Viral Infections, the Microbiome, and Probiotics

Ashton Harper, Vineetha Vijayakumar, Arthur C Ouwehand, Jessica Ter Haar, David Obis, Jordi Espadaler, Sylvie Binda, Shrilakshmi Desiraju, Richard Day, Ashton Harper, Vineetha Vijayakumar, Arthur C Ouwehand, Jessica Ter Haar, David Obis, Jordi Espadaler, Sylvie Binda, Shrilakshmi Desiraju, Richard Day

Abstract

Viral infections continue to cause considerable morbidity and mortality around the world. Recent rises in these infections are likely due to complex and multifactorial external drivers, including climate change, the increased mobility of people and goods and rapid demographic change to name but a few. In parallel with these external factors, we are gaining a better understanding of the internal factors associated with viral immunity. Increasingly the gastrointestinal (GI) microbiome has been shown to be a significant player in the host immune system, acting as a key regulator of immunity and host defense mechanisms. An increasing body of evidence indicates that disruption of the homeostasis between the GI microbiome and the host immune system can adversely impact viral immunity. This review aims to shed light on our understanding of how host-microbiota interactions shape the immune system, including early life factors, antibiotic exposure, immunosenescence, diet and inflammatory diseases. We also discuss the evidence base for how host commensal organisms and microbiome therapeutics can impact the prevention and/or treatment of viral infections, such as viral gastroenteritis, viral hepatitis, human immunodeficiency virus (HIV), human papilloma virus (HPV), viral upper respiratory tract infections (URTI), influenza and SARS CoV-2. The interplay between the gastrointestinal microbiome, invasive viruses and host physiology is complex and yet to be fully characterized, but increasingly the evidence shows that the microbiome can have an impact on viral disease outcomes. While the current evidence base is informative, further well designed human clinical trials will be needed to fully understand the array of immunological mechanisms underlying this intricate relationship.

Keywords: dysbiosis; immunity; microbiome; probiotics; viral infection.

Conflict of interest statement

AH was previously employed by ADM Protexin Ltd., VV and RD are currently employed by ADM Protexin Ltd. AO is employed by DuPont Nutrition and Biosciences. DO is employed by Danone NutriciaResearch. JE is employed by AB-BIOTICS S.A. SB is employed by Lallemand Health Solutions, and SD is employed by Triphase Pharmaceuticals, Pvt Ltd. The remaining author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Harper, Vijayakumar, Ouwehand, ter Haar, Obis, Espadaler, Binda, Desiraju and Day.

Figures

Figure 1
Figure 1
Antiviral microbiome mechanisms: 1. Enhanced mucosal barrier function: wet epithelial surfaces (e.g., GI tract, vagina, lung) are covered in a mucous layer containing glycoproteins - called mucins – which provide a physical barrier between invasive pathogenic microorganisms and host epithelial cells. Mucin production is influenced by the composition of the GI microbiome and they appear to have antiviral properties (Lieleg et al., 2012; Schroeder, 2019). Numerous lactic acid bacteria have been shown to regulate tight junctions and thus maintain normal mucosal permeability, 2. Antimicrobial compounds (bacteriocins) produced (e.g., subtilosin) by some bacteria (e.g., Bacillus spp.) are virucidal (Torres et al., 2013; Quintana et al., 2014). 3. Inhibit viral attachment to host epithelial cells by various means (Botić et al., 2007; Su et al., 2013). 4. Modulation of the immune system: probiotics stimulate plasmacytoid dendritic cells to produce interferon-alpha (IFN-a) thus inducing the cytotoxic activity of natural killer (NK) cells (innate immune system), which play a critical role in viral infection (Jounai et al., 2012). Probiotic bacterial strains have also been shown to enhance the production of antiviral immunoglobulins (produced by B lymphocytes – adaptive immune system) by an unknown mechanism; possibly through stimulation of intestinal epithelial cells or immunocytes (De Vrese et al., 2005).
Figure 2
Figure 2
The gut-lung axis crosstalk in the context of viral respiratory infections: A healthy gut microbiome offers protection against respiratory infection by maintaining the normal immune response. This may be achieved through inter-organ signaling by numerous bacterially derived immunomodulating compounds [e.g., lipopolysaccharides (LPS), peptidoglycan, and short-chain fatty acids (SCFAs)]. Gastrointestinal (GI) dysbiosis caused by infection or antibiotic exposure, for example, may alter these microbiome generated signals (e.g., via the blood) and potentially impair antiviral immune responses in the lung. Introduction of beneficial bacteria (i.e., probiotics) may help to bolster or recover effective immune function in the GI tract and also indirectly in the lung.

References

    1. Abraham B. P., Quigley E. M. M. (2017). Probiotics in Inflammatory Bowel Disease. Gastroenterol. Clin. North Am. 46, 769–782. 10.1016/j.gtc.2017.08.003
    1. Abt M. C., Osborne L. C., Monticelli L. A., Doering T. A., Alenghat T., Sonnenberg G. F., et al. . (2012). Commensal Bacteria Calibrate the Activation Threshold of Innate Antiviral Immunity. Immunity 37, 158–170. 10.1016/j.immuni.2012.04.011
    1. Adiliaghdam F., Jeffrey K. L. (2020). Illuminating the human virome in health and disease. Genome Med. 12, 66. 10.1186/s13073-020-00766-x
    1. Adler C. J., Dobney K., Weyrich L. S., Kaidonis J., Walker A. W., Haak W., et al. . (2013). Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat. Genet. 45, 450–455. 10.1038/ng.2536
    1. Agrawal A., Sharma B. C., Sharma P., Sarin S. K. (2012). Secondary prophylaxis of hepatic encephalopathy in cirrhosis: An open-label, randomized controlled trial of lactulose, probiotics, and no therapy. Am. J. Gastroenterol. 107, 1043–1050. 10.1038/ajg.2012.113
    1. Aguilar-Toalá J. E., Garcia-Varela R., Garcia H. S., Mata-Haro V., González-Córdova A. F., Vallejo-Cordoba B., et al. . (2018). Postbiotics: An evolving term within the functional foods field. Trends Food Sci. Technol. 75, 105–114. 10.1016/j.tifs.2018.03.009
    1. Agus A., Planchais J., Sokol H. (2018). Gut Microbiota Regulation of Tryptophan Metabolism in Health and Disease. Cell Host Microbe 23, 716–724. 10.1016/j.chom.2018.05.003
    1. Aiello A., Farzaneh F., Candore G., Caruso C., Davinelli S., Gambino C. M., et al. . (2019). Immunosenescence and its hallmarks: How to oppose aging strategically? A review of potential options for therapeutic intervention. Front. Immunol. 10, 1–19. 10.3389/fimmu.2019.02247
    1. Al Kassaa I., Hober D., Hamze M., Chihib N. E., Drider D. (2014). Antiviral Potential of Lactic Acid Bacteria and Their Bacteriocins. Probiotics Antimicrob. Proteins 6, 177–185. 10.1007/s12602-014-9162-6
    1. Al-Asmakh M., Hedin L. (2015). Microbiota and the control of blood-tissue barriers. Tissue Barriers 3, 1–7. 10.1080/21688370.2015.1039691
    1. Allen S. J., Martinez E. G., Gregorio G. V., Dans L. F. (2010). Probiotics for treating acute infectious diarrhoea. Cochrane Database Syst. Rev. 2010 (11), CD003048. 10.1002/14651858.CD003048.pub3
