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<journal-meta>
<journal-id journal-id-type="publisher-id">Front. Pharmacol.</journal-id>
<journal-title>Frontiers in Pharmacology</journal-title>
<abbrev-journal-title abbrev-type="pubmed">Front. Pharmacol.</abbrev-journal-title>
<issn pub-type="epub">1663-9812</issn>
<publisher>
<publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="publisher-id">1375137</article-id>
<article-id pub-id-type="doi">10.3389/fphar.2024.1375137</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Pharmacology</subject>
<subj-group>
<subject>Review</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group>
<article-title>Emerging insights into the impacts of heavy metals exposure on health, reproductive and productive performance of livestock</article-title>
<alt-title alt-title-type="left-running-head">Afzal and Mahreen</alt-title>
<alt-title alt-title-type="right-running-head">
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3389/fphar.2024.1375137">10.3389/fphar.2024.1375137</ext-link>
</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Afzal</surname>
<given-names>Ali</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff2">
<sup>2</sup>
</xref>
<xref ref-type="corresp" rid="c001">&#x2a;</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1332657/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/Writing - review &#x26; editing/"/>
<role content-type="https://credit.niso.org/contributor-roles/writing-original-draft/"/>
<role content-type="https://credit.niso.org/contributor-roles/software/"/>
<role content-type="https://credit.niso.org/contributor-roles/methodology/"/>
<role content-type="https://credit.niso.org/contributor-roles/investigation/"/>
<role content-type="https://credit.niso.org/contributor-roles/formal-analysis/"/>
<role content-type="https://credit.niso.org/contributor-roles/data-curation/"/>
<role content-type="https://credit.niso.org/contributor-roles/conceptualization/"/>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Mahreen</surname>
<given-names>Naima</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>3</sup>
</xref>
<uri xlink:href="https://loop.frontiersin.org/people/1597701/overview"/>
<role content-type="https://credit.niso.org/contributor-roles/Writing - review &#x26; editing/"/>
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<aff id="aff1">
<sup>1</sup>
<institution>Animal Sciences Division</institution>, <institution>Nuclear Institute for Agriculture and Biology College (NIAB-C)</institution>, <institution>Pakistan Institute of Engineering and Applied Sciences (PIEAS)</institution>, <addr-line>Faisalabad</addr-line>, <country>Pakistan</country>
</aff>
<aff id="aff2">
<sup>2</sup>
<institution>School of Zoology</institution>, <institution>Minhaj University Lahore</institution>, <addr-line>Lahore</addr-line>, <country>Pakistan</country>
</aff>
<aff id="aff3">
<sup>3</sup>
<institution>National Institute for Biotechnology and Genetics Engineering College (NIBGE-C)</institution>, <institution>Pakistan Institute of Engineering and Applied Sciences (PIEAS)</institution>, <addr-line>Faisalabad</addr-line>, <country>Pakistan</country>
</aff>
<author-notes>
<fn fn-type="edited-by">
<p>
<bold>Edited by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/1764772/overview">Vikas Kumar</ext-link>, University of Rovira i Virgili, Spain</p>
</fn>
<fn fn-type="edited-by">
<p>
<bold>Reviewed by:</bold> <ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/1882390/overview">Alicja Kowalczyk</ext-link>, Wroclaw University of Environmental and Life Sciences, Poland</p>
<p>
<ext-link ext-link-type="uri" xlink:href="https://loop.frontiersin.org/people/2614644/overview">Deepika Deepika</ext-link>, Pere Virgili Health Research Institute (IISPV), Spain</p>
</fn>
<corresp id="c001">&#x2a;Correspondence: Ali Afzal, <email>aliuaf1633@gmail.com</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>19</day>
<month>03</month>
<year>2024</year>
</pub-date>
<pub-date pub-type="collection">
<year>2024</year>
</pub-date>
<volume>15</volume>
<elocation-id>1375137</elocation-id>
<history>
<date date-type="received">
<day>23</day>
<month>01</month>
<year>2024</year>
</date>
<date date-type="accepted">
<day>04</day>
<month>03</month>
<year>2024</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright &#xa9; 2024 Afzal and Mahreen.</copyright-statement>
<copyright-year>2024</copyright-year>
<copyright-holder>Afzal and Mahreen</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/">
<p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p>
</license>
</permissions>
<abstract>
<p>Heavy metals, common environmental pollutants with widespread distribution hazards and several health problems linked to them are distinguished from other toxic compounds by their bioaccumulation in living organisms. They pollute the food chain and threaten the health of animals. Biologically, heavy metals exhibit both beneficial and harmful effects. Certain essential heavy metals such as Co, Mn, Se, Zn, and Mg play crucial roles in vital physiological processes in trace amounts, while others like As, Pb, Hg, Cd, and Cu are widely recognized for their toxic properties. Regardless of their physiological functions, an excess intake of all heavy metals beyond the tolerance limit can lead to toxicity. Animals face exposure to heavy metals through contaminated feed and water, primarily as a result of anthropogenic environmental pollution. After ingestion heavy metals persist in the body for an extended duration and the nature of exposure dictates whether they induce acute or chronic, clinical or subclinical, or subtle toxicities. The toxic effects of metals lead to disruption of cellular homeostasis through the generation of free radicals that develop oxidative stress. In cases of acute heavy metal poisoning, characteristic clinical symptoms may arise, potentially culminating in the death of animals with corresponding necropsy findings. Chronic toxicities manifest as a decline in overall body condition scoring and a decrease in the production potential of animals. Elevated heavy metal levels in consumable animal products raise public health concerns. Timely diagnosis, targeted antidotes, and management strategies can significantly mitigate heavy metal impact on livestock health, productivity, and reproductive performance.</p>
</abstract>
<kwd-group>
<kwd>heavy metals</kwd>
<kwd>toxicity</kwd>
<kwd>health</kwd>
<kwd>production performance</kwd>
<kwd>livestock</kwd>
</kwd-group>
<custom-meta-wrap>
<custom-meta>
<meta-name>section-at-acceptance</meta-name>
<meta-value>Predictive Toxicology</meta-value>
</custom-meta>
</custom-meta-wrap>
</article-meta>
</front>
<body>
<sec id="s1">
<title>Introduction</title>
<p>Technological developments have raised serious concerns about environmental safety as uncontrolled industrialization without emission control has put livestock health at risk (<xref ref-type="bibr" rid="B142">Prata et al., 2021</xref>). The livestock sector, an indispensable part of the global economy, is facing challenges because the production potential of animals depends on their health status, influenced by infectious and non-infectious diseases (<xref ref-type="bibr" rid="B16">Bailey et al., 2021</xref>). Heavy metal poisoning is one of the major causes of non-infectious diseases that adversely affect animal health. The risk of vulnerability is increasing due to widespread industrial, agricultural, domestic, technological, and medical applications of heavy metals (<xref ref-type="bibr" rid="B184">Vardhan et al., 2019</xref>).</p>
<p>Heavy metals like Zn and Cu are incorporated in animal feed as they play pivotal roles in immune function, growth, and metabolism (<xref ref-type="bibr" rid="B73">Hill and Shannon, 2019</xref>). These metals also serve as cofactors for numerous enzymes involved in protein synthesis and energy metabolism, thus promoting efficient nutrient utilization and growth in animals (<xref ref-type="bibr" rid="B42">Duffy et al., 2023</xref>). Moreover, Fe and Mn are indispensable for the formation of hemoglobin and enzymes involved in oxygen transport and antioxidant defense mechanisms (<xref ref-type="bibr" rid="B132">Pajarillo et al., 2021</xref>; <xref ref-type="bibr" rid="B173">Swecker, 2023</xref>). Adequate levels of these metals in livestock diets ensure optimal oxygen supply to tissues, which is particularly crucial for high-producing animals like dairy cows.</p>
<p>The escalating human activities contribute to a drastic increase in heavy metal addition to the environment, posing a continuous threat to livestock through water and soil pollution (<xref ref-type="bibr" rid="B110">Maurya et al., 2019</xref>; <xref ref-type="bibr" rid="B62">Ghazzal et al., 2022</xref>). The persistent exposure to these contaminants results in adverse health effects in livestock (<xref ref-type="bibr" rid="B23">Boudebbouz et al., 2023</xref>; <xref ref-type="bibr" rid="B7">Akbar et al., 2024</xref>). Additionally, the transfer of heavy metals from animals to humans through the food chain raises concerns about food safety and public health (<xref ref-type="bibr" rid="B5">Aftab et al., 2023</xref>; <xref ref-type="bibr" rid="B126">Noor et al., 2024</xref>).</p>
<p>The issue of metal toxicity has become a growing concern from evolutionary, ecological, environmental, and nutritional aspects particularly in the less developed countries of Africa, South Asia, and parts of Latin America (<xref ref-type="bibr" rid="B133">Pandey et al., 2014</xref>; <xref ref-type="bibr" rid="B39">Diarra and Prasad, 2021</xref>; <xref ref-type="bibr" rid="B156">Samy et al., 2022</xref>). In these countries, arid and semi-arid regions face particular challenges with metal pollution due to factors such as limited water resources, which concentrate pollutants, and the potential for windblown dust to spread contaminants over large areas (<xref ref-type="bibr" rid="B32">Chowdhury et al., 2016</xref>; <xref ref-type="bibr" rid="B156">Samy et al., 2022</xref>). Some countries in transition or with rapidly growing industrial sectors also face the challenge of heavy metal pollution due to lack of environmental regulations and limited resources for pollution control (<xref ref-type="bibr" rid="B40">Ding, 2019</xref>; <xref ref-type="bibr" rid="B43">Dutta et al., 2022</xref>; <xref ref-type="bibr" rid="B138">Patwa et al., 2022</xref>). While highly developed countries like the United States, China, Russia, and certain European nations have experienced issues with heavy metal contamination in soil, water, and air due to historical industrial practices (<xref ref-type="bibr" rid="B97">Li et al., 2014</xref>; <xref ref-type="bibr" rid="B199">Zhou et al., 2020</xref>). Altitude itself is not a direct factor in heavy metal pollution. However, certain activities more common at higher altitudes, such as mining in mountainous regions, can lead to localized heavy metal contamination. Additionally, factors like precipitation patterns and soil characteristics influenced by altitude can affect the transport and fate of metals in the environment (<xref ref-type="bibr" rid="B64">Giri et al., 2020</xref>).</p>
