Efforts to improve coupled in situ chemical oxidation with bioremediation: a review of optimization...

SOILS SEC 5 bull SOIL AND LANDSCAPE ECOLOGY bull REVIEW ARTICLE

Efforts to improve coupled in situ chemical oxidationwith bioremediation a review of optimization strategies

Nora B Sutton amp J Tim C Grotenhuis amp

Alette A M Langenhoff amp Huub H M Rijnaarts

Received 7 June 2010 Accepted 6 July 2010 Published online 10 August 2010 The Author(s) 2010 This article is published with open access at Springerlinkcom

AbstractPurpose In order to provide highly effective yet relativelyinexpensive strategies for the remediation of recalcitrantorganic contaminants research has focused on in situtreatment technologies Recent investigation has shownthat coupling two common treatmentsmdashin situ chemicaloxidation (ISCO) and in situ bioremediationmdashis not onlyfeasible but in many cases provides more efficient andextensive cleanup of contaminated subsurfaces Howeverthe combination of aggressive chemical oxidants withdelicate microbial activity requires a thorough understand-ing of the impact of each step on soil geochemistry biotaand contaminant dynamics In an attempt to optimizecoupled chemical and biological remediation investigationshave focused on elucidating parameters that are necessaryto successful treatment In the case of ISCO the impacts ofchemical oxidant type and quantity on bacterial populationsand contaminant biodegradability have been consideredSimilarly biostimulation that is the adjustment of redoxconditions and amendment with electron donors acceptorsand nutrients and bioaugmentation have been used toexpedite the regeneration of biodegradation followingoxidation The purpose of this review is to integrate recent

results on coupled ISCO and bioremediation with the goalof identifying parameters necessary to an optimizedbiphasic treatment and areas that require additional focusConclusions and recommendations Although a biphasictreatment consisting of ISCO and bioremediation is afeasible in situ remediation technology a thorough under-standing of the impact of chemical oxidation on subsequentmicrobial activity is required Such an understanding isessential as coupled chemical and biological remediationtechnologies are further optimized

Keywords Bioremediation Biostimulation Contaminantremediation In situ chemical oxidation Subsurfacecontamination

1 Introduction

Subsurface and groundwater contamination of recalcitrantorganic compounds has created a large industry fortechnologies able to clean up polluted sites The interna-tional market for the remediation sector is valued at US$50ndash60 billion (Singh 2009) Conventional technologiesfocus on ex situ or on-site removal of contaminants throughexcavation or by so-called pump-and-treat remediation ofgroundwater However the high costs and health risksassociated with removal of contaminated material havespurred a shift toward in situ technologies where decom-position of xenobiotic compounds via chemical or biolog-ical pathways is contained within the subsurfaceenvironment (EPA 1998) Of the pool of remediationstrategies in situ bioremediation and more recently in situchemical oxidation (ISCO) are arguably the most common-ly used in situ treatments adaptable to a variety ofsubsurface conditions and contaminant types

Responsible editor Ji-Zheng He

N B Sutton () J T C Grotenhuis H H M RijnaartsDepartment of Environmental TechnologyWageningen UniversityBomenweg 26703 HD Wageningen The Netherlandse-mail NoraSuttonwurnl

A A M LangenhoffDepartment of Subsurface and GroundwaterDeltares Princetonlaan 63508 AL Utrecht The Netherlands

J Soils Sediments (2011) 11129ndash140DOI 101007s11368-010-0272-9

During an ISCO treatment chemical oxidants arepumped into the subsurface to oxidize organic pollutantsThis aggressive treatment removes source zone contami-nants either sorbed to soil organic matter or pure productpresent as nonaqueous phase liquids (Seol et al 2003Watts and Teel 2005) Typical treatments include Fentonrsquosreagent with hydrogen peroxide and ferrous iron the lessacidic modified Fentonrsquos reagent permanganate persulfateand ozone injection (Table 1) A number of review articlesprovide insight into the chemistry and proper application ofoxidation regimens (Gates and Siegrist 1995 Kubal et al2008 Rivas 2006 Seol et al 2003 Tsai et al 2008 Wattsand Teel 2005) ISCO has been successfully used to oxidizeand thus lower the concentration of petroleum-derivedhydrocarbons (total petroleum hydrocarbons TPH Crimiand Taylor 2007 Gates and Siegrist 1995 Huang et al 2005Jung et al 2005 Lee and Kim 2002) polyaromatic hydro-carbons (PAH Lee and Hosomi 2001 Masten and Davies1997 Nam et al 2001 Watts et al 2002) and chlorinatedhydrocarbons (Huang et al 1999 2005 Hunkeler et al2003 Northup and Cassidy 2008 Ormad et al 1994Schnarr et al 1998 Siegrist et al 1999 Vella and Veronda1993 Watts et al 1990) ISCO is a versatile remediationstrategy providing rapid and extensive removal of both lightand dense recalcitrant compounds in pure phase

Biological-based remediation technologies require lon-ger time spans than chemical oxidation techniques and aremore appropriate for the bioavailable plume section of acontaminated site (Singh 2009) Whereas fungi and plantsalike can mediate removal of recalcitrant compounds herewe focus on biodegradation by bacterial populations Theubiquity of hydrocarbon-utilizing bacteria indicates thatnatural attenuation that is the inherent biodegrading abilityof contaminated soils will in most cases occur withoutintervention (Surridge et al 2009) That said a number oftechnologies aim to increase the rate of bioremediationeither by increasing the bioavailability of contaminantsthrough the application of surfactants (Menendez-Vega etal 2007 Tsai et al 2009c Volkering et al 1998) or bycreating conditions ideal for general microbial growth andfor specific reactivity to a compound In the case ofpetroleum-based hydrocarbons these include biostimula-tion with nutrients (Gallego et al 2001 Menendez-Vega etal 2007) and electron acceptor addition for example bybioventing to provide oxygen to accelerate aerobic degra-dation pathways (Hoeppel et al 1991 Malina andGrotenhuis 2000) Microbial dechlorination of highlychlorinated compounds occurs under anaerobic conditionsThus stimulation includes the addition of an appropriateelectron donor and nutrients to create ideal (redox)conditions (Aulenta et al 2006 Hoelen et al 2006 Songet al 2002) Bioaugmentation with a bacterial enrichmentor culture able to break down the contaminant of interest

has been used to improve bioremediation of (chlorinated)hydrocarbon contaminants (Demque et al 1997 Pu andCutright 2007 Salanitro et al 2000 Smith et al 2005Straube et al 2003) This strategy is most commonly usedto accelerate conversion of tetrachloroethene (PCE) toharmless ethene through the addition of cultures enrichedwith Dehalococcoides spp the only bacterial group knownto perform the complete chain of metabolic halorespirationreactions to produce ethene (Adamson et al 2003 Hood etal 2008 Krumins et al 2009 Major et al 2002 Scheutz etal 2008 Tas et al 2009)

Conventional wisdom dictates that chemical oxidation isnot compatible with biological-based remediation techni-ques The oxidative stress increase or decrease in pH(persulfate and Fentonrsquos reagent respectively) and changein redox conditions caused by ISCO treatments significant-ly alter subsurface conditions and are toxic to microbialpopulations (Buyuksonmez et al 1998 Macbeth et al2007 Miller et al 1996) However recent work indicatesthat although chemical oxidation can temporarily reducemicrobial activity bacterial populations do regeneratecontaminant degradation ability both in the field (Jones etal 2009 Koch et al 2007 Ladaa et al 2008 Luhrs et al2006 Macbeth et al 2005 Studer et al 2009) and inlaboratory experiments (Aunola et al 2006 Hood et al2006 Kao and Wu 2000 Kulik et al 2006 Ndjoursquoou et al2006) In many cases it has been concluded that ISCOpretreatment appears to improve overall remediation by (1)decreasing the concentration of pollutants to levels lesstoxic for the soil biota (Chapelle et al 2005) (2) improvingbioavailability of the parent compound (Kulik et al 2006Miller et al 1996) (3) producing bioavailable andbiodegradable oxidized daughter compounds (Lee andHosomi 2001 Marley et al 2003 Miller et al 1996 Namet al 2001) or (4) providing oxygen for aerobic biologicaltransformation of contaminants (Kulik et al 2006) It hasrecently been suggested that as ISCO treatment is not ableto access and oxidize all residual contaminants biologicalpolishing is required to fully remediate a site (Cassidy et al2009)

