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Assessing

Phytoremediation’s Progress
DANIËL VAN DER LELIE ,

J E A N - PAU L S C H W I T Z G U É B E L ,

D AV I D J . G L A S S ,

JACO VANGRONSVELD,

AND ALAN BAKER


in the United States
and Europe
Although commercial success stories abound,
an urgent need still exists for more research
and demonstration projects.

hytoremediation—using plants and trees to ing track record of commercial success, more demon-

P remove or neutralize contaminants—holds


great promise for unobtrusively and cost-
effectively treating soils, groundwater, and
wastewaters contaminated with heavy met-
als, organic xenobiotics, and radionuclides. Although
still an emerging technology, the phytoremediation
market is fast-growing, especially in the United States
stration projects will be needed to prove that this new
green technology works, quantify its underlying eco-
nomics, and expand applications.

Scope of applications
Potential obstacles to large-scale application of phy-
toremediation technologies include the time required
and Europe (1). for remediation, the pollutant levels tolerated by the
Like any other new approach, phytoremediation plants used, and the fact that only the bioavailable
will only be accepted if its success is demonstrated. fraction of the contaminants will be treated. From eco-
The key factors are low cost (compared to classical re- logical, toxicological, and health points of view, the
mediation techniques) and aesthetic aspects, mak- bioavailable fraction should be the most important
ing it suitable for remediating large contaminated consideration, but present environmental regulations
sites in populated areas. are mainly based on total pollutant concentrations.
U.S. researchers pioneered phytoremediation An example application of a current risk-based
demonstration projects and can be largely credited for phytoremediation concept involves using metal-in-
the positive image that phytoremediation has today. activating soil additives such as coal fly ash or zeo-
As a result of its more conservative attitude toward lites combined with revegetation. Using these soil
demonstration projects, only a few successful, well- amendments strongly reduces the availability of met-
documented demonstration projects have been per- als to plant uptake and limits eventual toxicity to
formed in Europe (Table 1). plants, allowing revegetation of contaminated sites.
Comparison of recent developments in Europe Establishment of the vegetative cover markedly de-
and the United States shows that efforts to market creases metal leaching to groundwater and prevents
LOEL BARR

the technology are somewhat different on the two the dispersal of polluted dusts through wind and rain
sides of the Atlantic. Despite differences and a grow- erosion from formerly bare sites (2, 3).

© 2001 American Chemical Society NOVEMBER 1, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY I 447 A
TA B L E 1

European phytoremediation field projects


These projects, successfully carried out in Europe, indicate the range of applications possible for cleanup of sites contaminated with
heavy metals and organic compounds.

Site name, location Institution Plant species Contaminants

Czechowice oil refinery, Phytotech, Florida State Brassica juncea Pb, Cd


Katowice, Poland University, Institute for Ecology
of Industrial Areas

Former landfill, Switzerland Swiss Federal Institute Salix viminalis (willow) Zn, Cd
of Technology
Sewage disposal site,
United Kingdom University of Glasgow Salix species (willow) Ni, Cu, Zn, Cd

Zinc waste landfill, International Graduate School H. annuus, C. sativa, Zn


Hlemyzdi, Czech Republic Zittau Z. mays, C. halleri

Zinc/copper-contaminated site, Several Improved tobacco plants Cu, Cd, Zn


Dornach, Switzerland

Zinc/cadmium-contaminated Limburgs University Grasses for phyto- Zn, Cd, Pb, Cu


playing ground, Overpelt, and zinc stabilization
smelter site, Lommel, Belgium

Zinc/cadmium-contaminated soil, Limburgs University Brassica napus for Zn, Cd, Pb


Balen, Belgium phytoextraction

Oil well blowout, Trecate, Italy Battelle Europe Alfalfa, clover, corn, rye, Petroleum hydrocarbons
sorghum, and soy

BTEX-contaminated groundwater, Limburgs University Populus x canadensis BTEX (benzene, toluene,


Ghent, Belgium (poplar) ethylbenzene, xylene)

