Impact of Sarcopenia on the Risk of Erosive Esophagitis

Chan Mi Heo; Tae Jun Kim; Hyuk Lee; Jeung Hui Pyo; Yang Won Min; Byung-Hoon Min; Jun Haeng Lee; Hee Jung Son; Sun-Young Baek; Kyunga Kim; Seungho Ryu; Poong-Lyul Rhee; Jae J. Kim

doi:10.4166/kjg.2020.75.3.132

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Heo, Kim, Lee, Pyo, Min, Min, Lee, Son, Baek, Kim, Ryu, Rhee, and Kim: Impact of Sarcopenia on the Risk of Erosive Esophagitis

Original Article

Korean J Gastroenterol 2020;75(3):132-140.

Published online: 4 October 2020

DOI: https://doi.org/10.4166/kjg.2020.75.3.132

Impact of Sarcopenia on the Risk of Erosive Esophagitis

Chan Mi Heo^1,^∗, Tae Jun Kim^1,^∗, Hyuk Lee¹

, Jeung Hui Pyo², Yang Won Min¹, Byung-Hoon Min¹, Jun Haeng Lee¹, Hee Jung Son^1,², Sun-Young Baek³, Kyunga Kim³, Seungho Ryu⁴, Poong-Lyul Rhee¹, Jae J. Kim¹

¹Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

²Center for Health Promotion, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

³Statistics and Data Center, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

⁴Department of Occupational and Environmental Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea

Correspondence to: Hyuk Lee, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, 81 Irwon-ro, Gangnam-gu, Seoul 06351, Korea. Tel: +82-2-3410-3409, Fax: +82-2-3410-6983, E-mail: leehyuk@skku.edu

^∗ The first two authors contributed equally to this work as co-first authors of this paper.

Received 31 August 201812 January 2020 Accepted 13 January 2020

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background/Aims

An association between obesity and erosive esophagitis has been reported, but the effects of sarcopenia and obesity on erosive esophagitis are unknown. This study examined the relationship between obesity, sarcopenia, sarcopenic obesity, and erosive esophagitis in a large population of asymptomatic men and women.

Methods

This study analyzed 32,762 subjects who underwent a comprehensive health checkup, which included upper gastrointestinal endoscopy, from August 2006 to December 2011 by a cross-sectional study. Sarcopenia was defined as a decrease in the appendicular skeletal muscle mass (ASM)/body weight value of two SD or more below the normal means for a younger reference group.

Results

The study was carried out on four groups according to obesity and sarcopenic status: normal, obesity, sarcopenic, and sarcopenic obese group. In a multivariable model, the risk of erosive esophagitis was higher in the obese (adjusted OR [aOR] 1.35, 95% CI 1.22-1.49), sarcopenic (aOR 2.12, 95% CI 1.40-3.19), and sarcopenic obese groups (aOR 1.54, 95% CI 1.27-1.87) than in the normal group. The risk of erosive esophagitis was higher in the sarcopenic and sarcopenic obese groups than the obese group; the ORs were 1.63 (95% CI 1.08-2.47) and 1.22 (95% CI 1.01-1.46), respectively. In dose-response analysis, in-creasing sarcopenia severity showed a positive and graded relationship with the overall, Los Angeles (LA)-B or higher grade, and LA-C erosive esophagitis.

Conclusions

This study suggests that sarcopenia is strongly and progressively associated with erosive esophagitis.

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Keywords: Sarcopenia, Obesity, Esophagitis

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Fig. 1.

(A-D) Prevalence of erosive esophagitis by the Los Angeles (LA) classification according to the sarcopenia and obesity status.

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Supplementary Fig. 1.

Study flow.

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Table 1.

Baseline Characteristics of the Study Participants according to the Obesity and Sarcopenia Status