    1. Altman M. C., Beigelman A., Ciaccio C., Gern J. E., Heymann P. W., Jackson D. J., et al. . (2020). Evolving concepts in how viruses impact asthma: A Work Group Report of the Microbes in Allergy Committee of the American Academy of Allergy, Asthma & Immunology. J. Allergy Clin. Immunol. 145, 1332–1344. 10.1016/j.jaci.2019.12.904
    1. Anthony S. (2013). A Strategy To Estimate Unknown Viral Diversity in Mammals. MBio 4, 1–15. 10.1128/mBio.00598-13
    1. Aqaeinezhad Rudbane S. M., Rahmdel S., Abdollahzadeh S. M., Zare M., Bazrafshan A., Mazloomi S. M. (2018). The efficacy of probiotic supplementation in rheumatoid arthritis: a meta-analysis of randomized, controlled trials. Inflammopharmacology 26, 67–76. 10.1007/s10787-017-0436-y
    1. Ardeshir A., Narayan N. R., Méndez-Lagares G., Lu D., Rauch M., Huang Y., et al. . (2014). Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems. Sci. Transl. Med. 6 (252), 252ra120. 10.1126/scitranslmed.3008791
    1. Arleevskaya M. I., Shafigullina A. Z., Filina Y. V., Lemerle J., Renaudineau Y. (2017). Associations between viral infection history symptoms, granulocyte reactive oxygen species activity, and active rheumatoid arthritis disease in untreated women at Onset: Results from a longitudinal cohort study of tatarstan women. Front. Immunol. 8, 1725. 10.3389/fimmu.2017.01725
    1. Atashili J., Poole C., Ndumbe P. M., Adimora A. A., Smith J. S. (2008). Bacterial vaginosis and HIV acquisition: A meta-analysis of published studies. AIDS 22, 1493–1501. 10.1097/QAD.0b013e3283021a37
    1. Baud D., Dimopoulou Agri V., Gibson G. R., Reid G., Giannoni E. (2020). Using Probiotics to Flatten the Curve of Coronavirus Disease COVID-2019 Pandemic. Front. Public Heal. 8, 1–5. 10.3389/fpubh.2020.00186
    1. Belkacem N., Serafini N., Wheeler R., Derrien M., Boucinha L., Couesnon A., et al. . (2017). Lactobacillus paracasei feeding improves immune control of influenza infection in mice. PLoS One 12, e0184976. 10.1371/journal.pone.0184976
    1. Belkacem N., Bourdet-Sicard R., Taha M. K. (2018). Lactobacillus paracasei feeding improves the control of secondary experimental meningococcal infection in flu-infected mice. BMC Infect. Dis. 18, 1–9. 10.1186/s12879-018-3086-9
    1. Belkaid Y., Hand T. W. (2014). Role of the microbiota in immunity and inflammation. Cell 157, 121–141. 10.1016/j.cell.2014.03.011
    1. Biliavska L., Pankivska Y., Povnitsa O., Zagorodnya S. (2019). Antiviral activity of exopolysaccharides produced by lactic acid bacteria of the genera Pediococcus, Leuconostoc and Lactobacillus against human adenovirus type 5. Medicina 55 (9), 519. 10.3390/medicina55090519
    1. Bolton M., van der Straten A., Cohen C. R. (2008). Probiotics: potential to prevent HIV and sexually transmitted infections in women. Sex Transm. Dis. 35, 214–225. 10.1097/OLQ.0b013e31815b017a
    1. Borgdorff H., Tsivtsivadze E., Verhelst R., Marzorati M., Jurriaans S., Ndayisaba G. F., et al. . (2014). Lactobacillus-dominated cervicovaginal microbiota associated with reduced HIV/STI prevalence and genital HIV viral load in african women. ISME J. 8, 1781–1793. 10.1038/ismej.2014.26
    1. Borgdorff H., Gautam R., Armstrong S. D., Xia D., Ndayisaba G. F., Van Teijlingen N. H., et al. . (2016). Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier. Mucosal Immunol. 9, 621–633. 10.1038/mi.2015.86
    1. Bosch A. A. T. M., Biesbroek G., Trzcinski K., Sanders E. A. M., Bogaert D. (2013). Viral and Bacterial Interactions in the Upper Respiratory Tract. PLoS Pathog. 9 (1), e1003057. 10.1371/journal.ppat.1003057
    1. Botić T., Klingberg T. D́., Weingartl H., Cencič A. (2007). A novel eukaryotic cell culture model to study antiviral activity of potential probiotic bacteria. Int. J. Food Microbiol. 115, 227–234. 10.1016/j.ijfoodmicro.2006.10.044
    1. Bouvier N. M., Palese P. (2008). The biology of influenza viruses. Vaccine 26, 49–53. 10.1016/j.vaccine.2008.07.039
    1. Bradley K. C., Finsterbusch K., Schnepf D., Crotta S., Llorian M., Davidson S., et al. . (2019). Microbiota-Driven Tonic Interferon Signals in Lung Stromal Cells Protect from Influenza Virus Infection. Cell Rep. 28 (1), 245–256.e4. 10.1016/j.celrep.2019.05.105
    1. Bradshaw C. S., Brotman R. M. (2015). Making inroads into improving treatment of bacterial vaginosis - striving for long-term cure. BMC Infect. Dis. 15, 1–12. 10.1186/s12879-015-1027-4
    1. Breshears L. M., Edwards V. L., Ravel J., Peterson M. L. (2015). Lactobacillus crispatus inhibits growth of Gardnerella vaginalis and Neisseria gonorrhoeae on a porcine vaginal mucosa model. BMC Microbiol. 15, 1–12. 10.1186/s12866-015-0608-0
    1. Bron P. A., Kleerebezem M., Brummer R. J., Cani P. D., Mercenier A., MacDonald T. T., et al. . (2017). Can probiotics modulate human disease by impacting intestinal barrier function? Br. J. Nutr. 117, 93–107. 10.1017/S0007114516004037
    1. Brotman R. M., Shardell M. D., Gajer P., Tracy J. K., Zenilman J. M., Ravel J., et al. . (2014). Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J. Infect. Dis. 210, 1723–1733. 10.1093/infdis/jiu330
    1. Byrd A. L., Belkaid Y., Segre J. A. (2018). The human skin microbiome. Nat. Rev. Microbiol. 16, 143–155. 10.1038/nrmicro.2017.157
    1. Chang A. H., Parsonnet J. (2010). Role of bacteria in oncogenesis. Clin. Microbiol. Rev. 23, 837–857. 10.1128/CMR.00012-10
    1. Chen C. J., Wu G. H., Kuo R. L., Shih S. R. (2017). Role of the intestinal microbiota in the immunomodulation of influenza virus infection. Microbes Infect. 19 (12), 570–579. 10.1016/j.micinf.2017.09.002
    1. Cheriyan V. T., Krishna S. M., Kumar A., Jayaprakash P. G., Balaram P. (2009). Signaling defects and functional impairment in T-cells from cervical cancer patients. Cancer Biother. Radiopharm. 24, 667–673. 10.1089/cbr.2009.0660
    1. Cherry D. K., Burt C. W., Woodwell D. A. (2003). National Ambulatory Medical Care Survey: 2001 summary. Adv. Data 337, 1–44.
    1. Chiba Y., Shida K., Nagata S., Wada M., Bian L., Wang C., et al. . (2010). Well-controlled proinflammatory cytokine responses of Peyer’s patch cells to probiotic Lactobacillus casei. Immunology 130, 352–362. 10.1111/j.1365-2567.2009.03204.x
    1. Council of the European Union (2009). Council Recommendation of 22 December 2009 on seasonal influenza vaccination. Off. J. Eur. Union L348, 0071–0072.
    1. Ctoi A. F., Corina A., Katsiki N., Vodnar D. C., Andreicuţ A. D., Stoian A. P., et al. . (2020). Gut microbiota and aging-A focus on centenarians. Biochim. Biophys. Acta - Mol. Basis Dis. 1866 (7), 165765. 10.1016/j.bbadis.2020.165765
    1. David L. A., Maurice C. F., Carmody R. N., Gootenberg D. B., Button J. E., Wolfe B. E., et al. . (2014). Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563. 10.1038/nature12820
    1. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J. B., Massart S., et al. . (2010). Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl. Acad. Sci. 107, 14691–14696. 10.1073/pnas.1005963107
    1. De Seta F., Campisciano G., Zanotta N., Ricci G., Comar M. (2019). The vaginal community state types microbiome-immune network as key factor for bacterial vaginosis and aerobic vaginitis. Front. Microbiol. 10, 2451.
