Environment International 53 (2013) 62–73

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Review

Comparative evaluation of antimicrobials for textile applications

Lena Windler a, Murray Height b, Bernd Nowack a,⁎a Empa – Swiss Federal Laboratories for Materials Science and Technology, Technology and Society Laboratory, Lerchenfeldstrasse 5, CH-9014 St. Gallen, Switzerlandb HeiQ Materials AG, Zürcherstrasse 42, CH-5330 Bad Zurzach, Switzerland

Abbreviations: Ag, silver; nano-Ag, nanosilver; AgCl,ZnPT, zinc pyrithione; PHMB, polyhexamethylene biguanconcentration; OIT, n-octyl-isothiazolinone; BIT, benz-islevel; Kow, octanol-water partition coefficient.⁎ Corresponding author.

E-mail address: nowack@empa.ch (B. Nowack).

0160-4120/$ – see front matter © 2013 Elsevier Ltd. Allhttp://dx.doi.org/10.1016/j.envint.2012.12.010

a b s t r a c t

a r t i c l e i n f o

Article history:Received 6 August 2012Accepted 20 December 2012Available online 21 January 2013

Keywords:AntimicrobialTextilesilverTriclosanSilane quaternary ammonium compoundsZinc pyrithione

Many antimicrobial technologies are available for textiles. Theymay be used inmany different textile applicationsto prevent the growth of microorganisms. Due to the biological activity of the antimicrobial compounds, the as-sessment of the safety of these substances is an ongoing subject of research and regulatory scrutiny. This reviewaims to give an overview on the main compounds used today for antimicrobial textile functionalization. Based onan evaluation of scientific publications, market data as well as regulatory documents, the potential effects ofantimicrobials on the environment and on human health were considered and also life cycle perspectives weretaken into account. The characteristics of each compound were summarized according to technical, environmen-tal and human health criteria. Triclosan, silane quaternary ammonium compounds, zinc pyrithione andsilver-based compounds are the main antimicrobials used in textiles. The synthetic organic compounds dominatethe antimicrobials market on a weight basis. On the technical side the application rates of the antimicrobials usedto functionalize a textile product are an important parameter with treatments requiring lower dosage ratesoffering clear benefits in terms of less active substance required to achieve the functionality. The durability ofthe antimicrobial treatment has a strong influence on the potential for release and subsequent environmental ef-fects. In terms of environmental criteria, all compounds were rated similarly in effective removal in wastewatertreatment processes. The extent of published information about environmental behavior for each compoundvaries, limiting the possibility for an in-depth comparison of all textile-relevant parameters across the antimicro-bials. Nevertheless the comparative evaluation showed that each antimicrobial technology has specific risks andbenefits that should be taken into account in evaluating the suitability of different antimicrobial products. Theresults also indicated that nanoscale silver and silver salts that achieve functionality with very low applicationrates offer clear potential benefits for textile use. The regular care of textiles consumes lots of resources(e.g. water, energy, chemicals) and antimicrobial treatments can play a role in reducing the frequencyand/or intensity of laundering which can give potential for significant resource savings and associatedimpact on the environment.

© 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 632. Use of antimicrobials in textile products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63

2.1. Why are antimicrobials used in textiles? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 632.2. Textile products that use antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64

3. Production of antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 643.1. Silver . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 653.2. Triclosan . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 663.3. Silane quaternary ammonium compounds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66

silver chloride; TCS, triclosan; QAC, quaternary ammonium compounds; Si-QAC, silane quaternary ammonium compounds;ides; MEC, measured environmental concentration; PEC, predicted environmental concentration; PNEC, predicted no effectothiazolinone; OBPA, 10,10′oxybispheloxarsine (OBPA); NOEL, no observed effect level; NOAEL, no observed adverse effect

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63L. Windler et al. / Environment International 53 (2013) 62–73

3.4. Zinc pyrithione . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 674. Antimicrobial application on textiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67

4.1. Application rate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 674.2. Durability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68

5. Environmental and health profile . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 685.1. Behavior in the environment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 685.2. Human health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695.3. Development of resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70

6. Use of antimicrobials from a life cycle perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 707. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 70

7.1. Antimicrobial production volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 707.2. Regulatory assessment of antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 717.3. Overall evaluation of antimicrobials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 71

Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

1. Introduction

Textiles are ubiquitous and are used throughout the world forvarious purposes every day. In 2008, the world per capita fiberconsumption was 10.4 kg (FAO and ICAC, 2011). A portion of thetextiles that are consumed today are treated with biocides thatprevent or inhibit the growth of microorganisms. Biocides are usedeither to protect the textile from the effects of microbial growth orto protect the user from harmful microorganisms (Hund-Rinke etal., 2008). For biocidal textile treatment mostly antimicrobials areused which, in contrast to the more general term biocides, excludeother biocide types such as herbicides, insecticides and rodenticides.Textiles treated with antimicrobials are not a recent phenomenonand have been present in the marketplace for decades. The currentuses of antimicrobial textiles range from outdoor applications suchas tents, tarpaulins, awnings, blinds, parasols, sails and waterproofclothing to indoor applications such as shower curtains and mattressticking (Lacasse and Baumann, 2004). They are also used in someconsumer textiles such as sportswear, T-shirts and socks and also inmedical settings for instance in bedding (Hoefer, 2006). In 2000, anestimated 100 thousand metric tonnes of antimicrobial fibers wereproduced (Gao and Cranston, 2008).

Many different compounds are used to impart antimicrobial func-tionality to textiles, ranging from synthetic organic compounds suchas triclosan, quaternary ammonium compounds, polybiguanides,N-halamines through to metals such as silver and naturally derivedantimicrobials such as chitosan (Gao and Cranston, 2008; Purwar andJoshi, 2004; Simoncic and Tomsic, 2010). Antimicrobials for textilesneed to fulfill many different criteria including efficacy against micro-organisms, suitability for textile processing, durability, and a favorablesafety and environmental profile (Gao and Cranston, 2008). Thedevelopment of new and better antimicrobials is an ongoing topic ofresearch (Bshena et al., 2011; Dastjerdi and Montazer, 2010) andantimicrobials based on naturally-derived products are increasinglydiscussed (Joshi et al., 2009). A survey by the European Commission(European Commission, 2009) listed the consumption of biocidalsubstances in Europe as 1546 metric tonnes for use in fibers, leather,rubber and polymerized materials and the demand for functionaltextiles equipped with antimicrobial substances is increasing(Papaspyrides et al., 2009). Since the biological activity of antimicro-bials can also be of potential concern for non-target organisms, theenvironment and human health, the assessment of the safety of biocid-al products is strictly regulated to ensure the safe use of these productsand is also an area of ongoing research.

Many studies have focused on the risks associated with individualantimicrobial substances (Blaser et al., 2008; Dann and Hontela,2011; Madsen et al., 2000; NICNAS, 2007; Wijnhoven et al., 2009)and the discussion on antimicrobial textiles has been largely focusedin recent years on the use of silver and nanosilver (Blaser et al., 2008;

Egger et al., 2009; Nowack et al., 2011; Scheringer et al., 2010). For in-stance several published studies have focused on the release of silverfrom textiles during washing to measure the environmental exposurethrough this process (Benn and Westerhoff, 2008; Benn et al., 2010;Geranio et al., 2009; Lorenz et al., 2012). A study by Kramer et al.(2006) outlined the potential environmental and health problems ofvarious antimicrobial textile treatments giving an emphasis on therisk associated with triclosan. But to date there is no conclusivecomparative risk assessment about the different antimicrobials usedin textiles. In order to properly inform the evaluation and selectionof antimicrobial technologies for textiles, it should be noted thatsilver (including nanosilver) is not the only antimicrobial substancethat is used to impart textiles with antimicrobial properties. It istherefore important to assess the risks and benefits of various antimi-crobial treatment technologies on an equal basis rather than focusingon single substances. The best antimicrobial technologies for textilesshould minimize potential risks while providing durable functionalityand associated benefits.

This review seeks to provide an overview of the various additivesused to impart antimicrobial functionality to textiles and to offer aplatform to evaluate and discuss which antimicrobial agents havepotential to provide the requested benefits with the lowest environ-mental impact. Based on scientific literature, regulatory documentsas well as market information, silver (Ag, including metallic Ag andAgCl nanoforms), triclosan (TCS), silane quaternary ammonium com-pounds (Si-QAC) and zinc pyrithione (ZnPT) were chosen as the focusof the present review. Table 1 presents the chemical formulas andstructures of the organic antimicrobials covered in this review. Ananalysis of the global antimicrobial usage, data on application ratesof the antimicrobials, an evaluation of environmental and humanhealth aspects and life cycle perspectives are discussed and summa-rized in comparison based on multiple criteria.

2. Use of antimicrobials in textile products

2.1. Why are antimicrobials used in textiles?

Textiles may be treated with antimicrobial agents for a range ofreasons depending on the market sector and application area. Antimi-crobials are typically applied to give textiles improved resilienceagainst microorganisms (e.g. preventing destruction of polymers,discoloration) and increased durability of the textile leading to longerlifetime of use (Lacasse and Baumann, 2004). Antimicrobials can alsobe used to protect textiles against colonization of odor-forming bacte-ria (Lacasse and Baumann, 2004). They may also be applied to textilesto play a role in addressing hygiene in clinical and sensitive environ-ments by minimizing the chances for microbial colonization oftextiles and the potential for transfer from fabric surfaces (Heine etal., 2007). There are many strategies for addressing the care and

Table 1Description of organic antimicrobials.

Antimicrobial Chemical class Chemical structure Chemical formula

Triclosan2,4,4′-trichloro-2′-hydroxydiphenyl ether

Chlorinated phenol C12H7Cl3O2

Si-QACe.g. 3-(trihydroxysilyl) propyldimethyl-octadecyl ammonium chloride

Quaternary ammonium compounds C26H58ClNO3Si

Zinc pyrithioneZinc-2-pyridinethiol 1-oxide

Organic metal complex C10H8N2O2S2Zn

64 L. Windler et al. / Environment International 53 (2013) 62–73

cleanliness of textiles, including regular laundering and treatmentwith laundry chemicals. Antimicrobial treatments do not seek towholesale replace laundering and other cleaning methods. Howeverantimicrobial treatments can provide consumers with an option toconsciously reduce the frequency and/or intensity of launderingwhich can give potential for significant savings in water use, energyconsumption and reduced need for chemical consumables in textilecare. Considering that the majority of resources used in the life of atextile occurs in the use and care phase this can be a significant envi-ronmental benefit. For consumers looking for ways to reduce envi-ronmental footprint in daily life, textiles that require less intensityof care can provide a way to contribute to this goal.

