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Abstract

Objectives

To compare the urine output and estimated glomerular filtration rate (eGFR) of patients postoperatively administered sugammadex or glycopyrrolate 7 days following kidney transplantation (KT).

Methods

We retrospectively enrolled 134 consecutive patients who underwent KT under general anesthesia. Their urine output and eGFR were recorded every 24 hours between postoperative day (POD) 1 and 7. We used regression analysis to evaluate the relationship between the reversal agent administered and the outcomes of the participants.

Results

The urine output and eGFR of the participants did not differ between the two groups. Multivariate analysis showed that body mass index (BMI) (odds ratio (OR) 1.21; 95% confidence interval (CI) 1.05–1.40), diabetes mellitus (OR 3.14; 95% CI 1.07–9.16), neurovascular disease (OR 7.00; 95% CI 1.61–30.42), and the duration of surgery (OR 1.01; 95% CI 1.00–1.01) were associated with lower urine output on POD 7. In addition, only BMI (OR 1.25; 95% CI 1.09–1.42) was associated with low eGFR on POD 7.

Conclusions

The urine output and eGFR of patients administered sugammadex or glycopyrrolate following KT did not differ 7 days later. Moreover, glycopyrrolate does not affect urine output or eGFR on POD 7, according to multivariate regression analysis.

Keywords

Glycopyrrolate kidney function kidney transplantation sugammadex urine output estimated glomerular filtration rate urinary retention

Introduction

Glycopyrrolate prevents the muscarinic effects of the cholinesterase inhibitors that are used to reverse neuromuscular blockade at the end of general anesthesia. However, it also blocks detrusor contractions and causes bladder hypotonia, resulting in urinary retention.¹ Therefore, to reduce the incidence of postoperative urinary retention (POUR), sugammadex has previously been used as the reversal agent.^2–4

The United States Food and Drug Administration does not recommend the use of sugammadex in patients with renal impairment because of its pharmacokinetic properties. However, a previous study showed that it can be used safely in patients with end-stage renal disease.⁵ Furthermore, in an analysis of patients who underwent kidney transplantation (KT), there was no additional risk of adverse effects of sugammadex on graft function, and a superior recovery profile was achieved, compared with that using a cholinesterase inhibitor plus glycopyrrolate.^6–8

Urine production begins soon after successful anastomosis and reperfusion during KT. The urine volume produced positively correlates with the serum creatinine concentration of patients soon after KT, and is related to early graft function.⁹ In addition, the urine output on postoperative day (POD) 7 is predictive of graft function during the first year following surgery.¹⁰

In the present study, we compared the urine output and estimated glomerular filtration rate (eGFR) on POD 7 of patients who were administered sugammadex or a cholinesterase inhibitor plus glycopyrrolate for the reversal of neuromuscular blockade following KT. In addition, we aimed to identify the factors associated with urine output and renal function, assessed using the estimated glomerular filtration rate (eGFR).

Materials and methods

We retrospectively collected data for patients who underwent KT between February 2016 and July 2021 at Soonchunhyang University Hospital Seoul and Soonchunhyang University Hospital Bucheon, Republic of Korea. This retrospective observational study was approved by the Institutional Review Board of Soonchunhyang University Hospital (approval numbers: SCHUH2021-09-011 and SCHBC2022-03-003). The necessity for written informed consent was waived because of the retrospective, case–control nature of the study. The findings are presented according to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines.¹¹ The procedures used complied with the relevant guidelines and regulations.

Study sample

We retrospectively enrolled consecutive adult patients who underwent KT under general anesthesia. Of these, patients who experienced postoperative hemodialysis within the study period, underwent simultaneous liver and kidney transplantation, or died during the period to July 2021 were excluded.

Data collection

The medical records of the participants were retrospectively reviewed and information regarding the general characteristics, durations of anesthesia and surgery, the type of anesthesia, the type of donor, and the perioperative drugs administered was extracted. The urine output and eGFR of the participants were recorded every 24 hours between POD 1 and 7.

