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Published in: Virology Journal 1/2016

Open Access 01-12-2016 | Research

Antiviral activity of Lactobacillus reuteri Protectis against Coxsackievirus A and Enterovirus 71 infection in human skeletal muscle and colon cell lines

Authors: Lei Yin Emily Ang, Horng Khit Issac Too, Eng Lee Tan, Tak-Kwong Vincent Chow, Pei-Chi Lynette Shek, Elizabeth Tham, Sylvie Alonso

Published in: Virology Journal | Issue 1/2016

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Abstract

Background

Recurrence of hand, foot and mouth disease (HFMD) pandemics continues to threaten public health. Despite increasing awareness and efforts, effective vaccine and drug treatment have yet to be available. Probiotics have gained recognition in the field of healthcare worldwide, and have been extensively prescribed to babies and young children to relieve gastrointestinal (GI) disturbances and diseases, associated or not with microbial infections. Since the faecal-oral axis represents the major route of HFMD transmission, transient persistence of probiotic bacteria in the GI tract may confer some protection against HFMD and limit transmission among children.

Methods

In this work, the antiviral activity of two commercially available probiotics, namely Lactobacillus reuteri Protectis (L. reuteri Protectis) and Lactobacillus casei Shirota (L. casei Shirota), was assayed against Coxsackieviruses and Enterovirus 71 (EV71), the main agents responsible for HFMD. In vitro infection set-ups using human skeletal muscle and colon cell lines were designed to assess the antiviral effect of the probiotic bacteria during entry and post-entry steps of the infection cycle.

Results

Our findings indicate that L. reuteri Protectis displays a significant dose-dependent antiviral activity against Coxsackievirus type A (CA) strain 6 (CA6), CA16 and EV71, but not against Coxsackievirus type B strain 2. Our data support that the antiviral effect is likely achieved through direct physical interaction between bacteria and virus particles, which impairs virus entry into its mammalian host cell. In contrast, no significant antiviral effect was observed with L. casei Shirota.

