Science of the Total Environment 601–602 (2017) 1591–1605

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Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Soil contamination with cadmium, consequences and remediation using

organic amendments
Muhammad Amjad Khan a, Sardar Khan a,b,⁎, Anwarzeb Khan a, Mehboob Alam c
a
Department of Environmental Sciences, University of Peshawar, Peshawar 25120, Pakistan
b
Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China
c
Department of Horticulture, University of Agriculture, Peshawar, Pakistan

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Industrialization and urbanization

have caused Cd contamination of
soil/vegetable.
• Cd poses high threats to soil quality, food
safety, and even human health.
• Organic amendments are an environ-
mentally friendly and cost effective tech-
nique.
• Organic amendments improve soil quali-
ty and reduce Cd availability in soil solu-
tion.
• Organic matter makes complexes with
Cd and minimizes its subsequent bioac-
cumulation.

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

Article history: Cadmium (Cd) contamination of soil and food crops is a ubiquitous environmental problem that has resulted from
Received 23 January 2017 uncontrolled industrialization, unsustainable urbanization and intensive agricultural practices. Being a toxic ele-
Received in revised form 2 June 2017 ment, Cd poses high threats to soil quality, food safety, and human health. Land is the ultimate source of waste dis-
Accepted 4 June 2017
posal and utilization therefore, Cd released from different sources (natural and anthropogenic), eventually reaches
Available online 9 June 2017
soil, and then subsequently bio-accumulates in food crops. The stabilization of Cd in contaminated soil using organ-
Editor: D. Barcelo ic amendments is an environmentally friendly and cost effective technique used for remediation of moderate to
high contaminated soil. Globally, substantial amounts of organic waste are generated every day that can be used
Keywords: as a source of nutrients, and also as conditioners to improve soil quality. This review paper focuses on the sources,
Cadmium contamination generation, and use of different organic amendments to remediate Cd contaminated soil, discusses their effects on
Plants uptake soil physical and chemical properties, Cd bioavailability, plant uptake, and human health risk. Moreover, it also pro-
Organic amendments vides an update of the most relevant findings about the application of organic amendments to remediate Cd con-
Bioavailability taminated soil and associated mechanisms. Finally, future research needs and directions for the remediation of Cd
Remediation
contaminated soil using organic amendments are discussed.
Daily intake and health risk
© 2017 Elsevier B.V. All rights reserved.

⁎ Corresponding author at: Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China.
E-mail address: sardar.khan2008@yahoo.com (S. Khan).

http://dx.doi.org/10.1016/j.scitotenv.2017.06.030
0048-9697/© 2017 Elsevier B.V. All rights reserved.
1592 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1592
2. Cd sources and soil contamination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1592
3. Cd bioaccumulation and its effects on plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1593
4. Effects on nutrients uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1594
5. Effects of Cd on human health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1595
6. Remediation techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1596
7. Organic amendments and Cd remediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1596
8. Effects of organic amendments on Cd availability . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1597
9. Effects of organic amendments on Cd plant uptake . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1599
10. Negative effects of organics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1600
11. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1600
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1600
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1600

1. Introduction
Cadmium (Cd) is a highly carcinogenic metal that can cause toxic re-
actions even in low concentration (Benavides et al., 2005; Khan et al.,
2015). Cd is a non-essential trace element, and does not play any identi-
fied role in the growth and development of human, plants and animals.
Generally it occurs in lithosphere (0.2 mg kg−1), sedimentary rocks
(0.3 mg kg−1) and soil (0.53 mg kg−1) (Greenwood and Earnshaw,
1997; Kabata-Pendias and Pendias, 2001). Cd enrichment in soil occurs
from both natural and anthropogenic sources, and is considered to be
of great environmental concern (Pan et al., 2016). Geological weathering
is a major natural source of Cd in soil (Khan et al., 2010; Liu et al., 2013),
while mining, smelting, wastewater irrigation, industrial and vehicular
emissions, manufacturing, and agrochemicals are primary anthropogen-
ic sources of Cd (S. Khan et al., 2016; Nawab et al., 2016). Uncontrolled
and improper waste disposal practices have significantly increased the
concentrations of Cd in soil.
High Cd concentration can have toxic effects on soil organisms and
can easily transfer into vegetative cover and ultimately enter the food
chain (Li et al., 2016; Wahid et al., 2009). Cd is considered to be a primary
soil pollutant, and is considered a major issue regarding human health
after intake from contaminated rice caused Itai-Itai disease in Japan in
1970 (Kobayashi, 1978). There is no known metabolic function of Cd in
plants, but it is taken up and accumulated in their roots, shoots, and ed-
ible parts along with essential elements (Rascio and Navari-Izzo, 2011;
Zarcinas et al., 2004). The uptake of Cd by vegetables from soil is a
major exposure pathway for humans (Franz et al., 2008; Kobayashi et
al., 2008), and exposure through vegetables consumption accounts for
approximately 70–80% of total intake in humans (Olsson et al., 2002;
Yang et al., 2017; Wang et al., 2016). Elevated intake by humans through
contaminated food can cause severe damage to vital organs including
lungs and liver, and can cause cancer and other fatal health disorders
(Adriano, 2001; Moynihan et al., 2017; Järup et al., 1998). Keeping in
view the above adverse health impacts of Cd, it is necessary to ensure
that Cd concentrations in food crops meet the regulatory standards set
by different agencies such as World Health Organization (FAO/WHO,
2001) and United States Environmental Protection Agency (USEPA,
2005).
Several soil remediation techniques have been investigated in both
field and controlled environment experiments, such as soil washing,
phytoremediation, solidification, stabilization, excavation, and
electroremediation techniques (Kumpiene et al., 2008; Mulligan et al.,
2001). Among these techniques, in-situ stabilization of contaminants
using organic amendments exhibits great potential for cost-effective per-
formance. Large volumes of organic wastes are routinely produced from
livestock and poultry industries to meet human consumption demand.
These wastes must be treated to meet environmental regulations, in-
cluding safe disposal to land. These materials, along with other
agricultural and urban wastes, can be used as organic amendments for
the remediation of metal contaminated soil. They may provide the
large quantities needed to treat large expanses of agricultural lands, be-
cause these wastes are available in large volume and are typically inex-
pensive (Kumpiene et al., 2008; Cruz-Paredes et al., 2017; Lombi et al.,
2002). The remediation of Cd contaminated soil using organic amend-
ments depends on the availability and costs of organic amendments, as
well as their effectiveness. This review paper focuses on soil contamina-
tion with Cd, uptake by vegetables and associated health risks. Further-
more, this paper discusses questions regarding what type of organic
amendment is cost effective and has greater potential to remediate Cd-
contaminated soil.
2. Cd sources and soil contamination
Cd is released to the environment in variable amounts from natural
and anthropogenic activities. Volcanic eruptions, forest fires, wind-
blown dust, and sea spray are among the natural sources of Cd to the at-
mosphere. Weathering of parent rocks also contributes to the release of
Cd to the environment (Khan et al., 2010; Liu et al., 2013). Mafic and ul-
tramafic rocks contain high amounts of Cd, and thus upon weathering,
these rocks release significant quantities to soil (Shah et al., 2010).
Black shales contain Cd up to 100 mg kg−1, and the soil derived from
their deposits is enriched with Cd (He et al., 2005). Mean concentrations
of Cd in mudstone and siltstone was 4.6 mg kg−1, while in carbonate
rocks was 1.7 mg kg−1 collected from Three Gorges Region of Jianping
(Liu et al., 2013). Soil contamination with Cd released from natural
sources in different countries is shown in Fig. 1A. However, the total con-
tribution of natural sources towards Cd contamination in soil counted for
10% as compared to the total release from all sources. Over 90% (5.6–
38 × 106 kg year− 1) of Cd is released into the environment from anthro-
pogenic sources including the use of phosphate fertilizers, fossil fuel
combustion, metallurgical works, wastes from cement industry, sewage
sludge, municipal and industrial wastes, and mining, smelting and
metals ore processing (Nriagu and Pacyna, 1988; Bi et al., 2006;
Cloquet et al., 2006). It is also widely used in plastic stabilizers, pigments,
solar panels, batteries, and steel plating to resist corrosion. Other sources
of Cd may include polyvinyl chloride plastic manufacturing, alloys, fungi-
cides, solders, motor oil, and rubber and textile manufacturing
(Tamaddon and Hogland, 1993). Based on the findings of the British Geo-
logical Survey, the total worldwide production of Cd in 2015 was approx-
imately 24,900 metric tons (Brown et al., 2017). In 2016, the worldwide
production of Cd excluding US was 23,000 metric tons (U.S. Geological
Survey, 2017). Mining activities release Cd to soil from mining sites to
the nearby fields (Fig. 1B). Cd occurs in all types of Zinc (Zn) ores as a
guest element due to geochemical similarity. Thus, substantial amounts
of Cd are released to the environment during Zn smelting. In the produc-
tion of Zn, Cd rich dust is released in to the atmosphere, has a short
 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605 1593

