The Influence of Patterned Surface Features on the Accumulation of Bovine Synovial Fluid-Induced Aggregates of Staphylococcus aureus

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_w = 0.0012 Pa) but minimal detachment from the patterned surfaces, even at flow rates as high as 13.9 mL/min (τ_w = 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.