The problem of sarcopenia in patients with infl ammatory bowel disease: a review
https://doi.org/10.31146/1682-8658-ecg-244-12-88-102
Abstract
Aim: to highlight the problem of sarcopenia among patients with inflammatory bowel diseases (IBD). Key points. In 2019, EWGSOP2 hypothesized that sarcopenia is promoted by many contributing factors including inflammatory bowel diseases (ulcerative colitis and Crohn’s disease). Article presented current hypotheses of the pathogenesis of sarcopenia in patients with IBD, with an emphasis on malnutrition, chronic inflammation, and intestinal dysbiosis. Current methods for diagnosing sarcopenia in patients with IBD are presented. The problem of sarcopenic obesity is separately described. Particular attention is paid to the influence of biological agents on the state of muscles. Although data on sarcopenia in IBD are limited, the available studies suggest the need for a comprehensive approach to assessment, early detection and interventions targeted on inflammation, malnutrition, and muscle wasting. And this is a key component of comprehensive strategies for the management of IBD-associated sarcopenia. Conclusion: The interaction between IBD and sarcopenia represents a significant clinical problem with profound implications for treatment outcomes.
About the Authors
O. E. Akchurina
Kazan State Medical University
Russian Federation
Russian Federation
D. D. Mukhametova
Kazan State Medical University
Russian Federation
Russian Federation
D. I. Abdulganieva
Kazan State Medical University
Russian Federation
Russian Federation
References
1. Cruz-Jentoft A.J., Bahat G., Bauer J. et al. Sarcopenia: revised European consensus on definition and diagnosis [published correction appears in Age Ageing. 2019 Jul 1;48(4):601. doi: 10.1093/ageing/afz046]. Age Ageing. 2019;48(1):16-31. doi: 10.1093/ageing/afy169.
2. Sayer A.A., Syddall H., Martin H. et al. The developmental origins of sarcopenia. J Nutr Health Aging. 2008;12(7):427-432. doi: 10.1007/BF02982703.
3. Shelygin Yu.A., Ivashkin V.T., Belousova E.A. et al. Ulcerative colitis (K51), adults. Coloproctology. 2023;22(1), pp. 10-44. (in Russ.) doi: 10.33878/2073-7556-2023-22-1-10-44.@@ Шелыгин Ю.А., Ивашкин В.Т., Белоусова Е.А., и др. Язвенный колит (К51), взрослые. Колопроктология. 2023;22(1):10-44. doi: 10.33878/2073-7556-2023-22-1-10-44.
4. Shelygin Yu.A., Ivashkin V.T., Achkasov S.I. et al. Clinical recommendations. Crohn’s disease (K50), adults. Coloproctology. 2023;22(3), pp. 10-49. (in Russ.) doi: 10.33878/2073-7556-2023-22-3-10-49.@@ Шелыгин Ю.А., Ивашкин В.Т., Ачкасов С.И., и др. Клинические рекомендации. Болезнь Крона (К50), взрослые. Колопроктология. 2023;22(3):10-49. doi: 10.33878/2073-7556-2023-22-3-10-49.
5. Kushner R.F., Schoeller D.A. Resting and total energy expenditure in patients with inflammatory bowel disease. Am J Clin Nutr. 1991;53(1):161-165. doi: 10.1093/ajcn/53.1.161.
6. Balestrieri P., Ribolsi M., Guarino M.P.L. et al. Nutritional Aspects in Inflammatory Bowel Diseases. Nutrients. 2020;12(2):372. Published 2020 Jan 31. doi: 10.3390/nu12020372.
7. Silva T.L.D., Mulder A.P. Sarcopenia and poor muscle quality associated with severe obesity in young adults and middle-aged adults. Clin Nutr ESPEN. 2021;45:299-305. doi: 10.1016/j.clnesp.2021.07.031.
8. Ryan E., McNicholas D., Creavin B., Kelly M.E., Walsh T., Beddy D. Sarcopenia and Inflammatory Bowel Disease: A Systematic Review. Inflamm Bowel Dis. 2019;25(1):67-73. doi: 10.1093/ibd/izy212.
9. Nishikawa H., Nakamura S., Miyazaki T. et al. Inflammatory Bowel Disease and Sarcopenia: Its Mechanism and Clinical Importance. J Clin Med. 2021;10(18):4214. Published 2021 Sep 17. doi: 10.3390/jcm10184214.
