Probiotics in respiratory virus infections

L Lehtoranta, A Pitkäranta, R Korpela, L Lehtoranta, A Pitkäranta, R Korpela

Abstract

Viral respiratory infections are the most common diseases in humans. A large range of etiologic agents challenge the development of efficient therapies. Research suggests that probiotics are able to decrease the risk or duration of respiratory infection symptoms. However, the antiviral mechanisms of probiotics are unclear. The purpose of this paper is to review the current knowledge on the effects of probiotics on respiratory virus infections and to provide insights on the possible antiviral mechanisms of probiotics. A PubMed and Scopus database search was performed up to January 2014 using appropriate search terms on probiotic and respiratory virus infections in cell models, in animal models, and in humans, and reviewed for their relevance. Altogether, thirty-three clinical trials were reviewed. The studies varied highly in study design, outcome measures, probiotics, dose, and matrices used. Twenty-eight trials reported that probiotics had beneficial effects in the outcome of respiratory tract infections (RTIs) and five showed no clear benefit. Only eight studies reported investigating viral etiology from the respiratory tract, and one of these reported a significant decrease in viral load. Based on experimental studies, probiotics may exert antiviral effects directly in probiotic-virus interaction or via stimulation of the immune system. Although probiotics seem to be beneficial in respiratory illnesses, the role of probiotics on specific viruses has not been investigated sufficiently. Due to the lack of confirmatory studies and varied data available, more randomized, double-blind, and placebo-controlled trials in different age populations investigating probiotic dose response, comparing probiotic strains/genera, and elucidating the antiviral effect mechanisms are necessary.

Figures

Fig. 1
Fig. 1
Schematic presentation of possible antiviral effect mechanisms of probiotics in respiratory virus infections (adapted from Lehtoranta [80]). 1 Probiotic bacteria may bind directly to the virus and inhibit virus attachment to the host cell receptor. 2 Adhesion of probiotics on the epithelial surface may block viral attachment by steric hindrance, cover receptor sites in a non-specific manner, or by competing for specific carbohydrate receptors. 3 Probiotics may induce mucosal regeneration: intestinal mucins may bind to viruses, and inhibit their adherence to epithelial cells and inhibit virus replication. 4 Probiotics also show direct antimicrobial activity against pathogens by producing antimicrobial substances. 5 Induction of low-grade nitric oxide (NO) production and dehydrogenase production may have antiviral activities. 6 Modulation of immune response through epithelial cells. 7 Modulation and activation of immune responses through macrophages and dendritic cells (DCs). 8 Upon activation, CD8+ T lymphocytes differentiate into cytotoxic T lymphocytes (CTLs), which destroy virus-infected cells. 9 CD4+ T lymphocytes differentiate into Th1 and Th2 cells. 10 T-helper cells type 1 (Th1) activates phagocytes, promoting virus killing. 11 Th2-cells induce proliferation of B-cells, which travel to secondary lymphatic organs in mucosa-associated lymphoid tissue (MALT) and differentiate into immunoglobulin (Ig)-producing plasma cells, which may migrate back to the infection site. 12 Secretory antibodies neutralize the virus

References

    1. Fendrick AM, Monto AS, Nightengale B, Sarnes M. The economic burden of non-influenza-related viral respiratory tract infection in the United States. Arch Intern Med. 2003;163:487–494. doi: 10.1001/archinte.163.4.487.
    1. Tapparel C, Siegrist F, Petty TJ, Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol. 2013;14:282–293. doi: 10.1016/j.meegid.2012.10.016.
    1. Zambon MC. Epidemiology and pathogenesis of influenza. J Antimicrob Chemother. 1999;44:3–9. doi: 10.1093/jac/44.suppl_2.3.
    1. Langley GF, Anderson LJ. Epidemiology and prevention of respiratory syncytial virus infections among infants and young children. Pediatr Infect Dis J. 2011;30:510–517.
    1. Robinson CM, Seto D, Jones MS, Dyer DW, Chodosh J. Molecular evolution of human species D adenoviruses. Infect Genet Evol. 2011;11:1208–1217. doi: 10.1016/j.meegid.2011.04.031.
