Rea, Federico MD, PhD; Schiavon, Marco MD; Di Chiara, Francesco MD; Marulli, Giuseppe MD
A variety of benign and malignant diseases can arise or involve the mediastinum, a small space between the two pleura. From a surgical point of view, the therapy for the diseases of this anatomic district remains a challenge for the thoracic surgeons for many aspects: resectability, radicality, and finally, but no less important, the choice of the surgical access.
In fact, although sternotomy is considered the standard and preferable approach for most cases of malignant diseases of the mediastinum (particularly for thymomas), a great debate is still ongoing on the use of minimally invasive techniques for benign indications or for small tumors.1–3 Since their introduction, minimally invasive procedures (represented mainly by cervicotomy and thoracoscopy) have found growing application, thanks to several advantages represented by reduced invasiveness, short hospitalization, lower costs, lower morbidity, better cosmetic results, and compliance of the patients.4,5
The most important and frequent disorders of the mediastinum involve the thymic gland with a spectrum of diseases that range from hyperplasia to thymoma and thymic carcinoma. Thymectomy for thymic hyperplasia in patients with myasthenia gravis (MG) is accepted worldwide as an effective treatment, but a variety of surgical approaches have been used, ranging from invasive methods (sternotomy or cervicosternotomy) to minimally invasive techniques (cervicotomy, thoracoscopy, or associated approaches) leading to a strong debate over the optimal resectional approach,6–9 although many centers are opting for minimally invasive methods.10–12 Recently, some authors advocated the introduction of thoracoscopic approaches for early-stage tumors.13,14
The development of robot-assisted technologies in the late 1990s provided an improvement in visualization and surgical dexterity over thoracoscopy, allowing the application of robot-assisted thoracoscopy in the treatment of various thoracic diseases, mainly of the mediastinum.15,16 The three-dimensional view, the articulated instruments with 360-degree rotation, 7 degrees of freedom, and the tremor filtering make the robotic instrumentation ideal and advantageous compared with standard thoracoscopy when applied for the diseases of the small and relatively fixed mediastinal space.
In this article, we report our experience covering over 8 years, with the application of robot-assisted thoracoscopy for mediastinal diseases.
Between April 2002 and December 2010, at the Division of Thoracic Surgery in Padua, 108 patients underwent robot-assisted thoracoscopy using the “da Vinci” robotic system (Intuitive Surgical Inc., Mountain View, CA USA) for different mediastinal diseases. There were 79 (73.1%) women and 29 (26.9%) men with a median age of 38 years (range 12–73 y). Patients' characteristics are reported in Table 1. Thymectomy (Fig. 1), especially for thymic hyperplasia in patients with MG, was the most common operation (n = 100); other procedures were the resection of paravertebral tumors (n = 3) (Fig. 2), thymic cyst (n = 1), ectopic goitre (n = 1) (Fig. 3), ectopic mediastinal parathyroidectomy (n = 1) (Fig. 4), mediastinal carcinoid secreting adrenocorticotropic hormone (ACTH) and determining an ectopic Cushing syndrome (n = 1), and foregut cyst (n = 1).
Preoperative evaluation included blood samples, electrocardiogram, and spirometry; radiologic evaluation was performed with chest radiogram, computed tomography, and magnetic resonance in selected patients, especially those with neurinoma for the risk of medullar involvement. In case of ectopic parathyroid, thyroid, and Cushing syndrome, a specific scan was used to detect the secreting lesions and to guide the resective procedure. Diagnosis of MG was based on clinical criteria, as well as by the results of electromyography, of edrophonium chloride (Tensilon; ICN Pharmaceuticals, Inc., Costa Mesa, CA USA) test and the dosage of circulating acetylcholine receptor antibodies. Myasthenia Gravis Foundation of America17 (MGFA) classification was adopted for pre- and postoperative evaluation, and both evaluations were conducted by a team of neurologists. Preoperative preparation of patients with MG included a reduction or an interruption of steroid treatment whenever possible; plasmapheresis or intravenous immunoglobulin G was used in patients at risk for postoperative respiratory failure (involvement of respiratory muscles or recent worsening of symptoms).
