bioavailability of organic compounds solubilized in nonionic surfactant micelles

MINI-REVIEW

Bioavailability of organic compounds solubilized in nonionicsurfactant micelles

Zhilong Wang

Received: 6 September 2010 /Revised: 1 October 2010 /Accepted: 1 October 2010 /Published online: 19 October 2010# Springer-Verlag 2010

Abstract Whether direct availability of organic compoundsolubilized in nonionic surfactant micelles (bioavailability)in a bioremediation or biotransformation process is uncer-tain to some extent, which is partially attributed to thedifficulty by direct experimental determination. In anotherpoint of view, it should be ascribed to the fuzzy conceptabout the solubilization of organic compound in a nonionicsurfactant micelle aqueous solution. In this mini-review, thesolubilization of organic compound in surfactant micellesaqueous solution is fully discussed; especially saturatedsolubilization and unsaturated solubilization have beenemphasized. Then the current methods for estimation ofbioavailability of organic compounds solubilized inmicelles are introduced, in which the possible drawbacksof each method are stressed. Finally, the conclusion thatorganic compound solubilized in micelles is unavailabledirectly by microbes has been drawn and the intensificationof bioremediation or biotransformation by nonionic surfac-tant micelle aqueous solution is contributed to enhancementof the hydrophobic organic compounds dissolution.

Keywords Bioavailability . Solubilization .

Bioremediation . Nonionic surfactant .Micelles

Introduction

Bioremediation or biotransformation is usually hindered bythe limited solubility of hydrophobic compounds. Anaddition of nonionic surfactant to enhance the apparent

solubility is regarded as a potential strategy to enhance thebioprocess efficiency (Paria 2008; Randazzo et al. 2001).Especially, a nonionic surfactant micelle aqueous solutionat a temperature above its cloud point should separate into adilute phase and a surfactant-rich phase or coacervatephase, which is called cloud point system (Hinze andPramauro 1993). The cloud point system has also beenexploited as a novel two-phase partitioning system forextractive microbial fermentation (Wang et al. 2004a; Wang2007; Wang and Dai 2010). Besides the intensification ofmicrobial fermentation of hydrophobic compounds, anextraction of organic product to eliminate the productinhibition or prevention of the product from furtherdegradation by the microbial cells is also found in thenonionic surfactant micelle aqueous solution (Xue et al.2009) and cloud point system (Wang et al. 2008).

Generally, it is believed that only the organic compounddissolved in the true aqueous solution phase of a nonionicsurfactant micelle aqueous solution can be directly avail-able by the microbial cells (Volkering et al. 1995; Grimberget al. 1996a; Jahan et al. 1999). The intensification ofbioremediation or biotransformation is contributed to theenhancement of the hydrophobic organic compound disso-lution by the nonionic surfactant micelles while theelimination of organic product inhibition or prevention oforganic product from further degradation by the microbes isascribed to the obstacle of nonionic surfactant micellesbetween the microbes and the organic compound solubi-lized in micelles. Guha and Jaffe propose a concept ofbioavailability about organic compounds solubilized inmicelles (Guha and Jaffe 1996a, b). They believe thatmicrobial cells cannot only directly utilize the organiccompounds dissolved in the true aqueous solution phase butalso partially utilize the organic compounds solubilized innonionic surfactant micelles. The bioavailability concept

Z. Wang (*)School of Pharmacy, Shanghai Jiao Tong University,Shanghai 200240, People’s Republic of Chinae-mail: [email protected]

Appl Microbiol Biotechnol (2011) 89:523–534DOI 10.1007/s00253-010-2938-z

perfectly explains the intensification of bioremediation orbiotransformation of hydrophobic organic compounds andthe elimination of organic product inhibition or preventionof organic product from further degradation by themicrobes at the same time, in which the partial availabilityof the organic compound solubilized in micelles increasesthe insoluble hydrophobic organic compound concentrationto the microbial cells while the partial unavailability oforganic compounds solubilized in micelles prevents theorganic compounds from further degradation by themicrobial cells or eliminates the organic compound toxicityto the microbes when the organic compound concentrationis above the microbial inhibition concentration.

Although the bioavailability concept about the organiccompound solubilized in micelles is ideal, the experimentalconfirmation of its authenticity meets some difficulties,which mainly include that the utilization of organiccompounds in a nonionic surfactant micelle aqueoussolution by microbial cells is a complex dynamic process;the solubilization of organic compounds in micelles is alsoa dynamic process when the organic compounds are beingdynamically degraded or transformed. The method formeasurement of organic compound solubilized in micellesunder dynamic condition is unavailable because of thedifficulty in differentiating the organic compound solubi-lized in nonionic surfactant micelles from the organiccompound dissolved in the true aqueous solution. Thenonionic surfactants themselves usually also affect themicrobial growth in a bioremediation or biotransformationprocess.

In this mini-review, solubilization of organic compoundin micelle as the groundwork of bioavailability of organiccompounds solubilized in micelles was fully discussed;especially saturated solubilization and unsaturated solubili-zation were emphasized. Then, the methods for estimationof bioavailability of the organic compounds solubilized inmicelles were introduced, in which the possible drawbacksof each method were stressed. Finally, the conclusionthat the organic compound solubilized in micelles isunavailable directly by microbes has been drawn, and theintensification of bioremediation or biotransformation in anonionic surfactant micelle aqueous solution was ascribedto its enhancement of hydrophobic organic compounddissolution.

Solubilization

Solubilization is defined as “preparation of a thermody-namically stable isotropic solution of a substance normallyinsoluble or barely soluble in a given solvent by anintroduction of additional amphiphilic compounds orcomponents” (Mackay 1987). The mechanism about solu-

bilization of organic compounds in surfactant micelles hasbeen studied comprehensively, such as a hydrocarbonsolubilized in the micelle hydrophobic core, a more polarmaterial oriented in palisades region, a polar additivesolubilized in the region of the hydrated layer, an additivedirectly associated with the electrical double layer, etc.(Myers 1999). Not only hydrophobic organic compoundsbut also hydrophilic organic compounds can be solubilizedinto surfactant micelles. Polar compounds, particularlythose with hydrogen bond functional groups and aromatichydrocarbons, are found to have high solubilization(Haddou et al. 2006).

A thermodynamic equilibrium of an organic compoundsolubilized in a nonionic surfactant micelle aqueoussolution is represented by solubilization equilibrium con-stant (Edwards et al. 1991)

K ¼ MSR

ðMSRþ 1ÞCwVw; ð1Þ

where Cw is the organic compound concentration in the trueaqueous solution phase of a surfactant micelle aqueoussolution, and Vw is the molar volume of water (0.01805 L/mol at 25 °C). MSR is the molar solubilization ratio, whichis defined as

MSR ¼ Cm

Cs; ð2Þ

where Cm is the organic compound concentration solubi-lized in the micelles and Cs is the surfactant concentrationin the micelle formation.

