Kobayashi et al.

BMC Surgery (2022) 22:321

https://doi.org/10.1186/s12893-022-01769-8

RESEARCH Open Access

Prediction model for irreversible intestinal

ischemia in strangulated bowel obstruction
Toshimichi Kobayashi, Naokazu Chiba, Itsuki Koganezawa, Masashi Nakagawa, Kei Yokozuka, Shigeto Ochiai,
Takahiro Gunji, Toru Sano, Koichi Tomita, Satoshi Tabuchi, Eiji Hidaka and Shigeyuki Kawachi*

Abstract
Background: Preoperatively diagnosing irreversible intestinal ischemia in patients with strangulated bowel obstruc-
tion is difficult. Therefore, this study aimed to establish a prediction model for irreversible intestinal ischemia in stran-
gulated bowel obstruction.
Methods: We included 83 patients who underwent emergency surgery for strangulated bowel obstruction between
January 2014 and March 2022. The predictors of irreversible intestinal ischemia in strangulated bowel obstruction
were identified using logistic regression analysis, and a prediction model for irreversible intestinal ischemia in strangu-
lated bowel obstruction was established using the regression coefficients. Receiver operating characteristic analysis
and fivefold cross-validation was used to assess the model.
Results: The prediction model (range, 0–4) was established using a white blood cell count of ≥ 12,000/µL and the
computed tomography value of peritoneal fluid that was ≥ 20 Hounsfield units. The areas of the receiver operating
characteristic curve of the new prediction model were 0.814 and 0.807 after fivefold cross-validation. A score of ≥ 2
was strongly suggestive of irreversible intestinal ischemia in strangulated bowel obstruction and necessitated bowel
resection (odds ratio = 15.938). The bowel resection rates for the prediction scores of 0, 2, and 4 were 15.2%, 66.7%,
and 85.0%, respectively.
Conclusion: Our model may help predict irreversible intestinal ischemia that necessitates bowel resection for
strangulated bowel obstruction cases and thus enable surgeons to recognize the severity of the situation, prepare
for deterioration of patients with progression of intestinal ischemia, and select the appropriate surgical procedure for
treatment.
Keywords: Bowel strangulation, Intestinal ischemia, Prediction, Computed tomography, Surgical emergency,
Preoperative diagnosis

Background immediate surgery because intestinal ischemia (II) due to

Strangulated bowel obstruction (SBO) is defined as bowel bowel strangulation can lead to bowel necrosis and even
obstruction with compromised intestinal blood flow and perforation, eventually causing septic shock. Particularly,
can be caused by a fibrous cord, torsion, internal her- as for SBO with irreversible II, a delayed intervention has
nia, or adhesions due to previous abdominal surgery [1]. a high risk of mortality, and the mortality rate for SBO
SBO is a serious condition requiring early diagnosis and is reportedly 16% in patients with irreversible II, com-
pared to 3% in patients with reversible II [2]. Identify-
ing patients with irreversible II is vital to understanding
*Correspondence: [email protected] the severity and managing the deteriorating condition,
Department of Digestive and Transplantation Surgery, Tokyo Medical including perioperative intensive care.
University Hachioji Medical Center, Tokyo, Japan

© The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
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Kobayashi et al. BMC Surgery (2022) 22:321 Page 2 of 7

