Chemosphere 93 (2013) 626–636

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Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Review

Electrokinetic-enhanced phytoremediation of soils: Status and

opportunities
Claudio Cameselle a,⇑, Reshma A. Chirakkara b, Krishna R. Reddy b
a
Department of Chemical Engineering, University of Vigo, 36310 Vigo, Spain
b
Department of Civil and Materials Engineering, University of Illinois at Chicago, 842 West Taylor Street, Chicago, IL 60607, USA

h i g h l i g h t s

 Identify the weaknesses and strengths of the coupled technology electrokinetic–phytoremediation.

 Evaluate the influence of the main variables is the remediation results.
 Define the possible future research directions.

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

Article history: Phytoremediation is a sustainable process in which green plants are used for the removal or elimination
Received 3 February 2013 of contaminants in soils. Both organic and inorganic contaminants can be removed or degraded by grow-
Received in revised form 3 June 2013 ing plants by several mechanisms, namely phytoaccumulation, phytostabilization, phytodegradation, rhi-
Accepted 4 June 2013
zofiltration and rhizodegradation. Phytoremediation has several advantages: it can be applied in situ over
Available online 5 July 2013
large areas, the cost is low, and the soil does not undergo significant damages. However, the restoration of
a contaminated site by phytoremediation requires a long treatment time since the remediation depends
Keywords:
on the growth and the biological cycles of the plant. It is only applicable for shallow depths within the
Phytoremediation
Electrokinetic remediation
reach of the roots, and the remediation efficiency largely depends on the physico-chemical properties
Coupled technology of the soil and the bioavailability of the contaminants. The combination of phytoremediation and electro-
Soil remediation kinetics has been proposed in an attempt to avoid, in part, the limitations of phytoremediation. Basically,
the coupled phytoremediation–electrokinetic technology consists of the application of a low intensity
electric field to the contaminated soil in the vicinity of growing plants. The electric field may enhance
the removal of the contaminants by increasing the bioavailability of the contaminants. Variables that
affect the coupled technology are: the use of AC or DC current, voltage level and mode of voltage appli-
cation (continuous or periodic), soil pH evolution, and the addition of facilitating agents to enhance the
mobility and bioavailability of the contaminants. Several technical and practical challenges still remain
that must be overcome through future research for successful application of this coupled technology
at actual field sites.
Ó 2013 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627
2. Phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 627
3. Electrokinetic remediation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 628
4. Coupled EK and phytoremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 629
4.1. Evaluation of coupled technology at laboratory scale. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 629
4.2. Influence of the DC electric field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 630
4.3. Improvement with chelating agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 630
4.4. Application of AC/DC electric field . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 631
4.5. Remediation of contaminated water . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 631

⇑ Corresponding author. Tel.: +34 986 812318; fax: 34 986 812 180.
E-mail addresses: claudio@uvigo.es (C. Cameselle), rac2@uic.edu (R.A. Chirakkara), kreddy@uic.edu (K.R. Reddy).

0045-6535/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.chemosphere.2013.06.029
 C. Cameselle et al. / Chemosphere 93 (2013) 626–636 627

4.6. Influence of electrode configuration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 631

4.7. Impacts on soil properties and microbial community . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 632
4.8. Patents and field applications. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 633
5. Issues and opportunities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 633
5.1. Inorganic contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 633
5.2. Organic contaminants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 634
5.3. Mixed contamination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 634
5.4. Future research direction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 635
6. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 635
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 635

