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A Questionnaire-Based Survey on Screening for Gastric and Colorectal Cancer by Physicians in East Asian Countries in 2010

Molecular Gastroenterology and Hepatology, Kyoto Prefectural University of Medicine, Kyoto, Japan.
Digestion (Impact Factor: 2.1). 07/2012; 86(2):94-106. DOI: 10.1159/000339342
Source: PubMed

ABSTRACT

Background: The incidence of gastric cancer (GC) is high, and colorectal cancer (CRC) has significantly increased in Asian countries. Aim: To examine the current screening for GC and CRC within East Asia by means of a questionnaire survey. Methods: Representative members of the Committee of the International Gastrointestinal Consensus Symposium provided a questionnaire to physicians in six East Asian countries. Results: A total of 449 physicians participated in this survey. In all countries, more than 70% of physicians started GC screening between 40 and 59 years. The most popular method to screen for GC was endoscopy (92.7%), but combination methods such as Helicobacter pylori (HP) antibody, barium X-ray, and tumor marker with endoscopy differed by country. For HP-positive individuals, most physicians screened every year by endoscopy, and for individuals post-HP eradication, about half of physicians (56.3%) thought there was a need to follow-up with GC screening. Among all physicians, the most common age to start CRC screening was in the 40s (39.8%) and 50s (40.9%). Based on the American Cancer Society Recommendations, a fecal occult blood test every year was the most popular method for CRC screening overall. However, among each country, this test was most popular in only Japan (76.9%) and Indonesia. In other countries, sigmoidoscopy every 5 years and total colonoscopy every 10 years were the most popular methods. Conclusion: There are similarities and differences in the screening of GC and CRC among East Asian countries.

Full-text (PDF)

Available from: Yuji Naito
Fax +41 61 306 12 34
E-Mail karger@karger.ch
www.karger.com
Original Paper
Digestion 2012;86:94106
DOI: 10.1159/000339342
A Questionnaire-Based Survey on Screening for
Gastric and Colorectal Cancer by Physicians in East
Asian Countries in 2010
Yuji Naito
a
Kazuhiko Uchiyama
a
Yoshikazu Kinoshita
b
Shin Fukudo
c
Takashi Joh
d
Hidekazu Suzuki
e
Shin’ichi Takahashi
f
Fumiaki Ueno
g
Yasuhiro Fujiwara
h
Tetsuo Arakawa
h
Takayuki Matsumoto
i
Ki-Baik Hahm
j
Udom Kachintorn
k
Ari Fahrial Syam
l
Abdul Aziz Rani
m
Jose D. Sollano
n
Qi Zhu
o
a
Molecular Gastroenterology and Hepatology, Kyoto Prefectural University of Medicine, Kyoto ,
b
Department of
Gastroenterology and Hepatology, Shimane University School of Medicine, Izumo ,
c
Tohoku University School of
Medicine, Sendai ,
d
Department of Gastroenterology and Metabolism, Nagoya City University Graduate School of
Medical Sciences, Nagoya ,
e
Division of Gastroenterology, Department of Internal Medicine, Keio University
School of Medicine, Tokyo ,
f
Department of Gastroenterology, School of Medicine, Kyorin University, Kyorin ,
g
Ofuna Chuo Hospital, Kamakura ,
h
Department of Gastroenterology, Osaka City University Graduate School of
Medicine, Osaka , and
i
Division of Lower Gastroenterology, Department of Internal Medicine, Hyogo College of Medicine,
Nishinomiya , Japan;
j
Gachon University of Medicine and Science, Lee Gil Ya Cancer and Diabetes Institution,
Incheon , Korea;
k
Division of Gastroenterology, Department of Internal Medicine, Faculty of Medicine, Siriraj Hospital
Mahidol University, Bangkok , Thailand;
l
Division of Gastroenterology, Department of Internal
Medicine, Faculty of
Medicine, University of Indonesia, Dr. Cipto Mangunkusumo Hospital, and
m
Department of Internal
Medicine, Faculty of
Medicine, University of Indonesia Cipto Mangunkusumo Hospital, Jakarta , Indonesia;
n
University of Santo Tomas,
Manila , Philippines;
o
Rui Jing Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai , China
but combination methods such as Helicobacter pylori (HP)
antibody, barium X-ray, and tumor marker with endoscopy
differed by country. For HP-positive individuals, most physi-
cians screened every year by endoscopy, and for individuals
post-HP eradication, about half of physicians (56.3%) thought
there was a need to follow-up with GC screening. Among all
physicians, the most common age to start CRC screening
was in the 40s (39.8%) and 50s (40.9%). Based on the Ameri-
can Cancer Society Recommendations, a fecal occult blood
test every year was the most popular method for CRC screen-
ing overall. However, among each country, this test was most
popular in only Japan (76.9%) and Indonesia. In other coun-
tries, sigmoidoscopy every 5 years and total colonoscopy ev-
ery 10 years were the most popular methods. Conclusion:
There are similarities and differences in the screening of GC
and CRC among East Asian countries.
