Quartz 4

19660215

21 min read

Laparoscopic Surgery for Malignant Adrenal Tumors

G. N. Zografos, MD, G. Vasiliadis, MD, A. N. Farfaras, MD, C. Aggeli, MD, M. Digalakis, MD

ABSTRACT

Advances in imaging have improved early detection of primary and metastatic adrenal tumors. The laparoscopic approach, the gold standard for benign adrenal diseases, is controversial for malignant adrenal tumors. A prospec- tive randomized study of the role of laparoscopic surgery in adrenal cancer is not feasible because of the rarity of the disease. A review of the literature demonstrates the safety and efficacy of laparoscopic adrenalectomy for solitary adrenal tumors. In primary adrenal malignancies, the lapa- roscopic approach should be considered cautiously, only when it can achieve complete tumor resection with an intact adrenal capsule. Conversion to an open procedure should be an early decision, prior to tumor morcellation or fracture of the tumor capsule. Patients who have local invasion, tumors that are too large, or require organ re- section require an open procedure.

Key Words: Laparoscopic adrenalectomy, Malignancy, Malignant tumors.

Third Department of Surgery, Athens General Hospital, Greece (Drs Zografos, Vasiliadis, Farfaras, Aggeli).

Department of Surgery, Asklipeion Hospital, Athens, Greece (Dr Digalakis).

Address correspondence to: G. N. Zografos, MD, Consultant Surgeon, 10 K. Ourani Street, Filothey 15237, Athens, Greece. Telephone: +306944918944, Fax: +302107706915, E-mail: gnzografos@yahoo.com

@ 2009 by JSLS, Journal of the Society of Laparoendoscopic Surgeons. Published by the Society of Laparoendoscopic Surgeons, Inc.

INTRODUCTION

Advances in biochemistry and imaging have led to earlier diagnosis and enrichment of adrenal pathology. Develop- ment of endocrinology and laparoscopic surgery has low- ered the morbidity of adrenal operations. Laparoscopic adrenalectomy is one of the successful applications of minimally invasive surgical techniques. Since the first laparoscopic adrenalectomy was performed in 1992,1 this approach has been adopted quickly as the procedure of choice to treat benign functioning and nonfunctioning adrenal tumors. It is widely accepted that the laparoscopic approach provides better visualization of anatomically complex areas through smaller and less painful incisions. Several series2,3 have documented that laparoscopic adre- nalectomy is followed by lower complication rates, less operative blood loss, and less need for transfusion, less postoperative pain, earlier return to activity and diet, bet- ter cosmetic results, shorter hospital stay, and lower over- all costs.

In the era of advanced laparoscopic surgery, laparoscopic adrenalectomy has gained popularity, and several institu- tions have expanded indications for this procedure. Po- tentially malignant primary adrenal tumors and solitary adrenal metastases, once considered contraindications for the laparoscopic approach, are now being removed lapa- roscopically in some centers.4-8 The suitability of the laparoscopic approach to primary adrenal carcinomas re- mains the focus of debate. A curative laparoscopic resec- tion incorporates the oncologic principles of the open technique, avoiding fracture of the tumor capsule.

Malignant tumors of the adrenal gland are categorized into those arising from the cortex or medulla and metastatic ones from known primary origin.

ADRENAL CORTICAL CARCINOMA

An adrenal cortical carcinoma (ACC) is a rare, highly malignant endocrine neoplasm with few effective thera- peutic options apart from surgical resection.9-11 It has a worldwide incidence of approximately 2 per million pop- ulation per year.12 It represents 0.2% of all cases of cancer. Regardless of size, approximately 1 per 1500 adrenal tu- mors is malignant.13 The incidence rate of malignancy is

small in all adrenal masses that are <4 cm. In series with tumors >5 cm, carcinoma may be found in as many as 7% of patients.14 About 60% of these tumors are functioning and may secrete excess cortisol, androgens, estrogens, aldosterone, or a combination of those.15,16 ACCs may occur sporadically or rarely as a component of multiple endocrine neoplasia type I (MEN I), Beckwith-Wiede- mann syndrome, and Li-Fraumeni syndrome.17,18

