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
Open accessAbstract
OBJECTIVES: VSL#3 is a high-potency probiotic mixture that has been used successfully in the treatment of pouchitis. The primary end point of the study was to assess the effects of supplementation with VSL#3 in patients affected by relapsing ulcerative colitis (UC) who are already under treatment with 5-aminosalicylic acid (ASA) and/or immunosuppressants at stable doses. METHODS: A total of 144 consecutive patients were randomly treated for 8 weeks with VSL#3 at a dose of 3,600 billion CFU/day (71 patients) or with placebo (73 patients). RESULTS: In all, 65 patients in the VSL#3 group and 66 patients in the placebo group completed the study. The decrease in ulcerative colitis disease activity index (UCDAI) scores of 50% or more was higher in the VSL#3 group than in the placebo group (63.1 vs. 40.8; per protocol (PP) P=0.010, confidence interval (CI)₉₅(%) 0.51-0.74; intention to treat (ITT) P=0.031, CI₉₅(%) 0.47-0.69). Significant results with VSL#3 were recorded in an improvement of three points or more in the UCDAI score (60.5% vs. 41.4%; PP P=0.017, CI₉₅(%) 0.51-0.74; ITT P=0.046, CI₉₅(%) 0.47-0.69) and in rectal bleeding (PP P=0.014, CI₉₅(%) 0.46-0.70; ITT P=0.036, CI₉₅(%) 0.41-0.65), whereas stool frequency (PP P=0.202, CI₉₅(%) 0.39-0.63; ITT P=0.229, CI₉₅(%) 0.35-0.57), physician's rate of disease activity (PP P=0.088, CI₉₅(%) 0.34-0.58; ITT P=0.168, CI₉₅(%) 0.31-0.53), and endoscopic scores (PP P=0.086, CI₉₅(%) 0.74-0.92; ITT P=0.366, CI₉₅(%) 0.66-0.86) did not show statistical differences. Remission was higher in the VSL#3 group than in the placebo group (47.7% vs. 32.4%; PP P=0.069, CI₉₅(%) 0.36-0.60; ITT P=0.132, CI₉₅(%) 0.33-0.56). Eight patients on VSL#3 (11.2%) and nine patients on placebo (12.3%) reported mild side effects. CONCLUSIONS: VSL#3 supplementation is safe and able to reduce UCDAI scores in patients affected by relapsing mild-to-moderate UC who are under treatment with 5-ASA and/or immunosuppressants. Moreover, VSL#3 improves rectal bleeding and seems to reinduce remission in relapsing UC patients after 8 weeks of treatment, although these parameters do not reach statistical significance.
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The probiotic mixture VSL#3 reduces ulcerative colitis symptoms in adults and induces remission in children.
“In IBD, the probiotic mixture VSL#3, which contains bifidobacteria of different species, was able to reduce the UC symptoms in adults (144, 145) as well as the remission of the disease in children (84).”
From Bifidobacteria and Their Health-Promoting Effects (2017) · cites this paper as [145]
High doses of the multistrain probiotic VSL#3 improve disease activity scores in mild to moderate flares of ulcerative colitis.
“Both demonstrate that high doses improve disease activity scores”
From The gut microbiota and host health: a new clinical frontier (2016) · cites this paper as [74]
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BackgroundĐorđević, Đ., Jančíková, S., Vítězová, M., & Kushkevych, I. V. (2020) · Journal of Advanced Research · doi:10.1016/j.jare.2020.03.003 · Cited by 248 · see citing works
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“Two other large, well designed, randomized, placebo-controlled trials found significantly more patients with mild to moderately active UC to reach at least 50% improvement in clinical activity indices after VSL#3 compared with placebo treatment for 12 (n= 147)([79]) and 8 weeks (n = 144)([81]) based on ITT analyses.”
BackgroundMethodInfluentialvon Schillde, M., Hörmannsperger, G., Weiher, M., Alpert, C.-A., Hahne, H., Bäuerl, C., Huynegem, K. V., Steidler, L., Hrnčíř, T., Pérez‐Martínez, G., et al. (2012) · Cell Host & Microbe · doi:10.1016/j.chom.2012.02.006 · Cited by 235 · see citing works
Microbiota in inflammatory bowel disease: mechanisms of disease and therapeutic opportunities
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“An eight-strain mixture containing Lactobacillus spp., Bifidobacterium spp. and Streptococcus spp. (VSL#3, Actial) was more effective in inducing remission in mild-to-moderate UC than placebo 179 , as well as efficacy in preventing recurrent pouchitis 180 .”
