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Comparing Robotic and Trans-Sternal Thymectomy For Early-Stage Thymoma - A Propensity Score-Matching Study.
Comparing Robotic and Trans-Sternal Thymectomy For Early-Stage Thymoma - A Propensity Score-Matching Study.
Cite this article as: Marulli G, Comacchio GM, Schiavon M, Rebusso A, Mammana M, Zampieri D et al. Comparing robotic and trans-sternal thymectomy for early-
stage thymoma: a propensity score-matching study. Eur J Cardiothorac Surg 2018;54:579–84.
Received 11 September 2017; received in revised form 8 January 2018; accepted 2 February 2018
Abstract
OBJECTIVES: Minimally invasive techniques seem to be promising alternatives to open approaches in the surgical treatment of early-stage
thymoma, although there are controversies because of lack of data on long-term results. The aim of the study was to evaluate the surgical
and oncological results after robotic thymectomy for early-stage thymoma compared to median sternotomy.
METHODS: Between 1982 and 2017, 164 patients with early-stage thymoma (Masaoka I and II) were operated on by median sternotomy
(108 patients) or the robotic approach (56 patients). Duration of surgery, amount of blood loss, complications, duration of chest drainage,
postoperative hospital stay, oncological results and total costs were retrospectively evaluated. Data were analysed also after propensity
score matching.
RESULTS: Compared to the trans-sternal group, robotic thymectomy had significantly longer average operative times (P < 0.001) but less
intraoperative blood loss (P = 0.01), less perioperative complications (P = 0.03), shorter time to chest drainage removal and hospital dis-
charge (P < 0.001). The median expense for the trans-sternal approach was significantly higher than the cost of the robotic procedure
(P < 0.001), mainly due to longer hospitalization. From an oncological point of view, there were no differences in thymoma recurrence, al-
though follow-up of the trans-sternal group was significantly longer (P < 0.001). Data were confirmed after propensity score matching.
CONCLUSIONS: Robotic thymectomy for early-stage thymoma is a technically safe and feasible procedure with low complication rate
and shorter hospital stay compared to the trans-sternal approach. Cost analysis revealed lower expenses for the robotic procedure due to
the reduced hospital stay. The oncological outcomes seemed comparable, but longer follow-up is needed.
Keywords: Thymoma • Surgery • Early stage • Robot • Trans-sternal thymectomy
THORACIC
INTRODUCTION increased risk of local recurrence (due to reduced safety margins
after minimally invasive resection) and the possible rupture of the
Thymomas are rare neoplasms, representing 0.2–1.5% of all capsule with implantation of the tumour during endoscopic ma-
malignancies, but are the most common tumours of the medias- nipulations. Furthermore, the lack of long-term oncological results,
tinum [1]. Surgery is the cornerstone of treatment, particularly for the learning curve required to perform this operation safely and
early-stage disease, and completeness of resection with adequate the relative rarity of these tumours are additional reasons that
safety margins is the main prognostic factor [2]. slow down the diffusion of the video-assisted thoracic surgery
Different surgical approaches have been described to perform (VATS) resection [3–5]. The introduction of robotic-assisted tech-
thymectomy, but to date, sternotomy still represents the gold nologies in the late 1990s provided a technical advancement able
standard. Minimally invasive approaches seem to be promising al- to overcome the limitations of conventional thoracoscopy: the
ternatives to open techniques and, in the last 2 decades, have three-dimensional vision system and the articulated instruments of
been slowly adopted in the surgery of malignant tumours of the the daVinci Surgical Robotic System (Intuitive Surgical, Inc.,
mediastinal district. The main downsides are the supposed Sunnyvale, CA, USA) allow for an ‘open-like’ intervention with a
minimally invasive access. The application of robotic technology
has been tested in a variety of thoracic surgery procedures, with a
†Presented at the 31st Annual Meeting of the European Association for Cardio-
Thoracic Surgery, Vienna, Austria, 7–10 October 2017. prevalent application for mediastinal diseases, where the robotic
‡The first two authors contributed equally to this work. system seems to provide the best advantages [6, 7].
