Abstract
Background:
Several lifestyle factors have been reported to be associated with erosive esophagitis (EE). Many studies examined the associated factors for EE independent of obesity. However, lifestyle factors associated with EE might differ depending on sex or the presence of obesity. This study thus aimed to investigate the lifestyle risk factors for EE stratified by obesity and sex.
Methods:
A cross-sectional survey was conducted among Japanese people who underwent an annual health checkup at the Oita Health Checkup Center between 2019 and 2021. Multivariate analysis was performed to determine the factors associated with EE in participants stratified by sex and the presence of obesity.
Results:
EE was diagnosed in 676 of 5240 participants (12.9%) who were analyzed, and occurred most often in males (601 cases). The percentage of obesity based on body mass index was significantly higher among EE than non-EE participants (50.3% and 26.5%, P < .001). In obese males, eating just before bedtime (OR = 1.34, 95% CI 1.01-1.78) and hiatal hernia (OR = 3.42, 95% CI 2.57-4.54) were significantly associated with EE in multivariate analysis. In non-obese males, current smoking (OR = 1.48, 95% CI 1.07-2.04), alcohol consumption of 40 to 60 g/day (OR = 1.60, 95% CI 1.11-2.30), and hiatal hernia (OR = 3.63, 95% CI 2.79-4.73) were significantly associated with EE.
Conclusions:
We found that factors associated with EE were different between obese and non-obese males. In obese males, avoiding going to bed within 2 h after dinner might contribute to preventing the occurrence of EE. In non-obese males, prevention of obesity, quitting smoking, and avoiding heavy alcohol consumption might be important for preventing the development of EE.
Keywords: life style, esophagitis, obesity
Introduction
Gastroesophageal reflux disease (GERD) is a condition caused by reflux of stomach contents into the esophagus, leading to troublesome symptoms and/or complications. 1 It includes 2 types as erosive esophagitis (EE) and non-erosive gastroesophageal reflux disease (NERD) based on endoscopic findings. EE is characterized by endoscopically visible distal esophageal mucosal tears with or without troublesome GERD symptoms. Heartburn and regurgitation are the most common symptoms of GERD,1,2 which reduce the patient’s quality of life (QOL). Additionally, EE might progress to Barrett’s esophagus (BE) and esophageal adenocarcinoma. 1 With the westernization of lifestyles, the incidence of GERD is on the rise in Japan. 3
The main pathophysiology of GERD is dysfunction of the anti-reflux barrier system, consisting of the lower esophageal sphincter (LES) and the diaphragm. 2 Esophageal acid exposure by high gastric acid production and intragastric pressure is also important factors for GERD development. 4 Hiatal hernia and obesity are risk factors of GERD. Hiatal hernia might result in prolonged esophageal acid exposure followed by mucosal injury. 4 Abdominal obesity elevates intra-abdominal pressure, which promotes hiatal hernia and GERD. 4 Although proton pump inhibitors (PPIs) can be used for the treatment of GERD symptoms and EE in most patients, it is not enough in some patients with EE. In addition, PPI use for long-term is associated with adverse effects, such as intestinal infections and hip and vertebral fractures. 5 Therefore, elucidation of the lifestyle-related factors and appropriate lifestyle interventions in addition to medication, are important for preventing and improving GERD, especially EE, and consequent BE and adenocarcinoma.
In addition to obesity, lifestyle and dietary factors such as smoking and alcohol consumption are strongly associated with GERD. 2 A recent systematic review showed that many such lifestyle and dietary factors are associated with GERD, including both EE and NERD. 6 In that review, 15 articles examined the lifestyle and dietary risk factors for EE; of them, 7 studies were from European and American countries, and 8 studies were from non-European countries. 6 Although 6 articles from Japan were included in that systematic review, the number of participants with EE was small in several of the studies. In addition, some studies examined only smoking and alcohol consumption as lifestyle risk factors. Therefore, data on these lifestyle factors for EE in Japanese individuals are limited and insufficient. In addition, several lifestyle factors were not reportedly associated with EE after adjustment for obesity in multivariate analysis.7 -9 This could be due to the fact that many studies examined the associated factors for EE independent of obesity. However, lifestyle factors might differ depending on the presence of obesity, and therefore, it is possible that factors associated with EE differ between subjects with and without it. It must also be noted that lifestyle factors can be quite different between males and females. In this study, we investigated the lifestyle risk factors for EE stratified by sex and the presence of obesity in Japanese participants undergoing annual health checkups.
Materials and Methods
Study Design and Participants
A cross-sectional survey was done among Japanese people who underwent upper endoscopy for health screening at an annual health check-up at the Oita Health Checkup Center between 2019 and 2021. Individuals taking medication for gastroesophageal reflux symptoms and those with gastroesophageal cancer were excluded from the study. If the participant had a health check-up more than twice between 2019 and 2021, the earlier data were used. The study protocol was approved by the ethics committee of Oita University (approval number 2046). Since this was a non-intrusive retrospective study, written informed consent was not obtained from each participant. Instead, participants were given the opportunity to decline participation (opt-out system).
