pISSN 1229-6929
eISSN 2005-8330
Open Access, Peer-reviewed
    Korean J Radiol. 2022 Mar;23(3):308-321. English.
    Published online Feb 18, 2022.
    https://doi.org/10.3348/kjr.2021.0692
    Copyright © 2022 The Korean Society of Radiology
    Review

    The Use of Transabdominal Ultrasound in Inflammatory Bowel Disease

    Jiro Hata, and Hiroshi Imamura
      • Division of Endoscopy and Ultrasound, Department of Clinical Pathology and Laboratory Medicine, Kawasaki Medical School, Okayama, Japan.
    • Corresponding author: Jiro Hata, MD, PhD, Division of Endoscopy and Ultrasound, Department of Clinical Pathology and Laboratory Medicine, Kawasaki Medical School, 577 Matsushima, Kurashiki, Okayama 701-0192, Japan. Email: ultrajiro@nifty.com
    Received September 01, 2021; Revised November 11, 2021; Accepted December 20, 2021.

    This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

    Abstract

    Transabdominal ultrasound (TAUS) is useful in all aspects of lesion screening, monitoring activity, or treating/diagnosing any related complications of inflammatory bowel disease. Its ability to screen or diagnose complications is almost the same as that of other methods, such as CT or MRI. Moreover, its noninvasiveness makes it a first-line examination method. A TAUS image depicting ulcerative colitis will show large intestinal wall thickening that is continuous from the rectum, which is mainly due to mucosal layer thickening, while for Crohn’s disease, a TAUS image is characterized by a diversity in the areas affected, distribution, and layer structure. Indicators of activity monitoring include wall thickness, wall structure, and vascular tests that use Doppler ultrasound or contrast agents. While all of these have been reported to be useful, at this time, no single parameter has been established as superior to others; therefore, a comprehensive evaluation of these parameters is justified. In addition, evaluating the elasticity of lesions using elastography is particularly useful for distinguishing between fibrous and inflammatory stenoses. However, the lack of objectivity is the biggest drawback of using ultrasound. Standardizing and popularizing the ultrasound process will be necessary, including scanning methods, equipment settings, and image analysis.

    Keywords
    Crohn’s disease; Ulcerative colitis; Ultrasound; Monitoring; Diagnosis

    INTRODUCTION

    Inflammatory bowel disease (IBD) is a global disease of the 21st century, and the number of patients is increasing rapidly, including in Asian countries [1, 2, 3, 4]. To date, there is not much disagreement between endoscopy and endoscopic mucosal healing as the basis of morphological diagnosis for IBD [5]. However, in addition to the invasiveness of this procedure, including pretreatment, as well as the inability to observe the distal side of stenosis and obtain information outside the wall, such as fistulas, the importance of transmural healing has also been emphasized, especially with regard to Crohn’s disease (CD) [6, 7]. Furthermore, since this disease frequently occurs in relatively young people and requires long-term, almost lifelong, medical care, simpler and less invasive screening and medical follow-up procedures are required. In recent years, tomographic diagnostic methods, such as CT, MRI, and transabdominal ultrasound (TAUS), have gained attention [8, 9, 10]. In particular, TAUS has many advantages, such as not requiring any pretreatment or exposure to radiation, simplicity of the technique, relatively inexpensive equipment, and widespread use. Thus, its usefulness in the diagnosis and treatment of this disease is gaining attention [11, 12, 13]. Moreover, compared to other methods, such as MRI or endoscopy, TAUS has been reported to have higher patient acceptability than when taking a blood sample [14, 15]. This study describes the usefulness of TAUS in the medical diagnosis and treatment of IBD.

    Screening IBD Using TAUS

    TAUS Equipment Used for Gastrointestinal Tract Examination

    While devices commonly used for abdominal USs may be adequate, using a high-frequency (7–12 MHz) probe for detailed observation of the lesion alongside a low frequency (3–4 MHz) probe for screening is desirable. In addition, a more accurate evaluation is expected if functions, such as color Doppler US, contrast-enhanced US, and elastography, are equipped. In contrast, highly portable devices, such as those used for point-of-care US (POCUS), are inferior to general devices in terms of image quality and functionality; these devices do not produce sufficient evidence to diagnose IBD.

    Gastrointestinal Tract Screening Scanning Method

    For the examination, special pretreatment such as colonic lavage or the use of an anticholinergic agent is not required. Performing scans requires an understanding of the gastrointestinal anatomy [16, 17]; therefore, to detect gastrointestinal lesions efficiently on US, a scanning method that reliably identifies areas that consistently appear in certain parts of the body, such as the stomach, duodenum, ascending and descending colon, and rectum, and continuously tracks the lumen (which we refer to as systematic scanning of the gastrointestinal tract) is recommended. For example, the ascending colon is located on the far-right side of the abdominal cavity, with the dorsal side fixed to the retroperitoneum. Additionally, the descending colon is bilaterally symmetrical to the ascending colon and is located on the far-left side of the abdominal cavity, with the dorsal side fixed to the retroperitoneum. However, since the small intestine, mainly the jejunum, is located on the ventral side, unlike the ascending colon, it is necessary to ensure that it occupies the deepest position in the abdominal cavity when performing a scan. Systematic scanning of the small intestine is difficult, but the jejunum and ileum can be distinguished from each other, in terms of the shape (density and height) of their folds and their location.

    The gastrointestinal screening procedure used at our facility is as follows: first, the region from the abdominal esophagus to the duodenal bulb is scanned, followed by a continuous scan from the ascending colon to the rectum. As the practitioner gets used to this technique, it takes between a minute or two to complete the procedure. When there is possibility of small intestinal lesions, light pressure is applied to extend the intestinal tract. Then, a scan is carefully conducted from the upper left abdomen (mainly the jejunum) to the lower abdomen (mainly the ileum), which takes a few minutes. Therefore, the total time required for the screening of the entire gastrointestinal tract is five minutes or less when the operator is experienced in gastrointestinal ultrasonography. Figure 1 shows the affected ileal loop detected during the screening of the small intestine.

    Fig. 1
    Crohn’s disease.
    An affected ileal loop in the pelvic cavity. There are two bowel segments showing loss of wall stratification (arrows), representing severe transmural inflammation.

    There are some tips to successfully screen and evaluate the lesions. The detection of a suspicious lesion starts with the use of a 4-MHz convex probe to visualize the entire abdomen since it permits better penetration of the US beam. Applying adequate pressure to the probe is crucial to minimize artifacts, such as multiple reverberations from the abdominal wall and sidelobe artifacts from the adjacent gastrointestinal tract. Application of pressure such that the examiner can visualize the lesion, at a depth of approximately 4–6 cm with a 4-MHz convex probe and at a depth of approximately 2–3 cm with a 7-MHz linear probe, can be helpful. The convex probe is switched to a 7-MHz linear probe after detecting a suspicious lesion to obtain detailed information regarding the lesion, including the wall stratification. Zooming in on the lesion with a 4-MHz convex probe can be an alternative when the 7-MHz probe cannot provide an image suitable for analysis because of beam attenuation caused by the patient’s constitution.

