Correlation between computed tomography imaging features of mesenteric fat and inflammatory activity in Crohn’s disease

Introduction

Crohn’s disease (CD) is a chronic nonspecific inflammatory bowel disease (IBD) that can affect any part of the digestive tract. In recent years, this disease has become quite common clinically, with a significant increase in the number of patients (1). Besides the poor prognosis and extremely complex etiology of CD, its postoperative complications and recurrence rate are high, which seriously affects the patients’ quality of life and imposes a heavy economic burden on society. CD diagnosis lacks a single-discipline gold standard and requires combined clinical, imaging, endoscopic, and histopathological evidence. Currently, colonoscopy and mucosal tissue biopsy are routinely used as the major diagnostic methods for clinical assessment of CD disease activity, yet they exhibit notable limitations. First, the invasive nature of endoscopic procedures carries potential risks of procedure-related complications, particularly in patients with severe intestinal inflammation. Second, conventional endoscopy demonstrates restricted diagnostic utility in detecting extra-intestinal manifestations, which frequently accompany intestinal inflammation in CD progression.

Creeping fat (CF) resulting from the inflammatory response associated with CD invading the surrounding intestinal mucosa was once considered a characteristic manifestation of CD. Neuropeptides and adipokines can cause adipose tissue to reshape the intestinal wall and promote fat fibrosis (2). CF is a characteristic lesion structure in the occurrence and development of CD. Although radiologists commonly employ computed CF measurements to quantify active lesion severity and spatial distribution, this methodology faces challenges in achieving standardized interpretation across diverse populations. Substantial variations in visceral and subcutaneous adipose tissue distribution—including regional disparities in gynoid and android fat deposition—demonstrate pronounced interethnic and interindividual heterogeneity (3). These anthropometric variations introduce confounding variables in cross-population comparative analyses.

A recent study has shown that the mesentery is a unique, integral, sheet-like structure that extends continuously from the root to the rectum and duodenum-jejunum curve (4), providing the intestinal tract with the stability and flexibility necessary for partial intestinal peristalsis (5). The mesenteric adipose tissue of CD encasing the diseased bowel is often localized to specific areas of the human trunk (android region of the body) (3), and the good resolution of computed tomography (CT) plain scanning and a variety of post-processing techniques allow for accurate quantitative assessment of adipose tissue changes in the abdomen. CT enhancement is useful for assessing perfusion in diseased tissue; Li et al. (6) showed that patients with active CD CF due to edema and hyperemia had higher iodinated contrast concentrations than other inactive diseases on contrast-enhanced images, and data could be collected non-invasively to monitor disease progression. The current study therefore aimed to explore whether a correlation exists between CD activity and the range of adipose tissue distributed along the mesentery, their mean of CT values, and the changes in mean of ΔCT (difference in Hounsfield units between contrast-enhanced CT and non-contrast CT scans) values after enhancement. Mesenteric adipose tissue was used for quantitative evaluation, and its feasibility in effectively guiding the treatment of CD was analyzed. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2606/rc).

Methods

General information

A total of 47 patients with pathologically confirmed CD (23 mild, 20 moderate, and 4 severe cases) and 25 patients with pathologically confirmed intestinal mucosal inflammation were retrospectively evaluated between May 2021 to March 2025. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board (IRB) of the Tongling Municipal Ethics Review Committee (IRB No. 2024-6) and the requirement for individual consent for this retrospective analysis was waived. Data on patients’ names, hospitalization numbers, clinical manifestations, CT enterography (CTE) images, CD-related colonoscopy, and corresponding pathological examination results were collected.

The inclusion criteria (CD group) were as follows: (I) all patients underwent colonoscopy at Tongling Municipal Hospital and the diagnosis of CD was confirmed; (II) there were no obvious extraintestinal symptoms during the examination; (III) good cooperation ability and no contraindications for enhanced CTE examination.

The inclusion criteria (control group) were as follows: all patients with clinical suspicion of IBD, later confirmed by endoscopy and pathology as common intestinal mucosal inflammation, and the rest of the criteria were the same as in the CD group.

The exclusion criteria were as follows: (I) CTE image motion or respiratory artifacts that prevented reliable diagnosis; (II) the lack of colonoscopy and pathological results; (III) combined extra-gastrointestinal infectious diseases, gastrointestinal tumors, and severe hepatic and renal insufficiency, and so on; (IV) those who had not undergone endoscopy in Tongling Municipal Hospital and those with incomplete relevant information.

