Renal Medullary Oxygenation during Laparoscopic vs Open Surgery: The Impact of Blood Pressure Management. A pilot randomized controlled trial

doi:10.21203/rs.3.rs-3227702/v1

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Research Article

Renal Medullary Oxygenation during Laparoscopic vs Open Surgery: The Impact of Blood Pressure Management. A pilot randomized controlled trial

https://doi.org/10.21203/rs.3.rs-3227702/v1

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Journal Publication

published 13 Oct, 2023

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Purpose

The impact of blood pressure targets and surgical approach (laparoscopic or open) on continuous urinary oxygenation (PuO₂), a validated surrogate of renal medullary PO₂, during general surgery, is unclear. We aimed to assess the effects of different blood pressure targets and surgical procedures on PuO₂.

Methods

We randomized patients receiving either laparoscopic or open surgery into two mean arterial pressure (MAP) target groups: usual MAP or a high MAP. We measured PuO₂ in real-time and analyzed it according to the type of surgery and blood pressure target. The study was retrospectively registered on the 5th of July 2023 (ACTRN12623000726651).

Results

We included 43 participants who underwent either laparoscopic (n = 20) or open surgery (n = 23). We found that PuO₂ significantly decreased during both laparoscopic and open surgery under a usual blood pressure target (-51% and − 49%, respectively). However, there was a sharper fall with laparoscopic surgery resulting in a higher PuO₂ with open surgery (mean difference: 11 ± 1 mmHg higher; p < 0.001). Targeting a higher MAP resulted in a higher PuO₂ over time during laparoscopic surgery (mean difference: 7 ± 1 mmHg, p < 0.001). In contrast, targeting a usual MAP resulted in a higher PuO₂ during open surgery (mean difference: 7 ± 1 mmHg, p < 0.001).

Conclusion

Surgical approach and intraoperative blood pressure targets significantly impact urinary oxygenation. Further studies with larger sample sizes are needed to confirm these findings and understand their potential clinical implications.

Urinary oxygenation

medullary oxygenation

Laparoscopic surgery

Open surgery

Mean Arterial Pressure

Acute kidney injury

This study demonstrates that surgical approach and blood pressure targets significantly affect urinary oxygenation. A higher blood pressure target during laparoscopic surgery and usual blood pressure during open surgery yielded better oxygenation results, suggesting the need for individualized intraoperative management strategies.

Laparoscopic surgery, as an alternative to open surgery, has become a standard procedure worldwide with an increasing variety of indications [1]. It provides several physiological benefits, such as a small incision, less blood loss, less postoperative pain, and may reduce overall morbidity and hospital lengths of stay [2–4]. However, the procedure requires gas insufflation into the peritoneal cavity [5]. This iatrogenic pneumoperitoneum can have several physiological implications. First, it increases venous return through a mobilization of the splanchnic circulation [6, 7]. Then, rapidly, it can lead to an inferior vena cava compression and a subsequent decrease in cardiac output [8] and increased systemic cardiovascular resistance [9–13]. Finally, the high intra-abdominal pressure affects renal vein pressure leading to kidney congestion [14–17]. Ultimately, all these physiological disturbances can lead to a significant kidney stress test, reduced renal blood flow [18–20] and subsequent acute kidney injury [18, 19, 21].

Despite the above physiological observations, no study has investigated whether targeting a higher mean arterial blood pressure (MAP) in order to increase renal perfusion in this context can provide a degree of renal protection. Moreover, if such an effect exists, no study has investigated whether it differs according to the use of laparoscopic or open surgery. This lack of evidence is partly because usual practice biomarkers cannot provide real-time information [22, 23]. However, new renal oxygenation monitoring technology by urinary PO₂ (PuO₂) measurement has now become available to address such limitations.

We have shown in previous studies that PuO₂ levels are a reliable marker of renal medullary oxygenation [24–26] and can be used as a real-time biomarker of acute renal stress. We also demonstrated a strong association between low PuO₂ levels and acute kidney injury in cardiac surgery patients [27]. Accordingly, in this a pilot randomized control trial, we sought to investigate the degree of physiological renal medullary stress during laparoscopic and open surgery. We hypothesized that PuO₂ would decrease in both surgery types but that such decrease would be greater in the laparoscopic group. Moreover, we hypothesized that targeting a higher MAP during the procedure would attenuate the fall in PuO₂ in both laparoscopic and open surgery groups.

