BIOE THI
OPTIKH, ‘ANAQUE TA
WORLD Journal of SURGERY @ 2002 by the Société Internationale de Chirurgie
Results of Laparoscopic Adrenalectomy for Large and Potentially Malignant Tumors
Jean-François Henry, M.D., Frederic Sebag, M.D., Maurizio Iacobone, M.D., Eric Mirallie, M.D.
Department of Endocrine Surgery, University Hospital La Timone, Boulevard Jean Moulin, 13385 Marseilles Cedex 05, France
Published Online: June 6, 2002
Abstract. Endoscopic adrenalectomy is the procedure of choice for pa- tients with small functioning adrenal tumors. For most surgeons invasive adrenal carcinoma is an absolute contraindication for laparoscopic ad- renalectomy (LA). Whether LA should be proposed for large (> 6 cm), potentially malignant tumors is questionable. The aim of this study was to evaluate the risks and outcome of LA performed in our department in patients with tumors > 6 cm and potentially malignant. We performed a retrospective study of 216 patients who underwent 233 LAs in our depart- ment from 1994 to 2000. We selected 19 patients with a tumor > 6 cm and potentially malignant: 8 nonfunctional tumors, 4 cortisol-secreting tu- mors, 1 virilizing tumor, and 6 pheochromocytomas. In none of these patients did preoperative investigations demonstrated invasive carci- noma. The median tumor size was 70 mm. LA was performed by a transperitoneal flank approach. Conversion to open adrenalectomy was performed in two patients owing to intraoperative evidence of invasive carcinoma. The median operating time was 150 minutes (range 95-240 minutes). Capsular disruption occurred during the dissection of two pheochromocytomas. There was no postoperative morbidity. Six patients had an adrenocortical carcinoma on pathologic diagnosis: three of the eight nonfunctional tumors, one of the four cortisol-secreting tumors, and one virilizing tumor. One patient presented with liver metastases 6 months after surgery and died. The five other patients are disease-free with a follow-up ranging from 8 to 83 months. The 13 patients with benign lesions (6 cortical adenomas, 1 ganglioneuroma, 6 pheochromocytomas) are disease-free with a median follow-up of 47 months (range 10-81 months). In experienced hands LA can be proposed for large, potentially malignant tumors. Conversion to open adrenalectomy should be per- formed if local invasion is observed during surgery. At present the risk of intraabdominal recurrence is unknown.
Endoscopic adrenalectomy is the procedure of choice for patients with small, benign, functioning adrenal tumors. On the other hand, for most surgeons preoperative demonstration of invasive adrenal carcinoma is an absolute contraindication for the endo- scopic approach. Up to now the role of minimally invasive surgery in the treatment of large, potentially malignant adrenal tumors has not been specifically addressed.
Without evidence of distant metastases or local invasion, the malignancy of large adrenal tumors is difficult to demonstrate
before and even during surgery. Tumor size is usually considered an indicator of malignancy but remains relatively insensitive and nonspecific. Computed tomography (CT) and magnetic resonance (MRI) characteristics of adrenal tumors are also used to help determine their risk of malignancy but are not always conclusive. Therefore whether endoscopic techniques should be performed for large, potentially malignant adrenal tumors is questionable. The aim of this study was to evaluate the risks and the outcome of laparoscopic adrenalectomy (LA) performed in our department in patients with large (> 6 cm), potentially malignant tumors.
Materials and Methods
We performed a retrospective study of 216 patients who under- went 233 LAs in our department from June 1994 to December 2000. We selected 19 patients with a solid tumor > 6 cm in diameter and potentially malignant (Table 1). Other large but benign-appearing lesions, such as cysts or myelolipomas, were not included in this series. Patients with a history of primary extra- adrenal malignancy and suspicion of adrenal metastases were also excluded.
There were 15 women and 4 men with a median age of 48 years (range 32-77 years). Classification of the physical status of pa- tients according to the American Society of Anesthesiology (ASA) score was ASA 1, 2 patients; ASA 2, 11 patients; ASA 3, 6 patients. Tumor size was evaluated on CT scan, MRI, or both. The median tumor size was 70 mm; the largest tumor measured 91 mm in diameter. Ten tumors were on the right side and nine on the left. There were eight nonfunctional tumors, four cortisol- secreting tumors, one virilizing tumor, and six solitary and spo- radic pheochromocytomas. In none of these patients did preop- erative investigations demonstrate invasive carcinoma. There was no evidence of local invasion, vascular invasion, or distant metas- tases on preoperative imaging studies.
