ATS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Henning A. Gaissert
Hermes C. Grillo
Cameron D. Wright
John C. Wain
Douglas J. Mathisen
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Gaissert, H. A.
Right arrow Articles by Mathisen, D. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Gaissert, H. A.
Right arrow Articles by Mathisen, D. J.
Related Collections
Right arrow Trachea and bronchi

Ann Thorac Surg 2006;82:268-273
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Uncommon Primary Tracheal Tumors

Henning A. Gaissert, MD a , b , * , Hermes C. Grillo, MD a , M. Behgam Shadmehr, MD a , Cameron D. Wright, MD a , Manjusha Gokhale, MA c , John C. Wain, MD a , Douglas J. Mathisen, MD a

a Division of Thoracic Surgery, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
b Center for Clinical Effectiveness in Surgery, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
c Policy Analysis, Inc, Brookline, Massachusetts

Accepted for publication January 17, 2006.

* Address correspondence to Dr Gaissert, Massachusetts General Hospital, Blake 1570, 55 Fruit St, Boston, MA 02114 (Email: hgaissert{at}partners.org).

Presented at the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 30–Feb 1, 2006.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: Primary tracheal tumors other than adenoid cystic or squamous cell carcinoma are uncommon and have a heterogeneous histologic appearance. The experience regarding their treatment and long-term outcome is limited, and alternatives to segmental tracheal resection, including endoscopic treatment or radiation, continue to be explored.

METHODS: A retrospective analysis was performed of uncommon tracheal tumors among 360 primary tracheal tumors seen over 40 years, excluding adenoid cystic and squamous cell carcinoma.

RESULTS: Of 90 patients, 34 (38%) had benign tumors and 56 malignant: 11 carcinoid tumors, 14 mucoepidermoid carcinomas, 13 sarcomas, 15 nonsquamous bronchogenic carcinomas, 2 lymphomas, and 1 melanoma. Three patients had a second tracheal malignancy. Dyspnea was the most common symptom in benign tumors and hemoptysis in malignant tumors. Twelve patients did not undergo tracheal resection (13.3%) and 1 died before resection. Surgical therapy in 77 patients (85%) consisted of laryngectomy in 3, laryngotracheal resection in 9, tracheal resection in 46, and carinal resection in 19. Hospital mortality was 2.6% (2 of 77 patients) and major complications occurred in 16% (12 of 77 patients). Mean follow-up was 9.7 years. After resection, survival at 10 years was 94% for benign and 83% for carcinoid tumors, and at 5 years survival was 60% for bronchogenic carcinoma, 100% for mucoepidermoid tumors, and 78% for sarcomas. Patients with lymphomas and melanoma are alive more than 8 years after resection. Ten patients experienced recurrence (14%).

CONCLUSIONS: Surgical resection of uncommon primary tracheal tumors alleviates airway obstruction, is curative in patients with benign or slow-growing malignant lesions, and prolongs survival in highly malignant lesions.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Discussion
 References
 
A majority of primary tracheal tumors are squamous cell or adenoid cystic carcinomas [1, 2]. In these primary carcinomas, we identified the extent of local disease as the most important factor determining therapy [2]. The other primary neoplasms involving the trachea, subglottic space, and carina belong to a diverse histologic spectrum ranging from nonsquamous bronchogenic carcinoma to benign tumors. These tumors defy easy categorization and are therefore reported either as part of a larger experience [3–5] or in separate series examining individual histologic appearance [6–8]. Local treatment modalities other than segmental airway resection, including endoscopic removal, laser application, and primary radiation, have been used, usually with inferior or unknown long-term survival. The present study reports a consecutive series of uncommon tracheal tumors to describe their long-term outcome.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 References
 
Patient Selection
A retrospective analysis was conducted at Massachusetts General Hospital of all primary tracheal tumors since 1962. Medical records and Department of Pathology databases were searched. Pathology reports, operative reports, and hospital charts were reviewed. Squamous cell and adenoid cystic carcinomas as well as tumors of adjacent anatomic regions, the glottic larynx, and those extending from mainstem bronchi or lung to the carina were excluded. Squamous papillomas and tumors of the subglottic larynx or the carina were included. The survival period began on the day of operation in resectable and the day of bronchoscopy in unresectable patients. The Massachusetts General Hospital institutional review board approved this protocol in October 2001. Consent was received from patients before obtaining follow-up information.