Measures
Information on age, sex, height, weight, and waist circumference was obtained for each participant. Body mass index (BMI) calculated as weight divided by height squared (kg/m2). “Obesity” was defined as BMI ≥25.0 kg/m2, based on the criteria of the Japanese Society of Obesity. 10 In addition, waist circumference was measured for abdominal obesity (waist circumference ≥85 cm in men and ≥90 cm in women according to the Japanese criteria for metabolic syndrome 10 and waist circumference ≥90 cm in men and ≥80 cm in women according to the WHO Asian criteria 11 ) as a variable. In all patients, waist circumference was measured at the navel level.
Survey Questionnaire
Participants were asked to complete a questionnaire before the endoscopic examination. Information on smoking (none, past, or current) and alcohol consumption per day (none, <20, 20-40, 40-60, or ≥60 g) was obtained from each participant. The questionnaire also contained items on eating habits, such as fast eating, skipping breakfast (more than 3 times a week), eating just before bedtime (within 2 h), and snacking between meals (never, sometimes, or every day), to evaluate their influence on EE. In addition, the questionnaire included items about daily physical activity, such as performance of sweat-inducing exercise for more than 30 min twice a week, walking for an hour or more a day, brisk walking, and whether or not the participant generally slept well at night.
Endoscopy
Eight experienced endoscopists had more than 5 years of experience performed the endoscopy. They were blinded to the results of the questionnaire. EE was diagnose when grade A or greater erosion according to the Los Angeles classification was reported in endoscopy, or if the presence of EE was reported in the records in cases in which the Los Angeles grade was not available.12,13 Hiatal hernia was diagnosed when reverse endoscopy showed a space at the level of the gastric orifice. 8 Finally, each subject’s endoscopic findings were independently validated by a single endoscopy specialist.
Statistical Analysis
Non-normally distributed variables were shown as the median (interquartile range) and compared using the Mann-Whitney U test. Categorical variables were analyzed using the chi-squared test. We also conducted an adjusted analysis using multivariable logistic regression to examine possible factors associated with EE. For other variables, those that were shown by univariate screening to have a P value of <.10 were considered as candidates for selection. Their multicollinearity was assessed using the variance inflation factor. 13 Subgroup analyses were then performed according to sex and the presence of obesity. The odds ratio (OR) and 95% confidence interval (CI) were calculated for each variable. Statistically significant was defined as a 2-tailed P value <.05. All statistical analyses were conducted using SPSS version 25 (SPSS Inc., Chicago, IL, USA) and EZR version 1.37 software (Saitama Medical Center; Jichi Medical University, Saitama, Japan).
Results
Participant characteristics
Between 2019 and 2021, a total of 9815 patients underwent endoscopy during their annual health check-up (3222 in 2019, 2869 in 2020, and 3724 in 2021), including some who underwent the procedure more than twice. Among them, 1292 were excluded due to insufficient height and weight data, 122 were excluded because they were on medication for EE, and 14 patients with evidence of gastric or esophageal resection including cancer were excluded. Further, since 3147 patients underwent endoscopy more than 2 times over the 3-year study period and only their earlier data were used, a total of 5240 participants were finally included in the analysis after excluding their latter data.
Among the 5240 eligible participants (3198 men and 2042 women, median age 50.0 years (interquartile range, 14.0), 1551 (29.6%) participants were classified as obese based on BMI (BMI ≥25.0 kg/m2). A BMI of greater than 30 kg/m2 was only observed in 5.3% (279/5420) of the participants. Abdominal obesity according to the Japanese criteria was found in 31.5% (1648/5420), whereas abdominal obesity according to WHO Asian criteria was found in 29.8% (1564/5420) of the participants. EE was diagnosed in 12.9% (676/5420) of all the participants, 18.8% (601/3198) of males, and 3.7% (75/2042) of females. Hiatal hernia was present in 18.1% (946/5420) of participants.
EE versus non-EE
We compared characteristics between participants with and without EE (Table 1). The percentage of males was significantly higher among EE than non-EE participants (88.9% vs 56.9%, P < .001), as was the incidence of obesity (50.3% (340/676) vs 26.5% (1211/4564), respectively, P < .001). Abdominal obesity according to the Japanese criteria was more common in EE than non-EE participants (55.2% vs 27.9%, P < .001). Abdominal obesity according to WHO Asian criteria was also more common in EE than non-EE participants (33.9% vs 28.4%, P < .001). Variance inflation factors of all the independent variables were less than 1.2, except for those for BMI and waist circumference in men.
Table 1.
