Sex difference in the associations among risk factors with gastroesophageal reflux disease in a large Taiwanese population study.
Humans
Gastroesophageal Reflux
/ epidemiology
Male
Female
Middle Aged
Taiwan
/ epidemiology
Risk Factors
Sex Factors
Adult
Prevalence
Smoking
/ epidemiology
Age Factors
Hypertension
/ epidemiology
Alcohol Drinking
/ epidemiology
Diabetes Mellitus
/ epidemiology
Uric Acid
/ blood
Blood Glucose
/ analysis
Aged
Gastroesophageal reflux disease
Sex difference
Taiwan Biobank
Journal
BMC gastroenterology
ISSN: 1471-230X
Titre abrégé: BMC Gastroenterol
Pays: England
ID NLM: 100968547
Informations de publication
Date de publication:
15 May 2024
15 May 2024
Historique:
received:
05
02
2024
accepted:
02
05
2024
medline:
16
5
2024
pubmed:
16
5
2024
entrez:
15
5
2024
Statut:
epublish
Résumé
Gastroesophageal reflux disease (GERD) is a common global health issue. Previous studies have revealed a higher prevalence of GERD in females than in males, however few studies have investigated sex differences in the risk factors associated with GERD. Therefore, the aim of this population-based study was to examine sex differences in the risk factors for GERD in a large cohort of over 120,000 Taiwanese participants. We enrolled 121,583 participants (male: 43,698; female: 77,885; mean age 49.9 ± 11.0 years) from the Taiwan Biobank. The presence of GERD was ascertained using self-reported questionnaires. Sex differences in the risk factors associated with GERD were examined using multivariable logistic regression analysis. The overall prevalence of GERD was 13.7%, including 13.0% in the male participants and 14.1% in the female participants (p < 0.001). Multivariable analysis showed that older age, hypertension, smoking history, alcohol history, low fasting glucose, and low uric acid were significantly associated with GERD in the male participants. In the female participants, older age, diabetes, hypertension, smoking history, alcohol history, low systolic blood pressure, low fasting glucose, high hemoglobin, high total cholesterol, low high-density lipoprotein cholesterol (HDL-C), low low-density lipoprotein cholesterol, and low uric acid were significantly associated with GERD. Significant interactions were found between sex and age (p < 0.001), diabetes (p < 0.001), smoking history (p < 0.001), fasting glucose (p = 0.002), triglycerides (p = 0.001), HDL-C (p = 0.001), and estimated glomerular filtration rate (p = 0.002) on GERD. Our results showed a higher prevalence of GERD among females compared to males. Furthermore, sex differences were identified in the risk factors associated with GERD, and older age, diabetes, smoking history, and low HDL-C were more closely related to GERD in females than in males.
Sections du résumé
BACKGROUND
BACKGROUND
Gastroesophageal reflux disease (GERD) is a common global health issue. Previous studies have revealed a higher prevalence of GERD in females than in males, however few studies have investigated sex differences in the risk factors associated with GERD. Therefore, the aim of this population-based study was to examine sex differences in the risk factors for GERD in a large cohort of over 120,000 Taiwanese participants.
METHODS
METHODS
We enrolled 121,583 participants (male: 43,698; female: 77,885; mean age 49.9 ± 11.0 years) from the Taiwan Biobank. The presence of GERD was ascertained using self-reported questionnaires. Sex differences in the risk factors associated with GERD were examined using multivariable logistic regression analysis.
RESULTS
RESULTS
The overall prevalence of GERD was 13.7%, including 13.0% in the male participants and 14.1% in the female participants (p < 0.001). Multivariable analysis showed that older age, hypertension, smoking history, alcohol history, low fasting glucose, and low uric acid were significantly associated with GERD in the male participants. In the female participants, older age, diabetes, hypertension, smoking history, alcohol history, low systolic blood pressure, low fasting glucose, high hemoglobin, high total cholesterol, low high-density lipoprotein cholesterol (HDL-C), low low-density lipoprotein cholesterol, and low uric acid were significantly associated with GERD. Significant interactions were found between sex and age (p < 0.001), diabetes (p < 0.001), smoking history (p < 0.001), fasting glucose (p = 0.002), triglycerides (p = 0.001), HDL-C (p = 0.001), and estimated glomerular filtration rate (p = 0.002) on GERD.
