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Urinary metabolites before and after cleanup and subjective symptoms in volunteer participants in cleanup of the Hebei Spirit oil spill
Science of the Total Environment 429 (2012) 167–173
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Urinary metabolites before and after cleanup and subjective symptoms in volunteer participants in cleanup of the Hebei Spirit oil spill Mina Ha a, b,⁎, Hojang Kwon a, b, Hae-Kwan Cheong c, Sinye Lim d, Seung Jin Yoo b, Eun-Jung Kim b, Seok Gun Park e, Jeongae Lee f, Bong Chul Chung f,⁎⁎ a
Department of Preventive Medicine, Dankook University College of Medicine, Cheonan, Republic of Korea Environmental Health Center, Dankook University Medical Center, Cheonan, Republic of Korea Department of Social and Preventive Medicine, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea d Department of Occupational and Environmental Medicine, Kyung Hee University Medical Center, Seoul, Republic of Korea e Department of Nuclear Medicine, Dankook University College of Medicine, Republic of Korea f Integrated Omics Center, Korea Institute of Science and Technology, Seoul, Republic of Korea b c
a r t i c l e
i n f o
Article history: Received 9 September 2011 Received in revised form 9 April 2012 Accepted 10 April 2012 Available online 15 May 2012 Keywords: Oil spill Subjective symptoms Urinary metabolites Cleanup
a b s t r a c t Background: On December 7th, 2007, the Hong Kong tanker Hebei Spirit (HS) (146,848 tons) was crushed by a crane ship near the shore of Taean, Korea. More than 12,547 kl of crude oil spilled into the sea and contaminated the western coastline of the Korean peninsula. For a period of six months after the accident, approximately 1,000,000 volunteers participated in the cleanup. Our goal in this study was to examine the exposure status and acute health effects on volunteers that participated in the oil spill cleanup. Methods: A survey questionnaire was filled out by 565 volunteers, requesting information regarding physical symptoms. Out of the total number of participants, urine samples from 105 university student volunteers were collected before and after the cleanup work, and metabolite levels of volatile organic compounds and polycyclic aromatic hydrocarbons were analyzed. Results: Volunteers that participated for longer cleanup work reported an increase in physical symptoms including visual disturbance, nasal and bronchus irritation, headaches, heart palpitations, fatigue and fever, memory and cognitive disturbance, and abdominal pain. The levels of t,t-muconic acid, mandelic acid, and 1-hydroxypyrene were significantly higher in samples after cleanup than those measured before participation (p b 0.05). Other than the associated risk of dermal irritation with the difference in the t,t-muconic acid level between the post- to pre-cleanup levels, no other physical symptoms demonstrated a significant association with changes observed in the levels of urinary metabolites. Conclusions: Based on the significant increase of subjective symptoms in volunteers participating in the study, monitoring of the long term health effects, focusing on those with longer exposure, is warranted. © 2012 Elsevier B.V. All rights reserved.
1. Introduction The Hong Kong tanker, the Hebei Spirit (HS) collided with a crane ship five miles northwest of Taean's Manri-po Beach, Korea on Dec 7th, 2007. It was estimated that more than 12,547 kl of oil (about
Abbreviations: HS, Hebei Spirit; VOCs, volatile organic compounds; PAHs, polycyclic aromatic hydrocarbons. ⁎ Correspondence to: M. Ha, Department of Preventive Medicine, Dankook University College of Medicine, 201 Mahyangno, Dongnam-gu, Cheoan, Chungnam 330‐714, Republic of Korea. Tel.: +82 41 550 3854; fax: +82 41 556 6461. ⁎⁎ Correspondence to: B.C. Chung, Bioanalysis and Biotransformation Research Center, Korea Institute of Science and Technology, Hwarangno 14-gil 5, Seongbuk-gu, Seoul 136‐791, Republic of Korea. Tel.: + 82 02 958 5067; fax: + 82 02 958 5059. E-mail addresses: [email protected] (M. Ha), [email protected] (H. Kwon), [email protected] (H-K. Cheong), [email protected] (S. Lim), [email protected] (SJ. Yoo), [email protected] (E-J. Kim), [email protected] (SG. Park), [email protected] (J. Lee), [email protected] (BC. Chung). 0048-9697/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2012.04.036
78,962 bbl or 3,314,562 gal) spilled into the sea. The oil reached the western coastline of the Korean peninsula with a range in spread of 1052 km and was found in Chungnam, Jeonbuk, Jeonnam, and as far as Jeju island. The spill was confirmed as the largest oil spill contamination to occur in Korean history (Ha et al., 2008). The Taean-gun area, an agricultural and fishing region including 119 small islands, 530.8 km of coastline, and an area of 503 km 2 with a recorded population of 63,939 people as of 2006 (County chief of Taean, 2007), received the most severe damage. Three types of crude oil were carried by the HS; UAE Upper Zakum, Kuwait Export Crude, and Iranian Heavy. The main chemical components were primarily composed of hydrocarbons, e.g., volatile organic compounds (VOCs) and polycyclic aromatic hydrocarbons (PAHs), including alkylated types, and minor heavy metals (Marine Environmental Information Service Center, 2009). Approximately 30–50% of VOCs in the crude oil were estimated to be volatized into the air during the first few days after the initial spill. The airborne
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concentrations of PAH (16 PAHs listed on the US EPA priority) were 130–277 ppm and those of alkylated PAHs were 4511–8259 ppm (Marine Environmental Information Service Center, 2009). The HS crude oil also contained traces of heavy metals and released hydrogen sulfide gas (Marine Environmental Information Service Center, 2009). VOC exposure is associated with acute, reversible effects to the CNS (headache, nausea, sleepiness) and irritation of mucous membranes. Prolonged exposure to certain VOCs and PAHs can cause axonal neuropathy. Aromatic compounds, such as 1,2-diethylbenzene, are more potent axonal neurotoxins than aliphatic compounds such as n-hexane (Agency for Toxic Substances and Disease Registry, 1995). Among the crude oil VOCs, benzene is classified as a Group I agent, a proven human carcinogen. Other VOCs including toluene, ethylbenzene, and stylene, belong to Group 2B, which are considered as possible human carcinogens based on published animal studies (International Agency for Research on Cancer, 2006). PAHs such as benzo[a]anthracene, benzo[a]pyrene, and dibenzo[a,h]anthracene are classified into Group 2A, probable human carcinogens, while chrysene, naphthalene, benzo[b]fluoranthene, benzo[k]fluoranthene, and indeno[1,2,3-cd]pyrene are members of Group 2B (International Agency for Research on Cancer, 2006). Following the accident, local residents, along with many other people from around Korea, worked to clean up the spilled oil. A total of 2,122,296 days were estimated as the total number of days dedicated by participants to the cleanup as of July 4th, 2008 (Lee et al., 2009). Most local residents participated in the cleanup for a period of days to several months and both military personnel and governmental employees (59,118 person-days) were also recommended by their organizations to voluntarily participate in the cleanup efforts for several days or months. Professional cleanup workers (about 200–300 persons) covered 48,809 person-days. Additionally, approximately 1,000,000 persons (contributing 1,161,086 person-days) voluntarily gathered at the spill sites to volunteer for a range of a few hours to days to clean up all around the country, i.e., members from civic groups, schools and universities, companies, communities, and families and individuals. Although some studies investigated the health effects of cleanup workers from exposure to an oil spill (Palinkas et al., 1992; Suarez et al., 2005; Carrasco et al., 2006; Zock et al., 2007; Perez-Cadahia et al., 2007, 2008; Rodríguez-Trigo et al., 2010; Goldstein et al., 2011) or local residents living in the polluted sites (Palinkas et al., 1993; Campbell et al., 1993; Crum, 1993; Campbell et al., 1994; Lyons et al., 1999; Morita et al., 1999; Janjua et al., 2006; Carrasco et al., 2007; Sim et al., 2010; Cheong et al., 2011), no study has been reported regarding the exposure of volunteers for a short range of time, including a few hours to several days. Since a huge number of volunteers participated in the cleanup work for the HS oil spill accident, even a small health risk, possibly due to exposure to crude oil during cleanup, may have an important impact on public health. This particular study examined the exposure of volunteers to crude oil by analyzing changes in urinary metabolites of VOCs and PAHs before and after cleanup as well as the incidence of subjective physical symptoms using a survey questionnaire.
