Strangulating Closed-Loop Obstruction: Sonographic Signs

Abstract

Purpose: To evaluate different sonographic signs of strangulating closed-loop obstruction retrospectively.

Materials and Methods: Over a period of approximately 10 years all documents, US scans and video clips of patients with strangulating intestinal obstruction were reviewed. The following sonographic signs were evaluated: akinetic bowel loops; echo-free luminal content; hyperechoic congestion of the mesentery; free peritoneal fluid; bowel wall thickening; signs of ischemia on color Doppler or contrast-enhanced US. Moreover, we looked for signs of bowel obstruction proximal to the closed loop and for the width of the strangulated segment.

Results: The most often documented features of strangulating closed-loop obstruction were an akinetic bowel loop (94 %), a hyperechoic and thickened mesentery (82 %) and free peritoneal fluid (100 %). In 54 % of cases the luminal content was almost anechoic. In 76 % of patients bowel wall thickening and in 50 % signs of ischemia on color Doppler or contrast-enhanced US were documented. In 67 % small bowel dilatation proximal to the strangulated bowel segment was present. The width of the strangulated bowel loops was 2.86 cm on average.

Conclusion: The akinetic bowel loops, hyperechoic thickening of the attached mesentery and free peritoneal fluid are typical for strangulating closed-loop obstruction. An anechoic luminal content is only visible in about half of the patients, but this eye-catcher can lead the investigator to the correct diagnosis. In about one third of patients no signs of bowel obstruction proximal to the strangulated loops are present. Dilatation of the strangulated loop may be absent or mild.

Zusammenfassung

Ziel: Retrospektive Auswertung aus der Literatur bekannter und von uns beobachteter sonographischer Zeichen der segmentalen Dünndarmstrangulation.

Material und Methoden: Aus einem Zeitraum von etwa 10 Jahren wurden Befunde, Bild- und Videodokumentationen von 29 Patienten mit operativ bestätigter segmentaler Dünndarmstrangulation durchgesehen. Folgende sonografische Zeichen wurden überprüft: aperistaltische Schlinge; weitgehend echofreies Lumen; echoreich alteriertes Mesenterium; Aszites; Darmwandverdickung; Ischämiezeichen im Farbdoppler oder Kontrastmittelultraschall. Weiter wurde erhoben, wie weit die strangulierten Schlingen waren und ob vor dem strangulierten Segment Zeichen eines mechanischen Dünndarmileus bestanden.

Ergebnisse: Die aperistaltische Darmschlinge (94 %), das echoreich alterierte Mesenterium (82 %) und freie Flüssigkeit (100 %) waren am häufigsten dokumentiert. Bei 54 % dieser Fälle war das Lumen der betroffenen Dünndarmschlingen weitgehend echofrei. In 76 % der Patienten war eine Darmwandverdickung beschrieben, in 50 % auch Ischämiezeichen im Farbdoppler oder Kontrastmittelultraschall erwähnt. In 67 % bestanden vor dem strangulierten Segment Zeichen eines mechanischen Dünndarmileus. Die Lumenweite der strangulierten Schlingen betrug durchschnittlich 2,86 cm.

Schlussfolgerung: Die aperistaltische Darmschlinge mit dem echoreich alterierten dazugehörigen Mesenterium bei gleichzeitig vorhandener freier Flüssigkeit sind typisch für die segmentale Dünndarmstrangulation. Die weitgehende Echofreiheit des Inhalts betroffener Schlingen ist nur in etwas mehr als der Hälfte zu beobachten, aber ein sehr markantes Zeichen, welches den Untersucher in die richtige Richtung führen kann. In etwa einem Drittel der Fälle mit Dünndarmstrangulation bestehen vorgeschaltet noch keine Ileuszeichen und die strangulierten Darmschlingen sind durchschnittlich nicht sehr stark dilatiert.

Key words

abdomen - small bowel - ultrasound - ischemia/infarction - strangulation

Introduction

The indication for surgery in case of bowel obstruction is based on clinical presentation, radiological findings and laboratory results [1]. Nowadays, ultrasound (US) and computed tomography (CT) are the most important imaging methods used for the evaluation of bowel obstruction and possible complications. One of the most important complications for a patient with bowel obstruction is the strangulation of a small intestine loop. If findings indicate that kind of complication, an immediate operation must be performed in order to save the ischemic intestinal segment or to remove already necrotic sections.

