Managing the clinical effects of drug-induced intestinal dysbiosis with a focus to antibiotics: Challenges and opportunities

Al Jalali, 2018, Clinical pharmacokinetics and pharmacodynamics of telavancin compared with the other glycopeptides, Clin. Pharmacokinet., 57, 797, 10.1007/s40262-017-0623-4 Andremont, 2021, Spare and repair the gut microbiota from antibiotic-induced dysbiosis: state-of-the-art, Drug Discov. Today, 26, 2159, 10.1016/j.drudis.2021.02.022 Anthony, 2022, Acute and persistent effects of commonly used antibiotics on the gut microbiome and resistome in healthy adults, Cell Rep., 39, 10.1016/j.celrep.2022.110649 Aronson, 2021, Analysis of reports of unintended pregnancies associated with the combined use of non-enzyme-inducing antibiotics and hormonal contraceptives, BMJ Evid. Med., 26, 112, 10.1136/bmjebm-2020-111363 Arvidsson, 1982, Ceftriaxone: renal and biliary excretion and effect on the colon microflora, J. Antimicrob. Chemother., 10, 207, 10.1093/jac/10.3.207 Azadkhan, 1982, The disposition and metabolism of sulphasalazine (salicylazosulphapyridine) in man, Br. J. Clin. Pharmacol., 13, 523, 10.1111/j.1365-2125.1982.tb01415.x Bamigbade, 2022, An updated review on prebiotics: insights on potentials of food seeds waste as source of potential prebiotics, Molecules, 27, 5947, 10.3390/molecules27185947 Baquero, 2012, The microbiome as a human organ, Clin. Microbiol. Infect., 18, 2, 10.1111/j.1469-0691.2012.03916.x Baral, 2021, Advancements in the pharmaceutical applications of probiotics: dosage forms and formulation technology, Int. J. Nanomed., 12, 7535, 10.2147/IJN.S337427 Barr, 1991, The pharmacokinetics of ceftibuten in humans, Diagn. Microbiol. Infect. Dis., 14, 93, 10.1016/0732-8893(91)90096-X Brogard, 1981, Biliary excretion of cefuroxime. experimental and human study, Chemotherapy, 27, 18, 10.1159/000237950 Brogard, 1977, Biliary excretion of ampicillin: experimental and clinical study, Chemotherapy, 23, 213, 10.1159/000221989 Buffie, 2013, Microbiota-mediated colonization resistance against intestinal pathogens, Nat. Rev. Immunol., 13, 790, 10.1038/nri3535 Cammarota, 2017, European consensus conference on faecal microbiota transplantation in clinical practice, Gut, 66, 569, 10.1136/gutjnl-2016-313017 Cipher Pharmaceuticals Inc, 2018. XYDALBA PRODUCT MONOGRAPH. https://www.cipherpharma.com/wp-content/uploads/2018/09/Xydalba-PM_Aug_2018_-EN.pdf (Accessed 26 March 2023). Collado, 2019, Postbiotics: facts and open questions. A position paper on the need for a consensus definition, Benef Microbes, 10, 711, 10.3920/BM2019.0015 Collinson, 2020, Probiotics for treating acute infectious diarrhoea, Cochrane Database Syst. Rev., 12 Connelly, 2019, Oral metallo-beta-lactamase protects the gut microbiome from carbapenem-mediated damage and reduces propagation of antibiotic resistance in pigs, Front. Microbiol., 10, 101, 10.3389/fmicb.2019.00101 Darkes, 2002, Cefditoren pivoxil, Drugs, 62, 319, 10.2165/00003495-200262020-00006 de Gunzburg, 2015, Targeted adsorption of molecules in the colon with the novel adsorbent-based Medicinal Product, DAV132: a proof of concept study in healthy subjects, J. Clin. Pharmacol., 55, 10, 10.1002/jcph.359 de Gunzburg, 2018, Protection of the human gut microbiome from antibiotics, J. Infect. Dis., 217, 628, 10.1093/infdis/jix604 Duvallet, 2017, Meta-analysis of gut microbiome studies identifies disease-specific and shared responses, Nat. Commun., 