Management of the anesthesia

The clinical characteristics of the participants, including their underlying diseases, body mass index (BMI), and history of KT were recorded on pre-anesthetic evaluation forms. General anesthesia was maintained using a volatile anesthetic (desflurane or sevoflurane) or total intravenous anesthesia (TIVA). Neuromuscular blockade was achieved and maintained using rocuronium during KT. The doses of volatile anesthesia and TIVA delivered were adjusted to achieve a target bispectral index between 40 and 60. The participants were intravenously administered ephedrine (4 mg), phenylephrine (50 μg), or a continuous infusion of dopamine or norepinephrine, as required, to maintain mean arterial blood pressures of >70 mmHg during surgery and >100 mmHg after reperfusion. Perioperative fluids were administered to maintain a central venous pressure of 10 to 15 mmHg, while avoiding volume overload. Before reperfusion, all the participants were intravenously administered ≥40 mg of furosemide, as required, and 15% mannitol (1.0 g/kg), as well as solumedrol (500 mg). Some were also administered a low-dose infusion of dopamine (LDD) (3 µg/kg/minute) to prevent ischemic reperfusion injury (IRI), and all were administered intravenous fentanyl (0.3–0.5 µg/kg) when the skin was closed.

At the end of the surgical procedure, the neuromuscular blockade was reversed using either an intravenously administered cholinesterase inhibitor (0.2 mg/kg of pyridostigmine or 0.05 mg/kg of neostigmine) plus glycopyrrolate (5 µg/kg) or with sugammadex (1–2 mg/kg). Tracheal extubation was performed when the train-of-four ratio was >0.9.

Specific agents were used during anesthesia at the discretion of the anesthesiologist assigned to each participant.

Outcomes

Previous studies have shown that a urine output <36 mL/kg/day and an eGFR <60 mL/minute/1.73 m² are associated with poor graft function.¹² Therefore, we set these values as the outcomes. Urine output was recorded every 24 hours, beginning the day after KT. We used the Chronic Kidney Disease Epidemiology Collaboration equation to calculate eGFR.

Statistical analysis

The primary outcome of the study was a low urine output, defined as <36 mL/kg/day, on POD 7. The secondary outcome was a low eGFR, defined as <60 mL/minute/1.73 m², on POD 7. We used regression analysis to evaluate the relationship between the reversal agents used and the outcomes. The variables used in the multivariate models to predict low urine output or eGFR were those identified as significant predictors (P < 0.10) on univariate analysis and those that had previously been demonstrated to be important.¹⁰ The Shapiro–Wilk test was used to test the normality of the distributions of continuous datasets. Continuous data are summarized as mean ± standard deviation (SD) or median (interquartile range, IQR), and categorical datasets are reported as frequency (percentage). Categorical datasets were compared using the chi-square or Fisher’s exact tests, and continuous datasets were compared using Student’s t-test. For non-parametric repeated measures analysis, a generalized estimating equation was used to construct marginal models for the effects of drugs and POD on urine output and eGFR. We also included an interaction factor for drug and POD, and compensated for multiple testing using the sequential Sidak method. We performed univariate and multivariate analyses to explore the relationships of urine output and eGFR with other clinical variables. R software (version 3.6.3; The R Foundation for Statistical Computing, Vienna, Austria) and SPSS version 26 (IBM Corp., Armonk, N.Y., USA) were used for statistical analyses. P < 0.05 was considered to represent statistical significance.

Results

Characteristics of the participants

Of the 142 patients identified who underwent KT during the study period, eight were excluded because they underwent postoperative hemodialysis before POD 7 owing to anuria (five), underwent simultaneous liver and kidney transplantation (two), or died (one). Thus, data from 134 participants were included in the analysis. No significant differences in the characteristics of the participants the sugammadex and glycopyrrolate groups were identified (Table 1).

Table 1.

Characteristics of the participants.

