Helicobacter pylori eradication increases the serum high density lipoprotein cholesterol level in the infected patients with chronic gastritis: A single-center observational study
Helicobacter pylori eradication increases the serum high density lipoprotein cholesterol level in the infected patients with chronic gastritis: A single-center observational study
Naoto IwaiID 0 1
Takashi Okuda 0 1
Kohei Oka 0 1
Tasuku Hara 0 1
Yutaka Inada 0 1
Toshifumi Tsuji 0 1
Toshiyuki Komaki 0 1
Ken Inoue 1
Osamu Dohi 1
Hideyuki Konishi 1
Yuji NaitoID 1
Yoshito Itoh 1
Keizo Kagawa 0 1
0 Department of Gastroenterology and Hepatology, Fukuchiyama City Hospital , Fukuchiyama-city, Kyoto , Japan , 2 Department of Molecular Gastroenterology and Hepatology, Graduate School of Medical Science, Kyoto Prefectural University of Medicine , Kyoto , Japan
1 Editor: Masaru Katoh, National Cancer Center , JAPAN
Extra-gastric manifestation of Helicobacter pylori infection involves systemic inflammation, which results in the production of several cytokines. Only a few clinical trials have investigated the effect of H. pylori eradication therapy on lipid metabolism in the infected patients with chronic gastritis. We aimed to evaluate the effect of H. pylori eradication therapy on lipid metabolism in a Japanese population with chronic gastritis.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: The authors received no specific funding
for this work.
Competing interests: The authors have declared
that no competing interests exist.
One hundred and sixty-three patients with H. pylori-associated chronic gastritis were
enrolled in this study between June 2015 and March 2017. They underwent H. pylori
eradication therapy; the effects of the therapy were assessed by the urea breath test performed
at least 4 weeks after the therapy. After confirming H. pylori eradication, the health
screening examination was repeated between May 2016 and August 2018. The clinical parameters
were compared before and after the administration of the eradication therapy.
The mean age of the enrolled patients was 56.7 years, and the mean follow-up duration was
514.7 days. Weight, body mass index, and obesity index were significantly increased
posteradication therapy compared to those pre-eradication therapy. White blood cell and platelet
counts were significantly decreased, and high density lipoprotein cholesterol (HDL) level
was significantly increased (P = 0.001), while low density lipoprotein cholesterol (LDL), total
cholesterol, and triglycerides levels were not altered significantly. Hence, the LDL/HDL ratio
was significantly decreased.
This study reported that H. pylori eradication therapy increase the HDL levels in the infected
patients with chronic gastritis. Hence, the LDL/HDL ratio, which is used to evaluate the risk
of atherosclerosis, was significantly decreased post-eradication therapy compared to that
Helicobacter pylori (H. pylori) is a gram-negative bacteria that causes chronic gastritis, peptic
ulcer, and gastric cancer.[
] H. pylori eradication therapy can prevent peptic ulcer
recurrence and may possibly result in decreasing the incidence of gastric cancer.[
] In contrast,
previous studies reported that H. pylori infection can cause extra-gastrointestinal (GI) disease,
including nonalcoholic fatty liver disease, dyslipidemia and coronary heart disease.[
pylori infection causes chronic and persistent inflammation, which results in the production of
cytokines, including tumor necrosis factor-?, interleukin (IL)-6 and IL-8.[
] The previous
reports revealed that H. pylori infection may worsen serum lipid levels through long-term
chronic inflammation caused by H. pylori.[
] In addition, H. pylori eradication
therapy may potentially improve the lipid profiles by inhibiting the release of inflammatory
] However, in some reports, the study subjects were confined to patients with
peptic ulcers or functional dyspepsia.[
19, 24, 25
] A few clinical trials have investigated whether
H. pylori eradication therapy improves lipid metabolism in patients with H. pylori-associated
In Japan, eradication therapy for H. pylori-associated chronic gastritis has been included in
the national health insurance program since February 2013.[
] Subsequently, H.
pyloriinfected patients without peptic ulcer or early gastric cancer have increasingly undergone
eradication therapy. The established insurance system may have a potential role in decreasing the
incidence of gastric cancer.[
] However, the mechanism of H. pylori eradication and its effect
on extra-gastric manifestations in patients with chronic gastritis remains controversial.
