Fruits and vegetables contaminated with particles of heavy metals: A narrative review to explore the use of electromagnetic fields as an alternative treatment method

Abstract Heavy metal pollution is a growing problem in the world. Regardless of the amount of heavy metal concentration in the soil, heavy metals can be easily absorbed by vegetable roots and accumulate in high concentration in the edible parts of plants. Studies have been conducted to associate the application of electromagnetic fields to treat fruits and vegetables contaminated with heavy metals. Primarily, this paper provides knowledge on the use of electromagnetic fields to remove heavy metals from contaminated fruits and vegetables and subsequently to highlight health effects associated with consumption of fruits and vegetables contaminated with heavy metals. In this paper, Google Scholar, PubMed, NCBI Science Direct, and Research Gate were utilized to conduct a literature search. Out of 72 articles, 51 were selected and used to compile this paper. A comparison of studies was conducted on the possible health effects of consuming fruits and vegetables contaminated with heavy metals. The application of electromagnetic fields to treat fruits and vegetables contaminated with heavy metals should be implemented as one of the methods necessary to remove heavy metals, as they are environmentally friendly and do not use chemical agents or microbiota.


Introduction
Globally, industries play an essential role in the development of every country's economy.Effluents from these particular industries contain heavy metals, and lead to soil and land pollution, which are a significant threat to food security.The release of heavy metals to the environment has been attributed to detrimental effects on both human and animal health leading to health-induced ABOUT THE AUTHORS Dr. Phoka Rathebe is young emerging scholar appointed as a senior lecturer at the University of Johannesburg, Faculty of Health Sciences, Department of Environmental Health.He focuses on exposure assessments for ionizing and non-ionizing radiation.Lerato Mosoeu is a MHSc.Environmental Health student at the Central University of Technology, Free State, Department of Life Sciences.His project is supervised by Dr Carien Weyers and Dr Phoka Rathebe.
outcomes in the gastrointestinal tract, nervous and immune systems or the formation of neoplasms (Balali-Mood et al., 2021).It is well known that vegetables and fruits are the most common food products consumed by humankind (Ruzaidy & Azura, 2020), and they provide necessary health benefits such as vitamin supplements, minerals, fiber, antioxidants, and antibacterial agents (Ali & Al-Qahtani, 2012).As a result of their benefit, these food products are the main significant crops in agricultural sectors, and are farmed on a big scale (Ruzaidy & Azura, 2020).Various methods and technologies are utilized to ensure growth and development of these products.In contrast, small-scale farmers continue to cultivate fruits and vegetables oldfashioned way, and harvested for market sales (Ruzaidy & Azura, 2020).Since fruits and vegetables are cultivated through soil, Gonzalez Henao and Ghneim-Herrera (2021) suggest that heavy metals such as arsenic (As), lead (Pb), cadmium (Cd) and mercury (Hg) from industrial processes can contaminate the soil.They can easily be absorbed from metal-polluted soil by the roots and build up to high levels in the edible parts of plants (Jolly et al., 2013).Consumption of heavy metals remains severely harmful to human health due to their longer biological half-life, nonbiodegradable nature, and can build up in different body parts (Heidarieh et al., 2013).In addition, due to the presence of pollutant particles in the ambient air, which suspend on earth surface, heavy metals may accumulate on fruits and vegetables surfaces.Figure 1 illustrates the interaction between heavy metals from polluted soil, fruits and vegetables and human health.
Consumption of fruits and vegetables contaminated with heavy metals introduces health destructive toxins to the internal body target organs.These toxins further metabolize and directly accumulate in the blood stream and cell tissues (Tasrina et al., 2015).Health risks associated with consuming contaminated fruits and vegetables are mostly dependent on the amount of contaminated products consumed, underlying health conditions, consumption frequency and person's own body makeup.However, due to inherent hygiene practices, such as washing of vegetables and fruits prior consumption, heavy metals remain in low concentration suggesting apparent health effects after several years of exposure (Bortey-Sam et al., 2015).The most common heavy metals are arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), zinc (Zn), nickel (Ni), manganese (Mn), lead (Pb), and iron (Fe) (Ullah et al., 2022), coming from industrial effluents, municipal waste, and natural disasters (Chibuike & Obiora, 2014).Water used for irrigation purposes mixed with effluents from these industries has direct effects on plants' seed development and reduced early growth (Pandey & Madhuri, 2014).Furthermore, lead (Pb) is reported to be the most detrimental heavy metal attributed to reduced plant growth where irrigation water is mixed with industrial effluents (Ullah et al., 2022).
According to Hossain et al. (2010), a large amount of waste is landfilled and dumped into the nearby rivers, acting as sinks for the waste disposal from industries.The widespread practice of using such contaminated water for agricultural products also poses a tremendous harm on consumers' health, reduces quality and growth of vegetables and crops, subsequently leading to numerous health issues (Gola et al., 2016).Kotuła et al. (2022) suggest that a healthy diet mostly consists of fruits and vegetables.The Polish Institute of Food and Nutrition recommends consuming at least 400 g of fruit and vegetables per day, with higher vegetable consumption being preferred.The United Nations Food and Agriculture Organization of the World Health Organization (FAO/WHO) issued the similar recommendation.Rusin et al. (2021) discovered that lead (Pb) and cadmium (Cd) levels in vegetables and fruits were only sometimes exceeded, with 9.3% vegetables, 1% fruits (Pb), and 2% vegetables (Cd).Through the literature, it is found that different methods are explored to treat fruits and vegetables contaminated with heavy metals.Such methods include the potential use of microbiota (Gonzalez Henao & Ghneim-Herrera, 2021), multidimensional detoxification approach (Rizvi et al., 2022), nanobiochar (Zhang et al., 2022) and other reliable methods.However, there is scarcity of literature in an attempt to use electromagnetic fields to treat heavy metals contamination in agricultural products.The objective of this review is to explore the use of electromagnetic fields as an alternative method to treat fruits and vegetables contaminated with heavy metals.

