Preventive Medicine 65 (2014) 13–22

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Review

Body mass index and biliary tract disease: A systematic review and meta-analysis of prospective studies Myungsook Park a, Da Young Song b, Youjin Je c, Jung Eun Lee a,⁎ a b c

Department of Food and Nutrition, Sookmyung Women's University, Seoul 140-742, Republic of Korea Division of Cancer Prevention, National Cancer Control Institute, National Cancer Center, 323 Ilsan-ro, Ilsandong-gu, Goyang-si, Gyeounggi-do 410-769, Republic of Korea Department of Food and Nutrition, Kyung Hee University, Seoul 130-701, Republic of Korea

a r t i c l e

i n f o

a b s t r a c t Objective. To evaluate the association between body mass index (BMI, kg/m2) and incidence of biliary tract disease. Methods. We performed a systematic review and a meta-analysis of prospective studies by searching the database of PubMed and EMBASE published up to December 31, 2013. Outcome of interest was disease of biliary tract system (gallbladder, extrahepatic bile duct and Ampullar of Vater). We used a random-effects model to combine the study-specific relative risks (RRs) and 95% confidence intervals (95% CIs) from 22 prospective studies. We examined whether BMI was associated with a higher risk of biliary tract disease in a combined analysis. Results. The positive association was stronger for non-cancer biliary tract disease than biliary tract cancer; combined RRs (95% CIs) comparing the top with bottom categories were 1.40 (1.15–1.65) for biliary tract cancer and 2.75 (2.35–3.15) for non-cancer biliary tract disease (P for difference b 0.001). For non-cancer biliary tract disease, combined RRs (95% CIs) comparing the top with bottom categories were 3.21 (2.48–3.93) for women and 2.01 (1.66–2.37) for men (P for difference = 0.04). Conclusion. Obesity is associated with higher risks of biliary tract cancer and, to a greater extent, non-cancer biliary tract disease. © 2014 Elsevier Inc. All rights reserved.

Available online 8 April 2014 Keywords: Obesity Body mass index Biliary tract diseases Biliary tract neoplasms Gallbladder Neoplasms Cholelithiasis Cholecystitis

Contents Introduction . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . Search strategy . . . . . . . . . . . Selection criteria . . . . . . . . . . . Data extraction and quality assessment . Statistical analysis . . . . . . . . . . Supplemental analysis . . . . . . . . Results . . . . . . . . . . . . . . . . . Study selection . . . . . . . . . . . Study characteristics . . . . . . . . . Meta-analysis . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . Study limitations and strengths . . . . Conclusions . . . . . . . . . . . . . . . Conflict of interest statement . . . . . . . Acknowledgment . . . . . . . . . . . . Appendix A. Supplementary data . . . . References . . . . . . . . . . . . . . .

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⁎ Corresponding author. Fax: +82 2 710 9479. E-mail addresses: [email protected] (M. Park), [email protected] (D.Y. Song), [email protected] (Y. Je), [email protected] (J.E. Lee).

http://dx.doi.org/10.1016/j.ypmed.2014.03.027 0091-7435/© 2014 Elsevier Inc. All rights reserved.