Copyright © 2012 S. Karger AG, Basel
Key Words
Colorectal cancer Gastric cancer Screening East Asian
countries Questionnaire-based survey
Abstract
Background: The incidence of gastric cancer (GC) is high,
and colorectal cancer (CRC) has significantly increased in
Asian countries. Aim: To examine the current screening for
GC and CRC within East Asia by means of a questionnaire
survey. Methods: Representative members of the Commit-
tee of the International Gastrointestinal Consensus Sympo-
sium provided a questionnaire to physicians in six East Asian
countries. Results: A total of 449 physicians participated in
this survey. In all countries, more than 70% of physicians
started GC screening between 40 and 59 years. The most
popular method to screen for GC was endoscopy (92.7%),
Received: February 3, 2012
Accepted: May 8, 2012
Published online: July 27, 2012
Yuji Naito
Molecular Gastroenterology and Hepatology
Kyoto Prefectural University of Medicine
465 Kajiicho Hirokoji Kawaramachi, Kamigyo-ku, Kyoto 602-8566 (Japan)
Tel. +81 75 251 5519, E-Mail ynaito
@ koto.kpu-m.ac.jp
© 2012 S. Karger AG, Basel
0012–2823/12/0862–0094$38.00/0
Accessible online at:
www.karger.com/dig
Page 1
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in East Asian Countries
Digestion 2012;86:94–106
95
Introduction
Gastric cancer (GC) is the fourth most common can-
cer in the world and the second leading cause of cancer-
related death
[1, 2] . Asian countries, including China, Ja-
pan, and Korea, show the highest incidence of GC in the
world
[1] . Since 1960, mass screening for GC using pho-
tof luorography has been done in Japan, and sur vival rates
have significantly improved due to early detection of can-
cer
[3] . Recently, other opportunistic screening methods
such as endoscopy, serum pepsinogen testing, and Heli-
cobacter pylori (HP) antibody testing have been used for
GC screening. However, the efficacy of these methods is
not clear. In addition, as new endoscopic techniques such
as chromoendoscopy, narrow band imaging, confocal en-
doscopy, and autofluorescence have been developed, fur-
ther studies on GC screening are needed.
Colorectal cancer (CRC) is one of the most common
cancers worldwide, accounting for more than 1 million
new cancer cases annually and approximately half a mil-
lion deaths each year. The incidence of CRC in Asia is
increasing
[4] . Although various screening examinations,
such as fecal occult blood testing, sigmoidoscopy, and
colonoscopy can be used, little is known about how or
when physicians recommend screening and whether pa-
tients follow different recommendations. Although Asia-
Pacific consensus recommendations for CRC screening
have been published
[4] , guidelines and recommenda-
tions for the screening and prevention of CRC in Asia
have not been established. Screening and surveillance of
CRC is effective for diagnosing early stages of CRC
[5] ,
but compliance rates are low in many countries world-
wide
[6–10] .
In this survey, we intended to define the current situ-
ation concerning screening strategies for GC and CRC in
East Asian countries.
Subjects and Methods
Subjects
Gastroenterologists, gastroenterological surgeons, and gener-
al physicians in China, Indonesia, Japan, Korea, Philippines, and
Thailand were asked to fill in a questionnaire about screening for
GC and CRC. All subjects work in an urban environment.
M e t h o d s
A representative person from each country was selected from
the Committee of the International Gastrointestinal Consensus
Symposium, which is the international part of the Japanese Gas-
troenterological Association. The representative members pro-
vided a questionnaire to physicians in each country, starting at
the beginning of July 2010 and collected responses until the end
of December 2010. The questionnaire asked the following ques-
tions about GC and CRC: (1) GC: age of starting screening ex-
aminations, the most common age when screening examinations
are done, and the preferred screening examination. In addition,
physicians were asked about the management of HP infection in
terms of the follow-up period for patient who did and did not un-
dergo HP eradication. (2) CRC: age of starting screening exami-
nations, the most common age when screening examinations are
done, and the preferred examination for screening. The question-
naire for CRC screening criteria was based on American Cancer
Society Recommendations
[11] ( table1 ). Details of the question-
naire are shown in the Appendix.
