Diagnosis of Fibrotic Distal Ileum Stenosis after Ischemic Enteritis Using Transabdominal Ultrasonography

Abstract

Ischemic enteritis (IE) is a rare disorder which is caused by inadequate blood flow to small intestine. The diagnostic procedure of this disease has not sufficiently established because of its rarity. Here, we report a case of IE in a hemodialysis-dependent 70-year-old man and summarize the diagnostic options for IE. The patient was admitted to our hospital because of acute abdominal distention and vomiting. He presented with mild tenderness in the lower abdomen and slightly elevated C-reactive protein level as revealed by blood tests. Radiographic imaging showed small bowel obstruction due to a stricture in the distal ileum. Contrast-enhanced abdominal ultrasonography revealed a 7-cm stenotic site with increased intestinal wall thickening, which preserved mucosal blood perfusion. Elastography revealed a highly elastic alteration of the stenotic lesion, indicating benign fibrotic changes resulting from chronic insufficient blood flow. Based on a clinical diagnosis of IE with fibrous stenosis, a partial ileostomy was performed. After surgical treatment, oral intake was initiated without recurrence of intestinal obstruction. Pathological findings revealed deep ulceration with inflammatory cell infiltration at the stenotic site. Occlusion and hyalinization of the venules in the submucosal layer indicated IE. In addition to current case, we reviewed past case reports of IE. Through this case presentation and literature review, we summarize the usefulness and safety of transabdominal ultrasonography for diagnosing IE.

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Published by S. Kar ger AG, Ba sel
Case and Review
Case Rep Gastroenterol 2021;15:568–577
Diagnosis of Fibrotic Distal Ileum
Stenosis after Ischemic Enteritis Using
Transabdominal Ultrasonography
Ryo Katsumata a Noriaki Manabe a Masaki Matsubara b Jun Nakamura c
Kazuma Kawahito a Maki Ayaki a Minoru Fujita a Aya Sunago d
Hideyo Fujiwara e Yasumasa Monobe e Tomoari Kamada d
Hirofumi Kawamoto c Tomoki Yamatsuji b Yoshio Naomoto b
Ken Haruma c
aDepartment of Clinical Pathology and Laboratory Medicine, Kawasaki Medical School
General Medical Center, Okayama, Japan; bDepartment of General Surgery, Kawasaki
Medical School General Medical Center, Okayama, Japan; cDepartment of General
Internal Medicine 2, Kawasaki Medical School General Medical Center, Okayama, Japan;
dDepartment of Health Care Medicine, Kawasaki Medical School General Medical Center,
Okayama, Japan; eDepartment of Pathology, Kawasaki Medical School General Medical
Center, Okayama, Japan
Keywords
Ischemia · Enteritis · Renal dialysis · Ultrasonography
Abstract
Ischemic enteritis (IE) is a rare disorder which is caused by inadequate blood flow to small in-
testine. The diagnostic procedure of this disease has not sufficiently established because of
its rarity. Here, we report a case of IE in a hemodialysis-dependent 70-year-old man and sum-
marize the diagnostic options for IE. The patient was admitted to our hospital because of
acute abdominal distention and vomiting. He presented with mild tenderness in the lower
abdomen and slightly elevated C-reactive protein level as revealed by blood tests. Radio-
graphic imaging showed small bowel obstruction due to a stricture in the distal ileum. Con-
trast-enhanced abdominal ultrasonography revealed a 7-cm stenotic site with increased in-
testinal wall thickening, which preserved mucosal blood perfusion. Elastography revealed a
highly elastic alteration of the stenotic lesion, indicating benign fibrotic changes resulting
from chronic insufficient blood flow. Based on a clinical diagnosis of IE with fibrous stenosis,
a partial ileostomy was performed. After surgical treatment, oral intake was initiated without
recurrence of intestinal obstruction. Pathological findings revealed deep ulceration with in-
flammatory cell infiltration at the stenotic site. Occlusion and hyalinization of the venules in
the submucosal layer indicated IE. In addition to current case, we reviewed past case reports
Receive d: April 7, 2021
Accepted: April 16, 2021
Published online: June 23, 2021
Correspondence to:
Noriaki Manabe, n_manabe @ med.kawasaki-m.ac.jp
www.karger.com/crg
This article is licensed under the Creative Commons Attribution-NonCommercial 4.0 Interna tional License
(CC BY-NC) (http://www.karger.com/Services/OpenAccessLicense). Usage and distribution for commercial
purposes requires written permission.
DOI: 10.1159/000516852

