3D vs. 2D simulated fetoscopy for spina bifida repair: a quantitative motion analysis

3D imaging technology is becoming more prominent every day. However, more validation is needed to understand the actual benefit of 3D versus conventional 2D vision. This work quantitatively investigates whether experts benefit from 3D vision during minimally invasive fetoscopic spina bifida (fSB) repair. A superiority study was designed involving one expert team (\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$>18$$\end{document}>18 procedures prior) who performed six 2D and six 3D fSB repair simulations in a high-fidelity animal training model, using 3-port access. The 6D motion of the instruments was recorded. Among the motion metrics are total path length, smoothness, maximum speed, the modified Spectral Arc Length (SPARC), and Log Dimensionless Jerk (LDLJ). The primary clinical outcome is operation time (power 90%, 5% significance) using Sealed Envelope Ltd. 2012. Secondary clinical outcomes are water tightness of the repair, CO\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$_2$$\end{document}2 insufflation volume, and OSATS score. Findings show that total path length and LDLJ are considerably different. Operation time during 3D vision was found to be significantly shorter compared to 2D vision (\documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$113\pm 9$$\end{document}113±9 vs. \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$149\pm 19$$\end{document}149±19 min; p \documentclass[12pt]{minimal} \usepackage{amsmath} \usepackage{wasysym} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{amsbsy} \usepackage{mathrsfs} \usepackage{upgreek} \setlength{\oddsidemargin}{-69pt} \begin{document}$$=$$\end{document}= 0.026). These results suggest enhanced performance with 3D vision during interrupted suturing in fetoscopic SBA repair. To confirm these results, a larger-scale follow-up study involving multiple experts and novice surgeons is recommended.

in subsequent pregnancies, significant efforts have been made to make this operation minimally invasive (MIS) using fetoscopic instrumentation 11 .
Prenatal MIS fetoscopic repair may reduce maternal and fetal risks, however, an MIS approach is more challenging than its open counterpart.The vulnerable surgical environment and difficult closure techniques are combined with common disadvantages of endoscopic approaches: the fulcrum effect that inverts motion, the reduction of motion to only four degrees of freedom, poor tactile feedback, loss of depth perception, and difficult hand-eye coordination together leading to increased operation times.3D imaging techniques could help the surgeon regain the sense of depth and improve efficiency.
This work exploits quantitative motion metrics to objectively assess whether 3D fetoscopy actually benefits expert surgeons in performing prenatal MIS for fSB-repair.Our hypothesis is that the skills of expert surgeons improve when performing fetoscopic repair with 3D vision rather than 2D vision and that these improvements are measurable using quantitative motion metrics.

Study design
A superiority study was designed involving one expert laparoscopic fetal surgeon (JD) and assistant (LJ) performing a simulated fetoscopic SB repair in a high-fidelity animal training model using 3-port access 12 .The primary outcome of this experiment was total operation time (TOT) which includes the preparation of the animal model until the end of the last step of the surgery.Based on estimated TOT, six surgeries per group (2D vs. 3D) were required (β = 90%, α = 5%) .Secondary clinical outcomes were water tightness at the end of the repair, total volume CO2 used, and OSATS score.To document the performance of the surgeon in terms of instrument use, 39 motion metrics were computed including path length, smoothness, maximum speed, the modified Spectral Arc Length (SPARC), Log Dimensionless Jerk (LDLJ), Number of Speed Peeks (NSP) and Number of Acceleration Peeks (NAP) [13][14][15][16][17][18][19][20] .These metrics are calculated for the surgeon's left hand (LH), right hand (RH) and the assistant's hand holding the fetoscope (FH).
Since clinically, today's fetoscopic surgeons would typically transit from 2D to 3D vision 21,22 , the surgeon first operated in 2D after which all 3D experiments were performed.Prior to the first operation herein, the surgeon conducted 18 interventions on the model.An earlier study using competency cumulative sum (C-CUSUM) analysis 12 demonstrated competency after six consecutive procedures.

Training model
The experiments used a high-fidelity training model as earlier described by Joyeux et al. 12 .In an adult male New Zealand rabbit animal model all operative steps and surgical conditions present in current clinical multi-layered fetoscopic spina bifida repair, can be simulated.The rabbit's abdominal cavity mimics the available intra-uterine workspace (15 × 10 × 5 cm) when insufflated with 3 l, of CO 2 at a pressure of 5 mmHg 23 .The back of the fetus (22-24 weeks of gestation) is represented by the rabbit stomach 24 .In this model, laparoscopic gastric Nissen fundoplication 25 the ten surgical steps required for fetoscopic spina bifida repair, including gastric wall patch suturing, can be mirrored, and necessitate delicate tissue handling, thorough dissection, hemostasis, and suturing.

