Alimentary Pharmacology & Therapeutics

The prevalence of and risk factors for erosive oesophagitis and

non-erosive reflux disease: a nationwide multicentre prospective
study in Korea
N. KIM*, S. W. LEE, S. I. CHO, C. G. PARK, C. H. YANG , H. S. KIM**, J. S. REW**, J. S. MOON,
S. KIM, S. H. PARK, H. C. JUNG*, I. S. CHUNG & THE H. PYLORI AND GERD STUDY GROUP
OF KOREAN COLLEGE OF HELICOBACTER AND UPPER GASTROINTESTINAL RESEARCH

*Department of Internal Medicine,

Seoul National University College of
Medicine, Seoul, Korea; Department
of Internal Medicine, Korea University, Ansan, Korea; School of Public
Health and Institute of Health and
Environment, Seoul National University, Seoul, Korea; Department of
Internal Medicine, Chosun University,
Gwangju, Korea; Department of
Internal Medicine, DongGuk
University, Pohang, Korea;
**Department of Internal Medicine,
Chonnam National University,
Gwangju, Korea; Department of
Internal Medicine, Inje University,
Seoul Paik Hospital, Seoul, Korea;
Department of Internal Medicine,
Kyungpook National University
Hospital, Daegu, Korea; Department
of Internal Medicine, Catholic University, Seoul, Korea
Correspondence to:
Dr I.-S. Chung, Department of Internal
Medicine, The Catholic University of
Korea, Kangnam St Marys Hospital,
505 Banpo-dong, Seocho-gu, Seoul
137-040, Korea.
E-mail: isc@catholic.ac.kr

Publication data
Submitted 12 September 2007
First decision 24 September 2007
Resubmitted 8 October 2007
Second decision 16 October 2007
Accepted 23 October 2007

SUMMARY
Background
Prospective nationwide multicentre studies that have evaluated endoscopic findings and reflux symptoms using a well-designed questionnaire are very rare.
Aim
To compare the prevalence rates of and risk factors for erosive oesophagitis and non-erosive reflux disease (NERD) in the Korean population.
Methods
A gastroscopic examination was performed on 25 536 subjects who visited 40 Healthcare Centers for a health check-up. A gastro-oesophageal
reflux questionnaire and multivariate analysis were used to determine
the risk factors for erosive oesophagitis and NERD.
Results
2019 (8%) and 996 subjects (4%) had erosive oesophagitis and non-erosive reflux disease, respectively; only 58% of subjects with erosive
oesophagitis had reflux symptoms. Multivariate analysis showed that the
risk factors for erosive oesophagitis and NERD differed, i.e. those of erosive oesophagitis were male, a Helicobacter pylori eradication history,
alcohol, body mass index 25 and hiatal hernia. In contrast, the risk factors for NERD were female, age <40 and 60 vs. 4059 years, body mass
index <23 and a monthly income <$1000, glucose 126 mg dL, smoking, a stooping posture at work and antibiotic usage.
Conclusions
The prevalence rates of erosive oesophagitis and NERD were 8% and
4%, respectively, in Korean health check-up subjects. The risk factors
for erosive oesophagitis and NERD were found to differ, which indicates
that their underlying pathogeneses are distinct.
Aliment Pharmacol Ther 27, 173185

2008 The Authors

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doi:10.1111/j.1365-2036.2007.03561.x

173

174 N . K I M et al.

INTRODUCTION
Gastro-oesophageal reflux disease (GERD) is caused by
abnormal reflux of gastric contents into the oesophagus and is characterized by specific symptoms such as
heartburn and acid regurgitation.15 However, only
about one-third to one-half of GERD patients have
endoscopically positive findings such as erosions and
ulcers, whereas others with GERD symptoms have no
obvious mucosal breaks during endoscopic examination.613 Thus, oesophagitis is being increasingly
viewed as a complication of GERD.14 The 1999 Genval
workshop report15 redefined GERD as a disorder in
which gastric contents recurrently reflux into the
oesophagus causing heartburn and other symptoms.
However, some patients have complications of gastrooesophageal reflux without the typical symptoms. In
2005, the American College of Gastroenterology published practice guidelines,12 and defined the diagnosis
of GERD as symptoms or mucosal damage produced
by abnormal reflux of gastric contents into the
oesophagus. Recently, the Montreal workshop report16
also defined GERD as a condition that develops when
the reflux of stomach contents causes troublesome
symptoms and or complications such as reflux
oesophagitis, stricture, Barretts oesophagus (BE) or
oesophageal adenocarcinoma, and subclassified the
disease into oesophageal or extraoesophageal syndromes. Therefore, GERD includes erosive oesophagitis
and endoscopy-negative reflux disease, which is also
known as non-erosive reflux disease (NERD). The
pathogeneses of these two categories of GERD are
believed to differ. For example, heartburn in NERD is
associated with a lower response to proton pump
inhibitor (PPI) acid suppression than heartburn in the
case of erosive oesophagitis.17 In addition, it is not
clear why some erosive oesophagitis patients suffer
from symptoms such as, heartburn and regurgitation,
while others with an apparently similar reflux profile
do not.1
Gastro-oesophageal reflux disease is known to be a
major clinical problem in Western countries, i.e. 14
24% of adults experience heartburn and acid regurgitation at least once a week,6, 1822 and recently, the
frequency has increased to approximately one-third
of the adult population.23, 24 In contrast, the prevalence of GERD (based on reflux symptoms) in East
Asia ranges from 3% to 7% for at least weekly
symptoms of heartburn and or acid regurgitation.2532 In addition, case study data have shown