Characteristic	Sugammadex group (n = 65)	Glycopyrrolate group (n = 69)	P-value
Sex (male/female)	35 (53.85%)/30 (46.13%)	42 (60.87%)/27 (39.13%)	0.52
Age (years)	48.97 ± 11.15	48.62 ± 11.76	0.86^†
BMI (kg/m²)	22.30 ± 3.75	22.81 ± 3.29	0.41^†
Hypertension	59 (90.77)	65 (94.20)	0.52^‡
Cardiovascular disease	12 (18.46)	19 (27.54)	0.23
Neurovascular disease	4 (6.15)	9 (13.04)	0.24
Diabetes mellitus	23 (35.38)	23 (33.33)	0.86
Respiratory disease	4 (6.15)	4 (5.80)	1.00^‡
Other diseases	17 (26.15)	11 (15.94)	0.20
Previous KT	3 (4.62)	3 (4.35)	1.00^‡

Continuous variables are reported as mean ± standard deviation and categorical variables are reported as n (%).

Data were analyzed using the ^†t-test, chi-square test, or ^‡Fisher’s exact test.

BMI, body mass index; KT, kidney transplantation.

Perioperative parameters

Table 2 shows the durations of anesthesia and surgery, the type of anesthesia administered, the type of donor, and the drugs administered perioperatively for the participants in each group. There were no differences between the groups, except with respect to the amount of LDD infused to prevent IRI (smaller in the Sugammadex group; P = 0.01) and the intraoperative dose of furosemide (higher in the Sugammadex group; P = 0.001).

Table 2.

Perioperative data.

	Sugammadex group (n = 65)	Glycopyrrolate group (n = 69)	P-value
Duration of anesthesia (minute)	311.62 ± 76.58	321.19 ± 73.76	0.46^‡
Duration of surgery (minute)	245.91 ± 64.94	238.62 ± 67.71	0.53^†
Type of anesthesia			0.74^‡
Desflurane	49 (75.38)	49 (71.01)
Sevoflurane	1 (1.54)	3 (4.35)
TIVA	15 (23.08)	17 (24.64)
Type of donor			0.29
Living donor	44 (67.69)	40 (57.97)
Dead donor	21 (32.31)	29 (42.03)
Inotropic agent used
Ephedrine dose (mg)	13.07 ± 16.59	11.12 ± 14.91	0.47^†
Dopamine infusion (μg/kg/min)	2 (3.08)	1 (1.45)	0.61^‡
Vasoactive agent used
Phenylephrine dose (μg)	89.41 ± 278.21	82.31 ± 270.91	0.88^†
Norepinephrine infusion (μg/kg/min)	2 (3.08)	3 (4.35)	1.00^‡
LDD to prevent IRI	1 (1.54)	12 (17.39)	0.01
Intraoperative furosemide dose	82.38 ± 49.67	59.13 ± 31.10	0.001

Continuous variables are reported as mean ± standard deviation and categorical variables are reported as n (%).

Data were analyzed using the ^†t-test, chi-square test, or ^‡Fisher’s exact test.

IRI, ischemia-reperfusion injury; LDD, low-dose dopamine; TIVA, total intravenous anesthesia.

Postoperative urine output and eGFR between POD 1 and 7

Figure 1 shows the postoperative urine outputs and eGFRs of the participants between POD 1 and 7. The urine outputs of the Glycopyrrolate group were significantly lower than those of the Sugammadex group on PODs 6 (P = 0.03) and 7 (P = 0.03). In addition, the eGFRs of the Glycopyrrolate group were significantly lower than those of the Sugammadex group on PODs 5 (P = 0.01), 6 (P = 0.01), and 7 (P = 0.03). However, non-parametric repeated measures analysis showed no differences in the urine output or eGFR of the two groups (Table 3).

Figure 1.

Postoperative urine output and eGFR of the participants on postoperative days 1 to 7. Data are mean ± standard deviation and were analyzed using the t-test. N = 65 and 69 for the Sugammadex and Glycopyrrolate groups, respectively.

Table 3.

Postoperative urine output and eGFR from POD 1 to 7.

