The Yield of Lymph Node Sampling Versus Comprehensive Lymph Node Dissection in Wilms Tumor

doi:10.21203/rs.3.rs-3937961/v1

Background: Nephroblastoma, commonly known as Wilms' tumor (WT), is the most prevalent primary kidney tumor in children aged 1 and peaks between the ages of 3 and 4. Since lymph node involvement in WT is linked to a less favorable prognosis, a thorough nodal examination should be performed.

Aim: To evaluate the outcome of hilar lymph node sampling versus comprehensive lymph node dissection regarding the pathological yield of the lymph node (LN) involvement post-nephrectomy in WT patients.

Patients and Methods: This prospective study involved 20 pediatric patients with WT who underwent nephrectomy with LN sampling (10) versus comprehensive LN dissection (10) in the same surgical setting. Internal Review Board (IRB) preapproval was obtained. All patients had their parents/guardians’ consent before participation.

Results: In our study, the comparison between LN dissection and hilar LN sampling showed a statistically significant increase in the number of excised LNs in dissection versus the number of excised LNs in sampling. However, there was no statistically significant difference regarding the yield of excised LNs. The majority of patients had no complications, whereas three patients had a diaphragmatic injury dissecting the adherent tumor, and only one patient had chylous ascites.

Conclusion: Our preliminary study shows that hilar LN sampling may be preferred over LN dissection in WT surgical management since it is a less intrusive approach that yields the same pathological LN yield.

Wilms tumor

Lymph node dissection

Sampling

Dissection

Wilms’ tumor (WT) is the commonest malignant renal neoplasm in children, and it is also considered the third most frequently encountered malignancy in the pediatric age group.^{(1, 2)} The management of WT is a true story of success regarding multimodal treatment in children’s oncology. Recent reports indicate that about 90% of the patients suffering from this tumor can be cured.^{(1, 3)}

The importance of pathological lymph node (LN) involvement in stratifying WT cannot be overstated, as it affects staging and thus adjuvant therapy as nodal involvement in WT correlates with suboptimal outcomes. However, concerns exist about the accuracy of LN sampling as currently practiced.^{(4, 5)}

Lack of standardized technique for representative nodal samples in surgical settings represents the most frequent surgical protocol deviation in WT,⁽⁶⁾ and has been observed in numerous studies to impact survival, likely through under-staging and inadequate administration of stage-directed adjuvant therapy.^{(7, 8)}

Factors that result in local stage III designation (LN involvement, tumor spillage, preoperative biopsy, and local residual disease) have all been independently associated with worse survival, and thus, such patients are managed with additional adjuvant therapies (radiation and doxorubicin).⁽⁹⁾ While excellent survival can still be achieved, there are reported toxicities associated with intensified therapy.⁽¹⁰⁾

Not all stage III patients experience the same outcome. LN positivity is associated with lower event-free survival than the other factors.^{(9, 11)} This emphasizes the importance of adequate LN sampling to accurately characterize LN involvement. This study aims to evaluate the outcome of hilar LNs sampling in comparison to comprehensive LNs dissection with regards to the pathological yield of the LNs post nephrectomy in patients with WT with a correlation to post-operative comorbidities for both techniques.

This was a prospective study that included 20 consecutive pediatric patients diagnosed with Wilms’ tumor who underwent nephrectomy followed by either lymph node sampling or lymph node dissection in the same surgical setting (being alternatively randomly allocated to avoid selection bias) at the Pediatric Oncology Center, Borg El-Arab University Hospital, Alexandria University, Egypt from 1/1/2020 to 31/12/2020. Internal Review Board (IRB) approval was obtained from Alexandria University Medical Ethical Research Committee (Approval no. 0106729). All patients’ parents/guardians have consented before participation in this study according to the World Medical Association Declaration of Helsinki – Ethical Principles for Medical Research Involving Human Subjects. No special funding was raised for this study.

