- Email: [email protected]
Assessment of hair metal levels in aluminium plant workers using scalp hair ICP-DRC-MS analysis
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
Contents lists available at ScienceDirect
Journal of Trace Elements in Medicine and Biology journal homepage: www.elsevier.com/locate/jtemb
Toxicology
Assessment of hair metal levels in aluminium plant workers using scalp hair ICP-DRC-MS analysis Anatoly V. Skalnya,b,c, Galina A. Kaminskayad, Tatyana I. Krekeshevad, Sholpan K. Abikenovad, ⁎ Margarita G. Skalnayac,e, Anatoly T. Bykove, Alexey A. Tinkova,c, a
Yaroslavl State University, Yaroslavl, Russia All-Russian Research Institute of Medicinal and Aromatic Plants (VILAR), Moscow, Russia c Peoples’ friendship university of Russia (RUDN University), Moscow, Russia d National Institute for Occupational Safety, Astana, Kazakhstan e Kuban State Medical University, Krasnodar, Russia b
A R T I C LE I N FO
A B S T R A C T
Keywords: Primary aluminium production Exposure Cadmium Lead Arsenic Risk
The objective of the present study was to assess the level of aluminium and toxic metals in hair of workers occupationally exposed to aluminium. 124 employees of the aluminium plant working in the hydrometallurgical (n = 43) and sintering units (n = 41), as well as 40 occupationally nonexposed controls were examined. Hair aluminium (Al), arsenic (As), beryllium (Be), cadmium (Cd), mercury (Hg), nickel (Ni), lead (Pb), and tin (Sn) content was assessed using inductively-coupled plasma mass spectrometry. The obtained data demonstrate that aluminium plant workers had significantly higher levels of hair Al (28.8 (15.4–58.6) vs 7.8 (4.3–14.2) μg/g, p < 0.001), Cd (0.053 (0.032 – 0.095) vs 0.025 (0.014 – 0.043) μg/g, p < 0.001) and Pb (0.672 (0.299–1.310) vs 0.322 (0.170 – 0.609) μg/g, p = 0.012) than the controls, respectively. Further analysis demonstrated that persons involved in different technological processes were characterized by distinct hair metal profiles. Hair Al, Be, Cd, Ni, Pb, and Sn levels in men working in the sintering unit of the aluminium plant exceeded the respective control values. In turn, workers of the hydrometallurgical unit were characterized by more than 2-fold higher levels of Al and Cd in hair as compared to the controls. The results of the present study demonstrate that workers of the aluminium plant are characterized by increased risk of Al as well as As, Cd, Pb, and Sn exposure.
1. Introduction Aluminium is the widespread metal comprising 8.23% of the Earth’s crust by weight [1]. Due to its physical and chemical properties it is widely used in various fields of modern industry including construction, food production, electronics, pharmacy, etc. [2]. Production of aluminium (both primary and secondary) is increasing worldwide [3]. In particular, global consumption of aluminium has increased from 29 Mt in 1994 to 45 Mt in 2004. The top-5 consumers of Al are USA, China, Japan, Germany, and Russia. In turn, the main producers of bauxite and alumina are Australia, Brazil, and China. Kazakhstan is also rich in bauxite reserves and its production [4]. In 2007, bauxite reserves in Kazakhstan were estimated to be 200 Mt, accounting for 1% of total value worldwide. At the same time, the total value of bauxite produced in Kazakstan accounted for 3% of global production (4.7 Mt) [4,5]. At the same time, aluminium exposure also has a significant adverse effect on human health [2] due to its prooxidant, proinflammatory, ⁎
excitotoxic and immune-modulatory properties [6]. The growing body of data demonstrate that aluminium may have neurotoxic effects [7]. However, association between Al exposure and Alzheimer’s disease or autism is still questionable [8]. Moreover, the existing studies demonstrate a link between aluminium and breast cancer [9]. Evidence on the association between occupational aluminium exposure and pulmonary fibrosis [10], lung cancer [11], and neurological dysfunction [12] exist. Therefore, monitoring of human exposure to aluminium is of great importance. Hair is widely used for biomonitoring of metal exposure due to a number of advantages like high mineralization and irreversible incorporation of metals into hair matrix [13]. In contrast to blood and urine, where metal levels are strictly regulated by homeostatic mechanisms [14], hair may be used for assessment of exposure history for several months due to accumulation of metals [15]. In addition, due to ability to absorb metals from environment hair may be used in biomonitoring studies [16]. Previous data demonstrate that hair may be used as a valuable marker of occupational exposure to metals and
Corresponding author. E-mail addresses: [email protected], [email protected] (A.A. Tinkov).
https://doi.org/10.1016/j.jtemb.2018.06.014 Received 7 September 2017; Received in revised form 14 June 2018; Accepted 15 June 2018 0946-672X/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Skalny, A.V., Journal of Trace Elements in Medicine and Biology (2018), https://doi.org/10.1016/j.jtemb.2018.06.014
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
current and former smoking; ii) excessive alcohol consumption; iii) acute and chronic infectious diseases (including gastritis that requires the use of alumunium-containing antacids); iv) surgical and traumatic diseases; v) metallic implants (including dental amalgams); vi) endocrine disorders; vii) vegetarianism and other specific dietary patterns (including the use of herbs that may be the source of alumunium); viii) dyed hair. Therefore, only healthy workers of aluminium plant and control persons were enrolled in the current study. Data on health condition are collected yearly during mandatory physical examination. The aluminium plant is the one of the ten largest producers of alumina in the world. The plant produces up to 1.7 million tons of metallurgic alumina that is exported to China and Russia. At the moment of investigation, the total number of employees of aluminium plant was 6,117, whereas 1262 of them were working in hazardous conditions. The system of health protection and safety is implemented in the plant. All employees are equipped with personal protective equipment: coveralls, safety shoes, gloves, helmet, balaclava, protective goggles, respirator, safety belt, dielectric bots, antinoise headphones (all protective equipment is certified No. KZ 41400285, No KZ 41400348). The overalls are cleaned by the plant’s laundry. All units are equipped with the sanitary facilities (wardrobe, shower room, dining room). The collective protective equipment includes aspiration and exhaust ventilation systems, noise protection system, as well as system of prevention of electrical damage. All persons working in hazardous conditions receive milk that is widely used for health protection in hazardous occupational conditions, as well as detergents (soap, powders). All protective activities are controlled by internal and external commissions. Indoor atmospheric pollution is regularly monitored by the environmental laboratory and the data obtained are compared with the existing maximum permissible concentrations (MPC). The results of monitoring demonstrate that the rate of indoor environmental pollution is within the limits provided by national regulations (Table 1). All employees are provided with similar meals in the dining room. The dining room is equipped with ceramic dish and stainless steel kitchen utensils, whereas the use of aluminium utensils is avoided. Tap water is used for drinking and preparation of meals. Systematic analysis of tap water demonstrates that the level of the studied metals is lower than MPC [24]. Hair sampling was performed after regular mandatory physical examination of the workers that excluded occupational and non-occupational pathology. All examinees have washed their hair at the day of sampling using their usual commercially available shampoos. Despite different chemical composition of shampoos, their use did not significantly affect hair metal content [25]. Occipital scalp hair samples were collected using ethanol-precleaned stainless scissors. Only proximal parts of strands were used for analysis. Prior to digestion, the hair samples were subjected to washing with acetone with subsequent rinsing with distilled deionized water for three times and drying in the air (60 °C). The existing data demonstrate that such type of washing procedure removes mechanical contamination (dust) but does not remove metals bound to hair matrix [26]. A total of 50 mg of washed hair samples were introduced into Teflon tubes containing concentrated nitric acid (HNO3). Digestion procedure was performed in Berghof Speedwave 4 (Berghof Products & Instruments, Germany) system at 170–180 °C for 20 min. The obtained
metalloids [17,18]. Moreover, the hair metal level was also shown to be associated with adverse health effects in occupationally exposed persons [19]. Taking into account the toxic effects of metal co-exposure [20], other toxic metals should be also monitored in persons exposed to aluminium. Therefore, the objective of the present study was to assess the level of aluminium and other toxic elements in hair of persons occupationally exposed to aluminium. 2. Materials and methods The protocol of the present investigation was approved by the Local Ethics Committee. The sampling and experimental procedures were performed in agreement with the principles of the Declaration of Helsinki and later amendments. All participants have provided informed consent prior to the examination. A total of 124 men took part in the present study. 84 employees of the aluminium plant in North-Eastern Kazakhstan working in the hydrometallurgical (n = 43) and sintering units (n = 41) of the plant presented the occupationally exposed groups. Briefly, the main technological process in the hydrometallurgical unit is the production of alumina from bauxite using the Bayer process. In turn, sintering unit performs recovery of alumina from Bayer red mud [21]. In 2012, the total amount of bauxite, aluminium oxide, and aluminium produced by the studied plant was 5.17, 1.51, and 0.249 Mt [5]. 40 healthy men living in more than 1.0 km from the plant in the north-western part of the city and not involved in industrial processes were used as the occupationally non-exposed controls (Fig. 1). The examinees in all groups were age- and body mass index (BMI)-matched to prevent the influence of ageing [22] and obesity [23] on hair metal levels. Age and BMI in the controls, hydrometallurgical and sintering unit workers were 36.6 ± 10.2 years and 24.7 ± 3.5 kg/m2, 36.3 ± 11.1 years and 24.5 ± 4.4 kg/m2, and 36.0 ± 11.3 years and 24.3 ± 5.2 kg/m2, respectively. No significant difference in working experience between the hydrometallurgical (11 ± 6 years) and sintering unit (9 ± 5 years) workers was detected. In addition, to avoid the influence of side factors on hair metal levels, the following exclusion criteria were used: i)
Table 1 Data on atmospheric pollution monitoring of the working environment.
