Laparoscopic trans- and retroperitoneal adrenal surgery for large tumors

Ayman Agha1 , Igors Iesalnieks1,3, Matthias Hornung1 , Wiggermann Phillip2 , Andreas Schreyer2 , Michael Jung2, Hans J Schlitt1

1Departments of Surgery and 2Radiology, University Hospital Regensburg, Regensburg, 3Department of Surgery, Marienhospital Gelsenkirchen, Gelsenkirchen, Germany

Address for correspondence: Prof. Ayman Agha, Department of Surgery, University of Regensburg Medical Center, Franz-Josef-Strauss- Allee 11, Regensburg - 93053, Germany. E-mail: ayman.agha@klinik.uni-regensburg.de

Abstract

BACKGROUND: Laparoscopic adrenalectomy for tumors larger than 6 cm is currently a matter of controversial discussion because of difficult mobilization from surrounding organs and a possible risk of capsule rupture. MATERIALS AND METHODS: Data of consecutive patients undergoing laparoscopic adrenalectomy between 1/1994 and 7/2012 were collected and analysed retrospectively. Intra- and postoperative morbidity in patients with tumors ≤6 cm (group 1, n = 227) were compared to patients with tumors >6 cm, (group 2, n = 52). RESULTS: Incidence of adrenocortical carcinoma was significantly higher in group 2 patients (6.3% vs. 0.4%, P=0.039) whereas the incidence of aldosterone-producing adenoma was lower (2% vs. 25%, P = 0.001). Mean duration of surgery was longer (105 min vs. 88 min, P = 0.03) and the estimated blood loss was higher (470 mL vs. 150 mL) in group 2 patients. Intraoperative bleeding rate (5.7% vs. 0.8%, P = 0.041), and the conversion rate were significantly higher (5.7% vs. 1.3%, P = 0.011) in group 2. Also, postoperative complication rate was significantly higher in group 2 (11.5% vs. 3.0%, P = 0.022). However, only two major complications occurred, one in each group. CONCLUSION: Minimally invasive adrenal surgery can be performed by an experienced surgeon even in patients with large tumors (>6 cm) with an increased but still acceptable intra- and postoperative morbidity.

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DOI: 10.4103/0972-9941.129943

Key words: Adrenocortical carcinoma, laparoscopic adrenalectomy, postoperative complications

INTRODUCTION

Laparoscopic surgery has developed to a standard of care in patients with small (<6 cm) adrenal masses. Recently, numerous authors reported on minimally invasive adrenalectomies also in patients with larger tumors,[1-6] but significant concerns regarding the adequacy of laparoscopic surgery in potentially malignant adrenal tumors still exist. Furthermore, malignancy can not always be ruled out preoperatively. Therefore, minimally invasive surgery of large adrenal tumors has to follow oncological principles:

1. Sufficient resection margins,

2. Intact tumor capsule,

3. No tumor cell dissemination, and

4. No risk for port site metastases.[7-9]

In the present study, intra- and postoperative morbidity were analysed retrospectively in patients with tumor size ≤6 cm and compared to patients with tumors larger than 6 cm undergoing minimally invasive trans- or retroperitoneal adrenalectomy.

MATERIALS AND METHODS

All 279 patients undergoing laparoscopic trans- or retroperitoneal adrenal surgery between 1994 and 2012 were included in this retrospective analysis. Patients were separated in 2 groups: Patients with tumor size ≤6 cm (group 1), and patients with larger tumors (group 2). Intra- and postoperative morbidity after adrenal surgery was analysed for the two groups.

Agha, et al .: Laparoscopic adrenalectomy for large tumors

Between 1994 and 2003, all surgeries included in present analysis were performed by the transperitoneal approach. After 2003, the decision to perform an adrenalectomy by a trans- or by a retroperitoneal approach was guided by the size of the tumor and by the body-mass-index (BMI).[10] Patients with tumors larger than 6 cm and a BMI of >40 kg/m2 underwent a transperitoneal adrenalectomy; all others underwent adrenalectomy by a retroperitoneoscopic approach.

