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STOTEN-21957; No of Pages 22

Science of the Total Environment xxx (2017) xxxxxx

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Advanced technologies for the remediation of


pesticide-contaminated soils
E. Morillo , J. Villaverde
Institute of Natural Resources and Agrobiology of Seville (IRNAS-CSIC), Av. Reina Mercedes, 10, Sevilla E-41012, Spain

H I G H L I G H T S G R A P H I C A L A B S T R A C T

Many soils impacted by pesticide pollu-


tion due to their increasing use world-
wide
Point-source or diffuse pollution dene
the selected technology.
The majority of scientic studies are
still at the lab-scale stage.
Lack of full-scale remediation technolo-
gies based on their complete degrada-
tion
Scaling up new technologies is needed
to know their real cost and efcacy.

a r t i c l e i n f o a b s t r a c t

Article history: The occurrence of pesticides in soil has become a highly signicant environmental problem, which has been in-
Received 25 October 2016 creased by the vast use of pesticides worldwide and the absence of remediation technologies that have been test-
Received in revised form 30 January 2017 ed at full-scale. The aim of this review is to give an overview on technologies really studied and/or developed
Accepted 3 February 2017
during the last years for remediation of soils contaminated by pesticides. Depending on the nature of the decon-
Available online xxxx
tamination process, these techniques have been included into three categories: containment-immobilization,
Editor: D. Barcelo separation or destruction. The review includes some considerations about the status of emerging technologies
as well as their advantages, limitations, and pesticides treated. In most cases, emerging technologies, such as
Keywords: those based on oxidation-reduction or bioremediation, may be incorporated into existing technologies to im-
Pesticides prove their performance or overcome limitations. Research and development actions are still needed for emerg-
Soil contamination ing technologies to bring them for full-scale implementation.
Remediation technologies 2017 Elsevier B.V. All rights reserved.
Pesticide availability

Contents

1. Fundamentals, history and general overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0


2. Technologies for soil pesticide remediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.1. Containment-immobilization technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

Corresponding author.
E-mail address: morillo@irnase.csic.es (E. Morillo).

http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
0048-9697/ 2017 Elsevier B.V. All rights reserved.

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
2 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

2.1.1. Containment technologies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0


2.1.2. Immobilization technologies. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.2. Separation technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.2.1. Soil washing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.2.2. Soil ushing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.3. Destruction technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.3.1. Chemical remediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.3.2. Biological remediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
2.4. Economic analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
3. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 0

1. Fundamentals, history and general overview will be treated in this chapter. As for the rest of organic contaminants,
technologies to treat pesticide-contaminated soils fall into two catego-
Agricultural production has increased dramatically during the last ries: containment-immobilization or treatment, and treatment technol-
decades to ensure the food supply of a population that is growing at a ogies fall into two different categories: separation and destruction.
vertiginous rate. Greatly enhanced agricultural production has been To reduce, eliminate, isolate or stabilize a pesticide, soil remediation
made possible due to an increase in the use of pesticides, which have be- technologies use physical, chemical, or biological processes. The selec-
come an important part of modern agriculture. Although pesticides use tion of appropriate technologies depends on several factors, such as
is an old practice, their development and use increased dramatically site characteristics and contamination (punctual or diffuse), concentra-
after the Second World War (Gavrilescu, 2005). According to the EPA tion and type of pesticides to be removed, and the end use of the con-
denition a pesticide is any substance or mixture of substances taminated media (Gavrilescu, 2009).
intended for preventing, destroying, repelling, or mitigating any pest Depending on the technology used, techniques for soil remediation
(insects, mice and other animals, unwanted plants (weeds), or microor- can be applied in three ways (Caliman et al., 2011): (I) In situ, the reme-
ganisms). Although pesticides constitute an important aspect of modern diation method is applied without excavating the soil and the contami-
agriculture, their excessive and persistent use results in damage farm- nants are treated on the place the contamination occurred; (II) on site,
land and causes serious soil pollution and deteriorated soil quality and contaminated soil is excavated, treated on site and returned to the orig-
environment. A large percentage of pesticides applied in agriculture inal location; (III) ex situ, contaminated soil is excavated and
never reach their target organisms (Niti et al., 2013). They are dispersed transported to another location for its treatment.
through soil, water and air, and detected in food for human consump- Remediation of organic pesticides can be done using any of the tech-
tion. In the case of soil-applied pesticides, their residues and metabolites niques developed for other organic pollutants with similar characteris-
can accumulate in the soil at unacceptable high levels. The potential im- tics (Castelo-Grande et al., 2010); however, in fact, only some specic
pacts of pesticides on the environment and human health have been techniques are really studied and/or developed for pesticides remedia-
now recognized by governments and the public. Remediating contami- tion due to the particular circumstances involved in soils contaminated
nated soils to protect human health and to achieve sustainable develop- by these compounds. Their contamination in the majority of soils is due
ment has become a desirable goal (Cheng et al., 2016). to diffuse pollution, and has to be treated in a different manner than in
In 1995, the United Nations Environment Programme Governing soils with point-source contamination. On the other hand, agricultural
Council recognized only 12 Persistent Organic Pollutants (POPs) due soil properties have to be maintained, and aggressive technologies
to their adverse effects on the environment and human health. A global used to remediate industrial polluted soils cannot be used for agricultur-
ban on these toxic compounds was placed, requiring taking measures to al soils. For this reason, the aim of the present manuscript is the actual-
eliminate or reduce the release in the environment of these POPs. Eight ization of literature about remediation of pesticide contaminated soils in
of these POPs were insecticides (endrin, heptachlor, mirex, toxaphene, the last years, and, therefore, the majority of references collected are
aldrin, chlordane, dieldrin and DDT), one of them was a fungicide from the last decade, and almost all referred exclusively to pesticides.
(hexachlorobencene, HCB), and the rest were dioxins (some of them
by-products in pesticide production), PCBs and PCDFs. As POPs, these
pesticides persist in the environment for long periods of time, are 2.1. Containment-immobilization technologies
toxic and biomagnify in the food chain (Ali et al., 2014). The signing of
the Stockholm Convention on Persistent Organic Pollutants took effect 2.1.1. Containment technologies
in May 2004. In this convention the previous list was expanded in Pesticide contamination of soils may result not only from agricultur-
2009 to include new POPs, being ve of them other organochlorine in- al processes, but also from manufacturing, handling, improper storage,
secticides: chlordecone, lindane, - and -hexachlorocyclohexane and and disposal of pesticides and wastes. In particular, environmental con-
pentachlorobencene. Endosulfans were included in 2011. This gives an tamination with organochlorine pesticides (OCPs) is widespread world-
idea of the importance of developing technologies to remediate pesti- wide because, with the signing of the Stockholm Convention, many OCP
cide contaminated sites such as soil, groundwater and aquifers, al- production factories close to cities were abandoned (Gauszkaa et al.,
though the present review will be focused only in soils. 2011). Most of these contaminated sites pose a threat to the environ-
ment and face urgent land use conversion (Li et al., 2008; Yang et al.,
2010; Ye et al., 2013). Due to specic properties of such pesticides, re-
2. Technologies for soil pesticide remediation mediation efforts at macroscale in those soils where OCPs were
manufactured or their waste disposed are based on containment-
As most of pesticide-contaminated soils contain complex mixtures immobilization technologies. Such techniques comprehend excavation
of different compounds rather than one single contaminant, their reme- and landlling both inside and outside the site, capping to limit inltra-
diation can be a complicated process. The majority of pesticides applied tion and leaching, as well as subgrade barriers to limit lateral plume mi-
in agriculture are organic compounds, therefore, only their remediation gration, and include engineering techniques to remove or isolate the

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 3

source of contamination. Barriers used to be amended with sorbents constitute an important carbon sink due to their stability to microbial
such as carbonaceous materials or organic-rich soils which additionally and chemical degradation. When produced from biological sources
binds the contaminant (Younas et al., 2013). and are added to soil, CM is often termed biochar (Kupryianchyk
This is the case of soils contaminated with the pesticides lindane and et al., 2016). The addition of biochar and other CM to soils and sedi-
DDT and their metabolites and isomers. Hexachlorocyclohexane (HCH) ments enhances the sorption of hydrophobic organic compounds
and its isomer (lindane) were among the most extensively used or- (HOC), playing an important role in controlling transport and bioavail-
ganochlorine pesticides, generating the world's largest POP stockpile, ability of organic contaminants. Pollutant sequestration depends upon
estimated at between four and seven million tons of wastes (Vijgen CM molecular (carbonized and non-carbonized fractions) and structural
et al., 2011; Fernndez et al., 2013). Although a containment cement (surface, pore, and bulk properties) characteristics, which in turn de-
or concrete wall is constructed to prevent the release of the pollutants pend on the CM starting material and on pyrolytic conditions
(Weber and Varbelow, 2013), in many cases traces of the contaminants (Khorram et al., 2016).
were detected in the groundwater and the surrounding soil (Usman Biochar is a carbon-rich solid made from agricultural crop residues,
et al., 2014). For example, a multilayered landll cover system was de- wood or waste via pyrolysis in the absence of oxygen. Although biochar
posited on top of a HCH/lindane landll in Hamburg, Germany, to was primarily introduced as a soil amendment for carbon sequestration,
cover and immobilize the hazardous wastes (Gtz et al., 2013), but reductions of greenhouse gas emissions, and improvement of soil fertil-
leaching from the landll continues to be a threat to the groundwater. ity (Diez et al., 2013a), it has attracted attention for its ability to reduce
Such disposal practices are unsustainable due to the risks of contamina- the bioavailability of pesticides (Martin et al., 2012; Mukherjee et al.,
tion of the food chain and ecosystems. These POPs will persist in land- 2016). Research dealing with this issue has increased in recent years
lls for many decades and possibly centuries due to their very slow or (Table 1). The impact of biochar in sorption and dissipation of pesticides
absent degradability. Over these extended time periods landll systems such as atrazine, terbuthylazine, pyrimethanil or bentazone has been
are likely to degrade, thus posing a risk of releasing large contaminant studied (Cao et al., 2009; Wang et al., 2010; Yu et al., 2009; Cabrera
loads to the environment. When this occurs, excavation of the waste et al., 2014). The irreversible adsorption of pesticides to soils has been
and associated contaminated soil and remediation of the site are carried demonstrated when using biochar as amendment (Yu et al., 2011)
out, and the nal destruction of the contaminant waste is frequently due to entrapment into biochar micropores, surface-specic adsorption
carried out in well-regulated incinerators (Lysychenko et al., 2015), and partitioning into condensed structures.
which is only possible in highly industrialized countries. Sopea et al. (2012) reported that the adsorption capacity for
These containment processes are considered as a type of waste dis- isoproturon on a soil amended with biochar was 5 times higher than
posal, because not a real remediation of the polluted site is reached, con- for the non-amended. Cabrera et al. (2011) observed a drastic increase
stituting only a provisional solution. In spite of this, they have been of in the adsorption of uometuron and MCPA in soil amended with 2%
great applicability because they appeared as the only possibility for (w/w) of some biochars made from different feedstocks. Adsorption
such highly polluted soils. None of the containment-encapsulation tech- was particularly increased using wood pellets (about 30 times higher
nologies are entirely satisfactory (Bini, 2009), and there is a need for for uometuron and up to 50 times for MCPA). However, the authors
continuous monitoring and careful supervision of these waste disposals observed an enhanced leaching of both herbicides after amendment
stockpiles. Nowadays, even in industrial countries, the regulatory with biochars containing soluble organic compounds. Martin et al.
framework for the management and control of POPs stockpiles, in gen- (2012) also observed that aging of biochars in the soil reduced their
eral, and pesticides stockpiles in particular, is not always effective and sorption capacity. The soil containing aged biochars over a 32 month pe-
appropriately implemented, and this is still a much wider problem in riod exhibited sorption-desorption properties similar to the control soil,
developing countries (Weber et al., 2015). while soils freshly amended showed an increase in herbicide sorption,
and desorption hysteresis was high.
2.1.2. Immobilization technologies The land management using organic green wastes and compost
Current remediation methods for removing contamination from soil from various origins as soil amendment to retain pesticides has also in-
which involve removing and processing a large amount of contaminat- creased. This practice is accepted as an ecological method to increase
ed soil are costly and time-consuming. These methods are not generally soil fertility and organic matter, preventing losses of pesticides from
applicable in agricultural elds because they can lead to problems such runoff or leaching due to increased pesticide immobilization by sorp-
as soil erosion, fertility loss or nutrient leaching. Therefore, for large tion, while allows the disposal of such wastes.
areas of contamination economical remediation approaches to reduce Additionally, benecial effects on soil biochemical properties and
risks and meet the requirements to protect human and ecological health microbiological parameters are reached, accelerating the dissipation
are needed. Such risks can be mitigated by reducing the bioavailability of pesticides in soil (Garca-Jaramillo et al., 2016). Lpez-Pieiro
of the contaminant and, thereby, a higher contaminant mass could be et al. (2013) studied the sorption and degradation of MCPA in soils
left in place, reducing the need for more expensive remediation actions amended with fresh composted and aged olive mill waste, observing
(Centofanti et al., 2016). The in situ application of an adsorbent amend- that the greater the amount and maturity of wastes applied, the
ment in contaminated soils is a new and cost-effective alternative for re- greater the retention of MCPA. However, they also observed that
mediation of pesticide-contaminated soils. MCPA could be easily desorbed if the amendment was not aged or
Adsorption is the rst process that takes place when pesticides are composted.
into contact with soil, affecting other processes such as leaching, bio- Also different organic residues from olive oil production were used
availability or toxicity against non-target organisms (Villaverde et al., by Garca-Jaramillo et al. (2014) to evaluate their effect on the leaching
2009). Organic amendments are usually used as an immobilization and immobilization of tricyclazole and bentazone. Tricyclazole was not
technology. According to Khorram et al. (2016), the use of organic detected in any of the leachates in the amended soil. The authors con-
amendments reduce bioavailabiliy due not only to binding of pesticides cluded that the sorption of dissolved organic matter from the amend-
to reduce their mobility into water resources and living organisms, but ments changed the physicochemical properties of the soil surface.
also due to the provided nutrients which stimulate plant growth and Centofanti et al. (2016) used biosolids compost and aged dairy manure
promote ecological restoration. Generally, carbonaceous materials amendments for risk mitigation of aged DDT, DDE and dieldrin residues
(CM) originated from biological matter are used because they require in an old orchard soil. The addition of waste material spent mushroom
minimal treatments before application to the soil. substrate (SMS) is also a promising strategy to optimize pesticide im-
Carbonaceous materials, often referred to as black carbon, are pro- mobilization and mitigate water pollution (Marn-Benito et al., 2009,
duced by incomplete combustion of fossil fuels and vegetation and 2013; lvarez-Martn et al., 2016).

