轮状病毒与肠道菌群的相互作用
Interaction between Rotavirus and Intestinal Flora
DOI: 10.12677/ACM.2023.133483, PDF,   
作者: 邝文涛:新疆医科大学研究生院,新疆 乌鲁木齐;杨学磊*:新疆维吾尔自治区人民医院医学研究与转化中心,新疆 乌鲁木齐
关键词: 轮状病毒肠道菌群相互作用轮状病毒疫苗Rotavirus Intestinal Flora Interaction Rotavirus Vaccine
摘要: 轮状病毒是引起全球学龄前儿童急性腹泻的主要病原体,过去的很多研究已经揭示了轮状病毒和肠道菌群之间存在一系列复杂的相互作用。轮状病毒感染会暂时改变肠道菌群的组成,同时益生菌给药也可以改善患者的胃肠道症状。目前轮状病毒疫苗是预防轮状病毒感染的最有效手段。有研究表明肠道菌群对疫苗使用也会产生一定的影响。现对轮状病毒与肠道菌群相互作用及肠道菌群对轮状病毒疫苗有效性影响作一综述。
Abstract: Rotavirus is the main pathogen of acute diarrhea in preschool children all over the world. many previous studies have revealed a series of complex interactions between rotavirus and intestinal flora. Rotavirus infection temporarily changes the composition of intestinal flora, and probiotic ad-ministration can also improve gastrointestinal symptoms. At present, rotavirus vaccine is the most effective means to prevent rotavirus infection. Some studies have shown that intestinal flora can al-so have a certain impact on the use of vaccine. This paper reviews the interaction between rotavirus and intestinal flora and the effect of intestinal flora on the effectiveness of rotavirus vaccine.
文章引用:邝文涛, 杨学磊. 轮状病毒与肠道菌群的相互作用[J]. 临床医学进展, 2023, 13(3): 3392-3401. https://doi.org/10.12677/ACM.2023.133483

参考文献

[1] Bishop, R.F., Davidson, G.P., Holmes, I.H. and Ruck, B.J. (1973) Virus Particles in Epithelial Cells of Duodenal Mu-cosa from Children with Acute Non-Bacterial Gastroenteritis. The Lancet, 2, 1281-1283. [Google Scholar] [CrossRef
[2] Saavedra, J.M., Bauman, N.A., Oung, I., et al. (1994) Feed-ing of Bifidobacterium bifidum and Streptococcus thermophilus to Infants in Hospital for Prevention of Diarrhoea and Shedding of Rotavirus. The Lancet, 344, 1046-1049. [Google Scholar] [CrossRef
[3] Fang, S.-B., Lee, H.-C., Hu, J.-J., et al. (2009) Dose-Dependent Effect of Lactobacillus rhamnosus on Quantitative Reduction of Faecal Rotavirus Shedding in Children. Journal of Tropical Pediatrics, 55, 297-301. [Google Scholar] [CrossRef] [PubMed]
[4] Teran, C.G., Teran-Escalera, C.N. and Villarroel, P. (2009) Nitazoxa-nide vs. Probiotics for the Treatment of Acute Rotavirus Diarrhea in Children: A Randomized, Single-Blind, Controlled Trial in Bolivian Children. International Journal of Infectious Diseases, 13, 518-523. [Google Scholar] [CrossRef] [PubMed]
[5] Huang, Y.-F., Liu, P.-Y., Chen, Y.-Y., et al. (2014) Three-Combination Probiotics Therapy in Children with Salmonella and Rotavirus Gastroenteritis. Journal of Clinical Gastroenterology, 48, 37-42. [Google Scholar] [CrossRef
[6] Zhang, W., Azevedo, M.S.P., Gonzalez, A.M., et al. (2008) Influence of Probiotic Lactobacilli Colonization on Neonatal B Cell Responses in a Gnotobiotic Pig Model of Human Rotavirus Infection and Disease. Veterinary Immunology and Immunopathology, 122, 175-181. [Google Scholar] [CrossRef] [PubMed]
[7] Kandasamy, S., Vlasova, A.N., Fischer, D., et al. (2016) Dif-ferential Effects of Escherichia coli Nissle and Lactobacillus rhamnosus Strain GG on Human Rotavirus Binding, Infec-tion, and B Cell Immunity. The Journal of Immunology, 196, 1780-1789. [Google Scholar] [CrossRef] [PubMed]