Fig. 1. Cd concentrations in soils of different countries. (A) Natural/geoganic sources (sources: Liu et al. (2015); Nezhad et al. (2014); Muhammad et al. (2011); Quezada-Hinojosa et al.
(2015); Jacob et al. (2013); Garrett et al. (2008) and Pavlović et al. (2016)). (B) Mine impacted soils (sources Liao et al., 2016; Daldoul et al., 2015; Wilson and Pyatt, 2007; Lim et al., 2016;
Dayani and Mohammadi, 2010; Pourret et al., 2016). (C) Urban soils (sources Chabukdhara and Nema, 2013; Li et al., 2014; Acosta et al., 2011; Gunawardana et al., 2015; Parizanganeh et
al., 2010; Khan et al., 2011). (D) Irrigated by wastewater (sources: Elbana et al., 2013; Lucho-Constantino et al., 2005; Avci and Deveci, 2013; Mapanda et al., 2007; Surdyk et al., 2010;
Chavez et al., 2015; Tiwari et al., 2011; Mahmood and Malik, 2014; Wang et al., 2012).

residence time and is deposited locally (Bi et al., 2006; Hogervorst et al.,
2007; Roy and McDonald, 2015).
Urban soil is mainly polluted with Cd from industrial processes and
vehicular emission (Khan et al., 2016). A large amount (67%) is used in
the production of metallic Cd electroplate used in nickel-cadmium batte-
ries (Greenwood and Earnshaw, 2001). In China for the year 2009, the
total estimated emission of Cd was 743 metric tons of which 57% was
contributed by industrial processes (Cheng et al., 2014). The concentra-
tions of Cd in urban soils of different countries are shown in Fig. 1C.
Nriagu and Pacyna (1988) reported that the worldwide estimated total
input of Cd to soil through different anthropogenic sources was 5 to
38 × 106 kg year−1 with 12% from agriculture and animal wastes includ-
ing fertilizers. The contamination of agriculture soil with Cd from waste-
water irrigation also contributes to a larger extent (Fig. 1D). In China, Cd
enriched farmland area has reached 27.86 × 104 km2 (Cao et al., 1999).
Among different sources, the use of phosphate fertilizers is generally
considered to be one of the major sources of Cd input to agricultural
soil (Smolders and Mertens, 2013). Concentrations in phosphate fertil-
izers used in Europe were observed in the range of 0.1 to
120 mg Cd (kg P2O5)−1 (Nziguheba and Smolders, 2008). In addition,
the application of contaminated manure also adds Cd to agricultural
soil. According to Nicholson et al. (2003), the input of Cd to agricultural
soil from manure, when applied at a rate of N equivalent to 250 kg N ha−1-
year−1, ranged from 1.4 to 6.1 g Cd ha−1 year−1. Sewage sludge also
contains a considerable amount of Cd. Nicholson et al. (2003) reported
that if sludge containing 3.4 mg Cd kg−1 (dry basis (d.w.)) used at an
equivalent N rate of 250 kg N ha−1 it would add 19 g Cd ha−1 year−1.
The highest Cd concentration in soil (16.7 mg kg−1) is reported in
France, followed by (7.61 mg kg−1) Belgium and China (7.43 mg kg−1).
3. Cd bioaccumulation and its effects on plants
Uptake of Cd from soil by plants depends on its concentration and
bioavailability, while a small amount is directly taken up from atmo-
sphere through dry deposition of contaminated dust (Clemens, 2006).
The entry of heavy metals to plant cells occurs through the same trans-
port systems used for carrying out the uptake of macro and
micronutrients. The uptake of Cd occurs through trans-membrane car-
riers involved in the uptake of magnesium (Mg), calcium (Ca), iron
(Fe), zinc (Zn) and copper (Cu) (Clemens, 2006; Roth et al., 2006).
From contaminated soil Cd can easily be taken up by plant roots and
then transported to above ground parts where it interacts with biochem-
ical and physiological processes, affecting the plant morphology and
growth rate (Fig. 2) (Sanita di Toppi and Gabbrielli, 1999; Sgherri et al.,
2002; Uraguchi et al., 2009). The transfer of Cd to vegetables from Cd pol-
luted soil has been reported in several studies. However, less focus has
been given to the mechanisms involved in Cd bioaccumulation in differ-
ent plant species and soil environments, which led to a bias in data inter-
pretation. For example, most of the studies are focused on soil to plant
bioaccumulation of Cd, but no mechanisms were shown (Yang et al.,
2011; Jan et al., 2010). Similarly, the data measured is mostly based on
total Cd concentrations in soil rather than the bioavailable fraction,
which has led to uncertainty regarding the magnitude of Cd bioaccumu-
lation. The soil to plant transfer is generally measured as a ratio between
1594 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605
Fig. 2. Diagrammatical presentation of Cd sources, uptake by plants, effects on plant growth and human health and how organic amendments reduce Cd uptake by plants and improve
plant growth.
Cd concentrations in plant to Cd concentration in respective soil (Khan et