C The Author(s) 2018. Published by Oxford University Press on behalf of the European Association for Cardio-Thoracic Surgery. All rights reserved.
V
580 G. Marulli et al. / European Journal of Cardio-Thoracic Surgery
The aim of the study was to evaluate the surgical and onco- close to the phrenic nerves. Carbon dioxide insufflation of
logical results after robotic thymectomy (RATS) for early-stage 6–10 mmHg was applied during the procedure to increase the
thymoma, compared with a population of patients operated on size of the mediastinal space. All surgeons involved in the pro-
through a median sternotomy. cedure adopted a ‘no-touch technique’ with an en bloc resection
of the thymus and perithymic fat tissue. During the application of
this technique, the thymoma was never touched, and normal
MATERIALS AND METHODS thymic tissue and perithymic fat were used for grasping and for
traction, so as to avoid direct manipulation of the tumour, capsu-
We retrospectively reviewed the medical records of 278 patients lar damage and potential seeding. All thymic and perithymic fat
with a thymic tumour who underwent surgical resection in the was dissected together with thymoma with safe surgical margins,
Unit of Thoracic Surgery of the University of Padova, from June in agreement with the International Thymic Malignancy Interest
1982 to December 2016. Exclusion criteria were thymic neoplas- Group (ITMIG) criteria [12]. In case of myasthenic patients,
tic diseases other than thymoma, advanced stage disease (Stage particular attention was posed on the removal of all the media-
III or IV according to Masaoka), incomplete resection (R1 or R2) stinal fat.
and surgical resection other than trans-sternal or robotic tech-
and tumour characteristics in the 2 groups are presented in Table 1. Regardless of the surgical approach, all patients had an R0 re-
Compared with the TST group, the RATS group was characterized section, and there were no intraoperative deaths.
by a younger age, a higher percentage of MG, a lower diameter of In the RATS group, the median operative time (skin-to-skin,
the tumour and a higher proportion of Masaoka Stage II thymoma. comprehensive of operative time at the console, docking, speci-
The surgical outcome in the RATS and TST groups are pre- men removal and undocking) was 132.5 min [interquartile range
sented in Table 2. In the RATS group, 6 patients were approached (IQR) 115.0–170.0 min], and in the TST group, it was significantly
from the right thoracic cavity and 50 patients from the left side. shorter (median 115.0 min, IQR 90.0–137.5 min; P < 0.001).
No intraoperative or perioperative mortality was recorded for The robotic group had significantly less intraoperative blood
both groups. Two (3%) patients in the minimally invasive group loss [when the cut-off is set at 100 ml (P = 0.02), while the signifi-
needed open conversion, in 1 case because of the dimension of cance was lost at a cut-off of 200 ml (P = 0.13)] and earlier chest
the specimen and difficult dissection (myasthenic patient with drain removal and hospital discharge.
