Assessing bioaccumulation of Pb, Cd, and As in Goats: Impacts of exposure to mine tailings in a polymetallic mining region

doi:10.21203/rs.3.rs-4614307/v1

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Assessing bioaccumulation of Pb, Cd, and As in Goats: Impacts of exposure to mine tailings in a polymetallic mining region

https://doi.org/10.21203/rs.3.rs-4614307/v1

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Pb, Cd, and As concentrations were measured in blood, edible tissues, urine, feces, and hair samples from goats raised in the vicinity of the abandoned El Fraile mine tailings (Taxco de Alarcón, Mexico) to evaluate the bioaccumulation levels to Pb, Cd, and As. The goats were fed grains, grasses, and sprouts that grew on top of mine tailings and drank from the mine leachate for seven months, reproducing the natural conditions of goats raised around and on top of mine tailings. Blood showed the lowest Pb, Cd, and As concentrations, followed by edible tissues (leg muscle, brain, and lungs) whose concentrations were below Mexican permissible limits (NOM-004-ZOO-1994). However, urine showed higher concentrations of Pb and As, but feces showed even higher concentrations and hair and bezoars exhibited the highest Pb, Cd, and As values. Even though these data suggest that consuming edible tissues does not represent a risk to human health, the high Pb, Cd, and As concentrations in urine, feces, and hair suggest that goats were exposed to chronic poisoning. Additionally, isotope data indicate that Pb determined in blood, urine, and bezoars is related to the remanent mineralization present in the mine tailings, highlighting the hazard that mine tailings represent to the environment and settlers of the region.

Toxic elements

goat edible tissues

consumer food safety

health risk

Pb isotopes

• Pb, Cd, and As concentrations in edible tissue of goats do not exceed recommended values.

• Pb, Cd, and As values in urine, faces, and hair indicate toxic elements exposure and pollution.

• Pb isotope ratios in urine, blood, and hair indicate the contribution of toxic elements from mine tailings

• El Fraile mine tailings influence toxic elements contents in the living beings of the region.

Lead (Pb), cadmium (Cd), and arsenic (As) are at the top of the list of the five toxic elements (TE) of most concern for public health and the environment since they produce several adverse effects in human beings (Pan et al., 2012). Because Pb, Cd, and As are not essential for life, there are no threshold limits below which they can be considered safe (e.g. Seraj and Rahman, 2018; Peana et al., 2021). In the environment or animal/human tissue, Pb, Cd, and As are among the most harmful chemical pollutants. This is due to their ability to access different trophic levels of ecosystems to bioaccumulate and magnify, and to their almost zero capacity for biodegradation (Sarker et al., 2022). Once these TE are consumed, they persist in the body for a considerable time and, depending on the degree of exposure, induce acute or chronic exposure in the host (Munir et al., 2021). TE often mimic the chemical features of essential elements like calcium and magnesium; therefore, the TE gain access to critical cellular functions, leading to their bioaccumulation. TE are generally bound to biomolecules (proteins, enzymes, phospholipids, and hormones) to form chemical complexes that produce harmful alterations such as DNA damage, carcinogenesis, and detrimental cell cycle. Fergusson (1990) listed the principally hazardous effects and diseases that Pb, Cd, and As produce in the human body. Pb exposure could produce chromosomal abnormalities, toxicity to a fetus, decreased fertility in women, altered spermatogenesis, reduce peripheral nerve conduction, reduce hemoglobin synthesis, impaired kidney function, anemia, peripheral neuropathy, encephalopathy (Pan et al., 2012; Rebelo and Caldas, 2016). Cd exposure may generate lungs, kidneys, and bons affectations like bronchitis, pneumonitis, pulmonary emphysema, proteinuria, renal damage, and Itai Itai disease (Okereafor et al., 2020; Munir et al., 2021; Njoga et al., 2021). Exposure to As could produce intense abdominal pains, nausea, vomiting, diarrhea, coma, and death (Pan et al., 2012).

Mine tailings increase the concentrations of Pb, Cd and As until 1,000 times the background or regional geochemical baselines levels, therefore mine waste represents one of the most important sources of TE in the Earth's crust (e.g., Dudka and Adriano, 1997; Okereafor et al., 2020). Mining has been an important activity in the region of Taxco de Alarcón, southern Mexico, for more than five centuries, genereting more than 55 million tons of mine tailings (Werre-Keeman and Rodarte, 1999, Talavera et al., 2006) that were deposited preferably near the banks of the rivers (Fig. 1). In the community of El Fraile, two mine tailings (Fig. 1), the La Concha (~ 0.6 million tons of waste) and the El Fraile (~ 2.0 million tons of waste) were accumulated on the banks of the Cacalatenango river (Talavera et al., 2005). However, villagers herd their goats and cattle above the El Fraile mine tailings because of the abundant grow of fresh grass and shrubs (Fig. 2). Due to their agility and voracious appetite, goats roam these areas several times a day in search of food (Fig. 2); where plants such as wild grass and huizache (Vachellia farnesiana) are among the preferred ones. Unfortunately, these plants hyper accumulative TE (Hernández and Pastor, 2008), and when they are ingested by goats, the risk of TE bioaccumulating in the goats' tissues increases (Duruibe et al., 2007).

The main objective of this research was to perform an exploratory assessment regarding the bioaccumulation of Pb, Cd, and As in edible meat of goats reared close to the El Fraile mine tailings. The studied edible tissues included muscle, brain, long, liver, and kidney tissues, along with blood, urine, feces, and hair. The information obtained was used to evaluate the potential risk that mine tailings represent for residents since those who live near the mine tailings may breathe mine tailings particles and use the leachate water for domestic purposes and irrigation. Thus, in this work, goats are considered sentinels of TE exposure related to mine tailings. Additionally, Pb isotope composition was determined to trace the source of Pb found in the goats. The data provided may help estimate the risk represented by meat consumption from this type of cattle and identify which of the studied matrices is the best bioindicator of TE exposure.

