Bad to the Bone: On In Vitro and Ex Vivo Microbial Biofilm Ability to Directly Destroy Colonized Bone Surfaces without Participation of Host Immunity or Osteoclastogenesis
Identifieur interne : 000007 ( Main/Exploration ); précédent : 000006; suivant : 000008Bad to the Bone: On In Vitro and Ex Vivo Microbial Biofilm Ability to Directly Destroy Colonized Bone Surfaces without Participation of Host Immunity or Osteoclastogenesis
Auteurs : Adam Junka [Pologne] ; Patrycja Szymczyk [Pologne] ; Grzegorz Zi Kowski [Pologne] ; Ewa Karuga-Kuzniewska [Pologne] ; Danuta Smutnicka [Pologne] ; Iwona Bil-Lula [Pologne] ; Marzenna Bartoszewicz [Pologne] ; Susan Mahabady [États-Unis] ; Parish Paymon Sedghizadeh [États-Unis]Source :
- PLoS ONE [ 1932-6203 ] ; 2017.
Abstract
Bone infections are a significant public health burden associated with morbidity and mortality in patients. Microbial biofilm pathogens are the causative agents in chronic osteomyelitis. Research on the pathogenesis of osteomyelitis has focused on indirect bone destruction by host immune cells and cytokines secondary to microbial insult. Direct bone resorption by biofilm pathogens has not yet been seriously considered. In this study, common osteomyelitis pathogens (
Url:
DOI: 10.1371/journal.pone.0169565
PubMed: 28076372
PubMed Central: 5226730
Affiliations:
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Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Szymczyk, Patrycja" sort="Szymczyk, Patrycja" uniqKey="Szymczyk P" first="Patrycja" last="Szymczyk">Patrycja Szymczyk</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Center for Advanced Manufacturing Technologies (CAMT/FPC), Faculty of Mechanical Engineering, Wroclaw University of Technology, Wroclaw, Poland</addr-line></nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Center for Advanced Manufacturing Technologies (CAMT/FPC), Faculty of Mechanical Engineering, Wroclaw University of Technology, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Zi Kowski, Grzegorz" sort="Zi Kowski, Grzegorz" uniqKey="Zi Kowski G" first="Grzegorz" last="Zi Kowski">Grzegorz Zi Kowski</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Center for Advanced Manufacturing Technologies (CAMT/FPC), Faculty of Mechanical Engineering, Wroclaw University of Technology, Wroclaw, Poland</addr-line></nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Center for Advanced Manufacturing Technologies (CAMT/FPC), Faculty of Mechanical Engineering, Wroclaw University of Technology, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Karuga Kuzniewska, Ewa" sort="Karuga Kuzniewska, Ewa" uniqKey="Karuga Kuzniewska E" first="Ewa" last="Karuga-Kuzniewska">Ewa Karuga-Kuzniewska</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Division of Infectious Diseases of Animals and Veterinary Administration, Wroclaw University, Wroclaw, Poland</addr-line></nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Division of Infectious Diseases of Animals and Veterinary Administration, Wroclaw University, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Smutnicka, Danuta" sort="Smutnicka, Danuta" uniqKey="Smutnicka D" first="Danuta" last="Smutnicka">Danuta Smutnicka</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Pharmaceutical Microbiology and Parasitology, Wroclaw Medical University, Wroclaw, Poland</addr-line></nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Department of Pharmaceutical Microbiology and Parasitology, Wroclaw Medical University, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Bil Lula, Iwona" sort="Bil Lula, Iwona" uniqKey="Bil Lula I" first="Iwona" last="Bil-Lula">Iwona Bil-Lula</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Clinical Chemistry, Wroclaw Medical University, Wroclaw, Poland</addr-line></nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Department of Clinical Chemistry, Wroclaw Medical University, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Bartoszewicz, Marzenna" sort="Bartoszewicz, Marzenna" uniqKey="Bartoszewicz M" first="Marzenna" last="Bartoszewicz">Marzenna Bartoszewicz</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Department of Pharmaceutical Microbiology and Parasitology, Wroclaw Medical University, Wroclaw, Poland</addr-line></nlm:aff><country