that the prevalence rates of oesophagitis in the East

Asian populations range from 3% to 16%,3338 which
are lower than that in the West. As Korean society
becomes increasingly westernized, Korean gastroenterologists commonly encounter individuals with reflux
symptoms, thus it is expected that the prevalence of
erosive oesophagitis and NERD will increase. In addition, because response failure to PPI is frequently
encountered in the clinical setting,39 especially, in
the NERD patients, the pathogeneses of erosive
oesophagitis and NERD are presumed to differ. However, large-scale prospective nationwide multicentre
studies have not been conducted to evaluate the
endoscopic findings and reflux symptoms using welldesigned questionnaires.
Health check-ups have recently become popular in
Korea, because such examinations allow the general
health to be checked in a few hours. Most Korean hospitals are now equipped with a Healthcare Center to
provide such health check-ups. Moreover, oesophagogastroduodenoscopy is performed as a part of a gastric
cancer-screening
programme.
A
questionnaire
designed to determine the subjects general health and
the presence of clinical symptoms is administered
before each health check-up examination. In addition,
research regarding national health issues is frequently
carried out in these Healthcare Center visitors because
the individuals undergoing screening are generally
regarded as representative of the general population.
Set against this background, we undertook this study
to evaluate the prevalence rates and risk factors of
erosive oesophagitis and NERD in 25 536 subjects who
visited 40 Healthcare Centers in South Korea for a
routine health check-up.

METHODS
Preparation of study
The design of this study was prepared by the Scientific
Committee of the Korean College of Helicobacter and
Upper Gastrointestinal Research. A workshop was held
on 25 June 2005 to approve the study design and to
develop a unified description of endoscopic erosive
oesophagitis and to agree on a gastro-oesophageal
reflux questionnaire. After repeated feedbacks from
experts in this field and after conducting practical
field tests over a period of 3 months to validate the
reflux symptom questionnaires,40 the study was started
at the beginning of January 2006 and continued until
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P R E V A L E N C E O F , A N D R I S K F A C T O R S F O R , G E R D 175

the end of July 2006 at the Healthcare Centers of

40 hospitals nationwide, located in all seven Korean
provinces.

Inclusion and exclusion criteria

Subjects with a history of gastrointestinal surgery or
with systemic disease requiring chronic medication
(except hypertension and diabetes mellitus) were
excluded. All subjects (over 16 years old) who agreed
to participate in this nationwide survey, by completion
of the gastro-oesophageal reflux questionnaire, and to
undergo endoscopy were included.

antidepressants, tranquilizers, liver drugs and gastroduodenal drugs), (2) the presence of diseases (again
split into seven categories, diabetes mellitus, liver disease, kidney disease, neuromuscular disease, heart
lung disease, gastroduodenal disease and other chronic
illness), (3) history of Helicobacter pylori eradication, (4)
alcohol consumption, (5) smoking, (6) a stooping
posture at work and (7) income per month. Body mass
indices (BMI) and biochemical test results, which
included glucose, cholesterol, triglyceride, H. pylori
tests (anti-H. pylori IgG, CLOtest or histology) and bone
densitometry findings were entered by assistants.

Oesophagogastric examinations
Questionnaire
An assistant conducted face-to-face interviews using
the gastro-oesophageal reflux questionnaire before
endoscopy at the 40 Healthcare Centers. The questionnaire consisted of 14 items, and included questions on
six reflux symptoms, namely, heartburn, acid regurgitation, chest pain, hoarseness, globus sensation and
coughing. The questions were as follows: 1. Have you
experienced heartburn [(a) soreness in the substernal
area, (b) a burning sensation or discomfort in the
substernal area or (c) a burning sensation induced by
water swallowing] within the past year?; 2. Have you
experienced acid regurgitation [(a) sour water brash in
the mouth or throat, (b) a sense of food regurgitation]
within the past year?; 3. Have you experienced chest
pain within the past year?; 4. Have you experienced
hoarseness within the past year?; 5. Have you experienced a globus sensation in the throat [(a) a foreign
body sensation in the throat, (b) a sticky food sensation in the substernal area] within the past year?; 6.
Have you experienced a frequent cough within the
past year? Subjects who responded positively to any
one of these six symptoms were asked to choose the
most bothersome symptom. In addition, the frequency
[(a) 12 times per year, (b) 12 times per month, (c)
12 times per week, (d) 34 times per week and (e)
daily] and severity [(a) mild, (b) moderate, bothersome
to everyday life and (c) severely disturbing work or
sleeping] of the most bothersome symptom were determined. In addition, the subjects were asked whether
they had taken H2 blocker or PPI to relieve these
symptoms. The next seven questions addressed factors
related to GERD, i.e. (1) a drug history (split into seven
major categories, aspirin or nonsteroidal anti-inflammatory drug (NSAID), antihypertensive, antibiotics,
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All study subjects underwent upper gastrointestinal

