ELSEVIER
BIOMEDICINE PHARMACOTHERAPY
Mini review
Section 3. Adrenal Laparoscopic surgery for malignant adrenal tumors Kazuo Suzuki *
Department of Urology, Hamamatsu University School of Medicine, 1-20-1 Handayama, Hamamatsu-shi 431-3192, Japan
Abstract
This paper outlines the indications and techniques of laparoscopic surgery for malignant adrenal tumors. Laparoscopic surgery is not indicated for adrenal tumors of any size when invasion of the surrounding tissues is clearly detected by preoperative imaging. When laparoscopic surgery is performed for a tumor without invasion that has a maximum diameter of more than 6 cm or a tumor that is considered potentially malignant from preoperative imaging or endocrine studies, it is important to inform the patient and family that the tumor may be malignant and that conversion to open surgery may be necessary. The transperitoneal approach is appropriate for primary adrenal malignancies. For metastatic cancer, the transperitoneal approach is suitable for radical surgery and the extraperitoneal approach for histological diagnosis by partial resection or tumor biopsy. In either case, it is important for the surgeon to have a sufficiently wide working space, to remove the tumor and surrounding fat en bloc, to never grasp the tumor or adrenal tissue, and to carefully handle the ultrasonically activated scalpel or ultrasonic aspirator so that it does not touch the tumor surface due to the risk of tumor cell dissemination. It is also essential not to unreasonably persist with laparoscopic procedures, but to immediately switch to open surgery when laparoscopic surgery becomes difficult. @ 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved.
Keywords: Laparoscopic surgery; Adrenalectomy; Malignant tumor
Laparoscopic adrenalectomy for adrenal tumors was first performed in 1992 in Japan [10,13,24]. Since then, it has spread around the world as a minimally invasive surgical technique and is now considered a gold standard for the treatment of small adrenal tumors. The indications for this method have gradually been extended as surgical techniques have improved and new devices have been developed. Now, laparoscopic surgery is also performed for pheochromocy- toma and tumors with a size of 10 cm or more [8,12]. However, no consensus has been reached about the indica- tions for laparoscopic surgery in patients with primary malignant adrenal tumors and metastatic adrenal cancer [18]. This paper outlines the indications and techniques of laparoscopic surgery for primary or metastatic adrenal malignancies.
1. Laparoscopic surgery for primary malignant adrenal tumors
1.1. Surgical indications
Primary malignant adrenal tumors include adrenocortical carcinoma and malignant pheochromocytoma. It is not always easy to make a preoperative diagnosis of such tumors. Honigschnabl et al. retrospectively examined the utility of MR imaging for the preoperative diagnosis of adrenal tumors in 229 patients and reported that its sensi- tivity for the differentiation of benign from malignant adrenal masses was 89%, while the specificity was 99% and the accuracy was 93.9%, resulting in a positive predictive value of 90.9% and a negative predictive value of 94.2% [16]. However, preoperative imaging or endocrine studies rarely yield a definite diagnosis of malignancy when the diameter of the adrenal tumor is 5-6 cm or smaller. More- over, it is often difficult to differentiate benign from malig- nant tumors even by histopathological examination of
* Corresponding author. Tel .: +81-53-435-2306; fax: +81-53-435-2305.
C) 2002 Éditions scientifiques et médicales Elsevier SAS. All rights reserved. PII: S0753- 3322 ( 02) 00230 - 5
ID P
00
L
resected specimens. Hirano et al. [14] measured the tissue telomerase activity of resected adrenal tumors and con- cluded that this test was effective for differentiating benign from malignant tumors. However, measurement of telom- erase cannot be used for preoperative diagnosis. It is generally considered that tumors with a diameter of 6 cm or more are probably malignant. Aso and Homma examined 210 Japanese patients with adrenal incidentalomas and reported that all 14 malignant tumors had a diameter of 6.5 cm or more [1]. Belldegrun et al. reported that a tumor diameter of 6 cm or more was observed in 105 out of 114 adrenal cancers [2].
Laparoscopic surgery has recently been performed for primary adrenal cancer [5,11,15,17]. However, the surgeon should be prudent in deciding on the indications for laparo- scopic surgery because many of the reported patients suffered from postoperative local recurrence or intraperito- neal dissemination. We experienced a patient with Cush- ing’s syndrome due to adrenocortical cancer who developed intraperitoneal dissemination at 19 months after laparo- scopic adrenalectomy [28]. The tumor diameter was 5.5 cm, and preoperative CT showed a partially heterogeneous internal structure as well as an irregular margin (Fig. 1).
