Anaerobic bacteria in chronic wounds: Roles in disease, infection and treatment failure.
Journal
Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society
ISSN: 1524-475X
Titre abrégé: Wound Repair Regen
Pays: United States
ID NLM: 9310939
Informations de publication
Date de publication:
12 Aug 2024
12 Aug 2024
Historique:
revised:
09
07
2024
received:
21
05
2024
accepted:
29
07
2024
medline:
12
8
2024
pubmed:
12
8
2024
entrez:
12
8
2024
Statut:
aheadofprint
Résumé
Infection is among the most common factors that impede wound healing, yet standard treatments routinely fail to resolve chronic wound infections. The chronic wound environment is largely hypoxic/anoxic, and wounds are predominantly colonised by facultative and obligate anaerobic bacteria. Oxygen (O
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Medical Research Foundation of Oregon
Informations de copyright
© 2024 The Wound Healing Society.
Références
Pratama V, Risni HW, Yunir E, Sauriasari R. A systematic review of randomized controlled trials of antibiotic use in diabetic foot ulcer infections: focus on clinical cure. Infect Chemother. 2022;54(1):125‐139.
Tchero H, Kangambega P, Noubou L, Becsangele B, Fluieraru S, Teot L. Antibiotic therapy of diabetic foot infections: a systematic review of randomized controlled trials. Wound Repair Regen. 2018;26(5):381‐391.
Schreml S, Meier RJ, Kirschbaum M, et al. Luminescent dual sensors reveal extracellular pH‐gradients and hypoxia on chronic wounds that disrupt epidermal repair. Theranostics. 2014;4(7):721‐735.
James GA, Zhao AG, Usui M, et al. Microsensor and transcriptomic signatures of oxygen depletion in biofilms associated with chronic wounds. Wound Repair Regen. 2016;24(2):373‐383.
Younis I. Role of oxygen in wound healing. J Wound Care. 2020;29(Sup5b):S4‐S10.
Little AS, Younker IT, Schechter MS, et al. Dietary‐ and host‐derived metabolites are used by diverse gut bacteria for anaerobic respiration. Nat Microbiol. 2024;9(1):55‐69.
Faber F, Bäumler AJ. The impact of intestinal inflammation on the nutritional environment of the gut microbiota. Immunol Lett. 2014;162(2):48‐53.
Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ. Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci. 2001;58(2):165‐178.
Kolpen M, Kühl M, Bjarnsholt T, et al. Nitrous oxide production in sputum from cystic fibrosis patients with chronic Pseudomonas aeruginosa lung infection. PLoS One. 2014;9(1):e84353.
Zhong Q, Kobe B, Kappler U. Molybdenum enzymes and how they support virulence in pathogenic bacteria. Front Microbiol. 2020;11:615860.
Chaffin DO, Taylor D, Skerrett SJ, Rubens CE. Changes in the Staphylococcus aureus transcriptome during early adaptation to the lung. PLoS One. 2012;7(8):e41329.
Tagini F, Pillonel T, Croxatto A, et al. Distinct genomic features characterize two clades of Corynebacterium diphtheriae: proposal of Corynebacterium diphtheriae subsp. diphtheriae subsp. nov. and Corynebacterium diphtheriae subsp. lausannense subsp. nov. Front Microbiol. 2018;9:1743.
Line L, Alhede M, Kolpen M, et al. Physiological levels of nitrate support anoxic growth by denitrification of Pseudomonas aeruginosa at growth rates reported in cystic fibrosis lungs and sputum. Front Microbiol. 2014;5:554.
Palmer KL, Brown SA, Whiteley M. Membrane‐bound nitrate reductase is required for anaerobic growth in cystic fibrosis sputum. J Bacteriol. 2007;189(12):4449‐4455.
Bernatchez SF, Menon V, Stoffel J, et al. Nitric oxide levels in wound fluid may reflect the healing trajectory. Wound Repair Regen. 2013;21(3):410‐417.
Dhall S, Do D, Garcia M, et al. A novel model of chronic wounds: importance of redox imbalance and biofilm‐forming bacteria for establishment of chronicity. PLoS One. 2014;9(10):e109848.
Spees AM, Wangdi T, Lopez CA, et al. Streptomycin‐induced inflammation enhances Escherichia coli gut colonization through nitrate respiration. mBio. 2013;4(4). doi:10.1128/mbio.00430‐13
Lopez CA, Winter SE, Rivera‐Chávez F, et al. Phage‐mediated acquisition of a type III secreted effector protein boosts growth of Salmonella by nitrate respiration. mBio. 2012;3(3). doi:10.1128/mbio.00143‐12
Kim JH, Spero M, Lebig EG, et al. Targeting anaerobic respiration in Pseudomonas aeruginosa with chlorate improves healing of chronic wounds. Adv Wound Care. 2024;13(2):53‐69.
Cao P, Fleming D, Moustafa DA, et al. A Pseudomonas aeruginosa small RNA regulates chronic and acute infection. Nature. 2023;618(7964):358‐364.
Troitzsch A, Loi VV, Methling K, et al. Carbon source‐dependent reprogramming of anaerobic metabolism in Staphylococcus aureus. J Bacteriol. 2021;203(8). doi:10.1128/jb.00639‐20
Glasser NR, Kern SE, Newman DK. Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation of ATP and a proton‐motive force. Mol Microbiol. 2014;92(2):399‐412.
Caslin HL, Abebayehu D, Pinette JA, Ryan JJ. Lactate is a metabolic mediator that shapes immune cell fate and function. Front Physiol. 2021;12:688485.
Nielsen BU, Kolpen M, Jensen PØ, et al. Neutrophil count in sputum is associated with increased sputum glucose and sputum L‐lactate in cystic fibrosis. PLoS One. 2020;15(9):e0238524.