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
4 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

Table 1
Selected reports on the use of immobilization technologies for remediation of pesticide-contaminated soils.

Pesticide Pesticide class Scale Contamination Reagent used/operation Results/pesticide removal Reference
in soil conditions

DDT, DDE, Dieldrin Organochlorine Laboratory Old orchard soil Dairy manure compost Dairy manure and Biosolids composts Centofanti et al.
insecticides (aged N 50 years) (5%) lowered bioavailability by 1839%. Biochar (2016)
Biosolids compost (5%) was ineffective.
Pine chip Biochar (5%)
Terbuthylazine Triazine herbicide Laboratory Articially Biosolids (1%) Biosolids: limited effect on adsorption Wang et al.
contaminated Sawdust and charcoal Sawdust Biochar: 63 times higher adsorption (2010)
Biochars (1%) Charcoal Biochar: 3 times higher adsorption
Acetamiprid Neonicotinoid Laboratory Articially Eucalyptus wood chips Dissipation decreased up to 31.5% in the soil Yu et al. (2011)
insecticide contaminated biochar (0.5%) with the lower OM content
Carbofuran Carbamate and Laboratory Articially Eucalyptus wood chips Chlorpyrifos and carbofuran bioavailability Yu et al. (2009)
chlorpyrifos organophosphate contaminated biochar (0.11%) decreased about 89% and 75% using biochar
insecticides at 1%.
Aminocyclopyrachlor Unclassied and Laboratory Articially Three biochars (10%) Increased retention up to 240% of Cabrera et al.
bentazone Benzothiazinone contaminated Aminocyclopyrachlor and up to 40% of (2014)
herbicides bentazone with one of the biochars
Isoproturon Urea herbicide Laboratory Articially Eucalyptus wood chips Mineralization reduced by 13, 40 and 50% at Sopea et al.
contaminated biochar (0.12%) 0.1%, 1% and 2% of biochar (2012)
Diuron Phenylurea and Laboratory Articially Poultry litter (PL) and 25 fold increase in sorption. Aging of Martin et al.
Atrazine triazine herbicides contaminated paper mill sludge (PM) biochars over 32 months reduced the (2012)
biochars (1%) sorption by 47% (PM) to 68% (PL) for diuron.
Bentazone Benzothiazinone Laboratory Articially Composted alperujo (CA) 3 fold increase in sorption for soil + BA. CA Garca-Jaramillo
Tricyclazole herbicide and contaminated and biochar from CA (BA) was ineffective for increased sorption et al. (2014)
triazolobenzothiazole (2%)
fungicide
MCPA Aryloxyalkanoic acid Laboratory Articially Composted and eld-aged Leaching losses of MCPA reduced by up 39% Lpez-Pieiro
herbicide contaminated olive mill waste (COW, and 53% in the COW- and AOW-amended et al. (2013)
AOW) (5%) soils
Tebuconazol Triazol fungicides Laboratory Articially Spent mushroom Adsorption increased 1.4023.1, 1.0823.7, lvarez-Martn
Triadimenol (2), cyanoacetamide contaminated substrate (SMS) (275%) 1.3142.1, and 0.5523.8 times for et al. (2016)
Cymoxanil oxime fungicide, tebuconazole, triadimenol, cymoxanil and
Pirimicarb carbamate insecticide pirimicarb for soils amended with
biosorbent.
Linuron Urea herbicide Laboratory Articially Sewage sludge (SS), grape Leaching reduced up to 65.6% for amendment Marn-Benito
Diazinon Organophosphate contaminated marc (GM) and spent incubated 1 month, and up to 53.5% after et al. (2013)
Myclobutanil insecticide mushroom substrate 1 year aging.
Triazole fungicide (SMS) (5%)
Penconazole Triazole and Pilot Articially Fresh and composted Enhanced adsorption of both fungicides (up Marn-Benito
Metalaxyl Phenylamide (undisturbed contaminated spent mushroom to 24-fold). Increased degradation of et al. (2009)
fungicides soil cores) substrate (SMS) added to metalaxyl after 77 d incubation, but not of
agricultural soils (25 tons penconazole.
ha1)

Biochar and organic green wastes and compost from various ori- 2.2.1. Soil washing
gins have demonstrated to be good physicochemical methods to im- Soil washing is an ex-situ remediation technique that uses liq-
mobilize pesticides, but they could act as a new source of pollution. uids, usually aqueous solutions of different kinds of extractants (or-
Taking into account that they can be altered due to aging, the envi- ganic compounds, acids, tensioactives, etc.), to remove chemical
ronmental fate of retained pesticides should be tested over the pollutants from soils. The excavated contaminated soil is mixed
years. In the case of biochar, its characteristics vary widely with the with the water containing extractants in an extractive unit and agi-
use of different biomass materials and pyrolysis conditions, and it tated. After washing, soil particles are allowed to settle out, and the
is important to check previously if any specic biochar could be suit- washing solutions can be separated and regenerated or sent to land-
able for remediation purposes and its application rate and frequency ll. The extraction of pesticides from soils has been studied in a wide
of biochar amendments to reach an optimal remediation. To date, as variety of papers, but few studies have focused on the regeneration
it can be observed in Table 1, the applications of biochar and organic of the washing solution. Soil washing is most appropriate for soils
green wastes for the remediation of contaminated soil have mainly that contain at least 50% sand and gravel. Table 2 shows some results
been conducted in the laboratory, greenhouses or small plot experi- obtained by using soil washing technologies for remediation of
ments. Large-scale eld trials are needed before operational scale re- pesticide-contaminated soils.
mediation projects are implemented.
2.2.1.1. Solvents. The solvent used is chosen depending on the type of
pollutant to be extracted. Ye et al. (2013) applied several organic sol-
2.2. Separation technologies vents as a remediation technique for OCP-contaminated soils and stud-
ied the effect of factors such as solvent concentration, contact time and
Remediation of many pesticide-contaminated soils is often limited temperature, mixing speed, or solution to soil ratio. The use of thermal
by their persistence and recalcitrance, decreasing their availability to desorption techniques and solvent washing approaches using n-
be treated by different destruction methods. In those cases the contam- alcohols and surfactants have been studied by Gao et al. (2013) to reme-
inant has to be removed from the host medium. diate OCPs-contaminated soils. N 90% of ethanol used could be

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 5

Table 2
Selected reports on the use of soil washing technologies for remediation of pesticide-contaminated soils.

Pesticide Pesticide class Scale Contamination Reagent used/operation Results/pesticide Reference


in soil conditions removal

BHC, DDT Organochlorine Laboratory Abandoned Thermal desorption (225-500o) Ethanol at 1:20 Gao et al. (2013)
fungicide and OCPs and solvent washing (n-alcohols soil:solvent ratio gave
insecticide manufacturing and surfactants) 87% OCPs removed
plant
DDTs, cis-chlordane, trans-chlordane, Organochlorine Laboratory Four ethanol, 1-propanol, petroleum 8090% OCPs removed. Ye et al. (2013)
mirex insecticides abandoned ether fractions Better parameters:
pesticide petroleum ether, soil:
factories solvent ratio 1:10, 50 C.
Aldicarb Carbamate Laboratory Articially Anionic (SDBS), cationic (HTAB) Best desorption Xu et al. (2006)
insecticide contaminated and non-ionic (OP) surfactants efciency with
anionic-nonionic
surfactant mixture
(77%).
2,4-D Alkylchlorophenoxy Laboratory Articially Sodium dodecyl sulfate (SDS) at Up to 89% 2,4-D Bandala et al.
herbicide contaminated 0.5%. removed. Complete (2013)
removal of pesticide and
surfactant from
wastewater using a
photo-Fenton process.
Methyl parathion (MP) Organophosphate Laboratory Articially 9 synthetic surfactants and 6398% of MP removed. Torres et al. (2012)
insecticide contaminated 3biosurfactants The best results obtained
using biosurfactants:
locust bean, guar,
mesquite gums.
DDT (and DDE) Organochlorine Laboratory Abandoned Triton X-100 66% DDT and 80% DDE Villa et al. (2010)
insecticide pesticide removed for three
factory sequential washings. 99
and 95% degradation of
DDT and DDE in
wastewater using a
photo-Fenton process.
DDT Organochlorine Laboratory Articially Tween 80, Brij 35, SDBS; in batch Better results: Batch, Rios et al. (2013)
insecticide contaminated and soil columns 18.5% with 2% Brij
35 + 0.5% SDBS +0.5%
EtOH./columns, 99.7%
with 2% Brij 35 + 1%
SDBS at very low
leaching rate
DDT (and DDE, DDD) Organochlorine Laboratory Long term Tween 80 + biostimulation with 94% DDT reduction only Betancurt-Corredor
insecticide contaminated nutrients with biostimulation, and et al. (2015)
agricultural 79% with Tween 80 +
soil biostimulation due to an
increasing toxicity.
Atrazine Triazine herbicide Laboratory Articially Sodium dodecyl sulfate (SDS) 99% removal of atrazine Dos Santos et al.
contaminated (0.010.5%) can be attained with (2015)
0.5 g surfactant/kg soil.
Total depletion of
atrazine in wastewater
using electrolysis with
diamond electrodes.
PCP Organochlorine Laboratory Articially Triton X-100 (1%) and 85% removed by Mulligan and
pesticide contaminated rhamnolipid (1%), both in the Triton-X100 (60% by Eftekhari (2003)
form of foam volatilization, 60%
removed by rhamnolipid
40% by volatilization)
Lindane (and their HCH isomers) Organochlorine Laboratory Articially Rhamnolipid, sophorolipid and 3050% enhanced Manickam et al.
insecticide contaminated trehalose-containing lipid degradation of lindane (2012)
and HCH isomers.
Sophorolipid offered
highest degradation
Lindane Organochlorine Laboratory Articially Rhamnolipids + citric acid 85.4% lindane desorption Wan et al. (2015)
insecticide contaminated from soil using 1%
rhamnolipids
+0.1 mol L1 citric acid
Norurazon Pyridazinone Laboratory Articially -Cyclodextrin (-CD) six soils Desorption depends on Villaverde et al.
contaminated with different characteristics the soil. With low (2005)
amount of NFL adsorbed,
desorption range
25100% with -CD
0.01 M, and 242% with
Ca(NO3)2 0.01 M
Acetochlor, alachlor, metolachlor, Chloroacetamide Laboratory Articially -CD, -CD, -CD, HP--CD, HP--CD and Flaherty et al.
dimethenamid, 2,4-D, dicamba, (4), contaminated methyl--CD, sulfated--CD, and methyl--CD displayed (2013)

(continued on next page)

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
6 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

Table 2 (continued)

Pesticide Pesticide class Scale Contamination Reagent used/operation Results/pesticide Reference


in soil conditions removal

propanil, Diazinon alkylchlorophenoxy carboxymethyl--CD the greatest levels of


(1), benzoic acid extraction enhancement
(1), anilide (up to 94%). -CD, -CD,
(1) herbicides, and -CD produced insoluble
organophosphate complexes.
insecticide (1)
DDTs, endosulfans, Organochlorine Laboratory Abandoned Methyl--cyclodextrin (0150% After four successive Ye et al. (2014a)
1,2,3,4,5,6-hexachlorocyclohexanes, pesticides pesticide w/w) + ultrasonication washing cycles the
heptachlors, and chlordanes factory removal efciency for
total OCPs were about
99% using 25 g L1 MCD
and 100 mL L1
sunower oil, 50 C.
Mirex, endosulfans and chlordanes. Organochlorine Laboratory Abandoned carboxymethyl--cyclodextrin + 94.7%, 87.2% and 98.5% Ye et al. (2014b)
pesticides pesticide ultrasonication at 60 C extraction for Mirex,
factory endosulfans and
chlordanes, respectively.
Cd and Pb were also
extracted.
DDTs, dieldrin, chlordanes, Organochlorine Laboratory Farm soil HP--CD Optimized extraction at Wong and
endosulfans pesticides highly HPCD:soil mass ratio of Bidleman (2010)
contaminated 5.8. About 3040% of
with OCs each OCP extracted.
DDTs Organochlorine Laboratory Articially HP--CD The amounts of Gao et al. (2015)
insecticide and contaminated HPCD-extractable
metabolites p,p'-DDT and o,p'- DDT
was similar to the
amounts biodegraded:
4580%, depending on
the soil and aging time
(20 or 100 days).
Hexachlorobencene (HCB) Organochlorine Laboratory Articially Methyl--cyclodextrin The combination Wan et al. (2009)
fungicide contaminated (MCD) + ethanol MCD/ethanol (30%) gave
the best results

