Journal of Clinical Monitoring and Computing https://doi.org/10.1007/s10877-023-01110-5 ORIGINAL RESEARCH Impact of graft reperfusion on cardiac function assessed by transesophageal echocardiography during liver transplantation: an observational retrospective study Susana González-Suárez1,2,3 · Matthew Corbett2 · Alberto Hernández-Martínez4 Received: 13 September 2023 / Accepted: 19 November 2023 © The Author(s) 2023 Abstract Cardiovascular instability is common during the reperfusion phase of orthotopic liver transplantation (OLT), and some patients experience a postreperfusion syndrome (PRS). However, there are no reports comparing the cardiac dysfunction between patients with PRS and those without. Thus, the aim of this study was to evaluate cardiac dysfunction in patients exhibiting PRS. This observational retrospective study included 34 patients who underwent OLT and were monitored with transesophageal echocardiography (TEE). The right ventricular/left ventricular (RV/LV) end diastolic area, tricuspid annular plane systolic excursion (TAPSE), left ventricular ejection fraction (LVEF) by Simpson method, pulsed Doppler of the mitral valve, and tissue Doppler motion of the mitral annulus were determined. Echocardiographic measurements were registered at the beginning of surgery and at 1 and 30 min after vascular unclamping. Patients with PRS (PRS group) were identified, and their echocardiographic parameters of ventricular function were compared with those in patients without PRS (non-PRS group). To check the evolution of diastolic-systolic dysfunction, general linear model-repeated measures were estimated. No patient presented systolic/diastolic dysfunction on the basal echocardiogram. One minute after vascular unclamping, the incidence of RV dilation was 4.5 times greater in patients with PRS (Cramer´s V > 0.6), and the incidence of RV systolic dysfunction was 62.5% in patients with PRS compared to 15.40% in patients without PRS (Cramer´s V = 0.45). The incidence of LV systolic dysfunction was 25% in patients with PRS compared to 0% in those without (Cramer´s V = 0.45), and left ventricular diastolic dysfunction was 4.8 times greater in patients with PRS (Cramer´s V = 0.45). No patient presented diastolic dysfunction type III. There were significant differences between groups in the evolutionary pattern at 1 and 30 min after unclamping for RV dilation (p = 0.008) and for TAPSE (p = 0.014). Liver graft reperfusion may alter cardiac function. Cardiac dysfunction was more frequent in patients with PRS. These patients exhibited temporary dysfunction of the RV associated with a varying degree of LV diastolic-systolic dysfunction. Trial registration: clinicaltrials.gov (NCT05175534). January 03, 2022; “retrospectively registered”. Keywords Transesophageal echocardiography · Liver transplantation · Hemodynamic instability · Ventricular dysfunction · Postreperfusion syndrome 3 Susana González-Suárez Vall d´Hebron Institut de Recerca (VHIR), Cardiovascular susana.gonzalez@uab.cat diseases Research Group, Passeig Vall d´Hebron 119-129, Barcelona 08035, Spain 1 Department of Surgery, Universitat Autònoma de Barcelona, 4 Department of Anesthesiology and Intensive Care, Grupo Unitat Docent Vall d´Hebron, Passeig Vall d´Hebron 119- Policlínica, Ibiza. Islas Baleares. Vía Romana s/n, 129, Barcelona 08035, Spain Ibiza, Baleares 07800, Spain 2 Department of Anesthesiology, Vall d´Hebron University Hospital, Passeig Vall d´Hebron 119-129, Barcelona 08035, Spain 13 Journal of Clinical Monitoring and Computing 1 Introduction the aim of this study was to describe the grade of right-left cardiac dysfunction in patients exhibiting PRS. During orthotopic liver transplantation (OLT), several surgi- cal stages can favor the appearance of hemodynamic insta- bility [1–3]. One of these episodes is observed during the 2 Methods reperfusion phase; the surgical clamp is removed, leading to the release of cold, hyperkalemic fluid and acidic contents 2.1 Ethics statement and registration of the liver allograft into the circulation, causing a reduc- tion in heart rate, an increase in pulmonary arterial pressure This retrospective observational single-center study was (PAP), a decrease in mean systemic blood pressure, and in approved by the Ethics Committee of Vall d’Hebron Uni- some cases, temporary myocardial dysfunction. In this con- versity Hospital, Barcelona, Spain (PR(AG)511/2019) and text, some patients may exhibit postreperfusion syndrome was registered at www.clinicaltrials.gov on January 03, (PRS), defined as a decrease in the mean arterial pressure 2022 (registration number: NCT05175534). All participants (MAP) ≥ 30% from baseline for more than 1 min and occur- signed written informed consent for anesthesia, as well as ring within 5 min of unclamping of the inferior