A comprehensive review on clinical outcome of probiotic and synbiotic therapy for inflammatory bowel diseases

Asian Pacific Journal of Tropical Biomedicine

Volumn 8, Issue 3, 2018, Pages 179-186

  Sivamaruthi, Bhagavathi Sundaram ^a  

^a CHIANG MAI UNIVERSITY   (Thailand)

Author keywords

Crohn's disease; Inflammatory bowel disease; Probiotic; Synbiotic; Ulcerative colitis

Indexed keywords

EID: 85044431266     PISSN: 22211691     EISSN: None     Source Type: Journal    
DOI: 10.4103/2221-1691.228000     Document Type: Review

References (99)

1. Baumgart DC, Carding SR. Inflammatory bowel disease: Cause and immunobiology. Lancet 2007; 369(9573): 1627-1640.
2. Knutsson A, Boggild H. Gastrointestinal disorders among shift workers. Scand J Work Environ Health 2010; 36(2): 85-95.
3. Ordas I, Eckmann L, Talamini M, Baumgart DC, Sandborn WJ. Ulcerative colitis. Lancet 2012; 380(9853): 1606-1619.
4. Vezza T, Rodríguez-Nogales A, Algieri F, Utrilla MP, Rodriguez-Cabezas ME, Galvez J. Flavonoids in inflammatory bowel disease: A review. Nutrients 2016; 8(4): 211.
5. World Cancer Research Fund and American Institute for Cancer Research. Food, nutrition, physical activity, and the prevention of cancer: A global perspective. Washington, DC: American Institute for Cancer Research; 2007.
6. Haggar FA, Boushey RP. Colorectal cancer epidemiology: Incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg 2009; 22(4): 191-197.
7. Siegel R, Desantis C, Jemal A. Colorectal cancer statistics, 2014. CA Cancer J Clin 2014; 64(2): 104-117.
8. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015; 65(2): 87-108.
9. Fujimori S, Gudis K, Mitsui K, Seo T, Yonezawa M, Tanaka S, et al. A randomized controlled trial on the efficacy of synbiotic versus probiotic or prebiotic treatment to improve the quality of life in patients with ulcerative colitis. Nutrition 2009; 25(5): 520-525.
10. Santana PS. Influence of a combination of lactobacilli and bifidobacteria upon disease activity, stool pattern and nutritional status of ulcerative colitis patients. Nutr Hosp 2010; 25(6): 971-983.
11. Li K, Zhang CF, Xia YH, Li ZJ, Han Y. Efficacy of probiotics on ulcerative colitis and its mechanism. Zhonghua Wei Chang Wai Ke Za Zhi 2013; 16(4): 336-339.
12. Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol 2014; 11(8): 506-514.
13. Sanders ME. Probiotics in 2015: Their scope and use. J Clin Gastroenterol 2015; 49(Suppl 1): S2-6.
14. Ozen M, Dinleyici EC. The history of probiotics: The untold story. Benef Microbes 2015; 6(2): 159-165.
15. Venugopalan V, Shriner KA, Wong-Beringer A. Regulatory oversight and safety of probiotic use. Emerg Infect Dis 2010; 16(11): 1661-1665.
16. Food and Agriculture Organization of the United Nations, World Health Organization. Probiotics in food: Health and nutritional properties and guidelines for evaluation. FAO Food Nutr Pap 2006; 85: 1-50.
17. Degnan FH. The US food and drug administration and probiotics: Regulatory categorization. Clin Infect Dis 2008; 46(S2): S133-136.
18. Johnston BC, Goldenberg JZ, Vandvik PO, Sun X, Guyatt GH. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev 2011; 11: CD004827.
19. Hempel S, Newberry SJ, Maher AR, Wang Z, Miles JN, Shanman R, et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: A systematic review and meta-analysis. JAMA 2012; 307(18): 1959-1969.