Patients with aldosterone-producing adenomas had been treated preoperatively with 200-400 mg/d of spironolactone for 6 weeks. Patients with pheochromocytoma had received alpha-receptor inhibitor during the last 10 preoperative days.

Laparoscopic Transperitoneal Technique

Patients are brought in 45°-60° lateral flank position. Three trocars are used for left adrenalectomy, an additional trocar is used to retract the liver for right adrenalectomy. The intra-abdominal pressure is kept at 12 mm Hg. For left adrenalectomy, the left colonic flexure is mobilized along the Gerota fascia. Dissecting through the avascular plain between the pancreatic tail and the kidney, the spleen and the pancreatic tail are moved medially. In right adrenalectomy, the liver is mobilized along the lateral border of the inferior vena cava to control potential bleeding. Subsequently, the adrenal vein is identified and divided. The fat tissue surrounding the adrenal gland is left in place to avoid tumor manipulation. Dorsal mobilization of the tumor is performed, and followed by lateral and cranial mobilization. The adrenal gland and the surrounding fat tissue are removed en bloc with a retrieval bag.

Retroperitoneoscopic adrenalectomy is performed in prone position. The procedure is started by a 1 cm incision below the 12th rib. Subsequently, fibers of the quadratus lumborum muscle are spread digitally and the perirenal fascia is opened from dorsal. After reaching the retroperitoneal space, this area is dilated with the forefinger. Operation starts with a retroperitoneoscopic exploration and insertion of three trocars. After blunt preparation of the retroperitoneal space, the operation is continued by dissection of the retrorenal fat tissue from the renal capsule at the upper renal pole. After visualization of the inferior vena cava at the right side and identification of the renal vein at the left side, the adrenal vein is divided. Subsequently, dorsal, lateral and cranial mobilization of the tumor is performed. The adrenal gland and the surrounding fat tissue are removed en bloc with a retrieval bag.

Statistics

Comparisons between patient groups were made using Fisher’s exact test for categorical variables. The Wilcoxon

signed rank test was employed for the evaluation of the distribution patterns. Using the t-test, P-value of <0.05 were regarded as statistically significant.

RESULTS

Between 1/1994 and 7/2012, 279 patients underwent laparoscopic trans- and retroperitoneal adrenalectomies: Tumor size was ≤6 cm in 227 cases (group 1) and >6 cm in 52 cases (group 2). Patients’ and tumor characteristics are shown in [Table 1]. In group 1, significantly more patients presented with aldosterone-producing adenomas (25% vs. 2%, P = 0.001). The incidence of the adrenocortical carcinoma was higher in group 2 patients (6.3% vs. 0.4%, P = 0.039). There were no statistically significant differences regarding other indications [Table 2].

Significantly more patients underwent transperitoneal adrenalectomy in group 2 than in group 1 (71% vs. 32%, P = 0.023, Table 3). Single-incision laparoscopic adrenalectomies (SILS) were performed only in group 1 patients. Duration of surgery was significantly longer (105 min vs. 88 min, P = 0.03) and the estimated blood loss was significantly higher (470 mL vs. 150 mL) in group 2 patients.

Three intraoperative bleedings occurred in group 2 patients (5.7%) as opposed to two bleedings in group 1 (0.8%, P = 0.041, Table 4) leading to one conversion in a group 2 patient.

