Journal of Pediatric Surgery 49 (2014) 15441548

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Journal of Pediatric Surgery

journal homepage: www.elsevier.com/locate/jpedsurg

Minimally invasive nephrectomy for Wilms tumors in children data

from SIOP 2001
Steven W. Warmann a,, 1, Jan Godzinski b, 1, Harm van Tinteren c, Hugo Heij d, Mark Powis e,
Bengt Sandstedt f, Norbert Graf g, Jrg Fuchs a The Surgical Panel of the SIOP Renal Tumor Strategy Group
a
Department of Pediatric Surgery and Pediatric Urology, University Children's Hospital Tuebingen, Germany
b
Department of Pediatric Surgery, Marciniak Hospital, Wroclaw and Chair of Emergency Medicine, Medical University, Wroclaw, Poland
c
Comprehensive Cancer Centre, Amsterdam, The Netherlands
d
Pediatric Surgical Center of Amsterdam (ECH-AMC/VUmc), Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
e
Department of Paediatric Surgery, Leeds Teaching Hospitals NHS Trust, Leeds, United Kingdom
f
Childhood Cancer Research Unit, Astrid Lindgren's Children's Hospital, Karolinska Institutet, Stockholm, Sweden
g
Department of Pediatric Hematology and Oncology, University Hospital Homburg/Saar, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Purpose: To analyse the surgical and oncological outcome of minimally invasive surgery (MIS) for tumor
Received 18 February 2014 nephrectomy in Wilms tumor (WT) patients.
Received in revised form 4 June 2014 Methods: WT patients from the SIOP 2001 trial, undergoing MIS for tumor nephrectomy were analyzed with
Accepted 5 June 2014 regard to demographic characterization, surgical specications, complications, and outcome.
Results: There were 24 children matching the inclusion criteria. Median age at operation was 40.35 months
Key words:
(14.365.4). All patients received preoperative chemotherapy. Median tumor volume was 177.5 ml at
Nephroblastoma
Laparoscopy
diagnosis (46.5958) and 73.0 ml at surgery (3.8776). There was one surgical complication (splenic injury),
Tumor resection no intraoperative tumor rupture occurred. Abdominal stage was I in 14, II in 7, and III in 3 patients. Adequate
lymph node sampling was performed in only 2 patients. One local relapse occurred. Event-free survival was
23/24, overall survival was 24/24, median follow up was 47 months (2114).
Conclusions: We present the largest series so far of minimally invasive nephrectomies for nephroblastoma
based on a multinational trial. Treatment results were comparable to those of open surgery; however,
experience of operating surgeons was generally high. Discipline of lymph node sampling was inadequate.
Based on this analysis a prospective study on MIS in nephroblastoma is planned by the SIOP Renal Tumor
Study Group.
2014 Elsevier Inc. All rights reserved.

Surgery plays a key role as local treatment for nephroblastoma. The
guidelines for resection of Wilms tumors (WT) have been well
established and have by now been thoroughly analyzed [14]. From
the surgical point of view, complete tumor resection is one of the main
prognostic factors in the treatment of WT [3,4]. For many years, open
nephrectomy was the common surgical approach in unilateral cases.
However, alternative surgical concepts have been introduced during
recent years and are meanwhile used to a relevant extent. Minimally
invasive surgical (MIS) procedures are regularly used in pediatric
surgery for standard as well as complex operations [5,6]. This approach
is especially relevant in pediatric urologic operations of the upper
urinary tract [7,8]. MIS also plays a certain role in pediatric surgical
oncology although the exact relevance in most entities has not yet been
determined [911]. The use of MIS in patients suffering from WT has
been reported in singular cases [1214], however, a systematic analysis
has not been undertaken so far and by now there are no evidence based
data available. This is of importance since the minimally invasive
approach seems to be increasingly used. Current treatment protocols do
not contain surgical guidelines or recommendations concerning
indications and contraindications for MIS in WT. In this study we
systematically assessed for the rst time the role of MIS in the treatment
of Wilms tumors based on a multicenter prospective data registration.
The outcome parameters were technical/surgical aspects (including
tumor rupture, lymph node sampling, and complications), as well as
oncological measures (event-free survival and overall survival).
1. Materials and methods

