Skip to main content

Advertisement

Log in

Incorporating Frailty in the Treatment Program of Elderly Patients with Gastrointestinal Disease

  • Gastroenterology for Geriatric Patients (S Katz and A Afzali, Section Editors)
  • Published:
Current Treatment Options in Gastroenterology Aims and scope Submit manuscript

Abstract

Purpose of review

The goal of this paper is to review the utilization of frailty as a predictor of poor outcomes in gastrointestinal disease, hepatology, and gastrointestinal surgery.

Recent findings

The frailty syndrome has been extensively described in the geriatric population as a predictor of poor clinical outcomes and its application has proven valuable in a variety of chronic and inflammatory disease states independent of age. In hepatology and gastroenterology, frailty has been associated with worsening pre- and post-liver transplant outcomes, post-operative complications, periprocedural adverse events during colonoscopy, and even possible early disruption of the gut microbiome. In patients undergoing immunosuppression, frailty has recently been independently associated with increased risk of infection, morbidity, and mortality.

Summary

Frailty has been associated with a wide range of adverse health outcomes in multiple patient populations and disease states including in chronic gastrointestinal and liver disease. The standardization and routine clinical application of frailty evaluation in groups at risk for frailty progression and deleterious outcomes have been recommended. Challenges regarding translating frailty evaluation to individualized frailty treatment remain. With emerging research examining frailty in gastrointestinal and liver disease, there is hope to bridge this gap to deter and ideally reverse frailty progression and its deleterious outcomes.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

ADLs:

Activities of daily living

IALDs:

Instrumental activities of daily living

IBD:

Inflammatory bowel disease

CGA:

Cognitive geriatric assessment

mFI:

Modified Frailty Index

CHS:

Cardiovascular Health Study

SPPB:

Short performance physical battery

NASH:

Non-alcoholic steatohepatitis

ALD:

Alcohol-related liver disease

CRP:

Interleukin-6 (IL-6), C-reactive protein

TNF-α:

Tumor necrosis factor-α

CXCL-10:

CXC chemokine ligand-10

ASA:

American Society of Anesthesiology

6MWT:

score, 6-min walk test

LFI:

Liver Frailty Index

References and Recommended Reading

Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. Vaupel JW, Manton KG, Stallard E. The impact of heterogeneity in individual frailty on the dynamics of mortality. Demography. 1979;16(3):439–54.

    Article  CAS  Google Scholar 

  2. Rockwood K, Stadnyk K, MacKnight C, McDowell I, Hébert R, Hogan DB. A brief clinical instrument to classify frailty in elderly people. Lancet. 1999;353(9148):205–6. https://doi.org/10.1016/S0140-6736(98)04402-X.

    Article  CAS  PubMed  Google Scholar 

  3. Rockwood K, Fox RA, Stolee P, Robertson D, Beattie BL. Frailty in elderly people: an evolving concept. CMAJ. 1994;150(4):489–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Uchmanowicz I, Młynarska A, Lisiak M, et al. Heart failure and problems with frailty syndrome: why it is time to care about frailty syndrome in heart failure. Card Fail Rev. 2019;5(1):37–43. https://doi.org/10.15420/cfr.2018.37.1.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rodríguez-Mañas L, Féart C, Mann G, Viña J, Chatterji S, Chodzko-Zajko W, et al. Searching for an operational definition of frailty: a Delphi method based consensus statement: the frailty operative definition – consensus conference project. J Gerontol A Bio Sci Med Sci. 2013;68:62–7.

    Article  Google Scholar 

  6. Cohen HJ. In search of the underlying mechanisms of frailty. J Gerontol A Biol Sci Med Sci. 2000;55(12):M706–8. https://doi.org/10.1093/gerona/55.12.m706.

    Article  CAS  PubMed  Google Scholar 

  7. Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people [published correction appears in Lancet. 2013 Oct 19;382(9901):1328]. Lancet. 2013;381(9868):752–62. https://doi.org/10.1016/S0140-6736(12)62167-9.

    Article  PubMed  Google Scholar 

  8. Lang PO, Michel JP, Zekry D. Frailty syndrome: a transitional state in a dynamic process. Gerontology. 2009;55(5):539–49. https://doi.org/10.1159/000211949.

    Article  PubMed  Google Scholar 

  9. Laube R, Wang H, Park L, Heyman JK, Vidot H, Majumdar A, et al. Frailty in advanced liver disease. Liver Int. 2018;38(12):2117–28. https://doi.org/10.1111/liv.13917.

    Article  PubMed  Google Scholar 

  10. Schaenman J, Castellon L, Liang EC, et al. The Frailty Risk Score predicts length of stay and need for rehospitalization after kidney transplantation in a retrospective cohort: a pilot study. Pilot Feasibility Study. 2019;5:144. Published 2019 Dec 10. https://doi.org/10.1186/s40814-019-0534-2.

  11. Czobor NR, Lehot JJ, Holndonner-Kirst E, Tully PJ, Gal J, Szekely A. Frailty in patients undergoing vascular surgery: a narrative review of current evidence. Ther Clin Risk Manag. 2019;15:1217–32. Published 2019 Oct 17. https://doi.org/10.2147/TCRM.S217717.

