robotic versus laparoscopic resection of large adrenal tumors

ORIGINAL ARTICLE – ENDOCRINE TUMORS

Robotic Versus Laparoscopic Resection of Large Adrenal Tumors

Orhan Agcaoglu, MD, Shamil Aliyev, MD, Koray Karabulut, MD, Jamie Mitchell, MD,

Allan Siperstein, MD, and Eren Berber, MD

Division of Endocrine Surgery, Endocrinology and Metabolism Institute, Cleveland Clinic, Cleveland, Ohio

ABSTRACT

Background. Although recent studies have shown the

feasibility and safety of robotic adrenalectomy, an advan-

tage over the laparoscopic approach has not been

demonstrated. Our hypothesis was that the use of the robot

would facilitate minimally invasive resection of large

adrenal tumors.

Methods. Adrenal tumors C5 cm resected robotically

were compared with those removed laparoscopically from

a prospective institutional review board-approved adrenal

database. Clinical and perioperative parameters were ana-

lyzed using t and chi-square tests. All data are expressed as

mean ± standard error of mean.

Results. There were 24 patients with 25 tumors in the

robotic group and 38 patients with 38 tumors in the lapa-

roscopic group. Tumor size was similar in both groups

(6.5 ± 0.4 [robotic] vs 6.2 ± 0.3 cm [laparoscopic],

P = .661). Operative time was shorter for the robotic ver-

sus laparoscopic group (159.4 ± 13.4 vs 187.2 ± 8.3 min,

respectively, P = .043), while estimated blood loss was

similar (P = .147). The conversion to open rate was less in

the robotic (4%) versus the laparoscopic (11%) group;

P = .043. Hospital stay was shorter for the robotic group

(1.4 ± 0.2 vs 1.9 ± 0.1 days, respectively, P = .009). The

30-day morbidity was 0 in robotic and 2.7% in laparoscopic

group. Pathology was similar between groups.

Conclusions. Our study shows that the use of the robot

could shorten operative time and decrease the rate of

conversion to open for adrenal tumors larger than 5 cm.

Based on our favorable experience, robotic adrenalectomy

has become our preferred minimally invasive surgical

approach for removing large adrenal tumors.

The first published robotic adrenalectomy (RA) was by

Piazza et al. about a patient with Conn’s syndrome who

underwent right adrenalectomy using the ZEUS AESOP in

1999.1 In the same year, Hubens et al. also reported a case

in which a left adrenalectomy was performed with

AESOP.2 While these studies were reported from Europe,

the first application of robotic system for adrenalectomy in

the United States was reported in pigs at the Cleveland

Clinic.3 After the approval by the U.S. Food and Drug

Administration (FDA) of the da Vinci system for use in

general surgical procedures in July 2000, Horgan and

Vanuno reported 34 advanced general surgical procedures

(including a single bilateral adrenalectomy) that were per-

formed with using the da Vinci system.4 Since then,

numerous case reports and series have been published in the

literature to describe the safety and feasibility of RA.5–10

The majority of studies in the literature describe the

technical aspect of robotic surgery. However, studies

comparing the outcomes of robotic versus laparoscopic

procedures are needed to clearly define the role of robotic

surgery.4,11,12 For robotic adrenalectomy, no benefit over

the laparoscopic approach has been demonstrated in the

comparison studies to date.5,13

Our group has had an extensive experience with lapa-

roscopic adrenalectomy. During this experience, we

acknowledged that dissection with rigid laparoscopic

instruments in the posterior retroperitoneal (PR) technique

in general and removal of large tumors with the lateral

transabdominal (LT) approach were cumbersome. In 2008,

our group established a robotic endocrine surgery program

and developed techniques for various surgical procedures.

We identified that the PR technique and LT adrenalectomy

for large adrenal tumors could potentially benefit from the

use of the robot. We previously reported our results

regarding the robotic PR technique.14 The aim of this study

is to compare the robotic versus laparoscopic approach for

resecting adrenal tumors[5 cm. Our hypothesis was that

the use of the robot would facilitate minimally invasive

resection of these large adrenal tumors.

