Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)

Matteo Boattini; Gabriele Bianco; Paulo Bastos; Viktoria Eirini Mavromanolaki; Sofia Maraki; Anastasia Spiliopoulou; Vasileios Kakouris; Yordan Kalchev; Ana Budimir; Branka Bedenić; Zana Rubic; Monica Licker; Corina Musuroi; Emese Juhász; Katalin Kristóf; Mateja Pirs; Ivana Velimirovic; Michael Berktold; Adriána Liptáková; Adriana Krajcikova; Pavel Drevinek; Anezka Gryndlerova; Monika Brzychczy-Wloch; Aldona Olechowska-Jarząb; Filip Bielec; Małgorzata Brauncajs; Edyta Podsiadly; Grażyna Nurzyńska; Patrycja Zalas-Więcek; Kristian Riesbeck; Hanna Sofia Andersson; Tone Tønjum; Johan Christian Berild; Truls Michael Leegaard; Asger Nellemann Rasmussen; Kristian Schønning; Stefan Glöckner; Jürgen Rödel; Mohamed Tarek Badr; Georg Alexander Häcker; Denise Stark; Axel Hamprecht; Anna Dudakova; Jonathan Jantsch; Stefano Mancini; Chantal Quiblier; Damien Jacot; Gilbert Greub; Tiziano Ferniani; Simone Ambretti; Maddalena Calvo; Stefania Stefani; Rogier Schade; Erlangga Yusuf; Stefanie van Kleef van Koeveringe; Sarah Vandamme; Alexia Verroken; Hector Rodriguez-Villalobos; François Duigou; Stéphane Corvec; Pauline Floch; Clémence Massip; Delphine Chainier; Olivier Barraud; Marie Bossuète Louissaint; Assaf Mizrahi; Saied Ali; Maeve Doyle; Clarice Egan; Sinead McNicholas; Javier Colomina-Rodriguez; Ignacio Torres; Raul Gilarranz Luengo; Maria Nieves Larrosa Escartín; Maria Belen Viñado Perez; Ana Verónica Halperin; Sergio Fuente García; Rafael Cantón; Miguel Seruca; Vasco Santos Mendes; Dinah Carvalho; Rossana Cavallo; José Melo Cristino; Cristina Costa

doi:10.1016/j.ijantimicag.2025.107478

Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)

Matteo Boattini^*
, Gabriele Bianco
, Paulo Bastos
, Viktoria Eirini Mavromanolaki
, Sofia Maraki
, Anastasia Spiliopoulou
, Vasileios Kakouris
, Yordan Kalchev
, Ana Budimir
, Branka Bedenić
, Zana Rubic
, Monica Licker
, Corina Musuroi
, Emese Juhász
, Katalin Kristóf
, Mateja Pirs
, Ivana Velimirovic
, Michael Berktold
, Adriána Liptáková
, Adriana Krajcikova

Pavel Drevinek, Anezka Gryndlerova, Monika Brzychczy-Wloch, Aldona Olechowska-Jarząb, Filip Bielec, Małgorzata Brauncajs, Edyta Podsiadly, Grażyna Nurzyńska, Patrycja Zalas-Więcek, Kristian Riesbeck, Hanna Sofia Andersson, Tone Tønjum, Johan Christian Berild, Truls Michael Leegaard, Asger Nellemann Rasmussen, Kristian Schønning, Stefan Glöckner, Jürgen Rödel, Mohamed Tarek Badr, Georg Alexander Häcker, Denise Stark, Axel Hamprecht, Anna Dudakova, Jonathan Jantsch, Stefano Mancini, Chantal Quiblier, Damien Jacot, Gilbert Greub, Tiziano Ferniani, Simone Ambretti, Maddalena Calvo, Stefania Stefani, Rogier Schade, Erlangga Yusuf, Stefanie van Kleef van Koeveringe, Sarah Vandamme, Alexia Verroken, Hector Rodriguez-Villalobos, François Duigou, Stéphane Corvec, Pauline Floch, Clémence Massip, Delphine Chainier, Olivier Barraud, Marie Bossuète Louissaint, Assaf Mizrahi, Saied Ali, Maeve Doyle, Clarice Egan, Sinead McNicholas, Javier Colomina-Rodriguez, Ignacio Torres, Raul Gilarranz Luengo, Maria Nieves Larrosa Escartín, Maria Belen Viñado Perez, Ana Verónica Halperin, Sergio Fuente García, Rafael Cantón, Miguel Seruca, Vasco Santos Mendes, Dinah Carvalho, Rossana Cavallo, José Melo Cristino, Cristina Costa