In contrast, phytoextraction requires the avail- modified plants, potential risks of transferring cont-
ability of metals to plants. In fact, amending the soil aminants to the food chain, and environmental im-
with chemical chelators that increase metal bioavail- pacts. An alternative phytoremediation enhancement
ability, uptake, and translocation in plants has been strategy might rely on improved interactions between
proposed as a way to overcome bioavailability limi- plants, rhizospheric bacteria, and mycorrhizal fungi,
tations, but this necessitates careful mass balances an approach that often assists plants in overcoming
to confirm that metals mobilized by chelators are not toxicity problems.
leached to groundwater. Using synthetic chelator The economics of phytoremediation is generally
chemicals is a questionable practice from an envi- favorable but can be improved. One option is using
ronmental standpoint. Natural chelators of plant or plants that provide added value by producing bio-
microbial origin seem more promising. Microbial pro- mass. For example, oil- or fragrance-producing plants
tection of plants against phytotoxic concentrations, such as vetiver, lavender, or coriander could be used
however, is often based on exclusion of heavy met- and their valuable oil and fragrance products recov-
als, and therefore, it is uncertain whether an approach ered. Alternatively, combustion can reduce the vol-
based on chemical chelators is practical for improv- ume of contaminated biomass, followed by selective
ing phytoremediation. recovery of heavy metals from residual ash.
Broadening the technology’s applicability will re- Depending on the type and concentration of the
quire using plants that perform better. This is partic- metal, this could provide an economically valuable re-
ularly true for phytoremediating metals, which cycled product.
requires plants with high biomass production and In developing phytoremediation strategies, pre-
heavy metal uptake and translocation capacities. harvest parameters (type and degree of pollution,
Plants phytoremediating organic xenobiotics would plant selection, treatability, agronomic techniques,
also need increased degradation potential. Use of ge- groundwater capture zone, uptake rate, transpiration
netically modified plants and organisms is conceiv- rate, and required cleanup time) and postharvest eval-
able, but this approach must consider the safety of uation parameters (collection, residues, waste dis-

448 A I ENVIRONMENTAL SCIENCE & TECHNOLOGY / NOVEMBER 1, 2001


posal, and contaminated plant material treatment) and was aimed at designing a suitable containment
must be considered. The success of phytoremedia- system for safe application of metal chelators.
tion thus depends on many biological, physical, and • Rhizodegradation investigated an integrated con-
chemical parameters with help from plant physiolo- cept for in situ remediation of hydrocarbons in soil
gists, agronomists, soil scientists, and engineers. through enhanced degradation by rhizospheric mi-
Creating multidisciplinary project teams to accom- croorganisms.
plish these tasks depends on funding opportunities, Over the past few years, however, European re-
and it is in this arena that differences between United search also has stronger involvement of small- and
States and European phytoremediation approaches medium-sized business enterprises. This might reflect
become evident. a general tendency to support more applications-
oriented research. EC-funded phytoremediation re-
Funding search is mostly aimed at heavy metals contamination,
Substantial funding has been allocated to phytore- despite the fact that soil and groundwater pollution by
mediation research in the United States and Europe, organic xenobiotics is a much more serious problem.
although the driving forces behind the type of re- Industrial funding for phytoremediation research
search performed in each of these markets differ. In has been very limited in Europe, and in general, much
Europe, phytoremediation research has been more of the long-term, ongoing research started in Europe
basic research-driven, with applications determined has been very broad-based research, supported by
by research outcomes. In the United States, phytore-
mediation research has always been more applica-
(a)
tion- and experience-driven. This may reflect a
U.S. culture supportive of entrepreneurship and risk
taking in business ventures, thereby accounting for a
larger, more mature phytoremediation industry and
a greater emphasis on applied research, even within
academia. Another explanation could be differences
in the types of funding support.
In Europe, the major opportunities involve basic
and exploratory research, although the increasing ten-
dency is for more applications-driven research, as
demonstrated by several phytoremediation projects
presently supported by the European Commission
(EC) 5th Framework Program (1999–2002):
• The Phytodec project is a decision support system
for quantifying the costs and benefits of using vege-
tation for managing metal-polluted soils and dredged
sediments. (b)
• Another project, Phytoc, evaluates willow planta-
tions for phytorehabilitation of contaminated arable
land and floodplain areas.
• Myrrh considers mycorrhizal fungi for phytostabi-
lizing radionuclide-contaminated environments.
• Mycorem explores whether mycorrhizal fungi oc-
curring at naturally contaminated sites confer toler-
ances to crop plants in soils polluted by heavy metals,
salts, and polycyclic aromatic hydrocarbons.
• Endegrade examines the use of endophytic bacte-
ria to improve plant degradation of organic xenobi-
otics.
• Last, Piramid combines artificial wetlands and sub-
surface reactive barriers for passive in situ remedia-
tion of acidic mine and industrial drainage.
Phytoremediation also received some support dur-
ing the previous 4th Framework Program (1995–1998).
These projects, which were more driven by basic re-
search than the projects presently funded by the EC,
included the following undertakings.
• Phytorehab compared strategies for rehabilitating
metal-polluted soils, including in situ phytoremedi-
ation, immobilization, and revegetation.
• Biorenew studies biomass fuel crops for bioremedi-
ating economic renewing degraded industrial lands. Thissite atM aatheide,Belgium ,heavilycontam inated
• Phytorem addressed phytoremediation of metal- w ith Zn,Cd,and Pb,isshow n here (a)before and (b)after
contaminated soil in a controlled land treatment unit phytostabilization using a 5% beringite soiladditive.