There are two main etiological mechanisms that can lead to segmental strangulation of the small intestine: on the one hand one or more intestinal loops can migrate under an adhesive band and consecutively their circulation may be compromised, and on the other hand a bowel loop may be twisted around an adhesive band so that its vessels are obstructed [2].

There are only few publications on the sonographic criteria of segmental strangulation of the small intestine. The following criteria are known from the literature: isolated conglomerate of dilated small bowel loops; U-shaped, distended loop; thickening of the intestinal wall; akinetic, distended loops; free peritoneal fluid; intraluminal fluid-fluid levels; increase in the resistance index of the superior mesenteric artery [3] [4] [5] [6].

A lot more publications refer to CT criteria. The following criteria have been published: isolated conglomerate of fluid-filled and dilated small bowel loops; C- or U-shaped loops; whirl sign; beak sign; mesenteric congestion and vascular engorgement; radial converging mesenteric vessels; intestinal wall thickening; high attenuation of the bowel wall; target sign; decreased contrast enhancement; local pneumatosis; free peritoneal fluid [2] [7] [8] [9] [10].

On different occasions we have observed that strangulated and akinetic intestinal loops show a dilated and almost echo-free lumen on US scans. In addition, congestion of the attached mesentery, which is a well-known CT sign, was visible as a hyperechoic and thickened mesentery.

The goal of this retrospective study was to investigate these two phenomena further and to gather information on the frequency of all the different sonographic signs in patients suffering from small bowel strangulation.

Materials and methods

An internal case archive (figures and video clips) was searched for cases of strangulating closed-loop obstruction which were gathered over the last ten years. In addition, the surgery reports from the last three years concerning the diagnosis of small bowel obstruction were reviewed for cases that showed signs of small intestine ischemia during surgery. Especially cases of strangulating closed-loop obstruction previous to this three-year period might not have been captured completely by this study.

Cases of small bowel ischemia without signs of adhesive bands or small bowel volvulus were excluded. Also cases with large bowel volvulus (cecal or sigmoid volvulus) and incarcerated external hernias or cases of complete mesenteric volvulus were not included in the trial. Two patients with known history of multiple abdominal surgeries were excluded due to conservative treatment despite suspected vascular impairment. One case with surgical findings of a strangulation mark indicating that the obstruction had resolved itself was not included in the trial. Another case of an oncological patient who presented without pain and had free peritoneal fluid in her ultrasound examination was excluded. In the following CT examination a contained perforation of a strangulated small intestinal loop was suspected and was confirmed during surgery. Additional cases going back more than 10 years could not be included in the trial due to insufficient documentation. 31 cases of strangulating closed-loop obstruction due to adhesive bands remained.

An isolated U- or Ω-shaped loop or a conglomerate of akinetic loops was judged as a typical B-mode US finding of a segmental strangulation. Two patients had loops with ischemic changes that were longer than 100 cm and could not be recognized as a segmental strangulation on US and CT.

Therefore, 29 cases of strangulating closed-loop obstruction were included in the trial. The study group consisted of 20 female and 9 male patients, mean age 67.8 years (17 – 93 years). All patients had an US examination and in addition 14 had a CT scan prior to surgery. The following US signs were retrospectively analyzed:

• lack of peristalsis: a single loop or a conglomerate of small bowel loops that showed no peristaltic activity during examination.

• dilated and echo-free fluid-filled loop(s): almost echo-free, dilated loops without whirling movement of bowel contents or intraluminal gas bubbles. Slight echoes or sediment can be present.

• hyperechoic mesenteric congestion: hyperechoic thickening of the involved bowel mesentery which is hardly compressible in comparison to the mesentery of neighboring non-involved loops.

• free peritoneal fluid: findings like locally trapped or free peritoneal fluid and larger amounts of peritoneal fluid than usually visible in cases of simple bowel obstruction.

• bowel wall thickening: wall thickening of more than 2 mm in dilated bowel loops or more than 4 mm in contracted loops was rated as a pathological finding.

• signs of ischemia: findings of reduced or missing perfusion on color Doppler US or delayed contrast on contrast-enhanced US are signs of ischemia. Lack of perfusion on contrast-enhanced US or the findings of pneumatosis in a thickened bowel segment without perfusion indicate irreversible bowel damage.

