Probiotics: Their place in therapy of irritable bowel syndrome

1. Ивашкин В.Т., Маев И.В., Шелыгин Ю.А., Баранская Е.К., Белоус С.С., Белоусова Е.А. с соавт. Диагностика и лечение синдрома раздраженного кишечника (клинические рекомендации Российской гастроэнтерологической ассоциации и Ассоциации колопроктологов России). Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2021;31(5):74–95. (Ivashkin VT, Maev IV, Shelygin YuA, Baranskaya EK, Belous SS, Belousova EA et al. Diagnosis and treatment of irritable bowel syndrome: Clinical recommendations of the Russian Gastroenterological Association and Association of Coloproctologists of Russia. Rossiyskiy zhurnal gastroenterologii, gepatologii, koloproktologii = Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2021;31(5):74–95 (In Russ.)).

EDN: MKBDEB. https://doi.org/10.22416/1382-4376-2021-31-5-74-95

2. Sperber AD, Dumitrascu D, Fukudo S, Gerson C, Ghoshal UC, Gwee KA et al. The global prevalence of IBS in adults remains elusive due to the heterogeneity of studies: A Rome Foundation working team literature review. Gut. 2017;66(6):1075–82.

PMID: 26818616. https://doi.org/10.1136/gutjnl-2015-311240

3. Sperber AD, Bangdiwala SI, Drossman DA, Ghoshal UC, Simren M, Tack J et al. Worldwide prevalence and burden of functional gastrointestinal disorders, results of Rome foundation global study. Gastroenterology. 2021;160(1):99–114.e3.

PMID: 32294476. https://doi.org/10.1053/j.gastro.2020.04.014

4. Black CJ, Ford AC. Global burden of irritable bowel syndrome: Trends, predictions and risk factors. Nat Rev Gastroenterol Hepatol. 2020;17(8):473–86.

PMID: 32296140. https://doi.org/10.1038/s41575-020-0286-8

5. Levy RL, Jones KR, Whitehead WE, Feld SI, Talley NJ, Corey LA. Irritable bowel syndrome in twins: Heredity and social learning both contribute to etiology. Gastroenterology. 2001;121(4):799–804.

PMID: 11606493. https://doi.org/10.1053/gast.2001.27995

6. Wadhwa A, Nahhas MFA, Dierkhising RA. High risk of post-infectious irritable bowel syndrome in patients with Clostridium difficile infection. Aliment Pharmacol Ther. 2016;44(6):576–82.

PMID: 27444134. PMCID: PMC4982831. https://doi.org/10.1111/apt.13737

7. Rahman MM, Goshal UC, Sultana S. Long-term gastrointestinal consequences are frequent following sporadic acute infectious diarrhea in a tropical country: A prospective cohort study. Am J Gastroenterol. 2018;113(9):1363–75.

PMID: 30171215. https://doi.org/10.1038/s41395-018-0208-3

8. Klem F, Wadhwa A, Prokop LJ, Sundt WJ, Farrugia G, Camilleri M et al. Prevalence, risk factors and outcomes of irritable bowel syndrome after infectious enteritis: A systemic review and meta-analysis. Gastroenterology. 2017;152(5):1042–54.e1.

PMID: 28069350. PMCID: PMC5367939. https://doi.org/10.1053/j.gastro.2016.12.039

9. Zanini B, Ricci C, Bandera F, Caselani F, Magni A, Laronga AM et al. Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am J Gastroenterol. 2012;107(6):891–99.

PMID: 22525306. https://doi.org/10.1038/ajg.2012.102

10. Noviello D, Costantino A, Muscatello A, Bandera A, Consonni D, Vecchi M, Basilisco G. Functional gastrointestinal and somatoform symptoms four month after SARS-CoV-2 infection: A controlled cohort study. Neurogastroenterol Motil. 2022;34(2):e14187.

PMID: 34060710. PMCID: PMC8209890. https://doi.org/10.1111/nmo.14187

11. Тхакушинова Н.Х., Горелов А.В. Повторные острые кишечные инфекции ротавирусной этиологии у детей: особенности течения, факторы риска, условия развития и исходы. Инфекционные болезни. 2017;15(1):29–34. (Tkhakushinova NKh, Gorelov AV. Repeated acute intestinal infections of rotavirus etiology in children: Specificities of the course, risk factors, conditions of development, and outcomes. Infektsionnye bolezni = Infectious diseases. 2017;15(1):29–34 (In Russ.)).