Differences in Characteristics Between Participants With and Without Erosive Esophagitis.
| EE (n = 676) | Non-EE (n = 4564) | P value | |||
|---|---|---|---|---|---|
| Age (median [IQR]) | 50.0 | 12.0 | 50.0 | 14.0 | .030 |
| Sex (male) | 601 | 88.9% | 2597 | 56.9% | <.001 |
| BMI (median [IQR]) | 25.0 | 4.7 | 22.7 | 4.5 | <.001 |
| BMI (≥25 kg/m2) | 340 | 50.3% | 1211 | 26.5% | |
| Waist circumference (median [IQR]) | 86.5 | 11.7 | 80.8 | 12.5 | <.001 |
| Abdominal obesity (Japanese) | 373 | (55.2%) | 1275 | (27.9%) | <.001 |
| Abdominal obesity (WHO) | 270 | (39.9%) | 1294 | (28.4%) | <.001 |
| Smoking | <.001 | ||||
| None | 218 | (32.2%) | 2517 | (55.1%) | |
| Past smoker | 224 | (33.1%) | 1117 | (24.5%) | |
| Current smoker | 234 | (34.6%) | 930 | (20.4%) | |
| Alcohol consumption (per day) | |||||
| None | 228 | (33.7%) | 2069 | (45.3%) | <.001 |
| <20 g | 63 | (9.3%) | 548 | (12.0%) | |
| 20-40 g | 173 | (25.6%) | 1112 | (24.4%) | |
| 40-60 g | 149 | (22.0%) | 606 | (13.3%) | |
| ≥60 g | 63 | (9.3%) | 229 | (5.0%) | |
| Exercise for more than 30 min | 185 | (27.4%) | 1048 | (23.0%) | .012 |
| Walking for 1 h or more | 219 | (32.4%) | 1619 | (35.5%) | .118 |
| Brisk walking | 352 | (52.1%) | 2405 | (52.7%) | .762 |
| Fast eating | 300 | (44.4%) | 1665 | (36.5%) | <.001 |
| Eating just before bedtime | 301 | (44.5%) | 1574 | (34.5%) | <.001 |
| Snacking between meals | |||||
| None | 198 | (29.3%) | 1007 | (22.1%) | <.001 |
| Sometimes | 371 | (54.9%) | 2468 | (54.1%) | |
| Everyday | 107 | (15.8%) | 1089 | (23.9%) | |
| Skipping breakfast | 178 | (26.3%) | 893 | (19.6%) | <.001 |
| Good sleep | 570 | (84.3%) | 3860 | (84.6%) | .864 |
| Hiatal hernia | 296 | (43.8%) | 650 | (14.2%) | <.001 |
Abbreviations: BMI, body mass index; EE, erosive esophagitis; IQR, interquartile range.
There were significant differences in the distribution of smoking and alcohol consumption between the 2 groups. The rates of fast eating, eating just before bedtime, skipping breakfast, and exercising more than 30 min twice a week were higher in EE than non-EE participants. Hiatal hernia was found in 43.8% (296/676) of EE participants, which was significantly higher than the incidence in non-EE participants (14.2% [650/4564]). More non-EE participants reported snacking between meals than EE participants.
Multivariable analysis showed that male sex (OR = 3.56, 95% CI 2.64-4.81), obesity based on BMI (OR = 1.56, 95% CI 1.19-2.04), current smoking (OR = 1.41, 95% CI 1.12-1.78), and hiatal hernia (OR = 3.63, 95% CI 3.03-4.36) were independently associated with EE (Table 2). Neither abdominal obesity based on Japanese criteria nor that based on the WHO criteria reached statistical significance for their association with EE. Drinking, eating just before bedtime, skipping breakfast, and exercise for more than 30 min twice a week were not independently associated with EE.
Table 2.
Multivariate Analyses of the Associated Factors for Erosive Esophagitis in Male.
| Odds ratio | 95% CI | |
|---|---|---|
| Risk factors for EE | ||
| Obesity as indicated by BMI | 1.56 | 1.19-2.04 |
| Current smoking | 1.41 | 1.12-1.78 |
| Hiatal hernia | 3.63 | 3.03-4.36 |
| Risk factors for EE in obese males | ||
| Eating just before bedtime | 1.34 | 1.01-1.78 |
| Hiatal hernia | 3.42 | 2.57-4.54 |
| Risk factors for EE in non-obese males | ||
| Current smoking | 1.48 | 1.07-2.04 |
| Drinking 40-60 g/day | 1.60 | 1.11-2.30 |
| Hiatal hernia | 3.63 | 2.79-4.73 |
| Risk factors for EE in non-obese females | ||
| Current smoking | 2.82 | 1.13-7.01 |
| Brisk walking | 0.47 | 0.22-0.99 |
| Hiatal hernia | 4.83 | 2.29-10.17 |
Abbreviations: BMI, body mass index; EE, erosive esophagitis.
Comparison between males and females
Baseline characteristics and lifestyle factors were compared between males and females (Supplemental Table S1). Obesity based on BMI was found in 36.3% (1160/3198) of males and 19.1% (391/2042) of females, indicating a significantly higher incidence in males than females (P < .001). Abdominal obesity according to the Japanese criteria was more common in males than females (44.5% vs 11.0%, P < .001). On the other hand, abdominal obesity according to WHO Asian criteria was less common in males than females (25.0% vs 37.5%, P < .001). Smoking and alcohol consumption were more common in males than females (31.5% vs 7.6% for smoking, 68.2% vs 37.3% for drinking, P < .001). Fast eating, eating just before bedtime, and skipping breakfast were more common in males than females, while snacking between meals was more common among females. exercise for more than 30 min twice a week, walking for 1 h or more in a day, brisk walking, and good sleep were more common among males than females. Hiatal hernia was more common in males than in females (23.4% vs 9.7%, P < .001).