Corresponding author at: Dpt. of Pediatric Surgery and Pediatric Urology, University 1.1. Patients
Children's Hospital Hoppe-Seyler-Str. 3, 72076 Tuebingen, Germany. Tel.: +49 7071
2986 621; fax: +49 7071 294 046.
E-mail address: steven.warmann@med.uni-tuebingen.de (S.W. Warmann). Patients with newly diagnosed nephroblastoma were registered in
1
SW Warmann and J Godzinski share equal rst authorship. the multicenter trial SIOP 2001 by participating institutions. We

http://dx.doi.org/10.1016/j.jpedsurg.2014.06.005
0022-3468/ 2014 Elsevier Inc. All rights reserved.
 S.W. Warmann et al. / Journal of Pediatric Surgery 49 (2014) 15441548 1545

retrospectively analyzed all children suffering from unilateral WT
who underwent laparoscopic tumor resection between June 2001 and
July 2013. Data were obtained from the central SIOP 2001 data base in
Amsterdam/The Netherlands. Patients' characteristics, surgical data as
well as clinical and oncological outcome measures were assessed. The
multi-institutional study was approved by the Institutional Review
Board of the rztekammer des Saarlandes, Germany (No. 136/01).
1.2. Treatment
All patients registered within the above cited time frame were to
be treated following the SIOP 2001 protocol guidelines. According to
this protocol, patients older than 6 months should receive neoadju-
vant chemotherapy depending on the tumor stratication:
Actinomyin D/Vincristin (AV) over 4 weeks in localized cases,
Actinomycin D/Vincristin/Doxorubicin (AVD) over 6 weeks in
metastasized cases. The recommended doses were: Actinomycin D
45 g/kg once every 2nd week, Vincristin 1.5 mg/m 2 once every
week, Doxorubicin 50 mg/m 2 every 4 weeks. Doses should be
reduced to 2/3 in cases of body weight below 12 kg (and further to
1/2 if poorly tolerated). Tumor response to initial chemotherapy was
dened comparing volume at diagnosis and volume at surgery.
Primary tumor response was assigned as complete response (CR:
complete disappearance of the tumor), partial response (PR: volume
regression more than 50%), stable disease (SD: volume regression
between 0 and 50%), and progressive disease (PD: volume increase
under chemotherapy).
Neoadjuvant chemotherapy was to be followed by resection of the
primary tumor as local treatment [3,15]. According to the protocol,
laparoscopy was not banned as approach for tumor nephrectomy. The
postoperative treatment strategy (chemotherapy radiotherapy
and treatment of possible metastases) depended on the postoperative
staging and the histological risk stratication [16,17].
2. Results
2.1. Population demographics (Table 1)

The total number of registered patients within SIOP 2001 during

the study period of this analysis was 4763, 4220 of the patients had
nephroblastoma. Overall there were 24 children undergoing MIS for
Wilms Tumor resection during the study period, 16 female and 8 male
patients. Of all patients, 11 were enrolled from the Children's Cancer
and Leukaemia Group (CCLG) in the UK, 7 from the Society of Pediatric
Oncology and Hematology (GPOH) in Germany, 5 from the French
Society against cancers in children and adolescents (SFCE) in France,
and 1 from the Brazilian Wilms Tumor Study Group(GCBTTW) in
Brazil. Median age of patients at diagnosis was 39.35 months (range
11.963.9). Tumor localization was on the right side in 14 patients and
on the left side in 10 patients. The median tumor volume at diagnosis
was 177.5 ml (range 46.5958). Localized tumors were present in 22
children, metastatic tumors in 2 (lung metastases in 1 patient and
abdominal metastases in 1 patient, Table 1).

Table 1
Patients demographic data. Gender: F = female, M = male; Side: L = left, R = right;
Neoadjuvant chemotherapy: AV = 4 weeks Actinomycin D + Vincristin; AVD = 6 weeks
Actionomycin D + Vincristin + Doxorubicin. n.d. = no data.

