Exposure to oil and oil products either directly or indirectly causes severe health issues in human that are principally depend on the type of contact with the oil spill. Direct exposures include breathing contaminated air (volatile fractions which are emitted as gases), and direct contact with the skin (while walking in contaminated areas). Indirect exposures to oil are due to bathing in contaminated water and eating contaminated food. Human health is badly affected by TPHs, and the effects are largely depending on type and site (land, river, and ocean) of oil spilled.
Other contributing factors that affect the human health upon oil exposure are what kind of exposure and how much exposure there was.
Cleaning workers at the oil spill site are at more risk. Health disorders include skin and eye irritation, breathing and neurologic problems, and stress. TPHs have a strong impact on mental health, induce physical/physiological effects, and they are potentially toxic to genetic, immune and endocrine systems.
Even though, long-term effects of TPHs in human are not fully understood yet, certain symptoms may persist for some years of post-exposure period. Thus, health protection in exposed individuals is a matter of concern. Health risk assessments have greatest impact in enabling the detection of any potential exposure-related harmful effects either at the time of exposure or for prolong periods following exposure. In this direction, the present chapter has been designed to provide comprehensive insights into understanding the effects of TPHs on human health.
Oil exploitation is usually consisting of several operational steps like exploration, extraction, refinement, and transportation.
But all these processes leave certain extent of environmental damage, including human health issues. Oil is a complex mixture variety of chemicals such as benzene, toluene, xylene, and polycyclic aromatic hydrocarbons (PAHs), and all these factions have wide range of toxicological properties. Once these fractions are discharged into the environment, they easily bioaccumulate in food chains, results in the disruption of biochemical and physiological activities in many ingested organisms and cause wide array of disorders and most important are carcinogenesis, mutagenesis, impaired reproductive capacity in exposed population.
TPHs come in direct contact with nature in different forms like atmospheric emissions, waste generation, and effluents and subsequently pollute air, water and soil. It is known that the contaminated river water contains PAHs at 10 to 10,000 times greater that the U.S. EPA guidelines, such polluted water is a used as a food source for finishing and for irrigation. The fundamental routes for the entry of TPHs into human body are absorption through the skin, ingestion of food and drink, or inhalation through breathing. But it is important to note that oil exposure is also possible even though they are not close to pollution. Because, one side heavier fractions tend to deposit sediment and contaminate surface waters by leaching or ground water by seeping. On the other side, spilled fractions are consumed by organisms and can enter the human food chain.
Once TPHs enter the human body, they often take months to produce a disease, and in severe cases it leads to death. Thus, post-impact assessments are important in assessing the long-term human health effects on impacted communities. As of now, the majority crude oil spills are due to technological disasters and reported in many high population density geographical areas including Mediterranean Europe, North Africa, North America etc. and simultaneously many studies have tried to provide epidemiological information from these parts of the globe (Linet et al., 2015). The adverse health disorders associated with exposure to oil products or TPHs include hematopoietic, hepatic, renal and pulmonary abnormalities, changes in cognitive functions, psychological problems, damage to reproductive and respiratory systems, cancer, and several general health problems. The toxicity of individual fractions has also been studied for certain extent.
Best example is benzene, which is present both in crude oil and gasoline, has been identified as a causative agent of leukemia in humans. This compound is also known for its activity of lowering white blood cells in human, which leads to immune suppression and increased susceptibility to infections in human. Studies have also identified the link between benzene exposure (ppb) and disorders like terminal leukemia, Hodgkin’s lymphoma, and other blood and immune disfunctions in people upon early-age exposure (5-15 years) to benzene. Nevertheless, the environmental impacts of TPHs are mainly negative due to their toxicity and contributes various illnesses in humans. The subsequent sections of this chapter provide in depth details on readily available sources of petroleum hydrocarbons for the human exposure, principal routes for the entry and establishment of these pollutants into the human body, impacts of TPHs on human health, and risk assessment strategies.
After Exxon Valdez disaster (Alaska, US), nearly 1,811 compensation claims were filed by affected individuals, who were suffering from different health problems, such as cuts, contusions, dermatitis, respiratory problems and sprains (Gina, 2010). In fact, oil exposed individuals at Exxon Valdez spill site were more likely to have anxiety disorder, post-traumatic stress disorder and depression by 3.9, 2.9 and 2.1 times, respectively. Risk of spontaneous abortions are nearly 2.5 times higher in woman who live closer to the oil fields or spill sites. People living in 5 km radius at the Braer oil spill (Shetland, Scotland) in 1993 had a high prevalence of certain health disorders including dermatitis, headache, itchy eyes and throat irritation besides DNA adducts and other genetic abnormalities. Similarly, victims of Sea Empress oil spill (Pembrokeshire, Wales, UK) in 1996, showed headaches, sore eyes, sore throats, back and leg pains.
Importantly, there was a direct positive correlation between the number of days worked at the spilled site and the number and duration of symptoms. Like the above effects, affected individuals after the Erika oil spill (Brittany, France, 1999) and Prestige oil spill (Galicia, Spain, 2002) also showed general health disorder and genotoxicity effects. The 2010 Deepwater Horizon disaster (Gulf of Mexico near Mississippi River Delta, US) claimed 11 deaths of oil rig workers and released over 200 million gallons of crude oil. Furthermore, recent investigations suggesting that exposure to the oils may also results in the increased risk of nonfatal myocardial infarction within 1-3 years of spillage (Strelitz et al., 2018).
