Abstract
PURPOSE
Damage to the cardiac conduction system is a major risk of congenital cardiac surgery. Localization of the conduction system is commonly based on anatomic landmarks, which are variable in congenital heart diseases. We introduce a novel technique for identification of conduction tissue regions based on real-time fiberoptic confocal microscopy.
DESCRIPTION
We developed a fiberoptic confocal microscopy–based technique to document conduction tissue regions and deployed it in pediatric patients undergoing repair of common congenital heart defects. The technique applies clockface schematics for intraoperative documentation of the location of conduction tissue regions.
EVALUATION
We created clockface schematics for 11 patients with ventricular septal defects, 6 with tetralogy of Fallot, and 10 with atrioventricular canal defects. The approach revealed substantial variability in the location of the conduction system in hearts with congenital defects. The clockface schematics were used to create plans for subsequent surgical repair.
CONCLUSIONS
The clockface schematic provides a reliable fiducial system to document and communicate variability of conduction tissue regions in the heart and applies this information for decision-making during congenital cardiac surgery.
TECHNOLOGY
Congenital heart disease is the most common type of birth defect. Approximately 32 000 new cases of congenital heart disease occur in the United States per year, and there are approximately 1.5 million new cases worldwide.1–3 More than 30 000 pediatric cardiac operations are performed each year in the United States to repair the defects, and congenital heart surgery in the neonatal period is the state-of-the-art approach to repair heart defects.4,5 Current emphasis is on the complete repair of congenital cardiac defects in infancy. A complication associated with surgical repairs of congenital heart disease is the disruption of the cardiac conduction system. This disruption can result in incomplete or complete heart block as well as bundle branch block. Conduction abnormalities such as dysfunction of sinoatrial and atrioventricular conduction pathways require chronic cardiac rhythm management using implantable pacemakers.6
A key strategy to avoid these complications is intraoperative localization of the cardiac conduction system, which is commonly based on anatomic landmarks established in histologic studies.7 Other strategies for locating the conduction system are based on technologies such as electrical impedance measurements, electrocardiography, and, recently, fiberoptic confocal microscopy (FCM).8 Despite the development of these technologies used in the surgical correction of these defects, identifying the location of the conduction tissues has been challenging because of the anatomic variation of these tissues in congenitally deformed hearts.
Here we introduce a technique to map conduction tissues adjacent to congenital heart lesions before surgical repair in pediatric patients with congenital heart defects. The technique is based on state-of-the-art FCM of tissue microstructure for the identification of tissue types. Although prior studies demonstrated that FCM provides real-time information on tissue microstructure,9 there have been no systematic means to communicate the location of conduction tissue aside from the anatomic relationship to adjacent structures. In this study we developed a clockface schematic to document the microstructural arrangement during repair of ventricular septal defects (VSDs), atrioventricular canal (AVC), and tetralogy of Fallot (TOF) for training, research, and the medical record.
TECHNIQUE
We designed clockface schematics to collate information related to the location of conduction tissue in children undergoing surgery for repair of VSDs, AVC, and TOF. The schematic was adapted for the different lesions while keeping the coronary sinus in a uniform region of the clockface. These schematics with the tricuspid valve and coronary sinus in view provide a common surgical perspective for these 3 types of congenital heart defects. In addition the clockface schematics illustrate these defects through the exposure used to perform the repair.
We applied previously developed methodology to discriminate between conduction tissue regions and regular working myocardium in the hearts of pediatric patients based on differences in tissue microstructure.9 The methodology uses a commercial FCM system (Cellvizio 100 series; Mauna Kea Technologies, Paris, France) with a GastroFlex UHD miniprobe in combination with fluorescein (Fluorescite 10%; Alcon Laboratories Inc, Fort Worth, TX). The miniprobe imaged tissue with a 240-μm diameter field of view at 65-μm depth, 1.8-μm lateral resolution, and 9-Hz frame rate.
