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Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects

  • Michaël Messaoudi (a1), Robert Lalonde (a2), Nicolas Violle (a1), Hervé Javelot (a3), Didier Desor (a4), Amine Nejdi (a1), Jean-François Bisson (a1), Catherine Rougeot (a5), Matthieu Pichelin (a6), Murielle Cazaubiel (a6) and Jean-Marc Cazaubiel (a6)...
Abstract

In a previous clinical study, a probiotic formulation (PF) consisting of Lactobacillus helveticus R0052 and Bifidobacterium longum R0175 (PF) decreased stress-induced gastrointestinal discomfort. Emerging evidence of a role for gut microbiota on central nervous system functions therefore suggests that oral intake of probiotics may have beneficial consequences on mood and psychological distress. The aim of the present study was to investigate the anxiolytic-like activity of PF in rats, and its possible effects on anxiety, depression, stress and coping strategies in healthy human volunteers. In the preclinical study, rats were daily administered PF for 2 weeks and subsequently tested in the conditioned defensive burying test, a screening model for anti-anxiety agents. In the clinical trial, volunteers participated in a double-blind, placebo-controlled, randomised parallel group study with PF administered for 30 d and assessed with the Hopkins Symptom Checklist (HSCL-90), the Hospital Anxiety and Depression Scale (HADS), the Perceived Stress Scale, the Coping Checklist (CCL) and 24 h urinary free cortisol (UFC). Daily subchronic administration of PF significantly reduced anxiety-like behaviour in rats (P < 0·05) and alleviated psychological distress in volunteers, as measured particularly by the HSCL-90 scale (global severity index, P < 0·05; somatisation, P < 0·05; depression, P < 0·05; and anger–hostility, P < 0·05), the HADS (HADS global score, P < 0·05; and HADS-anxiety, P < 0·06), and by the CCL (problem solving, P < 0·05) and the UFC level (P < 0·05). L. helveticus R0052 and B. longum R0175 taken in combination display anxiolytic-like activity in rats and beneficial psychological effects in healthy human volunteers.

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*Corresponding author: M. Messaoudi, fax +33 383 446 441, email mmessaoudi@etap-lab.com
References
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1Forsythe P, Sudo N, Dinan T, et al. (2010) Mood and gut feelings. Brain Behav Immun 24, 916.
2Mayer EA (2000) The neurobiology of stress and gastrointestinal disease. Gut 47, 861869.
3McEwen BS (2003) Mood disorders and allostatic load. Biol Psychiatry 54, 200207.
4O'Mahony SM, Marchesi JR, Scully P, et al. (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65, 263267.
5Lutgendorff F, Akkermans LM & Söderholm JD (2008) The role of microbiota and probiotics in stress-induced gastro-intestinal damage. Curr Mol Med 8, 282298.
6Drossman DA, Sandler RS & McKee DC (1982) Bowel patterns among subjects not seeking health care. Gastroenterology 83, 529534.
7Whitehead WE, Crowell MD, Robinson JC, et al. (1992) Effects of stressful life events on bowel symptoms: subjects with irritable bowel syndrome compared with subjects without bowel dysfunction. Gut 33, 825830.
8Gwee KA (1999) The role of psychological and biological factors in post-infective gut dysfunction. Gut 44, 400406.
9Duffy LC, Zielezny MA, Marshall JR, et al. (1991) Relevance of major stress events as an indicator of disease activity prevalence in inflammatory bowel disease. Behav Med 17, 101110.
10Garrett VD, Brantley PJ, Jones G, et al. (1991) The relationship between daily stress and Crohn's disease. J Behav Med 14, 8796.
11Greene B & Blanchard EB (1994) Cognitive therapy for irritable bowel syndrome. J Consult Clin Psychol 62, 576582.
12Bennett EJ, Tennant CC, Piesse C, et al. (1998) Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 43, 256261.
13Levenstein S, Kaplan GA & Smith MW (1997) Psychological predictors of peptic ulcer incidence in the Alameda County Study. J Clin Gastroenterol 24, 140146.
