Appropriate emergency hemostatic intervention is required for children who sustain blunt liver and/or spleen injuries (BLSIs), even in an era when nonoperative management (NOM) is the mainstay.1–4 children , a splenic and/or hepatic artery pseudoaneurysm (PA) may develop in a considerable number of patients. These have been reported to occasionally rupture, however, which may result in fatal delayed bleeding with a risk of unexpected circulatory compromise.5–7
To address the family burden arising because of late concerns such as rebleeding from injured organs, treatment indications for PA formation and the prevention of rupture should be investigated, and appropriate guidelines issued. Highly selective use of interventional radiology (IR) has been recommended for pediatric trauma patients as a better balance of risk, benefit, and resource utilization.3,8 1,9–12 children remains controversial because of insufficient evidence on the association between the use of IR and clinical outcomes.8
We previously reported that active contrast extravasation on admission computed tomography (CT) was an independent predictor of PA development in pediatric patients with BLSIs.9 1,3,5–7,13,14
Within this context, we conducted a large-scale multicenter cohort study with the two objectives, namely, to describe the incidence of delayed PA development based on treatment in the acute phase and to characterize the clinical manifestations and subsequent clinical course of PA following BLSIs in children .
PATIENTS AND METHODS
Study Design and Setting
This study was conducted under a retrospective, multicenter, cohort design and was sponsored by the Japanese Association for Surgery of Trauma Multicenter Trial Committee. Data were accumulated between January 2008 and December 2019 from academic, nonacademic, and children 's hospitals in Japan. The study protocol was approved by the Japanese Association for Surgery of Trauma ethics committee and sequentially by the institutional review board at each participating hospital. Because this study was noninterventional and of minimal risk to subjects, the need for informed consent from each patient was waived in all hospitals, but consent could be declined under an opt-out policy. Our study protocol was registered on University Hospital Medical Information Network-Clinical Trials Registry as UMIN000041296.
Inclusion and Exclusion Criteria
Pediatric trauma patients 16 years and younger who had sustained any BLSIs were eligible. Inclusion was limited to patients admitted to an emergency care setting with at least an Abbreviated Injury Scale (AIS) grade of ≥I BLSIs as detected by any imaging method or operative findings. Interhospital transfer patients were eligible for inclusion with the medical record information, such as imaging and laboratory data. To prevent duplicate enrollment of interhospital transfer cases from both institutions, data in the database were merged if age, sex, date of birth, date of injury, and facility location matched precisely.
Exclusion criteria were the following: (1) patient had cardiopulmonary arrest on arrival; (2) patient had an AIS 6 injury of any part of the body; (3) parent or guardian refusal of treatment, or request for limited treatment, because of a severe head injury (head AIS score, ≥5); and (4) patient transfer to another hospital within 5 days of admission without required follow-up information.
Data Acquisition and Management
Study data were collected and managed through the Research Electronic Data Capture (Vanderbilt University, Nashville, TN) tool. A standardized data entry guide in line with our research protocols was developed, and web conferences were held to explain the Research Electronic Data Capture entry process for all local researchers at participating centers. Anonymized data were entered manually by local researchers. Detailed information on data cleaning and quality control is provided in Supplemental Digital Content, https://links.lww.com/TA/C734
Study Variables and Exposure
The following variables were collected: characteristics of participating hospital, patient baseline demographics (age, sex, body weight, preexisting illness), the circumstances of the injury, physiologic status on arrival (systolic blood pressure; shock index [SI], pediatric age-adjusted; heart rate; Glasgow Coma Scale), the severity of injuries (Injury Severity Score, the highest AIS in each anatomic region, the American Association for Surgery of Trauma [AAST] grade 1994 and 2018 update of splenic and hepatic injury15 16,17
The exposure was the use of IR as emergent or urgent hemostatic intervention.8 8
Outcome Variables and Definitions
The outcome of interest was posttraumatic PA formation. The characteristics of all PAs were described and delayed PA formation, which was detected on or after the second day after injury (but undetectable on CT scan on admission) were evaluated separately.18 9 9,19
Statistical Analysis
Descriptive analysis was performed to summarize the baseline characteristics of the entire cohort. Values were reported as mean ± SD for continuous variables with normal distributions as determined by assessment of skewness and kurtosis. For those continuous variables not possessing a normal distribution, median ± interquartile range (IQR) was used. Categorical variables are expressed as numbers and percentages (%), as appropriate. Intergroup comparisons of continuous variables were performed using the Kruskal-Wallis test, and comparisons of each categorical variable between groups were performed using the χ2 test. We described the outcomes, including delayed PA formation, by the management group within 48 hours of admission. We performed subgroup analyses according to the injured organ (spleen or liver). In addition, we described the clinical manifestations of PA (date of diagnosis, size, location) based on injury grade and the subsequent clinical course. All statistical analyses were two-sided, and a p value ≤0.05 indicated statistical significance. All analyses were carried out with commercial software, Stata/MP version 17 (StataCorp, College Station, TX).
