Accumulation of heavy metals in Spinacia

oleracea irrigated with paper mill effluent

and sewage

Chakresh Pathak, A. K. Chopra & Sachin

Srivastava

Environmental Monitoring and

Assessment
An International Journal Devoted to
Progress in the Use of Monitoring Data
in Assessing Environmental Risks to
Man and the Environment

ISSN 0167-6369

Environ Monit Assess

DOI 10.1007/s10661-013-3104-8

1 23
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 Author's personal copy
Environ Monit Assess
DOI 10.1007/s10661-013-3104-8
Accumulation of heavy metals in Spinacia oleracea irrigated
with paper mill effluent and sewage
Chakresh Pathak & A. K. Chopra &
Sachin Srivastava
Received: 16 July 2012 / Accepted: 16 January 2013
# Springer Science+Business Media Dordrecht 2013
Abstract The present study on heavy metal contami-
nation in soil and their accumulation in edible part
(leaves) and roots of Spinacia oleracea (Spinach) on
irrigation with paper mill effluent (PME)/sewage
revealed that there was significant increase in the nickel
(Ni, +227.17 %) content of the soil irrigated with PME,
whereas in the soil irrigated with sewage chromium
(Cr, +274.84 %), iron (Fe, +149.56 %), and cadmium
(Cd, +133.39 %), contents were increased appreciably.
The value of enrichment factor (EF) for Ni (3.27) indi-
cated moderate enrichment in PME-irrigated soil. The
EF of Fe, zinc (Zn), Cd, and Cr were <2 in PME
effluent-irrigated soil which showed deficiency of min-
imal enrichment. In sewage irrigated soil, EF value for
Cr, Fe, and Cd indicated moderate enrichment, while the
values for Zn and Ni indicated deficiency of minimal
enrichment. Among various metallic concentrations, the
maximum concentration of Fe was observed in leaves
(400.12±11.47 mg/kg) and root (301.41±13.14 mg/kg)
of S. oleracea after irrigation with PME, whereas the
maximum concentrations of Fe was found in leaves
(400.49±5.97 mg/kg) and root (363.94±11.37 mg/kg)
of S. oleracea after irrigation with sewage for 60 days.
The bioaccumulation factor value was found maximum
C. Pathak (*) : A. K. Chopra : S. Srivastava
Department of Zoology and Environmental Science,
Gurukula Kangri University,
Haridwar 249404 Uttarakhand, India
e-mail: chakreshpathak@gmail.com
A. K. Chopra
e-mail: profakchopra@yahoo.co.in
for Cd (2.23) in the plants irrigated with PME while that
of Fe (0.90) in the plants irrigated with sewage. The
undiluted use of PME/sewage for irrigation increased
the concentration of Cr, Cd, Zn, Ni, and Fe metals which
were accumulated in S. oleracea, posing a potential
threat to human health from this practice of irrigation.
Keywords Bioaccumulation factor . Enrichment
factor . Heavy metals . Spinacia oleracea
Introduction
The industrial and municipal wastewater are increas-
ingly being utilized as a valuable resource for irriga-
tion in urban and peri-urban agriculture because of
their easy availability and thus partially solving the
problem of effluent disposal (Mishra et al. 2009;
Gupta et al. 2010; Ghosh et al. 2011). However,
long-term irrigation using industrial/wastewater
results in buildup of heavy metals in soil that can
restrict soil functioning, resulting in toxicity to plants
and contamination of the food chain affecting food
quality and safety (Singh et al. 2010; Ghosh et al.
2011). Thus, heavy metal contamination of vegetables
through soil, water, and other anthropogenic sources
may pose a serious threat to human health.
Heavy metals in wastewater coming from industries
and municipal sewage are one of the main causes of
water and soil pollution (Gupta et al. 2010; Chopra
and Pathak 2012). The concentration of heavy metals
in sewage effluents are usually low, but long-term use
 Author's personal copy
of these wastewaters on agricultural lands often results
in the buildup of the elevated levels of metals in soils
(Rattan et al. 2002). Spinach (Spinacia oleracea) is an
edible flowering plant in the family of Amaranthaceae.
It is a cool-season crop that is easily grown here
through winter and in early spring. It is a leafy vege-
table, and it had greater potential of accumulating
heavy metals in their edible parts than grain or fruit
