Discussion

RCCs are the most frequently encountered primary malignancy of the kidney. They refer to a group of cancers originating from the renal epithelial cells, which may arise either sporadically or as a familial disease. They can be categorised into different histological subtypes, with clear cell RCC (ccRCC) as the most common, followed by pRCC, chromophobe, oncocytoma, collecting duct and not otherwise specified (NOS).4 Most RCC cases are diagnosed incidentally as either solid or cystic mass through radiological imaging modalities, such as US, CT or MRI.5 Despite mostly present in the form of solid mass, approximately 1%–14% may have cystic components. More commonly known as cRCC, they are the leading cause of malignant cystic lesions in the kidney.5–7 They can manifest as intrinsic unilocular cysts, intrinsic multilocular cysts, cysts with necrotic features and unilocular cysts originating from existing mural tumours.6 7 Most of the different RCC histological subtypes can present as these complex cysts. but among which ccRCCs and pRCCs are the two most common.8–10

cRCCs are known to confer good prognosis, especially following surgical resection, as they typically present with smaller tumour size and of lower stage and grade.8–11 Winters et al demonstrated these through a retrospective study comparing 678 cRCCs with 46 677 solid ccRCCs, where cRCCs were reported to be significantly smaller (mean size of 38 mm for cRCC vs 45 mm for solid ccRCC, p<0.001), of lower stage (pT1a 66% for cRCC vs 55% for solid ccRCC, p<0.001) and more commonly well differentiated (33% for cRCC vs 16% for solid ccRCC, p<0.001). Winters et al also highlighted those with cystic necrosis, such as demonstrated in our patient, to have lower 4-year survival of 80% compared with 100% without necrotic features.11

The characterisation of cystic renal lesion relies on the Bosniak Classification, which provided means to stratify malignancy risks based on a multitude of radiological features, including the appearance of cyst wall, cystic content, septation, calcifications and contrast enhancement.8 Bosniak IIF, III and IV lesions are more likely to be cancerous, each with malignancy risks of 5%–38%, 40%–70% and 90%–91%, respectively.8–10 The latter two were more often referred for surgical management as, in addition to the risk of being malignant, higher Bosniak categories were known to be associated with raised likelihood of pT3–4 tumours (IIF 0% vs III 3.5% vs IV 15.6%, p=0.04) and of the higher nuclear grade 3–4 tumours (IIF 0% vs III 12% vs IV 36%, p<0.001), as demonstrated by Nouhaud et al and Boissier et al, respectively.8 9 Bosniak categories, however, were not associated with increased incidence of recurrence or differences in the 5-year recurrence-free survival (IIF 82% vs III 92% vs IV 92%, p=0.60).8–10

The recurrence rate of malignant cystic renal lesions following surgical resection, including those presenting as locoregional recurrence or distant metastases, is relatively low, ranging between 1.1% and 8.6%.8–10 More common metastatic sites include retroperitoneal lymph nodes, lung, liver, bone and brain. Peritoneal involvement in RCC, which can lead to malignant ascites, as observed in our case was relatively uncommon, only affecting 1% of the population.2 Nevertheless, the incidence of malignant ascites appeared to be higher in pRCC, compared with other histological subtypes of RCC, even in the absence of other distant metastatic sites. These were demonstrated by Sidana et al, who found malignant ascites in 20% of their 100 patients with pRCC. Of the 20 patients with ascites, distant metastatic sites at the time of diagnosis were identified in 30% with no significant differences compared with 24.1% patients without ascites (p=0.609). More importantly, malignant ascites was recognised as a poor prognostic indicator with significantly reduced median overall survival in those affected (25 months in patients with ascites vs 42.5 months in patients without ascites, p=0.041).1

The relatively high prevalence of malignant ascites reported by Sidana et al may be surprising given the limited number of prior publications for evidence of peritoneal carcinomatosis and/or malignant ascites attributed to RCC. Based on previous reports, peritoneal carcinomatosis, with or without ascites, can be associated with ccRCC, pRCC and NOS histological subtypes.2 12–18 As reported by Sidana et al, ascites may develop up to 73 months following the initial RCC diagnosis with a median time of 16 months.1 As reflected in table 1, peritoneal carcinomatosis may also be identified before or after primary tumour resection.2 12–18 Ploumidis et al identified a 5 mm omental nodule 24 months after a transperitoneal robot-assisted radical nephrectomy for a Fuhrman grade 1, pT2 pRCC.12 Pandey et al reported a case of multiple peritoneal nodules at the ileocolic junction diagnosed on exploratory laparotomy for right iliac fossa pain 6 months after radical nephrectomy.13 Similar to our patient, the two postoperative peritoneal carcinomatosis cases were diagnosed together with other potential distant metastatic foci, with ours being the subpleural apical nodule.12 13

In terms of pathophysiology, it was postulated that peritoneal carcinomatosis in RCC might be secondary to either direct tumour extension outside of the renal capsule and Gerota’s fascia, or an embolic haematogenous metastatic event into the omentum, mesentery and peritoneum.1 2 14 However, considering the possibility of the disease to manifest in the setting of smaller, low-stage and low-grade primary tumours, such as the Fuhrman grade 2, pT2 pRCC lesion in our case and the grade 1, pT2a pRCC lesion reported by Ploumidis et al,12 the latter hypothesis might be more likely. Certain general factors can contribute to tumour recurrence, which can be differentiated into tumour-related factors, local wound and patient’s immune response, as well as surgical approach and perioperative complications.19 Through their multivariate analysis, Boissier et al identified Fuhrman grade 4 tumours and patient’s general status at the time of surgery in the form of their American Society of Anaesthesiologist (ASA) score to be prognostic factors for recurrence.8

Regarding surgical approach, the cystic nature of cRCC should necessitate caution to minimise the risk of perioperative cyst rupture, which may lead to consequent seeding. This is more relevant for cRCC, for the smaller, well-localised and well-differentiated tumours often prompt clinicians to consider less invasive approaches, in the likes of laparoscopic and/or nephron-sparing surgeries. Chen et al identified that factors such as greater endophytic properties of the tumour, closer proximity to renal collecting system, Bosniak III lesions and surgeon’s experience correlate with risk of intraoperative cyst rupture.3 However, despite the risk, the incidence of tumour seeding following urological laparoscopic surgery is relatively low, ranging between 0.1% and 4%,19 and the cyst rupture may not necessarily cause tumour seeding and subsequent recurrence. In a study involving 268 partial nephrectomy patients with 18.7% incidence of cyst rupture, Pradere et al found no evidence of recurrence or peritoneal carcinomatosis and port-site metastasis up to 100 months postoperatively.20 A prior study by Spaliviero et al involving 284 laparoscopic partial nephrectomy cases echoed a similar phenomenon, whereby only one retroperitoneal recurrence was reported 14 months postoperatively despite the negative margins and absence of intraoperative cyst rupture in all cases.21 The study by Chen et al also highlighted that only four of nine patients with recurrence were reported to have cyst rupture, and no association can be derived between cyst rupture with the site of recurrence (p=1.00).3 Our case was an example of recurrence presenting as peritoneal carcinomatosis following a laparoscopic radical nephrectomy in the setting of negative cytology from the aspirated cystic content intraoperatively without any involvement of the renal bed or retroperitoneal lymph node. One potential explanation can be that tumour recurrence is more associated with the aggressiveness of the primary malignancy rather than intraoperative cyst rupture, as the malignant component of cystic tumours is usually more limited to its solid portion.20