a publication of the Swiss College of Surgeons

Focus

ICG-FS in minimal invasive pediatric surgery

Indocyanine Green Fluorescence-guided surgery is becoming an increasingly helpful tool in pediatric minimal invasive surgery. Recently, an international panel of 15 pediatric surgeons from 9 countries was assembled in order to create a consensus statement upon the utility of ICG-FS in various pediatric surgical applications, primarily focusing on its evidence base, safety, indications, use across different surgical specialties and dosing strategies.

Authors
Szavay Philipp
Prof. Dr. med. Philipp Szavay
Rentea Rebecca
MD Rebecca Rentea

Methods:

An international panel of 15 pediatric surgeons from 9 countries went through a structured process consisting of a rapid scoping review, iterative discussion sessions, mixed-methods studies with key stakeholders, and voting rounds on individual statements to create draft consensus statements.

Results:

100 articles were identified during the review and summarized by application. Based on this condensed evidence, consensus statements were generated after 3 iterative rounds of anonymous voting. Key areas of agreement were quality of evidence, the safety of ICG, pediatric surgical indications, utilization per surgical specialty, and dosing of ICG.

Conclusion:

This consensus statement aims to guide healthcare professionals in managing ICG-SF use in pediatric surgery based on the best available evidence, key stakeholder consultation, and expert opinions. Despite the promising potential of ICG-FS, the need for higher-quality evidence, prospective trials, and safety studies is underscored. The consensus also provides support for pediatric surgeons to facilitate the application of ICG-FS.

Key words: indocyanine green fluorescence, tissue perfusion, immunofluorescence, pediatric surgery, fluorescence-guided surgery

Introduction

Indocyanine Green (ICG) is a water-soluble, tricarbocyanine with a high binding affinity to plasma proteins and excitation and emission spectra in the near-infrared (NIR) range1,2.

ICG-fluorescence imaging (ICG-F) applications have expanded to various surgical fields, including oncological surgery, neurosurgery, and gastrointestinal surgery. It aids in intraoperative visualization, tissue perfusion assessment, and lymphatic mapping.

The evidence base for ICG-F use in pediatric surgery is primarily built on small-scale, retrospective studies, highlighting the need for high-quality, prospective research to confirm its potential and explore new applications3. While ICG-F is very promising, it remains unclear whether its use improves surgical outcomes in the pediatric population.

The assembled consensus group proposed a set of guidelines for using ICG-F in pediatric surgery.  Central issues such as the quality of current evidence, safety of ICG, specific pediatric indications, application across surgical specialties, and dosing strategies are addressed. We hypothesize that ICG-F can facilitate surgical procedures, improve decision-making, and decrease complications in pediatric surgery. This consensus statement offers clinicians, researchers, and surgeons an authoritative reference point for using ICG-F in pediatric surgery.

Methods

Literature Review

PubMed was systematically searched via a scoping review (intended to map the existing literature on a specific topic quickly)4–6 for articles on the use of ICG-F in pediatric surgery.  The review aimed to identify, categorize, and summarize relevant publications to provide insights into current practices, clinical outcomes, and gaps in the existing body of evidence. Standardized data extraction forms were used across all topics. A uniform Excel database template for entering the data extracted from the selected papers was provided to all participants.

Development of the Consensus Process

The methods for developing our pediatric surgery consensus statement involved a three-round Delphi process with 15 expert pediatric surgeons, each with over 5 years of post-qualification experience, selected via snowball and purposive sampling.

The Internal Review Board approved the study (IRB- 00002938). Initially, panelists responded to questions based on their professional expertise and stakeholder input (Supplement 2). The second round involved reviewing the literature to determine clinical consensus needs and address discrepancies. Panelists reviewed these findings to agree upon or adjust recommendations.

Panelists voted on each consensus statement via a RedCap™ survey, expressing agreement, disagreement, or neutrality. The process repeated until at least 80% agreement was achieved on each statement. Recommendations surpassing this threshold are reported,

Each article reviewed was assigned a level of evidence using the original Center for Evidence-Based Medicine levels (http://www.cebm.net/ocebm-levels-of-evidence/) and graded as 'strong', 'weak', or 'no recommendation' according to the GRADE system. Statements with sufficient data received a grade of recommendation (GoR)7.

