\\n\\n
More than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\\n\\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\\n\\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\\n\\nAdditionally, each book published by IntechOpen contains original content and research findings.
\\n\\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\\n\\n\\n\\n
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
Simba Information has released its Open Access Book Publishing 2020 - 2024 report and has again identified IntechOpen as the world’s largest Open Access book publisher by title count.
\n\nSimba Information is a leading provider for market intelligence and forecasts in the media and publishing industry. The report, published every year, provides an overview and financial outlook for the global professional e-book publishing market.
\n\nIntechOpen, De Gruyter, and Frontiers are the largest OA book publishers by title count, with IntechOpen coming in at first place with 5,101 OA books published, a good 1,782 titles ahead of the nearest competitor.
\n\nSince the first Open Access Book Publishing report published in 2016, IntechOpen has held the top stop each year.
\n\n\n\nMore than half of the publishers listed alongside IntechOpen (18 out of 30) are Social Science and Humanities publishers. IntechOpen is an exception to this as a leader in not only Open Access content but Open Access content across all scientific disciplines, including Physical Sciences, Engineering and Technology, Health Sciences, Life Science, and Social Sciences and Humanities.
\n\nOur breakdown of titles published demonstrates this with 47% PET, 31% HS, 18% LS, and 4% SSH books published.
\n\n“Even though ItechOpen has shown the potential of sci-tech books using an OA approach,” other publishers “have shown little interest in OA books.”
\n\nAdditionally, each book published by IntechOpen contains original content and research findings.
\n\nWe are honored to be among such prestigious publishers and we hope to continue to spearhead that growth in our quest to promote Open Access as a true pioneer in OA book publishing.
\n\n\n\n
\n'}],latestNews:[{slug:"intechopen-maintains-position-as-the-world-s-largest-oa-book-publisher-20201218",title:"IntechOpen Maintains Position as the World’s Largest OA Book Publisher"},{slug:"all-intechopen-books-available-on-perlego-20201215",title:"All IntechOpen Books Available on Perlego"},{slug:"oiv-awards-recognizes-intechopen-s-editors-20201127",title:"OIV Awards Recognizes IntechOpen's Editors"},{slug:"intechopen-joins-crossref-s-initiative-for-open-abstracts-i4oa-to-boost-the-discovery-of-research-20201005",title:"IntechOpen joins Crossref's Initiative for Open Abstracts (I4OA) to Boost the Discovery of Research"},{slug:"intechopen-hits-milestone-5-000-open-access-books-published-20200908",title:"IntechOpen hits milestone: 5,000 Open Access books published!"},{slug:"intechopen-books-hosted-on-the-mathworks-book-program-20200819",title:"IntechOpen Books Hosted on the MathWorks Book Program"},{slug:"intechopen-s-chapter-awarded-the-guenther-von-pannewitz-preis-2020-20200715",title:"IntechOpen's Chapter Awarded the Günther-von-Pannewitz-Preis 2020"},{slug:"suf-and-intechopen-announce-collaboration-20200331",title:"SUF and IntechOpen Announce Collaboration"}]},book:{item:{type:"book",id:"637",leadTitle:null,fullTitle:"Tissue Engineering for Tissue and Organ Regeneration",title:"Tissue Engineering for Tissue and Organ Regeneration",subtitle:null,reviewType:"peer-reviewed",abstract:"Tissue Engineering may offer new treatment alternatives for organ replacement or repair deteriorated organs. Among the clinical applications of Tissue Engineering are the production of artificial skin for burn patients, tissue engineered trachea, cartilage for knee-replacement procedures, urinary bladder replacement, urethra substitutes and cellular therapies for the treatment of urinary incontinence. The Tissue Engineering approach has major advantages over traditional organ transplantation and circumvents the problem of organ shortage. Tissues reconstructed from readily available biopsy material induce only minimal or no immunogenicity when reimplanted in the patient. This book is aimed at anyone interested in the application of Tissue Engineering in different organ systems. It offers insights into a wide variety of strategies applying the principles of Tissue Engineering to tissue and organ regeneration.",isbn:null,printIsbn:"978-953-307-688-1",pdfIsbn:"978-953-51-6449-4",doi:"10.5772/1146",price:139,priceEur:155,priceUsd:179,slug:"tissue-engineering-for-tissue-and-organ-regeneration",numberOfPages:468,isOpenForSubmission:!1,isInWos:1,hash:"5bef0b1c31f0555294c7d49580c8d241",bookSignature:"Daniel Eberli",publishedDate:"August 17th 2011",coverURL:"https://cdn.intechopen.com/books/images_new/637.jpg",numberOfDownloads:49581,numberOfWosCitations:36,numberOfCrossrefCitations:22,numberOfDimensionsCitations:69,hasAltmetrics:0,numberOfTotalCitations:127,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"November 4th 2010",dateEndSecondStepPublish:"December 2nd 2010",dateEndThirdStepPublish:"April 8th 2011",dateEndFourthStepPublish:"May 8th 2011",dateEndFifthStepPublish:"July 7th 2011",currentStepOfPublishingProcess:5,indexedIn:"1,2,3,4,5,6",editedByType:"Edited by",kuFlag:!1,editors:[{id:"6495",title:"Dr.",name:"Daniel",middleName:null,surname:"Eberli",slug:"daniel-eberli",fullName:"Daniel Eberli",profilePictureURL:"https://mts.intechopen.com/storage/users/6495/images/1947_n.jpg",biography:"Daniel Eberli MD. 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Together with his research team, he is working on novel biomaterials for bladder reconstruction, improving autonomic innervation, cellular treatment of incontinence and tracking of stem cells.",institutionString:null,position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"3",totalChapterViews:"0",totalEditedBooks:"4",institution:{name:"University Hospital of Zurich",institutionURL:null,country:{name:"Switzerland"}}}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"980",title:"Tissue Engineering and Regenerative Medicine",slug:"tissue-engineering-and-regenerative-medicine"}],chapters:[{id:"18187",title:"Myocardial Tissue Engineering",doi:"10.5772/22870",slug:"myocardial-tissue-engineering",totalDownloads:2396,totalCrossrefCites:2,totalDimensionsCites:5,signatures:"Tatsuya Shimizu",downloadPdfUrl:"/chapter/pdf-download/18187",previewPdfUrl:"/chapter/pdf-preview/18187",authors:[{id:"49606",title:"Prof.",name:"Tatsuya",surname:"Shimizu",slug:"tatsuya-shimizu",fullName:"Tatsuya Shimizu"}],corrections:null},{id:"18188",title:"Cardiac Muscle Engineering: Strategies to Deliver Stem Cells to the Damaged Site",doi:"10.5772/20178",slug:"cardiac-muscle-engineering-strategies-to-deliver-stem-cells-to-the-damaged-site",totalDownloads:2050,totalCrossrefCites:0,totalDimensionsCites:2,signatures:"Giancarlo Forte, Stefania Pagliari, Francesca Pagliari, Paolo Di Nardo and Takao Aoyagi",downloadPdfUrl:"/chapter/pdf-download/18188",previewPdfUrl:"/chapter/pdf-preview/18188",authors:[{id:"37701",title:"Dr.",name:"Giancarlo",surname:"Forte",slug:"giancarlo-forte",fullName:"Giancarlo Forte"},{id:"62146",title:"Dr.",name:"Stefania",surname:"Pagliari",slug:"stefania-pagliari",fullName:"Stefania Pagliari"},{id:"62147",title:"Dr.",name:"Francesca",surname:"Pagliari",slug:"francesca-pagliari",fullName:"Francesca Pagliari"},{id:"62777",title:"Prof.",name:"Paolo",surname:"Di Nardo",slug:"paolo-di-nardo",fullName:"Paolo Di Nardo"},{id:"62778",title:"Prof.",name:"Takao",surname:"Aoyagi",slug:"takao-aoyagi",fullName:"Takao Aoyagi"}],corrections:null},{id:"18189",title:"Cardiovascular Tissue Engineering Based on Fibrin-Gel-Scaffolds",doi:"10.5772/19761",slug:"cardiovascular-tissue-engineering-based-on-fibrin-gel-scaffolds",totalDownloads:4160,totalCrossrefCites:8,totalDimensionsCites:18,signatures:"Stefan Jockenhoevel and Thomas C. 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Discoveries in microbiology and the setup of aseptically processes in medical science allowed the possibility of high‐level surgery over the last century, with the hope of a safe healing. In return, major problems have appeared as nosocomial infections due to bacterial biofilm formations on medical devices [1, 2]. Despite the multiplication of surgical procedures in order to get as close as sterile environment, bacterial contamination remains an important risk. Bacteria could indeed acquire antibiotic resistances and an emergence of multidrug resistant strains is observed [3, 4]. Moreover, the most alarming is that bacteria with regular sensitivity to antibiotics are even able to develop a strategy to survive: the formation of a strong community named biofilm [1, 2, 5]. Biofilm‐associated infections represent 80% of nosocomial infections, and Staphylococcus aureus is the leading species in this domain [6–8].
