Reduced bacterial adhesion on ceramics used for arthroplasty applications

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Abstract

Orthopaedic-implant-related infections are challenging for clinicians: despite progresses in surgical procedures, the mortality rate of patients experiencing periprosthetic joint infections still ranges from 10 to 18%. Generally, infection starts when planktonic bacteria arising from surgery escape immunological surveillance adhering onto implant surface. Bacterial adhesion depends mainly on material’s intrinsic surface features depending on its chemical and physical properties. This study compares materials used for bearings of total hip arthroplasty, advanced ceramics (alumina and zirconia-platelet toughened alumina composites), metals (cobalt–chromium–molybdenum alloy) and polymers (highly cross-linked polyethylene), in terms of wettability and protein adsorption. Materials were infected with Staphylococcus aureus and Staphylococcus epidermidis biofilm for 24 or 48 h. Bacterial adhesion properties were evaluated by means of biofilm viability, morphology, and thickness, in a worst-case surface roughness condition. Thanks to selective protein adsorption, bioceramics reduced bacterial adhesion and subsequent biofilm formation more effectively in comparison with metal and polymer surfaces.

Introduction

Implant-related infections are one of the most common reasons for surgical failure (14–29% of total failures) [1], in most cases causing severe disability and leading to a significant reduction in the patient’s quality of life. According to the most recent surveys, the mortality rate of patients undergoing primary implant infections ranges from 10 to 18% [2], [3], [4]; moreover, if an infection occurs also in the revised implants, this percentage can double or triple [5], [6]. In the US alone, more than a million hip and knee arthroplasties are performed yearly [7]. Similarly, the number of patients undergoing orthopaedic surgery in Europe is now almost 200 per 100,000 inhabitants [8], [9], and has been steadily increasing over the last 10 years. Due to increasing life expectancy, the World Health Organization (WHO) foresees that osteoarthritis will be the fourth leading cause of disability by 2020.

Total hip or knee arthroplasty still remains the only applicable solution to improve the quality of life of joint-affected patients [10]. However, despite marked progresses in joint replacement surgery, the infection rate during the first 2 years is about 1% for primary implant failures, and 2% after knee replacement [3], [4]; moreover, due to the development of multi- or pan- drug-resistant bacterial strains, these rates are expected to rise in the near future. Hospital-acquired infections are now generally considered to be the third-largest cause affecting public health; they are chiefly caused by a group of multi-drug resistant (MDR) pathogenic biofilm producer strains, known as “ESKAPE” (in the acronym of the Infectious Diseases Society of America (IDSA) that identifies the emerging MDR strains Enterococcus faecium, Staphylococcus aureus, Klebsiellapneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp.) [11], [12]. Unfortunately, orthopaedic medical devices are not an exception, as they are highly subject to biofilm infections, which generally lead to the need for their removal and replacement. The presence of an implant reduces the bacterial concentration needed to induce infection by 100,000 times [1], since bacteria can survive in the periprosthetic environment by adhering to the implant. The necessity to find a post-antibiotic solution to periprosthetic joint infections may thus be relatively urgent.

Biofilm formation begins when planktonic bacteria, originating from the surgical incision site or from independent infection sources, escape immunological surveillance and adhere onto the implant surface [2]. Once adherent, bacteria proliferate and secrete different kinds of macromolecules, principally polysaccharides and glycolipids, known as extracellular polymeric substances (EPS), which embed and protect the neo-forming bacteria community [13]. Mature biofilm not only shields bacteria from the host immune system, but also undermines the effectiveness of antibiotics by up to one thousand times compared to planktonic cells. As a consequence, antibiotic treatment of implant-related infections frequently fails, with consequent implant loss and soft tissue invasion by bacterial communities [14], [15]. Although biofilms generally contain several different bacterial strains, the most common ones belong to the Staphylococcus genus: S. epidermidis and S. aureus (together with Pseudomonas aeruginosa), are responsible for three out of four cases of medical-device-related infection [2]. Accordingly, the most reliable way to reduce the poor outcome of medical device infections is to prevent bacterial adhesion to implant surfaces, thus reducing the development of mature biofilm.