10. Scaldaferri F., Pizzoferrato M., Lopetuso L.R. et al. Nutrition and IBD: Malnutrition and/or Sarcopenia? A Practical Guide. Gastroenterol Res Pract. 2017;2017:8646495. doi: 10.1155/2017/8646495.
11. Dhaliwal A., Quinlan J.I., Overthrow K. et al. Sarcopenia in Inflammatory Bowel Disease: A Narrative Overview. Nutrients. 2021;13(2):656. Published 2021 Feb 17. doi: 10.3390/nu13020656.
12. Pizzoferrato M., de Sire R., Ingravalle F. et al. Characterization of Sarcopenia in an IBD Population Attending an Italian Gastroenterology Tertiary Center. Nutrients. 2019;11(10):2281. Published 2019 Sep 24. doi: 10.3390/nu11102281.
13. Liu Y., Tian L. Research progress on the predictive role of sarcopenia in the course and prognosis of inflammatory bowel disease. Peer J. 2023;11: e16421. Published 2023 Nov 22. doi: 10.7717/peerj.16421.
14. Zhang T., Ding C., Xie T. et al. Skeletal muscle depletion correlates with disease activity in ulcerative colitis and is reversed after colectomy. Clin Nutr. 2017;36(6):1586-1592. doi: 10.1016/j.clnu.2016.10.004.
15. An H.J., Tizaoui K., Terrazzino S. et al. Sarcopenia in Autoimmune and Rheumatic Diseases: A Comprehensive Review.Int J Mol Sci. 2020;21(16):5678. Published 2020 Aug 7. doi: 10.3390/ijms21165678.
16. Tkacheva O.N., Tutelyan V.A., Shestopalov A.E. et al. Nutritional insuf ciency (malnutrition) in older adults. Clinical recommendations.Russian Journal of Geriatric Medicine. 2021;(1):15-34. (In Russ.) doi: 10.37586/2686-8636-1-2021-15-34.@@ Ткачева О.Н., Тутельян В.А., Шестопалов А.Е., и др. Недостаточность питания (мальнутриция) у пациентов пожилого и старческого возраста. Клинические рекомендации. Российский журнал гериатрической медицины. 2021;(1):15-34. doi: 10.37586/2686-8636-1-2021-15-34,
17. Lucendo A.J., De Rezende L.C. Importance of nutrition in inflammatory bowel disease. World J Gastroenterol. 2009;15(17):2081-2088. doi: 10.3748/wjg.15.2081.
18. Bass J.J., Kazi A.A., Deane C.S. et al. The mechanisms of skeletal muscle atrophy in response to transient knockdown of the vitamin D receptor in vivo. J Physiol. 2021;599(3):963-979. doi: 10.1113/JP280652.
19. Ashcroft S.P., Bass J.J., Kazi A.A. et al. The vitamin D receptor regulates mitochondrial function in C2C12 myoblasts. Am J Physiol Cell Physiol. 2020;318(3): C536-C541. doi: 10.1152/ajpcell.00568.2019.
20. Coen P.M., Musci R.V., Hinkley J.M., Miller B.F. Mitochondria as a Target for Mitigating Sarcopenia. Front Physiol. 2019;9:1883. Published 2019 Jan 10. doi: 10.3389/fphys.2018.01883.
21. Yin K., Agrawal D.K. Vitamin D and inflammatory diseases. J Inflamm Res. 2014;7:69-87. Published 2014 May 29. doi: 10.2147/JIR.S63898.
22. Calvez V., Becherucci G., Covello C. et al. Navigating the Intersection: Sarcopenia and Sarcopenic Obesity in Inflammatory Bowel Disease. Biomedicines. 2024 May 30;12(6):1218. doi: 10.3390/biomedicines12061218.
23. Ghishan F.K., Kiela P.R. Epithelial transport in inflammatory bowel diseases. Inflamm Bowel Dis. 2014;20(6):1099-1109. doi: 10.1097/MIB.0000000000000029.
24. Juckett G., Trivedi R. Evaluation of chronic diarrhea. Am Fam Physician. 2011;84(10):1119-1126.
25. Martínez-Arnau F.M., Fonfría-Vivas R., Buigues C. et al. Effects of Leucine Administration in Sarcopenia: A Randomized and Placebo-controlled Clinical Trial. Nutrients. 2020;12(4):932. Published 2020 Mar 27. doi: 10.3390/nu12040932.
26. Clark R., Johnson R. Malabsorption Syndromes. Nurs Clin North Am. 2018;53(3):361-374. doi: 10.1016/j.cnur.2018.05.001.