This statement reflects the new direction of coupledchemical and biological treatment Previous reviews echoedthe ldquowait and seerdquo mentality common to earlier experi-ments where following chemical oxidation the regenera-tion of biomass was merely monitored without stimulation(Sahl and Munakata-Marr 2006 Waddell and Mayer 2003)However in the open system encountered in situ even localsterilization with chemical oxidants will eventually bereversed as groundwater upstream will always transportindigenous microorganisms (Brown et al 2009) Thisacceptance of microbial resilience is reflected in a recentshift in the literature toward more studies investigatingwhich parameters are essential to a biphasic remediation

130 J Soils Sediments (2011) 11129ndash140

strategy and how these parameters can be manipulatedHere we first consider the ISCO step summarizing work inwhich aspects of chemical oxidation are tested for theirinfluence on biodegradation and thus the overall remedia-tion process Secondly we will review literature in whichparameters essential to the rebound of an actively bio-remediating microbial population are examined

2 Improving ISCO treatment to enhance bioremediation

Conditions created during ISCO can significantly influencethe effectiveness and efficiency of subsequent biodegrada-tion of residual contaminants As summarized in Table 1chemical oxidation can create adverse environments interms of pH and oxidation potential that inhibit generalmicrobial growth and function Recent work has indicatedthat the type (Cassidy et al 2009 Kulik et al 2006 Xieand Barcelona 2003) and quantity (Buyuksonmez et al1999 Jung et al 2005 Palmroth et al 2006a Sahl et al2007 Valderrama et al 2009) of chemical treatment haverepercussions on soil geochemistry and bacterial popula-tions and thus on the success of continued bioremediationAdditionally the ISCO step oxidizes a specific fraction ofthe contamination producing a range of oxidized sub-strates The variety of compounds remaining after chemicaloxidation must be bioavailable and biodegradable in orderto ensure an effective bioremediation step

21 Impact of chemical oxidant type on subsequentbioremediation

It has been shown that known ISCO treatments areversatile able to oxidize a wide variety of substrates Thus

rather than choosing chemical oxidation regimens basedprimarily on the contaminant type treatments can bedesigned that cater to the requirements of the microbialpopulation This strategy generally improves the overallremoval efficiency

For example the high sulfate concentrations that remainfollowing persulfate oxidation can stimulate sulfate-reducing bacteria To avoid the evolution of the toxicH2S Cassidy and Hampton (2009) investigated the poten-tial of activating persulfate with calcium peroxide atalkaline pHs which favor production of the dissolvedhydrosulfide ion (HSminus) This strategy not only reduced H2Sproduction but also minimized the presence of toxicmercury ions through precipitation of stable mercurysulfide

Studies have been performed to screen various oxidants todetermine their impact on biological activity Treatments ofpermanganate modified Fentonrsquos reagent a calciumperoxide-based product and ferric iron-activated persulfatewere used to oxidize tetrachloroethylene- and ethylbenzene-spiked samples (Bou-Nasr and Hampton 2006) Fromoverall contaminant removal and cell number it wasconcluded that calcium peroxide resulted in the largestmass removal of the two contaminants 96 and 95respectively and an order of magnitude increase in thenumber of culturable heterotrophic microbes

However in most cases the ISCO treatment providingthe highest mass removal shows the largest negative impacton microbial activity and thus on the overall remediationefficiency (Fig 1) Cassidy et al (2009) tested thefeasibility of coupling pre-oxidation by ozone modifiedFentonrsquos reagent or sodium persulfate with bioremediationof soil contaminated with 24-dinitrotoluene (24-DNT) Itwas determined that although sodium persulfate less

Table 1 Conditions and reactions associated with common ISCO treatments (ITRC 2005 Teel et al 2009 Tsitonaki et al 2010)

ISCO treatment Important reactions Optimal pH Oxidation potential (V) Type of injection

Fentonrsquos reagent and H2O2 + Fe2+ rarr OH OHminus +Fe3+ 3ndash4 28 Liquid

Modified Fentonrsquos reagent H2O2 + OHrarrHO2+ H2O Neutral Hydroxyl radical LiquidHO2rarrO2

minus + H+ (OHminus)2H2O2rarr2H2O + O2

Activated persulfate

Metal activated Mn+ + S2O82minusrarrSO4

minus + SO42minus + Mn+1 3ndash4 26 Solution

Heat activated S2O82minus + heatrarr2SO4

minus Neutral Sulfate radical

Alkaline activated Reaction unknown gt105 (SO4ndash)

Ozone O3 + OHminusrarrO2 + 2OH Neutral 21 Gas

Permanganate MnO4minus + 2H2O + 3eminusrarrMnO2(s) + 4OHminus Neutral 17 Solution

2KMnO4 + C2HCl3rarr2CO2 + 2MnO2(s)+ 3Clminus + H+ + 2 K+

J Soils Sediments (2011) 11129ndash140 131

effectively oxidized 24-DNT overall remediation occurredwithin 14 days as compared to 30ndash90 days for modifiedFentonrsquos reagent and ozone respectively This result wasexplained by the fact that pre-oxidation with persulfateshowed a minimal impact on the 24-DNT-degradingportion of the microbial population both in terms ofnumber of degraders and the time required for bacterialdegradation to rebound In experiments where permanga-nate Fentonrsquos reagent or an oxygen-release compoundcontaining MgO2 were paired with bioremediation on jetfuel contaminated soil similar results were found (Xie andBarcelona 2003) Permanganate was the oxidant thatshowed the highest mass reduction but did not providethe greatest overall remediation efficiency Rather by usingthe less aggressive oxygen-release compound minimaldisruption of microbial activity was observed allowingfor overall removal of up to 80 of the oil-derivedhydrocarbons

The interaction between various soil matrices a numberof ISCO treatments and subsequent bioremediation hasalso been investigated (Kulik et al 2006) Sand and peatsamples spiked with creosote were treated with ozone andhydrogen peroxide with and without the addition of ferrousiron Whereas pre-oxidation steps showed an overall greaterefficiency in organic-poor sand samples biodegradation ofPAH contaminants was greater in peat experimentsespecially when ferrous iron was added to the ISCOtreatment It was concluded that traditional Fentonrsquos reagentwas the most effective pre-oxidation step for PAH-spiked

sand whereas ozone was more effective in the case of peatsamples Although it is known that the efficiency ofchemical oxidation is related to the matrix this workindicates that soil type to some extent dictates theeffectiveness of coupled chemical and biological treatment

22 Optimizing the quantity of chemical oxidant

Just as the type of chemical oxidant impacts bioremediationto varying degrees the quantity and concentration of ISCOcompounds also influence subsequent biological degrada-tion of recalcitrant contaminants Similar to the aforemen-tioned section addressing the type of chemical oxidantsinvestigations into the impact of the amount of oxidants onbioremediation found that less aggressive mass removal inthe chemical phase allowed for overall more efficientremediation (see Fig 1) In the case of column experimentson diesel-containing soil that was ozonated at 30 mgL fortime intervals between 60 and 900 min the extent ofbiodegradation was found to be inversely proportional tothe ozonation time (Jung et al 2005) Whereas the highestchemical TPH removal was 50 for 900 min of ozonationno further biodegradation occurred upon incubation for9 weeks However the 180-min treatment oxidized initiallyonly 37 of TPH but ultimately removed more contami-nation as a coupled treatment Similar results were obtainedwhen various ratios of hydrogen peroxide to iron were usedto oxidize creosote in aged natural samples (Valderrama etal 2009) It was determined that a H2O2Fe ratio of 201

0

20

40

60

80

100

Bio

only

101

201

401

601

Bio

only

KM

nO4

H2O2

MgO2

Bio

only

Ozo

ne

MFR

SPS

180 m

in

300 m

in

900 m

in

Rem

oval

Eff

icie

ncy (

)

Biological

Chemical

A DB C

Fig 1 Summary of removal efficiency for combined chemical andbiological remediation in instances where a variety of ISCO treatmentswere tested Data from A (Valderrama et al 2009) where labelsindicate the H2O2Fe ratio used for treatment B (Xie and Barcelona2003) where labels indicate the type of chemical oxidant used prior to

incubation for 134 days C (Cassidy et al 2009) where labels indicatethe type of chemical oxidant including modified Fentonrsquos reagent andiron-activated sodium persulfate (SPS) and data are for the first20 days of experimentation and D (Jung et al 2005) where labelsindicate the duration of ozone treatment


