Fluid management during pediatric lung transplantation: a single-center experience

Introduction

Lung transplantation (LTx) is a highly specialized and effective treatment for end-stage lung disease (1). The first successful pediatric LTx was performed in 1987 at the University of Toronto (2). Although LTx procedures have been conducted for over 40 years, pediatric cases remain rare due to scarcity of size-matched donors, high operational and anesthesia requirements, complex pathophysiology, and the need for extracorporeal life support (ECLS). Reports on anesthesia management in pediatric LTx are scarce, and anesthesiologists working with this specific population must focus on assessing cardiopulmonary function, fluid balance, reperfusion injury, and ECLS.

Fluid management in LTx remains a critical challenge for anesthesiologists, particularly in pediatric patients who have a lower systemic blood volume and require more precise fluid regulation. Studies indicate that excessive intraoperative fluid administration increases the risk of pulmonary edema and primary graft dysfunction (PGD) (3-5), negatively affecting patient outcomes. However, the benefits of maintaining a “negative balance” to achieve a “drier” state remain uncertain, as excessive fluid restriction may lead to inadequate tissue perfusion and associated complications. International consensus guidelines recommend balancing perfusion pressure and cardiac output while minimizing fluid and blood transfusions, particularly to preserve renal function (5). Despite these recommendations, no standardized criteria exist for restrictive fluid replacement in LTx. In long surgical procedures, multiple interacting factors can influence fluid balance, leading to varying physiological outcomes. The effects of intraoperative fluid balance on the prognosis of pediatric LTx patients remain unclear, making its assessment a crucial consideration for anesthesiologists and surgeons, especially when implementing restrictive fluid therapy.

The absence of consensus recommendations for managing children with end-stage lung disease presents significant challenges, particularly in intraoperative fluid management (6). Due to the limited number of medical centers worldwide capable of routinely performing pediatric LTx (7), experience in this area remains scarce. In this study, we conducted a retrospective analysis of 20 pediatric LTx cases at our center to examine the impact of intraoperative fluid balance on post-transplant complications and to share our insights on fluid management in this specialized population. We present this article in accordance with the STROBE reporting checklist (available at https://tp.amegroups.com/article/view/10.21037/tp-2024-619/rc).

Methods

Patients

We reviewed the clinical data of 20 pediatric patients who underwent LTx from July 2019 to August 2023 at The Second Affiliated Hospital of Zhejiang University School of Medicine. Our analysis focused on the most recent case, involving a child who underwent unilateral LTx 23 months after a prior bilateral LTx. Ethical approval for this study was obtained from the Human Body Research Ethics Committee of The Second Affiliated Hospital of Zhejiang University School of Medicine (No. 2022-0352). This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Due to the retrospective observational nature of the study, the requirement for written informed consent was waived.

Anesthetic management

Children without preoperative tracheal intubation were given oxygen via masks immediately after admission into the operating room. Routine monitoring was performed, while invasive arterial blood pressure monitoring and peripheral venous access were rapidly established. All children received a standardized anesthesia regimen, which included propofol (1.5–2.5 mg/kg), midazolam (0.05–0.1 mg/kg), fentanyl (4–6 µg/kg) or sufentanil (0.5–1 µg/kg), and rocuronium bromide (0.6–0.9 mg/kg) or cisatracurium (0.1–0.3 mg/kg).

Anesthesia was maintained using a sedation-aspiration combination approach, incorporating continuous infusions of propofol (9–15 mg/kg/h), sufentanil (1–2 µg/kg/h), and cisatracurium (0.06–0.12 mg/kg/h), while the sevoflurane inhalation concentration was maintained between 0% and 2%. The depth of anesthesia was adjusted based on continuous monitoring of the electroencephalogram bispectral index (Covidien LLC, USA). An ultrasound-guided central venous catheter (B. Braun Melsungen AG, Germany) was inserted into the left internal jugular vein to establish central venous access and measure the central venous pressure (CVP). The central venous catheter was inserted into the right jugular vein, and pulmonary artery catheterization (Bioptimal International Pte. Ltd, Singapore) was performed.