Adequate imaging is essential for staging of the disease and operative planning. Both CT and MRI are useful for evaluating the primary tumor and especially for detecting regional disease, vascular disease, lymphadenopathy, and liver and lung metastases. ACCs are usually >6 cm, with heterogeneity, irregular margins, hemorrhage, necrosis, calcifications, or adjacent lymphadenopathy. Metastases and local invasion into adjacent organs or the vena cava are possible radiographic features of ACC.19 Radiocholes- terol scintigraphy, using 131 I-6-beta-iodomethylnorcho- lesterol (NP-59) has been used to determine whether an adrenal cortical tumor is benign. Decreased or no uptake of NP-59 is more likely in a cancer and the majority of ACCs have no NP-59 uptake.20

Local disease at diagnosis and complete tumor resection constitute the 2 most important factors for improved sur- vival. Five-year survival for patients with ACCs ranges from 16% to 60%. Even patients who undergo complete resection may have recurrence, metastatic disease, or both. Approximately two-thirds of patients develop recur- rence within 2 years, and about 85% eventually develop local recurrence or distant metastases. Resection of the primary tumor in the presence of metastatic disease can improve local symptoms but rarely affects overall surviv- al.21

MALIGNANT PHEOCHROMOCYTOMA

Pheochromocytomas are rare catecholamine-secreting tu- mors deriving from chromaffin cells. The incidence of pheochromocytoma is 1 to 2/100 000 adults per year.22 About 10% of pheochromocytomas were thought to be hereditary, but recently it has been shown that approxi- mately 25% of patients with sporadic pheochromocytoma and no family history have germ-line mutations in 1 of 4 susceptible genes for pheochromocytoma. These muta- tions may be seen in isolation or as part of a syndrome, such as multiple endocrine neoplasia (MEN) IIA and IIB, and various neuroectodermal disorders including neuro- fibromatosis, von Hippel-Lindau syndrome, Sturge-Weber syndrome, and Carney triad, the latter being associated with multifocal extraadrenal pheochromocytomas.23

When these tumors are found in patients with familial syndromes, they are more likely to be bilateral or multi- focal and benign unless there is a family history of malig- nant pheochromocytoma.24 A diagnosis of malignant pheochromocytoma can only be made reliably by the findings of local invasion or nodal and distant metastases. CT and MRI are very useful for the recognition of these tumors and so is scintigraphy with I-131-meta-iodo-ben- zyl-gouanidine (MIBG 131), which is a functional imaging test especially important for tumors that cannot be de- tected by CT or MRI for extraadrenal, multifocal, or met- astatic disease, for MEN syndromes and for the early detection of disease relapse.25-27 Malignant pheochromo- cytoma may recur early or late (even 20 years) after the initial resection.28-31 Unfortunately, no accurate histologic criteria exist to establish the diagnosis, and 5% to 26% of pheochromocytomas are malignant.32-35

METASTATIC TUMORS

Solitary adrenal metastases are quite common and nor- mally do not cause symptoms. Primary localization of metastatic tumors is lung (the most common), breast, kidney, bowel, stomach, lymphoma, and melanoma. In a patient with a history of an extraadrenal primary malig- nancy, an adrenal incidentaloma represents metastatic dis- ease in 32% to 73% of cases. Detection of metastases is becoming increasingly common with the widespread use of cross-sectional imaging (CT or MRI) and with 28-flu- orodeoxyglucose positron-emission tomography.36 Adre- nal metastases are in most cases confined within the capsule of the organ, which suggests that simple adrenal- ectomy may be sufficient to achieve negative margins.37-38 Many studies39-41 advocate that resection of isolated meta- chronous adrenal metastases from various primary can- cers may improve survival. These studies demonstrate median survival between 20 months and 30 months after adrenal metastasectomy, compared with 6 months to 8 months in cases with unresected adrenal metastases.

LAPAROSCOPIC SURGERY IN MALIGNANCY

Laparoscopic surgery can be an accepted method in the surgical management of cancer if it fulfils a number of parameters. First of all, there should be evidence drawn by operative morbidity and mortality that laparoscopic surgery is equally safe or even safer than conventional open surgery is. Moreover, it should be as radical as conventional open surgery.