14Levenstein S, Ackerman S, Kiecolt-Glaser JK, et al. (1999) Stress and peptic ulcer disease. JAMA 281, 1011.
15Levenstein S, Prantera C, Varvo V, et al. (2000) Stress and exacerbation in ulcerative colitis: a prospective study of patients enrolled in remission. Am J Gastroenterol 95, 12131220.
16Aoyama N, Kinoshita Y, Fujimoto S, Himeno S, et al. (1998) Peptic ulcers after the Hanshin-Awaji earthquake: increased incidence of bleeding gastric ulcers. Am J Gastroenterol 93, 311316.
17Finlay-Jones R & Brown GW (1981) Types of stressful life event and the onset of anxiety and depressive disorders. Psychol Med 11, 803815.
18Caspi A, Sugden K, Moffitt TE, et al. (2003) Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301, 386389.
19Kendler KS, Prescott CA, Myers J, et al. (2003) The structure of genetic and environmental risk factors for common psychiatric and substance use disorders in men and women. Arch Gen Psychiatry 60, 929937.
20Wheatley D (1998) Stress, anxiety and depression. Stress Med 13, 173177.
21Whitehead WE, Palsson O & Jones KR (2002) Systematic review of the comorbidity of irritable bowel syndrome with other disorders: what are the causes and implications? Gastroenterology 122, 11401156.
22Graff LA, Walker JR & Bernstein CN (2009) Depression and anxiety in inflammatory bowel disease: a review of comorbidity and management. Inflamm Bowel Dis 15, 11051118.
23Neufeld KA & Foster JA (2009) Effects of gut microbiota on the brain: implications for psychiatry. J Psychiatry Neurosci 34, 230231.
24Goehler LE, Park SM, Opitz N, et al. (2007) Campylobacter jejuni infection increases anxiety-like behavior in the holeboard: possible anatomical substrates for viscerosensory modulation of exploratory behavior. Brain Behav Immun 22, 354366.
25Sudo N, Chida Y, Aiba Y, et al. (2004) Postnatal microbial colonization programs the hypothalamic–pituitary–adrenal system for stress response in mice. J Physiol 558, 263275.
26Söderholm JD, Yates DA, Gareau MG, et al. (2002) Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress. Am J Physiol Gastrointest Liver Physiol 283, G1257G1263.
27Coutinho SV, Plotsky PM, Sablad M, et al. (2002) Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 282, G307G316.
28Gareau MG, Jury J, MacQueen G, et al. (2007) Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut 56, 15221528.
29Girard SA, Bah TM, Kaloustian S, et al. (2009) Lactobacillus helveticus and Bifidobacterium longum in combination reduce the apoptosis propensity in the limbic system after myocardial infarction in a rat model. Br J Nutr 102, 14201425.
30Bailey MT, Lubach GR & Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38, 414421.
31Qin J, Li R, Raes J, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 5965.
32Pineiro M & Stanton C (2007) Probiotic bacteria: legislative framework – requirements to evidence basis. J Nutr 137, 850S853S.
33Arvanitoyannis IS & Van Houwelingen-Koukaliaroglou M (2005) Functional foods: a survey of health claims, pros and cons, and current legislation. Crit Rev Food Sci Nutr 45, 385404.
34Diop L, Guillou S & Durand H (2008) Probiotic food supplement reduces stress-induced gastrointestinal symptoms in volunteers: a double-blind, placebo-controlled, randomized trial. Nutr Res 28, 15.
35Estrada A, Drew MD & Van Kessel A (2001) Effect of the dietary supplementation of fructooligosaccharides and Bifidobacterium longum to early-weaned pigs on performance and fecal bacterial populations. Can J Anim Sci 81, 141148.
36Wine E, Gareau MG, Johnson-Henry K, et al. (2009) Strain-specific probiotic (Lactobacillus helveticus) inhibition of Campylobacter jejuni invasion of human intestinal epithelial cells. FEMS Microbiol Lett 300, 146152.