(molmol) was aggressive enough to remove 43 ofcontaminants without impeding further bioremediationwhich led to a total removal of 75 of PAHs

Column experiments which may more accuratelyrepresent the injection of ISCO chemicals in the field havehighlighted the influence of oxidant concentration andvolumetric flux on further bioremediation at a givenlocation in the column Working with columns containingPAH-contaminated (3318 mgkg) iron-rich (164 gkg)soils Palmroth et al (2006a) first applied a total of 04 ghydrogen peroxide per gram soil over the course of either 4or 10 days Subsequently column sections were separatelyincubated in batch experiments to determine the potentialfor bioremediation Averaging 36 removal of PAHcoupled treatment did not perform significantly better thancontrol setups without chemical oxidation in which 20ndash30 of PAHs were biodegraded However the largest massremoval (54) was found in a microcosm-containing soilfrom the lower part of the column that received thehydrogen peroxide treatment spread over 10 days Adifferent study with PCE-spiked sand columns in whichthe amount of permanganate and velocity of injection wereadjusted investigated the potential for coupled chemicaloxidation and reductive microbial dechlorination (Sahl etal 2007) The best results were obtained when a largequantity of oxidant with a low concentration was rapidlyinjected into the columnmdash315 pore volumes of 063 mMKMnO4 at a rate of 120 cmday From each of these studiesit can be concluded that through minimizing the amount ofdirect contact that bacteria have with concentrated chemicaloxidants the biological impact of oxidation is reduced ingeneral less aggressive oxidation improves the overallremediation efficiency

23 Bioavailability and biodegradability of contaminantsfollowing ISCO

In addition to optimizing the ISCO step to reduce biologicalimpacts it is essential to understand the influence ofchemical oxidation on the biodegradability and bioavail-ability of the remaining contaminant pool (Lee and Hosomi2001 Miller et al 1996 Nam et al 2001) Although mostISCO treatments increase bioavailability oxidation withpermanganate can reduce bacterial access to contaminantsUpon reaction with organic compounds precipitation ofmanganese oxide occurs which reduces soil permeability(Siegrist et al 2002) and can encapsulate contaminantspresent as nonaqueous phase liquids (MacKinnon andThomson 2002) As a result this portion of the pollutantremains inaccessible to either bacterial degradation ordissolution into the aqueous phase In previous lab studiesincreased bioremediation was associated with setups with alow concentration permanganate solution which was

injected at high velocity (Sahl et al 2007) Althoughregeneration of microbial activity could occur more rapidlyunder less oxidizing conditions improved overall remedi-ation efficiency may also be attributed to higher bioavail-ability of the remaining contaminant concentration underlower permanganate concentrations This work reinforcesthe importance of considering whether post-ISCO condi-tions are amenable to bacterial polishing when planning achemical oxidation strategy

Whereas chemical oxidation can either positively ornegatively impact bioavailability ISCO generally improvesbiodegrability of the contaminant pool A number ofstudies have investigated which parent and daughtercompounds within a mix of substrates are broken downduring the chemical or biological remediation steps in aneffort to determine how to optimally treat the wholecontamination Some work has suggested that the readilybiodegradable fraction of PAHs was chemically removed inthe course of Fentonrsquos reagent oxidation thus impedingfurther bioremediation (Aunola et al 2006) Howeverother research has found that pre-ozonation produced shortchain daughter compounds that were more easily biode-gradable (Liang et al 2009) Similarly Fentonrsquos reagenttreatment of spiked benz(a)anthracene samples oxidized43 of the contamination to produce benz(a)anthracene-712-dione (Lee and Hosomi 2001) During 63 days ofincubation 98 of the daughter compound was removedas compared to only 12 of the parent compound for anoverall 54 removal of benz(a)anthracene Manipulation ofthe ISCO phase to optimize the removal of the lessbiodegradable fraction of the contaminant was not furtherdiscussed

Work on weathered crude oil samples indicated thatpretreatment with permanganate influenced the biodegra-dation efficiency of different components of the contami-nation (Wrenn et al 2007) Biological degradation of theresin and aromatic fractions increased following permanga-nate treatment while bioremediation of the aliphaticfraction was reduced by 50ndash60 Similarly when optimiz-ing Fentonrsquos reagent dosages for subsequent bioremediationof PAH-contaminated soil it was noted that chemicaltreatment parameters had an influence on the fraction ofring sizes removed (Valderrama et al 2009) More of theless biodegradable five-ring PAHs were chemically oxi-dized in treatments with higher hydrogen peroxide concen-trations However optimal oxidant ratios for five-ring PAHremoval (601 H2O2Fe) had a negative effect on theregeneration of the bioremediating microbial communityThus this study does indicate the potential for designingoptimized treatment strategies in which the costs in terms ofregeneration of the bacterial population are balanced withthe benefits associated with removal of less biodegradablecompounds


3 Optimizing microbial regeneration following ISCO

Ideally the last moment of ISCO coincides with the firstmoment of bioremediation In practice regeneration ofmicrobial activity is a process Just as the microbiologygeochemistry and residual contaminant concentrations ofsoil must be considered during chemical oxidation anumber of parameters can be manipulated at the beginningof bioremediation After ISCO the naturally occurringdegradation processes inherent to the subsurface so-callednatural attenuation have been disturbed In the process ofenhanced or stimulated natural attenuation optimal con-ditions for bioremediation are recreated through theaddition of electron acceptors or donors nutrients andbacteria (bioaugmentation) Significant work has investi-gated biostimulation bioaugmentation and natural attenu-ation However in view of the fact that chemical oxidationcan have profound impacts on soil characteristics and biotawe consider here only work in which pre-oxidation occursBiostimulation in terms of the adjustment of redoxconditions to promote either aerobic or anaerobic bioreme-diation (Section 31) and amendment with electron donorsand nutrients (Section 32) are techniques that have beenused to ensure the proper activity of biodegradingmicrobes Bioaugmentation to re-inoculate soils withdepleted microbial populations will also be considered Asummary of conditions set for aerobic and anaerobicbioremediation in chemically pre-oxidized soils is given inTables 2 and 3

31 Redox process conditions in pre-oxidized soils

Creating and maintaining aerobic or anaerobic environ-ments for rapid removal of a particular contaminant ischallenging Aerobic conditions are generally conducive tobiodegradation of petroleum-based hydrocarbons and lesshalogenated compounds whereas anaerobic conditions arerequired for microbial mediation of highly halogenatedcompounds Chemical oxidation and aerobic bioremedia-tion can be combined relatively easily Bioventing andaerobic flushing to encourage bioremediation of petroleum-derived hydrocarbons are practices common to the currentsubsurface remediation market and which in research havebeen mimicked in the lab by maintaining oxygen saturationin column or microcosm experiments (Cassidy et al 2009Jung et al 2005 Kulik et al 2006 Palmroth et al 2006b)Often increased biological degradation has been attributedto aerobic conditions created by chemical oxidation (Kuliket al 2006 Palmroth et al 2006a) Studies have shown thatlow concentrations of hydrogen peroxide can be usedinstead of air flushing to meet biological oxygen demandsfor oil degradation in soils pretreated with Fentonrsquos reagent(Tsai et al 2009b) Other work associated an increase in

hydrogen peroxide concentrations from 100 to 900 mgLwith TPH removal efficiencies improving from 47 to69 respectively (Tsai et al 2009a) In field applicationsthis has led to the development of a variety of commerciallyavailable oxygenating products that both mobilize andpartially oxidize contaminants while simultaneously pro-viding oxygen to stimulate aerobic biodegradation (Bairdand Knight 2008 Blondel et al 2007 Lessard et al 2007Ochs and Singh 2007)

