Skip to main content
SpringerLink
Log in

The Prevalence of Concomitant Skip Small Bowel Lesions in Crohn’s Disease and Their Effects on Reoperation in Patients Undergoing Ileocolic Resection

  • Original Article
  • Published:
Journal of Gastrointestinal Surgery

Abstract

Aims

Concomitant lesions in the small intestine are common in Crohn’s disease (CD). This study aimed to detect the incidence of small bowel (SB) lesions in patients undergoing surgical resection for symptomatic ileocolic disease and whether concomitant SB lesions are associated with reoperation due to recurrent CD.

Methods

In this observational, historical cohort study, consecutive patients with CD undergoing primary ileocolic resection (ICR) from 2007 to 2019 were included. Clinical variables and intraoperative findings were extracted from a prospectively maintained database and analyzed by Cox proportional hazards regression models for identifying risk factors of reoperation.

Results

Of the 404 patients included, there were 202 (50%) patients having concomitant SB lesions, and 108 of them underwent concurrent surgical intervention for SB lesions whereas 94 did not. The presence of concomitant SB lesions was a risk factor for reoperation (p = 0.041). Subgroup analysis indicated that patients with concomitant uncomplicated SB lesions left in situ had a comparable rate of reoperation (p = 0.605) whereas patients having concomitant complicated SB lesions undergoing simultaneous surgical intervention showed a higher reoperation rate (P = 0.006) when compared with those without concomitant SB lesions. Interestingly, the adverse effects of concomitant SB lesions can be reversed in the setting of postoperative anti-TNF agents [HR 0.2; 95% CI (0.04–0.9); P=0.040].

Conclusions

Concomitant SB lesion(s), especially those complicated lesions, could be a risk factor for postoperative surgical recurrence in patients undergoing ICR. Active postoperative management strategies such as anti-TNF agents should be provided for these patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

Alb:

albumin

anti-TNF:

anti-tumor necrosis factor

AZA:

azathioprine

CD:

Crohn’s disease

CI:

confidence interval

CRP:

C-reactive protein

ESR:

erythrocyte sedimentation rate

HR:

hazard ratio

IBD:

inflammatory bowel disease

ICR:

ileocolic resection

IFX:

infliximab

IQR:

interquartile range

References

  1. N.A. Molodecky, I.S. Soon, D.M. Rabi, W.A. Ghali, M. Ferris, G. Chernoff, E.I. Benchimol, R. Panaccione, S. Ghosh, H.W. Barkema, and G.G. Kaplan. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 142:46-54.e42; quiz e30 (2012).

    Article  PubMed  Google Scholar 

  2. J.J. Zheng, X.S. Zhu, Z. Huangfu, X.H. Shi, and Z.R. Guo. Prevalence and incidence rates of Crohn’s disease in mainland China: a meta-analysis of 55 years of research. J Dig Dis. 11:161-166 (2010).

    Article  PubMed  Google Scholar 

  3. S.K. Murthy, J. Begum, E.I. Benchimol, C.N. Bernstein, G.G. Kaplan, J.D. McCurdy, H. Singh, L. Targownik, and M. Taljaard. Introduction of anti-TNF therapy has not yielded expected declines in hospitalisation and intestinal resection rates in inflammatory bowel diseases: a population-based interrupted time series study. Gut. 69:274-282 (2020).

    Article  PubMed  Google Scholar 

  4. T. Yamamoto. Factors affecting recurrence after surgery for Crohn’s disease. World J Gastroenterol. 11:3971-3979 (2005).

    Article  PubMed  PubMed Central  Google Scholar 

  5. A.D. Frolkis, D.S. Lipton, K.M. Fiest, M.E. Negrón, J. Dykeman, J. deBruyn, N. Jette, T. Frolkis, A. Rezaie, C.H. Seow, R. Panaccione, S. Ghosh, and G.G. Kaplan. Cumulative incidence of second intestinal resection in Crohn’s disease: a systematic review and meta-analysis of population-based studies. The American journal of gastroenterology. 109:1739-1748 (2014).

    Article  PubMed  Google Scholar 

  6. J.T. Unkart, L. Anderson, E. Li, C. Miller, Y. Yan, C.C. Gu, J. Chen, C.D. Stone, S. Hunt, and D.W. Dietz. Risk factors for surgical recurrence after ileocolic resection of Crohn’s disease. Diseases of the colon and rectum. 51:1211-1216 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  7. S. Post, C. Herfarth, E. Böhm, G. Timmermanns, H. Schumacher, G. Schürmann, and M. Golling. The impact of disease pattern, surgical management, and individual surgeons on the risk for relaparotomy for recurrent Crohn’s disease. Annals of surgery. 223:253-260 (1996).