Bensel T, Stotz M, Borneff‐Lipp M, et al. Lactate in cystic fibrosis sputum. J Cyst Fibros. 2011;10(1):37‐44.
Florek LC, Lin X, Lin Y‐C, et al. The L‐lactate dehydrogenases of Pseudomonas aeruginosa are conditionally regulated but both contribute to survival during macrophage infection. bioRxiv. 2024. https://doi.org/10.1101/2024.03.21.586142
Lapébie P, Lombard V, Drula E, Terrapon N, Henrissat B. Bacteroidetes use thousands of enzyme combinations to break down glycans. Nat Commun. 2019;10(1):2043.
Flynn JM, Niccum D, Dunitz JM, Hunter RC. Evidence and role for bacterial mucin degradation in cystic fibrosis airway disease. PLoS Pathog. 2016;12(8):e1005846.
Cho D‐Y, Skinner D, Hunter RC, et al. Contribution of short chain fatty acids to the growth of Pseudomonas aeruginosa in rhinosinusitis. Front Cell Infect Microbiol. 2020;10:412.
Lucas SK, Villarreal AR, Ahmad MM, et al. Anaerobic microbiota derived from the upper airways impact Staphylococcus aureus physiology. Infect Immun. 2021;89(9):e00153‐e00221.
Karlsson C, Mörgelin M, Collin M, et al. SufA – a bacterial enzyme that cleaves fibrinogen and blocks fibrin network formation. Microbiology. 2009;155(Pt 1):238‐248.
Murphy EC, Mörgelin M, Reinhardt DP, Olin AI, Björck L, Frick I‐M. Identification of molecular mechanisms used by Finegoldia magna to penetrate and colonize human skin. Mol Microbiol. 2014;94(2):403‐417.
Lunar Silva I, Cascales E. Molecular strategies underlying Porphyromonas gingivalis virulence. J Mol Biol. 2021;433(7):166836.
Smalley JW, Olczak T. Heme acquisition mechanisms of Porphyromonas gingivalis – strategies used in a polymicrobial community in a heme‐limited host environment. Mol Oral Microbiol. 2017;32(1):1‐23.
Wildeboer D, Hill KE, Jeganathan F, et al. Specific protease activity indicates the degree of Pseudomonas aeruginosa infection in chronic infected wounds. Eur J Clin Microbiol Infect Dis. 2012;31(9):2183‐2189.
Serena TE, Bayliff SW, Brosnan PJ, et al. Bacterial protease activity as a biomarker to assess the risk of non‐healing in chronic wounds: results from a multicentre prospective cohort clinical trial. Wound Repair Regen. 2021;29(5):752‐758.
McCarty SM, Percival SL. Proteases and delayed wound healing. Adv Wound Care. 2013;2(8):438‐447.
Mathew‐Steiner SS, Roy S, Sen CK. Collagen in wound healing. Bioengineering. 2021;8(5):63.
Corrêa RO, Vieira A, Sernaglia EM, et al. Bacterial short‐chain fatty acid metabolites modulate the inflammatory response against infectious bacteria. Cell Microbiol. 2017;19(7):e12720.
Junka A, Wojtowicz W, Ząbek A, et al. Metabolic profiles of exudates from chronic leg ulcerations. J Pharm Biomed Anal. 2017;137:13‐22.
Rosier BT, Palazón C, García‐Esteban S, Artacho A, Galiana A, Mira A. A single dose of nitrate increases resilience against acidification derived from sugar fermentation by the oral microbiome. Front Cell Infect Microbiol. 2021;11:692883.
Mancabelli L, Tarracchini C, Milani C, et al. Vaginotypes of the human vaginal microbiome. Environ Microbiol. 2021;23(3):1780‐1792.
Watters C, Yuan TT, Rumbaugh KP. Beneficial and deleterious bacterial‐host interactions in chronic wound pathophysiology. Chronic Wound Care Manag Res. 2015;2:53‐62.
Percival SL, McCarty S, Hunt JA, Woods EJ. The effects of pH on wound healing, biofilms, and antimicrobial efficacy. Wound Repair Regen. 2014;22(2):174‐186.
Machado MG, Sencio V, Trottein F. Short‐chain fatty acids as a potential treatment for infections: a closer look at the lungs. Infect Immun. 2021;89(9):e0018821.
Fletcher JR, Villareal AR, Penningroth MR, Hunter RC. Staphylococcus aureus overcomes anaerobe‐derived short‐chain fatty acid stress via FadX and the CodY regulon. J Bacteriol. 2022;204(5):e00064‐e00122.
van der Hee B, Wells JM. Microbial regulation of host physiology by short‐chain fatty acids. Trends Microbiol. 2021;29(8):700‐712.
Corrêa‐Oliveira R, Fachi JL, Vieira A, Sato FT, Vinolo MAR. Regulation of immune cell function by short‐chain fatty acids. Clin Transl Immunol. 2016;5(4):e73.
Ney L‐M, Wipplinger M, Grossmann M, Engert N, Wegner VD, Mosig AS. Short chain fatty acids: key regulators of the local and systemic immune response in inflammatory diseases and infections. Open Biol. 2023;13(3):230014.
Tian X, Hellman J, Horswill AR, Crosby HA, Francis KP, Prakash A. Elevated gut microbiome‐derived propionate levels are associated with reduced sterile lung inflammation and bacterial immunity in mice. Front Microbiol. 2019;10:159.
Gethin G, Murphy L, Sezgin D, Carr PJ, Mcintosh C, Probst S. Resigning oneself to a life of wound‐related odour – a thematic analysis of patient experiences. J Tissue Viability. 2023;32(4):460‐464.
Silva ÁLDA, Matias LDM, Freitas JMS, Costa MML, Lima de Andrade L. Predictive factors for worsening chronic wounds. Rev Rene. 2020;21:e43615.