recovered. However, there are several factors that limit the applicability biodegradation when using Tween 80 plus biostimulation than when
of this extraction process, such as the extraction of organically bound only biostimulation was used.
metals together with pesticides, the low effectivity of the solvent extrac- Organic solvents and many synthetic surfactants have the disadvan-
tion on very high molecular weight pesticides, or the toxicity of the sol- tage of being toxic to resident microbial population. In the case of sur-
vent to the soil microbial population (Pavel and Gavrilescu, 2008). factants, they use to form high-viscosity emulsions difcult to remove
These are perhaps the reasons for the few studies using solvents as from soil due to their low water-solubility, and sometimes the adsorp-
extractants in the last years, particularly in the case of pesticide polluted tion of surfactants onto soils is high. Due to the environmental risk
soils. posed by solvents and chemosynthetic surfactants, an alternative is
the use of biogenic compounds such as biosurfactants.
2.2.1.2. Synthetic surfactants. Surfactants are compounds that lower
the surface tension (or interfacial tension) in aqueous solutions,
enhancing the solubilization of persistent environmental pollut- 2.2.1.3. Biosurfactants. Biosurfactants are biocompatible and favorable to
ants in the soil. Industrially synthesized surfactants include chem- the subsequent utilization of soils and, therefore, more ecologically ac-
ically ethoxylated alcohols, sulphonates, Triton, Brij 35 and ceptable in the bioremediation of pesticide-contaminated soils
sodium dodecyl benzene sulphonate (SDBS), among others (Mao (Mulligan, 2009). A wide range of bacteria capable of producing
et al., 2015). biosurfactants have been proposed. The biosurfactants commonly
Villa et al. (2010) chose the non-ionic surfactant TX-100 for remedi- used for soil remediation include glycolipid (e.g., rhamnolipids, fructose
ation of a soil contaminated by DDT and DDE, and the wastewaters lipids, sophorolipids) and lipopeptide (e.g., surfactin, polymyxin)
obtained from the washing experiments were treated using a solar compounds. In particular, the feasibility of rhamnolipid biosurfactants,
photo-Fenton processes. Bandala et al. (2013) also used Fenton and mostly produced by Pseudomonas aeruginosa, to remove pesticides
Fenton-like processes for treating wastewater from washing with sodi- from soil has been studied. Wan et al. (2015) used rhamnolipids
um dodecylsulfate (SDS) a soil articially contaminated by 2,4-D, combined with citric acid to remove simultaneously lindane, lead and
scaling-up parameters for site restoration process. Dos Santos et al. cadmium from soils. Biosurfactants not only have the capability of
(2015) used the surfactant SDS for atrazine removal from soil, and the desorbing and dissolving contaminants, but also facilitate the
resulting washing waste was treated by electrolysis with a boron- biodegradation of contaminants. The effect of several biosurfactants
doped diamond electrode. Surfactants are also used to increase the bio- (rhamnolipid, sophorolipid and trehalose-containing lipid) on solubili-
availability of pesticides to be degraded by soil microorganisms. In the zation and biodegradation of HCH and their isomers in soil was studied
paper from Torres et al. (2012) the removal of methyl parathion using by Manickam et al. (2012), indicating that sophorolipid offered highest
anionic, non-ionic, cationic and natural surfactants was studied, and degradation and enhanced solubilization. Odukkathil and Vasudevan
wastewater was biologically treated. However, surfactants present the (2015) observed an enhanced bioavailability of endosulfan and its me-
disadvantage that they could be used as a substrate for microorganisms tabolite when using biosurfactant-producing bacterial strains. Even
or have toxic effects when using at high concentrations (Laha et al., though further research regarding the behavior of biosurfactant in the
2009). Betancurt-Corredor et al. (2015) observed reduced DDT fate and transport of soil contaminants is still required, biosurfactant

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 7

appears as an attractive choice for surfactant-based soil remediation etc.), electrochemical processes (water oxidation and reduction, etc.),
technology. chemical processes (ion exchange, dissolution of precipitates, etc.) and
electrokinetic transport processes (electro-osmosis, electromigration,
2.2.1.4. Cyclodextrins. Cyclodextrins (CDs) have been proposed also as an electrophoresis, etc.), which signicantly change the soil (Rodrigo
alternative to organic solvents and synthetic surfactants for the removal et al., 2014). Such processes favour the transport and removal of pollut-
of hydrophobic contaminants from soils (Fenyvesi et al., 2009). The ad- ants from soils. This technology is particularly useful for ne-grained
vantage of using CDs as extractants is their low environmental impact. soils with low hydraulic conductivities and large specic surface areas,
CDs have been approved as non-toxic compounds that do not harm res- and it is capable of treating ne and low-permeability materials.
ident microbial populations. In addition, due to their glucose-based As a model ionic pollutant, the removal of the anionic herbicide 2,4-
composition, CDs are considered biodegradable, although some CDs D has been widely studied. Souza et al. (2016) observed 90% removal of
are resistant at least a few months (Fenyvesi et al., 2005). 2,4-D using electrokinetic soil ushing, and Risco et al. (2016) studied
CDs are widely used in pharmaceutical science, but, due to the low the inuence of the arrangement of electrodes in the soil to obtain in-
production cost of some of them, they have gained considerable atten- creasing amounts of 2,4-D removal. Ribeiro et al. (2011) observed that
tion in many other elds, such as nanocomposite technologies, chroma- electrokinetic processes could efciently remove molinate and
tography, biotechnology, and agriculture (Morillo, 2006). Recently, CDs bentazone from soils, and it was related to the differential pH values be-
have been used to improve the remediation efciency of contaminated tween both electrodes. Vieira dos Santos et al. (2016) used EKSF to re-
soil, because they can increase the apparent water solubility of low- mediate a soil spiked with four herbicides, demonstrating that
polarity organic compounds (Morillo et al., 2012), reducing their sorp- efciency depended on the chemical characteristic of the pesticide.
tion to soil (Snchez-Trujillo et al., 2013, 2014). This transfer of the con- In a study with kaolinite and humic acid-kaolinite complexes spiked
taminants into the soil solution is an important way of increasing the with diuron, results showed that the electrokinetic removal efciency of
subsequent efciency of soil remediation by chemical oxidation or bio- diuron decreased from 90 to 35% in the presence of humic acids (Polcaro
degradation (Gruiz et al., 2011; Morillo et al., 2014). et al., 2007). These results have important implications for the applica-
CDs used as pesticide complexation agents have gained much atten- tion in real soils, where most of pesticides tend to be strongly adsorbed
tion in recent years. Many of these studies have only determined the in- on the soil organic matter. In such cases, their extraction has to be car-
creasing solubility and complexation constants between specic ried out using enhanced electrokinetic techniques (Karagunduz, 2009;
pesticides with a variety of CDs (Orgovnyi et al., 2009; Yez et al., Gomes et al., 2012). The integration of EKSF with chemical oxidation, es-
2012), but increasingly more studies can be found indicating the capac- pecially Fenton's process, is a widely accepted technique to increase the
ity of CDs for soil remediation based on their extractant ability and degradation of organic compounds in soil. Bocos et al. (2015) used the
subsequent soil washing of a wide variety of pesticides, such as the her- electrokinetic-Fenton treatment to remediate a soil polluted with the
bicide norurazon (Villaverde et al., 2005, 2006), hexachlorobenzenes pesticide pyrimethanil and PAHs, evaluating also the effect of several
(Wan et al., 2009), other organochlorine pesticides (Wong and complexing agents. Surfactants have been used to bring DDT into soil
Bidleman, 2010; Mao et al., 2013; Ye et al., 2014a), 2,4-D, alachlor, solution (Karagunduz et al., 2007). Li et al. (2011) used permeable reac-
metolachlor, acetochlor, dimethenamid, dicamba, and propanil tive barriers (PRB) lled with Pd/Fe particles installed between anode
(Flaherty et al., 2013). The enhanced extraction from soils facilitates and cathode to reach the dechlorination of PCP during its EKSF move-
subsequent phytoremediation (Ye et al., 2014b), oxidation (Villaverde ment. Its distance from anode and decreased pHs were important fac-
et al., 2007) or biodegradation (Villaverde et al., 2012; Gao et al., tors to increase removed PCP. Also Wan et al. (2010) used EKSF
2015; Zhao et al., 2015). coupled with Pd/Fe particles to remediate hexachlorobenzene-
Although research studies using CDs to extract pesticides by soil contaminated soil using a surfactant as solubility-enhancing agent. Vol-
washing are mainly carried out at a laboratory scale, high desorption atilization presents a major signicance in the application of electroki-
yields with very low CD concentrations can be obtained with those pes- netic techniques to polluted soils (Risco et al., 2016; Vieira dos Santos
ticides which form strong inclusion complexes. However, in those soils et al., 2016; Lpez-Vizcano et al., 2017).
that present an extremely high pesticide adsorption, higher amounts of Most of the EKSF research works analyzed is based on spiked soils
CDs should be used. The results obtained indicate the potential use of and the successful results obtained cannot always be transferred direct-
CDs for remediation of pesticide-contaminated soils. ly to soils sampled at polluted sites. The relative rareness of data avail-
able for real contaminated soils may reect the challenges involved in
2.2.2. Soil ushing transferring this technology into the eld. Further research is needed
In-situ soil ushing using extractant eluents with additives that en- since technical and environmental issues will require a careful evalua-
hances contaminant solubility is another strategy for soil remediation. tion for further full-scale implementation. These include controlling
Flushing solutions are injected into the area of contamination via side effects during treatment (such as anodic precipitation, oxidation
injection wells. The soil contaminants are mobilized by solubilization of the conditioning agent and generation of toxic gases), as well as eval-
or chemical interactions. Surfactants or solvents are frequently used uating the potential ecotoxicological effects of the surfactants, co-
as additives. After passing through the contamination zone, the solvents, oxidants or reductants used.
contaminant-bearing uid is collected and brought to the surface for
disposal, recirculation, or on-site treatment and reinjection. The effec- 2.3. Destruction technologies
tiveness of this process is dependent on hydrogeologic variables
(e.g., type of soil, soil moisture) and the type of contaminant. This tech- 2.3.1. Chemical remediation
nique has been scarcely used for pesticides remediation in the tradition- A variety of reactions, such as ionization, hydrolysis or oxidation-
al pump-and-treat type technology, such as that used in the reduction, usually related to the pH value, take place when chemical
remediation of phosalone (Di Palma, 2003) and atrazine (Di Palma degradation or abiotic degradation occurs. In general, the technologies
et al., 2003) (Table 3). This technique is not in use at present for reme- based on chemical reactions use to take place ex situ, but the application
diation of pesticide-contaminated soils, but, nevertheless, electrokinetic of some of them can be in situ or on site. Table 4 shows some results ob-
soil ushing (EKSF) is one of the most promising technologies for pesti- tained by using chemical technologies for remediation of pesticide-
cides soil remediation, especially when the pesticides are ionic species. contaminated soils.
In electrokinetic soil ushing a current electric eld is applied across
the soil using electrodes located in the subsurface. This current simulta- 2.3.1.1. Chemical reduction. In redox reactions one reactant loses elec-
neously initiates many physical processes (heating, changes in viscosity, trons (is oxidized) and the other gains electrons (is reduced). Reducing

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
8 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

Table 3
Selected reports on the use of soil ushing technologies for remediation of pesticide-contaminated soils.

Pesticide Pesticide class Scale Contamination Reagent used/operation conditions Results/pesticide removal Reference
in soil

Phosalone Organophosphate Laboratory Articially Ethanol aqueous solution (510%), 99% extraction efciency with 7 PV Di Palma
insecticide contaminated several pHs and temperatures. extraction volume and 10% ethanol (2003)
Solution ow rate 0.15 L hr.1 concentration. Hydrolysis treatment of the
extracting solution
Atrazine Triazine herbicide Laboratory Articially Ethanol aqueous solution 5% 95% extraction efciency with 15PV Di Palma et al.
contaminated extraction volume. Fenton's oxidation on the (2003)
extracted solution achieved only 21%
atrazine degradation.
2,4-D Alkylchlorophenoxy Laboratory Articially Electrokinetic soil ushing (EKSF) on 2,4-D moved towards the bacteria. 87.1% Jackman et al.
herbicide contaminated sterilized silt soil. Addition of removed from the soil, 5.8% recovered as (2001)
Burkholderia spp. RASC c2 CO2.
DDT Organochlorine Laboratory Articially EKSF in soil columns using No ushing with Tween 80 due to its Karagunduz
insecticide contaminated surfactants. adsorption on the soil. Much better results et al. (2007)
with SDBS.
HCB Organochlorine Bench-scale Articially EKSF using Pd/Fe permeable reactive 60% HCB removed by EK-PRB versus 13% Wan et al.
fungicide plants contaminated barrier (PRB) and Triton X-100 with EK alone (2010)
Molinate Thiocarbamate and Laboratory Contaminated EKSF in three soils. Changing current Mobilization of pesticides from soils and Ribeiro et al.
Bentazone Benzothiazinone agricultural intensity, pH (36) and ow rate removal from soil solution towards both (2011)
herbicides soils (rice (1.45 ml min1) electrodes (bentazone) or only to cathode
crops) (molinate)
PCP Organochlorine Laboratory Articially EKSF in soil columns using Pd/Fe 49% PCP removed, 22.9 recovered as phenol Li et al. (2011)
pesticide contaminated permeable reactive barrier (PRB)
Pyrimethanil Anilinopyrimidine Laboratory Articially EKSF-Fenton treatment using 58 and 100% degraded after 27d without and Bocos et al.
fungicide contaminated complexing agents (ascorbic acid, with citric acid pH 5 as complexing agent, (2015)
citric acid, oxalic acid and EDTA) and respectively.
H2O2 as ushing agent.
2,4-D, Alkylchlorophenoxy, Bench-scale Articially EKSF. Water used as ushing uid. 95, 60, 80, 80% 2,4-D, oxyuorfen, Vieira dos
oxyuorfen, Diphenyl ether, plants contaminated SDS used as solubilizing agent for chlosulfuron, atrazine removed from soil, Santos et al.
chlosulfuron, Sulfonylurea and oxyuorfen and atrazine respectively, but 60, 40, 65 and 60% due to (2016)
atrazine Triazine herbicides evaporation.
2,4-D Alkylchlorophenoxy Pilot plant Articially EKSF. Two different electrode With one conguration 70% 2,4-D removed Risco et al.
herbicide (175 dm3) contaminated congurations. from soil in 35 days. With the other, 8% in (2016)
58 days.
Commercial Alkylchlorophenoxy, Pilot plant Articially EKSF. Compare results with those Electric heating of soil increased pesticides Lpez-Vizcano
2,4-D and Diphenyl ether (32 m3) contaminated from smaller plants: pilot-scale volatility. 85% oxyuorfen and 87% 2,4-D et al. (2017)
oxyuorfen herbicides (175 L) and lab-scale soil column were volatilized. Removal of herbicides from
(1 L). soil is affected by the size of the plant.