Therefore, it is important to investigate whether H. pylori eradication therapy for chronic
gastritis may significantly alter lipid metabolism in the infected patients. This study aimed to
evaluate the effect of H. pylori eradication therapy on lipid metabolism in the infected patients
with chronic gastritis.
Materials and methods
The patients who underwent the health screening examination between June 2015 and March
2017 were analyzed. When the upper GI endoscopic examination indicated the presence of an
H. pylori infection, the serum IgG anti-H. pylori test was performed based on patient
preferences. Based on the manufacturer?s instructions, H. pylori infection was defined as the
presence of a serum IgG antibody level of more than 10 IU/mL. When both endoscopic findings
and the serum IgG test indicated H. pylori infection, the patients underwent eradication
therapy. The patients with active gastroduodenal ulcers and gastric cancer and those undergoing
treatment for hyperlipidemia or failure of prior eradication were excluded. Finally, a total of
163 patients with successful eradication of H. pylori were enrolled in this study and underwent
a health screening examination again between May 2016 and August 2018.
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The first-line eradication therapy comprised administration of a proton pump inhibitor or
vonoprazan, amoxicillin, and clarithromycin twice daily for 1 week. The effects of the
eradication therapy were assessed by performing the urea breath test at least 4 weeks after the therapy.
A ?13C level of less than 2.5? indicated successful eradication of H. pylori, while that of more
than 2.5? was determined as a failure of H. pylori eradication.[
] When the urea breath test
results indicated failure of H. pylori eradication, the second-line eradication therapy
comprising administration of a proton pump inhibitor or vonoprazan, amoxicillin, and metronidazole
twice daily for 1 week was initiated. The clinical parameters recorded before and after the
administration of the eradication therapy were compared.
This study was conducted in accordance with the ethical guidelines of the Declaration of
Helsinki, and the study protocol was approved by the ethics committee of the Fukuchiyama
City Hospital. All data were fully anonymized before we accessed them, and the ethics committee of the Fukuchiyama City Hospital approved a waiver of informed consent because anonymized clinical data were used in this study.
The serum IgG anti-H. pylori test was performed using an enzyme-linked immunosorbent
assay (Eiken Chemical Co. Ltd, Tokyo, Japan). A serum IgG antibody level of more than 10
IU/mL was defined as the presence of H. pylori infection. The body mass index (BMI), obesity
index, and body fat percentage were automatically calculated using the Tanita DC-270A
analyzer (Tanita Corporation, Tokyo, Japan). All patients underwent blood and biochemical tests
twice, before and after H. pylori eradication. The biochemical tests were performed in the
morning after overnight fasting.
The following factors were evaluated for all the patients; white blood cell (WBC) count, red
blood cell (RBC) count, hematocrit (Hct) volume, mean corpuscular volume, mean
corpuscular hemoglobin, mean corpuscular hemoglobin concentration, platelets (Plt) count, and levels
of hemoglobin (Hb), total cholesterol (T-cho), high density lipoprotein cholesterol (HDL), low
density lipoprotein cholesterol (LDL), triglycerides, uric acid, aspartate aminotransferase,
alanine aminotransferase, blood urea nitrogen, creatinine, fasting plasma glucose, and
The continuous variables were expressed as means and standard deviations (SD). The categori
cal variables were expressed as numbers and percentages. The Wilcoxon signed-rank test was
used to compare the values of parameters before and after the administration of the
eradication therapy. P values <0.05 were considered statistically significant. All statistical analyses
were performed using IBM SPSS version 25.0 for Windows (IBM SPSS, Chicago, IL, USA).
The characteristics of the H. pylori-eradicated patients are shown in Table 1. The mean age of
the enrolled patients was 56.7 years. The mean anti-H. pylori IgG antibody titer in the serum
was 47.5 U/ml. The mean follow-up duration was 514.7 days.