The role of laparoscopic surgery for malignant adrenal tumors is controversial, because there are small series in

the literature for a rare disease. Furthermore, there have been concerns regarding local recurrences and port-site metastasis after potentially curative resections.42 The pathogenesis of port-site metastasis remains unknown but is probably multifactorial. Direct wound implantation of tumor cells plays a major role in the development of port-site metastasis. However, this does not explain the development of metastasis at nonextraction port sites. Other causal factors are contamination of instruments, aerolization of tumor cells, the chimney effect, poor sur- gical technique, improper handling of the tumor, pneu- moperitoneum, hematogenous spread, effect of the car- bon dioxide on tumor cells, and lack of preventive measures of local recurrence and port-site metastasis. Sev- eral strategies have been proposed to prevent port-site metastasis. To achieve better results, strictly oncologic techniques should be followed as in open surgery. More- over, additional techniques like wound protectors, evac- uation of the pneumoperitoneum through the port, and peritoneal wound closure have been proposed and ap- plied successfully.43-46

Three cases of diffuse peritoneal dissemination and death of patients who underwent laparoscopic adrenalectomy for adrenal cancer have been reported.46 Moreover in a study of 13 patients (6 with adrenal cortical carcinoma and 7 with metastasis),47 the mean size of the malignant le- sions was 5.9cm. The mean follow-up was 30 months, during which 3 patients died, one due to endoperitoneal and trocar port-site seeding. In another study,48 31 pa- tients underwent 33 laparoscopic adrenalectomies, 26 for metastatic cancer and 7 for primary adrenal malignancy. Follow-up was 26 months, during which 15 patients died. Local recurrence was noted in 7 patients. However, no port-site metastasis occurred. Five-year survival reached 40%.

LAPAROSCOPIC RESECTION OF SOLITARY ADRENAL METASTASES

Surgical excision in cases of solitary adrenal metastases is advantageous to the patient in terms of disease-free and overall survival. Solitary adrenal metastasis does not mean systemic disease, and studies have shown that these pa- tients may be treated with laparoscopic surgery. More- over, it has been suggested that patients who have a metachronous metastasis from any of a variety of primary tumors may benefit, as they will suffer less morbidity than with open surgery.

Heniford and colleagues49 in a review of 10 patients with metastatic adrenal tumors and 1 patient with adrenocorti-

cal carcinoma reported no local or port-site recurrence at a mean follow-up of 8.3 months. Another study50 has focused on solitary adrenal gland metastasis in patients who have been formerly operated on for non-small cell lung cancer. There were 11 patients with solitary adrenal metastases. All of them underwent laparoscopic adrenal- ectomy. Three were still alive and well 37 months to 80 months after the lung resection. One patient (who under- went bilateral adrenalectomy) was still alive 44 months later but with local relapse. Two patients died of other causes 5 months and 6 months after the adrenalectomy, one after 14 months of local and systemic relapse and the remaining 3 after 12 to 38 months of systemic relapse.

LAPAROSCOPIC SURGERY IN PRIMARY ADRENAL MALIGNANCY

Malignant pheochromocytomas and ACCs must be ap- proached cautiously. Peri-adrenal invasion is common, and the possibility of tumor fragmentation and abdominal dissemination is significant. The surgeon must mobilize the tumor and surrounding adipose tissue without grasp- ing the tumor or gland. The ultrasonically activated scalpel should be carefully used so that it does not divide tumor surface or adrenal tissue and thus create fragmentation and malignant cell dissemination.

Lombardi et al51 reported complete laparoscopic excision of 3 ACCs and 2 malignant pheochromocytomas, both well-encapsulated macroscopically. Unfortunately, one patient with ACC presented with pelvic recurrence 6 months later, and one patient with malignant pheochro- mocytoma developed intraabdominal recurrence 1 year after laparoscopic surgery. Li and colleagues52 have re- ported 3 cases of pheochromocytomatosis following lapa- roscopic adrenalectomy; however, it is not clear whether it was malignant dissemination or spillage of a benign tumor due to bad technique. Additionally, laparoscopic adrenalectomy for clinically unsuspected adrenocortical cancer was associated with a high recurrence rate.53 De- spite the several hundreds of laparoscopically resected pheochromocytomas reported in the literature, data are lacking on the long-term follow-up of patients who have undergone laparoscopic adrenalectomy for malignant pheochromocytoma.54,55 The natural history of the re- sected malignant pheochromocytoma is still unknown. Recurrence has been reported more often 6 years to 7 years following curative surgery, but it can occur as late as after 24 years.55