xml:lang="fr">Pologne</country><wicri:regionArea>Department of Pharmaceutical Microbiology and Parasitology, Wroclaw Medical University, Wroclaw</wicri:regionArea><wicri:noRegion>Wroclaw</wicri:noRegion></affiliation></author><author><name sortKey="Mahabady, Susan" sort="Mahabady, Susan" uniqKey="Mahabady S" first="Susan" last="Mahabady">Susan Mahabady</name><affiliation wicri:level="4"><nlm:aff id="aff005"><addr-line>Center for Biofilms and Craniofacial Molecular Biology, Ostrow School of Dentistry of University of Southern California, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Biofilms and Craniofacial Molecular Biology, Ostrow School of Dentistry of University of Southern California, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region><settlement type="city">Los Angeles</settlement></placeName><orgName type="university">Université de Californie du Sud</orgName></affiliation></author><author><name sortKey="Sedghizadeh, Parish Paymon" sort="Sedghizadeh, Parish Paymon" uniqKey="Sedghizadeh P" first="Parish Paymon" last="Sedghizadeh">Parish Paymon Sedghizadeh</name><affiliation wicri:level="4"><nlm:aff id="aff005"><addr-line>Center for Biofilms and Craniofacial Molecular Biology, Ostrow School of Dentistry of University of Southern California, Los Angeles, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Center for Biofilms and Craniofacial Molecular Biology, Ostrow School of Dentistry of University of Southern California, Los Angeles, California</wicri:regionArea><placeName><region type="state">Californie</region><settlement type="city">Los Angeles</settlement></placeName><orgName type="university">Université de Californie du Sud</orgName></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Bone infections are a significant public health burden associated with morbidity and mortality in patients. Microbial biofilm pathogens are the causative agents in chronic osteomyelitis. Research on the pathogenesis of osteomyelitis has focused on indirect bone destruction by host immune cells and cytokines secondary to microbial insult. Direct bone resorption by biofilm pathogens has not yet been seriously considered. In this study, common osteomyelitis pathogens (<italic>Staphylococcus aureus</italic>, <italic>Pseudomonas aeruginosa</italic>, <italic>Candida albicans</italic>, and <italic>Streptococcus mutans</italic>) were grown as biofilms in multiple <italic>in vitro</italic> and <italic>ex vivo</italic> experiments to analyze quantitative and qualitative aspects of bone destruction during infection. Pathogens were grown as single or mixed species biofilms on the following substrates: hydroxyapatite, rat jawbone, or polystyrene wells, and in various media. Biofilm growth was evaluated by scanning electron microscopy and pH levels were monitored over time. Histomorphologic and quantitative effects of biofilms on tested substrates were analyzed by microcomputed tomography and quantitative cultures. All tested biofilms demonstrated significant damage to bone. Scanning electron microscopy indicated that all strains formed mature biofilms within 7 days on all substrate surfaces regardless of media. Experimental conditions impacted pH levels, although this had no impact on biofilm growth or bone destruction. Presence of biofilm led to bone dissolution with a decrease of total volume by 20.17±2.93% upon microcomputed tomography analysis, which was statistically significant as compared to controls (p <0.05, ANOVA). Quantitative cultures indicated that media and substrate did not impact biofilm formation (Kruskall-Wallis test, post-hoc Dunne’s test; p <0.05). Overall, these results indicate that biofilms associated with osteomyelitis have the ability to directly resorb bone. These findings should lead to a more complete understanding of the etiopathogenesis of osteomyelitis, where direct bone resorption by biofilm is considered in addition to the well-known osteoclastic and host cell destruction of bone.