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Hegedus, C.; Pașcalău, S.; Andronie, L.; Rotaru, A.; Cucu, A.; Dezmirean, D.S. The Influence of Heavy Metal. Encyclopedia. Available online: https://encyclopedia.pub/entry/42693 (accessed on 02 July 2024).
Hegedus C, Pașcalău S, Andronie L, Rotaru A, Cucu A, Dezmirean DS. The Influence of Heavy Metal. Encyclopedia. Available at: https://encyclopedia.pub/entry/42693. Accessed July 02, 2024.
Hegedus, Cristina, Simona-Nicoleta Pașcalău, Luisa Andronie, Ancuţa-Simona Rotaru, Alexandra-Antonia Cucu, Daniel Severus Dezmirean. "The Influence of Heavy Metal" Encyclopedia, https://encyclopedia.pub/entry/42693 (accessed July 02, 2024).
Hegedus, C., Pașcalău, S., Andronie, L., Rotaru, A., Cucu, A., & Dezmirean, D.S. (2023, March 31). The Influence of Heavy Metal. In Encyclopedia. https://encyclopedia.pub/entry/42693
Hegedus, Cristina, et al. "The Influence of Heavy Metal." Encyclopedia. Web. 31 March, 2023.
The Influence of Heavy Metal
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This entry is adapted from the peer-reviewed paper 10.3390/agriculture13030735

There are a multitude of sources of heavy metal pollution which have unwanted effects on this super organism, the soil, which is capable of self-regulation, but limited. Living a healthy life through the consumption of fruits and vegetables, mushrooms, edible products and by-products of animal origin, honey and bee products can sometimes turn out to be just a myth due to the contamination of the soil with heavy metals whose values, even if they are below accepted limits, are taken up by plants, reach the food chain and in the long term unbalance the homeostasis of the human organism. Plants, these miracles of nature, some with the natural ability to grow on polluted soils, others needing a little help by adding chelators or amendments, can participate in the soil detoxification of heavy metals through phytoextraction and phytostabilization.

heavy metals health risks phytostabilization/phytoextraction

1. Phytotoxicity of Heavy Metals and Impact on Plants

The negative impact on plants depends on the metal, the form or compounds of the metal, and the ability of plants to regulate or store the metal [1]. The toxic response in plants varies between different heavy metals because the heavy metals possess different sites of action [2]. The toxic level of plant exposure to heavy metals leads to physiological, metabolic [3], structural, biochemical and molecular changes in their tissues and cells [4].
Some of the phytotoxic manifestations include the generation of reactive oxygen species and reactive nitrogen species [5], the replacement of enzyme cofactors, transcription factors, the inhibition of antioxidant enzymes [6], ion transport imbalance, DNA damage, protein oxidation and peroxidation of lipids [7][8], as well as affecting nutrient metabolism and influencing the absorption of essential macro and micro minerals [9].
The most common visual evidence of the stress given by the presence of heavy metals consists of the decrease in the growth capacity and reproductive capacity in plants [10][11][12], the speed of seed germination decreasing [13][14], photosynthetic pigments being reduced [15], and, as a result, the capacity for chlorophyll assimilation decreasing and the number of leaves decreasing, with chlorosis, leaf necrosis occurring, and curly leaves [16][17][18].

2. The Negative Impact of Heavy Metals on Human Health

Some heavy metals, such as Zn, can be eliminated from the human body in a few days [19][20]; others, such as Cd, remain for 16–33 years in the human body [21].
As a general characterization, heavy metals cause damage to the DNA structure [22][20][23][24]. Carcinogenic effects are produced by their mutagenic capacity [25][26]. Through the action of free radicals produced (OH, H2, H2O2), cellular destruction occurs when they act at the lipids level and the loss of the functionality of cell membranes occurs when the action acts on proteins [27]. Heavy metals can affect the normal functioning of the brain, lungs, kidneys, liver and other organs [24][28][29]. Long-term exposure can lead to the progression of physical, muscular and neurological degenerative processes, and the onset of diseases such as multiple sclerosis, Parkinson’s disease, Alzheimer’s, and muscular dystrophy [30][31]. The weakening of the immune system can induce immune diseases such as Hashimoto’s, Graves’, lupus, rheumatoid arthritis and Sjogren’s [32]. Delays in intrauterine development, intrauterine fetal deformities [29] and partial blindness are effects of Al, Cd, Mn and Pb ingestion [33], which can also accumulate in bone and fat tissue [34]. In addition to other diseases and cardiovascular, gastrointestinal and allergy effects, heavy metals also affect the reproductive sphere [34][35].

