Gender and Metabolic Differences of Gallstone Diseases

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BRIEF ARTICLES

Gender and metabolic differences of gallstone diseases

Hui Sun, Hong Tang, Shan Jiang, Li Zeng, En-Qiang Chen, Tao-You Zhou, You-Juan Wang

Hui Sun, Hong Tang, En-Qiang Chen, Tao-You Zhou,Center of Infectious Diseases, West China Hospital of Sichuan

University; Division of Molecular Biology of Infectious Diseases,

the State Key Laboratory of Biotherapy (Sichuan University),

Chengdu 610041, Sichuan Province, China

Shan Jiang, First Department of Internal Medicine, WushengPeoples Hospital, Guangan 638400, Sichuan Province, China

Li Zeng, You-Juan Wang, Physical Examination Center,West China Hospital of Sichuan University, Chengdu 610041,

Sichuan Province, China

Author contributions: Tang H, Sun H and Wang YJ designed theresearch; Sun H, Zeng L, Chen EQ and Zhou TY performed the

research; Jiang S and Sun H analyzed data; Sun H wrote the paper.

Supported by The National Natural Science Foundation ofChina, No. 30571640; and the National Basic Research Program

of China, No. 2006CB504302 and No. 2007CB512902

Correspondence to: You-Juan Wang, Associate Professor,Physical Examination Center, West China Hospital of Sichuan

University, Chengdu 610041, Sichuan Province,

China. [email protected]

Telephone: +86-28-85422866 Fax: +86-28-85422818Received: December 30, 2008 Revised: February 22, 2009

Accepted: March 1, 2009Published online: April 21, 2009

Abstract

AIM: To investigate the risk factors for gallstone

disease in the general population of Chengdu, China.

METHODS: This study was conducted at the WestChina Hospital. Subjects who received a physicalexamination at this hospital between January and

December 2007 were included. Body mass index, bloodpressure, fasting plasma glucose, serum lipid andlipoproteins concentrations were analyzed. Gallstone

disease was diagnosed by ultrasound or on the basisof a history of cholecystectomy because of gallstonedisease. Unconditional logistic regression analysiswas used to investigate the risk factors for gallstonedisease, and the Chi-square test was used to analyzedifferences in the incidence of metabolic disordersbetween subjects with and without gallstone disease.

RESULTS: A total of 3573 people were included,10.7% (384/3573) of whom had gallstone diseases.

Multiple logistic regression analysis indicated that theincidence of gallstone disease in subjects aged 40-64or 65 years was signicantly different from that in

a high level of fasting plasma glucose was obvious

in gallstone disease (P < 0.05), and in women,

hypertriglyceridemia or obesity were significant in

gallstone disease (P< 0.05).

CONCLUSION: We assume that age and sex are

profoundly associated with the incidence of gallstone

disease; the metabolic risk factors for gallstone diseasewere different between men and women.

2009 The WJG Press and Baishideng. All rights reserved.

Key words: Gallstone disease; Metabolic disorder; Risk

factor; Sex; Age

Peer reviewer: Dr. Karel van Erpecum, Department ofGastroenterology and Hepatology, University Hospital Utrecht,

PO Box 855003508 GA, Utrecht, The Netherlands

Sun H, Tang H, Jiang S, Zeng L, Chen EQ, Zhou TY, Wang YJ.

Gender and metabolic differences of gallstone diseases. World JGastroenterol2009; 15(15): 1886-1891 Available from: URL:http://www.wjgnet.com/1007-9327/15/1886.asp DOI: http://

dx.doi.org/10.3748/wjg.15.1886

INTRODUCTION

Gallstone disease is prevalent worldwide; however, its

prevalence varies by region. In Western countries, the

prevalence of gallstone disease reportedly ranges fromapproximately 7.9% in men to 16.6% in women

[1]. In

Asians it ranges from approximately 3% to 15%, isnearly non-existent (less than 5%) in Africans

[2,3], and

ranges from 4.21% to 11% in China[4]

. The prevalence

of gallstone disease is also high in some ethnic groups,

e.g. 73% in Pima Indian women; 29.5% and 64.1%of American Indian men and women, respectively;

and 8.9% and 26.7% of Mexican American men and

women, respectively[1,5,6]

. From a medical economicperspective, gallstone disease is the most common

reason for hospitalization and creates a high burden

in the United States[7]

and other Western countries[8]

.Many recent studies have shown that gallstone disease

is related to age, sex, and metabolic disorders, such asobesity, dyslipidemia (hypertriglyceridemia), and type 2diabetes

[9-11]. The pathogenesis of gallstone disease is

Online Submissions: wjg.wjgnet.com World J Gastroenterol 2009 il 2 : 9il 2 : 92 : [email protected] World Journal of Gastroenterology ISSN 0079327doi:0.374/wjg.. 2009 The WJG Pess and Baishideng. ll ights eseved.


