Laparoscopic transperitoneal lateral adrenalectomy for malignant and potentially malignant adrenal tumours

According to most, if not all guidelines, any suspected adrenal malignancy is an indication for open adrenalectomy and this recommendation is very rarely questioned [10, 11]. Nowadays, most adrenalectomies worldwide are performed laparoscopically. Analyzing indications it becomes obvious that, at least in some cases, the abovementioned rule is silently and unnoticeably violated. Indeed, the true indication for the removal of incidentalomas results from concern that the early stages of cancer may have been overlooked [12]. All guidelines raise the issue of selection of cases where the risk of malignancy is high enough to justify adrenalectomy in hormonally silent tumours. As a natural consequence the firm adherence to this principle “always open surgery in any suspicion of malignant tumour” automatically implies that all incidentalomas should be operated classically. Meanwhile, looking at most series of minimally invasive adrenalectomy, at least half of all patients operated on for incidentalomas and internal contradiction using this approach is never questioned [13‐15]. Thus, we believe that the opinion about open surgery for non-secreting tumours should be revised. In our series the risk of malignancy in unsuspected incidentalomas was 3.9 %. Similar data can be found elsewhere [15, 16]. This implies that removing every incidentaloma in this way would be unnecessary overtreatment in almost all cases.

Even though it may sound controversial, we believe that the same is true for cases with a higher risk of malignancy. The precise preoperative diagnostics of the potentially malignant character of pheochromocytomas remains an important challenge. It is generally accepted that in over 10 % of cases they can exhibit a malignant phenotype [17]. Only metastases observed at diagnosis or infiltration of surrounding organs observed at diagnosis are certain features of malignancy. This is, however, very rare. In most cases, they develop postoperatively in the follow-up period. Unfortunately, if there are no metastases, it is not possible to precisely evaluate the degree of malignancy based on biochemical and imaging tests [18, 19]. Pathological examination may also prove inconclusive. The most frequently employed scale for estimating the risk is PASS (Pheochromocytoma of the Adrenal Gland Scaled Score), proposed by Thompson in 2002 [20]. Though highly popular, its effectiveness for discovering malignant pheochromocytomas is highly debatable [21, 22]. Thompson has suggested that tumours with a PASS ≥ 6 were biologically more aggressive than tumours with a PASS <4. Meanwhile, Strong has observed that all patients in whom a progression of the disease was observed had tumours with a PASS over 6 [8]. This criterion was adapted for the purposes of our analysis. However, based on our observations, it appears that if there are no metastases during the operation, the risk of relapse is very low, since none of our patients relapsed. To some extent, this confirms the opinions that the PASS, despite being the most frequently used tool, does not allow for precisely predicting the postoperative course after the adrenalectomy for pheochromocytoma. An important conclusion arising from the analysis of our results is that laparoscopic adrenalectomy is a safe procedure in cases of pheochromocytoma considered as potentially malignant neoplasms. Additionally, if the pathological examination shows characteristics that may indicate a malignant phenotype, the procedure does not have a negative impact on the patient's outcomes, as compared to open surgery. Other authors also consider laparoscopic surgery a safe method, and recommend it as the method of choice, regardless of tumour size and the preoperative clinical picture, even though the malignant potential of pheochromocytoma is relatively high [23‐25].

Nowadays, laparoscopic surgery has become a good alternative to open surgery in patients with isolated metastases. Despite certain controversy surrounding attempts at surgical treatment in patients with advanced stage cancer, it seems that, taking into account the advantages of minimally invasive techniques, laparoscopic adrenalectomy is perceived as an effective treatment method in chosen cases [26‐28]. Research including relatively numerous groups of patients shows that such treatment enables prolonged disease free survival. In Moreno's study of 317 patients, the survival rate after one, two, three and five years was 80 %, 61 %, 42 % and 35 %, respectively [26]. Romero Arenas reported similar results (70 % survival after a year, 44 % after 3 years and 38 % after 5 years) [27]. Vazquez underlined one more important aspect – the treatment results depend also on the type of the primary tumour and thus may differ between study groups [29]. In our study, the survival rates for patients with metastases after a year, 2 years and 5 years were 82.4 %, 46.2 % and 40 %, respectively, which is similar to the results reported by other authors. The published papers comparing laparoscopic adrenalectomy with open surgery did not indicate any difference in survival rate between the methods, though they did note the obvious advantages of laparoscopy in early postoperative outcomes. All this contributes to a preference for laparoscopy in patients with metastases to the adrenal glands [30, 31, 26, 32‐35, 29].

