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Prevalence and risk factors of chronic liver disease among oil refinery workers

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J Occup Health 2002; 44: 22–27

Occupational Health

Prevalence and Risk Factors of Chronic Liver Disease among

Oil Refinery Workers

Hon-Ke S

IA1

, Jung-Der W

ANG2, 3

, Chun-Cheng H

UANG3

and Chi-Hung H

UANG3

1Department of Internal Medicine, Chang-Hua Christian Hospital,

2Department of Internal Medicine, National Taiwan University Hospital and

3Institute of Occupational Medicine and Industrial Hygiene, National Taiwan University College of Public Health,

Taiwan

Abstract: Prevalence and Risk Factors of Chronic Liver Disease among Oil Refinery Workers: Hon-Ke SIA, et al. Department of Internal Medicine,

Chang-Hua Christian Hospital—Objectives: The

objective of this study was to determine the prevalence and major risk factors of chronic liver diseases among workers in an oil refinery and research factory with ultrasonography as an assessment tool. Methods: After a walk-through survey in the factory, workers were classified into exposed and non-exposed groups. Regular health screening data for the past four years were collected and all 700 workers were asked to fill out a questionnaire about their life style. A total of 345 workers voluntarily participated in the study, and 326 of them had abdominal ultrasonography. Results: Fatty liver disease (FLD) was found to be the most common problem (27.9%), followed by hepatitis virus infection (HBsAg positive rate: 18.0%, anti-HCV positive rate: 2.6%). The major causes of persistent alanine aminotransferase (ALT) increase were FLD and hepatitis virus infection. Obesity was the most important determinant of FLD and hepatitis virus infection was that of parenchymal liver disease (PLD). Modeling by multiple logistic regression model demonstrated that exposure to petroleum distillates or other chemicals in this factory was not associated with FLD, PLD or persistent ALT increase even in workers employed for more than twenty years. Obesity and virus infection did not show a synergistic hepatotoxic effect on solvent exposure probably due to a low level of exposure. Conclusions: Fatty liver and chronic hepatitis B infection were the major chronic liver diseases in oil-refinery workers in Taiwan, where exposure to hepatotoxic solvents was low.

(J Occup Health 2002; 44: 22–27)

Received May 17, 2001; Accepted Sep 27, 2001

Correspondence to: J.D. Wang, Institute of Occupational Medicine and Industrial Hygiene, National Taiwan University College of Public Health, No. 1, Jen-Ai Road, Taipei, Taiwan

Key words: Chronic liver disease, Ultrasonography,

Solvent, Oil refinery worker

Acute liver injury due to some organic solvents such as halogenated hydrocarbons, dimethylformamide (DMF) are well known1, 2), but the chronic effects on liver of

long-term occupational exposure to low levels of organic solvents remain undetermined. Many cases of liver cirrhosis without known etiology raise the suspicion that

some may be of occupational origin3). A recent small

case-control study also showed that occupational exposure to organic solvents might play a role in the development of fatty liver disease (FLD)4).

Associated epidemiological studies in this field were difficult for several reasons, which included: (1) the approach to chronic liver damage among workers was unsuccessful due to vague symptoms and signs and the lack of specificity and sensitivity of conventional liver enzyme tests; (2) the cause of chronic liver damage might lie in a number of factors rather than in isolated

occupational exposure3). The limitations are further

highlighted by the studies among workers exposed to mixed solvents of aromatic and aliphatic hydrocarbon that have failed to detect any abnormality in these serum enzyme tests5).

The combination effect of occupational and non-occupational factors including alcohol consumption, hepatitis virus B (HBV) or C (HCV) infection,

medications and obesity may also be important6). Some

studies raised the concern that these factors may potentiate the effects of hepatotoxin exposure7–10). The causes of an

increase in liver transaminase detected in routine screening therefore usually need further diagnostic workup, in which noninvasive ultrasonography (US) may provide additional information.

The major objectives of this cross-sectional study are to determine the prevalence of CLD among workers in

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an oil refinery factory. We also identify the major determinants of CLD and investigate whether these factors have a synergistic hepatotoxic effect on solvent exposure. We control for non-occupational factors and apply abdominal US in this study.

Methods

The oil refinery factory produces petroleum distillates containing aliphatic and aromatic hydrocarbons except benzene, toluene and xylene. The general production process of this factory includes distillation, refining, extraction, blending and n-hexane hydrotreating. Many employees who also work in the laboratory of research and development might be occasionally exposed to halogenated hydrocarbons such as chloroform, carbon tetrachloride and trichloroethane.