Fedorak, R. N., Feagan, B. G., Hotte, N., Leddin, D., Dieleman, L. A., Petrunia, D. M., Enns, R. A., Bitton, A., Chiba, N., Paré, P., et al. (2014) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2014.10.031 · Cited by 230 · see citing works
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Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India
Kumari, R. (2013) · World Journal of Gastroenterology · doi:10.3748/wjg.v19.i22.3404 · Cited by 219 · see citing works
“Disease activity in UC patients was determined by simple clinical colitis activity index [18] and the patients with total index score of 7-10, > 10 and 0-2 were assigned moder - ate, severe and remission category, respectively [19] .”
Probiotics in Inflammatory Bowel Disease
Abraham, B. P., & Quigley, E. M. M. (2017) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2017.08.003 · Cited by 217 · see citing works
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ACG Clinical Guideline Update: Ulcerative Colitis in Adults
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“In one clinical trial using this probiotic as add-on therapy to 5-ASA, endoscopic improvement was not achieved (150).”
Gut Microbiota, Immunity, and Disease: A Complex Relationship
Kosiewicz, M. M., Zirnheld, A. L., & Alard, P. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00180 · Cited by 205 · see citing works
“…species (Bifidobacterium longum, Bifidobacterium breve, and Bifidobacterium infantis) and a Streptococcus salivarius subsp., Thermophilus, has been shown to decrease ulcerative colitis in patients with mild to moderately active ulcerative colitis (Sood et al., 2009; Tursi et al., 2010).”
BackgroundDevelopment of the Pediatric Gut Microbiome: Impact on Health and Disease
Ihekweazu, F. D., & Versalovic, J. A. (2018) · The American Journal of the Medical Sciences · doi:10.1016/j.amjms.2018.08.005 · Cited by 201 · see citing works
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Probiotics for maintenance of remission in ulcerative colitis
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The intestinal microbiota in inflammatory bowel disease
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“In several studies using VSL#3, treatment of patients with mild to moderate UC resulted in a combined induction of remission/response rate with no severe adverse effects (Sood et al. 2009; Tursi et al. 2010).”
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Probiotic Modulation of Innate Cell Pathogen Sensing and Signaling Events
Llewellyn, A., & Foey, A. (2017) · Nutrients · doi:10.3390/nu9101156 · Cited by 171 · see citing works
“Probiotics have been used to treat a range of health conditions encompassing intestinal and extraintestinal sites, including atopic dermatitis, necrotising enterocolitis, pouchitis and ulcerative colitis [142–144].”
Probiotics in the management of irritable bowel syndrome and inflammatory bowel disease
Whelan, K., & Quigley, E. M. M. (2013) · Current Opinion in Gastroenterology · doi:10.1097/mog.0b013e32835d7bba · Cited by 185 · see citing works
“boulardii, as well as Lactobacillus reuterii (by enema)([40]) and VSL#3([41]) in maintaining remission in ulcerative colitis and in treating mild to moderately active disease.”
BackgroundAhl, D., Liu, H., Schreiber, O., Roos, S., Phillipson, M., & Holm, L. (2016) · Acta Physiologica · doi:10.1111/apha.12695 · Cited by 181 · see citing works
The involvement of gut microbiota in inflammatory bowel disease pathogenesis: Potential for therapy
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“#3 probiotic mixture, administered for 6-12 weeks, in inducing the remission in patients with mildly-to-moderately active UC treated with conventional therapy (Bibiloni et al., 2005; Tursi et al., 2004; Tursi et al., 2010) or not receiving any other therapy (Lee et al., 2012; Sood et al., 2009).”
BackgroundSelf-citationIntestinal microbiota, probiotics and prebiotics in inflammatory bowel disease
Orel, R. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i33.11505 · Cited by 177 · see citing works
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Self-citationIniesta, M., Herrera, D., Montero, E., Zurbriggen, M. M., Matos, A. R. F., Marín, M. J., Sánchez‐Beltrán, M. C., Llama‐Palacios, A., & Sanz, M. (2012) · Journal Of Clinical Periodontology · doi:10.1111/j.1600-051x.2012.01914.x · Cited by 167 · see citing works
Probiotics, fibre and herbal medicinal products for functional and inflammatory bowel disorders
Currò, D., Ianiro, G., Pecere, S., Bibbò, S., & Cammarota, G. (2017) · British Journal of Pharmacology · doi:10.1111/bph.13632 · Cited by 160 · see citing works
“In several RCTs, it was effective in the induction of remission in patients with mild-to-moderate UC, together with conventional treatment (Tursi et al., 2004, 2010), or alone (Sood et al., 2009).”