With regard to malignant adrenal cortical tumors, it ap- pears from literature data (Table 1) that the risk of locore-

Table 1. Laparoscopic Surgery for Malignant Adrenal Tumors
AuthorJournalTumor Size (cm)Patients NumberAbdominal Dissemination
Heniford BTSemin Surg Oncol 1999;16:2931.8-1211 (10 metastatic, 1 ACC)(-) 0.5 -19 months
Henry JWorld J Surg 2000;24:13423.5-44 metastatic(-) 12 months
Valeri ASurg Endosc 2001;15:902.5-66 metastatic(-) 3 -18 months
Clark OHArch Surg 2002;137:948-9517-126 primary3 local recurrences
Clark OHArch Surg 2002;137:948-9512.5-1213 metastatic65% disease free survival in 3.3 years
Henry JFWorld J Surg 2002;26:1043>666 months liver metastasis
Rassweijer JJ UroI 2003;169:2072-111 local recurrence, 1 port-site metastasis
Lombardi CPTumori 2003;89:255-9(-)
Giraudo GMinerva Chir 2004;59(1):1-5-4 primary, 4 metastatic(-) 9-72 months
Porpiglia FBJU Int 2004;94(7):1026-1029Mean 5.96 primary, 7 metastatic1 port-site metastasis
KerherAnn Surg 2004;241(6):919-928-2(-) 21.4 months
Lucchi MEur J Cardiothorac Surg 2005;27(5):753-756-11 metastatic, 4 primary1 local relapse, 4 systemic relapses

gional recurrence and tumor dissemination is unclear. In spite of several reports of locoregional recurrence follow- ing laparoscopic adrenalectomy, data are insufficient to attribute the recurrences to the laparoscopy per se or to bad surgical technique with erratic patient selection. Fur- thermore, in most reports of laparoscopic adrenalectomy for ACC, a cancer diagnosis was not established or sus- pected preoperatively. Because the ACCs in these reports were localized tumors, possibly representing less aggres- sive disease, or potentially malignant tumors, results may not reflect the true survival and risk of local recurrence.54

Given that no reliable and accurate preoperative diagnos- tic test to confirm the diagnosis of primary malignant adrenal tumor or local invasion exists, it is often difficult to determine whether the laparoscopic approach can achieve a curative resection.

The role of the laparoscopic approach for large tumors is still controversial. There are not many reports of patients with malignancies >8 cm; however, a review of the liter- ature shows that these patients may undergo laparoscopic surgery. The overall morbidity and mortality is indepen- dent of the size of the tumor,53 and the mean operative time is not significantly different. Conversion to open surgery is necessary more often with larger tumors, due to

invasion of adjacent tissues or organs or due to capsular disruption. Lesion sizes of 12 cm to 14 cm have been cited as the upper limit for laparoscopic adrenalectomy in most of the studies.56

At present, laparoscopic adrenalectomy is contraindicated for invasive malignant tumors.57 En-block extensive resec- tions like nephrectomy, hepatectomy, pancreatectomy, and splenectomy are not well suited to the laparoscopic technique.58-63

CONCLUSION

A prospective randomized study of the role of laparo- scopic surgery in adrenal cancer is not feasible because of the rarity of primary and metastatic adrenal malignancies. It seems that metastatic lesions in the adrenal gland are more favorable for the laparoscopic approach than is primary malignant disease. Laparoscopy should be the initial step in the surgical approach to localized primary tumors as well as to solitary metastasis. Nevertheless, laparoscopic mobilization of the tumor with the minimum “handling,” without grasping the tumor should be the second step. Laparoscopic adrenalectomy should be per- formed only when it can achieve complete tumor resec-

Laparoscopic Surgery for Malignant Adrenal Tumors, Zografos GN et al

tion with an intact adrenal capsule. This is very important, as complete resection constitutes the only possibility of curing patients, and it should be taken into account that even small tumors may rarely be malignant. The principles of oncologic surgery should be routine for all adrenal tumors. If a complete resection cannot be performed safely, the operation should not be continued laparo- scopically. Conversion to an open procedure should be an early decision, prior to tumor morcellation or fracture of the tumor capsule. Patients who have local invasion, tu- mors that are too large, or require organ resection require an open procedure.

