Utilization of Robotics in Pediatric Surgical Oncology

Although survival rates for childhood cancer have substantially increased throughout the last several decades, pediatric surgical oncology practices have not significantly changed.1,2 Although minimally invasive surgery (MIS) has become increasingly utilized in pediatric surgery due to its numerous benefits including shorter hospital length of stay and improved cosmesis, robotic surgery for the oncologic resection of pediatric tumors remains controversial.3, 4, 5

Robotic-assisted resections have been increasingly utilized for adult malignancies with many studies demonstrating noninferior oncologic resection, margin status, and lymph node harvest compared to laparoscopic or open techniques.6,7 The robotic platform allows for enhanced three-dimensional visualization with improved magnification, freedom of motion, and tremor reduction.8,9 Furthermore, it facilitates ease of fluorescence-guided surgery (FGS) utilization, which has been demonstrated to enhance live identification and discrimination of malignant tumors versus benign tissue and therefore improve oncologic outcomes. FGS can also be used for sentinel lymph node biopsy and to augment identification of lesions and metastases undetectable on cross-sectional imaging due to size or unable to be palpated intraoperatively because of depth.8,10, 11, 12, 13, 14, 15 Despite these advantages, pediatric solid tumors are relatively rare, heterogeneous in their presentation, typically more primitive in nature, and frequently demonstrate rapid growth relative to adult malignancies.16 In combination with the increasing but still limited data regarding patient selection and outcomes, the adoption of robotic surgery for pediatric tumors has been slow and met with significant skepticism.3,16

However, robotic surgery has the potential to be particularly advantageous for resection of pediatric tumors. Pediatric malignancies typically require multimodal therapy including chemotherapy, radiation therapy, and surgery. In addition to the robotic approach's previously mentioned technical advantages, its minimally invasive nature shortens hospital length of stay and recovery times, which may allow patients to resume adjuvant chemotherapy more rapidly.17 This decreased recovery time plus smaller scars may also mitigate the psychological distress of cancer treatment in young children, particularly those with malignancies associated with cancer predisposition syndromes that increase their risk of multiple and metachronous tumors.4,18 Enhanced understanding and optimization of robotic-assisted resection is needed in order to successfully implement utilization and improve outcomes.

The successful implementation of the robotic approach to pediatric surgical oncology relies on several factors. First, it is recommended that surgeons overcome the learning curve associated with robotics by performing less challenging general surgery cases prior to performing a complex robotic-assisted oncologic resection.3 Furthermore, mentoring by surgeons with extensive experience in both oncologic surgery and the robotic platform is invaluable for maintaining the integrity of oncologic resection.16 The use of dual consoles can further facilitate the safe instruction of less experienced surgeons by those with more experience.16

The overall reported conversion rate to an open approach is approximately five percent, with challenging dissection and surgeon discomfort being the most commonly reported causes of conversion.16 This number decreased with increasing surgeon experience.17 Therefore, it is recommended that institutions early in the adoption of robotic pediatric surgical oncology consider tumor size and suspected ease of dissection during patient selection until surgeon experience increases.17 Furthermore, patient selection should be optimized by multidisciplinary team discussion that includes medical oncologists, radiologists, radiation oncologists, and experienced surgeons, as with any complex pediatric oncology case.

However, the need for adequate experience and comfort with the robotic platform extends to the entire team. Operating room providers should be cognizant of positioning patients in a manner that prevents hyperextension or flexion, as well as any potential collisions between the robot and the patient or surgical assistants.16,19 Furthermore, it is vital that vascular access is secured and that the anesthesiology time have adequate access to the patient throughout the operation in order to maintain patient safety.16

It is commonly stated that “in the world of surgical oncology, biology is king, selection is queen, technical maneuvers are the prince and princess.”20 However, there is a conspicuous absence of guidelines regarding indications for robotic-assisted resection, patient selection, and optimization of robotic techniques for pediatric surgical oncology.4

The oncologic principles of robotic-assisted resection should not deviate from those of open surgery. These include, but are not limited to, achievement of sufficient margins, prevention of tumor spillage, and adequate lymph node dissection (when indicated).4 It is of the utmost importance that the principles of oncologic resection are maintained regardless of the technique used. An open approach is always superior to an incomplete minimally invasive resection.

