Urologia Internationalis
Urol Int DOI: 10.1159/000446352
The Pathologic Point of View of Laparoscopic Adrenalectomy in the Era of Radiologic Imaging: A Multicenter Retrospective Study
Senol Tonyalia Fatih Atac” Unsal Eroglub Sertac Yazicia Ender Ozdenc Sinan Sozenb Cenk Yücel Bilenª
Departments of Urology, School of Medicine ªHacettepe University, and bGazi University, Ankara, and “Ondokuz Mayis University, Samsun, Turkey
Key Words
Laparoscopy . Adrenalectomy . Lung cancer . Adrenal metastasis · Adrenocortical carcinoma
Abstract
Introduction/Aim: This study aimed to determine if laparo- scopic adrenalectomy (LA) is feasible for the treatment of adrenal malignancies and metastasis, and to review the final pathology findings in order to clarify the indications for sur- gery. Materials and Method: The medical records of all pa- tients that underwent LA at 3 university hospitals between January 1, 2008, and May 1, 2015, were retrospectively re- viewed. Results: In total, 189 laparoscopic adrenalectomies were completed successfully. Mean duration of surgery was 79.3 ± 38.6 min and mean estimated intraoperative blood loss was 39.9 ml. Intraoperatively, 4 patients had major com- plications: spleen injury (n = 1), renal vein injury (n = 2) and diaphragm injury (n = 2). Histopathological examination showed that there were 20 different types of lesions. Surgical margins (SMs) were tumor free in 95.2% of the patients. Moreover, SMs were tumor free in all patients with adreno- cortical carcinomas; however, positive margins were noted in 7 of 23 patients (30.4%) with malignant adrenal tumors. Conclusions: The present findings support the use of lapa-
roscopy for metastatic adrenal masses, despite a high posi- tive margin rate. LA is a safe, feasible and cost-effective pro- cedure for the management of benign and malignant adre- nal masses.
@ 2016 S. Karger AG, Basel
Introduction
The most common adrenal lesion is incidentaloma - an unsuspected asymptomatic adrenal mass coinciden- tally observed via imaging. Adrenal incidentaloma (AI) can be seen in ≤5% of patients that undergo thoracic and abdominal CT [1]. Management of AI is challenging, as numerous differential diagnoses must be taken into con- sideration. It must be determined if an AI is hormonally active and its malignant potential must be estimated to effectively plan follow-up or surgery [2]. Up to 30% of adrenal adenomas cannot be differentiated from malig- nant lesions via CT. Despite the known indications for adrenalectomy, including tumor size, radiological ap- pearance indicative of malignancy, rapid growth during follow-up and an active hormonal status, the decision to perform surgical treatment is ultimately the surgeon’s [3].
KARGER
Recent adrenalectomy series reported numerous pa- thology results, including cortical adenoma, pheochro- mocytoma, adrenocortical hyperplasia, neurofibroma, myelolipoma, cortical carcinoma, schwannoma, ganglio- neuroma, spindle cell tumor, benign cyst, cystic tumor, lipoma, lymphangioma and inflammatory mass [4, 5]; however, the primary concern is the malignant character of the lesion, as it is well known that the complete resec- tion of adrenocortical tumors at an early stage improves prognosis [5]. Laparoscopic adrenalectomy (LA) is the gold standard treatment for benign adrenal lesions, but its use in patients with primary or metastatic disease re- mains controversial. Some researchers suggest that LA should be used in cases of potentially malignant tumors and adrenal metastases, although adrenocortical carcino- ma has a high recurrence rate following the procedure [6, 7]. The present study aimed to determine if LA is feasible for the treatment of adrenal malignancies and metastasis, and to review the final pathology findings in order to clar- ify the indications for surgery.
Material and Methods
The medical records of all patients who underwent LA at 3 uni- versity hospitals between January 1, 2008, and May 1, 2015, were retrospectively reviewed. The evaluated parameters were patient demographics, preoperative diagnostic findings (CT, USG, and endocrine tests), tumor localization, laparoscopic approach, tu- mor hormonal status, patient symptoms comorbidities, duration of surgery, intraoperative blood loss, intraoperative and postop- erative complications, histology, postoperative course, recurrence and long-term outcome for malignant and metastatic tumors. The study was conducted in accordance with the latest version of the Declaration of Helsinki. Statistical analysis was performed via a licensed commercial statistic program.
