ARTICLE IN PRESS

Ecotoxicology and Environmental Safety 69 (2008) 513524

www.elsevier.com/locate/ecoenv

Assessing risk of heavy metals from consuming food grown on sewage

irrigated soils and food chain transfer
N. Sridhara Charya,, C.T. Kamalaa, D. Samuel Suman Rajb
a

Analytical Chemistry and Environmental Sciences Division, Indian Institute of Chemical Technology, Hyderabad-500 007, India
Center for Environment, Institute of Science and Technology, Jawaharlal Nehru Technological University, Hyderabad-500 072, India

Received 24 April 2006; received in revised form 9 April 2007; accepted 14 April 2007
Available online 6 June 2007

Abstract
Heavy metal pollution of soils resulting from sewage and wastewater irrigation is causing major concern due to the potential risk
involved. In the present study Musi River and its environs were assessed for heavy metal contamination. The study area was assessed for
Zn, Cr, Cu, Ni, Co and Pb in soils, forage grass, milk from cattle, leafy and non-leafy vegetables. Partitioning pattern of soil revealed
high levels of Zn, Cr, and Cu associated with labile fractions, making them more mobile and plant available. The associated risk was
assessed using hazard quotient (HQ). Human risk was assessed in people known to consume these contaminated foods by analyzing
metals concentrations in venous blood and urine. Results showed high amounts of Pb, Zn, Cr, and Ni compared to permissible limits.
HQ was found to be high for Zn followed by Cr and Pb with special reference to leafy vegetables particularly spinach and amaranthus.
r 2007 Elsevier Inc. All rights reserved.
Keywords: Heavy metals; Sewage; Vegetables; Health hazard; Musi River; Risk assessment

1. Introduction
Land spreading of untreated sewage efuents is practiced
all over the world because of the economic advantage it
offers over efuent treatment. Heavy metals can also
accumulate in the soil at toxic levels as a result of long-term
application of untreated wastewaters. Soils irrigated by
wastewater accumulate heavy metals such as Cr, Zn, Pb,
Cd, Ni, etc in surface soil. When the capacity of the soil to
retain heavy metals is reduced due to repeated application
of wastewater, heavy metals leach into ground water or soil
solution available for plant uptake. For the metals derived
from anthropogenic sources, this can strongly inuence
their speciation and hence bioavailability. However, the
heavy metal content in plants can also be affected by other
factors such as the application of fertilizers, sewage sludge
or irrigation with wastewater (Devkota and Schmidt, 2000;
Frost and Ketchum, 2000; Mangwayana, 1995). Studies
have shown that heavy metals are potentially toxic to
crops, animals and humans when contaminated soils are
Corresponding author.

E-mail address: sreedharacharya@rediffmail.com (N. Sridhara Chary).

0147-6513/$ - see front matter r 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.ecoenv.2007.04.013

used for crop production (Xian, 1989). Heavy metals may

enter the human body through inhalation of dust,
consumption of contaminated drinking water, direct
ingestion of soil and consumption of food plants grown
in metal-contaminated soil (Cambra et al., 1999; Dudka
and Miller, 1999). Vegetables constitute an important part
of the human diet since they contain carbohydrates,
proteins, as well as vitamins, minerals, and trace elements.
It is known that serious systemic health problems can
develop as a result of excessive accumulation of dietary
heavy metals such as Cd, Cr, and Pb in the human body
(Oliver, 1997). One important dietary uptake pathway of
metals could be through crops irrigated with contaminated
wastewater.
In suburban parts of India, the use of industrial or
municipal wastewater for irrigation purpose is a common
practice (Singh et al., 2004). To face the growing demand
for irrigation water, non-conventional resources are often
used. Important sources of heavy metals in wastewater are
urban and industrial efuents and deterioration of
sewerage pipelines. Irrigation with wastewater is known
to contribute signicantly to the heavy metal content of
soils (Mapanda et al., 2005; Nan et al., 2002; Singh et al.,

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2004). In India, total wastewater generated per annum