Anaerobic in situ biodegradation of halogenated organiccontaminants dissolved in groundwater by adding electrondonors and nutrients has been proven and widely applied inthe last decade (Aulenta et al 2006 Hoelen et al 2006Song et al 2002) However the reduced bioavailability ofpure product in the source zone and adsorption to theorganic-rich fraction of the solid phase matrix impedes fullbioremediation (Semple et al 2003) For these recalcitrantsource areas chemical oxidation pretreatment followed byanaerobic bioremediation may offer a solution In contrastto aerobic bioremediation rapid recreation of anaerobicconditions for dehalogenation in pre-oxidized soils can bechallenging Work in the field has confirmed the rebound ofanaerobic dechlorination by molecular techniques in tri-chloroethylene (TCE)-contaminated sites pre-oxidized withpermanganate (Jones et al 2009) and persulfate (Studer etal 2009) The regeneration of anoxic conditions amenableto dehalogenation generally requires input of electrondonors In the field such an increase in available electrondonors has been attributed to the mobilization of soilorganic matter by chemical oxidation (Westersund et al2006) In soils and engineered lab systems with less organicmatter content addition of carbon substrates is often required(see Table 3 Hrapovic et al 2005 Sahl et al 2007)

Although providing proper and ample carbon andnutrient sources is essential to microbial activity the redoxprocess conditions required for bioremediation must beconsidered when choosing an ISCO treatment Thuschemical oxidants such as hydrogen peroxide that producemolecular oxygen are better suited to the aerobic biodeg-radation phases In contrast permanganate oxidation occursvia direct electron transfer without the generation of oxygen(Wiberg and Saegebarth 1957) however the by-product ofchemical oxidation manganese oxide can inhibit reductivedechlorination by acting as an alternative electron acceptor(Hood et al 2006) In spite of this permanganate is oftenpreferred for studies where anaerobic conditions must beregenerated (Hrapovic et al 2005 Jones et al 2009 Sahl etal 2007 Tsai et al 2009c)

Addition of carbon substrates has been used to increase therates of both aerobic and anaerobic bioremediation pathways(see Tables 2 and 3) In batch experiments with fuel oil-spiked soil increased biodegradation was observed whenmicrocosms were supplemented with cane molasses in the


presence of excess oxygen (Tsai et al 2009a) Similarlycarbon sources such as ethanol and acetate (each 100 mgLHrapovic et al 2005) and methanol (20 mM Sahl et al2007) have been added as electron donors to increase therate of anaerobic halorespiration Whereas regeneration ofanaerobic TCE dechlorination activity was successful in the

former citation multiple attempts by Hrapovic et al tobiostimulate with electron donors proved fruitless Aselaborated upon in Section 33 biological degradation ofTCE did occur upon flushing with natural groundwaterindicating that electron donor sources were sufficientlypresent and other factors were impeding halorespiration

Table 2 Summary of investigations on the feasibility and optimal conditions for combined chemical oxidation and aerobic bioremediation

Reference Contaminant typeand initial concentration

ISCO treatment (lengthof treatment)

Conditions set for bioremediation(length of incubation)

Removal efficiency

Cassidy et al2009

24-Dinitrotoluene Ozone (48 h) Aerobic incubation (2ndash14 weeks) 9811450 mgkg Modified Fentonrsquos reagent

(one treatment)Amendment with NH4 and PO4

Iron-activated sodiumpersulfate (one treatment)

Jung et al 2005 Diesel Ozone (3ndash15 h) Aerobic incubation (9 weeks) gt50 exact value notreported2700 mgkg TPH

Kulik et al 2006 PAH Fentonrsquos reagent (24 h) Aerobic incubation (8 weeks) 75ndash94 (sand samples)

1419 mgkg(sand samples)

Ozone (2ndash5 h) 55ndash75 (peat samples)

2370 mgkg(peat samples)

Liang et al 2009 Crude oil Ozone (6 h) Aerobic incubation (18 weeks) 35ndash40 (ozone +bioremediation)28000 mgkg

(before ozonation)Amendment with nutrientsBioaugmentation

Palmroth et al2006a

PAH Modified Fentonrsquos reagent(4ndash10 days)

Aerobic incubation (5ndash16 weeks) 36ndash543960 mgkg

Palmroth et al2006b

PAH Modified Fentonrsquos reagent(10 days)


Tsai et al 2009a Fuel oil Fentonrsquos reagent (one treatment) Aerobic incubation (17 weeks) 47ndash755000 mgkg TPH Amendment with N P and carbon

source

Tsai et al 2009b Fuel oil Fentonrsquos reagent (one treatment) Aerobic incubation (17 weeks) 100 in 3 step process withflushing with surfactantISCO and bioremediation

1000 mgkg TPH

5000 mgkg TPH

10000 mgkg TPH

Valderrama et al2009

PAH Fentonrsquos reagent (05 h) Aerobic incubation(length unclear)

751203 mgkg

Amendment with nutrients

Bioaugmentation

Xie and Barcelona2003

Jet fuel Permanganate (25 days) Aerobic incubation (19 weeks) 15ndash80 dependent uponfraction of oil27 mgL TPH Hydrogen peroxide (25 days) Amendment with nutrients carbon

source and trace elementsMagnesium peroxide (oxygen-release compound) (25 days) Bioaugmentation


such as nutrient availability and the presence of a microbialpopulation acclimated to biodegradation

32 Nutrients and biodegradation in pre-oxidized soils

Nutrient amendment is a common approach to stimulatebacterial growth and may be necessary in lab experimentswith nutrient-poor samples without natural influx ofnutrient-rich groundwater Many batch experiments withISCO have been performed in a phosphate buffer whichsimultaneously controls the pH and provides phosphate tomicrobes (Cassidy et al 2009 Liang et al 2009Valderrama et al 2009) Ammonium may be added foranalytical reasons (Cassidy et al 2009) or in conjunctionwith ample trace metals minerals and vitamins to createoptimal conditions for biomass growth (Sahl et al 2007Xie and Barcelona 2003) In experiments in whichammonium and phosphate were either added to or absentfrom microcosms with fuel oil-spiked samples TPHremoval was 6ndash14 higher when nutrients were present(Tsai et al 2009a)

Although excess nutrients may improve bioremediationamendment may not always be necessary It has beensuggested that through oxidizing soil organic matterchemical oxidants actually release nutrients (Sirguey et al2008 Westersund et al 2006) Researchers investigatingthe impact of ISCO on subsequent plant growth found thatphosphate concentrations increase in soils oxidized witheither Fentonrsquos reagent or permanganate due to oxidationand release of soil organic matter (Sirguey et al 2008)Although ammonium concentrations increased up to 20-fold upon treatment with Fentonrsquos reagent overall concen-trations of nitrate and organic carbon decreased such

reductions in the availability of electron donors andacceptors as well as nutrients would have repercussionson biomass growth Kulik et al (2006) suggested thatincreased bioremediation in pre-oxidized peat as comparedto sand was due to the high nutrient content in peatFurther investigation is required to understand the relation-ships between soil type nutrient availability and dynamicsthereof following chemical oxidation

33 Bioaugmentation in pre-oxidized soils

Addition of bacterial cultures or enrichments frequentlyoccurs in laboratory experiments This occasionally takesplace prior to chemical oxidation in order to ensure properbacterial function Microbial populations are added afterISCO to re-inoculate lab experiments and arguably tosimulate the processes encountered in the field Howeverwork investigating bioremediation in pre-oxidized soils hasnot yet conclusively shown the necessity of bioaugmenta-tion In two recent studies experimental setups wereinoculated prior to ISCO treatment with either a dechlori-nating microbial culture to guarantee PCE degradationability (Sahl et al 2007) or a wastewater enrichment cultureto ensure sufficient biomass was available (Valderrama etal 2009) Both investigations saw successful regenerationof bioremediation activity under some of the experimentalconditions tested Other researchers investigated the influ-ence of cell number on PCE degradation (Buyuksonmez etal 1999) Here a culture of Xanthobacter flavus ahydrogen peroxide-resistant species known to degrade themajor by-product of Fentonrsquos reagent oxidation of PCE(dichloroacetic acid) was grown under oxidative stressprior to experimentation Although results did identify

Table 3 Summary of investigations on the feasibility and optimal conditions for combined chemical oxidation and anaerobic bioremediation

Reference Contaminant typeand initialconcentration

ISCO treatment(length of treatment)


Removal efficiency

Buyuksonmezet al 1999

Tetrachloroethene Fentonrsquos reagent (addedhourly for 5 h)

Anaerobic incubation (3 days) 17ndash743ndash9 mgL (setupdependent)