We now consider that adrenal tumors with a diameter of 10 cm or less are indicated for laparoscopic surgery, but that all tumors with infiltration of the surrounding tissues on preoperative imaging are not. Careful consideration should be given to tumors without infiltration that have a diameter of 6 cm or more and tumors with an irregular margin because such lesions have a possibility of malignancy. When performing laparoscopic surgery for these suspicious tumors, it is important to inform the patient and family that the tumor may be malignant, that laparoscopic surgery may need to be switched to open surgery due to adhesions or
bleeding, and that local recurrence may occur postopera- tively. Nelson et al. and we have discussed the indications for laparoscopic surgery of primary malignant adrenal tumors [20,21,28].
1.2. Surgical techniques
The transperitoneal lateral approach is appropriate for primary adrenal tumors with a diameter of 6 cm or more because it provides a wide operating field and clearly exposes the adrenal gland [22,25].
1.2.1. Left adrenalectomy
The patient is placed in the full lateral position. Make an about 2 cm skin incision on the midclavicular line slightly below the costal arch to place the first trocar. Insert a laparoscope to carefully inspect the peritoneal cavity and examine whether laparoscopic surgery is possible or not. Place three 5 mm trocars along the costal arch under laparoscopic monitoring. Incise the phrenocolic ligament, and then extend the incision of the peritoneum and Gerota’s fascia upward along the lateral border of the spleen until the greater curvature of the stomach is seen. Allow the spleen to fall away in the medial direction until the posterior surface of the pancreas is exposed. These procedures expose the adrenal gland at the front of the surgical field. Expose the diaphragm at the lateral and superior aspects of the spleen. Dissect the fat around the upper pole of the adrenal gland along the diaphragm. Expose the superior adrenal vein draining into the inferior phrenic vein at the upper site of the adrenal gland, and transected. Detach the upper pole of the kidney from the adrenal gland. After dissecting the whole circumference of the adrenal gland, grasp the surrounding fat to lift the gland, and continue detaching the adrenal gland caudally and medially. Finally, the adrenal vein is exposed, clipped, and cut.
When the incision of the peritoneum and renal fascia is fully extended upward along the outer border of the spleen until the greater curvature of the stomach can be seen, the spleen is displaced in the medial direction by its own weight to provide a clear visual field. The pointers to this surgical technique are to expose the diaphragm first and to start gradually dissecting the adrenal gland from an easy site.
1.2.2. Right adrenalectomy
The patient is placed in the full lateral position. Trocars are placed symmetrically with those used for left adrena- lectomy. First, incise the hepatocolic ligament and extend the incision along the liver from the lateral to upper surfaces. Expose the diaphragm at the lateral border of the liver and detach the liver along the diaphragm. Incise the hepatic triangular ligament to allow the right lobe of the liver to fall away in the medial direction. This will allow
medial mobilization of the liver by pressure to a position near the inferior vena cava, thereby providing a wide visual field. When the upper pole of the adrenal gland is impacted in, or strongly adherent to the inferior surface of the liver, do not try to dissect it. Instead, detach the lateral border of the adrenal gland from the liver and leave dissection of the upper pole until the last step. The fat surrounding the adrenal gland on the superior and lateral borders of the gland is dissected along the diaphragm. Then separate the upper pole of the kidney from the adrenal gland. After treating the inferior and posterior adrenal vessels at the lower pole of the adrenal gland, carefully dissect the inferior vena cava to expose the adrenal vein, which is clipped and cut. After cutting this vein, dissect the adrenal gland in the cranial direction along the inferior vena cava to detach the superior adrenal vein and the upper pole of the gland.
It is important to extend the incision of the hepatocolic ligament as far as the lateral border of the liver in order to expose the diaphragm at the superior and lateral surfaces of the adrenal gland, and to use the diaphragm as a landmark when dissecting the adrenal gland. When the tumor is large, it is necessary to incise the hepatic triangular ligament to mobilize the liver in the medial direction. Since the right adrenal vein is short and directly enters the inferior vena cava, it should be carefully identified and dissected.