portal vein. echocardiography monitoring and recording of data, which The visual assessment of the heart in this reperfusion was obtained for further analysis. All methods were carried stage is of extreme importance, and the characteristic echo- out in accordance with relevant guidelines and regulations. cardiographic features include acute ventricular systolic- diastolic dysfunction and new global or focal wall motion 2.2 Patient characteristics abnormalities [4–6]. There are no reports describing the use of transesopha- Inclusion criteria included consecutive adult patients who geal echocardiography (TEE) in association with PRS; thus, underwent OLT from May 17, 2016 to November 14, 2019 (34 patients, 24% of the total OLT cases for this period in our hospital), who were monitored with TEE (they had no Table 1 Demographic characteristics, comorbidities, and their associa- absolute contraindications such as the presence of esopha- tion with PRS geal stricture, cancer, diverticulum, recent esophageal sur- Total Non-PRS PRS p-value gery, or active upper gastrointestinal bleeding) and in whom patients n = 26 n=8 the examination was performed by a TEE board-certified n = 34 anesthesiologist. The exclusion criteria for the analysis were Sex Woman 8 (23.5) 7 (26.9) 1 (12.5) 0.400 age under 18 years, hepatopulmonary syndrome, portopul- Man 26 (76.5) 19 (73.1) 7 (87.5) monary hypertension, previous cardiac surgeries, or cardiac CHILD diseases (heart failure, arrhythmias, left ventricular hyper- A 4 (11.8) 1 (3.8) 3 (37.5) 0.011 trophy, diastolic-systolic ventricular dysfunction, moderate- B 20 (58.8) 15 (57.7) 5 (62.5) severe valvular disease). C 10 (29.4) 10 (38.5) 0 (0) Cirrhosis 2.3 Anesthesia Hepatitis B 3 (8.8) 3 (11.5) 0 (0) 0.717 Hepatitis C 10 (29.4) 6 (23.1) 4 (50) After establishing non-invasive monitoring, anesthesia Alcoholic 12 (35.3) 9 (34.6) 3 (37.5) induction was performed with the administration of 2 µg/ NASH 2 (5.9) 2 (7.7) 0 (0) kg of fentanyl, 2 mg/kg of propofol, and 0.5 mg/kg of atra- Autoimmune 2 (5.9) 1 (3.8) 1 (12.5) curium. After tracheal intubation, mechanical ventilation Tumor 1 (2.9) 1 (3.8) 0 (0) PBC 1 (2.9) 1 (3.8) 0 (0) was started (55–60% oxygen–air mixture) and adjusted to Cryptogenic 2 (5.9) 2 (7.7) 0 (0) maintain an end-tidal carbon dioxide concentration between Hyperoxaluria 1 (2.9) 1 (3.8) 0 (0) 33 and 38 mmHg. Anesthesia was maintained with a des- Renal disease 5 (14.7) 3 (11.5) 2 (25) 0.347 flurane (3-6%) and fentanyl (2 µg/kg/h) infusion and atra- Diabetes 12 (35.3) 10 (38.5) 2 (25) 0.486 curium infusion (0.4 mg/kg/h). Hemodynamic parameters Hypertension 15 (44.1) 11 (42.3) 4 (50) 0.702 were obtained by Swan Ganz catheter placement or by the COPD 3 (8.8) 1 (3.8) 2 (25) 0.065 FloTrac/Vigileo™ system (Edwards Lifesciences, Irvine, Cardiopathy 3 (8.8) 3 (11.5) 0 (0) 0.603 CA). A TEE probe was inserted from the beginning of sur- Hepatocarcinoma 16 (47.1) 10 (38.5) 6 (75) 0.070 gery until the first thirty minutes of the neohepatic phase Data are expressed as number (percentage) (in cases of hemodynamic instability, it was removed at the NASH: nonalcoholic steatohepatitis, PBC: primary biliary cirrhosis, end of surgery). Electrolytes and arterial blood gases were COPD: chronic obstructive pulmonary disease 13 Journal of Clinical Monitoring and Computing Table 2 Frequency of ventricular dysfunction measured at 1 and 30 min after graft reperfusion Total Non-PRS PRS P-value Chi2 V de Cramer n = 34 n = 26 n=8 RV/LV end diastolic area-1 min < 0.6 22 (64.7) 21 (80.8) 1 (12.5) 0.000 0.606 ≥ 0.6 12 (35.3) 5 (19.2) 7 (87.5) TAPSE-1 min < 17 mm 9 (26.5) 4 (15.4) 5 (62.5) 0.008 0.453 ≥ 17 mm 25 (73.5) 22 (84.6) 3 (37.5) LVEF-1 min < 53% 2 (5.9) 0 (0) 2 (25) 0.009 0.451 ≥ 53% 32 (94.1) 26 (100) 6 (75) LV diastolic dysfunction-1 min 5 (14.7) 2 (7.7) 3 (37.5) 0.029 0.457 RV/LV end diastolic area-30 min < 0.6 33 (97.1) 26 (100) 7 (87.5) 0.067 0.314 ≥ 0.6 1 (2.9) 0 (0) 1 (12.5) TAPSE-30 min < 17 mm 3 (8.8) 3 (11.5) 0 (0) 0.314 0.173 ≥ 17 mm 31 (91.2) 23 (88.5) 8 (100) LVEF-30 min < 53% 0 (0) 0 (0) 0 (0) ≥ 53% 34 (100) 26 (100) 8 (100) - . LV diastolic dysfunction-30 min 1 (2.9) 0 (0.0) 1 (12.5) 0.067 0.314 Data are expressed as number (percentage). The magnitude of the effect for Cramer’s V was: 0.00–0.09 as negligible, 0.10–0.29 as low, 0.30– 0.49 as medium and from 0.50 as high PRS: postreperfusion syndrome, RV: right ventricle, LV: left ventricle, TAPSE: tricuspid annular plane systolic excursion, LVEF: left ventricle ejection fraction Table 3 Hemodynamic param- Basal 1 min 30 min eters in patients with postreperfu- Mean (CI 95%) Mean (CI 95%) Mean (CI 95%) p-value sion syndrome (PRS) and without postreperfusion syndrome CVP Non-PRS 5,80 (4.09,7.51) 6,96 (5.31,8.61) 7,23 (5.56,8.89) 0.574 PRS 7,50 (4.41,10.58) 7,50 (4.41,10.58) 