Background. Lead exposure is an environmental and occupational health problem associated with different clinical outcomes; however, its relationship with anemia in mining workers is not well characterized. This study evaluated the relationship between blood lead level (BLL) and anemia in mining workers who underwent annual medical-occupational evaluations. Methods. We conducted a cross-sectional study to estimate the association between the BLL and anemia in workers of a mining company during the year 2019. We obtained occupational information and laboratory test results, with the hemoglobin level for identifying anemia and BLL measured by atomic absorption spectrophotometry. The relationship between BLL and anemia was evaluated in a generalized linear model with a log link and the Poisson family to obtain crude and adjusted prevalence ratio (aPR) and its 95% confidence intervals (95% CIs). Results. Three hundred forty mining workers, mainly male (95%), with a mean age of 36.8 ± 9.4 years, were evaluated. The median hemoglobin and BLL were 14.1 g/dL (Interquartile range (IQR): 13.0–15.3) and 3.4 µg/dL (IQR: 2.1−4.8). Only one worker presented a BLL exceeding the upper limit value established by the Ministry of Health of Peru (up to 40.0 µg/dL). We found anemia in 21.8% of the mining workers (CI95%: 17.5–26.5). A low and inverse correlation between hemoglobin and BLL (rho: −0.169) was obtained in this study. BLLs were significantly associated with anemia (aPR: 1.04; 95% CI: 1.01–1.08). Conclusion. Occupational exposure to lead is weakly associated with anemia in mining company workers. Strengthening actions to prevent and control lead exposure is relevant and guarantees the comprehensive promotion of worker health and healthy workplaces.

1. Introduction

Mining is one of Peru’s most important economic activities, whose geography is highly rich in various metals such as copper, silver, gold, zinc, and lead [1]. Mineral extraction involves removing and excavating the earth’s surface using heavy machinery, generating occupational exposure to particulate matter and heavy metals such as lead. These activities increase the risk of occurrence of adverse effects on the health of workers in the medium and long term [2]. Lead is a ubiquitous toxicant found naturally in soil, plants, and water which is disturbed and dispersed from environmental by anthropogenic activities [3, 4]. Routes of exposure to lead in the work environment include ingestion and inhalation in its inorganic form. Inhaled or ingested lead is transported to the heart, bones, intestines, kidneys, and reproductive and nervous systems, causing tissue-specific adverse effects [5].

Although industrial hygiene implements and controls, measures have significantly decreased worker lead concentrations in recent decades [6]. Various studies indicate that workers exposed to lead may suffer adverse health effects by current standards [7, 8]. Blood lead levels (BLLs) less than 20 μg/dL in workers with chronic exposure may be associated with cognitive dysfunction and risk of hypertension and renal dysfunction [9]. Lead is also a significant factor of oxidative stress [10], which generates dysfunction in different blood cells.

Hematological effects are some manifestations of chronic lead poisoning in exposed workers [11]. Lead influences the expression of genes associated with enzymes involved in the synthesis of the heme group, and its inhibition causes a decrease in the production of hemoglobin [12]. On the other hand, decreased survival of red blood cells has been reported in people exposed to lead [13]. These alterations increase the risk of anemia; in fact, the type of anemia that has been evidenced in people with lead exposure is hypochromic microcytic anemia. It is characterized by maintaining mean corpuscular volume levels within the normal range [14]. The relationship between hemoglobin and lead is known, mainly in children and pregnant women [15, 16, 17].

According to the World Health Organization, the indicator of biological exposure is the measurement of BLL [18]. The Ministry of Health of Peru defines a limit value of 40 μg/dL for BLL in people with occupational exposure [19]. However, workers exposed to lead can experience adverse health effects even at levels below this limit [20]. In this sense, occupational medical surveillance programs are essential for evaluating the health of workers exposed to lead [19].

Scientific evidence linking occupational exposure to lead and anemia in mining workers is limited. Most studies focus on children and pregnant women; however, the risk factors for anemia in children differ from those in the adult population [21]. Likewise, anatomical, physiological, biochemical, and endocrine differences exist between age groups [22] and could modify the factors associated with anemia. On the other hand, in Peru, due to the high concentrations of lead in the soil, miners’ main exposure route is through inhalation [23]. Therefore, there is a need to explore the relationship between lead and hemoglobin in adults, particularly mining workers, who have a higher risk of lead exposure than the general population. Hence, the study aimed to evaluate the relationship between BLL and anemia in mining workers who underwent annual medical-occupational evaluations. The study results allow for identifying risk groups and, based on this, provide recommendations to improve workplace risk control and prevention measures.

