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Ann Thorac Surg 2009;87:385-391. doi:10.1016/j.athoracsur.2008.11.040
© 2009 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Comparative Clinical Outcomes of Thymectomy for Myasthenia Gravis Performed by Extended Transsternal and Minimally Invasive Approaches

Dan M. Meyer, MDa,*, Morley A. Herbert, PhDc, Nasin C. Sobhania, Paul Tavakoliane, Andrea Duncan, RNa, Michelle Bruns, MLAe, Kevin Korngut, BSe, Janet Williams, BAe, Syma L. Prince, RN, BSNe, L. Huber, RN, BSNa, Gil I. Wolfe, MDb, Michael J. Mack, MDd

a Department of Thoracic and Cardiovascular Surgery, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas
b Department of Neurology, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas
c Department of Clinical Research, University of Texas Southwestern Medical Center at Dallas, Dallas, Texas
d Medical City Dallas Hospital, Dallas, Texas
e Cardiopulmonary Research Science and Technology Institute, Dallas, Texas

Accepted for publication November 17, 2008.

* Address correspondence to Dr Meyer, Department of Thoracic and Cardiovascular Surgery, University of Texas Southwestern Medical Center at Dallas, 5939 Harry Hines Blvd., 9th Floor, Suite 935, Dallas, TX 75390-8879 (Email: danm.meyer{at}utsouthwestern.edu).

Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
Background: Both transsternal and video-assisted thoracoscopic surgery (VATS) approaches are used for thymectomy in myasthenia gravis. We compared outcomes of simultaneous experiences in two institutions: one utilizing the transsternal approach exclusively, the other using VATS procedures for all patients. The Myasthenia Gravis Foundation of America guidelines were used to standardize reporting.

Methods: Between March 1992 and September 2006, 95 thymectomies were performed for myasthenia gravis; 48 by VATS and 47 by transsternal approach. Preoperative classification and postoperative disease status were compared between the groups.

Results: Mean age was 39.8 ± 14.9 (VATS) versus 34.4 ± 13.2 years (transsternal) (p = 0.07); the proportion of females was 52% versus 67% (p = 0.15); and preoperative duration of myasthenia gravis was 27 ± 44 versus 20 ± 45 months (p = 0.43), respectively. Clinical follow up was 89.5% complete at a mean of 6.0 ± 4.0 years and 4.3 ± 2.9 years (p = 0.03). The operative time was 128 ± 34 minutes (VATS) versus 119 ± 27 minutes (transsternal) (p = 0.22). The need for postoperative ventilation was 4.2% versus 16.2% (p = 0.07) and mean length of stay was 1.9 ± 2.6 versus 4.6 ± 4.2 days (p < 0.001). Thymomas were found in 8.3% of VATS versus 13.3% of transsternal patients (p = 0.44). No myasthenia gravis related deaths occurred and 95.8% of the VATS and 97.9% of the transsternal patients were in either complete stable remission, pharmacologic remission, or minimal manifestations status. In the VATS group, 13 of 17 (76.5%) patients stopped prednisone usage after surgery versus 5 of 14 (35.7%) in the transsternal group (p = 0.022).

Conclusions: Thymectomy is an effective treatment in patients with myasthenia gravis with equivalent clinical outcomes obtained by either approach.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 References
 
Myasthenia gravis is the most common primary disorder of neuromuscular transmission. Treatment of myasthenia gravis involves both medical and surgical options. However, surgical management has been a mainstay in the treatment of this autoimmune disorder since Blalock performed a transsternal thymectomy in 1939 [1]. Since that time thymectomy has been a standard component in the treatment of all stages of myasthenia gravis [2, 3]. One of several controversies regarding the role of thymectomy in myasthenia gravis management has revolved around which operative procedure produces an adequate thymectomy while minimizing adverse outcomes and facilitating patient recovery from the procedure. Options have included the classic transsternal approach, the transcervical method, the combined transcervical-transsternal maximum thymectomy, and most recently, the video-assisted thymectomy (VATS) [4, 5]. Proponents of both the transsternal [6] and the maximum thymectomy [7] cite the importance of surgical removal of all accessible anterior mediastinal adipose tissue along with the thymus gland because of concern over the presence of thymic rest cells in that tissue. Randomized studies comparing medical versus surgical management of myasthenia gravis have yet to be completed, and comparisons between different surgical techniques have similarly not been performed. With the improved methods of classifying patient disease status using the Myasthenia Gravis Foundation of America (MGFA) classification system (Table 1) [8], this most current and detailed disease grading system for myasthenia gravis may allow more accurate comparisons between patient groups.