8,87 (5.87,11.87) PCP Non-PRS 11.74 (9.31,14.16) 13.47 (11.14,15.81) 14.65 (12.47,16.82) 0.635 PRS 14.33 (9.58,19.08) 15.50 (10.92,20.07) 14.00 (9.74,18.25) SVRI Non-PRS 1620.61 1474.92 1625.57 0.56 (1461.17,1780.05) (1324.40,1625.44) (1470.71,1780.43) PRS 1587.88 1297.37 1680.03 (1300.44,1875.31) (1026.01,1568.73) (1400.85,1959.21) MAP Non-PRS 76.54 (72.09,80.99) 63.08 (59.90,66.25) 81.46 (78.44,84.49) 0.000 CVP: central venous pressure, PRS 74.38 (66.35,82.40) 40.50 (34.77,46.23) 76.25 (70.80,81.70) PCP: pulmonary capillary pres- CI Non-PRS 3.72 (3.26,4.18) 3.24 (2.87,3.61) 3.84 (3.44,4.25) 0.021 sure, SVRI: systemic vascular PRS 3.51 (2.69,4.34) 2.10 (1.44,2.76) 3.42 (2.69,4.14) resistance index, MAP: mean HR Non-PRS 75.50 (69.36,81.64) 73.85 (68.08,79.61) 76.46 (71.83,81.09) 0.413 arterial pressure, CI: cardiac index, HR: heart rate PRS 82.25 (71.18,93.32) 76.50 (66.10,86.90) 82.25 (73.91,90.59) monitored and corrected throughout the surgery. Anesthetic 2.4 Surgical technique management during the anhepatic phase focused on the maintenance of cardiac preload and correction of arterial Liver allografts were preserved in a cold University of blood gas and electrolyte imbalances. A base deficit greater Wisconsin solution. Anastomosis of the liver graft was per- than 10 mmol/L was treated with sodium bicarbonate. An formed using the piggyback technique with or without tem- ionized calcium level of < 4 mg/dL was treated with calcium porary portocaval shunting. Before completing the hepatic chloride, and hyperkalemia (> 5 mmol/L) was treated with vein anastomosis, the liver graft was perfused with albu- insulin and glucose. Noradrenaline infusion was adminis- min through the portal vein. All patients were transported to tered when the systolic arterial blood pressure remained intensive care unit (ICU), postoperatively. below 90 mmHg. 13 Journal of Clinical Monitoring and Computing 2.5 Echocardiographic methods complications associated with TEE were collected from the patients’ medical records during hospital admission. A TEE scan was performed for intraoperative monitoring at the beginning of surgery, at 1 min and at 30 min, in all 2.8 Statistical analysis patients after vascular unclamping and in cases of hemody- namic instability (MAP minor than 60 mmHg). For categorical variables, frequencies and percentages are The systolic evaluation for the LV was performed by the shown for the total sample and the two groups (case/con- Simpson method using midesophageal 4-chamber (ME 4 C) trol). The differences between groups were evaluated with view; a value < 53% was considered pathological [7]. Pearson’s nonparametric Chi-squared test; Fisher’s exact The LV diastolic function was assessed in ME 4 C view test was applied only in the case of 2 × 2 tables. For con- by pulsed Doppler of the mitral valve at the level of the tinuous variables, descriptive values of mean and standard leaflet tips (E/A), and by tissue doppler of the mitral annu- deviation were displayed. The differences between groups lus at the septal (e´ septal) and lateral (e´ lateral) levels were evaluated using the Mann-Whitney test (nonparamet- [8]. Biplane left atrial (LA) volume was estimated using ric) or Student´s test for two independent samples (paramet- Simpson´s method [9]. RV systolic function was measured ric) based on the normality of the variables evaluated using with TAPSE; a value of less than 17 mm was considered the Shapiro-Wilks test. To check the evolution of diastolic/ pathological [7]. The presence of RV dilation was defined as systolic dysfunction, general linear model (GLM)-repeated an RV/LV end diastolic area ≥ 0.6 at ME 4 C [10–13]. measures were estimated with robust covariances. All con- ME 4 C was performed to detect possible venous air trasts were accompanied by the effect size estimator to embolism and thrombus and to evaluate the interaction of complete the interpretation of the results (Cramer’s V for the left and right ventricles [14]. categorical variables). The criteria for classifying the mag- The various complications of TEE were also registered nitude of the effect for Cramer’s V were as follows: negli- after orotracheal extubation, such as dental trauma, variceal gible, 0.00-0.09; low, 0.10–0.29; medium, 0.30–0.49; and bleeding, esophageal trauma, and recurrent laryngeal nerve high, 0.50. The significance level used in the analyzes was injury. set at 5% (α = 0.05). 