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Ann Thorac Surg 2000;69:1537-1541
© 2000 The Society of Thoracic Surgeons

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Original articles: General thoracic

Thoracoscopic thymectomy in autoimmune myasthenia: results of left-sided approach

^a Departments of Department of Thoracic Surgery, Tor Vergata University, Rome, Italy
^b Department of Neurology, Tor Vergata University, Rome, Italy
^c Department of Thoracic Surgery, Catholic University, Leuven, Belgium

Address reprint requests to Dr Mineo, Cattedra di Chirurgia Toracica, Università degli Studi Tor Vergata, Piazza delle Umanesimo, 10, 00144 Roma, Italy
e-mail: mineo{at}med.uniroma2.it

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. We undertook to analyze the results of video-assisted thoracoscopic thymectomy through a left-sided approach in patients with autoimmune myasthenia.

Methods. Between 1993 and 1997, 31 patients underwent thoracoscopic thymectomy by a uniform left-sided approach. There were 8 men and 23 women with a mean age of 34 ± 12 years.

Results. Preoperative duration of disease was 14.8 ± 11 months. There were no operative deaths or major complications. The mean hospital stay was 5.2 ± 2.8 days. Mean follow-up was 39.6 ± 15 months and was 100% complete. At 48 months, remission and improvement rates were 36% and 96%, respectively. Shorter duration of symptoms (< 12 months) correlated with improved outcome (13 of 13 patients versus 10 of 14 patients; p = 0.036). Age, sex, Osserman class, corticosteroid therapy, presence of ectopic thymic tissue, and temporary postoperative symptom increase (deterioration) did not affect outcome.

Conclusions. Thoracoscopic thymectomy facilitated the goal of early thymectomy. Through a left-sided approach, improvement or remission was achieved in more than 95% of the patients. Thoracoscopic thymectomy should be considered a valid less invasive alternative to the most radical open approaches.

	Introduction

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Autoimmune myasthenia is a chronic disorder affecting postsynaptic acetylcholine receptors that causes fluctuating weakness and fatigue of striated muscles. In the integrated management of myasthenia, thymectomy is recognized as effective surgical therapy [1], but the optimal surgical approach remains controversial [2]. The beneficial effect of thymectomy is thought to be maximized by the removal of all thymic tissue, including ectopic thymic tissue found in mediastinal and cervical fat [3–5]. Total or partial sternotomy and the transcervical or the combined transcervical-transsternal approach have been widely used. Symptomatic improvement or remission has been achieved in many patients with these different surgical modalities [3–7].

Video-assisted thoracoscopic surgery (VATS) has recently been successfully used for thymectomy through either a left- [8, 9] or right-sided [10] approach. We know of only one multicenter study presenting outcomes of VATS thymectomy [11] in patients having operation with either a left-sided or right-sided approach. However, variation in surgical details that can significantly affect the final outcome of the procedure is one of the potential shortcomings of multicenter studies. To date, the role of VATS thymectomy is still investigational, and many surgeons remain skeptical of the value of this recent option [12]. Our aim was to analyze the surgical and clinical results of VATS thymectomy performed through a uniform left-sided approach at two European universities.

	Material and methods

Top Abstract Introduction Material and methods Results Comment References

 
Between January 1993 and December 1997, 31 patients (8 men and 23 women) with autoimmune myasthenia (AM) underwent VATS thymectomy at two participating institutions (Tor Vergata University in Rome, Italy, and Catholic University in Leuven, Belgium). The thoracic surgeons at each institution had gained experience with various major thoracoscopic procedures before embarking on the study. Informed consent was obtained from all patients, who were given the basic information on the different approaches and the potential complications. The diagnosis of AM was based on clinical features and one or more of the following factors: response to edrophonium chloride, results of electromyography, and demonstration of circulating antibodies directed against the acetylcholine receptor. Preoperative diagnostic tests included spirometry and computed tomographic scanning in all patients and magnetic resonance imaging in select patients.