endoscopic examinations, which were performed by 51
well-trained gastroenterologists with at least 5 years of
endoscopy experience. All gastroenterologists who
participated in the workshop agreed on the description
method of erosive oesophagitis. Moreover, they also
agreed upon a method of diagnosing erosive oesophagitis in the workshop. Interobserver consistency was
tested using an electronic voting system and was
found to be over 95%. In addition, an educational
poster describing the agreed upon principles and
containing representative figures regarding erosive
oesophagitis, was distributed to the participating
gastroenterologists for reference purposes. The gastrooesophageal junction was defined as the squamocolumnar junction, the proximal margin of gastric
folds or the location of the pinchcock. The endoscopic
findings of erosive oesophagitis in the lower oesophagus were classified using the Los Angeles (LA) classification as grades AD (LA-A to D), and were based on
the longest length of a mucosal break, and the confluence of erosions. In addition, the number of mucosal
breaks was documented. Endoscopic photo-images of
erosive oesophagitis were transmitted to the Korean
College of Helicobacter and Upper Gastrointestinal
Research Scientific Committee, and the board members
(N.K. and J.J.P.) reviewed endoscopic photo-images.
Gastroscopic findings such as benign gastric ulcer,
duodenal ulcer and gastric cancer were also described.
The gastric cancers were confirmed by biopsy.

Definition of erosive oesophagitis and NERD

Erosive oesophagitis was defined based on the endoscopic findings according to the LA classification,

176 N . K I M et al.

which is based on the length of the longest mucosal

break, and confluence of erosions. NERD was diagnosed when a subject responded that heartburn or acid
regurgitation was the most bothersome symptom at a
frequency of at least once per week in the absence of
erosive oesophagitis. The endoscopists were unaware
of the questionnaire results.

Statistical analysis
Erosive oesophagitis and NERD were compared for the
different variables mentioned above. The ages were
categorized in deciles. BMI was categorized using 23
and 25 (kg m2) as cut-off points in accord with the
WHO recommendations for Asians. Blood glucose,
cholesterol and triglyceride levels were recorded using
the standard clinical cut-off points (126, 200 and
150 mg dL, respectively). The chi-squared test was
used to assess associations between covariates and
the prevalence of erosive oesophagitis and NERD. The
covariates that showed a significant association by the
chi-squared test were analysed by a multiple logistic
regression analyses. Model fit was assessed using the
Hosmer-Lemeshow goodness-of-fit test. The variables
that were significant according to the models or that
improved the model fit were included in the final
models, which showed appropriate goodness-of-fit
(P > 0.10). All analyses were performed using SAS statistical software. Differences were considered significant when the P-values were <0.05.

RESULTS
Characteristics of the participants
The response rate of the participants to the reflux
symptom questionnaire was 100%, and thus a nonresponse study was not required. Totally, 25 536 subjects (male 15 180, 59%; female 10 356, 41%) were
included in this study, and the mean subject age was
46.7 years. When the study population was compared
with the background population data collected in 2005
(http://www.index.go.kr/gams/default.jsp and http://
www.kosis.kr) in terms of gender, age and geographical area, the proportion of males and representation of
the 4059 age group were higher in the study population compared with the background population (Table 1).
However, the geographical distribution was representative of the Seoul population and the six other provinces. Demographic data regarding the educational

level, income, current smoking, alcohol, co-morbidities

(such as hypertension and diabetes) and BMI showed
that the income and education level were higher in the
study group than in the general Korean population in
2005.41 However, the other factors were comparable to
the background population. The endoscopic findings
included benign gastric ulcer (active 409, healing stage
423) and duodenal ulcer (active 243, healing stage
291). In addition, gastric cancer was confirmed histologically in the 65 subjects (0.25%; early gastric cancer 47, advanced gastric cancer 18).

Prevalence of erosive oesophagitis and NERD

Erosive oesophagitis was found in 2019 (8%) of the
25 536 participants; 1497 (6%) in LA-A, 471 (2%) in
LA-B, 47 (0.2%) in LA-C and four (0.02%) in LA-D. In
the absence of erosive oesophagitis, 996 subjects (4%)
of the 25 536 subjects reported that they experienced
heartburn or acid regurgitation as the most bothersome symptom at least once per week. In comparison,
the prevalence of GERD symptoms (defined as heartburn and or acid regurgitation as the most bothersome
symptom at least once per week regardless of endoscopic findings) was 5% (1161) among the 22 960 subjects who responded to questions concerning the most
bothersome symptom and its frequency. When these
1161 subjects were classified according to endoscopic
findings, 996 (86%) had normal results and 165 (14%)
had erosive oesophagitis.

