Irritable bowel syndrome and probiotics: from rationale to clinical use Elena F. Verdu and Stephen M. Collins

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1 Irritable bowel syndrome and probiotics: from rationale to clinical use Elena F. Verdu and Stephen M. Collins Purpose of review Few therapies are of proven efficacy in irritable bowel syndrome. Thus, there is great interest in the development of a natural therapy that can be both safe and effective. An understanding that probiotics are heterogeneous, with multiple targets and mechanisms of action, is fundamental to the development of clinical trials. Recent findings A bidirectional model for the pathogenesis of irritable bowel syndrome is proposed in which gut-driven and brain-driven mechanisms contribute to the genesis of gut dysfunction and symptoms. In-vitro and animal studies have generated most of the mechanistic rationale for the use of probiotics in functional bowel disorders. A MEDLINE search of publications from 1989 to date revealed only eight placebo-controlled clinical trials on the subject of probiotics and irritable bowel syndrome. All these studies suffer from methodologic problems. By contrast, numerous reviews have been published in the past 2 years on this subject. Summary Animal research will continue to identify novel targets and elucidate the mechanisms of action of probiotics, thus providing a rational basis for their use in irritable bowel syndrome. The notion of treating irritable bowel syndrome with probiotics is particularly attractive to patients and generates great interest, although clinical evidence is not yet sufficient to enable clear guidelines to be designed. Large, well-designed, controlled clinical trials using specific probiotics are warranted. Keywords functional bowel disorders, gut dysfunction, irritable bowel syndrome, probiotics Curr Opin Gastroenterol 21: ª 2005 Lippincott Williams & Wilkins. Intestinal Disease Research Programme, McMaster University, Hamilton, Ontario, Canada Correspondence to Elena F Verdu, 1200 Main Street West, McMaster University, Hamilton, Ontario, Canada Tel: x22212; fax: ; verdue@mcmaster.ca Current Opinion in Gastroenterology 2005, 21: Abbreviations IBS irritable bowel syndrome PI-IBS postinfective irritable bowel syndrome ª 2005 Lippincott Williams & Wilkins Introduction In this review we discuss the gut-driven pathophysiologic pathways involved in gut dysfunction and symptom generation in irritable bowel syndrome (IBS), including immune activation, dysmotility, altered mucosal barrier function, and visceral perception. This allows us to logically review the possible targets of probiotic therapy in IBS. Finally, we evaluate the relevant clinical trials published to date on probiotics and IBS. Gut dysfunction in irritable bowel syndrome The current goal of treatment in IBS is to alleviate symptoms and improve quality of life. The gut-driven pathophysiologic mechanisms believed to be involved in the origin or maintenance of IBS symptoms include intestinal infection and immune activation, dysmotility, abnormal fermentation, and visceral hypersensitivity [1 4,5,6 10]. Therapeutic approaches targeting some of these mechanisms have been developed and used with varied clinical efficacy [11]. Increased intestinal permeability and abnormal central processing of peripheral stimuli have also been proposed as possible mechanisms leading to or exacerbating IBS symptoms [12]. Changes in gut permeability have been demonstrated in postinfective IBS (PI-IBS), but this has not been proved in the unselected IBS population [2]. It is the opinion of the authors that low-grade inflammation is the basis for gut dysfunction in a proportion of patients with IBS. A recent study has shown that Bifidobacterium infantis improved systemic cytokine abnormalities and normalized symptoms in IBS patients [13 ]. This raises the possibility that specific probiotics may modify the natural history of IBS. Immune activation in irritable bowel syndrome Infectious gastroenteritis is the most significant environmental risk factor identified to date for the development of IBS [1]. IBS symptoms have been reported to develop in a significant proportion of individuals with documented Campylobacter, Salmonella, Escherichia coli, and Shigella infection as well as viral infection [2,14 16]. Evidence of immune activation is not restricted to patients with PI-IBS, and it has also been reported in a proportion of unselected IBS patients with no history of gastroenteritis [2 4,5,17]. 697