27. Nardone O.M., de Sire R., Petito V. et al. Inflammatory Bowel Diseases and Sarcopenia: The Role of Inflammation and Gut Microbiota in the Development of Muscle Failure. Front Immunol. 2021;12:694217. Published 2021 Jul 13. doi: 10.3389/fimmu.2021.694217.
28. van Langenberg D.R., Della Gatta P., Hill B. et al. 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(7):626-634. doi: 10.1016/j.crohns.2013.11.024.
29. Zavyalova A.N., Novikova V.P., Ignatova P.D. Axis “microbiota - muscle”. Experimental and Clinical Gastroenterology. 2022;(11):60-69. (In Russ.) doi: 10.31146/1682-8658-ecg-207-11-60-69.@@ Завьялова А.Н., Новикова В.П., Игнатова П.Д. Ось «микробиота - мышцы». Экспериментальная и клиническая гастроэнтерология. 2022;(11):60-69. doi: 10.31146/1682-8658-ecg-207-11-60-69.
30. Aldars-García L., Marin A.C., Chaparro M., Gisbert J.P. The Interplay between Immune System and Microbiota in Inflammatory Bowel Disease: A Narrative Review.Int J Mol Sci. 2021;22(6):3076. Published 2021 Mar 17. doi: 10.3390/ijms22063076.
31. Candelli M., Franza L., Pignataro G. et al.Interaction between Lipopolysaccharide and Gut Microbiota in Inflammatory Bowel Diseases.Int J Mol Sci. 2021;22(12):6242. Published 2021 Jun 10. doi: 10.3390/ijms22126242.
32. Malmstrom T.K., Morley J.E. SARC-F: a simple questionnaire to rapidly diagnose sarcopenia. J Am Med Dir Assoc. 2013;14(8):531-532. doi: 10.1016/j.jamda.2013.05.018.
33. Malmstrom T.K., Miller D.K., Simonsick E.M. et al. SARC-F: a symptom score to predict persons with sarcopenia at risk for poor functional outcomes. J Cachexia Sarcopenia Muscle. 2016;7(1):28-36. doi: 10.1002/jcsm.12048.
34. Ida S., Kaneko R., Murata K. SARC-F for Screening of Sarcopenia Among Older Adults: A Meta-analysis of Screening Test Accuracy. J Am Med Dir Assoc. 2018;19(8):685-689. doi: 10.1016/j.jamda.2018.04.001.
35. Matsui M., Asai A., Ushiro K. et al. Accurate SARC-F Score in Patients with Liver Disease. Diagnostics (Basel). 2023;13(11):1959. Published 2023 Jun 4. doi: 10.3390/diagnostics13111959.
36. Kurita N., Wakita T., Kamitani T. et al. SARC-F Validation and SARC-F+EBM Derivation in Musculoskeletal Disease: The SPSS-OK Study. J Nutr Health Aging. 2019;23(8):732-738. doi: 10.1007/s12603-019-1222-x.
37. Bahat G., Oren M.M., Yilmaz O. et al.Comparing SARC-F with SARC-CalF to Screen Sarcopenia in Community Living Older Adults. J Nutr Health Aging. 2018;22(9):1034-1038. doi: 10.1007/s12603-018-1072-y.
38. Mo Y.H., Zhong J., Dong X. et al.Comparison of Three Screening Methods for Sarcopenia in Community-Dwelling Older Persons. J Am Med Dir Assoc. 2021;22(4):746-750.e1. doi: 10.1016/j.jamda.2020.05.041.
39. Ushiro K., Nishikawa H., Matsui M. et al.Comparison of SARC-F Score among Gastrointestinal Diseases. J Clin Med. 2021;10(18):4099. Published 2021 Sep 10. doi: 10.3390/jcm10184099.
40. Roberts H.C., Denison H.J., Martin H.J. et al. A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing. 2011;40(4):423-429. doi: 10.1093/ageing/afr051.
41. Bae H.W., Lee Y.J., Park M.Y. et al. Clinical Significance of Prognostic Nutrition Index in Patients with Crohn’s Disease after Primary Bowel Resection. Yonsei Med J. 2024;65(7):380-388. doi: 10.3349/ymj.2023.0279.
42. Bedard K., Taylor L., Rajabali N. et al. Handgrip strength and risk of malnutrition are associated with an increased risk of hospitalizations in inflammatory bowel disease patients. Therap Adv Gastroenterol. 2023;16:17562848231194395. Published 2023 Aug 31. doi: 10.1177/17562848231194395.