The effect of H. pylori eradication is shown in Table 2. Weight, obesity index and BMI sig
nificantly increased post-eradication therapy compared to the pre-eradication therapy values.
The blood test results showed a significant decrease in the WBC and Plt counts, with no remarkable change in the RBC counts. No significant changes were observed in the liver function, renal function or glucose metabolism.
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In the lipid profile, the HDL level (61.2 ? 14.7 mg/dL at baseline versus 63.3 ? 15.8 mg/dL
at post-eradication therapy, P < 0.01) was significantly increased, while the T-cho (206.0 ?
32.5 mg/dL versus 205.1 ? 30.8 mg/dL), LDL (121.2 ? 28.7 mg/dL versus 119.0 ? 27.6 mg/dL),
and TG (98.1 ? 50.9 mg/dL versus 103.5 ? 58.0 mg/dL) levels did not change significantly (Fig
1). Hence, the LDL/HDL (2.11 ? 0.75 mg/dL at baseline versus 2.02 ? 0.76 mg/dL at post-erad
ication therapy, P < 0.01) ratio was significantly decreased post-eradication therapy compared
to that pre-eradication therapy (Fig 2).
In the present study, we noted a significant increase in the weight, BMI, and obesity index of
patients with H. pylori-associated chronic gastritis, approximately 1.5 years after the
administration of the H. pylori eradication therapy. In addition, H. pylori eradication induced a
decrease in the WBC and Plt counts. With respect to the lipid profiles, the HDL level was
significantly increased, while the LDL/HDL ratio was significantly decreased. The results show
that H. pylori eradication therapy may prevent the development of arteriosclerosis by the
regulation of serum lipid concentrations, especially the HDL levels.
Inflammatory cytokines may have an essential role in dyslipidemia and arteriosclerosis.[8,
28, 29] In Japan, the national health insurance system was originally established for H. pylori
eradication therapy to prevent chronic gastritis. Since an increasing number of patients with
chronic gastritis undergo H. pylori eradication, it is important to assess the systemic effects
caused by the eradication. However, little is known, especially, regarding the alterations in the
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BMI, body mass index; WBC, white blood cell; RBC, red blood cell; Hb, hemoglobin; Hct, hematocrit; MCV, mean corpuscular volume; MCH, mean corpuscular
hemoglobin; MCHC, mean corpuscular hemoglobin concentration; Plt, platelets; AST, aspartate aminotransferase; ALT, alanine aminotransferase; BUN, blood urea
nitrogen; Cre, creatinine; UA, uric acid; FPG, fasting plasma glucose; HbA1c, hemoglobin A1c.
lipid profiles after administration of the H. pylori eradication therapy in the infected patients
with chronic gastritis.[
In accordance with the previous reports, weight and BMI significantly increased after
administration of H. pylori eradication therapy.[
] Lane et al. confirmed that BMI and
weight significantly increased on administration of H. pylori eradication therapy not only in
the Japanese patients, but also in the European population because of improvement in
dyspepsia. In addition, the WBC and Plt counts significantly decreased after administration of
the H. pylori eradication therapy. The WBC count was reported to increase in proportion to
the ratio of the H. pylori infection.[
] These findings suggest that chronic inflammation
caused due to H. pylori infection increased both the WBC and Plt counts. The eradication
therapy could eliminate chronic inflammation, which results in decreased WBC and Plt counts.
Kanbay et al. reported that CRP levels were also decreased on administration of the H. pylori
eradication therapy [
]. This report provided additional evidence that the eradication therapy
could reduce systemic inflammation.
This study reported that the HDL level was significantly increased after the administration of the eradication therapy, as reported in previous studies.[19?21, 23, 24] Systemic inflammation was previously proven to alter the composition of HDL protein and lipid, and decrease the HDL levels.[35, 36] In addition, inflammation could transform HDL into a dysfunctional
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Fig 1. Lipid profiles at baseline and post-eradication therapy. (A) Box plot showing serum the T-cho levels at baseline and post-eradication therapy. (B) Box plot
showing the serum TG levels at baseline and post-eradication therapy. (C) Box plot showing the serum HDL levels at baseline and post-eradication therapy. P < 0.01.
