Comparison of laparoscopic transabdominal lateral versus posterior retroperitoneal adrenalectomy

Comparison of laparoscopic transabdominal lateral versus posterior retroperitoneal adrenalectomy Eren Berber, MD, Gurkan Tellioglu, MD, Adrian Harvey, MD, Jamie Mitchell, MD, Mira Milas, MD, and Allan Siperstein, Cleveland, OH

Background. For the past 14 years, we have been performing laparoscopic adrenalectomy via the lateral transabdominal as well as the posterior retroperitoneal approach. The aim of this study is to describe patient selection criteria for each approach with comparison of perioperative outcomes. Methods. In patients with smaller tumors, low body mass index (BMI), history of previous abdominal operations, appropriate body habitus, and bilateral pathology, we have performed preferentially the posterior approach. Data regarding clinical pathology, tumor size, BMI, estimated blood loss (EBL), operating time (OT), morbidity, mortality, and duration of stay were analyzed retrospectively. Data are expressed as mean ± standard error of the mean (SEM). Results. One hundred seventy-two laparoscopic adrenalectomy procedures were performed in 159 patients between 1994 and 2008. The lateral approach was used in 69 patients (right side: 39%, left side: 55%, bilateral: 6%) and the posterior approach in 90 patients (right side: 42%, left side: 48%, bilateral: 10%). The incidence of prior abdominal surgery was greater in the posterior group (26% vs 19%, NS). The lateral approach was used in 9% (3/34) of aldosteronoma, 38% (9/24) of Cushing’s disease/syndrome, 47% (18/38) of nonsecreting cortical adenoma, 66% (23/35) of pheochromocytoma, 41% (7/17) of malignant lesions, and 73% (8/11) of others. Thirty percent of the bilateral adrenalectomies were performed via lateral and 70% via posterior approach. Two patients in the posterior approach were converted to the laparoscopic lateral approach, and 2 patients in the lateral approach were converted to open. Overall, patient age and sex were similar between groups. BMI was higher in patients undergoing adrenalectomy via lateral vs posterior approach (32.4 vs 28.4; P = .005). Tumor size was larger than 6 cm in 11 (16%) and 1 (1%) of the patients in the lateral and posterior groups, respectively. On univariate analysis, mean OT for lateral and posterior approaches was similar for unilateral cases (157 ± 7 vs 138 ± 6 min, respectively; P = NS). This was also true on multivariate analysis when corrected for patient selection factors. EBL was 35 ± 7 mL for lateral versus 25 ± 6 mL for posterior approach (P = .05). The duration of stay in lateral and posterior approaches was 1 day in 56% vs 82%, 2 days in 29% vs 13%, and more than 2 days in 15% vs 5% of the patients, respectively. Two patients in the lateral group died postoperatively because of cardiac and pulmonary causes, and 2 patients in the posterior group developed temporary neuralgia. Conclusion. This series compares 2 different approaches for laparoscopic adrenalectomy. Our study shows that the lateral and posterior techniques have a similar peri-operative outcome when patients are selected for each option based on certain criteria. (Surgery 2009;146:621-6.) From Section of Endocrine Surgery, Endocrinology and Metabolism Institute, Cleveland Clinic, Cleveland, OH

DESPITE THE INTRODUCTION OF THE LATERAL TRANSABDO(LT) AND POSTERIOR RETROPERITONEAL (PR) AP-

MINAL

PROACHES FOR LAPAROSCOPIC ADRENALECTOMY IN A SIMILAR TIME FRAME, THE

LT

ADRENALECTOMY

has been more

Accepted for publication June 30, 2009. Reprint requests: Eren Berber, MD, Section of Endocrine Surgery, The Cleveland Clinic, Endocrinology and Metabolism Institute, 9500 Euclid Avenue A80, Cleveland, OH 44195. E-mail: [email protected]. 0039-6060/$ - see front matter Ó 2009 Mosby, Inc. All rights reserved. doi:10.1016/j.surg.2009.06.057

popular among surgeons because of the presence of identifiable landmarks and overall surgeon familiarity with intraperitoneal laparoscopic surgery.1,2 Nevertheless, the PR technique provides a direct access to the adrenal gland without intra-abdominal dissection and may be preferable in patients with prior abdominal surgery. For the past 14 years, we have been performing laparoscopic adrenalectomy via the LT, as well as the PR approach. In 2000, we reported an established technique for laparoscopic PR adrenalectomy using laparoscopic ultrasound in 31 patients.3 SURGERY 621

