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Ann Thorac Surg 2005;80:295-298
© 2005 The Society of Thoracic Surgeons


Original article: General thoracic

Alternative Surgical Approaches for Apical Neurinomas: A Thoracoscopic Approach

Shunsuke Endo, MD*, Fumio Murayama, MD, Shin-ichi Otani, MD, Kenji Tetsuka, MD, Tsuyoshi Hasegawa, MD, Yukio Sato, MD, Yasunori Sohara, MD

Division of General Thoracic Surgery, Department of Surgery, Jichi Medical School, Minamikawachi-machi, Kawachi-gun, Tochigi, Japan

Accepted for publication February 1, 2005.

* Address reprint requests to Dr Endo, Jichi Medical School, Division of General Thoracic Surgery, Department of Surgery, Minamikawachi-machi, Kawachi-gun, Tochigi, 329-0498 Japan (Email: tcvshun{at}jichi.ac.jp).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Neural tumors at the thoracic apex present technical problems for surgeons because of their inaccessibility and postoperative neural complications. Although several approaches offering better accessibility have been proposed, none have become standard.

METHODS: Between 1976 and 2004, 23 patients, histologically 20 neurilemmomas and three ganglioneuromas, underwent surgical intervention for apical neurinoma. Surgical approaches were in three groups: (1) open thoracotomy, 8 patients; (2) transcervical, 10 patients; and (3) video-assisted thoracoscopy utilizing intracapsular enucleation to preserve important nerves and vessels, 5 patients. Perioperative variables and postoperative neurological complications were reviewed and compared among the groups.

RESULTS: Operation time and t blood loss in the vessels group were significantly less than in the other groups. Multivariate analysis with the perioperative variables showed the transcervical approach to be an independent predictor for postoperative neurologic complications (p = 0.0029). All patients remain free from recurrence, even in the follow-up period for patients in the vessels group ranging from 6 to 60 months (average, 35 months).

CONCLUSIONS: Video-assisted thoracoscopic intracapsular enucleation, when an apical neurinoma is benign and well-capsulated, is the optimal treatment to preserve nerve function. Careful follow-up to monitor for recurrence is necessary.


    Introduction
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Neurogenic mediastinal tumors occurring in adults are generally benign lesions, except in patients with Von Recklinghausen’s disease [1]; their favorable oncological behavior makes neurogenic tumors ideal candidates for resection by video-assisted thoracoscopy. Treatment by thoracoscopic surgery has been widely accepted since the first report by Landreneau and colleagues [2] in 1992. Usual contraindications to this procedure are the dimension of the tumor (greater than 6cm), position (apex and cardio-diaphragmatic angle), and the presence of an intraspinal growth (dumbbell-shaped tumor) [3, 4]. The rare condition of apical neurinoma at the thorax presents technical problems for surgeons because of inaccessibility. The standard approach to provide better accessibility to the apex remains controversial because of the limited exposure of the vascular and neural structures in the thoracic inlet.

This study aims to clarify an optimal surgical approach for benign apical neurogenic tumors by reviewing the experience of our institution in which the surgical approach has alternated from median and lateral thoracotomy to cervicotomy, then to video-assisted thoracoscopy.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Patients
From 1976 to 2004, 23 patients (12 female and 11 males), ages 20 to 70 years (median 45 years) with benign neurogenic tumors of the thoracic apex were treated in our institute (Table 1). Seventeen tumors, 15 right-sided and eight left-sided, were discovered on routine chest roentgenogram. Six patients had symptoms (3 with shoulder pain and 3 with bronchial irritability due to tracheal compression).


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Table 1. Patient Characteristics
 
Alternation of Surgical Approaches
Until 1998, surgical intervention through a transcervical incision was attempted when feasible (Fig 1). Tumor resection was performed through an ipsilateral collar incision by division or retraction of the ipsilateral sternocleidomastoideus muscle. Otherwise, tumor resection was performed through a median sternotomy or lateral thoracotomy. In both approaches, the tumor was excised after division of a few rami without interruption of the originating nerve, except 1 patient who underwent complete division of the superior intercostal nerve, and in another who underwent intracapsular enucleation due to inaccessibility. Since 1999, intracapsular enucleation through video-assisted thoracoscopy was attempted when the tumor was well-capsulated. Patients were placed in a lateral position. Three access ports were established on the 4th intercostal space at the mid-clavicular line and on the 3rd intercostal spaces at the anterior-auxiliary and posterior-auxiliary lines, respectively. While the superior vena cava was retracted ventrally with a spatula through the ventral port to widen the apical space, the capsule of the tumor was opened with an electrical or harmonic scalpel if the bleeding was easy. After identification of an adequate plane, the tumor was then carefully dissected from the capsule without division of any rami (Fig 2). As much of the capsule as possible would be removed to avoid recurrences and to preserve the function of the originating nerve.



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Fig 1. Time distributions with the three surgical approaches (OT = open thoracotomy; TC = transcervicotomy; VT = video-assisted thoracoscopy).

 


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Fig 2. Thoracoscopic intracapsular enucleation for right apical neurilemmoma.

