Effects of Antibiotics upon the Gut Microbiome: A Review of the Literature

Theocharis Konstantinidis, Christina Tsigalou, Alexandros Karvelas, Elisavet Stavropoulou, Chrissoula Voidarou, Eugenia Bezirtzoglou, Theocharis Konstantinidis, Christina Tsigalou, Alexandros Karvelas, Elisavet Stavropoulou, Chrissoula Voidarou, Eugenia Bezirtzoglou

Abstract

The human gastrointestinal tract carries a large number of microorganisms associated with complex metabolic processes and interactions. Although antibiotic treatment is crucial for combating infections, its negative effects on the intestinal microbiota and host immunity have been shown to be of the utmost importance. Multiple studies have recognized the adverse consequences of antibiotic use upon the gut microbiome in adults and neonates, causing dysbiosis of the microbiota. Repeated antibiotic treatments in clinical care or low-dosage intake from food could be contributing factors in this issue. Researchers in both human and animal studies have strived to explain this multifaceted relationship. The present review intends to elucidate the axis of the gastrointestinal microbiota and antibiotics resistance and to highlight the main aspects of the issue.

Keywords: antibiotics; gut microbiome; microbiota; resistance.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Effects of antibiotics upon the gut microbiome. Antibiotic treatment is crucial for combating infections. On the other hand, antibiotic exposure can alter many basic equilibria in terms of intestinal microbiota and host immunity, promoting long-term disease. DC: dendritic cells; DAMP: damage-associated molecular patterns; PMNs: polymorphonuclear leukocytes; PAMP: pathogen-associated molecular patterns; Th: T helper cells.

References

    1. Gaynes R. The Discovery of Penicillin—New Insights after More Than 75 Years of Clinical Use. Emerg. Infect. Dis. 2017;23:849–853. doi: 10.3201/eid2305.161556.
    1. Aslam B., Wang W., Arshad M.I., Khurshid M., Muzammil S., Rasool M.H., Nisar M.A., Alvi R.F., Aslam M.A., Qamar M.U., et al. Antibiotic resistance: A rundown of a global crisis. Infect. Drug Resist. 2018;11:1645–1658. doi: 10.2147/IDR.S173867.
    1. de Jong J., Bos J.H.J., de Vries T.W., de Jong-van den Berg L.T.W. Use of antibiotics in rural and urban regions in The Netherlands: An observational drug utilization study. BMC Public Health. 2014;14:677. doi: 10.1186/1471-2458-14-677.
    1. Russo V., Monetti V.M., Guerriero F., Trama U., Guida A., Menditto E., Orlando V. Prevalence of antibiotic prescription in southern Italian outpatients: Real-world data analysis of socioeconomic and sociodemographic variables at a municipality level. ClinicoEcon. Outcomes Res. 2018;10:251–258. doi: 10.2147/CEOR.S161299.
    1. Stavropoulou E., Tsigalou C., Bezirtzoglou E. Spreading of Antimicrobial Resistance (AMR) across clinical borders. Erciyes Med. J. 2019;41:238–243. doi: 10.14744/etd.2019.99075.
    1. Bezirtzoglou P.E., Alexopoulos A., Voidarou C. Apparent antibiotic misuse in environmental ecosystems and food. Microb. Ecol. Health Dis. 2008;20:197–198. doi: 10.1080/08910600802408103.
    1. Bezirtzoglou E., Stavropoulou E. Immunology and probiotic impact of the newborn and young children intestinal microflora. Anaerobe. 2011;17:369–374. doi: 10.1016/j.anaerobe.2011.03.010.
    1. Cani P.D. Gut microbiota—At the intersection of everything? Nat. Rev. Gastroenterol. Hepatol. 2017;14:321–322. doi: 10.1038/nrgastro.2017.54.
    1. Leong K.S.W., Derraik J.G.B., Hofman P.L., Cutfield W.S. Antibiotics, gut microbiome and obesity. Clin. Endocrinol. 2018;88:185–200. doi: 10.1111/cen.13495.
    1. Belizário J.E., Faintuch J. Microbiome and Gut Dysbiosis. Exp. Suppl. 2018;109:459–476. doi: 10.1007/978-3-319-74932-7_13.
    1. Bartlett J.G., Gilbert D.N., Spellberg B. Seven ways to preserve the miracle of antibiotics. Clin. Infect. Dis. 2013;56:1445–1450. doi: 10.1093/cid/cit070.
    1. Tsigalou C., Stavropoulou E., Bezirtzoglou E. Current Insights in Microbiome Shifts in Sjogren’s Syndrome and Possible Therapeutic Interventions. Front. Immunol. 2018;9 doi: 10.3389/fimmu.2018.01106.
    1. Belizário J.E., Napolitano M. Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front. Microbiol. 2015;6:1050. doi: 10.3389/fmicb.2015.01050.
    1. Sender R., Fuchs S., Milo R. Are We Really Vastly Outnumbered? Revisiting the Ratio of Bacterial to Host Cells in Humans. Cell. 2016;164:337–340. doi: 10.1016/j.cell.2016.01.013.