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Table I. Demographic and clinical data Age (years) Sex (F:M) BMI Side Right Left Bilateral Previous abdominal surgery Pathology Aldosteronoma Cushing’s Nonsecreting adenoma Pheochromocytoma Malignant Other Size <6 cm >6 cm

Lateral transperitoneal (n = 69)

Posterior retroperitoneal (n = 90)

P value

52 ± 14 (44:25) 32 ± 9

51 ± 14 (47:43) 28 ± 6

NS NS .005 NS

27 38 4 13

38 43 9 23

3 9 18 23 7 9

31 15 20 12 10 2

58 11

89 1

.05 .005

.005

A recent interest has taken place in the PR approach by many centers reporting their experience.4-6 Overall, a clear superiority of the PR over the LT approach has not been demonstrated.4,7-10 With seemingly equivalent outcomes, it seems prudent to examine these operative procedures from the perspective of appropriate patient selection and selective use. The aim of this study is to describe patient selection criteria for each approach with comparison of perioperative outcomes. METHODS We reviewed the records of all patients undergoing laparoscopic adrenalectomy at the Cleveland Clinic, Section of Endocrine Surgery, from 1994 to 2008. Data were extracted from an Institutional Review Board-approved database. We reviewed the preoperative data with respect to patient selection. Data extracted included patient age, sex, body mass index (BMI), operative history, tumor size, side of disease, bilateral versus unilateral involvement, characteristics on computed tomography, and clinical diagnosis. In addition, information regarding perioperative course was extracted. Specific data points were operative time, estimated blood loss, conversion to open, and peri-operative mortality and complications. Operative time defined as time from initial incision to application of dressings and estimated blood loss were extracted from the anesthesia record. The remainder of the data points were recorded from the operative note and inpatient charts.

Lateral transperitoneal laparoscopic adrenalectomies were all performed in the lateral decubitis position. Posterior retroperitoneal procedures were performed in the prone jackknife position. Left transperitoneal and all posterior retroperitoneal procedures were initiated with a 3-port technique. A fourth port was added at the discretion of the operating surgeon. Right transperitoneal procedures used 4 ports routinely, because of an additional port for retraction of the liver. Both procedures have been well described previously in the literature.11 All data are expressed as mean and standard error of the mean. Comparisons were made using Student t test, Chi-square test, and logistic regression analysis using JMP 7.0 software (SAS Institute, Cary, NC). The level of statistical significance was set at P < .05. RESULTS During the last 14 years (1994--2008), 172 laparoscopic adrenalectomies were performed in 159 patients. Of these procedures, the PR approach was used in 90 patients and the LT approach in 69. Patient and disease characteristics are shown in Table I. Age and sex distribution were not significantly different between the 2 groups. BMI was greater in the LT group (32.4 vs 28.4; P = .005). Side of the diseased gland was similarly distributed among the 2 groups. The incidence of previous abdominal surgery was higher in the PR group (26%) versus the LT group (19%) (P = .05).

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Table II. Perioperative data Lateral transperitoneal (n = 69) Estimated blood loss (mL) Operative time (min) Conversion Duration of stay 1 day 2 days >2 days Mortality Neuralgia