  12. Telemi E, Trofymenko O, Venkat R, Pandit V, Pandian TK, Nfonsam VN. Frailty predicts morbidity after colectomy for ulcerative colitis. Am Surg. 2018;84(2):225–9.

    Article  Google Scholar 

  13. Nixon AC, Bampouras TM, Pendleton N, Mitra S, Brady ME, Dhaygude AP. Frailty is independently associated with worse health-related quality of life in chronic kidney disease: a secondary analysis of the Frailty Assessment in Chronic Kidney Disease study. Clin Kidney J. 2019;13(1):85–94. Published 2019 Apr 30. https://doi.org/10.1093/ckj/sfz038.

  14. Buchman AS, Boyle PA, Wilson RS, Tang Y, Bennett DA. Frailty is associated with incident Alzheimer’s disease and cognitive decline in the elderly. Psychosom Med. 2007;69(5):483–9. https://doi.org/10.1097/psy.0b013e318068de1d.

    Article  PubMed  Google Scholar 

  15. Buchman AS, Yu L, Wilson RS, Boyle PA, Schneider JA, Bennett DA. Brain pathology contributes to simultaneous change in physical frailty and cognition in old age. J Gerontol A Biol Sci Med Sci. 2014;69(12):1536–44. https://doi.org/10.1093/gerona/glu117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Willig AL, Overton ET, Saag MS. The silent epidemic - frailty and aging with HIV. Total Patient Care HIV HCV. 2016;1(1):6–17.

    PubMed  PubMed Central  Google Scholar 

  17. Geessink N, Schoon Y, van Goor H, Olde Rikkert M, Melis R, TOPICS-MDS consortium. Frailty and quality of life among older people with and without a cancer diagnosis: findings from TOPICS-MDS. PLoS One. 2017;12(12):e0189648. Published 2017 Dec 15. https://doi.org/10.1371/journal.pone.0189648.

  18. Bisset ES, Howlett SE. The biology of frailty in humans and animals: understanding frailty and promoting translation [published correction appears in Aging Med (Milton). 2019 Jun 20;2(2):121]. Aging Med (Milton). 2019;2(1):27–34 Published 2019 Mar 27. https://doi.org/10.1002/agm2.12058.

  19. Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, et al. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci. 2001;56(3):M146–56. https://doi.org/10.1093/gerona/56.3.m146.

    Article  CAS  PubMed  Google Scholar 

  20. Mitnitski AB, Mogilner AJ, Rockwood K. Accumulation of deficits as a proxy measure of aging. ScientificWorldJournal. 2001;1:323–36. Published 2001 Aug 8. https://doi.org/10.1100/tsw.2001.58.

  21. Yanase T, Yanagita I, Muta K, Nawata H. Frailty in elderly diabetes patients. Endocr J. 2018;65(1):1–11. https://doi.org/10.1507/endocrj.EJ17-0390.

    Article  PubMed  Google Scholar 

  22. Xue QL. The frailty syndrome: definition and natural history. Clin Geriatr Med. 2011;27(1):1–15. https://doi.org/10.1016/j.cger.2010.08.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Won CW. Frailty: its scope and implications for geriatricians. Ann Geriatr Med Res. 2019;23(3):95–7.

    Article  Google Scholar 

  24. Mogal H, Vermilion SA, Dodson R, Hsu FC, Howerton R, Shen P, et al. Modified frailty index predicts morbidity and mortality after pancreaticoduodenectomy. Ann Surg Oncol. 2017;24(6):1714–21. https://doi.org/10.1245/s10434-016-5715-0.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Al-Khamis A, Warner C, Park J, et al. Modified frailty index predicts early outcomes after colorectal surgery: an ACS-NSQIP study. Color Dis. 2019;21(10):1192–205. https://doi.org/10.1111/codi.14725.

    Article  CAS  Google Scholar 

  26. Subramaniam S, Aalberg JJ, Soriano RP, Divino CM. New 5-factor modified frailty index using American College of Surgeons NSQIP data. J Am Coll Surg. 2018;226(2):173–81. https://doi.org/10.1016/j.jamcollsurg.2017.11.005.

    Article  PubMed  Google Scholar 

  27. Kristjansson SR, Nesbakken A, Jordhøy MS, Skovlund E, Audisio RA, Johannessen HO, et al. Comprehensive geriatric assessment can predict complications in elderly patients after elective surgery for colorectal cancer: a prospective observational cohort study. Crit Rev Oncol Hematol. 2010;76(3):208–17. https://doi.org/10.1016/j.critrevonc.2009.11.002.

    Article  PubMed  Google Scholar 

  28. National Institutes of Health Consensus Development Conference Statement: geriatric assessment methods for clinical decision-making. J Am Geriatr Soc. 1988;36(4):342–7. https://doi.org/10.1111/j.1532-5415.1988.tb02362.x.

  29. Rolfson DB, Majumdar SR, Tsuyuki RT, Tahir A, Rockwood K. Validity and reliability of the Edmonton Frail Scale. Age Ageing. 2006;35(5):526–9. https://doi.org/10.1093/ageing/afl041.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Tapper EB, Finkelstein D, Mittleman MA, Piatkowski G, Lai M. Standard assessments of frailty are validated predictors of mortality in hospitalized patients with cirrhosis. Hepatology. 2015;62(2):584–90. https://doi.org/10.1002/hep.27830.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Taleban S, Toosizadeh N, Junna S, Golden T, Ghazala S, Wadeea R, et al. Frailty assessment predicts acute outcomes in patients undergoing screening colonoscopy. Dig Dis Sci. 2018;63(12):3272–80. https://doi.org/10.1007/s10620-018-5129-x.

