Effects of genetic, processing, or product formulation changes on efficacy and safety of probiotics

Annals of the New York Academy of Sciences

Volumn 1309, Issue 1, 2014, Pages 1-18

  Sanders, Mary Ellen ^a   Klaenhammer, Todd R ^b   Ouwehand, Arthur C ^c   Pot, Bruno ^d   Johansen, Eric ^e   Heimbach, James T ^f   Marco, Maria L ^g   Tennilä, Julia ^c   Ross, R Paul ^h   Franz, Charles ⁱ   Pagé, Nicolas ^j   Pridmore, R David ^j   Leyer, Greg ^k   Salminen, Seppo ^l   Charbonneau, Duane ^m   Call, Emma ^b   Lenoir Wijnkoop, Irene ⁿ  

^a International Scientific Association for Probiotics and Prebiotics   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

^c DUPONT COMPANY   (United States)

^d INSTITUT PASTEUR DE LILLE   (France)

^e CHR HANSEN A S   (Denmark)

^f JHeimbach LLC   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h TEAGASC FOOD RESEARCH CENTRE   (Ireland)

ⁱ FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

^j UAS Laboratories LLC ^*  (Switzerland)

^k UAS Labs   (United States)

^l UNIVERSITY OF TURKU   (Finland)

^m PROCTER AND GAMBLE COMPANY   (United States)

ⁿ DANONE RESEARCH   (France)

more..

Author keywords

Efficacy; Gene expression; Genetics; Probiotic; Regulatory; Safety

Indexed keywords

BIOLOGICAL MARKER; PROBIOTIC AGENT;

ARTICLE; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG FORMULATION; DRUG SAFETY; FECES MICROFLORA; NONHUMAN; PROCESS OPTIMIZATION; STRAIN IMPROVEMENT;

EFFICACY; GENE EXPRESSION; GENETICS; PROBIOTIC; REGULATORY; SAFETY;

GENETIC VARIATION; HUMANS; PATIENT SAFETY; PROBIOTICS; TREATMENT OUTCOME;

EID: 84894437195     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12363     Document Type: Article

References (97)

