ALCOHOLISM: CLINICAL AND EXPERIMENTAL RESEARCH

Vol. 38, No. 4 April 2014

Prevalence of Alcoholic Liver Disease and Its Association with Socioeconomic Status in North-Eastern China Haixia Wang, Lixian Ma, Qiling Yin, Xiaowei Zhang, and Cuiqin Zhang

Background: Alcohol consumption has substantially increased in China during the last 3 decades. Socioeconomic status (SES) most likely influences the development of alcoholic liver disease (ALD) in Chinese people who excessively consume alcohol. At the present time, however, little information is available in this field. The objectives of this study were to investigate the population-based prevalence of ALD and to identify the correlation of socioeconomics with the development of ALD. Methods: A cross-sectional survey was conducted in 8,186 individuals who resided in Shandong Province and were over 18 years old in 2011 using a randomized multistage clustered sampling approach. Among these subjects, 7,295 (89.12%) were interviewed. Questionnaires covered demographic characteristic, medical history, current medication, and health-relevant behavior, particularly alcohol consumption, dietary habit, and physical activity. Anthropometric measurements, biochemical tests, and abdominal ultrasonography were also performed. Results: Among the 7,295 subjects, 624 (8.55%) were diagnosed with ALD. The prevalence rate was significantly higher in males than in females (15.76% in males vs. 1.42% in females, p < 0.05). In this population, the risk of ALD was highest in the 40- to 49-year-old group. The incidence of ALD was highest in individuals who had a high level of occupation. Individuals who had received a low level of education had the highest incidence of ALD. Subjects with a low family income were more likely to have ALD than did those with an abundant family income. Currently, unmarried individuals had a higher incidence of ALD in the overall population. Conclusions: ALD is prevalent in north-eastern China. SES correlates with the development of ALD. Socioeconomic risk factors for ALD in north-eastern China include male gender, middle age, currently unmarried, low level of education, low family income, and high level of occupation. Key Words: Alcohol, Liver Diseases, Prevalence, Epidemiology, Socioeconomic Status, Risk Factors.

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URING THE PAST 3 decades, production and consumption of alcoholic beverage have significantly increased in China along with the continuing growth of economy in this country (Hao et al., 2004; Kim et al., 2008; Zhou et al., 2009). Alterations in life styles and dietary habits appear to be important factors associated with the increase in excessive alcohol consumption and the associated health problems in Chinese people. According to the World Health Organization global drinking database, China’s annual per capita consumption of alcoholic beverage is 0.49 l (over 15 years old) in 1961. In 1980, the per capita consumption of alcoholic beverage in China increased to 1.7 l. In 2003, this figure rose to 5.2 l (World Health Organization, 2007). Only 2 years later, the annual per capita consumption of alcoholic

From the Department of Infectious Diseases (HW, LM), Qilu Hospital of Shandong University, Jinan, China; and The Affiliated Hospital of Taishan Medical University (HW, QY, XZ, CZ), Taian, China. Received for publication June 21, 2013; accepted October 7, 2013. Reprint requests: Lixian Ma, Department of Infectious Diseases, Qilu Hospital of Shandong University, Jinan 250012, Shandong Province, China; Tel.: +86-531-82166855; Fax: +86-531-86927544; E-mails: [email protected], [email protected] Copyright © 2014 by the Research Society on Alcoholism. DOI: 10.1111/acer.12321 Alcohol Clin Exp Res, Vol 38, No 4, 2014: pp 1035–1041

beverage in China doubled again, increasing to 10.61 l in 2005 (World Health Organization, 2011). A recent report from the U.S. media (Neild, 2013) has indicated that China becomes the second country of heavy drinking in 2013, only next to the U.K. in the world. It has been known that moderate consumption of alcohol may reduce the risk of cardiovascular disease (Snow et al., 2009), but excessive drinking of alcoholic beverage is hazardous. Estimation suggests that only 0.51% of the drinking population currently has a correct concept of alcohol consumption. The proportion of individuals with an unacceptable concept of drinking is significantly higher in young people (Healthy drinking Chinese tour organizing committee, 2008). Changes in drinking status and increases in drinking-related health problems have drawn an urgent attention in China at the present time. Excessively drinking can result in at least 60 different kinds of diseases (Klatsky, 2007; Rehm et al., 2003). Particularly, excessive alcohol consumption injures the liver, causing hepatitis, liver steatosis (fat liver), fibrosis, and cirrhosis. More than 80% of heavy drinkers have been reported to have a certain degree of fat liver (Sussman et al., 2002). Indeed, excessive drinking of alcoholic beverage has become the second leading cause of liver disease in China in recent years. Currently, information about the prevalence of alcoholic liver disease (ALD) in China remains inconsistent. 1035