Saturated solubilization

An excess of very sparse soluble organic compound in asurfactant micelle aqueous solution is usually under itssaturation condition. Under this condition, the organiccompound concentration in the true aqueous solution phaseis the corresponding solubility in the aqueous solution, i.e.,

Cw ¼ Csatw ; ð3Þ

where Csatw is the solubility of organic compound in an

aqueous solution without surfactant.At a surfactant concentration below its critical micelle

concentration (CMC), the apparent solubility of an organiccompound in a surfactant aqueous solution is equal to itssolubility in the aqueous solution. At a surfactant concen-tration above its CMC, the apparent solubility increaseslinearly with increasing surfactant concentration, i.e.,

Capp ¼ MSRðCs � CMCÞ þ Csatw ; ð4Þ

where Capp is the apparent solubility. The saturatedsolubilization equilibrium constant of an organic compound

524 Appl Microbiol Biotechnol (2011) 89:523–534

in a surfactant micelle aqueous solution is usually deducedfrom its apparent solubility, in which MSR value isdetermined from the slope of apparent solubility versussurfactant concentration (Edwards et al. 1991). The MSR isa constant under this condition and the correspondingsolubilization equilibrium constant is a constant (Eq. 1), too.

There are many reports about saturated solubilizationequilibrium constant of an organic compound in a singlenonionic surfactant micelle aqueous solution, in which alinear correlation between the saturated solubilizationequilibrium constant and the log P (P is the partitioningcoefficient of an organic compound in a water–octanol two-phase partitioning system) has been established,

logK ¼ a logPþ b; ð5Þ

where a and b are coefficients, which are determined by thechemical structure of a given nonionic surfactant (Li andChen 2002; Swe et al. 2006). A correlation of the saturatedsolubilization equilibrium constant with different nonionicsurfactants and organic compounds finds that the effect ofnonionic surfactant on saturated solubilization equilibriumconstant is relatively smaller compared to that of theorganic compound polarity. Thus, the organic compoundpolarity is one of the main factors to affect the saturatedsolubilization equilibrium constant (Wang 2009).

Unsaturated solubilization

Different from an excess of very sparse soluble organiccompounds solubilized in a surfactant micelle aqueoussolution, most organic compounds have a relatively highsolubility in an aqueous solution. When an organiccompound concentration in the true aqueous solution phaseof a surfactant micelle aqueous solution is below itssolubility, the solubilization equilibrium is very differentfrom that of saturated solubilization (Sepulveda 1974;Christian et al. 1985). It is found that solubilizationequilibrium constant and MSR under this condition arechanged with the organic compound and nonionic surfac-tant concentrations in a surfactant micelle aqueous solution.In this point of view, referring to MSR as an organiccompound partitioning coefficient between the micellepseudophase and the true aqueous solution phase, whichhas also been found in the literature (Guha and Jaffe 1996b;Dupont-Leclercq et al. 2007), may be more appropriate. Itis parallel to the partitioning coefficient of organic solute ina water-organic solvent two-phase partitioning system,which is affected by organic solute concentration. However,MSR or partitioning coefficient is difficult to determine asthe surfactant micelle aqueous solution is a single phase inmacro-scale, in which it is difficult to differentiate the

organic compound concentration dissolved in the trueaqueous solution phase (Cw) from that of solubilized inmicelle pseudophase (Cm), i.e., the experimental determi-nation of Cw becomes a key issue.

Many methods have been developed for experimentaldetermination of the solubilization equilibrium constantunder unsaturated solubilization conditions (Christian et al.1981; Katsuta and Saitoh 1998; Dupont-Leclercq et al.2007). Among them, the determination of organic com-pound absorbance change in a surfactant micelle aqueoussolution (Sepulveda 1974) and semiequilibrium dialysis(Christian et al. 1985) are commonly utilized by mostresearchers.

Surfactant aqueous solution at a concentration above itsCMC forms micelle pseudophases. An organic compounddissolved in the true aqueous solution phase and solubilizedin the micelle pseudophase should be under different micro-environments. The different micro-environments lead to theorganic compound absorbance change in a surfactantmicelle aqueous solution. Defining absorbance of everymole organic compound dissolved in the true aqueoussolution phase and solubilized in the micelle pseudophaseas A0 and A∞, respectively, the organic compound absor-bance in a surfactant micelle solution can be represented as(Sepulveda 1974)

A ¼ A1q þ A0ð1� qÞ; ð6Þ

where θ, the fraction of the organic compound solubilizedin micelles, is defined as

q ¼ Cm

C; ð7Þ

where C is the total organic compound concentration in thesurfactant micelle aqueous solution.

Equation 7 is enough to distinguish the organiccompound dissolved in the true aqueous solution from thatsolubilized in the micelle pseudophase. However, the valueof A∞ in the Eq. 6 should be determined previously. Forsome organic compounds, such as phenol, the solubilizationof organic compounds into the micelle pseudophase can betreated as adsorption or association of the organic com-pounds onto the surface of micelles or some other siteswithin the micelles, in which MSR can be represented withLangmuir isotherm (Kandori et al. 1989)

MSR ¼ Cm

Cs¼ MSRmkCw

1þ kCw; ð8Þ

where MSRm and k are constants in Langmuir isotherm,which represents the maximum mole solubilization ratio forthe surfactant micelle and the corresponding adsorption orassociation constant, respectively. The Eq. 8 clearly indicates

Appl Microbiol Biotechnol (2011) 89:523–534 525

that MSR is a function of organic compound concentrationdissolved in the true aqueous solution (Cw).

Combining Eqs. 6–8 leads to

q ¼ MSRmkCs

MSRmkCs þ 1þ kCð1� qÞ ð9Þ

When kC0(1─q)<<1, Eq. 9 reduces to

1

A� A0¼ 1

MSRmkðA1 � A0ÞCsþ 1

A1 � A0ð10Þ

Determining the absorbance of a certain concentration oforganic compound under different surfactant concentrationcondition, a plot of 1/(A─A0) vs 1/Cs results in a straightline with an intercept 1/(A∞−A0). A∞ can be obtained fromEq. 10 by using the least squares methods (Wang et al.2003a, b).

Estimation of MSR or solubilization equilibrium con-stant by determination of the changing organic compoundabsorbance in a surfactant micelle aqueous solution isrelatively simple. However, it is limited by Eq. 8, in whicha clear picture of how the organic compound solubilized inmicelles should be known. On the contrary, semiequili-brium dialysis (SED) method can be applied for all organiccompounds in a surfactant micelle aqueous solution(Christian et al. 1985).