    Demonstration of the wall layer structure is key to judging the suitability of an US image. The image is considered suitable to evaluate the lesion if the layer structure of the lesion or the adjacent unaffected bowel segment can be appreciated when the lesion has lost the wall stratification. US can be used as a substitute for frequent CT or MRI examinations if a good quality image can be obtained.

    TAUS Images of a Normal Gastrointestinal Tract

    Regardless of the part of the body, a TAUS image of a normal gastrointestinal wall has the following five-layer structure: starting from the luminal side, hyperechoic (interface echo and part of the mucosal layer), hypoechoic (mucosa and muscularis mucosa), hyperechoic (submucosa), hypoechoic (muscularis propria), and hyperechoic (serous membrane and interface echo) [18, 19].

    In inflammatory diseases, lesions are depicted as areas with wall thickening, but there are some reports of lesions with normal wall thickness. At the same time, lesions are also affected by factors, such as the degree of the wall stretch or the frequency used. Therefore, setting a strict cutoff value for wall thickness is difficult [20]. Therefore, as a guide, an abnormality in the small or large intestine was suspected when the wall thickness was 4 mm or greater. However, in chronic inflammatory diseases, such as IBD, active lesions may be found endoscopically, even if they are less than 4 mm. Moreover, even if everything is normal, if the lumen is empty, the wall thickness may be 4 mm or greater. Therefore, it is necessary to make a comprehensive judgment that considers other factors, such as how that area compares to other areas, the normal parts of the body, and the layer structure.

    TAUS Images of UC

    A typical US image of ulcerative colitis (UC) depicts a distinct wall thickening with a layered structure extending continuously from the rectum to the oral cavity [21, 22, 23, 24]. When left untreated, the thickening of the mucosal layer was conspicuous (Fig. 2A-C). It is difficult for shallow ulceration to be depicted, but when an ulcer becomes relatively deep, the first layer, which is the interface echo of the luminal surface, becomes unclear. As it becomes deeper, it becomes identifiable as a missing part of the wall.

    Fig. 2
    Ulcerative colitis.
    A. Longitudinal view of the sigmoid colon. The wall layer structure and thickening of the mucosal layer are clearly demonstrated (probe: 7 MHz linear). B. Transverse view of the same lesion using a 24-MHz linear probe. Each layer of the lesion is clearly visible. C. Blood flow signals using Superb Microvascular Imaging. Increased blood flow signals, mainly in the mucosal layer as the focus of inflammation, are noted (probe: 24 MHz linear). D. Endoscopic figure of the same lesion. Endoscopy shows mild inflammation of the mucosa, with an endoscopic Matts score of grade 2.

    TAUS Images of CD

    CD can be characterized by the presence of lesions in all parts of the gastrointestinal tract, and the morphology of the lesions varies from aphthous ulcers to ulcers with a pavement-like appearance. Therefore, it is difficult to conclude what the condition is from a single image. In other words, it can be said that this diversity in body part location and morphology is characteristic of CD. Although there are reports about the thickness and layer structure, these findings are not necessarily CD-specific [25, 26]. If there are multiple lesions, skip lesions, which are interspersed along a normal gastrointestinal tract, can be found between them, and there are narrow and deep longitudinal ulcers (Fig. 3) that occur on the mesenteric side of the intestine. These are considered characteristic findings of this disease [27].

    Fig. 3
    Crohn’s disease.
    A. Super-wide view of the terminal ileum in a patient with Crohn’s disease. The wall thickness, as well as the wall stratification, varies according to the location (probe: 4 MHz convex). B. Close-up view of the lesion using a 7-MHz linear probe. The loss of wall stratification of the posterior wall is demonstrated. C. Transverse view of the same lesion. The focal loss of wall stratification on the side of the mesentery represents longitudinal ulcer (probe: 7 MHz linear). D. Transverse view of the same lesion using Superb Microvascular Imaging. Increased blood flow signals are prominent on the mesenteric side. E. Endoscopic figure of the same lesion. A longitudinal ulcer is demonstrated (arrow). Loss of wall stratification on the mesenteric side is one of the specific findings of Crohn’s disease.

    IBD Detection and Diagnostic Ability Using TAUS

    Although there are some reports on the ability of TAUS to detect and diagnose IBD lesions, they generally show a good diagnostic ability that is almost equivalent to other modalities [28, 29, 30, 31, 32, 33, 34, 35]. While normal equipment (not the portable type) was used in these studies, the usefulness of POCUS in IBD diagnosis and treatment in clinics has also been reported [36, 37]. Hence, for patients who complain of symptoms that suggest IBD, such as chronic diarrhea and bloody stool, TAUS could be the first-line testing method because of its simple technique and non-invasiveness, despite an associated lack of objectivity.

    Evaluation of IBD Activity Using TAUS

    Since IBD is a disease that repeatedly goes through a cycle of remission and exacerbation for more than a year at a time, repeated endoscopy is a heavy burden on patients, as well as the medical staff and the medical economy. The number of endoscopies that must be performed can be significantly reduced by using TAUS to evaluate IBD activity.

    The following indicators should be considered when evaluating IBD activity using TAUS. There are many reports on the usefulness of the following: 1) wall thickness, 2) wall layer structure, 3) intramural blood flow measured using Doppler US, 4) intra-intestinal blood flow measured using contrast-enhanced US, and 5) elastography. In extreme cases, when the inflammation becomes severe, the following trends occur: 1) the wall becomes thicker, 2) the submucosal thickening becomes more noticeable, and with extreme inflammation or fibrosis, the layer structure disappears, 3) the color Doppler signal increases (more blood vessels are displayed), and 4) the wall appears enhanced earlier with the contrast US. Although 1) and 2) are indicators that can be compared between different patients, they do not always accurately reflect the patient’s condition as the lesions are modified by fibrosis or other factors in the process of chronic inflammation. In contrast, intra-intestinal blood flow measured using Doppler US and intra-intestinal blood flow measured using contrast-enhanced US are relatively sensitive indicators that reflect the degree of inflammation. However, since the measurement of intramural blood flow using Doppler US or contrast US is also affected by other factors such as the device performance, the patient’s physique, and the location of the lesion in the body, these measurements should, in principle, be used for follow-up examinations of the same part of the body in the same patient.