abundant mediastinal fat) and in the other because of suspicions The overall incidence of perioperative complications was
of pericardial infiltration. In 1 patient, a cervicotomy was per- higher in the TST group than in the RATS group (15% vs 4%;
formed to complete the dissection of the thymus in the neck. P = 0.03); however, no significant difference was reached for
Robotic group TST group P-value Robotic group TST group P-value
(n = 56) (n = 108) (n = 41) (n = 41)
Age (years), (mean ± SD) 55.82 ± 12.01 59.44 ± 10.85 0.05 58.24 ± 10.97 57.66 ± 10.30 0.88a
Male, n (%) 25 (45) 49 (45.4) 1.00 18 (49.9) 19 (46.3) 0.98a
Female, n (%) 31 (55) 59 (54.6) 23 (56.1) 22 (53.7)
Myasthenia gravis, n (%) 30 (54) 31 (28.7) 0.002 19 (46.3) 15 (36.6) 0.38a
Masaoka stage, n (%) 0.07 0.09a
I 11 (20) 36 (33.3) 8 (19.5) 9 (22.0)
II 45 (80) 72 (66.7) 33 (80.5) 32 (78.0)
WHO type, n (%) 0.08 0.47a
A 4 (7) 18 (17) 3 (7) 4 (10)
AB 12 (21) 37 (34) 10 (24) 9 (22)
B1 18 (32) 26 (24) 14 (34) 13 (31)
B2 15 (27) 20 (18) 10 (25) 10 (25)
B3 7 (13) 7 (7) 4 (10) 5 (12)
Dimension (cm), mean ± SD 43.25 ± 18.43 76.17 ± 31.82 <0.001 50.36 ± 15.54 54.49 ± 21.53 0.05a
a
Adjusted to year of surgery.
SD: standard deviation; TST: trans-sternal thymectomy; WHO: World Health Organization.
THORACIC
Table 2: Operative and postoperative data (overall and after matching)
Robotic group TST group P-value Robotic group TST group P-value
(n = 56) (n = 108) (n = 41) (n = 41)
Operative time (min), median (IQR) 132.5 (115–170) 115 (90–137) <0.001 125 (115–160) 120 (95–135) 0.45a
Open conversion, n (%) 2 (3) 1 (2)
Intraoperative blood loss (ml), n (%)
>_50 3 (5) 21 (19) 0.01 3 (7) 9 (22) 0.99a
>_100 2 (3) 17 (16) 0.02
>_200 2 (3) 11 (10) 0.13
Postoperative complications, n (%)
Overall 2 (4) 16 (15) 0.03 2 (5) 3 (7) 0.50a
Major 2 (4) 7 (6) 0.72
Drain removal (days), median (IQR) 2 (1–2) 4 (4–5) <0.001 2 (1–2) 4 (3–5) 0.16a
Length of hospital stay (days), median (IQR) 3 (3–4) 6 (5–7) <0.001 3 (3–4) 6 (5–6) 0.04a
Total costs (e), median (IQR) 3395 (3395–4069) 4194 (3520–4868) <0.001 3395 (3395–4069) 4194 (3520–4868) <0.001a
Adjuvant radiotherapy, n (%) 25 (45) 39 (36) 0.30 15 (36) 18 (44) 0.50a
Length of follow-up (months), median (IQR) 30.9 (8.5–67.8) 90.7 (46.8–149.5) <0.001 28.3 (18.2–61.4) 88.3 (61.6–116.4) 0.04a
Recurrence, n (%) 1 (2) 2 (2) 1.0 1 (2) 0 (0) na
a
Adjusted to year of surgery and tumour dimension.
IQR: interquartile range; na: not applicable; TST: trans-sternal thymectomy.
582 G. Marulli et al. / European Journal of Cardio-Thoracic Surgery
major complications (P = 0.72). Seven patients in the TST group advantages and the plentiful literature confirming the superiority
had the following major complications: 3 respiratory failures, 2 of oncological results. As in other surgical fields, minimally inva-
myasthenic crisis, 1 sternal dehiscence and 1 cardiac arrest. Two sive techniques for performing thymectomy have gained atten-
patients in the RATS group presented with each one of the fol- tion in recent years for their capability to assure the complete
lowing complications: myasthenic crisis and haemothorax, which removal of the tumour, without the disadvantages of the open
required surgical treatment. techniques. Nevertheless, surgical and oncological issues are still
The median expense for a TST and consequent hospital stay matter of debate.
was e4194 (IQR e3520–e4868), which was significantly higher In the present study, we compared TST with RATS, both from
than the cost for a RATS (e3395, IQR e3395–e4069, P < 0.001). the surgical and oncological point of view, using a propensity
Sixty-four patients received postoperative radiotherapy, 25 score matching to make the 2 populations comparable.
