Background Gastroesophageal reflux disease (GERD) is a common cause of discomfort and morbidity worldwide. However, information on determinants of GERD from large-scale studies in low- to medium-income countries is limited. We investigated the factors associated with different measures of GERD symptoms, including frequency, patient-perceived severity, and onset time. Methods We performed a cross-sectional analysis of the baseline data from a population-based cohort study of ~50,000 individuals in in Golestan Province, Iran. GERD symptoms in this study included regurgitation and/or heartburn. Results Approximately 20% of participants reported at least weekly symptoms. Daily symptoms were less commonly reported by men, those of Turkmen ethnicity, and nass chewers. On the other hand, age, body mass index, alcohol drinking, cigarette smoking, opium use, lower socioeconomic status, and lower physical activity were associated with daily symptoms. Most of these factors showed similar associations with severe symptoms. Women with higher BMI and waist to hip ratio were more likely to report frequent and severe GERD symptoms. Hookah smoking (OR 1.34, 95% CI 1.02–1.75) and opium use (OR 1.70, 95% CI 1.55–1.87) were associated with severe symptoms, whereas nass chewing had an inverse association (OR 0.87, 95% CI 0.76–0.99). After exclusion of cigarette smokers, hookah smoking was still positively associated and nass chewing was inversely associated with GERD symptoms (all frequencies combined). Conclusion GERD is common in this population. The associations of hookah and opium use and inverse association of nass use with GERD symptoms are reported for the first time. Further studies are required to investigate the nature of these associations. Other determinants of GERD were mostly comparable to those reported elsewhere.
References
[1]
Friedenberg FK, Hanlon A, Vanar V, Nehemia D, Mekapati J, et al. (2010) Trends in gastroesophageal reflux disease as measured by the National Ambulatory Medical Care Survey. Dig Dis Sci 55: 1911–1917. doi: 10.1007/s10620-009-1004-0
[2]
Ness-Jensen E, Lindam A, Lagergren J, Hveem K (2012) Changes in prevalence, incidence and spontaneous loss of gastro-oesophageal reflux symptoms: a prospective population-based cohort study, the HUNT study. Gut 61: 1390–1397. doi: 10.1136/gutjnl-2011-300715
[3]
van Soest EM, Dieleman JP, Siersema PD, Sturkenboom MC, Kuipers EJ (2005) Increasing incidence of Barrett’s oesophagus in the general population. Gut 54: 1062–1066. doi: 10.1136/gut.2004.063685
[4]
Peery AF, Dellon ES, Lund J, Crockett SD, McGowan CE, et al. (2012) Burden of gastrointestinal disease in the United States: 2012 update. Gastroenterology 143: 1179–1187. doi: 10.1053/j.gastro.2012.08.002
[5]
Ronkainen J, Aro P, Storskrubb T, Johansson SE, Lind T, et al. (2005) High prevalence of gastroesophageal reflux symptoms and esophagitis with or without symptoms in the general adult Swedish population: a Kalixanda study report. Scand J Gastroenterol 40: 275–285. doi: 10.1080/00365520510011579
[6]
Zagari RM, Fuccio L, Wallander MA, Johansson S, Fiocca R, et al. (2008) Gastro-oesophageal reflux symptoms, oesophagitis and Barrett’s oesophagus in the general population: the Loiano-Monghidoro study. Gut 57: 1354–1359. doi: 10.1136/gut.2007.145177
[7]
Lofdahl HE, Lane A, Lu Y, Lagergren P, Harvey RF, et al. (2011) Increased population prevalence of reflux and obesity in the United Kingdom compared with Sweden: a potential explanation for the difference in incidence of esophageal adenocarcinoma. Eur J Gastroenterol Hepatol 23: 128–132. doi: 10.1097/meg.0b013e3283424e25
[8]
Sobieraj DM, Coleman SM, Coleman CI (2011) US prevalence of upper gastrointestinal symptoms: a systematic literature review. Am J Manag Care 17: e449–e458.
[9]
Nouraie M, Razjouyan H, Assady M, Malekzadeh R, Nasseri-Moghaddam S (2007) Epidemiology of gastroesophageal reflux symptoms in Tehran, Iran: a population-based telephone survey. Arch Iran Med 10: 289–294.
