World J Surg (2014) 38:709–715 DOI 10.1007/s00268-013-2326-9
Synchronous Bilateral Adrenalectomy for Cushing’s Syndrome: Laparoscopic Versus Posterior Retroperitoneoscopic Versus Robotic Approach Marco Raffaelli • Laurent Brunaud • Carmela De Crea • Guillaume Hoche • Luigi Oragano • Laurent Bresler • Rocco Bellantone • Celestino P. Lombardi
Published online: 19 November 2013 Ó Socie´te´ Internationale de Chirurgie 2013
Abstract Background Synchronous endoscopic bilateral adrenalectomy (BilA) can effectively provide definitive cure of hypercortisolism in ACTH-dependent Cushing’s syndrome and in primary adrenal bilateral disease. We compared three different approaches for BilA: transabdominal laparoscopic BilA (TL-BilA), simultaneous posterior retroperitoneoscopic BilA (PR-BilA), and robot-assisted BilA (RA-BilA). Methods All patients who underwent BilA between January 1999 and December 2012 at two referral centers (one performing TL-BilA and PR-BilA and one performing RA-BilA) were included. A comparative analysis was performed. Results Twenty-nine patients were included: 5 underwent TL-BilA, 11 underwent PR-BilA, and 13 underwent RABilA. No significant difference was found concerning age, gender, diagnosis, and previous abdominal surgery. No
conversion to open approach was registered. Operative time was significantly shorter for the PR-BilA group than for the TL-BilA and RA-BilA groups (157.4 ± 54.6 vs 256.0 ± 43.4 vs 221.5 ± 42.2 min, respectively) (P \ 0.001). No significant difference was found concerning intraoperative and postoperative complications rate and time to first flatus. Drains were used routinely after PRBilA and TL-BilA and electively in four RA-BilA patients (P \ 0.001). Hospital stay was longer in the TL-BilA and PR-BilA groups than in the RA-BilA group (12.0 ± 5.7 vs 10.8 ± 3.7 vs 4.4 ± 1.7 days, respectively) (P \ 0.001). No recurrence or disease-related death was registered. Conclusions Operative time was significantly shorter in the PR-BilA group, because it eliminates the need to reposition the patient. The number of drains and the length of hospital stay were reduced after RA-BilA, but this was likely related to different management protocols in different settings. Because no significant difference was found in terms of postoperative outcome, none of the three operative approaches can be considered the preferable one.
This article is based on work presented at the ISW 2013—IAES free paper session, 25–29 August 2013, Helsinki, Finland.
Introduction
M. Raffaelli C. De Crea (&) L. Oragano R. Bellantone C. P. Lombardi Division of Endocrine and Metabolic Surgery, Istituto di Semeiotica Chirurgica, Universita` Cattolica del Sacro Cuore, Policlinico ‘‘A. Gemelli’’, L.go A. Gemelli 8, 00168 Rome, Italy e-mail: [email protected]
Bilateral adrenalectomy (BilA) can provide definitive cure of hypercortisolism in persistent or recurrent Cushing’s disease after unsuccessful pituitary surgery, irradiation, or both, in nonresectable corticotrophin-secreting tumors, and in primary adrenal bilateral diseases [1]. Endoscopic adrenalectomy has become the standard option in the treatment of benign adrenal lesions, because of its advantages over conventional surgery in terms of postoperative morbidity and recovery, which are also obvious in patients with Cushing’s syndrome [2]. Although earlier studies showed less evident benefit for patients undergoing
M. Raffaelli e-mail: [email protected] L. Brunaud G. Hoche L. Bresler Service de Chirurgie Digestive, He´pato-biliaire et Endocrinienne, Hoˆpital Brabois-Adultes, CHU de Nancy, Vandœuvre-le`s-Nancy, France
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synchronous endoscopic BilA [2, 3], more recent articles have advocated endoscopic BilA as the procedure of choice for the management of patients with adrenocorticotropin hormone (ACTH)-dependent Cushing’s syndrome with persistent hypercortisolism despite tumor-directed treatment and/or medical treatment [4, 5]. Those patients represent a particular and unique subgroup because of the increased risk of complications related to uncontrolled cortisol excess and consequent comorbidities [1]. Different techniques for endoscopic adrenalectomy have been proposed, with the transperitoneal lateral approach (TL-BilA) and the posterior retroperitoneoscopic approach (PR-BilA) being the two more frequently used techniques worldwide [6]. The TL approach is used in about 70 % of medical centers [6] and is commonly used to perform bilateral procedures [3, 7]. The main disadvantage of this approach for BilA is the need to reposition the patient after completing the operation on the first side. This step of the procedure is time consuming and significantly prolongs the overall operative time. The PR approach has recently gained interest in the endocrine surgical community as an alternative, safe, and efficacious approach for endoscopic adrenalectomy and it appears as a very attractive procedure in patients requiring BilA, because it eliminates the need to reposition the patient [8, 9]. Also, PR makes it possible to perform a synchronous BilA with two different surgical teams operating on the two different sides of the patient. This reduces the surgical stress for patients with ACTHdependent Cushing’s syndrome [10]. Moreover, during the last few years, robot-assisted adrenalectomy (RA-BilA) has been investigated as an alternative or an extension of the capabilities for traditional laparoscopic or retroperitoneoscopic adrenalectomy [11, 12]. However, comparative studies [9] and metanalysis [13, 14] have failed to demonstrate any significant advantage of one technique over the other (TL vs PR). Similarly, no significant advantages or disadvantages (with the exception of increased overall costs) [15] were found for RA in comparison with traditional endoscopic adrenalectomy, even if recent series suggested a reduced complications rate and a better postoperative outcome for patients undergoing RA [12]. Consequently, it can be considered that scant data are available in the current literature regarding BilA. Only one article compares synchronous bilateral TL and PR, showing no significant advantages or disadvantages for either technique [7]. So far, no study has compared the results of RA to those of conventional endoscopic adrenalectomy for synchronous BilA. The present two-institution study aimed to compare the results of the transperitoneal lateral laparoscopic, simultaneous posterior retroperitoneoscopic, and robotic transperitoneal lateral approaches in patients with Cushing’s syndrome requiring BilA.
