Abstract
Objective: Vaccination is the second most important method after access to clean water that reduces the burden of infectious diseases.Vaccine efficacy varies among individuals. The fact that microbiota has many roles in the development of the immune system has suggested that it may play a role in vaccine efficacy. In this review, we aimed to summarize publications about the effects of microbiota on vaccine responses. Some studies have shown that different members of the gut microbiota have a systemic effect by regulating the development of certain immune cell segments. In addition, the results of the studies suggest that microbiota deterioration may be effective on the lower efficacy of vaccines in developing countries than developed countries. Although many studies showed that serum antibodies increased after the application of probiotics, these responses were not significantly higher than the placebo controls. Some probiotics show specific effects for a vaccine but have been ineffective for others. In human studies, the effect of prebiotic use on vaccine efficacy has not been demonstrated. Due to the central role of microbiota in the development of the immune system, it is common for the microbiota to have an impact on the efficacy of the vaccine. However, there are few data to date. Although the studies summarized here indicate a certain degree of vaccine-microbiota relationship, further studies are needed.
Keywords: immune system, microbiota, prebiotic, probiotic
References
- Andre, F. E., Booy, R., Bock, H. L., Clemens, J., Datta, S. K., John, T. J., Lee, B. W., Lolekha, S., Peltola, H., Ruff, T. A., Santosham, M., Schmitt, H. J. Vaccination greatly reduces disease, disability, death and inequity worldwide. Bull.World Health Organ. 2008; 86, 140–146.
- De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010 Aug 17;107(33):14691-6.
- Jamieson, A. M. Influence of the microbiome on response to vaccination. Hum. Vaccin. Immunother. 2015; 11, 2329–2331.
- Nguyen, Q. N., Himes, J. E., Martinez, D. R., Permar, S. R. The impact of the gut microbiota on humoral immunity to pathogens and vaccination in early infancy. PLoS Pathog. 2016; 12.
- Bäckhed, F., Roswall, J., Peng, Y., Feng,Q., Jia, H., Kovatcheva-Datchary, P., Li, Y., Xia, Y., Xie, H., Zhong, H., Khan, M. T., Zhang, J., Li, J., Xiao, L., Al-Aama, J., Zhang, D., Lee, Y. S., Kotowska, D., Colding, C., Tremaroli, V., Yin, Y., Bergman, S., Xu, X., Madsen, L., Kristiansen, K., Dahlgren, J.,Wang, J. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 2015; 17, 852.
- Madan, J. C., Hoen, A. G., Lundgren, S. N., Farzan, S. F., Cottingham,K. L., Morrison, H. G., Sogin, M. L., Li, H., Moore, J. H., Karagas, M. R. Association of cesarean delivery and formula supplementationwith the intestinal microbiome of 6-week-old infants. JAMA Pediatr.2016; 170, 212–219.
- Fouhy, F., Ross, R. P., Fitzgerald, G. F., Stanton, C., Cotter, P. D. Composition of the early intestinalmicrobiota: knowledge, knowledge gaps and the use of high-throughput sequencing to address these gaps.Gut Microbes 2012; 3, 203–220.
- Vangay, P., Ward, T., Gerber, J. S., Knights, D. Antibiotics, pediatricdysbiosis, and disease. Cell Host Microbe 2015; 17, 553–564.
- Doan, T., Arzika, A. M., Ray, K. J., Cotter, S. Y., Kim, J., Maliki, R., Zhong,L., Zhou, Z., Porco, T. C., Vanderschelden, B., Keenan, J. D., Lietman,T. M.Gut microbial diversity in antibiotic-naive children after systemic antibiotic exposure: a randomized controlled trial. Clin. Infect. Dis. 2017;64, 1147–1153.
- Azad, M. B.,Konya, T., Persaud, R. R.,Guttman,D. S.,Chari,R. S., Field, C. J., Sears, M. R., Mandhane, P. J., Turvey, S. E., Subbarao, P., Becker, A. B.,Scott, J. A., Kozyrskyj, A. L.; CHILD Study Investigators. Impact of maternal intrapartum antibiotics, method of birth and breastfeeding on gut microbiota during the first year of life: a prospective cohort study. BJOG. ,2015;123, 983–993.
- Kuppala VS, Meinzen-Derr J, Morrow AL, Schibler KR. Prolonged initial empirical antibiotic treatment is associated with adverse outcomes in premature infants. J Pediatr 2011; 159: 720- 5.