Amendment with nutrients traceelements and vitamins

Bioaugmentation

Hrapovic et al2005

Trichloroethene Permanganate(22 days)

Anaerobic incubation (290 days) Overall efficiency in terms of etheneproduction not reportedUnclear effluent

concentration of~500 mgL

Amendment with nutrients andcarbon sources Limited rebound of microbial

dechlorination following ISCO treatmentBioaugmentation

Addition of natural groundwater

Sahl et al2007

Tetrachloroethene Permanganate Anaerobic incubation (unclear) Overall efficiency in terms ofethene production not reported82ndash232 mgL

(column dependent)(17ndash610 h) Amendment with nutrients carbon

source trace elements Degradation of PCE to cis-DCE observed


optimal cell numbers associated with specific Fentonrsquosreagent dosages it would be nearly impossible to createsuch specific conditions in a field setting

Enrichments of indigenous soil microorganisms havebeen used for re-inoculation following chemical oxidationIn lab experiments where microcosms were autoclavedprior to ISCO to ensure that all contaminant removal couldbe attributed to chemical oxidation it was clear that re-inoculation was required to regenerate bioremediation (Xieand Barcelona 2003) The impact of bioaugmentation hasbeen less conclusive in other studies testing this as avariable in coupled chemical and biological remediation Inone case microbial community dynamics with or withoutaddition of an enriched mixed culture following ozonationof soil with an initial oil concentration of 56 mgg weremonitored on a microarray (Liang et al 2009) Althoughthere was slightly less residual TPH following treatmentnamely 17 mgg in the setup with added biomass versus18 mgg in the blank this could not be explained by asignificant difference in the amount or variety of genesmeasured by the microarray In permanganate-pre-oxidizedTCE-spiked samples no dechlorination was observedfollowing a variety of bioaugmentation steps with aninoculation of a TCE-degrading Dehalococcoides sp andother species able to respire on hydrogen and the carbonsource provided (Hrapovic et al 2005) However once thecolumn was flushed with site groundwater anaerobicconditions developed and cis-dichloroethene (DCE) wasdetected Thus it is not clear if bioremediation was initiatedby (1) biostimulation with specific nutrients present in thesite groundwater but not in synthetic groundwater (2) theintroduction of dehalogenating bacteria from the site or (3)the addition of a groundwater bacterial consortium able tocreate anaerobic conditions necessary for the activity ofcultured Dehalococcoides species In work focused oninvestigating bioremediation parameters an enrichmentculture or native sediment slurry was added to allexperimental setups (Lee et al 2008 Nam et al 2001)thus the impact of biomass addition could not be assessedClearly future work is required to judge both the necessityof and requirements for successful bioaugmentation in pre-oxidized soils in the lab in order to ascertain thetransferability of this technique to the field

4 Conclusions and future directions

Coupled ISCO and bioremediation is not only feasible butwhen properly implemented can provide more extensiverapid and cost-effective treatment than either chemical orbiological techniques alone Although pre-oxidationimpacts microbial communities and may adversely alterredox conditions chemical oxidation can stimulate biore-

mediation through improving bioavailability and biode-gradability of contaminant substrates providing oxygenand in some cases releasing nutrients In order to create abalanced and optimized treatment strategy a variety ofparameters within the chemical and biological remediationphases must be considered

ISCO regimens should be chosen and performed in amanner that minimizes microbial interaction with concen-trated chemical oxidants When a variety of chemicaloxidant types concentrations or injection strategies weretested heightened chemical mass removal was not associ-ated with overall increased efficiency This was due to thereduction in bioremediation potential from harsh chemicaltreatments Chemical oxidation can also be manipulated totarget the less biodegradable fraction of the contaminationleaving bioavailable oxidized by-products for microbialremediation Future investigations should focus on furtheroptimizing the chemical treatment to reduce microbialimpact and improve the ease of substrate biodegradationTo this end it is essential that experimentation include (1)more column setups which better recreate oxidant flowdynamics in the lab and (2) naturally aged samples withwhich the impact of field sorption of contaminants onto soilparticles can be assessed

Adjustment of redox conditions electron donors andelectron acceptors amendment with nutrients and addi-tion of bacterial cultures are techniques used to stimulatethe regeneration of microbial activity following ISCORedox conditions have been manipulated (in some caseswith chemical oxidants) to encourage specific aerobic oranaerobic biodegradation pathways Conclusive evidencefor the necessity andor success of bioaugmentationremains illusive As laboratory work with enrichedcultures under optimized conditions has proven to beinconclusive field application would obviously be evenmore challenging reliance on incomplete sterilization byISCO and a natural or geohydrologically enhanced re-inoculation by groundwater flow may be more feasiblestrategies Through providing an excess of electrondonors and acceptors rebound of biodegrading commu-nities may also be encouraged

In view of the fact that often the time required forremediation increases or that the efficiency decreaseswhen technologies are transferred from the laboratory tothe field a full understanding and optimization of theprocesses essential to sequential chemical and biologicaltreatment are required to ensure success in field applica-tions Future work should focus on the implications ofchemical oxidation on nutrient dynamics in a given soilmatrix and on the bacterial requirements for regenerationThrough concentrating on the aforementioned directionsresearch-based efficient and cost-effective biphasic treat-ment strategies can be designed Once tested in the lab


optimized coupled ISCO and bioremediation can then befurther developed as an effective remediation technologyin the field

Acknowledgments This research is funded by the European Unionconsortium Upsoil a Seventh Framework Programme within Theme6 number 226956 (wwwupsoileu) The authors would also like tothank two anonymous reviewers for their valuable comments

Open Access This article is distributed under the terms of theCreative Commons Attribution Noncommercial License which per-mits any noncommercial use distribution and reproduction in anymedium provided the original author(s) and source are credited

References

Adamson DT McDade JM Hughes JB (2003) Inoculation of DNAPLsource zone to initiate reductive dechlorination of PCE EnvironSci Technol 372525ndash2533

Aulenta F Majone M Tandoi V (2006) Enhanced anaerobicbioremediation of chlorinated solvents environmental factorsinfluencing microbial activity and their relevance under fieldconditions J Chem Technol Biotechnol 811463ndash1474

Aunola TA Goi A Palmroth MRT Langwaldt JH Tuhkanen TA(2006) Removal of PAHs from creosote oil contaminated soil byaddition of concentrated H2O2 and biodegradation J Adv OxidTechnol 911ndash19

Baird D Knight R (2008) Novel treatment approach in situ chemicaloxidation combined with enhanced aerobic bioremediation InProceedings of the sixth international conference on remediationof chlorinated and recalcitrant compounds Battelle Monterey ppD-012

Blondel J Nicolet P Jacquet RMichiels T (2007) Using dilute H2O2 forbioremediation of chlorinated phenols mass balance demonstratesthe results In Proceedings of the ninth international in situ and on-site bioremediation symposium Battelle Baltimore pp D-07

Bou-Nasr J Hampton D (2006) Comparative study of the effect offour ISCO oxidants on PCE oxidation and aerobic microbialactivity In Proceedings of the fifth international conference onremediation of chlorinated and recalcitrant compounds BattelleMonterey pp D-23

Brown RA Lewis R Leahy MC Luhrs RC (2009) In there life afterISCO The effect of oxidants on in situ bioremediation InProceedings of the tenth international in situ and on-sitebioremediation symposium Battelle Baltimore pp K-12

Buyuksonmez F Hess TF Crawford RL Watts RJ (1998) Toxiceffects of modified Fenton reactions on Xanthobacter flavusFB71 Appl Environ Microbiol 643759ndash3764

Buyuksonmez F Hess T Crawford R Paszczynski A Watts R (1999)Optimization of simultaneous chemical and biological minerali-zation of perchloroethylene Appl Environ Microbiol 652784

Cassidy D Hampton D (2009) Hydrogen sulfide production frompersulfate oxidationmdashimplications for remediation In Proceed-ings of the tenth international in situ and on-site bioremediationsymposium Battelle Baltimore pp K-15

Cassidy D Northup A Hampton D (2009) The effect of threechemical oxidants on subsequent biodegradation of 2 4-dinitrotoluene (DNT) in batch slurry reactors J Chem TechnolBiotechnol 84820ndash826

Chapelle FH Bradley PM Casey CC (2005) Behavior of achlorinated ethene plume following source-area treatment withFentonrsquos reagent Ground Water Monit Remediat 25131ndash141

