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Journal of Hazardous Materials 280 (2014) 797–815

Contents lists available at ScienceDirect

Journal of Hazardous Materials

j o ur nal ho me pa ge: www.elsev ier .com/ locate / jhazmat

eview

he biodegradation of monomeric and dimericlkylammonium surfactants

ogumił Brycki ∗, Małgorzata Waligórska, Adrianna Szulcaboratory of Microbiocides Chemistry, Faculty of Chemistry, Adam Mickiewicz University, Grunwaldzka 6, Poznan 60-780, Poland

i g h l i g h t s

The biodegradation of alkylammonium surfactants is described and discussed.The degradation process is very complex and depends on many factors.Monomeric and dimeric alkylammonium surfactants are hard to be degraded.Amide, peptide or carbohydrate substituents facilitate the biodegradation.

r t i c l e i n f o

rticle history:eceived 20 May 2014eceived in revised form 29 July 2014ccepted 6 August 2014vailable online 24 August 2014

eywords:iodegradationuaternary alkylammonium salts

a b s t r a c t

Quaternary ammonium compounds (QACs) are salts known for having antiseptic and disinfectant prop-erties. These compounds are toxic to aquatic organisms and should thus be removed from wastewaterbefore its discharge into surface waters. The biodegradation of QACs takes place in the presence ofmicroorganisms under aerobic conditions. The susceptibility of these compounds to degradation dependson numerous parameters. A number of them, such as the structure-adsorption on solids, and con-centration of the QACs, as well as the presence of additional substances, have been reviewed in thisarticle. Moreover, the biodegradability of new dimeric alkylammonium salts, i.e., cationic gemini surfac-tants, has been discussed and compared with that of anionic and nonionic geminis. The biodegradation

emini surfactantsastewater treatment

study of monomeric and dimeric alkylammonium surfactants show that they are not easily degraded.The degradation process is very complex and strongly depends on the structure of the compound,adsorption–desorption processes on sludge, type of microorganism consortia and the presence of anions.Alkylammonium surfactants with biological motifs, like amide, peptides or carbohydrates, are muchbetter degraded.

© 2014 Elsevier B.V. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2. Biodegradation of quaternary alkylammonium salts . . . . . . . . . . . . . . . . . . . . . .

Abbreviations: ACh-Cl, acetylcholine chloride; AnBUSDiC, test anaerobic biodeonium compounds; BAC, benzalkonium chloride; BNR, biologic nitrogen remova

hloride; C10TMAC, decyltrimethylammonium chloride; C12BAC, dodecylbenzyldimethyetradecylbenzyldimethylammonium chloride; C14TMAC, tetradecyltrimethylammoniuexadecyltrimethylammonium bromide; C16TMAC, hexadecyltrimethylammonium chyltrimethylammonium chloride; C22TMAC, docosyltrimethylammonium chloride; CMC,EEDMAC, diethylesterdimethylammonium chloride; DOC, dissolved organic carbon; Dcotoxicology and Toxicology of Chemicals; FEC, first effect concentration; HEQ, Hamburgnhibition constant; LAS, linear alkylbenzene sulphonate; LCh-Cl, lauroylcholine chloride; Mional Trade and Industry-Japan; OECD, Organization for Economic Co-operation and Develudge; SDS, sodium dodecyl sulphate; SRT, solid retention time; VSS, volatile suspended∗ Corresponding author. Tel.: +48 61 829 1314; fax: +48 61 829 1505.

E-mail address: brycki@amu.edu.pl (B. Brycki).

ttp://dx.doi.org/10.1016/j.jhazmat.2014.08.021304-3894/© 2014 Elsevier B.V. All rights reserved.

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 798 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 800

gradation under sludge digester conditions test; ATMAC, alkyltrimethylam-l; BOD, biochemical oxygen demand; C10DMAC, didecyldimethylammoniumlammonium chloride; C12TMAC, dodecyltrimethylammonium chloride; C14BAC,m chloride; C16BAC, hexadecylbenzyldimethylammonium chloride; C16TMAB,loride; C18DMAC, dioctadecyldimethylammonium chloride; C18TMAC, octade-

critical micelle concentration; DADMAC, dialkyldimethylammonium compounds;TDMAC, ditallowdimethylammonium chloride; ECETOC, European Centre for the

ester quat; ISO, International Organization for Standardization; KI , half-saturatione, methyl group; MIC, minimal inhibitory concentration; MITI, Ministry of Interna-

lopment; QAC, quaternary ammonium compound; SCAS, semicontinuous activated solids; WWTP, wastewater treatment plant.

798 B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815

2.1. Microorganisms. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8002.2. Biodegradation technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8002.3. Biodegradation mechanism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8012.4. QAC biodegradation kinetics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8022.5. Influence of QAC structure on its biodegradation kinetics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8032.6. Influence of QAC adsorption on its biodegradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8032.7. Influence of anions on the biodegradation of QACs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8042.8. Influence of QAC concentration and microbial adaptation on QAC biodegradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 804

3. Biodegradation of gemini surfactants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8054. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 813

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References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

. Introduction

Quaternary ammonium compounds (QACs, quats) are moleculesith at least one long hydrophobic hydrocarbon chain linked to aositively charged nitrogen atom (Fig. 1). The other alkyl groups areostly short-chain substituents such as methyl or benzyl groups.

he counter ions can be either inorganic or organic. QACs havever 10% share in a large group of surfactants, where anionicnd non-ionic surfactants combined account for roughly 85% oflobal demand for surfactants. [1]. Despite the global trend to non-onic surfactants, QACs will remain the widely used surfactants inharmaceutical and fabric softener formulations, cosmetics, com-ercial disinfectants, industrial saniters, food preservatives, and

hase transfer catalysts [2]. Global demand for non-ionic, anionic,mphoteric and cationic surfactants was over 12 million tonnesn 2010 and is projected to rise by 4.5% per year until 2018o generate revenues of more than US$41 billion in 2018. Asia-acific is the largest surfactant outlet, with a roughly 37% sharef global consumption, followed by North America and Westernurope [1].

Residual surfactants are discharged to wastewater treatmentlants (WWTPs) or directly to surface waters and then dispersed

nto the environment. However, surfactants have some negativeffects on surface waters, such as reducing air/water oxygen trans-er, damaging the water quality via the introduction of foam andorption on solid particles, and exerting a toxic effect on aquaticicroorganisms in trophic levels [3]. Hence, it is necessary to

nvestigate the susceptibility of these compounds to biodegrada-ion as well as the mechanisms of this process in the presencef mixed cultures, i.e. microbial consortia with well establishedutual interactions isolated from activated sludge, wastewater,

ediments, and rivers. However, it is hard to predict degradationfficiency or contamination level in the environment due to severalactors.

Two types of biodegradation can be distinguished. The first types primary biodegradation, during which a biological action causesn alteration in the chemical structure of a substance, resulting inhe loss of a specific property of that substance. The second types ultimate biodegradation (mineralisation), in which the test com-ound is completely utilised by microorganisms, resulting in the

roduction of carbon dioxide, water, mineral salts, and new micro-ial cellular constituents (biomass) [4,5].

The ultimate biodegradability (mineralisation) of QACs in aer-bic environments can be measured according to one of the

ig. 1. Structures of quaternary ammonium salts, where R1, R2, R3, R4 = CH3,CnH2n+1 (n = 8–18), CH2C6H5; X = inorganic or organic ions.

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 813

five following methods: the CO2 headspace test, carbon dioxideevolution (modified Sturm test), closed-bottle test, manometricrespirometry test, and MITI test. According to those tests, surfac-tants are readily biodegradable if at least 60% biodegradation isachieved within 28 days. Ultimate biodegradability can be eval-uated using the following tests: dissolved organic carbon (DOC)die-away and modified OECD screening-DOC die-away. The passcriterion of at least 70% of these two methods is considered equiv-alent to the pass criterion of at least 60% referred to in the methodslisted earlier. In all methods testing ultimate biodegradability, pre-adaptation is not required and the 10-day window principle is notapplied [5,6]. Environmental mineralisation is usually determinedwith either radio- or stable isotopes. The most frequently miner-alisation rates are determined by using 14C-labelled start materialand trapping the formed 14CO2 [7].

The primary biodegradability of QACs can be evaluated accord-ing to one of methods mentioned in Regulation EC No 648/2004,based on the disulphine blue active substance analysis orusing appropriate specific instrumental analyses, such as high-performance liquid chromatography [8].

Based on concern for the natural environment, the EuropeanParliament and the Council of the European Union have devel-oped regulations regarding synthetic surfactants. The RegulationEC No 648/2004, along with further amendments, harmonises thebiodegradability of surfactants in detergents and restrictions onor bans of surfactants on grounds of biodegradability. In accor-dance with these regulations, detergents containing surfactantsthat meet the criteria for ultimate aerobic biodegradation (readilybiodegradable surfactants) may be placed on the market withoutfurther limitations relating to biodegradability. For all surfactants indetergents failing ultimate aerobic biodegradation tests, the level ofprimary biodegradability shall be measured, and if it exceeds 80%,the manufacturers of industrial or institutional detergents contain-ing surfactants may ask for derogation [8].

Although anaerobic biodegradation is not required for surfac-tants in the regulations discussed above, there was an intentionto undertake further research to explore improved methods formeasuring anaerobic biodegradability [9]. Knowledge about QACanaerobic biodegradation is important because the strong adsorp-tion of quaternary ammonium compounds on solid particlescan occur in anaerobic environments, such as river sediments,sub-surface soil layers, or sludge digesters of wastewater treat-ment plants. Methods for testing anaerobic biodegradability canbe divided into screening tests for the determination of basicbiodegradability under stringent conditions (e.g., ISO 11734, OECD311) and tests at the simulation level, such as the OECD 314 orAnBUSDiC tests, for the assessment of data under more realisticconditions [9–14]. However, simulation tests are complex, lengthyand expensive; therefore, most surfactants have been aerobicallytested in screening tests [11].