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Katsumata et al.: Diagnosis of Fibrotic Distal Ileum Stenosis after Ischemic Enteritis
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© 2021 The Author(s). Published by S. Karger AG, Basel
DOI: 10.1159/000516852
of IE. Through this case presentation and literature review, we summarize the usefulness and
safety of transabdominal ultrasonography for diagnosing IE.
© 2021 The Author(s).
Published by S. Kar ger AG, Ba sel
Introduction
Ischemic enteritis (IE) is an acute or chronic condition that results from insufficient blood
perfusion in the small intestine. Known risk factors of IE include renal failure, arterioscle-
rosis, chronic heart failure, and diabetes mellitus [1, 2]. In contrast to ischemic colitis, which
results from inadequate blood flow in the large intestine, most IE patients progress to a severe
condition requiring operative intervention [1]. Due to the low prevalence of the disease and
difficulty in diagnosis, only a few case reports related to this disease have been published till
date. Several diagnostic methods, including angiography, balloon-assisted endoscopy, and
capsule endoscopy, have been suggested to diagnose IE [2–4].
At the early clinical stage, patients with IE show nonspecific abdominal symptoms, such
as mild tenderness and distention. In some cases, IE causes fibrous stenosis resulting in intes-
tinal obstruction [1, 3, 5]. Thus, differential diagnoses range widely from benign to malignant
[1]. Although several investigations can be performed to detect IE, there is no gold standard
for its diagnosis. Here, we report the first case of IE with fibrous stenosis in the ileum that was
diagnosed using transabdominal ultrasonography (TUS). Moreover, we reviewed previously
published case reports of IE. Regarding literature collection, we searched for case reports of
IE using the following terms on PubMed/MEDLINE (“ischemic enteritis” or “ischemic ileitis”)
AND (“case” or “case report”) by the end of February 2021. The inclusion criteria were case
reports with the clinical course from admission to treatment and full articles with abstracts
and reports written in English.
Case Report/Case Presentation
A 70-year-old man was referred to our institution because of abdominal distention
and vomiting that started 2 days prior to admission. The patient was undergoing hemo-
dialysis for chronic nephritis, and his past history included hypertension, chronic heart
failure, and arterial sclerosis. He was never a smoker and had no history of abdominal
surgery or nonsteroidal anti-inflammatory drug use. Upon hospitalization, the patient’s
blood pressure was 104/57 mm Hg, heart rate was 78 beats/min, and body temperature
was 36.5°C. Physical examination revealed mild tenderness and swelling in the lower
abdomen; the bowel sounds were enhanced. No purpura was found, which is character-
istic of Henoch-Schönlein purpura.
A blood test performed on admission revealed mild anemia (hemoglobin 11.2 g/dL),
hypoalbuminemia (2.6 g/dL), mildly elevated C-reactive protein (3.24 mg/dL), and elevated
serum creatinine (5.24 mg/dL) levels. The stool culture test results were negative. Tubercu-
losis and anisakiasis were ruled out by interferon-gamma releasing assays and anisakis
antibody tests, respectively.
Abdominal radiography in the standing position revealed dilatation of the small
intestine and air-fluid levels in the intestine (shown in Fig. 1a); plain computed tomog-
raphy (CT) showed a stenotic site with wall thickening and dilatation of the small intestine
on the oral side from the stenosis (shown in Fig. 1b, c). After admission, we inserted an