Pat. Gender Age at Side Neoadjuvant Tumor volume [ml]

No. diagnosis [M] chemotherapy
Initially At surgery

1 F 51.6 L AV 251.7 65.9

2 F 63.9 L AV 177.1 n.d.
3 F 39.7 R AV 177.8 94.1
4 M 33.2 L AVD 582.2 71.9
5 F 34.2 R AVD 154.3 12.8
6 F 51.8 L AV 52.8 4.2
7 F 32.9 R AV 46.5 12.9
8 M 36.4 R AV 69.3 6.6
9 F 41.2 R AV 50.3 6.4
10 M 44.5 R AV 593.0 88.0
11 F 44.1 L AV 93.0 23.0
12 M 42.3 L AV 317.0 110.9
Fig. 1. Clinical example: minimally invasive tumor nephrectomy for nephroblastoma in
13 M 60.9 R AVD 883.0 254.0
a boy. Right-sided Wilms' tumor, which was treated with neoadjuvant chemotherapy
14 F 11.9 R n.d. 346.3 n.d.
(actinomycin D + Vincristin) for 4 weeks. The tumor showed good response to
15 M 46.5 L AVD 958.0 3.8
treatment. Because of inltration of the renal pelvis, the decision for tumor
16 M 22.4 R AV 69.3 92.2
nephrectomy was taken. Patient's age at surgery was 23.5 months. A) MRI scan of
17 M 44.9 L AV 789.0 776.0
tumor at diagnosis showing a lower pole renal mass inltrating the renal pelvis (size
18 F 13.3 R AV 734.0 102.6
9.5 9.5 8.3 cm, sagittal view). B) MRI scan after neoadjuvant chemotherapy
19 F 24.1 R AV 370.0 158.0
showing tumor regression (size 3.9 3.4 3.0 cm, sagittal view). C) Patient after
20 F 14.0 L AV 171.0 207.0
surgery (4 ports plus Pfannenstiel incision for removal of the bag with the resected
21 F 39.0 R AV 170.0 58.0
specimen). D) Resected specimen. Histological workup revealed an intermediate risk
22 F 23.0 L AV 170.0 77.0
nephroblastoma (regressive subtype with less than 10% vital compounds), resection
23 F 56.0 R AV 162.0 74.0
status R0, lymph nodes were negative. Patient is without evidence for disease after
24 F 21.0 R AV 300.0 15.0
2 years follow-up.
1546 S.W. Warmann et al. / Journal of Pediatric Surgery 49 (2014) 15441548