Table 1: Patients' and tumor characteristics
VariableTumor ≤6 cm (N= 227)Tumor >6 cm (N= 52)P-Value
Age, mean (range)52 (16-83)55 (28-76)0.123
Gender (M:F)124/10332/200.010
BMI, kg/m2 Mean (range)27.8 (21-46)25.5 (18-34)0.121
Tumor localization
Right, n (%)98 (43.2)21 (40.5)0.242
Left, n (%)129 (56.8)31 (59.5)
Tumor size, cm mean±SD3.2+/-1.710.1+/-2.10.001
Table 2: Pathological characteristics
VariableTumor ≤6 cm (N= 227)Tumor >6 cm Total (N= 52)P-Value
Incidentaloma48 (21.1)13 (27.6)61n.s
Conn's syndrom57 (25.1)1 (2.1)580.001
Cushing tumors47 (20.7)8 (17.0)55n.s
Pheochromocytoma45 (19.8)11 (23.4)56n.s
Ganglioneuroma6 (2.6)4 (7.6)9n.s.
Myelolipoma13 (5.7)5 (10.6)18n.s
Adrenal metastasis10 (4.4)3 (6.3)13n.s
Adrenocortical1 (0.4)3 (6.3)40.039
carcinoma

Agha, et al .: Laparoscopic adrenalectomy for large tumors

Table 3: Surgical procedures and operative outcomes
VariableTumor ≤6 cm Tumor >6 cm P-Value (N = 227) (N= 52)
Surgical procedures, n (%)
Transperitoneal, lateral57 (25.1)29 (55.7)0.023
approach
Transperitoneal, anterior15 (6.6)8 (15.3)0.021
approach
Retroperitoneoscopic141 (62.1)15 (28.8)0.003
SILS14 (6.1)00.031
Mean operative time, min88+/-56105+/-510.03
Estimated blood loss, mL150+/-55470+/-1300.002
Blood transfusion, n (%)2 (0.8)1 (2.1)0.78
Length of hospital stay, days7.5+/-3.58.2+/-4.50.30

SILS = Single-incision laparoscopic adrenalectomy

Table 4: Intra- and postoperative complications
VariablesTumor ≤6 cm (N = 227)Tumor >6 cm (N = 52)P-Value
Intraoperative bleeding,2 (0.8)3 (5.7)0.041
n (%)
Tear of adrenal vein11
Clip dislocation01
Injury of adrenal capsule10
Injury of inferior cava vein01
Conversion, n (%)3 (1.3 %)3 (5.7%)0.011
Bleeding from10
surrounding fat
Inadequate visualization11
Technical difficulties01
Postoperative7 (3.0)6 (11.5)0.022
complications, n (%)
Hematoma12
Acute cardiac failure10
Pneumonia31
Pancreatic fistula01
Wound infection12
12th rib subcostal neuralgy*72

*Only in patients undergoing retroperitoneoscopic adrenalectomy

The conversion rate was significantly higher in group 2 than in group 1 (5.7% vs. 1.3%, P = 0.011, Table 4). Also, postoperative complication rate was significantly higher in group 2 than in group 1 (11.5% vs. 3.0%, P = 0.022). However, only two major complications occurred: An acute cardiac failure in a group 1 patient and one pancreatic fistula treated conservatively in a group 2 patient.

DISCUSSION

The current study presents a large patient population undergoing laparoscopic adrenalectomy for large (>6 cm) tumors. As it might have been expected, intra- and postoperative morbidity was slightly higher in patients with larger tumors, however, the complication rate of 11.5% was still acceptable. Only one patient developed a

major complication and no patient needed revision surgery. Moreover, morbidity and complication rates of up to 27% were observed following open adrenalectomy[11,12] and this was accompanied by prolonged hospital stay, more pain at the incision site and an increased risk of postoperative hernias.

