Int. J. Med. Sci. 2017, Vol.

14 173

Ivyspring
International Publisher International Journal of Medical Sciences
2017; 14(2): 173-180. doi: 10.7150/ijms.17502
Research Paper

Risk factors for intraoperative massive transfusion in

pediatric liver transplantation: a multivariate analysis
Seok-Joon Jin1, Sun-Key Kim1, Seong-Soo Choi1, Keum Nae Kang2, Chang Joon Rhyu2, Shin Hwang3,
Sung-Gyu Lee3, Jung-Man Namgoong3, Young-Kug Kim1
1. Department of Anesthesiology and Pain Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea;
2. Department of Anesthesiology and Pain Medicine, National Police Hospital, Seoul, Republic of Korea;
3. Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea.

Corresponding authors: Young-Kug Kim, MD, PhD, Professor, Department of Anesthesiology and Pain Medicine, Asan Medical Center, University of Ulsan
College of Medicine, 88 Olympic-ro 43-gil, Songpa-gu, Seoul 05505, Republic of Korea. Tel: +82-2-3010-5976; Fax: +82-2-3010-6790; Email: kyk@amc.seoul.kr;
Jung-Man Namgoong, MD, PhD, Assistant Professor, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, 88 Olympic-ro
43-gil, Songpa-gu, Seoul, 05505, Republic of Korea. Tel: +82-2-3010-1512; Fax: +82-2-3010-6701; Email: namgoong2940@gmail.com.

Ivyspring International Publisher. This is an open access article distributed under the terms of the Creative Commons Attribution (CC BY-NC) license
(https://creativecommons.org/licenses/by-nc/4.0/). See http://ivyspring.com/terms for full terms and conditions.

Received: 2016.09.07; Accepted: 2016.12.21; Published: 2017.02.08

Abstract
Background: Pediatric liver transplantation (LT) is strongly associated with increased
intraoperative blood transfusion requirement and postoperative morbidity and mortality. In the
present study, we aimed to assess the risk factors associated with massive transfusion in pediatric
LT, and examined the effect of massive transfusion on the postoperative outcomes.
Methods: We enrolled pediatric patients who underwent LT between December 1994 and June
2015. Massive transfusion was defined as the administration of red blood cells 100% of the total
blood volume during LT. The cases of pediatric LT were assigned to the massive transfusion or
no-massive transfusion (administration of red blood cells <100% of the total blood volume during
LT) group. Univariate and multivariate logistic regression analyses were performed to evaluate the
risk factors associated with massive transfusion in pediatric LT. Kaplan-Meier survival analysis, with
the log rank test, was used to compare graft and patient survival within 6 months after pediatric LT
between the 2 groups.
Results: The total number of LT was 112 (45.0%) and 137 (55.0%) in the no-massive transfusion
and massive transfusion groups, respectively. Multivariate logistic regression analysis indicated that
high white blood cell (WBC) count, low platelet count, and cadaveric donors were significant
predictive factors of massive transfusion during pediatric LT. The graft failure rate within 6 months
in the massive transfusion group tended to be higher than that in the no-massive transfusion group
(6.6% vs. 1.8%, P = 0.068). However, the patient mortality rate within 6 months did not differ
significantly between the massive transfusion and no-massive transfusion groups (7.3% vs. 7.1%, P =
0.964).
Conclusion: Massive transfusion during pediatric LT is significantly associated with a high WBC
count, low platelet count, and cadaveric donor. This finding can provide a better understanding of
perioperative blood transfusion management in pediatric LT recipients.
Key words: pediatric liver transplantation, massive transfusion, risk factors.

