Continuing Education Activity

Intestinal or bowel ultrasound is a non-invasive examination method of the gastrointestinal tract. It is a complementary examination of the more common abdominal ultrasound for providers who use ultrasound as part of their practice. Ultrasound does not involve radiation and is, therefore, safe for pregnant women and children and for patients that require repeated radiological examination. Operator technique and time allocation serve as potential limitations to this exam. This activity highlights the role of the interprofessional team in incorporating intestinal ultrasound in clinical practice and reviews its technique, equipment used, and limitations.

Objectives:

• Describe the importance of intestinal ultrasound in clinical practice and the techniques used in screening by ultrasound.
• Summarize the anatomical landmarks of intestinal ultrasound.
• Review the different indications for intestinal ultrasound and the pathologies potentially seen on imaging.
• Describe the potential role of ultrasound in evaluating infectious and inflammatory bowel disease.

Introduction

Intestinal or bowel ultrasound is a non-invasive sonographic exam of the gastrointestinal tract. It acts as a complementary examination to the standard abdominal ultrasound exam and offers clinical data that could be beneficial in patients unable to obtain CT or MRI examinations for various reasons.[1] Intestinal ultrasound also provides the option of being portable to those patients who are immobile.[2]

As a hollow organ, the gastrointestinal system contains air and fluid. While fluid is considered a good acoustic medium, the air is a poor acoustic medium that typically impairs ultrasound imaging. Thus patient preparation often improves the diagnostic quality of ultrasound evaluation of the small and large bowel. Bowel ultrasound can be used in the detection, diagnosis, and follow-up of various gastrointestinal illnesses. Ultrasound does not involve radiation and is, therefore, safe for pregnant women and children and for patients that require repeated radiological examination. Operator technique and time allocation serve as potential limitations to this exam.[3][4]

Anatomy and Physiology

Normal bowel anatomy as determined by ultrasound differs from other radiological techniques and its histological appearance under light microscopy. Multiple diagnostic scoring systems are present to detect gastrointestinal diseases.[5]

• Normal bowel wall appearance and thickness: Normal bowel wall consists of five layers, each differing in echogenicity, allowing some degree of discerning these layers from each other. Normal bowel diameter depends on the segment of the intestine interrogated. Bowel wall thickness is the most important feature in intestinal ultrasound assessment and an important parameter used in detecting intestinal disease. Thickness is determined by measuring all of the wall strata from the lumen interface to the serosa. Typically wall thickness between 3 to 4 mm is considered normal, except for the gastric wall, which could range up to 5 or 6 mm.[6]
• Normal bowel diameter: Pathology of the small and large bowel can manifest as an obstructive or paralytic process causing dilatation of the bowels. As such, bowel loop diameter can help in assessing for pathology. As a rule of thumb, the small intestine diameter may not exceed 2.5 to 3 cm. Similarly, the large intestine typically does not exceed 5 cm in diameter.[7]

• Echo pattern: Although the arrangement of wall layers does not correlate with histological layers exactly, this stratification is still important in identifying diseases by detecting loss of stratification.
  1. The lumen of the gut interface: hyperechoic
  2. The mucosa: hypoechoic
  3. The submucosa: hyperechoic
  4. The muscularis propria: hypoechoic
  5. The serosa: hyperechoic

• Vascularity: Determining abnormal vascularity, such as hyperemia or neovascularization, is important in diagnosing different intestinal diseases such as edema, inflammation, or malignancy. This is usually assessed by color doppler accompanying the usual greyscale evaluation on ultrasound examination.[8] Another critical parameter in sonographic bowel evaluation is assessing the appearance of large vessels supplying the gastrointestinal system, including the superior mesenteric artery, inferior mesenteric artery, and celiac trunk. Evaluating the superior and inferior mesenteric veins and portal and splenic veins can also provide important diagnostic information.
• Motility: Motility represents a subjective measure of assessing bowel health and is operator-dependent. Peristalsis is limited in cases of inflammation of the bowel or fibrous strictures. Increased peristalsis is present in diarrhea, celiac disease, and intestinal obstruction, among other causes.[9]
• Compressibility: Non-compressible bowel could indicate an inflammatory or malignant change in the bowel wall as infiltrative neoplasms result in the loss of the normal pliability of the bowel wall.[10]

Other important signs that could be found on intestinal ultrasound and be an indication of the underlying disease:

• Mesenteric fat: Mainly assessed from the epigastrium to the right iliac fossa. Increased thickness >6mm is associated with an abnormality, such as an inflammatory process like diverticulitis.
• Extraluminal gas: This usually indicates luminal perforation at the site of pathology.

