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Environ Monit Assess (2015) 187:161

DOI 10.1007/s10661-015-4355-3

Study on heavy metal levels and its health risk assessment


in some edible fishes from Nansi Lake, China
Fangkun Zhu & Li Qu & Wenxiu Fan & Airong Wang &
Hailing Hao & Xiaobo Li & Shuwen Yao

Received: 7 October 2014 / Accepted: 9 February 2015


# Springer International Publishing Switzerland 2015

Abstract Eight heavy metals, namely Cu, Zn, Fe, Mn, Introduction
Cd, Ni, Pb, and As in the muscles of nine fish species
collected from Nansi Lake, China. were determined, and Fish is widely consumed by humans in the world due to
the potential health risks to local residents via consump- their high protein supply and omega-3 fatty acids that
tion of the fishes were estimated. The results of two-way help reduce the risk of certain types of cancer and
ANOVA that showed the concentrations of heavy cardiovascular diseases (Storelli 2008). However, fish
metals in the investigated fish samples were influenced has been reported to accumulate large amounts of some
significantly by fish species and sampling sites. Corre- metals and is often at the top of the aquatic food chain
lation analysis indicated that sampling sites had signif- (Mansour and Sidky 2002; Tzen 2003; Bidar et al.
icant effects on the levels of correlation coefficients 2009). High content of heavy metals leads to severe
among different heavy metal concentrations. Interest- threat to fish and consequently results the health risks
ingly, although none of the hazard quotient (HQ) values to people associated with fish consumption. On the
of any individual element was greater than 1 for the other hand, fish is often used to monitor heavy metals
investigated exposure population through fish consump- and the other pollutions of aquatic ecosystems (Dorea
tion, the hazard index (HI) values were more than 1 for 2008; Ahmad and Shuhaimi-Othman 2010; Rahman
local fishermen, suggesting that local fishermen may be et al. 2012). The concentrations of heavy metals in the
experiencing some adverse health effects. Among the tissues and organs of fishes indicate the concentrations
investigated nine fish species, Cyprinus carpio had the of heavy metals in water and their accumulation in food
highest HQ and HI. As, Pb, and Cd were the most chains (Pintaeva et al. 2011). So, it is necessary to assess
concerning heavy metals in the investigated fish sam- the levels of heavy metals in fishes and to report possible
ples due to their higher relative contributions to the HI contamination that would represent a health hazard.
values. Lately, numerous investigations and monitoring pro-
grams have been carried out on heavy metal concentra-
tions in fishes (Tzen and Soylak 2007; Uluozlu et al.
Keywords Fish . Heavy metals . Health risk . Nansi Lake 2007; Mendil et al. 2005; Reynders et al. 2008; Tzen
2009; Tzen et al. 2009; Yi et al. 2011).
Nansi Lake (34 27 N35 20 N, 116 34 E117
F. Zhu (*) : W. Fan : A. Wang : H. Hao : X. Li : S. Yao
21 E) is the largest fresh water lake in Shandong Prov-
School of Chemistry and Chemical Engineering, Henan ince, China with a surface area of 1266 km2 and an
Institute of Science and Technology, 453003 Xinxiang, China average water depth of 1.46 m. It is composed of four
e-mail: fkzhu001@163.com lakes, namely Nanyang Lake, Dushan Lake, Zhaoyang
Lake, and Weishan Lake. Nansi area is one of the most
L. Qu
Xinke College, Henan Institute of Science and Technology, economically developed regions in China and has been
453003 Xinxiang, China polluted significantly by heavy metals originating from
161 Page 2 of 13 Environ Monit Assess (2015) 187:161

anthropogenic sources, such as electronics, metalwork, (Milli-Q Millipore; 18.2 M cm1) was used for all
and mining industries, putting thousands of people in dilutions. The element standard solutions were pre-
this area into tremendous health hazard. Previous studies pared by dilution of 1000 mg l1 certified standard
mostly focused on the sediments in Nansi Lake (An and solutions (Nssrc, China). XT-9912 model microwave
Li 2009; Li et al. 2009; Liu et al. 2010). However, there system (Xintuo, China) equipped with advanced
is a lack of studies regarding metal levels in edible fishes composite PTFE vessels was used for digestion of
from Nansi Lake and whether these levels represent a the samples. A Perkin Elmer Analyst 700 (CT, USA)
human health risk for local residents. Therefore, the atomic absorption spectrometer equipped with HGA
objectives of the present study were to determine the graphite furnace (GF-AAS) was used to determine
concentrations of Cu, Zn, Fe, Mn, Cd, Ni, Pb, and As in Cd, Ni, Pb, and As. For graphite furnace measure-
the muscles of nine fish species collected from Nansi ments, argon was used as inert gas. Pyrolytic-coated
Lake and estimate the potential health risk of heavy graphite tubes (Perkin Elmer part no. B3 001264)
metals to local residents through fish consumption. with a platform were used. Samples were injected
into the graphite furnace using Perkin Elmer AS-
800 autosampler. Optima 2100 DV model inductive-
Materials and methods ly coupled plasma atomic emission spectroscopy
(ICP-AES) (PE, USA) was used for simultaneous
Sampling multielement detection of Cu, Zn, Fe, and Mn. De-
tection limit values of elements as milligram per liter
A total of 288 fish samples belonging to ten fish species were found to be 0.018 for Cu, 0.010 for Zn, 0.016
were collected from four lakes, Nanyang Lake, Dushan for Fe, 0.020 for Mn, 0.09 for Cd, 0.35 for Ni, 0.18
Lake, Zhaoyang Lake, and Weishan Lake (Fig. 1) dur- for Pb, and 0.17 for As in this study. The operating
ing four seasons, from the spring to the winter of 2012. conditions of ICP-AES and GF-AAS were listed in
The species were Ophiocephalus argus, Carassius Table 1.
auratus, Pseudobagrus fulvidraco, Parabramis
pekinensis, Atractoscion nobilis, Ctenopharyngodon
Microwave digestion
idellus, Scomberomorus niphonius, Silurus asotus, and
Cyprinus carpio. The fish samples collected were
One gram muscle sample was digested with 5 ml of
washed with clean water at the point of collection,
65 % HNO3 and 2 ml of 30 % H2O2 in microwave
separated by species, placed on ice, brought to the
digestion system and finally diluted to 10 ml with dou-
laboratory on the same day, and then frozen at 20 C
ble deionized water. A blank digest was carried out in
until dissection.
the same way. All sample solutions were clear. Diges-
tion conditions for microwave system were applied as
Sample preparation
3 min for 400 W, 5 min for 600 W, 8 min for 900 W,
8 min for 1000 W, vent 8 min, respectively.
Frozen fish samples were thawed at room temperature
and dissected using stainless steel scalpels. One gram of
accurately weighed epaxial muscle was dissected. One Quality assurance
gram of accurately weighed epaxial muscle from each
sample was dissected for analysis. They were washed All glasswares and equipments were carefully
with distilled water, dried in filter paper, weighed, cleaned starting with 2 % HNO3 and ending with
packed in polyethylene bags, and stored at 20 C until repeated rinsing distilled deionized water to prevent
analysis. contamination. Reagent blank determinations were
used to correct the instrument readings. Detection
Reagents and apparatus limit is defined as the concentration corresponding
to three times the standard deviation of ten blanks.
All reagents were of analytical reagent grade unless Certified reference material (DORM-2 dogfish
otherwise stated. HNO3 and H2O2 were of suprapure muscle) were used for accuracy evaluation, and the
quality (Merck, Germany). Double deionized water recovered values were given in Table 2.
Environ Monit Assess (2015) 187:161 Page 3 of 13 161

