Intestinal Ultrasonography for Predicting Postoperative Endoscopic Recurrence and Assessing Risk of Intestinal Surgery in Crohn’s Disease—A Systematic Review and Meta-Analysis of Prospective Studies
Abstract
1. Introduction
2. Materials and Methods
2.1. Search Strategy
2.2. Eligibility Criteria
2.3. Outcomes
2.4. Data Extraction
2.5. Risk of Bias
2.6. Statistical Analysis
3. Results
3.1. Study Characteristics
3.2. Any Postoperative Endoscopic Recurrence
3.3. Conventional Endoscopic Recurrence
3.4. Severe Postoperative Endoscopic Recurrence
3.5. Additional Ultrasound Modalities and Factors Potentially Influencing Diagnostic Performance
3.5.1. Oral-Contrast Ultrasonography
3.5.2. Timing of Postoperative IUS
3.5.3. Colour Doppler
3.5.4. Length of Neoterminal Ileal Thickening
3.6. Modified Rutgeerts Classification
3.7. Pre-Operative IUS and Postoperative Outcomes
3.8. Intestinal Ultrasound Findings Associated with Future Intestinal Surgery
3.8.1. Mixed Primary-Resection and Re-Resection Cohorts
3.8.2. Primary Intestinal Resection
3.8.3. Postoperative IUS Predictors of Symptomatic Recurrence
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
| aHR | adjusted hazard ratio |
| anti-TNF | Anti-tumour necrosis factor |
| aOR | adjusted odds ratio |
| AUC | area under the curve |
| AUROC | area under the receiver operating characteristic curve |
| B-mode | brightness mode |
| BUSS | Bowel Ultrasound Score |
| BWCE | bowel-wall contrast enhancement |
| BWF | bowel-wall flow |
| BWP | bowel-wall pattern |
| BWS | bowel-wall stratification |
| BWT | bowel-wall thickness |
| CD | Crohn’s disease |
| CDS | colour Doppler signal |
| CEUS | contrast-enhanced ultrasonography |
| CI | confidence interval |
| CRP | C-reactive protein |
| df | degrees of freedom |
| DOR | diagnostic odds ratio |
| FC | fecal calprotectin |
| FN | false negative |
| FP | false positive |
| FPR | false-positive rate |
| H-FEI | harmonic flash-echo imaging |
| HR | hazard ratio |
| IBUS-SAS | International Bowel Ultrasound Segmental Activity Score |
| ICA | ileocolonic anastomosis |
| i-fat | inflammatory mesenteric fat |
| IQR | interquartile range |
| IUS | intestinal ultrasonography |
| LR+ | positive likelihood ratio |
| LR− | negative likelihood ratio |
| mo | months |
| MRI | magnetic resonance imaging |
| N/n | number |
| N/A | not applicable |
| NR | not reported |
| OCBS | oral-contrast bowel sonography |
| OCUS | oral-contrast ultrasonography |
| OR | odds ratio |
| POCER | Postoperative Crohn’s Endoscopic Recurrence trial |
| PRISMA-DTA | Preferred Reporting Items for Systematic Reviews and Meta-Analyses of Diagnostic Test Accuracy Studies |
| PROSPERO | International Prospective Register of Systematic Reviews |
| QUIPS | Quality In Prognosis Studies |
| QUADAS-2 | Quality Assessment of Diagnostic Accuracy Studies 2 |
| RE | random-effects |
| ROC | receiver operating characteristic |
| SD | standard deviation |
| Se | sensitivity |
| SICUS | small intestine contrast ultrasonography |
| Simple-US | Simple Ultrasound Score |
| Sp | specificity |
| SROC | summary receiver operating characteristic |
| SUS-CD | Simple Ultrasound Score for Crohn’s Disease |
| TA-IUS | transabdominal intestinal ultrasonography |
| TN | true negative |
| TP | true positive |
| y | years |
References
- Dolinger, M.; Torres, J.; Vermeire, S. Crohn’s Disease. Lancet 2024, 403, 1177–1191. [Google Scholar] [PubMed]
- Tsai, L.; Ma, C.; Dulai, P.S.; Prokop, L.J.; Eisenstein, S.; Ramamoorthy, S.L.; Feagan, B.G.; Jairath, V.; Sandborn, W.J.; Singh, S. Contemporary Risk of Surgery in Patients With Ulcerative Colitis and Crohn’s Disease: A Meta-Analysis of Population-Based Cohorts. Clin. Gastroenterol. Hepatol. 2021, 19, 2031–2045.e11. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Peyrin-Biroulet, L.; Loftus, E.V.; Colombel, J.F.; Sandborn, W.J. The Natural History of Adult Crohn’s Disease in Population-Based Cohorts. Am. J. Gastroenterol. 2010, 105, 289–297. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Buisson, A.; Chevaux, J.B.; Allen, P.B.; Bommelaer, G.; Peyrin-Biroulet, L. Review Article: The Natural History of Postoperative Crohn’s Disease Recurrence. Aliment. Pharmacol. Ther. 2012, 35, 625–633. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Ble, A.; Renzulli, C.; Cenci, F.; Grimaldi, M.; Barone, M.; Sedano, R.; Chang, J.; Nguyen, T.M.; Hogan, M.; Zou, G.; et al. The Relationship Between Endoscopic and Clinical Recurrence in Postoperative Crohn’s Disease: A Systematic Review and Meta-Analysis. J. Crohns Colitis 2022, 16, 490–499. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- De Cruz, P.; Kamm, M.A.; Hamilton, A.L.; Ritchie, K.J.; Krejany, E.O.; Gorelik, A.; Liew, D.; Prideaux, L.; Lawrance, I.C.; Andrews, J.M.; et al. Crohn’s Disease Management after Intestinal Resection: A Randomised Trial. Lancet 2015, 385, 1406–1417. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Kucharzik, T.; Taylor, S.; Allocca, M.; Burisch, J.; Ellul, P.; Iacucci, M.; Maaser, C.; Baldin, P.; Bhatnagar, G.; Ben-Horin, S.; et al. ECCO-ESGAR-ESP-IBUS Guideline on Diagnostics and Monitoring of Patients with Inflammatory Bowel Disease: Part 1. J. Crohns Colitis 2025, 19, jjaf106. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Moran, G.W.; Gordon, M.; Sinopolou, V.; Radford, S.J.; Darie, A.M.; Vuyyuru, S.K.; Alrubaiy, L.; Arebi, N.; Blackwell, J.; Butler, T.D.; et al. British Society of Gastroenterology Guidelines on Inflammatory Bowel Disease in Adults: 2025. Gut 2025, 74, s1–s101. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Nguyen, G.C.; Loftus, E.V.; Hirano, I.; Falck–Ytter, Y.; Singh, S.; Sultan, S.; Flamm, S.L.; Lim, J.K.; Rubenstein, J.H.; Smalley, W.E.; et al. American Gastroenterological Association Institute Guideline on the Management of Crohn’s Disease After Surgical Resection. Gastroenterology 2017, 152, 271–275. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Gionchetti, P.; Dignass, A.; Danese, S.; Dias, F.J.M.; Rogler, G.; Lakatos, P.L.; Adamina, M.; Ardizzone, S.; Buskens, C.J.; Sebastian, S.; et al. 3rd European Evidence-Based Consensus on the Diagnosis and Management of Crohn’s Disease 2016: Part 2: Surgical Management and Special Situations. J. Crohns Colitis 2017, 11, 135–149. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Dragoni, G.; Allocca, M.; Myrelid, P.; Noor, N.M.; Hammoudi, N.; Rivière, P.; Panis, Y.; Ferrante, M. Results of the Eighth Scientific Workshop of ECCO: Diagnosing Postoperative Recurrence of Crohn’s Disease After an Ileocolonic Resection With Ileocolonic Anastomosis. J. Crohns Colitis 2023, 17, 1373–1386. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rutgeerts, P.; Geboes, K.; Vantrappen, G.; Beyls, J.; Kerremans, R.; Hiele, M. Predictability of the of Crohn’s Disease Postoperative Course. Gastroenterology 1990, 99, 956–963. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Ma, C.; Gecse, K.B.; Duijvestein, M.; Sandborn, W.J.; Zou, G.; Shackelton, L.M.; Stitt, L.W.; Parker, C.E.; Bossuyt, P.; Löwenberg, M.; et al. Reliability of Endoscopic Evaluation of Postoperative Recurrent Crohn’s Disease. Clin. Gastroenterol. Hepatol. 2020, 18, 2139–2141.e2. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Kucharzik, T.; Wittig, B.M.; Helwig, U.; Börner, N.; Rössler, A.; Rath, S.; Maaser, C.; Naumann, A.; Pelster, G.; Spengler, J.; et al. Use of Intestinal Ultrasound to Monitor Crohn’s Disease Activity. Clin. Gastroenterol. Hepatol. 2017, 15, 535–542.e2. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Gu, P.; Karime, C.; Fleshner, P.; Falloon, K.; Qazi, T.; Ernest-Suarez, K.; Pabla, B.; St-Pierre, J.; Melmed, G.Y.; Damas, O.M.; et al. Intestinal Ultrasound for Monitoring Postoperative Crohn’s Disease: A Review and Visual Atlas. Inflamm. Bowel Dis. 2026, 32, 755–764. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Salameh, J.P.; Bossuyt, P.M.; McGrath, T.A.; Thombs, B.D.; Hyde, C.J.; MacAskill, P.; Deeks, J.J.; Leeflang, M.; Korevaar, D.A.; Whiting, P.; et al. Preferred Reporting Items for Systematic Review and Meta-Analysis of Diagnostic Test Accuracy Studies (PRISMA-DTA): Explanation, Elaboration, and Checklist. BMJ 2020, 370, m2632. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- McInnes, M.D.F.; Moher, D.; Thombs, B.D.; McGrath, T.A.; Bossuyt, P.M.; Clifford, T.; Cohen, J.F.; Deeks, J.J.; Gatsonis, C.; Hooft, L.; et al. Preferred Reporting Items for a Systematic Review and Meta-Analysis of Diagnostic Test Accuracy Studies The PRISMA-DTA Statement. J. Am. Med. Assoc. 2018, 319, 388–396. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Whiting, P.F.; Rutjes, A.W.S.; Westwood, M.E.; Mallett, S.; Deeks, J.J.; Reitsma, J.B.; Leeflang, M.M.G.; Sterne, J.A.C.; Bossuyt, P.M.M. QUADAS-2: A Revised Tool for the Quality Assessment of Diagnostic Accuracy Studies. Ann. Intern. Med. 2011, 155, 529–536. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Hayden, J.A.; Van Der Windt, D.A.; Cartwright, J.L.; Cô, P.; Bombardier, C. Assessing Bias in Studies of Prognostic Factors. Ann. Intern. Med. 2013, 158, 280–286. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Doebler, P. Mada: Meta-Analysis of Diagnostic Accuracy. In CRAN: Contributed Packages; CRAN: Vienna, Austria, 2012. [Google Scholar] [CrossRef] [Scilit]