Comparison of erosive oesophagitis vs. NERD

with respect to age and sex
2019 of the 25 536 study subjects were found to have
erosive oesophagitis, 996 NERD and the remaining
22 521 normal. Of these three groups the gender distribution for the erosive oesophagitis (P = 0.0001) and
NERD (P = 0.0006) groups were found to differ from
that of the normal group (Table 2). In addition, a gender distribution difference was observed between the
erosive oesophagitis and NERD groups. Specifically,
there were more men (11%) than women (3%) in the
erosive oesophagitis group, but more women (5%)
than men (3%) in the NERD group (Table 2, Figure 1a).
The age distribution of the erosive oesophagitis
(P = 0.0019) and NERD groups (P = 0.0005) also differed from that of the normal group, and the age distribution of the erosive oesophagitis and NERD group
also differed (P = 0.0002). When the NERD group was
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P R E V A L E N C E O F , A N D R I S K F A C T O R S F O R , G E R D 177

Table 1. Characteristics of the participating subjects (n = 25 536)

Variable category

Study population (%)

Gender

Male:female

15 180:10 356 (59:41)

Age (years; mean  s.d.: 46.7  11.1)

1619
2029
3039
4049
5059
6069
70
Seoul
Gyeonggi (Seoul vicinity)
Kangwon
Chungcheong
Kyungsang
Cholla
Jeju
Among 24 966
Among 21 875
Among 21 875

57 (0.2)
1235 (5)
5684 (22)
8885 (35)
6126 (24)
2936 (12)
613 (2)
9625 (37)
3085 (12)
1965 (8)
3094 (12)
3646 (14)
3759 (15)
462 (2)
21 571 (86)
8905 (41)
1815 (8)
6529 (26)
10 470 (41)
2691 (11)
1103 (4)
7737 (31)
1616 (6)

Geographic area

Proportion of urban to area rural

Educational level (college)
Income ($1000 per month)
Current smoking
Alcohol (once per week)
Hypertension
Diabetes
Body mass index (25)
NSAID history for more
than 1 month
Antibiotics history for 1 month
Endoscopic findings
Benign gastric ulcer (active
or healing)
Duodenal ulcer (active or healing)
Gastric cancer (histologically
confirmed)

Among 24 966

Background population in
Korea, 2005 (%)*
24 191 000:23 947
000 (50:495)
313 000 (7)
7 606 000 (16)
8 520 500 (18)
8 184 000 (17)
5 151 000 (11)
361 000 (8)
270 000 (6)
10 173 000 (21)
13 042 000 (27)
1 521 000 (3)
4 885 000 (10)
12 668 000 (26)
5 294 000 (11)
555 000 (1)
78%
21%
21%
29%
55%
13%
5%
32%

253 (1)
832 (3)
534 (2)
65 (0.3)
EGC:AGC

47 :18 (3:1)

* Source: http://www.index.go.kr/gams, http://www.kosis.nso.go.kr and The Third National Health and Nutrition Examination
Survey in 2005.41
s.d., Standard deviation; EGC, early gastric cancer; AGC, advanced gastric cancer; NSAID, nonsteroidal anti-inflammatory
drug.

divided into three age categories the proportion of

subjects between 40 and 59 years (527, 4%) was found
to be significantly lower than in the <40 years (299,
4%; P = 0.0037) and 60 years categories (170, 5%;
P = 0.0003; Figure 1b). For the geographic distribution, the only significant differences found were
between the relative prevalence of erosive oesophagitis
and unaffected normal individuals (P = 0.0001). No
difference was found between erosive oesophagitis and
NERD.
2008 The Authors, Aliment Pharmacol Ther 27, 173185
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Erosive oesophagitis vs. NERD with respect to

reflux symptoms
Of the 25 536 subjects, 11 525 (45%) stated that they
had experienced at least one of the six symptoms
(heartburn, acid regurgitation, chest pain, hoarseness,
globus sensation or cough) on at least a few occasions
during the previous year. The most bothersome symptoms were heartburn (9%), acid regurgitation (8%) and
a globus sensation (8%). However, only 14% of the

178 N . K I M et al.

Table 2. Demographic data of erosive oesophagitis or NERD groups

Variable category
Gender, n (%)
Male
Female
Age (years)
1619
2029
3039
4049
5059
6069
70
Geographic area
Seoul
Gyeonggi (Seoul vicinity)
Kangwon
Chungcheong
Kyungsang
Cholla
Jeju

Normal
(n = 22 521)

Erosive oesophagitis
(n = 2019)

NERD
(n = 996)

Total
(n = 25 536)

P-value between
EE and NERD

12 965 (85)
9556 (92)

1699 (11)
320 (3)

516 (3)
480 (5)

15 180
10 356

0.0006

53
1091
5003
7840
5442
2574
518

(93.0)
(88.3)
(88.0)
(88.2)
(88.8)
(87.7)
(84.5)

2
74
454
723
479
220
67

(3.5)
(6.0)
(8.0)
(8.1)
(7.8)
(7.5)
(10.9)

2
70
227
322
205
142
28

(3.5)
(5.7)
(4.0)
(3.6)
(3.4)
(4.8)
(4.6)

57
1235
5684
8885
6126
2936
613

0.0002

8350
2707
1723
2793
3209
3351
387

(87.7)
(87.7)
(87.7)
(90.3)
(88.0)
(89.2)
(83.8)

798
258
165
199
294
253
52

(8.4)
(8.4)
(8.4)
(6.4)
(8.1)
(6.7)
(11.2)

377
120
77
101
170
155
23

(4.0)
(3.9)
(3.9)
(3.3)
(4.8)
(4.1)
(5.0)

9525
3085
1965
3093
3646
3759
462

0.4275

EE, erosive oesophagitis; NERD, non-erosive reflux disease.