Conclusions

Should the antiviral activity of L. reuteri Protectis observed in vitro be translated in vivo, such probiotics-based therapeutic approach may have the potential to address the urgent need for a safe and effective means to protect against HFMD and limit its transmission among children.
Literature
1.
go back to reference Bruu AL: Enteroviruses: Polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. A Practical Guide to Clinical Virology, Second Edition 2003;44-45. doi:10.1002/0470857285.ch6 Bruu AL: Enteroviruses: Polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. A Practical Guide to Clinical Virology, Second Edition 2003;44-45. doi:10.​1002/​0470857285.​ch6
2.
go back to reference Hirata O, Ishikawa N, Mizoguchi Y, Nakamura K, Kobayashi M. A case of neonatal coxsackie B2 meningo-encephalitis in which serial magnetic resonance imaging findings reveal the development of lesions. Neuropediatrics. 2011;42:156–8.CrossRefPubMed Hirata O, Ishikawa N, Mizoguchi Y, Nakamura K, Kobayashi M. A case of neonatal coxsackie B2 meningo-encephalitis in which serial magnetic resonance imaging findings reveal the development of lesions. Neuropediatrics. 2011;42:156–8.CrossRefPubMed
3.
go back to reference Wang SM, Liu CC. Update of enterovirus 71 infection: epidemiology, pathogenesis and vaccine. Expert Rev Anti Infect Ther. 2014;12:447–56.CrossRefPubMed Wang SM, Liu CC. Update of enterovirus 71 infection: epidemiology, pathogenesis and vaccine. Expert Rev Anti Infect Ther. 2014;12:447–56.CrossRefPubMed
4.
go back to reference Huang H-I, Weng K-F, Shih S-R. Viral and host factors that contribute to pathogenicity of enterovirus 71. Future Microbiol. 2012;7:467–79.CrossRefPubMed Huang H-I, Weng K-F, Shih S-R. Viral and host factors that contribute to pathogenicity of enterovirus 71. Future Microbiol. 2012;7:467–79.CrossRefPubMed
5.
go back to reference Mao Q, Wang Y, Yao X, Bian L, Wu X, Xu M, Liang Z. Coxsackievirus A16: epidemiology, diagnosis, and vaccine. Hum Vaccin Immunother. 2014;10:360–7.CrossRefPubMed Mao Q, Wang Y, Yao X, Bian L, Wu X, Xu M, Liang Z. Coxsackievirus A16: epidemiology, diagnosis, and vaccine. Hum Vaccin Immunother. 2014;10:360–7.CrossRefPubMed
6.
go back to reference Zeng M, Zheng X, Wei R, Zhang N, Zhu K, Xu B, Yang CH, Yang CF, Deng C, Pu D et al. The cytokine and chemokine profiles in patients with hand, foot and mouth disease of different severities in Shanghai, China, 2010. PLoS Negl Trop Dis. 2013;7,e2599.CrossRefPubMedPubMedCentral Zeng M, Zheng X, Wei R, Zhang N, Zhu K, Xu B, Yang CH, Yang CF, Deng C, Pu D et al. The cytokine and chemokine profiles in patients with hand, foot and mouth disease of different severities in Shanghai, China, 2010. PLoS Negl Trop Dis. 2013;7,e2599.CrossRefPubMedPubMedCentral
7.
go back to reference Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010;10:778–90.CrossRefPubMed Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, Ooi MH. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010;10:778–90.CrossRefPubMed
8.
go back to reference Xing W, Liao Q, Viboud C, Zhang J, Sun J, Wu JT, Chang Z, Liu F, Fang VJ, Zheng Y et al. Hand, foot, and mouth disease in China, 2008–12: an epidemiological study. Lancet Infect Dis. 2014;14:308–18.CrossRefPubMedPubMedCentral Xing W, Liao Q, Viboud C, Zhang J, Sun J, Wu JT, Chang Z, Liu F, Fang VJ, Zheng Y et al. Hand, foot, and mouth disease in China, 2008–12: an epidemiological study. Lancet Infect Dis. 2014;14:308–18.CrossRefPubMedPubMedCentral
9.
go back to reference Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, Bailly JL, Peigue-Lafeuille H. Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: a large citywide, prospective observational study. Clin Microbiol Infect. 2012;18:E110–8.CrossRefPubMed Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, Bailly JL, Peigue-Lafeuille H. Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: a large citywide, prospective observational study. Clin Microbiol Infect. 2012;18:E110–8.CrossRefPubMed