43. Lu Z.L., Wang T.R., Qiao Y.Q. et al. Handgrip Strength Index Predicts Nutritional Status as a Complement to Body Mass Index in Crohn’s Disease. J Crohns Colitis. 2016;10(12):1395-1400. doi: 10.1093/ecco-jcc/jjw121.
44. Ashley T., Jenna A., Patrick S. et al. Hand Grip Strength Is Associated With Clinical Symptom Burden In Crohn’s Disease. Inflammatory Bowel Diseases. 2024;30: S19-S20. doi: 10.1093/ibd/izae020.047.
45. Stack R., Chonnacháin C. Ní., Doherty J. et al. P948 Hand Grip Strength is a useful objective measure associated with fatigue and impaired quality of life in patients with inflammatory bowel disease. Journal of Crohn’s and Colitis. 2024;18: i1724. doi: 10.1093/ecco-jcc/jjad212.1078.
46. Bryant R.V., Schultz C.G., Ooi S. et al. Obesity in Inflammatory Bowel Disease: Gains in Adiposity despite High Prevalence of Myopenia and Osteopenia. Nutrients. 2018;10(9):1192. Published 2018 Sep 1. doi: 10.3390/nu10091192,
47. Adams D.W., Gurwara S., Silver H.J. et al. Sarcopenia Is Common in Overweight Patients with Inflammatory Bowel Disease and May Predict Need for Surgery. Inflamm Bowel Dis. 2017;23(7):1182-1186. doi: 10.1097/MIB.0000000000001128.
48. Bryant R.V., Trott M.J., Bartholomeusz F.D., Andrews J.M. Systematic review: body composition in adults with inflammatory bowel disease. Aliment Pharmacol Ther. 2013;38(3):213-225. doi: 10.1111/apt.12372.
49. Rolland Y., Lauwers-Cances V., Cournot M. et al. Sarcopenia, calf circumference, and physical function of elderly women: a cross-sectional study. J Am Geriatr Soc. 2003;51(8):1120-1124. doi: 10.1046/j.1532-5415.2003.51362.x.
50. Tosato M., Marzetti E., Cesari M. et al. Measurement of muscle mass in sarcopenia: from imaging to biochemical markers. Aging Clin Exp Res. 2017;29(1):19-27. doi: 10.1007/s40520-016-0717-0.
51. Landi F., Liperoti R., Russo A. et al. Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr. 2012;31(5):652-658. doi: 10.1016/j.clnu.2012.02.007.
52. Rosenberg I.H. Summary Comments. American Journal of Clinical Nutrition. 1989;50,:1231-1233. doi: 10.1093/ajcn/50.5.1231.
53. Bryant R.V., Ooi S., Schultz C.G. et al. Low muscle mass and sarcopenia: common and predictive of osteopenia in inflammatory bowel disease. Aliment Pharmacol Ther. 2015;41(9):895-906. doi: 10.1111/apt.13156.
54. Zhang T., Cao L., Cao T. et al. Prevalence of Sarcopenia and Its Impact on Postoperative Outcome in Patients With Crohn’s Disease Undergoing Bowel Resection. JPEN J Parenter Enteral Nutr. 2017;41(4):592-600. doi: 10.1177/0148607115612054.
55. Engelke K., Museyko O., Wang L., Laredo J.D. Quantitative analysis of skeletal muscle by computed tomography imaging-State of the art. J Orthop Translat. 2018;15:91-103. Published 2018 Oct 28. doi: 10.1016/j.jot.2018.10.004.
56. Zakrevsky A.I., Fedorova A.A., Pasechnik I.N., Kutepov D.E. Sarcopenia and its diagnosis. Clinical nutrition and metabolism. 2021;2(1):13-22. (In Russ.) doi: 10.17816/clinutr71107.@@ Закревский А.И., Фёдорова А.А., Пасечник И.Н., Кутепов Д.Е. Саркопения: как её диагностировать? Клиническое питание и метаболизм. 2021;2(1):13-22. doi: 10.17816/clinutr71107.
57. Cankurtaran R.E., Güneş Y.C., Dirican E. et al. Sarcopenia and Myosteatosis Assessed by Magnetic Resonance Enterography May Predict Negative Outcomes in Patients with Crohn’s Disease. Turk J Gastroenterol. 2023;34(8):839-849. doi: 10.5152/tjg.2023.22644.