Comparison between obese and non-obese participants
Baseline characteristics and lifestyle factors were compared between obese and non-obese participants (Supplemental Table S2). Since obesity based on BMI was associated with EE overall, we used BMI as the criterion to define obesity in this study. The male:female ratio was higher in obese than non-obese participants. Smoking and alcohol consumption were more common in obese compared to non-obese participants. The incidences of fast eating and eating just before bedtime were higher in obese than non-obese participants. Hiatal hernia was more common in obese than non-obese participants (23.8% vs 15.6%, P < .001).
EE versus non-EE in males stratified by the presence of obesity
Next, we examined the factors associated with EE in males stratified by the presence of obesity as indicated by BMI. Among the 1160 obese males, 300 had EE. Univariate analysis of the 1160 obese males showed that smoking, eating before bedtime, and hiatal hernia were more common in EE than non-EE participants (Table 3). Multivariate analysis showed that eating just before bedtime (OR = 1.34, 95% CI 1.01-1.78) and hiatal hernia (OR = 3.42, 95% CI 2.57-4.54) were significantly associated with EE (Table 2). Even when using the Japanese criteria to stratify abdominal obesity, eating just before bedtime tended to be associated with EE (OR = 1.20, 95% CI 0.93-1.56).
Table 3.
Differences in Characteristics Between Erosive Esophagitis (EE) and Non-EE Males Stratified by Obesity.
| (a) Obese | EE (n = 300) | Non-EE (n = 860) | P value | ||
|---|---|---|---|---|---|
| Age (median [IQR]) | 50.8 | 8.2 | 50.5 | 9.2 | .800 |
| Smoking | |||||
| None | 73 | (24.3%) | 274 | (31.9%) | .049 |
| Past smoker | 121 | (40.3%) | 308 | (35.8%) | |
| Current smoker | 106 | (35.3%) | 278 | (32.3%) | |
| Alcohol consumption (per day) | |||||
| None | 102 | (34.0%) | 304 | (35.3%) | .602 |
| <20 g | 24 | (8.0%) | 71 | (8.3%) | |
| 20-40 g | 73 | (24.3%) | 236 | (27.4%) | |
| 40-60 g | 68 | (22.7%) | 173 | (20.1%) | |
| ≥60 g | 33 | (11.0%) | 76 | (8.8%) | |
| Exercise for more than 30 min | 75 | (25.0%) | 220 | (25.6%) | .842 |
| Walking for 1 h or more | 94 | (31.3%) | 320 | (37.2%) | .067 |
| Brisk walking | 142 | (47.3%) | 457 | (53.1%) | .083 |
| Fast eating | 159 | (53.0%) | 441 | (51.3%) | .608 |
| Eating just before bedtime | 150 | (50.0%) | 364 | (42.3%) | .021 |
| Snacking between meals | |||||
| None | 77 | (25.7%) | 226 | (26.3%) | .782 |
| Sometimes | 174 | (58.0%) | 508 | (59.1%) | |
| Everyday | 49 | (16.3%) | 126 | (14.7%) | |
| Skipping breakfast | 79 | (26.3%) | 198 | (23.0%) | .247 |
| Good sleep | 261 | (87.0%) | 739 | (85.9%) | .644 |
| Hiatal hernia | 143 | (47.7%) | 178 | (20.7%) | <.001 |
| (b) Non-obese | EE (n = 301) | non-EE (n = 1737) | P value | ||
| Age (median [IQR]) | 50.9 | 8.4 | 50.4 | 9.7 | .249 |
| Smoking | |||||
| None | 88 | (29.2%) | 617 | (35.5%) | .006 |
| Past smoker | 98 | (32.6%) | 611 | (35.2%) | |
| Current smoker | 115 | (38.2%) | 509 | (29.3%) | |
| Alcohol consumption (per day) | |||||
| None | 75 | (24.9%) | 535 | (30.8%) | .038 |
| <20 g | 33 | (11.0%) | 195 | (11.2%) | |
| 20-40 g | 88 | (29.2%) | 548 | (31.5%) | |
| 40-60 g | 77 | (25.6%) | 330 | (19.0%) | |
| ≥60 g | 28 | (9.3%) | 129 | (7.4%) | |
| Exercise for more than 30 min | 97 | (32.2%) | 497 | (28.6%) | .203 |
| Walking for 1 h or more | 101 | (33.6%) | 641 | (36.9%) | .265 |
| Brisk walking | 179 | (59.5%) | 991 | (57.1%) | .434 |
| Fast eating | 114 | (37.9%) | 603 | (34.7%) | .289 |
| Eating just before bedtime | 127 | (42.2%) | 681 | (39.2%) | .328 |
| Snacking between meals | |||||
| None | 117 | (38.9%) | 583 | (33.6%) | .192 |
| Sometimes | 147 | (48.8%) | 910 | (52.4%) | |
| Everyday | 37 | (12.3%) | 244 | (14.0%) | |
| Skipping breakfast | 83 | (27.6%) | 385 | (22.2%) | .039 |
| Good sleep | 254 | (84.4%) | 1516 | (87.3%) | .171 |
| Hiatal hernia | 129 | (42.9%) | 297 | (17.1%) | <.001 |
Abbreviations: EE, erosive esophagitis; IQR, interquartile range.