As of now there are no specific medical test to confirm whether a person has been exposed to TPHs or not. However, there are certain indirect methods to confirm the TPH exposure. For example, presence of a breakdown products of n-hexane, benzene, phenol in the urine, detection of benzene in inhaled air confirm the exposure to gasoline or to the TPH fraction containing benzene. Kerosene or gasoline can also be determined by its smell on the breath or clothing. Ethylbenzene, another TPH compound, can be measured in blood, urine, breath, and some tissue specimens of exposed individuals. The main constraints of these detection tests are, firstly, unavailability of these tests at the physicians or clinics; secondly, these tests cannot determine exactly what you were exposed to, since TPHs present in the body could be from exposure to several different compounds.
What is not yet known is, it is certainly difficult to conclude what the long-term effects will be, because still there are relatively few studies have focused on human health effects. More often, air quality monitoring at the time of oil spill is lacking. On the other hand, it is hard to find the coordination in screening the local people. Baseline evaluations are missing and follow up health assessments in affected individuals are very rare. The data is very scanty since not many of the oil spills worldwide have been studied for human health effects. In most cases, by the time of investigation, oil spillage is completed, and the people who have already undergone certain burden of disease and suffering due to the exposure to oil. Therefore, to monitor oil exposed individuals, long term studies are obligatory.
The main routes for the entry and establishment of petroleum hydrocarbons into human body is from breathing ambient air and indoor air, petroleum hydrocarbon contaminated food, smoothing cigarettes, breathing smoke from open file places etc. For example, tobacco smoke contains benzo(a)pyrene and more than 40 known or suspected human carcinogenic petroleum hydrocarbons. There are certain natural sources for the releasing or holding petroleum hydrocarbons in the environment. Certain crops (e.g. wheat, rye, lentils etc.) may synthesize PAHs or adsorb PAHs from environment (water, air or soil). Thus, in non-smoking persons, 70% of PAH exposure is associated with their diet. Food prepared (e.g. Charring meat or barbecuing food) over a charcoal, wood and other type of fire are usually contains high levels of PAHs.
For instance, the levels of PAHs and benzo(a)pyrene in charring meat and smoked fish were found to be 10-20 and 2.0 µg/kg, respectively. Many food stuffs such as cereals, coffee, peanuts, refined vegetable oils, roasted peanuts, spinach, tea contain PAHs. In certain incidences, patients with dermatological disorders (e.g. psoriasis and dandruff) are treated with coal tar products, causes additional PAHs exposure. It has also been reported that PAHs and their metabolites are found in the breast milk, and even they are able to cross the placenta.
Water may contain petroleum hydrocarbons, usually these chemicals are leached into water from polluted soils or from industrial effluents and/or marine accidental spills. Best example for this is Ecuadorian Amazon streams, where the levels of TPHs were found to be in the range of 0.097-2.883 ppm, which is nearly 10 to 288 times higher than the limits set by European Community regulations (0.01 ppm) (San Sebastian et al., 2001), whereas PAHs levels are even 10-10,000 times higher than the US EPA levels (Hurtig and San Sebastian, 2004), which are attributable to intense petrochemical pollution caused due to the use of inadequate and outdated oil extraction methods by oil companies for > 25 years between 1964 and 1990. Regarding of benzo(a)pyrene concentration in water, always its concentration is lower in drinking water than untreated water, and it is about 100-fold lower than the U.S. EPA (Environmental Protection Agency) drinking water standard.
According to EPA, 0.2 ppb of benzo(a)pyrene in drinking water is considered as maximum contaminant level (MCL). Airborne fallouts are key source of PAHs in soil. In soils, up to 200,000 µg PAHs per kg of dried soil has been documented near oil refineries, however, soils near the cities and areas with heavy traffic are typically having 100 times lesser PAHs’ contents than the soils nearby oil refineries. It is worth noting that sources other than petrogenic origin also vital in PAHs burden in the environment. According to one investigation, 6% of soil PAHs were contributed by petrogenic sources, whereas coal combustion, biomass burning, creosote, coke tar related sources, vehicular emissions were accounted for 21%, 13%, 16%, 23% and 21%, respectively (Wang et al., 2013). Such type of soil PAHs pose a great risk to human health and potable groundwater when they are subjected to leaching from soil.
Depending on the environmental pollution, the amount of PAHs in atmospheric air is in between 5 – 200,000 ng/m3 (Cherng et al., 1996). Compare to specific occupational exposures, environmental air levels of petroleum hydrocarbons are lower. It has been reported that the concentrations of priority PAHs in the ambient air in rural areas and urban areas were found to 0.02-1.2 and 0.15-19.3 ng/m3 strongly suggest that the industrialization has strongest impact in liberating huge amounts of petroleum hydrocarbons into environment. If we look at the statistics of cigarettes consumption and the yield of PAHs, smoke comes from one cigarette is an equivalent to 20-40 ng benzo(a)pyrene.