(a) 20

(b) 20

Erosive oesophagitis

Erosive oesophagitis

Non-erosive reflux disease

Prevalence (%)

15

Non-erosive reflux disease

15

P < 0.0001

P = 0.0037 P = 0.0003

11.2%
10

10
P < 0.0001

4.6%
3.4% 3.1%

3.9%

8.0%

7.9%

7.5%

7.9%

4.8%

4.3%
3.5%

0
Male

Female

Total

<40

4059
Age (years)

25 536 suffered from at least one of these on a weekly

basis.
Excluding subjects with active or healing stage
benign gastric ulcer or duodenal ulcer, gastric cancer
or BE, symptom analysis was successfully performed
in the 20 154 normal, 1810 erosive oesophagitis and
996 NERD subjects. One thousand and fifty-five

60

Figure 1. Comparisons of erosive oesophagitis and non-erosive reflux disease with respect
to gender (a) and age (b).

(58%) of the 1810 erosive oesophagitis subjects had

experienced at least one of the six itemized refluxrelated symptoms (heartburn, acid regurgitation, chest
pain, hoarseness, globus sensation or cough) on at least
several occasions during the previous year, which
was significantly higher than the 41% of normal
subjects (P < 0.0001). In addition, all of these six
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P R E V A L E N C E O F , A N D R I S K F A C T O R S F O R , G E R D 179

Table 3. Reflux symptoms of

those with erosive oesophagitis
or non-erosive reflux disease
(NERD)

Normal
Erosive oesophagitis
(n = 20 154) (n = 1810)
NERD (n = 996)

Variable category
Any one of following six symptoms
Heartburn
Acid regurgitation
Chest pain
Hoarseness
Globus sensation
Cough
The most bothersome symptom
Heartburn
Acid regurgitation
Chest pain
Hoarseness
Globus sensation
Cough

8182
4587
4330
2759
1873
3685
1390

(40.6)
(22.8)
(21.1)
(13.7)
(9.3)
(18.3)
(6.9)

1345
1208
1047
584
1772
564

(6.7)
(6.0)
(5.2)
(2.9)
(8.8)
(2.8)

1055
603
644
299
221
413
197

(58.3)
(33.3)
(35.6)
(16.5)
(12.2)
(22.8)
(10.9)

208 (11.5)
237 (13.1)
85 (4.7)
47 (2.6)
161 (8.9)
74 (4.1)

996
704
712
329
182
344
130

(100)
(70.7)
(71.5)
(33.0)
(18.3)
(34.5)
(13.1)

518 (52.0)
478 (48.0)
0
0
0
0

Values given in parentheses are percentages.

symptoms were found more frequently in the subjects

with erosive oesophagitis than in normal subjects
(Table 3).
Subjects with erosive oesophagitis (58%; 1055 of
1810) had the following most bothersome symptoms:
heartburn 208 (12%), acid regurgitation 237 (13%),
chest pain 85 (5%), hoarseness 47 (3%), globus sensation 161 (9%) and a cough 74 (4%) (Table 3). These
figures show that heartburn and acid regurgitation
occurred in 25% of subjects. The remaining 20% of
subjects with erosive oesophagitis subjects responded
that chest pain or extraoesophageal symptoms (probably related with gastro-oesophageal reflux) were most
bothersome. When the reflux symptoms of 165 erosive
oesophagitis and 996 NERD subjects were compared,
no difference was found with respect to the prevalence, frequency or severity of the most bothersome
symptoms.

Risk factors for erosive oesophagitis and NERD

When the risk factors for erosive oesophagitis and
NERD, respectively, were compared with the normal
population, significant differences were observed. The
risk factors for erosive oesophagitis by univariate
analysis were male, alcohol consumption, a BMI 25,
hiatal hernia, smoking, a glucose level 126 mg dL, a
triglyceride level 150 mg dL and a history of
H. pylori eradication, whereas H. pylori infection was
2008 The Authors, Aliment Pharmacol Ther 27, 173185
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found to be a protective factor. Multivariate analysis