2.6 Study outcome 3 Results Our study outcome was to describe the right and left cardiac dysfunction at the reperfusion phase between patients with Thirty-four patients were enrolled in the study, including 26 and without PRS. men and eight women. The mean age of patients with PRS (n = 8) was 58.42 ± 10.24 years, and that of patients without 2.7 Data collection PRS (n = 26) was 61 ± 8.32 years, p = 0.460. The baseline characteristics of the patients are shown Age, sex, Child-Pugh classification, cirrhosis etiology, pres- in Table 1. Differences between groups were observed for ence of hepatocarcinoma, hypertension, diabetes mellitus, Child-Pugh score. renal disease, chronic obstructive pulmonary disease, and No patient presented systolic/diastolic dysfunction on the cardiopathy were recorded at baseline. The following data preoperative echocardiogram. In six patients, cardiac moni- were analyzed at the beginning of surgery, one min after toring with TEE was not possible in the transgastric short reperfusion, and 30 min after reperfusion: MAP, heart rate axis view (TG mid SAX) due to retraction of the stomach (HR), cardiac index (CI), central venous pressure (CVP), by surgical separators. pulmonary capillary pressure (PCP), SVRI (systemic vas- After unclamping, the PRS group presented greater sys- cular resistance index), LA volume index, RV end diastolic tolic/diastolic dysfunction than the non-PRS group (RV area, LV end diastolic area, TAPSE, tricuspid regurgitation dilation ≥ 0.6, TAPSE < 17 mm, LVEF < 53%, and LV dia- (TR) velocity, LVEF, E/a (pulsed Doppler of the mitral stolic dysfunction (type II). No patient presented diastolic valve), and e´ (tissue Doppler of the mitral annulus). The dysfunction type III. Thirty minutes after vascular unclamp- data on need for vasoactive drugs during surgery, as well ing, only one patient in the PRS group presented RV dilation as postoperative data on graft rejection, the need for sec- and LV diastolic dysfunction. The main findings collected ond surgery after liver transplant (bleeding), the need for re- with TEE at 1 and 30 min after graft reperfusion are shown transplantation, renal dysfunction (glomerular filtration < 60 in Fig. 1; Table 2. mL/min/1.73 m2), days of hospitalization, mortality, and Twenty-nine patients were monitored with the Swan Ganz catheter (eight patients in the PRS group and 21 patients in 13 Journal of Clinical Monitoring and Computing Table 4 Evolution and comparation of systolic and diastolic function parameters between groups Basal 1 min 30 min 1 min-Basal Variation% 30 min-Basal Variation% P-Value Mean (CI95%) Mean (CI95%) Mean (CI95%) Mean Mean (CI95%) (CI95%) RV/LV Total 0.493 0.663 0.513 0.170 34.5%** 0.020 4.1% 0.000** (0.458,0.528) (0.616,0.710) (0.487,0.539) (0.112,0.227) (-0.023,0.063) Non- 0.524 0.602 0.500 0.078 14.9%** -0.024 -4.6% 0.008** PRS (0.490,0.558) (0.557,0.648) (0.475,0.526) (0.022,0.134) (-0.065,0.018) PRS 0.463 0.724 0.526 0.261 56.4%** 0.064 13.8%* (0.402,0.523) (0.641,0.806) (0.481,0.572) (0.161,0.362) (-0.011,0.139) TAPSE Total 19.120 16.764 18.731 -2.356 -12.3%** -0.389 -2.0% 0.000** (mm) (18.399,19.841) (16.161,17.368) (18.021,19.440) (-3.278, (-1.381,0.602) -1.433) Non- 18.615 17.654 18.962 -0.962 -5.2%* 0.346 1.9% 0.014* PRS (17.916,19.315) (17.068,18.239) (18.273,19.650) (-1.857, (-0.616,1.308) -0.067) PRS 19.625 15.875 18.500 -3.750 -19.1%** -1.125 -5.7% (18.365,20.885) (14.819,16.931) (17.259,19.741) (-5.363, (-2.860,0.610) -2.137) LVEF Total 64.053 60.111 61.620 -3.942 -6.2%* -2.433 -3.8% 0.045* (%) (61.785,66.321) (57.889,62.332) (59.662,63.578) (-7.056, (-5.373,0.507) -0.829) Non- 63.731 61.846 62.115 -1.885 -2.9% -1.615 -2.5% 0.416 PRS (61.530,65.931) (59.691,64.001) (60.216,64.015) (- (-4.468,1.237) 4.905,1.136) PRS 64.375 58.375 61.125 -6.000 -9.3%* -3.250 -5.0% (60.408,68.432) (54.490,62.260) (57.701,64.549) (-11.446, (-8.392,1.892) -0.554) E/A Total 1.252 1.475 1.305 0.223 17.8%** 0.053 4.2% 0.000** (1.201,1.303) (1.384,1.565) (1.238,1.372) (0.120,0.325) (-0.029,0.136) Non- 1.261 1.412 1.261 0.150 11.9%** 0.000 0.0% 0.281 PRS (1.212,1.310) (1.324,1.499) (1.196,1.326) (0.051,0.250) (-0.080,0.080) PRS 1.243 1.538 1.349 0.295 23.7%** 0.106 8.5% (1.154,1.331) (1.379,1.696) (1.232,1.466) (0.116,0.474) (-0.038,0.251) E/e´ Total 7.146 10.251 8.130 3.105 43.5%** 0.984 13.8%** 0.000** (6.911,7.382) (9.014,11.488) (7.451,8.810) (1.849, (0.270,1.698) 4.360) Non- 6.943 7.079 7.103 0.137 1.9% 0.161 2.3% 0.000** PRS (6.714,7.171) (5.879,8.279) (6.444,7.763) (-1.082,1355) (-0.532,0.853) PRS 7.350 13.423 9.157 6.072 82.6%** 1.807 24.6%** (6.939,7.761) (11.259,15.586) (7.969,10.346) (3876,8.269) (0.559,3.056) TR Total 0.224 1.160 0.333 0.936 417.9%** 0.109 48.7% 0.000** (m/s) (0.091,0.356) (0.821,1.498) (0.108,0.557) (0.576,1.296) (-0.148,0.366) Non- 0.135 0.719 0.115 0.585 433.3%** -0.019 -14.1% 0.009** PRS (0.006,0.263) (0.391,1.047) (-0.102,0.333) (0.235,0.934) (-0.268,0.230) PRS 0.313 1.600 0.550 1.288 411.5%** 0.238 76% (0.080,0.545) (1.009,2.191) (0.158,0.942) (0.658,1.917) (-0.212,0.687) LA vol. Total 25.558 27.058 26.053 1500 5.9% 0.495 1.9% 0.392 índex (24.246,26.898) (25.271,28.845) (24.631,27.475) (-0.678, (-1.402,2.393) (mL/m2) 