The LAs were performed by a transperitoneal flank approach in a full lateral decubitus position, as described by Gagner et al. [1]. Four trocars were used on both sides. Carbon dioxide pressure was maintained at 14 mmHg for the whole procedure. Before the Harmonic Scalpel was available the dissection was achieved using a cautery hook or coagulating scissors. The adrenal arteries were
| Gender | Age (years) | Adrenal disease | ASA score | Tumor size (mm) | Side | Conversion to open operation | Complication | Follow-up | |
|---|---|---|---|---|---|---|---|---|---|
| Months | Status | ||||||||
| F | 46 | Adenoma, NF | 2 | 60 | Left | – | – | 66 | DF |
| M | 71 | Adenoma, NF | 2 | 65 | Right | – | – | 59 | DF |
| F | 48 | Adenoma, NF | 2 | 60 | Right | – | – | 17 | DF |
| M | 45 | Adenoma, NF | 3 | 60 | Right | – | – | 10 | DF |
| F | 32 | Adenoma, Cushing | 1 | 60 | Right | – | – | 81 | DF |
| F | 42 | Adenoma, Cushing | 2 | 60 | Right | – | – | 10 | DF |
| F | 38 | Ganglioneuroma, NF | 1 | 90 | Right | – | – | 60 | DF |
| F | 60 | ACC, Cushing | 2 | 79 | Left | + | – | 83 | DF |
| F | 64 | ACC, androgen PT | 2 | 62 | Left | – | – | 42 | DF |
| F | 54 | ACC, NF | 2 | 65 | Left | + | – | 34 | DF |
| F | 54 | ACC, Cushing | 3 | 82 | Left | – | – | 21 | Liver M+, death |
| F | 77 | ACC, NF | 2 | 76 | Left | – | – | 15 | DF |
| F | 39 | ACC, NF | 2 | 80 | Right | – | – | 8 | DF |
| M | 32 | Pheo | 2 | 70 | Right | – | – | 55 | DF |
| F | 48 | Pheo | 3 | 75 | Right | – | – | 49 | DF |
| F | 44 | Pheo | 3 | 80 | Left | – | Capsular disruption | 47 | DF |
| F | 49 | Pheo | 2 | 70 | Left | – | – | 27 | DF |
| M | 49 | Pheo | 3 | 75 | Left | – | Capsular disruption | 35 | DF |
| F | 57 | Pheo | 3 | 80 | Right | – | – | 23 | DF |
NF: nonfunctional; androgen PT: androgen-producing tumor; ASA: American Association of Anesthesiology; ACC: adrenocortical carcinoma; Pheo: pheochromocytoma; M+: metastases; DF: disease-free; LA: laparoscopic adrenalectomy.
clipped. When the Harmonic Scalpel became available, only the main adrenal vein required application of clips. After complete dissection, the glands were placed in a plastic bag. Ten were cut up into small pieces inside the bag before being extracted. Drainage was used routinely. All patients received prophylaxis for deep vein thrombosis. Nasogastric suction was not used postoperatively. Oral fluids were given on the next day. All patients stood and walked, on average, at postoperative day 1.5. Preoperative prep- aration with nicardipine and intraoperative nicardipine infusion were used to help control the blood pressure in patients with pheochromocytoma.
Results
The median operating time was 150 minutes (range 95-240 min- utes). There was conversion to open surgery in two patients owing to high suspicion of malignancy at the start of the laparoscopic procedure. Suspicion of malignancy was based on the difficulty of dissection, dense adhesions, and unusual and numerous retroper- itoneal feeding vessels. In both patients open surgery was per- formed via a subcostal incision without repositioning the patient.
Capsular disruption of two pheochromocytomas on the left side occurred at the end of the dissection. Hemodynamic changes occurred in four patients with pheochromocytoma, corrected in all cases without morbidity. There was no postoperative morbid- ity.
On final histologic diagnosis, six patients were found to have an adrenocortical carcinoma (ACC) (31.6%): three of the eight non- functional tumors, two of the four cortisol-secreting tumors, and one virilizing tumor. The median size of these six malignant tumors was 77.5 mm. The six tumors were stage II according to the Macfarlane classification [2]. The other 13 patients had a benign lesion (68.4%): six cortical adenomas, one ganglioneu- roma, and six pheochromocytomas. The median size of these 13 benign tumors was 70 mm.