[8] Paim, F.C., Langel, S.N., Fischer, D.D., et al. (2016) Escherichia coli Effects of Nissle 1917 and Ciprofloxacin on Small Intestinal Epithelial Cell mRNA Expression in the Neonatal Piglet Model of Human Rotavirus Infection. Gut Pathogens, 8, 66. [Google Scholar] [CrossRef] [PubMed]
[9] Harris, V.C. (2018) The Significance of the Intestinal Microbiome for Vaccinology: From Correlations to Therapeutic Applications. Drugs, 78, 1063-1072. [Google Scholar] [CrossRef] [PubMed]
[10] Magwira, C.A. and Taylor, M.B. (2018) Composition of Gut Mi-crobiota and Its Influence on the Immunogenicity of Oral Rotavirus Vaccines. Vaccine, 36, 3427-3433. [Google Scholar] [CrossRef] [PubMed]
[11] Crawford, S.E., Ramani, S., Tate, J.E., et al. (2017) Rotavirus Infection. Nature Reviews Disease Primers, 3, 17083. [Google Scholar] [CrossRef] [PubMed]
[12] Donelli, G. and Superti, F. (1994) The Rotavirus Genus. Comparative Immunology, Microbiology & Infectious Diseases, 17, 305-320. [Google Scholar] [CrossRef] [PubMed]
[13] Dennehy, P.H. (2015) Rotavirus Infection: A Disease of the Past? Infectious Disease Clinics of North America, 29, 617-635. [Google Scholar] [CrossRef] [PubMed]
[14] Troeger, C., Khalil, I.A., Rao, P.C., et al. (2018) Rotavirus Vaccina-tion and the Global Burden of Rotavirus Diarrhea among Children Younger than 5 Years. JAMA Pediatrics, 172, 958-965. [Google Scholar] [CrossRef] [PubMed]
[15] 骆洪梅, 冉陆, 孟玲, 连怡遥, 王丽萍. 2005-2018年中国5岁以下轮状病毒腹泻报告病例流行特征分析[J]. 中华预防医杂, 2020, 54(2): 181-186. [Google Scholar] [CrossRef] [PubMed]
[16] Zhang, J., Duan, Z.J., Payne, D.C., et al. (2015) Rotavirus-Specific and Overall Diarrhea Mortality in Chinese Children Younger than 5 Years: 2003 to 2012. The Pediat-ric Infectious Disease Journal, 34, e233-e237. [Google Scholar] [CrossRef
[17] Burnett, E., Parashar, U.D. and Tate, J.E. (2020) Global Im-pact of Rotavirus Vaccination on Diarrhea Hospitalizations and Deaths among Children < 5 Years Old: 2006-2019. The Journal of Infectious Diseases, 222, 1731-1739. [Google Scholar] [CrossRef] [PubMed]
[18] Velasquez, D.E., Parashar, U. and Jiang, B.M. (2018) Decreased Per-formance of Live Attenuated, Oral Rotavirus Vaccines in Low-Income Settings: Causes and Contributing Factors. Expert Review of Vaccines, 17, 145-161. [Google Scholar] [CrossRef] [PubMed]
[19] 刘娜. 轮状病毒胃肠炎的免疫预防[J]. 国际病毒学杂志, 2021, 28(2): 89-92. [Google Scholar] [CrossRef
[20] Mo, Z., Mo, Y., Li, M., et al. (2017) Efficacy and Safety of a Pentavalent Live Human-Bovine Reassortant Rotavirus Vaccine (RV5) in Healthy Chinese Infants: A Ran-domized, Double-Blind, Placebo-Controlled Trial. Vaccine, 35, 5897-5904. [Google Scholar] [CrossRef] [PubMed]
[21] Guo, X.H., Okpara, E.S., Hu, W.T., et al. (2022) Interactive Relationships between Intestinal Flora and Bile Acids. International Journal of Molecular Sciences, 23, 8343. [Google Scholar] [CrossRef] [PubMed]
