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Journal of Indian Association of Pediatric Surgeons
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REVIEW ARTICLE
Year : 2022  |  Volume : 27  |  Issue : 1  |  Page : 13-24
 

Nephron-sparing surgery in nonsyndromic unilateral wilms' tumor: An insight into the ongoing surgical controversy


Department of Pediatric Surgery, Lady Hardinge Medical College, Associated Kalawati Saran Children's Hospital; Department of Pediatric Surgery, Maulana Azad Medical College, Associated Lok Nayak Hospital, New Delhi, India

Date of Submission29-Sep-2021
Date of Decision03-Nov-2021
Date of Acceptance05-Nov-2021
Date of Web Publication11-Jan-2022

Correspondence Address:
Dr. Yogesh Kumar Sarin
Department of Pediatric Surgery, Lady Hardinge Medical College, Associated Kalawati Saran Children's Hospital, New Delhi
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jiaps.jiaps_205_21

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   Abstract 


Background: Unilateral Wilms' tumor (uWT) is the most common renal malignancy in the pediatric population. Although the onset of surgical intervention like radical nephrectomy (RN) has substantially reduced the mortality rate, recent evidence has raised concerns regarding several postoperative complications associated with this procedure. Nephron-sparing surgery (NSS) has been reported to avoid such postoperative complications and have high technical success rate. However, not much literature is available comparing the efficacy of RN and NSS for managing nonsyndromic uWT, which makes it less acceptable globally. Materials and Methods and Results: A systematic identification of the literature was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-analyses guidelines on four academic databases: MEDLINE, Scopus, EMBASE, and CENTRAL. Out of 1017 records, 20 manuscripts including 312 patients were included in the review; 4 patients treated by the author (unpublished data) have also been included. The studies included 7 retrospective case series with no comparison group, 4 retrospective case series with comparison group, 4 retrospective series with a cursory mention of NSS in uWT, 2 case reports, 1 protocolized prospective trial with comparison group, 1 administrative database analysis with comparison group, and 1 randomized controlled study. In all, 316 patients with nonsyndromic uWT were studied. The pretherapy volumes of the WT ranged from 2.4 to 640 ml. Majority of them were administered preoperative chemotherapy. About half of the patients (n = 159) (50.3%) were Stage I tumors. Stage II, III, and IV tumors were seen in 23 (7.3%), 20 (6.3%), and 3 (1%) patients. Stage was not specified in 111 (35.1%) patients. Majority of them were “intermediate risk” WT. All these tumors were nonanaplastic. Surgical margins were reported positive in 13 (4%) patients. Overall and event-free survivals were 100% in most of the studies; only handful of relapses were noted in this systematic review. Conclusions: This qualitative systematic review recommends the use of NSS for nonsyndromic uWT. The procedure accounts for higher postoperative renal function and lesser incidence of hypertension as compared to the radical nephrectomy. Overall and event-free survivals are comparable or even better with NSS.


Keywords: Enucleation, nephrectomy, nephroblastoma, nephron-sparing surgery, partial nephrectomy, pediatric cancer, renal function, renal tumor, unilateral nonsyndromic Wilms' tumor, unilateral Wilms' tumor


How to cite this article:
Sarin YK. Nephron-sparing surgery in nonsyndromic unilateral wilms' tumor: An insight into the ongoing surgical controversy. J Indian Assoc Pediatr Surg 2022;27:13-24

How to cite this URL:
Sarin YK. Nephron-sparing surgery in nonsyndromic unilateral wilms' tumor: An insight into the ongoing surgical controversy. J Indian Assoc Pediatr Surg [serial online] 2022 [cited 2022 May 25];27:13-24. Available from: https://www.jiaps.com/text.asp?2022/27/1/13/335555





   Introduction Top


However true it may be that some diseases baffle the skill of the medical practitioner, resisting all his curative and palliative attempts, yet these disappointments ought never so to influence his mind as to damp his exertions, or restrain his endeavors in acquiring a more accurate knowledge of the malady under which his patient labors, for as diseases become more difficult to remove, so should his researches become the more unwearied and assiduous.…”

Thus wrote Rance of London in 1814[1] when he reported the first case of nephroblastoma, 85 years before Wilms' classical description. These words are as true today as they were more than two centuries ago.