Determination of Resectability
Every patient underwent rigid bronchoscopy. Bronchoscopic biopsy was performed of any lesion deemed malignant and selectively of those that were localized and apparently benign. Patients with malignant tumors also had an assessment of locoregional and distant metastatic disease before resection. The most striking change in the preoperative radiographic evaluation over 40 years has occurred with the shift from conventional tracheal tomography to computed tomography and its recent algorithms for three-dimensional depiction of the tracheal lumen. An improved yield of information that would affect the determination of resectability or a decreased need for exploration has not yet been identified. Tracheal resection was considered only when complete resection seemed feasible. Microscopic involvement of airway margins was accepted if the airway was normal on gross inspection and no further length of airway could be resected. Resection was not performed when it would have resulted in grossly positive peritracheal margins. A tumor was also considered unresectable when metastatic disease was present, the length of involved airway at bronchoscopy was judged to preclude safe reconstruction, or invasion of certain adjacent organs was found during operative exploration. Local resection of esophageal invasion with lateral excision of muscle or full-thickness esophageal wall was considered, but total esophagectomy was not performed to avoid devascularizing the trachea.

Types of Resection
The surgical technique has been detailed previously [9]. For standard tracheal resection, a sleeve of trachea is removed with end-to-end reconstruction. When laryngectomy is required, cervical or mediastinal end-tracheostomy is performed. For laryngotracheal resection, the tumor-bearing infraglottic larynx is removed while preserving at least one recurrent laryngeal nerve. A purely bronchoscopic resection is considered in patients with multiple mucosal tumors that cannot be encompassed with a segmental tracheal resection.

In malignant tumors, systematic lymph node dissection is avoided to preserve tracheal blood supply. Regional lymph nodes are often not included in the specimen if not grossly enlarged. Absence of tumor at the airway margins is confirmed by frozen section unless the limits of resection have been reached and no additional trachea can be removed. The resection is judged to be complete when airway margins are found to be disease-free, the peripheral soft tissue margin does not expose gross tumor, and no statement in the operative note indicates that the resection was incomplete.

Tumor Data
Tumor dimension in the long axis of the airway, depth of invasion, and the presence of tumor at airway or radial margins were recorded after resection from a review of pathology reports. Positive airway margins indicated true residual tumor, most often microscopic. In contrast, the radial margins were interpreted as positive when tumor was seen within 1 mm of the margin, usually indicating that only a thin layer of connective tissue covered the outside of the tumor. Tumor involvement of excised lymph nodes was noted.

Adjuvant and Primary Radiotherapy
Adjuvant postoperative radiotherapy was introduced for malignant tumors during the second decade of this experience for close or tumor-bearing margins. After bronchoscopic assessment of anastomotic healing, a recommended dose of 54 Gy was administered 6 weeks after resection. Primary radiotherapy with 60 Gy was recommended for patients who had unresectable tumors, but could not be confirmed in all patients. Most patients received radiation treatment outside Massachusetts General Hospital.

Follow-Up
Patients and their physicians were contacted for follow-up information. The Social Security Death Index was searched. Patients were determined to have died if name, date of birth, and social security number matched. Follow-up information on treatment and tumor status in patients who did not undergo resection was often limited to the date of death.

