Food and Chemical Toxicology 118 (2018) 753–765

Contents lists available at ScienceDirect

Food and Chemical Toxicology

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

A systematic review and meta-analysis of metal concentrations in canned T

tuna fish in Iran and human health risk assessment
Jamal Rahmania, Yadolah Fakhrib,∗, Abbas Shahsavanic,∗∗, Zohreh Bahmanid,
Mauricio A. Urbinae, Salvatore Chirumbolof, Hassan Keramatig, Bigard Moradih, Abotaleb Bayi,
Geir Bjørklundj,∗∗∗
a
Department of Clinical Nutrition and Dietetics, Faculty of Nutrition and Food Technology, Shahid Beheshti University of Medical Sciences, Tehran, Iran
b
Department of Environmental Health Engineering, Student Research Committee, School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran
c
Environmental and Occupational Hazards Control Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran
d
Department of Environmental Health Engineering, School of Public Health, Iran University of Medical Sciences, Tehran, Iran
e
Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
f
Department of Neurological and Movement Sciences, University of Verona, Italy
g
Department of Environmental Health Engineering, School of Public Health, Semnan University of Medical Sciences, Semnan, Iran
h
Research Center for Environmental Determinants of Health (RCEDH), Kermanshah University of Medical Sciences, Kermanshah, Iran
i
Environmental Health Research Center, Golestan University of Medical Sciences, Golestan, Iran
j
Council for Nutritional and Environmental Medicine, Mo i Rana, Norway

A R T I C LE I N FO A B S T R A C T

Keywords: Human consumption of fish protein, including canned tuna fish, is increasing steadily worldwide. However,
Food safety there are some concerns about the potential exposure to elevated concentrations of metals in canned tuna fish.
Canned tuna Several studies have been conducted in Iran regarding the concentration of metals in seafood, including copper
Heavy metal (Cu), selenium (Se), iron (Fe), zinc (Zn), mercury (Hg), lead (Pb), chromium (Cr), arsenic (As), nickel (Ni), tin
Systematic review
(Sn), and cadmium (Cd) in canned tuna fish. The main aim of this study was to gather data from existing papers
Risk assessment
and to perform a meta-analysis of the pooled concentrations of metals to evaluate their non-carcinogenic and
Iran
carcinogenic risks in children and adults consumers. Search was conducted retrieving data from the international
biomedical databases with highly public access and consultation, e.g., Web of Science, PubMed, Science Direct,
and Scopus, and national database (SID and Irandoc) between 1983 and November of 2017. Data from 23
articles and 1295 samples were assessed and extracted. The ranking order of metals based on mean con-
centrations (μg/g wet weight) were Fe (13.17) > Zn (9.31) > Se (2.23) > Al (1.8) > Cr (1.63) > Cu
(1.52) > As (0.38) > Ni (0.33) > Pb (0.24) > Cd (0.14) > Hg (0.11) > Sn (0.1). Except for Cd and Se,
concentrations of other metals in the canned tuna fish were lower than the limits recommended by the United
States Environmental Protection Agency (USEPA), World Health Organization (WHO), Food and Agriculture
Organization (FAO) and Iran National Standards Organization (INSO). The minimum and maximum target
hazard quotient (THQ) for adults were 5.55E-5 for Al and 2.23E-08 for Cr. For children, they were 7.23E-05 for
Al and 2.91E-08 for Cr. THQ, and total target hazard quotient (TTHQ) were ≤1.0 for adult and children con-
sumers. The Incremental Lifetime Cancer Risk (ILCR) of As was 3.21E-5 in adults and 4.18E-5 in children. Adults
and children that consume canned tuna fish in Iran are not at non-carcinogenic risk but have a carcinogenic risk
due to As.

1. Introduction human diet and their consumption is increasing all over the world
(Pieniak et al., 2010). Fish consumption reduces chronic non-commu-
Seafood provides a good source of protein, omega-3 fatty acids, nicable diseases such as cardiovascular diseases, psychological dis-
unsaturated fatty acids, vitamins, micro- and macronutrients in the orders, rheumatoid arthritis and some cancers, but it also contributes to

∗
Corresponding author. Department of Environmental Health Engineering, School of Public Health, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
∗∗
Corresponding author. Environmental and Occupational Hazards Control Research Center, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
∗∗∗
Corresponding author. Council for Nutritional and Environmental Medicine, Toften 24, 8610 Mo i Rana, Norway.
E-mail addresses: [email protected] (Y. Fakhri), [email protected] (A. Shahsavani), [email protected] (G. Bjørklund).

https://doi.org/10.1016/j.fct.2018.06.023
Received 25 January 2018; Received in revised form 6 June 2018; Accepted 13 June 2018
Available online 18 June 2018
0278-6915/ © 2018 Elsevier Ltd. All rights reserved.
J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

Fig. 1. Flow diagram showing the search and selection process, following Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.