Surgical procedure
We used adult New-Zealand rabbits and standard pediatric laparoscopic instruments and a 3D endoscope (Karl Storz™ 4 mm scope, TIPCAM1 S, 7240 BA3D).Four main motion sequences were identified containing similar movements to fetoscopic repair.These sequences are used for comparison of 3D vs. 2D motion-based skill: • I. Dissection movements: the surgeon performs a series of explorative, dissection and grasping movements to free up the esophagogastric junction (EGJ) in preparation of the fundoplication.• II.High-force movements: the surgeon creates an anti-reflux valve by pulling the upper part of the stomach (called the fundus) behind the EGJ.• III.Interrupted suturing: the surgeon performs the fundoplication with a series of interrupted sutures.
• IV.Running sutures: the surgeon sutures a patch on the large anterior curvature of the rabbit stomach with two semi-circular running sutures.
The secondary outcomes included the individual operation time for motion sequences I, II, III, and IV, and their sum which equals the fetal operation time (FOT) and the time spent on operative steps, while the TOT includes the preparation and conclusion steps as well.

Experimental setup
Figure 1 shows the experimental setup.The Aurora (NDI, Ontario, Canada) electromagnetic field generator (FG) henceforth referred to as the Aurora tracker, measures the 3D position and 3D orientation of the LH tool, the RH tool, the fetoscope, and the fetoscope port.All instruments had a dedicated electromagnetic tracking (EMT) sensor attached.Because the Aurora tracker has only four input ports, only four sensors can be tracked simultaneously.Therefore, during some instrument changes sensors needed to be dis-and reconnected.Upon instrument switch or when a surgical step or phase was completed, Aurora recordings were stopped.This results in each trial being segmented in multiple motion recordings.Notes were made during the surgery to keep track of the recorded segments or unexpected events.When non-connected instruments were used briefly, the connections were not changed.This results inevitably in motion recordings having partially invisible (sensor out of range) segments.
The endoscope used in this study was a Karl Storz™ 4 mm scope (TIPCAM1 S, 30° angle, 18 cm length, 7240 BA3D) which allows to easily switch from 2D to 3D vision 26 .To perform 3D surgery, we used the same HD monitor and operators were wearing the Karl Storz™ 3D glasses.Unlike autostereoscopy 27 , the HD monitor allows multiple users to have a stereo view as long as they wear the 3D glasses.During surgery, one surgical assistant manipulated the fetoscope while the expert surgeon performed the operation.Seven laparoscopic instruments were used.Video recordings of the full surgical scene and fetoscope were made.

Motion metrics and clinical outcomes
Motion can be analyzed to assess the surgeon's performance under different circumstances 14 .Table 1 lists the different motion metrics that were employed alongside the equations to calculate them.The metrics were computed for the LH, RH and fetoscope, and port motions.The SPARC, LDLJ, path length and maximum, mean, and consistency of the speed and acceleration are time-independent motion metrics while the others are timedependent.Time independence is an important characteristic for a metric to truly represent skill.
The EM sensors may have been only visible for a duration of time that is relevant for a specific segment of the procedure.For this, the visibility ratios v i are calculated to provide a metric for the reliability of the motion data.Here, the motion data is considered "visible" even if one of the three (RH, LH, and fetoscope) instrument's EM sensor measurements are available for a relevant surgical step.

Motion data processing
Both the motion and video data are used in the process to calculate the motion metrics.Figure 2 shows the process with three main steps: pre-processing, processing, and debugging.These steps are computed with MATLAB ® .The goal of pre-processing is to transform the raw motion data captured from the experiment into motion data that is suited for calculating the motion metrics.Pre-processing can be further split into five separate steps: Table 1.Metrics used for quantitative motion analysis.The | .| denotes the cardinal of a set and i denotes the metric corresponding to the ith segment.The function convhull() is a built-in MATLAB ® (Mathworks, Massachusetts, US) function.

