Retroperitoneoscopic Surgery in Children Does Not Cause Pathological Desaturation in Cerebral/Renal Oxygenation on Near-Infrared Spectroscopy Compared with Laparoscopic and Thoracoscopic Surgery

Abstract

Introduction:

Cerebral and renal regional oxygen saturation (C-rSO₂ and R-rSO₂, respectively) were monitored using near-infrared spectroscopy in pediatric patients (range: 0.3–14.3 years) during minimally invasive surgery (MIS) taking at least 3 hours performed by laparoscopy (Lap), thoracoscopy (Tho), or retroperitoneoscopy (Ret) from January 2019 to December 2021.

Materials and Methods:

Criteria compared were operative time, preoperative/intraoperative hemoglobin, blood loss, mean arterial pressure, arterial partial pressure of carbon dioxide (PaCO₂), peripheral oxygen saturation (SpO₂), C-rSO₂, and R-rSO₂. Pathological desaturation (PD) was defined as >20% decrease from baseline, and statistical significance as P < .05.

Results:

Subjects (n = 79) were similar for gender, age, and body mass index. MIS procedures were: Lap = 45, Tho = 20, Ret = 14; one Lap case required conversion for severe adhesions, not PD. Intraoperative PaCO₂ (mmHg) was significantly higher in Tho (maximum: 59.5 ± 17.0, minimum: 39.9 ± 7.5) versus Lap (maximum: 39.9 ± 5.1, minimum: 34.6 ± 3.9) and Ret (maximum: 37.8 ± 4.2, minimum: 35.0 ± 3.3); P < .0001 (maximum), P = .0013 (minimum). Minimum intraoperative SpO₂ was significantly lower in Tho (P < .0001). Mean operative times were significantly shorter in Tho (259 ± 114 minutes) versus Lap (433 ± 154 minutes) and Ret (342 ± 100 minutes); P < .0001, respectively. PD was absent during Ret (C-rSO₂: 0/14 = 0% and R-rSO₂: 0/14 = 0%). Differences in PD for Lap (C-rSO₂: 7/45 = 15.6% and R-rSO₂: 10/45 = 22.2%) and Tho (C-rSO₂: 9/20 = 45.0%, and R-rSO₂: 7/20 = 35.0%) were significant; P = .0028 for C-rSO₂ and P = .0497 for R-rSO₂. Hemoglobin and blood loss were similar.

Conclusions:

PD was absent during Ret, despite longer operative times. If Ret is indicated for a procedure, neurodevelopmental sequelae of MIS could be minimized.

Introduction

With technological advancements, the repertoire of procedures that can be performed using minimally invasive surgery (MIS) has grown and successful reports of surgery in patients that may not be ideal for conventional open intervention, such as the super elderly and preterm/premature neonates are increasing. With patients at the extremes of the human lifespan, physiology is less robust and utmost care is required to maintain cardiovascular function and tissue oxygenation.

While MIS is known to be associated with quicker recovery and less requirement for analgesia,¹ the impact of insufflation is unavoidable.^2–4 Several articles report increased intra-abdominal pressure and reduced renal perfusion secondary to pneumoperitoneum during laparoscopy (Lap),^5,6 an association between thoracoscopy (Tho) and risks for hypercapnia and acidosis during pneumothorax that can be severe, particularly in children, as well as hemodynamic derangement that can induce cerebral oxygen desaturation.^3,4

Reports about complications and technical aspects of MIS abound in the literature, but few focus on tissue oxygenation and sequelae of desaturation during MIS. In an earlier published study, the authors reported evidence of the profound fragility of neonatal vascular perfusion compared with older pediatric patients using intraoperative near-infrared spectroscopy (NIRS).⁷ NIRS enables real-time monitoring of tissue oxyhemoglobin and deoxyhemoglobin for measuring tissue oxygen uptake and consumption,⁸ providing data for oxygen demand, oxygen extraction, and oxygen reserve⁹ used to calculate regional oxygen saturation (rSO₂). NIRS is sensitive and monitoring dynamic changes in rSO₂ can identify resaturation faster than percutaneous oxygen saturation monitoring.¹⁰

The aim of this study was to determine cerebral and renal rSO₂ (C-rSO₂ and R-rSO₂, respectively) using NIRS during pediatric MIS procedures performed using Lap, Tho, and retroperitoneoscopy (Ret) to determine differences in physiological impact as reflected by the incidence of pathological desaturation (PD) in rSO₂.

