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World J Gastroenterol 2005;11(16):2477-2481

World Journal of Gastroenterology ISSN 1007-9327
2005 The WJG Press and Elsevier Inc. All rights reserved.

BRIEF REPORTS

Efficacy of omeprazole and amoxicillin with either clarithromycin

or metronidazole on eradication of Helicobacter pylori in Chinese
peptic ulcer patients
Wei-Hao Sun, Xi-Long Ou, Da-Zhong Cao, Qian Yu, Ting Yu, Jin-Ming Hu, Feng Zhu, Yun-Liang Sun, Xi-Ling Fu, Han Su
Wei-Hao Sun, Xi-Long Ou, Da-Zhong Cao, Qian Yu, Ting Yu,
Feng Zhu, Yun-Liang Sun, Xi-Ling Fu, Han Su, Department of
Gastroenterology, Zhongda Hospital of Southeast University,
Nanjing 210009, Jiangsu Province, China
Jin-Ming Hu, Department of Digestive Endoscopy, Golmud Railway
Hospital, Golmud 816000, Qinghai Province, China
Supported by the Scientific Research Foundation for ForeignReturned Chinese Scholars, State Education Ministry, China
Correspondence to: Dr. Wei-Hao Sun, Department of Geriatrics,
The First Affiliated Hospital of Nanjing Medical University, Nanjing
210009, Jiangsu Province, China
Telephone: +86-25-83718836-6044 Fax: +86-25-83783506
Received: 2004-02-02 Accepted: 2004-03-24

Abstract
AIM: One-week triple therapy with proton pump
inhibitors, clarithromycin and amoxicillin has recently
been proposed as the first-line treatment for Helicobacter
pylori (H pylori) infection; however, data regarding the
effects of this regimen in China are scarce. The aim of
this prospective and randomized study was to compare
the efficacy of clarithromycin and metronidazole when
they were combined with omeprazole and amoxicillin
on eradication of H pylori and ulcer healing in Chinese
peptic ulcer patients.
METHODS: A total of 103 subjects with H pylori-positive
peptic ulcer were randomly divided into two groups, and
accepted triple therapy with omeprazole 20 mg, amoxicillin
1 000 mg and either clarithromycin 500 mg (OAC group,
n = 58) or metronidazole 400 mg (OAM group, n = 45).
All drugs were given twice daily for 7 d. Patients with
active peptic ulcer were treated with omeprazole 20 mg
daily for 2-4 wk after anti-H pylori therapy. Six to eight
weeks after omeprazole therapy, all patients underwent
endoscopies and four biopsies (two from the antrum and
two others from the corpus of stomach) were taken for
rapid urease test and histological analysis (with modified
Giemsa staining) to examine H pylori . Successful
eradication was defined as negative results from both
examination methods.
RESULTS: One hundred patients completed the entire
course of therapy and returned for follow-up. The
eradication rate of H pylori for the per-protocol analysis
was 89.3% (50/56) in OAC group and 84.1% (37/44) in
OAM group. Based on the intention-to-treat analysis, the
eradication rate of H pylori was 86.2% (50/58) in OAC
group and 82.2% (37/45) in OAM group. There were no

significant differences in eradication rates between the

two groups on either analysis. The active ulcer-healing
rate was 96.7% (29/30) in OAC group and 100% (21/21)
in OAM group (per-protocol analysis, P>0.05). Six patients
in OAC group (10.3%) and five in OAM group (11.1%)
reported adverse events (P>0.05).
CONC LUSION: O ne - w e ek tr ipl e the ra py w i th
omeprazole and amoxicillin in combination with either
clarithromycin or metronidazole is effective for the
eradication of H pylori . The therapeutic regimen
co m prising m etro nidaz o le with low cos t, goo d
compliance and mild adverse events may offer a good
choice for the treatment of peptic ulcers associated with
H pylori infection in China.
2005 The WJG Press and Elsevier Inc. All rights reserved.