from 200 cities is about 2600 Mm3 (Kaul et al., 1989) and
also the use of sewage efuents for irrigating agricultural
lands is on the rise especially in the peri-urban areas.
Although the concentration of heavy metals in sewage
efuents are low, in many cases these are contaminated
with industrial wastes and long-term use of these wastewaters often results in the build-up of the elevated levels of
these metals in soils (Rattan et al., 2002). Since food chain
contamination is one of the major routes for entry of
metals into the animal system, monitoring the bioavailable
pools of metals in contaminated soils has generated a lot of
interest (Datta et al., 2000; Yadav et al., 2002).
The Musi River ows into Hyderabad, capital of Andhra
Pradesh, India as a clean resource until it reaches the
T-main sewer where 25 million liters per day (mld) of
untreated sewage is released. It is from this point that the
river serves as little more than a sewer drain. Even during
monsoon, runoff inows are very low in comparison to the
quantity of sewage discharged into the river. During
monsoon the Musi River catchment area receives
700800 mm of rainfall, but because of the large inputs of
domestic sewage and industrial wastewaters, self-purication within the river and dilution are minimum (EPTRI,
1997; Sircar, 2000). Due to the rapid unplanned development of the city of Hyderabad, the quantity of sewage
generated is many times more than the design capacity of
the Amberpet Sewage Treatment Plant (STP). This results
in a high percentage of under-treated and untreated sewage
entering the river. The capacity of the Amberpet STP is
115 mld, but the plant typically receives 350 mld, which
includes industrial efuents (Sircar, 2000; Musi River,
2001; CPCB, 2002). This drainage water which is from
both domestic and industrial sources, is channeled to
several contiguous plots of land or some times supplemented by water pumped from the river for irrigation.
Organic pollutants in the river are partially eliminated by
self-purication and accessible dilution. The inorganic
pollutants (heavy metals) are the fraction of greatest
concern due to their persistence in sewage sludge, which
later becomes a potential source of risk to the nearby soils
and vegetation. Episodes of heavy metal pollution of the
Musi River and its surroundings have been reported
(Chandra Sekhar et al., 2005; Kumari et al., 1991;
Venkateshwarulu and Sampath Kumar, 1982; Bansal,
1998). Along the banks of the Musi intensive cultivation
of fodder grass (para grass) and food crops occurs in the
sewage sludge, and the concentrations of heavy metals are
reported to be very high (Kumari et al., 1991; Venkateshwarulu and Sampath Kumar, 1982; Bansal, 1998;
Anjaneyulu, 2001; Chandra Sekhar et al., 2005). Grass
raised along the river is the fodder for most of the cattle in
and around Hyderabad (Buechler et al., 2002; Sircar,
2000). A variety of vegetable crops are also cultivated on
the banks of the river and sold in the nearby market.
Earlier studies by authors on river Musi reported
concentrations of metals in soils and corresponding

accumulation in nearby vegetation (Chandra Sekhar

et al., 2005). These studies can only be regarded as base
line data since there exists no explanation regarding the
metal accumulation status and also possible mobility into
nearby plants of the Musi River stretch. Further there are
no reported studies on the assessment of possible health
risk linked with consumption of these contaminated foods
(milk, vegetables). Thereby a study was conducted along
the stretch of Musi River to assess the concentration of
heavy metals in soils, resulted uptake by the plant and
elevated transfer to human food chain that helps in
assessing the related health hazard associated with it. The
metal concentrations in soil and vegetables are compared
with established permissible limits. Also a dietary intake of
vegetables by human were calculated and compared with
the recommended dietary intakes.
2. Experimental
2.1. Study site and sampling
2.1.1. Soil
Soil sampling was carried out at 12 different locations
along and across 8 km stretch of the Musi River, including
2 km on either side of the river. Soils were mainly red sandy
loam and brownish sandy soil with black clay subsoil.
Geologically the Musi basin is covered by granites of
Archean age and intercalated with quartz veins here and
there and is at an altitude of 500 m above mean sea level
(M1) and 470 MSL (M12). The location map of the Musi
River stretch along with the 12 sampling sites (M1M2) is
shown in Fig. 1. The study area consists of approximately
23.33 km2 under residential use, 4.95 km2 with plantations
and harvested land, and 18.12 km2 land with scrub
(Anjaneyulu, 2001).
Sampling was carried out using standard protocols
(USEPA, 1992). An 8 cm diameter stainless steel auger
capable of retrieving a cylindrical plug of soil 2 inch in
diameter and 2 inch deep was used for soil collection.
Twelve points where the surface was free of plant material
and debris were selected for soil sampling on each plot.
Samples were taken from surface till the depth of 20 cm
with a composite of 1015 subsamples taken across a
1  1 m square pit. Samples were placed in plastic bags and
sealed for transport and storage. In the laboratory, the
samples were air-dried, mechanically ground and sieved to
obtain o2 mm fraction. A 2030 g subsample was drawn
from the bulk soil (o2 mm fraction) and reground to
obtain o200 mm fraction using a mortar and pestle. Soil
samples were digested using HF/HClO4 for total metals
(Zn, Cr, Cu, Ni, Pb and Cu). The extracts were analyzed
using a Varian Ultra Mass 700 ICP-MS.
2.1.2. Vegetation
A diversity of crops are grown along the Musi River in
the study area. The predominant crop is forage grass/para

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515

Fig. 1. Location map of the study area showing the 12 sampling points.