al., 2010) as explained in Eq. (1).
Cplant
PTF ¼
Csoil
where PTF is plant transfer factor, Cplant represents the Cd concentrations
in plants and Csoil represents the Cd concentrations in soil (Khan et al.,
2010).
The PTF values for Cd vary by plant species and depend on factors in-
cluding, soil pH, texture, structure, EC, organic matter, geology, and geo-
graphical features of the area, and soil amendments used (discussed
later). The PTF values calculated from various studies are presented in
Table. 1.
Generally, many plant species are tolerant to a certain amount of Cd,
but at certain concentrations can induce phytotoxicity. Concentrations of
Cd causing phytotoxicity vary greatly with plant species. Hyper accumu-
lators can accumulate above 0.01% of their shoot dry weight without
showing toxicity symptoms (Verbruggen et al., 2009). Cd concentrations
N5 to 10 μg Cd g−1 DM are toxic to most plants (White and Brown,
2010). Street et al. (2010) reported a decrease in leaf length and fresh
weight of leaves of wild garlic with the application of Cd. Cd decreases
the chlorophyll content and concentration of adenosine triphosphate
ATP (Hédiji et al., 2010). It inhibits the leaf photosynthesis by affecting
the biosynthesis of chlorophyll and the function of the centres of photo-
chemical reaction (Chugh and Sawhney, 1999; Jing et al., 2005). Cd sig-
nificantly reduced the dry weight of roots and shoots of wheat (Zhang
et al., 2002). Cd is highly cytotoxic and causes swelling and degeneration
of mitochondria, therefore, induces necrosis, chlorosis, vein reddening,
retards root and shoot growth and reduces nutrient uptake (Júnior et
al., 2014; A. Khan et al., 2016; Mohamed et al., 2012). Similarly, in bean
plants Cd induced curling of stems (Imai and Siegel, 1973). It has been re-
ported that Cd alters the physiological and metabolic process, and in-
hibits the growth of tomato plants (Chaffei et al., 2004; Lopez-Milla'n
et al., 2009). Belkhadi et al. (2010) reported that at cell level Cd enhanced
the production of reactive oxygen species, resulting in the damages of
membrane. Cd decreases the concentration of total soluble sugar and
increases the concentration of free amino acid in both roots and shoot
(Ci et al., 2009). Total soluble sugar has a vital role in carbohydrate me-
tabolism, photosynthesis, and production (Wilcox, 2001). Similarly the
contents of amino acid regulate several processes and metabolic path-
ð1Þ
ways of nitrogen (N) metabolism in plants (Causin, 1996).
4. Effects on nutrients uptake
Cd has significant negative impacts on plant nutritional values and
growth rate and most of the plants grown in Cd contaminated soil are
nutrient deficient (Khan et al., 2015). Yang et al. (1996) reported Cd ef-
fects on the uptake of various nutrients by plants. At the root region Cd
causes mineral deficiency by competing for absorption with minerals
having similar chemical properties like Ca and Mg (Barcelo and
Poschenrieder, 1990). High concentrations of Cd may cause the reduc-
tion of Ca, Mg, and K in the tissues of tomato (Khan et al., 2016) and cu-
cumber plants (Burzynski, 1988). Bioaccumulation of Cd causes the
alteration of various physiological functions by affecting N metabolism
(Chaffei et al., 2004). A significant decrease occurred in K and P concen-
trations in the edible parts of tomato and potato at different Cd applica-
tion dozes while the content of vitamin C were increased (Khan et al.,
2016b). Being an important part of genetic, structural and metabolic
components, N plays an important role in plants growth and metabolism
(Hasan et al., 2008). In tomato, a decrease in N contents (70, 9 and 34%)
was observed at different dozes (1.0, 2.5 and 5 mg kg−1) of Cd (Khan et
al., 2016b). In hydroponic conditions, a decrease in N content of soybean
was also reported under Cd stress, but the changes in N content were not
consistent with increasing Cd stress. Similarly, a decrease in P content of
soybean was also observed because of Cd contamination in soil (Dražić et
al., 2004). Cd has been shown to interfere with uptake of micronutrients
like Cu, Fe, Zn, and Mo in medium and small size plants such as wild gar-
lic (Street et al., 2010). In sunflower the uptake and translocation of es-
sential nutrients has been imbalanced by Cd causing depletion of P,
Mn, Fe, and Mg in their leaves (Júnior et al., 2014). Most of the literature
regarding the impacts of Cd on nutrients uptake by plants is based on ar-
tificial contamination of Cd at different application doses to plants either
in hydroponic condition or soil contamination, which may not be fully
 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605 1595