The study included children who presented with WT. A thorough history including personal, present, medical, surgical, and family history was obtained from all parents/legal guardians. Presenting symptoms and general as well as thorough abdominal examination were conducted for all patients. Further routine and specific laboratory investigations, radiological imaging, and pathological examination (macroscopically or microscopically) were performed for tumor staging according to the Society of Paediatric Oncology (SIOP) 2001 guidelines.⁽¹²⁾

All patients received chemotherapy before surgery.⁽¹²⁾ After induction of general anesthesia, conventional standard open radical nephrectomy (excision of the affected kidney within Gerota’s fascia along with hilar lymph nodes as one specimen) was performed and sent as a separate specimen and labeled as “sampling lymphadenectomy”. The rest of the specimen was sent to the pathologist to assess LNs in the rest of the specimen outside Gerota’s fascia which in this case was labeled “completion lymphadenectomy”. All operative data and postoperative complications were recorded. Finally, postoperative chemotherapy +/- radiotherapy was scheduled as per SIOP protocol (Fig. 1).

Data management and statistical analysis: Data were fed to the SPSS window and analyzed using IBM SPSS software package version 20.0. (Armonk, NY: IBM Corp). Qualitative data were described using numbers and percentages. The Shapiro-Wilk test was used to verify the normality of distribution Quantitative data were described using range (minimum and maximum), mean, standard deviation, median, and interquartile range (IQR). The significance of the obtained results was judged at the 5% level. We used the Student t-test for normally distributed quantitative variables, Mann Whiney and Wilcoxon signed rank tests for abnormally distributed quantitative variables. Also, Kaplan-Meier and Cox regression were used to verify any correlation between progression-free survival and overall survival.

The average age of all patients ranged from 1 year to 7.3 years with mean ± SD (3.4 ± 2.2) years at the time of surgery. There were 13 females (65%). Only one patient (5%) showed a family history of WT. The most common clinical presentations were abdominal mass in 65% (13 patients) and abdominal pain in 20% (4 patients). In 20% (4 patients) preoperative renal mass biopsy was performed. Right-sided renal mass was more prevalent than the left-side renal mass (60% vs. 40%) as a presentation. Half of the patients showed intermediate risk while 25% of patients showed high risk and 25% showed low risk in most of the cases. LN distribution was as follows; 45% para-aortic lymph nodes on the left-sided tumor and 25% pericaval lymph nodes on the right-sided tumor. No metastases were reported in 90% while only 10% (2 patients) had pulmonary metastatic nodules (Table 1).

As regards tumor volume pre and post-chemotherapy, there was a statistically significant decrease in post-chemotherapy tumor volume with mean ± SD (453.25 ± 669.32) cm³ versus (1021.6 ± 898.86) cm³ for pre-chemotherapy tumor volume at (p = 0.0002). The comparison between dissection and sampling showed a statistically significant increase in the number of excised lymph nodes in dissection with mean ± SD (7.6 ± 2.7) lymph nodes versus (3.85 ± 1.18) lymph nodes for sampling at (p <0.0001). However, there was no statistically significant difference between dissection and sampling according to the yield of excised lymph nodes with mean ± SD (0.5 ± 1.61) and (0.2 ± 0.52) respectively at (p=0.948) (Table 2).

The majority of patients had no complications, whereas three patients (15%) had a diaphragmatic injury dissecting the adherent tumor, and only one patient (5%) had chylous ascites that resolved spontaneously. The survival rate was 95% when 19 patients were cured while one patient died. The median time needed for patients to be cured of Wilms tumor was 228 days (7.6 months) while there was only one dead patient after 300 days from the start of the treatment. Out of the 20 patients enrolled in our study, there was only one patient showed progression. The estimated time for progression was 100 days after the end of the treatment (Table 3).

Univariate and Multivariate Cox regression was carried out for progression-free survival (Table 4). There was a statistically significant difference in the right side at (p=0.029) and a smaller risk at (HR=0.29, 95% CI=0.09-0.88) as univariate analysis. While there was a statistically significant difference in the right side with a smaller risk at (HR=0, p<0.001), pre-chemotherapy tumor size with lack of association at (HR=0.95, p<0.001), post-chemotherapy tumor size with lack of association at (HR= 0.99, p<0.001), not invaded capsule with a smaller risk at (HR=0, p<0.001), excised Lymph nodes in dissection with a smaller risk at (HR=0, p<0.001) and excised Lymph nodes in sampling with a smaller risk at (HR=0, p<0.001).