Computed tomography (CT) can detect SBO with Finally, 83 patients were included, and all of these were
a sensitivity ranging from 73 to 100% and a specificity confirmed for closed-loop obstruction due to mesen-
ranging from 61 to 100% [3]. However, to distinguish teric torsion or internal herniation at operation. Of
between irreversible and reversible II in SBO preopera- these, 42 had irreversible II at laparotomy and required
tively remains challenging. Regardless of the experience bowel resection (resection group; n = 42), whereas 41
or seniority of the surgeon, physical examination for had reversible II and required lysis of adhesions but not
the detection of strangulation has a success rate of only bowel resection (non-resection group; n = 41). We com-
48% [4]. Moreover, despite advances in imaging, patients pared the clinical outcomes between the resection and
requiring emergency surgery are usually poor candidates non-resection groups.
for such examinations. Particularly, reduced bowel wall
enhancement on contrast-enhanced CT is reportedly Perioperative clinical variables
a significant predictive factor [5–7]. However, contrast Preoperative clinical variables included sex, age, body
agents are contraindicated in some patients due to severe mass index, previous history of laparotomy, vital signs
renal dysfunction or iodine allergy. Additionally, assess- (systolic blood pressure < 100 mmHg, body tempera-
ing the presence or absence of bowel wall enhancement ture ≥ 38 °C), blood gas analysis (pH, base excess), and
highly depends on clinicians and has a poor objective laboratory data, including white blood cell (WBC) count
value. Therefore, this study aimed to establish a predic- and C-reactive protein, hemoglobin, platelet, albumin,
tion model for irreversible II in SBO using objective fac- bilirubin, creatinine, and creatine kinase levels. Opera-
tors (besides contrast-enhanced CT findings). tive clinical variables included laparoscopic surgery,
intraoperative presence of hemorrhagic peritoneal fluid,
Methods operation time, and blood loss. In addition, pathologi-
Patients cal findings of resection specimens included ischemia,
This retrospective study was approved by the Tokyo mucosal hemorrhagic necrosis, and transluminal hemor-
Medical University Hachioji Medical Center Ethics Com- rhagic necrosis.
mittee (approval number TS2020-0358) and was con-
ducted in accordance with the principles outlined in the Radiographic variables
1964 Declaration of Helsinki and its later amendments. Radiographic variables included presence of free peri-
The need for informed consent was waived in view of toneal fluid around the strangulated intestine, emphy-
the retrospective study design by the Tokyo Medical sema, the mean CT value of the free peritoneal fluid on
University Hachioji Medical Center Ethics Committee. unenhanced CT, and reduced bowel wall enhancement
We examined the data of 89 patients diagnosed with on contrast-enhanced CT. The mean CT value of the free
SBO by clinical symptoms and CT findings of closed- peritoneal fluid was expressed in Hounsfield units (HU)
loop obstruction who underwent emergency operation and calculated as the mean of the region of interest by
between January 2014 and March 2022 at our depart- outlining the free peritoneal fluid without adjacent struc-
ment. Patients with large bowel obstruction, intraperito- tures and gases at the maximum area of free peritoneal
neal malignancy, and a history of ascites were excluded. fluid on the axial section of the CT image (Fig. 1a, b).

Fig. 1 CT values of peritoneal fluid. Free peritoneal fluid in the rectovesical pouch (a) and below the right diaphragm (b) on non-enhanced
computed tomography (CT) with mean CT values of 9.6 Hounsfield units (HU) and 38.6 HU, respectively, using a region-of-interest analysis
Kobayashi et al. BMC Surgery (2022) 22:321 Page 3 of 7