1. Introduction Phytoremediation, which involves the plants, is a green and sus-

tainable remediation technology, but it has several limitations to
The contamination of soils is a serious environmental problem be applied at actual contaminated sites. To overcome these limita-
and its occurrence is growing around the world. Human activities tions, coupling of phytoremediation with electrokinetic remedia-
such as agriculture, mining and especially industrial activities typ- tion (EKR) technology, which involves the application of a low
ically lead to contamination of soils in many ways. Contamination DC electric potential in the soil, has been proposed. The purpose
can be in the form of toxic heavy metals (e.g. Cd, Hg, Ni, Cu, and Cr), of this paper is to appraise the current state-of-the-art of coupled
inorganic compounds (e.g., F, CN, and arsenic compounds) and a phytoremediation and EKR technology and then identify various
wide variety of organic compounds (e.g., hydrocarbons, BTEX, PAH, technical issues that must be addressed through additional
PCBs, pesticides, and energetic compounds). In general, the most research.
common contamination of soils occurs in the form of heavy metals,
petroleum based hydrocarbon compounds and solvents, and agri-
cultural pesticides. 2. Phytoremediation
Despite the efforts spent in the last two decades, there is still no
reliable technology for the remediation of contaminated soils. In Phytoremediation is a green and sustainable process in which
addition, the cleanup of contaminated sites involves a series of green plants are used for the removal or degradation of contami-
expensive and time consuming tasks. Numerous technologies have nants in soils. Phytoremediation is primarily solar powered and
been developed to remediate contaminated sites; however, their thus more sustainable, especially compared to the typical mechan-
applicability is often limited to a particular type of contaminant ical approaches to contaminated site remediation. Vascular green
or site conditions. Moreover, many contaminated sites contain sev- plants have the excellent ability to self-engineer or exert limited
eral types of contamination simultaneously which makes the treat- control over the rhizosphere, local biogeochemistry, availability
ment of those sites even more difficult. Very few technologies have of water and nutrients and the local microclimate (McCutcheon
been proven to be efficient to address the problem of mixed con- and Schnoor, 2003). As such, phytoremediation is an important
tamination. Several methods available to treat mixed contami- part of ecological engineering. So far, phytoremediation has proved
nants include soil washing, stabilization and solidification, to be efficient for the treatment of large areas with low contami-
electrokinetic (EK) remediation, vitrification, bioremediation, phy- nant concentrations, at a very low cost compared to other remedi-
toremediation, pump and treat, in situ flushing, permeable reactive ation techniques.
barriers, and monitored natural attenuation (Sharma and Reddy, Furthermore, phytoremediation offers other benefits at contam-
2004). inated sites. It increases the soil microbial activity, stabilizes soil
Some of these technologies (e.g., soil washing, stabilization and reducing erosion and protects the soil of direct sunlight. It in-
solidification, and in situ flushing) require the treatment of soil creases the moisture content of the soil surface, reducing the for-
with chemicals. The major limitation of this kind of technology is
improper or inadequate delivery of reagents into low permeability
and heterogeneous soils and the possibility of contamination due
to the chemicals used for treatment. On the other hand, some of
those technologies (e.g., stabilization and solidification and vitrifi-
cation) are so intense that they dramatically change the texture
and properties of the soil mass. The final soil after the treatment
may not be appropriate for typical uses such as agriculture or nat-
ure preserve. Some of these technologies neither destroy nor re-
move all of the contaminants- instead they leave the
contaminants in the soil in a stabilized form (e.g. stabilization
and solidification, bioremediation of heavy metals, and vitrifica-
tion). There is a risk of future mobilization of contaminants in such
cases. Moreover, most of the methods mentioned above require
high amounts of energy consumption and long treatment times,
but their applicability is mainly limited by the high cost of the
treatment. In this context, phytoremediation appears to be a sus-
tainable, low cost, and environmentally friendly way of removing
contamination from soils by natural processes, with no significant
modification of the properties and texture of the soil after the
treatment. Fig. 1. Mechanisms in phytoremediation.
628 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
mation of dust and preventing the human exposure to soil contam-
inants. Plants also transpire considerable amounts of water that is
captured by the roots acting as a biological pump. This loss of
water can reverse the downward migration of chemicals by perco-
lation and can lead to absorption of surface leachate (Schnoor et al.,
1995).
Phytoremediation involves the removal, stabilization or degra-
dation of contaminants in soils and groundwater by plants (Shar-
ma and Reddy, 2004). Both organic and inorganic contaminants
can be accumulated in plant tissues or degraded by the enzymatic
activity of the plants. Alternatively, contaminants can be trans-
formed in other chemical species less bioavailable. The different
mechanisms involved in phytoremediation include rhizofiltration,
phytodegradation, phytoaccumulation (or phytoextraction), phy-
tostabilization, and rhizodegradation (also called phytostimula-
tion). These processes are depicted in Fig. 1.
Rhizofiltration is the removal of contaminants by the root mem-
branes when they pass from soil to root. Rhizofiltration has been
effectively demonstrated to remove heavy metals (Dushenkov
et al., 1995) and radionuclides like uranium (Lee and Yang, 2010)
in contaminated groundwater and aqueous solutions.
Phytodegradation is the plant’s capacity to break down the ab-
sorbed organic chemicals by plant metabolic processes (USEPA,
2000). Phytodegradation also includes the breakdown of contami-
nants in the soil if the degradation is carried out by compounds
produced by the plants like extracellular enzymes. Thus, phytode-
gradation of petroleum hydrocarbons (De Farias et al., 2009) can be
achieved in the soil even in the presence of heavy metals (Park
et al., 2011).
Phytoaccumulation or phytoextraction is the incorporation of
inorganic chemicals in plant tissue such as heavy metals (Cd, Cu,
Cr, Ni, Zn, Pb, Co, Mn, and Hg) and also As and Se (Vamerali
et al., 2010). In the cleanup of heavy metal contaminated sites, it
is necessary to use plant species with the capacity to hyperaccu-
mulate metals, especially in the aerial part of the plant Chaney
et al. (1997). Thus, after the remediation, the plant is harvested
and the biomass is disposed of in a secure way in a landfill with
or without previous incineration. Fortunately, there is a significant
number of species that accumulates metals in shoots and/or leaves
(Pulford and Watson, 2002; Bedmar et al., 2009; Vamerali et al.,
2010). Phytoaccumulation is a concentration technology that
leaves a much smaller mass to be disposed of compared to excava-
tion and landfilling (USEPA, 2000).
Phytostabilization of a heavy metal-contaminated substrate
may also be achieved by induced chemical changes to specific
metals, which result in becoming less bioavailable. Thus, deep
rooting plants could reduce the highly toxic Cr(VI) to Cr(III),
which is much less soluble and, therefore, less bioavailable. Men-
dez and Maier (2008) reported the phytostabilization of As, Cd,
Cu, Mn, Ni, Pb, and Zn in mine tailing even in arid and semiarid
environments.
Rhizodegradation is the degradation of organic contaminants
near the root mass by bacteria and fungi, which is stimulated by
the root exudes and enzymes released by the plants (USEPA,
2000). This process is also called phytostimulation because the
plant does not degrade the contaminants directly but creates the
necessary environment for the development of fungi and bacteria
that, in turn, degrade the contaminants. Thus, petroleum hydrocar-
bons (Maqbool et al., 2013) and polychlorinated biphenyls (PCBs)
(Kalinowski and Halden, 2012; Di Gregorio et al., 2013) can be de-
graded by rhizodegradation, although the soil texture (Maqbool
et al., 2012) and the use of surfactants (Memarian and Ramamur-
thy, 2012) may enhance the degradation.
Despite the ability and advantages of phytoremediation, the
application of phytoremediation has faced several limitations.
The action of the plants is limited to the maximum depth of
the growing roots, which have typical rooting depth from
20 cm to 2 m although the roots of some tree species may reach
10 m (USEPA, 2000, 2003). Another limiting factor is the slow
growth rate and low biomass production of naturally occurring
phytoremediation plants (Schwitzguebel et al., 2002). The uptake
of the contaminant (Baker et al., 1994) is limited by its toxicity
and bioavailability. Facilitating agents such us chelating agents
(Huang et al., 1997; Wu et al., 2007) and surfactants (Zheng
et al., 2007; Gao et al., 2008) can be used to increase the bio-
availability of contaminants. However, there have been concerns
about potential groundwater contamination by contaminant
leaching from the soil (Wu et al., 2007). As such, the addition
of chelating agents should be employed with caution and a thor-
ough understanding of subsurface geochemical and hydrologic
conditions.
3. Electrokinetic remediation
EKR is an environmental restoration technique especially de-
signed for the in situ treatment of contaminated soils (Reddy and
Cameselle, 2009). The technique is based on the application of a di-
rect electric potential to the contaminated soil by a series of elec-
trodes designated as anodes and cathodes. The application of the
electric potential induces a variety of reactions and transport pro-
cesses in the contaminated soil, which result in the mobilization
and transport of the contaminants towards the anode or cathode
electrodes for subsequent removal out of the contaminated soil.
The two main transportation mechanisms are called electromigra-
tion and electro-osmosis. Electromigration is the movement of io-
nic species in the electric field towards the electrode of opposite
charge. Electro-osmosis is the net flux of water induced by the
electric field through the porous structure of the soil. The elec-
tro-osmotic flux is the result of the combining effects of the electric
field and the electric charge on the surface of the soil particles.
Commonly, soil particles are negatively charged, and it results in
an electro-osmotic flow towards the cathode (Cameselle and Red-
dy, 2012).
The electric field also induces some reactions at the electrodes
and within the soil. These reactions include the electrolysis of
water, adsorption/desorption of contaminants on the solid particle
surfaces, redox reactions, and acid/base reactions. The global effect
of the chemical reactions during the EK treatment is a dramatic
change in soil pH, ion concentration in the pore water of soil, con-
taminant speciation, and contaminant dissolution or precipitation
(Reddy and Cameselle, 2009). In EKR, the operating conditions
and the addition of chemicals are specially designed to favor the
dissolution of contaminants and their transport out of the soil. In
cases where complete degradation of the contaminants is desired,
in situ chemical oxidation may be induced (Reddy and Chandhuri,
2009).
The EK technology has been researched for over last two dec-
ades for the removal of contaminants from contaminated soils.
The initial studies on EK focused on the removal of the heavy met-
als from soils. Subsequently, several studies investigated the re-
moval of recalcitrant and hydrophobic organic contaminants.
Some experimental studies focused on the restoration of soil con-
taminated with both heavy metals and hydrophobic organic con-
taminants. More recently, the combination of EK with other
remediation techniques was proposed and tested in an attempt
to develop new coupled technologies that use the advantages
and avoid the disadvantages of the individual technologies, gener-
ating a synergistic effect. Some of the technologies that can be
combined with EK are: bioremediation, chemical reduction/oxida-
tion, permeable reactive barriers, thermal desorption and phyto-
remediation (Reddy and Cameselle, 2009).
 C. Cameselle et al. / Chemosphere 93 (2013) 626–636 629

Table 1
Summary of laboratory studies of phytoremediation enhanced with electric current.

