A European survey on anaerobes from paediatric blood cultures: a comparative analysis with adults
Status Publisher Language English Country Germany Media print-electronic
Document type Journal Article
PubMed
40537731
DOI
10.1007/s10096-025-05185-7
PII: 10.1007/s10096-025-05185-7
Knihovny.cz E-resources
- Keywords
- Bacteroides spp., Cutibacterium spp., Anaerobes, Antimicrobial resistance, Paediatrics, Sepsis,
- Publication type
- Journal Article MeSH
Infections caused by anaerobes are common in children. However, limited data are available on bloodstream infections caused by these bacteria in Europe. A multicentre retrospective observational study was conducted over a 4-year period (2020-2023) across 44 European hospitals to analyze all anaerobes isolated from blood cultures. The study examined the epidemiology and antimicrobial resistance profiles of anaerobes identified in paediatric patients, comparing the findings with those observed in adults. Among the 14,527 total anaerobic isolates, 186 (1.3%) were detected from paediatric patients. These were predominantly Gram-positive (70%) and Gram-negative (22%) bacilli. The most prevalent species in paediatric patients were Cutibacterium acnes (24.7%), Schaalia odontolytica (9.7%), Actinomyces oris (8.1%), and Bacteroides fragilis (7.5%). Relative feature importance based on the mean SHAP (SHapley Additive exPlanations) values distinguished paediatric patients and adults based on their antibiotic resistance patterns with high accuracy. Compared to those from adult patients, Gram-positive bacilli detected in paediatric samples displayed higher resistance rates for meropenem (15% vs. 9%), metronidazole (52% vs. 24%), and vancomycin (27% vs. 6%), and lower resistance to benzylpenicillin (11% vs. 17%), amoxicillin/clavulanate (9% vs. 17%), and clindamycin (30% vs. 36%). Gram-negative bacilli in paediatric samples displayed lower resistance to benzylpenicillin (18% vs. 29%), piperacillin/tazobactam (26% vs. 33%), and clindamycin (20% vs. 27%), and they were highly susceptible to imipenem, meropenem, and metronidazole as those detected in adult patients. Bacteroides species detected in paediatric and adult patients displayed high resistance to piperacillin/tazobactam (33% vs. 39%) and clindamycin (38% vs. 29%), while they were highly susceptible to metronidazole. Compared to those from adult samples, Cutibacterium acnes in paediatric patients displayed lower resistance to benzylpenicillin (none vs. 15%) and clindamycin (17% vs. 29%). The comparison of species and susceptibility profiles of anaerobes detected in paediatric and adult patients highlighted the importance of reporting antimicrobial susceptibility surveillance data by age group.
Amsterdam UMC Department of Medical Microbiology and Infection Prevention Amsterdam The Netherlands
BIOSS Centre for Biological Signaling Studies University of Freiburg 79104 Freiburg Germany
CIBER de Enfermedades Infecciosas Instituto de Salud Carlos 3 Madrid Spain
Department of Biomedical and Biotechnological Sciences University of Catania 95123 Catania Italy
Department of Clinical Microbiology Cliniques Universitaires Saint Luc Brussels Belgium
Department of Clinical Microbiology Copenhagen University Hospital Rigshospitale Copenhagen Denmark
Department of Clinical Microbiology University Hospital Antwerp Edegem Belgium
Department of Clinical Microbiology University Hospital of Split Split Croatia
Department of Clinical Microbiology Vall d'Hebron Barcelona Hospital Campus Barcelona Spain
Department of Clinical Pathology Centro Hospitalar Universitário de Lisboa Central Lisbon Portugal
Department of Genetics and Microbiology Universitat Autònoma de Barcelona Bellaterra Spain