    Wall Thickness

    Wall thickening and the degree to which it has thickened are the simplest and most reproducible among examiners [38], and the measured values are not significantly affected by influences such as the patient’s condition or device performance, making them suitable for use as a global standard. As previously mentioned, it has been reported that there is a relatively good correlation between the wall thickness and the degree of inflammation in both CD and UC [39, 40, 41, 42, 43, 44]. However, the following points should be noted: in CD, it takes time to improve the wall thickness with treatment, and the proportion of the wall that reduces in thickness is not high [45, 46]. In addition, since the mucous membrane is the main cause of inflammation in UC, the wall is not as thick as that of CD. Therefore, it is not always easy to judge the therapeutic effect by only looking at the wall thickness [47]. Figure 4 shows an example of this phenomenon. With a wall thickness of approximately 3 mm, it is not necessarily pathological, but the layer structure makes it unclear. In addition, abundant blood flow signals were observed using Superb Microvascular Imaging (SMI), suggesting high activity, which was confirmed by endoscopy.

    Fig. 4
    Ulcerative colitis.
    A. Longitudinal view of the sigmoid colon in a patient with ulcerative colitis. Although the wall thickening is mild (3 mm), the wall layer structure is blurred (probe: 4 MHz convex). B. Close-up view of the lesion using a 7 MHz linear probe. Thickening of the submucosal layer is demonstrated, while the mucosal layer is not clearly recognized. C. Evaluation of blood flow using Superb Microvascular Imaging of the same lesion. Increased blood flow, especially on the side of the lumen, is demonstrated (probe: 7 MHz linear). D. Endoscopic view of the same lesion. Although the wall thickness observed with ultrasound is mild, endoscopy shows severe inflammation, classified as Matts grade 4.

    Layer Structure

    The layered structure reflects the histopathological changes of all layers and is an important piece of information that cannot be obtained by endoscopy. Loss of this layered structure in both CD and UC suggests a more severe and poor prognosis [48, 49, 50, 51, 52]. The disappearance of the local layered structure in CD also indicates a deep longitudinal ulcer [27, 53]. Meanwhile, some disadvantages of considering the layered structure as a parameter are that it may be affected by factors such as the frequency of the probe being used, the physical condition of the patient, and the fact that this evaluation metric cannot be quantified and lacks objectivity. Therefore, these obstacles need to be overcome to standardize the utilization of this parameter.

    Doppler US

    It has long been known that inflammation increases blood flow, and it is reasonable to consider that blood flow evaluation using Doppler US is likely to be useful for IBD. As the use of Doppler US has become widespread, there have been reports on the evaluation of blood flow in the superior mesenteric artery and/or vein, but contradictory results have been reported [54, 55, 56, 57]. Theoretically, blood flow in these vessels depends more on physiological conditions than on inflammation in certain parts of the intestinal tract. Moreover, measurement errors between examiners cannot be ignored [58, 59]. Accordingly, it would be reasonable to consider it unsuitable as a parameter for assessing lesion activity. Meanwhile, evaluating the degree of local inflammation mainly from the amount of blood flow signals using a color Doppler US seems to be a more appropriate method; its usefulness has been reported for both CD and UC [38, 60, 61, 62, 63, 64, 65]. However, from the perspective of ultrasonic engineering, Doppler US sensitivity is affected by various factors such as the frequency used, display flow velocity range (folded frequency), and brightness of the background B-mode image. It also depends greatly on the path (acoustic pathway) leading to the target organ. Therefore, it should be kept in mind that although these conditions are offset by comparing groups with large numbers of patients and certain tendencies can be observed, the results obtained for a lesion in one patient are not theoretically valid for comparison with lesions in other patients or even in the same patient at different sites. In addition, in the evaluation of intra-intestinal blood flow, the recently developed SMI has superior sensitivity, especially for a slower blood flow compared to the conventional color Doppler US [66, 67, 68]; although it is expected to be useful in assessing the activity of this disease, no clear evidence has been reported about its superiority over the conventional color or power Doppler US. Figure 5 shows an image of a patient follow-up that was conducted using SMI that looked at the same part of the body. It can be seen that the blood flow signal is reduced, reflecting an improvement in the pathological condition of the patient with treatment.

    Fig. 5
    Crohn’s disease.
    A. SMI image of a lesion in a patient with Crohn’s disease before treatment. Transmural increase of blood flow is demonstrated, and the ratio of the pixel counts of the colored area to those of the range of interest is 51.3% (probe: 7 MHz linear). B. SMI image of the lesion after successful treatment. The blood flow signals decrease as the ratio decreases to 27.0% (probe: 7 MHz linear). SMI = Superb Microvascular Imaging

    Contrast-Enhanced US

    Various indicators such as maximum peak intensity, area under the curve, and time until the enhancement reaches the maximum value (time to peak) when the time-course of contrast enhancement of the wall is displayed as a time-intensity curve (TIC), are used as parameters for evaluating activity when using contrast-enhanced US. For these parameters, compatibility between patients is not necessarily guaranteed. This is because if the ultrasonic wave is strongly attenuated by the time it reaches the target organ, parameters such as maximum peak intensity and area under the curve, will naturally be affected by this and decrease as a result; the time to peak may also be shortened if the time when the shading starts to appear on the US (zero point) is delayed. Therefore, the slope of the line connecting the peak from the zero point (coefficient of the enhancement wash-in slope) is theoretically considered to be the most compatible indicator. However, meta-analyses and systematic reviews have reported that contrast-enhanced US exhibits high sensitivity and specificity in the evaluation of CD activity [69, 70]; hence, it is possible that it may be useful. Figure 6 shows the TIC of the contrast-enhanced US of CD. On the other hand, there are few reports on the usefulness of contrast-enhanced US for UC [71, 72], and there is currently little evidence at the meta-analysis or systematic review level, regarding its usefulness.

    Fig. 6
    Contrast ultrasound of a lesion of Crohn’s disease.
    Contrast ultrasound images using Sonazoid™ and the time-intensity curve of the enhancement with some parameters are shown on the right (probe: 7 MHz linear).

    Contrast-enhanced US is more cost-effective than other scanning methods such as CT or MRI [73]; however, these reports were for masses found in the liver. In addition to other factors such as a longer examination time, the invasiveness of the procedure due to the use of an intravenous contrasting agent on the patient as well as the increased financial burden, a drawback of this method is that it requires equipment that can handle contrast-enhanced US and its TIC analysis. In addition, since the strongest enhancement of the lesion is observed only during the early vascular phase, it is difficult to evaluate multiple lesions at a time using contrast US. Therefore, we must decide the lesion of interest that is the most affected bowel segment, before performing contrast US. Thus, there is uncertainty as to whether this method will become widespread as a global standard.

    Hence, at present, it is considered more realistic to comprehensively judge wall thickness, layer structure, and Doppler US findings and, if necessary, perform contrast-enhanced US [44, 46, 74]. While we have previously published a report outlining a scoring system for CD activity using wall thickness and layer structure [49], it unfortunately never became widespread due to its complexity. In the future, the development of a simpler and more useful scoring system is desirable.

