Fatigue in Inflammatory Bowel Diseases: Etiologies and Management

Angelica Nocerino, Andrew Nguyen, Manasi Agrawal, Anjali Mone, Komal Lakhani, Arun Swaminath, Angelica Nocerino, Andrew Nguyen, Manasi Agrawal, Anjali Mone, Komal Lakhani, Arun Swaminath

Abstract

Fatigue is a burdensome, multidimensional, and multifactorial symptom that is associated with a wide array of chronic illnesses, specifically occurring in nearly 50% of patients with inflammatory bowel disease (IBD). Although common, given its subjective nature, physicians often under-recognize and undertreat this debilitating symptom. There are multiple etiologies that can contribute to fatigue in patients with IBD, including disease activity, anemia, medications, psychosomatic symptoms, and alterations to the gut-brain axis. The management of fatigue in IBD can be challenging, as it is often times multifaceted. In this review, we summarize the available tools for the diagnosis and measurement of fatigue, discuss etiologies, and make recommendations for their management. We identify knowledge gaps for the workup and treatment of fatigue and propose an algorithm to aid physicians in the evaluation and management of fatigue in this unique population. However, future research is needed to address several areas of knowledge deficits and improve the management of fatigue in IBD.

Keywords: Anemia; Crohn’s disease; Disease activity; Fatigue; Inflammatory bowel disease; Ulcerative colitis.

Figures

Fig. 1
Fig. 1
Validated questionnaires for assessing fatigue in IBD
Fig. 2
Fig. 2
Algorithm for the systematic workup of fatigue and treatment based on the etiology. IBD inflammatory bowel disease, IMM immunomodulators

References

    1. Barsevick AM, Cleeland CS, Manning DC, et al. ASCPRO recommendations for the assessment of fatigue as an outcome in clinical trials. J Pain Sympt Manag. 2010;39(6):1086–1099.
    1. Czuber-Dochan W, Norton C, Bassett P, et al. Development and psychometric testing of inflammatory bowel disease fatigue (IBD-F) patient self-assessment scale. J Crohns Colitis. 2014;8(11):1398–1406.
    1. Jelsness-Jørgensen LP, Bernklev T, Henriksen M, Torp R, Moum BA. Chronic fatigue is more prevalent in patients with inflammatory bowel disease than in healthy controls. Inflamm Bowel Dis. 2011;17(7):1564–1572.
    1. Grimstad T, Norheim KB, Isaksen K, et al. Fatigue in newly diagnosed inflammatory bowel disease. J Crohns Colitis. 2015;9(9):725–730.
    1. Graff LA, Clara I, Walker JR, et al. Changes in fatigue over 2 years are associated with activity of inflammatory bowel disease and psychological factors. Clin Gastroenterol Hepatol. 2013;11(9):1140–1146.
    1. Huppertz-Hauss G, Hoivik ML, Jelsness-Jorgensen LP, et al. Fatigue in a population-based cohort of patients with inflammatory bowel disease 20 years after diagnosis: the IBSEN study. Scand J Gastroenterol. 2017;52(3):351–358.
    1. Lakhani KAM, Bhardwaj R, Swaminath A. Fatigue is inversely associated with endoscopic but not histologic remission in IBD patients. ACG Annual Scientific Meeting and Postgraduate Course. PO511. 2019 Oct 27.
    1. Farrell D, McCarthy G, Savage E. Self-reported symptom burden in individuals with inflammatory bowel disease. J Crohns Colitis. 2016;10(3):315–322.
    1. Jonefjall B, Simren M, Lasson A, Ohman L, Strid H. Psychological distress, iron deficiency, active disease and female gender are independent risk factors for fatigue in patients with ulcerative colitis. United Eur Gastroenterol J. 2018;6(1):148–158.
    1. Bager Palle, Vestergaard Charlotte, Juul Therese, Dahlerup Jens F. Population-based normative data for the inflammatory bowel disease fatigue scale – IBD-F. Scandinavian Journal of Gastroenterology. 2018;53(10-11):1274–1279.