^*Corresponding author for this work

Medical Microbiology & Infectious Diseases

Research output: Contribution to journal › Article › Academic › peer-review

3 Citations (Scopus)

6 Downloads (Pure)

Abstract

Introduction:

Despite being implicated in a wide spectrum of community- and healthcare-acquired infections, anaerobes have not yet been incorporated into systematic surveillance programs in Europe.

Methods:

We conducted a multicentre retrospective observational study analysing all anaerobic strains isolated from blood cultures in 44 European Hospital Centres over a 4-y period (2020–2023). Diagnostic approach, epidemiology, and antimicrobial susceptibility according to EUCAST v. 15.0 were investigated.

Results:

Our study included 14,527 anaerobes, most of which were Gram-positive (45%) or Gram-negative (40%) bacilli. MALDI-TOF coupled to mass spectrometry was the most widely used tool for species identification (98%). Antimicrobial susceptibility testing was performed in the vast majority of centres, using mostly gradient diffusion strip (77%) and disk diffusion (45%) methods according to EUCAST guidelines. The most prevalent species were Cutibacterium acnes (18.7%), Bacteroides fragilis (16.3%), Clostridium perfringens (5.3%), Bacteroides thetaiotaomicron (4.2%), Fusobacterium nucleatum (3.5%), and Parvimonas micra (3.4%). C. acnes showed high resistance to benzylpenicillin (18%), clindamycin (39%), and imipenem (19% and 13% by MIC methods and disk diffusion, respectively). B. fragilis showed high resistance to amoxicillin/clavulanate (24%), piperacillin/tazobactam (22% and 14% by MIC methods and disk diffusion, respectively), clindamycin (22% by both MIC methods and disk diffusion), meropenem (13%), and metronidazole (10%, only by disk diffusion). A similar resistance pattern was observed in B. thetaiotaomicron, Bacteroides ovatus, and Parabacteroides distasonis. C. perfringens showed high resistance to clindamycin (69% and 45% by MIC methods and disk diffusion, respectively), while benzylpenicillin and metronidazole maintained over 90% activity. F. nucleatum showed high resistance to benzylpenicillin (11%), while Fusobacterium necrophorum showed alarming rates of resistance to clindamycin (12%), meropenem (16%) and metronidazole (11%).

Conclusions:

This study presented an up-to-date analysis of the diagnostics and epidemiology of anaerobic bacteria in Europe, providing insights for future comparative analyses and the development of antimicrobial diagnostic and management strategies, as well as the optimization of current antibiotic treatments.

Original language	English
Article number	107478
Journal	International Journal of Antimicrobial Agents
Volume	65
Issue number	6
DOIs	https://doi.org/10.1016/j.ijantimicag.2025.107478
Publication status	Published - Jun 2025

Bibliographical note

Publisher Copyright:
© 2025 The Authors

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)Final published version, 3.73 MBLicence: CC BY

Cite this

Boattini, M., Bianco, G., Bastos, P., Mavromanolaki, V. E., Maraki, S., Spiliopoulou, A., Kakouris, V., Kalchev, Y., Budimir, A., Bedenić, B., Rubic, Z., Licker, M., Musuroi, C., Juhász, E., Kristóf, K., Pirs, M., Velimirovic, I., Berktold, M., Liptáková, A., ... Costa, C. (2025). Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE). International Journal of Antimicrobial Agents, 65(6), Article 107478. https://doi.org/10.1016/j.ijantimicag.2025.107478