(D) Box plot showing the serum LDL levels at baseline and post-eradication therapy. Scatter dot plots show the measured serum levels. The middle line represents the
median. The symbol ?x? in the box plot represents the mean. T-cho, total cholesterol; TG, triglycerides; HDL, high density lipoprotein cholesterol; LDL, low density
condition. These observations suggested that inflammatory cascades induced by H. pylori
resulted in a decrease in the HDL levels. However, the eradication therapy restored the serum
HDL level by an improvement in the inflammatory status. Unlike the results of our study,
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Fig 2. Low density lipoprotein / high density lipoprotein cholesterol ratios at baseline and post-eradication therapy. Box plot showing the serum LDL/HDL ratios
at baseline and post-eradication therapy. P < 0.01. Scatter dot plots show the measured serum levels. The middle line represents the median. The symbol ?x? in the
box plot represents the mean. HDL, high density lipoprotein cholesterol; LDL, low density lipoprotein cholesterol.
PLOS ONE | https://doi.org/10.1371/journal.pone.0221349
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Elizalde et.al [
] reported that the HDL levels significantly increased in H. pylori infected
patients, irrespective of the administration of the eradication therapy, when the HDL level was
evaluated at baseline and 3 months after the administration of the eradication therapy. They
suggested that the increase in the HDL level may be due to improvement in dyspepsia and
lifestyle and, not due to the H. pylori eradication therapy itself. The difference may be because
treatment with antacids could inhibit H. pylori-induced chronic gastritis in some patients who
did not undergo eradication therapy but underwent treatment with antacids, with follow-up
periods shorter than that in our study. [
] Obesity was reportedly related to disturbances in
the lipid profiles [
]; however, administration of the H. pylori eradication therapy caused
both weight gain and improvement of lipid metabolism in this study. This discrepancy may be
because the regulation of the HDL levels in the H. pylori-eradicated patients was more strongly
influenced by the suppression of systemic inflammation than by weight gain. However, the
mean follow-up duration in this study was approximately 1.5 years. In further studies, we
should investigate the effect of H. pylori eradication on lipid profiles and weight over a longer
In general, HDL has an atheroprotective role, while LDL has an atherosclerotic role. More
over, the LDL/HDL ratio has been recently considered a better predictive parameter compared
with the HDL and LDL levels alone, for the assessment of the severity of coronary plaque or
] Our findings revealed that the LDL/HDL ratio significantly
decreased following the administration of the eradication therapy. The results suggested that
H. pylori eradication may possibly contribute to anti-atherogenic properties.
The present study has several limitations. First, this was a single center and retrospective
study. Second, due to the small sample size, it is difficult to generalize the results of this study.
Our results must be confirmed in a large-scale population validation analysis, such as a study
with moer than 500 cases. If possible, meta-analyses may be recommended to confirm the
effect of H. pylori eradication on lipid profiles. Third, the mean follow-up period was
approximately 1.5 years. Therefore, it is unclear whether our findings can be extrapolated to a longer
follow-up period. Our results must be validated in a prospective clinical trial allowing for a
longer observation period. Fourth, our study did not include the H. pylori-negative patients as a
control group. Thus, we could not evaluate the changes in lipid metabolism in H.
pylori-negative patients; however, we believe that our results provide insights into the lipid metabolism of
H. pylori-positive patients.
In conclusion, we showed that administration of the H. pylori eradication therapy increased
the HDL levels in the infected patients with chronic gastritis. In addition, a decrease in the
LDL/HDL ratio suggests that H. pylori eradication may possibly play an anti-atherogenic role
in the infected patients with chronic gastritis.
S1 Table. Summary of the published data on the changes in the lipid profiles at baseline
and post-eradication therapy.