The strategy of OECD tests consists of three levels, i.e., readybiodegradability tests or screening tests, inherent biodegradabilitytests and simulation tests. Biodegradability tests generally neglect

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surface water and sediments; hence, knowledge of their biodegrad-ability has become important. In this paper, the biodegradation ofcationic gemini surfactants will be discussed and compared withthe biodegradation of anionic and nonionic geminis.

B. Brycki et al. / Journal of Haza

inetics, since biodegradation rates are not required for the admis-ion of new chemicals. Nevertheless, the rate of biodegradations fundamental in estimating the environmental concentration of

chemical and, thus, in risk assessment. As biodegradation ratesn different environmental regions can vary significantly, precisestimation and calculation methods of such rates are necessaryo predict environmental concentrations. In general, the readilyiodegradable criterion does not guarantee the safety to environ-ent especially during long time of contact with some xenobiotics.As seen in Table 1, many quaternary ammonium salts show

ow biodegradability. For example, dioctadecyldimethylammo-ium chloride, the major component of the commercial productitallowdimethylammonium chloride (DTDMAC), was mineralisedery slowly, and its ultimate biodegradation was lower than 5%15]. In 1991, DTDMAC, the most widely used surfactant in fab-ic softeners, was found in sewage effluents at concentrations upo 62 �g/l [16] and in treated sludge at concentration 3670 mg/kg17].

Concern about the natural environment resulted in the devel-pment of cleavable surfactants. One of the main approaches takeno produce such compounds is to build into the structure a bondith limited stability [18]. These surfactants are readily biodegrad-

ble (Table 1) and rapidly and completely removed in WWTP;hus, they are not dangerous to the natural environment. Due tohe replacement of DTDMAC with more biodegradable QACs, suchs diethylesterdimethylammonium chloride (DEEDMAC), the con-entration of DTDMAC in sewage sludge declined to 210 mg/kg in994 [17,19]. This trend was also confirmed in a study by Miurat al. concerning the concentration of dialkyl dimethyl ammo-ium chloride in four Japanese rivers in the urban areas of Tokyond Osaka over the years 1998–2007 [20]. However, despite anncrease in the consumption of cleavable surfactants (ester-, amide-

carbonate- and amino-acid-based surfactants) in the last severalecades, quats are still used in many different formulations. Oneuat, benzalkonium chloride (BAC; the mixture of alkyldimethyl-enzyl ammonium chloride homologues C12-C18) is often usedy hospitals, laundries, the food industry, wellness centres, andwimming pools. It was shown that the concentrations of the mostbundant homologue, C12BAC, in wastewater from hospitals andaundries were 2800 and 2100 �g/l, respectively [21].

Many studies have confirmed the presence of QACs in surfaceater and sediments in different countries. Martinez-Carballo et al.

tudied the surface water and sediment samples from differentlaces in Austria and stated that the highest QAC concentration wasecorded for C12BAC, with a maximum of 1.9 �g/l and 3600 �g/kgn water samples and sediments, respectively [22,23]. Ferrer andurlog have reported that BAC concentrations ranged from 1.34 to.38 �g/l in filtered water samples from different rivers in Kansasnd Colorado (USA), while concentrations of BAC homologues inediment samples from the same sampling sites ranged from 22o 206 �g/kg, suggesting the preferential partitioning of BAC onediment from water [24,25].

Recently, the QAC concentrations in sediments from Nework have been measured. In samples of surficial sediments col-

ected from the urbanised lower Hudson River basin, it wasetermined that the concentrations of total quaternary ammo-ium compounds were higher than those of other conventionalrganic contaminants. The most abundant classes of QACs wereialkyldimethylammonium compounds (DADMAC) (26000), fol-

owed by BAC (1500) and alkyltrimethylammonium compoundsATMAC) (520 �g/kg) [26].

The high concentration of QACs was also confirmed in marine

ediments from Jamaica Bay collected between 1998 and 2008 [27].tudies of the occurrence and distribution of alkyltrimethylam-onium compounds revealed total concentrations ranging from

61 to 6750 �g/kg. The dominating homologue was C22TMAC, a

Materials 280 (2014) 797–815 799

component of a mixture called behentrimonium, which accountedfor approximately 80% of the total ATMAC in the studied samples.Moreover, analyses showed an exponential increase in the concen-tration of ATMAC over the last three decades, with a doubling timeof 3.9 years. This increase reflects the greater use of behentrimo-nium and its likely replacement of other products containing otherATMAC homologues in personal care products [27].

The data mentioned above indicate that the biodegradability ofQACs is still an important problem from an environmental pointof view. In our review, we will discuss the biodegradation mech-anisms of those surfactants and a number of factors affectingtheir biodegradation, such as the compound’s chemical structure,sorption on solids, complexation with anionic surfactants, and con-centration as well as microbial adaptation. Moreover, because QACbiodegradation takes place mainly in WWTPs, we will discuss theeffect of quaternary ammonium compounds on the course of deni-trification, nitrification, and anaerobic digestion processes.

In recent years, a new class of very effective surfactants hasattracted industry attention. Double quaternary ammonium salts– gemini surfactants – belong to a new class of very effectivesurfactants. Gemini surfactants possess at least two hydrophobichydrocarbon chains and two hydrophilic quaternary ammoniumgroups, which are connected by a spacer. The spacer can be eitherhydrophobic (polymethylene chain) or hydrophilic (polymethy-lene chain with ether or hydroxyl groups). From a structural pointof view, a spacer can be rigid (aromatic or unsaturated linear hydro-carbons) or flexible (polymethylene chain). The neutral charge ofthe molecule is retained by the presence of counterions, which areusually halide anions [28–32] (Fig. 2.).

Gemini alkylammonium salts show unique interfacial prop-erties in aqueous solution. The critical micelle concentrations ofgemini surfactants are much lower than those of the correspondingmonomeric surfactants [29,30,32–35]. For typical gemini sur-factant, ethylene-1,2-bis(N-dodecyl-N,N-dimethylammonium bro-mide) CMC value is 0.82 mmol/L and surface tension at the criticalmicelle concentration is 30.6 mN/m while for dodecyltrimethy-lammonium bromide (DTAB) these values are 15.1 mmol/L and36.4 mN/m, respectively [35]. Similarly, the values of C20 for 12-2-12 and DTAB are 0.0083 and 0.21 wt%, respectively [32].

The gemini alkylammonium compounds also exhibit a very highantimicrobial activity against bacteria, viruses, moulds, and yeasts[36]. The minimal inhibitory concentrations (MICs) of these com-pounds are in some cases even three orders of magnitude lowerthan those of their monomeric analogues [30,34,37,38]. However,despite the very vast literature dedicated to gemini surfactants,few studies investigate their biodegradability and or their fate inthe natural environment. However, the ever-widening applicationof gemini surfactants increases the possibility of their presence in

Fig. 2. Structures of double quaternary ammonium salts, where s = 2–12, n = 5–18.R1, R2 = CH3, CnH2n+1, CH2C6H5; X – inorganic or organic ions.

800 B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815

Table 1Biodegradability of monomeric cationic surfactants under aerobic conditions.

Compound Concentration (mg/l) Biodegradation Reference

(%) Method

Dioctadecyldimethylammonium chloride – >5 Closed bottle test [15]Decyltrimethylammonium chloride 15 53.7 BODa [67]Dodecyltrimethylammonium bromide 15 52.4 BODa [67]Tetradecyltrimethylammonium bromide 15 13.6 BODa [67]Hexadecyltrimethylammonium bromide 15 8.3 BODa [67]Octadecyltrimethylammonium chloride 15 7.2 BODa [67]Octadecyltrimethylammonium chloride 0.1/l 63-89 SCASb [71]Octadecyltrimethylammonium chloride 15 40 BODa [52]Icosyltrimethylammonium chloride 15 14 BODa [52]Docosyltrimethylammonium chloride 15 0 BODa [52]Tetracosyltrimethylammonium chloride 15 0 BODa [52]Dimethyldodecylammonium lactate 10 72 CO2 evolved [52]Dimethyltetradecylammonium lactate 10 59 CO2 evolved [52]N-[3(dimethylamino)propyl]-octadecanamide lactic acid salt 15 93 BODa [52]N-[3(dimethylamino)propyl]-docosanamide lactic acid salt 10 100 CO2 evolved [52]Dodecyldimethyldecyloxymethylammonium chloride 1 90 Simulation biodegradation test [113]Benzyldimethyldecyloxymethyl-ammomium chloride 1 90 Simulation biodegradation test [113]Diethyloxyesterdimethylammonium chloride 20 80 CO2 evolved [48]N�-lauroylarginine methyl ester 10 90 DOCc [51]N�-lauroyllysine methyl ester 40 90 Headspace test [106]N�-lauroyllysine methyl ester 40 80 Headspace test [106]N�-lauroylarginine-N�-lysine methyl ester 40 60 Headspace test [106]

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. Biodegradation of quaternary alkylammonium salts

.1. Microorganisms

Among the microorganisms that can use various QACs as car-on and energy sources were Gram-negative bacteria belongingo the genus Pseudomonas, which have been identified in acti-ated sludge [39–41]. This was also confirmed recently by Tandukart al., who compared the composition of the microbial commu-ity maintained for over 4 years with an easily assimilated carbonnd energy source or a BAC mixture [42]. The above researcherstated that culture diversity and richness decreased in the pres-nce of BAC and that the species in the BAC-sustained enrichedacterial community were predominantly related to Pseudomonaspp. Quaternary alkylammonium salts have also been catabolisedy Xanthomonas sp. [43]. Patrauchan and Oriel investigatederomonas hydrophila sp. K and found that these microorgan-

sms were able to degrade recalcitrant xenobiotics, such asctadecyldimethylbenzylammonium chloride, dodecyldimethyl-enzylammonium chloride, tetradecyldimethylbenzylammoniumhloride, and trimethylbenzylammonium chloride [44]. However,ecause the toxicity of BAC and benzylamines, the biodegradationrocess was not complete, and its efficacy depended on the initialurfactant concentration [44].