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DOI: 10.1159/000516852
Fig. 1. a Abdominal radiography reveals dilatation of the small intestine and presence of air-fluid levels in
the standing position. b, c Abdominal plain CT reveals intestinal wall thickening and a stricture at the distal
ileum (white arrows). Dilation of the small intestine detected on the oral side from the stenotic site. Coronal
image (a) axial image (b). d Small intestine series demonstrates a tubular stricture at the end of the ileum
(blue arrows). CT, computed tomography.
ab
cd
ileus tube to ameliorate the elevated intraluminal pressure. Contrast medium from the
tube showed a stricture at the end of the ileum (shown in Fig. 1d). We conducted TUS
using Sonazoid TM and elastography techniques, which demonstrated a thickened wall
and unclear stratification of the intestinal wall in the lower right abdomen (shown in
Fig. 2a, b). The length of stricture was 70 mm, and the minimum lumen diameter was 5 mm.
The small intestine on the oral side of the lesion was markedly dilated. Contrast-enhanced
ultrasonography showed sufficient mucosal blood flow in the stenotic lesion (Fig. 2c).
Ultrasound elastography revealed lower elasticity of the intestinal lesion site than the
elasticity of other intact parts of the small intestine that did not show wall thickening or
stenosis (strain ratio [local deformation ratio under slight pressure]: 2.52) (Fig. 2d).
Based on these findings, the patient was clinically diagnosed with IE. Conservative ther-
apies including fasting and total parenteral nutrition were initiated after the diagnosis;
however, the patient’s condition did not improve.
Surgery was performed, and the stenotic lesion was surgically resected. Macroscopic
findings of the resected ileum demonstrated circumferential ulceration and stricture.
Microscopic findings demonstrated penetration of the surrounding tissue and infiltration
of inflammatory cells mainly in the mucosal layer. The venules in the submucosal layer

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Fig. 2. a, b The B (brightness) mode of TUS illustrates longitudinal wall thickening and a circular stricture at
the distal ileum. c Contrast-enhanced ultrasonography demonstrates adequate mucosal blood flow in the
stenotic lesion. The length of stricture was 70 mm. d Ultrasound elastography reveals higher elasticity at the
stenosis site than the un-thickened small intestine. TUS, transabdominal ultrasonography.
ab
cd
were occluded by hyalinization (shown in Fig. 3a–d). Two days after the operation, the
patient started oral intake without the recurrence of IE and was discharged from our
hospital 1 month later. There was no relapse when the patient was last assessed 1 year
postoperatively.
Discussion/Conclusion
To the best of our knowledge, this is the first English case report of IE delineated by TUS. Since
the prevalence of IE is quite low and it is difficult to diagnose, only a limited number of case reports
concerning this condition have been published in English so far [1–7]. A summary of the clinical
backgrounds, relevant diagnostic methods, treatment, and outcomes from previous case reports
is presented in Table 1. Our patient was an elderly man, as is typical for IE, and his symptoms and
clinical course were largely consistent with those of the previous reports.
IE is thought to share risk factors with other ischemic diseases, such as myocardial
infarction and stroke [2]. Among the well-known risk factors for ischemic disease, the patient
displayed hypertension and hemodialysis. Hemodialysis is a risk factor for ischemic condi-
tions in the gastrointestinal tract, including the small intestine [8]. Repeated hypotensive
episodes during hemodialysis elevate the risk of ischemia of the mesenteric artery [9].
Additionally, the prevalence of peripheral arterial disease (a relevant risk factor of IE) among
hemodialysis patients is reportedly higher than that in the general population and is 24%
among hemodialysis patients and 4.3% in the general population [10]. For patients aged >60