Data were obtained from the hospital database, referring physicians, patients, or their families. The study was approved by the Institutional Review Board.
The patient was under general anesthesia and had a double-lumen endotracheal tube for selective single-lung ventilation during the time of operation. Our technique for thymectomy has been previously reported18: briefly, the patient is positioned left side up at a 30-degree angle with a bean bag. A camera port for the three-dimensional 0-degree stereo endoscope is introduced through a 15-mm incision in the left fifth intercostal space on the midaxillary line, and two additional thoracic ports are inserted, one in the left third intercostal space on the midaxillary region and another in the left fifth intercostal space on the parasternal line. The dissection of the thymus starts from below following the pericardial plane, until the innominate vein is found and the thymic veins are clipped and sectioned; finally, the upper horns in the neck are isolated and pulled down.
For posterior mediastinal diseases, the positioning of the patient is a standard lateral decubitus to favor the anterior positioning of the lung. The camera port is inserted in the anterior axillary line, and the choice of the intercostal space for the two working arms operating, placed symmetrically, is made on the basis of tumor localization. In case of resection for neurinoma, the tumor is excised in toto with the covering parietal pleura. The operative technique of resection of anterior and posterior mediastinal masses are described in different works.18–20
All the procedures were carried out endoscopically with no conversion to median sternotomy or thoracotomy. In three cases of thymectomy, a fourth access was performed, two on the right side to introduce an optic to better visualize the right phrenic nerve; in one patient, a cervicotomy was required to complete the dissection of thymic upper horns.
In one case of neurinoma, the resection required the additional use of posterior laminectomy because the tumor involved the conjugation foramen and the corresponding nerve. Operative and postoperative results are reported in Table 2. No deaths or intraoperative complications occurred, and all patients were extubated in the operating room within 1 hour from surgery. Median operative time was 120 minutes with a range from 60 to 300 minutes; median time to chest tube removal was 1 day (range 1–13 days) while median hospitalization was 3 days (range 2-14 days).
Postoperative complications occurred in four (3.6%) cases: one patient, in our early experience, had a chylothorax on the second postoperative day and required long hospitalization (2 weeks) to have conservative treatment; two patients had a hemothorax caused by bleeding from one access that also required conservative treatment with blood transfusions. Finally, one patient developed fever that required prolonged treatment with antibiotic therapy.
Among patients affected by MG, the pathologic examination revealed 75 (79%) thymic hyperplasia, 8 (8.4%) normal thymus, 6 (6.3%) atrophy, and 6 (6.3%) thymomas (World Health Organization classification: 2 B1 and 1 A, AB, B2, and B3 each). The other five thymomas in patients without MG had the following World Health Organization histotype: two B1 and one AB, B2, and B2-B each. Five cases were Masaoka stage I and six Masaoka stage II (all patients with Masaoka stage II thymoma received adjuvant radiotherapy). The mean weight of the specimens (thymus and perithymic tissue) was 51.5 g (range 12–189 g). Ectopic thymic tissue in mediastinal fat was found in 26 (27.4%) patients.
In myasthenic patients, clinical follow-up was performed, according to MGFA classification, on 76 (80%) cases that reached at least 12 months of observation. Median follow-up was 65 months (range 12–107 months).
A complete remission was observed in 13 (17.1%) cases, pharmacologic remission in 9 (11.8%), minimal manifestations in 21 (27.6%), improvement in 28 (36.9%), unchanged in 1 (1.3%), worsening in 3 (3.9%), and exacerbation in 1 (1.3%). Global benefit rate reached the value of 93.4% with a progressive improvement over years (5-y probability of remission and improvement: 33.4% and 95.1%, respectively). In patients who received thymomectomy, no evidence of tumor recurrence was found.