- Honda K, Littman DR. The microbiota in adaptive immune homostasis and disease. Nature 2011; 535: 75- 84.
- Schirmer M, Smeekens SP, Vlamakis H, Jaeger M, Oosting M, Franzosa EA et al. Linking the human gutmicrobiome to inflammatory cytokine production capacity. Cell 2016; 167: 1897.
- Quigley EM. Basic Definitions and Concepts: Organization of the Gut Microbiome. Gastroenterol Clin North Am 2017; 46: 1- 8.
- Hansen CH, Nielsen DS, Kverka M, Zakostelska Z, Klimesova K, Hudcovic T, et al. Patterns of early gut colonization shape future immune responses of the host. PLoS One 2012; 7: e34043.
- Slack E, Hapfelmeier S, Stecher B, Velykoredko Y, Stoel M, Lawson MA, et al. Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism. Science 2009; 325: 617- 20.
- Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 2013; 123: 700- 11.
- Macpherson AJ, Geuking MB, Slack E, Hapfelmeier S, McCoy KD. The habitat, double life, citizenship, and forgetfulness of IgA. Immunol Rev 2012; 245: 132- 46.
- Zimmermann P, Curtis N. The influence of the intestinal microbiome on vaccine responses. Vaccine 2018; 36: 4433- 9. Review.
- Eloe-Fadrosh EA, McArthur MA, Seekatz AM, Drabek EF, RaskoDA, Sztein MB, et al. Impact of oral typhoid vaccination on the human gut microbiota and correlations with s. Typhi-specific immunological responses. PLoS One 2013; 8: e62026.
- Seekatz AM, Panda A, Rasko DA, Toapanta FR, Eloe-Fadrosh EA, Khan AQ, et al. Differential response of the cynomolgus macaque gut microbiota to Shigella infection. PLoS One 2013; 8: e64212.
- Hallander HO, Paniagua M, Espinoza F, Askelöf P, Corrales E, Ringman M, et al. Calibrated serological techniques demonstrate significant different serum response rates to an oral killed cholera vaccine between Swedish and Nicaraguan children. Vaccine 2002; 21: 138-45.
- Levine MM. Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine. BMC Biol 2010; 8: 129.
- Jiang V, Jiang B, Tate J, Parashar UD, Patel MM. Performance of rotavirus vaccines in developed and developing countries. Hum Vaccin 2010; 6: 532- 42.
- Lopman BA, Pitzer VE, Sarkar R, Gladstone B, Patel M, Glasser J, et al. Understanding reduced rotavirus vaccine efficacy in low socio-economic settings. PLoS One 2012;7: e41720.
- Grassly NC, Jafari H, Bahl S, Durrani S, Wenger J, Sutter RW et al. Mucosal immunity after vaccination with monovalent and trivalent oral poliovirus vaccine in India. J Infect Dis 2009 1; 200: 794- 801.
- Korpe PS, Petri WA Jr. Environmental enteropathy: critical implications of a poorly understood condition. Trends Mol Med 2012;18: 328- 36.
- Ghoshal UC, Ghoshal U, Ayyagari A, Ranjan P, Krishnani N, Misra A, et al. Tropical sprue is associated with contamination of small bowel with aerobic bacteria and reversible prolongation of orocecal transit time. J Gastroenterol Hepatol 2003;18: 540-7.
- Reikie BA, Adams RC, Ruck CE, Ho K, Leligdowicz A, Pillay S, et al. Ontogeny of Toll-like receptor mediated cytokine responses of South African infants throughout the first year of life. PLoS One 2012;7: e44763.
- Humphrey JH. Child undernutrition, tropical enteropathy, toilets, and handwashing. Lancet 2009; 374: 1032-5.
- Moon SS, Groome MJ, Velasquez DE, Parashar UD, Jones S, Koen A, et al. Prevaccination rotavirus serum IgG and IgA are associated with lower immunogenicity of live, oral human rotavirus vaccine in South African infants. Clin Infect Dis 2016; 62: 157- 65.
- Chilengi R, Simuyandi M, Beach L, Mwila K, Becker-Dreps S, Emperador DM,et al. Association of maternal immunity with rotavirus vaccine immunogenicity in Zambian infants. PLoS One 2016; 11: e0150100.
