Lactobacillus rhamnosus Gorbach-Goldin (GG): A Top Well-Researched Probiotic Strain
AbstractProbiotics, living microorganisms which when used in adequate amounts, have health beneﬁts on the host, have attracted a considerable deal of interest in the biotechnology market. Various prokaryotic and eukaryotic microbes have been studied for probiotic purposes in human and animals. Lactobacillus and Bifidobacterium are the main probiotic genera; however, there are reports on the probiotic potential of strains belonging to Bacillus, Lactococcus, Pediococcus and also some yeast species. Lactobacillus species are regarded as the most investigated beneficial microbes for human and either animal probiotic development due to: a) anti-inflammatory effects, b) anti-allergic features, c) secretion of antimicrobial compounds, d) develops in aerobic and anaerobic conditions, and e) many Lactobacilli have been Generally Recognized As Safe (GRAS) by the Food and Drug Administration (FDA). Among Lactobacilli, Lactobacillus rhamnosus Gorbach-Goldin (GG) is known among the most in-detail studied strains and is regarded as a top well-researched and commercialized probiotic strain in the industrial biotechnology. Strain GG is a commercially significant probiotic which was originally isolated from the healthy human gastrointestinal tract in 1983. The documents studied this strain were reviewed here and it is shown that such successful strains in the probiotic market have been extensively studied from the probiotic traits and safety point of views and a minor part of the documents concerned the bioprocessing issues. Also, we showed that the beneficial and negative effects of this strain has been investigated in various clinical trial systems when it became commercialized. Various aspects of this strain are here reviewed, comparatively.
Hasler CM. Functional Foods: Benefits, Concerns and Challenges—A Position Paper from the American Council on Science and Health. J Nutr 2002; 132(12): 3772-81.
Tamime, AY, Saarela, M, Søndergaard AK, et al. Production and maintenance of viability of probiotic micro-organisms in dairy products, in probiotic dairy products (ed A. Tamime), Blackwell Science Ltd, Oxford, UK; 2006.
Sip A and Grajek W. Probiotics and prebiotics, in functional food product development (eds J. Smith and E. Charter), Wiley-Blackwell, Oxford, UK; 2010.
Joint FAO/WHO Working Group Report on Drafting Guidelines for the Evaluation of Probiotics in Food. London, Ontario, Canada. April 30- May 1, 2002.
Gerritsen J, Smidt H, Rijkers GT, et al. Intestinal microbiota in human health and disease: the impact of probiotics Genes. Nutr 2011; 6(3): 209-40.
Anukam KC and Reid G. Probiotics: 100 years (1907-2007) after Elie Metchnikoff’s observation, in communicating current research and educational topics and trends in applied microbiology. ed. Méndez-Vilas A., 466-74. 2007 ed. (Formatex.org.): 466-74.
McFarland LV. Evidence-based review of probiotics for antibiotic-associated diarrhea and Clostridium difficile infections. Anaerobe 2009; 15(6): 274-80.
Behnsen J, Deriu E, Sassone-Corsi M, et al. probiotics: properties, examples, and specific applications. Cold Spring Harb Perspect Med 2013; 3(3): a010074.
Doron S, Snydman DR, Gorbach SL. L. GG: bacteriology and clinical applications. Gastroenterol Clin North Am 2005; 34(3): 483-98.
Gupta V and Garg R (2009). Probiotics. Indian J Med Microbiol 2009; 27(3): 202-9.
Soccol C, Porto L, Rigon M, et al. The potential of probiotics: a review. Food Technol Biotech 2010; 48(4): 413-34.
Park YH, Hamidon F, Rajangan C, et al. Application of Probiotics for the Production of Safe and High-quality Poultry Meat. Korean J Food Sci Anim Resour 2016; 36(5): 567-76.
Weese JS, Anderson MEC, Lowe A, et al. Preliminary investigation of the probiotic potential of Lactobacillus rhamnosus strain GG in horses: fecal recovery following oral administration and safety. Can Vet J 2003; 44(4): 299-302.
Conway PL, Gorbach SL, Goldin BR. Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci 1987; 70(1): 1-12.
Pant AR, Graham SM, Allen SJ, et al. Lactobacillus GG and acute diarrhoea in young children in the tropics. J Trop Pediatr 1996; 42(3): 162-5.