[22] Qin, J.J., Li, R.Q., Raes, J., et al. (2010) A Human Gut Microbial Gene Catalogue Established by Metagenomic Sequencing. Nature, 464, 59-65. [Google Scholar] [CrossRef] [PubMed]
[23] Bidell, M.R., Hobbs, A.L.V. and Lodise, T.P. (2022) Gut Microbiome Health and Dysbiosis: A Clinical Primer. Pharmacotherapy, 42, 849-857. [Google Scholar] [CrossRef] [PubMed]
[24] Lee, Y.K. and Mazmanian, S.K. (2010) Has the Microbiota Played a Critical Role in the Evolution of the Adaptive Immune System? Science, 330, 1768-1773. [Google Scholar] [CrossRef] [PubMed]
[25] Karst, S.M. (2016) The Influence of Commensal Bacteria on Infection with Enteric Viruses. Nature Reviews Microbiology, 14, 197-204. [Google Scholar] [CrossRef] [PubMed]
[26] Milani, C., Duranti, S., Bottacini, F., et al. (2017) The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota. Microbiol-ogy and Molecular Biology Reviews, 81, e00036-17. [Google Scholar] [CrossRef
[27] Caricilli, A.M., Castoldi, A. and Câmara, N.O.S. (2014) Intestinal Barrier: A Gentlemen’s Agreement between Microbiota and Immunity. World Journal of Gastrointestinal Pathophysiology, 5, 18-32. [Google Scholar] [CrossRef] [PubMed]
[28] Ma, C.F., Wu, X.K., Nawaz, M., et al. (2011) Molecular Characteriza-tion of Fecal Microbiota in Patients with Viral Diarrhea. Current Microbiology, 63, 259-266. [Google Scholar] [CrossRef] [PubMed]
[29] Chen, S.-Y., Tsai, C.-N., Lee, Y.-S., et al. (2017) Intestinal Mi-crobiome in Children with Severe and Complicated Acute Viral Gastroenteritis. Scientific Reports, 7, Article No. 46130. [Google Scholar] [CrossRef] [PubMed]
[30] Lee, H. and Ko, G.P. (2016) Antiviral Effect of Vitamin A on Norovirus Infection via Modulation of the Gut Microbiome. Scientific Reports, 6, Article No. 25835. [Google Scholar] [CrossRef] [PubMed]
[31] Kanmani, P., Albarracin, L., Kobayashi, H., et al. (2018) Exopolysaccha-rides from Lactobacillus delbrueckii OLL1073R-1 Modulate Innate Antiviral Immune Response in Porcine Intestinal Ep-ithelial Cells. Molecular Immunology, 93, 253-265. [Google Scholar] [CrossRef] [PubMed]
[32] Nealon, N.J., Yuan, L.J., Yang, X.D., et al. (2017) Rice Bran and Probiotics Alter the Porcine Large Intestine and Serum Metab-olomes for Protection against Human Rotavirus Diarrhea. Frontiers in Microbiology, 8, 653. [Google Scholar] [CrossRef] [PubMed]
[33] Peña-Gil, N., Santiso-Bellón, C., Gozalbo-Rovira, R., et al. (2021) The Role of Host Glycobiology and Gut Microbiota in Rotavirus and Norovirus Infection, an Update. International Journal of Molecular Sciences, 22, 13473. [Google Scholar] [CrossRef] [PubMed]
[34] Kuss, S.K., Best, G.T., Etheredge, C.A., et al. (2011) Intestinal Micro-biota Promote Enteric Virus Replication and Systemic Pathogenesis. Science, 334, 249-252. [Google Scholar] [CrossRef] [PubMed]
[35] Robinson, C.M., Jesudhasan, P.R. and Pfeiffer, J.K. (2014) Bacterial Lipopolysaccharide Binding Enhances Virion Stability and Promotes Environmental Fitness of an Enteric Virus. Cell Host & Microbe, 15, 36-46. [Google Scholar] [CrossRef] [PubMed]