grass (Panicum maximum) (65%), followed by banana

(Musa domestica) (15%), coconut (Cocus nucifera) (10%)
and various vegetables (10%) (Buechler et al., 2002). The
vegetables are grown on small sections of land both for
subsistence and for sale in nearby markets. Rice being the
staple food and leafy vegetables constitute a major portion
of local diets, samples of spinach (Spinacae Oleracea),
amaranthus (Amaranthus graecizans.), coriander leaves
(Coriandrum sativum), mint leaves (Mentha spicata), and
other vegetables including ladies nger (Abelmoschus
esculentus), and brinjal (Solonum melengina) were harvested at marketable stages of development to assess the
human dietary intake of heavy metals. Also, forage grass
samples from the 12 sampling sites were collected and
analyzed for total metal content. The crops were taken to
the laboratory within 1 h of harvesting and washed
as would be done during normal food preparation to
remove any surface deposits. Further composite samples of
each vegetable (Spinach 46; Amaranthus 36; Mint
Leaves 40; Coriander 38; brinjal 33; Ladies nger 30)
for each species were separated into edible and non-edible
parts. The plant parts were then dried (80 1C, 24 h), 1 g of
dried sample was wet ashed (5 N HNO3/ 5 N HClO4/ 2 N
H2SO4 10:1:1) (Bech et al., 1997) and solutions were made
up to 50 ml and analyzed for metals content using ICP-MS.
2.1.3. Milk
A major part of land in the study area is used for fodder
cultivation. Approximately 60% of the fodder grass grown
is sold at market. The other 40% is used directly by the
farmers for their livestock (Buechler et al., 2002). Buffalos
milk is locally preferred over cows milk, and has relatively
low cholesterol and high fat content (Ismail, 2004; Indian

Dairy, 2004). Thus, most of the fodder is consumed by

buffaloes (Buechler et al., 2002; Buechler and Devi, 2003).
The forage grass harvested along the river is chopped into
small pieces and fed to the cattle. Milk samples were
collected soon after calving during early hours of the day
before milking. After discarding the rst 56 drops samples
of milk (300 ml) were collected from buffaloes and cows fed
on this forage grass. Milk samples were collected in sterile
polyethylene sampling bottles prewashed with 20% HNO3.
No pretreatment was given to the samples. After collection,
the samples were transferred to the lab in an ice-cold box
and then digested for metals analysis. A known volume of
milk (20 ml) was evaporated to near dryness, wet ashed
and taken up in 25 ml of 0.2% HNO3 (Tripathi et al.,
1999). For control samples, milk was collected from cattle
that were fed on pastures away from the city of Hyderabad.
2.2. Control samples
Samples of soil, forage grass, and vegetables were
collected from the residential campus area of our research
laboratory covering an area of 18 km2, which is free from
obvious sources of industrial and vehicular pollution. This
area is on the outskirts of the city of Hyderabad and is
distant from the most intense pollution zone. The campus
area is situated 7 km away from the main road, which
forms a subroute from the national highway, and trafc
density is very low. Because this campus is located in a
residential area, movement of heavy vehicles is restricted,
which helps minimize pollution. All the samples were
collected in triplicate from 10 different sampling sites (total
30 samples) in this area. The sampling was similar to that
of the contaminated soils.

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2.3. Fractionation studies

The distribution of heavy metals in the different forms
and phases in which they occur in soil can be determined
using sequential extraction procedures (Legreton, 1993).
Sequential extraction procedure provides information
about the differentiation of the relative binding strength
of the metal on various solid phases and about their
potential reactivity under different physico-chemical environmental conditions. In the present study a six-step
modied Tessier sequential extraction scheme (Chwastowska and Skalmowski, 1997) was applied for the extraction of
metals in soil samples for assessing the mobility of the
metals.
2.4. Reagents
All chemicals used were of analytical reagent grade. All
solutions were prepared in deionized water (zero metal
concentration). Calibration standards for each metal were
prepared by appropriate dilution of stock solution of
1000 ppm of J.T. Baker/E. Merck standards.
2.5. Instrumentation and analysis
Concentrations of Zn, Cu, Cr, Ni, Pb, and Co were
measured in all samples and sequentially extracted
fractions by Ultra Mass 700 ICP-MS (Varian, Australia).
Mathematical equations that were built into the software
(Jarvis et al., 1992) were used for isobaric interference
corrections. Quality control measures were taken to assess
contamination and reliability of the data. Canadian
reference standards CANMET SO-1, SO-2 and SO-4 were
used to conrm the accuracy of the analytical data. A 10%
Rhodium solution of 1 mg/L concentration was added to
all sample solutions as an internal standard before analysis
DDI

Conversely, an exposed population of concern will experience health risks if the dose is equal to or greater than the
RfD. Although the HQ-based risk assessment method does
not provide a quantitative estimate on the probability of an
exposed population experiencing a reverse health effect, it
indeed provides an indication of the risk level due to
pollutant exposure. This risk estimation method has recently
been used by researchers (Chien et al., 2002; Wang et al.,
2005) and proved to be valid and useful. An estimate of the
potential hazard to human health (HQ) through consumption of vegetables grown on metal-contaminated soil was
calculated using the equation below:
HQ