Results
In total, 189 patients underwent LA between January 1, 2008, and May 1, 2015. Among those patients, 102 (54%) were women and 87 were men (46%), and mean age was 48.6 years (range 18-74 years). In all, 16.9% (n = 32) of the patients were diagnosed incidentally. The most common patient symptoms were hypertension, dizzi- ness, palpitation, abdominal/lumbar pain, fatigue and weight gain (table 1).
LA was successfully completed in all 189 patients; however, the surgery in 3 cases was converted to open surgery due to abrupt bleeding or challenging dissection; 1 case had a giant (16 cm) adrenocortical carcinoma and
| Symptoms | n = 189 |
|---|---|
| Hypertension, % | 76 (40.2) |
| Incidental, % | 32 (16.9) |
| Abdominal/lumbar pain, % | 31 (16.4) |
| Fatigue, % | 17 (9.0) |
| Palpitation, % | 14 (7.4) |
| Weight gain, % | 13 (6.9) |
| Dizziness, % | 6 (3.2) |
| LA (n = 189) | |
|---|---|
| Mean age, years | 48.6±12.32 |
| Male/female, % | 87/102 (46/54) |
| Side (left/right), % | 103/86 (54.5/45.5) |
| Approach (trans/retroperitoneal), % | 187/2 (98.9/1.1) |
| Estimated blood loss (range), ml | 39.9 (0-500) |
| Transfusion, % | 5 (2.6) |
| Mean pathologic tumor size, mm | 40.17±22.3 |
| Intraoperative complications, % | 4 (2.1) |
| Conversion, % | 3 (1.5) |
| Postsurgical complication | |
| (Clavien grades 1-2), % | 22 (11.6) |
| Mean duration of hospitalization post surgery, days | 1.4±0.7 |
| Mortality | 0 |
| Functional tumor, % | 106 (56.1) |
2 had adrenocortical adenoma. These 3 patients were ex- cluded from the study. In total, 103 (54.5%) of the tumors were left-sided and the remaining 86 (45.5%) were right- sided. The transperitoneal laparoscopic approach was used in 187 patients versus the retroperitoneal approach in 2.
Mean duration of surgery was 79.3 + 38.6 min and es- timated mean intraoperative blood loss was 39.9 ml. There were not any significant differences in mean surgi- cal duration between the patients with adrenocortical ad- enomas (71.2 + 36.9 min) and those with adrenocortical carcinomas/pheochromocytomas (102.1 ± 37.6/79.4 ± 32.7 min) (p = 0.904 and p = 0.595, respectively). In all, there were 4 major intraoperative complications: spleen injury (n = 1), renal vein injury (n = 1) and diaphragm injury (n = 2) (table 2). Among the patients, 5 required blood transfusion postoperatively; the preoperative he- moglobin level in those patients was closer to the lower limit of normal ranges.
Histopathological examination of the tumors showed that there were 20 types, as summarized in table 3. Mean tumor size was 40.17 ± 22.3 mm. Mean postoperative du- ration of hospitalization was 1.4 ± 0.7 days. Surgical mar- gins (SMs) were tumor free in 95.2% (n = 180) of the pa- tients.
In histopathological examination, 28 patients were di- agnosed with pheochromocytoma. Mean pheochromo- cytoma size was 48.2 + 18.3 mm. Intraoperative hemody- namic instability occurred in 71.4% (n = 20) of the pa- tients despite preoperative alpha blockade for 3 weeks prior to surgery; fortunately, all procedures were com- pleted successfully using advanced monitoring and ag- gressive and immediate management. Pathologic exami- nation showed SM+ in 2 patients with pheochromocyto- mas. Local recurrence did not occur during a mean follow-up of 22.5 + 14.5 months in any patients with pheochromocytoma. In all, 89.2% (n = 25) of the patients that required antihypertensive medication prior to sur- gery had normal blood pressure without medication post surgery. In addition, 2 patients with SM+ did not require antihypertensive medication post surgery.
