Deposition of Potentially Toxic Metals in the Soil from Surrounding Cement Plants in a Karst Area of Southeastern Brazil

Abstract

Cement factories are the main sources of environmental pollutants among the different industrial activities, including soil contamination by potentially toxic metals. The karst region of Southeastern Brazil is known for the implementation of large cement producing facilities. This study aims to evaluate whether there is an increase in the concentration of PTM in the soil surrounding the cement plants and to estimate their harmfulness to both local human population and environment. In total, 18 soil samples were collected from the surroundings of three cement plants as well as four soil samples from areas outside the influence of cement plants and concentration of the following potentially toxic metals (PTM) were estimated: Cd, Pb, Co, Cu, Cr, Mn, Ni, and Zn. The results revealed that all PTM concentrations from cement plant surroundings were significantly higher than PTM concentrations from control areas and no PTM concentrations from CPS or CA soil samples exceeded national and global contamination thresholds. However, Igeo Index indicated low level soil contamination by Pb, Cu, and Cr, as well as high levels for Co. We could not verify significant non-carcinogenic risk to health for any soil sample, but carcinogenic risk analysis revealed different levels of carcinogenic risk among the sampled locations, for both adults and children. Our results indicate that exclusively evaluating the concentration of potentially toxic metals is not enough to verify the potential harmful effects of cement production for the surrounding population. Here we evidence that additional indices, based on both contamination indices and health risk assessments, should be considered for better evaluation of the impacts of cement production activity.

1. Introduction

Soils are remarkable systems, constituted of an extraordinarily diverse range of mineral and organic components, organized and interactive in particular ways that result in the delivery of the range of ecosystem services, contributing to basic human needs such as food, water, and air supply [1,2]. Soil ecosystem services depend on soil properties and their interactions, and are mostly influenced by its use and management [3]. The intensification and expansion of human activities has increased the pressure on land resources and led to soil degradation [4]. One of the main concerns regarding the impact of human activities in soil systems are soil contamination events by potentially toxic metals (PTM), since they pose alarming threats to agricultural productivity, food safety, and human health [5]. Potentially toxic metals (PTM)—the most widespread term for heavy metals—are those with high density (>5 g/cm³) compared to other elements and have an atomic number greater than 20. These metals are resistant to degradation and can accumulate in the components in which they manifest their toxicity [6].

Unlike organic pollutants, PTM cannot be biodegraded and, mainly due to their cumulative power in living organisms, pose risks to health and to the environment [7,8]. Moreover, PTM can remain in the soil for long periods, depending on soil retention capacity and physical-chemical properties [9,10]. Soil contamination by PTM is usually the result of anthropogenic activities related to urbanization, including automotive exhaust pipe and industrialization [11,12]. Cement plants are one of the most common sources of PTM pollution by gas emissions and production of cement powder [13].

The cement industry has a high polluting potential at all stages of production [14]. The levels and characteristics of pollutant emissions depend on the technological and operational characteristics of the industrial process, especially rotary kiln furnaces, the chemical and mineralogical composition of raw materials, the chemical composition of the fuels used; the operational speed of kiln furnaces, and the efficiency of the emission control systems of installed pollutants [15]. The primary pollutants emitted in the cement manufacturing process are particulate matter, carbon dioxide, sulfuroxides, and nitrogen oxides [16]. According to the U.S. environmental agency, cement manufacturing plants are among the largest sources of hazardous pollutant emissions, including PTM [17,18]. Significant parts of these pollutants are deposited in the soil, including the burning of fuels for the kiln furnaces, generating fine dust particles that are deposited in the soil [19]. This dust contains PTM that are deposited in the soil and cause serious environmental and health impacts since it is not biodegraded, therefore, accumulating [20].

About 2–3% of the Brazilian territory is formed by karst environments, structured in 19 karst regions [21]. These regions are characterized by vast areas of sedimentary carbonate rocks, with limestone, dolomite rock, and marbles being the most common components. Due to calcareous composition, these regions in Brazil are commonly used for limestone exploitation for use in agriculture, and also as an input in the manufacturing process of Portland cement, in which it is common to install this type of facility in the karstic regions of Brazil [21]. This study was carried out in an area located at the southern portion of one of the largest Brazilian karst regions (called Grupo Bambuí), in southeastern Brazil. This area represents a mosaic of environments characterized by areas used for agricultural production, limestone mining, small urban settlements, and presence of cement plants [22].