Introduction
Liver transplantation (LT) has been introduced immunosuppressant therapy have led to
as a curative treatment for children with end stage improvements in the long-term survival rate to >80%
liver disease. Since Starzl performed the first [2]. Nevertheless, hepatic graft failure may still
successful pediatric LT in 1967 [1], the advances in the develop, and often affects patient survival after LT.
surgical techniques, anesthetic management, and Death in most cases of pediatric LT occurs within 6

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months of the LT [3]. In addition, massive blood loss encephalopathy, peritonitis, previous abdominal
and subsequent blood transfusion, which are surgery, and portal vein thrombosis were recorded to
associated with higher morbidity and mortality, are evaluate the risk factors for intraoperative massive
frequently noted during pediatric LT [4-8]. Liver transfusion.
cirrhosis, associated with a bleeding tendency during
LT as a result of a complex hemostatic disorder, is not General anesthesia
commonly observed in children. In contrast, biliary After routine monitoring (pulse oximetry,
atresia, a very common disease requiring pediatric LT, electrocardiography, and non-invasive blood pressure
is associated with peritoneal adhesion and recurrent recording), general anesthesia was induced by using
inflammation of the bile tree, as most of these patients an intravenous bolus injection of thiopental sodium (5
have previously undergone hepatoportoenterostomy mg/kg), fentanyl (0.51 g/kg), and rocuronium (0.6
and experience recurrent cholangitis [9]. Thus, mg/kg) or vecuronium (0.15 mg/kg). After tracheal
peritoneal adhesion in these patients requires a intubation, anesthesia was maintained using 12 vol%
greater amount of blood products and a longer sevoflurane, 50% oxygen in medical air, a continuous
operation time during intraabdominal surgery [10]. infusion of fentanyl (35 g/kg/h), and rocuronium
The total blood volume of neonates and children (0.2 mg/kg/h) or vecuronium (0.05 mg/kg/h).
is usually small, and hence, there is a greater Patients were mechanically ventilated at a constant
possibility of massive transfusion during major tidal volume of 810 ml/kg, and the respiratory rate
operations in pediatric patients. Although major was adjusted to maintain the end-tidal carbon dioxide
advances have been made in surgical and anesthetic partial pressure between 35 and 40 mmHg during the
management to reduce the use of blood products operation. Arterial and central venous catheters were
during LT, the incidence of large blood loss during LT placed for hemodynamic monitoring and blood
remains high. As the intraoperative blood transfusion sampling. Crystalloid (plasma solution A, CJ
requirement is directly related to poor outcomes Pharmaceutical, Seoul, Korea) and colloid (albumin)
[11-13], minimizing and predicting the need for were administered during LT.
massive transfusion during pediatric LT are
Surgical procedure
important. However, only limited information is
available regarding the risk factors for intraoperative The surgical technique comprised a bilateral
massive transfusion in pediatric LT recipients. subcostal incision, with extension to the xiphoid, or an
In the present study, we aimed to evaluate the inverted T-shaped incision. Total hepatectomy was
risk factors associated with massive transfusion performed in the recipients after clamping the inferior
during pediatric LT. Moreover, we examined the vena cava, portal vein, and hepatic artery; a
effect of massive transfusion on postoperative venous-venous bypass was not adopted. Prior to
outcomes, such as graft failure and patient mortality, engraftment, the donor liver was flushed with 1000 ml
after pediatric LT. of Histidine-Tryptophan-Ketoglutarate solution via
the portal vein. Venoplasty of the hepatic vein and/or
Materials and Methods portal vein in the recipient was preceded by the
an-hepatic phase, and engraftment was performed
Patient characteristics with the anastomosis of the hepatic vein, portal vein,
The institutional review board of Asan Medical and hepatic artery. We routinely checked the vascular
Center, Seoul, Republic of Korea approved this study. perfusion of the liver graft using Doppler sonography
The medical records from the general ward and after engraftment. Hemostasis was achieved by direct
intensive care units, as well as data on the operation suture ligation or electrocoagulation. A Roux-en-Y
and anesthesia used, were retrospectively reviewed. hepaticojejunostomy was performed using
We enrolled pediatric patients who underwent LT interrupted sutures.
between December 1994 and June 2015. The exclusion
criteria were as follows: incomplete data from medical Definition of massive transfusion
records, preoperative anticoagulant use, and Since the total blood volume in children varies
simultaneous transplantation of another organ. The according to age, the definition of massive transfusion
demographic data, primary diagnosis, donor type, in children should be relative to the total body volume
surgical technique for the donor, preoperative of specific age groups [8]. The total blood volume in
laboratory values, and intraoperative variables, as children aged >3 months was considered to be 70
well as the presence of elective/emergent surgery, ml/kg [14]. Massive transfusion was defined as the
re-LT, ascites, chronic kidney disease, esophageal administration of red blood cells 100% of the total
varix, fulminant hepatic failure, hepatic blood volume. The cases of pediatric LT were

