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Department of Thoracic and Cardiovascular Surgery, St. Vincent Hospital, Indianapolis, Indiana
Accepted for publication April 15, 2011.
* Address correspondence to Dr Freeman, 8433 Harcourt Rd, Indianapolis, IN 46260 (Email: rfreeman{at}corvascmds.com).
Presented at the Fifty-seventh Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 3–6, 2010.
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Abstract |
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Methods: Data collection for patients undergoing robotic thymectomy for nonthymomatous myasthenia gravis over a 6-year period was prospectively performed. Patients were assessed using the Myasthenia Gravis Foundation of America's quantitative disease severity score and the post intervention status classification.
Results: During the study period, 75 patients underwent thymectomy by this method. Mean preoperative myasthenia gravis severity score was 2.7. Mean operative time was 113 ± 46 minutes. Extubation in the operating room occurred in 73 (98%) patients. Mean intensive care stay and total hospital length of stay were 0.9 and 2.2 days respectively. Mean interval between surgery and return to work (or prethymectomy activities of daily living) was 15 ± 6 days. Significant improvement of myasthenia gravis symptoms occurred in 65 (87%) patients with a mean follow-up of 45 ± 14 months.
Conclusions: Robotic-assisted thymectomy is a safe and effective technique for patients with symptomatic myasthenia gravis. It allowed an extended thymectomy to be performed without the associated length of stay or recovery period of a transsternal approach while producing comparable rates of symptom improvement.
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Introduction |
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TopAbstractIntroductionMaterial and MethodsResultsCommentDiscussionReferences |
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However, thoracic surgeons, neurologists, and patients are aware that transsternal thymectomy is an operation with a significant period of convalescence required prior to resuming a normal activity level or returning to full time employment. The ideal technique for thymectomy would be one which allowed the extended thymectomy performed with sternotomy to be performed using minimally invasive techniques. Transcervical, video-assisted thoracoscopic, and most recently robotic thymectomy, have all been studied in patients with NTMG in an attempt to find a balance between achieving a complete resection of the thymus and minimizing the effect of the surgery on the patient.
Robotic thymectomy offers several potential benefits for thymectomy. However, the reported series are relatively small, difficult to compare because of a lack of a standardized nomenclature, and provide relatively short periods of follow-up. The purpose of this investigation was to review the outcomes of a relatively large series of patients with a significant period of follow-up undergoing robotic thymectomy for NTMG.
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Material and Methods |
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Only patients with at least class II clinical symptoms (Myasthenia Gravis Foundation of America Clinical Classification) of myasthenia gravis designated by a neurologist were eligible to participate in this study [4]. Furthermore, patients with an anterior mediastinal mass or thymoma were not included in this review because of the potential difference in response to thymectomy and the prognosis of myasthenia gravis in these patients [6–11]. Patients found to have a thymoma in the surgical specimen after thymectomy were also excluded from the postoperative analysis, as were patients who required conversion to a sternotomy to complete the procedure.
It was the intention to perform an extended thymectomy including the removal of all tissue in the anterior mediastinum and pericardial fat between the thyroid gland, diaphragm, and phrenic nerves bilaterally. Histologic types of resected thymus were described as either hyperplastic, involuted, or normal. All resected thymic tissue was examined for evidence of an occult thymoma.
Statistical Analysis
Analysis of data was carried out using GraphPad Prism software 4.02 (San Diego, CA) for Windows (Microsoft, Redmond, WA). Continuous data are expressed as the mean ± standard deviation of the mean except where otherwise indicated.
Operative Technique: Anesthesia
General anesthesia was induced using a combination of a sedative-hypnotic (Propofol; AstraZeneca, Wilmington, DE) and a short- acting narcotic. If required for intubation, a non-depolarizing muscle relaxant was used. Blood pressure was monitored using a radial arterial catheter. A central line was not required. A single lumen endotracheal tube was utilized and contralateral, single lung ventilation established with the use of an Arndt bronchial blocker (Cook Medical, Bloomington, IN). Inhalational agents were utilized during the procedure and supplemented with the same sedative-hypnotic and narcotic combination if needed. Extubation was planned in the operating room at the conclusion of the procedure. Patients were then transferred to a specialty-specific intensive care environment.
Robotic Thymectomy Technique
Patients are positioned supine. A small roll is placed longitudinally under the left posterior chest with the cephalad end lying inferior to the tip of the scapula to allow the left shoulder to drop below the level of the anterior chest. This position facilitates maximal movement of the most cephalad robotic arm. The left-sided approach is used because the authors find it provides excellent exposure to the majority of the structures in the anterior mediastinum. Specifically, it allows excellent visualization of the thymus and pericardial fat overlying the pericardium and the innominate vein at the thoracic inlet.