Here, we hypothesized that cement production in the study area leads to the deposition of PTM in its surroundings and that these events of increasing in PTM concentrations can be potentially harmful to vicinal human population of the cement plants. Thus, our main goal is to evaluate whether there is an increase in the concentration of PTM in the soil surrounding the cement plants and to estimate their harmfulness to both local human population and environment, applying worldwide used indices. This investigation also aims to provide evidence that conventional strategies for estimating of soil contamination by cement production plants adopted by local regulatory agencies are not sufficient to estimate the risks of PTM soil contamination to human health.

2. Materials and Methods

2.1. Sampling and Quantification of Potentially Toxic Metals in the Soil

The study area comprises the southern portion of the widest karstic region in Brazil, called Grupo Bambuí, located in the southeast region of Brazil (Figure 1). In this area, soil samples were collected from the surroundings of three Portland Cement plants (named CPS1, CPS2 and CPS3), and also soil samples in two agricultural production areas located outside the influence of cement production plants (10 km far from CPSs) taken as control areas (CA). Six sampling points were selected around each cement production plant (CPS), in which each point presented a plant distance of less than 500 m (a circular scheme). In each control area, two sampling points were selected. The samples were collected in a single round, performed in May 2020 (dry season). In each sampling point, approximately 2000 g of surface soil was collected with depth between 0 and 15 cm, following procedures described by Pacchioni et al. [23].

Concentration of the following potentially toxic metals (PTM) were estimated in soil samples: Cd, Pb, Co, Cu, Cr, Mn, Ni, and Zn. The quantification of heavy metals was performed following the methodology of air-acetylene flame atomic absorption spectrometry proposed by USEPA 3050B [24] and USEPA 3051A [25]. All quantifications were performed by a laboratory facility certified by local regulatory agencies (Oceanus-Hidroquímica Laboratory, Rio de Janeiro, Brazil, certification code: UN015590/55.11.10).

2.2. Analysis of Potentially Toxic Metals Concentrations in the Soil

Soil PTM contamination analyses were performed using the following internationally recognized indices: Enrichment Factor (EF) and Geoaccumulation Index (Igeo). In addition to the indexes, raw data about PTM concentration were also included to compare them with previous studies and also to compare with soil PTM contamination limits established in both Brazilian (CONAMA No. 420/09) [26] and local (COPAM No. 166/11) [27] laws.

The Enrichment Factor (EF) was used to evaluate the degree of enrichment of PTM in soil. EF is used to assess the level of human impact, by a differentiation anthropogenic source from natural sources of PTM [28]. The EF value near to unity indicates natural origin; those less than unity suggests possible mobilization/depletion of metal, while EF value greater than unity recommends that the element is of anthropogenic origin [6]. EF index was calculated by Equation (1), as follows, where Ci is the concentration of individual elements in soil (mg/kg); CRef is the concentration of reference element for normalization (mg/kg). In this study, Fe is used as a reference element, so that Fe concentration was determined for all soil samples to perform EF calculations.

EF = (C_i/C_Ref)_soil/(C_i/C_Ref)_background

(1)

The Geoaccumulation Index (Igeo) was calculated to estimate the degree of soil pollution by a given PTM, comparing observed PTM concentration with its reference concentration, proposed by Muller [29]. Additionally, Igeo index was ranked in seven classes of soil pollution, described in Mohammadi et al. [30]. Igeo was calculated by Equation (2), as follows, where Ci is the PTM concentration in soil samples, and Bi is the background concentration of these elements. Background values (Bi) used in this study were based on reference values proposed for carbonate sedimentary rocks by Turekian and Wedepohl [31] and they are presented in the Supplementary Materials, in Table S1.

$${\mathrm{I}}_{\mathrm{geo}}={\log }_2\left(\frac{Ci}{1.5\times Bi}\right)$$

(2)

We performed non-paired Wilcoxon tests to compare PTM concentration as well as adopted contamination indices (EF and Igeo) between the CPS and CA soil samples, using R statistical program (R version 3.3.2, R Core Team, Vienna, Austria).

2.3. Health Risk Assessment

In this study, non-carcinogenic health risks assessments (NCR) for CPS vicinal human populations by soil PTM contamination was estimated using USEPA health risk methods for oral, dermal, and contact pathways [32]. First, the Average Daily Dose (ADD) in milligrams per kilogram per day values of PTM through oral, dermal, and inhalation pathways was calculated using Equations (3)–(5), respectively. References’ parameters for both adult and children exposure are presented in

Table 1. Assessment of heavy metal pollution and risks to human health.