Table. 1 Satarug and Moore, 2004). Cd has adverse health effects on the
Cd concentration (mg kg−1) in soil and its bioaccumulation in vegetables and plant trans- human body where bone and kidney are the most important target or-
fer factor (PTF) values.
gans (Aitio and Tritscher, 2004). Cd gradually accumulates in the human
Cd in soil Plant species Cd in plant PTF References body and ultimately gives rise to various adverse health effects especial-
tissues ly causing bone damage and nephron-toxicity (Nordberg et al., 1991;
0.30 Potato 0.11 0.366 Piotrowska and Kabata-Pendias WHO, 1992).
(1997) About half of the total Cd entering the body is stored in the kidney,
7.61 Bean 0.24 0.031 Meers et al. (2005)
where it binds to metallothionein, a metal binding protein (Nordberg
7.43 Cucumber 0.66 0.088 Yu et al. (2006)
Spinach 1.06 0.142 and Nordberg, 2001). Greater renal accumulation is observed in females
Cabbage 0.71 0.095 than males because of higher adsorption rates (Satarug et al., 2002). The
0.14 Potato 0.7 5 Gichner et al. (2006) half-life of Cd in kidney is approximately 10 years. Renal and hepatic ac-
Potato 6.3 45 cumulation of Cd is due to the ability of this organ to produce metallo-
5.54 Lettuce 0.213 0.0384 Kachenko and Singh (2006)
Spinach 0.361 0.065
thionein that has high affinity for Cd (Klaassen et al., 1999). A study
0.80–2.58 Lettuce 0.40–0.91 0.5 Khan et al. (2008a) conducted in Belgium on people exposed to Cd showed 10% prevalence
0.84 Spinach 0.52 0.619 Khan et al. (2008b) of tubular proteinuria at 2 nmol Cd/mmol creatinine (Buchet et al.,
Lettuce 0.9 1.07 1990). Similarly in another study conducted on Cd exposed population
0.67 Spinach 0.20 0.29 Bigdeli and Seilsepour (2008)
50% prevalence of tubular proteinuria was observed in most exposed
Tomato 0.01 0.014
3 Lettuce 0.27 0.09 Zhuang et al. (2009) group (Järup et al., 2000). Chronic exposure to Cd causes progressive
Carrot 0.14 0.046 dysfunction of renal tubular. In the last stages of kidney damage by Cd
Mustard 0.08 0.026 exposure, wasting of Ca and Phosphate, glycosuria and altered Ca metab-
0.325 Rice 0.23 0.71 Kim et al. (2009) olism with associated effects of osteoporosis and osteomalacia were ob-
3.54 Lettuce 0.08 0.023 Mishra et al. (2009)
served. The excretion of stored Cd from the body occurs very slowly, for
Brinjal 0.15 0.042
Spinach 0.34 0.01 instance over decades. This very slow elimination of stored Cd results in
Radish 0.24 greater body burden perceived in advanced age (McElroy et al., 2007;
0.99 Mustard 0.62 0.63 Khan et al. (2010) Staessen et al., 1991). If renal tubular disease is present, the excretion
Lettuce 0.84 0.85
of Cd along with other compounds may increase, but Cd is nephrotoxic
Spinach 2.10 2.12
2.98 Mustard 0.28 0.094 Singh et al. (2010)
and can cause renal tubular damage and ultimate reduction in glomeru-
0.19 Rice 0.03 0.16 Liu et al. (2011) lar filtration rate (Roels et al., 1999).
0.9 Lettuce 4.22 4.69 Luo et al. (2011) Cd exposure also reduces bone density due to loss of Ca and phospho-
Rice 0.43 rous (P) (Järup et al., 2000). In the OSCAR study conducted in Sweden
Cauliflower 2.74
with 1021 people, a significant negative correlation was observed be-
16.7 Lettuce 14.98 0.897 Waterlot et al. (2013)
1.2 Lettuce 0.13 0.11 Xu et al. (2013) tween urinary Cd concentration and bone density. Both Cd and Ca are
Garlic 0.02 0.017 absorbed in the small intestine, here Cd directly disturbs the absorption
Cabbage 0.04 0.033 of Ca by competing with Ca+2 ions for bonding sites in the epithelium in-
1.7 Tomato 0.03 0.018 Hu et al. (2013)
testinal villi and indirectly it effects the Ca absorption by disturbing vita-
Lettuce 0.06 0.035
0.75 Potato 0.18 0.24 Gebrekidan et al. (2013)
min D3 metabolism (Brzóska et al., 1997). In cells Cd interferes with the
Tomato 0.38 metabolism of Ca, Fe, Mg, Cu, and Zn, it leads to demineralization, osteo-
0.098 Pumpkin 0.09 0.92 Khan et al. (2013) porosis, osteomalacia, and bone disorders. Cd competitively displaces Ca
Potato 0.09 0.92 ions from the bones, which leads to their weakness and ultimately causes
Tomato 0.09 0.92
fracture, especially in children and women (Elinder et al., 1977; Sarkar et
Broad Bean 0.10 1.02
Bitter gourd 0.09 0.92 al., 2013). Chronic Cd toxicity causes glucose metabolism disorders
Lady finger 0.09 0.92 (Zhang et al., 2014). It is reported that Cd exposure is associated to a va-
Onion 0.09 0.92 riety of clinical conditions including cardiac failure, cancers, anosmia, ce-
0.17 Lettuce 0.049 0.29 Chang et al. (2014)
rebrovascular infarction, osteoporosis, emphysema, and proteinuria
Chinese cabbage 0.027 0.16
0.52–4.5 Lettuce 0.18 0.346 Augustsson et al. (2015)
(Nishijo et al., 1995); and eyes cataract formation (Ramakrishnan et al.,
Potato 0.031 0.0596 1995).
7.1 Chinese cabbage 3.57 0.502 Liu et al. (2015) Cd has been classified as a human carcinogen by the International
Pachyrhizus 0.08 0.011 Agency for Research on Cancer (IARC) (IARC, 2012) and causes the de-
Green cabbage 1.12 0.16
velopment of breast cancer in exposed females (Järup and Åkesson,
Chili 0.37 0.052
Radish 0.89 0.125 2009). High level of exposure to Cd influences testosterone and sex-hor-
Bean 0.62 0.087 mone binding globulin level, and finally, affects the sex hormones
Potato 0.16 0.022 (Kresovich et al., 2015). Exposure to Cd also disrupts the function of en-
Maize 0.02 0.002 docrine (Takiguchi and Yoshihara, 2005). Children are more susceptible
Rice 0.04 0.006
to Cd toxicity than adults and even low level of exposure to Cd can cause
adverse health effects (ATSDR, 2012).
representative of field conditions (Khan et al., 2016; Dražić et al., 2004). Consumption of Cd-contaminated vegetables is one of the main
Therefore more extensive and long term field studies need to be con- sources of Cd intake by non-occupationally exposed people. Vegetables
ducted to evaluate these effects under natural environmental conditions grown in Cd-contaminated soils have the potential to cause toxicologi-
to give a more realistic view about the findings. cal problems in humans especially women and children (Roy and
McDonald, 2015). About 95% of Cd is taken up with food and drink. Sev-
5. Effects of Cd on human health eral other factors like low intake of Ca, vitamin D, and trace elements
such as Cu and Zn can increase this amount (Schwarz, 1993). Cd is vir-
Cd toxicity to human health remains a global environmental and tually present in all foods, but the concentrations vary to a great extent
human health concern. Research has been conducted on the adverse ef- depending on the type of food. Thus, there are great variations in daily
fects of Cd on human health (Chen et al., 2008; Friberg et al., 1985; intake of Cd due to variation in concentration of Cd in foods and individ-
Haswell-Elkins et al., 2008; Inaba et al., 2005; Ning et al., 2006; ual dietary habits.
1596 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605