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Materials and methods Patient population Among all the patients who underwent adrenal surgery at two university third-care referral centers (Division of Endocrine and Metabolic Surgery, Policlinico ‘‘A. Gemelli,’’ Universita` Cattolica del Sacro Cuore, Rome, Italy, and Division of Digestive, Hepatobiliary and Endocrine Surgery, CHU de Nancy, France) between January 1999 and December 2012, those patients who underwent synchronous BilA for Cushing’s syndrome by traditional endoscopic adrenalectomy or by RA were included in the present study. Patients who underwent BilA by a conventional open approach were excluded. Study design Demographic, clinical, operative, pathological, and outcome data that were prospectively collected by each center into the relevant institutional database were retrospectively analyzed using a specifically designed spreadsheet (Microsoft Excel, Microsoft Corporation, Redmond, WA). The following parameters were registered: age, gender, preoperative diagnosis (Cushing’s disease, ectopic ACTH secretion, ACTH independent bilateral adrenal hyperplasia), previous abdominal surgery, surgical approach, body mass index (BMI), American Society of Anesthesiologists (ASA) score, operative time, conversion to open approach, blood transfusion, drain if any, intraoperative and postoperative complications, time to first flatus, hospital stay, corticosteroid replacement therapy at discharge, follow-up results. Follow-up evaluation was performed by outpatient consultation or telephone contact. Postoperative complications were graded according to the Clavien–Dindo classification [16]. Patients were divided into three groups on the basis of the surgical approach: TL-BilA, simultaneous PR-BilA, or transperitoneal lateral RA-BilA. A comparative analysis among the three groups concerning all included parameters was performed. Study end points The primary end point was to compare the operative outcome among the three groups of patients, as evaluated by morbidity rate and postoperative recovery. The secondary aim of the study was to compare operative time and conversion rate among the three different techniques. Surgical procedures All the procedures were performed by or under the supervision of a staff surgeon, with more than 50
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endoscopic adrenalectomies performed in both institutions. At the Division of Endocrine and Metabolic Surgery— Policlinico ‘‘A. Gemelli’’ in Rome (Italy) the operative approach was TL-BilA or PR-BilA. Patients operated on from January 1999 to December 2006 underwent TL-BilA, while all the patients operated on from January 2007 to December 2012 underwent PR-BilA. At the Division of Digestive, Hepatobiliary and Endocrine Surgery-CHU de Nancy, Nancy (France) the operative approach was RABilA (since April 2003). Synchronous TL-BilA was performed according to the surgical technique described for TL by Gagner et al. [17], with the patient on flank position. Four ports, in subcostal position, were used for the right side and three for the left side. The CO2 insufflation pressure was 12 mmHg. After adrenalectomy was accomplished on one side, the patient was rotated to the contralateral flank position and adrenalectomy was performed on the contralateral side. The technique for simultaneous PR-BilA has been described elsewhere [10]. Briefly, two different surgical teams (surgeon, assistant, nurse) and sets of equipment (monitor, insufflator, camera, and surgical instrumentation) were assembled on each side of the patient [10]. The setup of the operating room is outlined in Fig. 1. A simultaneous PR-BilA was performed with the two different teams, using two sets of surgical equipment, operating at the same time. The PR procedure was performed according to the technique described by Walz et al. [18]. The dressing of the external surgical field and the trocar insertion is usually accomplished one side at a time. This implies a slight time shift in the beginning of the procedure on both sides. Each team works at one side of the patient, looking at the monitor on the opposite side. Three ports are used for each side. CO2 insufflation pressure is 20 mmHg. All the surgical steps performed in unilateral adrenalectomy are carried out on each side without interference with the contralateral team. The RA-BilA was performed using a robotic endoscopic surgical device (Da Vinci system, Intuitive Surgical, Sunnyvale, CA, USA). All of the RA-BilA procedures were performed via the lateral transabdominal approach, as described elsewhere [19] with the patient placed in the lateral decubitus position, similarly to TL. One or two additional trocars with respect to the TL procedure are necessary for the assistant. CO2 insufflation pressure is the same as for TL. The operator is seated at the console where there are two handles controlling the robotic arms and four foot pedals for focusing and movement of the camera, coagulation, and disengaging the instrument. The image seen by the surgeon is tridimensional by the use of two optical canals and as many tri-CCD cameras. The assistant remains at the operating table, ensuring the change of surgical instruments and controlling one (or two) trocar (s) to contribute to better exposure of the operative field or
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Fig. 1 Setup of the operating room for simultaneous posterior retroperitoneoscopic BilA
assistance with clip placement. The surgical steps and principles are the same as performed in conventional TL. After adrenalectomy is accomplished on the first side, the patient needs to be repositioned as for TL. Statistical analysis Statistical analysis was performed with a commercially available software package (SPSS 15.0 for Windows, SPSS Inc., Chicago, IL, USA). The appropriate parametric or non-parametric test [analysis of variance (ANOVA); v2 test] was used when comparing group means or frequencies. A P value \0.05 was considered significant.
