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Polyhexamethylene Biguanide:Polyurethane Blend Nanofibrous Membranes for Wound Infection Control

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Polyhexamethylene Biguanide:Polyurethane Blend Nanofibrous Membranes for Wound Infection Control polymers Article Polyhexamethylene Biguanide:Polyurethane Blend Nanofibrous Membranes for Wound Infection Control Anna Worsley 1,2,* , Kristin Vassileva 1,2, Janice Tsui 2 , Wenhui Song 2 and Liam Good 1 1 Royal Veterinary College, Department of Pathobiology and Population Sciences, 4 Royal College Street, London NW1 0TU, UK; [email protected] (K.V.); [email protected] (L.G.) 2 University College London, Centre for Biomaterials in Surgical Reconstruction and Regeneration, Division of Surgery & Interventional Science, 9th floor, Royal Free Hospital, Pond Street, London NW3 2QG, UK; [email protected] (J.T.); [email protected] (W.S.) * Correspondence: [email protected] Received: 20 March 2019; Accepted: 20 May 2019; Published: 22 May 2019 Abstract: Polyhexamethylene biguanide (PHMB) is a broad-spectrum antiseptic which avoids many efficacy and toxicity problems associated with antimicrobials, in particular, it has a low risk of loss of susceptibility due to acquired antimicrobial resistance. Despite such advantages, PHMB is not widely used in wound care, suggesting more research is required to take full advantage of PHMB’s properties. We hypothesised that a nanofibre morphology would provide a gradual release of PHMB, prolonging the antimicrobial effects within the therapeutic window. PHMB:polyurethane (PU) electrospun nanofibre membranes were prepared with increasing PHMB concentrations, and the effects on antimicrobial activities, mechanical properties and host cell toxicity were compared. Overall, PHMB:PU membranes displayed a burst release of PHMB during the first hour following PBS immersion (50.5–95.9% of total released), followed by a gradual release over 120 h ( 25 wt % ≤ PHMB). The membranes were hydrophilic (83.7–53.3◦), gradually gaining hydrophobicity as PHMB was released. They displayed superior antimicrobial activity, which extended past the initial release period, retained PU hyperelasticity regardless of PHMB concentration (collective tensile modulus of 5–35% PHMB:PU membranes, 3.56 0.97 MPa; ultimate strain, >200%) and displayed minimal ± human cell toxicity (<25 wt % PHMB). With further development, PHMB:PU electrospun membranes may provide improved wound dressings. Keywords: PHMB; polyhexanide; wound dressing; polyhexamethylene biguanide; polyurethane; electrospinning; nanofibres; antimicrobial; antiseptic 1. Introduction Preventing and stabilising infection is a global challenge that is growing within healthcare systems. In addition to being a major cause of death, slow healing increases costs and perpetuates patient suffering. For example, one of the most common complications of diabetes mellitus is a chronic diabetic foot ulcer [1]; infection of these ulcers can contribute to serious negative outcomes including limb loss and sepsis [2]. The challenge of infection control is becoming more difficult with rising rates of acquired antimicrobial resistance. This is a worldwide concern that should be taken into consideration in wound infection control. With many populations still overusing antibiotics [3], research into non-antibiotic alternatives is essential. Topical antiseptic treatments are commonly used to prevent infection in wounds; they are effective against a wide range of different types of yeasts, fungi and bacteria and result in relatively low levels of antimicrobial resistance [4,5]. There are many different antiseptic treatments currently used in healthcare [5], and many different delivery systems are being investigated. For example, Polymers 2019, 11, 915; doi:10.3390/polym11050915 www.mdpi.com/journal/polymers Polymers 2019, 11, x FOR PEER REVIEW 2 of 20 Polymerslow levels2019, of11, antimicrobial 915 resistance [4,5]. There are many different antiseptic treatments currently2 of 20 used in healthcare [5], and many different delivery systems are being investigated. For example, silver nanoparticles have shown promise in hydrogel [6] and microemulsion [7] delivery systems, silverchlorhexidine nanoparticles in gel have form shown has displayed promise strong in hydrogel antimicrobial [6] and properties microemulsion [8], and [7] a delivery povidone-iodine systems, chlorhexidinefoam dressing in fully gel form prevented has displayed infection strong in a antimicrobial prospective phase properties 4 study [8], and[9]. aDespite povidone-iodine comprehensive foam dressingresearch fully on antiseptics prevented for infection wound in infection a prospective control, phase many 4 study have [ 9undesired]. Despite side comprehensive effects or have research poor ondelivery antiseptics systems: for wound Silver leads infection to skin control, sensitisatio manyn have and undesiredhas