� Society of Surgical Oncology 2012

First Received: 7 October 2011;

Published Online: 7 March 2012

E. Berber, MD

e-mail: [email protected]

Ann Surg Oncol (2012) 19:2288–2294

DOI 10.1245/s10434-012-2296-4

MATERIALS AND METHODS

Between 2000 and 2011, 219 patients with 233 tumors

underwent adrenalectomy at the Division of Endocrine

Surgery at the Cleveland Clinic. In 70 patients (30%),

tumor size was larger than 5 cm in diameter. Of these, 8

patients with tumor size[15 cm, and/or concerning fea-

tures for malignancy on preoperative imaging, underwent

open adrenalectomy. Of the remaining patients, laparo-

scopic adrenalectomy (LA) was performed in 38 patients

with 38 tumors and RA in 24 patients with 25 tumors

(Figs. 1, 2). The patient with bilateral tumors in the robotic

group had bilateral adrenalectomy performed in 2 separate

stages. These latter 2 groups were compared regarding age,

gender, body mass index (BMI), approach (LT or PR), side

(right/left), tumor diameter, history of previous abdominal

surgery, operative time (OT), estimated blood loss (EBL),

hospital stay, and pathology. All patients after the onset of

the robotic adrenalectomy in October 2008 were approa-

ched robotically, except for situations when the equipment

was not available. After October 2008, 74 out of a total of

105 adrenalectomies were done robotically at our center. In

both the robotic and laparoscopic technique, all tumors

[6 cm were removed through an LT approach. For tumors

\6 cm, decision for a LT or PR approach was made based

on body habitus and the history of previous abdominal

procedures that have been previously reported in detail.15

All procedures were done by the 3 surgeons in the study

(E.B., J.M., A.S.).

Data were extracted from a prospectively maintained

institutional review board (IRB)-approved database. The

data were analyzed using JMP 9.0.0 (SAS, Cary, NC)

software. Analyses were performed using t test, chi-square,

and univariate regression. Those parameters with a

significance of less than P\ .30 on univariate analysis

were entered into a multivariate regression model. The

number of instrument changes for robotic versus laparo-

scopic adrenalectomy was calculated from video

recordings. All results were expressed as mean ± standard

error of mean (SEM). Data of those patients converted to

open (n = 5) were excluded from OT analyses. Statistical

significance was defined as P\ .05.

Surgical Technique

Our techniques have been described in detail previ-

ously.14–16 All procedures were performed under general

anesthesia. The patients were placed on a lateral decubitus

position using a bean bag for the LT and on a prone

jackknife position over a Wilson frame for the PR

approach. The port placement was the same for both lap-

aroscopic and robotic procedures for a given approach. For

the LT approach, 4 trocars were placed underneath the

FIG. 1 CT scan of a patient with a 7.2-cm right adrenal mass. This

was resected laparoscopically through a transabdominal lateral

approach

FIG. 2 a CT scan of a patient with bilateral pheochromocytoma,

measuring 5 cm on the right and 7 cm on the left (arrows). In this

patient, both adrenal masses were resected robotically in 2 separate

stages. b Intraoperative photo showing the robotic dissection of the

left adrenal vein in the same patient

Robotic Resection of Large Adrenal Tumors 2289

costal margin for both right and left adrenalectomy. The

robotic procedures were performed using a camera and 2

working arms. On the right side, the most medial port was

made the first assistant’s port to retract the liver and suc-

tion, whereas on the left side, the most lateral trocar was

used as the first assistant’s port in general. For the PR

procedures, 3 incisions below the 12th rib were used, with

no additional first assistant ports.

RESULTS

RAwas performed on 24 patients with 25 tumors, and LA

was performed on 38 patients with 38 tumors. The 2 groups

were similar regarding age, gender, and diagnosis (Table 1).

BMI was less in the RA group (27.1 ± 0.8) compared with

the LA group (30.2 ± 0.9); P = .029. Tumor size was

similar in both groups (6.2 ± 0.3, range 5–15 cm [LA

group], vs 6.5 ± 0.4, range 5–10.2 cm [RA group],

P = .661). Skin-to-skin OT was significantly shorter in the

RA (159.4 ± 13.4 min) compared with the LA group

(187.2 ± 8.3 min); P = .043. Estimated blood loss was less

for RA versus LA (83.6 ± 59.4 vs 166.6 ± 51.2 cc,

respectively, P = .147). The number of instrument changes

were 14 ± 2 in the robotic and 34 ± 4 in the laparoscopic

group (P = .001). The conversion to open rate was signifi-

cantly higher in the LA (4 of 38, 11%) versus theRAgroup (1

of 25, 4%); P = .043. The causes of conversion in the LA

group were bleeding from an accessory left renal vein

(n = 1) (Fig. 3), bleeding from the adrenal (n = 1), adher-

ence of tumor to inferior vena cava (n = 1), and difficulty

with the dissection plane (n = 1),whereas in theRAgroup, 1

case was converted to open as a result of adherence of tumor

to the renal hilum. There was no mortality. Morbidity was 0

in the robotic and 2.7% in the laparoscopic group, including

the patientwith injury to the left accessory renal vein thatwas

converted to open.