\nBiofilm is defined as a multicellular lifestyle, an organized structure built by almost all bacterial species. Even if the term “biofilm” has been used for more than 60 years, the understanding of this structure started but recently. Fossilized biofilms of 3.5 billion years have been discovered and highlight the hypothesis that biofilm is a survival strategy always used by microorganisms since the dawn of time [5]. Scientists have recently understood that bacteria are not always living as free cells in nature; on the contrary, most of the time, bacteria build a real social life in a resistant community surrounded by a matrix composed of polysaccharides, extracellular DNA, proteins, lipids and other components [1, 2]. Biofilm is present on biotic or abiotic surface and bacteria embedded inside are 10–1000 times more resistant to conventional antibiotics than free‐floating bacteria according to the strains, the molecule applied and the model of study [7–9]. Life cycle of biofilm is nowadays well‐described. First, bacteria adhere on a surface and they enhance different mechanisms to irreversibly be attached. Then, the program of biofilm starts with a maturation of the multicellular structure. To complete this cycle, dispersion of swimming cells occurs under specific conditions [1, 2, 7–9]. However, the key of biofilm mechanism is the initiation that leads bacteria to form a biofilm and only under specific conditions. This trigger of biofilm mechanism is still an important question. Survival would be the answer, thus biofilm structure allows bacteria to resist to any types of environmental stress including UV, lack of nutrients and presence of antimicrobials [1, 2, 7–9].
\nAll these characteristics lead to major problems in industries as well as in the medical domain. In industry, for example, the presence of multispecies biofilms has a high impact on the processes or on the production and results in high costs. S. aureus can be isolated from biofilm found in food industry particularly in dairy process [10], and they are sanitizers resistant [11]. As a consequence, microorganisms can infect the milk or other food products and cleaning the production system is very complicated or impossible. Thus, all the structures need to be replaced representing an important waste of money.
\nIn the medical domain, numerous difficulties to treat biofilm‐associated infections are described: resistance to antibiotics and to immune system, spread of infection, sepsis shock and surgical risks to remove infected implant or tissues [1, 6, 8]. S. aureus is one of the most frequent germs found in biofilm‐associated infections partially resulting from the fact that they are commensal bacteria on the human skin and mucous [12]. Moreover, S. aureus multidrug resistant like methicillin resistant S. aureus strains (MRSA), is responsible for biofilm infections that are more difficult to treat that need more intensive care and replacement of medical devices as compared to Staphylococcus epidermidis biofilm infections, for example. S. aureus also embodies an important reservoir of dissemination to other human body sites [12]. Consequently, the development of new therapeutic strategies, through a better understanding of biofilms, is necessary and imperative [4] to fight against this structure resistant to the immune system and antimicrobial drugs.
\nHere after, to better understand the strength of S. aureus biofilms, different aspects relevant to biofilm, its mechanism and its physiology will highlight the aspects that are specific to Staphylococci and S. aureus more precisely. The consequence of S. aureus in clinical domain will be described and some “anti‐biofilm” strategies will be suggested.
Different steps of biofilm life cycle have been well‐described through the study of different bacterial species: reversible adhesion, irreversible attachment, maturation and dispersion [5, 13] (Figure 1). First, active bacteria can turn from “swimmers” to “stickers” on a support. A surface is supposed to always be in favor of adhesion because of the prediction that organic substances will concentrate on a surface and microorganisms will easily adhere and be protected from outsider challenges. Adhesion will dependent on the species of bacteria, surface composition, environmental factors, and essential gene products [14]. Microorganisms could adhere on inert or biotic surfaces. Most of the time, interaction between bacteria and abiotic surface involves nonspecific interactions as opposed to active interaction between microorganisms and live tissues [14]. The surface conditioning is quite important through various physiochemical parameters: hydrophobicity, chemical composition of the material, surface energy, eletrostatic charges, temperature, surface roughness and in the case of biotic adhesion: serum and tissue protein adsorption [14, 15]. Hydrophobicity increases bacterial adhesion in most cases [15, 16]. In some environmental conditions, macromolecules adsorption could form a “film” neutralizing excessive charges and surface free‐energy facilitating bacteria and surface proximity. It was shown that pH parameters influence S. aureus adherence on glass [17].
Biofilm life cycle.
As far as S.epidermidis is concerned, Sousa et al. [15] have shown that surface conditions influence bacterial adhesion but the cell surface hydrophobicity itself was not linked to adhesion capacity, underlying the importance of other factors as cell wall associated proteins. The first bacteria approaching a surface adhere to it because of good conditioning but afterwards when the rate of cells increases, the following bacteria tend to adhere to previous bacteria instead of the surface [15]. In a case of a bad conditioning of surface and the necessity of adhesion, pili or other bacterial appendices could overcome potential repulsion.
\nIn any case, the life of a biofilm starts by an adhesion. The latter is reversible but can turn irreversible. Indeed, under specific conditions, events of irreversible attachment tend to increase and lead to the formation of a biofilm. In fact, irreversible attachment is the first step to the maturation of a future biofilm.
\nAt the beginning, adhesion is the fortunate meeting between a good conditioned surface and a bacterium. In any environment, microorganisms can randomly get close to the surface or be attracted by chemotaxis involving their motility system [14]. Very recently, the ability for motility was observed for S. aureus even if they do not possess any appendages for movement [18]. This very particular movement is supposed to be a response to very specific conditions.
\nA surface could be attractive or repulsive for bacteria according to different parameters described above including hydrophobic and electrostatic interactions, hydrodynamic forces and temperature. Hydrophobicity is considered the most important. Bacteria could adhere on a biotic or abiotic surface thanks to the involvement of specific bacterial surface molecules such as the surface protein autolysin or the teichoic acids, altering the physicochemical properties of the bacterial surface rather than mediating the attachment via specific, receptor‐mediated interactions [13].
\nIn the human body, S. aureus is known to have specific targets in relation with its pathogenesis. Staphylococci attachment to a biotic surface such as human tissue is due to specific interactions with its virulent factors (Figure 1). These bacteria possess a large variety of surface‐anchored proteins such as the microbial surface components recognizing adhesive matrix molecules (MSCRAMMS). MSCRAMMS are structured in three parts: a binding domain, a cell wall spanning domain and a third part responsible for the covalent or non‐covalent attachment of the MSCRAMM proteins on bacterial surface. These adhesins are able to bind to one or several different human matrix proteins (fibronectin, fibrogen, etc.) [13, 19, 20] and are required for biofilm‐associated infections on indwelling medical devices covered by host matrix right after insertion [13]. Covalent bonds are catalyzed by sortases recognizing LPXTG motifs. S. aureus strains have a high variety of LPXTG‐type MSCRAMMs compared to S. epidermidis [21]. Other surface proteins involved in adhesion are Sdr proteins (Serin‐aspartate repeat family) or Aap (accumulation‐associated proteins) [13]. Non‐covalently bounds are insured by other proteins such as the autolysin Atl. Autolysins, involved in cell wall turnover, are one of the most abundant proteins on the staphylococcal cell surface and possess binding sites for human matrix proteins [22, 23].
\nStaphylococci are known for their high ability to stick to plastic surfaces. Teichoic acids, which are not involved in S. aureus attachment on biotic surface, are important compounds present in the cell wall and are important for adhesion on plastic surfaces thanks to their interaction with other surface polymers [13, 24]. However, in vitro assay over‐estimated the interactions between teichoic acids and devices mainly because devices in fluids or in tissue are rapidly covered by host matrix proteins preventing the direct interaction of teichoic acids to plastic. Despite teichoic acids, two other adhesins have a role for adherence on plastic: the cell wall bound surface protein Bap involved in adherence to polystyrene surfaces [25] and SasC a S. aureus surface protein involved in attachment on polystyrene that does not mediate binding to fibrinogen, thrombospondin‐1, von Willebrand factor or platelets [26]. Also, autolysins facilitate attachment to plastic in addition of their capacity to bind to human matrix and their enzymatic function [23].
Pseudomonas aeruginosa biofilm is one of the most studied biofilm models. A powerful system of communication between cells was described in P. aeruginosa biofilm and named “quorum‐sensing” [27]. First the quorum‐sensing system was linked to a communication based on cell density. Then, quorum‐sensing is virtually connected to biofilm formation and dispersal phenomena. The communication system in P. aeruginosa is based on molecules called acyl‐homoserine lactones (AHLs) which penetrate bacteria and directly regulate target genes. Quorum‐sensing systems have been described in Gram‐negative and Gram‐positive bacteria. Each quorum‐sensing system is composed with different molecules and can activate or inhibit biofilm formation. The most studied system in S. aureus is the Agr quorum‐sensing system but other systems of communication exist.
\nFor S. aureus, only one specific quorum‐sensing system was so far described, but most probably, there are other mechanisms for communication. At some point, some genes involved in S. aureus virulence were named accessory genes, and an accessory gene regulator (agr) was identified as a global regulator of virulence factors genes. Different experimental designs have shown that the Agr system induced by an extracellular ligand, the autoinducing peptides (AIP), is a sensor of population and so considered as a quorum‐sensing system. This system can be activated by addition of AIP or by glucose depletion [28]. Briefly, this system is composed of two promoters P2 and P3. P3 transcript encodes RNAIII, the intracellular effector of target gene regulation, answering to agr system activation. P2 operon encodes for a two‐component system and its autoinducing ligand AIP [29].