W plant   M plant 
,
Rf D  B

where [Wplant] is the dry weight of contaminated plant

material consumed (mg d1), [Mplant] is the concentration of
metal in the vegetable(s) (mg kg1), RfD is the food
reference dose for the metal (mg d1), and B is human
body mass (kg). Values of RfD for Zn (0.3 mg/kg) and Ni
(0.02 mg/kg) were taken from Integrated Risk Information
System (IRIS, 2003) for remaining four metals the RfD
values were used from Department of Environment, Food
and Rural Affairs (DEFRA) reference dose (DEFRA and
Environmental Agency, 1999). B an average adult body
weight of 68 kg was considered for the calculation of HQ.
Further a daily dietary index (DDI) was considered where
the residents of the study were asked to complete a
questionnaire. The questions included their occupation,
duration of stay, their diet and its source, and they were
asked to keep a dietary document of the precise food and
drinks ingested over a period prior to providing blood and
urine samples. As the migration of population is signicant,
samples were collected from residents only if their length of
residence in the community was more than 5 years. From
the above information DDI was calculated using following
equation (average body mass was taken as 68 kg):

metal in vegetable  Dry wt: of the vegetable  approximate daily intake

.
Body mass in kg

(Balaram et al., 1992). Precision and accuracy of analysis

were also ensured through repeated analysis of samples
against CRMs for all metals. For QA/QC of vegetation,
milk, and clinical samples, due to the non-availability of
CRMs in our laboratory, recovery studies were conducted
using standard additions. Recovery values in the range of
72% were accepted, otherwise analyses were repeated.
2.6. Risk assessment
Risk to human health from the intake of metalcontaminated vegetables was characterized using hazard
quotient (HQ). HQ is a ratio of determined dose of a
pollutant to the dose level (a reference dose or RfD). If the
ratio is less than 1, there will not be any obvious risk.

Urine samples and venous blood samples were collected

from people of varying age groups and analyzed for metals
content using ICP-MS. Upon collection the venous blood
and urine samples were placed in an ice-cold box (4 1C),
transferred to the lab, and then refrigerated until further
analysis. Samples were digested according to the method
suggested by Nelms (2003). For control, samples of blood
and urine were collected from authors and participants
residing in the campus area of our research laboratory.
3. Interpretation of results
3.1. Soil
The soil consisted of mainly red sandy loam/brown
sandy soil with clay subsoil. pH of the soil ranged from

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near neutral to moderately acidic (5.97.3). The soils

reported moderate cation exchange capacity (CEC) which
ranged between 22.7 and 29.2 c mol kg1 indicating average
metal retention capabilities. The % organic carbon was
found to be in high due to constant sewage ows and
ranged between 4.9 and 6.2%. As the subsoils were clayey
the organic carbon was found to be in high percent. Metal
Retention was found to be high in all soils due to high
percent of organic content, which is in good agreement
with our fractionation studies. The metal contents of the
soil along with background values, tolerable levels, normal
ranges and permissible Indian standards are presented in
Table 1.
Background values were considered from the earlier
studies conducted on these soils. The values have shown a
remarkable increase compared to earlier values indicating
the increase in the metal contents contributed by sewage
and constituent contaminants. Among the six metals
studied the concentration of Pb was found to be higher
than the permissible limits of Indian standards. Levels of
Zn and Pb were found to exceed the tolerable levels. The
industrial wastes mostly from electroplating, lead acid
battery manufacturing, bulk drug formulations and pharmaceuticals contribute to much of the Pb and Zn contents.
These results have clearly indicated higher concentration of
metals in soils which is contributed by sewage and other
contaminated waters owing in the river. If the same trend

517

continues the concentrations of metals will soon exceed the

permissible limits.
Many researchers have used pollution index (PI) of soils
and sludges to identify element contamination resulting in
the increased overall element toxicity (Nistida et al., 1982;
Chon et al., 1997). Although equations for the calculation
of the PI differ among individual researchers, the basic
concept of the method is the same. In the present study the
PI of each metal was computed by the average ratio of the
metal concentration in the sample to the tolerable/
permissible levels of the soil for the plant growth suggested
by Kloke (1979). When the PI values exceed 0.50, the metal
is said to be contaminated by anthropogenic inputs and
may recommend continuous environmental monitoring of
the area (Sponza and Karaoglu, 2002). The PI values for
the six metals were evaluated and found to be 2.9, 1.2, 0.9,
0.7, 0.5 and 3.2 for Zn, Cr, Cu, Ni, Co and Pb, respectively.
3.1.1. Fractionation of soil
Any metal derived from anthropogenic source is strongly
inuenced by their form, phase and oxidation state and
hence bioavailability. Chemical soil tests are designed to
extract a quantity of element from the soil solids that
correlates statistically to the size of the available pool in
the soil dened by the quantity of element taken up by the
plants (Earnest, 1984). Chemical extraction techniques
provide a well-established means of identifying and

Table 1
Metal concentration in soils of the study area compared with permissible limits
Metal

Concentration from soils of Musi River

PI

Normal
rangesa

Background
valuesb

Tolerable
levelsc

Permissible
limits of Indian
Standardsd

Zn

Range (n 38)
Mean
Control (n 12)

227401
386
6.513

2.9

1100

60

300

300600

Cr

Range (n 36)
Mean
Control (n 12)

2638
33
2.78.5

1.2

0.0314

2.5

50

Cu

Range (n 40)
Mean
Control (n 12)

2135
32
1.85.7

0.9

520

30

100

135270

Ni

Range (n 36)
Mean
Control (n 12)

3363
55
0.92.3

0.7

0.025.2

20

60

75150

Co

Range (n 40)
Mean
Control (n 12)

1219
16
4.36.7

0.5

520

10

40

60110

Pb

Range (n 36)
Mean
Control (n 12)

303580
512
1123

3.2

515

25

100

250500

PI: pollution index.

a
Alloway (1990).
b
Venkateshwarulu and Sampath Kumar (1982), Syamala (1999), Buechler et al. (2002).
c
Kabata-Pendias and Pendias (1992).
d
Awasthi (2000).