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14

M. Park et al. / Preventive Medicine 65 (2014) 13–22

Introduction Obesity has been increasing worldwide (WHO, 2000) and its relationship with mortality and chronic diseases has been well established (Calle et al., 2003; Chan et al., 1994; Kivipelto et al., 2005; Ogden et al., 2007; Poirier et al., 2006). Biliary tract diseases including gallbladder cancer, extrahepatic bile duct cancer, cancer for Ampullar of Vater, cholelithiasis (presence of gallstones), cholecystitis and cholangitis may be directly linked with body fatness possibly through increases in inflammation, insulin resistance and insulin-like growth factor levels, oxidative stress, cholesterol levels, and adipokine levels. Biliary tract cancer has poor prognosis (Carriaga and Henson, 1995) and a relatively low 5-year survival rate (b20%) (Everhart and Ruhl, 2009; Gatta et al., 2011; Jung et al., 2013). Non-cancer biliary tract disease is common and places economic burden (Everhart and Ruhl, 2009; Kortt et al., 1998; Shaffer, 2006; Wolf and Colditz, 1998) in developed countries. Also, the presences of cholecystitis and gallstones are established risk factors of gallbladder cancer (Wistuba and Gazdar, 2004). Biliary tract cancer is relatively rare in most parts of Europe and USA (Randi et al., 2006), but highly incident in some populations of Andean area, North American Indians, India, parts of Europe such as Poland, Czech Republic, and Slovakia and East Asia (Lazcano-Ponce et al., 2001). Gallstones, on the other hand, are common in most of Europe and USA and relatively uncommon in African and Asian countries (Yoo and Lee, 2009). This discrepancy may be explained by the dissimilarity in the distribution of risk factors, including obesity, smoking status, alcohol consumption, virus infection, and history of diabetes. Obesity has been shown to increase the risk of gallbladder cancer (Bergstrom et al., 2001; Larsson and Wolk, 2007; Renehan et al., 2008) and some non-cancer biliary tract diseases (Guh et al., 2009; Liu et al., 2008a; Williams, 2008). There was inconsistent longitudinal evidence supporting the hypothesis that obesity plays an important role in the progression of total biliary tract cancer (Ishiguro et al., 2008; Schlesinger et al., 2013). However, the magnitude of the association of biliary tract cancer may differ from that of non-cancer biliary tract disease given the geographic difference in incidence rates. The evidence of gender or ethnicity-difference in the association between BMI and risk of biliary tract disease is not conclusive, partly because of the insufficient sample size in individual studies. Therefore, to assess quantitatively the association between obesity and diseases of biliary tract system (gallbladder, extrahepatic bile duct and Ampullar of Vater) and to examine how the association may differ according to sex and geographic regions, we systematically reviewed and conducted a meta-analysis of prospective cohort studies which examined the associations between BMI and biliary tract cancer and other biliary tract diseases. Methods Search strategy We identified prospective studies examining the association between BMI and biliary tract diseases by searching the database of PubMed and EMBASE (including MEDLINE records) published through December 31, 2013. Two authors (M. Park and D. Y. Song) performed the literature search. We used Medical Subject Heading (MeSH) terms in PubMed and Excerpta Medica Tree (Emtree) in EMBASE. Search terms used included: (1) For PubMed: “obesity, overweight, body mass index, biliary tract neoplasms, bile duct neoplasms, gallbladder neoplasms, and cholangiocarcinoma” for biliary tract cancer; and “obesity, overweight, body mass index, cholelithiasis, choledocholithiasis, gallstones, cholecystitis gallbladder diseases and biliary tract diseases” for non-cancer biliary tract disease; and (2) For EMBASE: “obesity, body mass, gallbladder tumor, biliary tract tumor, and bile duct tumor” for biliary tract cancer; and “obesity, body mass, gallbladder disease, biliary tract disease, cholelithiasis, bile duct stone, gallstone, and biliary tract inflammation” for non-cancer biliary tract disease. The search was restricted to human studies published as full-text manuscript in English-language. In EMBASE, we additionally restricted the study type to prospective study. We also searched the bibliographies of retrieved