Whereas one pack of unfiltered and filtered cigarettes per day can yield up to 0.7 and 0.4 µg/day benzo(a)pyrene exposure, respectively. Interestingly, smoke emitted from a burning cigarette between puffs (called side-stream smoke) contains higher PAHs and other cytotoxic substances than smoke exhaled from a smoker (called mainstream smoke) (Jinot and Bayard, 1996). Recent investigation suggesting that areas of refining, basic chemical factories, and wastewater treatment settings are the good source for the emission of VOCs into the environment. Nearly 60 different VOCs have been detected in the air samples collected from Pearl River Delta region in china, and health risks to workers from VOCs were assessed by using US Environmental Protection Agency (US EPA) and American Conference of Governmental Industrial Hygienists (ACGIH) methods (Zhang et al., 2018).
Mostly these VOCs were belonging to C5-C6 alkanes, confirmed by gas chromatography-mass spectrometry/flame ionization detection (GS-MS/FID). Results confirmed that there is a high risk of cancer threat to workers in these areas since the total occupational exposure risks in these areas is > 1. Surprisingly, a new exposure route to petrogenic compounds in indigenous people living in the Peruvian Amazon has been identified recently (Orta-Martinez et al., 2018). Indigenous peoples’ diet in this region mainly depend on the four wild species namely collared peccary (Pecari tajacu), lowland tapir (Tapirus terrestris), paca (Cuniculus paca), and red-brocket deer (Mazama americana), which consume oil-contaminated soils and water. This pose grate threat and could be a route of exposure to petrocarbons for people living in the vicinity of oil drilling areas and relying on subsistence hunting.
Routes of entry
Ingestion, inhalation and dermal contact are the main routes of exposure in both occupational and non-occupational environment. There is more threat in occupational workers due to existence of even more exposure routes, such as breathing exhaust fumes is a very common route for the entry of petroleum hydrocarbons into the body of mechanics, street vendors, motor vehicle drives, mining workers, and workers of metallurgical and oil refineries. In certain incidences, people may expose to petroleum hydrocarbons by more than one route at a time, which enhances the total absorbed dose of petroleum hydrocarbons. Whereas diet, smoking, and burning of coal and wood are the major exposure routes at non-workplace environments.
During the inhalation, certain petroleum hydrocarbons odor provides adequate warning of hazardous concentrations, for example, odor threshold of gasoline is 0.025 ppm. It is also fundamental to note that lung surface area: body weight ratios are important, and which do decide the amount of petroleum hydrocarbon enters the body. For this reason, compare to children, adults may receive larger doses of gasoline vapors when both are exposed to same levels of gasoline vapor, because adults have greater ratios of lung surface area:body weight and minute volumes:weight than the children.
Generally, occupational exposure may occur within petrochemical industry during manual filling or discharge operations, repair or service of diesel engines, or sometimes from practices where diesel is used as a solvent or cleaning agent. Whereas domestic exposure to petroleum hydrocarbons is uncommon. But limited skin exposure is possible during refueling domestic vehicles. The other possible way for the domestic exposure is pulmonary exposure from aspiration of liquid during manual siphoning. It is also possible for the liberation of micrometer-sized, respirable aerosols of diesel particles due to leakage of diesel onto hot engine manifolds.
As a first aid therapy in dermal exposure to petroleum hydrocarbons, person must be removed from the exposure, and there should be subsequent removal of all soiled clothing. By using soap or water, contaminated area must be thoroughly washed, followed by symptomatic treatment. In case of ocular exposure, after removing the contact lenses, irrigate the affected eyes thoroughly either with water or 0.9% saline solution for at least 10-15 min. In case of inhalation, patient must be given oxygen, and maintain a clear airway and adequate ventilation. If the route of exposure is by ingestion, gastric aspiration should be considered within 1 h of ingestion. If small amounts of petroleum hydrocarbons are ingested, usually there will be no signs of aspirations.
Thus, TPHs can easily enter the human body during breath, swallow (water, food, soil) or touch the contaminated objects. Once TPHs enter the body, most fractions of TPHs will enter the bloodstream rapidly, then they will be circulated whole body and may be subjected to breakdown into more harmful products. But other TPHs are distributed slowly in the blood and not readily broken down into toxic metabolites. The above scenarios can be expected when TPHs enter the body either by breathing or swallowing. On the other side, when a person touches TPHs compounds, the absorption of these compounds is significantly slow when compare to breath or swallow them. Also, it is important to note that TPH compounds leave the body through urine or breath out.
Effects of TPHs on human health
There are many factors affect the health effects from exposure to TPH, such as quality of TPH, duration of exposure, amount of TPH contacted. At the same time, one must consider that is there any co-exposure to other chemicals, age, sex, diet, family traits, lifestyle and state of health. All these together will determine toxic effects of TPHs enter the body. Until now, very little is known about the toxic effects of many TPHs in human. For example, breathing of 100 ppm of toluene containing air for several hours can cause mild symptoms like drowsiness, fatigue, headache, and nausea. But long-term exposure to toluene leads to more severe effects like permanent damage to central nervous system (CNS) can occur.
The mode of action of n-hexane on CNS is different, and it causes nerve disorder called “peripheral neuropathy” and is characterized by numbness in the feet and legs. But under severe conditions, n-hexane causes paralysis. Swallowing of gasoline and kerosene can induce throat and stomach irritation, depression of CNS, difficulty in breathing, pneumonia is possible when breathing liquid enter lungs. Toxicity effects TPHs to blood, liver, spleen, kidneys, immune system, lungs and developing fetus are commonly encountered. Furthermore, carcinogenic TPHs have also been identified, for instance, benzene is known to cause leukemia in people. Vapors of gasoline are heavier than air, and inhalation of gasoline vapor may cause asphyxiation in areas of poorly ventilated (‘Toxic’, 2014). Generally, gasoline vapors cause mild irrigation to mucous membranes.