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  		Table 1 Myasthenia Gravis Foundation of America Clinical Classification
 
In this study, we compared the outcomes of the two distinctly different operative techniques in the management of myasthenia gravis, extended-transsternal thymectomy, and video-assisted (VATS) thymectomy. The question as to whether a more extensive resection of the mediastinal adipose tissue, as is performed with the extended transsternal approach, yields different remissions rates as compared with the less invasive and less extensive VATS approach. Outcome variables such as disease remission, postoperative medication requirements, and perioperative parameters will be compared. The results of the simultaneous experiences of two institutions, one exclusively performing VATS, the other the transsternal approach, were reviewed.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 References
 
The study was carried out at University of Texas Southwestern Medical Center at Dallas and Medical City Dallas Hospital with a retrospective chart review of all cases done from March 1992 to June 2006. Preoperative clinical staging was assessed by the MGFA clinical classification [8]. Medication usage and existing comorbidities were also recorded. Patient follow-up was by clinical appointment visits as well as by scripted telephone contact and included information as to patient status as assessed by the MGFA postintervention status classification [8]. Current medication profiles were also recorded. Institutional Review Board approval was obtained at both centers. The studies were classified as exempt.

Surgical Technique
Surgical technique involved either the transsternal or thoracoscopic (VATS) approaches. The transsternal technique involved a complete sternotomy accomplished through a limited skin incision. Dissection involved mobilization of anterior mediastinal fat from the diaphragm to the level of the thymus gland, often entering the pleura bilaterally. The thymus is removed en bloc with the mediastinal fat and included full removal of the cervical horns with the associated adipose tissue. Both phrenic nerves are visualized, comprising the lateral extent of the dissection, and the thymic drainage to the innominate vein is ligated and divided. Patients are typically extubated in the operating room.

The VATS technique has been previously described [5, 9]. Using single lung ventilation with carbon dioxide insufflation, four right-sided thoracoscopic ports (3 to 10 mm and 1 to 5 mm) are placed (Fig 1). Visualization is through a 30 degree, 5 mm thoracoscope placed through the most posterior port. Dissection is begun with a hook cautery along and anterior to the right phrenic nerve. A triangular field of resection is created by dissection caudal along the pericardium and anteriorly along the retrosternum. Using an endoscopic Kittner for blunt dissection, all anterior mediastinal tissue is swept cephalad. The innominate vein is located at the junction with the superior vena cava, and dissection continued until the thymic vein is located; this is then doubly clipped. The positive pressure from carbon dioxide insufflation serves to open up the cervical area cephalad to the innominate vein allowing dissection of the superior poles of the gland. The dissection is completed by dissection along the left pleura which is performed bluntly to avoid injury to the left phrenic nerve. The resected specimen is then placed in an endoscopic pouch and extracted through the 10 mm port site. A complete resection of all anterior mediastinal tissue including the pericardiophrenic fat pads is performed. Carbon dioxide is evacuated from the thoracic cavity and no thoracic drainage tube is necessary. The patients are extubated in the operating room and hospitalized over-night in a standard hospital room without the necessity for an intensive care unit.


Figure 1
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  		Fig 1. Patient positioning and port selection in patients undergoing video-assisted thoracoscopic surgery thymectomy.