MethodComplementary and Alternative Medicines Used by Patients With Inflammatory Bowel Diseases
Cheifetz, A. S., Gianotti, R. J., Luber, R. P., & Gibson, P. R. (2016) · Gastroenterology · doi:10.1053/j.gastro.2016.10.004 · Cited by 160 · see citing works
Microbiome therapeutics: exploring the present scenario and challenges
Yadav, M., & Chauhan, N. S. (2021) · Gastroenterology report · doi:10.1093/gastro/goab046 · Cited by 157 · see citing works
A Gastroenterologist's Guide to Probiotics
Ciorba, M. A. (2012) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2012.03.024 · Cited by 150 · see citing works
Probiotics for induction of remission in ulcerative colitis
Kaur, L., Gordon, M. A., Baines, P. A., Iheozor‐Ejiofor, Z., Sinopoulou, V., & Akobeng, A. K. (2020) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005573.pub3 · Cited by 148 · see citing works
“• Minor adverse events were reported in nine studies (Kato 2004; Liu 2014; Matthes 2010; Miele 2009; Sood 2009; Tamaki 2016; Tursi 2010; Vejdani 2017; Zhang 2018a).”
BackgroundMethodInfluentialDiet therapy for inflammatory bowel diseases: The established and the new
Durchschein, F., Petritsch, W., & Hammer, H. F. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i7.2179 · Cited by 146 · see citing works
Probiotic mixture VSL# 3: An overview of basic and clinical studies in chronic diseases
Cheng, F.-S., Pan, D., Chang, B., Jiang, M., & Sang, L.-X. (2020) · World Journal of Clinical Cases · doi:10.12998/wjcc.v8.i8.1361 · Cited by 147 · see citing works
Large-scale association analyses identify host factors influencing human gut microbiome compositionPreprint
Kurilshikov, A., Medina‐Gómez, C., Bacigalupe, R., Radjabzadeh, D., Wang, J., Demirkan, A., Roy, C. I. L., Garay, J. A. R., Finnicum, C. T., Liu, X., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.26.173724 · Cited by 143 · see citing works
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“Clinical studies have shown that probiotics can alleviate the symptoms of UC (Tursi et al. 2010) and maintain clinical remission (Yoshimatsu et al.”
BackgroundProbiotic Mix VSL#3 Is Effective Adjunctive Therapy for Mild to Moderately Active Ulcerative Colitis
Mardini, H. E., & Grigorian, A. Y. (2014) · Inflammatory Bowel Diseases · doi:10.1097/mib.0000000000000084 · Cited by 140 · see citing works
VSL#3 can prevent ulcerative colitis-associated carcinogenesis in mice
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Dickerson, F., Adamos, M. B., Katsafanas, E., Khushalani, S., Origoni, A. E., Savage, C. L. G., Schweinfurth, L. A. B., Stallings, C. R., Sweeney, K., Goga, J. K., et al. (2018) · Bipolar Disorders · doi:10.1111/bdi.12652 · Cited by 138 · see citing works
Torres, J., Ellul, P., Langhorst, J., Mikocka‐Walus, A. A., Acosta, M. B., Basnayake, C., Ding, N. S., Gilardi, D., Katsanos, K. H., Moser, G., et al. (2019) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjz051 · Cited by 137 · see citing works
Appleyard, C. B., Cruz, M. L., Isidro, A., Arthur, J. C., Jobin, C., & Simone, C. D. (2011) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00167.2011 · Cited by 131 · see citing works
Role of nutrition and microbiota in susceptibility to inflammatory bowel diseases
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The long-term effects of probiotics in the therapy of ulcerative colitis: A clinical study
Palumbo, V. D., Romeo, M., Marino, A., Carini, F., Damiani, P., Damiano, G., Buscemi, S., Monte, A. I. L., Geagea, A. G., Jurjus, A. R., et al. (2016) · Biomedical Papers · doi:10.5507/bp.2016.044 · Cited by 130 · see citing works
AGA Technical Review on the Management of Mild-to-Moderate Ulcerative Colitis
Singh, S., Feuerstein, J. D., Binion, D. G., & Tremaine, W. J. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.12.008 · Cited by 130 · see citing works
Cionci, N. B., Baffoni, L., Gaggìa, F., & Gioia, D. D. (2018) · Nutrients · doi:10.3390/nu10111723 · Cited by 130 · see citing works
“#3 administration in patients with diarrhoea predominant-IBS or functional diarrhoea; the probiotic intake caused changes in gut microbiota composition with a significantly increase of total lactobacilli, total bifidobacteria and S. thermophilus, which are component of VSL#3.”