The antimicrobials have different modes of action. The antimicrobi-al effect of ZnPT derives from its ability to disrupt membrane transport(Chandler and Segel, 1978). TCS permeates the bacterial cell wall andtargets multiple cytoplasmic and membrane sites such as RNA synthe-sis, the production of macromolecules and blocks the synthesis of fattyacids (Russell, 2004). Quaternary ammonium compounds such asSi-QACs irreversibly bind to the phospholipids and proteins of themembrane, thereby impairing membrane permeability (Maris, 1995).The bactericidal efficacy of silver is caused by multiple mechanismsincluding the strong binding of Ag+ with disulfide (S–S) andsulfhydryl (−SH) groups found in the proteins of microbial cell walls,(Silvestry-Rodriguez et al., 2007) and Ag+ ions disrupting normalmetabolic processes by displacement of essential metal ions such asCa2+ or Zn2+ (Schierholz et al., 1998) leading to cell death.

2.2. Textile products that use antimicrobials

Requirements for antimicrobial treatments differ according to theend use of a textile product. The human toxicity profile is importantfor skin-contact garments, while the photostability of the antimicrobialsubstance is important in the case of outdoor textiles. The strengths andweaknesses of the antimicrobials discussed here (Ag, TCS, Si-QAC and

Table 2Type of antimicrobial used in selected textile applications.

Textile application Ag TCS Si-QAC ZnPT Other organics a)

Apparel (sports, workwear,undergarments etc.)

++ ++ ++ + −

Medical ++ + ++ + −Bedding ++ + ++ − ++Mattresses & mattress covers − (+) + ++ ++Outdoor (tents, tarps) (+) (+) (+) () (++)

++ Effective technology and in common commercial use; + Some technical limitationshowever is in commercial use; ( ) Major limitations but found in commercial use; −Limited applicability and unknown commercial use. a)n-octyl-isothiazolinone (OIT),benz-isothiazolinone (BIT), 10,10′-oxybisphenoxarsine (OBPA);

ZnPT) as well as the end-use requirements that are placed on a sub-stance are reflected in the use pattern of the antimicrobial for differentapplicationswithin the textile sector. Ag, TCS and Si-QAC are commonlyused for apparel textiles and Ag and Si-QAC are also widely used in themedical field (Table 2). ZnPT is often favored for non-skin contact usessuch as mattresses or bedding. Other synthetic organic antimicrobialssuch as n-octyl-isothiazolinone (OIT), benz-isothiazolinone (BIT) or10,10′oxybispheloxarsine (OBPA) are often limited to non-skin contacttextile coatings.

3. Production of antimicrobials

The volume of antimicrobials in the marketplace today ranges fromhigh volume compounds to materials produced only in small volumes.The most prevalent antimicrobials for textile use include metals andmetal salts such as silver, quaternary ammonium compounds (QAC),halogenated phenols such as triclosan, metal–organic complexessuch as zinc pyrithione, polybiguanides such as polyhexamethylenebiguanides (PHMB) and N-halamine compounds (Gao and Cranston,2008; Heine et al., 2007; Joshi et al., 2009; Purwar and Joshi, 2004;Simoncic and Tomsic, 2010). In terms of volumes, QAC, phenols,organo-metal compounds, biguanides and silver are the most domi-nant compounds (Fig. 1). Fig. 1 also shows that in 2004 silver was re-sponsible for treating a 9% market share of antimicrobial textileswhile in 2011 this share had increased to an estimated 25%, indicatingthat while a larger proportion of the textile volume were treated withsilver, silver replaced synthetic organic compounds (hereinafter re-ferred to as organic compounds) that would otherwise have been used

Fig. 1. Active antimicrobial ingredients consumed in textiles for the years 2011 and2004. Data for 2011 are based on an industry estimate (Height, 2011) and data for2004 are modified after Lacasse and Baumann (2004).

Table 3Biocidal Ag consumption and biocidal Ag used in textile applications.

Reference or data source Estimate descriptiona Global biocidal Ag consumption Share of biocidal Ag in total global Ag demandb Global max. biocidal Ag used in textilesc

[metric tonnes] [%] [metric tonnes]

Hund-Rinke et al. (2008) Top-down 140 0.5 45Silver Institute (2011a) Top-down 129 0.5 42USEPA (2011) Bottom-upd 85 0.3 27Burkhardt et al. (2011) Top-down 56 0.2 18Burkhardt et al. (2011) Bottom-up e 29 0.1 9

a The top-down approach estimates the biocidal Ag consumption in textiles on the basis of data on global biocidal Ag consumption in all uses and the bottom-up approach es-timates the global biocidal Ag consumption in textiles based on regional data of Ag used in textile applications and also derives an extrapolated value for the global biocidal Agconsumption in all applications.

b Based on a global silver consumption (all uses) of 27333 metric tonnes in 2010 (Silver Institute, 2011b).c The separation between of biocidal Ag for water treatment and for other uses (maximally used in textiles) is based on data of the Silver Institute (2005a).d The biocidal Ag consumption in textiles was extrapolated from the Ag used as material preservative in the United States and the population number of the OECD member coun-

tries.e The biocidal Ag consumption in textiles was extrapolated from data about different Ag forms produced for textiles in Europe and the population number of the OECD member

countries.

Fig. 2. Ag consumption for all uses (left), biocidal uses (middle) and Ag forms used intextiles (right). Data are from Hund-Rinke et al. (2008), Silver Institute (2005a) andBurkhardt et al. (2011).

65L. Windler et al. / Environment International 53 (2013) 62–73

in significantly higher quantities. The relative market volumes of antimi-crobial consumption in textiles according to market information are asfollows (from high to low): QAC>phenolics>TCS>ZnPT>PHMB>OIT>tolysulfone>TCMTB>DCOIT>sodium pyrithione>silver (BI,2004). Literature sources and market data indicate that Ag, TCS,Si-QAC and ZnPT belong to the most prevalent antimicrobials onthe market today and these four classes of substances were chosenas the focus of the present review. In the subsequent sections thesecompounds are described in detail and antimicrobial productiondata is presented.

3.1. Silver

Silver is an important metal in manufacturing processes and inmany different end products due to its unique properties includingits electrical and thermal conductivity, its optical reflectivity and itsantimicrobial effect (Silver Institute, 2011a). A yearly survey commis-sioned by the Silver Institute (Silver Institute, 2011b) reported a globaldemand of 27,333 metric tonnes in 2010. Hund-Rinke et al. (2008)estimated the market share of all Ag uses, including biocidal Ag appli-cations, based on data of the Silver Institute and a survey of silver sup-pliers. Most of the global consumption was attributed to industrialapplications (38.2%), jewelry and silverware (32.5%) and photography(23.8%) and smaller percentages were attributed to the investmentsector (1.9%) and manufacture of coins and medals (3.1%). Industrialapplications (such as electrical systems, photovoltaic panels and hand-held devices) continue to gain in market share while use of Ag in pho-tography is diminishing (Silver Institute, 2005b, 2011b). Biocidalapplications accounted for less than 0.5% of the Ag supply — equatingto approximately 140 metric tonnes in total. The share of biocidal Agcompared to all Ag applications in Hund-Rinke et al. (2008) wasadapted by Burkhardt et al. (2011) which listed a share of biocidal Agof 0.2–0.5% (56–140 metric tonnes). Another estimate by The SilverInstitute (2011a) outlined new emerging uses of Ag and nano-Ag,and revealed a total biocidal Ag consumption of 129 metric tonnes in2010 (Table 3). From data on different Ag forms used in textiles in Eu-rope (Burkhardt et al., 2011) and on biocidal Ag use in the UnitedStates (USEPA, 2011) two more estimates for the global biocidal Agconsumption were derived by a population-adjusted extrapolation ofthe regional data relative to the biocidal Ag consumption in the OECDcountries. The extrapolation resulted in a global biocidal Ag consump-tion of 29 and 85 metric tonnes. Applications of these 29 to140 metric tonnes of biocidal Ag include many uses including watertreatment, detergents and softeners, paints and finishes, plastics, med-ical applications, sanitary facilities and also fibers and textiles(Hund-Rinke et al., 2008). Two decades ago it was estimated that>90% of biocidal Ag was used for water filters and 3% as algaecides(USEPA, 1992). A more recent estimate for average global consumption

stated that 68% of biocidal Ag is used for water treatment and 32% forother uses (Silver Institute, 2005a). If we take a highly conservative as-sumption that the 32% of ‘other’ biocidal Ag was used for textiles, thiswould equate 9 to 45 metric tonnes biocidal Ag used in textile applica-tions globally (Table 2). In 2004, quantitative market data showed alower value of 3.5 metric tonnes consumed in textiles (BI, 2004).Given the conservative assumption for the current estimate the actualbiocidal Ag consumption in textiles is likely to be at the lower end ofthe given range, even if accounting for the fact that the popularity ofantimicrobial silver applications has been increasing in the last decade.