Posterior retroperitoneal P (n = 90) value

35 ± 7

25 ± 6

.05

157 ± 7

138 ± 6

NS

2

2

39 20 10 2 0

74 12 4 0 2

.05

NS NS

The PR approach was used on a greater proportion of aldosterone-secreting tumors (91%) and Cushing’s syndrome/disease (63%) patients and a lower portion of pheochromocytomas (34%) (P = .005). Tumor size was 4.4 ± 0.3 cm (range, 1--14 cm) in the LT versus 2.8 ± 0.1 cm (0.4--7 cm) in the PR group (P < .0001). Tumors larger than 6 cm were more commonly removed using the LT approach (16% vs PR 1%). Peri-operative outcomes are shown in Table II. Operative times were calculated and compared for unilateral cases only. This analysis revealed similar times between the 2 approaches (157 ± 7 min LT vs 138 ± 6 min PR; P = NS). A slightly greater estimated blood loss was observed in the lateral compared with the posterior retroperitoneal approach (35 ± 7 mL LT vs 25 ± 6 mL PR; P = .05). Analysis of the duration of hospital stay revealed that a larger portion of those undergoing the lateral approach stayed longer than 1 day prior to discharge (LT 43%, PR 18%). Conversion from the PR to the LT approach was required in 2 patients. Both of these conversions occurred during the initial learning curve and were related to the establishment of PR space, which was not able to be developed in a satisfactory manner with the balloon to proceed with the dissection. In the first patient, the initial trocar was placed more lateral than usual and in the second patient, the body habitus with abundant retroperitoneal fat, precluded a reasonable space to be created. The second was related to maintenance of the PR space. In addition, 2 patients in the LT group required conversion to an open procedure. In both of these patients, the cause was bleeding from the adrenal vein on the vena cava that required suturing, which we elected to do open. Two patients in the LT group died postoperatively from cardiac and pulmonary causes. No patients died

within 30 days of the operation in the PR group. Two patients had temporary postoperative neuralgia, both in the PR group. DISCUSSION One year after the LT adrenalectomy was reported, Mercan et al2 described the technique performing the procedure via an PR approach using a balloon dissector to create a potential space. Our group reported subsequently a modification of the Mercan technique with the addition of percutaneous and laparoscopic intraoperative ultrasound.3 Subsequently, Walz et al6 described using greater insufflation pressures to maintain the operative fields without disturbing hemodynamic stability. With this large experience, we showed that the LT and PR techniques have a similar perioperative outcome when patients are selected based on certain criteria. Overall, we selected patients with smaller tumors (<6 cm) and previous abdominal operations for the PR approach. Likewise, we favored the PR approach in patients with lower BMIs, aldosteronomas, Cushing’s, and bilateral pathologies. Several patients had small (1--2 cm) tumors who underwent adrenalectomv through an LT approach in this series, because the body habitus of these obese patients with thick subcutaneous back tissue made the manipulation with the rigid laparoscopic instruments difficult. Likewise, bilateral LT adrenalectomies were also performed in some patients because of the same reasons. The abundant retroperitoneal fat in the patients made the establishment and maintenance of the potential space difficult. Although it is difficult to give exact numeric values, for these reasons, the surgeon should be wary of doing a PR approach in a patient with a BMI >35 and thick posterior back soft tissue planes (>4 cm between the skin and Gerota’s space). Once mastered, the PR technique provides direct exposure to the adrenal gland without the limitation caused by the liver and spleen with the LT technique, which can sometimes be significant and require zealous retraction, especially of the liver. Familiarity with the retroperitoneal anatomy, however, and having a mentor for the initial cases are crucial to avoid catastrophes. There is a steeper learning curve to the PR than the LT technique. In our opinion, the learning curve involves 20 patients. Positioning using a Wilson frame is important to relax the abdomen; otherwise the operative field will collapse frequently during the operation. Some groups have advocated using high pressures (20 mm Hg) to keep the space open, but the disadvantage is increasing the pCO2 with higher pressures. We prefer to keep the insufflation