Noohi N, Ebrahimipour G, Rohani M, et al. Phenotypic characteristics and probiotic potentials of Lactobacillus spp. isolated from poultry. Jundishapur J Microbiol 2014; 7: e17824.
Rohani M, N, Talebi M, et al. Highly heterogeneous probiotic Lactobacillus species in healthy Iranians with low functional activities. PLoS One 2015; 10(12): e0144467.
Yoshimi B, Fang H, Masataka H, et al. Effects of Lactobacillus GG Yogurt on Human Intestinal Microecology in Japanese Subjects. Nutr Today 1996; 31(6): 12S.
Noohi N, Ebrahimipour G, Rohani M, et al. Evaluation of potential probiotic characteristics and antibacterial effects of strains of Pediococcus species isolated from broiler chickens. Br Poult Sci 2016; 57(3): 317-23.
Venugopalan V, Shriner KA, Wong-Beringer A. Regulatory oversight and safety of probiotic use. Emerg Infect Dis 2010; 16(11): 1661-5.
Ganguli K and Walker WA. Probiotics in the prevention of necrotizing enterocolitis. J Clin Gastroenterol 2011; 45: 3.
Carr FJ, Chill D, Maida N. The lactic acid bacteria: a literature survey. Crit Rev Microbiol 2002; 28(4): 281-370.
De Vecchi E and Drago L. Lactobacillus sporogenes or Bacillus coagulans: Misidentification or mislabelling? Int J Probiot Prebiot 2006; 1: 3-10.
Chang YH, Jung MY, Park IS, Oh HM. Sporolactobacillus vineae sp. nov., a spore-forming lactic acid bacterium isolated from vineyard soil. Int J Syst Evol Microbiol 2008; 58: 2316-20.
Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature 2011; 473: 174-80.
Kleerebezem M and Hugenholtz J. Metabolic pathway engineering in lactic acid bacteria. Curr Opin Biotechnol 2003; 14: 232-7.
Hedberg M, Hasslöf P, Sjöström I, et al. Sugar fermentation in probiotic bacteria--an in vitro study. Oral Microbiol Immunol 2008; 23(6): 482-5.
Emiliano J, Juarez M, Savoy G, et al. Microbiology applicability of a Lactobacillus amylovorus strain as co-culture for natural folate bio-enrichment of fermented milk. Int J Food Microbiol 2014; 191: 10-6.
Reid G. The growth potential for dairy probiotics. International Dairy Journal
; 49: 16-22.
Gorbach SL. and Goldin BR. U.S. Patent. 1989; 4839281.
Coudeyras S, Marchandin H, Fajon C, et al. Taxonomic and Strain-Specific Identification of the Probiotic Strain Lactobacillus rhamnosus 35 within the Lactobacillus casei Group. Appl Environ Microbiol 2008; 74(9): 2679-89.
Banks JM, Williams AG, The role of the nonstarter lactic acid bacteria in Cheddar cheese ripening. Int J Dairy Technol 2004; 57(2–3): 145-52.
Manley KJ, Fraenkel MB, Mayall BC, et al. Probiotic treatment of vancomycin-resistant enterococci: a randomised controlled trial. Med J Aust 2007; 186(9): 454-7.
Gorbach SL, Chang TW, Goldin B. Successful treatment of relapsing Clostridium difficile colitis with Lactobacillus GG. The Lancet 1987; 2(8574): 1519.
Biller JA, Katz AJ, Flores AF, et al. Treatment of recurrent Clostridium difficile colitis with Lactobacillus GG. J Pediatr Gastroenterol Nutr 1995; 21(2): 224-6.
Gorbach SL. The Discovery of Lactobacillus GG. Nutr Today 1996; 31(6): (suppl.): 2S-4S.
Dong MY, Chang TW, Gorbach SL. Effects of feeding Lactobacillus GG on lethal irradiation in mice. Diagn Microbiol Infect Dis 1987; 7(1): 1-7.
Isolauri E, Juntunen M, Rautanen T, et al. A human Lactobacillus strain (Lactobacillus casei sp. strain GG) promotes recovery from acute diarrhea in children. Pediatrics 1991; 88(1): 90-7.
Isolauri E, Kirjavainen P, Salminen S. Probiotics: a role in the treatment of intestinal infection and inflammation?. Gut 2002; 50(Suppl 3): iii54–iii59.
Vanderhoof JA, Whitney DB, Antonson DL, et al. Lactobacillus GG in the prevention of antibiotic-associated diarrhea in children. J Pediatr 1999; 135 (5): 564-8.