Study design and ethical considerations

We performed a pilot, single-center, randomized controlled trial in a tertiary hospital in Melbourne, Australia. This study was approved by Austin Health Human Research Ethics Committee (HREC/59893/Austin-2019) and the trial was retrospectively registered on the 5th of July 2023 in the Australian New Zealand Clinical Trial Registry (ACTRN12623000726651). Informed consent was obtained from all patients during the first pre-operative visit. The study was conducted following the Declaration of Helsinki principles.

Study population

We screened all patients booked for upcoming general surgery from October 2020 to October 2022. We included all adult patients (≥ 18 years old) requiring a urinary catheter insertion as part of routine clinical care and who provided informed consent. We excluded patients with a baseline serum creatinine greater than 200 µmol/L or an estimated glomerular filtration rate according to the CKD-EPI method [28] below 30 ml/min/1.73m², patients with acute kidney injury as defined by the KDIGO consensus criteria [22], pregnant women and patient with pre-anesthetics MAP greater than 100 mmHg or lower than 65 mmHg.

Sample size

In this pilot study, we aimed to include a convenience sample of 40 patients.

Intervention

Each surgery group (laparoscopic and open) was divided into a usual MAP and a high MAP arm. In the usual MAP arm, the anesthetic team targeted a MAP between 65 and 75 mmHg, while in the high MAP arm, they targeted a MAP within 10% of the patient's pre-operative baseline or above 75 mmHg, whichever was the greater number.

Randomization

Group allocation was determined by fixed block randomization of four with a 1:1 allocation generated by a web-based computer random sequence generator (https://www.sealedenvelope.com). The randomization was stratified according to the laparoscopic or open surgery group. The treatment allocation was placed in an opaque, sealed envelope by an independent party not involved in collecting or analyzing the data and given to the clinical anesthetist.

Continuous measurement of PuO₂

The urine oximetry values were measured using a sterile fibre optic luminescence optode (NX-LAS-1/O/E-5 m, Oxford Optronix, Abingdon, UK), measuring PuO₂ every 0.6 seconds. The data were then recorded on the OxyLite^™ Pro device (Oxford Optronix, Abingdon, UK) (Supplemental Figure S1).

Outcomes

To assess the renal medullary stress during the procedure and whether it differed within the laparoscopic and open surgery groups, we studied the PuO₂ mean difference between those two surgery types among patients allocated to the control group for MAP management. Then we studied the PuO₂ slope and mean difference according to the intervention group (high vs. usual MAP management) in patients undergoing laparoscopic surgery. Finally, we evaluated if the same intervention (high MAP versus usual MAP management) was beneficial among patients who had open surgery.

Statistical analysis

Descriptive statistics were used to summarise patient characteristics for each group. Continuous variables were reported as median with interquartile range (IQR) or mean (SD) as appropriate and categorical variables as proportions. We fitted linear mixed-effect models to investigate the slope and mean PuO₂ differences between the groups. The models included random intercepts for both time and patients to account for the repeated measures nature of the data. We studied only the first 150 minutes after incision, which represented the mean surgery duration. For the exploratory analyses, we divided the time scale, if necessary, for descriptive purposes. The difference in arterial blood pressure among the groups was also assessed by linear mixed models with the same random intercepts. The model assumptions, including linearity and normality of the residuals, were checked using diagnostics plots (Supplemental Figure S2). As a sensitivity analysis, we robustly estimated the difference in area under the curves (AUC) for PuO₂ levels between the groups by a non-parametric bootstrapping procedure. This technique generated 10,000 bootstrap samples by randomly resampling our original data with replacement. For each sample, we calculated the AUC for both groups and the difference between these two values. This process generated a distribution of 10,000 bootstrapped differences in AUC from which we could determine the mean difference and construct a 95% confidence interval [29]. We calculated bias-corrected and accelerated (BCa) confidence intervals to account for any potential bias or skewness in the bootstrap distribution [30]. Statistical analyses were performed using R version 4.2.2 (R Foundation for Statistical Computing) with the packages: 'dplyr,' 'ggplot2,' 'ggpubr,' 'ggstatplot³⁰,' 'boot,' 'nlme,' 'dygraphs' and 'tableone.'

Baseline characteristics

From the 1st of October 2020 to the 31st of October 2022, we recruited a convenience sample of 43 participants, 20 of whom underwent laparoscopic surgery while 23 underwent open surgery. In each of these surgical groups, patients were further randomized to target a usual MAP or a high MAP (Fig. 1).