References:

1. Gagner M, Lacroix A, Bolte E. Laparoscopic adrenalectomy in Cushing’s syndrome and pheochromocytoma. N Engl J Med. 1992;327:1033.

2. Cobb WS, Kercher KW, Sing RF, Heniford TB. Laparoscopic adrenalectomy for malignancy. Am J Surg. 2005;189:405-411.

3. Gagner M, Pomp A, Heniford BT, et al. Laparoscopic adre- nalectomy: lessons learned from 100 consecutive procedures. Ann Surg. 1997;226(3):238-247.

4. Lal G, Duh QY. Laparoscopic adrenalectomy-indications and technique. Surg Oncol. 2003;12(2):105-123.

5. Palazzo FF, Sebag F, Sierra M, Ippolito G, Souteyrand P, Henry JF. Long-term outcome following laparoscopic adrenalec- tomy for large solid adrenal cortex tumors. World J Surg. 2006; 30(5):893-898.

6. Kebebew E, Siperstein AE, Duh QY. Laparoscopic adrenal- ectomy: the optimal surgical approach. J Laparoendosc Adv Surg Tech. 2001;11(6):409-413.

7. Novitsky YW, Czerniach DR, Kercher KW, et al. Feasibility of laparoscopic adrenalectomy for large adrenal masses. Surg Laparosc Endosc Percutan Tech. 2003;13(2):106-110.

8. Heniford BT, Area MJ, Walsh RM, et al. Laparoscopic adre- nalectomy for cancer. Semin Surg Oncol. 1999;16(4):293-306.

9. Terzolo M, Ali A, Osella G, et al. Prevalence of adrenal carcinoma among incidentally discovered adrenal masses. A retrospective study from 1989 to 1994. Arch Surg. 1997;132(8): 914-919.

10. Bernini GP, Miccoli P, Moretti A, et al. Sixty adrenal masses of large dimensions: hormonal and morphologic evaluation. Urology. 1998;51(6):920-925.

11. Al Fehaily M , Duh QY. Adenocortical carcinoma. In: Clark OH, Duh QY, Perrier N, et al, eds. Endocrine Tumors. Hamilton (Canada): BC Decker; 2003;123-30.

12. Third National Cancer Survey: incidence data. DHEW Publ.

No. (NIH) 75. NCI monograph. Bethesda: National Cancer In- stitute; 1975;41.

13. Latronico AC, Chrousos GP. Extensive personal experience: Adrenocortical tumors. J Clin Endocrinol Metab. 1997;82:1317.

14. Kasperlic Zaluska M, Migbalska BM, Makowska AM. Inci- dentally found adrenocortical carcinoma. Eur J Cancer. 1998;34: 1721.

15. Raeburn MD, McIntyre R. Laparoscopic approach to adrenal and endocrine pancreatic tumors. Surg Clin Am. 2000;80:1427- 1434.

16. Dackiw AP, Lee JE, Gagel RF, et al. Adrenal cortical carci- noma. World J Surg. 2001;25(7):914-926.

17. Sturgeon C, Kebebew E. Laparoscopic adrenalectomy for malignancy. Surg Clin North Am. 2004;84(3):755-759.

18. Fitzerald PA. Pheochromocytoma and paraganglioma. In: Clark OH, Duh QY, Perrier ND, Jahan T, eds. Endocrine Tumors. Hamilton (Canada): BC Decker Inc; 2003;100-122.

19. Gross MD, Shapiro B, Francis IR, et al. Scintigraphy of incidentally discovered bilateral adrenal masses. Eur J Nucl Med. 1995;22(4):315-321.

20. Saunders BD, Doherty GM. Laparoscopic adrenalectomy for malignant disease. Lancet Oncol. 2004;718-726.

21. Bravo EL, Gifford RW. Current concepts: pheochromocyto- ma-diagnosis, localization and management. N Engl J Med. 1984; 311:1298-1303.

22. Allolio B, Fassnacht M. Clinical review: Adrenocortical car- cinoma: clinical update. J Clin Endocrinol Metab. 2006;91(6): 2027-2037.