3.678) Non- 25.115 26.115 25.231 1.000 3.9% 0.115 0.5% 0.398 PRS (23.843,26.388) (24.382,27.849) (23.851,26.610) (-1.113,3.113) (-1.725,1.956) PRS 26.000 28.000 26.875 2.000 7.7% 0.875 3.4% (23.706,28.294) (24.875,31.125) (24.388,29.362) (- (-2.443,4.193) 1.809,5.809) General linear models (GLM) repeated measures to determine significant variations in the parameters of ventricular dysfunction over time and the influence of PRS. On the left of the table (non-shaded table), data are shown as mean (estimated marginal according to GLM) and 95% confidence interval (CI) at basal, 1 min, and 30 min after graft reperfusion. On the right of the table (shaded table), data are expressed as means of units of variation (95% CI) and percentages of variation in relation to baseline values at 1 min and at 30 min after vascular unclamping RV: right ventricle, TAPSE: tricuspid annular plane systolic excursion, LVEF: left ventricular ejection fraction, TR: tricuspid regurgitation, LA: left atrial *P-value <0.05 (significant result at 5%), **p-value <0.01 (significant result at 1%) 13 Journal of Clinical Monitoring and Computing Fig. 1 Evaluation of left ventricular diastolic function the non-PRS group). MAP decreased significantly in both stage, which was attributed to hypovolemia (collapse of study groups one minute after vascular unclamping, with the ventricular chambers in systole in the TG mid SAX) a greater reduction in the PRS group. Cardiac output also with systemic vascular resistance between 1100 and 1230 decreases significantly in the PRS group one minute after dyn.s/cm5). Two patients presented mild right pleural effu- vascular unclamping. There were no significant differences sion observed by the TEE descending aorta short-axis view, between groups in the general evolution of filling pres- which did not affect the oxygenation of the patients. sures (PVC, PCP), HR, and in systemic vascular resistance; Microembolizations were observed in all patients after although filling pressures increased, and systemic vascular vascular unclamping in cardiac right cavities. resistance decreased one minute after graft reperfusion. Fig- There were no differences between the groups in the dos- ure 2; Table 3 show the results. age of vasoactive drugs administered during surgery and in The evolution of ventricular function over time for two postoperative complications (Table 5). global population showed that the RV was dilated at 1 min Sixteen patients had esophageal varices, but no complica- after reperfusion (significant increase of 0.170 units (34.5%)), tions were associated with the use of the echocardiography returning to almost baseline values at 30 min (increase with probe. No patient experienced (documented) variceal hem- respect to basal value of 0.020 units (4.1%), p = 0.000). orrhage, dental trauma, esophageal or gastric perforation, There were significant differences between groups in the oropharyngeal trauma, or recurrent laryngeal nerve injury. evolutionary pattern at 1 and 30 min after unclamping for RV dilation (p = 0.008); thus, the PRS group experienced a more pronounced first increase (56.4%) at 1 min and a 4 Discussion subsequent decrease at 30 min (13.8%), leading to a slight, significant increase in RV dilation values between the basal The main finding of this study is that cardiac dysfunction and post-30-min timepoints. The non-PRS group presented was greater in patients with PRS, and that this dysfunction an increase of 14.9% at 1 min and of -4.6% at 30 min with was transient in most patients. The incidence of RV dila- respect to basal levels. There were significant differences in tion, LV diastolic dysfunction, and biventricular systolic the evolutionary pattern over time for TAPSE, LVEF, E/A, dysfunction was higher in patients with PRS than in those E/e´and tricuspid regurgitation (TR) velocity. There were without at one minute of vascular unclamping. By 30 min, also significant differences between groups in the evolu- all patients had recovered normal LV systolic function, with tionary pattern at 1 and 30 min for TAPSE (p = 0.014), E/e´ persistent dilation of the RV and LV diastolic dysfunction in (p = 0.000) and TR (p = 0.009). The evolution of ventricular one patient with PRS. dysfunction is shown in Table 4; Fig. 3. RV dilation occurred in 87.5% of patients with PRS and Hemodynamic instability was observed in one patient in 19.2% of the patients without PRS. Some authors [15] after orotracheal intubation due to severe pulmonary hyper- have also described RV abnormalities, such as dilation and/ tension; moderate tricuspid regurgitation allowed to obtain or abnormal interventricular septal wall motion (IVSWM) a pulmonary arterial systolic pressure of 58 mmHg (not pre- [6], as causes of hypotension after graft reperfusion. During