gms | German Medical Science

GMS German Plastic, Reconstructive and Aesthetic Surgery – Burn and Hand Surgery

Deutsche Gesellschaft der Plastischen, Rekonstruktiven und Ästhetischen Chirurgen (DGPRÄC)
Deutsche Gesellschaft für Verbrennungsmedizin (DGV)

ISSN 2193-7052

Infectious complications in implant based breast surgery and implications for plastic surgeons

Infektiöse Komplikationen bei alloplastischen Brustoperationen und Implikationen für Plastische Chirurgen

Review Article

  • corresponding author Raymund E. Horch - Plastisch- und Handchirurgische Klinik, Universitätsklinikum Erlangen, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany; Center for Breast Prosthesis Research, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany
  • Gregory Schultz - Institute for Wound Research, Department of Obstetrics and Gynecology, University of Florida, Gainesville, USA
  • Dirk W. Schubert - Lehrstuhl für Polymerwerkstoffe, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany; Center for Breast Prosthesis Research, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany
  • Marweh Schmitz - Plastisch- und Handchirurgische Klinik, Universitätsklinikum Erlangen, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany; Center for Breast Prosthesis Research, Friedrich-Alexander Universität Erlangen-Nürnberg, Erlangen, Germany

GMS Ger Plast Reconstr Aesthet Surg 2013;3:Doc04

doi: 10.3205/gpras000014, urn:nbn:de:0183-gpras0000146

Veröffentlicht: 4. Juli 2013

© 2013 Horch et al.
Dieser Artikel ist ein Open Access-Artikel und steht unter den Creative Commons Lizenzbedingungen (http://creativecommons.org/licenses/by-nc-nd/3.0/deed.de). Er darf vervielfältigt, verbreitet und öffentlich zugänglich gemacht werden, vorausgesetzt dass Autor und Quelle genannt werden.


Abstract

Implantation of breast prosthesis is still one of the most frequently performed breast reconstructing or contouring procedures.

Infectious complications and capsular contracture are inherent problems that may have different causes which are not clearly defined yet in terms of pathophysiology. Recent findings showed bacterial contamination as a major cause of implant failure. Since this has direct implications for the surgical management we report on biofilm development on alloplastic breast prostheses, characteristics and effects after implantation of medical devices in general. This article gives a review of the current literature and discusses possible issues to solve the problem of infection after implantation of breast prosthesis.

In conclusion the reinsertion of single-use devices should not be recommended and should be strictly avoided when a device related infection has occured. According to current knowledge contaminated implants should be removed, the infection then be cured and if necessary, a new prosthesis may be implanted after a regeneration period. Alternatively a change in therapy towards autologous tissue reconstruction should be considered if previous attempts with alloplastic prostheses have failed and if radiation therapy has worsened the local tissue situation in the recipient area.

Zusammenfassung

Implantationen von Brust-Prothesen sind für Brustrekonstruktionen oder Konturierungen noch immer die am häufigsten durchgeführten Verfahren. Typische inhärente Probleme sind dabei neben infektiösen Komplikationen die Kapselkontrakturen, deren unterschiedliche Ursachen bezüglich der Pathophysiologie noch nicht eindeutig geklärt sind.

Neuere Erkenntnisse weisen auf bakterielle Kontamination als eine der Hauptursachen von Implantatversagen hin. Da dies direkte Auswirkungen auf die chirurgische Behandlung hat, berichten wir über das Problem der Biofilmentwicklung auf alloplastischen Brustimplantaten sowie über deren Effekte nach Einsetzen von medizinischen Implantaten allgemein. Dieser Artikel gibt einen Überblick über die aktuelle Literatur und diskutiert mögliche Fragen der Problematik der Infektion nach der Implantation von Brust-Prothesen.

Zusammenfassend kann das Wiedereinsetzen von Implantaten für den Einmalgebrauch nicht empfohlen werden und sollte daher bei Verdacht auf eine Infektion unbedingt unterlassen werden. Nach derzeitigem Kenntnisstand sollten kontaminierte Implantate entfernt, eine bestehende Infektion zunächst ausgeheilt und, falls erforderlich, erst nach einer Regenerationsphase ein neues Implantat eingesetzt werden. Alternativ sollte immer auch ein Verfahrenswechsel auf eine Eigengewebsrekonstruktion in Betracht gezogen werden, insbesondere wenn vorherige alloplastische Verfahren versagt haben und die lokale Gewebesituation im Empfängergebiet etwa durch eine Strahlentherapie ungünstig ist.