8, 1784, 10.1038/s41467-017-01973-8 2015, Scientific Opinion on the substantiation of a health claim related to “native chicory inulin” and maintenance of normal defecation by increasing stool frequency pursuant to Article 13(5) of Regulation (EC) No 1924/2006, EFSA J., 13 European Medicines Agency, 2019. Committee for Medicinal Products for Human Use (CHMP) Assessment report [WWW Document]. https://www.ema.europa.eu/en/documents/referral/bacterial-lysate-medicines-article-31-referral-chmp-assessment-report_en.pdf (Accessed 26 March 2023). European Medicines Agency, 2014. Public summary of opinion on orphan designation Lactobacillus acidophilus and Bifidobacterium bifidum for the prevention of necrotising enterocolitis [WWW Document]. https://www.ema.europa.eu/en/documents/orphan-designation/eu/3/13/1213-public-summary-opinion-orphan-designation-lactobacillus-acidophilus-bifidobacterium-bifidum_en.pdf (Accessed 26 March 2023). Falony, 2016, Population-level analysis of gut microbiome variation, Science, 352, 560, 10.1126/science.aad3503 FDA In Brief, 2019. FDA warns about potential risk of serious infections caused by multi-drug resistant organisms related to the investigational use of fecal microbiota for transplantation. https://www.fda.gov/news-events/fda-brief/fda-brief-fda-warns-about-potential-risk-serious-infections-caused-multi-drug-resistant-organisms (Accessed 26 March 2023). FDA News Release, 2022. FDA approves first fecal microbiota product. https://www.fda.gov/news-events/press-announcements/fda-approves-first-fecal-microbiota-product (Accessed 26 March 2023). FDA News Release, 2023. FDA approves first orally administered fecal microbiota product for the prevention of recurrence of clostridioides difficile infection. https://www.fda.gov/news-events/press-announcements/fda-approves-first-orally-administered-fecal-microbiota-product-prevention-recurrence-clostridioides) (Accessed 02 June 2023). Ferring Pharmaceuticals Inc, 2022. Rebyota prescribing information. https://ferringus2.corporate-us.ferring.tech/wp-content/uploads/sites/12/2022/12/9009000002_REBYOTA-PI_11-2022.pdf. (Accessed 26 March 2023). Feuerstadt, 2022, Heterogeneity of randomized controlled trials of fecal microbiota transplantation in recurrent clostridioides difficile infection, Dig. Dis. Sci., 67, 2763, 10.1007/s10620-021-07141-9 Fish, 1997, The clinical pharmacokinetics of levofloxacin, Clin. Pharmacokinet., 32, 101, 10.2165/00003088-199732020-00002 Gibson, 2017, Expert consensus document: the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics, Nat. Rev. Gastroenterol. Hepatol., 14, 491, 10.1038/nrgastro.2017.75 Gibson, 1995, Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics, J. Nutr., 125, 1401, 10.1093/jn/125.6.1401 Gonzales-Luna, 2023, Emerging options for the prevention and management of clostridioides difficile infection, Drugs, 83, 105, 10.1007/s40265-022-01832-x Guo, 2019, Commensal gut bacteria convert the immunosuppressant tacrolimus to less potent metabolites, Drug Metab. Dispos., 47, 194, 10.1124/dmd.118.084772 Haiser, 2013, Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta, Science, 341, 295, 10.1126/science.1235872 Harbord, 2017, Third European evidence-based consensus on diagnosis and management of ulcerative colitis. part 2: current management, J. Crohns Colitis., 11, 769, 10.1093/ecco-jcc/jjx009 Hill, 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, 10.1038/nrgastro.2014.66 