Crimi ML Taylor J (2007) Experimental evaluation of catalyzedhydrogen peroxide and sodium persulfate for destruction ofBTEX contaminants Soil Sediment Contam 1629ndash45

Demque DE Biggar KW Heroux JA (1997) Land treatment of dieselcontaminated sand Can Geotech J 34421ndash431

EPA (1998) Field applications of in situ remediation technologieschemical oxidation In Solid waste and emergency responsesEPA Washington DC pp 37

Gallego JLR Loredo J Llamas JF Vazquez F Sanchez J (2001)Bioremediation of diesel-contaminated soils evaluation ofpotential in situ techniques by study of bacterial degradationBiodegradation 12325ndash335

Gates DD Siegrist RL (1995) In-situ oxidation of trichloroethyleneusing hydrogen-peroxide J Environ Eng 121639ndash644

Hoelen TP Cunningham JAHopkins GD Lebron CA ReinhardM (2006)Bioremediation of cis-DCE at a sulfidogenic site by amendment withpropionate Ground Water Monit Remediat 2682ndash91

Hoeppel RE Hinchee RE Arthur MF (1991) Bioventing soilscontaminated with petroleum hydrocarbons J Ind Microbiol8141ndash146

Hood E MacKinnon LK Bertrand D Major D Dennis P (2006)Evaluation of sequential application of chemical oxidation andbioaugmentation In Proceedings of the fifth internationalconference on remediation of chlorinated and recalcitrant com-pounds Battelle Monterey pp D-60

Hood ED Major DW Quinn JW Yoon WS Gavaskar A EdwardsEA (2008) Demonstration of enhanced bioremediation in a TCEsource area at Launch Complex 34 Cape Canaveral Air ForceStation Ground Water Monit Remediat 2898ndash107

Hrapovic L Sleep BE Major DJ Hood ED (2005) Laboratory studyof treatment of trichloroethene by chemical oxidation followedby bioremediation Environ Sci Technol 392888ndash2897

Huang K Hoag G Chheda P Woody B Dobbs G (1999) Kineticstudy of oxidation of trichloroethylene by potassium permanga-nate Environ Eng Sci 16265ndash274

Huang KC Zhao ZQ Hoag GE Dahmani A Block PA (2005)Degradation of volatile organic compounds with thermallyactivated persulfate oxidation Chemosphere 61551ndash560

Hunkeler D Aravena R Parker BL Cherry JA Diao X (2003)Monitoring oxidation of chlorinated ethenes by permanganate ingroundwater using stable isotopes laboratory and field studiesEnviron Sci Technol 37798ndash804

ITRC (2005) Technical and regulatory guidance for in situ chemicaloxidation of contaminated soil and groundwater InterstateTechnology and Regulatory Council In Situ Chemical OxidationTeam Washington

Jones A Escobar M Serlin C Sercu B Holden P Stollar R MurphyP (2009) Microbial community composition assessment during insitu chemical oxidation with permanganate In Proceedings ofthe tenth international in situ and on-site bioremediationsymposium Battelle Baltimore pp K-14

Jung H Ahn Y Choi H Kim IS (2005) Effects of in-situ ozonation onindigenous microorganisms in diesel contaminated soil survivaland regrowth Chemosphere 61923ndash932

Kao CM Wu MJ (2000) Enhanced TCDD degradation by Fentonrsquosreagent preoxidation J Hazard Mater 74197ndash211

Koch SA Rice JM Stolzenburg TR Baker K Haselow J (2007)Reversing full-scale ISCO In Proceedings of the ninth interna-tional in situ and on-site bioremediation symposium BattelleBaltimore pp G-06

Krumins V Park JW Son EK Rodenburg LA Kerkhof LJ HaggblomMM Fennell DE (2009) PCB dechlorination enhancement inAnacostia River sediment microcosms Water Res 434549ndash4558

Kubal M Janda V Benes P Hendrych J (2008) In situ chemicaloxidation and its application to remediation of contaminated soiland groundwater Chem Listy 102493ndash499


Kulik N Goi A Trapido M Tuhkanen T (2006) Degradation of polycyclicaromatic hydrocarbons by combined chemical pre-oxidation andbioremediation in creosote contaminated soil J Environ Manage78382ndash391

Ladaa T Tingle A Mayer R McInturff B Jerrard C Hodges JMorrissey D (2008) Phased full-scale remediation of a complex siteusing a treatment train of multiple technologies In Proceedings ofthe sixth international conference on remediation of chlorinated andrecalcitrant compounds Battelle Monterey pp D-002

Lee B Hosomi M (2001) A hybrid Fenton oxidationndashmicrobialtreatment for soil highly contaminated with benz(a)anthraceneChemosphere 431127ndash1132

Lee BT Kim KW (2002) Ozonation of diesel fuel in unsaturatedporous media Appl Geochem 171165ndash1170

Lee PKHMacbeth TW SorensonKS Deeb RAAlvarez-Cohen L (2008)Quantifying genes and transcripts to assess the in situ physiology ofldquoDehalococcoidesrdquo spp in a trichloroethene-contaminated ground-water site Appl Environ Microbiol 742728ndash2739

Lessard L Head M Glod C (2007) Gasoline and fuel oil remediationusing biologically enhanced chemical oxidation In Proceedingsof the ninth international in situ and on-site bioremediationsymposium Battelle Baltimore pp H-18

Liang YT Van Nostrand JD Wang J Zhang X Zhou JZ Li GH(2009) Microarray-based functional gene analysis of soil micro-bial communities during ozonation and biodegradation of crudeoil Chemosphere 75193ndash199

Luhrs RC Lewis RW Huling SG (2006) ISCOrsquos long-term impact onaquifer conditions and microbial activity In Proceedings of thefifth international conference on remediation of chlorinated andrecalcitrant compounds Battelle Monterey pp D-48

Macbeth T Peterson L Starr R Sorenson Jr K Goehlert R Moor K (2005)ISCO impacts on indigenous microbes in a PCE-DNAPL contami-nated aquifer In Proceedings of the eighth international in situ andon-site bioremediation symposium Battelle Baltimore pp D-22

Macbeth TW Goehlert R Moor K (2007) Effect of iterativepermanganate injections on indigenous microbes in a PCE-DNAPL contaminated aquifer In Proceedings of the ninthinternational in situ and on-site bioremediation symposiumBattelle Baltimore pp G-03

MacKinnon LK Thomson NR (2002) Laboratory-scale in situchemical oxidation of a perchloroethylene pool using permanga-nate J Contam Hydrol 5649ndash74

Major DW McMaster ML Cox EE Edwards EA Dworatzek SMHendrickson ER Starr MG Payne JA Buonamici LW (2002)Field demonstration of successful bioaugmentation to achievedechlorination of tetrachloroethene to ethene Environ SciTechnol 365106ndash5116

Malina G Grotenhuis JTC (2000) The role of biodegradation duringbioventing of soil contaminated with jet fuel Appl BiochemBiotechnol 8859ndash76

Marley MC Parikh JM Droste EX Lee AM Dinardo PM WoodyBA Hoag GE Chheda PV (2003) Enhanced reductive dechlo-rination resulting from a chemical oxidation pilot test In situ andon-site bioremediationmdash2003 In Proceedings of the SeventhInternational In Situ and On-Site Bioremediation SymposiumBattelle Orlando p A17

Masten SJ Davies SHR (1997) Efficacy of in-situ ozonation for theremediation of PAH contaminated soils J Contam Hydrol28327ndash335

Menendez-Vega D Gallego JLR Pelaez AI de Cordoba GF MorenoJ Munoz D Sanchez J (2007) Engineered in situ bioremediationof soil and groundwater polluted with weathered hydrocarbonsEur J Soil Biol 43310ndash321

Miller CM Valentine RL Roehl ME Alvarez PJJ (1996) Chemical andmicrobiological assessment of pendimethalin-contaminated soilafter treatment with Fentonrsquos reagent Water Res 302579ndash2586

Nam K Rodriguez W Kukor JJ (2001) Enhanced degradation ofpolycyclic aromatic hydrocarbons by biodegradation combinedwith a modified Fenton reaction Chemosphere 4511ndash20