 
Data Analysis
The collected clinical data were analyzed using SAS 9.1.3 (SAS Institute, Cary, NC). All continuous variables were tested for normality. Those failing tests for normality (Anderson-Darling) were analyzed using nonparametric statistics (Wilcoxon) while the rest were compared using the t test. Categoric variables were subjected to {chi}2 or Fisher exact tests for statistical significance. A p value of 0.05 or less was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 References
 
Ninety-five patients with myasthenia gravis were included in the study, consisting of 48 VATS patients and 47 transsternal patients. Clinical follow-up was 89.5% complete, with a mean follow-up of 6.0 ± 4.0 years (median = 6.1 years) in the VATS group and 4.3 ± 2.9 years (median = 4.2 years) in the transsternal patient group (p = 0.03).

The mean age in the transsternal group was 34.4 ± 13.2 years, versus 39.8 ± 14.9 years in the VATS group. There were no significant differences in patient gender, preoperative duration of myasthenia gravis, and operative time between the two groups (Table 2). While slightly more transternal patients required postoperative ventilation, the difference was not statistically significant. Moreover, there was a statistically significant difference in the postoperative length of stay; 4.6 days in the transsternal group versus 1.9 days in the VATS patients (p < 0.001; Table 2). There were 4 deaths in the series, none of which occurred perioperatively or were determined to be related to myasthenia gravis (causes of death included respiratory arrest [1], pulmonary embolus [1], cardiac arrest [1], and metastatic renal cell carcinoma, von Hippel-Lindau disease, and suffered a stroke [1]).


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  		Table 2 Comparative Demographics and Perioperative Parameters in the Two Patient Groups
 
When assessing preoperative disease classification using the MGFA classification, the distribution of patients in the early classes, I and II, appeared similar between the two techniques (Table 3). However, there were more class III (moderately affected) patients in the transsternal group when compared with the VATS group. Conversely, there were more severely affected (class IV) patients in the VATS population, a statistically significant difference (p = 0.003).


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  		Table 3 Patient Distribution of Preoperative Disease Status Using the Myasthenia Gravis Foundation of America (MGFA) Classification
 
Postinterventional status was also analyzed using MGFA guidelines. As seen in Figure 2, complete stable remission (those patients off myasthenia gravis medications for greater than one year) was seen in 15.8% of the transsternal group and 34.9% of the VATS patients. Pharmacologic remission (patient takes some medications except for anticholinesterase inhibitors) was seen in 7.9% of the transsternal patients and 4.7% of the VATS patients. Minimal manifestations (patients with no functional limitations but some detectable muscle weakness on examination) were seen in 73.7% of the transsternal patients and 55.8% of the VATS group. There were no significant differences in these groups or in the categories of unchanged, worse, or death from myasthenia gravis. Overall, when combining the postinterventional status categories, both patient populations improved after thymectomy whether the procedure was performed by the sternotomy or the VATS approach.


Figure 2
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  		Fig 2. Postinterventional status using MGFA classification. (Grey bars = video-assisted thoracoscopic surgery [VATS]; black bars = transsternal [TS]; CSR = complete stable remission; MG = myasthenia gravis; MM = minimal manifestations; PR = pharmacologic remission; Unch = unchanged.)

 
When assessing whether the surgical technique predicted outcome based upon the preoperative class, no correlation was found favoring one procedure over the other (Table 4). In class I, patients in both groups were better after surgery. Similarly, in class II, patients in both study groups had acceptable results. Similar trends are seen in classes III, IV, and V patients. At last follow-up (VATS + transsternal), 78 of 81 (96.3%) patients were in complete stable remission or pharmacologic remission or minimal manifestations only. The three exceptions were 1 of 15 class II patients who were treated by VATS and had a worse outcome, 1 of 20 class III patients treated in the transsternal group and were rated unchanged, and 1 of 17 class III VATS patients who were worse.