 
Stratification of Surgical Approaches
There were three groups of surgical approaches: (1) 8 patients underwent open thoracotomy (OT) tumor resection, 5 patients through a lateral thoracotomy and 3 through a median sternotomy; (2) 10 patients underwent transcervical (TC) tumor resection, 9 patients through an intracapsular enucleation and 1 through an ipsilateral collar incision; and (3) 5 patients underwent a video-assisted thoracoscopy (VT) through a thoracoscopic intracapsular enucleation. The originating nerves of the tumors were superior intercostal nerves in 9, sympathetic in 13, and vagus in 1. The greatest widths of all tumors ranged from 2.5 cm to 12.5 cm (median, 4 cm); in the OT group from 3 to 12.5 cm (average diameter, 6.6 cm), in the TC group from 2.5 to 6 cm (average diameter, 4.0 cm), and in the VT group from 2.5 to 3.5 cm (average diameter, 2.6cm).

Pathologic examination showed neurilemmoma in 20 patients and ganglioneuroma in 3. Each surgical approach group had 1 patient with ganglioneuroma (Table 1).

Data Analysis
Data were obtained by thorough reviews of the hospital’s and the physicians’ inpatient and outpatient records at the end of 2004. For analysis of differences in continuous variables such as operation time and the amount of operative blood loss between the groups, Student’s t test were used. To identify an independent predictor for postoperative neurologic complications, multivariate analyses was performed by forward stepwise logistic regression with the following perioperative variables: age (≥ 45 years vs < 45 years), histology (neurilemmoma vs others), origin (autonomous nerve vs others), presence of tumor-related symptom, tumor location (right vs left), tumor size (< 4 cm vs ≥ 4 cm), surgical approach (TC vs others), operation time (≤ 150 min vs > 150 min), and amount of operative blood loss (≤ 70 mL vs > 70 mL). A p value < 0.05 was considered significant.


    Results
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 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Operation Time and the Amount of Operative Blood Loss
Operation times ranged from 60 to 280 minutes (median, 150 minutes); group times were significantly shorter than in the OT (p = 0.0018) and TC (p = 0.0054) groups than in the VT (Fig 3A). The amounts of operative blood loss ranged from 20 to 670 mL (median 70 mL); losses were significantly larger in the OT group than in the VT group (p = 0.0016) and TC group (p < 0.0001) (Fig 3B).



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Fig 3. (A) Operation time and (B) the amount of operative blood loss in each group. Data are expressed as mean ± standard deviation. Student’s t test shows a significant difference as indicated by the asterisk (*). (OT = open thoracotomy; TC = transcervicotomy; VT = video-assisted thoracoscopy.)

 
Postoperative Neurologic Complications
Three of 8 patients in the OT group, 9 of 10 in the TC group, and 1 of 5 in the VT group had postoperative neurologic complications; 6 had Horner’s syndrome, 4 had phrenic nerve paralysis, 4 had ulnar neuralgia, and 1 had vocal cord palasia (Table 1). All resumed full daily activities; 1 from the OT group for 13 years suffered continuously from ulnar neuralgia due to the complete division of the superior intercostal nerve. Multivariate analysis with perioperative variables showed the transcervical approach to be an independent predictor for postoperative neurological complications (p = 0.0029).

Recurrence
On follow-up, all patients remain well and free from recurrence, even with the follow-up period of patients in the VT group ranging from 6 to 60 months (average, 35).


    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Neurogenic mediastinal tumors occurring in adults are generally benign neurilemmoma originating from Schwann cells. Benign apical neurologic tumors are rare for this condition, originating most commonly from the sympathetic chain and the brachial plexus. These tumors have always presented particular technical problems for surgeons because of their close association with important vascular and neural structures at the root of the neck, along with their inaccessibility through lateral thoracotomy [5]. Although various alternative approaches have been proposed, none has become the standard procedure. This study reported retrospective analysis associated with postoperative neurologic complications in relation to various surgical approaches based on a fairly large series of cases seen in our institute. Until the early 1980s, the standard approach was to use an open thoracotomy through a median sternotomy or lateral thoracotomy. When dealing with benign diseases, the functional and cosmetic results after such an aggressive approach could not be justified [5]. Thereafter, the transcervical approach, though technically demanding was utilized when feasible. When tumors were well-capsulated, intracapsular enucleation was available. Our results showed the transcervical approach to have a high rate of postoperative neurologic complications compared with open thoracotomy as well as video thoracoscopy, even though tumor size in the TC group was smaller than in the OT group. Even patients who underwent intracapsular enucleation in the TC group had postoperative neurologic complications. Palasia of the phrenic nerve, not being the originating nerve, occurred in 4 of 10 patients in the TC group. These results may be due not just to damage caused by the nerve of origin during the surgical procedure, but could also be due to excessive distension of several neural networks during the transcervicotomy procedure. In the transcervical approach, mini-sternotomy [5], clavicular resection [6], manubrial resection [7], or thoracoscopic assist [8] is additionally necessary for better accessibility without excessive distension.

