Original article 495

Gastro-oesophageal reflux disease, reflux oesophagitis and

non-erosive reflux disease in a multiracial Asian population:
a prospective, endoscopy based study
Modh Said Rosaida and Khean-Lee Goh

Objective To determine the prevalence of and risk factors strictures. Following logistic regression analysis, the
for gastro-oesophageal reflux disease (GORD), reflux independent risk factors for GORD were Indian race (odds
oesophagitis and non-erosive reflux disease (NERD) ratio (OR), 3.25; 95% confidence interval (CI), 2.38–4.45),
amongst Malaysian patients undergoing upper Malay race (OR, 1.67; 95% CI, 1.16–2.38), BMI > 25 (OR,
gastrointestinal endoscopic examination. 1.41; 95% CI, 1.04–1.92), presence of hiatus hernia (OR,
4.21; 95% CI, 2.41–7.36), alcohol consumption (OR, 2.42;
Design A cross-sectional study on consecutive patients 95% CI, 1.11–5.23) and high education level (OR, 1.52;
with dyspepsia undergoing upper gastrointestinal 95% CI, 1.02–2.26). For reflux oesophagitis independent
endoscopy. the risk factors male gender (OR, 1.64; 95% CI, 1.08–2.49),
Indian race (OR, 3.25; 95% CI, 2.05–5.17), presence of
Setting A large general hospital in Kuala Lumpur, hiatus hernia (OR, 11.67; 95% CI, 6.40–21.26) and alcohol
Malaysia. consumption (OR, 3.22; 95% CI, 1.26–8.22). For NERD the
independent risk factors were Indian race (OR, 3.45; 95%
Participants Consecutive patients undergoing endoscopy CI, 2.42–4.92), Malay race (OR, 1.80; 95% CI, 1.20–2.69),
for upper abdominal discomfort were examined for the BMI > 25 (OR, 1.47; 95% CI, 1.04, 2.06) and high education
presence of reflux oesophagitis, hiatus hernia and level (OR, 1.66; 95% CI, 1.06–2.59).
Barrett’s oesophagus. The diagnosis and classification of
reflux oesophagitis was based on the Los Angeles Conclusions Reflux oesophagitis and Barrett’s
classification. Patients with predominant symptoms of oesophagus were not as uncommon as previously thought
heartburn or acid regurgitation of at least one per month in a multiracial Asian population and a significant
for the past 6 months in the absence of reflux oesophagitis proportion of our patients had severe grades of reflux
were diagnosed as having NERD. The prevalence of GORD, oesophagitis. NERD, however, still constituted the larger
reflux oesophagitis and NERD were analysed in relation to proportion of patients with GORD. Indian race was
age, gender, race, body mass index (BMI), presence of consistently a significant independent risk factor for reflux
hiatus hernia, Helicobacter pylori status, alcohol intake, oesophagitis, NERD and for GORD overall. Eur J
smoking and level of education. Gastroenterol Hepatol 16:495–501 & 2004 Lippincott
Williams & Wilkins
Results One thousand patients were studied
prospectively. Three hundred and eighty-eight patients European Journal of Gastroenterology & Hepatology 2004, 16:495–501
(38.8%) were diagnosed as having GORD based on either
Keywords: gastro-oesophageal reflux disease, reflux oesophagitis, non-
predominant symptoms of heartburn and acid erosive reflux disease, prevalence, risk factors, multiracial Asian population
regurgitation and/or findings of reflux oesophagitis. One
Division of Gastroenterology, Dept of Medicine, University of Malaya, Kuala
hundred and thirty-four patients (13.4%) had endoscopic Lumpur, Malaysia.
evidence of reflux oesophagitis. Two hundred and fifty-four
Correspondence to Professor K.L. Goh, Department of Medicine, Faculty of
(65.5%) were diagnosed as having NERD. Hiatus hernia Medicine, University of Malaya, 50603 Kuala Lumpur, Malaysia.
was found in 6.7% and Barrett’s oesophagus in 2% of Tel: +60 3 795 02555; fax: +60 3 795 57740; e-mail: gohkl@um.edu.my
patients. Of our patients with reflux oesophagitis 20.1% Received 23 September 2003
had grade C and D oesophagitis. No patients had Accepted 20 November 2003

Introduction oesophagitis [2,3,4]. Various factors have been postu-

Gastro-oesophageal reflux disease (GORD) and reflux lated for this low prevalence, including diet, lower body
oesophagitis have been thought to be uncommon mass index (BMI) and genetic factors [1]. On the other
amongst Asians [1]. In clinical practice, particularly in hand, it has also been suggested that the reported low
East Asia, a diagnosis of peptic ulcer disease is much prevalence may be due to missed diagnosis of the
more commonly made than that of GORD or reflux condition [1].
0954-691X & 2004 Lippincott Williams & Wilkins DOI: 10.1097/01.meg.0000108291.74393.2c