Among the six patients with ACCs, three were treated with mitotane. The follow-up data of 12 patients were obtained by personal examination in the outpatient clinic; in the remaining 7 cases, the general practitioners or the endocrinologists were con- tacted to obtain follow-up data. All patients underwent follow-up measurements of tumor markers. Imaging studies (CT, MRI, or both) were repeated postoperatively in nine patients (six with ACCs and three with pheochromocytomas). The two patients with pheochromocytoma in whom there was capsular disruption of the tumor during dissection underwent, in addition to imaging stud- ies, postoperative scintigraphy using meta-iodobenzylguanidine. One patient with ACC presented with liver metastases 6 months after surgery and died. The five other patients with ACC are disease-free after a follow-up ranging from 8 to 83 months. The 13 patients with benign lesions are disease-free with a median fol- low-up of 47 months (range 10-81 months).
Discussion
Endoscopic adrenalectomy has become the gold standard in most patients with adrenal tumors. Several studies that compared en- doscopic with open adrenalectomy have shown that endoscopic procedures are associated with less postoperative discomfort, de- creased hospital stay, less postoperative disability, and a lower rate of complications [3-11].
There are few absolute contraindications for minimally invasive adrenal surgery, and most of them are not specific to adrenal surgery. Nevertheless, open surgery remains the approach of choice for invasive adrenal carcinoma. Open surgery provides the maximal exposure necessary for complete resection and allows vascular control of the inferior vena cava, aorta, and splenic and renal vessels when necessary. Whether large but well encapsulated adrenal masses without evidence of local invasion should be re- moved laparoscopically remains questionable. Up to now the
| Study | Patients (no.) | Adrenal disease | Delay (months) | Recurrence | Complication during LA |
|---|---|---|---|---|---|
| Hamoir [21] | 1 | ACC | 6 | PC | T. break |
| Foxius [22] | 1 | ACC | 6 | PC | T. break |
| Ushiyama [23] | 1 | ACC | 19 | LR | 0 |
| Iacconi [24] | 1 | ACC | 26 | LR + PC + PSM | 0 |
| Valeri [25] | 1 | ACC | — | LR | ? |
| Li [Abstract] | 4 | ACC | 3, 12, 24, 24 | LR | ? |
| Dackiw [26] | 1 | ACC | 6 | LR + PC | T. break |
| Li [27] | 2 | Pheo | 48, 48 | PC | T. break, excessive bleeding |
PC: peritoneal carcinomatosis; LR: local recurrence; PSM: port-site metastasis; T. break: tumor break.
consensus has been to restrict the endoscopic approach to adrenal tumors measuring < 5 to 6 cm in diameter.
Without taking into account the risk of malignancy, it has been recently demonstrated that in experienced hands the endoscopic resection of benign-appearing large adrenal masses up to 10 cm is technically feasible and safe [11-13]. For most surgeons the small working space provided by the retroperitoneal approach is not suitable for dissecting tumors > 5 to 6 cm in diameter. Therefore, the lateral transabdominal approach is the approach of choice. On the left side, once the spleen and the tail of the pancreas have been completely retracted medially, the dissection space is wide, and access to the blood vessels, particularly the adrenal vein, is easy and direct. On the right side, primary dissection of the vena cava and the adrenal vein may be impossible. One starts the mobilization of the tumor by dissecting its lateral, superior, and inferior aspects and then, after progressive mobilization of the mass, moves medially along the vena cava.
The main risk run by the surgeon during laparoscopic dissection of a large tumor is capsular disruption. Once the tumor capsule has been violated, if the tumor is malignant there is a risk of intraabdominal contamination. As with open surgery, large tu- mors should be excised en bloc. The possibly malignant nature of the tumor should be appreciated preoperatively as well as intra- operatively. Tumor size is usually considered an important vari- able when assessing the malignant potential of any adrenal mass. Tumors > 6 cm in diameter are likely to be malignant [14]. Nevertheless the exact frequency of large adrenal adenomas (> 6 cm) is unknown. In this series five of the eight nonfunctioning tumors were benign (four adenomas and one ganglioneuroma). In addition, the six pheochromocytomas were classified benign at final history.
The modalities CT and MRI are useful for distinguishing be- nign from malignant adrenal lesions. Myelolipomas, cysts, and adrenal hemorrhage each have specific features and are easily identified. Adenomas are homogeneous lesions with regular, en- capsulated margins. In contrast, CT characteristics of malignancy include tumor heterogeneity and irregular margins. Usually ade- nomas have low attenuation values (< 10 Hounsfeld units) or an unenhanced CT scan, whereas carcinomas have much higher attenuation values [15, 16]. As demonstrated by MRI, most adre- nal adenomas have a lipid-rich composition rather than the lipid depletion seen with most nonadenomatous lesions [17].