Literature search
A literature search was conducted using Google Scholar, PubMed, NCBI Science Direct and Research gate.The search was limited to articles focusing on the use of electromagnetic fields to treat vegetables and fruits contaminated with heavy metals published between 2012 and 2022.Search terms such as "heavy metals" and "fruits and vegetables" or "Electromagnetic fields" and "heavy metals" were used.The subject headings were "heavy metals" [All Fields] AND "vegetables and fruits" [All fields] or "Electromagnetic fields" [All Fields] AND "heavy metals".Articles were selected and narratively reviewed.A total of 72 articles met the search criteria requested.Of these,

Fruits and vegetables
Vinegar solution 51 titles appeared to be relevant to electromagnetic fields as well as fruits and vegetables contaminated with heavy metals and 21 titles were excluded.
In this study, other methods apart from electromagnetic fields used to treat heavy metal contamination in vegetables, fruits and agricultural crops were searched.Table 1 provides some of the recent widely used methods for removal of heavy metals in vegetables, fruits and other food products.
Previously, several studies have focused on the beneficial application of electromagnetic fields to treat wastewater (Rajczykowski & Loska, 2018;Rivera et al., 2019;Wang et al., 2021;Yadollahpour et al., 2014), and the possibilities to use electromagnetic fields to treat metal-polluted fruits and vegetables have not be sufficiently investigated.In the present study, we explore and propose the use of electromagnetic fields as an alternative treatment approach for vegetables and fruits contaminated with heavy metals.Mainly, these agricultural products are harvested from metal polluted soil.Bathla and Jain (2016) regard metals or semi-metals as any kind of metal contaminant present in an unfavorable location, in a form of a concentration, and produce acute or severe health effects on humans and their environment.Such metals are lead (Pb), cadmium (Cd), mercury (Hg), arsenic (As), chromium (Cr), copper (Cu), selenium (Se), nickel (Ni), silver (Ag), and zinc (Zn).However, aluminum (Al), cesium (Cs), cobalt (Co), manganese (Mn), molybdenum (Mo), strontium (Sr), and uranium (U) are also common metallic pollutants (Singh et al., 2011).Heavy metals such as lead and cadmium can significantly increase the levels of soil heavy metal content due to poorly disposed of batteries; however, arsenic is most frequently in the soil due to the ash from coal combustion (Ruzaidy & Azura, 2020).These compounds are easily adsorbed onto the soil, transported over a short distance to ground or surface water, and directly to the plant roots (Wuana & Okieimen, 2011).The absorption of metals into plant roots makes them extremely difficult to be removed (Elbagermi et al., 2012), attributes to health-induced outcomes on the fruits and vegetables consumers, and requires appropriate remedial approaches.