Introduction

In recent literature there is a growing body of scientific evidence that bacteriae could be a major cause for implant failure [1], [2]. We have previously reviewed the biofilm problem with regard to late seroma and revisional breast surgery [3] and want to highlight this issue because not only in aesthetic procedures but also in breast reconstruction implants still play a considerable role [4]. In contrast to this procedure, usually no long term infectious problems are seen when restoring the breast mound with the patient’s own tissue. Through an increased standardization of autologous breast reconstruction surgery this alternative has become a routine procedure in the hands of experienced reconstructive surgeons and it is available to many patients in Europe when amputation of the breast or partial loss of breast tissue as a consequence of cancer therapy is experienced. In addition, when performed in high volume centers, free microsurgical transplantation of suitable tissue has been optimized rendering reliable results with a high rate of safety, even in previously irradiated patients [5], [6], [7]. Other future options, such as creating replacement tissue by means of tissue engineering and regenerative medicine seem highly promising but are not clinically available yet [8], [9], [10], [11], [12], [13], [14], [15], [16], [17]. Nevertheless on a worldwide perspective implant based alloplastic breast reconstructions with or without skin expansion is believed to account for the majority of procedures to restore breast shape and volume. Moreover despite the undoubtable benefits of autologous breast repair authors have even proclaimed a shift of paradigm towards increasing alloplastic reconstructions recently [18].

Breast implants are also used for aesthetic reasons, malformation of the breast, expanders followed by definitive implants in reconstructive surgery, prophylactic mastectomy due to BRCA 1 mutations. After skin sparing mastectomy (with still approximately 5% of remaining breast tissue) often a critical perfusion of the skin envelope is experienced. In these patients it is questionable if less perfused tissue may present a sufficient mechanical barrier against microorganisms. If the skin is irradiated this problem might become even more significant. Patients who had radiotherapy have a significantly higher incidence of subclinical infection than patients who did not [19], Oposite after a risk-reducing mastectomy with approximately 20–30% of remaining breast tissue a robust skin envelope remains that could act as a good mechanical barrier of microorganisms.

Among other well known side effects of breast implants, such as displacement, double bubble deformity, undue scarring, implant rupture, systemic spreading of silicone into the body [20] etc., the event of a capsular contracture remains an unsolved but serious clinical problem [21], [22], [23], [24], [25]. Up to now numerous attempts to prevent capsular contracture failed and did not achieve a reliable effect for clinical use [23], [26]. Following the so called PIP scandal numerous questions were brought up again whether we do know enough about the material properties and longevity of alloplastic breast implants, the mechanisms of capsular contracture [27], and the involvement of subclinical infectious processes, long term side effects such as the occurance of anaplastic large cell lymphoma cells in the periprosthetic fluid etc. [28], [29], [30], [31], [32], [33], [34], [35], [36].

Anecdotally it has been reported that bacterial colonization was detected in the seroma fluid of patients with capsular contracture [37], [38], but even when infection was clinically seen bacterial counts were not positive in all cases [1], [2], [39], [40], [41], [42], [43]. Researchers removed breast prostheses from capsular contracture grade III and IV, and sonication detected bacteria in 41% of removed breast implants. The identified bacteria belonged to normal skin flora [2]. Although further investigations will be needed to determine a true causal relation between biofilms and capsular fibrosis, the infectious hypothesis has gained widespread acceptance as one major cause of capsular contracture [1], [44]. According to Jacobs et al. this is based on both clinical and research studies that have shown an association between the presence of bacteria and high grade capsular contracture [45]. With a better understanding of the complex interactions of planctonic bacteria in biofilms [46] an increasing number of publications now focuses on the problems of bacterial contamination of chronic wounds and infected implants of any type [47]. Knowledge about the behavior of various bacteria within biofilms, their diagnosis and treatment options in dental medicine and in microbiology is constantly growing, but data on biofilms in breast implants are still scarce [47], [48], [49], [50], [51], [52], [53], [54], [55], [56]. In the literature there is no clear description of a correlation of the grade of capsular contractures and microbiological structures found in biofilms so far.