1. Kleerebezem, M. et al. 2003. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100: 1990-1995.
2. Goh, Y.J. et al. 2009. Development and application of a upp-based counterselective gene replacement system for the study of the S-layer protein SlpX of Lactobacillus acidophilus NCFM. Appl Environ Microbiol 75: 3093-3105.
3. Kankainen, M. et al. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc Natl Acad Sci U S A 106: 17193-17198.
4. O'Connell Motherway, M. et al. 2011. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A 108: 11217-11222.
5. Grangette, C. et al. 2005. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci U S A 102: 10321-10326.
6. Khazaie, K. et al. 2012. Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci U S A 109: 10462-10467.
7. Mohamadzadeh, M. et al. 2011. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc Natl Acad Sci U S A 108(Suppl 1): 4623-4630.
8. Macho Fernandez, E. et al. 2011. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60: 1050-1059.
9. Drake, J.W. 1991. A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci U S A 88: 7160-7164.
10. Grzeskowiak, L., E. Isolauri, S. Salminen & M. Gueimonde. 2011. Manufacturing process influences properties of probiotic bacteria. Br J Nutr 105: 887-894.
11. Marcobal, A.M., D.A. Sela, Y.I. Wolf, et al. 2008. Role of hypermutability in the evolution of the genus Oenococcus. J Bacteriol 190: 564-570.
12. Barrangou, R. 2013. CRISPR-Cas systems and RNA-guided interference. Wiley Interdiscip Rev RNA 4, 267-278.
13. Foligne, B. et al. 2010. Probiotic properties of non-conventional lactic acid bacteria: immunomodulation by Oenococcus oeni. Int J Food Microbiol 140: 136-145.
14. Shimizu-Kadota, M. & T. Sakurai. 1982. Prophage curing in Lactobacillus casei by isolation of a thermoinducible mutant. Appl Environ Microbiol 43: 1284-1287.
15. Sybesma, W., D. Molenaar, W. van Ijcken, K. Venema & R. Kort. 2013. Genome instability in Lactobacillus rhamnosus GG. Appl Environ Microbiol 79: 2233-2239.
16. Rho, M., Y.W. Wu, H. Tang, et al. 2012. Diverse CRISPRs evolving in human microbiomes. PLoS Genet 8: e1002441.
17. Horvath, P. et al. 2009. Comparative analysis of CRISPR loci in lactic acid bacteria genomes. Int J Food Microbiol 131: 62-70.
18. Corcoran, B.M., Stanton, C., Fitzgerald, G. & Ross, R.P. 2008. Life under stress: the probiotic stress response and how it may be manipulated. Curr Pharm Des 14: 1382-1399.
19. Saxelin, M. et al. 2010. Persistence of probiotic strains in the gastrointestinal tract when administered as capsules, yoghurt, or cheese. Int J Food Microbiol 144: 293-300.
20. Kaila, M., E. Isolauri, E. Sepp, et al. 1998. Fecal recovery of a human Lactobacillus strain (ATCC 53103) during dietary therapy of rotavirus diarrhea in infants. Bioscience and Microflora 17: 149-151.
21. Kumpu, M. et al. 2012. Milk containing probiotic Lactobacillus rhamnosus GG and respiratory illness in children: a randomized, double-blind, placebo-controlled trial. Eur J Clin Nutr 66: 1020-1023.
22. Saxelin, M., M. Ahokas & S. Salminen. 1993. Dose response on the fecal colonisation of Lactobacillus strain GG administered in two different formulations. Microbial Ecol Health Dis 6: 119-122.
23. Saxelin, M., S. Elo, S. Salminen & H. Vapaatalo. 1991. Dose response colonisation of faeces after oral administration of Lactobacillus casei strain GG. Microbial Ecol Health Dis 4: 209-214.
24. Goldin, B.R. et al. 1992. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci 37: 121-128.
25. Dommels, Y.E. et al. 2009. Survival of Lactobacillus reuteri DSM 17938 and Lactobacillus rhamnosus GG in the human gastrointestinal tract with daily consumption of a low-fat probiotic spread. Appl Environ Microbiol 75: 6198-6204.
26. Kekkonen, R.A. et al. 2007. A combination of galacto-oligosaccharides and Lactobacillus GG increases bifidobacteria to a greater extent than Lactobacillus GG on its own. Milchwissenschaft 62: 326-330.
27. Klingberg, T.D. & B.B. Budde. 2006. The survival and persistence in the human gastrointestinal tract of five potential probiotic lactobacilli consumed as freeze-dried cultures or as probiotic sausage. Int J Food Microbiol 109: 157-159.