RESULTS
Study Population and Baseline Characteristics
A total of 1,462 pediatric patients were admitted with a diagnosis of BLSIs to 83 participating centers between 2008 and 2019, of whom 1,407 met our eligibility criteria. Details of the participating centers are listed in Supplementary Digital Content, Supplementary Table S1, https://links.lww.com/TA/C734 https://links.lww.com/TA/C734 Figure 1 shows a flow diagram of the participants and reasons for exclusion.
Figure 1: Selection process for the study population.
Patient and hospital characteristics of all participants by management group within 48 hours of admission are summarized in Table 1 and Supplementary Table S2, https://links.lww.com/TA/C734 liver injury , 532 (38%) had a spleen injury , and 54 (4%) had both liver and spleen injuries. Median age was 9 years (IQR, 6–13 years), 67% were male, and median Injury Severity Score was 10 (6–19) among the overall cohort. The department most commonly in charge of treatment was adult emergency medicine (51%), followed by pediatric surgery (20%) and adult surgery (15%).
TABLE 1 -
Patient Characteristics of All Participants by Management Group Within 48 Hours of Admission
Management Group by Intervention Within 48 h
Overall Cohort (n = 1,407)
NOM Without IR
NOM With IR
OM (n = 53)
Combined IR/OM (n = 22)
p
Patient characteristic
Age, median [IQR], y
9 [6–13]
9 [6–12]
11 [8–14]
10 [6–14]
11 [6–15]
0.001
Sex, male (%)
943 (67%)
698 (66%)
188 (68%)
41 (77%)
16 (73%)
0.329
Body weight, median [IQR], kg
29 [20–45]
27 [20–41]
37 [25–50]
29 [20–46]
28 [20–47]
0.002
Any preexisting illness, n (%)
224 (16%)
170 (16%)
42 (15%)
10 (19%)
2 (9%)
0.744
Circumstances of injury, n (%)
0.001
Fall from height
310 (22%)
251 (24%)
44 (16%)
12 (23%)
3 (14%)
Fall down
105 (7%)
86 (8%)
18 (7%)
4 (8%)
1 (5%)
Sport
122 (9%)
88 (8%)
30 (11%)
9 (17%)
0 (0%)
Bicycle
270 (19%)
199 (19%)
58 (21%)
6 (11%)
4 (18%)
MVC
164 (12%)
112 (11%)
42 (15%)
11 (21%)
4 (18%)
MV vs. ped
340 (24%)
258 (24%)
64 (23%)
3 (6%)
7 (32%)
Abuse/assault
36 (3%)
25 (2%)
4 (1%)
3 (6%)
1 (5%)
Others blunt injury
60 (4%)
37 (4%)
16 (6%)
5 (9%)
2 (9%)
Physiologic status on arrival
SBP, median [IQR], mm Hg
114 [102–126]
115 [103–126]
113 [102–129]
93 [72–113]
99 [70–120]
<0.001
Shock,* n (%)
383 (28%)
236 (23%)
97 (36%)
35 (67%)
15 (68%)
<0.001
HR, median [IQR], beat/min
102 [87–120]
101 [87–120]
103 [87–120]
112 [90–145]
123 [106–164]
0.003
GCS score (total), median [IQR]
15 [14–15]
15 [14–15]
15 [14–15]
13 [8–15]
13 [6–15]
<0.001
Type of injury, n (%)
<0.001
Spleen injury
532 (38%)
345 (33%)
156 (57%)
26 (49%)
5 (23%)
Liver injury
821 (58%)
686 (65%)
102 (37%)
20 (38%)
13 (59%)
Both spleen and liver injury
54 (4%)
25 (2%)
18 (7%)
7 (13%)
4 (18%)
Grade of injury**
ISS, median [IQR]
10 [6–19]
9 [5–17]
16 [9–26]
19 [13–38]
32 [13–42]
<0.001
Spleen injury , n (%)
<0.001
I/II
247/586 (42%)
212/370 (57%)
30/174 (17%)
4/33 (12%)
1/9 (11%)
III
192/586 (33%)
129/370 (35%)
51/174 (29%)
11/33 (33%)
1/9 (11%)
IV
107/586 (18%)
24/370 (6.5%)
69/174 (40%)
11/33 (33%)
3/9 (33%)
V
40/586 (7%)
5/370 (1.4%)
24/174 (14%)
7/33 (21%)
4/9 (44%)
Liver injury , n (%)
<0.001
I/II
552/875 (63%)
517/711 (73%)
25/120 (21%)
7/27 (26%)
3/17 (18%)
III
211/875 (24%)
151/711 (21%)
45/120 (38%)
9/27 (33%)
6/17 (35%)
IV
99/875 (11%)
42/711 (5.9%)
47/120 (39%)
4/27 (15%)
6/17 (35%)
V
13/875 (1.5%)
1/711 (0.1%)
3/120 (2.5%)
7/27 (26%)
2/17 (12%)
Imaging data on admission
FAST positive, n (%)
607 (43%)
370 (35%)
174 (63%)
43 (81%)
20 (91%)
<0.001
CE on initial CT scan, n (%)
<0.001
None or unknown
1,167 (83%)
1,010 (96%)
117 (42%)
32 (60%)
8 (36%)
Intraparenchymal CE
101 (7%)
27 (3%)
66 (24%)
4 (8%)
4 (18%)
CE within subcapsular hematoma
54 (4%)
10 (1%)
41 (15%)
2 (4%)
1 (5%)
CE into the free peritoneal cavity
85 (6%)
9 (1%)
52 (19%)
15 (28%)
9 (41%)
PA detected on the day of injury
16 (1%)
8 (0.8%)
16 (5.8%)
0 (0%)
0 (0%)
<0.001
*By SIPA above cutoff.