Fig. 1. Location of the aluminium plant (filled box) and the areas of control species sampling (empty box). 2
Parameter
MPC
Hydrometallurgical unit
Sintering unit
Alkaline aerosol (mg/m3) Abrasive dust (mg/m3) Metal dust (mg/m3) Alumina dust (mg/m3)
0.5 6 10 6
0.14 ± 0.04 2.8 ± 0.9 2.3 ± 0.8 3.8 ± 2.0
0.14 ± 0.06 3.3 ± 1.2 4.1 ± 1.5 5.4 ± 2.1
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
by more than 2-fold higher levels of Al as compared to the controls. The hair content of Cd significantly exceeded the control values by 63%, whereas hair Pb levels were nearly 2-fold higher. The level of Be, As, Hg, Ni, and Sn in hair of men working in the hydrometallurgical unit of the aluminium plant did not differ significantly from those in occupationally non-exposed persons. Hair metal content in the sintering unit workers also significantly exceeded that in men working in hydrometallurgical unit. In particular, the level of Al, Cd, Ni, and Pb in hair of sintering unit workers exceeded the hydrometallurgical unit values by 76%, 45%, 46%, and 9%, respectively. In turn, hair levels of Be and Sn in men involved in sintering were nearly 10- and 3-fold higher in comparison to those in workers of another unit of aluminium plant. Correlation analysis demonstrated that hair Al levels of the studied population were characterized by a significant correlation with hair Be and Pb content (Table 3). At the same time, no significant correlation was observed between hair Al and As, Cd, Hg, Ni, or Sn levels. Analysis of correlation between hair metal levels in workers of the aluminium plant demonstrated that hair Al content is directly associated with As, Be, Ni, and Pb, whereas no significant interaction with Cd, Hg, and Sn levels was observed.
samples were added to a total volume of 15 ml with distilled deionized water and subjected to analysis. The level of aluminium (Al), arsenic (As), beryllium (Be), cadmium (Cd), mercury (Hg), nickel (Ni), lead (Pb), and tin (Sn) content was assessed using inductively coupled plasma mass spectrometry (ICP-MS) with NexION 300D (PerkinElmer Inc., Shelton, CT 06484, USA) equipped with the 7-port FAST valve and ESI SC-2 DX4 autosampler (Elemental Scientific Inc., Omaha, NE 68122, USA). The use of Dynamic Reaction Cell in ICP-MS (ICP-DRC-MS) technology allowed to remove the majority of atomic interferences. The ICP-MS system was conditioned and calibrated in accordance with the manufacturer’s manual via external calibration. The external calibration solutions containing 0.5, 5, 10 and 50 μg/l of metals were freshly prepared from the Universal Data Acquisition Standards Kits (PerkinElmer Inc., Shelton, CT 06484, USA) by dilution with distilled deionized water and subsequent acidification with 1% HNO3. Taking into account incomplete acidity and viscosity matching between calibration and sample matrices the online internal standardization with yttrium-89 and rhodium-103 was used via 7-port FAST valve. The internal standard solution containing 10 ppb Y and Rh was prepared from Yttrium (Y) Pure Single-Element Standard and Rhodium (Rh) Pure Single-Element Standard (PerkinElmer Inc., Shelton, CT 06484, USA), respectively. Laboratory quality control was regularly performed using the certified reference material of human hair GBW09101 (Shanghai Institute of Nuclear Research, Shanghai, China). The recovery rates for all metals exceeded 85%. The laboratory also takes part in external quality assessment schemes in occupational and environmental laboratory medicine (OELM). All analyses are performed in clean laboratory environment (air filtration, exhaust ventilation). The obtained data were treated with Statistica 10.0 (Statsoft, Tulsa, OK, USA). Shapiro-Wilk test was used for assessment of data normality. As the distribution was found to be non-Gaussian, median and the respective 25 and 75 percentile boundaries were used for expression of hair metal levels. Group comparison was performed using MannWhitney U test The differences were considered significant at the level of p < 0.05.
4. Discussion Generally, the obtained data demonstrate that involvement in aluminium production was associated with increased levels of Al, Cd, Pb, and Sn levels in hair of workers. The obtained data are in agreement with previous study of hair aluminium levels in aluminium-exposed persons [27]. Earlier studies have detected a significant impact of occupational exposure to aluminium on the level of metal in the organism. In particular, it has been shown that workers of the aluminium industry are characterized by a significant elevated serum and urinary Al levels [28]. Similarly, increased serum Al concentrations were observed in persons exposed to Bayer-process alumina for a long period [29]. Assessment of plasma Al levels by flameless atomic absorption spectrometry revealed a significant increase in electrolysis-workers in comparison to non-exposed persons. It has been also noted that the total exposure time at the workplace correlates with plasma Al concentration at r = 0.4 [30]. The authors also state that occupational exposure to Al in anode changer not wearing a mask is associated with increased urinary Al levels [0]. Moreover, it has been stated that persons directly exposed to Al are characterized by significantly higher serum Al concentrations as compared to both indirectly exposed and non-exposed examinees [31]. Oppositely, another study examining workers of the bauxite mines did not reveal any significant difference in serum Al level in comparison to the group of non-exposed wood processors [32]. In parallel with increased hair Al levels, we have detected significantly elevated levels of As, Cd, Pb, and Sn in scalp hair of aluminium plant workers. These findings at least partially correspond to the results of the earlier studies, demonstrating the association between primary aluminium industry and Be, Cd, Ni, Hg, and Pb exposure [33,34]. In particular, it has been demonstrated that persons involved in secondary Al smelting may be exposed both to Al and Pb [35]. Biomonitoring studies also revealed a significant influence of aluminium production industry on the level of heavy metals in forest ecosystem. In particular, the level of Cd and Pb in plants and phytophagous insects was increased. Similarly, teeth and hair As, Cd, and Pb content was increased in roe-deers living in the aluminium plant region [36]. Simultaneous exposure of workers to various metals during Al production may be associated with the chemical composition of bauxite and its residues. Despite the fact that Al is the main metal constituent of bauxite, the latter also contains large amounts of Fe, Ti, and other metals [37]. It has been demonstrated that bauxite residues from a Western Australian refinery contain a significant amount of As (50 ppm), although being less abundant than Cr (650 ppm). At the same time, taking into account the higher solubility of As compounds the
3. Results The obtained data demonstrate that aluminium plant workers were characterized by significantly elevated hair metal levels (Fig. 2). In particular, the workers had more than 3-fold higher levels of hair Al content as compared to the occupationally non-exposed controls (28.8 (15.4–58.6) vs 7.8 (4.3–14.2) μg/g, p < 0.001). Hair Cd and Pb levels in aluminium plant employees exceeded the control group values by a factor of more than two (0.053 (0.032–0.095) vs 0.025 (0.014–0.043) μg/g, p < 0.001, and 0.672 (0.299–1.310) vs 0.322 (0.170–0.609) μg/ g, p = 0.012). Hair levels of Sn in occupationally-exposed persons exceeded the control values by 46% (0.118 (0.058–0.254) vs 0.081 (0.057–0.121) μg/g, p = 0.038). At the same time, hair As (0.044 (0.027–0.077) vs 0.042 (0.028 – 0.074) μg/g, p = 0.826), Be (0.0003 (0.0001–0.0012) vs 0.0004 (0.0001–0.0008) μg/g, p = 0.959), Hg (0.18 (0.13 – 0.33) vs. 0.20 (0.12–0.29) μg/g, p = 0.670), and Ni (0.268 (0.200–0.387) vs 0,226 (0.171–0.342) μg/g, p = 0.455) content in the occupationally exposed group did not differ significantly from the control values. Further analysis demonstrated that persons involved in different technological processes were characterized by distinct hair metal profiles (Table 2). In particular, hair Al, Be, Cd, Pb, and Sn levels in men working in the sintering unit of the aluminium plant exceeded the respective control values by the factors of nearly 4, 5, 2, 2, and 2. Hair Ni levels in the sintering unit workers were 45% higher as compared to the control level. The level of As and Hg in the sintering unit workers did not differ significantly from the control values. In turn, workers of the hydrometallurgical unit were characterized 3
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
Fig. 2. Hair metal levels in workers of the aluminium plant and occupationally non-exposed controls. The graph represents Median (25–75). Individual p values are indicated as assessed by Mann-Whitney U test Line – Median, Box – 25–75 percentile range, Whisker – Non-outlier range. C – control; A – aluminium plant workers.