Hoffman, 2008, Implications on emergence of antimicrobial resistance as a critical aspect in the design of oral sustained release delivery systems of antimicrobials, Pharm. Res., 25, 667, 10.1007/s11095-007-9373-6 Hooks, 2017, Dysbiosis and its discontents, MBio, 8, 10.1128/mBio.01492-17 Hsiao, 2013, Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders, Cell, 155, 1451, 10.1016/j.cell.2013.11.024 Imhann, 2016, Proton pump inhibitors affect the gut microbiome, Gut, 65, 740, 10.1136/gutjnl-2015-310376 Jackson, 2018, Gut microbiota associations with common diseases and prescription medications in a population-based cohort, Nat. Commun., 9, 2655, 10.1038/s41467-018-05184-7 Jaeggi, 2015, Iron fortification adversely affects the gut microbiome, increases pathogen abundance and induces intestinal inflammation in Kenyan infants, Gut, 64, 731, 10.1136/gutjnl-2014-307720 Janarthanan, 2012, Clostridium difficile-associated diarrhea and proton pump inhibitor therapy: a meta-analysis, Am. J. Gastroenterol., 107, 1001, 10.1038/ajg.2012.179 Jandhyala, 2015, Role of the normal gut microbiota, World J. Gastroenterol., 21, 8787, 10.3748/wjg.v21.i29.8787 Jehl, 1987, Investigation of the biliary clearances of cefotaxime and desacetylcefotaxime by an original procedure in cholecystectomised patients, Infection, 15, 450, 10.1007/BF01647231 Johanesen, 2015, Disruption of the gut microbiome: clostridium difficile infection and the threat of antibiotic resistance, Genes (Basel), 6, 1347, 10.3390/genes6041347 Kassam, 2013, Fecal microbiota transplantation for clostridium difficile infection: systematic review and meta-analysis, Am. J. Gastroenterol., 108, 500, 10.1038/ajg.2013.59 Kaur, 2020, Probiotics for induction of remission in ulcerative colitis, Cochrane Database Syst. Rev., 3 Kennedy, 2023, Questioning the fetal microbiome illustrates pitfalls of low-biomass microbial studies, Nature, 613, 639, 10.1038/s41586-022-05546-8 Khanna, 2016, A novel microbiome therapeutic increases gut microbial diversity and prevents recurrent clostridium difficile infection, J. Infect. Dis., 214, 173, 10.1093/infdis/jiv766 Khoder, 2010, Removal of residual colonic ciprofloxacin in the rat by activated charcoal entrapped within zinc-pectinate beads, Eur. J. Pharm. Sci., 41, 281, 10.1016/j.ejps.2010.06.018 Kim, 2021, Effects of vancomycin-induced gut microbiome alteration on the pharmacodynamics of metformin in healthy male subjects, Clin. Transl. Sci., 14, 1955, 10.1111/cts.13051 Kokai-Kun, 2019, Use of ribaxamase (SYN-004), a β-lactamase, to prevent Clostridium difficile infection in β-lactam-treated patients: a double-blind, phase 2b, randomised placebo-controlled trial, Lancet Infect. Dis., 19, 487, 10.1016/S1473-3099(18)30731-X Kootte, 2017, Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition, Cell Metab., 26, 10.1016/j.cmet.2017.09.008 Korpela, 2016, Intestinal microbiome is related to lifetime antibiotic use in Finnish pre-school children, Nat. Commun., 7, 10410, 10.1038/ncomms10410 Kotzampassi, 2015, A four-probiotics regimen reduces postoperative complications after colorectal surgery: a randomized, double-blind, placebo-controlled study, World J. Surg., 39, 2776, 10.1007/s00268-015-3071-z Kundu, 2017, Our gut microbiome: the evolving inner self, Cell, 171, 1481, 10.1016/j.cell.2017.11.024 Lahtinen, 2022, Effectiveness of fecal microbiota transplantation for weight loss in patients with obesity undergoing