A dialysis cell is the main device of SED method, whichis schematically represented in Fig. 1. The dialysis cell isseparated by an ultrafilter membrane into two compart-ments; one is called retentate compartment, the other iscalled permeate compartment. When a surfactant micelleaqueous solution with a certain concentration of surfactantand organic compound is filled into the retentate compart-

ment and an aqueous solution is filled into the permeatecompartment, the ultrafilter membrane lets the smallmolecules, such as water, organic compounds, and surfac-tant monomer, pass through freely. However, surfactantsforming micelles cannot permeate through the membrane.After reaching its dynamic equilibrium, assumptions can bemade (Christian et al. 1985)

1. There are the same organic compound concentrations inthe true aqueous solution phase (Cw) of both cells

2. Monomer surfactant concentration in the both cells isthe same (CMC)

Some authors further suppose that the surfactant con-centration in the permeate compartment is below or equal toits monomer concentration (CMC); thus, the organiccompound concentration in the permeate compartment isregarded as the organic compound concentration in the trueaqueous phase (Cw). An analysis of the surfactant concen-tration and organic compound concentration in the retentatecompartment is enough to determine the solubilizationequilibrium constant (Ergican and Geco 2008). However,experimental facts confirm that the surfactant concentrationin the permeate compartment is higher than thecorresponding CMC, which indicates the solubilization oforganic compound in surfactant micelles in the permeatecompartment as shown in Fig. 1 (Christian et al. 1985).Application of Eq. 4 in both permeate compartment andretentate compartment leads to

Cp ¼ MSRðCps � CMCÞ þ Cw ð11Þ

Cr ¼ MSRðCrs � CMCÞ þ Cw; ð12Þ

where the superscription p and r represents in the permeatecompartment and in the retentate compartment, respective-ly. After determining surfactant concentration and organiccompound concentration in both compartments, solubiliza-tion equilibrium constant can be determined with Eq. 11and 12. This is the theory of the famous SED (Christian etal. 1985).

It is well known that the solubilization of organiccompound in surfactant micelles aqueous solution is relatedto the micelle structures. The micelle structure is affectedby the temperature, surfactant concentration, solubilizationcapacity, etc. (Mackay 1987). The different surfactantconcentration in the permeate compartment and the reten-tate compartment in the SED experiment should affect thesolubilization equilibrium or MSR. However, this effect hasbeen neglected and it is supposed that MSR is constantunder a certain organic compound concentration in the trueaqueous solution phase (Cw).

In SED method, the determination of MSR and thensolubilization equilibrium constant should give the CMC

Fig. 1 Schematic represent of semiequilibrium dialysis (SED). Thetriangles represent organic compound, and the circles with tailsrepresent nonionic surfactants. The nonionic surfactant in the aqueoussolution exists as monomers or micelles. There is a dynamicequilibrium between the nonionic surfactant concentrations in themonomer state and the micelle state. The organic compounds in themicelle aqueous solution exist as free molecules in the aqueoussolution or solubilization in micelles. There is also a dynamicequilibrium between the organic compound concentrations in the freemolecules state and solubilization state


value of surfactant in an aqueous solution. For mostcommercial surfactants or mixture surfactants, theircorresponding CMC should be determined with an addi-tional experiment. A modified SED has been developed(Ucbiyama et al. 1993), in which a certain concentration ofsurfactant micelle aqueous solution, instead of an aqueoussolution as in the SED method, is filled in the permeatecompartment. After reaching dialysis equilibrium, thesurfactant concentrations in both permeate compartmentand retentate compartment are much higher than thecorresponding CMC. Thus, the Eqs. 11 and 12 can bereplaced with

Cp ¼ MSR � Cps þ Cw ð11aÞ

Cr ¼ MSR � Crs þ Cw ð12aÞ

The modified SED has been utilized for determination oforganic compound 2-phenylethanol solubilized in nonionicsurfactant Triton X-100 micelle aqueous solution (Dai et al.2010). As shown in Fig. 2, the MSR of moderate solubleorganic compound (2-phenylethanol) in the surfactantmicelle aqueous solution increases with the increase oforganic compound concentration in the true aqueoussolution phase (Cw). The organic compound concentrationin the true aqueous solution phase is affected by the organiccompound concentration (C), surfactant concentration (Cs),etc., which has been confirmed by many experimental facts(Christian et al. 1985; Rouse et al. 1995; Katsuta and Saitoh1998; Ucbiyama et al. 1993; Wang et al. 2003a, b).

Solubilization in coacervate phase

Application of cloud point system as an eco-friendlyseparation method for concentrated organic compounds,metal ions, and bioactive materials has been set up for along time (Hinze and Pramauro 1993), which attracts moreand more attention in recent years (Quina and Hinze, 1999).An exploitation of cloud point system as a novel two-phasepartitioning system for extractive microbial transformationhas also been reported (Wang et al. 2004a; Wang 2007;Wang and Dai 2010). However, the study of solubilizationof organic compound in the coacervate phase of a cloudpoint system is relatively few. Only a few reports about thistopic have been found (Sakulwongyai et al. 2000; Wanget al. 2003a).

Similar to the definition of solubilization equilibriumconstant and MSR in a surfactant micelle aqueous solution,the solubilization equilibrium constant (Kd) and MSRd inthe coacervate phase of a cloud point system are defined as

Kd ¼ MSRd

ðMSRd þ 1ÞCwVwð13Þ

MSRd ¼ Cdm

Cds; ð14Þ

where subscription d denotes in the coacervate phase. Inorder to estimate the organic compound solubilized in thecoacervate phase of a cloud point system, some assump-tions had been made:

1. The interaction between organic compound and surfac-tant in the dilute phase of a cloud point system abidesthe same rules as the solubilization of organic com-pound in a surfactant micelle aqueous solution

2. The organic compound concentration in the trueaqueous solution of the dilute phase (Cw) is the sameas that of in the coacervate phase

After determination of the solubilization of organiccompound in the corresponding surfactant micelle aqueoussolution, the solubilization of organic compound in thecoacervate phase can be estimated by a determination oforganic compound and surfactant concentration in thecoacervate phase of a cloud point system. However, thecloud point of a nonionic surfactant micelle aqueoussolution is the nature of a nonionic surfactant. Determina-tion of solubilization of organic compound in a surfactantmicelle aqueous solution under the temperature above itscloud point condition is impossible. Alternatively, determi-nation of solubilization of organic compound in a surfactantmicelle aqueous solution under the temperature below itscloud point condition cannot exclude the effect of temperatureon the solubilization. By application of SEDmethod, in which

0

0.02

0.04

0.06

0.08

0.1

0.12

0.14

0.16

0 0.5 1 1.5 2 2.5 3 3.5 4

Cw (ml/L)

MSR

(m

l/g)