\nDuring biofilm formation, Agr quorum‐sensing system is repressed to stop the expression of S. aureus colonization factors [29], and it gets activated during the dispersion of the bacteria [30]. Artificial activation of Agr has also been shown to induce biofilm dispersion [28]. Moreover, Agr quorum‐sensing system is necessary for the communication inside mature biofilm to establish the 3D structure through the control of cell dispersion. This probably requires phenol‐soluble modulins (PSMs) which are described in the next section and proteases activated by Agr and involved in the degradation of exopolysaccharides (EPS) matrix [31]. However, Agr does not control important biofilm adhesive molecules such as the polysaccharide intercellular adhesions, currently named PIA [32]. In conclusion, Agr system regulation is based on cell density. During the early stage of colonization, cell density is low and as consequences Agr quorum‐sensing activity gets weak and the cell wall protein or surface adhesins are not downregulated but highly expressed. In the later stage, Agr activity increases with cell density and thereafter Agr upregulates secreted virulence factors such as lipases, proteases and hemolysin [33]. Not surprisingly, Agr involvement in biofilm formation seems to be under specific environmental conditions as shown by the contradiction of experimental results relevant to the model used in the study [30]. One problem underlined each time is the difficulty to detect agr expression due to the very slow bacteria metabolism in the biofilm. During hospitalization, S. aureus strains isolated from patients are more frequently Agr‐defective strains showing their better ability to turn into a nosocomial infection agent [34]. Some agr‐defective mutants have been isolated from catheter infections, where they had the capacity to form a compact biofilm with the loss of their capacity to detach and disseminate.
\nOther regulators have been identified such as Rbf which is involved in S. aureus biofilm formation at the maturation stage rather than at the initial attachment [35]. This regulator did not affect ica gene locus coding for adhesins; however, a clinical isolate with rbf mutation showed a lower capacity to form biofilm. LuxS, another regulator first described in Vibrio cholerae, is under the control of the auto‐inducer AI‐2 and seems to play a role in biofilm formation through the icaR expression. However, LuxS is also involved in the S‐adenosyl methionine cycle, and its role in biofilm is consequently debated as it could be the result of this metabolic role [36].
\nIn conclusion, production of surfactant molecules dependent of quorum‐sensing system appears to be a general mechanism for the biofilm structuring as well as for the detachment of many bacteria. In the specific S. aureus quorum‐sensing, biofilm is based on the detection of signaling molecules by specific sensors which lead to a chain reaction with different molecular actors and not on a direct communication where the signal molecules enter in the cells and directly regulate different genes. In S. aureus, the sensors are numerous and allow a fast answer of the bacteria.
The maturation of biofilm is based on the development of the multicellular structure (Figure 1). Biofilm growth is controlled by the increase of bacterial mediators, the slowdown of metabolism and cell cooperation. Maturation starts when bacterial cells induce the biofilm program and create an intercellular aggregation through the production of a “slime” commonly named matrix. The latter sticks bacteria one to each other as well as on surface. The matrix is composed of exopolysaccharides (EPS), proteins and extracellular DNA (eDNA) and is responsible for biofilm maturation that is the result of an organized community construction. This specific 3‐dimensional structure appears as a typical mushroom‐like shape containing water or fluid channels formed thanks to a disruptive process [37]. Paradoxically, maturation in the construction of the community needs also disruption events. Fluid‐filled channels are vital in delivering nutrient into biofilm deeper layers [38]. This kind of structure is species‐specific.
\nExopolysaccharides are the first molecules discovered in biofilm matrix. In staphylococci, the most described adhesive biofilm molecule is the polysaccharide intercellular adhesion (PIA) or poly‐N‐acetylglucosamine (PNAG) and represents the major part of the staphylococci biofilm‐forming extracellular matrix [39]. PIA has an important role in the biofilm structure and the biofilm‐associated infections [40, 41]. Introducing a positive charge in the environment of the bacterial cell surface which is negatively charged, PIA works like a glue sticking the cells together by electrostatic interaction [42]. PIA is encoded by ica gene locus and regulated by numerous environmental factors [43]. For example, SarA and SigB upregulate PIA expression and on the contrary LuxS downregulates it [44–46]. PIA is the only factor identified so far as important for staphylococci biofilm formation in vivo [13, 43]; however, PIA is not present in all strains isolated from biofilm‐associated infections [47]. Therefore, some other compounds like proteins must also play a role.
\nNumerous specific proteins could be substitute for PIA in biofilm formation as proteins are now recognized as essential for biofilm structure, such as the following proteins: Aap (accumulation associated protein), extracellular matrix binding protein (Embp), protein A, fibrinogen‐binding proteins (FnbpA and FnbpB) or S. aureus surface protein G (SasG) [48]. This latter mediates intercellular aggregation thanks to hydrophilic interaction with the proteins present on other bacteria [49]. As for S. aureus surface protein SasC, which possesses a LPXTG‐motif to anchor to cell wall, it is involved in intercellular aggregation and biofilm maturation [26]. Depending on the Staphylococcus, the extracellular Aap protein [50] is involved in PIA‐independent biofilm formation in S. epidermidis [51] or in the maturation of the biofilm by interactions with PIA like in S. aureus [50].
\nAll these results underline the importance of the surfactants in biofilm maturation. Phenol‐soluble modulins (PSM) are surfactant peptides found in both S. aureus and S. epidermidis. Their sequence is species dependant, but they all have an amphipathic α‐helix [13]. PSMs are strictly controlled by Agr, with a direct binding of Agr regulator on the psm operon promoter, suggesting that Agr‐dependent biofilm maturation processes are due to PSMs expression [13]. Moreover, an agr mutant strain of S. aureus has the same behavior that a completely deleted PSM genes mutant in in vivo model [13]. As shown in S. epidermidis, the PSM involvement in biofilm maturation is independent of the PIA protein. In S. epidermidis, the lack of PSMs leads to biofilms that are more “compact”, suggesting that PSM are also involved In biofilm development. Furthermore, as seen in all the Staphylococcus, the presence of the PSM peptides is needed for biofilm volume, thickness, roughness and channel formation [52]. Surfactant peptides are therefore the key of the 3‐dimensional biofilm structure. PSMs also induce biofilm detachment [52] and are biofilm maturation in vivo determinant factors [13].
\nAmyloid proteins have also been revealed as important for biofilm structure, bringing stability to the matrix [53]. These protein fibers could bind the extracellular DNA. PSMs play also a role as inert fibrils in biofilm, acting as a solid bond, waiting for better conditions to induce their dissociation and promote biofilm dispersion [53, 54]. Bap another cell wall bound surface protein [25, 55–57], involved in adhesion, is also required for biofilm maturation and infection of bovine mammary glands [20, 45]. This protein is a real sensor, responding to environmental conditions (like calcium concentration), and Bap is also a scaffold protein forming amyloid‐like aggregates at low calcium concentration and under acidic pH [53].
\nUnder an organized construction, biofilm maturation is based on development and disruption events. Thus, PIA‐degrading enzymes (PIAse) are supposed to contribute to biofilm maturating but they have never been found in staphylococci [13]. Anyway other proteases could have an important role in staphylococci biofilm maturation as proven by strains showing PIA‐independent biofilm formation [58]. Those proteases are regulated mostly by SarA and more rarely by Agr, but so far no experiments have demonstrated direct evidence for their role on biofilm development or protease‐mediated biofilm detachment.
\nThe third important element of matrix composition is extracellular DNA (eDNA). DNA, a polyanionic molecule present in biofilm matrix, is described as a ligand able to link to other molecules present in the matrix such as teichoic acids or PIA. Therefore, DNA has a role in biofilm structure. This presence is based on the involvement of cell death: DNA released from lysed bacteria also called eDNA has a critical involvement during initial attachment and maturation. An increase of cell lysis influences biofilm formation through the Cid proteins [59–61]. Indeed, regulators like CidR which controls autolysis are involved in biofilm development and the formation of the tower mushrooms shapes [62]. Extracellular DNA appears through the bacterial programmed cell death and through the expression of cidA gene encoding for a holin responsible for lysis. This system is regulated by the production of an antiholin encoded by lrgAB genes which is an inhibitor of cidA‐mediated lysis [59, 62]. However, in vivo, the importance of eDNA is difficult to assess as well as to understand how a staphylococcal biofilm could survive in the presence of human DNAseI which succeed to disperse a mature biofilm in vitro [13].
\nIn conclusion, scientists have realized how important it is to have precise knowledge of the mechanisms involved in the biofilm extend matrix or in the detachment steps to be able to develop anti‐biofilm strategies. However, biofilms are also formed by four set of cells: some with an aerobic or fermentative growth, some dormant or dead [63]. This cell heterogeneity within the biofilms has to be kept in mind in the search of anti‐biofilm therapy.
Disruptive processes are vital for biofilm structure and disruption allows the detachment of single cells or large bacteria cluster from biofilm in case of good environmental conditions or in case of expansion of the biofilm (Figure 1). This dispersion has important consequences in biofilm‐associated infections as it leads to systemic dissemination. It is well known now that detached cells from biofilm could lead to endocarditis or sepsis [13].
\nDisruption is based on mechanical forces as well as the interruption of the production of the biofilm material and production of enzymes and surfactants that are considered as detachment factors able to destroy the matrix. Agr quorum‐sensing system involved in biofilm formation and extracellular protease activity are required to control biofilm dispersal molecules [28, 32, 52]. Expression of agr mostly carried out by the bacteria in the outer layers of the biofilm leads to detachment and regrowth [30], but agr is also expressed in deeper layers where it is required for channel formations [52]. In fact this dispersal effect linked to Agr system could be due to the involvement of PSMs whose expression is controlled by the Agr quorum‐sensing.
