Mutagenesis vol. 18 no. 6 pp. 533-537,
November 2003
© 2003 UK Environmental Mutagen Society/Oxford University Press
Associations between oxidative stress levels and total duration of engagement in jobs with exposure to fly ash among workers at municipal solid waste incinerators
National Institute of Industrial Health, 6-21-1 Nagao, Kawasaki, Kanagawa 214-8585, Japan and 1Shino-Test Corp., 2-29-14 Oonodai, Sagamihara, Kanagawa 229-0011, Japan
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The fly ash from municipal solid waste incinerators (MSWIs) is known to contain heavy metals, polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs), polyaromatic hydrocarbons (PAHs), and other organic materials. Heavy metals, PCDDs, PCDFs and PAHs reportedly cause oxidative stress in vitro and in vivo. In this study, we have measured the blood and urinary levels of several oxidative stress markers in MSWI workers and discuss herein whether the duration of engagement in jobs with exposure to MSWI fly ash is associated with these levels. The subjects were 81 male workers (mean age 42.7 years) from four MSWIs in the same city. Job history was determined from each subject and jobs were categorized according to the possibility of exposure to fly ash. The subjects were classified into four groups: long duration of engagement in jobs with exposure to fly ash, short duration of engagement in jobs with exposure to fly ash, engagement in jobs with limited exposure to fly ash and control. Blood and urine specimens were obtained from the subjects in the morning before breakfast. The levels of 8-hydroxy-2'-deoxyguanosine (8-OH-dG) in the urine and leukocytes were measured as markers of oxidative DNA damage. Blood malondialdehyde and lipid peroxide levels and the level of total urinary biopyrrins were also measured as markers of systemic oxidative stress. The mean levels of all markers were compared among the four groups. There was a significant trend showing that the level of urinary 8-OH-dG rose with increased duration of engagement in jobs with exposure to MSWI fly ash (P < 0.05). Considering this result, we speculate that certain chemicals in fly ash might have induced oxidative stress in the study subjects.
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It is well known that fly ash from municipal solid waste incinerators (MSWIs) includes heavy metals, polychlorinated dibenzo-p-dioxins (PCDDs), polychlorinated dibenzofuran (PCDFs), polyaromatic hydrocarbons (PAHs) and other toxic organic materials (Sovocool et al., 1988
; Rowat, 1999; Hong et al., 2000). Extracts from bottom ash and fly ash collected from MSWIs in the USA and Japan were mutagenic to Salmonella typhimurium strains TA98 and TA100 (Kamiya et al., 1990; Silkowski et al., 1992; Shane et al., 1993).
Air pollution control devices have been installed in MSWIs and toxic chemicals have been removed with fly ash from the gas emitted from furnaces (Gustavsson, 1989). However, the installation of these devices, such as electrostatic precipitators, concentrates the fly ash in certain areas (Gustavsson, 1989; Scarlett et al., 1990; Malkin et al., 1992). This has created frequent opportunities for workers to be exposed to a high density of fly ash when engaging in jobs such as furnace, flue duct and electrostatic precipitator cleaning and maintenance, as well as in fly ash disposal areas (Gustavsson, 1989; Scarlett et al., 1990; Malkin et al., 1992).
Gustavsson (1989) reported an increased risk of ischemic heart disease among MSWI workers, which was possibly attributable to working at MSWIs after electrostatic precipitators had been set up. There was also an excess of lung cancer deaths among these workers, although the elevated death rate was not clearly associated with working at MSWIs (Gustavsson, 1989).
Substances extracted from the urine of MSWI workers were mutagenic to S.typhimurium strain TA100 and the mutagenic potency of a urinary component from workers at MSWI without safety clothing was higher than that from workers who used safety clothing (Scarlett et al., 1990). Therefore, concern was raised that mutagenic and toxic chemicals were absorbed systemically upon exposure to bottom ash and fly ash at MSWIs, thereby increasing the risk of diseases such as cancer.