**The American Association for the Surgery of Trauma Organ Injury Scale grade (2018 revision).
p Values of the table are for four-group comparisons using the Kruskal-Wallis test or χ2 test.
Interquartile range presents the 25th and 75th percentiles, as appropriate.
CE, contrast extravasation; FAST, focused assessment with sonography for trauma: GCS, Glasgow Coma Scale; HR, heart rate; ISS, Injury Severity Score; MVC, motor vehicle crash; MV vs. ped, motor vehicle versus pedestrian; SBP, systolic blood pressure; SIPA, shock index, pediatric age-adjusted.
Descriptive Statistics of Endovascular and Surgical Intervention
A total of 316 patients (22% of the entire cohort) underwent IR treatment, of whom 276 (20% of the entire cohort) underwent IR treatment within 48 hours of admission. Twenty-five patients underwent two or more IR sessions during the same hospitalization. Of the 276 patients who underwent IR within 48 hours of admission, 236 (86%) underwent angioembolization, while 40 patients (14%) underwent diagnostic IR with angiography only. The most common indication for first IR intervention was acute hemorrhage (86%), followed by delayed hemorrhage (6%) and unruptured PA (6%). A higher proportion of patients in the NOM with IR group and combined IR/OM group had active contrast extravasation and PA detected on admission CT scan, regardless of hemodynamic status (Table 1 ). No patient required IR for arteriovenous or arterioportal shunt in the liver. The commonest location of splenic artery embolization was the distal splenic artery in 85% of cases (selective embolization), while proximal splenic artery embolization was performed in 13% of cases. The commonest location of hepatic artery embolization was distal branches from the right and left hepatic artery branches, in 63% of cases. Endovascular interventions were more frequently performed in those facilities and departments primarily serving adult patients, such as adult trauma centers and emergency medicine departments (Supplementary Table S2, https://links.lww.com/TA/C734
A total of 79 patients (5.6% of the entire cohort) underwent OM, of whom 53 (3.8% of the whole cohort) underwent OM within 48 hours of admission. Among the overall cohort, 22 patients (1.6%) underwent combined OM and IR intervention within 48 hours of admission, of whom 13 underwent IR intervention followed by OM, while 9 patients underwent OM followed by IR. The most common indication for first surgical intervention was acute hemorrhage (90%), followed by peritonitis (9%). The most common first surgical procedure for spleen injury was total splenectomy (63%) followed by suture repair and/or application of hemostatic agents (28%) and damage-control surgery (14%). The most common first surgical procedure for liver injury was damage-control surgery (51%) followed by suture repair and/or application of hemostatic agents (40%), and partial hepatectomy (13%).
Outcomes by Management Group
Overall, 80 of 1,407 patients (5.7%) developed delayed PA formation, and 14 of 1,407 (1.0%) experienced delayed PA rupture. By management group, 12% of patients in the NOM with IR group developed delayed PA, while 4.1% of patients in the NOM group developed delayed PA (Table 2 ). In both the spleen and liver injury subgroups, delayed PA formation occurred approximately two to four times more frequently in the NOM with IR group than in the NOM group (Supplementary Table S3, https://links.lww.com/TA/C734 p < 0.001) (Table 2 ). Similar trends were observed for the frequency of each blood product (packed red blood cell, fresh frozen plasma, and platelets) transfused and for the cumulative total transfusion volume during the entire hospitalization and within 24 hours of admission. No significant differences were found in in-hospital mortality between the NOM group and NOM with IR group on univariate analysis (0.7% vs. 1.1%, p = 0.467). The most common cause of death was traumatic brain injury, which was about twice as common a cause as death due to hemorrhagic shock caused by BLSIs.
