You are on page 1of 8

Chemosphere 136 (2015) 4249

Contents lists available at ScienceDirect

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

Humic substances from sewage sludge compost as washing agent


effectively remove Cu and Cd from soil
Dorota Kulikowska , Zygmunt Mariusz Gusiatin, Katarzyna Bukowska, Katarzyna Kierklo
Department of Environmental Biotechnology, University of Warmia and Mazury in Olsztyn, 10-719 Olsztyn, Poland

h i g h l i g h t s
 Humic substances (HS) from compost showed good surfactant properties.
 HS effectively removed Cu and Cd from contaminated soil.
 Cu and Cd removal efciency was higher for sandy clay loam than for clay.
 Soils washing with HS enable decrease of Cu and Cd ecological risk (on Er index).

a r t i c l e

i n f o

Article history:
Received 30 August 2014
Received in revised form 5 March 2015
Accepted 24 March 2015
Available online 15 May 2015
Handling Editor: Jrg E. Drewes
Keywords:
Soil washing
Cu
Cd
Humic substances
ER index

a b s t r a c t
Although commercially available biosurfactants are environmentally friendly and effectively remove
heavy metals from soil, they are costly. Therefore, this study investigated whether inexpensive humic
substances (HS) from sewage sludge compost could effectively remove copper (Cu) and cadmium (Cd)
from highly contaminated sandy clay loam (S1) and clay (S2). The optimum HS concentration and pH
were determined, as well process kinetics. Under optimum conditions, a single washing removed
80.7% of Cu and 69.1% of Cd from S1, and 53.2% and 36.5%, respectively, from S2. Triple washing increased
removal from S1 to almost 100% for both metals, and to 83.2% of Cu and 88.9% of Cd from S2. Triple
washing lowered the potential ecological risk (Eir) of the soils, especially the risk from Cd. HS substances
show potential for treating soils highly contaminated with heavy metals, and HS from other sources
should be tested with these and other contaminants.
2015 Elsevier Ltd. All rights reserved.

1. Introduction
Soil washing is one of the most effective forms of remediation
because it allows rapid cleanup of a contaminated site, it reduces
or eliminates long-term liability, and it is cost-effective. This process is based on the desorption of pollutants from contaminated
soils through the action of various agents. Washing agents that have
been commonly used include inorganic acids, such as sulfuric and
hydrochloric acids, organic acids, including acetic and citric acids,
and chelating agents like ethylenediaminetetracetic acid (EDTA)
and nitrilotriacetic acid (NTA) (Mulligan et al., 2001).
Interest in biosurfactants derived from microbes and plants has
been increasing, mainly because of their high capacity to bind with
metal ions, which allows them to effectively remove heavy metals.
Most studies on biosurfactants have been done with microbial
rhamnolipids (Wang and Mulligan, 2009a; Elouzi et al., 2012;
Corresponding author.
E-mail address: dorotak@uwm.edu.pl (D. Kulikowska).
http://dx.doi.org/10.1016/j.chemosphere.2015.03.083
0045-6535/ 2015 Elsevier Ltd. All rights reserved.

Meng et al., 2014), which have been shown to be highly effective


at removing different heavy metals from contaminated soils. In
addition, surfactants derived from plants have been shown to be
equally effective for soil washing. Saponin can effectively remove
Cd and Zn from clay loam, loam and sandy clay loam (Hong et al.,
2002), or Cu and Ni from kaolin (Chen et al., 2008). This is due to
the ability of the carboxyl groups on saponin to form complexes
with heavy metals, as shown by FTIR analysis (Hong et al., 1998).
Similarly, saponin and tannic acid can effectively remove heavy
metals and metalloids from both articially contaminated soils
and highly contaminated industrial soils (Gusiatin and Klimiuk,
2012; Gusiatin, 2014). However, the main drawback to both microbial and plant biosurfactants is their high price. Thus, there is a need
to nd washing agents that are equally effective but much cheaper.
The structural characteristics of humic substances (HS) from
urban green waste led to predictions that these compounds would
have good properties as complexing agents, ion-exchangers and
surfactants (Montoneri et al., 2009). This is because these substances are amphiphilic, with both hydrophobic and hydrophilic

43

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

components. In addition, their carboxyl and hydroxyl groups can


form complexes with heavy metals. Indeed, studies with industrially produced humic acids (HA) (leonardite humic acid; standard
humic acid purchased from International Humic Substances
Society; Aldrich humic acid, commercially available from Sigma
Aldrich) have conrmed that they can remove heavy metals
(Conte et al., 2005; Tsang and Yip, 2014). Unfortunately, these
commercial HA are expensive.
Although HS extracted from compost would have the advantage
of very low costs, we are not aware of any studies on the suitability
of these substances for washing soil contaminated with metals.
Because the properties of HA from compost differ from those of
industrial prepared HA (Klavins and Purmalis, 2010), there has
been a need to perform this kind of study.
In HS, HA and fulvic acids (FA) are distinguished. These fractions
differ in their molecular weight, number of functional groups,
degree of polymerization and elemental composition. The degree
of polymerization of FA is less, which means that they have a
lower molecular weight (5002000 Da), whereas the polymerization degree of HA is greater, as is their molecular weight
(50 000100 000 Da) (Stevenson, 1994). FA from soil contain less
carbon and more oxygen, which is present in numerous carboxylic
groups. This means that the carbon content is similar to the oxygen
content (4050%) in FA. HA from soil contain 5358% carbon and
3238% oxygen (Steelink, 1985). Many authors indicate that the
composition of HA from sewage sludge compost is similar to that
of HA from soil (Amir et al., 2005; Kalsom et al., 2006). FA contain
more functional groups than HA, mainly carboxylic (61.888.4%)
and hydroxyl (11.637.2%) groups. Many reports show that FA,
due to their higher content of functional groups, are generally the
fraction of humic substances that mainly reacts with metals,
irrespective of the acids origin (natural/polluted soils or compost).
Fulvic acids can act as metal carriers, mainly due to their lower
molecular weight and higher content of functional groups.
Boruvka and Drbek (2004) showed that in heavily polluted
Fluvisol soils, 98% of the organically bound Cd was in the fulvic fraction, as was 82% of Pb and 96% of Zn. A similar observation was made
by Donisa et al. (2003), who found that Cu, Cd and 9 other elements
were bound more with the fulvic than the humic fraction in natural
soils (andosol, podzol, cambisol). This means that both fractions of
HS (HA and FA) may act as metal carriers and fractionation of humic
substances into HA and FA may not be needed.
Therefore, we assessed the effectiveness of humic substances
recovered from compost for removing heavy metals (Cu, Cd) from
soils in single and multiple washing and metal distribution patterns. In addition to process efciency, ecological risk of individual
metal (Eir) was calculated. The (Eir), which has been widely used for
sediments, is directly related to metal toxicity and its mobility.
2. Materials and methods
2.1. Sampling and soil characterization
Samples of unpolluted surface soil (depth 030 cm) were
collected from two locations in Warmia and Mazury Province in
north-eastern Poland: Baranowo (soil S1) and Wiktorowo
(soil S2). The samples were air-dried and ground to pass through a
1-mm sieve, then homogenized and stored until analysis.
Physicochemical characteristics of the soils are shown in Table 1.
2.2. Soil contamination
The soil spiking procedure was adapted from Thawornchaisit
and Polprasert (2009). Each soil was contaminated by an individual
metal: for this purpose, 500 mL containing dissolved mixture of