Among 189 patients, 23 patients had malignant adre- nal tumors including lung cancer metastases (n = 9), RCC metastases (n = 5), adrenocortical cancer (n = 7), malig- nant mesenchymal tumor (n = 1) and lymphoma (n = 1). Mean age of patients with malignant adrenal tumors was 51.7 years (range 21-69 years). Seventeen of 23 patients were men and 6 were women. All patients with metastatic adrenal tumors due to lung cancer were men. Mean tumor size, mean operation time and mean intraoperative blood loss of all 23 patients was 35.5 ± 19.5 mm, 86.6 + 34.3 min and 21 ± 49 ml, respectively. Positive SMs were noted in 7 of 23 (30.4%) patients with malignant adrenal tumors, of whom 2 developed local recurrence (table 4).
Among the patients, 9 with adrenal metastasis of lung cancer underwent LA; pathologic examination showed SM+ in 6 (66.6%) of the 9 patients. Among the 6 patients with SM+, 2 developed local recurrence and underwent radiotherapy. Additionally, 4 (44.4%) of the 9 patients with adrenal metastasis of lung cancer, of which 3 had SM+, died a mean 17.2 months post surgery; the other 5 patients were still alive after a mean follow-up of 31 months (range 27-47 months). Among the patients, 5 had adrenal metastasis of RCC, of which 1 had SM+ and died 18 months post surgery. The remaining 4 patients had no evidence of disease and were alive at a mean fol- low-up of 16.2 months (range 4-47 months).
All 7 adrenocortical carcinomas were extirpated suc- cessfully with clear SMs. Mean adrenocortical carcinoma
| Pathology | n (%) | Mean ± SD tumor size, mm | Positive pathologic margin, n (%) |
|---|---|---|---|
| Adrenocortical adenoma | 93 (49.2) | 31.7±15.2 | 0 |
| Pheochromocytoma | 28 (14.8) | 48.2±18.3 | 2 (7.1) |
| Myelolipoma | 10 (5.3) | 50.8±16.3 | 0 |
| Metastatic carcinoma (lung) | 9 (4.7) | 44.3±23.1 | 6 (66) |
| Cortical hyperplasia | 8 (4.2) | 16.5±10.9 | 0 |
| Adrenocortical carcinoma | 7 (3.7) | 43±26.0 | 0 |
| Metastatic carcinoma (renal) | 5 (2.6) | 66±49.4 | 1 (20) |
| Ganglioneuroma | 5 (2.6) | 76±10.8 | 0 |
| Hyalinized cortical nodule | 4 (2.1) | 37±19.7 | 0 |
| Nodular hyperplasia | 3 (1.6) | 64±7.9 | 0 |
| Pseudo cyst | 3 (1.6) | 0 | |
| Cavernous hemangioma | 3 (1.6) | 0 | |
| Endothelial cyst | 2 (1.1) | 0 | |
| Schwannoma | 2 (1.1) | 0 | |
| Epithelial cyst | 2 (1.1) | 0 | |
| Malignant mesenchymal tumor | 1 (0.5) | 0 | |
| Granulomatous | |||
| lymphadenitis | 1 (0.5) | 0 | |
| Lymphoma | 1 (0.5) | 0 | |
| Meningomyelocele | 1 (0.5) | 0 | |
| Normal adrenal tissue | 1 (0.5) | 0 |
size (38.1 ± 18.2 mm) did not differ significantly from mean adenoma size (31.7 ± 15.3 mm; p < 0.05). All the patients were alive with no local recurrence at a mean follow-up of 19.5 months.
In addition, 1 malign mesenchymal tumor and 1 lym- phoma were extirpated with clear SMs, and these 2 pa- tients are alive without disease at 20 and 4 months of fol- low-up, respectively.