Lymph node involvement in WT is a proxy for advanced-stage disease whether it is regional (stage III) or non-regional (stage IV) nodal metastases. Spread to lymph nodes significantly worsens the prognosis in patients with WT. If hilar LNs alone are involved, the relapse-free survival (RFS) drops from 91.1–56.7%. If both hilar and periaortic LNs are found to harbor tumor deposits, only 33.3% of these patients remain free of tumors.⁽⁴⁾ The involved LNs among our patients (80%) were para-aortic, pericaval, or hilar LNs while no LNs were detected in 20% of patients.

In our study, there were no major reported complications but for 3 patients (15%) who were reported to suffer from a diaphragmatic injury due to the attached tumor which was managed intraoperatively by direct closure of the defect and insertion of chest tube, and only 1 patient (5%) developed chylous ascites that resolved spontaneously.

Similarly, the National Wilms' Tumor Study review (NWTS-4) identified a single case of chylous ascites in 534 randomly sampled patients (0.2%). This is lower than rates of splenic, diaphragmatic, or pancreatic injury.⁽¹³⁾ There is also a single institution report of 9 cases of chylous ascites in 80 resections for WT (3.75%).⁽¹⁴⁾

Because intraoperative gross assessment of LNs is not reliable for determining tumor involvement, LN sampling for histologic evaluation is required.⁽⁸⁾ Most of our patients were diagnosed as stage one, followed by stage three and stage two representing 60%, 30%, and 10% respectively. Half of the patients showed intermediate risk while the high-risk and low-risk patients were equally distributed (25% for each).

It is well-reported that LN yield is generally higher in patients with LN-positive disease, possibly owing to surgeon bias during the nephrectomy.^{(4, 8)} In contrast, prior work also demonstrates that surgeons are not reliably able to predict whether LNs are grossly involved.⁽⁸⁾ Surgical factors affecting LN yield are important to highlight, as these are modifiable. To determine what drives LN yield, human decision-making should be minimized, and this likely requires a minimal LN yield goal. It could be argued that removing as many LNs as possible is a strategy to accurately determine LN involvement.⁽⁵⁾

In the current study, the comparison between dissection and hilar LNs sampling showed a statistically significant increase in the number of excised LNs in dissection with a median (IQR) 7.0 (6.0–9.0) LNs versus 4.0 (3.0–5.0) LNs for sampling at (p < 0.0001), while there was no statistically significant difference between dissection and hilar LNs sampling according to the yield of excised LNs (p = 0.948). Our results indicate that hilar LNs sampling may be preferred over dissection, as although they give the same operative results, the dissection harbors many technical difficulties and a higher risk of complications compared to sampling.

To avoid the influences of surgeon bias, we suggest that accurate staging of patients with unilateral WT does not require sampling of a large number of LNs and we chose hilar LNs for sampling. One possibility is that lymphatic spread from a WT progresses in an anatomically orderly manner in which hilar lymph may be involved first. This LN is adherent to the resected tumor specimen itself and near the renal vessels and thus more often removed during the surgical procedure. In our study, 18 patients had negative LNs when hilar LN was sampled and there was no positive LN in further LN dissection. Accordingly, the removal of additional LNs, then, might not improve the detection of occult metastases or influence outcomes.

Along the same line, prior studies have suggested that extensive retroperitoneal LN dissection does not improve patient outcomes as compared with LN sampling and can be associated with significant procedure-related morbidity. Weiser et al.⁽¹⁴⁾ concluded that extensive LN dissection in WT patients, particularly above the level of the renal hilum, appears to be associated with the development of postoperative chylous ascites. Elimination of formal lymphadenectomy along with meticulous ligation of lymphatics should decrease the incidence of this complication.⁽¹⁵⁾

Godzinski et al.⁽¹⁶⁾ in a small study, conducted by the International Society of Pediatric Oncology (SIOP) Nephroblastoma Trial and Study Committee, demonstrated that the likelihood of LN positivity did not increase when more than 3 nodes were sampled. In comparison, Kieran et al.⁽⁸⁾ found that the percentage of patients with positive LNs increased as the number of LNs sampled increased, with a plateau in the LN positivity rate at about 28% at 7 or more LNs sampled. Both studies concluded that extensive LN sampling appeared to confer no clinical benefit. The precise number of LNs needed to ensure accurate characterization of nodal status differed between both studies because of the different number of patients in each study and different treatment protocols.