Among the 2038 non-obese males, 301 had EE (Table 3). Univariate analysis showed that current smoking, skipping breakfast, alcohol consumption (≥40 g/day) and hiatal hernia were more common in EE than non-EE participants. There was no statistically significant difference in the incidence of eating just before bedtime between EE and non-EE participants. Multivariate analysis showed that current smoking (OR = 1.48, 95% CI 1.07-2.04), alcohol consumption of 40 to 60 g/day (OR = 1.60, 95% CI 1.11-2.30), and hiatal hernia (OR = 3.63, 95% CI 2.79-4.73) were significantly associated with EE in non-obese individuals (Table 2).
Factors associated with EE in females stratified according to the presence of obesity
Although the number of female participants with EE was small (n = 75), similar analyses as in males were performed in females. Forty of the 391 obese females had EE. Univariate analysis showed that only hiatal hernia was associated with EE in obese females (Supplemental Table S3a). Among the 1651 non-obese females, 35 had EE (Supplemental Table S3b). Univariate analysis showed an association between EE and smoking, skipping breakfast, and hiatal hernia in non-obese females. Multivariate analysis showed that current smoking (OR = 2.82, 95% CI 1.13-7.01), and hiatal hernia (OR = 4.83, 95% CI 2.29-10.17) were associated with EE in non-obese females. In contrast, brisk walking was inversely associated with EE (OR = 0.47, 95% CI 0.22-0.99) in non-obese females.
Discussion
The most recent guideline from the American College of Gastroenterology recommends weight loss in overweight patients, elevation of the head end of the bed, cessation of smoking and alcohol consumption, avoidance of late night meals and bedtime snacks, sitting upright during and after meals, and avoidance of foods that might aggravate reflux symptoms in patients with GERD.2,14 However, the evidence supporting these recommendations is limited and is based on small and uncontrolled studies. 2 In this study, we confirmed that obesity and hiatal hernia are important factors associated with EE. Overall, male sex, obesity as indicated by BMI, current smoking, and hiatal hernia were independently associated with EE. However, stratified analyses according to sex and the presence of obesity showed different results. In obese males, eating just before bedtime was independently associated with EE. On the other hand, smoking and alcohol consumption were associated with EE in non-obese males.
Obesity is considered a risk factor for EE.2,15 Obesity increases upper abdominal pressure, which provokes gastroesophageal reflux. In addition, gastric overfilling can loosen the lower esophageal sphincter (LES) and cause a hiatal hernia. 16 In our study, obesity was independently associated with EE in multivariate analysis. On the other hand, neither abdominal obesity based on Japanese criteria nor that based on WHO criteria reached statistical significance for EE. To the best of our knowledge, this is the first study investigating the association between EE and abdominal obesity, as assessed by Japanese and WHO Asian criteria. A recent meta-analysis showed that abdominal obesity increases the risk of EE. 15 On the other hand, a study conducted in Japan showed that BMI, but not abdominal obesity, was associated with EE. 17 This might be due to the different criteria used to define abdominal obesity, since the criteria used to define abdominal obesity varied between previous studies. The meta-analysis showed that the increasing trend of the association between abdominal obesity and EE accelerated when the waist circumference reached 87.0 cm. In the Japanese Society of Obesity criteria, abdominal obesity is defined as a waist circumference of ≥85 cm in men and ≥90 cm in women. 10 In contrast, WHO Asian criteria define abdominal obesity as a waist circumference of ≥90 cm in men and ≥80 cm in women. 11 Further studies are needed to determine which obesity criteria should be considered relevant for the development of EE.
The pathophysiology of EE might differ between obese and non-obese individuals, and males and females. In our study, eating just before bedtime (within 2 h), in addition to hiatal hernia, was significantly associated with EE only in obese males. On the other hand, there was no difference in terms of eating just before bedtime between non-obese males with and without EE even in univariate analysis. Abdominal adipose tissue in obese individuals can easily increase abdominal pressure. In Japan, only 1 study showed an association between eating before bedtime and EE. 18 Fujiwara et al. studied the interval between dinner and bedtime in patients with GERD, including EE, and age- and sex-matched controls. Their study, which evaluated 147 GERD patients, including 109 EE patients and 294 controls, found that even after adjustment for smoking, alcohol consumption, and BMI, a dinner-to-bed interval of less than 3 h was associated with EE compared with an interval of 4 h or more. However, since the control group in their study did not undergo endoscopy, it is possible that asymptomatic EE patients were included in the control group. Although another study from Japan showed that eating just before bedtime (within 2 h) was associated with symptoms of GERD using the Frequency Scale for the Symptoms of GERD (FSSG), the participants in that study were not evaluated by endoscopy. 19 A study from China also showed that a short interval between dinner and sleep was positively associated with the onset of EE. 20 The supine position might increase abdominal pressure, promote gastric dilatation, and increase transient relaxation of the lower esophageal sphincter, all of which are associated with an increase in gastroesophageal reflux. 21 Interestingly, Piesman et al 22 examined the difference in esophageal acid exposure using a wireless pH system in patients who consumed an early or late standard meal (6 or 2 h before bedtime) in the supine position. They found that GERD patients who ate a late-night meal had significantly greater supine acid reflux compared to those who ate an early meal, especially in overweight patients. This was particularly noticeable in patients with EE. In addition, another study using an antimony pH catheter showed that patients who retired within 2 h of a meal had a higher percentage of reflux time than those who retired after more than 2 h in the supine position. 23 Therefore, avoiding eating within 2 to 3 h before bedtime might reduce the onset of EE, especially in obese males.