Results Among 795 patients who underwent adrenalectomy for various indications at the 2 institutions, 29 (3.6 %) had
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Operative time was significantly shorter in the PR-BilA group than in the TL-BilA and RA-BilA groups (157.4 ± 54.6 vs 256.0 ± 43.4 vs 221.5 ± 42.2 min, respectively) (P \ 0.001) (Table 1). Repositioning time was collected only for patients undergoing RA-BilA, and its mean value was 37.8 ± 9.5 min (range 25–55 min). No conversion to open approach was necessary in any patient. In one patient of the PR-BilA group (9 %), conversion to the hand-assisted technique was necessary on the right side because of difficult dissection related to adhesion with the vena cava. Overall, the intraoperative complications rate was 13.8 %. These complications corresponded to (1) splenic capsular lesions in one case (successfully treated with hemostatic agents), (2) bleeds in two patients in the RA-BilA group, and (3) a single bleed in the PR-BilA group (P = NS). In those three cases of complications, bleeding was related to a main adrenal vein injury resolved endoscopically with clip application. The postoperative complication rate was 17.3 %. Those complications involved
Cushing’s syndrome with bilateral adrenal hyperplasia and were included: 5 patients underwent TL-BilA, 11 underwent PR-BilA, and 13 underwent RA-BilA. Preoperative diagnosis was refractory Cushing’s disease (recurrence after trans-sphenoidal surgery and medical therapy) in 17 patients (58.6 %), ectopic ACTH secretion in 9 cases (31.0 %), and ACTH-independent bilateral adrenal hyperplasia (symmetrical bilateral macronodular hyperplasia) in the remaining 3 cases (10.3 %) (Table 1). Demographic, clinical, operative, pathological, and follow-up data are reported in Table 1. No significant difference was found among the three groups concerning age, gender, preoperative diagnosis, ASA score, BMI, and mean follow-up. Eight patients (28 %) had undergone previous abdominal operations: two in the TL-BilA group (appendectomy for both), three in the PR-BilA group (cholecystectomy in 2, appendectomy in 1), and the remaining three in the RA-BilA group (appendectomy in 2; sigmoidectomy and hysterectomy in one) (P = NS) (Table 1). Table 1 Comparative analysis among RA-BilA, PR-BilA, and TL-BilA Variables
RA-BilA
PR-BilA
TL-BilA
P value
Patients
13
11
5
Age (years)a
42.8 ± 13.6 (18–63)
41.2 ± 13.1 (18–62)
46.8 ± 19.9 (15–67)
Gender (male/female)
2/11
2/9
2/3
Cushing’s disease
7 (43.7 %)b
8 (72.7 %)c
2 (40.0 %)d
Ectopic ACTH secretion
4 (25 %)b
3 (27.3 %)c
2 (40.0 %)d
Preoperative diagnosis
0.591
2 (12.5 %)
b
Previous abdominal surgery
3 (25.0 %)
b
BMI (kg/m2)a
ACTH-independent Cushing
0.777
0 (0.0 %)
c
1 (20.0 %)d c
3 (27.2 %)
2 (40.0 %)d
0.772
30.2 ± 6.5 (18.5–46.0)
27.9 ± 4.6 (22.5–36.7)
31.9 ± 4.8 (25.4–36.6)
0.379
ASA score 0/10/3/0/0
0/8/3/0/0
0/4/1/0/0
0.945
Operative time (min)a
I/II/III/IV/V
221.5 ± 42.2 (155–285)
157.4 ± 54.6 (85–240)
256.0 ± 43.4 (210–300)
\0.001
Conversion to open approach
0
0e
0
NS
Blood transfusion
0
1 (9.1 %)c
1 (20.0 %)d
0.304
Drain yes/no
4/9
11/0
5/0
\0.001
Intraoperative complications Postoperative complications
3 (18.7 %)b 2 (12.5 %)b
1 (9.1 %)c 3 (27.2 %)c
0 0
0.378 0.397
Clavien–Dindo classification
IIIa, IV
I, II, II
Time to first flatus (days)a
1.8 ± 0.6 (1–3)
1.6 ± 0.5 (1–2)
a
Hospital stay (days) Follow-up (months)
a
4.4 ± 1.7 (2–8)
f
10.8 ± 3.7 (5–18)
2.3 ± 1.2 (1–3) f
12.0 ± 5.7 (8–22)
0.195 f
\0.001f
18.8 ± 16.4 (2–48)
33.5 ± 22.4 (8–72)
46.8 ± 43.6 (2–98)
0.094
Disease-related death
0 (0 %)b
0 (0 %)c
0 (0 %)d
NS
Death for unrelated causes
0 (0 %)b
1 (9.1 %)c
1 (20.0 %)d
0.304
a
Numbers represent the mean value, with ± SD and range in brackets
b
The percentage is expressed as a ratio to 13 patients in the RA-BilA group
c
The percentage is expressed as a ratio to 11 patients in PR-BilA group
d
The percentage is expressed as a ratio to 5 patients in the TL-BilA group One patient required conversion to the hand-assisted approach (see text)
e f
This reflects differences in management protocols between different institutions. See text
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one collection (managed conservatively) and one respiratory failure (recovered after medical treatment) (Clavien– Dindo’s grade IIIa and IV, respectively) in the RA-BilA group; one case of atypical chest pain, one pulmonary embolism (successfully treated with heparin), and one selflimiting bleed in the adrenal bed (indicating an adrenal bed hematoma, detected by CT scan, that required blood transfusion but no reoperation) (Clavien–Dindo grades I, II, and II, respectively) in the PR-BilA group (P = NS). Two drains, one per side, were used in all patients who underwent PR-BilA and TL-BilA (100 %). Among the RABilA patients, drains were positioned in 4 patients (30.7 %): one drain (on the left side) in 2 patients, two drains (one per side) in the remaining two patients (P \ 0.001). Global drain volume was registered only for patients in two groups: the PR-BilA group (211 ± 134 ml; range 80–440 ml) and the TL-BilA group (241 ± 154 ml; range 80–450 ml) (P = NS). Blood transfusions were required in two patients, one in the PR-BilA group and one in the TL-BilA group. No significant difference was found in the three groups concerning time to first flatus: 1.8 ± 0.6 days (range 1–3 days) versus 1.6 ± 0.5 days (range 1–2 days) versus 2.3 ± 1.2 days (range 1–3 days) in case of RA-BilA, PR-BilA, and TLBilA, respectively (P = NS). Mean hospital stay was longer in the TL-BilA and PRBilA groups than in the RA-BilA group (12.0 ± 5.7 vs 10.8 ± 3.7 vs 4.4 ± 1.7 days, respectively) (P \ 0.001). All patients were discharged on oral corticosteroid replacement therapy. At a mean follow-up of 30.0 ± 26.5 months, 2 patients died from unrelated causes (one in the TL-BilA group and one in the PR-BilA group). No recurrence or disease-related death was registered in any group.