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  		Table 4 Impact of Surgical Technique on Outcome Based Upon Preoperative Myasthenia Gravis Foundation of America (MGFA) Classification Status
 
The effect of thymectomy on the use of pyridostigmine and prednisone are shown in Table 5. The majority of patients were on pyridostigmine preoperatively, with only 7% of the transsternal patients and 44% of the VATS patients not on pyridostigmine preoperatively; 53.5% of the transsternal patients and 41.5 % of the VATS patients either started or continued to take pyridostigmine postoperatively. Most importantly, of the patients using pyridostigmine preoperatively, 42.5% of the transsternal patients and 65.2% of the VATS patients were able to discontinue the pyridostigmine postoperatively (Table 5). There was also no statistically significant difference between the two groups when examining the utilization of prednisone with 39.5% of the transsternal patients and 56.1% of the VATS group not on prednisone preoperatively. Again, 65.4% of the transsternal patients and 77.8% of the VATS patients taking prednisone preoperatively were able to discontinue their prednisone postoperatively. There were no statistical differences between the two groups. Immunosuppressive drug usage was smaller, with 25.6% of the transsternal and 4.9% of VATS patients using these agents before surgery. All the VATS patients and 54.6% of the transsternal patients had discontinued the drugs after surgery.


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  		Table 5 Postoperative Medication Requirements for the Most Commonly Used Pharmacologic Agents in the Treatment of Myasthenia Gravis, Mestinon (Valeant Pharmaceuticals International, Aliso Viejo, CA), and Prednisone
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 References
 
The earliest reported thymectomy in a myasthenia gravis patient was by Schumacher and Roth in 1912 [10]. However, it was the report by Blalock and colleagues [1] in 1941 that led to the widespread adoption of thymectomy in the management of myasthenia gravis. Since that time, both medical and surgical approaches have been advocated in the absence of rigorous randomized trials on which to draw firm conclusions regarding proper management in nonthymomatous myasthenia gravis. Similarly, different surgical approaches have not been compared in a prospective fashion.

Myasthenia gravis is a difficult disease process to investigate in that the disease is one of high variability with marked clinical fluctuation. Both medical and surgical studies have been limited by the lack of accepted outcome measures. As a result, the MGFA supported the development of preoperative and postintervention classifications to address the need for a universally accepted system, allowing for a more accurate method to assess and compare therapy outcomes in myasthenia gravis [8] (Table 1). In this study, standard transsternal evacuation of the thymus was compared to the VATS approach using the MGFA guidelines.

Since the first major report advocating the efficacy of thymectomy for myasthenia gravis, the transsternal approach became standard practice and for many years was the only method described. Expansions on the classic transsternal approach led to the extended thymectomy, which focused on the importance of removal of the mediastinal adipose tissue, a potential source of thymic rest cells. This technique was used in the current study. A series of 286 patients undergoing the extended transsternal procedure demonstrated remission rates at 5 years of 45.8%, with overall improvement of 92.2%, similar to that reported in the current study [11]. However, the morbidity of the surgical technique was not inconsequential, although actual mortality in contemporary series has been limited. Thymectomy by partial sternotomy has also been reported with acceptable results in a large study of 478 patients [12]. However, similar to most studies, MGFA classification was not yet available to better assess clinical outcomes.

Due to concern regarding morbidity, recovery, and cosmetic outcomes from the transsternal approach, Cooper and colleagues of Canada [13] and Calhoun and colleagues from Washington University [14], reported their experience with a less-invasive transcervical approach for thymectomy. In their series of 100 patients with myasthenia gravis, Calhoun and colleagues not only confirmed the efficacy of a transcervical approach, observing a significant improvement in the Osserman grade (from 3.0 preoperatively to 1.0 postoperatively), but the morbidity was very low and there was no mortality. The mean follow-up time was 5 years. They claimed a remission rate that parallels those studies using an extended transsternal approach [11]. Cooper and colleagues are clear in their belief that full resection of mediastinal adipose tissue is critical, and demonstrate their ability to accomplish this resection through a transcervical approach.

Jaretzki and Wolff [15] questioned whether cervical extensions of the thymus gland were completely accessed through a transsternal approach, and therefore developed a combined cervical and transsternal procedure [15]. The question as to whether complete resection of mediastinal adipose tissue impacts results from thymectomy in myasthenia gravis has been of chief concern to Jaretzki and his colleagues. They maintain that near complete exenteration of all the anterior mediastinal adipose tissue is critical, and cite cases where control of myasthenia gravis is compromised by even small remaining remnants of thymic tissue [16]. Patients undergoing the combined transsternal-transcervical procedure showed a remission rate of 62% at 7.4 years [17], with pathologic studies confirming the presence of residual thymus tissue in the resected adipose tissue. Mortality has remained low in their series (0.4%) but morbidity has included recurrent laryngeal nerve injuries ranging from 2% to 4% [18, 19]. It was the inherent morbidity related to the transsternal approach to the thymus gland that led to the development of other techniques for thymectomy.

With the development of improved video optics for surgery, thoracoscopic techniques quickly followed those adopted by abdominal surgeons. Thymectomy was an early application of the thoracoscopic techniques, with Mack and colleagues from five institutions reporting their initial experience [5]. While the technical efficacy was clearly demonstrated, the follow-up was too limited (23 months) to assess long-term effects of the procedure. More recently, Savcenko and colleagues [6] presented their experience in 38 myasthenia gravis patients, reporting minimal morbidity and no mortality with a follow-up of 53 months. Clinical improvement was observed in 83%, and 14% demonstrated complete stable remission. Similar results were reported by other groups [7, 9].

In the current study, the critical aspects of the transsternal and the VATS approaches were compared. Patient groups were assessed by the MGFA preoperative classification and postintervention status was analyzed using MGFA guidelines. Analysis of the two groups showed significant differences in postoperative length of stay. Operative mortality was not significantly different between the two groups. Late deaths in the thymectomy group were reviewed and were not found to be related to myasthenia gravis or the type of procedure performed. These deaths included metastatic renal cell carcinoma in a patient with Von Hippel-Landau disease 18 months postoperatively, a myocardial infarction 3 years postoperatively, pulmonary embolus 15 months postoperatively, and the postdischarge development of diverticulitis complicated by cardiac arrhythmias 2 months after thymectomy. Importantly, remission rates between the two techniques were not significantly different, with an acceptable mean follow-up in each cohort.

Limitations of the study include the retrospective nature at a period in time when the current MGFA clinical classification was not available. The introduction of this preoperative and postintervention grading system used in this study aimed to equalize the two patient cohorts to better compare the treatment strategies. The two patient groups were operated on at two different centers and cared for by different groups of clinicians. This could introduce bias into the study, an issue addressed by standardized preoperative and postoperative patient disease status classification using the MGFA guidelines. Follow-up was not complete, with data unavailable in approximately 10% of patients in each group. Importantly, duration of follow-up was shorter in the transsternal patients, which may underestimate the remission results in that group. Finally, small differences in populations at baseline are inherent to retrospective studies, although our analysis did not reveal major demographic differences that would clearly influence the response to surgery. Specifically, the only statistically significant preoperative difference between the two groups was the greater number of MGFA class IV patients in the VATS group. Despite this higher proportion of more clinically affected patients in the VATS group, the VATS group still had a shorter postoperative need for mechanical ventilation and a shorter postoperative hospital length of stay. The practical impact of the small, statistically insignificant, difference in age is difficult to predict.

Controversy persists regarding the indications and best approach for surgical intervention in the management of myasthenia gravis. While theoretic issues favor certain procedures over others, we demonstrated no significance difference in remission rates or other favorable outcomes in patients who received either transsternal or VATS thymectomy. The widespread adoption of the MGFA classification system offers the opportunity to more accurately assess the impact of both medical and surgical interventions in the management of this disease.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
References
 
DR SCOTT J. SWANSON (New York, NY): I enjoyed the paper. It was an excellent presentation.

Could you comment a little bit on your technique, how many ports you use, whether it's bilateral. Also, do you approach thymomas this way, and, if so, do you have a size cutoff?

DR MEYER: We do a unilateral technique utilizing four thoracoscopic ports. We had a slide from the left side, but most often we use a right-sided approach. We do not have a specific size cutoff for thymoma, but it has to be able to come out, of course, through the port without too much of an accessory incision.

