Research progress on the relationship between non-erosive gastroesophageal reflux disease and gastrointestinal flora_West China Medical Journal

Authors：

FENG Caiju ¹ , TANG Shilin ¹ , XU Zhihong ¹ , ZHANG Xiumei ¹ , XIONG Xin ² ,  HE Suyu ^1,2

1. Graduate School of Zunyi Medical University, Zunyi, Guizhou 563000, P. R. China;
2. The Fourth Department of Digestive Disease Center, Suining Central Hospital, Suining, Sichuan 629000, P. R. China;

Corresponding?author：

HE Suyu, Email: hesuyu2009@163.com

Keywords：

Non-erosive gastroesophageal reflux disease; gastrointestinal flora; Helicobacter pylori

DOI：

10.7507/1002-0179.202306190

Video：

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Abstract Full text Figures/Tables Video References Cited by

Non-erosive gastroesophageal reflux disease (NERD) refers to a disease that has typical gastroesophageal reflux symptoms but lacks endoscopic esophageal mucosal damage. Its exact pathogenesis remains unclear. Studies have shown that the occurrence and development of NERD may be related to the gastrointestinal flora. The digestive tract flora can directly or indirectly participate in the occurrence and development of NERD by affecting the body’s immune, metabolic, neurological and other functions. In order to further clarify the possible correlation between NERD and gastrointestinal flora, this article reviews the research progress on the correlation between NERD and gastrointestinal flora, with a view to providing new ideas for the diagnosis and treatment of NERD.

Citation： FENG Caiju, TANG Shilin, XU Zhihong, ZHANG Xiumei, XIONG Xin, HE Suyu. Research progress on the relationship between non-erosive gastroesophageal reflux disease and gastrointestinal flora. West China Medical Journal, 2023, 38(10): 1595-1600. doi: 10.7507/1002-0179.202306190 Copy

1.	Maret-Ouda J, Markar SR, Lagergren J. Gastroesophageal Reflux Disease. JAMA, 2020, 324(24): 2565.
2.	Eusebi LH, Ratnakumaran R, Yuan Y, et al. Global prevalence of, and risk factors for, gastro-oesophageal reflux symptoms: a meta-analysis. Gut, 2018, 67(3): 430-440.
3.	Nirwan JS, Hasan SS, Babar ZU, et al. Global prevalence and risk factors of gastro-oesophageal reflux disease (GORD): systematic review with meta-analysis. Sci Rep, 2020, 10(1): 5814.
4.	Fass R. Gastroesophageal reflux disease. N Engl J Med, 2022, 387(13): 1207-1216.
5.	Zheng Z, Shang Y, Wang N, et al. Current advancement on the dynamic mechanism of gastroesophageal reflux disease. Int J Biol Sci, 2021, 17(15): 4154-4164.
6.	Gillespie MR, Rai V, Agrawal S, et al. The role of microbiota in the pathogenesis of esophageal adenocarcinoma. Biology (Basel), 2021, 10(8): 697.
7.	Zhou J, Shrestha P, Qiu Z, et al. Distinct microbiota dysbiosis in patients with non-erosive reflux disease and esophageal adenocarcinoma. J Clin Med, 2020, 9(7): 2162.
8.	Sugihartono T, Fauzia KA, Miftahussurur M, et al. Analysis of gastric microbiota and Helicobacter pylori infection in gastroesophageal reflux disease. Gut Pathog, 2022, 14(1): 38.
9.	Gao L, Xu T, Huang G, et al. Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell, 2018, 9(5): 488-500.
10.	Lee YH, Chung SW, Auh QS, et al. Progress in oral microbiome related to oral and systemic diseases: an update. Diagnostics (Basel), 2021, 11(7): 1283.
11.	Kawar N, Park SG, Schwartz JL, et al. Salivary microbiome with gastroesophageal reflux disease and treatment. Sci Rep, 2021, 11(1): 188.
12.	Ziganshina EE, Sagitov II, Akhmetova RF, et al. Comparison of the microbiota and inorganic anion content in the saliva of patients with gastroesophageal reflux disease and gastroesophageal reflux disease-free individuals. Biomed Res Int, 2020, 2020: 2681791.
13.	Koeda M, Tanabe T, Kitasako Y, et al. Saliva secretion is reduced in proton pump inhibitor-responsive non-erosive reflux disease patients. Esophagus, 2021, 18(4): 900-907.
14.	Nascimento MM. Approaches to modulate biofilm ecology. Dent Clin North Am, 2019, 63(4): 581-594.
15.	Wang YJ, Lang XQ, Wu D, et al. Salivary pepsin as an intrinsic marker for diagnosis of sub-types of gastroesophageal reflux disease and gastroesophageal reflux disease-related disorders. J Neurogastroenterol Motil, 2020, 26(1): 74-84.
16.	蔣興宇, 趙霞, 鄒凌云, 等. 適度運動對人體腸道菌群結構的影響. 第三軍醫大學學報, 2017, 39(18): 1824-1831.
17.	Pignatelli P, Fabietti G, Ricci A, et al. How periodontal disease and presence of nitric oxide reducing oral bacteria can affect blood pressure. Int J Mol Sci, 2020, 21(20): 7538.
18.	Yang L, Francois F, Pei Z. Molecular pathways: pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res, 2012, 18(8): 2138-2144.
19.	Snider EJ, Compres G, Freedberg DE, et al. Barrett’s esophagus is associated with a distinct oral microbiome. Clin Transl Gastroenterol, 2018, 9(3): 135.
20.	Nardone G, Compare D, Rocco A. A microbiota-centric view of diseases of the upper gastrointestinal tract. Lancet Gastroenterol Hepatol, 2017, 2(4): 298-312.
21.	D’Souza SM, Houston K, Keenan L, et al. Role of microbial dysbiosis in the pathogenesis of esophageal mucosal disease: a paradigm shift from acid to bacteria?. World J Gastroenterol, 2021, 27(18): 2054-2072.
22.	Park CH, Seo SI, Kim JS, et al. Treatment of non-erosive reflux disease and dynamics of the esophageal microbiome: a prospective multicenter study. Sci Rep, 2020, 10(1): 15154.
23.	Pei Z, Bini EJ, Yang L, et al. Bacterial biota in the human distal esophagus. Proc Natl Acad Sci U S A, 2004, 101(12): 4250-4255.
24.	Sun QH, Zhang J, Shi YY, et al. Microbiome changes in the gastric mucosa and gastric juice in different histological stages of Helicobacter pylori-negative gastric cancers. World J Gastroenterol, 2022, 28(3): 365-380.
25.	Guccione C, Yadlapati R, Shah S, et al. Challenges in determining the role of microbiome evolution in Barrett’s esophagus and progression to esophageal adenocarcinoma. Microorganisms, 2021, 9(10): 2003.
26.	柳安琪, 陳汶. 食管微生物與食管相關疾病研究進展. 中華腫瘤雜志, 2019, 41(8): 561-564.
27.	Zou Q, Feng L, Cai X, et al. Esophageal microflora in esophageal diseases. Front Cell Infect Microbiol, 2023, 13: 1145791.
28.	Barona I, Fagundes DS, Gonzalo S, et al. Role of TLR4 and MAPK in the local effect of LPS on intestinal contractility. J Pharm Pharmacol, 2011, 63(5): 657-662.
29.	Lv J, Guo L, Liu JJ, et al. Alteration of the esophageal microbiota in Barrett’s esophagus and esophageal adenocarcinoma. World J Gastroenterol, 2019, 25(18): 2149-2161.
30.	Crouzet L, Gaultier E, Del’Homme C, et al. The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil, 2013, 25(4): e272-e282.
31.	Dimidi E, Christodoulides S, Scott SM, et al. Mechanisms of action of probiotics and the gastrointestinal microbiota on gut motility and constipation. Adv Nutr, 2017, 8(3): 484-494.
32.	Ye Y, Yin Y, Huh SY, et al. Epidemiology, etiology, and treatment of gastroparesis: real-world evidence from a large US national claims database. Gastroenterology, 2022, 162(1): 109-121.e5.
33.	Hunt RH, Yaghoobi M. The esophageal and gastric microbiome in health and disease. Gastroenterol Clin North Am, 2017, 46(1): 121-141.
34.	Zhang S, Shi D, Li M, et al. The relationship between gastric microbiota and gastric disease. Scand J Gastroenterol, 2019, 54(4): 391-396.
35.	Rajilic-Stojanovic M, Figueiredo C, Smet A, et al. Systematic review: gastric microbiota in health and disease. Aliment Pharmacol Ther, 2020, 51(6): 582-602.
36.	Hao Y, Karaoz U, Yang L, et al. Progressive dysbiosis of human orodigestive microbiota along the sequence of gastroesophageal reflux, Barrett’s esophagus and esophageal adenocarcinoma. Int J Cancer, 2022, 151(10): 1703-1716.
37.	Mladenova I. Clinical relevance of Helicobacter pylori infection. J Clin Med, 2021, 10(16): 3473.
38.	Li M, Sun Y, Yang J, et al. Time trends and other sources of variation in Helicobacter pylori infection in mainland China: a systematic review and meta-analysis. Helicobacter, 2020, 25(5): e12729.
39.	Chen TH, Cheng HT, Yeh CT. Epidemiology changes in peptic ulcer diseases 18 years apart explored from the genetic aspects of Helicobacter pylori. Transl Res, 2021, 232: 115-120.
40.	Miftahussurur M, Doohan D, Nusi IA, et al. Gastroesophageal reflux disease in an area with low Helicobacter pylori infection prevalence. PLoS One, 2018, 13(11): e0205644.
41.	Quach DT, Pham QTT, Tran TLT, et al. Clinical characteristics and risk factors of gastroesophageal reflux disease in Vietnamese patients with upper gastrointestinal symptoms undergoing esophagogastroduodenoscopy. JGH Open, 2021, 5(5): 580-584.
42.	郭薇薇, 陳玲, 繆鑫, 等. 幽門螺桿菌對胃食管反流病影響的 Meta 分析. 胃腸病學和肝病學雜志, 2017, 26(10): 1133-1137.
43.	朱曼, 張倩, 金珍婧. 幽門螺桿菌感染與食管疾病相關性的研究進展. 國際老年醫學雜志, 2020, 41(1): 57-61.
44.	Dore MP, Pes GM, Bassotti G, et al. Risk factors for erosive and non-erosive gastroesophageal reflux disease and Barrett’s esophagus in Nothern Sardinia. Scand J Gastroenterol, 2016, 51(11): 1281-1287.
45.	Zhao T, Liu F, Li Y. Effects of Helicobacter pylori eradication on esophageal motility, esophageal acid exposure, and gastroesophageal reflux disease symptoms. Front Cell Infect Microbiol, 2023, 13: 1082620.
46.	徐志洪, 張秀梅, 熊鑫, 等. Barrett 食管與胃腸道微生態研究進展. 華西醫學, 2022, 37(10): 1594-1600.
47.	He C, Yang Z, Lu NH. Helicobacter pylori infection and diabetes: is it a myth or fact?. World J Gastroenterol, 2014, 20(16): 4607-4617.
48.	Manes G, Mosca S, Laccetti M, et al. Helicobacter pylori infection, pattern of gastritis, and symptoms in erosive and nonerosive gastroesophageal reflux disease. Scand J Gastroenterol, 1999, 34(7): 658-662.
49.	Yucel O. Interactions between Helicobacter pylori and gastroesophageal reflux disease. Esophagus, 2019, 16(1): 52-62.
50.	Brawner KM, Kumar R, Serrano CA, et al. Helicobacter pylori infection is associated with an altered gastric microbiota in children. Mucosal Immunol, 2017, 10(5): 1169-1177.
51.	Liu B, Dong J, Wang S, et al. Helicobacter pylori causes delayed gastric emptying by decreasing interstitial cells of Cajal. Exp Ther Med, 2021, 22(1): 663.
52.	Niknam R, Lankarani KB, Moghadami M, et al. The association between Helicobacter pylori infection and erosive gastroesophageal reflux disease; a cross-sectional study. BMC Infect Dis, 2022, 22(1): 267.
53.	Mungan Z, P?narba?? ?im?ek B. Gastroesophageal reflux disease and the relationship with Helicobacter pylori. Turk J Gastroenterol, 2017, 28(Suppl 1): S61-S67.
54.	Zaman C, Osaki T, Hanawa T, et al. Analysis of the microbial ecology between Helicobacter pylori and the gastric microbiota of Mongolian gerbils. J Med Microbiol, 2014, 63(Pt 1): 129-137.
55.	艾合麥提·喀斯木, 買買提·依斯熱依力, 克力木·阿布都熱依木. 腸道菌群在胃食管反流病發病中的作用及相關性研究進展. 中國醫師雜志, 2022, 24(8): 1273-1276.
56.	Singh R, Zogg H, Wei L, et al. Gut microbial dysbiosis in the pathogenesis of gastrointestinal dysmotility and metabolic disorders. J Neurogastroenterol Motil, 2021, 27(1): 19-34.
57.	Yang F, Xie XH, Li X, et al. Analysis of psychological and gut microbiome characteristics in patients with non-erosive reflux disease. Front Psychiatry, 2022, 12: 741049.
58.	王煜姣, 賈慶玲, 李莉, 等. 腸道菌群與胃腸動力關系的研究進展. 世界華人消化雜志, 2021, 29(17): 1020-1025.
59.	Khan Z, Alastal Y, Khan MA, et al. On-demand therapy with proton pump inhibitors for maintenance treatment of nonerosive reflux disease or mild erosive esophagitis: a systematic review and meta-analysis. Gastroenterol Res Pract, 2018, 2018: 6417526.
60.	Yadlapati R, DeLay K. Proton pump inhibitor-refractory gastroesophageal reflux disease. Med Clin North Am, 2019, 103(1): 15-27.
61.	Kiecka A, Szczepanik M. Proton pump inhibitor-induced gut dysbiosis and immunomodulation: current knowledge and potential restoration by probiotics. Pharmacol Rep, 2023, 75(4): 791-804.
62.	Vereecke L, Elewaut D. Spondyloarthropathies: ruminococcus on the horizon in arthritic disease. Nat Rev Rheumatol, 2017, 13(10): 574-576.
63.	Imhann F, Bonder MJ, Vich Vila A, et al. Proton pump inhibitors affect the gut microbiome. Gut, 2016, 65(5): 740-748.
64.	Haworth JJ, Boyle N, Vales A, et al. The prevalence of intestinal dysbiosis in patients referred for antireflux surgery. Surg Endosc, 2021, 35(12): 7112-7119.
65.	Suri J, Kataria R, Malik Z, et al. Elevated methane levels in small intestinal bacterial overgrowth suggests delayed small bowel and colonic transit. Medicine (Baltimore), 2018, 97(21): e10554.

1. Maret-Ouda J, Markar SR, Lagergren J. Gastroesophageal Reflux Disease. JAMA, 2020, 324(24): 2565.
2. Eusebi LH, Ratnakumaran R, Yuan Y, et al. Global prevalence of, and risk factors for, gastro-oesophageal reflux symptoms: a meta-analysis. Gut, 2018, 67(3): 430-440.
3. Nirwan JS, Hasan SS, Babar ZU, et al. Global prevalence and risk factors of gastro-oesophageal reflux disease (GORD): systematic review with meta-analysis. Sci Rep, 2020, 10(1): 5814.
4. Fass R. Gastroesophageal reflux disease. N Engl J Med, 2022, 387(13): 1207-1216.
5. Zheng Z, Shang Y, Wang N, et al. Current advancement on the dynamic mechanism of gastroesophageal reflux disease. Int J Biol Sci, 2021, 17(15): 4154-4164.
6. Gillespie MR, Rai V, Agrawal S, et al. The role of microbiota in the pathogenesis of esophageal adenocarcinoma. Biology (Basel), 2021, 10(8): 697.
7. Zhou J, Shrestha P, Qiu Z, et al. Distinct microbiota dysbiosis in patients with non-erosive reflux disease and esophageal adenocarcinoma. J Clin Med, 2020, 9(7): 2162.
8. Sugihartono T, Fauzia KA, Miftahussurur M, et al. Analysis of gastric microbiota and Helicobacter pylori infection in gastroesophageal reflux disease. Gut Pathog, 2022, 14(1): 38.
9. Gao L, Xu T, Huang G, et al. Oral microbiomes: more and more importance in oral cavity and whole body. Protein Cell, 2018, 9(5): 488-500.
10. Lee YH, Chung SW, Auh QS, et al. Progress in oral microbiome related to oral and systemic diseases: an update. Diagnostics (Basel), 2021, 11(7): 1283.
11. Kawar N, Park SG, Schwartz JL, et al. Salivary microbiome with gastroesophageal reflux disease and treatment. Sci Rep, 2021, 11(1): 188.
12. Ziganshina EE, Sagitov II, Akhmetova RF, et al. Comparison of the microbiota and inorganic anion content in the saliva of patients with gastroesophageal reflux disease and gastroesophageal reflux disease-free individuals. Biomed Res Int, 2020, 2020: 2681791.
13. Koeda M, Tanabe T, Kitasako Y, et al. Saliva secretion is reduced in proton pump inhibitor-responsive non-erosive reflux disease patients. Esophagus, 2021, 18(4): 900-907.
14. Nascimento MM. Approaches to modulate biofilm ecology. Dent Clin North Am, 2019, 63(4): 581-594.
15. Wang YJ, Lang XQ, Wu D, et al. Salivary pepsin as an intrinsic marker for diagnosis of sub-types of gastroesophageal reflux disease and gastroesophageal reflux disease-related disorders. J Neurogastroenterol Motil, 2020, 26(1): 74-84.
16. 蔣興宇, 趙霞, 鄒凌云, 等. 適度運動對人體腸道菌群結構的影響. 第三軍醫大學學報, 2017, 39(18): 1824-1831.
17. Pignatelli P, Fabietti G, Ricci A, et al. How periodontal disease and presence of nitric oxide reducing oral bacteria can affect blood pressure. Int J Mol Sci, 2020, 21(20): 7538.
18. Yang L, Francois F, Pei Z. Molecular pathways: pathogenesis and clinical implications of microbiome alteration in esophagitis and Barrett esophagus. Clin Cancer Res, 2012, 18(8): 2138-2144.
19. Snider EJ, Compres G, Freedberg DE, et al. Barrett’s esophagus is associated with a distinct oral microbiome. Clin Transl Gastroenterol, 2018, 9(3): 135.
20. Nardone G, Compare D, Rocco A. A microbiota-centric view of diseases of the upper gastrointestinal tract. Lancet Gastroenterol Hepatol, 2017, 2(4): 298-312.
21. D’Souza SM, Houston K, Keenan L, et al. Role of microbial dysbiosis in the pathogenesis of esophageal mucosal disease: a paradigm shift from acid to bacteria?. World J Gastroenterol, 2021, 27(18): 2054-2072.
22. Park CH, Seo SI, Kim JS, et al. Treatment of non-erosive reflux disease and dynamics of the esophageal microbiome: a prospective multicenter study. Sci Rep, 2020, 10(1): 15154.
23. Pei Z, Bini EJ, Yang L, et al. Bacterial biota in the human distal esophagus. Proc Natl Acad Sci U S A, 2004, 101(12): 4250-4255.
24. Sun QH, Zhang J, Shi YY, et al. Microbiome changes in the gastric mucosa and gastric juice in different histological stages of Helicobacter pylori-negative gastric cancers. World J Gastroenterol, 2022, 28(3): 365-380.
25. Guccione C, Yadlapati R, Shah S, et al. Challenges in determining the role of microbiome evolution in Barrett’s esophagus and progression to esophageal adenocarcinoma. Microorganisms, 2021, 9(10): 2003.
26. 柳安琪, 陳汶. 食管微生物與食管相關疾病研究進展. 中華腫瘤雜志, 2019, 41(8): 561-564.
27. Zou Q, Feng L, Cai X, et al. Esophageal microflora in esophageal diseases. Front Cell Infect Microbiol, 2023, 13: 1145791.
28. Barona I, Fagundes DS, Gonzalo S, et al. Role of TLR4 and MAPK in the local effect of LPS on intestinal contractility. J Pharm Pharmacol, 2011, 63(5): 657-662.
29. Lv J, Guo L, Liu JJ, et al. Alteration of the esophageal microbiota in Barrett’s esophagus and esophageal adenocarcinoma. World J Gastroenterol, 2019, 25(18): 2149-2161.
30. Crouzet L, Gaultier E, Del’Homme C, et al. The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil, 2013, 25(4): e272-e282.
31. Dimidi E, Christodoulides S, Scott SM, et al. Mechanisms of action of probiotics and the gastrointestinal microbiota on gut motility and constipation. Adv Nutr, 2017, 8(3): 484-494.
32. Ye Y, Yin Y, Huh SY, et al. Epidemiology, etiology, and treatment of gastroparesis: real-world evidence from a large US national claims database. Gastroenterology, 2022, 162(1): 109-121.e5.
33. Hunt RH, Yaghoobi M. The esophageal and gastric microbiome in health and disease. Gastroenterol Clin North Am, 2017, 46(1): 121-141.
34. Zhang S, Shi D, Li M, et al. The relationship between gastric microbiota and gastric disease. Scand J Gastroenterol, 2019, 54(4): 391-396.
35. Rajilic-Stojanovic M, Figueiredo C, Smet A, et al. Systematic review: gastric microbiota in health and disease. Aliment Pharmacol Ther, 2020, 51(6): 582-602.
36. Hao Y, Karaoz U, Yang L, et al. Progressive dysbiosis of human orodigestive microbiota along the sequence of gastroesophageal reflux, Barrett’s esophagus and esophageal adenocarcinoma. Int J Cancer, 2022, 151(10): 1703-1716.
37. Mladenova I. Clinical relevance of Helicobacter pylori infection. J Clin Med, 2021, 10(16): 3473.
38. Li M, Sun Y, Yang J, et al. Time trends and other sources of variation in Helicobacter pylori infection in mainland China: a systematic review and meta-analysis. Helicobacter, 2020, 25(5): e12729.
39. Chen TH, Cheng HT, Yeh CT. Epidemiology changes in peptic ulcer diseases 18 years apart explored from the genetic aspects of Helicobacter pylori. Transl Res, 2021, 232: 115-120.
40. Miftahussurur M, Doohan D, Nusi IA, et al. Gastroesophageal reflux disease in an area with low Helicobacter pylori infection prevalence. PLoS One, 2018, 13(11): e0205644.
41. Quach DT, Pham QTT, Tran TLT, et al. Clinical characteristics and risk factors of gastroesophageal reflux disease in Vietnamese patients with upper gastrointestinal symptoms undergoing esophagogastroduodenoscopy. JGH Open, 2021, 5(5): 580-584.
42. 郭薇薇, 陳玲, 繆鑫, 等. 幽門螺桿菌對胃食管反流病影響的 Meta 分析. 胃腸病學和肝病學雜志, 2017, 26(10): 1133-1137.
43. 朱曼, 張倩, 金珍婧. 幽門螺桿菌感染與食管疾病相關性的研究進展. 國際老年醫學雜志, 2020, 41(1): 57-61.
44. Dore MP, Pes GM, Bassotti G, et al. Risk factors for erosive and non-erosive gastroesophageal reflux disease and Barrett’s esophagus in Nothern Sardinia. Scand J Gastroenterol, 2016, 51(11): 1281-1287.
45. Zhao T, Liu F, Li Y. Effects of Helicobacter pylori eradication on esophageal motility, esophageal acid exposure, and gastroesophageal reflux disease symptoms. Front Cell Infect Microbiol, 2023, 13: 1082620.
46. 徐志洪, 張秀梅, 熊鑫, 等. Barrett 食管與胃腸道微生態研究進展. 華西醫學, 2022, 37(10): 1594-1600.
47. He C, Yang Z, Lu NH. Helicobacter pylori infection and diabetes: is it a myth or fact?. World J Gastroenterol, 2014, 20(16): 4607-4617.
48. Manes G, Mosca S, Laccetti M, et al. Helicobacter pylori infection, pattern of gastritis, and symptoms in erosive and nonerosive gastroesophageal reflux disease. Scand J Gastroenterol, 1999, 34(7): 658-662.
49. Yucel O. Interactions between Helicobacter pylori and gastroesophageal reflux disease. Esophagus, 2019, 16(1): 52-62.
50. Brawner KM, Kumar R, Serrano CA, et al. Helicobacter pylori infection is associated with an altered gastric microbiota in children. Mucosal Immunol, 2017, 10(5): 1169-1177.
51. Liu B, Dong J, Wang S, et al. Helicobacter pylori causes delayed gastric emptying by decreasing interstitial cells of Cajal. Exp Ther Med, 2021, 22(1): 663.
52. Niknam R, Lankarani KB, Moghadami M, et al. The association between Helicobacter pylori infection and erosive gastroesophageal reflux disease; a cross-sectional study. BMC Infect Dis, 2022, 22(1): 267.
53. Mungan Z, P?narba?? ?im?ek B. Gastroesophageal reflux disease and the relationship with Helicobacter pylori. Turk J Gastroenterol, 2017, 28(Suppl 1): S61-S67.
54. Zaman C, Osaki T, Hanawa T, et al. Analysis of the microbial ecology between Helicobacter pylori and the gastric microbiota of Mongolian gerbils. J Med Microbiol, 2014, 63(Pt 1): 129-137.
55. 艾合麥提·喀斯木, 買買提·依斯熱依力, 克力木·阿布都熱依木. 腸道菌群在胃食管反流病發病中的作用及相關性研究進展. 中國醫師雜志, 2022, 24(8): 1273-1276.
56. Singh R, Zogg H, Wei L, et al. Gut microbial dysbiosis in the pathogenesis of gastrointestinal dysmotility and metabolic disorders. J Neurogastroenterol Motil, 2021, 27(1): 19-34.
57. Yang F, Xie XH, Li X, et al. Analysis of psychological and gut microbiome characteristics in patients with non-erosive reflux disease. Front Psychiatry, 2022, 12: 741049.
58. 王煜姣, 賈慶玲, 李莉, 等. 腸道菌群與胃腸動力關系的研究進展. 世界華人消化雜志, 2021, 29(17): 1020-1025.
59. Khan Z, Alastal Y, Khan MA, et al. On-demand therapy with proton pump inhibitors for maintenance treatment of nonerosive reflux disease or mild erosive esophagitis: a systematic review and meta-analysis. Gastroenterol Res Pract, 2018, 2018: 6417526.
60. Yadlapati R, DeLay K. Proton pump inhibitor-refractory gastroesophageal reflux disease. Med Clin North Am, 2019, 103(1): 15-27.
61. Kiecka A, Szczepanik M. Proton pump inhibitor-induced gut dysbiosis and immunomodulation: current knowledge and potential restoration by probiotics. Pharmacol Rep, 2023, 75(4): 791-804.
62. Vereecke L, Elewaut D. Spondyloarthropathies: ruminococcus on the horizon in arthritic disease. Nat Rev Rheumatol, 2017, 13(10): 574-576.
63. Imhann F, Bonder MJ, Vich Vila A, et al. Proton pump inhibitors affect the gut microbiome. Gut, 2016, 65(5): 740-748.
64. Haworth JJ, Boyle N, Vales A, et al. The prevalence of intestinal dysbiosis in patients referred for antireflux surgery. Surg Endosc, 2021, 35(12): 7112-7119.
65. Suri J, Kataria R, Malik Z, et al. Elevated methane levels in small intestinal bacterial overgrowth suggests delayed small bowel and colonic transit. Medicine (Baltimore), 2018, 97(21): e10554.

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