<p>The pervasive and mutinous nature of metal contaminants poses a potential risk for different animal populations. The distinct symptoms of metal poisoning in livestock include central nervous system (CNS) disorders, liver and kidney problems, reproductive failure, endocrine abnormalities, depression, and vision disturbances (<xref ref-type="bibr" rid="B109">Mass&#xe1;nyi et al., 2020</xref>; <xref ref-type="bibr" rid="B149">Rehman et al., 2021</xref>). If not diagnosed and treated properly, heavy metal exposure leads to complex problems with high morbidity and mortality rates. The sudden exposure to metals cause acute toxicity, with the severity of health issues depending on individual susceptibility, exposure route and duration, and the type and form of the element (<xref ref-type="bibr" rid="B86">Khan et al., 2016</xref>; <xref ref-type="bibr" rid="B163">Sinha et al., 2022</xref>). The pathophysiology of metals involves oxidative stress characterized by the generation of Reactive Oxygen and Reactive Nitrogen Species (ROS and RNS), reduction in intracellular free-radical scavengers and antioxidant stores, and decrease in enzyme capacity for detoxification of ROS. This leads to oxidative stress causing immunosuppression and a reduction in body condition scoring of domestic animals (<xref ref-type="bibr" rid="B131">Paithankar et al., 2021</xref>; <xref ref-type="bibr" rid="B170">Sun et al., 2022</xref>). Livestock populations are negatively influenced by exposure to excessive levels of harmful metals (e.g., Pb, Cd) or inadequate amounts of essential trace elements (e.g., Se and Mo) (<xref ref-type="bibr" rid="B147">Rajendran, 2013</xref>).</p>
<p>Ionic forms of metals exhibit high reactivity, engaging with biological systems in diverse ways that result in significant toxicological implications (<xref ref-type="bibr" rid="B24">Brandelli, 2020</xref>; <xref ref-type="bibr" rid="B135">Patel et al., 2021</xref>). The primary livestock species affected by metal poisoning in this scenario is cattle, mainly nourished with indigenously cultivated feed (<xref ref-type="bibr" rid="B187">Wang et al., 2013</xref>; <xref ref-type="bibr" rid="B159">Sharifian et al., 2023</xref>). To evaluate the potential effects of pollutants on livestock and measure contaminant intake in humans through milk and meat, it is essential to understand the concentrations of harmful metals in feed (<xref ref-type="bibr" rid="B179">Tortajada and Zhang, 2021</xref>; <xref ref-type="bibr" rid="B182">Ullah et al., 2023</xref>).</p>
<p>Research on the impacts of heavy metals exposure on the health, reproductive, and productive performance of livestock has garnered significant attention in recent years. Several published reviews have explored the diverse effects of heavy metals such as Pb, Cd, Hg, and As on various aspects of livestock physiology and productivity (<xref ref-type="bibr" rid="B108">Martinez et al., 2020</xref>; <xref ref-type="bibr" rid="B170">Sun et al., 2022</xref>; <xref ref-type="bibr" rid="B42">Duffy et al., 2023</xref>; <xref ref-type="bibr" rid="B153">Sadeghian et al., 2024</xref>). These reviews have elucidated the mechanisms by which heavy metals enter the animal body, their accumulation in tissues, and the resultant adverse effects on health. Some studies have highlighted the detrimental effects of heavy metals on immune function, oxidative stress, and reproductive functions in different livestock species (<xref ref-type="bibr" rid="B202">Garcia et al., 2017</xref>; <xref ref-type="bibr" rid="B190">Wang et al., 2019</xref>; <xref ref-type="bibr" rid="B135">Patel et al., 2021</xref>; <xref ref-type="bibr" rid="B176">Tahir and Alkheraije, 2023</xref>). Heavy metal contamination in livestock environments poses not only health risks to animals but also potential hazards to human consumers through the food chain. As such, this topic holds immense importance for informed decision-making in agricultural and veterinary practices. The study will comprehensively provide emerging insights and recent research findings regarding the effects of heavy metals on livestock. By collating and analyzing the latest scientific literature, this review aims to provide an overview of the current understanding of heavy metal toxicity in livestock and its implications for animal health and productive performance. Additionally, the review will explore potential mitigation strategies and areas for future research, contributing to the ongoing discourse on sustainable livestock management in the face of environmental challenges.</p>
<sec id="s1-1">
<title>Heavy metals and their biological significance</title>
<p>Metals are classified broadly into highly toxic, less toxic, essential, and non-essential categories. Essential metals like Fe, Zn, Mn, and Co are required in trace amounts for regulating various physiological functions such as hormone synthesis, oxygen and electron transportation, fertility, antioxidant defense, and immunity in livestock animals (<xref ref-type="bibr" rid="B95">Li et al., 2021</xref>). However, their presence beyond a certain limit in the biological system potentiates toxicity.</p>
<p>Highly toxic metals like As, Cu, Hg, Cd, and Pb can exert adverse effects even in minute concentrations without providing any beneficial biological impacts in animals (<xref ref-type="bibr" rid="B97">Li et al., 2014</xref>). Toxic metals impair the primary cellular functions by imitating the role of essential metals and this leads to their bioaccumulation. The elemental nature of metals affects the process of their biotransformation and detoxification through metabolic pathways that result in the breakdown of toxic atomic species into a less toxic or non-toxic species. In addition, the non-biodegradable nature of these metals further exacerbates the condition of toxicity (<xref ref-type="bibr" rid="B58">Florea et al., 2005</xref>).</p>
</sec>
<sec id="s1-2">
<title>Sources of heavy metals contamination</title>
<p>Sources of heavy metals contamination vary widely for livestock animals (<xref ref-type="fig" rid="F1">Figure 1</xref>), with industrial effluents emerging as a significant contributor (<xref ref-type="bibr" rid="B49">Elheddad et al., 2021</xref>). Wastewater from industries introduces hazardous pollutants like Cr into the soil and water bodies (<xref ref-type="bibr" rid="B41">Dotaniya et al., 2014</xref>). This contamination poses threats to livestock as they may drink poisonous water or graze on polluted pastures. Similarly, automobile emissions contribute to metal contamination along roadsides. Livestock grazing near roads exposed them to metal pollutants that adversely affect their health (<xref ref-type="bibr" rid="B63">Ghorani-Azam et al., 2016</xref>).</p>
<fig id="F1" position="float">
<label>FIGURE 1</label>
<caption>
<p>Sources of heavy metals contamination and routes of their entrance into animal body.</p>
</caption>
<graphic xlink:href="fphar-15-1375137-g001.tif"/>
</fig>
<p>Moreover, the application of fertilizers including phosphate fertilizers and organic materials (sewage sludge and animal manure) introduces heavy metals into agricultural soils (<xref ref-type="bibr" rid="B150">Rizzardini and Goi, 2014</xref>). Livestock may consume crops grown in such contaminated soils, resulting in the bioaccumulation of heavy metals in their tissues. Additionally, mining activities release toxic metals (As, Hg, and Pb) into the environment (<xref ref-type="bibr" rid="B128">Okereafor et al., 2020</xref>). Animals in mining areas may face direct exposure to these pollutants through soil, water, and vegetation, impacting their health, productivity, and welfare.</p>
</sec>
<sec id="s1-3">
<title>Toxic metal contents in livestock feedstuffs</title>
<p>Livestock exposure to toxic metals is significantly influenced by husbandry practices. Sometime different dietary supplements and ingestion of contaminated soil also contribute to potential exposure to heavy metals. While evaluating the concentration of heavy metals in primary feed ingredients, it is crucial to consider husbandry practices as contributing factors to metal exposure. This consideration is essential to limit the toxic effects on animal health and the potential transfer of these contaminants to human feed. Providing a comprehensive review of toxic metal contents in animal feed proves challenging due to restricted information regarding sample description, analysis methods, and data expression. The limit of toxic heavy metals in both individual feed ingredients and commercially manufactured compound feeds is presented in <xref ref-type="table" rid="T1">Table 1</xref> based on European Union (EU) organization standards (<xref ref-type="bibr" rid="B3">Adamse et al., 2017</xref>). Limited literature outside the EU provides information on toxic metal residues in livestock feedstuffs. Such data is often derived from samples collected at a very local level.</p>
<table-wrap id="T1" position="float">
<label>TABLE 1</label>
<caption>
<p>Amount (mg/kg DM) of heavy metals in animal feed components.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th rowspan="2" align="center">Feed components</th>
<th colspan="4" align="center">Heavy metals</th>
</tr>
<tr>
<th align="center">Cadmium</th>
<th align="center">Lead</th>
<th align="center">Arsenic</th>
<th align="center">Mercury</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="left">Barley Grain</td>
<td align="center">0.11</td>
<td align="center">0.97</td>
<td align="center">0.01</td>
<td align="center">0.006</td>
</tr>
<tr>
<td align="left">Citrus Pulp Meal</td>
<td align="center">0.19</td>
<td align="center">0.76</td>
<td align="center">0.04</td>
<td align="center">0.002</td>
</tr>
<tr>
<td align="left">Fish Meal</td>
<td align="center">0.4</td>
<td align="center">0.52</td>
<td align="center">4.7</td>
<td align="center">0.1</td>
</tr>
<tr>
<td align="left">Maize Grain</td>
<td align="center">0.06</td>
<td align="center">0.56</td>
<td align="center">0.26</td>