Biocidal Ag includes different Ag forms that act as sources of silverions (Ag+) which ultimately provide the antimicrobial effect. Thereare three main groups of commercially available silver antimicrobials:silver ion exchangers, silver salts and silver metal (Burkhardt et al.,2011). Silver ion exchangers include silver zirconium phosphates,silver zeolites and silver glasses. Silver salts include silver chloride(AgCl), nanosilver chloride and silver chloride microcomposites.Silver chloride microcomposites are composed of AgCl nanoparticlesattached to titanium dioxide as carrier material (Burkhardt et al.,2011; Kulthong et al., 2010). Metallic silver materials include silvermetal filaments and electrolytically coated fibers, nanosilver metaland silver metal microcomposites. Market data derived from manu-facturer surveys in Europe indicated that silver salts (includingnanosilver chloride) are the most widely used form of Ag in textilesaccounting for 79% (Burkhardt et al., 2011) while metallic Ag and sil-ver ion exchangers are responsible for 13% and 8% of silver use in tex-tiles respectively (Fig. 2). This data does not distinguish betweensilver salts in the nanorange and bulk silver salts. Even though the

66 L. Windler et al. / Environment International 53 (2013) 62–73

term “nanosilver” is conventionally attributed to silver metals, also afraction of the silver salts falls under the nanoparticle definition bythe International Standard Organisation which defines a nanoparticleas having three dimensions in the nanoscale between 1 and 100 nm(ISO, 2010). Taking this into account, between 13 and 79% of all Agin textiles (9–45 metric tonnes) may be in the nanoform, corre-sponding to 1.2–36 metric tonnes globally. To validate this, we usedadditional data to derive an independent estimate on how muchnano-Ag is used in textiles. Data on nano-Ag consumption was ex-trapolated proportionally to the population of the OECD membercountries. This calculation revealed a global nano-Ag consumptionof 53 metric tonnes based on data on nano-Ag production in the Unit-ed States, Japan and Europe (Scheringer et al., 2010), a production of11 to 80 metric tonnes based on data from the United States(Hendren et al., 2011) and to a production of 13 to 55 metric tonnesbased on production data in Europe (Piccinno et al., 2012). Accordingto Piccinno (Piccinno et al., 2012) the share of total nano-Ag used intextiles applications ranges from 30 to 50%, which equals a totalnano-Ag volume used in textiles of 3.4–40 metric tonnes per year.This corresponds well to the range of nano-Ag production providedon the basis of the different Ag forms used in textiles (1.2–36 metric tonnes) however it is considered likely that the actual vol-ume is at the lower end of this range.

3.2. Triclosan

Triclosan (2,4,4′-trichloro-2′-hydroxydiphenyl ether), belongingto the chlorinated phenolic compounds, is applied in a variety ofproducts as an antimicrobial and preservative (Dann and Hontela,2011). It is widely used in disinfectants, soaps, toothpastes, textiles,and personal care products such as shampoos and deodorants(Dann and Hontela, 2011). TCS has a worldwide production of1500 metric tonnes (Bester, 2005) with 350 metric tonnes producedin Europe (Singer et al., 2002) and 450 metric tonnes in the USA (vonder Ohe et al., 2011). These production volumes are consistent withDye et al. (2007) where annual production and import volumes ofTCS were reported in the order of 10 to 1000 metric tonnes for theEU. The Scientific Committee on Consumer Safety (SCCS, 2010) estimat-ed an annual consumption of 450 metric tonnes within the EU.

TCS is primarily used in the personal care sector (NICNAS, 2009;SCCS, 2010). In Australia up to 49% of TCS is used in personal care prod-ucts and cosmetics (NICNAS, 2009) and in the EU 85% is used in

Table 4Application rates in antimicrobial textile products from literature.

Antimicrobial Antimicrobial content [mg/kg textile] Description

Ag (all forms) 0.016–10,300 Experimental analysis of sixteenshower curtain, socks, top mattr

1.5–2925 Experimental analysis of seven c0.4–1360 Experimental analysis of sixteen

wipe, pajama, children body)30–270 Experimental analysis of three c230,000/270,000 Experimental analysis of two me

silver metal wires)0.99–15.16 Experimental analysis of three c2660/21,600 Experimental analysis of two co

metallic silver fibers)2.8–1310 Experimental analysis of four pr0.9–1358 Experimental analysis of five com

TCS 48.9/50.7 Experimental analysis of two comixture of triclosan and triclocatextiles was 3.5/4.5 mg/kg)

167 Concentration assumed for life c7–195 Experimental analysis of five an

Si-QAC 2500 Recommended application rateZnPT 600–2000 Concentration achieved in the fi

durability of equipped textiles2000 Maximal recommended applicat

personal care products, 10% for food contact materials and only 5% isused in textiles (SCCS, 2010). Assuming that 5% of global consumption(1500 metric tonnes) was used in textile manufacture, this would indi-cate that 75 metric tonnes are used worldwide for textile treatment. In2004 the TCS consumption in textiles was 210 metric tonnes accordingto market information (BI, 2004), which corresponds to 15% of theglobal TCS production. A small proportion of global TCS consumption(5 to 15%) is hence applied in the textile industry with other sectorsusing a higher proportion. At 1500 metric tonnes the global TCSproduction is several times higher than the global production of biocid-al Ag (29–140 metric tonnes). TCS consumption in textiles (75–210 metric tonnes) is at least twice as high as the consumption of bio-cidal Ag in textiles (9–45 metric tonnes).

3.3. Silane quaternary ammonium compounds

Quaternary ammonium compounds are a chemical class of cation-ic surface active agents (Simoncic and Tomsic, 2010). In textilemanufacturing they are used as biocides and also as auxiliaries at dif-ferent stages of the manufacturing process, e.g. during pretreatment,for coloring and finishing, as conditioning, antistatic or softeningagents and as detergents (KEMI, 1997; Lacasse and Baumann, 2004).Due to their antimicrobial properties QAC are also used as surface dis-infectants in the food sector and in the medical field (Mullen, 2002),in plant protection products and pharmaceuticals (Uhl et al., 2005).QAC represent a diverse and large group of compounds with 191compounds listed in the PAN Pesticides Database (PAN, 2012). Con-ventionally the term QAC refers to the subgroup of linear alkyl ammo-nium compounds (Morf, 2007) that are composed of a hydrophobicalkyl chain and a hydrophilic counterpart (Uhl et al., 2005). For anti-microbial textile treatments mainly the compounds containing longalkyl chains (12–18 carbon atoms) have been used (Purwar andJoshi, 2004). The dominant compound that is considered in this re-view, is a linear alkyl ammoniumQAC based on silane quaternary am-monium compounds.

Information about QAC and Si-QAC consumption in textiles is limit-ed in the scientific literature. Uhl et al. (2005) reported a global con-sumption of cationic and amphoteric surfactants of 1.16 millionmetric tonnes and stated that the largest share is consumed as fabricsofteners, in toiletries and as textile auxiliaries. According to Wahleand Falkowski (2002) only 4% of cationic surfactants is used for biocidalpurposes and Seidel (2007) gives a QAC production in the United States

Reference

consumer products (sport shirts, underwear,ess etc.)

DEPA (2012)

onsumer products (socks, shirts, trousers) Lorenz et al., (2012)consumer products (socks, underwear, shirts, buff, KEMI (2012)

onsumer products (shirt, teddy bear, towel) Benn et al. (2010)dical products (mask and cloth) (likely containing Benn et al. (2010)

ommercially available shirts Kulthong et al. (2010)mmercially available socks (likely containing Geranio et al. (2009)

oducts (socks, shirts) GSM (2009)mercially available socks Benn and Westerhoff (2008)

nsumer products (shorts and socks) that contained arban (the triclocarban concentration in those two

KEMI (2012)

ycle assessment based on considered literature Walser et al. (2011)timicrobial products (underwear, shorts, sandals) Rastogi et al.(2003)of a silane quaternary ammonium compounds BI (2004)nishing of textile samples to determine wash Morris and Welch (1983)

ion rate in a product registration document USEPA (2008a)

Table 5Total antimicrobial production, consumption in textiles and application rates.

Global antimicrobial production Global antimicrobialconsumption in textiles

Recommended application rates intextiles given as 25/75% quantilesa

[metric tonnes] [metric tonnes] [mg/kg textile]

Biocidal Ag Nano-Ag – 1.2–40 –

Nanosilver metal & silver metal microcomposites 29–140 9–45 33/77Silver chloride, silver zeolite 75/753, 376/1058Silver bulk 6461/21493

Synthetic organics TCS 1500 75–210 3057/9860Si-QAC 344,000b 1128 3158/7720ZnPT >1800c 100 2070/3984

a Based on data in the US National Pesticide Information Retrieval System (NPIRS, 2012).b Number for global QAC production that includes Si-QAC.c Number for global ZnPT consumption in creams, sprays, shampoos (which are the major uses of ZnPT).

Fig. 3. Recommended application rates of different silver forms and organic antimicro-bials. The data was retrieved from the US National Pesticide Information Retrieval System(NPIRS, 2012). For each antimicrobial type a different number of products (nano-Ag: 1,AgCl: 6, Ag zeolite: 6, Ag bulk: 19, TCS: 9, Si-QAC: 22, ZnPT: 7) contained informationabout the application rates for textiles. The bold line in the boxes marks the medianand the edges mark the 75% and 25% quantiles. Outliers outside the range confinedby the whiskers are not depicted in this graph (the upper and also the lower end ofthe whiskers are defined as 1.5 times the interquartile range).

67L. Windler et al. / Environment International 53 (2013) 62–73

of 344 thousand metric tonnes mostly for consumer products. Marketinformation however provided consumption data on biocidal QAC intextiles and listed a global QAC consumption in textiles of 1128 metrictonnes in 2004, most of it being a particular type of Si-QAC,3-(trimethoxysilyl) propyl dimethyl octadecyl ammonium chloride(BI, 2004). Compared to the total volume of QAC consumption in allforms of consumer products this is a very low amount. NeverthelessSi-QAC seems to have the largest consumption volume as textile anti-microbial compared to the consumption volumes of TCS and Ag.

3.4. Zinc pyrithione

Zinc pyrithione is a metallo-organic broad spectrum antimicrobialthat acts against the growth of bacteria, fungi, algae and mildew(Ranke and Jastorff, 2000; USEPA, 2004). The antimicrobial propertyof zinc pyrithione is used in many different end products. For decadesthe compound has been used in particular as a fungicide inanti-dandruff shampoos (Lacasse and Baumann, 2004). ZnPT is alsowell known as an antifouling agent for ship vessels (Thomas andBrooks, 2010) where it was introduced to replace tin compounds.Other common applications include textiles, adhesives, paints, wire/cable insulation and floor coverings (USEPA, 2004).

Themain proportion of ZnPT consumption volume can be attribut-ed to non-textile uses, mainly for the treatment of dandruff, seborrhe-ic dermatitis and psoriasis (Turley et al., 2000; USEPA, 2004). Lamoreet al. (2010) reported that the use of ZnPT for creams, sprays andshampoos exceeds 450 metric tonnes per year in the United States.This value was extrapolated proportionally based on population num-bers to the consumption of the OECD countries, which are assumed tobe responsible for the main share of the worldwide consumedvolume. Accordingly the worldwide ZnPT consumption volume wasestimated to exceed 1800 metric tonnes for applications in the per-sonal care sector. Market information revealed that the global ZnPTconsumption in textiles was 100 metric tonnes in 2004 (BI, 2004).The ZnPT consumption volume in textiles is smaller than the con-sumption of Si-QAC and TCS as textile antimicrobials but higherthan Ag. The antimicrobial production volumes of all compoundsare summarized in Table 5.