identified male gender (OR 3.0, 95% CI: 2.263.98),
alcohol consumption (OR 1.5, 95% CI: 1.211.81), a
BMI 25 (OR 1.3, 95% CI: 1.051.52) and a hiatal hernia (OR 5.4, 95% CI: 3.737.70) and a history of
H. pylori eradication (OR 2.2, 95% CI: 1.602.75) as
risk factors: a H. pylori infection (OR 0.47, 95% CI:
0.390.58) was a protective factor for erosive oesophagitis (Table 4).
In contrast, the risk factors for NERD by univariate
analysis were; female gender, age below 40 or
60 years vs. 4059 years, a BMI <23 and a monthly
income of <$1000, a glucose level 126 mg dL, antibiotic medication history, smoking, a stooping posture
at work, a history of H. pylori eradication, hiatal
hernia and NSAID medication. The multivariate analysis identified the following as risk factors for NERD:
female gender (OR 1.3, 95% CI: 1.101.50), age below
40 vs. 4059 (OR 1.2, 95% CI: 1.061.45) or 60 vs.
4059 years (OR 1.3, 95% CI: 1.021.54), a BMI <23
(OR 1.2, 95% CI: 1.061.41), monthly income of
<$1000 (OR 1.4, 95% CI: 1.061.69), glucose level
126 mg dL (OR 1.3, 95% CI: 1.041.73), an antibiotic
medication history (OR 2.1, 95% CI: 1.283.34), smoking (OR 1.2, 95% CI: 1.031.43) and a stooping posture at work (OR 1.2, 95% CI: 1.061.69) (Table 5).
However, a history of H. pylori eradication, hiatal
hernia and NSAID medication were not statistically
significant by the multivariate analysis.

180 N . K I M et al.

Variable
Male
Alcohol consumption
Body mass index 25
Hiatal hernia 1 cm
Helicobacter pylori
eradication history
H. pylori-positive
Glucose 126 mg dL
Triglyceride 150 mg dL
Smoking
Medication for liver disease
Medication for heart disease

Normal
(n = 20 154)

Erosive oesophagitis
(n = 1810)

Odds
ratio

11 401
7681
6523
383
1572

(56.6)
(38.1)
(29.8)
(1.9)
(7.8)

1633
1050
757
212
223

(84.2)
(58.0)
(41.8)
(11.7)
(12.3)

3.0
1.5
1.3
5.4
2.2

2.263.98
1.211.81
1.051.55
3.737.70
1.602.75

12 173
987
4655
4655
504
2096

(60.4)
(4.9)
(23.1)
(23.1)
(2.5)
(10.4)

832
119
653
795
65
250

(46.0)
(6.6)
(36.1)
(41.0)
(3.6)
(13.8)

0.47
1.1
1.2
1.2
1.1
1.1

0.390.58
0.781.45
0.941.41
0.981.45
0.751.47
0.791.50

95% CI

Table 4. Multivariate analysis

of the risk factors for erosive
oesophagitis

CI, confidence interval.

Values given in parentheses are percentages.

Variable

Normal
(n = 20 154)

NERD
(n = 996)

Odds
ratio

95% CI

Female
Age below 40 than 4059 years
Age 60 than 4059 years
Body mass index <23
Monthly income <$1000
Glucose 126 mg dL
Antibiotic medication history
Smoking
Stooping posture at work
Helicobacter pylori eradication history
Hiatal hernia 1 cm
Medication of NSAIDs

8753
5502
3003
8384
1632
987
198
4655
3396
1572
383
1380

480
299
170
498
120
82
23
270
230
103
30
86

1.3
1.2
1.3
1.2
1.4
1.3
2.1
1.2
1.2
1.3
1.1
1.3

1.101.50
1.061.45
1.021.54
1.061.41
1.061.69
1.041.73
1.283.34
1.031.43
1.061.69
0.991.57
0.761.70
0.971.62

(43.4)
(27.3)
(13.7)
(41.6)
(8.1)
(4.9)
(1.0)
(23.1)
(16.9)
(7.8)
(1.9)
(6.8)

(48.2)
(30.0)
(17.1)
(50.0)
(12.0)
(8.2)
(2.3)
(27.1)
(23.0)
(10.2)
(3.0)
(8.6)

Table 5. Multivariate analysis

of the risk factors for NERD

NERD, non-erosive reflux disease; CI, confidence interval; NSAID, nonsteroidal antiinflammatory drug.
Values given in parentheses are percentages.

DISCUSSION
The disease GERD is associated with life style, diet,
socioeconomic factors and co-morbidity. To determine
whether this study population is representative of the
Korean general population, the demographic data in
the study were compared with those of a national population survey conducted in 2005.41 In terms of age,
geographic distribution, proportion living in a rural or
urban community, education level, smoking, alcohol
and presence of co-morbidity, only slight differences
were observed. Specifically, the proportion of males in

the study population (59%) was slightly higher than

that of the Korean population (50%). In addition,
income and educational level were higher in the study
population. However, smoking, alcohol and the prevalence of diabetes, which were identified to be the risk
factors for GERD in this study, were similar in both
populations. Therefore, the results of this study regarding GERD can be taken to represent the Korean population. In addition, a multicentre, multinational study7
conducted in primary care clinics in the United
Kingdom, Germany and Ireland, found that their
study population was similar to the Korean population
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P R E V A L E N C E O F , A N D R I S K F A C T O R S F O R , G E R D 181

