PERSPECTIVE published: 25 March 2021 doi: 10.3389/fsurg.2021.649418 Pediatric Challenges in Robot-Assisted Kidney Transplantation Julien Grammens 1 , Michal Yaela Schechter 1 , Liesbeth Desender 2 , Tom Claeys 1 , Céline Sinatti 1 , Johan VandeWalle 3 , Frank Vermassen 2 , Ann Raes 3 , Caroline Vanpeteghem 4 , Agnieszka Prytula 3 , Mesrur Selçuk Silay 5 , Alberto Breda 6 , Karel Decaestecker 1 and Anne-Françoise Spinoit 1* 1 Department of Urology, ERN eUROGEN Accredited Centre, Ghent University Hospital, Ghent University, Ghent, Belgium, 2 Department of Vascular and Thoracic Surgery, Ghent University Hospital, Ghent University, Ghent, Belgium, 3 Department of Pediatric Nephrology and Rheumatology, ERN ERKNet Accredited Centre, Ghent University Hospital, Ghent University, Ghent, Belgium, 4 Department of Anesthesiology and Perioperative Medicine, Ghent University Hospital, Ghent University, Ghent, Belgium, 5 Division of Pediatric Urology, Department of Urology, Biruni University, Istanbul, Turkey, 6 Department of Urology, Fundació Puigvert, Universidad Autonoma de Barcelona, Barcelona, Spain Edited by: Felix K. H. Chun, University Hospital Frankfurt, Germany Kidney transplantation is universally recognized as the gold standard treatment in Reviewed by: patients with End-stage Kidney Disease (ESKD, or according to the latest nomenclature, Luis Alex Kluth, University Hospital Frankfurt, Germany CKD stage 5). Robot-assisted kidney transplantation (RAKT) is gradually becoming Christian P. Meyer, preferred technique in adults, even if applied in very few centra, with potentially University Medical Center improved clinical outcomes compared with open kidney transplantation. To date, only Hamburg-Eppendorf, Germany very few RAKT procedures in children have been described. Kidney transplant recipient *Correspondence: Anne-Françoise Spinoit patients, being immunocompromised, might be at increased risk for perioperative afspinoit@hotmail.com surgical complications, which creates additional challenges in management. Applying techniques of minimally invasive surgery may contribute to the improvement of clinical Specialty section: This article was submitted to outcomes for the pediatric transplant patients population and help mitigate the morbidity Genitourinary Surgery, of KT. However, many challenges remain ahead. Minimally invasive surgery has been a section of the journal Frontiers in Surgery consistently shown to produce improved clinical outcomes as compared to open surgery Received: 04 January 2021 equivalents. Robot-assisted laparoscopic surgery (RALS) has been able to overcome Accepted: 01 March 2021 many restrictions of classical laparoscopy, particularly in complex and demanding Published: 25 March 2021 surgical procedures. Despite the presence of these improvements, many challenges Citation: lie ahead in the surgical and technical–material realms, in addition to anesthetic and Grammens J, Schechter MY, Desender L, Claeys T, Sinatti C, economic considerations. RALS in children poses additional challenges to both the VandeWalle J, Vermassen F, Raes A, surgical and anesthesiology team, due to specific characteristics such as a small Vanpeteghem C, Prytula A, Silay MS, Breda A, Decaestecker K and abdominal cavity and a reduced circulating blood volume. Cost-effectiveness, esthetic Spinoit A-F (2021) Pediatric and functional wound outcomes, minimal age and weight to undergo RALS and effect Challenges in Robot-Assisted Kidney of RAKT on graft function are discussed. Although data on RAKT in children is scarce, Transplantation. Front. Surg. 8:649418. it is a safe and feasible procedure and results in excellent graft function. It should only doi: 10.3389/fsurg.2021.649418 be performed by a RAKT team experienced in both RALS and transplantation surgery, Frontiers in Surgery | www.frontiersin.org 1 March 2021 | Volume 8 | Article 649418 Grammens et al. Pediatric Challenges in RA Kidney Transplant fully supported by a pediatric nephrology and anesthesiology team. Further research is necessary to better determine the value of the robotic approach as compared to the laparoscopic and open approach. Cost-effectiveness will remain an important subject of debate and is in need of further evaluation as well. Keywords: pediatric kidney transplantation, kidney transplantation, pediatric robot-assisted kidney transplantation, robot-assisted kidney transplantation, robotics, robotic surgery, minimal-invasive surgery BACKGROUND pyeloplasty for an uretero-pelvic junction obstruction (Personal communication, Craig Peters, Children’s Hospital in Boston, Kidney transplantation (KT) is universally recognized as the gold 2002). Since then, surgical indications for robotics in pediatric standard treatment in the adult and pediatric populations with urology have expanded substantially. The principal robot- patients with End-Stage Kidney Disease (ESKD). assisted (RA) procedures in children are RA pyeloplasty, In contrast to the adult population, KT has taken longer RA hemi-nephrectomy, RA nephroureterectomy, RA ureteral to become an established and preferred treatment for pediatric reimplantation, RA bladder augmentation and RA Mitrafanoff patients with ESKD (1). KT offers major advantages to appendicovesicostomy (8). Because of the insufficient evidence- the pediatric population such as catch-up growth (2) and base related to the lack of randomized-controlled trials, longer survival (3).Immunosuppresive treatment increases the pyeloplasty surgery is the only procedure acknowledged by risk for perioperative surgical complications which creates the European Association of Urology Guidelines on Pediatric additional challenges in management of kidney transplant Urology as equally successful whether performed using an open, recipients. Specifically, wound-related complications have been laparoscopic or robotic approach (provided that the surgeon is shown to contribute significantly to morbidity post-transplant experienced in the chosen technique) (9). Better cosmesis, less (4). Applying techniques of minimally invasive surgery may pain and less hospital stay are the main three advantages of contribute to the improvement of clinical outcomes for the robotic surgery stated in the guidelines. pediatric ESKD population and help mitigate the morbidity Minimally invasive surgery such as laparoscopic surgery of KT. or RALS has consistently shown to produce improved The past decade has produced greatly improved KT outcomes clinical outcomes as compared to open surgery equivalents. largely due to enhanced immunosuppressive therapy, expanded These outcomes include fewer complications, reduced length living kidney donor transplantation, advances in perioperative of hospital stay, reduced need for blood transfusion, less care, better pre-transplant preparation of the recipient and postoperative pain, shorter convalescence period, fewer surgical improved surgical techniques in kidney extraction from donors. site infections, and better cosmetic results (10–12). At present, survival rates at 1-, 5- and 10-years post-transplant RALS has been able to overcome many restrictions of classical are 98, 95, and 91%, respectively (5). Survival rates are higher laparoscopy, particularly in complex and demanding surgical in recipients of living donor kidneys as compared to recipients procedures (e.g., kidney transplantation). Some major advantages of deceased donor kidneys (5). It should be noted that patient include a superb three-dimensional vision, image magnification, comfort is higher the procedure is pre-emptive, which is usually elimination of hand tremor and movement scaling, control thanks to living donor, even if cadaveric donor is possible. Pre- of the camera by the surgeon, good surgeon ergonomics to emptive grafting means the patient does not have to undergo lessen fatigue, and articulated instruments with seven degrees of dialysis, the kidney graft is achieved before the patient is in need freedom of movement (13). for dialysis. Despite the presence of these improvements, many challenges lie ahead in the surgical and technical–material realms, in addition to anesthetic and economic considerations (7, 8). ROBOT-ASSISTED LAPAROSCOPIC SURGERY CURRENT EVIDENCE Progression in robot-assisted laparoscopic surgery (RALS) has revolutionized minimally invasive surgery. Although it is The first adult robot-assisted kidney transplantation (RAKT) routinely utilized in urology, RALS has remained controversial was performed by Giulianotti et al. (14) in 2010. In 2014, since it is frequently challenging to demonstrate clear superiority Menon et al. (15) standardized the transperitoneal approach with in outcomes when compared to open or classical laparoscopic regional hypothermia maintenance during the re-warming time. surgery, whilst also being quite expensive (6). Adaptation of In the years since, RAKT has become an increasingly common RALS in children is even more hazardous than in adults as the procedure in selected high-volume centers. This can be attributed medical equipment for the procedure is produced for use in to promising results which have indicated RAKT to be a safe, adult-sized bodies (7). feasible and reproducible procedure with a potentially improved Usage of RALS in the pediatric urology population was first morbidity as compared to open kidney transplantation (OKT) described by Craig Peters’s team in 2002 after they performed a (16, 17). Frontiers in Surgery | www.frontiersin.org 2 March 2021 | Volume 8 | Article 649418 Grammens et al. Pediatric Challenges in RA Kidney Transplant However, this evidence is largely limited to adults (16, 18, two lost graft, and two deceased during follow-up. There was 19). Children are not just ‘small adults’ and must be assessed no significant observed difference in graft survival or overall within their own separate population, established results in adults survival (23). Both Modi et al. and Patel et al. (22, 23) concluded cannot be easily extrapolated to the pediatric population. To date, that RAKT is feasible and safe, however, a more thorough and RAKT experience remains limited in the pediatric population. comprehensive analysis of the specifics of their experiences could The first full case report on pediatric (8 years old child) help increase the external validity of their findings. RAKT was published in 2019 by Decaestecker and team at Ghent University Hospital, Belgium. It demonstrated that RAKT OUR EXPERIENCE in children is technically feasible