Materials and Methods

Subjects were Japanese pediatric patients whose caregivers consented to participate in an observational prospective study on the impact of MIS monitored using NIRS. The study was performed at a single institution from January 2019 to December 2021 by a single team of board-certified pediatric surgeons with specialist qualifications in MIS. All procedures had scheduled operative times of at least 3 hours. NIRS (INVOS 5100C; Covidien, Boulder, CO) sensors were applied to the forehead (C-rSO₂) and flanks (R-rSO₂) of each subject after induction of general anesthesia and removed after extubation or on exiting the operating room if postoperative intubation was required. Recordings were analyzed using the INVOS Monitoring System Analytics Tool software, provided by Covidien.

Criteria compared were: gender ratio, age at the time of surgery, body mass index (BMI), operative time, preoperative hemoglobin, hemoglobin from intraoperative blood gas measurement, blood loss, mean arterial pressure (MAP), MAP ratio (ratio of minimum to maximum MAP), arterial partial pressure of carbon dioxide (PaCO₂), peripheral oxygen saturation (SpO₂), C-rSO₂, and R-rSO₂. PD in C-rSO₂ and R-rSO₂ was defined as >20% decrease from preoperative baseline levels. PD ratio (ratio of minimum rSO₂ to baseline rSO₂; maximum PD ratio, indicating no change in perfusion related to surgery was 1) was also calculated to reflect intraoperative stability of vascular perfusion for each MIS technique.

Statistical analyses were performed with GraphPad Prism 9 (GraphPad Software, Inc., SanDiego, USA). Categorical data were analyzed using the chi-square test. Continuous data were analyzed using the one-way ANOVA. A P-value of <.05 was considered statistically significant.

This study was approved by the Institutional Review Board at Juntendo University School of Medicine (H20-0227) and complies with the Helsinki Declaration of 1975 (revised 1983).

Results

Subjects were 79 Japanese children from 0.3 to 14.3 years of age. Pediatric MIS procedures performed were: Lap: pull through for Hirschsprung's disease (n = 12), anorectoplasty for anorectal malformation (n = 11), choledochal cyst excision with hepaticojejunostomy anastomosis (n = 10), Nissen fundoplication (n = 4), Kasai portoenterostomy (n = 3), ectopic kidney resection (n = 2), adrenalectomy (n = 1), and tumor resection (n = 2); Tho: lung lobectomy (n = 12), mediastinal tumor resection (n = 6), esophageal anastomosis (n = 1), and diaphragmatic hernia repair (n = 1); and Ret: pyeloplasty (n = 12) and nephrectomy (n = 2).

The three groups had similar gender ratios, mean weights at surgery, mean heights at surgery, and mean BMI at surgery. Specifically, gender ratios (male:female) were: Lap (28:17), Tho (7:13), and Ret (9:5); P = .097, mean ages (years) at surgery were: Lap (3.4 ± 3.5), Tho (5.1 ± 4.8), and Ret (5.6 ± 2.8); P = .093, mean weights (kg) at surgery were: Lap (14.5 ± 9.4), Tho (18.9 ± 14.7), and Ret (20.3 ± 5.6); P = .122, mean heights (cm) at surgery were: Lap (89.8 ± 26.9), Tho (101.4 ± 32.8), and Ret (107.7 ± 16.4); P = .068, and mean BMI (kg/m²) at surgery were: Lap (16.6 ± 1.8), Tho (15.9 ± 2.0), and Ret (17.3 ± 2.2), P = .105 (Table 1).

Table 1.