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pressure at 15 mm Hg. Establishing the retroperitoneal space and placement of all 3 trocars is the most critical part of the case. For surgeons experienced with optical trocars, this first step could be done without the need for a cut down to the fascia. It is important to use the kidney as a landmark to prevent inadvertent trocar injuries. For others, a cut-down technique to the Gerota’s space will be safer. Even when a cut-down technique is used for the entry of the first trocar, we have found the use of optical trocars to insert the 2nd and 3rd trocars very useful. Doing a percutaneous ultrasonography with the patient in the prone position before prepping a patient helps identifying landmark structures such as the 12th rib and the kidney to guide these port placements. Our group added the use of the laparoscopic ultrasound to Mercan et al’s initial description of the technique, which we believe adds both safety and efficacy to the procedure.2 In contrast, the benefit of the ultrasound for adrenocortical hyperplasia cases is limited in regards to finding the adrenal gland but still can guide safe dissection by showing the landmarks. In this study, we recommended a posterior approach in patients anticipated to have substantive intra-abdominal adhesions involving the periadrenal dissection planes. Although the comfort level with a trans-abdominal laparoscopic approach could be different for each surgeon in a given patient based on laparoscopic skills, we have favored the PR approach in patients with multiple prior abdominal operations or an ipsilateral upper quadrant open incision. We do not consider minor laparoscopic procedures, such as laparoscopic cholecystectomy, to constitute a contra-indication for the LT procedure. Another technical caveat in selecting the appropriate patients for the PR approach is the relationship of the 12th rib with the adrenal gland. When the adrenal gland is too cephalad compared with the 12th rib, this decreases dexterity at the tip of the rigid laparoscopic instruments and can make the case very difficult. Likewise, in patients with a thicker section of soft tissue between the skin and the Gerota’s space, laparoscopic manipulation with the current rigid instruments is very difficult and we tend not to use this approach in such patients. Being skilled in LT adrenalectomy is a prerequisite to develop a PR adrenalectomy program. We recommend mastering this technique before embarking on PR adrenalectomy. Our experience with the LT technique enabled us to keep the case laparoscopic in 2 patients who initially had an attempted PR adrenalectomy. We prefer to use the LT approach in patients with larger tumors, higher

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BMIs, and without a history of extensive abdominal operations. The fact that we had to convert to an open procedure in 2 patients also emphasize that for a comprehensive adrenal surgery program, the surgeon needs to know how to do an open adrenalectomy even at the current era of advanced laparoscopic surgery. Because pathology was not an absolute criterion to determine the operative approach, pheochromocytomas were removed by both laparoscopic approaches in our study. Despite the concerns, we did not notice any hemodynamic instability with the posterior approach to such tumors. This requires gentle creation of the potential space when using the balloon dissector. Moreover, we also believe that stringent pre-operative placement of the patients on alpha blockade helped with the safety of the procedures. Literature supports that in the setting of adequate pre-operative alpha blockade these concerns may be unfounded. In this study, Zhang et al12 performed retroperitoneal laparoscopic adrenalectomies on 58 pheochromocytomas in 56 patients. No excess peri-operative morbidity or mortality was noted, and significant intra-operative fluctuations in blood pressure were observed in a minority of cases similar to more traditional approaches. Operative time, estimated blood loss, and conversion rates were comparable with those published in the literature.4,6-10,13,14 Although trends toward lesser blood loss and shorter operative times in the retroperitoneal approach were observed, it is difficult to draw conclusions from these findings given the nonrandomized nature of the study. Thus, as is the case in previously published literature, a clear superiority of 1 approach cannot be supported. Peri-operative morbidity and mortality were extremely low. Two patients died in the LT group, 1 from a cardiac cause and the other from pulmonary complications. In addition, 2 patients in the PR group developed painful but temporary neuralgia. Given the low rates of adverse outcomes and nonrandom selection of procedure in each patient, it is not possible to compare these outcomes appropriately across procedures. Rather, a more generalized conclusion that both procedures are appropriately safe seems warranted. Although the hospital stay also seems to be slightly shorter with the PR approach, this needs to be validated in a randomized study. Although these data represent a large series of laparoscopic adrenalectomies using both trans- and retroperitoneal approaches, the patients were not randomized, and the 2 groups cannot be considered