Fig. 1 Locating map of the study area (Nansi Lake, Shandong Province, China)

Risk assessment there may be concern for potential non-cancer effects.


As a rule, the greater the value of HQ above 1, the higher
A potential non-cancer risk for individual heavy metals the level of concern.
is expressed as the hazard quotient (HQ) (US EPA 1992, A hazard index (HI) approach was used to assess the
1999) and can be calculated as follows: overall potential non-carcinogenic health risk posed by
more than one heavy metal. The HI is equal to the sum
ADD
HQ 1 of the HQs, as described in Eq. (3) (US EPA 1989).
Rf D

HI HQ1 HQ2 HQn 3


C  IR
ADD 2
BW

where RfD is the daily intake reference dose Statistical analysis


(g kg1 day1); ADD is the average daily intake of
heavy metals (g kg1 day1); C is the mean concentra- Two-way analysis of variance (ANOVA) was employed
tions of heavy metals in fish (g kg1); IR is the con- to test whether varied significantly between the heavy
sumption rate of fish (g person1 day1); and BW is the metal concentrations and three factors (species, sites,
average adult body weight (kg). The RfD values were and seasons). The significance level was set at 0.05.
40, 300, 700, 240, 1, 20, and 0.3 g kg1 day1 for Person correlation analysis was adopted to examine
copper, zinc, iron, manganese, cadmium, nickel, and the inter-relationships among the investigated heavy
arsenic, respectively (US EPA 2007). Because the RfD metal concentrations in the fish samples. Data calcula-
f o r P b w a s n o t a v a il a b l e , w e u s e d J E C FA tion and statistical analysis were performed with EX-
3.57 g kg day1 (JECFA 2003). If the HQ exceeds 1, CEL and SPSS 19.0.
161 Page 4 of 13 Environ Monit Assess (2015) 187:161

Table 1 The operating conditions of ICP-AES and GF-AAS

Conditions for ICP-AES


RF power (W) 1200
Auxiliary gas (ml min1) 0.6
Coolant gas (ml min1) 18
Nebulizer gas (ml min1) 0.8
Sample uptake (ml min1) 1.5
Torch Axial
Elements Cu Zn Fe Mn
Wavelength (nm) 327.4 206.2 238.2 257.6
Conditions for GF-AAS
Elements Cd Ni Pb As
Wavelength (nm) 228.7 231.9 283.1 193.5
Argon flow (ml min1) 250 250 250 250
Sample volume (l) 20 20 20 20
Modifier (l) 10 5 5 5
Drying 1 120 (5, 20) 100 (5, 20) 100 (5, 20) 100 (5, 20)
Drying 2 140 (15, 15) 140 (15, 15) 140 (15, 15) 140 (15, 15)
Ashing 800 (10, 20) 1000 (10, 20) 800 (10, 20) 1300 (10, 20)
Atomization 1800 (0, 5) 2200 (0, 5) 2000 (0, 5) 2200 (0, 5)
Cleaning 2500 (1, 3) 2500 (1, 3) 2500 (1, 3) 2500 (1, 3)

Results and discussion be 1.475.67, 11.4328.23, 8.7335.81, 1.484.62,


0.120.35, 0.843.12, 0.280.65, and 0.05
The concentrations of heavy metals in fish 0.10 g g1, respectively. Among all determined heavy
metals, iron was found to be the dominant elemental ion
The concentrations of heavy metals in the studied nine followed by zinc and copper.
fish species were given in Table 3. All metal concentra- There was a great variation in zinc concentrations
tions were determined on a wet weight basis. The con- among the investigated fish muscles. Fishes are known
centrations of copper, zinc, iron, manganese, cadmium, to have a high threshold level of zinc. The minimum and
nickel, lead, and arsenic in fish samples were found to maximum lead levels observed were 11.43 g g1 in
A. nobilis and 28.23 g g1 in C. auratus. Zinc is known
Table 2 Heavy metal concentrations in certified reference mate- to be involved in most metabolic pathways in humans,
rial (DORM-2 dogfish muscle) (n=3) and zinc deficiency can lead to loss of appetite, growth
retardation, skin changes, and immunological abnor-
Element Certified value Our value Recovery
(g g1) (g g1) (%)
malities. The concentrations of zinc in all the fish sam-
ples were found to be lower than the standard of
Cu 2.340.16 2.280.15 97 30 g g1 (FAO 1983) and 50 g g1 (MAFF 1995).
Zn 25.62.3 25.11.2 98 Iron was found to be the dominant element as com-
Fe 14210 1445.2 101 pared with other heavy metals in fish samples. The iron
Mn 3.660.34 3.610.19 99 contents in the investigated fish samples ranged from
Cd 0.0430.008 0.0440.008 102 8.73 to 35.81 g g1. C. auratus had the highest iron
Ni 19.43.1 18.91.5 97 concentration whereas P. fulvidraco had the lowest. Iron
Pb 0.0650.007 0.0660.004 102 is vital for almost all living organisms, participating in a
As 181.1 17.71.0 98 wide variety of metabolic processes, such as oxygen
transport, DNA synthesis, and electron transport. The
Environ Monit Assess (2015) 187:161 Page 5 of 13 161