NA

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characterizing different fractions of heavy metals in the soil

(Evans, 1989; Van Straalen and Denneman, 1989; Ure et
al., 1995). Results of the geochemical partitioning using a
modied Tessier scheme revealed high concentrations of
Zn, Cr, and Cu to be associated with the mobile fraction of
the soil. The sum of metal extracted in each sequential
extraction scheme was compared with the total digestion
procedure for the recovery studies.
Fig. 2 presents mean values (in %) of metals associated
with different fractions viz., readily soluble, exchangeable,
soluble in weak acid, FeMn oxides, organic bound and
residual mineral. Nearly 40% of Zn was associated with the
labile pool (soluble and exchangeable) which can be
attributed to CEC of the soils which is in concurrence
with earlier studies (Ramos et al., 1994). Chromium
followed the trend next to Zn and showed 3035% of
association with mobile fraction (soluble and exchangeable), further 1012% of Cr was also found to be bound to
organic fraction of soil. Only 10% Cr was associated with
acid soluble fraction, which may become available to plant
with change in pH and Eh of respective soils (Kimbrough
et al., 1999). Copper showed a similar tendency to that of
Cr owing to 2530% association with mobile pool. Ni and
Co showed similar results where major portion of these
metals were bound with non-mobile fractions (acid
soluble+organic bound+FeMn oxides+residual). These
two metals are reported to mobilize more in acid soluble
soils (Mc Bride, 1994). Because Pb binds strongly with
organic matter and chemisorbs on oxides of Fe, Mn, and
Al, it is a low mobility metal in soil. Studies have reported
that accumulation of Pb in plants occurs only with high
concentrations of lead in soils (Cambier, 1997). All the
samples along the Musi River showed 7077% lead
associated with non-mobile fractions due to the high
organic content of the soils. As the soil lead concentration

was very high, the nearby vegetation is prone to

accumulate lead. All metals have shown 1012% of
association with organic fraction which is due to long
term supply of sewage to the soils.
Relatively higher amounts of Zn, Cr and Cu were in
bioavailable pool observed in the present study which
attributes to the reduction in soil pH to moderately acidic
conditions as well increase in organic carbon due to the
continuous use of sewage efuents. This may be a cause of
prime concern in near future. Long-term application of
sewage will result in increase in organic carbon and
decrease in pH which might result in remobilization of
metal pool to more labile fractions. Based on the
fractionation studies the metals under study can be
arranged in decreasing order of bioavailability:
Zn4Cr4Cu4Ni4Co4Pb:
3.2. Vegetation
3.2.1. Forage grass
As forage grass is the predominant crop with 65% of
cultivation and also main fodder to majority of cattle this
was taken as representative specimen to assess the metal
transfer and plant uptake. Mean concentrations of metals
in forage grass (Kabata-Pendias and Pendias, 1992) with
normal ranges compared with control samples are presented in Table 2. These data are further assessed by
calculating the plant-to-soil ratios commonly known as
transfer coefcients, a convenient way of quantifying
relative differences in bioavailability of metals to plants.
Thornton and Farogo (1997) considered that plant/soil
ratios for any particular element of 0.1 indicate that the
plant is excluding the element from its tissues. Although
soil concentrations may be high and source metals may be

Fig. 2. Association of metals with different fractions of soils of study area.

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519

Table 2
Metal concentration in fodder grass (mg/g) and plant soil transfer coefcient values
Metal

Normal rangesa

General transfer
coefcient valuesb

Control values

Fodder grass values

from study area

Transfer coefcient
values from study area

Zn
Cr
Cu
Ni
Co
Pb

1100
0.0314
520
0.025
210
510

110
0.010.1
0.010.1
0.011.0
0.010.1
0.010.2

2.48.2
0.060.91
0.020.26
0.231.6
0.010.11
2.810.6

164.2212.4 (206)
20.236.7 (32)
15.729.6 (24)
10.718.3 (16)
3.77.1 (5.2)
66.7101.7 (93)

0.530.68
0.700.95
0.760.84
0.290.38
0.280.33
0.210.35

Kabata-Pendias and Pendias (1992).