[10]
Somi MH, Farhang S, Nasseri-Moghadam S, Jazayeri ES, Mirinezhad SK, et al. (2008) Prevalence and risk factors of gastroesophageal reflux disease in Tabriz, Iran. Iran J Public Health 37: 85–90.
[11]
Fazel M, Keshteli AH, Jahangiri P, Daneshpajouhnejad P, Adibi P (2012) Gastroesophageal Reflux Disease in Iran: SEPAHAN Systematic Review No. 2. Int J Prev Med 3: S10–S17.
[12]
Sepanlou SG, Khademi H, Abdollahzadeh N, Noori F, Malekzadeh F, et al. (2010) Time trends of gastro-esophageal reflux disease (GERD) and peptic ulcer disease (PUD) in Iran. Middle East J Digest Dis 2: 78–83.
[13]
Ganji A, Malekzadeh F, Safavi M, Nasseri-Moghadam S, Nouraie M, et al. (2009) Digestive and liver disease statistics in Iran. Middle East J Digest Dis 1: 56–62.
[14]
Locke GR III, Talley NJ, Fett SL, Zinsmeister AR, Melton LJ III (1999) Risk factors associated with symptoms of gastroesophageal reflux. Am J Med 106: 642–649. doi: 10.1016/s0002-9343(99)00121-7
[15]
Nilsson M, Johnsen R, Ye W, Hveem K, Lagergren J (2003) Obesity and estrogen as risk factors for gastroesophageal reflux symptoms. JAMA 290: 66–72. doi: 10.1001/jama.290.1.66
[16]
Rey E, Moreno-Elola-Olaso C, Artalejo FR, Locke GR III, Diaz-Rubio M (2006) Association between weight gain and symptoms of gastroesophageal reflux in the general population. Am J Gastroenterol 101: 229–233. doi: 10.4321/s1130-01082006000700005
[17]
Jacobson BC, Somers SC, Fuchs CS, Kelly CP, Camargo CA Jr (2006) Body-mass index and symptoms of gastroesophageal reflux in women. N Engl J Med 354: 2340–2348. doi: 10.1056/nejmoa054391
[18]
Jansson C, Nordenstedt H, Johansson S, Wallander MA, Johnsen R, et al. (2007) Relation between gastroesophageal reflux symptoms and socioeconomic factors: a population-based study (the HUNT Study). Clin Gastroenterol Hepatol 5: 1029–1034. doi: 10.1016/j.cgh.2007.04.009
[19]
Nocon M, Labenz J, Willich SN (2006) Lifestyle factors and symptoms of gastro-oesophageal reflux – a population-based study. Aliment Pharmacol Ther 23: 169–174. doi: 10.1111/j.1365-2036.2006.02727.x
[20]
Nordenstedt H, Zheng Z, Cameron AJ, Ye W, Pedersen NL, et al. (2008) Postmenopausal hormone therapy as a risk factor for gastroesophageal reflux symptoms among female twins. Gastroenterology 134: 921–928. doi: 10.1053/j.gastro.2008.01.009
[21]
Gao L, Weck MN, Rothenbacher D, Brenner H (2010) Body mass index, chronic atrophic gastritis and heartburn: a population-based study among 8936 older adults from Germany. Aliment Pharmacol Ther 32: 296–302. doi: 10.1111/j.1365-2036.2010.04334.x
[22]
Jansson C, Wallander MA, Johansson S, Johnsen R, Hveem K (2010) Stressful psychosocial factors and symptoms of gastroesophageal reflux disease: a population-based study in Norway. Scand J Gastroenterol 45: 21–29. doi: 10.3109/00365520903401967
[23]
Pandeya N, Green AC, Whiteman DC (2012) Prevalence and determinants of frequent gastroesophageal reflux symptoms in the Australian community. Dis Esophagus 25: 573–583. doi: 10.1111/j.1442-2050.2011.01287.x
[24]
Matsuki N, Fujita T, Watanabe N, Sugahara A, Watanabe A, et al. (2013) Lifestyle factors associated with gastroesophageal reflux disease in the Japanese population. J Gastroenterol 48: 340–349. doi: 10.1007/s00535-012-0649-1
[25]
Wang JH, Luo JY, Dong L, Gong J, Tong M (2004) Epidemiology of gastroesophageal reflux disease: a general population-based study in Xi’an of Northwest China. World J Gastroenterol 10: 1647–1651.
