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Nutrition in acute and chronic diseases

Sarcopenia assessed by computed tomography is associated with colectomy in patients with acute severe ulcerative colitis

European Journal of Clinical Nutrition volume 76, pages 410–418 (2022)Cite this article

Subjects

Abstract

Background

Altered body composition is an important characteristic of malnutrition that may better reflect the clinical course. This study aimed to evaluate the prognostic role of sarcopenia by computed tomography (CT) on colectomy in acute severe ulcerative colitis (ASUC) during index hospitalization and follow-up.

Methods

254 ASUC patients undergoing CT scans at admission were retrospectively included. Sarcopenia was assessed by the skeletal muscle index (SMI) with CT scans at L3, and patients with an SMI below the lowest sex-specific quartile were diagnosed with sarcopenia. Body mass index (BMI) < 18.5 kg/m2 was defined as clinical malnutrition. Univariate and multivariate analyses were performed to determine the association between sarcopenia and colectomy.

Results

The prevalence of sarcopenia in ASUC was 50.0%, and malnutrition was 25.2%. Among sarcopenic patients, 36.2% was malnutrition, 51.2% had normal BMI, 11.8% was overweight, and 0.8% was obese. During index hospitalization, 66.9% patients needed rescue therapy with 52.4% received medical rescue therapy and 14.6% received colectomy. During follow-up, 33.2% patients needed colectomy. Significantly more sarcopenic patients required colectomy (22.0% vs 7.1%, p = 0.001) and rescue therapy (81.9% vs 52.0%, p < 0.001) during index hospitalization and colectomy during follow-up (44.4% vs 23.7%, p = 0.001) than non-sarcopenic patients. However, BMI < 18.5 kg/m2 was not related to the clinical course. In multivariate analyses, sarcopenia remained an independent risk factor for rescue therapy and colectomy during index hospitalization and colectomy during follow-up.

Conclusion

Sarcopenia rather than BMI was associated with clinical outcomes in ASUC and played an important role in predicting the need for colectomy.

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Fig. 1: Assessment of sarcopenia by computed tomography scan.

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Data availability

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

References

  1. Mak WY, Zhao M, Ng SC, Burisch J. The epidemiology of inflammatory bowel disease: East meets West. J Gastroenterol Hepatol. 2020;35:380–9.

    Article  Google Scholar 

  2. Casanova MJ, Chaparro M, Molina B, Merino O, Batanero R, Duenas-Sadornil C, et al. Prevalence of malnutrition and nutritional characteristics of patients with inflammatory bowel disease. J Crohns Colitis. 2017;11:1430–9.

    Article  Google Scholar 

  3. Chang JT. Pathophysiology of inflammatory bowel diseases. N Engl J Med. 2020;383:2652–64.

    Article  CAS  Google Scholar 

  4. Fiorindi C, Cuffaro F, Piemonte G, Cricchio M, Addasi R, Dragoni G. et al. Effect of long-lasting nutritional prehabilitation on postoperative outcome in elective surgery for IBD. Clin Nutr. 2021;40:928–35.

    Article  Google Scholar 

  5. Ray JJ, Esen E, McIntyre S, Kirat HT, Grieco M, Remzi F. Association of malnutrition with postoperative outcomes after ileal pouch-anal anastomosis. J Gastrointest Surg. 2020. https://doi.org/10.1007/s11605-020-04861-7.

  6. Cederholm T, Jensen GL, Correia M, Gonzalez MC, Fukushima R, Higashiguchi T, et al. GLIM criteria for the diagnosis of malnutrition—a consensus report from the global clinical nutrition community. Clin Nutr. 2019;38:1–9.

    Article  CAS  Google Scholar 

  7. Fiorindi C, Luceri C, Dragoni G, Piemonte G, Scaringi S, Staderini F. et al. GLIM criteria for malnutrition in surgical IBD patients: a pilot study. Nutrients. 2020;12:2222.

    Article  Google Scholar 

  8. Cushing KC, Kordbacheh H, Gee MS, Kambadakone A, Ananthakrishnan AN. Sarcopenia is a novel predictor of the need for rescue therapy in hospitalized ulcerative colitis patients. J Crohns Colitis. 2018;12:1036–41.

    Article  Google Scholar 

  9. Grillot J, D’Engremont C, Parmentier AL, Lakkis Z, Piton G, Cazaux D, et al. Sarcopenia and visceral obesity assessed by computed tomography are associated with adverse outcomes in patients with Crohn’s disease. Clin Nutr. 2020;39:3024–30.

    Article  Google Scholar 

  10. Zhang S, Tan S, Jiang Y, Xi Q, Meng Q, Zhuang Q, et al. Sarcopenia as a predictor of poor surgical and oncologic outcomes after abdominal surgery for digestive tract cancer: a prospective cohort study. Clin Nutr. 2019;38:2881–8.