Subject Demographics (n = 79)

	Laparoscopic surgery (n = 45)	Thoracoscopic surgery (n = 20)	Retroperitoneoscopic surgery (n = 14)	P
Gender ratio (male/female)	28/17	7/13	9/5	.097
Mean age (years)	3.4 ± 3.5	5.1 ± 4.8	5.6 ± 2.8	.093
Mean weight (kg)	14.5 ± 9.4	18.9 ± 14.7	20.3 ± 5.6	.122
Mean height (cm)	89.8 ± 26.9	101.4 ± 32.8	107.7 ± 16.4	.068
Mean BMI (kg/m²)	16.6 ± 1.8	15.9 ± 2.0	17.3 ± 2.2	.105

BMI, body mass index.

Data for MAP, MAP ratios, preoperative hemoglobin, intraoperative blood gas hemoglobin, and blood loss were also similar. Specifically, maximum MAP (mmHg) were: Lap (85.2 ± 14.2), Tho (79.0 ± 11.9), and Ret (89.8 ± 13.9); P = .078, minimum MAP (mmHg) were: Lap (51.5 ± 7.9), Tho (52.0 ± 6.8), and Ret (57.2 ± 10.1); P = .077, MAP ratios were: Lap (0.63 ± 0.12), Tho (0.67 ± 0.10), and Ret (0.64 ± 0.11); P = .24, mean preoperative hemoglobin (g/dL) were: Lap (12.5 ± 1.3), Tho (12.2 ± 2.0), and Ret (13.3 ± 0.9); P = .12, minimum intraoperative blood gas hemoglobin (g/dL) were: Lap (10.4 ± 1.4), Tho (10.7 ± 1.4), and Ret (11.5 ± 1.1); P = .068, and mean Table 2 blood loss (g) was: Lap (9.7 ± 11.0), Tho (5.6 ± 10.4), and Ret (6.2 ± 4.7); P = .25 (Table 2).

Table 2.

Subject Operative Data (n = 79)

	Laparoscopic surgery (n = 45)	Thoracoscopic surgery (n = 20)	Retroperitoneoscopic surgery (n = 14)	P
Mean operating time (minutes)	433 ± 154	259 ± 114	342 ± 100	<.0001
MAP
Maximum MAP (mmHg)	85.2 ± 14.2	79.0 ± 11.9	89.8 ± 13.9	.078
Minimum MAP (mmHg)	51.5 ± 7.9	52.0 ± 6.8	57.2 ± 10.1	.077
MAP ratio (minimum/maximum)	0.63 ± 0.12	0.67 ± 0.10	0.64 ± 0.11	.24
Preoperative hemoglobin (g/dL)	12.5 ± 1.3	12.2 ± 2.0	13.3 ± 0.9	.12
Minimum blood gas hemoglobin (g/dL)	10.4 ± 1.4	10.7 ± 1.4	11.5 ± 1.1	.068
Blood loss (g)	9.7 ± 11.0	5.6 ± 10.4	6.2 ± 4.7	.25

MAP, mean arterial pressure.

Mean operative times were significantly shorter in Tho, minimum SpO₂ were significantly lower in Tho, and PaCO₂ were significantly higher in Tho. Specifically, operative times (minutes) were: Tho (259 ± 114 minutes), Lap (433 ± 154 minutes), and Ret (342 ± 100 minutes); P < .0001, minimum SpO₂ (%) were: Tho (89.5 ± 11.4), Lap (97.4 ± 3.0), and Ret (97.9 ± 1.2); P < .0001, PaCO₂ (mmHg) were: Tho (maximum: 59.5 ± 17.0, minimum: 39.9 ± 7.5), Lap (maximum: 39.9 ± 5.1, minimum: 34.6 ± 3.9), and Ret (maximum: 37.8 ± 4.2, minimum: 35.0 ± 3.3); P < .0001 for maximum PaCO₂ and P = .0013 for minimum PaCO₂, respectively (Fig. 1).

FIG. 1.

Intraoperative gas exchange data according to MIS technique. MIS, minimally invasive surgery; PD, pathological desaturation; PD ratio, minimum/baseline rSO₂; Lap, laparoscopy; Ret, retroperitoneoscopy; rSO₂, regional oxygen saturation; Tho, thoracoscopy.