Morsli M, Salipante F, Magnan C, Dunyach‐Remy C, Sotto A, Lavigne J‐P. Direct metagenomics investigation of non‐surgical hard‐to‐heal wounds: a review. Ann Clin Microbiol Antimicrob. 2024;23(1):39.
Malone M, Johani K, Jensen SO, et al. Next generation DNA sequencing of tissues from infected diabetic foot ulcers. EBioMedicine. 2017;21:142‐149.
Gardner SE, Hillis SL, Heilmann K, Segre JA, Grice EA. The neuropathic diabetic foot ulcer microbiome is associated with clinical factors. Diabetes. 2013;62(3):923‐930.
Choi Y, Banerjee A, McNish S, et al. Co‐occurrence of anaerobes in human chronic wounds. Microb Ecol. 2019;77(3):808‐820.
Dunyach‐Remy C, Salipante F, Lavigne J‐P, et al. Pressure ulcers microbiota dynamics and wound evolution. Sci Rep. 2021;11(1):18506.
Uçkay I, Gariani K, Pataky Z, Lipsky BA. Diabetic foot infections: state‐of‐the‐art. Diabetes Obes Metab. 2014;16(4):305‐316.
Charles PGP, Uçkay I, Kressmann B, Emonet S, Lipsky BA. The role of anaerobes in diabetic foot infections. Anaerobe. 2015;34:8‐13.
Kalan LR, Meisel JS, Loesche MA, et al. Strain‐ and species‐level variation in the microbiome of diabetic wounds is associated with clinical outcomes and therapeutic efficacy. Cell Host Microbe. 2019;25(5):641‐655.e5.
Verbanic S, Shen Y, Lee J, Deacon JM, Chen IA. Microbial predictors of healing and short‐term effect of debridement on the microbiome of chronic wounds. npj Biofilms Microbiomes. 2020;6(1):21.
Nagy E, Boyanova L, Justesen US. How to isolate, identify and determine antimicrobial susceptibility of anaerobic bacteria in routine laboratories. Clin Microbiol Infect. 2018;24(11):1139‐1148.
Rodriguez C, Jary A, Hua C, et al. Pathogen identification by shotgun metagenomics of patients with necrotizing soft‐tissue infections. Br J Dermatol. 2020;183(1):105‐113.
Han A, Zenilman JM, Melendez JH, et al. The importance of a multifaceted approach to characterizing the microbial flora of chronic wounds. Wound Repair Regen. 2011;19(5):532‐541.
Lewis WH, Tahon G, Geesink P, Sousa DZ, Ettema TJG. Innovations to culturing the uncultured microbial majority. Nat Rev Microbiol. 2021;19(4):225‐240.
Goggin KP, Beckmann N, Bettin K, Carrillo‐Marquez M, Wood J, Arnold SR. Lemierre's syndrome due to the zoonotic anaerobe Bacteroides pyogenes: case report and literature review. J Pediatr Infect Dis Soc. 2021;10(8):886‐888.
Cobo F, Pérez‐Carrasco V, Martín‐Hita L, García‐Salcedo JA, Navarro‐Marí JM. Comparative evaluation of MALDI‐TOF MS and 16S rRNA gene sequencing for the identification of clinically relevant anaerobic bacteria. Critical evaluation of discrepant results. Anaerobe. 2023;82:102754.
Kim M. Update on the taxonomy of clinically important anaerobic bacteria. Korean J Clin Lab Sci. 2022;54(4):239‐248.
Brüggemann H, Jensen A, Nazipi S, et al. Pan‐genome analysis of the genus Finegoldia identifies two distinct clades, strain‐specific heterogeneity, and putative virulence factors. Sci Rep. 2018;8(1):266.
Aujoulat F, Mazuet C, Criscuolo A, et al. Peptoniphilus nemausensis sp. nov. A new Gram‐positive anaerobic coccus isolated from human clinical samples, an emendated description of the genus Peptoniphilus and an evaluation of the taxonomic status of Peptoniphilus species with not validly published names. Syst Appl Microbiol. 2021;44(5):126235.
Bay L, Barnes CJ, Fritz BG, et al. Universal dermal microbiome in human skin. mBio. 2020;11(1):e02945‐e03019.
Poyet M, Groussin M, Gibbons SM, et al. A library of human gut bacterial isolates paired with longitudinal multiomics data enables mechanistic microbiome research. Nat Med. 2019;25(9):1442‐1452.
Mancabelli L, Milani C, Fontana F, et al. Mapping bacterial diversity and metabolic functionality of the human respiratory tract microbiome. J Oral Microbiol. 2022;14:1‐16.
Delbeke H, Younas S, Casteels I, Joossens M. Current knowledge on the human eye microbiome: a systematic review of available amplicon and metagenomic sequencing data. Acta Ophthalmol. 2021;99(1):16‐25.
Dubourg G, Morand A, Mekhalif F, et al. Deciphering the urinary microbiota repertoire by culturomics reveals mostly anaerobic bacteria from the gut. Front Microbiol. 2020;11:513305.
Altmäe S, Franasiak JM, Mändar R. The seminal microbiome in health and disease. Nat Rev Urol. 2019;16(12):703‐721.
Gontcharova V, Youn E, Sun Y, Wolcott RD, Dowd SE. A comparison of bacterial composition in diabetic ulcers and contralateral intact skin. Open Microbiol J. 2010;4:8‐19.
Daunaraite K, Uvarovas V, Ulevicius D, et al. Reciprocal hematogenous osteomyelitis of the femurs caused by Anaerococcus prevotii: a case report. World J Clin Cases. 2021;9(4):830‐837.
Kirti M, Sharma B, Kumar K. Case series of Anaerococcus prevotii infection in road traffic accidents in New Delhi, India. Microbiol Indep Res J. 2023;10:65‐69.
