Abstract
Summary
This study was to investigate the fracture risk of irritable bowel syndrome (IBS) in comparison with non-IBS group. Our results found that IBS group has increased risk for fracture, in particular of the spine, forearm, hip, and hand.
Introduction
Patients with IBS might also be at increased risk of osteoporosis and osteoporotic fractures. Up to now, the association between IBS and the risk of fractures at different anatomic sites occurrences is not completely clear. We conducted a population-based cohort analysis to investigate the fracture risk of IBS in comparison with non-IBS group.
Methods
We identified 29,505 adults aged ≥ 20 years with newly diagnosed IBS using the Taiwan National Health Insurance Research Database in 2000–2012. A comparison group was constructed of patients without IBS who were matched according to gender and age. The occurrence of fracture was monitored until the end of 2013. We analyzed the risk of fracture events to occur in IBS by using Cox proportional hazards regression models.
Results
Patients with IBS had a higher incidence of osteoporotic fractures compared with the non-IBS group (12.34 versus 9.45 per 1000 person-years) and an increased risk of osteoporotic fractures (adjusted hazard ratio [aHR] = 1.27, 95% confidence interval [CI] = 1.20–1.35). Site-specific analysis showed that the IBS group had a higher risk of fractures for spine, forearm, hip, and hand than did the non-IBS group. With further stratification for gender and age, a higher aHR value for osteoporotic fractures in the IBS group was seen across all age groups in males, but seen in elderly females. In addition, female, elderly, low income, hypertension, coronary artery disease, cerebrovascular disease, and depressive disorders as independent osteoporotic fracture risk factors in IBS patients.
Conclusions
The IBS is considered as a risk factor for osteoporotic fractures, particularly in female individuals and fracture sites located at the spine, forearm, hip, and hand.
Similar content being viewed by others
References
Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17:1726–1733
Pisani P, Renna MD, Conversano F, Casciaro E, Di Paola M, Quarta E, Muratore M, Casciaro S (2016) Major osteoporotic fragility fractures: risk factor updates and societal impact. World J Orthop 7:171–181
Briot K, Roux C (2015) Glucocorticoid-induced osteoporosis. RMD Open 1:e000014
Sealand R, Razavi C, Adler RA (2013) Diabetes mellitus and osteoporosis. Curr Diab Rep 13:411–418
Heidari B, Hassanjani Roushan MR (2012) Rheumatoid arthritis and osteoporosis. Caspian J Int Med 3:445–446
Handzlik-Orlik G, Holecki M, Wilczynski K, Dulawa J (2016) Osteoporosis in liver disease: pathogenesis and management. Ther Adv Endocrinol Metab 7:128–135
Krela-Kazmierczak I, Szymczak A, Lykowska-Szuber L, Eder P, Linke K (2016) Osteoporosis in gastrointestinal diseases. Adv Clin Exp Med 25:185–190
Irwin R, Raehtz S, Parameswaran N, McCabe LR (2016) Intestinal inflammation without weight loss decreases bone density and growth. Am J Phys Regul Integr Comp Phys 311:R1149–r1157
Ali T, Lam D, Bronze MS, Humphrey MB (2009) Osteoporosis in inflammatory bowel disease. Am J Med 122:599–604
Tilg H, Moschen AR, Kaser A, Pines A, Dotan I (2008) Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57:684–694
Wada Y, Hisamatsu T, Naganuma M, Matsuoka K, Okamoto S, Inoue N, Yajima T, Kouyama K, Iwao Y, Ogata H, Hibi T, Abe T, Kanai T (2015) Risk factors for decreased bone mineral density in inflammatory bowel disease: a cross-sectional study. Clin Nutr (Edinb, Scotl) 34:1202–1209