Subjects and data collection

The study subjects were recruited from workers in an oil refinery factory with 700 employees during the time period from December 1999 to March 2000. All workers had a complete physical examination including serum alanine aminotransferase (ALT), total cholesterol, triglyceride and serological tests for HBV and HCV. All of them were also invited to fill out a questionnaire and have abdominal ultrasonography. Three hundred and forty-five of the 700 employees responded and participated in the study. The questionnaire asked about medical history, occupation (job title, chemical compounds used, duration of employment), alcohol consumption (average drinks per week and duration of drinking) and medications taken. All questionnaires were reviewed by an occupational physician to verify the data and assure data quality. We also collected the health data from regular annual physical examinations in the past four years that were conducted by the staff of St. Martins Hospital, which is a general hospital with 600 beds and has been accredited as a teaching hospital by the Department of Health of Taiwan since 1997. The serum ALT examination was done with an auto-analyzer Integra 700 (U.S.A.). Its cutoff value was provided by the clinical laboratory of this hospital. All workers who had an increase above the normal range twice or more during the last four years of annual screening were regarded as having a persistent ALT increase. In this study, we measured the serum ALT, total cholesterol and triglyceride with a Hitachi 7150 auto-analyzer (Tokyo, Japan). We used enzyme immunoassay (Murex Co., USA) to perform hepatitis B surface antigen (HBsAg) and anti-HCV antibody tests (anti-HCV III, Murex Co., USA).

Ultrasonography was performed and interpreted by two skilled board-certified gastroenterologists. A real-time machine, Panasonic PANAVISTA-LSCI (Panasonic Co. Ltd., Tokyo, Japan) equipped with a linear-type 3.5 MHz transducer, was used. In general, the two major

histological features in diffuse parenchymal liver disease

are steatosis and fibrosis11), which can be largely

differentiated by US12, 13). Briefly, the main indicator of

steatosis was an increase in the echogenicity of the liver in comparison with the cortex of the right kidney. We also applied additional parameters including masking the walls of portal vein branches in the right lobe, masking the gallbladder wall, and far gain attenuation of the liver. In contrast, a nodular surface of the liver, coarse or heterogenous echotexture compared with the spleen and irregular narrowing of the hepatic vein suggested a diagnosis of hepatic fibrosis. In our study, the term ‘fatty liver disease’ (FLD) meant steatosis of the liver whereas ‘parenchymal liver disease’ (PLD) indicated various diffuse parenchymal liver disease other than fatty liver and implied hepatic fibrosis.

Workplace evaluation

We conducted a comprehensive walk-through survey for every single unit of operation. After identifying all the potential hazards, we classified workers into the following four exposure zones: (1) manufacture: direct exposure to petroleum distillates; (2) utility: intermittent exposure to petroleum distillates; (3) laboratory: occasional exposure to halogenated hydrocarbons; (4) administration: no or very low exposure. Workers in the first three groups were further categorized as the exposed and the last one was the non-exposed.

Data analysis

We used multiple logistic regression to determine the association between risk factors and CLD. The following risk factors were included: age, gender, body mass index (BMI), duration of employment, occupational exposure zone, alcohol consumption, potentially hepatotoxic drugs taken, history of diabetes mellitus (DM), total cholesterol, triglyceride, HBsAg and anti-HCV. BMI was calculated as weight in kilograms divided by squared height in meters. A value greater than 27 was considered obese. Workers who drank 140 grams of ethanol weekly for at least 5 yr were defined as drinkers. Odds ratio with 95% confidence intervals (95% CI) were calculated. All of the statistical analyses were conducted with SPSS/PC 9.0®

software on a personal computer14).

For further evaluation of the relationship between specific solvent exposure and CLD, we also used the Haenszel summary procedure and the Mantel-extension for the test of trends15, 16).

Results

More than three-fourths of all workers were male and the average age was 48 yr. There was a low turnover rate in the factory and the average duration of employment was about 23 yr. Table 1 summarized the demographic characteristics of respondents and non-respondents for

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comparison. The prevalence of HBsAg carriers in respondents was 18.0% which was slightly higher than that in the non-respondents and close to the average

nationwide prevalence of 14–20%17). The prevalence of

anti-HCV was 2.6%, which was also within the range of

the general population in Taiwan (about 1–4%)18, 19).

There were no significant differences between the respondents and non-respondents in the factory except the sex ratio. Three hundred and twenty-six of 345 (94.5%) respondents had successful abdominal ultrasonography.

Table 2 shows the prevalence rates of various liver diseases stratified by persistent ALT increase. We used abdominal ultrasonography, HBsAg, anti-HCV and serum ALT values in the past four years as our diagnostic basis. We also found 39 patients with hepatic cysts, 6 patients with hepatic hemangioma, 11 patients with gallbladder stones and 22 patients with gallbladder polyps but they were not included as CLD in our study. FLD was found

to be the most common problem (27.9%), followed by chronic HBV infection (18.0%). Although FLD, HBsAg and anti-HCV carriers were found to be associated with persistent ALT increase, more than two-thirds of them did not show persistent ALT abnormalities.