2. Materials and methods 2.1. Study subjects The questionnaire survey for volunteers was conducted between the second and third week after the accident (Dec 14, 2007 to Dec 24, 2007). Questionnaires were administered to people working for the cleanup in three contaminated areas at the end of the work day. A total of 724 subjects (out of 1000 questionnaires distributed) responded to the questionnaire, which included questions about the cleanup work conducted, physical symptoms, and other socio-
demographic factors. After excluding incomplete questionnaires, 565 questionnaires were analyzed and included in our study. A subgroup of the total number of participants, included a group of university students (n = 312), who were organized by a university, were also asked to provide their urine before and after the cleanup work participation. A total of 121 out of 272 students responded to the questionnaire and provided urine samples, and a total of 105 urine pairs were analyzed after excluding unpaired urine. The study protocol was approved by the Institutional Review Board of Dankook University Hospital, and informed consent was obtained from all subjects. 2.2. Survey questionnaire on the cleanup work and subjective symptoms The authors developed a symptom questionnaire based on the possible effects of the crude oil composition (Agency for Toxic Substances and Disease Registry, 1995) following the format of previously published questionnaires and reported symptoms for oil spill accidents in other countries (Janjua et al., 2006; Rodriguez-Trigo et al., 2007). A total of 41 physical symptoms were grouped into 14 categories classified with regard to organ systems, which were described in previous reports (Lee et al., 2009; Cheong et al., 2011): eye irritation, visual disturbance, nasal irritation, sore throat, bronchial irritation, dermal irritation, headache, palpitations (fast heartbeat), nausea or vomiting, abdominal pain, fatigue and fever sensation (heat-stress related), memory or cognitive function disturbances, musculoskeletal symptoms, and back pain. Information on the duration of cleanup work was obtained (“How many days did you participate in the cleanup efforts?”(one day or more than one day) and “If the response is more than one day, write in the total number of days”). The type of job responsibility could be chosen among three possibilities: participating in direct cleanup work (i.e., oil skimming, cleaning of rocks, sands, and wildlife), a logisticsrelated job (i.e., pouring, moving or transporting oil trash), and others. The degree of skin contamination to oil could be reported as “not at all,” “a bit,” “much,” or “profound”. We also obtained and identified demographic information as confounders or covariates: age (open question, which was categorized: ≤29, 30–b39, 40–b49, or 50 or more), gender, occupation (students, office workers, manufacturing workers, agriculture, fishery, others), educational level (b12, 12, 13 or more years), current smoker (no, yes), health concerns about the oil spill (no, yes), past history of asthma diagnosis (no, yes), and wearing protective items, such as work clothes, gloves, boots, and mask (no or yes for each). 2.3. VOCs and PAHs metabolite analysis in urine sample pairs Urine collection was performed prior to the work day between 6 and 7 a.m. and at the end of the work day between 7 and 8 p.m. Collected urine samples were immediately stored in a portable refrigerator and transported to −20 °C freezers within 4 h of collection. One month later, the urine samples were packed on dry ice and transferred to the laboratory for analysis. Among the aromatic hydrocarbons, which composed approximately 30% of all chemicals in the HS crude oil, the VOCs, including benzene, toluene, ethylbenzene, and xylene (BTEX) composed 53–65%, followed by 33–45% of alkylated PAHs and 1% of 16 PAHs listed on the US EPA priority list (Marine Environmental Information Service Center, 2009). Based on the information on the chemical compositions of the oil spill and their known health effects, five metabolite compounds, t,t-muconic acid, mandelic acid, 2-methyl hippuric acid, 3-methyl hippuric acid, 4-methyl hippuric acid, and hippuric acid, were analyzed using gas chromatography–mass spectrometry (GC–MS, Agilent Technologies, Santa Clara, CA, USA). The analysis methods for metabolites of VOCs have previously been described in detail (Lee et al., 2010).
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We analyzed 1-hydroxypyrene and 2-naphthol as biomarkers of exposure to crude oil containing various PAHs. Two milliliters of each urine sample was combined with a 20 μl solution of 1 mg/L internal standards (1-naphthol-d7). Urine samples were enzymatically hydrolyzed by the addition of 1 ml of 0.2 M acetate buffer (pH 5.2), 50 μl of 0.2% ascorbic acid, and 50 μl of glucuronidase/ arylsulfatase (from Helix Pomatia, Penzberg, Germany) for 3 h at 55 °C. The hydrolyzed urine samples were subjected to Strata-X™ cartridges (60 mg, 3 ml; Phenomenox, Torrance, CA, USA), which were preconditioned five times with 2 ml of methanol and 2 ml of distilled water. After loading the samples, the cartridges were washed with 2 ml of 10% methanol. Urinary PAH metabolites were then eluted two times with 2 ml of 90% methanol, which were subsequently evaporated under nitrogen. The dried residues were derivatized with 40 μl of mixture reagent (MSTFA/TMCS/TMSI; 100:5:2, v/v/v) and heated at 60 °C for 15 min. A 2 μl derivatized aliquot was injected into the GC–MS (Agilent Technology, Santa Clara, CA, USA). The limit of detection (LOD, ng/mL) and limit of quantization (LOQ, ng/mL) were 3 and 10 for t,t-muconic acid and mandelic acid, 10 and 30 for (1,2,3-) methyl hippuric acid, 0.2 and 0.5 for 2-naphthol and 0.5 and 1.0 for 1-hydroxypyrene, respectively. 2.4. Statistical analysis The geometric means of the VOC and PAH metabolite concentrations in subjects before and after participation in the oil spill cleanup were calculated for 105 university student volunteers and compared using a paired t-test. Multiple logistic regression adjusted for age, gender, smoking, educational level, history of diagnosed asthma, health concern about the oil spill, and survey area was performed to estimate odds ratios and 95% confidence intervals of subjective physical symptoms for different types and the duration of cleanup work or urinary metabolite level differences between pre- and post-cleanup work. All analyses were conducted using SAS for windows (ver 9.2, SAS Institute Inc., Cary, NC, USA) with the significance set at a p value b 0.05. 3. Results Most of the study subjects were students in their 20s, non-smokers, participated in cleanup work for one day and were involved in direct cleanup jobs. Most subjects (84.6%) reported either no or a small amount of skin contamination by crude oil but almost all (more than 95%) were wearing good protective gear. Half of them were concerned about the health effects from the oil spill (Table 1). Out of a group of 13 people who reported two or more days of cleanup duration, the mean duration of work was 5.4 days (maximum = 15 days). The skin contamination rate was significantly higher in people involved in logisticsrelated jobs requiring an increased level of physical activity (91.4%) than in direct cleanup (71.6%), while no significant difference was seen in the proportion of individuals wearing protective devices between the two types of jobs. Out of 105 students who provided urine sample pairs, the average age was 20.9 years old (standard deviation, 2.1; range, 18 to 29), 12.4% (n = 13) were female and 19% (n = 20) were smokers. Eye (46.9%) and nose (41.6%) irritation and headache (42.0%) demonstrated the highest rate of positive symptoms, followed by fatigue and fever sensation (37.4%) and musculoskeletal symptoms (35.9%). People having logistics-related jobs and with longer durations showed increased rates of positive symptoms compared to those participating in the direct cleanup efforts and within a shorter period of time, respectively. In a full model including both type of jobs and the duration of work, the risks of visual disturbance, palpitation, fatigue and fever sensation, memory and cognitive disturbance, abdominal pain, nasal and bronchus irritation, and headache were
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Table 1 Socio-demographic characteristics of study subjects, 565 volunteers in the Hebei Spirit oil spill, 2007, Taean, Korea. Characteristics Survey areas A Ba C Age (years) 29 or less 30–b39 40–b49 50 or more Unknown Gender Male Female Unknown Occupation Student Office worker Fishery Others Unknown Education (years) b12 12 >12 Unknown
No.
(%)
107 313 145
(18.9) (55.4) (25.7)
457 46 44 14 4
(80.9) (8.1) (7.8) (2.5) (0.7)
275 288 2
(48.7) (51.0) (0.4)
402 114 1 31 17
(71.2) (20.2) (0.2) (5.5) (3.0)
16 50 485 14
(2.8) (8.8) (85.8) (1.9)
Duration of cleanup work 1 day 2 days or more Type of job involvedb Direct cleanup Logistics-related job Unknown Skin contamination to oilc Not at all A bit Much Profound Unknown Health concern about oil spill No Yes Unknown Current smoking No Yes Unknown Past history of asthma diagnosed No Yes Unknown
No.