Statistical analysis patients, as 6 patients with severe renal function impair-

Statistical analyses were performed using the IBM SPSS ment and 3 with a history of allergy to iodinated contrast
Statistics, version 27.00 (IBM Corp., Armonk, NY, USA). agents were excluded. The presence of free peritoneal
In univariate analysis, the clinical and radiographic vari- fluid was the most common CT finding, present in 100%
ables were compared between the resection and non- of the resection group and 73.2% of the non-resection
resection groups. The Mann–Whitney U test was used group (P < 0.001). Reduced bowel wall enhancement was
to examine the differences in continuous data. Fisher’s found in 56.4% of the resection group and 17.1% of the
exact test or the χ2 test was used to compare categorical non-resection group (P < 0.001). The free peritoneal fluid
data between groups. P < 0.05 was considered statistically CT value on unenhanced CT scans was significantly
significant. higher in the resection group than in the non-resection
According to univariate analysis, preoperative clinical group (21.4 vs. 15.1 HU; P < 0.001).
and radiographic variables (except for contrast-enhanced Regarding operative variables, laparoscopic surgery
CT findings) with P < 0.05 were included in the multi- was performed in 16.7% and 36.6% in the resection and
variate analysis. Forward stepwise logistic regression non-resection groups, respectively, (P = 0.04), and hem-
analysis identified independent predictors of irrevers- orrhagic peritoneal fluid at operation was found in 88.l%
ible II necessitating bowel resection, and a final logistic and 34.1% of patients in the resection and non-resection
regression model was obtained. Continuous variables groups, respectively (P < 0.001). Operation time was sig-
were converted to binary variables at a cutoff value with nificantly longer in the resection group than in the non-
the maximum Youden index, and a new prediction model resection group (104 vs. 74 min; P = 0.002), and blood
was established. This model calculated the prediction loss was significantly higher in the resection group than
score as the sum of the scores assigned to the binary vari- in the non-resection group (100 vs. 10 mL; P < 0.001).
ables from the independent predictors corresponding to In addition, pathological analysis revealed findings of
the regression coefficient. To assess the discrimination hemorrhagic necrosis in 92.8% of the resection speci-
and calibration of the prediction model, receiver operat- mens (transluminal hemorrhagic necrosis in 71.4% and
ing characteristic (ROC) analysis and the Hosmer–Leme- mucosal hemorrhagic necrosis in 21.4%).
show test were used. To avoid overfitting, this model Base excess, WBC count, presence of free peritoneal
was evaluated using fivefold cross-validation. The rate of fluid, and peritoneal fluid CT value on unenhanced CT
bowel resection, sensitivity, specificity, and positive and scans, which are significant preoperative variables on
negative likelihood ratios were estimated for each score. univariate analysis, were included in multivariate analy-
Finally, using logistic regression analysis, odds ratios sis. The forward stepwise logistic regression analysis
(ORs) and 95% confidence intervals (CIs) were evalu- results showed that WBC count and the peritoneal fluid
ated between groups categorized by the best cutoff score CT value on unenhanced CT were significant predictors
from the ROC analysis. The power of the two-tailed inde- of irreversible II, necessitating bowel resection. The areas
pendent t-test at 5% alpha was estimated to compare the under the ROC curve (AUCs) were 0.741 (95% CI 0.633–
model score for the groups by using a post hoc power 0.849) for WBC count and 0.750 (95% CI 0.639–0.862)
analysis. for free peritoneal fluid CT value.

Results Prediction model

Univariate and multivariate analyses of the resection The prediction model was based on the final logistic
and non‑resection groups regression model. WBC count and free peritoneal fluid
The clinical and radiographic characteristics of the CT value were identified as independent predictors and
resection and non-resection groups are summarized in were converted into binary variables at the cutoff values
Table 1. There were no significant differences in patient of 12,000/µL and 20 HU based on the maximum Youden’s
characteristics or vital signs between groups. In blood index from the ROC curve, respectively. Patients without
gas analysis, base excess was lower in the resection group free peritoneal fluid were considered as having a free per-
than in the non-resection group (− 1.7 mEq/L vs. 0.35 itoneal fluid CT value of < 20 HU. The regression coeffi-
mEq/L; P = 0.006). Regarding laboratory data, only WBC cients for the two binary variables in logistic regression
counts were significantly higher in the resection group analyses were 1.658 and 2.104, respectively. For conveni-
than in the non-resection group (12,550/µL vs. 9100/µL; ence, the regression coefficient was rounded off to the
P < 0.001). nearest integer to generate scores for the two independ-
Unenhanced CT scans were obtained in all 83 patients, ent predictors; thus, 2 points were assigned to each vari-
while contrast-enhanced CT scans were obtained in 74 able (Table 2). The prediction score was calculated as the
Kobayashi et al. BMC Surgery (2022) 22:321 Page 4 of 7