PD were absent in Ret (C-rSO₂: 0/14 = 0% and R-rSO₂: 0/14 = 0%). PD in Lap were (C-rSO₂: 7/45 = 15.6% and R-rSO₂: 10/45 = 22.2%) and Tho were (C-rSO₂: 9/20 = 45.0% and R-rSO₂: 7/20 = 35.0%). Differences were significant; P = .0028 for C-rSO₂ and P = .0497 for R-rSO₂, respectively (Table 3). PD ratios were significantly higher in Ret (C-rSO₂: 0.92 ± 0.06 and R-rSO₂: 0.96 ± 0.03) compared with Lap (C-rSO₂: 0.89 ± 0.07 and R-rSO₂: 0.85 ± 0.12) and Tho (C-rSO₂: 0.79 ± 0.12 and R-rSO₂: 0.85 ± 0.10); P < .0001 for C-rSO₂ and P = .0043 for R-rSO₂, respectively (Fig. 2).

FIG. 2.

PD ratios according to MIS technique. MIS, minimally invasive surgery; PD, pathological desaturation; PD ratio, minimum/baseline rSO₂; Lap, laparoscopy; Ret, retroperitoneoscopy; Tho, thoracoscopy; rSO₂, regional oxygen saturation.

Table 3.

Incidence of Pathological Desaturation in rSO₂

	Laparoscopic surgery (n = 45)	Thoracoscopic surgery (n = 20)	Retroperitoneoscopic surgery (n = 14)	P
C-rSO₂	7/45 (15.6%)	9/20 (45.0%)	0/14 (0.0%)	.0028
R-rSO₂	10/45 (22.2%)	7/20 (35.0%)	0/14 (0.0%)	.0497

C-rSO₂, cerebral regional oxygen saturation; rSO₂, regional oxygen saturation; R-rSO₂, renal regional oxygen saturation.

Discussion

From the finding that PD did not occur during Ret for MIS procedures taking at least 3 hours in pediatric cases, Ret would appear to be associated with more stable perfusion than Lap or Tho. While Ret subjects tended to be older and larger, differences were not statistically significant. Compromised ventilation during Tho and manipulation of abdominal organs during Lap could be expected to influence PD but the difference between Ret and Lap/Tho was unexpectedly distinct. This trend is worth considering when planning surgery for procedures that can be performed using alternative techniques.

Obviously, Tho compromises ventilation; minimum SpO₂ was significantly lower and both maximum and minimum PaCO₂ were significantly higher in Tho than Lap and Ret in this study. Bishay et al reported that cerebral oxygenation can also be decreased by hypercapnia and acidosis secondary to increased CO₂ absorption during pneumothorax.³ On the other hand, Lap causes compromise related to intra-abdominal pressure with insufflation limiting respiratory movements and perfusion affected by pressure on vessels and manipulation of abdominal organs. Pelizzo et al reported that decreased cerebral oxygen saturation correlated with increased intra-abdominal pressure during pediatric laparoscopic inguinal hernia repair.¹¹ In an earlier report by the authors, PD in R-rSO₂ was observed immediately in all procedures requiring reduction of viscera into the abdominal cavity, and seemed to be related directly to increased intra-abdominal pressure.⁷ From these perspectives, lack of PD seen during Ret procedures could be related to PaCO₂ and abdominal pressure resulting in stable rSO₂.

MIS procedures that can be performed using Ret in children are limited to urology, but some can be performed using Lap with no consensus about which approach is preferable among pediatric surgeons and pediatric urologists.^12–14 The reality is that few surgeons choose Ret because the retroperitoneal space is small, the operative field tends to get crowded by instruments, or less trocars are used, and maneuverability suffers.^15,16 Robotic surgical systems add extra restraints because trocars must be a certain minimum distance apart. The working space is larger with Lap, enabling more instruments to be used¹² and as a result, some articles have even reported that Lap is thus faster, safer, and technically easier than Ret.^12,13,16 These articles focus on technicalities without discussing any issues related to tissue oxygenation. Despite lack of PD during Ret, operator confidence and safety will be more influential when planning how to perform a procedure; few surgeons will opt to choose an approach based purely on oxygen saturation.