Plant Contaminant Treatment Amendment Application Voltage/intensity Reference

Period
Ryegrass Cu, Cd, As 98 d None 5 d after germination DC: 30 V O’Connor et al.
Continuous DC (2003)
Indian Mustard Pb 12 week EDTA EDTA and current after 12 week of DC: 0–40 V Lim et al. (2004)
growth.
1 h d1 for 9 d
Ryegrass Cu, Zn 50 d EDTA, EDDS Amendment after 42 d DC: 10 A m2 Zhou et al. (2007)
Electric current after 43 d, 6 h d1
for 7 d
Potato Zn, Pb, Cu, 90 d None Continuous AC or DC DC & AC: 500 mA Aboughalma et al.
Cd 30 d after planting (2008)
Lettuce Cd 60 d None Hydroponic culture, nutrient AC: 1 V cm1, 10 or 50 Hz Bi et al. (2010)
solution + Cd
Continuous AC
Indian mustard Cd, Cu, Pb, Off: 35 d None Continuous DC DC: 0, 1, 2, 4 V cm1 Cang et al. (2011)
Zn On:16 d 8 h d1 for 16 d
Rapeseed and Cd, Zn and Rapeseed: None 30 d for rapeseed AC: 1 V cm1 Bi et al. (2011)
tobacco Pb 90 d
Tobacco: 90 d for tobacco DC: 1 V cm1 switching polarity
180 d every 3 h
Kentucky Pb Urea Pre-grown plants DC: 500 mA Putra et al. (2013)
Bluegrass Continuous DC, 15 d

