Features
How bacterial biofilms can affect breast implants
A growing body of research has implicated bacteria as a major cause of implant failure. A Jacombs, J Allan, P Valente, K Vickery and AK Deva summarise recent findings related to bacterial contamination of breast implants by bacterial biofilms and their importance in causing capsular contracture
There is a more detailed understanding of the interaction of bacterial biofilms in many chronic and recurrent diseases and, in particular, infections and device failures of surgically implanted medical devices (IMD). Biofilms occur when micro-organisms contact surfaces. They quickly transform from a free-floating (or planktonic) state into a sessile form that uses a sticky exopolysaccharide (EPS) complex to bind irreversibly to the surface.
The combination of bacteria encased by their own protective proteins bound irreversibly onto a surface is termed bioflim. The biofilm state confers several advantages to these bacteria, including protection from host immune systems and antibiotic therapy, the ability to capture nutrients and remove waste, the ability to exchange genetic material and ultimately the ability respond to changes in the surrounding environment to ensure survival.
Structure
When bacteria first contact a surface, the attachment is mediated by physico-chemical factors such as Van der Waals forces and is reversible. If the interaction is favourable for attraction, then bacteria bind irreversibly to the surface by producing EPS that interlocks specific bacterial cell wall receptors to the surface. Growth and maturation of the biofilm result in complex three-dimensional structures consisting of cell clusters linked by EPS or mucoid slime, interspersed by connecting channels that allow transport of water and nutrients.
Cell-to-cell communication, or quorum sensing, is pivotal to the development and maintenance of these biofilm structures. Quorum sensing is a cell density-dependent signalling system mediated by bacterial chemical autoinducer molecules that regulate bacterial transcription. Once a mature biofilm is formed, surface bacteria are able to break off to form planktonic organisms that allow seeding further upstream or downstream from the original colony. Some organisms such as staphylococcus epidermidis and pseudomonas aeruginosa are more capable of forming biofilms. Additionally, biofilms can exist as mono or multispecies constructs.
Capsular contracture remains the most common complication following breast augmentation, with a reported incidence of 0.5–30% in reported series. The cause of capsular contracture remains uncertain but several hypotheses have been advanced. These include implant surface characteristics, placement of the prosthesis, haemaetoma, trauma, silicone leakage and subclinical infection.
The infectious hypothesis has gained widespread acceptance as the cause of most contractures. This is based on both clinical and research studies that have shown an association between the presence of bacteria and high grade capsular contracture. Staphylococcu epidermidis is the most commonly isolated organism from studies of contracted capsules.
Our laboratory has utilised an in vivo pig model to investigate the relationship between sub-clinical implant infection, biofilm formation and the development of capsular contracture. Fifty-one miniature breast implants were inserted into six pigs, 36 into submammary pockets that had been inoculated with staphylococcu epidermidis, and 15 into uninocculated (control) pockets.
Pocket inoculation was significantly associated with biofilm formation (p = 0.00950) confirmed by positive bacterial growth and scanning electron microscopy (SEM) imaging on 26 of the 36 (72.2%) of inoculated implants. Capsular contracture (Baker III/IV) was observed 77.8% (28/36) of the inoculated pockets compared with 46.7% (7/15) of the controls (p = 0.0291). Univariate analysis showed that pocket inoculation was associated with a five-fold increase in the risk of forming biofilm, and a four-fold increase in the risk of forming capsular contracture. None of the pigs ever showed evidence of clinical infection.
Seven of the uninoculated controls developed contracture. Analysis of these capsules showed biofilm formation on four grade III/IV contractures, and one grade II contracture. Staphylococcus spp isolated were native porcine subtypes. Predominate isolates from both capsules and implants were coagulase negative staphylococci (CoNS), which included staphylococcu epidermidis and porcine sub types. Seven of the inoculated implants developed contracture, although scanning electron microscopy (SEM) did not demonstrate biofilm formation.
Capsular contracture in this animal model was significantly associated bacterial biofilms (p = 00213). This finding was independent of whether the bacteria were inoculated or of pig origin and reinforces the hypothesis that bacterial biofilms on the surface of breast implants leads to the development of capsular contracture. Univariate analysis showed that the presence of biofilm was associated with a four-fold increased risk in developing contracture. Consequently, any efforts to reduce implant contamination by biofilm could be an important strategy in prevention of contracture.
Strategies such as the use of prophylactic antibiotics at the time of anaesthetic induction, antibiotic pocket irrigation and the avoidance of a transareolar incision have been shown to reduce bacterial contamination at the time of implant placement and have been supported by clinical and laboratory studies. These should now be used as standard practice in breast augmentation surgery.
Other strategies such as an introduction sleeve to isolate the nipple areola complex during surgery and frequently changing outer gloves should be considered to reduce the risk of biofilm contamination.
Other IMDs
Bacterial biofilms have been identified on most surgically implanted prosthetic devices (see table). Research shows that biofilm-related infections remain the major cause of ureteral stent failure and complications while orthopaedic implant and fracture fixation device infections and failures account for the vast majority of all surgical biofilm IMD infections. Biofilm infections complicating cardiovascular procedures have the highest mortality, ranging from 5% for vascular grafts and 7% for pacemakers and greater that 25% in cardiac-assist devices.
Mortality for non-cardiovascular surgical IMD is much lower at 3%. However, large numbers of patients receive urinary catheters, and up to 25% of these developed bacteruria, 24% become symptomatic and 3-6% develop bacteraemia, with a mortality rate approaching 30%. Failure of other non-cardiovascular implants, while exhibiting low mortality, are associated with significant disability, for orthopaedic and neurosurgical shunts, and disfigurement and psychological trauma with breast and inflatable penile implants.
Multiple different bacteria have been identified and prominent pathogens are commonly commensal flora or nosocomial in origin. Gram positive cocci, s aureus and CoNS, are most the most prevalent infective organisms found on IMD surfaces (see table). S. aureus biofilm infections tend to present earlier as they produce multiple toxins and enzymes that result in an acute inflammatory response and tissue damage.
By contrast, CoNS biofilm infection follows a chronic disease pattern that is often difficult to diagnose and treat. Commensal and opportunistic fungal biofilm infections, including candida and aspergillus species, are much less common, accounting for less than 10% of medical implant infections, but have a mortality rate approaching 50%.
This article has shown that for breast implants, bacterial biofilms have now been shown to be a significant cause of contracture. Surgeons need to be aware of the role of bacterial biofilms in IMD failure and be on the lookout for technologies being investigated by our group and others that will, no doubt, be translated into clinical practice in the near future.
A Jacombs, J Allan, P Valente, K Vickery and associate professor Anand Deva BSc (Med, MBBS (Hons), MS, FRACS, head, cosmetic plastic and reconstructive surgery, surgical infection research group, Australian School of Advanced Medicine,
Macquarie University, Sydney, Australia. All correspondence to Anand.deva@mq.edu.au
