Toxic Effect On Fish

11/28/2023 Toxics | Free Full-Text | Toxic Effects of Cadmium on Fish
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Citations 16
Table of Contents 

Abstract


Introduction

Detection
Share

Methods
Open Access Review
and
Toxic Effects of Cadmium on Fish
Accumulation Help
Effects
byof
Cite
Yinai Liu (https://sciprofiles.com/profile/author/R2JmOFcyS3NNcEYwVWd4QnY4WnpnR2Q5bHRkUkFvdWFtSE5CK0RW


Cadmium
†, in
Fish
Qianqian Chen (https://sciprofiles.com/profile/author/MkFOL3hISWk2TlFlY1lLL2txRmdOVS9PcnJGeUxhTGFSZ1pqaFR6
Discuss in
† SciProfiles
, Toxic
(https://s
Effects Li (https://sciprofiles.com/profile/1991420?utm_source=mdpi.com&utm_medium=website&utm_campaign=avatar_
Yaoqi
groups/p
, of utm_sou

Cadmium
Liuliu Bi (https://sciprofiles.com/profile/author/YVkwSGFRZ2FJVTNqTUdKS1BMYkZzanRVbTJwNW5vT0VwZC95eWZRd
Accumulation
,
on Endorse

Libo Jin (https://sciprofiles.com/profile/1814719?utm_source=mdpi.com&utm_medium=website&utm_campaign=avatar_
Fish
*  (mailto:please_login) and
Renyi Peng (https://sciprofiles.com/profile/1771271?utm_source=mdpi.com&utm_medium=website&utm_campaign=ava

Comment
*  (mailto:please_login)
Institute of Life Sciences & Biomedicine Collaborative Innovation Center of Zhejiang Province, College of Life and Environmental
Science, Wenzhou University, Wenzhou 325035, China Back to TopTop
 
 * Mechanism
Authors to whom correspondence should be addressed.
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† of
These authors contributed equally to this work.

the
Toxic
Toxics 2022, 10(10), 622; https://doi.org/10.3390/toxics10100622 (https://doi.org/10.3390/toxics10100622)
Effects
Received:
of 31 August 2022 / Revised: 6 October 2022 / Accepted: 17 October 2022 / Published: 19 October 2022

Cadmium
(This article belongs to the Section Ecotoxicology (/journal/toxics/sections/ecotoxicology))
Exposure
on  Share

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Conflicts
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of
Abstract

Interest
Large amounts of enriched cadmium (Cd) in the environment seriously threatens the healthy and sustainable development of the
Abbreviations
aquaculture industry and greatly restricts the development of the food processing industry. Studying the distribution and toxic
References
effects of Cd in fish, as well as the possible toxic effects of Cd on the human body, is very significant. A large number of studies

have shown that the accumulation and distribution of Cd in fish are biologically specific, cause tissue differences, and seriously
damage the integrity of tissue structure and function, the antioxidant defense system, the reproductive regulation system, and the
Share

immune system. The physiological, biochemical, enzyme, molecular, and gene expression levels change with different
concentrations and times of Cd exposure, and these changes are closely related to the target sites of Cd action and tissues in fish.
Therefore, the toxic effects of Cd on fish occur with multiple tissues, systems, and levels. Help
Keywords: aquatic ecosystems (/search?q=aquatic+ecosystems); food chain (/search?q=food+chain); cadmium

accumulation (/search?q=cadmium+accumulation); cadmium toxicity (/search?q=cadmium+toxicity); oxidative stress
Cite

(/search?q=oxidative+stress)
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 
Graphical Abstract
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1. Introduction

Cadmium (Cd), a toxic and nonessential transition metal, is a major threat to common organisms in aquatic ecosystems and
has been widely recognized as a major pollutant in waters worldwide, and Cd travels up the food chain, eventually threatening
human health, thus, Cd poses health risks to both humans and animals [1,2,3,4]. Cd causes a wide range of toxicological effects,
Share


including stomach cramps, vomiting, diarrhea, hematuria, kidney failure, and other symptoms. The Joint Expert Committee on
Food Additives (JECFA) has stipulated that the allowable weekly intake limit of Cd for humans is 7 μg/kg, and exceeding the limit
harms human health [1,5]. Epidemiological data suggest that environmental Cd exposure may be associated with various types Help of
cancer and is also an important factor in osteoporosis [6,7]. Moreover, the liver and kidney are extremely sensitive to Cd toxicity,
probably due to the ability of these tissues to synthesize metallothionein (MT), which is a Cd-induced protein that protects cells Cite by

tightly binding toxic Cd ions, thereby resulting in oxidative stress, this may be a cause of several liver and kidney diseases [8].
Cd has several characteristics, including high environmental toxicity, easy accumulation, and poor degradation. For
organisms, Cd displays toxic effects on many organs, and Cd pollution is not easily found, however, Cd is easily enriched and
Discuss in
can
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
transmit its toxic effects through the food chain [9]. Cd pollution in the environment is caused by the development and utilization(https://s
of
chemical fertilizers in agriculture, metals and minerals in industry, and the use of some industrial products containing Cd, which groups/p
may be discharged into water with wastewater. Even if the concentration of Cd is sometimes low, it can accumulate in algaeutm_sou and
sediment, be absorbed by fish, shellfish, shrimp, and crabs in water, be concentrated through the food chain, and eventually enter
the human body [1,10,11,12]. Endorse