They also cause transient corneal injury if splashed in the eyes. When liquid gasoline contact with skin repeatedly and for a long time, it results in the skin reduction, irritation and dermatitis. Within several hours of contact, liquid gasoline can cause first- and second-degree skin burns, but percutaneous absorption is very slow. Like from the respiratory tract, gasoline is not readily absorbed from the gastrointestinal tract too. A less than one-half ounce (10-15 g) of gasoline is fatal in children, but 12 ounces (350 g) of gasoline can cause death in an individual of 70 kg. But little dose of gasoline i.e. 20-50 g can cause severe intoxication, which results in several symptoms due to involvement of multiple organs. If a person is subjected to acute gasoline exposure, initially it can cause transient CNS (central nerve system) excitation and leads to CNS depression. Further consequences are blurred vision, confusion, dizziness, giddiness, headache, nausea, and weakness.
If a person is exposed to massive doses of gasoline, it causes rapid CNS and respiratory depression, coma, loss of consciousness, seizures, and death may also be possible. Nevertheless, acute CNS depression induced by hydrocarbons is generally reversible after exposure ceases. But the chances of reversibility are highly limited if episodes are complicated by lack of oxygen. Soil contamination with oil spills in Niger Delta region, Nigeria has become widespread and assumed international concern. People of some areas (e.g. Ogale Eleme, Ogoni) are drinking water which was found to contain benzene with 900 times higher than WHO permissible limits. In 1998, an outbreak due to Jesse pipeline spill fire in the same region claimed nearly 1000 deaths including children and woman. Still there are many serious publish health issues are witnessed in this region including birth defects, cancer, various illnesses and deaths. People living nearby petrochemical industrial complexes (PIC) experience nearly 1.03-fold higher risk of lung cancer mortality than people living away from PIC areas (Lin et al., 2017).
Chromosomal defects in human are also possible due to exposure to hydrocarbons. There many factors affect the effects of petroleum hydrocarbons on human health, such as length and route of exposure, the amount or concentration, and the course of innate toxicity of the compound, besides other factors like pre-existing health status and age. In fact, short-effects in human induced by PAHs is yet to be studied. General acute health effects of pollutant mixtures containing PAHs during occupational exposures including confusion, diarrhea, eye irritation, nausea and vomiting. But still we lack component or fraction wise effects, because persons exposed to PAHs with other compounds also exhibit similar symptoms. Skin irritation and inflammation are common effects caused by the mixtures of PAHs. Recent studies (Kim et al., 2013a) suggesting that the anthracene, BaP, and naphthalene are direct skin irritants; where first two compounds are generally known as skin sanitizers. On the other side, long-term exposure to PAHs can cause certain chronic effects such as asthma-like symptoms, breathing problems, cataracts, decreased immunity, abnormalities in lung functions.
Sometimes jaundice may be caused due to kidney and liver damage. Redness and skin inflammation are the common effects during repeated skin contacts with PAHs. Especially, inhaled or ingested naphthalene in large amounts can frequently cause the breakdown of red blood cells. During the cleaning operations at the spill site, there is an increased risk of hypertension, which is a primary risk factor for coronary heart disease (CHD) (Yusuf et al., 2004), due to workplace stressors (i.e. noise) and simultaneous exposure to volatile organic chemicals (VOCs). Discharge of oil and gas (O&G) wastewaters on road can also contribute to chronic respiratory and cardiovascular disease (Tasker et al., 2018).
In thirteen states, US government has allowed the spreading of O&G wastewaters on roads as a viable and cheap option for the suppression of dust, however, this could be a potential human and environmental consequence. Therefore, human exposures may include a wide array of petrocarbons such as a complex mixture of particulate matter (PM), PAHs, and VOCs depending on the nature, location and timing of work being performed. Human toxicity point of view, particulate matter is an important form of petrochemicals which has significant impact on cardiovascular system. Even individuals are exposed to PM for a short time, may increase risk of cardiovascular disorders and mortality. Especially, during the cleanup activities, the levels of PM are elevated in coastal communities and around the cleanup sites.
The worst oil-related environmental disaster on the planet can be seen in Ecuadorian Amazon rainforest (‘Human’, n.d.). Forty years of oil operations in this region lead to severe crisis of water pollution. Root cause for this mess is Texaco (now Chevron) oil company dumped ~ 18 billion gallons of toxic wastewater and million gallons of crude oil into local rivers, which caused Chevron to face possibly $ 27 billion-dollar damages claim. This environmental catastrophe is called by experts as “Chernobyl in the Amazon”. This surface water is a major source for the daily activities (e.g. drinking, cooking, bathing and fishing) of thousands of indigenous people.
Oil-contaminated-water related exposures in indigenous people resulted in cancer epidemics, miscarriages, birth defects, and other sicknesses. Number of different cancer incidences (e.g. mouth, stomach and uterine cancer) have been elevated in areas where there is high prevalence of oil pollution, unofficially total cancer deaths 1400 excess (‘Chevron’s’, n.d.). There are severe birth defects in children who born to mothers exposed to oil-contaminated water. Skin rashes, and diarrhea are very common reports in the people who bath in contaminated rivers, and drink the water, respectively. Below are the emotions of affected individuals in their own words (‘Chevron’s’, n.d.) as they are the primary victims of this massive calamity occurred in Ecuadorian amazon rainforest due to nontechnical and noxious oil operations:
“We lived in a house about 20 yards away from an oil well. Another Texaco oil well was upstream from where we got our drinking water, and the water was usually oily with a yellowish foam. I had 11 children. I lost Pedro when he was 19. He had three cancerous tumors: in his lungs, liver, and his leg.” – Woman from town of Sacha, Orellana, Ecuador.