Inclusion criteria, surgical technique, and preoperative and postoperative medical management were discussed at the beginning of the program and were uniformly applied at both participating institutions. Inclusion criteria were a diagnosis of nonthymomatous AM irrespective of the severity of symptoms. Patients with thymomatous myasthenia were included if the tumor was less than 3 cm in maximal size with no signs of invasiveness by computed tomography and magnetic resonance imaging. Only patients with a minimum of 12 months of follow-up were included in the study, and no patient was lost to follow-up.

The therapeutic effect of thymectomy was established by comparing the preoperative clinical status with the status recorded every 6 months postoperatively. Staging before operation and at follow-up clinics was done with a modified Osserman (13) classification (Table 1). Postoperative clinical status was rated on the basis of four responses that took into account changes in both symptoms and medication requirements (Table 2). Patients with severe symptoms (modified Osserman class 4), who were considered at risk for postoperative respiratory failure, underwent plasma exchange prior to operation. Anticholinesterase drugs were given as needed before and after the surgical procedure, whereas, steroid treatment was avoided preoperatively whenever feasible.

Surgical technique
The surgical technique has been described previously in detail [8]. Thymectomy was always performed with the patient under general anesthesia with double-lumen tube placement and lying in a 45-degree off-center position. Four flexible trocars were inserted into the left hemithorax. The procedure routinely included removal of the entire gland and all mediastinal perithymic tissue including fatty tissue in the aortocaval groove, the aortopulmonary window, both cardiophrenic sinuses, and the lower cervical area (Fig 1). During the operation, the lung was periodically reventilated, and bronchial secretions were aspirated to reduce the risk of postoperative atelectasis. At the completion of thymectomy, the specimen was extracted through an endo-bag, and a drainage tube was placed in the anterior mediastinum.

View larger version (89K): [in this window] [in a new window]   Fig 1. Potential sites of ectopic thymic tissue that are routinely dissected through left-sided thoracoscopic approach: 1 = thymic gland; 2 = pretracheal fat; 3 = under phrenic nerves; 4 = Behind innominate vein; 5 = aortopulmonary window; 6 = aortocaval groove; 7 = anterior mediastinal fat; 8 = cardiophrenic fat.

	Results

Top Abstract Introduction Material and methods Results Comment References

 
Patient age ranged from 20 to 69 years with a mean of 34 ± 12 years. The preoperative mean Osserman class was 2.16 ± 0.7; 6 patients were in class 1, 13 in class 2, 10 in class 3, and 2 in class 4. The duration of symptoms ranged from 1 month to 46 months with a mean of 14.8 ± 11 months. Preoperatively, pyridostigmine bromide alone was used in 23 patients (74%), and corticosteroids were used in 8 patients (26%), either alone (1 patient) or in association with pyridostigmine (7 patients).

Surgical results
Conversion to median sternotomy was required in 1 patient (3.2%) because of difficulty in dissecting the thymus. The patient was 69 years old and had received high doses of corticosteroids. The mean operative time was 148 ± 46 minutes. Operative time was significantly longer in patients aged more than 40 years (165 ± 64 minutes versus 143 ± 40 minutes; p = 0.04). All patients were extubated within 2 hours after the operation.

There were no operative deaths. One patient sustained a myasthenic crisis that occurred on postoperative day 2 and required reintubation and mechanical ventilation. Plasmapheresis was then started (five cycles), and the patient was successfuly weaned from the ventilator on postoperative day 8 without further complications. No patient had phrenic or recurrent nerve injury, and no patient had development of atelectasis or pneumonia postoperatively.

Pathologic examination revealed the following: normal thymus in 14 patients; thymic hyperplasia in 9; atrophied thymus in 4; and thymoma (maximal size range, 1.5 to 3 cm) in 4. Ectopic thymic tissue was found in 10 patients (32.3%); it was macroscopic in 3 patients and microscopic in 7. This tissue was located within the anterior mediastinal fat in 5 patients, in the aortopulmonary window in 3, and in the pretracheal fat or cardiophrenic fat on the left side in 2 patients each. In 2 patients, ectopic thymic tissue was found in two distinct locations. The results of computed tomography before operation in 1 patient with thymoma were considered negative, and the tumor (1.5 cm in size) was discovered incidentally at the pathologic examination. By the classification of Masaoka and colleagues, two thymomas were stage I and 2, stage IIa. Hospital stay ranged from 2 to 16 days with a mean of 5.2 ± 2.8 days.

