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REVIEW ARTICLE
Robot-assisted adrenalectomy: indications and drawbacks
C. Nomine-Criqui1 . A. Germain1 . A. Ayav1 . L. Bresler1 . L. Brunaud1,2
Received: 16 January 2017/ Accepted: 9 April 2017/Published online: 12 May 2017 @ Italian Society of Surgery (SIC) 2017
Abstract Adrenal tumors can vary from a benign adrenocortical adenoma with no hormonal secretion to a secretory adrenocortical malignancy (adrenocortical carci- noma) or a hormone-secreting tumor of the adrenal medulla (pheochromocytoma). Currently, laparoscopic adrenalectomy is regarded as the preferred surgical approach for the management of most adrenal surgical disorders, although there are no prospective randomized trials comparing this technique with open adrenalectomy. However, widespread adoption of robotic technology has positioned robotic adrenalectomy as an option in some medical centers. Speculative advantages associated with the use of the robotic system have rarely been evaluated in clinical settings and cost increase remains an important drawback associated with robotic surgery. This review summarizes current available data regarding robotic transperitoneal adrenalectomy including its indications, advantages, limitations, and comparison with conventional laparoscopic adrenalectomy. We believe that the use of a robotic system seems to be useful especially in more dif- ficult patients with larger tumors, truncal paragangliomas, and bilateral and/or partial adrenalectomies. Overall, we believe that overcosts due to robotic system use could be balanced by hospital stay decrease, patients’ referral increase, improved postoperative outcomes in more diffi- cult patients and ergonomics for the surgeon. However, we
also believe that the current surgical intuitive business model is counterproductive, because there are no available strong clinical data that could balance overcosts associated with the use of the robotic system.
Keywords Adrenalectomy . Robotics . Adrenal glands . Pheochromocytoma . Telerobotics . Laparoscopy
Introduction
Adrenal tumors encompass a broad spectrum of patholog- ical entities. These can vary from a benign adrenocortical adenoma with no hormonal secretion to a secretory adrenocortical malignancy (adrenocortical carcinoma) or a hormone-secreting tumor of the adrenal medulla (pheochromocytoma). Most adrenal tumors are diagnosed after they have become symptomatic-the most common presenting symptom being hypertension [1]. Currently, laparoscopic adrenalectomy (LA) is regarded as the pre- ferred surgical approach for the management of most adrenal surgical disorders, although there are no prospec- tive randomized trials comparing this technique with open adrenalectomy [2]. The acceptance of laparoscopic adrenalectomy has been primarily due to improved patient outcomes due to shorter hospitalization, reduced pain, and improved recovery. In addition, advances in surgical equipment for minimally invasive surgery and the increased familiarity of surgeons with laparoscopic tech- niques have pushed this technique to manage even complex adrenal masses. Laparoscopic transabdominal adrenalec- tomy is currently a gold standard for management of adrenal tumors. However, widespread adoption of robotic technology has positioned robotic adrenalectomy as an option in some medical centers, because this approach is
C. Nomine-Criqui
☒ c.nomine-criqui@chru-nancy.fr
1 Department of Digestive, Hepatobiliary, Endocrine, and Oncology Surgery, University of Lorraine, CHU Nancy- Brabois (Adultes), 54511 Vandoeuvre-Les-Nancy, France
2 Unité INSERM U954, Faculté de Médecine, University of Lorraine, 54511 Vandoeuvre-Les-Nancy, France
considered to be associated with superior ergonomics, a three-dimensional view of the operative field, a tremor filtration, and a “wrist” joint. Overall, all those charac- teristics have been considered to improve surgical dexter- ity. These advantages could theoretically improve laparoscopic adrenalectomy procedure and then lead to improved perioperative and postoperative outcomes. However, these speculative advantages have rarely been evaluated in clinical settings and cost increase remains also an important drawback associated with robotic surgery. Transperitoneal approach is currently the main surgical approach to perform laparoscopic adrenalectomy. Conse- quently, this review summarizes current available data regarding robotic transperitoneal adrenalectomy (RA) including its indications, advantages, limitations, and comparison with the conventional laparoscopic adrenalec- tomy [1-5].