Key words: Omeprazole; Amoxicillin; H pylori

Sun WH, Ou XL, Cao DZ, Yu Q, Yu T, Hu JM, Zhu F, Sun YL,
Fu XL, Su H. Efficacy of omeprazole and amoxicillin with
either clarithromycin or metronidazole on eradication of
Helicobacter pylori in Chinese peptic ulcer patients. World J
Gastroenterol 2005; 11(16): 2477-2481

http://www.wjgnet.com/1007-9327/11/2477.asp

INTRODUCTION
Helicobacter pylori (H pylori) infects the stomachs of more
than 50% of people worldwide, and is responsible for most
peptic ulcer diseases, gastritis and gastric malignancies[1-4].
According to the Maastricht 2-2000 consensus report[5] ,
eradication of H pylori infection is strongly recommended
in duodenal and gastric ulcers, whether they are active
or not. Cure of the infection not only promotes peptic
ulcer healing but also reduces ulcer relapse. Recently, 1-wk
triple therapy with a proton-pump inhibitor (PPI) and
two antimicrobial agents (clarithromycin, amoxicillin, or
metronidazole/tinidazole) has been shown to be one of the
most effective regimens and is recommended as the firstline treatment of H pylori eradication due to its high cure
rates and convenience [6-8]. However, as in many other
infectious diseases, antibiotic resistance is the major cause
of treatment failure. Metronidazole-resistant strains of
H pylori have been reported to be increasing worldwide[9-11].
Although clarithromycin is an excellent drug for
treating H pylori infection overseas[12,13], this drug has not

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been widely used in China due to its high cost. Therefore,

we evaluated the efficacy of 1-wk triple therapy with
omeprazole, amoxicillin and clarithromycin (OAC) for H pylori
eradication and active peptic ulcer healing in Chinese
population. We also compared the results of OAC regimen
with a conventional traditional triple therapy with
omeprazole, amoxicillin and metronidazole (OAM).

MATERIALS AND METHODS

Patients
Patients with endoscopically-confirmed peptic ulcers
(including scar stage), and biopsy-proven H pylori infection
were enrolled into this prospective, randomized, investigatorblind, single-center study. Patients excluded from the study
included patients with liver cirrhosis, renal failure, or other
serious concomitant illnesses; alcoholics; patients were
treated in the two months preceding study entry with
antibiotics, bismuth preparations, proton pump inhibitors
or H2-receptor antagonists; patients with known allergy to
the medications used; patients with a history of previous
gastric surgery; pregnant women; and patients who
previously underwent eradication therapy. These criteria
were ascertained by means of a complete history, physical
examination, appropriate hematological and biochemical
tests. A total of 103 patients (85 men and 18 women) who
were recruited prospectively in the gastroenterology unit at
Affiliated Zhongda Hospital of Southeast University,
fulfilled the criteria for admission to the study. All patients
gave their fully informed written consent before entering
the study. The study also received the approval of the
Medical Ethics Committee of Southeast University.
Eradication methods
Patients were randomly divided into two groups, and
accepted triple therapy with omeprazole 20 mg, amoxicillin
1 000 mg and either clarithromycin 500 mg (OAC group,
n = 58) or metronidazole 400 mg (OAM group, n = 45). All
drugs were given twice daily for 7 d. Patients with active
peptic ulcer were treated with omeprazole 20 mg daily for
2-4 wk after anti-H pylori therapy. Each patient was asked
to return at the end of antibiotic treatment for a structured
clinical interview to assess adverse events and compliance.
Evaluation of eradication therapy
Six to eight weeks after omeprazole therapy, all patients
underwent endoscopies and four biopsies (two from the
antrum and another two from the corpus of the stomach)
were taken for rapid urease test and histological analysis
(with modified Giemsa staining) to examine H pylori.
Successful eradication was defined as negative results from
both examination methods. The healing of active ulcer was
also evaluated during endoscopic examination.
Statistical analysis
The results of treatment were evaluated with per-protocol
(PP) analysis (which included only patients who completed
the study) and intention-to-treat (ITT) analysis (which
included also patients who did not complete the study). The
demographic and clinical characteristics of the two groups

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Number 16

were compared by 2 test. The results of treatment were

compared by 2 test or Fishers exact test. P<0.05 was
considered statistically significant.

RESULTS
Demographic and clinical characteristics
The demographic and clinical characteristics of the 103
patients in the two groups are shown in Table 1. No significant
differences in demographic and clinical characteristics were
found between the two groups.
Table 1 Baseline characteristics of patients in two groups

Age (yr, meanSD)

Sex (M/F)
Gastric ulcer, active
Gastric ulcer, scar
Duodenal ulcer, active
Duodenal ulcer, scar

OAC (n = 58)

OAM (n = 45)

5211
48/10
10
13
21
14

5012
37/8
8
11
14
12

Eradication rates of H pylori

Of the 103 patients enrolled in this study, 3 (2.9%) withdrew
from the study because of drug-related adverse events. Of
them, two patients (each from OAC group and OAM group)
with skin rash and one from OAC group with diarrhea
discontinued the treatment. As a result, 100 patients (97.1%,
56 patients in OAC group and 44 patients in OAM group)
completed the entire course of therapy and returned for
follow-up. The eradication rates based on PP or ITT analyses
are shown in Table 2. There were no significant differences
in eradication rates between the two groups.

Table 2 Eradication rates in two treatment groups

2

OAC (n = 58)

OAM (n = 45)

PP analysis (%)

50/56(89.3)

37/44(84.1)

0.59

0.44

ITT analysis (%)

50/58(86.2)

37/45(82.2)

0.31

0.58

Numbers in parentheses indicate percentages.

Healing rates of active peptic ulcer

The active ulcer-healing rate on PP analysis was 96.7%
(29/30) in OAC group and 100% (21/21) in OAM group.
There were no significant differences between the two groups
(2 = 0.71, P>0.05).
Adverse events and compliance
Completed questionnaires about the adverse events and
compliance were obtained from all the 103 patients. Adverse
events were noticed (Table 3) in six patients in OAC group,
and five patients in OAM group, with no statistically
significant differences between the two groups (2 = 0.02,
P = 0.90). The symptoms of adverse events were mild and
did not necessitate any additional treatment in both groups.
None of the other serious events such as hepatic or renal
functional damages were found by means of biochemical

Sun WH et al. Helicobacter pylori eradication

2479

examination in the two groups. All patients, except for two

who had acute allergic skin rashes and one who had diarrhea,
were able to take the study medication completely for the
full study period. Thus, 100 patients (97.1%) had an excellent
compliance.
Table 3 Adverse events during treatment
OAC (n = 58)

OAM (n = 45)

Skin rash

Diarrhea

Headache

Nausea

Anorexia

Metallic taste

6/58 (10.3)

5/45 (11.1)

Total (%)

DISCUSSION
Many authors have reported a correlation between H pylori
infection and peptic ulcers[1,7,8]. Incidence of H pylori infection
was higher in patients with gastroduodenal ulcers than in
subjects without gastroduodenal disorders. The eradication
of H pylori has been strongly recommended in all patients
with peptic ulcer, including those with complications[5] .
Eradication of H pylori could assure rapid symptom relief
and accelerate ulcer healing [14] , prevent ulcer relapse and
reduce complications[7,8,15-18]. Furthermore, eradication of
H pylori could also improve the healing of intractable
ulcers[19-21]. However, the survival capabilities of H pylori in
the stomach made it difficult to be eradicated, and effective
treatment required multi-drug regimens consisting of two
antibiotics (usually selected from clarithromycin, metronidazole,
amoxicillin, and tetracycline) combined with PPI or bismuth
compounds[5,22,23]. Although the optimal treatment of H pylori
infection is still a matter of debate, the effectiveness of
PPI based 1-wk triple therapy has now been well established
and remains one of the first-line therapies of choice[6,14,24,25].
Clarithromycin is a new generation of macrolide antibiotic
that inhibits bacterial protein synthesis. Its antibacterial
spectrum is similar to that of erythromycin, but it is more
acid-stable, better absorbed, and is thought to be an effective
drug for treating H pylori infection[7,12,13]. Among several
eradication regimens, PPI with clarithromycin and amoxicillin
is thought to be one of the most effective treatments of
H pylori. Amoxicillin resistance was rarely reported[26] but
clarithromycin resistance has increased year after year [27] ,
and eradication rates with clarithromycin-containing
regimens decreased significantly[28]. The present study showed
that the H pylori eradication rate in OAC group was 89.3%
(50/56, PP analysis). The result is in accordance with
previous reports from China and Spain[29,30]. However, in a
study from Japan by Ogura et al[31], eradication was achieved
in 39/40 (98%) by PP analysis in clarithromycin-based triple
therapy for non-resistant H pylori infection. These results
indicate that the therapeutic effect of clarithromycin for
H pylori eradication is not quite consistent. It may be related
to different resistance to clarithromycin of infecting H pylori
strains in various countries and regions. Widespread use of

antimicrobial drugs has resulted in a worldwide increase in

the prevalence of antibiotic resistance in H pylori, 5-11%
of clinical H pylori strains isolated in China are resistant to
clarithromycin[32,33]. Although clarithromycin was not available
in China before 1996, the other members of macrolides
such as spiramycin, erythromycin and roxithromycin have
been widely used over the past years for the treatment of
respiratory infection, sexually transmitted diseases and other
infectious diseases. Thus, H pylori is able to develop resistance
to clarithromycin rapidly after contact with it, as crossresistance exists between macrolides. Some studies have
shown that clarithromycin resistance in H pylori substantially
affected the success rate of eradication regimens containing
clarithromycin[28]. In the present randomized study, there
were no significant differences between OAC and OAM
treatment groups in terms of H pylori eradication and ulcer
healing, confirming that 1-wk triple therapy with omeprazole
and amoxicillin in combination with either clarithromycin
or metronidazole has the same effectiveness on eradicating
the bacterium. Both eradication regimens were well
tolerated and patient compliance was excellent. However,
clarithromycin is too expensive to be widely used in China.
Antibacterial treatment of H pylori is difficult because
of the very rapid development of resistance to antimicrobial
agents, especially to nitroimidazoles, such as metronidazole
and tinidazole, and clarithromycin[34]. The resistance of
H pylori to metronidazole and clarithromycin strongly
affected the success of regimens involving these drugs. The
prevalence of resistance to these anti-microbial agents varied
with gender, ethnic group and country of origin[34]. It was
reported from Hong Kong (China) that almost 50% of pretreatment strains of H pylori were resistant to metronidazole
and over 10% to clarithromycin[33]. Metronidazole resistance
has been shown to reduce H pylori eradication rates in the
regimens containing amoxicillin and metronidazole[35,36] .
Several studies have shown a significantly higher rate of
metronidazole resistant H pylori among women[37-39], indicating
that this drug can be widely used for pelvic inflammatory
diseases in females[37]. In the current study, the number of
men was absolutely more than that of women either in
OAC or in OAM group. Whether the sex bias of patients
was related to the better eradication in OAM group remains
unknown. We did not test in vitro sensitivity to metronidazole
and clarithromycin. Although Epsilometer (E) test has been
recommended as the best and simplest method for routine
testing of antibiotic sensitivity to H pylori, the technique is
not yet widely available in China. On the other hand,
the exact mechanism responsible for the development of
H pylori resistance to metronidazole still remains obscure,
antimicrobial effectiveness in vivo was poorly predicted by
sensitivity in vitro [37] . This is largely because the current
breakpoints, which are the in vitro concentrations defining
the cut off between sensitive and resistant strains, do not
correlate with levels required for eradication of infection
from the gastric mucosa.
In the past, prevention of peptic ulcer recurrence was
based on long term use of H2-receptor antagonists or PPIs.
Since H pylori was recognized, it has been well understood
that eradicating the bacterium could significantly reduce the
recurrence of peptic ulcer diseases[8,16-18]. In our study, the

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ulcer relapse rate during the 12-mo follow-up was 66.7%

(4/6) in H pylori-positive patients and none of the 24 H pylorinegative patients relapsed (data not shown). In conclusion,
1-wk triple therapy with omeprazole and amoxicillin in
combination with either clarithromycin or metronidazole is
equally effective for eradication of H pylori and ulcer healing.
Clarithromycin is the most expensive antimicrobial drug used
to treat H pylori infection. Metronidazole with lower cost,
good compliance and mild adverse events may offer a good
choice for the treatment of peptic ulcers associated with
H pylori infection in China.

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Science Editor Zhu LH, Wang XL and Li WZ Language Editor Elsevier HK