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assigned to the massive transfusion group analysis. Variables with a P value <0.2 in the
(administration of red blood cells 100% of the total univariate logistic regression analysis were included
blood volume during LT) or no-massive transfusion in the final multivariate logistic regression analysis. In
group (administration of red blood cells <100% of the all other analyses, except for univariate logistic
total blood volume during LT). Intraoperative red regression analysis, a P value <0.05 was considered
blood cell transfusion was performed in cases where statistically signicant. Kaplan-Meier survival
the hemoglobin level was <8.0 mg/dl. analysis, with a log rank test, was used to compare
graft and patient survival within 6 months of
Postoperative outcomes pediatric LT, between the massive transfusion and
The postoperative outcome measures included no-massive transfusion groups. Statistical analyses
graft failure and patient mortality. We used the were conducted using R (version 3.1.2; R Foundation
definition of early graft failure reported in previous for Statistical Computing, Vienna, Austria), SigmaStat
studies [15-17]. We limited the survival analysis of for Windows (version 3.5; Systat Software, Inc.,
grafts to 6 months in order to evaluate the influence of Chicago, IL), and SPSS for Windows (version 23.0.0;
massive transfusion on early graft dysfunction and to IBM Corporation, Chicago, IL).
minimize other factors that may contribute to late
graft dysfunction, such as newly developed liver Results
disease. We also defined early patient mortality as Of the 257 pediatric LT procedures conducted
death that occurred within 6 months of the surgery. during the study period, 249 were included in the
Statistical analysis analysis (Figure 1). The recipient age ranged from 3
months to 17 years. The total volume of red blood cell
Data were expressed as means standard transfusion for all patients was 126.7 175.4 ml/kg.
deviation or number (%), as appropriate. Continuous The distribution of the red blood cell transfusion
variables were compared using Students t-test or amount is illustrated in Figure 2. Intraoperative
Mann-Whitney U test, whereas categorical variables massive transfusion was observed in 137 (55.0%) of
were compared using the 2 test or Fishers exact test,
249 LT procedures, whereas 14 (5.6%) LT procedures
as appropriate. The most relevant risk factors did not require blood transfusion (Figure 2).
associated with intraoperative massive transfusion
were selected in the univariate logistic regression

Figure 1. Study flow chart.

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Figure 2. Histogram representing the distribution of the ratio of transfused red blood cell volume to total blood volume. No-massive transfusion (blue bars) indicates the
administration of red blood cell <100% of the total blood volume during liver transplantation. Massive transfusion (red bars) indicates the administration of red blood cell 100%
of the total blood volume during liver transplantation. LT, liver transplantation.

Preoperative characteristics were compared transfusion groups (7.3% vs. 7.1%, P = 0.964) (Figure
between the massive transfusion group and 3).
no-massive transfusion group (Table 1). The sex,
Table 1. Preoperative characteristics.
donor type, and surgical technique for the donor
excluding the left lateral segment, as well as the No-massive Massive transfusion P value
transfusion (n = 112) (n = 137)
presence of ascites and chronic kidney disease Sex
significantly differed between the massive transfusion Female/Male 51 (45.5%)/61 (54.5%) 80 (58.4%)/57 (41.6%) 0.043
and no-massive transfusion groups (Table 1). The Age (years) 4.7 4.7 4.1 5.0 0.337
Weight (kg) 19.8 15.5 18.7 18.3 0.593
WBC, hemoglobin, platelet, protein, and C-reactive
Height (cm) 99.4 32.0 94.1 35.1 0.221
protein values were also significantly different Body mass index (kg/m2) 18.1 5.6 17.3 3.0 0.135
between the 2 groups (Table 2). A greater amount of Primary diagnosis