    Article  PubMed  Google Scholar 

  32. Lai JC, Covinsky KE, McCulloch CE, Feng S. The liver frailty index improves mortality prediction of the subjective clinician assessment in patients with cirrhosis. Am J Gastroenterol. 2018;113(2):235–42. https://doi.org/10.1038/ajg.2017.443.

    Article  PubMed  Google Scholar 

  33. Lai JC, Covinsky KE, Dodge JL, Boscardin WJ, Segev DL, Roberts JP, et al. Development of a novel frailty index to predict mortality in patients with end-stage liver disease. Hepatology. 2017;66(2):564–74. https://doi.org/10.1002/hep.29219.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol. 1994;49(2):M85–94. https://doi.org/10.1093/geronj/49.2.m85.

    Article  CAS  PubMed  Google Scholar 

  35. Pavasini R, Guralnik J, Brown JC, et al. Short physical performance battery and all-cause mortality: systematic review and meta-analysis. BMC Med. 2016;14(1):215. Published 2016 Dec 22. https://doi.org/10.1186/s12916-016-0763-7.

  36. Carey EJ, Steidley DE, Aqel BA, Byrne TJ, Mekeel KL, Rakela J, et al. Six-minute walk distance predicts mortality in liver transplant candidates. Liver Transpl. 2010;16(12):1373–8. https://doi.org/10.1002/lt.22167.

    Article  PubMed  Google Scholar 

  37. Cederholm T, Barazzoni R, Austin P, Ballmer P, Biolo G, Bischoff SC, et al. ESPEN guidelines on definitions and terminology of clinical nutrition. Clin Nutr. 2017;36(1):49–64. https://doi.org/10.1016/j.clnu.2016.09.004.

    Article  CAS  PubMed  Google Scholar 

  38. Buchard B, Boirie Y, Cassagnes L, Lamblin G, Coilly A, Abergel A. Assessment of malnutrition, sarcopenia and frailty in patients with cirrhosis: which tools should we use in clinical practice? Nutrients. 2020;12(1):186. Published 2020 Jan 9. https://doi.org/10.3390/nu12010186.

  39. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159(4):413–21. https://doi.org/10.1093/aje/kwh058.

    Article  PubMed  Google Scholar 

  40. Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc. 2002;50(5):889–96. https://doi.org/10.1046/j.1532-5415.2002.50216.x.

    Article  PubMed  Google Scholar 

  41. Woo J, Ho SC, Sham A. Longitudinal changes in body mass index and body composition over 3 years and relationship to health outcomes in Hong Kong Chinese age 70 and older. J Am Geriatr Soc. 2001;49(6):737–46. https://doi.org/10.1046/j.1532-5415.2001.49150.x.

    Article  CAS  PubMed  Google Scholar 

  42. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International working group on sarcopenia. J Am Med Dir Assoc. 2011;12(4):249–56. https://doi.org/10.1016/j.jamda.2011.01.003.

    Article  PubMed  Google Scholar 

  43. Tandon P, Ney M, Irwin I, Ma MM, Gramlich L, Bain VG, et al. Severe muscle depletion in patients on the liver transplant wait list: its prevalence and independent prognostic value. Liver Transpl. 2012;18(10):1209–16. https://doi.org/10.1002/lt.23495.

    Article  PubMed  Google Scholar 

  44. Ebadi M, Bhanji RA, Mazurak VC, Montano-Loza AJ. Sarcopenia in cirrhosis: from pathogenesis to interventions. J Gastroenterol. 2019;54(10):845–59. https://doi.org/10.1007/s00535-019-01605-6.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Carey EJ, Lai JC, Wang CW, Dasarathy S, Lobach I, Montano-Loza AJ, et al. A multicenter study to define sarcopenia in patients with end-stage liver disease. Liver Transpl. 2017;23(5):625–33. https://doi.org/10.1002/lt.24750.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Sinclair M, Gow PJ, Grossmann M, Angus PW. Review article: sarcopenia in cirrhosis--aetiology, implications and potential therapeutic interventions. Aliment Pharmacol Ther. 2016;43(7):765–77. https://doi.org/10.1111/apt.13549.

    Article  CAS  PubMed  Google Scholar 

  47. Carey EJ, Lai JC, Sonnenday C, Tapper EB, Tandon P, Duarte-Rojo A, et al. A North American expert opinion statement on sarcopenia in liver transplantation. Hepatology. 2019;70(5):1816–29. https://doi.org/10.1002/hep.30828.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Olesen SS, Büyükuslu A, Køhler M, Rasmussen HH, Drewes AM. Sarcopenia associates with increased hospitalization rates and reduced survival in patients with chronic pancreatitis. Pancreatology. 2019;19(2):245–51. https://doi.org/10.1016/j.pan.2019.01.006.

    Article  PubMed  Google Scholar 

  49. 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(6):1586–92. https://doi.org/10.1016/j.clnu.2016.10.004.