viously known), and dilation of the RV was observed (RV/ the liver reperfusion stage, many right-sided microemboli LV = 0.9). Given these findings, pulmonary pressure moni- and inflammatory mediators flood the systemic circula- toring with a Swan Ganz catheter was employed to confirm tion from the liver graft, producing a sudden load of cold the findings. Two patients presented hemodynamic instabil- and acidotic blood. This can lead to right ventricle over- ity in the dissection stage and six patients in the anhepatic load and increase pulmonary circulation (typically, filling 13 Journal of Clinical Monitoring and Computing Fig. 2 Graphical representation of the evolution of hemodynamic parameters over time and between groups. Marginal estimated means and the error bars that are the confidence intervals 95% (CI 95%) at basal, at 1 and 30 min after graft reperfusion. Statistical differences in the evolutionary pattern of the two groups are marked with an asterisk 13 Journal of Clinical Monitoring and Computing pressures increase in this phase). The dilation of the RV also find some differences in our population study. Prospective pushes the interventricular septum to the left, inducing tran- studies should be performed to confirm the cardiac dysfunc- sient diastolic dysfunction and decreased preload in the left tion after liver graft reperfusion, and its repercussion on heart. In fact, in our study, 75% (26.47% of the total) of postoperative complications. On the other hand, we could the patients who presented RV dilation also presented LV be underestimating the degree of the LV diastolic dysfunc- diastolic dysfunction one minute after vascular unclamping. tion because TEE underestimates both the diameter and vol- This diastolic dysfunction was also observed by Wolf et al. ume of the LA compared to TTE. In any case, we performed [16] and by Devauchelle et al. [17] when analyzing e’ wave a Simpson biplane estimation of the LA volume in TEE, velocity during liver graft reperfusion. which is the best measure to estimate the LA volume from We also observed biventricular systolic dysfunction. 25% TTE with a mean difference of -6 ml [9]. Finally, we did not of patients with PRS had LV dysfunction and 62.5% had determine the diastolic function of the RV in our patients right ventricular systolic dysfunction (TAPSE < 17 mm) and only measured the ratio RV/LV end diastolic area and one minute after vascular unclamping. We measured TAPSE. Given the anatomical disposition of RV, the align- TAPSE because it is a very specific parameter of RV sys- ment of the Doppler cursor with the RV free wall is usually tolic function and is less dependent on preload than other not permitted on ME views in TEE, as the cursor and tissue markers of ventricular function. However, there are some motion are in distinctly different orientations. Consequently, disadvantages; the measurement is angle dependent, and the RV diastolic dysfunction is less frequently documented. displacement in the ME 4 C view is representative of total We can affirm that TEE monitoring offers some advan- RV function only if there are no regional RV wall motion tages at the reperfusion stage as cardiac function can be abnormalities [18]. monitored in real time, allowing an optimal outcome after Decreased left heart preload can lead to a decrease in vascular unclamping. Although we did not observe com- systemic systolic blood pressure. This can have two com- plications associated with the TEE probe, it is necessary ponents: the first cardiac, as described above, and a second to consider that serious complications such as esophageal component due to the liberation of the solute from the liver perforation have been reported in liver transplant recipients into the systemic circulation, sustaining the hypotension. [24]. Therefore, careful insertion and mobilization of the To decrease the air embolism, hypothermia, and ischemic probe during exploration should be a priority. metabolites from the donor liver, an albumin hot solu- tion was injected into the donor liver by our surgery team, discarding the effluent immediately before graft reperfu- 5 Conclusion sion. Even so, we observed right sided microemboli in all patients, although we were unable to document the impact PRS in OLT is related to RV dysfunction with a certain of less or more air embolization on the degree of cardiac degree of LV dysfunction, although this cardiac dysfunction dysfunction. We also normalize calcium chloride, potas- recovers in most patients at 30 min post vascular unclamp- sium, bicarbonate, and glucose levels before reperfusion of ing, without postoperative clinical repercussions. the donated liver. There are no conclusive results on the prognostic impact of cardiac dysfunction. Many of our patients recovered nor- mal cardiac