	Sugammadex group (n = 65)	Glycopyrrolate group (n = 69)	P-value
Urine output (mL/kg/day)
POD 1	68.06 (43.47, 94.82)	71.43 (48.64, 107.69)	0.988
POD 2	76.99 (51.65, 106.2)	85.73 (59.08, 127.91)	0.989
POD 3	69.82 (46.87, 98.34)	80.37 (54.23, 102.74)	0.932
POD 4	69.66 (48.7, 95.57)	80.78 (54.22, 106.64)	0.982
POD 5	64.73 (41.91, 82.00)	70.98 (50.79, 99.28)	0.932
POD 6	61.12 (40.56, 80.31)	68.7 (46.19, 89.89)	0.932
POD 7	57.33 (38.96, 74.34)	64.57 (43.04, 90.33)	0.742
eGFR (mL/minute/1.73 m²)
POD 1	13.96 (9.18, 18.88)	14.33 (9.11, 20.46)	0.997
POD 2	31.4 (18.55, 51.27)	34.64 (17.50, 54.54)	0.997
POD 3	45.63 (27.14, 65.15)	50.13 (31.00, 67.67)	0.966
POD 4	53.02 (31.62, 68.22)	62.29 (42.03, 77.45)	0.694
POD 5	55.82 (38.87, 69.96)	71.96 (48.46, 82.44)	0.245
POD 6	57.68 (44.24, 69.01)	70.81 (52.40, 84.93)	0.214
POD 7	56.17 (42.54, 69.01)	68.62 (47.17, 82.36)	0.416

The data are continuous variables and are reported as median (interquartile range).

A generalized estimating equation was used, and multiple comparisons were performed using the sequential Sidak method.

eGFR, estimated glomerular filtration rate; POD, postoperative day.

Results of the univariate and multivariate analyses to identify factors associated with postoperative urine output after the removal of the indwelling urinary catheter

Univariate analysis showed that BMI (odds ratio [OR] 1.27; 95% confidence interval [CI] 1.07–1.50), diabetes mellitus (DM) (OR 3.15; 95% CI 1.02–9.75), neurovascular disease (OR 7.54; 95% CI 1.51–37.68), and the duration of surgery (OR 1.01; 95% CI 1.00–1.01) significantly affected the urine output of the participants on POD 7 (Table 4). Similarly, multivariate analysis showed that BMI (OR 1.21; 95% CI 1.05–1.40), DM (OR 3.14; 95% CI 1.70–9.16), neurovascular disease (OR 7.00; 95% CI 1.61–30.42), and the duration of surgery (OR 1.01; 95% CI 1.00 to 1.01) were associated with lower urine output on POD 7.

Table 4.

Results of the univariate and multivariate analyses to identify factors associated with the postoperative urine output after removing the indwelling urinary catheter on POD 7.

	Univariable analysis		Multivariable analysis
	OR (95% CI)	P-value	OR (95% CI)	P-value
Glycopyrrolate	0.76 (0.24–2.43)	0.65	1.04 (0.39–2.76)	0.93
Sex (female)	2.57 (0.80–8.32)	0.11
Age	1.02 (0.97–1.07)	0.50
BMI	1.27 (1.07–1.50)	0.005	1.21 (1.05–1.40)	0.01
Hypertension	2.31 (0.14–37.00)	0.56
Diabetes mellitus	3.15 (1.02–9.75)	0.047	3.14 (1.07–9.16)	0.04
Neurovascular disease	7.54 (1.51–37.68)	0.01	7.00 (1.61–30.42)	0.01
Previous KT	4.90 (0.38–63.77)	0.22
Living donor	0.32 (0.10–1.06)	0.06	0.39 (0.13–1.18)	0.09
Sevoflurane	<0.001 (0–inf.)	0.99
TIVA	0.43 (0.14–1.37)	0.15
Duration of surgery	1.01 (1.00–1.01)	0.02	1.01 (1.00–1.01)	0.04
Inotropic agent used
Ephedrine dose	0.99 (0.96–1.03)	0.75
Dopamine infusion	<0.001 (0–inf.)	0.99
Intraoperative vasoactive agent used
Phenylephrine dose	1.00 (1.00–1.00)	0.73
Norepinephrine infusion	0.94 (0.10–8.72)	0.95
LDD to prevent IRI	1.47 (0.23–9.42)	0.68	1.42 (0.20–10.45)	0.73
Intraoperative furosemide	0.99 (0.98–1.00)	0.19	0.99 (0.98–1.01)	0.36

Wald confidence intervals were calculated.