\nNucleases, the enzymes degrading extracellular DNA are also necessary. The human DNaseI degrades staphylococcal biofilms [64]. Staphylococcal thermonuclease nuc2 is involved in the biofilm development probably to promote dispersion [65]. A second nuclease nuc1 showed the similar dispersal effect as nuc2 on biofilm in vitro [66]. Nevertheless, those effects are not detected so far in in vivo models [66].
\nOther factors, involved in dispersion, have been described such as bacteriophages which have been revealed as important for biofilm development, especially in dispersal stage [31]. Even proteases like Aur metalloprotease and Slp serine protease have been shown to be responsible of dispersal movement [67].
\nIn conclusion, biofilm life cycle starts under the impulse of a stress response (e.g., starvation) and bacteria attach on a surface where cell proliferation is more favorable. A monolayer is formed, and some specific genes are expressed inducing the production of microcolonies. Quorum‐sensing system acts as a supervisor, and biofilm is formed in a well‐organized structure.
Biofilms seem to be the best strategy for bacteria to survive to any kind of environmental stress. The detection of stress and thus the response needs to be fast enough to survive under those conditions. Therefore, the rapid process of activation of the biofilm program is crucial for the bacteria.
\nAs described for stress response, the setup of inducible processes is based on the differential expression of an important number of genes [68, 69]. Biofilm bacteria cells are physiologically different from free cells [12]. Indeed, the different steps as adhesion and immobilization need the expression of various genes. More important, the communication between bacteria (quorum‐sensing system) controls many metabolic systems and leads to regulation of many genes. The production of the quorum‐sensing molecules as an endogenous signal leads to changes according to the detected concentration. Environmental clues trigger genetic and physiological changes also called biofilm transition. As previously described, the matrix is the plinth of biofilm development and is responsible for many processes in the biofilm program. Moreover, biofilm cells show a general downregulation of their metabolism underlining the slow growing cell or the lack of oxygen due to the biofilm structure, like during fermentation. An upregulation of the urease and the arginine deiminase pathway to limit the side effects of the acidic pH during anaerobic growth was also observed in biofilm structure [12]. All those adaptations participate to a general biofilm setup process. The differential gene expressions also lead to antibiotic resistance mechanism. In S. epidermidis, some of these antibiotic resistance mechanisms are upregulated during biofilm stage [70]. In S. aureus, Agr expression and involvement in biofilm formation depend of the environmental conditions [30]. The agr expression shut down has no effect, enhances or inhibits biofilm formation according to the environmental parameters [30].
\nBiofilm program is a temporary response to stress conditions and this process is able to turn off quite quickly when conditions are more favorable for the bacteria.
Bacteria have the extraordinary ability to survive in any harsh conditions, and as recently discovered, this is due to their capacity to form biofilm. Many environments can be a source of stress for bacteria. S. aureus biofilm have been found in industry and in clinical domain, particularly in biofilm‐associated infections. Environmental stresses are supposed to induce biofilm formation. As evidence, sigma B, a protein required for transcription and activated under stress responses due to heat shock, MnCl2, NaCl2 and alkaline shock, is involved in biofilm formation [71, 72].
\nIn S. aureus, nutrients like glucose or NaCl can influence biofilm. For example, Rbf regulator is involved in biofilm formation under high concentrations of glucose and NaCl conditions, but not in the presence of ethanol [35]. Nutrient‐starvation has been underlined as an important environmental stress which could induce biofilm maturation [61, 73]. In vitro, however, the addition of glucose is required for biofilm formation and activation of the agr quorum‐sensing system [28], even if oldest results showed the contrary [74]. In fact, conditions to form biofilm seem to be very specific, such as a balance between an over‐concentration of glucose and a lack of carbon source. The pH maintenance also influences Agr system and, in consequence, probably acts on biofilm formation [74, 75].
\nNitrite stress also induces PIA expression, responsible for the major part of the matrix composition [76]. In fact, induction or repression of biofilm formation is due to a balance of concentration of specific nutrients or stress. For example, NO is necessary for biofilm formation until its concentration starts to be too high. Thereafter, NO is involved in the dispersion of the biofilm [77]. It has also been observed that low oxygen, even anaerobic state, like in the heart of the biofilm, increases PIA expression [78].
\nIn human body, the lack of nutrients (e.g., iron, carbon source, etc.) or oxygen, the presence of the immune system or even the antimicrobial molecules are felt by the bacteria as stresses and could induce biofilm program. In S. aureus, PIA expression and biofilm maturation are strongly inducible by conditions found in vivo as described in a device‐related infection model [79]. In S. epidermidis, subinhibitory concentrations of tetracycline and quinupristin ‐ dalfopristin induce ica gene cluster expression and the increase of Mg2+ concentrations increase biofilm production. On the contrary, the addition of EDTA (Ethylenediaminetetraacetic acid) decreases the number of cells on a plastic surface [14]. Zinc concentration might also influence biofilm adhesion through the activity of SasG a surface protein with zinc‐dependent mechanical properties [49]. Subinhibitory concentrations of furanone, molecules isolated from red algae, inhibit quorum sensing but also favor biofilm formation [80, 81]. This result reflects the possible inter‐species interaction domain and the importance of the specific microenvironment.
\nIn nature, many bacteria live under nutrient‐limited conditions, lack of oxygen and under many other dangers like humidity, osmotic pressure and mechanical forces. Biofilm through the presence of the matrix protect all the embedded bacteria from all those environmental variations and pressures.
During bacterial infection, host immune cells are the defenders of the organism. Through mechanisms such as phagocytosis or release of bactericidal components, these cells are able to fight and neutralize planktonic S. aureus. Concerning S. aureus biofilm, the general thought is that biofilm structure protects the bacteria against the immune cells, avoiding interaction between both actors. Nevertheless, recent studies reported that polymorphonuclear neutrophils (PMN), macrophages, myeloid‐derived suppressor cells (MDSCs) and T lymphocytes can interact with S. aureus biofilm in a double‐edged interplay (Figure 2).
Interplay between S. aureus biofilm and host immune cells.
PMNs are the first line of defense in bacterial infections. These cells can phagocyte planktonic bacteria and release bactericidal components such as reactive oxygen species or enzymes [82]. Contrary to the dogma, in vitro experiments revealed that PMN can also attack S. aureus in biofilm form. PMNs can migrate towards and into the S. aureus biofilm and clear it by phagocytosis. The extent of biofilm clearance is apparently depended on its maturation state. Indeed, mature biofilms were reported as more resistant to phagocytosis as young ones [83]. Following phagocytosis, PMNs underwent apoptosis, a programmed cell‐death in order to prevent spilling of the bactericidal and cytotoxic entities [84]. In addition to phagocytosis, PMNs can release lactoferrin and elastase through degranulation phenomenon, as well as DNA [85]. Oxygen radical production by the PMNs also participates to biofilm clearance and is depended on the coating of biofilms with IgG, a mechanism termed “opsonization” [86]. In a global manner, PMNs can be considered as an asset to fight against S. aureus biofilms.
\nIn parallel to PMNs response, a macrophage response is also triggered during S. aureus infections, which is altered in case of S. aureus biofilm infection. Indeed, planktonic S. aureus normally induces a proinflammatory microbicidal phenotype in macrophages defined as M1. It implies the phagocytosis of bacteria and the production of bactericidal components [87]. In the context of S. aureus biofilm infection, in vitro and in vivo studies reported that invasion of macrophages into biofilms is limited. S. aureus biofilms is able to secrete specific toxins called alpha‐toxin (Hla) and leukocidin AB (LukAB) that inhibit macrophage phagocytosis and induce cytotoxicity, promoting macrophage dysfunction and thus facilitating S. aureus biofilm development [88]. Moreover, S. aureus biofilm can also induce the polarization of macrophages from a proinflammatory microbicidal M1 phenotype to an alternatively activated M2 phenotype, displaying anti‐inflammatory properties and limited phagocytosis [33, 89]. A recent study showed that the treatment of established biofilm infections with M1‐activated significantly reduced biofilm burdens, supporting that M1 phenotype is unpropitious to S. aureus biofilm development whereas M2 polarization favors it [90].
\nThe most recent studies concerning interactions between S. aureus biofilms and immune cells focus on the MDSCs, a heterogeneous population of immature monocytes and granulocytes with immunosuppressive properties. In case of S. aureus biofilm infection, MDSCs prevent monocyte/macrophage pro‐inflammatory activity, inhibit T lymphocytes proliferation and facilitates biofilm persistence [91]. This phenomenon is in part orchestrated by the interleukins IL‐12 and IL‐10 [92, 93]. IL‐12 is a cytokine with both pro‐ and anti‐inflammatory properties that promotes the recruitment of MDSCs whereas IL‐10 is an anti‐inflammatory cytokine, mainly produced by MDSCs in context of biofilm infection. A recent study reported that IL‐10 promotes biofilm growth and anti‐inflammatory gene expression in monocytes, which can be assimilated to a polarization to M2 phenotype [93]. MDSCs would in the end be the effectors for the development of the anti‐inflammatory environment that favors S. aureus biofilm persistence.