Adrenal scintigraphy with 131I NP 59 also may be helpful, as increased tracer uptake by a nonhyperfunctioning lesion indicates that the lesion is probably benign [18]. Fine-needle aspiration biopsy is not adequate for differentiating an adenoma from an ACC.
Despite these investigations, one must admit that sometimes a diagnosis of malignancy is not established before surgery. In these cases we do not believe that LA is formally contraindicated. On the contrary, we believe LA an additional method of exploration to assess possible malignancy. Intraoperative findings such as the presence of dense adhesions, fixation of the mass, local tissue reaction, and unusually numerous retroperitoneal feeding vessels are suggestive of malignancy. Even large, benign adrenal masses are usually dissected and separated from adjacent structures with- out any particular difficulty. When the surgeon encounters diffi- culty locating the fat planes between the tumor and surrounding tissues, malignancy should be suspected. With experience, it seemed to us that it is easier to detect these difficulties properly during laparoscopic dissection than during an open dissection. Intraoperative imaging with laparoscopic ultrasonography may also be useful [19, 20]. In these circumstances the procedure should be converted to open surgery. This situation occurred in two patients in this series, and a diagnosis of ACC was confirmed at final histology. Conversion to open surgery was performed via a subcostal incision without repositioning the patient. Neverthe- less, to obtain the maximal exposure we believe that it is prefer- able to reinstall the patient in the dorsal decubitus position.
We have completely removed four other ACCs by the laparo- scopic approach without difficulty. There were no signs of local invasion during surgery, and the tumors were well encapsulated macroscopically. En bloc resections were performed in all cases without any capsular disruption. Retrospectively, we believe that we would not have performed more extensive surgery through an open approach, even knowing that the tumor was malignant.
During the same period we performed 56 open adrenalecto- mies. A preoperative diagnosis of malignancy was highly sus- pected in 19 patients and confirmed at final histology: 7 ACCs, 7 metastases, 3 pheochromocytomas, 2 lymphomas. Among the 37 benign lesions, 4 nonsecreting cortical adenomas measuring > 6 cm in diameter were preoperatively classified as potentially ma- lignant. Because of our lack of experience with LA, we preferred to operate on these four patients with open surgery. During surgery the tumors appeared benign and were removed without any difficulty. Retrospectively, we regretted not having proposed laparoscopic approach in these four patients.
Some cases of local recurrence and intraperitoneal tumor dis- semination after LA for malignant lesions have recently been reported in the literature [21-27] (Table 2). Recurrences may be due to incomplete resection or capsular disruption of the tumor during dissection. These intraoperative complications are also observed during open surgery. Nevertheless, it should be pointed out that the safety of laparoscopic tumor dissection depends
mainly on the training and skill of the surgeon. In unexperienced hands, endoscopic instruments may be highly aggressive.
It has been advocated that the pneumoperitoneum may favor the transit of malignant cells intraperitoneally and free intraab- dominal cancer cell implantation at the wound site or in the abdominal cavity. This may explain the “chimney effect” after deflation of the pneumoperitoneum [28]. Aerosolization of tumor cells is possible but supposes previous tumor damage during the dissection. A review of the 12 cases reported in the literature (Table 2) demonstrates that a complication occurred during dis- section of five tumors (four tumor fractures and one case of excessive bleeding). In only two cases did the authors mention that the tumor was removed without rupture of its capsule.
Parietal implants at port sites are related to laparoscopic tech- nique. The contamination of trocars by instruments that have been in contact with a damaged tumor and subsequently contact of the trocar with the abdominal wall is one of the mechanisms involved. On the other hand, parietal recurrences are also ob- served after open surgery. Comparative studies in colorectal sur- gery demonstrated that parietal relapse appears in 1% of cases regardless of technique is used [29].
Because of the risk of tumor spillage some authors have con- cluded that LA should not be proposed for patients with large, potentially malignant tumors. We do not think that any final conclusion can be made based on only a few case reports. It is too early to evaluate the rate of recurrence after laparoscopic resec- tion of malignant adrenal masses. In addition, one must keep in mind that recurrences are also observed after open adrenal sur- gery for stage I and II tumors [30].
In the current stage of development of endoscopic techniques we believe that LA is contraindicated in patients with locally advanced tumors that may require en bloc resection of adjacent organs. However, in experienced hands, LA can be proposed for large (> 6 cm), potentially malignant adrenal tumors. The pro- cedure should be converted to open surgery if local invasion is suspected intraoperatively. At present the exact risk of intraab- dominal and parietal recurrence is unknown.