CONCLUSIONS
CONCLUSIONS
Our results showed a higher prevalence of GERD among females compared to males. Furthermore, sex differences were identified in the risk factors associated with GERD, and older age, diabetes, smoking history, and low HDL-C were more closely related to GERD in females than in males.
Identifiants
pubmed: 38750425
doi: 10.1186/s12876-024-03254-3
pii: 10.1186/s12876-024-03254-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
165Subventions
Organisme : Kaohsiung Medical University Research Center
ID : KMU-TC111A01 and KMUTC111IFSP01
Informations de copyright
© 2024. The Author(s).
Références
El-Serag HB, Sweet S, Winchester CC, Dent J. Update on the epidemiology of gastro-oesophageal reflux disease: a systematic review. Gut. 2014;63(6):871–80.
pubmed: 23853213
doi: 10.1136/gutjnl-2012-304269
Hu WH, Wong WM, Lam CL, Lam KF, Hui WM, Lai KC, Xia HX, Lam SK, Wong BC. Anxiety but not depression determines health care-seeking behaviour in Chinese patients with dyspepsia and irritable bowel syndrome: a population-based study. Aliment Pharmacol Ther. 2002;16(12):2081–8.
pubmed: 12452941
doi: 10.1046/j.1365-2036.2002.01377.x
Li YM, Du J, Zhang H, Yu CH. Epidemiological investigation in outpatients with symptomatic gastroesophageal reflux from the Department of Medicine in Zhejiang Province, east China. J Gastroenterol Hepatol. 2008;23(2):283–9.
pubmed: 17645475
doi: 10.1111/j.1440-1746.2007.05045.x
Wang JH, Luo JY, Dong L, Gong J, Tong M. Epidemiology of gastroesophageal reflux disease: a general population-based study in Xi’an of Northwest China. World J Gastroenterol. 2004;10(11):1647–51.
pubmed: 15162542
pmcid: 4572771
doi: 10.3748/wjg.v10.i11.1647
Wong WM, Lai KC, Lam KF, Hui WM, Hu WH, Lam CL, Xia HH, Huang JQ, Chan CK, Lam SK, et al. Prevalence, clinical spectrum and health care utilization of gastro-oesophageal reflux disease in a Chinese population: a population-based study. Aliment Pharmacol Ther. 2003;18(6):595–604.
pubmed: 12969086
doi: 10.1046/j.1365-2036.2003.01737.x
Hung LJ, Hsu PI, Yang CY, Wang EM, Lai KH. Prevalence of gastroesophageal reflux disease in a general population in Taiwan. J Gastroenterol Hepatol. 2011;26(7):1164–8.
pubmed: 21517967
doi: 10.1111/j.1440-1746.2011.06750.x
Dent J, Dodds WJ, Friedman RH, Sekiguchi T, Hogan WJ, Arndorfer RC, Petrie DJ. Mechanism of gastroesophageal reflux in recumbent asymptomatic human subjects. J Clin Invest. 1980;65(2):256–67.
pubmed: 7356677
pmcid: 371362
doi: 10.1172/JCI109667
Storr M, Meining A, Allescher HD. Pathophysiology and pharmacological treatment of gastroesophageal reflux disease. Dig Dis. 2000;18(2):93–102.
pubmed: 11060472
doi: 10.1159/000016970
Buckles DC, Sarosiek I, McMillin C, McCallum RW. Delayed gastric emptying in gastroesophageal reflux disease: reassessment with new methods and symptomatic correlations. Am J Med Sci. 2004;327(1):1–4.
pubmed: 14722388
doi: 10.1097/00000441-200401000-00001
Cameron AJ. Barrett’s esophagus: prevalence and size of hiatal hernia. Am J Gastroenterol. 1999;94(8):2054–9.
pubmed: 10445527
doi: 10.1111/j.1572-0241.1999.01277.x
Ford AC, Forman D, Reynolds PD, Cooper BT, Moayyedi P. Ethnicity, gender, and socioeconomic status as risk factors for esophagitis and Barrett’s esophagus. Am J Epidemiol. 2005;162(5):454–60.