\nConcerning interactions between S. aureus biofilm and T lymphocytes, Leid et al. reported that mononuclear leukocytes, especially lymphocytes and in a lesser extend monocytes, can attach to the biofilm but they are not able to phagocyte maturing and fully matured S. aureus biofilm [94]. In case of S. aureus biofilm infection, early Th1 and Th17 inflammatory responses are increased and Th2 as well as Treg responses seem downregulated [95]. Th2/Treg responses appear as a protection mechanism for the organism as opposed to Th1/Th17 responses, which may favor the development of chronic S. aureus biofilm infection [96]. This response, in opposition to what is observed in the macrophage response, reveals the complexity of the interactions between S. aureus biofilms and the cells of the immune system.
Different bacteria are involved in infections associated with biofilm development in immunocompromised patients or medical devices. Sadly, the most famous example is P. aeruginosa species which develop highly resistant biofilm in pulmonary tract of cystic fibrosis patients.
\nBiofilm formation is linked to various staphylococcal diseases such as endocarditis, osteomyelitis, skin and soft tissues infections, urinary tract infection, nasal colonization and cystic fibrosis complications as well as implant‐associated infections [97–99]. In most of the case, the production of biofilm favors the chronicity of S. aureus infections. The colonization of implanted materials by staphylococcal biofilm is one of the highest important issues. Staphylococcal biofilm can develop on various structures such as catheters, prosthetic joints, prosthetic heart valves, contact lenses, cerebrospinal fluid shunts and cardiac pacemakers [100]. Furthermore, after their implantation in the body, medical devices become coated with host proteins, facilitating the attachment of S. aureus and the biofilm formation [101].
Biofilms have shown unbreakable structures resistant to antibiotics and many other molecules or environmental stresses. Many hypotheses have been tested to explain this incredible natural invincibility. First, the intrinsic structure of biofilm supposes that antimicrobials could not penetrate inside the biofilm. This hypothesis has been revealed unlikely for most of the antibiotics as the biofilm structure is composed with many water channels. A second hypothesis is based on the fact that the biofilm matrix can accumulate antibiotic‐degrading enzymes, and in consequence, antibiotics are quickly destroyed [9]. Then, scientists underline the fact that microorganisms have a very slow metabolism in the biofilm preventing most of the kinetic responses involved in the antibiotic mechanism. The use of antibiotics targeting more specifically those slow growth bacteria was not more successful, even combined with antimicrobial drugs that could target active bacteria present in the biofilm population, known to be heterogenic [63]. Persister cells can also be present in this heterogeneous population and can withstand high concentration of antimicrobial drugs.
\nNowadays, it seems that the natural resistance of biofilms comes from the induction of specific biofilm mechanisms [9]. Stress responses, as biofilm formation, lead to the changes of many gene expressions which increase the antimicrobial resistance. Nutrient starvations are now known to favor antibiotic tolerance [61].
\nBiofilm is the perfect example of an adaptive resistance, not due to a genetic mutation that could be transferred to daughter cells, even if the bacteria proximity in the biofilms increase horizontal transfer gene or mutation that could lead to intrinsic resistance [9].
Treatment of S. aureus biofilm is a therapeutic challenge. Even if everybody has in mind that the embedment of S. aureus in slime gives him an increased tolerance to antibiotics, two situations have to be defined concerning the treatment of S. aureus biofilm‐associated infections.
\nFirstly, antibiotics can have an inhibitive effect on the formation of biofilm. It is related to the capacity to inhibit the attachment and the initial growth of the biofilm. A recent study specifically evaluated the inhibition of S. aureus biofilm formation through the use of a new system the antibiofilmogram® [102]. Based on Biofilm Ring Test® method [103], this system permits to define, for a chosen antibiotic, the minimal inhibiting concentrations (MIC) needed to inhibit biofilm formation (called bMIC). In this study, Tasse et al. reported that the bMIC is equivalent or close to the MIC for planktonic bacteria. Similar values between MIC and bMIC were notably observed for clindamycin, fusidic acid, linezolid and rifampin [102].
\nThe second situation concerns the efficiency of antibiotics on formed/mature biofilm. The sessile community is already organized and persisters can be present. In this case, antibiotic efficiency is defined through the measure of the minimal biofilm eliminating concentration (MBEC) via the use of the Calgary Biofilm Device [104]. MBEC for S. aureus biofilms can be 10–1000 times higher than the MIC defined for planktonic bacteria, depending on the investigated strains and antibiotics [105–108].
\nThe difference between bMIC and MBEC is probably due to a lack of penetration/diffusion of antibiotics inside the biofilm, even if this statement still stays controverted. Indeed, a decreased penetration of antibiotics has been observed in in vitro models of S. aureus biofilm [109, 110]. The penetration inside biofilm varies depending on the type of antibiotics and the structure of the biofilm. On the contrary, other studies, such as the recent one by Boudjemaa et al. reported that the biofilm matrix was not a shield to the antibiotic diffusion. They observed that the concentration inside the biofilm is similar to the one that could be found outside the biofilm. In this case, the resistance to the treatment would be related to a decreased effect of the drug to S. aureus [98, 111]. An interesting compromise can be that several factors influence the efficiency of antibiotic treatment against S. aureus biofilm. Lack of penetration is one of them but cannot be the only answer by its own.
\nWith regards to this, the combination of antibiotics appears as an interesting solution for an effective treatment. Susceptibility test revealed that rifampin, but also vancomycin and fusidic acid were the most interesting constituent of antibiotic combinations active against the staphylococcal biofilms [112]. In an innovative in vitro model, Parra‐ruiz et al. demonstrated that the combination of daptomycin or moxifloxacin with clarithromycin is of greater effect than the individual effects of the three agents against a biofilm formed by a methicillin‐sensible S. aureus (MSSA) strain. Similar observations were made for the combination of linezolid and daptomycin as well as for daptomycin and rifampicin against a MRSA strain [113, 114]. However, recent studies suggested that combination of antibiotics could also have an antagonistic effect on the elimination of S. aureus biofilm. It was reported that linezolid can antagonize vancomycin and daptomycin activities [115]. In an infective endocarditis model of biofilm‐forming MRSA, Laplante and Woodmansee observed that rifampin and gentamicin antagonized or delayed the bactericidal activity of daptomycin and that daptomycin monotherapy had better in vitro activity than vancomycin‐containing combinations [116]. Moreover, according to Croes et al., the use of rifampin‐containing combinations against S. aureus biofilm remains unpredictable, ranging from a tendency toward antagonism to some synergism effects [117]. At the opposite, a recent study, analyzing the antibiotic susceptibility of 58 clinical isolates, emphasized that there are no evidence for advice against the daptomycin/rifampin combination therapy for MSSA/MRSA infection.
\nThe efficiency of antibiotic monotherapies or bi-therapies was most of the time evaluated through the use of in vitro models. In vivo models of infection are of high importance to comfort and strengthen the results between the bench and the patient bed. In a MRSA joint prosthesis rabbit infection model, the combination of rifampin with daptomycin was observed to be more effective than a treatment of either of these agents [118]. Similar results were reported about the combination of linezolid with rifampin or vancomycin with rifampin in a rabbit model of MRSA foreign body osteomyelitis [119]. Recently, study tested several antibiotics alone and in combination in a murine model of implant‐associated osteomyelitis. The authors reported that the most effective antibiotic combinations contained rifampicin and that the combinations containing two nonrifampicin antibiotics were not more active than single drugs [120].
\nGlobally, trying to prevent the biofilm formation appears as the most interesting way to fight this kind of infection. In case of full‐formed biofilm infections, using a combination of high‐dosed antibiotics containing rifampicin and/or daptomycin seems to be the best option.
\nIn addition to the difficulties to treat biofilm‐associated infection, there is also the important delay necessary to spot them. The emergency of finding a technical approach to detect biofilm in the analysis laboratories is huge. Some biomarkers have been searched, especially thanks to qPCR (quantitative polymerase chain reaction) techniques. For example, ica genes encoding for PIA can be identified by PCR [47]. However, ica operon is not present in all S. aureus strains [51], and therefore, it cannot be used as a general biomarker. There still is a lack of tool in the diagnosis of biofilm associated infections. It would be necessary to find either a universal biomarker that defines all biofilm species or at least, a biomarker species‐specific detectable in the particular case of the biofilm presence.
Nowadays biofilm existence cannot be ignored anymore. Scientist community has to find new ways of fighting this bacterial social network as to avoid biofilm formation, or to weaken its intrinsic resistance, to disrupt biofilm or to kill bacteria embedded in this structure as detailed by Bjarnsholt et al. [121] and summarized in Figure 3.
Strategies “anti‐S. aureus biofilm.”
Prevention will always be the best strategy to fight against biofilm formation. Moreover, inhibiting the biofilm formation, bacteria stay under “planktonic” form and are much more susceptible to antimicrobial or immune system molecules, and therefore easier to eliminate. Prevention has to be used as a prophylactic strategy, especially for devices implant during surgery [121]. The idea is to avoid bacterial adhesion on material. As a consequence, some anti‐adhesive surfaces are developed to be used in implant manufacturing [122]. For example, titan implants coated with gentamicin showed a local action and a short period release fighting S. aureus early infection and decreasing toxic side effect [123]. This strategy could be applied when the infection is not endogenous as the antibiotic release will end at some point and that the implant turns then again into a perfect bacterial support [121]. To prevent bacterial adhesion, it could be interesting to target molecules responsible of initial attachment as adhesins by using neutralizing antibodies [121]. A vaccine was developed based on 4 antigens involved in biofilm formation of S. aureus. Its efficiency was proved in chronic osteomyelitis rabbit model but only in combination with vancomycin to kill the free bacteria [124]. Inhibition of biofilm development could be also based on the use of enzymes degrading biofilm matrix components [121] such as DNase which avoid the irreversible attachment step but this strategy does not work in in vivo models. Inhibition of biofilm formation could be based on the perturbation of signal like the presence of endogenous nitrite or the addition of exogenous nitrite [76] or
To conclude, the conceptualization of molecules interfering with signals responsible for biofilm program induction could be imagined and this could lead to the presence of only free‐floating bacteria that are more susceptible to antibiotics.