@article{c27e089c944e46e19fafc9b4ba9d0aed,

title = "Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)",

abstract = "Introduction:Despite being implicated in a wide spectrum of community- and healthcare-acquired infections, anaerobes have not yet been incorporated into systematic surveillance programs in Europe. Methods: We conducted a multicentre retrospective observational study analysing all anaerobic strains isolated from blood cultures in 44 European Hospital Centres over a 4-y period (2020–2023). Diagnostic approach, epidemiology, and antimicrobial susceptibility according to EUCAST v. 15.0 were investigated. Results: Our study included 14,527 anaerobes, most of which were Gram-positive (45\%) or Gram-negative (40\%) bacilli. MALDI-TOF coupled to mass spectrometry was the most widely used tool for species identification (98\%). Antimicrobial susceptibility testing was performed in the vast majority of centres, using mostly gradient diffusion strip (77\%) and disk diffusion (45\%) methods according to EUCAST guidelines. The most prevalent species were Cutibacterium acnes (18.7\%), Bacteroides fragilis (16.3\%), Clostridium perfringens (5.3\%), Bacteroides thetaiotaomicron (4.2\%), Fusobacterium nucleatum (3.5\%), and Parvimonas micra (3.4\%). C. acnes showed high resistance to benzylpenicillin (18\%), clindamycin (39\%), and imipenem (19\% and 13\% by MIC methods and disk diffusion, respectively). B. fragilis showed high resistance to amoxicillin/clavulanate (24\%), piperacillin/tazobactam (22\% and 14\% by MIC methods and disk diffusion, respectively), clindamycin (22\% by both MIC methods and disk diffusion), meropenem (13\%), and metronidazole (10\%, only by disk diffusion). A similar resistance pattern was observed in B. thetaiotaomicron, Bacteroides ovatus, and Parabacteroides distasonis. C. perfringens showed high resistance to clindamycin (69\% and 45\% by MIC methods and disk diffusion, respectively), while benzylpenicillin and metronidazole maintained over 90\% activity. F. nucleatum showed high resistance to benzylpenicillin (11\%), while Fusobacterium necrophorum showed alarming rates of resistance to clindamycin (12\%), meropenem (16\%) and metronidazole (11\%). Conclusions: This study presented an up-to-date analysis of the diagnostics and epidemiology of anaerobic bacteria in Europe, providing insights for future comparative analyses and the development of antimicrobial diagnostic and management strategies, as well as the optimization of current antibiotic treatments.",