The mean arterial pressure (MAP) and CVP serve as key indicators of blood volume and vascular tone. Intraoperative transesophageal echocardiography (TEE) is essential for evaluating cardiac function, chamber size, and ventricular wall motion, providing valuable guidance for fluid management and vasoactive agent administration (3). Hence, MAP, CVP, and TEE are collectively used for volume monitoring in pediatric patients without ECLS. For children receiving extracorporeal membrane oxygenation (ECMO) support, ECMO flow becomes a crucial parameter for assessing active circulating blood volume (ACBV). At our center, we recommend maintaining an ECMO flow of 80–100 mL/kg. Additionally, MAP is used as a guide for determining fluid infusion requirements, with a recommended target of at least 50–60 mmHg during ECMO support.

We predominantly used Ringer’s acetate solutions and saline during the procedure, as the infusion of Ringer’s lactate solution can lead to lactate accumulation. Red blood cells (RBCs) were transfused when hemoglobin was <8.0 g/dL. However, a higher transfusion threshold was considered depending on the patient’s hemodynamic status, blood loss, and surgical complications. To optimize intraoperative coagulation management, we utilized thromboelastography (TEG) to monitor coagulation factors and platelet function. This guided the administration of fresh frozen plasma (FFP), platelets, fibrinogen, and prothrombin complex as needed.

Assessment of fluid overload (FO)

The restrictive fluid strategy is characterized by prioritizing vasopressor use while administering lower intravenous fluid volumes (8). Fluid intake includes blood products (such as RBCs, frozen plasma, and albumin), crystalloids (such as Ringer’s acetate solutions, Ringer’s lactate solutions, and saline), and artificial colloids. Fluid output includes hemorrhage, urine, and ultrafiltration fluids. Therefore, we recalculated the fluid balance in pediatric LTx patients as follows: Fluid balance% = [(Fluid intake − Fluid output)/admission weight (kg)] × 100% (9). Based on previous literature, FO is defined as a fluid balance percentage ≥10% (10).

Outcome definitions

PGD was assessed by X-imaging and the ratio of partial oxygen pressure to the fraction of inspired oxygen (PaO₂/FiO₂) in arterial blood gases. A grade 3 PGD was assigned if the X-ray revealed pulmonary edema with a PaO₂/FiO₂ <200, or if ECMO support was combined with bilateral pulmonary edema on X-ray (11). PaO₂ and FiO₂ values were recorded at four time points: T0, T24, T48, and T72. PGD was independently evaluated by two physicians with extensive experience in LTx treatment. Acute kidney injury (AKI) was defined as an absolute increase in serum creatinine by 0.3 mg/dL or more within 48 hours, or an increase in serum creatinine to 1.5 times the baseline level or more during the first seven postoperative days. The stage of AKI was determined using the KDIGO classification: stage 1: increase in serum creatinine of ≥0.3 mg/dL or 1.5–1.9 times baseline; stage 2: increase in serum creatinine to 2.0–2.9 times baseline; stage 3: increase in serum creatinine to ≥3.0 times baseline, or an increase of ≥4.0 mg/dL, or the initiation of renal replacement therapy.

Statistical analysis

The children undergoing LTx were divided into two groups: the FO group and the non-FO group. We compared baseline characteristics, donor information, intraoperative factors, and outcomes between the two groups. QQ plots and the Shapiro-Wilk test were employed to assess the normality of quantitative data. For data that met normal distribution criteria, we used mean ± standard deviation, and between-group comparisons were made using two independent sample t-tests. For non-normally distributed data, we reported median [interquartile range (IQR)] and used the Wilcoxon-Mann-Whitney test for group comparisons. Enumeration data were expressed as percentages, with differences between groups analyzed using the Chi-squared test or Fisher’s exact test. P<0.05 was considered statistically significant.

The transplanted organs were obtained from voluntary donors, with written informed consent provided by the next of kin. No lungs were procured from executed prisoners. The Institutional Ethics Committees of the Organ Procurement Organization (OPO) approved the donation procedures. Donor lungs were allocated through the China Organ Transplant Response System (COTRS) (https://www.cot.org.cn/), which takes into account various factors in the allocation process.

Results

A total of 20 pediatric patients underwent LTx. Of these, 17 were classified as ASA IV, and 3 were classified as ASA V during preoperative evaluation. The mean age of the patients was approximately 10 years, with the youngest being 3 years old. Fifty percent of the patients were male. Based on clinical diagnoses, 10 patients had bronchiolitis obliterans, 3 had cystic fibrosis, 3 had pulmonary hypertension (PH) and interstitial lung disease, and 1 had a pulmonary arteriovenous fistula. The baseline characteristics are presented in Table 1.