3. Food Safety Possibly Threatened by the Consumption of Edible Plant Products and Mushrooms as Source of Vegetable Protein

Vegetable products, fruits and vegetables, in addition to components such as proteins, vitamins, fibers, antioxidants, iron and calcium, may contain varying amounts of heavy metals, which may threaten the integrity of human health [36]. Contaminant limits are regulated in industrialized countries, but not in developing countries where rapid industrial development and demographic explosion, together with the lack of pollution control, have caused an enormous increase in the contamination of agricultural soils with heavy metals [37].
The sources of soil pollution, along with the accumulation of heavy metals in plants, especially vegetables, and this reaching the food chain, have been studied in various areas of the world (Table 1).
Table 1. Main sources of heavy metals and accumulation in products of vegetable origin.
Species Country The Source of Heavy Metals Accumulated Heavy Metals Author
1. Capsicum annuum (green pepper) and Lactuca sativa (lettuce) Northern
Ethiopia		 Irrigated soil Cu and Zn [32]
2. Beta vulgaris subsp. Vulgaris (Swiss chard) Fe, Mn, Cr, Cd, Ni and Co
3. Lactuca sativa (lettuce) and Solanum lycopersicum L. (tomato) Cd
4. Capsicum annuum (green pepper), Solanum lycopersicum L.(tomato), Allium cepa (onion) Pb
1. Allium cepa (onion, shoots and leaves)
2. Solanum tuberosum (potatoes)
3. Daucus carota (carrot)		 Greece Irrigated soil 1. Cr (VI), Ni (II)
2. Ni can also pass to potatoes, depending on the irrigation concentration of the two heavy metals, through cross contamination
3. The results did not prove that Cr and Ni can cross-contaminate carrot bulbs.		 [38]
1. Lactuca sativa (lettuce)
2. Cichorium endivia L. (endive)
3. Triticum (wheat) and Oryza sativa (rice)		 China Phosphate fertilizer, leakage of factory sewage 1, 2. Cd it has a concentration 4 times higher in leaves than in roots and 20–30 times higher than the concentration in the soil
3. Cd is accumulated in grains		 [39][40]
1. Spinacia oleracea (spinach)
2. Brassica oleracea (cabbage)
3. Solanum melongena (eggplant)
4. Daucus carota (carrot)		 India Irrigated soil Cd (1.30 ± 0.31 mg kg−1), Pb (4.23 ± 0.32 mg kg−1), Cu (1.42 ± 0.25 mg kg−1), Zn (3.4 ± 0.28 mg kg−1), Cr (1.16 ± 0.11 mg kg−1) and Ni (2.45 ± 0.86 mg kg−1) [41]
1. Mentha piperita (mint)
2. Spinacia oleracea (spinach)
3. Daucus carota (carrot)		 India Irrigated soil (wastewater) 1. Fe, Mn, Cu and Zn
2. Fe, Mn
3. Cu, Zn		 [42]
Solanum lycopersicum (tomatoes) Romania Experimental field Cu > Zn > Pb; [43]
Brassica oleracea (cabbage), Solanum lycopersicum (tomatoes) Ethiopia Soil As, Pb, Cd, Cr and Hg (even if the concentration is below the tolerable limit/day there is a risk of intoxication) [44]
1. Spinacia oleracea (spinach)
2. Solanum melongena (eggplant)
3. Cucurbita pepo L. (pumpkin)		 Pakistan Sewage
water		 1. Mn, Cr and Fe
2. Cd, Ni, Zn
3. Cu		 [45]
1. Spinacia oleracea (spinach)
2. Spinacia oleracea (spinach) >
Brassica oleracea var. italica (broccoli) >
Solanum lycopersicum (tomatoes)
3. Spinacia oleracea (spinach) > Beta vulgaris and (beetroot) > Petroselinum crispum (parsnips)		 Serbia Soil
(farm producers)		 1. Cd, Pb (Spinach appears to have the highest accumulation of heavy metals)
2. Ni
3. Cr		 [46]
1. Allium porrum (leek)
2. Petroselinum crispum (parsley)
3. Allium cepa (onion)		 Turkey Soil 1. As, Cu
2. Ni, Mn
3. Zn, Cd, Pb		 [47]
Solanum Tuberosum L. (potatoes) Turkey Soil cause by roadside industrial places irrigating pesticides High: zinc, copper, nickel
Less: cadmium, lead, chrome		 [48]
1. Solanum lycopersicum (tomatoes leaves)
2. Cucurbita pepo (zucchini)		 Italy Airborne pollutants 1. Cd, Cr, Ni, Sn, Zn,
2. Ni, Sn, Zn, Ba		 [49]
1. Lycopersicum (tomatoes) > Allium sativum (garlic) > Solanum melongena (eggplant)