    1. De Vrese M., Rautenberg P., Laue C., Koopmans M., Herremans T., Schrezenmeir J. (2005). Probiotic bacteria stimulate virus-specific neutralizing antibodies following a booster polio vaccination. Eur. J. Nutr. 44, 406–413. 10.1007/s00394-004-0541-8
    1. Demehri F. R., Barrett M., Teitelbaum D. H. (2015). Changes to the intestinal microbiome with parenteral nutrition: Review of a murine model and potential clinical implications. Nutr. Clin. Pract. 30, 798–806. 10.1177/0884533615609904
    1. Demirci M., Tokman H. B., Uysal H. K., Demiryas S., Karakullukcu A., Saribas S., et al. . (2019). Reduced Akkermansia muciniphila and Faecalibacterium prausnitzii levels in the gut microbiota of children with allergic asthma. Allergol. Immunopathol. (Madr) 47, 365–371. 10.1016/j.aller.2018.12.009
    1. Dethlefsen L., Relman D. A. (2011). Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl. Acad. Sci. U. S. A. 108 Suppl, 4554–4561. 10.1073/pnas.1000087107
    1. Dickson R. P., Huffnagle G. B. (2015). The Lung Microbiome: New Principles for Respiratory Bacteriology in Health and Disease. PLoS Pathog. 11, 1–5. 10.1371/journal.ppat.1004923
    1. Dickson R. P. (2017). The microbiome and critical illness. Lancet Respir. Med. 4, 59–72. 10.1016/S2213-2600(15)00427-0
    1. Dobson A., Cotter P. D., Paul Ross R., Hill C. (2012). Bacteriocin production: A probiotic trait? Appl. Environ. Microbiol. 78, 1–6. 10.1128/AEM.05576-11
    1. Doms R. W. (2016). “A Step-by-Step Guide to Viral Infection,” in Viral Pathogenesis, 29–40. 10.1016/B978-0-12-800964-2.00003-3
    1. Dumas A., Bernard L., Poquet Y., Lugo-Villarino G., Neyrolles O. (2018). The role of the lung microbiota and the gut–lung axis in respiratory infectious diseases. Cell. Microbiol 20 (12), e12966. 10.1111/cmi.12966
    1. Enaud R., Prevel R., Ciarlo E., Beaufils F., Wieërs G., Guery B., et al. . (2020). The Gut-Lung Axis in Health and Respiratory Diseases: A Place for Inter-Organ and Inter-Kingdom Crosstalks. Front. Cell. Infect. Microbiol. 10, 1–11. 10.3389/fcimb.2020.00009
    1. Favalli E. G., Ingegnoli F., De Lucia O., Cincinelli G., Cimaz R., Caporali R. (2020). COVID-19 infection and rheumatoid arthritis: Faraway, so close! Autoimmun. Rev. 19, 102523. 10.1016/j.autrev.2020.102523
    1. Fendrick A. M., Saint S., Brook I., Jacobs M. R., Pelton S., Sethi S. (2001). Diagnosis and treatment of upper respiratory tract infections in the primary care setting. Clin. Ther 23 (10), 1683–1706. 10.1016/S0149-2918(01)80137-5
    1. Finer N., Garnett S. P., Bruun J. M. (2020). COVID-19 and obesity. Clin. Obes. 10, 1–2. 10.1111/cob.12365
    1. Forsythe P. (2014). Probiotics and lung immune responses. Ann. Am. Thorac. Soc. 11, 33–37. 10.1513/AnnalsATS.201306-156MG
    1. Franzosa E. A., Sirota-Madi A., Avila-Pacheco J., Fornelos N., Haiser H. J., Reinker S., et al. . (2019). Gut microbiome structure and metabolic activity in inflammatory bowel disease. Nat. Microbiol. 4, 293–305. 10.1038/s41564-018-0306-4
    1. Gao Q. Y., Chen Y. X., Fang J. Y. (2020). 2019 Novel coronavirus infection and gastrointestinal tract. J. Dig. Dis. 21, 125–126. 10.1111/1751-2980.12851
    1. Gillet E., Meys J. F. A., Verstraelen H., Bosire C., De Sutter P., Temmerman M., et al. . (2011). Bacterial vaginosis is associated with uterine cervical human papillomavirus infection: A meta-analysis. BMC Infect. Dis. 11, 10. 10.1186/1471-2334-11-10
    1. Goeijenbier M., van Sloten T. T., Slobbe L., Mathieu C., van Genderen P., Beyer W. E. P., et al. . (2017). Benefits of flu vaccination for persons with diabetes mellitus: A review. Vaccine 35, 5095–5101. 10.1016/j.vaccine.2017.07.095
    1. Gonzalez-Ochoa G., Flores-Mendoza L. K., Icedo-Garcia R., Gomez-Flores R., Tamez-Guerra P. (2017). Modulation of rotavirus severe gastroenteritis by the combination of probiotics and prebiotics. Arch. Microbiol. 10.1007/s00203-017-1400-3
    1. Gonzalez-Perez G., Hicks A. L., Tekieli T. M., Radens C. M., Williams B. L., Lamousé-Smith E. S. N. (2016). Maternal Antibiotic Treatment Impacts Development of the Neonatal Intestinal Microbiome and Antiviral Immunity. J. Immunol. 196, 3768–3779. 10.4049/jimmunol.1502322
    1. Gu S., Chen Y., Wu Z., Chen Y., Gao H., Lv L., et al. . (2020). Alterations of the Gut Microbiota in Patients with COVID-19 or H1N1 Influenza. Clin. Infect. Dis. ciaa709. 10.1093/cid/ciaa709
    1. Gui Q., Wang A., Zhao X., Huang S., Tan Z., Xiao C., et al. . (2020). Effects of probiotic supplementation on natural killer cell function in healthy elderly individuals: a meta-analysis of randomized controlled trials. Eur. J. Clin. Nutr. 74 (12), 1630–l1637. 10.1038/s41430-020-0670-z
    1. Guo Y. L., You K., Qiao J., Zhao Y. M., Geng L. (2012). Bacterial vaginosis is conducive to the persistence of HPV infection. Int. J. STD AIDS 23, 581–584. 10.1258/ijsa.2012.011342
    1. Hagan T., Cortese M., Rouphael N., Boudreau C., Linde C., Maddur M. S., et al. . (2019). Antibiotics-Driven Gut Microbiome Perturbation Alters Immunity to Vaccines in Humans. Cell 178, 1313–1328. 10.1016/j.cell.2019.08.010
    1. Halfvarson J., Brislawn C. J., Lamendella R., Vázquez-Baeza Y., Walters W. A., Bramer L. M., et al. . (2017). Dynamics of the human gut microbiome in inflammatory bowel disease. Nat. Microbiol. 2, 1–7. 10.1038/nmicrobiol.2017.4
    1. Hand T. W., Vujkovic-Cvijin I., Ridaura V. K., Belkaid Y. (2016). Linking the Microbiota, Chronic Disease, and the Immune System. Trends Endocrinol. Metab. 27, 831–843. 10.1016/j.tem.2016.08.003
    1. Hao Q., Br D., Wu T. (2015). Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst. Rev (2), CD006895. 10.1002/14651858
    1. Harris V. C., Armah G., Fuentes S., Korpela K. E., Parashar U., Victor J. C., et al. . (2017). Significant Correlation Between the Infant Gut Microbiome and Rotavirus Vaccine Response in Rural Ghana. J. Infect. Dis. 215, 34–41. 10.1093/infdis/jiw518
    1. Hartstra A. V., Bouter K. E. C., Bäckhed F., Nieuwdorp M. (2015). Insights into the role of the microbiome in obesity and type 2 diabetes. Diabetes Care 38, 159–165. 10.2337/dc14-0769
    1. Hashimoto T., Perlot T., Rehman A., Trichereau J., Ishiguro H., Paolino M., et al. . (2012). ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation. Nature 487, 477–481. 10.1038/nature11228
    1. Hedges S. R., Barrientes F., Desmond R. A., Schwebke J. R. (2006). Local and Systemic Cytokine Levels in Relation to Changes in Vaginal Flora. J. Infect. Dis. 193, 556–562. 10.1086/499824
    1. Hendrickson C., Matthay M. (2013). Viral Pathogens and Acute Lung Injury: Investigations Inspired by the SARS Epidemic and the 2009 H1N1 Influenza Pandemic. Semin. Respir. Crit. Care Med. 34, 475–486. 10.1055/s-0033-1351122
    1. Hildebrandt M. (2009). High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137, 1716–1724. 10.1053/j.gastro.2009.08.042
    1. Hill C., Guarner F., Reid G., Gibson G. R., Merenstein D. J., Pot B., et al. . (2014). Expert consensus document: The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat. Rev. Gastroenterol. Hepatol. 11, 506–514. 10.1038/nrgastro.2014.66
    1. Holt P., Strickland D. MW-NR, 2008 undefined. Regulation of immunological homeostasis in the respiratory tract. Available at: (Accessed April 28, 2020). .