Taxco de Alarcón is located north of the state of Guerrero in southern Mexico (Fig. 1). The main lithological units in the region include the rocks of the Lower Cretaceous Taxco Schist Formation, the Albian-Cenomanian limestone of the Morelos Formation, the Cenomanian-Turonian sandstone and shale of the Mexcala Formation, the Paleogene red beds and conglomerates of the Balsas Formation, and Oligocene felsic volcanic rocks of the Tilzapotla Formation (Fig. 1) (Campa and Ramírez, 1979).

This region has been one of the largest producers of metals in Mexico, and locals have practiced mining for more than 500 years (Armienta et al., 2003; Talavera et al., 2005; 2006). At least eight mine tailings were deposited in this municipality with high concentrations of TE (Pb, Cd, As, Cr, Cu, Fe, Se, and Zn) (Talavera et al., 2005). In particular, the El Fraile mine tailings deposit (Figs. 1 and 2) is located southwest of Taxco de Alarcón city, near the boundary between the El Fraile and Santa Rosa villages, where the mining activity was suspended ~ 1970 (Gómez-Bernal et al., 2010). The El Fraile mine tailings are made up of two separate but very close reservoirs (Fig. 1) that together hold a volume of 7,191,000 m³ (Talavera et al., 2005; Olea and Zúñiga, 2009; Galarza Z, 2009). The tailings materials are mostly oxidized and developed efflorescent crusts composed of iron hydroxides and sulfates. Sidewall toxicant traps (Fig. 2d and 2g) also contain oxidized mine tailings material and efflorescent mineral crusts, which often contain high concentrations of TE and are highly soluble (Fig. 2). The average concentrations of Pb, Cd, and As on the El Fraile mine tailings is 6,166.0, 5.8, and 3,744.3 mg kg^− 1, respectively (Talavera et al., 2005). Leachates from these deposits are discharged with a different flow rate the entire year along the Cacalotenango River, impacting the river water with Pb (~ 0.01 mg kg^− 1), Cd (~ 0.005 mg kg^− 1), and As (~ 0.022 mg kg^− 1) (Ruiz and Armienta, 2012; Dotor et al., 2014).

High concentrations in soils (Pb ~ 1334.83 mg kg^− 1 and As ~ 89.02 mg kg^− 1), roots and stalks of maize plants from agricultural plots (Pb: 0.93 − 0.88 mg kg^− 1, Cd:0.33–5.65 mg kg^− 1, and As:0.42–4.62 mg kg^− 1) have been reported (Díaz-Villaseñor, 2006). Also, high lead blood concentrations (> 10 µg dL^− 1) were determined in women of reproductive age from the Santa Rosa and the El Fraile communities (Vázquez-Bahena et al., 2017).

Raising goats is a common economic activity in the rural communities belonging to the municipality of Taxco de Alarcón (e.g., El Fraile, Santa Rosa, Dolores, Tecalpulco, Campuzano). The goat meat plays an important role in the regional cuisine since various butcher shops sell the traditional Guerrero-style barbecued goat. Locals who raise goats in the Santa Rosa and the El Fraile region increase their profits by herding the goats over the El Fraile tailings (Fig. 2f). Unfortunately, the growth of grass and “huizache” plants (Vachellia farnesiana ) over mine tailings can potentially bioaccumulate TE in their tissues (root, stem, leaves, and fruits) (Chaney et al., 1997; Becerril et al., 2007; Landeros et al., 2011).

3.1 Experimental phase

Four creole-breed male goats (four months old) were selected for the experimental phase with an average weight of 13 kg. The four goats were obtained from a farm located in the community (Coacoyula de Álvarez, Guerrero) with non-pollution records by mine waste. The experimental phase was divided into two time periods that consisted of (1) adaptation, which lasted three months (May - July 2017), and (b) exposure, which lasted six months (August 2017 - January 2018), where the blood and urine samples were taken monthly. Three goats (CX-01, CX-02, and CX-03) were placed and raised during the experimental phase on land in the community of Santa Rosa, less than 60 meters from the El Fraile mine tailings (Fig. 1). A fourth goat (CX-04), that represents the control one, was taken to a community (Santiago Temixco) 7 km to the southwest of Santa Rosa, which is free of mine waste pollution. During the adaptation period, the goats were attended with food and water free of toxic elements. Subsequently, the goats began to be exposed to TE by being fed with maize cultivated (0.45 kg per day) next to the El Fraile mine tailings and consumed water from leachates of mine tailings and from the Cacalotenango River, following the routine of locals. The control goat in both periods of the experimental phase consumed food and water free of mine tailings pollution.

3.2 Sample collection

3.2.1 Water and grass

The water samples were collected in polyethylene bottles prewashed with nitric acid (50%) during the dry season. Three water samples were taken from different points of the Cacalotenango River, as well as two water samples from the ravine located in the lower part of the El Fraile mine tailings, where leachates are discharged (Fig. 1). Five grass samples were taken from the area where the goats grazed within 30 meters of the El Fraile tailings. The grass samples (Cynodon dactylon) were collected in disposable polyethylene bags, washed with MQ water in the laboratory to remove any residue, and stored in brown paper bags; then, the grass samples were dried in an oven at 80°C. Subsequently, the Cynodon dactylon samples were crushed and sieved to a diameter of 5 mm and stored in bags until acid digestion.

3.2.2 Blood, urine, and feces

Blood samples were taken from each goat through jugular vein puncture in 6 mL Vacutainer tubes with anticoagulant. They were then taken to the laboratory and stored at -20°C. The urine and feces samples were taken from spontaneous excretions and collected in sterile 120 mL polyethylene containers. Approximately 30 mL of urine and 15 g of feces samples were collected from each goat, labeled, and stored at -20°C.