20. Doron SI, Hibberd PL, Gorbach SL. Probiotics for prevention of antibiotic-associated diarrhea. J Clin Gastroenterol 2008; 42: S58-S63.
21. McFarland LV. Meta-analysis of probiotics for the prevention of traveler's diarrhea. Travel Med Infect Dis 2007; 5: 97-105.
22. Chmielewska A, Szajewska H. Systematic review of randomized controlled trials: Probiotics for functional constipation. World J Gastroenterol 2010; 16: 69-75.
23. Grin PM, Kowalewska PM, Alhazzan W, Fox-Robichaud AE. Lactobacillus for preventing recurrent urinary tract infections in women: Meta-analysis. Can J Urol 2013; 20: 6607-6614.
24. Aloisio I, Santini C, Biavati B, Dinelli G, Cencic A, Chingwaru W, et al. Characterization of Bifidobacterium spp. strains for the treatment of enteric disorders in newborns. Appl Microbiol Biotechnol 2012; 96: 561-576.
25. Di Gioia D, Aloisio I, Mazzola G, Biavati B. Bifidobacteria: Their impact on gut microbiota composition and their applications as probiotics in infants. Appl Microbiol Biotechnol 2014; 98: 563-577.
26. Dylag K, Hubalewska-Mazgaj M, Surmiak M, Szmyd J, Brzozowski T. Probiotics in the mechanism of protection against gut inflammation and therapy of gastrointestinal disorders. Curr Pharm Des 2014; 20: 11491155.
27. Demers M, Dagnault A, Desjardins JA. Randomized double-blind controlled trial: Impact of probiotics on diarrhea in patients treated with pelvic radiation. Clin Nutr 2014; 33(5): 761-767.
28. Isolauri E, Rautava S, Salminen S. Probiotics in the development and treatment of allergic disease. Gastroenterol Clin North Am 2012; 41: 747-762.
29. Tomaro-Duchesneau C, Saha S, Malhotra M, Jones ML, Labbe A, Rodes L, et al. Effect of orally administered L. fermentum NCIMB 5221 on markers of metabolic syndrome: An in vivo analysis using ZDF rats. Appl Microbiol Biotechnol 2014; 98: 115-126.
30. Tung JM, Dolovich LR, Lee CH. Prevention of Clostridium difficile infection with Saccharomyces boulardii: A systematic review. Can J Gastroenterol 2009; 23: 817-821.
31. Fitzpatrick LR. Probiotics for the treatment of Clostridium difficile associated disease. World J Gastrointest Pathophysiol 2013; 4: 47-52.
32. Tompkins TA, Xu X, Ahmarani JA. Comprehensive review of postmarket clinical studies performed in adults with an Asian probiotic formulation. Benef Microbes 2010; 1: 93-106.
33. Richard V, Auwera P, Snoeck R, Daneau D, Meunier F. Nosocomial bacteremia caused by Bacillus species. Eur J Clin Microbiol Infect Dis 1988; 7: 783-785.
34. Buller H, Chin S, Kirschner B, Kohn J, Markowitz J, Moore D, et al. Inflammatory bowel disease in children and adolescents: Working Group Report of the First World Congress of Pediatric Gastroenterology, Hepatology, and Nutrition. J Ped Gastroenterol Nutr 2002; 35(2): 151158.
35. Podolsky DK. Inflammatory bowel disease. New Eng J Medicine 2002; 347: 417-429.
36. Oliveira FM, Emerick APC, Soares EG. Epidemiology aspects of inflammatory bowel disease in the east region of Minas Gerais State. Ciencia Saude Coletiva 2010; 15(1): 1031-1037.
37. Shanahan F. Crohn's disease. Lancet 2002; 359: 62-69.
38. Sadlack B, Merz H, Schorle H, Schimpl A, Feller AC, Horak I. Ulcerative colitis-like disease in mice with disrupted interleukin-2 gene. Cell 1993; 75(2): 253-261.