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China has a broad territory with the largest population of people in the world. Social economic development in China is dramatically uneven. People living in different regions in China share distinctive styles of living with a diversity of cultures and traditions. The report of Science Evaluation System Research about the development of small- and mediumsized cities in China in 2012 has described 75.4% of the total population in China as residing in the administrative area of small- and medium-sized cities, which are defined as the cities with urban resident population less than 1 million and with the township area of independent development (Urban economic society of China small and medium-sized city’s economic development commission, 2012). Taian is a District of Shandong Province, the birthplace of Confucianism whose philosophy has dominated Chinese culture for over 2,000 years. Taian District is a typical small and mediumsized city with a resident population of 760,100. Therefore, we conducted our investigation in this representative resident population to analyze the prevalence of ALD in Chinese people living in north-eastern China. In this investigation, we employed a population-based cross-sectional survey complemented with anthropometric measurements, biochemical tests, and abdominal ultrasonography to identify the relationship of socioeconomic status (SES) and the development of ALD. MATERIALS AND METHODS Sampling The survey was carried out from September to November 2011. Primary sampling sites were in Taian City in Shandong province located in north-eastern China. Multistage randomized cluster sampling methods were used to identity subjects. In the first stage, 15 neighborhood communities were randomly selected. Then, 8,186 households were randomly selected from the 15 neighborhood communities. Among these selected 8,186 subjects, 170 (2.08%) refused to participate in the study and 721 (8.81%) only finished part of the interview. A total of 7,295 (89.12%) subjects completed the interview. All respondents were individuals aged over 18 years old. All of the respondents gave written informed consent, and the study protocol was approved by the Ethics committee of Taishan Medical University. Completion of the questionnaires was completely voluntary. Interview and Physical Examination A face-to-face interview was carried out by specially trained postgraduate students of Taishan Medical University under supervision of experienced investigators. Standard questionnaires, designed by coworking of epidemiologists and hepatologists, included the following items: demographic characteristics, current use of medication, medical history, and alcohol use including quantity of alcohol intake each time, times of alcohol intake each day, months of alcohol intake each year, years of alcohol intake, types and concentrations of alcoholic beverage, drinking and dietary habits. From these data, the average daily alcohol intake (g/d) and duration of drinking (years) were calculated using the alcohol dose converting formula. Physical examinations covered body height, weight, blood pressure, waist circumference (WC), and routine anthropometric parameters in healthy checkup.

Biochemical Tests Venous blood samples were collected from fasting subjects by routine methods. Fasting serum glucose levels and lipid profiles were measured with an automatic chemistry-immuno-analyzer (Olympus Corporation, Tokyo, Japan). Serum levels of aspartate aminotransferase (AST), alanine aminotransferase (ALT), gamma glutamyl transpeptidase (GGT), bilirubin, and albumin were determined by standard laboratory methods. Tests for the serum makers of hepatitis A virus, hepatitis B virus (HBV), and hepatitis C virus were also performed. Ultrasonography Real-time ultrasonography of the upper abdominal organs was performed for each subject by 2 experienced physicians using a scanner equipped with a 3.5-mmHz transducer (Siemens Adama, Erlangen, Germany). Physicians who performed the real-time ultrasonography were blocked from accessing to any clinical and laboratory results. Diagnostic Criteria Moderate or “low-risk” drinking was defined as an average daily consumption of no more than 25 g/d pure alcohol for men and less (15 g/d) for women (Chinese Nutrition Society, 2008). Heavy or “at-risk” drinking was defined as an average daily consumption of 40 g/d or more of pure alcohol for men (roughly equivalent to 4 or more standard drinks per day. A standard drink in the United States contains 13.7 g (0.6 ounces) of pure alcohol and generally is equivalent to a 12 ounce beer, 8 ounces of malt liquor, 5 ounces of wine, or 1.5 ounces of 80-proof distilled liquor (i.e., gin, vodka, whiskey) (Centers for Disease Control and Prevention, 2011) and 20 g or more of pure alcohol for women (roughly equivalent to 2 or more standard drinks per day) (Fatty liver and alcoholic liver disease study group of the Chinese liver disease association, 2010). ALD was diagnosed according to the guidelines for diagnosis and treatment of alcoholic fatty liver (AFL) diseases (Fatty liver and alcoholic liver disease study group of the Chinese liver disease association, 2010). Briefly, the diagnosis of ALD was based on the combination of medical history, clinical symptoms, laboratory, and real-time ultrasonography findings. Viral hepatitis and other chronic liver diseases needed to be ruled out. Clinical classifications of ALD included mild alcoholic liver disease (AML), AFL, alcoholic hepatitis (AH), and alcoholic cirrhosis (AC). In this epidemiological study, fatty liver disease (FLD) was diagnosed and staged by real-time ultrasonography findings. ALD was diagnosed when a subject met the FLD criteria along with drinking more than 40 g (male) or 20 g (female) alcohol per day over 5 years. The diagnostic patterns of FLD by real-time ultrasonography were the presence of a “bright” liver (brightness and posterior attenuation) with stronger echoes in the hepatic parenchyma than in the renal parenchyma and the existence of vessel blurring and narrowing of the lumen of hepatic veins in the absence of findings suggestive of other chronic liver diseases. Obesity was categorized according to the body mass index (BMI) criteria for Asians issued by the Regional Office for Western Pacific Region of the World Health Organization. Subjects with BMI ≥ 25 were considered as obese (Anuurad et al., 2003). Ventral obesity was diagnosed according to the WC criteria for Chinese (Joint committee for developing Chinese guidelines on prevention and treatment of dyslipidemia in adults, 2007). The respondents were categorized as nonventral obesity group (WC < 85 cm for men and WC < 80 cm for women) or ventral obesity group (WC ≥ 85 cm for men and WC ≥ 80 cm for women).