37Wallace TD, Bradley S, Buckley ND, et al. (2003) Interactions of lactic acid bacteria with human intestinal epithelial cells: effects on cytokine production. J Food Prot 66, 466472.
38Haskey N & Dahl WJ (2009) Synbiotic therapy improves quality of life and reduced symptoms in pediatric ulcerative colitis. Infant Child Adoles Nutr 1, 8893.
39Yamamura S, Morishima H, Kumano-go T, et al. (2009) The effect of Lactobacillus helveticus fermented milk on sleep and health perception in elderly subjects. Eur J Nutr 63, 100105.
40Treit D, Pinel JP & Fibiger HC (1981) Conditioned defensive burying: a new paradigm for the study of anxiolytic agents. Pharmacol Biochem Behav 15, 619626.
41Messaoudi M, Lalonde R, Schroeder H, et al. (2009) Anxiolytic-like effects and safety profile of a tryptic hydrolysate from bovine alpha s1-casein in rats. Fundam Clin Pharmacol 23, 323330.
42Derogatis LR, Lipman RS, Rickels K, et al. (1974) The Hopkins Symptom Checklist (HSCL): a self-report symptom inventory. Behav Sci 19, 115.
43Derogatis LR, Lipman RS, Rickels K, et al. (1974) The Hopkins Symptom Checklist (HSCL). A measure of primary symptom dimensions. Mod Probl Pharmacopsychiatry 7, 79110.
44Zigmond AS & Snaith RP (1983) The Hospital Anxiety and Depression Scale. Acta Psychiatr Scand 67, 361370.
45Cohen S & Williamson G (1988) Perceived stress in a probability sample of the United States. In The Social Psychology of Health: Claremont Symposium on Applied Social Psychology, pp. 3167 [Spacapan S and Oskamp S, editors]. Newbury Park, CA: Sage.
46Vitaliano PP (1985) The Ways of Coping Checklist: revision and psychometric properties. Multiv Behav Res 20, 326.
47Paulhan I, Nuissier J, Quintard B, et al. (1994) The measurement of “coping”. French translation and validation of the Vitaliano's scale (Vitaliano et al. 1985). Ann Med Psychol (Paris) 152, 292299.
48Mason JW, Giller EL, Kosten TR, et al. (1986) Urinary free-cortisol levels in posttraumatic stress disorder patients. J Nerv Ment Dis 174, 145149.
49Martin FP, Rezzi S, Peré-Trepat E, et al. (2009) Metabolic effects of dark chocolate consumption on energy, gut microbiota, and stress-related metabolism in free-living subjects. J Proteome Res 8, 55685579.
50ASAB/ABS (2006) Guidelines for the treatment of animals in behavioural research and teaching. Anim Behav 71, 245253.
51Canadian Council on Animal Care (1993) Guide to the Care and Use of Experimental Animals, vol. 1, 2nd ed. Ottawa, ON: CCAC.
52Naser SM, Hagen KE, Vancanneyt M, et al. (2006) Lactobacillus suntoryeus Cachat and Priest 2005 is a later synonym of Lactobacillus helveticus (Orla-Jensen 1919) Bergey et al. 1925 (approved lists 1980). Int J Syst Evol Microbiol 56, 355360.
53Hagen KE, Tramp CA, Altermann E, et al. (2010) Sequence analysis of plasmid pIR52-1 from Lactobacillus helveticus R0052 and investigation of its origin of replication. Plasmid 63, 108117.
54Ventura M, Callegari ML, Morelli L, et al. (2000) S-layer gene as a molecular marker for identification of Lactobacillus helveticus. FEMS Microbiol Lett 189, 275279.
55Ventura M, Canchaya C, Meylan V, et al. (2003) Analysis, characterization, and loci of the tuf genes in Lactobacillus and Bifidobacterium species and their direct application for species identification. Appl Environ Microbiol 69, 69086922.