39. Duchmann R, Kaiser I, Hermann E, Mayet W, Ewe K, Meyer zum Büschenfelde KH. Tolerance exists towards resident intestinal flora but is broken in active inflammatory bowel disease. Clin Exper Immunol 1995; 102: 448-455.
40. Duchmann R, May E, Heike M, Knolle P, Neurath M, Meyer zum Büschenfelde KH. T cell specificity and cross reactivity towards enterobacteria, Bacteroides, Bifidobacterium, and antigen from resident intestinal flora in humans. Gut 1999; 44(6): 812-818.
41. Matsumoto S, Hara T, Hori T, Mitsuyama K, Nagaoka M, Tomiyasu N, et al. Probiotic Lactobacillus induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clin Exp Immunol 2005; 140(3): 417-426.
42. Matsumoto S, Okabe Y, Setoyama H, Takayama K, Ohtsuka J, Funahashi H, et al. Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain. Gut 1998; 43(1):71-78.
43. Kaser A, Zeissig S, Blumberg RS. Inflammatory bowel disease. Annual Rev Immunol 2010; 28: 573-621.
44. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn's disease. Gastroenterology 2004; 127(2): 412-421
45. Sartor RB. Mechanisms of disease: Athogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006; 3: 390-407.
46. Clavel T, Haller D. Molecular interactions between bacteria, the epithelium, and the mucosal immune system in the intestinal tract: Implications for chronic inflammation. Curr Issues Intestinal Microbiol 2007; 8: 25-43.
47. Haller D, Antoine JM, Bengmark S, Enck P, Rijkers GT, Lenoir-Wijnkoop I. Guidance for substantiating the evidence for beneficial effects of probiotics: Probiotics in chronic inflammatory bowel disease and the functional disorder irritable bowel syndrome. J Nutr 2010; 140(3): 690S-697S.
48. Champagne CP, Ross RP, Saarela M, Hansen KF, Charalampopoulos D. Recommendations for viability assessment of probiotics as concentrated cultures and in food matrices. Inter J Food Microbiol 2011; 149(3): 185193.
49. Ocon B, Anzola A, Ortega-González M, Zarzuelo A, Suarez MD, Sanchez de Medina F, et al. Active hexose-correlated compound and Bifidobacterium longum BB536 exert symbiotic effects in experimental colitis. Eur J Nutr 2013; 52(2): 457-466.
50. Natividad JM, Petit V, Huang X, de Palma G, Jury J, Sanz Y, et al. Commensal and probiotic bacteria influence intestinal barrier function and susceptibility to colitis in Nod1-/-; Nod2-/-mice. Inflamm Bowel Dis 2012; 18(8): 1434-1446.
51. Liu YW, Su YW, Ong WK, Cheng TH, Tsai YC. Oral administration of Lactobacillus plantarum K68 ameliorates DSS-induced ulcerative colitis in BALB/c mice via the anti-inflammatory and immunomodulatory activities. Int Immunopharmacol 2011; 11(12): 2159-2166.
52. GirishKumar B, Henry DE, Srinivasan K, Prapulla SG. Beneficial effect of a probiotic Lactobacillus fermentum CFR 2195 in trinitrobenzenesulfonate induced colitis in rat. Ann Food Sci Technol 2012; 13(2): 231-239.
53. Venturi A, Gionchetti P, Rizzello F, Johansson R, Zucconi E, Brigidi P, et al. Impact on the composition of the fecal flora by a new probiotic preparation: Preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther 1999; 13(8): 1103-1108.
54. Miele E, Pascarella F, Giannetti E, Quaglietta L, Baldassano RN, Staiano A. Effect of a probiotic preparation (VSL#3) on induction and maintenance of remission in children with ulcerative colitis. Am J Gastroenterol 2009; 104(2): 437-443.
55. Sood A, Midha V, Makharia GK, Ahuja V, Singal D, Goswami P, et al. The probiotic preparation, VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis. Clin Gastroenterol Hepatol 2009; 7(11): 1202-1209.