    1. Jelsness-Jørgensen LP, Bernklev T, Henriksen M, Torp R, Moum BA. Chronic fatigue is associated with impaired health-related quality of life in inflammatory bowel disease. Aliment Pharmacol Ther. 2011;33(1):106–114.
    1. Romberg-Camps MJ, Bol Y, Dagnelie PC, et al. Fatigue and health-related quality of life in inflammatory bowel disease: results from a population-based study in the Netherlands: the IBD-South Limburg cohort. Inflamm Bowel Dis. 2010;16(12):2137–2147.
    1. Cohen BL, Zoëga H, Shah SA, et al. Fatigue is highly associated with poor health-related quality of life, disability and depression in newly-diagnosed patients with inflammatory bowel disease, independent of disease activity. Aliment Pharmacol Ther. 2014;39(8):811–822.
    1. Zand A, van Deen WK, Inserra EK, et al. Presenteeism in inflammatory bowel diseases: a hidden problem with significant economic impact. Inflamm Bowel Dis. 2015;21(7):1623–1630.
    1. Enns MW, Bernstein CN, Kroeker K, et al. The association of fatigue, pain, depression and anxiety with work and activity impairment in immune mediated inflammatory diseases. PLoS One. 2018;13(6):e0198975.
    1. Smets EM, Garssen B, Bonke B, De Haes JC. The multidimensional fatigue inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res. 1995;39(3):315–325.
    1. Belza BL, Henke CJ, Yelin EH, Epstein WV, Gilliss CL. Correlates of fatigue in older adults with rheumatoid arthritis. Nurs Res. 1993;42(2):93–99.
    1. Tinsley A, Macklin EA, Korzenik JR, Sands BE. Validation of the functional assessment of chronic illness therapy-fatigue (FACIT-F) in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2011;34(11–12):1328–1336.
    1. Chalder T, Berelowitz G, Pawlikowska T, et al. Development of a fatigue scale. J Psychosom Res. 1993;37(2):147–153.
    1. Norton C, Czuber-Dochan W, Bassett P, et al. Assessing fatigue in inflammatory bowel disease: comparison of three fatigue scales. Aliment Pharmacol Ther. 2015;42(2):203–211.
    1. van Langenberg DR, Gibson PR. Systematic review: fatigue in inflammatory bowel disease. Aliment Pharmacol Ther. 2010;32(2):131–143.
    1. Irvine EJ, Feagan B, Rochon J, et al. Quality of life: a valid and reliable measure of therapeutic efficacy in the treatment of inflammatory bowel disease. Canadian Crohn’s Relapse Prevention Trial Study Group. Gastroenterology. 1994;106(2):287–296.
    1. Ware J, Kosinski M, Bjorner J, Turner-Bowker D, Gandek B, Maruish M. Development. User's Manual for the SF-36v2® Health Survey. Lincoln (RI): QualityMetric Incorporated; 2007.
    1. US Department of Health and Human Services Food and Drug Administration Center for Drug Evaluation and Research (CDER). Ulcerative colitis: clinical trial endpoints guidance for industry. 2016 Aug. . Accessed 12 Aug 2019.
    1. Konig HH, Ulshofer A, Gregor M, et al. Validation of the EuroQol questionnaire in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2002;14(11):1205–1215.
    1. Papanicolaou DA, Amsterdam JD, Levine S, et al. Neuroendocrine aspects of chronic fatigue syndrome. NeuroImmunoModulation. 2004;11(2):65–74.
    1. Bower JE, Ganz PA, Aziz N, Fahey JL. Fatigue and proinflammatory cytokine activity in breast cancer survivors. Psychosom Med. 2002;64(4):604–611.
    1. Patarca R. Cytokines and chronic fatigue syndrome. Ann N Y Acad Sci. 2001;933:185–200.
    1. Vogelaar L, de Haar C, Aerts BR, et al. Fatigue in patients with inflammatory bowel disease is associated with distinct differences in immune parameters. Clin Exp Gastroenterol. 2017;10:83–90.
    1. Carabotti M, Scirocco A, Maselli MA, Severi C. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann Gastroenterol. 2015;28(2):203–209.