Smoking was independently associated with EE in the overall cohort, although stratified analysis showed that smoking was independently associated with EE in non-obese participants, but not in obese participants. A number of articles have reported that smoking is a risk factor for EE.20,24 Smoking reduces LES pressure, which facilitates gastric acid reaching the esophagus. In addition, smoking reduces salivary bicarbonate secretion, which normally neutralizes the acidity of gastric contents.24,25 A large cohort study showed that smoking cessation was associated with an improvement in severe reflux symptoms compared to continued daily smoking. However, this has only been observed in normal weight individuals and not in overweight individuals. 25 They suggested that the pathophysiology of GERD is probably driven by weight in overweight and obese individuals, with smoking only playing a minor role. On the other hand, smoking plays a more important role in the pathophysiology of EE in non-obese individuals. 25 Our study results showing that smoking is associated with EE only in non-obese participants support their results.
Alcohol consumption is also reported to be a risk factor for EE. Alcohol consumption is thought to be associated with an increase in gastric acid secretion and a decrease in LES pressure. 24 Another study also showed that excessive alcohol consumption (≥40 g) on drinking days was associated with the severity of EE in men. 26 Heavy drinking, but not light to moderate drinking, might be associated with EE. Research has shown that heavy alcohol consumption is associated with weight gain, while light-to-moderate consumption is not. 27 Individuals who frequently drink moderate amounts of alcohol might have a healthier lifestyle in general, which might protect them from weight gain. 27 However, we did not examine the frequency of drinking in this study. Further studies are needed to clarify the relationship between alcohol consumption and EE.
A previous study showed that fast eating was associated with GERD symptoms. 16 Fast eating can lead to the ingestion of very large volumes of food, which will increase gastric pressure. 16 Although fast eating was not associated with EE in our study, the rate of fast eating was higher in obese than in non-obese participants. Fast eating has been reported to be associated with increased adiposity. 28 Therefore, fast eating might influence EE via obesity. In addition, brisk walking was inversely associated with EE only in non-obese females. However, the findings from female were based on the small number of subjects with EE in non-obese female (n = 35). Further studies are needed to elucidate the mechanisms of the relationships between lifestyle factors and EE.
Several studies have investigated the associated factors in relation to the severity of EE.20,24 However, most of the EE cases in Japan are mild, and more than 80% of the EEs were Los Angeles classification A or B.7,24 Therefore, we do not believe that our findings would be altered even if the severity of reflux esophagitis were to have been taken into account. In addition, we focused on EE but not NERD. Many lifestyle and dietary factors are associated with not only EE but also NERD. 6 However, patients with NERD are a heterogeneous group with different etiologies and different diagnostic criteria. 2 We believe that our findings, in which the presence of EE was established based on the endoscopic findings, were based on objective rather than subjective data.
Our study has several limitations. First, we included participants who underwent a medical checkup program, and not the general population. In our study, subjects with obesity based on BMI (BMI ≥25.0 kg/m2) was 36.3% in male and 19.1% in female. According to Japanese national survey, the percentage of obesity based on BMI (BMI ≥25.0 kg/m2) was 32.5% in male and 22.0% in female. 29 The rates of obesity in this study were significantly higher in male and lower in female compared with Japanese national survey (P = .006 and .02, respectively). Therefore, our results cannot be generalized to Japanese people. In addition, we used a cutoff BMI value of 25 kg/m2 as the criteria for defining obesity, as indicated in Japanese guidelines. However, the risk factors for GERD define obesity as BMI >30 kg/m. 2 30 In our study, obesity with a BMI of >30 kg/m2 was found in only 5.3% of participants, suggesting that our results using a BMI of 25 kg/m2 might underestimate the effect of obesity on EE. Second, information on diet and exercise was established on the basis of self-reported but not objective definitions. We did not collect data on medications, such as calcium blockers, which influence the LES pressure. Additionally, such information obtained through self-administered questionnaires at health screenings might not be sufficient for analysis. Therefore, it might be difficult to compare our results with those of other studies.
Conclusions
We found that the factors associated with EE differ depending on the presence of obesity and patient sex. In obese males, eating just before bedtime was independently associated with EE. Smoking was associated with EE only in non-obese participants, and not in obese participants of either sex. In obese men, avoiding going to bed within 2 h of dinner might be important in preventing the occurrence of EE. In non-obese males, prevention of obesity, quitting smoking, and avoiding heavy alcohol consumption might be important for preventing the development of EE. Further studies are needed to examine whether lifestyle intervention, based on the presence or absence of obesity, can prevent the onset of EE.