    1. Hosoki K., Chakraborty A., Sur S. (2020). Molecular mechanisms and epidemiology of COVID-19 from an allergist’s perspective. J. Allergy Clin. Immunol. 146 (2), 285–299. 10.1016/j.jaci.2020.05.033
    1. Inoue T., Nakayama J., Moriya K., Kawaratani H., Momoda R., Ito K., et al. . (2018). Gut dysbiosis associated with hepatitis C virus infection. Clin. Infect. Dis. 67, 869–877. 10.1093/cid/ciy205
    1. Iuliano A. D., Roguski K. M., Chang H. H., Muscatello D. J., Palekar R., Tempia S., et al. . (2018). Estimates of global seasonal influenza-associated respiratory mortality: a modelling study. Lancet 391, 1285–1300. 10.1016/S0140-6736(17)33293-2
    1. Jakobsson H. E., Abrahamsson T. R., Jenmalm M. C., Harris K., Quince C., Jernberg C., et al. . (2014). Decreased gut microbiota diversity, delayed Bacteroidetes colonisation and reduced Th1 responses in infants delivered by Caesarean section. Gut 63, 559–566. 10.1136/gutjnl-2012-303249
    1. Jenssen H., Hamill P., Hancock R. E. W. (2006). Peptide antimicrobial agents. Clin. Microbiol. Rev. 19, 491–511. 10.1128/CMR.00056-05
    1. Jost T., Lacroix C., Braegger C., Chassard C. (2015). Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr. Rev. 73, 426–437. 10.1093/nutrit/nuu016
    1. Jounai K., Ikado K., Sugimura T., Ano Y., Braun J., Fujiwara D. (2012). Spherical lactic acid bacteria activate plasmacytoid dendritic cells immunomodulatory function via tlr9-dependent crosstalk with myeloid dendritic cells. PLoS One 7 (4), e32588. 10.1371/journal.pone.0032588
    1. Juhn Y. J. (2014). Risks for infection in patients with asthma (or other atopic conditions): Is asthma more than a chronic airway disease? J. Allergy Clin. Immunol. 134, 247–257. 10.1016/j.jaci.2014.04.024
    1. Kalil A. C., Thomas P. G. (2019). Influenza virus-related critical illness: pathophysiology and epidemiology. Crit. Care 23, 1–7. 10.1186/s13054-019-2539-x
    1. Karim Q. A. (2010). Effectiveness and Safety of Tenofovir Gel, an Antiretroviral Microbicide, for the Prevention of HIV Infection in Women. Science (80-) 329, 1168–1174. 10.1126/science.1193748
    1. Kaur L., Gordon M., Baines P. A., Iheozor-Ejiofor Z., Sinopoulou V., Akobeng A. K. (2020). Probiotics for induction of remission in ulcerative colitis. Cochrane Database Syst. Rev. 3, CD005573. 10.1002/14651858.CD005573.pub3
    1. Kim S., Jazwinski S. M. (2018). The Gut Microbiota and Healthy Aging: A Mini-Review. Gerontology 64, 513–520. 10.1159/000490615
    1. Klatt N. R., Cheu R., Birse K., Zevin A. S., Perner M., Noël-romas L., et al. . (2017). Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science (80-) 356, 938–945. 10.1126/science.aai9383
    1. Koutnikova H., Genser B., Monteiro-Sepulveda M., Faurie J.-M., Rizkalla S., Schrezenmeir J., et al. . (2019). Impact of bacterial probiotics on obesity, diabetes and non-alcoholic fatty liver disease related variables: a systematic review and meta-analysis of randomised controlled trials. BMJ Open 9, e017995. 10.1136/bmjopen-2017-017995
    1. Krautkramer K. A., Kreznar J. H., Romano K. A., Vivas E. I., Barrett-Wilt G. A., Rabaglia M. E., et al. . (2016). Diet-Microbiota Interactions Mediate Global Epigenetic Programming in Multiple Host Tissues. Mol. Cell 64, 982–992. 10.1016/j.molcel.2016.10.025
    1. Kumamoto Y., Iwasaki A. (2012). Unique features of antiviral immune system of the vaginal mucosa. Curr. Opin. Immunol. 24, 411–416. 10.1016/j.coi.2012.05.006
    1. Lamers M. M., Beumer J., van der Vaart J., Knoops Kèvin, Puschhof J., Breugem T. I, et al. . (2020). SARS-CoV-2 productively infects human gut enterocytes. Science (80-) 3, eabc1669. 10.1126/science.abc1669
    1. Lanteri M. C., Vahidnia F., Tan S., Stapleton J. T., Norris P. J., Heitman J., et al. . (2015). Downregulation of cytokines and chemokines by GB virus C after transmission via blood transfusion in HIV-positive blood recipients. J. Infect. Dis. 211, 1585–1596. 10.1093/infdis/jiu660
    1. Lasso G., Mayer S. V., Winkelmann E. R., Chu T., Elliot O., Patino-Galindo J. A., et al. . (2019). A Structure-Informed Atlas of Human-Virus Interactions. Cell 178, 1526–1541.e16. 10.1016/j.cell.2019.08.005
    1. Le Doare K., Holder B., Bassett A., Pannaraj P. S. (2018). Mother’s Milk: A purposeful contribution to the development of the infant microbiota and immunity. Front. Immunol. 9, 361. 10.3389/fimmu.2018.00361
    1. Lee D. K., Kang J. Y., Shin H. S., Park I. H., Ha N. J. (2013). Antiviral activity of Bifidobacterium adolescentis SPM0212 against Hepatitis B virus. Arch. Pharm. Res. 36, 1525–1532. 10.1007/s12272-013-0141-3
    1. Lee J. E., Lee S., Lee H., Song Y. M., Lee K., Han M. J., et al. . (2013). Association of the Vaginal Microbiota with Human Papillomavirus Infection in a Korean Twin Cohort. PLoS One 8 (5), e63514. 10.1371/journal.pone.0063514
    1. Lehtoranta L., Latvala S., Lehtinen M. J. (2020). Role of probiotics in stimulating the immune system in viral respiratory tract infections: A narrative review. Nutrients 12, 1–19. 10.3390/nu12103163
    1. Leifer C. A., McConkey C., Li S., Chassaing B., Gewirtz A. T., Ley R. E. (2014). Linking genetic variation in human Toll-like receptor 5 genes to the gut microbiome’s potential to cause inflammation. Immunol. Lett. 162, 3–9. 10.1016/j.imlet.2014.07.017
    1. Lenoir-Wijnkoop I., Merenstein D., Korchagina D., Broholm C., Sanders M. E., Tancredi D. (2019). Probiotics reduce health care cost and societal impact of flu-like respiratory tract infections in the USA: An economic modeling study. Front. Pharmacol. 10, 1–9. 10.3389/fphar.2019.00980
    1. Levy M., Kolodziejczyk A. A., Thaiss C. A., Elinav E. (2017). Dysbiosis and the immune system. Nat. Rev. Immunol. 17, 219–232. 10.1038/nri.2017.7
    1. Li R., Dee D., Li C. M., Hoffman H. J., Grummer-Strawn L. M. (2014). Breastfeeding and risk of infections at 6 years. Pediatrics 134, S13–S20. 10.1542/peds.2014-0646D
    1. Li L., Han Z., Niu X., Zhang G., Jia Y., Zhang S., et al. . (2019). Probiotic Supplementation for Prevention of Atopic Dermatitis in Infants and Children: A Systematic Review and Meta-analysis. Am. J. Clin. Dermatol. 20, 367–377. 10.1007/s40257-018-0404-3
    1. Li N., Ma W. T., Pang M., Fan Q. L., Hua J. L. (2019). The commensal microbiota and viral infection: A comprehensive review. Front. Immunol. 10, 1551. 10.3389/fimmu.2019.01551
    1. Libertucci J., Young V. B. (2019). The role of the microbiota in infectious diseases. Nat. Microbiol. 4, 35–45. 10.1038/s41564-018-0278-4
    1. Lieleg O., Lieleg C., Bloom J., Buck C. B., Ribbeck K. (2012). Mucin biopolymers as broad-spectrum antiviral agents. Biomacromolecules 13, 1724–1732. 10.1021/bm3001292
    1. Listing J., Gerhold K., Zink A. (2013). The risk of infections associated with rheumatoid arthritis, with its comorbidity and treatment. Rheumatol. (United Kingdom) 52, 53–61. 10.1093/rheumatology/kes305
    1. Liu G., Chong H. X., Chung F. Y. L., Li Y., Liong M. T. (2020). Lactobacillus plantarum DR7 modulated bowel movement and gut microbiota associated with dopamine and serotonin pathways in stressed adults. Int. J. Mol. Sci. 21(13), 4608. 10.3390/ijms21134608.