    1. Lucia Casadonte CJ, Brown J, Strople J, Neighbors K, Fei L, Alonso EM. Low insulin-like growth factor-1 influences fatigue and quality of life in children with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2018;67(5):616–621.
    1. Kreijne JE, Lie MR, Vogelaar L, van der Woude CJ. Practical guideline for fatigue management in inflammatory bowel disease. J Crohns Colitis. 2016;10(1):105–111.
    1. Vogelaar L, van’t Spijker A, van Tilburg AJ, Kuipers EJ, Timman R, van der Woude CJ. Determinants of fatigue in Crohn’s disease patients. Eur J Gastroenterol Hepatol. 2013;25(2):246–251.
    1. Artom M, Czuber-Dochan W, Sturt J, Norton C. Targets for health interventions for inflammatory bowel disease-fatigue. J Crohns Colitis. 2016;10(7):860–869.
    1. Gong J, Zuo L, Guo Z, et al. Impact of disease activity on resting energy expenditure and body composition in adult Crohn’s disease: a prospective longitudinal assessment. JPEN J Parenter Enteral Nutr. 2015;39(6):713–718.
    1. Elsherif Yasser, Alexakis Christopher, Mendall Michael. Determinants of Weight Loss prior to Diagnosis in Inflammatory Bowel Disease: A Retrospective Observational Study. Gastroenterology Research and Practice. 2014;2014:1–7.
    1. Louati K, Berenbaum F. Fatigue in chronic inflammation—a link to pain pathways. Arthrit Res Ther. 2015;17:254.
    1. Dantzer R, O’Connor JC, Freund GG, Johnson RW, Kelley KW. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci. 2008;9(1):46–56.
    1. Villoria A, Garcia V, Dosal A, et al. Fatigue in out-patients with inflammatory bowel disease: prevalence and predictive factors. PLoS One. 2017;12(7):e0181435.
    1. Chavarria C, Casanova MJ, Chaparro M, et al. Prevalence and factors associated with fatigue in patients with inflammatory bowel disease: a multicenter study. J Crohns Colitis. 2019;13(8):996–1002.
    1. Feagan BG, Yan S, Bala M, Bao W, Lichtenstein GR. The effects of infliximab maintenance therapy on health-related quality of life. Am J Gastroenterol. 2003;98(10):2232–2238.
    1. Loftus EV, Feagan BG, Colombel JF, et al. Effects of adalimumab maintenance therapy on health-related quality of life of patients with Crohn’s disease: patient-reported outcomes of the CHARM trial. Am J Gastroenterol. 2008;103(12):3132–3141.
    1. Sandborn WJ, Feagan BG, Stoinov S, et al. Certolizumab pegol for the treatment of Crohn’s disease. N Engl J Med. 2007;357(3):228–238.
    1. Sands BE, Han C, Gasink C, et al. The effects of ustekinumab on health-related quality of life in patients with moderate to severe Crohn’s disease. J Crohns Colitis. 2018;12(8):883–895.
    1. Feagan BG, Reinisch W, Rutgeerts P, et al. The effects of infliximab therapy on health-related quality of life in ulcerative colitis patients. Am J Gastroenterol. 2007;102(4):794–802.
    1. Sandborn WJ, van Assche G, Reinisch W, et al. Adalimumab induces and maintains clinical remission in patients with moderate-to-severe ulcerative colitis. Gastroenterology. 2012;142(2):257–265.e3.
    1. Feagan BG, Patel H, Colombel JF, et al. Effects of vedolizumab on health-related quality of life in patients with ulcerative colitis: results from the randomised GEMINI 1 trial. Aliment Pharmacol Ther. 2017;45(2):264–275.
    1. Panes J, Vermeire S, Lindsay JO, et al. Tofacitinib in patients with ulcerative colitis: health-related quality of life in phase 3 randomised controlled induction and maintenance studies. J Crohns Colitis. 2018;12(2):145–156.
    1. Probert CS, Sebastian S, Gaya DR, et al. Golimumab induction and maintenance for moderate to severe ulcerative colitis: results from GO-COLITIS (Golimumab: a Phase 4, UK, open label, single arm study on its utilization and impact in ulcerative Colitis) BMJ Open Gastroenterol. 2018;5(1):e000212.