Despite the fact that the level of metals in hair of aluminium plant workers was significantly higher than that of the controls, only hair Al values exceeded the background reference values for hair metals in Russia [44], Sweden [45], Poland [13], and France [46]. Taking into account the site specificity of hair metal content [47], the obtained data should be compared to the reference values of hair metal content in Kazakshtan, that seem to be lacking. However, the results of regular municipal monitoring of water and food metal content did not reveal any elevation of Al content exceeding the MPC. Taking into account a complex system of health protection aimed at prevention of excessive administration of aluminium and other toxic elements, the observed increase in hair Al levels may be indicative of cumulative external binding of Al to hair matrix due to emission of Al-
authors proposed that potential health effects of bauxite residues may be caused by As rather than Cr [38]. In addition, high As, Pb [39], and Cd [40] content was reported in bauxitic soils from Jamaica. We observed significantly increased levels of Be in hair of workers of the sintering unit, but not hydrometallurgical unit, being in contrast to earlier indication of exposure to Be in primary aluminium production [41,42]. The results of the present study also demonstrate that workers of sintering unit are characterized by significantly higher hair levels of metals than persons working in hydrometallurgical unit and non-exposed controls. The observed situation may be associated with significant difference in concentrations of aluminium and other chemical agents in air of units performing distinct technological processes [43].
Table 2 Hair metal levels (μg/g) in workers of different units of aluminium plant and occupationally non-exposed controls. Metal
Control (n = 40)
Hydrometallurgical unit (n = 43)
Sintering unit (n = 41)
Al As Be Cd Hg Ni Pb Sn
7.8 (4.3–14.2) 0.042 (0.028–0.074) 0.0002 (0.0001–0.0003) 0.025 (0.014–0.043) 0.192 (0.134–0.420) 0.226 (0.171–0.342) 0.322 (0.170–0.609) 0.081 (0.0570.121)
19.3 (9.68–42.8)* 0.041 (0.025–0.068) 0.0001 (0.0001–0.0002) 0.042 (0.027–0.073)* 0.204 (0.095–0.350) 0.224 (0.142–0.337) 0.633 (0.208–1.096)* 0.063 (0.046–0.125)
34.0 (21.3–80.2)*,† 0.051 (0.034–0.100) 0.0010 (0.0007–0.0017)*,† 0.060 (0.042–0.150)*,† 0.217 (0.134–0.304) 0.327 (0.237–0.430)*,† 0.687 (0.432–1.716)*,† 0.173 (0.118–0.386)*,†
Data expressed as median (25–75). * significant difference in comparison to Control values at p < 0.05. † significant difference in comparison to sintering unit values at p < 0.05. 4
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
References
Table 3 Correlation between hair Al and toxic metal levels. Element
As Be Cd Hg Ni Pb Sn
General cohort
[1] K.J. Orians, K.W. Bruland, Dissolved aluminium in the central North Pacific, Nature 316 (6027) (1985) 427–429. [2] D. Krewski, R.A. Yokel, E. Nieboer, D. Borchelt, J. Cohen, J. Harry, S. Kacew, J. Lindsay, A.M. Mahfouz, V. Rondeau, Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide, J. Toxicol. Environ. Health B Part. B 10 (S1) (2007) 1–269. [3] H. Bergsdal, A.H. Strømman, E.G. Hertwich, The Aluminium Industry-Environment, Technology and Production, IndEcol, Trondheim, Norway, 2004. [4] Z. Luo, A. Soria, Prospective study of the world aluminium industry, JRC Sci. Tech. Rep. (2007) 71. [5] P. von Hartlieb‐Wallthor, Market report on Kazakhstan, Min. Rep. 150 (4) (2014) 234–238. [6] S.J. Flora, Toxic metals: health effects, and therapeutic measures, J. Biomed. Ther. Sci. 1 (1) (2014) 48–64. [7] C. Exley, What is the risk of aluminium as a neurotoxin? Expert Rev. Neurother. 14 (6) (2014) 589–591. [8] C. Exley, The toxicity of aluminium in humans, Morphologie 100 (329) (2016) 51–55. [9] P.D. Darbre, F. Mannello, C. Exley, Aluminium and breast cancer: sources of exposure, tissue measurements and mechanisms of toxicological actions on breast biology, J. Inorg. Biochem. 128 (2013) 257–261. [10] P.V. De, P. Dumortier, F. Rickaert, R. de Weyer, C. Van, J.C. Lenclud, Yernault, Occupational lung fibrosis in an aluminium polisher, Eur. J Respir. Dis. 68 (1986) 131–140. [11] B. Armstrong, C. Tremblay, D. Baris, G. Thériault, Lung cancer mortality and polynuclear aromatic hydrocarbons: a case-cohort study of aluminum production workers in Arvida, Quebec, Can. Am. J. Epidemiol. 139 (1994) 250–262. [12] D.M. White, W.T. Longstreth, L. Rosenstock, K.H. Claypoole, C.A. Brodkin, B.D. Townes, Neurologic syndrome in 25 workers from an aluminum smelting plant, Arch. Int. Med. 152 (1992) 1443–1448. [13] K. Chojnacka, A. Zielińska, H. Górecka, Z. Dobrzański, H. Górecki, Reference values for hair minerals of Polish students, Environ. Toxicol. Pharmacol. 29 (3) (2010) 314–319. [14] I.B.-A. Razagui, I. Ghribi, Maternal and neonatal scalp hair concentrations of zinc, copper, cadmium, and lead, Biol. Trace Elem. Res. 106 (1) (2005) 1–27. [15] S. Foo, N. Khoo, A. Heng, L. Chua, S. Chia, C. Ong, C. Ngim, J. Jeyaratnam, Metals in hair as biological indices for exposure, Int. Arch. Occup. Environ. Health 65 (1) (1993) S83–S86. [16] E. Tamburo, G. Dongarrà, D. Varrica, D. D’Andrea, Trace elements in hair of urban schoolboys: a diagnostic tool in environmental risk assessment, Geophys. Res. Abstr. (2011) 1157. [17] R. Mehra, M. Juneja, Elements in scalp hair and nails indicating metal body burden in polluted environment, J. Sci. Ind. Res. 64 (2) (2005) 119–124. [18] A.R. Grabeklis, A.V. Skalny, S.P. Nechiporenko, E.V. Lakarova, Indicator ability of biosubstances in monitoring the moderate occupational exposure to toxic metals, J. Trace Elem. Med. Biol. 25 (2011) S41–S44. [19] R. Mehra, M. Juneja, Adverse health effects in workers exposed to trace/toxic metals at workplace, Indian J. Biochem. Biophys. 40 (2003) 131–135. [20] R. Altenburger, Understanding combined effects for metal Co-exposure in ecotoxicology, in: A. Sigel, H. Sigel (Eds.), Metal Ions in Toxicology: Effects, Interactions, Interdependencies, Royal Society of Chemistry, Great Britain, 2010, pp. 1–26. [21] X.-b. Li, X. Wei, L. Wei, G.-h. Liu, Z.-h. Peng, Q.-s. Zhou, T.-g. Qi, Recovery of alumina and ferric oxide from Bayer red mud rich in iron by reduction sintering, Trans. Nonferrous Met. Soc. China 19 (5) (2009) 1342–1347. [22] M.G. Skalnaya, A.A. Tinkov, V.A. Demidov, E.P. Serebryansky, A.A. Nikonorov, A.V. Skalny, Age-related differences in hair trace elements: a cross-sectional study in Orenburg, russia, Ann. Hum. Biol. 43 (5) (2016) 438–444. [23] M.G. Skalnaya, A.A. Tinkov, V.A. Demidov, E.P. Serebryansky, A.A. Nikonorov, A.V. Skalny, Hair toxic element content in adult men and women in relation to body mass index, Biol. Trace Elem. Res. 161 (1) (2014) 13–19. [24] Informational Bulletin on Environment in Kazakhstan Republic in 2016, (2016) Kazhydromet, Kazakhstan. [25] A. LeBlanc, P. Dumas, L. Lefebvre, Trace element content of commercial shampoos: impact on trace element levels in hair, Sci. Total Environ. 229 (1) (1999) 121–124. [26] L.-J. Zhao, T. Ren, R.-G. Zhong, Determination of lead in human hair by high resolution continuum source graphite furnace atomic absorption spectrometry with microwave digestion and solid sampling, Anal. Lett. 45 (16) (2012) 2467–2481. [27] M. Wilhelm, J. Passlick, T. Busch, M. Szydlik, F. Ohnesorge, Scalp hair as an indicator of aluminium exposure: comparison to bone and plasma, Hum. Toxicol. 8 (1) (1989) 5–9. [28] H.J. Gitelman, F.R. Alderman, M. Kurs-Lasky, H.E. Rockette, Serum and urinary aluminium levels of workers in the aluminium industry, Ann. Occup. Hyg. 39 (2) (1995) 181–191. [29] D. Waldron-Edward, P. Chan, S. Skoryna, Increased prothrombin time and metabolic changes with high serum aluminum levels following long-term exposure to Bayer-process alumina, Can. Med. Assoc. J. 105 (12) (1971) 1297. [30] C. Schlatter, A. Steinegger, U. Rickenbacher, C. Hans, A. Lengyel, Aluminium levels in the blood plasma of persons working in the aluminium industry, Environ. Geochem. Health 12 (1-2) (1990) 59–64. [31] W. Ruangyuttikarn, P. Pongraveevongsa, P. Winitchakoon, Serum aluminium in alumina exposed workers, J. Med. Assoc. Thai 85 (8) (2002) 928–934. [32] J.F. DeKom, H.M. Dissels, G.B. Van DerVoet, F.A. De Wolff, Serum aluminium levels of workers in the bauxite mines, J. Toxicol. Clin. Toxicol. 35 (6) (1997) 645–651.