    1. Nichols WG, Peck Campbell AJ, Boeckh M. Respiratory viruses other than influenza virus: impact and therapeutic advances. Clin Microbiol Rev. 2008;21:274–290. doi: 10.1128/CMR.00045-07.
    1. Jartti T, Jartti L, Ruuskanen O, Söderlund-Venermo M. New respiratory viral infections. Curr Opin Pulm Med. 2012;18:271–278. doi: 10.1097/MCP.0b013e328351f8d4.
    1. Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO) (2002) Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food
    1. Food and Agriculture Organization of the United Nations/World Health Organization (FAO/WHO) (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria
    1. Wolvers D, Antoine JM, Myllyluoma E, Schrezenmeir J, Szajewska H, Rijkers GT. Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of infections by probiotics. J Nutr. 2010;140:698S–712S. doi: 10.3945/jn.109.113753.
    1. Aureli P, Capurso L, Castellazzi AM, Clerici M, Giovannini M, Morelli L, et al. Probiotics and health: an evidence-based review. Pharmacol Res. 2011;63:366–376. doi: 10.1016/j.phrs.2011.02.006.
    1. Servin AL. Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev. 2004;28:405–440. doi: 10.1016/j.femsre.2004.01.003.
    1. Bodera P, Chcialowski A. Immunomodulatory effect of probiotic bacteria. Recent Pat Inflamm Allergy Drug Discov. 2009;3:58–64. doi: 10.2174/187221309787158461.
    1. Guarino A, Lo Vecchio A, Canani RB. Probiotics as prevention and treatment for diarrhea. Curr Opin Gastroenterol. 2009;25:18–23. doi: 10.1097/MOG.0b013e32831b4455.
    1. Hao Q, Lu Z, Dong BR, Huang CQ, Wu T (2011) Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst Rev (9):CD006895
    1. Hori T, Kiyoshima J, Shida K, Yasui H. Effect of intranasal administration of Lactobacillus casei Shirota on influenza virus infection of upper respiratory tract in mice. Clin Diagn Lab Immunol. 2001;8:593–597.
    1. Yasui H, Kiyoshima J, Hori T. Reduction of influenza virus titer and protection against influenza virus infection in infant mice fed Lactobacillus casei shirota. Clin Diagn Lab Immunol. 2004;11:675–679.
    1. Maeda N, Nakamura R, Hirose Y, Murosaki S, Yamamoto Y, Kase T, et al. Oral administration of heat-killed Lactobacillus plantarum L-137 enhances protection against influenza virus infection by stimulation of type I interferon production in mice. Int Immunopharmacol. 2009;9:1122–1125. doi: 10.1016/j.intimp.2009.04.015.
    1. Takeda S, Takeshita M, Kikuchi Y, Dashnyam B, Kawahara S, Yoshida H, et al. Efficacy of oral administration of heat-killed probiotics from Mongolian dairy products against influenza infection in mice: alleviation of influenza infection by its immunomodulatory activity through intestinal immunity. Int Immunopharmacol. 2011;11:1976–1983. doi: 10.1016/j.intimp.2011.08.007.
    1. Park MK, Ngo V, Kwon YM, Lee YT, Yoo S, Cho YH, et al. Lactobacillus plantarum DK119 as a probiotic confers protection against influenza virus by modulating innate immunity. PLoS One. 2013;8:e75368. doi: 10.1371/journal.pone.0075368.
    1. Kawase M, He F, Kubota A, Harata G, Hiramatsu M. Oral administration of lactobacilli from human intestinal tract protects mice against influenza virus infection. Lett Appl Microbiol. 2010;51:6–10.
    1. Kawase M, He F, Kubota A, Yoda K, Miyazawa K, Hiramatsu M. Heat-killed Lactobacillus gasseri TMC0356 protects mice against influenza virus infection by stimulating gut and respiratory immune responses. FEMS Immunol Med Microbiol. 2012;64:280–288. doi: 10.1111/j.1574-695X.2011.00903.x.