Although the bacterial strains involved in implant contamination are often host commensals, the adhesion of bacteria to the implant surface depends on many factors related to the biomaterial’s intrinsic properties, particularly its chemistry and physical properties (e.g. roughness, surface charge, wettability). It is thus crucial to study in depth the surface features of medical devices, with the aim of improving them in order to avoid bacterial proliferation on their surface.

Metals (Ti-6Al-4V, CoCrMo and stainless steel), polymers (poly(methyl methacrylate, PMMA), ultrahigh-molecular-weight polyethylene (UHMWPE), and ceramics (alumina, zirconia, alumina matrix composites and hydroxyapatite) are the three classes of materials commonly used for orthopaedic implants [16]. Whereas metals are the most widely used material in implantology, some retrospective studies have shown that they are more prone to bacterial adhesion than are ceramics [17], [18], [19]. In addition, both metals and polymers are usually affected by significant time-dependent surface degradation, leading to the significant increase of bacterial adhesion (enabled by surface roughening) and various other adverse events caused by the release of ions and particles [17], [18], [19]. In contrast, bioceramics, mainly used as bearing couples in artificial joints, have little tendency to degradation, and present peculiar physical-chemical surface properties that are potentially responsible for their antifouling features [20]. Although of crucial importance, there is no literature so far on comparing intrinsic antibacterial properties of systems actually used in orthopaedics.

In this study, monolithic alumina and zirconia-platelet toughened alumina (ZPTA) were compared to metallic cobalt–chromium–molybdenum (CoCrMo) and polymeric cross-linked polyethylene (XLPE) materials, assessing wettability, protein adsorption, and bacterial adhesion. These materials were selected for testing as being among the most widely used for artificial joint applications in hip, knee, and shoulder arthroplasty. Experiments were performed without accomplishing any specimens polishing practice in order to simulate the worst-case in-vivo scenario present in current orthopaedic implants to indisputably focus onto bare selected materials antibacterial properties.S. aureus and S. epidermidis biofilms were then cultivated for 24 or 48 h on the test materials’ surface, and evaluated in terms of viability, morphology, and thickness.

Section snippets

Samples

The samples comprised: ceramics, both monolithic alumina (Al2O3; ISO 6474-1) and zirconia-platelet toughened alumina (ZPTA; ISO 6474-2), marketed under the brand name BIOLOX®forte and BIOLOX®delta, respectively; metal cobalt–chromium–molybdenum (CoCrMo, ISO 5832-12) and cross-linked polyethylene (XLPE, ISO 5834-2); all were provided by CeramTec (CeramTec GmbH, Plochingen, Germany) as disks 2 cm in diameter, 6 mm thick. Bare specimens were voluntarily not further polished in order to mimic

Wettability

Fig. 2 shows the results of the contact angle assay, indicating specimens’ wettability. The ceramics (Alumina and ZPTA) showed the lowest contact angle; there was no statistical difference between the two types tested (t-test, p > 0.05). Preston et al. showed that oxides exhibit superhydrophilicity (≈0°angle) when no contamination is present [24]. However, this condition is not permanent, and upon exposure to the environment, hydrocarbon adsorption layers cover the surface, increasing the contact

Discussion

Septic failure, secondary to either primary or secondary implant contamination, is still one of the main threats to health, increasing the incidence of patient morbidity and mortality, and alarming healthcare authorities [6]. Whereas it is well known that the primary event in the contamination of materials is the interaction of prokaryotic cells with the material surface and their adhesion thereto [2], it is indispensable to investigate the adhesion mechanisms between bacteria and biomaterial

Conclusion

Ceramic specimens show reduced bacterial adhesion and slower biofilm development with both strains tested (S. aureus and S. epidermidis) compared to CoCrMo and XLPE. This was particularly evident when the dense biofilm morphology was visualized by SEM on CoCrMo and XLPE. Conversely, bacterial adhesion, viability and biofilm thickness were markedly reduced in the ceramic alumina and ZPTA specimens, thanks to their physicochemical properties. Accordingly, the current ceramic materials used in

Summary of novel conclusions

Thanks to selective protein adsorption, bioceramics reduced bacterial adhesion and subsequent biofilm formation more effectively in comparison with metal and polymer surfaces.

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