Robotic-assisted laparoscopy in pediatric surgical oncology: a narrative review
Review Article

Robotic-assisted laparoscopy in pediatric surgical oncology: a narrative review

Nicolas Vinit1,2, Sabine Sarnacki1,2, Thomas Blanc1,2

1Department of Pediatric Surgery and Urology, Necker-Enfants Malades Hospital, APHP, Paris, France; 2UFR de Médecine, Université Paris Cité, Paris, France

Contributions: (I) Conception and design: T Blanc, N Vinit; (II) Administrative support: None; (III) Provision of study materials or patients: None; (IV) Collection and assembly of data: N Vinit; (V) Data analysis and interpretation: N Vinit; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Prof. Thomas Blanc, MD, PhD. Department of Pediatric Surgery and Urology, Necker-Enfants Malades Hospital, APHP, 149 rue de Sèvres, 75015 Paris, France; UFR de Médecine, Université Paris Cité, Paris, France. Email: thomas.blanc@aphp.fr.

Background and Objective: Robotic surgical oncology in children calls for experienced surgeons in minimally invasive surgery (MIS) and a solid oncological background. The aim of this review was to analyze the current state of robotic-assisted laparoscopy in pediatric tumor resection, assess the necessary framework of minimally invasive surgical oncology and describe future developments of the robotic technology.

Methods: A literature search of the MEDLINE/PubMed database was conducted, using the terms “robotic surgery”, “pediatric” or “children” and “oncology” or “tumor”. All relevant English-language studies published between 2008 and 2022 were reviewed.

Key Content and Findings: Although concerns have been raised regarding the use of MIS in surgical oncology, current literature reports similar oncological outcome if surgeons comply with the oncologic principles. The benefits of MIS have been established for robotic surgery in adult studies, including a shorter time to adjuvant chemotherapy. Surgical feasibility should be assessed based on tumor characteristics, preoperative imaging focusing on vascular involvement and surgeon’s experience until clear guidelines are issued. The difficulties in establishing eligibility criteria for robotic resection of pediatric tumors lie in the great variability of indications, heterogeneity in tumor histology with their own surgical specificities, and wide range of age and weight, as shown by the literature review we performed. Between 2008 and 2022, 31 studies reported 171 cases with three studies including at least ten patients. The most reported procedure was adrenalectomy (41 cases). Current research in pediatric surgical oncology focuses on intraoperative locoregional treatment, improved vision with fluorescence and dyed-loaded specific probes and the many possibilities of enhancement software using the robotic console.

Conclusions: The robotic technology allows the surgeon to push the boundaries of conventional laparoscopy. Specific surgical guidelines are necessary.

Keywords: Robotic surgery; minimally invasive surgery (MIS); pediatric tumor; surgical oncology; pediatric surgery

Submitted Apr 20, 2023. Accepted for publication Dec 04, 2023. Published online Dec 18, 2023.

doi: 10.21037/tp-23-251

Introduction

The use of robotic surgery has spread in the pediatric population as precision and stability offered by the technology allow for minimally invasive treatment of more and more complex cases (1). Surgical oncology in children encompasses a wide range of surgical morbidity and difficulty, from simple organ removal to large tumors with vascular involvement and adjacent-organ invasion. All these procedures are to follow the oncologic principles to ensure the best possible oncologic outcome, keeping in mind that our patients have a long life ahead of them. Managing these cases calls for experienced surgeons in minimally invasive surgery (MIS) and a solid oncological background (2).

The aim of this review is to analyze the current state of robotic-assisted laparoscopy in pediatric tumor resection, show the pitfalls in establishing clear guidelines in minimally invasive surgical oncology and describe future developments of the robotic technology. We present this article in accordance with the Narrative Review reporting checklist (available at https://tp.amegroups.com/article/view/10.21037/tp-23-251/rc).

Methods

A literature search of the MEDLINE/PubMed database was conducted, using the terms “robotic surgery”, “pediatric” or “children” and “oncology” or “tumor”. All relevant English-language studies published between 2008 and 2022 were retrieved. All types of studies regarding thoracic, abdominal or oral robotic surgery were sought, including case reports. Literature reviews, meta-analyses or studies with patients’ overlap were excluded.

The search strategy summary is shown in Table 1.