Table 1
Physicochemical characteristics of experimental soils.
Characteristic

Unit

Soil S1

Soil S2

Sand content
Silt content
Clay content
Texture
Organic matter
CEC
pH (H2O)
Total Cu
Total Cd

%
%
%

%
cmol (+) kg1

mg kg1
mg kg1

64
16
20
Sandy clay loam
1.6
12.3
7.1
36
0.3

6
33
61
Clay
10.3
53.3
6.1
95
1.1

CuSO45H2O and 3CdSO48H2O salt were added to 500 g of airdried soils at concentrations of 2000 and 50 mg L1, respectively.
The samples were mixed for homogeneity by shaking overnight
(100 r min1), left at room temperature for one month with
frequent thorough mixing, then dried at 10305 C to a constant
mass, and nally ground manually and passed through a 1 mm
sieve. Total metal concentrations in articially contaminated soils
were: for Cu 1984.1 mg kg1 (S1) and 2042.2 mg kg1 (S2); and
for Cd, 49.8 mg kg1 (S1) and 55.2 mg kg1 (S2).
2.3. Compost the source of HS
Mature compost from sewage sludge and lignocellulosic
materials (wood chips, grass, rape straw) was the source of humic
substances (after 170 days of composting). Compost came from the
Department of Environmental Biotechnology at the University of
Warmia and Mazury (project No. N523455036). The compost had
a relatively high content of organic matter (47.9%), total organic
carbon (TOC) (22.65%), nitrogen (1.68%) and phosphorus (0.93%).
The concentration of HS was 162.3 g C kg1 OM. Importantly, the
concentrations of all heavy metals were below the permissible
values for heavy metals in organic and organo-mineral fertilizers
and organic and organo-mineral plant conditioner, as given in
the Ordinance of the Ministry of Agriculture and Rural
Development (OMARD 2004, 2008) on the implementation of
certain provisions of the Act on Fertilizers and Fertilization.
Because the concentrations of metals in the compost were low
(Cd 0.93 mg kg1, Cr 50.7 mg kg1, Cu 48.6 mg kg1, Fe
10.79 g kg1, Mn 294 mg kg1, Ni 24.2 mg kg1, Pb 25.3 mg kg1,
Zn 270 mg kg1, Hg 0.055 mg kg1, based on dry mass), it can be
concluded that only a negligible amount of metal was introduced
to the soil during washing with humic substances extracted from
the compost.
2.4. Washing agents
As washing agent, HS derived from compost were tested.
Additionally, for comparison studies, the effectiveness of heavy
metals removal with commercial HA (Fluka) and two plant biosurfactants, tannic acid (TA) and saponin (SAP) were evaluated.
HS extraction followed the methodology described in Jouraiphy
et al. (2005) and Amir et al. (2006). Before HS extraction, compost
was washed with distilled water to eliminate soluble non-humic
substances (e.g. sugars and proteins), which can interact with HS.
Then, the samples were defatted with a chloroform:methanol
(2:1) mixture in a microwave oven. After ltering, the defatted
samples were evaporated to eliminate the solvents. Next, HS were
extracted with 0.1 M NaOH. In order to nd out the concentration
of HA and the fulvic fraction (FF) in the solution of HS, humic substances were fractionated into HA and FF as follows. First, the solution of HS was acidied to pH 1 with H2SO4. Next, the precipitate
(HA) was allowed to coagulate for 24 h at 4 C. Then, HA were
redissolved in 0.1 M NaOH, and in the HS and HA, TOC was

44

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

determined using a Shimadzu Liquid TOC-VCSN analyzer. The FF


content was calculated by subtracting the concentration of HA
from HS.
A commercial and standardized HA (Fluka) was chosen as a
model for natural humic acids. It was used without any further
purication. Moreover, two plant biosurfactants TA (Product No.
16201) and SAP (Product No. 84510) were purchased commercially
(SigmaAldrich, Poland) as powders and used without further
purication as washing agents. TA is a type of polyphenol consisting of a hydroxyl group (OH) bonded directly to an aromatic
hydrocarbon group. TA is usually extracted from Caesalpinia
spinosa or Rhus semialata. It consists mainly of gallic acid residues
linked to glucose via glycosidic bonds. The chemical formula is
C76H52O46 and its molecular weight is 1701.2 g mol1. For soil
washing, puriss grade tannic acid was used.
SAP is a mixture of triterpeneglycosides extracted from the
bark of the tree Quillaja saponaria, in which the hydrophilic part
is composed of sugar chains with functional groups. In the present
study, SAP of premium quality was used, in which the maximum
sapogenin content (non-sugar hydrophobic part) was 25%.
2.5. Optimization of metal removal from soils by HS
For optimization, soil was washed in batch conditions. All the
soil washing experiments were conducted in 50 mL capacity polyethylene tubes with a soil to humic substances solution ratio of
1/40 (W/V). This ratio between soil mass (W) and volume of
washing solution (V) was optimized in our previous research and
found to be the most suitable for soil washing (Gusiatin and
Klimiuk, 2012). The samples were shaken in a mechanical shaker
at 150 r min1 at room temperature. To optimize humic substances
concentration, 100, 250, 500, 750, 1000, 1500, 2000, 2500, 3000,
3500 and 4000 mg L1 (based on C content) solutions were tested.
The optimum concentration was then tested at different pHs: 3, 5,
7, 9, 11 and 13.
Next, to determine the optimum extraction time, soil was
washed at optimum concentration and pH for specic time
intervals (5, 10, 30, 60, 90, 120, 180, 240, 300, 360, 720 and
1440 min), samples were collected, and Cu and Cd concentration
in the supernatants was measured. This allowed the determination
of the time needed to reach equilibrium and the kinetic constants
of heavy metals removal.
Because sorption of the washing agents onto soil might affect
pollutant removal, total organic carbon was measured in the
supernatant after soil washing to determine the sorption of HS.