limited side tissue effects penetration; or have poorchlorhexidine delivery systems:causes skin Silver sensitisation; leads to skin iodine-based sensitisation antiseptics and has limited stain the tissue skin penetration; and some of chlorhexidine the delivery causessystems skin for sensitisation;iodine can reduce iodine-based wound antiseptics healing stainor lead the skinto skin and sensitisation some of the delivery[4,5,10]. systemsTherefore, for iodinethere canis a reducerequirement wound for healing more orresearch lead to on skin alternative sensitisation anti [microbials4,5,10]. Therefore, and delivery there systems is a requirement that may for provide more researchreduced on side alternative effects. antimicrobials and delivery systems that may provide reduced side effects. PolyhexamethylenePolyhexamethylene biguanide biguanide (PHMB), (PHMB), also knownalso known as polyhexanide, as polyhexanide, is a polymerised is a polymerised biguanide compoundbiguanide compound used as a used broad-spectrum as a broad-spectrum antiseptic antise [4,11ptic], disinfectant [4,11], disinfectant [4], and [4], preservative and preservative [12]; see[12]; Scheme see Scheme1 . It has1. It provenhas proven to be to ebeffective effective against against a wide a wide range rang ofe of pathogens, pathogens, including including strains strains ofof EscherichiaEscherichia colicoli [11[11,13],,13], StaphylococcusStaphylococcus epidermidisepidermidis [13[13,14],,14], andand eveneven thethe ProtistaProtista AcanthamoebaAcanthamoeba castellaniicastellanii [14[14].]. It hashas previouslypreviously beenbeen thoughtthought toto workwork primarilyprimarily throughthrough microbialmicrobial membranemembrane disruptiondisruption [ 11[11,13,15,16],,13,15,16], however, however, more more recently recently it it was was reported reported to to also also selectively selectively bind bind and and condense condense bacterialbacterial DNA,DNA, arresting arresting bacterial bacterial cell cell division. division. ThisThis mechanicalmechanical antimicrobialantimicrobial mechanismmechanism ofof action action maymay helphelp explainexplain whywhy PHMBPHMB hashas aa lowlow riskrisk for for antimicrobial antimicrobial resistance,resistance, ofof which,which, nonenone hashas beenbeen recordedrecorded despite despite extensive extensive testingtesting since since its its first first synthesis synthesis [ 11[11].]. MammalianMammalian cellscells areare comparatively comparatively unaunaffectedffected by by the the polymer polymer as as it it is is segregated segregated into into endosomes, endosomes, seemingly seemingly protecting protecting the the nuclei nuclei from from its harmfulits harmful effects effects [11], [11], leading leading to faster to faster wound wound closures closures compared compared to other to other antimicrobials antimicrobials [17]. [17]. SchemeScheme 1. 1.The The molecular molecular structure structure of PHMB.of PHMB. The diThefferent different variations variations for end for structures end structures (x) and number (x) and ofnumber repeats of (n) repeats are indicated. (n) are indicated. [12]. [12]. ManyMany di differentfferent methods methods have have been been evaluated evaluated in attempts in attempts to improve to improve the release the of release PHMB [of16 ,18PHMB,19]. For[16,18,19]. example, For there example, is evidence there that is evidence the method that of the loading method and of the loading use of and other the substances use of other are substances important factorsare important for maintaining factors for PHMB’s maintaining microbicidal PHMB’s properties microbicid [19al,20 properties]. Specifically, [19,20]. it has Specifically, been suggested it has been that antimicrobialssuggested that in antimicrobials fibrous form havein fibrous superior form release have superior properties release [20]. Thisproperties may be [20]. due This to an may increased be due surfaceto an increased area, allowing surface for area, a high allowing loading for capacity a high and loading a more capacity gradual and release. a more As agradual strategy release. to improve As a releasestrategy properties, to improve electrospinning release properties, offers a e relativelylectrospinning simple offers and versatile a relatively technique simple to manufactureand versatile atechnique range of nanostructuredto manufacture drug a rang deliverye of nanostructured systems, from monolithicdrug delivery nanofibres systems, to variousfrom monolithic multiple drugnanofibres composition to various systems multiple [21]. drug Llorens composition et al. used systems electrospinning [21]. Llorens to fabricateet al used polylactide:PHMB electrospinning to nanofibresfabricate polylactide:PHMB [22]. Interestingly, nanofibres PHMB was [22]. only Interestingly, released in thePHMB first was 1–4 honly with released a substantial in the amountfirst 1–4 nothours released
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