Table 1

The search strategy summary

Items Specification
Date of search May 21st, 2022
Databases and other sources searched MEDLINE/PubMed
Search terms used Robotic surgery, pediatric/children, oncology/tumor
Timeframe 2008 to 2022
Inclusion and exclusion criteria English-language studies included. Reviews, meta-analyses and studies with patients’ overlap excluded; neurosurgery, orthopedics, ophthalmology and cardiac surgery excluded.
Selection process Performed by N.V. (author)

Robotic surgical oncology in children

The difficulties in establishing eligibility criteria for robotic resection of pediatric tumors lie in the great variability of indications, heterogeneity in tumor histology with their own surgical specificities, and wide range of age and weight (3,4). The literature search we conducted on robotic-assisted surgical oncology (Figure 1) yielded a total of 31 studies reporting 171 cases between 2008 and 2022, including 21 (68%) case reports (Table 2). Only three studies counted ten patients or more. The five most reported procedures were partial or radical adrenalectomy (41 cases), partial or radical nephrectomy (30 cases), anterior or posterior mediastinal mass excision (17 cases), partial or radical ovariectomy (15 cases) and retroperitoneal lymph node dissection (14 cases).

Figure 1 Flowchart of the reviewing process conducted on robotic-assisted surgical oncology in children.

Table 2

Results of the literature search on cases of robotic-assisted surgical oncology in children between 2008 and 2022