- Viechtbauer, W. Conducting Meta-Analyses in R with the Metafor Package. J. Stat. Softw. 2010, 36, 1–48. [Google Scholar]
- Sweeting, M.J.; Sutton, A.J.; Lambert, P.C. What to Add to Nothing? Use and Avoidance of Continuity Corrections in Meta-Analysis of Sparse Data. Stat. Med. 2004, 23, 1351–1375. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- DiCandio, G.; Mosca, F.; Campatelli, A.; Bianchini, M.; D’Elia, F.; Dellagiovampaola, C.; DiCandio, F.M.G.; Freeman, M.; Vick, C.; Taylor, K.; et al. Sonographic detection of postsurgical recurrence of Crohn disease. Am. J. Roentgenol. 1986, 146, 523–526. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Andreoli, A.; Cerro, P.; Falasco, G.; Giglio, A.; Prantera, C. Role of Ultrasonography in the Diagnosis of Postsurgical Recurrence of Crohn’s Disease. Am. J. Gastroenterol. 1998, 93, 1117–1121. [Google Scholar] [CrossRef] [PubMed]
- Orlando, A.; Modesto, I.; Castiglione, F.; Scala, L.; Scimeca, D.; Rispo, A.; Teresi, S.; Mocciaro, F.; Criscuoli, V.; Marrone, C.; et al. The Role of Calprotectin in Predicting Endoscopic Post-Surgical Recurrence in Asymptomatic Crohn’s Disease: A Comparison with Ultrasound. Eur. Rev. Med. Pharmacol. Sci. 2006, 10, 17–22. [Google Scholar] [PubMed]
- Rispo, A.; Bucci, L.; Pesce, G.; Sabbatini, F.; Domenico De Palma, G.; Grassia, R.; Compagna, A.; Testa, A.; Castiglione, F. Bowel Sonography for the Diagnosis and Grading of Postsurgical Recurrence of Crohn_s Disease. Inflamm. Bowel Dis. 2006, 12, 486–490. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Biancone, L.; Calabrese, E.; Petruzziello, C.; Onali, S.; Caruso, A.; Palmieri, G.; Sica, G.S.; Pallone, F. Wireless Capsule Endoscopy and Small Intestine Contrast Ultrasonography in Recurrence of Crohn’s Disease. Inflamm. Bowel Dis. 2007, 13, 1256–1265. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Castiglione, F.; Bucci, L.; Pesce, G.; de Palma, G.D.; Camera, L.; Cipolletta, F.; Testa, A.; Diaferia, M.; Rispo, A. Oral Contrast-Enhanced Sonography for the Diagnosis and Grading of Postsurgical Recurrence of Crohn’s Disease. Inflamm. Bowel Dis. 2008, 14, 1240–1245. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Calabrese, E.; Petruzziello, C.; Onali, S.; Condino, G.; Zorzi, F.; Pallone, F.; Biancone, L. Severity of Postoperative Recurrence in Crohn’s Disease: Correlation between Endoscopic and Sonographic Findings. Inflamm. Bowel Dis. 2009, 15, 1635–1642. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Paredes, J.M.; Ripollés, T.; Cortés, X.; Reyes, M.D.; López, A.; Martínez, M.J.; Moreno-Osset, E. Non-Invasive Diagnosis and Grading of Postsurgical Endoscopic Recurrence in Crohn’s Disease. Usefulness of Abdominal Ultrasonography and 99mTc-Hexamethylpropylene Amineoxime-Labelled Leucocyte Scintigraphy. J. Crohns Colitis 2010, 4, 537–545. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Pallotta, N.; Giovannone, M.; Pezzotti, P.; Gigliozzi, A.; Barberani, F.; Piacentino, D.; Hassan, N.A.; Vincoli, G.; Tosoni, M.; Covotta, A.; et al. Ultrasonographic Detection and Assessment of the Severity of Crohn’s Disease Recurrence after Ileal Resection. BMC Gastroenterol. 2010, 10, 69. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Onali, S.; Calabrese, E.; Petruzziello, C.; Zorzi, F.; Sica, G.S.; Lolli, E.; Ascolani, M.; Condino, G.; Pallone, F.; Biancone, L. Endoscopic vs Ultrasonographic Findings Related to Crohn’s Disease Recurrence: A Prospective Longitudinal Study at 3 years. J. Crohns Colitis 2010, 4, 319–328. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Paredes, J.M.; Ripollés, T.; Cortés, X.; Moreno, N.; Martínez, M.J.; Bustamante-Balén, M.; Delgado, F.; Moreno-Osset, E. Contrast-Enhanced Ultrasonography: Usefulness in the Assessment of Postoperative Recurrence of Crohn’s Disease. J. Crohns Colitis 2013, 7, 192–201. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Onali, S.; Calabrese, E.; Petruzziello, C.; Lolli, E.; Ascolani, M.; Ruffa, A.; Sica, G.; Rossi, A.; Chiaramonte, C.; Pallone, F.; et al. Post-Operative Recurrence of Crohn’s Disease: A Prospective Study at 5 Years. Dig. Liver Dis. 2016, 48, 489–494. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Allocca, M.; Fiorino, G.; Bonifacio, C.; Furfaro, F.; Gilardi, D.; Argollo, M.; Peyrin-Biroulet, L.; Danese, S. Comparative Accuracy of Bowel Ultrasound versus Magnetic Resonance Enterography in Combination with Colonoscopy in Assessing Crohn’s Disease and Guiding Clinical Decision-Making. J. Crohns Colitis 2018, 12, 1280–1287. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Martínez, M.J.; Ripollés, T.; Paredes, J.M.; Moreno-Osset, E.; Pazos, J.M.; Blanc, E. Intravenous Contrast-Enhanced Ultrasound for Assessing and Grading Postoperative Recurrence of Crohn’s Disease. Dig. Dis. Sci. 2019, 64, 1640–1650. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- MacEdo, C.P.; Sarmento Costa, M.; Gravito-Soares, E.; Gravito-Soares, M.; Ferreira, A.M.; Portela, F.; Figueiredo, P. Role of Intestinal Ultrasound in the Evaluation of Postsurgical Recurrence in Crohn’s Disease: Correlation with Endoscopic Findings. GE Port. J. Gastroenterol. 2022, 29, 178–186. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Dragoni, G.; Gottin, M.; Innocenti, T.; Lynch, E.N.; Bagnoli, S.; Macrì, G.; Bonanomi, A.G.; Orlandini, B.; Rogai, F.; Milani, S.; et al. Correlation of Ultrasound Scores with Endoscopic Activity in Crohn’s Disease: A Prospective Exploratory Study. J. Crohns Colitis 2023, 17, 1387–1394. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Furfaro, F.; D’Amico, F.; Zilli, A.; Craviotto, V.; Aratari, A.; Bezzio, C.; Spinelli, A.; Gilardi, D.; Radice, S.; Saibeni, S.; et al. Noninvasive Assessment of Postoperative Disease Recurrence in Crohn’s Disease: A Multicenter, Prospective Cohort Study on Behalf of the Italian Group for Inflammatory Bowel Disease. Clin. Gastroenterol. Hepatol. 2023, 21, 3143–3151. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Castiglione, F.; De Sio, I.; Cozzolino, A.; Rispo, A.; Manguso, F.; Blanco, G.D.V.; Di Girolamo, E.; Castellano, L.; Ciacci, C.; Mazzacca, G. Bowel Wall Thickness at Abdominal Ultrasound and the One-Year-Risk of Surgery in Patients with Crohn’s Disease. Am. J. Gastroenterol. 2004, 99, 1977–1983. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rispo, A.; Imperatore, N.; Testa, A.; Bucci, L.; Luglio, G.; De Palma, G.D.; Rea, M.; Nardone, O.M.; Caporaso, N.; Castiglione, F. Combined Endoscopic/Sonographic-Based Risk Matrix Model for Predicting One-Year Risk of Surgery: A Prospective Observational Study of a Tertiary Centre Severe/Refractory Crohn’s Disease Cohort. J. Crohns Colitis 2018, 12, 784–793. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Madsen, G.R.; Attauabi, M.; Ilvemark, J.F.K.F.; Theede, K.; Bjerrum, J.T.; Bendtsen, F.; Seidelin, J.B.; Wilkens, R.; Boysen, T.; Burisch, J. Intestinal Ultrasound Findings and Their Prognostic Value in Early Crohn’s Disease: A Copenhagen IBD Cohort Study. Clin. Gastroenterol. Hepatol. 2025, 23, 1398–1407.e6. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rigazio, C.; Ercole, E.; Laudi, C.; Daperno, M.; Lavagna, A.; Crocellà, L.; Bertolino, F.; Viganò, L.; Sostegni, R.; Pera, A.; et al. Abdominal Bowel Ultrasound Can Predict the Risk of Surgery in Crohn’s Disease: Proposal of an Ultrasonographic Score. Scand. J. Gastroenterol. 2009, 44, 585–593. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Castiglione, F.; Imperatore, N.; Testa, A.; De Palma, G.D.; Nardone, O.M.; Pellegrini, L.; Caporaso, N.; Rispo, A. One-Year Clinical Outcomes with Biologics in Crohn’s Disease: Transmural Healing Compared with Mucosal or No Healing. Aliment. Pharmacol. Ther. 2019, 49, 1026–1039. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Allocca, M.; Craviotto, V.; Bonovas, S.; Furfaro, F.; Zilli, A.; Peyrin-Biroulet, L.; Fiorino, G.; Danese, S. Predictive Value of Bowel Ultrasound in Crohn’s Disease: A 12-Month Prospective Study. Clin. Gastroenterol. Hepatol. 2022, 20, e723–e740. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Kunihiro, K.; Hata, J.; Manabe, N.; Mitsuoka, Y.; Tanaka, S.; Haruma, K.; Chayama, K. Predicting the Need for Surgery in Crohn’s Disease with Contrast Harmonic Ultrasound. Scand. J. Gastroenterol. 2007, 42, 577–585. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Maconi, G.; Sampietro, G.M.; Cristaldi, M.; Danelli, P.; Russo, A.; Porro, G.B.; Taschieri, A.M. Preoperative Characteristics and Postoperative Behavior of Bowel Wall on Risk of Recurrence After Conservative Surgery in Crohn’s Disease A Prospective Study. Ann. Surg. 2001, 233, 345–352. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Parente, F.; Sampietro, G.M.; Molteni, M.; Greco, S.; Anderloni, A.; Sposito, C.; Danelli, P.G.; Taschieri, A.M.; Gallus, S.; Bianchi Porro, G. Behaviour of the Bowel Wall during the First Year after Surgery Is a Strong Predictor of Symptomatic Recurrence of Crohn’s Disease: A Prospective Study. Aliment. Pharmacol. Ther. 2004, 20, 959–968. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Abu Halimah, J.; Alkhalifa, A.H.; Alqurashi, R.H.; Alahmadi, F.B.; Almousa, S.A.; Qarn, F.M.; Alshamrani, F.M.; Alanazi, F.N.; Balhareth, M.A.; Alghthy, A.M.; et al. Diagnostic Accuracy of Intestinal Ultrasound for Detecting Postoperative Recurrence in Crohn’s Disease: A Systematic Review. Cureus 2026, 18, e108712C. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Zhu, C.; Ma, X.; Xue, L.; Xu, J.; Li, Q.; Wang, Y.; Zhang, J. Small Intestine Contrast Ultrasonography for the Detection and Assessment of Crohn Disease: A Meta-Analysis. Medicine 2016, 95, e4235. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Samnani, S.; Ray, C.M.; Gill, P.; Stein, L.; Buhler, K.A.; Leong, R.W.; Smith, R.L.; De Cruz, P.; Kaplan, G.G.; Seow, C.H.; et al. Diagnostic Accuracy of Noninvasive Biomarkers and Imaging for Evaluating Postoperative Recurrence in Crohn’s Disease. Clin. Gastroenterol. Hepatol. 2025, 23, 2433–2447.e9. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Ananthakrishnan, A.N.; Adler, J.; Chachu, K.A.; Nguyen, N.H.; Siddique, S.M.; Weiss, J.M.; Sultan, S.; Velayos, F.S.; Cohen, B.L.; Singh, S. AGA Clinical Practice Guideline on the Role of Biomarkers for the Management of Crohn’s Disease. Gastroenterology 2023, 165, 1367–1399. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Ma, C.; Albashir, S.; Allocca, M.; de Buck van Overstraeten, A.; Kotze, P.G.; Lu, C.; Maaser, C.; Maconi, G.; Panaccione, R.; Regueiro, M.; et al. Intestinal Ultrasound to Detect Postoperative Recurrence in Patients with Crohn’s Disease: An International, Multidisciplinary, RAND/UCLA Appropriateness Method Study. Lancet Gastroenterol. Hepatol. 2026, 11, 602–615. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Maaser, C.; Sturm, A.; Vavricka, S.R.; Kucharzik, T.; Fiorino, G.; Annese, V.; Calabrese, E.; Baumgart, D.C.; Bettenworth, D.; Borralho Nunes, P.; et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial Diagnosis, Monitoring of Known IBD, Detection of Complications. J. Crohns Colitis 2019, 13, 144–164. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Jairath, V.; Vuyyuru, S.K.; Zou, G.; Ma, C.; Neustifter, B.; Agboton, C.; Romo Bautista, I.; Allocca, M.; An, Y.K.; Begun, J.; et al. Evaluating Treatment to a Target of Transmural Healing in Patients with Moderately to Severely Active Crohn’s Disease: Rationale, Design and Protocol for the Randomised Controlled VECTORS Trial. BMJ Open Gastroenterol. 2026, 13, e002088c. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Bak, M.T.J.; ten Bokkel Huinink, S.; Erler, N.S.; Bodelier, A.G.L.; Dijkstra, G.; Romberg-Camps, M.; de Boer, N.K.H.; Hoentjen, F.; Stassen, L.P.S.; van der Meulen–de Jong, A.E.; et al. Prognostic Value of the Modified Rutgeerts Score for Long-Term Outcomes After Primary Ileocecal Resection in Crohn’s Disease. Am. J. Gastroenterol. 2024, 119, 306–312. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Rivière, P.; Pekow, J.; Hammoudi, N.; Wils, P.; De Cruz, P.; Wang, C.P.; Mañosa, M.; Ollech, J.; Allez, M.; Nachury, M.; et al. Comparison of the Risk of Crohn’s Disease Postoperative Recurrence between Modified Rutgeerts Score I2a and I2b Categories: An Individual Patient Data Meta-Analysis. J. Crohns Colitis 2023, 17, 269–276. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- van der Does de Willebois, E.M.L.; Bellato, V.; Duijvestein, M.; van Dieren, S.; Danese, S.; Sileri, P.; Buskens, C.J.; Vignali, A.; Bemelman, W.A. How Reliable Is Endoscopic Scoring of Postoperative Recurrence in Crohn Disease?: A Systematic Review and Meta-Analysis. Ann. Surg. Open 2024, 5, e397. [Google Scholar] [CrossRef] [Scilit] [PubMed]
- Parra-Izquierdo, V.; Frías Ordoñez, J.S.; Eggermont, E.; Verstockt, B. Intestinal Ultrasound for the Detection of Postoperative Recurrence in Crohn’s Disease: A Systematic Review and Meta-Analysis. J. Crohns Colitis 2026, 20, jjag094c. [Google Scholar] [CrossRef] [Scilit] [PubMed]






| Abbreviations: Study, Year (Ref.) | N Centres | Patients, n | Type of IUS | Time from Surgery to IUS | Time Between IUS and Endoscopy | Evaluated IUS Parameters and Cut-Offs | Reference Standard and Outcome Definition | Study Findings |
|---|---|---|---|---|---|---|---|---|
