Next Article in Journal
Positioning System for Fishing Fleets’ Tracking and Assistance
Next Article in Special Issue
Epidemiology of Turbot (Scophthalmus maeoticus) Bacterial Contamination, a Fishery Limiting Factor on the Romanian Black Sea
Previous Article in Journal
Exploring European Eel Anguilla anguilla (L.) Habitat Differences Using Otolith Analysis in Central-Western Mediterranean Rivers and Coastal Lagoons from Sardinia
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Bioaccumulation of Metals in Some Fish Species from the Romanian Danube River: A Review

by
Anca Nicoleta Cordeli (Săvescu)
1,*,
Lucian Oprea
2,3,
Mirela Crețu
1,2,3,4,
Lorena Dediu
1,2,
Marian Tiberiu Coadă
1,2,3 and
Diana-Nicoleta Mînzală
1
1
Faculty of Food Science and Engineering, “Dunărea de Jos” University of Galați, 47 Domnească Street, 800008 Galați, Romania
2
Cross-Border Faculty, “Dunărea de Jos” University of Galați, 800008 Galați, Romania
3
Romanian Center for Modelling Recirculating Aquaculture Systems, “Dunărea de Jos” University of Galați, 800008 Galați, Romania
4
Research-Development Institute for Aquatic Ecology, Fisheries, and Aquaculture, 800211 Galați, Romania
*
Author to whom correspondence should be addressed.
Fishes 2023, 8(8), 387; https://doi.org/10.3390/fishes8080387
Submission received: 11 June 2023 / Revised: 19 July 2023 / Accepted: 23 July 2023 / Published: 26 July 2023
(This article belongs to the Special Issue Recent Advances in Aquaculture Production Technology)

Abstract

:
The Danube is the second-largest river in Europe and has been subject to pollution in the past. Additionally, in the last few years, the rapid pace of industrialization and urbanization has led to the inevitable pollution of this aquatic ecosystem by certain metals (essential and non-essential elements). This issue is considered the central problem of pollution in the Danube and is gaining increasing attention. Fish is a good source of proteins, polyunsaturated fatty acids (especially omega-3 fatty acids), essential vitamins, and minerals. Fish are often exposed to metals present in their aquatic environment through direct contact with contaminated water or by consuming organisms that have accumulated metals in their tissues; therefore, the elevated concentrations of metals in water and sediments are reflected in the fish flesh. In this context, the safety of fish and fishery products for human consumption is a public health concern. In the last two decades, more and more reports have shown that Danube River fish are contaminated with metals, causing great concern among consumers. The negative perception continues, although recent scientific studies show that metal levels in the edible parts of the fish are below acceptable limits. The objective of this study was to put together a multitude of scientific research studies that investigate the levels of some metals in various tissues of some fish species with high economic value in the Romanian market, as well as the levels of metals in the water and sediments. The collected data were then utilized to assess the potential health risks posed to humans.
Key Contribution: This article provides a comprehensive review of data regarding the concentrations of some important metals in the Romanian Danube River water and sediments and the bioaccumulation of these metals in fish tissues. By critically analyzing the available research, this article aims to strengthen the scientific community’s and the general public’s understanding of the magnitude of fish contamination with metals and its potential implications. The conclusion of our study revealed that in the Danube River, the levels of metals detected in fish meat generally remain below the maximum residue limits (MRLs) proposed in the Official Journal of the European Communities (2001). Nevertheless, monitoring metal concentrations in fish meat is necessary, particularly considering its consumption in the human diet.

Graphical Abstract

1. Introduction

The increase in pollution with metals has emerged as a critical environmental concern that has gathered more attention in recent decades. This is primarily due to the alarming levels of metal deposition in various ecosystems and the subsequent detrimental impact on human health and the environment [1,2]. Metals are stable, non-biodegradable, and tend to persist in the environment for prolonged periods [3,4,5]. Once the environmental levels of these metals surpass a certain threshold and accumulate in living organisms, they pose a significant threat to their health and well-being and lead to long-term adverse effects on humans [1,2]. Some metals, such as copper (Cu), zinc (Zn), cobalt (Co), or iron (Fe), are crucial for many biochemical processes in living organisms, being essential elements for aquatic plants and animals [6,7]. Cadmium (Cd), arsenic (As), and lead (Pb) are non-essential elements that can cause harmful effects even at trace concentrations [8].
Anthropogenic sources of metals include fuel combustion, industrial effluents, smelting, mining, the leaching of drill cuttings, and overburden leaching (Figure 1). The metals do not undergo degradation once they enter the water ecosystem; instead, they persist and can accumulate on solid surfaces or interact with aquatic organisms and plants through absorption, dissolution, suspension, or uptake [9,10,11,12,13,14].
Moreover, various fish species can serve as effective biological indicators for assessing the extent of exposure to metals and other pollutants [15,16].

1.1. Effect of Metals on Fish due to Exposure

Metals exert significant influences on fish following exposure. Upon uptake, metals can accumulate in fish tissues and disrupt physiological processes, leading to adverse health effects. Metal-induced pathophysiological changes in fish can include oxidative stress [17], alteration of the hematological profile [18], impaired immune function [19], disruption of ion regulation, and alterations in tissue morphology and cellular function [20].
Accordingly, metals can impair immune function, resulting in decreased resistance to pathogens and heightened susceptibility to infections [21]. Imbalances in ion regulation can modify the body’s homeostasis, resulting in disturbances in both osmoregulation and electrolyte balance. Moreover, metals can induce morphological changes in tissues, such as gill damage and liver abnormalities, while also interfering with cellular functions, including enzyme activity and gene expression [22]. Several other studies have indicated that fish exposed to metals experience a decline in various reproductive parameters, including the gonadosomatic index (GSI), fecundity, hatching rate, fertilization success, abnormal shape of reproductive organs, and ultimately reproductive failure [23,24,25].
Understanding the complex interactions between metals and fish pathophysiology is crucial for comprehending the consequences of metal pollution on aquatic ecosystems and developing effective mitigation strategies.

1.2. Effect of Metals on the Human Population

To safeguard human health, it is crucial to assess the levels of contaminants present in fish meat. Therefore, these pieces of information are important for making informed decisions and implementing measures to minimize human exposure to these contaminants [26,27].
However, the toxicity of the trace metals is correlated with the dose of exposure, pollutant concentration, duration of exposure, the individual’s susceptibility, and other relevant variables. Some studies have provided evidence of the potentially severe complications that can arise from human exposure to high doses of mercury (Hg) and Pb [28]. For example, Hg exposure can have detrimental effects on the nervous system, leading to symptoms such as neurological impairment, cognitive deficits, tremors, and, in severe cases, even paralysis. Prolonged exposure to high levels of Hg has been associated with Minamata disease, a neurological disorder characterized by symptoms such as ataxia, sensory disturbances, and visual impairments [29,30].
Pb exposure, on the other hand, can cause damage to multiple organ systems, including the nervous system, gastrointestinal tract, or kidneys [31,32]. The central nervous system is particularly vulnerable to Pb toxicity, and it can result in developmental delays and cognitive impairments in children. In adults, Pb poisoning can lead to abdominal colic pain, anemia, hypertension, and impaired renal function [33]. Additionally, metal poisoning causes damage to cells of the heart, liver, blood composition, and other important organs [34,35,36].
Consuming fish and seafood contaminated with Cd, Co, Cr, Ni, and Pb can cause neurological disorders, kidney damage, circulatory system problems, and an increased risk of cancer [31].
The target organ effects of inorganic As vary depending on the dose, mode of exposure, and duration of exposure. Consuming high doses (0.04 mg/kg/day) orally, either as a single exposure or repeatedly over weeks or months, can lead to nonspecific effects such as gastrointestinal issues (diarrhea, cramping), hematological effects (anemia, leucopenia), peripheral neuropathy, and cardiovascular effects. While these effects are generally reversible, they can cause permanent damage to the affected organ systems. Chronic exposure to small doses of As (0.01 mg/kg/day or higher) through inhalation or oral ingestion for 3 to 5 years can result in skin hyper-pigmentation (diffuse or spotted) and, over time, benign skin lesions (hyperkeratosis) and skin cancer. Prolonged exposure can also lead to liver disease, as indicated by abnormal porphyrin metabolism [37].
Cd, particularly in its inorganic form, can have various health effects; acute effects from oral exposure to Cd are uncommon [38]. Long-term exposure to low doses of Cd over several years can result in kidney tubular dysfunction and osteoporosis in susceptible populations, particularly elderly women with Fe deficiency [37,39].
Exposure to inorganic Pb compounds can have adverse effects on multiple organ systems. Infants and young children, particularly during the neonatal period and early childhood, are highly susceptible to lead exposure and may experience impaired motor function and cognitive development, along with the possibility of developing anemia. Chronic exposure to high levels of Pb in older children can also lead to anemia as well as central nervous system effects such as impaired motor function and cognitive function, and in severe cases, seizures, coma, and even death, especially when blood Pb levels exceed 80 μg/dL [37]. In adults, elevated blood Pb levels above 40 μg/dL can result in impaired heme synthesis and chronic kidney disease, while sustained levels above 80 μg/dL can lead to lethargy and cognitive impairment. Epidemiological studies indicate a slight dose-effect relationship between Pb exposure and blood pressure, with blood levels up to 30 to 40 μg/dL. Although Pb has been found to cause tumors in experimental animals, there is currently insufficient evidence to classify Pb as a human carcinogen [40,41].
Hg exists in three forms that are of toxicological concern: elemental Hg, inorganic Hg, and methyl Hg. The target organs affected by Hg exposure vary depending on the specific form. The central nervous system and the kidneys are the primary target organs for elemental Hg toxicity. Renal toxicity from elemental Hg exposure may involve an immunological mechanism that can lead to glomerulonephritis, potentially progressing to renal failure [37]. Methyl Hg exposure occurs through the consumption of fish that have accumulated methyl Hg in the aquatic food chain. The brain is the primary target organ in the case of methyl Hg exposure. The most vulnerable population is the developing fetus. Methyl Hg easily crosses the placenta, exposing the developing brain to its toxicity. Even low levels of exposure can result in impaired motor and language skill development during neonatal life and early childhood. Higher exposures can cause severe cognitive effects, including paresthesia, blindness, deafness, and, in the most severe cases, fetal death and abortion. Methyl Hg in the brain slowly transforms into inorganic Hg, raising questions about whether the actual toxic species of Hg in the brain is methyl Hg, inorganic Hg, or elemental Hg [41,42].
Human activities in the past centuries have left metal contamination in terrestrial and aquatic ecosystems [43]. Because of this historical metal contamination, metal concentrations in sediments and surface waters can remain above natural levels and potentially threaten the health of aquatic ecosystems [44,45,46].
In order to ensure the preservation of a healthy ecosystem for both food security and human safety, it is crucial to thoroughly investigate the negative consequences of heavy metal exposure on fish, which can ultimately impact humans. In this context, the objective of our research was to gather relevant information regarding nine different metals (Cd, Cu, Cr, Fe, Hg, Ni, Pb, and Zn) and the metalloid As in both water and sediment samples, as well as to overview the bioaccumulation of these metals in various organs (such as the gills, liver, kidneys, digestive tract, and muscles) of some fish species with high economic value in Romania. By comprehensively examining these factors, we can gain a better understanding of the potential risks associated with metal contamination and make informed decisions to mitigate their detrimental effects.