Methods
A literature review was performed using PUBMED to identify relevant studies from 2001 to January 2017. We used the following keywords for this search: “adrenalec- tomy”; “robotics”; and “laparoscopy”. Those searches were restricted to publications in English and human sub- jects. A total of 115 studies were identified, reporting the technique and perioperative outcomes of robotic assisted adrenalectomy. The principles of the Helsinki declaration were followed in this review.
Learning curve and operative time
Learning curve is defined as the number of cases required to achieve similar outcomes compared to laparoscopic adrenalectomy. The threshold of 20 robotic adrenalectomy cases has been reported in previous series [6-10]. Different studies showed a significant decrease in terms of operative time between initial cases and the latest operated patients in those series. In a prospective study, we observed that
operative time decreased significantly between the 50 first cases and the 45 last cases (from 101 to 88 min) and that this decrease was particularly significant for junior sur- geons (surgeons with less than 20 laparoscopic adrenalec- tomies prior to study) from 123 to 97 min for junior surgeons and from 90 to 81 min for senior surgeons [9]. Similarly, D’Annibale et al. showed in a study including 30 patients that operative times decreased significantly dif- ference between the five first cases and the last five cases (296 min versus 168 min, P = 0.013) [11]. For Pineda- Solís et al. and You et al., mean operative time was longer in robotic group patients and this difference was attributed to docking time [12, 13]. We believe that docking time should taken into account in comparative studies between RA and LA, because it can increase mean operative time by 15-40 min and can be as long as 1 h during the first cases. We observed that surgeon experience, first assistant training level and tumor size remained independent factors associated with mean operative time [5, 9].
Perioperative outcomes (morbidity and mortality)
Results of different available studies are summarized in Table 1. Mean postoperative morbidity rates were from 0 to 20% and conversion rates from 0 to 11% (Tables 1, 3). Most frequent reasons for conversion were local adherence of the tumor to the surrounding organs and intraoperative bleeding. Technical difficulties have also been reported [5]. We believe as others that conversion rate for robotic approach seems to decrease with surgical experience [5, 14]. Mean causes for postoperative morbidity as mostly Clavien 1 and 2 complications and severe complications leading to reoperation are unfrequent [9, 15] (Table 3). Overall, morbidity and mortality rates are considered to be comparable between the conventional laparoscopic and robotic-assisted adrenalectomy [4, 16] (Table 2). Conse- quently, no superiority has been clearly proved so far in terms of postoperative morbidity rate for robotic-assisted adrenalectomy. However, we believe that large randomized studies are still lacking.
| Authors | Patients | Robotic operative time (min) | Morbidity (%) | Mortality (%) | Conversion rate (%) | Hospital stay (days) |
|---|---|---|---|---|---|---|
| Pineda-Solís et al. [12] | 30 | 189 ± 32 | 0 | 0 | 0 | 1.3 ± 0.5 |
| D'Annibale et al. [11] | 30 | 231.1 (180-330) | 10 | 0 | 3.3 | 5.2 (2-11) |
| Agcaoglu et al. [18] | 24 | 159 ± 13 | 0 | 0 | 4 | 1.4 ± 0.2 |
| You et al. [13] | 15 | 208.2 (120-320) | 13.3 | 0 | 0 | 5.86 (4-7) |
| Aliyev et al. [42] | 26 | 149 (96-291) | 0 | 0 | 3.9 | 1.2 ± 1 |
| Brandao et al. [17] | 30 | 120 | 20 | 0 | 0 | 2 |
| Morelli et al. [19] | 41 | 177 | 4.8 | 0 | 0 | 3.3 |
| Authors | Patients | Laparoscopic operative time (min) | Morbidity (%) | Mortality (%) | Conversion rate (%) | Hospital stay |
|---|---|---|---|---|---|---|
| Pineda-Solís et al. [12] | 30 | 160 ± 41 | 0 | 0 | 3.3 | 1.9 ±2 |
| Agcaoglu et al. [18] | 38 | 187 ±8 | 2.7 | 0 | 11 | 1.9 ± 0.1 |
| You et al. [13] | 8 | 181.1 (74-270) | 25 | 0 | 0 | 6.7 (5-9) |
| Aliyev et al. [42] | 42 | 178 (80-320) | 10 | 2.5 | 7.5 | 1.7 ± 1 |