Discussion Patients with (ACTH)-dependent Cushing’s syndrome are debilitated from the chronic effects of cortisol overproduction. In this high-risk patient population, comparative data regarding different available approaches to perform BilA are scarce. The present study demonstrated that synchronous bilateral endoscopic adrenalectomy is safe and effective for the treatment of this particular subset of patients at high risk of perioperative complications, with no conversion in experienced centers, confirming previous studies [3, 7]. We found that operative time was significantly shorter in the PR-BilA group than in the TL-BilA and RA-BilA groups. Intraoperative and postoperative complications were similar in the three groups. The RA-BilA approach was associated with a reduced number of drains used and with shorter hospitalization duration.
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Miccoli et al. [7] had already compared the outcome of PR and TL in patients undergoing synchronous BilA for various diseases in a two-institution study. They failed to demonstrate any significant difference in the surgical outcome [7]. In recent years a simultaneous PR-BilA with two different surgical teams operating simultaneously on either side of the patient, has been proposed, in order to further reduce the operative time and, theoretically, the overall operative stress [10]. In addition, during the last decade RA has been explored as an alternative to conventional endoscopic adrenalectomy [11, 12, 20–22]. The RA approach provides a 3-dimensional display that enhances depth perception, enables the surgeon to operate in a comfortable seated position in which the eye, hand, and target are in line, and the instrumentation includes a ‘‘wrist’’ joint to improve dexterity [20]. These advantages could theoretically improve the endoscopic adrenalectomy procedure and then led to improved perioperative and postoperative outcomes. Unfortunately, these speculative advantages have not yet been demonstrated, and the cost increase also remains an important drawback associated with robotic surgery [20]. The theoretical advantages of RA for the patient in terms of perioperative and postoperative outcome and its unequivocal advantages in terms of comfort for the surgeon could be of particular interest in the case of BilA. Indeed, such procedure is usually longer, patients are frequently obese and, especially in the case of Cushing’s syndrome, at increased risk of intraoperative and postoperative complications. Moreover, adrenal glands in this group of patients are usually nestled within copious fat and in a background of very fragile tissues, which can hinder the identification of the anatomy and make the dissection more difficult [3, 4, 23]. For this reason the 3-dimensional view could theoretically permit an easier and more precise dissection in each particular situation. However, a few cases have been reported so far [24] and no comparative studies have been published on this particular subgroup of patients. We performed the present two-institution study in order to compare the results of the most broadly applied approach to BilA in patients with Cushing’s syndrome—TL-BilA—with the results of PR-BilA and RA-BilA, that could offer some theoretical advantages, as discussed above. All three of the techniques were effective in achieving an adequate surgical resection, as no persistent or recurrent diseases and no disease-related death was observed at a mean follow-up of about 30 months. Not surprisingly, one of the significant differences we found concerned operative time. Indeed, as expected, the mean operative time for PR-BilA was significantly shorter than for TL-BilA and RA-BilA. This was related to the fact that the prone position exposes both adrenal regions at the
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same time and eliminates the need to reposition the patient after the first adrenalectomy is accomplished. This repositioning time was registered only for patients undergoing RA-BilA and was about 40 min. This was in agreement with the reports in the literature. Indeed, it is well known that this step of the procedure is time consuming and significantly prolongs the operative time. In large-volume centers the operation requires *30 min, but it can be longer [3]. Moreover, the simultaneous posterior adrenalectomy implies that two different surgical teams operate at the same time on the two different sides with a further reduction of operative time for BilA [10]. The main limitations of this procedure are related to the need of having two different well-trained surgical teams working at the same time on the different sides. In other words, simultaneous PR-BilA implies that different surgeons of the same institution gain adequate experience with this approach. This requires a tertiary care referral center with a large volume of recruited patients and some senior surgeons with a quite large experience in adrenal and laparoscopic surgery who may become confident with performing PR-BilA. It is also clear that this approach necessitates a dedicated operating room team (at all levels), which includes dedicated anesthesiologists and nurses. The complexity of patient positioning and the management of two working surgical teams and equipment are minimized by having such a dedicated group. On the other hand, the mean operative time for RA-BilA tended to be shorter than that registered for TL-BilA, not only in the present series but also in the literature [3, 4]. This advantage of the RA-BilA procedure can be explained by the better visualization of the operative field and by the improved ease for the surgeon working at the console. The significant differences in operative time among the three techniques did not translate into different operative outcomes. In fact, no significant difference in terms of patient recovery (time to first flatus), intraoperative complications rate, and postoperative morbidity was observed. The only other significant differences we found among the three groups of patients were the number of drains used, which was significantly reduced in RA-BilA, and the duration of the hospital stay, which was significantly shorter after RA-BilA. However, this was likely related to different management protocols in different settings. Indeed, in one of the involved centers drains are routinely positioned after every procedure, and many patients are referred from a distance and they are kept hospitalized until a maintenance oral dose of hydrocortisone (30 mg/day) is reached and they are able to travel considerable distance back home. In the other center, drains are electively positioned on the basis of the surgeon’s discretion, and patients unable to be maintained under oral dose of hydrocortisone are referred to the endocrinology unit, shortly after surgery.
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The major limitation of the present study resides in the fact that it is a retrospective multi-institutional study. This implies the lack of information, in particular about quality of life and cost analysis. However, it is well known that robotassisted procedures are usually associated with increased costs when compared with conventional endoscopic procedures [25]. On the other hand, the costs tend to decrease as the number of procedures performed increases [22]; further reduction in costs should be expected in the future when a more competitive market is likely to develop [22]. In conclusion, although each technique might have some advantages and some limitations with respect to the others, no significant difference was found in terms of postoperative outcome among the three approaches we evaluated. In other words, the findings of the presents study were not sufficient to conclusively indicate a clear-cut advantage of one technique over the others. Conflict of interest
No conflict of interest is declared for this paper.