Factor	Definition	Unit	Children	Adult	Reference
C	Heavy metal concentration	mg/kg	-	-	-
IngR	Ingestion rate	mg/day	100	50	[6]
EF	Exposure frequency	days/year	320	320	[6]
ED	Exposure duration	years	6	24	[6]
BW	Body weight	kg	18.6	80	[6]
AT	Average time	days	ED × 365	ED × 365	[6]
InhR	Inhalation rate	m3/kg	5	20	[6]
PEF	Particle emission factor	m3/kg	1.36 × 109	1.36 × 109	[6]
SA	Exposed skin surface area	cm2	2699	3950	[6]
AF	Skin adherence factor	(mg/cm) day	0.2	0.07	[6]
ABS	Dermal absorption factor	unitless	0.001	0.001	[6]
CF	Conversion factor	kg/mg	1 × 10−6	1 × 10−6	[6]

.

$${\mathrm{ADD}}_{\mathrm{ing}}=\mathrm{C}\times \frac{IngR \times EF \times ED \times CF}{BW \times AT}$$

(3)

$${\mathrm{ADD}}_{\mathrm{derm}}=\mathrm{C}\times \frac{SA \times SL \times ABS \times EF \times ED \times EF}{BW \times AT}$$

(4)

$${\mathrm{ADD}}_{\mathrm{inh}}=\mathrm{C}\times \frac{InhR \times EF \times ED}{PEF \times BW \times AT}$$

(5)

As a second step, ADDs were used to calculate the Hazard Quotient (HQ) by dividing the daily exposure doses (ADDing, ADDinh, and ADDderm) for each PTM with its corresponding reference doses (RfD) (mg/kg⁻¹ × day⁻¹). Adopted RfDs and calculated ADDs values for the eight PTM were presented in Tables S2 and S3, respectively. Then, to estimate the non-carcinogenic risks of PTM for humans (NCR), we calculated the Hazard Index (HI) which corresponds to the sum of HQ indices: NCR = HI = ∑HQi. HI < 1 indicates that there are no significant risks of non-cancerous effect, and HI > 1 indicates a chance that non-carcinogenic effects may occur, with a probability that it tends to increase as HI value increases [33].

The carcinogenic risks to humans (CR) was estimated as described by Yadav et al. [6], which CR corresponds to the average daily doses (∑ADD) multiplied by respective slope factor (SF). A slope factor is an upper bound probability of an individual developing cancer as a result of a lifetime exposure to an agent by ingestion or inhalation. Adopted slope factors for the eight PTM were presented in Table S2. When CR < 10⁻⁶, no cancer risk exists. When 10⁻⁶ < CR < 10⁻⁴, the risk is within the acceptable range. When CR > 10⁻⁴, human tolerance is exceeded.

3. Results

Our first approach in this study was to compare PTM concentrations estimated for CPS and CA soil samples. The results of these comparative analyses revealed that all PTM concentrations from CPS were significantly higher than PTM concentrations from CA areas (Figure 2). Moreover, when we compared PTM concentrations between the three CPS (CPS1, CPS2 and CPS3), we could not verify significant differences in PTM concentrations between the three CPS, except for Cr element, in which soil samples from CPS3 presented values higher than CPS1 and CPS2 (Table S4).

Here, we also compared PTM concentrations from CPS soil samples with soil contamination thresholds established by local (COPAM No. 16/11) [26], national (CONAMA No. 420/09) [27] and global (WHO) recommendations [34]. The results revealed that several CPS soil samples exceeded local PTM contamination threshold for Co and Pb. However, no PTM concentrations from CPS or CA soil samples exceeded national and global contamination thresholds (Table S1). In addition, when we compared PTM concentrations estimated from CPS or CA soil samples with PTM concentration values reported for PTM soil contamination events worldwide by previous studies, we could observe that the levels of PTM concentration in CPS or CA soil samples were lower than those described in reported PTM soil contamination events (

Table 2. PTM concentrations in soil samples from this study and cities worldwide (mg/kg).