| Brandao et al. [17] | 46 | 120 | 11 | 0 | 2.3 | 2.1 |
| Morelli et al. [19] | 41 | 207.1 | 4.8 | 0 | 2.4 | 3.4 |
Comparative studies between robotic and conventional adrenalectomy
Several studies have been published comparing the two approaches and the results are conflicting [12, 13, 17]. Results are summarized in Table 2. Agcaoglu et al. com- pared the two approaches especially for tumors with a size >5 cm and showed that mean operative time was shorter in robotic group patients (159 min versus 187 min, P = 0.043) [18]. For Brandao et al., operative time was similar in the two groups, but tumor size was higher in laparoscopic group patients (3 cm versus 4 cm, P = 0.002) [17]. Recently, Morelli et al. showed in a case control study that operative time was significantly shorter in robotic group, and especially for patients with tumors >6 cm, with BMI
30 kg/m2, and in patients with previous surgery. Con- version rate was also lower in robotic group patients [19]. In a recent literature review including eight studies com- paring robotic versus laparoscopic approach, Teo and Lim concluded that mean operative time was shorter or similar in robotic group patients [5]. In a similar manner, mean hospital stay was also shorter after robotic-assisted adrenalectomy [5]. However, we believe that this decrease in terms of hospitalization duration may also be due to a chronological bias [20].
Capsular disruption has been reported in large tumors with the robotic approach, especially in patients with large pheochromocytoma (diameter ranging from 6 to 7.5 cm) [9, 10]. However, those results are likely similar in patients who undergo the conventional laparoscopic adrenalectomy [4]. Patients’ quality of life after robotic adrenalectomy has been evaluated [21]. In this study, the two techniques were compared at three times points across ten different quality- of-life measures. This study concluded that perioperative quality of life was globally similar between the two approaches.
Based on available literature, it appears that robotic assisted and conventional laparoscopic adrenalectomy does not have significant advantages over one another.
However, we believe that robotic approach may be potentially superior in some specific situations: obese patients, large tumors, and patients with previous abdominal surgery [8].
Adrenalectomy in obese patients
This impact of patient’s obesity on perioperative outcomes during and after adrenalectomy is controversial and avail- able studies are scarce [8, 9]. Aksoy et al. included 99 morbidly obese patients (BMI >30 kg/m2) who underwent adrenalectomy. Forty-two robotic adrenalectomies were compared to 57 laparoscopic adrenalectomies [22]. All perioperative outcomes were similar between the two groups. However, conversion rate was 0% in the robotic group versus 5.2% in the laparoscopic group patients (n = 3, P = 0.006). This study concluded that difficulties observed during the conventional laparoscopic adrenalec- tomy in obese patients were nullified when using the robotic system in those patients.
In a recent retrospective case-control study, Morelli et al. compared 41 robotic adrenalectomies to 41 laparo- scopic conventional adrenalectomies [19]. This study showed that robotic approach seemed to decrease mean operative time in obese patient (BMI >30 kg/m2) [19].
In a video, Maker et al. showed the technique of robotic left adrenalectomy in an obese patient (mean weight 99 kg and mean BMI 36 kg/m2) [23]. This video concluded that robotic adrenalectomy is feasible and safe in obese patients with large tumor adhering to oncological principles.
Overall, those data confirm our previous study showing that robotic approach may offer advantages in obese patients with no specific technical difficulty in patients with BMI >30 kg/m2 [9]. In conclusion, perioperative outcomes in obese patients are still controversial, but some data suggest that robotic approach is safe in those patients without a significant increase of postoperative morbidity rate in comparison with the conventional laparoscopic approach.