Wilms' tumor (WT) is one of the success stories of pediatric oncology with long-term overall survival (OS) approaching ~90% in localized disease and over 70% for metastatic disease quoted in the developed world. This is marked improvement from the OS of ~30% reported seven decades ago. This improvement is due to the development of multimodal treatment for this disease based through international collaboration on trials conducted by the International Society of Pediatric Oncology (SIOP) and the Children's Oncology Group (COG). Besides these two major groups, there have many other groups had been working for the guidelines for the management of WT such as the United Kingdom group, the Italian group, the French Group, the German Group, the Polish Group, Japanese Group, the Brazilian Group,[2] and more recently even an Indian Group.

The treatment of WT is multimodal, where surgery plays an important role in removing the bulk of the disease. It is not conclusively known whether it was Jessop[3] or Kocher and Langhans[4] who performed the first successful extirpation of a WT in a child. The addition of radiotherapy (XRT) in 1916[5] and chemotherapy (ChT) in 1955[6] has not changed the place of surgical extirpation in the treatment of WT. The radical nephroureterectomy (RN) along with lymph node sampling has been unquestionably the gold standard for surgical extirpation of unilateral WT (uWT) since 1963 after Robson described it for renal cell carcinoma.[7] In 1957, Rickham[8] first described a case of bilateral WT (BWT) treated by nephrectomy on one side and partial nephrectomy (PN) on the other side. However, the pendulum over the next half century has conclusively moved in favor of bilateral NSS in this context. The role of nephron-sparing surgery (NSS) or PN in the management of BWT, in single anatomic or functional kidney, in fused kidneys (e.g., horse-shoe kidney), in the presence of bilateral nephroblastomatosis or in patients with syndromic disposition, is indisputable now.

Simultaneously, some other newer concepts also crept in the management of WT during the last half century. These include the NSS in nonsyndromic uWT, use of minimally invasive surgery (MIS) in the treatment of WT, preoperative ChT, contralateral exploration, lymph node sampling, adrenal preservation, and pulmonary metastasectomy.[9] Some of these issues seem to have been settled for good, e.g., thorough lymph node sampling is considered mandatory for disease staging and to direct adjuvant therapy. Contralateral exploration has been almost written off in the era of highly sensitive and specific cross-sectional imaging, and data show that it is safe to preserve the ipsilateral adrenal gland where technically feasible. Pulmonary metastasectomy is now known to provide good overrall survival (OS) and also to obviate the need for whole-lung radiotherapy (XRT) in patients with a few nodules (n</=3) that do not clear with ChT. However, there is still a divided house on the utility of NSS and MIS techniques. In this systematic review, we shall review the role, feasibility, technical considerations, and outcomes of NSS in nonsyndromic uWT.


   Materials and Methods Top


This systematic review was carried in adherence to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Four academic databases (MEDLINE, CENTRAL, EMBASE, and Scopus) from inception until July 2021 using MeSH keywords were searched. The following terms in all academic databases in different combinations “Wilms' Tumor,” “Unilateral Wilms' Tumor,” “Unilateral Wilms' tumor,” “Nephron-Sparing Surgery,” “Partial Nephrectomy,” “Radical Nephrectomy,” and “Total Nephrectomy” were used. In addition, we manually screened the bibliography of the included studies for any additional relevant study. The inclusion criteria for the included studies were as follows:

  1. Studies mentioning NSS on uWT in pediatric population, i.e., <18 years old
  2. Studies published in peer-reviewed scientific journals and conferences.


The case reports and case series mentioning NSS in uWT where the contralateral kidney was either congenitally absent or nonfunctional or was removed earlier for WT (metachronous WT) or any other pathology were excluded.

The present study could at best be called a qualitative systematic review.


