Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization
Abstract To understand differences between asymptomatic colonized and infected states of indwelling medical devices, we sought to determine penile prosthesis biofilm composition, microbe-metabolite interaction networks, and association with clinical factors. Patients scheduled for penile prosthesis...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-07-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-38750-1 |
| _version_ | 1797774216062304256 |
|---|---|
| author | Glenn T. Werneburg Scott D. Lundy Daniel Hettel Petar Bajic Bradley C. Gill Ava Adler Sromona D. Mukherjee Hadley M. Wood Kenneth W. Angermeier Daniel A. Shoskes Aaron W. Miller |
| author_facet | Glenn T. Werneburg Scott D. Lundy Daniel Hettel Petar Bajic Bradley C. Gill Ava Adler Sromona D. Mukherjee Hadley M. Wood Kenneth W. Angermeier Daniel A. Shoskes Aaron W. Miller |
| author_sort | Glenn T. Werneburg |
| collection | DOAJ |
| description | Abstract To understand differences between asymptomatic colonized and infected states of indwelling medical devices, we sought to determine penile prosthesis biofilm composition, microbe-metabolite interaction networks, and association with clinical factors. Patients scheduled for penile prosthesis removal/revision were included. Samples from swabbed devices and controls underwent next-generation sequencing, metabolomics, and culture-based assessments. Biofilm formation from device isolates was reconstituted in a continuous-flow stir tank bioreactor. 93% of 27 analyzed devices harbored demonstrable biofilm. Seven genera including Faecalibaculum and Jeotgalicoccus were more abundant in infected than uninfected device biofilms (p < 0.001). Smokers and those with diabetes mellitus or cardiac disease had lower total normalized microbial counts than those without the conditions (p < 0.001). We identified microbe-metabolite interaction networks enriched in devices explanted for infection and pain. Biofilm formation was recapitulated on medical device materials including silicone, PTFE, polyurethane, and titanium in vitro to facilitate further mechanistic studies. Nearly all penile prosthesis devices harbor biofilms. Staphylococcus and Escherichia, the most common causative organisms of prosthesis infection, had similar abundance irrespective of infection status. A series of other uncommon genera and metabolites were differentially abundant, suggesting a complex microbe-metabolite pattern–rather than a single organism–is responsible for the transition from asymptomatic to infected or painful states. |
| first_indexed | 2024-03-12T22:17:48Z |
| format | Article |
| id | doaj.art-5bfd8368e4424259b4c177c69b62c7e7 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-12T22:17:48Z |
| publishDate | 2023-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-5bfd8368e4424259b4c177c69b62c7e72023-07-23T11:13:23ZengNature PortfolioScientific Reports2045-23222023-07-0113111210.1038/s41598-023-38750-1Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonizationGlenn T. Werneburg0Scott D. Lundy1Daniel Hettel2Petar Bajic3Bradley C. Gill4Ava Adler5Sromona D. Mukherjee6Hadley M. Wood7Kenneth W. Angermeier8Daniel A. Shoskes9Aaron W. Miller10Department of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteDepartment of Urology, Cleveland Clinic Foundation, Glickman Urological and Kidney InstituteAbstract To understand differences between asymptomatic colonized and infected states of indwelling medical devices, we sought to determine penile prosthesis biofilm composition, microbe-metabolite interaction networks, and association with clinical factors. Patients scheduled for penile prosthesis removal/revision were included. Samples from swabbed devices and controls underwent next-generation sequencing, metabolomics, and culture-based assessments. Biofilm formation from device isolates was reconstituted in a continuous-flow stir tank bioreactor. 93% of 27 analyzed devices harbored demonstrable biofilm. Seven genera including Faecalibaculum and Jeotgalicoccus were more abundant in infected than uninfected device biofilms (p < 0.001). Smokers and those with diabetes mellitus or cardiac disease had lower total normalized microbial counts than those without the conditions (p < 0.001). We identified microbe-metabolite interaction networks enriched in devices explanted for infection and pain. Biofilm formation was recapitulated on medical device materials including silicone, PTFE, polyurethane, and titanium in vitro to facilitate further mechanistic studies. Nearly all penile prosthesis devices harbor biofilms. Staphylococcus and Escherichia, the most common causative organisms of prosthesis infection, had similar abundance irrespective of infection status. A series of other uncommon genera and metabolites were differentially abundant, suggesting a complex microbe-metabolite pattern–rather than a single organism–is responsible for the transition from asymptomatic to infected or painful states.https://doi.org/10.1038/s41598-023-38750-1 |
| spellingShingle | Glenn T. Werneburg Scott D. Lundy Daniel Hettel Petar Bajic Bradley C. Gill Ava Adler Sromona D. Mukherjee Hadley M. Wood Kenneth W. Angermeier Daniel A. Shoskes Aaron W. Miller Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization Scientific Reports |
| title | Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization |
| title_full | Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization |
| title_fullStr | Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization |
| title_full_unstemmed | Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization |
| title_short | Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization |
| title_sort | microbe metabolite interaction networks antibiotic resistance and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization |
| url | https://doi.org/10.1038/s41598-023-38750-1 |
| work_keys_str_mv | AT glenntwerneburg microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT scottdlundy microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT danielhettel microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT petarbajic microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT bradleycgill microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT avaadler microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT sromonadmukherjee microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT hadleymwood microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT kennethwangermeier microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT danielashoskes microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization AT aaronwmiller microbemetaboliteinteractionnetworksantibioticresistanceandinvitroreconstitutionofthepenileprosthesisbiofilmsupportaparadigmshiftfrominfectiontocolonization |