    Diagnosis of Complications

    It is not always easy to use an endoscope to diagnose complications related to IBD, but the usefulness of US, which is a tomographic diagnostic method, is promising. Stenosis is a complication often encountered in CD that requires surgical or endoscopic interventions [75]. US stenosis is defined as luminal narrowing (< 10 mm) with oral dilation (> 25–30 mm) [76, 77]; however, it may not always be accompanied by pathological thickening of the stenotic site. Although only one end of the stenotic site can be evaluated with an endoscope, it is possible for the US to evaluate the length of the stenosis and the properties of the wall, including its relationship with surrounding tissues. The mechanism of stenosis is complicated, including hyperplasia of smooth muscle that is associated with chronic inflammation as well as the compression of adipose tissue outside the wall due to wall thickening. However, it is generally necessary to determine whether the stenosis is predominantly due to inflammation or fibrosis, as the former is likely to improve with conservative treatment, while the latter requires surgical treatment or endoscopic dilatation [78]. Regarding the differentiation between inflammation and fibrosis using TAUS, there are reports that, in B-mode, the hypoechoic pattern is more typical in inflammatory stenosis, while the stratified or nonhomogeneous echo pattern indicates fibrosis [79, 80]. At the same time, it is important to note that factors such as the appearance and uniformity of the layered structure differ depending on the frequency used or the patient’s condition. Additionally, reports using color Doppler and contrast-enhanced US indicated more blood flow with inflammatory stenosis compared to fibrous stenosis, and the finding is believed to be useful in differentiating between inflammatory and fibrous stenosis [81, 82, 83, 84, 85]. Recently, it has been reported that evaluation of lesion hardness using methods such as strain elastography or shear-wave elastography (SWE) is useful for diagnosing fibrosis [86, 87, 88, 89, 90]. In particular, SWE is expected to be used as an objective and quantitative indicator as well as for lesion activity evaluation in the future. Figure 7 shows stenotic lesions in CD. Clear stenosis of the upper lumen and dilation of the oral intestinal tract were observed in B-mode. When SWE was used, the lesion appeared hard, suggesting that the stenosis was accompanied by a high degree of fibrosis. TAUS can also be used to diagnose areas of stasis for capsule endoscopy and patency capsules [91]. Figure 8 shows an image of a patency capsule retained in the ileum in the case of CD.

    Fig. 7
    Bowel stenosis is seen in a patient with Crohn’s disease.
    A. Marked luminal narrowing with dilatation of the oral side. The wall stratification of the stenotic segments is lost (probe: 7 MHz linear). B. Shear-wave elastography of the stenotic lesions. The stenotic area is orange-colored, while the adjacent mesentery is blue, which indicates that the lesion has higher elasticity. The shear wave speed is as high as 3.81 m/s (probe: 7 MHz linear).

    Fig. 8
    Retention of a patency capsule in a patient with Crohn’s disease.
    The patency capsule demonstrated as a linear, strong echo accompanied by an acoustic window is trapped at the oral side of the stenotic lesion (probe: 4 MHz convex).

    The sinus and fistula are depicted as linear or band-shaped hypoechoic lesions, continuing from the superior intestinal lesions of the TAUS; air may also be observed inside (Fig. 9) [92, 93]. Abscesses are also considered to be low to non-echoic regions with liquid components and sometimes aeration (Fig. 10) [94]. Since it has been reported that the diagnostic abilities of TAUS are almost the same as those of other methods such as CT and MRI scans [95], this method should be tried first.

    Fig. 9
    Ileo-ileal fistula in a patient with Crohn’s disease.
    The fistula between the two bowel segments is demonstrated as a hypoechoic band with small air bubbles inside (probe: 7 MHz linear).

    Fig. 10
    Abscess in a patient with Crohn’s disease.
    A. An abscess is identified as a hypoechoic area attached to the bowel lesion. Fluctuations in the contents can be noticed by real-time observation (probe: 4 MHz convex). B. Superb Microvascular Imaging image of the same lesion. The abscess is identified as an avascular area (probe: 7 MHz linear). C. Contrast ultrasound of the same lesion. The image on the right shows the contrast ultrasound image and the image on the left shows the monitoring grayscale image. The abscess shows no contrast enhancement, while the surrounding area shows increased enhancement, which is known as ring enhancement (arrows) (probe: 4 MHz convex). D. Contrast-enhanced computed tomography image. The abscess is identified as an area without enhancement.

    Meanwhile, it is not easy to diagnose bleeding with B-mode (black and white images) or color Doppler; hence, we have reported a method for showing extravasation of a contrast agent using a contrast-enhanced US and making a diagnosis [96]. However, no IBD-specific papers have been found, and this method is not commonly used, as yet. Figure 11 shows a case of CD in which evidence of active bleeding was found using contrast-enhanced US.

    Fig. 11
    BBowel hemorrhage seen in a patient with Crohn’s disease.
    A. An echogenic mass in the ileal lumen with a small, rounded, hypoechoic area inside is detected. The echogenic mass (circled area) might represent a blood clot, and the hypoechoic area may represent fresh blood (probe: 7 MHz linear). B. Contrast ultrasound of the same lesion. The image on the right shows the contrast ultrasound image and the image on the left shows the monitoring grayscale image. Extravasation of the contrast agent into the hypoechoic area (arrows) is immediately demonstrated, and the contrast agent gradually spreads into the mass, which represents the blood clot (circled area) (probe: 7 MHz linear).

    Toxic megacolon is a serious intestinal complication that can occur in a case of UC, but there are very few reports on this complication, in which TAUS was used. In these cases, the large intestine was dilated (> 6 cm), the wall was thinned (< 2 mm), and the lumen was filled with watery stool (Fig. 12) [97]. Evidently, perforation is determined by detecting free air on US. In addition, TAUS can determine the perforation site and the risk of perforation; however, there are no reports on this. Figure 13 shows a case of UC in which a perforation occurred 12 hours after the examination, and deep subserosal ulcers in the cecum and turbid ascites in the surrounding area, signifying imminent perforation.

    Fig. 12
    Colonic perforation seen in a patient with ulcerative colitis.
    A. Free air is demonstrated as hyperechoic bands accompanied by multiple echoes beneath the parietal peritoneum (probe: 7 MHz linear). B. Longitudinal view of the ascending colon. The wall thickness is thin, and dilatation of the colonic lumen filled with watery stool is demonstrated, which indicates toxic megacolon (probe: 4 MHz convex). C. Abdominal X-ray. Colonic dilatation, suggesting toxic megacolon, as well as free air, is demonstrated.