Guandalini S, Pensabene L, Zikri MA et al. Lactobacillus GG administered in oral rehydration solution to children with acute diarrhea: a multicenter European trial. J Pediatr Gastroenterol Nutr 2000; 30(1): 54-60.
Hatakka K, Savilahti E, Pönkä A, et al. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ 2001; 322(7238): 1327.
Van Niel CW, Feudtner C, Garrison MM, et al. Lactobacillus therapy for acute infectious diarrhea in children: a meta-analysis. Pediatrics 2002; 109(4): 678-84.
Ridwan BU, Koning CJ, Besselink MG, et al. Antimicrobial activity of a multispecies probiotic (Ecologic 641) against pathogens isolated from infected pancreatic necrosis. Lett Appl Microbiol 2008; 46(1): 61-7.
Canaani RB, Cirillo P, Terrin G, et al. Probiotics for treatment of accute diarrhoea in children: randomised clinical trial of five different preparations. BMJ 2007; 335(7615): 340.
Österlund P, Ruotsalainen T, Korpela R, et al. Lactobacillus supplementation for diarrhoea related to chemotherapy of colorectal cancer: a randomised study. Br J Cancer 2007; 97(8): 1028-34.
Hojsak I, Snovak N, Abdović S, et al. Lactobacillus GG in the prevention of gastrointestinal and respiratory tract infections in children who attend day care centers: A randomized, double-blind, placebo-controlled trial. Clin Nutr 2009; 29(3): 312-6.
Boyle RJ, Bath-Hextall FJ, Leonardi-Bee J, et al. Probiotics for the treatment of eczema: a systematic review. Clin Exp Allergy 2009; 39(8): 1117-27.
Nanji AA, Khettry U, Sadrzadeh SM. Lactobacillus feeding reduces endotoxemia and severity of experimental alcoholic liver (disease). Proc Soc Exp Biol Med 1994; 205(3): 243-7.
Forsyth CB, Farhadi A, Jakate SM, et al. (2009). Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 2009; 43(2): 163-72.
Francavilla R, Miniello V, Magistà AM, et al. A randomized controlled trial of Lactobacillus GG in children with functional abdominal pain. Pediatrics 2010; 126(6): e1445-52.
Wang Y, Liu Y, Sidhu A, et al. Lactobacillus rhamnosus GG culture supernatant ameliorates acute alcohol-induced intestinal permeability and liver injury. Am J Physiol Gastrointest Liver Physiol 2012; 303(1): G32-41.
Sanchez M, Darimont C, Drapeau V, et al. Effect of Lactobacillus rhamnosus CGMCC1.3724 supplementation on weight loss and maintenance in obese men and women. Brit J Nutr 2014; 111(8): 1507-19.
Waigankar SS and Patel V. Role of probiotics in urogenital healthcare. J Midlife Health 2011; 2(1): 5-10.
Cribby S, Michelle Taylor M, Gregor Reid G. Vaginal Microbiota and the Use of Probiotics. Interdiscip Perspect Infect Dis 2008; 2008: 256-490.
Meurman JH, Antila H, Salminen S. Recovery of Lactobacillus Strain GG (ATCC 53103) from Saliva of Healthy Volunteers after Consumption of Yoghurt Prepared with the Bacterium. MEHD 1994; 7: 295-8.
Silva M, Jacobus NV, Deneke C, et al. Antimicrbial substance from a human Lactobacillus strain". Antimicrob Agents Chemother 1987; 31(8): 1231-3.
Siitonen S, Vapaatalo H, Salminen S, et al. Effect of Lactobacillus GG yoghurt in prevention of antibiotic associated diarrhoea. Ann Med 1990; 22(1): 57-9.
Goldin BR, Gorbach SL, Saxelin M, et al. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci 1992; 37(1): 121-8.
Kaila M, Isolauri E, Soppi E, et al. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res 1992; 32(2): 141-4.
Isolauri E, Majamaa H, Arvola T, et al. Lactobacillus casei strain GG reverses increased intestinal permeability induced by cow milk in suckling rats. Gastroenterology 1993; 105(6): 1643-50.
Guandalini S. Probiotics for prevention and treatment of diarrhea. J Clin Gastroenterol 2011; 45 Suppl: S149-53.