    Article  PubMed  Google Scholar 

  50. Lee CH, Yoon H, Oh DJ, Lee JM, Choi YJ, Shin CM, et al. The prevalence of sarcopenia and its effect on prognosis in patients with Crohn’s disease. Intest Res. 2020;18(1):79–84. https://doi.org/10.5217/ir.2019.00107.

    Article  PubMed  PubMed Central  Google Scholar 

  51. 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. JPEN J Parenter Enteral Nutr. 2017;41(4):592–600. https://doi.org/10.1177/0148607115612054.

    Article  PubMed  Google Scholar 

  52. Pedersen M, Cromwell J, Nau P. Sarcopenia is a predictor of surgical morbidity in inflammatory bowel disease. Inflamm Bowel Dis. 2017;23(10):1867–72. https://doi.org/10.1097/MIB.0000000000001166.

    Article  PubMed  Google Scholar 

  53. Gingrich A, Volkert D, Kiesswetter E, et al. Prevalence and overlap of sarcopenia, frailty, cachexia and malnutrition in older medical inpatients. BMC Geriatr. 2019;19(1):120. Published 2019 Apr 27. https://doi.org/10.1186/s12877-019-1115-1.

  54. Espinoza SE, Quiben M, Hazuda HP. Distinguishing comorbidity, disability, and frailty. Curr Geriatr Rep. 2018;7(4):201–9. https://doi.org/10.1007/s13670-018-0254-0.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Anderson G, Knickman JR. Changing the chronic care system to meet people’s needs. Health Aff (Millwood). 2001;20(6):146–60. https://doi.org/10.1377/hlthaff.20.6.146.

    Article  CAS  Google Scholar 

  56. Argyriou K, Kapsoritakis A, Oikonomou K, Manolakis A, Tsakiridou E, Potamianos S. Disability in patients with inflammatory bowel disease: correlations with quality of life and patient’s characteristics. Can J Gastroenterol Hepatol. 2017;2017:6138105–11. https://doi.org/10.1155/2017/6138105.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Machicado JD, Amann ST, Anderson MA, Abberbock J, Sherman S, Conwell DL, et al. Quality of life in chronic pancreatitis is determined by constant pain, disability/unemployment, current smoking, and associated co-morbidities. Am J Gastroenterol. 2017;112(4):633–42. https://doi.org/10.1038/ajg.2017.42.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Lai JC, Dodge JL, Sen S, Covinsky K, Feng S. Functional decline in patients with cirrhosis awaiting liver transplantation: results from the functional assessment in liver transplantation (FrAILT) study. Hepatology. 2016;63(2):574–80. https://doi.org/10.1002/hep.28316.

    Article  CAS  PubMed  Google Scholar 

  59. Dorner TE, Luger E, Tschinderle J, Stein KV, Haider S, Kapan A, et al. Association between nutritional status (MNA®-SF) and frailty (SHARE-FI) in acute hospitalised elderly patients. J Nutr Health Aging. 2014;18(3):264–9. https://doi.org/10.1007/s12603-013-0406-z.

    Article  CAS  PubMed  Google Scholar 

  60. Jeejeebhoy KN, Duerksen DR. Malnutrition in gastrointestinal disorders: detection and nutritional assessment. Gastroenterol Clin N Am. 2018;47(1):1–22. https://doi.org/10.1016/j.gtc.2017.09.002.

    Article  Google Scholar 

  61. Elliot Y, Sood AJ, Maatman TK, Colgate C, Zyromski NJ. Can baseline frailty metrics predict outcomes in necrotizing pancreatitis? Pancreas. Abstract presented at Digestive Disease Week on 5/2/20.

  62. Afilalo J, Karunananthan S, Eisenberg MJ, Alexander KP, Bergman H. Role of frailty in patients with cardiovascular disease. Am J Cardiol. 2009;103(11):1616–21. https://doi.org/10.1016/j.amjcard.2009.01.375.

    Article  PubMed  Google Scholar 

  63. Fried LP, Ferrucci L, Darer J, Williamson JD, Anderson G. Untangling the concepts of disability, frailty, and comorbidity: implications for improved targeting and care. J Gerontol A Biol Sci Med Sci. 2004;59(3):255–63. https://doi.org/10.1093/gerona/59.3.m255.

    Article  PubMed  Google Scholar 

  64. Graham JE, Snih SA, Berges IM, Ray LA, Markides KS, Ottenbacher KJ. Frailty and 10-year mortality in community-living Mexican American older adults. Gerontology. 2009;55(6):644–51. https://doi.org/10.1159/000235653.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Cron DC, Friedman JF, Winder GS, Thelen AE, Derck JE, Fakhoury JW, et al. Depression and frailty in patients with end-stage liver disease referred for transplant evaluation. Am J Transplant. 2016;16(6):1805–11. https://doi.org/10.1111/ajt.13639.

    Article  CAS  PubMed  Google Scholar 

  66. Tandon P, Tangri N, Thomas L, Zenith L, Shaikh T, Carbonneau M, et al. A rapid bedside screen to predict unplanned hospitalization and death in outpatients with cirrhosis: a prospective evaluation of the clinical frailty scale. Am J Gastroenterol. 2016;111(12):1759–67. https://doi.org/10.1038/ajg.2016.303.