| DiCandio et al. 1986 [23] | 1 | 32 | Conventional IUS | Mean 4.5 years (range, 1–12) | ≤2 weeks | Ileocolonic BWT > 5.0 mm; wall architecture; complications | Contrast radiography plus endoscopy/biopsy; postoperative relapse; no Rutgeerts classification | Se 0.82; Sp 1.00; accuracy 0.94 |
| Andreoli et al. 1998 [24] | 1 | 41 | Conventional IUS | Mean 35.4 months (range, 3–105) | ≤14 days | Neoterminal-ileal BWT > 5.0 mm | Ileocolonoscopy; typical lesions in the neoterminal ileum and/or ICA; Rutgeerts-derived mild, moderate, and severe grading | Se 0.81; Sp 0.86; accuracy 0.83 |
| Orlando et al. 2006 [25] | 2 | 50 | Conventional IUS | 3 months | 9-month forward-prediction interval; endoscopy at 12 mo | BWT ≥ 5.0 mm | Ileocolonoscopy at 12 months; Rutgeerts ≥ i2, defined as ≥5 aphthous lesions | Se 0.26; Sp 0.90 |
| Rispo et al. 2006 [26] | 1 | 45 | Conventional IUS | 12 months | ≤7 days | Neoterminal-ileal/ICA BWT > 3.0 mm; BWT > 5.0 mm for severe recurrence | Ileocolonoscopy; original Rutgeerts ≥ i1; severe recurrence i3–i4 | Any recurrence: Se 0.79, Sp 0.95; severe recurrence: Se 0.94, Sp 1.00 |
| Biancone et al. 2007 [27] | 1 | 22 | Oral-contrast IUS | 12 months; subgroup assessed at 3, 6, and 12 months | Sequential same-visit assessment at 12 months | Perianastomotic/neoterminal-ileal BWT > 3.0 mm; stiff loop; dilatation > 2.5 cm; stricture < 1 cm; fistula; abscess | Ileocolonoscopy; original Rutgeerts ≥ i1; secondary analysis restricted to the neoterminal ileum | Se 1.00; Sp 0.00; IUS was positive in 4/10, 8/10, and 10/10 patients at 3, 6, and 12 mo, respectively |
| Castiglione et al. 2008 [28] | 1 | 40 | Conventional IUS and oral-contrast IUS | 12 months | ≤7 days | ICA/neoterminal-ileal BWT ≥ 3.0 mm; severe recurrence: conventional-IUS BWT ≥ 5.0 mm or oral-contrast-IUS BWT ≥ 4.0 mm | Ileocolonoscopy; original Rutgeerts ≥ i1; severe recurrence i3–i4 | Conventional IUS: Se 0.77, Sp 0.94; oral-contrast IUS: Se 0.82, Sp 0.94. Severe recurrence: conventional IUS: Se 0.93, Sp 0.96; oral-contrast IUS: Se 0.86, Sp 0.96 |
| Calabrese et al. 2009 [29] | 1 | 72 | Oral-contrast IUS | Median 18 months (range, 3–396) | ≤6 months; clinically active subgroup median 1 month | Perianastomotic BWT > 3.0 mm for ≥4 cm; dilatation > 2.5 cm; stricture < 1 cm; fistula; abscess | Ileocolonoscopy; original Rutgeerts ≥ i1; ordinal analysis of recurrence severity | Se 0.93; Sp 0.20; accuracy 0.88; BWT correlated with Rutgeerts score (r = 0.67) |
| Onali et al. 2010 [32] | 1 | 25 at 1 y; 21 at 2 y; 15 at 3 y | Oral-contrast IUS | 12, 24, and 36 months | At 12 months, ileocolonoscopy followed by IUS; exact interval NR | BWT > 3.0 mm; stiff loop; dilatation > 2.5 cm; stricture < 1 cm; fistula; abscess | Ileocolonoscopy at 1 and 3 years; original Rutgeerts ≥ i1; secondary ≥ i2 analysis | At 1 y: Se 1.00, Sp 0.00; 1-y BWT did not predict clinical recurrence at 2 y (p = 0.19) |
| Pallotta et al. 2010 [31] | 1 | 58 | Oral-contrast IUS | 6 months, 12 months, and every 6–12 months thereafter (range, 6–100 months) | ≤2 weeks; different days and random order | ICA BWT > 3.5 mm; neoterminal-ileal BWT > 3.0 mm and length of thickening; stenosis; dilatation | Ileocolonoscopy; original Rutgeerts 0 versus 1–4 and ordinal categories 0, 1, and ≥i2 | ICA BWT > 3.5 mm detected all endoscopic lesions; ICA BWT combined with lesion length yielded AUC 0.95 |
| Paredes et al. 2010 [30] | 1 | 33 | Conventional IUS and colour Doppler | Mean 87.7 months (SD 75.4) | ≤3 days | Neoterminal-ileal BWT > 3.0 mm and/or positive colour Doppler; moderate/severe recurrence: BWT > 5.0 mm and/or Doppler grade 2–3 | Ileocolonoscopy; original Rutgeerts ≥ i1; moderate/severe recurrence i3–i4 | Any recurrence: Se 0.77, Sp 0.57; moderate/severe recurrence: Se 0.80, Sp 0.78 |
| Paredes et al. 2013 [33] | 1 | 60 | Conventional IUS, colour Doppler and CEUS | 60 mo (SD 71) | ≤3 days | Neoterminal-ileal BWT > 3.0 mm and/or positive colour Doppler; score 2: BWT > 5.0 mm or BWCE > 46%; score 3: BWT > 5.0 mm or BWCE > 70% or fistula | Ileocolonoscopy; original Rutgeerts ≥ i1; moderate/severe recurrence i3–i4 | Conventional IUS: Se 0.90, Sp 0.82; score 2: Se 0.98, Sp 1.00; score 3: Se 0.94, Sp 0.73 |
| Onali et al. 2016 [34] | 1 | 40 | Oral-contrast IUS | 12 months | NR | Perianastomotic/neoterminal-ileal BWT ≥ 3.0 mm | Ileocolonoscopy; original Rutgeerts ≥ i1 and secondary ≥ i2 analysis; clinical recurrence assessed through 5 years | IUS and endoscopy each identified recurrence in 39/40 patients; 1-y IUS did not discriminate clinical recurrence |