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years, hemodialysis and hypertension were found to be associated with the onset of ischemic
colitis [11]; hemodialysis in particular was associated with high mortality rates [12]. Based
on this information, although only a few case reports of IE with hemodialysis have been
published, patients undergoing hemodialysis (as in our case) are considered to have a high
risk for onset and exacerbation of IE.
Diagnosing IE is challenging; several investigations have been performed to delineate
the lesions, as found in our literature review. Enhanced-CT imaging is a useful option for
estimating abdominal disorders because of its ability to detect bowel dilatation, thickened
intestinal wall, and intestinal blood flow. Strictures with intestinal wall thickness in the
ileum are suggested to be typical findings of IE. The average length of the stricture was
7.4 cm, which is longer than that in other causes of intestinal obstruction, such as adeno-
carcinoma and Crohn’s disease [13]. Enhanced CT could not be performed in the current
case due to severe renal failure; however, plain CT findings and contrast medium from an
ileus tube revealed a typical longitudinal stricture for IE. Angiography is also an effective
examination method for assessing altered vascular conditions. Because of renal failure,
we also avoided angiography that enables us to describe blood vessel structures [2].
Endoscopic examination, including single or double balloon-assisted endoscopy [1, 3, 5]
and capsule endoscopy [4], provides information on the mucosal surface and luminal
condition and allows physicians to obtain specimens from the intestinal mucosa [5].
Although endoscopy is a considerably effective examination to estimate the cause of
small bowel obstruction, we did not perform endoscopy because of the patient’s under-
lying severe systemic conditions.
Fig. 3. a Macroscopic findings of the resected specimen demonstrate circumferential ulceration with steno-
sis. b Microscopic findings reveal a UI-IV ulcer with penetration to the peripheral lipid tissue. c Loss of crypt
and inflammatory cell infiltrate. d Dilatation and congestion of submucosal venules (b–d: H&E staining, c, d:
×40) UI, ulcer index; H&E, hematoxylin and eosin.
ab
cd

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Table 1. Summary of previous case reports and the characteristics of each patient with IE
Author, year Age Sex Country Symptoms Relevant diagnostic method Treatment Outcome
Delikoukos et al. [6],
2006
62 M Greece Abdominal pain, diarrhea,
and intestinal bleeding
CT Surgical resection Recurrence after 3 days
Yu et al. [2], 2010 81 F Korea Dyspnea Angiography and enhanced-CT Surgical resection Died 7 days after the
operation
Hotokezaka et al. [7],
2012
67 M Japan Symptoms of an
enterocutaneous fistula
Intestinal series Surgical resection Only a minor leakage
Jeong et al. [4], 2013 21 M Korea Upper abdominal pain Capsule endoscopy Steroid and warfarin No recurrence
Takeuchi et al. [3],
2013
69 M Japan Vomiting and abdominal
distention
Capsule endoscopy and
single-balloon endoscopy
Surgical resection No recurrence
Koshikawa et al. [1],
2016
75 M Japan Vomiting and abdominal
distention
Double-balloon endoscopy Surgical resection Uneventful
Iwai et al. [5], 2016 69 M Japan Abdominal pain Double-balloon endoscopy Surgical resection –
Our case (2021) 76 M Japan Vomiting and abdominal
distention
TUS Surgical resection No recurrence
CT, computed tomography; M, male; F, female; –, data not described; IE, ischemic enteritis; TUS, transabdominal ultrasonography.

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Table 2. Diagnostic methods for IE and the capabilities to evaluate findings
Examinations Evaluation of bowel
dilatation
Evaluation of intestinal
wall thickness
Evaluation of
blood flow
Evaluation of
vascularization
Evaluation of
mucosa
Biopsy and balloon
dilatation therapy
Evaluation of
elasticity
Abdominal radiography Possible – – – – – –
CT Possible Possible Possible – – – –
Intestinal series Possible – – – – – –
Endoscopy
Scope(including
balloon assisted)
Possible Possible – Possible Possible Possible –
Capsule Possible Possible – Possible Possible – –
Angiography – – Possible – – – –
TUS Possible Possible Possible – – – Possible
–, not possible; IE, ischemic enteritis; TUS, transabdominal ultrasonography, CT, computed tomography.