The average daily intake of Cd (DICd) is generally calculated using the
following formula:
CCd  Cfactor  Dfood intake
DICd ¼
BWaverage weight
where the DICd is the daily intake of Cd, CCd, Cfactor, Dfood intake and
BWaverage weight are Cd concentrations in vegetables, conversion factor
(fresh weight to dry weight), daily vegetables intake and the average
body weight, respectively. For adults the average daily intake of vegeta-
bles is 0.345 kg per person, while for children it is 0.232 kg per person
(FAO, 2000). The average body weight for adults is 73 kg (FAO, 2000)
and for children is 32.7 kg (Wang et al., 2005). The values of DICd report-
ed in different countries through consumption of Cd contaminated veg-
etables are presented in Table 2. From the available data it is clear that
the population of Netherlands ingests the highest Cd through contami-
nated vegetables, followed by France, and that the lowest ingestion is ob-
served for the people in USA.
Data presented reveals that the consumption of Cd contaminated
foods is an important pathway for exposure. Therefore, the consumption
of contaminated vegetables should be minimized to the greatest extent
possible to reduce adverse health effects. Similarly, different remediation
measures should be introduced to contaminated soil to bring the Cd con-
centration to the safe limit. Moreover, the values of DICd are based on
few studies from around the world. Additional studies are needed to
more fully characterize the occurrences and potential risks. Furthermore,
daily vegetable consumption, food habits, general nutritional status, and
average body weight of individual should be taken into account. The
daily dietary intake of Cd may not be exactly reflected from the few
field studies as the vegetables may be grown in one part of a country
and use in some other parts of the country or another country. Based
on these findings it is important to do market based studies along with
field and controlled environment experiments to clearly illustrate the
possible health effects of Cd to a particular group of population.
6. Remediation techniques
Remediation of Cd-contaminated soil depends on bioavailable frac-
tion of Cd in the soil. A number of remediation techniques have been
used for metal contaminated soil. These techniques include excavation,
soil washing, in-situ chemical stabilization, phytoremediation, and in-
situ physical stabilization.
In-situ physical stabilization is a method based on the application of
amendments to soil to stabilize contaminants and reduce their bioavail-
ability. Several types of amendments are used to remediate metal (Cd)
polluted soils. This technique minimizes the risk of food chain contam-
ination by reducing metal uptake by food plants and offsite
contamination through erosion and leaching. In soil environment,
metals form soluble or insoluble complexes with organic amendments.
Organic biomass is produced in large quantities, and has low economic
cost so use as soil conditioner, source of nutrients, and as soil Cd
ð2Þ
remediating agent could be a cost-effective way to integrate organic
waste management and disposal with soil remediation.
7. Organic amendments and Cd remediation
The use of organic wastes as a beneficial soil amendment for agricul-
ture has been in practice for several decades (Sims and Pierzynski, 2000).
The most commonly used organic wastes include animal manure, biosol-
id, municipal solid waste composts, crop residues, blood and bone meal,
sea weeds and humic substances (Beesley et al., 2014; Burton and
Turner, 2003; Khan et al., 2014, 2015). The commonly produced organic
wastes include animal manure, biosolid, plant residue, and municipal
solid waste. Animal manure is considered as a major source of organic
amendments (Burton and Turner, 2003). The major sources from
which manure are derived are poultry, pig, sheep, and cattle farms. The
increasing demand of food for the human population, increase in average
household income and changes in life style and dietary habits have re-
sulted in intense animal production. This increase in animal production
to meet the needs of human demands for food has led to various envi-
ronmental issues. Globally, approximately 7 × 109 Mg year−1 animal
manure is produced. The production of animal manure per year in differ-
ent countries is given in Fig. 3. Biosolid is another major organic waste
produced worldwide. Biosolids are obtained as the residue of treated
wastewater from municipal wastewater treatment plants. Globally, sub-
stantial quantities of biosolid (approximately10 × 107 Mg year−1) are
produced each year. The estimated annual biosolid production of differ-
ent countries is presented in Fig. 3. It has been reported that in US
6.5 million tons of biosolids were generated in 2004, out of which
4 million tons (60%) were applied to land (NEBRA, 2007). In Europe,
10 million tons of biosolids are produced year−1, out of the total pro-
duced biosolids 36% is used in agriculture (Gendebien et al., 2008). In
the USA, 7.2 million tons of biosolids are generated each year, out of
which approximately 49% are used in agriculture sector (NEBRA, 2007).
During agricultural and horticulture practices a large amount of plant
residues are generated as waste. It is reported that globally 3.8 × 10-
9
Mg year−1 plant residues are produced, of which 74, 8, 3, 10 and 5%
consist of cereals, legumes, oil crops, sugar crops and tubers, respectively
(Lal, 2005). In New Zealand 1360 × 103 Mg year−1 plants residues are
produced (Thangarajan et al., 2013). In China each year N 600 million tons
of rice straw is produced (Yang and Sheng, 2003; Zhong et al., 2003). In
the year 2005, China produced approximately 84,183.12 × 104 tons of
straw resources (Wang et al., 2010) and in 2010, 729 million tons crop
residues were produced (Qiu et al., 2014). In 2010, crop residue

Table. 2
Daily dietary intake of Cd (mg kg−1 day−1) through consumption of Cd contaminated vegetables.

Country Adults N 19 Children Adolescent 14–18 years References

MAL/RDAa 5.0E−02b EC (2006)

RfD (oral reference dose) 1.0E−03 1.0E−03 USEPA (2012)
Netherland 2.01E−02 4.10E−02 1.60E−02 Swartjes et al. (2013)
USA 1.08E−05 2.21E−05 8.63E−06 McBride et al. (2014)
Bangladesh 5.17E−05 1.06E−04 4.13E−05 Rahman et al. (2013)
Italy 1.54E−05 to 5.48E−05 3.16E−05 to 1.12E−04 1.23E−05 to 4.38E−05 Beccaloni et al. (2013); Ferri et al. (2015)
Ethiopia 1.16E−04 2.37E−04 9.24E−05 Gebrekidan et al. (2013)
Zimbabwe 8.87E−04 1.81E−03 7.09E−04 Mapanda et al. (2007)
China 2.05E−04 to 2.805E−03 4.18E−04 to 5.72E−03 1.63E−04 to 2.23E−03 Khan et al. (2008b); Liao et al. (2016);
Li et al. (2015); Liu et al. (2015); Luo et al. (2011)
Sweden 6.95E−05 1.42E−04 5.55E−05 Augustsson et al. (2015)
Uganda 8.22E−05 1.68E−04 6.56E−05 Nabulo et al. (2010)
India 8.03E−04 to 4.92E−03 1.64E−03 to 1.00E−02 6.41E−04 to 3.93E−03 Gupta et al. (2012); Sharma et al. (2008)
Pakistan 3.67E−05 to 8.10E−04 7.49E−05 to 1.66E−03 2.93E−05to 6.47E−04 Khan et al. (2013); Khan et al. (2010)
France 5.78E−03 1.18E−02 4.62E−03 Waterlot et al. (2013)
a
MAL/RDA maximum allowable limit/recommended dietary allowance.
b
E−02 represents 1 × 10−2.
 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605 1597

Fig. 3. Quantity (1 × 106 Mg year−1) of organic production per year in different countries.
Sources CH2MHill (2000); Déportes et al. (1995); Epstein (2003); Grodzińska-Jurczak (2001); Logan (1995); Pappu et al. (2007);
Thangarajan et al. (2013); Yang et al. (2003).