2.2. Chemotherapy/radiotherapy Pathologically, there were positive margins in the 2 cases, in which
the operating surgeon also had regarded the capsule as not being
Before operation, all children received neoadjuvant chemotherapy intact. Additionally, there were pathologically positive margins in one
(19 AV, 4 AVD, no data for 1 patient). The median tumor volume case, in which the surgeon had regarded the capsule as intact. Local
regressed under chemotherapy from initially 177.5 ml (range 46.5 tumor stage according to SIOP was I in 14, II in 7, and III in 3 instances.
883) to 73.0 ml (3.8776, Table 1). Taken together there was partial Reasons for stage III were positive margins in all three cases, in one of
response to chemotherapy in 18 tumors, stable disease in 2 tumors, them there were also positive lymph nodes and in another one there
and progressive disease in 2 tumors (no data for 1 patient). All was preoperative tumor rupture additionally.
children except one received postoperative chemotherapy (12 AV, Histological workup according to SIOP classication revealed inter-
9AVD, 2 other regimens). Postoperative local radiotherapy was mediate risk histology in 20 (13 regressive, 4 mixed, 3 stromal
applied in 2 children (Table 2). subtype), and high-risk histology in 3 tumors (all blastemal subtype).
There were no data for 1 case).
2.3. Surgical and pathological data (Tables 12)
2.4. Lymph nodes
All patients underwent transperitoneal laparoscopic tumor ne-
phrectomy (Fig. 1). The median age of patients at surgery was Lymph nodes (LN) were sampled in 15 of the 24 patients. Numbers
40.35 months (range 14.365.4). Before surgery the median tumor of sampled nodes differed between 0 and 11. Positive LN were
volume on imaging was 73 ml (3.8776). There was one preoperative observed in 5 patients (Table 3).
tumor rupture (patient #15). Among the operating surgeons, there
were 17 with pediatric surgery as subspecialty (no data for 7 cases).
During the 2 previous years the number of nephrectomies for WT 2.5. Oncological outcome
performed within the listed institutions was more than 10 in 7, 610
in 8, and 15 in 2 instances (no data in 7). The number of tumor One local relapse occurred in one patient (patient No. 12). In this
nephrectomies for WT performed by the listed operating surgeon patient initial treatment consisted of 4 weeks AV, histological subtype was
during the previous 2 years was more than 10 in 5 cases, 610 in 8 blastemal. The tumor had shown partial response under neoadjuvant
cases, and 15 in 4 cases (no data in 7 cases). chemotherapy, local stage was I, there were 3 lymph nodes sampled (all
Complete tumor nephrectomy was performed in all children. negative). Postoperative treatment consisted of AVD; no local irradiation
There was one intraoperative complication (splenic injury, surgically was applied. The relapse occurred 8.5 months after surgery.
managed by splenectomy). No conversion to open surgery had to be After a median follow-up of 47 months (2114) all patients were in
carried out. The median value of largest tumor diameter was 5.0 cm complete remission, resulting so far in an event-free survival of 23/24
(2.812), median weight of resected specimen was 134 g (47730). and an overall survival of 24/24 (Table 3).
According to the operating surgeon the tumor capsule was grossly
intact in 17 specimens, operating surgeons were uncertain in 3 cases, 3. Discussion
and they regarded the capsule as not being intact in 2 cases (no data
for 2 cases). Tumors were removed from the abdominal cavity using a Minimally invasive techniques are well established in pediatric
Pfannenstiel incision in 6 cases or using an anterior transverse surgery. Urology represents one major eld within this eld. Laparo-
abdominal incision in 1 case (no data given for 17 patients). scopic procedures have become the standard approach for several
operations on the upper urinary tract. This especially includes
Table 2 pyeloplasties and nephrectomies for benign pathologies [9,18,19]. In
Surgical and pathological data. Tumor histology: IR = intermediate risk, HR = high risk; adults, MIS is regularly used for the surgical treatment of renal
blast. = blastemal predominant subtype, regr. = regressive type, mixed = mixed malignancies [20]. In children, Wilms tumors (WT) are more and
subtype, stromal = stromal predominant subtype; Tumor margins: Neg. = histologically
more often resected laparoscopically, however, only infrequent analyses
free margins, Pos. = histologically detectable tumor cells on margins.
have been published by now, mostly reporting on small patients' cohorts
Pat. No. Age at Largest Tumor Specimen Local Tumor Tumor [1214,21,22]. Very recently, Varlet et al. published the rst multi center
surgery diameter [cm] weight [g] tumor histology margins
study on 17 children undergoing laparoscopic nephrectomy for renal
[M] stage
malignancies. This study included 15 children with WT [23].
1 53.6 4.4 125 I HR (blast.) Neg. Guidelines and recommendations for minimally invasive tech-
2 65.4 5.0 n.d. I IR (regr.) Neg.
3 40.7 6.0 157 II IR (regr.) Neg.
niques and criteria for their use have commonly not been included in
4 34.2 5.5 169 II IR (regr.) Neg. the multicenter treatment protocols so far. On its meeting in Rome in
5 35.7 3.8 68 III IR (regr.) Pos. 2012, the surgical panel of the SIOP Renal Tumor Study Group (RTSG)
6 52.8 3.0 91 I IR (regr.) Neg. found it important to retrospectively analyze respective data of the
7 33.8 3.0 134 I IR (mixed) Neg.
most recent study (SIOP 2001) in order to dene recommendations
8 37.4 2.8 56 I IR (regr.) Neg.
9 42.2 4.0 190 II IR (mixed) Neg. and guidelines for MIS in nephroblastoma to be included in the
10 45.5 7.5 177 II IR (regr.) Neg. upcoming new treatment protocol. Based on these guidelines a
11 46.6 4.0 98 II IR (mixed) Neg. prospective data acquisition and evaluation is then to be undertaken
12 43.3 6.5 254 I HR (blast.) Neg. within the next trial.
13 62.4 9.5 323 I HR (blast.) Neg.
The present study retrospectively analyzed data, which were
14 14.9 5.0 53 III IR (regr.) Pos.
15 48.5 4.0 105 III IR (regr.) Pos. obtained from various countries worldwide. Several limiting aspects
16 22.5 6.8 134 II IR (regr.) Neg. of the analyses have to be considered.
17 46.4 12.0 730 I IR (mixed) Neg. The patient number is small and general conclusions are thus
18 14.3 n.d. n.d. I IR (regr.) Neg.
difcult to draw. Furthermore, follow-up in some patients is short
19 25.6 n.d. n.d. I IR (stromal) Neg.
20 15.0 8.5 310 II IR (stromal) Neg. with respect to an oncological analysis. Nevertheless, we are
21 40.0 5.5. 157 I IR(regr.) Neg. presenting the largest cohort of respective patients with important
22 27.5 6.5 136 I IR (stromal) Neg. implications. The main purpose of this study was not to present a
23 57.5 7.2 47 I n.d. Neg. complete evaluation but rather to build up a basis for the further
24 23.5 3.5 63 I IR (regr.) Neg.
prospective analysis of MIS for nephroblastoma as stated above.
 S.W. Warmann et al. / Journal of Pediatric Surgery 49 (2014) 15441548 1547