The group of microorganisms capable of QAC degradationnclude the Gram-negative bacteria Thalassospira sp. and the Gram-ositive bacteria Bacillus niabensis isolated from marine sediments45]. The primary biodegradation of hexadecylbenzyldimethylam-

onium chloride carried out by these species was 90%.The surfactants in WWTP are degraded by consortia, which

ay operate on the basis of commensalistic or synergistic rela-ionships [46]. In the case of commensalism, one microorganismenefits, whereas the other is not affected [46]. The most obvi-us commensalistic interaction is the production of a substancelong with its release into the medium by one organism. This sub-

tance is utilised by another microorganism as a growth substrate. Aseudomonas sp. carried out the oxidation of the alkyl chain of hex-decyltrimethylammonium chloride, which resulted in the releasef trimethylamine. It was degraded by bacteria grown together

with Pseudomonas sp., enabling total mineralisation of the quater-nary ammonium salt [47].

Synergistic associations are capable of effecting biodegradationbeyond the separate abilities of each species in the community.Examples of synergistic relationships have been found with thedegradation of decyltrimethylammonium chloride, which is com-pletely mineralised by a mixed culture of Xanthomonas sp. andPseudomonas sp., while the pure cultures have not been capable ofusing the surfactant as a sole source of carbon and energy. Xan-thomonas sp. requires an unidentified cofactor produced by theother bacterium in the consortium [43].

As mentioned above, the degradation products of some surfac-tants can be detected in the effluents of activated sludge plants.The presence of these compounds is related to the solid reten-tion time, which is the most important parameter for controllingsurfactant-degrading microorganisms in wastewater treatment.The formation of a metabolite from a surfactant degraded by a com-mensalistic consortium may occur when the maximum growth rateof the surfactant-degraded microorganism is greater than the max-imum growth rate of the product-utilising microorganisms. Thissuggests that surfactants are only completely degraded when theSRT enables the maintenance of all microorganisms involved in thebiodegradation of the surfactant. If one member of a consortium isremoved, formation of a metabolite may occur [46].

The above data show that the effective degradation of alkylam-monium surfactants in WWPT can be completed by Gram-positiveand Gram-negative consortia of microorganisms, which cooper-ate by chemical commensalism or synergistic relationships andthe solid retention time is the most significant factor that controlssurfactant-degrading microorganisms in wastewater treatment.

2.2. Biodegradation technology

After usage, surfactants are transported with the wastewatersto the wastewater treatment plant. As mentioned in the introduc-

tion, studies of the environmental properties of cleavable quatshave shown that these molecules and their primary metabolitesare readily and ultimately biodegradable in different environments[48–52]. Giolando et al. studying diethylesterdimethylammonium

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B. Brycki et al. / Journal of Haza

hloride (DEEDMAC) under aerobic conditions (OECD 301B test)tated that biodegradability of DEEDMAC was approximately 80%Table 1) [48]. This compound had no adverse effects on the oper-tion of the wastewater treatment plant. Similarly, data obtainedrom properly operating conventional activated sludge treatmentlants in the Netherlands and Germany indicate that the removalfficiency of Hamburg ester quat (HEQ) was higher than 98%.oreover, the concentration of HEQ in the effluent and the concen-

rations of the typical primary biodegradation intermediates of thester quats were determined to be <10 �g/l and 0–4 �g/l, respec-ively [49,53,54]. The aforementioned results indicate that surfaceater receives only very low amounts of ester quats. The biodegra-ation of ester quats can also take place in the absence of oxygen.he ECETOC test was used to assess the anaerobic degradation ofEEDMAC and HEQ. The results indicated that 90% of DEEDMAC atay 60 and 83% of HEQ at day 28 were recovered as carbon dioxidend methane [48,49]. The results obtained by Watson et al. whennvestigating the biotransformation of acetylcholine chloride andauroylcholine chloride under methanogenic conditions showedhat ACh-Cl up to 300 mg/l was not inhibitory to methanogeniculture, while LCh-Cl above 50 mg/l inhibited methanogenesis [55].elow inhibitory concentrations, both ester quats were completelyransformed to methane, carbon dioxide, and ammonia.

Several studies have investigated the concentration of qua-ernary ammonium compounds not containing weak bonds inastewaters and WWTP effluent. Clara et al. have monitored the

oncentrations of BAC, DADMAC, and ATMAC in the influent ofeveral WWTPs [56]. They have reported that the most abun-ant C12 homologue of BAC, C10 homologue of DADMAC, and C16omologue of ATMAC were present at concentrations up to 170,00, and 27 �g/l, respectively. The effluent concentrations of theseomologues were 340, 250 and 25 times lower than the corre-ponding influent concentrations, respectively. Similar data haveeen obtained by Martinez-Carballo et al. [22]. The concentration of12BAC, C10DMAC, and C16TMAC in the influent were up to 170, 30,nd 9.1 �g/l respectively, whereas the contamination of effluentsy quats was low, with concentrations generally below 1 �g/l. Qua-ernary ammonium compounds are easily adsorbed onto sewageludge; for example, the total concentrations of QACs in sludgeamples estimated by Martinez-Carballo et al. ranged from 22 to03 mg/kg [23]. Hence, one can assume that quaternary ammo-ium compounds can be removed in WWTP in two different ways:egradation by microorganisms and adsorption to sewage sludge.he relative contributions of these pathways to QAC eliminationepend on the structure of the QAC [57].

Due to their antibacterial properties, quaternary ammoniumalts can exhibit detrimental effects on the performance of waste-ater treatment plants, especially biologic nitrogen removal and

ewage sludge digestion. BNR is a combination of two processes:itrification, during which ammonium is oxidised to nitrate in theresence of oxygen, and anoxic denitrification, during which nitrate

s reduced to dinitrogen in a four-step reaction, nitrate → nitrite nitric oxide → nitrous oxide → dinitrogen [22]. The effect of

AC on wastewater treatment depends on the type of surfactantnd its concentration. Pitter found that hexadecyltrimethylam-onium bromide (C16TMAB) strongly inhibited nitrification at

mg/l, while dioctadecyldimethyl ammonium chloride (C18DMAC)nhibited nitrification at 16 mg/l in the presence of 20 mg/l of LAS58]. Recently, the influence of benzalkonium chloride was inves-igated by Yang, who stated that BAC was inhibitory to a mixeditrifying culture at 10–15 mg/l [59]. The same trend was observeduring a batch assay with poultry-processing wastewater [60].

eries containing BAC at 10 and 15 mg/l reached only 43 and8% ammonia removal efficiency, while at concentrations above5 mg/l, nitrification was complete inhibited. Measurements of BAC

n these samples revealed 90% removal.

Materials 280 (2014) 797–815 801

The influence of quaternary ammonium salts on denitrifica-tion also depends on their concentration. Hajaya et al. observedcomplete nitrate reduction and transient accumulation of nitritewith increasing BAC concentration over a range of 10–100 mg/l,suggesting the inhibition of the nitrite reduction step [60,61]. More-over, BAC was not degraded under these conditions. The ranges ofBAC concentration causing inhibition were also determined, buttheir values varied strongly. In the first study of Hajaya et al., itwas reported that this concentration was 50 mg/l and above [61],whereas in the next study, inhibition took place at a concentrationof merely 15 mg/l [60]. This divergence can result from differencesin the preparation of the microbial community and the VSS valuein bioreactors.

During wastewater treatment, primary sludge and excess acti-vated sludge are created. QACs have high affinity for adsorptionon this sludge, which is then converted in the methane fermenta-tion process. This fact raises two questions: whether QACs can bedegraded under anaerobic conditions and how these compoundsaffect biogas production. Tezel et al. studied the biodegradation ofVigilquat, a commercial sanitiser, and four quaternary ammoniumcompounds (R1R2N+(CH3)2Cl− where R1 and R2 are octyl, benzyl,or decyl substituents), which are components of Vigilquat, underanaerobic conditions using methanogenic culture [2]. They con-cluded that none of the QACs tested in the study was biodegradedunder methanogenic conditions, which is consistent with theresults obtained previously by Garcia et al. [62,63]. Moreover, Tezelet al. assessed any short- and long-term inhibitory effects on themixed methanogenic culture of all QACs tested in their study at andabove 25 mg/l, reporting that methanogenesis was more sensitiveto QAC inhibition than acidogenesis [2]. The inhibition depended onthe structure of the quaternary ammonium salt, decreasing accord-ing to the series dioctyl > octyldecyl > alkylbenzyl > didecyl; thus,the shorter the alkyl chain length, the more inhibitory the com-pound was. The inhibitory effect was inversely proportional to theQAC adsorption affinity towards the biomass [2].

The high antimicrobial activity of quaternary alkylammoniumsalts has a principal factor affecting the degradation in WWTP. Theresearch conducted shows that QACs can interrupt each of the pro-cesses in the wastewater treatment. However, it is important tonote, that usually QACs are inhibitory toward the activated sludgemicrobial community at concentrations higher than that found inthe wastewater. Nevertheless, sudden discharges of QACs result-ing in temporarily high levels in treatment plants could upset plantfunction [60].

2.3. Biodegradation mechanism

It is believed that microorganisms metabolise quaternaryammonium compounds under aerobic conditions according tothree strategies. In the first, hydroxylation of the alkyl chain atthe C-terminal takes place, followed by oxidation to the aldehydegroup and then the acid group. Subsequently, the compounds areprocessed by a �-oxidation-generating acetyl-CoA. This strategywas proposed by Dean-Raymond and Aleksander in a study ofthe decyltrimethyl ammonium salt biodegradation carried out byXantomonas [43]. Evidence of this hypothesis was the presence of 9-carboxynonyltrimethylammonium and 7-carboxyheptyltrimethylammonium salts extracted from suspension after the process.