According to several in vivo and in vitro studies, heavy metals (Toyokuni et al., 1997; Chen et al., 2000; Kawanishi et al., 2002), PCDDs and PCDFs (Yoshida and Ogawa, 2000) and PAHs (Flowers et al., 1996, 1997; Murata et al., 1999a,b) may be responsible for oxidative stress in the body. Chronic oxidative stress caused by exposure to certain chemicals is thought to be associated with the occurrence of lung disorders (Witschi, 1997) and ischemic heart disease (Lefer and Granger, 2000; Pandya, 2001). There have been few studies investigating oxidative stress in MSWI workers. The purpose of the present study was to measure the levels of oxidative stress markers in blood and urine from MSWI workers and determine whether the duration of engagement in jobs with possible exposure to fly ash is related to the levels of these oxidative stress markers.
Approval for this study was obtained from the ethics board of our institute.
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Subjects
The subjects were 81 male workers (mean age 42.7 years) from four MSWIs in the same city. All subjects agreed to anonymously donate blood and urine samples and gave written informed consent to participate in the study. Occupational health doctors interviewed each subject about his work history and the jobs were then classified into four categories according to the level of possible exposure to fly ash (Table I). Type 1 jobs had ‘definite exposure to fly ash’ (cleaning and repair of furnaces, electrostatic precipitators and flue ducts); Type 2 jobs had ‘possible exposure to fly ash’ (operation and checking of incinerators and handling of aggregated fly ash); Type 3 jobs had ‘minimal exposure to fly ash (on the premises)’ (office work, collecting waste by car and disposal of inflammable waste); Type 4 jobs had ‘no exposure to fly ash (not on the premises)’ (jobs outside the MSWI). Then, the subjects were classified into four groups (G41, G42, G43 and G44) according to the categorized job and the duration of engagement in the job (Table II). These were: G41, long duration of engagement in jobs with exposure to fly ash (workers who had engaged in Type 1 jobs for
10 years); G42, short duration of engagement in jobs with exposure to fly ash (workers who had engaged in Type 1 jobs for <10 years); G43, engagement in jobs with limited exposure to fly ash (workers who had engaged in Type 2 jobs but not Type 1 jobs); G44, control (workers who had engaged in Type 3 and Type 4 jobs only). The subjects were also interviewed as to their drinking and smoking habits and other lifestyle factors.
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Exposure data
The concentration of blood dioxins in toxic equivalent (TEQ) [summation of 7 PCDDs and 10 PCDFs multiplied by each toxic equivalency factor (TEF) from WHO ’98 (Van den Berg et al., 1998
)] of 29 workers at the same MSWIs were measured by Ohtsuka Assay Laboratory (Tokushima, Japan). The measurements were conducted by the municipal government. Sixteen of 29 workers belonged to study group G41 or G42. The measurement averaged 14.59 TEQ pg/g fat (6.82–33.49 TEQ pg/g fat) and the median was 13.41 TEQ pg/g fat. The same laboratory measured the concentrations of blood dioxins of 154 workers at nine MSWIs in Japan under a project of the Ministry of Labor. The average blood dioxins level was 19.08 TEQ pg/g fat (2.66–124.99 TEQ pg/g fat) and the median was 14.96 (Ministry of Labor, 2000; Ministry of Health, Welfare and Labor, 2001).
Measurements of oxidative stress markers
Blood and urine specimens were obtained from subjects in the morning before breakfast. The urine samples, as well as leukocytes and sera separated with a centrifuge, were immediately frozen at –80°C until analysis. 8-Hydroxy-2'-deoxyguanosine (8-OH-dG) in urine and leukocytes was measured as an oxidative DNA damage marker. The level of leukocytic 8-OH-dG was measured by HPLC with electrochemical detection as described previously (Irie et al., 2001). Urinary 8-OH-dG was measured using an ELISA kit including anti-8-OH-dG monoclonal antibody N45.1 (Japan Institute for the Control of Aging, Fukuroi, Shizuoka, Japan) which had previously been validated in our laboratory (Yoshida et al., 2002). Blood malondialdehyde (MDA) and lipid peroxide (LPO) levels were measured, as general systemic oxidative stress markers, using a thiobarbituric acid (TBA) assay and an assay with a methylene blue derivative in the presence of hemoglobin, respectively (Mitsubishi Kagaku Bio-Clinical Laboratories Inc.). Total urinary biopyrrins, oxidative products of the antioxidant bilirubin (Yamaguchi et al., 1994), were also measured as a new systemic oxidative stress marker using an ELISA kit including anti-bilirubin monoclonal antibody 24G7 (Shino-Test Corp., Sagamihara, Kanagawa, Japan). Urinary creatinine was measured with an automated biochemical analyzer (7150 Automatic Analyzer; Hitachi Ltd, Japan) and Accuras Auto CRE (Shino-Test Corp.). Urinary 8-OH-dG and total biopyrrins were then normalized to the urinary creatinine level.