the normal neuronal development in children (Di Giuseppe et al., 2014; like dementia and dysarthria in the case of Hg (Zahir et al., 2005),
Swanson et al., 2012; Virtanen et al., 2008). cognitive and neurological deficits in the case of Pb (Goyer, 1990); hair
There are several ways to preserved fish such as freezing, smoking, loss and mild nerve damage in the case of Se (Fraga, 2005); cramps and
salting, drying and canning (Jedrychowski et al., 2007). Tuna fish is one nausea in the case of Cu (Fraga, 2005); genetic and metabolic diseases
of the most widely consumed worldwide, in part due to its quality and in the case of Fe (Fraga, 2005); skin and eye irritation in the case of tin
flavor when canned. Consumption of canned tuna in the world, United (Sn) (Winship, 1988), pigmentation and keratosis in the case of arsenic
States, and Iran have been estimated to be as high as 1.0, 1.36 and (As) (Jaishankar et al., 2014), cytotoxicity in the case of Zn (Plum et al.,
1.1 Kg per year per capita in the 2015 (Lee and Chang, 2014; NOAA, 2010), DNA damage(O'Brien et al., 2001), immunologic, neurologic and
2015). carcinogenic problems in the case of nickel (Ni) (Cempel and Nikel,
The primary source of metals in the fish tissue is the marine en- 2006), and aluminium (Al)-induced adynamic bone disease and Al-in-
vironment, polluted by heavy metals and industrial wastes (Fakhri duced osteomalacia in the case of Al (Cannata Andia, 1996).
et al., 2018c). Contamination of aquatic environment originates from Therefore, United States Environmental Protection Agency
natural sources such as metals leak from the Earth's crust and humans (USEPA), Food and Agriculture Organization (FAO), World Health
activities such as industrial discharge, municipal and agricultural Organization (WHO) and the Iran National Standards Organization
wastewater and solid wastes (Domingo et al., 2007). Furthermore, be- (INSO), have established guidelines and standards limits in order to
sides those sources, tuna fish can be contaminated during canning decrease the health risks of metals due to the ingestion of canned tuna
process (Mol, 2011). fish (Iran., 2009; WHO, 2004).
From a nutritional point of view, metals can be divided into es- Although several studies assessed the concentration of metals in
sentials and non-essential. Essential metals such as copper (Cu), sele- canned tuna fish in Iran (Andayesh et al., 2015; Hosseini et al., 2015a,
nium (Se), iron (Fe), chromium (Cr), manganese (Mn), and zinc (Zn), 2015b; Nazari Khorasgani et al., 2017; Pourjafar et al., 2014;
are all crucial for the right metabolism in the human body in trace Sobhanardakani, 2017; Zazouli et al., 2016), no systematic review,
levels. Non-essential metals, such as mercury (Hg), lead (Pb), and meta-analysis and health risk assessment for the consumers has been
cadmium (Cd), lack an essential role in the human body and may cause conducted to date. Therefore, the aims of the present study were to
damage at high concentrations (Ogundiran and Fasakin, 2015; Pirsaheb perform a meta-analysis of all data available to date in order to estimate
et al., 2013; Shahsavani et al., 2017a; Sharafi et al., 2015; Yılmaz et al., mean concentrations of metals in canned tuna fish, compare those mean
2010). Although toxic trace metals are usually present at low con- concentrations with FAO, WHO, USEPA, and national standard limits,
centrations in marine macro-environments, they are particularly dan- estimate current non-carcinogenic and carcinogenic risks in adults and
gerous because of their bioaccumulation and biomagnification proper- children consumers.
ties in the food chain, which can also endanger human health
(Alahabadi et al., 2017; Copat et al., 2018; Dadar et al., 2017; Pirsaheb
et al., 2016; Sadeghi et al., 2015; Shahsavani et al., 2017b). Consuming
foods containing metals may cause serious health hazards such as, renal
dysfunction and cancer in the case of Cd (Godt et al., 2006), Alzheimer

754
J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

2. Materials and method and Al were 0.0003, 0.0004, 0.0003, 0.001, 0.005, 0.0003, 0.3, 1.5,
0.7, 0.04, 0.02 and 0.0004 (mg/kg bw/day), respectively (EPA, 1993,
2.1. Searching strategy 2000a, 2018).

A systematic search was conducted according to PRISMA guideline 2.6. Estimated consumption of canned tuna fish
(Fig. 1) (Moher et al., 2010), in the databases Web of Science, PubMed,
Science Direct, Scopus and the national database SID and Irandoc be- According to the conducted studies by the Iranian fisheries organi-
tween 1983 to November 2017. The MESH-terms used were “metals”, zation, canned tuna fish consumption per capita of Iran was estimated
“heavy metals”, “trace metals”, “canned tuna”, “canned tuna fish”, 4.94 g/n-d (IFOSY, 2015). The consuming seafood's ratio between
“food”, “fish”, “Iran”, alone or combined with “OR” and/or “AND”. The children and adults has been estimated as 39% in Iran (Khoshnood
references to the selected articles were revised to obtain potential ar- et al., 2015). Therefore, FIR for canned tuna fish in children was as-
ticles not included in our search. sumed 1.53 g/n-day.