2 698 Immunology There is evidence for an imbalance in the genetic regulation of counterinflammatory cytokine secretion in patients with IBS [18]. This may promote a defective downregulation of immune responses to normal inflammatory stimuli in IBS. A recent study by Van Der Veek et al. [19] demonstrated changes in the genetic control of cytokines that play a critical role in regulating inflammation in the gut. The combination of genotypes encoding for high tumor necrosis factor-a secretion, a proinflammatory cytokine, and low interleukin-10 secretion, a counterregulatory cytokine, was significantly more prevalent in IBS patients than in control individuals. Phenotypic evidence demonstrating a lower ration of interleukin-10 to tumor necrosis factor-a in IBS patients has recently confirmed these earlier genotypic studies [13 ]. Putative mechanisms of action of probiotics in irritable bowel syndrome Inflammatory bowel syndrome is heterogeneous both in its clinical presentation and in its pathogenesis. No treatment to date has been proved to be substantially effective, although a recent study by O Mahony et al. [13 ]is encouraging. Probiotics may target one or more pathophysiologic pathways in IBS, and specific probiotics with more than one mechanism of action may prove to be an attractive natural approach compared with conventional drug therapy for patients with IBS. Eventually, combinations of specific strains carefully selected on the basis of documented targets in the gastrointestinal tract may provide the best therapeutic approach. A recent metaanalysis has shown that probiotic therapy reduces the duration of infectious diarrhea in children [20]. This is particularly relevant to PI-IBS, in which a shorter duration of the initial gastroenteritis episode or prevention of colonization by pathogens may reduce the risk for the subsequent development of IBS [21,22]. Numerous studies have demonstrated antiinflammatory effects of probiotics in animal models of inflammatory bowel disease [23,24]. We have shown in a murine model of PI-IBS that Lactobacillus paracasei NCC2461 attenuates postinfective muscle contractility, in part through modulation of the inflammatory response to infection [25 ]. Recently, L. salivarius UCC4331 and B. infantis have been shown to reduce an abnormal systemic ratio of interleukin-10 to interleukin-12 in patients with IBS [13 ]. Lactobacillus farciminis was shown to enhance barrier function and prevent bacterial translocation in trinitrobenzene sulfonic acid-induced colitis in rats [26]. Others have been unable to detect an improvement in gut permeability after trinitrobenzene sulfonic acid-induced colitis following administration of L. plantarum 299 (LP299). Human studies suggest that L. rhamnosus and L. reuteri DSM stabilize intestinal barrier function in children with atopic dermatitis [27]. Other studies, however, using a variety of probiotic species in critically ill patients, failed to demonstrate improvement in intestinal permeability despite favorable changes in the systemic inflammatory response and the microbial composition of the gastrointestinal tract [28,29]. The identification of subgroups of IBS patients in whom barrier dysfunction underlies symptom generation should be a prior logical step to the application of probiotic therapy to target barrier dysfunction. Dysmotility is considered to underlie altered bowel habit, which is a common symptom in IBS patients. Until recently, the neuromuscular apparatus was not considered as a possible target for probiotic therapy, presumably because of its distance from the lumen. Of five different probiotic species tested, only L. paracasei was able to significantly attenuate muscle dysfunction in the model of Trichinella spiralis-induced IBS. The beneficial effect was observed even when the probiotic was administered long after resolution of the initial infection [25]. L. paracasei significantly improved postinfective dysmotility in vivo, as assessed by video fluoroscopy and image analysis. Oral administration of spent culture medium from L. paracasei, devoid of live bacteria, also improved postinfective dysmotility [30]. Taken together, these studies demonstrate that specific probiotics may target the neuromuscular apparatus and improve muscle function in PI-IBS. Bloating and abdominal distension is commonly present in patients with IBS. Dysmotility and consequently difficulty in propelling gas may underlie these symptoms. King et al. [31] have shown a greater gas production in IBS patients than in control individuals, which suggests that abnormal fermentation may be responsible for bloating in some IBS patients. Probiotics aimed at reducing abnormal fermentation may be useful only in those patients in whom abnormal fermentation due to altered flora can be documented [32]. Pain is a cardinal symptom in IBS, and visceral hypersensitivity is believed to underlie this symptom. There is some evidence that specific probiotics may modulate neurotransmission in the gut. The administration of Saccaromyces boulardii to pigs has been shown to modulate the expression of neuronal markers in the submucous plexus [33]. L. farciminis has been shown to attenuate visceral hypersensitivity in rats [26]. We have found that the administration of L. paracasei NCC2461 attenuates the visceral hypersensitivity and sensory neurotransmitter expression associated with antibiotic administration [34]. Taken together, these results raise the possibility that specific probiotics may affect neurotransmission and modulate visceral perception. Considerable research is required in this area, both in animal models of IBS and in IBS patients.

