Abdominal obesity increases the risk of reflux esophagitis: a systematic review and meta-analysis

Figures & data

Figure 1. Flow chart of study selection in this meta-analysis.

Table 1(A). The baseline characteristics of studies presenting adjusted effect size estimates with 95% CI.

First author	Year	Design	Exposure assessment	Reference	Basic diseases	Adjusted variables
Kang, M. S.	2007	C-S	WC	WC: 90 (for men), 80 (for women)	No	Age, sex, BMI, smoking, lifestyle choices, hiatal hernia, diabetes, use of aspirin or NSAIDs, use of hypertensive drugs
Lee, H. L.	2007	C-C	WHR	WHR: 0.8	No	Sex, BMI, percentage of body fat, obesity degree, smoking, hiatal hernia
Park, J. H.	2008	C-C	WC	WC: 90 (for men), 80 (for women)	No	Sex, smoking, drinking, reflux symptoms, hiatal hernia, fatty liver, homeostasis model
Chung, S. J.	2008	C-C	WC, CT	WC: 90 (for men), 80 (for women)	No	BMI, smoking, drinking, VAT, SAT
				VFA: 104.6 (for men), 52.1 (for women)
Koo, J. S.	2009	Cohort	WC	WC: 80	No	Sex, BMI, increase of BMI, smoking, drinking, triglyceride
Nam, S. Y.	2009	Cohort	WC	WC: 80	No	Age, smoking, drinking, gastrointestinal symptoms, diet, hiatal hernia, duodenal ulcer
Chua, C. S.	2009	C-C	WC	WC: 90 (for men), 80 (for women)	No	BMI
Nam, S. Y.	2010	C-S	WC, WHR, CT	WC: 80	No	Age, sex, BMI, VAT, WC, education, smoking, drinking, hiatal hernia, atrophic gastritis, Helicobacter pylori, diabetes, medication for hypertension
				WHR: 0.8
				VAT: 500
Wu, P.	2011	C-C	WC, WHR	WC: 90 (for men), 80 (for women)	No	Age, sex
				WHR: 0.9 (for men), 0.8 (for women)
Chiba, H.	2012	C-S	WC	WC: 85	No	Age, sex, BMI, WC, smoking, drinking, hiatal hernia, blood pressure, Helicobacter pylori, blood glucose, triglyceride, HDL-C, LDL-C
Sogabe, M.	2012	Cohort	WC	WC: 90	MS	Age, BMI, WC, hiatal hernia, MS type, fatty liver
Jung, J. G.	2013	C-S	WC	WC: 90 (for men), 80 (for women)	No	Sex, WC, smoking, drinking, diet, Helicobacter pylori IgG antibody
Loke, S. S.	2013	C-C	WC	WC: 90 (for men), 80 (for women)	No	NA
Hung, W. C.	2014	C-S	WC	WC: 90 (for men), 80 (for women)	No	Age, sex, BMI, smoking, drinking, tea drinking, exercise, hiatal hernia, diabetes, hypertension, hypertriglyceridemia, HDL-C
Sogabe, M.	2014	C-S	WC	WC: 80	MS	Age, BMI, WC, drinking, hiatal hernia, Helicobacter pylori, HDL, LDL, glycated hemoglobin
Ze, E. Y.	2017	C-S	CT	V/S: 1.165	No	BMI
Lee, S. W.	2017	C-C	WC (self-reported)	WC: 90 (for men), 80 (for women)	No	NA
Baeg, M. K.	2018	C-S	WC	WC: 90 (for men), 80 (for women)	MS	Age, sex, smoking, drinking, coffee, Helicobacter pylori, white blood cell count
Mazzoleni, F.	2019	Cohort	WC	WC: 94 (for men), 80 (for women)	Dyspepsia	Age, sex
Kim, T. J.	2019	Cohort	WC	WC: 90 (for men), 85 (for women)	No	Age, sex, smoking, drinking, exercise, acid inhibitor use, blood glucose, blood pressure, triglyceride, HDL-C, homeostasis model, C-reactive protein
Yang, H. J.	2019	Cohort	WC	WC: 56.5–80 (for men), 74.1–79.5 (for women)	No	Age, BMI, education, smoking, drinking, exercise, year of screening exam, hypertension, diabetes, medication for hypertension, medication for diabetes, medication for dyslipidemia
Hsieh, Y. H.	2019	C-S	WC	WC: 90 (for men), 80 (for women)	No	Age, sex, smoking, drinking, hiatal hernia, blood pressure, hyperglycemia