    1. Harata G, He F, Hiruta N, Kawase M, Kubota A, Hiramatsu M, et al. Intranasal administration of Lactobacillus rhamnosus GG protects mice from H1N1 influenza virus infection by regulating respiratory immune responses. Lett Appl Microbiol. 2010;50:597–602. doi: 10.1111/j.1472-765X.2010.02844.x.
    1. Harata G, He F, Hiruta N, Kawase M, Kubota A, Hiramatsu M, et al. Intranasally administered Lactobacillus gasseri TMC0356 protects mice from H1N1 influenza virus infection by stimulating respiratory immune responses. World J Microbiol Biotechnol. 2011;27:411–416. doi: 10.1007/s11274-010-0472-x.
    1. Lee YN, Youn HN, Kwon JH, Lee DH, Park JK, Yuk SS, et al. Sublingual administration of Lactobacillus rhamnosus affects respiratory immune responses and facilitates protection against influenza virus infection in mice. Antiviral Res. 2013;98:284–290. doi: 10.1016/j.antiviral.2013.03.013.
    1. Youn HN, Lee DH, Lee YN, Park JK, Yuk SS, Yang SY, et al. Intranasal administration of live Lactobacillus species facilitates protection against influenza virus infection in mice. Antiviral Res. 2012;93:138–143. doi: 10.1016/j.antiviral.2011.11.004.
    1. Yeo JM, Lee HJ, Kim JW, Lee JB, Park SY, Choi IS, et al. Lactobacillus fermentum CJL-112 protects mice against influenza virus infection by activating T-helper 1 and eliciting a protective immune response. Int Immunopharmacol. 2014;18:50–54. doi: 10.1016/j.intimp.2013.10.020.
    1. Waki N, Yajima N, Suganuma H, Buddle BM, Luo D, Heiser A, et al. Oral administration of Lactobacillus brevis KB290 to mice alleviates clinical symptoms following influenza virus infection. Lett Appl Microbiol. 2014;58:87–93. doi: 10.1111/lam.12160.
    1. Izumo T, Maekawa T, Ida M, Noguchi A, Kitagawa Y, Shibata H, et al. Effect of intranasal administration of Lactobacillus pentosus S-PT84 on influenza virus infection in mice. Int Immunopharmacol. 2010;10:1101–1106. doi: 10.1016/j.intimp.2010.06.012.
    1. Kobayashi N, Saito T, Uematsu T, Kishi K, Toba M, Kohda N, et al. Oral administration of heat-killed Lactobacillus pentosus strain b240 augments protection against influenza virus infection in mice. Int Immunopharmacol. 2011;11:199–203. doi: 10.1016/j.intimp.2010.11.019.
    1. Kiso M, Takano R, Sakabe S, Katsura H, Shinya K, Uraki R, et al. Protective efficacy of orally administered, heat-killed Lactobacillus pentosus b240 against influenza A virus. Sci Rep. 2013;3:1–8. doi: 10.1038/srep01563.
    1. Goto H, Sagitani A, Ashida N, Kato S, Hirota T, Shinoda T, et al. Anti-influenza virus effects of both live and non-live Lactobacillus acidophilus L-92 accompanied by the activation of innate immunity. Br J Nutr. 2013;110:1810–1818. doi: 10.1017/S0007114513001104.
    1. Iwabuchi N, Xiao JZ, Yaeshima T, Iwatsuki K. Oral administration of Bifidobacterium longum ameliorates influenza virus infection in mice. Biol Pharm Bull. 2011;34:1352–1355. doi: 10.1248/bpb.34.1352.
    1. Wu S, Jiang ZY, Sun YF, Yu B, Chen J, Dai CQ, et al. Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza a virus infection. Curr Microbiol. 2013;67:414–422. doi: 10.1007/s00284-013-0380-z.
    1. Gabryszewski SJ, Bachar O, Dyer KD, Percopo CM, Killoran KE, Domachowske JB, et al. Lactobacillus-mediated priming of the respiratory mucosa protects against lethal pneumovirus infection. J Immunol. 2011;186:1151–1161. doi: 10.4049/jimmunol.1001751.