For both left and right adrenalectomy, it is important to reflect the intestines, liver, and spleen medially so as to obtain a wide field of view, to dissect the adrenal gland en bloc with the surrounding fat, and to never touch the tumor or the normal adrenal tissue. Use of an ultrasonic coagulat- ing shears (UCS) or ultrasonic aspirator requires extreme care to avoid touching the tumor surface because of the risk of disseminating tumor cells.
2. Laparoscopic surgery for metastatic adrenal cancer
2.1. Surgical indications
Laparoscopic adrenalectomy for metastatic adrenal can- cer has been reported recently [3,4,6,9,19,27,29]. All the reported patients had the metastases from lung cancer or renal cell carcinoma. Complete resection of the tumor was achieved in all cases and laparoscopic surgery was de- scribed as useful for metastatic adrenal cancer. However, care should be taken when preoperative imaging showed an unclear border between the tumor and the surrounding tissue or possible infiltration. We experienced a patient with metastatic adrenal cancer, in whom laparoscopic surgery was switched to open surgery [26]. The patient was a 62-year-old man who had the metastasis of lung cancer (poorly differentiated adenocarcinoma) to the adrenal gland. MR imaging showed a tumor measuring 5.5 × 4.0 cm in the
left adrenal gland with possible infiltration of the surround- ing tissue (Fig. 2A). Although retroperitoneoscopic adrena- lectomy was performed, it had to be switched to open surgery because the tumor was strongly adherent to the upper pole of the kidney. The tumor could not be separated from the kidney even at open surgery, and had to be removed en bloc with the upper pole of the kidney (Fig. 2B). This patient died of systemic lung cancer metastases at 8 months after surgery. On the other hand, we experienced a patient with metastatic adrenal cancer that was completely removed by laparoscopic surgery. The patient was a 49- year-old man with metastasis of lung cancer to the left adrenal gland. MR imaging showed a left adrenal tumor (4.5 × 4.0 cm), which was relatively well demarcated from the surrounding tissue (Fig. 3A). After obtaining informed consent from the patient and his family, laparoscopic adrenalectomy was performed via the transperitoneal ap- proach. The tumor could be completely excised and was histologically diagnosed as metastatic lung cancer (poorly differentiated adenocarcinoma) (Fig. 3B). The operating time was 151 min and estimated blood loss was 50 ml. There were no complications. He has subsequently survived for 12 months postoperatively without tumor recurrence.
Thus, laparoscopic surgery is considered a worthwhile option for metastasis to the adrenal gland from lung or renal cancer. However, it is not indicated when preoperative imaging shows possible infiltration of the surrounding tissues, as described above. Before surgery, it is important to fully inform the patient and family that laparoscopic surgery may be switched to open surgery and to immediately switch when the laparoscopic procedure is difficult, as is done for primary malignant adrenal tumors.
2.2. Surgical technique
As is the case with primary adrenal tumors, the transperi- toneal approach seems suitable for radical surgery, that is, when the primary tumor has been completely eliminated and the adrenal metastasis is the only residual tumor. The extraperitoneal approach is feasible when the primary ob- jective is to make a histopathological diagnosis that can be achieved by partial resection or biopsy of the tumor, depending on the situation. The surgical technique for retroperitoneoscopic adrenalectomy is outlined below. Refer to our previous article for more details [23].
Place the patient in the full lateral position. The first trocar is inserted in the midaxillary line slightly below the costal arch using open laparoscopy method. Then two trocars are inserted along with the costal margin. Place the additional trocar for mobilization of the kidney at the level of the umbilicus on the anterior axillary line. Widely incise Gerota’s fascia to detach the fat around the kidney and
174
A
B
adrenal gland en bloc. Then, incise the fat between the upper pole of the kidney and the adrenal gland. After exposing the upper pole of the kidney, detach it from the adrenal gland using the renal surface as a landmark for dissection. After freeing the kidney from the adrenal gland, elevate the adrenal gland by grasping the attached fat to expose the inferior vena cava (right) and to cut the adrenal vein. Metastatic adrenal cancer adheres to the surrounding tissues and bleeds readily because of its vascularity. Bipolar hemo- static forceps are useful for hemostasis. Use of a LCS to dissect the tissue surrounding the tumor requires special care to avoid touching the tumor surface, as is the case in primary adrenal tumors. When the patient is obese, it is difficult to locate the adrenal gland because the gland and the upper pole of the kidney are buried in fat. Attempts to directly locate the adrenal gland by pushing the fat aside will disturb the field of view due to bleeding and lead to disorientation. The pointer for this surgical technique is not to try to locate the adrenal gland directly, but to manage the tissue surrounding the gland first.