NOVEMBER 1, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY I 449 A


national funding. Research has only recently been di- Phytostabilization of heavy
rected to phytoremediation applicability, due to new
funding opportunities. metal-polluted soils, with or
In Europe, some coordination of phytoremedia-
tion efforts at the level of national research projects without addition of soil
and a successful network have been established under
the framework of COST Action 837 (http://lbewww. additives, is a proven
epfl.ch/COST837), a unique European initiative es-
tablished at the end of 1998. Several American pro- technology.
grams foster cooperation of various kinds, but they
often lack the interdisciplinary approach that COST
has assembled. In fact, a common complaint in the
United States among remediation professionals and plants, and contaminants in soils and sediments that
researchers alike is that engineers with remediation result in the degradation, extraction, volatilization, or
expertise and experience do not always communi- stabilization of waste chemicals. The program en-
cate with scientists who understand the underlying courages collaborations of life scientists with engi-
basis of the remediation approach. The ability of neers, and it is hoped that projects will take place on
COST Action 837 to bring together researchers with existing field sites controlled by the funding agencies.
different backgrounds is unique in this respect. At this writing, no grants have been awarded.
Early research on phytoremediating organic con- Industrial and private phytoremediation work in
taminants in the United States started in entrepre- the United States is also supported. Although it is a
neurial companies like Ecolotree, Phytokinetics, and larger effort than in Europe, we are not aware of pub-
Applied Natural Sciences. Some early applications- lished figures quantifying relative amounts of spend-
oriented research was conducted and funded by the ing on phytoremediation research in the American
U.S. EPA. In spite of long years of pioneering basic re- public and private sectors. Information on amounts
search on hyperaccumulation, metals phytoremedi- of industrial funding is often confidential and hard to
ation did not reach its current established level in the obtain. Many field phytoremediation projects un-
United States until the mid-1990s, with the founding dertaken in the United States have been conducted
of Phytotech. at sites owned by private companies, either as pilot
Most U.S. phytoremediation research is govern- research projects or as part of actual remediation ef-
ment funded—traditional federal support of acade- forts. Various chemical and petroleum companies
mic research, small business grants to companies for have led these efforts (4, 5), as well as industrial con-
applied research, and funding of remediation pro- sortia, such as the Petroleum Environmental Research
jects. Basic phytoremediation research is most com- Forum and the International Lead and Zinc Research
monly funded by individual competitive grants Organization.
awarded by government agencies, including EPA, the
U.S. Department of Agriculture (USDA), and the U.S. Applications and needs
Department of Energy (DOE). Individual research Phytostabilization of heavy metal-polluted soils, with
projects more specific to a given remediation prob- or without addition of soil additives, is a proven tech-
lem are funded by these agencies, as well as by var- nology, as indicated by the many successful studies
ious services within the U.S. Department of Defense in both Europe and the United States. In Europe, one
(DOD). Several programs within or among agencies, of the most successful examples was the use of berin-
such as the DOD/DOE/EPA Strategic Environmental gite for treating a site heavily contaminated with Zn
Research and Development Program (SERDP) and and Cd at Maatheide, Belgium (see photos on pre-
DOD’s Environmental Security Technology vious page). Beringite is a modified aluminosilicate
Certification Program have actively funded phytore- that originates from the fluidized bed burning of coal
mediation laboratory and field projects. Because the refuse from the former coal mine of Beringen
funding comes from divisions of these agencies de- (Belgium). The high metal immobilizing capacity of
voted to solving real-world environmental problems, beringite is based on chemical precipitation, ion ex-
the projects by their very nature are more applica- change, and crystal growth. Unfortunately, this ad-
tions-focused. ditive is no longer available. Several studies are
A limited number of larger-scale funding programs seeking alternatives. Although these initiatives are
in the United States focuses on phytoremediation. strongly supported by regional and national gov-
EPA has funded phytoremediation research at the ernments, indicating their willingness to accept in
Great Plains/Rocky Mountain Hazardous Substance situ immobilization as a remediation strategy, most
Research Center (HSRC) for about 10 years. Although recognize a need for cost-effective systems to mon-
this program is based at Kansas State University, funds itor the sustainability of phytostabilization (3).
have been distributed to 14 U.S. universities. In Because physical, chemical, and ecological parame-
September 2000, a competitive phytoremediation ters were all evaluated at the Maatheide site during
grant program was announced as a joint effort of EPA, the past decade, it provides an excellent example of
the National Science Foundation, the Office of Naval the sustainability of heavy metal immobilization
Research, and SERDP. Applications were solicited for combined with revegetation (2). Similar experiments
field research projects addressing the fundamental have been performed near a copper rod plant in
interaction mechanisms among microorganisms, Prescot, United Kingdom (6).