in terms of gender, age, smoking and alcohol

consumption.
Many people experience upper gastrointestinal
symptoms from time to time, and the most common
gastrointestinal symptoms are heartburn and regurgitation in Western countries.42, 43 In our study, 11 525
(45%) of the 25 536 study subjects, who visited the
Healthcare Centers for a health check-up, stated that
they had experienced at least one of the following
symptoms: heartburn, acid regurgitation, chest pain,
hoarseness, globus sensation or a cough at least for
several days during the previous year. The most bothersome symptoms were heartburn (9%), acid regurgitation (8%) and a globus sensation (8%): 14% of 25 536
subjects stated that they had suffered from at least one
of these on a weekly basis. In the West, most aspects
of health-related quality of life were found to be
impaired in individuals with daily or weekly reflux
symptoms.44 In addition, reflux symptoms were associated with impaired well-being in the general Swedish
population.45 Thus, this study suggests that reflux
symptoms have become an important issue in Korea.
Therefore, determination of what percentage of these
symptoms is due to GERD and what percentage can be
attributed to the reflux symptoms of erosive oesophagitis as determined endoscopically are important
clinical issues.
For GERD symptoms, a prevalence of 4% was
reported for at least weekly heartburn and or acid
regurgitation in the rural and urban areas of Asan-si,
Korea in a 20002001 survey (n = 1471), in which
endoscopy was not performed.31 In this study (conducted in 2006), which was the first nationwide survey conducted in an Asian country to include
endoscopy and a well-designed questionnaire, the
investigations were performed on subjects presenting
for a health check-up, generally considered to be representative of the Korean population. In this study,
the prevalence of GERD symptoms was found to be
5%, which indicates that this prevalence may have
increased over the past 5 years, but nevertheless, was
lower than expected. The reason for this could be the
definition of GERD symptoms used in this study. That
is, GERD symptoms were defined when heartburn
and or acid regurgitation were considered to be the
most bothersome symptom among six reflux symptoms, and this may well be a limitation of this study.
However, in other Asian countries the prevalence of
at least weekly heartburn and or acid regurgitation
has been reported to be consistently below 7%.2532
2008 The Authors, Aliment Pharmacol Ther 27, 173185
Journal compilation 2008 Blackwell Publishing Ltd

In a 1998 Singapore study, an overall prevalence of

2% was found for at least monthly heartburn and or
reflux by face-to-face interviews (n = 696),46 and this
rapidly increased to 11% during a 5-year followup.47, 48 Recent systematic review of the prevalence
of reflux symptoms in the general population showed
that significant increases over time were found in
North American and European populations (North
American annual increase of 5%, P = 0.0005; European annual increase of 2%, P < 0.0001).49 However,
this was not found in an Asian study (annual
increase of 1%, P = 0.49).49
When 1161 GERD subjects (diagnosed based on
reflux symptoms), who experienced at least weekly
heartburn and or acid regurgitation as the most bothersome symptom, were classified by endoscopic findings, erosive oesophagitis was found in only 14% of
subjects (165 of 1161). This is substantially lower than
the figures quoted by previous reports, which found
that one-third to one-half of subjects with GERD
symptoms did not have obvious mucosal breaks demonstrated by endoscopy.613 The low rate observed in
this study is closely related to the finding that only
58% of the endoscopically diagnosed erosive oesophagitis subjects in the health check-up have experienced
one of the reflux symptoms within the previous year.
This type of asymptomatic erosive oesophagitis is
commonly encountered in Korean subjects during
health check-ups.50 Moreover, only 4% of endoscopically diagnosed erosive oesophagitis subjects showed
an aggravation in the erosive oesophagitis grade during a 3-year period following the endoscopic check-up
in the absence of treatment.50 Further research is necessary to determine the natural history of the disease
course, and the most appropriate approach for the
management of these erosive oesophagitis subjects
without reflux symptoms in terms of preventing the
complications of erosive oesophagitis.
In general, erosive oesophagitis is increasing in
Asia.26, 28, 46, 47, 51, 52 For example, it has increased
from 3% in the late 1970s to 1015% in the late
1990s as reported by a Japanese comparative study of
upper gastrointestinal endoscopies.51 In addition, it
has increased from 3% in the early 1990s to 13% in
20002001 based on a Malaysian study.52 In a Korean
study conducted in 1999, the prevalence of erosive
oesophagitis was reported to be 5% for patients with
symptoms related to the gastrointestinal tract
(n = 1010),53 and it was 3% in a group of asymptomatic subjects presenting for a health check-up in 2001