    Article  Google Scholar 

  11. Binay Safer V, Tasci I, Safer U. Crohn’s disease, visceral obesity and sarcopenia. Clin Nutr. 2020;39:2315–6.

    Article  Google Scholar 

  12. Feuerstein JD, Isaacs KL, Schneider Y, Siddique SM, Falck-Ytter Y, Singh S, et al. AGA clinical practice guidelines on the management of moderate to severe ulcerative colitis. Gastroenterology. 2020;158:1450–61.

    Article  Google Scholar 

  13. Laharie D, Bourreille A, Branche J, Allez M, Bouhnik Y, Filippi J, et al. Ciclosporin versus infliximab in patients with severe ulcerative colitis refractory to intravenous steroids: a parallel, open-label randomised controlled trial. Lancet. 2012;380:1909–15.

    Article  CAS  Google Scholar 

  14. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:601.

    Article  Google Scholar 

  15. Eros A, Soos A, Hegyi P, Szakacs Z, Benke M, Szucs A, et al. Sarcopenia as an independent predictor of the surgical outcomes of patients with inflammatory bowel disease: a meta-analysis. Surg Today. 2020;50:1138–50.

    Article  Google Scholar 

  16. Saul D, Kosinsky RL. Dextran sodium sulfate-induced colitis as a model for sarcopenia in mice. Inflamm Bowel Dis. 2020;26:56–65.

    Article  Google Scholar 

  17. Bamba S, Inatomi O, Takahashi K, Morita Y, Imai T, Ohno M, et al. Assessment of body composition from CT images at the level of the third lumbar vertebra in inflammatory bowel disease. Inflamm Bowel Dis. 2020. https://doi.org/10.1093/ibd/izaa306.

  18. Whaley KG, Rosen MJ. Contemporary medical management of acute severe ulcerative colitis. Inflamm Bowel Dis. 2019;25:56–66.

    PubMed  Google Scholar 

  19. Guerra RS, Fonseca I, Sousa AS, Jesus A, Pichel F, Amaral TF. ESPEN diagnostic criteria for malnutrition—a validation study in hospitalized patients. Clin Nutr 2017;36:1326–32.

    Article  Google Scholar 

  20. Cima RR. Timing and indications for colectomy in chronic ulcerative colitis: Surgical consideration. Dig Dis. 2010;28:501–7.

    Article  Google Scholar 

  21. Tiu SPT, Hajirawala LN, Leonardi C, Davis KG, Orangio GR, Barton JS. Delayed surgery does not increase risk in urgent colectomy for ulcerative colitis. Am Surg. 2020:3134820971576.

  22. Harbord M, Eliakim R, Bettenworth D, Karmiris K, Katsanos K, Kopylov U, et al. Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 2: Current management. J Crohns Colitis. 2017;11:769–84.

    Article  Google Scholar 

  23. Zhang T, Cao L, Cao T, Yang J, Gong J, Zhu W, et al. Prevalence of sarcopenia and its impact on postoperative outcome in patients with Crohn’s Disease undergoing bowel resection. J Parenter Enter Nutr. 2017;41:592–600.

    Article  Google Scholar 

  24. Satsangi J, Silverberg MS, Vermeire S, Colombel JF. The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications. Gut. 2006;55:749–53.

    Article  CAS  Google Scholar 

  25. Thiberge C, Charpentier C, Gillibert A, Modzelewski R, Dacher JN, Savoye G, et al. Lower subcutaneous or visceral adiposity assessed by abdominal computed tomography could predict adverse outcome in patients With Crohn’s disease. J Crohns Colitis. 2018;12:1429–37.

    Article  Google Scholar 

  26. Houttu N, Kalliomaki M, Gronlund MM, Niinikoski H, Nermes M, Laitinen K. Body composition in children with chronic inflammatory diseases: a systematic review. Clin Nutr. 2020;39:2647–62.

    Article  Google Scholar 

  27. Galata C, Hodapp J, Weiss C, Karampinis I, Vassilev G, Reissfelder C, et al. Skeletal muscle mass index predicts postoperative complications in intestinal surgery for Crohn’s disease. J Parenter Enter Nutr. 2020;44:714–21.

    Article  Google Scholar 

  28. Fujikawa H, Araki T, Okita Y, Kondo S, Kawamura M, Hiro J, et al. Impact of sarcopenia on surgical site infection after restorative proctocolectomy for ulcerative colitis. Surg Today. 2017;47:92–8.

    Article  Google Scholar 

  29. Dedhia PH, White Y, Dillman JR, Adler J, Jarboe MD, Teitelbaum DH, et al. Reduced paraspinous muscle area is associated with post-colectomy complications in children with ulcerative colitis. J Pediatr Surg 2018;53:477–82.

    Article  Google Scholar 

  30. Zhang T, Ding C, Xie T, Yang J, Dai X, Lv T, et al. Skeletal muscle depletion correlates with disease activity in ulcerative colitis and is reversed after colectomy. Clin Nutr. 2017;36:1586–92.