[26]
Cho YS, Choi MG, Jeong JJ, Chung WC, Lee IS, et al. (2005) Prevalence and clinical spectrum of gastroesophageal reflux: a population-based study in Asan-si, Korea. Am J Gastroenterol 100: 747–753.
[27]
Chen M, Xiong L, Chen H, Xu A, He L, et al. (2005) Prevalence, risk factors and impact of gastroesophageal reflux disease symptoms: a population-based study in South China. Scand J Gastroenterol 40: 759–767. doi: 10.1080/00365520510015610
[28]
Nouraie M, Radmard AR, Zaer-Rezaii H, Razjouyan H, Nasseri-Moghaddam S, et al. (2007) Hygiene could affect GERD prevalence independently: a population-based study in Tehran. Am J Gastroenterol 102: 1353–1360.
[29]
Nasseri-Moghaddam S, Mofid A, Ghotbi MH, Razjouyan H, Nouraie M, et al. (2008) Epidemiological study of gastro-oesophageal reflux disease: reflux in spouse as a risk factor. Aliment Pharmacol Ther 28: 144–153. doi: 10.1111/j.1365-2036.2008.03708.x
[30]
Kumar S, Sharma S, Norboo T, Dolma D, Norboo A, et al. (2011) Population based study to assess prevalence and risk factors of gastroesophageal reflux disease in a high altitude area. Indian J Gastroenterol 30: 135–143. doi: 10.1007/s12664-010-0066-4
[31]
Pourshams A, Khademi H, Malekshah AF, Islami F, Nouraei M, et al. (2010) Cohort Profile: The Golestan Cohort Study–a prospective study of oesophageal cancer in northern Iran. Int J Epidemiol 39: 52–59. doi: 10.1093/ije/dyp161
[32]
Maziak W (2011) The global epidemic of waterpipe smoking. Addict Behav 36: 1–5. doi: 10.1016/j.addbeh.2010.08.030
[33]
Eissenberg T, Shihadeh A (2009) Waterpipe tobacco and cigarette smoking: direct comparison of toxicant exposure. Am J Prev Med 37: 518–523. doi: 10.1016/j.amepre.2009.07.014
[34]
Jacob P III, Abu Raddaha AH, Dempsey D, Havel C, Peng M, et al. (2011) Nicotine, carbon monoxide, and carcinogen exposure after a single use of a water pipe. Cancer Epidemiol Biomarkers Prev 20: 2345–2353. doi: 10.1158/1055-9965.epi-11-0545
[35]
Jacob P III, Abu Raddaha AH, Dempsey D, Havel C, Peng M, et al. (2013) Comparison of nicotine and carcinogen exposure with water pipe and cigarette smoking. Cancer Epidemiol Biomarkers Prev 22: 765–772. doi: 10.1158/1055-9965.epi-12-1422
[36]
Islami F, Kamangar F, Nasrollahzadeh D, Aghcheli K, Sotoudeh M, et al. (2009) Socio-economic status and oesophageal cancer: results from a population-based case-control study in a high-risk area. Int J Epidemiol 38: 978–988. doi: 10.1093/ije/dyp195
[37]
El Serag HB, Sweet S, Winchester CC, Dent J (2013) Update on the epidemiology of gastro-oesophageal reflux disease: a systematic review. Gut gutjnl-2012-304269. Published Online First: 13 July 2013 doi:10.1136/gutjnl-2012-304269.