concentration, pH 3.0 for both soils) were adopted from Gusiatin


and Klimiuk (2012).
The samples in both stages were shaken in a mechanical shaker
at 150 r min1 for 3 h at room temperature (2224 C). At the end
of the extraction, the suspensions were centrifuged at 8000 r min1
for 20 min and the supernatants ltered. In liquid samples the total
metal concentration was measured, whereas in solids the metal
fractions were determined after the second washing.
2.6.3. Triple soil washing
At each stage of triple soil washing, Cu and Cd were removed
from both soils using a HS solution at the optimal concentration
of HS and pH for the optimal time as determined in Section 2.5.
2.7. Analytical methods
2.7.1. Physicochemical characteristics of soils
Particle size was determined using a Mastersizer 2000 particle
size analyzer, and soil organic matter by the Tiurin method
(Ostrowska et al., 1991). The cation exchange capacity (CEC) of
the soils was calculated as a sum of the hydrolytic acidity (in 1 N
Ca(CH3COO)2) and exchangeable bases (in 0.1 M HCl) (Ostrowska
et al., 1991); and the equilibrium pH of soil in distilled water
(1:2.5 ratio, W/V) was measured with a pH meter (Hanna
Instruments).
2.7.2. Total metal concentration
Total Cu and Cd concentrations were determined both in
unpolluted and contaminated soils via digestion with an
HCl:HNO3 mixture in microwave oven (MARSXpress, CEM USA).
For that purpose, 1 g of dried soil (at 105 C) was weighed and
placed in polytetrauoroethylene vessels, treated with HCl:HNO3
mixture (SigmaAldrich) at a 3:1 ratio (v/v) and heated using a
one-stage microwave program (T = 170 C, P = 800 W, t = 30 min).
After cooling, the extracts were ltered through Whatman 40 lter
papers (pore size 8 lm) into 50-mL glass asks and lled to the
mark with distilled water. Metal concentration was measured
using a ame atomic absorption spectrometer (FAAS) (Varian,
AA28OFS), equipped with a sample introduction pump system.
2.7.3. Sequential extraction procedure
A modied BCR procedure (Pueyo et al., 2008) was performed to
assess Cu and Cd distribution in contaminated and treated soils.
Four operationally dened fractions were determined for each
metal: exchangeable and acid soluble (F1), reducible (F2),
oxidizable (F3) and residual (F4).

2.6. Single and multiple washing


2.6.1. Single soil washing
Cu and Cd removal from both soils was conducted using a solution of HS at optimal concentration, pH (for each soil) and washing
time, as determined on the basis of the experiments described in
Section 2.5.
2.6.2. Duplicate soil washing
In duplicate washing (1 and 2), following technological
options were tested with both soils:
 humic substances (1), humic substances (2) (HSHS)
 humic substances (1), saponin (2) (HSSAP)
 humic substances (1), tannic acid (2) (HSTA)

2.7.4. Surface-active properties of humic substances (HS) and humic


acid (HA)
Critical micelle concentration (CMC) and the ability to reduce
surface tension of HS and HA were determined. Surface tension
was measured with a Krss K100 tensiometer (Germany) employing the Wilhelmy plate method directly in fresh aqueous HS and
HA solutions, for 20 concentrations ranging between 0 and
1550 mg C L1 for HS and for 27 concentrations (from 0 to
4200 mg C L1 for HA). Surface tension values were plotted vs.
the logarithm of the HS and HA concentration; the intersection of
the two regression lines shows the CMC.
3. Results and discussion
3.1. CMC and the surface tension (c) of HS and HA

At each step, soil washing was conducted in optimal conditions.


For the HS, the optimal conditions were chosen on the basis of the
experiment described in Section 2.5 (as in the case of single
washing). For plant biosurfactants, the optimum conditions (3%

For HS extracted from sewage sludge compost, the CMC was


946 mg L1 and the surface tension at CMC 48.0 mN m1. For commercial HA, these values were 2049 mg L1 and 54.5 mN m1

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

(Fig. 1). Despite the fact that studies that have determined the CMC
and surface tension of HS and HA are not numerous, the ones that
are available in the literature conrm that HS and HA exhibit surfactant properties.
For example, Montoneri et al. (2009) reported that the CMC of
HA like substances from green waste composted for 60 days was
730 mg L1 and surface tension at CMC was 38.1 mN m1; both
these values were lower than those of HA commercially available
from Aldrich (CMC, 1530 mg L1; surface tension, 47.48 mN m1).
In our study, the value of c was higher than in Montoneri et al.
(2009). This may be because the surface tension of HS obtained
from different sources can vary signicantly depending on their
origin and molecular properties. Moreover, whereas HS isolated
from natural samples (soil, peat, sediments, sewage sludge) were
found to decrease surface tension as their concentration increased,
many industrially produced humic materials had little or no effect
on the surface tension of their solutions (Klavins and Purmalis,
2010). Similarly, our data indicates that HS show better surfactant
properties than HA. These ndings indicate that biomass or compost can be a good source of HS, natural biosurfactants.
3.2. The effect of HS and HA on the efciency of Cu and Cd removal
from soils
The efciency of removal of both Cu and Cd depended on HS
and HA concentration (Fig. 2). Removal of Cd from soil S2 was
not affected by the kind of washing agent. However, HS at
concentrations above 2500 mg C L1 did remove Cd slightly more
effectively from soil S1 (Fig. 2b).
HS were more effective than HA at removing Cu; this was
evident at all concentrations with soil S1 (Fig. 2a), but only at
concentrations above 2000 mg C L1 with soil S2 (Fig. 2c). The
effectiveness of Cu removal with HS from soil S1 increased quickly
up to a concentration of 1500 mg C L1, when it reached 50.5%,