    Article  PubMed  PubMed Central  Google Scholar 

  8. M.H. Wang, J.J. Friton, L.E. Raffals, J.A. Leighton, S.F. Pasha, M.F. Picco, K. Monroe, B.D. Nix, R.D. Newberry, and W.A. Faubion. Novel Genetic Variant Predicts Surgical Recurrence Risk in Crohn’s Disease Patients. Inflammatory bowel diseases. 27:1968-1974 (2021).

    Article  PubMed  Google Scholar 

  9. R. Bolckmans, T. Kalman, S. Singh, K.C. Ratnatunga, P. Myrelid, S. Travis, and B.D. George. Does Smoking Cessation Reduce Surgical Recurrence After Primary Ileocolic Resection for Crohn’s Disease? Diseases of the colon and rectum. 63:200-206 (2020).

    Article  PubMed  Google Scholar 

  10. P. Papay, W. Reinisch, E. Ho, C. Gratzer, D. Lissner, H. Herkner, S. Riss, C. Dejaco, W. Miehsler, H. Vogelsang, and G. Novacek. The impact of thiopurines on the risk of surgical recurrence in patients with Crohn’s disease after first intestinal surgery. The American journal of gastroenterology. 105:1158-1164 (2010).

    Article  PubMed  Google Scholar 

  11. E. Savarino, G. Bodini, P. Dulbecco, L. Assandri, L. Bruzzone, F. Mazza, A.C. Frigo, V. Fazio, E. Marabotto, and V. Savarino. Adalimumab is more effective than azathioprine and mesalamine at preventing postoperative recurrence of Crohn’s disease: a randomized controlled trial. The American journal of gastroenterology. 108:1731-1742 (2013).

    Article  PubMed  Google Scholar 

  12. M. Regueiro, B.G. Feagan, B. Zou, J. Johanns, M.A. Blank, M. Chevrier, S. Plevy, J. Popp, F.J. Cornillie, M. Lukas, S. Danese, P. Gionchetti, S.B. Hanauer, W. Reinisch, W.J. Sandborn, D. Sorrentino, and P. Rutgeerts. Infliximab Reduces Endoscopic, but Not Clinical, Recurrence of Crohn’s Disease After Ileocolonic Resection. Gastroenterology. 150:1568-1578 (2016).

    Article  PubMed  Google Scholar 

  13. B.P. Kline, T. Weaver, D.L. Brinton, Jr., L. Harris, G.S. Yochum, A.S. Berg, and W.A. Koltun. Clinical and Genetic Factors Impact Time to Surgical Recurrence After Ileocolectomy for Crohn’s Disease. Annals of surgery. 274:346-351 (2021).

    Article  PubMed  Google Scholar 

  14. G.R. Lichtenstein, E.V. Loftus, K.L. Isaacs, M.D. Regueiro, L.B. Gerson, and B.E. Sands. ACG Clinical Guideline: Management of Crohn’s Disease in Adults. The American journal of gastroenterology. 113:481-517 (2018).

    Article  PubMed  Google Scholar 

  15. F. Michelassi, T. Balestracci, R. Chappell, and G.E. Block. Primary and recurrent Crohn’s disease. Experience with 1379 patients. Annals of surgery. 214:230-238; discussion 238-240 (1991).

    Article  PubMed  PubMed Central  Google Scholar 

  16. J. Kusaka, H. Shiga, M. Kuroha, T. Kimura, Y. Kakuta, K. Endo, Y. Kinouchi, and T. Shimosegawa. Residual Lesions on Capsule Endoscopy Is Associated with Postoperative Clinical Recurrence in Patients with Crohn’s Disease. Dig Dis Sci. 63:768-774 (2018).

    Article  PubMed  Google Scholar 

  17. O. Klein, J.F. Colombel, D. Lescut, L. Gambiez, P. Desreumaux, P. Quandalle, and A. Cortot. Remaining small bowel endoscopic lesions at surgery have no influence on early anastomotic recurrences in Crohn’s disease. The American journal of gastroenterology. 90:1949-1952 (1995).