[36] Berger, A.K., Yi, H., Kearns, D.B., et al. (2017) Bacteria and Bacterial Envelope Components Enhance Mammalian Reovirus Thermostability. PLOS Pathogens, 13, e1006768. [Google Scholar] [CrossRef] [PubMed]
[37] Shi, Z.D., Zou, J., Zhang, Z., et al. (2019) Segmented Filamen-tous Bacteria Prevent and Cure Rotavirus Infection. Cell, 179, 644-658.e13. [Google Scholar] [CrossRef] [PubMed]
[38] Grandy, G., Medina, M., Soria, R., et al. (2010) Probiotics in the Treatment of Acute Rotavirus Diarrhoea. A Randomized, Double-Blind, Controlled Trial Using Two Different Probiotic Preparations in Bolivian Children. BMC Infectious Diseases, 10, 253. [Google Scholar] [CrossRef] [PubMed]
[39] Lee, D.K., Park, J.E., Kim, M.J., et al. (2015) Probiotic Bacteria, B. longum and L. acidophilus Inhibit Infection by Rotavirus in Vitro and Decrease the Duration of Diarrhea in Pediatric Pa-tients. Clinics and Research in Hepatology and Gastroenterology, 39, 237-244. [Google Scholar] [CrossRef] [PubMed]
[40] Park, M.S., Kwon, B., Ku, S., et al. (2017) The Efficacy of Bifidobacterium longum BORI and Lactobacillus acidophilus AD031 Probiotic Treatment in Infants with Rotavirus In-fection. Nutrients, 9, 887. [Google Scholar] [CrossRef] [PubMed]
[41] Sindhu, K.N.C., Sowmyanarayanan, T.V., Paul, A., et al. (2014) Immune Response and Intestinal Permeability in Children with Acute Gastroenteritis Treated with Lactobacillus rhamnosus GG: A Randomized, Double-Blind, Placebo-Controlled Trial. Clinical Infectious Diseases, 58, 1107-1115. [Google Scholar] [CrossRef] [PubMed]
[42] Schnadower, D., Tarr, P.I., et al. (2018) Lactobacillus rhamnosus GG versus Placebo for Acute Gastroenteritis in Children. The New England Journal of Medicine, 379, 2002-2014. [Google Scholar] [CrossRef
[43] Meurens, F., Summerfield, A., Nauwynck, H., et al. (2012) The Pig: A Model for Human Infectious Diseases. Trends in Microbiology, 20, 50-57. [Google Scholar] [CrossRef] [PubMed]
[44] Twitchell, E.L., Tin, C., Wen, K., et al. (2016) Modeling Human Enteric Dysbiosis and Rotavirus Immunity in Gnotobiotic Pigs. Gut Pathogens, 8, 51. [Google Scholar] [CrossRef] [PubMed]
[45] Vlasova, A.N., Chattha, K.S., Kandasamy, S., et al. (2013) Lac-tobacilli and Bifidobacteria Promote Immune Homeostasis by Modulating Innate Immune Responses to Human Rotavirus in Neonatal Gnotobiotic Pigs. PLOS ONE, 8, e76962. [Google Scholar] [CrossRef] [PubMed]
[46] Liu, F., Li, G., Wen, K., et al. (2013) Lactobacillus rhamnosus GG on Rotavirus-Induced Injury of Ileal Epithelium in Gnotobiotic Pigs. Journal of Pediatric Gastroenterology and Nutrition, 57, 750-758. [Google Scholar] [CrossRef
[47] Preidis, G.A., Saulnier, D.M., Blutt, S.E., et al. (2012) Host Response to Probiotics Determined by Nutritional Status of Rotavirus-Infected Neonatal Mice. Journal of Pediatric Gas-troenterology and Nutrition, 55, 299-307. [Google Scholar] [CrossRef
