Advertisement

Current Microbiology

, Volume 76, Issue 3, pp 329–337 | Cite as

Effect Oral Administration Ampicillin on the Ecological Balance of rat Enterococcal gut Microbiota

  • Taha Ahmed BenabbouEmail author
  • Halima Zadi Karam
  • Nour-Eddine Karam
Article
  • 27 Downloads

Abstract

The main objective of this work is to investigate the impact of oral administration of ampicillin on the ecological balance of enterococci in the intestinal microbiota of rats during a treatment and a post-treatment. The results have showed that the treated animals excreted significantly higher percentages of resistant enterococci compared to the control group (P ≤ 0.05) during the treatment and after the treatment. The most predominant species selected after the treatment began were Enterococcus faecium. The MICs for ampicillin for all isolates of E. faecium were 32 to 64 µg/mL, with the exception of two strains (TR1LBMB, TR5LBMB), were found to be highly resistant (MICs ≥ 128 µg/mL). Quantification of ampicillin in faeces by the RT-HPLC showed that the significant increase in the number of ampicillin-resistant enterococci was associated with the gradual accumulation of high levels of unabsorbed ampicillin in the faeces. Our results suggest that ampicillin treatment can now be understood as a side effect contributing to the increase in the number of resistant Enterococcus strains, particularly E. faecium strains, recognized as important nosocomial pathogens.

Notes

Acknowledgements

This study was funded by the Ministry of Higher Education and Scientific Research (MESRS; CNEPRU F01820090065) and General Directorate for Scientific Research and Technological Development (DGRSDT; 012/2000). Authors wish to thank Y. BELLIL and Dr M. MOKHTAR for technical support and helpful discussion. Funding was provided by Laboratory of Microorganisms Biology and Biotechnology.