- Huda MN, Lewis Z, Kalanetra KM, Rashid M, Ahmad SM, Raqib R, et al. Stool microbiota and vaccine responses of infants. Pediatrics 2014;134: e362-72.
- Harris VC, Armah G, Fuentes S, Korpela KE, Parashar U, Victor JC, et al. The infant gut microbiome correlates significantly with rotavirus vaccine response in rural Ghana. J Infect Dis 2017; 215: 34- 41.
- Mullié C, Yazourh A, Thibault H, Odou MF, Singer E, Kalach N,et al. Increased poliovirus-specific intestinal antibody response coincides with promotion of Bifidobacterium longum-infantis and Bifidobacterium breve in infants: a randomized, double-blind, placebocontrolled trial. Pediatr Res 2004; 56: 791- 5.
- Nemes E, Lefler E, Szegedi L, Kapitány A, Kovács JB, Balogh M, et al. Gluten intake interferes with the humoral immune response to recombinant hepatitis B vaccine in patients with celiac disease. Pediatrics 2008; 121: e1570- 6.
- Dorrestein PC, Mazmanian SK, Knight R. Finding the missing links among metabolites, microbes, and the host. Immunity 2014; 40: 824- 32.
- Rooks MG, Garrett WS. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol 2016; 16: 341- 52.
- Kim M, Qie Y, Park J, Kim CH. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe 2016; 20: 202- 14.
- Kim M, Kim CH. Regulation of humoral immunity by gut microbial products. Gut Microbes 2017; 8: 392- 9.
- Oh JZ, Ravindran R, Chassaing B, Carvalho FA, Maddur MS, Bower M, et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity 2014; 41: 478- 92.
- Woo PC, Tsoi HW, Wong LP, Leung HC, Yuen KY. Antibiotics modulate vaccine-induced humoral immune response. Clin Diagn Lab Immunol 1999;6:832-7.
- Lamousé-Smith ES, Tzeng A, Starnbach MN. The intestinal flora is required to support antibody responses to systemic immunization in infant and germ free mice. PLoS One 2011;6: e27662.
- Uchiyama R, Chassaing B, Zhang B, Gewirtz AT. Antibiotic treatment suppresses rotavirus infection and enhances specific humoral immunity. J Infect Dis 2014; 210:171-82.
- Biesbroek G, Bosch AA, Wang X, Keijser BJ, Veenhoven RH, Sanders EA, et al. The impact of breastfeeding on nasopharyngeal microbial communities in infants. Am J Respir Crit Care Med 2014; 190: 298- 308.
- García-López R, Pérez-Brocal V, Diez-Domingo J, Moya A. Gut microbiota in children vaccinated with rotavirus vaccine. Pediatr Infect Dis J 2012; 31: 1300- 2.
- Ang L, Arboleya S, Lihua G, Chuihui Y, Nan Q, Suarez M, et al. The establishment of the infant intestinal microbiome is not affected by rotavirus vaccination. Sci Rep 2014; 4: 7417.
- Chen SY, Tsai CN, Lee YS, Lin CY, Huang KY, Chao HC, et al. Intestinal microbiome in children with severe and complicated acute viral gastroenteritis. Sci Rep 2017; 7: 46130.
- Biavati B et al. Species of the Bifidobacterium in the feces of infants. Microbiologica 1984; 7: 341- 5.
- Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, et al. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 2000; 30: 61- 7.
- Pabst HF, Spady DW. Effect of breast-feeding on antibody response to conjugate vaccine. Lancet 1990; 336: 269- 70.
- Hahn-Zoric M, Fulconis F, Minoli I, Moro G, Carlsson B, Böttiger M,et al. Antibody responses to parenteral and oral vaccines are impaired by conventional and low protein formulas as compared to breastfeeding. Acta Paediatr Scand 1990; 79: 1137- 42.
- Guaraldi F, Salvatori G. Effect of breast and formula feeding on gut microbiota shaping in newborns. Front Cell Infect Microbiol 2012;2:94.
- Jost T, Lacroix C, Braegger CP, Chassard C. New insights in gut microbiota establishment in healthy breast fed neonates. PLoS One 2012; 7: e44595.
- Glass RI, Ing DJ, Stoll BJ, Ing RT. Immune response to rotavirus vaccines among breast-fed and nonbreast-fed children. Adv Exp Med Biol 1991; 310: 249- 54.