function by 30 min after unclamping, and we did not observe differences in postoperative complications between groups. Similarly, other authors did not obtain any prolonged cardiac dysfunction as a common problem during liver transplantation and concluded that an understanding of the physiological changes that occur during transplantation should allow the anesthesiologist to correct many factors that might cause hemodynamic instability [16]. Marella et al. obtained similar results and concluded that LV diastolic dysfunction did not affect post-transplant outcomes [19]. Nevertheless, other reports have shown that LV diastolic dysfunction is associated with an increased risk of graft rejection, graft failure, and mortality [20–23]. This present study has some limitations. The main limita- tion was the small sample size; nevertheless, we could still 13 Journal of Clinical Monitoring and Computing Fig. 3 Graphical representation of the evolution of ventricular function over time and between groups. Marginal estimated means and the error bars that are the confidence intervals 95% (CI 95%) at basal, at 1 and 30 min after graft reperfusion. Statistical differences in the evolutionary pattern of the two groups are marked with an asterisk 13 Journal of Clinical Monitoring and Computing Table 5 Dosage of intraoperative vasopressors and postoperative com- included in the article’s Creative Commons licence and your intended plications in the two groups use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright Mean ± SD p-value holder. To view a copy of this licence, visit http://creativecommons. Number org/licenses/by/4.0/. (percentage) Noradrenaline Non-PRS 9.56 ± 4.78 0.307 PRS 7.38 ± 6.38 Adrenaline Non-PRS 0.15 ± 0.25 0.39 References PRS 0.08 ± 0.2 1. Aggarwal S, Kang Y, Freeman JA, et al. Postreperfusion syn- Hospital stay (days) Non-PRS 15.12 ± 5.53 0.67 drome: cardiovascular collapse following hepatic reperfusion PRS 27 ± 34.18 during liver transplantation. Transpl Proc. 1987;19:54–5. Graft rejection Non-PRS 11.5% 0.94 2. Chung IS, Kim HY, Shin YH, et al. Incidence and predictors of PRS 12.5% post-reperfusion syndrome in living donor liver transplantation. Re-surgery Non-PRS 7.7% 0.67 Clin Transpl. 2012;26(4):539–43. 3. SiniscalchiA, Gamberini L, Laici C, et al. Post reperfusion syndrome PRS 12.5% during liver transplantation: from pathophysiology to therapy and Re-transplant Non-PRS 0% 0.06 preventive strategies. World J Gastroenterol. 2016;28(4):1551– PRS 12.5% 69. https://doi.org/10.1111/j.1399-0012.2011.01568.x. Renal disorder Non-PRS 26.9% 0.22 4. Burtenshaw AJ, Isaac JL. The role of trans-oesophageal echo- PRS 50% cardiography for perioperative cardiovascular monitoring during Mortality Non-PRS 3.8% 0.36 orthotopic liver transplantation. Liver Transpl. 2006;12(11):1577– PRS 12.5% 83. https://doi.org/10.1111/j.1399-0012.2011.01568.x. 5. Vetrugno L, Barbariol F, Baccarini U, et al. Transesophageal echocardiography in orthotopic liver transplantation: a com- Acknowledgements None. prehensive intraoperative monitoring tool. Crit Ultrasound J. 2017;9:15. https://doi.org/10.1186/s13089-017-0067-y. Author Contributions All authors have approved the final version of 6. Suriani RJ, Cutrone A, Feierman D, et al. Intraoperative trans- the manuscript and they take responsibility for the integrity of the data esophageal echocardiography during liver transplantation. J and the accuracy of the data analysis. The author contributions are as Cardiothorac Vasc Anesth. 1996;10(6):699–707. https://doi. follows: SGS: Study concept, design, acquisition, analysis, interpreta- org/10.1016/S1053-0770(96)80193-5. tion of study data, drafting of the manuscript. MC: Analysis, interpre- 7. Lang RM, Badano LP, Mor-Avi V, et al. Recommendations for tation of study data, drafting of the manuscript. AHM: Study concept. cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and Funding The authors declare that no funds, grants, or other support the European Association of Cardiovascular Imaging. Eur Heart were received during the preparation of this manuscript. J- Cardiovascular Imaging. 2015. https://doi.org/10.1093/ehjci/ Open Access Funding provided by Universitat Autonoma de Barce- jev014. 16,233 – 71. lona. 8. Nagueh SF, Smiseth OA, Appleton CP, et al. Recommendations for the evaluation of left ventricular diastolic function by echo- cardiography: an update from the American Society of Echo- Declarations cardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29(4):277–314. https:// Ethics approval This study was performed in line with the principles doi.org/10.1016/j.echo.2016.01.011. of the Declaration of Helsinki. Approval was granted by the Re- 9. Eshoo S, Ross DL. Evaluation of left atrial size on transoesopha- search Ethics Committee of the Vall d’Hebron University Hospital geal echocardiography: what is the best measure? Heart Lung and (PR(AG)511/2019, May 29, 2020), and was retrospectively registered Circulation. 