    Fig. 13
    Impending perforation of the cecum in a patient with ulcerative colitis.
    Deep ulcers are demonstrated, and an ulcer is as deep as the subserosa, indicating a high risk of perforation (probe: 7 MHz linear).

    CONCLUSION

    TAUS is considered to be extremely useful in the diagnosis and treatment of IBD as a non-invasive and simple tomographic diagnostic method. It is an indispensable examination method at our facility for the diagnosis of IBD and several other gastrointestinal diseases, such as acute inflammatory diseases and neoplasm. Since TAUS is non-invasive and does not require any special preparation, it can be easily performed and repeated at any time, whenever necessary. In addition, TAUS can provide detailed information regarding the transmural changes of the lesion, extramural complications, and even minute blood flow changes of the lesion, with its high special and temporal resolution. Therefore, we believe that TAUS has great potential to be the first-line morphological examination method in the diagnostic strategy of gastrointestinal diseases. However, there are some issues that need to be resolved related to the universalization and standardization, as for such a technique, the biggest drawback could be regarding equipment selection and settings, parameters used for evaluation, and lack of objectivity. In the future, discussions between facilities, academic societies, and nations would be necessary.

    Notes

    Conflicts of Interest:The authors have no potential conflicts of interest to disclose.

    Author Contributions:

    • Conceptualization: Jiro Hata.

    • Resources: Jiro Hata.

    • Supervision: Hiroshi Imamura.

    • Validation: Jiro Hata.

    • Writing—original draft: Jiro Hata.

    • Writing—review & editing: Jiro Hata.

    Funding Statement:None

    Availability of Data and Material

    The datasets generated or analyzed during the study are available from the corresponding author on reasonable request.