2. Materials and Methods

The Danube is the second-longest river in Europe, with a total length of 2826 km. Because of the very different geographical regions through which it flows as well as the different hydrobiological characteristics along its course, the Danube is divided into three sectors: the Upper Danube (Alpine sector) from its sources to Bratislava, with a length of 1021 km; the Middle Danube (Pannonian sector), running between Bratislava and Baziaş, with a length of 764 km; and the Lower Danube (Carpathian-Balkan sector) between Baziaş and the Black Sea, with a length of 1075 km [47].
The Romanian Danube is divided into five sectors: the Carpathian sector between Baziaş (km 1075) and Drobeta Turnu Severin (km 931); the upstream sector of Iron Gate II (km 862) to Calafat (km 795); the sector between Calafat (km 795) and Călăraşi (km 370); the sector between Călăraşi (km 370) and Brăila (km 170); and the sector between Brăila (km 170) and the Black Sea [47] (Figure 2).
In this paper, we have conducted a comprehensive review of published research focusing on the Pannonian sector of the Danube and the Romanian section. We aimed to provide an overview of the metal levels found in water, sediments, and some fish species within these regions, from entering Romania to reaching the Black Sea.
Taking into account the subdivision of the lower course of the Danube and the Pannonian sector, we have named five sectors of investigation: sector I includes the km from Bratislava to the entrance to Romania, sector II from Baziaş to the Iron Gate, sector III to Călăraşi, sector IV to Brăila, and sector V from Brăila to the Black Sea.
Our study is based on a systematic search of the Web of Science (Clarivate Analytics), Google Scholar, and ResearchGate for articles published between 1950 and 2023. We focused on selected metals, using keywords such as “metals in the Danube”, “bioaccumulation in commercial fish”, and “Danube pollutants”. Publications that included seasonal monitoring, the same sampling sites in different years, and various locations in the same period were taken into account to ensure a comprehensive perspective.
The assessment and interpretation of metal concentrations in the Danube were conducted based on the findings of previous studies [3,4,5,48,49] and international treaties and agreements such as the International Convention for the Protection of the Danube River [50] (Table 1).
Water quality indices are valuable tools for assessing the quality of water. Their origins can be traced back to 1965, when Horton introduced the initial version of the Water Quality Index (WQI). Based on the WQI value, surface water can be classified into five quality classes, as described in Table 2 [51].
The metal profile in the sediments of the Danube River has a particular configuration. Table 3 presents the standard values of some metal concentrations in the sediment according to Romanian Order 161/2006 [50].
The consumption of fish meat significantly influences the risk of metal accumulation in humans.
In order to assess the levels of metals in fish and compare them with the maximum allowable concentrations (MACs) established by the European Union [52], the Food and Agriculture Organization of the United Nations [53], and national legislation [54] for safe consumption of fish meat by humans, the concentrations are expressed in milligrams per kilogram (mg/kg) of wet tissue weight (WW). This enables a comprehensive evaluation of the potential risks associated with the presence of these substances in fish destined for human consumption.
The maximum limits for metals in fish muscle (mg/kg) according to international standards are listed in Table 4. The comparison of metal concentrations in fish was also carried out according to the guidelines of the Council of Ministers of the Environment of Romania (Decree No. 356/2001), with maximum limits for metal accumulation in fish tissue (fillets) of 0.2 mg/kg for Pb and 0.05 mg/kg for Cd, but these guidelines exclude Zn and Cu.
According to EU regulations, the maximum allowable Cd content in fish muscle is 0.05 mg/kg body weight, except in certain marine animals, because Cd is an element that can cause chronic poisoning at a minimum concentration of 1 mg/kg [56]. The literature indicates that Cd concentrations in freshwater fish range from 0.002 g/g in farmed carp to 0.011 g/g in wild fish. The primary source of Cd exposure is the food supply, i.e., highly contaminated fish and fish products. Higher Cd concentrations lead to kidney failure and lung cancer [57,58]. For Pb, fish meat’s maximum allowable concentration (MAC) is 0.3 mg/kg body weight. The limit for Zn recommended by the FAO of the United Nations is 30 mg/kg body weight [59]. According to FAO 1983, Heavy Metals Regulations Legal Notice No. 66/2003, and European Commission Regulation EC No. 1881/2006, the established limit for Hg is 0.5 mg/kg [55].

3. Results

Factors affecting metal concentration and accumulation in aquatic organisms include metal bioavailability, sampling season, environmental hydrodynamics, size, sex, tissue composition, reproductive cycle [60], and dietary habits [61]. As metabolically active organs, the liver and gills are the target organs for metal accumulation [62], while accumulation in muscle tissue is lower [63,64,65].
Fish species have different levels of metals in their tissues (muscle, liver, or digestive tract). Pollutants can enter fish through five pathways: feed, non-food particles, gills, oral intake, and skin [66].
Numerous research results show that the distribution of these contaminants depends on the affinity of fish tissues for metals, the degree of uptake and accumulation, and the ability of the organism to excrete them. A major problem with metals is their long biological half-life in living organisms [67]. Accumulated metal concentrations were higher in the gills, liver, and kidneys but lower in muscles, consistent with the essential functions of these tissues. The accumulation of metals in fish tissues, resulting from environmental pollution, poses a potential risk to human health due to their toxic effects on various organ systems. Given the worldwide consumption of fish as a protein source, the ingestion of contaminated fish can lead to adverse health effects associated with metal toxicity [6].

3.1. Sediments

To provide a comprehensive overview of the presence of selected metals in sediments, we have analyzed each sector of the Danube River (Table 5). Following the analyzed scientific works, the maximum concentration of non-essential elements reported in the Pannonian sector of the Danube was declared in 2004 [3] for As (14.73 mg/kg), Cd (4.03 mg/kg), Hg (0.30 mg/kg), and Pb (43.6 mg/kg). Similarly, the study [68] stated higher concentrations of metals in the sediments collected in 2013, with Hg and Pb values of 0.8 ± 0.09 mg/kg and 64.92 ± 2.39 mg/kg, respectively, from the Belgrade Region of the Danube River, near Vinča in Grocka. Additionally, in the same studies in this sector, the tendency to accumulate more essential elements was observed in the last decade compared to the previous twenty years.
At the entrance of the Danube to Romania, in terms of As and Cr concentrations, they have increased in the last two decades from 12.68 mg/kg in 2002 [3] to a value of 17.8 mg/kg in 2022 [69] for As, while for Cr, the values increased from 105.9 mg/kg [48] to 183 mg/kg in 2022 [69].
Concerning the concentrations of metals and metalloids in the sediments collected in the sector between Iron Gate and Călăraşi, As concentrations registered values between 7.3 and 12.9 mg/kg [70]. Milenkovic et al. [3] reported, for the same sector, lower values for As concentrations (3.16 mg/kg). Additionally, in the same study, higher values of Cd, Cr, Cu, Hg, Ni, Pb, and Zn were recorded compared to those found in the SIMONA Project [70]. Regarding the Fe concentrations, the studied articles provided no records for the last two decades.
Table 5. The values of metal concentrations in the sediment (mg/kg).
Table 5. The values of metal concentrations in the sediment (mg/kg).
YearsAsCdCrCuFeHgNiPbZnRef.
Sector I20025.082.8451.823.9-0.1846.8--[3]
14.734.03112.536.8-0.3116.4--
20128.90.61-35.9516,1040.69-32.58139.4[66]
201313.891.69-50.9317,5300.8-64.92270.4[68]
Sector II200212.683.2105.941-0.2799.940.9389.5[3]
3.153.796845.3-0.1969.925.8285.7
9.242.9893.357.6-0.2374.543.6307.8
2020----15.36----[71]
202217.8-18356--97-328[69]
Sector III20023.162.1271.131.6-0.1959.228197.5[3]
0.992.9130.617.8-<0.0623.72.8549.4
20207.3–8160–9612.9–29.4-0.04–0.00538.6–21.415.3–17.959.2–59.7[70]
8.49–12.90.24–0.364–65.923.3–29.2-0.16–0.2537.4–38.414.2–18.460–78.8
-0.27–0.459.4–74.926.3–29.8-0.05–0.0632.4–39--
Sector IV2011–2017-0.3838.9435.18--37.920.294.91[72]
--42.2838.56--33.83-98.37[73]
--42.7727.27--32.54-95.63
--44.7238.76--40.11-103.39
--40.4640.98--35.83-105.46
--33.1234.39--34.73-100.85
--36.6926.43--32.46-95.72
--37.4231.61--35.1-98.71
--32.131.42--34.6-106.35
--27.1224.85--32.26-89.33
--30.4727.73--27.48-88.87
--28.8330.69--30.4-97.55
--29.7734.12--34.08-103.9
--32.1635.96--34.28-104.72
--24.8930.03--33.89-92.85
--43.7626.16--33.49-89.83
--41.7125.58--31.7-83.99
-0.43429.4434.24--36.5214.45104.3[74]
-0.36830.6432.17--35.9314.4798.3
-0.39633.5533.23--42.1816.94112
-0.40129.831.93--34.4117.37101
2018-0.3-4.3--16.035.958.84[50]
2019-0.59-10.31--20.176.0278.69
20205.5–7.68-30–41.728.9–52.2-0.067–0.132.1–47.720.1–26.970.1–102[70]
Sector V1950-<0.55038--563690[75]
1995–1997-0.5–1018–1012.0–51.0--6.0–785.0–686–119[76]
2003–2009-<0.5–1.57.5–61.914.8–194--19–1117.5–51.329.8–218[77]
-0.115–1.920–1243.5–94--11–72.01.0–7317–202[76]
2007–2012-6.12–8.2688.1–134.2---54.6–79.17.16–13.99164.2–204.7[78]
-4.16–7.8167.2–93.1---31.2–67.16.22–7.61131.2–171.2
-4.97–7.8871.5–117.6---48.1–69.16.81–7.89158.2–187.5
-4.26–6.8144.9–58.6---33.3–54.67.14–12.2148.2–197.9
-2.12–4.9229.4–47.9---27.1–465.18–7.31122.1–168.3
-3.47–4.9938.5–52.4---28.3–49.56.02–8.99139.1–178.5
2012–2013-BDL7.62–32.54.65–45.9--10.8–49.84.76–41.317.7–93.1[53]
-0.59-10.72--29.128.96118.54[50]
-0.74-17.39--27.8812.57120.76
-0.5-12.58 22.318.4987.43
-0.5-12.54--20.537.9384.15
-0.46-7.6--145.1762.39
-0.57-11.81--19.997.2884.65
-0.54-10.24--22.0921.1477.64
-0.54-7.89--16.284.8464.48
-0.76-13.42--23.97.55146.23
-0.53-6.68--24.837.8385.4
-0.63-9.79--24.766.8496.11
-0.75-16.64--28.358.29121.38
-0.57-15.17--38.818.11117.01
-0.53-9.42--16.945.3469.97
2019-0.65-11.65--19.336.0584.21
-0.99-25.01--35.813.78177.33
-0.63-8.97--16.046.4173.57
-0.57-10.08--24.585.795.67
-0.41-7.55--19.094.1771.27
-0.46-7.47--17.655.6863.21
-0.78-19.47--28.4910.35131.5
-0.46-9.29--17.44.3166.06
-0.65-17.18--27.418.33121.05
-0.72-27.5--50.4614.64161.24
-0.77-20.75--32.559.87146.53
-0.82-23.29--39.039.9154.34
-0.48-9.29--25.856.7681.26
-0.52-10.07--28.138.0186.43
Sector IV, from Călăraşi to Brăila, was covered by studies starting in 2011, making it difficult to obtain an overview of the entire period before Order 161/2006. From 2011 to 2020, the levels of Cd remained relatively consistent, with readings ranging between 0.3 mg/kg [50] and 0.59 mg/kg [50]. According to national standards, these readings were discovered to be lower than the maximum permissible limits.
Also, some authors reported Cu concentrations in the sediments ranging from 26.16 to 40.98 mg/kg for this sector, which falls within the acceptable limits set by national regulations [50,70,73,74]. However, there were a few exceptions to this trend, in particular the minimum value of 4.3 mg/kg [50] and the maximum value of 52.2 [70]. The value of 52.2 mg/kg exceeded the allowable limits, according to international standards.
The Pb values achieved in 2011–2020 are identified as being lower than the 85 mg/kg limit. Regarding Ni, the concentrations have significantly increased over time; the maximum value that exceeded the allowed limit was declared in 2020 [70].
No specific study was identified that reported concentrations of Zn exceeding the permissible limit of 150 mg/kg. The highest value of Zn (106.35 mg/kg) was observed between 2011 and 2017, as reported by [73].
The studies on the last sector of the Romanian Danube, from Brăila to the Black Sea, spanned a more extensive timeframe from 1950 to 2019. As per the records examined in the relevant articles, it was found that most of the concentrations identified in the studies were within the acceptable limit. However, the values reported between 2005 and 2012 exceeded the permissible limits in most cases [58], while other researchers reported acceptable levels of metals [50,53,75,76,77].
The concentration of metals (Zn, Hg, and Cu) increased until 1989 due to industrialization in Central and Eastern Europe [52], including Romania. However, in the last five decades, a decrease in metal concentrations has been observed in the Danube River due to the management of intensive agricultural programs, which has led to a decline in Cd concentrations as this compound is a component of fertilizers [53].