and safe, and resulted in excellent graft function. Concomitant nephrectomy was done Based on our extensive experience in RALS in pediatric urology laparoscopically through the single-port GelPOINT R (AFS), (24–26) and robotic kidney transplantation surgery (16, 27, while another team retrieved the living donor kidney using 28), we decided to initiate a pediatric robot-assisted kidney robotic assistance (KDK). In order to minimize ischemia in transplantation program. For the time being, we have limited the donated kidney, the harvesting in the living donor and the program to cases of grafting performed with living donor the transplant preparation of the child were simultaneously transplants. Since the first pediatric RAKT case in 2018 (20), we performed in two operating rooms by two different transplant have operated on an additional two children with good results, teams (AFS—KDK). It should be noted that, given these and our program has continued to advance. We continue to demanding and complex aspects of the procedure, pediatric monitor our data and hope to further develop our experience in RAKT should only be attempted by an experienced RAKT team this unique field and improve patient outcomes. fully supported by a pediatric nephrology and anesthesiology team (20). DISCUSSION Recently, Bansal et al. released a comparative analysis of outcomes and long-term follow-up of pediatric RAKT with an End-stage Kidney disease (ESKD) occurs in about 5–10 children open kidney transplantation (OKT) counterpart (21). Twenty- per million each year (29). Although early pediatric KT was five patients were included in the study, 21 of whom underwent complicated by technical, immunologic, and logistic problems, OKT, and four of whom underwent RAKT. A significantly advances in these areas have led to dramatic improvements higher re-warming ischemia time was noted in the RAKT group and KT has become the preferred treatment for pediatric (21), but that may be attributable to the initial phase of the ESKD patients (1). Innovations in minimally invasive surgical learning curve for the procedure, a phenomenon which was techniques that have been successful in the adult population similarly observed in the initial phases of adult RAKT (16, 18). should be offered to children as well if the benefits are Peri-operative analgesic requirements were significantly higher comparable. Nonetheless, several considerations must first be among the OKT group as compared to the RAKT group. RAKT addressed regarding different aspects of a RAKT. complications included transplant renal artery stenosis and subcapsular hematoma, albeit not exclusive to RAKT. Despite the limitations of this study, it demonstrated that pediatric RAKT ANESTHETIC CONSIDERATIONS FOR is a feasible and safe procedure that results in excellent graft RALS function (21). In addition to these two articles, our literature search revealed Anesthetists should consider the following challenges in robotic two abstracts discussing pediatric RAKT. Modi et al. (22) surgical case: increased abdominal pressure, hypothermia, described a group of 5 children undergoing RAKT in 2013. All increased CO2 absorption, and the physiologic effects of but one kidney were issued from living donors. In two children, Trendelenburg position. These may impair cardiovascular concomitant seminal vesicle cyst excision and nephrectomy were function and ventilation, induce cerebral vasodilatation, and carried out. One child experienced spontaneous graft rupture on negatively affect urine output (30). Anesthetists should take note the 3rd postoperative day requiring emergency exploration (22). that intra-abdominal pressures lower than 10 mmHg do not A prospective non-randomized open label trial by Patel et al. (23) appear to induce any significant clinical hemodynamic effects, compared outcomes of open vs. robot-assisted pediatric KT at and pressures up to 12 mmHg seem to be well-tolerated (31). a single center, involving 60 and 22 patients undergoing RAKT and OKT, respectively. Endpoints of their trial were feasibility of SURGICAL CHALLENGES OF RALS IN RAKT and creatinine value at 30 days post-transplantation. Both CHILDREN ureteric reimplantation time and intraoperative blood loss were significantly decreased in the RAKT group. In the RAKT group The relatively small size of the abdominal cavity of a child (n = 60), five patients had slow graft function, and seven patients presents multiple operative challenges. This decreased workspace lost graft during follow-up. Two patients had acute antibody- in pediatric abdominal surgeries makes trocar placement a mediated rejection, four had chronic rejection, and one had de critical procedural component as it can impact desufflation risk, novo collapsing glomerulopathy with BKV nephropathy. Five bleeding risk, and organ damage. Poorly positioned trocars may patients from the RAKT group deceased during follow-up. In generate a gas leak, provoking rapid desufflation and further the OKT group (n = 20), two patients had slow graft function, decreasing the small workspace (32). The use of the AirSeal R Frontiers in Surgery | www.frontiersin.org 3 March 2021 | Volume 8 | Article 649418 Grammens et al. Pediatric Challenges in RA Kidney