(a)
-1

surface tension (mN m )

80
70
60
50

y1 = -20.068x + 108.59

40

y2 = -2.9412x + 57.62

30
20
10

CMC

0
0.0

0.8

1.6

2.4

3.2

log C

-1

surface tension (mN m )

(b)

60

y1 = -13.883x + 100.51

30
20
10

CMC

0
0.5

1.0

1.5

2.0

After a solution of HA is extracted from compost, its pH is about


13. Therefore, because the solubility of metals increases at low pH,
the effect of pH on process efciency was examined with a xed
concentration of HS (3000 mg C L1) at pHs ranging from 3.0 to
13.0 (Fig. 3).
With both metals in both soils, removal efciency depended on
pH. With soil S1, removal efciency for both metals was lowest at
pH 3 and did not exceed 40% (Fig. 3a). This was caused by adsorption of HS onto the soil (after washing, HS concentration had
decreased from 3000 mg C L1 to 1271 mg C L1) (Fig. 3a). Also with
this soil, the removal efciency of Cu and Cd was highest at pH 5:
80.7% of Cu and 69% of Cd. At higher pHs, efciency gradually
decreased. With soil S2, removal of both metals was also least efcient at pH 3 (approximately 20%) due to high adsorption of HS onto
soil (Fig. 3b). Removal was most efcient (53.2% of Cu and 36.6% of
Cd) at pHs ranging from 7 to 9, so pH 7 was selected for further
study. The sorption of biosurfactants like HS on soil is a rather common phenomena. For example, Hong (2000, after Hong 2002)
showed that the amount of SAP sorbed onto soils increases with
decreasing pH due to the increased electrostatic attraction between
SAP and the soil surface. Sorption of biosurfactants can reduce their
potential for removal of contaminants from various components of
the soil (Ochoa-Loza et al., 2007). Wang and Mulligan (2009b)
found that under acidic conditions (at pH 3.0), arsenic mobilization
with HA decreased due to their sorption to mine taillings.
Decreasing of pH leads to protonation of the OH+2 surface functional
groups, which has a signicant effect on the adsorption of HA.
According to Shaker et al. (2012), HA adsorption on hematite and
kaolinite increases with decreasing pH because the carboxylic
groups of humic acid become less negatively charged at low pH
and the electrostatic repulsion between HA and the soil minerals
decreases. The electrical double layer on the adsorbent also affects
the adsorption process by changing the polarity from positive to
negative as the pH changes from acidic to basic media. Wang
et al. (2012) showed that at lower pH, adsorption might depend
on palygorskite and the carboxylate groups of HA molecules, as well
as hydrogen bonding between hydroxyl surface groups on the palygorskite and the carboxylates of HA. In addition, palygorskite was
positively charged at lower pH, which might facilitate the adsorption of negatively charged HA.

dq1
k  qe  qt 2
dt

y2 = -0.552x + 56.364

0.0

3.3. Effect of pH on Cu and Cd removal efciency

For both metals in both soils, equilibrium was attained within


3 h (Fig. 4).
In all cases, removal of heavy metals followed second-order
kinetics:

70

40

then slowly up to 3000 mg C L1 (64.5%), and then only 1% as concentration was increased to 4000 mg C L1. Cu removal with HS
from soil S2 followed a similar trend. Therefore, a HS concentration
of 3000 mg C L1 was adopted as optimum for determination of
process kinetics and of the effect of pH on metal removal efciency.

3.4. Kinetics of metal removal with HA

80

50

45

2.5

3.0

3.5

4.0

log C
Fig. 1. Plot of surface tension (c) as a function of washing agent concentration (as
log C) (a) HS; (b) HA.

where, qt (mg kg1) is heavy metal concentration removed from


soil after time t; qe (mg kg1) is heavy metal concentration
removed from soil in equilibrium conditions, determined
from the linearized form of the second-order equation; k
(kg mg1 min1) is rate constant, and t (min) is time.
Eq. (1) after linearization has the form:

1
1
1

t
qt k  q2e qe

46

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

(b)

60
50
40
30
20
10

HS

HA

S1

60
50
40
30
20
10

HS

HA

500 1000 1500 2000 2500 3000 3500 4000

concentration (mg C

500

1000 1500 2000 2500 3000 3500 4000


-1
concentration (mg C L )

L -1)

(c)

(d)

70

Cu removal efficiency (%)

Cd removal efficiency (%)

70

S1

70

S2

60
50
40
30
20

HS

10

HA

Cd removal efficiency (%)

Cu removal efficiency (%)

(a)

70

S2

60
50
40
30
20
10

HS

HA

500 1000 1500 2000 2500 3000 3500 4000

500 1000 1500 2000 2500 3000 3500 4000

-1
concentration (mg C L )

concentration (mg C L -1)

Fig. 2. Cu and Cd removal efciency in dependence on washing agents (HS, HA) concentrations (a and b) soil S1; (c and d) soil S2.

2000
1600

-1

Qe (mg Cu kg d.m.)

(a)

Cu and Cd removal
efficiency (%)

3000
2500

80

2000
60
1500
40
1000
20

500
Cu

Cd

HS

0
2

10

12

14

(b)
S2

3000
2500

80

2000

60

1500
40

1000

20
Cu

Cd

500

HS

SH concentration after
washing (mgC/L)

Cu and Cd removal
efficiency (%)

100

10

12

14

pH

400
0
120 240 360 480 600 720 840 960 1080 1200

time (min)

-1

pH

800

S1-experimental data
pseudo 2. order kinetic

(b)

1200

Qe (mg Cd kg d.m.)