3.2.3 Sacrifice of the goats

The sacrifice of the goats was carried out following the methodology of the Official Mexican Standard NOM-033-SAG/ZOO-2014 to sacrifice domestic and wild animals. The procedures carried out in this research were authorized by the Bioethics Committee of the Autonomous University of Guerrero. The sacrifice was carried out by a qualified and trained person (veterinarian) in the matter, in compliance with the appropriate protocol.

3.2.4 Soft tissues

The soft tissue samples (muscle, brain, rumen, lung, liver, and kidney) were taken after the sacrifice of the goats; the samples were stored in polyethylene bags and placed in a cooler for conservation. Subsequently, the samples were taken to the laboratory and stored in a freezer at -20°C.

3.2.5 Bezoar and hair

Samples of bezoars (hairballs formed in goat rumen because of grooming to themselves) were found in the rumen at the time of necropsy. It should be noted that of the three goats exposed to toxic elements, only goats CX-01 and CX-03 presented bezoars. These samples were stored in polyethylene bags in a cooler for their conservation and taken to the laboratory for storage at -20°C. During the experiment, each month, a lock of hair was cut from the back of each goat, stored in a labeled sterile 120 mL polyethylene jar, and kept at -20°C.

3.3 Sample preparation

3.3.1 Blood, urine, feces, bezoars, hair, and grass

Blood, urine, feces, bezoars, hair, and grass samples were digested by the wet method for the measurements of TE (Licata et al., 2004). From each goat, 5 mL of blood, 10 mL of urine, 1 g of feces, 0.30 g of bezoars, 0.3 g of hair, and 0.5 g of grass were individually placed in ultra-clean Savillex vials, which were previously pre-washed with 2% nitric acid (HNO₃) and MQ water. The samples were predigested with 10 mL of 8M HNO₃ on a hot plate at 135°C until dryness. Subsequently, 5 mL of hydrogen peroxide (H₂O₂) was added, and the temperature was kept at 135°C for one hour until the sample dried and showed a light color.

3.3.2 Soft tissues

For total and wet digestion of the soft tissue samples (muscle, brain, rumen, lung, liver, and kidney), 0.5 g of sample were weighted in ultra-clean Savillex pumps. Subsequently, the samples were digested with 5 mL of 8M HNO₃ on a hot plate at 130°C. Later, 5 mL of peroxide was added and kept on the hot plate for one hour until evaporation. The addition of HNO₃ and peroxide was repeated to eliminate organic matter.

3.4 Elemental concentrations

Elemental concentrations of water, grass, blood, feces, hair, and soft tissue samples were measured at the Laboratory of Geochemistry (LG) of the Autonomous University of Guerrero, while blood, urine, and bezoar samples were analyzed at the Emerging Pollutants Laboratory (ALEC) of the University of Arizona. The concentrations of Pb, Cd, and As were determined in a Perkin Elmer Optima 3200 (LG) and Mass Spectrometry (ICP-MS) Emission Plasma Emission Spectrometer (ICP-MS). The accuracy and precision of the analytical methods were monitored using the reference standard Lyphochek Whole Blood Metals Control, Level 3, #529, for the quantification of Pb, Cd, and As in blood, urine, bezoars, and soft tissues. For the quantification of the concentration of Pb, Cd, and As, the equipment was calibrated with routine standards (CWW-TM-D; CWW-TM-H; CWW-TM-A; CWW-TM-E), Inorganic Ventures (Christiansburg, VA), and High-Purity Standards (North Charleston, SC). The detection limit of the equipment was 0.010 mg L^− 1.

3.5 Lead isotope measurements

For the determination of the Pb isotope ratios, 5 mL of blood, urine, bezoars, and water samples were used. Sample preparation for Pb isotope ratios was carried out by chromatographic methods following the procedure described by Thibodeau et al. (2013). The isotope ratios of Pb were determined in 35 and 10 ppb solutions, and the isotopic fractionation was monitored by the analysis of the NBS-981 certified standard ²⁰⁶Pb/²⁰⁴Pb=16.9405; ²⁰⁷Pb/²⁰⁴Pb=15.4963 and ²⁰⁸Pb/²⁰⁴Pb = 36.7219 (Galer and Abouchami, 1998). The error was calculated from the reproducibility of the NBS-981 standard throughout each measurement; the external errors (2 σ) were 0.0034–0.0140% (²⁰⁶Pb/²⁰⁴Pb), 0.0036–0.0136% (²⁰⁷Pb/²⁰⁴Pb), and 0.0099–0.0333% (²⁰⁸Pb/²⁰⁴Pb).

4.1 Accumulation of TE

Table 1A shows the data of the response variables of goats exposed to Pb, Cd, and As, as well as the control goat. The goats showed a constant increase in weight and growth throughout the experiment. Regarding the three goats exposed to TE, goat CX-01 was always the heaviest and largest; followed by goat CX-02 and goat CX-03, which always showed smaller dimensions. Control goat CX-04 always had the largest dimensions of all goats.

4.1.1 Water, Cynodon dactylon, Zea mays, and Vachellia farnesiana

Table 2A shows the concentration of Pb, Cd, and As in water samples from the mine tailings of the El Fraile and the Cacalotenango River, in addition to samples of maize (Zea mays), grass (Cynodon dactylon), and huizache (Vachellia farnesiana) plants, which were used to feed goats. The water river sample showed concentrations of Pb, Cd, and As of < 5, 9, and 10 µg L^− 1, respectively, whereas the leachates (from mine tailings) sample presented concentrations of Pb, Cd, and As of 2.6, 2.3, and 0.1 µg L^− 1, respectively (Arroyo-Diaz, 2019). These concentrations suggest that most of these data (river water and leachate samples) were below the Mexican reference values of water for human use and consumption (NOM-127, 1994), and wastewater discharges (NOM-001 SEMARNAT, 2021), as well as the recommended values for water consumption according to the European Union (European Council of the European Union, 1998) (Table 2A).