TABLE 2 -
Outcomes by Management Group Within 48 Hours of Admission
Management Group by Intervention Within 48 h
Outcome
Overall Cohort (n = 1,407)
NOM
NOM
OM
Combined IR/OM
p
Delayed PA formation
80 (5.7%)
43 (4.1%)
32 (12%)
2 (3.8%)
3 (14%)
<0.001
Blood transfusion requirement*
283 (20%)
102 (9.7%)
116 (42%)
44 (83%)
21 (95%)
<0.001
Cumulative blood transfusion**
PRBC, median [IQR] mean ± SD, mL
0 [0–0] 279 ± 1,000
0 [0–0] 98 ± 606
0 [0–560] 395 ± 854
1,120 [280–3,080] 1,968 ± 2,102
2,800 [1,680–5,320] 3,570 ± 2,902
<0.001
FFP, median [IQR] mean ± SD, mL
0 [0–0] 226 ± 821
0 [0–0] 70 ± 394
0 [0–480] 343 ± 790
720 [0–2,880] 1,573 ± 1,831
2,880 [960–5,280] 3,160 ± 2,542
<0.001
Platelets, median [IQR] mean ± SD, U
0 [0–0] 1.3 ± 7.0
0 [0–0] 0.4 ± 4.2
0 [0–0] 1.1 ± 5.9
0 [0–20] 11 ± 19
10 [0–30] 20 ± 21
<0.001
In-hospital mortality
21 (1.5%)
7 (0.7%)
3 (1.1%)
8 (15%)
3 (14%)
<0.001
Splenic salvage (in spleen injury cases)
558/586 (95%)
368/390 (94%)
174/174 (100%)
12/33 (36%)
4/9 (44%)
<0.001
*Any blood products (red blood cell, fresh frozen plasma, platelet, and whole blood) administered during hospitalization.
**Each blood component administered during hospitalization.
All statistics reported as n (%) or median [IQR]. Mean ± SD is also reported for median values of 0.
p Values of the table are for four-group comparisons using the Kruskal-Wallis test or χ2 test.
Interquartile range presents the 25th and 75th percentiles, as appropriate.
FFP, fresh frozen plasma; PRBC, packed red blood cell.
Clinical Manifestations and Natural History of PA Based on Injury Grade
Overall, 104 of 1,407 patients (7%) developed PA, including PA detected on the day of injury. Median time to all PA diagnoses and delayed PA diagnoses from injury day was 6 days (IQR, 2–10 days) and 7 days (5–10 days), respectively. Figure 2 illustrates the distribution of PA diagnosis dates by injury grade. The most common imaging modality that diagnosed PA was CT scan (82%), followed by angiography (11%) and abdominal ultrasound (8%). These imaging tests were performed when symptoms were present, as well as at the attending physician's discretion when symptoms were absent on follow-up imaging tests. Among the overall cohort, follow-up imaging tests with both CT scans and ultrasound were conducted in approximately 72% of patients in situations where the indication was not limited. Follow-up CT scans were also carried out in 84% of patients with an injury grade of III or higher and in 87% with contrast extravasation on the initial CT image. No significant differences were found in the diameter of PA and distance from spleen/liver capsule to PA among the different AAST grades of injury (2018 revision) (p = 0.515 and p = 0.151, respectively) (Fig. 3 ). Similar results were obtained using the AAST grade of injury 1994 version (Supplementary Fig. S2, https://links.lww.com/TA/C734 Fig. 3 ). In addition, the median distance from the spleen/liver capsule to PA was 13 mm (5–17 mm) in the ruptured PA group, while it was 11 mm (6–18 mm) in the unruptured PA group (Fig. 3 ). Among the 104 patients who developed PA, PA resolved spontaneously without intervention in 47 patients (45%) (Table 3 ). A total of 41 patients (39%) underwent prophylactic IR intervention for unruptured PA, while 14 patients (13%) underwent emergency angioembolization for PA rupture (Table 3 ). One patient (1%) underwent emergency total splenectomy because of delayed PA rupture. No patient required blood transfusion at the time of delayed PA rupture. Median time to PA rupture from injury day was 9 days (3–13 days).