| Authors | N | Operative time (min) | Morbidity (%) | Intra-operative event | Mortality (%) | Hospitalization stay (days) |
|---|---|---|---|---|---|---|
| Winter et al. [41] | 30 | 185 | 7 | – | 0 | 2 |
| Brunaud et al. [9] | 100 | 95 | 10 | – | 0 | |
| 1 wound infection | ||||||
| 1 facial edema 3 pneumonia | ||||||
| 2 urinary tract infection | ||||||
| 1 post-operative anemia | ||||||
| 1 hematoma | ||||||
| Giulianotti et al. | 42 | 118 ± 46 | 2.4 | 1 capsular disruption (6 cm | 2.4 | 4 |
| [10] | 1 clostridium difficile infection | pheochromocytoma) | Myocardial infarct | |||
| Nordenström et al. [15] | 100 | 109.5 | 13 | – | 0 | |
| D'Annibale et al. | 30 | 231 ± 46 | 10 | 1 capsular disruption | 0 | 5.2 (2-11) |
| [11] | 1 abdominal wall hematoma | 1 intra operative hemodynamic instability | ||||
| 1 pneumonia | ||||||
| 1 myocardial infarct | ||||||
| Morelli et al. [19] | 41 | 177.2 | 4.8 | 1 lesion of inferior vena cava | 0 | 3.3 |
| 1 pneumonia | 1 lesion of left renal vein | |||||
| 1 supra ventricular tachycardia |
Adrenalectomy in patients with large tumors
Adrenal tumors with large diameter (pheochromocytoma and adrenocarcinoma) are associated with frequent diffi- culties during laparoscopic resection. The two main risks are intraoperative capsular effraction and subsequent potential oncologic issue with local recurrence [16, 24]. This controversy has become less of an issue as specialized teams have gained experience and skill over time. At present, the threshold of what is considered to be “large” varies from 5 to 10 cm with a consensus of 6 cm [25-27]. In addition, endocrine surgeon expertise has become a relevant factor to avoid those difficulties and we believe that conversion to laparotomy should not be considered as a failure.
Several studies showed that adrenalectomy is feasible with both laparoscopic and robotic approaches in patients with large adrenal tumor. Some data emphasized that RA was more appropriate in this situation. Morelli et al. showed that mean operative time was shorter in robotic group patients with tumor diameter >6 cm [19]. In a review, Teo and Lim concluded that adrenalectomy was feasible in patients with larger tumors [5]. They also added that robotic approach was associated with decreased mean operative time in this subgroup of patients. Because
resection of large adrenal tumors can be challenging in restricted retroperitoneal space, they recommended to avoid robotic retroperitoneal approach in patients with larger tumors and to prefer the use of a transperitoneal approach in those patients.
Thompson et al. used the Swedish database including 659 adrenalectomies (37.9% were robotically assisted) to evaluate the role of robotic approach in patients with large tumors [28]. In this nationwide database, robotic approach was used in larger tumors preferentially. Those data sug- gest that there may be some benefits to use the robotic system in those patients and that it could avoid conversion to laparotomy with the corresponding postoperative increased morbidity. However, different conclusions have been reached by other authors. In a recent literature review, Ball et al. reported that no prospective studies have been published on robotic approach in patients with large tumor including adrenocortical carcinoma [4]. Furthermore, results of retrospective studies comparing laparoscopic versus open approach for adrenocortical carcinoma were still controversial. Consequently, they concluded that while laparoscopic approach seemed to be feasible in selected cases without any adjacent organs involvement, open approach should be still preferred to laparoscopic or robotic approach for adrenocortical carcinoma. In this
review, they did not recommend robotic approach for large tumors [4]. Overall, we believe that robotic adrenalectomy is well appropriate to obese patients and those with larger tumors. However, the use of the robotic system does not exempt surgeons from following simple oncological prin- ciples that have been already validated in adrenal surgery for years.
Robotic partial adrenalectomy
Partial adrenalectomy is considered as an option to spare adrenal parenchyma in some patients with familial pre- disposition (pheochromocytoma, aldosterone, or cortisol producing adenoma) [2]. After laparoscopic partial adrenalectomy, it is considered that about 9% of patients developed local recurrence over time and 86% of them do not require routine steroid supplementation [20, 24, 29, 30]. We believe that the robotic system is particulary interesting in those patients, because it provides a three-dimensional display. Since the first report published in 2006, case series and studies including less than 15 have been published [30, 31]. Only two studies included more than ten patients and are available currently. Asher et al. reported 15 partial adrenalectomies for pheochromocytoma with one conversion (6.6%) [30]. In this series, there were no recurrence and no patient required routine steroid sup- plementation. Boris et al. also studied 13 partial adrenalectomies with one patient converted to open sur- gery. In this experience, one patient required steroid replacement and no recurrence was detected with a 16.2 month median follow-up [31]. Overall, we believe that recent studies emphasize that partial adrenalectomy is feasible and safe with encouraging functional and onco- logic postoperative outcomes. However, further compara- tive, large, and prospective studies are needed to provide stronger data comparing robotic versus laparoscopic partial adrenalectomy.