Results and Consensus Recommendations

Quality of Evidence

The initial search identified 558 titles, from which 77 abstracts were screened, 46 were located by additional methods, and 100 full-text papers were reviewed.  The included studies are diverse, comprising 41 case reports, 18 case series, 21 retrospective studies, 13 prospective studies, and 7 others of various types.  The panel unanimously agreed on the need for high-quality research and standardized ICG-F results reporting.

Safety of ICG

In the pediatric population, in a combined study of 75 (45 receiving ICG-F) patients evaluating gastrointestinal perfusion, no complications were noted9. A recent Pediatric Health Information System database study of ICG-F in pediatrics between 2016 and 2021 in 1270 cases across 38 participating hospitals demonstrated no adverse events10. Of the 100 articles reviewed, 44 did not provide any safety information, and 56 articles reported no ICG-related complications except two cases of temporary skin color change from dermal ICG administration11,12.

Regarding the safety profile ICG-F utilization has demonstrated a favorable safety profile, including very young/small patients with rare allergic reactions. However, data on pediatric safety reporting remains limited. We recommend strongly that ICG-F has a positive safety record.

Indocyanine Green Fluorescence in Pediatric Surgical Applications

ICG-F continues to have an expanded role in pediatric surgery, enhancing real-time visualization across applications such as tumor visualization, perfusion assessment, visual assessment of anatomical structures, and lymphatic mapping, among other clinical utilities.

Tumor Visualization and tumor margin identification

In tumor visualization and margin identification, 22 articles highlighted the efficacy of ICG-F for both primary and metastatic tumors13–34. ICG-F’s application in malignancies like bone tumors, soft tissue sarcomas, and Wilms tumor is still being evaluated. For oncologic procedures, ICG-F typically involves a larger dose of ICG given 24 hours or more beforehand, capitalizing on the "enhanced permeability and retention effect" where dye washes out from normal tissues but remains in tumor tissues during this “second window.” Notably, Harris (2023)20 reported the safe and effective use of ICG in minimally invasive surgery for pediatric oncology, and Kitagawa (2015)21 highlighted its efficacy in identifying hepatoblastoma pulmonary metastases. Shen's study (2023)25, analyzing 23 pediatric hepatoblastoma resections using ICG-F, found the technique invaluable for margin identification and reducing residual tumor risk. Thus, efficacy in Tumor Visualization ICG-F can significantly enhance the visualization of  hepatic tumors, especially in metastatic settings, and play a pivotal role in delineating tumor margins.

The effectiveness of ICG-F for bone tumors, soft tissue sarcomas, and Wilms tumor remains under evaluation. ICG-F is both safe and effective in minimally invasive surgeries for pediatric oncology patients. ICG-F is an encouraging, emerging technology for tumor visualization and margin identification in pediatric oncological surgery. ICG-F significantly improves tumor visualization in hepatic and hepatoblastoma settings. Its efficacy for visualization of other tumors is more variable and remains under investigation. A more robust evidence base achieved through rigorous scientific research is needed to confirm these preliminary findings and to guide its integration into clinical practice protocols. ICG administration timing is based on the difference in the assessment goal desired (perfusion vs. retention).

Perfusion Assessment

In 31 articles, ICG-F effectively assessed tissue for bowel, esophagus, abdominal wall, skin flap etc. perfusion35–63. Through monitoring ICG-F, surgeons identified compromised perfusion, enabling timely interventions to reduce ischemic risks. Le-Nguyen et al. (2023)51 conducted a prospective study of 28 pediatric intestinal resections using ICG-F, including 14 patients from the NICU. They found that ICG-F may impact bowel resection sites by improving perfusion assessment and demonstrated a very favorable safety profile, even for very small patients. ICG-FA is a potential intraoperative tool for real-time tissue perfusion assessment, current non-randomized data supports ICG-FA's safety and efficacy in pediatric surgeries. Still, robust randomized trials are essential to determine if this impacts complications such as rates of anastomotic leak or stricture.