crops and has hypoglycemic properties. The leaves are
cooling, emollient, antipyretic, diuretic, maturant, lax-
ative, digestible, anthelmintic, useful in urinary con-
cretion, inflammation of the lungs and the bowels,
sore throat, pain in joints, thirst, lumbago, cold and
sneezing, sore eye, ring worm, scabies, leucoderma,
soalding urine, arrest vomiting, biliousness, flatulence,
and have been used in the treatment of febrile con-
ditions (Subhash et al. 2010). Keeping in view of its
medicinal importance, the present study was undertak-
en to assess the accumulation of heavy metals in the
leafy vegetable Spinacia oleracea (spinach) irrigated
with paper mill effluent (PME) and sewage.
Materials and methods
Experimental design
A comparative micro-plot study was conducted in the
experimental garden of the Department of Zoology
and Environmental Sciences, Faculty of Life Sciences,
Gurukula Kangri University Haridwar (29°55′10.81″
N and 78°07′08.12″ E), India during the period of
November 2008–January 2009 to study the accumula-
tion of heavy metals in Spinacia oleracea irrigated
with PME/sewage. The micro-plots (dia. 30 cm) were
used for growing spinach. The experiments were con-
ducted under completely randomized design and were
replicated four times.
Soil analysis
The soil was analyzed for the physicochemical param-
eters and heavy metals before and after harvesting the
crop which had been irrigated for 60 days with PME/-
sewage separately. The soil was analyzed for various
physicochemical parameters following standard meth-
ods, viz. bulk density (BD) by (Carter 1993); pH and
electrical conductivity (EC) by taking the soil:water
ratio of 1:2 using glass electrode pH meter and
Environ Monit Assess
electrical conductivity meter, respectively; sodium
(Na+) and sodium absorption ratio (SAR) (Chaturvedi
and Sankar 2006); organic carbon (OC) by (Walkley
and Black 1934); and total Kjeldahl nitrogen (TKN)
by the Kjeldahl method (Bremner and Mulvaney
1982); available phosphorous (Ava.P) in soil by
extraction with sodium bicarbonate (Na2CO3) (Olsen
et al. 1954); and available potassium (Ava.K+) by
ammonium acetate method (Hanway and Heidel 1952).
Determination of heavy metal content
The soil and S. oleracea (leaves and roots) samples
were dried in air at room temperature. The dried soil
was sieved through 2-mm sieve, and S. oleracea were
grounded in pestle and mortar. The 0.5-g samples were
used for further processing. Samples were digested in
a mixture of concentrated nitric and perchloric acids
(2:1, v/v) as per the method described in Association
of Official Analytical Chemists (1990). In short, after
digestion, all samples were diluted with water (1:3),
filtered through Whatmann no. 42 filter paper, and in
each case, volume was made to 50 ml in a volumetric
flask. Heavy metals such as chromium (Cr), cadmium
(Cd), zinc (Zn), nickel (Ni), and iron (Fe) were deter-
mined in the digested aliquot by atomic absorption
spectrophotometer (ECIL, Model No. 4129) using
specific lamp for particular metal using appropriate
drift blank.
Determination of enrichment factor and bioaccumulation
factor
Enrichment factor (EF) was calculated to determine
the degree of soil pollution and heavy metal accumu-
lation in plants growing in soil contaminated with the
effluents (PME/sewage irrigated) taking soil and
plants growing in the bore well water (BWW) as
control (Barman et al. 2000, and Pathak et al. 2011).
Bioaccumulation factor (BAF) was calculated to quan-
tify accumulation of the individual metals (Likar et al.
2010).
Results and discussion
The mean values (±SD) and percentage increase/de-
crease of different physicochemical parameters, viz.
BD, pH, EC, Cl−, Mg2+, Ca2+, OC, TKN, K, P, Na,
 Author's personal copy
Environ Monit Assess
SAR, and heavy metals (Cr, Ni, Cd, Zn, and Fe) in
soil before and after 60 days of irrigation with
PME, sewage, and BWW, separately, are given in
Table 1.
Physicochemical properties of soil
The present study observed that texture of soil was
loamy sand with alkaline pH (7.9). There was almost
no change in BD (+3.88 to +1.94 %) and pH (+1.24 to +