    Article  PubMed  Google Scholar 

  67. Bhanji RA, Narayanan P, Moynagh MR, Takahashi N, Angirekula M, Kennedy CC, et al. Differing impact of sarcopenia and frailty in nonalcoholic steatohepatitis and alcoholic liver disease. Liver Transpl. 2019;25(1):14–24. https://doi.org/10.1002/lt.25346.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Montano-Loza AJ, Duarte-Rojo A, Meza-Junco J, et al. Inclusion of sarcopenia within MELD (MELD-Sarcopenia) and the prediction of mortality in patients with cirrhosis. Clin Transl Gastroenterol. 2015;6(7):e102. Published 2015 Jul 16. https://doi.org/10.1038/ctg.2015.31.

  69. Lai JC, Volk ML, Strasburg D, Alexander N. Performance-based measures associate with frailty in patients with end-stage liver disease. Transplantation. 2016;100(12):2656–60. https://doi.org/10.1097/TP.0000000000001433.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kochar B, Cai W, Cagan A, Ananthakrishnan AN. Pretreatment frailty is independently associated with increased risk of infections after immunosuppression in patients with inflammatory bowel diseases [published online ahead of print, 2020 Feb 25]. Gastroenterology. 2020:S0016–5085(20)30243–2. https://doi.org/10.1053/j.gastro.2020.02.032 This was the first study to examine frailty as a predictor of poor outcomes after biologic and immunomodulatory therapy in the elderly population.

  71. Kochar B, Cai W, Cagan A, Ananthakrishnan A. Frailty is independently associated with increased mortality in patient with inflammatory bowel disease. IBD: special populations‚ conception‚ adolescent‚ and older. Abstract presented at Digestive Disease Week on 5/2/20.

  72. Chen X, Mao G, Leng SX. Frailty syndrome: an overview. Clin Interv Aging. 2014;9:433–41. Published 2014 Mar 19. https://doi.org/10.2147/CIA.S45300.

  73. Fried LP, Walston J. Frailty and failure to thrive. In: Hazzard WR, Blass JP, Ettinger Jr WH, Halter JB, Ouslander J, editors. Principles of geriatric medicine and gerontology. 5th ed. New York: McGraw-Hill; 2003. p. 1487–502.

    Google Scholar 

  74. Chen Y, Liu S, Leng SX. Chronic low-grade inflammatory phenotype (CLIP) and senescent immune dysregulation. Clin Ther. 2019;41(3):400–9. https://doi.org/10.1016/j.clinthera.2019.02.001.

    Article  PubMed  Google Scholar 

  75. Frisoli A Jr, Ingham SJ, Paes ÂT, et al. Frailty predictors and outcomes among older patients with cardiovascular disease: data from Fragicor. Arch Gerontol Geriatr. 2015;61(1):1–7. https://doi.org/10.1016/j.archger.2015.03.001.

    Article  PubMed  Google Scholar 

  76. Li Y, Zou Y, Wang S, et al. A pilot study of the frail scale on predicting outcomes in Chinese elderly people with type 2 diabetes. J Am Med Dir Assoc. 2015;16(8):714.e7–714.e12. https://doi.org/10.1016/j.jamda.2015.05.019.

    Article  Google Scholar 

  77. Leng S, Fried LP. Inflammatory markers and frailty. In: Fulop T, Franceschi C, Hirokawa K, Pawelec G, editors. Handbook on immunosenescence: basic understanding and clinical applications. New York: Springer; 2009. p. 1293–303.

    Chapter  Google Scholar 

  78. Yao X, Li H, Leng SX. Inflammation and immune system alterations in frailty. Clin Geriatr Med. 2011;27(1):79–87. https://doi.org/10.1016/j.cger.2010.08.002.

    Article  PubMed  PubMed Central  Google Scholar 

  79. Li H, Manwani B, Leng SX. Frailty, inflammation, and immunity. Aging Dis. 2011;2(6):466–73.

    PubMed  PubMed Central  Google Scholar 

  80. Leng SX, Margolick JB. Aging, sex, inflammation, frailty, and CMV and HIV infections. Cell Immunol. 2020;348:104024. https://doi.org/10.1016/j.cellimm.2019.104024.

    Article  CAS  PubMed  Google Scholar 

  81. Jagger A, Shimojima Y, Goronzy JJ, Weyand CM. Regulatory T cells and the immune aging process: a mini-review. Gerontology. 2014;60(2):130–7. https://doi.org/10.1159/000355303.

    Article  CAS  PubMed  Google Scholar 

  82. Norouzinia M, Chaleshi V, Alizadeh AHM, Zali MR. Biomarkers in inflammatory bowel diseases: insight into diagnosis, prognosis and treatment. Gastroenterol Hepatol Bed Bench. 2017;10(3):155–67.