- Rennels MB. Influence of breast-feeding and oral poliovirus vaccine on the immunogenicity and efficacy of rotavirus vaccines. J Infect Dis 1996; 174 Suppl 1: S107-11.
- Vesikari T, Prymula R, Schuster V, Tejedor JC, Cohen R, Bouckenooghe A, et al. Efficacy and immunogenicity of live-attenuated human rotavirus vaccine in breast-fed and formula-fed European infants. Pediatr Infect Dis J 2012; 31: 509- 13.
- Brüssow H, Benitez O, Uribe F, Sidoti J, Rosa K, Cravioto A. Rotavirus-inhibitory activity in serial milk samples from Mexican women and rotavirus infections in their children during their first year of life. J Clin Microbiol 1993; 31: 593- 7.
- Rennels MB, Wasserman SS, Glass RI, Keane VA. US Rotavirus Vaccine Efficacy Group. Comparison of immunogenicity and efficacy of rhesus rotavirus reassortant vaccines in breastfed and nonbreastfed children. Pediatrics 1995; 96: 1132- 6.
- Moon SS, Tate JE, Ray P, Dennehy PH, Archary D, Coutsoudis A, et al. Differential profiles and inhibitory effect on rotavirus vaccines of nonantibody components in breast milk from mothers in developing and developed countries. Pediatr Infect Dis J 2013; 32: 863- 70.
- Groome MJ, Moon SS, Velasquez D, Jones S, Koen A, van Niekerk N, Jiang B, et al. Effect of breastfeeding on immunogenicity of oral live-attenuated human rotavirus vaccine: a randomized trial in HIV-uninfected infants in Soweto, South Africa. Bull World Health Organ 2014; 92: 238- 45.
- John TJ, Devarajan LV, Luther L, Vijayarathnam P. Effect of breast-feeding on seroresponse of infants to oral poliovirus vaccination. Pediatrics 1976; 57: 47- 53.
- Davidson LE, Fiorino AM, Snydman DR, Hibberd PL. Lactobacillus GG as an immune adjuvant for live-attenuated influenza vaccine in healthy adults: a randomized double-blind placebo-controlled trial. Eur J Clin Nutr 2011; 65: 501-7.
- Paineau D, Carcano D, Leyer G, Darquy S, Alyanakian MA, Simoneau G, et al. Effects of seven potential probiotic strains on specific immune responses in healthy adults: a double-blind, randomized, controlled trial. FEMS Immunol Med Microbiol 2008; 53: 107- 13.
- Rizzardini G, Eskesen D, Calder PC, Capetti A, Jespersen L, Clerici M. Evaluation of the immune benefits of two probiotic strains Bifidobacterium animalis ssp. lactis, BB-12® and Lactobacillus paracasei ssp. paracasei, L. casei 431® in an influenza vaccination model: a randomised, double-blind, placebo-controlled study. Br J Nutr 2012; 107: 876- 84.
- Kukkonen K, Nieminen T, Poussa T, Savilahti E, Kuitunen M. Effect of probiotics on vaccine antibody responses in infancy--a randomized placebo-controlled double-blind trial. Pediatr Allergy Immunol 2006; 17: 416- 21.
- Matsuda F, Chowdhury MI, Saha A, Asahara T, Nomoto K, Tarique AA, et al. Evaluation of a probiotics, Bifidobacterium breve BBG-01, for enhancement of immunogenicity of an oral inactivated cholera vaccine and safety: a randomized, double-blind, placebo-controlled trial in Bangladeshi children under 5 years of age. Vaccine 2011; 29: 1855-8.
- West NP, Cripps AW. Are vaccination models suitable to determine whether probiotics have beneficial health effects in the general population? Hum Vaccin Immunother 2013; 9: 621- 4. Review.
- Youngster I, Kozer E, Lazarovitch Z, Broide E, Goldman M. Probiotics and the immunological response to infant vaccinations: a prospective, placebo controlled pilot study. Arch Dis Child 2011; 96: 345- 9.
- Soh SE, Ong DQ, Gerez I, Zhang X, Chollate P, Shek LP et al. Effect of probiotic supplementation in the first 6 months of life on specific antibody responses to infant Hepatitis B vaccination. Vaccine 2010; 28: 2577- 9.