The Zea mays samples showed concentrations of Pb, Cd, and As of 1.24, 5.12, and 4.31 mg kg^− 1, respectively (Díaz-Villaseñor, 2006; Table 2A); whereas lower concentrations were found in grass samples (Pb = 0.16 mg kg^− 1, Cd = 0.096 mg kg^− 1, and As = 0.096 mg kg^− 1; this study) and Vachellia farnesiana plants (Pb = 0.144 mg kg^− 1, Cd = 0.087 mg kg^− 1, and As = 0.072 mg kg^− 1; Cervantes-Ramírez et al., 2018). According to the maximum recommended daily dose limits for Pb, Cd, and As for humans and/or animals, the intake should not exceed 10, 5, and 15 µg day^− 1, respectively (Pandey and Madhuri, 2014). The exposed goats (CX-01, CX-02, CX-03) exceeded these limits, as they consumed around 153, 118, and 126 µg of Pb, Cd, and As, respectively, each day through the consumption of grass, maize, sweet acacia, and water.

4.1.2 Edible tissues

Table 1 shows the concentration of Pb, Cd, and As in edible tissue samples from the muscle, brain, rumen, lung, liver, and kidney of the goats studied. In general, the lowest concentrations were found in the muscle, brain, and lung tissues, while higher concentrations were found in the rumen, liver, and kidney tissues (Fig. 3).

Table 1

Concentration of TE of edible and visors tissues (mg kg-1) of exposed goats (CX-01, CX-02, and CX-03) and control goat (CX-04)
Goat	Element	Muscle	Brain	Rumen	Lung	Liver	Kidney
	Pb	ND	ND	0.513	ND	0.204	0.245
CX-01	Cd	0.006	0.006	0.022	0.017	0.029	0.049
	As	ND	0.012	0.022	0.017	0.029	0.049
	Pb	ND	ND	ND	ND	ND	ND
CX-02	Cd	0.042	0.019	0.023	0.019	0.030	0.111
	As	0.042	0.019	0.023	0.019	0.030	0.111
	Pb	ND	ND	ND	ND	0.056	0.130
CX-03	Cd	0.024	0.020	0.011	0.022	0.034	0.060
	As	0.024	0.020	0.021	0.022	0.034	0.060
	Pb	ND	ND	ND	ND	ND	ND
CX-04	Cd	0.019	0.021	ND	0.020	0.050	0.095
	As	0.019	0.021	ND	0.020	0.050	0.095

Particularly, the samples of muscle, brain, and lung tissues showed Pb concentrations below the detection limit (< 0.025 mg kg^− 1), while Cd and As were slightly higher between 6 and 42 mg kg^− 1, respectively (Fig. 3). Instead, rumen tissue of the goat CX-01 yielded a Pb concentration of 0.513 mg kg^− 1, clearly higher than the rest of the goats, whose concentrations were below the detection limit (< 0.025 mg kg^− 1), whereas Cd and As in rumen tissue yielded concentrations ranging from 0.011 to 0.023 mg kg^− 1 (Table 1). Liver and kidney tissue showed slightly higher concentrations, where Pb was in both type of tissues in a range between 0.056 and 0.245 mg kg^− 1, while Cd and As in the liver were within the range of 0.029 and 0.034 mg kg^− 1, and in the kidney within 0.049 to 0.111 mg kg^− 1 (Fig. 3).

Lead concentrations in the edible tissues of muscles, brain, and lungs are well below any permissible limit, while in liver and kidney samples showed higher, but still below the permissible values of the Mexican Official Standard, FAO (1989), USEPA (2002); and Chinese Food Health Criterion (GB 2762 − 2017; Table 2A), and barely similar to those of the Codex Alimentarius (CXS-193-1995) in a range of 50–100 µg kg^− 1 (Fig. 3a). The maximum permissible intake of Pb in food is between 75–150 µg d^− 1 for a human adult and 100 to 50 µg d^− 1 for children, with an absorption that varying from adult to child from 10 to 50% (Fergusson, 1990). Thus, the intake of 200 g of goat meat with a concentration of 100 µg L^− 1 would represent an intake of just 20 µg and an absorption of 2 µg for an adult and 5–10 µg for children, indicating a minimum danger for human health. After TE ingestion in humans, lead is distributed to different organs, mainly bones, kidneys, and liver, having the ability to cross the blood-brain and placental barriers, increasing bioaccumulation in the brain and in the fetus of exposed living beings (Okereafor et al., 2020). Animal meat for human consumption is considered safe when blood lead levels are below background levels during three consecutive samplings at least three weeks apart (Sharpe and Livesey, 2006).

In goats, lead affects various physiological processes in the body leading to neurotoxicity, gastrointestinal damage, oxidative stress, kidney and liver dysfunction, inhibition of the enzyme system associated with hemoglobin and calcium synthesis and metabolism of vitamin D, endocrine disruption, and other cellular disturbances (Swarup and Dwivedi, 2002; Patra et al., 2011; Slivinska et al., 2020). Lead also affects the reproductive system (Verma et al., 2020), and most of the findings indicate a higher tolerance to lead in sheep and goats compared to cattle. However, goats, although they can tolerate chronic doses of up to 400 mg per kg of body weight, can also exhibit cumulative lethal toxicity with predominant signs of central nervous system, following prolonged exposure to lead (Swarup and Dwivedi, 2011). Lead mimics calcium and zinc at the cellular level, which is suggested to be one of the mechanisms of neuropathy. Typical values for lead in ruminants have ranged between 0.05 and 0.25 mg kg^− 1 in whole blood, and the upper limit for lead in the liver has been set at 1 mg kg^− 1. Poisoned animals have a blood lead concentration greater than 0.35 mg kg^− 1. Although animals with less severe clinical signs may recover, tissue lead concentrations may remain elevated for months or years, subsequently posing a potential problem with lead residues in the food chain (Bates and Payne, 2017).