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Synchronous Bilateral Adrenalectomy for Cushing’s Syndrome: Laparoscopic Versus Posterior Retroperitoneoscopic Versus Robotic Approach Marco Raffaelli • Laurent Brunaud • Carmela De Crea • Guillaume Hoche • Luigi Oragano • Laurent Bresler • Rocco Bellantone • Celestino P. Lombardi
Published online: 19 November 2013 Ó Socie´te´ Internationale de Chirurgie 2013
Abstract Background Synchronous endoscopic bilateral adrenalectomy (BilA) can effectively provide definitive cure of hypercortisolism in ACTH-dependent Cushing’s syndrome and in primary adrenal bilateral disease. We compared three different approaches for BilA: transabdominal laparoscopic BilA (TL-BilA), simultaneous posterior retroperitoneoscopic BilA (PR-BilA), and robot-assisted BilA (RA-BilA). Methods All patients who underwent BilA between January 1999 and December 2012 at two referral centers (one performing TL-BilA and PR-BilA and one performing RA-BilA) were included. A comparative analysis was performed. Results Twenty-nine patients were included: 5 underwent TL-BilA, 11 underwent PR-BilA, and 13 underwent RABilA. No significant difference was found concerning age, gender, diagnosis, and previous abdominal surgery. No
conversion to open approach was registered. Operative time was significantly shorter for the PR-BilA group than for the TL-BilA and RA-BilA groups (157.4 ± 54.6 vs 256.0 ± 43.4 vs 221.5 ± 42.2 min, respectively) (P \ 0.001). No significant difference was found concerning intraoperative and postoperative complications rate and time to first flatus. Drains were used routinely after PRBilA and TL-BilA and electively in four RA-BilA patients (P \ 0.001). Hospital stay was longer in the TL-BilA and PR-BilA groups than in the RA-BilA group (12.0 ± 5.7 vs 10.8 ± 3.7 vs 4.4 ± 1.7 days, respectively) (P \ 0.001). No recurrence or disease-related death was registered. Conclusions Operative time was significantly shorter in the PR-BilA group, because it eliminates the need to reposition the patient. The number of drains and the length of hospital stay were reduced after RA-BilA, but this was likely related to different management protocols in different settings. Because no significant difference was found in terms of postoperative outcome, none of the three operative approaches can be considered the preferable one.
This article is based on work presented at the ISW 2013—IAES free paper session, 25–29 August 2013, Helsinki, Finland.
Introduction
M. Raffaelli C. De Crea (&) L. Oragano R. Bellantone C. P. Lombardi Division of Endocrine and Metabolic Surgery, Istituto di Semeiotica Chirurgica, Universita` Cattolica del Sacro Cuore, Policlinico ‘‘A. Gemelli’’, L.go A. Gemelli 8, 00168 Rome, Italy e-mail: [email protected]
Bilateral adrenalectomy (BilA) can provide definitive cure of hypercortisolism in persistent or recurrent Cushing’s disease after unsuccessful pituitary surgery, irradiation, or both, in nonresectable corticotrophin-secreting tumors, and in primary adrenal bilateral diseases [1]. Endoscopic adrenalectomy has become the standard option in the treatment of benign adrenal lesions, because of its advantages over conventional surgery in terms of postoperative morbidity and recovery, which are also obvious in patients with Cushing’s syndrome [2]. Although earlier studies showed less evident benefit for patients undergoing
M. Raffaelli e-mail: [email protected] L. Brunaud G. Hoche L. Bresler Service de Chirurgie Digestive, He´pato-biliaire et Endocrinienne, Hoˆpital Brabois-Adultes, CHU de Nancy, Vandœuvre-le`s-Nancy, France
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synchronous endoscopic BilA [2, 3], more recent articles have advocated endoscopic BilA as the procedure of choice for the management of patients with adrenocorticotropin hormone (ACTH)-dependent Cushing’s syndrome with persistent hypercortisolism despite tumor-directed treatment and/or medical treatment [4, 5]. Those patients represent a particular and unique subgroup because of the increased risk of complications related to uncontrolled cortisol excess and consequent comorbidities [1]. Different techniques for endoscopic adrenalectomy have been proposed, with the transperitoneal lateral approach (TL-BilA) and the posterior retroperitoneoscopic approach (PR-BilA) being the two more frequently used techniques worldwide [6]. The TL approach is used in about 70 % of medical centers [6] and is commonly used to perform bilateral procedures [3, 7]. The main disadvantage of this approach for BilA is the need to reposition the patient after completing the operation on the first side. This step of the procedure is time consuming and significantly prolongs the overall operative time. The PR approach has recently gained interest in the endocrine surgical community as an alternative, safe, and efficacious approach for endoscopic adrenalectomy and it appears as a very attractive procedure in patients requiring BilA, because it eliminates the need to reposition the patient [8, 9]. Also, PR makes it possible to perform a synchronous BilA with two different surgical teams operating on the two different sides of the patient. This reduces the surgical stress for patients with ACTHdependent Cushing’s syndrome [10]. Moreover, during the last few years, robot-assisted adrenalectomy (RA-BilA) has been investigated as an alternative or an extension of the capabilities for traditional laparoscopic or retroperitoneoscopic adrenalectomy [11, 12]. However, comparative studies [9] and metanalysis [13, 14] have failed to demonstrate any significant advantage of one technique over the other (TL vs PR). Similarly, no significant advantages or disadvantages (with the exception of increased overall costs) [15] were found for RA in comparison with traditional endoscopic adrenalectomy, even if recent series suggested a reduced complications rate and a better postoperative outcome for patients undergoing RA [12]. Consequently, it can be considered that scant data are available in the current literature regarding BilA. Only one article compares synchronous bilateral TL and PR, showing no significant advantages or disadvantages for either technique [7]. So far, no study has compared the results of RA to those of conventional endoscopic adrenalectomy for synchronous BilA. The present two-institution study aimed to compare the results of the transperitoneal lateral laparoscopic, simultaneous posterior retroperitoneoscopic, and robotic transperitoneal lateral approaches in patients with Cushing’s syndrome requiring BilA.