    PubMed  PubMed Central  Google Scholar 

  83. LeBlanc JF, Wiseman D, Lakatos PL, Bessissow T. Elderly patients with inflammatory bowel disease: updated review of the therapeutic landscape. World J Gastroenterol. 2019;25(30):4158–71. https://doi.org/10.3748/wjg.v25.i30.4158.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Mekli K, Marshall A, Nazroo J, Vanhoutte B, Pendleton N. Genetic variant of Interleukin-18 gene is associated with the Frailty Index in the English Longitudinal Study of Ageing. Age Ageing. 2015;44(6):938–42. https://doi.org/10.1093/ageing/afv122.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Sikka G, Miller KL, Steppan J, Pandey D, Jung SM, Fraser CD III, et al. Interleukin 10 knockout frail mice develop cardiac and vascular dysfunction with increased age. Exp Gerontol. 2013;48(2):128–35. https://doi.org/10.1016/j.exger.2012.11.001.

    Article  CAS  PubMed  Google Scholar 

  86. Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26:26191. Published 2015 Feb 2. https://doi.org/10.3402/mehd.v26.26191.

  87. Menees S, Chey W. The gut microbiome and irritable bowel syndrome. F1000Res. 2018;7:F1000 Faculty Rev-1029. Published 2018 Jul 9. https://doi.org/10.12688/f1000research.14592.1.

  88. Jackson MA, Jeffery IB, Beaumont M, et al. Signatures of early frailty in the gut microbiota [published correction appears in Genome Med. 2016;8(1):21. Jackson, Matt [corrected to Jackson, Matthew A]]. Genome Med. 2016;8(1):8. Published 2016 Jan 29. https://doi.org/10.1186/s13073-016-0262-7.

  89. Thota VR, Dacha S, Natarajan A, Nerad J. Eggerthella lenta bacteremia in a Crohn’s disease patient after ileocecal resection. Future Microbiol. 2011;6(5):595–7. https://doi.org/10.2217/fmb.11.31.

    Article  PubMed  Google Scholar 

  90. Baumgart DC, Carding SR. Inflammatory bowel disease: cause and immunobiology. Lancet. 2007;369(9573):1627–40. https://doi.org/10.1016/S0140-6736(07)60750-8.

    Article  CAS  PubMed  Google Scholar 

  91. Sokol H, Seksik P. The intestinal microbiota in inflammatory bowel diseases: time to connect with the host. Curr Opin Gastroenterol. 2010;26(4):327–31. https://doi.org/10.1097/MOG.0b013e328339536b.

    Article  PubMed  Google Scholar 

  92. Sokol H, Pigneur B, Watterlot L, Lakhdari O, Bermudez-Humaran LG, Gratadoux JJ, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105(43):16731–6. https://doi.org/10.1073/pnas.0804812105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104(34):13780–5. https://doi.org/10.1073/pnas.0706625104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Xu D, Chen VL, Steiner CA, et al. Efficacy of fecal microbiota transplantation in irritable bowel syndrome: a systematic review and meta-analysis. Am J Gastroenterol. 2019;114(7):1043–50. https://doi.org/10.14309/ajg.0000000000000198.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Paramsothy S, Kamm MA, Kaakoush NO, Walsh AJ, van den Bogaerde J, Samuel D, et al. Multidonor intensive faecal microbiota transplantation for active ulcerative colitis: a randomized placebo-controlled trial. Lancet. 2017;389(10075):1218–28. https://doi.org/10.1016/S0140-6736(17)30182-4.

    Article  PubMed  Google Scholar 

  96. Moayyedi P, Surette MG, Kim PT, et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology. 2015;149(1):102–109.e6. https://doi.org/10.1053/j.gastro.2015.04.001.

    Article  PubMed  Google Scholar 

  97. Vaughn BP, Vatanen T, Allegretti JR, Bai A, Xavier RJ, Korzenik J, et al. Increased intestinal microbial diversity following fecal microbiota transplant for active Crohn’s disease. Inflamm Bowel Dis. 2016;22(9):2182–90. https://doi.org/10.1097/MIB.0000000000000893.

    Article  PubMed  PubMed Central  Google Scholar 

  98. Gutin L, Piceno Y, Fadrosh D, Lynch K, Zydek M, Kassam Z, et al. Fecal microbiota transplant for Crohn disease: a study evaluating safety, efficacy, and microbiome profile. United European Gastroenterol J. 2019;7(6):807–14. https://doi.org/10.1177/2050640619845986.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Wagner D, DeMarco MM, Amini N, Buttner S, Segev D, Gani F, et al. Role of frailty and sarcopenia in predicting outcomes among patients undergoing gastrointestinal surgery. World J Gastrointest Surg. 2016;8(1):27–40. https://doi.org/10.4240/wjgs.v8.i1.27.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Makary MA, Segev DL, Pronovost PJ, Syin D, Bandeen-Roche K, Patel P, et al. Frailty as a predictor of surgical outcomes in older patients. J Am Coll Surg. 2010;210(6):901–8. https://doi.org/10.1016/j.jamcollsurg.2010.01.028.

    Article  PubMed  Google Scholar 

  101. Ryan E, McNicholas D, Creavin B, Kelly ME, Walsh T, Beddy D. Sarcopenia and inflammatory bowel disease: a systematic review. Inflamm Bowel Dis. 2019;25(1):67–73. https://doi.org/10.1093/ibd/izy212.

    Article  PubMed  Google Scholar 

  102. Hodari A, Hammoud ZT, Borgi JF, Tsiouris A, Rubinfeld IS. Assessment of morbidity and mortality after esophagectomy using a modified frailty index. Ann Thorac Surg. 2013;96(4):1240–5. https://doi.org/10.1016/j.athoracsur.2013.05.051.