Cadmium concentrations in muscle, brain, and lung tissues did not show differences with Cd concentrations in rumen, liver, and kidney samples (Fig. 3b). All the edible tissues presented Cd concentrations far below the Mexican guideline for control of toxic residues in meat, fat, liver, and kidney of goats (NOM-004-ZOO,1994; <10,000–2,000 µg kg^− 1). Except for kidney tissue, muscle, brain, lung, rumen and liver tissues presented Cd concentration below to the Codex Alimentarius (CXS-193-1995; 500 µg kg^− 1), FAO (1989; 1000 µg kg^− 1) ; USEPA (2002; 1400 µg kg^− 1), Chinese Food Health Criterion (GB 2762 − 2017; 100–1000 µg kg^− 1) (Table 2A), but within a permissible range for foods which is 10 to 40 µg kg^− 1. Fergusson (1990) defined that the permissible intake of Cd through food for an adult is between 15 and 60 µg d^− 1, with an absorption of 6%. Therefore, an intake of 200 g of any of these edible tissues with an average concentration of 50 µg kg^− 1 would represent an intake of 10 µg, which is close to the minimum daily intake value for this metal.

Cadmium is an extremely toxic metal with a destructive impact on most organ systems (Bernhoft, 2013). After absorption in humans, cadmium accumulates rapidly in the kidneys and liver (Patra et al., 2007). Cadmium readily binds to metallothionein, a cysteine-rich protein that binds to metals, and induces their production. This causes cadmium retention in tissues, as well as a longer (> 10 years in humans) residence time (Hooser, 2018). Cadmium also inhibits the production of essential enzymes for the Kreb cycle, affects normal cell proliferation and differentiation, and increases apoptosis. The induction of oxidative stress by reactive oxygen species (ROS) is the main route of cadmium toxicity (Rebelo and Caldas, 2016; Njoga et al., 2021). These effects cause DNA damage and interfere with DNA repair mechanisms. Accidental ingestion of large amounts of cadmium causes acute nephrotoxicity and liver damage in goats. In addition to the more obvious symptoms of toxicity, cadmium exposure is associated with subtle subclinical effects such as oxidative stress, immunotoxicity, endocrine disruption, poor reproductive performance, and poor weight gain (Swarup and Dwivedi, 2002). Long-term exposure to cadmium increases lipid peroxidation and causes inhibition of superoxide dismutase activity, leading to oxidative stress in the liver, kidneys, and testicles (Patra et al., 1999). Animals deficient in calcium, iron, and zinc are more prone to cadmium toxicity (Alonso et al., 2004).

Arsenic concentrations in edible tissue samples of muscle, brain, lung, rumen, liver, and kidney are well below the values established in Mexican guideline for for control of toxic residues in meat, fat, liver and kidney of goats (NOM-004-ZOO-1994 (500-2,000 µg kg^− 1), FAO, 1989; USEPA, 2002; and Chinese Food Health Criterion (GB 2762 − 2017), and barely below to those of the Codex Alimentarius (CXS-193-1995; 100 µg kg^− 1) (Fig. 3b). The arsenic intake through food for an adult should not exceed the range of 10–40 µg kg^− 1 by day for adults and 1–5 µg kg^− 1 by day for children (Fergusson, 1990). Since the absorption of arsenic in humans varies from 25 to 100% depending on the nature of the arsenic species, an intake of 200 g of edible tissues from these goats would represent an intake of 6 to 10 µg, which is very close to the value minimum allowed and occur since a single source (Fergusson, 1990; Liu ZP, 2003).

Arsenic, after absorption in animals, preferentially accumulates in the liver and is slowly distributed to other tissues. The spleen, kidneys, and lungs can also accumulate high concentrations of arsenic (Rebelo and Caldas, 2016; Ortega-Morales et al., 2020). Organs with tissues rich in oxidative enzymes are strongly affected. Thus, the liver is the best organ to diagnose acute poisoning, while the kidney can contain moderate concentrations and help diagnose chronic poisoning (Radostits et al., 2007). Therefore, As in the urine is maintained for several days after exposure (Swarup and Dwivedi, 2011). Despite goats being exposed to toxic elements, Pb, Cd, and As concentrations found in blood and edible tissues were very low, suggesting that the meat of goats raised in this region under these conditions does not represent a major risk for the people’s health who get used to consume as food.

4.2 Bioindicators of TE exposure

Tables 2 and 3 show the concentration of Pb, Cd, and As in samples of blood, urine, feces, hair, and bezoar from the studied goats. Blood samples showed low concentrations of Pb (5.8–13.2 µg L^− 1), Cd (0.1–0.35 µg L^− 1), and As (< DL) (Figs. 3 and 4). The TE concentrations determined in the blood of exposed goats were lower than the minimum permissible values to produce chronic poisoning (Pb = 100 µg L^− 1, Cd = 5 µg L^− 1, As = 10 µg L^− 1) (ATSDR, 2007; Jubril et al., 2020). Nevertheless, the fact that Pb was detected in blood samples confirms the TE exposure of goats and that traces of the TE were circulating in the bloodstream, triggering potential adverse effects in organs and the nervous system (Cretacci and Parsons, 2010).