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 496 European Journal of Gastroenterology & Hepatology 2004, Vol 16 No 5

There has been some evidence, however, that the phagitis was based on the Los Angeles classification [8]:
prevalence of reflux oesophagitis may be increasing in grade A, one or more mucosal breaks no longer than
Asians. In 1997 Yeh et al. reported a prevalence rate of 5 mm, none of which extends between the tops of the
14.5% [5]. In two recent consecutive surveys carried mucosal folds; grade B, one or more mucosal breaks
out on the same study population in our medical centre, more than 5 mm long, none of which extends between
a significant rise in the prevalence of reflux oesophagitis the tops of the mucosal folds; grade C, mucosal breaks
was noted [6,7]. There has to be some caution, how- that extend between the tops of two or more mucosal
ever, in interpreting prevalence figures from different folds, but which involve less than 75% of the oesopha-
studies, as surveys of reflux oesophagitis are exposed to geal circumference; and grade D, mucosal breaks which
confounding factors such as differences in the diagnos- involve at least 75% of the oesophageal circumference.
tic criteria used and variability in the interpretation of Hiatus hernia was defined as the occurrence of the Z
these criteria. Furthermore, several of the studies were line more than 1.5 cm higher than the cardio-oesopha-
retrospective in nature and may have underestimated geal junction. Barrett’s oesophagus was diagnosed when
the true prevalence of reflux oesophagitis. columnar epithelium was seen extending above the Z
line and confirmed on histological examination to show
In this prospective study we set out to accurately specialized intestinal metaplasia. These criteria were
determine the prevalence of GORD, reflux oesophagi- consistently applied and endoscopic diagnosis was con-
tis and non-erosive reflux disease (NERD) in a large firmed by either of the authors who were present
sample population of patients undergoing upper gastro- during every endoscopic procedure. Patients who re-
intestinal endoscopy. We also sought to determine the turned for endoscopic reassessment for any reason were
risk factors for the disease in this group of patients. In a excluded from the analysis to prevent duplication of
multiracial Asian population, with three major races – cases. Patients considered to have GORD but without
Malay, Chinese and Indian – living together, we were evidence of reflux oesophagitis were diagnosed as
particularly interested to know if ethnicity was a risk having NERD.
factor for GORD, reflux oesophagitis and NERD.
A previously validated [9] rapid urease test for the
Patients, materials and methods diagnosis of Helicobacter pylori, with a reported sensitiv-
A cross-sectional study was carried out on consecutive ity of 96.6% and a specificity of 99.2%, was routinely
patients with dyspepsia undergoing upper gastrointest- performed on antral and corpus biopsies in all patients.
inal endoscopy at the Endoscopy Unit, University of The study was approved by the ethics committee of
Malaya Medical Centre, Kuala Lumpur from June 2001 the University of Malaya Medical Centre.
to February 2002. The endoscopy service at our centre
is an open access facility within the hospital, which Statistical analysis
serves a large population in and around Kuala Lumpur. Comparison between proportions was carried out using
Patients who undergo upper gastrointestinal endoscopy the chi-squared test or Fisher’s exact test where appro-
were predominantly primary care patients. priate. A 2-tailed test was used and a P value of , 0.05
was taken as significant. The prevalence of GORD,
All subjects received a detailed questionnaire and were reflux oesophagitis and NERD was analysed in relation
interviewed by a single doctor before endoscopy. to the following variables: gender, age, race, H. pylori
Verbal consent was obtained from all patients before status, BMI, presence of hiatus hernia, level of educa-
the questionnaire was administered. Patients who had tion, smoking and alcohol intake. Odds ratios (ORs) of
taken proton pump inhibitors or H2 antagonists over the various conditions in the presence of a particular
the preceding 2 weeks were excluded from the survey. factor were used as a measure of association and are
Heartburn was defined as a burning or tight sensation presented with the 95% confidence interval (CI).
arising from the epigastrium and rising upwards retro- Factors with a P value of , 0.20 were subjected to
sternally. Acid regurgitation was defined as a sensation multivariate analysis using multiple binomial logistic
of acid coming up from the throat into the mouth regression analysis. Statistical analysis was performed
leaving a sour taste in the mouth. To avoid misdiagno- using SPSS 11.5 (for Windows) statistical program.
sis, patients were asked to describe their complaints of
heartburn and/or acid regurgitation to determine their Results
accuracy. Patients with predominant symptoms of One thousand consecutive patients were recruited for
heartburn and/or acid regurgitation occurring at least the study. The basic demography data of these patients
once per month for the past 6 months were considered are as follows: 442 (44.2%) males and 558 (55.8%)
to have GORD. females; mean age 51.1 years with a range 15–93 years.
The racial distribution of the patients was as follows:
Patients were examined for the presence of reflux Malays, 157 (15.7%), Chinese, 589 (58.9%) and Indian,
oesophagitis. Diagnosis and classification of reflux oeso- 254 (25.4%).

