Short-term effects of subchronic low-level hydrogen sulfide exposure on oil field workers

Abstract

Objectives

To investigate the short-term effects of low-level hydrogen sulfide (H₂S) exposure on oil field workers.

Materials and methods

Observational study included 34 patients who work at an oil field. All patients were males with age range of 22–60 years (mean 37 years). The data were collected by systematic questionnaire about symptoms. The inclusion criteria of patients were symptoms related to inhalation of H₂S gas in the oil field. The complaints should be frequent and relapsed after each gas exposure and disappeared when there was no gas exposure. Exclusion criteria were the symptoms which experienced with or without H₂S exposure. The presence of H₂S gas was confirmed by valid gas detector devices.

Results

The most frequent presenting symptom was nasal bleeding. It was revealed in 18 patients (52.9 %). This followed by pharyngeal bleeding, gum bleeding, and bloody saliva (mouth bleeding) which were encountered in five cases for each complaint (14.7 %). Other less frequent presenting symptoms were tongue bleeding, bloody sputum, headache, abdominal colic, pharyngeal soreness, fatigue, and sleepiness.

Conclusions

Nasal mucosa was the most vulnerable part to H₂S effect. Inhalation of H₂S produced upper respiratory tract epithelial damage that led to bleeding from nose, pharynx, gum, tongue, trachea, and bronchi. There were no complaints of asthmatic attack upon exposure to low level of H₂S. Sunlight had a significant role in reduction of ambient air H₂S level.

Introduction

Hydrogen sulfide (H₂S) is a toxic gas with a characteristic rotten egg odor. It is a by-product of numerous industrial processes, including sewage treatment, pulp and paper processing, petroleum and natural gas drilling and refining operations, and rayon textile manufacturing.

Human exposure to the toxic effects of H₂S is characteristically dose related and most notably involves the nervous, cardiovascular, and respiratory systems [1]. It was reported that exposure to higher H₂S concentration caused severe neurotoxicity, status epilepticus, bronchospasms, and delayed respiratory failure [2]. Following inhalation, H₂S dissociates into free sulfide and hydrogen ions in the blood circulation. Sulfide binds to many macromolecules, including cytochrome oxidase thereby preventing oxidative phosphorylation. This causes reversible inhibition of aerobic metabolism leading to cellular anoxia [3]. Olfactory deficits (hyposmia) with both a delayed and immediate onset have also been documented following repeated exposures to sublethal doses of H₂S in workers at a refinery construction site [4]. H₂S odor was strongly associated with reports of alteration of daily activities, negative mood states, mucosal irritation, and upper respiratory symptoms [5]. It was also concluded by experiment on rats that inhalation of H₂S had a severe cytotoxic effect on the nasal epithelium and a severe edematogenic effect on lung parenchyma [6] whereas acute exposure to 400 ppm H₂S induced severe mitochondrial swelling in support cells and olfactory neurons, which progressed to olfactory epithelial necrosis and sloughing [7]. On the other hand, subchronic exposure of rats to 30 or 80 ppm H₂S results in olfactory neuron loss and basal cell hyperplasia [1]. The lethal effect of acute exposure to H₂S is at persistent high concentrations (>500 ppm) [8]. Acute exposure to H₂S causes four dose-dependent human responses: hyperpnea, unconsciousness, apnea, and death [9]. Acute exposure to 50–100 ppm H₂S leads to neurological disorders (dizziness, headaches, loss of balance, lack of concentration, recent and long-term memory loss, mood unstableness, irritability, exhilaration, and sleep disturbances), behavior changes (anger, depression, tension, confusion, fatigue, and vigor), respiratory symptoms (apnea, cough, noncardiogenic pulmonary edema, and cyanosis), cardiovascular abnormalities (irregular heart beat or hypotension), eye irritations (conjunctivitis, lacrimation, and photophobia), skin symptoms (itching, dryness, and redness), and general deficits (nausea, libido decrease, gastrointestinal tract upsets, and loss of appetite) [10].