Kloke et al. (1984), Alloway and Ayres (1993).

taken up in the roots, only a portion of the root uptake is

translocated to the leaves, giving a leaf/soil concentration
ratio of about 0.2. Based on this, we suggest that transfer
factors above 0.2 indicate anthropogenic contamination of
the plants. Kloke et al. (1984) gave a generalized transfer
coefcient for soils and plants based on the root uptake of
metals. However, soil pH, soil organic matter, CEC, and
plant genotype can markedly affect metal uptake. The
generalized coefcients were in concurrence with the
studies of Thornton and Farogo (1997) except for Cd
and Zn, which had maximum transfer factors of 10. This is
due to high mobility and phytoavailability of these two
metals, which is a reection of their relatively poor
sorption in soils. In contrast, metals such as Ni, Co, and
Pb have low transfer coefcients because they are strongly
bound, usually to the soil colloids. The results of our study
(Table 2) were in good agreement with the earlier two
hypotheses and that of our fractionation studies of soils
(Fig. 2), which clearly indicates high concentration of Zn,
Cu, and Cr in plants and high transfer coefcient values
compared to Ni, Co, and Pb. Table 2 also contains the
metal concentrations in control samples, which is generally
free from anthropogenic contamination.
3.2.2. Vegetables
Mean contents of six metals in vegetables along with
ranges and control values are summarized in Table 3. From
the values it is clear that concentration of Zn, Cr, Cu, and
Pb are high, making them a direct source of entry into
human. Table 3 also presents recommended maximum
levels by FAO/WHO and UK and EU standards (EC,
2001; DEFRA, 2002) which are compared with the metal
contents of vegetables from Musi. Concentration of Zn, Cr
and Pb were found to be higher than the recommended
limits. Leafy vegetables viz., spinach and amaranthus
accumulated much higher contents of Zn, Cr and Ni
compared to control samples, while overall increase was
observed in all vegetables for Cr and Pb. In general this
trend was in good correlation with the fractionation data
where mobile fractions of these metals were in higher ratio.
While accumulation of Pb may be attributed to the high
concentration of Pb in corresponding soils which lead to its
progressive accumulation. Concentration of metals was

found to be low in brinjal and ladies nger in contrast with

leafy vegetables. This is due to the fact that leafy vegetables
have high translocation rate and high transpiration rate
compared to other vegetables and also the transfer of
metals from root to stem and further to the fruit
(vegetable) is longer which results in low accumulation
than leafy vegetables (Itanna, 2002; Muchuweti et al.,
2006).
Further to understand the extent of risk and associated
hazard, enrichment factor (EF) was calculated using the
following equation. For calculating EF the data was
collected from the questionnaire where the approximate
intake of edible portion of the vegetable was determined
and used in the following equation:
enrichment factor EF
Conc: of metal in edible part grown on contaminated soil
Conc: of metal in contaminated soil
.

Conc: of metal in edible part grown on control soil

Conc: of metal in control soil

From the Table 3 it can be understood that Zn, Cr, and Pb

show relatively high EF in all vegetables compared to other
metals. Because pesticides are not in use and air pollution
in this area is minimum (Anjaneyulu, 2001; Buechler and
Devi, 2003), the concentration of metals in vegetables are
contributed generally from soils. The EF was reported very
high for Zn and Pb with special reference to leafy
vegetables (Spinach, Amaranthus).
3.3. Milk
Since forage grass is the dominated crop with approximately 60% of irrigation, samples of milk was collected
and analyzed and determined for metal content. Concentrations of metals in cows and buffalo milk in contrast
with control are presented in Fig. 3. The values clearly
indicate high content of Zn, Cr and Pb in milk samples.
Concentrations of metals were high in buffalo milk
compared to cow milk which may be ascribed to the high
fat content in buffalos milk (Indian Diary, 2004), which
helps in metal retention due to the formation of bioactive
(lipophilic) complexes (Leeuwen and Pinheiro, 2001;

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Table 3
Metal content in vegetables (mg Kg1) of the study area along with recommended levels
Vegetable

Zn

Cr

Cu

Ni

Co

Pb

Range
Mean
Control
EF

1.611.2
10
0.060.09
1.6

0.63.1
2.9
0.030.05
0.67

0.11.1
0.09
0.020.03
0.23

0.23.6
3.2
0.0010.02
0.14

0.060.17
0.13
BDL
0.06

1.33.6
3.1
0.050.09
0.99

Range
Mean
Control
EF

1.28.9
8
0.040.06
1.2

0.82.9
2.4
0.020.04
0.54

0.11.7
1.4
0.010.02
0.21

0.173.3
3.1
0.0020.01
0.1

0.030.11
0.09
BDL
0.04

1.13.1
2.9
0.040.09
1.1

Range
Mean
Control
EF

1.36.7
6.5
0.020.06
0.94

0.31.7
1.4
0.0040.02
0.61

0.21.3
1.1
0.0020.01
0.21

0.22.9
2.4
BDL
0.08

0.020.06
0.04
BDL
0.03

0.92.7
2.2
0.030.08
0.81

Range
Mean
Control
EF

1.15.8
5.4
0.030.06
0.71

0.22.4
2.1
0.020.04
0.55

0.31.6
1.2
0.0050.02
0.22

0.13.1
2.7
0.0020.005
0.1

0.010.04
0.03
BDL
0.02

0.63.4
2.7
0.020.05
0.69

Range
Mean
Control
EF

1.14.9
4.5
0.020.09
0.66

0.21.3
1.1
0.010.05
0.48

0.20.9
0.7
BDL
0.05

0.73.4
3.1
0.020.05
3.1

BDL
BDL
BDL
BDL

0.83.4
3.0
0.030.08
0.54

Range
Mean
Control
EF

1.33.7
3.7
0.050.1
0.81

0.11.7
1.4
0.0050.02
0.59

0.30.7
0.6
0.010.05
0.06

0.62.7
2.4
0.020.05
0.02

BDL
BDL
BDL
BDL

0.614.1
3.6
0.060.11
0.61

Background values from other

studies in Indiaa

3.84

0.74

0.61

1.71

0.11

1.89

Recommended Maximum levels

for vegetablesb

9.4

2.3

73.3

66.9

50

0.3

UK or EU limits

50

NA

20

NA

NA

1.0

Spinach
(n 46)