Abdul Rani R, Raja Ali RA, Lee YY (2016) Irritable bowel syndrome and inflammatory bowel disease overlap syndrome: pieces of the puzzle are falling into place. Intest Res 14:297–304
Lu CL, Chen CY, Lang HC, Luo JC, Wang SS, Chang FY, Lee SD (2003) Current patterns of irritable bowel syndrome in Taiwan: the Rome II questionnaire on a Chinese population. Aliment Pharmacol Ther 18:1159–1169
Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC (2006) Functional bowel disorders. Gastroenterology 130:1480–1491
Theodorou V, Ait Belgnaoui A, Agostini S, Eutamene H (2014) Effect of commensals and probiotics on visceral sensitivity and pain in irritable bowel syndrome. Gut Microbes 5:430–436
Stobaugh DJ, Deepak P, Ehrenpreis ED (2013) Increased risk of osteoporosis-related fractures in patients with irritable bowel syndrome. Osteoporos Int 24:1169–1175
Yen CM, Muo CH, Lin MC, Chang SN, Chang YJ, Kao CH (2014) A nationwide population cohort study: irritable bowel syndrome is a risk factor of osteoporosis. Eur J Intern Med 25:87–91
Carroccio A, Soresi M, D'Alcamo A et al (2014) Risk of low bone mineral density and low body mass index in patients with non-celiac wheat-sensitivity: a prospective observation study. BMC Med 12:230
Norgaard M, Farkas DK, Pedersen L, Erichsen R, de la Cour ZD, Gregersen H, Sorensen HT (2011) Irritable bowel syndrome and risk of colorectal cancer: a Danish nationwide cohort study. Br J Cancer 104:1202–1206
Hsiao CW, Huang WY, Ke TW, Muo CH, Chen WT, Sung FC, Kao CH (2014) Association between irritable bowel syndrome and colorectal cancer: a nationwide population-based study. Eur J Intern Med 25:82–86
Lai SW, Liao KF, Lin CL, Sung FC (2014) Irritable bowel syndrome correlates with increased risk of Parkinson’s disease in Taiwan. Eur J Epidemiol 29:57–62
Klotzbuecher CM, Ross PD, Landsman PB, Abbott TA 3rd, Berger M (2000) Patients with prior fractures have an increased risk of future fractures: a summary of the literature and statistical synthesis. J Bone Miner Res 15:721–739
Kanis JA, Hans D, Cooper C et al (2011) Interpretation and use of FRAX in clinical practice. Osteoporos Int 22:2395–2411
Lai SW, Liao KF, Lai HC, Tsai PY, Lin CL, Chen PC, Sung FC (2013) Risk of major osteoporotic fracture after cardiovascular disease: a population-based cohort study in Taiwan. J Epidemiol 23:109–114
Dinan TG, Quigley EM, Ahmed SM, Scully P, O'Brien S, O'Mahony L, O'Mahony S, Shanahan F, Keeling PW (2006) Hypothalamic-pituitary-gut axis dysregulation in irritable bowel syndrome: plasma cytokines as a potential biomarker? Gastroenterology 130:304–311
Dinan TG, Clarke G, Quigley EM, Scott LV, Shanahan F, Cryan J, Cooney J, Keeling PW (2008) Enhanced cholinergic-mediated increase in the pro-inflammatory cytokine IL-6 in irritable bowel syndrome: role of muscarinic receptors. Am J Gastroenterol 103:2570–2576
Katz S, Weinerman S (2010) Osteoporosis and gastrointestinal disease. Gastroenterol Hepatol (NY) 6:506–517
Khayyat Y, Attar S (2015) Vitamin D deficiency in patients with irritable bowel syndrome: does it exist? Oman Med J 30:115–118
Williams CE, Williams EA, Corfe BM (2018) Vitamin D status in irritable bowel syndrome and the impact of supplementation on symptoms: what do we know and what do we need to know? Eur J Clin Nutr. https://doi.org/10.1038/s41430-017-0064-z
Cozma-Petrut A, Loghin F, Miere D, Dumitrascu DL (2017) Diet in irritable bowel syndrome: what to recommend, not what to forbid to patients! World J Gastroenterol 23:3771–3783
McKenzie YA, Bowyer RK, Leach H et al (2016) British Dietetic Association systematic review and evidence-based practice guidelines for the dietary management of irritable bowel syndrome in adults (2016 update). J Hum Nutr Diet 29:549–575