2.2. Inclusion and exclusion criteria 2.7. Total target hazard quotient (TTHQ)

After an initial screening, all potentially eligible articles were TTHQ is the sum of THQ of the metals (Ghasemidehkordi et al.,
downloaded. Any disagreement between the authors was resolved by 2018; USEPA, 2000a, 2016a), calculated as the summary of all TDH for
dispute and agreement. Inclusion criteria were: (1) Full-text available; every single metal considered in the studies:
(2) Evaluation of any detectable and undetectable (under law limits)
concentration of metals in canned tuna fish; (3) Published full or ab- TTHQ = THQAs +THQPb +THQHg +THQCd +THQSe +THQSn +THQZn-
stract text in the English language; (4) Original observational, epide- + THQCr + THQFe + THQCu + THQNi + THQAl (2)
miological and/or cross-sectional studies with assessed data mining; (5)
Research preferentially performed in Iran. When any of the above cri- 2.8. Estimation of carcinogenic risk
teria were not meet, articles were excluded.
The carcinogenic risk was estimated using the daily intake (EDI).
2.3. Extraction and definitions of data The EDI of As and Pb through the ingestion of canned tuna fish was
estimated by equation (3) (Fathabad et al., 2018; Heshmati et al., 2018;
Data in the articles were extracted and thoroughly checked. Data USEPA, 2000a; c):
from each article included the year of study; year of publication; total
sample size; average concentrations of metals; standard deviation; FIR × C
EDI =
BW (3)
geographical regions of study; and methods of detection.
Where EDI is the estimated daily intake of metals (mg/kg/day); FIR, per
2.4. Meta-analysis of data capita consumption (g/person/day); C, concentrations of metals in
(mg/kg, wet. weight) and BW, body weight (Kg). Since fish fillets
The I2 statistic was used to assess heterogeneity (Higgins and contain ̴79% moisture (ANZFA, 2011), we used this (100–79 = 21%) to
Thompson, 2002), with heterogeneous studies being considered with a convert dry weight (DW) of fillet fish to wet weight (WW), when data
I2 > 50%, as the present study. Therefore, random effects model was was reported in DW [WW =
DW × 100
].
21
used to assess the concentrations of metals in canned tuna fish in Iran The carcinogenic risk of As in canned tuna fish was calculated using
(Kuroki et al., 2017). Standard error for any study was calculated using Incremental Lifetime Cancer Risk (ILCR) and calculated by the equation
standard deviation and sample size (Nair, 1936). Meta-analysis was (4) (Cao et al., 2014; Fakhri et al., 2018b; Sultana et al., 2017):
performed by using Stata software, version 12.0 (Stata Corp, College (4)
ILCR = EDI × SF
Station, TX, USA) (Caldwell et al., 2005; Cipriani et al., 2013; Furukawa
et al., 2016; Salanti et al., 2009). To observe the association between Where, EDI is the estimated daily intake of metals (mg/kg/day); SF,
the concentrations of metals on a time-course, meta-regression analysis slope factor (mg/kg-d)−1 defined as the risk produced by lifetime mean
was used at the moment model (Stanley and Jarrell, 1989). The main dose 1 mg/kg Bw/day (Bamuwamye et al., 2015). SF for As was 1.5
area of distribution and fishery of tuna fish in Iran was the Persian Gulf. (mg/kg-d)−1 (OEHHA, 2009). ILCR is the probability of lifetime health
Therefore, the area of study was not considered a subgroup in our meta- risk from exposure carcinogenic metals.
analysis. Results were considered significant when p-value < 0.05 (i.e.,
α = 0.05). 3. Results and discussion

2.5. Estimate non-carcinogenic risk 3.1. Study characteristics

The non-carcinogenic risk in the consumers of canned tuna fish was From a total of 982 papers identified, 209 were excluded in the first
estimated by Target Hazard Quotient (THQ) (EPA, 2004; Fakhri et al., literature review. According to titles and abstracts, 773 papers were
2018a; IRIS, 2010), by the following equation: identified as probably suitable. Seven hundred and fifty papers were
excluded because of either reporting (1), no original data, (2) hista-
EF × ED × FIR × Cm
THQ = mine, mycotoxins, acid amines, and microbial contamination in canned
RFD × WAB × Ta (1)
tuna fish; or (3) further metals detected in tuna fishes. After evaluating
Where, EF is the frequency of exposure (365 days in year); ED, the ex- for eligibility, 23 papers containing 1295 samples, published between
posure period equivalent to the mean longevity in Iran (i.e., 70 years); 2007 and November 2017, were included in the meta-analysis risk as-
FIR, per capita consumption (g/n-d); Cm, concentrations of metal (mg/ sessment (Fig. 1). Overall, average concentration and standard devia-
kg-d.w); RFD, the oral reference dose (mg/kg/day); WAB, average body tion of 11 metals including As, Pb, Hg, Cd, Se, Sn, Zn, Cr, Fe, Cu, Ni, and
weight (BW); Ta (= EF × ED), exposure time for non-carcinogens (i.e., Al were extracted from 23 papers. Methods of analyzing concentration
70 years). The based on EPA assumptions, mean WAB the children and metals in canned tuna fish included inductively coupled plasma atomic
adults were 15 and 70 kg, respectively (EPA, 2011; EPA, 1989). The emission spectroscopy (ICP-OES), atomic absorption spectroscopy
oral reference dose (RFD) for As, Pb, Hg, Cd, Se, Sn, Zn, Cr, Fe, Cu, Ni, (AAS), polarography, and inductively coupled plasma mass

755
 Table 1
Summary of the studies reporting concentrations of metals found in canned tuna fish.
Year Sample size Metals concentrations (μg/g w.w) Method of Location Ref
study detection
J. Rahmani et al.