S1

100

SH concentration after
-1
washing (mg C L )

(a)

S2-experimental data

50
40
30
20
10
0

120

240

360

480

600

720

840

960 1080 1200

time (min)
S1-experimental data
pseudo 2. order kinetic

Soil

q e*

Cu
k **

S1
S2

1667
1111

2.25 10
.
-4
1.37 10

S2-experimental data

r ***
-4

624.838
169.520

q e*

Cd
k **
.

r ***
-3

3.89 10
.
-3
19.8 10

5.64
7.56

* mg kg -1; ** kg mg -1 min-1; *** mg kg 1min1


Fig. 3. Efciency of Cu and Cd removal by HS, and HS concentration after washing
at different pHs (a) soil S1; (b) soil S2.

Fig. 4. Kinetics of Cu (a) and Cd (b) washing from soil S1 and S2.

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

The coefcients from the regression were used to calculate the


constants, i.e. k and qe. Using these constants, the initial rate of the
process was determined:

r k  q2e

where r (mg kg1 min1) is initial rate of heavy metal removal; k


(kg mg1 min1) is rate constant, and qe (mg kg1) is heavy metal
concentration removed from soil in equilibrium conditions, determined from the linearized form of the second-order equation.
With HS as a washing agent, qe values of both heavy metals
were higher for soil S1 than for soil S2. However, irrespective of soil
type, k values were higher for Cd than for Cu (Fig. 4). This indicates
that Cd is more mobile in soil than Cu. Although Hong et al. (2002)
reported that washing with SAP followed 1st order kinetics, they
also found that the rate constant for Cd was larger than the constant for Cu removal. In their study, equilibrium was reached
within 6 h with most soils. Tsang et al. (2011) found that heavy
metals (Pb, Zn, Cu) removal from soil with EDTA followed 1st order
kinetics; however, this proceeded in two phases, rapid extraction
during the rst few hours followed by gradual extraction.
In the present study, the time needed to reach equilibrium was
3 h, on this basis, the metal washing time for the following experiments on multiple washing was set at 3 h.
3.5. Efciency of heavy metals removal in single and multiple washing
3.5.1. Efciency of Cu and Cd removal in single washing
Cu and Cd were removed relatively effectively with just a single
washing (Table 2). Both metals were removed more effectively
from soil S1, which had a lower organic matter content, than from
soil S2, with a higher organic matter content (Table 1). In soils with
higher clay and organic matter content, metals are more tightly
bound, which limits the efciency of their removal. Similarly,
Hong et al. (2002) found that a high content of organic matter in
soils (7.22% and 11.25%) makes removal of heavy metals quite
difcult due to their high sorptive capacity. From both soils in
the present study, Cu was removed more effectively than Cd.
Similarly, although their study used kaolin with a 4.5-times lower
concentration of Cu (450 mg kg1), Chen et al. (2008) found that
SAP effectively removes Cu (83%).

Table 2
Efciency of Cu and Cd removal in a single*, duplicate** and triple*** soil washing.
Washing agent

Heavy metals removal efciency (%)


Single soil washing
Soil S1

HS

Soil S2

Cu

Cd

Cu

Cd

80.7

69.1

53.2

36.5

Duplicate soil washing


Soil S1

HSHS
HSSAP
HSTA

Soil S2

Cu

Cd

Cu

Cd

94.4
89.4
87.7

89.0
85.0
76.8

72.6
66.8
60.3

57.2
54.0
40.8

Triple soil washing


Soil S1

HS
*

Soil S2

Cu

Cd

Cu

Cd

97.7

98.2

83.2

88.9

1

W/V = 1/40, HS = 3000 mg C L , pH 5 for soil S1 and pH 7 for soil S2.


HS: W/V = 1/40, 3000 mg C L1, pH 5 for soil S1 and pH 7 for soil S2; SAP or TA:
W/V = 1/40, 3% w/v, pH 3.
***
W/V = 1/40, HS = 3000 mg C L1, pH 5 for soil S1 and pH 7 for soil S2.
**

47

The high efciency of metal removal in our study may be connected with the fact that both the HA and FA in HS are known to
strongly affect the mobility and bioavailability of heavy metals in
soils (Stevenson, 1994). Both have many functional groups which
are involved in the formation of metalhumic complexes, mainly
carboxylic COOH and phenolic OH groups. In our study, the HS
concentration was 3000 mgC L1, and the concentrations of HA
and FA were 2160 mg C L1 and 840 mg C L1, respectively.
Despite the relatively low FA concentration, their role in heavy
metals removal may have been large because FA contain more
functional groups of an acidic nature, particularly COOH. The total
acidities of FA (9001400 meq 100 g1) can be considerably higher
than those of HA (400870 meq 100 g1). Donisa et al. (2003)
found that Cu, Cd and 9 other elements were bound more to the
fulvic than to the humic fraction in natural soils (andosol, podzol,
cambisol). In contrast, Laborda et al. (2008) found that in general,
both FA and HA contribute to binding Cu, whereas Cd preferentially associates with HA.
3.5.2. Efciency of Cu and Cd removal in duplicate soil washing
The effectiveness of heavy metals removal by HS was compared
to the effectiveness of SAP and TA in the 2nd step of soil washing.
Although SAP and TA are known to effectively remove Cu and Cd
(Chen et al., 2008; Gusiatin, 2014), their high price is a disadvantage. Thus, in this study SAP and TA were only used for the 2nd step
of washing. With both soils, HSHS washing was most effective
(Table 2) and HSTA washing was least effective. Regardless of
the combination of washing agents used, heavy metals were more
efciently removed from soil S1 than from soil S2. This means that
regardless of the type of washing agents, soil with low organic
matter (S1) can be more effectively remediated mainly because
the metals are less strongly sorbed to the soil.
3.5.3. Efciency of Cu and Cd removal in triple soil washing
With HS as a washing agent in triple washing, Cu and Cd was
almost completely removed from soil S1 (Table 2). In soil S2,
removal of both metals was lower, but also high.
Similarly, SAP very effectively removed heavy metals during triple washing, with 6597% Cu and 89100% Cd efciency from
three types of soils (sandy clay loam, loam, clay) (Gusiatin and
Klimiuk, 2012). However, heavy metals were removed much less
efciently from a real polluted construction site in Canada and lake
sediment from Japan (Mulligan et al., 2007; after Mulligan, 2009).
They used different biosurfactants (rhamnolipids, saponin and
mannosylerytritol lipids (MEL)) to remove heavy metals from soil
in a ve-step washing process. The authors showed that saponin
(30 g L1) removed zinc (88%, pH 3.0) and nickel (76%, pH 5.0) most
effectively from the construction site, 2% rhamnolipids (pH 6.5)
were best for removing copper (46%), and 4% MEL (pH 5.6)
removed contaminants least effectively (17% of the zinc and nickel
and 36% of the copper). From the sediment, 30 g L1 saponin (pH 5)
removed zinc (33%) and lead (24%) most effectively, and 2% rhamnolipids (pH 6.5) were again best for removing copper (84%).
Mulligan et al. (2001) stated that multiple washings may be more
effective because they can remove the easier metal phases rst
(e.g. exchangeable) and then the more difcult ones (e.g. carbonate
and reducible). It can be important especially for real pollution
caused many years ago, which is much more difcult to remove
than spiked pollution because the metals are included in minerals
and soil aggregates.
3.5.4. The distribution and environmental risk of heavy metals in
treated soils
Total Cu and Cd concentrations, their distributions and
ecological risks (as Eir) in contaminated and treated soils are given
in Table 3.