2.24 %) on irrigation of soil with PME/sewage for
60 days in comparison to soil irrigated with BWW taken
as control. There was a remarkable significant change in
EC (+71.43 %), OC (+90 %), Ava.P (+116.41 %), TKN
(+59.48 %), Na+ (+86.88 %), and SAR (+91.90 %) of
soil on irrigation with PME and in OC (+46.25 %) and
Cl− (+54.12 %) on irrigation of soil with sewage. How-
ever, there was no significant change in Cl− (+0.47 %),
Mg2+ (+20.42 %), and Ava.K+ (+38.43 %) of soil on
irrigation with PME and in EC (+14.29 %), Mg2+
(20.42 %), TKN (+5.60 %), Ava.P (+17.17 %), Na+ (+
10.44 %), and SAR (+17.04 %) of soil irrigated with
sewage. There was a decrease in Ca2+ (−4.44 %
to −20.56 %) of soil irrigated with PME/sewage where-
as Ava.K+ (−18.93 %) was found to be lower in sewage-
irrigated soil used for growing of the crop S. oleracea
for 60 days (Table 1).
Heavy metals contents in the soil
The study observed that among the concentration of
various heavy metals in PME irrigated soil, the con-
centration of Ni (206.18 mg/kg) and Cd (6.11 mg/Kg)
were above the permissible limit. Similarly in sewage-
irrigated soil concentration of Ni (70.78 mg/Kg), Cd
(13.42 mg/kg), and Zn (61.12±9.07) were above the
permissible limit of Temmerman et al. (1984), Kabata-
Pendias and Pendias (1992), and Indian Standards of
Awashthi (2000) (Table 2).
The concentrations of heavy metals Cr (29.53±
3.33 mg/kg), Ni (206.18±13.44 mg/kg), Cd (6.11±
1.74 mg/kg), Zn (49.58 ± 3.44 mg/kg), and Fe
(277.23±12.06 mg/kg) in soil irrigated with PME
was lower than the concentration reported by
Sinha et al. (2008) for Fe (14,285±1244 mg/kg),
Cr (197.76 ± 12.83 mg/kg), and Zn (104.91 ±
0.97 mg/kg) in the soil irrigated with tannery
wastewater and than the concentration reported by
Ahmad and Goni (2010) reported for Zn (115.43±
7.75 mg/kg), Cr (53.70±12.37 mg/kg), Cd (11.42±
4.63 mg/kg), Fe (1,715.80±421.33 mg/kg) except
Ni (58.16 ±18.15 mg/kg) in wastewater irrigated
soil at industrial areas of Bangladesh.
The concentration of Zn (61.12±9.07 mg/kg) and
Cd (13.42±4.59 mg/kg) in sewage irrigated soil were
found to be lower than the concentration of Zn
(264.09±3.05 mg/kg) and (Cd 24.66±1.87 mg/kg) in
sewage irrigated soil of Dehradun reported by Rai et
al. (2011); and the concentration of Fe (446.32 ±
8.15 mg/kg) and Zn (61.12±9.07 mg/kg) in the pres-
ent study were lower than the values reported by
Pathak et al. (2011) for Fe (487.05±59.37 mg/kg)
and Zn (254.65±32.95 mg/kg) in sewage irrigated soil
of Haridwar. The concentrations of Ni (+227.17 %),
Cr (+59.45 %), and Fe (+55.02 %) were found to be
more in PME-irrigated soil, while Cr (+274.84 %), Cd
(+133.39 %), Fe (+149.56 %) were more in sewage-
irrigated soil in comparison to BWW.
The Pearson’s correlation at 5 % level between
physicochemical parameters and heavy metals in
PME irrigated soil indicated that BD-P, BD-Cd, pH-
Ca, pH-P, Mg-Ca, OC-K, OC-Na, OC-SAR, OC-Fe,
N-Na, N-SAR, N-Ni, N-Zn, P-Cd, K-Na, K-SAR, K-
Cd, K-Fe, SAR-Cr, SAR-Zn, SAR-Fe, Cr-Fe, and Ni-
Zn had a strong positive correlation (Table 3). In the
sewage-irrigated soil, strong positive correlation was
found between BD-EC, BD-Ca, BD-OC, BD-Cd, pH-
Cl, pH-Mg, pH-Na, pH-SAR, EC-OC, Cl-Mg, Cl-Na,
Cl-SAR, Cl-Fe, Mg-Na, Mg-SAR, Ca-Cd, P-Cr, P-Ni,
P-Zn, K-Cr, Na-SAR, SAR-Fe, Cr-Zn, and Ni-Zn
(Table 4).
EF for soil
The EF for soil differed depending on the type and
concentration of the effluents and the type of soil. The
present value of Ni (3.27) in PME-irrigated soil
showed moderate enrichment while values of Cr
(1.59), Fe (1.55), Zn (1.14), and Cd (0.94) were found
to be deficient thereby indicating minimal enrichment
of the soil. In sewage-irrigated soil, the EF values
showed that Cr (3.74), Fe (2.49), and Cd (2.33) were
in moderate enrichment category, while Zn (1.40) and
Ni (1.12) were in deficient to minimal enrichment
category (Fig. 1). These EF values of Cr, Fe, and Zn
in sewage-irrigated soil were lower than the values of
Cr (4.58), Fe (2.81), and Zn (2.15) in soil irrigated
with wastewater generated from the sponge iron
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Environ Monit Assess