Warden SJ, Robling AG, Haney EM, Turner CH, Bliziotes MM (2010) The emerging role of serotonin (5-hydroxytryptamine) in the skeleton and its mediation of the skeletal effects of low-density lipoprotein receptor-related protein 5 (LRP5). Bone 46:4–12
Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, Schütz G, Glorieux FH, Chiang CY, Zajac JD, Insogna KL, Mann JJ, Hen R, Ducy P, Karsenty G (2008) Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell 135:825–837
Fernandes BS, Hodge JM, Pasco JA, Berk M, Williams LJ (2016) Effects of depression and serotonergic antidepressants on bone: mechanisms and implications for the treatment of depression. Drugs Aging 33:21–25
Sikander A, Rana SV, Prasad KK (2009) Role of serotonin in gastrointestinal motility and irritable bowel syndrome. Clin Chim Acta 403:47–55
Wu Q, Bencaz AF, Hentz JG, Crowell MD (2012) Selective serotonin reuptake inhibitor treatment and risk of fractures: a meta-analysis of cohort and case-control studies. Osteoporos Int 23:365–375
Zhou C, Fang L, Chen Y, Zhong J, Wang H, Xie P (2018) Effect of selective serotonin reuptake inhibitors on bone mineral density: a systematic review and meta-analysis. Osteoporos Int 29:1243–1251
Nevitt MC, Cummings SR, Stone KL, Palermo L, Black DM, Bauer DC, Genant HK, Hochberg MC, Ensrud KE, Hillier TA, Cauley JA (2005) Risk factors for a first-incident radiographic vertebral fracture in women > or = 65 years of age: the study of osteoporotic fractures. J Bone Miner Res 20:131–140
Melton LJ 3rd, Hartmann LC, Achenbach SJ, Atkinson EJ, Therneau TM, Khosla S (2012) Fracture risk in women with breast cancer: a population-based study. J Bone Miner Res 27:1196–1205
Chen Z, Maricic M, Bassford TL, Pettinger M, Ritenbaugh C, Lopez AM, Barad DH, Gass M, Leboff MS (2005) Fracture risk among breast cancer survivors: results from the Women’s Health Initiative Observational Study. Arch Intern Med 165:552–558
Khosla S, Amin S, Orwoll E (2008) Osteoporosis in men. Endocr Rev 29:441–464
Houghton LA, Jackson NA, Whorwell PJ, Morris J (2000) Do male sex hormones protect from irritable bowel syndrome? Am J Gastroenterol 95:2296–2300
Kim BJ, Rhee PL, Park JH, Chang DK, Kim YH, Son HJ, Kim JJ, Rhee JC, Lee H (2008) Male sex hormones may influence the symptoms of irritable bowel syndrome in young men. Digestion 78:88–92
Acknowledgements
This study was based in part on data from the National Health Insurance Research Database provided by the Bureau of National Health Insurance and the Department of Health and Welfare and managed by the National Health Research Institutes. The interpretation and conclusions contained within do not represent those of the Bureau of National Health Insurance, Department of Health, or National Health Research Institutes.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This study was approved by the Institutional Review Board (IRB) of Ditmanson Medical Foundation Chia-Yi Christian Hospital (CYCH-IRB No.2018032), Taiwan, and because the data were obtained from the LHID 2005, informed consent from the participants was not obtained.
Conflicts of interest
None.
Electronic supplementary material
ESM 1
(DOCX 16 kb)
Rights and permissions
About this article
Cite this article
Lee, HS., Chen, CY., Huang, WT. et al. Risk of fractures at different anatomic sites in patients with irritable bowel syndrome: a nationwide population-based cohort study. Arch Osteoporos 13, 80 (2018). https://doi.org/10.1007/s11657-018-0496-7
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11657-018-0496-7