Soil	Cd	Pb	Co	Cu	Cr	Mn	Ni	Zn	City/Region, Country	Reference
CPS 1	0.06	19.25	3.86	9.26	28.33	318.33	4.07	21.13	Arcos, Brazil	This study
CPS 2	0.05	13.59	1.85	7.03	19.64	205.51	3.12	13.23	Arcos, Brazil	This study
CPS 3	0.06	21.04	5.92	10.87	35.53	490.76	4.77	27.02	Pains, Brazil	This study
Control	0.06	19.67	5.22	8.47	25.20	376.93	4.07	19.57	Pains, Brazil	This study
CPS	-	29.70	-	28.50	131.00	-	37.70	98.20	Rabigh, South Arabia	[9]
CPS	289.90	469.20	-	404.40	186.20	-	-	168.10	Sagamu, Nigeria	[17]
CPS	147.80	31.47	-	-	57.21	-	-	138.50	Kingston, Jamaica	[19]
CPS	-	19.30	-	5.03	76.40	466.00	29.10	10.10	Gombe, Nigeria	[35]
CPS	5.00	55.00	-	2.89	22.18	-	-	44.51	Qadissiya, Jordan	[36]
Agricultural soil	1.90	11.20	-	6.40	18.80	-	4.90	16.20	Pernanbuco, Brazil	[37]
Agricultural soil	0.06	2.69	-	2.14	55.66	6.86	0.91	3.56	Piauí, Brazil	[38]
Forest soil	0.05	1.79	-	0.96	28.17	6.20	0.62	0.35	Piauí, Brazil	[38]
Forest soil	0.60	10.40	0.20	12.10	44.20	-	13.50	30.40	Paraná, Brazil	[39]
Industrial area soil	0.70	41.00	19.00	25.00	60.00	546.00	24.00	70.00	Anyang, China	[40]
Industrial area soil	0.20	27.00	24.00	48.00	124.00	-	36.00	110.00	Jharia, India	[41]
Urban area soil	1.10	137.00	46.00	277.00	309.00	1870.00	121.00	1020.00	Four cities, Nepal	[6]
Urban area soil	1.50	803.00	11.00	34.00	31.00	803.00	21.00	331.00	Mazarron Town, Spain	[42]
Urban area soil	0.50	31.00	18.00	21.00	59.00	488.00	36.00	100.00	Jiaozuo, China	[43]
Roadside soil	3.10	59.00	33.00	266.00	34.00	-	32.00	507.00	Suva, Fiji	[44]

).

The results of our PTM enrichment analyses, estimated by the EF Index, revealed that the soil enrichment by PTM was superior in CPS areas when compared with control areas (CA) for all studied PTM (

Table 3. Calculated Enrichment Factor (EF) of PTM from CA and CPS soil samples.

PTM	CA				Soil Enrichment 1	CPS				Soil Enrichment 1	CA vs. CPS p-Value 2
	Min	Max	SD	Mean		Min	Max	SD	Mean
Cd	0.038	0.148	0.049	0.062	No	0.123	0.830	0.171	0.252	No	0.003
Pb	0.109	0.238	0.060	0.005	No	0.168	1.069	0.201	0.345	No	0.042
Co	0.698	1.523	0.395	0.006	No	0.878	30.33 3	6.745	6.207	High	0.007
Cu	0.142	0.253	0.049	0.018	No	0.180	0.952	0.180	0.386	No	0.019
Cr	0.134	0.280	0.062	0.223	No	0.162	0.987	0.198	0.424	No	0.010
Mn	0.011	0.023	0.005	0.018	No	0.013	0.161	0.031	0.050	No	0.003
Ni	0.013	0.026	0.006	0.021	No	0.014	0.092	0.017	0.034	No	0.042
Zn	0.045	0.085	0.018	0.061	No	0.045	0.567	0.115	0.170	No	0.003

¹ EF < 2, deficiency to minimal enrichment; ² < EF < 5, moderate enrichment; 5 < EF < 20, high enrichment; 20 < EF < 40, very high enrichment, and EF > 40, extremely high enrichment [29]. 2. Wilcoxon test, non-paired. ³ Just one soil sample presented very high enrichment.

). However, we could verify high enrichment level only for Co element in CPS soil samples (EF > 5), with a single sampling point showing a very high level of enrichment (EF > 20). Similarly, our Igeo analysis of soil contamination by PTM revealed that the levels of soil contamination in CPS soil samples were higher when compared with CA samples, for all PTM (Figure 3). Considering the mean values of Igeo Index, we did not verify significant contamination by Mn, Ni and Zn in both CPS and CA soil samples. Low level soil contamination were verified for Pb, Cu and Cr elements. However, Igeo Index for Co element showed varying degrees of contamination between soil samples, ranging from moderate to extreme level of soil contamination (Figure 3).