Table 2

Pb, Cd and As concentration of blood samples of of exposed goats (CX-01, CX-02, and CX-03) and control goat (CX-04).
Goat	Blood Sampling months	Pb (µg/dL)	Cd (mg/L)	As (mg/L)
	May-2017	ND	0.010	0.010
	Jun-2017	ND	ND	ND
	Augost-2017	2.8	ND	ND
CX-01	September-2017	ND	ND	ND
	January-2018*	1.32	0.00032	ND
	February-2018	ND	ND	ND
	May-2017	2.6	ND	ND
	Jun-2017	ND	ND	ND
	Augost-2017	ND	ND	ND
CX-02	September-2017	ND	ND	ND
	January-2018*	1.03	0.0002	ND
	February-2018	ND	ND	ND
	May-2017	ND	0.006	ND
	Jun-2017	ND	ND	ND
	Augost-2017	ND	ND	ND
CX-03	September-2017	ND	ND	ND
	January-2018*	1.22	0.00007	ND
	February-2018	ND	ND	ND
	May-2017	ND	0.005	ND
	Jun-2017	ND	ND	ND
	Augost-2017	ND	ND	ND
CX-04	September-2017	ND	ND	ND
	January-2018*	0.58	0.00035	ND
	February-2018	ND	ND	ND
* Sampling month used for the evaluation.
ND of Pb = 2.5 µg D^− 1
ND of Cd = 5 µg L^− 1
ND of Pb = 10 µg D^− 1

Table 3

Concentration of TE in urine, feces, hair and bezoar samples of exposed goats (CX-01, CX-02, and CX-03) and control goat (CX-04).
Goats	Pb (µg/L)	Cd (µg/L)	As (µg/L)
	urine	urine	urine
CX-1	70	1	836
CX-2	19	0.32	148
CX-3	47	0.3	89
CX-4	9	0.34	37
	Pb µg/kg	Cd µg/kg	As µg/kg
	feces	feces	feces
CX-1	33098.93	327.35	363.72
CX-2	1270.67	302.54	302.54
CX-3	1331.85	166.48	208.10
CX-4	61.80	61.80	123.61
	Pb (µg/kg)	Cd (µg/kg)	As (µg/kg)
	bezoar	bezoar	bezoar
CX-1	921	84	993
CX-2	NA	NA	NA
CX-3	17767	48	841
CX-4	NA	NA	NA
	Pb µg/kg	Cd µg/kg	As µg/kg
	unclean hair	unclean hair	unclean hair
CX-1	0.00	80.34	80.34
CX-2	1048.95	104.90	209.79
CX-3	2002.97	111.28	222.55
CX-4	<DL	65.33	65.33
	Pb µg/kg	Cd µg/kg	As µg/kg
	clean hair	clean hair	clean hair
CX-1	<DL	723.86	643.43
CX-2	182.48	60.83	60.83
CX-3	536.54	229.94	229.94
CX-4	<DL	41.99	83.99

Urine samples showed slightly higher concentrations of Pb (19–70 µg L^− 1) and Cd (0.3-1 µg L^− 1); however, As concentrations were much higher (89–836 µg L^− 1), at least three orders of magnitude greater than those in blood. The control goat had only 20%, 0.12%, and 10% of the average concentrations of Pb, Cd, and As in the urine of the three exposed goats, respectively, demonstrating its role as a control organism. The data obtained from urine samples confirm arsenic as an effective biomarker for tracing As exposure in goats (Bera et al., 2010). Similarly, feces of the three exposed goats showed the highest concentrations of Pb (1,270 − 33,100 µg kg^− 1), Cd (167–327 µg kg^− 1), and As (208–364 µg kg^− 1) across all studied matrices, whereas the concentrations of the control goat did not exceed 0.5%, 23% and 21% of the mean of Pb, Cd, and As of the exposed goats. The urine and feces concentrations suggest that these excretes are an efficient mechanism to eliminate large amounts of TE from their organism, avoiding their bioaccumulation in the edible tissues and chronic toxicity in goats.

Hair is one of the most used bioindicators because it is the least invasive, easiest to collect, and most suitable for recording TE bioaccumulation for several weeks (Fergusson, 1990). Bezoars found in two exposed goats (CX-1 and CX-3; Fig. S1) showed relatively high concentrations of Pb (921 − 17,767 µg kg^− 1), Cd (42–724 µg kg^− 1), and As (841–993 µg kg^− 1) (Figs. 3 and 5). The high concentration in bezoars is explained by the bioaccumulation in the hair, or by the presence of fine TE particles attached to the goats’ hair (Fragoso-Arbelo et al., 2002). Therefore, two different samples of goat loin hair were evaluated: i) unclean hair with particulate matter attached to their surface (Hair D), and ii) clean hair, rinsed with MQ water (Hair C). The concentrations of unclean hair (Pb: 1,049 − 2,003 µg/kg; Cd: 11–80 µg/kg; and As: 80–223 µg/kg) and clean hair (Pb: 182–536 µg/kg; Cd: 61–724 µg/kg; and As: 61–643 µg/kg), with the exception of Pb, were not significantly different (p > 0.05). Figure 6 shows SEM images of fine particulate matter impregnated in goats’ hair and X-diffraction of those particles, displaying the abundance of the most enriched elements (Cr, Ni, Fe, Si, Al, Sn, K, and Mg). The control goat hair showed the least particulate matter and the least TE concentrations (Pb: < DL µg/kg; Cd:42–65 µg/kg; and As:65–84 µg/kg).