The rapid adoption of robotic-assisted surgery has been further complicated by concerns regarding the risks of inferior oncologic resection, tumor rupture or spillage, or port-site recurences.4,21

Data regarding outcomes of oncologic resection using robotic versus laparoscopic or open techniques remain in preliminary stages in the pediatric literature. However, data from the adult literature suggest that outcomes after robotic resection are not inferior for a variety of cancer types with standardized training and sufficient experience.22, 23, 24, 25, 26, 27, 28, 29 In fact, several studies demonstrated superior outcomes with robotic resection regarding time to return of bowel function and initiation of feeds, hospital length of stay, estimated blood loss, complication rates, and lymph node harvest.24,26,28,29

The lack of haptic feedback with robotics has raised concerns for potentially increased risk of tumor rupture and spillage. However, proponents of the robotic platform suggest that the enhanced three-dimensional high-definition stereoscopic optics, which can be controlled by the operating surgeon from the console, mitigate this limitation and allow for enhanced discrimination between malignant tumor and benign tissue.4,16,17,30

The incidence of port-site recurrences in robotic surgery is extremely rare with only a limited number of cases in the adult data and zero reported cases in the pediatric data to date.4,5,16,31,32 Traditionally thought to be secondary to increased manipulation of ports or the “chimney effect” associated with abdominal insufflation during MIS, recent studies in adults have suggested that port-site recurrences are instead an indication of generalized peritoneal recurrence unpreventable by port-site resection.33 Furthermore, outcomes appear to be equivalent between laparoscopic or robotic versus open approaches.16,33

A robotic-assisted approach should be considered for numerous thoracic pathologies including: paravertebral neuroblastomas, tumors of the thymic bed, or lung resection of a single metastasis.4 Resection of mediastinal tumors, in particular, can typically be safely and easily achieved using a robotic approach. Meehan et al. considered mediastinal masses to be the “golden indication” for robotic resection with zero conversions to an open or thoracoscopic approach in their ten-year case series regardless of tumor pathology.3,34 Furthermore, the robotic platform is conducive to the use of FGS including indocyanine green (ICG), which can be used as an adjunct for removal of thoracic tumors and pulmonary metastases, as well as lymph node biopsies.35, 36, 37

Reported relative contraindications to a robotic approach may include smaller children (i.e., less than two years of age or three to five kg in size) due to more limited working space.3,4,9 Currently, robotic endoscopes measure 8.5 mm and 12 mm with approved robotic instruments measuring 5 and 8 mm in size.3,38 This can be prohibitive in smaller children and neonates due to their narrow rib spaces and smaller thoracic cavities.3,38 However, the ongoing development of smaller robotic endoscopes and instruments is likely to mitigate this issue in the future.

Formal contraindications to a robotic-assisted approach include encasement of vessels or tumor extension into mediastinal structures such as the pericardium, esophagus, or trachea.4

Successful utilization of the robot has been documented for resection of numerous abdominal tumors in pediatric patients, including neuroblastic tumors, adrenal tumors, renal tumors, hepatic and biliary tumors, and pancreatic tumors.4,39, 40, 41, 42, 43, 44 With time and increased utilization of the robotic platform in children, it is likely that indications for the robotic approach will expand, subsequently improving guidelines for patient selection and optimization of robotic techniques.

The robotic approach has demonstrated feasibility for porta hepatis anastomosis and biliary reconstruction.40,45 In adult patients, robotic distal pancreatectomy was associated with higher rates of splenic preservation compared to open or laparoscopic approaches, which is of increased importance in pediatric patients due to their increased vulnerability of infection secondary to encapsulated bacteria.41,46,47 The robot's enhanced visualization and magnification and increased freedom of motion facilitate careful dissection of the splenic vessels off of the pancreas.41 For pancreatic operations in smaller children, insertion of robotic trocars below the umbilicus can aid in maximizing working space.43