The authors thank all members of the Department of Gastroenterology and Hepatology, Fukuchiyama City Hospital. We also thank Ms. Noriko Nishimura for assistance with data collection. Moreover, we would like to thank Editage (www.editage.jp) for English language editing.
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Conceptualization: Naoto Iwai.
Data curation: Naoto Iwai, Kohei Oka, Tasuku Hara, Yutaka Inada, Toshifumi Tsuji,
Formal analysis: Naoto Iwai.
Investigation: Naoto Iwai, Takashi Okuda, Kohei Oka, Tasuku Hara, Yutaka Inada, Toshifumi
Tsuji, Toshiyuki Komaki, Ken Inoue, Osamu Dohi.
Methodology: Naoto Iwai, Takashi Okuda.
Project administration: Naoto Iwai, Takashi Okuda, Keizo Kagawa.
Resources: Naoto Iwai.
Software: Naoto Iwai.
Supervision: Naoto Iwai, Hideyuki Konishi, Yuji Naito, Yoshito Itoh, Keizo Kagawa.
Validation: Naoto Iwai, Ken Inoue, Osamu Dohi, Hideyuki Konishi, Yuji Naito.
Visualization: Naoto Iwai.
Writing ? original draft: Naoto Iwai.
Writing ? review & editing: Naoto Iwai, Takashi Okuda, Yoshito Itoh, Keizo Kagawa.
9 / 11
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1. Marshall BJ , Warren JR . Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration . Lancet . 1984 ; 1 ( 8390 ): 1311 - 5 . https://doi.org/10.1016/s0140- 6736 ( 84 ) 91816 - 6 PMID: 6145023
2. Parsonnet J , Friedman GD , Vandersteen DP , Chang Y , Vogelman JH , Orentreich N , et al. Helicobacter pylori infection and the risk of gastric carcinoma . N Engl J Med . 1991 ; 325 ( 16 ): 1127 - 31 . https://doi.org/ 10.1056/NEJM199110173251603 PMID: 1891020
3. Graham DY . Treatment of peptic ulcers caused by Helicobacter pylori . N Engl J Med . 1993 ; 328 ( 5 ): 349 - 50 . https://doi.org/10.1056/NEJM199302043280512 PMID: 8419823
4. Asaka M , Kato M , Sugiyama T , Satoh K , Kuwayama H , Fukuda Y , et al. Follow-up survey of a largescale multicenter, double-blind study of triple therapy with lansoprazole, amoxicillin, and clarithromycin for eradication of Helicobacter pylori in Japanese peptic ulcer patients . J Gastroenterol . 2003 ; 38 ( 4 ): 339 - 47 . https://doi.org/10.1007/s005350300061 PMID: 12743773
5. Sumida Y , Kanemasa K , Imai S , Mori K , Tanaka S , Shimokobe H , et al. Helicobacter pylori infection might have a potential role in hepatocyte ballooning in nonalcoholic fatty liver disease . J Gastroenterol . 2015 ; 50 ( 9 ): 996 - 1004 . https://doi.org/10.1007/s00535-015 -1039-2 PMID: 25622927
6. Patel P , Mendall MA , Carrington D , Strachan DP , Leatham E , Molineaux N , et al. Association of Helicobacter pylori and Chlamydia pneumoniae infections with coronary heart disease and cardiovascular risk factors . BMJ . 1995 ; 311 ( 7007 ): 711 - 4 . https://doi.org/10.1136/bmj.311.7007.711 PMID: 7549683
7. Niemela S , Karttunen T , Korhonen T , Laara E , Karttunen R , Ikaheimo M , et al. Could Helicobacter pylori infection increase the risk of coronary heart disease by modifying serum lipid concentrations? Heart . 1996 ; 75 ( 6 ): 573 - 5 . https://doi.org/10.1136/hrt.75.6.573 PMID: 8697159
8. Laurila A , Bloigu A , Nayha S , Hassi J , Leinonen M , Saikku P. Association of Helicobacter pylori infection with elevated serum lipids . Atherosclerosis . 1999 ; 142 ( 1 ): 207 - 10 . https://doi.org/10.1016/s0021- 9150 ( 98 ) 00194 - 4 PMID: 9920523
9. Moss SF , Legon S , Davies J , Calam J . Cytokine gene expression in Helicobacter pylori associated antral gastritis . Gut . 1994 ; 35 ( 11 ): 1567 - 70 . https://doi.org/10.1136/gut.35.11.1567 PMID: 7828974