Three thoracoscopic ports are placed in the midclavicular line of the second and eighth intercostals space and the anterior axillary line of the fifth interspace of the left chest (Fig 1). Mild carbon dioxide insufflation is used to shift the mediastinum into the right pleural space. The 30-degree thoracoscope is used in the fifth interspace port with 2 robotic arms being placed in the other 2 ports. In most cases, the entire procedure was accomplished using a grasper and a monopolar cautery on the 2 robotic arms. The da Vinci robotic system (Intuitive Surgical, Irvine, CA) was used for all of the robotic thymectomies included in this series of patients.
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Mediastinal tissue at the thoracic inlet is then dissected. Visualization can often be improved by pushing the already mobilized mediastinal tissue into the right pleural space. During this portion of the procedure, the innominate vein is identified at the inferior, distal thoracic inlet. It is skeletonized with tributaries being ligated with hemoclips or electrocautery. Care is taken to remove, en bloc, all mediastinal tissue in the thoracic inlet including the cervical thymic horns (Fig 2).
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Results |
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Mean age was 38 ± 17 years (range, 18 to 54 years) comprised of 41 females and 34 males. The mean duration of symptoms prior to surgery was 17 ± 11 months. Preoperative myasthenia gravis clinical classifications are displayed in Table 1. The mean preoperative myasthenia gravis severity score was 30 ± 3.
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Histologic classification of resected thymus was normal (27), involuted (29), and hyperplastic (19). Morbidities included superficial wound infection (2), pneumonia (1), deep vein thrombosis (1), and an intraoperative injury to the right internal mammary vein requiring ligation (1). There were no permanent injuries to the phrenic or recurrent laryngeal nerves, postoperative myasthenic crises, or mortalities in this series of patients.
Mean follow-up of patients after thymectomy was 45 ± 14 months, with all 75 patients completing the 36-month follow-up visit. Mean interval between surgery and return to work (or prethymectomy activities of daily living) was 15 ± 6 days. Significant improvement of myasthenia gravis symptoms, as defined by the Myasthenia Gravis Foundation of America's postintervention status classification, occurred in 65 (87%) of the patients. This included 21 (28%) complete stable remissions, 19 (25%) pharmacologic remissions, and 35 (47%) patients with minimal manifestations. No patient experienced a worsening of his or her myasthenic symptoms after thymectomy.
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Comment |
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Even before the possibility of a pathogenic link between Myasthenia Gravis and the thymus was identified, clinicians recognized that thymectomy could improve an afflicted patient's symptoms. Von Harberer [14] is credited with reporting the first thymectomy in a patient who coincidentally had myasthenia gravis. After surgery, the patient's symptoms improved. Subsequently Blalock and colleagues [15] reported a similar patient's experience after thymectomy for a thymoma. Blalock [16] went on to report of their experience with 20 patients who underwent thymectomy for myasthenia gravis without thymoma. Their results were equally encouraging and Dr Blalock was the first to emphasize the importance of performing thymectomy early in the course of the disease and the need to achieve a complete resection of all thymic tissue.
Despite reports of multiple series of patients who have undergone thymectomy for myasthenia gravis since Blalock, neurologists continue to hold differing views as to when and if thymectomy is indicated in the treatment of patients with nonthymomatous myasthenia gravis. Such differences of opinion are not surprising given the fact that there has never been a well-controlled, prospective study comparing medical management alone with thymectomy. Further complicating this issue is the body of surgical literature outlining differing extents of thymectomy using different surgical approaches. As Jaretzki and colleagues [17] have pointed out, such reports suffer from the lack of uniform reporting of disease severity, extent of thymectomy performed, response to thymectomy, specimen histology, follow-up length, and nonstandard statistical methods of analysis.
Despite such valid criticism, analysis of the modern medical literature lends support both for thymectomy in the treatment of patients with NTMG and in performing as complete a thymectomy as possible. Gronseth and Barohn [1] and Buckingham and colleagues [2] separately reported that superior rates of remission and (or) symptom improvement occurred in patients undergoing thymectomy when compared to medical management alone. Jaretzki and colleagues [4] reviewed the modern thymectomy literature, comprised of 17 studies, with sufficient data to allow a comparison of the rates of remission of NTMG after different thymectomy techniques as defined by the Myasthenia Gravis Foundation of America's thymectomy classification scheme. While the data available for analysis are not optimal, they overwhelmingly supported the premise that the more extensive the resection, the higher the rate of remission seen [3].