450 A I ENVIRONMENTAL SCIENCE & TECHNOLOGY / NOVEMBER 1, 2001


Phytoextraction of heavy metals has been success- otics and to use this information to improve phy-
fully applied, mostly in the United States. The most toremediation efficiency in the field.
publicized example was Phytotech’s (now part of Although many organic pollutants are metabolized
Edenspace Corp.) phytoextraction of lead at a in plants, some xenobiotics can be toxic, limiting the
Superfund site in New Jersey—a facility formerly oper- applicability of phytoremediation. Moreover, in phy-
ated by a battery manufacturer (7 ). Phytotech has also toremediating volatile organic chlorinated compounds,
phytoremediated a lead-contaminated site in Bayonne, BTEX (benzene, toluene, ethylbenzene, xylene), and
NJ, and at a residential site in Dorchester, MA. MTBE (methyl tert-butyl ether) plants can release the
Phytomining of nickel is newer. Its primary aim is compounds and their metabolites to the atmosphere,
cost-efficient nickel mining instead of decontamina- which udermines the merits of phytoremediation for
tion. Nickel has a high value on the world market, these applications. This problem has prompted sever-
compared with other heavy metal contaminants, such al researchers to examine alternative strategies, in-
as cadmium, zinc, and lead. Moreover, several high cluding the use of improved rhizodegradation.
biomass-producing natural nickel-hyperaccumula- However, although rhizospheric microorganisms can
tor plants such as the South African Berckheya rod- improve phytoremediation of hydrophobic com-
dii are available. Recently, a hyperaccumulator fern pounds, such as hydrocarbons, recent results suggest
(Pteris vittata) was discovered for arsenic, which could that numerous compounds enter the plant faster than
also lead to interesting applications (8). soil microflora can degrade them (13).
An ideal plant for metal phytoextraction is toler- A study of phytoremediation of hydrocarbon-pol-
ant to accumulated metal concentrations and accu- luted agricultural soils that was successfully con-
mulates metal(s) in aboveground leaves and stems. ducted in Trecate, Italy, is instructive (14). Soil
It should also have fast-growing biomass that is high- contaminated following a blowout of a land-based
ly metal-accumulating and easily harvested (9). In oil well underwent treatment in a biopile before
addition, genetic engineering of plants opens up new being replaced in its original location. During three
possibilities for phytoremediating metal-polluted growing seasons, the ability of 11 agricultural plants
soils. Several metal transporter genes from small hy- to stimulate hydrocarbon removal via microbial
peraccumulator plants have been characterized, and degradation and plant uptake was compared with
these may be a potential source of genes for high bio- land farming and natural attenuation. Total petrole-
mass-producing hyperaccumulators. Another strate- um hydrocarbon reduction during the third season
gy for remediating metals involves introducing ranged from 0.21 to 0.57 kg/m2 in planted parcels,
gene-encoding enzymes (often bacterial) that detox- whereas the average reduction in land-farmed
ify metals by changing their redox state or by chem- parcels was only 0.01 kg/m2. Maize and sorghum
ically converting them into less hazardous were very efficient for such applications. Other hy-
compounds. drocarbon phytoremediation projects are under way
Phytoremediating organic xenobiotics is becom- in Europe (13).
ing increasingly popular as an unobtrusive, cost- A special phytoremediation application is con-
effective remediation strategy and is enjoying con- structed wetlands for cleanup of effluents and
siderable commercial use and success in the United drainage waters. For example, a constructed wetland
States. Several European and U.S. academic research near Aveiro in Portugal has successfully treated in-
teams are working to unravel the mechanisms un- dustrial effluents containing nitrogenous aromatic
derlying uptake, transformation, and accumulation of compounds from an aniline and nitrobenzene pro-
organic pollutants, such as pesticides, chlorinated duction plant for several years (project Reciclam). Up
solvents, and sulfonated aromatic compounds re- to 100% reductions in aromatic compounds are ob-
leased by dye and textile industries. tained using reed beds on a total planted area of
It is becoming increasingly clear that plants con- 10,000 m2. The reduction efficiency depends on the
tain a complex array of enzymes that can detoxify acclimatization period for inlet effluent compositions
herbicides and other xenobiotics (10–12). Plants read- of 10–300 mg/L aniline, 10–100 mg/L nitrobenzene,
ily take up moderately hydrophobic soil contami- and 10–30 mg/L nitrophenols.
nants having log Kow values between 0.5 and 3.5, and The U.S. Army Corps of Engineers, Waterways
rhizospheric microorganisms can degrade more hy- Experiment Station in Vicksburg, MS, is developing a
drophobic pollutants. More research is required to wetlands system to treat groundwater contaminated
better understand and exploit the interactions be- with 1 mg/L TNT (2,4,6-trinitrotoluene) and up to 13
tween plants, microorganisms, and organic xenobi- mg/L RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine).
Laboratory studies led to the selection of three aquat-
ic species: coon-tail (Ceratophyllum demersum),
Phytoremediating organic pondweed (Potamogeton nodosus), and emergent ar-
rowhead (Sagittaria latifolia), which all reduced TNT
xenobiotics is becoming levels by 95%, and RDX by 80%. It is believed that re-
mediation using these species involves endogenous
increasingly popular as an enzyme systems (nitroreductase, dioxygenases, and
laccase). A full-scale trial has been initiated (15, 16).
unobtrusive, cost-effective Radionuclide phytoremediation is less well docu-
mented, but some trials have been performed.
remediation strategy. Laboratory and greenhouse studies have determined