Figure 2: Histogram showing date of PA diagnosis by AAST grade of spleen/liver injury (2018 revision).
Figure 3: Dot plot showing (A ) diameter of PA and (B ) distance from spleen/liver capsule to PA by AAST grade of injury (2018 revision).
TABLE 3 -
Management of
Pseudoaneurysm Based on AAST Grade of Spleen/
Liver Injury (2018 Revision)
Grade of Injury*
Grades I and II
Grade III
Grade IV
Grade V
Type of management
Spontaneous resolution of PA without intervention
7/15 (47%)
18/41 (44%)
18/42 (43%)
4/6 (67%)
47/104 (45%)
Prophylactic IR for unruptured PA
7/15 (47%)
16/41 (39%)
16/42 (38%)
2/6 (33%)
41/104 (39%)
Prophylactic operation for unruptured PA
0
0
0
0
0
Emergent angioembolization for PA rupture
0
7/41 (17%)
7/42 (17%)
0
14/104 (13%)
Emergent operation for PA rupture
0
0
1/42 (2%)
0
1/104 (1%)
Conservative follow-up even after PA has ruptured
1/15 (7%)
0
0
0
1/104 (1%)
Total number
15
41
42
6
104
*The American Association for the Surgery of Trauma Organ Injury Scale grade (2018 revision).
DISCUSSION
In this retrospective multicenter cohort study, we found that the overall incidence of delayed PA formation was 5.7%. Delayed PA formation was identified in as many as 12% of patients who underwent emergent IR in the acute phase as an adjunct to NOM. Among patients who developed PA, 39% underwent prophylactic IR for unruptured PA, while 13% underwent emergent angioembolization for PA rupture and only one required splenectomy because of delayed PA rupture. At least 45% experienced spontaneous resolution of PA without intervention. Given that many of the identified PAs received prophylactic IR treatment, it is conceivable that some of them had a chance of resolving spontaneously. Our findings provide the new perspective that the risk of delayed PA formation still exists even after acute phase IR in pediatric BLSIs and that an accordingly high level of suspicion must be maintained whenever these patients are treated. Furthermore, given the paucity of clear evidence and latent risk of delayed PA rupture, the decision to perform prophylactic angioembolization for PA requires shared decision making with patients and their families under precisely informed consent.
Some review articles based on the findings of small studies reported no PA were found in AAST grade I or II injuries and that patients with high-grade (grade IV or V) injuries appeared to have the greatest risk of developing PA.1,5 9,20 18,21,22 9,18,20–22
In addition, many clinicians consider that patients who undergo IR treatment in the acute phase will be less likely to develop delayed PA in the late phase. However, in our study population, patients in the NOM with IR group had a relatively higher incidence of delayed PA development. In the group that received IR intervention as an adjunct to NOM, there was a higher proportion of patients with more complex and severe injury grades and accordingly may have had vascular injuries that were not detected on imaging in the acute postinjury phase. A retrospective study that reviewed adult blunt splenic injuries demonstrated that 10% of patients who underwent admission angiography eventually required either “second-look” angiography or laparotomy to control delayed hemorrhage.23,24 9 21,23 21,23
Whether all PA should receive equal intervention at the time of diagnosis is an important clinical question.9,25 25
One reason why only one patient in this study required total splenectomy for PA may be related to the very low rate of proximal embolization on admission angiography. In the absence of data regarding the use of IR in children , most of our knowledge on this topic is extrapolated from the adult literature. A recent retrospective evaluation of adult splenic injuries from a level I trauma center in the United States reported that a relatively high proportion of patients who developed PA required subsequent splenectomy.26 24,27 28
Our study has several strengths. First, many unique variables not available in the national trauma database were entered from directly reviewed medical records and historical images from trained site researchers, which proved a highly accurate assessment of PA, active bleeding, and AAST injury grade (both 1994 version and 2018 revision). Second, we included interhospital transfer cases in this study because pediatric trauma patients are often initially transported to a local emergency hospital and then transferred to an urban trauma center or transferred from an adult trauma center to a children 's hospital. Third, through repeated data cleaning, we developed a high-quality data set with few outliers and missing values.