Figure 1 shows the types of intraoperative blood products and crystalloid fluids administered during the procedures. The primary crystalloids used were Ringer’s acetate solutions and saline, with median infusion volumes of 8.975 mL/kg and 9.715 mL/kg, respectively. The mean total crystalloid infusion volume was 22.738 mL/kg. Albumin was the primary colloid for intraoperative volume expansion. A low concentration of albumin (5%) was administered to 16 patients, with a mean infusion volume of 21.45 mL/kg. In contrast, the median infusion volume for high-concentration albumin (20–25%) was 13.10 mL/kg. Approximately 90% of the children received intraoperative allogeneic RBC transfusions, and the median infusion volume was 20.43 mL/kg. Most children did not undergo autologous blood transfusions. The total fluid intake was 95.31 (IQR: 68.09, 120.12) mL/kg. Notably, only two children were transfused with platelets, and one received a cryoprecipitate transfusion. Two children, both diagnosed with PH, had cumulative hemorrhage exceeding 5 liters. The mean preoperative pulmonary artery pressure was 95.5 mmHg, reaching a maximum of 114 mmHg. Norepinephrine bitartrate dosage reached up to 56 mg, and both children had unfavorable prognoses.

Figure 1 Box plots of fluid infusion and output among children who underwent LTx. (A) Distribution of administered blood product volumes, showing the median and interquartile ranges for RBC, FFP, and albumin. (B) Distribution of different albumin concentrations, showing the median and interquartile ranges for 5% albumin and 20–25% albumin. (C) Distribution of administered crystalloid volumes, showing the median and interquartile ranges for normal saline and Plasma-Lyte 148. (D) Distribution of output volumes, showing the median and interquartile ranges for blood loss and urine. LTx, lung transplantation; FFP, fresh frozen plasma; RBC, red blood cell.

In terms of postoperative outcomes, 5 children developed grade 3 PGD, and 9 children developed AKI within 48 hours after surgery. The 30-day postoperative survival rate was 85%. The median postoperative lactate level was 2.65 mmol/L. The median durations of postoperative mechanical ventilation and ICU stay were 3.5 and 9.5 days, respectively.

Based on intraoperative fluid balance, the patients were categorized into the FO group (n=12) and the non-FO group (n=8). The percentage of fluid balance was 46.00% (IQR: 41.00%, 62.00%) and −16.00% (IQR: −23.00%, −2.00%) in the FO and non-FO groups, respectively. Exploratory analysis results showed that the FO and non-FO groups were well-balanced and comparable in terms of baseline, intraoperative information [except saline (P=0.04)], and donor information (only cold ischemia time was included). A total of 3 (37.5%) children in the non-FO group developed grade 3 PGD, and 3 (37.5%) children developed AKI within 48 hours after surgery. In the FO group, 2 (16.7%) children developed grade 3 PGD, and 6 (50.0%) children developed AKI within 48 hours after surgery. The median lactate levels were 2.80 (IQR: 1.68, 5.12) mmol/L in the non-FO group and 2.65 (IQR: 2.15, 6.60) mmol/L in the FO group. The median ICU stay was 20 (IQR: 6.25, 40.25) days in the non-FO group and 8.5 (IQR: 6.00, 25.75) days in the FO group. The median duration of mechanical ventilation was 15 (IQR: 3.50, 30.75) days in the non-FO group and 2 (IQR: 1.00, 9.00) days in the FO group. However, there were no statistically significant differences between the two groups regarding postoperative grade 3 PGD (P=0.35), AKI development within 48 hours after surgery (P=0.67), lactate levels (P=0.64), duration of postoperative mechanical ventilation (P=0.05), and duration of ICU stay (P=0.73). Detailed information is presented in Tables 2,3.

Regarding the use of blood products and fluids, there were increases in RBC (P=0.13), FFP (P=0.16), and crystalloid infusions (P=0.61), as well as total intake (P=0.23) in the group with grade 3 PGD compared to the group without grade 3 PGD (Figure 2), though the differences were not statistically significant. Similarly, Figure 3 demonstrates no significant differences in RBC (P=0.45), FFP (P=0.07), crystalloid (P=0.77), and total fluid infusions (P=0.20) between the AKI and non-AKI groups.