Ndjoursquoou AC Bou-Nasr J Cassidy D (2006) Effect of Fenton reagentdose on coexisting chemical and microbial oxidation in soilEnviron Sci Technol 402778ndash2783

Northup A Cassidy D (2008) Calcium peroxide (CaO2)for use inmodified Fenton chemistry J Hazard Mater 1521164ndash1170

Ochs D Singh IP (2007) Alkaline peroxidation treatment fieldapplications for BTEX and MTBE treatment In Proceedings ofthe ninth international in situ and on-site bioremediationsymposium Battelle Baltimore pp C-49

Ormad P Puig A Sarasa J Roche P Martin A Ovelleiro JL (1994)Ozonation of waste-water resulting from the production oforganochlorine plaguides derived from DDT and trichloroben-zene Ozone Sci Eng 16487ndash503

Palmroth MRT Langwaldt JH Aunola TA Goi A Munster UPuhakka JA Tuhkanen TA (2006a) Effect of modified Fentonrsquosreaction on microbial activity and removal of PAHs in creosoteoil contaminated soil Biodegradation 17131ndash141

Palmroth MRT Langwaldt JH Aunola TA Goi A Puhakka JATuhkanen TA (2006b) Treatment of PAH-contaminated soil bycombination of Fentonrsquos reaction and biodegradation J ChemTechnol Biotechnol 81598ndash607

Pu XC Cutright TJ (2007) Degradation of pentachlorophenol by pureand mixed cultures in two different soils Environ Sci Pollut Res14244ndash250

Rivas FJ (2006) Polycyclic aromatic hydrocarbons sorbed on soils ashort review of chemical oxidation based treatments J HazardMater 138234ndash251

Sahl J Munakata-Marr J (2006) The effects of in situ chemical oxidationon microbiological processes a review Remed J 1657ndash70

Sahl JW Munakata-Marr J Crimi ML Siegrist RL (2007) Couplingpermanganate oxidation with microbial dechlorination WaterEnviron Res 795ndash12

Salanitro JP Johnson PC Spinnler GE Maner PM Wisniewski HLBruce C (2000) Field scale demonstration of enhanced MTBEbioremediation through aquifer bioaugmentation and oxygena-tion Environ Sci Technol 344152ndash4162

Scheutz C Durant ND Dennis P Hansen MH Jorgensen T JakobsenR Cox EE Bjerg PL (2008) Concurrent ethene generation andgrowth of dehalococcoides containing vinyl chloride reductivedehalogenase genes during an enhanced reductive dechlorinationfield demonstration Environ Sci Technol 429302ndash9309

Schnarr M Truax C Farquhar G Hood E Gonullu T Stickney B(1998) Laboratory and controlled field experiments usingpotassium permanganate to remediate trichloroethylene andperchloroethylene DNAPLs in porous media J Contam Hydrol29205ndash224

Semple KT Morriss AWJ Paton GI (2003) Bioavailability ofhydrophobic organic contaminants in soils fundamental conceptsand techniques for analysis Eur J Soil Sci 54809ndash818

Seol Y Zhang H Schwartz FW (2003) A review of in situ chemicaloxidation and heterogeneity Environ Eng Geosci 937ndash49

Siegrist RL Lowe KS Murdoch LC Case TL Pickering DA (1999)In situ oxidation by fracture emplaced reactive solids J EnvironEng 125429ndash440

Siegrist RL Urynowicz MA Crimi ML Lowe KS (2002) Genesis andeffects of particles produced during in situ chemical oxidationusing permanganate J Environ Eng 1281068ndash1079

Singh A (2009) Biological remediation of soil an overview of globalmarket and available technologies In Singh A Ward OP (eds)Advances in applied bioremediation Soil biology SpringerBerlin pp 1ndash19

Sirguey C Silva P Schwartz C Simonnot MO (2008) Impact ofchemical oxidation on soil quality Chemosphere 72282ndash289


Smith AE Hristova KWood IMackayDM Lory E LorenzanaD ScowKM (2005) Comparison of biostimulation versus bioaugmentationwith bacterial strain PM1 for treatment of groundwater contaminat-ed with methyl tertiary butyl ether (MTBE) Environ HealthPerspect 113317ndash322

Song DL Conrad ME Sorenson KS Alvarez-Cohen L (2002) Stablecarbon isotope fractionation during enhanced in situ bioremedi-ation of trichloroethene Environ Sci Technol 362262ndash2268

Straube WL Nestler CC Hansen LD Ringleberg D Pritchard PHJones-Meehan J (2003) Remediation of polyaromatic hydro-carbons (PAHs) through landfarming with biostimulation andbioaugmentation Acta Biotechnol 23179ndash196

Studer J Davis G Baldwin B Cronk G (2009) Impact of in situchemical oxidation on native biological populationsmdashreview ofcase studies In Proceedings of the tenth international in situ andon-site bioremediation symposium Battelle Baltimore pp K-13

Surridge A Wehner F Cloete T (2009) Bioremediation of pollutedsoil In Singh A Ward OP Kuhad RC (eds) Advances in appliedbioremediation Soil biology Springer Berlin pp 103ndash121

Tas N MHAv E WMd V Smidt H (2009) The little bacteria thatcanmdashdiversity genomics and ecophysiology of lsquoDehalococ-coidesrsquo spp in contaminated environments Microb Biotechnol3389ndash402

Teel AL Cutler LM Watts RJ (2009) Effect of sorption oncontaminant oxidation in activated persulfate systems J EnvironSci Health A Tox Hazard Subst Environ Eng 441098ndash1103

Tsai T Kao C Yeh T Lee M (2008) Chemical oxidation ofchlorinated solvents in contaminated groundwater review PractPeriod Hazard Toxic Radioact Waste Manag 12116ndash126

Tsai TT Kao CM Surampalli RY Chien HY (2009a) Enhancedbioremediation of fuel-oil contaminated soils laboratory feasi-bility study J Environ Eng 135845ndash853

Tsai TT Kao CM Yeh TY Liang SH Chien HY (2009b) Remediationof fuel oil-contaminated soils by a three-stage treatment systemEnviron Eng Sci 26651ndash659

Tsai TT Kao CM Yeh TY Liang SH Chien HY (2009c) Application ofsurfactant enhanced permanganate oxidation and bidegradation oftrichloroethylene in groundwater J Hazard Mater 161111ndash119

Tsitonaki A Petri B Crimi M Mosbaek H Siegrist RL Bjerg PL(2010) In situ chemical oxidation of contaminated soil andgroundwater using persulfate a review Crit Rev Environ SciTechnol 4055ndash91

Valderrama C Alessandri R Aunola T Cortina JL Gamisans XTuhkanen T (2009) Oxidation by Fentonrsquos reagent combinedwith biological treatment applied to a creosote-comtaminatedsoil J Hazard Mater 166594ndash602

Vella P Veronda B (1993) Oxidation of trichloroethylene acomparison of potassium permanganate and Fentonrsquos reagentIn 3rd international symposium chemical oxidation technologyfor the nineties Vanderbilt University Nashville pp 17ndash19

Volkering F Quist JJ van Velsen AFM Thomassen PHG Olijve M(1998) A rapid method for predicting the residual concentrationafter biological treatment of oil-polluted soil ConSoil ThomasTelford Edinburgh pp 251ndash259

Waddell J Mayer G (2003) Effects of Fentonrsquos reagent andpotassium permanganate application on indigenous subsurfacemicrobiota a literature review In Proceedings of the 2003Georgia Water Resources Conference University of GeorgiaAthens pp 23ndash24

Watts RJ Teel AL (2005) Chemistry of modified Fentonrsquos reagent(catalyzed H2O2 propagationsmdashCHP) for in situ soil andgroundwater remediation J Environ Eng 131612ndash622

Watts RJ Udell MD Rauch PA Leung SW (1990) Treatment ofpentachlorophenol-contaminated soils using Fentons reagentHazard Waste Hazard Mater 7335ndash345

Watts RJ Stanton PC Howsawkeng J Teel AL (2002) Mineralizationof a sorbed polycyclic aromatic hydrocarbon in two soils usingcatalyzed hydrogen peroxide Water Res 364283ndash4292

Westersund J Fernandes L Jones S Clought H (2006) Stimulatinganaerobic reductive dechlorination following chemical oxidationtreatment In Proceedings of the fifth international conference onremediation of chlorinated and recalcitrant compounds BattelleMonterey pp D-56