58. Beaudart C., McCloskey E., Bruyère O. et al. Sarcopenia in daily practice: assessment and management. BMC Geriatr. 2016;16(1):170. Published 2016 Oct 5. doi: 10.1186/s12877-016-0349-4.
59. Petak S., Barbu C.G., Yu E.W. et al. The Official Positions of the International Society for Clinical Densitometry: body composition analysis reporting. J Clin Densitom. 2013;16(4):508-519. doi: 10.1016/j.jocd.2013.08.018.
60. Messina C., Maffi G., Vitale J.A. et al. Diagnostic imaging of osteoporosis and sarcopenia: a narrative review [published correction appears in Quant Imaging Med Surg. 2018 Apr;8(3):372. doi: 10.21037/qims.2018.04.07]. Quant Imaging Med Surg. 2018;8(1):86-99. doi: 10.21037/qims.2018.01.01.
61. Holt D.Q., Moore G.T., Strauss B.J. et al. Visceral adiposity predicts post-operative Crohn’s disease recurrence. Aliment Pharmacol Ther. 2017;45(9):1255-1264. doi: 10.1111/apt.14018.
62. Ashton J.J., Peiris D., Green Z. et al. Routine abdominal magnetic resonance imaging can determine psoas muscle area in paediatric Crohn’s disease and correlates with bioelectrical impedance spectroscopy measures of lean mass. Clin Nutr ESPEN. 2021;42:233-238. doi: 10.1016/j.clnesp.2021.01.031.
63. Więch P., Dąbrowski M., Bazaliński D. et al. Bioelectrical Impedance Phase Angle as an Indicator of Malnutrition in Hospitalized Children with Diagnosed Inflammatory Bowel Diseases-A Case Control Study. Nutrients. 2018;10(4):499. Published 2018 Apr 17. doi: 10.3390/nu10040499.
64. Gonzalez-Granda A., Schollenberger A., Haap M. et al. Optimization of Nutrition Therapy with the Use of Calorimetry to Determine and Control Energy Needs in Mechanically Ventilated Critically Ill Patients: The ONCA Study, a Randomized, Prospective Pilot Study. JPEN J Parenter Enteral Nutr. 2019;43(4):481-489. doi: 10.1002/jpen.1450.
65. Kim S.H., Kim Y.S., Lee S.H. et al. Evaluation of nutritional status using bioelectrical impedance analysis in patients with inflammatory bowel disease.Intest Res. 2022;20(3):321-328. doi: 10.5217/ir.2021.00022.
66. Buckinx F., Landi F., Cesari M. et al. Pitfalls in the measurement of muscle mass: a need for a reference standard. J Cachexia Sarcopenia Muscle. 2018;9(2):269-278. doi: 10.1002/jcsm.12268.
67. Sousa P., Rodrigues C. Expanding ultrasound horizons in inflammatory bowel disease: Beyond the bowel. United European Gastroenterol J. 2024;12(5):541-542. doi: 10.1002/ueg2.12580.
68. Perkisas S., Bastijns S., Baudry S. et al. Application of ultrasound for muscle assessment in sarcopenia: 2020 SARCUS update. Eur Geriatr Med. 2021;12(1):45-59. doi: 10.1007/s41999-020-00433-9.
69. Mulinacci G., Pirola L., Gandola D. et al. Ultrasound muscle assessment for sarcopenia detection in inflammatory bowel disease: A prospective study. United European Gastroenterol J. 2024;12(5):562-573. doi: 10.1002/ueg2.12566.
70. Papadimitriou K., Detopoulou P., Soufleris K. et al. Nutritional Risk and Sarcopenia Features in Patients with Crohn’s Disease: Relation to Body Composition, Physical Performance, Nutritional Questionnaires and Biomarkers. Nutrients. 2023;15(16):3615. Published 2023 Aug 17. doi: 10.3390/nu15163615.
71. Kara M., Kaymak B., Frontera W. et al. Diagnosing sarcopenia: Functional perspectives and a new algorithm from the ISarcoPRM. J Rehabil Med. 2021;53(6): jrm00209. Published 2021 Jun 21. doi: 10.2340/16501977-2851.