The cosmetic effect was rated excellent by 26 patients (86.7%) and good by 4 patients (13.3%). Two patients (6.5%) had thoracic pain (score < 5) at 6 months, which was easily controlled by oral analgesics. In both, the pain resolved completely within the first postoperative year.

Clinical results
Follow-up ranged from 16 to 75 months with a mean of 39.6 ± 15 months. At follow-up clinics, all patients were evaluated at 12 months, 28 patients at 24 months, 19 at 36 months, and 10 at 48 months. Mean Osserman class improved greatly with time (Fig 2). A significant improvement in symptom score was evident at 12 months compared with the preoperative status (mean symptom scores, 1.2 ± 0.9 versus 2.2 ± 0.8, respectively; p < 0.0009) and again at 24 months compared with the 12 months’ score (mean scores, 0.8 ± 0.8 versus 1.2 ± 0.9, respectively; p = 0.0001). No significant difference was found in symptom score at subsequent follow-up intervals. Remission and improvement rates are illustrated in Figure 3. The improvement rate was 59% at 12 months and increased to 96% at 36 and 48 months. The remission rate increased more slowly and more regularly over time, ranging from 13% at 12 months to 36% at 48 months.

View larger version (15K): [in this window] [in a new window]   Fig 2. Mean Osserman scores [13] before and after operation. The difference between the preoperative and 12-month scores was significant, as was the difference between the 12-month and 24-month scores.

View larger version (18K): [in this window] [in a new window]   Fig 3. Improvement and remission rates in patients with autoimmune myasthenia.

Univariate analysis of factors potentially affecting outcome revealed no significant association between improvement rate at 24 months and sex, age, histology (thymomatous versus nonthymomatous AM), preoperative modified Osserman class, preoperative use of corticosteroids, presence of ectopic thymic tissue, and temporary postoperative deterioration. On the other hand, shorter duration of disease (< 12 months) correlated significantly with improved outcome at 24 months (13 of 13 patients versus 10 of 14 patients; p = 0.036). Because of the small number of patients, multivariate analysis of factors was not performed.

	Comment

Top Abstract Introduction Material and methods Results Comment References

 
Video-assisted thoracoscopic surgery has provided a new approach for the surgical removal of the thymus. Proponents of VATS thymectomy believe that it combines the minimal surgical trauma of the transcervical approach and the excellent visualization of the anterior mediastinum of the transsternal approach. Also, VATS does not prevent easy access to the lower cervical area, thereby allowing complete removal of the superior thymic horns [8–11]. Recognized advantages of VATS over open approaches are the cosmetically acceptable incisions and the enhanced magnification.

Yim and colleagues [10] first proposed a right-sided approach for VATS thymectomy. Advocates of this approach maintain that it allows greater maneuverability of instruments in the wider right pleural cavity and easier identification of the left innominate vein because the superior vena cava serves as a landmark [11]. In a previous report, we [8] described the surgical details of our left-sided approach as well as the advantages of performing adjuvant pneumomediastinum to facilitate the dissection of both the thymus and the perithymic fatty tissue. Although we agree that the thymus can be safely approached by VATS from either side, we prefer access from the left. We believe that from the left, the dissection maneuvers are safer because the superior vena cava lies out of the surgical field, thus reducing the risk of an incidental lesion to this vessel. Moreover, we carried out extensive removal of the perithymic fatty tissue, which in our experience is prevalent in the left pericardiophrenic angle and in the aortopulmonary window. We consider this step essential to achieve intentional extended thymectomy. In our experience, the only limitation of the left-sided approach relates to the presence of cardiomegaly which can limit exposure of the thymus [8].

In this series, the mean duration of disease was 14.8 months. This compares favorably with the range of 23 to 49 months’ duration in other reports on transcervical and transsternal thymectomy [3–7]. We speculate that VATS thymectomy has been more easily and more rapidly accepted by both neurologists and young female patients because of its superior cosmetic results.

It is worthy of note that a longer operative time was recorded in patients aged more than 40 years. A possible explanation is that in this series, older patients (7 patients) usually were fatter than younger patients and had a greater amount of perithymic fatty tissue. Moreover, 3 of these patients had received steroids preoperatively, which also might have increased the amount of perithymic fatty tissue.