Signs of bowel obstruction proximal to the incarcerated loops and the diameter of the strangulated loops were also evaluated. Usually a diameter of 3 cm is used as a threshold value for small bowel dilatation. Documented bowel diameters of 2.7 to 3 cm in proximal loops in some cases in this study were estimated to be early signs of bowel obstruction. Therefore, a diameter of 2.7 cm was determined as the threshold value in this study.

Results

The data of each patient is summarized in [Table 1]. The US signs and the most important CT signs, if available, are compared in this table. The number of patients for the analysis of the different signs varies a bit because of the incomplete documentation in some cases in this retrospective study. Subsequently the results of the different sonographic signs are listed.

Table 1 Summary of different imaging findings.

patient number	akinetic loop	echo-free	mesenteric congestion	free fluid	ischemia/ infarction	bowel resection	wall thickening	local width	proximal dilatation
1	yes	yes	US	US	US	yes	US	3.2	yes
2	yes	yes	US	US	US+CEUS	yes	US	2.5	no
3	yes	yes	US+CT	US+CT	US+CEUS	yes	-	3.0	no
4	yes	---	US	US	-	-	-	2.7	no
5	?	---	US+CT	US+CT	US+CEUS	-	US	3.2	yes
6	yes	yes	US+CT	US+CT	-	-	-	3.5	no
7	?	---	CT	US+CT	-	-	US+CT	2.8	yes
8	?	---	US+CT	US+CT	US+CT	-	US+CT	2.0	no
9	yes	---	US	US	US	yes	US	2.5	yes
10	?	?	CT	US+CT	-	-	-	3.0	yes
11	yes	yes	US	US	?	-	-	3.0	yes
12	yes	yes	---	US	-	-	US	2.5	no
13	?	---	US+CT	US+CT	-	yes	US+CT	2.6	yes
14	?	---	US+CT	US+CT	?	-	US+CT	2.0	yes
15	?	---	US	US	US	yes	US+CT	2.6	yes
16	?	---	US	US	US	yes	US	2.3	no
17	yes	yes	US	US	?	-	US	3.8	no
18	yes	yes	US	US	US	yes	US	3.0	yes
19	yes	?	CT	US+CT	CT	yes	US+CT	3.0	yes
20	?	?	?	US	?	-	US	?	yes
21	yes	yes	US+CT	US+CT	CT	-	US+CT	3.3	no
22	yes	yes	US	US	-	-	US	3.0	yes
23	?	yes	US	US	US	-	US	2.5	yes
24	yes	yes	US	US+CT	-	-	-	2.8	yes
25	yes	---	US+CT	US+CT	CT	yes	US+CT	2.7	yes
26	yes	---	US +CT	US+CT	US+CT	yes	US	3.3	yes
27	yes	---	US	US	US	-	US	3.0	?
28	yes	yes	US	US	?	-	US	3.8	?
29	---	yes	---	US	-	-	-	2.5	yes

Gray background color in cases with both US and CT examination.

“?”: the criterion could not be assessed in the imaging report and on documented figures.

Cases with a large amount of free peritoneal fluid are highlighted in bold type.

• Lack of peristalsis in strangulated loops was documented in 17 of 18 cases (94 %). In one case reduced peristalsis was observed. Adjacent bowel loops proximal to the obstruction usually showed hyperperistalsis.

• Affected loop(s) showed an almost echo-free lumen in 14/26 cases (54 %) ([Fig. 1], [2], [3]). To-and-fro movement of spot echoes due to ingested particles and gas bubbles was always found if proximal, dilated bowel loops were present (

  ).

• Hyperechoic mesenteric congestion was found in a high percentage (23/28 = 84 %) ([Fig. 1], [2], [3]). In 3 cases mesenteric thickening with vascular engorgement could only be detected by CT. The remaining 2 negative US cases (CT was not performed) showed strangulation of a very short bowel segment without any significant mesenteric involvement ([Fig. 5]).

• Free peritoneal fluid was always present (29/29). In 10 patients we noticed a large amount of free fluid.

• Bowel wall thickening was recorded in 22/29 cases (76 %) ([Fig. 4]). Thirteen times wall thickening was present in dilated loops (> 2.7 cm).