Fig. 2 Unsaturated solubilization of 2-phenylethanol in Triton X-100micelle aqueous solution (Dai et al. 2010). The filled triangles areMSR values determined by the modified semi-equilibrium dialysis asshown in Eqs. 11a and 12a. The circles (filled ones and open onesrepresent 0.5 and 5 g/100 ml of nonionic surfactant Triton X-100concentration, respectively) are MSR value determined by dose–response method, which should be discussed in the next section


the determination of solubilization of organic compound insurfactant micelle aqueous solution is replaced with the sameseries of nonionic surfactant with high cloud point, showsthat solubilization equilibrium constant in the coacervate phase(Kd) of a cloud point system is only a little higher thanthat of its corresponding micelle aqueous solution. Theauthors attribute the difference to their experimental errors(Sakulwongyai et al. 2000). Similarly, applying the method ofdetermination of the changing organic compound absorbancein a surfactant micelle aqueous solution has also been carriedout, in which the solubilization of organic compound in asurfactant micelle aqueous solution has been determined.However, the cloud point system with the same nonionicsurfactant is formed by an addition of high concentration ofthe corresponding organic compound to decrease its cloudpoint, in which the effect of high organic compoundconcentration on solubilization may have existed (Wanget al. 2003a). The results show MSR value increases from2.9 (mole/mole) in the nonionic surfactant micelle aqueoussolution to 7.5 (mole/mole) in the coacervate phase of thecloud point system. Till now, those methods are only anapproximate estimation of organic compound solubilized inthe coacervate phase of a cloud point system due to theimmature experimental strategy for determining the solubili-zation of organic compound in the corresponding nonionicsurfactant micelle aqueous solution under the same condition.In a similar strategy, the solubilization of phenol in thecoacervate phase of nonionic surfactant C12E7 cloud pointsystem, in which the organic concentration in the trueaqueous solution (Cw) is replaced with the organic compoundconcentration in the dilute phase of a cloud point system (C),has also determined as shown in Fig. 3 (Wang et al. 2003b).It shows a remarkable difference between MSR value ofphenol in the coacervate phase of cloud point systems underdifferent phenol concentration conditions, in which the MSRin the coacervate phase and the phenol concentration in thedilute phase fits very well with Langmuir isotherm at arelatively lower phenol concentration whereas deviates at arelatively higher phenol concentration. Analogous to thephase structure of nonionic surfactant in the coacervate phasechanges from a lamellar to a reverse micelle with increasingtemperature (Sjoblom et al. 1987), changing phase structure isalso occurred with increasing phenol concentration. Itindicates that solubilization is related to the phase structureof nonionic surfactant in an aqueous solution. At the sametime, it also shows that MSRd is also a function of organiccompound concentration.

Bioavailability

Bioavailability is governed by a dynamic process of severaldistinctive phases. The first phase is physicochemical driven

(chemical availability) processes like sorption, desorption anddiffusion etc. Those processes are controlled by substrate-specific parameters such as hydrophobicity, aqueous solubil-ity etc. The second phases are physiological driven uptakeprocesses (biological availability) controlled by species-specific parameters like anatomy, surface–volume relation-ship, etc. Third, there are internal allocation processes(toxicological availability) controlled by organism-specificparameters like metabolism, detoxification and storagecapacity (Styrishave et al. 2008).

Chemical availability suitably refers to the degree ofinteraction between substrate and living microbes. A barriereffect of micelles between microbes and solubilized organiccompound reduces chemical availability. A direct-contactfraction of organic compound solubilized in micelles isdefined as

Ce ¼ Cw þ fCm; ð15Þwhere Ce is the directly utilized organic compoundconcentration by the microbial cells (Lee et al. 2007). f isthe bioavailability of organic compound solubilized inmicelles (Guha and Jaffe 1996a, b).

A direct determination of organic compound bioavail-ability in a nonionic surfactant micelle aqueous solution ishindered by the lack of appropriate methods to measure thepartitioning behavior of an organic compound among trueaqueous solution, micelle pseudophase and microbial cells.

0.6

0.8

1

1.2

1.4

1.6

1.8

0.01 0.015 0.02 0.025 0.03Reciprocal of phenol in dilute phase (L/mol)

Rec

ipro

cal o

f M

SR (

mol

/mol

)

Fig. 3 Langmuir isotherm plot for solubilization of phenol in coacervatephase of cloud point system (Wang et al. 2003b). With the increase ofphenol concentration, polyoxyethylene glycol monoether nonionicsurfactant (C12E7) micelle aqueous solution changes from an aqueoussolution to a two-phase system, then to a three-phase system, and thento a two-phase system again. Black circle indexes the coacervate phasein the two-phase region with a relatively lower phenol concentration.Within this phenol concentration ranges, solubilization of phenol isfitted with Langmuir isotherm, which is similar to that of in thesurfactant micelle aqueous solution. Blank square indexes the coacer-vate phase in the two-phase region with a relatively higher phenolconcentration. Within this phenol concentration ranges, solubilization ofphenol fails to fit with Langmuir isotherm and the solubilizationincreases markedly with the increasing phenol concentration


Similar to the determination of MSR under the unsaturatedsolubilization equilibrium condition, the obstacle of study-ing bioavailability (f) is how to experimentally determinethe Cw in a dynamic biodegradation of organic compoundprocess. Till now, there are three methods, i.e., dissolutionkinetic model (Grimberg et al. 1996a), dynamic micellemodel (Guha and Jaffe 1996a), and bio-toxicity experiment(Lee et al. 2007), which have been developed for estimationof the bioavailability of organic compound solubilized in anonionic surfactant micelle aqueous solution.

Dissolution kinetic model

A direct method to determine the bioavailability of organiccompounds solubilized in micelles is the degradation oforganic compounds in a nonionic surfactant micelleaqueous solution. However, it is hindered by how todifferentiate the organic compounds solubilized in themicelles (Cm) from those dissolved in the true aqueoussolution phase (Cw) in a dynamic process. Even markedorganic compound technique is invalid as the dynamicsolubilization of organic compound in micelles. Thus, anestimation of bioavailability based on the degradation oforganic compound must have the aid of dissolution kineticmodel.

When microbial growth occurs in a nonionic surfactantmicelle aqueous solution with a solid organic compound,such as phenanthrene, as the sole carbon resource, the totalorganic compound concentration in the nonionic surfactantmicelle aqueous solution (C) depends on both organiccompound biodegradation rate and organic compounddissolution rate

dC

dt¼ �vd þ vb; ð16Þ

where vd is the organic compound degradation rate and vb isthe organic compound dissolution rate.

An assumption is that the solubilization of organiccompounds in micelles is quickly equilibrated. Organiccompound solubilized in micelles is under-saturated solu-bilization condition at the interface of insoluble solidorganic compound while under unsaturated solubilizationcondition in the nonionic surfactant micelle aqueoussolution. The dissolution of organic compound from thesolid interfaces (Capp) to the nonionic surfactant micelleaqueous solution (C) follows the first-order rate model

vd ¼ kaaðCapp � CÞ; ð17Þ

where ka is the observed mass transfer coefficient, which isascribed to the mass transfer coefficient of organiccompounds dissolved in the true aqueous solution (Cw)

and the mass transfer coefficient of organic compoundssolubilized in micelles (Cm) (Grimberg et al. 1996a)

ka ¼ kmaMSRVm

MSRVm þ Vaþ kaa

Va

MSRVm þ Va; ð18Þ

where Vm and Va are the phase volume fraction of micellepseudophase and of aqueous solution phase, respectively. ais the area of the solid interfaces. kaa can be determinedexperimentally (Grimberg et al. 1994; Bernardez 2008).The apparent solubility (Capp) and the organic compoundconcentration under an unsaturated solubilization condition(C) can also be determined experimentally.