    PubMed  Google Scholar 

  18. F. Gomollón, A. Dignass, V. Annese, H. Tilg, G. Van Assche, J.O. Lindsay, L. Peyrin-Biroulet, G.J. Cullen, M. Daperno, T. Kucharzik, F. Rieder, S. Almer, A. Armuzzi, M. Harbord, J. Langhorst, M. Sans, Y. Chowers, G. Fiorino, P. Juillerat, G.J. Mantzaris, F. Rizzello, S. Vavricka, and P. Gionchetti. 3rd European Evidence-based Consensus on the Diagnosis and Management of Crohn’s Disease 2016: Part 1: Diagnosis and Medical Management. J Crohns Colitis. 11:3-25 (2017).

    Article  PubMed  Google Scholar 

  19. J. Satsangi, M.S. Silverberg, S. Vermeire, and J.F. Colombel. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut. 55:749-753 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  20. P. Gionchetti, A. Dignass, S. Danese, F.J. Magro Dias, G. Rogler, P.L. Lakatos, M. Adamina, S. Ardizzone, C.J. Buskens, S. Sebastian, S. Laureti, G.M. Sampietro, B. Vucelic, C.J. van der Woude, M. Barreiro-de Acosta, C. Maaser, F. Portela, S.R. Vavricka, and F. Gomollon. 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. 11:135-149 (2017).

    Article  PubMed  Google Scholar 

  21. F. Michelassiand S. Sultan. Surgical treatment of complex small bowel Crohn disease. Ann Surg. 260:230-235 (2014).

    Article  Google Scholar 

  22. S. Riss, I. Schuster, P. Papay, F. Herbst, M. Mittlbock, P. Chitsabesan, and A. Stift. Surgical recurrence after primary ileocolic resection for Crohn’s disease. Tech Coloproctol. 18:365-371 (2014).

    Article  PubMed  Google Scholar 

  23. C. Simillis, T. Yamamoto, G.E. Reese, S. Umegae, K. Matsumoto, A.W. Darzi, and P.P. Tekkis. A meta-analysis comparing incidence of recurrence and indication for reoperation after surgery for perforating versus nonperforating Crohn’s disease. Am J Gastroenterol. 103:196-205 (2008).

    Article  PubMed  Google Scholar 

  24. O. Bernell, A. Lapidus, and G. Hellers. Risk factors for surgery and recurrence in 907 patients with primary ileocaecal Crohn’s disease. Br J Surg. 87:1697-1701 (2000).

    Article  PubMed  Google Scholar 

  25. S.B. Kim, J.H. Cheon, J.J. Park, E.S. Kim, S.W. Jeon, S.A. Jung, D.I. Park, C.K. Lee, J.P. Im, Y.S. Kim, H.S. Kim, J. Lee, C.S. Eun, J.M. Lee, B.I. Jang, G.S. Seo. Risk factors for postoperative recurrence in Korean patients with Crohn’s disease. Gut Liver. 14(3):331-337 (2020).

    Article  PubMed  Google Scholar 

  26. L. Maggiori, A. Brouquet, P. Zerbib, J.H. Lefevre, Q. Denost, A. Germain, E. Cotte, L. Beyer-Berjot, N. Munoz-Bongrand, V. Desfourneaux, A. Rahili, J.P. Duffas, K. Pautrat, C. Denet, V. Bridoux, G. Meurette, J.L. Faucheron, J. Loriau, R. Souche, E. Vicaut, Y. Panis, and S. Benoist. Penetrating Crohn Disease Is Not Associated With a Higher Risk of Recurrence After Surgery: A Prospective Nationwide Cohort Conducted by the Getaid Chirurgie Group. Ann Surg. 270:827-834 (2019).

    Article  PubMed  Google Scholar 

  27. S. Shivananda, M.L. Hordijk, A.S. Pena, and J.F. Mayberry. Crohn’s disease: risk of recurrence and reoperation in a defined population. Gut. 30:990-995 (1989).

    Article  PubMed  PubMed Central  Google Scholar 

  28. J.D. Feuersteinand A.S. Cheifetz. Crohn Disease: Epidemiology, Diagnosis, and Management. Mayo Clin Proc. 92:1088-1103 (2017).

    Article  Google Scholar 

  29. M. Regueiro, W. Schraut, L. Baidoo, K.E. Kip, A.R. Sepulveda, M. Pesci, J. Harrison, and S.E. Plevy. Infliximab prevents Crohn’s disease recurrence after ileal resection. Gastroenterology. 136:441-450.e441; quiz 716 (2009).

