Does intraoperative cyst rupture of malignant cystic renal masses really have no negative impact on oncologic outcomes?

When CRM rupture occurs during PN, surgeons are disturbed by the theoretical risk of tumor recurrence [11,12,13]. Spaliviero M. et al. [17] particularly emphasized that extreme caution and skilled laparoscopic techniques must be exercised to avoid CR and local spillage. A new technique to minimize the risk of accidental intraoperative rupture of CRM by using a SAND balloon catheter was developed by Nozaki T. et al. [18]. However, the innovative finding recently reported by Pradere B. et al. [14] proposed that intraoperative CR at PN of CRM did not increase the risk of recurrence. Although encouraging, this conclusion is less convincing for some reasons. First of all, 38 malignancy ruptures out of 50 CR from 8 institutions were enrolled into the study. The involved surgeons with different surgical experience and managements after intraoperative CR might affect oncologic outcomes. Secondly, 25% CRM were benign, which might lead to selection bias due to insignificance of benign CRM rupture. Besides, different pathological types and Fuhrman grades were not further stratified in patients with and without CR considering that tumors in CR group may have a lower malignant potential compared with nonCR group and might not be aggressive enough to lead to disease recurrence. Lastly, the shorter follow-up time of CR group than that of 9 recurrence cases might miss the later recurrence in CR group. Therefore, the larger population-based study with 406 patients pathologically diagnosed as malignant CRM in our institution was conducted to externally discover the relationship between intraoperative CR and tumor recurrence.

In our study, the incidence of intraoperative malignant CR was 7.9%, which was lower than the previous report [14]. The following reasons may explain the lower incident in our institution. Firstly, our data came from a large volume center, and all the cases were performed by experienced surgeons. Secondly, only malignant CRM were enrolled into our study, and the benign CRM probably ruptured more easily. Lastly, some cases of CR might be incorrectly classified as unruptured because surgeons might not describe CR in surgery records.

Our study found that the risk of recurrence in patients with CR was higher than that in patients without CR. This is consistent with the theoretically increased recurrence risk due to tumor spillage [11,12,13]. Compared with cases without recurrence in CR group, the pathological type of cases with recurrence is more aggressive. Two of 3 cases with type II pRCC experienced recurrence. On the contrast, 2 cases with type I pRCC did not experience recurrence. This is consistent with the fact that in pRCC, type II is more aggressive than type I [19,20,21]. Renal carcinosarcoma is an extremely rare tumor that progresses rapidly and has a poor prognosis [22, 23]. In our study, one patient with renal carcinosarcoma immediately suffered from local recurrence and distance metastasis within 2 months after CR. Mixed epithelial and stromal tumors (MEST) tend to be benign. However, some studies reported the presence of malignant MEST [24,25,26,27]. In our study, one patient with malignant MEST experienced recurrence at 23 months after CR. Yap Y. S. et al. [28] also reported that the intraoperative CR probably was an important risk factor for recurrence in MEST cases. Although ccRCC is considerably aggressive, no recurrence occurred in all 14 cases with ccRCC in our study which may be due to the low Fuhrman II or I grade in these cases. Besides, all 6 cases with MCRNLMP did not experience recurrence due to the low malignant potential. Moreover, in CD group, 10 ccRCC with 6 and 4 Fuhrman I and II, respectively, and 7 MCRNLMP cases also did not experience recurrence. Therefore, the conclusion that intraoperative CR had negative impacts on oncologic outcomes was far from convincing. The CR of tumors with low malignant potential perhaps have no negative impact on the prognosis. Once an extremely aggressive tumor ruptures, it can bring catastrophic consequences for the patients. However, the exact pathological type was not known until a few days after surgery. It is vitally important to preoperatively identify cases with high risk of recurrence after CR.

Bosniak classification [29, 30] is a classical system which categorizes CRM into five groups of different malignancy risks on the basis of computerized tomography findings. A multicenter study [31] showed that CRM with Bosniak IV had a higher malignant potential than CRM with Bosniak III. In our study, CRM with Bosniak IV had a significantly higher rate of ccRCC and lower rate of MCRNLMP and pRCC compared to CRM with Bosniak III and Bosniak I-IIF. After three pathological types including ccRCC, type II pRCC, and renal carcinosarcoma were classified as highly aggressive tumors and other pathological types were classified as less aggressive tumors, CRM with Bosniak IV had a higher rate of highly aggressive tumors than CRM with Bosniak III and Bosniak I-IIF. Besides, CRM with Bosniak IV also had a significantly higher rate of Fuhrman II and III grade than CRM with Bosniak III and Bosniak I-IIF. In summary, CRM with Bosniak IV were more aggressive than CRM with Bosniak I-III. In this study, 2 of 4 cases with Bosniak IV and 2 of 20 cases with Bosniak III experienced recurrence. Meanwhile, no recurrence occurred in 8 CR cases with Bosniak IIF and 17 CD cases with Bosniak I or II. The recurrence rate of CRM with Bosniak IV (50%) was significantly higher than that of CRM with Bosniak I-III (4.4%). Moreover, in nonCR group, the recurrence rate of CRM with Bosniak IV was comparable to that of CRM with Bosniak IIF-III. Therefore, for CRM with higher Bosniak classification, especially Bosniak IV, rupture should be avoided because of the higher risk for recurrence.

Another important finding in our study was that tumor size and Bosniak classification were independent risk factors for CR. It is well understood that the larger the diameter of CRM, the greater the possibility of rupture during surgery. The cyst wall of CRM with Bosniak IV is thicker than that of CRM with Bosniak IIF and III [29], which may contribute to the higher probability of rupture in CRM with low Bosniak staging and explain the earlier recurrence in nonCR cohort than the CR group for the malignancy nature in Bosniak IV CRM. The larger number of CRM rupture with Bosniak IIF-III led to the larger number of less aggressive tumors in CR group, which could weaken and even cover up the true effect of intraoperative CR on oncologic outcomes.

The major limitation of our study is the retrospective and single-centered nature. Besides, the surgery records lack reliability for that some CR cases might be incorrectly classified as unruptured. Moreover, different techniques of various surgeons could lead to bias, and the follow-up time was not long enough for more convincing results. Prospective multicenter studies with a larger number of patients and longer follow-up time are expected in the future to further reassure the conclusions.

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