48

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

Table 3
Chemical form of Cu and Cd in contaminated soils and soil after three step washing with HS (W/V = 1/40, HS = 3000 mg C L1, pH 5 for soil S1 and pH 7 for soil S2).
Parameter

Unit

Total Cu
F1
F2
F3
F4
ECu
r
Total Cd
F1
F2
F3
F4
ECd
r

mg kg1 d.m.
mg kg1 d.m.
mg kg1 d.m.
mg kg1 d.m.
mg kg1 d.m.

mg kg1 d.m.
mg kg1 d.m.
mg kg1 d.m.
mg kg1 d.m.
mg kg1 d.m.

Soil S1

Soil S2

Contaminated

After washing

% removal

Contaminated

After washing

% removal

1984.1
1242.1
433.1
57.9
251.0
26.5
49.8
42.6
6.8
0.0
0.4
159.4

44.8
23.1
9.3
12.4
5.1
0.6
0.9
0.7
0.2
0.0
0.0
2.9

97.7
98.1
97.8
78.6
97.9

98.2
98.3
97.0
0.0
100

2042.2
273.2
735.9
864.5
168.7
20.4
55.2
19.1
35.6
0.6
0.0
154.6

341.9
124
18.4
111.5
86.0
4.0
6.1
1.6
4.5
0.0
0.0
14.1

83.2
54.6
97.5
87.1
49.0

88.9
91.6
87.3
100
0.0

The potential ecological risk of an individual metal (Eir), which is


directly related to its toxicity and mobility, was calculated according to the following formula:

Eir T ir 

C iD  X
C iR

where Tri is the toxic-response factor for a given metal (Cu = 5;


Cd = 30) (Hakanson, 1980); CDi (mg kg1) is its mean concentration
in the soil; X is the modied index of heavy metal concentration
calculated as Ad + B (A percentage of the F1 fraction according
to the BCR procedure, B = 1A, d the toxic index of the F1 fraction
for a given metal), and the CRi (mg kg1) is the background concentration or national criteria for metals (Qingjie et al., 2008), here it is
the threshold limits in soil for the metal according to Polish law (Cu,
600 mg kg1 d.m.; Cd, 15 mg kg1 d.m.). The d values change
depending on the percentage of metal in the F1 fraction: 1.0
(1% < F1 6 10%); 1.2 (11% 6 F1 6 30%); 1.4 (31% 6 F1 6 50%) and
1.6 (F1 > 50%) (Zhu et al., 2012). An Eir of <40 means that a single
metal poses a low risk, 4080 is moderate risk, 80160 is considerable risk, 160320, high risk; and >320, very high risk (Zhu et al.,
2012).
In the present study, although the total concentration of Cu was
similar in both soils, its fractionation differed. In soil S1, Cu concentration was highest in the easily soluble fraction F1, followed by F2,
then F4 and F3. In soil S2, Cu occurred in more stable forms, mainly
in the F3 fraction followed by F2. The predominance of Cu in the
organic fraction in soil S2 conrms the high afnity of Cu for
organic matter, with which it easily forms complexes due to the
high stability of organicCu compounds (Li et al., 2001). The
organic fraction includes also metals associated with mineral suldes, of which the solubility strongly depends on redox conditions.
Cu in soil S1 was found mainly in the F1 fraction (Table 3), but
the efciency of removal from this fraction was very high (98%).
Metal removal from the F2 and F4 fractions was similar (98%),
despite lower concentrations than in F1. Removal efciency was
lowest with the F3 fraction (12.4 mg1 kg d.m.; 79%). However, this
did not affect the overall efciency because in the contaminated
soil the amount of organically bound Cu was the lowest. It is worth
emphasizing that with Cu, extremely high effectiveness was
obtained even with the F4 fraction (5.1 mg kg1 d.m.; 98%). This
is a rather unusual phenomena as Li et al. (1995) found that in soil
contaminated by open burning and open detonation of chemical
reagents and munition, organically-bound metals are very stable
and not generally removed or changed by soil washing. They concluded that the metals in this phase could not be removed by EDTA
and should not be considered in the washing processes, since they
would be uneconomical to remove. In contrast, although spiked
soil was used instead of real polluted soil, the results of the present
study suggest that HS can remove metals associated with the
organic phase.