Nevertheless, while logistically, Ret is at a disadvantage, pediatric patients have yet to complete full neurological development and any potential cause for PD must be minimized, or prevented. Pediatric patients potentially have many decades of postoperative life after successful surgery, so tissue oxygenation should be an important topic for pediatric surgeons to consider when planning surgery. Thus, Kussman et al reported that intraoperative PD in C-rSO₂ is a risk factor for reduced neurodevelopment in infants using the Psychomotor Development Index and brain magnetic resonance imaging,¹⁷ Hoffman, et al reported that perioperative C-rSO₂ was correlated with neurodevelopmental performance in preschool-aged children,¹⁸ and Sood et al reported that patients with lower perioperative C-rSO₂ had lower receptive communication scores.¹⁹ On the other hand, active monitoring of perioperative C-rSO₂ has been reported to be adequate for reducing postoperative neurological complications, such as seizures, cerebral infarct, and speech problems.²⁰

While this study has limitations because it was an analysis from one center involving a small number of subjects, it identified that Ret has stable tissue oxygenation with no documented PD. Although Ret should be considered actively when indicated, the working space needs to be adequate for success. Thus, Ret is only likely to be used in selected patients to ensure safety although lack of PD is of high priority for normal neurological development. In this study, the correlation between PD and neurodevelopmental outcome was not investigated and a long-term follow-up study on the impact of PD could reveal the optimal threshold for rSO₂, and allow it to be incorporated into surgical planning.

Conclusions

PD was not observed in Ret, and PD ratios were highest for Ret suggesting that oxygenation during Ret is more stable than during Lap or Tho. Although customization is the norm in pediatric surgery, preventing deleterious events could contribute as much or more than mastering technical skills and management. Awareness that Ret procedures are not associated with PD is unlikely to be common knowledge and could help improve the acceptance of Ret for pediatric MIS procedures.

Footnotes

Authors' Contributions

Y.M.: conceptualization, methodology, and writing (original draft preparation); K.F.: formal data analysis; K.K., T.O., and S.S.: collation of data, H.K.: study administration; G.J.L.: writing (native English editing and reviewing); K.N.: resource management; M.H.: methodology; A.Y.: supervision.

Acknowledgments

The authors gratefully acknowledge the work of past and present members of their department.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Franzini

, Morandi

, Palmisani

, et al. Cerebral oxygenation by near-infrared spectroscopy in infants undergoing thoracoscopic lung resection. J Laparoendosc Adv Surg Tech A, 2021; 31,(9):1084–1091; doi: 10.1089/lap.2021.0177.

Westgarth-Taylor

, de Lijster

, van Bogerijen

, et al. A prospective assessment of renal oxygenation in children undergoing laparoscopy using near-infrared spectroscopy. Surg Endosc, 2013; 27,(10):3696–3704; doi: 10.1007/s00464-013-2950-3.

Bishay

, Giacomello

, Retrosi

, et al. Hypercapnia and acidosis during open and thoracoscopic repair of congenital diaphragmatic hernia and esophageal atresia: Results of a pilot randomized controlled trial. Ann Surg, 2013; 258,(6):895–900; doi: 10.1097/SLA.0b013e31828fab55.

Ellinas

, Seefelder

. Congenital diaphragmatic hernia repair in neonates: Is thoracoscopy feasible?. Paediatr Anaesth, 2010; 20,(10):967–969; doi: 10.1111/j.1460-9592.2010.03384.x.

Lindberg

, Bergqvist

, Björck

, et al. Renal hemodynamics during carbon dioxide pneumoperitoneum: An experimental study in pigs. Surg Endosc, 2003; 17,(3):480–484; doi: 10.1007/s00464-002-9044-y.

Demyttenaere

, Feldman

, Fried

. Effect of pneumoperitoneum on renal perfusion and function: A systematic review. Surg Endosc, 2007; 21,(2):152–160; doi: 10.1007/s00464-006-0250-x.