    1. Garcia-Crespo KE, Chan CC, Gabryszewski SJ, Percopo CM, Rigaux P, Dyer KD, et al. Lactobacillus priming of the respiratory tract: heterologous immunity and protection against lethal pneumovirus infection. Antiviral Res. 2013;97:270–279. doi: 10.1016/j.antiviral.2012.12.022.
    1. Tomosada Y, Chiba E, Zelaya H, Takahashi T, Tsukida K, Kitazawa H, et al. Nasally administered Lactobacillus rhamnosus strains differentially modulate respiratory antiviral immune responses and induce protection against respiratory syncytial virus infection. BMC Immunol. 2013;14:40. doi: 10.1186/1471-2172-14-40.
    1. Kechaou N, Chain F, Gratadoux JJ, Blugeon S, Bertho N, Chevalier C, et al. Identification of one novel candidate probiotic lactobacillus plantarum strain active against influenza virus infection in mice by a large-scale screening. Appl Environ Microbiol. 2013;79:1491–1499. doi: 10.1128/AEM.03075-12.
    1. Nagai T, Makino S, Ikegami S, Itoh H, Yamada H. Effects of oral administration of yogurt fermented with Lactobacillus delbrueckii ssp. bulgaricus OLL1073R-1 and its exopolysaccharides against influenza virus infection in mice. Int Immunopharmacol. 2011;11:2246–2250. doi: 10.1016/j.intimp.2011.09.012.
    1. Maruo T, Gotoh Y, Nishimura H, Ohashi S, Toda T, Takahashi K. Oral administration of milk fermented with Lactococcus lactis subsp. cremoris FC protects mice against influenza virus infection. Lett Appl Microbiol. 2012;55:135–140. doi: 10.1111/j.1472-765X.2012.03270.x.
    1. Yasui H, Kiyoshima J, Hori T, Shida K. Protection against influenza virus infection of mice fed Bifidobacterium breve YIT4064. Clin Diagn Lab Immunol. 1999;6:186–192.
    1. Hatakka K, Savilahti E, Pönkä A, Meurman JH, Poussa T, Näse L, et al. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. Br Med J. 2001;322:1327–1329. doi: 10.1136/bmj.322.7298.1327.
    1. Hojsak I, Snovak N, Abdović S, Szajewska H, Misak Z, Kolacek S. 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. 2010;29:312–316. doi: 10.1016/j.clnu.2009.09.008.
    1. Hojsak I, Abdović S, Szajewska H, Milošević M, Krznarić Ž, Kolaček S. Lactobacillus GG in the prevention of nosocomial gastrointestinal and respiratory tract infections. Pediatrics. 2010;125:e1171–e1177. doi: 10.1542/peds.2009-2568.
    1. Kumpu M, Kekkonen RA, Kautiainen H, Järvenpää S, Kristo A, Huovinen P, et al. Milk containing probiotic Lactobacillus rhamnosus GG and respiratory illness in children: a randomized, double-blind, placebo-controlled trial. Eur J Clin Nutr. 2012;66:1020–1023. doi: 10.1038/ejcn.2012.62.
    1. Luoto R, Ruuskanen O, Waris M, Kalliomäki M, Salminen S, Isolauri E (2013) Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: a randomized, placebo-controlled trial. J Allergy Clin Immunol pii: S0091-6749(13)01307-9
    1. Kumpu M, Lehtoranta L, Roivainen M, Rönkkö E, Ziegler T, Söderlund-Venermo M, et al. The use of the probiotic Lactobacillus rhamnosus GG and viral findings in the nasopharynx of children attending day care. J Med Virol. 2013;85:1652–1658. doi: 10.1002/jmv.23623.
    1. Liu S, Hu P, Du X, Zhou T, Pei X. Lactobacillus rhamnosus GG supplementation for preventing respiratory infections in children: a meta-analysis of randomized, placebo-controlled trials. Indian Pediatr. 2013;50:377–381. doi: 10.1007/s13312-013-0123-z.
    1. Lin JS, Chiu YH, Lin NT, Chu CH, Huang KC, Liao KW, et al. Different effects of probiotic species/strains on infections in preschool children: a double-blind, randomized, controlled study. Vaccine. 2009;27:1073–1079. doi: 10.1016/j.vaccine.2008.11.114.