56Altschul SF, Madden TL, Schaffer AA, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 33893402.
57Bjelland I, Dahl AA & Haug TT (2002) The validity of the Hospital Anxiety and Depression Scale. An updated literature review. Psychosom Res 52, 6977.
58Lazarus RS & Folkman S (1984) Stress, Appraisal and Coping. New York: Springer.
59Benton D, Williams C & Brown A (2007) Impact of consuming a milk drink containing a probiotic on mood and cognition. Eur J Nutr 61, 355361.
60Rao AV, Bested AC, Beaulne TM, et al. (2009) A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathogens 1, 16.
61Yan F & Polk DB (2002) Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. J Biol Chem 277, 5095950965.
62Lammers KM, Brigidi P, Vitali B, et al. (2003) Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol Med Microbiol 38, 165172.
63Ramiah K, van Reenen CA & Dicks LM (2008) Surface-bound proteins of Lactobacillus plantarum 423 that contribute to adhesion of Caco-2 cells and their role in competitive exclusion and displacement of Clostridium sporogenes and Enterococcus faecalis. Res Microbiol 159, 470475.
64Parracho H, McCartney AL & Gibson GR (2005) Probiotics and prebiotics in infant nutrition. Proc Nutr Soc 66, 405411.
65Hanstock TL, Clayton EH, Li KM, et al. (2004) Anxiety and aggression associated with the fermentation of carbohydrates in the hindgut of rats. Physiol Behav 82, 357368.
66Shultz SR, MacFabe DF, Ossenkopp KP, et al. (2008) Intracerebroventricular injection of propionic acid, an enteric bacterial metabolic end-product, impairs social behavior in the rat: implications for an animal model of autism. Neuropharmacology 54, 901911.
67Alesci S, Martinez PE, Kelkar S, et al. (2005) Major depression is associated with significant diurnal elevations in plasma interleukin-6 levels, a shift of its circadian rhythm, and loss of physiological complexity in its secretion: clinical implications. J Clin Endocrinol Metab 90, 25222530.
68Capuron L, Neurauter G, Musselman DL, et al. (2003) Interferon-alpha-induced changes in tryptophan metabolism. Relationship to depression and paroxetine treatment. Biol Psychiatry 54, 906914.
69Hauser P, Khosla J, Aurora H, et al. (2002) A prospective study of the incidence and open-label treatment of interferon-induced major depressive disorder in patients with hepatitis C. Mol Psychiatry 7, 942947.
70Musselman DL, Lawson DH, Gumnick JF, et al. (2001) Paroxetine for the prevention of depression induced by high-dose interferon alfa. N Engl J Med 344, 961966.
71Maes M (2001) The immunoregulatory effects of antidepressants. Hum Psychopharmacol 16, 95103.
72Desbonnet L, Garrett L, Clarke G, et al. (2008) The probiotic Bifidobacteria infantis: an assessment of potential antidepressant properties in the rat. J Psychiatr Res 43, 164174.
73Duncker SC, Wang L, Hols P, et al. (2008) The d-alanine content of lipoteichoic acid is crucial for Lactobacillus plantarum-mediated protection from visceral pain perception in a rat colorectal distension model. Neurogastroenterol Motil 20, 843850.
74Karimi K, Inman MD, Bienenstock J, et al. (2009) Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med 179, 186193.
75Logan AC & Katzman M (2005) Major depressive disorder: probiotics may be an adjuvant therapy. Med Hypotheses 64, 533538.
76Munck A, Guyre PM & Holbrook NJ (1984) Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 5, 2544.
77Ottenweller JE, Natelson BH, Pitman DL, et al. (1989) Adrenocortical and behavioral responses to repeated stressors: toward an animal model of chronic stress and stress-related mental illness. Biol Psychiatry 26, 829841.
78Lowry CA, Hollis JH, de Vries A, et al. (2007) Identification of an immune-responsive mesolimbocortical serotonergic system: potential role in regulation of emotional behavior. Neuroscience 146, 756772.
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