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Materials and methods Patient population Among all the patients who underwent adrenal surgery at two university third-care referral centers (Division of Endocrine and Metabolic Surgery, Policlinico ‘‘A. Gemelli,’’ Universita` Cattolica del Sacro Cuore, Rome, Italy, and Division of Digestive, Hepatobiliary and Endocrine Surgery, CHU de Nancy, France) between January 1999 and December 2012, those patients who underwent synchronous BilA for Cushing’s syndrome by traditional endoscopic adrenalectomy or by RA were included in the present study. Patients who underwent BilA by a conventional open approach were excluded. Study design Demographic, clinical, operative, pathological, and outcome data that were prospectively collected by each center into the relevant institutional database were retrospectively analyzed using a specifically designed spreadsheet (Microsoft Excel, Microsoft Corporation, Redmond, WA). The following parameters were registered: age, gender, preoperative diagnosis (Cushing’s disease, ectopic ACTH secretion, ACTH independent bilateral adrenal hyperplasia), previous abdominal surgery, surgical approach, body mass index (BMI), American Society of Anesthesiologists (ASA) score, operative time, conversion to open approach, blood transfusion, drain if any, intraoperative and postoperative complications, time to first flatus, hospital stay, corticosteroid replacement therapy at discharge, follow-up results. Follow-up evaluation was performed by outpatient consultation or telephone contact. Postoperative complications were graded according to the Clavien–Dindo classification [16]. Patients were divided into three groups on the basis of the surgical approach: TL-BilA, simultaneous PR-BilA, or transperitoneal lateral RA-BilA. A comparative analysis among the three groups concerning all included parameters was performed. Study end points The primary end point was to compare the operative outcome among the three groups of patients, as evaluated by morbidity rate and postoperative recovery. The secondary aim of the study was to compare operative time and conversion rate among the three different techniques. Surgical procedures All the procedures were performed by or under the supervision of a staff surgeon, with more than 50
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endoscopic adrenalectomies performed in both institutions. At the Division of Endocrine and Metabolic Surgery— Policlinico ‘‘A. Gemelli’’ in Rome (Italy) the operative approach was TL-BilA or PR-BilA. Patients operated on from January 1999 to December 2006 underwent TL-BilA, while all the patients operated on from January 2007 to December 2012 underwent PR-BilA. At the Division of Digestive, Hepatobiliary and Endocrine Surgery-CHU de Nancy, Nancy (France) the operative approach was RABilA (since April 2003). Synchronous TL-BilA was performed according to the surgical technique described for TL by Gagner et al. [17], with the patient on flank position. Four ports, in subcostal position, were used for the right side and three for the left side. The CO2 insufflation pressure was 12 mmHg. After adrenalectomy was accomplished on one side, the patient was rotated to the contralateral flank position and adrenalectomy was performed on the contralateral side. The technique for simultaneous PR-BilA has been described elsewhere [10]. Briefly, two different surgical teams (surgeon, assistant, nurse) and sets of equipment (monitor, insufflator, camera, and surgical instrumentation) were assembled on each side of the patient [10]. The setup of the operating room is outlined in Fig. 1. A simultaneous PR-BilA was performed with the two different teams, using two sets of surgical equipment, operating at the same time. The PR procedure was performed according to the technique described by Walz et al. [18]. The dressing of the external surgical field and the trocar insertion is usually accomplished one side at a time. This implies a slight time shift in the beginning of the procedure on both sides. Each team works at one side of the patient, looking at the monitor on the opposite side. Three ports are used for each side. CO2 insufflation pressure is 20 mmHg. All the surgical steps performed in unilateral adrenalectomy are carried out on each side without interference with the contralateral team. The RA-BilA was performed using a robotic endoscopic surgical device (Da Vinci system, Intuitive Surgical, Sunnyvale, CA, USA). All of the RA-BilA procedures were performed via the lateral transabdominal approach, as described elsewhere [19] with the patient placed in the lateral decubitus position, similarly to TL. One or two additional trocars with respect to the TL procedure are necessary for the assistant. CO2 insufflation pressure is the same as for TL. The operator is seated at the console where there are two handles controlling the robotic arms and four foot pedals for focusing and movement of the camera, coagulation, and disengaging the instrument. The image seen by the surgeon is tridimensional by the use of two optical canals and as many tri-CCD cameras. The assistant remains at the operating table, ensuring the change of surgical instruments and controlling one (or two) trocar (s) to contribute to better exposure of the operative field or
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Fig. 1 Setup of the operating room for simultaneous posterior retroperitoneoscopic BilA
assistance with clip placement. The surgical steps and principles are the same as performed in conventional TL. After adrenalectomy is accomplished on the first side, the patient needs to be repositioned as for TL. Statistical analysis Statistical analysis was performed with a commercially available software package (SPSS 15.0 for Windows, SPSS Inc., Chicago, IL, USA). The appropriate parametric or non-parametric test [analysis of variance (ANOVA); v2 test] was used when comparing group means or frequencies. A P value \0.05 was considered significant.