Table 1 Physicochemical properties of soil before and after irrigation of BWW-, PME-, and sewage-irrigated soil

Parameters Before irrigation BWW Irrigation After PME irrigation (60 days) After sewage irrigation (60 days)
(60 days)

Texture Sandy loam Sandy loam Sandy loam Sandy loam

BD g/cm3 1.08 1.03±0.05 1.07±0.01 (+3.88 %) 1.05±0.03 (+1.94 %)
−1
EC dsm 0.12 0.14±0.06 0.24±0.10 (+71.43 %) 0.16±0.02 (+14.29 %)
pH 7.9 8.05±0.06 8.15±0.06 (+1.24 %) 8.23±0.09 (+2.24 %)
Cl− (mg/kg) 6.53 48.74±7.25 48.97±9.63 (+0.47 %) 75.12±12.45 (+54.12 %)
Mg++ (mg/kg) 10.22 4.75±0.59 5.72±0.92 (+20.42 %) 5.72±3.11 (+20.42 %)
Ca+ (mg/kg) 20.02 45.04±4.77 43.04±8.88 (−4.44 %) 35.78±6.71 (−20.56 %)
OC (%) 1.07 0.80±0.14 1.52±0.13 (+90 %) 1.17±0.15 (+46.25 %)
K+ (mg/kg) 114 130.75±10.44 181±13.95 (+38.43 %) 106±8.68 (−18.93 %)
TKN (mg/kg) 2.06 2.32±0.86 3.70±0.16 (+59.48 %) 2.45±0.21 (+5.60 %)
P (mg/kg) 56.96 57.66±5.60 124.78±16.24 (+116.41 %) 67.56±3.56 (+17.17 %)
Na+(mg/kg) 17.30 17.91±1.59 33.47±2.66 (+86.88 %) 19.78±2.67 (+10.44 %)
SAR 1.14 3.58 6.87±0.94 (+91.90 %) 4.19±0.68 (+17.04 %)

Percentage increase/decrease given in parenthesis

industries (Gupta et al. 2008), Zn (4.8) in wastewater
irrigated soil (Mishra and Tripathi 2008), Cd (3) in
wastewater irrigated soil (Gupta et al. 2010), and Ni
(2.28) in wastewater-irrigated soil (Pathak et al. 2011)
which were also in the moderate enrichment catego-
ries. However, Pathak et al. (2011) observed EF for Zn
(7.96) in significant enrichment categories in sewage-
irrigated soil.
Heavy metals in leaves and root of Spinacia oleracea
The heavy metal concentrations in leaves and roots of
S. oleracea after 60 days of effluent irrigation are
shown in Table 5. The concentration of heavy metals
(Ni, Cr, Zn, and Cd) in edible parts of S. oleracea
irrigated with PME were found above the permissible
limits of Indian Standard (Awashthi 2000). In the
values of heavy metals in both leaves and roots of S.
oleracea irrigated with PME, it was observed that the
concentration of Ni, Cr, and Cd were also above the
permissible limits as indicated by (FAO/WHO stan-
dard Codex Alimentarious Commission 1984; SEPA
2005).
In sewage-irrigated soil, concentration of Ni, Cr, Cd
in both leaves and roots and Zn only in leaves of S.
oleracea were above the permissible limit of
(FAO/WHO standard Codex Alimentarious Commis-
sion 1984; Indian Standard Awashthi 2000 and SEPA
2005). Though the Fe was found to be maximum in
PME/sewage, it was lower than the permissible limit.