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 Gastro-oesophageal reflux disease in Asians Rosaida and Goh 497

Prevalence of GORD, reflux oesophagitis and NERD Indian versus Malay and Chinese was highly statisti-
Based on the presence of reflux oesophagitis and/or the cally significant (P , 0.001). The prevalence of GORD
presence of predominant reflux symptoms, 388 patients in Malay patients was also significantly higher com-
(38.8%) were diagnosed as having GORD. One hun- pared to Chinese (P , 0.001). Amongst Indian patients
dred and thirty-four patients (13.4%) were found to with GORD, 115 (65.3%) had NERD and 61 (34.7%)
have objective findings of reflux oesophagitis. Of these had reflux oesophagitis. Fifty-eight (71.6%) Malay
134 patients, only 78 (58.2%) reported predominant patients with GORD had NERD, while 23 ((28.4%)
symptoms of heartburn or acid regurgitation consistent had reflux oesophagitis. Amongst the Chinese patients
with the diagnosis of GORD. with GORD, 81 (61.8%) had NERD and 50 (38.2%)
had reflux oesophagitis.
Two hundred and fifty-four patients were diagnosed as
having GORD based on predominant symptoms of
Severity and complications of reflux oesophagitis and
heartburn and regurgitation alone without evidence of
correlation with symptoms
reflux oesophagitis. They were diagnosed as having
The distribution of different grades of reflux oesophagi-
NERD and comprised 65.5% of the total group of
tis is shown in Table 2. The majority of patients had
patients with GORD (Fig. 1).
grade A or B reflux oesophagitis (79.9%). Eighteen
patients (13.4%) had grade C reflux oesophagitis and
Racial distribution of GORD, reflux oesophagitis and NERD nine (6.7%) had grade D. Hiatus hernia was detected in
The racial distribution of GORD, reflux oesophagitis 67 patients (6.7%) and Barrett’s oesophagus in 20 (2%).
and NERD is shown in Table 1. Overall, for GORD, The prevalence of Barrett’s oesophagus in the different
the prevalence amongst Indians (56.6%) was the high- races was as follows: Indians, 11/250 (4.4%), Malay, 1/
est, followed by Malays (39.3%) and Chinese (27.1%). 183 (0.5%) and Chinese, 7/483 (1.4%). The differences
The difference in prevalence of GORD between between Indian versus Chinese and Malay were statis-
tically significant (P ¼ 0.028 and 0.016, respectively).
No strictures were noted in any of our patients.
Fig. 1
For all grades of reflux oesophagitis except for grade C
GORD only slightly more than half the patients complained of
n ⫽ 388 typical symptoms of GORD. Among grade C patients,
77.8% complained of heartburn and/or acid regurgita-
tion.

With RO
n ⫽ 134 Predominant symptoms of Table 2 Grading of reflux oesophagitis and the presence of
heartburn and regurgitation symptoms of heartburn and/or acid regurgitation in 134 patients
without RO (NERD)
Overall Presence of
n ⫽ 254
Grade number* symptoms**

With symptoms A 82 (61.2%) 45/82 (54.9%)

Without symptoms
B 25 (18.7%) 14/25 (56.0%)
n ⫽ 78 n ⫽ 56 C 18 (13.4%) 14/18 (77.8%)
D 9 (6.7%) 5/9 (55.6%)
Diagnosis of gastro-oesophageal reflux disease (GORD) based on *Values in parentheses are the percentages of all patients with reflux
symptoms and the presence of reflux oesophagitis (RO).
oesophagitis. **Values in parentheses are the percentages of patients within the
grade.

Table 1 Distribution of gastro-oesophageal reflux disease (GORD), reflux oesophagitis

and non-erosive reflux disease (NERD), by racial group
Race*

Disease Malay Chinese Indian Total**

Controls 125 352 135 612

GORD 81 (39.3) 131 (27.1) 176 (56.6) 388
Reflux oesophagitis 23 (11.2) 50 (10.4) 61 (19.6) 134
NERD 58 (28.2) 81 (16.8) 115 (37.0) 254
Total** 206 483 311 1000

*Values in parentheses are the percentages within the racial group. **Number of controls + number of
patients with GORD.