author = "Matteo Boattini and Gabriele Bianco and Paulo Bastos and Mavromanolaki, \{Viktoria Eirini\} and Sofia Maraki and Anastasia Spiliopoulou and Vasileios Kakouris and Yordan Kalchev and Ana Budimir and Branka Bedeni{\'c} and Zana Rubic and Monica Licker and Corina Musuroi and Emese Juh{\'a}sz and Katalin Krist{\'o}f and Mateja Pirs and Ivana Velimirovic and Michael Berktold and Adri{\'a}na Lipt{\'a}kov{\'a} and Adriana Krajcikova and Pavel Drevinek and Anezka Gryndlerova and Monika Brzychczy-Wloch and Aldona Olechowska-Jarz{\c a}b and Filip Bielec and Ma{\l}gorzata Brauncajs and Edyta Podsiadly and Gra{\.z}yna Nurzy{\'n}ska and Patrycja Zalas-Wi{\c e}cek and Kristian Riesbeck and Andersson, \{Hanna Sofia\} and Tone T{\o}njum and Berild, \{Johan Christian\} and Leegaard, \{Truls Michael\} and Rasmussen, \{Asger Nellemann\} and Kristian Sch{\o}nning and Stefan Gl{\"o}ckner and J{\"u}rgen R{\"o}del and Badr, \{Mohamed Tarek\} and H{\"a}cker, \{Georg Alexander\} and Denise Stark and Axel Hamprecht and Anna Dudakova and Jonathan Jantsch and Stefano Mancini and Chantal Quiblier and Damien Jacot and Gilbert Greub and Tiziano Ferniani and Simone Ambretti and Maddalena Calvo and Stefania Stefani and Rogier Schade and Erlangga Yusuf and Koeveringe, \{Stefanie van Kleef van\} and Sarah Vandamme and Alexia Verroken and Hector Rodriguez-Villalobos and Fran{\c c}ois Duigou and St{\'e}phane Corvec and Pauline Floch and Cl{\'e}mence Massip and Delphine Chainier and Olivier Barraud and Louissaint, \{Marie Bossu{\`e}te\} and Assaf Mizrahi and Saied Ali and Maeve Doyle and Clarice Egan and Sinead McNicholas and Javier Colomina-Rodriguez and Ignacio Torres and Luengo, \{Raul Gilarranz\} and Escart{\'i}n, \{Maria Nieves Larrosa\} and Perez, \{Maria Belen Vi{\~n}ado\} and Halperin, \{Ana Ver{\'o}nica\} and Garc{\'i}a, \{Sergio Fuente\} and Rafael Cant{\'o}n and Miguel Seruca and Mendes, \{Vasco Santos\} and Dinah Carvalho and Rossana Cavallo and Cristino, \{Jos{\'e} Melo\} and Cristina Costa",

note = "Publisher Copyright: {\textcopyright} 2025 The Authors",

year = "2025",

month = jun,

doi = "10.1016/j.ijantimicag.2025.107478",

language = "English",

volume = "65",

journal = "International Journal of Antimicrobial Agents",

issn = "0924-8579",

publisher = "Elsevier",

number = "6",

}

Boattini, M, Bianco, G, Bastos, P, Mavromanolaki, VE, Maraki, S, Spiliopoulou, A, Kakouris, V, Kalchev, Y, Budimir, A, Bedenić, B, Rubic, Z, Licker, M, Musuroi, C, Juhász, E, Kristóf, K, Pirs, M, Velimirovic, I, Berktold, M, Liptáková, A, Krajcikova, A, Drevinek, P, Gryndlerova, A, Brzychczy-Wloch, M, Olechowska-Jarząb, A, Bielec, F, Brauncajs, M, Podsiadly, E, Nurzyńska, G, Zalas-Więcek, P, Riesbeck, K, Andersson, HS, Tønjum, T, Berild, JC, Leegaard, TM, Rasmussen, AN, Schønning, K, Glöckner, S, Rödel, J, Badr, MT, Häcker, GA, Stark, D, Hamprecht, A, Dudakova, A, Jantsch, J, Mancini, S, Quiblier, C, Jacot, D, Greub, G, Ferniani, T, Ambretti, S, Calvo, M, Stefani, S, Schade, R, Yusuf, E, Koeveringe, SVKV, Vandamme, S, Verroken, A, Rodriguez-Villalobos, H, Duigou, F, Corvec, S, Floch, P, Massip, C, Chainier, D, Barraud, O, Louissaint, MB, Mizrahi, A, Ali, S, Doyle, M, Egan, C, McNicholas, S, Colomina-Rodriguez, J, Torres, I, Luengo, RG, Escartín, MNL, Perez, MBV, Halperin, AV, García, SF, Cantón, R, Seruca, M, Mendes, VS, Carvalho, D, Cavallo, R, Cristino, JM & Costa, C 2025, 'Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)', International Journal of Antimicrobial Agents, vol. 65, no. 6, 107478. https://doi.org/10.1016/j.ijantimicag.2025.107478

TY - JOUR

T1 - Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)