    Article  PubMed  Google Scholar 

  103. Valero V 3rd, Amini N, Spolverato G, et al. Sarcopenia adversely impacts postoperative complications following resection or transplantation in patients with primary liver tumors. J Gastrointest Surg. 2015;19(2):272–81. https://doi.org/10.1007/s11605-014-2680-4.

    Article  PubMed  Google Scholar 

  104. Harimoto N, Shirabe K, Yamashita YI, Ikegami T, Yoshizumi T, Soejima Y, et al. Sarcopenia as a predictor of prognosis in patients following hepatectomy for hepatocellular carcinoma. Br J Surg. 2013;100(11):1523–30. https://doi.org/10.1002/bjs.9258.

    Article  CAS  PubMed  Google Scholar 

  105. Neuman HB, Weiss JM, Leverson G, O’Connor ES, Greenblatt DY, LoConte NK, et al. Predictors of short-term postoperative survival after elective colectomy in colon cancer patients ≥ 80 years of age. Ann Surg Oncol. 2013;20(5):1427–35. https://doi.org/10.1245/s10434-012-2721-8.

    Article  PubMed  PubMed Central  Google Scholar 

  106. Zorbas KA, William LA, Farkas DT, Shah A, Velanovich V, Karachristos A. The enhanced Modified Frailty Index Score is a better predictor for post-operative morbidity and mortality after whipple procedure compared to modified frailty index score. Pancreas. Abstract presented at Digestive Disease Week on 5/2/20.

  107. Lai JC, Feng S, Terrault NA, Lizaola B, Hayssen H, Covinsky K. Frailty predicts waitlist mortality in liver transplant candidates. Am J Transplant. 2014;14(8):1870–9. https://doi.org/10.1111/ajt.12762.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Sinclair M, Poltavskiy E, Dodge JL, Lai JC. Frailty is independently associated with increased hospitalization days in patients on the liver transplant waitlist. World J Gastroenterol. 2017;23(5):899–905. https://doi.org/10.3748/wjg.v23.i5.899.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Lai JC, Segev DL, McColloch CE, Covinsky KE, Dodge JL, Feng S. Physical frailty after liver transplantation. Am J Transplant. 2018;18(8):1986–94.

    Article  Google Scholar 

  110. •• Fozouni L, Mohamad Y, Lebsack A, Freise C, Stock P, Lai JC. Frailty is associated with increased rates of acute cellular rejection within 3 months after liver transplantation. Liver Transpl. 2020;26(3):390–6. https://doi.org/10.1002/lt.25669 This study shows that pre-transplant frailty can predict post-liver transplant rejection. It highlights frailty as a valuable predictor of post-transplant outcomes other than mortality in those awaiting liver transplantation.

    Article  PubMed  Google Scholar 

  111. Jeuring SF, van den Heuvel TR, Zeegers MP, et al. Epidemiology and long-term outcome of inflammatory bowel disease diagnosed at elderly age-an increasing distinct entity? Inflamm Bowel Dis. 2016;22(6):1425–34. https://doi.org/10.1097/MIB.0000000000000738.

    Article  PubMed  Google Scholar 

  112. Asscher VER, Lee-Kong FVY, Kort ED, van Deudekom FJ, Mooijaart SP, Maljaars PWJ. Systematic review: components of a comprehensive geriatric assessment in inflammatory bowel disease-a potentially promising but often neglected risk stratification. J Crohns Colitis. 2019;13(11):1418–32. https://doi.org/10.1093/ecco-jcc/jjz082.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Yajnik V, Khan N, Dubinsky M, Axler J, James A, Abhyankar B, et al. Efficacy and safety of vedolizumab in ulcerative colitis and Crohn’s disease patients stratified by age. Adv Ther. 2017;34(2):542–59. https://doi.org/10.1007/s12325-016-0467-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Feagan BG, Sandborn WJ, Gasink C, Jacobstein D, Lang Y, Friedman JR, et al. Ustekinumab as induction and maintenance therapy for Crohn’s disease. N Engl J Med. 2016;375(20):1946–60. https://doi.org/10.1056/NEJMoa1602773.

    Article  CAS  PubMed  Google Scholar 

  115. Walston J, Buta B, Xue QL. Frailty screening and interventions: considerations for clinical practice. Clin Geriatr Med. 2018;34(1):25–38. https://doi.org/10.1016/j.cger.2017.09.004.

    Article  PubMed  PubMed Central  Google Scholar 

  116. Puts MTE, Toubasi S, Andrew MK, Ashe MC, Ploeg J, Atkinson E, et al. Interventions to prevent or reduce the level of frailty in community-dwelling older adults: a scoping review of the literature and international policies. Age Ageing. 2017;46(3):383–92. https://doi.org/10.1093/ageing/afw247.

    Article  PubMed  PubMed Central  Google Scholar 

  117. Fernando SM, McIsaac DI, Perry JJ, et al. Frailty and associated outcomes and resource utilization among older ICU patients with suspected infection. Crit Care Med. 2019;47(8):e669–76. https://doi.org/10.1097/CCM.0000000000003831.