Statistical analysis
The group means were compared by ANOVA. Multiple regression analysis was used to control for confounding variables.
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Results |
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First, the mean levels of all markers were compared among the four groups (G41–G44). None of these differed significantly among the four groups (Table III). The levels of all markers appeared to be similar in G43 and G44. We regrouped the subjects into three groups (G31–G33) such that the number of subjects were comparable: G31, same as G41; G32, same as G42; G33, G43 and G44 combined. Group G33 was considered as a reference group rather than a control. The marker levels were re-analyzed comparing these three groups. Without adjustment for age or smoking and drinking habit, none of the marker levels differed significantly among the three groups (Table IV). However, multiple regression analysis, using as independent variables the exposure factors (group differences), alcohol consumption, smoking and age revealed that the level of urinary 8-OH-dG was significantly increased (P < 0.05) with increased duration of engagement in jobs with exposure to MSWI fly ash (Table V).
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As we discuss more precisely later, materials included in fly ash from MSWIs, such as heavy metals, PCDDs, PCDFs and probably PAHs, are accumulated and the body burden will increase with increased duration engaged in jobs with possible exposure to fly ash. In the present study, we have aimed to assess the effects of chronic exposure to fly ash using oxidative stress markers.
Levels of urinary 8-OH-dG, but not leukocytic 8-OH-dG, tended to increase with the duration of engagement in fly ash exposed jobs. Urinary 8-OH-dG is thought to arise mainly from three sources: repair products of oxidized DNA, removal of oxidized dG in the nucleotide pool and cell turnover (Loft and Poulsen, 2000). This suggests that urinary 8-OH-dG represents the average level of oxidative DNA damage throughout the body (Loft and Poulsen, 2000), as opposed to leukocytic 8-OH-dG, which represents only the level of oxidative stress in blood. If chemicals included in fly ash induce reactive oxygen species (ROS) not in blood but rather in other tissues, the levels of leukocytic 8-OH-dG might not increase with increased duration of engagement in fly ash exposed jobs. Another possibility is that leukocytic 8-OH-dG is maintained at a constant level via repair of oxidative damage (Loft and Poulsen, 2000). If oxidative stress is sufficient to exceed repair activity, leukocytic 8-OH-dG may increase until enough repair enzymes are induced to maintain oxidative damage at the minimal level (Loft and Poulsen, 2000). This suggests that 8-OH-dG levels in leukocytes increase when a high level of oxidative stress is induced or when induction of oxidative stress is temporary but rapid. Moreover, increased oxidative stress probably causes rapid cell death, accelerates cell turnover and increases urinary 8-OH-dG, while increased 8-OH-dG in leukocytes might be concealed due to rapid cell turnover. For these reasons, even if ROS had been induced in blood by fly ash, leukocytic 8-OH-dG levels might not increase sensitively with increased duration of engagement in fly ash exposed jobs.
Although total urinary biopyrrin levels did not increase significantly with increased duration of engagement in jobs with exposure to fly ash, there was a tendency for these levels to be higher in workers who had engaged in such jobs than those in the reference group. The levels of LPO likewise did not increase with increased duration of engagement in fly ash exposed jobs. However, there was a tendency for the levels of LPO in workers who had engaged in jobs with exposure to fly ash to be higher than those in the reference group. While the MDA levels in workers who had been engaged for less than 10 years in fly ash exposed jobs were nearly the same as those of the reference group, the MDA level did appear to increase with longer duration of engagement in jobs with fly ash exposure. Even though there were no significant differences, these relations do not contradict our speculation that oxidative stress level increased in workers engaged in jobs with fly ash exposure. The levels of lipid oxidation products, as represented by levels of MDA and LPO, are considered to be valuable as systemic oxidative stress indicators, but these substances react readily with other substances in the body (Aruoma and Cuppett, 1997) and their levels may not sensitively reflect oxidative stress levels in the whole body as compared with urinary 8-OHdG.
Candidate chemicals contained in MSWI fly ash and possibly inducing oxidative stress in workers include heavy metals, PCDDs, PCDFs and PAHs.
A previous study demonstrated that blood lead levels in workers cleaning electrostatic precipitators were higher than those in a control group not working in a municipal incinerator (Malkin et al., 1992). Lead exposure reportedly depletes antioxidants in vivo (Hermes-Lima et al., 1991). Since fly ash generally includes other heavy metals, e.g. cadmium, chromium, cobalt, nickel, magnesium, iron and zinc (Hong et al., 2000), other heavy metals in the fly ash could also be systemically absorbed. Increasing such types of heavy metal in the body is thought to enhance redox cycling and consequentially to induce ROS, especially hydroxyl radicals (Halliwell, 1998). Furthermore, portions of these heavy metals are not immediately excreted (Gerhardsson and Skerfving, 1996). They are bound to proteins in the blood, e.g. albumin and transferrin, and distributed around the body and finally accumulated in the kidneys, liver, lungs, bone and other organs (Gerhardsson and Skerfving, 1996). The accumulated heavy metals may contribute to generating ROS for a long time.
The concentrations of PCDDs and PCDFs in blood from workers at a certain MSWI were higher than those of the control group (Schecter et al., 1995; Ministry of Labor, 1999), raising the possibility that MSWI workers are more likely to be exposed to PCDDs and PCDFs. A significant correlation between blood concentrations of certain types of PCDDs and PCDFs and the duration of engagement in fly ash exposed jobs at MSWIs was also reported, even though the levels of PCDDs and PCDFs among MSWI workers were not markedly elevated as compared with the general population (Ministry of Labor, 2000), which is the case for our subjects. Accordingly, there is a possibility that more PCDDs and PCDFs accumulate systemically in workers with prolonged engagement in fly ash exposed jobs than in the reference group or workers who had engaged in these jobs for less time. Although PCDDs and PCDFs do not cause systemic ROS directly, they can result in ROS indirectly via induction of metabolic enzymes that induce ROS during metabolism of xenobiotics and essential substances in the body. Since PCDDs and PCDFs are retained for a long time (IARC, 1997), these compounds could chronically increase oxidative stress marker levels in the body (Yoshida and Ogawa, 2000).
It has already been reported that PAHs exist in MSWI fly ash (Rowat, 1999). Some metabolites of PAHs have been shown to induce oxidative DNA damage by generating ROS (Flowers et al., 1996, 1997; Murata et al., 1999a,b). Although the concentrations of PAHs in blood and urine of MSWI workers have not been extensively reported, it is possible that the systemic concentrations of mutagenic PAHs are increased in MSWI workers because of their highly lipophilic character (Bostrom et al., 2002).
Other organic compounds, like PCB congeners, halogenated organic acids, aldehydes, alkanes and alkenes, are also considered to exist in fly ash (Rowat, 1999). These organic compounds can induce some cytochrome P450 isozymes (Nims and Lubet, 1996; Ronis et al., 1996). The cytochrome P450 isozymes induced by these organic compounds might generate ROS during metabolism of xenobiotics.
Oxidative stress is considered to act as an initiator and promoter in the process of carcinogenesis (Klaunig et al., 1997), as well as being associated with other diseases such as coronary heart disease (Bondy, 1992; Nagelkerke, 1997; Plaa, 1997; Subrahmanyam and Smith, 1997; Wallace, 1997; Pandya, 2001). If a disease relevant to oxidative stress increases among MWSI workers engaged in fly ash exposed jobs, the cause of the higher disease incidence might be oxidative stress induced by fly ash components. Further study is required to biomonitor the concentrations of heavy metals, PCDDs, PCDFs and PAHs among MSWI workers. Investigations of the association between systemic concentrations of such substances and engagement in jobs with exposure to fly ash, as well as ascertaining the cause of oxidative stress in workers, are also needed.
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2To whom correspondence should be addressed. Tel: +81 44 865 6111; Fax: +81 44 865 6124; Email; ogawa{at}niih.go.jp
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Received on May 9, 2003; accepted on August 27, 2003.
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