[48] Ventola, H., Lehtoranta, L., Madetoja, M., et al. (2012) Ef-fects of the Viability of Lactobacillus rhamnosus GG on Rotavirus Infection in Neonatal Rats. World Journal of Gas-troenterology, 18, 5925-5931. [Google Scholar] [CrossRef] [PubMed]
[49] Macpherson, A.J., Geuking, M.B. and McCoy, K.D. (2012) Home-land Security: IgA Immunity at the Frontiers of the Body. Trends in Immunology, 33, 160-167. [Google Scholar] [CrossRef] [PubMed]
[50] Sutherland, D.B., Suzuki, K. and Fagarasan, S. (2016) Fostering of Advanced Mutualism with Gut Microbiota by Immunoglobulin A. Immunological Reviews, 270, 20-31. [Google Scholar] [CrossRef] [PubMed]
[51] Blutt, S.E., Miller, A.D., Salmon, S.L., et al. (2012) IgA Is Important for Clearance and Critical for Protection from Rotavirus Infection. Mucosal Immunology, 5, 712-719. [Google Scholar] [CrossRef] [PubMed]
[52] Qiao, H.P., Duffy, L.C., Griffiths, E., et al. (2002) Immune Responses in Rhesus Rotavirus-Challenged BALB/c Mice Treated with Bifidobacteria and Prebiotic Supplements. Pediatric Research, 51, 750-755. [Google Scholar] [CrossRef] [PubMed]
[53] Yang, C., Mogno, I., Contijoch, E.J., et al. (2020) Fecal IgA Levels Are Determined by Strain-Level Differences in Bacteroides ovatus and Are Modifiable by Gut Microbiota Manipulation. Cell Host & Microbe, 27, 467-475.e6. [Google Scholar] [CrossRef] [PubMed]
[54] Gandhi, G.R., Santos, V.S., Denadai, M., et al. (2017) Cytokines in the Management of Rotavirus Infection: A Systematic Review of in Vivo Studies. Cytokine, 96, 152-160. [Google Scholar] [CrossRef] [PubMed]
[55] Rigo-Adrover, M., Saldaña-Ruíz, S., van Limpt, K., et al. (2017) A Combination of scGOS/lcFOS with Bifidobacterium breve M-16V Protects Suckling Rats from Rotavirus Gastroenteritis. European Journal of Nutrition, 56, 1657-1670. [Google Scholar] [CrossRef] [PubMed]
[56] Rigo-Adrover, M.D.M., van Limpt, K., Knipping, K., et al. (2018) Bifidobacterium breve Preventive Effect of a Synbiotic Combination of Galacto- and Fructooligosaccharides Mixture with M-16V in a Model of Multiple Rotavirus Infections. Frontiers in Immunology, 9, 1318. [Google Scholar] [CrossRef] [PubMed]
[57] Sommer, F. and Bäckhed, F. (2013) The Gut Microbiota—Masters of Host Development and Physiology. Nature Reviews Microbiology, 11, 227-238. [Google Scholar] [CrossRef] [PubMed]
[58] Rigo-Adrover, M.D.M., Franch, À., Castell, M., et al. (2016) Preclinical Immunomodulation by the Probiotic Bifidobacterium breve M-16V in Early Life. PLOS ONE, 11, e0166082. [Google Scholar] [CrossRef] [PubMed]
[59] Wang, Y.L., Yin, Y.S., Chen, X., et al. (2019) Induction of In-testinal Th17 Cells by Flagellins from Segmented Filamentous Bacteria. Frontiers in Immunology, 10, 2750. [Google Scholar] [CrossRef] [PubMed]
[60] Schnupf, P., Gaboriau-Routhiau, V., Sansonetti, P.J., et al. (2017) Segmented Filamentous Bacteria, Th17 Inducers and Helpers in a Hostile World. Current Opinion in Microbiology, 35, 100-109. [Google Scholar] [CrossRef] [PubMed]
[61] Denning, T.L. and Sitaraman, S.V. (2010) Segmented Filamentous Bacteria Shape Intestinal Immunity. Gastroenterology, 139, 351-353. [Google Scholar] [CrossRef] [PubMed]