10. Ando T , Kusugami K , Ohsuga M , Shinoda M , Sakakibara M , Saito H , et al. Interleukin-8 activity correlates with histological severity in Helicobacter pylori-associated antral gastritis . Am J Gastroenterol . 1996 ; 91 ( 6 ): 1150 - 6 . PMID: 8651162
11. Keates S , Hitti YS , Upton M , Kelly CP . Helicobacter pylori infection activates NF-kappa B in gastric epithelial cells . Gastroenterology . 1997 ; 113 ( 4 ): 1099 - 109 . https://doi.org/10.1053/gast. 1997 . v113 . pm9322504 PMID: 9322504
12. Chimienti G , Russo F , Lamanuzzi BL , Nardulli M , Messa C , Di Leo A , et al. Helicobacter pylori is associated with modified lipid profile: impact on Lipoprotein(a ). Clin Biochem . 2003 ; 36 ( 5 ): 359 - 65 . PMID: 12849867
13. Gunji T , Matsuhashi N , Sato H , Fujibayashi K , Okumura M , Sasabe N , et al. Helicobacter pylori infection is significantly associated with metabolic syndrome in the Japanese population . Am J Gastroenterol . 2008 ; 103 ( 12 ): 3005 - 10 . https://doi.org/10.1111/j.1572- 0241 . 2008 . 02151 . x PMID : 19086952
14. Kucukazman M , Yavuz B , Sacikara M , Asilturk Z , Ata N , Ertugrul DT , et al. The relationship between updated Sydney System score and LDL cholesterol levels in patients infected with Helicobacter pylori . Dig Dis Sci . 2009 ; 54 ( 3 ): 604 - 7 . https://doi.org/10.1007/s10620-008-0391-y PMID: 18649137
15. Satoh H , Saijo Y , Yoshioka E , Tsutsui H. Helicobacter Pylori infection is a significant risk for modified lipid profile in Japanese male subjects . Journal of atherosclerosis and thrombosis . 2010 ; 17 ( 10 ): 1041 - 8 . https://doi.org/10.5551/jat.5157 PMID: 20610892
16. Kim HL , Jeon HH , Park IY , Choi JM , Kang JS , Min KW . Helicobacter pylori infection is associated with elevated low density lipoprotein cholesterol levels in elderly Koreans . J Korean Med Sci . 2011 ; 26 ( 5 ): 654 - 8 . https://doi.org/10.3346/jkms. 2011 . 26 .5.654 PMID: 21532857
17. Chen TP , Hung HF , Chen MK , Lai HH , Hsu WF , Huang KC , et al. Helicobacter Pylori Infection is Positively Associated with Metabolic Syndrome in Taiwanese Adults: a Cross-Sectional Study . Helicobacter . 2015 ; 20 ( 3 ): 184 - 91 . https://doi.org/10.1111/hel.12190 PMID: 25582223
18. Kim TJ , Lee H , Kang M , Kim JE , Choi YH , Min YW , et al. Helicobacter pylori is associated with dyslipidemia but not with other risk factors of cardiovascular disease . Sci Rep . 2016 ; 6 : 38015 . https://doi.org/10. 1038/srep38015 PMID: 27892538
19. Scharnagl H , Kist M , Grawitz AB , Koenig W , Wieland H , Marz W. Effect of Helicobacter pylori eradication on high-density lipoprotein cholesterol . Am J Cardiol . 2004 ; 93 ( 2 ): 219 - 20 . https://doi.org/10.1016/j. amjcard. 2003 . 09 .045 PMID: 14715353
20. Kanbay M , Gur G , Yucel M , Yilmaz U , Boyacioglu S . Does eradication of Helicobacter pylori infection help normalize serum lipid and CRP levels? Dig Dis Sci . 2005 ; 50 ( 7 ): 1228 - 31 . https://doi.org/10.1007/ s10620-005 -2764-9 PMID: 16047464
21. Nam SY , Ryu KH , Park BJ , Park S. Effects of Helicobacter pylori infection and its eradication on lipid profiles and cardiovascular diseases . Helicobacter . 2015 ; 20 ( 2 ): 125 - 32 . https://doi.org/10.1111/hel. 12182 PMID: 25382033
22. Adachi K , Mishiro T , Okimoto E , Kinoshita Y. Influence of the Degree of Gastric Mucosal Atrophy on the Serum Lipid Levels Before and After the Eradication of Helicobacter pylori Infection . Intern Med . 2018 .
23. Adachi K , Mishiro T , Toda T , Kano N , Fujihara H , Mishima Y , et al. Effects of Helicobacter pylori eradication on serum lipid levels . J Clin Biochem Nutr . 2018 ; 62 ( 3 ): 264 - 9 . https://doi.org/10.3164/jcbn.17-88 PMID: 29892167
24. Mokhtare M , Mirfakhraee H , Arshad M , Samadani Fard SH , Bahardoust M , Movahed A , et al. The effects of helicobacter pylori eradication on modification of metabolic syndrome parameters in patients with functional dyspepsia . Diabetes Metab Syndr . 2017 ; 11 Suppl 2 : S1031 - s5 .
25. Kamada T , Hata J , Kusunoki H , Ito M , Tanaka S , Kawamura Y , et al. Eradication of Helicobacter pylori increases the incidence of hyperlipidaemia and obesity in peptic ulcer patients . Dig Liver Dis . 2005 ; 37 ( 1 ): 39 - 43 . https://doi.org/10.1016/j.dld. 2004 . 07 .017 PMID: 15702858
26. Asaka M , Kato M , Sakamoto N. Roadmap to eliminate gastric cancer with Helicobacter pylori eradication and consecutive surveillance in Japan . J Gastroenterol . 2014 ; 49 ( 1 ): 1 - 8 . https://doi.org/10.1007/ s00535-013 -0897-8 PMID: 24162382
27. Ohara S , Kato M , Saito M , Fukuda S , Kato C , Hamada S , et al. Comparison between a new 13C-urea breath test, using a film-coated tablet, and the conventional 13C-urea breath test for the detection of Helicobacter pylori infection . J Gastroenterol . 2004 ; 39 ( 7 ): 621 - 8 . https://doi.org/10.1007/s00535-004 - 1356-3 PMID: 15293131
28. Buzas GM . Metabolic consequences of Helicobacter pylori infection and eradication . World J Gastroenterol . 2014 ; 20 ( 18 ): 5226 - 34 . https://doi.org/10.3748/wjg. v20.i18.5226 PMID: 24833852
29. Franceschi F , Annalisa T , Teresa DR , Giovanna D , Ianiro G , Franco S , et al. Role of Helicobacter pylori infection on nutrition and metabolism . World J Gastroenterol . 2014 ; 20 ( 36 ): 12809 - 17 . https://doi.org/ 10.3748/wjg. v20.i36.12809 PMID: 25278679
30. Azuma T , Suto H , Ito Y , Muramatsu A , Ohtani M , Dojo M , et al. Eradication of Helicobacter pylori infection induces an increase in body mass index . Aliment Pharmacol Ther . 2002 ; 16 Suppl 2 : 240 - 4 .
31. Furuta T , Shirai N , Xiao F , Takashima M , Hanai H . Effect of Helicobacter pylori infection and its eradication on nutrition . Aliment Pharmacol Ther . 2002 ; 16 ( 4 ): 799 - 806 . PMID: 11929399
32. Fujiwara Y , Higuchi K , Arafa UA , Uchida T , Tominaga K , Watanabe T , et al. Long-term effect of Helicobacter pylori eradication on quality of life, body mass index, and newly developed diseases in Japanese patients with peptic ulcer disease . Hepatogastroenterology . 2002 ; 49 ( 47 ): 1298 - 302 . PMID: 12239930
33. Lane JA , Murray LJ , Harvey IM , Donovan JL , Nair P , Harvey RF . Randomised clinical trial: Helicobacter pylori eradication is associated with a significantly increased body mass index in a placebo-controlled study . Aliment Pharmacol Ther . 2011 ; 33 ( 8 ): 922 - 9 . https://doi.org/10.1111/j.1365- 2036 . 2011 . 04610 . x PMID : 21366634
34. Yu YY , Cai JT , Song ZY , Tong YL , Wang JH . The associations among Helicobacter pylori infection, white blood cell count and nonalcoholic fatty liver disease in a large Chinese population . Medicine (Baltimore) . 2018 ; 97 ( 46 ):e13271. https://doi.org/10.1097/MD.0000000000013271 PMID: 30431613
35. Rohrer L , Hersberger M , von Eckardstein A. High density lipoproteins in the intersection of diabetes mellitus, inflammation and cardiovascular disease . Curr Opin Lipidol . 2004 ; 15 ( 3 ): 269 - 78 . PMID: 15166782
36. Ansell BJ , Watson KE , Fogelman AM , Navab M , Fonarow GC . High-density lipoprotein function recent advances . J Am Coll Cardiol . 2005 ; 46 ( 10 ): 1792 - 8 . https://doi.org/10.1016/j.jacc. 2005 . 06 .080 PMID: 16286161
37. Elizalde JI , Pique JM , Moreno V , Morillas JD , Elizalde I , Bujanda L , et al. Influence of Helicobacter pylori infection and eradication on blood lipids and fibrinogen . Aliment Pharmacol Ther . 2002 ; 16 ( 3 ): 577 - 86 . PMID: 11876713
38. Loo VG , Sherman P , Matlow AG . Helicobacter pylori infection in a pediatric population: in vitro susceptibilities to omeprazole and eight antimicrobial agents . Antimicrob Agents Chemother . 1992 ; 36 ( 5 ): 1133 - 5 . https://doi.org/10.1128/aac.36.5.1133 PMID: 1510406
39. Terry RB , Wood PD , Haskell WL , Stefanick ML , Krauss RM . Regional adiposity patterns in relation to lipids, lipoprotein cholesterol, and lipoprotein subfraction mass in men . J Clin Endocrinol Metab . 1989 ; 68 ( 1 ): 191 - 9 . https://doi.org/10.1210/jcem-68-1-191 PMID: 2909551
40. Katakami N , Kaneto H , Osonoi T , Saitou M , Takahara M , Sakamoto F , et al. Usefulness of lipoprotein ratios in assessing carotid atherosclerosis in Japanese type 2 diabetic patients . Atherosclerosis . 2011 ; 214 ( 2 ): 442 - 7 . https://doi.org/10.1016/j.atherosclerosis. 2010 . 10 .035 PMID: 21146820
41. Fujihara K , Suzuki H , Sato A , Kodama S , Heianza Y , Saito K , et al. Carotid artery plaque and LDL-toHDL cholesterol ratio predict atherosclerotic status in coronary arteries in asymptomatic patients with type 2 diabetes mellitus . Journal of atherosclerosis and thrombosis . 2013 ; 20 ( 5 ): 452 - 64 . https://doi.org/ 10.5551/jat.14977 PMID: 23363982
42. Kawakami R , Matsumoto I , Shiomi M , Kurozumi M , Miyake Y , Ishizawa M , et al. Role of the Low-Density Lipoprotein-Cholesterol/High-Density Lipoprotein-Cholesterol Ratio in Predicting Serial Changes in the Lipid Component of Coronary Plaque . Circ J . 2017 ; 81 ( 10 ): 1439 - 46 . https://doi.org/10.1253/circj. CJ- 16 -1209 PMID: 28458377