Expertise in Laparoscopic Adrenal Surgery

Due to a close anatomical relation to spleen, kidney, liver and inferior caval vein, laparoscopic adrenal surgery for large tumors is technically demanding. Injury to the adrenal capsule is associated with increased probability of relevant consequences in patients with larger tumors: 23% of group 2 patients presented with pheochromocytoma and 12% had a malignant disease. Therefore, surgeons undertaking laparoscopic adrenalectomy in this particular population should have a large experience in laparoscopic adrenal surgery. Experience with other, particularly with gastrointestinal laparoscopic procedures might shorten the learning curve.[2,13] In the present study, 86.5% of the adrenalectomies for tumors >6 cm were performed by the first author of the study (A.A.) after an experience of 127 laparoscopic adrenalectomies and already twelve years experience in laparoscopic colorectal surgery.[14]

Own Strategy to Endoscopic Technique

Retroperitoneoscopic adrenalectomy in patient with very large tumors might pose serious additional technical difficulties because of a limited operative field. In obese patients, the prone positioning will lead to even more compression of the retroperitoneal space in spite of high insufflation pressure. Thus, laparoscopic transperitoneal adrenalectomy by a lateral approach is preferred in case of tumors larger than 8 cm and in patients with BMI >40 kg/m2 at our institution. Conventional adrenalectomy is reserved for cases with clear radiological signs of malignancy (invasion of surrounding structures, evidence of metastases) and was performed only in 8 cases since 2005.

Morbidity and Conversion

In our study, duration of surgery was longer and blood loss was slightly larger in patients with tumors >6 cm as compared to patients with smaller adrenal masses. Similar findings have been reported by others.[6,15_18] Some recent publications indicated that laparoscopic adrenalectomy can be performed safely for tumors up to 15 cm.[1,2,16,19]. Tsuru et al.[16] found no statistically significant difference regarding blood loss, time of surgery and complication rate between patients with tumors <5 cm (n = 155) and patients with larger tumors (n = 23), however, their study was smaller. The authors of the latter study recommended that invasion

Agha, et al .: Laparoscopic adrenalectomy for large tumors

of adjacent structures should serve as an only indication for conventional adrenalectomy.

Tumor size and the surgeon’s experience are both factors affecting the conversion rate.[6,20-22] The conversion rate of 5.7% was higher in group 2 patients in our study. However, it should be weighed against the fact that almost 95% of patients with large adrenal tumors still benefited from the laparoscopic approach. Nevertheless, one should not hesitate to convert to conventional adrenalectomy if oncological principles cannot be maintained safely.

Management of Intraoperative Bleeding

Increased risk of intraoperative bleeding is a serious concern when laparoscopic adrenalectomy is performed in a patient with large tumor. Causes of bleeding can be: Injuries to adrenal capsule, problems to close the adrenal vein or tears in the inferior cava or renal vein [Table 4]. We recommend to dissect the adrenal gland together with the adjacent fat instead of preparation beneath the adrenal capsule. This strategy might prevent injury to and bleeding from the adrenal capsule and diminish the risk of organ manipulation in patients with pheochromocytoma. Possible presence of a second adrenal vein should be kept in mind during medial dissection. In case of serious bleeding during a retroperitoneoscopic adrenalectomy, insufflation pressure can safely be increased to 25 mm Hg without any risk of CO2-emboly. This manoeuvre might compress the bleeding veins. Endoscopic suction should be avoided: Significant drop of the retroperitoneal pressure might increase the bleeding.

Laparoscopic Surgery for Malignant Adrenal Tumors

The recent study of the German adrenocortical carcinoma registry group[4] including 152 patients with adrenocortical carcinoma of ≤10 cm (35 laparoscopic and 117 open adrenalectomies) showed a comparable frequency of tumor capsule laceration and peritoneal carcinomatosis in both groups. Also, adjusted recurrence-free survival was not different between laparoscopic and open surgery. Other retrospective studies showed enhanced quality of life without impairment of overall survival in patients with adrenocortical carcinoma (ACC) undergoing laparoscopic surgery.[23,24] Also, local recurrences of ACC have been described both, after open and after laparoscopic adrenalectomy.[25-27]

However, some studies reported on worse oncological outcome in patients with ACC undergoing laparoscopic adrenalectomy as compared to open surgery.[28-30] Miller et al.[30] compared 17 laparoscopic (mean tumor size 7 cm) with 71 open adrenalectomies (mean tumor size 12.3 cm) in

patients with ACC. Mean disease-free survival was shorter after laparoscopic adrenalectomy (9.6 months vs. 19.2 months) and local recurrence rate was higher (35% vs. 28%). Thus, long-term outcome in laparoscopically treated patients with ACC should be assessed cautiously. Patients with preoperatively suspected ACC should be informed thoroughly about potential risks and benefits of both surgical techniques.