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 498 European Journal of Gastroenterology & Hepatology 2004, Vol 16 No 5

Comparison between GORD and non-GORD patients Table 4 Association between variables, determined by using
The prevalences of various variables in GORD patients univariate analysis: reflux oesophagitis (n 134) versus non-
GORD (n 612) patients
compared to non-GORD patients are shown in Table
3. On univariate analysis, Indian and Malay (vs Chi- RO present, Univariate OR
Variable n (%) P value (95% CI)
nese), BMI . 25, presence of hiatus hernia, alcohol
consumption and medium education level were found Age (years)
. 65 30/170 (17.6) 0.993 0.97 (0.61–1.56)
to be significant. On multivariate analysis, Indian race <65 104/576 (18.1)
(OR, 3.25; 95% CI, 2.38–4.45), Malay race (OR, 1.67; Gender
95% CI, 1.16–2.38), BMI . 25 (OR, 1.41; 95% CI, Male 77/343 (22.4) 0.004 1.76 (1.18–2.61)
Female 57/403 (14.1)
1.04–1.92), presence of hiatus hernia (OR, 4.21; 95% Race (vs Malay)
CI, 2.41–7.36), alcohol consumption (OR, 2.42; 95% Indian 61/196 (31.1) , 0.001 3.18 (2.04–4.97)
Malay 23/148 (15.5) 0.418 1.30 (0.73–2.28)
CI, 1.11–5.23) and high education level (OR, 1.52; Chinese 50/402 (12.4)
95% CI, 1.02–2.26) were found to be independent Body mass index
predictive factors for GORD. . 25 37/180 (20.6) 0.353 1.25 (0.80–1.95)
<25 97/566 (17.1)
Hiatus hernia
Yes 37/59 (62.7) , 0.001 10.23 (5.59–18.82)
No 97/687 (14.1)
Comparison between reflux oesophagitis versus non- Helicobacter pylori
GORD patients Yes 24/171 (14.0) 0.158 0.69 (0.42–1.14)
No 110/575 (19.1)
The prevalences of various variables in patients with Smoking
reflux oesophagitis compared to non-GORD patients Yes 21/111 (18.9) 0.880 1.08 (0.62–1.86)
are as shown in Table 4. On univariate analysis, male No 113/635 (17.8)
Alcohol
gender, Indian race (vs Chinese), presence of hiatus Yes 9/21 (42.9) 0.006 3.60 (1.36–9.39)
hernia and alcohol consumption were found to be No 125/725 (17.2)
Education level (vs high)
significant. On multivariate analysis, male gender (OR, High 24/133 (18.0) 0.787 1.12 (0.63–1.98)
1.64; 95% CI, 1.08–2.49), Indian race (OR, 3.25; 95% Medium 62/321 (19.3) 0.411 1.22 (0.79–1.88)
CI, 2.05–5.17), presence of hiatus hernia (OR, 11.67; Low 48/292 (16.4)
95% CI, 6.40–21.26) and alcohol consumption (OR, RO, reflux oesophagitis. Other abbreviations as in the footnote to Table 3.