Table 1 Comparison between the resection and non-resection groups

Resection group(n = 42) Non-resection group(n = 41) P-value

Patient characteristics
Age 75.5 (21–94) 72 (26–96) 0.433
Male sex 15 (35.7%) 22 (53.7%) 0.1
Body mass index (kg/m2) 19.9 (15.0–27.1) 20.4 (13.5–27.5) 0.909
Previous history of laparotomy 32 (76.2%) 31 (75.6%) 0.951
Vital signs
Systolic blood pressure < 100 mmHg 4 (9.5%) 1 (2.4%) 0.187
Body temperature > 38 °C 3 (7.1%) 3 (7.3%) 0.651
Blood gas analysis
pH 7.429 (7.219–7.575) 7.438 (7.23–7.542) 0.31
Base excess (mEq/L) −1.7 (− 14.7 to 6.3) 0.35 (− 17.8 to 8.5) 0.006
Laboratory data
WBC (/µL) 12,550 (4850–34,000) 9,100 (3060–20,600) < 0.001
CRP (mg/dL) 0.73 (0.02–28.84) 0.27 (0.02–33.16) 0.36
Hb (g/dL) 13.2 (7.4–20.6) 13.8 (8.3–22.1) 0.689
Plt (×104/µL) 25.7 (8.2–74.5) 22.6 (7.6–48.2) 0.515
Alb (g/dL) 3.5 (2.1–5.0) 3.7 (1.7–4.5) 0.45
Bil (mg/dL) 0.85 (0.2–1.7) 0.8 (0.3–7.0) 0.416
Cre (mg/dL) 0.735 (0.30–5.31) 0.75 (0.31–2.84) 0.743
CK (IU/L) 75 (20–1048) 81 (10–1156) 0.996
CT findings
Presence of peritoneal fluid 42 (100%) 30 (73.2%) < 0.001
Presence of emphysema 1 (2.4%) 0 (0%) 0.506
Poor or no contrast bowel wall ­enhancementa 22 (56.4%) 6 (17.1%) < 0.001
CT value of peritoneal fluid (HU) 21.4 (10.2–77.0) 15.1 (6.7–32.5) < 0.001
Operative factors
Laparoscopic surgery 7 (16.7%) 15 (36.6%) 0.04
Presence of hemorrhagic peritoneal fluid 37 (88.1%) 14 (34.1%) < 0.001
Operation time (min) 104 (53–291) 74 (36–143) 0.002
Blood loss (mL) 100 (10–2425) 10 (10–1570) < 0.001
Pathological findings
Ischemia 3 (7.1%) –
Mucosal hemorrhagic necrosis 9 (21.4%) –
Transluminal hemorrhagic necrosis 30 (71.4%) –
Categorical data are expressed as percentages, and continuous data are expressed as median (min–max)
WBC white blood cell, CRP C-reactive protein, Hb hemoglobin, Plt platelet, Alb albumin, Bil bilirubin, Cre creatinine, CK creatine kinase, CT computed tomography,
HU Hounsfield unit
a
Contrast-enhanced CT scan was not performed in three patients in the resection group and six patients in the non-resection group

Table 2 Predictors of irreversible intestinal ischemia necessitating

bowel resection
Table 3 Prediction model for irreversible intestinal ischemia
Variables Regression OR (95% CI) P-value Score necessitating bowel resection
coefficient
Variables Score
WBC (/µL) ≥ 12,000 1.658 5.249 (1.812–15.209) 0.002 2
(/µL) 0 2
CT value of free 2.104 8.201 (2.633–25.537) < 0.001 2 WBC (/µL) < 12,000 ≥ 12,000
peritoneal fluid
(HU) ≥ 20 (HU) CT value of free peritoneal fluid (HU) < 20 ≥ 20
The prediction score 0–4
WBC white blood cell, CT computed tomography, HU Hounsfield unit, OR odds
ratio, CI confidence interval WBC white blood cell, CT computed tomography, HU Hounsfield unit
Kobayashi et al. BMC Surgery (2022) 22:321 Page 5 of 7