2. Methods

2.1. Study Area and Participants

We conducted a cross-sectional study evaluating mining workers from a company located in the department of Ica, approximately 300 km from the capital Lima in Peru. This is a polymetallic mine that stands out mainly to produce iron and copper and to a lesser extent others such as lead, zinc, and gold. We evaluated workers in April 2019 in compliance with the annual occupational health surveillance program. According to the Peruvian law of safety and health at work, the employer is obliged to guarantee the medical evaluations to all his workers annually, as part of the health surveillance of workers [24]. These workers work in mining camps following a schedule that oscillates between 20 and 30 days of field activity and 10–15 days of rest outside the camp. Included miners were of both sexes and with blood lead and complete blood count results. We included only workers with at least one continuous year of work activity in the company. Pregnant workers and those who indicated consuming iron-based nutritional supplements were excluded.

2.2. Techniques and Procedures

We designed a data collection sheet to obtain demographic, occupational, and medical information from the annual occupational evaluation carried out on each worker. Information such as the company’s activity type, the work area, and the use of personal protective equipment (PPE) was collected.

Regarding the type of work, two main groups are classified depending on the nature of the activity. Administrative workers mainly include executives, logisticians, and desk personnel within the mining camp, while operational personnel are those within the mineral extraction and treatment process. This second group is subdivided into three groups according to the area where they perform their function. Subsoil are miners who extract minerals in tunnels underground. In contrast, surface workers complement the work outside, extracting in open pit mining. The concentrators work on mineral treatment with equipment and crushers that compact the rocks.

We obtained blood samples in two 3 mL tubes with EDTA K2 (dipotassium ethylenediaminetetraacetic acid). The first sample was used for blood lead measurement, and the second for the blood count analysis. We assessed the BLLs in an equipment with a measurement principle based on graphite furnace atomic absorption spectrophotometry (Analytik Jena, ZEENIT 700P, Germany). The test was carried out per the MTA/MB-011/R92 method [25] and by a toxicologic laboratory. We prepared the calibration curve with a standard lead solution at 0, 20, 50, 250, 500, and 750 µg/L concentrations. The sample processing was aspirated 50 µL of sample and 600 µL of the modifier mixture, stirred for 15 s, and placed in a bucket of the equipment autosampler. Linearity was verified in the calibration curve with a correlation coefficient greater than 0.998. The method’s detection and quantification limit were 0.2 µg/dL and 1.0 µg/dL, respectively. It was also run in triplicate of internal controls of the Bio-Rad brand (Lyphochek Whole Blood Metals Control) in three different levels, with less than 10% relative differences. The limit of lead detection in the assay was 1.0 µg/dL. We considered an elevated BLL if it exceeds 40 μg/dL, as established by the Peruvian Ministry of Health [19].

The blood count was obtained using a HORIBA ABX model ABX PENTRA XL80 (HORIBA Advanced Techno, Co., Kyoto/Japan) hematology autoanalyzer based on electrical impedance and photometry. Hemoglobin concentrations to define the diagnosis of anemia follows World Health Organization guidelines (anemia was considered when hemoglobin concentrations were less than 13.0 g/dL and 12.0 g/dL for men and women, respectively) [26]. Likewise, mild, moderate, and severe anemia was classified according to the hemoglobin concentrations of 10.0–12.9, 8.0−9.9, and less than 8.0 g/dL, respectively. The hemoglobin and BLL analysis were performed in a clinical laboratory with ISO/IEC 15189 international accreditation (EMA, NMX-EC-15189-IMNC-2015, CL150, and CL151 certificates) [27].