Table 3
Data on lymph nodes and oncological outcome. LN sampled = total number of biopsied lymph nodes, LN positive = total number of lymph nodes containing tumor cells; *: lymph node
sampling was documented by surgeon in patient No. 23; however, biopsies did not contain LN material; Postop Chemotherapy: AV-1 = Actinomycin-D + Vincristin, AVD = Actinomycin-
D + Vincristin + Doxorubicin, VCCD = VP-16 + Cyclophosphamid + Carboplatin + Doxorubicin; Outcome: NED = No evidence of disease.

Pat. No. LN sampled LN positive Postoperative chemotherapy Postoperative Radiotherapy Relapse Outcome Follow-up [M]

1 2 2 AVD - - NED 114

2 n.d. 4 AV-1 - - NED 50
3 n.d. 2 None - - NED 19
4 6 0 VCCD - - NED 81
5 0 - AVD - - NED 72
6 11 0 AV-1 - - NED 46
7 0 - AV-1 - - NED 37
8 5 0 AV-1 - - NED 30
9 2 0 AVD - - NED 114
10 1 0 AVD - - NED 81
11 1 0 AVD - - NED 68
12 3 0 AVD - + NED 68
13 0 - VCCD + - NED 62
14 1 1 AVD - - NED 54
15 2 0 AVD + - NED 52
16 n.d. 1 AVD - - NED 48
17 0 - AV-1 - - NED 46
18 0 - AV-1 - - NED 36
19 0 - AV-1 - - NED 31
20 4 0 AV-1 - - NED 33
21 1 0 AV-1 - - NED 19
22 2 0 AV-1 - - NED 13
23 0* -* AV-1 - - NED 13
24 1 0 AV-1 - - NED 2