56. Ng SC, Plamondon S, Kamm MA, Hart AL, Al-Hassi HO, Guenther T, et al. Immunosuppressive effects via human intestinal dendritic cells of probiotic bacteria and steroids in the treatment of acute ulcerative colitis. Inflamm Bowel Dis 2010; 16(8): 1286-1298.
57. Tursi A, Brandimarte G, Papa A, Giglio A, Elisei W, Giorgetti GM, et al. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: A double-blind, randomized, placebo-controlled study. Am J Gastroenterol 2010; 105(10): 2218-2227.
58. Fedorak RN, Feagan BG, Hotte N, Leddin D, Dieleman LA, Petrunia DM, et al. The probiotic VSL#3 has anti-inflammatory effects and could reduce endoscopic recurrence after surgery for Crohn's disease. Clin Gastroenterol Hepatol 2015; 13(5): 928-935.
59. Cui HH, Chen CL, Wang JD, Yang YJ, Cun Y, Wu JB, et al. Effects of probiotic on intestinal mucosa of patients with ulcerative colitis. World J Gastroenterol 2004; 10(10): 1521-1525.
60. Kato K, Mizuno S, Umesaki Y, Ishii Y, Sugitani M, Imaoka A, et al. Randomized placebo-controlled trial assessing the effect of bifidobacteria-fermented milk on active ulcerative colitis. Aliment Pharmacol Ther 2004; 20(10): 1133-1141.
61. Tsuda Y, Yoshimatsu Y, Aoki H, Nakamura K, Irie M, Fukuda K, et al. Clinical effectiveness of probiotics therapy (BIO-THREE) in patients with ulcerative colitis refractory to conventional therapy. Scand J Gastroenterol 2007; 42: 1306-1311.
62. Yoshimatsu Y, Yamada A, Furukawa R, Sono K, Osamura A, Nakamura K, et al. Effectiveness of probiotic therapy for the prevention of relapse in patients with inactive ulcerative colitis. World J Gastroenterol 2015; 21(19): 5985-5994.
63. Fujimori S, Gudis K, Mitsui K, Seo T, Yonezawa M, Tanaka S, et al. A randomized controlled trial on the efficacy of synbiotic versus probiotic or prebiotic treatment to improve the quality of life in patients with ulcerative colitis. Nutrition 2009; 25(5): 520-525.
64. Hegazy SK, El-Bedewy MM. Effect of probiotics on pro-inflammatory cytokines and NF-κB activation in ulcerative colitis. World J Gastroenterol 2010; 16(33): 4145-4151.
65. Wildt S, Nordgaard I, Hansen U, Brockmann E, Rumessen JJ. A randomized double-blind placebo-controlled trial with Lactobacillus acidophilus La-5 and Bifidobacterium animalis subsp. lactis BB-12 for maintenance of remission in ulcerative colitis. J Crohns Colitis 2011; 5(2): 115-121.
66. D'Inca R, Barollo M, Scarpa M, Grillo AR, Brun P, Vettorato MG, et al. Rectal administration of Lactobacillus casei DG modifies flora composition and Toll-like receptor expression in colonic mucosa of patients with mild ulcerative colitis. Dig Dis Sci 2011; 56(4): 1178-1187.
67. Oliva S, Di Nardo G, Ferrari F, Mallardo S, Rossi P, Patrizi G, et al. Randomized clinical trial: the effectiveness of Lactobacillus reuteri ATCC 55730 rectal enema in children with active distal ulcerative colitis. Aliment Pharmacol Ther 2012; 35(3): 327-334.
68. Ishikawa H, Matsumoto S, Ohashi Y, Imaoka A, Setoyama H, Umesaki Y, et al. Beneficial effects of probiotic bifidobacterium and galacto-oligosaccharide in patients with ulcerative colitis: A randomized controlled study. Digestion 2011; 84(2): 128-133.