On univariate analysis, the robotic versus laparoscopic

procedure (P = .043) and BMI (P = .064) affected skin-to-

skin OT (Table 2). The presence of 2 staff surgeons versus 1

staff plus a resident or fellow was analyzed in this univari-

ate analysis, but was not found to affect OT (P = .840).

Overall, 2 staff surgeons versus 1 staff surgeon plus a res-

ident or fellow were present in 50% and 50% of the robotic,

and 53% and 47% of the laparoscopic cases, respectively,

(P = .825). On multivariate analysis, the only parameter

that remained significant was the type of procedure (robotic

versus laparoscopic) (P = .048) (Table 3).

Hospital stay was shorter for the robotic group versus

the laparoscopic group (1.4 ± 0.2 vs 1.9 ± 0.1 days,

TABLE 1 Demographic and clinical parameters in the study

Parameters Laparoscopic Robotic P value

(n = 38) (n = 24)

Age 52.5 ± 2.3 52.4 ± 2.9 .987

BMI 30.2 ± 0.9 27.1 ± 0.8 .029

Gender (female/male) 20/18 14/10 .642

Side (right/left) 13/25 9/16a .771

Approach (LT/PR) 32/6 18/7a .039

Tumor size (cm) (range) 6.2 ± 0.3 6.5 ± 0.4 .661

(5–15) (5–10.2)

Previous abdominal surgery 10 (27%) 7 (29%) .932

Operative time (minute)

(range)

187.2 ± 8.3 159.4 ± 13.4 .043

(85–290) (64–357)

EBL (cc) 166.6 ± 51.2 83.6 ± 59.4 .147

Hospital stay (day) 1.9 ± 0.1 1.4 ± 0.2 .009

Conversion to open 4 1 .043

Pathologya .167

Pheochromocytoma 15 8

Nonsecreting ACA 7 7

Complex cyst 3 5

Cushing 5 1

Otherb 8 4

Continuous data are expressed as mean ± SEM

SEM standard error of mean, BMI body mass index (kg/m2), LT lateral

transabdominal, PR posterior retroperitoneal, EBL estimated blood

loss, ACA adrenocortical adenomaa For these parameters, the number of tumors, not patients, was

givenb Other includes adrenocortical carcinoma (n = 1), lymphangioma

(n = 1), and schwannoma (n = 2) in the robotic, and cystic lym-

phangioma (n = 1), hematoma (n = 1), lipoma (n = 1), myelolipoma

(n = 1), schwannoma (n = 1), aldosteronoma (n = 1), and adreno-

cortical carcinoma (n = 2) in the laparoscopic group

FIG. 3 CT scan of a patient with a 15-cm left-sided pheochromo-

cytoma, which shows the close relationship of the mass (arrow) with

the left adrenal vein. This case was started laparoscopically, but

converted to open as a result of bleeding from the accessory left renal

vein

2290 O. Agcaoglu et al.

respectively, P = .009). There was 1 case of adrenocortical

carcinoma (ACC) in the robotic and 2 in the laparoscopic

group. There was no evidence of invasion to surrounding

structures or lymphadenopathy on preoperative imaging in

these cases, and therefore adrenalectomy was approached

minimally invasively. Among these 3 cases, 1 of the lap-

aroscopic patients was converted to open as a result of

difficulty with the dissection plane. In each case, the

tumors were resected to clear margins. The robotic patient

died at 18 months with systemic multifocal recurrence in

the absence of local recurrence despite adjuvant mitotane

chemotherapy. The patient in whom the case was com-

pleted laparoscopically developed recurrence within the

adrenalectomy bed at 6 months, as well as lung metastasis,

and underwent local resection and chemotherapy. He is

alive at 49 months within stable lung metastases. The last

patient converted to open from laparoscopic received

mitotane chemotherapy after resection and is currently

alive at 9 months with no evidence of recurrence on

imaging studies.

DISCUSSION

In this study, we showed that RA shortens OT and

decreases the rate of conversion to open compared with

LA, for adrenal tumors larger than 5 cm. Laparoscopic

adrenalectomy for large adrenal masses ([5 cm) is chal-

lenging because of concerns for malignancy, technical

difficulty, and potential for complications. However, mul-

tiple studies have concluded that laparoscopic resection of

adrenal tumors larger than 5–8 cm is feasible and safe in

experienced hands. Currently, it is generally accepted that

these cases can be approached laparoscopically and con-

verted to open if local invasion is identified during the

laparoscopic procedure.17–21

The advances in robotic instrumentation have encour-

aged general surgeons to consider using the robot for many

intra-abdominal procedures that are already done well

laparoscopically. Adrenalectomy is such a procedure

that is very safely and effectively done laparoscopically.