    1. Qin J., Li R., Raes J., Arumugam M., Burgdorf K.S., Manichanh C., Nielsen T., Pons N., Levenez F., Yamada T., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature. 2010;464:59–65. doi: 10.1038/nature08821.
    1. Almeida A., Mitchell A.L., Boland M., Forster S.C., Gloor G.B., Tarkowska A., Lawley T.D., Finn R.D. A new genomic blueprint of the human gut microbiota. Nature. 2019;568:499–504. doi: 10.1038/s41586-019-0965-1.
    1. Forster S.C., Kumar N., Anonye B.O., Almeida A., Viciani E., Stares M.D., Dunn M., Mkandawire T.T., Zhu A., Shao Y., et al. A human gut bacterial genome and culture collection for improved metagenomic analyses. Nat. Biotechnol. 2019;37:186–192. doi: 10.1038/s41587-018-0009-7.
    1. Cani P.D., Delzenne N.M. Gut microflora as a target for energy and metabolic homeostasis. Curr. Opin. Clin. Nutr. Metab. Care. 2007;10:729–734. doi: 10.1097/MCO.0b013e3282efdebb.
    1. Clarke G., Stilling R.M., Kennedy P.J., Stanton C., Cryan J.F., Dinan T.G. Minireview: Gut microbiota: The neglected endocrine organ. Mol. Endocrinol. 2014;28:1221–1238. doi: 10.1210/me.2014-1108.
    1. Zoetendal E.G., Rajilic-Stojanovic M., de Vos W.M. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut. 2008;57:1605–1615. doi: 10.1136/gut.2007.133603.
    1. Segata N., Haake S.K., Mannon P., Lemon K.P., Waldron L., Gevers D., Huttenhower C., Izard J. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 2012;13:R42. doi: 10.1186/gb-2012-13-6-r42.
    1. Arumugam M., Raes J., Pelletier E., Le Paslier D., Yamada T., Mende D.R., Fernandes G.R., Tap J., Bruls T., Batto J.-M., et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–180. doi: 10.1038/nature09944.
    1. Slingerland A.E., Schwabkey Z., Wiesnoski D.H., Jenq R.R. Clinical Evidence for the Microbiome in Inflammatory Diseases. Front. Immunol. 2017;8:400. doi: 10.3389/fimmu.2017.00400.
    1. Jiménez E., Fernández L., Marín M.L., Martín R., Odriozola J.M., Nueno-Palop C., Narbad A., Olivares M., Xaus J., Rodríguez J.M. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr. Microbiol. 2005;51:270–274. doi: 10.1007/s00284-005-0020-3.
    1. Jiménez E., Marín M.L., Martín R., Odriozola J.M., Olivares M., Xaus J., Fernández L., Rodríguez J.M. Is meconium from healthy newborns actually sterile? Res. Microbiol. 2008;159:187–193. doi: 10.1016/j.resmic.2007.12.007.
    1. Aagaard K., Ma J., Antony K.M., Ganu R., Petrosino J., Versalovic J. The placenta harbors a unique microbiome. Sci. Transl. Med. 2014;6:237ra65. doi: 10.1126/scitranslmed.3008599.
    1. Traykova D., Schneider B., Chojkier M., Buck M. Blood Microbiome Quantity and the Hyperdynamic Circulation in Decompensated Cirrhotic Patients. PLoS ONE. 2017;12:e0169310. doi: 10.1371/journal.pone.0169310.
    1. Neuman H., Forsythe P., Uzan A., Avni O., Koren O. Antibiotics in early life: Dysbiosis and the damage done. FEMS Microbiol. Rev. 2018;42:489–499. doi: 10.1093/femsre/fuy018.
    1. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., 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. USA. 2010;107:14691–14696. doi: 10.1073/pnas.1005963107.
    1. Bezirtzoglou E., Romond C. Occurrence of Bifidobacterium in the feces of newborns delivered by cesarean section. Biol. Neonate. 1990;58:247–251. doi: 10.1159/000243275.
    1. Mitsuoka T., Hayakawa K. The fecal flora in man. I. Composition of the fecal flora of various age groups. Zentralbl. Bakteriol. Orig. A. 1973;223:333–342.
    1. Ellis-Pegler R.B., Crabtree C., Lambert H.P. The faecal flora of children in the United Kingdom. J. Hyg. 1975;75:135–142. doi: 10.1017/S002217240004715X.
    1. Zetterström R., Bennet R., Eriksson M. Sepsis in newborn infants: Its incidence, etiology and prognosis. Pediatriia. 1988:36–40.
    1. Hentges D.J. Human Intestinal Microflora in Health and Disease. Academic Press; Cambridge, MA, USA: 1983.
    1. Koenig J.E., Spor A., Scalfone N., Fricker A.D., Stombaugh J., Knight R., Angenent L.T., Ley R.E. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. USA. 2011;108(Suppl. 1):4578–4585. doi: 10.1073/pnas.1000081107.
    1. Bezirtzoglou E., Romond M.B., Romond C. Modulation of Clostridium perfringens intestinal colonization in infants delivered by caesarean section. Infection. 1989;17:232–236. doi: 10.1007/BF01639526.