69. Krag A, Israelsen H, von Ryberg B, Andersen KK, Bendtsen F. Safety and efficacy of Profermin® to induce remission in ulcerative colitis. World J Gastroenterol 2012; 18(15): 1773-1780.
70. Groeger D, O'Mahony L, Murphy EF, Bourke JF, Dinan TG, Kiely B, et al. Bifidobacterium infantis 35624 modulates host inflammatory processes beyond the gut. Gut Microbes 2013; 4(4): 325-339.
71. Persborn M, Gerritsen J, Wallon C, Carlsson A, Akkermans LM, Söderholm JD. The effects of probiotics on barrier function and mucosal pouch microbiota during maintenance treatment for severe pouchitis in patients with ulcerative colitis. Aliment Pharmacol Ther 2013; 38(7): 772-783.
72. Petersen AM, Mirsepasi H, Halkjær SI, Mortensen EM, Nordgaard-Lassen I, Krogfelt KA. Ciprofloxacin and probiotic Escherichia coli Nissle add-on treatment in active ulcerative colitis: A double-blind randomized placebo controlled clinical trial. J Crohns Colitis 2014; 8(11): 1498-1505.
73. Yasueda A, Mizushima T, Nezu R, Sumi R, Tanaka M, Nishimura J, et al. The effect of Clostridium butyricum MIYAIRI on the prevention of pouchitis and alteration of the microbiota profile in patients with ulcerative colitis. Surg Today 2016; 46(8): 939-949.
74. Palumbo VD, Romeo M, Marino Gammazza A, Carini F, Damiani P, Damiano G, et al. The long-term effects of probiotics in the therapy of ulcerative colitis: A clinical study. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2016; 160(3): 372-377.
75. Tamaki H, Nakase H, Inoue S, Kawanami C, Itani T, Ohana M, et al. Efficacy of probiotic treatment with Bifidobacterium longum 536 for induction of remission in active ulcerative colitis: A randomized, double-blinded, placebo-controlled multicenter trial. Dig Endosc 2016; 28(1): 67-74.
76. Baroja LM, Kirjavainen PV, Hekmat S, Reid G. Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin Exp Immunol 2007; 149(3): 470-479.
77. Shadnoush M, Hosseini RS, Khalilnezhad A, Navai L, Goudarzi H, Vaezjalali M. Effects of probiotics on gut microbiota in patients with inflammatory bowel disease: A double-blind, placebo-controlled clinical trial. Korean J Gastroenterol 2015; 65: 215-221.
78. Garcia Vilela E, De Lourdes De Abreu Ferrari M, Oswaldo Da Gama Torres H, Guerra Pinto A, Carolina Carneiro Aguirre A, Paiva Martins F, et al. Influence of Saccharomyces boulardii on the intestinal permeability of patients with Crohn's disease in remission. Scand J Gastroenterol 2008; 43(7): 842-848.
79. Vleggaar FP, Monkelbaan JF, van Erpecum KJ. Probiotics in primary sclerosing cholangitis: A randomized placebo-controlled crossover pilot study. Eur J Gastroenterol Hepatol 2008; 20(7): 688-692.
80. Bourreille A, Cadiot G, Le Dreau G, Laharie D, Beaugerie L, Dupas JL, et al. Saccharomyces boulardii does not prevent relapse of Crohn's disease. Clin Gastroenterol Hepatol 2013; 11(8): 982-987.
81. Steed H, Macfarlane GT, Blackett KL, Bahrami B, Reynolds N, Walsh SV, et al. Clinical trial: The microbiological and immunological effects of synbiotic consumption-a randomized double-blind placebo-controlled study in active Crohn's disease. Aliment Pharmacol Ther 2010; 32(7): 872-883.
82. Ahmed J, Reddy BS, Molbak L, Leser TD, MacFie J. Impact of probiotics on colonic microflora in patients with colitis: A prospective double blind randomized crossover study. Int J Surg 2013; 11(10): 1131-1136.
