This research note summarizes the results of a 7-year study on antibiotic resistance of Helicobacter pylori in Chinese patients from 13 provinces. The study found:
1) Resistance to metronidazole, clarithromycin, and levofloxacin was high at 78.2%, 22.1%, and 19.2% respectively.
2) Younger patients had lower resistance to clarithromycin, azithromycin, levofloxacin, and moxifloxacin than older patients.
3) Resistance to clarithromycin and amoxicillin increased in more recent years.
4) Geographic location was associated with differences in resistance to metron
3. (p 0.001). Compared to adult patients (40 years old), younger
patients (40 years old) showed lower resistance rates to CLA (p
0.008), AZI (p 0.019), LEV (p 0.001) and MOX (p 0.042). The resis-
tance rate for CLA (p 0.037) and AMO (p 0.014) were higher in
strains isolated in 2013e2016 than in those isolated in 2010e2012.
Resistance rates to LEV (p 0.009) and MOX (p 0.017) were higher in
strains isolated from gastritis patients than duodenal ulcer patients.
Furthermore, we also observed the prevalence of MET (p 0.041),
CLA (p 0.001), AZI (p 0.001) and AMO (p 0.025) resistance were
significantly different in different regions of China, and resistance
rates were high in the northeast area.
Discussion
This study included a large number of strains from 13 provinces
or cities in China collected between 2010 and 2016. Overall, the
results indicate that high rates of primary resistance to antibiotics
are still a challenge to the eradication of H. pylori in China. The
prevalence of MET and CLA resistance in China is significantly
higher than in previous decades [9], which may also induce low
eradication rates for sequential and concomitant therapies [3]. The
prevalence of AMO and CLA resistance has increased recently,
which suggests that the dynamic monitoring of AMO and CLA
susceptibility is essential. Our results also suggest that younger
patients have a lower resistance rate to CLA, AZI, LEV and MOX than
patients over 40, a phenomenon that may be related to the accu-
mulation of drug use with age as well as the fact that elderly pa-
tients are more likely experience respiratory tract and urinary
infections. In addition, the resistance rates to MET, CLA, AZI and
AMO were significantly different in different areas, indicating that
the use of these antibiotics should consider local antibiotic
resistance.
In China, antieH. pylori drugs such as bismuth, TET and FUR are
available. Therefore, quadruple therapy with proton pump in-
hibitors, bismuth and a combination of two antibioticsdspecifi-
cally FUR, TET or AMOdwould be more suitable for Chinese
patients. This treatment is also recommended in the Maastricht V/
Florence Consensus Report [3].
Conclusions
The resistance rates to MET, CLA and LEV were high in China.
Patient age, gender, disease and geographical location were asso-
ciated with the resistance of H. pylori to some antibiotics. Consid-
ering the antibiotic resistance profiles, FUR, AMO and TET are better
choices for H. pylori treatment.
Transparency Declaration
Funding was provided by grants from National Science and
Technology Major Projects for ‘Major New Drugs Innovation and
Development’ of China (2011ZX09302-007-03), National Key
Research and Development Grogram of China (2016YFC1302201);
and the National Natural Science Foundation of China (81460115),
Science and Technology Projects of Jiangxi province
(2014BBG70019). All authors report no conflicts of interest rele-
vant to this article.
Table 1
Factors associated with Helicobacter pylori resistance
Characteristic N MET CLA AZI LEV MOX AMO TCT RIF FUR
Age * * * *
40 years 522 397 (76.1) 97 (18.6) 105 (20.1) 78 (14.9) 80 (15.3) 19 (3.6) 8 (1.5) 5 (1.0) 0
40 years 595 477 (80.2) 150 (25.2) 155 (26.1) 136 (22.9) 120 (20.2) 19 (3.2) 13 (2.2) 12 (2.0) 0
Gender * *
Male 676 517 (76.5) 148 (21.9) 154 (22.8) 114 (16.9) 97 (14.3) 21 (3.1) 12 (1.8) 12 (1.8) 0
Female 441 357 (81.0) 99 (22.4) 106 (24.0) 100 (22.7) 103 (23.4) 17 (3.9) 9 (2.0) 5 (1.1) 0
Year of isolation * *
2010e2012 355 276 (77.7) 65 (18.3) 70 (19.7) 72 (20.3) 73 (20.6) 4 (1.1) 8 (2.3) 7 (2.0) 0
2013e2016 762 598 (78.5) 182 (23.9) 190 (24.9) 142 (18.6) 127 (16.7) 34 (4.5) 13 (1.7) 10 (1.3) 0
Disease * *
DU 1093 855 (78.2) 240 (22.0) 251 (23.0) 204 (18.7) 191 (17.5) 38 (3.5) 19 (1.7) 17 (1.6) 0
Gastritis 24 19 (79.2) 7 (29.2) 9 (37.5) 10 (41.7) 9 (37.5) 0 2 (8.3) 0 0
Area * * * *
Northeast 66 59 (89.4) 30 (45.5) 34 (51.5) 14 (21.2) 14 (21.2) 6 (9.1) 2 (3.0) 0 0
East 312 233 (74.7) 75 (24.0) 71 (24.4) 63 (20.2) 48 (15.4) 14 (4.5) 3 (1.0) 2 (0.6) 0
Central 683 535 (78.3) 127 (18.6) 138 (19.5) 121 (17.7) 122 (17.9) 17 (2.5) 14 (2.0) 13 (1.9) 0
West 56 47 (83.9) 15 (26.8) 17 (30.4) 13 (23.2) 16 (28.6) 1 (1.8) 2 (3.6) 2 (3.6) 0
Overall 1117 874 (78.2) 247 (22.1) 260 (23.3) 214 (19.2) 200 (17.2) 38 (3.4) 21 (1.9) 17 (1.5) 0
Data are presented as n (%).
AMO, amoxicillin; AZI, azithromycin; CLA, clarithromycin; DU, duodenal ulcer; FUR, furazolidone; LEV, levofloxacin; MET, metronidazole; MOX, moxifloxacin; RIF, rifampicin;
TCT, tetracycline.
*p 0.05.
Fig. 1. Characteristics of antibiotic resistance for Helicobacter pylori in China. M þ C,
metronidazole þ clarithromycin; M þ L, metronidazole þ levofloxacin; C þ L,
clarithromycin þ levofloxacin; A þ M, amoxicillin þ metronidazole; A þ C,
amoxicillin þ clarithromycin; A þ L, amoxicillin þ levofloxacin; A þ T,
amoxicillin þ tetracycline; A þ F, amoxicillin þ furazolidone; T þ M,
tetracycline þ metronidazole; T þ F, tetracycline þ furazolidone; M þ C þ Q,
metronidazole þ clarithromycin þ levofloxacin.
D.-S. Liu et al. / Clinical Microbiology and Infection 24 (2018) 780.e5e780.e8780.e7
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