(%)
552 13
(97.7) (2.3)
444 106 15
(78.6) (18.8) (2.7)
95 269 50 4 2
(22.6) (64.0) (11.9) (1.0) (0.5)
284 264 17
(50.3) (46.7) (3.0)
434 99 32
(76.8) (17.5) (5.7)
531 24 10
(94.0) (4.2) (1.8)
a 272 volunteers in area B were a group of students from a university, a part of them agreed to provide a pair of their urine samples before and after cleanup work. b Direct cleanup work included oil skimming, cleaning of rocks, sand, and wildlife; logistics-related jobs included pouring, moving, or transporting oil and trash. c The questionnaire administered to 145 subjects (by survey area C) did not have the question, and the percentages were calculated in 420 subjects.
significantly increased in subjects who worked for two days or more compared to those who worked for one day. Only the risk of palpitation was increased in people participating in logistics-related jobs compared to those participating in direct cleanup jobs (Fig. 1A). Metabolites of VOCs, t,t-muconic acid, mandelic acid, and those of PAHs, 1-hydroxypyrene, showed significantly increased levels after cleanup work compared to those measured before the cleanup work. Those of total methyl-hippuric acid, hippuric acid, and 2-naphthol showed no statistically significant difference between levels measured before and after cleanup work (Table 2). None of the metabolites were significantly different according to the degree of skin contamination to oil (Supplemental Table) or type of job (data not shown). Among 14 subjective physical symptoms, the risk of dermal irritation was associated with the level of difference pre and post of t,t-muconic acid. No statistically significant associations between the urinary level of pre and post differences of the VOCs and PAHs metabolites and physical symptoms were observed (Fig. 1B).
4. Discussion Volunteers participating for longer durations in the cleanup of the HS oil spill demonstrated several increased physical symptoms. The urinary levels of some VOC and PAH metabolites were significantly higher following cleanup than levels obtained before, although no material associations were observed between increased urinary levels due to the cleanup efforts and physical symptoms with the exception of t,t-muconic acid and dermal irritation. Although most of the volunteers in this study were only involved in a few hours of cleanup, their physical symptoms were generally similar with those reported by cleanup workers or local residents in other reported oil spill accidents (Campbell et al., 1993; Lyons et al., 1999; Morita et al., 1999; Suarez et al., 2005; Janjua et al.,
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A)
Work type (Logistics-related work vs direct cleanup) 0.0
0.2
1.0
5.0
25.0
Work duration (2 days+vs 1 day) 0.0
0.2
1.0
5.0
25.0
OR (95% CI) Eye irritation Visual disturbance Nasal irritation Sore throat Bronchial irritation Dermal irritation Headache Palpitation Nausea, vomiting Abdominal pain Fatigue and fever sensation Memory/cognitive disturbance Musculoskeletal symptom Back pain
B)
tt-muconic acid 0.0
0.2
1.0
Mandelic acid 5.0
0.0
0.2
0.0
0.2
1.0
Hippuric acid 5.0
0.0
0.2
1.0
5.0
OR (95% CI) Eye irritation Visual disturbance Nasal irritation Sore throat Bronchial irritation Dermal irritation Headache Palpitation Nausea, vomiting Abdominal pain Fatigue and fever sensation Memory/cognitive disturbance Musculoskeletal symptom Back pain
total methyl-hippuric acid 0.0 Eye irritation
0.2
1.0
5.0
2-naphthol 1.0
1-hydroxypyrene 5.0
0.0
0.2
1.0
5.0
OR (95% CI)
Visual disturbance Nasal irritation Sore throat Bronchial irritation Dermal irritation Headache Palpitation Nausea, vomiting Abdominal pain Fatigue and fever sensation Memory/cognitive disturbance Musculoskeletal symptom Back pain
Fig. 1. Odds ratios and 95% confidence intervals of subjective physical symptoms for type and duration of cleanup work in 565 volunteers (A) and urinary levels of pre- and postdifference of urinary metabolites in 105 student volunteers (B) in the Hebei Spirit oil spill, 2007, Taean, Korea. OR: odds ratio, CI: confidence intervals. Direct cleanup work included oil skimming, cleaning of rocks, sand, and wildlife; logistics-related jobs included pouring, moving, or transporting oil and trash. OR and 95% CI of each symptom for job type and duration of work estimated simultaneously using one multiple logistic regression model adjusted for age, gender, smoking, educational level, history of asthma diagnosed, health concern about oil spill, and survey groups (full model) (A). The level of urinary metabolites was the difference between levels before and after cleanup work. OR and 95% CI estimated for subjects with upper 50% of biomarker level referenced by those with lower 50% using multiple logistic regression model adjusted for age, gender, smoking, educational level, history of asthma diagnosed, and health concern about oil spill (B).
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Table 2 Urinary concentration of VOC and PAH metabolites in 105 student volunteers before and after cleanup in the Hebei Sprit oil spill, 2007, Taean, Korea. All (N = 105)
VOC metabolites t,t-muconic acid (μg/g cr.)
Mandelic acid (mg/g cr.)
Hippuric acid (mg/g cr.)
Total methyl-hippuric acid (mg/g cr.)
PAHs metabolites 2-Naphthol (μg/g.cr.)
1-Hydroxypyrene (μg/g cr.)
Smokers (N = 20)
Non-smokers (N = 79)
G mean
(Range)
G mean
(Range)
G mean
(Range)
Before After p-value Before After p-value Before After p-value Before After p-value
70.20 211.49
(14.31, 1223.04) (72.43, 608.34) b.0001 (0.00, 0.29) (0.02, 0.58) b.0001 (17.90, 1701.43) (4.30, 2527.45) 0.79 (0.01, 2.35) (0.06, 0.49) 0.27
87.78 218.89
(22.25, 541.31) (72.83, 525.73) 0.01 (0.05, 0.23) (0.13, 0.37) 0.001 (24.99, 775.19) (27.98, 638.40) 0.17 (0.05, 0.49) (0.12, 0.49) 0.10
65.80 208.73
(14.31, 1223.04) (72.43, 608.34) b.0001 (0.00, 0.29) (0.02, 0.58) b.0001 (17.90, 1701.43) (4.30, 2527.45) 0.72 (0.01, 2.35) (0.06, 0.43) 0.66
Before After p-value Before After p-value
1.27 2.41
0.10 0.19 175.51 147.08 0.14 0.21
0.96 1.58
(0.08, (0.10, 0.50 (0.13, (0.05, 0.003
0.12 0.19 187.16 149.57 0.17 0.27
382.01) 165.04)
4.67 3.14
22.17) 24.5)
0.98 1.36
(0.14, (0.24, 0.32 (0.21, (0.20, 0.29
0.09 0.19 173.92 159.06 0.14 0.20
40.03) 23.32)
0.97 2.41
5.46) 8.97)
0.95 1.66
(0.08, (0.10, 0.45 (0.13, (0.05, 0.007
382.1) 165.0) 22.17) 24.56)
G mean: geometric mean, VOCs: volatile organic compounds, PAHs: polycyclic aromatic hydrocarbons. p-value calculated using paired t-test.