RDA of iron for 712 months infants and 5170 years O. argus. Lead is similar to cadmium that has no bene-
adults is 11 and 8 mg day1, respectively (Ikem and ficial role in human metabolism, producing progressive
Egiebor 2005). toxicity. Lead creates health disorders such as sleepless-
Copper is an essential part of several enzymes and is ness, tiredness, and hear and weight loss. The maximum
necessary for the synthesis of hemoglobin (Sivaperumal permitted lead level is 2.0 g g1 set by MAFF (1995)
et al. 2007). However, high intake of Cu has been and WHO (1996). The maximum permitted concentra-
recognized to cause adverse health problem (Gorell tion of Pb proposed by Australian National Health and
et al. 1997). The lowest and highest Cu levels in fish Medical Research Council is 2.0 g g1 (wet weight)
species were found as 1.47 g g1 in O. argus and (Plaskett and Potter 1979). The lead levels in the inves-
5.67 g g1 in A. nobilis. The maximum copper level tigated fish samples were found to be lower than the
permitted is 30 g g1 (wet weight) for FAO (1983) and standard.
20 g g1 for WHO (1996). The Australian Food Stan- Inorganic arsenic is considered to be the most toxic to
dard Code established the maximum concentration for human health. Arsenic at low doses over a long period
Cu at 10 g g1 (wet weight) (Alam et al. 2002). The of time is known to cause skin changes that may lead to
copper levels in analyzed fish samples were found to be skin cancer. The lowest and highest arsenic content in
lower than these limits. fish species were found as 0.05 g g1 in S. niphonius
Manganese, one of the essential trace elements, is a and 0.10 g g1 in P. fulvidraco. The maximum arsenic
structure component of some enzymes and activates the level permitted for fishes is 1.0 g g1 according to
actions of some enzymes. The deficiency of manganese Australia standard (Australia New Zealand Food Au-
can produce severe skeletal and reproductive abnormal- thority 1998). US Environmental Protection Agency
ities in mammals. High doses of manganese produce (EPA) has set arsenic tissue residues of 1.3 g g1 in
adverse effects primarily on the lungs and brain. In this freshwater fish (wet weight) as the criterion for human
study, the lowest iron content was 1.48 g g1, for health protection (Burger and Gochfeld 2005). The ar-
C. auratus, whereas the highest was 4.62 g g1, for senic concentrations in the studied fish samples were far
C. carpio. The US National Academy of Science rec- below these standards.
ommends 2.55 mg manganese per day (National Acad-
emy of Sciences 1980), and the World Health Organi- Two-way ANOVA analysis
zation recommended 29 mg per day for an adult (WHO
1994). The results of two-way ANOVA presented in Table 3
In the present investigation, the lowest concentration indicating the concentrations of each heavy metal in the
of nickel was found in C. auratus (0.82 g g1) and the investigated fish samples changed significantly among
highest in C. idellus (3.12 g g1). Nickel normally different fish species. This might be a result of different
occurs at very low levels in the environment, and it ecological needs, metabolism, and feeding patterns for
can cause variety of pulmonary adverse health effects, different species. The results clearly showed that sites
such as lung inflammation, fibrosis, emphysema, and had significant effects on the levels of Zn, Cd, Ni, Pb,
tumors (Forti et al. 2011). The WHO recommends 100 and As in fish samples. Season variation, however, did
300 g nickel for daily intake (WHO 1994). not bring out significant content changes of heavy
Cadmium is not a part of natural biochemical pro- metals except Cu and Cd. The effects of the interaction
cesses and is extremely hazardous. The cadmium con- between species and sites suggested that the significant
centrations were found in the range of 0.120.35 g g1. variations were only found in Fe and Pb concentrations.
O. argus had the lowest lead concentration whereas It is also observed that only Cu level was influenced
C. carpio had the highest. The concentrations of cadmi- significantly by interaction of speciesseasons. On the
um in all fish samples were far below the Western whole, the concentrations of heavy metals in the inves-
Australian authorities proposed level of 5.5 g g1 tigated fish samples were mainly influenced by fish
(Plaskett and Potter 1979). But, the cadmium levels in species and sites. The fishes collected from Nanyang
some fish samples were higher than the standard of Lake had the highest concentrations of Cu, Fe, Mn, Cd,
2.0 g g1 (FAO 1983) and 50 g g1 (MAFF 1995). Pb, and As, while fishes from Weishan Lake had the
The minimum and maximum lead levels observed lowest concentrations of Zn, Fe, Mn, Ni, Cd, Pb, and
were 0.28 g g1 in S. asotus and 0.65 g g1 in As. The metal contents in fishes of other two lakes were
Table 3 Heavy metal concentrations in fish samples (g g1)
161

Element Species ANOVA

C. auratus P. fulvidraco O. argus P. pekinensis C. carpio C. idellus S. asotus S. niphonius A. nobilis Factor p value
Page 6 of 13