4. Antimicrobial application on textiles

4.1. Application rate

One of the factors that influences the antimicrobial activity of bio-cidal substances is the application concentration (Maillard, 2005).The antimicrobial concentration in a textile product (applicationrate) which is required to exert the antimicrobial effect depends onthe type of antimicrobial, the intended purpose of the treated product(e.g. medical vs. general apparel), the fabric construction, the fixationof the antimicrobial to the textile and stability during use (durability)

and the application procedure (bulk incorporation vs. topical treat-ment). In order to examine the application rates of textile productstreated with Ag, TCS, Si-QAC and ZnPT, an analysis of antimicrobialproduct registrations in the United States was conducted. Manufac-turer recommended antimicrobial application rates for textiles, listedin the corresponding product registration labels, were extracted fromthe National Pesticide Information Retrieval System (NPIRS, 2012). TheNPIRS was searched for the following Ag forms and organic com-pounds chosen on the basis of the categories and corresponding PCcodes given in the PAN Pesticides Database (PAN, 2012): Metallicsilver (PC code: 72501), nano-Ag (PC code: 72599), silver chloride(PC code: 72506), silver zeolite (PC code: 221700), TCS (PC code:54901), different Si-QAC types (PC codes: 107401, 107403, 107409and 169160) and ZnPT (PC code: 88002). Most registrations in thecategory “metallic silver” concerned coated fibers and unspecifiedAg forms and also included a number of zeolites, glasses andphosphate complexes. For the data analysis, the silver zeolites werecombined with the silver zeolites listed under PC code 221700, andthe phosphates and glasses were excluded. Since also silver productsregistered as “nano-Ag” can be composed of metallic Ag particles, thecategory “metallic silver” was retitled as “bulk Ag”.

For each antimicrobial substance, between 1 and 22 product regis-trations that provided recommended application rates for textileswere included. The recommended concentrations of the active sub-stance are usually given as mass of active per dry weight of textile(mg/kg textile or ppm). In some product registrations it was distin-guished between application rates for different textile uses (e.g. ap-parel vs. mattresses) or different incorporation methods (topical

68 L. Windler et al. / Environment International 53 (2013) 62–73

application or incorporation into synthetic fibers) and in others only amore general recommendation of possible application rates wasgiven. In order to obtain an average application rate for each antimi-crobial type, some of the input data was further processed. If a rangeof possible application rates for textiles was given, all values withinthis range were included in the dataset as single data points. If a max-imal and a minimal value were given, all data points in between wereconsidered. If only a maximal application rate was given, Monte Carlocalculations were used to generate random data points that were uni-formly distributed below this maximum value. For each compound adifferent number of data points was generated by Monte Carlocalculations. The number of data points generated for a particularcompound was equal to the maximum number of data points in theremaining product registrations of the same compound. These calcu-lations were carried out by using the statistical software environmentR (R Development Core Team, 2008).

The analysis results, presented as medians with the 25/75%quantiles, show that the recommended application rates cover abroad range (Fig. 3). The smallest recommended application rate(on a weight basis) was found for the category nano-Ag with arange of 10 to 100 mg/kg (median: 55 mg/kg). The highest applica-tion rate was found for bulk Ag (e.g. silver coated fibers) with a max-imum of 40000 mg/kg and a median of 12990 mg/kg. Applicationrates for the organic compounds were as follows (from high tolow): TCS>QAC>ZnPT, with medians of 6426 mg/kg, 5439 mg/kgand 3263 mg/kg respectively (Table 5). The application rates of silverchloride (median 753 mg/kg) and silver zeolite (median 617 mg/kg)were between the levels of nano-Ag and the organic compounds.

The application rates given in the product registrations are recom-mendation ranges and do not necessarily reflect the actual applica-tion rates found in textile products on the market. Therefore dataabout the antimicrobial concentration in textile products was addi-tionally compiled from literature (Table 4). The measured range ofAg in a selection of Ag containing products was between 0.016 and270,000 mg/kg. The maximum value was found in a medical maskwhich, given the very high concentration, presumably contained sil-ver metal wires. The smallest measured TCS concentration in a selec-tion of articles was 7 mg/kg and the highest measured TCSconcentration was 195 mg/kg. The literature values of Ag contentscorrespond reasonably well with the recommended concentrationsin Fig. 3, but it should be noted that the measured TCS contents area lot lower than the recommended application rates. This might bebecause the recommended application rates in Fig. 3 apply to abroad range of different textile products, while the experimentallydetermined concentrations in literature apply to specific antimicrobi-al products. Experimentally determined antimicrobial concentrationswere reported only for Ag and TCS. For Si-QAC a product recommen-dation suggested an application rate of 2500 mg/kg. Concentrationsfor ZnPT used to treat textiles and applications levels as indicatedby USEPA ranged from 600 to 2000 mg/kg.

4.2. Durability

Durability of antimicrobial textile treatments is fundamental toensuring that the treated textile maintains its biocidal performancethroughout its life cycle. Washing and wear of the textile can leadto a progressive loss of the antimicrobial, primarily due to dissolutionof the active substance and/or mechanical damage to the fabric ortreated surface. Progressive loss of the antimicrobial can continueuntil the concentration of the active falls below the inhibitory concen-tration, at which point the textile can no longer reliably fulfill its an-timicrobial function. For many textile applications the washdurability is a key parameter for assessing the performance of antimi-crobial treatments. Sun and Worley (2005) state that a durable anti-microbial textile finish should survive at least 50 machine washeswhich is a figure in line with industrial practices. It is a routine part

of the industrial assessment of antimicrobial treatments in practiceto perform activity testing on the initial unwashed textile and alsoafter a series of washes. Treatments that achieve highest washdurability with the lowest application rate (active concentration)are generally favored in the marketplace, so there is a strong tenden-cy towards adoption of the most efficient and highest performingtreatments. Results from routine durability tests from industry aregenerally not available in scientific literature, nevertheless there aresome studies that addressed either the leaching of Ag (Benn andWesterhoff, 2008; Benn et al., 2010; Geranio et al., 2009; Lorenz etal., 2012), the leaching of TCS (KEMI, 2012; Orhan et al., 2007), theleaching of Si-QAC (Kimiran Erdem and Sanli Yurudu, 2008) or theleaching of ZnPT (USEPA, 2008a) from textiles. From this literaturedata it is however not possible to determine the relative durabilityof the different substances because durability is influenced by manydifferent factors. The range of different study designs and textile sub-strates makes the task of compiling a comprehensive comparison ofthe durability of different antimicrobial textiles very difficult. If con-sumer products are used to assess the durability, there is little infor-mation available about the application procedure used to treat thetextile. For instance, the active ingredient may be added in differentstages of the textile manufacturing process, either during spinningof synthetic fibers or it can be applied topically in the final textilefinishing stage (Gao and Cranston, 2008). In any case a strong fixationof the antimicrobial to the textile is desirable to improve the durabil-ity of the antimicrobial (Papaspyrides et al., 2009). As discussedin Section 4.1, antimicrobial treatments typically have a range ofrecommended application rates (Fig. 3) that reflect how much ofthe active is required to offer competitive performance (includingwash durability) and so these values illustrate the trade-off betweenconcentration and durability for the various active substances.

5. Environmental and health profile

5.1. Behavior in the environment

The behavior of a substance in the environment is determinedthrough different characteristics that can serve as measures to assessthe environmental exposure and hazard of antimicrobial compounds.A selection of the most important compound characteristics that aretaken as a basis to compare Ag, TCS, Si-QAC and ZnPT is presentedin this section.

If antimicrobials are released from textiles, they may eventuallyend up in the aquatic environment if they are not removed in thewastewater treatment. Various studies have revealed that large frac-tions of Ag, nano-Ag and TCS are effectively removed during waste-water treatment, namely 85 – 99% for Ag (Blaser et al., 2008), >95%for AgCl (Burkhardt et al., 2010) and metallic nano-Ag (Kaegi et al.,2011) and 90–96% for TCS (Dann and Hontela, 2011). Besides remov-al through sedimentation, degradation is also an important processthat leads to the elimination of the compounds in wastewater andin the aquatic environment. TCS for instance is degradable under aer-obic conditions but can be persistent under anaerobic conditions(NICNAS, 2009). The photolysis half-life for TCS (the main degrada-tion process) has been measured as 41 min and the half-life in lakewater as 10 days (USEPA, 2008b). Data on Si-QAC and ZnPT removalfrom wastewater is unavailable in the published literature. Neverthe-less based on the results of a degradation experiment in aerobic acti-vated sludge, it was concluded that Si-QAC was readily biodegradable(after 6 days, 70% of the substance was degraded) (NICNAS, 2007)and is also expected to rapidly hydrolyze (USEPA, 2007). One of thereasons why ZnPT is considered as suitable antimicrobial in antifoul-ing paints is that degradation is a very rapid process. Photolysis, con-sidered to be the primary degradation process, has a half-life b0.5 h,but also for biodegradation a half-life of b2 h was measured(Konstantinou and Albanis, 2004). As mineral-derived materials, Ag

69L. Windler et al. / Environment International 53 (2013) 62–73

and nano-Ag by definition cannot be considered as biodegradable,however, all Ag forms are subject to transformation processes thatpossibly lead to their removal from the aquatic environment. It hasbeen shown that nano-Ag is immobilized by formation of stable sul-fide complexes (Kaegi et al., 2011). Silver sulfide is very insolubleand is much less toxic and bioavailable than dissolved Ag ornano-Ag (Levard et al., 2012). The formation of silver sulfide wouldthus significantly reduce the risk of silver-based compounds in theaquatic environment. In contrast the formation of degradation prod-ucts is of concern in the case of TCS, which can form degradationproducts such as methyltriclosan that is potentially more toxic thanthe parent compound (Dann and Hontela, 2011). The degradationproducts of ZnPT are less toxic than the parent compound and aregenerally of low concern (Madsen et al., 2000). It has also beensuggested that antimicrobials might disturb nitrifying bacteria criticalto the efficacy of wastewater treatment plants. No effect on nitrifyingbacteria was found at lower TCS concentration (Samsøe-Petersen etal., 2003). For Ag, the literature shows contradictory results. Choiand Hu (2009) found an inhibition of the nitrification process fromnano-Ag in an idealized simulated waste matrix, while Burkhardt etal. (2010) found no effect of nano-Ag on nitrification in real-worldwastewater. Similarly Kaegi et al. (2011) showed that Ag has no sig-nificant impact on the function of wastewater treatment processesfrom laboratory, pilot-scale and municipal-scale waste treatmentsystems.