Based on the simplified CD activity index (CDAI) score (1), the patients were divided into a moderate-to-severe active CD group (>8 points), a mildly active CD group (5c7 points), and a control group (pathologically confirmed intestinal mucosal inflammation).

CDAI score: according to the patient’s general condition, abdominal pain, and abdominal mass, the score is divided into 0–4 points according to the severity, and the number of diarrhea, extraintestinal conditions, and complications are scored 1 point for each type. A total score ≤4 is the remission stage, 5–7 is the mild active stage, 8–16 is the moderate active stage, and >16 is the severe active stage.

Inspection method

Bowel preparation before examination

Initially, patients fasted for 8 hours before scanning, and oral laxatives were administered to clean the intestine. Thereafter, the intestine was filled via oral administration of 1,600–2,000 mL of 2.5% isotonic mannitol solution (400–500 mL every 15 min for a total of 4 times) 1 hour before scanning. The scan was then performed 10–15 min after the last oral administration of isotonic mannitol solution.

Scanning scheme

Thin-slice multi-slice computed tomography (MSCT) scanning was performed using the Philips INGENUITY CORE 128 CT scanner (Philips Healthcare, Amsterdam, The Netherlands). The specific scanning parameters were set as follows: slice thickness of 1 mm, slice interval of 1 mm, tube voltage of 120 kV, and tube current of 250 mA. Plain CT, contrast-enhanced CT in the arterial phase (32–35 s after contrast agent injection), and contrast-enhanced CT in the venous phase (65–70 s after contrast agent injection) were also conducted. A high-concentration iodine contrast agent was used (350 mg/mL, iopamidol, Zhejiang Hisun Pharmaceutical Co., Ltd., Taizhou, China) with a total injection volume of 1.5–2.0 mL/kg and an injection rate of 3–4 mL/s. After scanning, the images were uploaded to the workstation (Extended Brilliance^TM Workspace, Philips) and then reconstruct using a multi-planar reconstruction (MPR) technique.

Image analysis and quality evaluation

CT and MPR images were independently evaluated by two abdominal radiologists under double-blind conditions: an attending radiologist with 9 years of abdominal radiology diagnostic experience and a chief radiologist with 20 years of abdominal radiology diagnostic experience. Measurements included plain and enhanced ΔCT values of the mesentery at multiple locations (mesenteric root, superior mesenteric artery, inferior mesenteric artery, lesion site, and adjacent branch vascular spaces), wall thickening degree in the diseased segment, and corresponding CT values. Intraclass correlation coefficients (ICCs) were calculated to assess interobserver concordance for these quantitative metrics. For evaluations of mural stratification, mesenteric CF index (MCFI), and bowel stenosis, the two radiologists reached consensus through joint consultation.

When selecting the region of interest (ROI) of the image, the influence of blood vessels and calcification need to be avoided. The CT values for the abdominal vascular space, mesenteric root (at the duodenal and jejunal junction), adipose tissue around the superior mesenteric artery, and inferior mesenteric artery were measured within 5 mm around the lesion segment and 10 mm outside the lesion segment (Figure 1). When measuring the CT values, the area of the circle was set at about 20 mm², with each part having been measured no less than three times. The collected data were then averaged to reduce errors.

Figure 1 Schematic diagram of the mesenteric adipose tissue measurement site (yellow circles). (A) Lesion of the peri-intestinal space. (B) Lesion of the peri-intestinal vascular space. (C) Mesenteric root fat gap. (D) Fat space around the superior mesenteric artery. (E) Fat space around the inferior mesenteric artery.

Mesenteric fat around the bowel were classified according to the MCFI (7). In particular, normal or the smallest fat package was assigned 1 point, whereas a fat wrapping ranges of ≤25%, 25–50%, 51–75%, and >75% starting from the edge of the mesentery, but limited, were assigned 2, 3–4, 5–6, and 7–8 points, respectively (Figures 2,3).

Figure 2 Female, 26 years old, mildly active CD, CF enveloping range of 25–50% (yellow arrows), CDAI score: 3. CD, Crohn’s disease; CF, creeping fat; CDAI, Crohn’s disease activity index.