Table 2 Heavy metals present in soil before and after irrigation of BWW-, PME-, and sewage-irrigated soil for 60 days

Parameters Before BWW After PME irrigation After sewage irrigation Permissible Permissible Permissible
(mg/kg) irrigation irrigation (60 days) (60 days) limit (a) limit (b) limit (c)
(60 days)

Cr 16.72 18.52±2.89 29.53±3.33 (+59.45 %) 69.42±6.74 (+274.84 %) NA 100 100

Ni 75.39 63.02±6.07 206.18±13.44 (+227.17 %) 70.78±5.05 (+12.31 %) 75–150 30 40
Cd 5.56 5.75±1.36 6.11±1.74 (+6.26 %) 13.42±4.59 (+133.39 %) 3–6 1 0.06
Zn 33.73 43.44±4.25 49.58±3.44 (+14.13 %) 61.12±9.07 (+40.69 %) 300–600 100 50
Fe 171.57 178.84±6.71 277.23±12.06 (+55.02 %) 446.32±8.15 (+149.56 %) – 1,000 –

% increase/decrease given in parenthesis. Source: (a) Awashthi (2000), (b) Kabata-Pendias and Pendias (1992), (c) Temmerman et al.
(1984)
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Table 3 Correlation between physicochemical parameters and heavy metals irrigated with PME

BD pH EC Cl Mg Ca OC N P K Na SAR Cr Cd Ni Zn Fe

BD 1
pH 0.392 1
EC 0.287 −0.629 1
Cl −0.115 0.017 −0.602 1
Mg −0.148 0.457 −0.070 −0.753 1
Ca 0.134 0.911 −0.541 −0.282 0.774 1
OC 0.358 0.002 −0.255 0.862 −0.888 −0.399 1
N −0.551 −0.271 −0.541 0.884 −0.631 −0.407 0.579 1
P 0.895 0.760 −0.086 −0.103 0.141 0.545 0.226 −0.545 1
K 0.461 0.000 −0.159 0.792 −0.884 −0.410 0.992 0.479 0.299 1
Na 0.057 0.448 −0.815 0.902 −0.471 0.145 0.766 0.677 0.230 0.701 1
SAR −0.069 −0.413 −0.152 0.877 −0.963 −0.702 0.872 0.817 −0.276 0.834 0.603 1
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Cr 0.037 −0.733 0.362 0.518 −0.935 −0.947 0.672 0.514 −0.346 0.680 0.141 0.865 1
Cd 0.927 0.402 0.037 0.267 −0.418 0.039 0.670 −0.202 0.837 0.742 0.403 0.257 0.217 1
Ni −0.952 −0.375 −0.430 0.413 −0.110 −0.231 −0.059 0.779 −0.862 −0.173 0.215 0.343 0.145 −0.768 1
Zn −0.656 −0.650 −0.167 0.663 −0.649 −0.693 0.403 0.905 −0.796 0.320 0.315 0.788 0.685 −0.393 0.816 1
Fe 0.408 −0.517 0.429 0.439 −0.913 −0.812 0.755 0.270 0.021 0.800 0.161 0.770 0.927 0.549 −0.221 0.384 1
Table 4 Correlation between physicochemical parameters and heavy metals irrigated with sewage

BD pH EC Cl Mg Ca OC N P K Na SAR Cr Cd Ni Zn Fe

BD 1
pH −0.454 1
EC 0.778 −0.215 1
Cl −0.293 0.981 −0.022 1
Mg −0.098 0.884 0.264 0.956 1
Ca 0.914 −0.611 0.469 −0.510 −0.406 1
OC 0.891 −0.147 0.951 0.047 0.296 0.632 1
N −0.008 −0.200 −0.634 −0.308 −0.526 0.376 −0.413 1
P −0.860 −0.065 −0.747 −0.233 −0.396 −0.674 −0.913 0.121 1
K −0.309 0.241 0.351 0.288 0.438 −0.630 0.087 −0.943 0.210 1
Na −0.305 0.984 −0.038 10.00 0.951 −0.516 0.032 −0.296 −0.222 0.281 1
SAR −0.326 0.986 −0.169 0.980 0.886 −0.471 −0.054 −0.115 −0.199 0.113 0.983 1
Author's personal copy