pubmed: 16076833
doi: 10.1093/aje/kwi218
Mishima I, Adachi K, Arima N, Amano K, Takashima T, Moritani M, Furuta K, Kinoshita Y. Prevalence of endoscopically negative and positive gastroesophageal reflux disease in the Japanese. Scand J Gastroenterol. 2005;40(9):1005–9.
pubmed: 16211699
doi: 10.1080/00365520510023260
Nguyen P, Scott M, Castell DO. Evidence of gender differences in esophageal pain threshold. Am J Gastroenterol. 1995;90(6):901.
pubmed: 7771417
Chang L, Toner BB, Fukudo S, Guthrie E, Locke GR, Norton NJ, Sperber AD. Gender, age, society, culture, and the patient’s perspective in the functional gastrointestinal disorders. Gastroenterology. 2006;130(5):1435–46.
pubmed: 16678557
doi: 10.1053/j.gastro.2005.09.071
Grishina I, Fenton A, Sankaran-Walters S. Gender differences, aging and hormonal status in mucosal injury and repair. Aging Dis. 2014;5(2):160.
pubmed: 24729941
pmcid: 3966674
doi: 10.14336/AD.2014.0500160
Mauvais-Jarvis F, Bairey Merz N, Barnes PJ, Brinton RD, Carrero JJ, DeMeo DL, De Vries GJ, Epperson CN, Govindan R, Klein SL, et al. Sex and gender: modifiers of health, disease, and medicine. Lancet. 2020;396(10250):565–82.
pubmed: 32828189
pmcid: 7440877
doi: 10.1016/S0140-6736(20)31561-0
Mittendorfer B. Insulin resistance: sex matters. Curr Opin Clin Nutr Metab Care. 2005;8(4):367–72.
pubmed: 15930959
doi: 10.1097/01.mco.0000172574.64019.98
Chiocca JC, Olmos JA, Salis GB, Soifer LO, Higa R, Marcolongo M. Argentinean gastro-oesophageal reflux study g: prevalence, clinical spectrum and atypical symptoms of gastro-oesophageal reflux in Argentina: a nationwide population-based study. Aliment Pharmacol Ther. 2005;22(4):331–42.
pubmed: 16098000
doi: 10.1111/j.1365-2036.2005.02565.x
Menon S, Jayasena H, Nightingale P, Trudgill NJ. Influence of age and sex on endoscopic findings of gastrooesophageal reflux disease: an endoscopy database study. Eur J Gastroenterol Hepatol. 2011;23(5):389–95.
pubmed: 21448069
doi: 10.1097/MEG.0b013e328345d429
Nasseri-Moghaddam S, Mofid A, Ghotbi MH, Razjouyan H, Nouraie M, Ramard AR, Zaer-Rezaie H, Habibi R, Rafat-Zand K, Malekzadeh R. Epidemiological study of gastro-oesophageal reflux disease: reflux in spouse as a risk factor. Aliment Pharmacol Ther. 2008;28(1):144–53.
pubmed: 18410559
doi: 10.1111/j.1365-2036.2008.03708.x
Chen CH, Yang JH, Chiang CWK, Hsiung CN, Wu PE, Chang LC, Chu HW, Chang J, Song IW, Yang SL, et al. Population structure of Han Chinese in the modern Taiwanese population based on 10,000 participants in the Taiwan Biobank project. Hum Mol Genet. 2016;25(24):5321–31.
pubmed: 27798100
pmcid: 6078601
Fan CT, Hung TH, Yeh CK. Taiwan regulation of biobanks. J Law Med Ethics. 2015;43(4):816–26.
pubmed: 26711420
doi: 10.1111/jlme.12322
Lin JC, Fan CT, Liao CC, Chen YS. Taiwan Biobank: making cross-database convergence possible in the big data era. Gigascience. 2018;7(1):1–4.
pubmed: 29635374
doi: 10.1093/gigascience/gix110
Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of diet in renal disease study group. Ann Intern Med. 1999;130(6):461–70.
pubmed: 10075613
doi: 10.7326/0003-4819-130-6-199903160-00002
Ministry of Education: Physical Fitness 333 Plan. http://www.fitness.org.tw/ .