Total time
Path length Mean speed Si mean(v i (t)) Speed consistency σ Si std(v i (t)) Mean acceleration Āi mean(a i (t)) Acceleration consistency σ Ai std(a i (t)) • Formatting (a) data in the right structure.The stored data files (encrypted ROS bag files) from the Aurora tracker is transformed into a readable database.• Transforming (b) the data to the correct reference frame.A corner of the operating table (number 5 in Fig. 1) is used as the base reference frame for all sensors.• Pruning (c) invisible data.Motion data that was invisible for more than 1 second is removed from the data to not affect the metrics.Segments that were invisible for less than a second are filled using quadratic spline interpolation based on the visible data points before and after the invisible segment.www.nature.com/scientificreports/Processing consists of calculating the required motion metrics for each of the four global motion sequences mentioned above.In order to do this, it is necessary to aggregate the results of the smaller motion segments i generated during step c.Depending on the motion metric, aggregation is done differently.For example, the path length P i of each segment is summed together to represent the total path length of the sequence, whereas the mean speed Si of each segment is averaged to find the overall mean speed.The maximum speed S i,max is aggregated by taking the maximum speed of all segments.The last step, named debugging ensures that the quadratic interpolation adopted to process the invisibility is performed accurately: If the interpolation generated a maximum acceleration above 6 ms −2 , which is outside the range of human-produced accelerations, this part of motion data is not included in the analysis .

Statistical data analysis
The null hypothesis states that the means of the motion metrics obtained in the 3D group are equal to those in the 2D group.This requires an unpaired t-test or, in the case the metrics were not normally distributed or when the variances σ 2 were not equal, a parametric Wilcoxon rank-sum test.To test for normality and equal variances we used the Saphiro-Wilk test and the F-test respectively.The software GraphPad Prism 8.4.2.(Dotmatics, Boston, MA, USA) was used for processing these tests.

Ethical approval statement
This experiment was approved by the Animal Ethics Committee of the Group Biomedical Sciences of the KU Leuven (P093-2016).The experiments were done following the ARRIVE guidelines for animal research 28,29 , and the guidelines of the National Centre for the Replacement, Refinement and Reduction of Animals in Research (NC3Rs).

Clinical outcomes
For each clinical outcome the mean for both the 2D ( µ 2D ) and 3D ( µ 3D ) groups are shown in Table 2, as well as their difference µ (2D−3D) .A 95% confidence interval (CI) is reported as well.All execution times are lower when using 3D and TOT, as well as FOT, are significantly reduced in the 3D group with an average reduction of respectively 35 and 24 minutes.Taking into account the different steps in the surgery, the operation time for the dissection movements (I) and interrupted suturing (III) show an even more obvious difference.For the dissections, a 40% reduction is appearing, and the time for interrupted suturing is reduced from an average time of 21.7 minutes in the 2D group to 13.2 minutes in the 3D group, which is more than a 30% reduction.No differences are found for the OSATS score nor for the insufflation volume.

Visibility
The visibility ratios of the motion recordings are shown in Table 3. Sequences III and IV are well recorded with an average visibility of respectively 91% and 94%.Sequences I and II are less well recorded due to missing recordings and lower visibility.The bold values show visibility below 80%, suggesting the motion data is less reliable.
Recordings for trial 3 for the 2D group as well as a segment in trial 5 for both 2D and 3D groups are missing due to technical issues.The asterisk (*) marks a potential mismatch between motion signals and surgical movements due to the difficulties with the annotations.In these cases the motion segment was chosen to be slightly longer than the actual movement on the video, to make sure that the motions typical for the surgical procedure are also included in the final sequence.The downside of this approach is that motions not representative of relevant surgical step might get introduced as well, reducing the data quality.Instead of a visibility ratio greater than 1, the visibility is set to be equal to the average visibility of that sequence.
Another way to check the reliability of the motion data is to compare the total motion time from Figs. 3 and  4 with the clinical fetal operation time from Table 2. Indeed, the previously reported clinical operation time is showing a considerable difference for the dissection motions (I) and interrupted suturing motions (III).For the latter, the motion-based total time is also demonstrating a considerable difference, confirming the clinically   measured operation time.In the case of the dissection motions, the motion-based total time is showing a considerable difference for the right hand but not for the left hand, even though the left and right hand are equally used.This contrasts with the clinically measured operation time and therefore suggests that the motion data of this sequence is not totally reliable.The visibility analysis confirms these findings.Therefore only detailed results are shown in the following for the interrupted suturing motions.

Motion metrics
The results of the statistical analysis comparing the motion metrics from the 3D and 2D groups are reported in Table 4.More detailed data for the right hand and left hand for the interrupted suturing motions are reported in Figs. 3 and 4. The surgeon's left hand has the Acceleration Peak Rate (APR) as an additional significantly different metric.Note that the total time shown in these tables is calculated using the motion data of the corresponding instruments rather than the clinically measured operation time.
There are no significant differences in the running suturing motions (IV) while multiple considerable differences are found when comparing interrupted suturing motions (III).The significant metrics for both surgeon's hands and the assistant's hand include path length, Log Dimensionless Jerk (LDLJ), Number of Speed Peaks (NSP), and Number of Acceleration Peaks (NAP).For the NSP and NAP metrics, the P-value is increasing with an increasing threshold α .At a higher threshold, the motion metrics are often not deemed normally distributed.Therefore a non-parametrical Wilcoxon-ranksum test instead of a student t-test is used.These metrics are marked in bold in the tables.The SPARC, Smoothness, MAPR, SPR and APR are not showing significant differences.