There was no mortality or major morbidity in this series. Our results are similar to those of Mack and colleagues [11] and compare favorably with the 33% rate of morbidity reported by Bulkley and colleagues [5] with aggressive transsternal thymectomy. Thoracoscopic thymectomy has been implicated as a potential cause of chronic thoracic pain [15]. Our data show that 6.5% of patients reported minimal pain at the 6-month follow-up, and no patient had pain at subsequent follow-up visits. Routine use of flexible trocars and 5-mm instruments and taking care not to place trocars posterior to the midaxillary line where intercostal spaces are narrower are factors that may have contributed to limiting the occurrence of chronic thoracic pain.

Anatomic studies [16, 17] have shown that islets of ectopic thymic tissue can be present in mediastinal and cervical fat. Thus, the extended transsternal approach and the transcervical-transsternal approach have been advocated to maximize the completeness of thymectomy and improve results. Other surgeons [6, 7] prefer the less invasive transcervical approach because they believe that it also allows performance of a complete thymectomy. Bril and colleagues [18] recently reported an excellent long-term remission rate (45%) with the improved transcervical thymectomy advocated by Cooper and associates [6]. One of us (T.C.M.) [19] also has used the transcervical approach in the past. With this approach, remission was achieved in 30.7% of 26 patients at 10 years of follow-up. Moreover, we [20] recently found residual thymic tissue at completion VATS thymectomy in patients who did not benefit from initial transcervical thymectomy. We now consider VATS superior to the transcervical approach because it permits wider visualization of the thymic area and avoids the crowding of instruments through the narrow cervical access [8, 10].

In this series, overall improvement and remission rates at 48 months were 96% and 36%, respectively. With reference to remission rate only, which is the best measure of comparison with other series, our result is similar to that achieved with the transcervical [18] or the transcervical-transsternal [3] approach at the same length of follow-up. It compares favorably with the 19% rate reported by Mack and coworkers [11] using VATS thymectomy. This latter difference could be due either to our longer follow-up (mean follow-up, 39.6 versus 23 months) or to the fact that through the left-sided approach, we were able to perform a more extended resection of the perithymic fatty tissue, thus improving the completeness of thymectomy.

Numerous variables including shorter duration of symptoms, female sex, limited disease, and thymic hyperplasia have been described as prognostic factors predictive of a positive response to thymectomy. Ectopic thymic tissue was considered an unfavorable prognostic factor by Ashour [21], who hypothesized that it might indicate the presence of additional ectopic sites inaccessible through even the transcervical-transsternal approach. Though the numbers are small, data from our series suggest that shorter duration of disease is a positive prognostic factor, whereas presence of ectopic thymic tissue, age, sex, histology, preoperative corticosteroid use, and temporary postoperative deterioration do not affect outcome. Also, we found no difference when comparing the results of patients with ocular or generalized AM. Nakamura and colleagues [22] reported in 1996 that results were better in class I patients when duration of disease was 12 months or less. In our series, all patients in class I had a similar short duration of disease, which may explain the high rate of remission (33%) in this subgroup. These data support the hypothesis that the earlier the thymectomy, the better the outcome, independent of preoperative severity of symptoms.

There are several reliable approaches that allow thymectomy to be accomplished on the basis of different philosophies. However, it seems logical to assume that a less invasive but still radical approach is desirable and may facilitate the goal of early thymectomy. Our data indicate that VATS thymectomy is readily accepted by the patients. The left-sided approach allows an extended resection of potential sites of ectopic thymic tissue including the aortopulmonary window and the left pericardiophrenic angle, which are difficult if not impossible to reach from the right hemithorax. The morbidity in this series was negligible, and sustained improvement or remission was achieved in more than 95% of patients. In conclusion we believe that VATS thymectomy should be considered a valid alternative to the established approaches aimed at achieving a "curative thymectomy" in patients with AM.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Tommaso C. Mineo Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Mineo, T. C. Articles by Nofroni, I. Search for Related Content PubMed PubMed Citation Articles by Mineo, T. C. Articles by Nofroni, I.