10.
go back to reference Ang LW, Tay J, Phoon MC, Hsu JP, Cutter J, James L, Goh KT, Chow VT. Seroepidemiology of Coxsackievirus A6, Coxsackievirus A16, and Enterovirus 71 Infections among Children and Adolescents in Singapore, 2008–2010. PLoS One. 2015;10:e0127999.CrossRefPubMedPubMedCentral Ang LW, Tay J, Phoon MC, Hsu JP, Cutter J, James L, Goh KT, Chow VT. Seroepidemiology of Coxsackievirus A6, Coxsackievirus A16, and Enterovirus 71 Infections among Children and Adolescents in Singapore, 2008–2010. PLoS One. 2015;10:e0127999.CrossRefPubMedPubMedCentral
11.
go back to reference Nguyen NT, Pham HV, Hoang CQ, Nguyen TM, Nguyen LT, Phan HC, Phan LT, Vu LN, Minh NNT. Epidemiological and clinical characteristics of children who died from hand, foot and mouth disease in Vietnam, 2011. BMC Infect Dis. 2014;14:341.CrossRefPubMedPubMedCentral Nguyen NT, Pham HV, Hoang CQ, Nguyen TM, Nguyen LT, Phan HC, Phan LT, Vu LN, Minh NNT. Epidemiological and clinical characteristics of children who died from hand, foot and mouth disease in Vietnam, 2011. BMC Infect Dis. 2014;14:341.CrossRefPubMedPubMedCentral
12.
go back to reference Sun S, Jiang L, Liang Z, Mao Q, Su W, Zhang H, Li X, Jin J, Xu L, Zhao D. Evaluation of monovalent and bivalent vaccines against lethal Enterovirus 71 and Coxsackievirus A16 infection in newborn mice. Hum Vaccin Immunother. 2014;10:2885–95.CrossRefPubMed Sun S, Jiang L, Liang Z, Mao Q, Su W, Zhang H, Li X, Jin J, Xu L, Zhao D. Evaluation of monovalent and bivalent vaccines against lethal Enterovirus 71 and Coxsackievirus A16 infection in newborn mice. Hum Vaccin Immunother. 2014;10:2885–95.CrossRefPubMed
13.
go back to reference Liu CC, Chow YH, Chong P, Klein M. Prospect and challenges for the development of multivalent vaccines against hand, foot and mouth diseases. Vaccine. 2014;32:6177–82.CrossRefPubMed Liu CC, Chow YH, Chong P, Klein M. Prospect and challenges for the development of multivalent vaccines against hand, foot and mouth diseases. Vaccine. 2014;32:6177–82.CrossRefPubMed
14.
go back to reference Li JX, Mao QY, Liang ZL, Ji H, Zhu FC. Development of enterovirus 71 vaccines: from the lab bench to Phase III clinical trials. Expert Rev Vaccines. 2014;13:609–18.CrossRefPubMed Li JX, Mao QY, Liang ZL, Ji H, Zhu FC. Development of enterovirus 71 vaccines: from the lab bench to Phase III clinical trials. Expert Rev Vaccines. 2014;13:609–18.CrossRefPubMed
15.
go back to reference Chou AH, Liu CC, Chang JY, Jiang R, Hsieh YC, Tsao A, Wu CL, Huang JL, Fung CP, Hsieh SM. Formalin-inactivated EV71 vaccine candidate induced cross-neutralizing antibody against subgenotypes B1, B4, B5 and C4A in adult volunteers. PLoS One. 2013;8:e79783.CrossRefPubMedPubMedCentral Chou AH, Liu CC, Chang JY, Jiang R, Hsieh YC, Tsao A, Wu CL, Huang JL, Fung CP, Hsieh SM. Formalin-inactivated EV71 vaccine candidate induced cross-neutralizing antibody against subgenotypes B1, B4, B5 and C4A in adult volunteers. PLoS One. 2013;8:e79783.CrossRefPubMedPubMedCentral
16.
go back to reference Group JFWW. Guidelines for the evaluation of probiotics in food. London: World Health Organization. Canada: Food and Agriculture Organization; 2002. Group JFWW. Guidelines for the evaluation of probiotics in food. London: World Health Organization. Canada: Food and Agriculture Organization; 2002.
17.
go back to reference Reid G, Sanders M, Gaskins HR, Gibson GR, Mercenier A, Rastall R, Roberfroid M, Rowland I, Cherbut C, Klaenhammer TR. New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol. 2003;37:105–18.CrossRefPubMed Reid G, Sanders M, Gaskins HR, Gibson GR, Mercenier A, Rastall R, Roberfroid M, Rowland I, Cherbut C, Klaenhammer TR. New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol. 2003;37:105–18.CrossRefPubMed
18.
go back to reference Mach T. Clinical usefulness of probiotics. J Physiol Pharmacol. 2006;57:23–33.PubMed Mach T. Clinical usefulness of probiotics. J Physiol Pharmacol. 2006;57:23–33.PubMed