In case the biofilm prevention fails, other strategies have to be developed. Weakening strategies are based on the idea of avoiding the biofilm properties set up, being efficient only on biofilm in formation not on mature biofilm [121]. Targets of this strategy are virulence factors, communication molecules or specific metabolic pathway involved in biofilm maturation. In S. aureus, Agr quorum‐sensing system and Agr‐regulated PSMs are key controllers of biofilm structure. In consequence, they are the perfect targets for vaccines or drugs [28, 127]. RNAIII‐inhibiting peptide negatively regulates quorum‐sensing response, and in consequence, it can reduce S. aureus biofilms in vivo [128].
\nMolecules interrupting the production or assembly of amyloid fibers could consequently destabilize biofilm structure. The compound (-)‐epi‐gallocatechine gallate (EGCG) used to fight against amyloid peptides involved in Alzheimer\'s and Parkinson\'s diseases is also active to inhibit S. aureus biofilm [53]. Another example is the functional micro‐domains which have been discovered in bacterial membranes and their inhibition through the application of zaragozic acid avoids biofilm formation [129].
\nIt will be interesting to develop other vaccines or drugs which target virulence factors that enhance biofilm formation.
As for “weakening” strategies, targeting Agr quorum‐sensing system in S. aureus will be interesting for triggering disruption [28, 127]. Other molecules have been screened for their ability to disperse biofilm. A fatty acid messenger named cis‐2‐decenoic acid produced during P. aeruginosa growth has shown a capacity to disperse S. aureus biofilm [130]. D‐amino acids trigger biofilm disassembly in affecting amyloid fibers and could be a potential strategy to disperse a preformed biofilm [125].
\nAnother target to disrupt biofilm is the matrix, using for example, PIA‐degrading enzymes. Two matrix polymers in staphylococcal biofilms poly‐N‐acetylglucosamine and eDNA could be targeted for their destruction by dispersin B and DNaseI, respectively. Dispersin succeeded in detaching pre‐formed S. epidermidis biofilm but not S. aureus ones, and on the contrary, DNaseI induced a disruption of S. aureus structures and not S. epidermidis ones [62]. However, nucleases do not impact biofilm‐associated infections [66]. Moreover, bacteriophages are known to be involved in biofilm dispersion stage [31]. Therefore, bacteriophages were engineered to produce dispersin B, and biofilm mass reduction was noticed [131, 132].
To eradicate a pre‐form biofilm is the last chance and this strategy remains the most difficult to fathom. Many molecules have been tested but they have to respect many criteria like the non‐cytotoxicity and the non‐pro‐inflammatory effects. Promising molecules are the “anti‐biofilm” peptides inspired by animal antimicrobial peptides (AMPs) which have anti‐inflammatory effects and are efficient to destroy Gram‐positive or Gram‐negative bacteria at very low concentrations [73, 133]. They have also shown their ability to act in synergy with conventional antibiotics, avoiding the use of too high concentrations of each molecule [133].
After the revolutionary discovery of antibiotics, the medical community thought that the battle against microorganisms was won. However, the fight had just begun as bacteria can develop resistant structure named biofilm among other strategies. S. aureus is one of the most common bacteria found on human epidermis thus when physical barrier such as skin is broken, S. aureus could penetrate and adhere to tissue or medical devices. Many S. aureus strains are drug‐resistant (MRSA), and moreover, S. aureus represents the most frequent germ responsible of chronic biofilm‐associated infection. The treatment against this kind of chronic infection is useless in most cases, especially against MRSA. S. aureus is also present in food infection and responsible of intoxication. For all these reasons, the understanding of S. aureus biofilm is necessary in order to develop new strategies to inhibit biofilm formation and/or to eradicate S. aureus biofilm. Nowadays, more and more molecular mechanisms are decrypted: bacterial communication, biofilm formation and dispersion. Consequently, new molecules are targeted but so far most of this targeting has revealed inefficient in in vivo models. Unfortunately, discoveries on biofilm in general and on S. aureus biofilm in particular, represent a drop in the ocean. Bacteria are simple organisms with complex mechanisms. We, scientists and physicians, have to integrate the fact that planktonic bacteria only reflect the optimal conditions of a laboratory environment. `Biofilm is the real enemy, and it changes the all entire picture. New biofilm models have to be developed, especially in vivo models.
We thank Kevin Delaitre for careful proofreading.
Today, information has become the main component of what we produce, do, buy, and consume. Having an economic value in almost all products and services that meet the needs of today’s societies, it has been now obligatory for individuals and organizations to obtain information technologies and to actively use them in both work and social life domains. Hence, in the current information age, where information is seen as power, this situation has made it imperative for organizations to become increasingly information-based and to benefit from information technologies in many processes and activities.
The intensive use of information technologies in many functions and processes has also required some changes in organizations [1]. This is due to the fact that information technologies, unlike traditional technologies, do not only change the technical fields but also affect the communication channels, decision-making functions and mechanisms, control, etc. [2]. Consequently, one of the most striking developments is on organizational structures that are becoming increasingly flattened and horizontal. Relatedly, information technologies have begun to take over the role of middle management, which supports decision-making processes of senior management and has reduced the importance of this level [3, 4, 5]. Similarly, while information technologies enable managers to obtain faster, more accurate, and more information [6, 7, 8], it also provides lower-level managers with more information about the general situation of the organization, the nature of current problems, and important organizational matters [9, 10, 11, 12].
Moreover, information technologies also have an important potential in determining whether organizations have a mechanical or an organic structure [13]. Within the mechanical organizational structures, people do not have much autonomy, and behaviors expected from employees are being careful and obedience to upper authority and respect for traditions. In such organizations, predictability, consistency, and stability are desirable phenomena. In contrast, people in organic structures have more freedom in shaping and controlling their activities, and being enthusiastic, creative, and taking risks have important places among the desired behaviors [14].
Accordingly, information technologies begin to influence the cultural values of the organization over time, through these transformations they create on organizational structures, processes, and operations. In other words, the fact that organizational structures are mechanical or organic causes the formation of diverse cultural values in organizations [15]. Therefore, the desired cultural values in mechanical organizations are quite different from those in organic structures [1, 16, 17]. In this context, this chapter deals with the influences of information technologies on cultural characteristics of organizations along with the reflections of the use of these technologies on organizational structures and their functioning.
When we look at studies on the relations between organizational culture and information technologies, we generally see the studies on the effects of culture on technology adaptation or use [18, 19, 20, 21], as well as on the effects of certain specific information technologies and applications (e.g., e-mail use, group support practices, etc.) on some aspects of any organizational culture [22, 23, 24, 25, 26, 27, 28, 29, 30, 31]. However, the number of studies that consider the use of information technologies as a “whole” and that address “why” and “how” its effects on organizational culture occurred is still limited. And so, this chapter aims to examine and discuss the overall effects of the usage and intensity of information technologies established in organizations on the cultural life within.
In this context, the chapter plan is as follows: Firstly, the basic concepts related to information and information technologies are included. Emphasis is placed on the meaning differences between knowledge and information, and their connections to information technologies are tried to be explained briefly. Secondly, the effects of information technologies on organizational structure are given particular attention. The reason for this is that as a system of values, beliefs, assumptions, and practices [32], organizational culture encompasses many features closely related to structures of organizations. Thirdly, possible links between organizational structure and organizational culture are included. Fourthly, important theoretical approaches and studies on the relationships between information technologies and organizational culture are provided. Finally, by deepening a bit more and by emphasizing key points, some important arguments are discussed.
In the literature, the concepts of information and knowledge are sometimes expressed by a single term, “information.” However, although the concepts of knowledge and information are intertwined, they are two different concepts that have different meanings and describe different phenomena. The reason for this is that knowledge is also included in the concept of information as it is transformed into a commodity when it begins to be processed, stored, and shared by information technologies.
Becoming the basic elements of today’s economic, social, and cultural systems, information is obtained in a certain hierarchy. The images are at the beginning of the process, and the process is completed with a hierarchical staging in the form of data, information, and knowledge, respectively [33]. Image is located in the first step of the process. Humans copy the picture of any object and event they previously perceived by sensory organs. When faced with a similar phenomenon in the later stages of life, these pictures in the mind are redesigned. We call these pictures of realities occurring in the human mind as images [33]. The next stage, the data, contains symbols that represent events and their properties. For this reason, data are expressed as figures and/or facts without content and interpretation [34]. Information that constitutes the next stage of the process and is mixed with knowledge and used interchangeably is expressed as a reporting of one system’s own status to another system [33]. In information, associated data are combined for a specific purpose. Therefore, we can explain information as meaningful data [35]. Knowledge, on the other hand, is defined as personalized information that allows people to fully and accurately grasp what is happening around them and manifests itself in the form of thoughts, insights, intuition, ideas, lessons learned, practices, and experiences [36]. According to Kautz and Thaysen [37] who stated that knowledge is found only in the people’s minds, knowledge is, therefore, a subjective formation. In other words, knowledge is the form of information enriched with interpretation, analysis, and context [38]. However, here, it should be emphasized again by highlighting a very important issue that knowledge is also accepted as information when this knowledge begins to be processed, stored, shared, and used over information technologies. Therefore, after this, when talking about information, one should consider not only the information created by the data brought together in a meaningful way but also the knowledge shared and used over information technologies.