BMI, body mass index; CI, confidence interval; IRI, ischemia-reperfusion injury; KT, kidney transplantation; LDD, low-dose dopamine; OR, odds ratio; POD, postoperative day; TIVA, total intravenous anesthesia; inf., infinity.

Results of the univariate and multivariate analyses to identify factors associated with eGFR on POD 7

Univariate analysis showed that BMI (OR 1.21; 95% CI 1.04–1.40) and a living donor (OR 0.40; 95% CI 0.17–0.97) significantly affected the eGFR of the participants on POD 7 (Table 5). However, multivariate analysis showed that only BMI (OR 1.25; 95% CI 1.09–1.42) was associated with lower eGFR on POD 7.

Table 5.

Results of the univariate and multivariate analyses to identify factors associated with eGFR on POD 7.

	Univariable analysis		Multivariable analysis
	OR (95% CI)	P-value	OR (95% CI)	P-value
Glycopyrrolate	2.24 (0.92–5.42)	0.075	2.00 (0.86–4.65)	0.11
Sex (female)	0.76 (0.32–1.83)	0.55
Age	0.99 (0.96–1.03)	0.68
BMI	1.21 (1.04–1.40)	0.009	1.25 (1.09–1.42)	0.001
Hypertension	1.79 (0.32–10.06)	0.51
Diabetes mellitus	0.47 (0.19–1.17)	0.10	0.45 (0.18–1.08)	0.07
Neurovascular disease	0.98 (0.25–3.77)	0.97	0.89 (0.21–3.68)	0.87
Previous KT	0.65 (0.09–4.70)	0.67
Living donor	0.40 (0.17–0.97)	0.04	0.47 (0.20–1.09)	0.08
Sevoflurane	2.94 (0.30–29.25)	0.36
TIVA	0.76 (0.34–1.70)	0.51
Duration of surgery	1.00 (1.00–1.01)	0.24	1.00 (1.00–1.01)	0.21
Inotropic agent used
Ephedrine dose	0.99 (0.96–1.02)	0.43
Dopamine infusion	0.50 (0.04–5.65)	0.58
Intraoperative vasoactive agent used
Phenylephrine dose	1.00 (1.00–1.00)	0.74
Norepinephrine infusion	1.55 (0.25–9.57)	0.64
LDD to prevent IRI	2.57 (0.40–16.14)	0.31	3.15 (0.61–16.39)	0.17
Intraoperative furosemide	1.01 (1.00–1.02)	0.06	1.01 (1.00–1.02)	0.08

Wald confidence intervals were calculated.

BMI, body mass index; CI, confidence interval; eGFR, estimated glomerular filtration rate; IRI, ischemic reperfusion injury; KT, kidney transplantation; LDD, low-dose dopamine; OR, odds ratio; POD, postoperative day; TIVA, total intravenous anesthesia.

Discussion

In this retrospective observational study, we found that glycopyrrolate did not affect the urine output or eGFR of patients on POD 7 following KT. However, BMI, DM, neurovascular disease, and the duration of surgery were associated with a lower urine output on POD 7; and BMI was associated with eGFR on POD 7.

The function of the primary transplanted graft affects the duration of survival of the graft in patients who undergo KT. The GFR is the best overall index of renal function, and can be used to evaluate the efficacy of therapy in patients with renal disease. However, the GFR must be estimated on the basis of creatinine clearance because it cannot be measured directly.¹³ In contrast, urine output is a direct and simple method of identifying acute kidney injury.¹⁴ Some previous studies have shown that a high urine volume during the first few PODs is a useful predictor of early graft outcomes.^15,16 In addition, the urine output on POD 7 might represent an easy and non-invasive means of assessing the risk of subsequent renal dysfunction.¹⁰

POUR is a common postoperative complication of anesthesia and surgery, and has reported incidences of 5% to 70%.¹⁷ Sometimes, POUR continues for 4 to 6 weeks.¹⁸ Numerous factors affect the incidence of POUR, including the age and sex of the patient, the type of surgery performed, the comorbidities present, the drugs administered, the intravenous fluids administered, the duration of surgery, and various anesthesia-related parameters.¹ Glycopyrrolate use has been reported to be a risk factor for POUR because it blocks muscarinic receptors in the detrusor muscle, causing bladder hypotonia.¹⁹