Cr −0.855 0.364 −0.355 0.274 0.224 −0.952 −0.589 −0.491 0.751 0.750 0.278 0.201 1
Cd 0.789 −0.670 0.253 −0.612 −0.568 0.971 0.426 0.565 −0.502 −0.760 −0.614 −0.536 −0.927 1
Ni −0.428 −0.597 −0.369 −0.703 −0.741 −0.253 −0.579 0.042 0.822 0.191 −0.698 −0.712 0.478 −0.113 1
Zn −0.656 −0.292 −0.393 −0.402 −0.443 −0.578 −0.650 −0.196 0.903 0.470 −0.397 −0.444 0.767 −0.470 0.930 1
Fe 0.329 0.629 0.174 0.700 0.677 0.231 0.420 0.147 −0.730 −0.342 0.699 0.750 −0.491 0.135 -0.977 -0.924 1
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Fig. 1 Enrichment factor

for soil irrigated with PME
and sewage

The present study revealed that concentration of
heavy metals such as Zn (52.40± 5.97 mg/kg), Fe
(400.12±11.47 mg/kg), Cr (40.45±8.39 mg/kg), and
Cd (13.64±2.56 mg/kg) was found to be higher in
leaves in comparison to Zn (42.53±4.84 mg/kg), Fe
(301.41±13.14 mg/kg), Cr (31.47±5.89 mg/kg), and
Cd (6.83±1.14 mg/kg) in roots, while concentration of
Ni (30.58±4.99 mg/kg) was found to be lower in
leaves than Ni (41.96±6.61 mg/kg) in roots of S.
oleracea irrigated with PME. The heavy metal con-
tents of Zn and Fe in leaves of S. oleracea were found
to be higher than the Zn (33.10±1.90 mg/kg) and (Fe-
309±27.0 mg/kg) as reported by Arora et al. (2008) in
S. oleracea irrigated with wastewater. Whereas Mishra
and Tripathi (2008) have reported lower values for Zn
(62.24 mg/kg) except for Cr (4.08 mg/kg) and Cd
(0.39 mg/kg) in S. oleracea grown in the wastewater
irrigated areas.
In the present study, the concentration of Zn (52.56±
3.95 mg/kg) in leaves of S. oleracea irrigated with
sewage was lower than in spinach (Zn-85.2 mg/kg)
grown in sewage irrigated areas of Najafgarh site, New
Delhi as reported by Singh and Kumar (2006). Chary et
al. (2008) also observed lower concentration of Zn
(10 mg/kg), Cr (2.9 mg/kg), and Ni (3.2 mg/kg) in S.
oleracea irrigated with sewage in the Musi river area of
Hyderabad.
The metal accumulation in the PME-irrigated plants
showed that concentration of Cr (40.45±8.39 mg/kg)
and Cd (13.64±2.56 mg/kg) was more in the leaves,

Table 5 Heavy metal contents and enrichment factor (EF) in leaves and roots of S. oleracea irrigated by PME, sewage and BWW for
60 days

Metals (mg/kg) S. oleracea PME Sewage BWW Permissible Permissible Permissible

irrigated irrigated irrigated limita limitb limitc

Zn Leaves 52.40±5.97 (1.29) 52.56±3.95 (1.29) 40.64±4.53 50 60 100

Root 42.53±4.84 (1.76) 37.13±4.66 (1.54) 24.18±4.04
Fe Leaves 400.12±11.47 (2.36) 400.49±5.97 (2.36) 169.52±3.50 – 450 –
Root 301.41±13.14 (2.153) 363.94±11.37 (2.60) 139.98±7.47
Ni Leaves 30.58±4.99 (0.99) 49.66±4.84 (1.60) 30.97±2.86 1.5 20 10
Root 41.96±6.61 (1.19) 134.73±6.76 (3.82) 35.24±6.08
Cr Leaves 40.45±8.39 (1.97) 29.97±5.95 (1.46) 20.57±1.79 20 5 0.5
Root 31.47±5.89 (1.14) 46.14±7.32 (1.67) 27.66±7.71
Cd Leaves 13.64±2.56 (3.88) 7.23±1.03 (2.05) 3.52±0.56 1.5 0.3 0.2
Root 6.83±1.14 (1.25) 9.21±2.40 (1.69) 5.46±1.08

