Primary aluminum production is one of the most important industries in the world with a total global production of 5438 thousand metric tonnes [1
]. The mechanism of the primary aluminum production is electrolytic reduction (Hall–Héroult process) of aluminum oxide–alumina (Al2
) dissolved in a molten fluoride electrolyte consisting of cryolite (Na3
) at a temperature of about 960 °C. Electrolytic reduction is a continuous process inside steel container cells coated with carbon. It gives pure liquid aluminum metal at the negative carbon electrode (cathode) and carbon dioxide (CO2
) at the positive carbon electrode (anode) [2
]. The anode slowly reacts under intense heat, carbon dioxide, and other gaseous emissions such as polycyclic aromatic hydrocarbons (PAH) and hydrogen fluoride (HF). Cell lines are situated in the potroom. Most current aluminum smelters use pre-bake anode technologies and the older plants use the Søderberg process [2
The purpose of the fluoride components in the electrolyte is to lower the melting point to operate the cells at a lower temperature. Aluminum fluoride (AlF3
) neutralizes the sodium oxide (Na2
O), which is an impurity in the alumina feed. Fluoride emissions increase as the excess AlF3
in the molten bath is increased [2
]. According to a summary risk assessment report, 99.6% of all AlF3
production is used by the aluminum industry [4
In general, the gastrointestinal tract is the major route of fluoride uptake; however, in the occupational environment, fluoride is released into the air from industrial processes and workers are exposed to these substances by inhalation in both gaseous and particulate forms [5
]. Emissions of fluoride dust (NaF, AlF3
, and unused cryolite) and fumes (PFCs and HF) dispersed into the occupational environment pose occupational health hazards [6
Fluoride contamination is common at industrial sites, especially aluminum factories (smelters). The occupational health control of primary aluminum workers being exposed to fluoride focuses on the measurement of the occupational environment exposure and biological monitoring of fluoride concentration in urine. Fluoride metabolism in humans is well understood and according to Villa et al. [7
], urinary fluoride excretion is the most important metabolic pathway for fluoride elimination from the body. The human body excretes rapidly about 50% absorbed amount of fluoride in urine (smaller amounts in feces, sweat and saliva) with a biological half-life of 2–9 h. The rest fluoride is deposited in the skeletal system and it is very slowly eliminated [8
Post-shift urinary fluoride is considered as an appropriate index for surveillance of exposure to fluoride in aluminum smelter [9
]. On the other hand, according to Aylward et al. [10
], urinary flow and creatinine excretion are strongly individual and may vary from person to person. Further, factors like age, dose, renal impairment, composition of diet, and genetics can modify fluoride metabolism and alter the intake and excretion balance [11
]. Secondary intake of fluoride in foods is also an important source even in non-contaminated areas. This can occur through consumption of tea and mineral water, by tobacco smoking and, in the pediatric population, also from toothpaste [12
]. Cigarette smoking and tea consumption increase urinary fluoride, both separately and when combined [13
]. In related research we have not found a detailed study that considered the effect of tobacco smoking on the fluoride content in the urine of primary aluminum workers. Generally, there is lack of information on the effect of tobacco smoking on fluoride levels in humans [13
]. According to the scoping review by Idowu et al. [11
], only a small proportion of previous studies investigated the association between fluoride intake and excretion. The research in this area should focus on detailed fluoride exposure and excretion sampling technique, and clearly define the relationship between intake and urinary excretion of fluoride.
The objectives of the present study were to measure the occupational exposure to fluoride in primary aluminum workers in the same smelter repeatedly over several years and to verify whether worker exposure to fluoride in the occupational environment is crucial for the absorption of fluorides and subsequent excretion in the urine. To examine the impact of fluoride exposure, the pre- and post-shift urinary fluoride concentrations were determined. The study also investigated the impact of tobacco smoking as the confounding factor of fluoride exposure. The research procedure and methodology were conducted in accordance with the requirements of the legislation of the Slovak republic [16
], for the assessment of occupational environment. Thereby, the partial objective of the investigation was to verify whether this monitoring of fluoride exposure is representative.