3 Irritable bowel syndrome and probiotics Verdu and Collins 699 Clinical studies Several uncontrolled studies have claimed beneficial effects of probiotics in functional bowel disorders. This review is limited to the eight placebo-controlled trials shown in Table 1 [13,35 41]. Streptococcus faecium was administered for 4 weeks to patients presenting with functional bowel symptoms for at least 6 months. The physicians overall assessment after 4 weeks of treatment determined that 81% of patients taking S. faecium reported a beneficial effect, compared with 41% of patients taking placebo [35]. Other studies have reported improvement in specific symptoms, which suggests a role for altered microbial flora in symptom generation in IBS. L. plantarum DSM 9843, but not placebo, decreased flatulence in patients with IBS; however, pain was reduced in both probiotic-treated and placebo-treated individuals [36]. L. plantarum has been used in other studies, with conflicting results. Sen et al [37] administered L. plantarum 299V or placebo to IBS patients in a crossover fashion. No beneficial effect was observed on colonic fermentation or symptoms after administration of the probiotic. By contrast, Saggioro [38] reported a significant decrease in pain using a either a combination of L. plantarum LP01 with B. breve BR0 or a combination of L. plantarum LP01 with L. acidophilus LA01. Neidzielin et al [39] reported resolution of abdominal pain in patients receiving L. plantarum 299V in comparison with placebo-treated patients. A study using L. casei strain GG did not find significant improvement in symptoms in patients with IBS; however, a subgroup of patients with diarrhea-predominant symptoms showed a trend toward a decrease in the number of loose stools when treated with this probiotic [40]. Kim et al [41] administered a cocktail of eight probiotic strains (VSL#3) to diarrhea-predominant IBS patients. The only symptom that was significantly reduced in patients randomized to VSL#3 for 8 weeks was abdominal bloating (Table 1). A recent study examined the effect of two probiotics, L. salivarius UCC4331 and B. infantis 35624, in patients fulfilling the Rome II criteria for IBS. Patients were randomized to receive either one of the two probiotics or placebo for 8 weeks. Symptoms of IBS were recorded daily and assessed each week. Quality of life assessment, stool microbiologic studies, and blood sampling were performed at the beginning and at the end of treatment. The patients receiving B. infantis had decreased composite symptom scores for every week during treatment and during the 4-week washout period. L. salivarius achieved a significant reduction of the symptom score only during the second week of treatment. Surprisingly, and despite improvement in composite symptom scores, quality of life was not improved in patients treated with probiotics [13]. One finding that distinguishes this study from the previous trials is that patients with IBS showed a reduced basal systemic ratio of interleukin-10 to interleukin-12 and that this was normalized by specific probiotic administration. The reported altered ratio of interleukin-10 to interleukin-12 is consistent with the hypothesis that in a substantial proportion of patients with IBS, gut dysfunction and symptom origin are immune mediated. All clinical trials performed to date are subject to methodologic caveats, including low numbers of patients and dubious statistical analysis. Moreover, comparison between trials is hampered by the different inclusion criteria, the heterogeneity of IBS patients, the different probiotic preparations, and the treatment protocols used; however, it is the opinion of the authors of this review that although there is not enough evidence to enable clear guidelines to be drawn for the use of any specific probiotic in IBS, larger well-designed clinical studies are warranted. This may prove to be a long way off because extrapolations from results with one probiotic to another, including Table 1. Placebo-controlled probiotic studies in irritable bowel syndrome (IBS). Study Probiotic Inclusion criteria No. Design Symptoms improved Gade and Thorn [35] Streptococcus faecium Functional lower bowel 54 Randomized Overall symptom score symptoms Nobaek et al. [36] Lactobacillus plantarum Rome I (all IBS) 60 Randomized Flatulence O Sullivan and O Morain [40] Lactobacillus casei GG Rome I (all IBS) 24 Crossover None Niedzielin et al. [39] Lactobacillus plantarum Manning (all IBS) 40 Randomized Pain Sen et al. [37] Lactobacillus plantarum Rome I (all IBS) 12 Crossover None Kim et al. [41] VSL#3 Rome II (diarrhea 25 Randomized Bloating predominant) Saggioro [38] Lactobacillus plantarum, Rome (all IBS) 70 Randomized Overall symptom score Lactobacillus acidophilus, Bifidobacterium breve O Mahony et al. [13] Lactobacillus salivarius, Bifidobacterium infantis Rome II 75 Randomized Overall composite score VSL#3, bifidobacteria (B. longum, B. infantis, B. breve); lactobacilli (L. acidophilus, L. casei, L. bulgaricus, L. plantarum); Streptococcus salivarius subspecies termophilus.