Gunji T, Sato H, Iijima K, Fujibayashi K, Okumura M, et al. (2011) Risk factors for erosive esophagitis: a cross-sectional study of a large number of Japanese males. J Gastroenterol 46: 448–455. doi: 10.1007/s00535-010-0359-5
[40]
Radwan G, Hecht SS, Carmella SG, Loffredo CA (2013) Tobacco-specific nitrosamine exposures in smokers and nonsmokers exposed to cigarette or waterpipe tobacco smoke. Nicotine Tob Res 15: 130–138. doi: 10.1093/ntr/nts099
[41]
Thomas GA, Rhodes J, Ingram JR (2005) Mechanisms of disease: nicotine–a review of its actions in the context of gastrointestinal disease. Nat Clin Pract Gastroenterol Hepatol 2: 536–544. doi: 10.1038/ncpgasthep0316
[42]
Trudgill NJ, Smith LF, Kershaw J, Riley SA (1998) Impact of smoking cessation on salivary function in healthy volunteers. Scand J Gastroenterol 33: 568–571. doi: 10.1080/00365529850171792
[43]
Shihadeh A, Azar S, Antonios C, Haddad A (2004) Towards a topographical model of narghile water-pipe cafe smoking: a pilot study in a high socioeconomic status neighborhood of Beirut, Lebanon. Pharmacol Biochem Behav 79: 75–82. doi: 10.1016/j.pbb.2004.06.005
[44]
Maziak W, Rastam S, Ibrahim I, Ward KD, Shihadeh A, et al. (2009) CO exposure, puff topography, and subjective effects in waterpipe tobacco smokers. Nicotine Tob Res 11: 806–811. doi: 10.1093/ntr/ntp066
[45]
Ayazi S, Demeester SR, Hsieh CC, Zehetner J, Sharma G, et al. (2011) Thoraco-abdominal pressure gradients during the phases of respiration contribute to gastroesophageal reflux disease. Dig Dis Sci 56: 1718–1722. doi: 10.1007/s10620-011-1694-y
[46]
Brunnemann KD, Genoble L, Hoffmann D (1985) N-Nitrosamines in chewing tobacco: An international comparison. J Agric Food Chem 33: 1178–1181. doi: 10.1021/jf00066a039
[47]
Zaridze DG, Blettner M, Matiakin EG, Poljakov BP, Stich HF, et al. (1986) The effect of nass use and smoking on the risk of oral leukoplakia. Cancer Detect Prev 9: 435–440.
[48]
Richter P, Hodge K, Stanfill S, Zhang L, Watson C (2008) Surveillance of moist snuff: total nicotine, moisture, pH, un-ionized nicotine, and tobacco-specific nitrosamines. Nicotine Tob Res 10: 1645–1652. doi: 10.1080/14622200802412937
[49]
Smoak BR, Koufman JA (2001) Effects of gum chewing on pharyngeal and esophageal pH. Ann Otol Rhinol Laryngol 110: 1117–1119.
[50]
Moazzez R, Bartlett D, Anggiansah A (2005) The effect of chewing sugar-free gum on gastro-esophageal reflux. J Dent Res 84: 1062–1065. doi: 10.1177/154405910508401118
[51]
Penagini R, Bianchi PA (1997) Effect of morphine on gastroesophageal reflux and transient lower esophageal sphincter relaxation. Gastroenterology 113: 409–414. doi: 10.1053/gast.1997.v113.pm9247457
[52]
Trenerry VC, Wells RJ, Robertson J (1995) Determination of morphine and related alkaloids in crude morphine, poppy straw and opium preparations by micellar electrokinetic capillary chromatography. J Chromatogr A 718: 217–225. doi: 10.1016/0021-9673(95)00670-2
[53]
Kikura-Hanajiri R, Kaniwa N, Ishibashi M, Makino Y, Kojima S (2003) Liquid chromatographic-atmospheric pressure chemical ionization mass spectrometric analysis of opiates and metabolites in rat urine after inhalation of opium. J Chromatogr B Analyt Technol Biomed Life Sci 789: 139–150. doi: 10.1016/s1570-0232(03)00096-5
[54]
Malaveille C, Friesen M, Camus AM, Garren L, Hautefeuille A, et al. (1982) Mutagens produced by the pyrolysis of opium and its alkaloids as possible risk factors in cancer of the bladder and oesophagus. Carcinogenesis 3: 577–585. doi: 10.1093/carcin/3.5.577
[55]
Friesen M, O’Neill IK, Malaveille C, Garren L, Hautefeuille A, et al. (1985) Characterization and identification of 6 mutagens in opium pyrolysates implicated in oesophageal cancer in Iran. Mutat Res 150: 177–191. doi: 10.1016/0027-5107(85)90114-9
[56]
Khademi H, Malekzadeh R, Pourshams A, Jafari E, Salahi R, et al. (2012) Opium use and mortality in Golestan Cohort Study: prospective cohort study of 50 000 adults in Iran. BMJ 344: e2502. doi: 10.1136/bmj.e2502
[57]
Locke GR III, Talley NJ, Fett SL, Zinsmeister AR, Melton LJ III (1997) Prevalence and clinical spectrum of gastroesophageal reflux: a population-based study in Olmsted County, Minnesota. Gastroenterology 112: 1448–1456. doi: 10.1016/s0016-5085(97)70025-8
[58]
Li YM, Du J, Zhang H, Yu CH (2008) Epidemiological investigation in outpatients with symptomatic gastroesophageal reflux from the Department of Medicine in Zhejiang Province, east China. J Gastroenterol Hepatol 23: 283–289. doi: 10.1111/j.1440-1746.2007.05045.x
[59]
Kotzan J, Wade W, Yu HH (2001) Assessing NSAID prescription use as a predisposing factor for gastroesophageal reflux disease in a Medicaid population. Pharm Res 18: 1367–1372.