Transplant system can help to maintain a stable working space with a very (21, 37, 38). RAKT can deliver superior esthetic outcomes, which low pneumoperitoneum pressure. At our center, it was used in are especially desired for young children (21). Barbosa et al. (38) all our pediatric RAKT procedures. Bleeding can be particularly demonstrated that parents consistently perceive smaller scars dangerous in children, as their already limited circulating resulting from RALS as esthetically superior to open surgical volume causes any unrecognized or uncontrolled bleeding to be scars following pediatric urological procedures. Regardless of hazardous to cardiovascular function (32). Pediatric abdominal scarring, most parents ultimately base their choice of surgical cavities typically contain adjacent organs in tight proximity technique on superiority of clinical outcomes (38). Surgeons to each other, increasing the risk for damage to surrounding should therefore discuss differences in clinical outcomes with organs during surgical procedures. Therefore, surgeons should be their patient’s parents, in addition to the resultant scarring of aware that open placement of the first trocar under direct vision different approach modalities. (Hasson technique) is the preferred method for the pediatric To date, an eight kilograms cut-off value is the lowest weight population (33, 34). allowed for consideration of robot-assisted minimally invasive Trocar positioning is also important for maximization of surgery in children. For RAKT specifically, 8 years of age is robot dexterity within the already restricted pediatric abdominal considered to be the minimum threshold, as most transplanted cavity. The recommended 8 cm gap for collision avoidance kidneys are adult-sized kidneys which are then transplanted between the robot arms in adult RALS cases is often impossible into a smaller child. At our center, we were able to adopt the in children due to workspace space limitations. Contrary standard trocar configuration from adult RAKT to pediatric to some adult procedures, there is no standardized trocar RAKT up to a lower age limit of 8 years old. Extending to placement in robotic pediatric procedures due to broad variations younger children would necessitate further adjustment of the in weight and height which are dependent on patient age. trocar configuration, but would as well be very challenging Trocar positioning should therefore be individually adjusted or impossible due to the size of an adult-sized kidney in the to allow optimal workspace (8). It is also worth to mention particularly small pneumoperitoneum space of a small child. that the later generation robots (such as Da Vinci Xi and Therefore, 8 years of age is currently considered to be the X) facilitate the docking procedure related to easy connection minimum threshold for RAKT. of instruments and the increased movement ability of the As the length of the incision in open surgery in smaller patient cart. children is limited, there is discussion whether this population Additionally, while most robotic adult procedures involve would benefit from this approach. While RA laparoscopic four robot arms, the limited workspace in pediatric patients approach can provide better visualization with decreased commonly only allows usage of three out of four robot arms inflammatory reaction and wound tension, opponents argue (camera port and two robotic ports) without any additional 5- that incisions for open surgery are already small in size and mm assisting port (8). In our initial phase of RAKT in children, that the sum of laparoscopic incisions equals the total length our team opted for four robot arms with two assisting ports of an open incision (8, 39). However, this argument assumes (the standardized adult port position) to limit operative time and that surgical morbidity is proportional to the sum of several more specifically to limit the (re)warm(ing) ischemia time, as incisions. However, morbidity has already proven to be a linear these factors are potentially associated with adverse long-term function of the tension present across the incision. As calculated patient and graft survival outcomes (35). by Blinman (37), an open incision is consistently subject to more total closing tension than any combination of trocar incisions of equal total length. By decreasing wound tension, there is an ECONOMIC CONSIDERATIONS important reduction in pain and morbidity (risk of dehiscence, hernia or infection) (37). Current studies have not found RALS to be cost-effective (6). It has been suggested that RALS may prove cost-effective in high-volume centers with at least 349 annual interventions (36). Therefore, cooperation between pediatric and adult urology units TRAINING AND EXPERIENCE might be necessary as the volume for pediatric urology RALS In order to start a pediatric RAKT program, a team of surgeons is not as high as it is in adults (8). RALS may become more experienced both in RALS and kidney transplantation surgery, cost-effective as more experience is gained, leading to improved along with the full support of a pediatric nephrology and outcomes and reduced length of hospital stay. This issue remains anesthesiology team, is recommended. Even during