    1. Grimstad T, Norheim KB, Kvaløy JT, et al. Conventional treatment regimens for ulcerative colitis alleviate fatigue—an observational cohort study. Scand J Gastroenterol. 2016;51(10):1213–1219.
    1. Casellas F, de Barreiro Acosta M, Iglesias M, et al. Mucosal healing restores normal health and quality of life in patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2012;24(7):762–769.
    1. Swaminath A, Berlin EP, Cheifetz A, et al. The role of cannabis in the management of inflammatory bowel disease: a review of clinical, scientific, and regulatory information. Inflamm Bowel Dis. 2019;25(3):427–435.
    1. Howlett AC, Barth F, Bonner TI, et al. International union of pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev. 2002;54(2):161–202.
    1. Izzo AA, Sharkey KA. Cannabinoids and the gut: new developments and emerging concepts. Pharmacol Ther. 2010;126(1):21–38.
    1. Lal S, Prasad N, Ryan M, et al. Cannabis use amongst patients with inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2011;23(10):891–896.
    1. Naftali T, Bar-Lev Schleider L, Dotan I, Lansky EP, Sklerovsky Benjaminov F, Konikoff FM. Cannabis induces a clinical response in patients with Crohn’s disease: a prospective placebo-controlled study. Clin Gastroenterol Hepatol. 2013;11(10):1276–1280.
    1. Irving PM, Iqbal T, Nwokolo C, et al. A randomized, double-blind, placebo-controlled, parallel-group, pilot study of cannabidiol-rich botanical extract in the symptomatic treatment of ulcerative colitis. Inflamm Bowel Dis. 2018;24(4):714–724.
    1. Bager P, Befrits R, Wikman O, et al. The prevalence of anemia and iron deficiency in IBD outpatients in Scandinavia. Scand J Gastroenterol. 2011;46(3):304–309.
    1. Gasche C, Lomer MC, Cavill I, Weiss G. Iron, anaemia, and inflammatory bowel diseases. Gut. 2004;53(8):1190–1197.
    1. Goldenberg BA, Graff LA, Clara I, et al. Is iron deficiency in the absence of anemia associated with fatigue in inflammatory bowel disease? Am J Gastroenterol. 2013;108(9):1392–1397.
    1. Madanchi M, Fagagnini S, Fournier N, et al. The relevance of vitamin and iron deficiency in patients with inflammatory bowel diseases in patients of the Swiss IBD cohort. Inflamm Bowel Dis. 2018;24(8):1768–1779.
    1. Battat R, Kopylov U, Szilagyi A, et al. Vitamin B12 deficiency in inflammatory bowel disease: prevalence, risk factors, evaluation, and management. Inflamm Bowel Dis. 2014;20(6):1120–1128.
    1. Egan LJ, Sandborn WJ. Methotrexate for inflammatory bowel disease: pharmacology and preliminary results. Mayo Clin Proc. 1996;71(1):69–80.
    1. Guagnozzi D, Lucendo AJ. Anemia in inflammatory bowel disease: a neglected issue with relevant effects. World J Gastroenterol. 2014;20(13):3542–3551.
    1. Plikat K, Rogler G, Scholmerich J. Coombs-positive autoimmune hemolytic anemia in Crohn’s disease. Eur J Gastroenterol Hepatol. 2005;17(6):661–666.
    1. Schwab M, Schaffeler E, Marx C, et al. Azathioprine therapy and adverse drug reactions in patients with inflammatory bowel disease: impact of thiopurine S-methyltransferase polymorphism. Pharmacogenetics. 2002;12(6):429–436.
    1. Dignass AU, Gasche C, Bettenworth D, et al. European consensus on the diagnosis and management of iron deficiency and anaemia in inflammatory bowel diseases. J Crohns Colitis. 2015;9(3):211–222.
    1. Lichtenstein GR, Loftus EV, Isaacs KL, Regueiro MD, Gerson LB, Sands BE. ACG clinical guideline: management of Crohn’s disease in adults. Am J Gastroenterol. 2018;113(4):481–517.