	Normal (n=22,810)	Obese (n=8,533)	Sarcopenic (n=311)	Sarcopenic obese (n=1,108)	p-value
Age (years)	49.6±8.3	51.1±6.8	54.9±7.8	53.0±7.7	<0.001
Male	49.7	70.5	73.0	81.6	<0.001
BMI (kg/m²)	22.5±2.2	26.5±2.2	25.4±2.0	29.6±3.1	<0.001
Waist circumference (cm)	78.9±6.5	92.9±4.6	84.2±4.2	98.9±7.4	<0.001
ASM (kg)	19.2±4.1	22.9±4.4	17.1±3.4	21.9±4.4	<0.001
ASM/weight	31±3	30±3	27±3	27±3	<0.001
ASM/BMI (m²)	1.41±0.57	1.13±0.32	0.82±0.19	0.77±0.16	<0.001
Body fat percentage	24.4±6.1	28.3±5.8	33.6±5.2	35.7±5.2	<0.001
Current smoking	19.7	27.5	18.5	29.0	<0.001
Modest alcohol intake	12.7	21.6	14.6	24.1	<0.001
Regular exercise	29.9	25.6	26.9	22.7	<0.001
SBP (mmHg)	116 (106–127)	123 (113–134)	126 (113–137)	127 (117–139)	<0.001
Triglycerides (mg/dL)	89 (65–128)	117 (85–162)	115 (84–160)	134 (99–191)	<0.001
HDL-C (mg/dL)	55 (46–66)	50 (44–61)	47 (41–56)	46 (39–55)	<0.001
Fasting glucose (mg/dL)	90 (84–97)	94 (88–103)	94 (87–104)	97 (90–109)	<0.001
hsCRP (mg/dL)	0.04 (0.03-0.08)	0.07 (0.04-0.15)	0.08 (0.04-0.16)	0.12 (0.06-0.24)	<0.001
Antihypertensive medication	13.2	26.4	32.7	42.5	<0.001
Hypoglycemic medication	5.0	8.8	5.7	13.1	<0.001
Dyslipidemia medication	9.4	16.0	24.6	21.2	<0.001
Cardiovascular disease	1.4	2.2	2.8	3.9	<0.001
Cerebrovascular disease	0.7	1.0	0.5	1.8	<0.001
Asthma	3.1	3.6	6.9	4.0	0.024
Aspirin use	10.0	14.6	18.5	17.5	<0.001
Sedatives use	2.2	2.1	2.8	3.0	0.25

Values are presented as mean±standard deviation, percentages, or median (interquartile range).

BMI, body mass index; ASM, appendicular skeletal muscle mass; SBP, systolic blood pressure; HDL-C, high-density lipoprotein cholesterol; hsCRP, high-sensitivity C-reactive protein.

Table 2.

Risk of Erosive Esophagitis according to Sarcopenia and Obesity Status

Subgroup	Normal OR	Obese OR (95% CI)	Sarcopenic OR (95% CI)	Sarcopenic obese OR (95% CI)	p-value
Crude model	1.00 (reference)	1.95 (1.79-2.12)	2.80 (1.92-4.09)	2.72 (2.29-3.24)	<0.001
Model 1 ^a	1.00 (reference)	1.53 (1.40-1.67)	2.23 (1.51-3.29)	1.93 (1.61-2.30)	<0.001
Model 2 ^b	1.00 (reference)	1.46 (1.33-1.59)	2.33 (1.57-3.46)	1.82 (1.51-2.18)	<0.001
Model 3 ^c	1.00 (reference)	1.44 (1.31-1.57)	2.28 (1.54-3.39)	1.75 (1.45-2.11)	<0.001
Model 4 ^d	1.00 (reference)	1.36 (1.23-1.49)	2.17 (1.45-3.24)	1.63 (1.35-1.97)	<0.001
Model 5 ^e	1.00 (reference)	1.35 (1.22-1.49)	2.12 (1.40-3.19)	1.54 (1.27-1.87)	<0.001

OR, odds ratio; CI, confidence interval; HDL, high-density lipoprotein.

^a Adjusted for age and sex;

^b Adjusted for age, sex, smoking status, alcohol intake, and regular exercise;

^c Adjusted for co-morbidities and/or medication use, aspirin use, and sedatives use in addition to the factors included in model 2;

^d Adjusted for systolic blood pressure, triglycerides, HDL-cholesterol, and fasting glucose in addition to the factors included in model 3;

^e Adjusted for the status of hiatal hernia in addition to the factors included in model 4.

Table 3.

The Risk of Erosive Esophagitis for Sarcopenic and Sarcopenic Obese Group Compared to the Obese Group

	Model 1 ^a		Model 2 ^b		Model 3 ^c
	OR (95% CI)	p-value	OR (95% CI)	p-value	OR (95% CI)	p-value
Obese	1.00 (reference)		1.00 (reference)		1.00 (reference)
Sarcopenic	1.46 (0.99-2.15)	0.05	1.63 (1.09-2.45)	0.02	1.63 (1.08-2.47)	0.02
Sarcopenic obese	1.26 (1.05-1.51)	0.01	1.25 (1.04-1.52)	0.02	1.22 (1.01-1.46)	0.04

OR, odds ratio; CI, confidence interval; HDL, high-density lipoprotein.