Figure 3 Male, 35 years old, moderate-to-severe active CD and a CF enveloping range of 50–75% (yellow arrows). CDAI score: 5 points. CD, Crohn’s disease; CF, creeping fat; CDAI, Crohn’s disease activity index.

Layered enhancement of the intestinal wall: 0 grade mucosal enhancement or uniform enhancement; level 1 layered strengthening (double layer); two-level layered strengthening (three layers) (Figures 4,5).

Figure 4 Female, 25 years old, mildly active CD, intestinal mucosal layer (blue arrow), serosal layer enhancement (yellow arrow). CD, Crohn’s disease.

Figure 5 Male, 35 years old, moderate-to-severe active CD, intestinal mucosal layer (yellow arrow), serosa layer enhanced (blue arrow), submucosa enhancement (red arrow). CD, Crohn’s disease.

Statistical analysis

All statistical analyses were conducted using the software SPSS 25.0 (IBM Corp., Armonk, NY, USA). Categorical variables were presented as frequencies and percentages. Continuous variables with normal distribution were expressed as mean ± standard deviation (SD), whereas non-normally distributed variables were described as median and interquartile range (IQR). Group comparisons were performed using one-way analysis of variance (ANOVA; for normally distributed data) or Kruskal-Wallis H test (for non-normally distributed data), followed by post-hoc Tukey’s test or Dunn’s test for pairwise comparisons, respectively. Kappa agreement and ICC were used to assess interobserver agreement. Categorical variables were compared using the chi-square test or Fisher’s exact test. Multivariable logistic regression analysis was conducted to identify independent predictors of disease severity, with results reported as odds ratios (ORs) and 95% confidence intervals (CIs). Receiver operating characteristic (ROC) curves were generated to evaluate diagnostic performance, and the optimal cutoff value was determined by maximizing the Youden index. The Bonferroni correction was applied to adjust for multiple comparisons. A P value <0.05 was considered significant.

Results

General information

Totals of 47 active CD patients and 25 control patients were included in this study. The quantitative parameters evaluated using ICC were >0.85. The Montreal classification (1) results of 47 patients with CD were as follows: (I) age: 3 cases (6.4%) ≤16 years old, 25 cases (53.2%) aged 17–40 years, and 19 cases (40.4%) over 40 years old; (II) lesion site: 25 segments (53.2%) in the terminal ileum, 2 cases (4.3%) in the colon, and 20 cases (42.5%) in the ileocolon; (III) disease behavior: 31 cases (65.9%) with non-stenosing non-penetrating type, 13 cases (27.7%) with stenosing type, 3 cases (6.4%) with penetrating type, and 6 cases (12.8%) with perianal lesions, including 1 case (2.1%) with anal fistula. The magnetic resonance imaging (MRI) and CT images of one of the patients with a complication of anal fistula and concomitant narrowing of the bowel lumen were included in the analysis (Figure 6).

Figure 6 Female, 25 years old, moderate-to-severe active CD. (A) MRI T2-TSE-SPAIR sequence clearly shows anal fistula (yellow arrows). (B) CT shows mild turbidity in the perianal fat space and fails to show fistulae clearly (yellow arrows). (C) Bowel wall thickening and intestinal stricture, thickness of the bowel wall was approximately 11.5 mm (yellow arrow), and the lesion had a less than 50% narrowing of the bowel lumen and a proximal bowel dilatation of more than 3 cm (blue arrows). CD, Crohn’s disease; CT, computed tomography; MRI, magnetic resonance imaging; SPAIR, spectral attenuated inversion recovery; TSE, turbo spin echo.

The mild group consisted of 23 patients (average age, 36.96±8.35 years; 15 males and 8 females); the moderate-to-severe group consisted of 24 patients (average age of 37.43±9.75 years; 16 males and 8 females); and the control group comprised 25 patients (average age of 40.22±9.16 years; 17 males and 8 females). No significant differences in sex and age were observed between the groups (P>0.05).

Changes in mean of CT values on mesenteric fat scanning in each phase

Significant differences in the CT values for adipose tissue were observed between the plain scan, arterial phase, and venous phase in the mesenteric traveling area (mesenteric root, superior mesenteric artery, inferior mesenteric artery, around the lesion, and vascular space around the lesion; P<0.001, Table 1). The CT values for mesenteric fat in the moderate-to-severe, mild, and control groups increased gradually, with the moderate-to-severe group having the highest density of mesenteric fat.