Our approach favours laparoscopy in all adrenal gland tumours, as it clearly emerges from this paper. In our series, in only 67.3 % (35/52) of the adrenal tumours with histologically confirmed malignant character was there significant suspicion of malignancy preoperatively. Furthermore, out of this group, 85.7 % (30/35) were patients with metastases. In other cases (17, 32.6 %) the character of the malignant or potentially malignant tumour was determined only postoperatively. Such a context calls into question the legitimacy of recommendations, which favour open techniques in these cases as nearly 1/3 of malignant tumours would be operated laparoscopically anyway. Some authors argue that in the case of primary adrenal malignancy, the preferred technique should be open surgery. They argue that local recurrence and peritoneal metastases occur sooner in patients who undergo laparoscopic adrenalectomy and positive resection margins are more frequently positive [36‐39]. Others believe that the surgical approach does not have such a significant impact [7, 40, 41]. It seems that the role of the operative technique is the key question in this debate. In our opinion, laparoscopy differs only in that it involves a different access to the operated area. It allows for performing exactly the same operation meeting all the oncological principles (including in multi-organ resection and full lymphadenectomy) as long as it is performed by a skilled and experienced surgeon. We are certain that this aspect has more influence on the outcomes than the type of access itself. Moreover, in tumours located elsewhere (for instance, colon cancer), laparoscopy is an equal alternative to open operations, while giving the well-known advantages of reduced surgical trauma [42, 43]. It is even more so from a practical point of view, since a return to more frequent application of open surgery seems impossible, and often stands in contradiction to the expectations of both the patients and surgeons. It seems, however, reasonable that beginning every operation with laparoscopy, even in cases of larger and potentially malignant tumours, may be beneficial. It allows for a minimally invasive assessment of the entire abdominal cavity, searching for distant metastases and estimating the possibility of radical resection of the lesion without exposing the patient to large surgical trauma. Obviously the need for conversion arises whenever technical difficulties put into question the oncological quality of the procedure (dissecting the tumour, which could lead to damaging the tumour capsule, or doubts as to possible infiltration of neighbouring organs) [44, 5, 45, 11]. We also do not support laparoscopic surgery at all costs. Overall, conversion was necessary for 5 patients, out of which in 3 cases it was for “oncological reasons” (impossibility of dissecting the tumour, suspicion of capsule rupture). In the remaining 47 (90.3 %) patients, the procedure was carried out laparoscopically. The presented R0 resection rate of 78.8 % is a fully acceptable result, and certainly comparable, if not better than the results for open surgery [7, 36, 39]. This suggests that the laparoscopy allows for the achievement of satisfactory oncological outcomes. According to our data, the survival rate for patients with ACC after 1, 2, and 5 years was, respectively, 81.8 %, 70 % and 50 %. These results are slightly better than in other papers; however, they need to be interpreted with some caution, given the small study group size [46, 6]. Another issue is that we are the high-volume referral centre for adrenal pathologies and this is a proven factor for better outcomes [47, 48].

Our study is not free from limitations. It is a single centre retrospective study on a small sample, therefore defining confounders can be difficult and there is a potential for population bias. All procedures were performed by the same very experienced laparoscopic surgeon (>370 laparoscopic adrenalectomies), therefore the results probably cannot be simply transferred to all surgical departments.