AU - Boattini, Matteo

AU - Bianco, Gabriele

AU - Bastos, Paulo

AU - Mavromanolaki, Viktoria Eirini

AU - Maraki, Sofia

AU - Spiliopoulou, Anastasia

AU - Kakouris, Vasileios

AU - Kalchev, Yordan

AU - Budimir, Ana

AU - Bedenić, Branka

AU - Rubic, Zana

AU - Licker, Monica

AU - Musuroi, Corina

AU - Juhász, Emese

AU - Kristóf, Katalin

AU - Pirs, Mateja

AU - Velimirovic, Ivana

AU - Berktold, Michael

AU - Liptáková, Adriána

AU - Krajcikova, Adriana

AU - Drevinek, Pavel

AU - Gryndlerova, Anezka

AU - Brzychczy-Wloch, Monika

AU - Olechowska-Jarząb, Aldona

AU - Bielec, Filip

AU - Brauncajs, Małgorzata

AU - Podsiadly, Edyta

AU - Nurzyńska, Grażyna

AU - Zalas-Więcek, Patrycja

AU - Riesbeck, Kristian

AU - Andersson, Hanna Sofia

AU - Tønjum, Tone

AU - Berild, Johan Christian

AU - Leegaard, Truls Michael

AU - Rasmussen, Asger Nellemann

AU - Schønning, Kristian

AU - Glöckner, Stefan

AU - Rödel, Jürgen

AU - Badr, Mohamed Tarek

AU - Häcker, Georg Alexander

AU - Stark, Denise

AU - Hamprecht, Axel

AU - Dudakova, Anna

AU - Jantsch, Jonathan

AU - Mancini, Stefano

AU - Quiblier, Chantal

AU - Jacot, Damien

AU - Greub, Gilbert

AU - Ferniani, Tiziano

AU - Ambretti, Simone

AU - Calvo, Maddalena

AU - Stefani, Stefania

AU - Schade, Rogier

AU - Yusuf, Erlangga

AU - Koeveringe, Stefanie van Kleef van

AU - Vandamme, Sarah

AU - Verroken, Alexia

AU - Rodriguez-Villalobos, Hector

AU - Duigou, François

AU - Corvec, Stéphane

AU - Floch, Pauline

AU - Massip, Clémence

AU - Chainier, Delphine

AU - Barraud, Olivier

AU - Louissaint, Marie Bossuète

AU - Mizrahi, Assaf

AU - Ali, Saied

AU - Doyle, Maeve

AU - Egan, Clarice

AU - McNicholas, Sinead

AU - Colomina-Rodriguez, Javier

AU - Torres, Ignacio

AU - Luengo, Raul Gilarranz

AU - Escartín, Maria Nieves Larrosa

AU - Perez, Maria Belen Viñado

AU - Halperin, Ana Verónica

AU - García, Sergio Fuente

AU - Cantón, Rafael

AU - Seruca, Miguel

AU - Mendes, Vasco Santos

AU - Carvalho, Dinah

AU - Cavallo, Rossana

AU - Cristino, José Melo

AU - Costa, Cristina

PY - 2025/6

Y1 - 2025/6

N2 - Introduction:Despite being implicated in a wide spectrum of community- and healthcare-acquired infections, anaerobes have not yet been incorporated into systematic surveillance programs in Europe. Methods: We conducted a multicentre retrospective observational study analysing all anaerobic strains isolated from blood cultures in 44 European Hospital Centres over a 4-y period (2020–2023). Diagnostic approach, epidemiology, and antimicrobial susceptibility according to EUCAST v. 15.0 were investigated. Results: Our study included 14,527 anaerobes, most of which were Gram-positive (45%) or Gram-negative (40%) bacilli. MALDI-TOF coupled to mass spectrometry was the most widely used tool for species identification (98%). Antimicrobial susceptibility testing was performed in the vast majority of centres, using mostly gradient diffusion strip (77%) and disk diffusion (45%) methods according to EUCAST guidelines. The most prevalent species were Cutibacterium acnes (18.7%), Bacteroides fragilis (16.3%), Clostridium perfringens (5.3%), Bacteroides thetaiotaomicron (4.2%), Fusobacterium nucleatum (3.5%), and Parvimonas micra (3.4%). C. acnes showed high resistance to benzylpenicillin (18%), clindamycin (39%), and imipenem (19% and 13% by MIC methods and disk diffusion, respectively). B. fragilis showed high resistance to amoxicillin/clavulanate (24%), piperacillin/tazobactam (22% and 14% by MIC methods and disk diffusion, respectively), clindamycin (22% by both MIC methods and disk diffusion), meropenem (13%), and metronidazole (10%, only by disk diffusion). A