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Increased risk of osteoporosis in patients with peptic ulcer: a follow-up study using a national sample cohort

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Abstract

Summary

We performed a nationwide, population-based cohort study to investigate the risk of osteoporosis in patients with peptic ulcer disease in South Korea and concluded that peptic ulcer disease is associated with an increased risk of osteoporosis.

Purpose

This study aimed to evaluate the association between peptic ulcer disease (PUD) and the occurrence of osteoporosis using a national sample cohort from South Korea.

Methods

Using the national cohort study from the Korean National Health Insurance Service, we extracted data for patients with PUD (n = 50,002) and for 1:1 matched control participants (n = 50,002); we then analyzed the occurrence of osteoporosis from 2002 to 2013. The patients were matched according to age, sex, income, region of residence, and past medical history. A stratified Cox proportional hazards model was used to analyze the hazard ratios (HRs) and the 95% confidence intervals (CIs). Subgroup analyses were performed based on age and sex.

Results

The adjusted HR for osteoporosis was 1.36 (95% CI = 1.33–1.40, P < 0.001) in the PUD group. In the subgroup analysis based on age and sex, the respective adjusted HRs of PUD for osteoporosis were 1.33 (95% CI = 1.21–1.47) in the < 65-year-old group of men and 1.42 (95% CI = 1.30–1.56) in the ≥ 65-year-old group of men (each P < 0.001). The respective adjusted HRs of PUD for osteoporosis were 1.34 (95% CI = 1.29–1.39) in the < 65-year-old group of women and 1.38 (95% CI = 1.33–1.47) in the ≥ 65-year-old group of women (each P < 0.001).

Conclusion

In the current nationwide cohort study, we found that PUD is associated with an increased risk of osteoporosis regardless of sex.

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References

  1. Rosenstock SJ, Jorgensen T (1995) Prevalence and incidence of peptic ulcer disease in a Danish County--a prospective cohort study. Gut 36:819–824

    Article  CAS  Google Scholar 

  2. Kim HS, Baik SJ, Kim KH, Oh CR, Lee JH, Jo WJ, Kim HK, Kim EY, Kim MJ (2013) Prevalence of and risk factors for gastrointestinal diseases in korean americans and native koreans undergoing screening endoscopy. Gut Liver 7:539–545. https://doi.org/10.5009/gnl.2013.7.5.539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rosenstock S, Jorgensen T, Bonnevie O, Andersen L (2003) Risk factors for peptic ulcer disease: a population based prospective cohort study comprising 2416 Danish adults. Gut 52:186–193

    Article  CAS  Google Scholar 

  4. Lorentzon M, Cummings SR (2015) Osteoporosis: the evolution of a diagnosis. J Intern Med 277:650–661. https://doi.org/10.1111/joim.12369

    Article  CAS  PubMed  Google Scholar 

  5. Choi YJ, Oh HJ, Kim DJ, Lee Y, Chung YS (2012) The prevalence of osteoporosis in Korean adults aged 50 years or older and the higher diagnosis rates in women who were beneficiaries of a national screening program: the Korea National Health and Nutrition Examination Survey 2008-2009. J Bone Miner Res 27:1879–1886. https://doi.org/10.1002/jbmr.1635

    Article  PubMed  Google Scholar 

  6. Sozen T, Ozisik L, Basaran NC (2017) An overview and management of osteoporosis. Eur J Rheumatol 4:46–56. https://doi.org/10.5152/eurjrheum.2016.048

    Article  PubMed  Google Scholar 

  7. Crabtree JE, Peichl P, Wyatt JI, Stachl U, Lindley IJ (1993) Gastric interleukin-8 and IgA IL-8 autoantibodies in Helicobacter pylori infection. Scand J Immunol 37:65–70

    Article  CAS  Google Scholar 

  8. Bravo D, Hoare A, Soto C, Valenzuela MA, Quest AF (2018) Helicobacter pylori in human health and disease: mechanisms for local gastric and systemic effects. World J Gastroenterol 24:3071–3089. https://doi.org/10.3748/wjg.v24.i28.3071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Figura N, Gennari L, Merlotti D, Lenzi C, Campagna S, Franci B, Lucani B, Trabalzini L, Bianciardi L, Gonnelli C, Santucci A, Nut A (2005) Prevalence of Helicobacter pylori infection in male patients with osteoporosis and controls. Dig Dis Sci 50:847–852

    Article  CAS  Google Scholar 

  10. Wood RJ, Serfaty-Lacrosniere C (1992) Gastric acidity, atrophic gastritis, and calcium absorption. Nutr Rev 50:33–40. https://doi.org/10.1111/j.1753-4887.1992.tb02510.x

    Article  CAS  PubMed  Google Scholar 

  11. Krela-Kazmierczak I, Szymczak A, Lykowska-Szuber L, Eder P, Linke K (2016) Osteoporosis in gastrointestinal diseases. Adv Clin Exp Med 25:185–190. https://doi.org/10.17219/acem/33746