Moraes-Filho JP, Chinzon D, Eisig JN, Hashimoto CL, Zaterka S. Prevalence of heartburn and gastroesophageal reflux disease in the urban Brazilian population. Arq Gastroenterol. 2005;42(2):122–7.
pubmed: 16127569
doi: 10.1590/S0004-28032005000200011
Tseng H, Lee J-I, Geng J-H, Chen S-C. Sex difference in the associations among risk factors with depression in a large Taiwanese population study. Front Public Health. 2023;11:1070827.
pubmed: 37006563
pmcid: 10060520
doi: 10.3389/fpubh.2023.1070827
Masaka T, Iijima K, Endo H, Asanuma K, Ara N, Ishiyama F, Asano N, Koike T, Imatani A, Shimosegawa T. Gender differences in oesophageal mucosal injury in a reflux oesophagitis model of rats. Gut. 2013;62(1):6–14.
pubmed: 22287598
doi: 10.1136/gutjnl-2011-301389
Velders M, Schleipen B, Fritzemeier KH, Zierau O, Diel P. Selective estrogen receptor-beta activation stimulates skeletal muscle growth and regeneration. FASEB J. 2012;26(5):1909–20.
pubmed: 22278942
doi: 10.1096/fj.11-194779
Braniste V, Leveque M, Buisson-Brenac C, Bueno L, Fioramonti J, Houdeau E. Oestradiol decreases colonic permeability through oestrogen receptor beta-mediated up-regulation of occludin and junctional adhesion molecule-A in epithelial cells. J Physiol. 2009;587(Pt 13):3317–28.
pubmed: 19433574
pmcid: 2727039
doi: 10.1113/jphysiol.2009.169300
Braniste V, Jouault A, Gaultier E, Polizzi A, Buisson-Brenac C, Leveque M, Martin PG, Theodorou V, Fioramonti J, Houdeau E. Impact of oral bisphenol A at reference doses on intestinal barrier function and sex differences after perinatal exposure in rats. Proc Natl Acad Sci U S A. 2010;107(1):448–53.
pubmed: 20018722
doi: 10.1073/pnas.0907697107
Boeckxstaens G, El-Serag HB, Smout AJ, Kahrilas PJ. Symptomatic reflux disease: the present, the past and the future. Gut. 2014;63(7):1185–93.
pubmed: 24607936
doi: 10.1136/gutjnl-2013-306393
Chen CL. Visceral hypersensitivity in non-erosive reflux disease: neurogenic overwhelming in esophagus? Dig Dis Sci. 2013;58(8):2131–2.
pubmed: 23812863
doi: 10.1007/s10620-013-2751-5
Bhat YM, Bielefeldt K. Capsaicin receptor (TRPV1) and non-erosive reflux disease. Eur J Gastroenterol Hepatol. 2006;18(3):263–70.
pubmed: 16462539
doi: 10.1097/00042737-200603000-00006
Pedersen J, Reddy H, Funch-Jensen P, Arendt-Nielsen L, Gregersen H, Drewes AM. Differences between male and female responses to painful thermal and mechanical stimulation of the human esophagus. Dig Dis Sci. 2004;49(7–8):1065–74.
pubmed: 15387323
doi: 10.1023/B:DDAS.0000037789.25734.06
Boehme MW, Autschbach F, Ell C, Raeth U. Prevalence of silent gastric ulcer, erosions or severe acute gastritis in patients with type 2 diabetes mellitus–a cross-sectional study. Hepatogastroenterology. 2007;54(74):643–8.
pubmed: 17523341
Horikawa A, Ishii-Nozawa R, Ohguro M, Takagi S, Ohtuji M, Yamada M, Kuzuya N, Ujihara N, Ujihara M, Takeuchi K. Prevalence of GORD (gastro-oesophageal reflux disease) in Type 2 diabetes and a comparison of clinical profiles between diabetic patients with and without GORD. Diabet Med. 2009;26(3):228–33.
pubmed: 19317816
doi: 10.1111/j.1464-5491.2009.02671.x
Lluch I, Ascaso JF, Mora F, Minguez M, Pena A, Hernandez A, Benages A. Gastroesophageal reflux in diabetes mellitus. Am J Gastroenterol. 1999;94(4):919–24.