As fish are among the most important sources of food protein for human beings, it is highly likely that Cd can be enriched in
fish and transferred into the human body through the food chain. Cd accumulation causes damage to the cardiovascular, immune,
Comment
reproductive, and nervous systems in the body [13]. At the same time, it disrupts the cell cycle, proliferation, differentiation, and

DNA replication and repair at the cellular level and then affects the apoptosis pathway [14,15]. Fish are an essential group of
organisms in the aquatic ecosystem that are at the top of the food chain and are very sensitive to Cd pollution. If fish are exposed
to Cd pollution for a long time, their different tissues will absorb and accumulate Cd, thus affecting the structure and function of the
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 
gills, liver, and gonad. Furthermore, Cd affects their physiological metabolism and reproductive and immune systems and
(/)
eventually leads to metabolic disorders, physical disorders, or even death [16,17,18]. Recently, studies have shown that Cd can

induce various epigenetic changes, thus, changes occur in the chemical modification of DNA, histones, and chromatin, but not the
sequence of DNA nucleotides, including DNA methyltransferase, histone acetyltransferase, histone deacetylase, histone
methyltransferase, and microRNA. As a result, fish incur a greater risk of disease and development of various types of cancer
[18,19,20,21]. Therefore, using these indicators to indicate the impact that Cd pollutants have on the environment is an effective
way to evaluate the safety of the ecosystem.
The toxic effects of Cd exposure in different fish are not the same. Adult male and female Japanese medaka were exposed 
Share
to
the non-lethal consequences of Cd, with 0–10 ppb concentration for 7 weeks, and the results displayed that gonadal steroid
release was significantly decreased, while female plasma estradiol levels altered more significantly. Meanwhile, physiological
Help

response to Cd exposure along the hypothalamus–pituitary–gonadal axis, including the hepatic estrogen receptor, plasma
vitellogenin, plasma steroids and gonadal–somatic indices, were more sensitive than the reproductive and developmental
endpoints, and the reproductive and physiological endpoints for adult medaka pairs exposed to Cd for 7 weeks are shown in Table
Cite
1 [22].

Discuss in
Table 1. Reproductive and physiological endpoints for adult medaka pairs exposed to Cd for 7 weeks. Adapted SciProfiles
with
permission from [22]. Copyright 2003, Elsevier Inc. All rights reserved. (https://s
groups/p
utm_sou

Endorse
When Oreochromis aureus were exposed to 0.5–10 ppm Cd, their food consumption showed a dramatic decrease, which

Comment
would take 21 days to return to normal after fish were returned to Cd-free water, however, Cd was still in tissues for 34 days, and
the accumulation was highest in the kidney after the fish were placed in Cd-free water [23]. Juvenile parrotfish, Oplegnathus
fasciatus, were exposed to Cd mixed with a fish diet, and the result displayed that tissue Cd concentrations increased with the Cd
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 
content of the diets, and Cd accumulated the most in the liver, followed by the gill and then muscle [24]. Because zebrafish (Danio
(/)
rerio) share 87% genetic homology with humans, their embryos, larvae, and adult fish are employed as standard models for many
toxicity tests, and a summary of the toxic effects of cadmium in zebrafish is shown as Table 2 [25].

Table 2. Summary of toxic effects of cadmium in zebrafish. Reproduced with permission from [25]. Copyright 2021, Korean
Society of Toxicology.
Share
Help
 Cite

2. Detection Methods and Accumulation Effects of Cadmium in Fish
2.1. Cadmium Accumulation Induces Cytotoxicity in Fish
Discuss in
Studies have shown that Cd can enter cells through calcium ion channels. Cd and calcium (Ca) are both divalent metal ions.
SciProfiles
(https://s
The radius of Cd2+ (0.097 nm) is similar to that of Ca2+ (0.099 nm), and Cd2+ has a higher affinity for anion binding sites in calcium
groups/p
ion channels than that of Ca2+, thus, Cd2+ can directly inhibit the active transport of Ca2+ for cells by competing with Ca2+. After
utm_sou
Cd2+ enters cells, the physiological processes related to Ca2+ can be affected [46,47]. For example, Cd2+ can inhibit the outflow of
Ca2+ by competing with Ca2+ for the binding site of Ca2+-ATPase, resulting in an increase in the intracellular Ca2+ concentration
[48]. At the same time, Cd2+ can function as a substitute for Ca2+ to bind calmodulin (CaM), activate CaM-dependent kinases