    Article  PubMed  Google Scholar 

  12. Sawicki A, Regula A, Godwod K, Debinski A (2003) Peptic ulcer disease and calcium intake as risk factors of osteoporosis in women. Osteoporos Int 14:983–986. https://doi.org/10.1007/s00198-003-1459-3

    Article  CAS  PubMed  Google Scholar 

  13. Wu CH, Tung YC, Chai CY, Lu YY, Su YF, Tsai TH, Kuo KL, Lin CL (2016) Increased risk of osteoporosis in patients with peptic ulcer disease: a nationwide population-based study. Medicine (Baltimore) 95:e3309. https://doi.org/10.1097/MD.0000000000003309

    Article  CAS  Google Scholar 

  14. Kim SY, Lim JS, Kong IG, Choi HG (2018) Hearing impairment and the risk of neurodegenerative dementia: a longitudinal follow-up study using a national sample cohort. Sci Rep 8:15266–15268. https://doi.org/10.1038/s41598-018-33325-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kim SY, Kim HJ, Lim H, Kong IG, Kim M, Choi HG (2018) Bidirectional association between gastroesophageal reflux disease and depression: two different nested case-control studies using a national sample cohort. Sci Rep 8:11748. https://doi.org/10.1038/s41598-018-29629-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Melton LJ 3rd, Crowson CS, Khosla S, O’Fallon WM (1999) Fracture risk after surgery for peptic ulcer disease: a population-based cohort study. Bone 25:61–67

    Article  Google Scholar 

  17. Scott EM, Scott BB (1998) A strategy for osteoporosis in gastroenterology. Eur J Gastroenterol Hepatol 10:689–696 discussion 696-8

    CAS  PubMed  Google Scholar 

  18. Lipkin EW (1998) Metabolic bone disease in gut diseases. Gastroenterol Clin North Am 27:513–523

    Article  CAS  Google Scholar 

  19. Zhu K, Prince RL (2012) Calcium and bone. Clin Biochem 45:936–942. https://doi.org/10.1016/j.clinbiochem.2012.05.006

    Article  CAS  PubMed  Google Scholar 

  20. Recker RR (1985) Calcium absorption and achlorhydria. N Engl J Med 313:70–73. https://doi.org/10.1056/NEJM198507113130202

    Article  CAS  PubMed  Google Scholar 

  21. Yu EW, Bauer SR, Bain PA, Bauer DC (2011) Proton pump inhibitors and risk of fractures: a meta-analysis of 11 international studies. Am J Med 124:519–526. https://doi.org/10.1016/j.amjmed.2011.01.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Scibora LM, Ikramuddin S, Buchwald H, Petit MA (2012) Examining the link between bariatric surgery, bone loss, and osteoporosis: a review of bone density studies. Obes Surg 22:654–667. https://doi.org/10.1007/s11695-012-0596-1

    Article  PubMed  Google Scholar 

  23. Waldum HL, Kleveland PM, Sordal OF (2016) Helicobacter pylori and gastric acid: an intimate and reciprocal relationship. Therap Adv Gastroenterol 9:836–844. https://doi.org/10.1177/1756283X16663395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Raisz LG (1999) Physiology and pathophysiology of bone remodeling. Clin Chem 45:1353–1358

    CAS  PubMed  Google Scholar 

  25. Russo F, Jirillo E, Clemente C, Messa C, Chiloiro M, Riezzo G, Amati L, Caradonna L, di Leo A (2001) Circulating cytokines and gastrin levels in asymptomatic subjects infected by Helicobacter pylori (H. pylori). Immunopharmacol Immunotoxicol 23:13–24. https://doi.org/10.1081/IPH-100102563

    Article  CAS  PubMed  Google Scholar 

  26. Manolagas SC (1995) Role of cytokines in bone resorption. Bone 17:63S–67S

    Article  CAS  Google Scholar 

  27. Souza PP, Lerner UH (2013) The role of cytokines in inflammatory bone loss. Immunol Invest 42:555–622. https://doi.org/10.3109/08820139.2013.822766

    Article  CAS  PubMed  Google Scholar 

  28. Kim HW, Kim YH, Han K, Nam GE, Kim GS, Han BD, Lee A, Ahn JY, Ko BJ (2014) Atrophic gastritis: a related factor for osteoporosis in elderly women. PLoS One 9:e101852. https://doi.org/10.1371/journal.pone.0101852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Konturek SJ, Bielanski W, Plonka M et al (2003) Helicobacter pylori, non-steroidal anti-inflammatory drugs and smoking in risk pattern of gastroduodenal ulcers. Scand J Gastroenterol 38:923–930

    Article  CAS  Google Scholar 

  30. Di Mario F, Goni E (2014) Gastric acid secretion: changes during a century. Best Pract Res Clin Gastroenterol 28:953–965. https://doi.org/10.1016/j.bpg.2014.10.006