Department of Medical and Clinical Pharmacology Toulouse University Hospital Toulouse France
Department of Medical and Surgical Sciences University of Bologna 40126 Bologna Italy
Department of Microbiology and Infection Control Akershus University Hospital Lørenskog Norway
Department of Microbiology and Laboratory Medical Immunology Medical University of Lodz Lodz Poland
Department of Microbiology Medical School University of Patras Patras Greece
Department of Microbiology Oslo University Hospital Oslo Norway
Department of Microbiology St Vincent's University Hospital Elm Park Dublin D04 T6 F4 Ireland
Department of Microbiology University of Oslo Oslo Norway
Department of Paediatrics Agios Nikolaos General Hospital 721 00 Crete Greece
Department of Public Health and Paediatrics University of Torino Turin Italy
Faculdade de Medicina Universidade de Lisboa Lisbon Portugal
Infectious Diseases Service Lausanne University Hospital Lausanne Switzerland
INSERM Immunology and New Concepts in ImmunoTherapy INCIT UMR 1302 Nantes Université Nantes France
Institut Micalis UMR 1319 Université Paris Saclay INRAe AgroParisTech Châtenay Malabry France
Institute of Hygiene and Medical Microbiology Medical University of Innsbruck 6020 Innsbruck Austria
Institute of Laboratory Medicine Semmelweis University Budapest Hungary
Institute of Medical Microbiology and Virology Klinikum Oldenburg Oldenburg Germany
Institute of Medical Microbiology University of Zurich Zurich Switzerland
Laboratoire de Bactériologie Hygiène CHU de Toulouse Université de Toulouse Toulouse France
Laboratory of Microbiology University Hospital St George Plovdiv 4000 Bulgaria
Microbiology Service University Clinical Hospital of Valencia Valencia Spain
Microbiology Unit IRCCS Azienda Ospedaliero Universitaria di Bologna Bologna Italy
Neonatal Intensive Care Unit IRCCS AOU Bologna 40139 Bologna Italy
Regional Department of Clinical Microbiology University Hospital Waterford Waterford Ireland
Service de Microbiologie Clinique Hôpitaux Saint Joseph and Marie Lannelongue Paris France
Service of Microbiology Hospital Universitario de Gran Canaria Dr Negrín Las Palmas Spain
Serviço de Patologia Clínica Centro Hospitalar Universitário Lisboa Norte Lisbon Portugal
U O C Laboratory Analysis Unit A O U Policlinico San Marco Via S Sofia 78 95123 Catania Italy
Université Limoges INSERM CHU Limoges UMR 1092 Limoges France
See more in PubMed
Brook I (2024) Overview of anaerobic infections in children and their treatment. J Infect Chemother 30:1104–1113. https://doi.org/10.1016/j.jiac.2024.07.014 PubMed DOI
Freedman SB, Roosevelt GE (2004) Utility of anaerobic blood cultures in a pediatric emergency department. Pediatr Emerg Care 20:433–436. https://doi.org/10.1097/01.pec.0000132215.57976.99 PubMed DOI
Goldstein EJ (1996) Anaerobic bacteremia. Clin Infect Dis 23:S97–101. https://doi.org/10.1093/clinids/23.supplement_1.s97 PubMed DOI
Dien Bard J, McElvania TE (2016) Diagnosis of Bloodstream Infections in Children. J Clin Microbiol 54:1418–1424. https://doi.org/10.1128/JCM.02919-15 PubMed DOI PMC
Dunne WM Jr, Tillman J, Havens PL (1994) Assessing the need for anaerobic medium for the recovery of clinically significant blood culture isolates in children. Pediatr Infect Dis J 13:203–206. https://doi.org/10.1097/00006454-199403000-00007 PubMed DOI
Iwata K, Takahashi M (2008) Is anaerobic blood culture necessary? If so, who needs it? Am J Med Sci 336:58–63. https://doi.org/10.1097/MAJ.0b013e31815dca24 PubMed DOI
Zaidi AK, Knaut AL, Mirrett S, Reller LB (1995) Value of routine anaerobic blood cultures for pediatric patients. J Pediatr 127:263–268. https://doi.org/10.1016/s0022-3476(95)70305-5 PubMed DOI