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Table 1. Sociodemographic Characteristics of Respondents

Socioeconomic Status Parameters of SES included educational level, monthly income, occupation, and current marital status. The educational levels were divided into below junior high school (9 years). Monthly income per capita was calculated by dividing the mean monthly total household income in the preceding year by the number of family numbers. Monthly income levels were divided into RMB1,600 based on the results calculated from monthly income per capita of all respondents. Occupational designations included white collar (professional or government employees), blue collar (manual workers, farmers), and unemployed (not in labor force or housewife or student). Marital status included currently unmarried (single/separated/divorced/widowed) and currently married. Quality Control Interviewers were trained using a standard training manual for 5 days prior to conducting the interview. Total trained interviewers were divided into 5 groups each containing 8 to 10 interviewers. Each group was supervised by an experienced psychiatrist or epidemiologist. After each interview, the questionnaire was checked and signed by the interviewer. The supervisors were responsible for checking questionnaires completed by their corresponding groups each day. Any missed item or inconsistent information was added or verified by reinterviewing the subject the next day. Statistical Analysis Continuous variables were described as means  standard deviation (SD) if they had normal distribution, and the differences were tested by Student’s t-tests or 1-way analysis of variance for statistical significance. The differences in categorical variables were tested by the chi-squared test (v2 test) or the Fisher’s exact probability test. Adjusted odds ratios and 95% confidential intervals derived from multiple logistic regression models were used to assess the relationship between ALD and sociodemographic variables. Two-tailed values were considered to be significant at 60 511 14.1 598 Years of education 9 1,347 37.1 1,443 Mean monthly per capita family income, RMB 60 1,109 Years of education 9 2,790 Mean monthly per capita family income, RMB 0.05). Association of ALD and Sociodemographics Adjusted odds ratios and 95% confidence intervals of ALD by sociodemographic characteristics are shown in Table 6. In overall population and male population, the risk of ALD was highest in the 40- to 49-year-old group. The highest risk of ALD was observed in subjects with high rank of occupation. The lowest risk of ALD was found in individuals with the highest level of education in overall population and male population. In male population, individuals with a higher family income were more likely to have ALD than those with the lowest level of family income. The risk of ALD was lower in subjects with higher family incomes in

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Table 4. Occurrence of Clinical Symptoms and Incidence of Abnormal Real-Time Ultrasonography Findings in Upper Abdominal Organs of ALD Patients Controls (n = 6,671) Fatigue and/or anorexia (n, %) United States (n, %)

AML (n = 455) a

763 (11.44) 706 (10.58)

36 (7.91) 455 (100)a

AFL (n = 125) 27 (21.60) 125 (100)a

AH (n = 31) a

31 (100) 31 (100)a

AC (n = 13) 13 (100)a 13 (100)a

ALD, alcoholic liver disease; AML, mild alcoholic liver diseases; AFL, alcoholic fatty liver, AH, alcoholic hepatitis; AC: alcoholic cirrhosis. a p < 0.05 compared to control group.