EDN: YIRFHD. https://doi.org/10.20953/1729-9225-2017-1-29-34

12. Spiller R, Garsed K. Postinfectious irritable bowel syndrome. Gastroenterology. 2009;136(6):1979–88.

PMID: 19457422. https://doi.org/10.1053/j.gastro.2009.02.074

13. Videlock EJ, Chang L. Latest insights on the pathogenesis of irritable bowel syndrome. Gastroenterol Clin North Am. 2021;50(3):505–22.

PMID: 34304785. https://doi.org/10.1016/j.gtc.2021.04.002

14. Mishima Y, Ishihara S. Enteric microbiota-mediated serotonergic signaling in pathogenesis of irritable bowel syndrome. Int J Mol Sci. 2021;22(19):10235.

PMID: 34638577. PMCID: PMC8508930. https://doi.org/10.3390/ijms221910235

15. Chen Y, Xu J, Chen Y. Regulation of neurotransmitters by the gut microbiota and effects on cognition in neurological disorders. Nutrients. 2021;13(6):2099.

PMID: 34205336. PMCID: PMC8234057. https://doi.org/10.3390/nu13062099

16. Keshteli AH, Madsen KL, Mandal R, Mandal R, Boeckxstaens GE, Bercik P, De Palma G et al. Comparison of the metabolomic profiles of irritable bowel syndrome patients with ulcerative colitis patients and healthy controls: New insights into pathophysiology and potential biomarkers. Aliment Pharmacol Ther. 2019;49(6):723–32.

PMID: 30706502. https://doi.org/10.1111/apt.15141

17. Groeger D, Murphy EF, Tan HTT, Larsen IS, O’Neill I, Quigley EMM. Interactions between symptoms and psychological status in irritable bowel syndrome: An exploratory study of the impact of a probiotic combination. Neurogastroenterol Motil. 2023;35(1):e14477.

PMID: 36178333. PMCID: PMC10078522. https://doi.org/10.1111/nmo.14477

18. Videlock EJ, Chang L. Latest insights on the pathogenesis of irritable bowel syndrome. Gastroenterol Clin North Am. 2021;50(3):505–22.

PMID: 34304785. https://doi.org/10.1016/j.gtc.2021.04.002

19. Ивашкин В.Т., Шелыгин Ю.А., Баранская Е.К., Белоусова Е.А., Бениашвили А.Г., Васильев С.В. с соавт. Клинические рекомендации Российской гастроэнтерологической ассоциации и Ассоциации колопроктологов России по диагностике и лечению синдрома раздраженного кишечника. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2017;27(5):76–93. (Ivashkin VT, Shelygin YuA, Baranskaya EK, Belousova EA, Beniashvili AG, Vasilyev SV et al. Diagnosis and treatment of the irritable bowel syndrome: Clinical guidelines of the Russian Gastroenterological Association and Russian Association of Coloproctology. Rossiyskiy zhurnal gastroenterologii, gepatologii, koloproktologii = Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2017;27(5):76–93 (In Russ.)).

EDN: ZHQRZJ. https://doi.org/10.22416/1382-4376-2017-27-5-76-93

20. Zhou Q, Zhang B, Verne GN. Intestinal membrane permeability and hypersensitivity in the irritable bowel syndrome. Pain. 2009;146(1–2):41–46.

PMID: 19595511. PMCID: PMC2763174. https://doi.org/10.1016/j.pain.2009.06.017

21. Zeng J, Li Y-Q, Zuo X-L, Zhen Y-B, Yang J, Liu C-H. Clinical trial: Effect of active lactic acid bacteria on mucosal barrier function in patients with diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther. 2008;28:994–1002.

PMID: 18671775. https://doi.org/10.1111/j.1365-2036.2008.03818.x

22. O’Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K et al. Lactobacillus and bifidobacterium in irritable bowel syndrome: Symptom responses and relationship to cytokine profiles. Gastroenterology. 2005;128(3):541–51.

PMID: 15765388. https://doi.org/10.1053/j.gastro.2004.11.050

23. Guarino MPL, Altomare A, Stasi E, Marignani M, Severi C, Alloni R et al. Effect of acute mucosal exposure to lactobacillus rhamnosus GG on human colonic smooth muscle cells. J Clin Gastroenterol. 2008;42 Suppl 3 Pt 2:S185–S190.