The second mechanism, proposed by van Ginkel et al., assumes�-hydroxylation of the alkyl moiety, followed by a centralfission of the Calkyl N bond [46,47]. They believed that thehexadecyltrimethylammonium chloride (C16TMAC) degradation

carried out by Pseudomonas began with N-dealkylation catal-ysed by an oxygen/NADH-dependent monooxygenase and yieldedtrimethylamine. The first intermediate in the biodegradationpathway of C16TMAC was hexadecanol, which was oxidised to

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exadecanoic acid by an alkanol dehydrogenase. The acid wasurther metabolised through �-oxidation. The degradation ofrimethylamine depended on the microorganism type. The strainsed in the study mentioned above did not degrade trimethy-

amine, while Pseudomonas sp. 3A2 may conduct N-oxygenationollowed by cleavage to yield methanol and dimethylamine [64].f the bacteria do not completely break down trimethylamine, the

ineralisation requires the presence of different type of microor-anisms, such as methylotrophic microorganisms [46,47]. In someethylotrophs, the pathway involved direct cleavage of the C N

ond by a dehydrogenase [64,65]. The obtained dimethylamine ishen demethylated via methylamine to ammonia [40,46,66,67]. Theiotransformation of alkyldimethylbenzylammonium salt (BAC)y Aeromonas hydrophila sp. K suggested that the Calkyl N fis-ion of alkyl compounds by microorganisms is a general strategyor the biodegradation of alkylammonium salts [46]. The degra-ation of C12BAC and C14BAC begins with the N-dealkylationtep and results in the formation of dimethylbenzylamine. Thisntermediate is then converted to ammonia through two demeth-lation reactions followed by deamination with the formation ofenzaldehyde. Benzaldehyde was rapidly converted into benzoiccid, which was further degraded [44]. This scheme is confirmedy HPLC and GC-MS analyses, which show the accumulation ofimethylbenzylamine, methylbenzylamine, benzylamine, benzal-ehyde, and benzoic acid during biotransformation. Moreover,eromonas hydrophila sp. K was able to utilise this compound as

ts sole source of carbon and energy and was unable to grow onrimethylamine, dimethylamine, and methylamine, which addi-ionally suggested that BAC first undergoes demethylation but notleavage of the Cbenzyl N bond [44]. This mechanism was also con-rmed during studies of BAC biodegradation in poultry wastewaterarried out by mixing culture from the aerobic reactor of BNRystem [60]. Benzyldimethylamine, benzylmethylamine and ben-ylamine were found, which are intermediate compounds of BACiodegradation. A different mechanism for the aerobic biodegra-ation of C14BAC by an enriched microbial community growingn BAC was proposed by Tezel et al. [68]. They suggested that14BAC also underwent dealkylation but that the next steps wereebenzylation followed by N-demethylation. The Pseudomonas spp.bserved in the enriched culture were able to catalyse the conver-ion of C14BAC to benzyldimethylamine. The biotransformation ofhis intermediate compound proceeded with a considerable timeag that suggested that it was achieved by a different group of

icroorganisms.The third pathway of QAC biodegradation involved hydroxyl-

tion of the methyl C, followed by demethylation. This schemeas proposed for the degradation of dodecyltrimethylammonium

hloride (C10TMAC) by Pseudomonas sp. strain 7-6 isolated from wastewater treatment plant [41]. In addition to the cleavagef the Calkyl N bond (main pathway), Pseudomonas sp. strain 7-6an cleave the Cmethyl N bond, producing methanol and dode-yldimethylamine.

A general biodegradation mechanism for the ester quatiodegradation includes the primarily biologically mediatedydrolysis of the ester bonds, yielding fatty acids and a polyalcoholuaternary ammonium salt, which are subsequently mineralised49]. A degradation pathway of ester quats was proposed basedn research with consortia of microorganisms and 14C-methyl-abelled DEEDMAC under aerobic conditions [48]. The solid-phasextraction of quaternary ammonium salts, followed by thin-layerhromatography with radiochemical detection, showed that theoss of DEEDMAC was followed by the appearance of tallow

atty acid (mono-)ester of di-2-hydroxyethyldimethylammoniumhloride. This compound was short-lived and rapidly catabolised48,49]. This degradation pathway was confirmed during theecomposition of C14HEQ labelled at three different positions

Materials 280 (2014) 797–815

[69]. The rate of HEQ disappearance varied with the positionof the radiolabel. HEQ labelled in the fatty acid moiety wasrapidly degraded without a detectable lag period. The mineralisa-tion of tetradecylmethyl- and tetradecyldihydroxypropyl-labelledHEQ was preceded by a lag period, followed by exten-sive degradation. The mineralisation of tetradecylmethyl- andtetradecyldihydroxypropyl-labelled HEQ following that of theC14-fatty-acid-labelled HEQ suggests the removal of fatty acidmoieties prior to the degradation of the quaternary ammoniumcompound. The hydrolysis of HEQ results in the formation of2,3-dihydroxypropyltrimethylammonium salts. This salt was ulti-mately biodegraded by a Pseudomonas putida strain, serving as agrowth substrate, and surplus nitrogen was excreted as ammoniumby the isolate [49,70].

The biodegradation of quaternary ammonium compounds is acomplex process where the hydroxylation of the alkyl moiety is acrucial step. In the case of ester quats biologically facilitated hydrol-ysis commences the consequent steps of the degradation.

2.4. QAC biodegradation kinetics

When dealing with the question of the biodegradability of qua-ternary ammonium salts, it is necessary to take into account thekinetics of this process and the parameters that affect it.

Various models have been used to describe the kinetics ofbiodegradation. Games and King investigated the decompositionof octadecyltrimethylammonium chloride (C18TMAC) using twotests: semicontinuous activated sludge (SCAS) and carbon diox-ide evolution (CO2) [71]. In SCAS studies, activated sludge and inthe CO2 studies, influent of wastewater was used as the inoculum.The obtained data were analysed by nonlinear regression mod-els to estimate the rate constants for and the extent of ultimatebiodegradation. In the CO2 evolution test C18TMAC was toxic tothe microorganism at a concentration of 20 mg/l, so the anionicsurfactant LAS was added to mitigate toxicity and allow biodegra-dation to occur [71]. Biodegradation of the mixture started after a2–3 day lag period, which indicated that the number of microor-ganisms was initially the rate-limiting factor. The process thenfollowed first-order kinetics, and its rate was proportional to sur-factant concentration. Over 80% CO2 was evolved, and the rateconstants were somewhat higher than the constant for LAS degra-dation alone. This result indicated that C18TMAC is degraded inthe presence of anionic surfactant when microbial toxicity is mit-igated. Studies with LAS were also conducted in the SCAS testwith a biomass level of 1 g/l and radiolabelled C18TMAC at concen-trations of 0.1 and 1 mg/l. In this system, biodegradation startedwithout a lag phase and achieved a level of 63–89% (Table 1).Moreover, most of the radioactivity remaining in the system waspresumably incorporated into biomass, and this amount was higherfor alkyl-labelled than for methyl-labelled C18TMAC. The rateof C18TMAC-LAS complex biodegradation was similar to that ofC18TMAC alone, confirming that the enhanced degradation of theC18TMAC-LAS complex in the CO2 evolution studies was due to areduction of the bacteriostatic properties [71].

A another kinetic model were proposed by Qin et al., whostudied the primary aerobic biodegradation of several cationic sur-factants using the shaking-flask method [72,73]. They obtainedsigmoidal curves described by the Boltzmann model. The follow-ing parameters were assessed: degradation extent A2 (%), i.e., thevalue at which the degradation curves stabilise, and the disappear-ance times DT-50 and DT-90, which refer to the time when 50 and

90% of the surfactants disappear, respectively. The values of theseparameters were as follows: A2 over 97%, DT-50 ranging from 8.6to 28 h and DT-90 ranging from 13 to 36 h, indicating a quick andvast primary degradation [72].

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Zhang et al. developed a comprehensive dynamic model tolucidate the effect of benzalkonium chloride (BAC) on glucosetilisation and the biodegradation of BAC in an aerobic, mixedeterotrophic culture. In this model, glucose consumption andn increase in biomass were described with Monod kinetics withompetitive inhibition [74]. The half-saturation inhibition con-tant (KI) ranged between 0.12 and 3.60 mg/L depending on theAC-to-biomass ratio. The highest KI values were recorded atnd below 10 mg BAC/g VSS, at which BAC was almost totallydsorbed onto the biomass and did not exhibit an inhibitoryffect toward activated sludge. In these studies, the surfactantas degraded completely. BAC degradation was modelled using

wo-phase biodegradation kinetics. This model involves the rapiddsorption of BAC to biomass and its consecutive degradation inoth aqueous and solid phases in the presence of the same enzymes.he aqueous-phase BAC degradation rate was an average of 20imes higher than the solid-phase degradation rate [74].

Recently, Hajaya and Pavlostathis developed sub-models forrocesses under various conditions (fermentation, anoxic anderobic conditions) in a BNR system treating poultry-processingastewater [75]. Such processes as the hydrolysis of particulate

rganic matter, fermentation, and ammonification taking placen the fermentation reactor were described assuming first-orderinetics and no inhibition. Monod kinetics was used to describehe processes in both bioreactors: anoxic (denitrification, anoxic

icrobial growth and utilisation of readily degradable organicubstrate) and aerobic (nitrification, utilisation of readily degrad-ble organics linked to heterotrophic microbial growth, decay ofitrifiers and heterotrophs). The inhibitory effect of BAC on deni-rification was described by the competitive inhibition model. Theotal, liquid-phase and solid-associated BAC concentrations wereonsidered, but the best fit was obtained with the liquid-phase BAConcentration. However, it is worth mentioning that the adsorp-ion behaviour of BAC determined the extent of the BAC inhibitionf denitrification. Increasing the BAC adsorption affinity to solidsesulted in a lower liquid-phase BAC concentration and denitri-cation inhibitory effect. The estimated competitive inhibitionoefficients for the denitrification process were, respectively, 0.27nd 0.19 mg BAC/l for nitrate and nitrite reduction for the assayonducted before BAC exposure and 0.29 and 0.21 mg BAC/l for thessay conducted during BAC exposure. These parameters indicatedhat acclimation of the microbial consortia to BAC occurred andhat the nitrite reduction was more susceptible to BAC than nitrateeduction was [75].