Principal findings
Results indicate significant differences in total operation time, fundoplication time, and dissection time between 3D and 2D fetoscopy, in line with available literature.This suggests that 3D vision makes fundoplication and dissections easier.A difference was found for several quantitative motion metrics such as path length, Log dimensionless jerk, number of speed peeks, and number of acceleration peaks when comparing interrupted suturing.No significant differences were detected when running suturing motions were compared.Highly standardized tasks like running sutures may over time become automatic for experienced surgeons, negating immediate benefits of 3D fetoscopy 30 .

Results in existing knowledge context
Several studies have looked at the differences in skill under 3D and 2D vision between novices or experts.In these, differences in operation time were found for running suturing tasks [14][15][16][17] .In our case, running suturing motions (IV) does not show quantitative differences.Motion analysis has been subject to a high degree of variability from study to study.Patel et al. 31 compared 2D and 3D fetoscopy's impact on spina bifida repair using a low fidelity simulator.Surgical performance was gauged subjectively through skin cutting, dural patch placement, and suturing, using the NASA-TLX questionnaire 32 .In 16 participants there were no significant differences except for 3D's shorter total operation time.In a study by Wilhelm et al. 33 , experienced laparoscopists among 48 study participants, excelled with a 3D endoscope.Operation time and instrument path length improved with 3D, but there was no difference in NASA-TLX scores.Nomura et al. 34 compared imaging modes for endoscopic submucosal dissection in animals, finding comparable operation times.3D reduced time and negatively impacted eyestrain symptoms (excluding blurred vision), as measured on a 100 mm visual analog scale 35 .
The SPARC, as proposed in 18 , is showing a non-significant improvement towards the 3D group.Although the metric is known to be time-independent and consistent such as in the detection of Parkinson's disease 19 , it is sensitive to noise and therefore requires the right tuning in order not to be affected too much.We assume that the interrupted suturing sequence that we have been using for the comparison includes too many different motions for this metric to appear decisive in our comparison.We expect that it would be necessary to further segment the four motion sequences into smaller more distinguishable movements to leverage this metric to allow for stronger conclusions.The LDLJ, another advanced and recurring motion metric in literature, does show a noticeable difference, although small.This suggests a detectable motion difference between 3D and 2D vision during interrupted suturing.As for the SPARC, our whole analysis could possibly be improved as well by further splitting the motion data.
The threshold α is slightly affecting the motion metrics NSP, NAP, and their corresponding SPRate and APRate.It appears that the metrics with a higher threshold are not normally distributed and become less suitable www.nature.com/scientificreports/for comparison.Although this group of metrics is showing very significant differences for both the right and left hand ( P NSP0,NAP0 =< 0.001 ), due to their nature they are highly dependent on the total motion time.Therefore they do not provide much additional information in addition to the motion time.

Clinical and research implications
Given the progressive nature of spina bifida, ensuring a watertight closure of the dura and fascia layers over the neural placode is critical to prevent amniotic fluid-related damage 36 .Various closure methods, like suturing, can significantly influence repair quality.Through subtask-level motion analysis, this study directly gauged the impact of stereo fetoscopy on these tasks.This approach could potentially unveil alternative closure techniques for better outcomes or optimize existing methods by leveraging specific imaging technology.During interrupted suturing motions (III), many significant differences are found.During this surgical step, four interrupted sutures are required in order to perform the fundoplication.In contrary to the running suture technique, a knot is required for every suture.The surgeon has to perform more manipulations with the suture.Moreover, the dynamic range of movements also increases; instead of a continuous motion making the semicircular suture, the surgeon has to move the fundus to perform the suture at a totally different location.Because the manipulations take place in the full range of the surgical field, it appears that improved depth perception is needed for successful completion.A similar interpretation could be made for the dissection motions (I), where the surgeon has to manipulate a series of soft tissues laying caudal in the rabbit.The surgeon has to extend the tools far in the rabbit to reach the tissues, also requiring more depth perception.Such surgical tasks provide an interesting opportunity to be used as a training or evaluation exercise to study the effects of 3D vision vs. 2D vision on the skill level of a surgeon.
Robot-assisted surgery's growing popularity prompts exploration of its application in spina bifida repair.Many available surgical robots feature console stereo displays.Falk et al. 3 evaluated 3D visualization's impact using the Da Vinci telerobotics system.Metrics included time, task errors, and kinematic analysis.Results demonstrated the superiority of 3D over 2D at the same/higher resolution, enabling faster, more precise performance.Given the delicate nature of fetal spina bifida repair, robotic solutions would offer stable instruments and high resolution 3D vision.Supported by this study, this makes them an encouraging consideration for surgical teams worldwide.