Aluminium plant workers
r
p
r
p
−0.041 0.366 0.109 −0.021 0.073 0.253 −0.050
0.652 < 0.001* 0.230 0.820 0.425 0.011* 0.580
0.545 0.423 0.084 0.002 0.195 0.155 −0.082
< 0.001* < 0.001* 0.278 0.980 0.011* 0.045* 0.292
Data expressed as correlation coefficients (r) and the respective p values. * Correlation is significant at p < 0.05.
containing dust into the occupational environment. In particular, it has been demonstrated that atmospheric metals are able to bind hair matrix irreversibly and may not be removed by washing procedures [26,48]. Therefore, workers of aluminium plant may have an increased risk of cumulative Al as well as As, Cd, Pb, and Sn exposure in the case of disruption of personal and/or general health protection systems. Therefore, simultaneous monitoring of the conditions of the protective systems as well as the levels of these metals in aluminium plant workers is essential for prevention of possible toxic effects that may occur during metal co-exposure [20]. Moreover, the possibility of altered essential trace elements status in Al-exposed persons should be also taken into account [49,50]. However, kinetic studies involving hair, blood, and urine investigation are required to specify the mechanisms of increased hair Al levels. At the same time, the present study has certain limitations: 1) although hair metal analysis demonstrated elevation of Al and other toxic element content, using blood and urine is highly required in order to highlight the exposure levels in details; 2) dietary intake of trace elements should be taken into account to reveal the contribution of environmental exposure into the total level of toxic metals and metalloids in the examinees; 3) the presence of other industries (petrochemical, ferroalloy) may also have a significant impact on trace element status of people, therefore, investigation of the impact of these industries is also required. 5. Conclusions Generally, the obtained data demonstrate: 1) Workers of aluminium plant are characterized by higher hair Al levels in comparison to occupationally non-exposed controls; 2) Hair Cd, Pb, and Sn values in persons involved in primary aluminium production exceeded those in the controls; 3) The level of Al, Cd, Pb, and Sn in men working in the sintering unit of aluminium plant was higher in comparison to both hydrometallurgical unit workers and occupationally non-exposed persons. Conflict of interest The authors declare no conflict of interest Acknowledgements The research was funded by the Ministry of Healthcare and Social Development of Kazakhstan within the program “Protection of labor rights of workers in hazardous and heavy working conditions and development a set of interrelated socio-economic, organizational, technical and preventive measures for health and safety management to ensure a safe and healthy environment for efficient and high-quality work” (0001/PPF-15MHSD/0-15-OS). 5
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
Appl. Occup. Environ. Hyg. 16 (1) (2001) 66–77. [44] A.V. Skalny, M.G. Skalnaya, A.A. Tinkov, E.P. Serebryansky, V.A. Demidov, Y.N. Lobanova, A.R. Grabeklis, E.S. Berezkina, I.V. Gryazeva, A.A. Skalny, Reference values of hair toxic trace elements content in occupationally non-exposed Russian population, Environ. Toxicol. Pharmacol. 40 (1) (2015) 18–21. [45] M.D.Axelsson Rodushkin, Application of double focusing sector field ICP-MS for multielemental characterization of human hair and nails. Part II. A study of the inhabitants of northern Sweden, Sci. Total Environ. 262 (1) (2000) 21–36. [46] J.-P. Goullé, L. Mahieu, J. Castermant, N. Neveu, L. Bonneau, G. Lainé, D. Bouige, C. Lacroix, Metal and metalloid multi-elementary ICP-MS validation in whole blood, plasma, urine and hair: reference values, Forensic Sci. Int. 153 (1) (2005) 39–44. [47] E. Tamburo, D. Varrica, G. Dongarrà, Coverage intervals for trace elements in human scalp hair are site specific, Environ. Toxicol. Pharmacol. 39 (1) (2015) 70–76. [48] J. Morton, V.A. Carolan, P.H. Gardiner, Removal of exogenously bound elements from human hair by various washing procedures and determination by inductively coupled plasma mass spectrometry, Anal. Chim. Acta 455 (1) (2002) 23–34. [49] H. Röllin, P. Theodorou, T. Kilroe-Smith, The effect of exposure to aluminium on concentrations of essential metals in serum of foundry workers, Occup. Environ. Med. 48 (4) (1991) 243–246. [50] F. Metwally, M. Mazhar, Effect of aluminium on the levels of some essential elements in occupationally exposed workers, Arh Hig Rada Toksikol 58 (3) (2007) 305–311.