Visualization Enhancement

ICG-F enhances intra-operative visualization, aiding surgeons in identifying key structures such as anatomic structures, vessels, and tumors (Table 2). Of 28 articles that were identified11,64–86, seven were prospective clinical studies.  Esposito et al. compared laparoscopic partial nephrectomy with and without ICG-F in 40 patients, finding that clearer vessels and renal visualization reduced operative time71. Esposito et al. (2020)87 confirmed ICG-F imaging effectiveness and safety in pediatric minimally invasive surgery for abdominal lymphoma and ovarian tumors. A review by Esposito et a. (2022) showed that ICG-F enhances surgical visualization in urologic oncology procedures, particularly through tumor inverse pattern of ICG-F visualization (hypo visualization of tumors).  Therefore, ICG-F enhances visualization in pediatric surgery via contrasting tissues, enhancing the visibility of vessels, anatomic structures, and tumors. Preliminary findings suggest ICG-F's may reduce operative time and complications related to anatomic visualization.

Lymphatic System and Lymphatic Mapping

Lymphatic mapping is essential for staging and surgical management in certain pediatric malignancies but carries morbidity. 16 articles described lymphatic drainage pathway mapping facilitated by ICG-F, aiding in the identification and excision of sentinel lymph nodes12,26,47–49,64,88–97. ICG-F reduced unnecessary lymphadenectomies and related complications.  Jeremiasse et al. (2023)91 reported ICG-F’s feasibility for imaging the sentinel lymph node during pediatric melanoma, squamous cell carcinoma, or sarcoma cases, noting superior detection rate and accuracy. Kato et al. (2019)92, studied lymphatic malformations and found ICG-F useful in identifying and guiding the treatment of lymph flow patterns in refractory lymphatic malformation.  Mansfield et al. (2020)93 compared the outcomes of retroperitoneal lymph node dissection (RPLND) for para testicular rhabdomyosarcoma concluding that a retroperitoneoscopic approach, combined with ICG-F enhanced outcomes. Thus, ICG-F-assisted lymphatic mapping is a promising tool in enhancing the surgical approach to pediatric malignancies. Existing literature affirms the safety and effectiveness of ICG-F for sentinel lymph node detection, but comparative prospective trials are required to ascertain ICG-F's advantage over conventional techniques. Implementing ICG-F for lymphatic mapping may diminish complication risks by obviating certain lymphadenectomy s and enabling precise lymph node operations. ICG-F may be applicable for congenital lymphatic malformation resection cases.

Fluorescence Cholangiography    

In total, 23 articles describing the application of ICG-F in hepato-pancreato-biliary surgery17,23,25,28,29,31–33,37,41,50,65–67,73–75,77,78,84,86 covering procedures such as laparoscopic cholecystectomy, Kasai procedure, and partial hepatectomy.  Calabro et al. (2020)66 studied the effects of ICG-F cholangiography (ICG-FC) during laparoscopic cholecystectomy in 50 pediatric patients, finding it safe and effective for biliary tree identification.  Esposito et al. published two retrospective studies in 2019 and 202267,72. The first analyzed 215 children’s long-term outcomes after laparoscopic cholecystectomy, showing its long-term safety and effectiveness. The 2022 study on 43 patients compared standard laparoscopic cholecystectomy to ICG-FC cholecystectomy. ICG-FC enhanced visualization and reduced specific operative step time, but overall operative time and hospital stay were insignificant between the comparative groups.  ICG-F is a safe and potentially effective instrument for a range of hepatobiliary operations within the pediatric population. ICG-F may even become mandatory for standard procedures such as cholecystectomy.

Pediatric colorectal and pelvic reconstructive surgery

ICG-F is increasingly utilized in pediatric colorectal and pelvic reconstruction surgeries46,54,59,63, aiding in repairs like anorectal malformations, Hirschsprung disease, and complex reoperations. It proves useful for evaluating tissue perfusion in structures such as the neovagina and colon and is crucial in re-operative fields for assessing pedicle viability. In Hirschsprung disease, ICG-F assesses visualizing colonic derotation and selecting vessels for division57. Clinical findings in adult colorectal surgeries demonstrate that ICG-F enhances surgical quality and reduces complications98. While one must be cautious extrapolating findings to pediatrics, ICG-F was demonstrated as safe and feasible in intestinal resections, with positive feedback from the surgical team, suggesting improved visualization and patient outcomes51. ICG-F has demonstrable efficacy in enhancing surgical visualization and decision-making in pediatric colorectal and pelvic reconstructive surgeries for viability of bowel pedicles and anastomotic perfusion. Extrapolation from adult data suggests similar benefits in pediatric settings, however, this requires more validation.