Another basic assumption is that mass transport is a ratelimiting step and the microbes can only directly utilize theorganic compound dissolved in the true aqueous solutionphase (Cw). The organic compound degradation rate can berepresented by Monod equation

vb ¼ mX=YX =S

¼ m0Cw

kmþCwX=YX=S

ð19Þ

The Monod equation in a nonionic surfactant micelleaqueous solution can be modified with the organiccompound concentration in the nonionic surfactant micelleaqueous solution (C) (Grimberg et al. 1996a)

m

m0sat

¼ C

kmCapp

Csatw

� �þ C

; ð20Þ

where m0sat is the specific growth rate of microbial growth in

the nonionic surfactant micelle aqueous solution undersaturated solubilization state, in which the solubilizationequilibrium constant (K) has been recognized as a constantunder different organic compound concentration conditions(Grimberg et al. 1994). Yx/s is biomass yield coefficient andX is biomass concentration. All those parameters can beexperimentally determined.

Combining the initial condition at t=0,

C ¼ Capp

X ¼ X0;ð21Þ

along with the experimentally measured parameters, thebiomass (X) and the organic compound concentration (C) inthe time course of biodegradation of organic compound in anonionic surfactant micelle aqueous solution can becalculated (Grimberg et al. 1996a). In a batch degradationof phenanthrene by Pseudomonas stutzeri P16 in thepresence of nonionic surfactant Tergitol NP-10 process,the model data of biomass and phenanthrene concentrationin the nonionic surfactant aqueous solution fits with thecorresponding experimental data very well, respectively(Grimberg et al. 1996a). Similarly, batch biodegradation ofphenanthrene by Pseudomonas stutzeri P-16 in the presenceof nonionic surfactant Brij 35 has also carried out, a similar


result is also achieved (Bernardez 2009). The assumption thatmicrobes can only directly utilize the organic compounddissolved in the true aqueous solution phase (Cw) has beenmade in the Eq. 19, which indicates that the organiccompounds solubilized in micelles cannot be directly utilizedby the microbes, i.e., the bioavailability of organic com-pounds solubilized in micelles is neglectable.

Alternatively, organic compound solubilized in micellesis under saturated solubilization condition at the interface ofinsoluble solid organic compound while under unsaturatedsolubilization condition in the nonionic surfactant micelleaqueous solution. As shown in Eq. 4, the Eq. 17 can bereplaced as

vd ¼ k0aaðA� CwÞ ð17aÞ

in which a constant solubilization equilibrium constant atdifferent organic compound concentrations has been sup-posed. A is a constant, ka′ is a lumped mass transfercoefficient including the effect of MSR. The Eq. 17a hasalso been utilized for simulation of batch degradation ofhydrophobic compounds in a nonionic surfactant aqueoussolution (Jahan et al. 1999). Its results also indicate that thebioavailability of organic compounds solubilized inmicelles can be neglected. However, as discussion aboutthe unsaturated solubilization in a surfactant micelleaqueous solution, the MSR is a function of organiccompound concentration. Thus the Eq. 17a is valid onlyunder the condition that changing Cw in the biodegradationprocess is so limited that the effect of Cw on MSR isneglectable.

Dynamic micelle model

Guha and Jaffe provide a novel model to explain thebioavailability of organic compounds solubilized inmicelles (Guha and Jaffe 1996a). The basic idea is that ahemi-micelle layer of surfactant molecules is formedaround the microbial cells. This allows a dynamic transferof the organic compound solubilized in micelle-phase to thehemi-micelles adjacent to the microbial cells. The organiccompound in the hemi-micelles then diffuses into the cellsand is biodegraded. ‘Empty micelles’ are exchanged withnew filled micelles in the surfactant micelle aqueoussolution. This mechanism provides an additional masstransfer pathway of the organic compound solubilized inthe micelles (fCm) to cells in paralleling to that of organiccompound dissolved in the true aqueous solution phase(Cw) as shown in Fig. 4.

To estimate the bioavailability of organic compoundssolubilized in micelles, Guha and Jaffe carry out aphenanthrene degradation experiment in the presence ofnonionic surfactant under strongly mixed condition, in

which the following assumption has been made (Guha andJaffe 1996b):

1. The system is completely mixed and transport is not ratelimiting, i.e., the solubilization of organic compound inmicelles under its solubilization equilibrium state

2. Transfer of organic compound between different phasesis instantaneous relative to the biodegradation timescale, so that equilibrium between different phases isalways established

3. The presence of the surfactant does not alter thespecific activity of the biomass, i.e., the kinetics is thesame as that of biodegradation in the aqueous solutioncontaining phenanthrene

Under the above assumptions, a similar kinetic model asEq. 16 has been set up, except that the organic compounddissolved in the true aqueous solution phase (Cw) in Eq. 19has been replaced with the effective organic compoundconcentration (Cw+fCm) as shown in Eq. 15. Stimulation ofexperimental data with this model finds that the value ofbioavailability f ranges from 0 to 1 (Guha and Jaffe 1996b).In the model calculation, the authors utilize MSR value,which is determined under saturated solubilization condi-tion, to calculate the organic compound partitioningbetween solubilized in micelles (Cm) and dissolved in trueaqueous solution phase (Cw). However, biodegradation ofphenanthrene in the well mixing system indicates thatorganic compound concentration decreases with the in-

Fig. 4 Pathway for transfer of organic compound solubilized inmicelles to cells (Guha and Jaffe 1996a). A transport process oforganic compound solubilized in micelles to cells may have thefollowing rate limiting steps: a Transport of contaminant by filledmicelles to the vicinity of the cell. b Exchange of the filled micelleswith the hemi-micelle layer. c Transfer of contaminant from the hemi-micelle to the cells


crease of degradation time, which hints that the organiccompound in the nonionic surfactant micelle aqueoussolution is under unsaturated solubilization condition (Guhaand Jaffe 1996b). The unsaturated solubilization as shownin Eq. 8 and Fig. 2 indicates that MSR increases with theincrease of organic compound in the true aqueous solution(Cw). It means that the utilization of MSR of saturatedsolubilization state to simulate the organic compounddegradation process should underestimate the organiccompound concentration dissolved in the true aqueoussolution (Cw), which has been ascribed to the bioavailabilityof organic compound solubilized in micelles (fCm).