Zn Average 28.231.41 13.351.16 12.610.87 11.540.82 21.781.35 15.881.23 25.491.57 15.921.21 11.430.85 Specie 5.88E46
Site 0.021
Season 0.004
Range 22.6635.17 11.8317.25 7.4118.58 6.8214.19 18.4427.61 9.5717.62 19.3528.26 13.5118.39 9.7515.53 Speciesite 0.227
Specieseason 0.415
Fe Average 35.811.74 8.730.68 19.561.33 31.622.15 28.351.74 16.521.16 25.311.53 28.121.83 16.461.17 Specie 1.16E61
Site 0.851
Season 0.527
Range 31.2637.83 6.529.94 15.7121.85 28.3736.43 24.1629.62 15.2819.81 18.4428.71 26.5434.39 11.8318.56 Speciesite 0.005
Specieseason 0.449
Cu Average 2.640.18 3.310.21 1.470.11 4.350.27 5.560.28 2.260.18 1.580.13 3.460.25 5.670.38 Specie 3.69E54
Site 0.191
Season 0.038
Range 1.932.86 2.543.75 0.971.93 3.584.86 4.376.91 1.752.82 1.141.88 2.723.97 4.346.51 Speciesite 0.951
Specieseason 0.028
Mn Average 1.480.11 1.770.15 2.810.23 2.860.23 4.620.31 2.730.22 3.550.28 3.210.26 1.960.15 Specie 1.71E60
Site 0.247
Season 0.363
Range 1.151.93 1.462.54 2.273.38 2.453.14 4.115.52 2.283.48 2.894.34 2.643.78 1.682.47 Speciesite 0.024
Specieseason 0.241
Cd Average 0.230.02 0.190.02 0.120.01 0.280.02 0.350.03 0.170.01 0.210.02 0.310.03 0.180.02 Specie 2.18E45
Site 0.005
Season 0.068
Range 0.150.27 0.140.23 0.060.15 0.220.37 0.280.41 0.130.24 0.150.28 0.240.36 0.130.23 Speciesite 0.605
Specieseason 0.956
Ni Average 0.840.06 1.280.09 2.650.17 1.810.12 2.760.17 3.120.19 1.630.10 2.060.14 1.140.09 Specie 2.83E68
Site 0.001
Environ Monit Assess (2015) 187:161

Season 0.453
Range 0.620.97 0.931.46 2.132.95 1.442.38 2.173.28 2.753.46 1.281.89 1.512.53 0.831.47 Speciesite 0.078
Specieseason 0.095
Environ Monit Assess (2015) 187:161 Page 7 of 13 161

5.01E59

6.57E56
1.87E5
found in between. This might suggest that heavy metal

p value

0.008
0.950

0.062
0.004

0.816
0.669

0.825
pollution in Nanyang Lake was more serious than the
other three lakes. The previous study showed that the

Specieseason

Specieseason
concentrations of heavy metals in fishes were seriously

Speciesite

Speciesite
affected by river input to the lake (Yu et al. 2012). In
ANOVA

fact, the Nanyang Lake receives a large amount of


Season

Season
Specie
Specie
Factor

Site

Site
wastewater containing heavy metals as several main
river branches flow across the important industrial cities
such as Jining, Yunzhou, and Hezhe, resulting the in-
0.090.02
0.430.03

0.360.52

0.070.13
A. nobilis

crease of heavy metal concentrations in the water and


sediment environment of Nanyang Lake. Consequently,
the metal concentrations in fishes living in this lake area
S. niphonius

increase.
0.050.01
0.370.03

0.320.47

0.030.09

Correlation analysis

Inter-element relationships can provide important infor-


0.080.02
0.280.02

0.210.36

0.060.11
S. asotus

mation on the sources and pathways of the heavy


metals. The correlation coefficients between different
heavy metal concentrations in the investigated fish sam-
ples were given in Table 4. The results clearly showed
0.060.02
0.530.04

0.440.65

0.040.10
C. idellus

that correlation coefficients were influenced significant-


ly by the sampling sites. For Nanyang Lake, there were
good correlations between Cu and Zn, Fe and Cd, Fe
and Pb, and Ni and As for the investigated fish species.
0.070.01
0.420.03

0.370.51

0.050.09
C. carpio

For Dushan Lake, significant correlations were found


between Fe and Cd, Mn and Ni, As and Ni, and As and
Pb. For Zhaoyang Lake, between Zn and Mn, Fe and
Mn, Fe and Cd, Fe and Pb, Mn and Cd, Mn and Pb, and
P. pekinensis

0.340.03

0.080.01
0.250.39

0.050.12

Cd and Pb were found to have significant correlations.


For Weishan Lake, CuPb, MnPb, CdPb, and Ni
As were significantly correlated. These significant
correlations might indicate that the distributions of
0.650.05

0.070.01
0.480.76

0.040.12

these pairs of metals were regulated by common


O. argus

local inputs and similar dispersion processes in the


study area.
P. fulvidraco

0.460.03

0.100.02

Comparison of metal levels in fish from Nansi Lake


0.370.51

0.070.12

with reported values

In order to determine the degree of contamination in the


studied area, the concentrations of heavy metals in the
0.310.02

0.080.02
C. auratus

0.240.39

0.050.11
Species

investigated fish samples collected from Nansi Lake


were compared with the reported values in other lakes
Table 3 (continued)

(Table 5). Reported results in the literatures showed that


Average

Average

metal concentrations in the fish muscles varied widely


Range

Range

depending on where and which species were caught.