19.
go back to reference Yan F, Polk DB. Probiotics as functional food in the treatment of diarrhea. Curr Opin Clin Nutr Metab Care. 2006;9:717–21.CrossRefPubMed Yan F, Polk DB. Probiotics as functional food in the treatment of diarrhea. Curr Opin Clin Nutr Metab Care. 2006;9:717–21.CrossRefPubMed
20.
go back to reference Reid G. Probiotic Lactobacilli for urogenital health in women. J Clin Gastroenterol. 2008;42:S234–6.CrossRefPubMed Reid G. Probiotic Lactobacilli for urogenital health in women. J Clin Gastroenterol. 2008;42:S234–6.CrossRefPubMed
21.
23.
go back to reference Casas IA, Dobrogosz WJ. Validation of the probiotic concept: Lactobacillus reuteri confers broad-spectrum protection against disease in humans and animals. Microb Ecol Health Dis. 2000;12:247–85. Casas IA, Dobrogosz WJ. Validation of the probiotic concept: Lactobacillus reuteri confers broad-spectrum protection against disease in humans and animals. Microb Ecol Health Dis. 2000;12:247–85.
24.
go back to reference Hatakka K, Savilahti E, Pönkä A, Meurman JH, Poussa T, Näse L, Saxelin M, Korpela R. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ. 2001;322:1327.CrossRefPubMedPubMedCentral Hatakka K, Savilahti E, Pönkä A, Meurman JH, Poussa T, Näse L, Saxelin M, Korpela R. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ. 2001;322:1327.CrossRefPubMedPubMedCentral
25.
go back to reference Näse L, Hatakka K, Savilahti E, Saxelin M, Pönkä A, Poussa T, Korpela R, Meurman JH. 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;35:412–20.CrossRefPubMed Näse L, Hatakka K, Savilahti E, Saxelin M, Pönkä A, Poussa T, Korpela R, Meurman JH. 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;35:412–20.CrossRefPubMed
26.
go back to reference Choi H-J, Song J-H, Park K-S, Baek S-H, Lee E-S, Kwon D-H. Antiviral activity of yogurt against enterovirus 71 in vero cells. Food Sci Biotechnol. 2010;19:289–95.CrossRef Choi H-J, Song J-H, Park K-S, Baek S-H, Lee E-S, Kwon D-H. Antiviral activity of yogurt against enterovirus 71 in vero cells. Food Sci Biotechnol. 2010;19:289–95.CrossRef
27.
go back to reference Urbanska M, Szajewska H. The efficacy of Lactobacillus reuteri DSM 17938 in infants and children: a review of the current evidence. Eur J Pediatr. 2014;173:1327–37.CrossRefPubMedPubMedCentral Urbanska M, Szajewska H. The efficacy of Lactobacillus reuteri DSM 17938 in infants and children: a review of the current evidence. Eur J Pediatr. 2014;173:1327–37.CrossRefPubMedPubMedCentral
28.
go back to reference Savino F, Ceratto S, Poggi E, Cartosio ME, Cordero di Montezemolo L, Giannattasio A. Preventive effects of oral probiotic on infantile colic: a prospective, randomised, blinded, controlled trial using Lactobacillus reuteri DSM 17938. Benef Microbes. 2015;6:245–51.CrossRefPubMed Savino F, Ceratto S, Poggi E, Cartosio ME, Cordero di Montezemolo L, Giannattasio A. Preventive effects of oral probiotic on infantile colic: a prospective, randomised, blinded, controlled trial using Lactobacillus reuteri DSM 17938. Benef Microbes. 2015;6:245–51.CrossRefPubMed
29.
go back to reference Dinleyici EC, Group PS, Vandenplas Y. Lactobacillus reuteri DSM 17938 effectively reduces the duration of acute diarrhoea in hospitalised children. Acta Paediatr. 2014;103:e300–5.CrossRefPubMed Dinleyici EC, Group PS, Vandenplas Y. Lactobacillus reuteri DSM 17938 effectively reduces the duration of acute diarrhoea in hospitalised children. Acta Paediatr. 2014;103:e300–5.CrossRefPubMed
30.
go back to reference Savino F, Fornasero S, Ceratto S, De Marco A, Mandras N, Roana J, Tullio V, Amisano G. Probiotics and gut health in infants: A preliminary case-control observational study about early treatment with Lactobacillus reuteri DSM 17938. Clin Chim Acta. 2015;451:82–7.CrossRefPubMed Savino F, Fornasero S, Ceratto S, De Marco A, Mandras N, Roana J, Tullio V, Amisano G. Probiotics and gut health in infants: A preliminary case-control observational study about early treatment with Lactobacillus reuteri DSM 17938. Clin Chim Acta. 2015;451:82–7.CrossRefPubMed