4. Coupled EK and phytoremediation
The combination of phytoremediation and EKR has been pro-
posed in an attempt to avoid, in part, the limitations of phytoreme-
diation (Hodko et al., 2000; Bedmar et al., 2009). Basically, the
coupled phytoremediation–EK technology consists of the applica-
tion of a low intensity electric field to the contaminated soil in
the vicinity of growing plants. The electric field may enhance the
removal of the contaminants by increasing the bioavailability of
the contaminants by desorption and transport of the contaminants,
even over short distances. Some significant variables that affect the
coupled technology are: the use of AC or DC current, the voltage le-
vel, the mode of voltage application (continuous or periodic), the
evolution of the soil pH by the electrolysis of water at the elec-
trodes, and the possible addition of facilitating agents to enhance
the mobility and bioavailability of the contaminants.
The effects of the electric fields on growing plants were re-
ported first by Lemstrom (1904). He investigated how the electric
field influences the plant characteristics. His investigations were
on the influence of electricity in agriculture and horticulture. He
exposed the plants to an electric field and compared them with
the control. It was found that most of the treated plants were
greener, and showed an increase in yield. These efforts in the early
20th century may have inspired present researchers in developing
a strategy of combining EKR with phytoremediation.
In the coupled phytoremediation–EK technology, the removal
or degradation of the contaminants is performed by the plant,
whereas the electric field enhances the plant activity by increasing
the bioavailability of the contaminants. Since the electric field effi-
ciently drives increased amounts of soluble heavy metals toward
plant roots, which results in stress conditions for the plants, hyper-
accumulator plants with a rapid growth period are considered the
best candidates for use in combination with EK techniques
(Bedmar et al., 2009). It should be mentioned that the sequential
use of both technologies may be possible. Phytoremediation can
be applied at the site after EKR to remove residual concentration
of contaminants and to achieve cleaner soil (Wan et al., 2012).
Moreover, the use of phytoremediation after EKR can contribute
to the recovery of soil properties altered or damaged by the EK
treatment, improving soil structure through the influence of root
system. The coupled phytoremediation–EK technology may lead
to more effective and efficient remedial strategy as compared to
the sequential use of these technologies. Table 1 summarizes the
conditions of some prominent studies of phytoremediation–EK
technology. These studies are commented in the following
sections.
4.1. Evaluation of coupled technology at laboratory scale
The use of a combination of EKR and phytoremediation to
decontaminate two metal-polluted soils has been demonstrated
in laboratory-scale reactors by O’Connor et al. (2003). These inves-
tigators used two different contaminated soils to test the ability of
ryegrass (Lolium perenne) to accumulate the heavy metals from the
soil with the simultaneous application of a constant DC electric
field of 30 V to a soil sample of 5.25 kg with the main electrodes
separated 18 cm. One soil was heavily contaminated with copper
(2500 mg kg1) and the other was contaminated with Cd: 300
and As: 230 mg kg1. As these soils were highly phytotoxic, a com-
mercial topsoil was mixed in the ratio 3:1 to achieve a suitable
contaminant level for plant growth.
The results from the test reactors with both soils showed that
the heavy metal contamination underwent a significant redistribu-
tion due to the EK movement of the heavy metals under the elec-
tric field and the partial uptake by the ryegrass. Both metals, Cu
and Cd were transported towards the cathode side. Metal content
was reduced by 90% on the anode side, about 50% in the center and
no removal was shown on the cathode side. These results conform
very well with the pH profile in the soil which is very acidic near
the anode and continuously increased towards the cathode where
it is slightly alkaline. There was not a significant accumulation of
heavy metals on the cathode side due to the presence of ryegrass
that partially accumulated the metals in its tissues.
The ryegrass growth and the analysis of heavy metal content in
the aerial part of the ryegrass showed a different behavior for Cu
and Cd contaminated soils. Thus, Cu contaminated soil supported
less grass growth than the Cd contaminated soil or the top soil
alone, which can be attributed to the greater phytotoxicity of the
630 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
Cu. It also explains why more Cu removed in the grass shoots in the
cathode side than in the anode side. The increasing amount of mo-
bile Cu on the anode might result in adverse effects on root growth,
lessening the potential for further uptake and transport of Cu to the
shoots. On the other hand, plants grew better in Cd contaminated
soil and the most Cd was removed by the shoots in the anode side,
where the Cd first increased its mobility by the effect of the electric
field. Unfortunately, a global mass balance for heavy metals was
not reported in O’Connor et al. (2003) due to the difficulty to eval-
uate the metal retained in the roots.
O’Connor et al. (2003) confirmed that the application of an elec-
tric current does not have severe adverse effects on the growth of
the plant, although the changes in the chemistry of soils provoked
by the electric field may inhibit partially the plant growth due to
soil pH changes, especially in the anode side, and increase in the
bioavailability of heavy metals that can interfere with the meta-
bolic processes of the plant. This preliminary study demonstrated
the good perspectives of the coupled phytoremediation–EK tech-
nology for the remediation of heavy metal contaminated soils,
although it requires validation under field conditions.
4.2. Influence of the DC electric field
The electric field intensity has a decisive influence on the effec-
tiveness of phytoremediation enhanced with EK. Cang et al. (2011)
have published an in-depth study of the influence of the DC electric
field on the removal of multiple heavy metals from a contaminated
soil by EK enhanced phytoremediation with Indian mustard (Bras-
sica juncea). The soil used was contaminated with Cd: 27.2, Cu:
838, Pb: 225 and Zn: 1360 mg kg1. The tests were carried out in
cylindrical pots with 1 kg of soil each. The Indian mustard was
grown for 35 d with no electric field. Then, the following different
voltage drops: 0, 1, 2 or 4 V; were applied to the pots for 16 d. The
electric current was only used for 8 h d1.
The results reported by Cang et al. (2011) confirm that low volt-
age enhanced the growth and development of Indian mustard,
whereas a decline in biomass production was observed with
increasing voltage. However, the mobility and bioavailability of
heavy metals was enhanced with the voltage. So, there was a
tradeoff between the bioavailability of the metals and the negative
effects of the voltage on the development of the plant. The optimal
approach is to use an intermediate voltage (in this case 2 V) where
the heavy metals can be mobilized with a minor effect on the
development of the plant. Thus, the best metal removal and accu-
mulation on plant tissues was achieved with 2 V. On the other
hand, the accumulation of metals in the plants also exerts a nega-
tive effect on their growth; that is why the test at 2 V showed the
least biomass production. Finally, it is very important to evaluate if
the Indian mustard can translocate the heavy metals in the roots
towards the shoots. Overall, higher accumulation was found in
the roots than in the shoots. It seems that longer cultivation times
are necessary for the plant to transport the metals from the roots to
the shoots. In a field application only the shoots are harvested, so
the metals accumulated in the roots will remain in the soil; this as-
pect was not addressed by Cang et al. (2011).
4.3. Improvement with chelating agents
The use of chelating or chelating agents is a common practice in
EKR (Reddy and Cameselle, 2009) as well as phytoremediation,
with the goal of heavy metal mobility and bioavailability. Lim
and others (Lim et al., 2004; Lim et al., 2012) investigated the
use of chelating agent (EDTA) alone and the combined use of EK
and EDTA on phytoremediation with Indian mustard. EK can deli-
ver EDTA into the soil facilitating the formation of soluble metal-
complexes as well as transport of metal–EDTA complexes towards
the root plants. The soil tested was sampled in a former apple orch-
ard site that was contaminated with Pb: 341, and As: 103 mg kg1
due to pesticide use. Tests were carried out in pots with 1.2 kg of
contaminated soil. The Pb in this soil posed a challenge to phyto-
remediation because of its low bioavailability due to Pb adsorption
to soil components (Butcher and Lim, 2007). EDTA favors the disso-
lution of Pb by forming two stable complexes: Pb(EDTA)2 with
stability constant of 1019.8; and PbH(EDTA) with stability constant
of 1023.0 (Morel and Hering, 1993).
The addition of EDTA to phytoremediation test clearly enhanced