ResultInfluentialAGA Technical Review on the Role of Probiotics in the Management of Gastrointestinal Disorders
Preidis, G. A., Weizman, A. V., Kashyap, P., & Morgan, R. L. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.05.060 · Cited by 135 · see citing works
Emerging pharmacotherapy for inflammatory bowel diseases
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Diet, gut microbes, and the pathogenesis of inflammatory bowel diseases
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Probiotics, Prebiotics and Synbiotics in Inflammatory Bowel Diseases
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“2010 [41] 144 adults higher efficacy of probiotic mixture as add-on therapy to conventional treatment in patients with relapsing disease compared to placebo”
BackgroundProbiotics and prebiotics in ulcerative colitis
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“The relatively low costs and excellent safety profile of probiotics and prebiotics make these therapies attractive for implementation into current treatment regimens [18,28,37].”
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Impact of air pollution on intestinal redox lipidome and microbiome
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Modulation of microbiota as treatment for intestinal inflammatory disorders: An uptodate
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Self-citationFecal Microbiota Transplantation for Ulcerative Colitis: A Systematic Review and Meta-Analysis
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Relationship between gut microbiota and development of T cell associated disease
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Probiotics modify human intestinal mucosa-associated microbiota in patients with colorectal cancer
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“Studies in animal models and humans have demonstrated that the consumption of probiotics is effective in various medical conditions, can delay senility (22), and improve acute infectious diarrhea (23,24), antibiotic‐associated diarrhea (21,25), constipation (26‐28), ulcerative colitis (29,30) and Crohn's disease (31,3…”
BackgroundProbiotics ameliorate intestinal pathophysiology in a mouse model of Alzheimer’s disease
Kaur, H., Nagamoto‐Combs, K., Golovko, S. A., Golovko, M. Y., Klug, M. G., & Combs, C. K. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.04.009 · Cited by 112 · see citing works
Prebiotics and Probiotics for Gastrointestinal Disorders
Rau, S., Gregg, A., Yaceczko, S. D., & Limketkai, B. N. (2024) · Nutrients · doi:10.3390/nu16060778 · Cited by 121 · see citing works
“® at 3600 × 10 9 CFU/day to improve disease activity scores and rectal bleeding, although the differences were not significantly different from placebo [145].”
BackgroundProbiotics for the Treatment of Inflammatory Bowel Disease
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- Authors
- Tursi, A., Brandimarte, G., Papa, A., Giglio, A., Elisei, W., Giorgetti, G. M., Forti, G., Morini, S., Hassan, C., Pistoia, M. A., Modeo, M. E., Rodino', S., D'Amico, T., Sebkova, L., Sacca', N., Di Giulio, E., Luzza, F., Imeneo, M., Larussa, T., Di Rosa, S., Annese, V., Danese, S., & Gasbarrini, A.
- Affiliations
- Ospedale L. Bonomo (IT)
- Ospedale Cristo Re (IT)
- Agostino Gemelli University Polyclinic (IT)
- Azienda Ospedaliera Pugliese Ciaccio (IT)
- St. Eugenio Hospital (IT)
- Ospedale Santa Maria Goretti (IT)
- Azienda Universitaria Ospedaliera Consorziale - Policlinico Bari (IT)
- Azienda Ospedaliero-Universitaria "Renato Dulbecco" (IT)
- Casa Sollievo della Sofferenza (IT)
- Corresponding author
- Tursi, Antonio
- ORCID
- Venue
- American Journal of Gastroenterology
- Published
- 2010-10
- Volume
- 105
- Issue
- 10
- Pages
- 2218-2227
- ISSN
- 0002-9270 (ISSN-L)
- PMC
- PMC3180711
- OpenAlex
- W1998335236
- Cited by
- 489
- References
- 39
- Citations by year
- 2026: 10 · 2025: 22 · 2024: 35 · 2023: 30 · 2022: 29 · 2021: 28 · 2020: 46 · 2019: 31 · 2018: 39 · 2017: 38 · 2016: 28 · 2015: 29 · 2014: 38 · 2013: 27 · 2012: 28
- FWCI
- 15.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (unspecified)
- Locations
- The American Journal of Gastroenterology (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- Archivio Istituzionale della Ricerca - Università degli Studi dell Aquila (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- ulcerative colitis, VSL#3, probiotics, adjunctive therapy, relapsing disease, 5-aminosalicylic acid, immunosuppressants, disease activity, rectal bleeding, stool frequency, inflammatory bowel disease treatment, pouchitis, Crohn's disease, irritable bowel syndrome, irritable bowel syndrome with diarrhea
- MeSH terms
- Adult, Azathioprine, Bifidobacterium, Colitis, Ulcerative, Combined Modality Therapy, Double-Blind Method, Female, Humans, Lactobacillus, Male, Middle Aged, Recurrence, Remission Induction, Severity of Illness Index, Treatment Outcome, Patient Selection, Mesalamine, Probiotics, Streptococcus thermophilus
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