Compliance with Ethical Standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. 1.
    Agerso H, Friis C (1998) Bioavailability of amoxycillin in pigs. J Vet Pharmacol Ther 21:41–46.  https://doi.org/10.1046/j.1365-2885.1998.00107.x CrossRefGoogle Scholar
  2. 2.
    Blaser M (2011) Antibiotic overuse: stop the killing of beneficial bacteria. Nature 476:393–394.  https://doi.org/10.1038/476393a CrossRefGoogle Scholar
  3. 3.
    Brown-Jaque M, Calero-Cáceres W, Espinal P et al (2018) Antibiotic resistance genes in phage particles isolated from human feces and induced from clinical bacterial isolates. Int J Antimicrob Agents 51:434–442.  https://doi.org/10.1016/j.ijantimicag.2017.11.014 CrossRefGoogle Scholar
  4. 4.
    Carpenter JW, Mashima TY, Rupiper DJ (2001) Exotic animal formulary, 2nd edn. Elsevier-Saunders, PhiladelphiaGoogle Scholar
  5. 5.
    Clinical and Laboratory Standards Institute (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved standard, 9th edn. M07-A9. CLSI, WayneGoogle Scholar
  6. 6.
    D’Argenio V, Salvatore V (2015) The role of the gut microbiome in the healthy adult status. Clin Chim Acta 451:97–102.  https://doi.org/10.1016/j.cca.2015.01.003 CrossRefGoogle Scholar
  7. 7.
    Facklam RR, Collins MD (1989) Identification of Enterococcus species isolated from human infections by a conventional test scheme. J Clin Microbiol 27:731–734.  https://doi.org/10.1016/0168-1605(94)00119-Q Google Scholar
  8. 8.
    Fernández-Hidalgo N, Almirante B, Gavaldà J et al (2013) Ampicillin plus ceftriaxone is as effective as ampicillin plus gentamicin for treating Enterococcus faecalis infective endocarditis. Clin Infect Dis 56:1261–1268.  https://doi.org/10.1093/cid/cit052 CrossRefGoogle Scholar
  9. 9.
    Flemera B, Gaci N, Borrel G et al (2017) Fecal microbiota variation across the lifespan of the healthy laboratory rat. Gut microbes 8:428–439.  https://doi.org/10.1080/19490976.2017.1334033 CrossRefGoogle Scholar
  10. 10.
    Fontana R, Aldegheri M, Ligozzi M et al (1994) Overproduction of a low-affinity penicillin-binding protein and highlevel ampicillin resistance in Enterococcus faecium. Antimicrob Agents Chemother 38:1980–1983CrossRefGoogle Scholar
  11. 11.
    Hitt CM, Nightingale CH, Quintiliani R et al (1997) Streamlining antimicrobial therapy for lower respiratory tract infections. Clin Infect Dis 2:231–237CrossRefGoogle Scholar
  12. 12.
    Jensen GM, Lykkesfeldt J, Frydendahl K et al (2004) Pharmacokinetics of amoxicillin after oral administration in recently weaned piglets with experimentally induced Escherichia coli subtype O149:F4 diarrhea. Am J Vet Res 65:992–995CrossRefGoogle Scholar
  13. 13.
    Johnson SA, Nicolson SW, Jackson S (2004) The effect of different oral antibiotics on the gastrointestinal microflora of a wild rodent (Aethomys namaquensis). Comp Biochem Physiol A 138:475–483CrossRefGoogle Scholar
  14. 14.
    Karimaei S, Sadeghi J, Asadian M et al (2016) Antibacterial potential and genetic profile of Enterococcus faecium strains isolated from human normal flora. Microb Pathog 96:67–71.  https://doi.org/10.1016/j.micpath.2016.05.004 CrossRefGoogle Scholar
  15. 15.
    Kostic AD, Howitt MR, Garrett WS (2013) Exploring host–microbiota interactions in animal models and humans. Genes Dev 27:701–718.  https://doi.org/10.1101/gad.212522.112 CrossRefGoogle Scholar
  16. 16.
    Kumar S, Stecher G, Tamura K (2016) Molecular Evolutionary Genetics Analysis version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefGoogle Scholar
  17. 17.
    Kung K, Hauser BR, Wanner M (1995) Effect of the interval between feeding and drug administration on oral ampicillin absorption in dogs. J Small Anim Pract 36:65–68CrossRefGoogle Scholar
  18. 18.
    Lizumi T, Battaglia T, Ruiz V et al (2017) Gut Microbiome and Antibiotics. Arch Med Res 48:727–734.  https://doi.org/10.1016/j.arcmed.2017.11.004 CrossRefGoogle Scholar
  19. 19.
    Manero A, Blanch AR (1999) Identification of Enterococcus spp. with a biochemical key. Appl Environ Microbiol 65:4425–4430Google Scholar
  20. 20.
    Murray BE (1998) Diversity among multidrug-resistant enterococci. Emerg Infect Dis 4:37–47CrossRefGoogle Scholar
  21. 21.