Conversely, our study also has several limitations. First, there was no standardized pediatric trauma protocol used to manage the patients in this study. The variation in management strategies across participating facilities and departments responsible for pediatric trauma patients might therefore have influenced our results and could have skewed the findings in favor of practices followed at those sites, which contributed more data to the study. The results of this study were obtained in the context of unique Japanese practice patterns that do not adhere to current standard guidelines in the United States, and these practice patterns need to be considered when interpreting the present findings. Second, delayed PA formation is a rare event; even with a large multicenter study, it can be challenging to capture all events. Moreover, some events may have been underreported because routine follow-up CT imaging for pediatric patients was not recommended.1,3 9 29,30
Notwithstanding these possible limitations, our findings have several important clinical implications for evidence on the natural history and clinical course of PA following BLSIs in pediatric patients. These will be essential in establishing standardized recommendations or guidelines. This research may provide an opportunity for countries where standardized guidelines do not exist, such as Japan, to review their own practice. Furthermore, it may improve evidence-based practice with reference to existing guidelines and trigger the establishment of standardized recommendations suited to national circumstances.
CONCLUSION
Endovascular intervention is widely applied to treat acute and delayed hemorrhage as well as to prevent future bleeding from PA rupture following pediatric BLSIs in Japan. Our study results suggest that patients undergoing angioembolization for acute hemorrhage are still at risk of delayed PA development and rebleeding from PA rupture, regardless of injury grade. While endovascular interventions are usually successful for PA management, including ruptured cases, given the high incidence of spontaneous resolution, the ideal management of delayed PA needs further clarification.
AUTHORSHIP
M.K., Y.K., H.Y, S.F., K.M., A.S., A.T., A.K., and S.K. designed the study. M.K. and K.M. searched the literature. M.K., Y.K., H.Y., A.K., M.G., K.H., N.M., K.S., K.T., and H.Y. collected the data. M.K. and S.F. analyzed the data. M.K. wrote the manuscript. All authors participated in data interpretation, article preparation, and critical revisions and approved the final article.
ACKNOWLEDGMENTS
The authors thank Dr. Keinosuke Ishido, Dr. Yukijya Kang, and Dr. Takafumi Shimizu for their contributions to data collection at each institution. The authors thank Dr. Soichi Murakami, Dr. Norio Sato, Dr. Satoru Murata, and Dr. Hidemitsu Mototake for recruiting facilities for this study. The authors thank Dr. Junichi Matsumoto and Dr. Ryoichi Kitamura for providing advice on the research plan regarding IR.
DISCLOSURE
The authors declare no conflicts of interest.
Collaborators of SHIPPs (Splenic and Hepatic Injury in Pediatric Patients) Study Group: Tomoya Ito (Department of Pediatric Emergency Medicine, Aichi Children 's Health and Medical Center, Aichi, Japan); Motoyoshi Yamamoto and Yoshihiro Yamamoto (Department of Emergency Medicine, Aizawa Hospital, Nagano, Japan); Hiroto Manase (Department of Surgery, Asahikawa Red Cross Hospital, Hokkaido, Japan); Nozomi Takahashi (Department of Emergency and Critical Care Medicine, Chiba University Hospital, Chiba, Japan); Akinori Osuka (Department of Trauma, Critical Care Medicine and Burn Center, Chukyo Hospital, Nagoya, Japan); Suguru Annen (Department of Emergency and Critical Care Medicine, Ehime University Hospital, Ehime, Japan); Nobuki Ishikawa (Department of Pediatric Surgery, Fukui Prefectural Hospital, Fukui, Japan); Kazushi Takayama (Trauma, Emergency and Critical Care Center, Fukuoka University Hospital, Fukuoka, Japan); Keita Minowa (Department of Emergency and Critical Care Medicine, Hachinohe City Hospital, Aomori, Japan); Kenichi Hakamada (Department of Gastroenterological Surgery, Hirosaki University Hospital, Aomori, Japan); Akari Kusaka (Critical Care Medical Center, Hiroshima Prefectural Hospital, Hiroshima, Japan); Mineji Hayakawa and Shota Kawahara (Department of Emergency Medicine, Hokkaido University Hospital, Hokkaido, Japan); Satoshi Hirano (Department of Gastroenterological Surgery II, Faculty of Medicine, Hokkaido University, Hokkaido, Japan); Marika Matsumoto (Department of Emergency and Critical Care Medicine, Hyogo Emergency Medical Center, Hyogo, Japan); Kohei Kusumoto (Department of Pediatric Intensive Care, Hyogo Prefectural Amagasaki General Medical Center, Hyogo, Japan); Hiroshi Kodaira (Department of Emergency Medicine, Hyogo Prefectural Awaji Medical Center, Hyogo, Japan); Chika Kunishige (Acute Care Medical Center, Hyogo Prefectural Kakogawa Medical Center, Hyogo, Japan); Keiichiro Toma and Yusuke Seino (Department of Pediatric Critical Care Medicine, Hyogo Prefectural Kobe Children 's Hospital, Hyogo, Japan); Michio Kobayashi (Department of Emergency Medicine, Ishinomaki Red Cross Hospital, Miyagi, Japan); Masaaki Sakuraya (Division of Emergency and Critical Care Medicine, JA Hiroshima General Hospital, Hiroshima, Japan); Takafumi Shinjo and Shigeru Ono (Department of Emergency and Critical Care Medicine and Department of Pediatric Surgery, Jichi Medical University Hospital, Tochigi, Japan); Hideto Yasuda and Haruka Taira (Department of Emergency and Critical Care Medicine, Jichi Medical University Saitama Medical Center, Saitama, Japan); Kazuhiko Omori (Department of Acute Critical Care Medicine, Juntendo University Shizuoka Hospital, Shizuoka, Japan); Yutaka Kondo (Department of Emergency and Critical Care Medicine, Juntendo University Urayasu Hospital, Chiba, Japan); Yoshio Kamimura (Department of Emergency Medicine, Kagoshima City Hospital, Kagoshima, Japan); Atsushi Shiraishi and Rei Tanaka (Emergency and Trauma Center, Kameda Medical Center, Chiba, Japan); Yukihiro Tsuzuki (Department of Pediatric Surgery, Kanagawa Children 's Medical Center, Kanagawa, Japan); Yukio Sato (Department of Emergency and Critical Care Medicine, Keio University Hospital, Tokyo, Japan); Noriaki Kyogoku (Department of Surgery, Kitami Red Cross Hospital, Hokkaido, Japan); Masafumi Onishi and Kaichi Kawai (Department of Emergency Medicine, Kobe City Medical Center General Hospital, Hyogo, Japan); Kazuyuki Hayashida and Keiko Terazumi (KRC Severe Trauma Center/Trauma and Critical Care, Japanese Red Cross Kumamoto Hospital, Kumamoto, Japan); Akira Kuriyama and Susumu Matsushime (Emergency and Critical Care Center, Kurashiki Central Hospital, Okayama, Japan); Osamu Takasu and Toshio Morita (Advanced Emergency Medical Service Center, Kurume University Hospital, Fukuoka, Japan); Nagato Sato (Department of Surgery, Kushiro City General Hospital, Hokkaido, Japan); Wataru Ishii and Michitaro Miyaguni (Department of Emergency Medicine and Critical Care, Kyoto Second Red Cross Hospital, Kyoto, Japan); Shingo Fukuma (Human Health Sciences, Kyoto University Graduate School of Medicine, Kyoto, Japan); Yosuke Nakabayashi and Yoshimi Ohtaki (Advanced Medical Emergency Department and Critical Care Center, Maebashi Red Cross Hospital, Gunma, Japan); Kiyoshi Murata and Masayuki Yagi (Department of Emergency Medicine and Acute Care Surgery, Matsudo City General Hospital, Chiba, Japan); Tadashi Kaneko (Emergency and Critical Care Center, Mie University Hospital, Mie, Japan); Shigeru Takamizawa (Department of Pediatric Surgery, Nagano Children 's Hospital, Nagano, Japan); Akihiro Yasui (Department of Pediatric Surgery, Nagoya University Hospital, Nagoya, Japan); Yasuaki Mayama (Department of Emergency Medicine, Nakagami Hospital, Okinawa, Japan); Masafumi Gima (Critical Care Medicine, National Center for Child Health and Development, Tokyo, Japan); Ichiro Okada (Department of Critical Care Medicine and Trauma, National Hospital Organization Disaster Medical Center, Tokyo, Japan); Asuka Tsuchiya and Koji Ishigami (Department of Emergency Medicine, National Hospital Organization Mito Medical Center, Ibaraki, Japan); Yukiko Masuda (Emergency and Critical Care Center, National Hospital Organization Nagasaki Medical Center, Nagasaki, Japan); Yasuo Yamada (Department of Emergency Medicine, National Hospital Organization Sendai Medical Center, Miyagi, Japan); Hiroshi Yasumatsu (Shock and Trauma Center, Nippon Medical School Chiba Hokusoh Hospital, Chiba, Japan); Kenta Shigeta (Department of Emergency and Critical Care Medicine, Nippon Medical School Hospital, Tokyo, Japan); Kohei Kato (Department of Surgery, Obihiro Kosei Hospital, Hokkaido, Japan); Fumihito Ito (Department of Emergency and Critical Care Medicine, Ohta