Recently smaller, less symptomatic benign neurogenic mediastinal tumors than before have been discovered in routine computed tomography and magnetic resonance imaging of thoracic diseases; thus thoracoscopic techniques are more in demand [9, 10]. In the past, total resection of a tumor, including the originating nerve fiber, was performed to prevent tumor recurrence [11]; in most cases, recovery of neural function was not satisfactory. However, now more emphasis is directed toward the benign nature, the excisability, and the infrequence of recurrence for these neoplasms [12]. Benign neurilemmomas are well encapsulated and individual fibers of the originating nerve are splayed over the surface of the neurilemmoma within a discrete capsule but not in the mass itself. For management, intracapsular enucleation is often performed in an effort to preserve nerve function [13–15]. As much of the capsule as possible should be removed to avoid recurrence. However, neurofibromas, likely now to be managed by enucleation should be carefully approached. Preoperative diagnosis using magnetic resonance imaging to differentiate neurofibromas from neurilemmomas should be utilized to select the appropriate surgical approach [16]. This procedure for removing the capsule does not demand techniques that should cause any anxiety about damage to important vascular systems and nerves, in particular the nerve of origin. Our results for this procedure showed not only less operating time and operative blood loss, but also less excessive distention of the neural network at the thoracic apex than with the other approaches. Even though the largest tumor was 3.5 cm in its greatest width in the VT group, much larger tumors can be enucleated through thoracoscopic techniques if the tumor is well-encapsulated. Tumors rarely recur after intracapsular enucleation for neurilemmomas originating from the vagus nerve [13]. If a tumor does recur, discovered on a program of careful follow-up, redo surgery through a transcervical approach, with or without the thoracic technique, can be performed.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Hajdu SI. Peripheral nerve sheath tumorsHistogenesis, classification and prognosis. Cancer 1993;72:3549-3552.[Medline]
  2. Landreneau RJ, Dowling RD, Ferson PF. Thoracoscopic resection of a posterior mediastinal neurogenic tumor Chest 1992;102:1288-1290.[Abstract/Free Full Text]
  3. Lui HP, Yim AP, Wan J, et al. Thoracoscopic removal of intrathoracic neurogenic tumorsa combined Chinese experience. Ann Surg 2000;232:187-190.[Medline]
  4. Venissac N, Leo F, Hofman P, Paquis P, Mouroux J. Mediastinal neurogenic tumors and video-assisted thoracoscopyalways the right choices?. Surg Laparosc Endosc Percutan Tech 2004;14:20-22.[Medline]
  5. Ladas G, Rhys-Evans PH, Goldstraw P. Anterior cervical-transsternal approach for resection of benign tumors at the thoracic inlet Ann Thorac Surg 1999;67:785-789.[Abstract/Free Full Text]
  6. Macchiarini P, Dartevelle P, Chapelier A, et al. Technique for resecting primary and metastatic nonbronchogenic tumors of the thoracic outlet Ann Thorac Surg 1993;55:611-618.[Abstract]
  7. Grunenwald D, Spaggiari L. Transmanubrial osteomuscukar sparing approach for apical chest tumors Ann Thorac Surg 1997;63:563-566.[Abstract/Free Full Text]
  8. Akashi A, Ohashi S, Yoden Y, et al. Thoracoscopic surgery combined with a supraclavicular approach for removing superior mediastinal tumor Surg Endosc 1997;11:74-76.[Medline]
  9. Riquet M, Mouroux J, Pons F, et al. Videothoracoscopic excision of thoracic neurogenic tumors Ann Thorac Surg 1995;60:943-946.[Abstract/Free Full Text]
  10. Bousamura M, Haasler GB, Patterson GA, Roper CL. A comparative study of thoracoscopic vs open removal of benign neurogenic mediastinal tumors Chest 1996;109:1461-1465.[Abstract/Free Full Text]
  11. Shields T. Primary lesions of the mediastinum and their investigation and treatmentIn: Shields TW, editor. General thoracic surgery. Philadelphia: Williams & Wilkins; 1994. pp. 1724-1769.
  12. Katz AD, Passy V, Kaplan L. Neurogenic neoplasma of major nerves of face and neck Arch Surg 1971;103:51-56.[Abstract/Free Full Text]
  13. Park CS, Suh KW, Kim CK. Neurilemmomas of the cervical vagus nerve Head & Neck 1991;13:439-441.[Medline]
  14. Gilmer-Hill HS, Kline DG. Neurogenic tumors of the cervical vagus nervereport of four cases and review of the literature. Neurosurgery 2000;46:1498-1503.[Medline]
  15. Fujino K, Shinohara K, Aoki M, et al. Intracapsular enucleation of vagus nerve-originated tumors for preservation of neural function Otolaryng Head Neck 2000;123:334-336.
  16. Jee WH, Oh SN, McCauley T. Extracranial neurofibromas versus neurilemmomasdiscrimination with MRI. AJR 2004;183:629-633.[Abstract/Free Full Text]



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Surgical treatment of benign neurogenic tumours of the mediastinum: a single institution report
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