   Results Top


A preliminary search on four academic databases resulted in a total of 1107 studies; 116 more studies were included after the bibliography of articles were screened. Thereafter, upon excluding the duplicates and applying the inclusion criteria, a total of 20 studies were retained. Qualitative data of 312 patients were then extracted from all the studies and summarized in [Table 1];[10],[11],[12],[13],[14],[15],[16],[17],[18],[19],[20],[21],[22],[23],[24],[25],[26] 4 patients treated by the author (unpublished data) have also been included. The studies included 7 retrospective case series with no comparison group,[11],[16],[17],[21],[24],[27],[28] 4 retrospective case series with comparison group,[12],[22],[25],[26] 4 retrospective series with a cursory mention of NSS in uWT,[13],[14],[15],[18] 2 case reports,[10],[20] 1 protocolized prospective trial with comparison group,[25] 1 administrative database analysis with comparison group,[23] and 1 randomized controlled study (RCT).[29]
Table 1: Patients characteristics and outcomes

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The patients with benign renal tumors (including cystic nephroma) or non-Wilms' renal tumors that were historically included as uWT undergoing NSS were excluded from the systematic review and that explains the discrepancy in the numbers of patients mentioned in [Table 1]. There were also minor discrepancies in the data regarding the same 8 patients who underwent NSS for uWT in different publications by the Italian group, but all efforts were done to correct the details.

In all, 316 patients with nonsyndromic uWT were studied. The pretherapy volumes of the Wilms' tumors ranged from 2.4 to 640 ml. Majority of them were administered preoperative ChT. About half of the patients (n = 159) (50.3%) were Stage I tumors. Stage II, III, and IV tumors were seen in 23 (7.3%), 20 (6.3%), and 3 (1%) patients. Stage was not specified in 111 (35.1%) patients. Majority of them were “intermediate risk” WT. All these tumors were nonanaplastic. Surgical margins were reported positive in 13 (4%) patients. Overall and event-free survivals were 100% in most of the studies; only handful of relapses were noted in this systematic review [Table 1].

The 4 patients treated by author in 2018–2019 by NSS (unpublished data) are also detailed in [Table 1].


   Discussion Top


Although the first recorded PN for nonsyndromic uWT was done in Cuba in 1966,[30] the contralateral kidney of this patient was not normal and eventually warranted its complete suppression (read excision). The real thrust to NSS in uWT was given by two groups - Cozzi et al. working at La Sapienza University, Rome, Italy[31] and Cost et al.[32] from University of Texas, Dallas, USA. There is no denial that the Italian group has published scores of articles but has operated on only 8 patients with nonsyndromic uWT and normal contralateral kidney in the past 3 decades! Met with initial skepticism, publications have accumulated data now on over 300 patients indicating a likely defining role for NSS for localized tumor lesions even in nonsyndromic uWT showing equivalent survival, morbidity - rupture rate(s), recurrence versus RN [Table 1]. A recent article from Germany has touted NSS in uWT as the most promising of the four innovations in the surgical treatment of pediatric solid tumors that would improve the long-term outcomes in the future;[33] they asserted that NSS would play an important role in the individualized and optimized risk-adapted therapy of children of uWT by avoiding the long-term consequences of a reduction in the renal parenchyma. Szymik-Kantorowicz et al.[22] had concluded in 2012 that RN is an overly aggressive treatment modality in children with Stage I WT and had proposed the employment of NSS for uWT up to 4 cm diameter and simple nephrectomy for larger Stage I uWT.

In the past one decade, some researches from USA that follows the philosophy of upfront surgery (COG protocol) did some post hoc feasibility analyses to determine the percentage of cases that could have been amenable to NSS. Cost et al.[34] addressed the issue in a review of pathologic specimens from 78 nonpretreated RN performed for uWT. The ideal surgical candidate for NSS was defined as demonstrating all of the following characteristics on pathologic review: (1) unifocal mass located outside of the renal hilum and sparing a third or more of normal kidney; (2) favorable histology; (3) absent renal sinus or segmental vascular tumor invasion; (4) absence of lymph node metastasis, intraoperative tumor spill, or gross regional disease at surgery; and (5) a distinct interface between tumor and renal parenchyma. They realized that about one-fourth patients met all of the strict criteria and would have been considered ideal surgical candidates for NSS. Ferrer et al.[35] reviewed imaging studies of 60 patients with a mean age of <2 years with very low-risk uWT (mean weight <550 g) to assess the feasibility of PN. They evaluated percentage of salvageable parenchyma, tumor location, and anatomical features preventing a NSS. They found a linear relationship exists between tumor weight and computerized tomography estimated tumor volume. They concluded that NSS was deemed feasible in only 8% of nonpretreated patients.