Table 3 Association between variables, determined by using

3.22; 95% CI, 1.26–8.22) remained as significant inde-
univariate analysis: GORD (n 388) versus non-GORD (n 612) pendent predictive factors.
patients
GORD present, Univariate OR Comparison between NERD and non-GORD patients
Variable n (%) P value (95% CI) The prevalences of various variables in patients with
Age (years) NERD compared to non-GORD patients are shown in
. 65 68/208 (32.7) 0.051 0.72 (0.51–1.00) Table 5. On univariate analysis, Indian and Malay race
<65 320/792 (40.4)
Gender
(vs Chinese), BMI . 25, alcohol consumption and high
Male 176/442 (39.8) 0.60 11.08 (0.83–1.41) and medium education level were found to be signifi-
Female 212/558 (38.0) cant. Age . 65 years was found to be a negative
Race (vs Chinese)
Indian 176/311 (56.6) , 0.001 3.50 (2.56–4.79)
predictive factor. On multivariate analysis, Indian race
Malay 81/206 (39.3) 0.002 1.74 (1.22–2.49) (OR, 3.45; 95% CI, 2.42–4.92), Malay race (OR, 1.80;
Chinese 131/483 (27.1) 95% CI, 1.20–2.69), BMI . 25 (OR, 1.47; 95% CI,
Body mass index
. 25 125/268 (46.6) 0.003 1.56 (1.16–2.09) 1.04–2.06) and high education level (OR, 1.66; 95% CI,
<25 263/732 (35.9) 1.06–2.59) remained as significant independent predic-
Hiatus hernia
Yes 45/67 (67.2) , 0.001 3.52 (2.02–6.17)
tive factors.
No 343/933 (36.8)
Helicobacter pylori Discussion
Yes 81/228 (35.5) 0.281 0.83 (0.61–1.15)
No 307/772 (39.8) Epidemiological data on reflux oesophagitis and GORD
Smoking in Asian patients have been sparse. Previous reports
Yes 63/153 (41.2) 0.572 1.12 (0.78–1.62) have noted a low prevalence of reflux oesophagitis in
No 325/847 (38.4)
Alcohol the Asian population. In 1993 Kang et al. [3] reported a
Yes 19/31 (61.3) 0.015 2.57 (1.17–5.71) prevalence of reflux oesophagitis of 3.3% in a large
No 369/969 (38.1)
Education level (vs low)
retrospective survey of over 10 000 endoscopies. In a
High 78/187 (41.7) 0.078 1.41 (0.96–2.06) prospective survey of 1060 consecutive dyspeptic pa-
Medium 186/445 (41.8) 0.021 1.41 (1.05–1.90) tients, Goh [4] noted a prevalence of only 0.8%.
Low 124/368 (33.7)
Similarly, Chen et al. [10], in large series of patients,
GORD, gastro-oesophageal reflux disease; OR, odds ratio; CI, confidence noted a prevalence of 2.4%, and Chang et al. [11] noted

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 Gastro-oesophageal reflux disease in Asians Rosaida and Goh 499

Table 5 Association between variables, determined by using care and who had agreed to undergo upper gastrointest-
univariate analysis: NERD (n 254) versus non-GORD (n 612) inal endoscopy. They are therefore not reflective of the
patients
prevalence in the community as a whole.
NERD present, Univariate OR
Variable n (%) P value (95% CI)
Surveys concerning the symptoms of GORD are
Age (years) fraught with errors. Many Asian patients do not under-
. 65 38/178 (21.3) 0.011 0.59 (0.39–0.89)
<65 216/688 (31.4)
stand the meaning of the word ‘heartburn’. Spechler et
Gender al. [21] observed that only 13.2% of East Asian patients
Male 99/365 (27.1) 0.253 0.83 (0.61–1.13) in their study correctly understood the term. In our
Female 155/501 (30.9)
Race (vs Chinese) study, we have asked our patients to describe to us
Indian 115/250 (46.0) , 0.001 3.70 (2.58–5.32) what they meant by heartburn and acid regurgitation to
Malay 58/183 (31.7) , 0.001 2.02 (1.33–3.05)
Chinese 81/433 (18.7)
ensure accurate interpretation of the symptom.
Body mass index
. 25 88/231 (38.1) , 0.001 1.74 (1.25–2.42) We have also noted a prevalence rate for hiatus hernia
<25 166/635 (26.1)
Hiatus hernia
of 6.7% and for Barrett’s oesophagus of 2.0%. These
Yes 8/30 (26.7) 0.903 0.87 (0.35–2.09) figures are in keeping with those reported by Yeh et al.
No 246/836 (29.4) [5] but higher than those reported by Chang et al. [11]
Helicobacter pylori
Yes 57/204 (27.9) 0.681 0.92 (0.64–1.31) and in the Asian group of patients in the study by Kang
No 197/662 (29.8) and Ho [15]. In this latter study, hiatus hernia was
Smoking
Yes 42/132 (31.8) 0.563 1.15 (0.76–1.74)
noted in 24% of English patients compared to 5% in a
No 212/734 (28.9) Singapore Asian population. Similarly, Barrett’s oeso-
Alcohol phagus was diagnosed in 6% of the English patients
Yes 10/22 (45.5) 0.148 2.05 (0.81–5.15)
No 244/844 (28.9) compared to none amongst the Asian patients [15].
Education level (vs low) Wong et al. [12] noted that only 0.06% of a large study
High 54/163 (33.1) 0.036 1.59 (1.03–2.46) population had Barrett’s oesophagus and 0.08% had
Medium 124/383 (32.4) 0.015 1.54 (1.08–2.18)
Low 76/320 (23.8) strictures.
NERD, non-erosive reflux disease. Other abbreviations as in the footnote to Table
3. While geographical and demographic differences are
inevitable, we believe that the figures recorded in our
study reflect the situation in the Asian population at
a prevalence of 5.0%. In a recent review of patients present. While reflux oesophagitis may have been truly
who had undergone endoscopy in Hong Kong, a uncommon in the past in Asians, the prevalence of
prevalence rate of 3.8% was recorded [12]. disease has likely increased with time. While there
have been no formal, planned studies looking at time
In our present study we have recorded a comparatively trends, single centre studies on the prevalence of reflux
high prevalence of reflux oesophagitis of 13.4%. This oesophagitis have shown a significant increase. Salem et
is consistent with the figure reported by Yeh et al. al. [6] reported a prevalence of 2.5% in patients who
from Taiwan in 1997 [5]. These figures are, however, had undergone upper gastrointestinal endoscopy in
lower than those for Western patients whose reported 1997/1998. A follow-up study carried out in 2000/2001
prevalence ranges from 20% to 30% [13–16]. In a by Rosaida and Goh [7] revealed an increased overall
comparative study by Kang and Ho [16], between a prevalence of 7.5% (P , 0.001). These two studies
multi-ethnic Asian versus an English group of patients, were performed in the same medical centre on essen-
a prevalence of 4% was recorded for the former tially the same study population.
compared to 25% for the latter.
In the comparative study by Kang and Ho [16], 25% of
Several studies have looked at the prevalence of the English study population had a severe grade of
symptoms of GORD in the Asian setting. These stud- oesophagitis compared to none in the Singapore pa-
ies are population based. Ho et al. [17] reported a figure tients. Chang et al. [11] reported only 6.0% prevalence
of 5.7% in 1998 and 4.6% in another study in 1999 [18]. of grade 3 or 4 oesophagitis using the Savary–Miller
Using a symptom scoring system for GORD, Pan et al. classification. Similarly, Wong et al. [12] also reported a
[19] reported a prevalence of 8.97% for GORD, and 6% prevalence of grade C and D oesophagitis based on
Wong et al. [20], in a telephone survey, recorded a the Los Angeles classification. The proportion of more
prevalence of 8.9% for monthly symptoms of GORD. severe grades of oesophagitis, however, may be increas-
In our study, 25.4% of patients complained of monthly ing. Yeh et al. [5] reported 16.7% of patients having
predominant GORD symptoms. Our figures are much grade 3 or 4 oesophagitis (Savary–Miller classification)
higher as our study population comprised patients with and Maekawa et al. [22] reported severe grades (Los
upper abdominal symptoms, who were seeking health Angeles classification) of oesophagitis C and D in