    1. Cobo Sanz JM, Mateos JA, Muñoz Conejo A. Effect of Lactobacillus casei on the incidence of infectious conditions in children. Nutr Hosp. 2006;21:547–551.
    1. Maldonado J, Cañabate F, Sempere L, Vela F, Sánchez AR, Narbona E, et al. Human milk probiotic lactobacillus fermentum CECT5716 reduces the incidence of gastrointestinal and upper respiratory tract infections in infants. J Pediatr Gastroenterol Nutr. 2012;54:55–61. doi: 10.1097/MPG.0b013e3182333f18.
    1. Taipale T, Pienihäkkinen K, Isolauri E, Larsen C, Brockmann E, Alanen P, et al. Bifidobacterium animalis subsp. lactis BB-12 in reducing the risk of infections in infancy. Br J Nutr. 2011;105:409–416. doi: 10.1017/S0007114510003685.
    1. Weizman Z, Asli G, Alsheikh A. Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics. 2005;115:5–9.
    1. Niittynen L, Pitkäranta A, Korpela R. Probiotics and otitis media in children. Int J Pediatr Otorhinolaryngol. 2012;76:465–470. doi: 10.1016/j.ijporl.2012.01.011.
    1. Agustina R, Kok FJ, Van De Rest O, Fahmida U, Firmansyah A, Lukito W, et al. Randomized trial of probiotics and calcium on diarrhea and respiratory tract infections in Indonesian children. Pediatrics. 2012;129(5):e1155–e1164. doi: 10.1542/peds.2011-1379.
    1. Hatakka K, Blomgren K, Pohjavuori S, Kaijalainen T, Poussa T, Leinonen M, et al. Treatment of acute otitis media with probiotics in otitis-prone children—a double-blind, placebo-controlled randomised study. Clin Nutr. 2007;26:314–321. doi: 10.1016/j.clnu.2007.01.003.
    1. Rautava S, Salminen S, Isolauri E. Specific probiotics in reducing the risk of acute infections in infancy—a randomised, double-blind, placebo-controlled study. Br J Nutr. 2009;101:1722–1726. doi: 10.1017/S0007114508116282.
    1. Rerksuppaphol S, Rerksuppaphol L. Randomized controlled trial of probiotics to reduce common cold in schoolchildren. Pediatr Int. 2012;54:682–687. doi: 10.1111/j.1442-200X.2012.03647.x.
    1. Lehtoranta L, Söderlund-Venermo M, Nokso-Koivisto J, Toivola H, Blomgren K, Hatakka K, et al. Human bocavirus in the nasopharynx of otitis-prone children. Int J Pediatr Otorhinolaryngol. 2012;76:206–211. doi: 10.1016/j.ijporl.2011.10.025.
    1. Hatakka K (2007) Probiotics in the prevention of clinical manifestations of common infectious diseases in children and in the elderly. Dissertation, University of Helsinki
    1. Olivares M, Díaz-Ropero MP, Sierra S, Lara-Villoslada F, Fonollá J, Navas M, et al. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition. 2007;23:254–260. doi: 10.1016/j.nut.2007.01.004.
    1. Winkler P, de Vrese M, Laue Ch, Schrezenmeir J. Effect of a dietary supplement containing probiotic bacteria plus vitamins and minerals on common cold infections and cellular immune parameters. Int J Clin Pharmacol Ther. 2005;43:318–326. doi: 10.5414/CPP43318.
    1. de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, et al. Effect of Lactobacillus gasseri PA 16/8, Bifidobacterium longum SP 07/3, B. bifidum MF 20/5 on common cold episodes: a double blind, randomized, controlled trial. Clin Nutr. 2005;24:481–491. doi: 10.1016/j.clnu.2005.02.006.
    1. de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, et al. Probiotic bacteria reduced duration and severity but not the incidence of common cold episodes in a double blind, randomized, controlled trial. Vaccine. 2006;24:6670–6674. doi: 10.1016/j.vaccine.2006.05.048.