[33] G. Benke, M. Abramson, M. Sim, Exposures in the alumina and primary aluminium industry: an historical review, Ann. Occup. Hyg. 42 (3) (1998) 173–189. [34] IARC working group on the evaluation of carcinogenic risks to humans, humans, arsenic, metals, fibres, and dusts, IARC Monogr. Eval. Carcinog. Risks Hum. 94 (2012) 1–412. [35] J. Healy, S. Bradley, C. Northage, E. Scobbie, Inhalation exposure in secondary aluminium smelting, Ann. Occup. Hyg. 45 (3) (2001) 217–225. [36] B. Maňkovská, E. Steinnes, Effects of pollutants from an aluminium reduction plant on forest ecosystems, Sci. Total Environ. 163 (1-3) (1995) 11–23. [37] N.N. Gow, G.P. Lozej, Bauxite, Geosci. Can. 20 (1) (1993) 9–16. [38] M. Grafe, R. Tappero, M. Landers, B. Gan, P. Austin, Z. Taylor, C. Klauber, Micronscale characterization of minerals, metals and processes in bauxite residue, Travaux 36 (40) (2011) 15–27. [39] B. Engel, G. Lalor, M. Vutchkov, Spatial pattern of arsenic and lead distributions in Jamaican soils, Environ. Geochem. Health 18 (3) (1996) 105–111. [40] G.C. Lalor, Review of cadmium transfers from soil to humans and its health effects in the Jamaican environment, Sci. Total Environ. 400 (1) (2008) 162–172. [41] J. Morton, E. Leese, R. Cotton, N. Warren, J. Cocker, Beryllium in urine by ICP-MS: a comparison of low level exposed workers and unexposed persons, Int. Arch. Occup. Environ. Health 84 (6) (2011) 697–704. [42] N.P. Skaugset, D.G. Ellingsen, K. Dahl, I. Martinsen, L. Jordbekken, P.A. Drabløs, Y. Thomassen, Occupational exposure to beryllium in primary aluminium production, J. Environ. Monit. 14 (2) (2012) 353–359. [43] H.B. Westberg, A.I. Seldén, T. Bellander, Exposure to chemical agents in Swedish aluminum foundries and aluminum remelting plants? A comprehensive survey,
6
Contents lists available at ScienceDirect
Journal of Trace Elements in Medicine and Biology journal homepage: www.elsevier.com/locate/jtemb
Toxicology
Assessment of hair metal levels in aluminium plant workers using scalp hair ICP-DRC-MS analysis Anatoly V. Skalnya,b,c, Galina A. Kaminskayad, Tatyana I. Krekeshevad, Sholpan K. Abikenovad, ⁎ Margarita G. Skalnayac,e, Anatoly T. Bykove, Alexey A. Tinkova,c, a
Yaroslavl State University, Yaroslavl, Russia All-Russian Research Institute of Medicinal and Aromatic Plants (VILAR), Moscow, Russia c Peoples’ friendship university of Russia (RUDN University), Moscow, Russia d National Institute for Occupational Safety, Astana, Kazakhstan e Kuban State Medical University, Krasnodar, Russia b
A R T I C LE I N FO
A B S T R A C T
Keywords: Primary aluminium production Exposure Cadmium Lead Arsenic Risk
The objective of the present study was to assess the level of aluminium and toxic metals in hair of workers occupationally exposed to aluminium. 124 employees of the aluminium plant working in the hydrometallurgical (n = 43) and sintering units (n = 41), as well as 40 occupationally nonexposed controls were examined. Hair aluminium (Al), arsenic (As), beryllium (Be), cadmium (Cd), mercury (Hg), nickel (Ni), lead (Pb), and tin (Sn) content was assessed using inductively-coupled plasma mass spectrometry. The obtained data demonstrate that aluminium plant workers had significantly higher levels of hair Al (28.8 (15.4–58.6) vs 7.8 (4.3–14.2) μg/g, p < 0.001), Cd (0.053 (0.032 – 0.095) vs 0.025 (0.014 – 0.043) μg/g, p < 0.001) and Pb (0.672 (0.299–1.310) vs 0.322 (0.170 – 0.609) μg/g, p = 0.012) than the controls, respectively. Further analysis demonstrated that persons involved in different technological processes were characterized by distinct hair metal profiles. Hair Al, Be, Cd, Ni, Pb, and Sn levels in men working in the sintering unit of the aluminium plant exceeded the respective control values. In turn, workers of the hydrometallurgical unit were characterized by more than 2-fold higher levels of Al and Cd in hair as compared to the controls. The results of the present study demonstrate that workers of the aluminium plant are characterized by increased risk of Al as well as As, Cd, Pb, and Sn exposure.
1. Introduction Aluminium is the widespread metal comprising 8.23% of the Earth’s crust by weight [1]. Due to its physical and chemical properties it is widely used in various fields of modern industry including construction, food production, electronics, pharmacy, etc. [2]. Production of aluminium (both primary and secondary) is increasing worldwide [3]. In particular, global consumption of aluminium has increased from 29 Mt in 1994 to 45 Mt in 2004. The top-5 consumers of Al are USA, China, Japan, Germany, and Russia. In turn, the main producers of bauxite and alumina are Australia, Brazil, and China. Kazakhstan is also rich in bauxite reserves and its production [4]. In 2007, bauxite reserves in Kazakhstan were estimated to be 200 Mt, accounting for 1% of total value worldwide. At the same time, the total value of bauxite produced in Kazakstan accounted for 3% of global production (4.7 Mt) [4,5]. At the same time, aluminium exposure also has a significant adverse effect on human health [2] due to its prooxidant, proinflammatory, ⁎
excitotoxic and immune-modulatory properties [6]. The growing body of data demonstrate that aluminium may have neurotoxic effects [7]. However, association between Al exposure and Alzheimer’s disease or autism is still questionable [8]. Moreover, the existing studies demonstrate a link between aluminium and breast cancer [9]. Evidence on the association between occupational aluminium exposure and pulmonary fibrosis [10], lung cancer [11], and neurological dysfunction [12] exist. Therefore, monitoring of human exposure to aluminium is of great importance. Hair is widely used for biomonitoring of metal exposure due to a number of advantages like high mineralization and irreversible incorporation of metals into hair matrix [13]. In contrast to blood and urine, where metal levels are strictly regulated by homeostatic mechanisms [14], hair may be used for assessment of exposure history for several months due to accumulation of metals [15]. In addition, due to ability to absorb metals from environment hair may be used in biomonitoring studies [16]. Previous data demonstrate that hair may be used as a valuable marker of occupational exposure to metals and
Corresponding author. E-mail addresses: [email protected], [email protected] (A.A. Tinkov).
https://doi.org/10.1016/j.jtemb.2018.06.014 Received 7 September 2017; Received in revised form 14 June 2018; Accepted 15 June 2018 0946-672X/ © 2018 Elsevier GmbH. All rights reserved.
Please cite this article as: Skalny, A.V., Journal of Trace Elements in Medicine and Biology (2018), https://doi.org/10.1016/j.jtemb.2018.06.014
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
current and former smoking; ii) excessive alcohol consumption; iii) acute and chronic infectious diseases (including gastritis that requires the use of alumunium-containing antacids); iv) surgical and traumatic diseases; v) metallic implants (including dental amalgams); vi) endocrine disorders; vii) vegetarianism and other specific dietary patterns (including the use of herbs that may be the source of alumunium); viii) dyed hair. Therefore, only healthy workers of aluminium plant and control persons were enrolled in the current study. Data on health condition are collected yearly during mandatory physical examination. The aluminium plant is the one of the ten largest producers of alumina in the world. The plant produces up to 1.7 million tons of metallurgic alumina that is exported to China and Russia. At the moment of investigation, the total number of employees of aluminium plant was 6,117, whereas 1262 of them were working in hazardous conditions. The system of health protection and safety is implemented in the plant. All employees are equipped with personal protective equipment: coveralls, safety shoes, gloves, helmet, balaclava, protective goggles, respirator, safety belt, dielectric bots, antinoise headphones (all protective equipment is certified No. KZ 41400285, No KZ 41400348). The overalls are cleaned by the plant’s laundry. All units are equipped with the sanitary facilities (wardrobe, shower room, dining room). The collective protective equipment includes aspiration and exhaust ventilation systems, noise protection system, as well as system of prevention of electrical damage. All persons working in hazardous conditions receive milk that is widely used for health protection in hazardous occupational conditions, as well as detergents (soap, powders). All protective activities are controlled by internal and external commissions. Indoor atmospheric pollution is regularly monitored by the environmental laboratory and the data obtained are compared with the existing maximum permissible concentrations (MPC). The results of monitoring demonstrate that the rate of indoor environmental pollution is within the limits provided by national regulations (Table 1). All employees are provided with similar meals in the dining room. The dining room is equipped with ceramic dish and stainless steel kitchen utensils, whereas the use of aluminium utensils is avoided. Tap water is used for drinking and preparation of meals. Systematic analysis of tap water demonstrates that the level of the studied metals is lower than MPC [24]. Hair sampling was performed after regular mandatory physical examination of the workers that excluded occupational and non-occupational pathology. All examinees have washed their hair at the day of sampling using their usual commercially available shampoos. Despite different chemical composition of shampoos, their use did not significantly affect hair metal content [25]. Occipital scalp hair samples were collected using ethanol-precleaned stainless scissors. Only proximal parts of strands were used for analysis. Prior to digestion, the hair samples were subjected to washing with acetone with subsequent rinsing with distilled deionized water for three times and drying in the air (60 °C). The existing data demonstrate that such type of washing procedure removes mechanical contamination (dust) but does not remove metals bound to hair matrix [26]. A total of 50 mg of washed hair samples were introduced into Teflon tubes containing concentrated nitric acid (HNO3). Digestion procedure was performed in Berghof Speedwave 4 (Berghof Products & Instruments, Germany) system at 170–180 °C for 20 min. The obtained
metalloids [17,18]. Moreover, the hair metal level was also shown to be associated with adverse health effects in occupationally exposed persons [19]. Taking into account the toxic effects of metal co-exposure [20], other toxic metals should be also monitored in persons exposed to aluminium. Therefore, the objective of the present study was to assess the level of aluminium and other toxic elements in hair of persons occupationally exposed to aluminium. 2. Materials and methods The protocol of the present investigation was approved by the Local Ethics Committee. The sampling and experimental procedures were performed in agreement with the principles of the Declaration of Helsinki and later amendments. All participants have provided informed consent prior to the examination. A total of 124 men took part in the present study. 84 employees of the aluminium plant in North-Eastern Kazakhstan working in the hydrometallurgical (n = 43) and sintering units (n = 41) of the plant presented the occupationally exposed groups. Briefly, the main technological process in the hydrometallurgical unit is the production of alumina from bauxite using the Bayer process. In turn, sintering unit performs recovery of alumina from Bayer red mud [21]. In 2012, the total amount of bauxite, aluminium oxide, and aluminium produced by the studied plant was 5.17, 1.51, and 0.249 Mt [5]. 40 healthy men living in more than 1.0 km from the plant in the north-western part of the city and not involved in industrial processes were used as the occupationally non-exposed controls (Fig. 1). The examinees in all groups were age- and body mass index (BMI)-matched to prevent the influence of ageing [22] and obesity [23] on hair metal levels. Age and BMI in the controls, hydrometallurgical and sintering unit workers were 36.6 ± 10.2 years and 24.7 ± 3.5 kg/m2, 36.3 ± 11.1 years and 24.5 ± 4.4 kg/m2, and 36.0 ± 11.3 years and 24.3 ± 5.2 kg/m2, respectively. No significant difference in working experience between the hydrometallurgical (11 ± 6 years) and sintering unit (9 ± 5 years) workers was detected. In addition, to avoid the influence of side factors on hair metal levels, the following exclusion criteria were used: i)
Table 1 Data on atmospheric pollution monitoring of the working environment.