Cd SDa Hg SD Pb SD Se SD Sn SD Zn SD Cr SD Fe SD Cu SD Ni SD Al SD As SD

2015 120 0.10 0.04 0.13 0.05 0.75 0.65 2.04 0.43 0.18 0.03 12.61 11.92 ICP-OES Tehran (Sobhanardakani,
2017)
2015 23 1.36 2.79 4.65 20.73 AAS Khuzestan (Nazari
Khorasgani et al.,
2017)
2015 23 0.67 2.23 0.19 0.15 Khuzestan
2015 36 0.05 0.01 0.50 0.01 0.30 0.00 AAS Mazandaran (Zazouli et al.,
2016)
2012 30 0.15 0.12 0.19 0.02 5.77 4.17 AAS Tehran (Hosseini et al.,
2015b)
2012 30 0.07 0.05 0.95 0.88 30.47 29.82 Qazvin
2012 30 0.12 0.09 0.28 0.23 6.77 5.21 Bushehr
2012 30 0.06 0.04 1.59 1.56 7.44 6.11 Tehran
2012 30 2.57 1.87 45.87 11.15 0.91 0.49 0.37 0.12 AAS Tehran (Hosseini et al.,
2015a)
2012 30 3.24 2.35 34.02 9.82 0.73 0.39 0.19 0.12 Qazvin
2012 30 3.16 2.97 77.53 57.22 1.18 0.43 0.14 0.11 Bushehr
2012 30 1.65 1.49 61.30 51.16 0.84 0.61 0.18 0.12 Tehran
2012 15 0.14 0.01 0.03 0.01 0.38 0.04 1.30 0.12 36.40 1.50 1.87 0.10 28.30 1.40 1.67 0.12 1.04 0.10 0.95 0.08 AAS Tehran (Fathabad et al.,
2015)
2012 15 0.08 0.01 0.04 0.01 0.20 0.01 2.62 0.15 18.20 0.90 1.18 0.12 14.90 1.20 2.45 0.10 0.85 0.16 0.49 0.14 Tehran
2012 15 0.05 0.02 0.12 0.02 0.25 0.02 1.87 0.07 9.31 0.60 1.16 0.23 11.20 0.80 1.34 0.10 0.72 0.03 0.71 0.05 Tehran
2012 15 0.21 0.01 0.06 0.02 0.18 0.03 2.71 0.24 8.34 0.45 0.90 0.09 18.40 1.30 1.88 0.12 0.62 0.15 1.12 0.10 Tehran

756
2012 15 0.35 0.02 0.08 0.01 0.24 0.01 3.65 0.35 15.20 1.20 1.54 0.10 13.80 1.50 1.29 0.15 0.58 0.20 2.15 0.12 Tehran
2013 54 0.01 0.02 0.11 0.09 0.05 0.05 0.64 0.26 AAS Tehran (Andayesh et al.,
2015)
2011 18 0.05 0.01 0.01 0.00 0.01 0.00 0.75 0.13 1.30 0.38 0.02 0.01 AAS Alborz (Velayatzadeh
et al., 2014)
2012 54 0.22 0.05 0.05 0.01 0.07 0.02 6.44 0.52 6.93 0.23 0.14 0.03 AAS Khuzestan (Velayatzadeh and
Askari, 2014)
2006 100 0.03 0.02 0.10 0.05 0.00 0.00 2.09 0.99 Polarography Chaharmahal (Rahimi et al.,
and Bakhtiari 2014)
2013 40 0.21 0.15 0.16 0.12 0.08 0.05 0.27 0.40 0.29 0.20 AAS Tabriz (Pourjafar et al.,
2014)
2013 42 0.61 0.38 0.20 0.08 0.50 0.13 ICP-AES Alborz (Davodi et al.,
2014)
2011 21 0.25 0.02 0.04 0.01 0.06 0.01 0.12 0.02 AAS Tehran (Motaghifar et al.,
2013)
2011 16 0.35 0.02 0.21 0.11 0.77 0.36 0.41 0.24 AAS Bandar abbas (Malakootian
& Ahvaz & et al., 2013)
Bushehr
2012 30 0.09 0.00 1.59 0.24 0.14 0.06 NM Tehran (Hosseini et al.,
2013b)
2012 30 0.18 0.01 2.04 0.51 0.17 0.05 Bushehr
2012 30 0.09 0.00 1.89 0.38 0.19 0.08 Qazvin
2012 30 0.14 0.01 2.61 0.60 0.20 0.15 Tehran
2012 70 0.29 0.20 ICP-MS Kerman (Dowlatshahi
et al., 2013)
2011 45 0.15 0.00 AAS Khuzestan (Behzadnia and
and Shiraz Rahimi, 2012)
2009 35 0.02 0.01 0.07 0.04 1.23 0.37 7.31 2.77 6.66 3.19 2.30 0.45 AAS Ahvaz (Zarei et al., 2010)
(continued on next page)
Food and Chemical Toxicology 118 (2018) 753–765
J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

spectrometry (ICP-MS) (Table 1).