RE: reflux esophagitis; C-C: case–control study; C-S: cross-sectional study; CT: computed tomography; VFA: visceral fat area (cm²); VAT (cm3): visceral adipose tissue; SAT: superficial adipose tissue; V/S: VAT to SAT ratio; WHR: waist-to-hip ratio; WC: waist circumference (cm); BMI: body mass index; MS: metabolic syndrome; NA: not applicable; HDL-C: high density lipoprotein cholesterol; LDL-C: low-density lipoprotein cholesterol.

Table 1(B). The baseline characteristics of studies presenting adjusted effect size estimates with 95% CI.

First author	Year	Country	Baseline age	Gender	Effect estimate	Sample size	Cases	Effect size	Low limit	High limit
Kang, M. S.	2007	Korea	43.9	All	OR	2442	161	2.36	1.44	3.86
Lee, H. L.	2007	Korea	45.4	All	OR	3188	292	2.316	1.282	4.186
Lee, H. L.	2007	Korea	45.4	All	OR	3188	292	4.055	1.622	10.14
Park, J. H.	2008	Korea	45.0	All	OR	5037	1679	1.33	1.15	1.54
Chung, S. J.	2008	Korea	48.3	All	OR	1500	750	1.6	1.03	2.48
Chung, S. J.	2008	Korea	48.3	All	OR	1500	750	1.47	1.06	2.06
Chung, S. J.	2008	Korea	48.3	All	OR	1500	750	1.52	1.04	2.22
Koo, J. S.	2009	Korea	43.7	All	OR	1029	42	7.21	1.78	29.19
Koo, J. S.	2009	Korea	43.7	All	OR	1029	42	3.52	1.23	10.10
Nam, S. Y.	2009	Korea	48.8	M	OR	8571	552	1.15	0.59	2.23
Nam, S. Y.	2009	Korea	48.8	M	OR	8571	552	1.24	0.76	2
Chua, C. S.	2009	China	48.3	All	OR	854	427	1.41	1.05	1.89
Nam, S. Y.	2010	Korea	50.2	All	OR	4274	495	2.09	1.28	3.58
Nam, S. Y.	2010	Korea	50.2	All	OR	4274	495	2.10	1.31	3.39
Nam, S. Y.	2010	Korea	50.2	All	OR	4274	495	2.35	1.27	4.32
Wu, P.	2011	China	46.7	M	OR	372	182	3.41	1.52	7.62
Wu, P.	2011	China	46.7	W	OR	372	182	3.37	1.61	7.06
Chiba, H.	2012	Japan	34.0	All	OR	4990	728	1.276	1	1.628
Sogabe, M.	2012	Japan	56.9	M	OR	265	55	1.17	0.468	2.924
Jung, J. G.	2013	Korea	52.9	All	OR	296	50	1.1	0.466	2.603
Jung, J. G.	2013	Korea	52.9	All	OR	296	50	1.23	0.524	2.867
Loke, S. S.	2013	China	51.2	All	OR	1014	507	1.38	1.00	1.86
Hung, W. C.	2014	China	48.9	All	OR	12090	1922	1.14	1	1.31
Sogabe, M.	2014	Japan	58.3	W	OR	454	51	0.687	0.324	1.455
Ze, E. Y.	2017	Korea	47.2	All	OR	728	65	2.04	1.18	3.51
Lee, S. W.	2017	China	54.3	All	OR	200	100	6.22	3.34	11.57
Baeg, M. K.	2018	Korea	51.6	All	OR	10338	970	1.807	1.496	2.182
Baeg, M. K.	2018	Korea	51.6	All	OR	10338	970	1.585	1.308	1.92
Mazzoleni, F.	2019	Brazil	46.7	All	OR	351	39	1.861	0.687	5.042
Kim, T. J.	2019	Korea	47.3	All	HR	14725	1167	1.31	1.11	1.55
Yang, H. J.	2019	Korea	39.0	M	HR	142679	29509	1.13	1.06	1.21
Yang, H. J.	2019	Korea	39.0	W	HR	142679	29509	1.10	1.03	1.17
Hsieh, Y. H.	2019	China	50.1	All	OR	4895	2916	1.173	1.02	1.349