31.
go back to reference Koebnick C, Wagner I, Leitzmann P, Stern U, Zunft HF. Probiotic beverage containing Lactobacillus casei Shirota improves gastrointestinal symptoms in patients with chronic constipation-The aim of the present study was to investigate the effect of a. Can J Gastroenterol. 2003;17:655–60.CrossRefPubMed Koebnick C, Wagner I, Leitzmann P, Stern U, Zunft HF. Probiotic beverage containing Lactobacillus casei Shirota improves gastrointestinal symptoms in patients with chronic constipation-The aim of the present study was to investigate the effect of a. Can J Gastroenterol. 2003;17:655–60.CrossRefPubMed
32.
go back to reference Shida K, Sato T, Iizuka R, Hoshi R, Watanabe O, Igarashi T, Miyazaki K, Nanno M, Ishikawa F. Daily intake of fermented milk with Lactobacillus casei strain Shirota reduces the incidence and duration of upper respiratory tract infections in healthy middle-aged office workers. Eur J Nutr. 2015. Shida K, Sato T, Iizuka R, Hoshi R, Watanabe O, Igarashi T, Miyazaki K, Nanno M, Ishikawa F. Daily intake of fermented milk with Lactobacillus casei strain Shirota reduces the incidence and duration of upper respiratory tract infections in healthy middle-aged office workers. Eur J Nutr. 2015.
33.
go back to reference Ishikawa H, Akedo I, Otani T, Suzuki T, Nakamura T, Takeyama I, Ishiguro S, Miyaoka E, Sobue T, Kakizoe T. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int J Cancer. 2005;116:762–7.CrossRefPubMed Ishikawa H, Akedo I, Otani T, Suzuki T, Nakamura T, Takeyama I, Ishiguro S, Miyaoka E, Sobue T, Kakizoe T. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumors. Int J Cancer. 2005;116:762–7.CrossRefPubMed
34.
go back to reference De Roos NM, Katan MB. Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: a review of papers published between 1988 and 1998. Am J Clin Nutr. 2000;71:405–11.PubMed De Roos NM, Katan MB. Effects of probiotic bacteria on diarrhea, lipid metabolism, and carcinogenesis: a review of papers published between 1988 and 1998. Am J Clin Nutr. 2000;71:405–11.PubMed
35.
go back to reference Srinivasan R, Meyer R, Padmanabhan R, Britto J. Clinical safety of Lactobacillus casei shirota as a probiotic in critically ill children. J Pediatr Gastroenterol Nutr. 2006;42:171–3.CrossRefPubMed Srinivasan R, Meyer R, Padmanabhan R, Britto J. Clinical safety of Lactobacillus casei shirota as a probiotic in critically ill children. J Pediatr Gastroenterol Nutr. 2006;42:171–3.CrossRefPubMed
36.
go back to reference Rosander A, Connolly E, Roos S. Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl Environ Microbiol. 2008;74:6032–40.CrossRefPubMedPubMedCentral Rosander A, Connolly E, Roos S. Removal of antibiotic resistance gene-carrying plasmids from Lactobacillus reuteri ATCC 55730 and characterization of the resulting daughter strain, L. reuteri DSM 17938. Appl Environ Microbiol. 2008;74:6032–40.CrossRefPubMedPubMedCentral
37.
go back to reference Pöyry T, Hyypiä T, Horsnell C, Kinnunen L, Hovi T, Stanway G. Molecular analysis of coxsackievirus A16 reveals a new genetic group of enteroviruses. Virology. 1994;202:982–7.CrossRefPubMed Pöyry T, Hyypiä T, Horsnell C, Kinnunen L, Hovi T, Stanway G. Molecular analysis of coxsackievirus A16 reveals a new genetic group of enteroviruses. Virology. 1994;202:982–7.CrossRefPubMed
38.
go back to reference Singh S, Poh CL, Chow VTK. Complete Sequence Analyses of Enterovirus 71 Strains from Fatal and Non‐Fatal Cases of the Hand, Foot and Mouth Disease Outbreak in Singapore (2000). Microbiol Immunol. 2002;46:801–8.CrossRefPubMed Singh S, Poh CL, Chow VTK. Complete Sequence Analyses of Enterovirus 71 Strains from Fatal and Non‐Fatal Cases of the Hand, Foot and Mouth Disease Outbreak in Singapore (2000). Microbiol Immunol. 2002;46:801–8.CrossRefPubMed
39.