83. Doron S, Snydman DR. Risk and safety of probiotics. Clin Infect Dis 2015; 60(S2): S129-134.
84. Munoz P, Bouza E, Cuenca-Estrella M, Eiros JM, Perez MJ, Sanchez-Somolinos M, et al. Saccharomyces cerevisiae fungemia: An emerging infectious disease. Clin Infect Dis 2005; 40(11): 1625-1634.
85. Niault M, Thomas F, Prost J, Ansari FH, Kalfon P. Fungemia due to Saccharomyces species in a patient treated with enteral Saccharomyces boulardii. Clin Infect Dis 1999; 28(4): 930.
86. Perapoch J, Planes AM, Querol A, Lopez V, Martinez-Bendayán I, Tormo R, et al. Fungemia with Saccharomyces cerevisiae in two newborns, only one of whom had been treated with ultra-levura. Eur J Clin Microbiol Infect Dis 2000; 19(6): 468-470.
87. Piechno S, Seguin P, Gangneux JP. Saccharomyces boulardii fungal sepsis: Beware of the yeast. Can J Anaesth 2007; 54: 245-246.
88. Trautmann M, Synowzik I, Nadji-Ohl M, Von Voigt TB, Reiter W. Fungemia due to Saccharomyces cerevisiae var. boulardii. Chemother J 2008; 17: 57-61.
89. De Groote MA, Frank DN, Dowell E, Glode MP, Pace NR. Lactobacillus rhamnosus GG bacteremia associated with probiotic use in a child with short gut syndrome. Pediatr Infect Dis J 2005; 24: 278-280.
90. Ledoux D, Labombardi VJ, Karter D. Lactobacillus acidophilus bacteraemia after use of a probiotic in a patient with AIDS and Hodgkin's disease. Int J STD AIDS 2006; 17(4): 280-282.
91. Tommasi C, Equitani F, Masala M, Ballardini M, Favaro M, Meledandri M, et al. Diagnostic difficulties of Lactobacillus casei bacteraemia in immunocompetent patients: A case report. J Med Case Reports 2008; 2: 315.
92. Vahabnezhad E, Mochon AB, Wozniak LJ, Ziring DA. Lactobacillus bacteremia associated with probiotic use in a pediatric patient with ulcerative colitis. J Clin Gastroenterol 2013; 47: 437-439.
93. Oggioni MR, Pozzi G, Valensin PE, Galieni P, Bigazzi C. Recurrent septicemia in an immunocompromised patient due to probiotic strains of Bacillus subtilis. J Clin Microbiol 1998; 36(1): 325-326.
94. Ohishi A, Takahashi S, Ito Y, Ohishi Y, Tsukamoto K, Nanba Y, et al. Bifidobacterium septicemia associated with postoperative probiotic therapy in a neonate with omphalocele. J Pediatr 2010; 156(4): 679-681.
95. Zein EF, Karaa S, Chemaly A, Saidi I, Daou-Chahine W, Rohban R. Lactobacillus rhamnosus septicemia in a diabetic patient associated with probiotic use: A case report. Ann Biol Clin (Paris) 2008; 66(2): 195-198.
96. Mackay AD, Taylor MB, Kibbler CC, Hamilton-Miller JM. Lactobacillus endocarditis caused by a probiotic organism. Clin Microbiol Infect 1999; 5: 290-292.
97. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: A randomized, double-blind, placebo-controlled trial. Lancet 2008; 371(9613): 651-659.
98. Munakata S, Arakawa C, Kohira R, Fujita Y, Fuchigami T, Mugishima H. A case of D-lactic acid encephalopathy associated with use of probiotics. Brain Dev 2010; 32(8): 691-694.
99. Brunser. Probiotics: Innocuousness, prevention and risks. Rev Chil Pediatr 2017; 88(4): 534-540.