On the other hand, information technologies, used as the most important tool of generating value today, are defined as the technologies that enable processes such as recording and storing data, producing information through certain operational processes, and accessing, storing, and transmitting this produced information effectively and efficiently [39, 40, 41, 42, 43, 44, 45, 46]. The term information technologies is used to cover computer and electronic communication technologies, as they are now inseparably intertwined in literature and everyday use and are generally used in this way [47]. In this context, data processing systems, management information systems (MIS), office automation systems, executive support systems, expert systems, intranet and extranet, electronic mail (e-mail), group applications (groupware), database management systems, decision support systems, artificial intelligence, and telecommunication systems can be given as examples of information technologies [33, 48, 49].
Towards the end of the twentieth century, the rapid changes with the impact of developments in information technologies led to the emergence of customer satisfaction-based, learning, knowledge-based, and constantly changing organizations [50]. The fact that organizations have become considerably information-based and benefit from information technologies intensively in their activities and processes has made also the changes in their organizational structures mandatory [1]. Accordingly, the effects of information technologies on organizational structure will be summarized under the subtitles of differentiation, centralization, and standardization/formalization, which are the three main components of organizational structure [15].
Differentiation within an organization occurs in three ways: Specialization/division of labor, horizontal and vertical differentiation, and hierarchy and size [15]. Specialization refers to the amount of different expertise or types of work [51, 52]. Specialization generally increases the number of subunits and makes it harder to understand the larger structure that people contribute to with their skills and expertise [53]. Information technologies have the potential to reduce this tendency by providing more access to information and experts at this point. In this way, access to information resources provides synergy [54].
Vertical and horizontal differentiation refers to the amount of hierarchical levels in an organization [55]. Information technologies, with the support of problem solving and decision-making, lead to the emergence of more flattened organizational structures as they require fewer levels within the hierarchy [56]. Since information technologies give employees in lower positions more autonomy to harmonize their activities, this can allow them to find and try better methods while performing their work. In this context, we can increasingly see that organizational structures have become horizontal and strengthened and that virtual organizations have begun to emerge as the most cost-effective structure [17].
In terms of hierarchy and size, Heinze and Stuart [4] argue that the mid-level management staff is unnecessary, increases bureaucracy, reduces efficiency, and has no function in organizations any more. Since most of the tasks performed by mid-level executives can be fulfilled by computers, both less costly and faster, information technology has begun to take over the role of mid-level management, which supports the decision-making process of senior management [5]. Sharing the same opinion, Fulk and DeSanctis [57] also stated that the largely witnessed situation in modern organizational designs is the reduction of intermediate-level managers and administrative support.
Centralization points to the extent to which decision-making power within an organization is scattered or centered [58]. Due to increasing local and global competition, many companies have started to leave their strategic decision-making task further down the organization to benefit from the expert people with more precise and timely local knowledge [10]. Information technologies affect these efforts directly in two ways. Firstly, information technologies increase local knowledge by contributing to obtaining closer information about market trends, opportunities, and customers. Secondly, information technologies can create synergies for organizations because, thanks to information technologies, communication and coordination between distributed decision makers, central planners, and senior managers can be realized more effectively and efficiently [59].
However, whether information technologies will lead to centralization or decentralization is a very controversial question. Regarding centralization, it enables managers to acquire faster, more accurate, and more information, reduces uncertainty, and allows them to make decisions that they cannot make before [6, 7, 8]. Conversely, by the use of other forms of information technologies (e.g., electronic bulletin boards), decentralization provides more information to lower- and mid-level managers about the general situation of the organization and the nature of current matters and problems [9, 10, 11, 12]. Raymond et al. [60] argued that because information technologies facilitate the use and transmission of information by all levels and units in the organization, it enables top management, which is the decision authority, to be disabled in certain areas and the decentralization of control. Thach and Woodman [61] maintained that this is due to the fact that as a result of sharing information at lower levels with the help of information technologies, this power of senior management has decreased to a certain extent, and the knowledge and participation of the staff in organizational matters have increased.
The literature shows that information technologies allow both centralization and decentralization. Researchers are in the agreement that information technologies make it possible for organizational managers to leave their decision-making power to a large part of the hierarchical levels without compromising the quality and timeliness of the decision [62, 63]. Keen [64] combined the concepts of centralization and decentralization and used the term “federated organization” in which organizations do not have to choose either because information technologies simultaneously allow centralization-decentralization [64, 65].
Formalization is the process of detailing how activities are coordinated for organizational purposes in order for employees and organizational units to respond routinely to recurring situations [51, 66]. Formalization involves rules, instructions, shared values, and norms [67]. In fact, formalization is based on the objective of more efficiency and less uncertainty [13].
Information technologies provide the ability to reduce the negative effects of formalization by facilitating the documenting and retrieving of information on organizational occurrences and endeavors that make behaviors and processes more consistent through formalization [63]. The more information technologies assist in reducing search times and preventing downtime, the more the administrative cost of formalization decreases and the productivity increases, which ultimately benefits the path to innovation [68].
Different organizational structures lead to the development of different cultural values [15]. The fact that the structure which an organization has established to control its activities and is defined as a formal system consisting of duties and authority relations is mechanical or organic causes the emergence of completely different cultural values, rules, and norms [69]. While mechanical structures are vertical, highly centralized, and almost everything in them are standardized, organic structures are horizontal, decentralized, and based on mutual adaptation [14]. People feel relatively less autonomous in vertical and centralized organizations, and being careful, obeying the upper authority, and respecting traditions are among the desired behaviors. Therefore, in a mechanical organizational structure, there are cultural values where predictability and stability are important [69]. In contrast, in horizontal and decentralized organizations, people can freely choose their own activities and control them. Creativity, courage, and risk-taking are given importance as desired behaviors. Therefore, organic structures contribute to the formation of cultures that value innovation and flexibility [15].
Organizational structure is also important for the development of cultural values that support integration and coordination. In a structure with stable task and role relations, sharing of rules and norms is more since there will be no communication problems and the information flow will be fast [70]. In organizations where the sharing of cultural values, norms, and rules is at a high level, the level of performance also increases [15]. Particularly in team or matrix structures where face-to-face communication is intense, the sharing of these cultural values and common reactions to the problems develop more rapidly [9].
Whether an organization is centralized or not causes different cultural values to emerge. In decentralized structures, authority is divided into subordinate levels, and an environment is created for the formation of cultural values in which creativity and innovation are rewarded [13]. Employees are allowed to use the organization’s resources and work in projects that they want, by spending some of their time in these projects, thus contributing to the production of innovative and creative products and services [15]. The structures of such organizations constitute the cultural values that give their employees the message “as long as it is in the interest of the organization, it is okay to do things in an innovative and the way you want.”
Conversely, in some organizations, it may be more important for employees not to decide on their own and all activities to be followed and controlled by their superiors. In such cases, a centralized structure is preferred to create cultural values that will ensure accountability and obedience [71]. Through norms and rules, all employees are expected to behave honestly and consistently and inform their superiors about wrongs or mistakes, because this is the only acceptable form of behavior within these structures [72].
Since working on the factors that determine the consequences of the adoption and use of information technologies, researchers have focused on people’s beliefs, values, assumptions, and codes of conduct. As a result, they have given names to this research field such as “socio-technical systems,” “social system,” “social structure,” and most recently “culture” [73]. For example, Markus and Robey [23] using “social elements” and Barley [26] using “social system” or “social structure” tried to explain this phenomenon. When examined more closely, it is seen that the details that these authors emphasize while depicting the case are the assumptions, beliefs, and values that exist in common among the group members, and this corresponds to the definition of organizational culture.
Research examining the relationships between information technologies and values, beliefs, and norms belonging to a particular group has gone through certain stages and used rich and complex research models to explain the relationships in each of these stages [74]. In the first studies on information technology applications, it has been suggested that information technologies cause changes in various organizational phenomena including structural features and thus have certain effects on organizations [74]. For instance, in some studies on adoption of groupware software, several researchers have used this deterministic approach to describe how groupware use affects communication and collaboration among employees and their productivity [27, 28]. These studies assume that certain results will certainly emerge after the adoption of information technologies, without considering the motives or activities that shape the use of information technologies by managers and employees. Like much more deterministic studies, these authors often assumed that information technologies would have predetermined influences on the adoption of information technologies, regardless of the environment in which information technologies were applied, how they were applied, and the users’ specific behaviors and particular purposes.
The second group of views concerning the relationships between organizational culture and information technologies includes the fact that information technologies are seen as a tool that can be used for any change that managers desire to make in organizational practices [22]. In studies in this approach, researchers believe that there is a wide range of possibilities to identify changes in organizational culture, structure, processes, and performance [22, 75]. Researchers from this tradition presume that with the right choice of information technologies and appropriate system design, managers can achieve whatever goals they desire.