Element

Considering the conversion factor 4.8 from wet weight


As
Pb

to dry weight, the heavy metal levels in fish from Nansi


161
Page 8 of 13

Table 4 Correlation coefficients between different heavy metals in the fish samples from different sampling sites

Zn Fe Cu Mn Cd Ni Pb As Zn Fe Cu Mn Cd Ni Pb As

Nanyang Lake Dushan Lake


Zn 1 1
Fe 0.032 1 0.355 1
Cu 0.912** 0.032 1 0.171 0.124 1
Mn 0.166 0.111 0.166 1 0.202 0.509 0.144 1
Cd 0.595 0.685* 0.595 0.093 1 0.083 0.737* 0.584 0.491 1
Ni 0.050 0.095 0.048 0.400 0.033 1 0.169 0.163 0.086 0.812** 0.233 1
Pb 0.120 0.668* 0.119 0.006 0.585 0.605 1 0.471 0.599 0.144 0.09 0.481 0.489 1
As 0.061 0.399 0.059 0.246 0.186 0.733* 0.544 1 0.036 0.428 0.181 0.441 0.363 0.674* 0.691* 1
Zhaoyang Lake Weishan Lake
Zn 1 1
Fe 0.432 1 0.462 1
Cu 0.070 0.246 1 0.319 0.143 1
Mn 0.852** 0.671* 0.174 1 0.145 0.280 0.096 1
Cd 0.618 0.857** 0.506 0.791* 1 0.106 0.604 0.576 0.586 1
Ni 0.210 0.067 0.253 0.400 0.086 1 0.365 0.145 0.249 0.523 0.005 1
Pb 0.479 0.813** 0.486 0.782* 0.930** 0.209 1 0.299 0.189 0.693* 0.745* 0.834** 0.464 1
As 0.564 0.556 0.213 0.433 0.582 0.349 0.445 1 0.028 0.384 0.26 0.428 0.208 0.772* 0.314 1

*Correlation is significant at 0.05 level


**Correlation is significant at 0.01 level
Environ Monit Assess (2015) 187:161
Table 5 Comparison of heavy metal accumulation in fish muscles with the reported values in other lakes (g g1)

Sample area Countries Unit Cu Zn Fe Mn Cd Ni Pb As References

Nansi Lake China ww 1.475.67 11.4328.23 8.7335.81 1.484.62 0.120.35 0.843.12 0.280.65 0.050.10 Present study
Environ Monit Assess (2015) 187:161

Taihu Lake China dw 0.250.97 8.8217.58 0.080.43 0.060.18 0.060.26 Yu et al. 2012
Taihu Lake China dw 14.5998.08 0.772.72 0.3216.24 0.010.05 0.041.01 0.020.34 Zeng et al. 2012
Taihu Lake China dw 1.0683.88 63.33367.39 0.471.76 1.896.35 6.6327.18 1.043.99 Fu et al. 2013
Nam Co Lake China ww 2 6.9 0.61 0.025 0.094 0.047 Yang et al. 2007
Yamdro Lake China ww 1.1 4.4 0.24 0.024 0.12 0.079 Yang et al. 2007
Macquarie Lake Australia dw 0.383.16 14.075.4 <0.211 <1.036 Roach et al. 2008
Ataturk Dam Lake Turkey ww 0.812.41 3.6420.70 0.131.76 ND ND ND 5.3217.96 Karadede and nl 2000
Manzala Lake Egypt dw 3.4305.490 12.98035.450 0.8101.610 1.4102.660 Mohamed et al. 2011
George Lake Uganda dw 0.22.5 8.364.4 <2.5 Lwanga et al. 2003
Chascomus Lake Argentina dw 0.951.35 20.823.1 25.552.1 0.841.58 <0.01 0.841.04 0.371.3 0.130.27 Schenone et al. 2014
Awassa Lake Ethiopia ww 0.540.65 3.675.30 ND 0.0020.01 0.0030.004 Yohannes et al. 2013
Tanganyika Lake Africa dw 3.64.04 16101 0.597.81 0.250.38 4.645.03 Chale 2002
alek Lake Slovenia ww 6.7116.5 <0.01 0.010.04 0.020.08 Petkovek et al. 2012
Itezhi-tezhi Lake Zambia dw 233 2178 0.280.82 0.041.36 Nakayama et al. 2010
Kariba Lake
Plitvice Lakes Croatia dw 115 258 10.9 11.7 Vukosav et al. 2010
Budi Lake Chile dw 0.4839.04 0.0212.17 <0.26 <1.88 Tapia et al. 2012
Rawal Lake Pakistan ww 0.1991.293 8.49124.23 1.8119.835 0.4872.336 0.4490.745 5.0388.796 Iqbal and Shah 2014

ww wet weight, dw dry weight, ND not detectable


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161 Page 10 of 13 Environ Monit Assess (2015) 187:161

Table 6 HQ and HI values for different exposure groups due to consumption of different fish species

Fish species Exposure group HQ HI

Zn Fe Cu Mn Cd Ni Pb As

C. auratus General population 0.058 0.031 0.040 0.004 0.141 0.026 0.053 0.163 0.516
Fishermen 0.148 0.080 0.104 0.010 0.361 0.066 0.136 0.418 1.323
P. fulvidraco General population 0.027 0.008 0.051 0.005 0.116 0.039 0.079 0.204 0.529
Fishermen 0.070 0.020 0.130 0.012 0.298 0.100 0.202 0.333 1.165
O. argus General population 0.026 0.017 0.022 0.007 0.073 0.081 0.111 0.143 0.480
Fishermen 0.066 0.044 0.058 0.018 0.188 0.208 0.286 0.366 1.234
P. pekinensis General population 0.024 0.028 0.066 0.007 0.171 0.055 0.058 0.163 0.572
Fishermen 0.060 0.071 0.171 0.019 0.439 0.142 0.149 0.418 1.469
C. carpio General population 0.044 0.025 0.085 0.012 0.214 0.084 0.072 0.143 0.679
Fishermen 0.114 0.064 0.218 0.030 0.549 0.216 0.185 0.366 1.742
C. idellus General population 0.032 0.014 0.035 0.007 0.104 0.095 0.091 0.122 0.500
Fishermen 0.083 0.037 0.089 0.018 0.267 0.245 0.233 0.314 1.286
S. asotus General population 0.052 0.022 0.024 0.009 0.128 0.050 0.048 0.163 0.496
Fishermen 0.133 0.057 0.062 0.023 0.329 0.128 0.123 0.418 1.273
S. niphonius General population 0.032 0.025 0.053 0.008 0.190 0.063 0.063 0.102 0.536
Fishermen 0.083 0.063 0.136 0.021 0.486 0.162 0.163 0.261 1.375
A. nobilis General population 0.023 0.014 0.087 0.005 0.110 0.035 0.074 0.183 0.531
Fishermen 0.060 0.037 0.222 0.013 0.282 0.089 0.189 0.471 1.350