3. Discussion
In general, malignant adrenal tumors have abundant vascularity, often adhere to the surrounding tissues, and are
likely to cause profuse bleeding during surgery. Gagner et al. [7] stated that open surgery should be chosen for pheochromocytoma that is suspected to be malignant by preoperative imaging in their report on laparoscopic adrena- lectomy. As described above, we experienced a case of Cushing’s syndrome that was successfully treated by lap- aroscopic adrenalectomy in whom intraperitoneal dissemi- nation and local recurrence occurred 19 months after surgery despite the postoperative pathological diagnosis of adrenocortical adenoma. The outcome would have been the same if he had been treated by open surgery because the tumor was not damaged and was removed en bloc. How- ever, the ultrasonic aspirator used during laparoscopic surgery may have caused the dissemination of tumor cells.
Laparoscopic surgery is not indicated for primary adrenal tumors of any size when preoperative imaging shows infiltration of the surrounding tissue. Careful dissection is required for adrenal tumors with a diameter of 6 cm or more even when no malignant features are observed preopera- tively because there remains a possibility of malignancy. Although metastatic adrenal cancer with a diameter of 7-8 cm or less is considered to be indicated for laparoscopic surgery, metastatic tumors with obvious infiltration of the surrounding tissues are not suitable, as is the case for primary adrenal tumors. The transperitoneal approach is suitable when laparoscopic surgery is aimed at radical
13:5
A
B
2
3
4
5
6
7
8
resection of the tumor, while the extraperitoneal approach is appropriate when the aim of surgery is to make a histo- pathological diagnosis.
In either case, experienced surgeons should perform laparoscopic adrenalectomy for malignant or potentially malignant adrenal tumors after informing the patient and family that a large amount of bleeding may occur, that the laparoscopic procedure may be switched to open surgery, and that the tumor can recur locally. During surgery, it is important to pay special attention to bleeding and not to persist with laparoscopic surgery, but immediately switch to open surgery if the laparoscopic procedure becomes diffi- cult.
References
[1] Aso Y, Homma Y. A survey on incidental adrenal tumors in Japan. J Urol 1992;147:1478-81.
[2] Belldegrum A, Hussain S, Seltzer SE, Loughlin KR, Gittes RF, Richie JP. Incidentally discovered mass of the adrenal gland. Surg Gynecol Obstet 1986;163:203-8.
[3] Bendinelli C, Lucchi M, Buccianti P, Iacconi P, Angeletti CA, Miccoli P. Adrenal masses in non-small cell lung carcinoma patients: is there any role for laparoscopic procedures? J Laparoendosc Adv Surg Tech A 1998;8:119-24.
[4] Breton X, Corbi P, Fare JP, Jailed C, Richer JP, Meurice JC, et al. Operable lung cancer and synchronous adrenal masses: role of laparoscopic adrenalectomy combined with pulmonary resection. Ann Chir 2002;127:193-7.
[5] Deckers S, Derdelinckx L, Col V, Hamels J, Maiter D. Peritoneal carcinomatosis following laparoscopic resection of an adrenocorti- cal tumor causing primary hyperaldosteronism. Horm Res 1999;52: 97-100.
[6] Elashry OM, Clayman RV, Soble JJ, McDougall EM. Laparoscopic adrenalectomy for solitary metachronous contralateral adrenal metastasis from renal cell carcinoma. J Urol 1997;157:1217-22.
[7] Gagner M, Breton G, Pharand D, Pomp A. Is laparoscopic adrena- lectomy indicated for pheochromocytomas? Surgery 1996;120: 1076-9.
[8] Gagner M, Pomp A, Heniford BT, Pharand D, Lacroix A. Laparo- scopic adrenalectomy: lessons learned from 100 consecutive proce- dures. Ann Surg 1997;226:238-46.
[9] Gill IS, Meraney AM, Thomas JC, Sung GT, Novick AC, Lieber- man I. Thoracoscopic transdiaphragmatic adrenalectomy: the initial experience. J Urol 2001;165:1875-81.
[10] Go H, Takeda M, Takahashi H, Imai T, Tsutsui T, Mizusawa T, et al. Laparoscopic adrenalectomy for primary aldosteronism: a new operative method. J Laparoendosc Surg 1993;3:455-9.