    Article  PubMed  Google Scholar 

  118. Bortz WM 2nd. A conceptual framework of frailty: a review. J Gerontol A Biol Sci Med Sci. 2002;57(5):M283–8. https://doi.org/10.1093/gerona/57.5.m283.

    Article  PubMed  Google Scholar 

  119. Chin A, Paw MJ, van Uffelen JG, Riphagen I, van Mechelen W. The functional effects of physical exercise training in frail older people : a systematic review. Sports Med. 2008;38(9):781–93. https://doi.org/10.2165/00007256-200838090-00006.

    Article  Google Scholar 

  120. Bi L, Triadafilopoulos G. Exercise and gastrointestinal function and disease: an evidence-based review of risks and benefits. Clin Gastroenterol Hepatol. 2003;1(5):345–55. https://doi.org/10.1053/s1542-3565(03)00178-2.

    Article  PubMed  Google Scholar 

  121. Orci LA, Gariani K, Oldani G, Delaune V, Morel P, Toso C. Exercise-based interventions for nonalcoholic fatty liver disease: a meta-analysis and meta-regression. Clin Gastroenterol Hepatol. 2016;14(10):1398–411. https://doi.org/10.1016/j.cgh.2016.04.036.

    Article  PubMed  Google Scholar 

  122. Dunn MA, Josbeno DA, Schmotzer AR, Tevar AD, DiMartini AF, Landsittel DP, et al. The gap between clinically assessed physical performance and objective physical activity in liver transplant candidates. Liver Transpl. 2016;22(10):1324–32. https://doi.org/10.1002/lt.24506.

    Article  PubMed  Google Scholar 

  123. Carli F, Zavorsky GS. Optimizing functional exercise capacity in the elderly surgical population. Curr Opin Clin Nutr Metab Care. 2005;8(1):23–32. https://doi.org/10.1097/00075197-200501000-00005.

    Article  PubMed  Google Scholar 

  124. Le Roy B, Pereira B, Bouteloup C, et al. Effect of prehabilitation in gastro-oesophageal adenocarcinoma: study protocol of a multicentric, randomized, control trial-the PREHAB study. BMJ Open. 2016;6(12):e012876. Published 2016 Dec 7. https://doi.org/10.1136/bmjopen-2016-012876.

  125. Gillis C, Li C, Lee L, Awasthi R, Augustin B, Gamsa A, et al. Prehabilitation versus rehabilitation: a randomized control trial in patients undergoing colorectal resection for cancer. Anesthesiology. 2014;121(5):937–47. https://doi.org/10.1097/ALN.0000000000000393.

    Article  PubMed  Google Scholar 

  126. Ngo-Huang A, Parker NH, Bruera E, Lee RE, Simpson R, O’Connor DP, et al. Home-based exercise prehabilitation during preoperative treatment for pancreatic cancer is associated with improvement in physical function and quality of life. Integr Cancer Ther. 2019;18:1534735419894061. https://doi.org/10.1177/1534735419894061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. •• Ng TP, Feng L, Nyunt MS, et al. Nutritional, physical, cognitive, and combination interventions and frailty reversal among older adults: a randomized controlled trial. Am J Med. 2015;128(11):1225–1236.e1. https://doi.org/10.1016/j.amjmed.2015.06.017 This study suggests that frailty intervention particularly a multimodal approach can improve frailty scores at various time intervals.

    Article  PubMed  Google Scholar 

  128. Byrne G, Rosenfeld G, Leung Y, Qian H, Raudzus J, Nunez C, et al. Prevalence of anxiety and depression in patients with inflammatory bowel disease. Can J Gastroenterol Hepatol. 2017;2017:6496727–6. https://doi.org/10.1155/2017/6496727.

    Article  PubMed  PubMed Central  Google Scholar 

  129. Huang X, Liu X, Yu Y. Depression and chronic liver diseases: are there shared underlying mechanisms? Front Mol Neurosci. 2017;10:134. Published 2017 May 8. https://doi.org/10.3389/fnmol.2017.00134.

  130. Jeppe CY, Szabo CP, Smith MD. Chronic pancreatitis, depression and substance use disorders: a not uncommon combination. S Afr Med J. 2015;105(3):179–80. https://doi.org/10.7196/samj.8885.

    Article  CAS  PubMed  Google Scholar 

  131. Soysal P, Veronese N, Thompson T, Kahl KG, Fernandes BS, Prina AM, et al. Relationship between depression and frailty in older adults: a systematic review and meta-analysis. Ageing Res Rev. 2017;36:78–87. https://doi.org/10.1016/j.arr.2017.03.005.

    Article  PubMed  Google Scholar 

  132. Morley JE. Pharmacologic options for the treatment of sarcopenia. Calcif Tissue Int. 2016;98(4):319–33. https://doi.org/10.1007/s00223-015-0022-5.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Thompson MD.

Additional information

Publisher’s Note

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

This article is part of the Topical Collection on Gastroenterology for Geriatric Patients

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thompson, C., Taleban, S. Incorporating Frailty in the Treatment Program of Elderly Patients with Gastrointestinal Disease. Curr Treat Options Gastro 18, 635–656 (2020). https://doi.org/10.1007/s11938-020-00310-1

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11938-020-00310-1

Keywords

Navigation