similar resistance pattern was observed in B. thetaiotaomicron, Bacteroides ovatus, and Parabacteroides distasonis. C. perfringens showed high resistance to clindamycin (69% and 45% by MIC methods and disk diffusion, respectively), while benzylpenicillin and metronidazole maintained over 90% activity. F. nucleatum showed high resistance to benzylpenicillin (11%), while Fusobacterium necrophorum showed alarming rates of resistance to clindamycin (12%), meropenem (16%) and metronidazole (11%). Conclusions: This study presented an up-to-date analysis of the diagnostics and epidemiology of anaerobic bacteria in Europe, providing insights for future comparative analyses and the development of antimicrobial diagnostic and management strategies, as well as the optimization of current antibiotic treatments.

AB - Introduction:Despite being implicated in a wide spectrum of community- and healthcare-acquired infections, anaerobes have not yet been incorporated into systematic surveillance programs in Europe. Methods: We conducted a multicentre retrospective observational study analysing all anaerobic strains isolated from blood cultures in 44 European Hospital Centres over a 4-y period (2020–2023). Diagnostic approach, epidemiology, and antimicrobial susceptibility according to EUCAST v. 15.0 were investigated. Results: Our study included 14,527 anaerobes, most of which were Gram-positive (45%) or Gram-negative (40%) bacilli. MALDI-TOF coupled to mass spectrometry was the most widely used tool for species identification (98%). Antimicrobial susceptibility testing was performed in the vast majority of centres, using mostly gradient diffusion strip (77%) and disk diffusion (45%) methods according to EUCAST guidelines. The most prevalent species were Cutibacterium acnes (18.7%), Bacteroides fragilis (16.3%), Clostridium perfringens (5.3%), Bacteroides thetaiotaomicron (4.2%), Fusobacterium nucleatum (3.5%), and Parvimonas micra (3.4%). C. acnes showed high resistance to benzylpenicillin (18%), clindamycin (39%), and imipenem (19% and 13% by MIC methods and disk diffusion, respectively). B. fragilis showed high resistance to amoxicillin/clavulanate (24%), piperacillin/tazobactam (22% and 14% by MIC methods and disk diffusion, respectively), clindamycin (22% by both MIC methods and disk diffusion), meropenem (13%), and metronidazole (10%, only by disk diffusion). A similar resistance pattern was observed in B. thetaiotaomicron, Bacteroides ovatus, and Parabacteroides distasonis. C. perfringens showed high resistance to clindamycin (69% and 45% by MIC methods and disk diffusion, respectively), while benzylpenicillin and metronidazole maintained over 90% activity. F. nucleatum showed high resistance to benzylpenicillin (11%), while Fusobacterium necrophorum showed alarming rates of resistance to clindamycin (12%), meropenem (16%) and metronidazole (11%). Conclusions: This study presented an up-to-date analysis of the diagnostics and epidemiology of anaerobic bacteria in Europe, providing insights for future comparative analyses and the development of antimicrobial diagnostic and management strategies, as well as the optimization of current antibiotic treatments.

UR - https://www.scopus.com/pages/publications/105001051935

U2 - 10.1016/j.ijantimicag.2025.107478

DO - 10.1016/j.ijantimicag.2025.107478

M3 - Article

C2 - 40024606

AN - SCOPUS:105001051935

SN - 0924-8579

VL - 65

JO - International Journal of Antimicrobial Agents

JF - International Journal of Antimicrobial Agents

IS - 6

M1 - 107478

ER -

Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE)

Abstract

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