The introduction of video-assisted thoracic surgery in the 90s has dramatically changed the attitude of thoracic surgeons in relation to the surgery of the mediastinum. In fact, if open access is still the standard approach for resection of malignant mediastinal tumors, the minimally invasive approach has gained popularity in cases of benign disease due to less trauma, morbidity, hospital stay, and better cosmetic results.4–21
More recently, some authors have also proposed thoracoscopic resection even in cases of early-stage malignant disease, especially for thymic tumors.13,14 However, the diseases arising in the mediastinal area are extremely difficult to manage through the minimally invasive approach because it is a delicate and difficult-to-reach anatomic region with vulnerable structures (especially large vessels and nerves). Moreover, all the limitations of thoracoscopy characterized by two-dimensional vision, tremor, and inability of the arms to articulate are highlighted when we operate in the mediastinal field, particularly in case of thymectomy where the dissection of contralateral mediastinum and the neck around the thymic horns in a relatively fixed three-dimensional space may be extremely difficult.22,23 These features obviously have determined a limitation on the extensive use of this approach in these particular cases.
The development of robotic technologies in recent years has led to an improvement of many of the technical problems mentioned above and provided significant advantages to the thoracic surgeon. The da Vinci robotic system is a telemanipulator system that consists of several key components, including a master console with a high-definition three-dimensional vision, a surgical cart with three or four interactive robotic arms, and a conventional monitor cart. In the surgical cart, two instrument arms and a central arm to guide a two-channel endoscope are present. On the master console, the surgeon handles telemanipulators and optical controls, using an intuitive three-dimensional vision. The main technological advantages of this system are, other than the three-dimensional view, the 7 degrees of freedom of the instruments and filtration of tremor.
Robotic procedures are usually performed by two surgeons, the surgeon at the console and the tableside surgeon, who places the trocars and connects them with the robotic arms, changes the robotic instruments, and manipulates additional endoscopic instruments via the auxiliary ports, if needed. The characteristics of this system allow the ability to perform resection of all the diseases of the mediastinum, both anterior and posterior, reaching even small and remote areas.
As reported by several authors,15,16 the diseases of the anterior mediastinum, particularly the thymic disorders, represent one of the areas of greatest use of robot-assisted technology in thoracic surgery. A triple anterior approach is usually sufficient for all type of resections, and the choice of the side depends on the anatomic location of the lesion. In particular, our group has already demonstrated the safety and feasibility of robotic-extended thymectomy for patients with MG,18 providing excellent surgical outcomes and disease control. Our experience now consists of more than 90 cases performed, confirming the good short- and long-term data reported by other works,24,25 in particular the low number of complications, reduced hospitalization, and improved clinical follow-up of these patients with a percentage of improvement at the MGFA classification of more than 90%.
The ability of robot-assisted thoracoscopy to perform a thymic resection also extended to the mediastinal fat is demonstrated by the large proportion of ectopic thymic tissue found at the histopathologic analysis in the fat of all areas of mediastinum. Although we agree that the thymus can be safely approached from either side,16,24 we prefer the left-sided approach proposed also by other authors26 as it offers an enhanced visualization of the aortic window and reduces the probability of phrenic nerve injury. In fact, the left-sided approach permits an excellent view of the left phrenic nerve, while the right phrenic nerve is partially protected by the superior vena cava.
The absence of vascular and neurologic complications, need for conversions, and the small number of additional access reported in our experience testify the safety and effectiveness of this method. Probably, the only limitation of the left-sided approach is related to the presence of cardiomegaly, which can limit the exposure of the thymus.27 In our experience, however, the use of an additional insufflation of CO2 at 10 to 12 mm Hg in the chest seems useful to wind up the mediastinal space making the view and the dissection easier.
