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Original research
Helicobacter pylori resistance to antibiotics in Europe in 2018 and its relationship to antibiotic consumption in the community
  1. Francis Megraud1,2,
  2. Robin Bruyndonckx3,4,
  3. Samuel Coenen3,
  4. Linda Wittkop5,
  5. Te-Din Huang6,
  6. Martin Hoebeke6,
  7. Lucie Bénéjat2,
  8. Philippe Lehours1,2,
  9. Herman Goossens3,
  10. Youri Glupczynski3,6
  11. The European Helicobacter pylori Antimicrobial Susceptibility Testing Working Group
    1. 1UMR BaRITOn, INSERM U1053, University of Bordeaux, Bordeaux, France
    2. 2National Reference Centre for Helicobacters, Bacteriology Laboratory, Pellegrin University Hospital, Bordeaux, France
    3. 3Laboratory of Medical Microbiology, Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, Belgium
    4. 4Data Science Institute (DSI), Hasselt University, Hasselt, Belgium
    5. 5ISPED, University of Bordeaux, Bordeaux, France
    6. 6Laboratory of Clinical Microbiology and National Reference Centre for Helicobacter pylori, CHU UCL Namur, Mont-Godinne, Belgium
    1. Correspondence to Professor Francis Megraud, UMR BaRITOn, INSERM U1053, University of Bordeaux, Bordeaux, France; francis.megraud{at}chu-bordeaux.fr; Professor Youri Glupczynski, Laboratory of Medical Microbiology, Vaccine & Infectious Disease Institute (VAXINFECTIO), University of Antwerp, Antwerp, Belgium; gyglupczynski{at}gmail.com

    Abstract

    Objective Our aim was to prospectively assess the antibiotic resistance rates in Helicobacter pylori strains in Europe in 2018 and to study the link between antibiotic consumption in the community and H. pylori resistance levels in the different countries.

    Design The proportion of primary antibiotic resistance cases of H. pylori and their corresponding risk factors were investigated in 24 centres from 18 European countries according to a standardised protocol. Data on antibiotic consumption in the community were collected for the period 2008–2017. The link between antibiotic consumption and resistance data was assessed using generalised linear mixed models. The model with the best fit was selected by means of the Akaike Information Criterion.

    Results H. pylori resistance rates for the 1211 adult patients included were 21.4% for clarithromycin, 15.8% for levofloxacin and 38.9% for metronidazole and were significantly higher in Central/Western and Southern than in the Northern European countries.

    The best model fit was obtained for the Poisson distribution using 2013 consumption data. A significant association was found between H. pylori clarithromycin resistance and consumption in the community of macrolides (p=0.0003) and intermediate-acting macrolides (p=0.005), and between levofloxacin resistance and consumption of quinolones (p=0.0002) and second-generation quinolones (p=0.0003).

    Conclusion This study confirms the positive correlation between macrolide and quinolone consumption in the community and corresponding H. pylori resistance in European countries. Hence, H. pylori treatment with clarithromycin and levofloxacin should not be started without susceptibility testing in most European countries.

    • antibiotics
    • drug resistance
    • gastric diseases
    • Helicobacter pylori infection

    Data availability statement

    Data are available on reasonable request at ORCID number: 0000-0002-2481-1612.

    Statistics from Altmetric.com

    Data availability statement

    Data are available on reasonable request at ORCID number: 0000-0002-2481-1612.

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    Footnotes

    • FM and RB contributed equally.

    • Correction notice Thsi article has been corrected since it published Online First. The references have been updated.