[62] Zhang, B.Y., Chassaing, B., Shi, Z.D., et al. (2014) Viral Infec-tion. Prevention and Cure of Rotavirus Infection via TLR5/NLRC4-Mediated Production of IL-22 and IL-18. Science, 346, 861-865. [Google Scholar] [CrossRef] [PubMed]
[63] Hernández, P.P., Mahlakoiv, T., Yang, I., et al. (2015) Interferon-λ and Interleukin 22 Act Synergistically for the Induction of Interferon-Stimulated Genes and Control of Rotavirus Infec-tion. Nature Immunology, 16, 698-707. [Google Scholar] [CrossRef] [PubMed]
[64] Uchiyama, R., Chassaing, B., Zhang, B.Y., et al. (2014) Antibiotic Treatment Suppresses Rotavirus Infection and Enhances Specific Humoral Immunity. The Journal of Infectious Diseases, 210, 171-182. [Google Scholar] [CrossRef] [PubMed]
[65] Engevik, M.A., Banks, L.D., Engevik, K.A., et al. (2020) Rotavirus In-fection Induces Glycan Availability to Promote Ileum-Specific Changes in the Microbiome Aiding Rotavirus Virulence. Gut Microbes, 11, 1324-1347. [Google Scholar] [CrossRef] [PubMed]
[66] Ferreira, R.B.R., Antunes, L., Caetano, M. and Finlay, B.B. (2010) Should the Human Microbiome Be Considered When Developing Vaccines? PLOS Pathogens, 6, e1001190. [Google Scholar] [CrossRef] [PubMed]
[67] Huda, M.N., Lewis, Z., Kalanetra, K.M., et al. (2014) Stool Mi-crobiota and Vaccine Responses of Infants. Pediatrics, 134, e362-e372. [Google Scholar] [CrossRef] [PubMed]
[68] Harris, V., Ali, A., Fuentes, S., et al. (2018) Rotavirus Vaccine Re-sponse Correlates with the Infant Gut Microbiota Composition in Pakistan. Gut Microbes, 9, 93-101. [Google Scholar] [CrossRef] [PubMed]
[69] Harris, V.C., Armah, G., Fuentes, S., et al. (2017) Signifi-cant Correlation between the Infant Gut Microbiome and Rotavirus Vaccine Response in Rural Ghana. The Journal of Infectious Diseases, 215, 34-41. [Google Scholar] [CrossRef] [PubMed]
[70] Fix, J., Chandrashekhar, K., Perez, J., et al. (2020) Association between Gut Microbiome Composition and Rotavirus Vaccine Response among Nicaraguan Infants. American Journal of Tropi-cal Medicine and Hygiene, 102, 213-219. [Google Scholar] [CrossRef] [PubMed]
[71] Parker, E.P.K., Praharaj, I., Zekavati, A., et al. (2018) Influence of the Intestinal Microbiota on the Immunogenicity of Oral Rotavirus Vaccine Given to Infants in South India. Vaccine, 36, 264-272. [Google Scholar] [CrossRef] [PubMed]
[72] Michael, H., Langel, S.N., Miyazaki, A., et al. (2020) Malnutri-tion Decreases Antibody Secreting Cell Numbers Induced by an Oral Attenuated Human Rotavirus Vaccine in a Human Infant Fecal Microbiota Transplanted Gnotobiotic Pig Model. Frontiers in Immunology, 11, 196. [Google Scholar] [CrossRef] [PubMed]
[73] Lazarus, R.P., John, J., Shanmugasundaram, E., et al. (2018) The Effect of Probiotics and Zinc Supplementation on the Immune Response to Oral Rotavirus Vaccine: A Randomized, Fac-torial Design, Placebo-Controlled Study among Indian Infants. Vaccine, 36, 273-279. [Google Scholar] [CrossRef] [PubMed]