^a Adjusted for age and sex;

^b Adjusted for age, sex, smoking status, alcohol intake, regular exercise, co-morbidities and/or medication use, aspirin use, sedatives use, systolic blood pressure, triglycerides, HDL-cholesterol, and fasting glucose;

^c Adjusted for the status of hiatal hernia in addition to the factors included in model 2.

Table 4.

Risk of Erosive Esophagitis by LA Classification according to the Sarcopenia Status

	Multivariable-adjusted OR (95% CI)
	≥ LA-A	≥ LA-B	≥ LA-C
Cutoff values for sarcopenia
Normal	1.00 (reference)	1.00 (reference)	1.00 (reference)
Class I sarcopenia ^a	1.12 (1.01-1.24)	1.28 (1.02-1.61)	2.41 (0.91-6.43)
Class II sarcopenia ^b	1.35 (1.12-1.63)	1.54 (1.05-2.28)	4.21 (1.06-16.76)
p for trend	0.004	0.034	0.048
Per 1% decrease in ASM/weight	1.03 (1.01-1.05)	1.06 (1.00-1.11)	1.32 (1.07-1.52)
Central obesity
No	1.00 (reference)	1.00 (reference)	1.00 (reference)
Yes	1.35 (1.23-1.48)	1.57 (1.28-1.93)	2.37 (0.94-5.96)
p-value	<0.001	<0.001	0.068

Values are presented as median (range). A multivariable model was adjusted for age, sex, waist circumference, smoking status, alcohol intake, regular exercise, co-morbidities and/or medication use, aspirin use, sedatives use, systolic blood pressure, triglycerides, HDL-cholesterol, fasting glucose, and the status of hiatal hernia.

LA, Los Angeles; OR, odds ratio; CI, confidence interval; ASM, appendicular skeletal muscle mass; HDL, high-density lipoprotein.

^a Participants with class I sarcopenia were those with weight-adjusted skeletal muscle mass index between one and two standard deviations below the sex-specific values measured in young, healthy adults;

^b Participants with class II sarcopenia were those with weight-adjusted skeletal muscle mass index more than two standard deviations below the sex-specific values measured in young, healthy adults.

Table 5.

Risk of Erosive Esophagitis by Sarcopenia and Obesity Status in Clinically-relevant Subgroups

Subgroup	Normal	Obese	Sarcopenic	Sarcopenic obese	p for interaction
Age (years)					0.25
<60 (n=27,957)	Reference	1.52 (1.33-1.82)	2.77 (1.80-4.27)	1.91 (1.46-2.55)
≥60 (n=4,805)	Reference	1.33 (1.14-1.72)	2.03 (1.10-4.55)	1.48 (1.17-2.16)
Sex					0.69
Women (n=14,373)	Reference	1.45 (1.10-1.91)	1.73 (1.18-6.52)	2.45 (1.27-4.74)
Men (n=18,389)	Reference	1.46 (1.32-1.60)	2.32 (1.54-3.51)	1.74 (1.44-2.11)
Current smoking					0.5
No (n=25,584)	Reference	1.43 (1.27-1.61)	2.11 (1.32-3.38)	1.94 (1.54-2.44)
Yes (n=7,178)	Reference	1.51 (1.31-1.74)	2.65 (1.28-5.51)	1.56 (1.15-2.12)
Alcohol intake					0.96
Mild (n=27,736)	Reference	1.47 (1.31-1.63)	2.20 (1.41-3.44)	1.83 (1.47-2.28)
Modest (n=5,026)	Reference	1.46 (1.23-1.74)	2.61 (1.10-6.16)	1.70 (1.21-2.39)
Regular exercise					0.06
No (n=23,395)	Reference	1.47 (1.32-1.64)	2.84 (1.84-4.38)	1.96 (1.60-2.41)
Yes (n=9,367)	Reference	1.44 (1.21-1.71)	2.14 (1.21-4.72)	1.44 (1.13-1.92)

Values are presented as median (range). Estimated from logistic regression models adjusted for age, sex, smoking status, alcohol intake, regular exercise, and metabolic variables.

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ORCID iDs: Hyuk Lee
https://orcid.org/0000-0003-4271-7205
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