Endorse or
Cd2+ can replace Ca2+ to bind to microtubules, microfilaments, and actin, destroy tight junctions and gap junctions betweenComment
directly activate its related enzymes, interfere with intracellular Ca2+-related signaling, and cause cytotoxicity [49,50]. In addition,
cells,
damage cytoskeleton integrity, and ultimately affect the basic functions of cells [46,51,52]. Cd can induce cell apoptosis in two
ways. First, Cd can bind to GSH rich in sulfhydryl groups on the mitochondrial membrane, causing proton (H+) influx, Ca2+
overload, and oxidative phosphoric acid uncoupling, which further leads to a decrease in the mitochondrial membrane potential,
leads to the activation of Ca2+/Mg2+-dependent endonuclease (DNase I), and finally induces cell apoptosis [53,54]. Second, Cd
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 
can also lead to the release of cytochrome c and other apoptosis-related factors and increase the activity of caspases by inducing
(/)
the opening of the mitochondrial permeability transition pore, which eventually leads to apoptosis [55,56]. In addition, Cd plays an

important role in the induction of apoptosis by upregulating the expression of a series of proto-oncogenes [57]. The lethal effects of
cadmium on different fish species are shown as Table 3.
Table 3. Table of lethal effects of cadmium on different fish species.
Share
Help
2.2. Test Method for Cadmium Accumulation in Fish Cite
Usually, there are multiple methods to detect the content of Cd in living organisms, and each method exhibits its own
advantages and disadvantages. In the natural state, Cd mainly exists in the ionic state, but after entering the fish, most Cd  ions
Discuss in
SciProfiles
quickly combine with metallothionein to form organic complexes, and a small part forms coordination compounds with nucleosides,
(https://s
proteins, and other substances in the body through ionic bonds [71,72]. At present, the methods used for detecting Cd in fish are
groups/p
usually atomic absorption spectroscopy (AAS) and inductively coupled plasma (ICP), the former includes graphite furnace atomic
utm_sou

absorption spectrometry (GFAAS) and flame atomic absorption spectrometry (FAAS), and the latter includes inductively coupled
plasma‒mass spectrometry (ICP‒MS) and inductively coupled plasma optical emission spectrometry (ICP‒OES) [73,74]. GFAAS
has been widely used in the determination of Cd, due to its high sensitivity, low detection limit, and small sample amount, however,
Endorse
this method also has certain limitations, such as being susceptible to the influence of ash temperature, atomization temperature,
matrix modifier condition, and the content of Cd in the sample. The FAAS method, which exhibits a high sensitivity, strong  anti-
Comment
interference ability, high precision, and good selectivity, is suitable for detecting the content of trace heavy metals, including Cd.
The ICP‒MS method is widely used in determining the content of metal elements due to its advantages, including a strong anti-
interference ability, low detection limit, high accuracy, good precision, convenient detection process, and accurate detection of low
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 
metal content. ICP‒OES has several advantages, including a wide linear range and a rapid and convenient detection process, but
(/)
it is easily interfered with by spectrum and matrix effects [73,74,75].
2.3. The Accumulation of Cadmium in Fish Was Influenced by Feeding Habits and Routes

The degree of Cd accumulation in fish has a strong relationship with the fish feeding type. In the aquatic food chain, a step-by-
step amplification effect, with increasing trophic levels, is observed for Cd accumulation. Considering the different cumulative

effects of Cd on different feeding fish, the average accumulation coefficient of Cd in fish tissues can be generally arranged as
omnivorous > carnivorous > herbivorous. The average accumulation coefficient of Cd, from largest to smallest, in the tissues of fish
Share

that live in different water layers is generally the bottom fish, middle and lower fish, and middle and upper fish, which may be due
to a variety of factors, such as the position of the fish in the food chain and their metabolic capacity [76,77,78]. For instance,
herbivorous fish mostly live in the upper and middle layers of water and mainly feed on phytoplankton or aquatic plants.Help The
accumulation of Cd is mainly derived from intestinal food digestion. Omnivorous and carnivorous fish mostly inhabit the middle and
lower layers of water and feed on small fish, aquatic insects, and shrimp, and they are exposed to Cd in the water environmentCite and
sediments, thus, the Cd accumulation in omnivorous and carnivorous fish is higher because they may ingest large amounts of Cd-
containing sediments during feeding in the lower water [76,78]. 
Discuss in
The feeding route is another important factor that affects the accumulation and distribution of Cd in fish [79]. Cd is absorbed
SciProfiles
with water or foods and transported through the blood circulation to migrate and distribute in the different tissues and organs (https://s
of
fish. After being absorbed with water and transported through the blood circulation, Cd is mainly enriched in detoxifying organs, groups/p
such as the kidney and liver, but when ingested with foods, Cd is mainly enriched in intestinal tissues, due to digestionutm_sou and
with water and foods displays gradual decreases in different organs or tissues. When absorbed with water, Cd ions are directly 
absorption in the intestine [80]. However, along with migration and distribution in fish, the accumulation of Cd that is both absorbed
Endorse