Different Scoring Systems In Intestinal Ultrasound

The use of regular ultrasound or bubble contrast (contrast-enhanced ultrasound CEUS) is a common medical practice in Europe and North America.[11] Different scoring systems have been evaluated, but no universal scoring system has been proven effective to date. Most of the scoring systems include various parameters to include bowel wall thickness, wall stratification, detection of fistula formation, ascites, mesenteric fat, lymph nodes, compressibility, peristalsis, and inflammatory signs in the bowel wall with color doppler.[2][12]

A simple ultrasound score that can be used for Crohn disease monitoring was validated through clinical studies. The authors claimed that it could be used in follow-up in lieu of endoscopy for Crohn disease patients.[13]

The Difference in Wall Thickness in Children with Crohn Disease

The normal bowel thickness in children is typically less than 2 mm, similar to that of adults. Intestinal ultrasound is helpful in the detection and follow-up of Crohn disease in children.[14]

Indications

Intestinal ultrasound is a non-invasive procedure that could be ancillary to the more frequently performed abdominal ultrasound. Some clinicians can use it as the initial examination of choice depending on operator comfort using an ultrasound machine and image interpretation.[15][16][17]

Intestinal Ultrasound Could Assist in Evaluating the Following Pathologies

Acute Abdomen

1. Acute appendicitis: Different compression techniques are used to assess for acute appendicitis. The diagnostic signs on ultrasound are a noncompressible, enlarged blind-ending tubular structure representing an inflamed appendix in the right iliac fossa.[18] 
2. Acute diverticulitis: Ultrasound can demonstrate bowel wall thickening, diverticulosis, and foci of varying echogenicity, along with hyperechoic pericolic inflammatory fat.[19] Perforation can manifest as foci of dirty shadowing representing gas.
3. Ischemic colitis: An increase in the colon wall diameter >5 mm (typically involving the left colon), with loss of bowel wall stratification can be seen. Absent or markedly increased vascular flow on color doppler can also be demonstrated.[20] 
4. Intestinal obstruction: Intestinal ultrasound is not the most conclusive method for diagnosing intestinal obstruction due to the gaseous distension associated with obstruction. However, if small bowel loops are distended with fluid, this can be assessed on sonography to some degree. Rarely the underlying cause of obstruction(such as in the setting of a large mass a) can be visualized. The small bowel diameter is typically greater than 2.5 cm in the setting of obstruction, while the length of the obstructed segment typically needs to be greater than 10 cm, with affected bowel loops typically distended with fluid or debris.[21] 
5. Enlargement of mesenteric lymph nodes: While paraaortic lymph nodes are typically too deep for adequate visualization, mesenteric lymph nodes can often be seen.[22] This can include enlarged mesenteric lymph nodes adjacent to a thickened ileum in the setting of Crohn disease-related inflammation or generalized adenopathy as in sclerosing mesenteritis.