Kalliomäki M, Salminen S, Arvilommi H, et al. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. The Lancet 2001; 357(9262): 1076-9.
Kalliomäki M, Salminen S, Poussa T, et al. Probiotics during the first 7 years of life: a cumulative risk reduction of eczema in a randomized, placebo-controlled trial. J Allergy Clin Immunol 2007; 119(4): 1019-21.
Avlami A, Kordossis T, Vrizidis N, et al. Lactobacillus rhamnosus endocarditis complicating colonoscopy. J Infect 2001; 42: 283-285.
Salminen MK, Tynkkynen S, Rautelin H, et al. Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis 2002; 35(10): 1155-60.
Salminen MK, Rautelin H, Tynkkynen S, et al. Lactobacillus bacteremia, clinical significance, and patient outcome, with special focus on probiotic L. rhamnosus GG. Clin Infect Dis 2004; 38(1): 62-9.
Saxelin, M. Lactobacillus GG—a human probiotic strain with thorough clinical documentation. Food Rev Int 1997; 13: 293-313.
Broccali G, Berti M, Pistolesi E, et al. Study of the effect of lactobacillus GG supplementation in combination with and without arginine aspartate on lipoproteins and liver peroxidation in cholesterol-fed rats. Int J Food Sci Nutr 2000; 51(6): 475-82.
Näse L1, Hatakka K, Savilahti E, et al. Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res 2001; 35(6): 412-20.
Armuzzi A, Cremonini F, Bartolozzi F, et al. The effect of oral administration of Lactobacillus GG on antibiotic-associated gastrointestinal side-effects during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2001; 15(2): 163-9.
Walter J. The ecological role of lactobacilli in the gastrointestinal tract: Implications for fundamental and biomedical research. Appl Environ Microbiol 2008; 74(16): 4985-96.
Muraro A, Hoekstra MO, Meijer Y, et al. Extensively hydrolysed casein formula supplemented with Lactobacillus rhamnosus GG maintains hypoallergenic status: randomised double-blind, placebo-controlled crossover trial. BMJ Open 2012; 2(2): e000637.
Kankainen M, Paulin, L, Tynkkynen S, et al. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci SA 2009; 106(40): 17193-8.
Segers ME and Lebeer S. Towards a better understanding of Lactobacillus rhamnosus GG--host interactions. Microb Cell Fact 2014; 29; 13 Suppl 1:S7.
Reid G and Bruce AW. Selection of Lactobacillus Strains for Urogenital Probiotic Applications. J Infect Dis 2001; 183: Suppl 1: S77-S80.
Morita H, Toh H, Oshima K, Murakami M, Taylor TD, Igimi S, Hattori M. Complete genome sequence of the probiotic Lactobacillus rhamnosus ATCC 53103. J Bacteriol 2009; 191(24): 7630-1.
Von Wright A. Regulating the safety of probiotics--the European approach. Curr Pharm Des 2005; 11(1): 17-23.
Reid G, Kim SO, Köhler GA. Selecting, testing and understanding probiotic microorganisms. FEMS Immunol Med Microbiol 2006; 46(2): 149-57.
Saldanha LG. US Food and Drug Administration regulations governing label claims for food products, including probiotics. Clin Infect Dis 2008; 1(46) Suppl 2: S119-21; discussion S144-51.
Roberfroid MB. Concepts and strategy of functional food science: the European perspective1, 2, 3. Am J Clin Nutr 20007; 1(6): 1660-4.
Gismondo MR, Drago L, Lombardi A. Review of probiotics available to modify gastrointestinal flora. Int J Antimicrob Agents 1999; 12: 287-92.
Chow J. Probiotics and prebiotics: A brief overview. J Ren Nutr 2002; 12: 76-86.
Shah N.P. Functional cultures and health benefits. Int Dairy J 2007; 17: 1262-77.
Savard P, Lamarche B, Paradis ME, et al. Impact of Bifidobacterium animalis subsp. lactis BB-12 and, Lactobacillus acidophilus LA-5-containing yoghurt, on fecal bacterial counts of healthy adults. Int J Food Microbiol 2011; 149(1): 50-7.
Jungersen M, Wind A, Johansen E, et al. The Science behind the Probiotic Strain Bifidobacterium animalis subsp. lactis BB-12®. Microorganisms 2014; 2(2), 92-110.