A recent clinical trial established a clinical protocol for FCM usage and demonstrated the safety of the FCM imaging protocol.10 The trial was performed in compliance with the requirements of the US Food and Drug Administration and Boston Children’s Hospital policies. The trial was approved by the US Food and Drug Administration and institutional review board (IRB-P00031701) and registered at ClinicalTrials.gov (NCT04017975), which provides information on the study design and patient population.
In short, after cannulation and cardioplegic arrest the defect was exposed in the standard fashion through atriotomy or ventriculotomy. The surgeon then applied the fluorescein dropwise to the heart tissue and used the imaging miniprobe in the region of interest by holding the miniprobe with fingers or forceps. Fluorescein was diluted to 1:1000 in phosphate-buffered saline and served as a fluorescent marker of the extracellular space. In most cases 0.1 to 0.2 mL of the fluorescein solution was used. Once a region of interest was located, the surgeon used voice commands to signal the FCM operator when to begin and end the recording of image sequences. The surgeon called out the clockface location and tissue arrangement to record the information on the schematic. The surgeon continued imaging around the tissue region covering relevant sections in the clockface. After surveying the region of interest and recording the tissue types and locations, the completed clockface schematic was consulted, and subsequent surgical decisions were made in part based on the tissue type identification and clockface location.
CLINICAL EXPERIENCE
We applied the approach to 11 pediatric patients with VSDs, 10 with AVC, and 6 with TOF. The FCM miniprobe was maneuvered around lesion sites with cardiac microarchitectural features identified according to the positions on the clockface schematic (Figure 1A). Imaging time including creation of the clockface schematics averaged 4 minutes, 37 seconds for VSDs; 4 minutes, 5 seconds for AVC; and 3 minutes, 51 seconds for TOF. Overall the average imaging time was 4 minutes, 15 seconds. FCM images and associated positions are shown in Figure 1B. The intraoperative mapping shows an area with features consistent with conduction tissue.
FIGURE 1.

Intraoperative identification of conduction tissue regions using fiberoptic confocal microscopy. (A) View of the pediatric heart surgical site from the surgeon’s head camera. The imaging probe is held by the surgeon’s fingers, stabilized with forceps, and placed on the region of interest. The faint blue coloration at the probe tip is light from the laser. (B) Clockface schematic with sites marked for imaging with example images taken from clockface regions 1 to 4 o’clock. Striated patterns at 1, 3, and 4 o’clock indicate the tissue in this region is working myocardium and the region safe for operative procedures. The pattern taken at the 2 o’clock position is irregular and reticulated, indicating a nodal tissue region, which should be avoided in surgical procedures.
Examples of the clockface schematics for VSD, AVC, and TOF are shown in Figures 2A, B, and C, respectively. The schematics were superimposed over the drawing of the surgical repair site to provide a common polar coordinate system. We used the clockface schematic to document the location of conduction tissue regions around different lesions. We noted substantial variability in the location of conduction tissue in these relatively simple cardiac defects as noted in Figures 3A, B, and C for VSD, AVC, and TOF, respectively. Conduction tissue was noted in the expected location (3-4 o’clock position) in some patients; however a significant number of patients had conduction tissue in unexpected locations, as illustrated in Figure 3.
FIGURE 2.

Clockface schematics for surgical repair of (A) ventricular septal defects (VSDs), (B) atrioventricular canal (AVC), and (C) tetralogy of Fallot (TOF). Viewing directions are through the right atrium in A and B and from the right ventricle in C. In VSD and TOF the clockface is superimposed onto the crest of the defect where the imaging was performed. In AVC the imaging is performed near the CS and interventricular septum, which is considered the 12 o’clock position. (Ant, anterior; AVN, atrioventricular node; CA, caudal; CB, conduction bundle; CE, cephalic; CS, coronary sinus; LBB, left bundle branch; Post, posterior; TV, tricuspid valve.)
FIGURE 3.