R e s u l t s
Characteristics of Respondents
A total of 449 physicians were enrolled in this survey.
Among all countries, the number of physicians partici-
pating in this survey was largest in Japan and smallest in
the Philippines ( table2 ).
GC: Age of Starting Screening Examinations
Among all physicians, the most common age to start
GC screening was in the 40s (54.7% of physicians; fig.1 a).
Table 1. CRC screening criteria by American Cancer Society re-
commendation
1 Fecal occult blood test every year
2 Fecal DNA test every year
3 Sigmoidoscopy every 5 years
4 Total colonoscopy every 10 years
5 Barium enema every 5 years
6 CT colonography every 5 years
Table 2. Number of physicians who participated in the survey by
speciality
Gastro-
enterologists
Gastro-
enterological
surgeons
General
physicians
Total
China 26 12 0 38
Indonesia 34 0 10 44
Japan 216 11 21 248
Korea 44 0 7 51
Philippines 21 0 7 28
Thailand 18 14 8 40
Total 359 37 53 449
Page 2
Naito et al.
Digestion 2012;86:94–106
96
Among the countries surveyed, Korea had the largest ra-
tio of physicians who started GC screening in the 40s
( fig.1 b). In terms of physician type, 56% of gastroenter-
ologists start GC screening in the 40s; 46 and 44% of gas-
troenterological surgeons start in the 40s and 50s, respec-
tively, and 55% of general physicians start in the 40s
( fig.1 c).
GC: Preferred Screening Examination
The most common screening method for GC was en-
doscopy both among all physicians (92.7%) and in each
country (China, 100%; Indonesia, 100%; Japan, 89.8%;
Korea, 100%; Philippines, 95.2%; Thailand, 83.3%). There
were no differences among gastroenterologists, gastroen-
terological surgeons, and general physicians in terms of
the preference for endoscopy as the best GC screening
method (92.7, 92.9, and 92.0%, respectively). However,
there were several different suggestions about combina-
tion screening methods ( fig.2 a). Though endoscopy was
included in most combination methods, HP antibody,
barium X-ray, and tumor marker surveys were also pop-
ular as part of combination screening methods for GC
( fig. 2 b).
Screening Methods for HP-Positive Patients
Data on the duration of follow-up and the methods of
screening HP-positive patients were provided by 359 gas-
troenterologists. Results showed that 65% of gastroenter-
ologists follow up every year ( fig.3 a) and 77% of them use
endoscopy ( fig.3 b).
Gastroenterologists
Gastroenterological
surgeons
General physicians
a
0
20
40
60
80
100
30–39 40–49 50–59 60–69 70–79 ≥80
%
Age (years)
Age (years)
Age (years)
Age (years)
Age (years)
Age (years)
Age (years)
Age (years)
0
20
40
60
80
100
30–39 40–49 50–59 ≥60
c
%
0
20
40
60
80
100
30–39 40–49 50–59 60–69 70–79 ≥80
China
%
Korea
b
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 70–79 ≥80
Philippines
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 70–79 ≥80
Thailand
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 70–79 ≥80
Indonesia
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 70–79 ≥80
Japan
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 70–79 ≥80
Fig. 1. Starting age of GC screening. a Among all physicians. b Screening by country. c Differences among gas-
troenterologists, gastroenterological surgeons, and general physicians for starting age of GC screening.
Page 3
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in East Asian Countries
Digestion 2012;86:94–106
97
0
20
40
60
80
100
123456
a
%
%
%
%
%
%
%
China
0
20
40
60
80
100
123456
Indonesia
0
20
40
60
80
100
123456
Japan
0
20
40
60
80
100
123456
Korea
0
20
40
60
80
100
123456
Philippines
0
20
40
60
80
100
123456
Thailand
0
20
40
60
80
100
123456
1. Endoscopy + HP antibody
2. Endoscopy + barium X-ray
3. Endoscopy + tumor marker
4. Endoscopy + serum pepsinogen
5. Serum pepsinogen + HP antibody
6. Others
b
Fig. 2. Combination of GC screening methods used by all physicians ( a ) and by country ( b ).
0
20
40
60
80
100
Every
year
Every 2
years
Every 3
years
Every 5
years
Unclear
%
a
b
77.1%
1.1%
21.7%
Endoscopy
Barium X-ray
Unclear
Fig. 3. a Interval to follow-up of HP-positive patients among gastroenterologists. b Methods used by gastroenterologist to follow up
HP-positive patients.
Page 4
Naito et al.
Digestion 2012;86:94–106
98
Screening after HP Eradication
Among the 359 gastroenterologists who provided data
on HP eradication, 202 (56.3%) thought that follow-up
GC screening after HP eradication was necessary ( fig.4 a).
Among these 202 gastroenterologists, more than 60%
perform GC screening every year ( fig.4 b). The duration
of follow-up varied ( fig.4 c). Whole-life follow-up was the
most popular response (22.9%) regarding the follow-up
period; however, 42.5% answered ‘unclear’.
CRC: Age of Starting Screening Examinations
Among all physicians, the most common ages to start
CRC screening were in the 40s (39.8%) and 50s (40.9%),
and more than 90% of physicians start CRC screening
before 60 years ( fig.5 a). Among the countries surveyed,
Japan tended to start earlier compared with other coun-
tries ( fig.5 b). There were no significant differences be-
tween gastroenterologists and gastroenterological sur-
geons in terms of starting age of screening ( fig.5 c).
CRC: Preferred Screening Examination among
Gastroenterologists
Among all gastroenterologists, fecal occult blood test
every year was the most popular method (52.5%) for CRC
screening ( fig.6 a). However, this result was largely driven
by responses of Japanese gastroenterologists, who repre-
sented the largest number of gastroenterologists (n = 216).
Sigmoidoscopy every 5 years and total colonoscopy every
10 years were common responses from gastroenterolo-
gists in other countries ( fig.6 b).
Discussion
Although a decline in the number of GC patients has
been observed in Japan, China, and Korea, GC still rep-
resents a tremendous burden in each country. According
to GLOBOCAN 2008, GC is the third most frequently
diagnosed cancer and the second leading cause of cancer
deaths in Japan, with an estimated 102,040 new cases and
50,156 cancer deaths in 2008. The overall estimated age-
adjusted incidence rate in 2008 was 31.1 per 100,000 peo-
ple
[12] . In China, there is no systematic national vital
statistics, but a retrospective sampling survey from 2004
to 2005 found that the mortality rate from GC ranked
third in overall cancer mortality
[13] . GC is the second
most frequently diagnosed cancer in China and the third
leading cause of cancer death, with an estimated 464,439
new cases and 352,315 cancer deaths in 2008. The overall
estimated age-adjusted incidence rate in 2008 was 29.9
a
Need to
follow up
No need to
follow up
Unclear
56.3%
17.6%
26.1%
0
20
40
60
80
100
%
Every year Every 2
years
Every 3
years
Unclear
b
0
20
40
60
80
100
1–4 years 5–9 years ≥10 years Whole life Unclear
%
c
Fig. 4. a Need to follow up after HP eradication among gastroen-
terologists.
b Interval of follow-up examinations for patients post-
HP eradication among gastroenterologists.
c Length of follow-up
period of patients post-HP eradication among gastroenterolo-
gists.
Page 5
Gastrointestinal Tract Cancer Screening
in East Asian Countries
Digestion 2012;86:94–106
99
per 100,000 people. In Korea, GC mortality has been con-
sistently decreasing; however, it is still a clinically impor-
tant disease due to its high incidence and mortality
[14] .
In 2008, an estimated 28,078 new cases were diagnosed,
accounting for 15.7% of new cancer cases. The incidence
of disease was 43.8 per 100,000 in 2008. In Thailand, the
estimated age-standardized incidence rate in 2002 of GC
shows some variation with higher rates in Bangkok,
which were 4.9 per 100,000 for males and 3.7 per 100,000
for females
[15] . The estimated age-standardized inci-
dence rate in 2007 of stomach cancer in the Philippines
was 7.9 per 100,000 for males and 5.4 per 100,000 for fe-
males
[16] . The incidence of GC in Indonesia is exceed-
ingly rare and it has been reported to relate with the rela-
tive lack of infection with HP
[17] . These statistical data
include that although the number of GC patients is de-
creasing in Asian countries, it is still the second most
common cause of death worldwide
[1, 18] as well as in
many Asian countries, such as China, Japan, and Korea.
However, a screening program for GC has not been estab-
lished in Asian countries.
According to the Asia-Pacific Working Group on GC,
the optimum age for initiation of screening should be 40–
45 years
[19] . In particular, in high-risk regions, such as
Gastroenterologists
Gastroenterological
surgeons
General physicians
0
20
40
60
80
100
30–39 40–49 50–59 60–69 ≥70
China
%
0
20
40
60
80
100
Korea
%
30–39 40–49 50–59 60–69 ≥70
Philippines
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 ≥70
Thailand
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 ≥70
Indonesia
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 ≥70
Japan
0
20
40
60
80
100
%
30–39 40–49 50–59 60–69 ≥70
0
20
40
60
80
100
30–39 40–49 50–59 60–69 ≥70
%
0
20
40
60
80
100
%
30–39 40–49 50–59 ≥60
a
b
Age (years)
Age (years)
Age (years)
Age (years) Age (years)
Age (years) Age (years) Age (years)
c
Fig. 5. Starting age of CRC screening. a Starting age of CRC screening among all physicians. b Starting age of CRC screening by coun-
try.
c Differences among gastroenterologists, gastroenterological surgeons, and general physicians for starting age of CRC screening.
Page 6
Naito et al.
Digestion 2012;86:94–106
100
Japan and Korea, the working group recommends screen-
ing all individuals older than 40 years. In this survey,
most physicians agreed about starting GC screening at 40
years.
Endoscopy was the most popular screening method
for GC among physicians in this survey. In general, en-
doscopy is increasingly used for GC screening because of
a high detection rate of superficial flat and non-ulcerative
lesions that conventional barium examination cannot de-
tect
[20] . However, the sensitivity of GC detection by en-
doscopy compared with that of barium X-ray (photof luo-
rography) is not clear. Although endoscopic screening is
expected to be an alternative strategy to photofluorog-
raphy, no studies have evaluated whether endoscopic
screening reduces GC mortality. As new endoscopic tech-
niques such as chromoendoscopy, narrow band imaging,
confocal endoscopy, and autofluorescence are developed,
the sensitivity and detection of GC are expected to in-
crease. Although most physicians in this survey recom-
mend endoscopy, further study is necessary to evaluate
the efficacy of endoscopy for GC screening using up-to-
date screening tools.
Photofluorography has been used for GC screening in
Japan since 1960
[21] . Though there is no randomized,
controlled study of GC screening using photofluorogra-
phy, several case-control and cohort studies dealing with
photofluorography have been published
[3, 2226] . These
studies indicate that GC screening with photofluorogra-
phy resulted in a reduction in mortality from GC. How-
ever, data from prospective studies that define death from
1. Fecal occult blood test every year
2. Fecal DNA test every year
3. Sigmoidoscopy every 5 years
4. Total colonoscopy every 10 years
5. Barium enema every 5 years
6. CT colonography every 5 years
7. Others
8. Unclear
0
20
40
60
80
100
12345678
China
%
12345678
Philippines
0
20
40
60
80
100
%
12345678
Thailand
0
20
40
60
80
100
%
12345678
Indonesia
0
20
40
60
80
100
%
12345678
Japan
0
20
40
60
80
100
%
12345678
Korea
0
20
40
60
80
100
%
b
a
%
0
20
40
60
80
100
12345678
Fig. 6. Methods for CRC screening by all physicians ( a ) and by country ( b ) .
Page 7
Gastrointestinal Tract Cancer Screening
in East Asian Countries
Digestion 2012;86:94–106
101
GC as an endpoint are inconsistent. In the current survey,
photofluorography was the second most common meth-
od used in combination with endoscopy to screen for GC.
Use of this method was higher in Japan compared with
other countries (data not shown).
Measurement of serum pepsinogen (PG) levels is a
popular serological screening test for GC, particularly in
Japan. There are two types of serum PG – PGI and PGII.
PGII remains constant, but PGI concentrations decrease
with loss of fundic gland mucosa. Therefore, a low PGI
concentration or a low PGI/II ratio indicates atrophic
gastritis, which represents a preneoplastic gastric lesion.
A PGI/II ratio of 1 3.0 has a sensitivity of 93% and a spec-
ificity of 88% for diagnosis of a normal fundic gland in
Japanese patients
[27] . In a Japanese study, subjects with
atrophic gastritis diagnosed by pepsinogen concentra-
tions had a significantly higher risk of developing GC
than those with normal pepsinogen concentrations who
were negative for the HP antibody
[28] . However, the se-
rum pepsinogen test detects the presence of atrophic gas-
tritis and is therefore more applicable to detect intestinal
cancer only. In this survey, the serum pepsinogen test was
used in combination with other methods by a small num-
ber of physicians.
HP is a well-known carcinogen for GC, and the Asia-
Pacific H. pylori Consensus Group concluded that eradi-
cation of HP is a good strategy in selected societies where
the risk of GC is high
[29] . There is one randomized con-
trolled study from China that showed that eradication of
HP reduced the incidence of GC
[30] . In that cohort, in-
dividuals who had not developed gastric mucosal atrophy
and intestinal metaplasia had a lower incidence of GC af-
ter HP eradication, but those who already had gastric mu-
cosal atrophy and intestinal metaplasia showed no such
difference after HP eradication. There is no randomized
controlled study concerning the duration of follow-up
among HP-positive individuals. It has been reported that
the doubling time of early GC is approximately 16.6
months
[31] . Based on that study, results of the current
survey showing that most physicians insist on annual GC
screening in HP-positive individuals seem appropriate.
In terms of follow-up after HP eradication, GC has been
seen to develop in some patients even after HP eradica-
tion
[3234] . From these studies, the rate of GC develop-
ment is about 0.3% per year as long as 10 years after HP
eradication. Based on these results, it has been suggested
that follow-up GC screening for patients who have been
treated for HP infection should be continued for more
than 10 years
[33] . However, in this survey, 17.6% of gas-
troenterologists indicated they thought there was no need
for follow-up of patients after HP eradication. Though
there does not appear to be a consensus regarding follow-
up after HP eradication, it seems prudent to continue GC
screening even after HP eradication for at least several
years. Further studies are needed to clarify the length of
follow-up required.
The usefulness of screening for the GC risk method
using a combined assay for serum anti-HP IgG antibody
and serum PG levels, called the ‘ABC method’, has been
reported. Subjects are classified into one of four risk
groups based on the results of two serologic tests: group
A (HP() PG(): infection-free subjects), group B (HP(+)
PG(): chronic atrophic gastritis-free or mild), group C
(HP(+) PG(+): chronic atrophic gastritis), and group D
(HP() PG(+): severe chronic atrophic gastritis with ex-
tensive intestinal metaplasia). The ABC method allows
stratification of risk for development of GC, as chronic
gastritis progressed, a gradual and significant increase in
the incidence of GC and hazard ratio was noted
[28, 35
38]
.
The Asia-Pacific Working Group on CRC has report-
ed that CRC is one of the most common cancers in Asia
in both males and females, and that the incidence of CRC
in Asian Pacific countries is similar to that of Western
countries. Although the death rate of CRC is declining
in Western countries, mortality associated with CRC is
rising in Asian countries
[4] . According to the database
of GLOBOCAN
[39] , the incidence of CRC for males is
especially high in Japan and Korea, that is 41.7 and 46.9
per 100,000. In China, the Philippines, Indonesia, and
Thailand, the incidence of CRC for males shows almost
same numbers, that is 16.3, 10.0, 19.1, and 13.2 per
100,000. For females, the tendency of CRC incidence
shows the same as males, that is high group as Japan and
Korea, 22.8 and 25.6 per 100,000, and low group as Chi-
na, the Philippines, Indonesia, and Thailand, 12.2, 7.3,
15.6, 13.4 per 100,000. Screening and surveillance for
CRC is useful for early disease detection
[5] , but compli-
ance with screening recommendations is low in many
countries
[6–10] .
Based on the recommendations of Asia-Pacific Con-
sensus Group, CRC screening should be started at the age
of 50 years
[4] . Most national guidelines also recommend
starting CRC screening at this age because the risk of
CRC begins to increase at age 50
[40, 41] . In Asian coun-
tries, the risk of finding advanced CRC significantly in-
creases by 1 to 1 3% at the age of 50 years compared with
younger subjects
[4245] . This survey showed that most
physicians, except those in Japan, start screening for CRC
at 50 years. Japanese physicians tend to start screening
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Naito et al.
Digestion 2012;86:94–106
102
for CRC earlier. Overall, all physicians in this survey
started screening for CRC between 40 and 50 years.
Fecal occult blood tests (FOBTs) are based on the fun-
damentals of detecting blood in stool that may originate
from a bleeding CRC or large adenoma. Because of their
ease of use, FOBTs have been used to screen for CRC
worldwide. However, FOBTs cannot detect precursor le-
sions. In addition, because CRCs usually bleed intermit-
tently, repeat testing may be required to detect CRC. Two
primary FOBTs are available: guiac-FOBT and immuno-
chemical FOBT (iFOBT). Though dietary intake of red
meat leads to false-positive findings and vitamin C intake
to false-negative findings in guiac-FOBT, iFOBT is spe-
cific for human hemoglobin. The sensitivity of iFOBT in
detecting CRC is 66–82% and the specificity is 95–97%
[46, 47] . Previous reports showed that FOBT screening
reduced mortality resulting from CRC
[4853] , and sev-
eral countries emphasize this procedure for general pop-
ulation screening. With the use of FOBT, the number of
patients with stage I or II disease has significantly in-
creased, while the number of patients with stage IV dis-
eases has decreased
[53] . In this survey, physicians from
Japan and Indonesia tended to choose FOBT for CRC
screening. However, there is no evidence from random-
ized, controlled trials that CRC-related mortality is re-
duced over a 10-year period of iFOBT screening. One
large study included 94,000 persons who were random-
ized to one round of iFOBT or no screening. Colon cancer
mortality did not differ significantly between groups
over an 8-year follow-up period: CRC mortality was 90
per 100,000 in the screening group versus 83 per 100,000
in the control group
[54] . Based on this study, which
shows no benefit of iFOBT on mortality, physicians in
Japan and Indonesia may want to consider other methods
of CRC screening.
Flexible sigmoidoscopy is an endoscopic procedure
that shows up to 40–60 cm distal of the colon. When an
adenoma of any size is detected, a full colonoscopy is rec-
ommended, because the risk of advanced adenomas or
cancer in the proximal colon is increased
[55] . The prob-
lem with flexible sigmoidoscopy is that the quality of the
examination is not always as good as it should be, as the
insertion depth is sometimes difficult to determine. In
addition, sigmoidoscopy should be performed by trained
endoscopists with acceptable adenoma detection rates
[56] . In one study, sigmoidoscopy had a higher detection
rate for advanced adenomas and cancer compared with
FOBT
[57] . In addition, individuals without adenomas in
the distal colon, as shown by sigmoidoscopy, frequently
do not receive a follow-up colonoscopy. The percentage of
asymptomatic individuals with isolated advanced proxi-
mal adenomas or cancer who undergo a colonoscopy is
1.35%
[58, 59] . Atkin et al. [60] reported that sigmoidos-
copy screening reduces the mortality from CRC. They
compared a control group (113,195 persons) and an inter-
vention group (57,237 persons) and showed that advanced
adenomas or cancer were detected in 5% of subjects in the
intervention group. In their study, sigmoidoscopy led to
a 23% reduction of CRC incidence and 31% reduction
in CRC-related mortality
[60] . However, other studies
showed a higher percentage of missing transverse and
right-sided lesions (24%
[61] , 20% [62] ) even when sig-
moidoscopy was combined with FOBT. In this survey,
only China reported a higher rate of sigmoidoscopy for
screening for CRC compared with other screening meth-
ods. Sigmoidoscopy might be better than FOBT for CRC
screening, but results from ongoing large, randomized,
controlled trials
[63, 64] are needed to confirm any ad-
vantages of this procedure.
Colonoscopy allows observation of the entire colon
and is considered the gold standard for detection of
colorectal neoplasia. However, polyps can still be missed
when using colonoscopy to screen for CRC. The miss rate
of adenomas, as reported in tandem colonoscopy studies,
is 2026% for any adenoma and 2.1% for large adenomas
( 1 10 mm)
[65] . These detection rates are reported to de-
pend on the quality of the procedure, including the tech-
nique of the colonoscopist and several other factors such
as optimal bowel preparation, sufficient withdrawal time,
and complete examination of the colon
[66–70] . The par-
ticipation rates of patients in colonoscopy screening are
lower compared with FOBT and sigmoidoscopy because
of its invasive and burdensome nature. However, most
patients only need to undergo a colonoscopy once every
10 years after a negative colonoscopy because the risk of
developing CRC after a negative colonoscopy remains
low for more than 10 years
[71, 72] . In this survey, physi-
cians in Korea, the Philippines, and Thailand recom-
mended a colonoscopy every 10 years for CRC screening,
and this procedure was the second most popular CRC
screening method overall. Several ongoing studies are
evaluating the role of colonoscopy screening on CRC-re-
lated incidence and mortality. The Nordic-European Ini-
tiative on CRC (NordIGG) trial includes 66,000 individ-
uals randomized to either colonoscopy screening or no
screening. A 15-year follow-up is planned, and the results
are expected in 2026. In a Spanish trial, CRC-related
mortality is being compared between patients who un-
dergo biannual FOBT and colonoscopy; results are ex-
pected in 2021.
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Gastrointestinal Tract Cancer Screening
in East Asian Countries
Digestion 2012;86:94–106
103
The use of DNA markers in stool (sDNA) for CRC
screening is a relatively new method. Because no single
gene mutation is present in all adenomas or cancer cells,
a multipanel of DNA markers is needed. The point muta-
tions on APC, KRAS, and P53 genes plus long DNA (Pre-
Gen-Plus
[73] ) are being tested in two large average-risk
cohorts
[74] . Methylated vimentin, mutant KRAS, and
mutant APC (SDT-2) are being tested in a smaller study
[75] . Several studies on the efficacy of CRC screening by
PreGen-Plus have been done, with one study showing a
sensitivity of 52% and a specificity of 94%
[74] , and an-
other study showing a sensitivity of 20% and a specificity
of 96%
[75] . The low sensitivity of this method was based
on the kinds of panel DNA markers that identify most but
not all CRCs. There are no data based on a randomized
controlled study regarding the efficacy of sDNA for CRC
screening, and it is not known which patients would be
better off undergoing CRC screening by sDNA than by
FOBT. In this survey, physicians from China recom-
mended fecal DNA test as a second-line method for CRC
screening. However, overall, fecal DNA tests were a mi-
nor screening method in this survey. Further studies are
needed to confirm if fecal DNA tests are effective for
screening for CRC compared with other methods.
With the development of new instruments and tests,
the diagnostic and therapeutic approach to GC and CRC
is continuously changing. In this survey, we conducted an
attitude survey of Asian physicians, including gastroen-
terologists, regarding screening for GC and CRC. Some
countries should likely change their screening approach-
es based on recent results of reliable controlled surveys
that show decreases in the mortality GC and CRC with
specific screening methods. However, the social situation
in each country, including insurance systems, is different.
Thus establishment of strong evidence for cancer surveil-
lance using up-to-date methods that have been proven
effective in well-controlled studies is imperative.
Acknowledgement
This study was sponsored by the IGICS, a keynote program of
the Japanese Gastroenterological Association. We thank all phy-
sicians for their contributions in providing questionnaires and
collecting responses.
Disclosure Statement
Yuji Naito received scholarship funds from Otsuka Pharma-
ceutical Co. Ltd and Takeda Pharmaceutical Co. Ltd.
Questionnaire used in the present survey
Gastric cancer (GC)
1. How old were the patients when you started GC
screening? (Circle one)
2. What is the most common age group you screen for GC in
your hospital?
3. Which do you think is the best screening method for GC?
a. Barium X-ray examination
b. Endoscopy
c. Serum pepsinogen test
d. H. pylori antibody
e. Tumor marker
f. Others
4. Which is the most popular screening method in your
hospital?
5. Which combination among a–e is the best for GC
screening (for those who answered from a to e)?
6. For those who answered f, what kind of examination did
you perform?
7. What kind of follow-up examination did you perform in
H. pylori-positive patients who did not receive H. pylori
eradication?
8. What kind of follow-up examination and how often did
you perform it in patients who received H. pylori
eradication?
Colorectal cancer (CRC)
1. How old were the patients when you started CRC
screening?
2. What is the most common age group you screen for CRC
in your hospital?
3. Which do you think is the best screening method for
CRC?
a. Fecal occult blood test every year
b. Fecal DNA test every year
c. Sigmoidoscopy every 5 years
d. Total colonoscopy every 10 years
e. Barium enema every 5 years
f. CT colonography every 5 years
g. Others
4. Which is the most popular screening method in your
hospital?
5. For those who answered g, what kind of examination did
you perform?
6. Did you change the screening method of CRC after 10
years or before (for those who have had CRC over 10
years)?
7. For those who answered yes, what kind of examination
did you perform?
Appendix
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104
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