Biofilm development on devices

The detrimental effects of bacterial biofilms on medical devices have been established within the scientific literature to be responsible for persisting infections in concerned implants and recently have been shown to be responsible for non-healing chronic wounds too.

Electron microscopy of biopsies from chronic wounds found that 60% of the specimens contained biofilm structures in comparison with only 6% of biopsies from acute wounds. According to Philips et al. [57] biofilms are complex microbial communities that contain bacteria and fungi. The microorganisms synthesize and secrete a protective matrix that attaches the biofilm firmly to a vital or non-vital surface. Bacteria within biofilms interact with each other and exchange signals. This phenomenon has been termed “quorum sensing”. Cell-to-cell communication is pivotal to the development and maintenance of biofilm structures [45]. This system confers several advantages to these microorganisms, including protection from the host immune system and antibiotic treatment. Biofilms are considered to be dynamic heterogeneous communities which are continuously changing their composition [45]. They may consist of a single bacterial or fungal species, or more commonly, may be polymicrobial [58], [59], [60], [61], [62]. At the most basic level a biofilm can be described as bacteria embedded in a thick, slimy barrier of sugars and proteins. The biofilm barrier protects the microorganisms from external threats [57].

They have been for long time known to form on surfaces of medical devices, such as central venous lines, urinary catheters, endotracheal tubes, dental replacement materials and teeth, orthopaedic and breast implants, contact lenses, intrauterine devices sutures and dialysis catheters [63], [64], [65].

Biofilms were mainly found in aqueous systems, which are based on a water surface or on a boundary surface to a solid phase [35], [46]. Biofilms on teeth are well known under the term “plaque” [47]. They are assumed to be a major contributor to diseases that are characterized by an underlying bacterial infection and chronic inflammation, e.g. periodontal disease, cystic fibrosis, chronic acne and osteomyelitis. Microorganisms in biofilms excrete extracellular polymeric substances and form hydrogels in combination with water. Essentially, there are polysaccharides, proteins, lipids and nucleic acids that compose the film. The product can be seen as a slimy matrix in which nutrients and other substances are dissolved, and that gives a stable form to the biofilm.

Several steps have been characterized that are typical for the timing of biofilm formation. Various terms have been published to describe typical states of biofilm development and among them three time periods have been commonly accepted. These include an induction phase, agglomeration phase and the phase of existence (see Figure 1 [Fig. 1]).

Biofilm formation is a very complex, multistep process with microorganisms attraction and adhesion, with pluristratification of bacteria onto the artificial surface as the first and decisive step to a given surface [53] (Figure 1 [Fig. 1]). The first step requires the mediation of bacterial surface proteins, in which the main bacterium is S. aureus autolysin [38]. Free-floating microorganisms are attracted to dirty, wet surfaces and initially adhere to these surfaces using weak intermolecular van der Waals forces. If not physically separated from the surface immediately, these microorganisms “permanently” attach to such surfaces using cell adhesion molecules such as pili. Water coated surfaces provide better attachment conditions than dry surfaces. As the biofilm begins to form, an increasing number of microorganisms is attracted to cell adhesion sites [56], [57].

The second step is dominated by the growth period. As the biofilm grows, the structure is held together and protected by an excreted EPS (extracellular polymeric substance). As already mentioned biofilm molecules, often consist of many different Bacteria, and they communicate with one another using “quorum sensing” [56]. Quorum sensing, an interbacterial communication mechanism itself is dependent on population densit. The EPS protects the microorganisms living within and provides pathways for efficient communication between cells and microorganisms also undergo a genetic change when living within biofilms [57]. Several studies suggest that some cells such as E. coli become virtually immune to antibiotics due to a low level of metabolic activity. In their study from 2001 Stewart and Costerton have estimated that antibiotic resistance of sessile bacteria living within biofilms can be 1000 fold greater than that of free-floating planktonic bacteria [63]. The biofilm matrix forms both mechanical stability and the possibility that the individual organisms build synergistic interactions among themselves, to survive periods of starvation and remain extracellular enzymes get into the mucus layer [38], [66].

The third phase is characterized by detachment. This is seen when biofilms grow into large macroscopic three-dimensional structures. This is when shear forces may cause large sections of the biofilm to detach – releasing millions of organisms [57], [67].