3.2. Water

Between 2007 and 2021, several authors conducted analyses of metal levels in the Danube water, both upstream of the Baziaş entry point and in the sections before Brăila leading to the Black Sea. The results indicated that the Danube contained acceptable levels of essential and non-essential elements, which met the water quality criteria outlined in Class I of the national standards (Table 6).
After passing through ten countries and being subjected to agricultural pollution, industrial pollution, and human impact, the Danube flows into the Black Sea. The metal concentrations in this region showed significant variations, but the water quality was classified as Class II (indicating a good ecological status) [78,79]. The only exception was Zn, where excessive levels were detected in most cases.
Table 6. The value of each metal concentration in the water (mg/L).
Table 6. The value of each metal concentration in the water (mg/L).
YearsAsCdCrCuFeHgNiPbZnRef.
Sector I20120.004ND-0.0040.33ND-ND0.032[66]
20130.006ND-0.0040.41ND-ND0.063[68]
2011–20130.0010.000040.0020.0060.260.00010.00140.00060.02[80]
0.00060.000020.0090.0060.210.00010.0030.00050.02
2010–2012-0.002-1.8----1.82[81]
---3.17----1.35
-0.008-1.46---2.760.78
20200.090.004--0.7660.011-0.2121.4[71]
0.120.009--0.8210.017-0.2418.5
0.120.008--0.6850.012-0.2820.1
0.140.012--0.8010.014-0.2118.5
0.10.014--0.8040.011-0.2117.9
0.110.008--0.7920.009-0.2219.1
0.090.011--0.8030.01-0.2219.7
0.110.042--0.9110.009-0.2219.4
0.140.088--2.1930.015-0.3118.1
2011–20130.0020.000020.0070.0060.080.000010.00090.00050.009[80]
Sector IV2010-18.4-112.3---21.4447.14[82]
--1.134.14--2.78-12.5[73]
--1.094.12--2.5-11.95
--1.124.18--2.44-12.18
--1.214.79--2.6-13.14
--0.773.52--1.75-15.62
--0.713.49--1.76-15.94
--0.643.92--1.96-16.4
--0.633.26--1.7-15.12
--0.613.43--1.84-16.07
--0.633.14--1.63-14.03
--0.693.27--1.9-15.76
--0.643.29--1.62-15.11
--0.523.06--1.78-15.76
--0.63.51--1.61-16.45
--1.135.2--2.57-11.28
--0.934.03--2.38-10.6
-0.0670.7183.1--1.820.78423[74]
-0.0670.893.31--1.940.78122.1
-0.0650.8673.2--1.740.88423.7
-0.0630.8483.26--1.70.91723.3
Sector V2007–2012-6.62–10.543.1–81.2---49.6–78.97.76–11.2161.2–209.8[78]
-4.26–8.4131.0–64.2---41.2–59.16.11–7.52138.2–188.7
-6.26–8.4135.2–73.1---43.4–71.26.83–8.91146.9–179.6
-4.71–8.4630.1–48.2---40–59.16.81–8.96124.5–181.9
-3.5–6.4620.6–37.0---27.9–46.66.24–7.21100.2–164.0
-3.6–7.3229.4–44.6---36.2–52.86.23–7.81117.7–179.3
-8.381.24---86.1842.61333.78[79]
-7.1126---104.2821.39144.56
-7.828.59---67.9724.33230.59
-5.8256.8---64.059.29175.95
-8.6772.56---38.1648.04249.58
-6.3332.67---31.6734.67124.5
-6.2747.67---27.1536.02165.54
-5.828.65---47.98.23167.95
-9.1371.81---41.132.52310.79
-9.3335---89.6728.22178.89
-7.6947.67---39.529.35187.15
-9.2629.4---35.856.81128.35
-10.4755.39---98.5535.99312.02
-9.556.67---92.3311.33197.33
-10.0961.27---88.8223.21182.27
-6.656.23---48.77.31125.58
-11.0573.12---54.9539.37209.12
-847.33---41.1717172
-7.2841.72---85.3832.11161.4
-4.2158.5---47.86.93150.6
-15.7-93.5---14.3132.58[82]
20.21.4--0.2121.61.2[83]
2.10.191.3--0.222.11.51.3
1.90.211.2--0.22.31.761.1
2.20.055---0.22.11.51.2
2.40.056---0.162.11.51.3
2.30.054---0.182.31.51.1
2.90.28---0.221.5-
2.80.11---0.162.11.5-
2.70.21---0.182.31.5-
2018-0.243-5.7722.65-7.23.6716.27[84]
-0.158-9.591244.7-5.652.7638.9
-0.4<1.3<1–2.9--<1<0.75<2.1–14.9[85]
2020-0.4–0.9<1.30.9–1.3--<1–1.2<0.75<2.1–6.3
2021-0.4–0.8<1.30.9–2.8--0.9–1.8<0.75–1.13.3–11.6
ND—not detected.

3.3. Fish Tissues

The accumulation of metals in different tissues varies depending on their physiological functions. Fish gills and digestive tracts have a high capacity for metal accumulation, with levels influenced by the concentrations of metals in the water and food. In comparison, muscle tissue accumulates lower levels of metals and is commonly used to assess water pollution and associated health risks related to fish consumption [86].
Gills are important entry points for essential elements, such as Cu, Zn, Se, Mn, and Fe, and non-essential elements, including Al, As, Cd, Cr, and Pb [87]. Furthermore, the analysis of gills can be utilized to evaluate bioaccumulation levels. For example, the carp gills can accurately reflect metal pollutants in water, as the negatively charged gill attracts positively charged metal species in water [87,88,89,90]. Therefore, monitoring metal content in carp gills can be important for assessing water quality and potential risks to public health.
However, some studies on common carp showed that Pb, Cd, and As concentrations in the digestive tract and liver were higher than in muscle [68].
The liver and kidney are commonly studied in bioaccumulation research [91,92]. It is important to note that the liver is a vital organ responsible for detoxification and is particularly prone to metal accumulation [54].
Studies conducted on various fish species have shown that elements accumulate mainly in metabolic organs such as the liver, which produces metal-binding proteins [93] (Table 7).
Lenhardt et al. conducted studies on the levels of metals and trace elements in the tissues of freshwater fish in the Danube River and found that carp had higher levels of Zn in their liver, muscle, and gill samples than catfish, while catfish had higher levels of Mn in their gill samples than carp [96]. These differences in metal bioaccumulation between the two species could be due to their feeding habits, physiology, and habitat variations.
Overall, the results confirm the differences in elemental accumulation in different tissues. The highest concentrations of Cu, Fe, Mn, and Zn were found in the liver, which agrees with other studies [112,113,114,115,116,117].
On the other hand, Hg concentrations are highest in muscles [116,117,118]. Muscle is not an active tissue for element accumulation, as reported in many studies [112,119,120]. For example, Figure 3 shows the bioaccumulation trends of As, Cd, and Pb in the muscle tissues of certain fish species upon their entry into the river sector of Romania (2010–2013).
Metal accumulation was lower in muscle than in other fish organs such as the gills, skin, and liver [121]. Although muscle tissue may not always accurately measure metal contamination in fish, it remains a crucial concern as it is part of the fish most commonly consumed by humans.
Lower Cu, Fe, manganese, and Zn concentrations in muscle tissue may be due to lower amounts of binding proteins in muscle tissue [122].
Compared to other species, the lower Hg concentration in carp muscle tissue can be attributed to biomagnification in the food chain [123]. This means that as Hg travels up the food chain, it accumulates in higher concentrations in the bodies of organisms at higher trophic levels.
In Figure 4, the analysis of muscle tissue samples taken from Freshwater bream (Abramis brama), Wels catfish (Silurus glanis), and Pike-perch (Sander lucioperca) collected from sectors I and II reveals some noteworthy findings. Although all values for As, Cr, Cu, and Pb fall within acceptable limits, the Abramis brama samples exhibit relatively higher concentrations than the other species. Conversely, regarding Hg and Pb, the muscle tissue samples from Sander lucioperca demonstrate slightly elevated levels, which still meet acceptable standards. Notably, the samples taken from Silurus glanis in sector I exhibit the highest values for Fe and Zn, measuring 19.46 mg/kg and 19.62 mg/kg, respectively.
Metal contamination in fish tissue has been linked to various health issues, including neurological problems, kidney damage, and cancer [124]. Thus, to ensure the safety of fish as a food source and to protect public health, regular monitoring of metal content in fish tissue is crucial [125,126]. Moreover, it is essential to note that the level of metal contamination can vary significantly depending on the fish’s species, age, location, and type of metal involved. Therefore, a comprehensive and continuous monitoring system is necessary to identify potential risks and ensure the safety of fish consumption.

4. Discussion

Several industrial accidents in the Romanian Carpathian region, where there is a long mining tradition, especially for gold, silver, Pb, Zn, Cu, Cd, and Mn, have led to pollution of the Danube River [127,128]. Toxic elements such as As, Cd, Hg, and Pb, as well as essential trace elements such as Ca, Co, Cu, Fe, Mn, molybdenum (Mo), nickel (Ni), selenium (Se), and Zn, are toxic to organisms at high concentrations, according to Barlas [129] and Lopez Alosno et al. [130].
While some of these elements are essential for human metabolism [131], they can be divided into potentially toxic (aluminum (Al), As, Cd, Pb, Hg, etc.), possibly essential (Ni, vanadium, and Co), and elemental (Cu, Zn, and Se) [132,133]. When metals are ingested through long-term food consumption, they can accumulate in the body, causing damage to the liver (hepatotoxicity), kidneys (nephrotoxicity), central nervous system (neurotoxicity), and DNA (genotoxicity) [134,135]. Metals have unique physicochemical properties and exhibit variable tissue distribution and bioaccumulation in fish [136,137].
Fish that contain metals can cause serious health problems, such as developmental disorders, neurological disorders, liver and kidney damage, reproductive and hematological effects, cancer, and cardiovascular disease, if the exposure concentrations are exceeded [138,139,140,141,142,143,144,145]. As a result, many researchers have recently focused on the potential risk posed by contaminated fish to consumers health.
Studies conducted by Jarup [146] and Ko [147] have indicated that consuming fish containing elevated levels of metals, including Hg, Cd, As, and Pb, can potentially result in severe skin diseases and autism in children. The disparity in metal exposure may be attributed to variations in dietary habits, with coastal populations consuming more fish than inland populations.
While chromium and Cu are essential for good health, excessive intake can lead to liver and kidney damage. The hexavalent form of chromium is toxic when ingested and has been classified as carcinogenic by the International Agency for Research on Cancer (IARC). The maximum allowable Fe content in fish, as determined by [59], is set at 100 mg/g. Ni is a significant pollutant in aquatic environments, and its toxicity can cause respiratory cancer and harm the immune and reproductive systems.
From 2008 to 2013, a study conducted on fish species such as Common carp (Cyprinus carpio), Crucian carp (Carassius carassius), Silver carp (Hypophthalmichthys molitrix), Wels catfish (Silurus glanis), and Barbel (Barbus barbus), specifically in sector I, revealed a significant accumulation of Cd, particularly in the muscle tissue. Furthermore, in sectors closer to the point where the Danube River flows into the Black Sea, Cd levels exceeded the optimal accepted threshold between 2007 and 2010. This excessive Cd content was observed not only in the muscle tissue but also in the liver and gonads of the fish.
The elevated concentrations of Cd in the samples of fish in sector I could be caused by the sediment samples, which displayed increased metal values collected between 2002 and 2013 [3,66].
Secondly, fish belonging to the Cyprinidae family, such as Common carp (Cyprinus carpio) and Crucian carp (Carassius carassius), primarily consume phytoplankton during the fry period. As phytoplankton can accumulate Cd, it is plausible that the phytoplanktonophagous nature of these stages of carps led to higher Cd levels in their tissues. The Common carp (Cyprinus carpio) is an omnivorous fish that feeds on various food sources, including detritus, chironomids, mollusks, amphipods, zooplankton, and epiphytes [48].
Moreover, fish species such as catfish and barbel, which spend a significant part of their lives dwelling at the bottom of the water, near the shore, and in the sand, exhibited Cd concentrations exceeding the accepted level. This behavior makes them more susceptible to contact with sediments and substances, including Cd, in these environments.
It is worth noting that all other samples detailed in Table 6 showed Cd concentrations below the accepted level, indicating that the bioaccumulation of Cd was predominantly observed in the fish species mentioned above and in specific areas rather than being a widespread issue across all samples.
Between 2010 and 2014, studies reported increased accumulation of Cu in liver samples obtained from Common carp (Cyprinus carpio), Freshwater bream (Abramis brama), and Silver carp (Hypophthalmichthys molitrix) samples in sector I [96,97,103]. Additionally, elevated Cu levels were observed in Silurus glanis gonads during 2010 in the same sector. Surprisingly, these accumulations cannot directly correlate with the Cu values measured in water and sediments from the corresponding study area.
Despite the lack of a clear correlation between Cu bioaccumulation in fish tissues and the Cu levels found in water and sediments, several factors could contribute to this disparity. Various complex interactions within the aquatic environment may influence Cu accumulation in fish organs. Factors such as the bioavailability and speciation of Cu in the water column and the fish species’ physiology and dietary habits may play significant roles in the differential accumulation patterns observed.
Moreover, variations in the exposure routes and uptake mechanisms of Cu can also contribute to the mismatch between tissue and environmental Cu levels. The fish species studied, including Common carp (Cyprinus carpio), Freshwater bream (Abramis brama), and Wels catfish (Silurus glanis), may exhibit unique physiological and metabolic processes that lead to differential Cu accumulation in their livers and gonads. Additionally, the timing and duration of exposure to Cu in the aquatic environment may further complicate the relationship between environmental Cu concentrations and fish tissue accumulation.
It is essential to consider these complexities and explore additional factors that could influence Cu accumulation in fish tissues, such as other contaminants, inter-species differences in metabolism, and potential interactions between Cu and other trace elements. Further research is necessary to fully understand the mechanisms underlying the observed variations in Cu accumulation in the studied fish species and to ascertain the factors driving these disparities between tissue and environmental concentrations.
Based on the examination of three data consolidation tables obtained from the specialized literature, it is possible to postulate various correlations between elevated metal levels in water and sediments and their presence in the muscle tissue of various fish species.
In the case of the species Cyprinus carpio, the slightly elevated Cd values (0.059 and 0.082) reported in the year 2013 [94] can be attributed to the increased Cd levels found in the sediments within the same study area and year (1.69) [68]. Similarly, high Cd values were observed in sector 1 in 2013 for Carassius carassius (0.057 and 0.051) and Silurul glanis, as documented in the aforementioned study [94].
Pb, due to its lipophilic properties, can be readily absorbed by fish into their blood and bones. Omnivorous fish are more likely to accumulate metals than pelagic species due to the higher metal concentrations in sediment than in the water column [148]. This diverse diet may contribute to their high bioaccumulation of Pb.
The analysis of fish muscle samples from Cyprinus carpio and Alosa immaculata species obtained from sectors IV and V revealed elevated Pb levels, as reported in 2008 [98]. These higher Pb concentrations in the fish muscles could potentially be associated with the increased values found in water samples, as indicated by Burada in their articles from 2014 and 2015, covering the period between 2007 and 2012.
The findings suggest a potential relationship between the Pb levels detected in the fish muscles and the corresponding Pb concentrations in the water samples. The studies conducted by Burada (2014–2015) likely provide valuable insights into environmental Pb contamination during the specified timeframe [78,79]. By examining the water samples, Burada may have identified elevated Pb values that could have influenced the accumulation of lead in the muscle tissues of carp and mackerel species.
It is essential to consider that Pb accumulation in fish can occur through various pathways, including direct exposure to contaminated water or through the food chain. Fish species such as carp and mackerel exhibit different feeding habits and ecological behaviors, which can affect their susceptibility to Pb contamination. Factors such as the proximity of the sampled sectors to potential pollution sources, the concentration and availability of Pb in the water, and the migratory patterns of the fish species should also be taken into account.
Further research and investigation are necessary to establish a more definitive cause-and-effect relationship between the Pb levels in the fish muscles and the corresponding water samples. This would involve assessing the temporal and spatial correlation, considering other potential sources of Pb contamination, and evaluating the bioaccumulation and biomagnification processes within the aquatic ecosystem.
The analysis of samples collected between 2003 and 2013 indicated that the Zn content in muscle tissue, liver, gonads, and tegument exceeded the accepted limits for Cyprinus carpio and Alosa immaculata in all studied sectors. These findings suggest a widespread issue of elevated Zn levels in these fish species.
In sector V, there was a notable correlation between the high Zn values observed in water and sediment samples. The elevated Zn levels in the water and sediment samples from sector V may have contributed to the higher Zn concentrations found in the fish species, thus potentially playing a role in the occurrence of diseases.
Regarding catfish, barbel, and perch samples from sector I, higher Zn values were specifically detected in the gonads and liver. This indicates that these organs of the studied fish species in sector I accumulated elevated amounts of Zn. The reasons behind these higher Zn levels in the gonads and liver of Silurus glanis, Barbus barbus, and Perca fluviatilis in sector I may be associated with specific environmental factors or biological characteristics of these fish species, such as their feeding habits or habitat preferences.
Further investigation is necessary to determine the causes of the high Zn content in the various fish tissues and sectors. Factors such as pollution sources, dietary patterns, and species-specific physiological processes should be considered to understand the mechanisms leading to Zn accumulation in different organs. Additionally, assessing the potential health implications of these elevated Zn levels in fish species is essential to evaluating the overall ecological impact and potential risks to human consumption.
The differences in metal concentrations within tissues can be attributed to the tissue’s capacity to generate metal-binding proteins such as metallothionein [68].
Various pathways facilitate the entry of metals into the human body, which can occur through multiple sources, such as water, food, air, and even cosmetics. Among these avenues, the most prevalent metal intake method is regularly consuming contaminated food.
Several factors influence the potential risk to human health related to fish consumption. These include the size of the meal, the type of fish consumed, variations in bioaccumulation among different fish species, and the presence of specific chemicals [98]. Monitoring the concentration of substances, including inorganic and organic compounds, is essential for reducing pollution and minimizing metal contamination.
Due to regular consumption of such contaminated food, these metals gradually accumulate in the body over time. Addressing and monitoring this primary pathway of metal intake is important to safeguard public health and minimize the potential risks associated with metal exposure.