4.3 Source of lead

The Pb isotope composition of blood, urine, and bezoar samples from exposed goats, river water, and leachates are shown in Table 4. The water from the Cacalotenango River and leachates from the El Fraile tailings exhibit an extremely homogenous composition of the ²⁰⁶Pb/²⁰⁴Pb, ²⁰⁷Pb/²⁰⁴Pb, and ²⁰⁸Pb/²⁰⁴Pb ratios, ranging from 18.741 to 18.750, 15.646 to 15.654, and 38.692 to 38.714, respectively (Fig. 7). The blood samples showed ²⁰⁶Pb/²⁰⁴Pb, ²⁰⁷Pb/²⁰⁴Pb, and ²⁰⁸Pb/²⁰⁴Pb isotope ratios ranging from 18.715 to 18.772, 15.460 to 15.666, and 38.562 to 38.708, respectively, whereas urine showed a more heterogeneous isotope composition yielding ²⁰⁶Pb/²⁰⁴Pb, ²⁰⁷Pb/²⁰⁴Pb, and ²⁰⁸Pb/²⁰⁴Pb ratios ranging from 18.737 to 18.301, 15.657 to 15.634, and 38.717 to 38.186, respectively. The bezoars showed a composition relatively similar to those of the blood samples with ²⁰⁶Pb/²⁰⁴Pb, ²⁰⁷Pb/²⁰⁴Pb, and ²⁰⁸Pb/²⁰⁴Pb ratios ranging from 18.722 to 18.720, 15.651 to 15.631, and 38.666 to 38.613, respectively.

Table 4

Pb isotopes data from blood, urine and bezoars of the goats, as well as the water from the area where the goats exposed to toxic elements (CX-01, CX-02 and CX-03) and the control goats (CX-04).
Goat	Type of sample	²⁰⁶Pb/²⁰⁴Pb	²⁰⁷Pb/²⁰⁴Pb	²⁰⁸Pb/²⁰⁴Pb
CX-01	Blood	18.73624	15.64760	38.66491
CX-02	Blood	18.71586	15.64017	38.61911
CX-03	Blood	18.75299	15.66693	38.70827
CX-04	Blood	18.77299	15.64774	38.56202
CX-01	Urine	18.73730	15.65746	38.71787
CX-02	Urine	18.52837	15.64411	38.43521
CX-03	Urine	18.70549	15.65482	38.67151
CX-04	Urine	18.30119	15.63460	38.18617
CX-01	Bezoar	18.72274	15.65104	38.66698
CX-03	Bezoar	18.72057	15.63136	38.61367
B1	Drinking water	18.75075	15.65405	38.71477
B2	Drinking water	18.75011	15.65218	38.71129
R1	Drinking water	18.74866	15.65107	38.70431
R2	Drinking water	18.74657	15.65081	38.70461
R2	Drinking water	18.74148	15.64660	38.69273

Based on Pb isotope data, Vázquez et al. (2017) demonstrated the influence of mine tailings as an important source of Pb and other TE that are dispersed through the environmental media. However, these authors found that humans are exposed to more Pb sources, including, for instance, indoor dust, paints, gasoline, cigarettes, and glazed pottery. Since goats were confined to a specific location with controlled feeding and water intake, the Pb isotope composition of blood, urine, and bezoar samples suggests that the main source of Pb in goats living in the vicinity of the El Fraile mine tailings is the residual mineralization in the mine tailings (Fig. 7). The geochemical and isotope data provided in this research demonstrate the negative health impact that mine tailings represent for most living beings in historical mining regions.

4.4 TE distribution in the environment

The El Fraile mine tailings have been present for over 70 years (Talavera-Mendoza et al., 2005); during this time, oxidation and erosion triggered the dispersion of TE to river water, soils (mainly used for agriculture purposes), and air (Talavera-Mendoza et al., 2016; Arroyo-Diaz et al., 2022). Since TE (e.g., Pb: 3,677 mg/kg; Cd: 39.5 mg/kg; As: 1,324 mg/kg; Talavera-Mendoza et al., 2005) have been released from mine tailings into the environment, they could be ingested by living beings such as plants, animals, and humans through different various pathways (e.g., inhalation, dermal, and oral ingestion). Because some families have been raising goats for more than 40 years, grazing them mainly around and on top of the mine tailings (Figs. 1 and 2), there is great concern about the exposure of goats to TE in small, chronic, and constant doses through ingestion of grass and bush shoots, as well as ingestion of river water impacted by mine tailings leachates, and/or inhalation of mine tailings particles.

Since Pb, Cd, and As are at the top of the list of most harmful TE (Okereafor et al., 2020; Munir et al., 2021; Njoga et al., 2021), the goats can suffer several health damages. Thus, goats exposed to Pb may yield high levels of Pb in blood, triggering a significant reduction in erythrocyte parameters and a significant increase in platelet count values and some leukocyte parameters (Jubril et al., 2020). Exposure to Cd may produce an increase in the generation of free radicals and alterations in antioxidant mechanisms and enzymatic processes (Jubril et al., 2020). Goats exposed to As have shown a 2.5% decrease in body weight and respiratory rate, as well as irregularities in the heart rate (Ortega-Morales et al., 2020). All these symptoms highlight the harmful effects of TE exposure in small ruminants.

Most of the experiments describing harmful effects in goats due to TE exposure were carried out using high doses in short periods (2–3 months) (Ortega-Morales et al., 2020) or with food with high TE concentrations (Bashir et al., 2020). In contrast, the present investigation used natural inputs, approaching the real conditions of the region (Table 2A) for a longer period (7 months). However, it was found that edible tissues (e.g., muscle, kidney, liver) of exposed goats showed similar concentrations of Pb, Cd, and As to goat tissues exposed to high doses. In real conditions, many goats in the study region are exposed to the interaction with mine tailings waste every day during longer periods (> 7 months), or even in a complete life cycle (10–13 years), potentially representing higher TE exposure and bioaccumulation. Furthermore, the families involved in goat farming have been grazing them on and around the El Fraile mine tailings for more than 40 years. This long-standing practice increases the probability of generating health damage, bioaccumulating TE, and transferring TE from maternal blood to the fetus via the placenta. Consequently, exposure continues throughout the lives of the newborns (Roels et al., 1978; Chen et al., 2014; Rebelo and Caldas, 2016).