Table 5. Multivariate Regression Logistic Models for the Association Between SES and Prevalence of ALD Variables Age Occupation Marriage Male FBG Duration of drinking Daily alcohol intake BMI Education Constant

ß 0.024 1.230 0.846 0.589 0.996 0.043 0.052 0.118 0.178 13.408

SE

Wals

p

OR

95% CI

0.008 0.164 0.145 0.231 0.072 0.007 0.003 0.036 0.105 1.047

9.005 56.064 33.994 6.506 189.387 43.101 422.481 10.496 2.844 164.029

0.003 0.000 0.000 0.011 0.000 0.000 0.000 0.001 0.092 0.000

0.976 3.420 2.330 0.555 2.708 1.044 1.054 1.125 0.837 0.000

0.961 to 0.992 2.479 to 4.718 1.753 to 3.097 0.353 to 0.872 2.350 to 3.121 1.031 to 1.057 1.049 to 1.059 1.048 to 1.208 0.681 to 1.029

ALD, alcoholic liver disease; BMI, body mass index; FBG, fasting blood sugar; SES, socioeconomic status.

overall population. Being currently unmarried was a risk factor for ALD in overall population and male population. DISCUSSION Using a phased random sampling method, we investigated residents over the age of 18 in Taian, Shandong Province. In this study, we have observed that the prevalence of ALD is highest in individuals with ages from 40 to 49 years old. This observation is different from results of studies in foreign countries in which the highest ALD prevalence is usually found in individuals with ages from 18 to 34 years old. In a recent report from the U.S. Centers for Disease Control and Prevention (2009), it is documented that the highest prevalence of heavy episodic drinking is among persons with ages of 18 to 24 and 25 to 34. In China, the traditional culture is not in favor of young people consuming alcoholic beverages. It is widely accepted that young people under the age of 20 should not be actively involved in drinking activities. Furthermore, the youth commonly depend on family for financial support in China, which restricts their access to alcoholic beverages. Excessively drinking alcoholic beverages, particularly distilled alcoholic beverages containing high concentrations of alcohol (liquor or spirit), usually occurs in circumstances of formal social events in China, such as banquets and dinners among friends and business partners or clients in middle-aged Chinese people. Peer pressure for consuming excessive amount of alcohol frequently exists among participants in these social events for the expectation of establishing, maintaining, and/or developing personal friendship or social networking relationships.

Middle-aged people constitute the major population involved in these social activities. In addition, middle-aged Chinese people are relatively stable in family income. Their independence in financial status facilitates accessing and consuming alcoholic beverages. All these factors may contribute to the increased ALD prevalence in individuals with ages of 30 to 39 years old in China. With accumulation of life experience, senior people are relatively less active in participating in social events. In turn, they tend to be concerned more about maintaining physical and mental health, which may be beneficial for reducing ALD prevalence rate in these people (Healthy drinking Chinese tour organizing committee, 2008). Our study shows that there are differences of drinking rate and ALD prevalence between male and female subjects (drinking rate 74.51% vs. 11.32%, p < 0.05; the ALD prevalence rate of 15.76% vs. 1.42% in male and female subjects, respectively, p < 0.05). These data are in agreement with Chinese national averages (Cui et al., 2010; Huang et al., 2005; Li et al., 2003; Lu et al., 2003;). The reason for lower rates of drinking and ALD prevalence in female subjects in China may include the following elements. First, adult females in Chinese families traditionally contribute more effort in management of family daily life including taking care of kids and elderly family members. They commonly have less opportunities to participate in social events and expose themselves to the environment of alcohol abuse. It is generally acceptable that no peer pressure of excessive drinking should be exerted on females even if they participate in social banquets. Second, females have a strong sense of self-protection because of traditional education and thus, to some extent, limit their alcohol intake (Li et al., 2012). Third, females have the

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Table 6. Adjusted Relative Riska (95% CI) of ALD Prevalence from all Causes within Socidemographic Characteristics

Predictors

Total ALD OR (95%CI)