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equivalent for the purpose of comparing perioperative outcomes. Although blood loss was better marginally in the PR group, this would be expected given the larger tumor size in the LT patients.15 Also, the trend toward greater operative times in the LT group may simply reflect tumor size and a greater proportion of pheochromocytoma.15,16 In conclusion, the mastery of 2 laparoscopic adrenalectomy techniques have enabled us to treat a large number of patients with a wide spectrum of adrenal disorders with high patient and surgeon satisfaction. Despite the current opinion, the LT and PR approaches are complementary, not competitive, to each other when certain patient selection criteria are followed. REFERENCES 1. Gagner M, Lacroix A, Bolte E. Laparoscopic adrenalectomy in Cushing’s syndrome and pheochromocytoma. N Engl J Med 1992;327:1033. 2. Mercan S, Seven R, Ozarmagan S, Tezelman S. Endoscopic retroperitoneal adrenalectomy. Surgery 1995;118:1071-5. 3. Siperstein AE, Berber E, Engle KL, Duh QY, Clark OH. Laparoscopic posterior adrenalectomy: technical considerations. Arch Surg 2000;135:967-71. 4. Giger U, Vonlanthen R, Michel JM, Krahenbuhl L. Transand retroperitoneal endoscopic adrenalectomy: experience in 26 consecutive adrenalectomies. Dig Surg 2004;21:28-32. 5. Perrier ND, Kennamer DL, Bao R, Jimenez C, Grubbs EG, Lee JE, et al. Posterior retroperitoneoscopic adrenalectomy: preferred technique for removal of benign tumors and isolated metastases. Ann Surg 2008;248:666-74. 6. Walz MK, Alesina PF, Wenger FA, Deligiannis A, Szuczik E, Petersenn S, et al. Posterior retroperitoneoscopic adrenalectomy---results of 560 procedures in 520 patients. Surgery 2006;140:943-8. 7. Lezoche E, Guerrieri M, Feliciotti F, Paganini AM, Perretta S, Baldarelli M, et al. Anterior, lateral, and posterior retroperitoneal approaches in endoscopic adrenalectomy. Surg Endosc 2002;16:96-9. 8. Naya Y, Nagata M, Ichikawa T, Amakasu M, Omura M, Nishikawa T, et al. Laparoscopic adrenalectomy: comparison of transperitoneal and retroperitoneal approaches. BJU Int 2002;90:199-204. 9. Rubinstein M, Gill IS, Aron M, Kilciler M, Meraney AM, Finelli A, et al. Prospective, randomized comparison of transperitoneal versus retroperitoneal laparoscopic adrenalectomy. J Urol 2005;174:442-5. 10. Suzuki K, Kageyama S, Hirano Y, Ushiyama T, Rajamahanty S, Fujita K. Comparison of 3 surgical approaches to laparoscopic adrenalectomy: a nonrandomized, background matched analysis. J Urol 2001;166:437-43. 11. Berber E, Duh QY, Clark OH, Siperstein AE. A critical analysis of intraoperative time utilization in laparoscopic adrenalectomy. Surg Endosc 2002;16:258-62. 12. Zhang X, Lang B, OuYang JZ, Fu B, Zhang J, Xu K, et al. Retroperitoneoscopic adrenalectomy without previous control of adrenal vein is feasible and safe for pheochromocytoma. Urology 2007;69:849-53. 13. Dudley NE, Harrison BJ. Comparison of open posterior versus transperitoneal laparoscopic adrenalectomy. Br J Surg 1999;86:656-60.

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14. Tai CK, Li SK, Hou SM, Fan CW, Fung TC, Wah MK. Laparoscopic adrenalectomy: Comparison of lateral transperitoneal and lateral retroperitoneal approaches. Surg Laparosc Endosc Percutan Tech 2006;16:141-5. 15. Castillo OA, Vitagliano G, Secin FP, Kerkebe M, Arellano L. Laparoscopic adrenalectomy for adrenal masses: does size matter? Urology 2008;71:1138-41. 16. Humphrey R, Gray D, Pautler S, Davies W. Laparoscopic compared with open adrenalectomy for resection of pheochromocytoma: a review of 47 cases. Can J Surg 2008;51: 276-80.