Fig. 1. Location of the aluminium plant (filled box) and the areas of control species sampling (empty box). 2
Parameter
MPC
Hydrometallurgical unit
Sintering unit
Alkaline aerosol (mg/m3) Abrasive dust (mg/m3) Metal dust (mg/m3) Alumina dust (mg/m3)
0.5 6 10 6
0.14 ± 0.04 2.8 ± 0.9 2.3 ± 0.8 3.8 ± 2.0
0.14 ± 0.06 3.3 ± 1.2 4.1 ± 1.5 5.4 ± 2.1
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
by more than 2-fold higher levels of Al as compared to the controls. The hair content of Cd significantly exceeded the control values by 63%, whereas hair Pb levels were nearly 2-fold higher. The level of Be, As, Hg, Ni, and Sn in hair of men working in the hydrometallurgical unit of the aluminium plant did not differ significantly from those in occupationally non-exposed persons. Hair metal content in the sintering unit workers also significantly exceeded that in men working in hydrometallurgical unit. In particular, the level of Al, Cd, Ni, and Pb in hair of sintering unit workers exceeded the hydrometallurgical unit values by 76%, 45%, 46%, and 9%, respectively. In turn, hair levels of Be and Sn in men involved in sintering were nearly 10- and 3-fold higher in comparison to those in workers of another unit of aluminium plant. Correlation analysis demonstrated that hair Al levels of the studied population were characterized by a significant correlation with hair Be and Pb content (Table 3). At the same time, no significant correlation was observed between hair Al and As, Cd, Hg, Ni, or Sn levels. Analysis of correlation between hair metal levels in workers of the aluminium plant demonstrated that hair Al content is directly associated with As, Be, Ni, and Pb, whereas no significant interaction with Cd, Hg, and Sn levels was observed.
samples were added to a total volume of 15 ml with distilled deionized water and subjected to analysis. The level of aluminium (Al), arsenic (As), beryllium (Be), cadmium (Cd), mercury (Hg), nickel (Ni), lead (Pb), and tin (Sn) content was assessed using inductively coupled plasma mass spectrometry (ICP-MS) with NexION 300D (PerkinElmer Inc., Shelton, CT 06484, USA) equipped with the 7-port FAST valve and ESI SC-2 DX4 autosampler (Elemental Scientific Inc., Omaha, NE 68122, USA). The use of Dynamic Reaction Cell in ICP-MS (ICP-DRC-MS) technology allowed to remove the majority of atomic interferences. The ICP-MS system was conditioned and calibrated in accordance with the manufacturer’s manual via external calibration. The external calibration solutions containing 0.5, 5, 10 and 50 μg/l of metals were freshly prepared from the Universal Data Acquisition Standards Kits (PerkinElmer Inc., Shelton, CT 06484, USA) by dilution with distilled deionized water and subsequent acidification with 1% HNO3. Taking into account incomplete acidity and viscosity matching between calibration and sample matrices the online internal standardization with yttrium-89 and rhodium-103 was used via 7-port FAST valve. The internal standard solution containing 10 ppb Y and Rh was prepared from Yttrium (Y) Pure Single-Element Standard and Rhodium (Rh) Pure Single-Element Standard (PerkinElmer Inc., Shelton, CT 06484, USA), respectively. Laboratory quality control was regularly performed using the certified reference material of human hair GBW09101 (Shanghai Institute of Nuclear Research, Shanghai, China). The recovery rates for all metals exceeded 85%. The laboratory also takes part in external quality assessment schemes in occupational and environmental laboratory medicine (OELM). All analyses are performed in clean laboratory environment (air filtration, exhaust ventilation). The obtained data were treated with Statistica 10.0 (Statsoft, Tulsa, OK, USA). Shapiro-Wilk test was used for assessment of data normality. As the distribution was found to be non-Gaussian, median and the respective 25 and 75 percentile boundaries were used for expression of hair metal levels. Group comparison was performed using MannWhitney U test The differences were considered significant at the level of p < 0.05.
4. Discussion Generally, the obtained data demonstrate that involvement in aluminium production was associated with increased levels of Al, Cd, Pb, and Sn levels in hair of workers. The obtained data are in agreement with previous study of hair aluminium levels in aluminium-exposed persons [27]. Earlier studies have detected a significant impact of occupational exposure to aluminium on the level of metal in the organism. In particular, it has been shown that workers of the aluminium industry are characterized by a significant elevated serum and urinary Al levels [28]. Similarly, increased serum Al concentrations were observed in persons exposed to Bayer-process alumina for a long period [29]. Assessment of plasma Al levels by flameless atomic absorption spectrometry revealed a significant increase in electrolysis-workers in comparison to non-exposed persons. It has been also noted that the total exposure time at the workplace correlates with plasma Al concentration at r = 0.4 [30]. The authors also state that occupational exposure to Al in anode changer not wearing a mask is associated with increased urinary Al levels [0]. Moreover, it has been stated that persons directly exposed to Al are characterized by significantly higher serum Al concentrations as compared to both indirectly exposed and non-exposed examinees [31]. Oppositely, another study examining workers of the bauxite mines did not reveal any significant difference in serum Al level in comparison to the group of non-exposed wood processors [32]. In parallel with increased hair Al levels, we have detected significantly elevated levels of As, Cd, Pb, and Sn in scalp hair of aluminium plant workers. These findings at least partially correspond to the results of the earlier studies, demonstrating the association between primary aluminium industry and Be, Cd, Ni, Hg, and Pb exposure [33,34]. In particular, it has been demonstrated that persons involved in secondary Al smelting may be exposed both to Al and Pb [35]. Biomonitoring studies also revealed a significant influence of aluminium production industry on the level of heavy metals in forest ecosystem. In particular, the level of Cd and Pb in plants and phytophagous insects was increased. Similarly, teeth and hair As, Cd, and Pb content was increased in roe-deers living in the aluminium plant region [36]. Simultaneous exposure of workers to various metals during Al production may be associated with the chemical composition of bauxite and its residues. Despite the fact that Al is the main metal constituent of bauxite, the latter also contains large amounts of Fe, Ti, and other metals [37]. It has been demonstrated that bauxite residues from a Western Australian refinery contain a significant amount of As (50 ppm), although being less abundant than Cr (650 ppm). At the same time, taking into account the higher solubility of As compounds the
3. Results The obtained data demonstrate that aluminium plant workers were characterized by significantly elevated hair metal levels (Fig. 2). In particular, the workers had more than 3-fold higher levels of hair Al content as compared to the occupationally non-exposed controls (28.8 (15.4–58.6) vs 7.8 (4.3–14.2) μg/g, p < 0.001). Hair Cd and Pb levels in aluminium plant employees exceeded the control group values by a factor of more than two (0.053 (0.032–0.095) vs 0.025 (0.014–0.043) μg/g, p < 0.001, and 0.672 (0.299–1.310) vs 0.322 (0.170–0.609) μg/ g, p = 0.012). Hair levels of Sn in occupationally-exposed persons exceeded the control values by 46% (0.118 (0.058–0.254) vs 0.081 (0.057–0.121) μg/g, p = 0.038). At the same time, hair As (0.044 (0.027–0.077) vs 0.042 (0.028 – 0.074) μg/g, p = 0.826), Be (0.0003 (0.0001–0.0012) vs 0.0004 (0.0001–0.0008) μg/g, p = 0.959), Hg (0.18 (0.13 – 0.33) vs. 0.20 (0.12–0.29) μg/g, p = 0.670), and Ni (0.268 (0.200–0.387) vs 0,226 (0.171–0.342) μg/g, p = 0.455) content in the occupationally exposed group did not differ significantly from the control values. Further analysis demonstrated that persons involved in different technological processes were characterized by distinct hair metal profiles (Table 2). In particular, hair Al, Be, Cd, Pb, and Sn levels in men working in the sintering unit of the aluminium plant exceeded the respective control values by the factors of nearly 4, 5, 2, 2, and 2. Hair Ni levels in the sintering unit workers were 45% higher as compared to the control level. The level of As and Hg in the sintering unit workers did not differ significantly from the control values. In turn, workers of the hydrometallurgical unit were characterized 3
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
Fig. 2. Hair metal levels in workers of the aluminium plant and occupationally non-exposed controls. The graph represents Median (25–75). Individual p values are indicated as assessed by Mann-Whitney U test Line – Median, Box – 25–75 percentile range, Whisker – Non-outlier range. C – control; A – aluminium plant workers.