Figure 2 Box plots of blood product and fluid infusion in two groups (PGD 3 and non-PGD 3) among children who underwent LTx. (A) RBC transfusion volumes, showing higher median values in the PGD 3 group [40.00 (16.95, 70.00) mL/kg] compared to the non-PGD 3 group [19.23 (13.71, 28.02) mL/kg] but not statistically significant (P=0.13). (B) FFP administration was higher in the PGD 3 group [34.75 (0.00, 78.00) mL/kg] compared to the non-PGD 3 group [0.00 (0.00, 11.46) mL/kg] but not statistically significant (P=0.16). (C) Crystalloid fluid administration was higher in the PGD 3 group [19.50 (8.33, 30.00) mL/kg] than in the non-PGD 3 group [17.80 (11.95, 34.89) mL/kg] but not statistically significant (P=0.61). (D) Total fluid input was higher in the PGD 3 group [129.50 (94.07, 246.13) mL/kg] compared to the non-PGD 3 group [84.13 (67.62, 111.75) mL/kg] but not statistically significant (P=0.23). Data are presented as median (interquartile range). LTx, lung transplantation; FFP, fresh frozen plasma; RBC, red blood cells; PGD, primary graft dysfunction.

Figure 3 Box plots of blood product and fluid infusion in two groups (AKI and non-AKI) among children who underwent LTx. (A) RBC transfusion volumes, showing higher median values in the AKI group [21.62 (16.95, 40.00) mL/kg] compared to the non-AKI group [18.42 (14.10, 28.02) mL/kg] but not statistically significant (P=0.45). (B) FFP administration was higher in the AKI group [14.07 (0.00, 34.75) mL/kg] compared to the non-AKI group [0.00 (0.00, 6.79) mL/kg] but not statistically significant (P=0.07). (C) Crystalloid fluid administration was lower in the AKI group [17.80 (9.62, 30.00) mL/kg] than in the non-AKI group [21.27 (11.31, 34.89) mL/kg] but not statistically significant (P=0.77). (D) Total fluid input was higher in the AKI group [102.70 (84.13, 129.50) mL/kg] compared to the non-AKI group [80.91 (59.18, 113.77) mL/kg] but not statistically significant (P=0.20). Data are presented as median (interquartile range). AKI, acute kidney injury; LTx, lung transplantation; FFP, fresh frozen plasma; RBC, red blood cells.

Discussion

Current evidence highlights the importance of closely controlling fluid infusion during LTx, as increased fluid intake is associated with an elevated risk of grade 3 PGD (12). Excessive fluid administration can exacerbate lung injury, contributing to PGD by inducing FO and increasing microcirculatory hydrostatic pressure. While strict fluid management is essential, our study found no significant difference in adverse postoperative outcomes between the FO and non-FO groups. This suggests that maintaining a strictly restrictive fluid replacement strategy throughout the surgical procedure may present significant challenges.

Children undergoing LTx are required to follow strict preoperative fasting protocols and abstain from food and fluids. Additionally, preoperative fluid administration is tightly regulated to minimize circulatory load and reduce the risk of pulmonary edema. Consequently, nearly all children undergoing LTx experience decreased blood volume and increased blood viscosity. While continuous restriction of intraoperative fluid intake can lead to sustained hypoperfusion and hypoxia in vital organs, the use of high doses of vasoactive agents often becomes necessary. However, blood volume depletion can negatively affect microcirculatory perfusion, potentially causing severe lactic acid accumulation and acidosis. Although this approach may reduce the risk of pulmonary edema, it may lead to organ insufficiency in other areas. Turkish researchers (13) noted that restrictive rehydration, which leads to hypovolemia during LTx, could result in cardiac arrhythmias, creating an unstable hemodynamic state that necessitates the use of inotropic agents. Additionally, an international consensus recommendation (5) the need to maintain perfusion pressure in vital organs, particularly the kidneys, while restricting fluid and blood product infusions. Furthermore, considering the multifactorial origins of pulmonary edema and PGD (14,15), it would be overly simplistic to attribute these complications solely to volume overload. Casiraghi et al. (16) identified reversible cytoskeletal alterations and the activation of inflammatory pathways and cytokines as potential causes of pulmonary edema following ischemic reperfusion injury. Donor lung quality and cold ischemia time are also critical factors that influence postoperative outcomes.