    1. Liu S., Zhi Y., Ying S. (2020). COVID-19 and Asthma: Reflection During the Pandemic. Clin. Rev. Allergy Immunol. 59 (1), 78–88. 10.1007/s12016-020-08797-3
    1. Lloyd-Price J., Abu-Ali G., Huttenhower C. (2016). The healthy human microbiome. Genome Med. 8, 1–11. 10.1186/s13073-016-0307-y
    1. Lunia M. K., Sharma B. C., Sharma P., Sachdeva S., Srivastava S. (2014). Probiotics Prevent Hepatic Encephalopathy in Patients With Cirrhosis: A Randomized Controlled Trial. Clin. Gastroenterol. Hepatol. 12, 1003–1008.e1. 10.1016/j.cgh.2013.11.006
    1. Magro F., Gionchetti P., Eliakim R., Ardizzone S., Armuzzi A., Barreiro-de Acosta M., et al. . (2017). Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: Definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and ileo-anal pouch disorders. J. Crohn’s Colitis 11, 649–670. 10.1093/ecco-jcc/jjx008
    1. Maier H. E., Lopez R., Sanchez N., Ng S., Gresh L., Ojeda S., et al. . (2018). Obesity increases the duration of influenza a virus shedding in adults. J. Infect. Dis. 218, 1378–1382. 10.1093/infdis/jiy370
    1. Mangiola F., Nicoletti A., Gasbarrini A., Ponziani F. R. (2018). Gut microbiota and aging. Eur. Rev. Med. Pharmacol. Sci. 22 (21), 7404–7413. 10.26355/eurrev_201811_16280
    1. Marchand V., Boctor D. L., Critch J. N., Gowrishankar M., Roth D., Unger S. L., et al. . (2012). Using probiotics in the paediatric population. Paediatr. Child Heal. 17, 575. 10.1093/pch/17.10.575
    1. Marchesi J. R., Ravel J. (2015). The vocabulary of microbiome research: a proposal. Microbiome 3, 31. 10.1186/s40168-015-0094-5
    1. Marcobal A., Barboza M., Froehlich J. W., Block D. E., German J.B., Lebrilla C. B., et al. . (2010). Consumption of human milk oligosaccharides by gut-related microbes. J. Agric. Food Chem. 58, 5334–5340. 10.1021/jf9044205
    1. Marín A. C., Gisbert J. P., Chaparro M. (2015). Immunogenicity and mechanisms impairing the response to vaccines in inflammatory bowel disease. World J. Gastroenterol. 21, 11273–11281. 10.3748/wjg.v21.i40.11273
    1. Martín V., Maldonado A., Fernández L., Rodríguez J. M., Connor R. I. (2010). Inhibition of human immunodeficiency virus type 1 by lactic acid bacteria from human breastmilk. Breastfeed Med. 5, 153–158. 10.1089/bfm.2010.0001
    1. Mastromarino P., Cacciotti F., Masci A., Mosca L. (2011). Antiviral activity of Lactobacillus brevis towards herpes simplex virus type 2: Role of cell wall associated components. Anaerobe 17, 334–336. 10.1016/j.anaerobe.2011.04.022
    1. Mcburney M. I., Davis C., Fraser C. M., et al. . (2019). Establishing What Constitutes a Healthy Human Gut Microbiome: State of the Science, Regulatory Considerations, and Future Directions. J. Nutr 149 (11), 1882–1895. 10.1093/jn/nxz174
    1. McCabe M., Sane R. S., Keith-Luzzi M., Xu J., King I., Whitcher-Johnstone A., et al. . (2015). Special section on drug metabolism and the microbiome: Defining the role of gut bacteria in the metabolism of deleobuvir: In vitro and in vivo studies. Drug Metab. Dispos. 43, 1612–1618. 10.1124/dmd.115.064477
    1. Mcfarland L. V. (2014). Use of probiotics to correct dysbiosis of normal microbiota following disease or disruptive events : a systematic review. BMJ 4, e005047. 10.1136/bmjopen-2014-005047
    1. Milani C., Duranti S., Bottacini F., Casey E., Turroni F., Mahony J., et al. . (2017). The First Microbial Colonizers of the Human Gut: Composition, Activities, and Health Implications of the Infant Gut Microbiota. Microbiol. Mol. Biol. Rev. 81, 1–67. 10.1128/MMBR.00036-17
    1. Miller L. E., Lehtoranta L., Lehtinen M. J. (2019). Short-term probiotic supplementation enhances cellular immune function in healthy elderly: systematic review and meta-analysis of controlled studies. Nutr. Res. 64, 1–8. 10.1016/j.nutres.2018.12.011
    1. Milner J. J., Beck M. A. (2012). The impact of obesity on the immune response to infection. Proc. Nutr. Soc. 71, 298–306. 10.1017/S0029665112000158
    1. Milosevic I., Vujovic A., Barac A., Djelic M., Korac M., Radovanovic Spurnic A., et al. . (2019). Gut-liver axis, gut microbiota, and its modulation in the management of liver diseases: A review of the literature. Int. J. Mol. Sci. 20, 1–16. 10.3390/ijms20020395
    1. Mitra A., MacIntyre D. A., Lee Y. S., Smith A., Marchesi J. R., Lehne B., et al. . (2015). Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci. Rep. 5, 1–11. 10.1038/srep16865
    1. Mitra A., MacIntyre D. A., Marchesi J. R., Lee Y. S., Bennett P. R., Kyrgiou M. (2016). The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: What do we know and where are we going next? Microbiome 4, 1–15. 10.1186/s40168-016-0203-0
    1. Moeller A. H. (2017). The shrinking human gut microbiome. Curr. Opin. Microbiol. 38, 30–35. 10.1016/j.mib.2017.04.002
    1. Moelling K., Broecker F. (2019). Viruses and evolution - Viruses first? A personal perspective. Front. Microbiol. 10, 1–13. 10.3389/fmicb.2019.00523
    1. Morris D. E., Cleary D. W., Clarke S. C. (2017). Secondary bacterial infections associated with influenza pandemics. Front. Microbiol. 8, 1–17. 10.3389/fmicb.2017.01041
    1. Moscicki A. B. (2005). Human papilloma virus, papanicolaou smears, and the college female. Pediatr. Clin. North Am. 52, 163–177. 10.1016/j.pcl.2004.10.005
    1. Nagpal R., Yadav H. (2017). Bacterial translocation from the gut to the distant organs: An overview. Ann. Nutr. Metab. 71, 11–16. 10.1159/000479918
    1. Neil J. A., Cadwell K. (2018). The Intestinal Virome and Immunity. J. Immunol. 201, 1615–1624. 10.4049/jimmunol.1800631
    1. Norheim O. F., Jha P., Admasu K., Godal T., Hum R. J., Kruk M. E., et al. . (2015). Avoiding 40% of the premature deaths in each country, 2010-30: Review of national mortality trends to help quantify the un Sustainable Development Goal for health. Lancet 385, 239–252. 10.1016/S0140-6736(14)61591-9
    1. Norman J. M., Handley S. A., Baldridge M. T., Droit L., Liu C. Y., Keller B. C., et al. . (2015). Disease-specific alterations in the enteric virome in inflammatory bowel disease. Cell 160, 447–460. 10.1016/j.cell.2015.01.002
    1. Norrby E. (2008). Nobel Prizes and the emerging virus concept. Arch. Virol. 153, 1109–1123. 10.1007/s00705-008-0088-8
    1. Nunn K. L., Wang Y. Y., Harit D., Humphrys M. S., Ma B., Cone R., et al. . (2015). Enhanced trapping of hiv-1 by human cervicovaginal mucus is associated with lactobacillus crispatus-dominant microbiota. MBio 6, 1–9. 10.1128/mBio.01084-15
    1. Offit P. A. (2018). Challenges to Developing a Rotavirus Vaccine. Viral Immunol. 31 (2), 104–108. 10.1089/vim.2017.0121
    1. Oh J. Z., Ravindran R., Chassaing B., Carvalho F. A., Maddur M. S., Bower M., et al. . (2014). TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 41, 478–492. 10.1016/j.immuni.2014.08.009
    1. Oh J. E., Kim B. C., Chang D. H., Kwon M., Young Lee S., Kang D., et al. . (2016). Dysbiosis-induced IL-33 contributes to impaired antiviral immunity in the genital mucosa. Proc. Natl. Acad. Sci. U. S. A. 113, E762–E771. 10.1073/pnas.1518589113