As mentioned, a number of techniques have evolved for thymectomy in patients with NTMG. One such category has been termed minimally invasive procedures. These would include the transcervical approach and several versions of a video-assisted thoracoscopic approach, including bilateral and adjunct cervical incisions. These techniques are certainly more attractive for patients and some referring physicians and seek to take advantage of the benefits realized in other minimally invasive thoracic procedures, including shorter hospital stay, fewer morbidities, and less recuperation time.
Transcervical thymectomy, however, suffers from a substantial learning curve, does not attempt to remove tissue lateral to the mediastinal pleura, and in experienced hands has a nearly 8% conversion rate to sternotomy [5]. Video-assisted thoracoscopic thymectomy, originally described as a unilateral procedure, has undergone several modifications in an attempt to compensate for the lack of visualization and instrument dexterity many have experienced. A bilateral approach has become more common with some authors recommending the addition of a cervical and (or) subxiphoid incision, as well. These modifications call into question the term "minimally invasive" and suggest the procedure's potential benefits may not be realized.
The theoretical advantages of a robotic technique stem from the improved optics and dexterity of the instruments available when compared with the transcervical and thoracoscopic techniques. The robotic surgical system utilizes a three-dimensional camera as well as image-processing software that provide superior image quality, magnification, and depth perception to standard thoracoscopy. Similarly, the "endowrist" technology of the robotic instruments allows 7 degrees of freedom of motion, up to 90 degrees of articulation, and motion scaling capabilities. Such features surpass even the most advanced thoracoscopic instrumentation available today. A possible benefit of such robotic technology, found in other procedures such as prostatectomy, could be to allow the thoracic surgeon to perform an extended thymectomy using a unilateral, three-port approach rather than a bilateral thoracoscopic approach with or without counter incisions.
Robotic thymectomy has been previously reported to be successful in smaller series of patients [18–22]. Although 4 of these reports included 1, 3, and 9 patients each undergoing thymectomy for NTMG, they represent the recognition and evolution of robotic thymectomy techniques. Rea and colleagues [21], however, reported their results with 33 patients undergoing robotic thymectomy using a similar technique to the one utilized in this review. That number of patients should have provided the opportunity for the evolution of a learning curve for the procedure. Although they did not choose to use the Myasthenia Gravis Foundation of America's standardized reporting scales, their mean operative time and symptomatic improvement rate are similar to the results seen in this investigation.
Goldstein and Yang [23] did utilize the Myasthenia Gravis Foundation's nomenclature in their report of 26 patients undergoing robotic thymectomy for myasthenia gravis. They found that 82% of patients experienced an improvement in their symptoms after surgery. Mean follow-up was 26 months and 5 patients included in their analysis were found to have a thymoma in the resected specimen.
This investigation found that robotic thymectomy produced rates of symptomatic improvement that compare favorably with transsternal, thoracoscopic, and transcervical thymectomy. Robotic thymectomy, however, allowed a complete thymectomy without the significant rate of conversion to sternotomy seen with the transcervical approach, even with an experienced surgeon. Unlike the trend in the video-assisted approach, it can be performed using a unilateral approach without the need for a cervical incision. Compared with transsternal thymectomy, the robotic technique produced significantly shorter hospital lengths of stay and recuperation [7]. This investigation also reports a relatively long follow-up period which, for robotic thymectomy, has been lacking in the literature.
Although robotic thymectomy appears to provide several advantages for performing extended thymectomy, this investigation has some weaknesses. Like many reports of techniques using new technology, the absolute number of patients included is relatively small. The initial follow-up of 36 months, although the longest reported thus far for this technique, remains relatively brief.
We chose to recognize patients as having realized a significant improvement after thymectomy if they were classified by their neurologist as a complete stable remission, pharmacologic remission, or minimal manifestation patient [4]. This decision is based on the practice pattern of many neurologists who care for patients with Myasthenia Gravis who are reluctant to stop immunosuppression despite improvement after thymectomy because of the significant risk of relapse [5, 24]. It also seemed reasonable to categorize patients as significantly improved who could only be found to have slight muscle weakness on careful examination by their neurologist.
In conclusion, this investigation reports the outcomes of a large group of patients undergoing extended robotic thymectomy after a relatively long follow-up period. The technique was found to be safe and produced hospital stay and return to work intervals that were decreased when compared with transsternal thymectomy, while observing similar rates of improvement in myasthenia gravis. The improved optics and instrument dexterity consistently allowed a unilateral, three-port approach for minimally invasive thymectomy with a very low rate of conversion to sternotomy. These findings lead us to suggest that robotic thymectomy is an effective approach for patients undergoing extended thymectomy and should be considered when discussing surgical options with patients with myasthenia gravis.
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Discussion |
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TopAbstractIntroductionMaterial and MethodsResultsCommentDiscussionReferences |
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DR FREEMAN: We have tried the right. Overall, it is the surgeon's preference. I like the left. I use mild insufflation, push the heart out of the way, and I just like looking at the innominate vein and finding it from the left rather than looking around the SVC from the right.
DR CERFOLIO: Do you find it easier to see more of the right phrenic nerve from the left chest than the left phrenic nerve from the right chest, because that is the critical issue. Otherwise the dissections are the name. Because you struggle a little bit seeing the whole phrenic nerve either way. Which do you find easier?
DR FREEMAN: Well, obviously I find the left easier because that is what we do.
DR CERFOLIO: How many rights have you tried?
DR FREEMAN: A handful. But I will tell you that that is not really the reason that I will go one side versus the other. I use a 30 degree scope, I use it in the up position for 90% of the case, and then after I have widely opened the right pleura and I am dissecting the tissue medial to the right phrenic nerve, I place the camera so that it is looking down and generally have a good view.
DR CERFOLIO: I do the whole thing with the 30 down. That is fine. I think you see more of the opposite nerve from the left chest but the vein dissection is easier from the right.
Last question. How many VATS thymectomies did you do before this? I did four or five and found this dramatically easier. It may have been my inexperience with VATS. But if you have done more, can you address that?
Thank you.
DR FREEMAN: We actually tried to compare those in a previous series, and our group, my partner and I, have done a large number of VATS thymectomies, and still do occasionally. I think this is easier, personally.
DR STEPHEN R. HAZELRIGG (Springfield, IL): That is just a great series, and I guess I have a similar question the way Cerf ended. When I look at all of this, our institution has done a high volume of thoracoscopic thymectomies. We go from the right, by the way, which I think is a better approach. I am still struggling with whether there is any significant advantage to robotics. I know that you seem to feel there is some advantage and I am aware of the movement of the instruments and visualization. We have not had problems with these issues thoracoscopically, however, our visualization is fine. Your results in your series are excellent. Certainly your results are comparable to those achieved thoracoscopically, but not better. The question for me is; why should I switch over to a more expensive approach that takes longer to perform because of the setup time. I am still trying to understand for myself where the big advantage is, and I would like to hear from you. You have done some of both.
DR FREEMAN: I think if you can do a unilateral approach VATS thymectomy such as Dr Mack and others have described, and you can do that in an hour and a half or an hour and forty-five minutes, there is probably no reason for you to look at the robot. That is my personal opinion.
We started doing this looking at where we wanted to be a couple of years down the road with masses and posterior mediastinal work, et cetera, and it has become so much easier that we have gone to the robot as our standard approach. But if you don't have to do a bilateral approach, which some people advocate, if you don't have to make all these counter incisions with VATS, and you can do it in an hour and a half, why change.
DR MICHAEL DIMAIO (Dallas, TX): Once again, Rich, a great presentation, great series, and for Cerfolio who believes in the right, I also use the left side, as we have talked about last week in Miami. And also I might comment as well that if you do VATS thymectomy with a robot, it is night and day with the visualization and the dexterity, and getting up the innominate vein, like you said, and clean that out is much, much easier with the robot.
The main question, though, Richard, is why 2.2 days, because I am trying to get my patients home the next day. Are you trying to shorten that up?
DR FREEMAN: Well, I will tell you that two days works well for us. Could I push some of these people out in one? I could. What I don't know is what my readmission rate would be, especially as we have very involved neurologists, which I think is one of the reasons that our patients do so well. It is usually a joint decision as to when the patient is discharged which likely extends the length of stay. And, quite frankly, a lot of these people just aren't ready.
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References |
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TopAbstractIntroductionMaterial and MethodsResultsCommentDiscussionReferences |
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This article has been cited by other articles:
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  G. Marulli, M. Schiavon, E. Perissinotto, A. Bugana, F. Di Chiara, A. Rebusso, and F. Rea Surgical and neurologic outcomes after robotic thymectomy in 100 consecutive patients with myasthenia gravis J. Thorac. Cardiovasc. Surg., March 1, 2013; 145(3): 730 - 736. [Abstract] [Full Text] [PDF]
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S. C. Murthy Niche for a technology or technology for a niche? J. Thorac. Cardiovasc. Surg., March 1, 2013; 145(3): 737 - 737. [Full Text] [PDF]
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 I. C. Okereke, K. A. Kesler, R. K. Freeman, K. M. Rieger, T. J. Birdas, A. J. Ascioti, S. Badve, R. P. Nelson, and P. J. Loehrer Thymic Carcinoma: Outcomes After Surgical Resection Ann. Thorac. Surg., May 1, 2012; 93(5): 1668 - 1673. [Abstract] [Full Text] [PDF]
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