The stimulation result of bioavailability (f) with a valuebetween 0 and 1 (Guha and Jaffe 1996b) is further used todevelop a dynamic micelle model by the authors (Guha andJaffe, 1996a; Guha et al. 1998), which has been furtherdeveloped by Brown (Brown 2007). Those dynamic micellemodels predict bioavailability with physical parameters.However, some of those parameters are immeasurable withexperiments, which have to estimate by fitting the knownbioavailability (f). To our depressed, the bioavailability dataare estimated by same method as described in biodegrada-tion of organic compound in nonionic surfactant micelleaqueous solution (Guha and Jaffe 1996b). Besides, anadditional mass transfer pathway of the organic compoundsolubilized in micelles to the microbial cells by hemi-micelles (Fig. 4) may be questionable in the point of viewthat dynamic organic compound solubilization equilibriumbetween solubilized in micelles (Cm) and dissolved in trueaqueous solution (Cw). Under equilibrium condition, libera-tion of organic compound from hemi-micelles (Cm) to thecells should instantly be equilibrated by the solubilization ofthe organic compound in the true aqueous solution (Cw) intothe “empty micelles”. For microbial degradation, theincreasing utilization of organic compounds by hemi-micelle adsorption pathway should be counteracted by thelow organic compound concentration dissolved in the trueaqueous solution (Cw).

Bio-toxicity experiment

Estimation of bioavailability with dissolution kinetic modelor dynamic micelle formation model should stimulate theexperimental data of batch degradation of organic com-pound in a nonionic surfactant micelle aqueous solution.The dynamic degradation process makes the direct deter-mination of organic compound solubilized in micelles (Cm)and dissolved in true aqueous solution (Cw) impossible.Different from fitting model values to the experimental dataof biodegradation process, Lee et al. propose a method toestimate the bioavailability of organic compound solubi-lized in micelles by measurement of the organic compoundbio-toxicity in a nonionic surfactant micelle aqueous

solution (Jang et al. 2007; Lee et al. 2007). A modificationof Eq. 15 includes the effect of the nonionic surfactantthemselves (Lee et al. 2007; Dai et al. 2010)

Ce ¼ Cse þ Cw þ fCm; ð15aÞ

where Cse is the bioequivalent concentration of the nonionicsurfactant, i.e., a given concentration of nonionic surfactantaqueous solution causes the same toxicity to the microbesas that in the corresponding concentration of organiccompound aqueous solution. Comparison to dissolutionkinetic model method or dynamic micelle model, determi-nation of organic compound toxicity to microbes in the bio-toxicity experiment is not necessary for degradation oforganic compound by the microbes and then the organiccompound concentration in the nonionic surfactant micelleaqueous solution can be kept as a constant. Thus thesolubilization equilibrium of organic compound betweensolubilized in micelles (Cm) and dissolved in true aqueoussolution (Cw) can be determined experimentally under thiscondition. However, another parameter, i.e., the synergictoxicity of the nonionic surfactant to the microbial cells(Cse), should be determined in the bio-toxicity experiment.

Lee et al. determines the bio-toxicity of organic compoundin nonionic surfactant micelle aqueous solution by measuringthe microbial survival rate (Jang et al. 2007; Lee et al. 2007).The bioavailability of organic compound solubilized inmicelles is estimated to be f=0–1, which is similar to theresult of dynamic micelle model (Guha and Jaffe 1996a, b;Guha et al. 1998). However, this is questionable in theirexperimental methods. First, the bio-toxicity has beendetermined by dose–response method. It is well known thatthe dose (organic compound concentration) and response(bio-toxicity) is a nonlinear relationship. Thus, a directaddition of the organic compound toxicity (Cw+fCm) andthe nonionic surfactant toxicity (Cse), which are determinedin separated experiments, to represent the bio-toxicity oforganic compounds in an nonionic surfactant aqueoussolution (Ce) as shown in Eq. 15a is inappropriate (Lee etal. 2007). Second, the authors carry out the bio-toxicityexperiment under a certain organic compound concentrationin an unsaturated solubilization state while calculating theorganic compound dissolved in the true aqueous solution(Cw) with MSR value under saturated solubilization equilib-rium condition. It leads to underestimate the organiccompound dissolved in the true aqueous solution (Cw) whileoverestimate the bioavailability of organic compound solu-bilized in micelles (fCm) as discussed in the above section.

A bioequivalence concept has been introduced torepresent the bio-toxicity of organic compound in anonionic surfactant micelle aqueous solution (Dai et al.2010). The bioequivalence is defined as the organic


compound concentration in an aqueous solution causing thesame bio-toxicity to the microbes as that of a certainconcentration of organic compound in a nonionic surfactantmicelle aqueous solution. Thus, the nonionic surfactanttoxicity (Cse) or the synergic bio-toxicity of nonionicsurfactant and organic compound (Cw+fCm+Cse) can berepresented with its corresponding bioequivalence, respec-tively. For example, as shown in Fig. 5, a dose–responseanalysis in an aqueous solution (control) exhibits anonlinear relationship between the relative activity (bio-toxicity) and the organic compounds concentration. 0.1% 2-phenylethanol in 0.5% Triton X-100 aqueous solutionexhibits about 45% relative activity, while 0.42% 2-phenylethanol in the aqueous solution also exhibits about45% relative activity. The bioequivalence of 0.1% 2-phenylethanol in 0.5% Triton X-100 aqueous solution is0.42% 2-phenylethanol in the aqueous solution. Thus, thebio-toxicity of each component in Eq. 15a can be addeddirectly. A deduction the bio-toxicity of the nonionicsurfactant, the bioavailability can be in principal determinedwith the organic compound solubilization data in thenonionic surfactant micelle aqueous solution.

The synergic bio-toxicity of excess naphthalene indifferent concentrations of nonionic surfactant micelleaqueous solution is nearly a constant (Dai et al. 2010), inwhich the organic compound solubilized in micelles (Cm)should increase linearly under the saturated solubilizationcondition. According to Eq. 15a, one of the cases is adecrease of f with the increase of Cm (Guha and Jaffe

1996a, b), which keeps the constant fCm value. A morepossible case is that bioavailability of organic compoundsolubilized in micelles (f) equals zero, which reducesEq. 15a to

Ce ¼ Cse þ Cw; ð15bÞi.e., the toxicity of organic compounds to microbes in anonionic surfactant micelle aqueous solution is attributed tothe organic compound dissolved in the true aqueoussolution and the nonionic surfactant themselves. Accordingto Eq. 15b, the bioequivalence concentration of the synergictoxicity of 2-phenylethanol in the nonionic surfactantmicelle aqueous solution (Fig. 5) has been further used tocalculate 2-phenylethanol solubilized in micelles (Cm) andthe corresponding MSR values. The calculated MSR valuesand experimental data of semi-equilibrium dialysis bymodified SED are consisted very well as shown in Fig. 2,which indicates that the organic compound solubilized inmicelles is indirectly bioavailable or at least be neglectable.