The biodegradation of BAC and its influence on the nitrificationrocess was estimated based on the data obtained from the threeatch aerobic assays. BAC biodegradation follows mixed-substrateonod kinetics, where BAC degradation competed with the readily

egradable organic substrate. The BAC inhibition of nitrificationas described by a non-competitive model, whereas the BAC inhi-

ition of the heterotrophic readily degradable organics utilisationas modelled as a competitive one [75]. The inhibitory effect ofAC on nitrification was evaluated using the autotrophic biomass-ssociated BAC concentration as the inhibitor. The autotrophicitrifying microbial population is incapable of BAC biodegrada-ion; therefore, the BAC fraction associated with the autotrophiciomass was persistent and more available to inhibit the nitrifiers.he values for ammonia and nitrite oxidation differed when theatch assay was performed before, during, and after BAC exposure.he estimated BAC half-saturation inhibition constant values formmonia and nitrite oxidation were, respectively, 0.11 and 0.20 mgAC/l before BAC exposure, 5.41 and 4.14 mg BAC/l during BAC

xposure, and 0.55 and 3.64 mg BAC/l after BAC exposure had beenerminated for over 100 days. The aforementioned values show thathe nitrifiers’ resistance to BAC is dynamic and depends on the dura-ion of the exposure to BAC. The dynamic change in BAC resistance

Materials 280 (2014) 797–815 803

can be modelled with increasing values of the inhibition coefficientfor ammonia and nitrite oxidation over time [75].

The kinetic parameters and coefficients obtained in the batchassays described above were used in a comprehensive, dynamicmodel simulating the fate of BAC and its effect on the overallcontinuous BNR system performance. The model simulated wellthe long-term performance of the BNR system treating poultry-processing wastewater, including enhanced BAC degradation byheterotrophs and increased resistance of nitrifiers to BACs [75].

The kinetics of biodegradation is of fundamental meaning tothe environment. Many models have been described to estimatethe rate constants and the extent of ultimate biodegradation.The most important factors that influence kinetic models are thebiocidal activity of QACs, structure of alkylammonium surfac-tants, adsorption–desorption phenomena of QACs on sludge andbiosolids and the presence of anionic compounds which can miti-gate the biocidal activity of cationics

2.5. Influence of QAC structure on its biodegradation kinetics

The biodegradation of surfactants is a multi-step process catal-ysed by microorganisms. The microbial attack requires recognitionof the compound, induction enzymes, and substrate-enzyme bind-ing and, to some degree, depends on the structure of the compound[76]. The structure of surfactants and their physicochemical prop-erties can thus play an essential role in the biodegradation ofthese compounds in the environment. The length, number, andtype of substituents in quaternary ammonium salt are of primeimportance. The increase in the alkyl chain length results in adecrease in the surfactant biodegradability (Table 1). Nishiyamaet al. concluded that, after 28 days, biodegradation as determinedbased on biochemical oxygen consumption decreased from 46.9to 7.2% when the alkyl substituents were changed from octyl tooctadecyl [67]. Those results were confirmed by Yamane et al.,who stated that the ultimate biodegradation of octadecyl- and ico-syltrimethylammonium bromide was 40 and 14%, respectively, andultimate biodegradation was not observed for docosyl- and tetra-cosyltrimethylammonium bromide (Table 1) [52]. The increasein the alkyl chain length also decreased the biodegradation rate[77]. This trend has been connected to differences in solubility.The longer the alkyl chain length, the lower the solubility of thecationic surfactant, such that the surfactant was less bioavailablefor biodegradation [77]. Moreover, low biodegradability may beattributed to the antimicrobial activity of these surfactants, whichwas enhanced by extending the alkyl chain length [67,78].

The rate of quaternary ammonium salt biodegradation isaffected by the number of alkyl substituents. van Ginkel and Kol-venbach stated that under aerobic conditions, the biodegradabilityof QACs decreases as the number of non-methyl alkyl groupsincreases (i.e., R4N+ < R3MeN+ < R2Me2 N+ < RMe3N+ < Me4N+) [76].Additionally, the substitution of a methyl group in a quaternaryammonium salt by a benzyl group decreases biodegradability[76,77]. This was confirmed by Tezel et al., who proved that therate of C14TMAC transformation was five times higher than that ofthe C14BAC transformation [68].

2.6. Influence of QAC adsorption on its biodegradation

The adsorption–desorption phenomena of QACs on sludge andbiosolids are very important from an environmental point of viewbecause sorption can affect the toxicity, bioavailability, biodegra-dation, bioaccumulation, and the overall fate of QACs in the

environment. In WWTP, QACs exhibit strong adsorption on pri-mary sludge and activated sludge and can have negative effects onanaerobic digestion. Furthermore, the land application of biosolidscontaining QAC may result in the accumulation of these pollutants

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n soil. The desorption of these compounds can eventually lead tohe contamination of water resources through leaching and runoff78–80].

The adsorption of QACs onto sludge is an equilibrium process.n SCAS tests performed by Games and King with 3 g/l of acti-ated sludge and 20 mg/l of C18DMAC, up to 98% of the surfactantas adsorbed on activated sludge, and equilibrium was reachedithin 30 min [71]. Kinetic studies indicated that biodegradation

ccurred both in solution and on sludge solids. The biodegrada-ion of adsorbed C18TMAC exhibited an exponential decay with arst-order rate constant of 0.28/h [71].

The adsorption of QACs onto sludge has a biphasic character: annitial fast adsorption and then a slow phase. This has been con-rmed in a kinetic assay performed by Zhang et al. to evaluate theynamics of BAC partitioning in the activated sludge [74]. They usedhe Freundlich isotherm to model the equilibrium. The estimatedalues for KF (capacity factor/sorption affinity) and n (Freundlichxponent) were 42.1 (mg/g VSS) (L/mg)n and 0.25, respectively,uggesting rapid and extensive BAC adsorption. The adsorptionrocess is dependent on temperature and decreases with increas-

ng temperature [81]. Moreover, adsorption onto sludge improvesith increasing alkyl chain length in cationic surfactants [82].

The mechanism of quaternary ammonium salt sorption oniosolids is complex, and both hydrophobic and ionic interactionsre most likely in effect. Cationic surfactants having a posi-ive charge have a strong affinity for the surface of particulatesn sewage sludge, which are predominantly negatively charged83]. On the other hand, the affinity to sorption depends on theAC structure. QACs with a longer alkyl chain adsorb more thanACs with a shorter one. The benzyl group further enhances thedsorption of QACs, but this effect diminishes as the alkyl chainength increases [79]. This was confirmed by the behaviour ofour quaternary ammonium compounds: dodecyltrimethylammo-ium chloride (C12TMAC), hexadecyltrimethylammonium chlorideC16TMAC), dodecylbenzyldimethylammonium chloride (C12BAC),nd hexadecylbenzyldimethylammonium chloride (C16BAC). Thedsorption of these QACs onto municipal primary sludge was asollows: C12TMAC, 13; C16TMAC, 88; C12BAC, 67; and C16BAC, 89%79]. These observations are in agreement with those reported byarcia et al. [82] and suggest a hydrophobic sorption mechanism

84].Sludge-sorbed QACs desorbed to various degrees, and the

xtent of desorption was inversely proportional to the extent ofdsorption. After 10 days, 35% of adsorbed C12TMAC underwentesorption compared to only 5% for C16BAC [79].

The adsorption of a surfactant is also affected by its concen-ration. Ren et al. have observed that the adsorption capacity ofctivated sludge increased from 17.61 to 148.5 mg/g as the initialetradecylbenzyldimethylammonium salt (C14BAC) concentrationncreased from 5 to 50 mg/l [85] This result may be related to theriving force, which generally changes with the adsorbate concen-ration in the bulk solution. The higher the adsorbate concentration,he higher the adsorption capacity.

In binary QAC mixtures, QACs with relatively high adsorptionffinities, such as C16BAC, decreased the adsorption of QACs with

low adsorption affinity, such as C12TMAC. On the other hand, theresence of C12TMAC did not have a significant effect on the adsorp-ion of C16BAC regardless of the initial C12TMAC concentration [79].

.7. Influence of anions on the biodegradation of QACs

The presence of different inorganic and organic anions has

n effect on the amount of quaternary ammonium salts andheir biodegradability in the aquatic environment [86,87]. Theydrophobic ion pairs formed by the combination of QAC withnionic compounds exhibit different physical–chemical properties

Materials 280 (2014) 797–815

than the individual compounds, e.g., masked bipolar surfactantcharacter, lower water solubility, modified bacterial toxicity, andincreased tendency for sorption. Biodegradability tests [88,89] haveshown that some surfactants that are normally easily degradable(e.g., LAS, SDS) became less biodegradable in the presence of QACssuch as benzalkonium chloride (BAC), alkyltrimethylammoniumchloride (ATMAC), and dialkyldimethylammonium chloride (DAD-MAC). The stability of the ion pairs may be affected by the polarityof the environment. In environments less polar than water, suchas sewage sludge and sediments, the formation of less polar ionpairs should be favoured, as the ion pair is much less polar than thefree ions [87]. This could explain the strong adsorption of QACs tonegatively charged sewage sludge. On the one hand, the competi-tion of these sorption processes with ion pair formation has to betaken into account. On the other hand, the formation of ionic pairsmay lead to increased “dissolution” of the less polar ionic pairs inthese matrices. The significance of each of these processes will varywith the polarity of the environment and the nature of the sorbingsurface [87].