pubmed: 10201457
doi: 10.1111/j.1572-0241.1999.987_j.x
Kinekawa F, Kubo F, Matsuda K, Fujita Y, Tomita T, Uchida Y, Nishioka M. Relationship between esophageal dysfunction and neuropathy in diabetic patients. Am J Gastroenterol. 2001;96(7):2026–32.
pubmed: 11467628
doi: 10.1111/j.1572-0241.2001.03862.x
Selim MM, Wendelschafer-Crabb G, Redmon JB, Khoruts A, Hodges JS, Koch K, Walk D, Kennedy WR. Gastric mucosal nerve density: a biomarker for diabetic autonomic neuropathy? Neurology. 2010;75(11):973–81.
pubmed: 20837965
pmcid: 3463013
doi: 10.1212/WNL.0b013e3181f25f19
Jin HY, Kang YM, Kim CY, Kim SH, Liu WJ, Piao MH, Park JH, Baek HS, Park TS. Morphological comparison of small nerve fibres in gastric mucosa in non-diabetic and Type 2 diabetic subjects. Diabet Med. 2009;26(9):943–6.
pubmed: 19719718
doi: 10.1111/j.1464-5491.2009.02787.x
Jiang YD, Chang CH, Tai TY, Chen JF, Chuang LM. Incidence and prevalence rates of diabetes mellitus in Taiwan: analysis of the 2000–2009 Nationwide Health Insurance database. J Formos Med Assoc. 2012;111(11):599–604.
pubmed: 23217595
doi: 10.1016/j.jfma.2012.09.014
Sheen YJ, Hsu CC, Jiang YD, Huang CN, Liu JS, Sheu WH. Trends in prevalence and incidence of diabetes mellitus from 2005 to 2014 in Taiwan. J Formos Med Assoc. 2019;118(Suppl 2):S66–73.
pubmed: 31300322
doi: 10.1016/j.jfma.2019.06.016
Goedecke JH, Mtintsilana A, Dlamini SN, Kengne AP. Type 2 diabetes mellitus in African women. Diabetes Res Clin Pract. 2017;123:87–96.
pubmed: 28006698
doi: 10.1016/j.diabres.2016.11.017
Sarafidis PA, Nilsson PM. The metabolic syndrome: a glance at its history. J Hypertens. 2006;24(4):621–6.
pubmed: 16531786
doi: 10.1097/01.hjh.0000217840.26971.b6
Ilanne-Parikka P, Eriksson JG, Lindstrom J, Hamalainen H, Keinanen-Kiukaanniemi S, Laakso M, Louheranta A, Mannelin M, Rastas M, Salminen V. Prevalence of the metabolic syndrome and its components: findings from a finnish general population sample and the diabetes prevention study cohort. Diabetes Care. 2004;27(9):2135–40.
pubmed: 15333474
doi: 10.2337/diacare.27.9.2135
Ribas V, Drew BG, Zhou Z, Phun J, Kalajian NY, Soleymani T, Daraei P, Widjaja K, Wanagat J, de AguiarVallim TQ. Skeletal muscle action of estrogen receptor α is critical for the maintenance of mitochondrial function and metabolic homeostasis in females. Sci Transl Med. 2016;8(334):334ra354-334ra354.
doi: 10.1126/scitranslmed.aad3815
Misiewicz JJ, Waller SL, Anthony PP, Gummer JW. Achalasia of the cardia: pharmacology and histopathology of isolated cardiac sphincteric muscle from patients with and without achalasia. Q J Med. 1969;38(149):17–30.
pubmed: 5765090
Kahrilas PJ, Gupta RR. Mechanisms of acid reflux associated with cigarette smoking. Gut. 1990;31(1):4–10.
pubmed: 2318431
pmcid: 1378332
doi: 10.1136/gut.31.1.4
Kahrilas PJ, Gupta RR. The effect of cigarette smoking on salivation and esophageal acid clearance. J Lab Clin Med. 1989;114(4):431–8.
pubmed: 2794756
Nilsson M, Johnsen R, Ye W, Hveem K, Lagergren J. Lifestyle related risk factors in the aetiology of gastro-oesophageal reflux. Gut. 2004;53(12):1730–5.
pubmed: 15542505
pmcid: 1774312
doi: 10.1136/gut.2004.043265
Powell HA, Iyen-Omofoman B, Hubbard RB, Baldwin DR, Tata LJ. The association between smoking quantity and lung cancer in men and women. Chest. 2013;143(1):123–9.
pubmed: 22797799
doi: 10.1378/chest.12-1068
Mollerup S, Ryberg D, Hewer A, Phillips DH, Haugen A. Sex differences in lung CYP1A1 expression and DNA adduct levels among lung cancer patients. Can Res. 1999;59(14):3317–20.