- Wu BB, Yang Y, Xu X, Wang WP. Effects of Bifidobacterium supplementationon intestinal microbiota composition and the immune response in healthy infants. World J Pediat: WJP 2016; 12: 177- 82.
- Isolauri E, Joensuu J, Suomalainen H, Luomala M, Vesikari T. Improved immunogenicity of oral D x RRV reassortant rotavirus vaccine by Lactobacillus casei GG. Vaccine 1995; 13: 310- 2.
- Perez N, Iannicelli JC, Girard-Bosch C, Gonzalez S, Varea A, Disalvo L, et al. Effect of probiotic supplementation on immunoglobulins, isoagglutinins and antibody response in children of low socio-economic status. Europ J Nutrit 2010; 49: 173- 9.
- Licciardi PV, Tang ML. Vaccine adjuvant properties of probiotic bacteria. Discov Med 2011;12: 525- 33.
- Fang H, Elina T, Heikki A, Seppo S. Modulation of humoral immune response through probiotic intake. FEMS Immunol Med Microbiol 2000; 29: 47- 52.
- de Vrese M, Rautenberg P, Laue C, Koopmans M, Herremans T, Schrezenmeir J. Probiotic bacteria stimulate virus-specific neutralizing antibodies following abooster polio vaccination. Europ J Nutrit 2005; 44: 406- 13.
- Bunout D, Barrera G, Hirsch S, Gattas V, de la Maza MP, Haschke F, et al. Effects of a nutritional supplement on the immune response and cytokine production in free-living Chilean elderly. JPEN J Parenter Enteral Nutr 2004; 28: 348-54.
- Olivares M, Diaz-Ropero MP, Sierra S, Lara-Villoslada F, Fonolla J, Navas M, et al. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 2007; 23: 254- 60.
- Boge T, Remigy M, Vaudaine S, Tanguy J, Bourdet-Sicard R, van der Werf S. A probiotic fermented dairy drink improves antibody response to influenza vaccination in the elderly in two randomised controlled trials. Vaccine 2009; 27: 5677- 84.
- Namba K, Hatano M, Yaeshima T, Takase M, Suzuki K. Effects of Bifidobacterium longum BB536 administration on influenza infection, influenza vaccine antibody titer, and cell-mediated immunity in the elderly. Biosci Biotechnol Biochem 2010; 74: 939- 45.
- Bosch M, Mendez M, Perez M, Farran A, Fuentes MC, Cune J. Lactobacillus plantarum CECT7315 and CECT7316 stimulate immunoglobulin production after influenza vaccination in elderly. Nutr Hosp 2012; 27: 504- 9.
- Akatsu H, Arakawa K, Yamamoto T, Kanematsu T, Matsukawa N, Ohara H, et al. Lactobacillus in jelly enhances the effect of influenza vaccination in elderly individuals. J Am Geriatr Soc 2013; 61: 1828- 30.
- Jespersen L, Tarnow I, Eskesen D, Morberg CM, Michelsen B, Bugel S, et al. Effect of Lactobacillus paracasei subsp. paracasei, L. casei 431 on immune response to influenza vaccination and upper respiratory tract infections in healthy adult volunteers: a randomized, double-blind, placebo-controlled, parallel-group study. Am J Clin Nutrit 2015; 101: 1188- 96.
- Maruyama M, Abe R, Shimono T, Iwabuchi N, Abe F, Xiao JZ. The effects of non-viable Lactobacillus on immune function in the elderly: a randomised, double-blind, placebo-controlled study. Internat J Food Sci Nutrit 2016; 67: 67-73.
- Redondo N, Nova E, Gheorghe A, Diaz LE, Hernandez A, Marcos A. Evaluation of Lactobacillus coryniformis CECT5711 strain as a coadjuvant in a vaccination process: a randomised clinical trial in healthy adults. Nutrition and Metabolism 2017; 14.
- Chattha KS, Vlasova AN, Kandasamy S, Rajashekara G, Saif LJ. Divergent immunomodulating effects of probiotics on T cell responses to oral attenuated human rotavirus vaccine and virulent human rotavirus infection in a neonatal gnotobiotic piglet disease model. J Immunol 2013; 191: 2446- 56.
- Chattha KS, Vlasova AN, Kandasamy S, Esseili MA, Siegismund C, Rajashekara G, et al. Probiotics and colostrum/milk differentially affect neonatal humoral immune responses to oral rotavirus vaccine. Vaccine 2013; 31: 1916- 23.