absorbed by gills in a dissolved state, and the accumulation of Cd in different tissues is generally in the following descending order:
kidney, liver, intestine, gill, and muscle [81,82]. While absorbed with foods, they are absorbed by the digestive system, and the Cd
Comment
accumulation in different tissues is generally in the following order, from high to low: intestine, kidney, liver, gill, and muscle
[81,82,83]. The accumulation and distribution of Cd in fish were slightly different with different exposure methods. In order to
assess health risk of some heavy metals, including Cd, from canned tuna and fish in Tijuana, Mexico, Rodriguez-Mendivil et al.
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 
diaplayed the range, mean concentrations, and incidence of occurrence in four species of fish for Cd in the analyzed samples in
(/)
Table 4 [84].
Table 4. Minimum, maximum, mean, and standard deviation (SD) of Cd in canned tuna samples and fresh fish samples
(mg/kg ww). Adapted with permission from [84]. Copyright 2019, Health Scope.


Share
Help
3. Toxic Effects of Cadmium Accumulation on Fish Cite

3.1. Cadmium Toxicity Damages Fish Tissue Structure
When fish are exposed to Cd for a long time, their organs or tissues become pathologically damaged, which can even lead to
Discuss in
inflammation or necrosis [83]. The physiological functions of gills include regulating osmotic pressure, gas exchange, ion transport,
SciProfiles
acid-base balance, and excretion of metabolites, which play a key role in physiological, biochemical, and metabolic activities (https://s
groups/p
[85,86]. Gills are the first targets of Cd in water, through which fish continuously absorb Cd ions during respiration, and the
utm_sou

absorbed Cd ions first accumulate in the surface cells of the gill tissue and are then transported through the blood to various
organs or tissues. Therefore, Cd first has a toxic effect on the gill tissue structure of fish, leading to inflammation, apoptosis,
necrosis, and so on [87,88]. Under Cd ion stress conditions in water, the structure of cells in gills changes, as well as the activities
Endorse
concentration and time of Cd exposure, the problems, regarding inflammation, apoptosis, and necrosis, of gill tissue cells became
more serious, and the lesions of the tissue structure became more obvious [89,90]. Evidence has shown that Lates calcarifer was

of ion transport and ATPase, thus, the ability of gills to regulate osmotic pressure and ion transport is affected. With the increase in
Comment
exposed to 20.12 mg/L Cd for 48 h, resulting in aneurysm lesions in gill tissue. With the extension of exposure time, obvious
pathological lesions, including hyperplasia, occurred in gill tissue at 72 h and 96 h [91]. The pathological changes in gill tissue
caused by Cd mainly included cell proliferation, gill lamellae bending, aneurysm and cell shedding, and oxidative damage, such as
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 
vacuolization and swelling of mitochondria, and with the increase in Cd exposure dose and time, the problems became more
(/)
obvious [88]. On the one hand, gill tissue lesions impact physiological function. On the other hand, the lesions also act a defense
mechanism against Cd stress, as the distance that Cd must travel, the blood circulation is increased through the change in gill
tissue structure, and to some extent, Cd can be prevented from entering other tissues in fish [92]. 
The liver, as the main detoxifying organ of fish, mainly protects the body from damage, turning heavy metals into less toxic
substances, which are excreted from the body (Figure 1) [93]. Usually, Cd ions in the water environment first enter the fish body

through gill respiration, then accumulate in the liver through the blood circulation system, and finally redistribute in various tissues.
If fish are exposed to water that contains Cd ions for a long time, the Cd content in the liver exceeds its detoxification capacity,Share
which affects the structural and functional integrity of fish liver tissue to different degrees [94,95]. With the increase in Cd
concentration, the degree of irreversible damage to the structure of fish liver cells also increases significantly, which mainly Help

includes endoplasmic reticulum expansion, nuclear deformation, nuclear membrane mitochondrial swelling, distortion, granular
cytoplasm, and cell edema and cavitation. When the liver tissue structure is destroyed, the detoxification ability of the liver is
significantly reduced, which has an irreversible impact on growth, reproduction, and survival [17,95,96]. Cite

Discuss in
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(https://s
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utm_sou

Endorse
Figure 1. Schematic diagram of toxic effects of Cd on fish organs.