The octanol–water partition coefficients (Kow) can be a measure ofthe extent to which a specific compound is taken up by organismsand is often a suitable parameter to compare different antimicrobialsubstances, particularly for organic compounds. TCS has the highestbioaccumulation potential with a Kow of 4.8 (Dann and Hontela,2011) followed by Si-QAC with a Kow of 2.9 (NICNAS, 2007). ZnPT incontrast has a much lower bioaccumulation potential with a Kow of0.9 (NRAAVC, 2001) and the Kow of AgCl and Ag+ are 0.09 and 0.03(Reinfelder and Chang, 1999). Since substances with a Kow>3 areconsidered as substances that bioaccumulate because they are morelikely to partition into lipids than to stay in the aqueous environment(Thomas and Brooks, 2010), TCS and Si-QAC are more problematicaccording to this measure. Despite its low Kow there is also some con-cern about the bioaccumulation potential of ZnPT (Marcheselli et al.,2010).

Comparison of environmental concentrations in the aquatic envi-ronment is important to assess if different antimicrobials present atoxicity risk to aquatic life and is typically performed in risk assess-ment of individual substances. The measured (MEC) and predictedenvironmental concentrations (PEC) for each antimicrobialcompound are shown in Fig. 4. The long historical use of Ag and

Fig. 4. Measured environmental concentrations (MEC), predicted environmentalconcentrations (PEC) and predicted no effect concentration (PNEC) for the aquaticenvironment (note the log scale). Data was extracted from the following papers andreviews: nano-Ag predicted (Gottschalk et al., 2009); Ag measured (Luoma, 2008;USEPA, 2010, 2011); Ag predicted (Blaser et al., 2008); TCS measured (Dann andHontela, 2011; NICNAS, 2009; SCCS, 2010); TCS predicted (NICNAS, 2009;Samsøe-Petersen et al., 2003); Si-QAC predicted (NICNAS, 2007); ZnPT measured(Thomas, 1999); ZnPT predicted (Madsen et al., 2000; Turley et al., 2000). n.a.: nodata available; bdl: below detection limit.

also more recent use of TCS have led to measurable backgroundconcentrations in the aqueous environment, for Ag between 0.03and 1000 ng/L and for TCS 0.001 and 40,000 ng/L (Dann andHontela, 2011; Luoma, 2008; NICNAS, 2009; SCCS, 2010; USEPA,2010, 2011). Whereas the signal of the synthetic TCS is solely the re-sult of relatively recent human use, the environmental Ag concentra-tion is composed of a natural background level from soil and mineralsources together with Ag derived from human use over a period ofcenturies (e.g. cutlery, currency). Published data for MEC of nano-Agand Si-QAC was unavailable and for ZnPT only concentrations belowthe detection limit have been reported (b20 ng/L) (Thomas, 1999).The PEC for all antimicrobials also stretches across a large range. Fornano-Ag, Si-QAC and ZnPT only modeled concentrations are available.The predicted no effect concentrations (PNEC), which indicate theconcentration up to which no adverse effect on the most sensitive or-ganisms can be expected, are in the range of the PEC and MEC valuesfor all compounds except for Ag. For Ag the PNEC is below the PEC butstill in the range of the MEC, however, this analysis makes no distinc-tion between biologically active dissolved silver and silvertransformed into sulfides. This implies that the expectation for riskto aquatic life based on a risk quotient (PEC/PNEC) >1 dependsstrongly on the locally measured concentration and chemical com-plexation of the compound. Other studies concluded for nano-Agthat there is no expected risk with risk quotients b1 (Gottschalk etal., 2009; Mueller and Nowack, 2008; USEPA, 2011). Blaser et al.(2008) listed PEC and PNEC values and did not indicate a risk expec-tation from Ag use. A risk assessment for Si-QAC found no expectedrisk for most of the examined scenarios (NICNAS, 2007). For ZnPTone study found no expected risk (Turley et al., 2000) and in anotherstudy ZnPT turned out to be problematic in harbors andunproblematic in the open ocean (Madsen et al., 2000). For TCS onereport expects a risk for aquatic organisms (NICNAS, 2009), two re-ports found a risk quotient >1 but did not generalize their finding(Remberger et al., 2005; Samsøe-Petersen et al., 2003) and anotherrisk assessment by von der Ohe et al. (2011) suggested the monitor-ing of triclosan as priority substance.

5.2. Human health

Exposure pathways and potential health effects need to be consid-ered in order to evaluate the safety of antimicrobial compounds forhumans. The type of active material (free or bound), the concentra-tion in the product, the routes of exposure and the frequency of useall influence the extent to which humans may be exposed to antimi-crobials in a textile product (Wijnhoven et al., 2009). Potential expo-sure routes are comparable for Ag, nano-Ag, TCS, Si-QAC and ZnPT asthey may all be used for skin-contact uses and so people can poten-tially be exposed to the compounds through dermal, oral or inhala-tion pathways. Among the parameters that are usually assessed todetermine the risk profile of an antimicrobial are toxicity (acute andchronic), skin sensitization and irritation, disturbance of skin ecologyas well as genotoxicity, mutagenicity, carcinogenicity and teratoge-nicity (Kramer et al., 2006). Antimicrobials are designed to specifical-ly address microorganisms but most of them have a relatively lowacute toxicity to humans with oral LD50 (lethal dose at which 50% ofthe test animals die) measured in rats between 92 mg/kg for ZnPT(SCCNFP, 2002) and >5000 mg/kg for Ag (USEPA, 1992) and Si-QAC(USEPA, 2007). Skin sensitization and (sub)chronic toxicity are highlyrelevant parameters for textile antimicrobials and may be used tocompare the hazardous effects of various substances. There are noconcerns for skin sensitization for bulk Ag (USEPA, 1992) andnano-Ag (Christensen et al., 2010) and there is only limited concernfor dermal sensitization for ZnPT (USEPA, 2008a), there is howeverevidence of skin sensitization for Si-QAC (NICNAS, 2007) and forTCS (Hahn et al., 2010). Chronic toxicity studies aim to identify suit-able NOAEL (no observed adverse effect level) or NOEL (no observed

70 L. Windler et al. / Environment International 53 (2013) 62–73

effect level) to determine the chronic harmful doses of a substance.The studies reviewed here indicate that ZnPT has an oral NOAEL inrats of 0.5 mg/kg/day (SCCNFP, 2002) compared to oral NOAEL inrats of 40 mg/kg/day for TCS (NICNAS, 2009), 30 mg/kg/day fornano-Ag (USEPA, 2011), 240 mg/kg/day for Si-QAC (USEPA, 2007)and an oral NOEL in rats of 63.5 mg/kg/day for bulk Ag (USEPA,1992). For all antimicrobial compounds discussed in this reviewthere remain open questions regarding toxicity and effects onhuman health that can benefit from further research. Ag for instanceis seen as relatively non-toxic to humans and nano-Ag continues tobe a topic of intense research (Christensen et al., 2010). Fornano-Ag it should be noted that historical data and real-life experi-ence with nanoparticulate Ag (such as colloidal silver) strongly sug-gests that the toxicity of nano-Ag is not significantly different tobulk or dissolved Ag (Nowack et al., 2011). This was also confirmedin a recent study that allocated the antimicrobial effect of nanosilverentirely to the release of silver ions and reported the absence ofparticle-specific effects (Xiu et al., 2012). The effects and toxicity ofTCS are of concern as TCS is suspected to act as an endocrine disrupter(Dann and Hontela, 2011) and has been observed to be distributed inhuman tissues (Adolfsson-Erici et al., 2002). Dann and Hontela(2011) consider the use of TCS as safe but emphasize that further re-search is required to exclude adverse effects. Although Si-QAC is acorrosive chemical, the USEPA does not expect any severe effects ofSi-QAC use on human health (USEPA, 2007) and ZnPT may presentsome risks due to potential for developmental and neurotoxicity(USEPA, 2008a).

5.3. Development of resistance

For any substance that addresses microorganisms there is a needto consider the potential for development of resistance. The propensi-ty to induce resistance depends on the chemical nature of thesubstance, on the properties of the microorganisms and on environ-mental conditions (Maillard, 2005). An important factor for risk ofresistance development is if the antimicrobial substance has a singlemode of action against the target microorganism and particularly ifit shares a mode of action with antibiotics used in clinical environ-ments (Kuck and Kugler, 2001). In contrast, antimicrobials withmultiple modes of action are generally associated with lower risk ofresistance development. The impact of these factors on the risk todevelop widespread resistance under environmentally relevantconditions needs to be carefully evaluated.

As for many antimicrobial substances, TCS, QAC, Ag and ZnPT haveexhibited development of resistance in some microorganisms underidealized laboratory conditions (Guardiola et al., 2012; Malek et al.,2009; SCCS, 2010; SCENIHR, 2009). For a discussion of the underlyingprocesses related to the potential for acquisition of resistance werefer to the literature, e.g. (Dann and Hontela, 2011; Silver, 2003).TCS has been thoroughly investigated with respect to potential forresistance in the laboratory, nevertheless the Scientific Committee onConsumer Safety (SCCS, 2010) highlights that despite the fact that theTCS levels in the environment might theoretically lead to the develop-ment of resistance, there is a lack of evidence if the compound inducesresistance in real-life. Similarly for Ag an extensive survey of wild bac-teria strains showed no evidence of resistance to Ag (Jakobsen et al.,2011). Percival et al. (2005) emphasized that despite the long historyof human use, and exposure to natural sub-inhibitory levels of silver,no widespread occurrence of resistance has been observed.

Due to a lack of data on the resistance potential under environ-mentally relevant conditions of the antimicrobials discussed in thisreview and also due to the inherent difficulty of exhaustively survey-ing all bacteria strains and use contexts, it is not possible to reach adefinitive conclusion in respect to which antimicrobial is more orless prone to select for resistance (SCENIHR, 2009). While furtherresearch on this topic is needed to understand fundamental

microbiological mechanisms, there seems to be a large gap betweenidealized laboratory studies and a considered reflection upon any re-alistic potential for risk of resistance development under environ-mentally relevant conditions. It should be noted that antimicrobialuse in textiles is demonstrably a relatively minor use pattern for anti-microbials and any analysis of risk of resistance should be seen incontext of other more prevalent, wide-spread and long-use applica-tion sectors of the substances. Meanwhile the selection of antimicro-bials with multiple modes of action and high durability on the treatedtextile should be preferred.