    Article  PubMed  Google Scholar 

  31. Brown ES, Varghese FP, McEwen BS (2004) Association of depression with medical illness: does cortisol play a role? Biol Psychiatry 55:1–9

    Article  CAS  Google Scholar 

  32. Azuma K, Adachi Y, Hayashi H, Kubo KY (2015) Chronic psychological stress as a risk factor of osteoporosis. J UOEH 37:245–253. https://doi.org/10.7888/juoeh.37.245

    Article  CAS  PubMed  Google Scholar 

  33. Erez HB, Weller A, Vaisman N, Kreitler S (2012) The relationship of depression, anxiety and stress with low bone mineral density in post-menopausal women. Arch Osteoporos 7:247–255. https://doi.org/10.1007/s11657-012-0105-0

    Article  PubMed  Google Scholar 

  34. Fink HA, Kuskowski MA, Cauley JA, Taylor BC, Schousboe JT, Cawthon PM, Ensrud KE, Osteoporotic Fractures in Men (MrOS) Study Group (2014) Association of stressful life events with accelerated bone loss in older men: the osteoporotic fractures in men (MrOS) study. Osteoporos Int 25:2833–2839. https://doi.org/10.1007/s00198-014-2853-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Nguyen TV, Eisman JA, Kelly PJ, Sambrook PN (1996) Risk factors for osteoporotic fractures in elderly men. Am J Epidemiol 144:255–263

    Article  CAS  Google Scholar 

  36. Peris P, Guanabens N, Monegal A et al (1995) Aetiology and presenting symptoms in male osteoporosis. Br J Rheumatol 34:936–941

    Article  CAS  Google Scholar 

  37. Clarke BL, Khosla S (2009) Androgens and bone. Steroids 74:296–305. https://doi.org/10.1016/j.steroids.2008.10.003

    Article  CAS  PubMed  Google Scholar 

  38. Cauley JA (2015) Estrogen and bone health in men and women. Steroids 99:11–15. https://doi.org/10.1016/j.steroids.2014.12.010

    Article  CAS  PubMed  Google Scholar 

  39. Machowska A, Brzozowski T, Sliwowski Z, Pawlik M, Konturek PC, Pajdo R, Szlachcic A, Drozdowicz D, Schwarz M, Stachura J, Konturek SJ, Pawlik WW (2008) Gastric secretion, proinflammatory cytokines and epidermal growth factor (EGF) in the delayed healing of lingual and gastric ulcerations by testosterone. Inflammopharmacology 16:40–47. https://doi.org/10.1007/s10787-007-1600-6

    Article  CAS  PubMed  Google Scholar 

  40. Machowska A, Szlachcic A, Pawlik M, Brzozowski T, Konturek SJ, Pawlik WW (2004) The role of female and male sex hormones in the healing process of preexisting lingual and gastric ulcerations. J Physiol Pharmacol 55(Suppl 2):91–104

    PubMed  Google Scholar 

  41. Tuo B, Wen G, Wei J, Liu X, Wang X, Zhang Y, Wu H, Dong X, Chow JY, Vallon V, Dong H (2011) Estrogen regulation of duodenal bicarbonate secretion and sex-specific protection of human duodenum. Gastroenterology 141:854–863. https://doi.org/10.1053/j.gastro.2011.05.044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Jung SJ, Shin A, Kang D (2015) Active smoking and exposure to secondhand smoke and their relationship to depressive symptoms in the Korea national health and nutrition examination survey (KNHANES). BMC Public Health 15:1053. https://doi.org/10.1186/s12889-015-2402-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Laniado-Laborin R (2009) Smoking and chronic obstructive pulmonary disease (COPD). Parallel epidemics of the 21 century. Int J Environ Res Public Health 6:209–224. https://doi.org/10.3390/ijerph6010209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Yeo SH, Yang CH (2016) Peptic ulcer disease associated with Helicobacter pylori Infection. Korean J Gastroenterol 67:289–299. https://doi.org/10.4166/kjg.2016.67.6.289

    Article  PubMed  Google Scholar 

  45. Malfertheiner P, Chan FK, McColl KE (2009) Peptic ulcer disease. Lancet 74:1449–1461. https://doi.org/10.1016/S0140-6736(09)60938-7

    Article  CAS  Google Scholar 

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Funding

This work was supported in part by a research grant (NRF-2015-R1D1A1A01060860) from the National Research Foundation (NRF) of Korea.

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Correspondence to Suk Woo Lee.

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The ethics committee of Hallym University (2017–I102) approved the use of these data. A written informed consent was exempted by the Institutional Review Board.

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Choi, H.G., Rhim, C.C., Yoon, J.Y. et al. Increased risk of osteoporosis in patients with peptic ulcer: a follow-up study using a national sample cohort. Arch Osteoporos 14, 105 (2019). https://doi.org/10.1007/s11657-019-0659-1

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