These works were mostly adopted in the 1980s and reflect a perspective that managers think can manipulate organizational culture in the way they want. Often called “management and control,” “a functional or instrumental approach” to organizational culture, this methodology has caused serious debate in the literature [76]. This approach attributes great powers to the management level in this regard, which conflicts with anthropologists’ views that culture cannot be consciously controlled and goes much deeper to understand it [76]. Robey and Azevido [77] also do not accept the rational thought on the assumption that culture can be manipulated directly in this way.
Studies with this rational perspective in the information technology literature assume that managers can use information technologies as a leverage to make changes in the norms of behavior, strategy, structure, and performance among members within the organization. For example, in studies on group support systems (GSS), we find managers’ beliefs that they can use collaborative technologies to create a more cooperative organizational culture. This perspective was not accepted by Karsten [78] and some experimental research on GSS [30, 79]. Organizational necessity is no longer accepted, as it is viewed by information technology researchers as an overly simple approach [23, 80].
Researchers who take another approach suggest that information technologies and organizational culture can interact with each other to produce various results [22, 23]. These results can be in the form of adoption and effective use of information technologies (if there is a harmony between organizational culture and information technologies) or user reluctance, refusal, or sabotage (if no fit). Researchers who have been working on information systems since the 1980s have focused on understanding information technology features and functionality that cause effective or problematic information technology applications and the interaction between users’ values, assumptions, and other elements of organizational culture. In this regard, Romm et al. [81] argued that many forms of information technologies comprise cultural assumptions embedded within themselves and these assumptions may conflict with existing values of a particular organization. The authors argued that these embedded assumptions present information technologies as a “cultural boundary” and that a cultural analysis should be made to predict compliance or incompatibility. The authors in this approach warn managers to think of organizational culture as a binding limitation in information technology applications. In a warning by Pliskin et al. [76], managers are advised not to try to change the culture of the organization. Regarding this issue, Orlikowski [30] cites Lotus Notes (a group software) application at Alpha Corporation, a consultancy company. In this example, this system, which was established by the CEO of the company only with the benefits to be obtained, did not create the expected effects, became unsuccessful, and disappointed due to reasons such as no cultural analysis and inadequate training. Employees responded to the use of Notes with resistance and refrained from using it. The reason for this was that the employees in this organization, which had a competitive culture where information was seen as a power, avoided sharing information with others. As a result, this incompatibility between the collaborative culture that Notes had in itself and the competitive culture of the organization in question had failed this application of information technologies.
In a different approach, it is stated that information technologies and culture are not fixed and they are more flexible in terms of change [23, 75]. Managers in this approach may set specific goals for the use of information technologies, but actual results of the use of information technologies are not deterministic, and results cannot be predicted or controlled even under the best conditions [23]. The effects of information technologies are not deterministic because technology has interpretable flexibility considering that it can have different meanings for different employees. Similar technology can be interpreted in a different way by distinct people, based on certain assumptions, beliefs, and values. Robey and coauthors [24, 25], for instance, showed that it would be an empty attempt for organizational managers to try to intentionally manipulate the effects of these technologies, since there are many ways that diverse employees can configure a particular technology in different social environments.
Gopal and Prasad [31] also achieved similar results in their work on group support system (GSS), claiming that for researchers seeking fixed laws or regulations on how information technologies affect user behaviors, this would be an impossible goal to pursue. Conversely, the results of using information technologies depend on the symbolic meanings that information technologies have for a particular user. This work of Gopal and Prasad [31] expresses similar results with the work of Barley [26] and Robey and Sahay [25]. The authors stated that the symbolic meanings of certain technologies for users affect their perceptions of information technologies and their specific behaviors.
In the light of the above-mentioned approaches, arguments, and important studies in the literature, it will be useful to discuss some important points by deepening a little more and by emphasizing the key features related to the concepts of information, information technologies, and organizational culture.
First, organizational culture is a complex phenomenon that develops and changes in a historical process [32, 82, 83]. Thus, although it might seem like a plain and simple concept, organizational culture includes many subdimensions and processes. When considered as a complex pattern of these interactions of many factors with each other, it is also a difficult process to identify the direct and indirect effects of information technologies on organizational culture within this cluster of relationships and interactions. Moreover, culture is not a phenomenon that changes and develops in a short time and is therefore open to manipulations of managers. On the contrary, from this point of view, it is not possible to easily achieve control over cultural changes, and it is necessary to go much deeper [76]. So, it is not rational to expect that the rapid developments and changes in information technologies will cause changes in cultural characteristics at the same speed. In this sense, it could be inaccurate to seek direct relationships between two phenomena in question, whose rates of change are quite different.
Second, for cultural changes, there must also be changes in the basic assumptions, beliefs, and values on which the culture is built [84]. It would be misleading to expect little or intensive use of information technologies to cause changes in these rooted assumptions. For the desired changes in these basic assumptions, beliefs, and values, it is necessary to design the structure accordingly, to recruit employees who are qualified for the targeted culture, and to set ethical values and property rights to employees in accordance with this culture [15]. In this sense, information technologies may only catalyze the contribution of organizational structure to organizational culture.
Third, there are many and different types of hardware and software that fall under the scope of information technologies. It is not logical to accept all of them as homogeneous technologies in all aspects (with the same functions and features, similar usage areas, standard conditions they are applied, similar intentions, and behaviors of all users), and it can be, therefore, misleading to carry out research under a single “IT” concept from this perspective. The reason for this is that, as stated in the sections above, cultural features of each information technology application or product embedded in it might be different. The interactions between the cultural characteristics of the environment in which information technologies are applied and the unique cultural contents of information technologies may cause different results on the culture of the organization.
Fourth, contrary to what is believed, some of cultural features that we anticipate to support information technology applications and products may be interpreted otherwise by diverse people contingent on different assumptions, beliefs, and values. In fact, Robey et al. [24, 25] showed that managers cannot control the effects of these technologies, since different users can configure a particular technology in numerous ways in different social environments. Also, Gopal and Prasad [31] argued that this would be an impossible achievement for researchers looking for fixed laws or regulations on how information technologies affect user behaviors.
Fifth, information technologies were defined above as technologies that enable processing, storage, and sharing of information. The key concept in this definition is “knowledge-based” information and not the technology itself. Therefore, what makes information technologies essential and important is the information itself. According to the definition of knowledge, the most significant characteristic that differentiates it from information is its being a product of the human mind [37]. Because knowledge is the interpretation of information and expresses the value produced from it, qualifying information technologies as good-bad, useful-useless, and necessary-unnecessary can be a meaningless evaluation. So, the basic thing that creates value-added for organizations is not the technology used but the information itself, which is processed, stored, and shared on this technology. In this context, even if it is the latest, most advanced, and most expensive technology in the world, if the organization does not have a qualified human resource capable of producing knowledge that will create value-added, an appropriate organizational structure and culture that will activate this creative potential, and a management approach, all investments in these technologies will also be wasted.
This chapter has aimed to examine the impacts of information technologies on organizations’ cultures, and for this purpose, a special emphasis is given to the concept of “organizational structure” within the theoretical framework presented above. The most important reason for this is that relevant literature shows that organizational culture and organizational structure are in a very close relationship. Indeed, when the question items in the Denison organizational culture scale [85], which is the most frequently used in the literature, are examined, it is possible to see that most of these items point to many features of organizational structure concerning centralization, formalization, and differentiation dimensions. Therefore, it is a very rational approach to expect that information technologies can have direct and indirect effects on organizational cultures based on the influences of information technologies on structures of organizations. However, it should be underlined that different and controversial approaches and findings in the literature mentioned above on the relations between information technologies and organizational culture generate question marks in the minds as well.
In this regard, it is already quite difficult to draw a clear picture of the impacts of information technologies on cultural characteristics of organizations. The number of studies on the subject in the literature is still very limited. Accordingly, it is necessary to underline the great need for interdisciplinary studies in this field. But still, this study argues that the main factor that determines the actual impact and value of information technologies, which have become an integral part of human life in today’s world, is the information itself rather than technology, and it should be kept in mind that information technologies can only function as a means or tool in this knowledge-based social, economic, and cultural life. In other words, the determinant of the benefits, meaning, and importance of information technologies might be the conditions created by organizational factors such as cultural environment and organizational structure where knowledge is created, developed, and used and human resources have become the most important capital element and source of wealth.
The author declares no conflict of interest.
IntechOpen implements a robust policy to minimize and deal with instances of fraud or misconduct. As part of our general commitment to transparency and openness, and in order to maintain high scientific standards, we have a well-defined editorial policy regarding Retractions and Corrections.
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\\n\\nIntechOpen wishes to emphasize that the final decision on whether a Retraction, Statement of Concern, or a Correction will be issued rests with the Academic Editor. The publisher is obliged to act upon any reports of scientific misconduct in its publications and to make a reasonable effort to facilitate any subsequent investigation of such claims.
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\n\n4. FINAL REMARKS
\n\nIntechOpen wishes to emphasize that the final decision on whether a Retraction, Statement of Concern, or a Correction will be issued rests with the Academic Editor. The publisher is obliged to act upon any reports of scientific misconduct in its publications and to make a reasonable effort to facilitate any subsequent investigation of such claims.
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