72. Samoilova Y.G., Matveeva M.V., Khoroshunova E.A. et al. Markers for the Prediction of Probably Sarcopenia in Middle-Aged Individuals. Journal of Personalized Medicine. 2022; 12(11):1830. doi: 10.3390/jpm12111830.@@ Самойлова Ю.Г., Матвеева М.В., Хорошунова Е.А., и др. Маркеры для прогнозирования вероятной саркопении у лиц среднего возраста. Журнал персонализированной медицины. 2022; 12(11):1830. doi: 10.3390/jpm12111830.
73. Calvani R., Marini F., Cesari M. et al. Biomarkers for physical frailty and sarcopenia: state of the science and future developments. J Cachexia Sarcopenia Muscle. 2015;6(4):278-286. doi: 10.1002/jcsm.12051.
74. Lazebnik L.B., Golovanova E.V., Alekseenko S.A. et al.Russian Consensus “Hyperammonemia in Adults” (Version 2021). Experimental and Clinical Gastroenterology. 2021;(3):97-118. (In Russ.) doi: 10.31146/1682-8658-ecg-187-3-97-118.@@ Лазебник Л.Б., Голованова Е.В., Алексеенко С.А., и др. Российский консенсус «Гипераммониемии у взрослых» (Версия 2021). Экспериментальная и клиническая гастроэнтерология. 2021;187(3): 97-118. doi: 10.31146/1682-8658-ecg-187-3-97-118.
75. Melnyk J.L., Cavaliere K.R, Roth N.C. Non-Hepatic Hyperammonemia Associated With Acute Bowel Perforation. The American Journal of Gastroenterology. 2019;114:1235-1236. doi: 10.14309/01.ajg.0000598348. 10384.ef.
76. Zhou Y., Zhang M., Zhao X., Feng J. Ammonia exposure induced intestinal inflammation injury mediated by intestinal microbiota in broiler chickens via TLR4/TNF-α signaling pathway. Ecotoxicol Environ Saf. 2021;226:112832. doi: 10.1016/j.ecoenv.2021.112832.
77. Osipenko M.F., Krasner Ya.A., Borodin I.D., Kholin V.D. Ammonia level of capillary blood in patients with inflammatory bowel diseases and nonalcoholic fatty liver disease. Medical alphabet. 2020;(10):49-51. (In Russ.) doi: 10.33667/2078-5631-2020-10-49-51.@@ Осипенко М.Ф., Краснер Я.А., Бородин И.Д., Холин В.Д. Уровень аммиака капиллярной крови у больных воспалительными заболеваниями кишечника с неалкогольной жировой болезнью печени. Медицинский алфавит. 2020;(10):49-51. doi: 10.33667/2078-5631-2020-10-49-51.
78. Mendes J., Simões C.D., Martins J.O., Sousa A.S. Inflammatory Bowel Disease And Sarcopenia: A Focus On Muscle Strength - Narrative Review. Arq Gastroenterol. 2023;60(3):373-382. doi: 10.1590/S0004-2803.230302023-45.
79. Cederholm T., Jensen G.L., Correia M.I.T.D. et al. GLIM criteria for the diagnosis of malnutrition - A consensus report from the global clinical nutrition community. Clin Nutr. 2019;38(1):1-9. doi: 10.1016/j.clnu.2018.08.002.
80. Huang L., Niannian F., Zhang Y. et al. Rapid assessment of malnutrition based on GLIM diagnosis in Crohn’s disease. Front Nutr. 2023;10:1236036. Published 2023 Sep 6. doi: 10.3389/fnut.2023.1236036.
81. Wall C.L., Wilson B., Lomer M.C.E. Development and validation of an inflammatory bowel disease nutrition self-screening tool (IBD-NST) for digital use. Front Nutr. 2023;10:1065592. Published 2023 Feb 3. doi: 10.3389/fnut.2023.1065592.
82. Godala M., Gaszyńska E., Walczak K., Małecka-Wojciesko E. An Evaluation of the Usefulness of Selected Screening Methods in Assessing the Risk of Malnutrition in Patients with Inflammatory Bowel Disease. Nutrients. 2024;16(6):814. Published 2024 Mar 13. doi: 10.3390/nu16060814.
83. Bischoff S.C., Barazzoni R., Busetto L. et al. European guideline on obesity care in patients with gastrointestinal and liver diseases - Joint European Society for Clinical Nutrition and Metabolism / United European Gastroenterology guideline. United European Gastroenterol J. 2022;10(7):663-720. doi: 10.1002/ueg2.12280.