In the overall population, 33 (77%) were male and the median (IQR) age was 66 (55–74). The interventions were various, but mostly gastrointestinal surgeries. The median duration of surgery was 142 minutes (65–251) and was similar between the groups. There was no significant imbalance of demographic, comorbidities, or biological parameters among the four sub-groups (Table 1). The perioperative and total intravenous anesthesia drugs are presented in Supplemental Table S1.

Table 1

Baseline characteristics
	Overall n = (43)	Laparoscopic Surgery (n = 20)		Open Surgery (n = 23)
	Overall n = (43)	High MAP (n = 10)	Usual MAP (n = 10)	High MAP (n = 12)	Usual MAP (n = 11)
Demographic
Sex male \(—\) n (%)	33 (77)	8 (80)	9 (90)	10 (83)	6 (55)
Age — yrs (IQR)	66 (55–74)	69 (64–76)	56 (51–65)	65 (54–73)	66 (53–74)
Body mass index — kg.m^-2 (IQR)	26 (24–29)	28 (27–29)	26 (22–28)	26 (25–30)	26 (23–27)
Comorbidities
Chronic hypertension — n (%)	11 (26)	4 (40)	2 (20)	2 (17)	3 (27)
Coronary artery disease — n (%)	4 (9)	1 (10)	0 (0)	2 (17)	1 (9)
Chronic heart failure — n (%)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
Stroke — n (%)	2 (5)	0 (0)	2 (20)	0 (0)	0 (0)
Diabetes — n (%)	3 (7)	0 (0)	1 (10)	1 (8)	1 (9)
Obesity — n (%)	3 (7)	0 (0)	0 (0)	1 (8)	2 (18)
Depression — n (%)	3 (7)	1 (10)	0 (0)	1 (8)	1 (9)
Anxiety disorder — n (%)	3 (7)	1 (10)	0 (0)	0 (0)	2 (18)
Cognitive impairment — n (%)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
Chronic kidney disease — n (%)	2 (5)	0 (0)	0 (0)	1 (8)	1 (9)
Chronic liver impairment — n (%)	2 (5)	0 (0)	1 (10)	0 (0)	1 (9)
Autoimmune disease — n (%)	2 (5)	1 (10)	0 (0)	0 (0)	1 (9)
Biological parameters
Arterial pH	7.39 (7.34–7.45)	7.40 (7.34–7.43)	7.39 (7.32–7.44)	7.38 (7.36–7.42)	7.38 (7.34–7.46)
Arterial pCO₂ — mmHg	45 (42–49)	46 (43–48)	43 (37–51)	45 (38–48)	45 (43–51)
Arterial pO₂ — mmHg	170 (113–244)	156 (126–184)	171 (105–209)	241 (124–246)	144 (113–321)
Arterial bicarbonate — mEq.L^-1	26 (25–28)	27 (25–29)	26 (25–27)	27 (26–28)	26 (25–30)
Arterial lactate — mEq.L^-1	0.8 (0.6–1.1)	0.8 (0.6-1.0)	0.8 (0.8–0.9)	1 (0.8–1.2)	0.6 (0.6–1.2)
Serum creatinine — mg.dL^-1	0.8 (0.7-1.0)	1.0 (0.7-1.0)	0.8 (0.7–0.9)	0.7 (0.7-1.0)	0.7 (0.7–0.8)
Surgery
ASA score	3 (3–3)	3 (3–3)	30 (3–3)	3 (3–3)	3 (3–3)
Duration — min	142 (65–251)	123 (58–222)	140 (63–238)	124 (57–228)	175 (83–288)
MAP: Mean arterial blood pressure; IQR: Interquartile range; ASA score: American Society of Anesthesiologists (ASA) physical status classification Continuous values are expressed as median (IQR)

Blood pressure intervention

Metaraminol was used in 31 patients (72%) to achieve the blood pressure target, noradrenaline was used in 26% of cases, and ephedrine in 17 patients (39%). Overall, 86% required vasopressor use with a similar distribution among the four groups apart from the control group in laparoscopic surgery, in which only 7 patients (70%) required blood pressure support versus 90% in the three other groups (Supplemental Table S1).

Among patients in the laparoscopic group, the average MAP at incision was 100 (22) mmHg in the high MAP group versus 88) 15) mmHg in the control group. The mean difference across time by linear mixed modelling was 15 )2) mmHg (p < 0.001) (Supplemental Figure S2a). In the open surgery group, the mean MAP at surgery start was similar at 84 (10) mmHg vs 83 (20) mmHg in high vs usual MAP patients, respectively. However, it became significantly higher during the procedure (14 ± 1 mmHg mean difference) in the high MAP group vs the usual MAP group (p < 0.001) (Supplemental Figure S2b).