Concerning our experience in thymectomy for thymoma, we believe that the robotic approach is justified in cases of early-stage disease associated with MG or not. The technique of no-touch dissection with particular care to not open the capsule of the tumor is mandatory to avoid any dissemination in the pleural cavity. In all our cases, histologic analysis confirmed the integrity of the tumor and the presence of free resection margins. Finally, the follow-up excluded any presence of recurrence, and our results are consistent with those recently published by other authors.15,16 At this moment, however, although thoracoscopic thymectomy for early-stage tumors is technically sound, the data on long-term outcome are still lacking.28 Even the diseases of the posterior mediastinum may benefit from minimally invasive approach. In cases of esophageal diseases (eg, leiomyoma, diverticula, or foregut cyst)19 and of paravertebral neurinomas (especially for dumbbell tumors),20 the enhanced magnification allows a clear distinction of the anatomic structures (nerve or esophagus), minimizing the risk of damages. In addition, the motion-scaling system that translates large hand movements into precise surgical maneuvers facilitates safe dissection of these delicate anatomic structures. Finally, the articulation of the instruments represents a further decisive benefit, particularly for neurinomas located in the apical area of the chest.
The main problems related to robotic instrumentation are the high initial costs and the long operating time compared with conventional procedures, mainly during the learning curve. On the other hand, the reduction of hospital stay and a reduced number of instruments needed for thoracic surgery outweigh the initial investment. In addition, the learning curve required for these operations is reduced for surgeons with good experience on standard thoracoscopy and allows for operating times comparable with other minimally invasive procedures.
Further larger studies are needed to validate the use of robotic procedure in early-stage thymoma. Moreover, an accurate assessment of patients and lesions characteristics, especially the size, constitutes one of the key points to achieve good results, preventing the conversion to open approach. In conclusion, our series represents one of the largest published on several mediastinal diseases resected by thoracoscopy with the aid of the da Vinci system, and the excellent short- and long-term results reported confirm the great benefit of the use of robot in this field.
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3. Zielinski M, Kuzdzal J, Szlubowski A, et al. Transcervical-subxiphoid-videothoracoscopic “maximal” thymectomy—operative technique and early results. Ann Thorac Surg. 2004;78:404–409.
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Professor Federico Rea and his team in Padova, Italy, have reviewed their consecutive 8-year experience of robotic thymic resections in over 100 patients for a variety of thymic pathologies. To date, this represents the largest reported series of robotic thymic resections for the widest indications and, along with many other investigators, demonstrates feasibility and safety of the use of robotics to remove the thymus.
Video-assisted thoracic surgery (VATS) and the transcervical methods have been alternatives to median sternotomy and thoracotomy for removal of thymic pathology. However, both may not have the broad applicability to perform a sufficiently thorough anterior mediastinal dissection given the small space and the major structures involved; for malignancy and myasthenia gravis, an incomplete resection may result in recurrence or persistent disease. Unlike many nonthoracotomy/nonmedian sternotomy series, the Rea series required no conversions and had a low complication rate, less than 4%.
Early retrospective comparisons have demonstrated that the robotic resection seems equivalent to the median sternotomy and to the VATS approaches. Cakar et al1 and Augustin et al,2 in 2007 and 2008, respectively, compared robotics to the nonrobotic approaches and found that the median sternotomy method seemed to have a longer length of stay, 5 days versus 10 days, with a similar operating room time, 110 to160 minutes. In a recent report, Rückert and his team in Berlin performed a matched comparison of their robotic cases to their VATS cases, approximately 75 cases in each group.3 With a follow-up of 42 months, the remission rate for myasthenia gravis was almost twice the rate for VATS, 39.25% versus 20.3% (P = 0.01). With greater experience, technological and clinical management refinements, we may find that the precision afforded by robotics will result in more expedient recovery and better long-term results.
1. Cakar F, Werner P, Augustin F, et al. A comparison of outcomes after robotic open extended thymectomy for myasthenia gravis. Eur J Cardiothorac Surg. 2007;31:501–504.
2. Augustin F, Schmid T, Sieb M, et al. Video-assisted thoracoscopic surgery versus robotic-assisted thoracoscopic surgery thymectomy. Ann Thorac Surg. 2008;85:S768–S771.
3. Rückert JC, Swierzy M, Ismail M. Comparison of robotic and nonrobotic thoracoscopic thymectomy: a cohort study. J Thorac Cardiovasc Surg. 2011;141:673–677.
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