production estimated in Africa were 23,082 × 104, while in America, Asia
and Europe these values were 99,604 × 104, 190,851 × 104 and
62,084 × 104 tons, respectively (Gupta and Verma, 2015). In Europe,
the wine sector produced 4 million tons solid waste per year including
seeds, skins and stalk of grapes (Grub's Up, 2009). In the year 2010, the
worldwide estimated production of rice husk was 1.40 × 108 tons
while in 2014 it was 1.482 × 108 tons. Similarly, in China the production
of rice husk in 2014 was 0.412 × 108 tons, India 0.309 × 108 tons, Bangla-
desh 14,166,400 tons, USA 2,005,200 tons and Pakistan 2,015,000 tons
(FAO, 2013; IRRI, 2014). Different types and large amount of organic
wastes are produced at municipalities which can be applied as soil
amendments for the reclamation of degraded soil (Kashmanian et al.,
2000). Municipalities produce two major types of organic wastes includ-
ing biosolids (sewage sludge) and municipal solid wastes. Municipal
solid wastes including garden wastes, food scraps, and other miscella-
neous products (Hargreaves et al., 2008). Municipal solid waste produc-
tion of different countries is given in Fig. 3.
8. Effects of organic amendments on Cd availability
Bioavailability is a major factor governing Cd toxicity in soil. Bioavail-
able Cd is the fraction of total Cd in the interstitial water and soil particles
that is readily available to the receptor organisms. Organic matter
amendment significantly affects Cd availability in soil by bringing chang-
es in soil physico-chemical properties like pH, EC, and macro and micro
nutrients concentration (Khan et al., 2014). Organic matter plays a vital
role regarding bioavailability of trace metals in soil (Van Gestel, 1992).
The amendment of trace metals polluted soil with organic matter is con-
sidered as an environmentally friendly option to immobilize trace metals
in soil and reduce uptake by plants (Table. 3). Organic amendments due
to high amount of humidified organic matter minimize the bioavailabil-
ity of metals by adsorption or by making stable complexes with humic
substances (Shuman, 1999).
Addition of organic amendments to soil enhances immobilization of
Cd through adsorption reactions (Fig. 4). Organic amendments increase
the retention of Cd by increasing surface charge (Clark et al., 2007). Cd
concentration in soil is not decreased by the use of organic amend-
ments, but reduces its bioavailability. Organic minerals, aluminium
compounds, and phosphates, present in organic amendments, retain
heavy metals (Brown et al., 1998). Organic matter in soil converts the
soluble/exchangeable Cd into organic bond fraction thus reducing up-
take (Han-Song et al., 2010; Liu et al., 2009). Concentrations of water
soluble Cd decrease with the increase in organic content of soil, because
increasing the content of soil organic matter increases the availability of
binding sites in soil (Beesley et al., 2014; Crommentuijn et al., 1997).
In addition, dissolved organic matter interacts with soil toxic metals
forming soluble organic complexes (Wong et al., 2007) this can increase
availability. Dissolved organic matter having low molecular weight has a
strong influence on the migration and mobility of Cd in soil (Mahara et
al., 2007). Natural organic molecules, instead of high cost synthetic che-
lating agents, can be used as organic amendment. Dissolved organic mat-
ter of soil and organic matrices like manure, compost, and sewage sludge
contain natural ligands (Antoniadis and Alloway, 2002). Natural ligands
are organic molecules that bind to metals (Hamon et al., 1995). Ligands
and functional groups present in organic amendments have high affinity
for Cd ions. The use of organic amendments in Cd polluted soil control
the soil to plant transfer of Cd by increasing the soil pH. As the pH of
soil increases, Cd concentrations in soil solution decrease, and the accu-
mulation of Cd by plants also decreases (Chaudri et al., 2007; K. Liu et
al., 2015). Increase in soil pH enhances H+ dissociation from functional
groups such as hydroxyl, phenolic, carbonyl, and carboxyl thereby en-
hancing the affinity for Cd ions (Bolan et al., 2003). It is evident from
the Table 4 data that the soil pH increases with increasing of organic mat-
ter in soil and limits Cd uptake by plants. Similarly, pH affects the solubil-
ity and distribution of Cd between soil and solution phase (Eriksson,
1990; Naidu et al., 1994). Decrease in Cd availability in soil, after applica-
tion of different organic amendments, has been linked with changes in
1598 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605

Table. 3
Organic amendments effects on Cd fractions, uptake and plants growth.

Amendments Parameters Decrease in Cd (%) Plant parameters Increase References

Green waste compost Leaching 48 – Van Herwijnen et al. (2007)

Pig manure Rice grain 42–46 Straw yield 235–313% Ping et al. (2008)
Rice straw 70–77 Grain yield 1128–1531%
Root biomass 275–316%
Peat Rice grain 41–44 Straw yield 112–214%
Rice straw 73–79 Grain yield 135–396%
Root biomass 126–227%
Compost Exchangeable 70 – Liu et al. (2009)
Poultry manure Compost Soluble/Exchangeable 48–70 – Han-Song et al. (2010)
Pakchoi 56–63
Cattle compost Spinach 34 Yield (Mg ha−1) 804% Sato et al. (2010)
Swine compost 38 Yield (Mg ha−1) 771%
Poultry compost 37 Yield (Mg ha−1) 775%
Rapeseed residue Rice leaves 20 – Ok et al. (2011)
Rice stem 18
Rice hulls 34
Available fraction 5–14
Swine manure Sunflower roots 71 – Xiu-Zhen et al. (2012)
Stem 23
Leaves 45
Flower 52
Compost Rice roots 20–48 Roots dry weight 32% Juang et al. (2012)
Shoot 43 Shoot dry weight 37%
Cattle manure Shoot 6–33 – Wang et al. (2012)
Roots 41–67
Cow manure Tobacco plant (field experiment) 67 – Nyambaka et al. (2014)
Tobacco plant (pot experiment) 72
Farmyard manure Amaranthus caudatus 23 Fresh weight plant−1
20.5 g Singh and Prasad (2014)
Saw dust 45 16.9 g
Rice husk 36 15.5 g