Amplitude changes in mean of ΔCT values for mesenteric fat enhancement

Differences in CT values for fat density around the mesenteric traveling area in the control, mild, and moderate-to-severe groups were compared. The difference between the arterial phase and plain CT value and the difference between the venous phase and plain CT value were statistically different (P<0.001, Table 2). The ΔCT values for mesenteric fat increased with disease activity. Moreover, the ΔCT values in the venous phase were greater than 10 Hounsfield units (HU), among which those for the lesion site and vascular space around the lesion were the highest (greater than 20 HU).

Diagnosis of active CD by other CT imaging features and serological examinations

There were statistically significant differences in intestinal thickness, mean of ΔCT value in noncontrast-enhanced scan, intestinal stricture, mural stratification, CF score, neutrophils, C-reactive protein, and platelet. Each of these indicators increased with the elevation of CD activity (Table 3).

The correlation between ΔCT values in mesenteric adipose tissue and CT imaging parameters of the lesion segment

A significant positive correlation was observed between ΔCT values in mesenteric adipose tissue and CT imaging parameters of the lesion segment. Notably, the mean ΔCT value measured in the venous phase at the lesion periphery demonstrated strong positive correlations with three key indicators: the mean ΔCT value in the venous phase of the intestinal wall, mural stratification severity, and intestinal wall thickness. All correlation coefficients exceeded 0.6, indicating substantial statistical associations (Table 4).

ROC curve and logistic regression analysis of each indicator for evaluating CD activity

There were statistically significant differences in the diagnosis of CD activity by imaging and serological indicators. The area under the curve (AUC) of the mean of ΔCT in the venous phase of the lesion was the highest (0.964). Logistic step-by-step regression analysis showed that the mean of ΔCT in the venous phase of the lesion was a relevant factor for moderate-to-severe active CD (Figure 7, Tables 5,6).

Figure 7 ROC curves of various indicators for diagnosing the activity of CD. AUC, area under the curve; CD, Crohn’s disease; ΔCT, difference in Hounsfield units between contrast-enhanced CT and non-contrast CT scans; ROC, receiver operating characteristic.

Discussion

Patients with active CD generally experience mesenteric lipid metabolism dysregulation and disorganized arrangement of adipocytes. The mesenteric fat in such patients is abundantly supplied with blood vessels and lymphoid tissues, demonstrating a strong correlation with the extent of surgical resection, the likelihood of postoperative recurrence, and the progression of the inflammatory process (8). Recent studies (9,10) have shown that CD is complex due to mesenteric fat-inflammation interaction with a poor prognosis. Chinese and international studies (11,12) have mostly evaluated the degree of mesenteric hypertrophy based on the ratio of the visceral fat area to the subcutaneous fat area (MFAI) at the third or fourth lumbar vertebra on plain CT. However, this approach is limited by the fact that the measured fat area at a single level does not correspond to the fat volume of the actual diseased intestinal segment and contains various structures, such as the greater omentum and perirenal fat, which prevent the accurate assessment of the degrees of mesenteric fat hypertrophy and active inflammatory response associated with CD at the time of examination (12). In the current study, the mesenteric adipose tissue at different positions within the running area were selected for measurement, which can not only effectively avoid the error between a single level and the overall lesion but also eliminate the influence of irrelevant adipose tissue. Our findings revealed that the inflammatory activity of CD was correlated with mesangial adipose tissue density and coverage. The density of the mesangial adipose tissue not only increased in the lesion and its surrounding vascular space but also changed around the mesenteric root, superior mesenteric artery, and inferior artery. The overall density of the mesenteric adipose tissue in patients with CD was higher than that in the control group. This indicates that CD will lead to the proliferation and hypertrophy of the entire mesenteric adipose tissue, which is similar to the results of Ding et al. (11), who found that single-level mesenteric fat hypertrophy is positively correlated with CD activity. However, the range of CT values to evaluate adipose tissue hypertrophy is further narrowed, and the CT values are also different from those of patients with common intestinal mucosal inflammation.