Sources of heavy metals on soil to crops (vegetables and fruits)
The pollutants deposition, livestock manure and phosphate-based fertilizers, irrigation using waste or polluted water, application of herbicides, and sludge-based additives remain the principal sources of heavy metals in the agricultural soil (Elgallal et al., 2016;Lv et al., 2015).Particulate matter (PM 2.5 or 10 ) from Industries and vehicle emissions eventually fall of, build up in the soil and threaten sustainability of the food chain (Franca et al., 2017;Rai, 2016aRai, , 2016b)).According to Li et al. (2017), consumption of lettuce, amaranth, water spinach, cowpea, and grains produced on Hg-contaminated soil is a potential health hazard.Similarly, a number of processes such as the use of wastewater for irrigation, sewage sludge as a soil additive for food crops, and PM deposition on soils and crops are significant risks to food security.In many countries, particularly low and middle income, lack adequate water supplies to support their agricultural needs.Poorly treated wastewater and sewage sludge are utilized to assure agricultural production; however, the quality and safety of food crops cultivated on soil irrigated with improperly treated water cannot be guaranteed (Bourioug et al., 2015;Jaramillo & Restrepo, 2017).The use of unreliable or poorly treated wastewater and sludge for irrigation purposes has been directly linked to rising public health concerns (El-Kady & Abdel-Wahhab, 2018).According to Chandra and Kumar (2017), heavy metals such as Fe, Cu, Cr, Pb, Ni, and Mn have been previously found in higher concentrations in sludge from distilleries, electroplating, textile, and leather industries.In China, Franca et al. (2017) found that Pb-acid battery manufacturing facilities released metals bound in the form of PM, which eventually deposit in soil and plant of the agroecosystem.

Related studies conducted on fruits and vegetables contaminated with heavy metals
A number of health challenges have been linked to consumption of fruits contaminated with heavy metals.Dickin et al. (2016) suggest that metal-polluted fruits lead to improper nutritional balance, gastrointestinal tumors, weakened immune system, and induced mental retardation.Consumption of heavy metals is mostly inadvertent, and leads to buildup of metal particles in bone structures or adipose tissues.Dickin et al. (2016) further indicated that a significant amount of Pb and Cd were removed from the pericarp, ranging from 50% to 80% Pb and 30% to 60% Cd.It is evident that a considerable percentage of pollutants from machinery and vehicle emissions are deposited on crops.The well-known hygiene practice of thoroughly washing vegetables and fruits before consumption remains a readily available solution to reduce metal contents on edible agricultural products.In 2011, a study by Aweng et al. conducted in Kota Bharu, Kelantan, Malaysia, found a high concentration of heavy metals in soil and irrigation water, which to heavy metal build-up in vegetables.The study showed that accumulation of heavy metals on vegetables differed among vegetable plants, and irrigation water used, was a dominant factor that led to high concentration compared to soil.In 2014, Elbagermi et al. found the levels of heavy metals in fruits and vegetables in the Misurata region of Libya to be within the permissible threshold limits recommended by the World Health Organization (1999).Due to compliance, they recommended ongoing biomonitoring of trace elements in freshly produced fruits.Figure 2 demonstrates varying concentrations of heavy metals on vegetables.Koleayo et al. (2017) found elevated levels of nickel (Ni) and chromium (Cr) in apples, which were above the WHO guidelines.High levels of heavy metals, such as Ni and Cr, are associated with the etiology of several effects such as cardiovascular, renal, and neurological conditions.Furthermore, excessive consumption of Ni and Cr is associated with skin rashes, stomach distress, kidney and liver damage as well as lung cancer.The study by Mawari et al. (2022) suggested that the accumulation of heavy metals (As, Cd, Hg and Pb) in fruits and vegetables was not attributed to the soil but direct irrigation using wastewater contaminated with heavy metals.In 2019, Prabhat et al. reviewed heavy metals in food crops: health risks, fate, mechanisms, and management, and reported that metal-pollutants have negative effects on crop quality, putting human health and food security in a significant danger.The sources of heavy metals in food crops vary greatly between industrialized and developing countries.In the developed countries, industrial wastewater and sewage sludge are the main sources of heavy metal  contamination to soil culture system, while irrigation with inadequately treated wastewater remains the main contaminator of food crops in developing countries.Fruits and vegetables contaminated with heavy metals pose health risks to both humans and animals.Table 2 provides a summary of studies reviewed in this section.