Dissolution and bioaccessibility

Besides the above examples, there are many other exper-imental facts about the non-available organic compoundsolubilized in micelles. For example, based on a linearsolubilization model, Volkering et al. correlates the micro-

0

20

40

60

80

100

120

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1

2-phenylethanol (%, V/V)

activ

ity (

%)

control

0.5g/100ml

5g/100ml

Fig. 5 Effect of nonionic surfactant Triton X-100 on dose–responsecurves of 2-phenylethanol (Dai et al. 2010). The bio-toxicity oforganic compound 2-phenylethanol to baker's yeast in the nonionicsurfactant Triton X-100 micelle aqueous solution is determined bydose–response analysis. The activity is measured with metabolism ofglucose ability of with a certain amount of biomass (resting cell) in a(micelle) aqueous solution with a certain glucose concentration. Thebio-toxicity is indexed by the relative activity to that of in an aqueoussolution without organic compound and nonionic surfactant

0.45

0.46

0.47

0.48

0.49

0.5

0.51

0 1 2 3 4 5 6 7time (day)

Cw

(m

g/L

)

Fig. 6 Simulated cholesterol concentration in the aqueous solution ofmicrobial transformation in cloud point system (Wang et al. 2004b).The product concentration in the microbial transformation ofcholesterol in a cloud point system has been determined, which isutilized to simulate the complex kinetics and the cholesterolconcentration in the true aqueous solution. In the initial microbialgrowth phase, the cholesterol concentration in the true aqueoussolution is the same as its solubility in an aqueous solution; with theincreasing time, corresponding to the microbial logarithmic growthphase, the cholesterol concentration in the true aqueous solutiondecreases to meet the demand of microbial growth. The dissolution ofcholesterol becomes limited; with further increasing time,corresponding the microbial growth stagnant phase, the cholesterolconcentration in the true aqueous solution increases again


bial growth kinetic with the organic compound concentrationdissolved in the true aqueous solution (Cw) in the presenceand absence of nonionic surfactant, which find that the effectof nonionic surfactant on microbial growth kinetics isneglectable and draws a conclusion that the organic com-pound solubilized in micelles is non-bioavailable (Volkeringet al. 1995). It is safe to believe that the bioavailability oforganic compounds solubilized in micelles is neglectable.

Wang et al. has simulated the microbial transformationof hydrophobic compound cholesterol in a cloud pointsystem. The basic model is the same as Eq. 16, in which thedissolution of solid organic compound cholesterol from thesolid interfaces to the aqueous solution is calculated withEq. 17a and the microbial growth model Eq. 19 is modifiedwith a product inhibition (Wang et al. 2004b). Bymeasurement of product concentration in the batch micro-bial transformation, the organic compound dissolved in thetrue aqueous solution (Cw) has been stimulated as shown inFig. 6. In the overall process, the organic compoundconcentration in the true aqueous solution maintains nearlyto its solubility. The enhancement of hydrophobic cholesteroldissolution intensifies microbial growth and the correspondingmicrobial transformation process (Wang et al. 2004a; 2006).Similarly, the enhancement of dissolution of hydrophilicorganic compounds by the nonionic surfactant micelleaqueous solution has also been reported (Grimberget al. 1996b), which provides positive effect of nonionicsurfactants on biodegradation (Paria 2008) or biotransforma-tion (Randazzo et al. 2001; Berti et al. 2002) of hydrophobiccompounds. In the same way, intracellular organic compoundconcentration of a microbial biodegradation in a nonionicsurfactant micelle aqueous solution is higher than that of in anaqueous solution (Keane et al. 2008), which may be causedby the enhancement dissolution by the surfactant micelles andcannot be used as evidence for the bioavailability of organiccompound solubilized in micelles.

It should be stressed that bioavailability and bioaccessibilityare not necessarily identical terms and they are depending onthe species in question (Semple et al. 2004). Bioavailablecompound is defined as which is freely available to cross amicrobial cellular membrane from the medium the microbialinhabits at a given time. Bioaccessible compound is definedas which is available to cross a microbial cellular membranefrom the environment. However, the organic compound maybe either physically removed from the microbes or onlybioavailable after a period of time. According to thosedefinitions, the organic compound solubilized in micelles isbioaccessible while not bioavailable.

Acknowledgements The authors acknowledge the financial supportfrom the National Natural Science Foundation of China (No. 20676080;21076123) andMorning Star Promotive Program for Young Scholar ofShanghai Jiao Tong University, Shanghai, China (No. T241460631).

References

Bernardez LA (2008) Dissolution of polycyclic aromatic hydrocarbonsfrom a non-aqueous phase liquid into a surfactant solution using arotating disk apparatus. Colloids Surf A 320:175–182

Bernardez LA (2009) A rotating disk apparatus for assessing thebiodegradation of polycyclic aromatic hydrocarbons transferringfrom a non-aqueous phase liquid to solutions of surfactant Brij35. Bioprocess Biosyst Eng 32:415–424

Berti D, Randazzo D, Briganti F, Scozzafava A, Gennaro PD, Galli E,Bestetti G, Baglioni P (2002) Nonionic micelles promote wholecell bioconversion of aromatic substrates in an aqueous environ-ment. Langmuir 18:6015–6020

Brown D (2007) Relationship between micellar and hemi-micellarprocesses and the bioavailability of surfactant-solubilized hydro-phobic organic compounds. Environ Sci Technol 41:1194–1199

Christian SD, Tucher EE, Lane EH (1981) Precise vapor pressuremeasurements of the solubilization of cyclohexane by sodiumoctyl sulfate and sodium actyl sulfate micelles. J ColloidInterface Sci 84(2):423–432

Christian S, Smith GA, Tucker EE (1985) Semiequilibrium dialysis: anew method for measuring the solubilization of organic solutesby aqueous surfactant solutions. Langmuir 1:564–567

Dai Z, Wang Z, Xu J-H, Qi H (2010) Assessing bioavailability of thesolubilization of organic compound in nonionic surfactant micellesby dose–response analysis. Appl Microbiol Biotechnol 88:327–339

Dupont-Leclercq L, Giroux S, Henry B, Rubini P (2007) Solubiliza-tion of amphiphilic carboxylic acids in nonionic micelles:determination of partition coefficients from pKa measurementsand NMR experiments. Langmuir 23:10463–10470

Edwards DA, Luthy RG, Liu Z (1991) Solubilization of polycyclicaromatic hydrocarbons in micellar nonionic surfactant solutions.Environ Sci Technol 25(1):127–133

Ergican E, Geco H (2008) Nonlinear two-phase equilibrium model forthe binding of arsenic anions to cationic micelles. J MembraneSci 325:69–80

Grimberg SJ, Aitken MD, Stringfellow WT (1994) The influence ofsurfactant on the rate of phenanthrene mass transfer into water.Water Sci Technol 30(7):23–30

Grimberg SJ, Miller CM, Aitken MD (1996a) Surfactant-enhanceddissolution of phenanthrene into water for laminar flow con-ditions. Environ Sci Technol 30:2967–2974

Grimberg SJ, Stringfellow WT, Aitken MD (1996b) Quantifying thebiodegradation of phenanthrene by Pseudomonas stutzeri P16 inthe presence of a nonionic surfactant. Appl Environ Microbiol 62(7):2387–2392

Guha S, Jaffe PR (1996a) Bioavailability of hydrophobic compoundspartitioned into the micellar phase of nonionic surfactants.Environ Sci Technol 30(4):1382–1391