Results Among 795 patients who underwent adrenalectomy for various indications at the 2 institutions, 29 (3.6 %) had
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Operative time was significantly shorter in the PR-BilA group than in the TL-BilA and RA-BilA groups (157.4 ± 54.6 vs 256.0 ± 43.4 vs 221.5 ± 42.2 min, respectively) (P \ 0.001) (Table 1). Repositioning time was collected only for patients undergoing RA-BilA, and its mean value was 37.8 ± 9.5 min (range 25–55 min). No conversion to open approach was necessary in any patient. In one patient of the PR-BilA group (9 %), conversion to the hand-assisted technique was necessary on the right side because of difficult dissection related to adhesion with the vena cava. Overall, the intraoperative complications rate was 13.8 %. These complications corresponded to (1) splenic capsular lesions in one case (successfully treated with hemostatic agents), (2) bleeds in two patients in the RA-BilA group, and (3) a single bleed in the PR-BilA group (P = NS). In those three cases of complications, bleeding was related to a main adrenal vein injury resolved endoscopically with clip application. The postoperative complication rate was 17.3 %. Those complications involved
Cushing’s syndrome with bilateral adrenal hyperplasia and were included: 5 patients underwent TL-BilA, 11 underwent PR-BilA, and 13 underwent RA-BilA. Preoperative diagnosis was refractory Cushing’s disease (recurrence after trans-sphenoidal surgery and medical therapy) in 17 patients (58.6 %), ectopic ACTH secretion in 9 cases (31.0 %), and ACTH-independent bilateral adrenal hyperplasia (symmetrical bilateral macronodular hyperplasia) in the remaining 3 cases (10.3 %) (Table 1). Demographic, clinical, operative, pathological, and follow-up data are reported in Table 1. No significant difference was found among the three groups concerning age, gender, preoperative diagnosis, ASA score, BMI, and mean follow-up. Eight patients (28 %) had undergone previous abdominal operations: two in the TL-BilA group (appendectomy for both), three in the PR-BilA group (cholecystectomy in 2, appendectomy in 1), and the remaining three in the RA-BilA group (appendectomy in 2; sigmoidectomy and hysterectomy in one) (P = NS) (Table 1). Table 1 Comparative analysis among RA-BilA, PR-BilA, and TL-BilA Variables
RA-BilA
PR-BilA
TL-BilA
P value
Patients
13
11
5
Age (years)a
42.8 ± 13.6 (18–63)
41.2 ± 13.1 (18–62)
46.8 ± 19.9 (15–67)
Gender (male/female)
2/11
2/9
2/3
Cushing’s disease
7 (43.7 %)b
8 (72.7 %)c
2 (40.0 %)d
Ectopic ACTH secretion
4 (25 %)b
3 (27.3 %)c
2 (40.0 %)d
Preoperative diagnosis
0.591
2 (12.5 %)
b
Previous abdominal surgery
3 (25.0 %)
b
BMI (kg/m2)a
ACTH-independent Cushing
0.777
0 (0.0 %)
c
1 (20.0 %)d c
3 (27.2 %)
2 (40.0 %)d
0.772
30.2 ± 6.5 (18.5–46.0)
27.9 ± 4.6 (22.5–36.7)
31.9 ± 4.8 (25.4–36.6)
0.379
ASA score 0/10/3/0/0
0/8/3/0/0
0/4/1/0/0
0.945
Operative time (min)a
I/II/III/IV/V
221.5 ± 42.2 (155–285)
157.4 ± 54.6 (85–240)
256.0 ± 43.4 (210–300)
\0.001
Conversion to open approach
0
0e
0
NS
Blood transfusion
0
1 (9.1 %)c
1 (20.0 %)d
0.304
Drain yes/no
4/9
11/0
5/0
\0.001
Intraoperative complications Postoperative complications
3 (18.7 %)b 2 (12.5 %)b
1 (9.1 %)c 3 (27.2 %)c
0 0
0.378 0.397
Clavien–Dindo classification
IIIa, IV
I, II, II
Time to first flatus (days)a
1.8 ± 0.6 (1–3)
1.6 ± 0.5 (1–2)
a
Hospital stay (days) Follow-up (months)
a
4.4 ± 1.7 (2–8)
f
10.8 ± 3.7 (5–18)
2.3 ± 1.2 (1–3) f
12.0 ± 5.7 (8–22)
0.195 f
\0.001f
18.8 ± 16.4 (2–48)
33.5 ± 22.4 (8–72)
46.8 ± 43.6 (2–98)
0.094
Disease-related death
0 (0 %)b
0 (0 %)c
0 (0 %)d
NS
Death for unrelated causes
0 (0 %)b
1 (9.1 %)c
1 (20.0 %)d
0.304
a
Numbers represent the mean value, with ± SD and range in brackets
b
The percentage is expressed as a ratio to 13 patients in the RA-BilA group
c
The percentage is expressed as a ratio to 11 patients in PR-BilA group
d
The percentage is expressed as a ratio to 5 patients in the TL-BilA group One patient required conversion to the hand-assisted approach (see text)
e f
This reflects differences in management protocols between different institutions. See text
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one collection (managed conservatively) and one respiratory failure (recovered after medical treatment) (Clavien– Dindo’s grade IIIa and IV, respectively) in the RA-BilA group; one case of atypical chest pain, one pulmonary embolism (successfully treated with heparin), and one selflimiting bleed in the adrenal bed (indicating an adrenal bed hematoma, detected by CT scan, that required blood transfusion but no reoperation) (Clavien–Dindo grades I, II, and II, respectively) in the PR-BilA group (P = NS). Two drains, one per side, were used in all patients who underwent PR-BilA and TL-BilA (100 %). Among the RABilA patients, drains were positioned in 4 patients (30.7 %): one drain (on the left side) in 2 patients, two drains (one per side) in the remaining two patients (P \ 0.001). Global drain volume was registered only for patients in two groups: the PR-BilA group (211 ± 134 ml; range 80–440 ml) and the TL-BilA group (241 ± 154 ml; range 80–450 ml) (P = NS). Blood transfusions were required in two patients, one in the PR-BilA group and one in the TL-BilA group. No significant difference was found in the three groups concerning time to first flatus: 1.8 ± 0.6 days (range 1–3 days) versus 1.6 ± 0.5 days (range 1–2 days) versus 2.3 ± 1.2 days (range 1–3 days) in case of RA-BilA, PR-BilA, and TLBilA, respectively (P = NS). Mean hospital stay was longer in the TL-BilA and PRBilA groups than in the RA-BilA group (12.0 ± 5.7 vs 10.8 ± 3.7 vs 4.4 ± 1.7 days, respectively) (P \ 0.001). All patients were discharged on oral corticosteroid replacement therapy. At a mean follow-up of 30.0 ± 26.5 months, 2 patients died from unrelated causes (one in the TL-BilA group and one in the PR-BilA group). No recurrence or disease-related death was registered in any group.