    1. Salminen S., von Wright A. Lactic Acid Bacteria: Microbiology and Functional Aspects. 2nd ed. Marcel Dekker; New York, NY, USA: 1998.
    1. Gaon D., Garmendia C., Murrielo N.O., de Cucco Games A., Cerchio A., Quintas R., González S.N., Oliver G. Effect of Lactobacillus strains (L. casei and L. acidophillus Strains cerela) on bacterial overgrowth-related chronic diarrhea. Medicina. 2002;62:159–163.
    1. Chakraborti C.K. New-found link between microbiota and obesity. World J. Gastrointest. Pathophysiol. 2015;6:110–119. doi: 10.4291/wjgp.v6.i4.110.
    1. Van Tyne D., Manson A.L., Huycke M.M., Karanicolas J., Earl A.M., Gilmore M.S. Impact of antibiotic treatment and host innate immune pressure on enterococcal adaptation in the human bloodstream. Sci. Transl. Med. 2019;11 doi: 10.1126/scitranslmed.aat8418.
    1. Murphy E.F., Cotter P.D., Healy S., Marques T.M., O’Sullivan O., Fouhy F., Clarke S.F., O’Toole P.W., Quigley E.M., Stanton C., et al. Composition and energy harvesting capacity of the gut microbiota: Relationship to diet, obesity and time in mouse models. Gut. 2010;59:1635–1642. doi: 10.1136/gut.2010.215665.
    1. Palmer C., Bik E.M., DiGiulio D.B., Relman D.A., Brown P.O. Development of the human infant intestinal microbiota. PLoS Biol. 2007;5:e177. doi: 10.1371/journal.pbio.0050177.
    1. Nord C.E., Edlund C. Impact of antimicrobial agents on human intestinal microflora. J. Chemother. 1990;2:218–237. doi: 10.1080/1120009X.1990.11739021.
    1. Agerholm-Larsen L., Raben A., Haulrik N., Hansen A.S., Manders M., Astrup A. Effect of 8 week intake of probiotic milk products on risk factors for cardiovascular diseases. Eur. J. Clin. Nutr. 2000;54:288–297. doi: 10.1038/sj.ejcn.1600937.
    1. Crovesy L., Ostrowski M., Ferreira D.M.T.P., Rosado E.L., Soares-Mota M. Effect of Lactobacillus on body weight and body fat in overweight subjects: A systematic review of randomized controlled clinical trials. Int. J. Obes. 2017;41:1607–1614. doi: 10.1038/ijo.2017.161.
    1. Rolhion N., Chassaing B. When pathogenic bacteria meet the intestinal microbiota. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2016;371 doi: 10.1098/rstb.2015.0504.
    1. Mikelsaar M. Human microbial ecology: Lactobacilli, probiotics, selective decontamination. Anaerobe. 2011;17:463–467. doi: 10.1016/j.anaerobe.2011.07.005.
    1. Sequeira S., Kavanaugh D., MacKenzie D.A., Šuligoj T., Walpole S., Leclaire C., Gunning A.P., Latousakis D., Willats W.G.T., Angulo J., et al. Structural basis for the role of serine-rich repeat proteins from Lactobacillus reuteri in gut microbe–host interactions. Proc. Natl. Acad. Sci. USA. 2018;115:E2706–E2715. doi: 10.1073/pnas.1715016115.
    1. Ingrassia I., Leplingard A., Darfeuille-Michaud A. Lactobacillus casei DN-114 001 Inhibits the Ability of Adherent-Invasive Escherichia coli Isolated from Crohn’s Disease Patients To Adhere to and To Invade Intestinal Epithelial Cells. Appl. Environ. Microbiol. 2005;71:2880–2887. doi: 10.1128/AEM.71.6.2880-2887.2005.
    1. Jayasinghe T.N., Chiavaroli V., Holland D.J., Cutfield W.S., O’Sullivan J.M. The New Era of Treatment for Obesity and Metabolic Disorders: Evidence and Expectations for Gut Microbiome Transplantation. Front. Cell. Infect. Microbiol. 2016;6:15. doi: 10.3389/fcimb.2016.00015.
    1. Walker A.W., Ince J., Duncan S.H., Webster L.M., Holtrop G., Ze X., Brown D., Stares M.D., Scott P., Bergerat A., et al. Dominant and diet-responsive groups of bacteria within the human colonic microbiota. ISME J. 2011;5:220–230. doi: 10.1038/ismej.2010.118.
    1. Binns N. Probiotics, Prebiotics and the Gut Microbiota. ILSI Europe; Brussels, Belgium: 2013.
    1. Modi S.R., Collins J.J., Relman D.A. Antibiotics and the gut microbiota. J. Clin. Investig. 2014;124:4212–4218. doi: 10.1172/JCI72333.
    1. Mutlu E.A., Gillevet P.M., Rangwala H., Sikaroodi M., Naqvi A., Engen P.A., Kwasny M., Lau C.K., Keshavarzian A. Colonic microbiome is altered in alcoholism. Am. J. Physiol. Gastrointest. Liver Physiol. 2012;302:G966–G978. doi: 10.1152/ajpgi.00380.2011.