There are numerous reports of robotic-assisted resections of neuroblastic tumors ranging from localized to metastatic disease.4,5,16,48, 49, 50, 51 For patients with low-risk disease, a robotic-assisted resection affords a minimally invasive approach with reduction of morbidity and improved recovery time.49 For patients with high-risk disease determined to be good candidates for a robotic approach, the rapid recovery time may decrease time to adjuvant therapy and therefore optimize oncologic control of systemic disease.49 Increased visualization and freedom of motion with enhanced tremor control allows for precise and delicate dissection in experienced hands, particularly when dissecting the tumor off of adjacent blood vessels.49

Blanc et al. suggested that a robotic approach should be considered for: paravertebral neuroblastic tumors without foraminal extension, adrenal tumors, tumors of the Zuckerkandl ganglia, tumors with an ellipsoid tumor volume to estimated patient blood volume (ETV/EPBV) ratio of less than 1%, and neuroblastic tumors without image-defined risk factors (IDRFs).4 The authors considered relative contraindications of the robotic approach to include: tumors with one or two IDRFs, paravertebral tumors with extension into the foramen but without a spinal component, or tumors with an ETV/EPBV of 1-2%.4 In their case series, the robotic platform was advantageous for large neuroblastoma tumors with IDRFs, particularly those abutting the ipsilateral renal pedicle, and for pelvic tumors.4 Formal contraindications included: three or more IDRFs, IDRFs involving the celiac artery, superior mesenteric artery, and/or both renal pedicles, or tumors with an ETV/EPBV ratio greater than 2%.4

The robotic platform offers numerous advantages for the resection of renal tumors, including enhanced visualization and fine motor control for extended lymph node dissections and ease of intracorporeal suturing of the nephrectomy bed for nephron-sparing surgery or partial nephrectomy.5,51, 52, 53 Partial nephrectomy, when indicated, is particularly advantageous in pediatric patients, especially for those who may require nephrotoxic systemic chemotherapy.51

Trocar placement in pediatric renal tumor resection is similar to that of adults. However, for smaller patients with larger tumors, working ports may need to be adjusted (e.g., preferentially placed in the midline) to maximize distance between robotic arms and therefore working space within the abdomen.51,54 The specimen should be placed in a specimen retrieval bag and removed through one of the port sites or through a Pfannenstiel incision for improved cosmesis.53

Despite reports demonstrating the feasibility of a minimally invasive approach for renal tumor resection, including Wilms tumor resection, the risk of tumor rupture and spillage has led to hesitancy regarding the utilization of a laparoscopic or robotic approach.55,56 Blanc et al. recommend that a robotic approach be considered for tumors with a thick rim of normal parenchyma that do not infiltrate adjacent structures or cross the ipsilateral border of the spine and that have an ETV/EPBV less than 1.5%.4 Relative contraindications include: tumors with a thin rim of normal parenchyma, tumors that cross the ipsilateral border of the spine (but not midline), or tumors with an ETV/EPBV of 1.5-2%. Formal contraindications include: tumors crossing midline or infiltrating adjacent structures, tumors encasing renal vessels, and tumors with ETV/EPBV greater than 2%.4 Given that tumor size is positively correlated with risk of tumor spillage, it must be accounted for when choosing a surgical approach.57 In addition to ETV/EPBV, tumor diameter greater than 10% of a patient's height has been proposed as another indication for an open approach.58

Robotic surgery has been successfully incorporated into both gynecologic and urologic surgery for resection of pelvic masses. It provides seven degrees of freedom in a limited working space, making it ideal for deep pelvic operations.19,59 However, trocar placement is critical for maximizing working space in the abdomen and pelvis of children. Patients with at least 13 centimeters between their anterior superior iliac spines or at least 15 centimeters of puboxyphoid distance are thought to be best suited for a robotic approach due to the decreased likelihood of collisions between robotic arms.60 Typically, the endoscope should be placed in the midline of the upper abdomen with working ports placed on each side of the scope at the interior axillary line below the costal margins.61 Robotic-assisted surgery for complex pelvic procedures is thought to confer an ergonomic advantage with surgeon reports demonstrating decreased musculoskeletal pain in comparison to open or laparoscopic procedures.62 In addition, the enhanced ergonomic support of the robotic platform improves surgeon comfort and prevents muscle fatigue during prolonged pelvic dissections.59