Comment
3.2. Cadmium Toxicity Damages Fish Reproduction, Development and Endocrine System
Cd exposure seriously damages the reproductive system of fish. When exposed to Cd for a long time, the cellular structure
and function of ovarian tissue or sperm tissue is significantly damaged, causing the reproductive ability of fish to Back
reduce, the
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 
development of hatched embryos to be incomplete, and the growth and development of juvenile fish to be significantly retarded
(/)
(Figure 1) [97,98]. Cd not only destroys the structural and functional integrity of fish gonads, but also affects the reproductive
regulation system of fish by affecting the expression and secretion of hormones [99,100]. On the one hand, Cd can affect the
expression and secretion of endocrine hormones, mainly by affecting the synthesis and secretion of hormones related to the 
hypothalamic–pituitary–gonadal (HPG) axis, and Cd also directly inhibits the expression of estrogen receptors [22,101]. For
example, under Cd exposure, the expression of estrogen receptors in the gonads of Oncorhynchus mykiss was significantly
inhibited, which affected the downstream pathways involved in estrogen receptors, resulting in disordered yolk production,
abnormal egg development, and finally, reproductive abortion [102,103]. In addition, after Cd ion exposure, the pituitary gland
Share

secreted gonadotropin abnormally, resulting in the secretion of estrogen disorder and, finally, reducing the reproductive ability of
fish. In addition to the direct inhibition of estrogen receptor expression, Cd can also bind to estrogen receptors in the form of
Help

estrogen analogs, thereby reducing the concentration of estrogen receptors in the gonads [31,102,104]. On the other hand, Cd can
also affect the content of sex hormones in fish serum by inhibiting the synthesis of sterols, which has been demonstrated in mullet
and guppies, in which the offspring numbers and survival rates were decreased under Cd stress conditions [103,105]. In addition,
Cite
Cd can damage the genesis and maturation of germ cells, and high concentrations of Cd can reduce sperm motility and sperm
number [106]. Zebrafish is a standard model animal for toxicity assessment, and studies showed that, after zebrafishDiscuss 
were in
SciProfiles
exposed to Cd solution, the gonad somatic index (GSI) of the ovary and seminal gland decreased significantly [18]. Cd mainly
(https://s
causes developmental abnormalities in zebrafish embryos, and the toxicity results of Cd in zebrafish are summarized in Table 2.
groups/p
3.3. Cadmium Toxicity Damages the Immune System of Fish utm_sou
The toxic effect of Cd on the fish immune system mainly occurs on the nonspecific immune system, and this affect mainly

results in the inhibition of the number of white blood cells, the proliferation of lymphocytes, the phagocytosis rate of neutrophils,
Endorse
and the activity of macrophages [107,108]. The hemolymph system is an important target of Cd toxicity, and Cd exposure affects
the organizational structural integrity of the fish hemolymph system and causes dysfunction, thereby resulting in an 
Comment
immunosuppressive effect [109,110]. Both in vitro and in vivo toxicity tests on Ictalurus melas showed that the proliferation of
lymphocytes was significantly inhibited when the concentration of Cd used for exposure was higher than 2 μmol/L [111]. It has
been found that exposure to high concentrations of Cd can inhibit the activities of lysozyme, alkaline phosphatase, and acid
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 
phosphatase in the liver of yellow catfish [112]. In addition, Cd can induce the proliferation of neutrophils in zebrafish larvae, and
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the secreted neutrophils will gradually accumulate in the inflammatory site of liver tissue (Figure 1) [113].
The other pathways that inhibit the nonspecific immune system, due to Cd exposure, inhibit the synthesis of essential trace
elements [114]. Chronic exposure to environmental cadmium affects growth and survival, cellular stress, and glucose metabolism 
in juvenile channel catfish (Ictalurus punctatus) [115]. Because both zinc and copper are essential trace elements for organism
immunity, if the zinc content is insufficient in an organism, the coefficient of the thymus, spleen, lymph node, and other organs will
be reduced, and the cellular immune function will be reduced. Furthermore, if the copper content in the organism is deficient,
humoral and cellular nonspecific immune functions will be reduced [114,116,117,118]. 
Share
3.4. Cadmium Toxicity Damages the Energy Metabolism System of Fish

Energy metabolism plays an essential role in the growth and survival of organisms and is the basis of various life processes,
Help
such as proliferation and development, immune stress, and osmotic pressure regulation [19,119]. Cd can change ATPase activity
and affect the function of ion channels. Studies have found that the activities of Ca2+-ATPase are inhibited as a result ofCitethe
decrease in Ca2+ concentration in blood, which may be because Cd competitively binds to calcium channels in the gills after Cd
exposure [120,121]. Researchers found that the activities of Na+/K+-ATPase in gills could be inhibited when the concentration of
Cd in water was up to 1 mg/L, and the reason was that a large number of free radicals oxidize the amino acid and destroy

