984;147760- 762Article
29.
Choi  TKSiu  KFLam  KHWong  J Bronchoscopy and carcinoma of the esophagus, I: findings of bronchoscopy in carcinoma of the esophagus. Am J Surg. 1984;147757- 759Article
30.
Watanabe  ASaka  HSakai  SHirao  THattori  TShimokata  K Bronchoscopic and cytopathological findings of tracheobronchial involvement in esophageal carcinoma. Endoscopy. 1990;22273- 275Article
31.
Riedel  MHauck  RWStein  HJ  et al.  Preoperative bronchoscopic assessment of airway invasion by esophageal cancer: a prospective study. Chest. 1998;113687- 695Article
Original Article
October 2001

Bronchoscopic Diagnosis of Thyroid Cancer With Laryngotracheal Invasion

Author Affiliations

From the Noguchi Thyroid Clinic and Hospital Foundation, Oita, Japan.

Arch Surg. 2001;136(10):1185-1189. doi:10.1001/archsurg.136.10.1185
Abstract

Hypothesis  Some controversy exists concerning the appropriate surgical management for patients with thyroid cancer invading the laryngotracheal wall. We have used shaving of the wall when cancer invasion was confined to the perichondrium, and extensive resection when it invaded further. Preoperative assessment of the depth and length of laryngotracheal invasion is important when choosing an appropriate surgical procedure.

Design  Prospective study.

Setting  A Japanese center for thyroid diseases, where about 1400 thyroid operations are performed each year.

Patients  Of 171 patients with thyroid cancer who were surgically treated between January 1, 2000, and July 30, 2000, 37 were suspected to have laryngotracheal invasion on preoperative magnetic resonance imaging or ultrasonography.

Intervention  We used bronchoscopy to examine the 37 patients suspected to have laryngotracheal invasion.

Main Outcome Measure  Bronchoscopic findings (localized mucosal redness, telangiectasia, mucosal elevation, mucosal edema, and mucosal erosion) were compared with pathological results in the 30 patients who underwent curative resections. Seven patients were excluded because of palliative resections.

Results  Of the 18 patients without localized mucosal changes, we performed shaving of the laryngotracheal wall in 4 patients because we found laryngotracheal invasion during surgery. Shaving of the laryngotracheal wall was performed successfully in terms of obtaining a cancer-free margin. Twelve patients with localized mucosal redness required extensive resections. Other mucosal changes were found depending on the depth of cancer invasion.

Conclusion  Surgeons should perform extensive resections when encountering localized mucosal redness on bronchoscopy.

DIFFERENTIATED thyroid cancer usually has a good prognosis; however, it sometimes invades the adjacent organs and causes death by asphyxia. The practice of complete resection of malignant tumors has improved local control and survival rates.14 Among cases in which cancer spread, laryngotracheal extension has been reported in 35% to 60% of patients with locally invasive diseases.57 Preoperative assessment of laryngotracheal invasion is important when choosing the appropriate treatment. The surgical procedures used currently include shaving of the laryngotracheal wall and extensive resection (fenestration, segmental tracheal resection, and partial or total laryngectomy). The choice of procedure depends on several variables, such as patient age, histological type, and depth and extent of invasion.516 We have applied shaving of the laryngotracheal wall for differentiated thyroid cancer invading the perichondrium and, when feasible, extensive resection for differentiated thyroid cancer with deeper invasion. Judging whether thyroid cancer invades deeper than the perichondrium of the trachea can be difficult to do during surgery. Therefore, it is important to make a correct preoperative assessment of the depth and length of laryngotracheal invasion.

We describe the cases in which we evaluated bronchoscopic findings of laryngotracheal invasion of thyroid cancer to predict the depth and length of invasion so that we could determine the appropriate surgical procedure. Although many reports8,14,1618 document the preoperative evaluation of laryngotracheal invasion by computed tomography, magnetic resonance imaging (MRI), or bronchoscopy, none of these has comprehensively addressed the issue of determining surgical procedures.

PATIENTS AND METHODS
PATIENTS

Between January 1, 2000, and July 30, 2000, 171 patients underwent surgery for thyroid cancer, and 16 (9.4%) of these had laryngotracheal invasion. There were 3 men and 13 women whose ages ranged from 33 to 84 years (mean, 60.8 years). The mean tumor size was 32.9 mm. We examined all 171 patients using MRI and ultrasonography (US). Selection criteria for bronchoscopy were based on either MRI or US findings. An unclear border between the thyroid tumor and the laryngotracheal wall or destruction of the laryngotracheal wall was defined as a positive sign of invasion. We suspected laryngotracheal invasion when deletion of the fat plane between the thyroid tumor and the laryngotracheal wall was seen. We used bronchoscopy to examine 37 patients in whom laryngotracheal invasion was diagnosed or suspected by MRI or US. Seven patients were excluded because complete resections of the thyroid tumor were not performed. Shaving of the laryngotracheal wall was performed in 4 patients in whom invasion was suspected during dissection; although bronchoscopic diagnosis in them was negative for laryngotracheal invasion. Extensive resection was performed in 12 patients in whom diagnosis by bronchoscopy indicated laryngotracheal invasion. Fourteen patients received no laryngotracheal resection because no invasion was found at operation. Other organs (the esophagus, the recurrent laryngeal nerve, or the strap muscle) were resected in 10 patients. Demographic data, tumor stage, surgical procedure performed, and bronchoscopic findings of 16 patients with laryngotracheal invasion are presented in Table 1.

BRONCHOSCOPY

Bronchoscopic examination with a BF 1T30 endoscope (Olympus Co Ltd, Tokyo, Japan) was done with patients under local anesthesia. Localized mucosal redness, telangiectasia, mucosal elevation, mucosal edema, or mucosal erosion were considered the signs of invasion. Laryngotracheal invasion was diagnosed when at least 1 of these mucosal changes was seen. Diffuse mucosal redness and telangiectasia caused by compression were not considered positive signs. In 30 patients, the preoperative bronchoscopic diagnosis was compared with pathological results.

PATHOLOGICAL STAGING

We adopted the pathological staging system for laryngotracheal invasion by thyroid cancer as reported by Shin et al19 (stage 0, no invasion; stage I, invasion limited to the external perichondrium; stage II, invasion between the rings or destroyed the cartilage; stage III, invasion extending through or between the cartilage into the lamina propria of tracheal mucosa; stage IV, tracheal mucosal invasion) (Figure 1).

RESULTS

According to the classification by Shin et al,19 of 30 patients who underwent complete resections, 14 patients without laryngotracheal invasion were at stage 0. Four patients in whom cancer cells were detected in the shaved materials, although they showed no macroscopic residual tumors, were at stage I. Two patients were at stage II, 8 were at stage III, and 2 were at stage IV. Of these16 patients between stage I and stage IV, 14 had papillary cancers, 1 had follicular cancer, and 1 had anaplastic cancer.

The diagnostic usefulness of bronchoscopy was evaluated by stages. Because of the lack of localized mucosal changes, no stage I patients were diagnosed as showing invasion. In contrast, all patients in stages II, III, and IV were correctly diagnosed as having laryngotracheal invasion. Typical bronchoscopic images from each stage are shown in Figure 2. Of 4 patients with stage I tumors, none showed localized mucosal changes of the larynx and trachea regardless of tumor compression. In 12 patients with tumors at stages II, III, or IV who required extensive resection, localized mucosal changes were always present in various degrees. Localized mucosal redness was seen in all patients with or without compression, and telangiectasia was occasionally seen in patients at each stage. Mucosal edema, elevation, and erosion were occasionally seen in patients at stages III and IV.

All patients with complete resections (except 1 patient with anaplastic cancer who died 5 months after surgery) were alive without recurrence at the time of this study.

COMMENT

Differentiated thyroid cancer usually has a good prognosis, particularly if the tumor is confined to the gland. Invasion of adjacent organs makes the prognosis unfavorable.1,8,20,21 Laryngotracheal invasion is common, accounting for 35% to 60% of all locally invasive diseases,57 and it has been reported to occur in 3.7% to 12.4% of all thyroid cancers.810,18,2224 Although complete resection of a malignant tumor improves local control and survival rate,14 appropriate indications for either shaving the laryngotracheal wall or extensive resection for the laryngotracheal invasion is controversial.516,18,20,2527 Czaja et al6 have applied extensive resection of thyroid cancers invading the laryngotracheal mucosa or submucosa, and shaving of the laryngotracheal wall for tumors invading only the laryngotracheal perichondrium. Several groups have agreed to this indication for determining surgical procedures.7,1012,16 We also have applied these indications because we ascertained a cancer-free margin by intraoperative pathological diagnosis. Other groups did not advocate shaving of the laryngotracheal wall, but they did not discuss the depth of cancer invasion. Only Park et al18 concluded that extensive resection should be performed even if thyroid cancer invaded only the perichondrium.

To our knowledge to date, this is the first study to evaluate the bronchoscopic invasive signs of thyroid cancer by focusing on its depth and length as preoperative indicators for choosing an appropriate surgical treatment. Computed tomography scanning and MRI are useful for massive intraluminal involvement of thyroid cancer, but they seem to be of limited use for examining the depth and length of laryngotracheal invasion. Some authors have reported the usefulness of bronchoscopy for tracheal invasion with esophageal cancer.2831 Esophageal cancer invades the trachea from the posterior wall that lacks cartilage. Thyroid cancer usually invades the trachea between the rings of the cartilage. Therefore, the invasive signs of esophageal cancer on bronchoscopy cannot simply be applied as an invasive sign of thyroid cancer.

Localized mucosal change is an important sign of laryngotracheal invasion, especially localized mucosal redness. In stage I patients, the only mucosal change is diffuse mucosal redness caused by compression. In patients at stages II, III, and IV, localized mucosal redness always exists at various degrees, and this redness is stronger than that caused by compression. Histologically, the trachea consists of 4 layers: epithelium, lamina propria of mucosa, tracheal cartilage, and adventitia. The lamina propria of mucosa, which occupies a wide area under the epithelium and extends between the rings of the cartilage, is rich in blood and lymph vessels. Disturbance of blood and lymph flow by injury to the lamina propria induces mucosal changes such as redness, telangiectasia, and edema. Injury of the lamina propria by a large thyroid nodule is caused by strong compression on the tracheal cartilage, causing congestion and lymphostasis in the lamina propria, and resulting in diffuse mucosal changes. The injury to the lamina propria by thyroid cancer usually occurs between the rings of the cartilage, and only the invaded area shows congestion and lymphostasis resulting in localized mucosal changes.

Bronchoscopy is useful as a preoperative procedure for determining the appropriate surgical strategy for thyroid cancer invading the laryngotracheal wall.

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Article Information

Corresponding author: Hiroyuki Yamashita, MD, PhD, 6-33 Noguchi Nakamachi, Beppu, Oita, 874-0932 Japan (e-mail: yama@noguchi-med.or.jp).

References
1.
McConahey  WMHay  IDWoolner  LBvanHeerden  JATaylor  WF Papillary thyroid cancer treated at the Mayo Clinic, 1946 through 1970: initial manifestations, pathologic findings, therapy, and outcome. Mayo Clin Proc. 1986;61978- 996Article
2.
Ishihara  TKobayashi  KKikuchi  KKato  RKawamura  MIto  K Surgical treatment of advanced thyroid carcinoma invading the trachea. J Thorac Cardiovasc Surg. 1991;102717- 720
3.
Hay  IDBergstralh  EJGoellner  JREbersold  JRGrant  CS Predicting outcome in papillary thyroid carcinoma: development of a reliable prognostic scoring system in a cohort of 1779 patients surgically treated at one institution during 1940 through 1989. Surgery. 1993;1141050- 1058
4.
Dean  DSHay  ID Prognostic indicators in differentiated thyroid carcinoma. Cancer Control. 2000;7229- 239
5.
Tovi  FGoldstein  J Locally aggressive differentiated thyroid carcinoma. J Surg Oncol. 1985;2999- 104Article
6.
Czaja  JMMcCaffrey  TV The surgical management of laryngotracheal invasion by well-differentiated papillary thyroid carcinoma. Arch Otolaryngol Head Neck Surg. 1997;123484- 490Article
7.
McCaffrey  TVBergstralh  EJHay  ID Locally invasive papillary thyroid carcinoma: 1940-1990. Head Neck. 1994;16165- 172Article
8.
Nakao  KMiyata  MIzukura  MMonden  YMaeda  MKawashima  Y Radical operation for thyroid carcinoma invading the trachea. Arch Surg. 1984;1191046- 1049Article
9.
Bayles  SWKingdom  TTCarlson  GW Management of thyroid carcinoma invading the aerodigestive tract. Laryngoscope. 1998;1081402- 1407Article
10.
Segal  KAbraham  ALevy  RSchindel  J Carcinomas of the thyroid gland invading larynx and trachea. Clin Otolaryngol. 1984;921- 25
11.
Nishida  TNakao  KHamaji  M Differentiated thyroid carcinoma with airway invasion: indication for tracheal resection based on the extent of cancer invasion. J Thorac Cardiovasc Surg. 1997;11484- 92Article
12.
Ballantyne  AJ Resections of the upper aerodigestive tract for locally invasive thyroid cancer. Am J Surg. 1994;168636- 639Article
13.
Yang  CCLee  CHWang  LSHuang  BSHsu  WHHuang  MH Resectional treatment for thyroid cancer with tracheal invasion: a long-term follow-up study. Arch Surg. 2000;135704- 707Article
14.
Fujimoto  YObara  TIto  Y  et al.  Aggressive surgical approach for locally invasive papillary carcinoma of the thyroid in patients over forty-five years of age. Surgery. 1986;1001098- 1107
15.
Ishihara  TYamazaki  SKobayashi  K  et al.  Resection of the trachea infiltrated by thyroid carcinoma. Ann Surg. 1982;195496- 500Article
16.
McCaffrey  JC Evaluation and treatment of aerodigestive tract invasion by well-differentiated thyroid carcinoma. Cancer Control. 2000;7246- 252
17.
McCaffrey  TVLipton  RJ Thyroid carcinoma invading the upper aerodigestive system. Laryngoscope. 1990;100824- 830Article
18.
Park  CSSuh  KWMin  JS Cartilage-shaving procedure for the control of tracheal cartilage invasion by thyroid carcinoma. Head Neck. 1993;15289- 291Article
19.
Shin  DHMark  EJSuen  HCGrillo  HC Pathologic staging of papillary carcinoma of the thyroid with airway invasion based on the anatomic manner of extension to the trachea: a clinicopathologic study based on 22 patients who underwent thyroidectomy and airway resection. Hum Pathol. 1993;24866- 870Article
20.
Friedman  MDanielzadeh  JACaldarelli  DD Treatment of patients with carcinoma of the thyroid invading the airway. Arch Otolaryngol Head Neck Surg. 1994;1201377- 1381Article
21.
Akslen  LAHaldorsen  TThoresen  SOGlattre  E Survival and causes of death in thyroid cancer: a population-based study of 2479 cases from Norway. Cancer Res. 1991;511234- 1241
22.
Talpos  GB Tracheal and laryngeal resections for differentiated thyroid cancer. Am Surg. 1999;65754- 760
23.
Batsakis  JG Laryngeal involvement by thyroid disease. Ann Otol Rhinol Laryngol. 1987;96718- 719
24.
Ebihara  MEbihara  SKishimoto  S  et al.  Surgical treatment of differentiated thyroid cancer with tracheal invasion [in Japanese]. Nippon Jibiinkoka Gakkai Kaiho. 1998;1011406- 1411Article
25.
Melliere  DJBen Yahia  NEBecquemin  JPLange  FBoulahdour  H Thyroid carcinoma with tracheal or esophageal involvement: limited or maximal surgery? Surgery. 1993;113166- 172
26.
Britto  EShah  SParikh  DMRao  RS Laryngotracheal invasion by well-differentiated thyroid cancer: diagnosis and management. J Surg Oncol. 1990;4425- 31Article
27.
Grillo  HCSuen  HCMathisen  DJWain  JC Resectional management of thyroid carcinoma invading the airway. Ann Thorac Surg. 1992;543- 10Article
28.
Choi  TKSiu  KFLam  KHWong  J Bronchoscopy and carcinoma of the esophagus, II: carcinoma of the esophagus with tracheobronchial involvement. Am J Surg. 1984;147760- 762Article
29.
Choi  TKSiu  KFLam  KHWong  J Bronchoscopy and carcinoma of the esophagus, I: findings of bronchoscopy in carcinoma of the esophagus. Am J Surg. 1984;147757- 759Article
30.
Watanabe  ASaka  HSakai  SHirao  THattori  TShimokata  K Bronchoscopic and cytopathological findings of tracheobronchial involvement in esophageal carcinoma. Endoscopy. 1990;22273- 275Article
31.
Riedel  MHauck  RWStein  HJ  et al.  Preoperative bronchoscopic assessment of airway invasion by esophageal cancer: a prospective study. Chest. 1998;113687- 695Article
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