Supplemental Material
Supplemental material, sj-docx-1-jpc-10.1177_21501319231205383 for Lifestyle Factors Associated With Erosive Esophagitis in Japanese Individuals With and Without Obesity Undergoing Health Checkups by Seiji Shiota, Aika Shibata, Noboru Horinouchi, Kyoko Yamamoto and Eishi Miyazaki in Journal of Primary Care & Community Health
Acknowledgments
We are very grateful to Dr. Hiroki Takayama and the staff of the Oita Health Checkup Center for their assistance in this study.
Footnotes
Author Contributions: All authors contributed to study conception and design. Additionally, SS was responsible for data acquisition, analysis, interpretation, and drafted the article. AS, NH, and KY contributed to data acquisition and revised the article critically for important intellectual content. The first draft of the manuscript was written by SS and all authors commented on previous versions of the manuscript. EM approved the final version to be submitted. All authors read and approved the final manuscript.
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical Statement: The present study was approved by the ethics committee of Faculty of Medicine, Oita University (Approval No. 2046). Since this was a non-intrusive retrospective study, written informed consent was not obtained from each participant. Instead, participants were given the opportunity to decline participation (opt-out system).
ORCID iDs: Seiji Shiota 
https://orcid.org/0000-0001-9811-218X
Kyoko Yamamoto
https://orcid.org/0000-0003-2166-4423
Supplemental Material: Supplemental material for this article is available online.
References
- 1. Vakil N, van Zanten SV, Kahrilas P, Dent J, Jones R, Global Consensus G. The Montreal definition and classification of gastroesophageal reflux disease: a global evidence-based consensus. Am J Gastroenterol. 2006;101(8):1900-1920; quiz 1943. doi: 10.1111/j.1572-0241.2006.00630.x [DOI] [PubMed] [Google Scholar]
- 2. Katz PO, Dunbar KB, Schnoll-Sussman FH, Greer KB, Yadlapati R, Spechler SJ. ACG clinical guideline for the diagnosis and management of gastroesophageal reflux disease. Am J Gastroenterol. 2022;117(1):27-56. doi: 10.14309/ajg.0000000000001538 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Fujiwara Y, Arakawa T. Epidemiology and clinical characteristics of GERD in the Japanese population. J Gastroenterol. 2009;44(6):518-534. doi: 10.1007/s00535-009-0047-5 [DOI] [PubMed] [Google Scholar]
- 4. Boeckxstaens G, El-Serag HB, Smout AJ, Kahrilas PJ. Symptomatic reflux disease: the present, the past and the future. Gut. 2014;63(7):1185-1193. doi: 10.1136/gutjnl-2013-306393 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Ness-Jensen E, Hveem K, El-Serag H, Lagergren J. Lifestyle intervention in gastroesophageal reflux disease. Clin Gastroenterol Hepatol. 2016;14(2):175-82.e1-3. doi: 10.1016/j.cgh.2015.04.176 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Zhang M, Hou ZK, Huang ZB, Chen XL, Liu FB. Dietary and lifestyle factors related to gastroesophageal reflux disease: a systematic review. Ther Clin Risk Manag. 2021;17:305-323. doi: 10.2147/TCRM.S296680 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Mochizuki N, Fujita T, Kobayashi M, et al. Factors associated with the presentation of erosive esophagitis symptoms in health checkup subjects: a prospective, multicenter cohort study. PLoS One. 2018;13(5):e0196848. doi: 10.1371/journal.pone.0196848 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. Murao T, Sakurai K, Mihara S, Marubayashi T, Murakami Y, Sasaki Y. Lifestyle change influences on GERD in Japan: a study of participants in a health examination program. Dig Dis Sci. 2011;56(10):2857-2864. doi: 10.1007/s10620-011-1679-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Matsuki N, Fujita T, Watanabe N, et al. Lifestyle factors associated with gastroesophageal reflux disease in the Japanese population. J Gastroenterol. 2013;48(3):340-349. doi: 10.1007/s00535-012-0649-1 [DOI] [PubMed] [Google Scholar]
- 10. Examination Committee of Criteria for ‘Obesity Disease’ in Japan; Japan Society for the Study of O. New criteria for ‘obesity disease’ in Japan. Circ J. 2002;66(11):987-992. doi: 10.1253/circj.66.987 [DOI] [PubMed] [Google Scholar]
- 11. Alberti KG, Eckel RH, Grundy SM, et al. Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation. 2009; 120(16):1640-1645. doi: 10.1161/CIRCULATIONAHA.109.192644 [DOI] [PubMed] [Google Scholar]