Huxley RR, Woodward M. Cigarette smoking as a risk factor for coronary heart disease in women compared with men: a systematic review and meta-analysis of prospective cohort studies. Lancet. 2011;378(9799):1297–305.
pubmed: 21839503
doi: 10.1016/S0140-6736(11)60781-2
Burke AP, Farb A, Malcom GT. Liang Y-h, Smialek J, Virmani R: Effect of risk factors on the mechanism of acute thrombosis and sudden coronary death in women. Circulation. 1998;97(21):2110–6.
pubmed: 9626170
doi: 10.1161/01.CIR.97.21.2110
Hsieh Y-H, Wu M-F, Yang P-Y, Liao W-C, Hsieh Y-H, Chang Y-J, Lin I-C. What is the impact of metabolic syndrome and its components on reflux esophagitis? A cross-sectional study. BMC Gastroenterol. 2019;19:1–10.
doi: 10.1186/s12876-019-0950-z
Song HJ, Shim K-N, Yoon SJ, Kim S-E, Oh HJ, Ryu KH, Ha CY, Yeom HJ, Song JH, Jung S-A. The prevalence and clinical characteristics of reflux esophagitis in koreans and its possible relation to metabolic syndrome. J Korean Med Sci. 2009;24(2):197–202.
pubmed: 19399258
pmcid: 2672116
doi: 10.3346/jkms.2009.24.2.197
Takashima T, Adachi K, Kawamura A, Yuki M, Fujishiro H, Rumi MA, Ishihara S, Watanabe M, Kinoshita Y. Cardiovascular risk factors in subjects with Helicobacter pylori infection. Helicobacter. 2002;7(2):86–90.
pubmed: 11966866
doi: 10.1046/j.1083-4389.2002.00064.x
Shirota T, Kusano M, Kawamura O, Horikoshi T, Mori M, Sekiguchi T. Helicobacter pylori infection correlates with severity of reflux esophagitis: with manometry findings. J Gastroenterol. 1999;34(5):553–9.
pubmed: 10535481
doi: 10.1007/s005350050372
Chung SJ, Lim SH, Choi J, Kim D, Kim YS, Park MJ, Yim JY, Kim JS, Cho SH, Jung HC, et al. Helicobacter pylori serology inversely correlated with the risk and severity of reflux esophagitis in helicobacter pylori endemic area: a matched case-control study of 5,616 health check-up Koreans. J Neurogastroenterol Motil. 2011;17(3):267–73.
pubmed: 21860818
pmcid: 3155062
doi: 10.5056/jnm.2011.17.3.267
Chen MJ, Fang YJ, Wu MS, Chen CC, Chen YN, Yu CC, Kuo CC, Chiu MC, Hu WH, Tsai MH, et al. Application of Helicobacter pylori stool antigen test to survey the updated prevalence of Helicobacter pylori infection in Taiwan. J Gastroenterol Hepatol. 2020;35(2):233–40.
pubmed: 31408909
doi: 10.1111/jgh.14828
Irino Y, Toh R, Ishida T. A novel indicator for HDL functionality. J Atheroscler Thromb. 2019;26(11):945–6.
pubmed: 31167979
pmcid: 6845690
doi: 10.5551/jat.ED111
Hiltbold EM, Poloso NJ, Roche PA. MHC class II-peptide complexes and APC lipid rafts accumulate at the immunological synapse. J Immunol. 2003;170(3):1329–38.
pubmed: 12538693
doi: 10.4049/jimmunol.170.3.1329
El Khoudary SR, Nasr A, Billheimer J, Brooks MM, McConnell D, Crawford S, Orchard TJ, Rader DJ, Matthews KA. Associations of endogenous hormones with HDL novel metrics across the menopause transition: the SWAN HDL study. J Clin Endocrinol Metab. 2022;107(1):e303–14.
pubmed: 34390340
doi: 10.1210/clinem/dgab595