    1. West NP, Horn PL, Pyne DB, Gebski VJ, Lahtinen SJ, Fricker PA et al (2013) Probiotic supplementation for respiratory and gastrointestinal illness symptoms in healthy physically active individuals. Clin Nutr pii: S0261-5614(13)00261-6
    1. Smith TJ, Rigassio-Radler D, Denmark R, Haley T, Touger-Decker R. Effect of Lactobacillus rhamnosus LGG® and Bifidobacterium animalis ssp. lactis BB-12® on health-related quality of life in college students affected by upper respiratory infections. Br J Nutr. 2013;109:1999–2007. doi: 10.1017/S0007114512004138.
    1. Cox AJ, Pyne DB, Saunders PU, Fricker PA. Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. Br J Sports Med. 2010;44:222–226. doi: 10.1136/bjsm.2007.044628.
    1. West NP, Pyne DB, Cripps AW, Hopkins WG, Eskesen DC, Jairath A, et al. Lactobacillus fermentum (PCC®) supplementation and gastrointestinal and respiratory-tract illness symptoms: a randomised control trial in athletes. Nutr J. 2011;10:30. doi: 10.1186/1475-2891-10-30.
    1. Haywood BA, Black KE, Baker D, McGarvey J, Healey P, Brown RC (2013) Probiotic supplementation reduces the duration and incidence of infections but not severity in elite rugby union players. J Sci Med Sport pii: S1440-2440(13)00190-4
    1. Kekkonen RA, Vasankari TJ, Vuorimaa T, Haahtela T, Julkunen I, Korpela R. The effect of probiotics on respiratory infections and gastrointestinal symptoms during training in marathon runners. Int J Sport Nutr Exerc Metab. 2007;17:352–363.
    1. Tiollier E, Chennaoui M, Gomez-Merino D, Drogou C, Filaire E, Guezennec CY. Effect of a probiotics supplementation on respiratory infections and immune and hormonal parameters during intense military training. Mil Med. 2007;172:1006–1011.
    1. Gleeson M, Bishop NC, Oliveira M, McCauley T, Tauler P, Lawrence C. Effects of a Lactobacillus salivarius probiotic intervention on infection, cold symptom duration and severity, and mucosal immunity in endurance athletes. Int J Sport Nutr Exerc Metab. 2012;22:235–242.
    1. Guillemard E, Tanguy J, Flavigny A, de la Motte S, Schrezenmeir J. Effects of consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114 001 on common respiratory and gastrointestinal infections in shift workers in a randomized controlled trial. J Am Coll Nutr. 2010;29:455–468. doi: 10.1080/07315724.2010.10719882.
    1. Turchet P, Laurenzano M, Auboiron S, Antoine JM. Effect of fermented milk containing the probiotic Lactobacillus casei DN-114001 on winter infections in free-living elderly subjects: a randomised, controlled pilot study. J Nutr Health Aging. 2003;7:75–77.
    1. Guillemard E, Tondu F, Lacoin F, Schrezenmeir J. Consumption of a fermented dairy product containing the probiotic Lactobacillus casei DN-114001 reduces the duration of respiratory infections in the elderly in a randomised controlled trial. Br J Nutr. 2010;103:58–68. doi: 10.1017/S0007114509991395.
    1. Fujita R, Iimuro S, Shinozaki T, Sakamaki K, Uemura Y, Takeuchi A, et al. Decreased duration of acute upper respiratory tract infections with daily intake of fermented milk: a multicenter, double-blinded, randomized comparative study in users of day care facilities for the elderly population. Am J Infect Control. 2013;41:1231–1235. doi: 10.1016/j.ajic.2013.04.005.
    1. Van Puyenbroeck K, Hens N, Coenen S, Michiels B, Beunckens C, Molenberghs G, et al. Efficacy of daily intake of Lactobacillus casei Shirota on respiratory symptoms and influenza vaccination immune response: a randomized, double-blind, placebo-controlled trial in healthy elderly nursing home residents. Am J Clin Nutr. 2012;95:1165–1171. doi: 10.3945/ajcn.111.026831.