DR SWANSON: Was there any way to objectively compare the specimens between the VATS (video-assisted thoracoscopic surgery) and the sternotomy?

DR MEYER: That's an excellent question, and after I was through with this study, I thought if we had the weights of the specimens, that would have been a much more useful comparison, but we do not have that data.

DR FRANK C. DETTERBECK (New Haven, CT): I enjoyed the presentation. It's certainly a nice attempt to try to shed some light on a controversy. On the other hand, it's very difficult to interpret the results because I think the patient populations are somewhat different. There were more patients with grade III symptoms and more patients that were on Mestinon (Valeant Pharmaceuticals International, Aliso Viejo, CA) and on prednisone in the transsternal group. That certainly is known to contribute to being able to extubate the patients immediately and also influence the longer term results. So I think that really confounds any comparison.

My question is, how were the patients prepared prior to surgery? I had the opportunity to work with a very good neuromuscular neurologist who really prepared the patients very, very carefully, and I think that this is the key to getting them extubated early. So do they get plasmapheresis, how stable was their disease when they underwent surgery, and is there a difference between the two institutions?

DR MEYER: Thank you for your questions. Yes, the patients were prepared quite carefully by the neurologist, but the interesting thing is, at the one hospital where the VATS procedure was performed, I think only one patient received plasmapheresis preoperatively, whereas the patients who had the transsternal approach, a larger percentage of those patients underwent preoperative plasmapheresis. Also, regarding early extubation, the VATS group, as you could see, had a much earlier extubation time. That is despite the difference in the groups, because there were more severely affected class IV patients in the VATS group and they still were able to be extubated earlier than the transsternal group. Our goal with this project was to use the MGFA preoperative classification system to better assess the two groups.

DR STEPHEN C. YANG (Baltimore, MD): I echo my colleagues on your great talk.

There are some institutions doing these robotically, including myself, and in keeping some prospective data now, I found that some patients who are on chronic steroid use, high BMIs, actually don't tolerate one-lung ventilation very well. What percent of your patients crossed over from a VATS technique over to an open technique?

DR MEYER: None of the VATS patients required conversion to an open technique, and in the VATS population, if the one-lung ventilation is a problem, we typically are using CO2 insufflation as well to help with this.

DR JOEL D. COOPER (Philadelphia, PA): Isn't there an award at the Southern Thoracic for the person who pops up the most to discuss the most papers, and I'm at risk of perhaps winning this if I get up again, but I think Dr Kaiser, who is not here, would not forgive me if I didn't comment.

I'm in the embarrassing situation of being a person who is somewhat skeptical about minimally invasive surgery and I'm getting up to defend the most minimally invasive procedure for thymectomy and to ask a question. I've done about 400 transcervicals. I send them home the next morning. Dr Kaiser does it and he sends them home the same day; no double-lumen tube, no chest tubes, no intercostal nerves injured, no lung collapsed. I know it's not easy to learn, but a transcervical thymectomy, if learned, does give as good a result as any series ever has reported. And, if you put in four ports, aren't you creating some thoracotomy discomfort or other problems? I don't think we have kept a post op patient past the next morning for several years. Every patient is extubated. As I say, Dr Kaiser has gone even one step further; he doesn't keep them overnight. So, I guess I would argue in favor of a more minimally invasive procedure. But I think what you've basically shown is that it doesn't matter how you take it out. If you take out the whole thymus, you're going to get the same result whether it's transcervical, transsternal, robotic, or video-assisted. So I guess I would ask you what you feel is the major benefit of your approach. I did enjoy the paper. Thanks.