23. Terachi T, Kawakita M, Yoshiyuka K. Laparoscopic adrenal- ectomy: results of 47 cases. J Urol. 1995;153:513.

24. Eustace D, Han X, Gooding R, et al. Interleukin-6 (IL-6) functions as an autocrine growth factor in cervical carcinomas in vitro. Gynecol Oncol. 1993;50:15-19.

25. Rufini V, Calcani ML, Baum RP. Imaging of neuroendocrine tumors. Semin Nucl Med. 2006;36(3):228-247.

26. Li S, Beheshti M. The radionuclide molecular imaging and therapy of neuroendocrine tumors. Curr Cancer Drug Targets. 2005;5(2):139-148.

27. Esfandiari NH, Shulkin BL, Bui C, Jaffe CA. Multimodality imaging of malignant pheochromocytoma. Clin Nucl Med. 2006; 31(12):822-825.

28. Kaji P, Carrasquillo JA, Linehan WM, et al. The role of 6-[18F]fluorodopamine positron emission tomography in the lo- calization of adrenal pheochromocytoma associated with von Hippel-Lindau syndrome. Eur J Endocrinol. 2007;156(4):483- 487.

JSLS

29. Ilias I, Pacak K. Diagnosis and management of tumors of the adrenal medulla. Horm Metab Res. 2005;37(12):717-721.

30. Asgreirsson KS, Olafsdottir K, Jonasson JG, Ogmundsdottir HM. The effects of IL-6 on cell adhesion and e-cadherin expres- sion in breast cancer. Cytocine. 1998;10:720-728.

31. Meyer-Rochow GY, Sidhu SB, Soon PS, Sywak MS, Bambach CP. Laparoscopic adrenalectomy for pheochromocytoma is safe and effective. Aust N Z J Surg. 2007;77 Suppl 1:A25.

32. Mornex R, Badet C, Peyrin L. Malignant pheochromocytoma: a series of 14 cases observed between 1996-1990. J Endocrinol Invest. 1992;15(9):643-649.

33. Tato A, Orte L, Diz P, et al. Malignant pheochromocytoma, still a therapeutic challenge. Am J Hypertens. 10(4Pt 1):479-481, 1997.

34. Schlumberger M, Gicquel C, Lumbroso J, et al. Malignant pheochromocytoma: clinical, biological, histologic and thera- peutic data in a series of 20 patients with distant metastases. J Endocrinol Invest. 1992;15(9):631-642.

35. Nativ O, Grant CS, Sheps SG, et al. Prognostic profile for patients with pheochromocytoma derived from clinical and pathological factors and DNA ploidy pattern. J Surg Oncol. 1992;50(4):258-262.

36. Guerrieri M, De Sanctis A, Crosta F, et al. Adrenal inciden- taloma: surgical update. J Endocrinol Invest. 2007;30(3):200- 204.

37. Kebebew E, Duh QY. Benign and malignant pheochromo- cytoma: diagnosis, treatment and follow up. Surg Oncol Clin N Am. 1998;7(4):765-789.

38. Sarela AI, Murphy I, Coit DG, et al. Metastasis to the adrenal gland: the emerging role of laparoscopic surgery. Ann Surg Oncol. 2003;10:1191-1196.

39. Ayabe H, Tsuji H, Hauri D, et al. Surgical management of adrenal metastasis from bronchogenic carcinoma. J Surg Oncol. 1995;58(3):149-154.

40. Tanaka S, Ito T, Tomoda J, et al. Malignant pheochromocy- toma with hepatic metastasis diagnosed 20 years after resection of the primary adrenal lesion. Intern Med. 1993;32(10):789-794.

41. Kim SH, Brennan MF, Russo P, et al. The role of surgery in the treatment of clinically isolated adrenal metastasis. Cancer. 1998;82(2):389-394.

42. Shen WT, Kebebew E, Clark OH, Duh QY. Reasons for conversion from laparoscopic to open or hand-assisted adrenal- ectomy: review of 261 laparoscopic adrenalectomies from 1993 to 2003. World J Surg. 2004;28(11):1176-1179.

43. Henry JF, Sebag F, Iacobone M, Hubbard J, Maweja S. Lessons learned from 274 laparoscopic adrenalectomies. Ann Chir. 2002;127(7):512-519.

