Health Changes in Fishermen 2 Years After Clean-up of the Prestige Oil Spill
- Gema Rodríguez-Trigo, MD;
- Jan-Paul Zock, PhD;
- Francisco Pozo-Rodríguez, MD;
- Federico P. Gómez, MD;
- Gemma Monyarch, MSc;
- Laura Bouso, MSc;
- M. Dolors Coll, PhD;
- Héctor Verea, MD;
- Josep M. Antó, MD;
- Carme Fuster, PhD;
- Joan Albert Barberà, MD; and
- for the SEPAR (Sociedad Española de Neumología y Cirugía Torácica)-Prestige Study Group*
+Author Affiliations
Abstract
Background: In 2002, the oil tanker Prestige spilled more than 67 000 tons of bunker oil, heavily contaminating the coast of northwestern Spain.
Objective: To assess respiratory effects and chromosomal damage in clean-up workers of the oil spill 2 years after the exposure.
Design: Cross-sectional study.
Setting: Fishermen cooperatives in coastal villages.
Participants: Local fishermen who were highly exposed (n = 501) or not exposed (n = 177) to oil 2 years after the spill.
Measurements: Respiratory symptoms; forced spirometry; methacholine challenge; markers of oxidative stress (8-isoprostane), airway inflammation (interleukins, tumor necrosis factor-α, and interferon-γ), and growth factor activity in exhaled breath condensate; and chromosomal lesions and structural alterations in circulating lymphocytes.
Results: Compared with nonexposed participants, persons exposed to oil were at increased risk for lower respiratory tract symptoms (risk difference, 8.0 [95% CI, 1.1 to 14.8]). Lung function did not significantly differ between the groups. Among nonsmoking participants, exposed individuals had higher exhaled 8-isoprostane levels than nonexposed individuals (geometric mean ratio, 2.5 [CI, 1.7 to 3.7]), and exposed individuals with lower respiratory tract symptoms had higher 8-isoprostane levels than exposed individuals without symptoms. Exposed nonsmoking participants also had higher levels of exhaled vascular endothelial growth factor (risk difference, 44.8 [CI, 27.9 to 61.6]) and basic fibroblast growth factor (risk difference, 16.0 [CI, 3.5 to 28.6]). A higher proportion of exposed participants had structural chromosomal alterations (risk difference, 27.4 [CI, 10.0 to 44.8]), predominantly unbalanced alterations. The risk for elevated levels of exhaled 8-isoprostane, vascular endothelial growth factor, basic fibroblast growth factor and structural chromosomal alterations seemed to increase with intensity of exposure to clean-up work.
Limitations: The clinical significance of exhaled biomarkers and chromosomal findings are uncertain. The association between oil exposure and the observed changes may not be causal. The findings may not apply to spills involving other types of oil or to different populations of oil spill workers.
Conclusion: Participation in clean-up of a major oil spill was associated with persistent respiratory symptoms, elevated markers of airway injury in breath condensate, and chromosomal damage.
Primary Funding Source: Instituto de Salud Carlos III, Spanish Ministry of Science and Innovation.
Editors' Notes
Context
- Oil spills are ecological disasters, but their health effects on humans are not well known.
Contribution
- This study found that Spanish fishermen who participated in the clean-up of a coastal oil spill had a higher prevalence of respiratory symptoms, higher levels of markers suggestive of airway injury in exhaled breath condensate, and chromosomal alterations in lymphocytes compared with those who did not participate in clean-up activities.
Caution
- The clinical significance of the marker and chromosomal findings is not known. The study does not prove that oil exposure caused the abnormalities.
Implication
- Participation in clean-up of a major oil spill seemed to have adverse health effects. The clinical significance of the findings is not known.
—The Editors
More than 2.2 billion metric tons of oil is shipped by tanker every year around the world by a fleet comprising more than 11 000 oil tankers. Between 1974 and 2008, more than 9000 tanker incidents were reported, among which 348 resulted in spills of more than 700 tons of oil (1). Oil spills cause great public concern, especially among people living in affected coastal areas, and large numbers of volunteers are mobilized to clean up the oil sediment.
Consequences of oil spills are usually evaluated in terms of environmental damage, effects on marine species, and economic losses, but relatively little is known about the effects of oil exposure on humans. Acute exposure to aromatic hydrocarbons, which are common constituents of oil, are known to cause respiratory symptoms (2). Certain volatile organic oil compounds, in particular benzene, are carcinogenic in humans and have been associated with hematologic cancer (3). Exposure to polycyclic aromatic hydrocarbons can damage the skin and mucous membranes and have been implicated in the pathogenesis of skin tumors (4).
In November 2002, the oil tanker Prestige foundered and spilled more than 67 000 tons of bunker oil, heavily contaminating the coast of Galicia in northwestern Spain. The spilled oil contained aromatic hydrocarbons (including benzene), saturated hydrocarbons, heavy metals, resins, and asphaltenes (5). More than 300 000 volunteers participated in clean-up activities; among them, local fishermen were a large and highly exposed group. Studies of persons who participated in clean-up activities either as volunteers or as paid workers during the active period of clean-up showed that exposure to oil was associated with genomic damage (6–8), and a questionnaire that we distributed to fishermen showed increased rates of respiratory symptoms 1 to 2 years after participating in clean-up (9).
We sought to follow up those observations in this study of longer-term health effects of the Prestige oil spill. Specifically, we evaluated changes in lung function, assessed respiratory markers of oxidative stress and airway inflammation in exhaled breath condensate (10), and assessed chromosomal damage, a biomarker of increased risk for cancer (11, 12), 22 to 27 months after the spill in fishermen who had been highly exposed to oil during the clean-up work. We hypothesized that exposure to spilled oil would be associated with persistent abnormalities in lung function, inflammatory and oxidative changes in the airways, and evidence for genotoxicity similar to those reported in other occupational exposures to oil and its components (13–16).
Methods
Design and Participants
Study participants were fishermen who had taken part in a previous questionnaire survey that included qualitative and quantitative information about participation in clean-up activities (9). Using this self-reported information, we distinguished exposed from nonexposed individuals (Figure). Exposed individuals (n = 1119) were members of fishermen cooperatives in heavily affected areas of the Atlantic coast who had participated at least 15 days in clean-up activities, for 4 or more hours per day, including November-December 2002, when exposure presumably was greatest. Nonexposed fishermen (n = 577) were members of cooperatives in areas of the Cantabrian coast (which was less affected by the oil spill) who did not participate in clean-up activities for reasons other than those related to health. Among the 598 (53%) exposed and 205 (35%) nonexposed fisherman who agreed to participate in the study, 97 exposed and 28 nonexposed individuals reported inconsistencies in details of clean-up work in a subsequent interview and were excluded from this analysis, leaving 501 exposed and 177 nonexposed persons in the final study population (Figure).
Figure. Study flow diagram.
* Participated in clean-up activities for at least 15 days, for 4 or more hours per day on average, including November and December 2002.
† Did not participate in clean-up activities for non–health-related reasons.
‡ Met the above inclusion criteria both at the questionnaire survey and at the face-to-face interview of our study.
§ Participants reported never having had asthma both at the questionnaire survey and at the face-to-face interview.
|| 8-Isoprostane was measured in all participants indicated; the numbers in brackets indicates those for whom additional analyses of cytokines and growth factors were done.
¶ Participants reported having children (which proved their fertility) and had no history of malignant neoplasms.
The study was performed between September 2004 and February 2005, 22 to 27 months after the spill and almost 2 years after most of the exposed participants came into contact with the oil (Appendix Figure 1 shows the timing of events). A face-to-face interview and obtaining of the outcome measures were performed on the same day at the fishermen cooperative in a mobile unit that traveled to participants' coastal villages; because the coastal area affected by the oil spill was known, nurses obtaining the measures were not blinded to exposure status. The project was approved by the Ethics Committee on Clinical Research of Galicia, and all participants provided written informed consent.
Appendix Figure 1. Timeline of the study relative to the oil spill and clean-up events.
Interview and Clinical Testing
All participants completed a second interviewer-led questionnaire on respiratory symptoms and medication use, smoking habits, participation in clean-up activities, and characteristics of these activities. Items in this questionnaire were the same as in the previous survey (9). Participants underwent spirometry testing for FEV1 and FVC and methacholine challenge; bronchial hyperresponsiveness was defined as a 20% decrease in FEV1 associated with a methacholine dose of 2 mg or less. Participants also had serum total IgE measurement and skin prick testing for 19 common and occupational allergens to help distinguish intrinsic (atopic) from extrinsic (environmental) causes of symptoms. Atopy was defined as a positive reaction to at least 1 of the tested allergens (Appendix Table 1).