McGinniss JE, Imai I, Simon‐Soro A, et al. Molecular analysis of the endobronchial stent microbial biofilm reveals bacterial communities that associate with stent material and frequent fungal constituents. PLoS One. 2019;14(5):e0217306.
Pammi M, Thapa S, Balderas M, Runge JK, Venkatachalam A, Luna RA. Microbiome signatures in neonatal central line associated bloodstream infections. PLoS One. 2020;15(1):e0227967.
Turner NA, Charalambous LT, Case A, Byers IS, Seidelman J. 242. Rising incidence of Finegoldia magna among prosthetic joint infections. Open Forum Infect Dis. 2021;8(Supplement_1):S230.
Zhao‐Fleming HH, Wilkinson JE, Larumbe E, Dissanaike S, Rumbaugh K. Obligate anaerobes are abundant in human necrotizing soft tissue infection samples – a metagenomics analysis. APMIS. 2019;127(8):577‐587.
Marrazzo JM, Thomas KK, Fiedler TL, Ringwood K, Fredricks DN. Relationship of specific vaginal bacteria and bacterial vaginosis treatment failure in women who have sex with women. Ann Intern Med. 2008;149(1):20‐28.
Schell SL, Schneider AM, Nelson AM. Yin and Yang: a disrupted skin microbiome and an aberrant host immune response in hidradenitis suppurativa. Exp Dermatol. 2021;30(10):1453‐1470.
Larsen JM. The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology. 2017;151(4):363‐374.
Hajishengallis G, Darveau RP, Curtis MA. The keystone pathogen hypothesis. Nat Rev Microbiol. 2012;10(10):717‐725.
Wang M, Krauss JL, Domon H, et al. Microbial hijacking of complement–toll‐like receptor crosstalk. Sci Signal. 2010;3(109):ra11.
Maekawa T, Krauss JL, Abe T, et al. Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host Microbe. 2014;15(6):768‐778.
Olsen I, Lambris JD, Hajishengallis G. Porphyromonas gingivalis disturbs host–commensal homeostasis by changing complement function. J Oral Microbiol. 2017;9(1):1340085.
Matsui A, Jin J‐O, Johnston CD, Yamazaki H, Houri‐Haddad Y, Rittling SR. Pathogenic bacterial species associated with endodontic infection evade innate immune control by disabling neutrophils. Infect Immun. 2014;82(10):4068‐4079.
Neumann A, Björck L, Frick I‐M. Finegoldia magna, an anaerobic gram‐positive bacterium of the normal human microbiota, induces inflammation by activating neutrophils. Front Microbiol. 2020;11:65.
Anderson AL, Zheng Y, Song D, et al. The B‐cell superantigen Finegoldia magna protein L causes pulmonary inflammation by a mechanism dependent on MyD88 but not B cells or immunoglobulins. Inflamm Res. 2012;61(2):161‐169.
Neumann A. Rapid release of sepsis markers heparin‐binding protein and calprotectin triggered by anaerobic cocci poses an underestimated threat. Anaerobe. 2022;75:102584.
Ling W‐L, Su CT‐T, Lua W‐H, et al. Variable‐heavy (VH) families influencing IgA1&2 engagement to the antigen, FcαRI and superantigen proteins G, A, and L. Sci Rep. 2022;12(1):6510.
Deacy AM, Gan SK‐E, Derrick JP. Superantigen recognition and interactions: functions, mechanisms and applications. Front Immunol. 2021;12:731845.
Ricci S, Medaglini D, Marcotte H, Olsén A, Pozzi G, Björck L. Immunoglobulin‐binding domains of peptostreptococcal protein L enhance vaginal colonization of mice by Streptococcus gordonii. Microb Pathog. 2001;30(4):229‐235.
Wall IB, Davies CE, Hill KE, et al. Potential role of anaerobic cocci in impaired human wound healing. Wound Repair Regen. 2002;10(6):346‐353.
Stephens P, Wall IB, Wilson MJ, et al. Anaerobic cocci populating the deep tissues of chronic wounds impair cellular wound healing responses in vitro. Br J Dermatol. 2003;148(3):456‐466.
Ezaki T, Kawamura Y, Li N, Li ZY, Zhao L, Shu S. Proposal of the genera Anaerococcus gen. nov., Peptoniphilus gen. nov. and Gallicola gen. nov. for members of the genus Peptostreptococcus. Int J Syst Evol Microbiol. 2001;51(4):1521‐1528.
Castro PR, Bittencourt LFF, Larochelle S, et al. GPR43 regulates sodium butyrate‐induced angiogenesis and matrix remodeling. Am J Physiol Heart C. 2021;320(3):H1066‐H1079.
Trompette A, Pernot J, Perdijk O, et al. Gut‐derived short‐chain fatty acids modulate skin barrier integrity by promoting keratinocyte metabolism and differentiation. Mucosal Immunol. 2022;15(5):908‐926.
Pham VT, Lacroix C, Braegger CP, Chassard C. Lactate‐utilizing community is associated with gut microbiota dysbiosis in colicky infants. Sci Rep. 2017;7(1):11176.
Llibre A, Grudzinska FS, O'Shea MK, et al. Lactate cross‐talk in host–pathogen interactions. Biochem J. 2021;478(17):3157‐3178.
Porporato PE, Payen VL, De Saedeleer CJ, et al. Lactate stimulates angiogenesis and accelerates the healing of superficial and ischemic wounds in mice. Angiogenesis. 2012;15(4):581‐592.
Kozlov AM, Lone A, Betts DH, Cumming RC. Lactate preconditioning promotes a HIF‐1α‐mediated metabolic shift from OXPHOS to glycolysis in normal human diploid fibroblasts. Sci Rep. 2020;10(1):8388.