2.8. Influence of QAC concentration and microbial adaptation onQAC biodegradation

QACs used as disinfectants have low half-maximal effectiveconcentrations (EC50), which indicates a high toxicity. Toxicity inlow-biomass systems causes the biodegradability to depend on theinitial concentration of the surfactant [90]. The growth of bacteria ismore rapid under lower initial QAC concentrations, and an increasein the dose leads to an inhibitory effect [91]. This inhibition makesit harder to distinguish between true non-biodegradability and theinhibition of biodegradability due to the toxic effect of the QACs[92]. The adaptation of aquatic microbial communities to QACs canbe separated into fate and effect components. In fate adaptationprocesses, microorganisms are pre-exposed to the compound, sig-nificantly increasing biodegradation. Such adaptation allows forthe rapid removal of QACs from the environment and minimisesthe potential for the exposure of sensitive aquatic biota to thesechemicals. A second adaptation process resulting in the selection ofmore tolerant microbial populations may also be important, espe-cially taking into account the antimicrobial properties of QACs [93].Research has shown that both types of adaptation may be impor-tant when quaternary ammonium salts are concerned.

Ventullo and Larson, based on short-term acute studies, haveobserved for dodecyltrimethylammonium chloride (C12TMAC) arelatively low (0.1 mg/l) first effect concentration (FEC) [93]. How-ever, the chronic exposure of microbial communities to C10TMACdid not cause toxic effects at concentrations two orders of magni-tude higher than its acute FEC, which suggests a significant adaptiveresponse with respect to the development of biodegradation capa-bility. The maximum degradation rate and number of C10TMACdegraders increased by 1–5 orders of magnitude relative to unex-posed controls, even at initial C10TMAC concentrations as low as1 �g/l. Ventullo and Larson suggested that the increase in themaximum degradation rate was a result of increases in both thenumber of degraders and the activity per cell at high concentra-tions while the increased number of C10TMAC degraders in thecommunity at low concentrations [93]. The acclimation of purecultures and microbiological consortia to quaternary ammoniumsalts was also observed by Patrauchan and Oriel, who stated thatAeromonas hydrophila sp. degraded benzalkonium chloride twiceas fast after the acclimation, with a fourfold-shorter lag phase, and

the biodegradation range increased threefold [44]. Therefore, onecan say the adaptation is a strategy that induces QAC-degradingenzymes and allows for a faster removal of the toxic compoundfrom the surroundings.

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A change in microbiological community composition and anncrease in BAC removal ability was also reported after long-termxposure to the BAC mixture [68]. Assays at concentrations below0 and 250 �g/ml yielded 100 and 60% BAC degradation, respec-ively, and a lack of biodegradation was observed at 500 �g/mlAC.

A susceptibility test of enriched microbial culture against theAC mixture to determine the importance of action efflux pumps

n BAC removal was conducted in the presence and absence ofn efflux pump inhibitor, thioridazine [42]. The susceptibility ofhis community to BAC was not affected by the presence of thior-dazine, suggesting that mechanisms other than efflux pumpingontribute to the observed resistance against BACs. In this study,he main mechanism of communities’ resistance to BAC is believedo be BAC degradation. As biotransformation products of BAC wereignificantly less toxic than BAC themselves, biotransformation isffective in reducing the antimicrobial properties of BAC [68].

However, the acclimation process may have a negative aspect.he long-term exposure microbial community to subinhibitoryoncentrations may enhance bacterial resistance to clinically rel-vant antibiotics [94]. Tandukar et al. showed that the bacteria innrichment communities harbour a much higher number of copiesf multidrug resistance genes, which can lead to the evolution ofuperbugs [42]. Therefore, it is necessary to develop biological sys-ems to effectively degrade such agents to prevent the spread ofuperbugs.

. Biodegradation of gemini surfactants

As mentioned in the introduction, few papers investigate theiodegradability of gemini surfactants. Banno et al. have stud-

ed the biodegradation of conventional gemini cationic surfactantsnd surfactants with carbonate linkages introduced into theydrophobic moiety in the spacer or in both the hydrophobicnd spacer moieties [95,96]. They have proved that trimethylene-,3-bis-(N,N-dimethyl-N-dodecylammonium) diiodide and theomologous C10, C12, and C14 of pentamethylene-1,5-bis-(N,N-imethyl-N-alkylammonium) diiodide (Table 2, compounds 1 and, respectively) showed practically no biodegradation by acti-ated sludge (the maximum BOD-biodegradability was reached foromologue C10 and was only approximately 10%). The introductionf a carbonate linkage into the hydrophobic moiety of this typef gemini surfactant enhanced its biodegradability. However, theiodegradation of this surfactant was still low, being only approx-

mately 25% after 28 days of incubation (Table 2, compound 3, = Pr).

The biodegradability of the primary biodegradation interme-iates, 1-dodecanol and quaternary ammonium alcohol (Table 2,ompounds 4 and 5, respectively), was approximately 75 and 10%,espectively. Based on these results, one can state that the lowiodegradability of the studied gemini surfactant may be due tohe low biodegradability of the intermediate having two ammo-ium groups [96]. The introduction of a carbonate linkage into thepacer between the two single-type cations (Table 2, compound 6)r in both the hydrophobic and spacer moieties (Table 2, compound) significantly improved the biodegradability of those surfactants.he maximum BOD-biodegradability of homolog C12 exceeded 70%fter a 28-day incubation [95,96]. High biodegradation (above 60%)as also been observed for two alcohols (Table 2, compounds 8 and, respectively), which may be primary degradation products of

he studied surfactants with the carbonate linkage into the spacer.ased on these observations, it was concluded that the gemini-ype cationic surfactants containing a carbonate linkage maye enzymatically hydrolysed by environmental microbes at the

Materials 280 (2014) 797–815 805

carbonate with the evolution of carbon dioxide and forming easilybiodegradable quaternary ammonium alcohols [95].

Significant differences in the biodegradation of the compoundswith carbonate linkages introduced in both the hydrophobic andlinker moieties or only into the hydrophobic moiety (70% vs. 25%)seem to be strongly related to the hydrolytic degradation. The car-bonate linkage in the linker moiety was gradually hydrolysed inwater, and only 18% remained after 9 h of reaction, while 97% ofthe carbonate linkage in the hydrophobic moiety remained afterthe same period. These results indicated that the carbonate linkagein the hydrophobic moiety was more stable against hydrolysis thanthe carbonate linkage in the linker moiety [96].

The biodegradability of gemini-type cations containing carbon-ate linkages was also influenced by the amount of the methylenegroup in the spacer structure. A comparison the biodegradabilityof surfactants with even and odd numbers of methylene groupsin the spacer (Table 2, compounds 6 and 7) showed much higherbiodegradation for the surfactant with two methylene groups. Tak-ing into account that both intermediates (quaternary ammoniumalcohols) are biodegradable, these results may be due to the cleav-ability at the carbonate linkage of the spacer moiety. This has beenconfirmed in hydrolysis studies of those surfactants (Table 2, com-pound 6, n = 12, m = 2 and 3) without activated sludge. It was foundthat the carbonate linkage in the spacer moiety of surfactants withtwo methylene groups was hydrolytically less stable than the car-bonate linkage in the spacer moiety with three methylene groups.After an 8-day incubation, 83% of the carbonate linkage of theformer surfactant was hydrolysed compared to only 18% of thatof the latter. Based on these results, the carbonate linkage of com-pounds with an even number of methylene groups in the spacercould be enzymatically and non-enzymatically cleaved; therefore,its BOD-biodegradability was higher than that of compounds withan odd number of methylene groups in the spacer moiety.

A group of cationic surfactants finding an ever-wider range ofapplications is surfactants containing ester groups in the hydropho-bic moiety [97].

Tatsumi et al. investigated the biodegradation 1,3-bis[(acyloxyalkyl)-dimethylammonio]-2-hydroxypropane dichloride[98]. The biodegradability of homologs with decanoyloxyethyl,dodecanoyloxyethyl, and tetradecanoyloxyethyl substituents after14 d was in the range of 50 to 59% (Table 2, compound 10, m = 2,n = 10, 12, 14, respectively). Moreover, biodegradability graduallydecreased with as the number of methylene groups between theoxycarbonyl group and the ammonium group increased whenthese surfactants have the same number of carbon atoms in thelipophilic part [98].

Another group of gemini ester quats was bis(ester-ammonium)dichlorides having butane, t-butene, c-butene, and butyne as aspacer (Table 2, compound 11). Most of the studied compoundsshowed biodegradability similar to the surfactants mentionedabove with a 2-hydroxypropane spacer. Only the biodegradation oftrans-1,4-bis[6-(octanoyloxy)hexyldimethyl ammonio]-2-butenedichloride (Table 2, compound 11, n = 8, m = 6) was lower (40%),showing that the biodegradability decreased with increasing dis-tance between the oxycarbonyl group and the hydrophilic groupwhen these surfactants possess the same number of carbon atomsin the lipophilic part. This result is similar to that in previous work[98,99].

Cationic surfactants with ester bonds have also been stud-ied by Tehrani-Bagha et al. [97,100]. They have prepared decyland dodecyl homologs of gemini ester quats and betaine esters(Table 2, compound 12 and 13, respectively) with different num-

bers of methylene groups in the spacer. Moreover, they synthesisedcorresponding monomeric compounds. The authors stated thatthe monomeric surfactants were rapidly degraded (above 80%at day 28), while the gemini surfactants were more resistant

806 B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815

Table 2Biodegradability of gemini surfactants and their intermediate products of biodegradation.