CONCLUSION

Minimally invasive adrenalectomy for large adrenal tumors is a technically demanding procedure necessitating appropriate expertise in laparoscopic and oncologic surgery. Even in patients with large tumors (>6 cm), laparoscopic adrenal surgery can be performed by an experienced surgeon at large volume centers with an increased but still acceptable intra- and postoperative morbidity.

REFERENCES

1. Boylu U, Oommen M, Lee BR, Thomas R. Laparoscopic adrenalectomy for large adrenal masses: Pushing the envelope. J Endourol 2009;23:971-5.

2. Zografos GN, Farfaras A, Vasiliadis G, Pappa T, Aggeli C, Vassilatou E, et al. Laparoscopic resection of large adrenal tumors. JSLS 2010;14:364-8.

3. Perry KA, El Youssef R, Pham TH, Sheppard BC. Laparoscopic adrenalectomy for large unilateral pheochromocytoma: Experience in a large academic medical center. Surg Endosc 2010;24:1462-7.

4. Brix D, Allolio B, Fenske W, Agha A, Dralle H, Jurowich C, et al .; German Adrenocortical Carcinoma Registry Group. Laparoscopic versus open adrenalectomy for adrenocortical carcinoma: Surgical and oncologic outcome in 152 patients. Eur Urol 2010;58:609-15.

5. Wang B, Ma X, Li H, Shi T, Hu D, Fu B, et al. Anatomic retroperitoneoscopic adrenalectomy for selected adrenal tumors >5 cm: Our technique and experience. Urology 2011;78:348-52.

6. Asari R, Koperek O, Niederle B. Endoscopic adrenalectomy in large adrenal tumors. Surgery 2012;152:41-9.

7. Deckers S, Derdelinckx L, Col V, Hamels J, Maiter D. Peritoneal carcinomatosis following laparoscopic resection of an adrenocortical tumor causing primary hyperaldosteronism. Horm Res 1999;52:97-100.

8. Foxius A, Ramboux A, Lefebvre Y, Broze B, Hamels J, Squifflet J. Hazards of laparoscopic adrenalectomy for Conn’s adenoma. When enthusiasm turns to tragedy. Surg Endosc 1999;13:715-7.

9. Henry JF, Sebag F, Iacobone M, Mirallie E. Results of laparoscopic adrenalectomy for large and potentially malignant tumors. World J Surg 2002;26:1043-7.

10. Agha A, von Breitenbuch P, Gahli N, Piso P, Schlitt HJ. Retroperitoneoscopic Adrenalectomy: Lateral versus dorsal approach. J Surg Oncol 2008;97:90-3.

11. Wu CT, Chiang YJ, Chou CC, Liu KL, Lee SH, Chang YH, et al. Comparative study of laparoscopic and open adrenalectomy. Chang Gung Med J 2006;29:468-73.

12. Hallfeldt KK, Mussack T, Trupka A, Hohenbleicher F, Schmidbauer S. Laparoscopic lateral adrenalectomy versus open posterior adrenalectomy for the treatment of benign adrenal tumors. Surg Endosc 2003;17:264-7.

13. Dimas S, Roukounakis N, Kafetzis I, Bethanis S, Anthi S, Michas S, et al. Feasibility of laparoscopic adrenalectomy for large pheochromocytomas. JSLS 2007;11:30-3.

14. Agha A, Hornung M, Iesalnieks I, Glockzin G, Schlitt HJ. Single-incision retroperitoneoscopic adrenalectomy and single-incision laparoscopic adrenalectomy. J Endourol 2010;24:1765-70.