5. Conclusions

It is crucial to have a comprehensive understanding of metal concentrations in fish to safeguard human health and effectively manage the environment. Metal poisoning can cause damage to the brain, kidneys, liver, and other important organs and even lead to the development of cancer, as exemplified by the carcinogenic properties of As. Symptoms of metal poisoning can range from weakness to headaches. Therefore, continuous monitoring of metal concentrations in fish is of utmost importance.
Fish have long been considered practical pollution biomarkers in aquatic environments. Evaluating the levels of metals in edible fish is essential for ensuring the safety of fish protein for consumers and comprehending its detrimental effects on individuals, populations, or ecosystems.
It is vital to assess the ecological and health risks associated with metal exposure through food, especially when consuming fish contaminated with metals. However, there is a lack of comprehensive studies addressing this issue in Romania. Previous studies have focused on small areas or solely examined sediment contamination without exploring the connection between metals in entire watersheds or sediments and their impact on humans through the food chain.
Specific populations, such as pregnant women, children, and fishermen relying heavily on fish as a protein source, may be disproportionately affected by consuming contaminated fish. Therefore, assessing the potential health risks associated with exposure to metals is essential.
Further research is needed to evaluate the nutrient and metal concentrations in commonly consumed fish to determine acceptable toxicity levels and understand their potential effects on human health. While several studies have already addressed the risks of metal exposure from fish consumption, more research is required to compare different thresholds and better understand the impact on human health.
Although many fish species can absorb metals, in the Danube River, the levels detected in fish meat generally remain below the maximum residue limits (MRLs) proposed in the Official Journal of the European Communities (2001). Nevertheless, monitoring metal concentrations in fish meat is necessary, particularly considering its consumption in the human diet.
Monitoring fish welfare and assessing the quality of aquatic ecosystems in proximity to significant human activities is essential to proactively mitigate potential health risks for consumers.

Author Contributions

Conceptualization, A.N.C., L.O. and L.D.; formal analysis, A.N.C.; investigation, A.N.C., M.C. and M.T.C.; methodology, A.N.C.; validation, L.O. and L.D.; draft manuscript writing, A.N.C.; manuscript revision, L.D., L.O., M.C. and D.-N.M.; final editing, L.O., L.D. and M.C. All authors have read and agreed to the published version of the manuscript.

Funding

The work of Anca Nicoleta Cordeli (Săvescu) was supported by the project “PROINVENT”, Contract No. 62487/03.06.2022—POCU/993/6/13—Code 153299, financed by The Human Capital Operational Programme 2014–2020 (POCU), Romania.