sum of the points for each of the two independent pre- according to the degree of strangulation, and the count
dictors and ranged from 0 to 4 (Table 3). was higher in patients with bowel resection than in those
The AUC for the new prediction model was 0.814 (95% without [16]. In our study, hemorrhagic peritoneal fluid
CI 0.720–0.908) and 0.807 (95% CI 0.622–0.993) after during surgery was observed more frequently in the
fivefold cross-validation, which indicated good discrimi- resection than in the non-resection group, which may
nation. The Hosmer–Lemeshow test indicated adequate reflect the transmural hemorrhage due to strangulation.
goodness of fit (P = 0.391). The post hoc power analysis Previous studies have reported CT values of the exuda-
showed a power of 100% based on 83 patients at a 5% tive body fluids < 10 HU [17], while those of hemorrhagic
alpha level. peritoneal fluid range from 15 to 75 HU [18]. A recent
The bowel resection rate and the model’s diagnostic study reported that CT values of peritoneal fluid > 10 HU
performance are shown in Table 4. A score of 2 was set in cases of SBO indicate the need for bowel resection
as the optimal cutoff score based on the ROC curve, and [19]. It has been suggested that the greater the hemor-
logistic regression analysis showed that a score of 2 or rhage associated with the progression of II due to stran-
higher was strongly associated with irreversible II, neces- gulation, the higher the CT values of free peritoneal fluid.
sitating bowel resection (OR = 15.938, 95% CI 5.086– In our study, the AUC was 0.750, indicating a relatively
49.95, P < 0.001). accurate prediction of irreversible II.
The two indicators in our prediction model are objec-
Discussion tive indicators, allowing for objective and reproducible
In this study, we established a prediction model for irre- prediction of irreversible II in SBO. Additionally, these
versible II necessitating bowel resection in cases of SBO. indicators are readily available at most hospitals. Further-
Our model is based on two independent objective pre- more, the CT value of free peritoneal fluid can be quickly
dictors: the WBC count and the value of free peritoneal evaluated using only unenhanced CT scans. Reduced
fluid on unenhanced CT. bowel wall enhancement on contrast-enhanced CT has
Systemic inflammatory response syndrome is report- been reported as being helpful in predicting irreversible
edly associated with SBO [6, 8–12]. Particularly, only II in SBO, with a sensitivity of 75–81% and specificity of
high WBC counts have been associated with irreversible 19–74% [5, 7, 14]. However, contrast-enhanced CT may
II, reflecting the severity of inflammation due to the irre- be contraindicated in patients with severe renal dysfunc-
versible ischemic changes found in SBO [10]. Consistent tion or iodine allergy. In contrast, our model is useful
with previous studies, the WBC count was significantly even when contrast agents are contraindicated.
higher in the resection than in the non-resection group In our model, higher scores were associated with a
in the present study, and the AUC was 0.741, indicating a higher probability of bowel resection. Accordingly, we
relatively accurate prediction of irreversible II. believe that this model might help surgeons in recog-
Various CT findings, such as reduced bowel wall nizing the severity of the situation and in selecting the
enhancement, increased unenhanced bowel wall attenu- appropriate surgical procedure. For example, at a score
ation, and the presence of mesenteric fluid, have been of 0 (with a resection probability of 15.2%), immediate
associated with irreversible II in cases of SBO [5–7, 13– surgery may avoid a bowel resection for many patients
15]. In our study, the value of the free peritoneal fluid on with SBO. Moreover, it may be sufficient to release the
unenhanced CT was a significant predictor of irreversible strangulation, allowing for the choice of laparoscopic
II. SBO is caused by venous occlusion due to compres- surgery. In fact, in this study, laparoscopic surgery was
sion of the mesentery, causing transmural hemorrhage performed significantly more often in the non-resec-
following congestion, edema, and mucosal hemorrhage. tion group than in the resection group. At a score of
Thus, hemorrhagic peritoneal fluid is often observed in 2 (with a resection probability of 66.7%), laparoscopic
SBO. Kobayashi et al. reported that the presence of red surgery may be prioritized, keeping in mind that open
blood cells in the free peritoneal fluid in SBO increases surgery might be required due to resection of ischemic