PMID: 18685510. https://doi.org/10.1097/mcg.0b013e31817e1cac

24. Wang B, Mao Y-K, Diorio C, Wang L, Huizinga JD, Bienenstock J, Kunze W. Lactobacillus reuteri ingestion and IK(Ca) channel blockade have similar effects on rat colon motility and myenteric neurones. Neurogastroenterol Motil. 2010;22(1):98–107, e33.

PMID: 19788711. https://doi.org/10.1111/j.1365-2982.2009.01384.x

25. Dong Y, Han Y, Wang Z, Qin Z, Yang C, Cao J, Chen Y. Role of serotonin on the intestinal mucosal immune response to stress-induced diarrhea in weaning mice. BMC Gastroenterol. 2017;17(1):82.

PMID: 28633646. PMCID: PMC5479009. https://doi.org/10.1186/s12876-017-0634-5

26. Jiang H, Ling Z, Zhang Y, Mao H, Ma Z, Yin Y et al. Altered fecal microbiota composition in patients with major depressive disorder. Brain Behav Immun. 2015;48:186–94.

PMID: 25882912. https://doi.org/10.1016/j.bbi.2015.03.016

27. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu X-N et al. Postnatal microbial colonization programs the hypothalamic-pituitary-adrenal system for stress response in mice. J Physiol. 2004;558(Pt 1):263–75.

PMID: 15133062. PMCID: PMC1664925. https://doi.org/10.1113/jphysiol.2004.063388

28. Jasarevic E, Howerton CL, Howard CD, Bale TL. Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology. 2015;156(9):3265–76.

PMID: 26079804. PMCID: PMC4541625. https://doi.org/10.1210/en.2015-1177

29. Golubeva AV, Crampton S, Desbonnet L, Edge D, O’Sullivan O, Lomasney KW et al. Prenatal stress-induced alterations in major physiological systems correlate with gut microbiota composition in adulthood. Psychoneuroendocrinology. 2015;60:58–74.

PMID: 26135201. https://doi.org/10.1016/j.psyneuen.2015.06.002

30. Yang R, Jiang J, Ouyang J, Zhao Yuanpei, Xi Biao. Efficacy and safety of probiotics in irritable bowel syndrome: A systematic review and meta-analysis. Clin Nutr ESPEN. 2024;60:362–72.

PMID: 38479936. https://doi.org/10.1016/j.clnesp.2024.02.025

31. Wu Y, Li Y, Zheng Q, Li L. The efficacy of probiotics, prebiotics, synbiotics, and fecal microbiota transplantation in irritable bowel syndrome: A systematic review and network meta-analysis. Nutrients. 2024;16(13):2114.

PMID: 38999862. PMCID: PMC11243554. https://doi.org/10.3390/nu16132114

32. Konstantis G, Efstathiou S, Pourzitaki C, Kitsikidou E, Germanidis G, Chourdakis M. Efficacy and safety of probiotics in the treatment of irritable bowel syndrome: A systematic review and meta-analysis of randomised clinical trials using ROME IV criteria. Clin Nutr. 2023;42(5):800–9.

PMID: 37031468. https://doi.org/10.1016/j.clnu.2023.03.019

33. Goodoory VC, Khasawneh M, Black CJ, Quigley EMM, Moayyedi P, Ford AC. Efficacy of probiotics in irritable bowel syndrome: Systematic review and meta-analysis. Gastroenterology. 2023;165(5):1206–18.

PMID: 37541528. https://doi.org/10.1053/j.gastro.2023.07.018

34. Zhang WX, Shi LB, Zhou MS, Wu J, Shi HY. Efficacy of probiotics, prebiotics and synbiotics in irritable bowel syndrome: A systematic review and meta-analysis of randomized, double-blind, placebo-controlled trials. J Med Microbiol. 2023;72(9).

PMID: 37772692. https://doi.org/10.1099/jmm.0.001758

35. Chen M, Yuan L, Xie C-R, Wang X-Y, Feng S-J, Xiao X-Y, Zheng H. Probiotics for the management of irritable bowel syndrome: A systematic review and three-level meta-analysis. Int J Surg. 2023;109(11):3631–47.

PMID: 37565634. PMCID: PMC10651259. https://doi.org/10.1097/js9.0000000000000658

36. Xie P, Luo M, Deng X, Fan J, Xiong L. Outcome-specific efficacy of different probiotic strains and mixtures in irritable bowel syndrome: A systematic review and network meta-analysis. Nutrients. 2023;15(17):3856.