cryoprecipitate, fresh frozen plasma, platelet Biliary atresia 53 (47.3%) 69 (50.4%) 0.633
Wilsons disease 5 (4.5%) 12 (8.8%) 0.181
concentrate, crystalloid, and colloid was administered Other diseasesa 54 (48.2%) 56 (40.9%) 0.246
in the massive transfusion group than in the Donor type
no-massive transfusion group (Table 2). Living/Cadaveric donor 105 (93.8%)/7 (6.3%) 111 (81.0%)/26 0.003
(19.0%)
The results of univariate analysis are Surgical technique for
summarized in Table 3. Sex, cadaveric donor, and the donor
Left lateral segment 37 (33.0%) 55 (40.1%) 0.248
surgical technique for the donor; WBC, hemoglobin, Left lobe 61 (54.5%) 48 (35.0%) 0.002
platelet, albumin, and creatinine values; presence of Other techniquesb 14 (12.5%) 34 (24.8%) 0.014
emergent LT, re-LT, ascites, and chronic kidney Elective/Emergent LT
Elective/Emergent 89 (79.5%)/23 (20.5%) 97 (70.8%)/40 (29.2%) 0.118
disease; and operation time were selected for
Re-LTc 4 (3.6%) 13 (9.5%) 0.066
inclusion in the multivariate logistic regression Ascites 49 (43.8%) 78 (56.9%) 0.038
analysis (P <0.2). Multivariate logistic regression Chronic kidney disease 2 (1.8%) 11 (8.0%) 0.028
analysis indicated that high WBC count, low platelet Esophageal varix 29 (25.9%) 30 (21.9%) 0.461
Fulminant hepatic failure 31 (27.7%) 29 (21.2%) 0.232
count, and cadaveric donor were significant Hepatic encephalopathy 23 (20.5%) 30 (21.9%) 0.794
predictive risk factors of massive transfusion during Peritonitis 24 (21.4%) 34 (24.8%) 0.529
pediatric LT (Table 4). Previous abdominal 52 (46.4%) 70 (51.1%) 0.464
surgery
The graft failure rate within 6 months of LT in Portal vein thrombosis 8 (7.1%) 6 (4.4%) 0.346
the massive transfusion group tended to be higher Data are the mean standard deviation or number (%), as appropriate. LT, liver
than that in the no-massive transfusion group, transplantation. aOther diseases included hepatoblastoma, viral hepatitis, toxic hepatitis,
liver cirrhosis, acute liver failure, glycogen storage disease, and metabolic disease. bOther
although the values did not significantly differ (6.6% techniques included right lobe, dual left lobe, and whole liver. cNumber of re-LT included
14 re-LT, of which the first and second LTs were conducted during study period, as well as
vs. 1.8%, P = 0.068) (Figure 3). However, the mortality 3 re-LT, of which the first LT was not conducted during study period.
rate within 6 months of LT did not differ significantly
between the massive transfusion and no-massive

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Table 2. Preoperative laboratory values and intraoperative from a single institution that had highly experienced
variables. surgical and anesthetic teams [25-27].
No-massive Massive P value
transfusion transfusion
(n = 112) (n = 137)
Preoperative laboratory values
WBC (103/l) 7.1 3.8 8.8 5.4 0.005
Hemoglobin (g/dl) 10.0 1.9 9.3 1.9 0.009
Platelet (103/l) 167.5 103.6 133.9 86.9 0.006
Aspartate transaminase (U/l) 406.3 633.6 590.7 1610.5 0.255
Alanine transaminase (U/l) 382.5 891.2 410.2 1044.3 0.824
Total bilirubin (mg/dl) 16.2 11.4 17.1 12.0 0.536
Protein (g/dl) 6.3 0.9 6.0 1.0 0.005
Albumin (g/dl) 3.2 0.7 3.0 0.6 0.107
Creatinine (mg/dl) 0.4 0.3 0.6 1.0 0.146
Prothrombin time (INR) 1.9 1.2 2.0 1.1 0.547
aPTT (sec) 47.9 27.7 49.9 28.4 0.655
C-reactive protein (mg/l) 1.0 1.4 1.5 1.8 0.025
Intraoperative variables
Packed red blood cell use 0.1 0.1 0.7 0.7 <0.001
(U/kg)
Cryoprecipitate use (U/kg) 0.02 0.1 0.10 0.1 <0.001
Fresh frozen plasma use 0.1 0.2 0.3 0.4 <0.001
(U/kg)
Platelet concentrate use 0.02 0.1 0.10 0.1 <0.001
(U/kg)
Crystalloid use (ml/kg) 150.0 151.6 183.2 110.1 0.047
Colloid use (ml/kg) 47.4 45.4 83.4 65.9 <0.001
Operation time (min) 664.8 174.5 700.7 164.8 0.097
Data are the mean standard deviation. WBC, white blood cell; INR, international
normalized ratio; aPTT, activated partial thromboplastin time.