2. Allium cep (onions), Allium. Sativum (garlic), Solanum lycopersicum (tomatoes) and Solanum melongena (eggplant)		 Pakistan Waste water and household wastes and the use of heavy duty vehicles to convey sand from the river Acid–lead batteries as waste dumped in the river 1. Cu
2. Pb, Co		 [50]
Lactuca sativa (lettuce) > Allium cepa (onions) > Daucus carota (carrots) India Polluted and degraded environmental conditions Pb [51]
Malus domestica (apple fruits) Greece Local geology, plus fertilizers, pesticides, fungicides and insecticides As (0.05–0.2); Cd (0.01–0.1); Hg (0.001–0.008)
Ni (0.05–0.7);Pb (0.01–0.46); Zn (1.1–10.3)		 [52]
Lactuca sativa (lettuce), Amaranthus (amaranth), Vigna unguiculata (cowpea), Oryza sativa (rice) China Soil near by coal-fired power plants, thermal power plants Hg [34]
1. Lactuca sativa (lettuce)
2. Phaseolus vulgaris L. (bean)		 Hungary Irrigated water containing sodium arsenate (0.1, 0.25 and 0.5 mg L−1) 1. As: root > stem > leaf > bean fruit
2. root > leaves		 [53]
Beta vulgaris L. (Spinach leaves) Bangladesh soil ppm [34]
Cr Mn Ni Cu Zn As Sr Cd Pb  
<0.05 <0.06 <0.65 5.59 ± 0.33 112.24
± 0.47		 <0.01 23.75
± 0.23		 <0.06 0.98
± 0.00
Lycopersicon esculentum L. (tomato) 0.51 ±
0.03		 <0.06 <0.65 3.62
± 0.29		 31.1
± 0.43		 0.05
± 0.0		 <0.14 <0.06 0.12
± 0.00
Raphanus sativus L. (radish—root) <0.05 0.87
± 0.13		 0.87 ± 0.13 4.45 ± 0.34 25.78
± 0.46		 0.05
± 0.00		 7.23
± 0.28		 0.65
± 0.05		 0.51
± 0.06
Phaseolus lunatus L. (bean—fruit) <0.05 25.95 ± 2.56 0.87 ± 0.13 5.91 ± 0.22 68.34
± 0.44		 0.05
± 0.00		 <0.14 <0.06 0.65
± 005
Daucus carota var sativus L. (carrot—root) <0.05 <0.06 <0.65 5.35 ± 0.31 45.28
± 0.45		 0.04
± 0.00		 <0.14 <0.06 0.72
± 0.03
Brassica oleracea L. (cauliflower—inflorescence) <0.05 <0.06 0.94 ± 0.29 4.59 ± 0.35 42.05
± 0.43		 0.05
± 0.00		 <0.14 0.16
± 0.04		 0.23
± 0.00
  Pakistan Soil mg/kg dw Cd Pb Ni Co Zn Cu Mn [54]
Coriandrum sativum (coriander) 0.23 2.12 0.77 0.47 36.65 5.92 21.65
Allium cepa (onion) 0.13 0.66 0.54 0.32 23.94 6.25 20.15
Lycopersicon esculentum L. (tomato) 0.14 0.46 0.89 0.22 16.77 4.77 14.46
  Quatar Soil
Irrigated farms		 mg/kg V Cr Ni Cu As Cd Pb  
Eruca vesicaria (rocca) 17.09 6.41 1.70 13.074 14.72 0.9 6.36 [55]
Coriandrum sativum (coriander) 15.91 6.03 1.38 15.30 16.86 0.43 5.00
Petroselinum crispum (parsley) 16.25 6.26 2.19 17.97 16.60 0.51 5.46
Almost all plants accumulate small amounts of Pb, because it is normally found in the earth’s crust in a percentage of 0.002%; however, among the plants studied by Zulfiqar, U. et al. [56], it seems that Brassica oleracea L. var. capitata (cabbage) accumulates high levels of Pb (1.7 mg kg−1). Among the cereals Triticum aestivum (wheat), Zea mays (maize), Avena sativa (oat), Hordeum vulgare (barley) and Secale cereale (rye), Zea mays accumulates 0.88 mg kg−1 followed by Avena sativa and Secale cereale (0.64 mg kg−1). In addition to Pb, Brassica oleracea var. botrytis. (cauliflower) and Brassica oleracea L. var. capitata have a high affinity for Ni but a low one for Cd and Cu.
Fruit-type vegetables Pisum sativum (peas), Glycine max (soybean) and Cyamopsis tetragonoloba (cluster bean) can be grown on soils contaminated with Cd because it is not absorbed in the edible parts, but these crops are not suitable for soils contaminated with Ni and Pb. Root vegetables such as Daucus carota (carrots) and Raphanus raphanistrum (radish) accumulate small amounts of heavy metals, but leafy vegetables such as Spinacia oleracea (spinach), Amaranthus sp. (amaranthus) and Sinapis sp. (mustard) accumulate both essential and non-essential metals: Cd, Ni and Pb. Allium cepa L. (onion) and Solanum tuberosum (potatoes) accumulate high amounts of Cd and Ni, and low amounts of Zn and Cu [57].
Glycine max L. can accumulate large amounts of Pb [58], and Solanum melongena (eggplant) can accumulate Cd, Pb and Mn; Lycopersicon esculentum (tomato) can have large amounts of Fe, Pb, Mn and Zn [59].