the training to be further evaluated. phase of learning how to perform RAKT, the safety of the Figure 1, also published in a previous paper of our group procedure and optimal graft survival should be guaranteed. (8), provides a diagrammatic overview of the main challenges in According to Decaestecker et al. (27), it cannot be emphasized adapting the robotic platform to children. enough that a high level of robotic experience is recommended before initiating a RAKT program. Training the technique on OUTCOMES both dry and wet lab models is mandatory (27). The only structured RAKT course, provided at ORSI Academy (Melle, The differences in both the esthetic and functional outcomes Belgium) (40), is recommended. And additional structured of RAKT as compared to OKT must not be underestimated RA pediatric course is available at the same place, and is Frontiers in Surgery | www.frontiersin.org 4 March 2021 | Volume 8 | Article 649418 Grammens et al. Pediatric Challenges in RA Kidney Transplant FIGURE 1 | Challenges to be encountered when adapting the robotic platform to infants. highly recommended. In conjunction with an experienced RAKT (43). The potential damage to the graft as a result proctor supporting first cases, a safe introduction of this new of pneumoperitoneum is not yet fully known, and a technique is possible (16, 27, 41, 42). correlation between operative time (and thus exposure to pneumoperitoneum) and graft function in adult RAKT has not yet been identified (16). Aside from the anesthetic concerns SPECIFICS REQUIRING SPECIAL regarding intra-abdominal pressure, this might be another ATTENTION IN PEDIATRIC RAKT reason to keep intra-abdominal pressure around 10 mmHg or lower. We prefer a stable low pneumoperitoneum pressure of Warm ischemia time has already been shown to be a negative 8 mmHg for the (RA) laparoscopic living donor nephrectomy predictive factor of long-term patient and graft survival outcomes and for RAKT as of the moment of reperfusion to mitigate (35). In the adult RAKT series, a wide range of ischemia times any potential adverse influence of higher pneumoperitoneum has been described, but no correlation has been found between pressures in donor and/or recipient (44, 45). rewarming time and graft function (16, 17). To reduce potential damage after prolonged warm ischemia times, Menon et al. have reported a new technique for regional hypothermia with ice slush during vascular anastomosis (15). COMPLICATIONS AND LENGTH OF Contrary to the adult RAKT procedure, in pediatric RAKT HOSPITAL STAY the graft renal vessels are anastomosed to the common iliac vessels instead of the external iliac vessels, in order to match the Differences regarding complications and length of hospital stay vessel size of the donor (adult-sized renal vessels) and acceptor after RAKT as compared to OKT are still subject to debate. (pediatric-sized iliac vessels) (20, 21). To date, RAKT in children remains in the initiation phase. A It should be noted that according to the literature, renal larger patient database could lead to more valuable conclusions. blood flow and function are reduced in the presence of A randomized controlled trial comparing outcomes of RAKT and pneumoperitoneum, potentially leading to graft impairment OKT should provide the best level of evidence. Frontiers in Surgery | www.frontiersin.org 5 March 2021 | Volume 8 | Article 649418 Grammens et al. Pediatric Challenges in RA Kidney Transplant CONCLUSION AUTHOR CONTRIBUTIONS Although data on RAKT in children is scarce, it is a JG was the main author and carried out literature search. KD safe and feasible procedure and results in excellent graft and A-FS performed the initial surgery reported in Spinoit function. It should only be performed by a RAKT team et al. (20). A-FS initiated the scientific project and develops experienced in both robot-assisted laparoscopic surgery the pediatric robotic program of minimally invasive surgery. and transplantation surgery, fully supported by a team KD initiated the scientific and develops the surgical robotic of pediatric nephrologists and anesthesiologists. Further kidney transplantation program in Ghent. AB and MS are research is necessary to better determine the value of the promotors of the international robotic programs, respectively robotic approach as compared to the laparoscopic and open for Kidney transplant and for pediatric urology. They critically approach. Cost-effectiveness will remain an important revised the manuscript and approved the submitted version. subject of debate and is in need of further evaluation All authors from Ghent are part of the pediatric uro- as well. nephrology team making the development of the program possible and critically revised the manuscript and approved the submitted version. DATA AVAILABILITY STATEMENT FUNDING The original contributions generated for this study are included in the article/supplementary material, further inquiries can be MS was fully supported by the Gianni Eggermont Fund for directed to the corresponding author/s. advancement of research in pediatric Urology. REFERENCES 14. 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Frontiers in Surgery | www.frontiersin.org 7 March 2021 | Volume 8 | Article 649418