2.3. Statistical Analysis

Descriptive characteristics of the study participants were reported (frequencies, percentages, median, interquartile range (IQR), and range). BLL below the detection limit (LOD = 1 μg/dL) was treated as missing data. Barr et al. [28] recommended the assignment value in those cases, who calculated the value lost as a function of LOD/√2. We have already used this method to manage values less than LOD [29]. We used Fisher’s exact and Pearson’s chi-squared test (according to the analysis of expected frequencies) to compare the proportion of workers with anemia according to the independent variables. We performed Spearman’s correlation test between hemoglobin and BLL (non-normal distribution identified by the Kolmogorov–Smirnov test) and its 95% confidence interval (95% CI) using the Bootstrap method at 1,000 replicates. The relationship between BLL and anemia was evaluated in a generalized linear model with a log link and the Poisson family to obtain the prevalence ratio and 95% CI as a measure of association. We considered a p-Value less than 0.05 as significant for univariate and multivariate model. We selected and included variables in the multivariate model based on an epidemiological approach and according to previous studies that considered them as potentially confusing [30, 31]. We conducted all the analyses using the Stata v.17 software (Stata Corp College Station, TX).

2.4. Ethical Aspects

The research was approved on April 15, 2019, by the Ethical Review Committee of the Universidad Alas Peruanas, with Directorial Resolution No. 237-2019-EPTM-FCS-UAP. Since the workers were evaluated with an occupational medical examination in compliance with Peruvian regulations, each worker was asked for their informed consent to use the data generated in the medical evaluation after explaining the objectives, benefits, risks, and use of the instruments during the study. Consent was obtained in person and signed by each worker. The data were handled as confidential, encrypted, and accessible only to the principal investigator.

3. Results

We just excluded two pregnant women from study, according to inclusion and exclusion criteria (Figure 1). Of the 340 mining workers included in the study, 95% were male. The mean age was 36.8 ± 9.4 years, 92.6% were operational workers, 87.8% carried out surface activities, and 81.8% reported whether to use PPE. Of the operational workers, 17.3% indicated they did not use PPE. For those who worked on the surface, concentrator, and underground, 20.7%, 29.4%, and 13.6% did not use PPE either, respectively. The medians of hemoglobin and lead were 14.1 g/dL and 3.4 µg/dL, respectively. Only one worker presented a blood lead concentration that exceeded the upper limit value established by the Ministry of Health of Peru (greater than 40.0 µg/dL), and three cases had BLL below the detection limit of method. We found anemia in 21.8% of the mining workers (95% CI: 17.5–26.5). According to the degrees of anemia, we observed that 98.8% of the cases were of mild anemia, and only one case of moderate anemia was registered. We did not observe cases of severe anemia (Table 1).

Details are in the caption following the image — **Figure 1**
Open in figure viewer PowerPoint

Study participant selection process.

Table 1. Demographic and occupational characteristics of the study population.

Characteristic	N	%
Age (years)	36.8 ± 9.4	20–64^∗∗
Sex
Male	323	95.0
Female	17	5.0
Type of job
Administrative	25	7.4
Operational	313	92.6
Work area
Surface	280	87.8
Concentrator	17	5.3
Subsoil	22	6.9
PPE use
No	70	20.6
Yes	270	79.4
Hemoglobin (g/dL)	14.1 (13.0–15.3) ^∗	8.7–17.7^∗∗
BLL (µg/dL)	3.4 (2.1–4.8) ^∗	0.7–53.9^∗∗
Anemia
No	266	78.2
Yes	74	21.8

PPE, personal protective equipment; BLL, blood lead level. ^∗Median (Interquartile range); ^∗∗Min–Max.

The distribution of the study variables according to the presence of anemia is presented in Table 2. The median (and interquartile range) of BLL (µg/dL) in the groups with and without anemia was 3.3 (IQR: 2.0–4.8) and 3.5 (IQR: 2.8–6.0), respectively, not difference was found (p = 0.073, Mann–Whitney nonparametric test). The maximum values of BLL in workers without and with anemia were 23.7 and 53.9 µg/dL, respectively.

Table 2. Characterization of mining workers according to the presence of anemia.