The high overall effectiveness of Cu removal from soil S2 (83%)


was connected mainly with its highly effective removal from the
F2 (18.4 mg kg1 d.m.; 97.5%) and F3 fractions (111.5 mg kg1 d.m.;
87%). Although the HS removed less from F4 (49%) than from F2
and F3, they removed more Cu from this fraction than other washing
agents in other studies. For example, Gusiatin and Klimiuk (2012)
showed that SAP removed a negligible amount of copper (4%) from
the residual fraction. This might be associated with longer soil aging
(3 months) after contamination. It is known that the strength of
metal bonding in soil increases within time as a result of metal
diffusion or occlusion into mineral and organic soil constituents
(Han et al., 2003). In the present study, soil was aged for only one
month after metal spiking. Therefore, metal removal from more
stable fractions (i.e. F3 and F4) was higher than that obtained by
Gusiatin and Klimiuk (2012).
In contaminated soil S1, Cd was mostly bound to the F1 fraction,
followed by F2. The large share of this metal in the F1 fraction indicates its relative solubility and mobility in soils. The small amount
of Cd in the organic matter fraction is consistent with the low constant of adsorption of Cd ions on organic matter; additionally, Cd
does not appear to form a strong complex with organic matter
(Kashem et al., 2007; in Gusiatin and Klimiuk, 2012). After triple
washing in the present study, the share of Cd in F1 in soil S1
decreased markedly, which led to a high total washing efciency.
In contrast to soil S1, in soil S2 Cd was associated mainly with
the reducible fraction (F2), followed by exchangeable and acid soluble fraction (F1). After washing with HS, the F2 fraction was
extracted with 87% efciency. Because this fraction was the largest,
its removal efciency had the greatest effect on overall Cd efciency from soil S2.
Metal distribution affects not only the efciency of soil washing,
but also determines environmental risk because the individual
metal fractions have different chemical reactivity. Therefore, a risk
assessment should be considered during remediation of soils contaminated with heavy metals. Before soil washing in the present
study, environmental risk from Cd was considerable in both soils,
according to the Eir index, whereas risk from Cu was low. The risks
from these metals differed despite the fact that they both were
found predominantly in the most mobile fraction in soil S1. The
difference is due to the fact that Cd is more toxic than Cu
Cu
(ECd
r > Er ) and its permissible soil concentration is much lower.
Triple washing with HS sufciently decreased Cd concentration
in the F1 fraction to reduce the environmental risk posed by this
metal.
4. Conclusions
HS from sewage-sludge compost effectively removed Cu and Cd
from both spiked soils, sandy clay loam and clay, which indicates
that they may be a useful, environmentally friendly and cost-

D. Kulikowska et al. / Chemosphere 136 (2015) 4249

effective biosurfactant. Because these HS proved to be an effective


substitute for commercial biosurfactants, it is worth investigating
whether HS obtained from other kinds of compost or waste
materials rich in HS can remove Cu, Cd and other heavy metals
from highly contaminated soils. Also, the effectiveness of HS for
removing metals from real, aged polluted soil should be tested to
follow up on these promising results with spiked soils.
Acknowledgement
The study was supported by a Ministry of Science and Higher
Education in Poland (Statutory Research, 528-0809-0801).
References
Amir, S., Hadi, M., Merlina, G., Revel, J.C., 2005. Structural characterization of fulvic
acids during composting of sewage sludge. Process Biochem. 40, 16931700.
Amir, S., Hadi, M., Lemee, L., Merlina, G., Guiresse, M., Pinelli, E., Revel, J.C., Bailly,
J.R., Ambles, A., 2006. Structural characterization of humic acids, extracted from
sewage sludge during composting, by thermochemolysisgas chromatography
mass spectrometry. Process Biochem. 41, 410422.
Boruvka, L., Drbek, O., 2004. Heavy metal distribution between fractions of humic
substances in heavily polluted soils. Plant Soil Environ. 50, 339345.
Chen, W.J., Hsiao, L.Ch., Chen, K.K.Y., 2008. Metal desorption from copper(II)/
nickel(II)-spiked kaolin as a soil component using plant-derived saponin
biosurfactant. Process Biochem. 43, 488498.
Conte, P., Agretto, A., Spaccini, R., Piccolo, A., 2005. Soil remediation: humic acids as
natural surfactants in the washings of highly contaminated soils. Environ.
Pollut. 135, 515522.
Donisa, C., Mocanub, R., Steinnes, E., 2003. Distribution of some major and minor
elements between fulvic and humic acid fraction in natural soils. Geoderma
111, 7584.
Elouzi, A.A., Akasha, A.A., Elgerbi, A.M., El-Baseir, M., El Gammudi, B.A., 2012.
Removal of heavy metals contamination by bio-surfactants (Rhamnolipids). J.
Chem. Pharm. Res. 4, 43374341.
Gusiatin, Z.M., 2014. Tannic acid and saponin for removing arsenic from browneld
soils: mobilization, distribution and speciation. J. Environ. Sci. (China) 26,
855864.
Gusiatin, Z.M., Klimiuk, E., 2012. Metal (Cu, Cd and Zn) removal and stabilization
during multiple soil washing by saponin. Chemosphere 86, 383391.
Hakanson, L., 1980. An ecological risk index for aquatic pollution control a
sedimentecological approach. Water Res. 14, 9751000.
Han, F.X., Banin, A., Kingery, W.L., Triplett, G.B., Zhou, L.X., Zheng, S.J., 2003. New
approach to studies of heavy metal redistribution in soil. Adv. Environ. Res. 8,
113120.
Hong, K.J., 2000. Application of plant-derived biosurfactant to heavy metal removal
from y ash and soil. PhD Thesis. Tokyo Institute of Technology, Tokyo, Japan.
Hong, K.J., Choi, Y.K., Tokunaga, S., Ishigami, Y., Kajiuchi, T., 1998. Removal of
cadmium and lead from soil using asecin as a biosurfactant. J. Surfactant Deterg.
2, 247250.
Hong, K.J., Tokunaga, S., Kajiuchi, T., 2002. Evaluation of remediation process with
plant-derived biosurfactant for recovery of heavy metals from contaminated
soils. Chemosphere 49, 79387.
Jouraiphy, A., Amir, S., Gharous, M., Revel, J.C., Hadi, M., 2005. Chemical and
spectroscopic analysis of organic matter transformation during composting of
sewage sludge and green plant waste. Int. Biodeter. Biodegr. 56, 101108.
Kalsom, M.S., Nur, H., Norlea, A.A., Ngaspan, S., 2006. Characterization of humic acid
from humication of oil palm empty fruit bunch bre using Trichoderma viride.
J. Trop. Agric. Fd. Sc. 34, 165172.
Kashem, M.A., Singh, B.R., Kawai, S., 2007. Mobility and distribution of cadmium,
nickel and zinc in contaminated soil proles from Bangladesh. Nutr. Cycl.
Agroecosys. 77, 187198.
Klavins, M., Purmalis, O., 2010. Humic substances as surfactants. Environ. Chem.
Lett. 8, 349354.