Our non-carcinogenic health risk (NCR) analyses, estimated by Hazard Quotient (HQs) and Hazard Index (HI) calculations, revealed that for all sampled locations (CPS1, CPS2, CPS3 and CA), we could not verify significant risk to health (HI > 1), for all studied PTM. Still, similar NCR results were verified for both adults and children estimates (

Table 4. Calculated enrichment factor (EF) of PTM from CA and CPS soil samples.

Sampling Site	PTM	HQing		HQinh		HQderm		HI		NCR 1
		Children	Adult	Children	Adult	Children	Adult	Children	Adult
CPS1	Cd	2.83 × 10−10	1.32 × 10−10	1.04 × 10−16	3.87 × 10−16	1.53 × 10−12	7.27 × 10−13	2.84 × 10−10	1.32 × 10−10	No
	Pb	3.18 × 10−7	1.48 × 10−7	1.75 × 10−11	6.52 × 10−11	1.72 × 10−9	8.22 × 10−10	3.19 × 10−7	1.49 × 10−7	No
	Co	1.82 × 10−7	8.48 × 10−8	1.07 × 10−11	3.99 × 10−11	5.62 × 10−13	2.68 × 10−13	1.82 × 10−7	8.49 × 10−8	No
	Cu	1.75 × 10−6	8.13 × 10−7	1.93 × 10−11	7.17 × 10−11	9.43 × 10−9	4.49 × 10−9	1.76 × 10−6	8.17 × 10−7	No
	Cr	4.01 × 10−7	1.86 × 10−7	2.95 × 10−13	1.10 × 10−12	2.06 × 10−11	9.82 × 10−12	4.01 × 10−7	1.86 × 10−7	No
	Mn	6.90 × 10−5	3.21 × 10−5	1.02 × 10−10	3.78 × 10−10	1.16 × 10−10	5.52 × 10−11	6.90 × 10−5	3.21 × 10−5	No
	Ni	3.84 × 10−7	1.78 × 10−7	3.81 × 10−12	1.42 × 10−11	2.13 × 10−9	1.02 × 10−9	3.86 × 10−7	1.79 × 10−7	No
	Zn	2.99 × 10−5	1.39 × 10−5	2.20 × 10−10	8.17 × 10−10	1.61 × 10−7	7.68 × 10−8	3.00 × 10−5	1.40 × 10−5	No
CPS2	Cd	2.36 × 10−10	1.10 × 10−10	8.66 × 10−17	3.22 × 10−16	1.27 × 10−12	6.06 × 10−13	2.37 × 10−10	1.10 × 10−10	No
	Pb	2.24 × 10−7	1.04 × 10−7	1.24 × 10−11	4.60 × 10−11	1.22 × 10−9	5.80 × 10−10	2.25 × 10−7	1.05 × 10−7	No
	Co	8.75 × 10−8	4.07 × 10−8	5.15 × 10−12	1.91 × 10−11	2.70 × 10−13	1.28 × 10−13	8.75 × 10−8	4.07 × 10−8	No
	Cu	1.33 × 10−6	6.17 × 10−7	1.46 × 10−11	5.44 × 10−11	7.16 × 10−9	3.41 × 10−9	1.33 × 10−6	6.20 × 10−7	No
	Cr	2.78 × 10−7	1.29 × 10−7	2.04 × 10−13	7.60 × 10−13	1.43 × 10−11	6.81 × 10−12	2.78 × 10−7	1.29 × 10−7	No