RE: reflux esophagitis; M: men; W: women; All: all genders; OR: odds ratio; HR: hazard ratio.

Table 2. The baseline characteristics of studies presenting continuous data.

First author	Year	Design	Exposure assessment	Basic diseases	Country	Baseline age	Gender	Sample size	Reflux esophagitis			Control
									Cases	Mean	SD	Cases	Mean	SD
Lee, H. L.	2009	C-C	CT: VFA	No	Korea	51.7	All	200	100	104.68	39.47	100	75.9	49.1
Lee, H. L.	2009	C-C	WHR	No	Korea	51.7	All	200	100	0.92	0.04	100	0.89	0.05
Mulholland, H. G.	2009	C-C	WHR	No	Britain	64.1	All	338	219	0.94	0.08	119	0.96	0.07
Tai, C. M.	2010	C-S	WHR	Obese	China	31.4	All	260	84	0.95	0.08	176	0.92	0.08
Tai, C. M.	2010	C-S	WC	Obese	China	31.4	All	260	84	123.7	16.8	176	117.3	15.1
Gunji, T.	2011	C-S	CT: VFA	No	Japan	51.7	M	9840	1831	104.7	52.8	8009	92.6	49.2
Gunji, T.	2011	C-S	WC	No	Japan	51.7	M	9840	1831	87.7	8.5	8009	85.3	8.1
Hsu, C. S.	2011	C-S	WC	No	China	51.7	All	741	131	83.8	10	610	80.4	9.4
Chung, S. J.	2011	C-C	WC	No	Korea	48.7	All	5616	2808	88.0	8.2	2808	85.9	7.8
Mokrowiecka, A.	2012	C-C	WHR	No	Poland	54.5	All	60	30	0.71	0.11	30	0.6	0.11
Wu, P.	2013	C-C	WHR	No	China	49.7	All	537	268	0.87	0	269	0.86	0
Wu, P.	2013	C-C	WC	No	China	49.7	All	537	268	82.8	0.6	269	81	0.6
Wu, Y. W.	2014	C-S	CT: VAT	No	China	55.0	All	458	178	72.8	27.6	280	61.7	29
Wu, Y. W.	2014	C-S	WC	No	China	55.0	All	458	178	90.7	8.4	280	87.1	9.6
Matsuzaki, J.	2015	C-C	CT: VFA	No	Japan	59.8	W	2608	34	105	46	949	64	38
Matsuzaki, J.	2015	C-C	WC	No	Japan	59.8	W	2608	34	85.9	11.1	949	78.3	10
Matsuzaki, J.	2015	C-C	CT: VFA	No	Japan	59.8	M	2608	182	117	47	1443	103	47
Matsuzaki, J.	2015	C-C	WC	No	Japan	59.8	M	2608	182	85.7	7.7	1443	83.3	8.4
Chung, H.	2016	C-S	WC	No	Korea	53.5	All	705	66	90.5	10	639	82.1	8.5
Hung, W. C.	2016	C-S	WC	No	China	49.4	M	11,952	1438	89.5	8.7	5739	87.6	8.7
Hung, W. C.	2016	C-S	WC	No	China	49.4	W	11,952	484	78.3	9.7	4429	77.0	9.3
Nam, S. Y.	2017	Cohort	CT: VAT	No	Korea	50.7	All	1503	83	1170	430	1420	915	458
Nam, S. Y.	2017	Cohort	WC	No	Korea	50.7	All	1503	83	90.9	7.3	1420	85.2	8
Park, J. K.	2017	C-S	WC	No	Korea	52.0	W	182,407	2858	81.38	8.4	76,377	78.66	7.72
Park, J. K.	2017	C-S	WC	No	Korea	52.0	M	182,407	15,965	89.35	7.6	87,207	87.3	7.44
Rafat, M. N.	2018	C-C	WHR	Patient	Egypt	48.7	All	130	40	0.91	0.06	40	0.83	0.05
Rafat, M. N.	2018	C-C	WC	Patient	Egypt	48.7	All	130	40	99	8	40	81	8
Rafat, M. N.	2018	C-C	WHR	Patient	Egypt	48.7	All	130	50	0.83	0.06	40	0.83	0.05
Rafat, M. N.	2018	C-C	WC	Patient	Egypt	48.7	All	130	50	86	9	40	81	8
Bang, K. B.	2018	Cohort	WC	No	Korea	41.0	All	1126	481	88	8	645	86	9.3
Nam, S. Y.	2019	Cohort	CT: VAT	No	Korea	51.4	All	163	83	1424	503	80	1118	440
Nam, S. Y.	2019	Cohort	WC	No	Korea	51.4	All	163	83	90.9	7.3	90	88.3	7.7
Takahashi, K.	2020	Cohort	CT: VFA	Obese	Japan	41.2	All	674	163	195.07	74.35	511	187.59	157.01
Chung, T. H.	2020	Cohort	WC	No	Korea	50.1	All	7123	276	87.1	6.9	6847	84.4	7.0
Tae, C. H.	2020	C-S	WC	No	Korea	45.2	W	1902	40	75.5	7.7	740	75.9	33.8
Tae, C. H.	2020	C-S	WC	No	Korea	45.2	M	1902	178	85.7	6.6	944	83.6	7.5