Compound Chemical structure Biodegradation Reference

(%) Method

1

NH3C

CH3

C12H25

(CH2)3

NH3C C12H25

CH3

2I-2 BODa [96]

2

NH3C

CH3

CnH2n+1(CH2)5

NH3C CnH2n+1

CH3

2I-

n = 10, 12, 14

≤ 10 BODa [95]

3

H3C N

CH3

(CH2)3

X

NH3C

CH3

O C

O

O C12H25

X O C

O

O C12H25

X = -CH2CH2CH2- (Pr), -CH(CH3)CH2- ( iPr)

2I-

25–30depending on X groupstructure

BODa [96]

4 C12H25OH 75 BODa [96]

5

H3C N

CH3

(CH2)3

(CH2)3

NH3C

CH3

OH

(CH2)3 OH10 BODa [96]

6

H3C N

CH3

(CH2)m

CnH2n+1

O

C O

O

(CH2)m

N CnH2n+1H3C

CH3

2I-

m = 2, 3n = 10, 12,14

60–70 (m = 2)depending on n value

20–45(m = 3)depending on n value

BODa [95]

7

H3C N

CH3

(CH2)m

(CH2)3

O

C O

O

(CH2)m

N (CH2)3H3C

CH3

2I-

O C

O

O C12H25

O C

O

O C12H25

m = 2, 3

depending on m value70 (m = 2)30 (m = 3)

BODa [96]

B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815 807

Table 2 (Continued)

Compound Chemical structure Biodegradation Reference

(%) Method

8

H3C N

CH3

(CH2)2

C12H25

OH

I-

60 BODa [95]

9

H3C N

CH3

(CH2)3

C12H25

OH

I-

70 BODa [95]

10

Cn-1H2n-1

C O

O

(CH2)m

NH3C

CH3

2Cl-

N

OH CH3

CH3

Cn-1H2n-1

C O

O

(CH2)m

n = 8, 10, 12, 14m = 2,4,6

42–59depending on m value

BODa [98]

11

Cn-1H2n-1

C O

O

(CH2)m

NH3C

CH3

2Cl-

N

CH3

CH3

Cn-1H2n-1

C O

O

(CH2)m

X

n = 8, 12m = 2, 6

X = t-butene , c-butene, butyne, butane

40–58depending on m value

BODa [99]

12

CnH2n-1

C O

O

(CH2)2

NH3C

CH3

2Br-

N

CH3

CH3

CnH2n-1

C O

O

(CH2)2

(CH2)m

n = 10, 12m = 3, 6

40–54depending on n and mvalues

BODa [97,100]

13

C12H25

C O

CH2

NH3C

CH3

2Br-

N

CH3

CH3

C12H25

C O

CH2

(CH2)2

OO

52 BODa [97]

14

OH

(CH2)2

NH3C

CH3

2Br-

N

CH3

CH3

OH

(CH2)2

(CH2)315 BODa [97]

808 B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815

Table 2 (Continued)

Compound Chemical structure Biodegradation Reference

(%) Method

15

C O

CH2

NH3C

CH3

2Br-

N

CH3

CH3

C O

CH2

(CH2)2

OHOH

12 BODa [97]

16

HC

(H2C)3

C

HN

CH2N

HN (CH2)n

. ..NH2

.

HN C CH

(CH2)3

NH

Cl-+C

H2N NH2..

Cl-+

..

Cn(LA)2 when x=10 and n(2, 3,4, 6, 9, 10)Cn(CA)2 when x=8 and n(2, 3,4, 6, 9, 10)

HN

Cx(H2C)

CH3

O

NHC

(CH2)x

H3C

O

O O

49–90 depending onthe x and n values

DOCb [103]

17

NH3+ Cl-

HN C11H23

O

O

NH

NH

+H3N

O

NH

Cl- ( )6

C11H23

O

C6(LK)2

61 CO2 headspacetest

[106]

18

NH

O

NH

NH

HN

O

NH3+ Cl-

( )6

OC11H23

OC11H23

NH3+ Cl-

C6(LL)2

65 CO2 headspacetest

[106]

19

N+

HN C11H23

O

O

NH

NH

N+O

NH

Cl- ( )6

C11H23

O

H3CH3C CH3

CH3H3C

CH3Cl-

C6(LK)2TM

42 CO2 headspacetest

[106]

20

NH3+ Cl-

HN C11H23

O

NH

NH

+H3N

O

NH

Cl- ( )3

C11H23

O

NH

( )4

O

Cl-

C7NH(LK)2

70 CO2 headspacetest

[106]

B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815 809

Table 2 (Continued)

Compound Chemical structure Biodegradation Reference

(%) Method

21

HON N

OH

OH

OH

OH

OH OH

OH

OH

OH

R R

R' R's

2I-

s = 4, 6

R = C8H17, C10H21, C12H25R ' = C2H5, C3H7, C12H25

20–33depending on s, R, R′

DOCb [108]

22 HON N

OH

OH

OH

OH

OH OH

OH

OH

OH

H H

H H4

2Cl-

14 DOCb [108]

23 HON N

OH

OH

OH

OH

OH OH

OH

OH

OH

R R

H H6

2 CH3COO-

R = C12H25

62 DOCb [108]

24HO

N NOH

OH

OH

OH

OH OH

OH

OH

OH

R R

4

R = C12H25

89.6 DOCb [108]

25

N (CH2)3R NH

N (CH2)3R NH

R = C8H17, C12H25

C OH

OOH OH

OH OH

C OH

OOH OH

OH OH

CH2

CH2 36–42depending on R group

BODa [109]

26

N (CH2)3R NH

N (CH2)3R NH

R = C12H25

COH

O

OH

OH

OH

OH

OH

COH

O

OH

OH

OH

OH

OH

CH2

CH216 BODa [109]

810 B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815

Table 2 (Continued)

Compound Chemical structure Biodegradation Reference

(%) Method

27

HN (CH2)3R NH

N (CH2)3R NH

X

C OH

O

OH

OH

O

OH

OOH

HOHO

HO

X

R = C8H17, C12H25

X =

CH2

CH2

46–55depending on R group

BODa [109]

28

NOH

CO

H2n+1Cn

NH

HN

CO

NH2n+1CnOH

OH

OH

OH

OH

OH

OH

OH

OH

n = 4, 6, 8, 10, 12

48–55depending on n value

Closed bottletest

[110]

29

N

C12H25

HN

C

OH

HO

OH

OOH

O

O

OH

OH

OHOH

N

C12H25

HN

C

OH

HO

OH

OOH

O

O

OH

OH

OHOH

C

O

C

O

2C12 peLac

33 BODa [111]

30

C12H25

N

C

OH

HO

OH

O

OH

O

O

OH

OH

OHOH

N

C

OH

HO

OH

O

OH

O

O

OH

OH

OHOH

C12H25

2C12 Lac

31 BODa [111]

B. Brycki et al. / Journal of Hazardous Materials 280 (2014) 797–815 811

Table 2 (Continued)

Compound Chemical structure Biodegradation Reference

(%) Method

31

N

C12H25

N

C12H25

H3C

H3C

C O

HO OHHOH2CHO

OH

Br -

2C12 AmGlu

6 BODa [111]

32

NH

C12H25

HN

C

OH

HO

OH

O

OH

O

O

OH

OH

OHOH

C12 peLac

63 BODa [111]

33

N

COO

H

HOHN

O

( )n

( )n

n = 7, 9, 11

12–47depending on n value

BODa [112]

34

N H

HOHN

O

( )n

( )n

n = 7, 9, 11

COO

29–40depending on n value

BODa [112]

trhTbitae1aaer

a BOD = biochemical oxygen demand.b DOC = dissolved organic carbon.

o biodegradation. Dodecyl betainate and dodecyl ester quatsequired 42 days to reach >60% biodegradation, while the decylomologs of ester quats did not exceed 45%, even after 55 days.hus, the gemini surfactants that have been studied could note classified as readily biodegradable. The poor biodegradabil-

ty of those cationic ester gemini surfactants is most likely dueo the slow degradation of the dicationic species that are gener-ted together with the fatty acid after the hydrolysis of the twoster bonds, e.g., N,N′-bis(2-hydroxyethyl)-N,N,N′,N′-tetramethyl-,3-propanediammonium dibromide (Table 2, compound 14)

nd N,N′-bis(2-carboxymethyl)-N,N,N′,N′-tetramethyl-1,2-ethanemmonium dibromide (Table 2, compound 15), which are gen-rated from the ester quat gemini and the betainate gemini,espectively. These species, which were synthesised and tested for

biodegradation, degraded very slowly (less than 20% after 28 days),indicating that they are resistant to biodegradation [97,101]. It isprobable that the dicationic product of hydrolysis of the homologwith a six-carbon spacer also degrades slowly, as reflected in thelower value of the ultimate biodegradation of the correspondinggemini surfactant (40%) [100]. Tehrani-Bagha et al. also suggestedthat the low biodegradation percentages found in Tatsumi’s works[97–99] for gemini surfactants with octanoate chains (Table 2,compounds 10, 11) can be explained by assuming that dicationicsubstances with a high number of carbons between the ester bond

and the nitrogen (creating a large hydrophilic moiety) are non-biodegradable. However, additional biodegradability tests to fullyunderstand the biodegradation potential of those compounds arenecessary [97].