the Pb uptake and its accumulation in the shoots of Indian mus-
tard. Without EDTA, no Pb was detected in the shoots and with
the addition of 0.5 mmol kg1 EDTA to the soil, the Pb concentra-
tion in shoots peaked at 700 mg kg1. The presence of EDTA also
increased the accumulation of Pb in the roots although the effect
is not as remarkable as in the shoots. Therefore, the use of the elec-
tric field and EDTA also caused the translocation of Pb from roots to
the shoots of Indian mustard. In general, the application of electric
field resulted in 2–4 times higher concentration of Pb in the shoots
than in the experiments with EDTA alone. The highest Pb concen-
tration in the shoots, around 1100 mg kg1, was reached with
5 mmol kg1 of EDTA and about 30–40 V. Moreover, Lim et al.
(2004) reported that the combination of EK, EDTA and phytoreme-
diation increased not only the amount of Pb remediated, but also
the speed of the remediation process.
Lim et al. (2004) studied the periodic application of electric po-
tential to the plants. This study was carried out because of the neg-
ative effect found in the development of the plants due to the EDTA
and the electric field, which decreases the biomass and the amount
of Pb remediated. The results showed that the application of the
electric voltage for 1 h d1 resulted in better metal uptake in a
shorter time. Moreover, as it was reported by Cang et al. (2011),
low voltages (10 V) were more beneficial than higher voltages
(30 V); although in the study of Lim et al. (2004), the difference
was not so remarkable.
Zhou et al. (2007) also studied the addition of chelating agents
to the phytoremediation enhanced by EK of a soil contaminated
with Cu: 1200–1550, and Zn: 1200–1550 mg kg1. The chelating
agents selected in this study were EDTA and EDDS (ethyl-
endiaminedisuccinic acid). The remediation tests were performed
with ryegrass planted in columns with 6 cm in diameter and
62 cm in depth. The novelty of this study is the direction of appli-
cation of the electric field. The cathode was placed at the bottom of
the soil column and the anode was installed 5 cm below the soil
surface. Thus, the electric field was applied vertically in order to fa-
vor the transport of the heavy metals towards the surface of the
soil, where the roots of the ryegrass were growing.
The results showed that the application of EDTA or EDDS to the
soil columns increased the concentrations of Cu and Zn in the
interstitial fluid along the column. The increase of soluble metal re-
sulted in a higher metal uptake by the ryegrass of Cu and Zn com-
pared with the test with no application of chelating agents. The
application of a vertical electric field along the column of soil re-
sulted in a significant redistribution of Cu and Zn. Thus, Cu and
Zn concentrations decreased in the interstitial fluid in the bottom
of the column, suggesting an effective control of the leaching risk
of Cu and Zn when the vertical electric field is applied. This is an
important point to consider in field applications. The addition of
chelating agents rapidly dissolves heavy metals forming the corre-
sponding complexes or chelates. It increases the bioavailability of
the heavy metals by the remediating plants, but at the same time,
the metals complexes may lixiviate toward the groundwater
spreading the contamination. The results reported by Zhou et al.
(2007) confirmed that the application of the electric field also
 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
enhanced the metal uptake by the ryegrass about 0.46–0.61 times
higher than the experiments without the electric field. The applica-
tion of the electric field also promoted the transportation of Cu and
Zn form the roots to the shoots.
The addition of chemical agents such as EDTA adds an increased
cost and may induce other environmental impacts, so the chemical
agent should be carefully selected in order to remove the desired
contaminant with low doses. Biodegradable chemicals may be
preferable for field applications.
4.4. Application of AC/DC electric field
Aboughalma et al. (2008) tested the capability of potato tuber to
remediate a soil contaminated with Zn, Cu, Pb and Cd. Tests were
carried out in pots whose dimensions were 330 by 280 mm, for
30 d. Then an electric current AC or DC was applied for 60 d until
plant harvesting, keeping the current intensity at about 500 mA.
They found that the application of a DC electric field to the pots in-
duced a significant change in the pH soil (initial pH = 6.5). The soil
pH decreased up to 3 near the anode and increased up to 8 near the
cathode. Heavy metals migrated from the anode side towards the
cathode, but they were accumulated (especially Zn, Cu, and Cd)
in the middle of the pot where the soil pH was 5. This behavior
was completely different from the test performed with AC electric
current. The alternate current did not provoke any transport or
accumulation of metals in the soil and no pH changes occurred
in the soil. The use of AC electric current was beneficial for the
development and growth of potato plant considering the biomass
production was 72% higher in this test than in the control test with
no electric current. However, the DC current resulted in 27% less
biomass than the control test, probably due to soil pH induced
by the DC electric field.
Metals were removed from the soil and accumulated in the po-
tato plant, mainly in the roots. The tests with AC electric current
showed higher accumulation of heavy metals in both roots and
shoots than the control test (no electric field) or the DC test. The
acidification or alkalinization of soil was the responsible of the lim-
ited result found in the DC tests, as well as the precipitation of met-
als in the center of the cell, which decreases their availability.
Bi et al. (2011) also studied the effect of AC and DC electric fields
on phytoremediation of heavy metal contaminated soils. Specifi-
cally, they evaluated the influence of the AC/DC electric fields on
the biomass production, increase in the ionic flux from the bulk
interstitial fluid to the roots and stimulate the metabolic activity
of the plant. Tobacco plants and rapeseed were cultivated in three
different soils: un-contaminated soil from a forest area, Cd spiked
soil (15 mg kg1) and multi-contaminated soil with Zn, Cu, Pb and
Cd (the same used for Aboughalma et al., 2008). AC (1 V cm1,
50 Hz) or DC (1 V cm1) electric fields were applied to the rapeseed
and the tobacco plants for 30 or 90 d respectively.
The application of a continuous DC electric field tends to induce
pH changes in the soil due to the acid and basic fronts generated by
the electrolysis of water (Aboughalma et al., 2008). In order to
avoid those negative effects, Bi et al. (2011) inverted the polarity
of the DC electric field every 3 h. Thus, the pH variation between
anode and cathode was eliminated and the comparison of the ef-
fects of DC and AC electric field on phytoremediation can be done
without the influence of the pH changes. Despite the DC polarity
inversion, Bi et al. (2011) reported that the plants reacted differ-
ently to the electric fields. AC electric current enhanced slightly
the production of rapeseed biomass, and gave a tendency to in-
crease the concentration of mainly Cu and Cd in plant shoots.
The total metal uptake by rapeseed was enhanced by AC field
mainly due to the beneficial effect on biomass production. On
the other hand, the AC field did not enhance the biomass produc-
tion of tobacco and the DC field showed a negative effect. AC field
631
slightly increased the metal uptake by tobacco. In general, the best
remediation results were found for both rapeseed and tobacco
when growing in the Cd spiked soil, probably due to the age and
availability of the heavy metals.
All of these studies show that the electric field enhances the
biomass production of phytoremediation plants, improves the me-
tal uptake and the translocation of metals from roots to shoots. AC
current tends to give better results because it does not provoke
alterations in the chemistry of the soil (i.e. metal redistribution
and pH change).
4.5. Remediation of contaminated water
Phytoremediation has also been investigated for the removal of
contaminants from groundwater (Adams et al., in press; Fester,
2013). It is difficult to design a system at laboratory scale for the
remediation of contaminants in a stream of groundwater. How-
ever, an electro-phyto-remediation study at lab scale was per-
formed in hydroponic cultures (Bi et al., 2010). The aim of this
study was to determine if AC electric field can improve the reten-
tion of Cd in the roots of lettuce and the possible translocation to
the aerial part of the plant. The concentration of Cd in the hydro-
ponic solution was 5 mg L1. An AC electric field (1 V cm1) was
applied to the pots with two different frequencies: 10 and 50 Hz.
These studies can simulate the feasibility of electro-phyto-remedi-
ation for the treatment of contaminated water and groundwater.
The results showed that the presence of the Cd in the hydroponic
medium inhibited the growth and development of the lettuce. How-
ever, the AC electric field had a positive effect stimulating the bio-
mass production and accelerating the metal ion uptake. The best