RE: reflux esophagitis; C-C: case–control study; C-S: Cross-sectional study; CT: computed tomography; VFA: visceral fat area (cm²); VAT (cm3): visceral adipose tissue; WHR: waist-to-hip ratio; WC: waist circumference (cm); M: men; W: women; All: all genders.

Figure 2. Association of abdominal obesity with reflux esophagitis in cohort studies.

Table 3. Overall and subgroup analyses of studies presenting adjusted effect size estimates with 95% CI.

Groups	Number of qualified studies	OR	95% CI	p	I^2
Overall analysis
Risk of RE	22	1.51	1.37–1.66	<.001	78.2%
Subgroup analysis
Characteristics of population
Geographic region
Asia	21	1.50	1.36–1.66	<.001	80.50%
South America	1	1.86	0.69–5.04	–	–
Gender
Man	6	2.04	1.34–3.10	<.001	86.50%
Woman	5	1.72	1.07–2.76	.025	71.90%
History of diseases
Health	19	1.49	1.35–1.65	<.001	79.50%
MS	3	1.23	0.65–2.32	.530	69.80%
Dyspepsia	1	1.86	0.69–5.04	–	–
Characteristics of research
Study design
Cohort	6	1.15	1.05–1.25	.002	49.40%
C-C	7	1.92	1.52–2.43	<.001	73.90%
C-S	9	1.52	1.29–1.80	<.001	73.40%
Measurement of central obesity
CT-measured visceral fat	3	1.74	1.47–2.05	<.001	0
WHR	3	2.47	1.85–3.30	<.001	0
WC	20	1.40	1.28–1.54	<.001	78.50%
Exposure assessment
By researchers	21	1.45	1.32–1.58	<.001	76.40%
Self-reported	1	6.22	3.34–11.58	–	–
Adjusted for covariates
Age	13	1.37	1.24–1.52	<.001	79.30%
Sex	13	1.64	1.43–1.89	<.001	73.70%
BMI	13	1.42	1.27–1.58	<.001	72.20%
Smoking status	14	1.41	1.28–1.55	<.001	78.60%
Drinking status	14	1.34	1.22–1.46	<.001	76.20%
Hiatal hernia	10	1.45	1.25–1.69	<.001	62.50%
Helicobacter pylori infection	5	1.60	1.34–1.92	<.001	50.60%