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To delineate the stenotic site noninvasively, we carried out TUS and elastography tech-
niques. TUS has been reported to be an effective option for diagnosing small intestinal
disorders [14]. In our case, a 7-cm stenotic site with a thickened small intestinal wall at the
end of the ileum was observed using TUS. The lesion was nonsegmental and did not show
hypervascularization. The findings were neither consistent with a tumor, which exhibits
short localized thickening of the wall without stratification, nor with inflammatory bowel
disease, which demonstrates segmental wall thickening with focal disappearance of its strat-
ification [15]. Moreover, using contrast-enhanced ultrasonography imaging, we were able to
rule out complete intestinal ischemia. Comprehensive evaluation of the contrast-enhanced
and noncontrast-enhanced ultrasonographic findings made it possible to rule out small intes-
tinal carcinoma, which is known to demonstrate enhanced blood perfusion and hypervascu-
larization [16]. Elastography is an emerging evaluation method for elasticity and utilizes a
sonographic technique by which the relative elasticity of the lesion site can be assessed
compared to the elasticity of the other tissues [17]. While this method has primarily been
adopted to evaluate mammary neoplasms and fibrotic alterations of liver tissue, it has also
been reported to be a useful option to assess gastrointestinal disorders such as Crohn’s
disease and colorectal cancer [18]. In this case, the stenotic lesion was detected to be more
elastic than the normal small intestine by using strain ratio, which displayed the ratio of elas-
ticity on the lesion to normal intestine. Further, the strain ratio was much lower than that of
adenocarcinoma [19]. Based on the findings, we clinically diagnosed our patient with fibrous
stenosis resulting from IE. The sonographic findings and diagnoses were consistent with the
pathological diagnosis in this case.
Combining past case reports published in English, we summarized the diagnostic methods
for IE with their potential targets (Table 2). Various diagnostic options were used depending
on the patient’s general condition, access to equipment, and technical issues. Compared to
other examinations, TUS can be used to assess a broader range of information, including
tissue elasticity, without any radiation exposure. Furthermore, real-time assessment can be
performed noninvasively using TUS, and its cost-effective and noninvasive features allow for
the examination to be performed repeatedly.
Although conservative treatment and balloon dilatation can partially alleviate symptoms
[5], surgical resection is needed in most IE cases, especially in those with fibrous stenosis [1].
This clinical course is not consistent with that of ischemic colitis, for which surgical options
are rarely performed [20]. We also resected the stenotic lesion in our case based on the known
clinical course of IE. An additional advantage of surgical resection in addition to symptom
improvement is that the entire intestinal layer can be pathologically evaluated. The histo-
logical characteristics of IE include the following findings [3]: variable ulcer depth with mostly
UI (ulcer index)-II or UI-III ulceration, ulcer bases lined with vascular-rich granulation tissue;
severe fibrosis within the submucosal layers, severe inflammatory cell infiltration, and hemo-
siderin-laden macrophages spread throughout the thickened intestinal wall. In our case, the
histological findings largely matched the typical features of IE.
In conclusion, fibrotic stenosis with IE is a critical differential diagnosis of small bowel
obstruction. Older subjects with cardiovascular complications and severe general conditions
have a high risk of developing IE. TUS can be a harmless and highly beneficial diagnostic method
for IE, especially in patients with unstable systemic conditions, including severe renal failure.
Acknowledgements
We would like to express our gratitude to the patient and to Editage (www.editage.com)
for English language editing.

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Statement of Ethics
We reported this case in compliance with the principles of the Declaration of Helsinki.
This case was reviewed and approved by the institutional Ethics Committee of Kawasaki
Medical School. Approval number was 2020-1528. Written informed consent was obtained
from the patient for publication of this case report and any accompanying images.
Conflict of Interest Statement
The authors have no conflicts of interest to declare.
Funding Sources
The authors disclose no sponsorship or funding arrangements relating to their research.
Author Contributions
Conceptualization: N.M., K.H. Data curation: R.K., N.M., A.S., J.N., K.K., M.M., H.F., Y.M.
Formal analysis: R.K. Investigation: R.K., N.M., M.A. Methodology: N.M. Project administration:
R.K., N.M. Resources: R.K., N.M., J.N., K.K., M.M., H.F., Y.M., T.K., T.Y., Y.N. Software: R.K. Super-
vision: N.M., H.K., K.H. Validation: N.M. Visualization: R.K., N.M. Writing – original draft: R.K.
Writing – review and editing: N.M., H.K. Approval of final manuscript: all the authors.
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