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The Influence of Patterned Surface Features on the Accumulation of Bovine Synovial Fluid-Induced Aggregates of
Niraj Gupta1, Tripti Thapa Gupta1, Khushi Patel2
1Department of Microbial Infection and Immunity, The Ohio State Universitygrid.261331.4, Columbus, Ohio, USA.
Abstract:
Periprosthetic joint infection (PJI) after joint replacement is a major clinical issue requiring multiple surgeries and antibiotic interventions. Recent in vitro research has shown that PJI staphylococcal strains rapidly form antibiotic-resistant free-floating aggregates in the presence of bovine synovial fluid (BSF). Staphylococcal aggregates are also present in human PJI joint fluid. However, the influence of surface roughness and fluid shear on the attachment and retention of such aggregates on surfaces is not known. Our aim was to assess how surface roughness and fluid shear stress influenced the attachment and retention of Staphylococcus aureus BSF-mediated aggregates on smooth- and rough-patterned titanium in flow cells compared to nonaggregated cells. The attachment of S. aureus aggregates was significantly greater than that of single cells but was independent of surface roughness; however, on the patterned surfaces, aggregates preferentially accumulated in the grooves. Fibrous components in the BSF were also colocalized with the grooves. After a 24-h attachment-and-incubation period, different shear stresses were applied. There was significant detachment from flat surfaces at a flow rate of 1 mL/min (τ = 0.0012 Pa) but minimal detachment from the patterned surfaces, even at flow rates as high as 13.9 mL/min (τ = 0.0169 Pa). The retention of bacterial aggregates and biofilms on rough surfaces exposed to shear might be an important consideration for the location of colonization on orthopedic implants, which can have wide ranges of roughness and surface features and can influence the efficacy of shear-based debridement methods such as pulse lavage. IMPORTANCE Periprosthetic joint infections occurring after joint replacement are a major clinical problem requiring repeated surgeries and antibiotic interventions. Staphylococcus aureus is the most prominent bacterium causing most implant-related infections. S. aureus can form a biofilm, which is defined as a group of attached bacteria with the formation of an envelope that is resistant to antibiotics. The attachment and retention of these bacteria on implant surfaces are not clearly understood. Recent in vitro research investigations have shown that staphylococcal strains rapidly form aggregates in the presence of bovine synovial fluid (BSF) in the joints, which allows bacteria time to attach to the implant surface, leading to biofilm formation. Thus, in this study, we examined the attachment of aggregates on titanium surfaces with varying roughnesses and found robust bacterial attachment and retention along the ridges and grooves, which colocalized with the deposition of fibrous components present in the BSF.
Insights
Periprosthetic joint infections (PJI) involve Staphylococcus aureus aggregates that readily attach to implant surfaces. Surface patterns, not roughness, influence aggregate retention, impacting biofilm formation and treatment strategies for PJI.
Area of Science:
- Biomedical Engineering
- Microbiology
- Orthopedic Surgery
Background:
- Periprosthetic joint infection (PJI) is a significant complication following joint replacement surgery.
- Staphylococcus aureus forms antibiotic-resistant aggregates in synovial fluid, contributing to PJI.
- Understanding bacterial aggregate behavior on implant surfaces is crucial for PJI prevention and treatment.
Purpose of the Study:
- To investigate the influence of surface roughness and fluid shear on Staphylococcus aureus aggregate attachment and retention on titanium surfaces.
- To compare the behavior of aggregated versus non-aggregated S. aureus cells.
- To assess the role of bovine synovial fluid (BSF) components in aggregate adhesion.
Main Methods:
- Utilized flow cells with smooth and rough-patterned titanium surfaces.
- Exposed Staphylococcus aureus aggregates and single cells to bovine synovial fluid (BSF).
- Applied varying fluid shear stresses to quantify bacterial aggregate detachment.
Main Results:
- S. aureus aggregates showed significantly greater attachment than single cells, irrespective of surface roughness.
- Aggregates preferentially accumulated in the grooves of patterned surfaces, where BSF fibrous components also localized.
- Patterned surfaces exhibited significantly higher aggregate retention under shear stress compared to flat surfaces.
Conclusions:
- Bacterial aggregate retention on implant surfaces is influenced by surface topography, particularly grooves, rather than overall roughness.
- The findings highlight the importance of surface features in PJI pathogenesis and debridement efficacy.
- Targeting aggregate formation and retention mechanisms could offer novel PJI therapeutic strategies.