    Article  PubMed  Google Scholar 

  30. T.Y. Zhang, Y. Lin, R. Fan, S.R. Hu, M.M. Cheng, M.C. Zhang, L.W. Hong, X.L. Zhou, Z.T. Wang, and J. Zhong. Potential model for differential diagnosis between Crohn’s disease and primary intestinal lymphoma. World J Gastroenterol. 22:9411-9418 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  31. J. Kusakaand H. Shiga. Residual Lesions on Capsule Endoscopy Is Associated with Postoperative Clinical Recurrence in Patients with Crohn’s Disease. 63:768-774 (2018).

    Google Scholar 

  32. W.A. Bemelman, J. Warusavitarne, G.M. Sampietro, Z. Serclova, O. Zmora, G. Luglio, A. de Buck van Overstraeten, J.P. Burke, C.J. Buskens, F. Colombo, J.A. Dias, R. Eliakim, T. Elosua, I.E. Gecim, S. Kolacek, J. Kierkus, K.L. Kolho, J.H. Lefevre, M. Millan, Y. Panis, T. Pinkney, R.K. Russell, C. Shwaartz, C. Vaizey, N. Yassin, and A. D’Hoore. ECCO-ESCP Consensus on Surgery for Crohn’s Disease. Journal of Crohn’s & colitis. 12:1-16 (2018).

    Google Scholar 

Download references

Acknowledgements

This work was partly supported by the National Natural Science Foundation of China (Grant 81670471, 81770556, and 81570500) and Jiangsu Provincial Medical Youth Talent (QNRC2016900, to Yi Li).

Funding

This work was partly supported by the National Natural Science Foundation of China (Grant 82170573, 81770556, and 81670471) and Jiangsu Provincial Medical Youth Talent (QNRC2016900, to Yi Li).

Author information

Author notes

  1. Wenwei Qian, Lei Gao and Liangyu Huang contributed equally to this work.

Authors and Affiliations

  1. Department of General Surgery, Jinling Hospital, Medical School of Southeast University, No. 305 East Zhongshan Road, Nanjing, People’s Republic of China

    Wenwei Qian, Yi Li & Weiming Zhu

  2. Department of General Surgery, Jinling Hospital, Medical School of Nanjing University, No. 305 East Zhongshan Road, Nanjing, People’s Republic of China

    Lei Gao, Liangyu Huang, Zhen Guo, Lei Cao, Jianfeng Gong, Yi Li & Weiming Zhu

Authors
  1. Wenwei Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lei Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liangyu Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhen Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lei Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianfeng Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yi Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Weiming Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Weiwen Qian, Lei Gao, and Liangyu Huang contributed equally to this work. Yi Li and Weiming Zhu conceived and designed the study, acquisition, and interpretation of data. Weiwen Qian, Lei Gao, and Liangyu Huang were involved in the interpretation of data and drafting of the manuscript; Zhen Guo and Lei Cao were involved in the analysis, acquisition, and interpretation of data; Jianfeng Gong was involved in the interpretation of data for the work, critical revision of the manuscript for important intellectual content.

Corresponding authors

Correspondence to Yi Li or Weiming Zhu.

Ethics declarations

Ethics Approval and Informed Consent

This study was approved by the ethics committee of Jinling Hospital and all participants provided written informed consent for voluntary participation in this study.

Consent for Publication

All authors agree to the final approval of the version to be published.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Figure S1.

The schematic diagram of surgery and residual lesions. (A) Ileocecal lesion (lesion I) led to penetration and obstruction. Lesion II and III were nonstricturing nonpenetrating diseases, which were macroscopically abnormal during operation. (B) Ileocecal lesion (lesion I) was resected and anastomosis was performed. Lesion II and III were retained as residual lesions. (PNG 1605 kb)

High Resolution Image

(TIF 10244 kb)

ESM 1

(DOCX 14 kb)

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Qian, W., Gao, L., Huang, L. et al. The Prevalence of Concomitant Skip Small Bowel Lesions in Crohn’s Disease and Their Effects on Reoperation in Patients Undergoing Ileocolic Resection. J Gastrointest Surg 26, 2330–2341 (2022). https://doi.org/10.1007/s11605-022-05436-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11605-022-05436-4

Keywords

Search

Navigation