Statistical Analysis
Crude (arithmetic) survival rates were calculated for tumor type and resection, whereas adjusted (Kaplan–Meier) survival rates were selected for benign and malignant tumors using the SAS system (SAS, version 9.13, Cary, NC).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 References
 
Between 1962 and 2002, 357 patients were evaluated for primary tracheal tumors. A tracheal histologic appearance other than squamous cell or adenoid cystic carcinoma was found in 87 patients. Three additional patients had squamous cell carcinoma and a second histologic diagnosis (small cell carcinoma in 2 and mucoepidermoid carcinoma in 1); the procedures of these patients are counted, but they were excluded from survival analysis. There were 54 men and 36 women with a mean age of 43 years (range, 4 to 81 years). Symptoms and their duration are detailed in Table 1. The mean duration of symptoms was 12 months, ranging from 7 months in patients with sarcoma or nonsquamous bronchogenic carcinoma to 20 months in benign tumors. Cough and hemoptysis were present in both benign and malignant tumors, although hemoptysis was more prevalent in the latter.


View this table:
[in this window]
[in a new window]
  		Table 1. Symptoms
 
Table 2 lists the histologic diagnosis obtained from either bronchoscopic biopsy or resection specimen. Fifty-six of 90 patients (62%) had malignant neoplasms of diverse differentiation, most belonging to four main categories: nonsquamous carcinoma, carcinoid tumors, mucoepidermoid carcinoma, and sarcoma. Two patients with lymphoma underwent tracheal resection for strictures after chemotherapy. One patient underwent curative resection of a melanoma. A variety of benign tumors were found in 34 patients (38%), of whom 9 had squamous papillomas. In this series, 27 patients (30%) underwent other procedures before resection. An endoscopic tumor core-out was performed in 19 patients and laser treatments in 6. Two patients were referred after tracheostomy.


View this table:
[in this window]
[in a new window]
  		Table 2. Tumor Types
 
One patient died before planned resection of a tracheal sarcoma eroding into the azygous vein. Disease not amenable to resection was found in 12 patients (13.3%). The extent of airway involvement prohibited resection in 4 patients with squamous papillomas and in 1 patient each with sarcoma, bronchogenic carcinoma, and a benign but diffuse glomus tumor. Extensive regional disease was discovered in 2 patients with mucoepidermoid carcinoma, one of whom underwent mediastinal exploration, and in 1 patient with bronchogenic carcinoma. Distant metastasis was found in 2 other patients with bronchogenic carcinoma.

Seventy-seven patients underwent segmental resection of the tumor. These procedures were the first attempt at tracheal resection except in 2 patients who had prior interventions elsewhere: 1 had a local excision of the cervical tracheal wall through which a tracheostomy had been placed. The other had a tracheal resection for adenocarcinoma and was referred with a positive resection margin. The resection rate for benign tumors was 96%, excluding squamous papillomas. For malignant tumors, the resection rate was 89%. The types of procedures are detailed in Table 3. A majority of resections, 60%, involved tracheal end-to-end reconstruction. One tracheal resection for a recurrent plexiform neurofibroma included lateral full-thickness resection of the esophageal wall.


View this table:
[in this window]
[in a new window]
  		Table 3. Surgical Procedures and Pathologic Data a
 
The hospital mortality was 2.6% (2 of 77 patients). Both deaths occurred after carinal resection, for a procedure-specific mortality of 10.5% (2 of 19 patients). A patient with carcinoid tumor died 7 days after operation of respiratory insufficiency. Another patient with a mixed small cell and squamous cell carcinoma (also counted in Gaissert and associates [2]) died 102 days after operation of respiratory failure and heparin-induced thrombocytopenia. Postoperative complications are listed in Table 4.


View this table:
[in this window]
[in a new window]
  		Table 4. Complications
 
Reoperation was required in 7 patients. One patient needed reexploration for bleeding early after operation. Two of 77 patients (2.6%) underwent tracheal re-resection for anastomotic stricture occurring early after resection. A local airway recurrence was resected in 2 patients, in 1 patient after postoperative radiation for a spindle cell sarcoma; he later died with local and distant recurrence. An additional patient with spindle cell sarcoma required completion thyroidectomy after laryngotracheal resection. A second, more peripheral tumor in the bronchus intermedius of identical histologic appearance was resected in a patient with granular cell tumor.