Patients who undergo LTx are often hypovolaemic before surgery. This phenomenon poses an additional challenge to volume management if fluid intake is restricted throughout the procedure. In our study, children in the non-FO group were administered a more stringent fluid intake, possibly due to a reduced basal fluid requirement (BFR). While a precise definition of a restrictive fluid strategy is lacking, the intraoperative fluid volume should be determined by considering the BFR and fluid losses directly linked to the surgery (17). Failing to consider the BFR while excessively restricting fluid intake could result in a substantial hemodynamic disturbance, a finding also observed in our study. The non-FO group, for instance, required higher doses of norepinephrine (5.26 vs. 0.6 mg) and endured longer periods of mechanical ventilation (20 vs. 8.5 days) compared to the FO group. Based on these observations, we advocate for a “staged” fluid management strategy. In the first phase (pre-reperfusion), fluid infusion should not be excessively restricted; rather, it should account for the BFR and surgery-related fluid losses. Failure to address these factors could result in severe consequences, such as cardiac arrhythmias (10), hemodynamic collapse after positional changes, overuse of vasoactive and inotropic drugs, and organ dysfunction. In the second phase (post-reperfusion), fluid infusion must be tightly controlled, and diuretics should be used to manage fluid balance. However, maintaining electrolyte balance and homeostasis is equally important. In addition, maintaining intra-alveolar pressure above atmospheric pressure in the expiratory phase by adjusting the positive end-expiratory pressure can reduce pulmonary edema. Notably, 80% of the children in our center had LTx with VA-ECMO support, making it challenging to assess volume and cardiac function via CVP and TEE alone. Given that adequate blood volume is crucial for ECMO procedures, ECMO flow becomes an important reference for guiding intraoperative volume management. In cases without ECLS, the pulse index continuous cardiac output monitoring system offers valuable guidance for hemodynamic and volume management.

Crystalloids and albumin are highly recommended for volume expansion and resuscitation during LTx (18). The use of artificial colloids, however, is not recommended as they may exacerbate lung injury and increase the risk of PGD (5,19). Both low and high albumin concentrations have been used for intraoperative volume expansion, with low albumin concentrations recommended before reperfusion to optimize fluid balance. After reperfusion, higher albumin concentrations can be administered to maintain appropriate colloid osmotic pressure. In secondary analyses, we found no associations between blood products, crystalloids, or total fluid intake and adverse outcomes such as grade 3 PGD or AKI. However, the patient population undergoing LTx was heterogeneous, with varying underlying pathologies that could affect fluid tolerance. For example, children with right heart disease associated with pulmonary artery hypertension (PAH) and interstitial fibrosis might have a reduced tolerance to fluid administration compared to others. Unfortunately, due to the limited sample size, we were unable to perform further analysis to investigate these potential variations in fluid tolerance. Additionally, we did not have the resources to conduct subgroup analyses to explore the associations between different types of blood products, crystalloids, and postoperative outcomes.

Conclusions

This exploratory analysis is the first to explore the effect of fluid balance on the outcome of pediatric LTx. Our results showed a similar incidence of adverse postoperative outcomes between the FO and non-FO groups. However, this does not suggest that we advocate for excessive fluid infusion during LTx. Rather, it emphasizes that BFR should be incorporated into the framework of a restrictive fluid strategy.

The effectiveness of a “staged” volume management strategy in pediatric LTx remains unclear and warrants further investigation through high-quality prospective studies.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://tp.amegroups.com/article/view/10.21037/tp-2024-619/rc

Data Sharing Statement: Available at https://tp.amegroups.com/article/view/10.21037/tp-2024-619/dss

Peer Review File: Available at https://tp.amegroups.com/article/view/10.21037/tp-2024-619/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-2024-619/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Ethical approval for this study was obtained from the Human Body Research Ethics Committee of The Second Affiliated Hospital of Zhejiang University School of Medicine (No. 2022-0352). This study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. Due to the retrospective observational nature of the study, the requirement for written informed consent was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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