Despite the fact that the level of metals in hair of aluminium plant workers was significantly higher than that of the controls, only hair Al values exceeded the background reference values for hair metals in Russia [44], Sweden [45], Poland [13], and France [46]. Taking into account the site specificity of hair metal content [47], the obtained data should be compared to the reference values of hair metal content in Kazakshtan, that seem to be lacking. However, the results of regular municipal monitoring of water and food metal content did not reveal any elevation of Al content exceeding the MPC. Taking into account a complex system of health protection aimed at prevention of excessive administration of aluminium and other toxic elements, the observed increase in hair Al levels may be indicative of cumulative external binding of Al to hair matrix due to emission of Al-
authors proposed that potential health effects of bauxite residues may be caused by As rather than Cr [38]. In addition, high As, Pb [39], and Cd [40] content was reported in bauxitic soils from Jamaica. We observed significantly increased levels of Be in hair of workers of the sintering unit, but not hydrometallurgical unit, being in contrast to earlier indication of exposure to Be in primary aluminium production [41,42]. The results of the present study also demonstrate that workers of sintering unit are characterized by significantly higher hair levels of metals than persons working in hydrometallurgical unit and non-exposed controls. The observed situation may be associated with significant difference in concentrations of aluminium and other chemical agents in air of units performing distinct technological processes [43].
Table 2 Hair metal levels (μg/g) in workers of different units of aluminium plant and occupationally non-exposed controls. Metal
Control (n = 40)
Hydrometallurgical unit (n = 43)
Sintering unit (n = 41)
Al As Be Cd Hg Ni Pb Sn
7.8 (4.3–14.2) 0.042 (0.028–0.074) 0.0002 (0.0001–0.0003) 0.025 (0.014–0.043) 0.192 (0.134–0.420) 0.226 (0.171–0.342) 0.322 (0.170–0.609) 0.081 (0.0570.121)
19.3 (9.68–42.8)* 0.041 (0.025–0.068) 0.0001 (0.0001–0.0002) 0.042 (0.027–0.073)* 0.204 (0.095–0.350) 0.224 (0.142–0.337) 0.633 (0.208–1.096)* 0.063 (0.046–0.125)
34.0 (21.3–80.2)*,† 0.051 (0.034–0.100) 0.0010 (0.0007–0.0017)*,† 0.060 (0.042–0.150)*,† 0.217 (0.134–0.304) 0.327 (0.237–0.430)*,† 0.687 (0.432–1.716)*,† 0.173 (0.118–0.386)*,†
Data expressed as median (25–75). * significant difference in comparison to Control values at p < 0.05. † significant difference in comparison to sintering unit values at p < 0.05. 4
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
References
Table 3 Correlation between hair Al and toxic metal levels. Element
As Be Cd Hg Ni Pb Sn
General cohort
[1] K.J. Orians, K.W. Bruland, Dissolved aluminium in the central North Pacific, Nature 316 (6027) (1985) 427–429. [2] D. Krewski, R.A. Yokel, E. Nieboer, D. Borchelt, J. Cohen, J. Harry, S. Kacew, J. Lindsay, A.M. Mahfouz, V. Rondeau, Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide, J. Toxicol. Environ. Health B Part. B 10 (S1) (2007) 1–269. [3] H. Bergsdal, A.H. Strømman, E.G. Hertwich, The Aluminium Industry-Environment, Technology and Production, IndEcol, Trondheim, Norway, 2004. [4] Z. Luo, A. Soria, Prospective study of the world aluminium industry, JRC Sci. Tech. Rep. (2007) 71. [5] P. von Hartlieb‐Wallthor, Market report on Kazakhstan, Min. Rep. 150 (4) (2014) 234–238. [6] S.J. Flora, Toxic metals: health effects, and therapeutic measures, J. Biomed. Ther. Sci. 1 (1) (2014) 48–64. [7] C. Exley, What is the risk of aluminium as a neurotoxin? Expert Rev. Neurother. 14 (6) (2014) 589–591. [8] C. Exley, The toxicity of aluminium in humans, Morphologie 100 (329) (2016) 51–55. [9] P.D. Darbre, F. Mannello, C. Exley, Aluminium and breast cancer: sources of exposure, tissue measurements and mechanisms of toxicological actions on breast biology, J. Inorg. Biochem. 128 (2013) 257–261. [10] P.V. De, P. Dumortier, F. Rickaert, R. de Weyer, C. Van, J.C. Lenclud, Yernault, Occupational lung fibrosis in an aluminium polisher, Eur. J Respir. Dis. 68 (1986) 131–140. [11] B. Armstrong, C. Tremblay, D. Baris, G. Thériault, Lung cancer mortality and polynuclear aromatic hydrocarbons: a case-cohort study of aluminum production workers in Arvida, Quebec, Can. Am. J. Epidemiol. 139 (1994) 250–262. [12] D.M. White, W.T. Longstreth, L. Rosenstock, K.H. Claypoole, C.A. Brodkin, B.D. Townes, Neurologic syndrome in 25 workers from an aluminum smelting plant, Arch. Int. Med. 152 (1992) 1443–1448. [13] K. Chojnacka, A. Zielińska, H. Górecka, Z. Dobrzański, H. Górecki, Reference values for hair minerals of Polish students, Environ. Toxicol. Pharmacol. 29 (3) (2010) 314–319. [14] I.B.-A. Razagui, I. Ghribi, Maternal and neonatal scalp hair concentrations of zinc, copper, cadmium, and lead, Biol. Trace Elem. Res. 106 (1) (2005) 1–27. [15] S. Foo, N. Khoo, A. Heng, L. Chua, S. Chia, C. Ong, C. Ngim, J. Jeyaratnam, Metals in hair as biological indices for exposure, Int. Arch. Occup. Environ. Health 65 (1) (1993) S83–S86. [16] E. Tamburo, G. Dongarrà, D. Varrica, D. D’Andrea, Trace elements in hair of urban schoolboys: a diagnostic tool in environmental risk assessment, Geophys. Res. Abstr. (2011) 1157. [17] R. Mehra, M. Juneja, Elements in scalp hair and nails indicating metal body burden in polluted environment, J. Sci. Ind. Res. 64 (2) (2005) 119–124. [18] A.R. Grabeklis, A.V. Skalny, S.P. Nechiporenko, E.V. Lakarova, Indicator ability of biosubstances in monitoring the moderate occupational exposure to toxic metals, J. Trace Elem. Med. Biol. 25 (2011) S41–S44. [19] R. Mehra, M. Juneja, Adverse health effects in workers exposed to trace/toxic metals at workplace, Indian J. Biochem. Biophys. 40 (2003) 131–135. [20] R. Altenburger, Understanding combined effects for metal Co-exposure in ecotoxicology, in: A. Sigel, H. Sigel (Eds.), Metal Ions in Toxicology: Effects, Interactions, Interdependencies, Royal Society of Chemistry, Great Britain, 2010, pp. 1–26. [21] X.-b. Li, X. Wei, L. Wei, G.-h. Liu, Z.-h. Peng, Q.-s. Zhou, T.-g. Qi, Recovery of alumina and ferric oxide from Bayer red mud rich in iron by reduction sintering, Trans. Nonferrous Met. Soc. China 19 (5) (2009) 1342–1347. [22] M.G. Skalnaya, A.A. Tinkov, V.A. Demidov, E.P. Serebryansky, A.A. Nikonorov, A.V. Skalny, Age-related differences in hair trace elements: a cross-sectional study in Orenburg, russia, Ann. Hum. Biol. 43 (5) (2016) 438–444. [23] M.G. Skalnaya, A.A. Tinkov, V.A. Demidov, E.P. Serebryansky, A.A. Nikonorov, A.V. Skalny, Hair toxic element content in adult men and women in relation to body mass index, Biol. Trace Elem. Res. 161 (1) (2014) 13–19. [24] Informational Bulletin on Environment in Kazakhstan Republic in 2016, (2016) Kazhydromet, Kazakhstan. [25] A. LeBlanc, P. Dumas, L. Lefebvre, Trace element content of commercial shampoos: impact on trace element levels in hair, Sci. Total Environ. 229 (1) (1999) 121–124. [26] L.-J. Zhao, T. Ren, R.-G. Zhong, Determination of lead in human hair by high resolution continuum source graphite furnace atomic absorption spectrometry with microwave digestion and solid sampling, Anal. Lett. 45 (16) (2012) 2467–2481. [27] M. Wilhelm, J. Passlick, T. Busch, M. Szydlik, F. Ohnesorge, Scalp hair as an indicator of aluminium exposure: comparison to bone and plasma, Hum. Toxicol. 8 (1) (1989) 5–9. [28] H.J. Gitelman, F.R. Alderman, M. Kurs-Lasky, H.E. Rockette, Serum and urinary aluminium levels of workers in the aluminium industry, Ann. Occup. Hyg. 39 (2) (1995) 181–191. [29] D. Waldron-Edward, P. Chan, S. Skoryna, Increased prothrombin time and metabolic changes with high serum aluminum levels following long-term exposure to Bayer-process alumina, Can. Med. Assoc. J. 105 (12) (1971) 1297. [30] C. Schlatter, A. Steinegger, U. Rickenbacher, C. Hans, A. Lengyel, Aluminium levels in the blood plasma of persons working in the aluminium industry, Environ. Geochem. Health 12 (1-2) (1990) 59–64. [31] W. Ruangyuttikarn, P. Pongraveevongsa, P. Winitchakoon, Serum aluminium in alumina exposed workers, J. Med. Assoc. Thai 85 (8) (2002) 928–934. [32] J.F. DeKom, H.M. Dissels, G.B. Van DerVoet, F.A. De Wolff, Serum aluminium levels of workers in the bauxite mines, J. Toxicol. Clin. Toxicol. 35 (6) (1997) 645–651.