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Sun H et al. Gender and metabolic differences of gallstone disease 1887

environmental factors[12,13].Because of an increase in the Westernization of

dietary habits and a decrease in physical activity, theprevalence of gallstone disease has increased in theChinese population in recent years. From a public

health standpoint, it is not only important to study thebackground prevalence of gallstone disease regionally,but to also explore the demographic and biologicalmarkers related to the development of gallstonedisease. Meanwhile, gallstone disease can result inserious outcomes, such as acute gallstone pancreatitisand gallbladder cancer. If we can predict which factorscontribute to the development of gallstone disease, wecan prevent it by controlling these factors. The presentstudy was designed to explore the potential risk factorsfor gallstone disease and to improve the understandingof the overall pathogenesis of this disease.

MATERIALS AND METHODS

Data resource and data collectionThis study was conducted at the physical examinationcenter of West-China Hospital at Sichuan University.This hospital provides medical care mainly for middle-and high-income individuals from Chengdu City and thesurrounding metropolitan areas. Our sample populationconsisted of consecutive subjects who were referred tothe physical examination center by their companies asan annual requirement. Data collection, including age,sex, demographic data, history of systemic diseases

and gastrointestinal surgery, and a complete physicalexamination were done by the doctors at the physicalexamination center. Ultrasonography of the abdomenwas conducted by ultrasonographers using a scannerequipped with a 3.5-MHz transducer (Philips MedicalSystems, Bothell, USA). Blood samples were drawn via venipuncture from the study participants, after theyhad fasted overnight, by clinical nurses for laboratoryexamination. Fasting plasma glucose (FPG), triglyceride,total cholesterol, high-density-lipoprotein cholesterol(HDL-C), and low-density-lipoprotein cholesterol(LDL-C) concentrations were measured using Hitachi

Modular analyze system (Roche Modular DPP, HitachiLtd, Tokyo, Japan).

Diagnosis criteriaGallstone disease was dened as the presence of strongintraluminal echoes that were gravity-dependent or thatattenuated ultrasound transmission (acoustic shadowing)during abdominal ultrasonography or as a history ofcholecystectomy because of gallstone disease.

Obesity was defined as a body mass index (BMI) 25 kg/m

2 in both men and women according to theredened World Health Organization criteria for the AsiaPacic Region[14]. High blood pressure was dened as a

systolic blood pressure (SBP) 140 mmHg or a diastolicblood pressure (DBP) 90 mmHg or a history ofhypertension Subjects with an FPG 1260 mg/L and/or

triglyceride concentration 1500 mg/L. Low HDL-Cwas dened as an HDL-C level < 350 mg/L in men or< 390 mg/L in women. Hypercholesterolemia wasdened as a total cholesterol level 2200 mg/L. HighLDL-C was dened as an LDL-C level 1550 mg/L.

Statistical analysisCategorical data are presented as the number of casesand percentages. Statistical analysis was performed usingSPSS software (SPSS Inc., Chicago, IL). Odds ratios

(ORs) were calculated with the variables coded in amultivariate form. Pearsons Chi-square or Fishers exacttests were used for categorical variables. Multiple logisticregression analysis was performed to investigate theindependent factors associated with gallstone disease.In all cases, tests of signicance were 2-tailed, P < 0.05indicated statistical signicance.

RESULTS

A total of 3573 subjects undergoing an annual healthexamination from January to December 2007 wereincluded: 1825 men and 1748 women. The prevalenceof gallstone disease among the study subjects was 10.7%(384/3573): 9.9% in men and 11.6% in women. Theresults of univariate analysis of individual factors and

Table 1 OR of individual risk factors and their association

with gallstone disease

Risk factors n Gallstone (%) OR 95% CI

Sex

Men /2 9.9 .00

Women 203/74 . .9 0.97.4

ge y

39 9/22 . .00

404 22/9 3.3 2. 2.03.42

9/2 27.0 .3 4.49.0

BMI

< 2.0 kg/m2 2/24 9.9 .00

2.0 kg/m2

03/732 4. .49 .7.90

Hyetension

No 29/2933 9.2 .00

Yes /40 .0 2.7 .72.7

FPG

< 00 mg/L 34/347 0.0 .00

00 mg/L and

< 20 mg/L

4/0 23.3 2.7 .49.0

20 mg/L 29/9 30.2 3.90 2.49.2

Tiglyceide

< 00 mg/L 20/244 .4 .00

00 mg/L 7/2 . 2.04 .42.2

HDL

< 30 mg/L men

< 390 mg/L women

2/33 9. .00

30 mg/L men

390 mg/L women

3/3440 0.4 0.4 0.30.74

Total cholesteol

< 2200 mg/L 343/3323 0.3 .00

2200 mg/L 4/20 .4 .70 .202.43

LDL

< 0 mg/L 30/3429 0. .00

0 mg/L 24/44 .7 .7 .092.