PuO₂ changes in laparoscopic and open surgery under usual blood pressure target

To compare the PuO₂ in the two types of surgeries, we focused on the usual MAP group of each surgery type. Both developed an increase in PuO₂ within 10 minutes after incision reaching similar peak values (77 mmHg in open surgery vs 74 mmHg in laparoscopic surgery) before decreasing. After this peak, the PuO₂ decreased in both procedure types but with different trends. In the laparoscopic group, the PuO₂ showed a sharper decrease within the first hour after incision and remained steady, while the decline was smoother and progressive in open surgery patients (Fig. 1). The decrease from baseline to the end of measurement was similar between the two surgery types (-49% in open surgery vs. -51% in laparoscopic surgery). Regarding the mean difference over time, however, open surgery patients experienced higher PuO₂ values during the analysis period (mean difference of 11 ± 1 mmHg, p < 0.001).

PuO₂ changes in laparoscopic surgery according to blood pressure target

PuO₂ changes during the overall analysis period

During laparoscopic surgery, the mean PuO₂ was similar between groups at incision with a mean value of 62 (40) mmHg in the high MAP versus 62 (26) mmHg in the controls. However, during the procedure, the PuO₂ was, on average, 7 (1) mmHg lower in the usual MAP group than in the higher MAP group. The usual MAP group also showed a significantly steeper decline in PuO₂ over time, with a slope of -0.08 (p < 0.001) (Fig. 2, Supplemental Figure S3).

PuO₂ changes during different timeframes

During the first ten minutes after incision, the trend in PuO₂ showed a sharp increase in the usual MAP group, reaching a peak of 74 mmHg at 8 minutes, while it almost instantly decreased in the high MAP group (p = 0.01). The mean PuO₂ was also significantly higher in the usual MAP group during this period (mean difference: 10 ± 4 mmHg, p < 0.001). However, after the first 10 minutes, this relationship was reversed with a more negative slope in the usual MAP group (-0.08, p < 0.001). Thus, the mean value of PuO₂ was 35 mmHg in the higher MAP versus 43 mmHg in the usual MAP group (mean difference of 8 ± 1 mmHg, p < 0.001) (Fig. 2, Supplemental Figure S3).

PuO₂ changes in open surgery according to blood pressure target

At incision, baseline PuO₂ differed significantly between the high MAP and usual MAP groups (73 mmHg in the control group versus 52 mmHg in the high MAP group). This higher PuO₂ in the usual MAP group progressively declined over time compared to the high MAP group, in which the PuO₂ trend sharply decreased at 20 minutes (Fig. 3). The overall mean difference between the two groups remained in favour of the usual MAP target (7 ± 1 mmHg, p < 0.001) (Supplemental Figure S3).

Robustness of findings

Bootstrapping analyses of AUC differences aligned with our findings for PuO₂ evolution during laparoscopic surgery, suggesting that the PuO₂ improvements in the high MAP group were robust. The bootstrapping findings computed for all our exploratory analyses showed similar results (Supplemental Table S2, Supplemental Figures S4-6)

Key findings

In a pilot randomized trial, we investigated the impact of blood pressure targeting on PuO₂ changes during laparoscopic or open surgery. Firstly, we found that both surgical approaches were associated with a rapid and profound decrease in PuO₂. Secondly, we showed that the PuO₂ decrease was greater with laparoscopic surgery compared to open surgery. Finally, we found that targeting a higher blood pressure in patients undergoing laparoscopic surgery attenuated such a decrease in PuO_2, but a higher MAP target had the opposite effect in open surgery patients.

Comparison to previous studies

Our findings build upon previous physiological data and contribute novel insights to the current renal perfusion body of literature. Indeed, previous retrospective studies have reported a potential risk of AKI associated with laparoscopic surgery [21, 31–33]. Here, we provide physiological clues to support the potential hazards of laparoscopic surgery, showing a rapid and substantial decrease in PuO₂ during laparoscopic procedures. However, some studies also reported lower acute kidney injury incidence in laparoscopic patients than in open surgery [34–36]. As we showed, open surgery is not free from renal medullary stress: although the fall appeared less sharp in open surgery, the PuO₂ still consistently decreased over time. This observation is aligned with the previously reported association between postoperative complications and surgery duration [37]. Our study also builds upon the growing body of literature around the utility of continuous PuO₂ monitoring as a surrogate of renal medullary PO₂ which provides unique physiological insights [38, 39]. Future real-time physiological monitoring studies with interventions in response to PuO₂ may help improve renal protection.