Acknowledgments

The authors of the article thank the “Dunărea de Jos” University of Galați, which, through the University Degree Program and the doctoral studies contract, has supported the achievement. Anca Nicoleta Cordeli (Săvescu) is thankful for the project “PROINVENT”, Contract No. 62487/03.06.2022—POCU/993/6/13—Code 153299, financed by The Human Capital Operational Programme 2014–2020 (POCU), Romania. Additionally, the work of Mirela Crețu, Lorena DEDIU and Marian Tiberiu COADĂ is grateful for the technical support offered by MoRAS through Grant POSCCE ID1815, cod SMIS 48745 www.moras.ugal.ro (accessed on 5 March 2023).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Goyer, R.; Golub, M.; Choudhury, H.; Hughes, M.; Kenyon, E.; Stifelman, M. Issue Paper on the Human Health Effects of Metals; U.S. Environmental Protection Agency, Risk Assessment Forum: Washington, DC, USA, 2004.
  2. Tuzen, M. Toxic and essential trace elemental contents in fish species from the Black Sea, Turkey. Food Chem. Toxicol. 2009, 47, 1785–1790. [Google Scholar] [PubMed]
  3. Milenkovic, N.; Damjanovic, M.; Ristic, M. Study of heavy metal pollution in sediments from the Iron Gate (Danube River), Serbia and Montenegro. Pol. J. Environ. Stud. 2005, 14, 781–787. [Google Scholar]
  4. Vuković, Ž.; Vuković, D.; Radenković, M.; Stanković, S. A new approach to the analysis of the accumulation and enrichment of heavy metals in the Danube River sediment along the Iron Gate reservoir in Serbia. J. Serb. Chem. Soc. 2012, 77, 381–392. [Google Scholar]
  5. Vuković, D.; Vuković, Ž.; Stanković, S. The impact of the Danube Iron Gate Dam on heavy metal storage and sediment flux within the reservoir. Catena 2014, 113, 18–23. [Google Scholar]
  6. Akan, J.C.; Mohmoud, S.; Yikala, B.S.; Ogugbuaja, V.O. Bioaccumulation of Some Heavy Metals in Fish Samples from River Benue in Vinikilang, Adamawa State, Nigeria. Am. J. Anal. Chem. 2012, 3, 727–736. [Google Scholar]
  7. Wei, Y.; Zhang, J.; Zhang, D.; Tu, T.; Luo, L. Metal concentrations in various fish organs of different fish species from Poyang Lake, China. Ecotoxicol. Environ. Saf. 2014, 104, 182–188. [Google Scholar]
  8. Varola, M.; Sünbül, M.R. Environmental contaminants in fish species from a large dam reservoir and their potential risks to human health. Ecotoxicol. Environ. Saf. 2019, 169, 507–515. [Google Scholar] [CrossRef]
  9. Dehn, L.A.; Follmann, E.H.; Thomas, D.L.; Sheffield, G.G.; Rosa, C.; Duffy, L.K.; O’Hara, T.M. Trophic relationships in an Arctic food web and implications for trace metal transfer. Sci. Total Environ. 2006, 362, 103–123. [Google Scholar] [CrossRef]
  10. Bibi, M.; Hashmi, M.Z.; Malik, R.N. The level and distribution of heavy metals and changes in oxidative stress indices in humans from Lahore district, Pakistan. Hum. Exp. Toxicol. 2016, 35, 78–90. [Google Scholar] [CrossRef]
  11. Janjić, J.; Ivanović, J.; Marković, R.; Starčević, M.; Bošković, M.; Đorđević, V.; Baltić, Ž.M. Metal concentration in muscle tissue of carp and pike from different fish ponds in Belgrade area. J. Agric. Sci. Technol. 2015, 5, 429–436. [Google Scholar]
  12. Noël, L.; Chekri, R.; Millour, S.; Merlo, M.; Leblanc, J.; Guérin, T. Distribution and relationships of As, Cd, Pb, and Hg in freshwater fish from five French fishing areas. Chemosphere 2013, 90, 1900–1910. [Google Scholar] [PubMed]
  13. Verep, B.; Multu, C.; Apaydin, G.; Cevik, U. The trace element analysis in freshwater fish species, water and sediments in Iyidere Stream (Rize-Turkey). Pak. J. Biol. Sci. 2012, 15, 658–665. [Google Scholar]
  14. Bawuro, A.A.; Voegborlo, R.B.; Adimado, A.A. Bioaccumulation of heavy metals in some tissues of fish in Lake Geriyo, Adamawa State, Nigeria. J. Environ. Public Health 2018, 2018, 1854892. [Google Scholar] [PubMed] [Green Version]
  15. Dural, M.; Goksu, M.Z.L.; Ozak, A.A. Investigation of heavy metal levels in economically important fish species captured from the Tuzla Lagoon. Food Chem. 2007, 102, 415–421. [Google Scholar]
  16. Lana, R.; Vavrova, M.; Navratil, S.; Brabencova, E.; Vecerek, V. Organochlorine pollutants in chub, Leuciscus cephalus, from the Svratka River, Czech Republic. Bull. Environ. Contam. Toxicol. 2010, 84, 726–730. [Google Scholar] [PubMed]
  17. Farombi, E.O.; Adelowo, O.A.; Ajimoko, Y.R. Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African catfish (Clarias gariepinus) from Nigeria Ogun River. Int. J. Environ. Res. Public Health 2007, 4, 158–165. [Google Scholar] [PubMed] [Green Version]
  18. Drąg-Kozak, E.; Łuszczek-Trojnar, E.; Socha, M.; Bojarski, B. Effects of Melatonin on Cadmium Accumulation and Haematological Parameters in Cadmium Intoxicated Prussian Carp (B.). Ann. Anim. Sci. 2021, 21, 899–923. [Google Scholar]
  19. Guo, J.; Pu, Y.; Zhong, L.; Wang, K.; Duan, X.; Chen, D. Lead impaired immune function and tissue integrity in yellow catfish (Peltobargus fulvidraco) by mediating oxidative stress, inflammatory response and apoptosis. Ecotoxicol. Environ. Saf. 2021, 226, 112857. [Google Scholar]
  20. Shahjahan, M.; Taslima, K.; Rahman, M.S.; Al-Emran, M.; Alam, S.I.; Faggio, C. Effects of heavy metals on fish physiology—A review. Chemosphere 2022, 300, 134519. [Google Scholar]
  21. Ackland, M.L.; Bornhorst, J.; Dedoussis, G.V.; Dietert, R.R.; Nriagu, J.O.; Pacyna, J.M.; Pettifor, J.M. Metals in the environment as risk factors for infectious diseases. In Trace Metals and Infectious Diseases; MIT Press: Cambridge, MA, USA, 2015. [Google Scholar]
  22. Macirella, R.; Curcio, V.; Ahmed, A.I.M.; Talarico, F.; Sesti, S.; Paravani, E.; Odetti, L.; Mezzasalma, M.; Brunelli, E. Morphological and Functional Alterations of Zebrafish (Danio rerio) Liver after Exposure to Two Ecologically Relevant Concentrations of Lead. Fishes 2023, 8, 342. [Google Scholar]
  23. Ebrahimi, M.; Taherianfard, M. The effects of heavy metals exposure on reproductive systems of cyprinid fish from Kor River. Iran. J. Fish. Sci. 2011, 10, 13–26. [Google Scholar]
  24. Bera, T.; Kumar, S.V.; Devi, M.S.; Kumar, V.; Behera, B.K.; Das, B.K. Effect of heavy metals in fish reproduction: A review. J. Environ. Biol. 2022, 43, 631–642. [Google Scholar]
  25. Taslima, K.; Al-Emran, M.; Rahman, M.S.; Hasan, J.; Ferdous, Z.; Rohani, M.F.; Shahjahan, M. Impacts of heavy metals on early development, growth and reproduction of fish—A review. Toxicol. Rep. 2022, 9, 858–868. [Google Scholar]
  26. Munaretto, J.S.; Ferronato, G.; Ribeiro, L.C.; Martins, M.L.; Adaime, M.B.; Zanella, R. Development of a multi-residue method for the determination of endocrine disrupters in fish fillet using gas chromatography–triple quadrupole tandem mass spectrometry. Talanta 2013, 116, 827–834. [Google Scholar] [PubMed]
  27. Dang, V.D.; Kroll, K.J.; Supowit, S.D.; Halden, R.U.; Denslow, N.D. Tissue distribution of organochlorine pesticides in largemouth bass (Micropterus salmoides) from laboratory exposure and a contaminated lake. Environ. Pollut. 2016, 216, 877–883. [Google Scholar]
  28. Tsai, M.-T.; Huang, S.-Y.; Cheng, S.-Y. Lead poisoning can be easily misdiagnosed as acute porphyria and nonspecific abdominal pain case report in emergency medicine 2017. Case Rep. Emerg. Med. 2017, 2017, 9050713. [Google Scholar] [CrossRef] [Green Version]
  29. Abadin, H.; Ashizawa, A.; Stevens, Y.W.; Llados, F.; Diamond, G.; Sage, G.; Citra, M.; Quinones, A.; Bosch, S.J.; Swarts, S.G. Toxicological Profile for Lead; Atlanta (GA) Agency for Toxic Substances and Disease Registry (US): Atlanta, GA, USA, 2007. [PubMed]
  30. Fernandes Azevedo, B.; Barros Furieri, L.; Peçanha, F.M.; Wiggers, G.A.; Frizera Vassallo, P.; Ronacher Simões, M.; Fiorim, J.; de Batista, P.R.; Fioresi, M.; Rossoni, L.; et al. Toxic effects of mercury on the cardiovascular and central nervous systems. J. Biomed. Biotechnol. 2012, 2012, 949048. [Google Scholar]
  31. World Health Organization. Elemental Speciation in Human Health Risk Assessment; World Health Organization: Geneva, Switzerland, 2006. [Google Scholar]
  32. Sanders, T.; Liu, Y.; Buchner, V.; Tchounwou, P.B. Neurotoxic effects and biomarkers of lead exposure: A review. Rev. Environ. Health 2009, 24, 15–46. [Google Scholar]
  33. Bondar, C. Hydromorphological Balance of the Danube River Channel on the Sector between Bazias (km 1072.2) and Danube Delta Inlet (km 80.5); National Institute of Marine Geology and Geo-Ecology: Bucharest, Romania, 2008; Available online: https://www.osce.org/files/f/documents/0/8/32944.pdf (accessed on 1 March 2023).
  34. Shabani, M.; Hadeiy, S.K.; Parhizgar, P.; Zamani, N.; Mehrad, H.; Hassanian-Moghaddam, H.; Phillips, S. Lead poisoning; a neglected potential diagnosis in abdominal pain. BMC Gastroenterol. 2020, 20, 134. [Google Scholar]
  35. Jaishankar, M.; Tseten, T.; Anbalagan, N.; Mathew, B.B.; Beeregowda, K.N. Toxicity, mechanism and health effects of some heavy metals. Interdiscip. Toxicol. 2014, 7, 60. [Google Scholar]
  36. Mitra, S.; Chakraborty, A.J.; Tareq, A.M.; Emran, T.B.; Nainu, F.; Khusro, A.; Idris, A.M.; Khandaker, M.U.; Osman, H.; Alhumaydhi, F.A.; et al. Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter the toxicity. J. King Saud. Univ. Sci. 2022, 34, 101865. [Google Scholar]
  37. Goyer, R.A.; Clarkson, T.M. Chapter 23: Toxic effects of metals. In Casarett & Doull’s Toxicology; Klaassen, C.D., Ed.; McGraw-Hill: New York, NY, USA, 2001; pp. 811–868. [Google Scholar]
  38. Davison, A.G.; Taylor, A.; Darbyshire, J. Cadmium fume inhalation and emphysema. Lancet 1988, 26, 663–667. [Google Scholar]
  39. Järup, L.; Berglund, M.; Elinder, C.G.; Nordberg, G.; Vahter, M. Health effects of cadmium exposure—A review of the literature and a risk estimate. Scand. J. Work Environ. Health 1998, 24 (Suppl. 1), 1–52. [Google Scholar]
  40. IPCS (World Health Organization, International Programme on Chemical Safety). Inorganic Lead. Environmental Health Criteria Document No. 165; WHO: Geneva, Switzerland, 1995; pp. 152–192.
  41. ATSDR (Agency for Toxic Substances and Disease Registry). Toxicological Profile for Mercury; ATSDR: Atlanta, GA, USA, 1999.
  42. NAS/NRC (National Academy of Sciences/National Research Council). Arsenic in Drinking Water 2001 Update; National Academy of Science, National Academy Press: Washington, DC, USA, 2001. [Google Scholar]
  43. De Vleeschouwer, F.; Gérard, L.; Goormaghtigh, C.; Mattielli, N.; Le Roux, G.; Fagel, N. Atmospheric lead and heavy metal pollution records from a Belgian peat bog spanning the last two millennia: Human impact on a regional to global scale. Sci. Total Environ. 2007, 377, 282–295. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Fu, Z.; Wu, F.; Chen, L.; Xu, B.; Feng, C.; Bai, Y.; Liao, H.; Sun, S.; Giesy, J.P.; Guo, W. Copper and zinc, but not other priority toxic metals, pose risks to native aquatic species in a large urban lake in Eastern China. Environ. Pollut. 2016, 219, 1069–1076. [Google Scholar] [CrossRef]
  45. Golovanova, I.L. Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates. Inc. Water Biol. 2008, 1, 93–101. [Google Scholar] [CrossRef]
  46. Meena, R.A.A.; Sathishkumar, P.; Ameen, F.; Yusoff, A.R.M.; Gu, F.L. Heavymetal pollution in immobile and mobile components of lentic ecosystems—A review. Environ. Sci. Pollut. Res. 2018, 25, 4134–4148. [Google Scholar] [CrossRef]
  47. ICPDR/International Commission for the Protection of the Danube River. Water Quality in the Danube River Basin—2019—TNMN—Yearbook; ICPDR: Vienna, Austria, 2019; Available online: www.icpdr.org (accessed on 12 March 2023).
  48. Subotić, S.; Jeftić, V.; Spasić, S.; Hegediš, A.; Krpo-Ćetković, J.; Lenhardt, M. Distribution and accumulation of elements (As, Cu, Fe, Hg, Mn, and Zn) in tissues of fish species from different trophic levels in the Danube River at the confluence with the Sava River (Serbia). Environ. Sci. Pollut. Res. 2013, 20, 5309–5317. [Google Scholar] [CrossRef]