Liu W, Wang Y, Bozi LHM, et al. Lactate regulates cell cycle by remodelling the anaphase promoting complex. Nature. 2023;616(7958):790‐797.
Lu Z, Imlay JA. When anaerobes encounter oxygen: mechanisms of oxygen toxicity, tolerance and defence. Nat Rev Microbiol. 2021;19(12):774‐785.
Ślesak I, Kula M, Ślesak H, Miszalski Z, Strzałka K. How to define obligatory anaerobiosis? An evolutionary view on the antioxidant response system and the early stages of the evolution of life on Earth. Free Radic Biol Med. 2019;140:61‐73.
Perry EK, Tan M‐W. Bacterial biofilms in the human body: prevalence and impacts on health and disease. Front Cell Infect Microbiol. 2023;13:1237164.
Malone M, Bjarnsholt T, McBain AJ, et al. The prevalence of biofilms in chronic wounds: a systematic review and meta‐analysis of published data. J Wound Care. 2017;26(1):20‐25.
Johani K, Malone M, Jensen S, et al. Microscopy visualisation confirms multi‐species biofilms are ubiquitous in diabetic foot ulcers. Int Wound J. 2017;14(6):1160‐1169.
Patterson JL, Stull‐Lane A, Girerd PH, Jefferson KK. Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial‐vaginosis‐associated anaerobes. Microbiology. 2010;156(2):392‐399.
Donelli G, Vuotto C, Cardines R, Mastrantonio P. Biofilm‐growing intestinal anaerobic bacteria. FEMS Immunol Med Microbiol. 2012;65(2):318‐325.
Gerits E, Verstraeten N, Michiels J. New approaches to combat Porphyromonas gingivalis biofilms. J Oral Microbiol. 2017;9(1):1300366.
Murphy EC, Frick I‐M. Gram‐positive anaerobic cocci – commensals and opportunistic pathogens. FEMS Microbiol Rev. 2013;37(4):520‐553.
Roilides E, Simitsopoulou M, Katragkou A, Walsh TJ. How biofilms evade host defenses. Microbiol Spectr. 2015;3(3). doi: 10.1128/microbiolspec.MB‐0012‐2014
Alhede M, Lorenz M, Fritz BG, et al. Bacterial aggregate size determines phagocytosis efficiency of polymorphonuclear leukocytes. Med Microbiol Immunol (Berl). 2020;209(6):669‐680.
Ciofu O, Moser C, Jensen PØ, Høiby N. Tolerance and resistance of microbial biofilms. Nat Rev Microbiol. 2022;20(10):621‐635.
Wright TL, Ellen RP, Lacroix J‐M, Sinnadurai S, Mittelman MW. Effects of metronidazole on Porphyromonas gingivalis biofilms. J Periodontal Res. 1997;32(5):473‐477.
Wuersching SN, Huth KC, Hickel R, Kollmuss M. Targeting antibiotic tolerance in anaerobic biofilms associated with oral diseases: human antimicrobial peptides LL‐37 and lactoferricin enhance the antibiotic efficacy of amoxicillin, clindamycin and metronidazole. Anaerobe. 2021;71:102439.
Percival SL, Malone M, Mayer D, Salisbury A‐M, Schultz G. Role of anaerobes in polymicrobial communities and biofilms complicating diabetic foot ulcers. Int Wound J. 2018;15(5):776‐782.
Dalton T, Dowd SE, Wolcott RD, et al. An in vivo polymicrobial biofilm wound infection model to study interspecies interactions. PLoS One. 2011;6(11):e27317.
Fox EP, Cowley ES, Nobile CJ, Hartooni N, Newman DK, Johnson AD. Anaerobic bacteria grow within Candida albicans biofilms and induce biofilm formation in suspension cultures. Curr Biol. 2014;24(20):2411‐2416.
Thaarup IC, Iversen AKS, Lichtenberg M, Bjarnsholt T, Jakobsen TH. Biofilm survival strategies in chronic wounds. Microorganisms. 2022;10(4):775.
Dubreuil L, Veloo AC, Sóki J. Correlation between antibiotic resistance and clinical outcome of anaerobic infections; mini‐review. Anaerobe. 2021;72:102463.
Senneville É, Albalawi Z, van Asten SA, et al. IWGDF/IDSA guidelines on the diagnosis and treatment of diabetes‐related foot infections (IWGDF/IDSA 2023). Clin Infect Dis. 2023;ciad527. https://doi.org/10.1093/cid/ciad527
Roberts MC. Distribution of tetracycline and macrolide‐lincosamide‐streptogramin B resistance genes in anaerobic bacteria. Clin Infect Dis. 1995;20(Supplement_2):S367‐S369.
Johnson CC. Susceptibility of anaerobic bacteria to β‐lactam antibiotics in the United States. Clin Infect Dis. 1993;16(Supplement_4):S371‐S376.
Rodloff AC, Dowzicky MJ. In vitro activity of tigecycline and comparators against a European collection of anaerobes collected as part of the Tigecycline Evaluation and Surveillance Trial (T.E.S.T.) 2010–2016. Anaerobe. 2018;51:78‐88.
Di Bella S, Antonello RM, Sanson G, et al. Anaerobic bloodstream infections in Italy (ITANAEROBY): a 5‐year retrospective nationwide survey. Anaerobe. 2022;75:102583.
Alauzet C, Lozniewski A, Marchandin H. Metronidazole resistance and nim genes in anaerobes: a review. Anaerobe. 2019;55:40‐53.
Smith A. Metronidazole resistance: a hidden epidemic? Br Dent J. 2018;224(6):403‐404.