6. Use of antimicrobials from a life cycle perspective

When selecting antimicrobial treatments for textiles, the advan-tages of a given antimicrobial substance should outweigh the poten-tial environmental costs of the antimicrobial application (Blackburn,2004). Potential environmental benefits of antimicrobial treated tex-tiles include a prolonged useful period of textile wear, potential forless frequent laundry cycles, lower washing temperatures and a re-duction of chemical consumption in each wash cycle. More efficientsubstances that require lower dosing levels while achieving durablefunctionality are desirable (Bauer et al., 2008). Environmental impactof an antimicrobial substance can derive from raw material selection,antimicrobial production, textile treatment processes and subsequentuse and disposal of the product. The first published study to addressthe environmental costs of different antimicrobial textile products in-volved a life cycle assessment of a conventional T-shirt compared toT-shirts treated either with TCS or nano-Ag (Walser et al., 2011).The authors showed that the contribution of the use of TCS tothe greenhouse gas emissions of a T-shirt was insignificant andBlackburn (2004) stated that the additional resources consumed toapply an antimicrobial treatment are negligible compared to the envi-ronmental benefits. Walser et al. (2011) also demonstrated that theenvironmental costs of nano-Ag functionalized T-shirts were highlydependent upon the nano-Ag production technology. Neverthelessmultiple studies agree that the use phase (laundry, drying and iron-ing) strongly influences the environmental performance of textiles(Cartwright et al., 2011; Meyer et al., 2011; Walser et al., 2011). Thepotential environmental benefits of antimicrobial textiles, enabling areduction of energy and water demand during use, should thereforebe considered in the evaluation of antimicrobial use in textiles.Given that there are billions of people on earth using on average10 kg of textiles each year (FAO and ICAC, 2011), the potential bene-fits of antimicrobials textiles to reduce the environmental burden oftextiles should be integral to any discussion on the sustainability oftextiles. While there is clear potential to realize significant environ-mental benefits through antimicrobial treatments, further researchto examine the potential for uptake of modified textile care practicesof consumers would be valuable. Adopting a broader perspective ofthe role that various antimicrobial technologies can play within thetextile sector and evaluating both the environmental costs and bene-fits of these uses would contribute to informing which antimicrobialtechnologies provide the highest benefit while minimizing risks tothe environment and human health.

7. Conclusions

7.1. Antimicrobial production volumes

Up-to date market information on the consumption of antimicro-bials in textiles is scarce. Uncertainty about actual consumption levelswas compounded by different sources referring variously to biocides,antimicrobials or active ingredients. Nevertheless the reviewed dataprovided a valuable contribution to future estimates about antimicrobi-al usage. Synthetic organic compounds clearly dominate the antimicro-bial volumes used in the textiles market (1300–1400 metric tonnes in

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total for TCS, Si-QAC and ZnPT). Silver-based compounds made up onlya minor market fraction (9–45 metric tonnes). A realistic assessmentof antimicrobial textiles must therefore consider the full variety of an-timicrobial substances that are available. Estimates on nano-Ag usagemust always specify which Ag forms are included since the range of es-timated nano-Ag production volumes for textiles is large (1.2–40 metric tonnes). Nanoscale silver may also include silver salts in ad-dition to metallic silver particles.

7.2. Regulatory assessment of antimicrobials

Antimicrobial substances are amongst the most thoroughly regu-lated class of chemicals. Changes in regulations can have a majorinfluence on antimicrobial use patterns and the market share ofparticular compounds. Altering the antimicrobial use pattern in tex-tiles would result in significantly reduced antimicrobial flow to theenvironment only if textiles are a major contributor to the totalusage volume for a given antimicrobial. Textiles are a higher propor-tion of total TCS use for instance compared to the use of QAC wheretextile use is a minor proportion of all QAC uses. It is therefore essen-tial that regulations are made in consideration of the full context ofantimicrobial usage patterns. Similarly a disproportional focus on sin-gle substances, or inconsistency in the regulatory assessment processapplied to different actives, can result in the substitution by less suit-able antimicrobial substances with potentially counterproductiveoutcomes for the environment such as an increased total antimicrobi-al exposure. For example, replacing the 210 metric tonnes TCS usedin textiles can be achieved by either less than 2 metric tonnes ofnano-Ag or by 180 metric tonnes of Si-QAC. Regulatory assessmentof single antimicrobial substances must therefore be informed by abroader perspective of antimicrobial use, taking into account a bal-anced view of risks and benefits of their use in relation to alternativeantimicrobial substances.

7.3. Overall evaluation of antimicrobials

An overall comparison of the antimicrobial substances accordingto selected criteria presented in this review is shown in Table 6. The

Table 6Comparative evaluation of the antimicrobials according to technical, environmental and humthe use of a particular antimicrobial can result in increased exposure (technical criteria) or tand human health criteria); i.e. one black dot indicates low anticipated exposure/impact, moillustrate uncertainty.

Criteria Nano-Aga Ag bulkb TCS Si-

Technical 1 Proportion of overall usein textiles

●●[●] ●● ●● ●

2 Application rate ● ●●● ●● ●●

3 Durable functionality ● ● ●● ●●

Environmental 4 Persistence in the environment ●c ●c ●● ●

5 Removal during wastewatertreatment

● ● ● ●

6 Potential for bioaccumulation ● ● ●●● ●●

7 Environmental concentrations ● ●●● ●● ●●

Human health 8 Dermal sensitizationpotential

● ● ●● ●●

9 Chronic toxicity at lowconcentrations

● ● ● ●

Relative Ranking 1d 4 5 3

n.a.: no data available.a Nano-Ag: includes metallic or salt particles in the nanoform.b Ag bulk: includes metallic silver threads, silver coated yarns, ion-based additives and cc Silver as an element is not degradable, however, it rapidly transforms to environmentad Ranking from 1 (lowest impact) to 5 (highest impact) based on the cumulative numbe

table summarizes three main areas of analysis: 1) technical criteriasuch as consumption volume in textiles, application rates anddurability; 2) environmental criteria such as persistence in the envi-ronment, elimination in wastewater treatment plants, bioaccu-mulation and environmental concentrations and 3) criteria relatedto human health such as sensitization and chronic toxicity. The eval-uation differentiated between different Ag forms. Data relevant tometallic Ag particles or Ag salts in the nano-range was included inthe category “nano-Ag” and data that referred to Ag in general,including ion exchange or bulk Ag (e.g. silver wires) was includedin the category “Ag bulk”.

The proportion of the total antimicrobial consumption used in tex-tiles seemed to be lowest with Si-QAC and highest with nano-Aghowever there is uncertainty about the nano-Ag fraction actuallyused in textiles because a range of silver products use unspecifiedAg forms that are likely based on nanoforms (Nowack et al., 2011).The most favorable application rate (lowest dosing level) was foundfor nano-Ag, in contrast to bulk silver products (such as silverfilaments or silver-coated fibers) that require significantly higher ap-plication rates to achieve the desired functionality. The use of less ma-terial intensive compounds, such as metallic nano-Ag and nanosilverchloride, therefore has clear potential to significantly decrease theoverall environmental burden of antimicrobial exposure. Differentantimicrobial technologies can show a range of durabilities on textilesbut this could not be conclusively assessed based on published litera-ture. The evaluation of durability consequently considered if the anti-microbials are suitable to be incorporated into synthetic fibers whichhas potential to enable a more durable antimicrobial treatment rela-tive to topical treatments (Gressler et al., 2010). The durability ofZnPT was classified as being low compared to silver-based com-pounds. The relative evaluation of the persistency of the compoundsin the environment showed that synthetic organic antimicrobialssuch as TCS can persist in the environment for some time and Agtransforms rapidly into other silver forms. Nevertheless it must beconsidered that Ag cannot be degraded or removed from the environ-ment as it is a mineral substance. For all antimicrobials except forZnPT the data indicated that they can be easily removed in wastewa-ter treatment plants which ultimately results in a low release to the

an health criteria based on reviewed literature. The black dots indicate to which extento which extent the behavior and effects of a compound are of concern (environmentalre black dots indicates higher anticipated exposure/impact and dots in square brackets

QAC ZnPT Comments

●● A small (●) or a large fraction (●●●) of the total compoundconsumption as antimicrobial is used in textiles.

●● The medium recommended application rate for textile products islow (●) or high (●●●).

●● It is technically possible (●) or technically challenging (●●) toproduce a textile with high antimicrobial durability.

● Fast degradation/transformation (●) or limited degradation (●●)under environmental conditions.

n.a. Efficient removal in the wastewater treatment process (●) thatresults in low exposure of the environment.

● Low (●) to high (●●●) potential for bioaccumulation based onoctanol-water partition coefficients.

●● The measured or predicted environmental concentrations are lower(●) or higher (●●●) than predicted environmental no effectconcentrations.

● Low (●) to medium (●●) dermal sensitization potential based onexperimental studies from literature.

●● Chronic toxicity unlikely (●) or likely (●●) at low concentrationsbased on literature values about No Observed (Adverse) Effect Levels.

2

onsiders sources that refer to Ag in general.lly benign silver forms (e.g. silver sulfide) under environmental conditions.r of dots (fewer dots equals lower impact/exposure).

72 L. Windler et al. / Environment International 53 (2013) 62–73

environment. The high bioaccumulation potential for TCS is of con-cern and high environmental concentrations were in particularreported for bulk silver however this should be seen in the contextof silver being a material present naturally in the mineral environ-ment and of the long historical use of silver by humans. In the caseof dermal sensitization in particular TCS and Si-QAC might be ofconcern. ZnPT appears to be the substance with the highest relativetoxicity potential. Due to the lack of published literature, no differen-tiation could be made between the potential to develop resistance ofdifferent antimicrobials and consequently this topic was not includedin the evaluation.