conditions used to be more favorable for degradation of pesticides per- 2.3.1.2. Chemical oxidation. Advanced oxidation processes. The purpose of
sistent in aerobic environments. Nano-scale zero-valent iron (nZVI) is chemical oxidation in contaminated soils is to mineralize the pollutants
usually used as a chemical reductant for a cost-efcient degradation of to CO2, water and inorganics, or transform them into biodegradable or
chlorinated pollutants in soil. Treatment with nZVI promotes a rapid harmless products. The most commonly used oxidizing agents are
abiotic degradation of such contaminants via reductive dechlorination ozone, hydrogen peroxide, hypochlorites, chlorine, and chlorine dioxide
and can be used to remediate soils contaminated with OCPs (Shea (Pavel and Gavrilescu, 2008). However, these traditional chemical oxi-
et al., 2004; Cong et al., 2010; Yang et al., 2010; Han et al., 2016). In dation methods are not effective enough to degrade pesticides, but
one study, metolachlor degradation was enhanced by adding these oxidants can be combined with iron salts, semiconductors (such
Al2(SO4)3 to the Fe0, increasing acidity and promoting the formation as TiO2) and/or ultraviolet-visible light irradiation to yield better results.
of green rust [mixed Fe(II)/Fe(III) double hydroxides], which facilitated Such remediation processes are called advanced oxidation processes
the pesticide dechlorination (Satapanajaru et al., 2003). (AOPs), a promising technology for the remediation of soils contaminat-
The combination of chemical treatment using nZVI with biodeg- ed with highly refractory organic chemical such as pesticides (Cheng
radation can maximize the remediation of pesticide-polluted soils. et al., 2016).
Boparai et al. (2008) reduced the concentration of metolachlor in a Fenton processes, TiO2 photocatalysis, plasma oxidation, ozonation
contaminated soil after chemical treatment with nZVI and aluminum and electrochemical oxidation processes are the most common AOPs
sulfate, but atrazine and nitrate remained. After adding sucrose, a de- techniques (Rodrigo et al., 2014). However, their application to
crease in atrazine and nitrate concentrations were observed. The soil remediation is very scarce, being Fenton oxidation and TiO2
presence of readily available carbon gave as result an enhanced mi- photocatalysis the most typical techniques. AOPs neither transfer pol-
crobial activity. Amendments such as nZVI improved the reductive lutants from one phase to the other nor produce massive amounts of
dechlorination process of DDT because it serves as an electron hazardous sludge. Strong oxidizing intermediates (mainly OH radicals)
donor under anaerobic conditions, thereby stimulating biological de- are formed and their reaction with organic contaminants not only leads
chlorination (Sudharshan et al., 2012). to their destruction, but also provides optimal conditions for their com-
However, properties such as the small size and high redox reactivity plete mineralization (John and Shaike, 2015).
of nZVI, which are useful for environmental remediation, also make The Fenton process, initially investigated in the 1990s by Watts et al.
them harmful to microbial populations, plants or earthworms (El- (1990), is the most commonly used AOP in the remediation of pesticides
Temsah et al., 2016). Moreover, as a certain percentage of nZVI is lost in soil. Hydroxyl radicals (OH) are generated by the catalytic decompo-
due to its reaction with dissolved oxygen, oxide minerals and organic sition of hydrogen peroxide (H2O2) due to soluble iron (II) in acidic me-
matter of soils, it has to be compensated with increasing amounts of ap- dium. Fenton process has the possibility to be used for in situ
plied nZVI. remediation, allowing the rapid treatment of non-easily removable

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ

Table 4
Selected reports on the use of chemical technologies for remediation of pesticide-contaminated soils.

Pesticide Pesticide class Scale Contamination in soil Reagent used/ Results/Pesticide removal Reference
Operation conditions

Metolachlor, Chloroacetamide (2), Field-scale in situ Contaminated soil due to Zerovalent iron (ZVI) 5% (w/w) to N60% degradation of all pesticides in 90 d Shea et al. (2004)
alachlor, triazine, dinitroaniline (3.5 1.20 2660 m3) accidental spill promote reductive dechlorination N90% when 2% (w/w) Al2(SO4)3 was added to the Fe0
atrazine, herbicides and and nitro group reduction
pendimethalin, organophosphate
chlorpyrifos insecticides
HCHs Organochlorine Laboratory Soil from a ZVI as reducing agent (10% w/w) Reductive dechlorination rate HCHs N DDTs. Cong et al. (2010)
DDTs pesticides and pesticide-manufacturing Limited by dissolution rate in aqueous phase.
metabolites plant
HCHs Organochlorine Laboratory Soil from a ZVI as reducing agent (0.55% Increased DDT degradation with Fe0 concentration, but Yang et al. (2010)
DDTs pesticides and pesticide-manufacturing w/w). Ultrasonic extraction not for all metabolites. DDTs not decreased markedly.
metabolites plant
DDT Organochlorine Laboratory and in situ treatments DDT spiked soil and ZVI, different conditions: iron The degradation half-life of p,p'-DDT decreased Han et al. (2016)

E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx


insecticide DDT-contaminated eld. sources and dosage, and soil signicantly from 58.3 to 27.6 h with nZVI dosage from 0.5
moisture, temperature, and types. to 2.0% and from 46.5 to 32.0 h with temperature from 15
to 35 C.
DDT Organochlorine Laboratory DDT historically Two types of nZVI in soil columns 25.4% DDTdegradation in 24 h. Both types of nZVI had El-Temsah et al. (2016)
insecticide contaminated soil negative impact on some tested organisms.
Atrazine Triazine and Field-scale in situ Contaminated soil due to ZVI (5% w/w), aluminum sulfate ZVI (5% w/w) and aluminum sulfate (2% w/w) degraded Boparai et al. (2008)
Metolachlor Chloroacetamide accidental spill (2% w/w), sucrose (5% w/w) 100% metolachlor in 95 days. For atrazine reduction
herbicides addition of sucrose (5% w/w) was necessary
Atrazine Triazine herbicides Field-Scale (275 m3 soil) Soil from a Chemical-biological treatment Atrazine and cyanazine concentrations decreased by 79 to Waria et al. (2009)
Cyanazine pesticide-manufacturing (Fe0 + FeSO4 + emulsied 91% in 342 d.
plant soybean oil to stimulate
biodegradation)
Diuron Phenylurea herbicide Laboratory Articially contaminated Photocatalysis with solar light in 100% diuron degradation in the top 4 cm of contaminated Higarashi and Jardim
presence of TiO2 (02%). soil in 50 h with 0.1% TiO2 (2002)
Glyphosate Phosphonoglycine Laboratory Articially contaminated Photocatalysis with solar light in 90% degradation in 2 h. the best results with 3050% Xu et al. (2011)
herbicide presence of Fe3O4/SiO2/TiO2 moisture content and 610 mW/cm2 sunlight intensity.
(0.5%).
Imidacloprid Neonicotinoid Laboratory Articially contaminated Photocatalysis with UV light in Best result: 83% degradation with pH 3, UV light 30 W m2, Sharma et al. (2015)
insecticide presence of TiO2 (0.10.5 g/kg) soil depth 0.2 cm, initial concentration of imidacloprid
10 mg/kg.
DDT Organochlorine Laboratory Soil from a Fenton process 75% DDT disappear from the slurry system in 70 h, but in Villa et al. (2008)
insecticide pesticide-manufacturing great part due to volatilization. 80% soil OM degraded.
plant Drastic increase in metals in ltrates.
DDT Organochlorine Laboratory Soil from a former pesticide Three sequential washings with 66% (DDT), 80% (DDE) removal from soil by the surfactant. Villa et al. (2010)
DEE insecticide and warehouse Triton X-100 and photo-Fenton After 6 h of photo-Fenton oxidation on wastewater, 99
metabolite oxidation of wastewater (DDT) and 95% (DDE) degradation.
generated.
HCHs Organochlorine Laboratory Articially contaminated H2O2 (HP), H2O2 + FeII (Fenton- Isomers degradation: F N PS N AP N HP N PM, but -HCH Usman et al. (2014)
insecticide (lindane) and from a pesticide F), sodium persulfate (PS), FeII was the most recalcitrant. Lindane in spiked soil: 95, 90,
and isomers manufacturing plant activated persulfate (AP) and 70, 60, 55% using PS, F, HP, AP, PM, respectively. Lesser
permanganate (PM) extent of degradation in real contaminated soil
Diuron Phenylurea herbicide Laboratory Articially contaminated H2O2, trisodium citrate (CT) as Oxidation rate dependent on iron and H2O2 Rosas et al. (2014)
chelant, and Fe(III) as catalyst concentrations. 100% degradation in 50 h with the best
conditions
DDT Organochlorine Laboratory Articially contaminated Hydroxyl radicals and ozone Ozone alone did not degrade DDT in soil. 90% reduction of Balawejder et al. (2014)
insecticide DDT in uidized bed reactor with hydroxyl radicals
generated from ozone and water vapor.
DDT Organochlorine Pilot-scale Articially contaminated Utilization of hydroxyl radicals 80% degraded, without generation of DDT degradation Balawejder et al. (2016)
insecticide generated from water aerosol and products.
ozone in a uidized bed reactor

9
10 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

Table 5
Selected reports on the use of bioremediation by microorganisms in pesticide contaminated soils.

Pesticide/biological Scale/contamination Bioremediation Technique Microorganisms involved Results/pesticide removal References


function

Molinate (herbicide) Laboratory (paddy Natural attenuation Endogenous ora 39% mineralised Lopes et al.,
eld soils) Bioaugmentation Microbial consortium: G. molinativorax 63% mineralised after 42 days 2012
ON4T, Pseudomonas (two strains),
Stenotrophomonas and Achromobacter
Myclobutanil, Pilot (vineyard Bioaugmentation Bacillus strains, namely, DR-39, CS-126, N85% biodegraded after Salunkhe et al.,
tetraconazole and plots) TL-171, and TS-204 20 days 2015
usilazole
(fungicides)
Fenpropathrin Laboratory Bioaugmentation Bacillus sp. DG-02 93.3% biodegraded after 72 h Chen et al., 2014
(insecticide) (solution)
2,4-D (herbicide) Laboratory Bioaugmentation Novosphingobium, strain DY4 5095% biodegraded after 3 Dai et al., 2015
(paddy-planted and 7 days, respectively
eld)
Chlorpyrifos Laboratory Bioaugmentation Bacillus cereus, strain Ct3 88% biodegraded after 7 days Farhan et al.
(herbicide) (Agricultural soil) (2014)
Laboratory (paddy Bioaugmentation Aspergillus terreus JAS1 100% biodegraded after 48 h Silambarasan
eld soils) and Abraham,
2013
Bensulphuron-methyl Laboratory Bioaugmentation Penicillium pinophilum strain, BP-H-02 87% biodegraded after 60 h Peng et al.
(herbicide) (Agricultural soil) (2012)
Organochlorine Pilot (agricultural Bioestimulation (soil Endogenous ora Biodegradation Islas-Garca
pesticides soil) macronutrients C:N:P et al. (2015)
100:10:1)
DDTs Laboratory (soil Natural attenuation Endogenous ora 23% biodegraded after Ortz et al.
(insecticide) from rural areas) 7 weeks (2013)
Bioestimulation (phenol, N56% biodegraded after
hexane and toluene) 7 weeks
Pentachlorophenol Laboratory (paddy Bioestimulation (lactate and Endogenous ora Up to 97% biodegraded after Chen et al.
(herbicide) eld soils) anthraquinone-2,6-disulfonate) 6 days (2012)
Atrazine (herbicide) Laboratory Natural attenuation Endogenous ora 54.4% mineralised after Silva et al.
(Agricultural soil) 67 days (2004)
Bioaugmentation Pseudomonas sp. strain ADP 30.6% mineralised after
7 days
Bioaugmentation + Pseudomonas sp. strain ADP 79.9% mineralised after
bioestimulation (citrate and 13 days
succinate)
Chlorpyrifos Laboratory Bioaugmentation CS2 strain 55% biodegraded after 6 days Singh et al.
(herbicide) (agricultural soil) Bioaugmentation, CS2 strain, bio-surfactant rhamnolipid 82.3% biodegraded after (2016)
bioavailability enhancer 6 days
Atrazine (herbicide) Laboratory Bioaugmentation Strain A6 (Acinetobacter) 30% biodegraded after 6 days Singh and
(agricultural soil) Bioaugmentation, Strain A6, rhamnolipids and Triton X-100 80% biodegraded after 6 days Cameotra
bioavailability enhancer (2014)
Diuron (herbicide) Laboratory Bioaugmentation Bacterial consortium: Arthrobacter sp. 45% mineralised after Villaverde et al.
(agricultural soil) N2, Variovorax sp. SRS16 120 days (2012)
Bioaugmentation, Bacterial consortium, 98% mineralised after
bioavailability enhancer hydroxypropyl--cyclodextrin 120 days
Organochlorine Laboratory (paddy Bioestimulation, bioavailability Nitrate (KNO3), methyl--cyclodextrin 74.3% biodegraded after Ye et al. (2014a)
pesticides (OCPs) eld soils) enhancer 180 days
Atrazine, metolachlor, Laboratory Composting Corn stalks, corn fermentation byproduct, 30, 33 and 44% biodegraded Moorman et al.
triuralin (agricultural soil) peat, manure, and sawdust after 245 days (2001)
(herbicides)
Triazine herbicides Laboratory Composting Olive cake, compost and vermicompost of Faster decrease in the Delgado-Moreno
(agricultural soil) olive cake herbicides concentration and Pea (2009)
during the rst week of
incubation
Atrazine (herbicide) Laboratory Bioestimulation, composting Sodium citrate, farmyard manure 34% biodegraded after Kadian et al.
(agricultural soil) 21 days (2008)
Diuron (herbicide) Laboratory Bioestimulation, composting, Micronutrients, sewage sludge mixed 46.5% mineralised after Rubio-Bellido
(agricultural soil) bioavailability enhancer with pruning wastes, urban solid 140 days et al. (2015)
residues, hydroxypropyl--cyclodextrin
Linuron, diazinon and Pilot (agricultural Composting Sewage sludge, grape marc, spent Positive or negative effects on Marn-Benito
myclobutanil soil) mushroom substrate mineralisation depending on et al. (2014)
(herbicides) organic amendment
Hexachlorocyclohexane Pilot Lindane Landfarming Endogenous ora 89% biodegraded after Rubinos et al.
(insecticide) manufacturing site 21 days (2007)
Lindane (herbicide) Laboratory Aerobic soil slurry bioreactors Lindane-acclimated inoculum, nal 5570% biodegraded after Varo-Arguello
bioestimulation, electron acceptor (O2, CO2 and SO2
4 ), 7 days et al. (2012)
bioaugmentation co-substrate (sucrose)
Pendimethalin Laboratory Slurry bioreactor (composting) Sewage sludge 91% biodegraded Ramakrishnan
(herbicide) et al. (2011)
2,4-D (herbicide) Laboratory Slurry bioreactor Aerobic (endogenous ora) 93% biodegraded after Robles-Gonzlez
(bioaugmentation) 14 days et al. (2008)
Sulfate-reducing bacteria 25% biodegraded after
14 days