Guha S, Jaffe PR (1996b) Biodegradation kinetics of phenanthrenepartitioned into the micellar phase of nonionic surfactants.Environ Sci Technol 30(4):605–611

Guha S, Jaffe P, Peters CA (1998) Bioavailability of mixtures of PAHspartitioned into the micellar phase of a nonionic surfactant.Environ Sci Technol 32:2317–2324

Haddou B, Canselier JP, Gourdon C (2006) Cloud point extraction ofphenol and benzyl alcohol from aqueous stream. Separ PurifTechnol 50:114–121

Hinze WL, Pramauro E (1993) A critical review of surfactant-mediated phase separations (cloud-point extraction): theory andapplications. Criti Rev Anal Chem 24(2):133–177

Jahan K, Ahmed T, Maier W (1999) Modeling the influence ofnonionic surfactants on biodegradation of phenanthrene. WaterRes 33(9):2181–2193


Jang SA, Lee DS, Lee MW, Woo SH (2007) Toxicity of phenanthrenedissolved in nonionic surfactant solutions to Pseudomonas putidaP2. FEMS Microbiol Lett 267:194–199

Kandori K, McGreevy RJ, Schechter RS (1989) Solubilization ofphenol in polyethoxylated nonionic micelles. J Colloid InterfaceSci 132(2):395–402

Katsuta S, Saitoh K (1998) A micellar electrokinetic chromatographicmethod for determination of solubilization isotherms in surfactantmicelles. Anal Chem 70:1389–1393

Keane A, Lau PCK, Ghoshal S (2008) Use of a whole-cell biosensorto assess the bioavailability enhancement of aromatic hydrocar-bon compounds by nonionic surfactants. Biotechnol Bioeng 99(1):86–98

Lee HJ, Lee MW, Lee DS, Woo SH, Park JM (2007) Estimation ofdirect-contact fraction for phenanthrene in surfactant solutions bytoxicity measurement. J Biotechnol 131:448–457

Li J-L, Chen B-H (2002) Solubilization of model polycyclic aromatichydrocarbons by nonionic surfactants. Chem Eng Sci 57:2825–2835

Mackay RA (1987) Solubilization. In: Schick MJ (ed) Nonionicsurfactants physical chemistry. Marcel Dekker, Inc, New York

Myers D (1999) Surfaces, interfaces and colloids: principles andapplications, 2nd edn. Wiley, New York, pp p271–273

Paria S (2008) Surfactant-enhanced remediation of organic contami-nated soil and water. Adv Colloid Interface Sci 138:24–58

Quina FH, Hinze WL (1999) Surfactant-mediated cloud pointextractions: an environmentally benign alternative separationapproach. Ind Eng Chem Res 38:4150–4168

Randazzo D, Berti D, Briganti F, Baglioni P, Scozzafava A, GennaroPD, Galli E, Bestetti G (2001) Efficient polycyclic aromatichydrocarbons dihydroxylation in direct micellar systems. Bio-technol Bioeng 74(3):240–248

Rouse J, Sabatini D, Deeds N, Ericbrown R (1995) Micellar solubiliza-tion of unsaturated hydrocarbon: semiequilibrium dialysis. EnvironSci Technol 29:2484–2489

Sakulwongyai S, Trakultumupatam S, Scamehron JF, Oswan S,Christian SD (2000) Use of a surfactant coacervate phase toextraction of chlorinated aliphatic compounds from water:extraction of chlorinated ethanes and quantitative comparison tosolubilization in micelles. Langmuir 16(22):8226–8230

Semple KT, Doick KJ, Jones KC, Burauel P, Craven A, Harms H(2004) Defining bioavailability and bioaccessibility of contami-nated soil and sediment is complicated. Environ Sci Technol38:229A–231A

Sepulveda L (1974) Absorbance of solutions of cationic micelles andorganic anions. J Colloid Interface Sci 46(3):372–379

Sjoblom J, Stenius P, Danielession I (1987) Phase equilibrium ofnonionic surfactants and the formation of microemulsion. In:

Schick MJ (ed) Nonionic surfactants physical chemistry. MarcelDekker, Inc, New York

Styrishave B, Mortensen M, Krogh PH, Andersen O, Jensen J (2008)Solid-phase microextraction (SPME) as a tool to predict thebioavailability and toxicity of pyrene to the springtail, Folsomiacandida, under various soil conditions. Environ Sci Technol42:1332–1336

Swe MM, Yu LE, Hung K-C, Chen B-H (2006) Solubilization ofselected polycyclic aromatic compounds by nonionic surfactants.J Surfactants Deterg 9(3):237–244

Ucbiyama H, Tucker CSD, EE SJF (1993) A modified semiequili-brium dialysis method for studying solubilization in surfactantmicelles: testing the semiequilibrium assumption. J Phys Chem97:10868–10871

Volkering F, Breure A, van Andel JG, Rulkens WH (1995) Influenceof nonionic surfactants on bioavailability and biodegradation ofpolycyclic aromatic hydrocarbons. Appl Environ Microbiol 61(5):1699–1705

Wang Z (2007) The potential of cloud point system as a novel two-phase partitioning system for biotransformation. Appl MicrobiolBiotechnol 75:1–10

Wang Z (2009) Predicting organic compound recovery efficiency ofcloud point extraction with its quantitative structure-solubilizationrelationship. Colloids Surf A 349:214–217

Wang Z, Dai Z (2010) Extractive microbial fermentation in cloudpoint system. Enzyme Microb Technol 46:407–418

Wang Z, Zhao F, Li D (2003a) Determination of solubilization ofphenol of coacervate phase in cloud point extraction. ColloidsSurf A 216(1–3):207–214

Wang Z, Zhao F, Li D (2003b) Solubilization of phenol in coacervatephase of cloud point extraction. J Chem Ind Eng China 54(10):1387–1390

Wang Z, Zhao F, Hao X, Chen D, Li D (2004a) Microbialtransformation hydrophobic compound in cloud point system. JMol Catal B Enzym 27:147–153

Wang Z, Zhao F, Hao X, Chen D, Li D (2004b) Model of bioconversionof cholesterol in cloud point system. Biochem Eng J 19:9–13

Wang Z, Zhao F, Chen D, Li D (2006) Biotransformation ofphytosterol to produce androsta-diene-dione by resting cellsMycobacterium in cloud point system. Process Biochem 41(3):557–561

Wang Z, Xu J-H, Liang R, Qi H (2008) A downstream process withmicroemulsion extraction for microbial transformation in cloudpoint system. Biochem Eng J 41:24–29

Xue Y, Qian C, Wang Z, Xu J-H, Yang R, Qi H (2009) Investigationof extractive microbial transformation in nonionic surfactantmicelle aqueous solution using response surface methodology.Appl Microbiol Biotechnol 85(1):517–524


bioavailability of organic compounds solubilized in nonionic surfactant micelles

Documents