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associated with gallstone disease were an age of40-64 years and an age 65 years, a BMI 25.0 kg/m2,high blood pressure, an FPG level between 1100 and1260 mg/L, an FPG level 1260 mg/L, a triglyceride level 1500 mg/L, a total cholesterol level 2200 mg/L, andan LDL level 1550 mg/L (P < 0.05). In contrast, alow HDL-C level was inversely associated with gallstonedisease (P < 0.05). As shown in Table 1, the prevalenceof gallstone disease for each metabolic disorder was14.1% for obesity, 18.0% for hypertension, 30.2% forDM, 15.8% for hypertriglyceridemia, and 10.4% for alow HDL-C level.

In order to identify the risk factors, we furtherperformed a multivariate logistic regression analysis(backward stepping); the results are shown in Table 2.Women aged 40-64 years and 65 years, with an FPGlevel 1260 mg/L, and a triglyceride level 1500 mg/Lwere positively correlated with gallstone disease.

The incidence of metabolic disorders in the groupswith and without gallstone disease is shown in Table 3.Obesity, hypertension, DM, hypertriglyceridemia, a lowHDL-C level, and hypercholesterolemia were foundin 26.8%, 29.9%, 7.6%, 46.4%, 6.8%, and 10.7% ofsubjects with gallstone disease, respectively. In the group without gallstone disease, the incidences of obesity,

hypertension, DM, hypertriglyceridemia, a low HDL-Clevel, and hypercholesterolemia were 19.7%, 16.5%, 2.1%,29.8%, 3.4%, and 6.6%, respectively. The incidences ofall metabolic disorders were higher in the group withgallstone disease than in the group without gallstonedisease (P< 0.01).

The results of univariate analysis of metabolicfactors and their association with gallstone disease indifferent sexes are shown in Table 4. In men, the factorssignificantly associated with gallstone disease werehigh blood pressure, an FPG level between 1100 and1260 mg/L, an FPG level 1260 mg/L, and a triglyceride

level 1500 mg/L (P < 0.05). In women, the factorssignificantly associated with gallstone disease werea BMI 25.0 kg/m

2, high blood pressure, an FPG

cholesterol level 2200 mg/L, and an LDL-C level 1550 mg/L (P< 0.05). A low HDL-C level was inverselyassociated with gallstone disease only in women (P< 0.05).

To control the covariates simultaneously, multivariatelogistic regression analysis (backward stepping) was

performed (Table 5). The analysis revealed that anFPG level 1260 mg/L was a signicant independentpredictor of gallstone disease in men (P = 0.005) and aBMI 25.0 kg/m

2and a triglyceride level 1500 mg/L

were predictors of gallstone disease in women (P< 0.05).

DISCUSSION

One of the important benefits of early screening forgallstone disease is that ultrasonography can detectasymptomatic cases, which results in early treatmentand the prevention of serious outcomes such asacute gallstone pancreatitis and gallbladder cancer[15].

However, few reports on the prevalence and possibleetiology of gallstone disease have been published inChina. In the present study, gallstone disease appearedto be common in the test population, i.e. an estimated10.7% of the test population in Chengdu, China, hadgallstone disease. The reported prevalence of gallstonedisease is approximately 3.6% in Japan and 4.3%-5.0%in Taiwan[16-18]. The apparently higher prevalence rate inour study may have been due to the Westernized lifestyleof our patients, who were of middle-to-high incomeclass. Another possible reason for such differences hasbeen related to the fact that this was a hospital-based

study which was unlikely the population study that couldrepresent the general population.The present study, in accordance with reports from

Western countries and other regions of Asia, showedthat an older age is a signicant risk factor for gallstonedisease

[16,18,19]. In contrast, gallstone disease is virtually

absent in children and adolescents aged 8-19 years[20].Long-term exposure to many risk factors, as is true forthe elderly, may increase the risk of gallstone disease. Atthe same time, sedentary activity, which is greater in theelderly than in younger populations, may also increasethe risk of gallstone disease

[21,22]. Furthermore, gallstone

disease is also an acquired disease inuenced by chronic

environmental factors plus an aging effect[23].In concordance with the findings of previous

studies, female sex was also a major risk factor forgallstone disease in the present study. The commonlyperceived opinion that women are at greater risk ofdeveloping gallstone disease than men may largely bedue to extraneous risk factors, such as pregnancy and sexhormones. The number of pregnancies is the main onerelated to the high rates of gallstone disease in women.Sex hormones are most likely to be responsible for theincreased risk. Estrogen increases biliary cholesterolsecretion causing cholesterol super saturation of bile.