    1. Hou JK, Gasche C, Drazin NZ, et al. Assessment of gaps in care and the development of a care pathway for anemia in patients with inflammatory bowel diseases. Inflamm Bowel Dis. 2017;23(1):35–43.
    1. Aksan A, Isik H, Radeke HH, Dignass A, Stein J. Systematic review with network meta-analysis: comparative efficacy and tolerability of different intravenous iron formulations for the treatment of iron deficiency anaemia in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2017;45(10):1303–1318.
    1. Peyrin-Biroulet L, Lopez A, Cummings JRF, Dignass A, Detlie TE, Danese S. Review article: treating-to-target for inflammatory bowel disease-associated anaemia. Aliment Pharmacol Ther. 2018;48:610–617.
    1. Eiden KA. Nutritional consideration in inflammatory bowel disease. Pract Gastroenterol. 2003;27:33–54.
    1. Bulletins-Obstetrics CoP. Practice Bulletin No. 187: Neural Tube Defects. Obstet Gynecol 2017;130(6):e279–90.
    1. Hwang C, Ross V, Mahadevan U. Micronutrient deficiencies in inflammatory bowel disease: from A to zinc. Inflamm Bowel Dis. 2012;18(10):1961–1981.
    1. Lucendo AJ, De Rezende LC. Importance of nutrition in inflammatory bowel disease. World J Gastroenterol. 2009;15(17):2081–2088.
    1. Limketkai BN, Wolf A, Parian AM. Nutritional interventions in the patient with inflammatory bowel disease. Gastroenterol Clin N Am. 2018;47(1):155–177.
    1. Allen B, Orfila C. The availability and nutritional adequacy of gluten-free bread and pasta. Nutrients. 2018;10(10):1370.
    1. Vagianos K, Bector S, McConnell J, Bernstein CN. Nutrition assessment of patients with inflammatory bowel disease. JPEN J Parenter Enteral Nutr. 2007;31(4):311–319.
    1. Frigstad SO, Høivik ML, Jahnsen J, et al. Fatigue is not associated with vitamin D deficiency in inflammatory bowel disease patients. World J Gastroenterol. 2018;24(29):3293–3301.
    1. Lee TW, Iser JH, Sparrow MP, Newnham ED, Headon BJ, Gibson PR. Thiopurines, a previously unrecognised cause for fatigue in patients with inflammatory bowel disease. J Crohns Colitis. 2009;3(3):196–199.
    1. Ibrahim A, Dahlqvist P, Olsson T, et al. The clinical course after glucocorticoid treatment in patients with inflammatory bowel disease is linked to suppression of the hypothalamic–pituitary–adrenal axis: a retrospective observational study. Therap Adv Gastroenterol. 2017;10(11):829–836.
    1. Minderhoud IM, Oldenburg B, van Dam PS, van Berge Henegouwen GP. High prevalence of fatigue in quiescent inflammatory bowel disease is not related to adrenocortical insufficiency. Am J Gastroenterol. 2003;98(5):1088–1093.
    1. Docherty MJ, Jones RCW, Wallace MS. Managing pain in inflammatory bowel disease. Gastroenterol Hepatol. 2011;7(9):592–601.
    1. Hashash JG, Ramos-Rivers C, Youk A, et al. Quality of sleep and coexistent psychopathology have significant impact on fatigue burden in patients with inflammatory bowel disease. J Clin Gastroenterol. 2018;52(5):423–430.
    1. Leadbeater Bonnie J., Ames Megan E., Linden-Carmichael Ashley N. Age-varying effects of cannabis use frequency and disorder on symptoms of psychosis, depression and anxiety in adolescents and adults. Addiction. 2018;114(2):278–293.
    1. Clapp M, Aurora N, Herrera L, Bhatia M, Wilen E, Wakefield S. Gut microbiota’s effect on mental health: the gut-brain axis. Clin Pract. 2017;7(4):987.
    1. Borren NZ, van der Woude CJ, Ananthakrishnan AN. Fatigue in IBD: epidemiology, pathophysiology and management. Nat Rev Gastroenterol Hepatol. 2019;16(4):247–259.