2006; Perez-Cadahia et al., 2007; Sim et al., 2010; Cheong et al., 2011; Goldstein et al., 2011), mainly symptoms of mucosal irritation and headaches, which were induced from direct contact with or inhalation of vaporized crude oil and hydrogen sulfide gas. The increased rates of musculoskeletal symptoms and back pain, which are not supposed to be direct effects of crude oil exposure, may be explained by the fact that most volunteers were students or office workers who usually are not accustomed to the manual labor required for this type of cleanup work, i.e., frequent bending over and heavy lifting. During an initial period after the accident, the evaporation of the most volatile components from VOCs and PAHs is the major exposure factor and biomarker measured at this phase. Although the exposure duration in the present student volunteers was limited, the half lives of metabolites are relatively short and the levels of them measured at the time of pre- and post-exposure may be well reflected in the internal exposure of the crude oil. The main components of oil spills are presumably similar, but proportions of those components are most likely altered between different oil spills (Rodríguez-Trigo et al., 2010). While the oil spills from the Erika and Prestige tankers contained heavy fuel oil with a high sulfur content (4%) (Rodríguez-Trigo et al., 2010), which was a heavy fraction of refined oil, that of the HS is unrefined crude oil with low sulfur content (1%) and was mainly composed of saturated (53%) and aromatic (30%) hydrocarbons (Marine Environmental Information Service Center, 2009). Therefore, direct comparisons of the levels of exposure biomarkers between different oil spills are not necessarily appropriate but may be helpful to understand the general exposure characteristics and health effects of oil spills. Unfortunately, only two oil spill accidents reported urinary metabolites of VOCs (Campbell et al., 1993; Morita et al., 1999), but none reported PAHs. While no reports have been published on the level of t,t-muconic acid in previous oil spills, the post cleanup t,tmuconic acid level was similar with an occupationally exposed group, i.e., taxi drivers and slightly higher than a control population reported in Italy and Iran (Manini et al., 2006; Bahrami et al., 2007). The post cleanup hippuric acid level was similar with those reported in local residents 7–12 days after the occurrence of the Braer oil spill (Campbell et al., 1993) but slightly higher than the general populations in Japan, the Philippines (Villanueva et al., 1994) and Korea (Kim et al., 2008). The level of 2-naphthol in subjects after the cleanup was not higher than those reported for occupationally exposed groups in
Korea (Lee et al., 2001; Kim et al., 2001). However, the level of 1hydroxypyrene after cleanup was much higher than those previously reported among various groups in Korea (Kim et al., 2001; Kang et al., 2002; Kim et al., 2008), including aircraft maintenance workers (Lee et al., 2001) and shipyard workers (Kim et al., 2001). Therefore, exposure to crude oil in volunteers seems to be reflected well with the level of 1-hydroxypyrene rather than in 2-naphthol, while the levels of both metabolites of PAHs are within the range of the background level of the German general population (Schulz et al., 2012). The post cleanup levels of biomarkers in the volunteers were not higher than those in the residents participated in cleanup of HS oil spill with the exception in t,t-muconic acid and 1-hydroxypyrene (Cheong et al., 2011). It may be partly due to a different sampling time since the accident: at two weeks after the accident in the student volunteers and three or more weeks after in the residents. No significant differences observed in the levels of biomarkers according to the degree of skin contamination may suggest that oil absorption through skin contamination does not play a major role, compared to inhalation or ingestion, in terms of the exposure pathways from oil spills. No associations between the levels of urinary VOC and PAH metabolites and physical symptoms were observed, except for t,t-muconic acid and dermal irritation, which may be partially due to the lack of statistical power. There have been 1744 reported accidents spilling more than 7 tons of oil from 1970 to 2007 for a total of 5,648,000 tons of oil spilled into the ocean worldwide (International Tankers Owners Pollution Federation Limited, 2008, 2010). Furthermore, the recent BP oil spill in the Gulf of Mexico released almost 5 billion barrels of crude oil for a period of four months (Goldstein et al., 2011; Zock et al., 2011). In spite of the high frequency and huge volume of oil spilled, only a few studies regarding the health effects as a direct result of oil spills have been performed and summarized (RodriguezTrigo et al., 2007; Ha et al., 2008; Aguilera et al., 2010; Goldstein et al., 2011). Usually, many people voluntarily rush to the disaster site immediately after an accident and often do not have the training and advanced equipment that protect professional emergency responders to some degree (Weinhold, 2010). Therefore, the health risk may be even greater for the many non-professional emergency responders (Weinhold, 2010). In addition, crude oil contains various
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types of carcinogenic chemicals which could induce genetic toxicity after a period (Rodriguez-Trigo et al., 2007; Rodríguez-Trigo et al., 2010). Theoretically mutagenic effects can result from a single molecular DNA alteration without a threshold concentration of exposure (Goldstein et al., 2011). A long-term follow-up surveillance program involving people exposed to crude oil, particularly for various types of cancer, needs to be considered for volunteer cleanup workers as well. The present opportunistic study successfully conducted a survey questionnaire and for the first time to date, collected urine sample pairs before and after cleanup efforts immediately after the accident and established the potential importance regarding the issues related to the health of volunteers due to their participation in the oil spill cleanup. However, this study has several limitations. First, because the sampling time of urine was two weeks past the initial accident, the highest exposure to VOCs and PAHs, which occurred within a few days of the spill, could not be reflected in the urine samples analyzed in the present study. According to simulation results involving PAH evaporation from spilled oil (Ministry of Environment, Korea, 2008), PAH exposure was sustained for at least several months. Therefore, collected urine samples in the present study may reflect this extended exposure of PAHs. Second, the study does not have a non-exposed control group, meaning that we could not compare exposed and nonexposed subjects for the risk of physical symptoms. Third, the selfreported physical symptoms are subjective; thus, a misclassification bias might be present in this study. However, this is unlikely because most volunteers, unlike local residents, presumably do not have conflicts of interest related with economic compensation and no intention to exaggerate their health effects. In fact, there was no significant difference in the rate of positive symptoms between people who reported health concerns about oil spills and those who did not, with an exception for the symptoms of headache and nausea/vomiting, of which the concerned people demonstrated a higher symptom positive rate in the present study. Fourth, the small number of subjects and restricted survey areas in this study might not represent the entire population of volunteers participating in cleanup work, particularly those who participated for longer periods of time. In conclusion, we found that increasing physical symptoms were associated with longer durations of work and significantly higher VOC and PAH metabolite levels following cleanup than observed prior to cleanup. Based on the fact that large numbers of volunteers participated in the cleanup efforts, the long term health effects to monitor volunteers focusing on those with relatively longer exposures, are warranted. Authors' contributions MH, HK, and SL made contributions to the conception and design and MH, SGP, SJY, and SL to the acquisition of data. JL, BCC, EJK analyzed the data, and MH, JL, and HK drafted the manuscript. All authors participated in the interpretation of data and contributed to the revision. All authors read and approved the final revised manuscript. Supplementary data related to this article can be found online at doi:10.1016/j.scitotenv.2012.04.036 Acknowledgments This study was supported by a special Grant for the Investigation of Acute Health Effects of the Hebei Spirit Oil Spill, Ministry of Environment, Republic of Korea, 2008. References Agency for Toxic Substances and Disease Registry. US Department of Health and Human Services. Public health service: toxicological profile for fuel-oil; 1995 [http://www.atsdr.cdc.gov/toxprofiles/tp75.pdf]. (Accessed April 2009)].