Walser F, Prinz J, Rahm S, et al. Antimicrobial susceptibility testing is crucial when treating Finegoldia magna infections. Eur J Clin Microbiol Infect Dis. 2022. https://doi.org/10.1007/s10096-022-04439-y
Schaper NC, Dryden M, Kujath P, et al. Efficacy and safety of IV/PO moxifloxacin and IV piperacillin/tazobactam followed by PO amoxicillin/clavulanic acid in the treatment of diabetic foot infections: results of the RELIEF study. Infection. 2013;41(1):175‐186.
Lipsky BA, Itani K, Norden C, Linezolid Diabetic Foot Infections Study Group. Treating foot infections in diabetic patients: a randomized, multicenter, open‐label trial of linezolid versus ampicillin‐sulbactam/amoxicillin‐clavulanate. Clin Infect Dis. 2004;38(1):17‐24.
Lipsky BA, Stoutenburgh U. Daptomycin for treating infected diabetic foot ulcers: evidence from a randomized, controlled trial comparing daptomycin with vancomycin or semi‐synthetic penicillins for complicated skin and skin‐structure infections. J Antimicrob Chemother. 2005;55(2):240‐245.
Smith R, Russo J, Fiegel J, Brogden N. Antibiotic delivery strategies to treat skin infections when innate antimicrobial defense fails. Antibiotics. 2020;9(2):56.
Seabrook GR, Edmiston CE, Schmitt DD, Krepel C, Bandyk DF, Towne JB. Comparison of serum and tissue antibiotic levels in diabetes‐related foot infections. Surgery. 1991;110(4):671‐676.
Tseng BS, Zhang W, Harrison JJ, et al. The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ Microbiol. 2013;15(10):2865‐2878.
Walters MC, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother. 2003;47(1):317‐323.
Cao B, Christophersen L, Thomsen K, et al. Antibiotic penetration and bacterial killing in a Pseudomonas aeruginosa biofilm model. J Antimicrob Chemother. 2015;70(7):2057‐2063.
Anderl JN, Franklin MJ, Stewart PS. Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother. 2000;44(7):1818‐1824.
Singh R, Sahore S, Kaur P, Rani A, Ray P. Penetration barrier contributes to bacterial biofilm‐associated resistance against only select antibiotics, and exhibits genus‐, strain‐ and antibiotic‐specific differences. Pathog Dis. 2016;74(6):ftw056.
Ortíz‐Pérez A, Martín‐de‐Hijas N, Alonso‐Rodríguez N, Molina‐Manso D, Fernández‐Roblas R, Esteban J. Importance of antibiotic penetration in the antimicrobial resistance of biofilm formed by non‐pigmented rapidly growing mycobacteria against amikacin, ciprofloxacin and clarithromycin. Enferm Infecc Microbiol Clín. 2011;29(2):79‐84.
Singh R, Ray P, Das A, Sharma M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Antimicrob Chemother. 2010;65(9):1955‐1958.
Jefferson KK, Goldmann DA, Pier GB. Use of confocal microscopy to analyze the rate of vancomycin penetration through Staphylococcus aureus biofilms. Antimicrob Agents Chemother. 2005;49(6):2467‐2473.
Brauner A, Fridman O, Gefen O, Balaban NQ. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat Rev Microbiol. 2016;14(5):320‐330.
Coates A, Hu Y, Bax R, Page C. The future challenges facing the development of new antimicrobial drugs. Nat Rev Drug Discov. 2002;1(11):895‐910.
Leviton IM, Fraimow HS, Carrasco N, Dougherty TJ, Miller MH. Tobramycin uptake in Escherichia coli membrane vesicles. Antimicrob Agents Chemother. 1995;39(2):467‐475.
Lopatkin AJ, Stokes JM, Zheng EJ, et al. Bacterial metabolic state more accurately predicts antibiotic lethality than growth rate. Nat Microbiol. 2019;4(12):2109‐2117.
Greulich P, Scott M, Evans MR, Allen RJ. Growth‐dependent bacterial susceptibility to ribosome‐targeting antibiotics. Mol Syst Biol. 2015;11(3):796.
Lee AJ, Wang S, Meredith HR, Zhuang B, Dai Z, You L. Robust, linear correlations between growth rates and β‐lactam–mediated lysis rates. Proc Natl Acad Sci. 2018;115(16):4069‐4074.
Evans DJ, Allison DG, Brown MRW, Gilbert P. Susceptibility of Pseudomonas aeruginosa and Escherichia coli biofilms towards ciprofloxacin: effect of specific growth rate. J Antimicrob Chemother. 1991;27(2):177‐184.
Spero MA, Newman DK. Chlorate specifically targets oxidant‐starved, antibiotic‐tolerant populations of Pseudomonas aeruginosa biofilms. mBio. 2018;9(5). doi:10.1128/mbio.01400‐18
Gupta S, Laskar N, Kadouri DE. Evaluating the effect of oxygen concentrations on antibiotic sensitivity, growth, and biofilm formation of human pathogens. Microbiol Insights. 2016;9:37‐46.
Pabst B, Pitts B, Lauchnor E, Stewart PS. Gel‐entrapped Staphylococcus aureus bacteria as models of biofilm infection exhibit growth in dense aggregates, oxygen limitation, antibiotic tolerance, and heterogeneous gene expression. Antimicrob Agents Chemother. 2016;60(10):6294‐6301.
Jorth P, Spero MA, Livingston J, Newman DK. Quantitative visualization of gene expression in mucoid and nonmucoid Pseudomonas aeruginosa aggregates reveals localized peak expression of alginate in the hypoxic zone. mBio. 2019;10(6). doi:10.1128/mbio.02622‐19
Kolpen M, Kragh KN, Enciso JB, et al. Bacterial biofilms predominate in both acute and chronic human lung infections. Thorax. 2022;77(10):1015‐1022.