Although, a number of studies have reported the feasibility

of robotic adrenalectomy, an advantage over the laparo-

scopic procedure has not been demonstrated when all cases

are compared.14,22–24 The critical difference between

robotic and laparoscopic surgery is in essence related to the

fact that the robotic instruments are wristed, whereas lap-

aroscopic are rigid. Therefore, it is difficult to demonstrate

a benefit of the robot for removing small tumors that are

very straightforward with the laparoscopic technique, since

most robotic series also include the learning-curve factor.

We foresaw that the most significant benefit of the robot

could be for removing large adrenal tumors and rendering

the posterior retroperitoneal technique more ergonomic.

We previously reported our favorable experience with the

robotic PR technique.14 In this study, we have demon-

strated a benefit of the robot for removing large adrenal

tumors in terms of OT and shorter hospital stay. We

believe that the reasons the OT was shorter were related to

the fact that the robotic instruments and the three-dimen-

sional view made dissection faster—as we were able to get

into difficult angles around the tumor more easily—and

TABLE 2 Univariate analysis of skin-to-skin operative time in the

study patients

Parameter Operative time P value

Age .328

[65 174.2 ± 15.0

\65 185.4 ± 10.1

Gender .947

Female 178.5 ± 12.0

Male 184.3 ± 12.6

BMI NA .064

Tumor size NA .283

Tumor type .252

Pheochromocytoma 183.7 ± 70.2

Others 171.5 ± 71.6

Approach .158

Lateral 179.4 ± 10.3

Posterior 168.7 ± 17.1

Procedure type .043

Laparoscopic 187.2 ± 8.3

Robotic 159.4 ± 13.4

Side .673

Right 184.0 ± 16.6

Left 179.0 ± 10.4

First assistant .840

Staff 169.1 ± 10.9

Fellow/resident 175.4 ± 12.3

Body mass index and tumor size were taken as continuous values

BMI body mass index

TABLE 3 Multivariate analysis of skin-to-skin operative time

Parameters P value

BMI .209

Tumor size .407

Approach .654

Procedure type .048

Tumor type .725

Approach refers to ‘‘lateral transabdominal versus posterior retro-

peritoneal’’ and procedure type ‘‘robotic versus laparoscopic.’’

BMI body mass index


more accurate, so that we had to spend less time with

hemostasis after adrenalectomy was completed. There were

also fewer instrument changes and less of a need to clean

the camera because of the more stable robotic setup. The

difference in hospital stay is clinically small, and we

believe that needs to be investigated in future studies.

Body mass index was smaller and the percentage of

the posterior approach was higher in the robotic versus

the laparoscopic group in our study. Although these

differences theoretically could be responsible for the

shorter OT in the robotic group, we showed that on

multivariate analysis, the robotic approach independently

affected OT.

One criticism to the shorter OT with the robotic

approach could be that the setup of the robotic system

would take additional time, therefore invalidating these

time savings. It is true that the transport of the robotic unit

to the operating room, booting of the system, calibration of

the robotic camera, and draping of the robotic arms can

take up to 20–25 min. This is in addition to the docking

time, which involves attachment of the robotic arms to the

trocars, and insertion of the robotic instruments to the field.

These did not add to the skin-to-skin OT in the current

study, as we keep the robot in a dedicated operating room

and do the other preparations of the robot during either

induction of anesthesia or the laparoscopic portion of the

procedure. Therefore, there was no additional prolongation

of the OT due to robotic setup in our study.