| Allocca et al. 2018 [35] | 1 | 60 | Conventional IUS and Power Doppler | NR | ≤3 days | BWT > 3.0 mm; BWP; BWF; ulcers; strictures; fistulas; abscesses; lymph nodes; mesenteric hypertrophy | Ileocolonoscopy; modified Rutgeerts ≥ i2b in the postoperative subgroup | Recurrence occurred in 6/17 postoperative patients; postoperative-specific Se and Sp were NR |
| Martínez et al. 2019 [36] | 1 | 108 | Conventional IUS, colour Doppler and CEUS | Mean 6 years (range, 3 months–30 years) | Median 1 month 28 days (range, 0–86 days) | ICA/neoterminal-ileal BWT ≥ 3.0 mm; BWCE ≥ 46%; severe recurrence BWT ≥ 5.0 mm; severe model: BWT ≥ 6.0 mm or BWT 5–6 mm plus BWCE ≥ 70% or complications | Ileocolonoscopy; original Rutgeerts ≥ i1; severe recurrence i3–i4 | BWT ≥ 3.0 mm: accuracy 0.91; BWT plus BWCE: Se 0.91, Sp 0.89; severe model: Se 0.90, Sp 0.87 |
| Macedo et al. 2022 [37] | 1 | 39 | Conventional IUS and Power Doppler | Median 9 years (IQR, 3–12) | Same day; IUS performed first | BWT at the thickest ileocolic segment; abnormal IUS: BWT > 3.0 mm and/or Limberg > 1; ROC-derived BWT ≥ 3.9 mm | Ileocolonoscopy; original Rutgeerts ≥ i2 | Composite IUS: Se 0.89, Sp 0.62; BWT ≥ 3.9 mm: Se 0.89, Sp 0.71; IUS severity AUC 0.82 |
| Dragoni et al. 2023 [38] | 1 | 73 | Conventional IUS and colour Doppler | NR | Median 3 weeks (IQR, 2–5); maximum 6 weeks | IBUS-SAS; BUSS; Simple-US; SUS-CD; BWT; CDS; BWS; i-fat | Ileocolonoscopy; modified Rutgeerts ≥ i2b; severe recurrence i4 | Correlations with Rutgeerts score were ρ = 0.88 for IBUS-SAS, 0.84 for BUSS, 0.84 for Simple-US, and 0.78 for SUS-CD |
| Furfaro et al. 2023 [39] | 3 | 91 | Conventional IUS and colour Doppler | Within 1 y; exact IUS timing NR; endoscopy median 6.5 months (range, 4–12) | ≤90 days | Neoterminal-ileal/ICA BWT ≥ 3.0 mm; mesenteric lymph nodes; FC ≥ 50 μg/g | Ileocolonoscopy; original Rutgeerts ≥ i2 | BWT ≥ 3.0 mm: Se 0.77, Sp 0.65; BWT plus FC using an AND rule: Se 0.65, Sp 0.93; lymph nodes: Se 0.35, Sp 0.97; BWT per 1 mm increase: aOR 2.43 |
| Abbreviations: Study, Year (Ref.) | N Centres | Patients, n | Type of IUS | Time from Surgery to IUS | Time Between IUS and Endoscopy | Evaluated IUS Parameters and Cut-Offs | Reference Standard and Outcome Definition | Study Findings |
|---|---|---|---|---|---|---|---|---|
| Panel A: Postoperative longitudinal prognostic studies | ||||||||
| Maconi et al. 2001 [47] | 1 | 85 | Conventional IUS | Pre-operative and 6 months postoperative, then every 6 months; median follow-up 28.4 months (range 3–70) | N/A | maximum BWT; length of thickening; wall pattern; BWT ≥ 4.0 mm | Clinical recurrence requiring medium- or high-dose corticosteroids; surgical recurrence requiring a new procedure | Unchanged/worsened 6-mo BWT predicted clinical recurrence (aHR 9.98) and surgical recurrence (aHR 16.15); greater pre-operative disease length was associated with surgery |
| Parente et al. 2004 [48] | 1 | 127 | Conventional IUS | Pre-Operative, 6 months, 12 months, and annually thereafter, median follow-up 41.0 months | N/A | BWT ≥ 4.0 mm; 12-mo BWT > 6.0 mm | Symptomatic recurrence requiring systemic corticosteroids | Unchanged/worsened 12-mo BWT predicted symptomatic recurrence (aHR 8.90); BWT > 6.0 mm was also predictive (aHR 6.50) |
| Panel B: Studies evaluating future intestinal surgery in broader Crohn’s disease populations | ||||||||
| Castiglione et al. 2004 [40] | 1 | 174 | Conventional IUS | NR | N/A | BWT > 7.0 mm | Intestinal resection within 12 months | BWT > 7.0 mm: Se 0.88; Sp 0.78; AUC 0.83; aOR 19.52 |
| Kunihiro et al. 2007 [46] | 1 | 70 | Conventional IUS and H-FEI | N/A | N/A | BWT ≥ 4.0 mm; loss of BWS; H-FEI echo intensity > 40 | Bowel resection within 3 months | Loss of BWS: aOR 5.98; H-FEI echo intensity: OR 1.02 per unit; combined rule: Se 0.52, Sp 0.91 |
| Rigazio et al. 2009 [43] | 1 | 147 | Conventional IUS | N/A | N/A | BWT > 4.5 mm; disrupted BWS; fistula/abscess; stenosis; composite IUS score | Actual intestinal surgery within 30 days; controls remained surgery-free for ≥1 year | BWT > 4.5 mm: Se 0.92, Sp 0.52, OR 12.21; disrupted BWS: OR 16.24; composite score correctly classified 84% of patients |
| Rispo et al. 2018 [41] | 1 | 100 | Conventional IUS | N/A | ≤1 week | BWT ≥ 7.0 mm; small-bowel disease extent ≥ 33 cm; complications | Major intestinal surgery within 12 months; minor and perianal procedures excluded | BWT ≥ 7.0 mm: Se 0.67, Sp 0.87, AUC 0.87, aOR 15.80; risk-matrix probabilities ranged from 0.48% to 87.5% |