28. Lahtinen, S.J. et al. 2012. Probiotic cheese containing Lactobacillus rhamnosus HN001 and Lactobacillus acidophilus NCFM(R) modifies subpopulations of fecal lactobacilli and Clostridium difficile in the elderly. Age (Dordr) 34: 133-143.
29. Ouwehand, A.C., K. Tiihonen, M. Saarinen, et al. 2009. Influence of a combination of Lactobacillus acidophilus NCFM and lactitol on healthy elderly: intestinal and immune parameters. Br J Nutr 101: 367-375.
30. Savard, P. et al. 2011. 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 149: 50-57.
31. Larsen, C.N. et al. 2006. Dose-response study of probiotic bacteria Bifidobacterium animalis subsp lactis BB-12 and Lactobacillus paracasei subsp paracasei CRL-341 in healthy young adults. Eur J Clin Nutr 60, 1284-1293.
32. Matto, J. et al. 2006. Intestinal survival and persistence of probiotic Lactobacillus and Bifidobacterium strains administered in triple-strain yoghurt. International Dairy J 16: 1174-1180.
33. Wolvers, D. et al. 2010. Is ice cream a suitable carrier for probiotics? Proc Nutr Soc 69: E240.
34. Rochet, V. et al. 2008. Modulation of Lactobacillus casei in ileal and fecal samples from healthy volunteers after consumption of a fermented milk containing Lactobacillus casei DN-114 001Rif. Can J Microbiol 54, 660-667.
35. Suomalainen, T., P. Sigvart-Mattila, J. Matto & S. Tynkkynen. 2008. In vitro and in vivo gastrointestinal survival, antibiotic susceptibility and genetic identification of Propionibacterium freudenreichii ssp. shermanii JS. International Dairy J 18: 271-278.
36. Hatakka, K. et al. 2008. The influence of Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp. shermanii JS on potentially carcinogenic bacterial activity in human colon. Int J Food Microbiol 128: 406-410.
37. Palaria, A., I. Johnson-Kanda & D.J. O'Sullivan. 2012. Effect of a synbiotic yogurt on levels of fecal bifidobacteria, clostridia, and enterobacteria. Appl Environ Microbiol 78: 933-940.
38. Ahmed, M., J. Prasad, H. Gill, et al. 2007. Impact of consumption of different levels of Bifidobacterium lactis HN019 on the intestinal microflora of elderly human subjects. J Nutr Health Aging 11: 26-31.
39. Gopal, P., J. Prasad & H.S. Gill. 2003. Effects of the consumption of Bifidobacterium lactis HN019 (DR10 TM) and galacto-oligosaccharides on the microflora of the gastrointestinal tract in human subjects. Nutr Res 23: 1313-1328.
40. Verdenelli, M.C., S. Silvi, C. Cecchini, et al. 2011. Influence of a combination of two potential probiotic strains, Lactobacillus rhamnosus IMC 501(R) and Lactobacillus paracasei IMC 502(R) on bowel habits of healthy adults. Lett Appl Microbiol 52: 596-602.
41. Martarelli, D. et al. 2011. Effect of a probiotic intake on oxidant and antioxidant parameters in plasma of athletes during intense exercise training. Curr Microbiol 62: 1689-1696.
42. Lahtinen, S.J. et al. 2009. Prenatal probiotic administration can influence Bifidobacterium microbiota development in infants at high risk of allergy. J Allergy Clin Immunol 123: 499-501.
43. Gill, H.S., K.J. Rutherfurd, M.L. Cross & P.K. Gopal. 2001. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 74: 833-839.
44. Morimoto, K., T. Takeshita, M. Nanno, et al. 2005. Modulation of natural killer cell activity by supplementation of fermented milk containing Lactobacillus casei in habitual smokers. Prev Med 40: 589-594.
45. Reale, M. et al. 2012. Daily intake of Lactobacillus casei Shirota increases natural killer cell activity in smokers. Br J Nutr 108, 308-314.
46. Koebnick, C., I. Wagner, P. Leitzmann, et al. 2003. Probiotic beverage containing Lactobacillus casei Shirota improves gastrointestinal symptoms in patients with chronic constipation. Can J Gastroenterol 17: 655-659.
47. Isolauri, E., M. Juntunen, T. Rautanen, et al. 1991. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88: 90-97.
48. Gao, X.W., M. Mubasher, C.Y. Fang, et al. 2010. Dose-response efficacy of a proprietary probiotic formula of Lactobacillus acidophilus CL1285 and Lactobacillus casei LBC80R for antibiotic-associated diarrhea and Clostridium difficile-associated diarrhea prophylaxis in adult patients. Am J Gastroenterol 105: 1636-1641.
49. Ibrahim, F. et al. 2010. Probiotics and immunosenescence: cheese as a carrier. FEMS Immunol Med Microbiol 59: 53-59.