DISCUSSION Dr Judiann Miskulin (Indianapolis, IN): One of the questions that is important in defining is, how would you approach a patient in whom it is determined has an initially undiagnosed adrenal cancer via the posterior approach? Dr Eren Berber (Cleveland, OH): In this series we had a number of malignancies. Interestingly, we only had 1 adrenocortical cancer. The patient had a tumor which was approached laterally. In that patient we did not anticipate and we did not have any evidence on preoperative imaging there was any invasion of the surrounding structures. And in our opinion and to make it a little easier, a patient that we suspect to have adrenocortical cancer, I would personally approach with an open technique so that I can get wider margins with a more radical resection. So if I anticipate a patient is going to have adrenocortical cancer, I would go with an open operation. Dr Judiann Miskulin (Indianapolis, IN): How does the BMI influence your approach? Do you find it difficult in patients with Cushing’s who have a large amount of retroperitoneal fat to provide a good dissectional plane? Dr Eren Berber (Cleveland, OH): I think that’s a problem with both techniques. But still I find that those patients when they are approached with the posterior technique, I think the procedures are done more easily. And I would like to open up the issue about the BMI. It’s not actually BMI, but how much soft tissue the patients have in their posterior back on top of and posterior to the adrenal gland, because if that tissue is thick, it’s really difficult with the current laparoscopic instruments. The BMI obviously correlates with that. But most importantly, we look at how thick that soft tissue in the back posterior to the adrenal gland. Dr Judiann Miskulin (Indianapolis, IN): And since the original description of the posterior approach, you have added the addition of a preoperative ultrasound to define your anatomy. Are there any other additional features that you found to be influential in having a good outcome from this approach? Dr Eren Berber (Cleveland, OH): The largest series in the world is actually from Germany---560 patients were he reported. The authors advocated using an insufflation pressure of 20 millimeters Mercury at all times. We use that selectively, and only if I have difficulty establishing the space, I will increase the pressure to 20. But other than that, the technique has been straightforward, and that’s why we were able to get good results.

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Dr Richard A Prinz (Chicago, IL): I enjoyed the paper very much, and especially the main conclusion is that if you are going to be doing adrenal surgery, you should be doing both of these types of approaches. My questions first deal with technique. You describe using a balloon dissector and also doing intraoperative or preoperative ultrasound. Do you think these are really that essential? Because we first started using the balloon dissector and no longer use that and have not really used ultrasound and did not find it an advantage. Secondly, I would ask about your deaths. We have had 2 deaths also in our series of over 200, and they have all been in patients who developed complications after having a pheochromocytoma resected. Are your deaths in patients with the pheochromocytomas? Dr Eren Berber (Cleveland, OH): We have not tried not using the balloon dissector. Sometimes I don’t get a good dissection with the balloon when it is inserted more laterally than usual and I struggle a lot. I think the balloon dissector helps keeping the space open and defining the adrenal gland. Regarding ultrasound, when Mercan first described his technique, he did not use ultrasound either. We have a special academic interest in laparoscopic ultrasound, and that’s why we added this modification. And I can tell that it helps with identification of the kidney and the adrenal gland, especially in the learning curve and makes the operation safer In bilateral hyperplasia cases , I still think that finding the kidney and identifying either the aorta or venacava adds some safety to the procedure. Regarding the patients who died---1 patient had bad pulmonary hypertension

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which was underestimated pre-operatively. The patient had actually a nonsecreting cortical adenoma and she died postoperatively from significant pulmonary hypertension. The other patient died from ischemic heart disease. Again this was not a pheochromocytoma case but was related to a cardiac complication. Dr L. Michael Brunt (St. Louis, MO): I would like to pin you down a little more about the BMI. A lot of patients I see in my practice are BMI of 35 or higher. Are you doing the retroperitoneal approach in that patient population? Secondly, learning curve issues. Are residents able to adapt and learn this technique without all the familiar landmarks as easily as the lateral approach? Then finally, have you shifted towards preferentially doing the retroperitoneal approach for most patients with adrenal tumors now? Dr Eren Berber (Cleveland, OH): Regarding the BMI---I had to use those parameters to have some kind of comparison. But I agree with you: in those patients with higher BMIs, we tend to use the lateral technique. But for patients with BMIs in the 25 to 35 range, we look at how thick the posterior back soft tissue is---to decide if the patient will be a candidate for the posterior approach or not. For the residents and the fellows, it is difficult for them to recognize the landmarks. I think this is a training issue. We have to do more cases to make them more comfortable with the technique. We like doing posterior adrenalectomies, and when a patient presents, we first see if he/she is a candidate for the posterior approach by using the criteria outlined in this paper.