Authors Year Surgical procedure Tumor pathology Total # cases (N=171) # cases (N=171) Age at surgery (years) Conversion rate Complications
Meehan et al. 2008 Mediastinal mass excision Neuroblastic tumor 5 2 9.8 [2–17] 0 0
Mature teratoma 1
Germ cell tumor 1
Inflammatory mass of unclear etiology 1
Rogers et al. 2008 Partial adrenalectomy Pheochromocytoma 1 1 14 0 0
Meehan et al. 2008 Radical ovariectomy Mature teratoma 10 1 NA 40% (4/10) Incomplete resection (neuroblastoma)
Partial ovariectomy NA 1
Unilateral adrenalectomy Neuroblastoma 6
Pheochromocytoma
Resection of pancreatic tumor NA 1
Retroperitoneal tumor resection Ganglioneuroma 1
Cost et al. 2012 RPLND Paratesticular embryonal rhabdomyosarcoma 2 1 15 0 0
Malignant non-seminomatous germ-cell tumor 1
Cost et al. 2012 Partial nephrectomy Clear cell renal carcinoma 1 1 14 0 0
Kokot et al. 2013 TORS Synovial sarcoma 1 1 15 0 0
Cost et al. 2015 Radical nephrectomy Wilms tumor (prechemotherapy) 1 1 14 0 0
Glaser et al. 2017 RPLND Non-seminomatous germ cell tumor 2 1 15 and 17 0 0
Ectomesenchymoma with a spindle-cell rhabdomyosarcoma component 1
Hu et al. 2017 Distal pancreatectomy Insulinoma 1 1 9 0 0
Yadav et al. 2018 Partial nephrectomy Wilms tumor 1 1 1.5 0 Lymphorrhea
Agarwal et al. 2018 Radical prostatectomy Embryonal rhabdomyosarcoma 1 1 7 0 0
Hagendoorn et al. 2018 Pancreatoduodenectomy Solid pseudopapillary tumor 1 1 10 0 Delayed gastric emptying
Arnold et al. 2018 TORS Neurofibroma 1 1 6 0 Incomplete resection
Liang et al. 2018 Pancreatic enucleation Insulinoma 1 1 9 0 0
Varda et al. 2018 Partial nephrectomy Papillary renal cell carcinoma 4 1 3–17 0 0
Unilateral adrenalectomy Ganglioneuroma 1
RPLND Paratesticular rhabdomyosarcoma 2
Non-seminomatous germ-cell tumor
Lalli et al. 2019 Distal pancreatectomy Solid pseudopapillary tumor 1 1 17 0 0
Llorens de Knecht et al. 2019 Radical prostatectomy Primitive prostatic carcinoid tumor 1 1 3 0 Two febrile episodes, death due to local recurrence and bone metastasis
Xie et al. 2019 Ovarian tumorectomy Mature teratoma 4 3 7.5 [1–13] 0 0
Mucinous cystadenoma 1
Navarrete Arellano et al. 2019 Unilateral adrenalectomy Pheochromocytoma 4 1 4.8 (average) 25% (1/4) 0
Radical nephrectomy NA 1
Mediastinal mass excision Mature teratoma 1
Retroperitoneal mass excision Lipoma 1
Canevari et al. 2020 TORS Base-tongue Ewing sarcoma 1 1 16 0 0
Brown et al. 2020 RPLND Testicular or paratesticular cancer (NA) 4 4 NA NA NA
Mitra et al. 2020 Unilateral adrenalectomy Ganglioneuroblastoma 3 2 2–13 0 0
Pheochromocytoma 1
Silveri et al. 2020 Partial nephrectomy Perivascular epithelioid cell tumor 1 1 14 0 0
Nishio et al. 2020 Radical cystectomy Embryonal rhabdomyosarcoma 1 1 6 0 0
Nota et al. 2021 Distal pancreatectomy Neuroendocrine tumor 1 1 11 0 0
van Ramshorst et al. 2021 Central pancreatectomy Solid pseudopapillary tumor 1 1 16 0 Grade B pancreatic fistula
Schulte Am Esch et al. 2021 Pancreatic enucleation Insulinoma 1 1 10 0 Pancreatic pseudocyst
Lowrey et al. 2021 Unilateral adrenalectomy Adrenocortical tumor 1 1 4 0 0
Li et al. 2021 Partial or radical cystectomy Bladder/prostate rhabdomyosarcoma 8 8 NA NA NA
Vatta et al. 2022 Radical ovariectomy Mature teratoma 13 4 13.2 [8–16.9] 0 0
Partial ovariectomy Mature teratoma 5
Serous cystadenoma
Mucinous cystadenoma
Seromucinous cystadenoma
Pelvic mass excision Serous papillary cystadenofibroma of the fallopian tube 2
Mediastinal mass excision Ganglioneuroblastoma 1
Perirenal mass excision Neuroblastoma recurrence 1
Blanc et al. 2022 Unilateral adrenalectomy Neuroblastic tumor 93 18 8.2 [3.6–13] 8% (7/93) Pneumothorax (n=2), postoperative collection (n=1), anastomotic stenosis (n=1), bowel adhesion (n=1)
Pheochromocytoma
Adrenocortical adenoma
Bilateral adrenalectomy McCune Albright 5
Carney complex
Pheochromocytoma
Radical nephrectomy Wilms tumor 17
Undifferentiated renal sarcoma
Radical nephrectomy with caudal splenopancreatectomy Wilms tumor 1
Partial nephrectomy Wilms tumor 6
Tubular papillary carcinoma
Metanephric adenoma
Nephrogenic rest
Central pancreatectomy Focal congenital hyperinsulinism 3
Somatostatinoma
Distal pancreatectomy Focal congenital hyperinsulinism 1
Mediastinal mass excision Neuroblastic tumor 10
Mature teratoma
Thymectomy Thymoma 4
Myasthenia
Prophylactic thymectomy for MEN1
Partial gastrectomy Inflammatory myofibroblastic tumor 1
Radical gastrectomy (totalization) Inflammatory myofibroblastic tumor 1
Pulmonary lobectomy Bronchial carcinoid tumor 1
Pelvic mass excision Lipoma 9
Embryonal rhabdomyosarcoma
Neurofibroma
Inflammatory myofibroblastic tumor
Mature teratoma
Germ cell tumor
Neuroblastic tumor
Paraganglioma
Omentectomy Inflammatory myofibroblastic tumor 1
Mesenteric mass excision Leiomyoma 1
RPLND Seminomatous or Non-seminomatous germ cell tumor 4
Retroperitoneal tumor resection Neuroblastic tumor 10
Paraganglioma

In the "Age at surgery" column, data are presented as median [range], number, or range unless otherwise specified. NA, not available; RPLND, retroperitoneal lymph-node dissection; TORS, transoral robotic surgery; MEN1, multiple endocrine neoplasia type 1.

The scarcity and great diversity of pediatric tumors are a serious impediment in building the large series needed to establish robotic surgery oncologic guidelines.

Initially intended for damage control surgery on the battlefield, robotic surgery was first reported in 1998 by Himpens et al. (5). Meininger et al. (6) were then the first to borrow this adult-designed surgical technology and use it in children in 2001. Seven years later, robotic surgery was first used for pediatric tumor resection (7).