    1. Estevinho MM, Rocha C, Correia L, et al. Features of fecal and colon microbiomes associate with responses to biologic therapies for inflammatory bowel diseases: a systematic review. Clin Gastroenterol Hepatol. 2019. 10.1016/j.cgh.2019.08.063.
    1. Longman RS, Swaminath A. Microbial manipulation as primary therapy for Crohn’s disease. World J Gastroenterol. 2013;19(10):1513–1516.
    1. P&T Community. ExeGi wins court ruling against VSL#3®*, permanent injunction blocks false advertising to doctors, consumers. 2019 Jun. . Accessed 12 Aug 2019.
    1. Ranjbaran Z, Keefer L, Stepanski E, Farhadi A, Keshavarzian A. The relevance of sleep abnormalities to chronic inflammatory conditions. Inflamm Res. 2007;56(2):51–57.
    1. Tang Y, Preuss F, Turek FW, Jakate S, Keshavarzian A. Sleep deprivation worsens inflammation and delays recovery in a mouse model of colitis. Sleep Med. 2009;10(6):597–603.
    1. Graff LA, Vincent N, Walker JR, et al. A population-based study of fatigue and sleep difficulties in inflammatory bowel disease. Inflamm Bowel Dis. 2011;17(9):1882–1889.
    1. Chrobak AA, Nowakowski J, Zwolinska-Wcislo M, et al. Associations between chronotype, sleep disturbances and seasonality with fatigue and inflammatory bowel disease symptoms. Chronobiol Int. 2018;35(8):1142–1152.
    1. van Langenberg DR, Papandony MC, Gibson PR. Sleep and physical activity measured by accelerometry in Crohn’s disease. Aliment Pharmacol Ther. 2015;41(10):991–1004.
    1. Swanson GR, Burgess HJ, Keshavarzian A. Sleep disturbances and inflammatory bowel disease: a potential trigger for disease flare? Exp Rev Clin Immunol. 2011;7(1):29–36.
    1. Burgess HJ, Swanson GR, Keshavarzian A. Endogenous melatonin profiles in asymptomatic inflammatory bowel disease. Scand J Gastroenterol. 2010;45(6):759–761.
    1. Graff LA, Walker JR, Russell AS, Bissonnette R, Bernstein CN. Fatigue and quality of sleep in patients with immune-mediated inflammatory disease. J Rheumatol Supp. 2011;88:36–42.
    1. Zimmerman J. Extraintestinal symptoms in irritable bowel syndrome and inflammatory bowel diseases: nature, severity, and relationship to gastrointestinal symptoms. Dig Dis Sci. 2003;48(4):743–749.
    1. Gingold-Belfer R, Peled N, Levy S, et al. Impaired sleep quality in Crohn’s disease depends on disease activity. Dig Dis Sci. 2014;59(1):146–151.
    1. Ali T, Madhoun MF, Orr WC, Rubin DT. Assessment of the relationship between quality of sleep and disease activity in inflammatory bowel disease patients. Inflamm Bowel Dis. 2013;19(11):2440–2443.
    1. Ananthakrishnan AN, Long MD, Martin CF, Sandler RS, Kappelman MD. Sleep disturbance and risk of active disease in patients with Crohn’s disease and ulcerative colitis. Clin Gastroenterol Hepatol. 2013;11(8):965–971.
    1. Wilson RG, Stevens BW, Guo AY, et al. High C-reactive protein is associated with poor sleep quality independent of nocturnal symptoms in patients with inflammatory bowel disease. Dig Dis Sci. 2015;60(7):2136–2143.
    1. Sofia MA, Andersen M, Rubin DT. Sleep dysfunction and inflammatory bowel disease. Sleep effect on gastrointestinal health and disease: translational opportunities for promoting health and optimizing disease management. New York: Nova Science; 2018. pp. 177–199.
    1. Ananthakrishnan AN, Khalili H, Konijeti GG, et al. Sleep duration affects risk for ulcerative colitis: a prospective cohort study. Clin Gastroenterol Hepatol. 2014;12(11):1879–1886.