| Castiglione et al. 2019 [44] | 1 | 218 | Conventional IUS | N/A; baseline after 2 y of anti-TNF therapy | ≤1 week | Transmural healing: BWT ≤ 3.0 mm in all affected segments; mucosal healing only; no healing | CD-related surgery within 12 months; major intestinal resection/colectomy and minor procedures included | Surgery occurred in 0%, 10.0%, and 35.5% of patients with transmural, mucosal-only, and no healing, respectively; HR 0.94 versus mucosal healing |
| Allocca et al. 2022 [45] | 1 | 225 | Conventional IUS and Power Doppler | N/A; baseline before 12-mo follow-up | 3 days–3 months | BWT ≤ 3.0 mm; BWF; BWP; complications; BUSS > 3.52 | Individual need for surgery within 12 mo; composite adverse disease course also assessed | Surgery occurred in 13.7% with baseline complications versus 1.7% without; complications independently predicted surgery (aOR 7.56); BUSS was not independently predictive of surgery |
| Madsen et al. 2025 [42] | 2 | 201 | Conventional IUS and colour Doppler | N/A; baseline at diagnosis, median 5 days after diagnosis (IQR, 0–22) | NR | Terminal-ileal IBUS-SAS; BWT; CDS; BWS; i-fat; cut-offs: IBUS-SAS 63 and BWT 5.0 mm | Ileocecal resection within 12 months of diagnosis | IBUS-SAS 63: AUC 0.92, Se 1.00, Sp 0.73; BWT 5.0 mm: AUC 0.87, Se 1.00, Sp 0.69 |
| Endoscopic Outcome and Index-Test Group | Studies, n | Patients, n | TP | FN | FP | TN | Bivariate Sensitivity, 95% CI | Bivariate Specificity, 95% CI | LR+, 95% CI | LR−, 95% CI | DOR, 95% CI | AUC, 95% CI | Heterogeneity |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Any postoperative endoscopic recurrence (original Rutgeerts ≥ i1); conventional transabdominal IUS with study-defined BWT > 3.0 mm, with or without colour Doppler | 5 | 286 | 185 | 26 | 12 | 63 | 0.85 (0.75–0.92) | 0.83 (0.65–0.92) | 5.27 (2.5010.50) | 0.19 (0.10–0.30) | 30.80 (10.60–70.70) | 0.91 (0.75–0.93) | I2 = 0.00%; τ2 = 0.00 |
| Conventional postoperative endoscopic recurrence (original Rutgeerts ≥ i2); conventional transabdominal IUS with study-defined BWT ≥ 3.0 or ≥ 3.9 mm | 2 | 130 | 62 | 16 | 17 | 35 | 0.79 (0.68–0.87) | 0.67 (0.53–0.79) | 2.47 (1.64–3.71) | 0.33 (0.19–0.50) | 8.31 (3.42–17.00) | 0.76 (0.76–0.78) | I2 = 29.46%; τ2 = 0.22 |
| Severe postoperative endoscopic recurrence (original Rutgeerts i3–i4); conventional transabdominal IUS with study-defined BWT > 5.0 or ≥ 5.0 mm | 4 | 246 | 101 | 26 | 18 | 101 | 0.79 (0.70–0.85) | 0.81 (0.72–0.88) | 4.29 (2.79–6.49) | 0.27 (0.19–0.37) | 16.80 (8.12–30.90) | 0.86 (0.80–0.94) | I2 = 79.21%; τ2 = 5.71 |
| Any postoperative endoscopic recurrence (original Rutgeerts ≥ i1); oral-contrast ultrasonography with study-defined BWT around 3.0 mm, with or without ancillary findings | 5 | 199 | 164 | 9 | 7 | 19 | 0.93 (0.84–0.97) | 0.52 (0.14–0.87) | 2.43 (1.10–6.89) | 0.17 (0.07–0.42) | 18.70 (2.75–66.10) | 0.91 (0.52–0.95) | I2 = 72.46%; τ2 = 3.72 |
| BWT ≥ 7.0 mm and intestinal surgery within one year | 2 | 274 | 66 | 16 | 36 | 156 | 19.70 (9.80–39.70) | I2 = 0.00%; τ2 = 0.00 |
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Alramahy, M.A.; Alramahy, B.A.; Seidelin, J.B.; Wetwittayakhlang, P.; Bjerrum, J.T.; Attauabi, M. Intestinal Ultrasonography for Predicting Postoperative Endoscopic Recurrence and Assessing Risk of Intestinal Surgery in Crohn’s Disease—A Systematic Review and Meta-Analysis of Prospective Studies. J. Clin. Med. 2026, 15, 7024. https://doi.org/10.3390/jcm15187024
Alramahy MA, Alramahy BA, Seidelin JB, Wetwittayakhlang P, Bjerrum JT, Attauabi M. Intestinal Ultrasonography for Predicting Postoperative Endoscopic Recurrence and Assessing Risk of Intestinal Surgery in Crohn’s Disease—A Systematic Review and Meta-Analysis of Prospective Studies. Journal of Clinical Medicine. 2026; 15(18):7024. https://doi.org/10.3390/jcm15187024
Chicago/Turabian StyleAlramahy, Murtaja Ahmad, Batol Ahmad Alramahy, Jakob Benedict Seidelin, Panu Wetwittayakhlang, Jacob Tveiten Bjerrum, and Mohamed Attauabi. 2026. "Intestinal Ultrasonography for Predicting Postoperative Endoscopic Recurrence and Assessing Risk of Intestinal Surgery in Crohn’s Disease—A Systematic Review and Meta-Analysis of Prospective Studies" Journal of Clinical Medicine 15, no. 18: 7024. https://doi.org/10.3390/jcm15187024
APA StyleAlramahy, M. A., Alramahy, B. A., Seidelin, J. B., Wetwittayakhlang, P., Bjerrum, J. T., & Attauabi, M. (2026). Intestinal Ultrasonography for Predicting Postoperative Endoscopic Recurrence and Assessing Risk of Intestinal Surgery in Crohn’s Disease—A Systematic Review and Meta-Analysis of Prospective Studies. Journal of Clinical Medicine, 15(18), 7024. https://doi.org/10.3390/jcm15187024