44. Curet MJ. Port site metastases. Am J Surg. 2004;187:705-712.

45. Gonzalez R, Smith CD, McClusky DA 3rd, et al. Laparoscopic approach reduces likelihood of perioperative complications in patients undergoing adrenalectomy. J Am Coll Surg. 2004;70(8): 668-674.

46. Suzuki K, Ushiyama T, Mugiya S, et al. Hazards of laparo- scopic adrenalectomy &iacgr;n patients with adrenal malig- nancy. J Urol. 1997;158:2227.

47. Porpiglia F, Fiori C, Tarabuzzi R, et al. Is laparoscopic adre- nalectomy feasible for adrenocortical carcinoma or metastasis? BJU Int. 2004;94(7):1026-1029.

48. Moinzadeh A, Gill IS. Laparoscopic radical adrenalectomy for malignancy in 31 patients. J Urol. 2005;173(2):519-525.

49. Heniford BT, Arca MJ, Walsh RM, Gill IS. Laparoscopic adrenalectomy for cancer. Semin Surg Oncol. 1999;16:293-306. 50. Giraudo G, Del Genio G, Porpiglia F, Parini D, Garrone C, Morino M. Laparoscopic adrenalectomy in multiple endocrine tumors, in secreting and non-secreting lesions. Minerva Chir. 2004;59(1):1-5.

51. Lombardi CP, Raffaeli M, Crea C, Bellantone R. Role of laparoscopy in the management of adrenal malignancies. J Surg Oncol. 2006;94:128-131.

52. Li ML, Fitzgerald PA, Price DC, et al. Iatrogenic pheochro- mocytosis: a previously unreported result of laparoscopic adre- nalectomy. Surgery. 2001;130(6):1072-1077.

53. Kebebew E, Siperstein A, Clark O, Quan-Yang D. Results of laparoscopic adrenalectomy for suspected and unsuspected ma- lignant adrenal tumors. Arch Surg. 2002;137:948-953.

54. Sturgeon C, Kebebew E. Laparoscopic adrenalectomy for malignancy. Surg Clin Am. 2004;84:755-774.

55. Matsuda T, Murota T, Oguchi N, et al Laparoscopic adrenal- ectomy for pheochromocytoma: a literature review. Biomed Pharmacother. 2002;56(suppl 1):132S-8s.

56. Zografos GN, Kothonidis K, Aggeli C, et al. Laparoscopic resection of large adrenal ganglioneuroma. JSLS. 2007;11(4):487- 492.

57. Lucchi M, Dini P, Ambrogi MC, et al. Metachronous adrenal masses in resected non-small cell lung cancer patients: therapeu- tic implications of laparoscopic adrenalectomy. Eur J Cardiotho- rac Surg. 2005;27(5):753-756.

58. Henry JF, Sebag F, Iacobone M, Mirallie E. Results of lapa- roscopic adrenalectomy for large and potentially malignant tu- mors. World J Surg. 2002;26(8):1043-1047.

59. Raeburn CD, McIntyre RC. Laparoscopic approach to adre- nal and endocrine pancreatic tumors. Surg Clin North Am. 2000; 80:1427-1433.

Laparoscopic Surgery for Malignant Adrenal Tumors, Zografos GN et al

60. Zografos GN, Markou A, Aggeli CH, et al. Laparoscopic surgery for adrenal tumors. A retrospective analysis. Hormones. 2006;5(1):52-56.

61. Nocca D, Aggarwal R, Mathieu A, et al. Laparoscopic surgery and corticoadrenalomas. Surg Endosc. 2007;21(8):1373-1376.

62. Zografos GN , Farfaras A, Ageli C, Kontogeorgos, Vasiliadis G, Papastratis G. Laparoscopic adrenalectomy for large adrenal

metastasis from contralateral renal cell carcinoma. JSLS. 2007; 11(2):261-265.

63. Kirshtein B, Yelle JD, Moloo H, Poulin E. Laparoscopic adrenalectomy for adrenal malignancy: a preliminary report comparing the short-term outcomes with open adrenalectomy. J Laparoendosc Adv Surg Tech A. 2008;18(1):42-46.

Graph View

Backlinks