    1. Davies J., Davies D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 2010;74:417–433. doi: 10.1128/MMBR.00016-10.
    1. Smith R.A., M’ikanatha N.M., Read A.F. Antibiotic resistance: A primer and call to action. Health Commun. 2015;30:309–314. doi: 10.1080/10410236.2014.943634.
    1. Vrieze A., Out C., Fuentes S., Jonker L., Reuling I., Kootte R.S., van Nood E., Holleman F., Knaapen M., Romijn J.A., et al. Impact of oral vancomycin on gut microbiota, bile acid metabolism, and insulin sensitivity. J. Hepatol. 2014;60:824–831. doi: 10.1016/j.jhep.2013.11.034.
    1. Jernberg C., Löfmark S., Edlund C., Jansson J.K. Long-term impacts of antibiotic exposure on the human intestinal microbiota. Microbiology. 2010;156:3216–3223. doi: 10.1099/mic.0.040618-0.
    1. Panda S., El khader I., Casellas F., López Vivancos J., García Cors M., Santiago A., Cuenca S., Guarner F., Manichanh C. Short-term effect of antibiotics on human gut microbiota. PLoS ONE. 2014;9:e95476. doi: 10.1371/journal.pone.0095476.
    1. Zaura E., Brandt B.W., Teixeira de Mattos M.J., Buijs M.J., Caspers M.P.M., Rashid M.-U., Weintraub A., Nord C.E., Savell A., Hu Y., et al. Same Exposure but Two Radically Different Responses to Antibiotics: Resilience of the Salivary Microbiome versus Long-Term Microbial Shifts in Feces. MBio. 2015;6:e01693-15. doi: 10.1128/mBio.01693-15.
    1. Yassour M., Vatanen T., Siljander H., Hämäläinen A.-M., Härkönen T., Ryhänen S.J., Franzosa E.A., Vlamakis H., Huttenhower C., Gevers D., et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci. Transl. Med. 2016;8:343ra81. doi: 10.1126/scitranslmed.aad0917.
    1. de Lastours V., Fantin B. Résistance aux fluoroquinolones en 2010: Quel impact pour la prescription en réanimation ? Réanimation. 2010;19:347–353. doi: 10.1016/j.reaurg.2010.03.021.
    1. Johanesen P.A., Mackin K.E., Hutton M.L., Awad M.M., Larcombe S., Amy J.M., Lyras D. Disruption of the Gut Microbiome: Clostridium difficile Infection and the Threat of Antibiotic Resistance. Genes. 2015;6:1347–1360. doi: 10.3390/genes6041347.
    1. Leffler D.A., Lamont J.T. Clostridium difficile Infection. N. Engl. J. Med. 2015;373:287–288. doi: 10.1056/NEJMra1403772.
    1. Belkaid Y., Hand T.W. Role of the microbiota in immunity and inflammation. Cell. 2014;157:121–141. doi: 10.1016/j.cell.2014.03.011.
    1. Cox L.M., Blaser M.J. Antibiotics in early life and obesity. Nat. Rev. Endocrinol. 2015;11:182–190. doi: 10.1038/nrendo.2014.210.
    1. Arat S., Spivak A., Van Horn S., Thomas E., Traini C., Sathe G., Livi G.P., Ingraham K., Jones L., Aubart K., et al. Microbiome changes in healthy volunteers treated with GSK1322322, a novel antibiotic targeting bacterial peptide deformylase. Antimicrob. Agents Chemother. 2015;59:1182–1192. doi: 10.1128/AAC.04506-14.
    1. Arboleya S., Sánchez B., Milani C., Duranti S., Solís G., Fernández N., de los Reyes-Gavilán C.G., Ventura M., Margolles A., Gueimonde M. Intestinal microbiota development in preterm neonates and effect of perinatal antibiotics. J. Pediatr. 2015;166:538–544. doi: 10.1016/j.jpeds.2014.09.041.
    1. Clarke S.F., Murphy E.F., O’Sullivan O., Lucey A.J., Humphreys M., Hogan A., Hayes P., O’Reilly M., Jeffery I.B., Wood-Martin R., et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014;63:1913–1920. doi: 10.1136/gutjnl-2013-306541.
    1. Abdulkadir B., Nelson A., Skeath T., Marrs E.C.L., Perry J.D., Cummings S.P., Embleton N.D., Berrington J.E., Stewart C.J. Routine Use of Probiotics in Preterm Infants: Longitudinal Impact on the Microbiome and Metabolome. Neonatology. 2016;109:239–247. doi: 10.1159/000442936.
    1. Cox L.M., Yamanishi S., Sohn J., Alekseyenko A.V., Leung J.M., Cho I., Kim S.G., Li H., Gao Z., Mahana D., et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014;158:705–721. doi: 10.1016/j.cell.2014.05.052.
    1. Bezirtzoglou E.E.V. Intestinal cytochromes P450 regulating the intestinal microbiota and its probiotic profile. Microb. Ecol. Health Dis. 2012;23 doi: 10.3402/mehd.v23i0.18370.