Résumé. La surrénalectomie laparoscopique (SL) est le procédé de choix pour les petites tumeurs fonctionnelles de la surrénale. Pour la plupart des auteurs, le cancer invasif de la surrénale est une contraindication absolue de la SL. Proposer la SL pour des tumeurs plus larges (> 6 cm) et potentiellement malignes reste problématique. Le but de cette étude a été d’évaluer les risques et l’évolution de la SL réalisée dans notre département pour des tumeurs dont le diamètre était supérieur à 6 cm et potentiellement malignes. Nous avons étudié de façon rétrospective 216 patients qui ont eu 233 SL entre 1994 et 2000. Nous avons sélectionné 19 patients ayant une tumeur > 6 cm et potentiellement malignes: huit tumeurs non fonctionnelles, quatre tumeurs sécrétant du cortisol, une tumeur virilisante et six phéochromocytomes. Aucun de ces patients avait un cancer invasif selon les examens préopératoires. La médiane de taille tumorale a été de 70 mm. La SL a été réalisée par une voie d’abord transpéritonéale située dans le flanc. Une conversion a été nécessaire chez deux patients en raison de l’envahissement. La médiane du temps opératoire a été de 150 minutes (range 95-240). La capsule a été déchirée pendant la dissection dans deux cas de phéochromocytome. Il n’y a eu aucune morbidité postopératoire. Six patients avaient un cancer de la corticosurrénale décelé sur la pièce anatomopathologique: trois parmi les huit tumeurs non-fonctionnelles, un parmi les quatre tumeurs sécrétantes, et la tumeur virilisante. Un patient est décédé six mois après chirurgie de métastases hépatiques. Les cinq autres patients sont sans récidive avec un suivi de huit à 83 mois. Les 13 patients porteurs de lésions bénignes (6 adénomes corticosurrénaux, un neurogangliome, 6 phéochromocytomes) sont sans récidive avec une médiane de suivi de 47
mois (extrêmes 10 à 81 mois). Dans des mains expérimentées, la SL peut être proposée pour des tumeurs volumineuses et potentiellement malignes. La conversion est conseillée s’il existe une invasion locale. A ce jour, le risque de récidive abdominale n’est pas connue.
Resumen. La suprarrenalectomía endoscópica constituye el tratamiento de elección de los pequeños tumores funcionantes de las suprarrenales. Para muchos autores, la suprarrenalectomía laparoscópica (LA) está formalmente contraindicada en los carcinomas suprarrenales invasivos. Se debate, sí la LA puede o no proponerse para el tratamiento de neoplasias potencialmente malignas, mayores de 6 cm. El objetivo del estudio fue valorar los riesgos y los resultados de la LA en pacientes, intervenidos en nuestro Servicio, por neoplasias suprarrenales mayores de 6 cm y, potencialmente, malignas. Se realiza un estudio reprospectivo de 216 pacientes, que entre 1994 y 2000, fueron 233 veces sometidos a una LA. Seleccionamos 19 casos con neoplasias > 6 cm, potencialmente malignas; se trataba de: 8 incidentalomas (no funcionantes), 4 tumores secretores de cortisol, 1 neoplasia virilizante y 6 feocromocitomas. En ningún caso las pruebas preoperatorias mostraron indicio alguno de carcinoma infiltrante. El tamaño medio de los tumores fue de 70 mm. La LA se realizó mediante abordaje transperitoneal a través de un flanco abdominal. Registramos dos reconversiones en sendos pacientes que, durante la intervención, demostraron padecer carcinomas invasivos. La duración media de la operación fue 150 minutos (rango 95-240). Durante la disección de dos feocromocitomas se produjo un desgarro capsular. Mortalidad operatoria nula. En el diagnóstico anatomopatológico 6 pacientes eran portadores de carcinoma suprarrenal: 3 en 8 incidentalomas, 1 en 4 tumores secretores de cortisol y en el caso de tumor virilizante. Un paciente desarrolló metástasis hepáticas a los 6 meses de la operación y murió. Los restantes (5 casos) están asintomáticos a los 8-83 meses de seguimiento. Los 13 pacientes con lesiones benignas (6 adenomas corticales, 1 ganglioneuroma, 6 feocromocitomas) no tenían síntoma alguno a los 47 meses de seguimiento (rango 10-81 meses). En manos experimentadas la LA está indicada en grandes tumores, potencialmente malignos, de las suprarrenales. La reconversión a cirugía abierta debe de realizarse cuando se observe infiltración local del tumor. Se desconoce el riesgo de recidivas.
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