Age, in years 18 to 29 0.341 (0.128 to 0.911)b 30 to 39 0.684 (0.355 to 1.319) 40 to 49 2.387 (1.371 to 4.156)b 50 to 59 2.092 (1.243 to 3.521)b >60 1.00 (Ref) Years of education 9 0.788 (0.471 to 1.316) Mean monthly per capita family income, RMB 0 1.00 (Ref) 800 to 1,599 0.920 (0.665 to 1.272) ≥1,600 0.922 (0.664 to 1.280) Occupation Unemployed 1.00 (Ref) Blue collar 10.347 (3.567 to 30.001)b White collar 14.989 (4.964 to 42.256)b Marital status Married 1.00 (Ref) Unmarried 3.170 (2.286 to 4.395)b

Male ALD OR (95%CI)

Female ALD OR (95%CI)

0.245 (0.088 to 0.685)b 0.379 (0.179 to 0.803)b 1.227 (0.663 to 2.270) 1.204 (0.687 to 2.110) 1.00 (Ref)

7,562.614 ( ) 51.777 ( ) 0.000 ( ) 56.139 ( ) 1.00 (Ref)

1.00 (Ref) 0.767 (0.476 to 1.234) 0.319 (0.175 to 0.583)b

1.00 (Ref) 41.111 ( ) 1,460.598 ( )

1.00 (Ref) 1.054 (0.710 to 1.565) 1.205 (0.834 to 1.739)

1.00 (Ref) 0.000 ( ) 0.017 ( )

1.00 (Ref) 10.968 (2.852 to 42.178)b 25.518 (6.282 to 104.164)b

1.00 (Ref) 21.225 ( ) 28.327 ( )

1.00 (Ref) 2.420 (1.666 to 3.515)b

1.00 (Ref) 973.436 ( )

ALD, alcoholic liver disease. a Adjusted for age, education, income, occupation, marital status, serum lipid profiles, fasting blood sugar, hepatitis B virus infection, causes of alcohol, types of alcohol beverage, daily alcohol intake, duration of drinking, body mass index, and waist circumference. b Odds ratio is significant, p < 0.05. Ref, reference category.

responsibility of fertility. Negative effects of alcohol consumption by the mother on the health of the next generation in the family are well recognized in the Chinese society. Our data demonstrate that low level of education and low income are associated with a high risk rate of ALD. In the past several decades, poorly-educated people in China have fewer opportunities to obtain a stable job with high pay and usually work in manual labor. People working on jobs required for hard laboring frequently consume alcohol after duties to relax themselves. These individuals, therefore, often develop a habit of drinking in their dinner times. Associated with this style of alcohol consumption is a higher ALD prevalence rate in people working with high intensity of laboring, which constitutes one of the risky drinking patterns in current China (Hao et al., 1999). Interestingly, individuals who have high level of occupation suffer a high prevalence of ALD. This is a unique observation in our current study. Actually, they are the major population actively participating in social interaction. Frequent exposure to group activities of alcohol consumption may account for the increased risk of ALD in folks who received a high level of education. This result strongly supports the idea that heavily social drinking is a major problem of unhealthy consumption of alcohol in current China (Tao et al., 2004). In this study, currently, unmarried subjects suffer a higher rate of ALD than the married in China. Chinese people usually drink due to social activities (Cochrane et al., 2003; Yang, 2002). Unmarried individuals usually have a better economic condition and enjoy more social activities and/or drinking opportunities than those have successful marriage.

As described previously, this study was conducted in Taian where is a representative district for small- and medium-sized cities in China. Drinking patterns and the associated ALD prevalence in large cities such as Beijing, Shanghai, and Guangzhou may not be identical to our currently reported features. Geographically, Taian is located in north-eastern China. Due to uneven development of the economy and differences in social life styles as well as eating habits in the North compared with those in the South (Cochrane et al., 2003; Zhou et al., 2011), data obtained from this study may typically represent the ALD prevalence in the north-eastern part of China. In summary, our current study shows that ALD is prevalent in north-eastern China. SES correlates with the development of ALD. Socioeconomic risk factors for ALD in north-eastern China include male gender, middle age, low level of education, low family income, and high level of occupation. Identifying these unique features of alcohol consumption and the associated ALD prevalence in relation to SES is critical for developing population-based effective strategy to educate people for adjusting their drinking patterns in order to prevent ALD. ACKNOWLEDGMENTS This project was supported by Taishan District Health Bureau in Taian City. We are grateful to Dr. Ning Fu (Taishan University, China) for her linguistic guidance on the manuscript.

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Prevalence of alcoholic liver disease and its association with socioeconomic status in north-eastern China.

Alcohol consumption has substantially increased in China during the last 3 decades. Socioeconomic status (SES) most likely influences the development ...
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