Biofilm and the “re”-use of medical implants

Historically implant sizers (implants with smooth surfaces to find out the appropriate size of the definitive prosthesis) were routinely and repeatedly resterilized until the early 1990s. Also anecdotally it was reported that implants had been washed in antibacterial disinfectants or antibiotics and then were reinserted during revisional surgery when they macroscopically looked intact. However, when recommendations had been issued that no implant may be reinserted once it had been taken out, in Germany the regulation for medical products and interpretations of the appropriate laws has been discussed by various authors and institutions, among them by a special task force for questions of hygiene in medicine by the AWMF (Arbeitsgemeinschaft der Wissenschaftlichen Medizinischen Fachgesellschaften/working group of scientific medical associations) [66]. Since then it has been considered common knowledge and has become a standard that breast implants may not be used twice, being designed as one way products. Since at the time of implant exchange one cannot definitely know the result of bacterial swabs (which have to be processed for several days) it seems clear that the existence of a biofilm on a prosthesis cannot be ruled out visually, even when there were no typical clinical signs. Biofilms may not be visible by inspection. According to the current data it is not possible to reliably remove a biofilm on a breast implant in situ and under clinical conditions. Methods to eliminate biofilms on implant currently rely on harsh procedures that can be applied only outside the human body, such as plasma sterilization, ultrasonic treatment, oxidants, chlorine/ sodium hypochlorite, hydrolysis with microbubbling, bacteriophage therapy, x-ray or UV/ozone-irradiation, electroporation and application of electric fields in combination with biocides, laser radiation etc., to name the most frequently discussed options [68]. Necessarily, for these interventions implants will have to be removed from the body. This applies also for the use of other alloplastic or biological materials that are inserted or implanted into the human organism, such as “fillers” for instance [56], [69]. Ideas to protectively coat prostheses with antibactericidal surfaces have been investigated, but are not clinically available yet [70].

Because on the one hand the rapidly evolving knowledge about biofilms in this context is not yet generally recognized, and on the other hand, however, plastic surgeons may get into considerable and potentially avoidable legal conflicts when they deviate from current guidelines, we want to reflect on this topic against the background of current insights with regard to the biofilm problem on breast implants [2], [71].


Infectious complications after breast implants and biofilms

Infection after breast implant surgery occurs in 1.1% to 2.5% of procedures performed for augmentation and up to 35% of procedures performed for reconstruction after mastectomy. Most infections result from skin organisms and occur in the immediate postoperative period, although infections can occasionally present after many years [72]. Many product recalls and product contamination issues are caused by biofilm detachment. Generally there is a consensus that despite all safety measures local complications cannot be completely avoided after breast implant surgery. Devices such as sterile funnels to prevent skin contact during insertion of breast prostheses have been developed for this reason. Similar to infections of other medical devices the removal of the potentially contaminated implant is the cornerstone of treatment. Bacterial cells which detach from these biofilms can enter the circulatory system. This can lead to severe systemic side effects such as sepsis. For instance, in patients with catheter sepsis, sepsis has been described to occur in 6%, and endocarditis in 1% [73].

In general, in current reviews any device in place is considerd to bacterially contaminated during its life span in around 7% [74].

For any exposed or infected implant the main aim is to cure the infection in the first step before reinsertion of another implant can be considered. A time frame of 3–6 months is generally accepted to be sufficient before repeating the device implantation [75], [76], [77], [78]. Failed post cancer breast reconstructions frequently are converted into autologous reconstructive procedures [79], [80], [81], [82] to get rid of the alloplastic material.

Only within the last years the impact of bacterial biofilms on the pathogenesis and maintenance of chronic inflammation processes could be shown as the most frequent reason for implant failure, which is why the strict removal of potentially infected breast prosthesis is essential [83].

In contrast to the scientific aspects especially for Plastic Surgeons the legal aspects have to be taken into consideration when dealing with one way products and devices.

Due to economic needs in modern medicine the repeated use or “re-use” of single-use products has become an increasingly contentious issue. Obviously this is not primarily a pure medical problem. But if surgeons deviate from the standard regulations concerning medical devices lawful they take over the responsibility of delivering a certified product. This usually would be the task of the manufacturer who has to oblige certain laws and regulations in order to get permission to distribute medical devices for implantation into a human body which have been shown to cause no harm. There has been considerable debate if medical devices that are intended for single use may be recycled or not. In Germany the Robert Koch Institute and the Association of Scientific Medical Societies (AWMF) have issued a consensus statement that covers also the handling of silicone implants for breast surgery [66].