  49. Teodorović, I.; Đukić, N.; Maletin, S.; Miljanović, B.; Jugovac, N. Metal pollution index: Proposal for freshwater monitoring based on trace metal accumulation in fish. Tiscia 2000, 32, 55–60. [Google Scholar]
  50. ORDER, no. 161 for the Approval of the Norm Regarding the Classification of Surface Water Quality in Order to Establish the Ecological Status of Water Bodies. Available online: http://www.monitoruljuridic.ro/monitorul-oficial/161/2006-02-21 (accessed on 10 March 2022). (In Romanian).
  51. Horton, R.K. An index number system for rating water quality. J. Water Pollut. Cont. Fed. 1965, 37, 300–305. [Google Scholar]
  52. Official Journal of the European Communities. Commission Regulation (EC) No 466/2001, of 8 March 2001. Setting Maximum Levels for Certain Contaminants in Foodstuffs; EC: Brussels, Belgium, 2001. [Google Scholar]
  53. FAO (Food and Agriculture Organization). Compilation of Legal Limits for Hazardous Substances in Fish and Fishery Products; FAO Fishery Circular 1983 No. 464; FAO: Rome, Italy, 1983; pp. 5–100. [Google Scholar]
  54. Official Gazzette of FRY, No 28/2011. Regulation on Quantity of Pesticides, Metals, Metalloids, and Other Toxic Substances, Chemotherapeutics, Anabolics, and Other Substances Which Can Be Found in Food. Available online: https://legislatie.just.ro/Public/DetaliiDocument/129856 (accessed on 5 March 2023).
  55. Derakhshan, Z.; Mahvi, A.H.; Faramarzian, M.; Dehghani, M.; Salari, M.; Fakhri, Y.; Afsharnia, M.; Hosseini, M.S.; Marzban, A.; Taghavi, M. Data on heavy metal concentration in common carp fish consumed in Shiraz, Iran. Elsevier Inc. Data Brief. 2018, 21, 1890–1894. [Google Scholar] [CrossRef]
  56. Al-Hashemi, A.H.; Sekhavatjou, M.S.; Kiabi, B.H.; Karbassi, A.R. Bioaccumulation of trace elements in water, sediment, and ProcZool Soc 123 Six fish species from a freshwater wetland, Iran. Microchem. J. 2012, 104, 1–6. [Google Scholar]
  57. ATSDR. Toxicological Profile for Chromium; U.S. Department of Health and Human Services, Public Health Service: Atlanta, GA, USA, 2012.
  58. Buha, A.; Wallace, D.; Matovic, V.; Schweitzer, A.; Oluic, B.; Micic, D.; Djordjevic, V. Cadmium exposure as a putative risk factor for the development of pancreatic cancer: Three different lines of evidence. BioMed. Res. Int. 2017, 2017, 1981837. [Google Scholar]
  59. FAO/WHO. Compilation of Legal Limits for Hazardous Substances in Fish and Fishery Products. Fisheries Circular. No. 764. 1983. Available online: http://www.fao.org/inland-fisheries/topic/detail/fr/c/1150083/ (accessed on 2 April 2023).
  60. Boyden, C.R.; Phillips, D.J.H. Seasonal variation and inherent variability of trace elements in oysters and their implications for indicator studies. Mar. Ecol. Prog. 1981, 5, 29–40. [Google Scholar]
  61. Ural, M.; Yildirim, N.; Danabas, D.; Kaplan, O.; Cikcikoglu Yildirim, N.; Ozcelik, M.; Kurekci, E.F. Some heavy metals accumulation in tissues in Capoeta umbla (Heckel, 1843) from Uzuncayir Dam Lake (Tunceli, Turkey). Bull. Environ. Contam. Toxicol. 2012, 88, 172–176. [Google Scholar]
  62. Yilmaz, F.; Özdemir, N.; Demirak, A.; Levent Tuna, A. Heavy metal levels in two fish species, Leuciscus cephalus and Lepomis gibbosus. Food Chem. 2007, 100, 830–835. [Google Scholar]
  63. Jarić, I.; Višnjić-Jeftić, Ž.; Cvijanović, G.; Gačić, Z.; Jovanović, L.; Skorić, S.; Lenhardt, M. Determination of differential heavy metal and trace element accumulation in liver, gills, intestine and muscle of starlet (Acipenser ruthenus) from the Danube River in Serbia by ICP-OES. Microchem. J. 2011, 98, 77–81. [Google Scholar]
  64. Poleksić, V.; Lenhardt, M.; Jarić, I.; Đorđević, D.; Gačić, Z.; Cvijanović, G.; Rašković, B. Liver, gills, and skin histopathology and heavy metal content of the Danube starlet (Acipenser ruthenus Linnaeus, 1758). Environ. Toxicol. Chem. 2010, 29, 515–521. [Google Scholar]
  65. Višnjić-Jeftić, Ž.; Jarić, I.; Jovanović, L.; Skorić, S.; Smederevac-Lalić, M.; Nikčević, M.; Lenhardt, M. Heavy metal and trace element accumulation in muscle, liver and gills of the Pontic shad (Alosa immaculata Bennet 1835) from the Danube River(Serbia). Microchem. J. 2010, 95, 341–344. [Google Scholar]
  66. Milanov, R.; Krstić, M.; Marković, R.; Jovanović, D.; Baltić, B.; Ivanović, J.; Jovetić, M.; Baltić, Ž.M. Analysis of heavy metals concentration in tissues of three different fish species included in human diet from Danube River, in the Belgrade Region, Serbia. Acta Vet. 2016, 66, 89–102. [Google Scholar]
  67. Antonijević, M.D.; Arsović, M.; Čáslavský, J.; Cvetković, V.; Dabić, P.; Franko, M.; Ilić, G.; Ivanović, M.; Ivanović, N.; Kosovac, M.; et al. Actual contamination of the Danube and Sava rivers at Belgrade. J. Serb. Chem. Soc. 2013, 9, 1169–1184. [Google Scholar]
  68. Ivanović, J.; Janjić, J.; Baltić, M.; Milanov, R.; Bošković, M.; Marković, R.V.; Glamočlija, N. Metal concentrations in water, sediment and three fish species from the Danube River, Serbia: A cause for environmental concern. Environ. Sci. Pollut. Res. 2016, 23, 17105–17112. [Google Scholar] [CrossRef]
  69. Culicov, O.A.; Trtíc-Petrovíc, T.; Nekhoroshkov, P.S.; Zinicovscaia, I.; Duliu, O.G. On the Geochemistry of the Danube River Sediments (Serbian Sector). Int. J. Environ. Res. Public Health 2022, 19, 12879. [Google Scholar] [CrossRef] [PubMed]
  70. Sediment-Quality Information, Monitoring and Assessment System to Support Transnational Cooperation for Joint Danube Basin Water Management (Project SIMONA). 2021. Available online: https://www.icpdr.org/main/publications/danube-watch-3-2021-simona-sediment-quality-information-monitoring-and-assessment (accessed on 2 March 2023).
  71. Popescu, F.; Trumić, M.; Cioabla, A.E.; Vujić, B.; Stoica, V.; Trumić, M.; Opris, C.; Bogdanović, G.; Trif-Tordai, G. Analysis of Surface Water Quality and Sediments Content on Danube Basin in Djerdap-Iron Gate Protected Areas. Water 2022, 14, 2991. [Google Scholar] [CrossRef]
  72. Radu, V.; Ionescu, P.; Diacu, E.; Deak, G.; Ivanov, A.A. Assessing and Spatio-Temporal Variations of Potentially Toxic Elements in the Sediments from Lower Danube River in 2011–2017 Period. Rev. Chim. 2020, 71, 126–135. [Google Scholar]
  73. Anghel, A.M.; Diacu, E.; Ilie, M.; Petrescu, A.; Ghita, G.; Marinescu, F.; Deak, G. Statistical Analysis of Heavy Metals Concentration in Water and Sediments in the Lower Part of the Danube River—Romanian Section. Rev. Chim. 2016, 11, 2151–2155. [Google Scholar]
  74. Ilie, M.; Marinescu, F.; Ghita, G.; Deak, G.Y.; Tanase, G.S.; Raischi, M. Assessment of Heavy Metal in Water and Sediments of the Danube River. J. Environ. Prot. Ecol. 2014, 15, 825–833. [Google Scholar]
  75. Winkels, H.J.; Kroonenberg, S.B.; Lychagin, M.Y.; Marin, G.; Rusakov, G.V.; Kasimov, N.S. Geochronology of priority pollutants in sedimentation zones of the Volga and Danube delta in comparison with the Rhine delta. Appl. Geochem. 1998, 13, 581–591. [Google Scholar] [CrossRef]
  76. Vignati, D.A.; Secrieru, D.; Bogatova, Y.I.; Dominik, J.; Céréghino, R.; Berlinsky, N.A.; Oaie, G.; Szobotka, S.; Stanica, A. Trace element contamination in the arms of the Danube Delta (Romania/Ukraine): Current state of knowledge and future needs. J. Environ. Manag. 2013, 125, 169–178. [Google Scholar]
  77. Vosniakos, F.; Petre, J.; Pascu, L.; Vasile, G.; Iancu, V.; Staniloae, D.; Nicolau, M.; Cruceru, L.; Golumbeanu, M. Aquatic ecosystem quality assessment of the Danube Delta in the periods April-Oct. 2007 and 2008. Fresenius Environ. Bull. 2010, 19, 20–29. [Google Scholar]
  78. Burada, A.; Topa, C.M.; Georgescu, L.P.; Teodorof, L.; Nastase, C.; Seceleanu-Odor, D.; Iticescu, C. Heavy Metals Environment Accumulation in Somova—Parches Aquatic Complex from the Danube Delta Area. Rev. Chim. 2015, 66, 48–54. [Google Scholar]
  79. Burada, A.; Odor, D.S.; Teodorof, L.; Nastasea, C.; Nastase, A.; Navodaru, I.; Georgescu, L.P. Mercury levels in fish tissues with and without commercial value from Danube Delta biosphere reserve. J. Environ. Prot. Ecol. 2014, 15, 842–850. [Google Scholar]
  80. Milošković, A.; Dojčinović, B.; Kovačević, S.; Radojković, N.; Radenković, M.; Milošević, D.; Simić, V. Spatial monitoring of heavy metals in the inland waters of Serbia: A multispecies approach based on commercial fish. Environ. Sci. Pollut. Res. 2016, 23, 9918–9933. [Google Scholar] [CrossRef]
  81. Matache, M.L.; Marin, C.; Rozylowicz, L.; Tudorache, A. Plants accumulating heavy metals in the Danube River wetlands. J. Environ. Health Sci. Eng. 2013, 11, 39. [Google Scholar] [CrossRef] [Green Version]
  82. Ionita, C.; Mititelu, M.; Morosan, E. Analysis Of Heavy Metals And Organic Pollutants From Some Danube River Fishes. Farmacia 2014, 62, 299–305. [Google Scholar]
  83. Tiberiu, R.; Rusu, T.A.; Vida, C.; Pădurețu, S. Determining Heavy Metal Concentrations in the Waters of Babadag River. ProEnvironment 2014, 7, 80–84. [Google Scholar]
  84. Ira-Adeline, S.; Victor, C.; Stefan-Mihai, P.; Alina, M.; Aurelia, N.; Stefan-Adrian, S.; Antoaneta, E.; Ancuta, S.D. Heavy Metal Evaluation in the Lower Sector of Danube River. Available online: https://landreclamationjournal.usamv.ro/pdf/2020/Art1.pdf (accessed on 20 March 2023).
  85. Catianis, I.; Tiron, D.L.; Grosu, D. Heavy Metals Occurrence in Lakes of the Danube Delta, Romania. Geo-Eco-Marina 2022, 28, 49–63. Available online: https://geoecomar.ro/beta/wp-content/uploads/2023/01/04_CATIANIS_c4_2022.pdf (accessed on 5 April 2023).
  86. Zhang, J.L.; Fang, L.; Song, J.Y.; Luo, X.; Fu, K.D.; Chen, L.Q. Health Risk Assessment of Heavy Metals in Cyprinus carpio (Cyprinidae) from the Upper Mekong River; Environmental Science and Pollution Research; Springer: Berlin/Heidelberg, Germany, 2019. [Google Scholar] [CrossRef]
  87. Calmuc, V.A.; Calmuc, M.; Arseni, M.; Topa, C.M.; Timofti, M.; Burada, A.; Iticescu, C.; Georgescu, L.P. Assessment of Heavy Metal Pollution Levels in Sediments and of Ecological Risk by Quality Indices, Applying a Case Study: The Lower Danube River, Romania. Water 2021, 13, 1801. [Google Scholar] [CrossRef]
  88. Teien, H.-C.; Kroglund, F.; Salbu, B.; Rosseland, B.O. Gill reactivity of aluminum-species following liming. Sci. Total Environ. 2006, 358, 206–220. [Google Scholar] [CrossRef] [PubMed]
  89. Hansen, B.H.; Garmo, A.; Olsvik, P.A.; Andersen, R.A. Gill metal binding and stress gene transcription in brown trout (Salmo trutta) exposed to metal environments: The effect of preexposure in natural populations. Environ. Toxicol. Chem. 2007, 26, 944–953. [Google Scholar] [CrossRef]
  90. Terra, B.F.; Araújo, F.G.; Calza, C.F.; Lopes, R.T.; Teixeira, T.P. Heavy metal in tissues of three fish species from different trophic levels in a tropical Brazilian River. Water Air Soil Pollut. 2008, 187, 275–284. [Google Scholar] [CrossRef]
  91. Čelechovská, O.; Svobodová, Z.; Žlábek, V.; Macharáčková, B. Distribution of metals in tissues of the common carp (Cyprinus carpio L.). Acta Vet. Brno 2007, 76, 93–100. [Google Scholar] [CrossRef]
  92. Beltcheva, M.; Metcheva, R.; Peneva, V.; Marinova, M.; Yankov, Y.; Chikova, V. Heavy metals in Antarctic notothenioid fish from South Bay, Livingston Island, South Shetlands (Antarctica). Biol. Trace Elem. Res. 2011, 141, 150–158. [Google Scholar] [CrossRef] [PubMed]
  93. de Carvalho Costa, S.; Hartz, S.M. Evaluation of trace metals (Cadmium, chromium, Copper and Zinc) in tissues of commercially important fish (Leporinus outsiders) from Guaíba Lake, Southern Brazil. Braz. Arch. Biol. Technol. 2009, 52, 241–250. [Google Scholar] [CrossRef]
  94. Jovanović, D.A.; Marković, R.V.; Teodorović, V.B.; Šefer, D.S.; Krstić, M.P.; Radulović, S.B.; Ćirić, J.; Janjić, J.M.; Baltić, M. Determination of heavy metals in muscle tissue of six fish species with different feeding habits from the Danube River, Belgrade—Public health and environmental risk assessment. Environ. Sci. Pollut. Res. 2017, 24, 11383–11391. [Google Scholar] [CrossRef]