It is well known that acute exposure to high concentration of H₂S has immediate toxic or lethal sequelae whereas chronic exposure to lower concentration leads to different types of illnesses. There were few human or animal studies in regard to short-term subchronic health disorders of low H₂S level especially on the upper respiratory airways. Effect of sunlight on the ambient air H₂S level was also considered in the present study. The aim of the present study is to investigate the short-term effects of low-level H₂S exposure on oil field workers.

Patients and methods

An observational study was conducted including 34 patients who attended oil field clinic at Oil Company. They were complaining from symptoms related to H₂S exposure. The study was carried out between February 2012 and December 2013. It was exempted from ethical approval. The patients were oil field employee. Their ages were 22–60 years (mean 37 years). All were males. The study was performed at four oil field camps. One oil field was exposed to intermittent, fluctuating low concentration of H₂S in which workers regarded as case study group, whereas the other three oil fields were exposed to little or no H₂S gas in which workers regarded as control group. About 400–800 workers were available at each oil field. Their duties were administrative, maintenance, oil station operators, engineering, drilling, and service sectors. Oil-separation station (the units which separate crude oil from water) operators were the most likely people vulnerable to highest level of H₂S (up to 50 ppm). In the field with high H₂S level, the natural consistency of the crude oil contains high concentration of H₂S where the camp was built in between oil wells and oil-separation stations. All cases were reported in the field with high H₂S level. In the other three oil fields, there were no complaints related to gas effects. H₂S concentration was measured in the oil fields at several sites (oil-separation stations, workshops, living accommodation, and remote working areas with suspected high H₂S level). The H₂S gas was measured by fixed gas detectors, which are continuous monitoring devices, from which daily peak concentrations were recorded. Portable gas detectors were also used especially for tasks at remote areas. Dräger gas detectors were employed in the oil fields. Dräger portable gas detectors can be used to detect and measure more than 400 gases including combustible gases or vapors, toxic gases and also monitoring for low oxygen levels. These gas detectors which can be used for personal monitoring, area monitoring, confined space entry clearance measurements and gas leak detection. All work places and living accommodation have alarming system to alert employee when the H₂S concentration approaches a dangerous level. The H₂S sources were extinguished gas flares, crude oil-separation stations, leaking oil wells, and waste water. The latter was separated from crude oil in the separation stations and dumped out into opened reservoirs in the desert.

The inclusion criteria of patients were complaints which were related to inhalation of H₂S in the oil field at their living accommodation or at work place. The included cases were exposed to subchronic 4–50 ppm H₂S for few hours to few days whereas complaints of acute exposure to high H₂S concentration for brief period or complaints of chronic exposure for several months or years were excluded. The data were collected from patients who were seeking medical treatment about symptoms resulting from H₂S exposure. Systematic questionnaires were used to differentiate between complaints which were related or unrelated to H₂S gas. The following question items were applied: Is your symptom experienced after H₂S gas exposure? Is it recurring on each gas exposure? Is it disappearing when there is no gas odor? Is it correlated with potency of gas odor? Do you experience same symptom or free of symptom at your home residency outside the oil field? Do you have the same symptom before you have been employed in the oil field? Therefore, the symptoms should be frequent and recur at least twice after each gas exposure and disappear when there is no gas exposure. Exclusion criteria were whenever same symptoms experienced while the patient at home (outside oil field) or at work site. However, two patients whose symptoms were experienced at home, but exaggerated at work place after H₂S exposure were included. Specific symptoms of certain illnesses which were unrelated to gas inhalation were also excluded. These involved upper respiratory acute or chronic illnesses such as flu, pneumonia, chronic gum disease, bronchiectasis, or chronic obstructive airway disease.

There were 168 patients excluded from the study because their symptoms did not coincide with study criteria. Although they believed that their symptoms were related to H₂S inhalation. Most notably, the encountered symptoms were headache, eyes irritation, throat irritation, nasal blockage, weight loss, reduce sense of smell, sleep disturbances and sudden wake up with chest tightness, and difficulty of breathing for brief period. Reduced sense of smell might be the effect of chronic H₂S exposure which is outside the scope of the present study. It is worth to mention that most of oil field workers who complained from gas effects did not consult a physician because they used to experience the symptoms for long time. On the other hand, many people might not get symptoms from such exposure which could be explained by their native resistant to H₂S effects.

Results

Thirty-four patients were investigated whose symptoms were agreed with the inclusion criteria of the present study. Hydrogen sulfide was intermittently affecting oil field workers. In each time of gas spreading through the oil field camp, the duration of patients’ inhalation of H₂S usually ranged from 8 to 12 h and rarely for few days. However, the cycles of H₂S exposure were repeated irregularly on daily bases or within every few days. H₂S bouts were intermittent with fluctuating concentrations because it was related to natural factors such as wind direction or speed, ambient temperature (highest H₂S level during winter season/lesser UV light intensity), day or night time, location of the worker within the camp, extinguished or non-extinguished gas flares, level of ventilation, and quantity of gas emission from its sources. H₂S concentration was ranged from 4 to 50 ppm during the period of ambient gas existence whereas 0 ppm was recorded during gas absence and in the other three oil field locations. There was no other abnormal high concentration of poisonous gases detected other than H₂S. On daily bases monitoring, the highest H₂S level was observed at night especially before sunrise, while at midday it almost always disappeared except in places nearby its sources. The dominant range of H₂S level during the days of gas existence was 8–50 ppm before sunrise and 0–2 ppm at midday time. After sunrise, there was gradual reduction in level of H₂S. This might be the effect of sunlight (UV light) that dispenses or destroys the gas. The peak level (50 ppm) was recorded in the vicinity of oil-separation stations.

The symptoms of H₂S exposure were bleeding from nose, pharynx, gum, mouth, and tongue. Other patients also presented with bloody sputum, bloody saliva, headache, abdominal colic, pharyngeal soreness, fatigue, and sleepiness. The most common presenting complaint was nasal bleeding. It was observed in 18 patients (52.9 %), of which 14 cases (41.2 %) presented with nasal bleeding alone whereas four cases had additional symptoms related to H₂S exposure. This was followed by pharyngeal bleeding (five cases, 14.7 %), gum bleeding (five cases, 14.7 %), and bloody saliva which is unrecognized site of origin of mouth bleeding (five cases, 14.7 %) as shown in Table 1. All categories of bleeding were intermittent which observed after H₂S exposure. It was unassociated with pain or abnormal clinical features except those mentioned in Table 1, which included chronic sinusitis, nasal soreness, common cold, rhinitis, gingivitis, atrophic rhinitis, and acute bronchitis. The other less frequent symptoms were tongue bleeding, bloody sputum, headache, abdominal colic, pharyngeal soreness, fatigue, and sleepiness. The headache resulting from H₂S exposure was not responding to analgesics. Two patients had similar complaints at home and at oil field (pharyngeal bleeding and bloody saliva), though the symptoms were mild and less frequent at home than those experienced at the oil field. The features of bleeding resulting from H₂S were somewhat different from ordinary bleeding. It was usually rusty color, mixed homogenously with nasal discharge or with saliva or sputum. It was not flowing or dripping. The site of bleeding was diffuse and cannot pin point the site of origin on clinical examination. It was noticed by performing certain maneuver such as mouth gargle with water, expulsion of sputum, or nose blowing.

Table 1.

The symptoms and associated illnesses in 34 patients complaining from H₂S effects

Symptoms	No. of cases (%)	Associated illnesses (no.) and remarks
Nasal bleeding	14 (41.2)	Chronic sinusitis (1), nasal soreness (1), common cold (1), rhinitis (1)
Pharyngeal bleeding	5 (14.7)	Mild and less frequent bleeding at home (1)
Gum bleeding	3 (8.8)	Gingivitis (1)
Bloody saliva (mouth bleeding)	4 (11.8)	Mild and less frequent bleeding at home (1)
Tongue bleeding	1 (2.9)
Nasal and tongue bleeding	1 (2.9)	Atrophic rhinitis
Nasal bleeding and bloody sputum	1 (2.9)	Acute bronchitis and common cold
Gum bleeding and bloody saliva	1 (2.9)
Nasal and gum bleeding	1 (2.9)
Nasal bleeding, headache, and abdominal colic	1 (2.9)
Pharyngeal soreness	1 (2.9)	Complaining at oil field only
Headache, fatigue, and sleepiness	1 (2.9)	Complaining at oil field only

No serious H₂S poisoning (fatal cases, respiratory failure, or severe neurotoxicity) was reported because the H₂S was diffused on large surface area with low concentration. There were also no patients complained from bronchial asthmatic attack or exaggeration of bronchial asthma upon exposure to H₂S. All patients were given non-specific conservative treatment such as antibiotics, mouthwash, vitamin C, multivitamin, or normal saline nasal drops.

Discussion

The predominant complaint from short-term/low-concentration H₂S exposure in the present study was upper respiratory tract bleeding. The previous experimental studies on rats and human revealed a role of H₂S on the living cells. A study on experimental rats, H₂S inhalation was found to have a severe cytotoxic effect on the nasal epithelium [6] and olfactory epithelial necrosis and sloughing [7]. In human studies, H₂S was also found to have a dose-dependent intensification of cell death via apoptosis and necrosis [11]. The intracellular acidification of nasal epithelial cells by high-dose H₂S exposure and the inhibition of cytochrome oxidase at much lower H₂S concentrations suggest that changes in intracellular pH play a secondary role in H₂S-induced nasal injury [12]. Furthermore, physiological concentrations of H₂S could induce apoptosis of human periodontal ligament cells and human gingival fibroblasts in periodontitis, suggesting that H₂S may play an important role in periodontal tissue damage in periodontal diseases [13]. These findings suggest that H₂S causes upper respiratory tract epithelial damage that lead to bleeding from nose, pharynx, gum, tongue, trachea, and bronchi. The same mechanism may cause pharyngeal soreness, gingivitis, rhinitis, and eyes irritation. On chronic exposure, this also might cause gingival and periodontal disease among people who work in environment with presence of H₂S. Acute, subchronic, and prolong exposure to H₂S might also cause neuronal olfactory damage, loss of smell sensation, and rhinitis which was reported in previous studies on human, rats, and mice [4, 7, 14, 15]. At lower concentrations, H₂S was found to cause eye mucosal irritation, and keratoconjunctivitis called ‘gas eye’, and at higher concentrations there was risk of pulmonary edema [16]. There was evidence that chronic low-level exposure to H₂S might be associated with reduced lung function [17]. Lambert et al. (2006) reviewed several studies in regard to H₂S effect on eye. They concluded from some previous studies that acute H₂S exposure could produce eye irritation and toxic effects whereas with chronic exposure, serious eye effects were suggested [18]. Overproduction of endogenous H₂S was also found stimulating human aorta smooth muscle cells apoptosis [19]. An experimental study on mouse also revealed that the enzymes producing H₂S in lungs/H₂S system play a critical protective role in the development of asthma [20]. A recent study in New Zealand provided no evidence that asthma risk increases with H₂S exposure. Suggestions of a reduced risk in the higher exposure areas are consistent with recent evidence that H₂S has signaling functions in the body, including induction of smooth muscle relaxation and reduction of inflammation [21]. This coincide with the findings in the present study in which there were no reported cases of asthmatic attack or exaggeration of pre-existent bronchial asthma upon H₂S exposure. A study on rat revealed a specific effect of inhalation natural H₂S-containing gas on myelin sheaths in the brain, which determines its neurotoxicity even at low concentrations in the inspired air [22]. In human studies, it was concluded that neurophysiological abnormalities were associated with exposure to H₂S from crude oil among former workers and neighbors of a refinery [23]. Another study had investigated the cognitive functions among workers of sewer networks. It demonstrated that exposure to H₂S was associated with cognitive impairment [24]. However, in a community-based study on people with chronic exposure to H₂S, the investigators revealed that deficits in overall neurobehavioral performance were not associated with such exposure [25].

The present study showed that nasal mucosa was the most profound respiratory site affected by H₂S. This could be explained by fact that the nose is more vulnerable to the gas especially during sleep at night. It is the first part of respiratory passage for breathing process that exposed to the highest level of H₂S concentration. Thereafter H₂S might be reduced in concentration as it proceeds down into respiratory airways where the vast majority of H₂S is absorbed by nasal and sinuses mucosa. This finding is in concordance with that found in the animal studies in which they had shown that the nose was a particularly sensitive respiratory tract target for inhaled H₂S [26, 27]. The nasal cavity is lined with specialized epithelial cells that maintain the normal function of the nose. These surface epithelial cells have specific roles in conducting airflow and maintaining normal nasal function and include squamous, respiratory, transitional, and olfactory epithelium [28]. The vicinity of the respiratory and olfactory epithelial cells to inspired air makes them a target for cytotoxic damage [29]. Therefore, long-term exposure of low concentration of H₂S might cause loss of smell sensation.

The limitation of the present study is the small sample size because of the difficulty to confirm that H₂S was the culprit among several excluded cases. The study revealed subchronic H₂S effects on the upper respiratory system which had been rarely mentioned in the previous human studies. The prominent factor, which affects the health of oil field workers in regard to prolonged H₂S exposure, was the construction of the camp in the vicinity of oil wells and oil-separation stations. It is highly recommended to build workshops and living accommodation far away from these locations with especial emphasis on the dominant annual wind direction. The oil field camp should be constructed where the usual wind direction passes through camp first and then toward the oil wells and oil-separation stations. The waste water, which is separated from crude oil and expelled near the oil field camp, should be either injected into dead oil wells or throw far away from the camp. An advanced technological system could also reduce H₂S emission from its sources. In addition, automatic fire ignition devices for gas flares, which burn excess crude oil gas, should replace the old style manual fire ignition by pistol. The manual ignition was used at the oil fields during the period of the present study. These gas flares were extinguished spontaneously when there was reduction in pipe gas flow rate and/or high-speed wind. This led to high emission of H₂S whenever there was delay in manual ignition of the gas flares.

Reduction or disappearance of H₂S gas during midday period and summer season in the oil fields might be related to ultraviolet (UV) light destruction of the gas. This was confirmed experimentally in two previous studies. The photolysis was performed by applying UV light beam on H₂S gas inside pipe or container [30, 31]. The experiments revealed that UV light reduced H₂S concentration by photolysis or gas destruction. The level of H₂S photolysis was also related to several factors which included initial H₂S concentration, pipe diameter, ultraviolet light wavelength, relative humidity, and oxygen content. The highest activity for H₂S destruction was achieved with decreasing initial H₂S concentration, reduced pipe diameter, 80 % relative humidity, and 21 % oxygen content.

Conclusion

There was significant toxicant-induced damage of H₂S on the upper respiratory tract especially bleeding from several parts after subchronic exposure to low concentration of H₂S. Few animal or human studies have mentioned subchronic health disturbances of low H₂S level. Long-term effects need to be evaluated especially in regard to periodontal disease. There should be discrimination between the health effects of high H₂S toxic level and lower concentration exposures. Larger studies upon several populations who live near low ambient concentration of H₂S might show some detrimental effects of such exposure. Reduction of ambient air H₂S level by sunlight was confirmed in the present study, but not reported in previous literature.