    1. Merenstein D, Murphy M, Fokar A, Hernandez RK, Park H, Nsouli H, et al. Use of a fermented dairy probiotic drink containing Lactobacillus casei (DN-114 001) to decrease the rate of illness in kids: the DRINK study. A patient-oriented, double-blind, cluster-randomized, placebo-controlled, clinical trial. Eur J Clin Nutr. 2010;64:669–677. doi: 10.1038/ejcn.2010.65.
    1. Agarwal S, Busse PJ. Innate and adaptive immunosenescence. Ann Allergy Asthma Immunol. 2010;104:183–190. doi: 10.1016/j.anai.2009.11.009.
    1. Lehtoranta L (2012) Probiotics and virus infections: the effects of Lactobacillus rhamnosus GG on respiratory and gastrointestinal virus infections. Dissertation, University of Helsinki
    1. Botić T, Klingberg TD, Weingartl H, Cencic A. A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int J Food Microbiol. 2007;115:227–234. doi: 10.1016/j.ijfoodmicro.2006.10.044.
    1. Choi H-J, Song J-H, Ahn Y-J, Baek S-H, Kwon D-H. Antiviral activities of cell-free supernatants of yogurts metabolites against some RNA viruses. Eur Food Res Technol. 2009;228:945–950. doi: 10.1007/s00217-009-1009-0.
    1. Ivec M, Botić T, Koren S, Jakobsen M, Weingartl H, Cencic A. Interactions of macrophages with probiotic bacteria lead to increased antiviral response against vesicular stomatitis virus. Antiviral Res. 2007;75:266–274. doi: 10.1016/j.antiviral.2007.03.013.
    1. Pipenbaher N, Moeller PL, Dolinšek J, Jakobsen M, Weingartl H, Cencič A. Nitric oxide (NO) production in mammalian non-tumorigenic epithelial cells of the small intestine and macrophages induced by individual strains of lactobacilli and bifidobacteria. Int Dairy J. 2009;19:166–171. doi: 10.1016/j.idairyj.2008.09.003.
    1. Miettinen M, Matikainen S, Vuopio-Varkila J, Pirhonen J, Varkila K, Kurimoto M, et al. Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect Immun. 1998;66:6058–6062.
    1. Vinderola G, Matar C, Perdigon G. Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: Involvement of Toll-like receptors. Clin Diagn Lab Immunol. 2005;12:1075–1084.
    1. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, Poiret S, et al. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol. 2007;13:236–243. doi: 10.3748/wjg.v13.i2.236.
    1. Miettinen M, Veckman V, Latvala S, Sareneva T, Matikainen S, Julkunen I. Live Lactobacillus rhamnosus and Streptococcus pyogenes differentially regulate Toll-like receptor (TLR) gene expression in human primary macrophages. J Leukoc Biol. 2008;84:1092–1100. doi: 10.1189/jlb.1206737.
    1. O’Hara AM, O’Regan P, Fanning A, O’Mahony C, MacSharry J, Lyons A, et al. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology. 2006;118:202–215. doi: 10.1111/j.1365-2567.2006.02358.x.
    1. Latvala S, Miettinen M, Kekkonen R, Korpela R, Julkunen I. Potentially probiotic bacteria induce cytokine production and suppressor of cytokine signaling 3 gene expression in human monocyte-derived macrophages. Cytokine. 2009;48:100–101. doi: 10.1016/j.cyto.2009.07.423.
    1. Miettinen M, Lehtonen A, Julkunen I, Matikainen S. Lactobacilli and streptococci activate NF-kappa B and STAT signaling pathways in human macrophages. J Immunol. 2000;164:3733–3740. doi: 10.4049/jimmunol.164.7.3733.
    1. Veckman V, Miettinen M, Matikainen S, Lande R, Giacomini E, Coccia EM, et al. Lactobacilli and streptococci induce inflammatory chemokine production in human macrophages that stimulates Th1 cell chemotaxis. J Leukoc Biol. 2003;74:395–402. doi: 10.1189/jlb.0402212.
    1. Veckman V, Miettinen M, Pirhonen J, Sirén J, Matikainen S, Julkunen I. Streptococcus pyogenes and Lactobacillus rhamnosus differentially induce maturation and production of Th1-type cytokines and chemokines in human monocyte-derived dendritic cells. J Leukoc Biol. 2004;75:764–771. doi: 10.1189/jlb.1003461.