3. Results and Discussion
shows the descriptive statistics for all study participants (for each study participant´s data, see Appendix A
), group of smokers and non-smokers including measured data of air samples and urinary fluoride samples.
Among the monitored work positions in Table 1
there were no statistically significant differences (p
> 0.05) for measured fluoride concentrations (particulate and gas-phase fluoride) in the occupational air. Within the total fluoride exposure, workers are the most exposed to the particulate fluoride emissions. The highest total (particulate + gas phase) fluoride concentration (12.120 mg/m3
) was registered in anode replacement work position. Our findings are consistent with the assumption that during anode replacement the worker is temporarily exposed to the open environment of the steel container and despite the increased efficiency of the air conditioning, the highest rate of fluoride exposure occurs in this operation. By contrast, the lowest concentration (0.018 mg/m3
) was found for the crane operator who is relatively isolated from direct exposure in the crane cabin.
A similar conclusion was reached by Ehrnebo and Ekstrand [22
] who investigated 41 workers in an aluminum plant in Sweden during an eight-hour work shift; the mean total fluoride exposure in this study was 0.91 mg/m3
, of which 34% was HF. For comparison, Seixas et al. [9
] found mean particulate fluoride and gas-phase fluoride (HF) concentrations were 4.1 and 0.7 mg/m3
when they evaluated the relationship between particulate fluoride exposure and urinary excretion in an aluminum smelter.
Contrary to determined distribution of particulate and gas-phase fluoride in the occupational environment of investigated potroom, the Risk assessment report [4
] concluded that the average fluoride emission of a primary aluminum smelter within the EU consists of 53% HF and 47% particulate fluoride. This may be explained due to the composition of study participants. The majority of workers were exposed to emissions during anode replacement in cells, including the particulates during crust cleaning of the anode cavity before installing new anodes. Gas-phase fluoride is formed in electrolysis process directly in the cell and it is emitted especially during anode replacement process; however, particulates are formed from handling by application of cryolite powder in the molten bath mixture and when crust is disrupted. Crust is a solid matter transformed from anode covering material by heat [23
The Kruskal–Wallis test (K-W test) showed that there was no statistically significant difference (p
= 0.57) in particulate fluoride concentrations in the monitored years of the research. However, gas-phase concentrations were statistically significantly different (p
= 0.003). As can be seen in Figure 1
, this was due to increased gas-phase fluoride concentrations in 2014 (an approximately five times higher mean value compared to other years).
Occupational Safety and Health Administration (OSHA) permissible exposure limit (PEL) of fluorides (as F) at a value of 2.5 mg/m3
(as time-weighted average) was exceeded (2.67–10.29) in 10 workers (see Appendix A
]. Compared to the general population, inhalation of fluoride present in ambient air does not contribute more than 0.01 mg per day to the total fluoride intake [25
]. Since 1996, long-term average annual concentrations of fluorides in ambient air are <1 µg/m3
in the district of Žiar nad Hronom [12
shows a comparison of mean ± SE urinary fluoride concentrations during the research period. No statistically significant difference (p
> 0.05) was found for either pre- or post-shift urinary fluoride over the monitored years.
The most effective way to examine fluoride exposure provides the relation between the concentration in the air and the quantities excreted in the urine at the end of the shift [27
The results of correlation analysis between fluoride exposure in the occupational environment (i.e., by inhalation) and corresponding urinary fluoride levels in monitored participants are presented in Table 3
and Figure 3
No significant correlation between fluoride concentrations in the occupational environment and in urine corrected to creatinine was found in the present study. Pierre et al. [27
] reported an association between fluoride concentration of 2.5 mg/m3
(OSHA PEL) in an occupational environment and post-shift urinary fluoride concentration of 6.4 mg/g creatinine, and a peak value of 7.4 mg/g creatinine, respectively. As mentioned above, our results showed OSHA PEL exceeded in 10 workers. In contrast with Pierre et al. [27
], post-shift urinary fluoride levels in this workers reached only 0.2–1.2 mg/g creatinine and peak post-shift urinary fluoride 3.73 mg/g creatinine corresponds to 0.16 mg/m3
of total fluoride concentration in the occupational environment. More than 50% exceeded samples above OSHA PEL were associated with anode handling working position (i.e., anode replacement, cell operator). Post-shift urinary fluoride levels in these workers proved that personal respiratory protection used during high exposure periods while working over open cells was effective. A similar conclusion was reached by Seixas et al. [9
] who ascribed the lack of relationship between particulate fluoride exposure and the post-shift urinary fluoride by the effective use of respiratory protection in carbon setters (anode replacement).