Health effects of consuming vegetables and fruits contaminated with heavy metals
Various factors expose individuals to particles of heavy metals.One of the key route of exposure for heavy metals is inadvertent ingestion through contaminated food.A range of internal biochemical processes tends to be disrupted by heavy metal exposure in food products and results in direct deposition of heavy metals in kidneys and liver, causing cardiovascular, neurological, kidney, and bone illnesses (Sankhla & Kumar, 2019).Table 3 shows some of the studies on heavy metals and health effects.

Application of electromagnetic fields to treat fruits and vegetables contaminated with heavy metals
The rising concentration of heavy metals in the environment is of great health concern.Both natural and synthetic activities, such as land pollution by waste disposal, the use of chemical fertilizers and pesticides, and sewage sludge to irrigate agricultural crops; have direct implications on the accumulation of heavy metals in soil and related environmental components (Kabatapendias & Pendias, 2011).Due to industrialization, climate change and a need for food security, it is essential to use appropriate heavy metal remediation techniques.In this section, the use of electromagnetic fields (EMFs) as an alternative heavy metal contamination remedial technique is explored.As opposed to other remedial methods indicated in Table 1, Mokarram et al. (2020) investigated the response of plants contaminated with heavy metals to electromagnetic waves ranging from 400 to 1030 nm at different growth stages.The findings suggested that the control samples had the lowest reflectance in 400-500 and 600-700 nm wavelength ranges, since the plants need to absorb light at these wavelengths in order to generate chlorophyll.On the contrary, in plants exposed to heavy metals, the rates of these waves' reflection increased.It was also evident that control plants had a low reflectance in the 700-750 nm spectrum range, which was required for embalming and fruiting.This was further discovered in the second stage of growth; plants polluted with Cd had greater reflectance in the 400-500 and 500-600 nm ranges, demonstrating a poor generation of chlorophyll.Based on the finding of this study, it is comprehended that there is viability and effectiveness for utilizing electromagnetic waves to detect illness, pollution, and stress in plants (Mokarram et al., 2020).Balakhnina et al. (2015) and Khetsha et al. (2022) indicated that pretreating seeds with physical elements like UV, laser, microwave, or ionizing radiation as well as with EMFs speed up seed germination, boosts plant growth, and activates enzymes, which in turn makes plants more resilient to stress.Similarly, Bulak et al. (2018) revealed that white mustard seeds exposed to either 60 or 120 mT alternating EMF (50 Hz) for 1 minute after adding Cd to the petri dish had higher Cd contents in shoots from EMF-treated seeds than the control (73% and 78%, respectively; p < 0.05).Plants exposed to 60 mT had a significantly lower (3%) Ca content than the control.Results above have shown the potential advantages of this physical seed pretreatment method in the context of Cd phytoextraction, and EMF stimulation had no influence on biomass production (Bulak et al., 2018).A study by Jin et al. (2017) used a multi-series system combining pipeline flow and induced electric field (IEF) to pretreat orange peel for essential oil extraction.From 0 V to 1 kV, the output of essential oils dramatically increased.Due to the dissolution of cell contents during the IEF pretreatment phase, fluid impedance decreased.There was also a slight drop in essential oil yield with increased frequency.A substantial difference in the yield of essential oils between the IEF pre-treatments and sample coils' various winding directions was observed.The use of IEF pretreatment to intensify essential oil extraction, without using metal electrodes, prevents corrosion of the electrode surface and heavy metal contamination (Jin et al., 2017).In the literature, there are limited studies that explore the use of EMFs to treat metal-polluted fruits and vegetables.Chen et al. (2017) compared the effects of exposing wheat seeds to a magnetic field (0-800 millitesla) and laser radiation (0-8 min at 20 mW/mm 2 ) on germination of wheat seeds as well as on the physiology and growth of early seedlings exposed to Pb and Cd.Higher germination was achieved at intermediate magnetic field (MF) and laser radiation (LR) levels.When Cd and Pb were exposed to seeds that had not received MF or LR, the concentrations of malondialdehyde (MDA), superoxide anion radicals, and electrolyte leakage conductivity significantly increased.Additionally, the activity of catalase, superoxide dismutase, and glutathione reductase reduced dramatically.Both MF and LR enhanced the physiological effects of Cd and Pb exposure on young seedlings, but only LR reduced Cd and Pb levels in the wheat (Chen et al., 2017).Figure 3 illustrates the use of magnetic fields to enhance plants tolerance for various environmental stressors, including heavy metals.
In 2019, Yusuf et al. discovered that using magnetized seed and water improved tomato yield by 44%, compared to using non-magnetized seed and water, which raised output by 27%.When compared to simply magnetizing the seeds and using non-magnetized water for irrigation, magnetized water had a higher effect on tomato yield.All heavy metal concentrations in the tomato were within FAO/WHO permissible levels, and magnetized water did not introduce any metal contents that would be detrimental to the biochemical processes of tomato and humans.A non-chemical, environmentally friendly technique that boosts crop output is magnetic treatment of irrigation water (magnetized water), and it should be embraced and used for agricultural production (Yusuf et al., 2019).In 2017, the study of Yusuf et al. suggested an average yield for tomatoes grown with Magnetically Treated Water (MTW) at percentages of 100%, 80%, and 60% to be 275.8,281.0, and 216.8 g/pot, respectively.While the equivalent yields for non-magnetically treated water (NMTW) were 200.1, 210.9, and 163.2 g/pot.Copper, Pb, Mg, and iron (Fe) concentrations in tomato for MTW at 100%, 80%, and 60% were 0.03, 0.02, and 0.12 mg/L, respectively, and the corresponding heavy metals for NMTW were 0.04, 0.02, and 0.08 mg/L.Zinc was 0.01 mg/L for MTW but undetectable for NMTW.The MTW boosted tomato productivity while decreasing the uptake of heavy metals that could pose health risks to humans.Mokarram et al. (2020) determined the levels of Cd, Zn, Pb, and Ni on peppers grown from contaminated soils.The responses of the target plants to various heavy metals were also examined using electromagnetic waves.Plants with Pb and Zn had the greatest target hazard quotients (THQ = 62 and 5.07, respectively).Principal Component Analysis and random search results showed that the best spectra for evaluating THQ were those at the bands of b570, b650, and b760 for Pb, b400 and b1030 for Ni, b400 and b880 for Cd, and b560, b910, and b1050 for Zn.Instead of determining heavy metals in plants by chemical analysis in the laboratory, the response of plants to electromagnetic waves in the identified bands can be readily investigated in the field based on the established correlations.Studies that use electromagnetic waves for treatment of fruits contaminated with heavy metals are relatively none existence in the literature.Many studies focus on fruits maturity (Araujo et al., 2016), quality retention (Jia et al., 2015) and protein synthesis (Saletnik et al., 2022).Studies included in this section suggest the use of EMFs as a pretreatment for seeds (for both fruits and vegetables) rapid germination, accelerated plant growth and enzyme activity as well as more resilient to environmental stress.It is worth noting that EMFs enhance plant tolerance to heavy metal intake by producing ROS, which activates cell division, photosynthesis, and growth of affected crops affected with Cadmium (Cd) (Radhakrishnan, 2019).