Aluminium plant workers
r
p
r
p
−0.041 0.366 0.109 −0.021 0.073 0.253 −0.050
0.652 < 0.001* 0.230 0.820 0.425 0.011* 0.580
0.545 0.423 0.084 0.002 0.195 0.155 −0.082
< 0.001* < 0.001* 0.278 0.980 0.011* 0.045* 0.292
Data expressed as correlation coefficients (r) and the respective p values. * Correlation is significant at p < 0.05.
containing dust into the occupational environment. In particular, it has been demonstrated that atmospheric metals are able to bind hair matrix irreversibly and may not be removed by washing procedures [26,48]. Therefore, workers of aluminium plant may have an increased risk of cumulative Al as well as As, Cd, Pb, and Sn exposure in the case of disruption of personal and/or general health protection systems. Therefore, simultaneous monitoring of the conditions of the protective systems as well as the levels of these metals in aluminium plant workers is essential for prevention of possible toxic effects that may occur during metal co-exposure [20]. Moreover, the possibility of altered essential trace elements status in Al-exposed persons should be also taken into account [49,50]. However, kinetic studies involving hair, blood, and urine investigation are required to specify the mechanisms of increased hair Al levels. At the same time, the present study has certain limitations: 1) although hair metal analysis demonstrated elevation of Al and other toxic element content, using blood and urine is highly required in order to highlight the exposure levels in details; 2) dietary intake of trace elements should be taken into account to reveal the contribution of environmental exposure into the total level of toxic metals and metalloids in the examinees; 3) the presence of other industries (petrochemical, ferroalloy) may also have a significant impact on trace element status of people, therefore, investigation of the impact of these industries is also required. 5. Conclusions Generally, the obtained data demonstrate: 1) Workers of aluminium plant are characterized by higher hair Al levels in comparison to occupationally non-exposed controls; 2) Hair Cd, Pb, and Sn values in persons involved in primary aluminium production exceeded those in the controls; 3) The level of Al, Cd, Pb, and Sn in men working in the sintering unit of aluminium plant was higher in comparison to both hydrometallurgical unit workers and occupationally non-exposed persons. Conflict of interest The authors declare no conflict of interest Acknowledgements The research was funded by the Ministry of Healthcare and Social Development of Kazakhstan within the program “Protection of labor rights of workers in hazardous and heavy working conditions and development a set of interrelated socio-economic, organizational, technical and preventive measures for health and safety management to ensure a safe and healthy environment for efficient and high-quality work” (0001/PPF-15MHSD/0-15-OS). 5
Journal of Trace Elements in Medicine and Biology xxx (xxxx) xxx–xxx
A.V. Skalny et al.
Appl. Occup. Environ. Hyg. 16 (1) (2001) 66–77. [44] A.V. Skalny, M.G. Skalnaya, A.A. Tinkov, E.P. Serebryansky, V.A. Demidov, Y.N. Lobanova, A.R. Grabeklis, E.S. Berezkina, I.V. Gryazeva, A.A. Skalny, Reference values of hair toxic trace elements content in occupationally non-exposed Russian population, Environ. Toxicol. Pharmacol. 40 (1) (2015) 18–21. [45] M.D.Axelsson Rodushkin, Application of double focusing sector field ICP-MS for multielemental characterization of human hair and nails. Part II. A study of the inhabitants of northern Sweden, Sci. Total Environ. 262 (1) (2000) 21–36. [46] J.-P. Goullé, L. Mahieu, J. Castermant, N. Neveu, L. Bonneau, G. Lainé, D. Bouige, C. Lacroix, Metal and metalloid multi-elementary ICP-MS validation in whole blood, plasma, urine and hair: reference values, Forensic Sci. Int. 153 (1) (2005) 39–44. [47] E. Tamburo, D. Varrica, G. Dongarrà, Coverage intervals for trace elements in human scalp hair are site specific, Environ. Toxicol. Pharmacol. 39 (1) (2015) 70–76. [48] J. Morton, V.A. Carolan, P.H. Gardiner, Removal of exogenously bound elements from human hair by various washing procedures and determination by inductively coupled plasma mass spectrometry, Anal. Chim. Acta 455 (1) (2002) 23–34. [49] H. Röllin, P. Theodorou, T. Kilroe-Smith, The effect of exposure to aluminium on concentrations of essential metals in serum of foundry workers, Occup. Environ. Med. 48 (4) (1991) 243–246. [50] F. Metwally, M. Mazhar, Effect of aluminium on the levels of some essential elements in occupationally exposed workers, Arh Hig Rada Toksikol 58 (3) (2007) 305–311.
[33] G. Benke, M. Abramson, M. Sim, Exposures in the alumina and primary aluminium industry: an historical review, Ann. Occup. Hyg. 42 (3) (1998) 173–189. [34] IARC working group on the evaluation of carcinogenic risks to humans, humans, arsenic, metals, fibres, and dusts, IARC Monogr. Eval. Carcinog. Risks Hum. 94 (2012) 1–412. [35] J. Healy, S. Bradley, C. Northage, E. Scobbie, Inhalation exposure in secondary aluminium smelting, Ann. Occup. Hyg. 45 (3) (2001) 217–225. [36] B. Maňkovská, E. Steinnes, Effects of pollutants from an aluminium reduction plant on forest ecosystems, Sci. Total Environ. 163 (1-3) (1995) 11–23. [37] N.N. Gow, G.P. Lozej, Bauxite, Geosci. Can. 20 (1) (1993) 9–16. [38] M. Grafe, R. Tappero, M. Landers, B. Gan, P. Austin, Z. Taylor, C. Klauber, Micronscale characterization of minerals, metals and processes in bauxite residue, Travaux 36 (40) (2011) 15–27. [39] B. Engel, G. Lalor, M. Vutchkov, Spatial pattern of arsenic and lead distributions in Jamaican soils, Environ. Geochem. Health 18 (3) (1996) 105–111. [40] G.C. Lalor, Review of cadmium transfers from soil to humans and its health effects in the Jamaican environment, Sci. Total Environ. 400 (1) (2008) 162–172. [41] J. Morton, E. Leese, R. Cotton, N. Warren, J. Cocker, Beryllium in urine by ICP-MS: a comparison of low level exposed workers and unexposed persons, Int. Arch. Occup. Environ. Health 84 (6) (2011) 697–704. [42] N.P. Skaugset, D.G. Ellingsen, K. Dahl, I. Martinsen, L. Jordbekken, P.A. Drabløs, Y. Thomassen, Occupational exposure to beryllium in primary aluminium production, J. Environ. Monit. 14 (2) (2012) 353–359. [43] H.B. Westberg, A.I. Seldén, T. Bellander, Exposure to chemical agents in Swedish aluminum foundries and aluminum remelting plants? A comprehensive survey,
6