182 N . K I M et al.

(n = 7015).33 In this study, erosive oesophagitis was

found to be present in 8% of subjects presenting for a
health check-up. This is still lower than the levels
reported in other Asian countries-like Japan9, 51 and
Malaysia.52 This difference among countries is also
observed in the distribution based on the LA classification of erosive oesophagitis. In Korea, LA-A accounted
for 74%, LA-B 23% and LA-C plus LA-D of 3% in this
study, which differs from the LA-C plus LA-D of 12%
reported in Japan9 and the LA-C plus LA-D of 20%
reported in Malaysia.38 These differences regarding the
prevalence and severity of erosive oesophagitis in
Asian populations are not easily explained but may be
because of genetic background, diet or H. pylori infection status.
Reflux symptoms in Asians are frequently associated
with extraoesophageal symptoms. For example, in
Korea, the globus sensation, chest pain and nonobstructive dysphagia were found to be the main symptoms for 63% of GERD patients when GERD was
diagnosed by endoscopy, oesophageal manometry or
24-h ambulatory oesophageal pH meter criteria.54 In
this study, 45% of the erosive oesophagitis group
chose one of the six reflux symptoms (heartburn, acid
regurgitation, chest pain, hoarseness, globus sensation
and cough) as being most bothersome, but heartburn
and acid regurgitation were chosen only by 12% and
13%, respectively. The remaining 20% chose chest
pain (5%) or an extraoesophageal symptom such as
hoarseness (3%), a globus sensation (9%) or a cough
(4%), which suggests that the reflux symptom spectrum differs in Korea from that in the West.15 Similarly, significant associations were reported between
GERD and chest pain, dysphagia, globus sensation,
hoarseness, asthma and bronchitis in another Korean
study,31 and between GERD and chest pain, chronic
cough, hoarseness, asthma and pneumonia in a Hong
Kong population.25 These findings suggest that extraoesophageal symptoms are very important as GERD
symptoms in Asia. Thus, further research is required to
determine whether these symptoms should be used as
diagnostic criteria for GERD.
When erosive oesophagitis and NERD were compared in this study, the risk factors for erosive oesophagitis and NERD were found to be quite different. The
significant risk factors for erosive oesophagitis by
multivariate analysis were: male gender, regular alcohol drinking, BMI 25, hiatal hernia and a history of
H. pylori eradication. Furthermore, a H. pylori-positive
state was found to protect against erosive oesophagitis.

These results suggest that H. pylori-associated inflammation plays a role in the prevention of the development of erosive oesophagitis, which is consistent with
a previous report.55, 56 In contrast, the risk factors for
NERD were: female, an age below 40 or 60 vs. 40
59, a low BMI <23, a monthly income <$1000, a glucose level of 126 mg dL, an antibiotic medication
history, smoking and a stooping posture at work.
These results suggest that physical factors that affect
lower oesophageal pressure or acid secretion are risk
factors for erosive oesophagitis. In contrast, factors
that are affected by socioeconomic status appear to be
related to heartburn and or acid regurgitation in the
absence of mucosal breaks by endoscopy. Different
risk factors for erosive oesophagitis and NERD have
been reported in Japan,9, 13 which support the likelihood that the pathogenesis differs for these two categories of GERD. However, it has been suggested that
GERD is not a categorical disease because 25% of
patients with NERD at baseline progressed to LA A B
and 1% to LA C D after 2 years in Germany, Austria
and Switzerland.57 Further research is needed to
address this issue.
In addition to the GERD findings, another gastrointestinal disease pattern was found in the 25 536 health
check-up subjects, namely, that the prevalence rates of
the active and healing stages of benign gastric ulcer
and duodenal ulcer were 3% and 2%, respectively,
which is lower than that of erosive oesophagitis (8%).
This pattern of gastrointestinal disease might be
related to a decrease in the prevalence of H. pylori
and an increase in BMI (25, 31% in this study). A
two nation-wide seroprevalence survey performed in
1998 and 2005 among asymptomatic Korean adults
over the age 16 found the H. pylori prevalence of
67%58 and 60%,59 respectively. The prevalence of gastric cancer, which is unacceptably high in Korea, by
the age standardized incidence of gastric cancer during
19902001 in South Korea, as determined by the Cancer Registry at the Korean National Cancer Center in
2002, was 65.6 per 100 000 person-years for men and
25.8 for women. The detection rate of gastric cancer
(in histologically confirmed cases) in this study was
0.3% and the proportion of early gastric cancer (47
subjects) to advanced gastric cancer (18 subjects) was
72%, which demonstrate that the instituted health
check-up programmes have been successful in detecting early gastric cancer.
In conclusion, this nationwide, multicentre, well
designed, prospective study shows that the prevalence
2008 The Authors, Aliment Pharmacol Ther 27, 173185
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P R E V A L E N C E O F , A N D R I S K F A C T O R S F O R , G E R D 183

rates of erosive oesophagitis and NERD were 8% and

4%, respectively, which corresponds to a prevalence
rate of GERD of 12% in Korea. Moreover, 42% of subjects with erosive oesophagitis were asymptomatic and
the risk factors for erosive oesophagitis and NERD
were found to differ, which suggest that their underlying pathogenesis may differ.

ACKNOWLEDGEMENTS
The authors thank the following participating gastroenterologists for their contribution to this study:
Ki-Nam Shim, Ewha Womans University Hospital;
Jun Haeng Lee, Samsung Medical Center; Jae Woo
Kim, Wonju University; Hyun Jin Kim, Kyungsang
University; Moon Gi Chung, Gachon Medical School,
Seon Mee Park, Chungbuk National University;
Gwang Ho Baik, Hallym University; Byung Kyu Nah,
University of Ulsan; Su Youn Nam, Korean National
Cancer Center; Kang Seok Seo, Kwangju Christian
Hospital; Yun-Ju Jo and Byung Sung Ko, Eulji

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