    1. Olszak T., An D., Zeissig S., Pinilla Vera M., Richter J., Franke A., et al. . (2012). Microbial exposure during early life has persistent effects on natural killer T cell function. Science (80-) 336, 489–493. 10.1126/science.1219328
    1. Ou Y. C., Fu H. C., Tseng C. W., Wu C. H., Tsai C. C., Lin H. (2019). The influence of probiotics on genital high-risk human papilloma virus clearance and quality of cervical smear: a randomized placebo-controlled trial. BMC Womens Health 19, 103. 10.1186/s12905-019-0798-y
    1. Ozen M., Sandal G. K., Dinleyici E. C. (2015). Probiotics for the prevention of pediatric upper respiratory tract infections: A systematic review. Expert Opin. Biol. Ther. 15, 9–20. 10.1517/14712598.2015.980233
    1. Palma E., Recine N., Domenici L., Giorgini M., Pierangeli A., Panici P. B. (2018). Long-term Lactobacillus rhamnosus BMX 54 application to restore a balanced vaginal ecosystem: a promising solution against HPV-infection. BMC Infect. Dis. 18, 13. 10.1186/s12879-017-2938-z
    1. Panwar H., Calderwood D., Grant I. R., Grover S., Green B. D. (2014). Lactobacillus strains isolated from infant faeces possess potent inhibitory activity against intestinal alpha- and beta-glucosidases suggesting anti-diabetic potential. Eur. J. Nutr. 53, 1465–1474. 10.1007/s00394-013-0649-9
    1. Pedersen P. B., Hrobjartsson A., Nielsen D. L., Henriksen D. P., Brabrand M., Lassen A. T. (2017). Prevalence and prognosis of acutely ill patients with organ failure at arrival to hospital: Protocol for a systematic review. Syst. Rev. 6, 1–5. 10.1186/s13643-017-0622-4
    1. Pera A., Campos C., López N., Hassouneh F., Alonso C., Tarazona R., et al. . (2015). Immunosenescence: Implications for response to infection and vaccination in older people. Maturitas 82, 50–55. 10.1016/j.maturitas.2015.05.004
    1. Petersen C., Round J. L. (2014). Defining dysbiosis and its influence on host immunity and disease. Cell Microbiol. 16, 1024–1033. 10.1111/cmi.12308
    1. Pinti M., Appay V., Campisi J., Frasca D., Fülöp T., Sauce D., et al. . (2016). Aging of the immune system: Focus on inflammation and vaccination. Eur. J. Immunol. 46, 2286–2301. 10.1002/eji.201546178
    1. Plaza-diaz J., Gomez-llorente C., Campaña-martin L., Matencio E., Ortuño I., Martínez-Silla R., et al. . (2013). Safety and Immunomodulatory Effects of Three Probiotic Strains Isolated from the Feces of Breast-Fed Infants in Healthy Adults: SETOPROB Study 8 (10), e78111. 10.1371/journal.pone.0078111
    1. Poon T., Juana J., Noori D., Jeansen S., Pierucci-Lagha A., Musa-Veloso K. (2020). Effects of a Fermented Dairy Drink Containing Lacticaseibacillus paracasei subsp. paracasei CNCM I-1518 (Lactobacillus casei CNCM I-1518) and the Standard Yogurt Cultures on the Incidence, Duration, and Severity of Common Infectious Diseases: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Nutrients 12, 3443. 10.3390/nu12113443
    1. Prescott H. C., Dickson R. P., Rogers M. A. M., Langa K. M., Iwashyna T. J. (2015). Hospitalization type and subsequent severe sepsis. Am. J. Respir. Crit. Care Med. 192, 581–588. 10.1164/rccm.201503-0483OC
    1. Przemska-Kosicka A., Childs C. E., Maidens C., Dong H., Todd S., Gosney M. A., et al. . (2018). Age-related changes in the natural killer cell response to seasonal influenza vaccination are not influenced by a synbiotic: A randomised controlled trial. Front. Immunol. 8, 1–9. 10.3389/fimmu.2018.00591
    1. Pyeon D., Pearce S. M., Lank S. M., Ahlquist P., Lambert P. F. (2009). Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog 5 (2), e1000318. 10.1371/journal.ppat.1000318
    1. Quintana V. M., Torres N. I., Wachsman M. B., Sinko P. J., Castilla V., Chikindas M. (2014). Antiherpes simplex virus type 2 activity of the antimicrobial peptide subtilosin. J. Appl. Microbiol. 117, 1253–1259. 10.1111/jam.12618
    1. Renegar K. B., Kudsk K. A., Dewitt R. C., Wu Y., King B. K. (2001). Impairment of mucosal immunity by parenteral nutrition: Depressed nasotracheal influenza-specific secretory IgA levels and transport in parenterally fed mice. Ann. Surg. 233, 134–138. 10.1097/00000658-200101000-00019
    1. Rigo-Adrover M., Pérez-Berezo T., Ramos-Romero S., van Limpt K., Knipping K., Garssen J., et al. . (2017). A fermented milk concentrate and a combination of short-chain galacto-oligosaccharides/long-chain fructo-oligosaccharides/pectin-derived acidic oligosaccharides protect suckling rats from rotavirus gastroenteritis. Br. J. Nutr. 117 (2), 209–217. 10.1017/S0007114516004566
    1. Rizzardini G., Eskesen D., Calder P. C., Capetti A., Jespersen L., Clerici M. (2012). 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. 107, 876–884. 10.1017/S000711451100420X
    1. Robertson R. C., Manges A. R., Finlay B. B., Prendergast A. J. (2019). The Human Microbiome and Child Growth – First 1000 Days and Beyond. Trends Microbiol. 27, 131–147. 10.1016/j.tim.2018.09.008
    1. Rondy M., El Omeiri N., Thompson M. (2017). Effectiveness of influenza vaccines in preventing severe influenza illness among adults: A systematic review and meta- analysis of test-negative design case-control studies. J. Infect. 75, 381–394. 10.1016/j.jinf.2017.09.010
    1. Rothhammer V., Quintana F. J. (2019). The aryl hydrocarbon receptor: an environmental sensor integrating immune responses in health and disease. Nat. Rev. Immunol. 19, 184–197. 10.1038/s41577-019-0125-8
    1. Sartor R. B., Wu G. D. (2017). Roles for Intestinal Bacteria, Viruses, and Fungi in Pathogenesis of Inflammatory Bowel Diseases and Therapeutic Approaches. Gastroenterology 152, 327–339.e4. 10.1053/j.gastro.2016.10.012
    1. Schett G., Manger B., Simon D., Caporali R. (2020). COVID-19 revisiting inflammatory pathways of arthritis. Nat. Rev. Rheumatol. 16, 465–470. 10.1038/s41584-020-0451-z
    1. Schiffman M., Doorbar J., Wentzensen N., de Sanjosé S., Fakhry C., Monk B. J., et al. . (2016). Carcinogenic human papillomavirus infection. Nat. Rev. Dis. Prim. 2, 16086. 10.1038/nrdp.2016.86
    1. Schroeder B. O. (2019). Fight them or feed them: How the intestinal mucus layer manages the gut microbiota. Gastroenterol. Rep. 7, 3–12. 10.1093/gastro/goy052
    1. Schuijt T. J., van der Poll T., de Vos W. M., Wiersinga W. J. (2013). The intestinal microbiota and host immune interactions in the critically ill. Trends Microbiol. 21, 221–229. 10.1016/j.tim.2013.02.001
    1. Semic-Jusufagic A., Belgrave D., Pickles A., Telcian A. G., Bakhsoliani E., Sykes A., et al. . (2014). Assessing the association of early life antibiotic prescription with asthma exacerbations, impaired antiviral immunity, and genetic variants in 17q21: A population-based birth cohort study. Lancet Respir. Med. 2, 621–630. 10.1016/S2213-2600(14)70096-7
    1. Sender R., Fuchs S., Milo R. (2016). Revised Estimates for the Number of Human and Bacteria Cells in the Body. PLoS Biol. 14, 1–14. 10.1371/journal.pbio.1002533
    1. Serkedjieva J., Danova S., Ivanova I. (2000). Antiinfluenza virus activity of a bacteriocin produced by Lactobacillus delbrueckii. Appl. Biochem. Biotechnol. 88, 285–298. 10.1385/ABAB:88:1-3:285.