Merenstein DJ, Tan TP, Molokin A, et al. Safety of Bifidobacterium animalis subsp. lactis (B. lactis) strain BB-12-supplemented yogurt in healthy adults on antibiotics: a phase I safety study. Gut Microbes 2015; 6(1): 66-77.
Kim WS, Tanaka T, Kumura H, et al. Lactoferrin-binding proteins in Bifidobacterium bifidum. Biochem Cell Biol 2002; 0(1): 91-4.
Bartosch S, Woodmansey EJ, Paterson JCM, et al. Microbiological effects of consuming a synbiotic containing Bifidobacterium bifidum, Bifidobacterium lactis, and Oligofructose in elderly persons, determined by Real-Time polymerase chain reaction and counting of viable bacteria. Clin Infect Dis 2005; 40(1): 28-37.
Ward AR (1901) Bacillus lactis viscosus; a cause of ropiness in milk and cream. J Boston Soc Med Sci 1901; 5(7): 386.
Wei-Yin Ng E. Effect of starter cultures on Lactobacillus acidophilus survival and gene expression in yogurt. Master of Science thesis. Obispo. Polytechnic State University, San Luis Obispo, California, USA; 2009.
Ringel-Kulka T, Palsson OS, Maier D, et al. Probiotic bacteria Lactobacillus acidophilus NCFM and Bifidobacterium lactis Bi-07 versus placebo for the symptoms of bloating in patients with functional bowel disorders: a double-blind study. J Clin Gastroenterol 2011; 45(6): 518-25.
Shah N. P. Health benefits of yogurt and fermented milks, in manufacturing yogurt and fermented milks (eds R. C. Chandan and A. Kilara), John Wiley & Sons, Oxford, UK; 2013.
Shah N. P. Other dairy products: yogurt, kefir, kumys, in the oxford handbook of food fermentations (eds. Bamforth CW and Ward RE), Oxford University Press, Oxford, UK; 2014.
Cats A, Kuipers EJ, Bosschaert MA, et al. Effect of frequent consumption of a Lactobacillus casei-containing milk drink in Helicobacter pylori-colonized subjects. Aliment Pharmacol Ther 2003; 17(3): 429-35.
Randazzo CL, Restuccia C, Romano AD, et al. Lactobacillus casei, dominant species in naturally fermented Sicilian green olives. Int J Food Microbiol 2004; 90(1): 9-14.
Seesuriyachan P, Takenaka S, Kuntiya A, et al. Metabolism of azo dyes by Lactobacillus casei TISTR 1500 and effects of various factors on decolorization. Water Res 2007; 41(5): 985-92.
Eun CS, Kim YS, Han DS, et al. Lactobacillus casei prevents impaired barrier function in intestinal epithelial cells. APMIS 2011; 119(1): 49-56.
Zakostelska Z, Kverka M, Klimesova K, et al. Lysate of probiotic Lactobacillus casei DN-114 001 ameliorates colitis by strengthening the gut barrier function and changing the gut microenvironment. PLOS ONE 2011; 6(11): e27961.
Gan BS, Kim J, Reid G, et al. Lactobacillus fermentum RC-14 Inhibits Staphylococcus aureus Infection of Surgical Implants in Rats. J Infect Dis 2002; 185(9): 1369-72.
Gardiner GE, Heinemann C, Bruce AW, et al. Persistence of Lactobacillus fermentum RC-14 and Lactobacillus rhamnosus GR-1 but not L. rhamnosus GG in the human vagina as demonstrated by randomly amplified polymorphic. DNA Clin Diagn Lab Immunol 2002; 9(1): 92-96.
Reid G, Charbonneau D, Erb J, et al. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol Med Microbiol 2003; 35(2): 131-4.
Taverniti V and Guglielmetti S. Health-Promoting Properties of Lactobacillus helveticus. Front Microbiol 2012; 3: 392.
Prajapati JB, Khedkar CD, Chitra J, et al. Whole-genome shotgun sequencing of Lactobacillus rhamnosus MTCC 5462, a strain with probiotic potential. J Bacteriol 2012; 194(5): 1264-5.
Ceapa C, Davids M, Ritari J, et al. The Variable Regions of Lactobacillus rhamnosus Genomes Reveal the Dynamic Evolution of Metabolic and Host-Adaptation Repertoires. Genome Biol Evol 2016; 8(6): 1889-905.
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|Lactobacillus rhamnosus Strain GG Generally Recognized as Safe (GRAS) Industrial Strain Probiotics.|
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