Postoperative radiation was administered to 18 patients with malignant tumors. Fifteen patients received more than 45 Gy and 3 patients received 45 Gy or less.

Follow-Up
Mean follow-up was 9.7 ± 8.3 years. Follow-up was 84% complete. Resection was associated with improved survival. The rate of survival at 1, 5, and 10 years was 96%, 87%, and 75%, respectively, in patients undergoing resection and 73%, 30%, and 12%, respectively, without resection. As demonstrated in Table 5, benign tumors and low-grade malignancies had comparable long-term outcome, whereas high-grade malignant tumors demonstrated marked attrition of survival after resection and no long-term survivors without resection. Figure 1 depicts the survival curve of benign and malignant tumors.


View this table:
[in this window]
[in a new window]
  		Table 5. Survival Rates Among Uncommon Tracheal Tumors
 

Figure 1
View larger version (17K):
[in this window]
[in a new window]
  		Fig 1. Overall survival after resection or bronchoscopy of uncommon tumors. Error bars denote 95% confidence interval.

 
Recurrence was recorded in 10.8% of patients (8 of 74 patients). Recurrence was distant only in 4, local and distant in 2, and local and regional only in 1 patient each. Of 3 known local recurrences, 1 was noted above. Microscopically close margins were left deliberately in another patient after laryngotracheal resection of a low-grade chondrosarcoma arising from the posterior cricoid plate; a local recurrence is suspected 5 years later but the voice is not affected and laryngectomy is presently deferred. The only local recurrence of a presumed benign tumor happened 2 years after tracheal resection for a leiomyoma without mitoses. In this patient, a recurrent leiomyosarcoma required carinal resection and the patient died 10 years later of distant metastasis.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 References
 
Uncommon tumors of the trachea in 90 patients with 33 different histologic diagnoses were reviewed to emphasize similarities and differences in presentation and management. On the basis of our observations, these tumors may be grouped into five main types. Benign tumors display heterogeneous histologic appearance and do not recur after complete resection unless they transform into malignant tumors (1 observation). Carcinoid tumors, as elsewhere in the bronchial tree and lung, are low-grade malignancies that were not observed to progress or recur. Most mucoepidermoid carcinomas are localized and cured by resection, with early dissemination in a small proportion of highly malignant tumors. A conspicuous decrement in survival is noted after resection for both sarcoma and nonsquamous bronchogenic carcinoma and is more marked in the latter. Unresectable malignant tumors in our study were invariably fatal. Despite the wide range in malignant potential and a long symptomatic interval, 85% of all patients (77 of 90 patients) were candidates for surgical resection, which did not exclude any patient with unresectable disease or multiple lesions, ie, papilloma. Our results confirm other reports of uncommon tracheal tumors [4, 5, 10] and support an attitude that assumes resectability unless proven otherwise by endoscopic or radiographic evaluation, or after exploration.

Surgical resection should be offered to patients with benign tumors. As newer techniques for local tumor destruction become available, these will without doubt be applied to tracheal tumors, as have cryoablation [11], photodynamic therapy [12], laser [13], and brachytherapy [14]. Because these alternatives focus on restoring the airway lumen, rather than on complete resection, they should be reserved for isolated mucosal lesions in multiple sites, notably squamous papillomas. Most tumors, however, grow into or through the tracheal wall and can therefore not be completely excised by endoscopic techniques. Surgical risk cannot serve as justification for incomplete endoscopic resection even in benign tumors; medical contraindications did not preclude resection in any of our patients. Complete resection is compromised only by excessive length of tumor or extensive radial growth into adjacent soft tissue and organs. Carinal resection in malignant tumors continues to have a higher risk than standard tracheal procedures and remains a challenge when tumor length increases tension on the remaining airway. In all other patients, segmental airway resection for uncommon tracheal tumors is a low-risk procedure [9].


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
References
 
DR ROBERT J. KORST (New York, NY): I enjoyed that very much. Can you educate me on squamous papillomatosis of the trachea? I notice that a group of your patients you didn't resect, and I presume that's because it's like the patients that I've seen where it's all over the airway. If you have a local lesion, do you resect that, and if you do resect, is the disease cured; meaning it won't come back in other parts of the airway?