Discuss in
the
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structure of ATPase, thus showing the inhibitory effects of Cd on ATPase [122]. Cd can not only affect the energy metabolism (https://s
process in fish, but also cause damage to mitochondria, the main energy metabolism site. Regarding the effects of Cd on groups/p
the
utm_sou
mitochondria in Silurus meridionalis, it was shown that in Silurus meridionalis exposed to 500 μg/L Cd, the mitochondrial structure
and function of the liver was significantly damaged and the activity of mitochondria enzymes was decreased, which results in a

decrease in the energy of the liver metabolism [95]. Additional evidence verified that Cd could significantly reduce the level ofEndorse
ATP
in the hemolymph of Ostreidae and induce energy metabolism disorder [123]. In addition, Cd exposure significantly affects the
respiratory control rate and oxidative phosphorylation efficiency of mitochondria in Ostreidae and Oncorhynchus mykiss and
interferes with the expression of key mitochondrial genes [53,124]. For example, Cd can induce the production of differentially

Comment
expressed metabolites, such as succinate and glycogen, and proteins, including isocitrate dehydrogenase, pyruvate carboxylase,
and glyceraldehyde-3-phosphate, that are related to energy metabolism in the gill tissues of Tegillarca granosa (Figure 1) [125].
3.5. Cadmium Toxicity Affects Nervous System Development in Fish Back to TopTop
 
The neurotoxicity caused by Cd stress seriously threatens the normal life activities of fish because Cd directly inhibits the
(/)
biological activities of enzymes that contain sulfhydryl by binding with sulfhydryl groups. At the same time, Cd leads to a decrease

in the content of a series of metabolic intermediates, which causes serious damage to the nervous system of fish [126,127,128].
Cd can enter the brain tissue of fish and affect cerebellar functions, causing the fish to lose balance during swimming, while the
effects on the brain are mainly neuronal damage. Cd exposure inhibited the formation of neural crest cells during the early
development of fish, resulting in motor neuron damage and behavioral abnormalities [27,29,129]. Research has shown that Cd
induces damage to nerve cells in the lateral line system of Dicentrarchus labrax and affects its escape and swimming behavior

[130]. Cd also significantly inhibited acetylcholinesterase (AChE) activity in the brain tissue of zebrafish and Lepisosteus oculatus
Share
and induced neurological disorders [131,132]. Similarly, the behavior of juvenile zebrafish was severely inhibited under Cd

exposure conditions [133]. In addition, Cd accumulates in the olfactory epithelium and bulb of fish, which reduces the expression of
Help

the genes related to olfactory sensory neurons, thereby damaging the olfactory sense of fish and damaging their anti-predator
behavior (Figure 1) [134].
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
3.6. Cadmium Toxicity Leads to Changes in Blood Plasma Parameters
A study on Nile tilapia showed that albumin concentrations and serum total protein were decreased significantly (p < 0.001),
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while serum creatinine, glutamic-pyruvic transaminase (GPT), and aspartate aminotransferase (AST) significantly (p < SciProfiles
0.001)
(https://s
increased with increasing cadmium level in fish diets, and the urea-N concentration was insignificantly affected [135]. The results
of the study on carp showed that cadmium poisoning would cause renal tubule reabsorption dysfunction and a large amount groups/p
of
calcium and phosphorus excretion, along with urine, and result in a decrease in serum calcium and phosphorus. In addition, utm_sou

cadmium can damage renal tubules, inhibit the activation of vitamin D, and also show a series of negative effects on calcium and
phosphorus metabolism [92,136,137]. Usually, aminotransferases are most abundant in the liver and kidney, as well as in theEndorse
heart
muscle and bones, with very little in the serum, however, when these tissues, especially the liver and kidneys, are damaged or

diseased, the enzyme enters the bloodstream and increases the activity of transaminase in the serum. Therefore, the increase and
decrease of glutamic oxalacetic transaminase (GOT) and GPT activities in the serum may reflect the poisoning or pathological
Comment
changes [138,139]. A study on the effects of cadmium exposure to Sparus aurata suggested that GOT activity decreased in liver
cytoplasm, but increased in serum (Figure 1) [140].
Back to TopTop
 