Characteristic	Anemia, n (%)		p-Value
Characteristic	No	Yes	p-Value
Age (years)	37 (30–42)	36 (31–40)	0.734
Sex
Male	256 (96.2)	67 (90.5)	0.052
Female	10 (3.8)	7 (9.5)	—
Type of job
Administrative	18 (6.8)	7 (9.6)	0.419
Operational	247 (93.2)	66 (90.4)	—
Work area
Surface	220 (89.1)	60 (83.3)	—
Concentrator	14 (5.7)	3 (4.2)	0.096
Subsoil	13 (5.3)	9 (12.5)	—
PPE use
No	27 (21.1)	8 (18.9)	0.688
Yes	114 (78.9)	43 (81.1)	—
BLL (µg/dL)	3.3 (2.0–4.8) ^∗	3.5 (2.8–6.0) ^∗	0.073

PPE, personal protective equipment; BLL, blood lead level. ^∗Median (interquartile range).

Figure 2 shows the correlation between the BLL and the workers’ hemoglobin. The relationship between BLL and the workers’ hemoglobin was inversely correlated (rho = −0.169, 95CI%: −0.271 to −0.067, p < 0.05).

In the crude regression model, BLLs were significantly associated with anemia (prevalence ratio (PR) = 1.04; 95% CI: 1.01–1.07). After adjusting for sex, age, type of job (administrative/operational), work area, and PPE use, the association between BLL and anemia was also found (adjusted prevalence ratio (aPR) = 1.04; 95% CI: 1.01–1.08) (Table 3).

Table 3. Relationship between blood lead level and anemia in multivariate analysis.

Characteristic	Crude model		Adjusted model^a
Characteristic	PR (95% CI)	p-Value	PR (95% CI)	p-Value
BLL (µg/dL)	1.04 (1.01–1.07)	0.028	1.04 (1.01–1.08)	0.011

^aGeneralized linear model with log link and Poisson family. Adjusted by sex, age, type of job (administrative/operational), work area, and personal protective equipment.

4. Discussion

This study aims to determine the association between BLL and anemia in mining workers. We found that for each µg/dL increase in BLL, the frequency of anemia increases by 4%. Since only one of the mining workers has a BLL above those regulated in Peruvian regulations (above 40 µg/dL), study results show that values of BLL below that parameter could be related to anemia in this population. We found that the BLL had a median of 3.4 ug/dL, which does not exceed the upper limit indicated in the Peruvian regulations. However, it is known that even low blood lead concentrations can cause long-term adverse health effects. Previous studies have shown that levels less than 5 ug/dL are associated with cognitive deficits and neurodevelopmental alterations, although these findings have been on children and adolescents [32, 33]. However, a study in India reported increased blood pressure in workers exposed to low levels of lead [34]. Reports of adverse health events for workers with low BLLs are limited.

A low and inverse correlation (rho = −0.169) between BLL and hemoglobin was obtained in this study. Kutllovci et al. [15] reported a correlation of −0.304, not in mining workers, but in a community that presented an average lead level of 2.4 ± 1.9 µg/dL, a value lower reported in this study (4.2 ± 4.0 µg/dL). This finding could be explained since mining workers use PPE, reducing the level of exposure compared to the general population. Another investigation found more robust correlations between BLL and other indicators of anemia than hemoglobin, such as serum ferritin, with a correlation value of −0.54, and found lead levels of 13.1 μg/dL. However, it was evaluated in children [35]. Although previous studies have shown an inverse correlation between BLL and hemoglobin, the decrease in the latter reaches a limit of up to 30 μg/dL of BLL, finding a nonlinear U-shaped dose–response relationship [30]. Lead exposure decreases the number of erythrocytes in whole blood, mainly due to the depletion of enzymes related to the cycle that reduces their viability [36]. Hence, the types of anemia generated due to lead toxicity are normocytic normochromic and microcytic hypochromic [37]. Future studies in mining workers could should include other indicators regarding anemia, such as ferritin, serum iron, and transferrin, for a better characterization of the studied phenomena.

Additionally, this finding can be transferred to other populations. The literature shows that children are the most vulnerable to lead (they absorb more lead than adults and are more susceptible to developing toxicity), particularly neurological toxicity, even at low levels of exposure [38, 39]. In Peru, where various investigations have shown BLL between 10 and 40 μg/dL in children in areas surrounding large-scale mining industries [40], as well as in informal workers, such as battery recyclers, in whom average lead concentrations of 37.7 μg/dL have been found [41].