results in metal uptake were found in the test with 50 Hz AC electric
field. The electric current also favored the translocation of the metals
to the aerial part of plant. Overall, the efficiency of phytoremediation
was 90% higher under the influence of the AC 50 Hz electrical field
and 44% higher under the influence of the AC 10 Hz electrical field.
However, selectivity in metal uptake by the plant was detected.
Thus, the higher accumulation of certain metal ion could also limit
the capacity of the plant to accept other metal ions, causing a metal
competition effect in the plants. One of these competing metals ions
was Cu, which was present in the hydroponic medium at a small
concentration (0.025 mg L1). These results confirmed the viability
of the coupled electro-phyto-remediation technology for the treat-
ment of heavy metal contaminated groundwater; however, the
specificity of the heavy metal–plant system requires experimental
tests for each particular application.
Kubiak et al. (2012) tested the viability of the coupled electro-
phyto-remediation technology for the retention of arsenic in water.
Arsenic is a very toxic element for living organisms. Its toxicity and
its complex chemistry made it difficult to remediate in both water
and soils (Zabłudowska et al., 2009; Vithanage et al., 2012). Kubiak
et al. (2012) used a species of Lemna minor. Fresh water with no
pretreatment was contaminated with sodium arsenate at a concen-
tration of 150 lg L1 As. Unfortunately, in this study, no As uptake
by the plant was found; however, a strong depletion of As was ob-
served in the tests where current was applied. Preliminary results
showed that DC electric current caused 90% removal of As from the
spiked surface water. No evidence of interaction between EK and
phytoremediation was detected due to the lack of As uptake by
the plant. It should be pointed out here that the competition of P
and As for its adsorption by the plant could be the reason for the
insignificant uptake of As.
4.6. Influence of electrode configuration
EK–phytoremediation studies use a horizontal electric field
with one-dimensional electrode configuration. In practice, the
632 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
Fig. 2. Phytoremediation enhanced with electric fields. Possible electrode configurations to prevent leaching of contaminants to groundwater and to extend the remediation
deeper that the roots depth.
electrode configurations can vary and influence the effectiveness of
the coupled EK–phytoremediation technology. Zhou et al. (2007)
used a vertical direct-current electric field to favor the transport
of Pb towards the root zone. The vertical application of the electric
field extends the effectiveness of phytoremediation deeper than
the root zone. Furthermore, the vertical electric field prevents the
leaching of Pb towards the groundwater when it is mobilized by
the combined effect of the electric field and EDTA addition.
Hodko et al. (2000) proposed several electrode arrangements in
the phytoremediation enhanced by EK of a Pb-contaminated soil.
One of the proposed configurations placed the cathode in the cen-
ter, surrounded by anodes in the perimeter of the soil to be treated.
This configuration maximizes the acid front that mobilizes the Pb,
and minimizes the basic front to a small area around the cathode
(Alshawabkeh et al., 1999). Hodko et al. (2000) reported that the
application of the electric field induced much higher accumulation
of metals (in this case Pb) in the plants than in the tests conducted
with no electric fields. However, there is no detailed information
about the metal transport and redistribution in the soil after the
treatment. Hodko et al. (2000) also proposed several electrode con-
figuration in order to increase the depth of the soil where phyto-
remediation can be applied, preventing the leaching of the
mobilized metals into the groundwater (Fig. 2).
Recently, Putra et al. (2013) evaluated 2D electrode configura-
tion on the removal of heavy metals from a commercial top soil
spiked in the lab with lead nitrate at a concentration of
1000 mg kg1 Pb. Kentucky bluegrass (Poa pratensis L.) was culti-
vated in rectangular chambers whose dimensions were 180
(L)  60 (W)  180 (L) cm. Graphite electrodes were used as an-
odes, and they were installed vertically in the four corners of the
chamber. The cathode was a mesh of stainless steel placed on
the surface of the soil.
First, they evaluated the effectiveness of the electrode configu-
ration in a rapid test (48 h) using agar medium. The results showed
transport of Pb2+ from anode to cathode with increasing concentra-
tions from the bottom to the top of the chamber. A similar behavior
was observed when Pb contaminated soil was used, but the
movement of Pb was significantly slower due to the retention/
interaction with the soil. The researchers concluded that the 2D
electrode design could be used in EK–phytoremediation. Kentucky
bluegrass grew better in the experiments with electric current than
in the experiments with no current as it was observed by the bio-
mass production. Furthermore the electric field favored the accu-
mulation of Pb in both, the roots and the shoots, enhancing the
translocation of Pb to the shoots.
4.7. Impacts on soil properties and microbial community
EKR induces changes in the chemistry of the soil (Reddy and
Cameselle, 2009) that may negatively affect soil properties. The
most common effect is the acidification of the soil by the acid front
generated at the anode. Thus, the soil may become very acidic
(with pH of 2–3) and most of the natural microflora could disap-
pear due to the toxic effect of the acidic pH. On the other hand,
plant growth during phytoremediation favors the natural pro-
cesses in the soil that increase microbial and enzymatic activity.
This is why phytoremediation is considered a benign technology.
In fact, plants establish symbiotic relations with soil microorgan-
isms (Miransari, 2011), thus, the microflora increases the bioavail-
ability of the necessary nutrients for the plant, and in turn, the
plant releases substrate for the microorganisms as well as provide
the appropriate environment for their development. Phytoremedi-
ation can take advantage of the symbiotic relation plant–soil
microflora. Various metabolites produced by plant-associated mi-
crobes have been identified to be involved in many biogeochemical
processes operating in the rhizosphere, including nutrient acquisi-
tion, metal detoxification and alleviation of biotic/abiotic stress in
plants. Rhizosphere microbes release inorganic and organic com-
pounds that are thought to play an essential role in plant metal up-
take (Rajkumar et al., 2012) and in the biodegradation of
recalcitrant organic contaminants (Teng et al., 2011). Overall, phy-
toremediation enhanced with EK is a technology that includes sev-
eral processes, some are considered negative for the properties of
the soil while others are considered positive. Hence, the net change
 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
in the soil quality when applying the coupled EK–phytoremedia-
tion should be properly assessed based on the site-specific condi-
tions and post-treatment use of the site.
Cang et al. (2012) investigated the effect of electric current on
the physico-chemical properties of soil and its enzymatic and
microbial activity. The EK-assisted phytoremediation influenced
the soil physico-chemical properties, enzymatic and microbial
activities in the different soil regions (anode, center, and cathode)
especially in those tests with higher voltage (4 V). The results of
this study showed that the average content of soil of the following
parameters was increased with respect to the initial content: NO 3,
NHþ 4 , available P and K. Moreover, the soil urease, invertase and
phosphatase activities were strongly inhibited, but the basal soil
respiration and microbial biomass carbon near the anode and cath-
ode were significantly increased. However, plant growth increased
the soil enzymatic activity and partially counteracted the impact of
the DC electric fields on soil properties. The analysis of the results
concluded that the main variable that affected the soil properties
was DC electric field. On the other hand, the remediation can be
accelerated with the voltage applied (Cang et al. (2011). It can be
concluded that the selection of the electric field strength is a
trade-off between the acceleration of phytoremediation and the
negative effects on soil and microbial community.
4.8. Patents and field applications
There are no full-scale field applications reported in EK–phyto-
remediation. However, it is worth noting that several researchers
patented this coupled technology. The first patent was established
in 1998 by Rasking et al. (1998, 2000). These researchers claim that
phytoremediation of metal contaminated soil can be carried out by
species of the genus Brassica. They used crop or crop-related Bras-
sica species instead of wild species because they can be grown to
high biomass, are adaptable to various agroclimatic conditions,
can produce several crops per year and are amenable to genetic
manipulation. The preferred members of the Brassicaceae family
are those able to accumulate at least 10 times more metals in