Lee CS, Hwang B, Chung RL, Tang RB (2000) The assessment of anaerobic blood culture in children. J Microbiol Immunol Infect 33:49–52 PubMed
Paisley JW, Lauer BA (1994) Pediatric blood cultures. Clin Lab Med 14:17–30 PubMed DOI
Baron EJ, Miller JM, Weinstein MP, Richter SS, Gilligan PH, Thomson RB Jr et al (2013) A guide to utilization of the microbiology laboratory for diagnosis of infectious diseases: 2013 recommendations by the Infectious Diseases Society of America (IDSA) and the American Society for Microbiology (ASM)(a). Clin Infect Dis 57:e22–e121. https://doi.org/10.1093/cid/cit278 PubMed DOI PMC
Miller JM, Binnicker MJ, Campbell S, Carroll KC, Chapin KC, Gilligan PH et al (2018) A Guide to Utilization of the Microbiology Laboratory for Diagnosis of Infectious Diseases: 2018 Update by the Infectious Diseases Society of America and the American Society for Microbiology. Clin Infect Dis 67:e1–e94. https://doi.org/10.1093/cid/ciy381 PubMed DOI
Shoji K, Komuro H, Watanabe Y, Miyairi I (2013) The utility of anaerobic blood culture in detecting facultative anaerobic bacteremia in children. Diagn Microbiol Infect Dis 76:409–412. https://doi.org/10.1016/j.diagmicrobio.2013.05.003 PubMed DOI
Messbarger N, Neemann K (2018) Role of Anaerobic Blood Cultures in Neonatal Bacteremia. J Pediatric Infect Dis Soc 7:e65–e69. https://doi.org/10.1093/jpids/pix088 PubMed DOI
Dien Bard J, Chang TP, Yee R, Manshadi K, Lichtenfeld N, Choi HJ et al (2020) The Addition of Anaerobic Blood Cultures for Pediatric Patients with Concerns for Bloodstream Infections: Prevalence and Time to Positive Cultures. J Clin Microbiol 58:e01844–e1919. https://doi.org/10.1128/JCM.01844-19 PubMed DOI PMC
Ransom EM, Burnham CD (2022) Routine Use of Anaerobic Blood Culture Bottles for Specimens Collected from Adults and Children Enhances Microorganism Recovery and Improves Time to Positivity. J Clin Microbiol 60:e0050022. https://doi.org/10.1128/jcm.00500-22 PubMed DOI
Kato H, Shoji K, Jinguji M, Nishimura N, Nakagawa S, Miyairi I (2023) The Utility of Performing Anaerobic Blood Cultures in Pediatric Intensive Care Units. J Pediatric Infect Dis Soc 12:372–378. https://doi.org/10.1093/jpids/piad037 PubMed DOI
Noh GY, Park YS, Kim SH, Song SA, Shin JH (2023) Clinical usefulness of anaerobic blood culture in pediatric patients with bacteremia. Anaerobe 84:102804. https://doi.org/10.1016/j.anaerobe.2023.102804 PubMed DOI
Gottschalk A, Coggins S, Dhudasia MB, Flannery DD, Healy T, Puopolo KM et al (2024) Utility of Anaerobic Blood Cultures in Neonatal Sepsis Evaluation. J Pediatric Infect Dis Soc 13:406–412. https://doi.org/10.1093/jpids/piae056 PubMed DOI
Thé T, Curfman A, Burnham CD, Hayes E, Schnadower D; with the Pediatric Emergency Medicine Collaborative Research Committee (PEM-CRC) (2019) Pediatric Anaerobic Blood Culture Practices in Industrialized Countries. J Appl Lab Med 3:553–558. https://doi.org/10.1373/jalm.2018.027128
Hajjar N, Ting JY, Shah PS, Lee KS, Dunn MS, Srigley JA et al (2023) Blood culture collection practices in NICU. Nat Survey Paediatr Child Health 15(28):166–171. https://doi.org/10.1093/pch/pxac112 DOI
Dubreuil LJ (2024) Fifty years devoted to anaerobes: historical, lessons, and highlights. Eur J Clin Microbiol Infect Dis 43:1–15. https://doi.org/10.1007/s10096-023-04708-4 PubMed DOI
Buttery JP. Blood cultures in newborns and children: optimising an everyday test. Arch Dis Child Fetal Neonatal Ed 87:F25–8. https://doi.org/10.1136/fn.87.1.f25
Salonen JH, Eerola E, Meurman O (1998) Clinical significance and outcome of anaerobic bacteremia. Clin Infect Dis 26:1413–1417. https://doi.org/10.1086/516355 PubMed DOI