DePas WH, Starwalt‐Lee R, Van Sambeek L, Ravindra Kumar S, Gradinaru V, Newman DK. Exposing the three‐dimensional biogeography and metabolic states of pathogens in cystic fibrosis sputum via hydrogel embedding, clearing, and rRNA labeling. mBio. 2016;7(5):e00796‐e00816.
Kragh KN, Alhede M, Jensen PØ, et al. Polymorphonuclear leukocytes restrict growth of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Infect Immun. 2014;82(11):4477‐4486.
Neubauer C, Kasi AS, Grahl N, et al. Refining the application of microbial lipids as tracers of Staphylococcus aureus growth rates in cystic fibrosis sputum. J Bacteriol. 2018;200(24). doi:10.1128/jb.00365‐18
Valentini TD, Lucas SK, Binder KA, et al. Bioorthogonal non‐canonical amino acid tagging reveals translationally active subpopulations of the cystic fibrosis lung microbiota. Nat Commun. 2020;11(1):2287.
Ibberson CB, Barraza JP, Holmes AL, Cao P, Whiteley M. Precise spatial structure impacts antimicrobial susceptibility of S. aureus in polymicrobial wound infections. Proc Natl Acad Sci. 2022;119(51):e2212340119.
Turner KH, Everett J, Trivedi U, Rumbaugh KP, Whiteley M. Requirements for Pseudomonas aeruginosa acute burn and chronic surgical wound infection. PLoS Genet. 2014;10(7):e1004518.
Ibberson CB, Whiteley M. The Staphylococcus aureus transcriptome during cystic fibrosis lung infection. mBio. 2019;10(6). doi:10.1128/mbio.02774‐19
Gefen O, Chekol B, Strahilevitz J, Balaban NQ. TDtest: easy detection of bacterial tolerance and persistence in clinical isolates by a modified disk‐diffusion assay. Sci Rep. 2017;7:41284.
Van den Bergh B, Michiels JE, Fauvart M, Michiels J. Should we develop screens for multi‐drug antibiotic tolerance? Expert Rev Anti‐Infect Ther. 2016;14(7):613‐616.
Pamp SJ, Gjermansen M, Johansen HK, Tolker‐Nielsen T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB‐oprM genes. Mol Microbiol. 2008;68(1):223‐240.
Brochmann RP, Toft A, Ciofu O, et al. Bactericidal effect of colistin on planktonic Pseudomonas aeruginosa is independent of hydroxyl radical formation. Int J Antimicrob Agents. 2014;43(2):140‐147.
Kolpen M, Appeldorff CF, Brandt S, et al. Increased bactericidal activity of colistin on Pseudomonas aeruginosa biofilms in anaerobic conditions. FEMS Pathog Dis. 2016;74(1):ftv086.
Bergkessel M, Basta DW, Newman DK. The physiology of growth arrest: uniting molecular and environmental microbiology. Nat Rev Microbiol. 2016;14(9):549‐562.
Basta DW, Bergkessel M, Newman DK. Identification of fitness determinants during energy‐limited growth arrest in Pseudomonas aeruginosa. mBio. 2017;8(6). doi:10.1128/mbio.01170‐17
Harms A, Maisonneuve E, Gerdes K. Mechanisms of bacterial persistence during stress and antibiotic exposure. Science. 2016;354(6318):aaf4268.
Conlon BP, Nakayasu ES, Fleck LE, et al. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature. 2013;503(7476):365‐370.
Trombetta RP, Dunman PM, Schwarz EM, Kates SL, Awad HA. A high‐throughput screening approach to repurpose FDA‐approved drugs for bactericidal applications against Staphylococcus aureus small‐colony variants. mSphere. 2018;3(5):e00422‐e00518.
Stokes JM, Gutierrez A, Lopatkin AJ, et al. A multiplexable assay for screening antibiotic lethality against drug‐tolerant bacteria. Nat Methods. 2019;16(4):303‐306.
Cook GM, Greening C, Hards K, Berney M. Energetics of pathogenic bacteria and opportunities for drug development. Adv Microb Physiol. 2014;65:1‐62.
Spero MA, Jones J, Lomenick B, Chou TF, Newman DK. Mechanisms of chlorate toxicity and resistance in Pseudomonas aeruginosa. Mol Microbiol. 2022;118(4):321‐335.
Hasenoehrl EJ, Wiggins TJ, Berney M. Bioenergetic inhibitors: antibiotic efficacy and mechanisms of action in Mycobacterium tuberculosis. Front Cell Infect Microbiol. 2021;10:611683.
Manuse S, Shan Y, Canas‐Duarte SJ, et al. Bacterial persisters are a stochastically formed subpopulation of low‐energy cells. PLoS Biol. 2021;19(4):e3001194.
Jensen PØ, Møller SA, Lerche CJ, et al. Improving antibiotic treatment of bacterial biofilm by hyperbaric oxygen therapy: not just hot air. Biofilms. 2019;1:100008.
Laulund AS, Schwartz FA, Christophersen L, et al. Hyperbaric oxygen therapy augments ciprofloxacin effect against Pseudomonas aeruginosa biofilm infected chronic wounds in a mouse model. Biofilms. 2023;5:100100.
Kolpen M, Lerche CJ, Kragh KN, et al. Hyperbaric oxygen sensitizes anoxic Pseudomonas aeruginosa biofilm to ciprofloxacin. Antimicrob Agents Chemother. 2017;61(11). doi:10.1128/aac.01024‐17
Gottrup F, Dissemond J, Baines C, et al. Use of oxygen therapies in wound healing: focus on topical and hyperbaric oxygen treatment. J Wound Care. 2017;26(Sup5):S1‐S43.
Armstrong DG, Edmonds ME, Serena TE. Point‐of‐care fluorescence imaging reveals extent of bacterial load in diabetic foot ulcers. Int Wound J. 2023;20(2):554‐566.