The effects of various non-occupational and occupational factors on FLD, PLD and persistent ALT increase are summarized in Table 3. It shows that workers who had a BMI greater than 25, total cholesterol greater than 200 mg/dl or triglyceride greater than 200 mg/dl were associated with increased risk for FLD. Positive HBsAg increased and total cholesterol between 200 and 240 mg/dl reduced the risk for PLD. Factors related to persistent ALT increase were male gender, age younger than 45 yr, positive anti-HCV, BMI greater than 25 and a history of DM. Obesity, defined as the BMI index, appeared to be an important contributor to both FLD and persistent ALT increase, and the associations showed a dose-response relationship. HCV infection was

Table 1. Comparison of demographic and health characteristics of respondents and non-respondents in the refinery company

Items Respondents Non-respondents

(N=345) (N=372)

Male Gender 74.5% 81.7%†

Age (yr) 47.5 ± 6.8* 48.4 ± 7.5

Duration of employment (yr) 22.9 ± 8.4 22.7 ± 9.9

HBsAg positive rate 18.0% 14.9%

Anti-HCV positive rate 2.6% 5.5%

Body mass index (kg/m2) 24.3 ± 2.9 24.4 ± 3.1

Serum total cholesterol (mg/dl) 207.5 ± 36.1 204.7 ± 35.3 Serum triglyceride (mg/dl) 127.2 ± 76.4 134.4 ± 108.3

Serum ALT (U/L) 32.7 ± 46.0 31.2 ± 25.0

*Mean ± SD. †p<0.05.

Table 2. Frequencies of various liver diseases, stratified by the presence of persistent ALT increase or not

Persistent ALT increase

Total Yes No Hepatitis marker Study subjects 66 279 345 Positive HBsAg 17 45 62 Positive Anti-HCV 5 4 9 Abdominal ultrasonography Study subjects 56 270 326

Fatty liver disease 32 59 91

Parenchymal liver disease 5 18 23

Hepatocellular carcinoma 0 1 1

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associated with persistent ALT increase (OR 6.6; 95% CI 1.3, 33.0). But HBV infection did not show a similar association, because a large proportion of them were so-called healthy carriers. Nonetheless, HBV infection did play a major role in the formation of PLD (OR 15.8; 95 %CI 5.4, 46.6). Because there were only 10 workers who fulfilled the definition of alcohol drinker, our data did not show a significant effect of alcohol.

We tried several ways to define and analyze occupational exposures in the oil refinery factory. Neither employment for more than 20 years, exposure to various kinds of solvents, nor working in different exposure zones resulted in a statistically significant difference between

the exposed and the non-exposed workers for FLD, PLD and persistent ALT increase after adjusting for other potential confounders. There was also no synergistic effect of hepatitis virus infection and solvent exposure on the development of FLD, PLD and persistent ALT increase (data not shown here).

Discussion

The study showed that present exposure to petroleum distillates in the factory or hepatotoxic solvents used in the laboratory was not significantly associated with increased risk of FLD, PLD or persistent ALT increase. Because this is a cross-sectional study and we assume a

Table 3. Effects of various potential confounders and of solvent exposure on odds ratios (OR, with 95 % confidence interval abbreviated as CI) of persistent alanine aminotransferase (ALT) increase, fatty liver disease and parenchymal liver disease, analyzed by multiple logistic regression (NS: statistically non-significant)

Dependent variable Independent Persistent ALT Fatty liver Parenchymal

Variable increase disease liver disease

Adjusted OR Adjusted OR Adjusted OR

(95% CI) (95% CI) (95% CI)

Gender Male: 1 4.5 NS NS Female: 0 (1.4, 14.1) Age > 45 y/o: 1 0.4 NS NS ≦45 y/o: 0 (0.2, 0.9) HBsAg Positive: 1 NS NS 15.8 Negative: 0 (5.4, 46.6) Anti-HCV Positive: 1 6.6 NS NS Negative: 0 (1.3, 33.0) Alcohol ≧140 g/wk: 1 NS NS NS consumption < 140 g/wk: 0

Medications taken Yes: 1 NS NS NS

No: 0

Body mass index 25≦BMI<27 2.6 4.5 NS

(kg/m2) vs. BMI<25 (1.2, 5.5) (2.3, 9.1)

BMI≧27 6.3 15.7 NS

vs. BMI<25 (2.9, 13.5) (7.2, 34.2)