The results of this comparative evaluation indicate that in particu-lar the use of TCS and the use of bulk silver forms (e.g. silver metalthreads and silver coated yarns) requiring high application rates areleast preferable. Nanoscale silver and silver salts that achieve func-tionality with very low application rates offer clear potential benefitsfor textile use. The results of this evaluation should be seen as astarting point to more distinctive scientific assessments of anti-microbials in textiles. The extent of published data varied for thecompounds, complicating the comparison between substances. Ex-periments about the durability of different antimicrobials under con-trolled conditions are necessary to definitively examine whichantimicrobial treatments offer the highest durability, which is animportant parameter for the sustainability of the compounds. Dataon the environmental behavior and environmental concentrationsof the compounds in different environmental compartments and theextent to which antimicrobial use in textiles contributes to the envi-ronmental concentrations compared to other application sectorswill further improve their comparative evaluation. In addition thecomparative evaluation of antimicrobials must consider that all ofthese treatments can play a role in reducing the frequency and/or in-tensity of textile care, which in turn can give potential for significantsavings in water, energy and chemical consumption. The benefits ofparticular antimicrobial substances should be weighed along withthe risks of the compounds to inform practical choices of best avail-able technologies for textiles and also for policy makers to avoidcounterproductive consequences of compound-specific regulatorydecisions on the environment and consumers. Antimicrobialsubstances are available today that provide this balance and theyshould also be the focus of future product development.

Acknowledgements

We thank Fadri Gottschalk from Empa SG for his support in statis-tics. MH wishes to thank Walter Bender for valuable discussions onthe topic. This project was partially funded by HeiQ Materials AG.

References

Adolfsson-Erici M, Pettersson M, Parkkonen J, Sturve J. Triclosan, a commonly usedbactericide found in human milk and in the aquatic environment in Sweden.Chemosphere 2002;46:1485–9.

Bauer C, Buchgeister J, Hischier R, Poganietz WR, Schebek L, Warsen J. Towards aframework for life cycle thinking in the assessment of nanotechnology. J CleanerProd 2008;16:910–26.

Benn TM, Westerhoff P. Nanoparticle silver released into water from commerciallyavailable sock fabrics. Environ Sci Technol 2008;42:4133–9.

Benn T, Cavanagh B, Hristovski K, Posner JD, Westerhoff P. The release of nanosilverfrom consumer products used in the home. J Environ Qual 2010;39:1875–82.

Bester K. Fate of triclosan and triclosan-methyl in sewage treatment plants and surfacewaters. Arch Environ Contam Toxicol 2005;49:9-17.

BI. Biocides in textiles. Biocide Information Services; 2004.Blackburn RS. Life cycle analysis of cotton towels: impact of domestic laundering and

recommendations for extending periods between washing. R Soc Chem 2004;6.Blaser SA, Scheringer M, MacLeod M, Hungerbuehler K. Estimation of cumulative

aquatic exposure and risk due to silver: contribution of nano-functionalized plas-tics and textiles. Sci Total Environ 2008;390:396–409.

Bshena O, Heunis TDJ, Dicks LMT, Klumperman B. Antimicrobial fibers: therapeuticpossibilities and recent advances. Future Med Chem 2011;3:1821–47.

Burkhardt M, Zuleeg S, Kaegi R, Sinnet B, Eugster J, Boller M, et al. Fate of nanosilver inwastewater treatment plants and their impact on nitrification activity in sewagesludge. Umweltwiss Schadst-Forsch 2010;22:529–40.

Burkhardt M, Englert M, Iten R, Schärer S. Entsorgung nanosilberhaltiger Abfälle in derTextilindustrie — Massenflüsse und Behandlungsverfahren. Forschungsbericht.Rapperswil, Schweiz: Hochschule für Technik (HSR); 2011.

Cartwright J, Cheng J, Hagan J, Murphy C, Stern N, Williams J. Assessing the environ-mental impacts of industrial laundering: life cycle assessment of polyester/cottonshirts. Bren School of Environmental Science and Management, University ofCalifornia, Santa Barbara; Mission Linen Supply; 2011.

Chandler CJ, Segel IH. Mechanism of the Antimicrobial action of pyrithione: effects onmembrane transport, ATP levels, and protein synthesis. Antimicrob AgentsChemother 1978;14:60–8.

Choi OK, Hu ZQ. Nitrification inhibition by silver nanoparticles. Water Sci Technol2009;59:1699–702.

Christensen FM, Johnston HJ, Stone V, Aitken RJ, Hankin S, Peters S, et al. Nano-silver —feasibility and challenges for human health risk assessment based on open litera-ture. Nanotoxicology 2010;4:284–95.

Dann AB, Hontela A. Triclosan: environmental exposure, toxicity and mechanisms ofaction. J Appl Toxicol 2011;31:285–311.

Dastjerdi R, Montazer M. A review on the application of inorganic nano-structured ma-terials in the modification of textiles: focus on anti-microbial properties. ColloidsSurf B 2010;79:5-18.

DEPA. Assessment of nanosilver in textiles on the Danish market. EnvironmentalProject No. 1432. Copenhagen: Danish Environmental Protection Agency; 2012.

Dye C, Schlabach M, Green J, Remberger M, Kaj L, Palm-Cousins A, et al. Bronopol, Res-orcinol, m-Cresol and Triclosan In the Nordic Environment. Copenhagen: NordicCouncil of Ministers; 2007.

Egger S, Lehmann RP, Height MJ, Loessner MJ, Schuppler M. Antimicrobial properties of anovel silver-silica nanocomposite material. Appl Environ Microbiol 2009;75:2973–6.

European Commission. Assessment of different options to address risks from the usephase of biocides; 2009.

FAO, ICAC. A summary of the world apparel fiber consumption survey 2005–2008.Food and Agriculture Organization of the United Nation; International CottonAdvisory Committee; 2011.

Gao Y, Cranston R. Recent advances in antimicrobial treatments of textiles. Text Res J2008;78:60–72.

Geranio L, Heuberger M, Nowack B. The behavior of silver nanotextiles during washing.Environ Sci Technol 2009;43:8113–8.

Gottschalk F, Sonderer T, Scholz RW, Nowack B. Modeled environmental concentra-tions of engineered nanomaterials (TiO(2), ZnO, Ag, CNT, fullerenes) for differentregions. Environ Sci Technol 2009;43:9216–22.

Gressler S, Simkó M, Gazsó A, Fiedeler U, Nentwich M. Nano-Textilien. Nanotrust Dos-siers Nr.015. Institut für Technikfolgen-Abschätzung der ÖsterreichischenAkademie der Wissenschaften; 2010.

GSM. Analyser av kemikalier i varor. R 2009:8. Göteborgs Stad Miljöförvaltningen;2009. ISSN 1401-243X.

Guardiola FA, Cuesta A, Meseguer J, Esteban MA. Risks of using antifouling biocides inaquaculture. Int J Mol Sci 2012;13:1541–60.

Hahn S, Schneider K, Gartiser S, Heger W, Mangelsdorf I. Consumer exposure to bio-cides — identification of relevant sources and evaluation of possible health effects.Environ Health 2010;9.

Height MJ. Nanosilver in perspective. Presentation "Health Risk Assessment ofNanosilver" Workshop, 17. February 2011. Berlin: Federal Institute for Risk Assess-ment (BfR); 2011.

Heine E, Knops HG, Schaefer K, Vangeyte P, Moeller M. Antimicrobial functionalisationof textile materials: multifunctional barriers for flexible structure. In: Duquesne S,Magniez C, Camino G, editors. Berlin Heidelberg: Springer; 2007.

Hendren CO, Mesnard X, Droege J, Wiesner MR. Estimating production data for fiveengineered nanomaterials as a basis for exposure assessment. Environ Sci Technol2011;45:2562–9.

Hoefer D. Antimicrobial textiles — evaluation of their effectiveness and safety. CurrProbl Dermatol 2006;33:42–50.

Hund-Rinke K, Marscheider-Weidemann F, Kemper M. Beurteilung derGesamtumweltexposition von Silberionen aus Biozid-Produkten. Umweltbundesamt;2008.

ISO. Technical specification ISO/TS 80004–1:2010(E). Nanotechnologies — Vocabulary.Geneva: International Standard Organization; 2010.

Jakobsen L, Andersen AS, Friis-Møller A, Jørgensen B, Krogfelt KA, Frimodt-Møller N. Silverresistance: an alarming public health concern? Int J Antimicrob Agents 2011;38:454–5.

Joshi M, Wazed Ali S, Purwar R. Ecofriendly antimicrobial finishing of textiles using bio-active agents based on natural products. Indian J Fibre Text Res 2009;34:295–304.

Kaegi R, Voegelin A, Sinnet B, Zuleeg S, Hagendorfer H, Burkhardt M, et al. Behavior ofmetallic silver nanoparticles in a pilot wastewater treatment plant. Environ SciTechnol 2011;45:3902–8.

KEMI. Chemicals in textiles - report of a Government Commission: The Swedish Nation-al Chemicals Inspectorate; 1997.

KEMI. Antibacterial substances leaking out with the washing water - analyses of silver,triclosan and triclocarban in textiles before and after washing. Sundbyberg:Swedish Chemicals Agency; 2012.

Kimiran Erdem A, Sanli Yurudu NO. The evaluation of antibacterial activity of fabricsimpregnated with dimethyltetradecyl (3-(trimethoxysilyl) propyl) ammoniumchloride. J Biol 2008;2:115–22.

Konstantinou IK, Albanis TA. Worldwide occurrence and effects of antifouling paintbooster biocides in the aquatic environment: a review. Environ Int 2004;30:235–48.

73L. Windler et al. / Environment International 53 (2013) 62–73

Kramer A, Guggenbichler P, Heldt P, Junger M, Ladwig A, Thierbach H, et al. Hygienicrelevance and risk assessment of antimicrobial-impregnated textiles. Curr ProblDermatol 2006;33:78-109.

Kuck K, Kugler M. Mikrobiozide Ausrüstung von Textilien und anderen Materialien —Nutzen und Resistenzrisiko. Aachen Textile Conference. Aachen: DeutschesWollforschungsinstitut; 2001.

Kulthong K, Srisung S, Boonpavanitchakul K, Kangwansupamonkon W, Maniratanachote R.Determination of silver nanoparticle release from antibacterial fabrics into artificialsweat. Part Fibre Toxicol 2010;7.

Lacasse K, Baumann W. Textile Chemicals: Environmental Data and Facts. Berlin:Springer; 2004.