    1. Sevelsted A., Stokholm J., Bønnelykke K., Bisgaard H. (2015). Cesarean section chronic immune disorders. Pediatrics 135, e92–e98. 10.1542/peds.2014-0596
    1. Shao Y., Forster S. C., Tsaliki E., Vervier K., Strang A., Simpson N., et al. . (2019). Stunted microbiota and opportunistic pathogen colonization in caesarean-section birth. Nature 574, 117–121. 10.1038/s41586-019-1560-1
    1. Simon J. C., Marchesi J. R., Mougel C., Selosse M. A. (2019). Host-microbiota interactions: From holobiont theory to analysis. Microbiome 7, 1–5. 10.1186/s40168-019-0619-4
    1. Smith S. B., Ravel J. (2017). The vaginal microbiota, host defence and reproductive physiology. J. Physiol. 595, 451–463. 10.1113/JP271694
    1. Soh S. E., Ong D. Q. R., Gerez I., Zhang X., Chollate P., Shek L. P. C., et al. . (2010). Effect of probiotic supplementation in the first 6 months of life on specific antibody responses to infant Hepatitis B vaccination. Vaccine 28, 2577–2579. 10.1016/j.vaccine.2010.01.020
    1. Stefan N., Birkenfeld A. L., Schulze M. B., Ludwig D. S. (2020). Obesity and impaired metabolic health in patients with COVID-19. Nat. Rev. Endocrinol. 16, 341–342. 10.1038/s41574-020-0364-6
    1. Stenman L. K., Lehtinen M. J., Meland N., Christensen J. E., Yeung N., Saarinen M. T., et al. . (2016). Probiotic With or Without Fiber Controls Body Fat Mass, Associated With Serum Zonulin, in Overweight and Obese Adults—Randomized Controlled Trial. EBioMedicine 13, 190–200. 10.1016/j.ebiom.2016.10.036
    1. Stoyancheva G., Marzotto M., Dellaglio F., Torriani S. (2014). Bacteriocin production and gene sequencing analysis from vaginal Lactobacillus strains. Arch. Microbiol. 196, 645–653. 10.1007/s00203-014-1003-1
    1. Su Y., Zhang B., Su L. (2013). CD4 detected from Lactobacillus helps understand the interaction between Lactobacillus and HIV. Microbiol. Res. 168, 273–277. 10.1016/j.micres.2012.12.004
    1. Su G., Ko C., Bercik P., Falck-Ytter Y., Sultan S., Weizman A. V., et al. . (2020). AGA Clinical Practice Guidelines on the Role of Probiotics in the Management of Gastrointestinal Disorders. Gastroenterology 159 (2), 697–705. 10.1053/j.gastro.2020.05.059
    1. Su M., Jia Y., Li Y., Zhou D., Jia J. (2020). Probiotics for the Prevention of Ventilator-Associated Pneumonia: A Meta-Analysis of Randomized Controlled Trials. Respir. Care 65 (5), 673–685. 10.4187/respcare.07097
    1. Sung C. M., Chen K. F., Lin Y. f., Ke H. M., Huang H. Y., Gong Y. N., et al. . (2019). Predicting Clinical Outcomes of Cirrhosis Patients With Hepatic Encephalopathy From the Fecal Microbiome. Cmgh 8, 301–318. 10.1016/j.jcmgh.2019.04.008
    1. Szajewska H., Guarino A., Hojsak I., Indrio F., Kolacek S., Orel R., et al. . (2020). Use of Probiotics for the Management of Acute Gastroenteritis in Children. An Update. J. Pediatr. Gastroenterol. Nutr. Publish Ah, 261–269. 10.1097/MPG.0000000000002751
    1. Tabata T., Petitt M., Puerta-Guardo H., Michlmayr D., Wang C., Fang-Hoover J., et al. . (2016). Zika Virus Targets Different Primary Human Placental Cells, Suggesting Two Routes for Vertical Transmission. Cell Host Microbe 20, 155–166. 10.1016/j.chom.2016.07.002
    1. Tamburini S., Shen N., Wu H. C., Clemente J. C. (2016). The microbiome in early life: Implications for health outcomes. Nat. Med. 22, 713–722. 10.1038/nm.4142
    1. Thaiss C. A., Zmora N., Levy M., Elinav E. (2016). The microbiome and innate immunity. Nature 535, 65–74. 10.1038/nature18847
    1. Thèves C., Biagini P., Crubézy E. (2014). The rediscovery of smallpox. Clin. Microbiol. Infect. 20, 210–218. 10.1111/1469-0691.12536
    1. Tian Y., Rong L., Nian W., He Y. (2020). Review article: gastrointestinal features in COVID-19 and the possibility of faecal transmission. Aliment Pharmacol. Ther. 51, 843–851. 10.1111/apt.15731
    1. Tilg H., Moschen A. R. (2015). Food, immunity, and the microbiome. Gastroenterology 148, 1107–1119. 10.1053/j.gastro.2014.12.036
    1. Torres N. I., Noll K. S., Xu S., Li J., Huang Q., Sinko P. J., et al. . (2013). Safety, Formulation and In Vitro Antiviral Activity of the Antimicrobial Peptide Subtilosin Against Herpes Simplex Virus Type 1. Probiotics Antimicrob. Proteins 5, 26–35. 10.1007/s12602-012-9123-x
    1. Toumi M., Ricciardi W. (2015). The Economic Value of Vaccination: Why Prevention is Wealth. J. Mark, Access Health Policy 3, 10.3402/jmahp.v3.29414. 10.3402/jmahp.v3.29204
    1. Tregoning J. S., Russell R. F., Kinnear E. (2018). Adjuvanted influenza vaccines. Hum. Vaccin. Immunother. 14, 550–564. 10.1080/21645515.2017.1415684
    1. Turnbaugh P., Ley R., Hamady M., Fraser-Liggett C. M., Knight R., Gordon J. I. (2017) The Human Microbiome Project. Nature 449, 804–810. 10.1038/nature06244
    1. Turnbaugh P. J., Quince C., Faith J. J., McHardy A. C., Yatsunenko T., Niazi F., et al. . (2010). Organismal, genetic, and transcriptional variation in the deeply sequenced gut microbiomes of identical twins. Proc. Natl. Acad. Sci. U. S. A. 107, 7503–7508. 10.1073/pnas.1002355107
    1. van de Wijgert J. H. H. M., Verwijs M. C. (2020). Lactobacilli-containing vaginal probiotics to cure or prevent bacterial or fungal vaginal dysbiosis: a systematic review and recommendations for future trial designs. BJOG Int. J. Obstet. Gynaecol. 127, 287–299. 10.1111/1471-0528.15870
    1. van Ruissen M. C. E., Bos L. D., Dickson R. P., Dondorp A. M., Schultsz C., Schultz M. J. (2019). Manipulation of the microbiome in critical illness—probiotics as a preventive measure against ventilator-associated pneumonia. Intensive Care Med. Exp. 7 (Suppl 1), 37. 10.1186/s40635-019-0238-1
    1. Vandenplas Y. (2016). Probiotics and prebiotics in infectious gastroenteritis. Best Pract. Res. Clin. Gastroenterol. 30, 49–53. 10.1016/j.bpg.2015.12.002
    1. Verdecchia P., Cavallini C., Spanevello A., Angeli F. (2020). The pivotal link between ACE2 deficiency and SARS-CoV-2 infection. Eur. J. Intern. Med. 76, 14–20. 10.1016/j.ejim.2020.04.037