Contrary to adult surgery, the development of a new technology in children cannot wait for randomized control trials. This was the case with laparoscopy and robotic surgery is no exception. Potential benefits and pitfalls are inferred from retrospective studies (8). Pediatric robotic-assisted surgical oncology has spread without ironclad proof of safety and effectiveness (9), hence the initial skepticism that surrounded its initial use.

The use of MIS in surgical oncology has long been debated. The main concern was the risk of incomplete resection and recurrence (10,11). When performing such procedures, abiding by the oncologic principles is paramount: avoid tumor spillage, en-bloc macroscopically complete resection, optimal lymph node resection and preserving adjacent organs (3,12,13). MIS does not worsen the oncologic outcome as long as the above-mentioned principles are respected, as shown by Bouty et al. (14) or Blanc et al. (15) for the resection of Wilms tumor using laparoscopy or robotic-assisted surgery, respectively. Furthermore, MIS is associated with a shorter time to adjuvant chemotherapy in large adult series (16,17) and might, therefore, improve the oncologic outcome in selected cases.

Several other concerns have been addressed in the literature: the greater risk of port-site tumor recurrence, which has been disproven by adult series (18,19); the lack of haptic feedback as a possible cause of tumor rupture, which has been replaced by an enhanced visualization of the tension applied to the tissue and limited tumor manipulation (20); and the need for a larger scar to extract the tumor since the latter can be concealed and reduced to the minimum to allow safe extraction (21,22).

While the benefits of MIS on postoperative outcome are being reported in children (23,24), they have been established for robotic surgery in adult studies. For adult pancreatic resection, MIS has been shown to decrease intraoperative blood loss and postoperative complications, reduce time to oral intake and length of hospital stay, without any difference on mortality and reoperation rate compared to an open approach in a meta-analysis by Nigri et al. (25). Robotic pancreatic resection has also been shown to decrease the conversion rate compared to laparoscopy in adults with benign or malignant lesions of the distal pancreas (26), decrease the rate of postoperative fistula compared to open Whipple’s procedure in adults (27) and significantly improve spleen preservation in pancreatic caudal resections compared to laparoscopy in adult benign or malignant pancreatic lesions (28). A randomized control trial on robotic versus laparoscopic oncologic gastrectomy in adults has also yielded great results with a higher Clavien ≥II complication rate in the laparoscopic group, no difference regarding the number of retrieved lymph nodes or surgical curability and an improved postoperative recovery in the robotic group (29). A comparative study on robotic versus open thymectomy in adult myasthenia and thymoma has shown a significant decrease of postoperative pain and hospital stay without any difference in operative time and postoperative complications (30). In retroperitoneal lymph node dissection, a large cohort study of testicular and para-testicular cancer, including pediatric patients, reported a significantly shorter length of hospital stay using the robotic technology compared to a non-robotic approach (31). MIS retroperitoneal lymph node dissection is also associated with a lower rate of retrograde ejaculation and bowel complication compared to an open approach, although the risk of vascular injury and chylous ascites was greater (32).

Vascular involvement remains one the greatest challenges of minimally invasive pediatric surgical oncology (15). Surgical feasibility should be assessed based on tumor characteristics, preoperative imaging possibly with tridimensional reconstruction and surgeon’s experience until clear guidelines are issued.

The growing number of cases entails the development of surgical guidelines for robotic surgery, similar to the use of image-defined risk factors in the laparoscopic treatment of neuroblastic tumors (33,34). Robot-specific guidelines are required as robotic technology has pushed the boundaries of laparoscopic surgery in terms of surgical complexity (3). Robotic surgery is closer to open surgery than laparoscopy with a less steep learning curve, allowing for the resection of larger and more complex tumors than laparoscopy (7,15). The substantial experience of Blanc et al. (3) in robotic surgical oncology led to a primary set of guidelines in patient selection based on tumor location and pathology, as shown in Table 3.