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 11

Table 5 (continued)

Pesticide/biological Scale/contamination Bioremediation Technique Microorganisms involved Results/pesticide removal References


function

Lindane (herbicide) Laboratory Slurry bioreactor (anaerobic Sewage sludge 90% biodegraded after Quintero et al.
composting) 10 days (2006)
Methoxychlor Laboratory Slurry bioreactor Actinobacteria N60% biodegraded after 12 h Fuentes et al.
(herbicide) (bioaugmentation) (2014)
2,4-D (herbicide) Laboratory Slurry bioreactor (aerobic Acclimatised activated sludge N90% biodegraded after 6 h Znad et al.
composting) (2010)
Bentazone, boscalid, Pilot (agricultural Biobed (biomixture) Biolter materials (mixtures of soil with Desorption was hysteretic for Mukherjee et al.
and pyrimethanil soil) digestate and/or biochar) all pesticides on these (2016)
(herbicides) materials
Carbofuran Pilot (agricultural Biobed (biomixture) Lignocellulosic materials mixed with 98.5% mineralised after Chin-Pampillo
(insecticide) soil) compost 16 days et al. (2015)
Chlorothalonil Laboratory Biobed (biomixture) Spent mushroom substrate DT50 79 days, Gao et al. (2015)
(fungicide) biodegradation
Atrazine (herbicide) Laboratory Biobed (biomixture) Soil, peat and straw, lignocellulosic b90% biodegraded after Diez et al.
residues. 90 days (2013a, 2013b)
Oxyuorfen (herbicide) Laboratory Biobed (biomixture) Vermicompost 70% biodegraded after Castillo-Diaz
30 days et al. (2016)
Carbofuran Carbofuran Biobed (biomixture) Ligninolytic fungus Trametes versicolor, 100% biodegraded after Madrigal-Ziga
(insecticide) (insecticide) compost 48 days et al. (2016)

without having to excavate the contaminated soils. DDT, diuron, 2,4-di- An alternative to using AOPs as single treatment technologies is to
chlorophenol (2,4-DCP), pentachlorophenol (PCP), and other pesticides combine AOPs with other technologies to minimize cost or enhance ef-
in soils can be degraded by Fenton/Fenton-like processes (Usman et al., ciency by exploiting complementarities or synergies between technol-
2014; Rosas et al., 2014). However, there are collateral effects of the ogies. Innovations such as the use of chelating agents or surfactants on
Fenton process. Villa et al. (2008) observed that, although a high per- the traditional AOPs and the combined utilization with bioremediation
centage of DDT was degraded in soil, an increase of dissolved organic or soil washing are also documented.
carbon (from 80 to 880 mg l1) occurred, and 80% of the natural organic In studies evaluating the difference in efcacies between Fenton and
matter was degraded; also an increase in metal concentrations was ob- photo-Fenton processes for treating pesticide-contaminated wastewa-
served in the slurry ltrate. Direct application of the Fenton process is ter, laboratory data showed that 99% degradation for chlorimuron-
very aggressive to the soil and can be also a disaster to the microbes ethyl was achieved in 10 min by using photo-Fenton oxidation, howev-
(Brillas et al., 2009). er, only 68% degradation was observed after 30 min Fenton oxidation
In photocatalysis technique, hydrogen peroxide molecule is separat- (Gozzi et al., 2012). Villa et al. (2010) observed that 99% of DDT could
ed into two hydroxyl radicals by UV/vis photolysis, increasing the rate of be removed by Fenton oxidation after soil washing using a Triton X-
photolysis with alkaline conditions. As catalyst, it uses the semiconduc- 100 solution and subsequent treatment of wastewater using photo-
tor metal oxide, and TiO2 in the anatase form is the most appropriate Fenton oxidation.
due to its characteristics: high photoactivity, non-toxic, low cost, chem- Research in advanced oxidation processes is still at an early stage.
ical inertness, and easy to obtain. Different pesticides have been suc- Most studies to date have been conducted at the lab-scale and many im-
cessfully decomposed in soils using TiO2 under solar light or UV- provements are required before the technology can be scaled up to
irradiation. Xu et al. (2011) and Sharma et al. (2015) observed for bench and pilot plant levels in terms of assessing cost and operation
glyphosate and imidacloprid that the photocatalytic reaction mainly oc- conditions. According to Rodrigo et al. (2014), most of the studies pub-
curs in the surface part of the soil and the degradation efciency de- lished in the literature have focused on pollutant removal at concentra-
creases as the soil layer increases. It was observed by Xu et al. (2011) tions that are signicantly higher than typical pollutant concentrations
that only a small amount of catalyst (0.5%) was needed to remediate a in a soil, and which are only found in industrial wastes. However,
soil with low gyphosate content. Similar results were observed for diu- these studies are the only way of determining the efciency of the
ron (Higarashi and Jardim, 2002). technology.
Although Fenton processes and TiO2 photocatalysis are the two typ-
ical AOPs, ozonation has to be also considered because it is one of the 2.3.2. Biological remediation
most promising techniques which can be applied in situ or on site. The The conventional techniques used for remediation of organic pollut-
pesticide can be directly decomposed by O3 or can react with OH radi- ants in soil such as landlling, high temperature incineration or chemi-
cal which has been generated by the O3 decomposition on active sur- cal decomposition can be effective. However, they are also associated
faces of soil, such as metal oxides or organic matter. As ozonation is a with many drawbacks such as complexity and high costs, and some
relatively new technique for pesticides remediation, the majority of may pose environmental risks; consequently, public acceptance is
the studies have been performed in aqueous medium. often low. There is a signicant risk in the excavation, handling, and
However, there are strong limitations for using the ozonation transportation of hazardous materials, apart from the cost of removal
technique to degrade organic contaminants in soil due to the dif- of contaminated soil. In addition, these traditional techniques are not al-
culty of the diffusion process through this heterogeneous matrix. ways sufcient and therefore alternative greener remediation ap-
Ozone can only penetrate the upper 1545 mm of the soil. proaches, low cost and easy methods are needed to completely
Balawejder et al. (2014, 2016) developed an effective remediation destroy the pesticides, if possible, or at least to transform them to innoc-
method for DDT-contaminated soil based on the utilization of hy- uous substances, reducing risk for both the environment and human
droxyl radicals that were generated from water aerosol and ozone health.
in a uidized bed reactor. Soil contamination was reduced by 90%. Bioremediation, i.e. the use of living organisms to remediate
The total organic carbon was preserved and no degradation prod- pesticide-polluted sites, is an emerging technology (Chawla et al.,
ucts were detected. 2013). Bioremediation of contaminants includes different techniques

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
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12 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

such as biodegradation using soil microorganisms, phytoremediation microorganisms with an environment which favors the development
using plants, or vermiremediation using earthworms. One of the most of metabolic pathways for contaminant biodegradation. Islas-Garca
important reasons for using bioremediation to eliminate organic pollut- et al. (2015) studied different parameters such as concentrations of hy-
ants is that it is a cost-effective and environmentally friendly technique drocarbons and organochlorine pesticides (OCPs), nutrients and toler-
and offers the possibility to destroy or render harmless organic contam- ant microorganisms in an agricultural soil to dene its feasibility for
inants using natural biological activity. Bioremediation is well accepted bioremediation. The decreasing in the pollutant concentration and the
by the general public and can often be carried out on site. Although any increasing in microbial activity indicated that the use of bio-
procedure for removing or destroying pollutants is expensive, biological stimulation of native microorganisms was feasible in a soil contaminat-
procedures tend to be the least expensive ones (Alexander, 2000). ed with hydrocarbons and pesticides. In a similar study, Ortz et al.
(2013) proved that stimulation of indigenous microbial soil ora by
2.3.2.1. Bioremediation by microorganisms. The main biological agents the addition of small amounts of secondary carbon sources enhanced
used in bioremediation are bacteria and fungi which use the contami- the biodegradation/mineralization of DDT and its main metabolites.
nants as nutrient or energy source. The microbial diversity of the site Chen et al. (2012) explored biostimulation mechanisms with an elec-
is one of the most important parameters for bioremediation, together tron donor and a shuttle for accelerating pentachlorophenol (PCP) deg-
with the nature of the pollutants, and some properties of the soil (pH, radation in iron-rich soils. Bioestimulation of indigenous microbial soil
moisture content, nutritional state, temperature, oxidation-reduction communities by the addition of lactate and anthraquinone-2,6-
potential) (Niti et al., 2013). Table 5 shows some results obtained by disulfonate increased the rates of pentachlorophenol dechlorination.
using biodegradation by soil microorganisms for remediation of Silva et al. (2004) developed a joint bioaugmentation and biostimula-
pesticide-contaminated soils. tion approach for the clean-up of soil contaminated with high concen-
In natural soil bioremediation, the existing native microora al- trations of the herbicide atrazine. The Pseudomonas sp. strain ADP was
ready present in the polluted soil is used to degrade the target con- used for bioaugmentation and citrate and succinate for biostimulation.
taminants. Bioremediation of soils contaminated with pesticides They also concluded that the studied soil had indigenous potential for
has drawn considerable research interest, mainly because pesticide atrazine mineralization, but a signicant mineralization rate only took
pollution is constantly increasing and most chemicals are persistent place after a acclimation phase.
in the environment. However, in situations in which microbial pop- As mentioned previously, bioavailability of pesticides and other or-
ulations are not large or diverse enough to efciently degrade the ganic contaminants is a major limitation to complete bioremediation of
target pollutants, inoculation of enriched/acclimated consortia or contaminated soils (US EPA, 1999). It affects the clean-up time, cost,
single pollutant degrading strains is carried out; this procedure is and the end-point of the process (Pignatello et al., 2010). From a biodeg-
called bioaugmentation. Lopes et al. (2012) assessed the potential ca- radation point of view, bioavailability was dened as the accessibility of a
pacity of natural attenuation or bioaugmentation to degrade chemical for assimilation by microorganisms (Alexander, 1995). The
molinate in an agricultural soil, as well as the impact of these biore- term bioaccessibility encompasses what is immediately available plus
mediation technologies on the composition of indigenous that which may become available, whereas bioavailability refers to
microbiota. A molinate mineralizing consortium was used as inocu- what is available immediately. In this sense, a number of pollutant soil
lum in the bioaugmentation assays, and a signicantly higher remov- risk assessments based on bioaccessibility studies have been published.
al of molinate was observed in bioaugmentation than in a natural For this purpose, non-exhaustive extractions have been used to deter-
attenuation system. The strains can be obtained from the indigenous mine the bioaccessible fraction of the contaminant after different aging
soil ora isolating strains from the polluted site and selecting them periods. Recently, Villaverde et al. (2013) have used different non-
under laboratory conditions according to the pollutant (enrichment exhaustive extraction techniques to determine whether their extraction
cultures); after growth, microorganisms are inoculated on site in abilities correlated with the bioaccessible diuron fraction in an aged con-
the polluted area. Salunkhe et al. (2015) report the in vitro and taminated soil. Diuron bioaccessibility was evaluated through correla-
in vivo biodegradation of three triazole fungicides by isolated tions between the biodegraded diuron after different aging periods
Bacillus strains. Chen et al. (2014) observed that Bacillus sp. DG-02, (diuron biodegrader microbial consortium) and the diuron extracted by
previously isolated from a pyrethroid-manufacturing wastewater, a biomimetic extraction using a 50 mM hydroxypropyl--cyclodextrin
was capable to degrade fenpropathrin, and a wide range of synthetic (HPBCD) solution, 10 mM CaCl2, hexane, or butanol. The authors conclud-
pyrethroids. Dai et al. (2015) investigated the bioremediation poten- ed that the aqueous HPBCD extraction technique has potential to become
tial of a novel degrader for 2,4-D-polluted soil and its bioaugmenta- a valuable tool for estimating the bioaccessible fraction of soil-associated
tion impact on the microbial soil community. Farhan et al. (2014) diuron at different aging times, and this could be applicable in the assess-
isolated microbial strains from cotton-growing agricultural soils ment of risk and contaminated land bioremediation potential.
which were managed with chlorpyrifos. Nagy et al. (2013) investigated reliable methods for assessing the
Although microbial biodegradation of pesticides has mostly been soil microora and its activity as a prerequisite for successful technology
studied using bacteria, a number of fungal strains belonging to different planning and sustainable bioremediation of different contaminated
genera have also been isolated and characterized to be used for biodeg- sites. The contaminant concentrations were measured by using a
radation of different pesticides (Maqbool et al., 2016). Peng et al. (2012) harsh extraction and by a biomimetic extraction using a cyclodextrin so-
isolated from a contaminated soil a fungal strain (BP-H-02) able to rap- lution. Most of the applied biological and chemical methods were reli-
idly degrade bensulphuron-methyl. This strain could be used to able indicators of chlorophenol biodegradation in soil. Baczynski et al.
bioremediate sulphonylurea herbicide contamination. Biodegradation (2012) obtained results of desorption kinetics using Tenax solid phase
of chlorpyrifos was studied in mineral medium and soil with the novel extraction (SPE) as predictors after 3 weeks of anaerobic soil biodegra-
fungal strain JAS1 isolated from a paddy eld soil (Silambarasan and dation effectiveness for chlorinated pesticides gamma-HCH, DDT, and
Abraham, 2013). However, and because environmental microbiologists methoxychlor. Fenlon et al. (2011) performed a study on the formation
estimate that b 2% of bacteria have been cultured in the laboratory, of bound residues and mineralization of the insecticide cypermethrin in
molecular approaches to study microorganisms for bioremediation four organically managed soils. The potential bound residues formed
have become important tools for assessing potential natural attenua- were measured using three different non-exhaustive extractions
tion, and hence, the need to apply a bioremediation technique employing, 0.01 M CaCl2 and 0.05 M HPBCD solutions and acetonitrile
(Chakraborty and Das, 2016). solvent; biodegradation was assessed by mineralization bioassays of
On the other side, bioestimulation consists in the addition of appro- cypermethrin. The bound residues formation assessment varied accord-
priate nutrients (nitrogen, phosphorus, trace elements) to provide the ing to the mild extraction tested, soil type and the aging period.