	Mn	4.46 × 10−5	2.07 × 10−5	6.55 × 10−11	2.44 × 10−10	7.48 × 10−11	3.56 × 10−11	4.46 × 10−5	2.07 × 10−5	No
	Ni	2.94 × 10−7	1.37 × 10−7	2.92 × 10−12	1.08 × 10−11	1.63 × 10−9	7.78 × 10−10	2.95 × 10−7	1.37 × 10−7	No
	Zn	1.87 × 10−5	8.70 × 10−6	1.38 × 10−10	5.12 × 10−10	1.01 × 10−7	4.81 × 10−8	1.88 × 10−5	8.75 × 10−6	No
CPS3	Cd	2.90 × 10−4	1.35 × 10−10	1.07 × 10−16	3.97 × 10−16	1.57 × 10−12	7.46 × 10−13	2.90 × 10−4	1.36 × 10−10	No
	Pb	2.83 × 10−2	1.61 × 10−7	1.91 × 10−11	7.12 × 10−11	1.88 × 10−9	8.98 × 10−10	2.83 × 10−2	1.62 × 10−7	No
	Co	2.79 × 10−3	1.30 × 10−7	1.64 × 10−11	6.11 × 10−11	8.61 × 10−13	4.10 × 10−13	2.79 × 10−3	1.30 × 10−7	No
	Cu	1.28 × 10−3	9.53 × 10−7	2.26 × 10−11	8.41 × 10−11	1.11 × 10−8	5.27 × 10−9	1.28 × 10−3	9.58 × 10−7	No
	Cr	5.58 × 10−2	2.34 × 10−7	3.69 × 10−13	1.37 × 10−12	2.59 × 10−11	1.23 × 10−11	5.58 × 10−2	2.34 × 10−7	No
	Mn	5.03 × 10-2	4.95 × 10-5	1.56 × 10-10	5.82 × 10-10	1.79 × 10-10	8.51 × 10-11	5.03 × 10-2	4.95 × 10-5	No
	Ni	1.12 × 10-3	2.09 × 10-7	4.46 × 10-12	1.66 × 10-11	2.50 × 10-9	1.19 × 10-9	1.12 × 10-3	2.10 × 10-7	No
	Zn	4.24 × 10-4	1.78 × 10-5	2.81 × 10-10	1.04 × 10-9	2.06 × 10-7	9.82 × 10-8	4.25 × 10-4	1.79 × 10-5	No
CA	Cd	4.83 × 10−10	2.24 × 10−10	1.77 × 10−16	6.60 × 10−16	2.60 × 10−12	1.24 × 10−12	4.85 × 10−10	2.26 × 10−10	No
	Pb	4.50 × 10−7	2.09 × 10−7	2.48 × 10−11	9.23 × 10−11	2.44 × 10−9	1.16 × 10−9	4.52 × 10−7	2.10 × 10−7	No
	Co	3.32 × 10−7	1.54 × 10−7	1.95 × 10−11	7.26 × 10−11	1.02 × 10−12	4.87 × 10−13	3.32 × 10−7	1.54 × 10−7	No
	Cu	3.15 × 10−6	1.47 × 10−6	3.48 × 10−11	1.29 × 10−10	1.70 × 10−8	8.11 × 10−9	3.17 × 10−6	1.47 × 10−6	No
	Cr	4.28 × 10−7	1.99 × 10−7	3.15 × 10−13	1.17 × 10−12	2.20 × 10−11	1.05 × 10−11	4.28 × 10−7	1.99 × 10−7	No
	Mn	1.37 × 10−4	6.35 × 10−5	2.01 × 10−10	7.47 × 10−10	2.29 × 10−10	1.09 × 10−10	1.37 × 10−4	6.35 × 10−5	No
	Ni	6.06 × 10−7	2.82 × 10−7	6.01 × 10−12	2.24 × 10−11	3.37 × 10−9	1.60 × 10−9	6.09 × 10−7	2.83 × 10−7	No
	Zn	6.73 × 10−5	3.13 × 10−5	4.95 × 10−10	1.84 × 10−9	3.63 × 10−7	1.73 × 10−7	6.76 × 10−5	3.15 × 10−5	No