bariatric surgery: a randomized clinical trial, JAMA Netw. Open, 5, 10.1001/jamanetworkopen.2022.47226 Langlands, 2004, Prebiotic carbohydrates modify the mucosa associated microflora of the human large bowel, Gut, 53, 1610, 10.1136/gut.2003.037580 Lavi, 2022, Serum cholesterol increase in statin users associated with antibiotic use: case-crossover study, Eur. J. Pharmacol., 932, 10.1016/j.ejphar.2022.175209 Lee, 2015, Gut microbiota and tacrolimus dosing in kidney transplantation, PLoS One, 10 Lennernäs, 2010, The use of biopharmaceutic classification of drugs in drug discovery and development: current status and future extension, J. Pharm. Pharmacol., 57, 273, 10.1211/0022357055263 Lescure, F., de Gunzburg, J., 2018. Formulations for oral delivery of adsorbents in the gut https://patentimages.storage.googleapis.com/4e/c5/9c/4400b2ffff2741/US9968562.pdf (Accessed 26 March 2023). Leventogiannis, K., Gkolfakis, P., Spithakis, G., Tsatali, A., Pistiki, A., Sioulas, A., Giamarellos-Bourboulis, E.J., Triantafyllou, K., 2019. Effect of a preparation of four probiotics on symptoms of patients with irritable bowel syndrome: association with intestinal bacterial overgrowth. 11, 627–634. https://doi.org/10.1007/s12602-018-9401-3. Lockyer, 2019, Prebiotics − an added benefit of some fibre types, Nutr. Bull., 44, 74, 10.1111/nbu.12366 Luke, 1997, Disposition of oral azithromycin in humans, Clin. Pharmacol. Ther., 61, 641, 10.1016/S0009-9236(97)90098-9 Lurienne, 2020, NSCLC immunotherapy efficacy and antibiotic use: a systematic review and meta-analysis, J. Thorac. Oncol., 15, 1147, 10.1016/j.jtho.2020.03.002 Lynch, 2016, The human intestinal microbiome in health and disease, N. Engl. J. Med., 375, 2369, 10.1056/NEJMra1600266 Maher, 2014, Clinical consequences of polypharmacy in elderly, Expert Opin. Drug Saf., 13, 57, 10.1517/14740338.2013.827660 Maier, 2018, Extensive impact of non-antibiotic drugs on human gut bacteria, Nature, 555, 623, 10.1038/nature25979 Marra, 2009, Antibiotic use in children is associated with increased risk of asthma, Pediatrics, 123, 1003, 10.1542/peds.2008-1146 Matzke, 1986, Clinical pharmacokinetics of vancomycin, Clin. Pharmacokinet., 11, 257, 10.2165/00003088-198611040-00001 Maynard, 2012, Reciprocal interactions of the intestinal microbiota and immune system, Nature, 489, 231, 10.1038/nature11551 McFarland, 2008, Antibiotic-associated diarrhea: epidemiology, trends and treatment, Fut. Microbiol., 3, 563, 10.2217/17460913.3.5.563 McGovern, 2021, SER-109, an investigational microbiome drug to reduce recurrence after clostridioides difficile infection: lessons learned from a phase 2 trial, Clin. Infect. Dis., 72, 2132, 10.1093/cid/ciaa387 Mitsuoka, 1990, Bifidobacteria and their role in human health, J. Ind. Microbiol., 6, 263, 10.1007/BF01575871 Mulder, 2020, Long-term effects of antimicrobial drugs on the composition of the human gut microbiota, Gut Microbes, 12, 10.1080/19490976.2020.1791677 Munita, 2016, Mechanisms of antibiotic resistance, Microbiol. Spectr., 4, 10.1128/microbiolspec.VMBF-0016-2015 Murray, 2018, Novel insights into selection for antibiotic resistance in complex microbial communities, MBio, 9, 10.1128/mBio.00969-18 Nakashima, 1992, Phase I study of levofloxacin, (S)-(-)-Ofloxacin, Jpn. J. Clin. Pharmacol. Ther., 23, 515, 10.3999/jscpt.23.515 Nakayama, 1997, Intestinal anaerobic bacteria hydrolyse sorivudine, producing the high blood concentration of 5-(E)-(2-bromovinyl)uracil that increases the level and toxicity of 5-fluorouracil, Pharmacogenetics, 7, 35, 10.1097/00008571-199702000-00005 Neuman, 1988, Clinical pharmacokinetics of the newer antibacterial 4-quinolones, Clin. Pharmacokinet., 14, 96, 10.2165/00003088-198814020-00003 Nord C.E., 2000. Pharmacology of moxifloxacin – absorption, distribution, metabolism and excretion, Chapter 22, in: L. Mandell (Ed.), First International Moxifloxacin Symposium. Springer-Verlag Berlin, Heidelberg, pp. 122–126. O'Toole, 2017, Next-generation probiotics: the spectrum from probiotics to live biotherapeutics, Nat. Microbiol., 2, 17057, 10.1038/nmicrobiol.2017.57 Paganini, 2017, The effects of iron fortification and supplementation on the gut microbiome and diarrhea in infants and children: a review, Am. J. Clin. Nutr., 106, 1688, 10.3945/ajcn.117.156067 Parker, 1974, Probiotics, the other half of the antibiotic story, Anim. Nutr. Health, 29, 4 Raine, 2022, ECCO guidelines on therapeutics in ulcerative colitis: medical treatment, J. Crohns Colitis., 16, 2, 10.1093/ecco-jcc/jjab178 Rodvold, 1999, Clinical pharmacokinetics of clarithromycin, Clin. Pharmacokinet., 37, 385, 10.2165/00003088-199937050-00003 Rolfe, 2006, Probiotics for maintenance of remission in Crohn's disease, Cochrane Database Syst. Rev., 18 Roy Sarkar, 2020, Probiotics protect against gut dysbiosis associated decline in learning and memory, J. Neuroimmunol., 348, 10.1016/j.jneuroim.2020.577390 Saha, 1983, Digoxin-inactivating bacteria: identification in human gut flora, Science, 220, 325, 10.1126/science.6836275 Salminen, 2021, The International Scientific Association of Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics, Nat. Rev. Gastroenterol. Hepatol., 18, 649, 10.1038/s41575-021-00440-6 Samuels, 2016, Necrotising enterocolitis and mortality in preterm infants after introduction of probiotics: a quasi-experimental study, Sci. Rep., 6, 31642, 10.1038/srep31643 Scaldaferri, 2016, Role and mechanisms of action of Escherichia coli Nissle 1917 in the maintenance of remission in ulcerative colitis patients: an update, World J. Gastroenterol., 22, 5505, 10.3748/wjg.v22.i24.5505 Schrezenmeir, 2001, Probiotics, prebiotics, and synbiotics—approaching a definition, Am. J. Clin. Nutr., 73, 361S, 10.1093/ajcn/73.2.361s Schröder, 1973, Azo reduction of salicyl-azo-sulphapyridine in germ-free and conventional rats, Xenobiotica, 3, 225, 10.3109/00498257309151518 Semenec, 2023, Cross-protection and cross-feeding between Klebsiella pneumoniae and Acinetobacter baumannii promotes their co-existence, Nat. Commun., 14, 702, 10.1038/s41467-023-36252-2 Shanahan, 2019, Language, numeracy and logic in microbiome science, Nat. Rev. Gastroenterol. Hepatol., 16, 387, 10.1038/s41575-019-0163-5 Shaw, 2010, Mass balance and pharmacokinetics of [14C] telavancin following intravenous administration to healthy male volunteers, Antimicrob. Agents Chemother., 54, 3365, 10.1128/AAC.01750-09 Shaw, 2010, Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease, Am. J. Gastroenterol., 105, 2687, 10.1038/ajg.2010.398 Shenderov, 2013, Metabiotics: novel idea or natural development of probiotic conception, Microb. Ecol. Health Dis., 24 Shyu, 1992, Oral absolute bioavailability and intravenous dose-proportionality of cefprozil in humans, J. Clin. Pharmacol., 32, 798, 10.1002/j.1552-4604.1992.tb03885.x Skandalis, 2021, Environmental spread of antibiotic resistance, Antibiotics, 10, 640, 10.3390/antibiotics10060640 Spyker, 1977, Pharmacokinetics of amoxicillin: dose dependence after intravenous, oral, and intramuscular administration, Antimicrob. Agents Chemother., 11, 132, 10.1128/AAC.11.1.132 Stass, 1999, Pharmacokinetics and elimination of moxifloxacin after oral and intravenous administration in man, J. Antimicrob. Chemother., 43, 83, 10.1093/jac/43.suppl_2.83 Stewart, 2018, Temporal development of the gut microbiome in early childhood from the TEDDY study, Nature, 562, 583, 10.1038/s41586-018-0617-x Thabit, 2020, Antibiotics in the biliary tract: a review of the pharmacokinetics and clinical outcomes of antibiotics penetrating the bile and gallbladder wall, Pharmacotherapy, 40, 672, 10.1002/phar.2431 Ticinesi, 2017, Gut microbiota composition is associated with polypharmacy in elderly hospitalized patients, Sci. Rep., 7, 11102, 10.1038/s41598-017-10734-y Tooke, 2019, β-Lactamases and β-lactamase inhibitors in the 21st century, J. Mol. Biol., 431, 3472, 10.1016/j.jmb.2019.04.002 Trasande, 2013, Infant antibiotic exposures and early-life body mass, Int. J. Obes. (Lond.), 37, 16, 10.1038/ijo.2012.132 Triggs, 1980, Absorption and disposition of ampicillin in the elderly, Eur. J. Clin. Pharmacol., 18, 195, 10.1007/BF00561590 Tsilika, 2022, A four-probiotic preparation for ventilator-associated pneumonia in multi-trauma patients: results of a randomized clinical trial, Int. J. Antimicrob. Agents, 59, 10.1016/j.ijantimicag.2021.106471 Tzikos, 2022, A four-probiotic regime to reduce surgical site infections in multi-trauma patients, Nutrients, 14, 2620, 10.3390/nu14132620 Vehreschild, 2022, An open randomized multicentre Phase 2 trial to assess the safety of DAV132 and its efficacy to protect gut microbiota diversity in hospitalized patients treated with fluoroquinolones, J. Antimicrob. Chemother., 77, 1155, 10.1093/jac/dkab474 Vrieze, 2012, Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome, Gastroenterology, 143, 10.1053/j.gastro.2012.06.031 Wang, 2015, Modulation of gut microbiota during probiotic-mediated attenuation of metabolic syndrome in high fat diet-fed mice, ISME J., 9, 1, 10.1038/ismej.2014.99 Wilson, 2000, Clinical pharmacokinetics of teicoplanin, Clin. Pharmacokinet., 39, 167, 10.2165/00003088-200039030-00001 Wistrand-Yuen, 2018, Evolution of high-level resistance during low-level antibiotic exposure, Nat. Commun., 9, 1599, 10.1038/s41467-018-04059-1 Wlodarska, 2011, Antibiotic treatment alters the colonic mucus layer and predisposes the host to exacerbated Citrobacter rodentium-induced colitis, Infect. Immun., 79, 1536, 10.1128/IAI.01104-10 Yagi, 2021, Association between the prothrombin time–international normalized ratio and concomitant use of antibiotics in warfarin users: focus on type of antibiotic and susceptibility of bacteroides fragilis to antibiotics, Ann. Pharmacother., 55, 157, 10.1177/1060028020940728 Yatsunenko, 2012, Human gut microbiome viewed across age and geography, Nature, 486, 222, 10.1038/nature11053 Zhernakova, 2016, Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity, Science, 352, 565, 10.1126/science.aad3369 Zimmermann, 2010, The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Cô te d'Ivoire, Am. J. Clin. Nutr., 92, 1406, 10.3945/ajcn.110.004564 Zimmermann, 2019, The effect of antibiotics on the composition of the intestinal microbiota - a systematic review, J. Infect., 79, 471, 10.1016/j.jinf.2019.10.008