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
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E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 13

On the other side, surfactants can be used as bioremediation pro- myclobutanil, in an un-amended agricultural soil and in soil amended
moters accelerating pesticide mineralization through increasing the with three different organic residues. DT50 values decreased in both
amount of the pollutant present in the soil solution. Singh et al. the unamended and amended soils for linuron, but increased for the un-
(2016) used a crude rhamnolipid biosurfactant produced by ChlD, amended and amended soil for diazinon and myclobutanil, due to the
which improved the aqueous phase solubility of chlorpyrifos by 215 formation of non-extractable residues formation in amended soils. The
folds. Singh and Cameotra (2014), studied the effect of different surfac- results obtained revealed that the simultaneous use of amendments
tants (rhamnolipids and triton X-100) on biodegradation of atrazine and pesticides in soils requires a preliminary study in order to evaluate
herbicide by a degrader strain A6, belonging to the genus Acinetobacter. the environmental specic persistence of these compounds and the ef-
Bacterial cell surface hydrophobicity as well as atrazine solubility in- fectiveness of amended soils to enhance pesticide biodegradation.
creased in the presence of surfactant. Villaverde et al. (2012) developed The presence of water-soluble compounds such as humic or fulvic
a cyclodextrin-based bioremediation technology which showed for the acids as well as small biomolecules such as peptides and fatty acids (nat-
rst time an almost complete diuron mineralization in soil, using a diu- ural surfactants) may cause desorption, solubilization and complexation
ron biodegrader consortium. Ye et al. (2014a) performed a study to in- of organic pollutants. Rubio-Bellido et al. (2015) concluded that the dis-
vestigate the anaerobic biodegradation potential of biostimulation by solved organic matter from the organic amendments, used for soil diu-
nitrate (KNO3) and the application of methyl--cyclodextrin on an ron bioremediation, acted as a natural surfactant provoking an increase
aged organochlorine pesticide-contaminated paddy soil. Gao et al. of the bioavailable fraction of the herbicide, and hence improving its
(2015) carried out a study to verify the feasibility of the HPBCD biomi- mineralisation rate. Therefore, compost may be used for the balance be-
metic extraction for assessing the bioavailability of DDT and their me- tween sorption to soil particles and biodegradation in contaminated
tabolites in soils. The effect of HPBCD on their biodegradation in sites (Kstner and Miltner, 2016). The success of composting in the bio-
different soils was also investigated. However, HPBCD affected nega- remediation of contaminated soils depends on a number of physical,
tively to DDT soil biodegradation when was applied as a bioestimulant. chemical and biological characteristics of the reaction environment. A
The use of microbial processes have been broadly used for the elim- key factor is the microbial bioaccessibility to the pollutants, which is de-
ination of chemicals from household or industry efuents as waste- termined both by the mechanical conditions (mixing, moisture con-
treatment systems. However, many compounds are not always tents, soil composition), and by the properties of the applied
completely degraded, not necessarily because of the absence of a amendment.
biodegradative microora, but rather because the technique have not In many cases, it is necessary to move the contaminated soil to a site
been optimized which highlights the need for new or modied biore- where a suitable treatment system can be applied (ex situ bioremedia-
mediation techniques. A number of novel and promising methods tion). If the economic and technical analysis favors ex situ bioremedia-
have been developed, where biostimulation combined with bioaug- tion, it can be concluded that such treatment is the optimal approach.
mentation and bioavailability improvements have yielded promising There are a variety of technologies available which can be considered
results. In situ treatments, in which soil is not removed from the con- and they could be classied into two generic technologies:
taminated land, have several advantages, such as the relatively low i) landfarming and biopiles; ii) slurry bioreactors. Landfarming and
costs, but the disadvantage of diminished rigorous control. biopiles dominate the ex situ bioremediation of contaminated soils, al-
though however, bioreactors offer advantages in the level of process
2.3.2.1.1. Composting. Composting is a conventional treatment technolo- monitoring and the modications of the operation.
gy employed in remediation of agricultural and municipal solid wastes
and sewage sludge, but the application of composting in soil as an in 2.3.2.1.2. Land farming and biopiles. Landfarming is an ex-situ treatment
situ bioremediation is somewhat more recent. The principle of opera- procedure that is performed in the upper soil close to the contaminated
tion consists of mixing the contaminated soil with non-hazardous or- soil zone or in biotreatment cells. Contaminated soils are transported to
ganic amendments, generally other solid wastes (i.e., manure, the landfarming site, incorporated into the soil surface over large areas
agricultural wastes) suitable for composting applications, to encourage with a thickness of a few ten centimeters and periodically tilled to aer-
the development of bacterial populations or other organisms, such as ate the mixture. This technique is easy to implement, does not require
fungi, earthworms, etc., which are able to degrade the pollutants in heavy infrastructure, and is cost-efcient. However, operations last a
the soil via cometabolic pathways. Moorman et al. (2001) employed long time (years or decade) and are likely to produce odors and visual
several organic amendments, including compost, corn fermentation nuisances. In addition, pesticides may leach from the site contaminating
byproduct, corn stalks, manure, peat and sawdust to improve the re- groundwater, and volatile emissions may pose hazards in the vicinity of
moval of the herbicides atrazine, triuralin and metolachlor from con- the site. Therefore, leaching or volatilization of toxic compounds (origi-
taminated soils. On the contrary, Delgado-Moreno and Pea (2009) nal compound and metabolites) must be controlled or prevented. To
observed that the addition of vermicompost and olive cake in soils did avoid any risk of inltration, a waterproof cover must be in place before
not increase the removal of different pesticides, simazine, cyanazine, the start of the treatment.
terbuthylazine and prometryn. Kadian et al. (2008) investigated the ef- Land farming requires a signicant period of time, since slow kinetic
fects of different organic amendments on the removal of atrazine in con- microbial degradation takes place; its applicability is therefore limited
taminated soils. The addition biogas slurry showed the highest atrazine to supercially contaminated soil. Landfarming has been successfully
removal, and the study on synergistic effect of sodium citrate with farm- employed for the treatment of contaminated soils by different organic
yard manure showed initially a negative effect, increasing dissipation pollutants, aliphatic and aromatic hydrocarbons, pesticides, etc., and it
gradually. Diuron desorption and mineralization were studied on an is still a valid technology when remediation times are not a critical con-
amended and articially contaminated soil by Rubio-Bellido et al. cern, or the degree of contamination is not high enough to expect a
(2015). Two different composted organic residues, sewage sludge strong inhibitory effect on the endogenous bacterial community.
mixed with pruning wastes, and urban solid residues, and two different An application of landfarming in the bioremediation of soils heavily
solutions (micronutrients and cyclodextrin) were used, concluding that contaminated (N5 g/kg) with hexachlorocyclohexane (HCH) isomers
the joint application of all treatments investigated at the best concentra- was reported by Rubinos et al. (2007). They found different behaviours
tion studied showed the best diuron mineralization results. of the four investigated isomers: two of them, and , could be signif-
The addition of particulate organic matter from composts has impor- icantly removed (89% and 82%, respectively) while for the others ( and
tant effects especially when the contaminant is present in relatively low ) a negligible decrease was observed. This nding is a good example of
concentrations in soils. Marn-Benito et al. (2014) studied the dissipa- the high specicity of the microbial bioremediation. Felsot and Dzantor
tion kinetics of three different pesticides, linuron, diazinon and (1997) suggested landfarming as an efcient method for soil pesticide

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
14 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

remediation, which could be made more efcient by amendments with of this approach would be the accurate control of the bioremediation
different organic nutrients, mixing contaminated with uncontaminated process, which can be optimized by setting and monitoring the most
soil, with the result that the dissipation of several herbicides (alachlor, critical parameters. The main disadvantage is the high cost, which has
atrazine, metolachlor, and triuralin) was stimulated. Rodrguez- to be justied for each particular application, and hence, slurry bioreac-
Vzquez and Acosta-Ramrez (2015) performed a biological technology, tors need a good record of medium- and full-scale success prior to the
based on Solid Cultivation On-site, (Mexican Patent No. 291975), large investments.
using coffee grain and straws, as well as low humidity and aeration, In slurry bioreactors contaminated soil is mixed with wastewater
for the removal of the organochloride pesticide DDT and its metabolites. residue to obtain slurry of a predetermined consistency, an aqueous sus-
A somewhat more sophisticated approach is associated with soil pensions in the range of 1030% w/v. The system can work under aero-
piles, which are also called biopiles, where a piping system is placed in bic or anaerobic conditions and in different feed modes: continuous,
the pile, and air or O2 is introduced to enhance aerobic decomposition semicontinuous, and batch. Slurry bioreactors have been applied to
of the pollutant. In addition, a solution containing nutrients is applied the bioremediation of persistent or recalcitrant contaminants such as
to the soil surface to stimulate microbial activity, and the leachate may herbicides, pesticides and explosives. An interesting emerging area is
be collected through the pile. In biopiles, the sample, after excavation, the use of slurry bioreactors with simultaneous electron acceptors,
is scraped up in a waterproof slab. A biopile can reach a height of 3 which has demonstrated to work for the bioremediation of PAHs in
4 m, with a volume of several hundred m3 (Bertrand et al., 2015). In soils and some organochlorinated compounds (Robles-Gonzlez et al.,
this technology, more engineering controls can be included, such as sys- 2008). Varo-Arguello et al. (2012) performed a study with two main ob-
tems to provide irrigation water and nutrients, a liner at the bottom of jectives: to evaluate the effect of co-substrate supplementation and pos-
the soil (clay or a synthetic material), and a means to collect the gener- sible synergistic effects of the indigenous population and a lindane-
ated leachate. Hence, the level of sophistication, and consequently the acclimated inoculum on the removal of lindane in three-phase, aerobic
cost, will vary enormously. slurry bioreactors; they also evaluated the effect of a nal electron accep-
tor and supplementation with carbon source on the removal of lindane in
2.3.2.1.3. Slurry bioreactors. Slurry bioreactors (SB) are considered as the triphasic laboratory scale slurry bioreactors. In both cases, under aerobic
most engineered treatment for soil bioremediation. The main advantage and anaerobic conditions, pesticide biodegradation was enhanced.

Table 6
Selected reports on the use of phytoremediation in pesticide contaminated soils.