Chronic Diseases or Non-urgent Conditions

1. Crohn disease: Ultrasound has a limited role in evaluating Crohn disease but can be used as a screening or follow-up modality in assessing for complications of Crohn disease. Sonographic findings can often be nonspecific. Findings include loss of peristalsis, mural hyperemia of the affect bowel, fibrofatty proliferation as evidenced by a hyperechoic layer surrounding the bowel wall, and small bowel wall thickening. Additional findings include a loss of compressibility and bowel wall fibrosis which can mimic normal bowel wall submucosa. Other nonspecific findings include mesenteric lymphadenopathy and intraperitoneal fluid.[23] Complications of Crohn disease can also be seen including abscess formation and fistula formation.[24] 
2. Ulcerative colitis: Ultrasound can demonstrate increased bowel wall thickness of the rectosigmoid colon typically measuring greater than 4 mm in ulcerative colitis patients. Loss of wall haustrations, wall stratification, hyperemia on power color doppler, and enlarged mesenteric fat can also be seen.[25] 
3. Infectious diseases (bacterial enteritis, tuberculous enteritis, pseudomembranous colitis, amebic or parasitic enteritis, ascariasis): Depending on the bacterial or parasitic organism, findings can range from nonspecific wall thickening secondary to inflammation, localized fluid collections(such as in the setting of a hydatid cyst), or in rare cases the actual parasite can be visualized(such as in the setting of ascariasis).[26]
4. Colorectal and gastric cancers: Malignancy can have various shapes from a focal endophytic (or even occasionally an exophytic mass) or infiltrative wall thickening (either circumferential or involving limited portions of the wall circumference).[27]
5. Peritoneal metastasis: Peritoneal metastasis can often manifest as multi-focal masses adhering to the bowel with increased vascularity. Associated complex ascitic fluid can also be seen on occasion.[28]
6. Appendiceal mucoceles are often well visualized on ultrasound, especially when large, and typically appear as a unilocular mass and have been described to have a "whipped cream" appearance.[29]

Contraindications

There are no contraindications to this non-invasive procedure. When appropriate, such as in the setting of acute pain, when available and clinically appropriate, CT imaging should be prioritized over sonographic imaging of the bowel.

Equipment

In the bowel-ultrasound, the sonographer uses the same equipment as the normal abdominal ultrasound but requires more experience to detect abnormalities in the intestinal wall. The bowel screening can start with the common convex low-frequency probe (3.5 to 5 MHz) used in a standard abdominal ultrasound examination. Detailed visualization of the bowel can be performed using a linear high-frequency (4 to 13 MHz) probe, as it possesses high resolution.[9] When possible, it is better to use tissue harmonic imaging (THI) owing to the additional diagnostic information it can provide regarding bowel wall, lumen, and fluid content.

Personnel

Intestinal ultrasound is typically performed by:

• Sonographers
• Radiologists
• Gastroenterologists
• Emergency medicine physicians with specialized ultrasound training

Preparation

The patient should be fasting for at least 8 to 10 hours. Food can induce gaseous distension, which makes the visualization of the bowel difficult. Ingestion of a large amount of fluid could fill the bowel with water and mimic an intestinal obstruction. Thus, ideally, patients should be fasting for better intestinal visualization. Although fasting is preferable, it is not mandatory when evaluating the acute abdomen.

Technique or Treatment

The Sequence of Intestinal Ultrasound Examination

In chronic conditions: as ulcerative colitis, Crohn disease follow-up, celiac disease, etc., it is preferred to start from the epigastric region or the left iliac (sigmoid) quadrant and then proceed to examine the rest of the intestine and colon, including the terminal ileum and appendix in the right iliac quadrant.

While the sequential search patterns can differ depending on operator training, a consistent search pattern helps avoid missed diagnoses.

In acute conditions: In the setting of an acute abdomen, the examiner should start with the abdominal quadrant most tender as directed by the patient.

Limitations

If the intestinal visualization is not possible due to gaseous distension, then "graded compression" of the bowel will help shift gaseous shadows and improve image quality. Another maneuver is to turn the patient on their side (right or left according to the bowel examined), assisting in displacing visually obstructing gas.

Complications

There are no complications to this non-invasive procedure.

Clinical Significance

The Impact of Intestinal Ultrasound on the Medical Care of Inflammatory Bowel Disease

Intestinal ultrasound could be used to diagnose multiple gastrointestinal diseases (acute and chronic).[30][31][25] Inflammatory bowel diseases could be diagnosed and followed up by intestinal ultrasound, as these patients need close monitoring and follow-up. Using a cost-effective, non-invasive method with no radiological hazard such as intestinal ultrasound is greatly beneficial to the patients.

Enhancing Healthcare Team Outcomes

Intestinal ultrasound as a part of the follow-up for patients with inflammatory bowel diseases (Crohn disease and ulcerative colitis) has an important role, especially when performed by a trained operator. It can decrease the need for repeated CT or MR imaging of the abdomen. An interprofessional team approach in which family clinicians, specialists, nurses, mid-level practitioners, and ultrasound techs exercise open communication regarding conducting the examination and the findings that result can help the team guide patient care leading to better outcomes. [Level 5]