Boattini M, Bianco G, Bastos P, Mavromanolaki VE, Maraki S, Spiliopoulou A et al (2025) Diagnostic and epidemiological landscape of anaerobic bacteria in Europe, 2020–2023 (ANAEuROBE). Int J Antimicrob Agents 65:107478. https://doi.org/10.1016/j.ijantimicag.2025.107478 PubMed DOI
https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_15.0_Breakpoint_Tables.pdf . Last accessed on 20
https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Guidance_documents/When_there_are_no_breakpoints_2024-09-03.pdf . Last accessed on 20
Brook I (2010) The role of anaerobic bacteria in bacteremia. Anaerobe 16:183–189. https://doi.org/10.1016/j.anaerobe.2009.12.001 PubMed DOI
Brook I (1995) Bacteroides infections in children. J Med Microbiol 43:92–98. https://doi.org/10.1099/00222615-43-2-92 PubMed DOI
Boman J, Nilson B, Sunnerhagen T, Rasmussen M (2022) True infection or contamination in patients with positive Cutibacterium blood cultures-a retrospective cohort study. Eur J Clin Microbiol Infect Dis 41:1029–1037. https://doi.org/10.1007/s10096-022-04458-9 PubMed DOI PMC
Scaggs Huang F, Griffin C, Fenchel M, DuBose M, Ankrum A, Schaffzin JK (2024) An outbreak after all: Cutibacterium acnes among pediatric patients with cerebrospinal fluid diversion device infections highlights gaps in guidelines. Antimicrob Steward Healthc Epidemiol 4:e128. https://doi.org/10.1017/ash.2024.359 PubMed DOI PMC
Reid R, McKnight RR, Secrist E, Clark C (2021) Sternoclavicular Septic Arthritis Caused by Cutibacterium acnes in a Previously Healthy 13-Year-Old Male: A Case Report. JBJS Case Connect 11. https://doi.org/10.2106/JBJS.CC.20.00690
Okabe K, Nakagawa K, Yamamoto E (1995) Factors affecting the occurrence of bacteremia associated with tooth extraction. Int J Oral Maxillofac Surg 24:239–242 PubMed DOI
Mann C, Dertinger S, Hartmann G, Schurz R, Simma B (2002) Actinomyces neuii and neonatal sepsis. Infection 30:178–180. https://doi.org/10.1007/s15010-002-2165-3 PubMed DOI
Abozaid S, Peretz A, Nasser W, Zarfin Y (2013) Rare infection--prolonged A. naeslundii bacteremia caused by severe caries. Harefuah 152:379–380. 435
Sonbol H, Spratt D, Roberts GJ, Lucas VS (2009) Prevalence, intensity and identity of bacteraemia following conservative dental procedures in children. Oral Microbiol Immunol 24:177–182. https://doi.org/10.1111/j.1399-302X.2008.00492.x PubMed DOI
Savoca E, Mehra S, Waldman EH (2019) A case of pediatric cervicofacial actinomyces masquerading as malignancy: Case report and review of the literature. Int J Pediatr Otorhinolaryngol 116:204–208. https://doi.org/10.1016/j.ijporl.2018.11.001 PubMed DOI
Goussard P, Eber E, Rabie H, Nel P, Schubert P (2022) Paediatric pulmonary actinomycosis: A forgotten disease. Paediatr Respir Rev 43:2–10. https://doi.org/10.1016/j.prrv.2021.09.001 PubMed DOI
Wacharachaisurapol N, Bender JM, Wang L, Bliss D, Ponrartana S, Pannaraj PS (2017) Abdominal Actinomycosis in Children: A Case Report and Literature Review. Pediatr Infect Dis J 36:e76–e79. https://doi.org/10.1097/INF.0000000000001416 PubMed DOI PMC
Demirhan S, Orner E, Szymczak W, Lee PJ, Aldrich M (2024) Skin and Soft Tissue Actinomycosis in Children and Adolescents. Pediatr Infect Dis J 43:743–747. https://doi.org/10.1097/INF.0000000000004345 PubMed DOI
Rueda MS, Hefter Y, Stone B, Hahn A, Jantausch B (2021) A Premature Infant With Neonatal Actinomyces odontolyticus Sepsis. J Pediatric Infect Dis Soc 10:533–535. https://doi.org/10.1093/jpids/piaa121 PubMed DOI
Grewing A, Jujjavarapu H, Price C, Eilers LF, Zimmerman S, Hiermandi N et al (2023) Esophageal Lesion Reveals an Aortic Pseudoaneurysm in the Setting of Actinomyces odontolyticus Bacteremia. JACC Case Rep 15:101867. https://doi.org/10.1016/j.jaccas.2023.101867 PubMed DOI PMC