Discussion Patients with (ACTH)-dependent Cushing’s syndrome are debilitated from the chronic effects of cortisol overproduction. In this high-risk patient population, comparative data regarding different available approaches to perform BilA are scarce. The present study demonstrated that synchronous bilateral endoscopic adrenalectomy is safe and effective for the treatment of this particular subset of patients at high risk of perioperative complications, with no conversion in experienced centers, confirming previous studies [3, 7]. We found that operative time was significantly shorter in the PR-BilA group than in the TL-BilA and RA-BilA groups. Intraoperative and postoperative complications were similar in the three groups. The RA-BilA approach was associated with a reduced number of drains used and with shorter hospitalization duration.
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Miccoli et al. [7] had already compared the outcome of PR and TL in patients undergoing synchronous BilA for various diseases in a two-institution study. They failed to demonstrate any significant difference in the surgical outcome [7]. In recent years a simultaneous PR-BilA with two different surgical teams operating simultaneously on either side of the patient, has been proposed, in order to further reduce the operative time and, theoretically, the overall operative stress [10]. In addition, during the last decade RA has been explored as an alternative to conventional endoscopic adrenalectomy [11, 12, 20–22]. The RA approach provides a 3-dimensional display that enhances depth perception, enables the surgeon to operate in a comfortable seated position in which the eye, hand, and target are in line, and the instrumentation includes a ‘‘wrist’’ joint to improve dexterity [20]. These advantages could theoretically improve the endoscopic adrenalectomy procedure and then led to improved perioperative and postoperative outcomes. Unfortunately, these speculative advantages have not yet been demonstrated, and the cost increase also remains an important drawback associated with robotic surgery [20]. The theoretical advantages of RA for the patient in terms of perioperative and postoperative outcome and its unequivocal advantages in terms of comfort for the surgeon could be of particular interest in the case of BilA. Indeed, such procedure is usually longer, patients are frequently obese and, especially in the case of Cushing’s syndrome, at increased risk of intraoperative and postoperative complications. Moreover, adrenal glands in this group of patients are usually nestled within copious fat and in a background of very fragile tissues, which can hinder the identification of the anatomy and make the dissection more difficult [3, 4, 23]. For this reason the 3-dimensional view could theoretically permit an easier and more precise dissection in each particular situation. However, a few cases have been reported so far [24] and no comparative studies have been published on this particular subgroup of patients. We performed the present two-institution study in order to compare the results of the most broadly applied approach to BilA in patients with Cushing’s syndrome—TL-BilA—with the results of PR-BilA and RA-BilA, that could offer some theoretical advantages, as discussed above. All three of the techniques were effective in achieving an adequate surgical resection, as no persistent or recurrent diseases and no disease-related death was observed at a mean follow-up of about 30 months. Not surprisingly, one of the significant differences we found concerned operative time. Indeed, as expected, the mean operative time for PR-BilA was significantly shorter than for TL-BilA and RA-BilA. This was related to the fact that the prone position exposes both adrenal regions at the
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same time and eliminates the need to reposition the patient after the first adrenalectomy is accomplished. This repositioning time was registered only for patients undergoing RA-BilA and was about 40 min. This was in agreement with the reports in the literature. Indeed, it is well known that this step of the procedure is time consuming and significantly prolongs the operative time. In large-volume centers the operation requires *30 min, but it can be longer [3]. Moreover, the simultaneous posterior adrenalectomy implies that two different surgical teams operate at the same time on the two different sides with a further reduction of operative time for BilA [10]. The main limitations of this procedure are related to the need of having two different well-trained surgical teams working at the same time on the different sides. In other words, simultaneous PR-BilA implies that different surgeons of the same institution gain adequate experience with this approach. This requires a tertiary care referral center with a large volume of recruited patients and some senior surgeons with a quite large experience in adrenal and laparoscopic surgery who may become confident with performing PR-BilA. It is also clear that this approach necessitates a dedicated operating room team (at all levels), which includes dedicated anesthesiologists and nurses. The complexity of patient positioning and the management of two working surgical teams and equipment are minimized by having such a dedicated group. On the other hand, the mean operative time for RA-BilA tended to be shorter than that registered for TL-BilA, not only in the present series but also in the literature [3, 4]. This advantage of the RA-BilA procedure can be explained by the better visualization of the operative field and by the improved ease for the surgeon working at the console. The significant differences in operative time among the three techniques did not translate into different operative outcomes. In fact, no significant difference in terms of patient recovery (time to first flatus), intraoperative complications rate, and postoperative morbidity was observed. The only other significant differences we found among the three groups of patients were the number of drains used, which was significantly reduced in RA-BilA, and the duration of the hospital stay, which was significantly shorter after RA-BilA. However, this was likely related to different management protocols in different settings. Indeed, in one of the involved centers drains are routinely positioned after every procedure, and many patients are referred from a distance and they are kept hospitalized until a maintenance oral dose of hydrocortisone (30 mg/day) is reached and they are able to travel considerable distance back home. In the other center, drains are electively positioned on the basis of the surgeon’s discretion, and patients unable to be maintained under oral dose of hydrocortisone are referred to the endocrinology unit, shortly after surgery.
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The major limitation of the present study resides in the fact that it is a retrospective multi-institutional study. This implies the lack of information, in particular about quality of life and cost analysis. However, it is well known that robotassisted procedures are usually associated with increased costs when compared with conventional endoscopic procedures [25]. On the other hand, the costs tend to decrease as the number of procedures performed increases [22]; further reduction in costs should be expected in the future when a more competitive market is likely to develop [22]. In conclusion, although each technique might have some advantages and some limitations with respect to the others, no significant difference was found in terms of postoperative outcome among the three approaches we evaluated. In other words, the findings of the presents study were not sufficient to conclusively indicate a clear-cut advantage of one technique over the others. Conflict of interest
No conflict of interest is declared for this paper.
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