Note: ¹ HI > 1, which may be concerning non-carcinogenic health risks [33].

). On the other hand, carcinogenic risk analysis (CR) revealed different levels of carcinogenic risk (CR) among the sampled locations (CPS1, CPS2, CPS3 and CA), for both adults and children (

Table 5. Indices of carcinogenic risks (CR) for the PTM Cd, Pb, Co, Cr, and Ni, including indication of potential carcinogenic health risks.

Sampling Site	PTM	∑CR
		Children	Potential Risk 1	Adult	Potential Risk 1
CPS1	Cd	2.00 × 10−6	Low	9.33 × 10−7	NS
	Pb	2.56 × 10−5	Low	1.19 × 10−5	Low
	Co	1.80 × 10−4	High	8.36 × 10−5	Low
	Cr	5.64 × 10−3	High	2.62 × 10−3	High
	Ni	1.62 × 10−5	Low	7.54 × 10−6	Low
CPS2	Cd	1.67 × 10−6	Low	7.77 × 10−7	NS
	Pb	1.80 × 10−5	Low	8.39 × 10−6	Low
	Co	8.62 × 10−5	Low	4.01 × 10−5	Low
	Cr	3.91 × 10−3	High	1.82 × 10−3	High
	Ni	1.24 × 10−5	Low	5.77 × 10−6	Low
CPS3	Cd	2.06 × 10−6	Low	9.56 × 10−7	NS
	Pb	2.79 × 10−5	Low	1.30 × 10−5	Low
	Co	2.75 × 10−4	High	1.28 × 10−4	High
	Cr	7.07 × 10−3	Low	3.29 × 10−3	High
	Ni	1.90 × 10−5	Low	8.83 × 10−6	Low
CA	Cd	3.42 × 10−6	Low	1.59 × 10−6	Low
	Pb	3.62 × 10−5	Low	1.68 × 10−5	Low
	Co	3.27 × 10−4	High	1.52 × 10−4	High
	Cr	6.03 × 10−3	High	2.80 × 10−3	High
	Ni	2.56 × 10−5	Low	1.19 × 10−5	Low

Note: ¹ CR < 10⁻⁶, 10⁻⁶ > RI > 10⁻⁴, and CR > 10⁻⁴ indicates non-significative (NS), low and high cancer risk, respectively [30].

). In addition, the five PTMs, which were possible to perform the CR analysis (Cd, Pb, Co, Cr and Ni), also presented distinct levels of CR among the sampled locations where soil were accessed (Table 5).

4. Discussion

Several studies reporting events of soil enrichment contamination by PTM in Brazilian territory have been published recently: Brito et al. [38] also estimated PTM concentration in soils from areas under agricultural exploration and natural Cerrado vegetation, but in northeast region; Silva et al. [37] verified and differentiated the sources of emission of PTMs in soils used for sugarcane cultivation in northeast region; Smidt et al. [45] identified potential sources of pollution by PTMs in soils highly influenced by a phosphorus fertilizer factory. However, this is the first study performed in Brazil which focused on estimating potential soil PTM contamination caused by cement plants’ operation and their potential health risks to local human population. Some studies have already been published relating concerning events of soil contamination by PTM and the anthropic activity of cement production in some regions of the world, reporting events of PTM soil contamination more severe than those observed in this study (Table 2), which is probably related to the fact that these previous studies have been performed in countries whose laws about gas emissions as well as soil contamination by PTM are less restrictive than in Brazil [9,17,20,38,39]. On the other hand, when considering studies on PTM contamination events in general, China is the country where most of these studies have been reported, indicating that soils from areas of intense urban and industrial activity are severely contaminated by PTM, creating alarming risks to the environment and the health of local populations [6,40,41,42,43].

In this study, we hypothesized that PTM concentration around the cement plants would be higher than in control areas, which was in accordance with our findings, even at moderate levels when compared with other similar studies [9,17,19,35,36], and also with the concentration thresholds of PTM recommended by local and national regulatory laws as well as WHO recommendations [26,27,34]. On the other hand, when we accessed the status of PTM contamination not by PTM concentration solely, but by applying contamination (Igeo) and enrichment (EF) indices, these parameters could indicate that some PTM contamination presented above the “negligible status”, attributing environmental concerns to soil contamination in cement plant surroundings which are operating in the study area. Thus, we consider that our results constitute strong evidence of the need to incorporate the contamination and enrichment indices (Igeo and EF) not only in instruments of risk assessment to the environmental contamination by local environmental agencies, but also as a tool for monitoring programs of PTM pollution to be incorporated in Environmental Management Systems of cement industries.

PTMs can be introduced in soil environment by natural routes, such as volcanic activities and weathering of rocks, or by anthropogenic disturbances [46,47]. The entry of PTMs into the ecosystem via the food chain can collapse the ecosystem since they affect the biodegradability of organic pollutants and magnify their toxic effects; change soil properties such as pH and porosity and can disrupt the taxonomic and functional structure of biological communities that maintain part of the ecosystem services provided by the soil [48,49,50]. In addition to interfering in the ecosystem, PTMs also directly influence people’s health, causing inhibition of enzymatic activities, altering protein synthesis, nucleic acid functions and changes in membrane permeability, cause lipid peroxidation, dehydration of sulfhydryl proteins, along with other effects [51,52].