On the contrary, Kieran et al.⁽⁸⁾ observed that LN yield in stage I and II WT did not predict event-free survival (EFS). Also, Saltzman et al.⁽⁴⁾ extended this finding into the LN-positive FH patients, where LN yield alone was not associated with OS. Yet, in the entire cohort, the median LN yield was higher in those with LN-positive disease (five versus three, P < 0.001) which was due to surgeon bias at the time of nephrectomy as the surgeons were not reliably or accurately able to predict whether LNs are grossly involved.

In the current study, the estimated 6-months overall survival (OS) and event-free survival (OS 95%, EFS 95%) showed that the median time of patients to be cured and showed no progression of WT was 228 days (7.6 months) as (19/20) patients were cured without progression while only one patient (1/20) patient started WT progression after 100 days and died after 300 days from the start of the treatment.

The survival rates were reported above 90% in developed countries.^{(17, 18)} In this study, such data was better than declared in a previous national series by Naguib et al.⁽¹⁹⁾ [OS 95% vs 78.9%], and Elgendy et al. ⁽²⁰⁾ reported that 30-month OS and EFS for all patients were 84.3% and 81.1%, respectively. This can be explained by the small sample size and only two patients who had stage IV tumors in the present study.

Also, our results regarding OS and EFS were higher than those reported from other developing countries in North Africa and Asia [OS 74–89%, EFS 73–86%].^(21–24) Impressive outcomes were achieved by a study in Latin America with OS and EFS of 91% and 85%, respectively.⁽²⁵⁾ While dismal survival rates were observed in sub-Saharan Africa of 25–46%.⁽²⁶⁾

In the current study, to potentially recognize prognosis prediction, we made univariate and multivariate logistic regression analyses for different parameters affecting progression-free survival. The multivariate logistic regression analysis revealed that right side tumor, pre and post-operative tumor size, capsular invasion, surgical complication, and the number of excised LN in dissection and sampling are independent factors associated with progression-free survival.

As regards lymph node sampling, patients who had no LNs sampled had worse EFS than those with positive LNs during the NWTS-4.⁽²⁷⁾ As omission of lymph node sampling likely results in understaging and subsequent undertreatment of patients with occult positive LNs.⁽²⁸⁾. Kieran et al.⁽⁸⁾ reported that the chance of finding a positive LN was higher when at least seven LNs were sampled, and hence, the UMBRELLA protocol now advises sampling at least seven lymph nodes.⁽²⁹⁾

Up to date, there is a lack of standardized guidelines for what constitutes LN sampling in particular regarding the extent and location. Thus, LN yield can vary widely, making any conclusions involving LN yield limited. We suggest in the current study, that accurate staging of patients with unilateral WT can be achieved via hilar LNs sampling instead of radical dissection.

Overall, irrespective of whether increased LN counts affect the quality of stage assignment, regional disease control, or both, proper prediction of postoperative stage-specific survival and decisions for adjuvant therapy are significantly influenced by the number of LN examined during pathologic evaluation. Failure to biopsy LNs during surgical resection of WT not only increases the risk of local recurrence due to understaging and inadequate adjuvant therapy but is also an independent prognostic indicator of lower survival

Limitations

The limitations of this study are inherent to its small sample size and short duration. A large-scale prospective study is needed to determine if submitting hilar LN sampling will positively have an impact on tumor staging, treatment, or overall survival for WT.

Considering the aforementioned limitations, our preliminary limited hilar lymph node sampling may be preferable over comprehensive lymph node dissection in the surgical management of Wilms tumor being less invasive with similar pathological lymph node yield as lymph node dissection.