Lake were mostly in the high levels compared with the the average consumption rates of fresh fish were 38.4
other lakes. For all collected fresh water fish species and 98.5 g per day for general population and fishermen,
considered collectively, Zn, Mn, and Cd concentrations respectively.
were around the 90th percentile (n=15 for Zn, n=9 for The HQ values of individual metal through fish
Mn, n=14 for Cd) and Pb, Cu, and As around the 75th consumption were calculated and listed in Table 6. For
percentile of the collected worldwide results (n=15 for different exposure population, HQs of individual metal
Pb, n=14 for Cu, n=4 for As). Fe and Ni concentrations were all below 1, which means that the daily intake of
in fishes from Nansi Lake were found to be higher than individual metal through the consumption of fish would
the reported values in other lakes. The above results may be unlikely to cause adverse health effects for local
indicate that Nansi Lake has been suffering more severe residents. However, for different exposure groups, HQ
pollution. values exhibited different potential risks. The HQ of
every metal for fishermen was higher than for general
Potential health risk to local residents via consumption population, which is a coincidence with those found in
of fish previous report (Yu et al. 2012). There was a big dis-
crepancy of HQ among different metals. HQs of As and
Fish from Nansi Lake is an important daily food re- Cr were the biggest, ranging from 0.102 to 0.471 and
source for local residents. Therefore, it is necessary to 0.073 to 0.549. HQ of Cr was the lowest, having con-
assess the potential health risks caused by the consump- centrations between 0.004 and 0.030. On the whole,
tion of local fishes. A total of 1450 adult volunteers who A. nobilis had the highest HQs whereas S. niphonius
have been told the objectives of this study before the had the lowest.
face-to-face survey were randomly recruited from local It is very interesting that there is no single metal
villages in 2012. The results of our questionnaires exposure that exceeds its RfD, but the potential risk
showed that the average body weight is 62.8 kg, and due to the combined effects of all heavy metals through
Environ Monit Assess (2015) 187:161 Page 11 of 13 161

fish consumption is significant for fishermen other than exposure routs were considered, total heavy metals
general population. As shown in Table 6, the HI values would be likely to pose higher health risks to local
were observed in the range of 0.4800.679 for general residents.
population, suggesting that general population were not
likely to be hurt by heavy metals through fish consump-
tion. However, the HI values ranged from 1.165 to 1.742 Conclusions
for fishermen, indicating that local fishermen may ex-
perience some adverse health effects. Generally, The heavy metal concentrations found in the fish
C. carpio consumption had the highest health risk for muscles sampled from Nansi Lake decreased in the
the investigated exposure groups, while P. fulvidraco order of Fe>Zn>Cu>Mn>Ni>Pb>Cd>As. In gen-
consumption had the lowest. The results indicated that eral, the levels of Zn, Cu, Ni, Pb, and As in the
the consumption of the fishes from Nanyang Lake had investigated fish samples were found to be lower than
the highest health risk for local residents, while the the legal limits. However, the cadmium levels in
consumption of the fishes from Weishan Lake had the some fish samples were higher than the standards
lowest. The data listed in Table 6 and Fig. 2 showed that set by FAO and MAFF. The results of two-way
As, Pb, and Cd were the key elements contributing to ANOVA showed that the concentrations of heavy
the HI values, and the sum of the three components was metals in the investigated fish samples were affected
more than 50 %, with Cu and Ni being secondary and significantly by fish species and sampling sites. The
Zn, Mn, and Fe the least important. High potential risk HQ values for any individual heavy metal were be-
due to As, Pb, and Cd may be related to wastewater low 1, which means that the daily intake of individual
released from metallurgy and chemical plants in this metal through fish consumption would be unlikely to
area. cause health risk for local residents. It should be
It is worth mentioning that the exposure risk esti- noted, however, that the aggregate effects of eight
mates in this study were only for fish, without account- heavy metals were more than 1 for local fishermen,
ing for any other sources. Many studies showed that indicating that the fishermen were more likely to
human beings are significantly exposed to heavy metals experience adverse health effects. As, Pb, and Cd
through other foods such as rice, wheat, and vegetable are the key elements contributing to the potential
(Zheng et al. 2007; Huang et al. 2008; Hang et al. 2009). health risk of non-carcinogenic effects for general
If potential health risks of heavy metals through these population and fishermen. Furthermore, considerable

Fig. 2 HI values to local


residents via consumption of
fishes from different lakes. 1
General population, 2 fishermen
161 Page 12 of 13 Environ Monit Assess (2015) 187:161