Robotic adrenalectomy has received increased attention

in the recent years.3,7–9,14,25 However, there is a paucity of

reports comparing LA and RA. In the largest comparison

study to date, Brunaud et al. reported that RA (n = 50) was

associated with lower blood loss (49 mL) but longer

operative times (104 min) (P\ .001) compared with LA

(n = 50). However, the difference in operative time was

not significant after the learning curve of 20 cases.13 In this

study, for tumors larger versus smaller than 5.5 cm, mean

operative time was longer in the LA group (100 vs 80 min,

P = .009), but not in the RA group. In another study, the

same authors analyzed quality of life in 33 patients who

underwent laparoscopic (n = 14) and robotic adrenalec-

tomy (n = 19). They noted that the morbidity rate was

similar in both groups and that the mean OT was 86 ± 7.8

and 107 ± 6.6 min, respectively.26 Morino et al. reported a

prospective randomized clinical trial comparing RA and

LA in 2004.5 In this study, they showed that in 4 of 10

robotic patients, conversion to the laparoscopic procedure

was required. They also noted that laparoscopic adrenal-

ectomy was superior to the robotic adrenalectomy

regarding total OT (115.3 min, range 95–155 min, vs 169.2

min, range 136–215 min, respectively, P\ .001).5

Recently, Giulianotti et al. reported on 42 patients who

underwent robot-assisted TL adrenalectomy. In this study

postoperative morbidity was 2.4% and mortality 2.4%,

with a median hospital stay of 4 days.9

In our opinion, experience with laparoscopic adrenal

surgery and skill in robotic procedures are mandatory for

preventing complications. In the literature, causes of con-

version to laparoscopic or open adrenalectomy from

robotic surgery have been reported to be due to visceral

injury, difficulty in hemostasis, malposition of robotic

trocars, and prolonged operation time.5,13,22

The drawbacks of RA are increased cost of surgical

equipment and longer operative times during the learning

curve. In our study, we were able to achieve 28 min of time

savings and zero morbidity with the robotic technique. We

believe that these good results are related to our prior large

laparoscopic adrenalectomy and other ongoing robotic

general surgical experience with thyroidectomy, parathy-

roidectomy, and hepatectomy procedures. However, 2 of

the 3 surgeons in the study (J.M. and A.S.) were in their

learning curve, which means that time saving with robotic

adrenalectomy could be even greater for surgeons beyond

the learning curve.

The management of adrenocortical cancer laparoscopi-

cally is controversial. In our series, adrenocortical cancer

was resected to clear margins laparoscopically in 2 patients

and robotically in 1 patient. Of our 3 patients, 1 has

developed local recurrence at the adrenalectomy bed at

6 months and 2 patients distant metastasis. In the literature,

there is a controversy regarding laparoscopic resection of

ACC. In 2010, Miller et al. reported a study comparing

laparoscopic (n = 17) versus open (n = 71) resection of

ACC. In this study, the incidence of positive margins or

intraoperative tumor spillage was 50% for the laparoscopic

and 18% for the open group (P = .01). Local recurrence

was observed in 25% of the patients in the laparoscopic and

20% in the open group (P = .23).27 On the other hand, in

another study of 43 patients with stage 1 and 2 ACC,

recurrence rate was 64% after open and 50% after lapa-

roscopic adrenalectomy (P = NS).28 In the largest study to

date, Brix et al. compared 35 patients undergoing LA and

117 patients open adrenalectomy for ACC. In this study,

disease-free survival was similar between study groups

(P = .69). The frequency of tumor capsule violation and

peritoneal carcinomatosis was comparable between study

groups. In 12 of 35 patients of the LA group, procedure

was converted to open with no impact on the clinical

outcome. The authors concluded that, for localized

ACC B 10 cm, LA by an experienced surgeon was not

inferior to open adrenalectomy regarding oncologic out-

comes.29 We believe that LA for large tumors, without

preoperative suggestion for malignancy (i.e., local inva-

sion, lymph nodes) on imaging, can be done, as long as

surgical oncologic principles, such as wide resection and

keeping the capsule intact, are followed. In none of our


patients was there any capsule violation or tumor con-

tamination of the abdominal cavity. In our practice, we

approach patients with preoperative suggestion of ACC

through an open procedure up front. These patients were

not included in this study.

There were 15 patients with pheochromocytoma resec-

ted laparoscopically and 8 patients robotically in our series.

We did not notice any differences in hemodynamics

between the 2 approaches. In Giulianotti et al.’s series,

there were 9 patients with pheochromocytoma. One of

these patients was reported to have a capsular tear intra-

operatively, and another developed clostridium difficile

colitis.9

In our previous report of the first 50 robotic adrenalec-

tomy cases, we noted that the presence of 2 staff surgeons

versus 1 staff and resident/fellow was associated with

shorter OT for robotic lateral, but not for robotic posterior

adrenalectomy.30 In this study, we did not demonstrate this

parameter to affect OT for removal of large adrenal tumors.

This could be related to the fact that our previous report

reflects our learning curve, where the experience of the first

assistant had a greater impact on the conduct of the

operation.

In summary, we have demonstrated that the use of the

robot could provide advantages over the laparoscopic

approach for removing adrenal tumors larger than 5 cm. To

our knowledge, this is the first subgroup of patients with

adrenal tumors who have been identified to benefit from

robotic surgery. We believe that comparative studies are

absolutely necessary to define the role of robotic surgery

for various general surgical procedures.

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robotic versus laparoscopic resection of large adrenal tumors

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