Pediatric Urological Surgeries and the Role of ICG-F

Ten studies examined the utility of ICG-F in pediatric urological procedures13,35,56,67,69,71,83,99,100. ICG-F was employed in lymphatic sparring varicocele repairs, various renal surgeries (partial and total nephrectomies and renal cyst unroofing), ureteral mapping, and evaluating vascular and tissue perfusion for living-donor kidney transplantation. It has also been utilized in complex duplex renal surgeries, retroperitoneal lymph node dissections, and to define the ureter during tumor resections (ICG-F applied cystoscopically). Esposito et al. (2020)69 detailed 57 urological procedures, including 41 varicocele repairs featuring intraoperative lymphography and 16 renal surgeries. Intravenous injection of ICG was used for renal procedures, whereas intra-testicular injection was employed for varicocele repairs, resulting in visualization within 30-60 seconds after injection. The study confirmed ICG as a reliable tool for improving visualization in pediatric urology. ICG-F is a safe and effective tool for visualizing anatomical and vascular structures in pediatric urological surgeries. It proves essential for renal surgeries, ureteral mapping, and varicocele repairs with lymphography. Intravenous or intra-testicular ICG administration results in rapid visualization, enhancing surgery outcomes.

Pediatric Neurosurgical Applications of ICG-F

Ten studies examined ICG-F’s role in pediatric neurosurgical procedures15,30,44,45,58,60,60,80,82,85. ICG-F enhances the visualization and localization of cerebral lesions and maps vascular structures during operations, including tumor resections and arteriovenous malformation surgeries. Lehner et al. (2023)101 demonstrated ICG-F's ability to visualize the basilar artery during an endoscopic third ventriculostomy for an infant with congenital hydrocephalus.  Horie et al. (2014)45 evaluate the utility of ICG video angiography (ICG-VA) in 50 patients to assess postoperative hyperperfusion in Moya Moya and atherosclerotic disease cases. They found that ICG-VA provides real-time cerebral blood flow data and helps identify patients at risk for postoperative hyperperfusion. Tanabe et al. (2017)82 studied 19 patients (8 pediatric) and demonstrated ICG-F’s efficacy in visualizing the middle meningeal artery before craniotomy for Moya Moya disease. ICG-F is an instrumental tool in pediatric neurosurgical applications, playing a significant role in enhancing visualization, delineating cerebral and vascular structures, and tissue perfusion. The technology demonstrates utility in intraoperative applications, contributing significantly to the safety and efficacy of complex procedures. Evidence from prospective studies suggests that ICG-F can provide real-time information crucial for surgical decision-making in intricate vascular neurosurgical diseases like MMD.

Thoracic

Sixteen articles in the review discussed the utility of ICG-F in pediatric thoracic surgery11,13,16,18–22,28,31–34,81,102,103 covering thoracoscopic tracheoesophageal fistula surgery, tumor resections, lung metastasectomies, and congenital cardiac surgery, thoracoscopic vascular ring surgery, and thoracoscopic repair of chylothorax. A prospective study by Abdelhafeez et al. (2023)14 investigated ICG-F’s efficacy in localizing metastatic pulmonary nodules in pediatric patients with solid tumors. Of the 50 patients with a total of 63 pulmonary nodules, ICG-F accurately detected 75% of positive nodules, falling short of the 90% accuracy goal. Notably, while pre-operative CT missed 26% of nodules linked to primary liver tumors, ICG-F was sensitive to them. The study advocated for further ICG-focused trials and measured use of ICG-F based on tumor histology.  The study also suggested the cautious application of ICG-F imaging in patients with non-hepatic tumor metastases, depending on the tumor histology. ICG-F has demonstrated utility in many pediatric thoracic surgical interventions. ICG-F has a 75% accuracy for metastatic pulmonary nodules, without meeting the predefined target accuracy rate of 90%, but picks up 26% of preoperative CT missed nodules from hepatic solid tumors.

We recommend ICG-F, which has shown promise in various applications in pediatric thoracic surgery. However, its limitations in the context of nodule detection indicate a need for further prospective clinical trials using accepted standards for assessment and validation. The most reliable is solid hepatic tumor metastasis.

Additional Surgical Applications of ICG-F

The utility of ICG-F has been reported in various other surgical domains, including head and neck surgeries24,42,43, orthopedics36,38,39, endocrinological interventions, and plastic and reconstructive surgeries52. The limited breadth of the literature presents a pressing need for more research to assess the efficacy and safety of ICG-F in these surgical fields.

ICG-F dosing: Current Landscape and Challenges

Considerable variations in ICG-F dosing protocols emphasizing the absence of uniform reporting standards. According to the product guidelines from a recognized ICG distributor[1], the following maximum daily dosing parameters are recommended: Adults and Elderly: Up to 5 mg/kg of body weight. Adolescents (11-18 years): Up to 5 mg/kg of body weight. Children (2-11 years): Up to 2.5 mg/kg of body weight. Infants (0 months to 2 years): Up to 1.25 mg/kg of body weight.

However, most research articles advocate a more conservative daily dose of 0.6 mg/kg of ICG. A notable exception is the study by Abdelhafeez et al. (2022)104, which prescribes up to  1.5 mg/kg. Some use higher doses for non-liver lung metastasis of 4mg/kg. The optimal dosing standard protocols still need to be determined due to robust, evidence-driven research scarcity. The panel unanimously agrees that a weight-based dosing methodology appears most appropriate currently.   However, ideal dosages may be contingent upon specific surgical procedures and individual patient characteristics.

Limitations

The consensus process highlighted several limitations: the diversity in study designs and lack of large-scale trials limit the strength of the evidence. Moreover, the variability in ICG-F dosing protocols across the literature points to the necessity for standardized guidelines. These limitations underline the preliminary nature of the consensus and the need for ongoing evaluation as further evidence emerges.

Conclusion

In summary, this consensus statement on ICG-F use in pediatric surgery aims to serve as a foundational reference that highlights its potential benefits. While promising, the current evidence remains scarce and calls for further investigation to establish comprehensive, evidence-based guidelines. The collective expert opinion, nevertheless, recognizes ICG-F as a valuable tool in pediatric surgical practice, with the potential to substantially elevate the standard of care.

Acknowledgements:

Keri Swaggart, Children’s Mercy – Kansas City Librarian

Marc Harms, Stryker Endoscopy, Stryker Nederland BV, Amsterdam, CM 1101, Netherlands.

Manuscript on behalf of the expert consensus group: Alex Bondoc, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA; Ciro Esposito, Federico II University Hospital, Naples, Italy; Seth D. Goldstein, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA; Grzegorz Kowalewski, Children's Memorial Health Institute, 04-730 Warsaw, Poland; Timothy B. Lautz, Ann & Robert H. Lurie Children's Hospital of Chicago, Chicago, IL, USA; Manuel Lopez, Val d'Hebron Maternity and Children's Hospital, Barcelona, Spain; Max Pachl, Birmingham Women's and Children's NHS Foundation Trust, University of Birmingham, UK; Samir Pandya, University of Texas Southwestern Medical Center, Dallas, Texas 75235, USA; Nelson Piché, Université de Montréal, Montréal, Québec, Canada ; Steven S. Rothenberg, Rocky Mountain Hospital for Children, Denver, CO 80205, USA; Jetske Ruiterkamp, Wilhelmina Children's Hospital, University Medical Center Utrecht, Utrecht, EA 3584, Netherlands; Stefan Scholz, UPMC Children's Hospital of Pittsburgh, University of Pittsburgh, Pittsburgh, Pennsylvania, USA;  Benjamin Zendejas, Boston Children's Hospital, Boston, MA, USA.

The manuscript provided represents a shortened version of the original manuscript submitted to the Journal of Pediatric Surgery in January 2024 by Rebecca M. Rentea as corresponding author currently being under review and thus not representing an original article. 

[1] https://diagnosticgreen.com/row/product-information/ [29.Sept.2023]

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