- 12. Lundell LR, Dent J, Bennett JR, et al. Endoscopic assessment of oesophagitis: clinical and functional correlates and further validation of the Los Angeles classification. Gut. 1999;45(2):172-180. doi: 10.1136/gut.45.2.172 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Toki Y, Yamauchi R, Kayashima E, et al. Predictive factors for future onset of reflux esophagitis: a longitudinal case-control study using health checkup records. J Neurogastroenterol Motil. 2022;28(1):86-94. doi: 10.5056/jnm20237 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Kaltenbach T, Crockett S, Gerson LB. Are lifestyle measures effective in patients with gastroesophageal reflux disease? An evidence-based approach. Arch Intern Med. 2006;166(9): 965-971. doi: 10.1001/archinte.166.9.965 [DOI] [PubMed] [Google Scholar]
- 15. Zhan J, Yuan M, Zhao Y, et al. Abdominal obesity increases the risk of reflux esophagitis: a systematic review and meta-analysis. Scand J Gastroenterol. 2022;57(2):131-142. doi: 10.1080/00365521.2021.1994643 [DOI] [PubMed] [Google Scholar]
- 16. Yuan LZ, Yi P, Wang GS, et al. Lifestyle intervention for gastroesophageal reflux disease: a national multicenter survey of lifestyle factor effects on gastroesophageal reflux disease in China. Therap Adv Gastroenterol. 2019;12:1756284819877788. doi: 10.1177/1756284819877788 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Gunji T, Sato H, Iijima K, et al. Risk factors for erosive esophagitis: a cross-sectional study of a large number of Japanese males. J Gastroenterol. 2011;46(4):448-455. doi: 10.1007/s00535-010-0359-5 [DOI] [PubMed] [Google Scholar]
- 18. Fujiwara Y, Machida A, Watanabe Y, et al. Association between dinner-to-bed time and gastro-esophageal reflux disease. Am J Gastroenterol. 2005;100(12):2633-2636. doi: 10.1111/j.1572-0241.2005.00354.x [DOI] [PubMed] [Google Scholar]
- 19. Yamamichi N, Mochizuki S, Asada-Hirayama I, et al. Lifestyle factors affecting gastroesophageal reflux disease symptoms: a cross-sectional study of healthy 19864 adults using FSSG scores. BMC Med. 2012;10:45. doi: 10.1186/1741-7015-10-45 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Wang R, Wang J, Hu S. Study on the relationship of depression, anxiety, lifestyle and eating habits with the severity of reflux esophagitis. BMC Gastroenterol. 2021;21(1):127. doi: 10.1186/s12876-021-01717-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Dodds WJ, Dent J, Hogan WJ, et al. Mechanisms of gastroesophageal reflux in patients with reflux esophagitis. N Engl J Med. 1982;307(25):1547-1552. doi: 10.1056/NEJM198212163072503 [DOI] [PubMed] [Google Scholar]
- 22. Piesman M, Hwang I, Maydonovitch C, Wong RK. Nocturnal reflux episodes following the administration of a standardized meal. Does timing matter? Am J Gastroenterol. 2007;102(10):2128-2134. doi: 10.1111/j.1572-0241.2007.01348.x [DOI] [PubMed] [Google Scholar]
- 23. King AL, Baburajan B, Wong T, Anggiansah R, Anggiansah A. Determinants of abnormal supine reflux in 24-hour pH recordings. Dig Dis Sci. 2007;52(10):2844-2849. doi: 10.1007/s10620-006-9707-y [DOI] [PubMed] [Google Scholar]
- 24. Sogabe M, Okahisa T, Kurihara T, et al. Differences in several factors in the development of erosive esophagitis among patients at various stages of metabolic syndrome: a cross-sectional study. Diabetes Metab Syndr Obes. 2021;14:1589-1600. doi: 10.2147/DMSO.S298326 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Ness-Jensen E, Lindam A, Lagergren J, Hveem K. Tobacco smoking cessation and improved gastroesophageal reflux: a prospective population-based cohort study: the HUNT study. Am J Gastroenterol. 2014;109(2):171-177. doi: 10.1038/ajg.2013.414 [DOI] [PubMed] [Google Scholar]
- 26. Matsuzaki J, Suzuki H, Kobayakawa M, et al. Association of visceral fat area, smoking, and alcohol consumption with reflux esophagitis and Barrett’s Esophagus in Japan. PLoS One. 2015;10(7):e0133865. doi: 10.1371/journal.pone.0133865 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Traversy G, Chaput JP. Alcohol consumption and obesity: an update. Curr Obes Rep. 2015;4(1):122-130. doi: 10.1007/s13679-014-0129-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Fagerberg P, Charmandari E, Diou C, et al. Fast eating is associated with increased BMI among high-school students. Nutrients. 2021;13(3):880. doi: 10.3390/nu13030880 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Office of Nutrition, Cancer Measures and Health Promotion Division, Health Service Bureau, Ministry of Health, Labour and Welfare, Japan. The National Health and Nutrition Survey in Japan, 2019. Accessed September 5, 2023. https://www.mhlw.go.jp/content/001066903.pdf
- 30. Fass R. Gastroesophageal reflux disease. N Engl J Med. 2022;387(13):1207-1216. doi: 10.1056/NEJMcp2114026 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplemental material, sj-docx-1-jpc-10.1177_21501319231205383 for Lifestyle Factors Associated With Erosive Esophagitis in Japanese Individuals With and Without Obesity Undergoing Health Checkups by Seiji Shiota, Aika Shibata, Noboru Horinouchi, Kyoko Yamamoto and Eishi Miyazaki in Journal of Primary Care & Community Health