Hoffman PS. Amixicile: a concept therapeutic for treatment of chronic anaerobic infections. Br J Gastroenterol. 2020;2(1):138‐142.
Sasmanto S, Wasito EB. Odontogenic brain abscess due to Anaerococcus prevotii infections: a case report and review article. Int J Surg Case Rep. 2022;97:107450.
Chatterjee T, Roy M, Reddy YPS, Ahmad S. Finding of Anaerococcus hydrogenalis in blood using cell‐free DNA technique in a patient with infective endocarditis. Germs. 2023;13(3):282‐287.
Nema S, Brahmachari S, Vishnu TN, Biswas D. Clinico‐microbiological spectrum of anaerobic pyogenic infections in an Indian tertiary care teaching hospital: a two‐year study. J Family Med Prim Care. 2021;10(7):2512‐2517.
Matsuoka T, Shimizu T, Minagawa T, et al. First case of an invasive Bacteroides dorei infection detected in a patient with a mycotic aortic aneurysm—raising a rebellion of major indigenous bacteria in humans: a case report and review. BMC Infect Dis. 2021;21(1):625.
Cobo F. Brain abscesses caused by anaerobic microorganisms: a systematic review. Rev Esp Quimioter. 2023;36(2):152‐159.
Hua DT, Spiegel J, Fu P‐Y, Yuchno D. A case of native joint septic arthritis caused by Bacteroides fragilis. Am J Case Rep. 2021;22:e934266‐1‐e934266‐4.
Salavitabar K, Vyas A, Barry M, Masih M, Gandhi S, et al. Chronic osteomyelitis caused by Finegoldia magna. Consultant. 2022;62(5):e4‐e5.
Cobo F, Calatrava E, Navarro‐Marí JM. Early prosthetic valve endocarditis due to Finegoldia magna. Microbiol Insights. 2019;12:1178636119876640.
Breidung D, Delavari S, Megas I‐F, Reichert B, Billner M. Necrotizing fasciitis after panniculectomy caused by Finegoldia magna. Plast Reconstr Surg Glob Open. 2024;12(4):e5773.
Thomas N, Taggarsi D, Dasari P, Rathna R. A rare case of spontaneous anterior abdominal wall necrotizing soft tissue infection caused by Finegoldia magna. Cureus. 2021;13(11).
Szymczak Z, Michalski P, Dudek J, et al. Finegoldia magna the cause of hip revision surgery ‐ a two case report. Pol Merkur Lek Organ Pol Tow Lek. 2019;47(279):99‐102.
Alsubaie S, Dolgum S, Binkhamis K, Alweijri I, Bugshan A, Alzamil F. Finegoldia magna causing intramedullary thoracic spinal cord abscess in an infant. Anaerobe. 2019;56:57‐60.
Wan X, Wang S, Wang M, Liu J, Zhang Y. Identification of Peptoniphilus harei from blood cultures in an infected aortic aneurysm patient: case report and review published literature. Front Cell Infect Microbiol. 2021;11:755225.
Ji C, Xu F, Wang Y, Qin Y. Peptoniphilus indolicus infection in a pregnant woman: a case report. Curr Med Res Opin. 2022;38(8):1439‐1442.
Sreenivasan P, Sharma B, Singh A, Kataria MS, Ray P, Angrup A. Secondary anaerobic infection in a case of multidrug resistant tubercular paraspinal abscess: a rare presentation. Access Microbiol. 2021;3(8):000253.
Lu Y, Xia W, Ni F, Xu Y. Septic shock, renal abscess, and bacteremia due to Peptoniphilus asaccharolyticus in a woman with nephrosis and diabetes mellitus: case report and literature review. Infect Drug Resist. 2022;15:831‐837.
Enault C, Aujoulat F, Pantel A, et al. Surgical site infection after hip replacement due to a novel Peptoniphilus species, provisionally named ‘Peptoniphilus nemausus’ sp. nov. Anaerobe. 2020;61:102071.
Zhang Y, Zhu Y, Wan H. Case report: multiple abscesses caused by Porphyromonas gingivalis diagnosed by metagenomic next‐generation sequencing. Front Med. 2023;9:1089863.
Sha J, Shao J, Lu S, et al. Pyopneumothorax with bronchopleural fistula due to pulmonary infection caused by Porphyromonas gingivalis in a patient with periodontitis. Clin Respir J. 2023;17(9):962‐965.
Wang X, Liu L, Lu B, et al. The thoracoabdominal wall abscess and sepsis caused by Porphyromonas pogonae: Case report and literature review. Heliyon. 2023;9(4):e14860.
Di Marco BA, Inchingolo R, Smargiassi A, et al. Empyema caused by Prevotella bivia complicating an unusual case of spontaneous chylothorax. J Clin Microbiol. 2020;52(4):1284‐1286.
Ye Z, He J, Ji H, et al. Case report: isolated prevotella intermedia causing intracranial infection detected using metagenomic next generation sequencing. BMC Neurol. 2023;23(1):383.
Simsek B, Zhang R, Morton C, Villanueva MS. Lemierre syndrome with pulmonary empyema caused by Prevotella intermedia. BMJ Case Rep. 2024;17(3):e258158.
Asif AA, Roy M, Ahmad S. Rare case of Prevotella pleuritidis lung abscess. BMJ Case Rep. 2020;13(9):e235960.
Ogawa T. A rare case of fulminant sepsis secondary to postpartum pyomyoma caused by Prevotella bivia: a case report. Ann Med Surg. 2023;85(3):606‐610.
Dodin RE, Thompson H, Storandt MH, Vilenski L, Guerrero DM. Prevotella bivia septic arthritis in an immunocompetent adult: a case report and review of literature. J Investig Med High Impact Case Rep. 2023;11:23247096231194842.