(Emami Khansari
(Ganjavi et al.,
(Rahimi et al.,
(Velayatzadeh

(Velayatzadeh
et al., 2010b)

et al., 2010a)

et al., 2005)
3.2. Concentrations of metals in canned tuna fish

2010)

2010)
Mean concentrations and standard deviations (Average ± SD) of
Ref

As, Pb, Hg, Cd, Se, Sn, Zn, Cr, Fe, Cu, Ni and Al obtained in the canned
tuna fish in Iran are presented in Table 1. Our results indicated that the

and bakhtiari
Chaharmahal
Baluchestan

and Isfahan
Sistan and
Khuzestan

ranking from high to low concentration of metals based on mean con-

Hamedan
Location

Isfahan

Tehran

Tehran
centrations (μg/g wet weight) were Fe (13.17) > Zn (9.31) > Se
(2.23) > Al (1.8) > Cr (1.63) > Cu (1.52) > As (0.38) > Ni
(0.33) > Pb (0.24) > Cd (0.14) > Hg (0.11) > Sn (0.1). Similar to
our investigation, studies performed in Argentina, Nigeria, Turkey,
Method of
detection

Brazil, Ghana, Jordan, Portugal, Egypt and united states countries

concentrations of Fe and Zn were higher than other metals (Afonso
AAS

AAS

AAS

AAS

AAS

et al., 2015; Boadi et al., 2011; Çelik and Oehlenschläger, 2007; Griboff
0.08

et al., 2018; Ikem and Egiebor, 2005; Iwegbue, 2015; Massadeh et al.,
SD

2017; Morshdy et al., 2013).

0.13

The variation in metal concentrations found in canned tuna fish

As

might be due to differences in trophic level of tuna fish (Li et al., 2015),
variances in size and age of tuna fish (Merciai et al., 2014), differences
SD

in fishing season (Mendil et al., 2010), and bioaccumulation and bio-

Al

magnification metals in the food chain (Burger and Gochfeld, 2005).

Likewise, it is not possible to ignore possible contamination during the
0.03

0.05
0.03
0.01
SD

processing of canned tuna fish, for example, Fe and Sn can enter the
0.09

0.05
0.17
0.14

foodstuff from the can wall (Sobhanardakani, 2017).

Ni

3.2.1. Arsenic
SD

Arsenic is a potentially toxic and ubiquitous metalloid in the en-

vironment, which originates from natural and anthropogenic sources.
Cu

More than 90% of total human exposure to As is inducted to intake

3.10

4.50
0.04
0.67

seafood (EPA, 1989). The concentrations of As in canned tuna fish of

SD

Iran ranged from 0.13 ± 0.26 to 0.64 ± 0.08 μg/g ww (Andayesh

6.37

4.29
0.76
5.97

et al., 2015; Emami Khansari et al., 2005). Also, the mean concentra-
Fe

tions of As according to our meta-analysis was 0.38 (95%CI:

0.02–0.88 μg/g ww) (Fig. 2). The maximum admitted concentration of
SD

As in the fillet of fish established by USEPA, FAO/WHO, and national

standard limit are 1.3, 0.5 and 1 μg/g ww, respectively (FAO/WHO.,
Cr

2009; Iran, 2009; USEPA., 2000). Mean concentration of As in canned

0.27

4.20
0.82
1.00

tuna fish in Iran were lower than recommended values by USEPA, FAO/
SD

WHO, and INSO. The mean concentrations of As were lower than stu-
0.47

2.84
5.36
4.84

dies performed in the Jordan, South Korea, the United States, and
Zn

Thailand (Ababneh and Al-Momani, 2013; Ikem and Egiebor, 2005;

0.15

0.00
0.01
0.01

Islam et al., 2010; Massadeh et al., 2017) (Fig. 6).

SD

0.42

0.03
0.06
0.08
Sn

3.2.2. Cadmium
Cadmium is a heavy metal that induces severe toxic health effects
SD

even at concentrations lower or equal to 1 μg/g. Its bioaccumulation in

the human body may lead to pulmonary, hepatic, skeletal, reproductive
Se

and renal effects, and even cancer (Ahmed et al., 2015; Saha et al.,
2016). The range of concentrations of Cd in canned tuna fish of Iran was
0.06

0.03

0.02
SD

from 0.01 ± 0.02 to 0.61 ± 0.38 μg/g ww (Andayesh et al., 2015;

Metals concentrations (μg/g w.w)

0.10

0.11

0.04

Davodi et al., 2014). Also, the mean concentrations of Cd according to

Pb

our meta-analysis was 0.14 (95% CI: 0.13–0.16 μg/g ww) (Fig. 2). The
0.00

0.00
0.01
0.01

0.09

0.06

maximum permitted concentration of Cd in the fillet of fish established

SD

by FAO/WHO, and INSO is 0.2 and 0.1 μg/g ww, respectively (FAO/
0.04

0.04
0.05
0.04

0.13

0.01
Hg

WHO., 2009; Iran, 2009). The mean concentrations of Cd were lower

than FAO/WHO but were higher than INSO. The mean concentration of
0.05

0.01
0.05
0.01

0.04

0.00

0.02
a
SD

Cd in Iran was higher than Egypt, United States, Turkey, India, Canada,
0.20

0.14
0.30
0.34

0.05

0.02

0.02

and Italy (Ikem and Egiebor, 2005; Mahalakshmi et al., 2012; Mol,
Standard deviation.
Cd

2011; Morshdy et al., 2013; Russo et al., 2013; Tuzen and Soylak, 2007)
Table 1 (continued)

Sample size

but lower than Jordan (based on mean 2 studies) (Ababneh and Al-
Momani, 2013; Massadeh et al., 2017) and Nigeria (Iwegbue, 2015)
(Fig. 6).
18

18
18
18

60

10

21
study

2007

2007
2007
2007

2009

2009

2003
Year

3.2.3. Aluminum
a

Aluminum is a non-essential metal, and acute and chronic exposures

757
J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

Fig. 2. Meta-analysis on the concentrations of cadmium (Cd), aluminum (Al), arsenic (As), and chromium (Cr) reported in canned tuna fish in Iran (μg/g ww). Study
ID: Study identified and EF: Effect size that in the current study is concentrations of metals.

of Al have several adverse health effects including encephalopathy and respectively (FAO/WHO., 2009; USEPA., 2000). Mean concentration of
may contribute to dialysis dementia, Alzheimer's and Parkinson's dis- Cr in the canned tuna fish in Iran was lower than FAO/WHO and USEPA
eases (Narin et al., 2004). Concentrations of Al in canned tuna fish in standard limits. Mean concentrations of Cr in the canned tuna fish in
Iran ranged from 0.49 ± 0.14 to 2.15 ± 0.12 μg/g ww. Also, the Iran were higher than Jordan, Turkey, Saudi Arabic (Ababneh and Al-
mean concentrations of Al according to our meta-analysis was 1.08 Momani, 2013; Ashraf, 2006; Tuzen and Soylak, 2007) but lower than
(95%CI: 0.63–1.53 μg/g ww) (Fig. 2). The maximum permitted con- Nigeria and United States (Ikem and Egiebor, 2005; Iwegbue, 2015)
centration of Al in the fillet of fish established by FAO/WHO and 15 μg/ (Fig. 6).
g ww, respectively (FAO/WHO., 2009). Mean concentration of Al in
canned tuna fish in Iran were lower than recommended values by FAO/ 3.2.5. Copper
WHO standard limit. The mean concentration of Al in Iran was higher Copper is an essential metal due to its presence in the hemoglobin
than united states and turkey (Islam et al., 2010; Tuzen and Soylak, synthesis and several enzymes (Elvehjem and Hart, 1929; Sivaperumal
2007) but lower than India, Canada and Jordan (Ababneh and Al- et al., 2007; Soylak and Unsal, 2010). Range concentrations of Cu in
Momani, 2013; Mahalakshmi et al., 2012). canned tuna fish of Iran were 0.73 ± 0.39 to 2.45 ± 0.1 μg/g ww
(Fathabad et al., 2015; Hosseini et al., 2015a). Also, the mean con-
3.2.4. Chromium centrations of Cu according to our meta-analysis was 1.52 (95%CI:
Chromium is an essential metal, playing an active role in lipid 1.20–1.84 μg/g ww) (Fig. 3). The maximum permitted concentration of
metabolism and insulin function (da Cunha Leme et al., 2015; Hossain Cu in the fillet of fish established by FAO/WHO 30 μg/kg ww, respec-
and Hasan, 2014), however excessive bioaccumulation of Cr in the tively (FAO/WHO., 2009). The mean concentrations of Cu in canned
human body may cause adverse effects (Türkmen et al., 2008). The tuna fish in Iran was lower than FAO/WHO standard limit. The mean
range of concentrations of Cr in canned tuna fish of Iran was from concentrations of Cu in the canned tuna fish in Iran were higher than
0.67 ± 2.23 to 3.24 ± 2.35 μg/g ww (Hosseini et al., 2015a; Nazari Egypt, United States, Jordan, Brazil, Saudi Arabia, and Nigeria
Khorasgani et al., 2017). Also, the mean concentrations of Cr according (Ababneh and Al-Momani, 2013; Ashraf, 2006; Boufleur et al., 2013;
to our meta-analysis was 1.63 (95%CI: 1.33–1.93 μg/g ww) (Fig. 2). Ikem and Egiebor, 2005; Iwegbue, 2015; Morshdy et al., 2013) but
The maximum permitted concentration of Cr in the fillet of fish estab- lower than Turkey (mean 3 studies) (Çelik and Oehlenschläger, 2007;
lished by FAO/WHO and EPA 1000 μg/kg ww and 8000 μg/kg ww, Mol, 2011; Tuzen and Soylak, 2007) (Fig. 6).

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Fig. 3. Meta-analysis on the concentrations of copper (Cu), iron (Fe), mercury (Hg), and zinc (Zn) reported in canned tuna fish in Iran (μg/g ww). Study ID: Study
identified and EF: Effect size that in the current study is concentrations of metals.