    • Collaborators The European Helicobacter pylori Antimicrobial Susceptibility Testing Working Group: A Makristathis (Division for Clinical Microbiology, Department of Laboratory Medicine, Medical University, Vienna, Austria, athanasios.makristathis@meduniwien.ac.at), L Boyanova (Department of Medical Microbiology, Medical University, Sofia, Bulgaria, l.boyanova@hotmail.com), A Tonkic (University Hospital & School of Medicine, Split, Croatia, atonkic@mefst.hr), M Tonkic (University Hospital & School of Medicine, Split, Croatia, mtonkic@mefst.hr), L Andersen (Department of Clinical Microbiology, University Hospital, Copenhagen, Denmark, leifpercivalandersen@outlook.dk), B Blumel (Faculty of Medicine, Institute of Medical Microbiology and Hygiene, Medical Center-University of Freiburg, Freiburg, Germany, benjamin.bluemel@uniklinik-freiburg.de), E Glocker (Faculty of Medicine, Institute of Medical Microbiology and Hygiene, Medical Center-University of Freiburg, Freiburg, Germany, erik-oliver.glocker@uniklinikfreiburg.de), I Tammer (Department of Gastroenterology, Hepatology & Infectious Diseases and Institute of Medical Microbiology, Otto-von-Guericke University, Magdeburg, Germany, Ina.Tammer@med.ovgu.de), A Link (Department of Gastroenterology, Hepatology & Infectious Diseases and Institute of Medical Microbiology, Otto-von-Guericke University, Magdeburg, Germany, Alexander.Link@med.ovgu.de), S Suerbaum (National Reference Centre for Helicobacter pylori, Max von Pettenkofer Institute, LMU Munich Faculty of Medicine, Munich, Germany, Suerbaum@mvp.lmu.de), K Dichtl (National Reference Centre for Helicobacter pylori, Max von Pettenkofer Institute, LMU Munich Faculty of Medicine, Munich, Germany, dichtl@mvp.lmu.de), A Mentis (Laboratory of Medical Microbiology, Hellenic Pasteur Institute, Athens, Greece, mentis@pasteur.gr), B Martinez-Gonzales (Laboratory of Medical Microbiology, Hellenic Pasteur Institute, Athens, Greece, bmartinez@pasteur.gr), S Smith (Department of Clinical Medicine, Trinity College Dublin, Dublin, Ireland, smithsi@tcd.ie), D McNamara (Department of Clinical Medicine, Trinity College Dublin, Dublin, Ireland, mcnamad@tcd.ie), M Pina Dore (Department of Medical, Surgical & Experimental Sciences, University of Sassari, Italy, mpdore@uniss.it), R Monno (Laboratory of Microbiology & Virology, National Institute of Gastroenterology, Bari, Italy, rosa.monno@uniba.it), A Lippolis (Laboratory of Microbiology & Virology, National Institute of Gastroenterology, Bari, Italy, antonio.lippolis@irccsdebellis.it), D Rudzite (Institute of Clinical & Preventive Medicine, University of Latvia, Riga, Latvia, dacerudzite2008@inbox.lv), M Leja (Institute of Clinical & Preventive Medicine, University of Latvia, Riga, Latvia, marcis.leja@lu.lv), J Kupcinskas (Department of Gastroenterology, Academy of Medicine, Lithuanian University of Health Sciences, Kaunas, Lithuania, Juozas.Kupcinskas@lsmuni.lt), K K Melby (Department of Microbiology, Institute of Clinical Medicine, University of Oslo, Norway, k.k.melby@medisin.uio.no), G Gosciniak (Department of Microbiology, Faculty of Medicine, Wroclaw Medical University, Wroclaw, Poland, grazyna.gosciniak@umed.wroc.pl), T M Karpinski (Department of Medical Microbiology, University of Medical Sciences, Poznan, Poland, tkarpin@ump.edu.pl), M Oleastro (National Reference Laboratory for GastroIntestinal Infections, Department of Infectious Diseases, National Institute of Health Dr Ricardo Jorge, Lisbon, Portugal, Monica.Oleastro@insa.min-saude.pt), S Jeverica (National Laboratory of Health, Environment and Food, Maribor, Slovenia, Samo.Jeverica@nlzoh.si), X Calvet (Digestive Diseases Service, Hospital Universitari Parc Tauli, Departament de Medicina, Universitat Autonoma de Barcelona, CIBEREHD. Sabadell, Spain, xavier.calvet.c@gmail.com), M J Ramirez-Lázaro (Digestive Diseases Service, Hospital Universitari Parc Tauli, Departament de Medicina, Universitat Autonoma de Barcelona, CIBEREHD. Sabadell, Spain, mramirezl@tauli.cat), M Montes Ros (Department of Microbiology, Donostia University Hospital IIS Biodonastia, San Sebastian, Spain, MARIAMILAGROSA.MONTESROS@osakidetza.eus), A Morilla (Department of Microbiology, University Hospital Central Asturias, Oviedo, Spain, anamorillamorilla@gmail.com), S Boonstra (Jeroen Bosch Hospital, 'S-Hertogenbosch, The Netherlands, S.Boonstra@jbz.nl) and P M Schneeberger (Jeroen Bosch Hospital, 'S-Hertogenbosch, The Netherlands, P.Schneeberger@jbz.nl).

    • Contributors FM and YG designed the protocol, organised the study, interpreted susceptibility results and wrote the manuscript. RB SC and HG established the correlation with antibiotic consumption. LW studied the risk factors for Helicobacter pylori resistance. T-DH, MH, LB and PL performed the strain control. All made a critical review of the manuscript. FM and YG are the guarantors of the article.

    • Funding Support was received from bioMérieux for ETEST and from Mobidiag for real-time PCR kits, but the companies were not involved in the design nor in the interpretation of the results. We are thankful for their support.

    • Disclaimer The views and opinions of the authors expressed herein do not necessarily state or reflect those of European Centre for Disease Prevention and Control (ECDC). The accuracy of the authors’ statistical analysis and the findings they report are not the responsibility of ECDC. ECDC is not responsible for conclusions or opinions drawn from the data provided. ECDC is not responsible for the correctness of the data and for data management, data merging and data collection after provision of the data. ECDC shall not be held liable for improper or incorrect use of the data.

    • Competing interests None declared.

    • Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

    • Provenance and peer review Not commissioned; externally peer reviewed.

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