EF values of leaves and root given in parenthesis

a
Source: Indian standard (Awashthi 2000)
b
Source: FAO/WHO standard (Codex Alimentarious Commission 1984)
c
Source: SEPA (2005)
 Author's personal copy
while the Zn (42.53±4.84 mg/kg) was increased in
roots of PME-irrigated plants. The Fe, Cd, and Cr
were found to be increased in the roots, while Ni
was found to be increased in both leaves and roots of
sewage-irrigated plants. It was observed that the nu-
trient status including the heavy metals was increased
in soil and S. oleracea irrigated with undiluted PME.
Similarly, Kumar and Chopra (2011) have reported the
increase of heavy metals like Fe, Zn, Cd, Cu, Pb, and
Cr in soil and Trigonella foenum-graecum L.
(Fenugreek) with increase in effluent concentration
(100 %) of distillery effluent.
EF and BAF for S. oleracea
In case of PME irrigation, the EF values (>2) for Fe
and Cd indicated moderate enrichment of these metals
in leaves and root of the crop S. oleracea, while in
case of sewage irrigation, the EF values (>2) for Ni in
roots and for Cd in leaves and for Fe in both leaves
and roots indicated moderate enrichment (Table 4).
The values of Fe (2.36) in leaves and roots (2.60) were
lower than the values recorded for Fe (2.89) in the
tomato plants grown in the soil irrigated with waste-
water generated from the sponge iron industries by
Gupta et al. (2008).
According to Cluis (2004), hyperaccumulating
plants have a BAF more than 1.0. Mishra et al.
(2009) stated that BAF values differed significantly
among locations or plant species. The difference in
BAF between locations may be related to soil nutrient
management and soil properties. They observed that S.
oleracea had the maximum BAF of heavy metals
followed by Raphanus sativus (Radish), Solanum
Fig. 2 Bioaccumulation
factor for soil to leaves of
S. oleracea irrigated with
PME, sewage and BWW
Environ Monit Assess
melongena (Brinjal), and Oryza sativa (Rice). Zhuang
et al. (2009) found that average BAF values of leafy
vegetables were significantly higher than for non-leafy
vegetables. In the present study, BAF values obtained
from the PME-irrigated soil showed efficient
accumulation of Cd (2.23), Fe (1.44), Cr (1.37), and
Zn (1.06) from root to leaves of S. oleracea (Fig. 2).
The present study revealed that irrigation with undi-
luted concentration of PME/sewage increased the values
of EC, OC, K+, TKN, P, Na+, and SAR in the soil, while
there was a maximum increase in the amount of Cl− in
sewage-irrigated soil. Among the heavy metals present in
the soil, the concentration of Fe (277.23/446.32 mg/kg)
was found maximum in PME/sewage irrigated soil, but it
was below the permissible limit of standards. The con-
centrations of Ni (206.18/70.78 mg/kg) and Cd
(6.11/13.42 mg/kg) were found above the permissible
limits on irrigation with PME/sewage.
In the crop S. oleracea, the concentration of Fe was
found maximum in leaves/roots (400.12/301.41 mg/kg)
on irrigation with PME, while in sewage irrigated
leaves/roots, Fe was also found maximum
(400.49/363.94 mg/kg) but below the permissible limit.
However, the concentration in leaves/roots of Ni
(30.58/41.96 mg/kg), Cr (40.45/31.47 mg/kg) and Cd
(13.64/6.83 mg/kg) were found increased above the
permissible limit in PME-irrigated S. oleracea. In sew-
age irrigated crop, concentration in leaves/roots of Ni
(49.66/134.73 mg/kg), Cr (29.97/46.14 mg/kg), and Cd
(7.23/9.21 mg/kg) were also found increased above
permissible limit. The concentration of Zn
(52.40/52.56 mg/kg) increased above the permissible
limit only in leafy part of the crop on irrigation with
PME/sewage.
 Author's personal copy
Environ Monit Assess
Conclusion
It was concluded that undiluted effluent irrigation of
PME/sewage for 60 days increased the nutrient status
of the soil including an increase in heavy metals like
Ni and Cd which in turn was responsible for the
increase of heavy metals like Ni, Cr, and Cd in leaves/-
roots of S. oleracea. Thus, the practice of using undi-
luted PME/sewage as agro-based organic fertilizer for
irrigation may accumulate the heavy metals in vegeta-
bles posing a potential threat to human health. The
regular monitoring of these toxic heavy metals in soil
and parts of vegetables is essential to prevent their
excessive buildup in the food chain. Therefore, proper
dilution of PME and sewage appears to be necessary
for irrigation purpose for the minimum accumulation
of heavy metals in soil and plants.
Acknowledgments The University Grant Commission, New
Delhi, India is acknowledged for providing the financial support
in the form of UGC research fellowship (F.7-70/2007 BSR) to
Mr. ChakreshPathak.
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