4 700 Immunology from the same species but a different strain, seem to be inappropriate. Conclusion Considerable research is still needed in the area of probiotics and IBS. Basic research will be useful in identifying potential probiotic strains and gastrointestinal targets. These strains can be then tested in large well-designed clinical trials. Although extrapolation from animal studies to clinical trials is not always possible, this is the only sensible practical approach that will select potentially useful probiotic strains on a pathophysiologic basis. Clinical studies will be crucial to elaborate clear guidelines for the use of probiotics in IBS. Larger clinical studies using specific probiotic strains are needed. Ideally, these studies should apply probiotic strains with known therapeutic targets previously determined in animal models and should include symptom and quality of life assessments as well as objective markers of intestinal immune activation and gut function. References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as: of special interest of outstanding interest Additional references related to this topic can also be found in the Current World Literature section in this issue (p. 740). 1 Rodriguez LA, Ruigomez A. Increased risk of irritable bowel syndrome after bacterial gastroenteritis: cohort study. BMJ 1999; 318: Spiller RC, Jenkins D, Thornley JP, et al. Increased rectal mucosal enteroendocrine cells, T lymphocytes, and increased gut permeability following acute Campylobacter enteritis and in post-dysenteric irritable bowel syndrome. Gut 2000; 47: Gwee KA, Collins SM, Read NW, et al. Increased rectal mucosal expression of interleukin-1beta in recently acquired post-infectious irritable bowel syndrome. Gut 2003; 52: Chadwick VS, Chen W, Shu D, et al. Activation of the mucosal immune system in irritable bowel syndrome. Gastroenterology 2002; 122: Barbara G, Stanghellini V, De Giorgio R, et al. Activated mast cells in proximity to colonic nerves correlate with abdominal pain in irritable bowel syn- drome. Gastroenterology 2004; 126: This was the first study to demonstrate a correlation between activated mast cells and symptom severity in IBS patients. 6 Cann PA, Read NW, Brown C, et al. Irritable bowel syndrome: relationship of disorders in the transit of a single solid meal to symptom patterns. Gut 1983; 24: King TS, Elia M, Hunter OH. Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998; 352: Mertz H, Naliboff B, Munakata J, et al. Altered rectal perception is a biological marker of patients with irritable bowel syndrome. Gastroenterology 1995; 109: Whitehead WE, Holtkotter B, Enck P, et al. Tolerance for rectosigmoid distension in irritable bowel syndrome. Gastroenterology 1990; 98: Naliboff BD, Munkata J, Fullerton S, et al. Evidence for twodistinct perceptual alterations in irritable bowel syndrome. Gut 1997; 41: Lesbros-Pantoflickova D, Michetti P, Fried M, et al. Meta-analysis: the treatment of irritable bowel syndrome. Aliment Pharmacol Ther 2004; 20: Silverman DH, Munakata JA, Ennes H, et al. Regional cerebral activity in normal and pathological perception of visceral pain. Gastroenterology 1997; 112: O Mahony L, McCarthy J, Kelly P, et al. Lactobacilli and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005; 128: This clinical trial demonstrated an imbalance in systemic proinflammatory and counterinflammatory cytokines that can be corrected by specific probiotic therapy. 14 Neal KR, Hebden J, Spiller R. Prevalence of gastrointestinal symptoms six months after bacterial gastroenteritis and risk factors for development of the irritable bowel syndrome: postal survey of patients. BMJ 1997; 314: Wang LH, Fang XC, Pan GZ. Bacillary dysentery as a causative factor of irritable bowel syndrome and its pathogenesis. Gut 2004; 53: James C, Thabane M, Borgaonkar M, Marshall J. Post-infectious irritable bowel syndrome is transient following a foodborne outbreak of acute gastroenteritis attributed to a viral pathogen. Gastroenterology 2004; 126(suppl 2): A Tornblom H, Lindberg G, Nyberg B, Veress B. Full-thickness biopsy of the jejunum reveals inflammation and enteric neuropathy in irritable bowel syndrome. Gastroenterology 