Thus, hormone replacement therapy in postmenopausalwomen has been described to be associated with anincreased risk for gallstone disease [24,25]. Some studies

Table 2 Multivariate logistic regression analysis for gallstone

disease

Variables OR 95% CI P

Female sex .70 .32. < 0.00

ge y

40 to 4 2.44 .3.7 < 0.00

.3 4.02.44 < 0.00

FBG 20 mg/L 2.2 .33.43 0.002

Tiglyceides 00 mg/L .7 .32.3 < 0.00

The deendent vaiable was the esence o absence of gallstone disease.

The covaiates included sex, age of 404 and yeas, BMI 2.0 kg/m2,

high blood essue SBP 40 mmHg o DBP 90 mmHg o a histoy of

hyetension, an FPG level between 00 and 20 mg/L and 20 mg/L,

a tiglyceide level 00 mg/L, an HDL level 30 mg/L in men o

390 mg/L in women, a total cholesteol level 2200 mg/L, and an LDL

level 0 mg/L.

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Previous population studies have reported inconsistentassociations of DM with gallstone disease. A study inRome showed that DM was associated with an increasedrisk of gallstone disease in men and women separately

[28].

A study of Hispanic Americans found a positive

association between DM and self-reported gallstonedisease in women, but not in men

[26]. A study in Italy

failed to find any relation between DM and gallstone

and gallstone disease in men, but not in women. The

mechanism underlying the relation of DM with gallstone

disease may be fasting hyperinsulinemia, which canoverly activate the rate-limiting enzyme for cholesterol

synthesis[30]

and nally leads to cholesterol saturation in

the bile. Reduced motility of the gallbladder in personswith diabetes is another possible explanation

[31,32].

In our study, obesity only showed a positive

association with gallstone disease in women. Previousstudies have found disparate ndings for BMI or relative

weight in men with gallstone disease[29,33,34]. However,

three population screening surveys using ultrasonographyfailed to find a positive association between BMI and

gallstone disease in men in Italy, Denmark, and the

United States[26,35,36]

, whereas all three showed a positiveassociation in women. The discrepant ndings for BMI in

men with gallstone disease have not been fully explained.

A possible reason for these ndings may be that BMI isnot a suitable standard of obesity in men. Waist-to-hip

ratio may be a better measure of obesity. The mechanism

responsible for the increased risk of gallstone diseasein obese persons may be the increase in bile saturation

that results from an increase in the biliary secretion ofcholesterol, which likely depends on the higher synthesisrate of cholesterol in obese persons

[23]

Table 3 Prevalence of metabolic disorders in the subjects with and without gallstone disease n (%)

Metabolic disorders Gallstone disease No gallstone disease c2

P

Obesity 03/34 2. 29/39 9.7 0.03 0.00

Hyetension /34 29.9 2/39 . 42.37 < 0.00

Diabetes mellitus 29/34 7. 7/39 2. 40.0 < 0.00

Hyetiglyceidemia 7/34 4.4 90/39 29. 43.29 < 0.00

Low HDLC 2/34 . 07/39 3.4 .7 0.00

Hyecholesteolemia 4/34 0.7 209/39 . .94 0.003

Table 4 Univariate analysis of metabolic risk factors for gallstone disease in gender

Risk factors Men Women

n Gallstone

disease (%)

OR 95% CI n Gallstone

disease (%)