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 500 European Journal of Gastroenterology & Hepatology 2004, Vol 16 No 5

14.3% of their patients. In our study, 20.1% of patients Furthermore, although the number of patients with
had grade C or D based on the Los Angeles classifica- Barrett’s oesophagus was small in our study, it was
tion. Reflux oesophagitis may, therefore, be increasing interesting to note again that the prevalence of Barrett’s
not just in prevalence but in severity as well. However, oesophagus in Indian patients was significantly higher
the rate of complications appears to be very low compared with both Chinese and Malay patients.
amongst Asian patients.
It appears, therefore, that Indians not only complain of
The reasons for this increase in prevalence and in- more heartburn and acid regurgitation but also develop
creased proportion of severe grades of reflux oesophagi- more structural damage from the disease. Why are
tis in the Asian population are not entirely clear. No Indians more prone to developing GORD? Are there
single factor or sets of factors are obviously putative. true host genetic factors affecting lower oesophageal
The whole Asian region is undergoing dramatic socio- sphincter tone or relaxation or are ethnic differences
economic changes with inevitable changes in diet and surrogate markers of environmental factors such as
eating habits and other ‘modern’ lifestyle changes. food? Malays, on the other hand, complained more
Increased body weight and BMI have often been about reflux symptoms rather than exhibiting objective
quoted as important risk factors. Asians have in the past changes of reflux damage. Different susceptibility to
been thought to be less obese than Caucasians. In our several other upper gastrointestinal diseases has also
study, however, BMI was noted to be an independent been observed between the different major races in
significant risk factor for NERD and GORD, as a Malaysia [4,24–27]. This must reflect, therefore, not
whole, but not for reflux oesophagitis. only differences in environmental factors but also host
genetic factors.
In our study we have found that GORD, reflux
oesophagitis and NERD were most common amongst The prevalence of NERD has shown it to be the
Indians. NERD and GORD overall but not reflux predominant form of GORD [28, 29] in the West. In
oesophagitis were also more common amongst Malays Asian studies, Wu et al. [30] recorded a prevalence of
compared to Chinese. The issue of ethnicity in reflux 46.7%. In our study, 65.5% of our patients were diag-
oesophagitis has been addressed by the novel compara- nosed as having NERD. It was interesting to note that,
tive study by Kang and Ho [16]. In their study, they following logistic regression analysis, apart from ethni-
have clearly shown that being English was a major risk city (i.e., Indian and Malay race), a BMI greater than
factor for reflux oesophagitis. Although not explicitly 25 and a high education level were significant indepen-
reported, we have assumed that their English patients dent risk factors, suggesting an influence of a more
were all Caucasians. Furthermore, the multi-ethnic affluent lifestyle on the causation of reflux symptoms.
Singapore population was not studied separately with Hiatus hernia was not a significant risk factor for
respect to the different races. In another interesting NERD. On the other hand, hiatus hernia was a highly
study by Neumann and Cooper [23], white patients significant risk factor for reflux oesophagitis, indicating
were found to have a significantly increased risk of that an anatomical abnormality would present with
reflux oesophagitis compared to Indian and Afro-Car- damage to the lower oesophagus as a manifestation of
ibbean ‘British’ patients. Similarly, Spechler et al. [21], the disease.
in a review of 2477 patients who had undergone upper
gastrointestinal endoscopy in a large hospital in Boston, Conflict of interest
None declared
USA, reported a 12.3% prevalence rate of ‘GORD
complications’ in white patients compared to 4.8% in Authors’ contributions
West Asian patients (Indians, Pakistanis and Iranians) Dr Rosaida administered the questionnaire, performed the majority of the
and none in East Asian patients (Chinese, Vietnamese, endoscopies, collected and collated the data and helped write the manuscript.
Professor K.L. Goh conceived the idea of the study, helped perform the
Thais, Japanese and Koreans). endoscopies, performed the data analysis and wrote the manuscript.

In our study, we have sought to further identify any

References
ethnic differences in our multiracial Asian study popu- 1 Goh KL, Chang SC, Fock KM, Ke MY, Park HJ, Lam SK. Gastro-
lation. Indian race (vs Chinese) was an independent oesophageal reflux disease in Asia. J Gastroenterol Hepatol 2000;
significant risk factor for GORD overall and for reflux 15:230–238.
2 Kang JY, Yap I, Gwee KA. The pattern of functional and organic disorders
oesophagitis and NERD. Indian patients were exposed in an Asian gastroenterological clinic. J Gastroenterol Hepatol 1994;
to a more than 3-fold increased risk of suffering from 9:124–127.
3 Kang JY, Tay HH, Yap I, Guan R, Lim KP, Math MV. Low frequency of
GORD, reflux oesophagitis and NERD. Malay race (vs endoscopic esophagitis in Asian patients. J Clin Gastroenterol 1993;
Chinese) was also an independent risk factor for NERD 16:70–73.
and GORD but not for reflux oesophagitis. The in- 4 Goh KL. Prevalence of and risk factors for Helicobacter pylori in a
multiracial population undergoing endoscopy. J Gastroenterol Hepatol
creased prevalence in GORD amongst the Malays was 1997; 12:S29–S35.
a result of a high proportion of patients with NERD. 5 Yeh C, Hsu C, Ho A, Sampliner RE, Fass R. Erosive esophagitis and

Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
 Gastro-oesophageal reflux disease in Asians Rosaida and Goh 501