4. Mechanism of the Toxic Effects of Cadmium Exposure on Fish
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4.1. Cadmium Toxicity Leads to Oxidative Damage in Fish
When fish are stressed due to Cd in the water environment, a large number of reactive oxygen species (ROS) and reactive
nitrogen species (RNS) radicals, which are beyond their own scavenging capacity, will accumulate in the fishs’ bodies, thereby

resulting in a series of oxidative damage reactions [42,108]. The toxic effect of Cd on fish is mainly reflected in the oxidative stress
caused by ROS, and the excessive accumulation of ROS will lead to structural changes in biological macromolecules, such as
proteins and DNA, disorder of DNA replication and repair, and eventually pathological changes [141]. At the same time, ROS can
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

cause unsaturated fatty acids on the cell membrane lipid peroxidation reaction to produce malondialdehyde (MDA) and cause cell
membrane structural damage, in addition, MDA itself is a kind of toxic substance [94,142]. Combined, all of these factors will
further affect the function of enzymes related to regulating cell proliferation and differentiation and apoptosis on the membrane, Help
finally causing a series of functional disorders and damage to the body [94,143,144]. The increase in intracellular ROS caused by
Cd mainly occurs through the following pathways: (I) Cd affects cellular respiration by inhibiting the respiratory transmission chain
Cite

in the mitochondria, resulting in an increase in byproduct ROS content [145]; (II) Cd can increase ROS content by increasing the
activity of nitric oxide synthase and the expression level of the related genes in the body [146]; (III) Cd can also remove Ca, Cu,
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Fe, and other elements from the binding proteins in the cell, thereby causing an increase in calcium, copper, iron, andSciProfiles other

elements in the cytoplasm, resulting in oxidative stress and an increase in intracellular ROS content [147,148]; (IV) Cd reduces (https://s
the
antioxidant capacity of cells by reducing the activity of intracellular antioxidant enzymes (Figure 2) [143,149]. groups/p
utm_sou
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

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Figure 2. Schematic diagram of ROS metabolism and oxidative stress induced by Cd. Under normal physiological
conditions, the ROS in the body are mainly converted into less toxic or harmless substances by antioxidant enzymes, such
Cite
as superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx), while under the condition of Cd
exposure, a large amount of ROS are generated and destroy the antioxidant system in cells.
4.2. Cadmium Toxicity Affected the Expression of Stress Genes in Fish

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(https://s
Usually, when fish are subjected to various stresses in a water environment, a series of stress-related genes in the body are
groups/p
significantly inhibited or induced to be expressed, so that the toxic effect of stress can be alleviated through the body’sutm_sou self-

regulation [150]. As a stress defense mechanism, multiple types of genes are induced to be expressed under Cd stress, such as
the oxidative stress-related genes GR, CYP1A, MT, and HSPs, antioxidant enzyme genes, such as CAT, SOD, and GSH-Px, and
Endorse

apoptosis-related genes, such as Bax, Bcl-2, Caspase-3, Caspase-8, and Caspase-9 [143,151]. The expression levels of
antioxidant enzyme genes in the liver, spleen, and muscle of Takifugu obscurus exposed to Cd in a water environment were
detected, and the results showed that the expression levels of MN-SOD, Cu/Zn-SOD, and CAT genes in the liver and spleenComment were
significantly increased. These levels in muscle tissue were inhibited at the early stage and significantly increased at the middle and
late stages of Cd stress, indicating that the muscle produced a large amount of antioxidant enzymes to protect the fish body in the
middle and late stages of Cd stress through body self-regulation [152]. Therefore, the fish body can regulate the generation of a
large number of antioxidant enzymes to reduce the oxidative damage caused by ROS. Moreover, Cd also induces the abnormal
Back to TopTop
 
expression of stress response protein genes, such as heat shock protein and metallic globulin, as determined in studies on the
(/)
liver in Cyprinus carpio and Labeo rohita, in which the expression levels of CYP1A, HSP47, HSP60, HSP70, HSP90, and MT-B
genes were significantly increased and then inhibited with prolonged Cd exposure time [153,154]. Furthermore, the expression
levels of anti-stress genes in different tissues of Cyprinus carpio were significantly different after Cd exposure for 96 h. For 
example, the expression level of HSP60 in the liver was significantly induced, but the expression levels of HSP70 and HSP90 were
not significantly changed and inhibited. The expression level of HSP70 in the gills first significantly increased and then decreased,
and the HSP90 expression level was significantly inhibited at all times (Figure 3) [153,155,156].
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utm_sou
Figure 3. Schematic diagram of Cd toxicity on molecule and cell in fish.


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4.3. Cadmium Toxicity Inhibits Multiple Enzyme Activities

Cd can reduce the activities of many enzymes in fish, especially antioxidant enzymes that contain zinc and sulfhydryl, and Cd