  95. Subotić, S.; Spasić, S.; Višnjić-Jeftić, Ž.; Hegediš, A.; Krpo-Ćetković, J.; Mićković, B.; Skorić, S.; Lenhardt, M. Heavy metal and trace element bioaccumulation in target tissues of four edible fish species from the Danube River (Serbia). Ecotoxicol. Environ. Saf. 2013, 98, 196–202. [Google Scholar] [CrossRef] [PubMed]
  96. Lenhardt, M.; Jarić, I.; Višnjić-Jeftić, Z.; Skorić, S.; Gačić, Z.; Pucar, M.; Hegediš, A. Concentrations of 17 elements in muscle, gills, liver and gonads of five economically important fish species from the Danube River. Knowl. Manag. Aquat. Ecosyst. 2012, 407, 2. [Google Scholar] [CrossRef] [Green Version]
  97. Zrnčić, S.; Oraić, D.; Ćaleta, M.; Mihaljević, Z.; Zanella, D.; Bilandžić, N. Biomonitoring of heavy metals in fish from the Danube River. Environ. Monit. Assess. 2013, 185, 1189–1198. [Google Scholar] [CrossRef]
  98. Mititelu, M.; Nicolescu, F.; Ionita, C.-A.; Nicolescu, T.-O. Study of Heavy Metals and organic pollutants in some fishes of the Danube River. J. Environ. Prot. Ecol. 2012, 13, 869–874. [Google Scholar]
  99. Burada, A.; Teodorof, L.; Despina, C.; Seceleanu-Odor, D.; Tudor, M.; Ibram, O.; Navodaru, I.; Murariu, G.; Topa, C.M.; Tudor, M. Trace elements in fish tissue with commercial value of the Danube Delta biosphere reserve. Environ. Eng. Manag. J. 2017, 16, 731–738. [Google Scholar] [CrossRef]
  100. Jovicic, K.; Jankovic, S.; Visnjic-Jeftic, Z.; Skoric, S.; Djikanovic, V.; Lenhardt, M.; Hegedis, A.; Krpo-Cetkovic, J.; Jaric, I. Mapping differential elemental accumulation in fish tissues: Importance of fish tissue sampling standardization. Biol. Sci. 2016, 68, 303–309. [Google Scholar] [CrossRef] [Green Version]
  101. Gheorghe, S.; Vasile, G.G.; Gligor, C.; Lucaciu, I.E.; Lazar, M.N. Metallic Elements (Cu, Zn, Ni and Mn) Toxicity effects determination on a freshwater fish Cyprinus carpio (Common Carp) laboratory acclimatized. Rev. Chim. 2017, 68, 8. [Google Scholar] [CrossRef]
  102. Diaconescu, C.; Urdes, L.; Marius, H.; Ianitchi, D.; Popa, D. The influence of heavy metal content on superoxide dismutase and glutathione peroxidase activity in the fish meat originated from different areas of Danube river. Roum. Biotechnol. Lett. 2008, 13, 3859–3862. [Google Scholar]
  103. Kostić-Vuković, J.; Kolarević, S.; Kračun-Kolarević, M.; Višnjić-Jeftić, Ž.; Rašković, B.; Poleksić, V.; Gačić, Z.; Lenhardt, M.; Vuković-Gačić, B. Temporal variation of biomarkers in common bream Abramis brama (L. 1758) exposed to untreated municipal wastewater in the Danube River in Belgrade, Serbia. Environ. Monit. Assess. 2021, 193, 465. [Google Scholar] [CrossRef]
  104. Kalyoncu, L.; Kalyoncu, H.; Arslan, G. Determination of heavy metals and metals levels in five fish species from I¸sıklı Dam Lake and Karacaören Dam Lake (Turkey). Environ. Monit. Assess 2021, 184, 2231–2235. [Google Scholar] [CrossRef]
  105. Pantelica, A.; Ene, A.; Georgescu, I.I. Instrumental neutron activation analysis of some fish species from Danube River in Romania. Microchem. J. 2012, 103, 142–147. [Google Scholar] [CrossRef]
  106. Nachev, M.; Rozdina, D.; Michler-Kozma, D.N.; Raikova, G.; Sures, B. Metal accumulation in ecto- and endoparasites from the anadromous fish, the Pontic shad (Alosa immaculata). Parasitology 2022, 149, 496–502. [Google Scholar] [CrossRef]
  107. Jovičić, K.; Nikolić, D.M.; Višnjić-Jeftić, Z.; Đikanović, V.; Skorić, S.; Stefanović, S.M.; Lenhardt, M.; Hegediš, A.; Krpo-Ćetković, J.; Jarić, I. Mapping differential elemental accumulation in fish tissues: Assessment of metal and trace element concentrations in wels catfish (Silurus glanis) from the Danube River by ICP-MS. Environ. Sci. Pollut. Res. 2014, 22, 3820–3827. [Google Scholar] [CrossRef]
  108. Rašković, B.; Poleksić, V.; Višnjić-Jeftić, Ž.; Skorić, S.; Gačić, Z.; Djikanović, V.; Jarić, I.; Lenhardt, M. Use of histopathology and elemental accumulation in different organs of two benthophagous fish species as indicators of river pollution. Environ. Toxicol. 2014, 30, 1153–1161. [Google Scholar] [CrossRef] [PubMed]
  109. Sunjog, K.; Gačić, Z.; Kolarević, S.; Višnjić-Jeftić, Ž.; Jarić, I.; Knežević-Vukčević, J.; Vuković-Gačić, B.; Lenhardt, M. Heavy Metal Accumulation and the Genotoxicity in Barbel (Barbus barbus) as Indicators of the Danube River Pollution. Sci. World J. 2012, 2012, 351074. [Google Scholar] [CrossRef] [Green Version]
  110. Morina, A.; Morina, F.; Djikanović, V.; Spasić, S.; Krpo-Ćetković, J.; Kostić, B.; Lenhardt, M. Common barbel (Barbus barbus) as a bioindicator of surface river sediment pollution with Cu and Zn in three rivers of the Danube River Basin in Serbia. Environ. Sci. Pollut. Res. 2016, 23, 6723–6734. [Google Scholar] [CrossRef]
  111. Subotić, S.; Višnjić-Jeftić, Ž.; Spasić, S.; Hegediš, A.; Krpo-Ćetković, J.; Lenhardt, M. Concentrations of 18 Elements in Muscle, Liver, Gills, and Gonads of Sichel (Pelecus cultratus), Ruffe (Gymnocephalus cernua), and European Perch (Perca fluviatilis) in the Danube River near Belgrade (Serbia). Water Air Soil Pollut. 2015, 226, 287. [Google Scholar] [CrossRef]
  112. Karadede, H.; Ünlü, E. Concentrations of some heavy metals in water, sediment and fish species from the Ataturk Dam Lake (Euphrates), Turkey. Chemosphere 2000, 41, 1371–1376. [Google Scholar] [CrossRef] [PubMed]
  113. Papagiannis, I.; Kagalou, I.; Leonardos, J.; Petridis, D.; Kalfakakou, V. Copper and Zinc in four freshwater fish species from Lake Pamvotis (Greece). Environ. Int. 2004, 30, 357–362. [Google Scholar] [CrossRef] [PubMed]
  114. Karadede-Akin, H.; Ünlü, E. Heavy metal concentration in water, sediment, fish and some benthic organisms from Tigris River, Turkey. Environ. Monit. Assess. 2007, 131, 323–337. [Google Scholar] [CrossRef]
  115. Tekin-Özan, S.; Kir, I. Seasonal variations of heavy metals in some organs of carp (Cyprinus carpio L., 1758) from Beyşehir Lake (Turkey). Environ. Monit. Assess 2008, 138, 201–206. [Google Scholar] [CrossRef]
  116. Mazej, Z.; Sayegh-Petkovšek, S.; Pokorny, B. Heavy metal concentrations in food chain of Lake Velenjsko jezero, Slovenia: An artificial lake from mining. Arch. Environ. Contam. Toxicol. 2010, 58, 998–1007. [Google Scholar] [CrossRef]
  117. Kenšová, R.; Čelechovská, O.; Doubravová, J.; Svobodová, Z. Concentrations of metals in tissues of fish from the Vĕstonice Reservoir. Acta Vet. Brno 2010, 79, 335–345. [Google Scholar] [CrossRef] [Green Version]
  118. Petkovšek, S.A.S.; Grudnik, Z.M.; Pokorny, B. Heavy metals and arsenic concentrations in ten fish species from the Šalek lakes (Slovenia): Assessment of potential human health risk due to fish consumption. Environ. Monit. Assess. 2012, 184, 2647–2662. [Google Scholar] [CrossRef]
  119. Carpene, E.; Vasak, M. Hepatic metallothionein from goldfish (Carassius auratus). Comp. Biochem. Physiol. 1989, 92B, 463–468. [Google Scholar] [CrossRef]
  120. Kargin, F.; Erdem, C. Accumulation of Copper in liver, spleen, stomach, intestine, gill and muscle of Cyprinus carpio, Doga. Turk. J. Zool. 1991, 15, 306–314. [Google Scholar]
  121. Yılmaz, A.B.; Sangün, M.K.; Yağlıoğlu, D.; Turan, C. Metals (major, essential to non essential) composition of the different tissues of three demersal fish species from İskenderun Bay, Turkey. Food Chem. 2010, 123, 410–415. [Google Scholar] [CrossRef]
  122. Coger, V.; Million, N.; Rehbock, C.; Sures, B.; Nachev, M.; Barcikowski, S.; Wistuba, S.; Strauß, S.; Vogt, P.M. Tissue concentrations of zinc, iron, copper, and magnesium during the phases of full thickness wound healing in a rodent model. Biol. Trace Elem. Res. 2019, 191, 167–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  123. Paterson, S.A.; Ralston, N.V.C.; Peck, D.V.; VanSickle, J.; Robertson, J.D.; Spate, V.L.; Morris, J.S. How might selenium moderate the toxic effects of mercury in stream fish of the western U.S.? Environ. Sci. Technol. 2009, 43, 3919–3925. [Google Scholar] [CrossRef] [PubMed]
  124. Maktabi, P.; Javaheri Baboli, M.; Jafarnejadi, A.R.; Askary Sary, A. Mercury concentrations in common carp (Cyprinus carpio) tissues, sediment and water from fish farm along the Karoun River in Iran. Vet. Res. Forum. 2015, 6, 217–221. [Google Scholar]
  125. Culha, S.T.; Yabanli, M.; Baki, B.; Yozukmaz, A. Heavy metals in tissues of scorpionfish (Scorpaena porcus) caught from Black Sea (Turkey) and potential risks to human health. Environ. Sci. Pollut. Res. Int. 2016, 23, 20882–20892. [Google Scholar] [CrossRef]
  126. Mehanna, S.F.; Abd El-Azim, H.; Belal, A.A. Impact of metal pollution, food availability, and excessive fishing on Rhabdosargus haffara stock (family: Sparidae) in Timsah lake. Environ. Sci. Pollut. Res. Int. 2016, 23, 15888–15898. [Google Scholar] [CrossRef]
  127. UNEP/OCHA. Cyanide Spill at Baia Mare, Romania; UNEP/OCHA Assessment Mission Report; United Nations Environment Programme (UNEP)/Office for the Co-ordination of Humanitarian Affairs (OCHA): Geneva, Switzerland, 2000. [Google Scholar]
  128. Triebskorn, R.; Telcean, I.; Casper, H.; Farkas, A.; Sandu, C.; Stan, G.; Colărescu, O.; Dori, T.; Köhler, H.-R. Monitoring pollution in River Mureş, Romania, part II: Metal accumulation and histopathology in fish. Environ. Monit. Assess. 2008, 141, 177–188. [Google Scholar] [CrossRef]
  129. Barlas, N. A pilot study of heavy metal concentration in various environments and fishes in the Upper Sakarya River Basin, Turkey. Environ. Toxicol. 1999, 14, 367–373. [Google Scholar] [CrossRef]
  130. Alonso, M.L.; Montaña, F.P.; Miranda, M.; Castillo, C.; Hernández, J.; Benedito, J.L. Interactions between toxic (As, Cd, Hg and Pb) and nutritional essential (Ca, Co, Cr, Cu, Fe, Mn, Mo, Ni, Se, Zn) elements in the tissues of cattle from NW Spain. BioMetals 2004, 17, 389–397. [Google Scholar] [CrossRef]
  131. Belitz, H.-D.; Grosch, W.; Schieberle, P. Lehrbuch der Lebensmittelchemie; Springer: Berlin/Heidelberg, Germany, 2001; ISBN 3-540-41096-15. [Google Scholar]
  132. Çelik, U.; Oehlenschläger, J. Zinc and copper content in marine fish samples collected from the eastern Mediterranean sea. Eur. Food Res. Technol. 2005, 220, 37–41. [Google Scholar] [CrossRef]
  133. Özden, Ö.; Erkan, N.; Ulusoy, Ş. Determination of mineral composition in three commercial fish species (Solea solea, Mullus surmuletus, and Merlangius merlangus). Environ. Monit. Assess. 2010, 70, 353–363. [Google Scholar] [CrossRef] [PubMed]
  134. Sharma, B.; Singh, S.; Siddiqi, N.J. Biomedical implications of heavy metals induced imbalances in redox systems. Biomed. Res. Int. 2014, 2014, 640754. [Google Scholar] [CrossRef] [Green Version]
  135. Gupta, V.K.; Singh, S.; Agrawal, A.; Siddiqi, N.J.; Sharma, B. Phytochemicals mediated remediation of neurotoxicity induced by heavy metals. Biochem. Res. Int. 2015, 2015, 534769. [Google Scholar] [CrossRef] [Green Version]
  136. Arnot, J.A.; Gobas, F.A. A review of bioconcentration factor (BCF) and bioaccumulation factor (BAF) assessments for organic chemicals in aquatic organisms. Environ. Rev. 2006, 14, 257–297. [Google Scholar] [CrossRef]
  137. Uysal, K.; Emre, Y.; Köse, E. The determination of heavy metal accumulation ratios in muscle, skin and gills of some migratory fish species by inductively coupled plasma-optical emission spectrometry (ICP-OES) in Beymelek Lagoon (Antalya/Turkey). Microchem. J. 2008, 90, 67–70. [Google Scholar] [CrossRef]
  138. Saha, N.; Mollah, M.Z.I.; Alam, M.F.; Rahman, M.S. Seasonal investigation of heavy metals in marine fishes captured from the Bay of Bengal and the implications for human health risk assessment. Food Control 2016, 70, 110–118. [Google Scholar] [CrossRef] [Green Version]
  139. Tao, Y.; Yuan, Z.; Xiaona, H.; Wei, M. Distribution and bioaccumulation of heavy metals in aquatic organisms of different trophic levels and potential health risk assessment from Taihu Lake, China. Ecotoxicol. Environ. Saf. 2012, 81, 55–64. [Google Scholar] [CrossRef]