Barrett’s esophagus in Taiwan. A higher frequency than expected. Dig

Dis Sci 1997; 42:702–706.
6 Salem O, Chin SC, Goh KL. Incidence of reflux oesophagitis in Malaysian
patients – a prospective endoscopic survey [Abstract]. J Gastroenterol
Hepatol 2000; 15:A83.
7 Rosaida MS, Goh KL. Racial differences in the prevalence of reflux
oesophagitis in a multi-racial Malaysian population undergoing endoscopy
[Abstract]. Med J Malaysia 2001; 56:42.
8 Armstrong D, Bennett JR, Blum AL, Dent J, De Dombal FT, Galmiche JP,
et al. The endoscopic assessment of oesophagitis: a progress report on
observer agreement. Gastroenterology 1996; 111:85–92.
9 Goh KL, Parasakthi N, Peh SC, Puthucheary SD, Wong NW. The rapid
urease test in the diagnosis of Helicobacter pylori infection. Singapore
Med J 1994; 35:161–162.
10 Chen PC, Wu CS, Chang-Chien SC, Liaw YF. Comparison of Olympus
GIF-P2 and GIF-K panendoscopy. Taiwan I Hsueh Hui Tsa Chih
(Formosan Med Assoc) 1979; 78:136–140.
11 Chang C, Poon S, Lien H, Chen G. The incidence of reflux esophagitis
among the Chinese. Am J Gastroenterol 1997; 92:668–671.
12 Wong WM, Lam SK, Hui WM, Lai KC, Chan CK, Hu WHC, et al. Long-
term prospective follow-up of endoscopic oesophagitis in southern
Chinese – prevalence and spectrum of the disease. Aliment Pharmacol
Ther 2002; 16:1–6.
13 Avidan B, Sonnenberg A, Schnell TG, Sontag SJ. Risk factors for erosive
reflux esophagitis: a case control study. Am J Gastroenterol 2001;
96:41–46.
14 Hollenz M, Stolte M, Labenz J. Prevalence of gastro-oesophageal reflux
disease in general practice. Dtsch Med Wochenschr 2002; 127:
1007–1012.
15 Mansi C, Savarino V, Mela GS, Picciotto A, Mele MR, Celle G. Are
clinical patterns of dyspepsia a valid guideline for appropriate use of
endoscopy? A report of 2253 dyspeptic patients. Am J Gastroenterol
1993; 88:1011–1015.
16 Kang JY, Ho KY. Different prevalence of reflux esophagitis and hiatus
hernia among dyspeptic patients in England and Singapore. Eur J
Gastroenterol Hepatol 1999; 11:845–850.
17 Ho KY, Kang JY, Seow A. Prevalence of gastrointestinal symptoms in a
multiracial Asian population with particular reference to reflux-type symp-
toms. Am J Gastroenterol 1998; 93:1816–1822.
18 Ho KY, Kang JY, Seow A. Patterns of consultation and treatment for
heartburn: findings from a Singapore community survey. Aliment Pharma-
col Ther 1999; 11:1029–1033.
19 Pan GZ, Xu GM, Ke MY, Han SM, Guo HP, Li ZS, et al. Epidemiological
study of symptomatic gastro esophageal reflux disease in China: Beijing
and Shanghai. Ch J Dig Dis 2000; 1:2–8.
20 Wong WM, Lai KC, Lam KF, Hui WM, Hu WHC, Lam CLK, et al.
Prevalence, clinical spectrum and health care utilization of gastro-
oesophageal reflux disease in a Chinese population: a population-based
study. Aliment Pharmacol Ther 2003; 18:595–604.
21 Spechler SJ, Jain SK, Tendler DA, Parker RA. Racial differences in the
frequency of symptoms and complications of gastro-oesophageal relfux
disease. Aliment Pharmacol Ther 2002; 16:1795–1800.
22 Maekawa T, Kinoshita Y, Okada A, Fukui H, Waki S, Hassan S, et al.
Relationship between severity and symptoms of reflux oesophagitis in
elderly patients in Japan. J Gastroenterol Hepatol 1998; 13:927–930.
23 Neumann CS, Cooper BT. Ethnic differences in gastro-oesophageal reflux
disease. Eur J Gastroenterol Hepatol 1999; 11:735–739.
24 Ranjeev P, Goh KL. Racial differences in the incidence of carcinoma of
the esophagus in Malaysia [Abstract]. Med J Malaysia 1999; 54
(suppl B):10.
25 Ranjeev P, Rosmawati M, Tan YM, Goh KL. Racial differences in the
prevalence of hepatoma in a multiracial South East Asian population.
[Abstract]. J Gastroenterol Hepatol 1999; 14:S93.
26 Rosaida MS, Goh KL. Racial differences in the prevalence of gastric and
duodenal ulcers in a multi-racial Malaysian population undergoing endo-
scopy [Abstract]. Med J Malaysia 2000; 55 (suppl B):17.
27 Goh KL, Cheah PL, Noorfaridah M, Parasakthi N. Ethnic differences in
gastric cancer in a multiracial Asian population: a case–control study.
Gastroenterology 2003; 124:A168.
28 Jones RH, Hungin APS, Phillips J, Mills JG. Gastroesophageal reflux
disease in primary care in Europe: clinical presentation and endoscopic
findings. Eur J Gen Pract 1995; 1:149–154.
29 Fass R, Fennerty B, Vakil N. Non-erosive reflux disease – current
concepts and dilemmas. Am J Gastroenterol 2001; 96:303–314.
30 Wu JCY, Chan FKL, Ching JYL, Leung WK, Lee YT, Sung JJY. Empirical
treatment based on ‘typical’ reflux symptoms is inappropriate in a popu-
lation with a high prevalence of Helicobacter pylori infection. Gastrointest
Endosc 2002; 4:461–465.

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