PMID: 37686889. PMCID: PMC10490209. https://doi.org/10.3390/nu15173856

37. van der Geest AM, Schukking I, Brummer RJM, van de Burgwal LHM, Larsen OFA. Comparing probiotic and drug interventions in irritable bowel syndrome: A meta-analysis of randomised controlled trials. Benef Microbes. 2022;13(3):183–94.

PMID: 35848115. https://doi.org/10.3920/bm2021.0123

38. Wang F, Zhao T, Wang W, Dai Q, Ma X. Meta-analysis of the efficacy of probiotics to treat diarrhea. Medicine (Baltimore). 2022;101(38):e30880.

PMID: 36197181. PMCID: PMC9509072. https://doi.org/10.1097/md.0000000000030880

39. Fatahi S, Hosseini A, Sohouli MH, Sayyari A, Khatami K, Farsani ZF et al. Effects of probiotic supplementation on abdominal pain severity in pediatric patients with irritable bowel syndrome: A systematic review and meta-analysis of randomized clinical trials. World J Pediatr. 2022;18(5):320–32.

PMID: 35106700. https://doi.org/10.1007/s12519-022-00516-6

40. Shang X, E F-F, Guo K.-L, Li Y-F, Zhao H-L, Wang Y et al. Effectiveness and safety of probiotics for patients with constipation-predominant irritable bowel syndrome: A systematic review and meta-analysis of 10 randomized controlled trials. Nutrients. 2022;14(12):2482.

PMID: 35745212. PMCID: PMC9231226. https://doi.org/10.3390/nu14122482

41. Zhang T, Zhang C, Zhang J, Sun F, Duan L. Efficacy of probiotics for irritable bowel syndrome: A systematic review and network meta-analysis. Front Cell Infect Microbiol. 2022;12:859967.

PMID: 35433498. PMCID: PMC9010660. https://doi.org/10.3389/fcimb.2022.859967

42. Wang Y, Chen N, Niu F, Li Y, Guo K, Shang X et al. Probiotics therapy for adults with diarrhea-predominant irritable bowel syndrome: A systematic review and meta-analysis of 10 RCTs. Int J Colorectal Dis. 2022;37(11):2263–76.

PMID: 36251040. https://doi.org/10.1007/s00384-022-04261-0

43. Xu H-L, Zou L-L, Chen M-B, Wang H, Shen W-M, Zheng Q-H, Cui W-Y. Efficacy of probiotic adjuvant therapy for irritable bowel syndrome in children: A systematic review and meta-analysis. PLoS One. 2021;16(8):e0255160.

PMID: 34358238. PMCID: PMC8345868. https://doi.org/10.1371/journal.pone.0255160

44. Asha MZ, Khalil SFH. Efficacy and safety of probiotics, prebiotics and synbiotics in the treatment of irritable bowel syndrome: A systematic review and meta-analysis. Sultan Qaboos Univ Med J. 2020;20(1):e13–e24.

PMID: 32190365. PMCID: PMC7065695. https://doi.org/10.18295/squmj.2020.20.01.003

45. Sun J-R, Kong C-F, Qu X-K, Deng C, Lou Y-N, Jia L-Q. Efficacy and safety of probiotics in irritable bowel syndrome: A systematic review and meta-analysis. Saudi J Gastroenterol. 2020;26(2):66–77.

PMID: 31898645. PMCID: PMC7279071. https://doi.org/10.4103/sjg.sjg_384_19

46. Niu H-L, Xiao J-Y. The efficacy and safety of probiotics in patients with irritable bowel syndrome: Evidence based on 35 randomized controlled trials. Int J Surg. 2020;75:116–27.

PMID: 32014597. https://doi.org/10.1016/j.ijsu.2020.01.142

47. Wen Y, Li J, Long Q, Yue C-C, He B, Tang X-G. The efficacy and safety of probiotics for patients with constipation-predominant irritable bowel syndrome: A systematic review and meta-analysis based on seventeen randomized controlled trials. Int J Surg. 2020;79:111–19.

PMID: 32387213. https://doi.org/10.1016/j.ijsu.2020.04.063

48. Ford AC, Harris LA, Lacy BE, Quigley EMM, Moayyedi P. Systematic review with meta-analysis: The efficacy of prebiotics, probiotics, synbiotics and antibiotics in irritable bowel syndrome. Aliment Pharmacol Ther. 2018;48(10):1044–60.

PMID: 30294792. https://doi.org/10.1111/apt.15001

49. Hungin APS, Mitchell CR, Whorwell P, Mulligan C, Cole O, Agréus L et al.; European Society for Primary Care Gastroenterology. Systematic review: Probiotics in the management of lower gastrointestinal symptoms – an updated evidence-based international consensus. Aliment Pharmacol Ther. 2018;47(8):1054–70.

PMID: 29460487. PMCID: PMC5900870. https://doi.org/10.1111/apt.14539

50. Ивашкин В.Т., Маев И.В., Абдулганиева Д.И., Алексеенко С.А., Горелов А.В., Захарова И.Н. с соавт. Практические рекомендации Научного сообщества по содействию клиническому изучению микробиома человека (НСОИМ) и Российской гастроэнтерологической ассоциации (РГА) по применению пробиотиков, пребиотиков, синбиотиков и обогащенных ими функциональных пищевых продуктов для лечения и профилактики заболеваний гастроэнтерологического профиля у детей и взрослых. Российский журнал гастроэнтерологии, гепатологии, колопроктологии. 2021;31(2):65–91. (Ivashkin VT, Maev IV, Abdulganieva DI, Alekseenko SA, Gorelov AV, Zakharova IN et al. Practical recommendations of Scientific Society for the Study of Human Microbiome and the Russian Gastroenterological Association on use of probiotics, prebiotics, synbiotics and functional foods in treatment and prevention of gastroenterological diseases in children and adults. Rossiyskiy zhurnal gastroenterologii, gepatologii, koloproktologii = Russian Journal of Gastroenterology, Hepatology, Coloproctology. 2021;31(2):65–91 (In Russ.)).

EDN: IWBRVV. https://doi.org/10.22416/1382-4376-2021-31-2-65-91

51. Lenoir M, Wienke J, Fardao-Beyler F, Roese N. An 8-week course of Bifidobacterium longum 35624® is associated with a reduction in the symptoms of irritable bowel syndrome. Probiotics Antimicrob Proteins. 2023;17(1):315–27.

PMID: 37702965. https://doi.org/10.1007/s12602-023-10151-w

52. Sabate J-M, Iglicki F. Effect of Bifidobacterium longum 35624 on disease severity and quality of life in patients with irritable bowel syndrome. World J Gastroenterol. 2022;28(7):732–44.

PMID: 35317278. PMCID: PMC8891724. https://doi.org/10.3748/wjg.v28.i7.732

53. Munoz SC, Palma SV, Marqués LL, Pizarro MNE, Mechasqui JM, Sorensen K. Effects of Bifidobacterium longum 35624 in children and adolescents with irritable bowel syndrome. Nutrients. 2024;16(12):1967.

PMID: 38931319. PMCID: PMC11206369. https://doi.org/10.3390/nu16121967

54. Глобальные практические рекомендации Всемирной гастроэнтерологической организации. Пробиотики и пребиотики. Доступ: https://www.worldgastroenterology.org/UserFiles/file/guidelines/probiotics-and-prebiotics-russian-2017.pdf (дата обращения – 19.05.2025). (Global Practice Guidelines of the World Gastroenterology Organization. Probiotics and prebiotics. URL: https://www.worldgastroenterology.org/UserFiles/file/guidelines/probiotics-and-prebiotics-russian-2017.pdf (date of access – 19.05.2025) (In Russ.)).

55. Turner RB, Woodfolk JA, Borish L, Steinke JW, Patrie JT, Muehling LM et al. Effect of probiotic on innate inflammatory response and viral shedding in experimental rhinovirus infection – a randomised controlled trial. Benef Microbes. 2017;8(2):207–15.

PMID: 28343401. PMCID: PMC5797652. https://doi.org/10.3920/bm2016.0160

56. Славко Е.А., Желдыбаева А.Е. Применение синбиотиков в комплексной терапии заболеваний с синдромом избыточного бактериального роста. Лечение и профилактика. 2022;12(4):85–89. (Slavko EA, Zheldybaeva AE. The use of synbiotics in the complex therapy of diseases with bacterial overgrowth syndrome. Lechenie i profilaktika = Treatment and Prevention. 2022;12(4):85–89 (In Russ.)). EDN: ADDZAH.