50. Maldonado, J. et al. 2012. Human milk probiotic Lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J Pediatr Gastroenterol Nutr 54: 55-61.
51. Vriens, H.P. 2009. Restoring the balance: Why chocolate proves to be an ideal carrier for probiotics. NutraCos May/June: 6-7.
52. Shah, N.P., W.K. Ding, M.J. Fallourd & G. Leyer. 2010. Improving the stability of probiotic bacteria in model fruit juices using vitamins and antioxidants. J Food Sci 75: M278-82.
53. Ouwehand, A.C., T. Kurvinen & P. Rissanen. 2004. Use of a probiotic Bifidobacterium in a dry food matrix, an in vivo study. Int J Food Microbiol 95: 103-106.
54. Graff, J., K. Brinch & J.L. Madsen. 2001. Gastrointestinal mean transit times in young and middle-aged healthy subjects. Clin Physiol 21: 253-259.
55. Lebeer, S., J. Vanderleyden & S.C. De Keersmaecker. 2008. Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol Rev 72: 728-764, Table of Contents.
56. Marco, M.L., R.S. Bongers, W.M. de Vos & M. Kleerebezem. 2007. Spatial and temporal expression of Lactobacillus plantarum genes in the gastrointestinal tracts of mice. Appl Environ Microbiol 73: 124-132.
57. Denou, E. et al. 2007. Gene expression of commensal Lactobacillus johnsonii strain NCC533 during in vitro growth and in the murine gut. J Bacteriol 189: 8109-8119.
58. Walter, J. et al. 2005. A high-molecular-mass surface protein (Lsp) and methionine sulfoxide reductase B (MsrB) contribute to the ecological performance of Lactobacillus reuteri in the murine gut. Appl Environ Microbiol 71: 979-986.
59. Bron, P.A., M. Meijer, R.S. Bongers, et al. 2007. Dynamics of competitive population abundance of Lactobacillus plantarum ivi gene mutants in faecal samples after passage through the gastrointestinal tract of mice. J Appl Microbiol 103: 1424-1434.
60. Denou, E. et al. 2008. Identification of genes associated with the long-gut-persistence phenotype of the probiotic Lactobacillus johnsonii strain NCC533 using a combination of genomics and transcriptome analysis. J Bacteriol 190: 3161-3168.
61. Lozupone, C.A., J.I. Stombaugh, J.I. Gordon, et al. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-230.
62. Hugot, J.P. et al. 2001. Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 411: 599-603.
63. Hugot, J.P. et al. 1996. Mapping of a susceptibility locus for Crohn's disease on chromosome 16. Nature 379: 821-823.
64. Ogura, Y. et al. 2001. A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411: 603-606.
65. Kolida, S. & G.R. Gibson. 2011. Synbiotics in health and disease. Annu Rev Food Sci Technol 2: 373-393.
66. Tachon, S., B. Lee & M.L. Marco. 2013. Diet alters probiotic Lactobacillus persistence and function in the intestine. Environ Microbiol. DOI: 10.1111/1462-2920.12297. [Epub ahead of print].
67. Marco, M.L. et al. 2010. Convergence in probiotic Lactobacillus gut-adaptive responses in humans and mice. ISME J 4: 1481-1484.
68. Marco, M.L. et al. 2009. Lifestyle of Lactobacillus plantarum in the mouse caecum. Environ Microbiol 11: 2747-2757.
69. Reid, G. et al. 2010. Responders and non-responders to probiotic interventions: how can we improve the odds? Gut Microbes 1: 200-204.
70. van Loveren, H., Y. Sanz & S. Salminen. 2012. Health claims in Europe: probiotics and prebiotics as case examples. Annu Rev Food Sci Technol 3: 247-261.
71. Koponen, A., M. Sandell, S. Salminen & I. Lenoir-Wijnkoop. 2012. Nutrition economics: towards comprehensive understanding of the benefits of nutrition. Microb Ecol Health Dis 23: 46-50.
72. U.S. Food and Drug Administration. 2011. Draft Guidance for Industry: Dietary Supplements: New Dietary Ingredient Notifications and Related Issues. http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/DietarySupplements/ucm257563.htm.
73. Organization for Economic Cooperation and Development (OECD). 1993. Safety evaluation of foods derived by modern biotechnology: concepts and principles. Paris: OECD Publications Service.
74. World Health Organization and Food and Agricultural Organization of the United Nations. 1996. Joint FAO/WHO Expert Consultation on Biotechnology and Food Safety ftp://ftp.fao.org/es/esn/food/biotechnology.pdf.