    1. Korpela K., de Vos W.M. Early life colonization of the human gut: Microbes matter everywhere. Curr. Opin. Microbiol. 2018;44:70–78. doi: 10.1016/j.mib.2018.06.003.
    1. Edwards A.N., Karim S.T., Pascual R.A., Jowhar L.M., Anderson S.E., McBride S.M. Chemical and Stress Resistances of Clostridium difficile Spores and Vegetative Cells. Front. Microbiol. 2016;7:1698. doi: 10.3389/fmicb.2016.01698.
    1. Korpela K., de Vos W.M. Antibiotic use in childhood alters the gut microbiota and predisposes to overweight. Microb Cell. 2016;3:296–298. doi: 10.15698/mic2016.07.514.
    1. Drummond L.J., Smith D.G.E., Poxton I.R. Effects of sub-MIC concentrations of antibiotics on growth of and toxin production by Clostridium difficile. J. Med. Microbiol. 2003;52:1033–1038. doi: 10.1099/jmm.0.05387-0.
    1. Zhernakova A., Kurilshikov A., Bonder M.J., Tigchelaar E.F., Schirmer M., Vatanen T., Mujagic Z., Vila A.V., Falony G., Vieira-Silva S., et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science. 2016;352:565–569. doi: 10.1126/science.aad3369.
    1. Amoroso C., Perillo F., Strati F., Fantini M., Caprioli F., Facciotti F. The Role of Gut Microbiota Biomodulators on Mucosal Immunity and Intestinal Inflammation. Cells. 2020;9 doi: 10.3390/cells9051234.
    1. Shuang G., Yu S., Weixiao G., Dacheng W., Zhichao Z., Jing L., Xuming D. Immunosuppressive activity of florfenicol on the immune responses in mice. Immunol. Investig. 2011;40:356–366. doi: 10.3109/08820139.2010.551434.
    1. Cho I., Yamanishi S., Cox L., Methé B.A., Zavadil J., Li K., Gao Z., Mahana D., Raju K., Teitler I., et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature. 2012;488:621–626. doi: 10.1038/nature11400.
    1. Grochla I., Ko H.L., Beuth J., Roszkowski K., Roszkowski W., Pulverer G. Effects of beta-lactam antibiotics imipenem/cilastatin and cefodizime on cellular and humoral immune responses in BALB/c-mice. Zentralbl. Bakteriol. 1990;274:250–258. doi: 10.1016/s0934-8840(11)80108-8.
    1. Garrido-Mesa N., Camuesco D., Arribas B., Comalada M., Bailón E., Cueto-Sola M., Utrilla P., Nieto A., Zarzuelo A., Rodríguez-Cabezas M.E., et al. The intestinal anti-inflammatory effect of minocycline in experimental colitis involves both its immunomodulatory and antimicrobial properties. Pharmacol. Res. 2011;63:308–319. doi: 10.1016/j.phrs.2010.12.011.
    1. Garrido-Mesa J., Rodríguez-Nogales A., Algieri F., Vezza T., Hidalgo-Garcia L., Garrido-Barros M., Utrilla M.P., Garcia F., Chueca N., Rodriguez-Cabezas M.E., et al. Immunomodulatory tetracyclines shape the intestinal inflammatory response inducing mucosal healing and resolution. Br. J. Pharmacol. 2018;175:4353–4370. doi: 10.1111/bph.14494.
    1. Konstantinidis T., Kambas K., Mitsios A., Panopoulou M., Tsironidou V., Dellaporta E., Kouklakis G., Arampatzioglou A., Angelidou I., Mitroulis I., et al. Immunomodulatory Role of Clarithromycin in Acinetobacter baumannii Infection via Formation of Neutrophil Extracellular Traps. Antimicrob. Agents Chemother. 2016;60:1040–1048. doi: 10.1128/AAC.02063-15.
    1. Zhang M., Liang W., Gong W., Yoshimura T., Chen K., Wang J.M. The Critical Role of the Antimicrobial Peptide LL-37/ CRAMP in Protection of Colon Microbiota Balance, Mucosal Homeostasis, Anti-Inflammatory Responses, and Resistance to Carcinogenesis. Crit. Rev. Immunol. 2019;39:83–92. doi: 10.1615/CritRevImmunol.2019030225.
    1. Fan D., Coughlin L.A., Neubauer M.M., Kim J., Kim M.S., Zhan X., Simms-Waldrip T.R., Xie Y., Hooper L.V., Koh A.Y. Activation of HIF-1α and LL-37 by commensal bacteria inhibits Candida albicans colonization. Nat. Med. 2015;21:808–814. doi: 10.1038/nm.3871.
    1. Yoshimura T., McLean M.H., Dzutsev A.K., Yao X., Chen K., Huang J., Gong W., Zhou J., Xiang Y., H Badger J., et al. The Antimicrobial Peptide CRAMP Is Essential for Colon Homeostasis by Maintaining Microbiota Balance. J. Immunol. 2018;200:2174–2185. doi: 10.4049/jimmunol.1602073.