concentration of dissolved organic carbon and pH (Kołodyńska et al.,
2012; Zheng et al., 2012).
The effect of organic matter amendments on Cd mobility and bio-
availability are influenced by soil type. Soil physico-chemical properties
play a major role in the availability of Cd. Generally available fraction of
Cd in soil decreases with increase in organic matter and clay contents
in soil. Compost application to alfisol transformed 48 to 70% of soluble/
exchangeable Cd to the organic bond Cd (Han-Song et al., 2010). Similar-
ly in a fine clay loam soil compost application decreased exchangeable
Fig. 4. The possible mechanisms of organic matter affecting Cd in soil.
Modified from Ahmad et al. (2014).
Cd by 70% (Liu et al., 2009). In paddy soil, the addition of sewage sludge
biochar significantly reduced (from 3.53 to 3.02 mg kg−1) bioavailable
concentration of Cd and other heavy metals (Khan et al., 2014). A field
study revealed that the addition of compost to acidic loam soil did not af-
fect the soil Cd level (Zhang et al., 2006), while Pinamonti et al. (1999)
found that the application of compost amendment to neutral sandy soil
significantly increased soil Cd level.
Pardo et al. (2014) studied the effects of pig slurry and compost com-
bined with hydrated lime in acidic soil contaminated with heavy metals
from mining activities. The addition of pig slurry and compost with lime
significantly reduced the mobility of trace elements in the top soil. Con-
centrations of Cd were significantly reduced in the soil pores in the top
5 cm layer and moderately in the intermediate 12 cm layer. Despite
the success reported by researchers the potential of organic amendments
for long term remediation of Cd contaminated soil is still questionable.
The potential for loading Cd in soil after organic amendments application
depends on the source of organic amendments and concentration of Cd
in the organic amendments.
Compost generally contains high concentration of heavy metals so
there is a possible risk of metals accumulation in soil with repeated use
of compost (Zhang et al., 2006). High concentration of Cd in sewage sludge
may account for the non-suitability of sewage sludge as soil amendment
for remediation of Cd polluted soil (Singh and Pandeya, 1998). Therefore
prior to application, organic amendments and agriculture soil should be
evaluated for total Cd concentration and bioavailable Cd fractions.
There is a need for research regarding the use of organic amendments
for remediation purposes. In this area, research should also consider and
account for the effects of organics on soil physicochemical properties
while applying to different soil types and also account for the effects of
these organics on available and total Cd concentration in a variety of
soils. Organic amendments after application to the soil eventually de-
compose and release the bounded metals. In spite of the fact that a frac-
tion of organics is considered to be resistant to decomposition, still there
is a risk of remobilization of bounded metals. Many researchers agree
that in organic amendments, the presence of inorganic residues like
 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605
Table. 4
The effects of organic amendments on soil pH changes.
Types of organic amendments
Municipal refuse compost
Municipal solid waste compost
Municipal solid waste compost
Source-separated municipal solid waste (SSMSW)
Municipal solid waste compost
Ruminant compost
Biosolids/municipal solid waste compost
Chicken manure
Green waste compost, hard wood derived Biochar and both combined
Farmyard manure
Miscanthus straw biochar
Mixture of sludge and sewage sludge
Sheep horse manure
Wood derived Biochar (pyrolysed at 450 °C, 48 h)
Straw manure and pig manure
silicates, phosphate, and Mn, Al, and Fe oxides are responsible for long
term retention of metals (Brown et al., 1998; McBride, 1995). However,
although there may be an immediate immobilization impact this may
not be true into the future.
9. Effects of organic amendments on Cd plant uptake
Addition of organic matter to soil improves its chemical, physical and
biological qualities by increasing the contents of organic matter, chang-
ing its pH, providing essential nutrients, improving the water holding ca-
pacity, and altering the bioavailability of heavy metals. Soil pH is the
most influential factor affecting the Cd uptake by plants grown on Cd
contaminated soil (Eriksson, 1990; K. Liu et al., 2015: Naidu et al.,
1994). It has been reported by a number of studies that the organic
amendments increase the soil pH (Table. 4). The possible reasons for
this increase of pH may be due to mineralization of carbon, OH−1 ions
production by ligands exchange and the release of basic cations such as
Ca2+, K+, and Mg2+ (Mkhabela and Warman, 2005). It has been ob-
served that lettuce (Lactuca sativa) and Swiss chard (Beta vulgaris) up-
take higher Cd grown on acidic soil (pH 4.8 to 5.7) than calcareous soil
(pH 7.4 to 7.8) (Mahler et al., 1978).
The application of organic amendments to Cd contaminated soil
changes the soil physico-chemical properties which in turn affect the
phyto-availability of Cd. Changes in physico-chemical properties of soil
and availability of Cd depend on the quality and quantity of organic
amendments (Table. 3). Plants grown in soil with low organic matter
have higher uptake of potentially toxic elements than those cultivated
in soil with high organic matter (Oudeh et al., 2002). Decrease in Cd up-
take by plants with the application of organic amendments has been re-
ported by a number of researchers (Table 3). A significant decrease (77%)
in rice uptake of Cd associated with pig manure addition was reported by
Ping et al. (2008). Similarly 38% decrease in Cd uptake was observed with
compost amendment in spinach (Sato et al., 2010). Application of chick-
en manure compost resulted in a decrease of N 50% in Cd uptake by
wheat (Liu et al., 2009). A list of effectiveness of organic amendments
in reducing Cd uptake by different plants is given in Table 3. The Cd in
soil forms chelates with organic matter reducing its phytoavailability
(Singh and Prasad, 2014). Reactive groups of organic matter, such as
phenoxyl, carboxyl and hydroxyl react with Cd forming stable complexes
(Mahmood, 2010). Organic amendments decrease Cd bioavailability by
altering the pore water concentration and the metals blocking capacity
of iron oxides (Zheng et al., 2012). Cattle manure compost has high affin-
ity for Cd, therefore could be a best remedy for Cd contaminated soil
(Sato et al., 2010). In general, we assume that organic amendments de-
crease Cd bioavailability and plant transfer, however, this is not true in
all cases, as different soil types respond differently.
1599
pH increases References
6.1 to 7.6 Hernando et al. (1989)
5.8 to 6.4 Maynard (1995)
5.6 to 6.1 Bhattacharyya et al. (2003).
5.3 to 6.6 and 6.0 to 6.6 Zheljazkov and Warman (2004)
5.9 to 6.3, and 5.4 to 5.8 Mkhabela and Warman (2005)
4.9 to 5.8 and 5.1 to 5.9 Shanmugam (2005)
5.8 to 6.7 and 6.1 to 6.5 Zhang et al. (2006)
5.6 to 6.2 Clark et al. (2007)
5.45 to 6.19, 5.45 to 7.56 and 5.45 to 7.88 Beesley et al. (2010)
6.93 to 7.19 Singh et al. (2010)
5.62 to 5.65, 5.62 to 6.21 and 5.62 to 6.70 Houben et al. (2013)
2.56 to 3.63 and 2.56 to 3.16 Forján et al. (2014)
6.2 to 6.5 and 6.2 to 6.8, 5.5 to 5.8 and 5.5 to 6.1 Pérez-Esteban et al. (2014)
6.8 to 7.55 Lucchini et al. (2014)
4.62 to 5.5 and 4.62 to 5.4 Tang et al. (2015)
The literature related to the effectiveness of organic amendments for
the remediation of Cd contaminated soil and reducing Cd uptake by
plants is controversial. Pinto et al. (2004) reported an increase in trans-
location of Cd from root to shoot of sorghum with the application of or-
ganic matter. Similarly in another study, a 3-fold increase in sorghum
shoot Cd concentration was observed with organic matter application
(Pinto et al., 2005). In acidic paddy soil, application of organic amend-
ments may increase Cd uptake by plants (S. Khan et al., 2013), while
in neutral pH soil the available concentration of Cd may significantly
be reduced (S. Khan et al., 2015).
Although, many researchers have reported on the successful use of
organic wastes for the immobilization of Cd, for long term immobiliza-
tion of Cd the role of organic wastes is still not clear and often
questioned. The problem associated with the application of organic
amendments is Cd leaching. Application of organic amendments to Cd
polluted soil has shown to increase Cd leaching compared to non-
amended soil (Schwab et al., 2007). Similarly, nutrients leaching losses
from soil with organic amendments is another issue. A number of stud-
ies have shown that organic amendments reduce the uptake of Cd by
plants, but leaching of metals and nutrients is an issue related to organic