papers. This meta-analysis was performed according to the Meta-analysis of Observational Studies in Epidemiology (MOOSE) guidelines (Stroup et al., 2000). We excluded intrahepatic bile duct cancer from biliary tract cancer, because it can be classified as primary liver cancer on the basis of the ICD-10 criteria (WHO, 2010). Selection criteria Eligibility criteria were assessed as follows by two authors (M. Park and J. E. Lee) and selected manuscripts were checked by an independent author (Y. Je); (1) prospective design, published as full-text manuscripts; (2) the main exposure of interest was BMI; (3) the endpoints of interest were biliary tract cancer (cancers of gallbladder, extrahepatic bile duct and Ampullar of Vater) and non-cancer biliary tract disease defined as one of the following conditions — cholelithiasis (gallstones), bile duct stone, choledocholithiasis, and cholecystitis; and (4) relative risks (RRs) with 95% confidence intervals (CIs) for every category of BMI or per unit increase in BMI were reported. When there were multiple publications that covered the same study population (Ko et al., 2000, 2005; Misciagna et al., 1999, 2000; Oh et al., 2005; Robsahm and Tretli, 1999; Song et al., 2008; Stampfer et al., 1992; Syngal et al., 1999), we only included the study with a larger sample size. Data extraction and quality assessment We abstracted from each publication the data (Tables 1A, 1B). Two authors (M. Park and Y. Je) independently assessed the quality of each study using the Newcastle–Ottawa Scale (Wells et al., 2011). Disagreements of more than 1 score by both authors were resolved by consensus. Statistical analysis We used a random-effects model to combine RRs and 95% CIs reported in each study (DerSimonian and Laird, 1986). We also extracted the RRs and 95% CIs for BMI categories or per unit change in BMI. When there were one or more RR values for the same exposure within a manuscript, we selected the most adjusted RRs for potential confounders or estimates from more segmented categories. When 95% CIs were not reported, but there were numbers of cases and person-time for BMI categories, we calculated the standard error and 95% CIs using the number of sample and reported relative risk and unified unit of BMI in kg/m2 (Layde et al., 1982). We estimated the RR per 5 kg/m2 increase in BMI by regressing the natural log RRs using the method described by (Greenland and Longnecker (1992)_) and Orsini (Orsini et al., 2012) to assess the dose–response relationship between BMI and biliary tract disease. For this analysis, we assigned the midpoint of the upper and lower levels in each category to a corresponding relative risk estimate. When the lowest or highest category was open-ended, we considered it at the same amplitude as the neighborhood categories. Studies that reported RRs for three or more categories of BMI were included in the dose–response analysis. We performed subgroup analyses and meta-regression analyses to assess potential sources of heterogeneity by gender (men or women), type of endpoint (biliary tract cancer or non-cancer biliary tract disease), follow-up duration (≥10 years or b10 years), site of cancer (only gallbladder or gallbladder and other biliary tract), geographic location (Western or Asian population), assessment type of weight and height [self-report or others (direct measurement or data linkage)], ascertainment method of outcomes [self-report or others (data review, data linkage or physician diagnosis)], adjustment for covariates (alcohol consumption, cigarette smoking or parity for women) and the Newcastle–Ottawa Scale (≤5 scores or N5 scores). For subgroup analysis by site of cancer, we calculated summary RRs and 95% CIs comparing top category with bottom category of BMI. If only continuous estimate was available (Schlesinger et al., 2013), we estimated the relevant interval by subtracting the median value in the bottom category from the median value in the top category. We also conducted stratified analysis according to the cutoff for the highest BMI category in non-cancer biliary tract disease because the top category of BMI varied across the studies. The statistical significance of heterogeneity among studies was tested by using the I2 statistic (Higgins et al., 2003). We performed sensitivity analyses to examine the influence of individual studies by creating a sensitivity plot using metaninf command, which sequentially omitted one study at a time. We investigated whether there was any individual study that produced heterogeneity in a meta-analysis using metaregression, such as a study of pregnant women in nested case–control study

Table 1A Characteristics of prospective studies included in meta-analysis of association between BMI and biliary tract cancer. Author (year)

Country (study population)

End point

Sex No. of case/ at risk

BMI category (kg/m2)

Relative Risk (95% CI)

Schlesinger et al. (2013) 9 countries of Europe (EPIC)

1992–2010 mean: 8.6 years

EBDSC (=BTC; includes GBC)

C

210/359,290

Tertile median M/W T1:23.3/21.4 T2:26.3/24.7 T3:29.9/29.6

Combined men and women T1: 1.00 (reference) T2: 1.21 (0.84–1.74) T3: 1.26 (0.87–1.83)

Jee et al. (2008)

Korea (KCPS)

1992–2006 Mean: 10.8 years

GBC

M W

Japan (JPHC)

1990–2004 mean: 10.9 years

BTC (GBC and EBDC)

M W C

b20.0 20.0–22.9 23.0–24.9 25.0–29.9 ≥30.0 mean: 23.2 (M) 23.2 (W) 129/48,681 (M) ≤22.9 23.0–24.9 106/53,187 25.0–26.9 (W) ≥27.0