    References

      1. GBD 2017 Inflammatory Bowel Disease Collaborators. The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol 2020;5:17–30.
      1. Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI, et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 2018;390:2769–2778.
      1. Olfatifar M, Zali MR, Pourhoseingholi MA, Balaii H, Ghavami SB, Ivanchuk M, et al. The emerging epidemic of inflammatory bowel disease in Asia and Iran by 2035: a modeling study. BMC Gastroenterol 2021;21:204
      1. Park J, Cheon JH. Incidence and prevalence of inflammatory bowel disease across Asia. Yonsei Med J 2021;62:99–108.
      1. Neurath MF, Travis SP. Mucosal healing in inflammatory bowel diseases: a systematic review. Gut 2012;61:1619–1635.
      1. Civitelli F, Nuti F, Oliva S, Messina L, La Torre G, Viola F, et al. Looking beyond mucosal healing: effect of biologic therapy on transmural healing in pediatric Crohn’s disease. Inflamm Bowel Dis 2016;22:2418–2424.
      1. Fernandes SR, Rodrigues RV, Bernardo S, Cortez-Pinto J, Rosa I, da Silva JP, et al. Transmural healing is associated with improved long-term outcomes of patients with Crohn’s disease. Inflamm Bowel Dis 2017;23:1403–1409.
      1. Gomollón F, Dignass A, Annese V, Tilg H, Van Assche G, Lindsay JO, et al. 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis 2017;11:3–25.
      1. Annese V, Daperno M, Rutter MD, Amiot A, Bossuyt P, East J, et al. European evidence based consensus for endoscopy in inflammatory bowel disease. J Crohns Colitis 2013;7:982–1018.
      1. Panes J, Bouhnik Y, Reinisch W, Stoker J, Taylor SA, Baumgart DC, et al. Imaging techniques for assessment of inflammatory bowel disease: joint ECCO and ESGAR evidence-based consensus guidelines. J Crohns Colitis 2013;7:556–585.
      1. Maconi G, Nylund K, Ripolles T, Calabrese E, Dirks K, Dietrich CF, et al. EFSUMB recommendations and clinical guidelines for intestinal ultrasound (GIUS) in inflammatory bowel diseases. Ultraschall Med 2018;39:304–317.
      1. Fraquelli M, Castiglione F, Calabrese E, Maconi G. Impact of intestinal ultrasound on the management of patients with inflammatory bowel disease: how to apply scientific evidence to clinical practice. Dig Liver Dis 2020;52:9–18.
      1. Bryant RV, Friedman AB, Wright EK, Taylor KM, Begun J, Maconi G, et al. Gastrointestinal ultrasound in inflammatory bowel disease: an underused resource with potential paradigm-changing application. Gut 2018;67:973–985.
      1. Buisson A, Gonzalez F, Poullenot F, Nancey S, Sollellis E, Fumery M, et al. Comparative acceptability and perceived clinical utility of monitoring tools: a nationwide survey of patients with inflammatory bowel disease. Inflamm Bowel Dis 2017;23:1425–1433.
      1. Rajagopalan A, Sathananthan D, An YK, Van De Ven L, Martin S, Fon J, et al. Gastrointestinal ultrasound in inflammatory bowel disease care: patient perceptions and impact on disease-related knowledge. JGH Open 2020;4:267–272.
      1. Atkinson NSS, Bryant RV, Dong Y, Maaser C, Kucharzik T, Maconi G, et al. How to perform gastrointestinal ultrasound: anatomy and normal findings. World J Gastroenterol 2017;23:6931–6941.
      1. Atkinson NS, Bryant RV, Dong Y, Maaser C, Kucharzik T, Maconi G, et al. WFUMB position paper. Learning gastrointestinal ultrasound: theory and practice. Ultrasound Med Biol 2016;42:2732–2742.
      1. Aibe T, Fuji T, Okita K, Takemoto T. A fundamental study of normal layer structure of the gastrointestinal wall visualized by endoscopic ultrasonography. Scand J Gastroenterol Suppl 1986;123:6–15.
      1. Folvik G, Bjerke-Larssen T, Odegaard S, Hausken T, Gilja OH, Berstad A. Hydrosonography of the small intestine: comparison with radiologic barium study. Scand J Gastroenterol 1999;34:1247–1252.
      1. Chiorean L, Schreiber-Dietrich D, Braden B, Cui X, Dietrich CF. Transabdominal ultrasound for standardized measurement of bowel wall thickness in normal children and those with Crohn’s disease. Med Ultrason 2014;16:319–324.
      1. Hata J, Haruma K, Suenaga K, Yoshihara M, Yamamoto G, Tanaka S, et al. Ultrasonographic assessment of inflammatory bowel disease. Am J Gastroenterol 1992;87:443–447.
      1. Antonelli E, Giuliano V, Casella G, Villanacci V, Baldini V, Baldoni M, et al. Ultrasonographic assessment of colonic wall in moderate-severe ulcerative colitis: comparison with endoscopic findings. Dig Liver Dis 2011;43:703–706.
      1. Bru C, Sans M, Defelitto MM, Gilabert R, Fuster D, Llach J, et al. Hydrocolonic sonography for evaluating inflammatory bowel disease. AJR Am J Roentgenol 2001;177:99–105.
      1. Strobel D, Goertz RS, Bernatik T. Diagnostics in inflammatory bowel disease: ultrasound. World J Gastroenterol 2011;17:3192–3197.
      1. Worlicek H, Lutz H, Heyder N, Matek W. Ultrasound findings in Crohn’s disease and ulcerative colitis: a prospective study. J Clin Ultrasound 1987;15:153–163.
      1. Nylund K, Leh S, Immervoll H, Matre K, Skarstein A, Hausken T, et al. Crohn’s disease: comparison of in vitro ultrasonographic images and histology. Scand J Gastroenterol 2008;43:719–726.
      1. Kunihiro K, Hata J, Haruma K, Manabe N, Tanaka S, Chayama K. Sonographic detection of longitudinal ulcers in Crohn disease. Scand J Gastroenterol 2004;39:322–326.
      1. Nassef MA, Botros SM, Ghaffar MKA. The update of ultrasound techniques in diagnosis of inflammatory bowel disease. Egypt J Radiol Nucl Med 2014;45:289–294.
      1. van Wassenaer EA, de Voogd FAE, van Rijn RR, van Der Lee JH, Tabbers MM, van Etten-Jamaludin FS, et al. Diagnostic accuracy of transabdominal ultrasound in detecting intestinal inflammation in paediatric IBD patients—a systematic review. J Crohns Colitis 2019;13:1501–1509.
      1. Horsthuis K, Bipat S, Bennink RJ, Stoker J. Inflammatory bowel disease diagnosed with US, MR, scintigraphy, and CT: meta-analysis of prospective studies. Radiology 2008;247:64–79.
      1. Fraquelli M, Colli A, Casazza G, Paggi S, Colucci A, Massironi S, et al. Role of US in detection of Crohn disease: meta-analysis. Radiology 2005;236:95–101.
      1. Dong J, Wang H, Zhao J, Zhu W, Zhang L, Gong J, et al. Ultrasound as a diagnostic tool in detecting active Crohn’s disease: a meta-analysis of prospective studies. Eur Radiol 2014;24:26–33.
      1. Ziech ML, Hummel TZ, Smets AM, Nievelstein RA, Lavini C, Caan MW, et al. Accuracy of abdominal ultrasound and MRI for detection of Crohn disease and ulcerative colitis in children. Pediatr Radiol 2014;44:1370–1378.
      1. Gonzalez-Montpetit E, Ripollés T, Martinez-Pérez MJ, Vizuete J, Martín G, Blanc E. Ultrasound findings of Crohn’s disease: correlation with MR enterography. Abdom Radiol (NY) 2021;46:156–167.
      1. Dong J, Wang H, Zhao J, Zhu W, Zhang L, Gong J, et al. Ultrasound as a diagnostic tool in detecting active Crohn’s disease: a meta-analysis of prospective studies. Eur Radiol 2014;24:26–33.
      1. Novak K, Tanyingoh D, Petersen F, Kucharzik T, Panaccione R, Ghosh S, et al. Clinic-based point of care transabdominal ultrasound for monitoring Crohn’s disease: impact on clinical decision making. J Crohns Colitis 2015;9:795–801.
      1. Sathananthan D, Rajagopalan A, Van De Ven L, Martin S, Fon J, Costello S, et al. Point-of-care gastrointestinal ultrasound in inflammatory bowel disease: an accurate alternative for disease monitoring. JGH Open 2019;4:273–279.