Comment
can bind to glutathione and metallothionein, which are two important thiol proteins that play an antioxidant role, thus, the ability of
ROS elimination in the body is reduced and oxidative damage eventually occurs [157,158]. Cd binds to the sulfhydryl groups of
superoxide dismutase (SOD) and glutathione reductase (GR), forms a Se-Cd complex with selenium (Se) in glutathione
Back to TopTop
 
peroxidase (GPx), or replaces Zn in SOD to form Cd-SOD, thus, the activity of these enzymes is reduced or lost [159,160]. Studies
(/)
have shown that the activities of SOD, catalase (CAT), and glutathione peroxidase (GPx) display an increasing trend in fish
exposed to Cd at low concentrations, but usually show a decreasing trend at high concentrations, and the dose‒response curve of
Cd generally shows a parabolic form, which has been verified in the liver and gills of Charybdis japonica [161]. Furthermore, 
excessive ROS will further lead to lipid peroxidation, mediate DNA damage, and promote the activation of poly-ADP-
ribotransferase, thus reducing intracellular ATP levels. In addition, Cd inhibits the repair of DNA damage and the activity of DNA
polymerase β, thereby affecting the immune function of the fish (Figure 3) [162,163].
Share
5. Conclusions and Future Perspectives
This review summarizes the biological accumulation and toxicological effects of Cd in fish, including the research progress
 Helpon
the toxic effects of Cd on tissue structure and functional integrity, physiological metabolism, reproduction, immune system, and
blood plasma parameters. We focus on the toxicological effects and mechanism of Cd in fish and anticipate future research  Cite

directions to discover and reduce Cd pollution in the aquatic environment in a timely manner, achieve the purpose of protecting the
aquatic ecological environment and aquatic life, and provide scientific evidence for humans to develop safe aquatic products.
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At present, research on Cd toxicity is very active. Although many achievements have been made, from the molecular and
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metabolic perspectives, we believe that further research needs to be performed, as follows: (I) analyze the effects of low-dose(https://s
and
long-period Cd stress on fish and establish a database of toxicological effects of fish over time to provide a scientific basis groups/p
for
formulating water environmental sanitation standards; (II) strengthen the study on the combined toxicological effects of Cdutm_sou and

other environmental pollutants in the water environment, improve the database of toxicological indicators of the water environment
and fish collected in the field, and comprehensively evaluate the ecotoxicological effects of Cd in the water environment; (III) Eand
ndorse
it

is of great significance to strengthen the research on the toxicological effects and mechanisms of different forms of Cd on fish, to
evaluate the ecological risk of Cd completely, to set environmental quality standards for Cd, and to repair and control Cd pollution
Comment
in the water environment. Anyway, the mechanisms of the toxic effects of cadmium, combined with other heavy metals, on fish
needs to be further studied. In recent years, the environmental hazards of microplastics are gaining researchers’ attention, and
microplastics enhance the movement of cadmium through the food chain, which should be taken seriously.
Back to TopTop
 
Author Contributions
(/)
Investigation, data curation, writing—original draft, Y.L. (Yinai Liu) and Q.C.; writing—review and editing, Y.L. (Yinai Liu), Q.C.,
L.J. and R.P.; software, supervision, validation, Y.L. (Yaoqi Li) and L.B.; conceptualization, L.J. and R.P. All authors have read and
agreed to the published version of the manuscript.


Funding
This research was funded by the Natural Science Foundation of Zhejiang Province (grant No. LQ20C020003). Share
Institutional Review Board Statement Help
Not applicable.
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Informed Consent Statement
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Data Availability Statement groups/p
Not applicable. utm_sou
Conflicts of Interest 
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The authors declare that there are no conflicts of interest.

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Abbreviations
Cd cadmium
MT metallothionein Back to TopTop

 
AAS atomic absorption spectroscopy
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ICP inductively coupled plasma
GFAAS
FAAS
graphite furnace atomic absorption spectrometry
flame atomic absorption spectrometry


ICP‒MS inductively coupled plasma‒mass spectrometry

ICP‒OES inductively coupled plasma optical emission spectrometry
HPG hypothalamic–pituitary–gonadal axis

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
GSI gonad somatic index
AChE acetylcholinesterase
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CaM calmodulin
ROS reactive oxygen species
RNS reactive nitrogen species Cite
MDA
GR
malondialdehyde
glutathione reductase 
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SciProfiles
SOD superoxide dismutase
(https://s
CAT catalase
groups/p
GPx glutathione peroxidase utm_sou
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Keywords: aquatic ecosystems (/search?q=aquatic+ecosystems); food chain (/search?q=food+chain); cadmium

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Table 3. Table of lethal effects of cadmium on different fish species.

2.2. Test Method for Cadmium Accumulation in Fish Cite

3. Toxic Effects of Cadmium Accumulation on Fish Cite

Figure 1. Schematic diagram of toxic effects of Cd on fish organs.

3.4. Cadmium Toxicity Damages the Energy Metabolism System of Fish

4.2. Cadmium Toxicity Affected the Expression of Stress Genes in Fish

Figure 3. Schematic diagram of Cd toxicity on molecule and cell in fish.

4.3. Cadmium Toxicity Inhibits Multiple Enzyme Activities

5. Conclusions and Future Perspectives

Institutional Review Board Statement Help

The authors declare that there are no conflicts of interest.

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HPG hypothalamic–pituitary–gonadal axis

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