    1. Latvala S, Miettinen M, Kekkonen RA, Korpela R, Julkunen I. Lactobacillus rhamnosus GG and Streptococcus thermophilus induce suppressor of cytokine signalling 3 (SOCS3) gene expression directly and indirectly via interleukin-10 in human primary macrophages. Clin Exp Immunol. 2011;165:94–103. doi: 10.1111/j.1365-2249.2011.04408.x.
    1. Weiss G, Rasmussen S, Zeuthen LH, Nielsen BN, Jarmer H, Jespersen L, et al. Lactobacillus acidophilus induces virus immune defence genes in murine dendritic cells by a Toll-like receptor-2-dependent mechanism. Immunology. 2010;131:268–281. doi: 10.1111/j.1365-2567.2010.03301.x.
    1. Weiss G, Christensen HR, Zeuthen LH, Vogensen FK, Jakobsen M, Frøkiær H. Lactobacilli and bifidobacteria induce differential interferon-beta profiles in dendritic cells. Cytokine. 2011;56:520–530. doi: 10.1016/j.cyto.2011.07.024.
    1. Miettinen M, Pietilä TE, Kekkonen RA, Kankainen M, Latvala S, Pirhonen J, et al. Nonpathogenic Lactobacillus rhamnosus activates the inflammasome and antiviral responses in human macrophages. Gut Microbes. 2012;3:510–522. doi: 10.4161/gmic.21736.
    1. Hori T, Kiyoshima J, Shida K, Yasui H. Augmentation of cellular immunity and reduction of influenza virus titer in aged mice fed Lactobacillus casei strain Shirota. Clin Diagn Lab Immunol. 2002;9:105–108.
    1. Davidson LE, Fiorino AM, Snydman DR, Hibberd PL. Lactobacillus GG as an immune adjuvant for live-attenuated influenza vaccine in healthy adults: a randomized double-blind placebo-controlled trial. Eur J Clin Nutr. 2011;65:501–507. doi: 10.1038/ejcn.2010.289.
    1. Rizzardini G, Eskesen D, Calder PC, Capetti A, Jespersen L, Clerici M. Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12® and Lactobacillus paracasei ssp. paracasei, L. casei 431® in an influenza vaccination model: a randomised, double-blind, placebo-controlled study. Br J Nutr. 2011;107:876–884. doi: 10.1017/S000711451100420X.
    1. Boge T, Rémigy M, Vaudaine S, Tanguy J, Bourdet-Sicard R, van der Werf S. A probiotic fermented dairy drink improves antibody response to influenza vaccination in the elderly in two randomised controlled trials. Vaccine. 2009;27:5677–5684. doi: 10.1016/j.vaccine.2009.06.094.
    1. Boyle RJ, Robins-Browne RM, Tang MLK. Probiotic use in clinical practice: what are the risks? Am J Clin Nutr. 2006;83:1256–1264.
    1. Sanders ME, Akkermans LM, Haller D, Hammerman C, Heimbach J, Hörmannsperger G, et al. Safety assessment of probiotics for human use. Gut Microbes. 2010;1:164–185. doi: 10.4161/gmic.1.3.12127.
    1. Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK. Lactobacillus sepsis associated with probiotic therapy. Pediatrics. 2005;115:178–181.
    1. Kalima P, Masterton RG, Roddie PH, Thomas AE. Lactobacillus rhamnosus infection in a child following bone marrow transplant. J Infect. 1996;32:165–167. doi: 10.1016/S0163-4453(96)91622-9.
    1. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet. 2008;371:651–659. doi: 10.1016/S0140-6736(08)60207-X.
    1. European Food Safety Authority (EFSA) Scientific Opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2011 update) EFSA J. 2011;9:2497.
    1. Salminen MK, Tynkkynen S, Rautelin H, Saxelin M, Vaara M, Ruutu P, et al. Lactobacillus bacteremia during a rapid increase in probiotic use of Lactobacillus rhamnosus GG in Finland. Clin Infect Dis. 2002;35:1155–1160. doi: 10.1086/342912.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться