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1. Introduction

Many water treatment plants use conventional water treatment methods, but the persistence of metals, heavy metals, and metalloids in sediments poses ongoing challenges for water quality improvement. Urban rivers often face significant metal contamination, primarily due to industrial and domestic discharges [1], domestic sewage and inadequate treatment [2], urban stormwater [3], atmospheric deposition [4], and leaching from landfills and solid waste [5]. In addition, metals or metalloids can come from other sources including agricultural regions. Heavy metals commonly found in pesticides (insecticides, herbicides, and fungicides) include cadmium (Cd), lead (Pb), copper (Cu), and zinc (Zn), which also contaminate river sediments [6].

The analysis of metals (Al, Cd, Co, Cu, Cr, Pb, Hg) and metalloids (As) is crucial in monitoring the safety of aquatic ecosystems because these elements can have significant impacts on both the environment and human health [7,8,9,10]. Suspended sediments play a significant role in driving metals and metalloids along waterways [11,12]. Studies show that fishes exposed to contaminated environments have significant concentrations of Al, Cu, Zn, Pb, Cd, Fe, Ni, and Mn in organs such as gills and muscles [13,14,15]. In this scenario, humans can become contaminated with heavy metals by eating fishes or using contaminated water to irrigate crops [16]. Thus, the health risks posed by Al, Cd, Co, Cr, Cu, Mo, Ni, Pb, Hg, and As in fishes are significant due to their bioaccumulation and chronic toxicity mechanisms. These chemical elements can enter the human body through the consumption of contaminated fishes, leading to various health issues such as neurological impairment; cardiovascular, nervous, and bone diseases; and increased cancer risk [17,18]. Therefore, it is necessary to monitor metals and metalloids in water, sediments, and fishes, and assess possible effects on the ecosystem.

Despite the studies conducted in some countries highlighting the role of urbanization and its effect on river water and sediment quality [19,20], carrying out continuous monitoring of metal and metalloid levels in rivers to identify sources of pollution and implement corrective actions requires integrated efforts between governments, industries, and population [2,21,22]. Therefore, identifying and describing pollution sources in a quantitative and qualitative way has been challenging due to the impacts of human activities and their relationship with natural decomposition processes [23].

In Brazil, the state of Mato Grosso do Sul (MS) is characterized by a rich network of rivers that play a crucial role in the state’s ecology and economy. The region’s hydrographic basins, including significant rivers like the Dourados, Miranda, Aquidauana, Anhanduí, Pardo, and Lontra rivers, are vital for water management and environmental sustainability. Rivers are used for fishing both by riverside dwellers and sport fishermen. According to studies, the concentrations of Al, As, Cd, Cu, Fe, and Pb in the water samples of the Aquidauana River were in disagreement with the Brazilian legislation and presented risks to the aquatic biota [24]. In addition, the concentrations of metals (Cu, Zn, Mn, Fe, Cr, Al, and Co) in the Dourados River and land-use and land-cover assessment of the study area revealed extensive agriculture activity, particularly in areas surrounding the Dourados River headwaters [25]. Sampaio and Ribeiro (2003) [26] indicated that there are significant concentrations of Co, Cu, Fe, Cd, Zn, Pb, Ni, Ag, Cr, and Al in the sediments and water of the Aquidauana River; however, only Cu exceeded the limit values. Conversely, there are no data on the concentration of metals and metalloids in the sediments, waters, and tissues of some species of fishes that inhabit the Anhanduí River, the Pardo River, and the Lontra River. This information is important since the state of Mato Grosso do Sul has several leather industries, in addition to being one of the Brazilian states with the largest cattle herds and being a major producer of soy, rice, and cassava [27].

The illegal disposal of waste from tanneries, alongside cattle feces and agricultural runoff, significantly contaminates river waters, sediments, and aquatic life, posing serious health risks to humans. This multifaceted issue stems from the complex mixture of toxic chemicals released into waterways, which not only degrades water quality but also affects the entire ecosystem. Contaminants include pharmaceuticals, heavy metals, and emerging pollutants, each contributing to ecological and health risks. Thus, we were motivated by the manuscripts published by Alengebawy et al. (2021) [6], Sheikhzadeh and Hamidian (2021) [7], and Dan (2021) [8], which emphasize the need for the monitoring of metals in aquatic ecosystems, sediments along waterways [10,11,12], and studies on fishes exposed to environments contaminated by Al, Cu, Zn, Pb, Cd, Fe, Ni, and Mn [13,14,15]. Therefore, we aimed to (1) determine current concentrations of metals (Al, Cd, Co, Cr, Cu, Mo, Ni, Pb, Hg) and metalloid (As) in waters, sediments, and muscles of curimba Prochilodus lineatus and catfish Pimelodus maculatus fish species from the Anhanduí, Pardo, and Lontra rivers located in the state of Mato Grosso do Sul, Brazil, using inductively coupled plasma optical emission spectrometry (ICP OES); and (2) identify possible pollution sources using the geo-accumulation index (Igeo), contamination factor (CF), pollution load index (PLI), and enrichment factor (EF).

2. Materials and Methods

2.1. Study Area

The Anhanduí River arises from the confluence of the Prosa and Segredo streams, within the urban area of the city of Campo Grande (MS). It is 297 km long and flows into the Pardo River. On the other hand, the Pardo River has an extension of 457 km from the confluence of the Água Vermelha and Capim Branco river streams and reaches the Paraná River [28]. Finally, another river studied in our research is the Lontra River, which has an extension of approximately 115 km.

According to Figure 1 and Table 1, sample collections of soil, water, and fishes in the Anhanduí River were carried out in three locations, and only one collection location in the Pardo and Lontra rivers. Information on sampling sites in river area are described as follows:

-. Location 1 (Anhanduí River-1 (L1), coordinates 20°59′39.79″ S, 54°30′24.83″ W; border with the district of Anhanduí, distance from the city of Campo Grande: 60–60.3 km), located on the BR-163 highway, which has high vehicle traffic during peak hours, reaching around 4000 vehicles per hour during peak times. The BR-163 highway is 845.4 km long and crosses different Brazilian states [27]. Collections were carried out 250 m from the Anhanduí River bridge.

-. Location 2 (Anhanduí River-2 (L2), coordinates 21°24′07.34″ S, 54°07′50.59″ W; distance from the city of Campo Grande: 79–80.3 km), located to the right of the district of Anhanduí; soybean, corn, and livestock farming region, located on the MS-455 highway. Collections were carried out 150 m from the Anhanduí River bridge.

-. Location 3 (Anhanduí River-3 (L3), coordinates 21°07′15.91″ S, 54°20′14.87″ W; distance from the city of Campo Grande: 36–40.4 km), located to the left of the district of Anhanduí. Collections were carried out 250 m from the Anhanduí River bridge.

-. Location 4 (Pardo River (L4), coordinates 21°08′21.8″ S, 53°08′28.7″ W; distance from the city of Campo Grande: 168.06–169.53 km). Collections were carried out at just one point in the Pardo River, 550 m from the Pardo River bridge.

-. Location 5 (Lontra River (L5), coordinates 21°06′20.9″ S, 53°44′17.1″ W; distance from the city of Campo Grande: 104.68–116.60 km) (Figure 1). Collections were carried out at just one point in the Lontra River, 500 m from the Lontra River bridge.

Quality assessment of sediments, water, and fishes was conducted in the period from July 2020 to July 2021. Distances were measured using GPS resources—considering a straight-line distance between two points. The sample collections carried out in Anhanduí-1 were carried out close to the urban area, but the rest collected were carried out close to urban agriculture.

2.2. Water and Sediment Collection

A 1 L quantity of water samples was collected manually by directly submerging a sterile amber glass bottle to a depth of 20 cm at the sampling sites. Each sample bottle was labeled during collection, and after collection, water samples were filtered using a 0.45 μm membrane filter (MF-Millipore^® Membrane Filter, Merck, Darmstadt, Germany), acidified to 5 mL of acid 65% nitric acid (HNO₃, Merck, Darmstadt, Germany) for metal preservation, transported in refrigerators, and stored at 4 °C until analysis. We emphasize that the water sample represents a snapshot of water quality, and more frequent sampling is necessary to adequately characterize the range.

An amount of 350 g of sediment was collected using a PVC collection tube (50 mm in diameter and 2 m in length) according to the methodology of the Environmental Company of the state of São Paulo [29]. At each location, three surface sediment samples at depths of 0 to 10 cm were collected at a distance of 0.70 m–1 m from each other. A total of 15 sediment samples were collected from the 5 locations. In addition, for each collection of surface sediment samples, new tubes were used to avoid contamination.

The first collection of bottom sediment and water samples was carried out in July of 2020, and the second collection was carried out in July of 2021, both called the dry season in the region of the country. According to the National Institute of Meteorology (INMET), in July 2020, Campo Grande recorded only 4.6 millimeters (mm) of rain and reached temperatures of 29.2–32.2 °C. On the other hand, in July 2021, the city recorded 10 mm of rain and reached temperatures of 17–29 °C [30].

2.3. Obtaining Fish Samples

Fishes collected by fishermen and donated for this study were the curimba (Prochilodus lineatus), which has an iliophagous feeding habit, i.e., feed on bottom sediments, and the catfish (Pimelodus maculatus) with an omnivorous feeding habit (Table 1). Both species are commonly consumed by humans. The capture method of fish used in this study is categorized as passive capture techniques (capture fish with a baited hook and line). Fishermen were instructed to use a new pair of latex gloves after each collection and the correct storage of samples. All fish samples after collection were immediately placed in individual plastic bags and placed in a cooler of crushed ice. Then, the fish samples were taken to the laboratory, where they were washed with ultra-pure water. Muscle tissues of the fish (dorsal muscle) were pooled and analyzed in triplicate. Muscle samples were ground using an IKA M20 Mill (Biovera, Brazil), developed for dry grinding of soft and hard substances.

2.4. Acid Digestion of Sediment, Water, and Fish Tissues

After collection, the sediment samples were dried at room temperature until they reached a constant weight, and then sieved through a polyethylene sieve (Verder Scientific, São Bernardo do Campo, Brazil) to remove very large particles and obtain a homogeneous sample. After sieving, the sediment samples were ground and sieved through a 2 mm sieve. Approximately 0.5 g of dry sediment samples were weighed directly into Teflon DAP60^® containers (The Chemours Company FC, Wilmington, DE, USA). Then, 9 mL of hydrochloric acid (HCl) (35%, Merck, Darmstadt, Germany) and 3 mL of hydrogen peroxide (H₂O₂) (30%, Merck, Darmstadt, Germany) were added for acid digestion. The entire sample was left to rest for pre-digestion for 20 h. The experimental procedure was performed in triplicate.

An amount of 5 mL of water samples filtered through a filter membrane was placed in Teflon DAP60^® containers. Then, 0.5 mL of HNO₃ (65%, Merck, Darmstadt, Germany) and 0.100 mL of 37% HCl were added. The water samples were digested using a microwave digestion system (Speedwave four, Berghof, Eningen, BW, Germany) that was programmed to reach and maintain a temperature equal to 180 °C for 15 min, before going through a linear heating ramp of 10 min, totaling 25 min of digestion.

Fish samples (300 mg of dorsal muscle) were weighed and added 8 mL of HNO₃ (65%, Merck, Darmstadt, Germany), 1.0 mL of ultra-pure water (18 MΩ cm, Milli-Q, Millipore, Bedford, MA, USA), and 1.5 mL of H₂O₂ (30%, Merck, Darmstadt, Germany). The samples were transferred to a Teflon DAP60 digestion tube and digested using the microwave system (Speedwave four, Berghof, Eningen, BW, Germany).

2.5. Elemental Measurement by ICP OES

Quantification of the elemental content in sediment, water, and tissue (muscle) samples after digesting was carried out using inductively coupled plasma optical emission spectrometry (ICP-OES, iCAP 6300 Duo, Thermo Fisher Scientific, Bremen, Germany). The operating conditions of the ICP OES used to determine the elemental content are the following: RF power 1250 W, sample flow 0.35 L∙min⁻¹, plasma flow rate 12 L∙min⁻¹, integration time 5 s, stabilization time 20 s, nebulization pressure 30 psi, plasma view axial. The wavelengths used for the quantification of Al, As, Cd, Co, Cr, Cu, Ni, Pb, Mo, and Hg were 309.271,189.042, 228.802, 228.616, 267.716, 324.754, 221.647, 220.353, 202.030, and 253.652 nm, respectively.

The calibration standard solutions were prepared by diluting stoke multi-elemental standard solution (SpecSol, Quimlab, Jacareí, Brazil) containing 1000 mg/L of each element (Al, As, Cd, Co, Cr, Cu, Ni, Pb, Mo, and Hg). For quantification of the investigated elements in the sediment, water, and fishes, external calibration curves were built on five different concentrations in the range of 0.01–5.0 mg/L. Optimal conditions were evaluated in terms of accuracy (by recovery test) and limit of detection. The spiking solution was made from a single multi-element stock solution of 1000 ppm. Thus, a recovery test was performed, and the solutions were spiked with 1 ppm. The method had a recovery interval of 89–110%. The limits of detection (LOD) and limit of quantification (LOQ) were calculated according to Rosa (2021) and Rosa et al. (2022) [31,32]. Therefore, the range of all elements LOD was 0.00008–0.001 mg/L, and the range of all elements LOQ was 0.0003 to 0.004 mg/L. The range of the correlation coefficient (R²) was 0.9980–0.9999 (Table 2).

2.6. Calculation of Geo-Accumulation Index (Igeo)

The geo-accumulation index (Igeo) is used to assess the contamination of sediment samples [33], considering the 7 classifications of pollution levels. The calculation is shown in Equation (1):

(1) $I_{g e o} = l o g_{2} (\frac{C_{n}}{1.5 \times B_{n}})$

C_n is the concentration of each metal quantified by ICP OES in the sediment (mg/kg) and B_n is the reference value established for uncontaminated soils. In this study, we consider as reference values those established for soils in the state of Mato Grosso do Sul, Brazil (mg/kg): As (3.17), Cd (0.07), Co (11.68), Cu (28.49), Cr (30.30), Mo (0.13), Ni (8.61), and Pb (11.05) and 1.5 for the reference correction factor due to lithological effects [34]. There are no reference values for Al and Hg.

2.7. Calculationf of Contamination Factor (CF)

The contamination factor (CF) provides the estimation of contamination by considering the measured heavy metal concentrations from sediments and the background concentrations in the sediments. In the present research, the CF for the sediments was calculated using Equation (2) [35].

(2) $C F = \frac{C_{n}}{C_{s}}$

where C_n is the average concentration of metal(loid)s in the sediment and C_s is the background values (mg/kg) established for soils or sediments in the state of Mato Grosso do Sul [34]. The CF was classified as: CF < 1 denotes low contamination; 1 ≤ CF < 3 denotes moderate contamination; 3 ≤ CF < 6 denotes considerable contamination, and CF > 6 denotes very high contamination [36].

2.8. Calculation of Pollution Load Index (PLI)

The pollution load index (PLI) was obtained according to Tomlinson et al. (1980) [37]. In this case, PLI < 1 is considered no pollution load by toxic elements; PLI = 1 indicates that baseline levels of pollutants are present; and PLI > 1 indicates that it is polluted. The PLI was calculated using Equation (3) [37].

(3) $P L I = \sqrt[n]{{C F}_{1} \times {C F}_{2} \times {C F}_{3} \times \dots {C F}_{n}}$

where CF is the contamination factor (Equation (2)), and n is the number of metals.

2.9. Calculation of Enrichment Factor (EF)

To evaluate the degree of contamination by metal(loid)s, we used Equation (4), based on Mokhtarzadeh et al. (2020) [38], to estimate enrichment factors (EFs).

(4) $E F = {(\frac{C_{i}}{C_{r e f}})}_{S a m p l e s} / {(\frac{C_{i}}{C_{r e f}})}_{b a c k g r a o u n d}$

where C_i is the concentration of the target element and C_ref is the concentration of the reference element. Arsenic was chosen as the reference element due to the low coefficient of variation in samples [38]. Background metal concentrations for EF calculation were based on the National Council for the Environment (Conama) [39], where EF < 1 indicates no enrichment, EF < 3 indicates minor enrichment, EF = 3–5 indicates moderate enrichment, EF = 5–10 indicates moderately severe enrichment, EF = 10–25 indicates severe enrichment, EF = 25–50 indicates a very serious enrichment, and EF > 50 indicates an extremely serious enrichment.

2.10. Calculation of Human Health Risk Assessment

From the quantification of metal(loid)s, it is possible to estimate carcinogenic and non-carcinogenic risks to human health. The assessment of exposure due to average daily intake (Average Daily Dose—ADD), i.e., ADD dose (mg/kg/day), was used to quantify the deleterious effects due to the oral exposure dose. The ADD due to food consumption can be calculated using the following equation (Equation (5)):

(5) $A D D = \frac{C \times I R \times E D \times E F}{B w \times A T}$

where C represents the content of metal(loid)s quantified by ICP-OES in units of mg/kg or mg/L, IR is the ingestion rate that corresponds to the amount of capsules or sap ingested daily, ED is the duration of exposure, Bw is the reference body mass, EF is equivalent to the exposure frequency (EF), and AT is the average time. The mean weight of Brazilian adults is 70.40 ± 15.20 kg aged ≥18 years [40]. However, for our calculations, we considered 70 kg and 50 years for adults, and mass of 26 kg aged 8 years for children [41]. To determine the intake dose, the amount of IR = 150 g/day of fish, consumed three times a week, for both children and adults, was considered.

The non-carcinogenic risk to human health due to the ingestion of fish contaminated by the presence of metal(loid)s was characterized using the hazard quotient [42]. The hazard quotient (HQ), which is a ratio between the average daily intake dose (ADD) and the reference dose (RfD), characterizes the health risk of non-carcinogenic adverse effects due to exposure to toxic elements, and is therefore determined by the following equation (Equation (6)):

(6) $H Q = \frac{A D D}{R f D}$

where RfD is the chronic oral reference dose. In this study, we considered the following chronic oral reference dose values: As 0.0003 mg/kg/day; Cd 0.0001 mg/kg/day; Co 0.0003 mg/kg/day; Cr 1.5 mg/kg/day; Cu 0.04 mg/kg/day; Mo 0.005 mg/kg/day; Ni 0.011 mg/kg/day; and Pb 0.0035 mg/kg/day [43]. For the elements Al and Hg, to date, there are no RfD values established by the United States Environmental Protection Agency (USEPA) [43]. Therefore, an index value < 1 is considered safe throughout life.

2.11. Statistical Analysis

Data were analyzed using Origin 9.0 software (OriginLab Corporation, Northampton, MA, USA). Concentrations were expressed as mean ± standard deviation. Investigation of normality tests as well as the Kruskal–Wallis test and principal components analysis (PCA) were used to interpret the data.

3. Results and Discussion

3.1. Metal(loid) Concentration in the River Waters

The values of metal(loid) concentrations in river water samples from different locations are shown in Table 3. According to the results of the Kruskal–Wallis test, there are significant differences between the median values of concentrations of elements in the respective locations (p = 1.5 × 10⁻⁷). However, to understand the association of water samples from the five different sampling sites, depending on metal(loid) content, principal component analysis was applied. According to PCA results, the first two principal components explain 95.68% of the total variance of the results, that is, with PC1 contributing 75.47%, and the factor loads of Cu, Cr, Ni, and Pb are all higher than 0.2 (Figure 2), and with PC2 contributing 20.21% (Figure 2), and the factor loads of Cu, Cr, Ni, and Pb are all higher than 0.15. Finally, according to Figure 2, the factor loads of As, Co, Cd, Hg, and Mo for PC1 and PC2 are less than 0.1. In addition, the PCA showed a spatial distribution pattern with a greater tendency for elements in Anhanduí River-1 and Anhanduí River-2 (Figure 2). There is a greater trend in the concentrations of metal(loid)s such as Cu (2020–2021), Ni (2021), Co (2020–2021), As (2020), Hg (2020), and Al (2020–2021) in Anhanduí River-1. On the other hand, a greater trend was found for elements such as Cr (2021–2021) and Pb (2020–2021) in Anhanduí River-2. According to PCA, the concentrations values of As, Co, Cd, Cr, Cu, Hg, Mo, Ni, and Pb in water contributed to a lesser extent to Anhanduí River-3, Pardo River, and Lontra River.

The Al concentrations (Table 3) are below the value established by Conama for freshwater (0.1 mg/kg). The concentrations of As, Cd, Cr, and Hg in the waters of the Anhanduí River (sites 1, 2, and 3) are above these permitted limit values for heavy metal ions in drinking water established by the World Health Organization (WHO) (As 0.05 mg/kg; Cd 0.003 mg/kg; Cr 0.05 mg/kg; and Hg 0.001 mg/kg) [44]. In addition, the concentrations of Cu in the waters of the Anhanduí River-2 are above those established by the WHO (2 mg/kg). The Ni concentrations in rivers are above those established by the WHO for Ni (0.07 mg/kg). The concentrations of Pb in Table 3 are above those values established by the WHO for Pb (0.05 mg/kg) [44].

Taking into account that the level of Cd, Co, Cr, Hg, Cu, Ni, and Pb in the river water samples obtained (Table 3) significantly exceeded the WHO criterion concentration limits, this indicates that the water from these rivers may not be safe for drinking and/or cooking by riverside residents or for use in crop irrigation [1]. In fact, the ingestion of heavy metals such as Cd, Co, Cr, Hg, Cu, Ni, and Pb in water poses significant potential health risks, with no safe levels established for many of these elements. Heavy metals are toxic even at low concentrations, leading to severe health issues, including cancer and neurological disorders [4,9]. Studies indicate that average concentrations of these metals often exceed permissible limits set by organizations like the WHO [10].

The Anhanduí River rises from the urban area of the city of Campo Grande (MS), being exposed to vehicle traffic and illegal discharge of contaminated substances from residences or gas stations. In addition, this river crosses large cattle ranches and agricultural activities. All these factors can significantly contribute to increasing the concentration of elements such as Al, As, Ni, Pb, Hg, Co, Cu, Cr, and Cd in the water [1,2,4]. In fact, vehicles release oil, fuel residues, brake fluid, and wear-and-tear particles from tire fragments and brake pads, which contain heavy metals such as Pb, Cu, Cr, Al, and Cd. During rainstorms, these contaminants are washed off roads and highways into storm drains, which often discharge directly into rivers without treatment. In addition, the use of agricultural pesticides is associated with the presence of heavy metals such as cadmium (Cd), lead (Pb), copper (Cu), and zinc (Zn), which also contaminate rivers [4,6], mainly at location 2 (Anhanduí River-2). Thus, our results presented in Table 3 corroborate those obtained by Mohammad et al. (2022) [1], in which the presence of elements such as As, Cr, Cd, and Pb in urban rivers is due to industrialization and the influence of agricultural activity [4]. However, the non-industrialized areas are also contaminated, suggesting the dispersal of heavy metals along the rivers. Therefore, the contamination of Pardo and Lontra rivers by Al, As, Ni, Pb, Hg, Co, Cu, Cr, and Cd throughout the years is a significant concern in both urban and rural areas, despite the distance from the urban center of the city of Campo Grande. In fact, various anthropogenic and natural factors contribute to this issue, affecting water quality and the ecosystem health of these rivers.

The concentration of metal(loid)s in rivers is significantly influenced by seasonal variations, particularly between dry and rainy seasons. However, although our study was carried out during the dry season in July 2020 and July 2021, there was a small variation in the metal concentration values in the waters of these rivers. In addition, there is a possibility that the concentration of certain heavy metals may be higher during the dry season, while others are higher in the rainy season [45,46]. Recent studies have shown that higher water volume can dilute some heavy metal concentrations, leading to variable results depending on the location and intensity of rainfall [47], while lower water flow reduces dilution capacity, potentially increasing the concentration of heavy metals in the water [48].

3.2. Metal(loid) Concentration in the Sediments

Concentrations of metal(loid)s quantified in sediments are shown in Table 4 and are compared with maximum limits established by the Brazilian regulation [39]. The concentration of metal(loid)s in sediments (non-parametric Kruskal–Wallis test) differed among locations (Anhanduí River-2 and Anhanduí River-3) for Cu (p = 7.7 × 10⁻⁵). According to PCA, there is a greater trend in metal concentrations in locations Anhanduí River-1, Anhanduí River-2, and Anhanduí River-3 (Figure 3). In this case, the highest element concentration trend is observed in Anhanduí River-2.

Only the concentration of As in the sediments of the Pardo River in 2020 is below the value established by Conama [39] (Table 4). Moreover, with the exception of Lontra River in 2021, the concentrations of Ni and Hg in river sediments were above the values established by Conama. Only the Pardo River, in 2020 and 2021, and the Lontra River, in 2020 and 2021, presented Pb concentrations below the values established by Conama. The Pardo River in 2020 and the Lontra River in the period 2020–2021 both presented Cu concentrations below those established by Conama. Similarly, Cr concentrations in the sediments of rivers were lower than those values established by Conama. In contrast, Mo concentrations in the period studied were above those of Conama.

The values of Al concentrations (Table 4) were below those found in sediments (125.47 mg/kg) from the Strzegomka River in southwestern Poland [49], which has highest aluminium concentrations that vary across different rivers in that country. In addition, Mo concentrations were below river sediments near the molybdenite mining region (13.2 mg/kg) in China [50], which has critical pollution levels. Cobalt concentration in Anhanduí River-2 was higher than the Chinese sediment value (17.38 mg/kg) [51]. On the other hand, the mean concentration of Cr, Ni, Cu, Cd, and Pb in river sediments (Table 4) was higher in relation to values of study by Poland for Cr 165.1 mg/kg, Ni 8.21 mg/kg, Cu 10.92 mg/kg, Cd 0.168, and Pb 18.0 mg/kg in river sediments [52].

The dry and rainy seasons also influence the concentration and distribution of heavy metals in river sediments. Heavy metal concentrations often peak due to reduced water flow and increased sedimentation, which can lead to higher levels of metals like Pb and Cr. According to studies, the concentrations of metals such as Cu were lower in the dry season compared to the rainy season [53,54]. However, the concentration values of elements such as Al, As, Ni, Pb, Hg, Co, Cu, Cr, Cd, and Mo in sediment samples collected from rivers during a seasonal dry period vary between the year 2020 and 2021 (Table 4). Future studies should consider the rainy season to understand the influence of rainfall and other factors on these rivers. These variations are driven by processes like erosion, sediment deposition, resuspension, and organic matter changes, which differ between seasons.

3.3. Geo-Accumulation Index

According to the Igeo classification, the sediments in the rivers were classified as not polluted to moderately polluted by As and Ni (Figure 4). However, the sediments were strongly to extremely polluted by Cd and Mo, moderately polluted by Pb, and practically not polluted by Co, Cr, and Cu. The Igeo values obtained from the sediment, mainly related to Cd, may indicate the anthropogenic influence on the quality of the rivers [55]. However, according to Chiba et al. (2011) [56], the presence of Al, Cd, Pb, Zn, Cr, Co, Cu, Fe, Mn, and Ni in sediment samples comes from different sources.

3.4. Contamination Factor (CF) and Pollution Load Index (PLI)

According to the CF calculations, the sediments of some rivers are moderately contaminated with As, Cu, Co, Ni, and considerably contaminated by Pb (Table 5). On the other hand, the CF calculations show that the sediments are very highly contaminated by Cd and Mo. In addition, only Cr in the sediments showed low contamination. Elements such as Cd and Mo showed very high contamination in the sediment of all rivers analyzed. With regard to the level of multi-element contamination of the sediment based on the calculation of the pollution load index (PLI), all sampled rivers showed a decline in site quality with PLI > 1 (Table 5).

3.5. Enrichment Factor (EF)

Cadmium enrichment at all rivers was considered severe, with the exception of the first collection (2020) at site Anhanduí River-2, where EF ranged from 11.11 to 18.79 (Table 6). Compared with the values of all metal(loid)s, the EF values indicated that Cd was the element that most contributed to the enrichment of the rivers. In fact, our results corroborate with those obtained by Wang et al. (2022) [57] when evaluating the EF in surface sediments in the intertidal zones of the Yellow River estuary in China, in which they considered two seasons of the year (summer and autumn); however, their EF values are lower than those found in our study.

Molybdenum was classified to have severe enrichment in locations Anhanduí River-2 and Lontra River in 2020 and in all locations in the second collection (2021). Enrichment ranged from 5 to 10 at sites Anhanduí River-1, Anhanduí River-3, and Pardo River (first collection 2020) and was considered moderately severe for Mo. Thus, EF analysis makes it possible to determine the possible origin of the metals present in river sediments [57]. The results of our study suggest that elements such as Cd and Mo quantified in the sediments of rivers in the state of Mato Grosso do Sul come from anthropogenic factors, as they present EF > 1.5. In contrast, As, Co, Cr, Cu, and Pb may come from natural weathering processes of rocks present at the bottom of rivers, as they have EF < 1.5.

3.6. Concentration of Metal(loid)s Quantified in Prochilodus lineatus and Pimelodus maculatus

For a better understanding of our results, metal(loid) concentration in Prochilodus lineatus muscle (Table 7) and Pimelodus maculatus muscle (Table 8) were compared to the maximum limit for human consumption established by Anvisa/Brazil and values of permissible limits of metals in fishes recommended by the FAO. In addition, the metal(loid) concentration values obtained in muscle samples from Prochilodus lineatus (Table 7) and Pimelodus maculatus (Table 8) were compared with those available in the literature. The concentration of Al was the highest in P. lineatus (Table 7) and P. maculatus (Table 8) in relation to the Cr, Cu, Cd, Hg, Ni, As, Pb, Mo, and Co analyzed in this study. Furthermore, in both fishes there was an increase in the concentration found in the second collection (2021), up to 3.5 mg/kg, with minimum values of 4.05 ± 0.86 and 3.88 ± 0.73 mg/kg in the first collection (2020) and maximum values of 12.763 ± 2.50 and 9.98 ± 1.0 mg/kg in the second collection (2021) of P. lineatus and P. maculatus, respectively. The levels of Pb in the P. lineatus muscle was greater than 0.3 mg/kg in the first collection (2020) in Anhanduí River-2 and Pardo River and in the second collection (2021) in Anhanduí River-1 and Pardo River. The concentration of this element in P. maculatus was also higher than 0.3 mg/kg in Anhanduí River-1, Anhanduí River-2, and Anhanduí River-3 in both collections (2020–2021).

Our study corroborates with Meche et al. (2010) [58], who obtained high levels of Al when analyzing 16 fish species in the Piracicaba River, state of São Paulo (SP), Brazil. The average concentrations among all samples ranged from 8.38 to 24.9 mg/kg found in Geophagus brasiliensis. According to the authors [58], the soil in the region is rich in Al and this element can be released from the soil by acid rain. Furthermore, the high concentration of Al can be attributed to the burning of sugar cane, which is common in that region. There is no limit established by Anvisa/Brazil and the FAO for Al in fishes. However, Al concentration in fish muscles varies significantly across species and environmental conditions. Studies indicate that aluminium bioaccumulation occurs in fish tissues, with muscle concentrations generally lower than in organs like gills and liver. In commercially important fish from the Caspian Sea in Iran, Al concentrations in muscle of the Cyprinus carpio ranged from 0.89 to 4.63 μg/g, influenced by seasonal variation [13]. Therefore, with the exception of the Al concentration in Pardo River in 2020 and 2021 (Table 7 and Table 8) and Lontra River in 2020 (Table 8), the concentrations of Al are above those quantified in the Caspian Sea [13]. Histological changes in gill tissues, such as alterations in morphology and increased reactive oxygen species (ROS), have been observed using zebrafish as an experimental model [59].

The average levels of As found in P. lineatus and P. maculatus in the five collection sites were lower than that established by Anvisa/Brazil, which provides for the Mercosur Technical Regulation on Maximum Limits of Inorganic Contaminants in Food [60]. According to the results published by Sheikhzadeh et al. (2021) [7], As concentrations in the muscles of some fish species from the Persian Gulf are high when compared to other countries [7]. In fact, the mean concentration of As in the muscle tissue of Pomadasys spp. (1 mg/kg) from the northern region of the Persian Gulf [7] was higher than in P. lineatus (Table 7) and P. maculatus (Table 8) in the five collection sites. Studies on various fish species, including rohu carp and zebrafish, reveal that arsenic leads to deformities, behavioral changes, and biochemical disruptions [61,62].

On the other hand, the concentration of Cd with minimum values of 0.66 ± 0.074 (2021) to 0.59 ± 0.14 mg/kg (2020) and maximum values of 1.56 ± 0.31 (2021) to 2.24 ± 0.69 mg/kg (2021) in P. lineatus and P. maculatus was higher than the limit established by Anvisa/Brazil (0.05 mg/kg), respectively. Mean concentrations of Cd in the muscle tissue of P. lineatus (Table 7) and P. maculatus (Table 8) were higher than Otolithes ruber (0.33 mg/kg) and Scomberomorus guttatus (0.21 mg/kg) from Khark Island in the Persian Gulf and Otolithes ruber (0.23 mg/kg) from Bushehr Port in Iran [7]. The results in Table 7 and Table 8, when compared with other studies, reveal that the concentrations of metals such as Cd in samples of Prochilodus lineatus muscle (Table 7) and Pimelodus maculatus muscle (Table 8) are higher than those obtained in Iran for fish species Liza aurata (0.04 mg/kg) and Rutilus frisii kutum (0.17 mg/kg) [13]. The accumulation of Cd varies across fish species and tissues, leading to diverse toxic effects, including damage to the immune and reproductive systems [63]. That is, reproductive capabilities are compromised, as seen in rare minnows where Cd exposure resulted in reduced spawning success and altered gonadal health [64].

Cobalt concentrations in muscle tissue of the species Prochilodus lineatus (0.049 ± 0.02–0.124 ± 0.056 mg/kg) and Pimelodus maculatus (0.022 ± 0.010–0.06 ± 0.008 mg/kg) are lower than the values established by the FAO (0.26 mg/kg) [65] and those obtained in muscle tissue of Euryglossa orientalis (3.21 mg/kg) and Otolithes ruber (1.94 mg/kg) from the mouth of the Arvand River and northwestern coastal waters of the Persian Gulf [7]. There are no Co values established by Anvisa/Brazil for fishes. Cobalt exposure in fishes has been shown to induce various toxic effects, impacting growth, biochemical parameters, and overall health. Studies indicate that cobalt chloride and other cobalt compounds can lead to significant physiological alterations in species such as rainbow trout Oncorhynchus mykiss, Mozambique tilapia Oreochromis mossambicus, and zebrafish [66,67,68].

The mean concentrations of Cr were 1.22 (±0.29)–3.47 (±0.78) mg/kg (Table 7) in Prochilodus lineatus and 1.02 (±0.1)–2.97 (±0.30) mg/kg in Pimelodus maculatus (Table 8), which are above the values of permissible limits of metals in fish recommended by the FAO (1 mg/kg). Moreover, the concentration of Cr quantified in P. lineatus from the rivers in the state of Mato Grosso do Sul were higher than that found by Meche et al. (2010) [58], who studied P. lineatus (0.76 mg/kg) in the Piracicaba (SP), Brazil. However, our findings are below those found in the muscle tissue of Liza subviridis from the Persian Gulf (4.54–8 mg/kg) [7]. Chromium poses significant toxic effects on fishes; this element leads to various physiological and biochemical alterations, including hematological changes, organ damage, and impaired immune responses. According to studies, Cr can enter fish through the gills, skin, and digestive tracts, accumulating in vital organs and disrupting oxidative homeostasis [69,70].

Table 7

Metal(loid) concentration in Prochilodus lineatus muscle (mg/kg) compared to the maximum limit established by Anvisa/Brazil and values of permissible limits of metals in fish recommended by the FAO.

Element	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	Pardo River	Lontra River	Maximum Limit *
Al	2020	7.49 ± 0.66	9.26 ± 1.78	6.78 ± 0.62	4.05 ± 0.86	5.44 ± 0.50	NE
Al	2021	9.34 ± 1.20	12.763 ± 2.5	8.359 ± 0.90	5.312 ± 1.12	6.256 ± 1.07	NE
As	2020	0.15 ± 0.05	0.601 ± 0.12	0.346 ± 0.051	0.155 ± 0.032	0.167 ± 0.054	1.0 *
As	2021	0.22 ± 0.04	0.66 ± 0.06	0.39 ± 0.05	0.204 ± 0.047	0.134 ± 0.050	1.0 *
Cd	2020	1.04 ± 0.06	1.32 ± 0.36	1.07 ± 0.15	0.68 ± 0.096	1.05 ± 0.06	0.05 *
Cd	2021	1.10 ± 0.06	1.56 ± 0.31	1.17± 0.30	0.66 ± 0.074	0.856 ± 0.096	0.05 *
Co	2020	0.049 ± 0.02	0.071 ± 0.01	0.083 ± 0.010	0.055 ± 0.011	0.067 ± 0.010	0.26 **
Co	2021	0.050 ± 0.01	0.086 ± 0.05	0.124 ± 0.056	0.053 ± 0.011	0.080 ± 0.015	0.26 **
Cr	2020	2.5 ± 0.46	2.87 ± 0.70	2.36 ± 0.55	1.22 ± 0.29	1.52 ± 0.43	1.0 **
Cr	2021	3.12 ± 0.47	3.47 ± 0.78	2.41 ± 0.31	1.37 ± 0.27	1.65 ± 0.37	1.0 **
Cu	2020	1.37 ± 0.14	2.14 ± 0.18	1.09 ± 0.16	0.450 ± 0.09	0.134 ± 0.05	30.0 **
Cu	2021	1.29 ± 0.30	3.13 ± 0.55	0.991 ± 0.11	0.201 ± 0.06	0.122 ± 0.02	30.0 **
Hg	2020	0.956 ± 0.03	1.13 ± 0.12	0.801 ± 0.01	0.722 ± 0.016	0.652 ± 0.042	1.0 ***
Hg	2021	1.00 ± 0.02	1.27 ± 0.27	1.319 ± 0.55	0.913 ± 0.065	0.882 ± 0.102	1.0 ***
Mo	2020	0.39 ± 0.09	0.046 ± 0.009	0.04 ± 0.017	0.123 ± 0.024	0.035 ± 0.008	NE
Mo	2021	0.62 ±0.11	0.272 ± 0.074	0.081 ± 0.013	0.272 ± 0.074	0.060 ± 0.02	NE
Ni	2020	0.427 ± 0.04	0.836 ± 0.044	0.73 ± 0.033	0.230 ± 0.032	0.503 ± 0.047	80.0 **
Ni	2021	0.495 ± 0.10	0.90 ± 0.18	1.04 ± 0.16	0.467 ± 0.138	0.659 ± 0.05	80.0 **
Pb	2020	0.209 ± 0.06	0.318 ± 0.064	0.212 ± 0.028	0.310 ± 0.069	0.198 ± 0.040	0.30 *
Pb	2021	0.317 ± 0.011	0.392 ± 0.034	0.238 ± 0.035	0.403± 0.047	0.248 ± 0.039	0.30 *

Note: * Maximum limit of Inorganic Contaminants in Food, fish (Anvisa, 2013) [60]. ** FAO (1983) [65]. *** Value established for non-predatory fish (Anvisa, 2013) [60]. NE—Not established.

Table 8

Metal(loid) concentration in Pimelodus maculatus muscle (mg/kg) compared to the maximum limit established by Anvisa/Brazil and values of permissible limits of metals in fish recommended by the FAO.

Element	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	Pardo River	Lontra River	Maximum Limit *
Al	2020	5.40 ± 0.54	6.36 ± 1.15	4.58 ± 0.85	3.88 ± 0.73	4.01 ± 0.51	NE
Al	2021	7.11 ± 0.17	9.98 ± 1.0	5.04 ± 0.96	4.91 ± 0.22	4.63 ± 0.55	NE
As	2020	0.105 ± 0.017	0.230 ± 0.05	0.132 ± 0.20	0.011 ± 0.018	0.119 ± 0.30	1.00 *
As	2021	0.239 ± 0.011	0.367 ± 0.074	0.191 ± 0.011	0.032 ± 0.012	0.119 ± 0.020	1.00 *
Cd	2020	1.66 ± 0.51	1.52 ± 0.60	1.46 ± 0.38	0.59 ± 0.14	1.20 ± 0.45	0.05 *
Cd	2021	2.24 ± 0.69	1.86 ± 0.70	1.59 ± 0.58	0.628 ± 0.14	1.30 ± 0.47	0.05 *
Co	2020	0.034 ± 0.012	0.054 ± 0.012	0.015± 0.004	0.033 ± 0.010	0.050 ± 0.004	0.26 **
Co	2021	0.048 ± 0.005	0.06 ± 0.008	0.022 ± 0.010	0.040 ± 0.013	0.048 ± 0.019	0.26 **
Cr	2020	2.55 ± 0.58	3.02 ± 0.46	2.32 ± 0.57	1.37 ± 0.23	1.02 ± 0.1	1.0 **
Cr	2021	2.97 ± 0.30	2.95 ± 0.50	2.81 ± 0.47	1.20 ± 0.26	1.10 ± 0.30	1.0 **
Cu	2020	1.08 ± 0.28	1.95 ± 0.70	0.99 ± 0.12	0.215 ± 0.056	0.081 ± 0.025	30.0 **
Cu	2021	1.90 ± 0.120	2.20 ± 0.95	1.0 ± 0.13	0.42 ± 0.072	1.4 ± 0.05	30.0 **
Hg	2020	0.742 ± 0.13	1.05 ± 0.08	0.599 ± 0.013	0.493 ± 0.030	0.50 ± 0.11	1.0 ***
Hg	2021	0.96 ± 0.06	1.50 ± 0.46	0.560 ± 0.230	0.60 ± 0.30	0.46 ± 0.20	1.0 ***
Mo	2020	0.17 ± 0.06	0.027 ± 0.011	0.027 ± 0.09	0.12 ± 0.024	0.016 ± 0.03	NE
Mo	2021	0.290 ± 0.02	0.12 ± 0.03	0.034 ± 0.06	0.32 ± 0.09	0.031 ± 0.09	NE
Ni	2020	0.216 ± 0.073	0.437 ± 0.028	0.459 ± 0.038	0.187 ± 0.054	0.197 ± 0.039	80.0 **
Ni	2021	0.201 ± 0.052	0.560 ± 0.049	0.450 ± 0.046	0.236 ± 0.03	0.303 ± 0.043	80.0 **
Pb	2020	0.457 ± 0.053	0.560 ± 0.054	0.413 ± 0.069	0.11 ± 0.013	0.13 ± 0.007	0.3 *
Pb	2021	0.590 ± 0.031	0.742 ± 0.084	0.449 ± 0.063	0.140 ± 0.078	0.169 ± 0.038	0.3 *

Note: * Maximum limit of Inorganic Contaminants in Food, fish (Anvisa, 2013) [60]. ** FAO (1983) [65]. *** Value established for predatory fish (Anvisa, 2013) [60]. NE—Not established.

The mean concentrations of Cu in fish samples from Table 7 ranged between 0.991 (±0.11) and 3.13 (±0.55) mg/kg in Prochilodus lineatus muscle, and 0.081 (±0.025)–2.20 (±0.95) mg/kg in Pimelodus maculatus muscle (Table 8). All values of Cu concentration were below the permissible limits of Cu in fish recommended by the FAO (30 mg/kg). Meche et al. (2010) in Brazil [58] obtained concentration values of 1.80 mg/kg in their study using muscle samples from Prochilodus lineatus, and 0.76 mg/kg in Pimelodus maculatus muscle. Thus, the concentrations of Cu values in Anhanduí River-2 in 2020–2021 (Table 7 and Table 8) are above the results obtained by Meche et al. (2010) [58] for both species. It can be seen from the results obtained in Table 7 and Table 8 and comparisons with other studies that the same or different species of fish within a country have different variations in concentration values of metal(loid)s. In fact, the mean Cu concentration in the muscle tissue of Otolithes ruber from Mahshahr Port in Khozestan Province in Iran (25.3 mg/kg) is higher than the all values in Table 7 and Table 8. Copper exhibits both essential and toxic effects on fish, depending on its concentration and form. Excessive exposure can lead to significant physiological and biochemical disruptions, while high concentrations of copper sulfate can cause skin irritation, gill damage, and even mortality in fishes [71,72].

According to Table 7 and 8, Hg concentrations range from 0.652 (±0.042) to 1.319 (±0.55) mg/kg in Prochilodus lineatus muscle tissue and 0.46 (±0.20)–1.50 (±0.46) mg/kg in Pimelodus maculatus muscle tissue. However, only the concentration of Hg in muscle samples of Prochilodus lineatus from Anhanduí-2 River (year 2020–2021) and Anhanduí-3 River (2021), and Hg in the muscle of Pimelodus maculatus from Rio Anhanduí-2 (2021) are higher than the concentrations stipulated by Anvisa for predatory fish (1.0 mg/kg). However, the Hg concentration values in the fish muscle samples presented in Table 7 and Table 8 are below the concentration values obtained for other species, such as Anodontostoma chacunda (2.04 mg/kg), Johnius belangerii (4.40 mg/kg), and Cynoglossurs arel (5.82 mg/kg) from the Musa Estuary and Mahshahr Port in the Persian Gulf [7]. Mercury exposure in fish leads to significant toxic effects, impacting their health and development. Histological examinations revealed severe tissue damage in the gills, liver, and stomach of Clarias batrachus [73]. Furthermore, chronic exposure in silver carp larvae resulted in decreased antioxidant capacity and neurotoxic changes [74]. These findings underscore the urgent need for monitoring mercury levels in aquatic ecosystems to protect fish health and, by extension, human health through the food chain.

In Table 7, Mo concentration was 0.035 (±0.008)–0.62 (±0.11) mg/kg in Prochilodus lineatus muscle, and 0.016 (±0.03)–0.290 (±0.02) mg/kg in Pimelodus maculatus muscle (Table 8). There are no permitted levels defined by Anvisa/Brazil and the FAO for Mo in fishes. However, some values of Mo in Table 7 and Table 8 are above those obtained by other Brazilian studies, which quantified 0.05 mg/kg of this element in samples of Pimelodus maculatus muscle [58]. According to study using wild rainbow trout captured from Zayandeh-Rood River in Chaharmahal-va-Baghtiari province, Iran, concentration of Mo in tissues of wild rainbow trout was 0.121 (±0.046) mg/kg [75]. After comparison, it was found that the concentration of Mo in the muscle of Prochilodus lineatus and Pimelodus maculatus from Anhanduí River-1 and Pardo River during the years 2020–2021 and from Anhanduí River-2 in 2021 are above those obtained in Iran. Molybdenum in high concentrations is a toxic element for fishes. Studies indicate that molybdenum can be acutely lethal to various fish species, including rainbow trout [76]. Furthermore, it has been shown to adversely affect fish embryos and spermatogenesis, raising concerns about its ecological impact [77]. According to Wang et al. (2022) [57], the toxicity of molybdenum is influenced by its chemical form, with ammonium molybdate exhibiting the highest toxicity in aquatic environments. Additionally, current water quality guidelines for molybdenum may not accurately reflect its potential toxicity, suggesting a need for reevaluation [78].

The mean contents of Ni in fish species sampled in 2020 and 2021 from the river waters of the city of Campo Grande range from 0.230 (±0.032) to 1.04 (±0.16) in Prochilodus lineatus muscle, and from 0.187 (±0.054) to 0.560 (±0.049) in Pimelodus maculatus muscle. All mean concentrations of Ni found in the muscle tissue of Prochilodus lineatus and Pimelodus maculatus from the rivers are below the 80.0 mg/kg acceptable limit recommended by the FAO. Meche et al. (2010) [58], who studied Pimelodus maculatus and Prochilodus lineatus in Brazilian rivers, obtained 0.34 mg/kg and 1.53 mg/kg in muscle samples of those fishes. Therefore, the highest values of Ni concentrations in the samples in Table 7 and Table 8 are above the values obtained by Meche et al. (2010) [58]. Ni concentration in Prochilodus lineatus muscle (Table 7) and Pimelodus maculatus muscle (Table 8), depending on the year of collection, are above or below the levels of Ni in fish species from Caspian Sea (0.52, 0.12 Rutilus frisii kutum) and 0.44 μg/g of wet weight in Cyprinus carpio [13]. Nickel poses toxicity risks to fish, primarily through bioaccumulation and oxidative stress mechanisms. Studies indicate that nickel can enter fish through the gills, skin, and ingestion of contaminated food, leading to various physiological and histopathological effects [79]. Chronic exposure results in oxidative stress, organ damage, and altered gene expression, affecting growth and reproductive capabilities [79,80]. Furthermore, nickel’s presence in aquatic ecosystems disrupts ecological balance, causing cellular dysfunction in some species [81].

In Table 7, the Ni concentration in Prochilodus lineatus muscle ranged from 0.198 (±0.040) to 0.403 (±0.047) mg/kg, and in Table 8, the concentration in Pimelodus maculatus muscle ranged from 0.11 (±0.013) to 0.742 (±0.084) mg/kg. All values of concentrations of Ni in Table 7 and Table 8 are notably lower than those established by the FAO (80.0 mg/kg) and one Brazilian study using fish from the Piracicaba River Pimelodus maculatus (3.25 mg/kg) and Prochilodus lineatus (0.57 mg/kg). On the other hand, Pb concentrations in samples of Prochilodus lineatus muscle from the rivers Anhanduí River-1 (2020), Anhanduí River-3 (2020–2021), and Lontra River (2020–2021) in Table 7, as well as Pimelodus maculatus muscle in Pardo River (2020–2021) and Lontra River (2020–2021) were lower than those obtained fish species from the Caspian Sea (0.38 mg/kg of wet weight in Rutilus frisii kutum and Cyprinus carpio) [13]. Exposure to lead can lead to genotoxicity, hepatotoxicity, and reproductive impairments, affecting fish health and populations [82].

As seen above, the variation in metal(loid) levels in fishes across different studies can be attributed to geographical, geological, and climatic factors. Research indicates that metal concentrations in fish tissues vary significantly based on location, species, and environmental conditions [13].

For instance, in the trans-Himalayan ecosystem, chemical elements like Cu and Zn showed substantial differences in concentration across seasons and sites in Cyprinus carpio muscle, highlighting the influence of local pollution sources [83]. In the Gulf of California, mining activities contributed to elevated metal levels in fishes, demonstrating the impact of anthropogenic factors on metal accumulation [84]. Furthermore, the study of Sheikhzadeh and Hamidian (2021) [7] showed that fishes from different aquatic ecosystems, particularly the Persian Gulf and Caspian Sea, exhibit varying levels of metal and metalloid accumulation, influenced by factors such as species habitat and feeding habits [7]. These findings underscore the complex interplay of environmental factors in determining metal levels in fishes, necessitating ongoing monitoring and assessment.

3.7. Human Health Risk Assessment

3.7.1. Daily Intake of Metal(loid)s Due to Fish Consumption

Based on the maximum concentration of As, Cd, Co, Cr, Cu, Mo, Ni, and Pb, the average daily doses (ADD) were calculated considering the oral exposure of 8-year-old children and 50-year-old adults and can be seen in Table 9 for P. lineatus consumption and Table 10 for P. maculatus consumption.

When comparing the ADDs due to P. lineatus consumption with the maximum daily oral dose (Rfd) recommended by USEPA, we can verify that Cu, Mo, Ni, and Pb presented values lower than their respective Rfds (4 × 10⁻² mg/kg/d; 5 × 10⁻³ mg/kg/d; 1.1 × 10⁻² mg/kg/d; 3.5 × 10⁻³ mg/kg/d) for both children and adults, thus being within a safe limit for consumption. However, the estimated daily intake of metal(loid)s was above the Rfd for As (3 × 10⁻⁴ mg/kg/d), Cr (3 × 10⁻³ mg/kg/d), and Cd (1 × 10⁻⁴ mg/kg/d) in all collection sites when the fish is consumed by children, representing a threat to health [84]. Cobalt presented ADD greater than Rfd (3 × 10⁻⁴ mg/kg/d) for children only in locations Anhanduí River-2 and Anhanduí River-3.

The consumption of P. maculatus presents ADD of Co, Cu, Mo, Ni, and Pb < Rfd. In contrast, the ADD of As was shown to be above Rfd, when consumed by children, with the exception of the data found in Pardo River, and above Rfd also when consumed by adults in sites Anhanduí River-2 (2021), Anhanduí River-3 and Lontra River (2020). Cadmium presented ADD greater than Rfd for both children and adults in all collection sites, and Cr obtained ADD higher than Rfd for children, with the exception of Lontra River (2020).

These results demonstrate that the consumption of both P. lineatus and P. maculatus from the studied rivers can pose health risks, especially to children, when exposed to a frequency of 156 days/year to these elements, that is, a 150 g portion consumed three times a week. As a consequence of long-term exposure, metal(loid)s can accumulate in the vital organs of the human body, posing serious risks to human health such as cancer, bone disorders, neurological, renal, hematopoietic, and reproductive effects [85,86].

3.7.2. Hazard Quotient (HQ) and Hazard Index (HI) Due to Fish Consumption

The values of the hazard quotient (HQ) and hazard index (HI) of metal(loid)s, considering the consumption of P. lineatus and P. maculatus from the rivers in the state of Mato Grosso do Sul, are presented in Table 11 and Table 12. Regarding the exposure of children and adults to metal(loid)s due to the consumption of P. lineatus, we can highlight that As presented HQ > 1 for children in all studied locations, presenting a maximum HQ value of 5.926 in Anhanduí River-2 (2020), and for adults in Anhanduí River-2 and Anhanduí River-3, with a maximum HQ of 2.201 also in Anhanduí River-2 in the first collection (2020).

Still regarding P. lineatus consumption, Co presented HQ > 1 for children in 40% of the rivers studied, and Cr presented HQ > 1 for children in 80% of the locations evaluated in 2020 and 100% in 2021. The greatest contribution to HI was the HQ of Cd, which presented 100% of the values found above 1, both for children and adults in the rivers evaluated.

Regarding the non-carcinogenic risk inherent in the consumption of P. maculatus, we can highlight that Co, Cu, Mo, Ni, and Pb presented HQ < 1. On the other hand, As presented HQ > 1 in Anhanduí River-1, Anhanduí River-2, Anhanduí River-3, and Lontra River for children and in Anhanduí River-2, Anhanduí River-3, and Lontra River for adults in 2020. In 2021, Anhanduí River-3 and Lontra River had HQ < 1 for adults. The values found for HQ of Cd were greater than 1 for children and adults in all studied locations, as observed for P. lineatus. Chromium presented 80% of the HQ values greater than 1 in the first collection (2020) and 100% in the second collection (2021) for children, while for adults the HQ values greater than 1 corresponded to 20% in the first collection and 40% in the second.

The HI values calculated based on the sum of the HQs of all elements evaluated were greater than 1 in both collections from all locations studied. It should be noted that Cd represents the largest part of the potential cumulative risk (81–82%) for P. lineatus in Anhanduí River-3 in the first and second collections, respectively, and (92%) for P. maculatus in Anhanduí River-1 in both collections. These results indicate that there is a high risk of non-carcinogenic adverse effects on human health [87] when consuming P. lineatus and P. maculatus from the rivers evaluated, especially if we consider that these metal(loid)s have no physiological function and can bioaccumulate, causing chronic diseases and potential damage to the health of the population [88]. Given this fact, the importance of monitoring heavy metals in fishes becomes even more relevant, providing support for guiding the population regarding the rate of ingestion, origin and quality of the fish flesh.

Brazilian populations in river ecosystems are exposed to metals not only through fish consumption but also via various environmental pathways. These pathways include contaminated water, sediment, and agricultural runoff, which contribute to the overall metal exposure. Thus, while fish consumption is a notable source of metal exposure, the broader environmental context including water quality and agricultural practices plays a critical role in the overall exposure of Brazilian receptors to toxic metals.

3.7.3. Carcinogenic Risk (CR) Due to Fish Consumption

The estimated lifetime carcinogenic risks (CRs) for children and adults due to exposure to metal(loid)s inherent in the consumption of 450 g of fish per week are presented in Table 13. The values found in this study for exposure to Cu and Pb presented CR values between the acceptable risk values of 1 × 10⁻⁴ and 1 × 10⁻⁶. The As, Cd, and Cr for children and adults were all greater than 1 × 10⁻⁴. Considering the P. lineatus results, As presented maximum values of 2.67 × 10⁻³ for children and 9.90 × 10⁻⁴ for adults. Chromium presented 5.24 × 10⁻³ for children and 1.95 × 10⁻³ for adults, while Cd exhibited a maximum value of 1.75 × 10⁻³ for children and 6.51 × 10⁻⁴ for adults. All these maximum values were found in Anhanduí River-2 during 2021.

In the results recorded for P. maculatus, it is observed that the maximum CR values are lower than those found for P. lineatus, where As presented a value of 1.63 × 10⁻³ for children and 6.06 × 10⁻⁴ for adults in Anhanduí River-2 during 2021. Chromium presented 4.29 × 10⁻³ for children and 1.59 × 10⁻³ for adults in Anhanduí River-2 during 2020. Cadmium registered values of 2.75 × 10⁻³ for children and 1.02 × 10⁻³ for adults in Anhanduí River-1 during 2021.

Heavy metal contamination in rivers in the state of Mato Grosso do Sul is a cause for great concern, as these rivers are extensive in urban areas and easily accessible, and are often used for fishing. This leads us to believe that periodic monitoring should be established by control agencies in order to minimize impacts on human health. In addition, health safety must be guaranteed for the riverside population, which often depends on aquatic resources and may consume larger portions and more frequently than estimated in this study, as well as for the general population due to the commercialization of these fish [58,84,89].

4. Conclusions

The ecological risk assessment in sediment samples from rivers in the state of Mato Grosso do Sul based on the Igeo classification revealed that the rivers are unpolluted to moderately polluted by Cu, As, Ni, and Pb. Conversely, they are strongly to extremely polluted by Cd. According to the PLI, all rivers showed a decline in environmental quality.

The concentration of Al was the highest in P. lineatus and P. maculatus in relation to the other elements analyzed. In addition, the average concentrations of Cd, Hg, and Pb are higher than the maximum limit established by Anvisa for non-predatory fish such as P. lineatus and higher than the maximum limit established for predatory fish such as P. maculatus. The As, Cd, Cu, Pb, and Cr contents in P. lineatus and P. maculatus were higher than the average found in other Brazilian studies. The concentration values of Co, Cu, and Ni in P. lineatus and P. maculatus are below the values of permissible limits of heavy metals in fishes recommended by the FAO. In the two years of collecting samples such as sediment, water, and fish tissues, there was variation in the analyzed metal concentrations. Levels of metals and metalloids varied between different species and the same species of fish in different locations and countries. Furthermore, the estimate of carcinogenic risk due to chronic exposure of children and adults to heavy metals based on an ingestion of these fish three times a week demonstrated that the risk is mainly related to As and Cd.

Contamination by heavy metals and metalloids in the rivers in the state of Mato Grosso do Sul in Brazil represents a cause for great concern as they are large rivers located in urban areas with easy access and are frequently used for fishing. This leads us to believe that periodic monitoring should be carried out by control bodies with the aim of minimizing impacts on human health.

Author Contributions

Conceptualization., M.R.F. and E.S.d.P.M.; methodology, M.R.F.; validation, R.d.C.A.G., P.A.H., K.d.C.F.G. and D.B.; formal analysis, M.R.F., R.J.O. and C.S.d.A.M.; data curation, M.R.F.; writing—original draft preparation, V.A.d.N.; writing—review and editing, D.A.Z.G. and V.A.d.N.; visualization, M.A.P.A., A.C.G.R., D.B., R.d.C.A.G., K.d.C.F.G., P.F.S.T., M.L.B.V. and P.A.H.; supervision, V.A.d.N.; project administration, V.A.d.N.; funding acquisition, V.A.d.N. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

The data used to support the findings of this study are available from the corresponding author upon request.

Acknowledgments

The authors thank the Faculty of Medicine, Federal University of Mato Grosso do Sul, for their scientific support.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

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Figures and Tables

Figure 1 Sediment, water, and fish collection sites in the rivers in the state of Mato Grosso do Sul (MS), Central-West Brazil (A). Brazilian territory (B). State of Mato Grosso do Sul (C). Sampling sites: L1. Anhanduí River-1; L2. Anhanduí River-2; L3. Anhanduí River-3; L4. Pardo River; L5. Lontra River. The arrows indicate the flow of rivers.

Figure 2 Loading graphs for PC1 versus PC2 obtained by processing metal(loid) determination data in the water collected at different sampling sites (L1 = Anhanduí River-1, L2 = Anhanduí River-2, L3 = Anhanduí River-3, L4 = Pardo River, and L5 = Lontra River).

Figure 3 Loading graphs for PC1 versus PC2 obtained by processing metal(loid) determination data in the sediment collected at different sampling sites (L1 = Anhanduí River-1, L2 = Anhanduí River-2, L3 = Anhanduí River-3, L4 = Pardo River, and L5 = Lontra River).

Figure 4 Matrix plot: geo-accumulation index (Igeo) of different metal(loid)s in sediment samples, the right column represents the Igeo Classification values. Igeo < 0 practically not polluted; 0 < Igeo < 1 not polluted to moderately polluted, 1 < Igeo < 2 moderately polluted, 3 < Igeo < 4 strongly polluted, 4 < Igeo < 5 strongly to extremely polluted.

Table 1

Number of samples collected in 2020 and 2021.

	Year of Collection	Number of Specimens Collected
	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	PardoRiver	Lontra River
Prochilodus lineatus	2020	6	7	9	6	8
Prochilodus lineatus	2021	9	6	8	7	6
Pimelodus maculatus	2020	11	13	14	18	12
Pimelodus maculatus	2021	12	16	9	15	10

Table 2

External calibration parameters, limit of detection (LOD), and limit of quantification (LOQ) obtained by ICP OES and correlation coefficient (R²).

Element	LOD (mg/L)	LOQ (mg/L)	R²
Al	0.001	0.003	0.9996
As	0.001	0.004	0.9999
Cd	0.00008	0.0003	0.9998
Co	0.0002	0.0008	0.9999
Cr	0.0002	0.0006	0.9999
Cu	0.0002	0.0006	0.9999
Hg	0.001	0.005	0.0956
Mo	0.0003	0.001	0.9999
Ni	0.0005	0.002	0.9999
Pb	0.0006	0.001	0.9980

Table 3

Mean concentrations of metal(loid)s and standard deviation (mg/kg) quantified in the waters of rivers in the state of Mato Grosso do Sul between 2020 and 2021.

Element	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	Pardo River	Lontra River
Al	2020	0.059 ± 0.012	0.081 ± 0.021	0.042 ± 0.003	0.064 ± 0.0045	0.028 ± 0.0026
Al	2021	0.044 ± 0.016	0.056 ± 0.0079	0.041 ± 0.002	0.033 ± 0.004	0.030 ± 0.0092
As	2020	0.081 ± 0.010	0.095 ± 0.006	0.036 ± 0.005	0.0051 ± 0.0003	0.0023 ± 0.0009
As	2021	0.060 ± 0.017	0.073 ± 0.003	0.024 ± 0.008	0.0038 ± 0.0005	0.0042 ± 0.0007
Ni	2020	0.96 ± 0.05	1.32 ± 0.54	0.80 ± 0.06	0.397 ± 0.04	0.092 ± 0.006
Ni	2021	0.89 ± 0.05	1.24 ± 0.16	0.71 ± 0.05	0.314 ± 0.06	0.616 ± 0.13
Pb	2020	0.82 ± 0.06	1.23 ± 0.56	0.52 ± 0.05	0.81 ± 0.15	0.065 ± 0.04
Pb	2021	0.58 ± 0.09	0.90 ± 0.07	0.29 ± 0.009	0.83 ± 0.13	0.064 ± 0.015
Hg	2020	0.046 ± 0.01	0.074 ± 0.002	0.031 ± 0.005	0.0037 ± 0.0005	0.0078 ± 0.0009
Hg	2021	0.027 ± 0.02	0.049 ± 0.007	0.043 ± 0.004	0.0031 ± 0.0007	0.0078 ± 0.0010
Co	2020	0.051 ± 0.03	0.090 ± 0.009	0.028 ± 0.005	0.0046 ± 0.0006	0.0029 ± 0.00009
Co	2021	0.033 ± 0.003	0.064 ± 0.004	0.018 ± 0.009	0.003 ± 0.007	0.0023 ± 0.0005
Cu	2020	0.84 ± 0.16	2.28 ± 0.59	0.57 ± 0.10	0.369 ± 0.085	0.576 ± 0.084
Cu	2021	0.44 ± 0.09	1.105 ± 0.71	0.52 ± 0.035	0.251 ± 0.046	0.374 ± 0.125
Cr	2020	1.34 ± 0.43	1.92 ± 0.70	1.26 ± 0.52	1.20 ± 0.46	0.024 ± 0.001
Cr	2021	1.21 ± 0.67	1.48 ± 0.45	0.96 ± 0.11	1.55 ± 0.48	0.023 ± 0.008
Cd	2020	0.079 ± 0.020	0.068 ± 0.02	0.048 ± 0.01	0.0057 ± 0.001	0.0048 ± 0.0015
Cd	2021	0.057 ± 0.016	0.063 ± 0.017	0.066 ± 0.02	0.0054 ± 0.002	0.0035 ± 0.0012
Mo	2020	<LOD	<LOD	<LOD	<LOD	<LOD
Mo	2021	<LOD	<LOD	<LOD	<LOD	<LOD

LOD—Limit of detection.

Table 4

Mean concentrations of metal(loid)s and standard deviation (mg/kg) quantified in the sediments of rivers in Mato Grosso do Sul in the period 2020–2021 compared with Conama/Brazil set by sediments.

Element	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	Pardo River	Lontra River	Conama/Brazil
Al	2020	6.45 ± 0.52	7.324 ± 0.152	5.657 ± 0.232	4.045 ± 0.986	4.447 ± 0.732	ND
Al	2021	7.28 ± 0.036	8.98 ± 0.95	6.754 ± 0.813	5.9578 ± 0.852	5.458 ± 0.452	ND
As	2020	7.20 ± 0.62	8.124 ± 0.85	6.657 ± 0.232	5.045 ± 0.986	6.447 ± 0.232	5.9
As	2021	7.96 ± 0.768	9.985 ± 0.643	7.754 ± 0.513	6.9578 ± 0.456	5.458 ± 0.634	5.9
Ni	2020	22.38 ± 1.15	25.348 ± 1.12	20.654 ± 0.195	21.236 ± 0.188	20.654 ± 0.542	18
Ni	2021	23.06 ± 1.05	26.265 ± 1.24	23.145 ± 0.736	24.765 ± 0.452	22.345 ± 0.236	18
Pb	2020	35.12 ± 2.06	38.02 ± 1.365	37.34 ± 1.205	24.978 ± 1.065	25.02 ± 0.78	35
Pb	2021	37.09 ± 3.91	40.54 ± 2.265	39.98 ± 2.081	30.232 ± 1.065	22.12 ± 0.56	35
Hg	2020	0.650 ± 0.570	0.970 ± 0.012	0.673 ± 0.068	0.562 ± 0.07	0.254 ± 0.078	0.17
Hg	2021	0.349 ± 0.035	0.563 ± 0.046	0.395 ± 0.089	0.463 ± 0.024	0.120 ± 0.019	0.17
Co	2020	10.05 ± 1.054	14.54 ± 1.26	13.23 ± 1.05	9.659 ± 0.180	8.057 ± 1.26	ND
Co	2021	10.23 ± 1.893	17.987 ± 1.04	14.825 ± 1.00	10.112 ± 1.09	9.532 ± 0.185	ND
Cu	2020	40.48 ± 2.381	50.978 ± 3.08	45.105 ± 1.85	30.352 ± 2.205	33.289 ± 2.45	35.7
Cu	2021	43.23 ± 1.98	53.873 ± 1.48	48.894 ± 1.95	35.456 ± 2.89	34.476 ± 1.76	35.7
Cr	2020	20.02 ± 1.298	20.02 ± 0.66	19.058 ± 0.401	18.54 ± 0.586	16.845 ± 0.435	37.3
Cr	2021	23.23 ± 0.53	24.02 ± 0.32	21.527 ± 0.982	20.02 ± 1.096	21.653 ± 0.102	37.3
Cd	2020	2.218 ± 0.065	2.52 ± 0.07	2.432 ± 1.05	2.32 ± 0.85	2.257 ± 0.916	0.60
Cd	2021	2.899 ± 0.784	3.0521 ± 0.86	3.904 ± 0.74	3.50 ± 0.94	3.309 ± 0.107	0.60
Mo	2020	2.943 ± 0.257	3.320 ± 0.754	2.710 ± 0.264	2.910 ± 0.157	2.910 ± 0.741	ND
Mo	2021	3.042 ± 0.724	4.610 ± 0.402	3.560 ± 0.756	3.710 ± 0.687	3.585 ± 0.321	ND

Conama: Resolution N° 420, of 28 December 2009, Brazil. ND—Not determined.

Table 5

Contamination factor and pollution load index in the river sediment.

Element	Year of Collection	Contamination Factor (CF)
Element	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	Pardo River	Lontra River
As	2020	2.468	2.832	2.173	1.903	2.107
As	2021	2.755	3.353	2.608	2.339	1.922
Cd	2020	32.613	37.00	49.743	45.29	45.33
Cd	2021	52.614	55.887	66.343	63.43	48.80
Co	2020	0.951	1.353	1.223	0.842	0.798
Co	2021	1.038	1.629	1.355	0.959	0.832
Cr	2020	0.704	0.683	0.642	0.631	0.570
Cr	2021	0.784	0.803	0.743	0.697	0.718
Cu	2020	1.505	1.897	1.648	1.143	1.254
Cu	2021	1.587	1.943	1.785	1.346	1.272
Mo	2020	24.615	31.34	22.87	23.59	28.09
Mo	2021	28.969	38.55	33.20	33.82	30.04
Ni	2020	2.734	3.074	2.421	2.488	2.462
Ni	2021	2.801	3.194	2.774	2.929	2.623
Pb	2020	3.365	3.564	3.488	2.357	2.335
Pb	2021	3.711	3.874	3.06	2.832	2.052
	PLI—pollution load index
Total	2020	3.412	3.981	3.581	3.037	3.112
Total	2021	3.926	4.673	4.262	3.730	3.219

Table 6

River sediment enrichment factor.

Element	Year of Collection	Enrichment Factor (EF)
Element	Year of Collection	Anhanduí River-1	Anhanduí River-2	Anhanduí River-3	Pardo River	Lontra River
As	2020	0.90	0.92	0.90	0.76	0.86
As	2021	0.98	1.05	0.94	0.80	0.73
Cd	2020	11.93	8.09	11.11	14.97	15.13
Cd	2021	18.79	11.24	13.58	17.45	18.53
Co	2020	0.35	0.44	0.51	0.34	0.32
Co	2021	0.37	0.51	0.49	0.33	0.32
Cr	2020	0.26	0.22	0.27	0.25	0.23
Cr	2021	0.28	0.25	0.27	0.24	0.27
Cu	2020	0.55	0.62	0.68	0.46	0.51
Cu	2021	0.57	0.61	0.64	0.46	0.48
Mo	2020	9.00	10.19	9.45	9.48	11.41
Mo	2021	10.34	12.07	11.97	11.55	11.46
Pb	2020	1.23	1.16	1.44	0.95	0.95
Pb	2021	1.32	1.21	1.37	0.97	0.78

Table 9

Average daily dose (mg/kg/day) of metal(loid)s for the oral exposure route for children and adults when consuming Prochilodus lineatus.

Element	Year of Collection	Anhanduí River-1		Anhanduí River-2		Anhanduí River-3		Pardo River		Lontra River
Element	Year of Collection	Children	Adults	Children	Adults	Children	Adults	Children	Adults	Children	Adults
As	2020	5.01 × 10⁻⁴	1.86 × 10⁻⁴	1.78 × 10⁻³	6.60 × 10⁻⁴	9.79 × 10⁻⁴	3.64 × 10⁻⁴	4.61 × 10⁻⁴	1.71 × 10⁻⁴	5.45 × 10⁻⁴	2.02 × 10⁻⁴
As	2021	6.56 × 10⁻⁴	2.44 × 10⁻⁴	1.77 × 10⁻³	6.58 × 10⁻⁴	1.08 × 10⁻³	4.03 × 10⁻⁴	6.19 × 10⁻⁴	2.30 × 10⁻⁴	4.54 × 10⁻⁴	1.69 × 10⁻⁴
Ni	2020	2.71 × 10⁻³	1.01 × 10⁻³	4.14 × 10⁻³	1.54 × 10⁻³	3.01 × 10⁻³	1.12 × 10⁻³	1.91 × 10⁻³	7.11 × 10⁻⁴	2.74 × 10⁻³	1.02 × 10⁻³
Ni	2021	2.86 × 10⁻³	1.06 × 10⁻³	4.61 × 10⁻³	1.71 × 10⁻³	3.62 × 10⁻³	1.35 × 10⁻³	1.81 × 10⁻³	6.72 × 10⁻⁴	2.35 × 10⁻³	8.72 × 10⁻⁴
Pb	2020	1.65 × 10⁻⁴	6.14 × 10⁻⁵	2.15 × 10⁻⁴	7.97 × 10⁻⁵	2.29 × 10⁻⁴	8.52 × 10⁻⁵	1.63 × 10⁻⁴	6.04 × 10⁻⁵	1.90 × 10⁻⁴	7.05 × 10⁻⁵
Pb	2021	1.48 × 10⁻⁴	5.50 × 10⁻⁵	3.35 × 10⁻⁴	1.25 × 10⁻⁴	4.44 × 10⁻⁴	1.65 × 10⁻⁴	1.58 × 10⁻⁴	5.86 × 10⁻⁵	2.34 × 10⁻⁴	8.70 × 10⁻⁵
Co	2020	7.92 × 10⁻³	2.94 × 10⁻³	8.80 × 10⁻³	3.27 × 10⁻³	7.18 × 10⁻³	2.67 × 10⁻³	3.72 × 10⁻³	1.38 × 10⁻³	4.81 × 10⁻³	1.79 × 10⁻³
Co	2021	8.85 × 10⁻³	3.29 × 10⁻³	1.05 × 10⁻²	3.89 × 10⁻³	6.71 × 10⁻³	2.49 × 10⁻³	4.04 × 10⁻³	1.50 × 10⁻³	4.98 × 10⁻³	1.85 × 10⁻³
Cu	2020	3.72 × 10⁻³	1.38 × 10⁻³	5.72 × 10⁻³	2.12 × 10⁻³	3.08 × 10⁻³	1.14 × 10⁻³	1.33 × 10⁻³	4.95 × 10⁻⁴	4.54 × 10⁻⁴	1.69 × 10⁻⁴
Cu	2021	3.92 × 10⁻³	1.46 × 10⁻³	9.07 × 10⁻³	3.37 × 10⁻³	2.71 × 10⁻³	1.01 × 10⁻³	6.44 × 10⁻⁴	2.39 × 10⁻⁴	3.50 × 10⁻⁴	1.30 × 10⁻⁴
Cr	2020	1.20 × 10⁻³	4.44 × 10⁻⁴	1.36 × 10⁻⁴	5.04 × 10⁻⁵	1.41 × 10⁻⁴	5.22 × 10⁻⁵	3.62 × 10⁻⁴	1.35 × 10⁻⁴	1.06 × 10⁻⁴	3.94 × 10⁻⁵
Cr	2021	1.79 × 10⁻³	6.64 × 10⁻⁴	8.53 × 10⁻⁴	3.17 × 10⁻⁴	2.32 × 10⁻⁴	8.61 × 10⁻⁵	8.53 × 10⁻⁴	3.17 × 10⁻⁴	1.97 × 10⁻⁴	7.33 × 10⁻⁵
Cd	2020	1.16 × 10⁻³	4.32 × 10⁻⁴	2.17 × 10⁻³	8.06 × 10⁻⁴	1.88 × 10⁻³	6.99 × 10⁻⁴	1.36 × 10⁻³	5.04 × 10⁻⁴	1.36 × 10⁻³	5.04 × 10⁻⁴
Cd	2021	1.47 × 10⁻³	5.45 × 10⁻⁴	2.66 × 10⁻³	9.89 × 10⁻⁴	2.96 × 10⁻³	1.10 × 10⁻³	1.49 × 10⁻³	5.54 × 10⁻⁴	1.75 × 10⁻³	6.49 × 10⁻⁴
Mo	2020	6.63 × 10⁻⁴	2.46 × 10⁻⁴	9.42 × 10⁻⁴	3.50 × 10⁻⁴	5.92 × 10⁻⁴	2.20 × 10⁻⁴	9.35 × 10⁻⁴	3.47 × 10⁻⁴	5.87 × 10⁻⁴	2.18 × 10⁻⁴
Mo	2021	8.09 × 10⁻⁴	3.00 × 10⁻⁴	1.05 × 10⁻³	3.90 × 10⁻⁴	6.73 × 10⁻⁴	2.50 × 10⁻⁴	1.11 × 10⁻³	4.12 × 10⁻⁴	7.08 × 10⁻⁴	2.63 × 10⁻⁴

Table 10

Average daily dose (mg/kg/day) of metal(loid)s for the oral exposure route for children and adults when consuming Pimelodus maculatus.

Element	Year of Collection	Anhanduí River-1		Anhanduí River-2		Anhanduí River-3		Pardo River		Lontra River
Element	Year of Collection	Children	Adults	Children	Adults	Children	Adults	Children	Adults	Children	Adults
As	2020	3.01 × 10⁻⁴	1.12 × 10⁻⁴	6.90 × 10⁻⁴	2.56 × 10⁻⁴	8.19 × 10⁻⁴	3.04 × 10⁻⁴	7.15 × 10⁻⁵	2.66 × 10⁻⁵	1.03 × 10⁻³	3.84 × 10⁻⁴
As	2021	6.16 × 10⁻⁴	2.29 × 10⁻⁴	1.09 × 10⁻³	4.04 × 10⁻⁴	4.98 × 10⁻⁴	1.85 × 10⁻⁴	1.08 × 10⁻⁴	4.03 × 10⁻⁵	3.43 × 10⁻⁴	1.27 × 10⁻⁴
Ni	2020	7.13 × 10⁻⁴	2.65 × 10⁻⁴	1.15 × 10⁻³	4.26 × 10⁻⁴	1.23 × 10⁻³	4.55 × 10⁻⁴	5.94 × 10⁻⁴	2.21 × 10⁻⁴	5.82 × 10⁻⁴	2.16 × 10⁻⁴
Ni	2021	6.24 × 10⁻⁴	2.32 × 10⁻⁴	1.50 × 10⁻³	5.58 × 10⁻⁴	1.22 × 10⁻³	4.54 × 10⁻⁴	6.56 × 10⁻⁴	2.44 × 10⁻⁴	8.53 × 10⁻⁴	3.17 × 10⁻⁴
Pb	2020	1.26 × 10⁻³	4.67 × 10⁻⁴	1.51 × 10⁻³	5.62 × 10⁻⁴	1.19 × 10⁻³	4.41 × 10⁻⁴	3.03 × 10⁻⁴	1.13 × 10⁻⁴	3.38 × 10⁻⁴	1.25 × 10⁻⁴
Pb	2021	1.53 × 10⁻³	5.69 × 10^-4	2.04 × 10⁻³	7.56 × 10⁻⁴	1.26 × 10⁻³	4.69 × 10⁻⁴	5.38 × 10⁻⁴	2.00 × 10⁻⁴	5.10 × 10⁻⁴	1.90 × 10⁻⁴
Co	2020	1.13 × 10⁻⁴	4.21 × 10⁻⁵	1.63 × 10⁻⁴	6.04 × 10⁻⁵	4.68 × 10⁻⁵	1.74 × 10⁻⁵	1.06 × 10⁻⁴	3.94 × 10⁻⁵	1.33 × 10⁻⁴	4.95 × 10⁻⁵
Co	2021	1.31 × 10⁻⁴	4.85 × 10⁻⁵	1.68 × 10⁻⁴	6.23 × 10⁻⁵	7.89 × 10⁻⁵	2.93 × 10⁻⁵	1.31 × 10⁻⁴	4.85 × 10⁻⁵	1.65 × 10⁻⁴	6.14 × 10⁻⁵
Cu	2020	3.35 × 10⁻³	1.25 × 10⁻³	6.53 × 10⁻³	2.43 × 10⁻³	2.74 × 10⁻³	1.02 × 10⁻³	6.68 × 10⁻⁴	2.48 × 10⁻⁴	2.61 × 10⁻⁴	9.71 × 10⁻⁵
Cu	2021	4.98 × 10⁻³	1.85 × 10⁻³	7.77 × 10⁻³	2.88 × 10⁻³	2.79 × 10⁻³	1.03 × 10⁻³	1.21 × 10⁻³	4.51 × 10⁻⁴	2.69 × 10⁻³	9.98 × 10⁻⁴
Cr	2020	7.72 × 10⁻³	2.87 × 10⁻³	8.58 × 10⁻³	3.19 × 10⁻³	7.13 × 10⁻³	2.65 × 10⁻³	3.95 × 10⁻³	1.47 × 10⁻³	2.76 × 10⁻³	1.03 × 10⁻³
Cr	2021	8.06 × 10⁻³	2.99 × 10⁻³	8.51 × 10⁻³	3.16 × 10⁻³	8.09 × 10⁻³	3.00 × 10⁻³	3.60 × 10⁻³	1.34 × 10⁻³	3.45 × 10⁻³	1.28 × 10⁻³
Cd	2020	5.35 × 10⁻³	1.99 × 10⁻³	5.23 × 10⁻³	1.94 × 10⁻³	4.54 × 10⁻³	1.69 × 10⁻³	1.80 × 10⁻³	6.69 × 10⁻⁴	4.07 × 10⁻³	1.51 × 10⁻³
Cd	2021	7.22 × 10⁻³	2.68 × 10⁻³	6.31 × 10⁻³	2.34 × 10⁻³	5.35 × 10⁻³	1.99 × 10⁻³	1.89 × 10⁻³	7.03 × 10⁻⁴	4.36 × 10⁻³	1.62 × 10⁻³
Mo	2020	5.67 × 10⁻⁴	2.11 × 10⁻⁴	9.37 × 10⁻⁵	3.48 × 10⁻⁵	2.88 × 10⁻⁴	1.07 × 10⁻⁴	3.55 × 10⁻⁴	1.32 × 10⁻⁴	1.13 × 10⁻⁴	4.21 × 10⁻⁵
Mo	2021	7.64 × 10⁻⁴	2.84 × 10⁻⁴	3.70 × 10⁻⁴	1.37 × 10⁻⁴	2.32 × 10⁻⁴	8.61 × 10⁻⁵	1.01 × 10⁻³	3.75 × 10⁻⁴	2.98 × 10⁻⁴	1.11 × 10⁻⁴

Table 11

Hazard quotient (HQ) and hazard index (HI) of As, Cd, Co, Cr, Cu, Mo, Ni, and Pb considering the consumption of Prochilodus lineatus by children (8 years) and adults (50 years).

Element	Year of Collection	Anhanduí River-1		Anhanduí River-2		Anhanduí River-3		Pardo River		Lontra River
Element	Year of Collection	Children	Adults	Children	Adults	Children	Adults	Children	Adults	Children	Adults
As	2020	1.668	<1	5.926	2.201	3.263	1.212	1.537	<1	1.816	<1
As	2021	2.186	<1	5.901	2.192	3.616	1.343	2.063	<1	1.512	<1
Cd	2020	27.123	10.074	41.425	15.386	30.082	11.173	19.134	7.107	27.370	10.166
Cd	2021	28.603	10.624	46.110	17.126	36.247	13.463	18.099	6.722	23.474	8.719
Co	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Co	2021	<1	<1	1.118	<1	1.479	<1	<1	<1	<1	<1
Cr	2020	2.573	<1	2.860	1.062	2.375	<1	1.315	<1	<1	<1
Cr	2021	2.688	<1	2.836	1.053	2.696	1.001	1.200	<1	1.151	<1
Cu	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Cu	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Mo	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Mo	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Ni	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Ni	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Pb	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Pb	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
HI	2020	32.608	12.112	51.637	19.179	36.947	13.723	22.951	8.5246	31.745	11.791
HI	2021	35.054	13.02	57.562	21.38	44.154	16.4	22.675	8.4221	27.837	10.339

Table 12

Hazard quotient (HQ) and hazard index (HI) of As, Cd, Co, Cr, Cu, Mo, Ni, and Pb considering the consumption of Pimelodus maculatus by children (8 years) and adults (50 years).

Element	Year of Collection	Anhanduí River-1		Anhanduí River-2		Anhanduí River-3		Pardo River		Lontra River
Element	Year of Collection	Children	Adults	Children	Adults	Children	Adults	Children	Adults	Children	Adults
As	2020	1.003	<1	2.301	0.855	2.729	1.014	<1	<1	3.444	1.279
As	2021	2.055	<1	3.625	1.346	1.660	<1	<1	<1	1.142	<1
Cd	2020	53.507	19.874	52.274	19.416	45.370	16.852	18.000	6.686	40.685	15.112
Cd	2021	72.247	26.834	63.123	23.446	53.507	19.874	18.937	7.034	43.644	16.211
Co	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Co	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Cr	2020	2.573	<1	2.860	1.062	2.375	<1	1.315	<1	<1	<1
Cr	2021	2.688	<1	2.836	1.053	2.696	1.001	1.200	<1	1.151	<1
Cu	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Cu	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Mo	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Mo	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Ni	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Ni	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Pb	2020	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
Pb	2021	<1	<1	<1	<1	<1	<1	<1	<1	<1	<1
HI	2020	58.082	21.573	58.697	21.802	51.207	19.02	20.135	7.4788	45.672	16.964
HI	2021	78.196	29.044	71.129	26.419	58.714	21.808	21.38	7.9411	46.838	17.397

Table 13

Carcinogenic risk for children and adults when consuming Prochilodus lineatus and Pimelodus maculatus.

*Prochilodus lineatus*
Element	Year of Collection	Anhanduí River-1		Anhanduí River-2		Anhanduí River-3		Pardo River		Lontra River
Element	Year of Collection	Children	Adults	Children	Adults	Children	Adults	Children	Adults	Children	Adults
As	2020	7.51 × 10⁻⁴	2.79 × 10⁻⁴	2.67 × 10⁻³	9.90 × 10⁻⁴	1.47 × 10⁻³	5.45 × 10⁻⁴	6.92 × 10⁻⁴	2.57 × 10⁻⁴	8.17 × 10⁻⁴	3.04 × 10⁻⁴
As	2021	9.84 × 10⁻⁴	3.65 × 10⁻⁴	2.66 × 10⁻³	9.86 × 10⁻⁴	1.63 × 10⁻³	6.04 × 10⁻⁴	9.28 × 10⁻⁴	3.45 × 10⁻⁴	6.81 × 10⁻⁴	2.53 × 10⁻⁴
Pb	2020	5.64 × 10⁻⁶	2.09 × 10⁻⁶	8.01 × 10⁻⁶	2.97 × 10⁻⁶	5.03 × 10⁻⁶	1.87 × 10⁻⁶	7.94 × 10⁻⁶	2.95 × 10⁻⁶	4.99 × 10⁻⁶	1.85 × 10⁻⁶
Pb	2021	6.87 × 10⁻⁶	2.55 × 10⁻⁶	8.93 × 10⁻⁶	3.32 × 10⁻⁶	5.72 × 10⁻⁶	2.13 × 10⁻⁶	9.43 × 10⁻⁶	3.50 × 10⁻⁶	6.02 × 10⁻⁶	2.23 × 10⁻⁶
Cu	2020	3.16 × 10⁻⁵	1.18 × 10⁻⁵	4.86 × 10⁻⁵	1.81 × 10⁻⁵	2.62 × 10⁻⁵	9.73 × 10⁻⁶	1.13 × 10⁻⁵	4.20 × 10⁻⁶	3.86 × 10⁻⁶	1.43 × 10⁻⁶
Cu	2021	3.33 × 10⁻⁵	1.24 × 10⁻⁵	7.71 × 10⁻⁵	2.86 × 10⁻⁵	2.31 × 10⁻⁵	8.57 × 10⁻⁶	5.47 × 10⁻⁶	2.03 × 10⁻⁶	2.98 × 10⁻⁶	1.11 × 10⁻⁶
Cr	2020	3.96 × 10⁻³	1.47 × 10⁻³	4.40 × 10⁻³	1.63 × 10⁻³	3.59 × 10⁻³	1.33 × 10⁻³	1.86 × 10⁻³	6.91 × 10⁻⁴	2.40 × 10⁻³	8.93 × 10⁻⁴
Cr	2021	4.43 × 10⁻³	1.64 × 10⁻³	5.24 × 10⁻³	1.95 × 10⁻³	3.35 × 10⁻³	1.25 × 10⁻³	2.02 × 10⁻³	7.51 × 10⁻⁴	2.49 × 10⁻³	9.25 × 10⁻⁴
Cd	2020	1.03 × 10⁻³	3.83 × 10⁻⁴	1.57 × 10⁻³	5.85 × 10⁻⁴	1.14 × 10⁻³	4.25 × 10⁻⁴	7.27 × 10⁻⁴	2.70 × 10⁻⁴	1.04 × 10⁻³	3.86 × 10⁻⁴
Cd	2021	1.09 × 10⁻³	4.04 × 10⁻⁴	1.75 × 10⁻³	6.51 × 10⁻⁴	1.38 × 10⁻³	5.12 × 10⁻⁴	6.88 × 10⁻⁴	2.55 × 10⁻⁴	8.92 × 10⁻⁴	3.31 × 10⁻⁴
*Pimelodus maculatus*
Element	Year of Collection	Anhanduí River-1		Anhanduí River-2		Anhanduí River-3		Pardo River		Lontra River
Element	Year of Collection	Children	Adults	Children	Adults	Children	Adults	Children	Adults	Children	Adults
As	2020	4.51 × 10⁻⁴	1.68 × 10⁻⁴	1.04 × 10⁻³	3.85 × 10⁻⁴	1.23 × 10⁻³	4.56 × 10⁻⁴	1.07 × 10⁻⁴	3.98 × 10⁻⁵	1.55 × 10⁻³	5.76 × 10⁻⁴
As	2021	9.25 × 10⁻⁴	3.43 × 10⁻⁴	1.63 × 10⁻³	6.06 × 10⁻⁴	7.47 × 10⁻⁴	2.78 × 10⁻⁴	1.63 × 10⁻⁴	6.04 × 10⁻⁵	5.14 × 10⁻⁴	1.91 × 10⁻⁴
Pb	2020	1.07 × 10⁻⁵	3.97 × 10⁻⁶	1.29 × 10⁻⁵	4.78 × 10⁻⁶	1.01 × 10⁻⁵	3.75 × 10⁻⁶	2.58 × 10⁻⁶	9.58 × 10⁻⁷	2.87 × 10⁻⁶	1.07 × 10⁻⁶
Pb	2021	1.30 × 10⁻⁵	4.83 × 10⁻⁶	1.73 × 10⁻⁵	6.43 × 10⁻⁶	1.07 × 10⁻⁵	3.99 × 10⁻⁶	4.57 × 10⁻⁶	1.70 × 10⁻⁶	4.34 × 10⁻⁶	1.61 × 10⁻⁶
Cu	2020	2.85 × 10⁻⁵	1.06 × 10⁻⁵	5.55 × 10⁻⁵	2.06 × 10⁻⁵	2.33 × 10⁻⁵	8.64 × 10⁻⁶	5.68 × 10⁻⁶	2.11 × 10⁻⁶	2.22 × 10⁻⁶	8.25 × 10⁻⁷
Cu	2021	4.23 × 10⁻⁵	1.57 × 10⁻⁵	6.60 × 10⁻⁵	2.45 × 10⁻⁵	2.37 × 10⁻⁵	8.80 × 10⁻⁶	1.03 × 10⁻⁵	3.83 × 10⁻⁶	2.28 × 10⁻⁵	8.49 × 10⁻⁶
Cr	2020	3.86 × 10⁻³	1.43 × 10⁻³	4.29 × 10⁻³	1.59 × 10⁻³	3.56 × 10⁻³	1.32 × 10⁻³	1.97 × 10⁻³	7.33 × 10⁻⁴	1.38 × 10⁻³	5.13 × 10⁻⁴
Cr	2021	4.03 × 10⁻³	1.50 × 10⁻³	4.25 × 10⁻³	1.58 × 10⁻³	4.04 × 10⁻³	1.50 × 10⁻³	1.80 × 10⁻³	6.69 × 10⁻⁴	1.73 × 10⁻³	6.41 × 10⁻⁴
Cd	2020	2.03 × 10⁻³	7.55 × 10⁻⁴	1.99 × 10⁻³	7.38 × 10⁻⁴	1.72 × 10⁻³	6.40 × 10⁻⁴	6.84 × 10⁻⁴	2.54 × 10⁻⁴	1.55 × 10⁻³	5.74 × 10⁻⁴
Cd	2021	2.75 × 10⁻³	1.02 × 10⁻³	2.40 × 10⁻³	8.91 × 10⁻⁴	2.03 × 10⁻³	7.55 × 10⁻⁴	7.20 × 10⁻⁴	2.67 × 10⁻⁴	1.66 × 10⁻³	6.16 × 10⁻⁴

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Abstract

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This study aimed to assess the pollution levels, sources, ecological risk, and human health risks of metal(loid)s in water, sediment, and muscle tissue of Prochilodus lineatus and Pimelodus maculatus from rivers in the state of Mato Grosso do Sul, Brazil. The metal(loid)s content in river sediment, water, and fish tissue were determined by inductively coupled plasma optical emission spectrometry. Sediment pollution assessment was carried out by geo-accumulation index, contamination factor, enrichment factor, and pollution load index. There were significant differences in concentration values for Al, As, Cd, Co, Cr, Cu, Mo, Ni, Pb, and Hg. There was greater tendency for the elements Cu, Ni, Cu, N, Co, As, Hg, Al, and Co in the waters of the Anhanduí River in 2020 and Cr and Pb in 2021. The concentrations of As, Cd, Co, Cr, and Hg in the waters of the Anhanduí River are above the permitted limit values for heavy metal ions in drinking water established by the WHO. The concentrations of heavy metals in the sediments of rivers are above the limit set by Conama/Brazil and other countries. The sediments were very highly contaminated by Cd and Mo, and with moderate contamination of Pb. All sediments of rivers showed a decline in site quality, which indicates that it is polluted. Sediments were classified with severe enrichment by Cd and Mo. The content of Al was the highest in P. lineatus and P. maculatus in relation to other elements analyzed. There was also the presence of elements such as Cr, Cu, Cd, Hg, Ni, As, Pb, Mo, and Co in the tissues of the fish species. Therefore, the contamination of these rivers is a concern due to human consumption of fish, since there is a carcinogenic risk related mainly to As and Cd.

Details

Title

Assessment of the Risk to Human Health and Pollution Levels Due to the Presence of Metal(loid)s in Sediments, Water, and Fishes in Urban Rivers in the State of Mato Grosso do Sul, Brazil

Author

Fernandes, Melina Ribeiro¹; Melo Elaine Silva de Pádua²

; Ancel Marta Aratuza Pereira¹; Guimarães Rita de Cássia Avellaneda¹; Hiane, Priscila Aiko¹

; Geilow Karine de Cássia Freitas¹

; Bogo Danielle¹; Tschinkel Paula Fabiana Saldanha¹; Rosa Ana Carla Gomes¹

; Medeiros Cláudia Stela de Araújo¹

; Oliveira Rodrigo Juliano³

; Vilela Marcelo Luiz Brandão¹

; Garcia Diego Azevedo Zoccal¹

; Nascimento Valter Aragão do¹

¹ Group of Spectroscopy and Bioinformatics Applied to Biodiversity and Health (GEBABS), Faculty of Medicine, Federal University of Mato Grosso do Sul (UFMS), Cidade Universitária, Campo Grande 79079-900, MS, Brazil; [email protected] (M.R.F.); [email protected] (E.S.d.P.M.); [email protected] (M.A.P.A.); [email protected] (R.d.C.A.G.); [email protected] (P.A.H.); [email protected] (K.d.C.F.G.); [email protected] (D.B.); [email protected] (P.F.S.T.); [email protected] (A.C.G.R.); [email protected] (C.S.d.A.M.); [email protected] (M.L.B.V.); [email protected] (D.A.Z.G.)
² Group of Spectroscopy and Bioinformatics Applied to Biodiversity and Health (GEBABS), Faculty of Medicine, Federal University of Mato Grosso do Sul (UFMS), Cidade Universitária, Campo Grande 79079-900, MS, Brazil; [email protected] (M.R.F.); [email protected] (E.S.d.P.M.); [email protected] (M.A.P.A.); [email protected] (R.d.C.A.G.); [email protected] (P.A.H.); [email protected] (K.d.C.F.G.); [email protected] (D.B.); [email protected] (P.F.S.T.); [email protected] (A.C.G.R.); [email protected] (C.S.d.A.M.); [email protected] (M.L.B.V.); [email protected] (D.A.Z.G.), Faculty of Medicine, State University of Mato Grosso do Sul, Dourados 79804-970, MS, Brazil
³ Stem Cell, Cell Therapy and Toxicological Genetics Research Centre (CeTroGen), Medical School, Federal University of Mato Grosso do Sul (UFMS), Cidade Universitária, Campo Grande 79079-900, MS, Brazil; [email protected]

First page

114

Publication year

2025

Publication date

2025

Publisher

MDPI AG

e-ISSN

24138851

Source type

Scholarly Journal

Language of publication

English

DOI

https://doi.org/10.3390/urbansci9040114

ProQuest document ID

3194648923