84. Pavlova Z. Sh., Golodnikov I.I. Latent presarcopenic obesity in a patient with inflammatory bowel disease. Endokrinologiya: novosti, mneniya, obuchenie. Endocrinology: News, Opinions, Training. 2020; 9 (3): 59-62. (in Russ.) doi: 10.33029/2304-9529-2020-9-3-59-62.@@ Павлова З.Ш., Голодников И.И. Скрытое пресаркопеническое ожирение у пациента с воспалительными заболеваниями кишечника. Эндокринология: новости, мнения, обучение. 2020;9(3):59-62. doi: 10.33029/2304-9529-2020-9-3-59-62.
85. Bikbavova G.R., Livzan M.A., Lisyutenko N.S., Romanyuk A.E. Pathomorphosis of ulcerative colitis: from body weight deficiency to sarcopenic obesity. Experimental and Clinical Gastroenterology. 2023;(10):57-62. (In Russ.) doi: 10.31146/1682-8658-ecg-218-10-57-62.@@ Бикбавова Г.Р., Ливзан М.А. Патоморфоз язвенного колита: от дефицита массы тела к саркопеническому ожирению. Экспериментальная и клиническая гастроэнтерология. 2023; 218(10): 57-62. doi: 10.31146/1682-8658-ecg-218-10-57-62.
86. Grillot J., D’Engremont C., Parmentier A.L. 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(10):3024-3030. doi: 10.1016/j.clnu.2020.01.001.
87. Michalak A., Kasztelan-Szczerbińska B., Cichoż-Lach H. Impact of Obesity on the Course of Management of Inflammatory Bowel Disease-A Review. Nutrients. 2022;14(19):3983. Published 2022 Sep 25. doi: 10.3390/nu14193983.
88. Bilski J., Pierzchalski P., Szczepanik M. et al. Multifactorial Mechanism of Sarcopenia and Sarcopenic Obesity. Role of Physical Exercise, Microbiota and Myokines. Cells. 2022;11(1):160. Published 2022 Jan 4. doi: 10.3390/cells11010160.
89. Faye A.S., Khan T., Cautha S., Kochar B. Sarcopenia in Inflammatory Bowel Diseases: Reviewing Past Work to Pave the Path for the Future. Curr Treat Options Gastroenterol. 2022;20(3):250-260. doi: 10.1007/s11938-022-00389-8.
90. Michalak A., Kasztelan-Szczerbińska B., Cichoż-Lach H. Impact of Obesity on the Course of Management of Inflammatory Bowel Disease-A Review. Nutrients. 2022;14(19):3983. Published 2022 Sep 25. doi: 10.3390/nu14193983.
91. Boparai G., Kedia S., Kandasamy D. et al.Combination of sarcopenia and high visceral fat predict poor outcomes in patients with Crohn’s disease. Eur J Clin Nutr. 2021;75(10):1491-1498. doi: 10.1038/s41430-021-00857-x.
92. Skrzypczak D., Ratajczak A.E., Szymczak-Tomczak A. et al. A Vicious Cycle of Osteosarcopeniain Inflammatory Bowel Diseases-Aetiology, Clinical Implications and Therapeutic Perspectives. Nutrients. 2021;13(2):293. Published 2021 Jan 20. doi: 10.3390/nu13020293.
93. Subramaniam K., Fallon K., Ruut T. et al. Infliximab reverses inflammatory muscle wasting (sarcopenia) in Crohn’s disease. Aliment Pharmacol Ther. 2015;41(5):419-428. doi: 10.1111/apt.13058.
94. Kochar B.D., Cai W., Ananthakrishnan A.N. Inflammatory Bowel Disease Patients Who Respond to Treatment with Anti-tumor Necrosis Factor Agents Demonstrate Improvement in Pre-treatment Frailty. Dig Dis Sci. 2022;67(2):622-628. doi: 10.1007/s10620-021-06990-8.
95. Dobrovolskaya O.V., Demin N.V., Feklistov A. Yu. et al. Sarcopenic phenotype and functional status of skeletal muscles in rheumatoid arthritis patients with biological therapy. The Clinician. 2023;17(2):19-27. (In Russ.) doi: 10.17650/1818-8338-2023-17-2-К680.@@ Добровольская О.В., Демин Н.В., Феклистов А.Ю. и др. Саркопенический фенотип и функциональное состояние скелетных мышц у больных ревматоидным артритом на фоне биологической терапии. Клиницист. 2023;17(2):19-27. doi: 10.17650/1818-8338-2023-17-2-К680.