NOVEMBER 1, 2001 / ENVIRONMENTAL SCIENCE & TECHNOLOGY I 451 A


Radionuclide is an urgent need for research aimed at fundamen-
tal understanding of mechanisms involved in soil
phytoremediation is less and plant compartments and demonstration pro-
jects to optimize the phytoremediation process and
well documented, convince regulators and the general public of the
technique’s applicability.
but some trials have been
Acknowledgment
performed. D.v.d.L. is supported by Laboratory Directed Research
and Development funds at the Brookhaven National
Laboratory under contract with the U.S. Department
the phytoremediation potential for removing low lev- of Energy.
els of Cs-137 at a former waste disposal site at
Argonne National Laboratory’s facility in Idaho. References
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present in test soils. In field trials, redroot pigweed diation really deliver what industry needs? In IBC’s 4th
Annual International Conference on Phytoremediation,
(A. retroflexus L.) showed the best performance, ac- Toronto, Ontario, Canada; June 23–25, 1999; International
cumulating ⬎900 pCi/g, well over the goal of 300 Business Communications: Southborough, MA, 1999.
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Outreach (14) Plata, N. Ph.D. Thesis Nr 2306, EPFL, Lausanne,
Initiatives have been undertaken to improve the dis- Switzerland, 2000.
(15) Hughes, J. B.; Shanks, J.; Vanderford, M.; Lauritzen, J.;
semination of results to the general public and the sci- Bhadra, R. Environ. Sci. Technol. 1997, 31, 266–271.
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phytonet), the EPA’s Citizen’s Guide to Phytoreme-
diation (http://cluin.org/products/citguide/phyto2. Daniël van der Lelie is a senior scientist at Brookhaven
htm), and a forthcoming publication by the Interstate National Laboratory, Upton, NY. Jean-Paul Schwitzguébel
Technology and Regulatory Cooperation Working is senior scientist at the Swiss Federal Institute of
Group, which explains phytoremediation and its ap- Technology Lausanne, Laboratory for Environmental
plications primarily for state and local regulators. In Biotechnology, Lausanne, Switzerland and the chair of
addition, the Kansas State University HSRC program COST Action 837. David J. Glass is the chief executive of-
sponsors the Phytoremediation Discussion Group ficer at Applied PhytoGenetics, Inc., Athens, GA, and head
(www.engg.ksu.edu/HSRC/phytorem). of D. Glass Associates, Inc., Needham, MA. Jaco
These undertakings primarily target the scientif- Vangronsveld is a professor at Limburgs Universitair
ic community rather than the general public and are Centrum, Centre for Environmental Sciences, Diepenbeek,
aimed at creating discussions among scientists from Belgium. Alan Baker is professor at the University of
different disciplines. Overall, the message is that there Melbourne, Parkville, Victoria, Australia.

452 A I ENVIRONMENTAL SCIENCE & TECHNOLOGY / NOVEMBER 1, 2001

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