attention should also be paid to the potential health Hang, X. S., Wang, H. Y., Zhou, J. M., Ma, C. L., Du, C. W., &
Chen, X. Q. (2009). Risk assessment of potentially toxic
risks of heavy metals through other exposure
element pollution in soils and rice (Oryza sativa) in a typical
pathways. area of the Yangtze River Delta. Environmental Pollution,
157, 25422549.
Huang, M. L., Zhou, S. L., Sun, B., & Zhao, Q. G. (2008). Heavy
Acknowledgments The authors would like to thank the key metals in wheat grain: assessment of potential health risk for
science and technology project of Henan for its financial support inhabitants in Kunshan, China. Science of the Total
[142101310425]. Environment, 405, 5461.
Ikem, A., & Egiebor, N. O. (2005). Assessment of trace elements
in canned fishes (mackerel, tuna, salmon, sardines and her-
rings) marketed in Georgia and Alabama (United States of
America). Journal of Food Composition and Analysis, 18,
References 771787.
Iqbal, J., & Shah, M. H. (2014). Study of seasonal variations and
health risk assessment of heavy metals in Cyprinus carpio
Ahmad, A. K., & Shuhaimi-Othman, M. (2010). Heavy metal from Rawal Lake, Pakistan. Environmental Monitoring and
concentrations in sediments and fishes from Lake Chini, Assessment, 186, 20252037.
Pahang, Malaysia. Journal of Biological Sciences, 10(2), JECFA. (2003). Summary and conclusions of the 61st meeting of
93100. the Joint FAO/WHO Expert Committee on Food Additives.
Alam, M. G. M., Tanaka, A., Allinson, G., Laurenson, L. J. B., JECFA/61/SC. Rome, Italy.
Stagnitti, F., & Snow, E. T. (2002). A comparison of trace Karadede, H., & nl, E. (2000). Concentrations of some heavy
element concentrations in cultured and wild carp (Cyprinus metals in water, sediment and fish species from the Ataturk
carpio) of Lake Kasumigaura, Japan. Ecotoxicology and Dam Lake (Euphrates), Turkey. Chemosphere, 41, 13711376.
Environmental Safety, 53, 348354. Li, H. L., Gao, H., Zhu, C., Li, G. G., Yang, F., Gong, Z. Y., &
An, W. C., & Li, X. M. (2009). Phosphate adsorption characteris- Lian, J. (2009). Spatial and temporal distribution of polycy-
tics at the sedimentwater interface and phosphorus fractions clic aromatic hydrocarbons (PAHs) in sediments of the Nansi
in Nansi Lake, China, and its main inflow rivers. Lake, China. Environmental Monitoring and Assessment,
Environmental Monitoring and Assessment, 148, 173184. 154, 469478.
Australia New Zealand Food Authority. (1998). Food standards Liu, E. F., Shen, J., Yang, L. Y., Zhang, E. L., Meng, X. H., &
code. Standard A12, Issue 37. Wang, J. J. (2010). Assessment of heavy metal contamination
Bidar, G., Pruvot, C., Garon, G., Verdin, A., Shirali, P., & Douay, in the sediments of Nansihu Lake Catchment, China.
F. (2009). Seasonal and annual variations of metal uptake, Environmental Monitoring and Assessment, 161, 217227.
bioaccumulation, and toxicity in Trifolium repens and Lwanga, M. S., Kansiime, F., Denny, P., & Scullion, J. (2003).
Lolium perenne growing in a heavy metal-contaminated Heavy metals in Lake George, Uganda, with relation to metal
field. Environmental Science and Pollution Research, 16, concentrations in tissues of common fish specie.
4253. Hydrobiologia, 499, 8393.
Burger, J., & Gochfeld, M. (2005). Heavy metals in commercial MAFF. (1995). Monitoring and surveillance of non-radioactive
fish in New Jersey. Environmental Research, 99, 403412. contaminants in the aquatic environment and activities reg-
Chale, F. M. M. (2002). Trace metal concentrations in water, ulating the disposal of wastes at sea, 1993. Aquatic
sediments and fish tissue from Lake Tanganyika. Science of Environment Monitoring Report No. 44. Direcorate of
the Total Environment, 299, 115121. Fisheries Research, Lowestoft.
Dorea, J. G. (2008). Persistent, bioaccumulative and toxic sub- Mansour, A. A., & Sidky, M. M. (2002). Ecotoxicological studies:
stances in fish: human health consideration. Science of the heavy metals contaminating water and fish from Fayum
Total Environment, 400, 93114. Governorate, Egypt. Food Chemistry, 78, 1522.
FAO. (1983). Compilation of legal limits for hazardous substances Mendil, D., Uluzl, . D., Hasdemir, E., Tzen, M., Sar, H., &
in fish and fishery products. FAO Fishery Circular No. 464, Suimez, M. (2005). Determination of trace metal levels in
510. Rome: Food and Agriculture Organization of the seven fish species in lakes in Tokat, Turkey. Food Chemistry,
United Nations. 90, 175179.
Forti, E., Salovaara, S., Cetin, Y., Bulgheroni, A., Pfaller, R. W., & Mohamed, M., Khidr, A. A., & Dheina, N. (2011). Assessment of
Prieto, P. (2011). In vitro evaluation of the toxicity induced heavy metal concentrations in water, plankton, and fish of
by nickel soluble and particulate forms in human airway Lake Manzala, Egypt. Turkish Journal of Zoology, 35,
epithelial cells. Toxicology in Vitro, 25, 454461. 271280.
Fu, J., Hu, X., Tao, X. C., Yu, H. X., & Zhang, X. W. (2013). Risk Nakayama, S. M. M., Ikenaka, Y., Muzandu, K., & Choongo, K.
and toxicity assessments of heavy metals in sediments and (2010). Heavy metal accumulation in lake sediments, fish
fishes from the Yangtze River and Taihu Lake, China. (Oreochromis niloticus and Serranochromis thumbergi), and
Chemosphere, 93, 18871895. crayfish (Cherax quadricarinatus) in Lake Itezhi-tezhi and
Gorell, J. M., Johnson, C. C., Rybicki, B. A., Peterson, E. L., & Lake Kariba, Zambia. Archives of Environmental
Kortsha, G. X. (1997). Occupational exposures to metals Contamination and Toxicology, 59, 291300.
as risk factors for Parkinsons disease. Neurology, 48, National Academy of Sciences. (1980). Recommended dietary
650658. allowances (9th ed.). Washington: National Academic Press.
Environ Monit Assess (2015) 187:161 Page 13 of 13 161