<td align="center">0.026</td>
</tr>
<tr>
<td align="left">Rapeseed</td>
<td align="center">0.15</td>
<td align="center">0.6</td>
<td align="center">0.08</td>
<td align="center">0.031</td>
</tr>
<tr>
<td align="left">Soya Bean Meal</td>
<td align="center">0.07</td>
<td align="center">0.93</td>
<td align="center">0.022</td>
<td align="center">0.055</td>
</tr>
<tr>
<td align="left">Sugar Beet Pulp</td>
<td align="center">0.14</td>
<td align="center">1.47</td>
<td align="center">0.36</td>
<td align="center">0.028</td>
</tr>
<tr>
<td align="left">Sun Flower Meal</td>
<td align="center">0.41</td>
<td align="center">0.37</td>
<td align="center">0.001</td>
<td align="center">0.003</td>
</tr>
<tr>
<td align="left">Mineral Supplements</td>
<td align="center">0.58</td>
<td align="center">3.38</td>
<td align="center">6.8</td>
<td align="center">0.02</td>
</tr>
<tr>
<td align="left">Wheat</td>
<td align="center">0.19</td>
<td align="center">0.26</td>
<td align="center">0.043</td>
<td align="center">0.003</td>
</tr>
<tr>
<td align="left">Meat and Bone Meal</td>
<td align="center">0.063</td>
<td align="center">0.81</td>
<td align="center">0.005</td>
<td align="center">0.15</td>
</tr>
<tr>
<td align="left">Fish Oil</td>
<td align="center">0.021</td>
<td align="center">0.14</td>
<td align="center">7.6</td>
<td align="center">0.03</td>
</tr>
<tr>
<td align="left">Oil Seed Meals</td>
<td align="center">0.005</td>
<td align="center">0.06</td>
<td align="center">0.09</td>
<td align="center">0.007</td>
</tr>
<tr>
<td align="left">Cereal and By Products</td>
<td align="center">0.03</td>
<td align="center">0.048</td>
<td align="center">0.06</td>
<td align="center">0.011</td>
</tr>
<tr>
<td colspan="5" align="center">Amount (mg/kg DM) of Heavy Metals in Animal Forages</td>
</tr>
<tr style="background-color:#c6c7c9">
<td rowspan="2" align="center">Forages</td>
<td colspan="4" align="center">Heavy Metals</td>
</tr>
<tr style="background-color:#c6c7c9">
<td align="left">Cadmium</td>
<td align="center">Lead</td>
<td align="left">Arsenic</td>
<td align="left">Mercury</td>
</tr>
<tr>
<td align="left">Grass/Herbage</td>
<td align="center">0.62</td>
<td align="center">4.93</td>
<td align="center">0.12</td>
<td align="center">0.071</td>
</tr>
<tr>
<td align="left">Hey</td>
<td align="center">0.73</td>
<td align="center">3.89</td>
<td align="center">0.05</td>
<td align="center">0.18</td>
</tr>
<tr>
<td align="left">Grass Silage</td>
<td align="center">0.09</td>
<td align="center">2.02</td>
<td align="center">0.12</td>
<td align="center">0.023</td>
</tr>
<tr>
<td align="left">Maize Silage</td>
<td align="center">0.28</td>
<td align="center">2.19</td>
<td align="center">0.05</td>
<td align="center">0.007</td>
</tr>
<tr>
<td align="left">Different Straws</td>
<td align="center">0.15</td>
<td align="center">0.033</td>
<td align="center">0.05</td>
<td align="center">0.026</td>
</tr>
<tr>
<td align="left">Alfalfa</td>
<td align="center">0.057</td>
<td align="center">0.21</td>
<td align="center">0.38</td>
<td align="center">0.005</td>
</tr>
<tr>
<td colspan="5" align="center">Amount (mg/kg DM) of Heavy Metals in Complete Animal Feeds</td>
</tr>
<tr style="background-color:#c6c7c9">
<td rowspan="2" align="center">Animals</td>
<td colspan="4" align="center">Heavy Metals</td>
</tr>
<tr style="background-color:#c6c7c9">
<td align="center">Cadmium</td>
<td align="center">Lead</td>
<td align="center">Arsenic</td>
<td align="center">Mercury</td>
</tr>
<tr>
<td align="left">Ruminants</td>
<td align="center">0.11</td>
<td align="center">0.34</td>
<td align="center">0.27</td>
<td align="center">0.012</td>
</tr>
<tr>
<td align="left">Poultry</td>
<td align="center">0.16</td>
<td align="center">0.87</td>
<td align="center">1.83</td>
<td align="center">0.039</td>
</tr>
<tr>
<td align="left">Pigs</td>
<td align="center">0.09</td>
<td align="center">1.03</td>
<td align="center">0.62</td>
<td align="center">0.032</td>
</tr>
<tr>
<td align="left">Horses</td>
<td align="center">0.21</td>
<td align="center">0.13</td>
<td align="center">0.39</td>
<td align="center">0.022</td>
</tr>
<tr>
<td align="left">Mink</td>
<td align="center">0.003</td>
<td align="center">0.28</td>
<td align="center">0.061</td>
<td align="center">0.053</td>
</tr>
<tr>
<td align="left">Rabbits</td>
<td align="center">0.14</td>
<td align="center">0.29</td>
<td align="center">0.09</td>
<td align="center">0.031</td>
</tr>
<tr>
<td align="left">Rodents</td>
<td align="center">0.36</td>
<td align="center">0.002</td>
<td align="center">0.73</td>
<td align="center">0.05</td>
</tr>
<tr>
<td align="left">Dogs and cats</td>
<td align="center">0.13</td>
<td align="center">0.04</td>
<td align="center">0.002</td>
<td align="center">0.02</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec id="s1-4">
<title>Livestock husbandry practices related to toxic metal exposure</title>
<p>Livestock husbandry practices, particularly those involving feed supplements and their waste management; contribute to elevated levels of toxic metal exposure in animals, posing risks to their health and production (<xref ref-type="bibr" rid="B187">Wang et al., 2013</xref>). Feed supplementation is a primary pathway for toxic metal introduction in animal production systems. Heavy metals such as Cu and Zn are often added to animal feed to promote growth and boost immune function (<xref ref-type="bibr" rid="B71">Harvey et al., 2021</xref>). These metals are essential in trace amounts, over-supplementation or improper formulation of feed can lead to accumulation in animal tissues, potentially reaching levels harmful for the animals themselves and as well as consumers of their products.</p>
<p>Furthermore, the disposal of livestock waste presents another avenue for toxic metal contamination. Manure from animals fed supplemented diets can contain elevated levels of heavy metals, which may leach into soil and water systems if not managed properly. As a result, crops grown in these environments can uptake these metals, perpetuating the cycle of contamination (<xref ref-type="bibr" rid="B98">Liu et al., 2020a</xref>). In addition, the spreading of manure on agricultural fields as fertilizer can introduce heavy metals into the food chain, posing risks to human health through consumption of contaminated crops or water sources (<xref ref-type="bibr" rid="B144">Qin et al., 2021</xref>). The exposure of animals to toxic heavy metals during husbandry practices also depends on the type of production system (extensive or intensive) under which they are housed. Therefore, effective waste management strategies are crucial to mitigate the spread of toxic metals from livestock operations to the broader environment.</p>
</sec>
<sec id="s1-5">
<title>Extensive production system</title>
<p>Regions of the world where animals are kept under extensive production systems, such as parts of South America, Africa, and Asia, are particularly vulnerable to heavy metal contamination due to factors such as industrial activities, mining operations, and improper waste disposal practices (<xref ref-type="bibr" rid="B120">Modernel et al., 2019</xref>; <xref ref-type="bibr" rid="B130">Otte et al., 2019</xref>; <xref ref-type="bibr" rid="B111">McAllister et al., 2020</xref>). The impact of heavy metals on livestock health and performance in these regions is most pronounced during the dry or winter seasons when forage availability is limited, and animals are forced to graze on contaminated vegetation or drink from contaminated water sources. During these periods, livestock animals experience heightened levels of heavy metal exposure, exacerbating the negative effects on their efficiency in extensive production system (<xref ref-type="bibr" rid="B4">Adegoke and Abioye, 2016</xref>; <xref ref-type="bibr" rid="B80">Johnsen and Aaneby, 2019</xref>). Prolonged exposure to elevated levels of these metals has led to various health issues, including gastrointestinal disturbances, liver and kidney damage, and neurological disorders. The presence immune system of animals is also compromised, reducing their resistance to pathogens and making them susceptible to infectious diseases (<xref ref-type="bibr" rid="B186">Villalba et al., 2016</xref>; <xref ref-type="bibr" rid="B31">Chen et al., 2022</xref>).</p>
<p>The heavy metal poisoning also disrupts the productive performance of animals in extensive system due to poor nutrient absorption and utilization. This leads to reduced feed efficiency, slower growth rate and decreased milk and meat production (<xref ref-type="bibr" rid="B118">Miroshnikov et al., 2021</xref>). Moreover, metal toxicity also causes metabolic disorders that further compromise the profitability of extensive livestock operations. In severe cases, metal poisoning results in acute illness and death, posing significant welfare concerns for animals (<xref ref-type="bibr" rid="B128">Okereafor et al., 2020</xref>). Effective management strategies, including regular monitoring of soil and water quality, implementation of proper waste management practices, and targeted nutritional interventions, are essential to mitigate the risks associated with heavy metal contamination and ensure the sustainability of extensive livestock farming operations (<xref ref-type="bibr" rid="B144">Qin et al., 2021</xref>).</p>
</sec>
<sec id="s1-6">
<title>Intensive production system</title>
<p>Non-ruminant (pigs and poultry) animal species whose diet entirely consists of concentrates and ruminant animals (feedlots and milk production cattle) with a high rate (90%) of concentrates in their feed are managed under intensive production system (<xref ref-type="bibr" rid="B121">Moorby and Fraser, 2021</xref>). The feed for animals in this system is composed of various materials selected from national and international markets based on cost, availability, and nutritional suitability according to the physiological requirements of the animals.</p>
<p>The complete feed given to these animals is supplemented with specific feed additives and minerals that contain higher toxic metal contents compared to their basic feed. Due to low inclusion rate, the contribution of these supplements to total metal intake (TMI) is minimal, except for certain elements like Hg and As in marine-originated feedstuffs (<xref ref-type="bibr" rid="B51">Elliott et al., 2017</xref>).</p>
<p>In the intensive production system, toxic metal exposure is easily calculable by multiplying the toxic metal contents in the complete feed by the amount ingested. Furthermore, the diets in this system are highly standardized resulting in lower intra- and inter-farm variability of toxic metal exposure through the diet compared to the extensive system (<xref ref-type="bibr" rid="B187">Wang et al., 2013</xref>).</p>