- Zimmermann P, Curtis N. The influence of probiotics on vaccine responses – A systematic review. Vaccine 2018; 36: 207- 213.
- Benyacoub J, Rochat F, Saudan KY, Rochat I, Antille N, Cherbut C, et al. Feeding a diet containing a fructooligosaccharide mix can enhance Salmonella vaccine efficacy in mice. J Nutr 2008; 138: 123- 9.
- Vos AP, Knol J, Stahl B, M’rabet L, Garssen J. Specific prebiotic oligosaccharides modulate the early phase of a murine vaccination response. Int Immunopharmacol 2010; 10: 619-25.
- Stam J, van Stuijvenberg M, Garssen J, Knipping K, Sauer PJ. A mixture of three prebiotics does not affect vaccine specific antibody responses in healthy term infants in the first year of life. Vaccine 2011; 29: 7766- 72.
- Duggan C, Penny ME, Hibberd P, Gil A, Huapaya A, Cooper A, et al. Oligofructose-supplemented infant cereal: 2 randomized, blinded, community-based trials in Peruvian infants. Am J Clin Nutr 2003; 77: 937- 42.
- van den Berg JP, Westerbeek EA, van der Klis FR, Berbers GA, Lafeber HN, van Elburg RM. Neutral and acidic oligosaccharides supplementation does not increase the vaccine antibody response in preterm infants in a randomized clinical trial. PLoS One 2013; 8: e70904.
- Enani S, Przemska-Kosicka A, Childs CE, Maidens C, Dong H, Conterno L, et al. Impact of ageing and a synbiotic on the immune response to seasonal influenza vaccination; a randomised controlled trial. Clin Nutr 2018; 37: 443- 451.
- Pabst O, Hornef M. Gutmicrobiota: a natural adjuvant for vaccination. Immunity 2014; 41: 349- 51.
- Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, et al. Programming themagnitude and persistence of antibody responses with innate immunity. Nature 2011; 470, 543- 7.
- Kim D, Kim YG, Seo SU, Kim DJ, Kamada N, Prescott, D et al. Nod2- mediated recognition of the microbiota is critical formucosal adjuvantactivity of cholera toxin. Nat Med 2016; 22:524- 30.
- Chow JC, Young DW, Golenbock DT, Christ WJ, Gusovsky F.Toll-like receptor-4 mediates lipopolysaccharide-induced signaltransduction. J Biol Chem 1999; 274:10689-92.
- Vatanen T, Kostic AD, d’Hennezel E, Siljander H, Franzosa EA, Yassour M, et al. Variation in microbiome LPS immunogenicity contributes to autoimmunity in humans. Cell 2016;165:842- 53.
- Pulendran B, Kumar P, Cutler CW, Mohamadzadeh M, Van Dyke T, Banchereau J. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J Immunol 2001; 167: 5067-76.
- Zeng MY, Inohara N, Nuñez G. Mechanisms of inflammationdriven bacterial dysbiosis in the gut. Mucosal Immunol 2017;10:18- 26.
- Fei N, Zhao L. An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice. ISME J 2013;7:880- 4.
- Tulstrup MV, Christensen EG, Carvalho V, Linninge C, Ahrné S, Højberg O, et al. Antibiotic treatment affects intestinal permeability and gut microbial composition in Wistar rats dependent on antibiotic class. PLoS One 2015; 10: e0144854.
- Brenchley JM, Douek DC. Microbial translocation across the GI tract. Annu Rev Immunol 2012; 30: 149- 73.
- Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao, S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12:1365- 71.
- Cooke KR, Olkiewicz K, Erickson N, Ferrara JL. The role of endotoxin and the innate immune response in the pathophysiology of acute graft versus host disease. J Endotoxin Res 2002; 8: 441-8.
- Caradonna L, Amati L, Magrone T, Pellegrino NM, Jirillo E, Caccavo D. Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. J Endotoxin Res 2000; 6: 205- 14.
- Zeng MY, Cisalpino D, Varadarajan S, Hellman J, Warren HS, Cascalho M, et al. Gut microbiota-induced immunoglobulin G controls systemic infection by symbiotic bacteria and pathogens. Immunity 2016;44: 647- 58.
- Kim YG. Microbiota Influences Vaccine and Mucosal Adjuvant Efficacy. Immune Netw 2017;17: 20-4.
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