Strengths and limitations
In this study, we have underscored the significance of pre-processing raw data and introduced methods for that.Also, this study has undertaken a more detailed analysis of surgical steps by breaking them down into specific actions and maneuvers at sub-task level, subsequently annotating the data accordingly.Additionally, we have conducted a comprehensive exploration of 39 motion metrics extracted from existing literature to determine which metrics are most conducive to providing meaningful comparisons in future investigations.
An important limitation of this research is the low number of simulations performed (sample size n 2D = n 3D = 6 ) while comparing the impact on just one expert endoscopic-fetal surgeon.This study however was powered to detect differences in operation time (primary outcome) and not in motion metrics.Furthermore, technical challenges, such as sensor breakage, workspace being moved out of range during procedure, recording system crash resulted in a further reduction of the motion tracking data, making the data for dissection (sequence I) and high-force movements (sequence II) unreliable.In case of technical errors in the motion tracking system and loss of signals, the trial was not interrupted in order not to increase operation time and animal suffering.
Interested surgeons may face some challenges in replicating this study due to ethical, logistical and financial hurdles linked to animal trials.To address this concern and further improve the external validity by increasing trial numbers and surgeons, one could adopt high or low fidelity surgical simulators, including for spina bifida repair 31,37,38 .

Conclusion
In the high-fidelity rabbit model for fetoscopic SBA repair, 3D vision via 3-port access substantially shortens operation time for an expert fetal surgeon during interrupted suturing.A substantial difference was found for several quantitative motion metrics such as path length, Log dimensionless jerk, number of speed peeks, and number of acceleration peaks.No substantial differences were detected when running suturing motions were compared.
Three takeaways with respect to motion analysis for future research are summarised here.Firstly, this research shows that one can draw interesting conclusions from comparing interrupted and running suturing motions.Secondly, the importance of time-independent motion metrics, like SPARC, has been pointed out.It is indeed important to have different motion metrics based on multiple aspects.The SPARC and LDLJ are two metrics that have been consistently performing in other literature under the right conditions which is why the recommendation is made to define the sample size based on this metric.The challenge will be to segment the motion data up to a sufficiently small resolution.Finally, it is extremely important to record the full surgical scene and to provide cues in the video when the motion recording is started or stopped.This provides major help in annotating the motion recordings such that accurate and precise motion segments can be used for comparison.
This research opens the door for follow-up studies in the field of 3D vs 2D motion analyses.The results should be interpreted from a guidance perspective.It is a pilot study that demonstrates the urge and potential for research on this topic and has proposed key learnings to help future research.
• Smoothing (d) the data.A butterworth filter ( f c = 10 Hz, n = 5 ) and an exponential filter ( α = 0.05 ) are applied to the motion data.• Annotating (e) the data.Starting and ending timestamps of relevant surgical step segments in motion data are noted manually based on the fetoscope's video.

Figure 1 .
Figure 1.Set-up of experiment.(1) Assistant's hand holding the fetoscope.(2) Left hand (LH) of expert surgeon holding a tool.(3) Right hand (RH) of expert surgeon holding a tool.(4) Aurora sensors taped to LH tool, RH tool, fetoscope.(5) Operating table corner used as a reference for Aurora tracker.(6) The fetoscope port with aurora sensor attached.(7)The male adult New Zealand rabbit.(8) Aurora tracker magnetic field generator (FG).(9) The display showing images from the fetoscope.

Table 4 .
P values for unpaired t-tests comparing the motion metrics.α = 0.05 , * p ≤ 0.05 , **p ≤ 0.01 , ***p ≤ 0.001 , bold: rank sum test.SAL spectral arc length, SPARC modified spectral arc length, LDLJ log dimensionless jerk, NSPx number of speed peaks with threshold equal to x times the average speed, SPRx speed peak rate, MAPRx movement arrest period ratio, NAPx number of acceleration peaks, APRx acceleration peak rate, IAV integral of acceleration vector.