Quantitative CTE demonstrates superior spatial resolution and diagnostic consistency (13). However, previous studies (7,14-18) have mainly focused on the changes in the lesion itself and its surrounding CF, such as the MCFI (15) and quantitative scoring system (16); however, distinguishing between physiological peri-intestinal fat and CF still remains difficult. Intestinal stenosis and penetrating ulcers often indicate disease progression. In fact, Li et al. (7) found a strong positive correlation between intestinal stenosis and CD activity based on MCFI measurements, with CF playing a key role. The changes in the amplitude of contrast-enhanced CT for mesenteric fat often reflect the blood perfusion of organs and diseased tissues. More inflammatory cell infiltration and fibrosis-like changes occur in the interstitial lesions, accompanied by small vasculitis and small lymphangitis (19). Given the significant differences in the proportion of extracellular matrix (ECM) proteins between the adipose tissues of different individuals, the size and morphology of adipocytes in expanded fat can also vary; however, these specific manifestations still remain unclear (20). To avoid differences in adipose tissue among different individuals, the current study selected changes in CT and ΔCT values for adipose tissue measured at multiple positions along the mesenteric running area, which effectively avoids errors caused by individual differences. In other words, the entire mesentery was used to evaluate the CT value (i.e., the change in the ΔCT value). It was found that the moderate-to-severe activity group showed the greatest changes in ΔCT values for fat around the lesion and along the mesenteric route area (22.66 and 24.02 HU, respectively), followed by the superior mesenteric artery, inferior mesenteric artery, and mesenteric root (14.95, 14.43, and 19.47 HU, respectively). Our findings demonstrate that the degree of mesenteric fat fibrosis and inflammatory response increases with inflammatory activity, exhibiting a strong positive correlation with CT imaging changes of the bowel wall in the lesion segment. Furthermore, these findings indicate that CF not only proliferates around the lesion and adjacent vascular interstitium but may also progress along the mesenteric root, with the degree of encapsulation closely associated with inflammatory activity. Thus, our results may offer a novel mechanism for CF development and a method for clinical assessment of surgical extent in CD and prognostic evaluation.

The range of CF wrapping the intestine indicates the progression of the lesion, which is proportional to the inflammatory activity score, indicating that the higher the CD score in the active phase, the more severe the inflammatory response and integration of the intestinal lesions to the surrounding fat, and the promotion of CF wrapping the intestine. The current study also found that the changes in contrast-enhanced ΔCT values can effectively distinguish CD from other intestinal inflammatory lesions. Among them, the fat density around the lesion and adjacent vascular space showed the greatest change, whereas other intestinal inflammatory lesions involved the adipose tissue around the intestine. Mean ΔCT values less than 10 HU indicated that CD has high specificity for fat invasion around the intestine.

This study analyzed conventional imaging biomarkers and serological markers in CD, revealing their differential diagnostic values in identifying active disease stages. Patients with moderate-to-severe disease activity exhibited more pronounced inflammatory infiltration and more severe microcirculatory impairment compared to other groups, as evidenced by elevated ΔCT values (fat attenuation gradient changes) and increased C-reactive protein levels—findings consistent with other reports (21,22). However, our comparative analysis demonstrated that individual conventional parameters showed inferior diagnostic performance when compared to the quantitative assessment of perienteric fat density alterations through ΔCT measurement. Notably, one case developed an anal fistula complication, wherein MRI precisely delineated the fistulous tract with superior soft tissue contrast compared to CT. The inherent advantages of MRI—including zero ionizing radiation exposure and exceptional soft tissue discrimination—position this modality as a pivotal component in emerging multimodal frameworks for comprehensive CD evaluation.

This study has some limitations. First, it was a single-center retrospective study with a small sample size; the small number of severe CD cases (usually treated at tertiary centers) limits the generalizability. Second, the ROI area of the mesenteric adipose tissue was limited; changes in the density of mesenteric vascular enhancement on contrast-enhanced CT may have a certain impact on the measurement of the CT values of the surrounding adipose tissue. Future quantitative studies with larger samples as well as other techniques (e.g., MRI) may be needed to further clarify our findings.

Conclusions

In the present study, the changes in the CT values, contrast-enhanced ΔCT values, and CF wrapping range for mesenteric adipose tissue in patients with CD were closely associated with CD activity. Thus, changes in such values can be used as a simple and practical index to determine CD activity and identify other IBD, thereby aiding clinical diagnosis and treatment.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2606/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2606/dss

Funding: The study was supported by the City’s Key Research and Development Plan Social Development Field Category (No. 20230203055).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2024-2606/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Institutional Review Board (IRB) of Tongling Municipal Ethics Review Committee (IRB No. 2024-6) and the requirement for individual consent for this retrospective analysis was waived.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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