DR MEYER: Thank you, Dr Cooper. In this analysis, of course, we did just compare the two procedures that we are more familiar with, the VATS and the transsternal. I have seen you perform the transcervical approach, and it is a quite extensive and equally effective approach for managing these patients, but there is the learning aspect of it. More so than with the transsternal and VATS techniques, unless you have been well trained with the few experts facile in the transcervical approach, there is the possibility of not getting as complete a resection.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 

  1. Blalock A, McGehee HA, Ford FR, et al. The treatment of myasthenia gravis by removal of the thymus gland JAMA 1941;117:1529.[Abstract/Free Full Text]
  2. Mussi A, Lucchi M, Murri L, Ricciardi R, Luchini L, Angeletti A. Extended thymectomy in myasthenia gravis: a team-work of neurologist, thoracic surgeon, and anaesthesist may improve the outcome Eur J Cardiothorac Surg 2001;19:570-575.[Abstract/Free Full Text]
  3. Roberts PF, Venuta F, Rendina E, et al. Thymectomy in the treatment of ocular myasthenia gravis J Thorac Cardiovasc Surg 2001;122:562-568.[Abstract/Free Full Text]
  4. Popescu I, Tomulescu V, Ion V, Tulbure D. Thymectomy by thoracoscopic approach in myasthenia gravis Surg Endosc 2002;16:679-684.[Medline]
  5. Mack MJ, Landreneau RJ, Yim AP, Hazelrigg SR, Scruggs G. Results of video-assisted thymectomy in patients with myasthenia gravis J Thorac Cardiovasc Surg 1996;112:1352-1360.[Abstract/Free Full Text]
  6. Savcenko M, Wendt GK, Prince SL, Mack MJ. Video-assisted thymectomy for myasthenia gravis: an update of a single institution experience Eur J Cardiothorac Surg 2002;22:978-983.[Abstract/Free Full Text]
  7. Mineo TC, Pompeo E, Lerut TE, Bernardi G, Coosemans W, Nofroni I. Thoracoscopic thymectomy in autoimmune myasthenia: results of left sided approach Ann Thorac Surg 2000;69:1537-1541.[Abstract/Free Full Text]
  8. Jaretzki A, Barohn R, Ernstoff RM, et al. Myasthenia gravis: recommendations for clinical research standards Ann Thorac Surg 2000;70:327-334.[Free Full Text]
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  10. Schumacher R, Roth J. Thymektomie bei cenem fall von morbus basedowii mit myasthenia Med Chir 1912;25:746.
  11. Masaoka A, Yamakawa Y, Niwa H, et al. Extended thymectomy for myasthenia gravis patients: a 20-year review Ann Thorac Surg 1996;62:853-859.[Abstract/Free Full Text]
  12. Pêgo-Fernandes PM, de Campos JR, Jatene FB, Marchiori P, Suso FV, de Oliveira SA. Thymectomy by partial sternotomy for the treatment of myasthenia gravis Ann Thorac Surg 2002;74:204-208.[Abstract/Free Full Text]
  13. Cooper JF, Al-Jalaihawa AN, Pearson FG, Humphrey JG, Humphrey HE. An improved technique to facilitate transcervical thymectomy for myasthenia gravis Ann Thorac Surg 1988;45:242-247.[Abstract/Free Full Text]
  14. Calhoun RF, Ritter JH, Guthrie TJ, et al. Results of transcervical thymectomy for myasthenia gravis in 100 consecutive patients Ann Surg 1999;230:555-561.[Medline]
  15. Jaretzki III A, Wolff M. "Maximal" thymectomy for myasthenia gravis. Surgical anatomy and operative technique. J Thorac Cardiovasc Surg 1988;96:711-716.[Abstract]
  16. Jaretzki III A, Penn AS, Younger DS, et al. "Maximal" thymectomy for myasthenia gravis: results J Thorac Cardiovasc Surg 1988;95:747-757.[Abstract]
  17. Jaretzki III A. Thymectomy for myasthenia gravis: analysis of controversies—patient management Neurologist 2003;9:77-92.[Medline]
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  19. Uchiyama A, Shimizu S, Murai H, Kuroki S, Okido M, Tanaka M. Infrasternal mediastinoscopy thymectomy in myasthenia gravis: surgical results in 23 patients Ann Thorac Surg 2001;72:1902-1905.[Abstract/Free Full Text]



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