[60]
Nocon M, Keil T, Willich SN (2006) Prevalence and sociodemographics of reflux symptoms in Germany–results from a national survey. Aliment Pharmacol Ther 23: 1601–1605. doi: 10.1111/j.1365-2036.2006.02924.x
[61]
El Serag H, Hill C, Jones R (2009) Systematic review: the epidemiology of gastro-oesophageal reflux disease in primary care, using the UK General Practice Research Database. Aliment Pharmacol Ther 29: 470–480. doi: 10.1111/j.1365-2036.2008.03901.x
[62]
Triadafilopoulos G, Sharma R (1997) Features of symptomatic gastroesophageal reflux disease in elderly patients. Am J Gastroenterol 92: 2007–2011.
[63]
Pilotto A, Franceschi M, Leandro G, Scarcelli C, D’Ambrosio LP, et al. (2006) Clinical features of reflux esophagitis in older people: a study of 840 consecutive patients. J Am Geriatr Soc 54: 1537–1542. doi: 10.1111/j.1532-5415.2006.00899.x
[64]
Johnson DA, Fennerty MB (2004) Heartburn severity underestimates erosive esophagitis severity in elderly patients with gastroesophageal reflux disease. Gastroenterology 126: 660–664. doi: 10.1053/j.gastro.2003.12.001
[65]
Nusrat S, Nusrat S, Bielefeldt K (2012) Reflux and sex: what drives testing, what drives treatment? Eur J Gastroenterol Hepatol 24: 233–247. doi: 10.1097/meg.0b013e32834f6baa
[66]
Cook MB, Wild CP, Forman D (2005) A systematic review and meta-analysis of the sex ratio for Barrett’s esophagus, erosive reflux disease, and nonerosive reflux disease. Am J Epidemiol 162: 1050–1061. doi: 10.1093/aje/kwi325
[67]
Cho JH, Kim HM, Ko GJ, Woo ML, Moon CM, et al. (2011) Old age and male sex are associated with increased risk of asymptomatic erosive esophagitis: analysis of data from local health examinations by the Korean National Health Insurance Corporation. J Gastroenterol Hepatol 26: 1034–1038. doi: 10.1111/j.1440-1746.2011.06686.x
[68]
Corley DA, Kubo A, Zhao W (2007) Abdominal obesity, ethnicity and gastro-oesophageal reflux symptoms. Gut 56: 756–762. doi: 10.1136/gut.2006.109413
[69]
Wang A, Mattek NC, Holub JL, Lieberman DA, Eisen GM (2009) Prevalence of complicated gastroesophageal reflux disease and Barrett’s esophagus among racial groups in a multi-center consortium. Dig Dis Sci 54: 964–971. doi: 10.1007/s10620-009-0742-3
[70]
Chen Z, Thompson SK, Jamieson GG, Devitt PG, Watson DI (2011) Effect of sex on symptoms associated with gastroesophageal reflux. Arch Surg 146: 1164–1169. doi: 10.1001/archsurg.2011.248
[71]
Moshkowitz M, Horowitz N, Halpern Z, Santo E (2011) Gastroesophageal reflux disease symptoms: prevalence, sociodemographics and treatment patterns in the adult Israeli population. World J Gastroenterol 17: 1332–1335. doi: 10.3748/wjg.v17.i10.1332
[72]
El Serag H (2008) The association between obesity and GERD: a review of the epidemiological evidence. Dig Dis Sci 53: 2307–2312. doi: 10.1007/s10620-008-0413-9
[73]
Eslick GD (2012) Gastrointestinal symptoms and obesity: a meta-analysis. Obes Rev 13: 469–479. doi: 10.1111/j.1467-789x.2011.00969.x
[74]