Implications of study findings

Our findings imply that both laparoscopic and open surgery induces a degree of hypoxic renal medullary stress. They also imply that the timing, pattern and intensity of medullary stress differ according to the laparoscopic versus the open approach. Finally, they suggest that targeting a higher MAP during laparoscopy surgery may decrease such medullary stress. In contrast, they suggest that targeting a higher MAP may increase medullary stress during open surgery.

Strengths and limitations

Our study has several strengths. First, it is based on a randomized control design, which allowed us to compare the surgery categories and the intervention groups with limited confounders and minimized selection bias. Second, we collected continuous measurements, which allowed us to provide accuracy in describing complex physiological phenomena and markedly minimized ascertainment bias. Finally, we validated our observations with two independent statistical tools, confirming our results, which increased the robustness of our observations.

Nonetheless, we acknowledge some limitations. First, the sample size of our physiological study was not designed to show differences in clinical outcomes, such as acute kidney injury incidence. Therefore, the analysis of biomarkers of renal injury and their correlation with medullary oxygenation in these situations should be investigated in future studies. Second, due to the single-centre nature and limited sample size of our investigation, our results are only hypothesis generating, provide the framework for further investigations and cannot be considered for translation into practice. Third, we did not collect data on urinary output for all patients. This could have provided additional information on kidney function concerning PuO₂. However, we previously investigated these questions in pre-clinical and human previous studies [24, 26, 38]. Finally, the PuO₂ difference at incision between usual and high MAP targets among the patients undergoing open surgery is a confounder and may be due to the variability related to the small sample size of the groups.

Our physiological study found that both laparoscopic and open surgery are associated with impaired renal medullary oxygenation but to a greater extent in the laparoscopic group. Higher blood pressure targets may reduce medullary hypoxic stress in patients undergoing laparoscopic surgery but may increase such stress in those having open surgery. Further investigations are needed to confirm these findings, explore the complex relationship between blood pressure targets, surgical procedures, and renal oxygenation and guide future investigations aiming to personalize renal protective perioperative management strategies.

Acknowledgements

We acknowledge research support from Austin Health Hospital and the work of all staff in supporting the health system and their patients.

Details of authors' contributions

Research idea and study design: DH, RB; data acquisition: DH, HS; data analysis/interpretation: all authors; supervision or mentorship: DH, CF, and RB Each author contributed important intellectual content during manuscript drafting or revision and accepted accountability for the overall work by ensuring that questions about the accuracy or integrity of any portion of the work are appropriately investigated and resolved.

Availability of data and material

The study protocol, data set and statistical code are available from the corresponding author on reasonable request.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Declaration of interest

The authors declare having no conflict of interest to declare.

Registration number: ACTRN12623000726651

Date of registration: 05/07/2023 (retrospectively registered)

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No competing interests reported.

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02 Aug, 2023
First submitted to journal
02 Aug, 2023

You are reading this latest preprint version

Renal Medullary Oxygenation during Laparoscopic vs Open Surgery: The Impact of Blood Pressure Management. A pilot randomized controlled trial

Status:

Journal Publication

Version 1

Abstract

Purpose

Methods

Results

Conclusion

Figures

Implication statement

Introduction

Methods

Study design and ethical considerations

Study population

Sample size

Intervention

Randomization

Continuous measurement of PuO2

Outcomes

Statistical analysis

Results

Baseline characteristics

Blood pressure intervention

PuO2 changes in laparoscopic and open surgery under usual blood pressure target

PuO2 changes in laparoscopic surgery according to blood pressure target

PuO2 changes during the overall analysis period

PuO2 changes during different timeframes

PuO2 changes in open surgery according to blood pressure target

Robustness of findings

Discussion

Key findings

Comparison to previous studies

Implications of study findings

Strengths and limitations

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1

Continuous measurement of PuO₂

PuO₂ changes in laparoscopic and open surgery under usual blood pressure target

PuO₂ changes in laparoscopic surgery according to blood pressure target

PuO₂ changes during the overall analysis period

PuO₂ changes during different timeframes

PuO₂ changes in open surgery according to blood pressure target