Amaranthus
(n 36)

Mint leaves
(n 40)

Coriander leaves
(n 38)

Brinjal
(n 33)

Ladies nger
(n 30)

BDL: Below detection limit.

a
Tripathi et al. (1997), Singh and Garg (2006).
b
Source: FAO/WHOCodex alimentarius commission (2001).

Fig. 3. Heavy metal distribution in milk samples.

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N. Sridhara Chary et al. / Ecotoxicology and Environmental Safety 69 (2008) 513524

521

Buechler et al., 2002). These concentrations of metals in

milk are clear reections of the fractionation data and
respective concentrations in forage grass.
3.4. Risk assessment
The DDI along with the recommended dietary allowances is presented in Table 4. The dietary intake of Zn, Ni
and Pb were found to be greater than the recommended
values. Also there was a substantial build-up of metals in
the soil of the study area which may become available to
the labile pool and further result in slow accumulation into
the plant and becomes a direct source of entry into human.
It was observed that females are more in number whose
dietary consumption of metals happens to be high. HQ, i.e.
ratio of determined dose of a pollutant to the dose level for
intake of these metals were worked out. The HQ for Zn
varied from 1.9 to 5.3, Cr 2.2 to 3.05, Pb 0.02 to 0.11 and
for Ni 0.002 to 0.013, Co and Cu showed negligible values.
Among the vegetables, leafy vegetables showed high HQ
with Spinach showing as high as 5.3 and Amaranthus 4.3
followed by mint leaves with a HQ of 3.5. Among the six
metals studied, Zn exhibited relatively higher HQ for all
vegetables in general and leafy vegetables in particular
compared to all other metals. Further Cr and Pb also
showed high HQ owing to their potential of risk concerned
to human consumption of vegetables. Hence, intake of
these contaminated vegetables is likely to induce health
hazard with special reference to Zn, Pb and Cr.
The participants had a variety of reactions indicating
possible health risks. Irritation of skin with black rashes
was among the commonest symptoms, which may be
attributed to exposure to Pb, Cr, and Zn (Abbasi et al.,
Table 4
Dietary intake in contrast with recommended dietary allowances
Metal

Zn (mg/
day)
Cu (mg/
day)
Cr (mg/
day)
Pb (mg/
day)
Co (mg/
day)
Ni (mg/
day)
a

Daily
dietary
index
(DDI)a

Average
daily
intake
through
foodb

% DDI

Recommended
dietary allowances
(RDA)c

Male

Female

11

8.47

7.2

911

68

1.12

5.4

750900

750900

0.6

0.33

6.1

2530

1520

0.4

0.61

6.7

1020

1015

1.2

0.72

4.3

24

23

1.3

0.81

5.1

0.71

0.61

From our questionnaire.

Tripathi et al. (1997), Singh and Garg (2006) (comparison with other
studies in India).
c
Food and Nutrition Board (2004).
b

Fig. 4. Concentration of metals in clinical samples (mg/ml).

1998; Syamala, 1999). Fig. 4 represents the concentration

of metals in clinical samples of which Pb, Zn, Cr, and Ni
were high in the blood and urine. The concentration of Zn
was relatively high in urine sample indicating the possible
elimination mechanism of this metal from the body.
Comparatively, all other metals reported low metal
concentration in urine owing to their high retention
capabilities in the body. Earlier studies on toxic metals in
farmers working on sludge farms (Srikanth et al., 1994)
indicated high concentrations of Pb, Zn, and Cr. The high
concentration of metals in blood and urine of the
participants compared to control individuals (Fig. 4) may
be attributed to the consumption of contaminated vegetables, milk, and other foods. Due to slow accumulation
rates of these metals in the human body, concentrations
were found to be higher in the age group of 3560. From
our survey and questionnaire it is evident that the
participants are exposed to higher-than expected and
acceptable concentration of metals (Syamala, 1999; Rattan
et al., 2005).
4. Discussion and conclusion
Heavy metals accumulation increases with time in the
soils when irrigation is carried out using wastewaters. In
this scenario the present article gains signicance indicating
the need for proper disposal of sewage and further
abatement of metal pollution and associated risk due to
the consumption of foods grown on sewage wastewaters.
There are few such studies conducted in India on the metal
contamination of soils resulting from sewage irrigation
(Agrawal, 1999; Singh et al., 2004; Rattan et al., 2005;
Sharma et al., 2007). Singh et al. (2004) conducted studies
to assess the impact of wastewater disposal from STPs in
Kanpur, Dinapur, Varanasi, on health, agriculture and
environmental quality. The study showed elevated concentrations of metals in all environmental media suggesting
a denite adverse impact on the environmental quality of
the disposal area. All these studies have clearly indicated