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Kim H, Cho SH, Kang JW, Kim YD, Nan HM, Lee CH, et al. Urinary 1-hydroxypyrene and 2-naphthol concentrations in male Koreans. Int Arch Occup Environ Health 2001;74(1):59–62. Kim DS, Lee CH, Eom SY, Kang T, Kim YD, Kim H. Effects of the exposure to polycyclic aromatic hydrocarbons or toluene on thiobarbituric acid reactive substance level in elementary school children and the elderly in a rural area. J Prev Med Public Health 2008;41(1):61–7. Lee CY, Lee JY, Kang JW, Kim H. Effects of genetic polymorphisms of CYP1A1, CYP2E1, GSTM1, and GSTT1 on the urinary levels of 1-hydroxypyrene and 2-naphthol in aircraft maintenance workers. Toxicol Lett 2001;123(2–3):115–24. Lee SM, Ha M, Kim EJ, Jeong WC, Hur J, Park SG, et al. The effects of wearing protective devices among residents and volunteers participating in the cleanup of the Hebei Spirit oil spill. J Prev Med Public Health 2009;42(2):89–95. Lee J, M-h Kim, Ha M, Chung BC. Urinary metabolic profiling of volatile organic compounds in acute exposed volunteers after an oil spill in Republic of Korea. Biomed Chromatogr 2010;24:562–8. Lyons RA, Temple JM, Evans D, Fone DL, Palmer SR. Acute health effects of the Sea Empress oil spill. J Epidemiol Community Health 1999;53:306–10. Manini P, De Palma G, Andreoli R, Poli D, Mozzoni P, Folesani G, et al. Environmental and biological monitoring of benzene exposure in a cohort of Italian taxi drivers. Toxicol Lett 2006;167(2):142–51. Marine Environmental Information Service Center. The first year's final report of ocean pollution in Hebei Spirit oil spill (′07.12 ~′08.12). http://www.meis.go.kr/ WebSite_Sub_SCAT/App_Page/Page_List_Report.aspx?&site=3&menu=12&sub= 29&sub2nd=&tab=#tab01. [(Korean) (Accessed March 2012)]. Ministry of Environment, Korea. Investigation of acute health effect of residents and volunteers participating in clean-up works in Hebei Spirit oil spill accident: final report of the United Committee for Investigation of Acute Health Problems in HS Oil Spill [Gwacheon]; 2008 [Korean]. Morita A, Kusaka Y, Deguchi Y, Moriuchi A, Nakanaga Y, Iki M, et al. Acute health problems among the people engaged in the cleanup of the Nakhodka oil spill. Environ Res 1999;81:185–94. Palinkas LA, Russell J, Downs MA, Petterson JS. Ethnic differences in stress, coping, and depressive symptoms after the Exxon Valdez oil spill. J Nerv Ment Dis 1992;180: 287–95. Palinkas LA, Petterson JS, Russell J, Downs MA. Community patterns of psychiatric disorders after the Exxon Valdez oil spill. Am J Psychiatry 1993;150:1517–23. Perez-Cadahia B, Lafuente A, Cabaleiro T, Pasaro E, Mendez J, Laffon B. Initial study on the effects of Prestige oil on human health. Environ Int 2007;33(2):176–85. 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The International Tanker Owners Pollution Federation Limited: Statistics in information service. http://www.itopf.com/informationservices/data-and-statistics/ statistics/#no.; 2008 [Accessed July 2008]. Villanueva MB, Jonai H, Kanno S, Takeuchi Y. Dietary sources and background levels of hippuric acid in urine: comparison of Philippine and Japanese levels. Ind Health 1994;32(4):239–46. Weinhold B. Emergency responder health: what have we learned from past disaster? Environ Health Perspect 2010;118(8):A346–50. Zock JP, Rodriguez-Trigo G, Pozo-Rodriguez F, Barbera JA, Bouso L, Torralba Y, et al. Prolonged respiratory symptoms in clean-up workers of the Prestige oil spill. Am J Respir Crit Care Med 2007;176:610–6. Zock JP, Rodriguez-Trigo G, Pozo-Rodriguez F, Barbera JA. Health effects of oil spills: lessons from the Prestige. Am J Respir Crit Care Med 2011. http: //dx.doi.org/10.1164/rccm.201102-0328ED.
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Urinary metabolites before and after cleanup and subjective symptoms in volunteer participants in cleanup of the Hebei Spirit oil spill Mina Ha a, b,⁎, Hojang Kwon a, b, Hae-Kwan Cheong c, Sinye Lim d, Seung Jin Yoo b, Eun-Jung Kim b, Seok Gun Park e, Jeongae Lee f, Bong Chul Chung f,⁎⁎ a
Department of Preventive Medicine, Dankook University College of Medicine, Cheonan, Republic of Korea Environmental Health Center, Dankook University Medical Center, Cheonan, Republic of Korea Department of Social and Preventive Medicine, Sungkyunkwan University School of Medicine, Suwon, Republic of Korea d Department of Occupational and Environmental Medicine, Kyung Hee University Medical Center, Seoul, Republic of Korea e Department of Nuclear Medicine, Dankook University College of Medicine, Republic of Korea f Integrated Omics Center, Korea Institute of Science and Technology, Seoul, Republic of Korea b c
a r t i c l e
i n f o
Article history: Received 9 September 2011 Received in revised form 9 April 2012 Accepted 10 April 2012 Available online 15 May 2012 Keywords: Oil spill Subjective symptoms Urinary metabolites Cleanup
a b s t r a c t Background: On December 7th, 2007, the Hong Kong tanker Hebei Spirit (HS) (146,848 tons) was crushed by a crane ship near the shore of Taean, Korea. More than 12,547 kl of crude oil spilled into the sea and contaminated the western coastline of the Korean peninsula. For a period of six months after the accident, approximately 1,000,000 volunteers participated in the cleanup. Our goal in this study was to examine the exposure status and acute health effects on volunteers that participated in the oil spill cleanup. Methods: A survey questionnaire was filled out by 565 volunteers, requesting information regarding physical symptoms. Out of the total number of participants, urine samples from 105 university student volunteers were collected before and after the cleanup work, and metabolite levels of volatile organic compounds and polycyclic aromatic hydrocarbons were analyzed. Results: Volunteers that participated for longer cleanup work reported an increase in physical symptoms including visual disturbance, nasal and bronchus irritation, headaches, heart palpitations, fatigue and fever, memory and cognitive disturbance, and abdominal pain. The levels of t,t-muconic acid, mandelic acid, and 1-hydroxypyrene were significantly higher in samples after cleanup than those measured before participation (p b 0.05). Other than the associated risk of dermal irritation with the difference in the t,t-muconic acid level between the post- to pre-cleanup levels, no other physical symptoms demonstrated a significant association with changes observed in the levels of urinary metabolites. Conclusions: Based on the significant increase of subjective symptoms in volunteers participating in the study, monitoring of the long term health effects, focusing on those with longer exposure, is warranted. © 2012 Elsevier B.V. All rights reserved.
1. Introduction The Hong Kong tanker, the Hebei Spirit (HS) collided with a crane ship five miles northwest of Taean's Manri-po Beach, Korea on Dec 7th, 2007. It was estimated that more than 12,547 kl of oil (about
Abbreviations: HS, Hebei Spirit; VOCs, volatile organic compounds; PAHs, polycyclic aromatic hydrocarbons. ⁎ Correspondence to: M. Ha, Department of Preventive Medicine, Dankook University College of Medicine, 201 Mahyangno, Dongnam-gu, Cheoan, Chungnam 330‐714, Republic of Korea. Tel.: +82 41 550 3854; fax: +82 41 556 6461. ⁎⁎ Correspondence to: B.C. Chung, Bioanalysis and Biotransformation Research Center, Korea Institute of Science and Technology, Hwarangno 14-gil 5, Seongbuk-gu, Seoul 136‐791, Republic of Korea. Tel.: + 82 02 958 5067; fax: + 82 02 958 5059. E-mail addresses: [email protected] (M. Ha), [email protected] (H. Kwon), [email protected] (H-K. Cheong), [email protected] (S. Lim), [email protected] (SJ. Yoo), [email protected] (E-J. Kim), [email protected] (SG. Park), [email protected] (J. Lee), [email protected] (BC. Chung). 0048-9697/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.scitotenv.2012.04.036
78,962 bbl or 3,314,562 gal) spilled into the sea. The oil reached the western coastline of the Korean peninsula with a range in spread of 1052 km and was found in Chungnam, Jeonbuk, Jeonnam, and as far as Jeju island. The spill was confirmed as the largest oil spill contamination to occur in Korean history (Ha et al., 2008). The Taean-gun area, an agricultural and fishing region including 119 small islands, 530.8 km of coastline, and an area of 503 km 2 with a recorded population of 63,939 people as of 2006 (County chief of Taean, 2007), received the most severe damage. Three types of crude oil were carried by the HS; UAE Upper Zakum, Kuwait Export Crude, and Iranian Heavy. The main chemical components were primarily composed of hydrocarbons, e.g., volatile organic compounds (VOCs) and polycyclic aromatic hydrocarbons (PAHs), including alkylated types, and minor heavy metals (Marine Environmental Information Service Center, 2009). Approximately 30–50% of VOCs in the crude oil were estimated to be volatized into the air during the first few days after the initial spill. The airborne
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concentrations of PAH (16 PAHs listed on the US EPA priority) were 130–277 ppm and those of alkylated PAHs were 4511–8259 ppm (Marine Environmental Information Service Center, 2009). The HS crude oil also contained traces of heavy metals and released hydrogen sulfide gas (Marine Environmental Information Service Center, 2009). VOC exposure is associated with acute, reversible effects to the CNS (headache, nausea, sleepiness) and irritation of mucous membranes. Prolonged exposure to certain VOCs and PAHs can cause axonal neuropathy. Aromatic compounds, such as 1,2-diethylbenzene, are more potent axonal neurotoxins than aliphatic compounds such as n-hexane (Agency for Toxic Substances and Disease Registry, 1995). Among the crude oil VOCs, benzene is classified as a Group I agent, a proven human carcinogen. Other VOCs including toluene, ethylbenzene, and stylene, belong to Group 2B, which are considered as possible human carcinogens based on published animal studies (International Agency for Research on Cancer, 2006). PAHs such as benzo[a]anthracene, benzo[a]pyrene, and dibenzo[a,h]anthracene are classified into Group 2A, probable human carcinogens, while chrysene, naphthalene, benzo[b]fluoranthene, benzo[k]fluoranthene, and indeno[1,2,3-cd]pyrene are members of Group 2B (International Agency for Research on Cancer, 2006). Following the accident, local residents, along with many other people from around Korea, worked to clean up the spilled oil. A total of 2,122,296 days were estimated as the total number of days dedicated by participants to the cleanup as of July 4th, 2008 (Lee et al., 2009). Most local residents participated in the cleanup for a period of days to several months and both military personnel and governmental employees (59,118 person-days) were also recommended by their organizations to voluntarily participate in the cleanup efforts for several days or months. Professional cleanup workers (about 200–300 persons) covered 48,809 person-days. Additionally, approximately 1,000,000 persons (contributing 1,161,086 person-days) voluntarily gathered at the spill sites to volunteer for a range of a few hours to days to clean up all around the country, i.e., members from civic groups, schools and universities, companies, communities, and families and individuals. Although some studies investigated the health effects of cleanup workers from exposure to an oil spill (Palinkas et al., 1992; Suarez et al., 2005; Carrasco et al., 2006; Zock et al., 2007; Perez-Cadahia et al., 2007, 2008; Rodríguez-Trigo et al., 2010; Goldstein et al., 2011) or local residents living in the polluted sites (Palinkas et al., 1993; Campbell et al., 1993; Crum, 1993; Campbell et al., 1994; Lyons et al., 1999; Morita et al., 1999; Janjua et al., 2006; Carrasco et al., 2007; Sim et al., 2010; Cheong et al., 2011), no study has been reported regarding the exposure of volunteers for a short range of time, including a few hours to several days. Since a huge number of volunteers participated in the cleanup work for the HS oil spill accident, even a small health risk, possibly due to exposure to crude oil during cleanup, may have an important impact on public health. This particular study examined the exposure of volunteers to crude oil by analyzing changes in urinary metabolites of VOCs and PAHs before and after cleanup as well as the incidence of subjective physical symptoms using a survey questionnaire.