Kono et al. [28
] found a linear relationship between HF concentration (>5 ppm) in the occupational environment and mean urinary fluoride levels in electronics industry workers. The wide variation of fluoride levels in urine has been ascribed to the consumption of tea and seafood (water intake was not considered because only <1% of the water supply is fluoridated in Japan). In agreement with Kono et al. [28
], we also rejected the fluoride intake by potable water in Žiar nad Hronom which met hygienic standards. In the occupational environment, fluoride intake via inhalation can reach 16.8 mg per day; nevertheless, daily intake of fluoride by optimally fluoridated potable water is about 1.4–2.4 mg [8
]. During our research, participants were asked to avoid tea consumption and use of toothpastes enriched with fluoride for at least 48 h prior to urine collection; however, an apparent limitation of this procedure is its verification. Waugh et al. [29
] and Koç et al. [13
] concluded that tea is a significant source of fluoride intake. A major source of limitation in this study is fluoride intake effected by the composition of diet. With low water fluoride, the urinary fluoride concentration is much more influenced by eating habits [27
]. According to Whitford [30
], vegetarian diet leads to more alkaline urine and in addition increases the urinary fluoride excretion. Assessment of fluoride intake by food is quite challenging due to exposure to multiple dietary sources and supplements. Some authors in other studies used diet standardization to reduce this limitation, however, it is quite difficult to conduct [7
Urinary fluoride concentrations of 0.8–1.2 mg/L are regarded as indicating optimal exposure to fluoride in population [31
]. Figure 4
compares pre- and post-shift urinary fluoride concentrations for all study participants.
According to Wilcoxon signed-rank test, mean post-shift urinary fluoride concentration was significantly (p
< 0.001) higher compared to mean pre-shift urinary fluoride concentration for all investigated participants. From this, it can be concluded that there is an increase in fluoride concentration in primary aluminum workers during their work performance, although the relationship between occupational exposure and urinary fluoride levels was not confirmed. Overall, these findings are in accordance with previous findings reported by Rees et al. [32
] who found significant (p
< 0.05) difference between mean pre- and post-shift concentrations in workers exposed above OSHA PEL (2.5 mg/m3
) to calcium fluoride (CaF2
), and a weak correlation between intensity of occupational exposure to calcium fluoride and post-shift urinary fluoride concentration. Mean fluoride exposure in the dustiest environment was 24.3 mg/m3
(40.6% respirable fraction) which is approximately 10 times OSHA PEL. Only one urinary concentration exceeded the recommended limit value of 7 mg fluoride per liter. It is important to highlight the fact that potroom of aluminum smelter is a high-temperature workplace; therefore, the relating of the urinary excretion of fluoride to g-creatinine is necessary. According to the World Health Organization (WHO) [31
], the mean 24-h urinary creatinine value is 15 mg/kg of body weight per day. Several previous studies have not reported creatinine correction. Zohouri et al. [33
] reported the mean urinary fluoride concentration of 1.49 (±0.63) mg/g creatinine in children.
The biological exposure index (BEI) for fluoride exposure is 3 mg/g creatinine prior to shift and 10 mg/g creatinine at end of shift [34
]. The BEI were not exceeded in the monitored spot urine samples. We found that maximum pre- and post-shift urinary fluoride concentrations were 2.42 mg/g creatinine and 3.73 mg/g creatinine.
In agreement with WHO [31
], the time of urine collection was approximately equal during the whole study period, which is important for correct interpretation of the results, because urine that has accumulated in the body over a shorter time period may manifest a short-lived peak of the fluoride concentration. The findings of the present study demonstrate variations in urinary fluoride levels within participants. We assume that improper use of a personal respiratory protection might contribute to these differences.