RE: reflux esophagitis; C-C: case–control study; C-S: cross-sectional study; CT: computed tomography; WHR: waist-to-hip ratio; WC: waist circumference (cm); OR: odds ratio; BMI: body mass index; MS: metabolic syndrome.

Table 4. Overall and subgroup analyses of studies presenting continuous data.

Groups	Number of qualified studies	SMD	95% CI	p	I^2
Overall analysis
Risk of RE	20	0.36	0.30–0.42	<.001	89.3%
Subgroup analysis
Characteristics of population
Geographic region
Asia	17	0.36	0.30–0.42	<.001	88.40%
Europe	2	0.34	−0.89 to 1.58	.584	94.40%
Africa	1	0.72	−0.70 to 2.14	–	–
Gender
Man	5	0.26	0.24–0.28	<.001	12.20%
Woman	4	0.35	0.12–0.57	.003	92.30%
History of diseases
Health	18	0.37	0.31–0.44	<.001	89.90%
Obesity	2	0.20	−0.12 to 0.51	.215	75.00%
Characteristics of research
Study design
Cohort	5	0.35	0.18–0.52	<.001	80.70%
C-C	7	0.57	0.29–0.85	<.001	94.20%
C-S	8	0.29	0.24–0.35	<.001	84.00%
Exposure assessment
By researchers	18	0.38	0.28–0.47	<.001	89.50%
Self-reported	2	0.36	0.26–0.45	<.001	90.90%
Subgroup analysis	Number of qualified studies	MD	95% CI	p	I^2
Characteristics of research
Measurement of central obesity
VAT	3	0.50	0.35–0.64	<.001	16.10%
VFA	4	0.41	0.20–0.62	<.001	88.30%
WHR	6	0.03	0.00–0.06	.028	92.00%
WC	16	2.87	2.46–3.28	<.001	90.10%

RE: reflux esophagitis; C-C: case–control study; C-S: cross-sectional study; VFA: visceral fat area (cm²); VAT (cm³): visceral adipose tissue; WHR: waist-to-hip ratio; WC: waist circumference (cm); SMD: standardized mean difference; MD: mean deviation.

Figure 3. The dose–response plot for the association of abdominal obesity with reflux esophagitis.

Table 5. Dose–response relationship of abdominal obesity with risk of RE.

Measurement of abdominal obesity	Number of qualified studies	OR	95% CI	p	I^2
CT-measured visceral fat
Highest quantile (versus lowest quantile)	4	2.28	1.23–4.24	.009	70.2%
Mid quantile (versus lowest quantile)	4	1.65	1.37–2.00	<.001	1.6%
WHR
Highest quantile (versus lowest quantile)	2	2.79	1.57–4.99	.001	4.1%
Mid quantile (versus lowest quantile)	2	1.60	1.09–2.35	.016	19.3%
WC
Highest quantile (versus lowest quantile)	6	1.17	1.06–1.30	.003	68.1%
Mid quantile (versus lowest quantile)	5	1.12	1.03–1.21	.007	67.8%

RE: reflux esophagitis; CT: computed tomography; WHR: waist-to-hip ratio; WC: waist circumference (cm); OR: odds ratio.

Figure 4. (A) The Begg’s funnel plots for studies presenting adjusted effect size estimates (OR or HR) with 95% CI. (B) The filled funnel plots for studies presenting adjusted effect size estimates (OR or HR) with 95% CI. (C) The filled funnel plots for studies presenting continuous data.

Data availability statement

All the data generated or analyzed in this study are included in this article and its supplementary information files.