Lamore SD, Cabello CM,Wondrak GT. The topical antimicrobial zinc pyrithione is a heatshock response inducer that causes DNA damage and PARP-dependent energy cri-sis in human skin cells. Cell Stress Chaperones 2010;15:309–22.

Levard C, Hotze EM, Lowry GV, Brown GE. Environmental transformations of silvernanoparticles: impact on stability and toxicity. Environ Sci Technol 2012;46:6900–14.

Lorenz C, Windler L, Lehmann RP, Schuppler M, Von Goetz N, Hungerbühler K, et al.Characterization of silver release from commercially available functional (nano)textiles. Chemosphere 2012;89:817–24.

Luoma SN. Silver nanotechnologies and the environment: old problems or newchallenges? Project on Emerging Nanotechnologies. PEN 15: Woodrow WilsonInternational Center for Schlolars; 2008.

Madsen T, Samsøe-Petersen L, Gustavson K, Rasmussen D. Ecotoxicological assessmentof antifouling biocides and nonbiocidal antifouling paints. Environmental ProjectNo. 531. Hørsholm, Denmark: Danish Environmental Protection Agency; 2000.

Maillard JY. Antimicrobial biocides in the healthcare environment: efficacy, usage,policies, and perceived problems. Ther Clin Risk Manage 2005;1:307–20.

Malek SMA, Al-Adham IS, Matalka KZ, Collier PJ. Pseudomonas aeruginosa PAO1 resis-tance to zinc pyrithione: phenotypic changes suggest the involvement of effluxpumps. Curr Microbiol 2009;59:95-100.

Marcheselli M, Rustichelli C, Mauri M. Novel antifouling agent zinc pyrithione: deter-mination, acute toxicity, and bioaccumulation in marine mussels (Mytilusgalloprovincialis). Environ Toxicol Chem 2010;29:2583–92.

Maris P. Modes of action of disinfectants. Rev Sci Tech 1995;14:47–55.Meyer DE, Curran MA, Gonzalez MA. An examination of silver nanoparticles in socks

using screening-level life cycle assessment. J Nanopart Res 2011;13:147–56.Morf L. Projekt Biomik: Biozide als Mikroverunreinigungen in Abwasser und Gewässern;

Teilprojekt 2: Stofflussanalyse für die Schweiz. Quartäre Ammoniumverbindungen;2007.

Morris CE, Welch CM. Antimicrobial finishing of cotton with zinc pyrithione. Text Res J1983;53:725–8.

Mueller NC, Nowack B. Exposure modeling of engineered nanoparticles in the environ-ment. Environ Sci Technol 2008;42:4447–53.

Mullen K. The biocides business - regulation, safety and applications, chapter 11: disin-fectants and public health biocides. In: Knight DJ, Cook M, editors. Wiley-VCHVerlag; 2002. p. 251–66.

NICNAS. Chemical in Sanitized T99-19. Sidney: National Industrial Chemicals Notifica-tion and Assessment Scheme; 2007.

NICNAS. Priority existing chemical assessment Report No. 30 - triclosan. Sidney:National Industrial Chemicals Notification and Assessment Scheme; 2009.

Nowack B, Krug HF, Height M. 120 years of nanosilver history: implications for policymakers. Environ Sci Technol 2011;45:1177–83.

NPIRS. National Pesticide Information Retrieval System; 2012.NRAAVC. Evaluation of the new active zinc pyrithione in the product "International

intersmooth 360 ecoloflex antifouling". Canberra: National Registration Authorityfor Agricultural and Veterinary Chemicals; 2001.

Orhan M, Kut D, Gunesoglu C. Use of triclosan as antibacterial agent in textiles. Indian JFibre Text Res 2007;32:114–8.

PAN. PAN pesticide database; 2012.Papaspyrides CD, Pavlidou S, Vouyiouka SN. Development of advanced textile mate-

rials: natural fibre composites, anti-microbial, and flame-retardant fabrics. ProcInst Mech Eng Part L 2009;223:91.

Percival SL, Bowler PG, Russell D. Bacterial resistance to silver in wound care. J Hosp In-fect 2005;60:1–7.

Piccinno F, Gottschalk F, Seeger S, Nowack B. Industrial production quantities and usesof ten engineered nanomaterials for Europe and the world. J Nanopart Res2012;14:1109.

Purwar R, Joshi M. Recent developments in antimicrobial finishing of textiles — a review.AATCC Rev 2004;4:22–6.

R Development Core Team. A Language and Environment for Statistical Computing. Vienna,Austria: R Foundation for Statistical Computing; 2008.

Ranke J, Jastorff B. Multidimensional risk analysis of antifouling biocides. Environ SciPollut Res 2000;7:105–14.

Rastogi SC, Krongaard T, Jensen GH. Survey of chemical substances in consumer products:antibacterial compounds in clothing articles. Survey No. 24. Copenhagen: Danish Envi-ronmental Protection Agency; 2003.

Reinfelder JR, Chang SI. Speciation and microalgal bioavailability of inorganic silver. EnvironSci Technol 1999;33:1860–3.

Remberger M, Woldegiorgis A, Kaj L, Andersson J, Palm Cousins A, Dusan B, et al. Re-sults from Swedish screening 2005: Subreport 2 Biocides. Swedish EnvironmentalResearch Institute; 2005.

Russell AD. Whither triclosan? J Antimicrob Chemother 2004;53:693–5.Samsøe-Petersen L, Winther-Nielsen M, Madsen T. Fate and effects of triclosan. Envi-

ronmental Project No. 861. Hørsholm, Denmark: Danish Environmental ProtectionAgency; 2003.

SCCNFP. Opinion concerning zinc pyrithione. SCCNFP/0671/03: The Scientific Committeeon Cosmetic Products and Non-Food Products intended for consumers; 2002.

SCCS. Opinion on triclosan (antimicrobial resistance). Brussels: Scientific Committeeon Consumer Safety; 2010.

SCENIHR. Assessment of the antibiotic resistance effects of biocides. Brussels: ScientificCommittee on Emerging and Newly Identified Health Risks; 2009.

Scheringer M, Macleod M, Behra R, Sigg L, Hungerbühler K. Environmental risks asso-ciated with nanoparticulate silver used as biocide. Nanosafety. Household and Per-sonal Care TODAY - n1/2010; 2010.

Schierholz JM, Lucas LJ, Rump A, Pulverer G. Efficacy of silver-coated medical devices.J Hosp Infect 1998;40:257–62.

Seidel A. Kirk-Othmer concise encyclopedia of chemical technology, vol. 1. Hoboken,N.J: Wiley-Interscience; 2007.

Silver S. Bacterial silver resistance: molecular biology and uses and misuses of silvercompounds. FEMS Microbiol Rev 2003;27:341–53.

Silver Institute. Wood preservation, crop protection, nanotechnology among loomingapplications for silver biocides. Silver News, Second Quarter; 2005a (Washington).

Silver Institute. World silver survey 2005: a summary. Prepared byGFMS Ltd.; 2005bSilver Institute. The future of silver industrial demand. Prepared byGFMS Ltd.; 2011aSilver Institute. World silver survey 2011: a summary. Prepared byGFMS Ltd.; 2011bSilvestry-Rodriguez N, Sicairos-Ruelas EE, Gerba CP, Bright KR. Silver as a disinfectant.

Rev Environ Contam Toxicol 2007;191.Simoncic B, Tomsic B. Structures of novel antimicrobial agents for textiles — a review.

Text Res J 2010;80:1721–37.Singer H, Mueller S, Tixier C, Pillonel L. Triclosan: occurrence and fate of a widely used

biocide in the aquatic environment: field measurements in wastewater treatmentplants, surface waters, and lake sediments. Environ Sci Technol 2002;36:4998–5004.

Sun G, Worley SD. Chemistry of durable and regenerable biocidal textiles. J Chem Educ2005;82:60–4.

Thomas KV. Determination of the antifouling agent zinc pyrithione in water samples bycopper chelate formation and high-performance liquid chromatography atmo-spheric pressure chemical ionisation mass spectrometry. J Chromatogr A1999;833:105–9.

Thomas KV, Brooks S. The environmental fate and effects of antifouling paint biocides.Biofouling 2010;26:73–88.

Turley PA, Fenn RJ, Ritter JC. Pyrithiones as antifoulants: environmental chemistry andpreliminary risk assessment. Biofouling 2000;15:175–82.

Uhl M, Gans O, Grillitsch B, Fürhacker M, Kreuzinger N. Grundlagen zur Risikoabschätzungfür quaternäre Ammoniumverbindungen. Wien: Umweltbundesamt; 2005.

USEPA. R.E.D. facts - silver. United States Environmental Protection Agency; 1992.USEPA. Preliminary risk assessment for zinc pyrithione. United States Environmental

Protection Agency; 2004.USEPA. Reregistration eligibility decision for trimethoxysilyl quaternary ammonium

chloride compounds. United States Environmental Protection Agency; 2007.USEPA. Memorandum: zinc 2-pyridinethiol-1-oxide (Zinc Omadine®): occupational

and residential exposure risk assessment for new uses (textiles) on EPA RegNumbers 1258–840 and 1258–841. Washington, D.C.: United States Environmen-tal Protection Agency; 2008a

USEPA. Reregistration eligibility decision for triclosan. United States EnvironmentalProtection Agency; 2008b.

USEPA. External review draft — nanomaterial case study: nanoscale silver in disinfec-tant spray. United States Environmental Protection Agency; 2010.

USEPA. Decision document: conditional registration of HeiQ AGS-20 as a materialspreservative in textiles. United States Environmental Protection Agency; 2011.

von der Ohe PC, Schmitt-Jansen M, Slobodnik J, Brack W. Triclosan-the forgotten prior-ity substance? Environ Sci Pollut Res 2011;19:585–91.

Wahle B, Falkowski J. Softeners in textile processing. Part I: an overview. Rev Prog Color2002;32.

Walser T, Demou E, Lang DJ, Hellweg S. Prospective environmental life cycle assess-ment of nanosilver T-shirts. Environ Sci Technol 2011;45:4570–8.

Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, HeugensEHW, et al. Nano-silver — a review of available data and knowledge gaps inhuman and environmental risk assessment. Nanotoxicology 2009;3:109–38.

Xiu Z, Zhang Q, Puppala HL, Colvin VL, Alvarez PJJ. Negligible particle-specificantibacterial activity of silver nanoparticles. Nano Lett 2012.