“It started with a little sore on my toe, which grew a bit larger. The water near my house, where I washed clothes, was full of crude and the sore grew bigger, as if the flesh were rotting. It didn’t hurt, but I couldn’t stand its stink. I had a fever and chills.” – Woman whose leg was surgically excised due to cancer.
“The girl is 15, she’s very sick. She was born that way, not moving with soft bones. The doctors were never able to tell me what was wrong with her. Now she can sit up, crawl, pull herself along the floor, turn over. She says “mama”, “papa”, and cries when she’s hungry or thirsty….I have to feed her by hand.” – Mother whose daughter has birth defects.
In a nutshell, oil spills may occur all around us, have potential to soils, sediment and water (both surface and groundwaters) and air. Subsequently, spill oils have significant negative impacts on the residents of the affected areas either by direct or indirect way depending on the type of contact with the oil spill. Prevailing weather conditions will play key role in influencing the physical characteristics and behavior of spilled oil at the site.
Effects on mental health
Mental health in cleanup workers and residents who exposed to oil is significantly affected. Studies conducted after massive oil spills (such as Exxon Valdez accident, Sea Express and Prestige spills) revealed that there is high prevalence of anxiety disorder, depression, posttraumatic stress disorder, psychological stress in oil-exposed population. Individuals living closer to the spill sites showed increased frequency of psychopathological symptoms like anxiety, hostility, and somatization, with lower perception of physical health and functional capacity (Palinkas et al., 1993). After the Prestige oil spill, though there were no general effects in the preschool children, but primary school aged children showed higher hostility to others after oil spill, suggesting that the ‘problem of social adjustment’ was clearly appearing in the oil-exposed individuals (Perez-Pereira et al., 2012).
The academic scores in adolescent group were dramatically dropped after Prestige oil spill. Higher risks of stress and depression, but no signs of suicidal impulse were observed in the residents exposed to Hebei Sprit spill. However, the scenarios were different in a larger group of residents of coastal communities at Hebei Spirit spill, where people showed wide array of mental disorders including anxiety, depression, posttraumatic stress disorder, suicidal thoughts, which is attributed to their exposure level and/or proximity to the spill site. It has also been found that mental health effects, especially anxiety and depression were higher in residents living closer to heavy and moderately oil-soaked areas than in residents from lightly oil-soaked areas.
Also, increased levels of depression have been observed in children living closest distance to contaminated coastline compared to children living farthest distance. In order to know the impact of pollution effect on mental health in human, a factor or scale has been introduced called ‘burden of disease’ (BOD) (Kim et al., 2013b), which helps to measure the health damage and useful for the assessment of compensation cost. Data analysis in contaminated sites revels that BOD remains for 1 year for the people exposed to oil and residing near contaminated coastal areas. However, BOD is known to be affected by several parameters, such as proximity to the spill site, participation in the cleanup activities, posttraumatic stress disorder, asthma etc.
After Deepwater Horizon oil spill also, oil-exposed individuals were found to show increased symptoms of anxiety, depression, and posttraumatic stress. Especially, the risk was higher in individuals with low income, low social support, and high levels of nonorganizational religiosity. In Gulf Coast, more than one-third children exposed to oil experienced either mental health distress or physical symptoms. Economic problems are the additional contributors to the mental health disorders in oil exposed individuals. Worse scores of anxieties, confusion, depression, fatigue, total mood disturbance scales, less resilience were observed in people with spill-related income loss than those with stable income.
A questionnaire was conducted in the Gulf Coast area after an oil spill, which revealed that though emotional and psychological symptoms were declining and more individuals were started to work, families were still experiencing severe chronic stressors and disruption. Such metal disorders in the family is attributed to job loss and changes in the economic conditions. Thus, there is abundant evidence to establish the relationship between oil spills and mental health effects in exposed individuals.
Effects on respiratory system
About the respiratory tract, gasoline can irritate the mucous membranes. But in the case of severe exposures, extensive damage in respiratory tract is possible by gasoline, such as acute exudative tracheobronchitis, edema, intrapulmonary hemorrhage, pulmonary congestion etc. Pneumonitis is possible from the pulmonary aspiration of ingested gasoline. The vapors of petroleum hydrocarbons (e.g. gasoline) can sensitize the myocardium to circulating epinephrine, which may result in the potentially fatal ventricular fibrillation. There is a high possibility for fatty degeneration of the proximal convoluted tubules and glomeruli, and renal failure if massive amounts of petroleum hydrocarbons are inhaled.
Persistent respiratory symptoms with elevated of airway injury in breath condensate has been found in cleanup workers 2 years after Prestige oil spill. But even after 5 years also, Prestige oil spill affected individuals were found to show increased risk of lower-respiratory-track symptoms including cough, phlegm, shortness of breath, wheeze etc., which suggest that the respiratory symptoms may persist up to several years (~ 5 y) after exposure. In individuals exposed to the Tasman Spirit oil spill have suffered higher rate of health effects such as cough, eye irritation/redness, general illness, head-ache, nausea, runny nose, sore throat etc. But effects were even worse in persons exposed to oil for 15 days at the Tasman Spirit oil spill site, mainly there was lung dysfunctions with significant reductions in the spirometry parameters.