According to Seixas et al. [9
], mean urinary fluoride concentrations were 1.3 and 3.0 mg/g creatinine in pre-shift and post-shift urine samples. The results of our study showed markedly lower mean concentrations of particulate fluoride and HF in the occupational environment. Our results also showed lower pre- and post-shift urinary fluoride concentrations. Research by Seixas et al. [9
] was performed on a sample of 32 workers in a shorter period (days 1 and 3 of a three-day workweek), making it more sensitive to local and short-term increases in fluoride concentration in the occupational environment. On the other hand, our study provided information obtained from a longer time period and various operational situations that may have occurred in aluminum smelter.
A frequency distribution in Figure 5
shows that 89% of all study participants had urinary fluoride difference (post-shift minus pre-shift concentration) below 1 mg/g creatinine, with the maximum value at 3.38 mg/g creatinine and the minimum was at a negative value of −0.82 mg/g creatinine (a negative result of urinary fluoride difference was found in nine workers). According to Lauwerys et al. [35
], the difference between post- and pre-shift urinary fluoride concentration should not exceed 3 to 4 mg/g creatinine, respectively, pre-shift values should be <3 mg/g creatinine.
Tobacco smoking was the main confounding factor of fluoride exposure we decided to investigate. In total, 35 study participants were regular smokers consuming at least 10 cigarettes per day. Other 39 participants declared they were strict non-smokers and they were not aware of the regular secondhand smoke exposure. There was a separate smoking area in smelter. Workers had the right to one uninterrupted 30-min rest break during their working day, if they worked 8 h per day. Majority of smokers took this break also as smoking break. Further, each of the smokers confirmed that they smoked at least one cigarette before their shift.
shows a comparison of mean pre- and post-shift urinary fluoride concentrations according to smoking habits of investigated primary aluminum workers. The results in the present study showed no statistically significant difference of the urinary fluoride level among group of smokers and non-smokers before the shift (p
= 0.62) and after the shift (p
= 0.11) by K-W test. This suggests that under the given research conditions, tobacco smoking does not affect the fluoride content of workers in primary aluminum smelter. It remains unclear why non-smokers show higher or equal pre-shift mean urinary fluoride concentration (0.469 ± 0.379 mg/g creatinine) than smokers (0.441 ± 0.338 mg/g creatinine). We assume that pre-shift samples reflected the worker´s total burden of fluoride and although smokers consumed a cigarette before shift, this was not reflected despite to rapid kinetics and the biological half-life of fluoride in human body. From the difference between pre- and post-shift urinary fluoride values, a decreasing trend of urinary fluoride concentration in smokers was found (r = −0.133, p
= 0.447). The group of non-smokers was characterized by a slightly increasing trend (r = 0.03, p
The research on the interaction between tobacco smoking and fluoride absorption and, subsequently, excretion is limited. It is estimated that heavy cigarette smoking could daily contribute about 0.01 mg of fluoride intake per kg of body weight [36
]. Laisalmi et al. [37
] reported the relationship between smoking and inorganic fluoride levels due to anesthesia with enflurane (2-chloro-1,1,2,-trifluoroethyl-difluoromethyl ether). In contrast with the present study, they observed that the serum fluoride concentrations were significantly different between group of smokers and non-smokers. On the other hand, our results are in agreement with Radon et al. [38
], who found no combined effect of smoking and occupational exposure in aluminum potroom workers exposed to hydrogen fluoride and inhalable dust below OSHA PEL. A similar conclusion also reached Tu et al. [39
], who concluded that age, work history, smoking, and alcohol consumption did not affect the blood fluoride and urinary fluoride levels in 300 workers from an aluminum plant in China.
According to Koç et al. [13
], urinary fluoride concentration is higher in smokers compared to non-smokers among 300 students at the University of Kafkas, Turkey. The present study found no significant differences between pre- and post-shift urinary fluoride levels in groups of smokers and non-smokers, although non-smokers had slightly higher levels of pre-shift urinary fluoride. This effect may be caused by other confounding variables, which we did not consider, such as drinking tea, dietary intake of fluoride, or metabolic disorders. Therefore, further research needs to be supplemented with data on excessive intake of fluoride.