(45%) in the robotic group and 39 (36%) in the trans-sternal From the surgical point of view, minimally invasive thymec-
group, with no significant difference between groups (P = 0.30). tomy, particularly through the VATS approach, has always been
Two (2%) patients in the TST group had a thymoma recur- considered a challenging operation requiring a long learning
rence, whereas in the robotic group, 1 (2%) patient experienced curve to perform this operation safely. Nevertheless, several
pleural recurrence 32 months after the initial operation. This dif- groups have published their experiences, demonstrating good
included in the total account of the time. As shown by Bodner Finally, one of the main criticisms directed at robotic surgery is
et al. [6], there are important differences when evaluating the the high cost. To date, no author performed a direct cost com-
time for the setting up of the robot, for the surgeon working at parison of the 2 techniques. Augustin et al. [25] performed an
the console and the skin-to-skin time. Indeed, the long time for evaluation of the procedural costs for a RATS compared with the
the robot set-up represents a bias when comparing the robotic standard VATS approach, showing that the robotic approach was
approach with the standard sternotomy, making it difficult to 91% more expensive than its counterpart.
compare the 2 techniques. In addition, this bias can be deter- The cost for the DaVinci robot is variable between 1 000 000e
mined by the steep learning curve of the robotic technique and, and 2 500 000e. In addition to this, the average costs for the an-
therefore, it is inversely proportional to the surgeon’s experience. nual maintenance are around 100 000e/175 000e. However,
Indeed, different authors have found a reduction of the opera- these fee could be divided among the different surgical units
tive time with an increasing number of operations performed other than the thoracic surgical unit that use the robotic system,
[21, 22]. such as urology and gynaecology: this ‘shared’ use of the DaVinci
Nevertheless, several surgeons have been reluctant to use robot allows for the division of the initial and running costs.
these surgical approaches for thymoma because of the possible Apart from the initial cost of the DaVinci system, the extra costs
oncological concerns related to rupture of the capsule with im- are mainly related to disposables. Performing a RATS requires an
THORACIC
follow-up of 180 months, we can state that the RATS also appears
to be safe in the mid-term follow-up from an oncological point Limitations
of view.
Another important issue is the dimension of the tumour. The The present study has some limitations, in particular the low
size of thymoma appropriate for robotic resection is still a matter number of patients, the non-randomized and retrospective fash-
of debate. The majority of the literature deals with lesions <5 cm ion. In addition, the follow-up is still inadequate in allowing for a
[5, 14]. Although a large tumour size may not be considered an definitive conclusion regarding the oncological outcome.
absolute contraindication, it may interfere with the thoracoscopic Anyway, the propensity score matching enabled us to over-
procedure, causing the manipulation to be more difficult with come some intrinsic bias and make the 2 populations more com-
increased chance of an open conversion, or it may prolong the parable, confirming the encouraging results of the robotic
operative time [14]. On the contrary, trans-sternal operation has technique especially from a surgical point of view.
no dimensional limitation. Indeed, in the current series, the mean
diameter of thymomas in patients operated through a robotic
approach was 43.25 ± 18.43 mm, which was significantly lower CONCLUSION
than the diameter of thymomas of the other group
(76.17 ± 31.82 mm, P < 0.001). Because of this, tumor dimension In conclusion, although the ‘pure’ operation cost for a RATS is
might represent an important bias when comparing the two sensibly higher than that for conventional sternotomy, this ex-
techniques. However, after matching the patients also for the pense is compensated by a reduced postoperative hospital stay
tumor dimension, there were no significant differences in the and a faster recovery.
final result with only blood losses losing significance. On the con-
trary, the reduction in terms of hospital stay and the oncological
outcomes were confirmed. Conflict of interest: none declared.
584 G. Marulli et al. / European Journal of Cardio-Thoracic Surgery
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