• Ischemia was documented in 15/24 cases, including 3 cases with documentation only on CT scans. Signs of ischemia on color Doppler or contrast-enhanced US were present in 50 % of cases (12/24) ([Fig. 2]). On the one hand the ischemic bowel loop could be preserved during surgery in five cases. On the other hand an intestinal resection had to be done in one case without documentation of ischemia by means of US.

Fig. 1 This C-shaped strangulated small-bowel loop shows echo-free luminal content except for some sedimentation. Hyperechoic and voluminous mesenteric fat is visible in the center.

Fig. 2 This cross section of the small bowel shows some dilated and almost echo-free loops a. Adjacent thereto, some ascites is demonstrated (x). Again thickened and hyperechoic mesentery is visible. The mesentery is converging towards the point of obstruction (arrows). Contrast-enhanced US b shows reduced vascularization of the strangulated loops in comparison to an adjacent small-bowel loop (arrow).

Fig. 3 Cross section a and longitudinal section b of dilated and almost echo-free small-bowel loops. In the cross section we can clearly see the edematous and hyperechoic mesentery and minimal free peritoneal fluid. A CT scan of the same patient c shows the dilated small-bowel loops with the thickened, attached mesentery (arrows).

Fig. 4 The small–bowel loops in a are not dilated, but their wall is thickened (arrow) as a consequence of strangulation due to adhesive bands. Proximal to these strangulated loops signs of small-bowel obstruction were visible with bright luminal echoes caused by ingested food and gas bubbles b. The CT scan c also shows the strangulated bowel loops with the thickened mesentery (arrows) and the dilated loops proximal to this strangulated segment (thin arrows).

Fig. 5 Solitary, short and strangulated small-bowel loop without demonstration of a thickened mesentery. On color Doppler ultrasound vascularization was still visible. Proximal to this loop no signs of small-bowel obstruction were present.

In 18/27 cases (67 %) dilation of the loops proximal to the akinetic loop was present as a sign of mechanical intestinal obstruction ([Fig. 4],

). The maximum diameter of the strangulated loops ranged from 2 to 3.8 cm (mean 2.86 cm).

11 of 29 patients had small bowel resection.

2 patients (90 and 93 years old) died after surgery during hospital care.

Discussion

The significance of sonography for the diagnosis of mechanical small bowel obstruction is unquestionable and well documented [13] [14] [15] [16] [17]. Especially concerning impending complications, US and CT have replaced plain abdominal radiographs [4] [10] [11] [12]. Yet, concerning one of the most important complications of small bowel obstruction – the segmental strangulation – US-based articles are sparse. The reported typical sonographic findings of strangulation should be completed with this study.

In comparison to other imaging methods, US has the advantage of real-time assessment of peristalsis. A single loop or a conglomerate of akinetic loops is the most important sign of segmental bowel strangulation and impending ischemic damage, especially when neighboring loops show regular or increased peristaltic activity.

The sign of the dilated echo-free loop has not been reported so far in this form. A possible similar observation has been noted by Cozza et al. describing intraluminal fluid-fluid levels due to sedimentation [6]. In our retrospective study we could find sedimentations only in a relatively small number of cases. Even though the echo-free lumen sign was only found in a little more than half of the cases, it is an eye-catcher and can be a hint for guiding the examiner towards the right diagnosis. Two relevant factors can be noted as a possible cause of the echo-free loop. On the one hand ingested particles and gas bubbles cannot be transported from proximal loops into the closed loop due to the obstruction [19]. On the other hand vascular impairment causes paralysis and sedimentation of intraluminal particles so that most of the luminal fluid appears almost echo-free. In addition, gas bubbles swirled up by permanent peristaltic movement are no longer visible in the luminal fluid of paralytic segments.

The assumption that a lack of peristalsis is an important factor for the genesis of the echo-free loop sign is supported by its appearance in other cases of bowel paralysis.

The echo-free loop sign is not specific for segmental bowel strangulation. Its appearance in conjunction with acute clinical signs should guide the examiner to search for other signs of strangulation.