The low number of kidney-conserving interventions above can to a certain extent be explained by the lack of guidelines for NSS previously. Umbrella protocol of SIOP-Renal Tumor Study Group (SIOP-RTSG) recently suggested that ideal candidates for NSS include those with small tumor volume (<300 ml), negative regional lymph nodes and those who would have substantial remnant kidney function.[36] A new classification system for NSS was also suggested in the Umbrella protocol to optimize the comparison of patient outcomes [Table 2].[37] Umbrella protocol differentiates the two popular techniques of NSS into NSS A (PN) and NSS B (enucleation) [Figure 1][38] and suggests to go for NSS A. It was further emphasized that minimally invasive or laparoscopic surgery should not be done in patients in whom NSS can be safely performed.[36] As such, there are very few examples of NSS in uWT performed laparoscopically.[39],[40]
Table 2: Nephron-sparing surgery (NSS)*

Click here to view
Figure 1: Different types of nephron-sparing surgery (NSS). (a) Partial nephrectomy: NSS A. (b) Enucleation (tumorectomy): NSS B (Reproduced from Mrad et al. 2020[38] with permission from Wiley)

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The systematic review of all reported patients of nonsyndromic uWT with normal contralateral kidney globally [Table 1] clearly demonstrates that upfront ChT approach purported by SIOP is far better way to go for NSS for uWT. Mean reduction in volume of tumor after neoadjuvant ChT was 38% (Sarin; unpublished data) to 79% in series by Linni et al.[17] Even a tumor as big as 1346 ml was pretreated with ChT and was amenable to NSS when it shrank to 594 ml.[17] Even the author had a patient with pretreated tumor volume of 378 ml in his series of patients of uWT undergoing NSS.

As of date, some excellent systematic reviews[40],[41] and meta-analysis[42] on the topic of NSS in uWT are available. The first and only (RCT) study hitherto on the topic has been recently reported by a team of urologists from Belgaum, Karnataka, India.[29]

Romao and Lorenzo[40] reviewed the existing literature pertaining to renal function in these patients. Incidence rates, causes, and methods to mitigate renal dysfunction are presented in 3 distinct clinical situations: sporadic uWT, syndromic uWT, and BWT. They emphasized that renal function in pediatric cancer survivors must be carefully ascertained prospectively using methods that allow diagnosis of mild cases, rather than focus solely on extreme cases represented by the development of end-stage renal disease (ESRD).

Low incidence of ESRD that is often quoted as one of the reasons why paradigm shift from RN to NSS should not be considered for nonsyndromic uWT is the most dramatic, final stage of chronic kidney disease (CKD) and represents just the tip of the iceberg. There could be a significant number of patients who underwent nephrectomy and had further exposure to other nephrotoxic treatments for WT in childhood growing up with under-recognized CKD. Direct toxicity from ChT and XRT radiation as well as direct nephron ablation from surgical treatment (nephrectomy) renders the kidney susceptible to a multitude of problems over time in patients with WT.[40]

Romao and Lorenzo[40] stressed on the individualized treatment of children with nonsyndromic uWT keeping molecular stratification for disease aggressiveness as well as multifocality and renal dysfunction in mind [Figure 2].[40] They emphasized a maintaining balance between survival with preservation of renal function and mentioned that the role and potential benefits of NSS deserve careful exploration under well-designed protocols.
Figure 2: Individualized care of unilateral Wilms' tumor (WT) based on molecular stratification based on biomarkers that could influence WT treatment (Reproduced from Romao et al. 2015;[40] reproduced with permission from Elsevier)

Click here to view


An excellent recent systematic review available in French states that NSS for uWT seems to be a credible therapeutic alternative.[41] The authors emphasize on new technologies such as 3D reconstruction that could help surgeons define the best parameters to select ideal tumors for this surgery in the near future. They believed that small tumors (<4 cm), distant from the renal hilum (ideally on the upper pole) that respect at least 50% of the renal parenchyma (ideally superficial with exophytic development), seem to be the perfect indication for NSS.