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N. Sridhara Chary et al. / Ecotoxicology and Environmental Safety 69 (2008) 513524

the distressing situation and warrant the need for controlling the metal pollution from sewage. The present study
envisages methodical evaluation and interpretation of
results pertaining to the metal pollution status of river
Musi and surrounding environs. From this study it can be
deduced that continuous usage of sewage and sewage
contaminated efuents will result in possible accumulation
of metals in receiving soils which further become potential
source of entry into human through food chain. This study
conrms the degraded quality of the Musi and surrounding
environs with reference to metal pollutants. Concentrations
of metals were found to be high in soils with special
reference to Pb and Zn contents, which were found to be
very high.
The fractionation studies of Musi soils clearly indicate
that Zn, Cr, and Cu are more mobile and in other ways
more phytoavailable, reected by high plant transfer
coefcients. Srikanth et al. (1992) conducted studies on
forage grass cultivated in sewage sludge along the banks of
the Musi River and reported accumulation of heavy metals
by the fodder grass. The same authors further reported
high concentrations of Pb, Cr, and Zn in various vegetables
grown on urban sewage sludge, indicating possible health
hazards for consumers (Srikanth and Raja Papi Reddy,
1991). There are reports elsewhere stating long term sewage
irrigation signicantly increased the mobile metal fraction
of all metals in general and Pb, Zn, Ni and Cd in particular
(Siebe, 1995). Agrawal (1999) observed that the plant
uptake and concentration of metal accumulation increased
with time attributed to the higher amount of mobile
fraction. These two hypotheses are in concurrence with the
amplied concentration of metals in vegetables and forage
of Musi River. The present study has clearly indicated high
concentrations of metals in vegetables grown on the banks
of the Musi River with leafy vegetables having high HQ,
which is in concurrence with the conclusions of Siebe and
Agrawal (Siebe, 1995; Agrawal, 1999). Many researchers
have experienced HQ as a reliable data for evaluation of
risk associated with the consumption of metal contaminated vegetables (Rupert et al., 2004; Rattan et al., 2005).
Kachenko and Singh (2004) studied the potential danger of
heavy metals accumulation at Boolaroo and Port Kembla,
Australian particularly Cd, Zn and Pb in vegetables grown
in the vicinity of smelters. Vegetables from Boolaroo
contained the highest levels of Cd (0.082.22 mg kg1 DW)
and Pb (0.6957.5 mg kg1 DW), and samples from Port
Kembla had the highest level of Cu and Zn in all vegetable
types. Concurrently, the risk associated was reported high
for metals having high mobility in relation with dietary
intake. The metals uptake of leafy vegetables is assigned to
large leaf area i.e., high transpiration rate and also fast
growth rate of these plants (Itanna, 2002).
Samples of milk collected from cattle fed on contaminated grass indicated high amounts of Zn, Pb, and Cr,
which is in agreement with studies conducted by Ayyadurai
et al. (1998). Studies on the biosorptive behaviour of metals
in milk revealed good uptake and followed rst order rate

law and obeyed Freundlich isotherm with poor desorption

response indicating high retention of metal concentrations
in milk (Mishra et al., 1998). Biomonitoring of metals in
the residents of the area were conducted by collecting
blood and urine samples. Human exposure pathways
revealed that concentrations of Zn, Pb, Cr, and Ni are in
higher concentrations than the permissible limits (Abbasi
et al., 1998; Iyengar, 1984) in the participants of the study
area. From this it is clear that the length of river Musi is
prone to anthropogenic contamination of metals and
requires continuous environmental monitoring.
For each of the metals there exist several exposure
pathways that depend on the particular contaminated
media of air, water, soil, and food and on the receptor
population (Caussy et al., 2003). Food is an important
pathway for several metals, particularly in populations
consuming regionally contaminated foods. This would be
true for people consuming vegetables or grains grown on
soils contaminated with metals. In general it is very difcult
to draw a correlation between metals contents of blood and
urine with age and number of people. Many factors such as
intake of metals-contaminated food (vegetables, milk),
health and nancial status of people, and nutritional
quality of food all play important roles.
Wastewater agriculture in area along the Musi River
provides livelihood to diverse group of people. The
agricultural and livestock activities based mainly on the
forage grass and vegetable market seems to be well suited
to the only type of water available (sewage water). The
results of the current study will be helpful for the local
pollution control authorities and policy-makers in managing the intrusion of industrial efuents into the Musi
River. Further, remedial measures may be taken to abate
the metal pollution and also restrict the cultivation of
vegetables on contaminated soils.
Acknowledgments
All the authors would like to thank the Council for
Scientic and Industrial Research (CSIR), Ministry of
Human Resources development, Government of India, for
providing research fellowship.
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