</sec>
<sec id="s1-7">
<title>Health risks and toxic effects of heavy metals in animals</title>
<p>Health risks and toxic effects of heavy metals in animals depend on the type and form of the metal, the extent of exposure, sex, age, nutritional and physiological status of the exposed animal, and the route of poisoning. Due to their non-biodegradable nature heavy metals tend to accumulate in vital organs more rapidly than they are metabolized and excreted. This bioaccumulation of heavy metals poses a significant health risk adversely affecting the production performance of domestic animals. The potential health menaces caused by various heavy metals are described below.</p>
</sec>
<sec id="s1-8">
<title>Arsenic</title>
<p>Arsenic (As) known as the &#x201c;Poison of Kings and the King of Poisons,&#x201d; is an ancient toxin. Domestic animals face As exposure from contaminated pastures, dipping and spraying chemicals, pesticides, herbicides, growth promoters, and feed additives. Groundwater and metal-bearing ores are natural sources of As (<xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>). After absorption As accumulates in the liver then slowly dispenses to the tissues of other organs like kidneys, spleen, and lungs. Animals in As toxicity exhibit gastrointestinal, nervous, and cardiovascular symptoms. The acute poisoning cases show restlessness, abdominal pain, respiratory distress, and vomiting (<xref ref-type="bibr" rid="B67">Gupta et al., 2021</xref>).</p>
<p>A meta-analysis of 156 cases in 16 outbreaks revealed common clinical signs in cattle including ataxia, diarrhea, dehydration, respiratory stress, and death (<xref ref-type="bibr" rid="B54">Faires, 2004</xref>). Hematuria, azotemia, increased hematocrit and liver enzyme activities were observed as biochemical changes (<xref ref-type="bibr" rid="B18">Bertin et al., 2013</xref>). Survival in acute As toxicity is possible with aggressive fluid therapy and antidote administration. Chronic As toxicity manifests as capricious appetite, weight loss, mucosal lesions, mouth ulceration, and reduced milk yield in dairy cattle. Biochemical changes in subclinical cases include high blood as levels, low plasma proteins and erythrocyte count (<xref ref-type="bibr" rid="B148">Rana et al., 2010</xref>).</p>
<p>Quantification of As in stomach contents and tissues is a standard test for diagnosis. While for sample collection liver is regarded as the best organ for acute poisoning and kidneys for sub-acute or chronic cases (<xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>). Levels exceeding 3&#xa0;ppm in liver and kidneys indicate toxicity. As also appears in urine samples a few days after exposure (<xref ref-type="bibr" rid="B158">Sharaf et al., 2020</xref>). The diagnostic range for As in feces is 10&#x2013;20&#xa0;mg/g, while As quantification in hair and urine serves as a biomarker for monitoring chronic exposure in livestock (<xref ref-type="bibr" rid="B36">Das et al., 2021</xref>; <xref ref-type="bibr" rid="B178">Tiffarent et al., 2022</xref>).</p>
</sec>
<sec id="s1-9">
<title>Lead</title>
<p>Lead (Pb) recognized as the first toxic element that poses a higher frequency of poisoning in animals than any other metal (<xref ref-type="bibr" rid="B68">Gupta, 2019</xref>). This issue spans worldwide affecting all species of livestock, with cattle and calves being susceptible while caprine and swine show tolerance. Cattle due to their indiscriminate eating and licking habits ingest Pb-bearing objects from their environment including agricultural, industrial, and domestic wastes resulting in acute Pb poisoning (<xref ref-type="bibr" rid="B99">Liu et al., 2020b</xref>). Apart from natural exposure anthropogenic activities also introduce Pb into the food chain through contaminated feed and water, burning of fossil fuels, paint industries, and combustion of coal. (<xref ref-type="bibr" rid="B201">Zyambo et al., 2022</xref>). Pastures near highways may carry up to 390&#xa0;ppm&#xa0;Pb (<xref ref-type="bibr" rid="B12">Anil et al., 2021</xref>). Organic Pb compounds are more toxic than inorganic forms and animals with essential dietary mineral deficiencies are more prone to lead toxicity (<xref ref-type="bibr" rid="B141">Prabhakar et al., 2012</xref>; <xref ref-type="bibr" rid="B168">Su et al., 2022</xref>).</p>
<p>Pb has ability to cross blood-brain and placental barriers, so it adversely affects the brain and fetus of exposed animals. Clinical signs manifest due to chronic exposure when Pb levels surpass saturation limits in natural sinks like bones (<xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>). Pb affects various physiological functions leading to gastrointestinal damage, neurotoxicity, liver and kidney dysfunctions, oxidative stress, and disruptions in enzyme systems (<xref ref-type="bibr" rid="B55">Finnie et al., 2011</xref>; <xref ref-type="bibr" rid="B136">Patra et al., 2011</xref>; <xref ref-type="bibr" rid="B165">Slivinska et al., 2020</xref>). Clinical signs in Pb poisoning mainly result from toxic effects on the CNS, gastrointestinal tract (GIT), and haemopoietic system. Neurological signs include bellowing, blindness, dullness, head pressing, opisthotonus, convulsions, and coma. Gastrointestinal signs include distension, pain, cramping, and diarrhea. Sub-acute Pb toxicity presents anorexia, dullness, depression, weight loss, eye sight loss, staggering, in co-ordinations, and sometimes circling, followed by death (<xref ref-type="bibr" rid="B92">Krametter-Froetscher et al., 2007</xref>; <xref ref-type="bibr" rid="B122">Mukherjee et al., 2022</xref>). Pb also affects the reproductive system impacting animal productivity (<xref ref-type="bibr" rid="B128">Okereafor et al., 2020</xref>). Pb exposure alters essential trace mineral profiles, with cows exhibiting lowered blood Cu and Fe at blood Pb levels &#x3e;0.60&#xa0;&#x3bc;g/mL (<xref ref-type="bibr" rid="B137">Patra et al., 2006</xref>). Some studies show higher tolerance to Pb in sheep and goats than cattle as these animals excrete higher concentration of Pb in their excretions (<xref ref-type="bibr" rid="B107">Makridis et al., 2012</xref>). Goats being highly resistant may show signs of CNS involvement following long-term exposure (<xref ref-type="bibr" rid="B172">Swarup et al., 2005</xref>).</p>
<p>Diagnosis is based on significantly high Pb concentrations in blood, liver, and kidney samples (<xref ref-type="bibr" rid="B129">Oluokun et al., 2007</xref>). Management and prevention involve identifying sources and adopting preventive measures providing supportive care with chelation therapy and ensuring food safety. Calcium versenate is an effective antidote with combination therapy showing promising results. Recovery may occur rapidly in less severe cases but Pb concentrations in tissues remain high posing a potential source of residues in the food chain (<xref ref-type="bibr" rid="B161">Siddiqui and Rajurkar, 2008</xref>).</p>
</sec>
<sec id="s1-10">
<title>Mercury</title>
<p>Mercury (Hg) exists naturally in elemental, organic, and inorganic forms in the environment. Historically, it was used in traditional Chinese and Indian medicines. Different sources of Hg including vinyl chloride, chlor-alkali, electrical and electronic batteries, posing a potential threat to marine ecosystems through industrial effluents (<xref ref-type="bibr" rid="B17">Barregard et al., 2022</xref>). Domestic animals are less prone to Hg poisoning. However, accidental cases may occur especially in cattle (<xref ref-type="bibr" rid="B38">de Los Santos et al., 2023</xref>). Hg exposure stems from ingestion of organic or inorganic compounds, while toxicity observed at an average daily intake of 10&#xa0;mg per kg body weight. Sheep and horses also exhibit toxic effects under certain intake levels (<xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>). Hg absorption occurs through the GIT and then it affects other vital organs of the body (<xref ref-type="bibr" rid="B26">Bubber, 2019</xref>). Hg is slowly excreted through feces, milk, and urine, making the liver, kidneys, and milk from poisoned animals unsafe for human consumption (<xref ref-type="bibr" rid="B26">Bubber, 2019</xref>; <xref ref-type="bibr" rid="B38">de Los Santos et al., 2023</xref>).</p>
<p>Some organic Hg compounds are neurotoxic, affecting the nervous system even at lower concentrations (<xref ref-type="bibr" rid="B29">Ceccatelli et al., 2010</xref>). Inorganic Hg adversely affects the GIT mucosa causing vomiting, diarrhea, and colic, with acute poisoning signs in cattle including sudden behavioral changes, blindness, convulsions, and death (<xref ref-type="bibr" rid="B92">Krametter-Froetscher et al., 2007</xref>). Diagnostic importance lies in Hg concentration in blood, urine, brain, kidney, liver, and hair. Kidneys are ideal for detecting Hg poisoning in deceased animals, with a tissue concentration of &#x3e;5&#xa0;ppm regarded as clinically toxic. Blood Hg concentration provides more information about acute exposure, while urine samples determine inorganic Hg poisoning. Combining blood, urine, and hair samples provides accurate information about different forms of Hg exposure (<xref ref-type="bibr" rid="B69">Gupta, 2018</xref>). Effective treatment involves using 2,3-dimercapto-propanesulphonate (DMPS) and Meso-2,3-dimercaptosuccinic acid (DMSA) which mobilize Hg deposits for excretion in urine. Se supplementation in the diet proves useful in protecting against organic and inorganic Hg toxicity in poultry, as Se and Hg are mutual antagonists. Phytoremediation, utilizing plant species like <italic>Brassica juncea</italic> has emerged as a proven approach to reduce Hg contamination in soil (<xref ref-type="bibr" rid="B47">Ekino et al., 2007</xref>). However, multidisciplinary research is essential to manage Hg toxicity and understand various treatment mechanisms.</p>
</sec>
<sec id="s1-11">
<title>Cadmium</title>