    1. Arampatzioglou A., Papazoglou D., Konstantinidis T., Chrysanthopoulou A., Mitsios A., Angelidou I., Maroulakou I., Ritis K., Skendros P. Clarithromycin Enhances the Antibacterial Activity and Wound Healing Capacity in Type 2 Diabetes Mellitus by Increasing LL-37 Load on Neutrophil Extracellular Traps. Front. Immunol. 2018;9:2064. doi: 10.3389/fimmu.2018.02064.
    1. Inomata M., Horie T., Into T. Effect of the Antimicrobial Peptide LL-37 on Gene Expression of Chemokines and 29 Toll-like Receptor-Associated Proteins in Human Gingival Fibroblasts Under Stimulation with Porphyromonas gingivalis Lipopolysaccharide. Probiotics Antimicrob. Proteins. 2020;12:64–72. doi: 10.1007/s12602-019-09600-2.
    1. Alexandre-Ramos D.S., Silva-Carvalho A.É., Lacerda M.G., Serejo T.R.T., Franco O.L., Pereira R.W., Carvalho J.L., Neves F.A.R., Saldanha-Araujo F. LL-37 treatment on human peripheral blood mononuclear cells modulates immune response and promotes regulatory T-cells generation. Biomed. Pharmacother. 2018;108:1584–1590. doi: 10.1016/j.biopha.2018.10.014.
    1. Kappel B.A., De Angelis L., Heiser M., Ballanti M., Stoehr R., Goettsch C., Mavilio M., Artati A., Paoluzi O.A., Adamski J., et al. Cross-omics analysis revealed gut microbiome-related metabolic pathways underlying atherosclerosis development after antibiotics treatment. Mol. Metab. 2020;36:100976. doi: 10.1016/j.molmet.2020.100976.
    1. Kapoor A., Noronha V., Patil V.M., Joshi A., Menon N., Mahajan A., Janu A., Prabhash K. Concomitant use of antibiotics and immune checkpoint inhibitors in patients with solid neoplasms: Retrospective data from real-world settings. Ecancermedicalscience. 2020;14:1038. doi: 10.3332/ecancer.2020.1038.
    1. Xu L., Zhang C., He D., Jiang N., Bai Y., Xin Y. Rapamycin and MCC950 modified gut microbiota in experimental autoimmune encephalomyelitis mouse by brain gut axis. Life Sci. 2020;253:117747. doi: 10.1016/j.lfs.2020.117747.
    1. Hill J.M., Clement C., Pogue A.I., Bhattacharjee S., Zhao Y., Lukiw W.J. Pathogenic microbes, the microbiome, and Alzheimer’s disease (AD) Front. Aging Neurosci. 2014;6:127. doi: 10.3389/fnagi.2014.00127.
    1. Obrenovich M., Jaworski H., Tadimalla T., Mistry A., Sykes L., Perry G., Bonomo R.A. The Role of the Microbiota-Gut-Brain Axis and Antibiotics in ALS and Neurodegenerative Diseases. Microorganisms. 2020;8 doi: 10.3390/microorganisms8050784.
    1. Sasmita A.O. Modification of the gut microbiome to combat neurodegeneration. Rev. Neurosci. 2019;30:795–805. doi: 10.1515/revneuro-2019-0005.
    1. Zumkehr J., Rodriguez-Ortiz C.J., Cheng D., Kieu Z., Wai T., Hawkins C., Kilian J., Lim S.L., Medeiros R., Kitazawa M. Ceftriaxone ameliorates tau pathology and cognitive decline via restoration of glial glutamate transporter in a mouse model of Alzheimer’s disease. Neurobiol. Aging. 2015;36:2260–2271. doi: 10.1016/j.neurobiolaging.2015.04.005.
    1. Zhong S., Zhou Z., Liang Y., Cheng X., Li Y., Teng W., Zhao M., Liu C., Guan M., Zhao C. Targeting strategies for chemotherapy-induced peripheral neuropathy: Does gut microbiota play a role? Crit. Rev. Microbiol. 2019;45:369–393. doi: 10.1080/1040841X.2019.1608905.
    1. Bajic J.E., Johnston I.N., Howarth G.S., Hutchinson M.R. From the Bottom-Up: Chemotherapy and Gut-Brain Axis Dysregulation. Front. Behav. Neurosci. 2018;12:104. doi: 10.3389/fnbeh.2018.00104.
    1. Ramakrishna C., Corleto J., Ruegger P.M., Logan G.D., Peacock B.B., Mendonca S., Yamaki S., Adamson T., Ermel R., McKemy D., et al. Dominant Role of the Gut Microbiota in Chemotherapy Induced Neuropathic Pain. Sci. Rep. 2019;9:20324. doi: 10.1038/s41598-019-56832-x.
    1. Rocha B.S., Correia M.G., Pereira A., Henriques I., Da Silva G.J., Laranjinha J. Inorganic nitrate prevents the loss of tight junction proteins and modulates inflammatory events induced by broad-spectrum antibiotics: A role for intestinal microbiota? Nitric Oxide. 2019;88:27–34. doi: 10.1016/j.niox.2019.04.001.