Wiberg KB Saegebarth KA (1957) The mechanisms of permanganateoxidation IV Hydroxylation of olefins and related reactions JAm Chem Soc 792822ndash2824

Wrenn BA Ma X King T Lee K Venosa AD (2007) Effect ofpotassium permanganate on the biodegradation of weatheredcrude oil from Indiana Harbor Canal In Proceedings of the ninthinternational in situ and on-site bioremediation symposiumBattelle Baltimore pp C-55

Xie GB Barcelona MJ (2003) Sequential chemical oxidation and aerobicbiodegradation of equivalent carbon number-based hydrocarbonfractions in jet fuel Environ Sci Technol 374751ndash4760


During an ISCO treatment chemical oxidants arepumped into the subsurface to oxidize organic pollutantsThis aggressive treatment removes source zone contami-nants either sorbed to soil organic matter or pure productpresent as nonaqueous phase liquids (Seol et al 2003Watts and Teel 2005) Typical treatments include Fentonrsquosreagent with hydrogen peroxide and ferrous iron the lessacidic modified Fentonrsquos reagent permanganate persulfateand ozone injection (Table 1) A number of review articlesprovide insight into the chemistry and proper application ofoxidation regimens (Gates and Siegrist 1995 Kubal et al2008 Rivas 2006 Seol et al 2003 Tsai et al 2008 Wattsand Teel 2005) ISCO has been successfully used to oxidizeand thus lower the concentration of petroleum-derivedhydrocarbons (total petroleum hydrocarbons TPH Crimiand Taylor 2007 Gates and Siegrist 1995 Huang et al 2005Jung et al 2005 Lee and Kim 2002) polyaromatic hydro-carbons (PAH Lee and Hosomi 2001 Masten and Davies1997 Nam et al 2001 Watts et al 2002) and chlorinatedhydrocarbons (Huang et al 1999 2005 Hunkeler et al2003 Northup and Cassidy 2008 Ormad et al 1994Schnarr et al 1998 Siegrist et al 1999 Vella and Veronda1993 Watts et al 1990) ISCO is a versatile remediationstrategy providing rapid and extensive removal of both lightand dense recalcitrant compounds in pure phase

Biological-based remediation technologies require lon-ger time spans than chemical oxidation techniques and aremore appropriate for the bioavailable plume section of acontaminated site (Singh 2009) Whereas fungi and plantsalike can mediate removal of recalcitrant compounds herewe focus on biodegradation by bacterial populations Theubiquity of hydrocarbon-utilizing bacteria indicates thatnatural attenuation that is the inherent biodegrading abilityof contaminated soils will in most cases occur withoutintervention (Surridge et al 2009) That said a number oftechnologies aim to increase the rate of bioremediationeither by increasing the bioavailability of contaminantsthrough the application of surfactants (Menendez-Vega etal 2007 Tsai et al 2009c Volkering et al 1998) or bycreating conditions ideal for general microbial growth andfor specific reactivity to a compound In the case ofpetroleum-based hydrocarbons these include biostimula-tion with nutrients (Gallego et al 2001 Menendez-Vega etal 2007) and electron acceptor addition for example bybioventing to provide oxygen to accelerate aerobic degra-dation pathways (Hoeppel et al 1991 Malina andGrotenhuis 2000) Microbial dechlorination of highlychlorinated compounds occurs under anaerobic conditionsThus stimulation includes the addition of an appropriateelectron donor and nutrients to create ideal (redox)conditions (Aulenta et al 2006 Hoelen et al 2006 Songet al 2002) Bioaugmentation with a bacterial enrichmentor culture able to break down the contaminant of interest

has been used to improve bioremediation of (chlorinated)hydrocarbon contaminants (Demque et al 1997 Pu andCutright 2007 Salanitro et al 2000 Smith et al 2005Straube et al 2003) This strategy is most commonly usedto accelerate conversion of tetrachloroethene (PCE) toharmless ethene through the addition of cultures enrichedwith Dehalococcoides spp the only bacterial group knownto perform the complete chain of metabolic halorespirationreactions to produce ethene (Adamson et al 2003 Hood etal 2008 Krumins et al 2009 Major et al 2002 Scheutz etal 2008 Tas et al 2009)

Conventional wisdom dictates that chemical oxidation isnot compatible with biological-based remediation techni-ques The oxidative stress increase or decrease in pH(persulfate and Fentonrsquos reagent respectively) and changein redox conditions caused by ISCO treatments significant-ly alter subsurface conditions and are toxic to microbialpopulations (Buyuksonmez et al 1998 Macbeth et al2007 Miller et al 1996) However recent work indicatesthat although chemical oxidation can temporarily reducemicrobial activity bacterial populations do regeneratecontaminant degradation ability both in the field (Jones etal 2009 Koch et al 2007 Ladaa et al 2008 Luhrs et al2006 Macbeth et al 2005 Studer et al 2009) and inlaboratory experiments (Aunola et al 2006 Hood et al2006 Kao and Wu 2000 Kulik et al 2006 Ndjoursquoou et al2006) In many cases it has been concluded that ISCOpretreatment appears to improve overall remediation by (1)decreasing the concentration of pollutants to levels lesstoxic for the soil biota (Chapelle et al 2005) (2) improvingbioavailability of the parent compound (Kulik et al 2006Miller et al 1996) (3) producing bioavailable andbiodegradable oxidized daughter compounds (Lee andHosomi 2001 Marley et al 2003 Miller et al 1996 Namet al 2001) or (4) providing oxygen for aerobic biologicaltransformation of contaminants (Kulik et al 2006) It hasrecently been suggested that as ISCO treatment is not ableto access and oxidize all residual contaminants biologicalpolishing is required to fully remediate a site (Cassidy et al2009)

This statement reflects the new direction of coupledchemical and biological treatment Previous reviews echoedthe ldquowait and seerdquo mentality common to earlier experi-ments where following chemical oxidation the regenera-tion of biomass was merely monitored without stimulation(Sahl and Munakata-Marr 2006 Waddell and Mayer 2003)However in the open system encountered in situ even localsterilization with chemical oxidants will eventually bereversed as groundwater upstream will always transportindigenous microorganisms (Brown et al 2009) Thisacceptance of microbial resilience is reflected in a recentshift in the literature toward more studies investigatingwhich parameters are essential to a biphasic remediation































0

20

40

60

80

100

Bio

only

101

201

401

601

Bio

only

KM

nO4

H2O2

MgO2

Bio

only

Ozo

ne

MFR

SPS

180 m

in

300 m

in

900 m

in

Rem

oval

Eff

icie

ncy (

)

Biological

Chemical

A DB C



























Removal efficiency

Cassidy et al2009











Palmroth et al2006a



Palmroth et al2006b




source


1000 mgkg TPH

5000 mgkg TPH

10000 mgkg TPH



751203 mgkg


Bioaugmentation
















Removal efficiency





Bioaugmentation

Hrapovic et al2005







Sahl et al2007

















References





























































































































0

20

40

60

80

100

Bio

only

101

201

401

601

Bio

only

KM

nO4

H2O2

MgO2

Bio

only

Ozo

ne

MFR

SPS

180 m

in

300 m

in

900 m

in

Rem

oval

Eff

icie

ncy (

)

Biological

Chemical

A DB C



























Removal efficiency

Cassidy et al2009











Palmroth et al2006a



Palmroth et al2006b




source


1000 mgkg TPH

5000 mgkg TPH

10000 mgkg TPH



751203 mgkg


Bioaugmentation
















Removal efficiency





Bioaugmentation

Hrapovic et al2005







Sahl et al2007

















References























































































































Removal efficiency

Cassidy et al2009











Palmroth et al2006a



Palmroth et al2006b




source


1000 mgkg TPH

5000 mgkg TPH

10000 mgkg TPH



751203 mgkg


Bioaugmentation
















Removal efficiency





Bioaugmentation

Hrapovic et al2005







Sahl et al2007

















References











































































































Removal efficiency





Bioaugmentation

Hrapovic et al2005







Sahl et al2007

















References












































































































References
































































































Efforts to improve coupled in situ chemical oxidation with bioremediation: a review of optimization...

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Transcript of Efforts to improve coupled in situ chemical oxidation with bioremediation: a review of optimization...