<p>Cadmium (Cd) a ductile and soft element with toxic properties, poses severe damage to vital organ systems (<xref ref-type="bibr" rid="B146">Rahimzadeh et al., 2017</xref>). It enters the environment through natural (volcanic activities, mineral ores, forest fires) and anthropogenic (processing facilities, non-ferrous metal smelters) sources, often released in combination with metals like Pb and Zn (<xref ref-type="bibr" rid="B151">Robards and Worsfold, 1991</xref>; <xref ref-type="bibr" rid="B169">Suhani et al., 2021</xref>). It is usually found as an impurity along with Zn and Pb deposits and therefore can be extracted as a byproduct during the smelting process of these metals. Rock phosphate fertilizer and sewage sludge leakage contribute to soil contamination leading to Cd transfer to plants and the food chain (<xref ref-type="bibr" rid="B146">Rahimzadeh et al., 2017</xref>). Domestic animals are exposed to Cd mainly through ingestion of plants grown in contaminated soils or in the vicinity of industrial units emitting Cd in the environment. Cd is mainly accumulated in leaves that act as a potential source of exposure to grazing animals (<xref ref-type="bibr" rid="B105">Madejon et al., 2009</xref>). Studies in Croatia and China revealed Cd concentrations exceeding limits in kidneys and liver, indicating environmental contamination (<xref ref-type="bibr" rid="B27">Cai et al., 2009</xref>; <xref ref-type="bibr" rid="B21">Bilandzic et al., 2010</xref>). Water from deep wells in certain areas may also carry high Cd levels (<xref ref-type="bibr" rid="B140">Perez-Carrera et al., 2016</xref>).</p>
<p>Cd ingestion causes acute liver damage and nephrotoxicity, while chronic exposure leads to organ accumulation and various clinical signs including in-appetence, weight loss, hoof and hair abnormalities (<xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>). Severe vascular degeneration and necrotic changes occur in vital organs around industrial areas (<xref ref-type="bibr" rid="B66">Gumasta et al., 2018</xref>). Experimental administration in sheep resulted in nephropathy, anemia, bone demineralization, congenital defects, stillbirths, and abortion (<xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>).</p>
<p>Limited exposure to Cd leads to subclinical effects like immunotoxicity, oxidative stress, reduced reproductive performance, endocrine disruption, altered micronutrient profiles, and poor weight gain (<xref ref-type="bibr" rid="B171">Swarup and Dwivedi, 2002</xref>). Long-term exposure causes lipid peroxidation, inhibits antioxidant enzymes, indicating oxidative damage in liver, kidneys, and testes (<xref ref-type="bibr" rid="B188">Wang et al., 2020</xref>). Ca, Fe, and Zn deficiency increases susceptibility to Cd toxicity, while Se supplementation protects the liver and kidneys (<xref ref-type="bibr" rid="B10">Alonso et al., 2004</xref>; <xref ref-type="bibr" rid="B78">Jemai et al., 2020</xref>). Including Mo and Fe in the diet prevents Cd poisoning signs (<xref ref-type="bibr" rid="B166">Smith and White, 1997</xref>; <xref ref-type="bibr" rid="B10">Alonso et al., 2004</xref>; <xref ref-type="bibr" rid="B196">Young et al., 2019</xref>).</p>
</sec>
<sec id="s1-12">
<title>Copper</title>
<p>Copper (Cu) is an essential element crucial for various enzyme systems in the body, but excessive intake can lead to severe toxicity in farm animals particularly in ruminants lacking efficient regulatory mechanisms for Cu (<xref ref-type="bibr" rid="B180">Trouillard et al., 2021</xref>). Sheep are highly susceptible to Cu poisoning while cattle show relative resistance, though cases are increasing especially in dairy cattle (<xref ref-type="bibr" rid="B102">Lopez-Alonso et al., 2017</xref>).</p>
<p>Ruminants have poor homeostatic mechanisms for Cu, storing excess in the liver. When exposed to levels beyond physiological requirements they fail to regulate it leading to severe Cu toxicity (<xref ref-type="bibr" rid="B124">National Research Council, 2005</xref>; <xref ref-type="bibr" rid="B9">Almeida et al., 2022</xref>). Acute poisoning in sheep and young calves occurs with an intake of 20&#x2013;100&#xa0;mg/kg of body weight (BW), while adult cattle require 200&#x2013;800&#xa0;mg/kg BW. Chronic poisoning in sheep results from a daily intake of 3.5&#xa0;mg/kg BW from pastures with 15&#x2013;20&#xa0;ppm Cu on a dry matter basis (<xref ref-type="bibr" rid="B69">Gupta, 2018</xref>). Goats tolerate higher Cu dietary intake (640&#xa0;mg/kg BW) and toxic doses for non-ruminants are higher than this (<xref ref-type="bibr" rid="B124">National Research Council, 2005</xref>; <xref ref-type="bibr" rid="B33">Constable et al., 2017</xref>). Cu absorption varies in animals influenced by diet, husbandry practices, and breed types (<xref ref-type="bibr" rid="B101">Lopez-Alonso and Miranda, 2020</xref>).</p>
<p>Acute Cu poisoning in animals exhibits signs like gastric pain, diarrhea, anorexia, excessive salivation, dehydration, collapse, and incoordination, with some survivors developing icterus and dysentery (<xref ref-type="bibr" rid="B50">Elliott et al., 2020</xref>). Chronic poisoning manifests as hemolytic conditions, causing thirst, anorexia, depression and jaundice along with nervous signs (<xref ref-type="bibr" rid="B145">Quevedo et al., 2022</xref>). Cattle and buffaloes in chronic Cu poisoning show apathy, hemoglobinuria, reduced ruminal movements, dehydration, mild diarrhea, and icteric mucus membrane. Cu toxicity affects reproductive performance causing disorders related to pregnancy and influencing estrogen receptors (<xref ref-type="bibr" rid="B74">Hinde, 2021</xref>).</p>
<p>Diagnosis involves assessing Cu concentrations in tissues with liver biopsy being the most authenticated method. Serum Cu and cerulo-plasmin levels in live animals are commonly used parameters. Toxic levels in liver and kidneys are &#x3e;250&#xa0;ppm and 10&#xa0;ppm in cattle, and &#x3e;250&#xa0;ppm and &#x3e;18&#xa0;ppm in sheep (<xref ref-type="bibr" rid="B100">Lopez-Alonso et al., 2006</xref>; <xref ref-type="bibr" rid="B35">Dalefield, 2017</xref>). Treatment involves using Mo and chelating agents (<xref ref-type="bibr" rid="B13">Antonelli et al., 2016</xref>; <xref ref-type="bibr" rid="B113">Mecitoglu et al., 2017</xref>; <xref ref-type="bibr" rid="B108">Martins et al., 2020</xref>). Zn supplementation is effective in preventing excessive Cu accumulation in sheep (<xref ref-type="bibr" rid="B117">Minervino et al., 2009</xref>). The potential health risks of heavy metals along with their maximum dose limits are summarized in <xref ref-type="table" rid="T2">Table 2</xref>.</p>
<table-wrap id="T2" position="float">
<label>TABLE 2</label>
<caption>
<p>Heavy metals and their associated health risks in animals.</p>
</caption>
<table>
<thead valign="top">
<tr>
<th rowspan="2" align="center">Heavy metal</th>
<th rowspan="2" align="center">Form</th>
<th rowspan="2" align="center">Sources</th>
<th rowspan="2" align="center">Entry routes</th>
<th colspan="2" align="center">Maximum daily dose (&#x3bc;g/day) limits</th>
<th rowspan="2" align="center">Associated symptoms</th>
<th rowspan="2" align="center">Pronounced health effects</th>
<th rowspan="2" align="center">References</th>
</tr>
<tr>
<th align="center">Parenteral</th>
<th align="center">Oral/Topical/Mucosal</th>
</tr>
</thead>
<tbody valign="top">
<tr>
<td align="center">Arsenic (As)</td>
<td align="center">Inorganic</td>
<td align="center">Pesticides, Contaminated water</td>
<td align="center">Ingestion, Inhalation</td>
<td align="center">1.5</td>
<td align="center">15</td>
<td align="center">Skin lesions, Gastrointestinal issues, Neurological disorders</td>
<td align="center">Skin cancer, Diabetes Cardiovascular disease</td>
<td align="center">
<xref ref-type="bibr" rid="B54">Faires, (2004)</xref>; <xref ref-type="bibr" rid="B148">Rana et al., (2010)</xref>; <xref ref-type="bibr" rid="B18">Bertin et al., (2013)</xref>; <xref ref-type="bibr" rid="B67">Gupta et al., (2021)</xref>
</td>
</tr>
<tr>
<td align="center">Lead (Pb)</td>
<td align="center">Inorganic</td>
<td align="center">Contaminated soil, Water, Air</td>
<td align="center">Ingestion, Inhalation</td>
<td align="center">1</td>
<td align="center">10</td>
<td align="center">Anemia, Neurological disorders, Developmental delays</td>
<td align="center">Impaired cognitive functions, Reproductive issues</td>
<td align="center">
<xref ref-type="bibr" rid="B92">Krametter-Froetscher et al., (2007)</xref>; <xref ref-type="bibr" rid="B55">Finnie et al., (2011)</xref>; <xref ref-type="bibr" rid="B136">Patra et al., (2011)</xref>; <xref ref-type="bibr" rid="B128">Okereafor et al., (2020)</xref>; <xref ref-type="bibr" rid="B165">Slivinska et al., (2020)</xref>; <xref ref-type="bibr" rid="B122">Mukherjee et al., (2022)</xref>
</td>
</tr>
<tr>
<td align="center">Mercury (Hg)</td>
<td align="center">Organic, Inorganic</td>
<td align="center">Coal combustion, Seafood</td>
<td align="center">Ingestion, Inhalation</td>
<td align="center">1.5</td>
<td align="center">15</td>
<td align="center">Neurological disorders, Tremors, Developmental delays</td>
<td align="center">Growth retardation, Impaired vision, Kidney damage</td>
<td align="center">
<xref ref-type="bibr" rid="B92">Krametter-Froetscher et al., (2007)</xref>; <xref ref-type="bibr" rid="B29">Ceccatelli et al., (2010)</xref>; <xref ref-type="bibr" rid="B26">Bubber, (2019)</xref>
</td>
</tr>
<tr>
<td align="center">Cadmium (Cd)</td>
<td align="center">Inorganic</td>
<td align="center">Industrial waste, Fertilizers</td>
<td align="center">Ingestion, Inhalation</td>
<td align="center">0.5</td>
<td align="center">5</td>
<td align="center">Renal dysfunction, Osteoporosis, Gastrointestinal problems</td>
<td align="center">Kidney damage, Bone demineralization, Cancer risk</td>
<td align="center">
<xref ref-type="bibr" rid="B171">Swarup and Dwivedi, (2002)</xref>; <xref ref-type="bibr" rid="B27">Cai et al., (2009)</xref>; <xref ref-type="bibr" rid="B21">Bilandzic et al., (2010)</xref>; <xref ref-type="bibr" rid="B66">Gumasta et al., (2018)</xref>; <xref ref-type="bibr" rid="B188">Wang et al., (2020)</xref>
</td>
</tr>
<tr>
<td align="center">Copper (Cu)</td>
<td align="center">Inorganic</td>
<td align="center">Waste water, Feed supplements, Copper-based fungicides</td>
<td align="center">Ingestion</td>
<td align="center">250</td>
<td align="center">2,500</td>
<td align="center">Liver damage, Gastrointestinal disturbances</td>
<td align="center">Hemolytic anemia, Cirrhosis, Neurological issues</td>
<td align="center">
<xref ref-type="bibr" rid="B50">Elliott et al., (2020)</xref>; <xref ref-type="bibr" rid="B74">Hinde, (2021)</xref>; <xref ref-type="bibr" rid="B145">Quevedo et al., (2022)</xref>
</td>
</tr>
</tbody>
</table>
</table-wrap>
</sec>
<sec id="s1-13">
<title>Effects of heavy metals on reproductive performance</title>
<sec id="s1-14">
<title>Male reproductive performance</title>