49

Laborda, F., Bolea, E., Grriz, M.P., Ruiz, M.P.M., Ruiz-Begueria, S., Castillo, J.R., 2008.
A speciation methodology to study the contributions of humic-like and fulviclike acids to the mobilization of metals from compost using size exclusion
chromatographyultraviolet absorptioninductively coupled plasma mass
spectrometry and deconvolution analysis. Anal. Chim. Acta. 606, 18.
Li, W., Peters, R.W., Brewster, M.D., Miller, G.A., 1995. Sequential extraction
evaluation of heavy-metal contaminated soil: how clean is clean? In:
Proceedings of the 88th Annual Meeting and Exhibition of Air and Waste
Management Association. San Antonio, USA. June 1823.
Li, X., Shen, Z., Wai, O.W.H., Li, Y.S., 2001. Chemical forms of Pb, Zn and Cu in the
sediment proles of the Pearl River Estuary. Mar. Pollut. Bull. 42, 215223.
Meng, D., Wan, J., Zhang, S., Yao, H., Lin, Y., 2014. Simultaneous removal of lindane
and heavy metals from contaminated soils by rhamnolipids enhanced washing.
Huanjing Kexue Xuebao/Acta Sci. Circumst. 34, 229237.
Montoneri, E., Boffa, V., Savarino, P., Perrone, D.G., Musso, G., Mendichi, R., Chierotti,
M.R., Gobetto, R., 2009. Biosurfactants from urban green waste. ChemSusChem.
2, 239247.
Mulligan, C.N., 2009. Recent advances in the environmental applications of
biosurfactants. Curr. Opin. Colloid In. 14, 372378.
Mulligan, C.N., Yong, R.N., Gibbs, B.F., 2001. Heavy metal removal from sediments
by biosurfactants. J. Hazard. Mater. 85, 111125.
Mulligan, C.N., Oghenekevwe, C., Fukue, M., Shimizu, Y., 2007. Biosurfactant
enhanced remediation of a mixed contaminated soil and metal contaminated
sediment. In: Proceedings of the 7th Geoenvironmental Engineering Seminar,
JapanKoreaFrance, Grenoble, France.
Ochoa-Loza, F.J., Noordman, W.H., Jannsen, D.B., Brusseau, M.L., Miller, R.M., 2007.
Effects of clays, metal oxides, and organic matter on rhamnolipid sorption by
soil. Chemosphere 66, 16341642.
OMARD, 2004. Ordinance of the Minister of Agriculture and Rural Development on
fertilizers and fertilization. J. Law. 236, 1683416839 (in Polish).
OMARD, 2008. Ordinance of the Minister of Agriculture and Rural Development on
fertilizers and fertilization. J. Law. 119, 65156520 (in Polish).
Ostrowska, A., Gawlinski, S., Szczubiaka, Z., 1991. Methods of Analysis and
Assessment of Soil Properties and Plants. Institute of Environmental
Protection. Warsaw, Poland. 5195.
Pueyo, M., Mateu, J., Rigol, A., Vidal, M., Lopez-Sanchez, J.F., Rauret, G., 2008. Use of
the modied BCR three-step sequential extraction procedure for the study of
trace element dynamics in contaminated soils. Environ. Pollut. 152, 330341.
Qingjie, G., Jun, D., Yunchuan, X., Qingfei, W., Liqiang, Y., 2008. Calculating pollution
indices by heavy metals in ecological geochemistry assessment and a case study
in parks of Beijing. J. China Univ. Geosci. 19, 230241.
Shaker, A.M., Komy, Z.R., Heggy, S.E.M., El-Sayed, E.A., 2012. Kinetic study for
adsorption humic acid on soil minerals. J. Phys. Chem. 116, 1088910896.
Steelink, C., 1985. Implications of elemental characteristics of humic substances. In:
Aiken, G.R., McKnight, D.M., Wershaw, R.L., MacCarthy, P. (Eds.), Humic
Substances in Soil, Sediment and Water. Wiley, New York, pp. 457476.
Stevenson, F.J., 1994. Humus Chemistry, Genesis, Composition, Reactions. John
Wiley Sons Inc., Canada.
Thawornchaisit, U., Polprasert, C., 2009. Evaluation of phosphate fertilizers for the
stabilization of cadmium in highly contaminated soils. J. Hazard. Mater. 165,
11091113.
Tsang, D.C.W., Yip, A.C.K., 2014. Comparing chemical-enhanced washing and
waste-based stabilisation approach for soil remediation. J. Soils Sediments.
14, 936947.
Tsang, D.C.W., Yip, T.C.M., Lo, I.M.C., 2011. Conceptual model and sensitivity
analysis for simulating the extraction kinetics of soil washing. J. Soils
Sediments. 11, 12211233.
Wang, S., Mulligan, C.N., 2009a. Rhamnolipid biosurfactant-enhanced soil ushing
for the removal of arsenic and heavy metals from mine tailings. Process
Biochem. 44, 296301.
Wang, S., Mulligan, C.N., 2009b. Effect of natural organic matter on arsenic
mobilization from mine tailings. J. Hazard. Mater. 168, 721726.
Wang, M., Liao, L., Zhang, X., Li, Z., 2012. Adsorption of low concentration of humic
acid from water by palygorskie. Appl. Clay Sci. 6768, 164168.
Zhu, H.N., Yuan, X.Z., Zeng, G.M., Jiang, M., Liang, J., Zhang, C., Yin, J., Huang, H.J., Liu,
Z.F., Jiang, H.W., 2012. Ecological risk assessment of heavy metals in sediments
of Xiawan Port based on modied potential ecological risk index. Trans.
Nonferrous Met. Soc. China (english edition) 22, 14701477.