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Boody, Bs" uniqKey="Boody B">BS Boody</name></author><author><name sortKey="Jenkins, Tj" uniqKey="Jenkins T">TJ Jenkins</name></author><author><name sortKey="Maslak, J" uniqKey="Maslak J">J Maslak</name></author><author><name sortKey="Hsu, Wk" uniqKey="Hsu W">WK Hsu</name></author><author><name sortKey="Patel, Aa" uniqKey="Patel A">AA Patel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sanders, J" uniqKey="Sanders J">J Sanders</name></author><author><name sortKey="Mauffrey, C" uniqKey="Mauffrey C">C Mauffrey</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Maffulli, N" 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Mitchell</name></author><author><name sortKey="Quinton, Js" uniqKey="Quinton J">JS Quinton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cassat, Je" uniqKey="Cassat J">JE Cassat</name></author><author><name sortKey="Hammer, Nd" uniqKey="Hammer N">ND Hammer</name></author><author><name sortKey="Campbell, Jp" uniqKey="Campbell J">JP Campbell</name></author><author><name sortKey="Benson, Ma" uniqKey="Benson M">MA Benson</name></author><author><name sortKey="Perrien, Ds" uniqKey="Perrien D">DS Perrien</name></author><author><name sortKey="Mrak, Ln" uniqKey="Mrak L">LN Mrak</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Krzy Ciak, W" uniqKey="Krzy Ciak W">W Krzyściak</name></author><author><name sortKey="Jurczak, A" uniqKey="Jurczak A">A Jurczak</name></author><author><name sortKey="Ko Cielniak, D" uniqKey="Ko Cielniak D">D Kościelniak</name></author><author><name sortKey="Bystrowska, B" uniqKey="Bystrowska B">B Bystrowska</name></author><author><name sortKey="Skalniak, A" uniqKey="Skalniak A">A Skalniak</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Falsetta, Ml" uniqKey="Falsetta M">ML Falsetta</name></author><author><name sortKey="Klein, Mi" uniqKey="Klein M">MI Klein</name></author><author><name sortKey="Colonne, Pm" uniqKey="Colonne P">PM Colonne</name></author><author><name sortKey="Scott Anne, K" uniqKey="Scott Anne K">K Scott-Anne</name></author><author><name sortKey="Gregoire, S" uniqKey="Gregoire S">S Gregoire</name></author><author><name sortKey="Pai, Ch" uniqKey="Pai C">CH Pai</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gellatly, Sl" uniqKey="Gellatly S">SL Gellatly</name></author><author><name sortKey="Hancock, Re" uniqKey="Hancock R">RE Hancock</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Brady, Ra" uniqKey="Brady R">RA Brady</name></author><author><name sortKey="Leid, Jg" uniqKey="Leid J">JG Leid</name></author><author><name sortKey="Calhoun, Jh" uniqKey="Calhoun J">JH Calhoun</name></author><author><name sortKey="Costerton, Jw" uniqKey="Costerton J">JW Costerton</name></author><author><name sortKey="Shirtliff, Me" uniqKey="Shirtliff M">ME Shirtliff</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Pologne</li><li>États-Unis</li></country><region><li>Californie</li></region><settlement><li>Los Angeles</li></settlement><orgName><li>Université de Californie du Sud</li></orgName></list><tree><country name="Pologne"><noRegion><name sortKey="Junka, Adam" sort="Junka, Adam" uniqKey="Junka A" first="Adam" last="Junka">Adam Junka</name></noRegion><name sortKey="Bartoszewicz, Marzenna" sort="Bartoszewicz, Marzenna" uniqKey="Bartoszewicz M" first="Marzenna" last="Bartoszewicz">Marzenna Bartoszewicz</name><name sortKey="Bil Lula, Iwona" sort="Bil Lula, Iwona" uniqKey="Bil Lula I" first="Iwona" last="Bil-Lula">Iwona Bil-Lula</name><name sortKey="Karuga Kuzniewska, Ewa" sort="Karuga Kuzniewska, Ewa" uniqKey="Karuga Kuzniewska E" first="Ewa" last="Karuga-Kuzniewska">Ewa Karuga-Kuzniewska</name><name sortKey="Smutnicka, Danuta" sort="Smutnicka, Danuta" uniqKey="Smutnicka D" first="Danuta" last="Smutnicka">Danuta Smutnicka</name><name sortKey="Szymczyk, Patrycja" sort="Szymczyk, Patrycja" uniqKey="Szymczyk P" first="Patrycja" last="Szymczyk">Patrycja Szymczyk</name><name sortKey="Zi Kowski, Grzegorz" sort="Zi Kowski, Grzegorz" uniqKey="Zi Kowski G" first="Grzegorz" last="Zi Kowski">Grzegorz Zi Kowski</name></country><country name="États-Unis"><region name="Californie"><name sortKey="Mahabady, Susan" sort="Mahabady, Susan" uniqKey="Mahabady S" first="Susan" last="Mahabady">Susan Mahabady</name></region><name sortKey="Sedghizadeh, Parish Paymon" sort="Sedghizadeh, Parish Paymon" uniqKey="Sedghizadeh P" first="Parish Paymon" last="Sedghizadeh">Parish Paymon Sedghizadeh</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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