Chen et al.[42] in a recent meta-analysis recommended the use of NSS for uWT. The procedure accounted for higher survivability and postoperative renal function and lesser incidence of relapse as compared to RN.

Nerli et al.[29] in a recent RCT concluded that the oncological outcome of NSS was as good as RN in children with uWTs. NSS also minimized the loss of renal function. The children who underwent RN presented with considerably higher mean systolic and diastolic blood pressures, as well as significantly elevated mean values of serum creatinine compared to their NSS counterparts. The feasibility criteria were based on post-ChT CT as follows: (a) ≥50% reduction in the size of the tumor; (b) feasibility to excise the tumor by clamping the main renal vessels; and (c) after resection, the residual renal parenchyma should be a minimum of 20% of the original volume.

It is importance to note that over the last two decades, the criterion for size of the renal remnant has shifted from being two-third of the kidney[12] to even as low as 20% of the kidney.[29] Historically, it was believed that at least 50% of renal tissue should be spared after the tumor resection with a margin of healthy tissue, to give any worthwhile protection against hyperperfusion.[44]

Next is the issue of paradigm shift about positive surgical margins (PSMs) after NSS. Although complete tumor removal is an oncologic principle of paramount importance, accumulating data suggest that completion nephrectomy might not be the treatment of choice in all patients with PSMs after NSS. PSMs are present in 0%–7% of patients after open NSS, in 0.7%–4% after laparoscopic NSS, and in 3.9%–5.7% after robot-assisted NSS. As indicated by intermediate follow-up data, the majority of patients with PSMs after PN remain without disease recurrence, and a surveillance strategy seems preferable to surgical reintervention.[45]

The operative steps of NSS in WT are beyond the purview of this article. These are beautifully illustrated elsewhere.[27],[46],[47],[48],[49],[50],[51],[52]

Warmann and Fuchs[52] have highlighted the use of magnetic resonance imaging (MRI) in NSS. MRI can better visualize the soft tissue boundary between kidney tissue and tumor. Furthermore, it can provide information on the histological background of different tumor areas based on the different weightings and diffusion analyses. However, general anesthesia is usually necessary to perform a high-quality MRI in the infants and younger children. Even if MRI is performed, a CECT scan cannot be written off as it displays the vascular situation far better. They have also highlighted the use of Uro-MRI and scintigraphy for the patients undergoing NSS so as to know the split renal function. They also emphasized on doing an intraoperative contrast-enhanced sonography to verify the findings of the preoperative imaging and to determine the procedure for tumor resection. The same group of authors had earlier described longitudinal PN for central tumors involving the renal hilum.[53] When the renal pelvis is involved and has to be resected, care must be taken to leave a sufficient margin of renal pelvis tissue on the kidney side for subsequent reconstruction of the collecting system. The author (Sarin) has routinely used preoperative and postoperative DMSA scans for all patients undergoing NSS, and none of the patients had any adverse oncological result on 2-year follow-up. He had also resected part of the pelvis along with the botryoid WT and closed the pelvis over a double-J stent in one of the patients.


   Conclusions Top


This qualitative systematic review recommends the use of NSS for nonsyndromic uWT. The procedure accounts for higher postoperative renal function and lesser incidence of hypertension as compared to the radical nephrectomy. Overall and event-free survivals are comparable or even better with NSS.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

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    Tables

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  2005 - Journal of Indian Association of Pediatric Surgeons | Published by Wolters Kluwer - Medknow 

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