shoots than in the contaminated soil. This invention can be applied
to Pb, Cr, Cd, Ni and Zn among other stable or radioactive metals. In
order to increase the bioavailability of the metals by the plants,
Rasking et al. (1998, 2000) proposed the use of chelating agents
in the soil, organic or inorganic acids (to decrease the soil pH at
least to 5.5 or less), and the use of DC fields. The researchers claim
that a direct current electric field applied across electrode pairs
placed in the ground induces motion of liquids and dissolved ions
as reported by Probstein and Hicks (1993); as a result, metal up-
take by the plant is enhanced. Unfortunately, there is no detailed
information in the patent about how the electric field is applied,
current or voltage values, heavy metal uptake and any remediation
results.
Hodko et al. (2000) registered a patent specifically oriented to
the application of EK to enhance the phytoextraction of contami-
nants from porous media. The researchers claim that their inven-
tion is a method for remediating soil, water and other porous
materials contaminated with organic and/or inorganic contami-
nants. The invention uses plants combined with electric field ap-
plied directly to the porous material to be decontaminated.
Hodko et al. (2000) reported that the electric field is used to control
the movement of the contaminants and enhance the removal of
contaminants. The contaminants are transported by the EK phe-
nomena: electro-osmosis and electromigration. So, both ionic and
non-ionic contaminants can be transported. In their invention,
the researchers claim that the EK phenomena are used to transport
the contaminants towards the rhizosphere. The contaminants can
be transported even from zones deeper in the soil than the root
zone, thus, the EK transport can extend the depth of activity, which
633
is limited to the root depth in phytoremediation alone (Fig. 2). As
Hodko et al. (2000) reported, the effectiveness of the remediation
is also enhanced by preventing the soil from becoming as strongly
acidic or basic as to kill the plant.
Pool (2005, 2007) combined the previous experience in EKR
with phytoremediation to patent a benign technology for the res-
toration of heavy metal contaminated soils. The electro-phyto-
remediation is defined here as the harvesting of plants to take up
ions and ion complexes from the soil, wherein spatial extent of
the uptake is increased by moving ions and ion complexes in the
soil around the roots of the plants under influence of electric fields.
The innovations of Pool’s patents are related to the electrode con-
figuration, the electric field strength and the mode of operation.
In electro-phyto-remediation, the contaminants are mobilized
and transported towards the rizhosphere, being captured by the
roots of the plants. Because the contaminants are not collected at
the electrodes like in EKR, a relatively simple electrode installation
can be used. For example, DC electric field can be applied to anodes
and cathodes encased in bentonite, without a liquid circulation
system. However, when the electrodes have no circulation system,
there is a risk of electrode clogging and developing of high acidic or
basic pH in the soil. The use of bentonite around the electrodes can
increase the time interval until clogging occurs, because of its high
buffering capacity (for both protons and hydroxyl ions). Other
materials with similar buffering properties can be used. However,
even in this case clogging will occur. This can be prevented by reg-
ularly changing the polarity of the electric current. A relatively
high frequency reduces the risk of clogging, but decreases the con-
taminant transport. On the other hand, a low frequency increases
the transport at the expense of an increased risk of clogging. The
time at which polarity to be switched is the key parameter for a
stable operation. Inventors claim that the suitable time to switch
polarity may be determined based upon the mobility of the con-
taminants, the pH-buffering capacity of the soil, and the applied
electric field strength. The inventors determined that the electric
charge that passed through the system (since the last switch) is
the most appropriate variable to determine the time to switch
the polarity. The electric charge threshold must be determined
experimentally for each application. The polarity has to be inverted
every time the charge threshold is exceeded. In practice, the polar-
ity is typically changed after a period of half a day to a couple of
days, depending on the site geochemistry after each application.
An additional aspect of Pool’s invention is related to the selec-
tion of the strength of the electric field. Contaminants are mobi-
lized and transported by the electric field. The roots of the plants
are able to absorb contaminants at a certain rate only. If the electric
field is too high, a fraction of the contaminants will pass by the
roots before they can be absorbed. Thus, electric power is wasted.
If the electric field is too small, the contaminants will be depleted
in the rhizosphere before they are replaced by new contaminants
transported by the electric field, increasing the remediation time.
So, the electric field strength has to be selected to match the trans-
port rate of the contaminants and the uptake rate of the plants. In
general, the electric power consumption of electro-phyto-remedi-
ation is low. Thus, renewable energy sources like solar or wind
power can be used, which extend the application of this technology
to areas where electricity is not available.
5. Issues and opportunities
5.1. Inorganic contaminants
Phytoremediation enhanced with electric field has great poten-
tial for the restoration of contaminated soils. Only a limited num-
ber of studies have investigated the applicability of this technology
634 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
for heavy metal contaminated soils. The reported studies use Cu,
Cd, Pb and Zn as typical metal contaminants. Although some stud-
ies use artificially contaminated soils, most of the literature refer-
ences use field contaminated soils obtained from industrial or
mining sites. It is widely known that aged heavy metal contamina-
tion is more difficult to remove than laboratory contaminated soils.
Thus, the feasibility of phytoremediation enhanced with electric
fields has been demonstrated based on the real field contaminated
soils. On the other hand, only six plant species were tested in the
investigations conducted on phytoremediation enhanced with
electric fields: ryegrass, Indian mustard, rapeseed, Kentucky blue-
grass, tobacco, and potato. However, phytoremediation has been
studied extensively (Bhargava et al., 2012) and several plant spe-
cies were reported to be useful for heavy metal accumulation or
for degradation of organic and inorganic contaminants (Bedmar
et al., 2009). The most promising plant species used in literature
for phytoremediation of heavy metal contaminated soils can be
used to evaluate if the application of AC/DC electric fields may im-
prove the metal bioavailability, the plant uptake and/or the trans-
location of metals to the shoots. Furthermore, the possible positive
or negative effects of the electric field on the plant and soil micro-
flora have to be considered. In fact, the removal of heavy metals by
phytoremediation is a complex phenomenon where the biotic
interactions in the rhizosphere exert a critical influence in the me-
tal uptake (Upadhyay, 2011; Rajkumar et al., 2012). Endophytic
bacteria (Cherian et al., 2012) and transgenic plants can be also
used to improve plant metal uptake (Seth, 2012). The influence
of these factors is still under investigation and there are no reports
on the possible influence of the electric field in the system soil-
microflora-plant.
The operating conditions reported in the literature shows that
the combination of phytoremediation with electric field shows
very interesting perspectives at lab scale and a promising future
in field application. However, the variables and conditions tested
are rather limited. More research is necessary to elucidate the ef-
fect of the main variables that affect this technology: voltage drop,
current intensity, AC/DC electric fields, and enhancing chemicals.
Moreover, the mechanisms of how the electric field affects or en-
hances the biomass production, metal uptake or metabolic activity
of the plant are still unknown. It is necessary to conduct more re-
search to understand the basic mechanisms that affect the system
plant–soil-electric field in order to be able to design stable and reli-
able field applications.
5.2. Organic contaminants
Organic contaminants are a major concern at many polluted
sites. Although enhanced phytoremediation with electric fields is
considered appropriate for the treatment of contaminated soils with
both organic and inorganic contaminants, no studies have reported
on remediation of organic contaminants in soils using electro-
phytoremediation. However, the degradation of organics has been
confirmed in phytoremediation alone (Teng et al., 2011; Fester,
2013). Even recalcitrant organics in soils can be satisfactorily treated
by phytoremediation with the appropriate plant selection. Thus,
PCBs (Ficko et al., 2011), PAHs (Teng et al., 2011), nitroaromatic com-