In the case of strangulation thickened mesenteric leafs are mostly present but often not perceived during US examination because the dilation of loops is the center of attention. Similar to diverticulitis or appendicitis, hyperechoic surrounding fatty tissue is an important sign. As a consequence of venous congestion and edema, the mesenteric fat presents thickened and hyperechoic and is well visible by US. In only 2 cases of our study this sign could not be found due to very short affected loops.

On CT scans edematous mesenteric tissue with venous congestion is the most important and reliable sign. CT might be superior to US in detection mostly because it can demonstrate the mesentery free of overlying structures. In 3 cases strangulation was detected only by CT.

Free peritoneal fluid is present in almost all cases of small bowel obstruction, even in uncomplicated cases. Findings of larger amounts of free fluid in context with small bowel obstruction should always raise suspicion of strangulation. Sometimes trapped fluid can be found adjacent to the strangulated bowel loops. As for the rest, free peritoneal fluid is nonspecific.

A thickened bowel wall does not necessarily mean irreversible ischemic damage. As a result of strangulation, the bowel wall develops venous congestion and tissue edema. Subsequently, increasing ischemic damage causes wall hemorrhage and intestinal necrosis. So it is hardly surprising that wall thickening is described more often than signs of ischemia. Depending on the duration and extent of strangulation, bowel wall thickening is more or less distinct.

Concerning bowel wall ischemia, color Doppler and contrast-enhanced US can provide additional information. Missing perfusion on color Doppler US can raise suspicion of bowel necrosis whereas on contrast-enhanced US it can prove bowel necrosis [18]. On the other hand, evident bowel perfusion can derive from remaining arterial blood flow in the bowel, while venous congestion has already resulted in bowel infarction. In addition, the situation can rapidly deteriorate. An increased resistance index in pulsed Doppler US of the superior mesenteric artery as described by Okada et al. probably only occurs if longer bowel segments are affected [5]. The decision regarding the resection of ischemic small bowel segments can only be made during surgery except for those cases with typical signs of infarction. The sooner surgery is performed, the higher the probability of saving the small bowel tissue.

An Ω- or U-shaped loop or a conglomerate of dilated loops indicates closed-loop obstruction [3]. Depending on the duration, dilation of the proximal loops can be missing. In our study we found this in one third of cases. Therefore, there can be only segmental intestinal dilation or the typical presentation of small bowel obstruction also with dilation of bowel loops proximal to the obstruction.

The relatively low mean diameter of 2.86 cm of the strangulated loops is also remarkable. A possible explanation could be that kinking around adhesive bands mainly leads to vascular congestion with alteration of mesenteric fatty tissue, while the obstruction with dilatation of the lumen is less predominant. Therefore, the affected bowel wall thickens but the luminal diameter does not increase. Moreover, due to the obstruction, bowel content from oral loops cannot add to the volume of the affected loop. Marked dilation of the affected loop can only happen when the loop is trapped under an adhesive band or through an internal hernia and when strangulation occurs only with increasing dilatation.

There are some limitations to this study. This is a retrospective analysis which might not contain all cases that happened in the period of ten years. The inspection of the surgery reports turned out to be laborious and so it was limited to the last 3 years. No definitive statement can be made concerning the accuracy of US in the case of small bowel strangulation. At least one false-negative case was excluded (see materials and methods) due to missing documentation of typical US signs following confusing clinical presentation. In addition, not all US signs evaluated in this study were documented in some of the cases.

Conclusion

The combination of increased peristaltic activity proximal to the obstruction and a single loop or a conglomerate of loops without peristalsis is highly suspicious of strangulating small bowel obstruction.

The almost echo-free lumen of an akinetic loop is an eye-catcher and should be considered as an important sign of segmental strangulation, but at the same time it is not specific.

Hyperechoic thickening of the mesenteric fat can support the suspicion of strangulation, especially in conjunction with local trapped fluid or noticeable free peritoneal fluid.

Intestinal wall thickening, reduced perfusion on color Doppler or contrast-enhanced US or the occurrence of intramural gas are signs of impending ischemic damage or infarction.

Absence of US findings of strangulation does not rule out this relevant complication.

Depending on the mechanism of strangulation, the dilation of the bowel lumen or the venous congestion of the bowel wall and its mesentery can be in the foreground.

Dilatation of small bowel loops proximal to the strangulated segment is not necessarily present. The duration from onset of symptoms to diagnosis and surgery is crucial for the development of proximal dilatation.

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