<p>Heavy metal toxicity has adverse effects on male reproductive performance impacting sperm maturation, concentration, and motility as shown in <xref ref-type="fig" rid="F2">Figure 2</xref> (<xref ref-type="bibr" rid="B76">Ilieva et al., 2020</xref>). In some livestock animal species sperm antioxidant defense system is poorly developed, so heavy metals disrupt normal motility and symmetry by accessing flagellum proteins through the sperm plasma-lemma (<xref ref-type="bibr" rid="B82">Kanous et al., 1993</xref>). Metal exposure in other species negatively affects the expression of metallo-thionein mRNA in testicular tissue crucial for protecting spermatogenesis from adverse effects of harmful substances (<xref ref-type="bibr" rid="B160">Sheng et al., 2015</xref>).</p>
<fig id="F2" position="float">
<label>FIGURE 2</label>
<caption>
<p>Adverse effects of heavy metals on sperm production.</p>
</caption>
<graphic xlink:href="fphar-15-1375137-g002.tif"/>
</fig>
<p>Mammalian testes are particularly susceptible to metal toxicities undergo remodeling of gene expression, alkalization of luminal fluid, and destabilization of sperm chromatin (<xref ref-type="bibr" rid="B103">Machado-Neves, 2022</xref>). Metals like Cd and Pb inhibit androgen production, microtubule movement, and the expression of regulatory protein genes resulting in a drastic decline in sperm count and histopathological changes in the testis (<xref ref-type="bibr" rid="B19">Bhardwaj et al., 2021</xref>; <xref ref-type="bibr" rid="B154">Salihu et al., 2021</xref>). Metal exposure also initiates testicular damage by altering angiogenesis processes (<xref ref-type="bibr" rid="B152">Rzymski et al., 2015</xref>). Cd exposure to Leydig cells increases cytokine production, inducing DNA breaks and reducing testosterone production leading to male infertility (<xref ref-type="bibr" rid="B195">Yang et al., 2022</xref>). Cd also stimulates &#x3b1;-adrenergic receptors producing excess glucocorticoids, inhibiting steroidogenesis and causing Sertoli cell damage (<xref ref-type="bibr" rid="B37">de Angelis et al., 2017</xref>; <xref ref-type="bibr" rid="B164">Slaby et al., 2019</xref>). A positive correlation between blood Cd levels and sperm abnormalities and an inverse relation with sperm density has been observed (<xref ref-type="bibr" rid="B115">Meligy et al., 2019</xref>).</p>
<p>Blood-Testicular Barrier (BTB) disruption due to heavy metal toxicity distorts tight junctions that negatively influences spermatogenesis and increases sperm abnormalities (<xref ref-type="bibr" rid="B122">Mukherjee et al., 2022</xref>). DNA hypermethylation due to metal toxicity leads to the overexpression of DNMT3b causing malignancy of prostate epithelial cells and permanent infertility (<xref ref-type="bibr" rid="B11">An&#x111;elkovi&#x107; et al., 2023</xref>). Further, metal toxicities may result in conditions like teratozoospermia, asthenozoospermia, reduced sperm surface mannose expression, loss of sperm head actin, acrosome reaction insufficiency, increased apoptosis, and altered transvascular fluid exchange with varicocele (<xref ref-type="bibr" rid="B11">An&#x111;elkovi&#x107; et al., 2023</xref>). Varicocele affects semen quantity and quality by influencing sperm count, morphology, and motility (<xref ref-type="bibr" rid="B76">Ilieva et al., 2020</xref>). Certain other biochemical and histological changes are also associated with heavy metals that adversely influence the reproductive performance of animals (<xref ref-type="bibr" rid="B83">Kar et al., 2015</xref>). Heavy metal in low concentration for a short period of time does not significantly affect reproductive performance of animals but moderate to high level in blood leads to poor semen quality and also reduces the reproductive hormones levels (<xref ref-type="bibr" rid="B19">Bhardwaj et al., 2021</xref>).</p>
</sec>
</sec>
<sec id="s1-15">
<title>Toxic effects on female reproductive performance</title>
<p>The exposure of female animals to heavy metals affects oocyte maturation rate, germinal vesicle breakdown, and sex organ weight causing impairment in the reproductive process (<xref ref-type="fig" rid="F3">Figure 3</xref>) (<xref ref-type="bibr" rid="B59">Fort et al., 2001</xref>; <xref ref-type="bibr" rid="B43">Dutta et al., 2022</xref>). During the embryonic development process, 17&#x3b2;-estradiol was found to synergistically modify the harmful effects of heavy metals on the female reproductive system (<xref ref-type="bibr" rid="B203">Chedrese et al., 2006</xref>). Metals like Cd disrupt the functions of the reproductive endocrine system, impairing oocyte release from graafian follicles, affecting ovulation, and ultimately impacting animal breeding (<xref ref-type="bibr" rid="B59">Fort et al., 2001</xref>; <xref ref-type="bibr" rid="B43">Dutta et al., 2022</xref>).</p>
<fig id="F3" position="float">
<label>FIGURE 3</label>
<caption>
<p>Reproductive failure in response to heavy metals exposure in cattle.</p>
</caption>
<graphic xlink:href="fphar-15-1375137-g003.tif"/>
</fig>
<p>DNA damage induced by heavy metals leads to excessive ROS production, causing oocyte death during meiosis-I and reducing the number of oocytes entering Metaphase-II stage (<xref ref-type="bibr" rid="B52">Engwa et al., 2019</xref>). Chronic metal exposure inhibits the functional activity of the p450 gene that influences the morphology and physiology of ovarian granulosa cells (<xref ref-type="bibr" rid="B203">Chedrese et al., 2006</xref>). Heavy metals interfere with FSH production, binding with its receptor and lower the rate of steroid synthesis in ovarian granulosa cells that affect steroidogenesis (<xref ref-type="bibr" rid="B90">Kirmizi et al., 2020</xref>).</p>
<p>Metal ions enter cells through L-type voltage-gated channels inhibiting Ca<sup>2&#x2b;</sup> ATPase pump activity and accelerating the expression of ERK, p38, and c-jun, crucial for granulosa cell proliferation and steroidogenesis (<xref ref-type="bibr" rid="B170">Sun et al., 2022</xref>). Some metals like Cd<sup>2&#x2b;</sup> replace Zn<sup>2&#x2b;</sup> in the regulatory domain of estrogen receptors (ERs) causing adverse changes in DNA binding domain elasticity and variations in steroidogenic gene expression at the transcriptional level (<xref ref-type="bibr" rid="B131">Paithankar et al., 2021</xref>). The development process of mammary glands is also adversely affected by the presence of metal ions inducing early arrival of puberty (<xref ref-type="bibr" rid="B116">Migdal&#x201a; et al., 2023</xref>).</p>
<p>Changes in estrogen and progesterone receptors due to heavy metal alterations act as causative agents for reproductive issues like spontaneous abortion, endometrial cancer, and estrogen-dependent diseases of mammary glands (<xref ref-type="bibr" rid="B20">Bhat et al., 2023</xref>). Metals like Cd can replace bivalent ions (Ca<sup>2&#x2b;</sup> and Zn<sup>2&#x2b;</sup>), and their deficiency during pregnancy increases the chances of spontaneous abortion. <italic>In vitro</italic> and <italic>in vivo</italic> studies show that Cd<sup>2&#x2b;</sup> exposure unfavorably influences oocyte maturation and causes chromosomal abnormalities (<xref ref-type="bibr" rid="B94">Leoni et al., 2002</xref>; <xref ref-type="bibr" rid="B79">Jia et al., 2011</xref>; <xref ref-type="bibr" rid="B6">Aglan et al., 2020</xref>).</p>
<p>The influx of metals in females increases during nutritionally critical stages (pregnancy and lactation), decreasing essential mineral elements (Zn<sup>2&#x2b;</sup>, Fe<sup>2&#x2b;</sup>, Cu<sup>2&#x2b;</sup>) and promoting metal-induced reproductive toxicity. Metal exposure during pregnancy increases the chances of preterm labor, premature delivery, and low birth weight (<xref ref-type="bibr" rid="B44">Eaves and Fry, 2023</xref>). Tobacco smoke a source of metallo-toxins decreases female reproductive performance and causes structural changes in the fallopian tube and uterus (<xref ref-type="bibr" rid="B157">Semczuk and Semczuk-sikora, 2001</xref>).</p>
<p>Heavy metals can accumulate in the placenta of some animal species, affecting progesterone synthesis, inhibiting the transcription of essential enzymes, and preventing the maintenance of pregnancy (<xref ref-type="bibr" rid="B177">Thompson and Bannigan, 2008</xref>; <xref ref-type="bibr" rid="B28">Caserta et al., 2013</xref>; <xref ref-type="bibr" rid="B61">Geng and Wang, 2019</xref>). <italic>In vitro</italic> administration of different heavy metals in endothelial cells promotes the synthesis of placentation growth factor (PLGF) and vascular endothelial growth factor-A (VEGF-A) by mediating certain changes in mRNA expression. The transcription of the growth factors (VEGF-A and PLGF) alters the process of angiogenesis that is required for placentation, implantation and embryogenesis (<xref ref-type="bibr" rid="B197">Y&#xfc;ksel et al., 2021</xref>). The defects in expression of VFGF-A and PLGF lead to lack of proper implantation of embryo, endothelial dysfunction, sub-infertility, pre-eclampsia and premature delivery (<xref ref-type="bibr" rid="B152">Rzymski et al., 2015</xref>; <xref ref-type="bibr" rid="B119">Mishra and Bhardwaj, 2018</xref>).</p>
</sec>
<sec id="s1-16">
<title>Toxic metals and animal products quality</title>
<p>Heavy metals present a significant concern in the quality of animal products reared under commercial conditions as they are more susceptible to contamination from environmental pollution and industrial wastes (<xref ref-type="bibr" rid="B72">Hejna et al., 2019</xref>). While organic farming of animals emphasizes natural methods of production, including pasture-based systems and restricted use of synthetic inputs such as pesticides and fertilizers, organic animals are less likely to be exposed to heavy metals from industrial sources such as contaminated soil, water, and feed additives. Among heavy metals contamination in commercial production of animals, As stands out as a particular concern as livestock animals can experience its toxic effects through the consumption of contaminated feedstuffs. As is primarily excreted in the milk of exposed animals, while its residues have also been detected in chicken, duck, cow, and goat meat (<xref ref-type="bibr" rid="B198">Zahrana and Hendy, 2015</xref>). As contamination deteriorates milk and meat quality that poses a serious risk to consumer health. Human exposure to As occurs through the consumption of contaminated foodstuff (milk and meat) as highlighted by a survey conducted by the European Food Safety Authority (EFSA) (<xref ref-type="bibr" rid="B15">Authority et al., 2021</xref>).</p>