Tissue type mapping on the clockface schematic during surgical repair of (A) ventricular septal defects, (B) atrioventricular canal , and (C) tetralogy of Fallot for 11, 10, and 6 patients, respectively. Each patient’s mapping is stacked radially in concentric rings in increasing order of patient number . Mapping of the working myocardium and the conduction tissue region is indicated in green and red, respectively. Each arc describes the mapping for a single patient.
After full annotation of the clockface schematic, the surgeon created a surgical plan for subsequent repair to avoid the FCM-identified conduction regions in and around the lesion site. This concept is illustrated in Figure 1B. The repair was performed in such a way that the VSD patch was sewn away from this region of interest. Postoperatively these patients were noted to have intact conduction with no need for permanent pacemaker implantation in the postoperative period.
COMMENT
In this study implementation of clockface schematics based on intraoperative FCM during pediatric cardiac surgery for congenital heart defects was introduced and evaluated. FCM was used to survey conduction tissue regions in arrested hearts. We based these clockface schematics on the common surgical approaches to these defects, thus making them translatable to these repairs in general. The clockface schematics helped to communicate the precise location of conduction tissue around the lesion of interest. With this information in hand the surgical team made necessary adjustments to the reparative procedure to minimize injury to the cardiac conduction system. The use of the FCM system to identify the myocardial microarchitecture provides the surgeon with a map of the conduction regions and facilitates subsequent repair. In addition to helping identify the tissue microarchitecture, conduction tissue mapping can also help increase surgeon confidence during the procedure. The FCM system can be effective in surgical correction of complex lesions like transposition of the great arteries and double-outlet right ventricle and left ventricular outflow tract obstruction where risk of conduction tissue injury is high.
Eight surgeons at Boston Children’s Hospital in Boston, Massachusetts were trained in the use of this system and the clockface schematic for intraoperative decision-making. The inclusion of this tissue identification system was not believed to be burden-some to the operative procedure, and the surgeons quickly became facile with the use of the system. The surgeons uniformly believed the additional information helped them perform the procedure with more confidence about avoiding the conduction tissue.
Limitations of the described approach include estimation of imaging locations within the polar coordinate system of the clockface schematics and subjective identification of tissue types from FCM images by the surgeon. A further limitation is a need for an operator to annotate the clockface schematic. Of note, there are opportunities to automate the clockface schematics using technologies such as 3-dimensional tracking systems and automated tissue identification previously developed by us.9
In summary, clockface schematics created from intraoperative microscopic imaging of heart tissues allow surgeons to systematically describe and effectively communicate the location of conduction tissue regions. We suggest that the schematics will guide surgeons in decision-making for avoiding injury to conduction tissues and provide a foundation for the development of novel intraoperative methodologies.
FREEDOM OF INVESTIGATION
Clockface schematics were developed by the authors. The authors had full control of the study design, methods, outcome parameters, data analysis, and production of the written report.
FUNDING SOURCES
This work was supported by a grant from the National Institutes of Health (R01 HL135077). The authors also received funding from the National Institutes of Health (R56 HL128813, R01 HL135077, and R13 HL160044) and support from the Nora Eccles Treadwell Foundation.
DISCLOSURES
Drs Kaza, Sachse, and Hitchcock have been granted patents and are applying for patents associated with techniques discussed in this article.
Footnotes
DISCLAIMER
The Society of Thoracic Surgeons, The Southern Thoracic Surgical Association, and The Annals of Thoracic Surgery neither endorse nor discourage the use of the new technology described in this article.
OPTIMA Trial Investigators: David Hoganson, MD, Eric Feins, MD, Michael Kwon, MD, Christopher Baird, MD, Francis Fynn-Thompson, MD, Sitaram Emani, MD, Luis Quinonez, MD, and Douglas Mah, MD. The authors thank Mrs Kai-Ou Tang for preparing the congenital defect illustrations in Figures 2A–C.
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