Pesticide Pesticide class Scale Contamination Plant used/operation conditions Results/pesticide removal Reference
in soil

DDE Organochlorine Field Agricultural soil Zucchini, pumpkin, spinach After 3 months 40, 70 and 20% DDE removed from White (2001)
insecticide experiment (up to soil grown with zucchini, pumpkin, and spinach,
(metabolite) 500 mg/kg) respectively.
Aldicarb Carbamate Growth Articially Corn, mung bean and cowpea. Aldicarb t1/2 in soil was 2.7d, but it was 1.6, 1.4 and Sun et al. (2004)
pesticide chamber contaminated 1.7d in the soil grown with corn, mung bean and
(20 mg/kg) cowpea, respectively.
PCP Organochlorine Greenhouse Articially Rhizoremediation After 20d 40% removal from soil only with P. After 6d Dams et al.
pesticide experiment contaminated (P) (wheat) + 80% removal with I + P. (2007)
(100 mg/kg) Bioaugmentation (I) (S.
chlorophenolicum)
DDT Organochlorine Greenhouse Articially Alfalfa + arbuscular 66.895.4% removed in the rhizosphere soils, Wu et al. (2008)
insecticide experiment contaminated mycorrhizal fungus + Triton X- 13.164.8% in the bulk soils after 4 weeks,
(2.510 mg/kg) 100 depending on initial concentration.
DDT Organochlorine Greenhouse Soil in a former Cucurbita pepo ssp. Six Root DDT concentrations lower in soils with high Lunney et al.
insecticide experiment military site amendments to increase soil OM. No signicant adverse effects on (2010)
OM (2.427.3%) phytoextraction.
DDTs Organochlorine Greenhouse Contaminated Pumpkin/surfactants (Biosolve, Soil amendments did not increase DDTs extracted Whiteld Aslund
insecticide and experiment soil Aqueduct) or mycorrhizal fungi from soil, but a different distribution on plants. et al. (2010)
metabolites (1500 mg/kg)
Endosulfan Organochlorine Greenhouse Articially Ocimum basilicum L. and Both species can endure endosulfan pollution up to Ramrez-Sandoval
insecticide experiment contaminated Ocimum minimum L. 1 g/kg in soils. 37% removed from soil with O. et al. (2011)
(100 mg/kg) basilicum, but not with O. minimum.
DDTs Organochlorine Greenhouse Agricultural soil Willow trees + organic Increased p,p-DDE/p,p-DDT ratio when compared Mitton et al.
insecticide and experiment amendments: root exudates, with initial soil. Leaves translocation in willow plants (2012)
metabolites Tween 80, sodium citrate and especially with carboxylic acids.
oxalate
Cypermethrin Pyrethroid GreenhouseArticially Pennisetum pedicellatum. 10065% removed from soil for 10100 mg/kg in Dubey and
insecticide experimentcontaminated Rhizoremediation 60d. Degrading strain Stenotrophomonas maltophilia Fulekar (2013)
(10100 mg/kg) MHF ENV 22 isolated from rhizosphere
Lindane Organochlorine Greenhouse Articially Jatropha curcas L 8972% removed from soil for 520 mg/kg in 300d Abhilash et al.
insecticide experiment contaminated Rhizoremediation (2013)
(520 mg/kg)
DDTs and Organochlorine Greenhouse Old pesticide 17 naturally growing plants Artemisia annua accumulated 8 mg/kg of pesticides Nurzhanova et al.
HCHs pesticides and and eld storehouses (up in plant tissue. X. strumarium and S. dulcamara (2013)
metabolites experiments to 6.3 mg/kg) extracted 7080% pesticides from soil in 6 months.
DDTs Organochlorine Greenhouse Agricultural soil Tomato, sunower, soybean, Tomato the best phytoremediator, inceased Mitton et al.
insecticide and experiment alfalfa bioavailability in rhizophere. Translocation to roots N (2014)
metabolites leaves.
Endosulfan Organochlorine Field Abandoned Seven naturally growing plants Vetiveria zizanioides and Digitaria longiora Singh and Singh
insecticide and experiment pesticide factory accumulate 343 and 163 ng g1 of endosulfan (2014)
metabolites isomers.
Endosulfan Organochlorine Greenhouse Articially tomato, sunower, soybean, 72% removal from bulk soil in alfalfa. Lower levels in Mitton et al.
insecticide experiment contaminated alfalfa the rhizosphere with regards to bulk soil. The highest (2016)
(8 mg/kg) levels in roots and leaves in sunower.

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
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E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 15

Biodegradation of pendimethalin, a pre-emergence herbicide, was BB. Castillo-Diaz et al. (2016) used 6 bacteria and 4 fungus strains
carried out by Ramakrishnan et al. (2011) in a bioslurry reactor operat- from different mixtures incubated during one month to increase the
ed with native microora and amended with sewage, reaching 91% re- mineralization rates of different herbicides. Madrigal-Ziga et al.
moval efciency. The bioreactor operated as an anoxic-aerobic-anoxic (2016) used ligninolytic fungus Trametes versicolor as bioaugmentation
at different soil-water ratios and substrate loads. The effect of different agents in a compost- and peat-based biomixtures for obtaining a rapid
operating conditions, electron acceptors, and additional carbon sources biodegradation of the pesticide carbofuran.
were studied by Robles-Gonzlez et al. (2008) in the bioremediation of It is generally agreed that b1% of prokaryote species can be cultivat-
a clay soil with a high organic matter content contaminated with 2,4-D. ed. The extent of genomic diversity is unknown, but comparative geno-
They studied two parallel slurry bioreactors inoculated with aerobic a mic analysis suggests that the genetic diversity in microorganisms is
degrader strain, and with sulfate-reducing anaerobic bacteria. The aero- greater than expected. This suggests that there is much catalytic diver-
bic system showed better results in terms of overall removal extent, sity yet to be discovered. Form this basis, more information on microbial
while the sulfate-reducing bacteria showed better specic removal genomic will be necessary to translate a DNA sequence into knowledge
rates. Batch slurry bioreactors were used by Quintero et al. (2006) for of the specic reaction encoded by that gene. On the other side, the
the remediation of a soil contaminated with lindane, one of the most range of possible organic structure of pesticides is enormous and
widely used pesticides in agriculture. Fuentes et al. (2014) observed hence, more challenges will be posed for microbial metabolism, and it
an increase of about 10% in methoxychlor removal in stimulated slurry will be necessary to continually discover new microbial microorganisms
bioreactors. Znad et al. (2010) conducted biodegradation assays for the to match the discovery of new organic pesticide compounds.
herbicide 2,4-D in a net draft tube airlift bioreactor at different concen-
trations and air ow rates, using activated sludge. Characterization of
microbial communities of SB is still in the early stages, despite their sig- 2.3.2.2. Phytoremediation. The use of plants to remediate contaminants
nicance for improving reactor operation and optimization. in the environment is called phytoremediation. The term
phytoremediation was rst used in the 1980s, but its rapid expansion
2.3.2.1.4. Soil contamination prevention. Biobeds. Biobeds (BB) are simple in organic contaminants remediation began at the end of the last centu-
and inexpensive systems for bioremediation designed to collect and biode- ry (Gerhardt et al., 2009). Low molecular weight compounds such as
grade pesticide spills. The original design consists of a hole in the ground in some pesticides can be transported across plant membranes and re-
which a layer of clay is placed on the bottom. A mixture of straw, peat and moved from the soil. They can be released through leaves via evapo-
soil is added, followed by a layer of grass. Straw is the main component transpiration processes (phytovolatilization). Non-volatile compounds
used for fungi growth, the soil is used for the contaminant adsorption can be degraded (phytodegradation) or become non-toxic via
and improves the microbial activity, and the peat contributes to moisture enzymatic modication and sequestration in planta (phytoextraction),
control. An efcient mix of materials for a BB must include wide surfaces or are degraded by microorganisms present in the rhizosphere
for the retention of pesticides, which will reduce leaching, and at the (rhizodegradation). Compounds sequestered in the plants can be re-
same time provide an active soil microbial ora. The principal component moved with the biomass for incineration (Gerhardt et al., 2009). The
is straw due to its positive effects on biological activity and hence, pesticide plant activity depends on the medium to be remediated, the type of
biodegradation. However, access to straw can be limited in some regions, plant used, and also on the properties of the contaminant (Newman
and must be replaced by other more readily available residues. In this and Reynolds, 2004). Till date, the majority of phytoremediation re-
sense, recent works are focused on the improvement of the biomixtures search has focused on PAHs, PCBs, explosives, antibiotics, etc., and
employing novel materials for BB replace. Mukherjee et al. (2016) assessed very few studies are reported on the phytoremediation of pesticides
the sorption-desorption potential of three pesticides with different proper- (Lunney et al., 2004).
ties on novel biomixture materials based on bioenergy residues (biochar) Phytoremediation presents numerous advantages: reduced costs
in laboratory batch equilibrium experiments, determining that desorption in comparison to other remediation technologies, reduction of ero-
was hysteretic for all pesticides on the materials used, and concluding that sion rate, improvement of chemical, physical and biological soil
these biomixtures can be used as effective and alternative adsorbents for properties; land esthetic improvement and high population consen-
removing pesticides from percolating water in different biolters. Chin- sus. But it also presents some disadvantages such as the prolonger
Pampillo et al. (2015) prepared ve novel biomixtures using different lig- duration of land restoration, and its strong dependence upon: cli-
nocellulosic materials mixed with either compost or peat and soil to eval- matic conditions, contaminant concentration and bioavailability,
uate the dissipation of the insecticide carbofuran. Detoxication capacity of plant tolerance to contaminants, contamination area extent and
the matrices was high, and compost-based biomixtures showed better depth (limited by the rhizosphere or the root zone) or the disposal
performance than peat-based biomixtures. Gao et al. (2015) investigated of plant wastes. This technique is particularly suitable at sites
the effect of replacing peat by spent mushroom substrate (SMS), a locally where contamination is low and diffused over large areas, and
available material. The pesticides, chlorothalonil and imidacloprid were when there are no temporal limits to the intervention (Bini, 2009).
used in this research. They were selected based on the different physico- Table 6 shows some results obtained by using phytoremediation
chemical properties, biological activity and preliminary results on pesticide technologies in pesticide-contaminated soils.
degradation. The authors concluded that SMS is suitable and can therefore There are signicant differences in the tolerance of plants to pesti-
be used as a substitute for peat. Diez et al. (2013a) studied the effect of bio- cides. Karthikeyan et al. (2004) gave exhaustive information regarding
char as a partial replacement of peat in pesticide-degrading biomixtures the potential use of non-target plants such as trees, shrubs and grasses
for BBs. In general, pesticide degradation was higher in the control (con- in remediating pesticide-contaminated soil. White (2002) and White
ventional biomixtures) than in biomixtures prepared with biochar, except et al. (2003a) reported that the uptake of DDE was specic for certain
in the case of the herbicide iprodione, which presented a signicant bio- subspecies. Cultivars such as those from Cucurbitaceae family show sig-
degradation when biochar was included in the biomixture. Diez et al. nicant higher uptake. The difference was the result of higher exudation
(2013b) used two lignocellulosic materials (barley husks and pine saw- rates of low molecular weight organic acids. Also Murano et al. (2010)
dust) as substitutes for straw. The degradation of the six pesticides was en- observed that cucurbits have uptake mechanisms for dieldrin. Mitton
hanced for mixtures containing the new tested materials, concluding that et al. (2016) observed that sunower presented the highest
straw in the traditional biomixture can be replaced by other lignocellulosic phytoextraction capacity of endosulfan in comparison to tomato, soy-
materials to efciently degrade different pesticides. bean or alfalfa. However, in the case of DDT polluted soils, tomato plants
A combination of BBs and bioaugmentation (previously commented seem to be the most suitable phytoremediator candidates (Mitton et al.,
technique) is used to accelerate the efciency of biodegradation in the 2014).

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
16 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

Table 7
Selected reports on the use of vermiremediation in pesticide-contaminated soils.

Pesticide Pesticide class Scale Contamination in organism used/operation Results/pesticide removal Reference
soil conditions

Atrazine Triazine herbicide Laboratory Articially Lumbricus terrestris L. Half-life 23.6, 16.5 and 19.1 d in soil without Farenhorst
experiment contaminated worms, soil with worms, and soil conditioned et al.
(3.64 mg/kg) with worms prior to herbicide application, (2000)
respectively.
Isoproturon (I) dicamba Urea, benzoic acid and Laboratory Articially Aporrectodea longa After 28d 30, 20, and 90% of A, I and D, Gevao
(D) atrazine (A) triazine herbicides experiment contaminated respectively, remained as bound residue in soils et al.
(2.6, 0.2 and without earthworms; 5, 10, and 50%, (2001)
2 mg/kg, respectively, in soils with earthworms.
respectively)
Atrazine Triazine herbicide Laboratory Articially Lumbricus terrestres and 70% atrazine mineralized in soil without worms, Kersant
experiment contaminated Aporrectodea caliginosa. 60% in soil with worms. Only 30% mineralized in et al.
(1 kg/ha) Inoculation with burrow linings and 15% in casts. (2006)
Pseudomonas sp. ADP
Atrazine Triazine herbicide Laboratory Articially Aporrectodea Adsorption in earthworm casts higher than in Alekseeva
experiment contaminated giardia + Pseudomonas bulk soil. Degradation higher in bulk soil than in et al.
sp. ADP bulk soil + earthworm casts (2006)
Atrazine Triazine herbicide Laboratory Articially Lumbricus terrestres and Reduced mineralization from 15.2 to 11.7% in Binet et al.
experiment contaminated Aporrectodea caliginosa. the presence of earthworms at 86 d. Greater (2006)
(1 kg/ha) Soil columns leaching losses in soil amended with
earthworms.
-Cyhalothrin Pyrethroid and Laboratory Concentrations of Aporrectodea caliginosa After 34 d, 99, 21, 99.5, 28.1% of C, CE, Me, My, Schreck
(C) Chlorpyrifos-ethyl organophosphate experiment pesticides used in nocturna respectively, removed from soils without et al.
(CE) Metalaxyl (Me) insecticides vineyard soils. earthworms; 15, 4, 19, 17.2%, respectively, from (2008)
Myclobutanil (My) Phenylamide and soils with earthworms.
triazole fungicides
DDE Organochlorine Laboratory Old agricultural Eisenia fetida, Lumbricus DDE phytoextraction by ssp. pepo increased 25% Kelsey
insecticide (metabolite) experiment soil terrestris, Apporectodea in the presence of any of the earthworm et al.
(0.2 mg/kg) caliginosa species. No effect in ssp. ovifera (2011)
Plants: Cucurbita pepo
ssp. and ssp. ovifera
DDT Organochlorine Laboratory Articially Eisenia fetidaand, After 360 d, 25% DDT removed from soils Lin et al.
insecticide experiment contaminated (2 Amynthas robustus without earthworms, and 65% in soils with (2012)
and 4 mg/kg) earthworms.
PCP Organochlorine Greenhouse Articially Eisenia fetidaand, Both earthworm species enhanced soil PCP Li et al.
pesticide experiment contaminated Amynthas robustus disappearance. Earthworms introduce (2015)
(40 mg/kg) PCP-degrading bacteria into soils.
PCP Organochlorine Greenhouse Articially Eisenia fetidaand, After 42d A. robustus removed 82.5% PCP, and Lin et al.
pesticide experiment contaminated Amynthas robustus 50% E. Fetida. Both stimulated indigenous PCP (2016a,
(40 mg/kg) bacterial degraders. 2016b)