[11] Hamoir E, Meurisse M, Defechereux T. Is laparoscopic resection of a malignant corticoadrenaloma feasible? Case report of early, diffuse and massive peritoneal recurrence after attempted laparoscopic resection. Ann Chir 1998;52:364-8.
[12] Henry JF, Defechereux T, Gramatica L, Raffaelli M. Should laparo- scopic approach be proposed for large and/or potentially malignant adrenal tumors? Langenbecks Arch Surg 1999;384:366-9.
[13] Higashihara E, Tanaka Y, Horie S, Aruga S, Nutahara K, Minowada S, et al. Laparoscopic adrenalectomy: the initial three cases. J Urol 1993;149:973-6.
[14] Hirano Y, Fujita K, Suzuki K, Ushiyama T, Ohtawara Y, Tsuda F. Telomerase activity as an indicator of potentially malignant adrenal tumors. Cancer 1998;83:772-6.
[15] Hofle G, Gasser RW, Lhotta K, Janetschek G, Kreczy A, Finkenst- edt G. Adrenocortical carcinoma evolving after diagnosis of pre- clinical Cushing’s syndrome in an adrenal incidentaloma. A case report. Horm Res 1998;50:237-42.
[16] Honigschnabl S, Gallo S, Niederle B, Prager G, Kaserer K, Lechner G, et al. How accurate is MR imaging in characterization of adrenal masses: update of a long-term study. Eur J Radiol 2002;41: 113-22.
[17] Inoue T, Terai A, Terachi T, Souma T, Yoshida O. Synchronous testicular seminoma and adrenocortical carcinoma: a case report. Int J Urol 1998;5:615-7.
[18] Kumar U, Albala DM. Laparoscopic approach to adrenal carcinoma. J Endourol 2001;15:339-43.
[19] Linos DA, Avlonitis VS, Iliadis K. Laparoscopic resection of solitary adrenal metastasis from lung carcinoma: a case report. JSLS 1998;2:291-3.
[20] Nelson JB, Kavoussi LR. RE: a case of Cushing’s syndrome due to adrenocortical carcinoma with recurrence 19 months after laparo- scopic adrenalectomy. J Urol 1998;159:1310.
[21] Nelson JB, Kavoussi LR. RE: a case of Cushing’s syndrome due to adrenocortical carcinoma with recurrence 19 months after laparo- scopic adrenalectomy. J Urol 1999;161:1580-1.
[22] Suzuki K. Laparoscopic adrenalectomy. In: Hemal AK, editor. Laparoscopic urologic surgery. New Delhi: BI Churchill Livingstone; 2000. p. 109-23.
[23] Suzuki K. Laparoscopic adrenalectomy: retroperitoneal approach. Urol Clin North Am 2001;28:85-95.
[24] Suzuki K, Kageyama S, Ueda D, Ushiyama T, Kawabe K, Tajima A, et al. Laparoscopic adrenalectomy: clinical experience with 12 cases. J Urol 1993;150:1099-102.
[25] Suzuki K, Kageyama S, Hirano Y, Ushiyama T, Rajamahanty S, Fujita K. Comparison of three surgical approaches to laparoscopic adrenalectomy: a nonrandomized, background matched analysis. J Urol 2001;166:437-43.
[26] Suzuki K, Ushiyama T, Mugiya S, Kageyama S, Saisu K, Fujita K. Hazards of laparoscopic adrenalectomy in patients with adrenal malignancy. J Urol 1997;158:2227.
[27] Tsuji Y, Yasuhuku M, Haryu T, Watanabe Y, Ataka K, Okada M. Laparoscopic adrenalectomy for solitary metachronous adrenal metastasis from lung cancer: report of a case. Surg Today 1999;29: 1277-9.
[28] Ushiyama T, Suzuki K, Kageyama S, Fujita K, Oki Y, Yoshimi T. A case of Cushing’s syndrome due to adrenocortical carcinoma with recurrence 19 months after laparoscopic adrenalectomy. J Urol 1997;157:2239.
[29] Valeri A, Borrelli A, Presenti L, Lucchese M, Venneri F, Man- nelli M, et al. Adrenal masses in neoplastic patients: the role of laparoscopic procedure. Surg Endosc 2001;15:90-3.