75. U.S. Food and Drug Administration. 2008. Agency Response Letter GRAS Notice No. GRN 000254. http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm154990.htm.
76. Savino, F., E. Pelle, E. Palumeri, et al. 2007. Lactobacillus reuteri (American Type Culture Collection Strain 55730) versus simethicone in the treatment of infantile colic: a prospective randomized study. Pediatrics 119: e124-30.
77. Savino, F. et al. 2010. Lactobacillus reuteri DSM 17938 in infantile colic: a randomized, double-blind, placebo-controlled trial. Pediatrics 126: e526-33.
78. Indrio, F. et al. 2008. The effects of probiotics on feeding tolerance, bowel habits, and gastrointestinal motility in preterm newborns. J Pediatr 152: 801-806.
79. Indrio, F. et al. 2011. Lactobacillus reuteri accelerates gastric emptying and improves regurgitation in infants. Eur J Clin Invest 41: 417-422.
80. Bennedsen, M., B. Stuer-Lauridsen, M. Danielsen & E. Johansen. 2011. Screening for antimicrobial resistance genes and virulence factors via genome sequencing. Appl Environ Microbiol 77: 2785-2787.
81. Zhou, C.E. et al. 2007. MvirDB-a microbial database of protein toxins, virulence factors and antibiotic resistance genes for bio-defence applications. Nucleic Acids Res 35: D391-4.
82. Liu, B. & M. Pop. 2009. ARDB-Antibiotic Resistance Genes Database. Nucleic Acids Res 37: D443-7.
83. Hill, C. 2012. Virulence or niche factors: what's in a name? J Bacteriol 194: 5725-5727.
84. Thomas, C.M. et al. 2012. Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 7: e31951.
85. Garrigues, C., E. Johansen & R. Crittenden. 2013. Pangenomics-an avenue to improved industrial starter cultures and probiotics. Curr Opin Biotechnol 24: 187-191.
86. Desmond, C., G.F. Fitzgerald, C. Stanton & R.P. Ross. 2004. Improved stress tolerance of GroESL-overproducing Lactococcus lactis and probiotic Lactobacillus paracasei NFBC 338. Appl Environ Microbiol 70: 5929-5936.
87. Desmond, C., C. Stanton, G.F. Fitzgerald, et al. 2001. Environmental adaption of probiotic lactobacilli towards improvement of performance during spray drying. Int. Dairy J. 11: 801-808.
88. van Bokhorst-van de Veen, H. et al. 2011. Short- and long-term adaptation to ethanol stress and its cross-protective consequences in Lactobacillus plantarum. Appl Environ Microbiol 77: 5247-5256.
89. Muller, J.A., R.P. Ross, W.F. Sybesma, et al. 2011. Modification of the technical properties of Lactobacillus johnsonii NCC 533 by supplementing the growth medium with unsaturated fatty acids. Appl Environ Microbiol 77: 6889-6898.
90. Muller, J.A., C. Stanton, W. Sybesma, et al. 2010. Reconstitution conditions for dried probiotic powders represent a critical step in determining cell viability. J Appl Microbiol 108: 1369-1379.
91. du Toit, E., S. Vesterlund, M. Gueimonde & S. Salminen. 2013. Assessment of the effect of stress-tolerance acquisition on some basic characteristics of specific probiotics. Int J Food Microbiol 165: 51-56.
92. Desmond, C., R.P. Ross, E. O'Callaghan, et al. 2002. Improved survival of Lactobacillus paracasei NFBC 338 in spray-dried powders containing gum acacia. J Appl Microbiol 93: 1003-1011.
93. Corcoran, B.M., C. Stanton, G.F. Fitzgerald & R.P. Ross. 2005. Survival of probiotic lactobacilli in acidic environments is enhanced in the presence of metabolizable sugars. Appl Environ Microbiol 71: 3060-3067.
94. Rochet, V. et al. 2008. Survival of Bifidobacterium animalis DN-173 010 in the faecal microbiota after administration in lyophilised form or in fermented product - a randomised study in healthy adults. J Mol Microbiol Biotechnol 14: 128-136.
95. Smith, T.J., D. Anderson, L.M. Margolis, et al. 2011. Persistence of Lactobacillus reuteri DSM17938 in the human intestinal tract: response to consecutive and alternate-day supplementation. J Am Coll Nutr 30: 259-264.
96. European Food Safety Authority. 2007. Introduction of a Qualified Presumption of Safety (QPS) approach for assessment of selected microorganisms referred to EFSA - Opinion of the Scientific Committee. http://www.efsa.europa.eu/EFSA/efsa_locale-1178620753812_1178667590178.htm.
97. U.S. Food and Drug Administration. 2013. Generally Recognized as Safe (GRAS). http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/.