96. Ding N.S., Malietzis G., Lung P.F.C. et al. The body composition profile is associated with response to anti-TNF therapy in Crohn’s disease and may offer an alternative dosing paradigm. Aliment Pharmacol Ther. 2017;46(9):883-891. doi: 10.1111/apt.14293.
97. Grova M., Crispino F., Maida M. et al. Sarcopenia is a negative predictive factor for endoscopic remission in patients with Crohn’s disease treated with biologics. Dig Liver Dis. 2023;55(7):865-871. doi: 10.1016/j.dld.2023.02.017.
98. Neelam P.B., Sharma A., Sharma V. Sarcopenia and frailty in inflammatory bowel disease: Emerging concepts and evidence. JGH Open. 2024;8(1): e13033. Published 2024 Jan 27. doi: 10.1002/jgh3.13033.
99. Kochar B., Cai W., Cagan A., Ananthakrishnan A.N. Pretreatment Frailty Is Independently Associated With Increased Risk of Infections After Immunosuppression in Patients With Inflammatory Bowel Diseases. Gastroenterology. 2020;158(8):2104-2111.e2. doi: 10.1053/j.gastro.2020.02.032.
100. Tan Z., Chin A., Welman C.J., Thin L. A High Visceral-to-Skeletal Muscle Area Ratio on Cross-Sectional Imaging Is Associated With Failure of Standard Ustekinumab Doses: A Multicenter Study. Clin Transl Gastroenterol. 2024;15(7): e00722. Published 2024 Jul 1. doi: 10.14309/ctg.0000000000000722.
101. Shrager J.B., Randle R., Lee M. et al. JAK inhibition with tofacitinib rapidly increases contractile force in human skeletal muscle. Life Sci Alliance. 2024;7(11): e202402885. Published 2024 Aug 9. doi: 10.26508/lsa.202402885.
102. Erős A., Soós A., Hegyi P. et al. Sarcopenia as an independent predictor of the surgical outcomes of patients with inflammatory bowel disease: a meta-analysis. Surg Today. 2020;50(10):1138-1150. doi: 10.1007/s00595-019-01893-8.
103. Nuzzo A., Adam Hassan F., Dermine S. et al. P311 Prevalence and impact of sarcopenia in patients with inflammatory bowel diseases: a prospective cohort study. Journal of Crohn’s and Colitis. 2024;18: i692. doi: 10.1093/ecco-jcc/jjad212.0441.
104. Atlan L., Pratt L.T., Cohen S. et al. P123 Sarcopenia is a predictor for severe disease course in paediatric inflammatory bowel disease. Journal of Crohn’s and Colitis. 2020;14:197-198. doi: 10.1093/ecco-jcc/jjz203.252.
105. Bamba S., Sasaki M., Takaoka A. et al. Sarcopenia is a predictive factor for intestinal resection in admitted patients with Crohn’s disease. PLoS One. 2017;12(6): e0180036. Published 2017 Jun 23. doi: 10.1371/journal.pone.0180036.
106. Ding N.S., Tassone D., Al Bakir I. et al. Systematic Review: The Impact and Importance of Body Composition in Inflammatory Bowel Disease. J Crohns Colitis. 2022;16(9):1475-1492. doi: 10.1093/ecco-jcc/jjac041.
107. Grova M., Crispino F., Maida M. et al. P347 Sarcopenia is a poor prognostic factor for endoscopic outcomes in patients with Crohn’s disease. Journal of Crohn’s and Colitis. 2023;16: i360-i361. doi: 10.1093/ecco-jcc/jjab232.474.
108. O’Brien S., Kavanagh R.G., Carey B.W. et al. The impact of sarcopenia and myosteatosis on postoperative outcomes in patients with inflammatory bowel disease. Eur Radiol Exp. 2018;2(1):37. Published 2018 Nov 21. doi: 10.1186/s41747-018-0072-3.
109. Fiorindi C., Giudici F., Testa G.D. et al. Multimodal Prehabilitation for Patients with Crohn’s Disease Scheduled for Major Surgery: A Narrative Review. Nutrients. 2024;16(11):1783. Published 2024 Jun 6. doi: 10.3390/nu16111783.
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For citations:
Akchurina O.E., Mukhametova D.D., Abdulganieva D.I. The problem of sarcopenia in patients with infl ammatory bowel disease: a review. Experimental and Clinical Gastroenterology. 2025;(12):88-102. (In Russ.) https://doi.org/10.31146/1682-8658-ecg-244-12-88-102
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