While people living around the mine tailings neither eat grass nor drink water from the tailings leachates, they use nearby land to grow vegetables and maize. Additionally, during dry times, people use mine tailings leachates for irrigating plants and crops, feeding pets and livestock, but also, for personal hygiene, house cleaning, and washing cloths and dishes. Thus, inhabitants of this region are exposed to TE. Exposure to high Pb levels could cause health problems such as distortions in hemoglobin synthesis, abnormalities in erythropoiesis and disorders in central nervous system functions (Sindhu and Sutherling, 2015), attention-deficit/hyperactivity disorder, low intelligence quotient and dysfunctional behavior in children, young people and adults (Lee et al., 2018). In cases of chronic Pb exposure, adults may present hypertension, cardiovascular diseases, mental retardation, behavioral disorders, neuropsychological deficits, early cognitive impairment, and other neurological disorders. Exposure to As produces health risks and it is highly carcinogenic, especially during gastrointestinal or respiratory exposure (Hirano, 2020). Likewise, exposure to As, according to the International Agency for Research on Cancer, causes skin, lung, and bladder cancers (Hong et al., 2014). Whereas exposure to Cd causes dysfunctions of both taste and smell (Zheng et al., 2020). Excessive level of Cd in the body can cause hepatotoxicity, osteoporosis, teratogenicity, neurotoxicity, and immunosuppression due to induction of apoptosis in normal human mononuclear cells (De la Fuente et al., 2020; Al-Ghafari et al. 2019). Cadmium is involved in the pathogenesis and pathophysiology of type 2 diabetes mellitus (Hildebrand et al., 2019), by decreasing pancreatic insulin production and increasing insulin resistance (Njoga et al., 2021).

This research evaluated exposure to Pb, Cd and As in goats raised near the El Fraile mine tailings, by measuring the concentrations of Pb, Cd and As in blood, edible tissues, urine, feces and hair. Geochemical data indicate that goats likely consumed Pb, Cd, and As through ingestion (food and water), demonstrating that grass, maize, sweet acacia, water from the Cacalotenango River, and leachates from the mine tailings can act as transport agents of TE whose fate is living beings. The concentrations of Pb, Cd, and As in blood and soft tissues of the lung and brain of goats were very low, even well below the maximum permissible limits established by Mexican (NOM-004-ZOO-1994) and international regulation agencies (FAO, 1989; USEPA, 2002; GB 2762 − 2017; CXS-193-1995). These data indicate that the use of this livestock for human consumption does not represent an important health risk. However, the relatively high concentrations found in urine and feces demonstrate the great capability of goats to eliminate TE from their organisms, reducing exposure and poisoning, and decreasing the risk for human consumption. The high concentrations of Pb, Cd, and As determined in hair and bezoar samples also serve as evidence of impact of living beings by mine tailings. These data highlight the effectiveness of non-invasive samples (i.e., urine, feces, hair) as bioindicators of TE exposure. Moreover, the Pb isotope composition of blood, urine, and bezoar from goats was similar to the composition of the El Fraile mine tailings, indicating that the El Fraile mine tailings represent a hazard to the environment and health. The findings of this research demonstrate the existence of a significant risk to the health of living beings that interact with the mine tailings or their derivatives. In just seven months, the exposed goats managed to ingest, bioaccumulate, and eliminate TE from their systems. In real conditions, goats are exposed for longer periods, which makes them more likely to have higher rates of exposure and bioaccumulation of TE. Thus, the goats serve as an indirect indicator of the potential exposure to TE for people living near mine tailings, who may interact with the contaminated environment over longer periods due to their daily activities.

FUNDING

This research was conducted without any funding or financial support.

Author Contribution

MUER: sample preparation and investigationSASS: Conceptualization, investigation, resources, project administration, Validation, Visualization, Writing – originalRDS: Visualization, Writing – review and editingOTM: ConceptualizationMBBL: autopsy and dissection of goatsGNM: autopsy and dissection of goatsJLAN: Writing – review and editingGHF: Writing – review and editingAll authors commented on previous versions of the manuscriptAll authors read and approved the final version of the manuscript.

Acknowledgment

The authors are grateful to Mark Baker, manager of the Laboratory of Geochemistry of the Department of Geosciences, at the University of Arizona, for the support in acquiring Pb isotope measurements. We also thank to Jazmin Alaide López-Díaz and the Scanning Electron Microscopy and Microanalysis Laboratory (LMEByM) at the Universidad Autónoma de Guerrero (CONAHCYT, grants 231511 and 322409) for provide the imaging and geochemical data. We thank Daniel Ramos Pérez and the Environmental Sciences Laboratory (LCA) for acquiring geochemical data. This contribution was part of a Master of Science thesis by Martín Ubaldo Escorcia-Reynoso, who received support from the National Council of Humanities, Science and Technology, Mexico (CONAHCYT) through a postgraduate scholarship for his support during his studies.

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Assessing bioaccumulation of Pb, Cd, and As in Goats: Impacts of exposure to mine tailings in a polymetallic mining region

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Abstract

Figures

Highlights

1. INTRODUCTION

2. ENVIRONMENTAL FRAMEWORK

3. MATERIALS AND METHODS

3.1 Experimental phase

3.2 Sample collection

3.2.1 Water and grass

3.2.2 Blood, urine, and feces

3.2.3 Sacrifice of the goats

3.2.4 Soft tissues

3.2.5 Bezoar and hair

3.3 Sample preparation

3.3.1 Blood, urine, feces, bezoars, hair, and grass

3.3.2 Soft tissues

3.4 Elemental concentrations

3.5 Lead isotope measurements

4. RESULTS AND DISCUSSION

4.1 Accumulation of TE

4.1.1 Water, Cynodon dactylon, Zea mays, and Vachellia farnesiana

4.1.2 Edible tissues

4.2 Bioindicators of TE exposure

4.3 Source of lead

4.4 TE distribution in the environment

5. CONCLUSIONS

Declarations

FUNDING

Author Contribution

Acknowledgment

References

Additional Declarations

Supplementary Files

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