3.2.6. Iron effects including loss of peripheral vision, lack of coordination of

Fish is the main source of Fe and deficiency of this metal causes movements, impairment of speech, hearing, walking, memory loss, and
anemia (Ikem and Egiebor, 2005), yet, as other metals if its intake is muscle weakness (Albores-Garcia et al., 2016; USEPA, 2017). Con-
excessively high can induce toxic effects in the human body (Ashraf centrations of Hg in canned tuna fish of Iran ranged from 0.01 ± 0.01
et al., 2006; Soylak and Unsal, 2010). Ponka et al. (2007) study showed to 0.05 ± 0.01 μg/g ww. Also, the mean concentrations of Hg ac-
that mammals are not able to excrete excess Fe from the body. There- cording to our meta-analysis was 0.11 (95%CI: 0.09–0.13 μg/g ww)
fore, long-term chronic exposure with Fe overload may cause an slow (Fig. 3). The maximum permitted concentration of Hg in the fillet of
and progressive failure of body organs (Ponka et al., 2007). The con- fish established by FAO was 1 μg/g ww; and WHO, 0.5 μg/g ww (FAO/
centrations of Fe in canned tuna fish of Iran ranged from 0.19 ± 0.15 WHO., 2009). The mean concentrations of Hg in canned tuna fish in
to 77.53 ± 57.22 μg/g ww (Hosseini et al., 2015a; Nazari Khorasgani Iran was lower than FAO/WHO standard limits. The mean concentra-
et al., 2017). Also, the mean concentrations of Fe according to our tion of Hg in Iran was similar than in Turkey, South Korea, Thailand,
meta-analysis was 13.17 (95%CI: 11.34–14.99 μg/g ww) (Fig. 3). The and Italy (Islam et al., 2010; Mol, 2011; Russo et al., 2013), but lower
maximum permitted concentration of Fe in the fillet of fish established than Portugal, India, Canada, Jordan, and Ghana (Ababneh and Al-
by FAO/WHO 100 μg/kg ww, respectively (FAO/WHO., 2009). Mean Momani, 2013; Afonso et al., 2015; Boadi et al., 2011; Mahalakshmi
concentrations of Fe in the canned tuna fish in Iran were lower than et al., 2012) (Fig. 6).
FAO/WHO standard limit is established. The mean concentrations of Fe
in the canned tuna fish in Iran were equal to Brazil (Boufleur et al., 3.2.8. Zinc
2013) almost but lower than United States, Turkey (mean 2 studies), Zinc is an essential trace metal for metabolic processes (Bredesen,
Nigeria, and Ghana (Boadi et al., 2011; Ikem and Egiebor, 2005; 2015). However, exposure to excessive levels of Zn can inducted to
Iwegbue, 2015; Mol, 2011; Tuzen and Soylak, 2007) (Fig. 6). deficiencies of Cu and Fe, and its symptoms include nausea, headache,
fever, vomiting, skin irritant, abdominal pain, and tiredness (Fosmire,
3.2.7. Mercury 1990). Range concentrations of Zn in canned tuna fish of Iran were
One of the main uptake pathways of methylmercury in the human 0.47 ± 0.27 to 36.40 ± 1.50 μg/g ww. Also, the mean concentrations
body is by fish and shellfish ingestion. Exposure to Hg can have adverse of Zn according to our meta-analysis was 9.31 (95%CI: 7.05–11.56 μg/g

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Fig. 4. Meta-analysis on the concentrations of nickel (Ni), lead (Pb), tin (Sn), and selenium (Se) reported in canned tuna fish in Iran (μg/g w. w). Study ID: Study
identified and EF: Effect size that in the current study is concentrations of metals.

ww) (Fig. 3). The maximum permitted concentration of Zn in the fillet Iwegbue, 2015; Massadeh et al., 2017; Tuzen and Soylak, 2007)
of fish established by FAO/WHO was 40 μg/g ww (FAO/WHO., 2009). (Fig. 6).
The mean concentration of Zn in the canned tuna fish In Iran was lower
than FAO/WHO is established. The mean concentrations of Zn in Iran 3.2.10. Lead
was higher than Egypt, United States, Jordan, Brazil, and Nigeria Lead is a non-essential metal. Its adverse health effects including the
(Boufleur et al., 2013; Ikem and Egiebor, 2005; Iwegbue, 2015; cardiovascular and renal systems (mainly for adults) and the central
Massadeh et al., 2017; Morshdy et al., 2013) but lower than Turkey nervous system (particularly for children) are well known (Rebelo and
(mean 3 studies) and Ghana (Boadi et al., 2011; Çelik and Caldas, 2016; Sanders et al., 2009). Range concentrations of Pb in
Oehlenschläger, 2007; Mol, 2011; Tuzen and Soylak, 2007) (Fig. 6). canned tuna fish of Iran were 0.04 ± 0.02 to 1.59 ± 1.56 μg/g ww.
Also, the mean concentrations of Pb according to our meta-analysis was
3.2.9. Nickel 0.24 (95%CI: 0.19–0.28 μg/g ww) (Fig. 4). The maximum permitted
The levels of Ni in various environments is very low, however it can concentration of Pb in the fillet of fish established by FAO/WHO, and
still induce adverse health effects including emphysema, fibrosis, lung INSO is 6 and 0.3 μg/g ww, respectively (FAO/WHO., 2009; Iran,
inflammation, and tumors (Denkhaus and Salnikow, 2002; Zhang et al., 2009). The mean concentrations of Pb in the canned tuna fish was
2003). Range concentrations of Ni in canned tuna fish of Iran were lower than FAO/WHO and NLM. The mean concentrations of Pb in the
0.02 ± 0.01 to 1.04 ± 0.10 μg/g ww. Also, the mean concentrations canned tuna fish in Iran was lower than Jordan, Nigeria, and Saudi
of Ni according to our meta-analysis was 0.33 (95%CI: 0.27–0.40 μg/g Arabia (Fig. 6).
ww) (Fig. 4). The maximum permitted concentration of Ni in the fillet
of fish established by FAO/WHO was 0.40 μg/g ww (FAO/WHO., 3.2.11. Tin
2009). The mean concentration of Ni in the canned tuna fish in Iran was Exposure to high concentration of Sn can cause adverse health effect
lower than FAO/WHO standard limit. The mean concentration of Ni in including vomiting, nausea, anemia, diarrhea, alterations in gastro-
the canned tuna fish in Iran was equal to Saudi Arabia almost (Ashraf, intestinal irritation, liver and kidney diseases, as well as eye and skin
2006) but lower than United States, Jordan (mean 2 studies), Turkey, irritation (Ikem and Egiebor, 2005; Winship, 1988). A high con-
and Nigeria (Ababneh and Al-Momani, 2013; Ikem and Egiebor, 2005; centration of Sn in canned fish may be a result of its container because

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J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

Fig. 5. Meta-regression on the concentrations of metals reported in canned tuna fish in Iran. Meta-regression for arsenic (As) and aluminum (Al) were due to the low
number of studies (fewer than three studies) not performed.