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12 B. Brycki et al. / Journal of Haza

One of the strategies to reduce the environmental impact ofurfactants is to build up gemini structures from environmentallyriendly single-chain amino acid surfactants. Gemini surfactantsave been developed and studied based on two different aminocids: arginine and lysine [51,102,103]. Perez et al. synthesisednd studied gemini cationic surfactants derived from argi-ine analogues: N�,N�-bis(N�-acylarginine)�,�-alkylendiamides,r bis(Args) (Table 2, compound 16) [103]. These compounds con-ist of two symmetrical long-chain N�-acyl-l-arginine residues of2 or 10 carbon atoms (the Cn(LA)2 and Cn(CA)2 series, respec-ively) linked by amide bonds to an �,�-alkylenediamine spacerhain of varying length (n = 2–10) [104]. The results of the ulti-ate biodegradation obtained for bis(Args) showed that except for

ne homolog, C9(CA)2 (49%), those surfactants can be classified aseadily biodegradable compounds. However, the experimental datandicate that in most cases, the biodegradation extent of bis(Args)

as lower than those of single-chain structures containing amideroups, such as lauroyl arginine methyl ester (90%) (Table 1). Thisas most likely due to the greater complexity and hydrophobic-

ty of the gemini surfactant in relation to its single counterparts.oreover, the biodegradation rate of bis(Args) decreased when

oth the spacer chain and the alkyl chain length increased. Hence,he higher the hydrophobicity of the surfactants, the lower theiriodegradation rate [103,104].

Recently, Colomer et al. reported the synthesis and biologicalroperties of cationic lysine derivatives [105,106]. They preparedour gemini surfactants in which the spacer chain and the num-er and type of cationic charges were regulated: (C6(LK)2), withwo positive charges on the �-amino groups of the lysine and a

ethylene-based spacer chain (Table 2, compound 17); (C6(LL)2),ith two positive charges on the �-amino groups of the lysine

nd a methylene-based spacer chain (Table 2, compound 18);C6(LK)2TM), with two positive charges on the two trimethylated-amino groups of the lysine and a methylene-based spacer chain

Table 2, compound 19); and (C7NH(LK)2), with a spermidine-basedpacer and two positive charges on the �-amino groups of the lysineut a third positive charge on the spacer chain (Table 2, compound0).

The ultimate biodegradation of those surfactants was evaluatedn the CO2 headspace test. The degradation started immediately,nd no induction period was detected. Except for C6(LK)2TM, theiodegradation of the gemini surfactants reached 60% in 20 days,hich classifies them as readily biodegradable. These results are

imilar to the findings for cationic surfactants from arginine aminocids. These good biodegradation levels could be due to the amideinkage between the polar head and the hydrophobic part of the

olecules as well as the low toxicity of the initial compounds andntermediates. Microorganisms usually break the amide linkageetween the alkyl chain and the lysine and then completely degrademino acids. The fatty acids are decomposed through fatty-acid-oxidation [106,107].

In the recent years, much interest has been dedicated tourfactants with biological motifs, such as peptide and carbohy-rates, belonging to the “green chemistry” area. Brycki and Szulcerformed biodegradability measurements for the selected com-ounds with sugar substituents: quaternised dimeric surfactants,rotonated dimeric surfactants, complexes of dimeric surfactantsith weak hydrogen bonds, and neutral dimeric surfactants [108].

his study showed that biodegradation depends on the chargef the nitrogen atoms. Dimeric quaternary alkyldeoxyglucitolmmonium iodides and a completely protonated compound,etramethylene-1,4-bis(N-deoxy-d-glucitolammonium) chloride

Table 2, compounds 21, 22, respectively), were relatively resistanto biodegradation, which did not exceed 35%. This is due to theositively charged nitrogen atoms and lack of easily hydrolysedroups in the structure of these compounds. The biodegradability

Materials 280 (2014) 797–815

of the compounds with weak hydrogen bonds (Table 2, compounds23) and neutral gemini surfactants (Table 2, compounds 24) wassignificant higher (62 and 90%, respectively). Hence, these dataindicate that the decrease in the nitrogen atom charge caused anincrease in biodegradability [108].

Surfactants with sugar substituents were also studied byWilk et al. [109]. They tested the biodegradability of nonionicaldonamide-type gemini surfactants with gluconyl, glucoheptonyl,and lactobionyl groups (Table 2, compounds 25, 26, 27, respec-tively). The measurement showed that after 28 days of testing,the surfactants were degraded by 16–55%; therefore, they couldnot be classified as readily biodegradable. However, in the pro-longed closed-bottle test, most of the studied compounds achievedapproximately 60% biodegradation, indicating slow but completemineralisation. Apart from the activated sludge, biodegradationwas carried out by environmental microorganisms from the soiland river water. The results obtained were similar to data fromtests in the presence of activated sludge [109].

The data in Table 2 indicate that the structure of aldonamide-type gemini surfactants influences the rate and range ofbiodegradation. The surfactants with gluconyl and lactobionyl sub-stituents were biodegraded more quickly and extensively than thesurfactants with a glucoheptonyl group. Moreover, variation in thealkyl chain length (C8 and C12) also changed the biodegradabil-ity of this class of surfactant. The compounds containing shorterhydrocarbon chains, i.e., n-octyl tails, are more slowly degradedthan those with n-dodecyl tails [109].

Another nonionic gemini surfactant with carbohydrate groups(Table 2, compound 28) has been studied by Laska et al. [110]. Dataobtained from the closed-bottle test showed that the surfactantwith an n-butyl substituent achieved the highest biodegradabil-ity, 55% on day 28. However, in contrast to the results from Wilk’swork [109], extension of the alkyl chain length slightly reduced thebiodegradability of the tested surfactants. Hence, these results donot allow these compounds to be classified as readily biodegrad-able. However, in the prolonged closed-bottle test, all surfactantsachieved more than 60% biodegradation and required 64–75 daysto degrade to 62–68% levels, indicating slow but complete miner-alisation [110].

Sugar-based nonionic gemini surfactants containing two pep-tide bonds and two amide bonds have also been studied byYoshimura et al. [111]. These researchers prepared the gemini sur-factants 2 C12peLac and 2 C12Lac and the heterogemini surfactant2 C12AmGlu with a sugar moiety and an ammonium headgroup(Table 2, compounds 29, 30, 31, respectively). Moreover, the corre-sponding monomeric surfactant C12peLac was synthesised (Table 2,compound 32).

The authors expected these surfactants to be environmen-tally acceptable. However, only the monomeric-type C12peLac wasrapidly biodegraded. The biodegradation of the gemini-type sur-factants was slight, 6-33%. These biodegradation values are muchlower than the results of Wilk [109] and Laska [110]. Yoshimuraet al. suggested that the introduction of the additional hydro-carbon chain to the monomeric surfactant and the creation of atertiary amine are responsible for these low biodegradation rates[111].

A series of amphoteric gemini surfactants (Table 2, compounds33, 34) have been obtained from 2[5H]-furanone and primary fattyamines by Gassama et al. [112]. The biodegradation was deter-mined by a method using a manometric respirometer to follow theconsumption of oxygen during 28 days in a closed flask containing30–60 mg l−1 of the test substance and inoculums from a sewage

plant. In all cases, degradation started immediately, and no induc-tion period was detected. The biodegradation rate was the highestfor compounds with a 7-methylene group (n) in each chain (47%).An increase in the methylene group number slows the process (12%

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B. Brycki et al. / Journal of Haza

or n = 11). Thus, according to the E.U. directive, those surfactantsere not readily biodegradable.

The biodegradation of gemini surfactants is similar to somextent to the biodegradation of monomeric QACs. However, thenfluence of structure of gemini surfactants, especially these con-aining amide or sugar derivatives, on kinetics and degree ofegradation, is much stronger than the corresponding monomericlkylammonium surfactants.

. Conclusions

Alkylammonium surfactants are the primary group of cationicurfactants. This group of compounds possesses not only very goodurface-active properties but also strong antimicrobial activity,ncluding that toward bacteria, fungi, algae, and viruses. Some yearsgo, a new type of alkylammonium surfactants were introduced:.e., dimeric surfactants. Dimeric surfactants are superior to the cor-esponding conventional surfactants in a number of aspects, suchs having a lower critical micelle concentration (cmc), a higherfficiency in reducing the oil/water interfacial tension, unusualggregation morphologies, and better wetting, solubilising, andoaming properties, which make them potentially useful in manypplications, such as detergents and cleaning agents, emulsionolymerisation, enhanced oil recovery, the construction of high-orosity materials, cosmetics and pharmaceutical and biologicalpplications. Dimeric alkylammonium salts also show excellentntimicrobial activity, which can be even up to three orders of mag-itude higher than the biocidal activity of monomeric salts. The

ncreasing use of alkylammonium surfactants, both monomeric andimeric, creates a serious environmental risk. Therefore, detailednowledge about the biodegradation of monomeric and especiallyimeric alkylammonium surfactants is necessary.

The effective degradation of alkylammonium surfactants inWPT can be accomplished by Gram-positive and Gram-negative

onsortia of microorganisms, which cooperate by chemical com-ensalism or synergistic relationships and the solid retention time

s the most significant factor which controls surfactant-degradingicroorganisms in wastewater treatment. The biodegradation of

uaternary ammonium compounds is a complex process wherehe hydroxylation of the alkyl moiety is a crucial step. In the casef ester quats biologically facilitated hydrolysis commences theonsequent steps of the degradation. The kinetics of biodegrada-ion is of fundamental meaning to environment. Monod kineticss well many other models have been described to estimate theate constants and the extent of ultimate biodegradation. Theost important factors that influence kinetic models are the

iocidal activity of QACs, structure of alkylammonium surfac-ants, adsorption–desorption phenomena of QACs on sludge andiosolids and the presence of anionic compounds which can miti-ate the biocidal activity of cationics. The biodegradation of geminiurfactants is similar to some extent to the biodegradation ofonomeric QACs. However, the influence of structure of gemini

urfactants, especially these containing amide or sugar derivatives,n kinetics and degree of degradation is much stronger than theorresponding monomeric alkylammonium surfactants.

The results of the biodegradation study of alkylammonium sur-actants, both monomeric and dimeric, show that the structure ofhe compound, adsorption–desorption processes on sludge, typef microorganism consortia, and presence of anions have a funda-ental influence on the degree of QAC decomposition.

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Materials 280 (2014) 797–815 813

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