Table 4 The rate of bowel resection and diagnostic performance of each score in the scoring model
Score Number of patients Rate of bowel resection Sensitivity (%) Specificity (%) LR+ LR−
(%)

0 33 15.2 100 0 1 –
2 30 66.7 88.1 68.3 2.78 0.17
4 20 85 40.5 92.7 5.53 0.64
LR+: positive likelihood ratio; LR−: negative likelihood
Kobayashi et al. BMC Surgery (2022) 22:321 Page 6 of 7

bowel and patient deterioration. Conversely, at a score Declarations

of 4 (with a resection probability of 85%), open surgery
Ethics approval and consent to participate
may be preferable considering the need for emergency This retrospective study was approved by the Tokyo Medical University
resection of the ischemic bowel immediately before Hachioji Medical Center Ethics Committee (approval number TS2020-0358)
patient deterioration. In addition, respiratory and cir- and was conducted in accordance with the principles outlined in the 1964
Declaration of Helsinki and its later amendments. The need for informed
culatory management can be considered preoperatively consent was waived in view of the retrospective study design by the Tokyo
as a precaution against further deterioration in patients Medical University Hachioji Medical Center Ethics Committee.
with progressive intestinal ischemia. Furthermore,
Consent for publication
higher scores were also associated with higher rates of Not applicable.
necrosis in the resection specimens. All 17 specimens
with a score of 4 in the resection group showed patho- Competing interests
The authors declare that they have no competing interests.
logical hemorrhagic necrosis, and of them, 14 (82.4%)
specimens showed transluminal hemorrhagic necrosis Received: 5 May 2022 Accepted: 8 August 2022
(data not shown).
Our study has several limitations. This was a single-
center retrospective study with a small sample size.
Multi-center prospective studies with large sample References
1. Hashimoto D, Hirota M, Matsukawa T, Yagi Y, Baba H. Clinical features of
sizes are required to support the findings. To reduce strangulated small bowel obstruction. Surg Today. 2012;42:1061–5.
overfitting, fivefold cross-validation was used to assess 2. Fevang BT, Fevang J, Stangeland L, Søreide O, Svanes K, Viste A. Complica-
the internal validation of our prediction model. How- tions and death after surgical treatment of small bowel obstruction: a
35-year institutional experience. Ann Surg. 2000;231:529–37.
ever, additional external validation is necessary to ver- 3. Millet I, Taourel P, Ruyer A, Molinari N. Value of CT findings to predict
ify its application. surgical ischemia in small bowel obstruction: a systematic review and
meta-analysis. Eur Radiol. 2015;25:1823–35.
4. Ten Broek RPG, Krielen P, Di Saverio S, Coccolini F, Biffl WL, Ansaloni L, et al.
Bologna guidelines for diagnosis and management of adhesive small
Conclusion bowel obstruction (ASBO): 2017 update of the evidence-based guide-
In conclusion, we established a prediction model for lines from the world society of emergency surgery ASBO working group.
World J Emerg Surg. 2018;13:24.
irreversible II in cases of SBO based on objective vari- 5. Millet I, Boutot D, Faget C, Pages-Bouic E, Molinari N, Zins M, et al.
ables, namely, the WBC count and the CT value of Assessment of strangulation in adhesive small bowel obstruction on the
free peritoneal fluid on unenhanced CT scans. Our basis of combined CT findings: implications for clinical care. Radiology.
2017;285:798–808.
model can be made readily available in most hospitals 6. Schwenter F, Poletti PA, Platon A, Perneger T, Morel P, Gervaz P. Clinico-
and may enable surgeons to recognize the severity of radiological score for predicting the risk of strangulated small bowel