2008;17(2):100–6. at clinicaltrials.gov (NCT05175534). 10. Vieillard-Baron A, Prigent A, Repessé X, et al. Right ventricular failure in septic shock: characterization, incidence and impact on Consent to participate Informed consent was obtained from all indi- fluid responsiveness. BMC Crit Care. 2020;24:360. https://doi. vidual participants included in the study. org/10.1186/s13054-020-03345-z. 11. Vieillard-Baron A, Prin S, Chergui K, et al. Echo-Doppler dem- Consent to publish The authors affirm that human research partici- onstration of acute Cor Pulmonale at the bedside in the Medical/ pants provided informed consent for publication of their clinical data. Intensive Care Unit. Am J Respir Crit Care Med. 2002;166:1310– 9. https://doi.org/10.1164/rccm.200202-146CC. Competing interests The authors declare no competing interests. 12. Horton KD, Meece RW, Hill JC. Assessment of the right ventricle by echocardiography: a primer for cardiac sonographers. J Am Soc Echocardiogr. 2009;22(7):776–92. https://doi.org/10.1016/j. Open Access This article is licensed under a Creative Commons echo.2009.04.027. Attribution 4.0 International License, which permits use, sharing, 13. Ayuela Azcarate JM, Clau Terre F, Ochagavia A, et al. Role of adaptation, distribution and reproduction in any medium or format, echocardiography in the hemodynamic monitorization of criti- as long as you give appropriate credit to the original author(s) and the cal patients. Med Intensiva. 2012;36(3):220–32. https://doi. source, provide a link to the Creative Commons licence, and indicate org/10.1016/j.medin.2011.11.025. if changes were made. The images or other third party material in this 14. Vetrugno L, Cherchi V, Lorenzin D, et al. The Challenging article are included in the article’s Creative Commons licence, unless Management of an intracardiac Thrombus in a liver transplant indicated otherwise in a credit line to the material. If material is not patient at the reperfusion phase: a case report and brief literature 13 Journal of Clinical Monitoring and Computing review. Transpl Direct. 2021;7(10):e746. https://doi.org/10.1097/ 20. Mittal C, Qureshi W, Singla S, et al. Pre-transplant left ventricu- TXD.0000000000001200. lar diastolic dysfunction is associated with post-transplant acute 15. Krenn CG, De Wolf AM. Current approach to intraoperative graft rejection and graft failure. Dig Dis Sci. 2014;59(3):674–80. monitoring in liver transplantation. Curr Opin Organ Transplant. https://doi.org/10.1007/s10620-013.2955-8. 2008;13:285–90. https://doi.org/10.1097/MOT.0b013e3. 21. Shilcutt SK, Ringenberg KJ, Chacon MM, et al. Liver transplan- 16. Wolf AMD. Does ventricular dysfunction occur during liver tation: intraoperative transesophageal echocardiography findings transplantation? Transpl Proc. 1991;23(3):1922–3. and relationship to major postoperative adverse cardiac events. J 17. Devauchelle P, Schmitt Z, Bonnet A, et al. The evolution of Cardiothorac Vasc Anesth. 2016;30:107–14. diastolic function during liver transplantation. Anesth Crit 22. Vetrugno L, Cherchi V, Zanini V, et al. Association between pre- Care Pain Med. 2018;37(2):155–60. https://doi.org/10.1016/j. operative diastolic dysfunction and early allograft dysfunction accpm.2016.09.009. after orthotopic liver transplantation: an observational study. 18. Rudski LG, Lai WW, Afidalo J, et al. Guidelines for the echo- Echocardiography. 2022;39(4):561–7. https://doi.org/10.1111/ cardiographic assessment of the right heart in adults: a report echo.15328. from the American Society of Echocardiography endorsed by the 23. Vetrugno L, Barnariol F, Bignami E, et al. Transesophageal European Association of Echocardiography, a registered branch ultrasonography during orthotopic liver transplantation: show of the European Society of Cardiology, and the Canadian Society me more. Echocardiography. 2018;35(8):1204–15. https://doi. of Echocardiography. J Am Soc Echocardiogr. 2010;23:685–713. org/10.1111/echo.14037. https://doi.org/10.1016/j.echo.2010.05.010. 24. Mazilescu LI, Bezinover D, Paul A, et al. Unrecognized esopha- 19. Marella HK, Yedlapati N, Kothadia JP, et al. Impact of left ven- geal perforation after liver transplantation. J Cardiothorac Vasc tricular diastolic dysfunction on liver transplantation outcomes Anesth. 2018;32(3):1407–10. based on the latest American Society of echocardiography/Euro- pean Association of cardiovascular imaging recommendations. Publisher’s Note Springer Nature remains neutral with regard to juris- Clin Exp Hepatol. 2021;7(4):390–5. https://doi.org/10.5114/ dictional claims in published maps and institutional affiliations. ceh.2021.111001. 13