Discussion
In the present study, we found that the risk
factors for intraoperative massive transfusion in
pediatric LT were high WBC count, low platelet
count, and cadaveric donor. We also found that early
graft failure tended to be higher in the massive
transfusion group than in the no-massive transfusion
group.
Massive transfusion may be associated with
serious complications such as hypothermia, electro-
lyte abnormalities, immunologic complications,
coagulopathy, transfusion reactions, and
Figure 3. Kaplan-Meier curves of graft survival (A) and patient survival (B) within 6
postoperative mortality [14, 18, 19]. Although the months of the pediatric liver transplantation. The blue solid line indicates patient or
factors predicting blood loss and transfusion during graft survival in the no-massive transfusion group. The red solid line indicates patient
or graft survival in the massive transfusion group.
LT have been previously evaluated, those studies
primarily included adult patients [13, 20-24].
Moreover, the factors influencing blood transfusion in In our present series, a high WBC count was a
pediatric LT were evaluated under preoperative unique factor that predicted intraoperative massive
conditions, with varying anatomical and surgical transfusion during pediatric LT. Previous studies
factors [4, 5]. However, the results have not been have indicated that bacterial infections are common in
consistent, due to the differences in the preoperative patients with upper gastrointestinal hemorrhage
status, surgical techniques [22], massive transfusion [28-30], possibly because of preoperative invasive
definitions [5], and transfusion triggers between procedures, bacterial translocation in the intestine,
studies. In our present study, we followed a and defects in the scavenging system [29, 31]. Bernard
commonly used definition of massive transfusion in et al. showed that bacterial infection is not only an
children [14] and divided the cases into the massive independent factor of bleeding in liver dysfunction
blood transfusion and no-massive blood transfusion patients, but is also an important prognostic factor for
groups. Furthermore, we believe that our current mortality [30]. The relationship between bleeding and
results are reliable because the data were collected bacterial infection in these studies supports our

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Int. J. Med. Sci. 2017, Vol. 14 178