OR 95% CI

BMI

< 2 kg/m2 3/23 9. .00 - /0 0. .00

2 kg/m2

/90 . .29 0.94.7 3/42 24. 2.0 .4.24

HyetensionNo 20/39 . .00 49/42 9.7 .00

Yes /434 4.4 .73 .22.4 4/20 2.2 3.32 2.334.73

FPG

< 00 mg/L 2/70 .9 .00 9/707 . .00

00 mg/L and < 20 mg/L /47 23.4 3.3 ..2 3/3 23. 2.4 0..3

20 mg/L / 2. 3.9 2.0.49 /2 39.3 .20 2.40.2

Tiglyceide

< 00 mg/L 79/02 7. .00 27/433 .9 .00

00 mg/L 02/3 2. .9 .242.3 7/3 24. 3.27 2.34.49

HDL

< 30 mg/L men < 390 mg/L women 7/73 9. .00 9/702 .2 .00

30 mg/L men 390 mg/L women 4/7 . .0 0.993.27 2/4 2. 2.79 .42.4

Total cholesteol

< 2200 mg/L 3/2 9.7 .00 0/4 .0 .00

2200 mg/L /43 2. .34 0.02.2 23/07 2. 2.22 .373.2

Table 5 Multivariate logistic regression analysis for gallstone

disease in gender

Variables Men Women

OR 95% CI OR 95% CI

BMI 2.0 kg/m2

- .9 .02.0

P = 0.04

FBG 20 mg/L 2.30 .24.2

P = 0.00

Tiglyceide

00 mg/L

.37 0.99.90

P = 0.07

2.7 .43.07

P < 0.00

The deendent vaiable was the esence o absence of gallstone disease.

The covaiates included a BMI 2.0 kg/m2, high blood essue SBP

40 mmHg o DBP 90 mmHg o a histoy of hyetension, an FPG

level between 00 and 20 mg/L and 20 mg/L, a tiglyceide level

00 mg/L, a low HDL level men: 30 mg/L women: 390 mg/L,

and a total cholesteol level 2200 mg/L.



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However, high total cholesterol, low HDL-C, and highLDL-C levels were negatively associated with the risk ofgallstone disease in both men and women. The presentnding is different from that of previous studies, which

noted a positive relation between hypertriglyceridemia

and gallstone disease

[36]

. However, a cross-sectionalstudy in Denmark failed to nd a signicant associationbetween gallstone disease and plasma lipid levels(including triglyceride, total cholesterol, HDL-C, andLDL-C)[37]. Further studies are needed to clarify whetherelevated levels of plasma lipids are independent riskfactors for gallstone disease.

A major limitation of the present study was thepotential self-selection bias due to the hospital-basedstudy design, which resulted in a sample that was notrepresentative of the general population in westernChina. However, we believe that our findings areuseful as background data for future studies of theepidemiology of gallstone disease in China. Second, ourmeasurements were inadequate. Some factors that mightplay an important role in gallstone disease development,such as oral contraceptive use and waist-to-hip ratio, were not collected in detail. Third, measurement errorand different pathogenicities may have occurred, becausethe measurements were only made at one time point.Therefore, future studies need to determine whetherthese factors affect the results of our study.

In conclusion, older age, and female sex are associatedwith the prevalence of gallstone disease in both men andwomen. Obesity and hypertriglyceridemia were positively

associated with gallstone disease in women, but not inmen, whereas DM (FPG 1260 mg/L) was positivelyassociated with gallstone disease only in men.

COMMENTS

BackgroundGallstone disease is one of the most prevalent gastrointestinal diseases with

a substantial burden to health care systems. Because the pathogenesis of

gallstone disease is still not well defined and strategies for prevention and

efcient non-surgical therapies are missing, further studies are required. Many

researchers have shown that gallstone disease is related to age, sex, and

metabolic disorders, such as obesity, dyslipidemia (hypertriglyceridemia), and

type 2 diabetes. However, the findings concerning metabolic disorders andgallstone disease are disparate in different regions and ethnicity.

Research frontiersThere are a cluster of metabolic syndromes which includes obesity, glucose

intolerance, increased low-density-lipoprotein cholesterol, triacylglycerol,

diminished high-density-lipoprotein cholesterol and hypertension. The number of

gallstone patients is increasing with a high prevalence of metabolic syndrome.

Innovations and breakthroughsThis study confirmed that age and sex are positive risk factors for gallstone

disease; but, the association between metabolic disorders and gallstone

disease is different for men and women. Furthermore, the study complemented

the background prevalence of gallstone disease in Chengdu, China.

ApplicationsThe results of this paper can guide clinicians to target high-risk groups for

related inspection and early treatment. Furthermore, preventive strategies can

be identied and planned according to these results.

TerminologyGallstone disease formally known as cholelithiasis occurs when gallstones

in most patients. Sometimes it can cause dyspepsia and other gastrointestinal

symptoms or biliary colic or Mirizzi syndrome.

Peer reviewThis paper provides information about the incidence and risk factors of

gallstone disease in China. The results of this study can give information for

further research to explore the pathogenesis of gallstone disease and the role

of metabolic syndrome in the process of gallstone formation.

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S- Editor Li LF L- Editor Ma JY E- Editor Zheng XM



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Gender and Metabolic Differences of Gallstone Diseases

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