    Article  Google Scholar 

  31. van Langenberg DR, Della Gatta P, Hill B, Zacharewicz E, Gibson PR, Russell AP. Delving into disability in Crohn’s disease: dysregulation of molecular pathways may explain skeletal muscle loss in Crohn’s disease. J Crohns Colitis. 2014;8:626–34.

    Article  Google Scholar 

  32. de Sire R, Rizzatti G, Ingravalle F, Pizzoferrato M, Petito V, Lopetuso L, et al. Skeletal muscle-gut axis: emerging mechanisms of sarcopenia for intestinal and extra intestinal diseases. Minerva Gastroenterol Dieto.l 2018;64:351–62.

    Google Scholar 

  33. Subramaniam K, Fallon K, Ruut T, Lane D, McKay R, Shadbolt B, et al. Infliximab reverses inflammatory muscle wasting (sarcopenia) in Crohn’s disease. Aliment Pharm Ther. 2015;41:419–28.

    Article  CAS  Google Scholar 

  34. Singh S, Dulai PS, Zarrinpar A, Ramamoorthy S, Sandborn WJ. Obesity in IBD: epidemiology, pathogenesis, disease course and treatment outcomes. Nat Rev Gastroenterol Hepatol. 2017;14:110–21.

    Article  CAS  Google Scholar 

  35. Sun X, Xu J, Chen X, Zhang W, Chen W, Zhu C, et al. Sarcopenia in patients with normal body mass index is an independent predictor for postoperative complication and long-term survival in gastric cancer. Clin Transl Sci. 2020. https://doi.org/10.1111/cts.12940.

  36. Adams DW, Gurwara S, Silver HJ, Horst SN, Beaulieu DB, Schwartz DA, et al. Sarcopenia is common in overweight patients with inflammatory bowel disease and may predict need for surgery. Inflamm Bowel Dis. 2017;23:1182–6.

    Article  Google Scholar 

  37. Cederholm T, Krznaric Z, Pirlich M. Diagnosis of malnutrition in patients with gastrointestinal diseases: recent observations from a global leadership initiative on malnutrition perspective. Curr Opin Clin Nutr Metab Care. 2020;23:361–6.

    Article  Google Scholar 

  38. Holt DQ, Moore GT, Strauss BJ, Hamilton AL, De Cruz P, Kamm MA. Visceral adiposity predicts post-operative Crohn’s disease recurrence. Aliment Pharm Ther. 2017;45:1255–64.

    Article  CAS  Google Scholar 

  39. Lim Z, Welman CJ, Raymond W, Thin L. The effect of adiposity on anti-tumor necrosis factor-alpha levels and loss of response in Crohn’s disease patients. Clin Transl Gastroenterol. 2020;11:e00233.

    Article  Google Scholar 

  40. Cravo ML, Velho S, Torres J, Costa Santos MP, Palmela C, Cruz R, et al. Lower skeletal muscle attenuation and high visceral fat index are associated with complicated disease in patients with Crohn’s disease: an exploratory study. Clin Nutr Espen. 2017;21:79–85.

    Article  Google Scholar 

  41. Ha CWY, Martin A, Sepich-Poore GD, Shi B, Wang Y, Gouin K. et al. Translocation of viable gut microbiota to mesenteric adipose drives formation of creeping fat in humans. Cell. 2020;183:666–83e17.

    Article  CAS  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge all of the investigators for their contributions to the trial, as well as Bin Chen, who provided medical writing assistance.

Funding

This work was supported by National Natural Science Foundation of China (grant number 81800474).

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Author notes

  1. These authors contributed equally: Xiaolong Ge, Jingya Xia

Authors and Affiliations

  1. Department of General Surgery, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, 310016, China

    Xiaolong Ge, Wei Liu, Weilin Qi, Rongpan Bai & Wei Zhou

  2. Department of Radiology, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, 310016, China

    Jingya Xia

  3. Department of Gastroenterology, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, Zhejiang, 310016, China

    Yan Wu, Linna Ye & Qian Cao

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  1. Xiaolong Ge
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Contributions

GXL, XJY, and BRP: conceptual design of the study. YLN, LW, WY, and QWL: data collection, data analysis, and data interpretation. GXL, ZW: manuscript writing. CQ, BRP, and ZW: overall supervision of the study. All authors critically revised the manuscript, agree to be fully accountable for ensuring the integrity and accuracy of the work, and read and approved the final manuscript.

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Correspondence to Rongpan Bai or Wei Zhou.

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Ge, X., Xia, J., Wu, Y. et al. Sarcopenia assessed by computed tomography is associated with colectomy in patients with acute severe ulcerative colitis. Eur J Clin Nutr 76, 410–418 (2022). https://doi.org/10.1038/s41430-021-00953-y

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