Singh S, Sharma AN, Murad MH, Buttar NS, El Serag HB, et al. (2013) Central Adiposity is Associated with Increased Risk of Esophageal Inflammation, Metaplasia, and Adenocarcinoma: a Systematic Review and Meta-Analysis. Clin Gastroenterol Hepatol 11: 1399–1412. doi: 10.1016/j.cgh.2013.05.009
[75]
Derakhshan MH, Robertson EV, Fletcher J, Jones GR, Lee YY, et al. (2012) Mechanism of association between BMI and dysfunction of the gastro-oesophageal barrier in patients with normal endoscopy. Gut 61: 337–343. doi: 10.1136/gutjnl-2011-300633
[76]
Anggiansah R, Sweis R, Anggiansah A, Wong T, Cooper D, et al. (2013) The effects of obesity on oesophageal function, acid exposure and the symptoms of gastro-oesophageal reflux disease. Aliment Pharmacol Ther 37: 555–563. doi: 10.1111/apt.12208
[77]
Robertson EV, Derakhshan MH, Wirz AA, Lee YY, Seenan JP, et al. (2013) Central obesity in asymptomatic volunteers is associated with increased intrasphincteric acid reflux and lengthening of the cardiac mucosa. Gastroenterology 145: 730–739. doi: 10.1053/j.gastro.2013.06.038
[78]
Nilsson M, Lundegardh G, Carling L, Ye W, Lagergren J (2002) Body mass and reflux oesophagitis: an oestrogen-dependent association? Scand J Gastroenterol 37: 626–630. doi: 10.1080/00365520212502
[79]
Jacobson BC, Moy B, Colditz GA, Fuchs CS (2008) Postmenopausal hormone use and symptoms of gastroesophageal reflux. Arch Intern Med 168: 1798–1804. doi: 10.1001/archinte.168.16.1798
[80]
Nam SY, Choi IJ, Ryu KH, Park BJ, Kim HB, et al. (2010) Abdominal visceral adipose tissue volume is associated with increased risk of erosive esophagitis in men and women. Gastroenterology 139: 1902–1911. doi: 10.1053/j.gastro.2010.08.019
[81]
Collings KL, Pierce PF, Rodriguez-Stanley S, Bemben M, Miner PB (2003) Esophageal reflux in conditioned runners, cyclists, and weightlifters. Med Sci Sports Exerc 35: 730–735. doi: 10.1249/01.mss.0000064937.99001.56
[82]
Murao T, Sakurai K, Mihara S, Marubayashi T, Murakami Y, et al. (2011) Lifestyle change influences on GERD in Japan: a study of participants in a health examination program. Dig Dis Sci 56: 2857–2864. doi: 10.1007/s10620-011-1679-x
[83]
Djarv T, Wikman A, Nordenstedt H, Johar A, Lagergren J, et al. (2012) Physical activity, obesity and gastroesophageal reflux disease in the general population. World J Gastroenterol 18: 3710–3714. doi: 10.3748/wjg.v18.i28.3710
[84]
Zheng Z, Margolis KL, Liu S, Tinker LF, Ye W (2008) Effects of estrogen with and without progestin and obesity on symptomatic gastroesophageal reflux. Gastroenterology 135: 72–81. doi: 10.1053/j.gastro.2008.03.039
[85]
Eherer AJ, Netolitzky F, Hogenauer C, Puschnig G, Hinterleitner TA, et al. (2012) Positive effect of abdominal breathing exercise on gastroesophageal reflux disease: a randomized, controlled study. Am J Gastroenterol 107: 372–378. doi: 10.1097/00004836-200609001-00062
[86]
Irwin RS, Madison JM (2000) The diagnosis and treatment of cough. N Engl J Med 343: 1715–1721. doi: 10.1056/nejm200012073432308