amendment application. An increase in leaching of metals from contam-
inated soil with organic amendments is often observed in short term
(Schwab et al., 2007). In fact, the decomposition of organic matter in
biosolid takes place over a long period of time and only limited amount
of Cd is supposed to be released (Brown et al., 1998). The enhanced af-
finity of the inorganic components of biosolid for Cd adsorption indi-
cates that biosolid induced Cd adsorption is of a persistent nature (Li
et al., 2001). However, in the long term remediation of Cd contaminated
soil using organic amendments may facilitate release, because organic
amendments will mineralize/decompose and Cd will be remobilized
and may become available to plants.
Moreover, the application of organic amendments make the Cd less
mobile, but the total concentration still remains the same and may be
increased if the organic amendments contain Cd. Jinadasa et al. (1997)
reported an increase in Cd concentration in soil and vegetables due to
long term applications of poultry manure. Most of the Cd ingested by
the animals with the ingestion of soil during grazing and with ingestion
of contaminated plants is excreted in the manure (Lee et al., 1996;
Loganathan et al., 1999). Similarly biosolids have also been regarded
as a source of Cd contamination to soil. The repeated application of bio-
solid has considerably increased the Cd concentration in soil as a result
of large amount of available Cd (Illera et al., 2000). The most important
problem in the use of organic amendments for Cd contaminated soil re-
mediation is the availability of Cd free organic amendments, although if
the organic amendments having Cd with in the regulation standards are
used for a long time there is a risk of increasing accumulation of Cd in
soil.
1600 M.A. Khan et al. / Science of the Total Environment 601–602 (2017) 1591–1605
10. Negative effects of organics
Excessive use of organic wastes like composts, sewage sludge and an-
imal manure etc. can result in a source of water pollution by contributing
excess N and P to the soil (Bernal et al., 2007). Animal manure may con-
tain antibiotics which are added to their feed to improve growth and
control diseases (Kumar et al., 2005). Organic wastes may also contain
considerable amount of Cd. The concentration of Cd in animal manure
collected from ten provinces of China ranged from 0 to 10 mg kg−1,
showing a significant increase from 1990 to 2010 (Wang et al., 2014).
Similarly, Cd at variable concentrations in farm yard manure (0.13 to
0.38 mg kg−1), dairy cattle manure (0.87 mg kg−1), pig manure
(59.66 mg kg−1) and sewage sludge (7.3 mg kg−1) were also reported
(Bolan et al., 2004; Nicholson et al., 1999; Henry and Harrison, 1992;
Zhang et al., 2005). The applications of biosolid compost have substantial
contribution to soil Cd concentration (McLaughlin et al., 1996). The con-
centrations of Cd in sludge and composts range from 0 to 16 mg kg−1,
depending on the source and technology used to produce organic
amendments (Alloway, 2013; Kabata-Pendias, 2011; Smith, 2009). In a
three year experiment, the application of green waste compost increased
the concentration of available Cd by 24% as compared to control, while
poultry manure compost increased its total concentration by 76%
(Hanč et al., 2008). A higher proportion of exchangeable and soluble Cd
concentrations in soil were also observed 23 years after termination of
sewage sludge application (McGrath et al., 2000). Walter and Cuevas
(1999) found N55% of total Cd in EDTA extractable form after 5 years of
sludge application. Carbonell et al. (2011) reported that the application
of municipal solid waste increased the concentrations of Cu, Pb, and Zn
in soil.
Moreover, organic amendments having high proportion of fulvic
acids and high concentrations of soluble organic carbon increase the mo-
bility of metals by forming soluble metal-organic complexes (Ashworth
and Alloway, 2008), enhancing their uptake by plants (Bolan et al.,
2003) and leaching to the groundwater (Clemente et al., 2006; Schwab
et al., 2007). In spite of various benefits associated with the utilization
of organic wastes in agriculture may result in adverse environmental im-
pacts such as pollutants loading, metal, and nutrients leaching. Their use
may pose risk of being contaminated with various types of toxic ele-
ments that may ultimately enter the food chain, as they may be readily
taken up by the plants. Little research studies are available on the long
term application of organic wastes in agriculture as soil remediation.
For the effective use of organics in agriculture and soil management,
long term research data is needed. Businelli et al. (2009) reported that
during a 10 year trial period of application of municipal solid waste com-
post, the accumulation of toxic metals in the topsoil were in the order of
CuNZnNPbNCd. Similarly, the consecutive application of swine compost
for six years significantly increased the concentrations of Cu and Zn in
the upper 10–20 cm depth of soil as compared to control (Zhao et al.,
2006). In N 10 year experiments the application of sludge and composted
sludge resulted in high accumulation of Cu, Zn and Cr due the concentra-
tions of the metals in raw materials (Kunito et al., 2001; Saviozzi et al.,
1999).
It may be possible to reduce the concentration of toxic metals in com-
post by proper separation of suitable organic wastes at source
(Montemurro et al., 2009). Keeping in view the protection of the envi-
ronment from toxic metals in long run it is necessary to develop and
strictly implement sophisticated treatments for potentially polluting or-
ganic wastes. The repeated application of high quality bio-waste com-
post for 10 years, in spite of high application rate, showed no
significant variation in total and bioavailable fraction of toxic metal con-
centrations (Erhart et al., 2008). Regular monitoring of total toxic metal
concentrations, different fractions, and their percentage contributions
to total metal concentrations are the key determinants. In context of
long term application of organic wastes to agriculture soil especially or-
ganic wastes containing high concentrations of toxic metals, these deter-
minants can not only provide key information about the present scenario
but also help to predict the future situation (Businelli et al., 2009; Zhao et
al., 2006). Similarly the application rate of organic wastes is also an im-
portant factor regarding toxic metals loading to soil. Scientific informa-
tion is needed on organic amendments, for these can increase toxic
metal concentrations in contaminated soil, while other soil properties
like concentrations of essential macro- and micro-nutrients also need
to be considered. Organic amendments can result in overdose of essen-
tial and non-essential elements and secondary pollution. Based on the
above mentioned discussion, it is necessary to carefully evaluate the
amendments prior to their application. Similarly, soil to be remediated
and organic amendments must be analysed for all physicochemical pa-
rameters, including essential macro- and micro-nutrients to avoid over
application and secondary contamination of soil.
11. Conclusion
The consumption of foods contaminated by Cd poses great threat to
human health. The use of organic amendments to reduce Cd uptake by
plants appears to have potential as a cost-effective remediation option.
Their application to agriculture soils not only improves the soil physical-
ly, but also provides essential nutrients to soil and plants. Organic
amendments reduce the exchangeable fraction of Cd in soil by adsorp-
tion and complexation reactions thus reducing their bioaccessibility
and plant uptake. Organic amendments also enhance plant growth and
increase biomass production. Among different organic amendments,
sewage sludge biochar, solid waste compost, and organic fertilizers
have shown the promising results for plant production, while animal
manure, saw dust, biochar, and rice husk significantly reduce Cd bioaccu-
mulation. However, some amendments may contain elevated levels of
Cd, and their application could therefore exacerbate soil contamination
problems. Therefore, it is recommended that the metal concentration
in organic amendments be characterized prior to their application to ag-
riculture soils, thus ensuring soil quality and food safety.
Acknowledgement
This study is financially supported by Higher Education Commission,
Pakistan (112-23334-2PS1-4221). S. Khan acknowledges the funding
from the Chinese Academy of Sciences President's International Fellow-
ship for Visiting Scientists (2015VEB055). We thank Prof. Mark L
Brusseau, The University of Arizona, USA for editing/polishing the
manuscript.
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