The use of sugammadex is associated with a lower incidence of POUR because the use of glycopyrrolate can be avoided.² Although the kidney is responsible for the excretion of the rocuronium-sugammadex complex, sugammadex administration does not affect relevant kidney recovery outcomes following KT.²⁰ Carron et al. showed that sugammadex reduces the postoperative incidence of respiratory complications, enables faster discharge to the ward, and is associated with fewer intensive care unit admissions and superior kidney function following KT.⁸ In the present study, adjusted multivariate analysis did not show an effect of sugammadex on urine output or eGFR on POD 7.

In the present study, the dopamine infusion needed to prevent IRI was defined as an LDD (2–5 µg/kg/minute) infusion and was administered during the perioperative period to hemodynamically stable patients at the discretion of the attending anesthesiologist. LDD was used for its documented renoprotective effect.²¹ A previous study showed that LDD infusion improves the renal plasma flow, creatinine clearance, and total urinary sodium excretion of KT recipients,²² whereas another study showed no improvement in their hemodynamics or kidney function.²³ In the present study, the number of patients who were administered an LDD infusion to prevent IRI significantly differed between the two groups, but multivariate analysis did not show a significant relationship with urine output or eGFR.

The risk factors associated with poor outcomes following KT have been shown to be recipient BMI, hypertension, DM, ischemic heart disease, cerebrovascular accident, and the duration of renal replacement therapy.²⁴ A high BMI has also been shown to be associated with delayed graft function.²⁵ However, although BMI was found to be associated with urine output and eGFR on POD 7 in the present study, it might be difficult to apply this finding because we did not categorize the participants as underweight, normal, overweight, or obese using BMI. DM, neurovascular disease, and the duration of surgery were found to be associated with lower urine output on POD 7, as reported previously.^24,26

Some limitations of the present study should be discussed. First, in common with most retrospective observational studies, the data were incomplete, and this may have introduced bias into the results. Second, an indwelling urinary catheter is used in the treatment of POUR, and the participants had indwelling urinary catheters until POD 4, which may have masked the presence of POUR. However, POUR can persist after the removal of the indwelling urinary catheter, and differences in urine output began to appear on POD 6 in the present study. Third, urinary retention does not reflect renal function; however, it impairs renal blood flow, which might affect GFR.²⁷

In conclusion, the urine output and eGFR of patients that are administered sugammadex or glycopyrrolate do not differ on POD 7. In addition, glycopyrrolate does not affect the urine output or eGFR of patients on POD 7 following KT, according to the results of multivariate regression analysis. However, additional prospective investigations should be performed to confirm the present findings.

Footnotes

Author contributions

BSK and SYP: writing – original draft; SHK, YSJ, and YHW: data analysis; SS and JHY: writing – review & editing; MGK and JWC: data curation; HBC: supervision and conceptualization. All the authors contributed to the article and approved the submitted version.

Declaration of conflicting interests

The authors declare that there is no conflict of interest.

Funding

This research was supported by the Soonchunhyang University Research Fund and the Korean Society of Transplantation Anesthesiologists (grant no. KSTA-2021-02).

ORCID iD

Ho Bum Cho

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Effect of glycopyrrolate on the postoperative urine output of patients following kidney transplantation: a retrospective observational study

Abstract

Objectives

Methods

Results

Conclusions

Keywords

Introduction

Materials and methods

Study sample

Data collection

Management of the anesthesia

Outcomes

Statistical analysis

Results

Characteristics of the participants

Perioperative parameters

Postoperative urine output and eGFR between POD 1 and 7

Results of the univariate and multivariate analyses to identify factors associated with postoperative urine output after the removal of the indwelling urinary catheter

Results of the univariate and multivariate analyses to identify factors associated with eGFR on POD 7

Discussion

Footnotes

Author contributions

Declaration of conflicting interests

Funding

ORCID iD

References