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Original Article | Open Access

Effects of Helicobacter pylori eradication on the profiles of blood metabolites and their associations with the progression of gastric lesions: a prospective follow-up study

Wenhui Wu1,*Zongchao Liu1,*Zhexuan Li1Weidong Liu2Lanfu Zhang3Yang Zhang1Tong Zhou1Weicheng You1Kaifeng Pan1 ( )Wenqing Li1 ( )
Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Cancer Epidemiology, Peking University Cancer Hospital and Institute, Haidian District, Beijing 100142, China
Linqu County Public Health Bureau, Linqu 262600, China
Linqu County People’s Hospital, Linqu 262600, China

*These authors contributed equally to this work.

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Abstract

Objective

This study aimed at examining the alterations in metabolomic profiles caused by treatment of H. pylori infection, and the associations between key plasma metabolites and the risk of gastric lesion progression during follow-up after treatment.

Methods

An intervention trial was performed in 183 participants, 117 of whom were H. pylori positive participants receiving treatment for H. pylori infection. H. pylori positive participants were prospectively followed for 182 to 1,289 days. Untargeted metabolomics assays were conducted on plasma samples collected at baseline, 6 months after treatment, and during continued follow-up.

Results

We identified 59 metabolites with differential posttreatment changes between participants with successful and failed H. pylori eradication, 17 metabolites significantly distinguished participants with successful vs. failed eradication. Two metabolites [PC(18:1(11Z)/14:1(9Z)) and (2S)-6-amino-2-formamidohexanamide] showed posttreatment changes positively associated with successful H. pylori eradication, and were inversely associated with the risk of gastric lesion progression among participants with successful eradication. In contrast, 9-decenoic acid showed posttreatment changes inversely associated with successful eradication: its level was positively associated with the risk of gastric lesion progression among participants with successful eradication. Although the identified metabolites showed a temporary but significant decline after treatment, the trend generally reversed during continued follow-up, and pretreatment levels were restored.

Conclusions

Treatment of H. pylori infection significantly altered plasma metabolic profiles in the short term, and key metabolites were capable of distinguishing participants with successful vs. failed eradication, but might not substantially affect metabolic regulation in the long term. Several plasma metabolites were differentially associated with the risk of gastric lesion progression among participants with successful or failed eradication.

Electronic Supplementary Material

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References

1

Correa P. Human gastric carcinogenesis: a multistep and multifactorial process – First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 1992; 52: 6735-40.

2

Peek RM, Jr., Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002; 2: 28-37.

3
Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June 1994. IARC Monogr Eval Carcinog Risks Hum. 1994; 61: 1-241.
4

Li WQ, Zhang JY, Ma JL, Li ZX, Zhang L, Zhang Y, et al. Effects of Helicobacter pylori treatment and vitamin and garlic supplementation on gastric cancer incidence and mortality: follow-up of a randomized intervention trial. BMJ. 2019; 366: l5016.

5

Ford AC, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer: systematic review and meta-analysis. Gut. 2020; 69: 2113-21.

6

Nam SY, Park BJ, Nam JH, Kook MC. Effect of Helicobacter pylori eradication and high-density lipoprotein on the risk of de novo gastric cancer development. Gastrointest Endosc. 2019; 90: 448-56.e1.

7

Ganeshan K, Chawla A. Metabolic regulation of immune responses. Annu Rev Immunol. 2014; 32: 609-34.

8

Hotamisligil GS. Foundations of immunometabolism and implications for metabolic health and disease. Immunity. 2017; 47: 406-20.

9

Pavlova NN, Thompson CB. The emerging hallmarks of cancer metabolism. Cell Metab. 2016; 23: 27-47.

10

Faubert B, Solmonson A, DeBerardinis RJ. Metabolic reprogramming and cancer progression. Science. 2020; 368: eaaw5473.

11

Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discov. 2022; 12: 31-46.

12

Martin-Nuñez GM, Cornejo-Pareja I, Clemente-Postigo M, Tinahones FJ. Gut microbiota: the missing link between Helicobacter pylori infection and metabolic disorders? Front Endocrinol. 2021; 12: 639856.

13

Yang YJ, Sheu BS. Metabolic interaction of Helicobacter pylori infection and gut microbiota. Microorganisms. 2016; 4: 15.

14

Huang JY, Sweeney EG, Sigal M, Zhang HC, Remington SJ, Cantrell MA, et al. Chemodetection and destruction of host urea allows Helicobacter pylori to locate the epithelium. Cell Host Microbe. 2015; 18: 147-56.

15

Liu Y, Zhang Z, Wang J, Chen C, Tang X, Zhu J, et al. Metabolic reprogramming results in abnormal glycolysis in gastric cancer: a review. Onco Targets Ther. 2019; 12: 1195-204.

16

Fang LJ, Lin XC, Huang D, Pan TT, Yan XM, Hu WG, et al. 1H NMR-based metabolomics analyses in children with Helicobacter pylori infection and the alteration of serum metabolites after treatment. Microb Pathog. 2020; 147: 104292.

17

Yap TW, Leow AH, Azmi AN, Callahan DL, Perez-Perez GI, Loke MF, et al. Global fecal and plasma metabolic dynamics related to Helicobacter pylori eradication. Front Microbiol. 2017; 8: 536.

18

Orihara T, Wakabayashi H, Nakaya A, Fukuta K, Makimoto S, Naganuma K, et al. Effect of Helicobacter pylori eradication on gastric mucosal phospholipid content and its fatty acid composition. J Gastroenterol Hepatol. 2001; 16: 269-75.

19

Allison KR, Brynildsen MP, Collins JJ. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature. 2011; 473: 216-20.

20

You WC, Blot WJ, Chang YS, Ershow AG, Yang ZT, An Q, et al. Diet and high risk of stomach cancer in Shandong, China. Cancer Res. 1988; 48: 3518-23.

21

You WC, Blot WJ, Li JY, Chang YS, Jin ML, Kneller R, et al. Precancerous gastric lesions in a population at high risk of stomach cancer. Cancer Res. 1993; 53: 1317-21.

22

Huang S, Guo Y, Li ZW, Shui G, Tian H, Li BW, et al. Identification and validation of plasma metabolomic signatures in precancerous gastric lesions that progress to cancer. JAMA Netw Open. 2021; 4: e2114186.

23

Dunn WB, Broadhurst D, Begley P, Zelena E, Francis-McIntyre S, Anderson N, et al. Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc. 2011; 6: 1060-83.

24

Zhang P, Liu J, Xiong B, Zhang C, Kang B, Gao Y, et al. Microbiota from alginate oligosaccharide-dosed mice successfully mitigated small intestinal mucositis. Microbiome. 2020; 8: 112.

25

Koh A, Molinaro A, Ståhlman M, Khan MT, Schmidt C, Mannerås-Holm L, et al. Microbially produced imidazole propionate impairs insulin signaling through mTORC1. Cell. 2018; 175: 947-61.e17.

26

Rao N, Nowak R, Cox C, Rogers T. Classification with the sparse group lasso. IEEE T Signal Proces. 2015; 64: 448-63.

27

Liang KY, Zeger SL. Longitudinal data analysis using generalized linear models. Biometrika. 1986; 73: 13-22.

28

Guo Y, Zhang Y, Gerhard M, Gao JJ, Mejias-Luque R, Zhang L, et al. Effect of Helicobacter pylori on gastrointestinal microbiota: a population-based study in Linqu, a high-risk area of gastric cancer. Gut. 2020; 69: 1598-607.

29

Huang S, Guo Y, Li Z, Zhang Y, Zhou T, You W, et al. A systematic review of metabolomic profiling of gastric cancer and esophageal cancer. Cancer Biol Med. 2020; 17: 181-98.

30

Lagace TA. Phosphatidylcholine: greasing the cholesterol transport machinery. Lipid Insights. 2015; 8: 65-73.

31

Lichtenberger LM, Dial EJ, Ottlecz A, Romero JJ, Lechago J, Fox JG. Attenuation of hydrophobic phospholipid barrier is an early event in Helicobacter felis-induced gastritis in mice. Dig Dis Sci. 1999; 44: 108-15.

32

Nardone G, d’Armiento F, Corso G, Coscione P, Esposito M, Budillon G. Lipids of human gastric mucosa: effect of Helicobacter pylori infection and nonalcoholic cirrhosis. Gastroenterology. 1994; 107: 362-8.

33

Chen EC-H, Ho C-T. Identification of 9-decenoic acid in beer and yeast. J Am Soc Brew Chem. 1981; 39: 70-71.

34

Elahi A, Sabui S, Narasappa NN, Agrawal S, Lambrecht NW, Agrawal A, et al. Biotin deficiency induces Th1- and Th17-mediated proinflammatory responses in human CD4(+) T lymphocytes via activation of the mTOR signaling pathway. J Immunol. 2018; 200: 2563-70.

35

Luzardo-Ocampo I, Campos-Vega R, Gonzalez de Mejia E, Loarca-Piña G. Consumption of a baked corn and bean snack reduced chronic colitis inflammation in CD-1 mice via downregulation of IL-1 receptor, TLR, and TNF-α associated pathways. Food Res Int. 2020; 132: 109097.

36

Boedtkjer E, Pedersen SF. The acidic tumor microenvironment as a driver of cancer. Annu Rev Physiol. 2020; 82: 103-26.

37

Fuchsmann P, Tena Stern M, Münger LH, Pimentel G, Burton KJ, Vionnet N, et al. Nutrivolatilomics of urinary and plasma samples to identify candidate biomarkers after cheese, milk, and soy-based drink intake in healthy humans. J Proteome Res. 2020; 19: 4019-33.

38

Corona G, Cannizzaro R, Miolo G, Caggiari L, De Zorzi M, Repetto O, et al. Use of metabolomics as a complementary omic approach to implement risk criteria for first-degree relatives of gastric cancer patients. Int J Mol Sci. 2018; 19: 750.

39

Lee GB, Lee JC, Moon MH. Plasma lipid profile comparison of five different cancers by nanoflow ultrahigh performance liquid chromatography-tandem mass spectrometry. Anal Chim Acta. 2019; 1063: 117-26.

Cancer Biology & Medicine
Pages 1259-1273
Cite this article:
Wu W, Liu Z, Li Z, et al. Effects of Helicobacter pylori eradication on the profiles of blood metabolites and their associations with the progression of gastric lesions: a prospective follow-up study. Cancer Biology & Medicine, 2022, 19(8): 1259-1273. https://doi.org/10.20892/j.issn.2095-3941.2022.0255

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Received: 07 May 2022
Accepted: 17 June 2022
Published: 29 August 2022
©2022 Cancer Biology & Medicine.

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