Petkovek, S. A. S., Grudnik, Z. M., & Pokorny, B. (2012). Heavy vapour atomic absorption spectrometry combination. Food
metals and arsenic concentrations in ten fish species from the and Chemical Toxicology, 47, 16481652.
alek lakes (Slovenia): assessment of potential human health Uluozlu, O. D., Tzen, M., Mendil, D., & Soylak, M. (2007).
risk due to fish consumption. Environmental Monitoring and Trace metal content in nine species of fish from the Black and
Assessment, 184(5), 26472662. Aegean Seas, Turkey. Food Chemistry, 104, 835840.
Pintaeva, E. T., Bazarsadueva, S. V., Radnaeva, L. D., Pertov, E. US EPA. (1989). Risk assessment guidance for superfund. Human
A., & Smirnova, O. G. (2011). Content and character of metal health evaluation manual (part A). Interim final, vol. I.
accumulation in fish of the Kichera River (a tributary of Lake Washington (DC): United States Environmental Protection
of Baikal). Contemporary Problems of Ecology, 4, 6468. Agency.
Plaskett, D., & Potter, I. C. (1979). Heavy metal concentrations in US EPA. (1992). Guidelines for exposure assessment, environ-
the muscle tissue of 12 species of teleost from Cockburn mental protection agency, risk assessment forum.
Sound, Western Australia. Australian Journal of Marine & Washington DC.
Fresh Water Research, 30, 607616. US EPA. (1999). Guidance for performing aggregate exposure
Rahman, M. S., Molla, A. H., Saha, N., & Rahman, A. (2012). and risk assessments, environmental protection agency, of-
Study on heavy metals levels and its risk assessment in some fice of pesticide programs. Washington DC.
edible fishes from Bangshi River, Savar, Dhaka, Bangladesh. US EPA. (2007). EPA region 3 RBC table. http://www.epa.gov/
Food Chemistry, 134, 18471854. reg3hwmd/risk/human/rbc/RBCapr07.pdf. Accessed Aug
Reynders, H., Bervoets, L., Gelders, M., & De Coen, W. M. 2008.
(2008). Accumulation and effects of metals in caged carp Vukosav, P., Mlakar, M., Cukrov, N., Kwokal, ., & Pieta, I.
and resident roach along a metal pollution gradient. Science (2010). Heavy metal contents in water, sediment and fish in a
of the Total Environment, 391, 8295. karst aquatic ecosystem of the Plitvice Lakes National Park
Roach, A. C., Maher, W., & Krikowa, F. (2008). Assessment of (Croatia). Archives of Environmental Contamination and
metals in fish from Lake Macquarie, New South Wales, Toxicology, 59, 291300.
Australia. Archives of Environmental Contamination and WHO. (1994). Quality directive of potable water, 2nd ed. (p. 197).
Toxicology, 54, 292308. WHO.
Schenone, N. F., Avigliano, E., Goessler, W., & Cirelli, A. F. WHO. (1996). Health criteria other supporting information. In:
(2014). Toxic metals, trace and major elements determined Guidelines for Drinking Water Quality, vol. 2, 2nd ed. (pp.
by ICPMS in tissues of Parapimelodus valenciennis and 31388). Geneva.
Prochilodus lineatus from Chascomus Lake, Argentina. Yang, R. Q., Yao, T. D., Xu, B. Q., Jiang, G. B., & Xin, X. D.
Microchemical Journal, 112, 127131. (2007). Accumulation features of organochlorine pesticides
Sivaperumal, P., Sankar, T. V., & Nair, P. G. V. (2007). Heavy and heavy metals in fish from high mountain lakes and Lhasa
metal concentrations in fish, shellfish and fish products from River in the Tibetan Plateau. Environment International, 33,
internal markets of India vis--vis international standards. 151156.
Food Chemistry, 102, 612620. Yi, Y. J., Yang, Z. F., & Zhang, S. H. (2011). Ecological risk
Storelli, M. M. (2008). Potential human health risk from metals assessment of heavy metals in sediment and human health
(Hg, Cd, and Pb) and polychlorinated biphenyls (PCBs) via risk assessment of heavy metals in fishes in the middle and
seafood consumption: estimation of target hazard quotients lower reaches of the Yangtze River basin. Environmental
(THQs) and toxic equivalents (TEQs). Food and Chemical Pollution, 159, 25752585.
Toxicology, 46, 27822788. Yohannes, Y. B., Ikenaka, Y., Nakayama, S. M. M., Saengtienchai,
Tapia, J., Vargas-Chacoff, L., Bertrn, C., & Pea-Corts, F. A., Watanabe, K., & Ishizuka, M. (2013). Organochlorine
(2012). Heavy metals in the liver and muscle of pesticides and heavy metals in fish from Lake Awassa,
Micropogonias manni fish from Budi Lake, Araucania Ethiopia: insights from stable isotope analysis.
Region, Chile: potential risk for humans. Environmental Chemosphere, 91, 857863.
Monitoring and Assessment, 184, 31413151. Yu, T., Zhang, Y., Hu, X. N., & Meng, W. (2012). Distribution and
Tzen, M. (2003). Determination of heavy metals in fish samples bioaccumulation of heavy metals in aquatic organisms of
of the Middle Black Sea (Turkey) by graphite furnace atomic different trophic levels and potential health risk assessment
absorption spectrometry. Food Chemistry, 80, 119123. from Taihu lake, China. Ecotoxicology and Environmental
Tzen, M. (2009). Toxic and essential trace elemental contents in Safety, 81, 5564.
fish species from the Black Sea, Turkey. Food and Chemical Zeng, J., Yang, L. Y., Wang, X., Wang, W. X., & Wu, Q. L. (2012).
Toxicology, 47, 17851790. Metal accumulation in fish from different zones of a large,
Tzen, M., & Soylak, M. (2007). Determination of trace metals in shallow freshwater lake. Ecotoxicology and Environmental
canned fish marketed in Turkey. Food Chemistry, 101(4), Safety, 86, 116124.
13951399. Zheng, N., Wang, Q. C., Zheng, X. W., Zheng, D. M., Zhang, Z. S., &
Tzen, M., Karaman, I., Ctak, D., & Soylak, M. (2009). Zhang, S. Q. (2007). Population health risk due to dietary intake
Mercury(II) and methyl mercury determinations in water of heavy metals in the industrial area of Huludao city, China.
and fish samples by using solid phase extraction and cold Science of the Total Environment, 387, 96104.

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