Cannon JP, Lee TA, Bolanos JT, Danziger LH (2005) Pathogenic relevance of Lactobacillus: a retrospective review of over 200 cases. Eur J Clin Microbiol Infect Dis 24:31–40. https://doi.org/10.1007/s10096-004-1253-y PubMed DOI
Wu WH, Lee CC, Chen YC, Chiang MC, Chiu CH (2024) Invasive lactobacillus infection in pediatric patients in a tertiary center in Taiwan - 16 years’ experience and literature review. Pediatr Neonatol 65:282–287. https://doi.org/10.1016/j.pedneo.2023.05.013 PubMed DOI
Gilliam CH, Brazelton de Cardenas J, Carias D, Maron Alfaro G, Hayden RT, Hakim H (2023) Lactobacillus bloodstream infections genetically related to probiotic use in pediatric hematopoietic cell transplant patients. Infect Control Hosp Epidemiol 44:484–487. https://doi.org/10.1017/ice.2021.515
Cavicchiolo ME, Magnani M, Calgaro S, Bonadies L, Castagliulo I, Morelli L et al (2019) Neonatal sepsis associated with Lactobacillus supplementation. J Perinat Med 48:87–88. https://doi.org/10.1515/jpm-2019-0268 PubMed DOI
Land MH, Rouster-Stevens K, Woods CR, Cannon ML, Cnota J, Shetty AK (2005) Lactobacillus sepsis associated with probiotic therapy. Pediatrics 115:178–181. https://doi.org/10.1542/peds.2004-2137 PubMed DOI
De Groote MA, Frank DN, Dowell E, Glode MP, Pace NR (2005) Lactobacillus rhamnosus GG bacteremia associated with probiotic use in a child with short gut syndrome. Pediatr Infect Dis J 24:278–280. https://doi.org/10.1097/01.inf.0000154588.79356.e6 PubMed DOI
Hefter Y, Powell L, Tabulov CE, Sadler ED, Campos J, Hanisch B (2023) An 11-Year Review of Lactobacillus Bacteremia at a Pediatric Tertiary Care Center. Hosp Pediatr 13:e140–e143. https://doi.org/10.1542/hpeds.2022-006892 PubMed DOI
Gouriet F, Million M, Henri M, Fournier PE, Raoult D (2012) Lactobacillus rhamnosus bacteremia: an emerging clinical entity. Eur J Clin Microbiol Infect Dis 31:2469–2480. https://doi.org/10.1007/s10096-012-1599-5 PubMed DOI
Robin F, Paillard C, Marchandin H, Demeocq F, Bonnet R, Hennequin C (2010) Lactobacillus rhamnosus meningitis following recurrent episodes of bacteremia in a child undergoing allogeneic hematopoietic stem cell transplantation. J Clin Microbiol 48:4317–4319. https://doi.org/10.1128/JCM.00250-10 PubMed DOI PMC
Buhl MEJ, Sunnerhagen T, Join-Lambert O, Morris T, Jeverica S, Assous MV et al (2024) Antimicrobial resistance surveillance of Bacteroides fragilis isolated from blood cultures, Europe, 2022 (ReSuBacfrag). Int J Antimicrob Agents 64:107241. https://doi.org/10.1016/j.ijantimicag.2024.107241 PubMed DOI
Beig M, Shirazi O, Ebrahimi E, Banadkouki AZ, Golab N, Sholeh M (2024) Prevalence of antibiotic-resistant Cutibacterium acnes (formerly Propionibacterium acnes) isolates, a systematic review and meta-analysis. J Glob Antimicrob Resist 39:82–91. https://doi.org/10.1016/j.jgar.2024.07.005 PubMed DOI
Williams A, Coombs GW, Bell JM, Daley DA, Mowlaboccus S, Bryant P et al (2024) Antimicrobial resistance in Staphylococcus aureus and Enterococci spp. isolates from bloodstream infections in Australian children, 2013 - 2021. J Pediatric Infect Dis Soc piae110. https://doi.org/10.1093/jpids/piae110
Green MB, Zevallos Barboza A, Mukhopadhyay S, Gerber JS, Morowitz MJ, Puopolo KM, Flannery DD (2024) Anaerobe-targeted antibiotic therapy in the neonatal intensive care unit. J Pediatric Infect Dis Soc piae109. https://doi.org/10.1093/jpids/piae109
Woodford EC, Dhudasia MB, Puopolo KM, Skerritt LA, Bhavsar M, DeLuca J et al (2021) Neonatal blood culture inoculant volume: feasibility and challenges. Pediatr Res 90:1086–1092. https://doi.org/10.1038/s41390-021-01484-9 PubMed DOI PMC