15. Walz MK, Petersenn S, Koch JA, Mann K, Neumann HP, Schmid KW. Endoscopic treatment of large primary adrenal tumours. Br J Surg 2005;92:719-23.

Agha, et al .: Laparoscopic adrenalectomy for large tumors

16. Tsuru N, Suzuki K, Ushiyama T, Ozono S. Laparoscopic adrenalectomy for large adrenal tumors. J Endourol 2005;19:537-40.

17. Naya Y, Suzuki H, Komiya A, Nagata M, Tobe T, Ueda T, et al. Laparoscopic adrenalectomy in patients with large adrenal tumors. Int J Urol 2005;12:134-9.

18. MacGillivray DC, Whalen GF, Malchoff CD, Oppenheim DS, Shichman SJ. Laparoscopic resection of large adrenal tumors. Ann Surg Oncol 2002;9:480-5.

19. Telem DA, Nguyen SQ, Chin EH, Weber K, Divino CM. Laparoscopic resection of giant adrenal cavernous hemangioma. JSLS 2009;13:260-2.

20. Shen ZJ, Chen SW, Wang S, Jin XD, Chen J, Zhu Y, et al. Predictive factors for open conversion of laparoscopic adrenalectomy: A 13-year review of 456 cases. J Endourol 2007;21:1333-7.

21. Shen WT, Kebebew E, Clark OH, Duh QY. Reasons for conversion from laparoscopic to open or hand-assisted adrenalectomy: Review of 261 laparoscopic adrenalectomies from 1993 to 2003. World J Surg 2004;28:1176-9.

22. Bergamini C, Martellucci J, Tozzi F, Valeri A. Complications in laparoscopic adrenalectomy: The value of experience. Surg Endosc 2011;25:3845-51.

23. Fassnacht M, Allolio B. What is the best approach to an apparently nonmetastatic adrenocortical carcinoma? Clin Endocrinol (Oxf) 2010;73:561-5.

24. Gerber E, Dinlenc C, Wagner JR. Laparoscopic adrenalectomy for isolated adrenal metastasis. JSLS 2004;8:314-9.

25. Favia G, Lumachi F, Carraro P, D’Amico DF. Adrenocortical carcinoma. Our experience. Minerva Endocrinol 1995;20:95-9.

26. Icard P, Chapuis Y, Andreassian B, Bernard A, Proye C. Adrenocortical carcinoma in surgically treated patients: A retrospective study on 156 cases by the French Association of Endocrine Surgery. Surgery 1992;112:972-9; discussion 979-80.

27. Plouin PF, Chatellier G, Fofol I, Corvol P. Tumor recurrence and hypertension persistence after successful pheochromocytoma operation. Hypertension 1997;29:1133-9.

28. Henry JF, Sebag F, Iacobone M, Mirallie E. Results of laparoscopic adrenalectomy for large and potentially malignant tumors. World J Surg 2002;26:1043-7.

29. Gonzalez RJ, Shapiro S, Sarlis N, Vassilopoulou-Sellin R, Perrier ND, Evans DB, et al. Laparoscopic resection of adrenal cortical carcinoma: A cautionary note. Surgery 2005;138:1078-85; discussion 1085-6.

30. Miller BS, Ammori JB, Gauger PG, Broome JT, Hammer GD, Doherty GM. Laparoscopic resection is inappropriate in patients with known or suspected adrenocortical carcinoma. World J Surg 2010;34:1380-5.

Cite this article as: Agha A, Iesalnieks I, Hornung M, Phillip W, Schreyer A, Jung M, et al. Laparoscopic trans- and retroperitoneal adrenal surgery for large tumors. J Min Access Surg 2014;10:57-61.

Date of submission: 14/02/2013, Date of acceptance: 26/12/2013

Source of Support: Nil, Conflict of Interest: None declared.