Discussion
Management of adrenal masses is challenging due to the various differential diagnoses and variation in clinical behavior. Adrenal masses can be detected in symptom- atic patients or incidentally. Patients can present with such symptoms as hypertension and flushing suggestive of adrenal origin, or the masses can be detected during work-up for another malignancy. Diagnosis of adrenal masses is difficult and is usually not possible based on preoperative imaging. First, it must be determined if an adrenal mass is functioning or non-functioning, and be- nign or malignant. Approximately 6% of AIs are func-
| Patient No. | Age | Sex | Adrenalectomy pathology | Tumor size | Tumor side | Surgical margin | Local recurrence | Follow-up, months | Ex or alive |
|---|---|---|---|---|---|---|---|---|---|
| 1 | 57 | M | Lung cancer metastases | 63 | R | – | No | 6 | Ex |
| 2 | 45 | M | Lung cancer metastases | 45 | R | + | No | 47 | Alive |
| 3 | 52 | M | Lung cancer metastases | 40 | L | + | Yes | 36 | Alive |
| 4 | 69 | M | Lung cancer metastases | 26 | R | + | No | 25 | Ex |
| 5 | 60 | M | Lung cancer metastases | 13 | L | + | No | 20 | Ex |
| 6 | 66 | M | Lung cancer metastases | 66 | L | + | Yes | 18 | Ex |
| 7 | 58 | M | Lung cancer metastases | 20 | L | – | No | 27 | Alive |
| 8 | 66 | M | Lung cancer metastases | 12 | R | + | No | 27 | Alive |
| 9 | 57 | M | Lung cancer metastases | 15 | L | – | No | 18 | Alive |
| 10 | 60 | M | RCC metastases | 35 | L | – | No | 4 | Alive |
| 11 | 57 | M | RCC metastases | 40 | L | – | No | 47 | Alive |
| 12 | 59 | F | RCC metastases | 12 | R | – | No | 6 | Alive |
| 13 | 59 | F | RCC metastases | 12 | L | – | No | 8 | Alive |
| 14 | 69 | M | RCC metastases | 40 | L | + | No | 18 | Ex |
| 15 | 39 | F | Adrenocortical carcinoma | 25 | L | – | No | 36 | Alive |
| 16 | 67 | M | Adrenocortical carcinoma | 46 | R | – | No | 36 | Alive |
| 17 | 39 | M | Adrenocortical carcinoma | 70 | L | – | No | 14 | Alive |
| 18 | 32 | M | Adrenocortical carcinoma | 16 | L | – | No | 9 | Alive |
| 19 | 33 | M | Adrenocortical carcinoma | 46 | L | – | No | 1 | Alive |
| 20 | 41 | F | Adrenocortical carcinoma | 24 | R | – | No | 26 | Alive |
| 21 | 21 | F | Adrenocortical carcinoma | 40 | L | – | No | 15 | Alive |
| 22 | 50 | F | Malign mesenchymal tumor | 36 | L | – | No | 20 | Alive |
| 23 | 34 | M | Lymphoma | 75 | R | – | No | 4 | Alive |
M = Male; F = female; R = right; L = left.
tional and secreting cortisol, aldosterone and sex hor- mones [8]. As many as 30% of AIs cannot be differenti- ated from malignancy based on CT [3]; thus, surgical resection is necessary to rule out possibly malignant and aggressive tumors.
Pathologic examination is likely to show functioning and non-functioning adenomas, pheochromocytomas, myelolipomas, adrenocortical carcinomas and metastasis of various malignancies, as 70-80% of incidentalomas are benign adenomas, and ≤14% can be pheochromocytomas [9]. The remaining consists of benign cysts, adrenocorti- cal hyperplasias, schwannomas, ganglioneuromas, lymph- angiomas, liposarcomas, lymphomas, cavernous heman- giomas, angiomyolipomas, angiosarcomas and leiomyo- sarcomas [5, 9]. Additionally, there are some rarely seen pathologies, most of which have been presented as case reports, including plasmacytoma, ganglioneuroblastoma, sarcomatoid carcinoma, leiomyosarcoma, cavernous hemangioma, malignant perivascular epithelioid tumor, primitive neuroectodermal tumor, oncocytoma, lymph- angioma, fibrous tumor and lymphoma [10-20]. In addi- tion to these, in the present study, 1 malignant mesenchy-
mal tumor, 1 meningomyelocele and 1 granulomatous lymphadenitis were observed.