The literature on the association between BLL and anemia in mining workers is scarce. Studies comparing hemoglobin concentrations and other hematological parameters in workers exposed and not exposed to lead available [42, 43, 44, 45]. A study in 2017 showed that BLLs between 15 and 25 µg/dL were associated with anemia, the frequency of which was 11.1% in workers at a lead factory [31]. The frequency of anemia in our study was 21.8%, a value that almost doubles the antecedent and is worrisome for a predominantly male population. On the other hand, Sadaf et al. [46] estimated a marginal OR of 1.02 for the risk of anemia in workers exposed to lead from car paints, which is very similar to our results. Hence, the exposure to lead in mining workers would be related to anemia, and the study and the results of the study are consistent with what was reported in previous studies. Lead toxicity is a significant health problem, especially in developing countries, such as Peru, one of the primary lead producers in the world [47]. However, despite the large number of formal mining workers (over 200,000 according to Ministry of Energy and Mines of Peru) [48] at the many active mines, the information of health effects on these workers is scarce [49]. This situation may be due to limited access to occupational biological monitoring information, among other shortcomings in the regulations still needing improvement in Peruvian national regulations.

Among the study’s limitations, there were no environmental exposure measurements, so it is difficult to objectively establish the occupational risk to lead. Furthermore, information on diet, smoking, altitude living, and employment status in term of sex, among other variables potentially confounding the association of interest, were unavailable from the data source. However, a low variability among these variables is expected, considering that the workers are in mining camps, where conditions are highly controlled. On the other hand, occupational surveillance did not include more specific markers to identify the type of anemia, which would have made it possible to explore the relationship with BLL. We also did not evaluate the effect biomarkers for lead exposure, such as delta amino levulinic acid activity and zinc protoporphyrin, since data for these biomarkers were unavailable in the data source. Likewise, evaluating erythrocyte pyrimidine 5’-nucleotidase (P5’N) is helpful as a specific biomarker for evaluating personnel exposed to lead [50]. It should be included as a criterion to exclude iron deficiency anemia in occupational surveillance programs. Although notwithstanding these limitations, the study results show that mining workers could be a subgroup at high risk of anemia due to the BLL. Finally, we recommend that the Peruvian Ministry of Health update the regulations regarding the permissible limit values for BLL. The evidence shows a tendency to reduce these values and to be more demanding with measures to prevent and control exposure to lead [51].

5. Conclusions

We found a weak association between BLL and anemia and with hemoglobin concentration in Peruvian mining workers. Given the limitations stated in this study, these results could be explained by other no available factors. However, the mining industry must continue to implement and strengthen the prevention and control programs for exposure to lead and other chemical compounds. Even BLL below what is established in the Peruvian regulations could increase the occurrence of anemia. Improvement in the measures adopted by companies, particularly in administrative controls (annual medical examinations and food controlled by concessionaires) and engineering (personal protection measures), could reduce the probability of anemia in mining workers.

Abbreviations

CI:: Confidence interval
BLL:: Blood lead level
PR:: Prevalence ratio
aPR:: Adjusted prevalence ratio
IQR:: Interquartile range
PPE:: Personal protective equipment.

Ethical Approval

The research was approved on April 15, 2019, by the Ethical Review Committee of the Universidad Alas Peruanas, with Directorial Resolution No. 237-2019-EPTM-FCS-UAP.

Consent

We obtained the informed consent of each participating worker after informing them of the objectives, use of instruments, benefits, risks, and confidentiality of the information.

Conflicts of Interest

The authors have no conflicts of interest to declare.

Authors’ Contributions

Bertha Pummalanqui-Ramirez and Jaime Rosales-Rimache designed and conducted the study, collected and analyzed data, and wrote the manuscript; Bertha Pumallanqui-Ramirez, Jair Li, and Lenin Rueda-Torres collected the data and gave conceptual advice; Jair Li and Lenin Rueda-Torres analyzed data and gave technical support; Jaime Rosales-Rimache gave conceptual advice. All authors read and approved the final manuscript.

Open Research

Data Availability

The data presented in this study are available on request from the corresponding author.

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Relationship between Blood Lead Levels and Anemia: A Cross-Sectional Study on Mining Workers from Peru

Abstract

1. Introduction