In our Igeo results, we found moderate to extreme soil contamination by cobalt, since observed concentrations of this metal were higher than the reference values defined for sedimentary carbonatic rocks which form the geological context of the study area [31]. Natural occurrence of cobalt is highly concentrated in mafic rocks as well as in black shales, commonly forming minerals with S, As and Se, such as cobaltite, smaltite, linneite, and arsenosulfide. In soils, high level of Co were found in loamy (Cambisols) and in organic (Histosols) soils [53]. Events of soil contamination by cobalt has been associated with mining and smelting activity, fertilizer use, and sewage sludge spreading [54], and this study represents the first record of soil contamination by cobalt in studies focused on soils from cement plant surroundings. Although cobalt is considered a plant micronutrient (component of several enzymes and co-enzymes), it has been shown to affect growth and metabolism of plants, depending on the concentration and status of cobalt in rhizosphere and soil [55]. In addition to harmful effects on plants, soil contamination events by Cobalt are also associated with disturbances in the soil microbiota [56,57,58]. Cobalt contamination has direct interactions with human health, with skin and respiratory issues [59]. Cobalt has been noted to have a high affinity to the sulphydryl group, thus causing inhibition of crucial enzymes [60]. Moreover, it has also been linked to carcinogenic effects, possibly related to the evidence that cobalt interferes in the process of DNA repair and can cause direct induction of DNA-protein crosslinking DNA damage and sister-chromatid, as well as evidences of cobalt-mediated free radicals formation [61]. Here, we also verified low levels of soil contamination by lead, copper and chromium in soil samples from cement plant surroundings. Small particles of inorganic lead can be absorbed through the respiratory and gastrointestinal tract, and chronic exposure to lead contributes to alterations in hormonal and neuronal systems, toxicity in renal cells and affects the hematopoietic system [52]. Chromium, which is not absorbed through the lungs, may then enter the gastrointestinal tract, primarily absorbed in the jejunum. Toxicity mechanism and carcinogenicity of chromium is a complex process, including higher redox potential, free radicals production and DNA lesions [62]. Oral intake of copper may cause hepatic and kidney disease, including Wilson’s disease, related to copper accumulation in organs instead of being excreted by bile [63]. In addition to the harmful effects of these PTMs on human health, there are strong evidences that events of soil contamination by these three MTPs are related to disturbances of the soil ecosystem, which is related to deterioration of soil quality [64,65,66,67,68].

Our Carcinogenetic Risks (CR) estimates showed significant carcinogenic risks for children related to soil contamination by chromium and cobalt in all sampled locations, with the exception of two sampling points in CPS2 and CPS3. Considering the estimated CR for adults, risks for chromium were also detected, and the other PTMs (Co, Pb, Ni, and Cd) presented low or non-significant risks [69]. Similar results were also observed in previous studies performed in Bangladesh, China and Iran [70,71,72,73], while Kormoker et al. [74] reported low non-carcinogenic and cancer risk for adults and children by PTMs in agricultural soils near the industrial areas of Bangladesh. Other studies related significant carcinogenic risks related to soil contamination by Cd, Ni and Zn [6,7,30]. Our results raised the need for constant monitoring of the levels of PTMs in the soil from cement plant surroundings, using both NCR and CR indices of health risk for local human populations. These indices proved to be more sensitive to conventional metrics recommended by local and national environmental laws (CONAMA, 420/09, COPAM, 166/11) [26,27]. Thus, we consider that our results constitute strong evidences of the need to incorporate the contamination and enrichment indices (Igeo and EF) as well as Health Risk Assessments (NCR and CR indices), not only in instruments of risk assessment to the environmental contamination by local environmental agencies, but also as a tool for monitoring programs of PTM pollution to be incorporated in Environmental Management Systems of cement industries.

5. Conclusions

In this study, we hypothesized that cement production at karstic areas from southeast Brazil could be related to soil PTM contamination at cement plant surroundings, and that these events could be potentially harmful to vicinal human population. Our findings revealed that all PTM concentrations from cement plant surroundings were significantly higher than PTM concentrations from control areas. Moreover, although the soil contamination events seen in this study can be considered mild when compared to other similar studies, health risk assessments revealed there are concerning carcinogenic risks by the local human population due to long-term exposure to PTM found in soil surrounding the cement plants.