LA is considered to be the most appropriate method for pheochromocytoma surgery. Several studies suggest that LA is a safe, feasible and effective treatment modal- ity with favorable surgical duration, duration of hospital- ization, intraoperative blood loss and a low recurrence rate, even in patients with tumors ≥6 cm; however, intra- operative tumor spillage with subsequent pheochromo- cytosis and hemodynamic instability must be considered [21, 22]. As such, preoperative evaluation and prepara- tion must be carried out carefully. In the present study, common serious hemodynamic instability have been ex- perienced in up to 71% of patients with pheochromocy- toma, but no instances of tumor spillage occurred. More- over, microscopic SM+ observed in 2 patients had no ef- fect on the prognosis and both patients were disease free without antihypertensive medication. As AI is difficult to treat, LA for pheochromocytoma should be performed in experienced centers by a multidisciplinary team in- cluding an endocrinologist, anesthesiologist and sur- geon.
Adrenocortical carcinoma is a rare malignancy with an incidence of 0.5-2 per 1 million people and is associated with a poor prognosis. Tumor size on cross-sectional im- aging is the best predictor of malignancy of an adrenal mass, with a 4-cm cutoff and 93% sensitivity [23]. An ab- normal radiological appearance was reported to be supe- rior to tumor size for predicting malignancy [24]. None- theless, use of laparoscopy for aggressive malignant tu- mors remains controversial due to the low recurrence-free survival rate [25]. Miller et al. [26] reported higher rates of SM+ or intraoperative tumor spillage associated with laparoscopic resection of adrenocortical cancer compared to open resection. Another study reported that open and LA had similar disease-free survival rates. The researchers concluded that LA performed for localized adrenocortical carcinomas <10 cm by an experienced surgeon yields re- sults comparable with open adrenalectomy [27]. Agcao- glu et al. [28] reported local recurrence in 1 of 2 patients that underwent LA for adrenocortical carcinoma, despite clear SM. LA in experienced hands could be considered for resection of adrenal tumors >5 cm, but in such cases conversion to an open procedure must be considered if there is suspicion of local invasion [28, 29]. In the present study, SM was tumor free in all patients with adrenocorti- cal carcinoma and all were alive without disease during follow-up. As SM+ is a major factor for long-term sur- vival in adrenocortical carcinoma patients, candidates for laparoscopic surgery should be carefully selected.
Although 3% of all AIs are metastatic adrenal masses, adrenal metastasis can occur in 53% of lung cancer pa- tients. Adrenal metastasectomy can prolong survival in lung cancer patients with solitary adrenal metastasis. Many studies suggest that LA is a safe and feasible tech- nique in cases of adrenal metastasis, with acceptable out- comes [30, 31]; however, SM+ remains a major concern and occurred in 1 of 5 patients with RCC metastasis and in 6 of 9 patients with lung cancer metastasis in the pres- ent study.
The present study’s 9 patients with lung cancer metas- tasis and SM+ did not receive adjuvant treatment. During follow-up, 2 of these patients developed local recurrence and were treated with local radiotherapy. Additionally, during a mean follow-up of 17.2 months, 4 of the 9 pa- tients with lung cancer metastasis died due to disease pro- gression, of which 3 had SM+; the other 5 patients were alive at a mean follow-up of 31 months (27-47), of which 3 had SM+. All 9 of the patients with adrenal metastasis were alive with no evidence of adrenal disease at a mean follow-up of 24.4 + 16.7 months, which supports the use of LA for the treatment of metastatic adrenal masses.
Conclusion
LA is a safe, feasible and cost-effective procedure for treating both malignant and benign adrenal masses and yields favorable surgical and oncologic outcomes. Fur- thermore, LA is associated with a comfortable postopera- tive course and, therefore, might be considered the treat- ment of choice, especially in chemo-frayed patients. A multidisciplinary approach to LA, including an experi- enced clinician, radiologist, pathologist and surgeon, is associated with satisfactory outcomes.
Acknowledgments
None.
Funding
None.
Disclosure Statement
The authors declare that there are no conflicts of interest - fi- nancial or otherwise - related to the material presented herein.
Ethical Approval
The study was performed in accordance with the most recent version of the Declaration of Helsinki. Based on the study design, written informed consent of the patients was not required.
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Urol Int DOI: 10.1159/000446352
Tonyali/Atac/Eroglu/Yazici/Ozden/ Sozen/Bilen