Fig. 6. Compare concentrations of metals in canned tuna fish in Iran with other studies in the world.

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J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

Fig. 7. Target hazard quotient (THQ) in the adults (A) and children (B) due to ingestion canned tuna fish content of metals in Iran.

w. w (FAO/WHO., 2009). The mean concentration of Sn in the canned

tuna fish was lower than FAO standard limit, similar to Turkey (Mol,
2011), and lower than Egypt (Morshdy et al., 2013) (Fig. 6).

3.2.12. Selenium
Selenium is an essential trace element in oxidation-reduction pro-
cesses. However, high intake of Se can cause adverse health effects
including brittleness, tooth decay, hair and nail loss, garlic breath odor,
skin lesions, bronchopneumonia, lung edema, nervous system ab-
normalities, and gastrointestinal problems (Rayman, 2000; Yang et al.,
1983). Concentrations of Se in canned tuna fish of Iran ranged from
1.30 ± 0.12 to 3.65 ± 0.35 μg/g ww. Also the mean concentrations of
Se according to our meta-analysis was 2.23 (95%CI: 1.90–2.55 μg/g
ww) (Fig. 4). The maximum permitted concentration of Se in fish fillets
established by FAO/WHO is 2 μg/g ww (FAO/WHO., 2009). The mean
concentration of Se in the canned tuna fish was higher than FAO/WHO
standard limit. The mean concentration of Se in canned tuna fish in Iran
Fig. 8. Total target hazard quotient (TTHQ) in the adults and children due to was lower than turkey (Mol, 2011) but higher than Portugal (Afonso
ingestion canned tuna fish content of metals in Iran. et al., 2015) (Fig. 6).

3.3. Meta-regression of metals in canned tuna fish

As showed in Fig. 5, the concentration of Cr, Cu and Se in the

canned tuna fish in Iran decreased over time, while concentrations of
Fe, Cd, Ni, Sn, and Zn increased (p-values > 0.05). The concentrations
of Pb (C = 0.02, p-value = 0.02) and Hg (C = 0.19, p-value = 0.006)
increased over time significantly (p-value < 0.05). The outcomes of
meta-regression indicated that the concentration of the main metals
analyzed increased over time, especially Fe and Hg (p-value < 0.05).
The meta-regression showed that overall metal contamination of
canned tuna fish in Iran has increased over time. This might be due to
the reported increase in emissions of pollutant in the Persian Gulf and
the Gulf of Oman (Adel et al., 2016a; Saei-Dehkordi et al., 2010).

3.4. Health risk assessment

Although the concentration of metals in canned tuna fish was

Fig. 9. ILCR in the adults and children due to ingestion canned tuna fish con- compared to standard limits, the potential risk depends on several
tent of As in Iran. variables, such as metal toxicity, per capita consumption, body weight,
exposure time, etc. Therefore, to a better interpretation of obtaining
data, non-carcinogenic and carcinogenic risk assessment was performed
of weak lacquering (Hosseini et al., 2013a). Range concentrations of Sn
(OEHHA, 2009; Pepper et al., 2012; Shahsavani et al., 2017b; Storelli,
in canned tuna fish of Iran were 0.01 ± 0.01 to 1.23 ± 0.37 μg/g ww
2008).
Also, the mean concentrations of Sn according to our meta-analysis was
0.1 (95%CI:0.09–0.11 μg/g ww) (Fig. 4). The maximum permitted
concentration of Sn in the fillet of fish established by FAO is 250 μg/g 3.3.1. Non-carcinogenic risk assessment
When THQ of metals is < 1 adverse effects are unlikely to occur,

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J. Rahmani et al. Food and Chemical Toxicology 118 (2018) 753–765

but if THQ is ≥ 1 adverse effects might occur. Also, When TTHQ Shahid Beheshti University of Medical Sciences for the financial grants
is ≥ 10, the health risk is considered high for exposed population of this study (1396/62422).
(Dadar et al., 2017; Fakhri et al., 2017a; Lei et al., 2015). THQ in the
adults consumers induced to As, Pb, Hg, Cd, Se, Sn, Zn, Cr, Fe, Cu, Ni, Transparency document
and Al were 2.60E-05, 1.23E-05,7.53E-06, 2.88E-06, 9.16E-06, 6.85E-
06, 6.38E-07, 2.23E-08,3.87E-07, 7.81E-07, 3.39E-07, and 5.55E-05, Transparency document related to this article can be found online at
and children were 3.39E-05,1.61E-05,9.81E-06,3.75E-06,1.19E- http://dx.doi.org/10.1016/j.fct.2018.06.023.
05,8.92E-06,8.31E-07,2.91E-08,5.04E-07,1.02E-06, 4.42E-07, and
7.23E-05, respectively (Fig. 3). The rank order of metals based on THQ References
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