History of DM Yes: 1 5.3 NS NS

No: 0 (1.5, 18.2)

Total cholesterol 200≦Chol<240 NS 2.0 0.3

(mg/dl) vs. Chol<200 (1.0, 3.8) (0.1, 0.9)

Chol≧240 NS 2.4 NS

vs. Chol<200 (1.0, 5.9)

Triglyceride TG≧200:1 NS 2.9 NS

(mg/dl) TG<200:0 (1.2, 7.2)

Solvent exposure Exposed: 1 NS NS NS

Non-exposed: 0

Duration of > 20 yr: 1 NS NS NS

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present exposure zone for the previous long-term effect, it does not necessarily indicate that there was relatively little risk of CLD with the present exposure level, but the following observations seemed to corroborate the above conclusion. Firstly, petroleum distillates including aliphatic and aromatic solvents were thought to be less hepatotoxic in past studies with the exception of heavy exposure during a short period7, 20–22). Secondly, modern

oil-refinery factories, like this one, are fully automated and enclosed. There was relatively little chemical exposure, which was demonstrated by the regular air sampling data showing below one-tenth of TLV (threshold limit value) recommended by the ACGIH (American

Conference of Governmental Industrial Hygienists)23).

From our field investigation and discussion with the safety specialist, the major exposure occurred mainly in maintenance operations and unscheduled events such as a leak or spillage. Although laboratory workers are occasionally exposed to well-known hepatotoxic agents, they are protected with adequate equipment especially local exhaust ventilation. Thirdly, HBsAg carriers may be more likely to develop liver damage caused by alcohol and other hepatotoxic agents such as DMF24, 25), but there

were no significant synergistic effects due to various occupational exposures and HBV infection on liver damage in our study. A similar concern was also

postulated for obesity and hepatotoxic exposure8). But

our multi-variate modeling did not find such an effect either on laboratory workers exposed to halogenated hydrocarbons or other workers exposed to petroleum distillates. Although we could not completely rule out the effect of random misclassification or the healthy

worker effect on a cross-sectional study design26), we

might still conclude the that non-occupational factors rather than occupational factors play the main role in the occurrence of FLD, PLD and persistent ALT increase in our study subjects.

In general, conventional liver enzyme tests such as ALT reflect acute cytotoxicity and are proposed to be an effective screening marker for acute liver injury27). It

has been adopted for regular medical surveillance of workers potentially exposed to hepatotoxic or even organic chemicals in many developed countries such as the United States, Germany and Japan, etc.28). But, as a

result of improved industrial hygiene, acute liver injury seems to have decreased in recent years, even in Taiwan. Current concerns are related to the prolonged, low-level exposure that causes chronic liver damage including chronic inflammation, hepatic fibrosis, steatosis, vascular injury and malignancy, as seen in our study. In this circumstance, ALT provides limited sensitivity and specificity27). It might be improved in two ways: firstly,

by obtaining serial follow-up ALT data rather than only one single ALT value. If ALTs show persistent abnormalities, chronic liver inflammation should be

considered. This is the reason why we used ALT values for four years as a potential indicator of CLD. Secondly, use image study, especially abdominal ultrasonography. For mild liver disease with structural change but no persistent biochemical abnormality, ultrasonic study could provide additional information in assessing either focal or diffuse parenchymal liver disease29). The drawback to

ultrasonic study is its dependence on the subjective judgement of the operators and it is less feasible to be performed on a large number of exposed individuals as serum biochemical tests. In our study, the ultrasonic studies were performed by two operators with the same training background and reviewed by a third physician according to the diagnostic criteria but without knowing

the degree of exposure12). Therefore, the bias between

operators could be reduced to a minimal. As current ultrasonograph equipment is usually portable, very accurate and non-invasive, we recommend that it be used for screening of chronic liver damage to supplement serial liver enzyme tests, especially for workers with potential hepatotoxin exposure or risk factors of CLD.

We found a low prevalence of alcohol drinking among oil-refiners. This could be partially attributed to the higher prevalence of allele ALDH22 and ADH22 in the Taiwanese

population30, 31) compared with western countries.

Subjects with these genetypes would experience more intense reaction to alcohol than those without them. Moreover, because workers in this oil-refinery factory were considered to be governmental employees, they were forbidden to drink alcohol in public bars and thus less likely to develop such a habit. Therefore, there might be some healthy selection effect and a tendency to underestimate the prevalence of CLD.

Acknowledgments: This study was supported by a grant

from the National Health Research Institute (NHRI-GT-EX89 P5049).

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數據

Table 2. Frequencies of various liver diseases, stratified by the presence of persistent ALT increase or not

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