  140. Bosch, A.C.; O’Neill, B.; Sigge, G.O.; Kerwath, S.E.; Hoffman, L.C. Heavy metals in marine fish meat and consumer health: A review. J. Sci. Food Agric. 2016, 96, 32–48. [Google Scholar] [CrossRef] [PubMed]
  141. Durmaz, E.; Kocagöz, R.; Bilacan, E.; Orhan, H. Metal pollution in biotic and abiotic samples of the Büyük Menderes River, Turkey. Environ. Sci. Pollut. Res. 2017, 24, 4274–4283. [Google Scholar] [CrossRef] [PubMed]
  142. Türkmen, M.; Türkmen, A.; Tepe, Y. Metal contaminations in five fish species from Black, Marmara, Aegean and Mediterranean seas, Turkey. J. Chil. Chem. Soc. 2008, 53, 1424–1428. [Google Scholar] [CrossRef] [Green Version]
  143. Türkmen, M.; Türkmen, A.; Tepe, Y.; Töre, Y.; Ateş, A. Determination of metals in fish species from Aegean and Mediterranean seas. Food Chem. 2009, 113, 233–237. [Google Scholar] [CrossRef]
  144. Türkmen, A.; Tepe, Y.; Türkmen, M. Determination of metals in tissues of fish species from Hurmabogazı Lagoon. Indian J. Mar. Sci. 2016, 45, 277–282. [Google Scholar]
  145. Griboff, J.; Wunderlin, D.A.; Monferran, M.V. Metals, As and Se determination by inductively coupled plasma-mass spectrometry (ICP-MS) in edible fish collected from three eutrophic reservoirs. Their consumption represents a risk for human health? Microchem. J. 2017, 130, 236–244. [Google Scholar] [CrossRef]
  146. Jarup, L. Hazards of heavy metal contamination. Br. Med. Bull. 2003, 68, 167–182. [Google Scholar] [CrossRef] [Green Version]
  147. Ko, L.Y.Y. A pilot study on the effect of heavy metals detoxification in children with chronic allergy. In Proceedings of the 6th Asia Pacific Congress of Allergology and Clinical Immunology, Tokyo, Japan, 4–7 October 2004. [Google Scholar]
  148. Alam, M.; Tanaka, A.; Allinson, G.; Laurenson, L.; Stagnitti, F.; Snow, E. A comparison of trace element concentrations in cultured and wild carp (Cyprinus carpio) of Lake Kasumigaura, Japan. Ecotoxicol. Environ. Saf. 2002, 53, 348–354. [Google Scholar] [CrossRef] [PubMed]
Figure 1. The process of metal bioaccumulation in the aquatic trophic chain.
Figure 1. The process of metal bioaccumulation in the aquatic trophic chain.
Fishes 08 00387 g001
Figure 2. Romanian part of the Danube River sector, between Baziaş and the Black Sea [33].
Figure 2. Romanian part of the Danube River sector, between Baziaş and the Black Sea [33].
Fishes 08 00387 g002
Figure 3. Bioaccumulation of As, Cd, and Pb in the muscle of some fish species.
Figure 3. Bioaccumulation of As, Cd, and Pb in the muscle of some fish species.
Fishes 08 00387 g003
Figure 4. Metal bioaccumulation in some fish muscle (sectors I and II).
Figure 4. Metal bioaccumulation in some fish muscle (sectors I and II).
Fishes 08 00387 g004
Table 1. National water quality criteria and standards for heavy metals in surface water [50].
Table 1. National water quality criteria and standards for heavy metals in surface water [50].
CategoryClass IClass IIClass IIIClass IVClass V
Cd (µg/L)0.5125>5
Co (µg/L)102050100>100
Cr total (µg/L)2550100250>250
Cu (µg/L)203050100>100
Ni (µg/L)102550100>100
Pb (µg/L)5102550>50
Zn (µg/L)1002005001000>1000
Table 2. Water quality status based on the Water Quality Index (WQI).
Table 2. Water quality status based on the Water Quality Index (WQI).
WQI ValuesStatus
0–25Excellent (I)
26–50Good (II)
51–75Poor (III)
76–100Very poor (IV)
>100Unsuitable for drinking (V)
Table 3. The standard value of some metal concentrations in the sediment according to Romanian Order 161/2006 [50].
Table 3. The standard value of some metal concentrations in the sediment according to Romanian Order 161/2006 [50].
Standard Value (mg/kg)
Cd0.8
Cu40
Pb85
Zn150
Ni35
Table 4. Maximum metal limits in fish muscles according to international standards [55].
Table 4. Maximum metal limits in fish muscles according to international standards [55].
OrganizationMetals (mg/kg)
AsCdCrCuFeHgNiPbZn
FAO (1983)1.00.050.15–1.0301000.5800.230
FAO/WHO limit (1989) 0.5 -- 0.5
European Commission Regulation EC No. 1881/2006 0.05 --0.5 0.3
Decree No. 365/2001 0.05 -- 0.2
Heavy Metals Regulations Legal Notice No. 66/2003 0.05 0.5 0.2
Table 7. The value of each metal concentration in the fish tissue (µg/g).
Table 7. The value of each metal concentration in the fish tissue (µg/g).
TissuesAsCdCrCuFeHgNiPbZnYearsRef.Sect
Common carp (Cyprinus carpio)
M0.010.01---0.24-0.048-2013[68]I
0.2580.059-0.6889.380.393-0.0596.162013[94]I
0.3330.082-0.7579.680.466-0.0846.172013[94]I
0.660.0050.011.319.620.89--59.012010[95]I
0.395---7.42---54.702010[96]I
0.66----0.89--54.232010[48]I
0.0550.016---0.234-0.014-2010[97]I
0.0130.014---0.207-0.036-2012[66]I
-0.01---0.5-0.16-2018[96]I
-0.084-5.10---0.5842.22008[98]IV
-0.010-3.22---0.3839.202008[98]V
0.412-1.14351.291-0.23151.68550.1445-2013–2014[99]V
-----0.054---2014[85]V
Int0.020.10---0.22-0.21-2013[68]I
0.0160.103---0.207-0.266-2012[66]I
---13.5--0.9-6442003–2013[100]V
G0.290.030.011.90139.260.89--1186.32010[97]I
----261.97---1773.762010[96]I
---4.33--<0.03-6742003–2013[101]V
---6.13--9.5-8722003–2013[101]V
Skin---3.98--<0.03-2632003–2013[101]V
---3.15--12.9-4852003–2013[101]V
L0.490.280.0133.49141.441.63--325.3772010[95]I
---21.97418.36---582.792010[96]I
0.020.13---0.22-0.06-2013[68]I
0.0180.132---0.206-0.047-2012[66]I
0.48----0.63--325.372010[48]I
---73.3--4.41-4502003–2013[101]V
---110--8.17-2432003–2013[101]V
---89.9--2.46-1892003–2013[101]V
Gon----6.28---74.532010[96]I
Crucian carp (Carassius carassius, Carassius gibelio)
M0.0310.017---0.087-0.052-2010[97]I
0.1390.057-0.8098.050.094-0.03011.162013[94]I
0.1720.051-0.8247.250.139 0.04010.262013[94]I
0.6045-1.3451.4115-0.32.24650.1835-2013–2014[99]V
0.5985-1.20851.5005-0.2671.9940.1675-2013–2014[99]V
-----0.0255---2014[79]V
-----0.073---2014[79]V
---0.715-0.15--11.722007[102]V
Freshwater bream (Abramis brama)
M0.160.0040.230.22.310.160.020.213.152011–2013[80]I + II
0.210.0040.20.142.320.080.020.253.92011–2013[80]I + II
0.150.0040.260.171.660.150.050.234.642011–2013[80]I + II
1.73-0.261.139.72--0.08-2014[103]I
0.46-0.301.4114.23--ND-2014[103]I
ND-0.330.6627.64--ND-2014[103]I
ND-0.191.4915.40--ND-2014[103]I
ND---1.31---23.842010[96]I
0.0350.018---0.237-0.030-2010[97]I
0.1090.021-0.70713.60.110-0.0199.062013[94]I
0.1540.027-0.71713.540.161-0.0289.022013[94]I
-0.01---0.17-0.08-2018[96]I
-0.053-2.77---0.2733.272008[98]IV
---2.15---0.2935.772008[98]V
0.2375-0.9621.889-0.23952.67350.1685-2013–2014[99]V
-----0.02–0.035---2014[79]V
L0.22-0.2544.25177.56--0.20-2014[103]I
0.14-0.1822.07225.11--0.05-2014[103]I
ND-0.2044.06190.35--0.47-2014[103]I
ND-0.2164.66177.74--0.11-2014[103]I
ND--14.14213.53---66.772010[96]I
GND-1.322.11428.22--0.23-2014[103]I
3.2-0.910.85158.45--0.12-2014[103]I
ND-3.711.76167.64--ND-2014[103]I
ND-0.760.98117--ND-2014[103]I
ND--ND369.21---59.852010[96]I
Gon1.75-0.081.1620.67--0.08-2014[103]I
1.21-0.181.5433.80--0.08-2014[103]I
1.61-0.101.3128.12--0.09-2014[103]I
1.04-0.210.8129.26--ND-2014[103]I
0.15--ND19.24---137.762010[1]I
Grass carp (Ctenopharyngodon idella)
M0.0390.018---0.367-0.034-2010[97]I
W.B.48.5-0.03-11.6<7.3109-15.42011[104]I
Silver carp (Hypophthalmichthys molitrix)
MND--ND12.53---31.902010[96]I
0.0180.015---0.441-0.015-2010[97]I
0.0360.014---0.140-0.048-2012[66]I
0.040.01---0.16-0.056-2013[68]I
L0.080.21---0.20-0.14-2013[68]I
0.21--188.78511.72---222.402010[96]I
0.0730.191---0.185-0.125-2012[66]I
GND--ND211.88---73.722010[96]I
Int0.0650.062---0.253-1.518-2012[66]I
0.070.07---0.26-1.3-2013[68]I
W.B.58.7-0.24-51.4<13284-82.52011[105]I
Pontic shad (Alosa immaculata)
M7.7250.433-4.07440.346---66.0982007–2008[65]III
12.60.17-3.45143.26--0.1358.42010[106]III
6.530.31-15.5269--0.3544.12010[106]III
-0.091-5.34---0.6544.552008[98]IV
-0.012-3.3---0.4541.452008[98]V
L9.420.8-34.21225--0.2783.52010[106]III
6.3890.714-20.003751.814---99.7592007–2008[65]III
G1.630.219-2.987289.506---80.5072007–2008[65]III
Wels catfish (Silurus glanis)
M0.10.090.1450.070.950.330.0740.177.622011–2013[80]I + II
0.090.0010.130.071.330.20.0160.182.972011–2013[80]I + II
0.110.0040.140.070.550.620.030.1632011–2013[80]I + II
NDNDNDNDNDNDNDND7.912010[96]I
0.0340.02---0.235-0.032-2010[97]I
0.220.010.081.4227.061.63--20.812011[97]I
0.0030.008---0.327-0.014-2012[66]I
0.1310.0040.1380.94919.461.5980.1200.00619.622013[100]I
0.0030.01---0.53-0.06-2013[68]I
0.1600.068-1.558.320.208-0.0587.062013[94]I
0.2110.069-1.628.170.260-0.0696.682013[94]I
0.7635-3.6381.9455-0.2351.823–4.0890.145–0.382-2013–2014[99]V
-----0.014–0.042---2014[79]V
GND--160.1154.93---53.772010[96]I
0.160.070.061.9874.881.50--58.052010[97]I
0.008-0.2704.460163.00.3280.1700.23680.422013[107]I
0.1170.0050.0900.41243.980.0710.2110.38769.812013[100]I
LND--ND412.29---38.692010[96]I
0.240.020.048.37396.161.90--41.522010[97]I
0.0040.064---0.143-0.034-2012[66]I
0.096-0.01017.77745.70.6390.0600.06793.142013[107]I
0.0050.12---0.23-0.10-2013[68]I
Int0.0050.101---0.167-0.036-2012[66]I
0.0060.14---0.30-0.10-2013[68]I
Skin0.3600.0050.1541.90225.860.6570.2440.00958.952013[100]I
W.B< 29-0.062-13.7<3.184-12.42011[105]I
Gon0.960-0.1002.20099.290.1140.2200.018134.32013[107]I
Pike-perch (Sander lucioperca)
M0.110.0030.180.090.810.150.010.252.742011–2013[80]I + II
0.130.040.180.112.350.30.0160.233.762011–2013[80]I + II
0.150.0020.110.114.630.280.080.183.072011–2013[80]I + II
0.0320.018---0.173-0.043-2010[97]I
0.170.0050.0430.7517.971.32--15.142010[95]I
0.199–0.219-0.708–1.5870.979–1.244-0.205–0.2232.084–3.5430.091–0.143-2013–2014[99]V
-----0.016–0.041---2014[79]V
L0.500.020.046.18241.071.66--58.372010[95]I
G0.250.010.021.0173.011.52--40.112010[95]I
Barbel (Barbus barbus)
M0.84--4.811.122.15--10.062010[108]I
1.4--NDND---12.892010[109]I
1.57-0.411.90-0.270.190.1118.372012[110]I
0.1890.052-0.82612.220.222-0.0485.22013[94]I
0.2390.062-0.83911.910.325-0.0626.022013[94]I
L1.4880.014-19.6374.81-14.88-25.652010[108]I
0.54--27.4978.82---47.082010[109]I
1.74-0.3725.85-0.090.160.1259.502012[110]I
G0.001--12.15106.221.1870.96-40.592010[108]I
0.59--ND120.91---47.852010[109]I
0.85-0.642.68-0.020.22ND68.332012[110]I
Gon1.41--NDND---71.692010[109]I
M-0.01---0.09-0.15-2018[111]I
Int1.80-0.575.81-ND0.330.3749.762012[110]I
Northern pike (Esox lucius)
M.0.0300.015---0.236-0.036-2010[97]I
0.1050.023-0.54810.100.106-0.0325.102013[94]I
0.1530.036-0.5749.970.162-0.0375.172013[94]I
-0.044-2.9---0.3623.92008[98]IV
---1.5---0.2621.922008[98]V
0.173–1.199-0.781–2.0710.901–2.696-0.182–0.4281.892–3.6010.060–0.270-2013–2014[99]V
-----0.021–0.058---2014[79]V
European perch (Perca fluviatilis)
M1.00ND0.090.4511.852.72ND-18.892011[111]I
-0.034-3.85---0.1932.332008[98]IV
---1.25---0.3332.362008[98]V
0.150–0.341-0.248–3.0631.588–2.319-0.190–0.4171.252–3.3530.182–0.582-2013–2014[99]V
-----0.012–0.038---2014[79]V
---0.26–0.37-0.29–0.35--6.13–6.362007[102]V
L3.03ND0.1118.202252.52ND-77.662011[111]I
G1.11ND0.250.66189.391.84ND-64.822011[111]I
Gon1.43ND0.112.2153.981.19ND-68.062011[111]I
M—muscle, L—liver, Gon—gonads, G—gills, Int—intestine, W.B.—whole body, ND—not detected.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Cordeli, A.N.; Oprea, L.; Crețu, M.; Dediu, L.; Coadă, M.T.; Mînzală, D.-N. Bioaccumulation of Metals in Some Fish Species from the Romanian Danube River: A Review. Fishes 2023, 8, 387. https://doi.org/10.3390/fishes8080387

AMA Style

Cordeli AN, Oprea L, Crețu M, Dediu L, Coadă MT, Mînzală D-N. Bioaccumulation of Metals in Some Fish Species from the Romanian Danube River: A Review. Fishes. 2023; 8(8):387. https://doi.org/10.3390/fishes8080387

Chicago/Turabian Style

Cordeli (Săvescu), Anca Nicoleta, Lucian Oprea, Mirela Crețu, Lorena Dediu, Marian Tiberiu Coadă, and Diana-Nicoleta Mînzală. 2023. "Bioaccumulation of Metals in Some Fish Species from the Romanian Danube River: A Review" Fishes 8, no. 8: 387. https://doi.org/10.3390/fishes8080387

Article Metrics

Back to TopTop