the situation, prepare for the deterioration of patients obstruction. Br J Surg. 2010;97:1119–25.
7. Nakashima K, Ishimaru H, Fujimoto T, Mizowaki T, Mitarai K, Nakashima
with progression of intestinal ischemia, and select the K, et al. Diagnostic performance of CT findings for bowel ischemia and
appropriate surgical procedure for treatment. necrosis in closed-loop small-bowel obstruction. Abdom Imaging.
2015;40:1097–103.
8. Huang X, Fang G, Lin J, Xu K, Shi H, Zhuang L. A prediction model for rec-
Abbreviations ognizing strangulated small bowel obstruction. Gastroenterol Res Pract.
AUC​: Area under the receiver operating characteristic curve; CI: Confidence 2018;2018:7164648.
interval; CT: Computed tomography; HU: Hounsfield units; II: Intestinal 9. Mu JF, Wang Q, Wang SD, Wang C, Song JX, Jiang J, et al. Clinical factors
ischemia; OR: Odds ratio; ROC: Receiver operating characteristic; SBO: Strangu- associated with intestinal strangulating obstruction and recurrence in
lated bowel obstruction; WBC: White blood cell. adhesive small bowel obstruction: a retrospective study of 288 cases.
Medicine. 2018;97:e12011.
Acknowledgements 10. Miyauchi T, Kuroda T, Nisioka M, Hashimoto T, Kasamatu T, Kuratate S,
Not applicable. et al. Clinical study of strangulation obstruction of the small bowel. J Med
Invest. 2001;48:66–72.
Author contributions 11. Tsumura H, Ichikawa T, Hiyama E, Murakami Y, Sueda T. Systemic inflam-
Study conception and design: TK, NC, and SK. Acquisition of data: TK. Opera- matory response syndrome (SIRS) as a predictor of strangulated small
tion procedures: all authors. Analysis and interpretation of data: TK. Drafting of bowel obstruction. Hepatogastroenterology. 2004;51:1393–6.
manuscript: TK. Critical revision of manuscript: all authors. All authors read and 12. Takeuchi K, Tsuzuki Y, Ando T, Sekihara M, Hara T, Yoshikawa M, et al.
approved the final manuscript. Clinical studies of strangulating small bowel obstruction. Am Surg.
2004;70:40–4.
Funding 13. Kohga A, Kawabe A, Yajima K, Okumura T, Yamashita K, Isogaki J, et al.
The authors received no specific funding for this work. CT value of the intestine is useful predictor for differentiate irreversible
ischaemic changes in strangulated ileus. Abdom Radiol. 2017;42:2816–21.
Availability of data and materials 14. Rondenet C, Millet I, Corno L, Boulay-Coletta I, Taourel P, Zins M. Increased
All data generated or analyzed during this study are included in this article. unenhanced bowel-wall attenuation: a specific sign of bowel necrosis in
Further inquiries can be directed to the corresponding author. closed-loop small-bowel obstruction. Eur Radiol. 2018;28:4225–33.
15. Makita O, Ikushima I, Matsumoto N, Arikawa K, Yamashita Y, Taka-
hashi M. CT differentiation between necrotic and nonnecrotic small
Kobayashi et al. BMC Surgery (2022) 22:321 Page 7 of 7

bowel in closed loop and strangulating obstruction. Abdom Imaging.

1999;24:120–4.
16. Kobayashi S, Matsuura K, Matsushima K, Okubo K, Henzan E, Maeshiro
M. Effectiveness of diagnostic paracentesis and ascites analysis for sus-
pected strangulation obstruction. J Gastrointest Surg. 2007;11:240–6.
17. Abramowitz Y, Simanovsky N, Goldstein MS, Hiller N. Pleural effusion:
characterization with CT attenuation values and CT appearance. AJR Am
J Roentgenol. 2009;192:618–23.
18. Federle MP, Jeffrey RB Jr. Hemoperitoneum studied by computed tomog-
raphy. Radiology. 1983;148:187–92.
19. Matsushima K, Inaba K, Dollbaum R, Cheng V, Khan M, Herr K, et al. High-
density free fluid on computed tomography: a predictor of surgical inter-
vention in patients with adhesive small bowel obstruction. J Gastrointest
Surg. 2016;20:1861–6.

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