    1. Verhoeven V., Renard N., Makar A., Van Royen P., Bogers J. P., Lardon F., et al. . (2013). Probiotics enhance the clearance of human papillomavirus-related cervical lesions: A prospective controlled pilot study. Eur. J. Cancer Prev. 22, 46–51. 10.1097/CEJ.0b013e328355ed23
    1. Vlasova A. N., Takanashi S., Miyazaki A., Rajashekara G., Saif L. J. (2019). How the gut microbiome regulates host immune responses to viral vaccines. Curr. Opin. Virol. 37, 16–25. 10.1016/j.coviro.2019.05.001
    1. Wachsman M. B., Castilla V., De Ruiz Holgado A. P., De Torres R. A., Sesma F., Coto C. E. (2003). Enterocin CRL35 inhibits late stages of HSV-1 and HSV-2 replication in vitro. Antiviral Res. 58, 17–24. 10.1016/S0166-3542(02)00099-2
    1. Wang Y., Pan C. Q., Xing H. (2019). Advances in Gut Microbiota of Viral Hepatitis Cirrhosis. BioMed. Res. Int. 2019, 9726786. 10.1155/2019/9726786
    1. Wang J., Wang Y., Zhang X., Liu J., Zhang Q., Zhao Y., et al. . (2017). Gut microbial dysbiosis is associated with altered hepatic functions and serum metabolites in chronic hepatitis B patients. Front. Microbiol. 8, 1–12. 10.3389/fmicb.2017.02222
    1. Wang Y., Liu L., Moore D. J., Shen X., Peek R. M., Acra S. A., et al. . (2017). An LGG-derived protein promotes IgA production through upregulation of APRIL expression in intestinal epithelial cells. Mucosal Immunol. 10, 373–384. 10.1038/mi.2016.57
    1. Wei X., Jiang P., Liu J., Sun R., Zhu L. (2020). Association between probiotic supplementation and asthma incidence in infants: a meta-analysis of randomized controlled trials. J. Asthma 57, 167–178. 10.1080/02770903.2018.1561893
    1. Weng S. F., Redsell S. A., Swift J. A., Yang M., Glazebrook C. P. (2012). Systematic review and meta-analyses of risk factors for childhood overweight identifiable during infancy. Arch. Dis. Child 97, 1019–1026. 10.1136/archdischild-2012-302263
    1. Widdifield J., Bernatsky S., Paterson J. M., Gunraj N., Carter Thorne J., Pope J., et al. . (2013). Serious infections in a population-based cohort of 86,039 seniors with rheumatoid arthritis. Arthritis Care Res. (Hoboken) 65, 353–361. 10.1002/acr.21812
    1. Wiersinga W. J. (2017). The gut microbiome takes center stage in critical care. Curr. Opin. Crit. Care 23, 140–142. 10.1097/MCC.0000000000000390
    1. Wopereis H., Oozeer R., Knipping K., Belzer C., Knol J. (2014). The first thousand days - intestinal microbiology of early life: Establishing a symbiosis. Pediatr. Allergy Immunol. 25, 428–438. 10.1111/pai.12232
    1. Wu S., Jiang Z. Y., Sun Y. F., Yu B., Chen J., Dai C. Q., et al. . (2013). Microbiota regulates the TLR7 signaling pathway against respiratory tract influenza a virus infection. Curr. Microbiol. 67 (4), 414–422. 10.1007/s00284-013-0380-z
    1. Wu Y., Guo C., Tang L., Hong Z., Zhou J., Dong X., et al. . (2020). Prolonged presence of SARS-CoV-2 viral RNA in faecal samples. Lancet Gastroenterol. Hepatol. 5, 434–435. 10.1016/S2468-1253(20)30083-2
    1. Wylie K. M., Mihindukulasuriya K. A., Zhou Y., Sodergren E., Storch G. A., Weinstock G. M. (2014). Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Med. 12, 71. 10.1186/s12915-014-0071-7
    1. Xu K., Cai H., Shen Y., Ni Q., Chen Y., Hu S., et al. . (2020). Management of corona virus disease-19 (COVID-19): the Zhejiang experience. J. Zhejiang Univ. Med. Sci. 49 (1), 147–157. 10.3785/j.issn.1008-9292.2020.02.02
    1. Yang X., Xie L., Li Y., Wei C. (2009). More than 9,000,000 unique genes in human gut bacterial community: Estimating gene numbers inside a human body. PLoS One 4, 0–7. 10.1371/journal.pone.0006074
    1. Yatsunenko T., Rey F. E., Manary M. J., Trehan I., Dominguez-Bello M. G., Contreras M., et al. . (2012). Human gut microbiome viewed across age and geography. Nature 486, 222–227. 10.1038/nature11053
    1. Yeh T. L., Shih P. C., Liu S. J., Lin C. H., Liu J. M., Lei W. T., et al. . (2018). The influence of prebiotic or probiotic supplementation on antibody titers after influenza vaccination: A systematic review and meta-analysis of randomized controlled trials. Drug Des. Devel. Ther 12, 217–230. 10.2147/DDDT.S155110
    1. Yu Z. T., Chen C., Newburg D. S. (2013). Utilization of major fucosylated and sialylated human milk oligosaccharides by isolated human gut microbes. Glycobiology 23, 1281–1292. 10.1093/glycob/cwt065
    1. Zabihollahi R., Motevaseli E., Sadat S. M., Azizi-Saraji A. R., Asaadi-Dalaie S., Modarressi M. H. (2012). Inhibition of HIV and HSV infection by vaginal lactobacilli in vitro and in vivo. DARU J. Pharm. Sci. 20 (1), 53. 10.1186/2008-2231-20-53
    1. Zeng Y., Chen S., Fu Y., Wu W., Chen T., Chen J., et al. . (2020). Gut microbiota dysbiosis in patients with hepatitis B virus–induced chronic liver disease covering chronic hepatitis, liver cirrhosis and hepatocellular carcinoma J. Viral Hepat. 27 (2), 143–155. 10.1111/jvh.13216
    1. Zhang X., Zhang D., Jia H., Feng Q., Wang D., Liang D., et al. . (2015). The oral and gut microbiomes are perturbed in rheumatoid arthritis and partly normalized after treatment. Nat. Med. 21, 895–905. 10.1038/nm.3914
    1. Zhao W., Ho H., Bunyavanich S. (2019). The gut microbiome in food allergy. Ann. Allergy Asthma Immunol. 122, 276–282. 10.1016/j.anai.2018.12.012
    1. Zimmermann P., Curtis N. (2017). The influence of probiotics on vaccine responses – A systematic review. Vaccine 36 (2), 207–213. 10.1016/j.vaccine.2017.08.069
    1. Zou S., Caler L., Colombini-Hatch S., Glynn S., Srinivas P. (2016). Research on the human virome: Where are we and what is next. Microbiome 4 (1), 32. 10.1186/s40168-016-0177-y
    1. Zuo T., Zhang F., Lui G. C. Y., Yeoh Y. K., Li A., Zhan H., et al. . (2020). Alterations in Gut Microbiota of Patients With COVID-19 During Time of Hospitalization. Gastroenterology 159 (3), 944–955.e8. 10.1053/j.gastro.2020.05.048

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다