DR GAISSERT: We found squamous papilloma in multiple locations in 5 patients and in a solitary location in 4 patients and these 4 patients underwent resection, and so far we have not seen recurrences. We have treated multiple locations with laser, in a similar manner as you did, but all solitary lesion we have resected with good results.

DR KORST: Excellent. Thank you.

DR THOMAS J. WATSON (Rochester, NY): Henning, I really enjoyed the talk. Along similar lines, I'm a bit curious about your recommendation for resection of benign lesions. You reported on a number of benign lesions that were not resected, yet with 100% 10-year survival. And your last point was that alternative treatments, other than resection, must show equal or better results. I would argue that for benign lesions, non-resectional therapies yielded results that were equal or better. Can you comment on that, please?

DR GAISSERT: In benign tumors you still have the issue of airway obstruction, so the question is how do you deal with airway obstruction. You can locally destroy the tumor, but then you leave a tumor behind and you need to follow the tumor. The alternative is to resect the lesion and obviate further follow-up if you have performed a complete resection.

DR ROBERT J. CERFOLIO (Birmingham, AL): Just a quick question about the chin stitch. I know youR group has written to leave that in 7 or 8 days. We've used this as well, but have only left it for in place, if there is not much anastomotic tension for only 3 or 4 days. Have you shortened your time for the chin stitch, any tricks to having your patients and more importantly their family members tolerate it, and do you still use 7 days? Thanks.

DR GAISSERT: The chin stitch was not part of our database, so I cannot comment on the use in these patients. But it is meant to prevent neck extension. It is not meant to attach the chin to the chest. That would have rather deleterious results. I cannot recommend that at all. It is fairly well tolerated if it just prevents extension, and then we use it in any tracheal resection; however, usually not in carinal resection unless larger segments of trachea are resected at the same time. We have somewhat different practices, but these chin stitches stay in for about 6 to 7 days.

DR REZA J. MEHRAN (Houston, TX): I have one question about the slow-growing adenoid cystic carcinoma. Patients in your group with this histology with locoregional disease, meaning N2 disease, how did you treat them; neoadjuvant treatment followed by resection, resection followed by adjuvant treatment, or no resection at all? Thank you.

DR GAISSERT: This is an experience that extends over about 40 years, so there are patients with node-positive adenoid cystic carcinoma that we didn't know about before the operation, and we do not perform a radical lymphadenectomy as part of the procedure because we are concerned about the blood supply of the trachea. In a separate review of our experience in adenoid cystic carcinomas, we could not show a clear relationship between node-positive results and worse survival. We suspect that that is the case, and if we would find an adenoid cystic carcinoma with extensive lymphadenopathy, we would probably not operate. We would regard that as extensive regional disease and not operate.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 

  1. Manninen MP, Antila PJ, Pukander JS, Karma PH. Occurrence of tracheal carcinoma in Finland Acta Otolaryngol 1991;111:1162-1169.[Medline]
  2. Gaissert HA, Grillo HC, Shadmehr MB, et al. Long-term survival after resection of primary adenoid cystic and squamous cell carcinoma of the trachea and carina Ann Thorac Surg 2004;78:1889-1897.[Abstract/Free Full Text]
  3. Grillo HC. Tracheal tumorssurgical management. Ann Thorac Surg 1978;26:112-125.[Abstract]
  4. Perelman MI, Koroleva N, Birjukov J, Goudovsky L. Primary tracheal tumors Semin Thorac Cardiovasc Surg 1996;8:400-402.[Medline]
  5. Pearson FG, Todd TR, Cooper JD. Experience with primary neoplasms of the trachea and carina J Thorac Cardiovasc Surg 1984;88:511-518.[Abstract]
  6. Briselli M, Mark GJ, Grillo HC. Tracheal carcinoids Cancer 1978;42:2870-2879.[Medline]
  7. Tan-Liu NS, Matsubara O, Grillo HC, Mark EJ. Invasive fibrous tumor of the tracheobronchial treeclinical and pathologic study of seven cases. Hum Pathol 1989;20:180-184.[Medline]
  8. Heitmiller RF, Mathisen DJ, Ferry JA, Mark EJ, Grillo HC. Mucoepidermoid lung tumors Ann Thorac Surg 1989;47:394-399.[Abstract]
  9. Grillo HC. Surgical techniques Surgery of the trachea and bronchi. Hamilton, Ontario: BC Decker; 2004. pp. 499.
  10. Regnard JF, Fourquier P, Levasseur P, The French Society of Cardiovascular Surgery Results and prognostic factors in resections of primary tracheal tumorsa multicenter retrospective study. J Thorac Cardiovasc Surg 1996;111:808-813.[Abstract/Free Full Text]
  11. Marasso A, Gallo E, Massaglia GM, Onoscuri M, Bernardi V. Cryosurgery in bronchoscopic treatment of tracheobronchial stenosisindications, limits, personal experience. Chest 1993;103:472-474.[Abstract/Free Full Text]
  12. McCaughan Jr JS, Williams TE. Photodynamic therapy for endobronchial malignant diseasea prospective fourteen-year study. J Thorac Cardiovasc Surg 1997;114:940-946.[Abstract/Free Full Text]
  13. Shah H, Garbe L, Nussbaum E, Dumon JF, Chiodera PL, Cavaliere S. Benign tumors of the tracheobronchial treeendoscopic characteristics and role of laser resection. Chest 1995;107:1744-1751.[Abstract/Free Full Text]
  14. Harms W, Becker HD, Krempien R, Wannenmacher M. Contemporary role of modern brachytherapy techniques in the management of malignant thoracic tumors Semin Surg Oncol 2001;20:57-65.[Medline]



This article has been cited by other articles:


Home page
 ICVTSHome page
T. Krajc, M. Janik, R. Benej, M. Lucenic, I. Majer, J. Demian, and S. Harustiak
Urgent segmental resection as the primary strategy in management of benign tracheal stenosis. A single center experience in 164 consecutive cases
Interactive CardioVascular and Thoracic Surgery, December 1, 2009; 9(6): 983 - 989.
[Abstract] [Full Text] [PDF]

Home page
 ICVTSHome page
I. Cordos, C. Bolca, C. Paleru, R. Posea, and R. Stoica
Sixty tracheal resections - single center experience
Interactive CardioVascular and Thoracic Surgery, January 1, 2009; 8(1): 62 - 65.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
R. M. Terra, H. Minamoto, J. J.M. Junqueira, R. Falzoni, P. M. Pego-Fernandes, and F. B. Jatene
Tracheal Malignant Melanoma: Successful Outcome With Tracheal Resection
Ann. Thorac. Surg., July 1, 2008; 86(1): 308 - 310.
[Abstract] [Full Text] [PDF]

Home page
 Br. J. Radiol.Home page
S JAIN, J P AGARWAL, T GUPTA, P M PARIKH, R C MISTRY, H MENON, C S PRAMESH, and S K SHRIVASTAVA
Second primary small cell carcinoma of the trachea in a breast cancer survivor: a case report and literature review
Br. J. Radiol., April 1, 2008; 81(964): e120 - e122.
[Abstract] [Full Text] [PDF]

Home page
 NEJMHome page
K. E. Haver, C. J. Hartnick, D. P. Ryan, R. Shailam, and E. J. Mark
Case 10-2008 -- A 10-Year-Old Girl with Dyspnea on Exertion
N. Engl. J. Med., March 27, 2008; 358(13): 1382 - 1390.
[Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Henning A. Gaissert
Hermes C. Grillo
Cameron D. Wright
John C. Wain
Douglas J. Mathisen
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Gaissert, H. A.
Right arrow Articles by Mathisen, D. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Gaissert, H. A.
Right arrow Articles by Mathisen, D. J.
Related Collections
Right arrow Trachea and bronchi

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS