Application value of probiotics in regulating proton pump inhibitor-induced gastrointestinal microecological disorders_West China Medical Journal

Authors：

ZHAO Handong ¹ ,  ZHAN Li ² , YANG Xiaoping ¹ , ZHAO Xin ¹ , ZHAO Xinyan ¹

1. The First Clinical Medical College of Gansu University of Chinese Medicine (Gansu Provincial Hospital), Lanzhou, Gansu 730000, P. R. China;
2. Department of Gastroenterology, Gansu Provincial Hospital, Lanzhou, Gansu 730000, P. R. China;

Corresponding author：

ZHAN Li, Email: zhanlilanzhou@163.com

Keywords：

Proton pump inhibitor; digestive tract microecology; probiotics; intestinal flora

DOI：

10.7507/1002-0179.202106273

Video：

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Abstract Full text Figures/Tables Video References Cited by

Proton pump inhibitors (PPIs) are widely used in digestive system diseases, but long-term use of PPI may cause Clostridium difficile infection, small intestinal bacterial overgrowth, spontaneous bacterial peritonitis and gastrointestinal barrier dysfunction. Probiotics can improve the digestive tract microecological disorder caused by the application of PPI by inhibiting the colonization of bacteria in the intestinal tract, regulating the body’s immunity, reducing the pH value of the intestinal tract, and enhancing the barrier function of the intestinal mucosa. This article elaborates on the influence of PPI on the microecology of the digestive tract and the regulation of probiotics on the microecology of the digestive tract, aiming to provide some ideas for the digestive tract microecological disorders caused by the application of PPI in clinical practice and their intervention strategies.

Citation： ZHAO Handong, ZHAN Li, YANG Xiaoping, ZHAO Xin, ZHAO Xinyan. Application value of probiotics in regulating proton pump inhibitor-induced gastrointestinal microecological disorders. West China Medical Journal, 2022, 37(1): 125-130. doi: 10.7507/1002-0179.202106273 Copy

1.	Sung JJ, Chiu PW, Chan FKL, et al. Asia-Pacific working group consensus on non-variceal upper gastrointestinal bleeding: an update 2018. Gut, 2018, 67(10): 1757-1768.
2.	刘文忠, 谢勇, 陆红, 等. 第五次全国幽门螺杆菌感染处理共识报告. 中华消化杂志, 2017, 37(6): 364-378.
3.	中华医学会消化病学分会. 2020年中国胃食管反流病专家共识. 中华消化杂志, 2020, 40(10): 649-663.
4.	Trifan A, Stanciu C, Girleanu I, et al. Proton pump inhibitors therapy and risk of Clostridium difficile infection: systematic review and meta-analysis. World J Gastroenterol, 2017, 23(35): 6500-6515.
5.	Franco DL, Disbrow MB, Kahn A, et al. Duodenal aspirates for small intestine bacterial overgrowth: yield, PPIs, and outcomes after treatment at a tertiary academic medical center. Gastroenterol Res Pract, 2015, 2015: 971582.
6.	Dam G, Vilstrup H, Watson H, et al. Proton pump inhibitors as a risk factor for hepatic encephalopathy and spontaneous bacterial peritonitis in patients with cirrhosis with ascites. Hepatology, 2016, 64(4): 1265-1272.
7.	Zheng YM, Chen XY, Cai JY, et al. Washed microbiota transplantation reduces proton pump inhibitor dependency in nonerosive reflux disease. World J Gastroenterol, 2021, 27(6): 513-522.
8.	Hungin APS, Mitchell CR, Whorwell P, et al. Systematic review: probiotics in the management of lower gastrointestinal symptoms - an updated evidence-based international consensus. Aliment Pharmacol Ther, 2018, 47(8): 1054-1070.
9.	Kim GH. Proton pump inhibitor-related gastric mucosal changes. Gut Liver, 2021, 15(5): 646-652.
10.	Savarino V, Marabotto E, Zentilin P, et al. The appropriate use of proton-pump inhibitors. Minerva Med, 2018, 109(5): 386-399.
11.	Ward RM, Kearns GL. Proton pump inhibitors in pediatrics: mechanism of action, pharmacokinetics, pharmacogenetics, and pharmacodynamics. Paediatr Drugs, 2013, 15(2): 119-131.
12.	Clooney AG, Bernstein CN, Leslie WD, et al. A comparison of the gut microbiome between long-term users and non-users of proton pump inhibitors. Aliment Pharmacol Ther, 2016, 43(9): 974-984.
13.	朱苗苗, 李慧兰, 罗佳, 等. 质子泵抑制剂的使用与艰难梭菌感染风险相关性的Meta分析. 中国循证医学杂志, 2016, 16(3): 278-285.
14.	McDonald EG, Milligan J, Frenette C, et al. Continuous proton pump inhibitor therapy and the associated risk of recurrent Clostridium difficile infection. JAMA Intern Med, 2015, 175(5): 784-791.
15.	Massey BT, Wald A. Small intestinal bacterial overgrowth syndrome: a guide for the appropriate use of breath testing. Dig Dis Sci, 2021, 66(2): 338-347.
16.	张茹, 李园, 马金霞, 等. 长期维持质子泵抑制剂治疗对老年人小肠细菌过度生长的影响分析. 中华内科杂志, 2020, 59(9): 706-710.
17.	Giamarellos-Bourboulis EJ, Pyleris E, Barbatzas C, et al. Small intestinal bacterial overgrowth is associated with irritable bowel syndrome and is independent of proton pump inhibitor usage. BMC Gastroenterol, 2016, 16(1): 67.
18.	Su T, Lai S, Lee A, et al. Meta-analysis: proton pump inhibitors moderately increase the risk of small intestinal bacterial overgrowth. J Gastroenterol, 2018, 53(1): 27-36.
19.	Lo WK, Chan WW. Proton pump inhibitor use and the risk of small intestinal bacterial overgrowth: a meta-analysis. Clin Gastroenterol Hepatol, 2013, 11(5): 483-490.
20.	王洪艳, 孙士东, 毕英杰, 等. 长期使用质子泵抑制剂与小肠细菌过度生长的关系研究. 胃肠病学和肝病学杂志, 2016, 25(11): 1302-1304.
21.	Tsuda A, Suda W, Morita H, et al. Influence of proton-pump inhibitors on the luminal microbiota in the gastrointestinal tract. Clin Transl Gastroenterol, 2015, 6(6): e89.
22.	Chen X, Xu J, Su Y, et al. Effects of intravenous infusion with sodium butyrate on colonic microbiota, intestinal development- and mucosal immune-related gene expression in normal growing pigs. Front Microbiol, 2018, 9: 1652.
23.	Freedberg DE, Lamousé-Smith ES, Lightdale JR, et al. Use of acid suppression medication is associated with risk for C. difficile infection in infants and children:a population-based study. Clin Infect Dis, 2015, 61(6): 912-917.
24.	张旭东, 庄伟清, 陈代杰, 等. 双歧杆菌与消化系统疾病的关系. 中国微生态学杂志, 2021, 33(1): 104-111.
25.	韦炜, 洪依萍. 肝硬化门静脉高压相关并发症的防治原则. 临床肝胆病杂志, 2021, 37(1): 22-25.
26.	Yu T, Tang Y, Jiang L, et al. Proton pump inhibitor therapy and its association with spontaneous bacterial peritonitis incidence and mortality: a meta-analysis. Dig Liver Dis, 2016, 48(4): 353-359.
27.	Elzouki AN, Neffati N, Rasoul FA, et al. Increased risk of spontaneous bacterial peritonitis in cirrhotic patients using proton pump inhibitors. GE Port J Gastroenterol, 2019, 26(2): 83-89.
28.	Naito Y, Kashiwagi K, Takagi T, et al. Intestinal dysbiosis secondary to proton-pump inhibitor use. Digestion, 2018, 97(2): 195-204.
29.	van Vlerken LG, Huisman EJ, van Hoek B, et al. Bacterial infections in cirrhosis: role of proton pump inhibitors and intestinal permeability. Eur J Clin Invest, 2012, 42(7): 760-767.
30.	El Chemaly A, Nunes P, Jimaja W, et al. Hv1 proton channels differentially regulate the pH of neutrophil and macrophage phagosomes by sustaining the production of phagosomal ROS that inhibit the delivery of vacuolar ATPases. J Leukoc Biol, 2014, 95(5): 827-839.
31.	Terg R, Casciato P, Garbe C, et al. Proton pump inhibitor therapy does not increase the incidence of spontaneous bacterial peritonitis in cirrhosis: a multicenter prospective study. J Hepatol, 2015, 62(5): 1056-1060.
32.	Reid G, Food and Agricultural Organization of the United Nation and the WHO. The importance of guidelines in the development and application of probiotics. Curr Pharm Des, 2005, 11(1): 11-16.
33.	毛晓丽, 文煜, 费龙. 益生菌辅助埃索美拉唑镁四联疗法对幽门螺杆菌阳性十二指肠溃疡患者肠道菌群分布及血清IFN-γ、IL-10的调节作用. 中国微生态学杂志, 2020, 32(9): 1069-1073.
34.	Pinto-Sanchez MI, Hall GB, Ghajar K, et al. Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology, 2017, 153(2): 448-459.e8.
35.	Marlicz W, Wunsch E, Mydlowska M, et al. The effect of short term treatment with probiotic VSL#3 on various clinical and biochemical parameters in patients with liver cirrhosis. J Physiol Pharmacol, 2016, 67(6): 867-877.
36.	Guo Q, Goldenberg JZ, Humphrey C, et al. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev, 2019, 4(4): CD004827.
37.	Bliss ES, Whiteside E. The gut-brain axis, the human gut microbiota and their integration in the development of obesity. Front Physiol, 2018, 9: 900.
38.	Tai N, Wong FS, Wen L. The role of gut microbiota in the development of type 1, type 2 diabetes mellitus and obesity. Rev Endocr Metab Disord, 2015, 16(1): 55-65.
39.	Eslami M, Yousefi B, Kokhaei P, et al. Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol, 2019, 234(10): 17127-17143.
40.	Sotoudegan F, Daniali M, Hassani S, et al. Reappraisal of probiotics’ safety in human. Food Chem Toxicol, 2019, 129: 22-29.
41.	陈爱方, 田霞, 韩峥, 等. 质子泵抑制剂与小肠细菌过度生长的相关性及双歧杆菌三联活菌胶囊疗效观察. 临床消化病杂志, 2019, 31(3): 159-162.
42.	Belei O, Olariu L, Dobrescu A, et al. Is it useful to administer probiotics together with proton pump inhibitors in children with gastroesophageal reflux?. J Neurogastroenterol Motil, 2018, 24(1): 51-57.
43.	王松, 肖丹, 陈兰, 等. 曲美布汀联合质子泵抑制剂以及益生菌对胃食管反流病患者临床疗效及肠道菌群的影响. 临床消化病杂志, 2019, 31(6): 349-353.
44.	Liang S, Xu L, Zhang D, et al. Effect of probiotics on small intestinal bacterial overgrowth in patients with gastric and colorectal cancer. Turk J Gastroenterol, 2016, 27(3): 227-232.
45.	Hegar B, Hutapea EI, Advani N, et al. A double-blind placebo-controlled randomized trial on probiotics in small bowel bacterial overgrowth in children treated with omeprazole. J Pediatr (Rio J), 2013, 89(4): 381-387.
46.	Wombwell E, Patterson ME, Bransteitter B, et al. The effect of saccharomyces boulardii primary prevention on risk of hospital-onset clostridioides difficile infection in hospitalized patients administered antibiotics frequently associated with C. difficile infection. Clin Infect Dis, 2021, 73(9): e2512-e2518.
47.	Gunaratnam S, Diarra C, Paquette PD, et al. The acid-dependent and independent effects of Lactobacillus acidophilus CL1285, Lacticaseibacillus casei LBC80R, and Lacticaseibacillus rhamnosus CLR2 on Clostridioides difficile R20291. Probiotics Antimicrob Proteins, 2021, 13(4): 949-956.
48.	Lewis PO, Lundberg TS, Tharp JL, et al. Implementation of global strategies to prevent hospital-onset Clostridium difficile infection: targeting proton pump inhibitors and probiotics. Ann Pharmacother, 2017, 51(10): 848-854.
49.	卢世云, 潘秀珍. 益生菌对肝硬化自发性腹膜炎的预防及对肝功能的影响. 中国微生态学杂志, 2018, 30(10): 1181-1184.
50.	Pace F, Pace M, Quartarone G. Probiotics in digestive diseases: focus on lactobacillus GG. Minerva Gastroenterol Dietol, 2015, 61(4): 273-292.
51.	刘琳, 周婕妤, 吴亚菲, 等. 益生菌生态调节在牙周病防治中的应用. 国际口腔医学杂志, 2020, 47(2): 131-137.
52.	Wang J, Ji H, Wang S, et al. Probiotic lactobacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Front Microbiol, 2018, 9: 1953.
53.	Wang L, Cao H, Liu L, et al. Activation of epidermal growth factor receptor mediates mucin production stimulated by p40, a Lactobacillus rhamnosus GG-derived protein. J Biol Chem, 2014, 289(29): 20234-20244.
54.	Fu J, Wang T, Xiao X, et al. Clostridium butyricum ZJU-F1 benefits the intestinal barrier function and immune response associated with its modulation of gut microbiota in weaned piglets. Cells, 2021, 10(3): 527.
55.	Kumar Singh A, Cabral C, Kumar R, et al. Beneficial effects of dietary polyphenols on gut microbiota and strategies to improve delivery efficiency. Nutrients, 2019, 11(9): 2216.
56.	Milajerdi A, Mousavi SM, Sadeghi A, et al. The effect of probiotics on inflammatory biomarkers: a meta-analysis of randomized clinical trials. Eur J Nutr, 2020, 59(2): 633-649.
57.	Donaldson GP, Ladinsky MS, Yu KB, et al. Gut microbiota utilize immunoglobulin A for mucosal colonization. Science, 2018, 360(6390): 795-800.
58.	Feng Q, Liang S, Jia H, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun, 2015, 6: 6528.

1. Sung JJ, Chiu PW, Chan FKL, et al. Asia-Pacific working group consensus on non-variceal upper gastrointestinal bleeding: an update 2018. Gut, 2018, 67(10): 1757-1768.
2. 刘文忠, 谢勇, 陆红, 等. 第五次全国幽门螺杆菌感染处理共识报告. 中华消化杂志, 2017, 37(6): 364-378.
3. 中华医学会消化病学分会. 2020年中国胃食管反流病专家共识. 中华消化杂志, 2020, 40(10): 649-663.
4. Trifan A, Stanciu C, Girleanu I, et al. Proton pump inhibitors therapy and risk of Clostridium difficile infection: systematic review and meta-analysis. World J Gastroenterol, 2017, 23(35): 6500-6515.
5. Franco DL, Disbrow MB, Kahn A, et al. Duodenal aspirates for small intestine bacterial overgrowth: yield, PPIs, and outcomes after treatment at a tertiary academic medical center. Gastroenterol Res Pract, 2015, 2015: 971582.
6. Dam G, Vilstrup H, Watson H, et al. Proton pump inhibitors as a risk factor for hepatic encephalopathy and spontaneous bacterial peritonitis in patients with cirrhosis with ascites. Hepatology, 2016, 64(4): 1265-1272.
7. Zheng YM, Chen XY, Cai JY, et al. Washed microbiota transplantation reduces proton pump inhibitor dependency in nonerosive reflux disease. World J Gastroenterol, 2021, 27(6): 513-522.
8. Hungin APS, Mitchell CR, Whorwell P, et al. Systematic review: probiotics in the management of lower gastrointestinal symptoms - an updated evidence-based international consensus. Aliment Pharmacol Ther, 2018, 47(8): 1054-1070.
9. Kim GH. Proton pump inhibitor-related gastric mucosal changes. Gut Liver, 2021, 15(5): 646-652.
10. Savarino V, Marabotto E, Zentilin P, et al. The appropriate use of proton-pump inhibitors. Minerva Med, 2018, 109(5): 386-399.
11. Ward RM, Kearns GL. Proton pump inhibitors in pediatrics: mechanism of action, pharmacokinetics, pharmacogenetics, and pharmacodynamics. Paediatr Drugs, 2013, 15(2): 119-131.
12. Clooney AG, Bernstein CN, Leslie WD, et al. A comparison of the gut microbiome between long-term users and non-users of proton pump inhibitors. Aliment Pharmacol Ther, 2016, 43(9): 974-984.
13. 朱苗苗, 李慧兰, 罗佳, 等. 质子泵抑制剂的使用与艰难梭菌感染风险相关性的Meta分析. 中国循证医学杂志, 2016, 16(3): 278-285.
14. McDonald EG, Milligan J, Frenette C, et al. Continuous proton pump inhibitor therapy and the associated risk of recurrent Clostridium difficile infection. JAMA Intern Med, 2015, 175(5): 784-791.
15. Massey BT, Wald A. Small intestinal bacterial overgrowth syndrome: a guide for the appropriate use of breath testing. Dig Dis Sci, 2021, 66(2): 338-347.
16. 张茹, 李园, 马金霞, 等. 长期维持质子泵抑制剂治疗对老年人小肠细菌过度生长的影响分析. 中华内科杂志, 2020, 59(9): 706-710.
17. Giamarellos-Bourboulis EJ, Pyleris E, Barbatzas C, et al. Small intestinal bacterial overgrowth is associated with irritable bowel syndrome and is independent of proton pump inhibitor usage. BMC Gastroenterol, 2016, 16(1): 67.
18. Su T, Lai S, Lee A, et al. Meta-analysis: proton pump inhibitors moderately increase the risk of small intestinal bacterial overgrowth. J Gastroenterol, 2018, 53(1): 27-36.
19. Lo WK, Chan WW. Proton pump inhibitor use and the risk of small intestinal bacterial overgrowth: a meta-analysis. Clin Gastroenterol Hepatol, 2013, 11(5): 483-490.
20. 王洪艳, 孙士东, 毕英杰, 等. 长期使用质子泵抑制剂与小肠细菌过度生长的关系研究. 胃肠病学和肝病学杂志, 2016, 25(11): 1302-1304.
21. Tsuda A, Suda W, Morita H, et al. Influence of proton-pump inhibitors on the luminal microbiota in the gastrointestinal tract. Clin Transl Gastroenterol, 2015, 6(6): e89.
22. Chen X, Xu J, Su Y, et al. Effects of intravenous infusion with sodium butyrate on colonic microbiota, intestinal development- and mucosal immune-related gene expression in normal growing pigs. Front Microbiol, 2018, 9: 1652.
23. Freedberg DE, Lamousé-Smith ES, Lightdale JR, et al. Use of acid suppression medication is associated with risk for C. difficile infection in infants and children:a population-based study. Clin Infect Dis, 2015, 61(6): 912-917.
24. 张旭东, 庄伟清, 陈代杰, 等. 双歧杆菌与消化系统疾病的关系. 中国微生态学杂志, 2021, 33(1): 104-111.
25. 韦炜, 洪依萍. 肝硬化门静脉高压相关并发症的防治原则. 临床肝胆病杂志, 2021, 37(1): 22-25.
26. Yu T, Tang Y, Jiang L, et al. Proton pump inhibitor therapy and its association with spontaneous bacterial peritonitis incidence and mortality: a meta-analysis. Dig Liver Dis, 2016, 48(4): 353-359.
27. Elzouki AN, Neffati N, Rasoul FA, et al. Increased risk of spontaneous bacterial peritonitis in cirrhotic patients using proton pump inhibitors. GE Port J Gastroenterol, 2019, 26(2): 83-89.
28. Naito Y, Kashiwagi K, Takagi T, et al. Intestinal dysbiosis secondary to proton-pump inhibitor use. Digestion, 2018, 97(2): 195-204.
29. van Vlerken LG, Huisman EJ, van Hoek B, et al. Bacterial infections in cirrhosis: role of proton pump inhibitors and intestinal permeability. Eur J Clin Invest, 2012, 42(7): 760-767.
30. El Chemaly A, Nunes P, Jimaja W, et al. Hv1 proton channels differentially regulate the pH of neutrophil and macrophage phagosomes by sustaining the production of phagosomal ROS that inhibit the delivery of vacuolar ATPases. J Leukoc Biol, 2014, 95(5): 827-839.
31. Terg R, Casciato P, Garbe C, et al. Proton pump inhibitor therapy does not increase the incidence of spontaneous bacterial peritonitis in cirrhosis: a multicenter prospective study. J Hepatol, 2015, 62(5): 1056-1060.
32. Reid G, Food and Agricultural Organization of the United Nation and the WHO. The importance of guidelines in the development and application of probiotics. Curr Pharm Des, 2005, 11(1): 11-16.
33. 毛晓丽, 文煜, 费龙. 益生菌辅助埃索美拉唑镁四联疗法对幽门螺杆菌阳性十二指肠溃疡患者肠道菌群分布及血清IFN-γ、IL-10的调节作用. 中国微生态学杂志, 2020, 32(9): 1069-1073.
34. Pinto-Sanchez MI, Hall GB, Ghajar K, et al. Probiotic Bifidobacterium longum NCC3001 reduces depression scores and alters brain activity: a pilot study in patients with irritable bowel syndrome. Gastroenterology, 2017, 153(2): 448-459.e8.
35. Marlicz W, Wunsch E, Mydlowska M, et al. The effect of short term treatment with probiotic VSL#3 on various clinical and biochemical parameters in patients with liver cirrhosis. J Physiol Pharmacol, 2016, 67(6): 867-877.
36. Guo Q, Goldenberg JZ, Humphrey C, et al. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev, 2019, 4(4): CD004827.
37. Bliss ES, Whiteside E. The gut-brain axis, the human gut microbiota and their integration in the development of obesity. Front Physiol, 2018, 9: 900.
38. Tai N, Wong FS, Wen L. The role of gut microbiota in the development of type 1, type 2 diabetes mellitus and obesity. Rev Endocr Metab Disord, 2015, 16(1): 55-65.
39. Eslami M, Yousefi B, Kokhaei P, et al. Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol, 2019, 234(10): 17127-17143.
40. Sotoudegan F, Daniali M, Hassani S, et al. Reappraisal of probiotics’ safety in human. Food Chem Toxicol, 2019, 129: 22-29.
41. 陈爱方, 田霞, 韩峥, 等. 质子泵抑制剂与小肠细菌过度生长的相关性及双歧杆菌三联活菌胶囊疗效观察. 临床消化病杂志, 2019, 31(3): 159-162.
42. Belei O, Olariu L, Dobrescu A, et al. Is it useful to administer probiotics together with proton pump inhibitors in children with gastroesophageal reflux?. J Neurogastroenterol Motil, 2018, 24(1): 51-57.
43. 王松, 肖丹, 陈兰, 等. 曲美布汀联合质子泵抑制剂以及益生菌对胃食管反流病患者临床疗效及肠道菌群的影响. 临床消化病杂志, 2019, 31(6): 349-353.
44. Liang S, Xu L, Zhang D, et al. Effect of probiotics on small intestinal bacterial overgrowth in patients with gastric and colorectal cancer. Turk J Gastroenterol, 2016, 27(3): 227-232.
45. Hegar B, Hutapea EI, Advani N, et al. A double-blind placebo-controlled randomized trial on probiotics in small bowel bacterial overgrowth in children treated with omeprazole. J Pediatr (Rio J), 2013, 89(4): 381-387.
46. Wombwell E, Patterson ME, Bransteitter B, et al. The effect of saccharomyces boulardii primary prevention on risk of hospital-onset clostridioides difficile infection in hospitalized patients administered antibiotics frequently associated with C. difficile infection. Clin Infect Dis, 2021, 73(9): e2512-e2518.
47. Gunaratnam S, Diarra C, Paquette PD, et al. The acid-dependent and independent effects of Lactobacillus acidophilus CL1285, Lacticaseibacillus casei LBC80R, and Lacticaseibacillus rhamnosus CLR2 on Clostridioides difficile R20291. Probiotics Antimicrob Proteins, 2021, 13(4): 949-956.
48. Lewis PO, Lundberg TS, Tharp JL, et al. Implementation of global strategies to prevent hospital-onset Clostridium difficile infection: targeting proton pump inhibitors and probiotics. Ann Pharmacother, 2017, 51(10): 848-854.
49. 卢世云, 潘秀珍. 益生菌对肝硬化自发性腹膜炎的预防及对肝功能的影响. 中国微生态学杂志, 2018, 30(10): 1181-1184.
50. Pace F, Pace M, Quartarone G. Probiotics in digestive diseases: focus on lactobacillus GG. Minerva Gastroenterol Dietol, 2015, 61(4): 273-292.
51. 刘琳, 周婕妤, 吴亚菲, 等. 益生菌生态调节在牙周病防治中的应用. 国际口腔医学杂志, 2020, 47(2): 131-137.
52. Wang J, Ji H, Wang S, et al. Probiotic lactobacillus plantarum promotes intestinal barrier function by strengthening the epithelium and modulating gut microbiota. Front Microbiol, 2018, 9: 1953.
53. Wang L, Cao H, Liu L, et al. Activation of epidermal growth factor receptor mediates mucin production stimulated by p40, a Lactobacillus rhamnosus GG-derived protein. J Biol Chem, 2014, 289(29): 20234-20244.
54. Fu J, Wang T, Xiao X, et al. Clostridium butyricum ZJU-F1 benefits the intestinal barrier function and immune response associated with its modulation of gut microbiota in weaned piglets. Cells, 2021, 10(3): 527.
55. Kumar Singh A, Cabral C, Kumar R, et al. Beneficial effects of dietary polyphenols on gut microbiota and strategies to improve delivery efficiency. Nutrients, 2019, 11(9): 2216.
56. Milajerdi A, Mousavi SM, Sadeghi A, et al. The effect of probiotics on inflammatory biomarkers: a meta-analysis of randomized clinical trials. Eur J Nutr, 2020, 59(2): 633-649.
57. Donaldson GP, Ladinsky MS, Yu KB, et al. Gut microbiota utilize immunoglobulin A for mucosal colonization. Science, 2018, 360(6390): 795-800.
58. Feng Q, Liang S, Jia H, et al. Gut microbiome development along the colorectal adenoma-carcinoma sequence. Nat Commun, 2015, 6: 6528.

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