Paraganglioma robotic resection
Paragangliomas are located in the thorax and/or the abdo- men in 30% of cases and appropriate management corre- sponds to complete surgical resection [29, 30]. We believe that the robotic system is well adapted to paragangliomas resection, because those tumors are mostly benign and often located in narrow and remote anatomical locations [2]. Although not consensual, laparoscopic approach has been used by some surgical teams and can be considered as a first option to manage truncal paragangliomas [32-34]. Only few papers evaluating paraganglioma robotic resec- tion are currently available. Further studies are needed to evaluate the role of the robotic system in patients with paraganglioma.
Bilateral adrenalectomy
The majority of patients who required bilateral adrenalectomy present a persistent Cushing disease after failed hypophysectomy or ectopic ACTH production. This procedure can also be indicated for bilateral pheochro- mocytoma in patients with NEM 2 and Von Hippel Lindau syndrome, for adrenal gland metastasis, and for congenital adrenal hyperplasia. No significant difference was clearly observed between transperitoneal laparoscopic versus robotic approach in patients who undergo bilateral adrenalectomy [35]. Because patient positioning is a lat- eral decubitus position during transperitoneal bilateral adrenalectomy, one of the main difficulties is the time duration needed to re-position the patient between the two sides. Interestingly, two studies evaluated bilateral adrenalectomies with a retroperitoneal approach and no patient repositioning was needed [36]. In Raffaelli et al.’s study, mean operative time was shorter for the retroperi- toneoscopic approach with no significant difference regarding intraoperative and postoperative complication rates [37]. No recurrence or disease-related death was registered. Further studies are also needed to better evaluate the role of the robotic system in this surgical indication using transperitoneal or retroperitoneal approaches.
Laparoscopic single site surgery (less)
Preliminary data on robotic single-site adrenalectomy are available. Lee et al. reported 33 procedures with 5 con- versions to laparoscopy and 2 conversions to open surgery [38]. In this study, the surgeon learning curve was asso- ciated with shortened operative times and not increased complication rates. In a recent retrospective multicentric study, Pavan et al. included 737 adrenalectomies from 14 medical centers. Most adrenalectomies were performed using the conventional laparoscopy (46%), but the robotic system represented about 11% of all procedures. Interest- ingly, LESS represented 36% of patients [39].
Costs
Overcosts associated with the use of the robotic system likely explain that laparoscopic conventional adrenalec- tomy is still more developed and frequently used world- wide. Bodner et al. estimated that robotic adrenalectomy was 1.5 times more expansive than laparoscopic adrenalectomy [40]. Other studies have tried to estimate actual costs for robotic adrenalectomy, but different con- clusions have been observed: from no cost difference to 2.3 times more expansive in patients after robotic adrenalec- tomy in other studies [9, 41].
Conclusions
Since its first description, about 120 studies have been published to evaluate the role of the robotic system to perform an adrenalectomy. Most of them were retrospec- tive and none were randomized controlled trials. In most cases of adrenal tumors, robotic and conventional laparo- scopic adrenalectomy has similar perioperative outcomes [3]. We believe that the use of a robotic system seems to be useful especially in more difficult patients with larger tumors, truncal paragangliomas, and bilateral and/or partial adrenalectomies. Overall, we believe that overcosts due to robotic system use could be balanced by hospital stay decrease, patients’ referral increase, improved postopera- tive outcomes in more difficult patients, and ergonomics for the surgeon [3]. However, we also believe that the current surgical intuitive business model is counterpro- ductive, because there are no available strong clinical data that could balance overcosts associated with the use of the robotic system. Ultimately, this may stop the development of robotic adrenalectomy in the near future. Finally, the development of robotic adrenalectomy may also be dependent upon country specific characteristics. Thus, Pavan et al. showed that the robotic approach was adopted largely in the USA and European medical centers mostly adopted laparoscopic conventional approaches [39].
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of interest.
Research involving human participants and/or animals This article does not contain any studies with human participants or ani- mals performed by any of the authors.
Informed consent For this type of study formal consent is not required.
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