Solanum tuberosum L. belongs to the category of candidate plants for the bioremediation of soils contaminated with Pb [60]. The positive correlation between heavy metals in the soil and their content in potato tubers varies, however, depending on the cultivars [61]. Codling, E.E et al. [62] recommend eating peeled potatoes, because Pb and As are mostly found in the peels.
Although a value below 300 ppm Pb is considered safe for consumption and Pb does not accumulate in the fruiting parts of tomatoes, strawberries and apples, still, those can be contaminated due to deposits on plants in a greater proportion than the absorption of lead by the plants [63]. From cereals and legumes, wheat, corn, oats, beans and lentils, rice has the highest capacity to accumulate heavy metals [64].
Asgari, K. and Cornelis, W.M. [65] found that, in Triticum aestivum (wheat) and Zea mays grains (maize), the concentration of Cd and Cr exceeds the safety limit and maize grains have the ability to accumulate large amounts of Cr. Brassica oleracea subsp. capitata f. alba has the ability to accumulate large amounts of zinc in cabbage heads, being considered a candidate for zinc phytoextraction [66].
Solanum tuberosum L., beans, fruits, cereals, especially rice, olive oil [67][68], Brassica oleracea and Amaranthus oleracea contain significant levels of mercury [69].
Among the fruit trees, peaches and apricots are very sensitive to the increase of arsenic in the soil and apple and pear are the least sensitive and cherry is intermediate, according to Torres, M. [66].
Stevia rebaudiana (candyleaf) accumulates large amounts of As, Cd, Cr, Cu, Fe, Mg, Pb, Se, Zn, Al, Ag, Co, Ca, Mn and Ni in flowers and edible parts such as leaves and stems [70]; Taraxacum officinale (dandelion) is recognized as a hyperaccumulator for Cd, Zn and Cu [71], and Artemisia dracunculus (tarragon) bioaccumulates Pb and Hg [72].
From the category of medicinal plants that can take up large amounts of heavy metals, Bağdat, R.B. et al. [73], Pirzadah, T.B. et al. [74] and Gawęda, M. [75] mention Mentha arvensis (mint—Cu, Zn), Lavandula vera (lavender—Pb, Zn, Cd), Rosmarinus Officinalis (Cd, Pb), Matricaria chamomilla (Cd, Zn, Pb), Aloe vera (Cr), marigold, hollyhock, carraway, garlic, Rumex Acetosa (garden sorrel: high affinity for Pb, Cd Zn, Cu, Mn, Fe, Cr, Ni) and Cannabis sativa (common hemp). The melliferous plants, Sambucus nigra L., Hypericum perforatum and Tilia tomentosa, accumulate Cd from the soil in the parts of the plants consumed as a tea infusion [76].
Boawn, L.C. and Rasmussen, P.E. [77] specify that the toxic potential of heavy metals in the above-ground parts of plants, including leaves and stems, varies according to plant species and occurs at values > 400 mg Zn/kg, Mn > 1000 mg/kg and Cu > 40 mg/kg.
A valuable source of vegetable protein for human consumption is edible wild species of mushrooms: Armillaria mellea, Cantharellus cibarius, Coprinus comatus, Lycoperdon perlatum, Tricholoma portentosum, Suillus luteus and Xerocomus badius, that can accumulate Hg, Pb, Cd and As. L.perlatum concentrates the highest amounts of Hg and As in the results obtained by Nowakowski, P. et al. [78]. Other edible mushrooms, such as Boletus pulverulentus, Cantharellus cibarius, Lactarius quietus, Macrolepiota procera, Russula xerampelina and Suillus grevillei, show a high capacity to accumulate Hg, Cd and in some cases Pb [79]. The presence of mercury in Imlera badia, Boletus subtomentosus and Xerocomellus chrysenteron is dependent on its amount in the soil, but among all species, Boletus subtomentosus can represent a real threat to consumer safety due to the high capacity to accumulate this metalloid [80]. The amount of Hg in Pleurotus ostreatus is also dependent on the degree of soil or substrate contamination [81].