    Nelson N, Kusmiesz J, Jackson HH et al (1980) Treatment of Salmonella gastroenteritis with ampicillin, amoxicillin, or placebo. Pediatrics 65:1125–1130Google Scholar
  22. 22.
    Nguyen TL, Vieira-Silva S, Liston A et al (2015) How informative is the mouse for human gut microbiota research? Dis Model Mech 8:1–16.  https://doi.org/10.1242/dmm.017400 CrossRefGoogle Scholar
  23. 23.
    Picozzi SC, Casellato S, Rossini M et al (2014) Extended-spectrum beta-lactamase-positive Escherichia coli causing complicated upper urinary tract infection: urologist should act in time. Urol Ann 6:107–112.  https://doi.org/10.4103/0974-7796.130536 CrossRefGoogle Scholar
  24. 24.
    Prichula J, Pereira RI, Wachholz GR et al (2016) Resistance to antimicrobial agents among enterococci isolated from fecal samples of wild marine species in the southern coast of Brazil. Mar Pollut Bull 105:51–57.  https://doi.org/10.1016/j.marpolbul.2016.02.071 CrossRefGoogle Scholar
  25. 25.
    Radhouani H, Pinto L, Coelho C et al (2010) MLST and genetic study of antibiotic resistance and virulence factors in vanA-containing Enterococcus from buzzards (Buteo buteo). Lett Appl Microbiol 50:537–541.  https://doi.org/10.1111/j.1472-765X.2010.02807.x CrossRefGoogle Scholar
  26. 26.
    Radimersky T, Frolkova P, Janoszowska D et al (2010) Antibiotic resistance in faecal bacteria (Escherichia coli, Enterococcus spp.) in feral pigeons. J Appl Microbiol 109:1687–1695.  https://doi.org/10.1111/j.1365-2672.2010.04797.x Google Scholar
  27. 27.
    Ramos S, Igrejas G, Rodrigues J et al (2012) Genetic characterization of antibiotic resistance and virulence factors in vanA-containing enterococci from cattle, sheep and pigs subsequent to the discontinuation of the use of avoparcin. Vet J 193:301–303.  https://doi.org/10.1016/j.tvjl.2011.12.007 CrossRefGoogle Scholar
  28. 28.
    Rice LB, Carias LL, Hutton-Thomas R et al (2001) Penicillin-binding protein 5 and expression of ampicillin resistance in Enterococcus faecium. Antimicrob Agents Chemother 45:1480–1486CrossRefGoogle Scholar
  29. 29.
    Rice LB, Lakticová V, Helfand MS et al (2004) In vitro antienterococcal activity explains associations between exposures to antimicrobial agents and risk of colonization by multiresistant enterococci. J Infect Dis 190:2162–2166.  https://doi.org/10.1086/425580 CrossRefGoogle Scholar
  30. 30.
    Semedo-Lemsaddeka T, Pedrosob NM, Freire D et al (2018) Otter fecal enterococci as general indicators of antimicrobial resistance dissemination in aquatic environments. Ecol Ind 85:1113–1120.  https://doi.org/10.1016/j.ecolind.2017.11.029 CrossRefGoogle Scholar
  31. 31.
    Shah KJ, Cherabuddi K, Shultz J et al (2018) Ampicillin for the treatment of complicated urinary tract infections caused by vancomycin resistant Enterococcus spp (VRE): a single-center university hospital experience. Int J Antimicrob Agents 51:57–61.  https://doi.org/10.1016/j.ijantimicag.2017.06.008 CrossRefGoogle Scholar
  32. 32.
    Sullivan Å, Edlund C, Nord CE (2001) Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis 1:101–114CrossRefGoogle Scholar
  33. 33.
    Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  34. 34.
    Walters MS, Eggers P, Albrecht V et al (2015) Vancomycin-Resistant Staphylococcus aureus-Delaware, 2015. MMWR Morb Mortal Wkly Rep 64:1056.  https://doi.org/10.15585/mmwr.mm6437a6 CrossRefGoogle Scholar
  35. 35.
    Welling PG (1989) Effects of food on drug absorption. Pharmacol Ther 43:425–441.  https://doi.org/10.1016/0163-7258(89)90019-3 CrossRefGoogle Scholar
  36. 36.
    Williams MR, Stedtfeld RD, Guo X et al (2016) Antimicrobial resistance in the environment. Water Environ Res 88:1951–1967.  https://doi.org/10.2175/106143017X15023776270179 CrossRefGoogle Scholar
  37. 37.
    Zoetendal EG, Rajilic-Stojanovic M de Vos WM (2008) High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut 57:1605–1615.  https://doi.org/10.1136/gut.2007.133603 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Taha Ahmed Benabbou
    • 1
    • 2
    Email author
  • Halima Zadi Karam
    • 1
  • Nour-Eddine Karam
    • 1
  1. 1.Laboratory of microorganisms biology and biotechnologyUniversity of Oran1 Ahmed BenbellaOranAlgeria
  2. 2.Department of Biology, Faculty of Nature Science and LifeHassiba Benbouali University of ChlefChlefAlgeria

Personalised recommendations