European Union member states have propagated certain steps to tighten regulatory controls over medical devices and technologies in the wave of revelations that French breast implant manufacturer Poly Implant Prothèse Company (PIP) used non-medical-grade silicone in its products. Coordinated efforts have been initiated at national levels to ensure full implementation and enforcement of existing medical device legislation to guarantee safety and improve patient confidence in the EU regulatory system. On a regulatory level verification of notified body designations needs to be evaluated whether these entities are truly designated only for assessment of medical devices and technologies, as well as making sure that Notified Bodies fully leverage their authority being laid out in conformity assessments, including their power to conduct unannounced inspections. In any respect it seems advisable for Plastic Surgeons to be informed about the legal implications of deviating from common standards and how to perform safely during revisional breast implant surgery. Infections after breast implants and the role of potential biofilms are a common cause for legal cases. As long as the microscopically thin biofilms containing bacteria or fungi are not visible by pure inspection an implant that may look otherwise intact the implant should be considered to be potentially afflicted with biofilm once it has been exposed. It should be clear that washing breast implants in bactericidal solutions or in antibiotics intra-operatively in order to get rid of biofilm is not sufficient to ensure product safety. Given the complex 3D surface structure of breast prosthesis (Figure 2 [Fig. 2], Figure 3 [Fig. 3]) it can easily be perceived that a full penetration of any antimicrobial agent into the deepest holes and spaces of the surface is almost impossible. Case reports in the literature about successful retainment of exposed silicone breast implants were based on clinical experience and did not discuss the removal of a biofilm or the problems of incomplete microbicidal action and penetration into the structure [20], [73], preventing complete removement of the biofilm [74].

Furthermore on it has been suggested that aggressive biocides may well alter the surface of a silicone implant and could lead to implant failure by destroying the original material properties of the membrane. Testing potential side effects of antimicrobial agents and various disinfectants on the material properties of breast implants is necessary and is currently envisioned by researchers to clarify these questions.

It seems currently common sense, although various experimental methods to prevent or combat biofilms have been published, that all of these measures are not applicable to the patient in the clinical situation yet. In particular, the high-frequency ultrasound treatment of implants or the plasma treatment of implants outside the body or the introduction of selected metals into a biofilm, such as silver, platinum or bismuth, coatings of urinary catheters with non-pathogenic Escherichia coli bacteria, electrical current, Chlorine or UV- and X-ray irradiation are unsuitable for intraoperative removal of biofilms [20], [71], [72], [73], [74], [75], [76], [77], [84]. Even if some major bacterial load of biofilms could be removed, disinfectants will probably not penetrate deep enough into the biofilm. Remaining bacteria can be quiescent for years. These are termed “persisters”.

According to our current understanding, the chemical composition of the biofilm can also offer unfavorable conditions that render bactericides effectless. Moreover, the different cells or groups of cells within a biofilm can behave very differently. For example bacterial biofilm can grow in the aerobic and/or anaerobic zone. Thus, different parts of the biofilm vary by the distance to nutrients or oxygen or antibiotics or reactions of the immune system. In addition, microbes within a biofilm show a reduced metabolism and rate of growth up to extended periods of quiescence [85], [86], [87], [88], [89]. Such bacteria frequently cannot be propagated in culture and hence are not detected in swabs [43]. They do ingest cytotoxins and protect themselve by their failure to respond to antibiotics or bactericides. This special phenomenon has been accused to cause the so called “late seroma” in breast prosthesis [40]. It is one reason why perioperative antibiotic prophylaxis is recommended when breast implants are inserted [90]. There is no clear evidence yet if the use of sterile plastic bags to protect contact between implants and skin definitely decreases this complication risk. One reason might be the contamination possibility by the contact to glandula/ducts [47], [91].


Conclusion

In conlusion our current knowledge about biofilms and breast implants implicate that a reliable elimination of biofilm on breast implants during operative revisions is not safely possible so far. Moreover, exposed prostheses need to be replaced by new ones to make sure that any risk of persisting biofilm is excluded. It seems obvious and is highly advisable to not reuse single-use products when an infection might have occurred. The safest resolution is first of all to remove the implant, then cure the infect and either come back to reinsert another prosthesis or change the procedure to an autologous reconstruction.


Notes

Competing interests

The authors declare that they have no competing interests.


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