Miyake

, Seo

, Kataoka

, et al. Significant neonatal intraoperative cerebral and renal oxygen desaturation identified with near-infrared spectroscopy. Pediatr Surg Int, 2022; 38,(5):737–742; doi: 10.1007/s00383-022-05102-5.

Marin

, Moore

. Understanding near-infrared spectroscopy. Adv Neonatal Care, 2011; 11,(6):382–388. doi: 10.1097/ANC.0b013e3182337ebb.

Costerus

, Vlot

, van Rosmalen

, et al. Effects of neonatal thoracoscopic surgery on tissue oxygenation: A Pilot Study on (Neuro-) Monitoring and Outcomes. Eur J Pediatr Surg, 2019; 29,(2):166–172; doi: 10.1055/s-0037-1615277.

10.

Eichhorn

, Erdfelder

, Kessler

, et al. Evaluation of near-infrared spectroscopy under apnea-dependent hypoxia in humans. J Clin Monit Comput, 2015; 29,(6):749–757; doi: 10.1007/s10877-015-9662-2.

11.

Pelizzo

, Bernardi

, Carlini

, et al. Laparoscopy in children and its impact on brain oxygenation during routine inguinal hernia repair. J Minim Access Surg, 2017; 13,(1):51–56; doi: 10.4103/0972-9941.181800.

12.

Esposito

, Escolino

, Corcione

, et al. Twenty-year experience with laparoscopic and retroperitoneoscopic nephrectomy in children: Considerations and details of technique. Surg Endosc, 2016; 30,(5):2114–2118; doi: 10.1007/s00464-015-4472-7.

13.

Esposito

, Escolino

, Castagnetti

, et al. Retroperitoneal and laparoscopic heminephrectomy in duplex kidney in infants and children. Transl Pediatr, 2016; 5,(4):245–250; doi: 10.21037/tp.2016.09.12.

14.

Bowlin

, Farhat

. Laparoscopic nephrectomy and partial nephrectomy: Intraperitoneal, retroperitoneal, single site. Urol Clin North Am, 2015; 42,(1):31–42; doi: 10.1016/j.ucl.2014.09.012.

15.

Valla

. Retroperitoneoscopic surgery in children. Semin Pediatr Surg, 2007; 16,(4):270–277; doi: 10.1053/j.sempedsurg.2007.06.010.

16.

Esposito

, Escolino

, Miyano

, et al. A comparison between laparoscopic and retroperitoneoscopic approach for partial nephrectomy in children with duplex kidney: A multicentric survey. World J Urol, 2016; 34,(7):939–948; doi: 10.1007/s00345-015-1728-8.

17.

Kussman

, Wypij

, Laussen

, et al. Relationship of intraoperative cerebral oxygen saturation to neurodevelopmental outcome and brain magnetic resonance imaging at 1 year of age in infants undergoing biventricular repair. Circulation, 2010; 122,(3):245–254; doi: 10.1161/CIRCULATIONAHA.109.902338.

18.

Hoffman

, Brosig

, Mussatto

, et al. Perioperative cerebral oxygen saturation in neonates with hypoplastic left heart syndrome and childhood neurodevelopmental outcome. J Thorac Cardiovasc Surg, 2013; 146,(5):1153–1164; doi: 10.1016/j.jtcvs.2012.12.060.

19.

Sood

, Benzaquen

, Davies

, et al. Predictive value of perioperative near-infrared spectroscopy for neurodevelopmental outcomes after cardiac surgery in infancy. J Thorac Cardiovasc Surg, 2013; 145,(2):438–445.e431; discussion 444–445; doi: 10.1016/j.jtcvs.2012.10.033.

20.

Austin

, Edmonds

, Auden

, et al. Benefit of neurophysiologic monitoring for pediatric cardiac surgery. J Thorac Cardiovasc Surg, 1997; 114,(5):707–715, 717; discussion 715–716; doi: 10.1016/S0022-5223(97)70074-6.