Phytoextraction of pesticides has mainly focused on food crops e.g. phytoremediation. White and Kottler (2002) and White et al. (2003b)
members of the genus Cucurbita known to extract from soil chlordane showed that several organic acids increased the desorption of DDE. Sim-
and DDT (Whiteld Aslund et al., 2010) or dieldrin and endrin (Otani ilarly Mitton et al. (2012) studied the effects of citric and oxalic acids
and Seike, 2006). Therefore, it would be very interesting to screen and plant root exudates on the desorption of DDTs in soils. These natural
non-food crops and other wild species for phytoremediation. As the se- organic acids alter the organomineral linkages disrupting the soil struc-
lection of a plant for phytoremediation purposes must be tailored for ture, and resulting in the release of metals and organic carbon in the
each environment to be treated, a good candidate should be naturally aqueous phase. Pesticides are usually complexed with this fraction of
growing vegetation in the pesticide-contaminated area or able to organic carbon, and, therefore, their desorption was enhanced. Also sur-
grow in the specic polluted soil. In both cases, plants should be able factants can enhance the desorption of pesticides from the soil to be
to decrease pollutant concentration (Ramrez-Sandoval et al., 2011; phytodegraded (Wu et al., 2008; Mitton et al., 2012).
Nurzhanova et al., 2013; Singh and Singh, 2014). As a recent advance in phytoremediation, in the last decade trans-
The effects of phytoremediation and microbial bioremediation strat- genic plants expressing specic pesticide-degrading enzymes have
egies have led to a more successful approach to remediation of organic been developed (Doty, 2008; Hussain et al., 2009). The overexpression
compounds. Rhizodegradation is a specic type of phytoremediation of genes involved in metabolism, uptake or transport of specic pollut-
that involves both plants and their associate rhizosphere microbes, ants in transgenic plants enable to overcome some of the disadvantages
whose growth is enhanced by the release of root exudates (Agnello of phytoremediation, such as high concentrations of pesticides or the
et al., 2014). Sun et al. (2004) observed that the enhanced removal of al- disposal of plants that accumulate organic pollutants (Kawahigashi
dicarb in plant-grown soil was mainly due to plant-promoted degrada- et al., 2006; Viktorova et al., 2014). Once pesticides are degraded by spe-
tion in the rhizosphere. The same was observed by Abhilash et al. cic transgenic plants to non-toxic metabolites or completely mineral-
(2013) in the phytoremediation of lindane and by Dubey and Fulekar ized, the plants can be disposed of safely. Although their eld
(2013) for cypermethrin. Microbe-assisted phytoremediation can be applications have not yet been regulated due to their possible impacts
also carried out by stimulation via inoculation with pesticides degrading on the environment and biodiversity, in the near future this strategy
microorganisms (Dams et al., 2007; Mitton et al., 2012). may receive an increasing attention.
Phytoremediation of pesticides is affected by a number of factors. As mentioned above, in the last decade there have been a growing
Their low bioavailability in soils may restrict the success of this technol- number of papers dealing with phytoremediation of pesticides under
ogy. In order to increase the ability of pesticides to be transferred from laboratory and greenhouse conditions, but efforts to translate
the soil to the degrader microorganisms, some of the natural low molec- phytoremediation research to the eld have proven challenging
ular weight organic acids excreted by roots were used to enhance (Gerhardt et al., 2009), and there have been numerous inconclusive

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx 17

and unsuccessful attempts, due to the multitude of variables: plant considerations in the decision-making process. However, no reports
stress factor, uneven distribution of contaminants, moisture content, have been found in the literature about the costs of remediation
spatial variability of microbial activity, changing climatic conditions, dif- techniques applied to pesticide-contaminated soils. As remediation
ferent soil properties, nutrient contents, aeration of the soil, etc. Al- of organic pesticides in soil can be done using any of the techniques
though the limits of this remedial strategy need to be acknowledged, developed for other organic pollutants with similar characteristics,
phytoremediation, and particularly rhizoremediation, have more po- the economic costs should be also similar. Costs associated with
tential than ever before for becoming cost-efcient and effective ways soil remediation are highly variable and depend on the contaminant,
of removing organic contaminants from the environment. soil properties, site conditions and the volume of material to be
remediated. Techniques that remediate a soil in site are less expen-
2.3.2.3. Vermiremediation. The term vermiremediation has been intro- sive than those that require excavation. According to Gruiz et al.
duced recently to indicate the use of earthworms in the removal of con- (2010), cost-benet assessment is part of spatial planning and com-
taminants from soils or when earthworms help to degrade non- plex land management, and has economic and social implications
recyclable compounds (Rodriguez-Campos et al., 2014). Several studies both for the owner and for local authorities. The cost-benet ratio
have reported on the accelerated removal of pesticides when earth- depends on the future land use, and does not always agree with the
worms were added to a contaminated soil, but there are other studies needs of nature and people.
that demonstrated the contrary (Hickman and Reid, 2008). Earthworm The most expensive remediation technology is excavation of con-
gut transit can greatly modify the structure of the soil, destroying and taminated soil and nal disposal on landlls. Policies regarding the re-
forming organomineral complexes The ability of earthworms to change mediation of such landlls vary considerably among different
the structure, biomass, and functioning of soil microbial communities countries, but all remediation projects are enormously expensive (US$
may indirectly stimulate POPs biodegradation, which depends predom- 22002400 ton1, Weber et al., 2011).
inantly on microbial activity (Natal-Da-Luz et al., 2012). Earthworm ac- With respect to soil washing/ushing technologies, Bini (2009) esti-
tivity is generally known to increase nutrient availability (water-soluble mated a cost of $50$80/m3 for in situ treatments, and $150$200/m3 if
C and carbohydrate concentrations, and extractable mineral N and the treatment is performed ex situ. For in situ ushing of contaminated
P) that can be used by soil microorganisms as co-metabolites, leading soils with alternate periods of water and water/surfactant was estimat-
to an increase in the biodegradation rate of pesticides (Meharg, 1996). ed a total cost of $104/m3 (Iturbe et al., 2004).
A number of studies have investigated the use of earthworms within The data currently available indicate that the cost of production for
bioremediation to enhance losses of pesticides in soil (Table 7). Gevao biosurfactants is between 1 and 60 USD/kg, depending on the degree
et al. (2001) observed a higher removal of atrazine, isoproturon and di- of purity and product specications required by the desired application
camba when the earthworm A. longa was added to soil, and concluded (Mao et al., 2015). Considering the huge production of synthetic surfac-
that earthworms not only limit the formation of the soil-bound fraction, tants and their lower average price (12 USD/kg surfactant),
but they also promoted the release and mineralization of bound residues. biosurfactant is currently not a cost-competitive substitute in the mar-
Other authors have also observed increased pesticide degradation in soils ketplace. Therefore, a massive and cost-effective production of
in the presence of earthworms (Farenhorst et al., 2000; Schreck et al., biosurfactant is very crucial to promoting its extensive use. There is no
2008; Lin et al., 2012). Kelsey et al. (2011) observed a decrease in hydro- information about costs of technologies such as EKSF because they
phobicity of humic acids in soil in the presence of plants and earthworms, need to be scaled up to be able to calculate their real cost.
and suggested that bioavailability of organic contaminants could increase. Although in situ technologies based on natural biological processes
Lin et al. (2016a, 2016b) used two earthworm species and revealed are particularly mistrusted due to lack of information, objective evalua-
that only one of them could enhance pentachlorophenol removal from tion and transparent verication, what we can know is the approximate
soil due to stimulation of indigenous PCP bacterial degraders; Li et al. cost for the different remediation processes. Conventional ex situ
(2015) also investigated the effect of two earthworm species on the methods, such as excavation and incineration, off-site storage, soil
soil microbial degradation of PCP, and observed that earthworms intro- washing, and in situ capping for stabilization are generally much more
duced new functional bacteria into soils for PCP biodegradation. expensive than in situ bioremediation.
Previous ndings are in conict with those of Binet et al. (2006) and In phytoremediation protocols are relatively easy to implement, and
Kersant et al. (2006) who observed an increased pesticide sorption due after initial site preparation and planting, the maintenance costs for
to earthworm activity. Alekseeva et al. (2006) observed that the transit phytoremediation are minimal (Gerhardt et al., 2009). The estimated
of OM through the earthworm gut leads to changes in its composition cost of phytoremediation is between $10 and $50/ton - $12$60/m3 if
(greater C, HA/FA ratio and degree of humication). All these changes we consider that 1 m3 of soil is about 1.2 ton - (Pilon-Smits and Free-
in the OM can also modify the pesticide-solid matrix (bioavailability), man, 2006), similar to the cost proposed by Gavrilescu (2005) ($60/m3).
and it can be more important the OM composition than its content For bioremediation using microorganisms, Gavrilescu (2005) esti-
that contributes to the enhancement of pesticide retention in soil. mated a cost of $6.4$150/m3, and Bini (2009), $50$100/m3 if the
Until today, all experiments with vermiremediation have been done treatment is in situ or $150$500/m3 if it is performed ex situ. The feasi-
in the laboratory or in outdoors mesocosms, but it is clear that earth- bility of cyclodextrins use concerning the price of bulk material is fre-
worms can help to remediate pesticide-contaminated soils. However, quently argued for not selecting them as remediation technology.
they need rather well dened conditions to survive, such as enough Gruiz et al. (2009) compared the use of cyclodextrin (RAMEB) as
food to be active, adequate climatic conditions and soil water content. bioavalability enhancer for in situ bioremediation with various realistic
On the other hand, the costs might be too high to remediate large con- alternative technologies (monitored natural attenuation, excavation
taminated areas. However, their contribution to soil quality should be and disposal on landlls, on-site bioventing, soil ushing with water
taken into account when calculating the cost of remediating a contam- (pump-and-treat)). They demonstrated that the cost-efciency was
inated soil with earthworms. More knowledge and research is required similar or even lower than in the others technologies, proving their ef-
in the eld so that the practical application of vermiremediation can be ciency and competitiveness. The estimated cost of this bioremediation
demonstrated on a large scale. technology using CDs was $220/ton, and the duration of the treatment
was only 1.5 years (for monitored natural attenuation the cost was
2.4. Economic analysis $218/ton, but the duration was 15 years). One of the strengths is that
CDs technologies are less time consuming than other alternative ones
Cost assessment and comparative cost evaluation of the potential (4070% lower than the other treatments), and it compensates the
technological alternatives may be some of the most important price of the bulk material.

Please cite this article as: Morillo, E., Villaverde, J., Advanced technologies for the remediation of pesticide-contaminated soils, Sci Total Environ
(2017), http://dx.doi.org/10.1016/j.scitotenv.2017.02.020
18 E. Morillo, J. Villaverde / Science of the Total Environment xxx (2017) xxxxxx

In the case of vermiremediation, the most important limitation for even 1980s. However, landlling may not be viable because of space
its use in contaminated soils is its cost, which might be too high to reme- limitations and its highly possible environmental concerns. According
diate large contaminated areas. Rodriguez-Campos et al. (2014) calcu- to the Stockholm Convention such highly polluted soils are not allowed
lated that for each ha of soil they would need 33,800 kg earthworms, to be landlled but need to be managed in an environmentally sound
and each kg costs about 40 USD. manner and pesticides destroyed without the generation of other POPs.
The majority of scientic studies published in the literature to date
3. Conclusions are still at the lab scale stage and were conducted using articially con-
taminated soils. In the present review a lack of studies exploring natu-
Pesticide occurrence in soils is a highly signicant environmental rally (eld) pesticide-contaminated soils and eld scale scenarios have
issue on which the attention of the scientic community is currently fo- been highlighted. Within the next few years a signicant effort should
cused. This review gives an overview on the technologies used for be done to scaling up these remediation technologies to be able to
pesticide-contaminated soils remediation. The fundamentals, advan- know their real cost and the possible operation problems at full-scale.
tages and disadvantages, progress and limitations of the technologies But, according with Lpez-Vizcano et al. (2017), here a problem arises:
are summarized and analyzed. For the different technologies, perspec- nancial support for doing large-scale studies is not easy to be obtained
tives are proposed for future research, and their limitations for applica- without the participation of companies, and in this case, they are inter-
tion are also discussed. ested in keeping the information to get a benet and non-disclosure
A number of techniques have been developed to remediate soils agreements prevent a good diffusion of results.
contaminated by pesticides, traditionally either by treating or isolating
the soil in situ, or by removing it for disposal or removal of the contam- Acknowledgements
inant, both by extraction or degradation. However, the selection of a
technique depends on its suitability for the extension of the contamina- This work was supported by the Spanish Ministry of Economy and
tion (point-source or diffuse pollution), type and concentration of the Competitiveness (MINECO) under the research project CTM 2013-
pesticide to be removed as well as the type of soil, climatic conditions 42599-R (co-funded by FEDER) and Junta de Andaluca in the frame of
and the presence of other potential contaminants. Social and economic
the project P12-RNM-894.
factors must also be taken into account, and the range of application can
be limited by energy and cost considerations.
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