finding that leukocytosis can produce massive Table 4. Multivariate analysis of the risk factors for a massive
bleeding in patients with liver dysfunction. Moreover, transfusion during pediatric liver transplantation.
peritoneal adhesion is inevitable after trans-peritoneal Variables Regression Wald Odds 95% confidence P
value
surgery. Children with biliary atresia, recurrent coefficient ratio interval
WBC 0.159 17.1 1.172 1.0871.264 <0.001
peritonitis, or cholangitis, which cause inevitable Platelet -0.007 15.7 0.993 0.9890.996 <0.001
peritoneal adhesion, are commonly encountered, Donor type
particularly among those with hepatoportoen- Living donor 1.000
Cadaveric donor 1.503 10.5 4.496 1.80911.173 0.001
terostomy. Adhesiolysis during LT can lead to
WBC, white blood cell.
increased blood loss [10], which may then contribute
to massive transfusion in patients with coagulopathy
or hemodynamic instability. Moreover, bacterial
infection can lead to failure of bleeding control in the Our finding of the association between low
esophageal varix [32]. Our study suggests that platelet count and massive transfusion is consistent
massive transfusion during LT occurs more easily in with that observed in previous studies [22, 33]. Deakin
children who are susceptible to bacterial infection and et al. demonstrated that low platelet count was the
recurrent inflammation of the abdominal cavity. best predictor of massive transfusion. Similarly, the
intraoperative transfusion requirement during LT
was strongly associated with lower platelet count [33].
Marino et al. showed that patients who could not
Table 3. Univariate analysis of the risk factors for a massive
transfusion during pediatric liver transplantation. maintain normal platelet levels, despite the
preoperative correction of platelet counts, were likely
Variables Odds ratio 95% confidence P value
interval
to have a high level of blood usage [34]. Importantly, a
Sex lower platelet count is associated with impaired
Female 1.000 coagulation function, which can lead to bleeding and
Male 0.596 0.3600.986 0.044
Age 0.975 0.9271.026 0.336
blood transfusion during pediatric LT.
Weight 0.996 0.9821.011 0.592 We found that the incidence of massive
Height 0.995 0.9881.003 0.220 transfusion was higher in patients who underwent
Primary diagnosis
cadaveric donor LT than in those who underwent
Biliary atresia 1.000
Wilsons disease 1.843 0.6125.555 0.277 living-donor LT [35]. Fasco et al. reported that
Other diseasesa 0.797 0.4751.337 0.389 patients who underwent living-donor LT required
Donor type 66% fewer total blood products, as compared to those
Living donor 1.000
Cadaveric donor 3.514 1.4638.439 0.005
who underwent cadaveric donor LT, and that patients
Surgical technique for the donor in the living-donor LT group had milder disease and
Left lateral segment 1.000 more preserved coagulation function than those in the
Left lobe 0.529 0.3020.929 0.027
cadaveric donor LT group. In our present study,
Other techniquesb 1.634 0.7723.455 0.199
Elective/Emergent LT cadaveric donor LT was selected if the patient was
Elective 1.000 undergoing an emergent operation or had fulminant
Emergent 1.596 0.8862.873 0.119
hepatic failure, and if the patient did not have a living
Re-LT 2.831 0.8968.939 0.076
Ascites 1.700 1.0272.813 0.039
donor. However, some other studies have indicated
Chronic kidney disease 4.802 1.04222.134 0.044 conflicting results [7, 36, 37]. Pirate et al. did not
Esophageal varix 0.802 0.4471.441 0.461 observe a significant difference in blood transfusion
Peritonitis 1.210 0.6682.194 0.529
Previous abdominal surgery 1.206 0.7311.988 0.464
between cadaveric donor LT and living-donor LT. The
Portal vein thrombosis 0.595 0.2001.770 0.351 reasons for such discrepancies may be due to the
WBC 1.082 1.0221.145 0.006 differences in the preoperative conditions of patients,
Hemoglobin 0.833 0.7220.960 0.012
blood transfusion triggers, and inclusion criteria for
Platelet 0.996 0.9930.999 0.007
Total bilirubin 1.007 0.9851.029 0.534 LT recipients.
Albumin 0.718 0.4791.076 0.108 In our present analysis, the incidence of early
Creatinine 1.358 0.8742.110 0.173 graft failure tended to be higher in the massive
Prothrombin time 1.070 0.8591.334 0.546
Operation time 1.001 1.0001.003 0.101
transfusion group than in the no-massive transfusion
LT, liver transplantation; WBC, white blood cell. aOther diseases included group (6.6% vs. 1.8%, P = 0.068). Previous studies
hepatoblastoma, viral hepatitis, toxic hepatitis, liver cirrhosis, acute liver failure, glycogen showed that massive transfusion was commonly
storage disease, and metabolic disease. bOther techniques included right lobe, dual left
lobe, and whole liver. associated with a wide range of complications, such as
transfusion reactions to liver graft, systemic
immunological deteriorations, metabolic
deteriorations, and coagulopathy [14], and indicated

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the need for careful monitoring and strategy to reduce 13. Ramos E, Dalmau A, Sabate A, Lama C, Llado L, Figueras J, et al.
Intraoperative red blood cell transfusion in liver transplantation: influence on
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