      1. Fraquelli M, Sarno A, Girelli C, Laudi C, Buscarini E, Villa C, et al. Reproducibility of bowel ultrasonography in the evaluation of Crohn’s disease. Dig Liver Dis 2008;40:860–866.
      1. Civitelli F, Di Nardo G, Oliva S, Nuti F, Ferrari F, Dilillo A, et al. Ultrasonography of the colon in pediatric ulcerative colitis: a prospective, blind, comparative study with colonoscopy. J Pediatr 2014;165:78–84.
        e2.
      1. Parente F, Molteni M, Marino B, Colli A, Ardizzone S, Greco S, et al. Are colonoscopy and bowel ultrasound useful for assessing response to short-term therapy and predicting disease outcome of moderate-to-severe forms of ulcerative colitis?: a prospective study. Am J Gastroenterol 2010;105:1150–1157.
      1. Maconi G, Parente F, Bollani S, Cesana B, Bianchi Porro G. Abdominal ultrasound in the assessment of extent and activity of Crohn’s disease: clinical significance and implication of bowel wall thickening. Am J Gastroenterol 1996;91:1604–1609.
      1. Mayer D, Reinshagen M, Mason RA, Muche R, von Tirpitz C, Eckelt D, et al. Sonographic measurement of thickened bowel wall segments as a quantitative parameter for activity in inflammatory bowel disease. Z Gastroenterol 2000;38:295–300.
      1. Hirche TO, Russler J, Schröder O, Schuessler G, Kappeser P, Caspary WF, et al. The value of routinely performed ultrasonography in patients with Crohn disease. Scand J Gastroenterol 2002;37:1178–1183.
      1. Maaser C, Petersen F, Helwig U, Fischer I, Roessler A, Rath S, et al. Intestinal ultrasound for monitoring therapeutic response in patients with ulcerative colitis: results from the TRUST&UC study. Gut 2020;69:1629–1636.
      1. Castiglione F, Testa A, Rea M, De Palma GD, Diaferia M, Musto D, et al. Transmural healing evaluated by bowel sonography in patients with Crohn’s disease on maintenance treatment with biologics. Inflamm Bowel Dis 2013;19:1928–1934.
      1. Ripollés T, Paredes JM, Martínez-Pérez MJ, Rimola J, Jauregui-Amezaga A, Bouzas R, et al. Ultrasonographic changes at 12 weeks of anti-TNF drugs predict 1-year sonographic response and clinical outcome in Crohn’s disease: a multicenter study. Inflamm Bowel Dis 2016;22:2465–2473.
      1. Dietrich CF. Significance of abdominal ultrasound in inflammatory bowel disease. Dig Dis 2009;27:482–493.
      1. Bozkurt T, Rommel T, Stabenow-Lohbauer U, Langer M, Schmiegelow P, Lux G. Sonographic bowel wall morphology correlates with clinical and endoscopic activity in Crohn’s disease and ulcerative colitis. Eur J Ultrasound 1996;4:27–33.
      1. Futagami Y, Haruma K, Hata J, Fujimura J, Tani H, Okamoto E, et al. Development and validation of an ultrasonographic activity index of Crohn’s disease. Eur J Gastroenterol Hepatol 1999;11:1007–1012.
      1. Kunihiro K, Hata J, Manabe N, Mitsuoka Y, Tanaka S, Haruma K, et al. Predicting the need for surgery in Crohn’s disease with contrast harmonic ultrasound. Scand J Gastroenterol 2007;42:577–585.
      1. Haber HP, Busch A, Ziebach R, Dette S, Ruck P, Stern M. Ultrasonographic findings correspond to clinical, endoscopic, and histologic findings in inflammatory bowel disease and other enterocolitides. J Ultrasound Med 2002;21:375–382.
      1. Dixit R, Chowdhury V, Kumar N. Hydrocolonic sonography in the evaluation of colonic lesions. Abdom Imaging 1999;24:497–505.
      1. Hata J, Haruma K, Yamanaka H, Fujimura J, Yoshihara M, Shimamoto T, et al. Ultrasonographic evaluation of the bowel wall in inflammatory bowel disease: comparison of in vivo and in vitro studies. Abdom Imaging 1994;19:395–399.
      1. Bolondi L, Gaiani S, Brignola C, Campieri M, Rigamonti A, Zironi G, et al. Changes in splanchnic hemodynamics in inflammatory bowel disease. Non-invasive assessment by Doppler ultrasound flowmetry. Scand J Gastroenterol 1992;27:501–507.
      1. Giovagnorio F, Diacinti D, Vernia P. Doppler sonography of the superior mesenteric artery in Crohn’s disease. AJR Am J Roentgenol 1998;170:123–126.
      1. Karoui S, Nouira K, Serghini M, Ben Mustapha N, Boubaker J, Menif E, et al. Assessment of activity of Crohn’s disease by Doppler sonography of superior mesenteric artery flow. J Crohns Colitis 2010;4:334–340.
      1. Maconi G, Parente F, Bollani S, Imbesi V, Ardizzone S, Russo A, et al. Factors affecting splanchnic haemodynamics in Crohn’s disease: a prospective controlled study using Doppler ultrasound. Gut 1998;43:645–650.
      1. Dietrich CF, Jedrzejczyk M, Ignee A. Sonographic assessment of splanchnic arteries and the bowel wall. Eur J Radiol 2007;64:202–212.
      1. Zoli M, Merkel C, Sabbà C, Sacerdoti D, Gaiani S, Ferraioli G, et al. Interobserver and inter-equipment variability of echo-Doppler sonographic evaluation of the superior mesenteric artery. J Ultrasound Med 1996;15:99–106.
      1. Sasaki T, Kunisaki R, Kinoshita H, Yamamoto H, Kimura H, Hanzawa A, et al. Use of color Doppler ultrasonography for evaluating vascularity of small intestinal lesions in Crohn’s disease: correlation with endoscopic and surgical macroscopic findings. Scand J Gastroenterol 2014;49:295–301.
      1. Migaleddu V, Scanu AM, Quaia E, Rocca PC, Dore MP, Scanu D, et al. Contrast-enhanced ultrasonographic evaluation of inflammatory activity in Crohn’s disease. Gastroenterology 2009;137:43–52.
      1. Drews BH, Barth TF, Hänle MM, Akinli AS, Mason RA, Muche R, et al. Comparison of sonographically measured bowel wall vascularity, histology, and disease activity in Crohn’s disease. Eur Radiol 2009;19:1379–1386.
      1. Epifanio M, Baldisserotto M, Spolidoro JV, Gaiger A. Grey-scale and colour Doppler sonography in the evaluation of children with suspected bowel inflammation: correlation with colonoscopy and histological findings. Clin Radiol 2008;63:968–978.
      1. Ruess L, Blask AR, Bulas DI, Mohan P, Bader A, Latimer JS, et al. Inflammatory bowel disease in children and young adults: correlation of sonographic and clinical parameters during treatment. AJR Am J Roentgenol 2000;175:79–84.
      1. Arienti V, Campieri M, Boriani L, Gionchetti P, Califano C, Giancane S, et al. Management of severe ulcerative colitis with the help of high resolution ultrasonography. Am J Gastroenterol 1996;91:2163–2169.
      1. Durmaz MS, Sivri M. Comparison of superb micro-vascular imaging (SMI) and conventional Doppler imaging techniques for evaluating testicular blood flow. J Med Ultrason (2001) 2001;45:443–452.
      1. Gao J, Thai A, Erpelding T. Comparison of superb microvascular imaging to conventional color Doppler ultrasonography in depicting renal cortical microvasculature. Clin Imaging 2019;58:90–95.
      1. Ayaz E, Aslan A, İnan İ, Yıkılmaz A. Evaluation of ovarian vascularity in children by using the “superb microvascular imaging” ultrasound technique in comparison with conventional Doppler ultrasound techniques. J Ultrasound Med 2019;38:2751–2760.
      1. Ma X, Li Y, Jia H, Zhang J, Wang G, Liu X, et al. Contrast-enhanced ultrasound in the diagnosis of patients suspected of having active Crohn’s disease: meta-analysis. Ultrasound Med Biol 2015;41:659–668.
      1. Serafin Z, Białecki M, Białecka A, Sconfienza LM, Kłopocka M. Contrast-enhanced ultrasound for detection of Crohn’s disease activity: systematic review and meta-analysis. J Crohns Colitis 2016;10:354–362.