go back to reference Al Kassaa I, Hober D, Hamze M, Chihib NE, Drider D. Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics Antimicrob Proteins. 2014;6:177–85.CrossRefPubMed Al Kassaa I, Hober D, Hamze M, Chihib NE, Drider D. Antiviral potential of lactic acid bacteria and their bacteriocins. Probiotics Antimicrob Proteins. 2014;6:177–85.CrossRefPubMed
40.
go back to reference Ong KC, Wong KT. Understanding Enterovirus 71 Neuropathogenesis and Its Impact on Other Neurotropic Enteroviruses. Brain Pathol. 2015;25:614–24.CrossRefPubMed Ong KC, Wong KT. Understanding Enterovirus 71 Neuropathogenesis and Its Impact on Other Neurotropic Enteroviruses. Brain Pathol. 2015;25:614–24.CrossRefPubMed
41.
go back to reference Chen CS, Yao YC, Lin SC, Lee YP, Wang YF, Wang JR, Liu CC, Lei HY, Yu CK. Retrograde axonal transport: a major transmission route of enterovirus 71 in mice. J Virol. 2007;81:8996–9003.CrossRefPubMedPubMedCentral Chen CS, Yao YC, Lin SC, Lee YP, Wang YF, Wang JR, Liu CC, Lei HY, Yu CK. Retrograde axonal transport: a major transmission route of enterovirus 71 in mice. J Virol. 2007;81:8996–9003.CrossRefPubMedPubMedCentral
42.
go back to reference Vollenweider S, Grassi G, König I, Puhan Z. Purification and structural characterization of 3-hydroxypropionaldehyde and its derivatives. J Agric Food Chem. 2003;51:3287–93.CrossRefPubMed Vollenweider S, Grassi G, König I, Puhan Z. Purification and structural characterization of 3-hydroxypropionaldehyde and its derivatives. J Agric Food Chem. 2003;51:3287–93.CrossRefPubMed
43.
go back to reference Cleusix V, Lacroix C, Vollenweider S, Duboux M, Le Blay G. Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 2007;7:101.CrossRefPubMedPubMedCentral Cleusix V, Lacroix C, Vollenweider S, Duboux M, Le Blay G. Inhibitory activity spectrum of reuterin produced by Lactobacillus reuteri against intestinal bacteria. BMC Microbiol. 2007;7:101.CrossRefPubMedPubMedCentral
44.
go back to reference Mastromarino P, Cacciotti F, Masci A, Mosca L. Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: role of cell wall associated components. Anaerobe. 2011;17:334–6.CrossRefPubMed Mastromarino P, Cacciotti F, Masci A, Mosca L. Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: role of cell wall associated components. Anaerobe. 2011;17:334–6.CrossRefPubMed
45.
go back to reference Xin KW, Huimin Y, Alonso S. Enterovirus 71: pathogenesis, control and models of disease. Futur Virol. 2012;7:989–1004.CrossRef Xin KW, Huimin Y, Alonso S. Enterovirus 71: pathogenesis, control and models of disease. Futur Virol. 2012;7:989–1004.CrossRef
46.
go back to reference Khong WX, Yan B, Yeo H, Tan EL, Lee JJ, Ng JK, Chow VT, Alonso S. A non-mouse-adapted enterovirus 71 (EV71) strain exhibits neurotropism, causing neurological manifestations in a novel mouse model of EV71 infection. J Virol. 2012;86:2121–31.CrossRefPubMedPubMedCentral Khong WX, Yan B, Yeo H, Tan EL, Lee JJ, Ng JK, Chow VT, Alonso S. A non-mouse-adapted enterovirus 71 (EV71) strain exhibits neurotropism, causing neurological manifestations in a novel mouse model of EV71 infection. J Virol. 2012;86:2121–31.CrossRefPubMedPubMedCentral
47.
go back to reference Hashimoto I, HAGIWARA A. Pathogenicity Of A Poliomyelitis‐Like Disease In Monkeys Infected Orally With Enterovirus 71: A Model For Human Infection. Neuropathol Appl Neurobiol. 1982;8:149–56.CrossRefPubMed Hashimoto I, HAGIWARA A. Pathogenicity Of A Poliomyelitis‐Like Disease In Monkeys Infected Orally With Enterovirus 71: A Model For Human Infection. Neuropathol Appl Neurobiol. 1982;8:149–56.CrossRefPubMed
Metadata
Title
Antiviral activity of Lactobacillus reuteri Protectis against Coxsackievirus A and Enterovirus 71 infection in human skeletal muscle and colon cell lines
Authors
Lei Yin Emily Ang
Horng Khit Issac Too
Eng Lee Tan
Tak-Kwong Vincent Chow
Pei-Chi Lynette Shek
Elizabeth Tham
Sylvie Alonso
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2016
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-016-0567-6

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