pounds, (Van Dillewijn et al., 2008), BTEX (Boonsaner et al., 2011;
Fester, 2013) and hydrocarbons (Macci et al., 2013) can be degraded
in soils by phytoremediation. Based on these studies, and similar to
the case of heavy metals in soils, it can be predicted that the electric
field will also enhance the phytoremediation of soils contaminated
with organic contaminants. In fact, it has been demonstrated that
the application of low intensity electric field, either AC or DC, stim-
ulates the growth and development of the plant, resulting in higher
biomass production. If the growth of the plant is enhanced by the
electric field, other physiological and enzymatic processes will be
also enhanced in the plant and in the rhizosphere. Thus, the degra-
dation of organic contaminants will be improved because it is
mainly associated with the microbial activity in the rhizosphere
and the enzymatic activity of the plant. In order to demonstrate
the possible beneficial effects of the electric field in the phytoreme-
diation of organic contaminants, it is recommended to select several
examples where phytoremediation showed limited efficiency, and
test if the electric field causes enhanced degradation and removal
of the organic contaminant. In these tests, the operational conditions
must be carefully selected to avoid any damage or growth inhibition
of plant and soil microflora. Since the rhizosphere is the place where
degradation mainly occurs, it is important to adjust the intensity of
the electric field to a value that not affects living organisms. Cang
et al. (2012) confirmed in heavy metals contaminated soils, that
the presence of the electric field decreased or increased in some ex-
tent the enzymatic activity and the basal soil respiration depending
on the strength of the electric field.
5.3. Mixed contamination
Contaminated sites usually contain a mixture of inorganic and
organic contaminants that require a more complex remediation
process. Phytoremediation is considered to be a potential technol-
ogy for the remediation of soils contaminated with both organic
and inorganic contaminants; however, there are only limited phy-
toremediation studies dealing with contaminant mixtures (combi-
nation of organic and inorganic contaminants), and these studies
have shown that phytoremediation is performed satisfactorily at
selected sites with mixed contaminants (Wang et al., 2013). In
general, it is difficult to remediate mixed contamination sites,
and the effectiveness of phytoremediation at such sites may be
limited due to synergistic effects, toxicity, growth inhibition and
low contaminant bioavailability, in mixed contaminated sites.
The possible crossed interactions among contaminants-soil–plants
will add more complexity to the system. The combined EK–phyto-
remediation technology has great potential to induce conditions
favorable for the simultaneous degradation and/or removal of
both organic and inorganic contaminants, but it has not been ex-
plored to date.
In general, heavy metals cause toxicity in the plant growth
resulting in less biomass production, but the toxicity also affects
the microorganisms in the soil, reducing the diversity and popula-
tion of fungi and bacteria in the rhizosphere. Thus, the degradation
of organic contaminants is reduced or even suppressed due to the
presence of heavy metals. More specifically, degrading hydrocar-
bon bacteria was inhibited by the presence of heavy metals (Al-
Saleh and Obuekwe, 2005). But in other cases, the presence of
co-contamination was favorable for the remediation process. Thus,
in soil co-contaminated with pentachlorophenol and Cu, the plant
species L. perenne L. and Raphanus sativus were observed to grow
better with increasing concentrations of Cu. This confirms that
combinations of inorganic and organic contaminants exert antago-
nistic effects on plant toxicity (Lin et al., 2006). On the other hand,
the remediation of hydrocarbons in the rhizosphere has decreased
the pH in the soil with the subsequent solubilization of heavy met-
als. Thus, the action of the microorganisms in the soil upon the or-
ganic contaminants increases the toxicity. One way to address the
remediation of mixed contaminants is to inject in the soil engi-
neered bacteria. Wu et al. (2006) used engineered Pseudomonas
putida to increase the sequestration of Cd in a sunflower culture
by reducing the toxicity. Wick et al. (2007) demonstrated that
the degradation of organic contaminants with a consortium of
microbes was more effective than the degradation with individual
microbes. So, it is important to favor the development of a wide
variety of microbes in the rhizosphere for optimal degradation
rates. This can be achieved with the co-culture of a variety of plant
 C. Cameselle et al. / Chemosphere 93 (2013) 626–636
species. The microbes associated to the rhizosphere are quite spe-
cific to the plant species. Moreover, it is widely accepted that bio-
diversity produces more stable and active ecosystems (Batty and
Dolan, 2013). It can be assumed that phytoremediation with multi-
ple plant species will result in better remediation of contaminated
sites with contaminant mixtures. The selection of plant species has
to be based on the results on individual cultures. But, when the
plants are growing in the same location, some species can develop
faster and outcompete neighboring plants. The dominant species
will colonize all the soil replacing other species, leading to a mono-
culture with low diversity. In this case, the phytoremediation can
be carried out with sequential cultures of one or more compatible
species. The difficulty of addressing mixed contaminated sites and
the limited information about their phytoremediation demonstrate
the need for additional research before this technology can be ap-
plied on a large scale. The application of electric fields to manipu-
late the conditions to favor the enhanced phytoremediation also
needs detailed investigation.
5.4. Future research direction
The coupled EK–phytoremediation technology has showed very
promising results for the restoration of heavy metal contaminated
soils. More research is necessary before this technology can be
used at field scale. It is necessary to test and select hyperaccumu-
lator plants of heavy metals, but it is even more critical to under-
stand the geobiochemistry involved in the degradation of
organics in the rhizosphere, as well as the influence of the electric
field in the physiology of the plants and soil microflora. Carefully
designed and monitored laboratory and field studies are necessary
to explore the fundamental and practical aspects of coupled EK–
phytoremediation. The following research lines are suggested:
Plant species: Test the technology with other plant species that
have shown their ability at accumulating or degrading organic
and inorganic contaminants.
Inorganic contaminants: Test a wider range of heavy metals and
combinations of them. Study the possible accumulation or degra-
dation of inorganic contaminants other than heavy metals (F, per-
chlorate, etc.).
Contaminant speciation: Determine the influence of heavy metal
speciation in plant metal uptake.
Organic contaminants: Study the possible degradation of organ-
ics with EK–phytoremediation.
Enhancing chemicals: Test a wider variety of enhancing chemi-
cals, focusing on biodegradable chemicals or natural products.
Mixed contamination: Test the feasibility of the technique for
soil contaminated with both inorganic and organic contaminants
with individual plant species. Test the feasibility of cultures with
various plant species.
Electric parameters: Determine the influence of the electric cur-
rent in the metabolism of the plant and contaminant uptake. Test
the influence of AC/DC electric fields with more plant species and
try to elucidate the mechanism of their influence in plant growth,
metal uptake and metal translocation.
6. Conclusions
Coupled EK–phytoremediation technology is an innovative
green and sustainable technology for the remediation of contami-
nated sites. This technology combines the advantages of each tech-
nology, while try to overcome the limitations of each individual
technology. This technology has been tested at the laboratory scale
with soils contaminated with heavy metals. Several studies dem-
onstrate that this technology improves biomass production of the
plants, enhances metal uptake, and favors translocation of the
635
metals from roots to shoots. The use of AC/DC electric fields, mode
of electric field application, and addition of chelating agents have
been tested. Overall, the best remediation results were found with
AC electric field or low DC voltage, in order to increase the bioavail-
ability of the contaminants and avoid damage and toxicity to the
plants. Phytoremediation is shown to be feasible for organic and
combination of organic and inorganic contaminants, but there
are no studies reported on combined EK–phytoremediation of or-
ganic or mixed contaminants. Phytoremediation enhanced with
electric fields is a benign technology for soil and the environment.
The adverse effect of the electric field caused by the electric current
on the soil microorganisms and enzymatic activity is partially
counteracted by the plant.
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