Human Ethics Approval Declarations:

This study was performed according to the Declaration of Helsinki (attached). Ethical approval was obtained from the Ethics Committee of the Faculty of Medicine, Alexandria University (Approval no. 0106729).

Consent to Participate declaration:

Written informed consent was obtained from each patient’s parent/legal guardian before participation in this study.

Availability of Data and Materials:

Data Availability Statement (DAS): Raw patient data have been hidden to protect patient privacy. Still, they are available in the Electronic Medical Record filing system in the Pediatric Oncology Center, Borg El-Arab University Hospital, Alexandria University, Alexandria, Egypt, and are available upon request from the corresponding authors.

Funding Declaration:

Open access funding was provided by the Science, Technology & Innovation Funding Authority (STDF) in cooperation with the Egyptian Knowledge Bank (EKB). No other special funding for this study.

Competing Interest Declaration:

No competing interests for all authors involved in this study.

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Table 1: Distribution of the studied cases according to history and tumor characteristics

Total Participants		20 (100%)
Age:
Min.- Max.		1.0 – 7.3 years
Mean ± SD		3.4 ± 2.2
Median (IQR)		2.75 (1.58 – 5.13)
		n (%)
Sex:	Female	13 (65.0%)
Sex:	Male	7 (35.0%)
Family History:	Negative
Family History:	Positive
Cosenguinty:	Negative	14 (70.0%)
Cosenguinty:	Positive	6 (30.0%)
Tumor distribution Side:	Left	8 (40.0%)
Tumor distribution Side:	Right	12 (60.0%)
Clinical Presentation	Abdominal mass	13 (65.0%)
	Abdominal pain	4 (20.0%)
	Abdominal mass & HTN	1 (5.0%)
	Hematuria	1 (5.0%)
	Hematuria & abdominal mass	1 (5.0%)
Stage:	One	12
	Three	6
	Two	2
Risk:	High	5 (25.0%)
	Intermediate	10 (50.0%)
	Low	5 (25.0%)
Lymph Node Site:	Para-aortic LN(on the left-sided tumor)	9
	Pericaval LN(on the right-sided tumor)=	5
	Hilar & periaortic LN	1
	Hilar & pericaval LN	1
	No LN

Table (2): Comparison between tumor volume pre-chemotherapy and post-chemotherapy and comparison between retroperitoneal LN dissection and LN sampling yield

Tumor Size:
	Pre-Chemotherapy		Post-Chemotherapy		Wilcox Paired test
Min. – Max.	18 – 4104 cm³		3.0 – 2992.0 cm³		P= 0.0002*
Mean ± SD	1021.6 ± 898.86		453.25 ± 669.32
Median (IQR)	855.0 (496.1 – 1288.4)		210.0 (86.25 – 570.0)
The number of the Lymph Nodes collected:
		Dissection	Sampling	Student T-test
Min. – Max.		4 – 15 LN	2.0 – 6.0 LN	P <0.0001*
Mean ± SD		7.6 ± 2.7	3.85 ± 1.18
Median (IQR)		7.0 (6.0 – 9.0)	4.0 (3.0 – 5.0)
Yield Lymph Nodes:
Min. – Max.		0 – 7	0 – 2	Mann-whitney test
Mean ± SD		0.5 ± 1.61	0.2 ± 0.52	P = 0.948

Table 3: Survival analysis between Survival probability and survival time and between Progression-free survival probability and progression time

Overall Survival:
Number of all cases	Number of cases (survived)	Number of cases censor (died)	Median time		95% CI		P-value
20 (100%)	19 (95%)	1 (5%)	228 days		(70-273)		NA
Prognosis Free survival:
Number of all cases	Number of events (Not progressed)	Number of cu censor (Progressed)		Median time		95% CI	P-value
20 (100%)	19 (95%)	1 (5%)		228 days		(70-273)	NA

Table 4 is available in the Supplementary Files section.

No competing interests reported.

The Yield of Lymph Node Sampling Versus Comprehensive Lymph Node Dissection in Wilms Tumor

Status:

Version 1

Abstract

Figures

Introduction

Patients and Methods

Results

Discussion

Conclusion

Declarations

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1