Table 3

Guidelines on patient selection in robotic surgical oncology published by Blanc et al. (3)

Tumor type Robotic surgery may be considered Relative contraindications Formal contraindications
Thoracic tumors Paravertebral neuroblastoma Age <2 years old (limited access) Encasement of vessel
Tumor limited to the thymic bed (teratoma, thymoma) Mediastinal extension (pericardium, esophagus, trachea)
Lung resection (single metastasis)
Renal tumors Tumor not crossing the ipsilateral border of the spine AND Tumor with a thin rim of normal parenchyma Tumor crossing the midline
Tumor with a thick rim of normal parenchyma AND Tumor crossing the ipsilateral border of the spine (but not the midline) Tumor infiltrating extrarenal structures (liver, diaphragm)
Tumor without any sign of infiltration of extrarenal structures AND Tumor with encasement of renal vessels (e.g., sarcomas, carcinomas)
ETV/EPBV <1.5% ETV/EPBV 1.5–2% ETV/EPBV >2%
Neuroblastic tumors Paravertebral (thoracic, abdominal or pelvic) neuroblastoma without foramen extension One or two IDRFs >2 IDRFs
Adrenal tumor Paravertebral neuroblastoma with foramen extension but without spinal component Any IDRF number involving median vessels and/or both renal pedicles
Neuroblastoma of the Zuckerkandl ganglia Paravertebral neuroblastoma with foraminal and intraspinal extension
ETV/EPBV >1% AND ETV/EPBV 1–2% ETV/EPBV >2%
No IDRF
Paragangliomas/pheochromocytomas Encasement of major vessels
Adrenocortical carcinomas All adrenocortical carcinomas
Solid pseudopapillary neoplasms All solid pseudopapillary tumors

ETV/EPBV, ellipsoid tumor volume (0.52 × width × length × height, mm3) over estimated patient blood volume (75 mL/kg for children >3 months); IDRF, image-defined risk factors.

The widespread use of robotic surgery paved the way for future technologic advancements. Current research in pediatric surgical oncology focuses on intraoperative locoregional treatment, improved vision with fluorescence and dyed-loaded specific probes and the many possibilities of enhancement software using the robotic console (35). A case of pediatric pancreatic enucleation using a robotic ultrasound probe with dual visual and ultrasound images integrated in the robotic console was recently reported (36). Tridimensional image overlay can be implemented in the console to guide the surgeon’s hand (37). Such an approach has proven beneficial for patients with a decreased complications rate, better resection margins and preserved renal function in a multicentric study on partial nephrectomy in adult renal cancer (38). Several papers have reported the use of Indocyanine green in tumor resection using FireflyÒ (Intuitive Surgical, Sunnyvale, CA, USA), the dedicated robotic interface for near-infrared-fluorescence-guided surgery, both in pediatric and adult surgery (39-41). Robotic gamma detection probes are also being explored for radio-guided surgery as described by Martelli et al. who used radiopharmaceuticals for the resection of neuroblastic tumors (42).

Andras et al. (43) have reviewed possible applications of integrated artificial intelligence in robotic surgery: as an assessment tool for surgical skills in surgical training, to predict operative time and postoperative outcome based on clinical and intraoperative data, to replace haptic feedback with a suture breakage warning system, or using enhanced reality as surgical guidance. Autonomous robotic surgery with human supervision could be a future prospect as the use of such a technology has already been described on human cadavers (44). With continued miniaturization and instrumentation improvements, robotic surgery should be able to overcome its current challenges in the pediatric population, namely in neonatal surgery with the use of 3-mm robotic instruments (45).

Conclusions

The robotic technology may reduce the morbidity of surgical oncology in children and improve the postoperative outcome in terms of pain, recovery, hospital stay and scarring. The oncologic outcome remains the primary goal and robotic-assisted laparoscopy cannot be used at the expense of the oncologic principles. The robotic technology allows the surgeon to push the boundaries of conventional laparoscopy. Specific surgical guidelines are, therefore, necessary to define the indications and contraindications of robotic resection for pediatric tumors. Their heterogeneity and scarcity make it all the more difficult and underline the need to identify expert centers.

Acknowledgments

Funding: None.

Footnote

Provenance and Peer Review: This article was commissioned by the Guest Editor (Ciro Esposito) for the series “Pediatric Robotic Surgery” published in Translational Pediatrics. The article has undergone external peer review.

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://tp.amegroups.com/article/view/10.21037/tp-23-251/rc

Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-23-251/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-23-251/coif). The series “Pediatric Robotic Surgery” was commissioned by the editorial office without any funding or sponsorship. T.B. is an official proctor in Intuitive Surgical. The authors have no other conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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Cite this article as: Vinit N, Sarnacki S, Blanc T. Robotic-assisted laparoscopy in pediatric surgical oncology: a narrative review. Transl Pediatr 2023;12(12):2256-2266. doi: 10.21037/tp-23-251

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