    1. Qazi T, Farraye FA. Sleep and inflammatory bowel disease: an important bi-directional relationship. Inflamm Bowel Dis. 2019;25(5):843–852.
    1. 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(2):110–121.
    1. Keefer L, Stepanski EJ, Ranjbaran Z, Benson LM, Keshavarzian A. An initial report of sleep disturbance in inactive inflammatory bowel disease. J Clin Sleep Med. 2006;2(4):409–416.
    1. Young T, Peppard PE, Gottlieb DJ. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med. 2002;165(9):1217–1239.
    1. Walia HK, Mehra R. Practical aspects of actigraphy and approaches in clinical and research domains. In: Kerry H, Levin PC, editors. Handbook of clinical neurology. New Work: Elsevier; 2019. pp. 371–379.
    1. Bar-Gil Shitrit A, Chen-Shuali C, Adar T, et al. Sleep disturbances can be prospectively observed in patients with an inactive inflammatory bowel disease. Dig Dis Sci. 2018;63(11):2992–2997.
    1. Krueger JM. The role of cytokines in sleep regulation. Curr Pharm Des. 2008;14(32):3408–3416.
    1. Irwin MR, Wang M, Campomayor CO, Collado-Hidalgo A, Cole S. Sleep deprivation and activation of morning levels of cellular and genomic markers of inflammation. Arch Intern Med. 2006;166(16):1756–1762.
    1. Sonnenberg A. Occupational distribution of inflammatory bowel disease among German employees. Gut. 1990;31(9):1037–1040.
    1. Born J, Lange T, Hansen K, Molle M, Fehm HL. Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol. 1997;158(9):4454–4464.
    1. Haack M, Sanchez E, Mullington JM. Elevated inflammatory markers in response to prolonged sleep restriction are associated with increased pain experience in healthy volunteers. Sleep. 2007;30(9):1145–1152.
    1. Uthgenannt D, Schoolmann D, Pietrowsky R, Fehm HL, Born J. Effects of sleep on the production of cytokines in humans. Psychosom Med. 1995;57(2):97–104.
    1. Vgontzas AN, Papanicolaou DA, Bixler EO, Kales A, Tyson K, Chrousos GP. Elevation of plasma cytokines in disorders of excessive daytime sleepiness: role of sleep disturbance and obesity. J Clin Endocrinol Metab. 1997;82(5):1313–1316.
    1. Shoham S, Davenne D, Cady AB, Dinarello CA, Krueger JM. Recombinant tumor necrosis factor and interleukin 1 enhance slow-wave sleep. Am J Physiol. 1987;253(1 Pt 2):R142–R149.
    1. Mullington J, Korth C, Hermann DM, et al. Dose-dependent effects of endotoxin on human sleep. Am J Physiol Regul Integr Comp Physiol. 2000;278(4):R947–R955.
    1. Stevens BW, Borren NZ, Velonias G, et al. Vedolizumab therapy is associated with an improvement in sleep quality and mood in inflammatory bowel diseases. Dig Dis Sci. 2017;62(1):197–206.
    1. Watson NF, Lawlor C, Raymann R. Consumer sleep technologies, clinical guidelines, and evidence-based medicine: this is not a zero-sum game. J Clin Sleep Med. 2019;15(5):797–798.
    1. Hoffenberg EJ, McWilliams S, Mikulich-Gilbertson S, Murphy B, Hoffenberg A, Hopfer CJ. Cannabis oil use by adolescents and young adults with inflammatory bowel disease. J Pediatr Gastroenterol Nutr. 2019;68(3):348–352.
    1. Park YS, Chung SH, Lee SK, et al. Melatonin improves experimental colitis with sleep deprivation. Int J Mol Med. 2015;35(4):979–986.
    1. Li JH, Yu JP, Yu HG, et al. Melatonin reduces inflammatory injury through inhibiting NF-kappaB activation in rats with colitis. Mediat Inflamm. 2005;2005(4):185–193.
    1. Mei Q, Yu JP, Xu JM, Wei W, Xiang L, Yue L. Melatonin reduces colon immunological injury in rats by regulating activity of macrophages. Acta Pharmacol Sin. 2002;23(10):882–886.

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