2. Materials and methods 2.1. Study subjects The questionnaire survey for volunteers was conducted between the second and third week after the accident (Dec 14, 2007 to Dec 24, 2007). Questionnaires were administered to people working for the cleanup in three contaminated areas at the end of the work day. A total of 724 subjects (out of 1000 questionnaires distributed) responded to the questionnaire, which included questions about the cleanup work conducted, physical symptoms, and other socio-
demographic factors. After excluding incomplete questionnaires, 565 questionnaires were analyzed and included in our study. A subgroup of the total number of participants, included a group of university students (n = 312), who were organized by a university, were also asked to provide their urine before and after the cleanup work participation. A total of 121 out of 272 students responded to the questionnaire and provided urine samples, and a total of 105 urine pairs were analyzed after excluding unpaired urine. The study protocol was approved by the Institutional Review Board of Dankook University Hospital, and informed consent was obtained from all subjects. 2.2. Survey questionnaire on the cleanup work and subjective symptoms The authors developed a symptom questionnaire based on the possible effects of the crude oil composition (Agency for Toxic Substances and Disease Registry, 1995) following the format of previously published questionnaires and reported symptoms for oil spill accidents in other countries (Janjua et al., 2006; Rodriguez-Trigo et al., 2007). A total of 41 physical symptoms were grouped into 14 categories classified with regard to organ systems, which were described in previous reports (Lee et al., 2009; Cheong et al., 2011): eye irritation, visual disturbance, nasal irritation, sore throat, bronchial irritation, dermal irritation, headache, palpitations (fast heartbeat), nausea or vomiting, abdominal pain, fatigue and fever sensation (heat-stress related), memory or cognitive function disturbances, musculoskeletal symptoms, and back pain. Information on the duration of cleanup work was obtained (“How many days did you participate in the cleanup efforts?”(one day or more than one day) and “If the response is more than one day, write in the total number of days”). The type of job responsibility could be chosen among three possibilities: participating in direct cleanup work (i.e., oil skimming, cleaning of rocks, sands, and wildlife), a logisticsrelated job (i.e., pouring, moving or transporting oil trash), and others. The degree of skin contamination to oil could be reported as “not at all,” “a bit,” “much,” or “profound”. We also obtained and identified demographic information as confounders or covariates: age (open question, which was categorized: ≤29, 30–b39, 40–b49, or 50 or more), gender, occupation (students, office workers, manufacturing workers, agriculture, fishery, others), educational level (b12, 12, 13 or more years), current smoker (no, yes), health concerns about the oil spill (no, yes), past history of asthma diagnosis (no, yes), and wearing protective items, such as work clothes, gloves, boots, and mask (no or yes for each). 2.3. VOCs and PAHs metabolite analysis in urine sample pairs Urine collection was performed prior to the work day between 6 and 7 a.m. and at the end of the work day between 7 and 8 p.m. Collected urine samples were immediately stored in a portable refrigerator and transported to −20 °C freezers within 4 h of collection. One month later, the urine samples were packed on dry ice and transferred to the laboratory for analysis. Among the aromatic hydrocarbons, which composed approximately 30% of all chemicals in the HS crude oil, the VOCs, including benzene, toluene, ethylbenzene, and xylene (BTEX) composed 53–65%, followed by 33–45% of alkylated PAHs and 1% of 16 PAHs listed on the US EPA priority list (Marine Environmental Information Service Center, 2009). Based on the information on the chemical compositions of the oil spill and their known health effects, five metabolite compounds, t,t-muconic acid, mandelic acid, 2-methyl hippuric acid, 3-methyl hippuric acid, 4-methyl hippuric acid, and hippuric acid, were analyzed using gas chromatography–mass spectrometry (GC–MS, Agilent Technologies, Santa Clara, CA, USA). The analysis methods for metabolites of VOCs have previously been described in detail (Lee et al., 2010).
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We analyzed 1-hydroxypyrene and 2-naphthol as biomarkers of exposure to crude oil containing various PAHs. Two milliliters of each urine sample was combined with a 20 μl solution of 1 mg/L internal standards (1-naphthol-d7). Urine samples were enzymatically hydrolyzed by the addition of 1 ml of 0.2 M acetate buffer (pH 5.2), 50 μl of 0.2% ascorbic acid, and 50 μl of glucuronidase/ arylsulfatase (from Helix Pomatia, Penzberg, Germany) for 3 h at 55 °C. The hydrolyzed urine samples were subjected to Strata-X™ cartridges (60 mg, 3 ml; Phenomenox, Torrance, CA, USA), which were preconditioned five times with 2 ml of methanol and 2 ml of distilled water. After loading the samples, the cartridges were washed with 2 ml of 10% methanol. Urinary PAH metabolites were then eluted two times with 2 ml of 90% methanol, which were subsequently evaporated under nitrogen. The dried residues were derivatized with 40 μl of mixture reagent (MSTFA/TMCS/TMSI; 100:5:2, v/v/v) and heated at 60 °C for 15 min. A 2 μl derivatized aliquot was injected into the GC–MS (Agilent Technology, Santa Clara, CA, USA). The limit of detection (LOD, ng/mL) and limit of quantization (LOQ, ng/mL) were 3 and 10 for t,t-muconic acid and mandelic acid, 10 and 30 for (1,2,3-) methyl hippuric acid, 0.2 and 0.5 for 2-naphthol and 0.5 and 1.0 for 1-hydroxypyrene, respectively. 2.4. Statistical analysis The geometric means of the VOC and PAH metabolite concentrations in subjects before and after participation in the oil spill cleanup were calculated for 105 university student volunteers and compared using a paired t-test. Multiple logistic regression adjusted for age, gender, smoking, educational level, history of diagnosed asthma, health concern about the oil spill, and survey area was performed to estimate odds ratios and 95% confidence intervals of subjective physical symptoms for different types and the duration of cleanup work or urinary metabolite level differences between pre- and post-cleanup work. All analyses were conducted using SAS for windows (ver 9.2, SAS Institute Inc., Cary, NC, USA) with the significance set at a p value b 0.05. 3. Results Most of the study subjects were students in their 20s, non-smokers, participated in cleanup work for one day and were involved in direct cleanup jobs. Most subjects (84.6%) reported either no or a small amount of skin contamination by crude oil but almost all (more than 95%) were wearing good protective gear. Half of them were concerned about the health effects from the oil spill (Table 1). Out of a group of 13 people who reported two or more days of cleanup duration, the mean duration of work was 5.4 days (maximum = 15 days). The skin contamination rate was significantly higher in people involved in logisticsrelated jobs requiring an increased level of physical activity (91.4%) than in direct cleanup (71.6%), while no significant difference was seen in the proportion of individuals wearing protective devices between the two types of jobs. Out of 105 students who provided urine sample pairs, the average age was 20.9 years old (standard deviation, 2.1; range, 18 to 29), 12.4% (n = 13) were female and 19% (n = 20) were smokers. Eye (46.9%) and nose (41.6%) irritation and headache (42.0%) demonstrated the highest rate of positive symptoms, followed by fatigue and fever sensation (37.4%) and musculoskeletal symptoms (35.9%). People having logistics-related jobs and with longer durations showed increased rates of positive symptoms compared to those participating in the direct cleanup efforts and within a shorter period of time, respectively. In a full model including both type of jobs and the duration of work, the risks of visual disturbance, palpitation, fatigue and fever sensation, memory and cognitive disturbance, abdominal pain, nasal and bronchus irritation, and headache were
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Table 1 Socio-demographic characteristics of study subjects, 565 volunteers in the Hebei Spirit oil spill, 2007, Taean, Korea. Characteristics Survey areas A Ba C Age (years) 29 or less 30–b39 40–b49 50 or more Unknown Gender Male Female Unknown Occupation Student Office worker Fishery Others Unknown Education (years) b12 12 >12 Unknown
No.
(%)
107 313 145
(18.9) (55.4) (25.7)
457 46 44 14 4
(80.9) (8.1) (7.8) (2.5) (0.7)
275 288 2
(48.7) (51.0) (0.4)
402 114 1 31 17
(71.2) (20.2) (0.2) (5.5) (3.0)
16 50 485 14
(2.8) (8.8) (85.8) (1.9)
Duration of cleanup work 1 day 2 days or more Type of job involvedb Direct cleanup Logistics-related job Unknown Skin contamination to oilc Not at all A bit Much Profound Unknown Health concern about oil spill No Yes Unknown Current smoking No Yes Unknown Past history of asthma diagnosed No Yes Unknown
No.
(%)
552 13
(97.7) (2.3)
444 106 15
(78.6) (18.8) (2.7)
95 269 50 4 2
(22.6) (64.0) (11.9) (1.0) (0.5)
284 264 17
(50.3) (46.7) (3.0)
434 99 32
(76.8) (17.5) (5.7)
531 24 10
(94.0) (4.2) (1.8)
a 272 volunteers in area B were a group of students from a university, a part of them agreed to provide a pair of their urine samples before and after cleanup work. b Direct cleanup work included oil skimming, cleaning of rocks, sand, and wildlife; logistics-related jobs included pouring, moving, or transporting oil and trash. c The questionnaire administered to 145 subjects (by survey area C) did not have the question, and the percentages were calculated in 420 subjects.
significantly increased in subjects who worked for two days or more compared to those who worked for one day. Only the risk of palpitation was increased in people participating in logistics-related jobs compared to those participating in direct cleanup jobs (Fig. 1A). Metabolites of VOCs, t,t-muconic acid, mandelic acid, and those of PAHs, 1-hydroxypyrene, showed significantly increased levels after cleanup work compared to those measured before the cleanup work. Those of total methyl-hippuric acid, hippuric acid, and 2-naphthol showed no statistically significant difference between levels measured before and after cleanup work (Table 2). None of the metabolites were significantly different according to the degree of skin contamination to oil (Supplemental Table) or type of job (data not shown). Among 14 subjective physical symptoms, the risk of dermal irritation was associated with the level of difference pre and post of t,t-muconic acid. No statistically significant associations between the urinary level of pre and post differences of the VOCs and PAHs metabolites and physical symptoms were observed (Fig. 1B).
4. Discussion Volunteers participating for longer durations in the cleanup of the HS oil spill demonstrated several increased physical symptoms. The urinary levels of some VOC and PAH metabolites were significantly higher following cleanup than levels obtained before, although no material associations were observed between increased urinary levels due to the cleanup efforts and physical symptoms with the exception of t,t-muconic acid and dermal irritation. Although most of the volunteers in this study were only involved in a few hours of cleanup, their physical symptoms were generally similar with those reported by cleanup workers or local residents in other reported oil spill accidents (Campbell et al., 1993; Lyons et al., 1999; Morita et al., 1999; Suarez et al., 2005; Janjua et al.,
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A)
Work type (Logistics-related work vs direct cleanup) 0.0
0.2
1.0
5.0
25.0
Work duration (2 days+vs 1 day) 0.0
0.2
1.0
5.0
25.0
OR (95% CI) Eye irritation Visual disturbance Nasal irritation Sore throat Bronchial irritation Dermal irritation Headache Palpitation Nausea, vomiting Abdominal pain Fatigue and fever sensation Memory/cognitive disturbance Musculoskeletal symptom Back pain
B)
tt-muconic acid 0.0
0.2
1.0
Mandelic acid 5.0
0.0
0.2
0.0
0.2
1.0
Hippuric acid 5.0
0.0
0.2
1.0
5.0
OR (95% CI) Eye irritation Visual disturbance Nasal irritation Sore throat Bronchial irritation Dermal irritation Headache Palpitation Nausea, vomiting Abdominal pain Fatigue and fever sensation Memory/cognitive disturbance Musculoskeletal symptom Back pain
total methyl-hippuric acid 0.0 Eye irritation
0.2
1.0
5.0
2-naphthol 1.0
1-hydroxypyrene 5.0
0.0
0.2
1.0
5.0
OR (95% CI)
Visual disturbance Nasal irritation Sore throat Bronchial irritation Dermal irritation Headache Palpitation Nausea, vomiting Abdominal pain Fatigue and fever sensation Memory/cognitive disturbance Musculoskeletal symptom Back pain
Fig. 1. Odds ratios and 95% confidence intervals of subjective physical symptoms for type and duration of cleanup work in 565 volunteers (A) and urinary levels of pre- and postdifference of urinary metabolites in 105 student volunteers (B) in the Hebei Spirit oil spill, 2007, Taean, Korea. OR: odds ratio, CI: confidence intervals. Direct cleanup work included oil skimming, cleaning of rocks, sand, and wildlife; logistics-related jobs included pouring, moving, or transporting oil and trash. OR and 95% CI of each symptom for job type and duration of work estimated simultaneously using one multiple logistic regression model adjusted for age, gender, smoking, educational level, history of asthma diagnosed, health concern about oil spill, and survey groups (full model) (A). The level of urinary metabolites was the difference between levels before and after cleanup work. OR and 95% CI estimated for subjects with upper 50% of biomarker level referenced by those with lower 50% using multiple logistic regression model adjusted for age, gender, smoking, educational level, history of asthma diagnosed, and health concern about oil spill (B).
M. Ha et al. / Science of the Total Environment 429 (2012) 167–173
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Table 2 Urinary concentration of VOC and PAH metabolites in 105 student volunteers before and after cleanup in the Hebei Sprit oil spill, 2007, Taean, Korea. All (N = 105)
VOC metabolites t,t-muconic acid (μg/g cr.)
Mandelic acid (mg/g cr.)
Hippuric acid (mg/g cr.)
Total methyl-hippuric acid (mg/g cr.)
PAHs metabolites 2-Naphthol (μg/g.cr.)
1-Hydroxypyrene (μg/g cr.)
Smokers (N = 20)
Non-smokers (N = 79)
G mean
(Range)
G mean
(Range)
G mean
(Range)
Before After p-value Before After p-value Before After p-value Before After p-value
70.20 211.49
(14.31, 1223.04) (72.43, 608.34) b.0001 (0.00, 0.29) (0.02, 0.58) b.0001 (17.90, 1701.43) (4.30, 2527.45) 0.79 (0.01, 2.35) (0.06, 0.49) 0.27
87.78 218.89
(22.25, 541.31) (72.83, 525.73) 0.01 (0.05, 0.23) (0.13, 0.37) 0.001 (24.99, 775.19) (27.98, 638.40) 0.17 (0.05, 0.49) (0.12, 0.49) 0.10
65.80 208.73
(14.31, 1223.04) (72.43, 608.34) b.0001 (0.00, 0.29) (0.02, 0.58) b.0001 (17.90, 1701.43) (4.30, 2527.45) 0.72 (0.01, 2.35) (0.06, 0.43) 0.66
Before After p-value Before After p-value
1.27 2.41
0.10 0.19 175.51 147.08 0.14 0.21
0.96 1.58
(0.08, (0.10, 0.50 (0.13, (0.05, 0.003
0.12 0.19 187.16 149.57 0.17 0.27
382.01) 165.04)
4.67 3.14
22.17) 24.5)
0.98 1.36
(0.14, (0.24, 0.32 (0.21, (0.20, 0.29
0.09 0.19 173.92 159.06 0.14 0.20
40.03) 23.32)
0.97 2.41
5.46) 8.97)
0.95 1.66
(0.08, (0.10, 0.45 (0.13, (0.05, 0.007
382.1) 165.0) 22.17) 24.56)
G mean: geometric mean, VOCs: volatile organic compounds, PAHs: polycyclic aromatic hydrocarbons. p-value calculated using paired t-test.
2006; Perez-Cadahia et al., 2007; Sim et al., 2010; Cheong et al., 2011; Goldstein et al., 2011), mainly symptoms of mucosal irritation and headaches, which were induced from direct contact with or inhalation of vaporized crude oil and hydrogen sulfide gas. The increased rates of musculoskeletal symptoms and back pain, which are not supposed to be direct effects of crude oil exposure, may be explained by the fact that most volunteers were students or office workers who usually are not accustomed to the manual labor required for this type of cleanup work, i.e., frequent bending over and heavy lifting. During an initial period after the accident, the evaporation of the most volatile components from VOCs and PAHs is the major exposure factor and biomarker measured at this phase. Although the exposure duration in the present student volunteers was limited, the half lives of metabolites are relatively short and the levels of them measured at the time of pre- and post-exposure may be well reflected in the internal exposure of the crude oil. The main components of oil spills are presumably similar, but proportions of those components are most likely altered between different oil spills (Rodríguez-Trigo et al., 2010). While the oil spills from the Erika and Prestige tankers contained heavy fuel oil with a high sulfur content (4%) (Rodríguez-Trigo et al., 2010), which was a heavy fraction of refined oil, that of the HS is unrefined crude oil with low sulfur content (1%) and was mainly composed of saturated (53%) and aromatic (30%) hydrocarbons (Marine Environmental Information Service Center, 2009). Therefore, direct comparisons of the levels of exposure biomarkers between different oil spills are not necessarily appropriate but may be helpful to understand the general exposure characteristics and health effects of oil spills. Unfortunately, only two oil spill accidents reported urinary metabolites of VOCs (Campbell et al., 1993; Morita et al., 1999), but none reported PAHs. While no reports have been published on the level of t,t-muconic acid in previous oil spills, the post cleanup t,tmuconic acid level was similar with an occupationally exposed group, i.e., taxi drivers and slightly higher than a control population reported in Italy and Iran (Manini et al., 2006; Bahrami et al., 2007). The post cleanup hippuric acid level was similar with those reported in local residents 7–12 days after the occurrence of the Braer oil spill (Campbell et al., 1993) but slightly higher than the general populations in Japan, the Philippines (Villanueva et al., 1994) and Korea (Kim et al., 2008). The level of 2-naphthol in subjects after the cleanup was not higher than those reported for occupationally exposed groups in
Korea (Lee et al., 2001; Kim et al., 2001). However, the level of 1hydroxypyrene after cleanup was much higher than those previously reported among various groups in Korea (Kim et al., 2001; Kang et al., 2002; Kim et al., 2008), including aircraft maintenance workers (Lee et al., 2001) and shipyard workers (Kim et al., 2001). Therefore, exposure to crude oil in volunteers seems to be reflected well with the level of 1-hydroxypyrene rather than in 2-naphthol, while the levels of both metabolites of PAHs are within the range of the background level of the German general population (Schulz et al., 2012). The post cleanup levels of biomarkers in the volunteers were not higher than those in the residents participated in cleanup of HS oil spill with the exception in t,t-muconic acid and 1-hydroxypyrene (Cheong et al., 2011). It may be partly due to a different sampling time since the accident: at two weeks after the accident in the student volunteers and three or more weeks after in the residents. No significant differences observed in the levels of biomarkers according to the degree of skin contamination may suggest that oil absorption through skin contamination does not play a major role, compared to inhalation or ingestion, in terms of the exposure pathways from oil spills. No associations between the levels of urinary VOC and PAH metabolites and physical symptoms were observed, except for t,t-muconic acid and dermal irritation, which may be partially due to the lack of statistical power. There have been 1744 reported accidents spilling more than 7 tons of oil from 1970 to 2007 for a total of 5,648,000 tons of oil spilled into the ocean worldwide (International Tankers Owners Pollution Federation Limited, 2008, 2010). Furthermore, the recent BP oil spill in the Gulf of Mexico released almost 5 billion barrels of crude oil for a period of four months (Goldstein et al., 2011; Zock et al., 2011). In spite of the high frequency and huge volume of oil spilled, only a few studies regarding the health effects as a direct result of oil spills have been performed and summarized (RodriguezTrigo et al., 2007; Ha et al., 2008; Aguilera et al., 2010; Goldstein et al., 2011). Usually, many people voluntarily rush to the disaster site immediately after an accident and often do not have the training and advanced equipment that protect professional emergency responders to some degree (Weinhold, 2010). Therefore, the health risk may be even greater for the many non-professional emergency responders (Weinhold, 2010). In addition, crude oil contains various
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types of carcinogenic chemicals which could induce genetic toxicity after a period (Rodriguez-Trigo et al., 2007; Rodríguez-Trigo et al., 2010). Theoretically mutagenic effects can result from a single molecular DNA alteration without a threshold concentration of exposure (Goldstein et al., 2011). A long-term follow-up surveillance program involving people exposed to crude oil, particularly for various types of cancer, needs to be considered for volunteer cleanup workers as well. The present opportunistic study successfully conducted a survey questionnaire and for the first time to date, collected urine sample pairs before and after cleanup efforts immediately after the accident and established the potential importance regarding the issues related to the health of volunteers due to their participation in the oil spill cleanup. However, this study has several limitations. First, because the sampling time of urine was two weeks past the initial accident, the highest exposure to VOCs and PAHs, which occurred within a few days of the spill, could not be reflected in the urine samples analyzed in the present study. According to simulation results involving PAH evaporation from spilled oil (Ministry of Environment, Korea, 2008), PAH exposure was sustained for at least several months. Therefore, collected urine samples in the present study may reflect this extended exposure of PAHs. Second, the study does not have a non-exposed control group, meaning that we could not compare exposed and nonexposed subjects for the risk of physical symptoms. Third, the selfreported physical symptoms are subjective; thus, a misclassification bias might be present in this study. However, this is unlikely because most volunteers, unlike local residents, presumably do not have conflicts of interest related with economic compensation and no intention to exaggerate their health effects. In fact, there was no significant difference in the rate of positive symptoms between people who reported health concerns about oil spills and those who did not, with an exception for the symptoms of headache and nausea/vomiting, of which the concerned people demonstrated a higher symptom positive rate in the present study. Fourth, the small number of subjects and restricted survey areas in this study might not represent the entire population of volunteers participating in cleanup work, particularly those who participated for longer periods of time. In conclusion, we found that increasing physical symptoms were associated with longer durations of work and significantly higher VOC and PAH metabolite levels following cleanup than observed prior to cleanup. Based on the fact that large numbers of volunteers participated in the cleanup efforts, the long term health effects to monitor volunteers focusing on those with relatively longer exposures, are warranted. Authors' contributions MH, HK, and SL made contributions to the conception and design and MH, SGP, SJY, and SL to the acquisition of data. JL, BCC, EJK analyzed the data, and MH, JL, and HK drafted the manuscript. All authors participated in the interpretation of data and contributed to the revision. All authors read and approved the final revised manuscript. Supplementary data related to this article can be found online at doi:10.1016/j.scitotenv.2012.04.036 Acknowledgments This study was supported by a special Grant for the Investigation of Acute Health Effects of the Hebei Spirit Oil Spill, Ministry of Environment, Republic of Korea, 2008. References Agency for Toxic Substances and Disease Registry. US Department of Health and Human Services. Public health service: toxicological profile for fuel-oil; 1995 [http://www.atsdr.cdc.gov/toxprofiles/tp75.pdf]. (Accessed April 2009)].
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