2002; 123: Gonsalkorale WM, Perrey C, Pravica V, et al. Interleukin 10 genotypes in irritable bowel syndrome: evidence for an inflammatory component? Gut 2003; 52: Van der Veek, de Kroon Y, van der Berg M, et al. Tumor necrosis factor alpha and interleukin 10 gene polymorphism in irritable bowel syndrome. Gastroenterology 2004; 126(suppl 2):A Huang JS, Bousvaros A, Lee JW, et al. Efficacy of probiotic use in acute diarrhea in children: a meta-analysis. Dig Dis Sci 2002; 47: Isolauri E, Kirjavainen PV, Salminen S. Probiotics: a role in the treatment of intestinal infection and inflammation? Gut 2002; 50: Resta-Lenert S, Barrett KE. Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC). Gut 2003; 52: Madsen KL, Doyle JS, Jewell LD, et al. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 1999; 116: Schultz M, Strauch UG, Linde HJ, et al. Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin Diagn Lab Immunol 2004; 11: Verdu EF, Bercik P, Bergonzelli GE, et al. Lactobacillus paracasei normalizes muscle hypercontractility in a murine model of postinfective gut dysfunction. Gastroenterology 2004; 127:82. This was the first study to demonstrate the differential effects of probiotic strains on neuromuscular function in a model of PI-IBS. 26 Lamine F, Eutamene H, Fioramonti J, et al. Colonic responses to Lactobacillus farciminis treatment in trinitrobenzene sulphonic acid-induced colitis in rats. Scand J Gastroenterol 2004; 39: Rosenfeldt V, Benfeldt E, Valerius NH, et al. Effect of probiotics on gastrointestinal symptoms and small intestinal permeability in children with atopic dermatitis. J Pediatr 2004; 145: Jain PK, McNaught CE, Anderson ADG, et al. Influence of symbiotic containing Lactobacillus acidophilus La5, Bifidobacterium lactis Bb 12, Streptococcus thermophilus, Lactobacillus bulgaricus and oligofructose on gut barrier function and sepsis in critically ill patients: a randomized controlled trial. Clin Nutr 2004; 23: McNaught CE, Woodcock NP, Anderson AD, Macfie J. A prospective randomized trial of probiotics in critically ill patients. Clin Nutr 2005; 24: Verdú EF, Bercik P, Bergonzelli G, et al. Lactobacillus paracasei normalizes post-infective dysmotility in vivo and induces a sustained attenuation of inflammatory mediators. Gastroenterology 2004; 126(suppl 2):A King TS, Elia M, Hunter JO. Abnormal colonic fermentation in irritable bowel syndrome. Lancet 1998; 352: Balsari A, Ceccarelli A, Dubini F, et al. The fecal microbial population in the irritable bowel syndrome. Microbiologica 1982; 5: Kamm K, Hoppe S, Breves G, et al. Effects of the probiotic yeast Saccharomyces boulardii on the neurochemistry of myenteric neurons in pig jejunum. Neurogastroenterol Motil 2004; 16:53 60.

5 Irritable bowel syndrome and probiotics Verdu and Collins Verdú EF, Bercik P, Verma-Gandhu M, et al. Specific probiotic therapy attenuates antibiotic-induced visceral hypersensivity in mice. Gut 2005 [Epub ahead of print]. 35 Gade J, Thorn P. Paraghurt for patients with irritable bowel syndrome: a controlled clinical investigation from general practice. Scand J Prim Health Care 1989; 7: Nobaek S, Johansson ML, Molin G, et al. Alteration of intestinal microflora is associated with reduction in abdominal bloating and pain in patients with irritable bowel syndrome. Am J Gastroenterol 2000; 95: Sen S, Mullan MM, Parker TJ, et al. Effect of lactobacillus plantarum 299v on colonic fermentation and symptoms of irritable bowel syndrome. Dig Dis Sci 2002; 47: Saggioro A. Probiotics in the treatment of irritable bowel syndrome. J Clin Gastroenterol 2004; 38:S104 S Niedzielin K, Kordecki H, Birkenfeld B. A controlled, double-blind, randomized study on the efficacy of lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol 2001; 13: O Sullivan MA, O Morain CA. Bacterial supplementation in the irritable bowel syndrome: a randomized double-blind placebo-controlled cross-over study. Dig Liver Dis 2000; 32: Kim HJ, Camilleri M, McKinzie S, et al. A randomized controlled trial of a probiotic, VSL#3, on gut transit and symptoms in diarrhoea-predominant irritable bowel syndrome. Aliment Pharmacol Ther 2003; 17:

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