<p>Despite the absence of a universally accepted safe limit for As in food, WHO has set an acceptable intake level of 3.0&#xa0;g/kg BW for this toxic metal (<xref ref-type="bibr" rid="B77">Islam et al., 2014</xref>). The detection of As in cow&#x2019;s milk and poultry liver suggests them as preferred deposition sites compared to other meat parts (<xref ref-type="bibr" rid="B36">Das et al., 2021</xref>). Notably, milk contains inorganic As due to the inability of methylated As to cross the udder epithelium of cows. The highest accumulation of As occurs in casein (83%), while fat, whey protein and skimmed milk contain minute amounts of 10%, 4%, and 3% respectively. This highlights the complexity of metal distribution within dairy products (<xref ref-type="bibr" rid="B36">Das et al., 2021</xref>).</p>
<p>Moreover, milk can also be affected to some extent by Cr and Ni (<xref ref-type="bibr" rid="B167">Somasundaram et al., 2005</xref>; <xref ref-type="bibr" rid="B181">Ubwa et al., 2017</xref>). Some other potential sources of contamination include milk utensils, feed, and the animals&#x2019; environment (<xref ref-type="bibr" rid="B204">Ismail et al., 2019</xref>). A study involving Jersey cows substantiated the bioaccumulation of toxic metals in milk with concentrations of Pb, Cd, Ni, and Cr reaching significant levels (<xref ref-type="bibr" rid="B167">Somasundaram et al., 2005</xref>). Interestingly, Pb concentrations exhibit an increasing pattern in the initial stages, followed by a stable level over time, contrasting with Cd levels that double after 10 days and remain constant thereafter (<xref ref-type="bibr" rid="B167">Somasundaram et al., 2005</xref>).</p>
<p>Feed additives and industrial emissions lead to varying heavy metal concentrations in the muscle tissue of pigs. A significantly high concentration of Pb (0.05&#x2013;0.58&#xa0;mg&#xa0;kg<sup>&#x2212;1</sup> d.m.) and Cd (0.02&#x2013;0.04&#xa0;mg&#xa0;kg<sup>&#x2212;1</sup>) has been reported in the muscles of fattening pigs (<xref ref-type="bibr" rid="B114">Medardus et al., 2014</xref>; <xref ref-type="bibr" rid="B30">Cha&#x142;abis-Mazurek et al., 2021</xref>). Sheep reared under pasture and extensive systems accumulate Cd in kidneys and udder, while Pb, Zn and Cu are predominant in ribs, liver, and long bones (<xref ref-type="bibr" rid="B1">Abd-Elghany et al., 2020</xref>).</p>
<p>Poultry, especially from backyard rearing systems accumulate heavy metals from sources like landfills and contaminated soil, resulting in exceeding permissible limits in meat and eggs. Duck and goose reared near industrial areas show higher concentrations of As, Cd, and Hg in their eggs as compared to non-industrial sites (<xref ref-type="bibr" rid="B91">Korish and Attia, 2020</xref>; <xref ref-type="bibr" rid="B81">Kabeer et al., 2021</xref>). Bees serve as bioindicators of toxic metal contamination and retain a significant portion of these metals from their surrounding environment during honey processing (<xref ref-type="bibr" rid="B22">Bosancic et al., 2020</xref>). Horse muscles generally lack excess heavy metals, but kidneys and liver often accumulate Cd and Zn (<xref ref-type="bibr" rid="B67">Gupta et al., 2021</xref>). Wildlife in industrially exploited regions exhibits levels of heavy metals surpassing legal limits for human consumption, with wild boar being the most affected species (<xref ref-type="bibr" rid="B185">Verma et al., 2023</xref>).</p>
</sec>
<sec id="s1-17">
<title>Cytotoxic and oxidative effects of heavy metals</title>
<p>Pb exerts its cytotoxic effects by interfering with enzymes involved in heme synthesis, such as &#x3b4;-aminolevulinic acid dehydratase (ALAD) leading to anemia (<xref ref-type="bibr" rid="B45">Ebrahimi et al., 2023</xref>). Further, Pb disrupts calcium signaling pathways by interfering with calcium-dependent processes that affects neurotransmitter release and synaptic plasticity (<xref ref-type="bibr" rid="B34">Cory-Slechta et al., 2016</xref>). Hg impairs mitochondrial function and energy metabolism, causing cellular dysfunction and apoptosis (<xref ref-type="bibr" rid="B85">Ke et al., 2023</xref>). Moreover, by disrupting neurotransmitter signaling, Hg interferes with the function of ion channels and neurotransmitter transporters, contributing to neurotoxicity (<xref ref-type="bibr" rid="B127">Novo et al., 2021</xref>). Cd binds to sulfhydryl groups in proteins. This binding inhibits their activity and disrupting cellular functions (<xref ref-type="bibr" rid="B60">Genchi et al., 2020</xref>; <xref ref-type="bibr" rid="B169">Suhani et al., 2021</xref>). As toxicity inactivates enzymes involved in cellular metabolism, including those in the tricarboxylic acid (TCA) cycle and oxidative phosphorylation (<xref ref-type="bibr" rid="B104">Machado-Neves and Spuza, 2023</xref>). As also disrupts cell cycle regulation, resulting in aberrant cell proliferation and apoptosis resistance (<xref ref-type="bibr" rid="B125">Naujokas et al., 2013</xref>).</p>
<p>Heavy metals induce the generation of highly reactive free radicals causing DNA damage, oxidation, protein depletion, lipid peroxidation, and various cytotoxic effects. The toxicity of different metals is primarily attributed to the production of ROS and RNS disrupting cellular redox potential. ROS with their high chemical reactivity produce free radicals like hydroxyl (OH), superoxide (O<sup>2-</sup>), alkoxyl (RO), and peroxyl (RO<sup>2</sup>) as well as non-radicals such as H<sub>2</sub>O<sub>2</sub> and peroxynitrite (ONOO<sup>&#x2212;</sup>) acting as oxidizing agents or converting into other radicals.</p>
<p>Intracellular, superoxide anion (O<sup>2-</sup>) generation involves redox components (e.g., semi-ubiquinone), enzymes (e.g., NADPH-oxidase (NOX), xanthine-oxidase), or auto-oxidation reactions (<xref ref-type="bibr" rid="B25">Brochin et al., 2008</xref>; <xref ref-type="bibr" rid="B56">Flora et al., 2012</xref>; <xref ref-type="bibr" rid="B8">Alkadi, 2020</xref>; <xref ref-type="bibr" rid="B174">Sylvester et al., 2022</xref>). Superoxide anion (O<sup>2-</sup>) exhibits limited reactivity under specific physiological conditions and cannot cross biological membranes. However, its reaction with nitric oxide (NO) leads to the production of peroxynitrite (ONOO<sup>&#x2212;</sup>) with highly reactive intermediates like the short-lived hydroxyl radical (OH) (<xref ref-type="bibr" rid="B134">Pastor et al., 2000</xref>).</p>
<p>Involvement of nitric oxide synthase isozymes, such as mitochondrial nitric oxide synthase (mtNOS) and endothelial nitric oxide synthase (eNOS) also result in the production of nitric oxide (NO) from L-arginine to citrulline. NO due to its amphipathic nature remains stable in anaerobic environments and can diffuse through plasma membranes and cytoplasm. Its interaction with superoxide anion results in the production of peroxynitrite (ONOO<sup>&#x2212;</sup>) (<xref ref-type="bibr" rid="B175">Szabo et al., 2007</xref>). An imbalance in ROS and RNS production or a decrease in scavenging activities as a consequence of external stimuli like metal exposure leads to alterations in cellular functions through direct changes in biomolecules and aberrant stimulation of specific signaling pathways that directly affect growth performance and production potential of animals.</p>
</sec>
<sec id="s1-18">
<title>Epigenetic modifications</title>
<p>Epigenetic modifications such as DNA methylation, DNA repair, histone modifications, transcription, RNA regulation, RNA stability, protein degradation, transposon activation, and gene copy number alterations are intricate processes influenced by pollutants containing heavy metals. These metals induce gene alterations, contributing to complex changes responsible for malignancies, allergic reactions, respiratory diseases, intrauterine growth inhibition, pre-eclampsia, and permanent infertility in affected animals (<xref ref-type="bibr" rid="B46">Edwards and Myers, 2007</xref>; <xref ref-type="bibr" rid="B65">Godfrey et al., 2016</xref>).</p>
<p>Current interest in epigenetics research and evidence of environmental variables influencing DNA methylation has expanded the study of health-related causes (<xref ref-type="bibr" rid="B155">Salnikow and Zhitkovich, 2008</xref>; <xref ref-type="bibr" rid="B14">Arita and Costa, 2009</xref>; <xref ref-type="bibr" rid="B93">Larson et al., 2010</xref>). Alteration in protein synthesis mechanisms due to heavy metal pollutants in the nucleus may lead to cellular toxicity, initiating the process of cell apoptosis (<xref ref-type="fig" rid="F4">Figure 4</xref>) (<xref ref-type="bibr" rid="B58">Florea et al., 2005</xref>). In response to As, epigenetic modifications involve glutathione-reactive oxidation, increased expression of proteins (e.g., alpha-B-crystallin, heat-shock anti-oxidative stress proteins ferritin light chain) and enzymes (e.g., heme oxygenase-1, reductase, aldose), while glyceraldehyde-3-phosphate dehydrogenase activity is downregulated and extracellular signal-regulated kinases ERK-1 and ERK-2 are inactivated. These activities cause genomic damage and disrupt the cell cycle. DNA methylation is observed in the case of Cr and Cd exposure (<xref ref-type="bibr" rid="B46">Edwards and Myers, 2007</xref>; <xref ref-type="bibr" rid="B14">Arita and Costa, 2009</xref>). Trivalent Cr is essential in trace quantities for normal reproductive functions. While, it is chronic exposure leads to significant epigenetic alterations in sperm influencing parental imprinting, ovarian cyst formation, uterine anomalies, and tumors in male offspring. Trivalent As and bivalent Cd exposure affects cell associations in urothelial cells, lowering SPARC expression and playing a role in bladder tumor development (<xref ref-type="bibr" rid="B93">Larson et al., 2010</xref>). Prolonged Pb exposure increases superoxide dismutase (SOD) enzyme activity in neoplasia, suggesting a potential mechanism for reactive oxygen species production and carcinogenesis (<xref ref-type="bibr" rid="B84">Kasperczyk et al., 2004</xref>). These examples provide evidence that heavy metal exposures cause epigenetic alterations, linking heritable changes in gene expression to increased likelihood of various physiological disorders, including reproductive issues.</p>
<fig id="F4" position="float">
<label>FIGURE 4</label>
<caption>