      1. Socaciu M, Ciobanu L, Diaconu B, Hagiu C, Seicean A, Badea R. Non-invasive assessment of inflammation and treatment response in patients with Crohn’s disease and ulcerative colitis using contrast-enhanced ultrasonography quantification. J Gastrointestin Liver Dis 2015;24:457–465.
      1. Smajerova M, Petrasova H, Little J, Ovesna P, Andrasina T, Valek V, et al. Contrast-enhanced ultrasonography in the evaluation of incidental focal liver lesions: a cost-effectiveness analysis. World J Gastroenterol 2016;22:8605–8614.
      1. Girlich C, Schacherer D, Jung EM, Klebl F, Huber E. Comparison between quantitative assessment of bowel wall vascularization by contrast-enhanced ultrasound and results of histopathological scoring in ulcerative colitis. Int J Colorectal Dis 2012;27:193–198.
      1. Kucharzik T, Wittig BM, Helwig U, Börner N, Rössler A, Rath S, et al. Use of intestinal ultrasound to monitor Crohn’s disease activity. Clin Gastroenterol Hepatol 2017;15:535–542.e2.
      1. Cosnes J, Cattan S, Blain A, Beaugerie L, Carbonnel F, Parc R, et al. Long-term evolution of disease behavior of Crohn’s disease. Inflamm Bowel Dis 2002;8:244–250.
      1. Calabrese E, Zorzi F, Onali S, Stasi E, Fiori R, Prencipe S, et al. Accuracy of small-intestine contrast ultrasonography, compared with computed tomography enteroclysis, in characterizing lesions in patients with Crohn’s disease. Clin Gastroenterol Hepatol 2013;11:950–955.
      1. Castiglione F, Mainenti PP, De Palma GD, Testa A, Bucci L, Pesce G, et al. Noninvasive diagnosis of small bowel Crohn’s disease: direct comparison of bowel sonography and magnetic resonance enterography. Inflamm Bowel Dis 2013;19:991–998.
      1. Dignass A, Van Assche G, Lindsay JO, Lémann M, Söderholm J, Colombel JF, et al. European Crohn’s and Colitis Organisation (ECCO). The second European evidence-based consensus on the diagnosis and management of Crohn’s disease: current management. J Crohns Colitis 2010;4:28–62.
      1. Nylund K, Jirik R, Mezl M, Leh S, Hausken T, Pfeffer F, et al. Quantitative contrast-enhanced ultrasound comparison between inflammatory and fibrotic lesions in patients with Crohn’s disease. Ultrasound Med Biol 2013;39:1197–1206.
      1. Maconi G, Carsana L, Fociani P, Sampietro GM, Ardizzone S, Cristaldi M, et al. Small bowel stenosis in Crohn’s disease: clinical, biochemical and ultrasonographic evaluation of histological features. Aliment Pharmacol Ther 2003;18:749–756.
      1. Coelho R, Ribeiro H, Maconi G. Bowel thickening in Crohn’s disease: fibrosis or inflammation? Diagnostic ultrasound imaging tools. Inflamm Bowel Dis 2017;23:23–34.
      1. Kratzer W, von Tirpitz C, Mason R, Reinshagen M, Adler G, Möller P, et al. Contrast-enhanced power Doppler sonography of the intestinal wall in the differentiation of hypervascularized and hypovascularized intestinal obstructions in patients with Crohn’s disease. J Ultrasound Med 2002;21:149–157.
      1. Ripollés T, Rausell N, Paredes JM, Grau E, Martínez MJ, Vizuete J. Effectiveness of contrast-enhanced ultrasound for characterisation of intestinal inflammation in Crohn’s disease: a comparison with surgical histopathology analysis. J Crohns Colitis 2013;7:120–128.
      1. Quaia E, De Paoli L, Stocca T, Cabibbo B, Casagrande F, Cova MA. The value of small bowel wall contrast enhancement after sulfur hexafluoride-filled microbubble injection to differentiate inflammatory from fibrotic strictures in patients with Crohn’s disease. Ultrasound Med Biol 2012;38:1324–1332.
      1. Pallotta N, Vincoli G, Montesani C, Chirletti P, Pronio A, Caronna R, et al. Small intestine contrast ultrasonography (SICUS) for the detection of small bowel complications in Crohn’s disease: a prospective comparative study versus intraoperative findings. Inflamm Bowel Dis 2012;18:74–84.
      1. Baumgart DC, Müller HP, Grittner U, Metzke D, Fischer A, Guckelberger O, et al. US-based real-time elastography for the detection of fibrotic gut tissue in patients with stricturing Crohn disease. Radiology 2015;275:889–899.
      1. Serra C, Rizzello F, Pratico’ C, Felicani C, Fiorini E, Brugnera R, et al. Real-time elastography for the detection of fibrotic and inflammatory tissue in patients with stricturing Crohn’s disease. J Ultrasound 2017;20:273–284.
      1. Dillman JR, Stidham RW, Higgins PD, Moons DS, Johnson LA, Keshavarzi NR, et al. Ultrasound shear wave elastography helps discriminate low-grade from high-grade bowel wall fibrosis in ex vivo human intestinal specimens. J Ultrasound Med 2014;33:2115–2123.
      1. Lu C, Merrill C, Medellin A, Novak K, Wilson SR. Bowel ultrasound state of the art: grayscale and Doppler ultrasound, contrast enhancement, and elastography in Crohn disease. J Ultrasound Med 2019;38:271–288.
      1. Vestito A, Marasco G, Maconi G, Festi D, Bazzoli F, Zagari RM. Role of ultrasound elastography in the detection of fibrotic bowel strictures in patients with Crohn’s disease: systematic review and meta-analysis. Ultraschall Med 2019;40:646–654.
      1. Shiotani A, Hata J, Manabe N, Imamura H, Ishii M, Fujita M, et al. Clinical relevance of patency capsule combined with abdominal ultrasonography to detect small bowel strictures. Eur J Gastroenterol Hepatol 2014;26:1434–1438.
      1. Kumar S, Hakim A, Alexakis C, Chhaya V, Tzias D, Pilcher J, et al. Small intestinal contrast ultrasonography for the detection of small bowel complications in Crohn’s disease: correlation with intraoperative findings and magnetic resonance enterography. J Gastroenterol Hepatol 2015;30:86–91.
      1. Maconi G, Sampietro GM, Parente F, Pompili G, Russo A, Cristaldi M, et al. Contrast radiology, computed tomography and ultrasonography in detecting internal fistulas and intra-abdominal abscesses in Crohn’s disease: a prospective comparative study. Am J Gastroenterol 2003;98:1545–1555.
      1. Gasche C, Moser G, Turetschek K, Schober E, Moeschl P, Oberhuber G. Transabdominal bowel sonography for the detection of intestinal complications in Crohn’s disease. Gut 1999;44:112–117.
      1. Panés J, Bouzas R, Chaparro M, García-Sánchez V, Gisbert JP, Martínez de Guereñu B, et al. Systematic review: the use of ultrasonography, computed tomography and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn’s disease. Aliment Pharmacol Ther 2011;34:125–145.
      1. Manabe N, Hata J, Haruma K, Imamura H, Kamada T, Kusunoki H. Active gastrointestinal bleeding: evaluation with contrast-enhanced ultrasonography. Abdom Imaging 2010;35:637–642.
      1. Maconi G, Sampietro GM, Ardizzone S, Cristaldi M, Danelli P, Carsana L, et al. Ultrasonographic detection of toxic megacolon in inflammatory bowel diseases. Dig Dis Sci 2004;49:138–142.
    Cited by
    Crossref 3
    Google Scholar 
    PubMed Central 2
    Scopus 4
    Web of Science 3
    MeSH Terms
    Colitis, Ulcerative
    Constriction, Pathologic
    Contrast Media
    Diagnosis
    Elasticity
    Elasticity Imaging Techniques
    Inflammatory Bowel Diseases*
    Magnetic Resonance Imaging
    Mass Screening
    Rectum
    Ultrasonography*
    Ultrasonography, Doppler
    Metrics
    Share
    Links to
    Figures
    slide
    slide
    slide
    slide
    slide
    slide
    slide
    slide
    slide
    slide
    slide
    slide
    slide

    1 / 13

    ORCID IDs
    PERMALINK