On the other hand, several volatile organic compounds (VOCs) such as benzene, ethylbenzene, xylene, and PAHs are known to induce respiratory tract irritation, bronchitis and irritation to skin. Especially, PAHs with 3 to 5 benzene rings have potential to induce oxidative stress in the respiratory tract and aggravate asthma symptoms. Multiple diagnostic and clinical tests (e.g. skin prick test, methacholine bronchial provocation test, pulmonary function test) have confirmed that the children exposed to crude oil spill will increase the risk of asthma. VOCs, especially aromatic compounds are associated with adverse respiratory effects like asthma in adults. Nevertheless, respiratory hospitalizations, nocturnal cough, pleural mesothelioma, obstructive lung disease etc., are very common effects in individuals exposed to oil spill. In one study, transcriptomics has been used to reveal the potential effects of oil and oil dispersants on the respiratory system at molecular level.
Human airway epithelial cells were grown by exposing them to crude oil, dispersants (Corexit 9500 and Corexit 9527), and oil-dispersant mixtures (Liu et al., 2016). Corexit 9500 had shown drastic changes in the expression of ~ 84 response genes. According to gene ontology functional term and pathway-based analysis, gene sets related to angiogenesis and immune responses were upregulated, and gene sets involved in cell junctions and steroid synthesis were downregulated. Such effects were observed in cells treated with Corexit 9500, oil or Corexit 9500 + oil mixture. Nevertheless, key molecular signatures identified in this study have been well coincide with pathological features observed in common lung diseases, including asthma, cystic fibrosis, and chronic obstructive pulmonary diseases, which suggest that crude oil and dispersants have an immense effect on respiratory system.
Sometimes, as a part of cleanup procedures, spilled sites are treated by “in situ burning” of trapped oil on the surface of water columns. However, this generates potentially toxic substance called oil sail particulate matter (OSPM) (Jaligama et al., 2015). In experimental mouse, OSPM caused cytotoxicity in a dose- and time-dependent manner, concurrently results in the generation of reactive oxygen species, and superoxide radicles. OSMP exposed mice have shown decreased body weight gain, systemic oxidative stress, airway inflammation. Additionally, OSPM was found to be as a key element in increasing the number of T helper 2 cells (Th2), peribronchiolar inflammation, increased airway mucus production in a mouse model of allergic asthma.
These findings clearly demonstrate that OSPM has potential to cause pulmonary inflammation and alters the innate/adaptive immune responses in experimental animals and suggest the threat to respiratory system from cleaning up an oil spill by “in situ burning”. In sub-Saharan Africa, ambient air pollutants have been assessed for their toxicity effects on respiratory system in schoolchildren living in a city (Durban, South Africa) where there is intense activities concerning importation of crude oil and exportation of petroleum and petroleum products (Mentz et al., 2018). As anticipated, increased occurrence of respiratory symptoms among the schoolchildren were identified, with the evidence of chest tightness, cough, shortness of breath etc.
Effects on hematopoietic, renal and digestive systems
Hematologic system in human is also known to be affected by TPHs. Incidences of nonlymphocytic leukemia, acute lymphocytic leukemia, chronic myelocytic leukemia, and chronic lymphocytic leukemia are higher in individuals exposed to oil than unexposed individuals. In DWH oil spill victims, decreased blood parameters have been observed, such as white blood cells and platelet counts, blood urea nitrogen, creatinine, hemoglobin, hematocrit, and urinary phenol levels (D’Andrea and Reddy, 2014). In contrast, mean hemoglobin and hematocrit levels were significantly increased in people exposed to oil compared with the unexposed individuals. Furthermore, in spill affected individuals, high levels of serum liver enzymes such as alkaline phosphatase, aspartate amino transferase, and alanine amino transferase were observed.
After Prestige oil spill, elevated levels of two heavy metals (e.g. aluminum and nickel) were detected in the blood samples of exposed humans. Incidences of childhood leukemias were positively correlated with in the children living closer to oilfields in Ecuadorian Amazon (Hurtig and San Sebastian, 2004). Ninety-one cancer cases have been recognized in age group of 0-14 years, with significantly elevated levels in the youngest age group of 0-4 years, with a relative risk of leukemia ranging from 2.56 to 3.48. The most toxicological VOCs of petroleum hydrocarbons e.g. benzene, toluene, xylene and PAHs. In these, benzene is a well-known cause of leukemia and other hematologic neoplasms. Nevertheless, studies conducted in US and China also revealed that there are high incidences of leukemia cases in oil-field workers (Yang and Zhang, 1991; Sathiakumar et al., 1995).
The incidences of several kinds of leukemia (e.g. acute nonlymphocytic leukemia, acute lymphocytic leukemia, chronic myelocytic leukemia, chronic lymphocytic leukemia etc.) were significantly were higher in people living in oil fields and polluted areas that those in other areas (Yang and Zhang, 1991). In the renal system, many disorders are caused by the ingestion of gasoline, including elevated levels of serum creatinine, urinary protein, glucose, hemoglobin, and BUN. The other frequently observed symptoms are oliguria, tubular necrosis, interstitial edema, hematuria, and reduced creatinine clearance.
In general, acute renal toxicity resolves with treatment. Ingestion of petroleum hydrocarbons causes severe damage to the digestive tract such as esophagitis, gastritis, disruption of epithelium and mucositis of the oral cavity. Vapors of petroleum hydrocarbons such as gasoline can cause skin inflammation. Irritant contact dermatitis, degreasing, burns, redness and blisters are common during prolonged contact with liquid petroleum hydrocarbons. Vapors of petrocarbons induce eye irritation, which starts from a concentration of 200 ppm. Burning pain and transient corneal injury are possible when petroleum hydrocarbons splashed in the eyes. But chronic exposure to these compounds leads to sever damage to cornea, retina, and ciliary body.
Carcinogenicity and genotoxic effects
Regarding of the carcinogenicity, PAHs in surface polluted-soils cause cancer in humans through multiple exposure pathways such as ingestion, dermal contact and inhalation. High molecular weight PAHs are easily bioaccumulated in the tissues. The principal reason for the carcinogenicity, malformation, and gene mutation is PAHs have lipophilic nature, therefore, they are easily dissolved and transported to cell membranes (Franco et al., 2008). There is also potential risk from the metabolized PAHs, such as epoxides and dihydrodiols, which have greater ability to bind to cellular proteins and DNA. Covalent binding of diol-epoxides with DNA is essential for carcinogenic effect. Mutations, developmental malformations, tumors and cancer are the consequences of biochemical disruption and cell damage caused by the reactivity of reactive metabolites and vital cell components. Experiments with animal models have provided more insights about the PAHs and their role in cancer.
Prolonged exposure of animals to high levels of certain PAHs caused cancers of lung, stomach, and skin through inhalation, ingestion of PAHs in food, and skin contact respectively. BaP (benzo(a)pyrene) was found to be as a first chemical carcinogen, which is the most common PAH to be a carcinogenic in animals. Seven PAH compounds namely benz(a)anthracene, BaP, benzo(b)fluoranthene, benzo(k)fluoranthene, chrysene, dibenz(ah)anthracene, and indeno(1,2,3-cd)pyrene have been classified as a probable human carcinogens by the EPA (environmental protection agency). The most important group of enzymes that are involved in the metabolism of PAHs are cytochrome P450 enzyme CYP 1A1, 1A2, 1B1, and 3A4.
DNA adducts are witnessed in several tissues upon exposure to PAHs. PAH-DNA adducts have been positively correlated with the level of PAH exposure, such as persons exposed to coke oven emissions, or cigarette smokers. Generally, DNA adducts are eliminated from the genome by a refined repair system, similarly PAH-DNA adducts are also excised. Permanent mutations are caused if the DNA adducts are left unrepaired. Depending on the locations of mutations in the genes (e.g. tumor suppressor genes or oncogenes), cellular transformation and tumor development is possible. For instance, smoking associated mutations are resulted from the preferential binding of PAHs in cigarette smoke to Tp53 gene (Abedin et al., 2013). The mode of action of BaP as a carcinogen in experimental animals has been well documented. When BaP is administered locally into experimental anima, it forms (7R,8S)-epoxy-7,8-dihydrobenzo(a)pyrene (B(a)P-7,8-oxide) by the action of cytochrome P450 enzyme.
Later this metabolite is converted to (7R,8R)-dihydroxy-7,8dihydrobenzo(a)pyrene (B (a)P-7,8-diol) by epoxide hydrolase. Finally, again by the action of cytochrome P450 enzyme, there is a formation of BPDE ((7R,8S)-dihydroxy-(9S,10R)-epoxy-7,8,9,10-tetrahydrobenzo(a) pyrene), which is an ultimate carcinogen. There is a formation of large amounts of BPDE-DNA adducts due to the specific biding of DPDE to DNA at guanine residues. There is an induction of cytochrome P4501A1 (CYP1A1) by the binding of BaP to the aryl hydrocarbon receptor in the cytosol, then the transformed receptor enters the nucleus and is further modified by dimerization with aryl hydrocarbon receptor nuclear translocator. These dimers have potential to bind at specific sites (e.g. xenobiotic response elements) in the promoter regions of certain genes.
Ultimately which leads to increased transcription of CYP1A1 gene with increased production of CYP1A1 protein. PAHs have also been found to show increased risk for breast cancer through the investigations on animals. DMBA (7,12-Dimethylbenz(a)anthracene), a kind of PAH, is commonly found in environment (e.g. diesel exhaust, barbequed meat, tobacco smoke, overheated cooking oil etc. Being a fat-soluble compound, DMBA is likely to accumulate in the adipose tissue of mammary gland, and thus causes breast cancer. CYP enzymes are responsible for the transformation of DMBA to carcinogenic form i.e. DMBA-3-4-epoxide. This epoxide is converted to DMB-3,4 diol by epoxide hydrolase. Finally, diol form is oxidized to ultimate carcinogen i.e. DMBA-3,4-diol-1,2-epoxide by CYP enzyme. In this form, DMBA can interact with DNA and produce adducts which are responsible for its mutagenicity and carcinogenicity.
There are several convincing examples for the genotoxic effects in human exposed to spilled oils. Two years after the accident of Prestige oil spill, affected human has shown severe genotoxicity in the form of structural chromosomal alterations, primarily chromosomal imbalances (e.g. acentric fragments, deletions, markers, translocations etc.), and impaired DNA repair mechanism (Rodríguez-Trigo et al., 2010). Even after two years of oil spill and with extensive cleanup, sediment materials have shown genotoxicity and alteration of steroidogenesis in chicken DT40 cells and H295R cells, respectively (Ji et al., 2011). Cytogenic analysis revealed the presence of three chromosomal bands with the outcome of hematological cancer in individuals experienced acute oil exposure. Breakages in the chromosomal bands leads to chromosomal instability, which increases the risk of certain cancer incidences such as leukemia and lymphomas.
The same has been reported in individuals having chronic benzene exposure. In order to confirm these results, laboratory experiments have been conducted with model animals under controlled conditions, where rodents have been subjected to subchronic exposure (by inhalation) to a fuel oil which is very similar to the oil spilled at Prestige tanker accident (Valdiglesias et al., 2012). Severe DNA damage and alterations in DNA repair responses have been observed in rats. However, there are no convincing evidence for the persistence of genotoxic damage in individuals exposed to oil spills. Nonetheless, crude oil contains several volatile organic compounds (e.g. benzene, ethylbenzene, toluene, xylene etc.) and PAHs, which are known to be as potential genotoxic endocrine disrupting agents (Ji et al., 2011).
According to International Agency for Research on Cancer (IARC) several VOCs and other petroleum hydrocarbons have been classified based on the carcinogenicity. For example, benzene belongs to Group 1 agent, which has proven its carcinogenicity in human. Toluene, ethylbenzene, and styrene have been classified under Group 2B, are considered as possible human carcinogens based on their carcinogenic history in animals. On the other hand, some PAHs compounds (e.g. benz[a]-anthracene, benzo[a]pyrene, and dibenz[a,h]anthracene) have been classified under Group 2A, and other PAHs (e.g. naphthalene, benzo[b]fluoranthene, benzo[j]fluoranthene, and benzo[k]fluoranthene) have been considered as Group 2B.
On the other hand, teratogenic effects of PAHs have also been studied by exposing experimental animals to different PAHs during the pregnancy stage (Ng et al., 2009). These studies indicated that exposure to high levels of BaP has caused significant embryotoxic effects with birth defects and decreased body weight in the offspring. But there are no evidence or reports of similar symptoms in human yet. CCEH (Center for Children’s Environmental Health) reports suggesting that exposure to PAHs during pregnancy causes adverse birth outcomes such as heart malformations, low birth weight, and premature delivery. Nevertheless, high prenatal exposure to PAHs causes different effects at different age levels, such as low IQ at age three, increased behavioral problems at ages six and eight, and even there is a possibility for childhood asthma.
On the other hand, benzene shows transplacental transfer and may harm a developing fetus (Goldstein et al., 2011). Chromosomal aberrations (i.e. direct damage to DNA) is also possible in oil exposed individuals. Due to exposure to petrochemicals, increased rates of spontaneous abortions (SAB) were observed in the pregnant woman working in the laboratories of petrochemical plant (Merhi, 2010). SAB rate has been increased approximately by 8.8% in pregnant woman exposed to petrochemicals such as benzene, gasoline, and hydrogen sulfide. Similarly, high prevalence of toxemia, SAB and prematurity were observed in the woman living in the areas polluted by petrochemical industries in Bulgaria. In oil exposed men, several abnormal characteristics were found in their semen, such as changes in viscosity, liquefaction capacity, sperm count and motility, and increased normozoospermia (De Celis et al., 2000). Such altered sperm characteristics will increase the delayed conception and congenital malformation.
Immunotoxicity and endocrine toxicity
PAHs are also known to induce immunotoxicity in experimental animals like rodents, however, precise mechanism of immunotoxicity of PAHs is uncleared. In most investigations it was found that the immunotoxic effects are systemic, which is independent of route of exposure. Upon exposure to PAHs, immune suppression is the major the major observable effect. Other disorders of immune system associated with PAHs exposure include immune potentiation, tumor development, expression of hypersensitivity, auto immunity etc. The major obstacle in understanding the effects of PAHs on immune system is that there is an ambiguity between literature and experimental results.
Most literature has cited that subcutaneous, intra-peritoneal injection and inhalation are the main routes of exposure. On the other hand, most experimental studies have been conducted using oral route by the ingestion of PAH-contaminated food. Experiments with cell lines of animals and mammalians (including human) revealed that the metabolites (e.g. diol epoxides) of some PAHs have potential to induce genotoxic effects by reacting with DNA. Such type of genotoxicities is crucial in the further development of carcinogenic and/or developmental toxic effects. In Prestige oil spill exposed individuals, decreased levels of endocrine hormones (e.g. cortisol and prolactin) were observed, which are the good indicators of psychophysiological stress.
Oil spill effects are even worse on immune system of an individuals who have been exposed to same spill site for longer periods (several months), with significant modifications in lymphocyte subpopulations and concentrations of plasma cytokines. Even after 7 years of Prestige accident, symptoms of impaired immune and endocrine systems have been observed in oil-exposed individuals. Workers those involved in the manual cleanup of Prestige oil for 3 months have showed altered immune system with decreased % of CD3+ and CD4+ lymphocytes, and increased % of CD8+ cells together with IL2, IL4, IL10 and IFNγ plasma concentrations.