    1. Svensson L., Poljakovic M., Demirel I., Sahlberg C., Persson K. Host-Derived Nitric Oxide and Its Antibacterial Effects in the Urinary Tract. Adv. Microb. Physiol. 2018;73:1–62. doi: 10.1016/bs.ampbs.2018.05.001.
    1. Giraud-Gatineau A., Coya J.M., Maure A., Biton A., Thomson M., Bernard E.M., Marrec J., Gutierrez M.G., Larrouy-Maumus G., Brosch R., et al. The antibiotic bedaquiline activates host macrophage innate immune resistance to bacterial infection. Elife. 2020;9 doi: 10.7554/eLife.55692.
    1. Wang J., Chen W.-D., Wang Y.-D. The Relationship Between Gut Microbiota and Inflammatory Diseases: The Role of Macrophages. Front. Microbiol. 2020;11:1065. doi: 10.3389/fmicb.2020.01065.
    1. Maekawa T., Tamura H., Domon H., Hiyoshi T., Isono T., Yonezawa D., Hayashi N., Takahashi N., Tabeta K., Maeda T., et al. Erythromycin inhibits neutrophilic inflammation and mucosal disease by upregulating DEL-1. JCI Insight. 2020 doi: 10.1172/jci.insight.136706.
    1. Pérez M.M., Martins L.M.S., Dias M.S., Pereira C.A., Leite J.A., Gonçalves E.C.S., de Almeida P.Z., de Freitas E.N., Tostes R.C., Ramos S.G., et al. Interleukin-17/interleukin-17 receptor axis elicits intestinal neutrophil migration, restrains gut dysbiosis and lipopolysaccharide translocation in high-fat diet-induced metabolic syndrome model. Immunology. 2019;156:339–355. doi: 10.1111/imm.13028.
    1. Triner D., Devenport S.N., Ramakrishnan S.K., Ma X., Frieler R.A., Greenson J.K., Inohara N., Nunez G., Colacino J.A., Mortensen R.M., et al. Neutrophils Restrict Tumor-Associated Microbiota to Reduce Growth and Invasion of Colon Tumors in Mice. Gastroenterology. 2019;156:1467–1482. doi: 10.1053/j.gastro.2018.12.003.
    1. Motoyama S., Yamada H., Yamamoto K., Wakana N., Terada K., Kikai M., Wada N., Saburi M., Sugimoto T., Kubota H., et al. Social Stress Increases Vulnerability to High-Fat Diet-Induced Insulin Resistance by Enhancing Neutrophil Elastase Activity in Adipose Tissue. Cells. 2020;9 doi: 10.3390/cells9040996.
    1. Oriano M., Gramegna A., Terranova L., Sotgiu G., Sulaiman I., Ruggiero L., Saderi L., Wu B., Chalmers J.D., Segal L.N., et al. Sputum Neutrophil Elastase associates with microbiota and P. aeruginosa in bronchiectasis. Eur. Respir. J. 2020 doi: 10.1183/13993003.00769-2020.
    1. Dicker A.J., Crichton M.L., Pumphrey E.G., Cassidy A.J., Suarez-Cuartin G., Sibila O., Furrie E., Fong C.J., Ibrahim W., Brady G., et al. Neutrophil extracellular traps are associated with disease severity and microbiota diversity in patients with chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 2018;141:117–127. doi: 10.1016/j.jaci.2017.04.022.
    1. Zhang D., Chen G., Manwani D., Mortha A., Xu C., Faith J.J., Burk R.D., Kunisaki Y., Jang J.-E., Scheiermann C., et al. Neutrophil ageing is regulated by the microbiome. Nature. 2015;525:528–532. doi: 10.1038/nature15367.
    1. National Research Council (US) Antibiotics in Animal Feeds. National Academies Press; Washington, DC, USA: 1980. Committee to Study the Human Health Effects of Subtherapeutic Antibiotic Use in Animal Feeds.
    1. CDC Antibiotic Resistance and Food Are Connected. [(accessed on 27 October 2020)]; Available online: .
    1. Anderson A.D., Nelson J.M., Rossiter S., Angulo F.J. Public health consequences of use of antimicrobial agents in food animals in the United States. Microb. Drug Resist. 2003;9:373–379. doi: 10.1089/107662903322762815.
    1. U.S. Food & Drug Administration . 2017 Summary Report on Antimicrobials Sold or Distributed for Use in Food-Producing Animals. U.S. Food & Drug Administration; Tulsa, OK, USA: 2018. 52p
    1. FDA, US . FDA Releases Annual Summary Report on Antimicrobials Sold or Distributed in 2017 for Use in Food-Producing Animals Showing Declines for Past Two Years. FDA; Tulsa, OK, USA: 2020.
    1. Chattopadhyay M.K. Use of antibiotics as feed additives: A burning question. Front. Microbiol. 2014;5:334. doi: 10.3389/fmicb.2014.00334.
    1. Linton A.H., Howe K., Bennett P.M., Richmond M.H., Whiteside E.J. The Colonization of the Human Gut by Antibiotic Resistant Escherichia coli from Chickens. J. Appl. Bacteriol. 1977;43:465–469. doi: 10.1111/j.1365-2672.1977.tb00773.x.
    1. Richmond M.H., Linton K.B. The use of tetracycline in the community and its possible relation to the excretion of tetracycline-resistant bacteria. J. Antimicrob. Chemother. 1980;6:33–41. doi: 10.1093/jac/6.1.33.
    1. Septimus E.J. Antimicrobial Resistance: An Antimicrobial/Diagnostic Stewardship and Infection Prevention Approach. Med. Clin. N. Am. 2018;102:819–829. doi: 10.1016/j.mcna.2018.04.005.
    1. Teoh L., Stewart K., Marino R., McCullough M. Antibiotic resistance and relevance to general dental practice in Australia. Aust. Dent. J. 2018;63:414–421. doi: 10.1111/adj.12643.
    1. Kruse H., Sørum H. Transfer of multiple drug resistance plasmids between bacteria of diverse origins in natural microenvironments. Appl. Environ. Microbiol. 1994;60:4015–4021. doi: 10.1128/AEM.60.11.4015-4021.1994.
    1. Bauer M.A., Kainz K., Carmona-Gutierrez D., Madeo F. Microbial wars: Competition in ecological niches and within the microbiome. Microb. Cell. 2018;5:215–219. doi: 10.15698/mic2018.05.628.
    1. Sundin G.W., Wang N. Antibiotic Resistance in Plant-Pathogenic Bacteria. Annu. Rev. Phytopathol. 2018;56:161–180. doi: 10.1146/annurev-phyto-080417-045946.
    1. Midtvedt T., Lingaas E., Carlstedt-Duke B., Höverstad T., Midtvedt A.C., Saxerholt H., Steinbakk M., Norin K.E. Intestinal microbial conversion of cholesterol to coprostanol in man. Influence of antibiotics. APMIS. 1990;98:839–844. doi: 10.1111/j.1699-0463.1990.tb05004.x.
    1. Sullivan A., Edlund C., Nord C.E. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect. Dis. 2001;1:101–114. doi: 10.1016/S1473-3099(01)00066-4.
    1. Tsigalou C., Konstantinidis T., Stavropoulou E., Bezirtzoglou E.E., Tsakris A. Potential Elimination of Human Gut Resistome by Exploiting the Benefits of Functional Foods. Front. Microbiol. 2020;11 doi: 10.3389/fmicb.2020.00050.
    1. Wright G.D. The antibiotic resistome: The nexus of chemical and genetic diversity. Nat. Rev. Microbiol. 2007;5:175–186. doi: 10.1038/nrmicro1614.
    1. D’Costa V.M., McGrann K.M., Hughes D.W., Wright G.D. Sampling the Antibiotic Resistome. Science. 2006;311:374–377. doi: 10.1126/science.1120800.
    1. Ruppé E., Ghozlane A., Tap J., Pons N., Alvarez A.-S., Maziers N., Cuesta T., Hernando-Amado S., Clares I., Martínez J.L., et al. Prediction of the intestinal resistome by a three-dimensional structure-based method. Nat. Microbiol. 2019;4:112–123. doi: 10.1038/s41564-018-0292-6.
    1. de Smet A.M.G.A., Kluytmans J.A.J.W., Cooper B.S., Mascini E.M., Benus R.F.J., van der Werf T.S., van der Hoeven J.G., Pickkers P., Bogaers-Hofman D., van der Meer N.J.M., et al. Decontamination of the Digestive Tract and Oropharynx in ICU Patients. N. Engl. J. Med. 2009;360:20–31. doi: 10.1056/NEJMoa0800394.
    1. Buelow E., Gonzalez T.B., Versluis D., Oostdijk E.A.N., Ogilvie L.A., van Mourik M.S.M., Oosterink E., van Passel M.W.J., Smidt H., D’Andrea M.M., et al. Effects of selective digestive decontamination (SDD) on the gut resistome. J. Antimicrob. Chemother. 2014;69:2215–2223. doi: 10.1093/jac/dku092.
    1. Goldenberg J.Z., Mertz D., Johnston B.C. Probiotics to Prevent Clostridium difficile Infection in Patients Receiving Antibiotics. JAMA. 2018;320:499. doi: 10.1001/jama.2018.9064.
    1. Wu G., Zhang C., Wang J., Zhang F., Wang R., Shen J., Wang L., Pang X., Zhang X., Zhao L., et al. Diminution of the gut resistome after a gut microbiota-targeted dietary intervention in obese children. Sci. Rep. 2016;6:24030. doi: 10.1038/srep24030.
    1. Zhang C., Yin A., Li H., Wang R., Wu G., Shen J., Zhang M., Wang L., Hou Y., Ouyang H., et al. Dietary Modulation of Gut Microbiota Contributes to Alleviation of Both Genetic and Simple Obesity in Children. EBioMedicine. 2015;2:968–984. doi: 10.1016/j.ebiom.2015.07.007.

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