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Ubiquity of Biofilms on Penile Prostheses: Paradigm Shifts in Understanding of Device-Related Infection
By: Bradley J. Roth, BS, Cleveland Clinic Foundation, Ohio; Glenn T. Werneburg, MD, PhD, Cleveland Clinic Foundation, Ohio; Aaron W. Miller, PhD, Cleveland Clinic Foundation, Ohio; Petar Bajic, MD, Cleveland Clinic Foundation, Ohio | Posted on: 05 Apr 2024
The penile prosthesis microbiome has been an area of increasingly active research. It was previously believed that biofilms, which are communities of microbial organisms that adhere to each other and a surface, were inherently associated with prosthesis infection.1,2 However, studies recently published by our group have questioned these conclusions.
The earliest of these studies was centered around the hypothesis that penile biofilm composition would differ based on clinical indication for explantation.3 In this study, 27 patients had penile prosthesis explanted for a variety of reasons including infection, pain, and mechanical failure. We swabbed the first encountered area of the device components and utilized subcutaneous tissue swabs as controls. We found that β-diversity, the similarity between microbial communities based on the presence/absence of specific microbes and their relative abundances, was not significantly different (P = .16) no matter the indication for explantation. Astonishingly, increased species richness (the degree of diversity) was associated with increased indwelling time and lower likelihood of infection. Put plainly, devices that remained implanted longer were less likely to become infected but showed a more diverse community of microbes on their surface. Metabolomic analyses, using mass spectrometry, demonstrated that Staphylococcus and Escherichia/Shigella were similarly enriched in the presence and absence of infection. While these organisms are commonly identified in culture-based studies of inflatable penile prosthesis infection,4 our results demonstrate that it is not the simple presence of these uropathogens and their associated biofilms that lead to infection. Thus, the ubiquity of microbes, along with their respective biofilms and metabolites found in this study, refutes the dogma that biofilms always lead to infection and that biofilm prevention will prevent infectious sequelae.
We followed this study with a more robust approach to sampling and evaluating biofilms.5 In this study we sampled all device components (cylinders, pump, and reservoir) and utilized sonication of whole device components to remove biofilms. We identified biofilms via scanning electron microscopy throughout our samples regardless of infection status, validating the results of our prior study. Interestingly, 16S ribosomal RNA sequencing, which evaluates bacterial RNA only, demonstrated significantly different biofilm composition based on infection status (P = .001). When this analysis was repeated using more inclusive shotgun metagenomics (nonspecific sequencing of all microbial genes6), biofilm composition was similar regardless of indication for removal. Key results from this study found that biofilm composition, again measured by β-diversity, differed based on device manufacturer and between individual patients. This significance held across both 16S ribosomal RNA sequencing and shotgun metagenomics. Overall, the findings of this study add credence to the results of our earlier work and affirm that biofilms are found on all prosthesis device components. Furthermore, there appear to be underlying patient and device component factors driving differences in biofilm composition.
Altogether, our studies provide solid evidence for the presence of biofilms on both infected and noninfected penile prostheses. What remains unknown is the significance of biofilms on noninfected devices, and more importantly, what disruptions occur in the postimplant microbiome that lead to specific clinical sequelae like infection or pain. Future studies aimed at testing these disruptions may help elucidate why certain devices become infected while others do not. Doing so may inform future work aimed at making safer device coatings and preventing or treating clinical infections. We hope our work provides the foundation for future research to examine biofilms differently, and not solely as an indicator of infection.
- Wilson SK, Gross MS. Biofilm and penile prosthesis infections in the era of coated implants: 2021 update. Int J Impot Res. 2022;34(5):411-415.
- Chung PH, Leong JY, Phillips CD, Henry GD. Microorganism profiles of penile prosthesis removed for infection, erosion, and mechanical malfunction based on next-generation sequencing. J Sex Med. 2022;19(2):356-363.
- Werneburg GT, Lundy SD, Hettel D, et al. Microbe-metabolite interaction networks, antibiotic resistance, and in vitro reconstitution of the penile prosthesis biofilm support a paradigm shift from infection to colonization. Sci Rep. 2023;13(1):11522.
- Bole R, Habashy E, Yang D, et al. Timing and causative organisms associated with modern inflatable penile prosthesis infection: an institutional retrospective. J Sex Med. 2023;20(1):107-112.
- Werneburg GT, Adler A, Khooblall P, et al. Penile prostheses harbor biofilms driven by individual variability and manufacturer even in the absence of clinical infection. J Sex Med. 2023;20(12):1431-1439.
- Quince C, Walker AW, Simpson JT, Loman NJ, Segata N. Shotgun metagenomics, from sampling to analysis. Nat Biotechnol. 2017;35(9):833-844.
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