Conclusion
This study provided an overview of heavy metals uptake by fruit and vegetable plants.Various studies suggest that the use of industrial effluents, improper treated water, and sewage sludge contaminated with heavy metals for irrigation purposes are the main source of plants heavy metal uptake from the roots structure.Heavy metals related health risks are mostly attributed to inadvertent consumption of contaminated fruits and vegetables.Different techniques, mostly chemical and microbiota, have been used successfully to remedy heavy metals contamination from these products.However, these techniques reduce the quality retainment on the nutritional content of fruits and vegetables.The current study advocates for the use of EMFs to remove heavy metals uptake on fruit and vegetable plants, which has not been given much attention in the literature.This method introduces no harm to plant structures; instead, it accelerates seed germination, activates protein formation and produces ROS to enhance plants tolerance towards environmental stressors including heavy metals removal.It is noted that there are different and specific frequencies of EMFs that plants respond to positively.Future studies should explore the use of different frequencies and wavelengths of EMFs to determine which band could successful remove heavy metals contamination rapidly before human consumption.

Figure
Figure 1.Interaction between fruits and vegetables, heavy metals and health (adopted from a study of A. Kumar et al., 2019).

Figure
Figure 3. Magnetic field treatment for plants exposed to heavy metals (applicable to both fruit and vegetable plants) to enhance tolerance and produce reactive oxygen species (ROS) (adopted from a study of Radhakrishnan, 2019).

Table 1 . Current methods for treatment of heavy metals in plants References Contaminant Plant type (agricultural product) Treatment methods
(Cd)and lead (Pb).