The successful utilization of robotic surgery has been documented for numerous gynecologic oncology indications including the resection of ovarian tumors in children.61 Robotic sealing devices facilitate dissection while minimizing bleeding. In addition, FGS enhances: differentiation of tumor from benign tissue, identification of lymph nodes, and assessment of ovarian perfusion in cases of torsion.63

Initially used in adult patients, robotic-assisted resections have been used for endometrial cancer, cervical cancer, ovarian cancer, debulking operations, and staging procedures including sentinel lymph node mapping.23 A robotic-assisted approach has comparable outcomes to conventional laparoscopy for the management of gynecologic cancers but with a shorter learning curve.23 In comparison to open surgery, robotic surgery has been associated with decreased blood loss and faster recovery times.24

The use of robotics has experienced widespread dissemination within the field of adult urologic oncology.4,51 Despite this success in adult urology, the utilization of robotics in pediatric urologic oncology has been relatively slower to progress.51 The reasoning for this is thought to be multifactorial, including: the relatively lower incidence of pediatric genitourinary malignancies leading to lower case volumes, prohibitively large or complex masses at time of presentation, the success of current management techniques limiting incentives to test new techniques, and the frequent management of pediatric genitourinary malignancies by general surgeons who may have less robotic experience than urologists.51 However, collaboration between an adult urologic oncologist with extensive robotic experience and a pediatric urologist can be beneficial for adapting adult robotic techniques for pediatric genitourinary oncology cases when first establishing a robotics program.30,51

A robotic-assisted approach allows for patients to benefit from a minimally invasive approach and for surgeons to benefit from enhanced visualization and dexterity with comparable outcomes.51 The use of robotic-assisted approaches for prostatectomies, cystectomies, urinary diversion, and retroperitoneal lymph node dissection have been successfully documented in pediatric patients.22,30,51,64, 65, 66 Benefits of the robotic approach include improved cosmesis, enhanced visualization and dissection in the narrow pelvis, particularly for patients treated with neoadjuvant chemotherapy and radiation that may increase the difficulty of dissection, potentially decreased adhesion formation should a patient need additional operations, and increased adherence to enhanced recovery after surgery protocols.22,30,64,65

The robotic platform continues to be adapted for an increasing number of indications in pediatric oncology. For instance, the ROSA system has been utilized for assisting biopsies and/or laser interstitial thermotherapy in the diagnosis and management of neurooncological disease.67 The ROSA system registers preoperative imaging studies and utilizes a computer-driven robotic arm to perform minimally invasive frameless stereotactic surgery, directing surgical instruments along a planned trajectory with precision.67 These procedures can be successfully performed with concurrent intraoperative magnetic resonance imaging.67

The rapid development and research surrounding robotic surgery and augmented reality have the potential to induce vast changes in pediatric surgical oncology practice.8 Oncological outcomes could be improved by enhancing visualization of cancer and precision of dissection via the robotic platform's enhanced degrees of freedom, tremor reduction capabilities, and improved surgeon ergonomics.5,8 Furthermore, this minimally invasive approach, in addition to improving cosmesis, can expedite patient recovery and decrease the time to adjuvant therapy.5,22 Therefore, robotic-assisted surgery has the potential to substantially improve the care of pediatric patients with cancer.

Improvements in the current technology, including the development and implementation of smaller robotic endoscopes and instruments, as well as mechanisms for cost reduction, are needed for more widespread implementation of robotic surgery in pediatrics.5,19 Increased utilization and assessment of outcomes will facilitate further development of indications and guidelines for robotic-assisted resections.4,5 With more widespread adoption of robotics, mechanisms of standardized training and assessment of technical and long-term oncologic outcomes will need to be established. Proficiency-based curriculums involving: virtual reality simulation and inanimate biotissue drills, video libraries, intraoperative training and evaluation, and ongoing skills maintenance and assessment, have demonstrated feasibility in training surgeons to a level of mastery needed to maintain patient safety and oncologic outcomes.27

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