By the time the study, from which the analyzed data were
collected, was set up, MIS did not play a great role in pediatric
oncology and urology. Many technical improvements, surgical
advances, and innovations of MIS in children have only been
introduced during recent years through which MIS for nephroblas-
toma became more and more feasible. As a consequence, the number
of laparoscopic WT operations was altogether low in the present
study. Although feasibility is not the main aim of surgery in
oncological patients, it seems very likely that the rate of laparoscopic
nephrectomies for WT will further increase.
Another limitation of the present study results from the data
collection. Many relevant details of surgical procedures were not
recorded because MIS did not play a relevant role at the time when the
collection modalities of surgical data were established. For example
there was no information about why surgeons chose the laparoscopic
approach or why they didn't. Details of the operative technique were
regularly lacking including trocar number and positioning, insufa-
tion parameters, modality of specimen removal, and others. Further-
more, it is not known whether the removed kidneys were extracted in
a bag without breakage (to allow an adequate pathologic evaluation),
because this information was not considered in the surgical form. This
information will be included in the next study. The same holds true for
the extent of surgical incision to allow excision of the bag. With these
experiences in mind, the surgical data acquisition will be adapted and
improved for the next trial.
Despite the cited limitations there were numerous relevant
aspects drawn from the analyzed data. There is an ongoing debate
about indications and the general role of MIS in nephroblastoma. The
SIOP 2001 protocol commonly recommends neoadjuvant chemother-
apy in unilateral Wilms tumors except in patients younger than
6 months or older than 16 years. All children in this study received
chemotherapy before surgery. Arguments pro and contra chemother-
apy before operation have been thoroughly discussed between
different Study Groups. Following the SIOP protocol, the rate of
intraoperative ruptures with spillage of tumor cells is lower after
neoadjuvant chemotherapy compared to primary surgery due to
tumor shrinking and encapsulation [3]. This certainly holds true in
MIS and therefore the authors emphasize the recommendations of
preoperative chemotherapy before laparoscopic WT resection. There
is a relevant difference of approaching nephroblastoma between
different study trials. This mainly concerns the use of upfront surgery
in North America (COG) without neodadjuvant chemotherapy in
tumors that seem resectable. However, because of the stated risks of
intraoperative tumor rupture and subsequent spillage, MIS should
only be considered in Wilms tumors after initial chemotherapy.
Furthermore, large tumors are an important issue because once they
become dissected and more and more liberated they are potentially
difcult to handle intra-abdominally. In such cases there is a relevant
risk for rupture with subsequent tumor spillage. Herein, the ipsilateral
border of the vertebral corpuses seems to be a certain limit. In
addition, visualization and management of the renal pedicle is
relevantly restricted in such cases.
Recently, there has been a discussion about a possible overlapping
of indications for MIS and nephron sparing surgery (NSS) in
nephroblastoma. From the pure technical point of view, minimally-
invasive resection of a kidney with a small tumor nodule is certainly
similar to a standard MIS nephrectomy for benign reasons in children.
However, oncological and functional considerations have to be taken
strongly into account at this point. Recent studies indicate that NSS in
unilateral WT is associated with a comparable oncological outcome as
classical tumor nephrectomies [2426]. At the same time there is
growing evidence that late effects after tumor nephrectomy result in
renal failure to a relevant degree; this seems not as much to be the
case after NSS in unilateral WT [2630]. The discussion process within
the surgical panel of the SIOP RTSG therefore resulted in the
recommendation that MIS and NSS should not interfere in terms of
surgical approach: If feasible according to the guidelines of the SIOP
Wilms Tumor protocol [31], NSS should be performed. If NSS is not
feasible and the decision for tumor nephrectomy has been estab-
lished, MIS may be chosen as surgical approach but only by those
surgeons that have a substantial expertise in oncologic pediatric
surgery, pediatric urology, and minimally invasive surgery.
Lymph node (LN) sampling was not sufcient in the present study.
Adequate sampling of LN is precondition for correct tumor staging,
risk stratication, and a correct treatment approach for WT patients in
order to minimize the risk for a local relapse [3,32]. Ehrlich et al.
clearly have shown that LN metastases and microscopic residual
disease have a negative impact on Overall- and Event Free-Survival in
1548 S.W. Warmann et al. / Journal of Pediatric Surgery 49 (2014) 15441548
WT patients (stage III, favorable histology) [32]. These aspects are
especially important with regard to MIS. The adequate number of LN to
be sampled (more than 6) has been determined previously [16,17],
indicating an inadequate LN sampling in the present study. Because of
the above stated limits of data collection in the analyzed study, the
reasons for this were not recorded. Decits of the discipline of LN
sampling in WT surgery have been previously reported analyzing the
open surgical approach [3]. These decits seem even more severe in MIS.
Because of the small total number of patients, a statistical negative
impact of the inadequate sampling could not be calculated. Neverthe-
less, the laparoscopic approach for WT nephrectomy can only be
accepted provided that the common oncological guidelines are strictly
respected. Technical aspects of the operative approach must never be
reason for compromises concerning the correct way of performing WT
surgery. A thorough analysis of the role of MIS in WT surgery is
mandatory, especially since there are already reports on the combined
use with NSS, which underline further possible problems [33].
MIS for WT surgery is a challenging procedure requiring
exceptional expertise by the operating surgeon. The correct estab-
lishment of indications together with a careful patient selection is
essential. The outcome of patients in the presented study was so far
excellent; however certain limitations of the study have to be taken
into consideration. The general guidelines for WT surgery have to be
strictly and consequently respected, especially with regard to LN
sampling. The future prospective evaluation of MIS for WT will bring
further insight into the role of MIS in surgery for nephroblastoma.
Acknowledgement
The following members of the SIOP RTSG surgical panel made
general contributions to this study: Beata Sznajder, Georges Audry,
Giovanni Cecchetto, Frdric Gauthier, Bruce Okoye, Dietrich von
Schweinitz, Jan de Kraker .
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