Nishinouchi Hospital, Fukushima, Japan); Atsuyoshi Iida (Department of Emergency Medicine, Okayama Red Cross Hospital, Okayama, Japan); Tetsuya Yumoto and Hiromichi Naito (Department of Emergency, Critical Care and Disaster Medicine, Okayama University Hospital, Okayama, Japan); Morihiro Katsura and Yoshitaka Saegusa (Department of Surgery, Okinawa Chubu Hospital, Okinawa, Japan); Tomohiko Azuma (Department of Surgery, Okinawa Hokubu Hospital, Okinawa, Japan); Shima Asano (Department of Surgery, Okinawa Miyako Hospital, Okinawa, Japan); Takehiro Umemura and Norihiro Goto (Department of Emergency Medicine, Okinawa Nanbu Medical Center and Children 's Medical Center, Okinawa, Japan); Takao Yamamoto (Department of Surgery, Okinawa Yaeyama Hospital, Okinawa, Japan); Junichi Ishikawa (Department of Pediatric Emergency Medicine, Osaka City General Hospital, Osaka, Japan); Elena Yukie Uebayashi (Department of Pediatric Surgery, Osaka Red Cross Hospital, Osaka, Japan); Shunichiro Nakao (Department of Traumatology and Acute Critical Medicine, Osaka University Graduate School of Medicine, Osaka, Japan); Yuko Ogawa (Department of Intensive Care Medicine, Osaka Women's and Children 's Hospital, Osaka, Japan); Takashi Irinoda (Department of Emergency and Critical Care Medicine, Osaki Citizen Hospital, Osaka, Japan); Yuki Narumi (Senshu Trauma and Critical Care Center, Rinku General Medical Center, Osaka, Japan); Miho Asahi (Department of Emergency and Critical Care Medicine, Saga University Hospital, Saga, Japan); Takayuki Ogura and Takashi Hazama (Department of Emergency Medicine and Critical Care Medicine, Saiseikai Utsunomiya Hospital, Tochigi, Japan); Shokei Matsumoto (Department of Trauma and Emergency Surgery, Saiseikai Yokohamashi Tobu Hospital, Kanagawa, Japan); Daisuke Miyamoto (Department of Emergency, Trauma and Critical Care Medicine, Saitama Children 's Medical Center, Saitama, Japan); Keisuke Harada and Narumi Kubota (Department of Emergency Medicine, Sapporo Medical University Hospital, Hokkaido, Japan); Yusuke Konda (Department of Emergency and Critical Care, Sendai City Hospital, Miyagi, Japan); Takeshi Asai (Department of Pediatric Surgery, Shikoku Medical Center for Children and Adults, Kagawa, Japan); Tomohiro Muronoi (Department of Acute Care Surgery, Shimane University Hospital, Shimane, Japan); Kazuhide Matsushima (Division of Acute Care Surgery, University of Southern California, Los Angeles, CA); Toru Hifumi and Kasumi Shirasaki (Department of Emergency and Critical Care Medicine, St. Luke's International Hospital, Tokyo, Japan); Shigeyuki Furuta and Atsuko Fujikawa (Department of Pediatric Surgery and Department of Radiology, St. Marianna University School of Medicine Hospital, Kanagawa, Japan); Makoto Takaoka (Himeji Emergency Trauma and Critical Care Center, Steel Memorial Hirohata Hospital, Hyogo, Japan); Kaori Ito (Department of Emergency Medicine, Division of Acute Care Surgery, Teikyo University Hospital, Tokyo, Japan); Satoshi Nara (Emergency and Critical Care Medical Center, Teine Keijinkai Hospital, Hokkaido, Japan); Shigeki Kushimoto and Atsushi Tanikawa (Department of Emergency and Critical Care Medicine, Tohoku University Hospital, Miyagi, Japan); Masato Tsuchikane (Department of Emergency Medical and Critical Medicine, Tokai University Hachioji Hospital, Tokyo, Japan); Naoya Miura and Naoki Sakoda (Department of Emergency and Critical Care Medicine, Tokai University Hospital, Kanagawa, Japan); Tadaaki Takada (Department of Emergency and Critical Care Medicine, Tokushima Red Cross Hospital, Tokushima, Japan); Shogo Shirane (Department of Emergency and Critical Care Medicine, Tokyo Bay Urayasu Ichikawa Medical Center, Chiba, Japan); Akira Endo and Keita Nakatsutsumi (Trauma and Acute Critical Care Center, Tokyo Medical and Dental University Hospital of Medicine, Tokyo, Japan); Kenta Sugiura and Yusuke Hagiwara (Division of Pediatric Emergency Medicine, Tokyo Metropolitan Children 's Medical Center, Tokyo, Japan); and Tamotsu Gotou (Tajima Emergency and Critical Care Medical Center, Toyooka Hospital, Hyogo, Japan).
This study was supported by a medical research grant for traffic accident from The General Insurance Association of Japan (grant number: 21-1-016). The funding source and the study sponsor had no role in study design, collection, analysis, or interpretation of the data.
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