4. The Potential Risk of Contamination of the Food Chain with Products of Animal Origin and Bee Honey

In small quantities, certain metals such as Mn, Zn, Fe or Mo are essential for the normal functioning of the human or animal body, but in large quantities they can become toxic and can accumulate in some organs and/or tissues together with other non-essentials [82]. Comparatively, among the organs with affinity for Pb accumulation, its values in the kidneys are slightly higher, in horses, cows, pigs and lambs, than in the liver, “the body’s detoxification plant” [83]. Soil contamination with Pb affects the quality of feed administered to dairy animals, reaching, in this way, the food chain, through milk [84]. Arnich, N. et al. [85] found Ni, Cr, Pb, Hg and Ca in the content of cow’s milk. According to Briffa, J. et al. [86], heavy metals may be present in products of animal origin such as Cr in meat, Co in meat, butter and cheese, Cu in liver, As in meat, poultry and dairy products, Cd in liver, Pb in red meat and Zn in lamb, beef and cheese. Research conducted by several authors demonstrates the potential for the accumulation of heavy metals in different organs, tissues, and edible products, both in farm animals and in wild ones.
The authors [87][88] found Pb and Cd in muscle tissue from cows, sows and even wild boars, Cu in the livers of wild animals and animal farms, and in beef, pork and broiler chicken both frozen and fresh meat [89][90][91][92][93]. A series of research [86][94][95][96][97][98] has highlighted the fact that, in the egg/yolk albumen, Cu, Zn, Ni, Cr, Pb, Cd, Hg and As are present in different amounts depending on the geographical area.
Not only products of vegetable or animal origin can contain heavy metals, but also honey and bee products. Most often, honey and bee products are considered detectors of air pollution. Pollen can be considered a bioindicator of environmental pollution, while honey is considered a detector of lead in time and space [99]. Depending on the area and harvesting period, the quality and composition of honey and bee products can be “enriched” with heavy metals and metalloids: Ag, As, Cd, Cr, Cu, Pb, Sn, Zn, Ni and Hg [100][101][102][103]. More recently, bees have come to the attention of researchers to highlight the links between soil–plant–bee body-beekeeping products [104]. Borg, D. and Attard, E. [105] demonstrate that there is an extremely positive correlation between soil contamination, the accumulation of stannum (Sn) and As in plants, and the amount of these heavy metals in honeybees and propolis. The research carried out by Bakhtegareeva, Z. et al. [106] highlighted the fact that, on an alkaline soil rich in Cu and As, all bee products, but especially bee bread, accumulate high amounts of these metals.
Tomczyk, M. et al. [107] believe that Cd migration is possible through the soil–plant–bee–honey food chain due to melliferous plants such as goldenrod and Taraxacum officinale, considered Cd accumulators. Bees, although they can avoid plants whose principles are toxic, are not able to detect heavy metals in plants except at high concentrations, when they were found to decrease bee visit duration at Helianthus annus (sunflowers). If this finding applies to all melliferous plant accumulators and hyperaccumulators, the negative impact would be reflected in the entire ecosystem by reducing pollination [108][109].

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Cristina Hegedus
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Luisa Andronie
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