<p>Mechanism of heavy metals induced cytotoxic and oxidative stress. Heavy metals negatively impact the process of protein biosynthesis, resulting in cellular toxicity. This disruption may induce the release of cytochrome c (Cyt c) from mitochondria, ultimately causing cellular apoptosis. Additionally, heavy metals contribute to the heightened generation of reactive oxygen species (ROS), leading to the induction of oxidative stress (OS). The consequences of OS include oxidative damage to cellular macromolecules, ultimately culminating in cell death. Furthermore, OS mediates epigenetic changes in reproductive cells, such as DNA methylation and histone modifications, altering the expression of crucial cellular proteins. The adverse effects extend to the inactivation of heat shock antioxidant proteins, disrupting the mitogen-activated protein kinases (MAPKs) pathways. This disruption results in uncontrolled cellular proliferation and may even contribute to carcinogenesis. Moreover, heavy metals activate the phosphoinositide 3-kinase (PI3K) pathway and induce hypoxia-inducible factor 1 (HIF1), promoting cancer, angiogenesis, and various cellular processes. The activation of the nuclear factor kappa-light-chain enhancer of activated B cells (NF-&#x3ba;B) by heavy metals also contributes to carcinogenesis. These cytotoxic and oxidative effects have a detrimental impact on the reproductive and productive efficiency of animals.</p>
</caption>
<graphic xlink:href="fphar-15-1375137-g004.tif"/>
</fig>
</sec>
<sec id="s1-19">
<title>Monitoring of toxic metals contamination</title>
<p>Toxic metals stemming from escalating human activities necessitate increased monitoring due to their accumulation in the environment and animal tissues. This monitoring is crucial for estimating health hazards for both humans and animals as it involves identifying environmental contaminants and assessing affected areas (<xref ref-type="bibr" rid="B89">Khan et al., 2018</xref>). Estimating metal contents in animal tissues aids in diagnosing environmental pollution, accomplished through various biological techniques including the use of bio-indicators (<xref ref-type="bibr" rid="B88">Khan et al., 2019</xref>). Animal exposure to toxic metal poisoning is primarily influenced by contaminated feeds containing toxins like pesticides and metals (<xref ref-type="bibr" rid="B87">Khan et al., 2023</xref>). Monitoring animal feeds for toxic metal contamination is imperative especially in areas with polluted soils or industrial wastes (<xref ref-type="bibr" rid="B183">Usman et al., 2022</xref>).</p>
<p>The accumulation of toxic metals in the soil which enters the food chain through plants poses a direct threat to humans consuming animal products (<xref ref-type="bibr" rid="B123">N&#x103;st&#x103;sescu et al., 2020</xref>). Despite the accumulation of toxic metals in animal tissues, a lack of international standards for certain elements in food products poses risks to consumer health (<xref ref-type="bibr" rid="B53">European Commission, 2006</xref>). Toxic metal bio-monitoring using blood plasma, urine, or hair samples offer insights into metal concentration and excretion patterns. Hg excretion occurs in urine and feces, while Pb is found in hair, blood, and urine samples (<xref ref-type="bibr" rid="B75">Hsieh et al., 2019</xref>). As can be detected in blood, feces, and keratin tissues hours after exposure. Diagnosis of toxic metal poisoning in cattle also involves testing milk, an indirect indicator of environmental pollution (<xref ref-type="bibr" rid="B143">P&#x161;enkov&#xe1; et al., 2020</xref>).</p>
<p>Toxic metals predominantly accumulate in internal organs making it feasible to establish standard levels in the body (<xref ref-type="bibr" rid="B85">Ke et al., 2023</xref>). Diagnosis and control of contamination in animal feed ensure the safety of human food and health. High concentrations of Cd and Hg in animal feed (&#x3e;10&#xa0;ppm) are considered toxic, while Co, Cu, Pb, Mo, or Ba are regarded as toxic at concentrations above 40&#xa0;ppm (<xref ref-type="bibr" rid="B112">Mc Geehan et al., 2020</xref>). Mandatory bio-monitoring programs should be established, requiring regular testing of blood, body fluids and tissue samples from livestock is essential, as relying solely on feed testing is insufficient for detecting metal contamination (<xref ref-type="bibr" rid="B112">McGeehan et al., 2020</xref>). These programs, overseen by veterinary authorities or certified laboratories, should set safe thresholds for heavy metal concentrations. Additionally, state authorities must monitor and regulate industrial activities that contribute to metal contamination, implement education programs for livestock owners, and enforce penalties for non-compliance. Investing in research and fostering inter-agency collaboration will further strengthen efforts to prevent heavy metals toxicities in livestock environments.</p>
<p>Further, Collaborative efforts between veterinary, environmental, agricultural, and public health agencies are essential to address heavy metal contamination comprehensively. Public awareness campaigns should also be launched to educate farmers and the public about the risks of heavy metal contamination in livestock, while investments in testing facilities and laboratories will bolster monitoring efforts (<xref ref-type="bibr" rid="B31">Chen et al., 2022</xref>). Additionally, policy development and implementation, alongside surveillance systems to monitor contamination trends, are crucial for prompt response to outbreaks or incidents of toxicity. Through these measures, state authorities can safeguard livestock health and ensure the safety of the food supply chain.</p>
</sec>
<sec id="s1-20">
<title>Prevention and control of bioaccumulation of toxic metals</title>
<p>Soil remediation is used to reinstate the effectiveness of soil that indirectly reduces the chances of toxic metal exposure and their harmful effects (<xref ref-type="bibr" rid="B192">Xu et al., 2021</xref>). The techniques used for remediation of soil are based on biological and/or chemical protocols (<xref ref-type="bibr" rid="B106">Mahey et al., 2020</xref>). Bioremediation is used to clear water and soil from toxic metals that are harmful for living beings. This process utilizes a variety of plants and different microorganisms for biological restoration of contaminated areas. Soil can be reclaimed from Cu contents by using <italic>Pseudomonas aeruginosa</italic> and <italic>Bacillus</italic> spp. whereas phytoremediation is helpful in the clearance of Co from soil and water. The toxic metals are immobilized in plants, thus their further spread is prevented. The symbiotic bacteria of these plants possess the potential to adsorb these toxic metal pollutants. Chemical techniques for reduction of toxic metal pollutants reduce the bioavailability of metals (<xref ref-type="bibr" rid="B162">Singh and Prasad, 2015</xref>).</p>
<p>Environmental contamination with toxic metals extends to animal feed, leading to potential risks upon consumption (<xref ref-type="bibr" rid="B102">Lopez-Alonso et al., 2017</xref>). Contaminated animal feed introduces metals into animal bodies, eventually excreted in urine and feces (<xref ref-type="bibr" rid="B70">Hao et al., 2019</xref>). Animal dung rich in proteins and minerals may act as a fertilizer but can also be a source of toxic metal contaminants (<xref ref-type="bibr" rid="B96">Li et al., 2020</xref>). Composting reduces metal concentrations in manure by altering physicochemical properties and utilizing microorganisms to immobilize and oxidize metals (<xref ref-type="bibr" rid="B70">Hao et al., 2019</xref>; <xref ref-type="bibr" rid="B190">Wang et al., 2019</xref>). Landfills contribute to environmental pollution with toxic metals, generating leachate that contaminates soil and groundwater. Phytoremediation, using plants to extract and accumulate metals, aids in the recovery of landfill soils. Biochar produced during biomass pyrolysis reduces the bioavailability of toxic metals, improving soil quality. The deposition of sewage sludge in landfills poses a contamination risk but pyrolysis transforms sewage sludge into biochar, reducing metal spread and increasing soil pH (<xref ref-type="bibr" rid="B139">Penido et al., 2019</xref>; <xref ref-type="bibr" rid="B48">Elbehiry et al., 2020</xref>). The use of biochar in sewage sludge treatment minimizes pollution risks and enhances soil fertility (<xref ref-type="bibr" rid="B139">Penido et al., 2019</xref>; <xref ref-type="bibr" rid="B96">Li et al., 2020</xref>).</p>
</sec>
</sec>
<sec sec-type="conclusion" id="s2">
<title>Conclusion</title>
<p>Heavy metal toxicity has emerged as a major environmental challenge with detrimental impacts on livestock health and productivity. Heavy metals accumulate in the environment and then infiltrate animals from both natural and anthropogenic sources. Despite the essential role of some metals in maintaining biochemical and physiological functions, all metals exert their toxic effects via metabolic interference and mutagenesis. These metals affect various organs in animals, with the liver being typically the first impacted followed by the kidneys, brain, and reproductive system. The accumulation of heavy metals results in both gross and histopathological changes, ultimately leading to impaired growth and production. Prevention is paramount in addressing heavy metal contamination in livestock. Phytoremediation and intercropping can help to remove heavy metals from the environment before ingestion by animals. If heavy metals do enter the body, entero-absorbents can be employed to chelate them. Additionally, heavy metals commonly induce oxidative stress through various mechanisms, leading to altered redox potential, so including antioxidants in the therapeutic regimen has shown promise in significantly reducing the toxic effects associated with heavy metal exposure. Moreover, upcoming research will benefit from evaluating innovative targets as protective measures against organ toxicity caused by heavy metals.</p>
</sec>
</body>
<back>
<sec id="s3">
<title>Author contributions</title>
<p>AA: Writing&#x2013;review and editing, Writing&#x2013;original draft, Software, Methodology, Investigation, Formal Analysis, Data curation, Conceptualization. NM: Writing&#x2013;review and editing, Software, Methodology.</p>
</sec>
<sec sec-type="funding-information" id="s4">
<title>Funding</title>
<p>The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.</p>
</sec>
<sec sec-type="COI-statement" id="s5">
<title>Conflict of interest</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
<sec sec-type="disclaimer" id="s6">
<title>Publisher&#x2019;s note</title>
<p>All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p>
</sec>
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