Ishiguro et al. (2008)

Máchová et al. (2007)a

Czech Republic (District Sumperk)

1987–2002

GBC

M W

Samanic et al. (2006)

Sweden

1971–1999 mean: 19 years

GBC

M

Case/control 14/16,996 (M) 79/20,776 (W) 109/362,552

Kuriyama et al. (2005)

Japan (Miyagi Prefecture)

1984–1992

GBC

M W

9/12,485 (M) 24/15,054 (W)

Engeland et al. (2005)

Norway (the national tuberculosisscreening program)

1963–2001 mean: 23 years

GBC

M W

628/962,901 (M) 1087/ 1,037,077 (W)

2276/ 70,556 (M) 1062/443,273 (W)

Men

Women

BMI Case ascertainment determination

Adjustment for confounders

NOS scale

Direct measurement

1) Record linkage with regional cancer registry at 6 countries 2) Combination of record linkage for health insurance and cancer and pathology registries together with an active follow-up at 3 countries Confirmation by using the report of national cancer registry or a hospital admission

Age at recruitment, sex, center, education, smoking status, and alcohol consumption

8

Age at enrollment and smoking status

9

Age at baseline, study area, past history of cholelithiasis, diabetes mellitus, smoking status, and ethanol consumption Age, smoking, hypertension and height

8

0.80 (0.68– 0.94) 0.86 (0.77– 0.96) 1.00 (reference) 0.97 (0.86–1.10) 1.65 (1.11–2.44)

0.97 (0.78–1.21) 1.12 (0.90–1.41) 1.00 (reference) 1.27 (1.02–2.12) 1.44 (0.98–2.12)

Direct measurement

1.00 (reference) 1.09 (0.71–1.68) 1.14 (0.68–1.92) 1.62 (0.93–2.84)

1.00 (reference) 0.85 (0.51–1.41) 0.98 (0.56–1.71) 1.19 (0.69–2.04)

Self-report

Active notification from the hospitals and linkage with population-based cancer registries

Direct measurement

Linkage to the national cancer registry

Direct measurement

Linkage to the populationbased Swedish cancer registry

18.5–25 25–30 ≥30 b25 25.0–29.9 N30.0 mean: 24.1 18.5–24.9 25.0–27.4 27.5–29.9 ≥30.0

1.00 (reference) 1.00 (reference) 1.01 (0.24–4.32) 1.07 (0.58–1.95) 0.76 (0.08–7.41) 0.73 (0.36–1.50) 1.00 (reference) 0.93 (0.62–1.39) 1.40 (0.73–2.70) 1.00 (reference) 0.46 (0.05–3.93) Non-case Non-case

1.00 (reference) 0.83 (0.23–2.98) 3.43 (1.19–9.94) 4.45 (1.39– 14.23)

Self-report

Linkage with the records of the Miyagi prefectural cancer registry

b18.5 18.5–24.9 25.0–29.9 ≥30.0

0.31 (0.04– 2.24) 1.00 (reference) 1.00 (0.84–1.17) 1.38 (1.01–1.89)

1.02 (0.54–1.91) 1.00 (reference) 1.27 (1.10–1.47) 1.88 (1.60–2.21)

Direct measurement

Linkage to the cancer registry of Norway

8

Age group (10-year intervals) 7 and calendar year (5-year intervals), and smoking status 7 Age, smoking status, alcohol drinking status, consumption of meat, fish, fruits, green or yellow vegetables, and beanpaste soup, and type of health insurance (menopausal status, age at menarche and age at end of first pregnancy for women, additionally) Age at measurement and 8 birth cohort

M. Park et al. / Preventive Medicine 65 (2014) 13–22

Follow-up years

Abbreviations: BMI, body mass index; CI, confidence interval; NA, data not applicable in this manuscript; M, men; W, women; C, combined gender; BTC, biliary tract caner; GBC, gallbladder cancer; EBDSC, extrahepatic bile duct system cancer; EBDC, extrahepatic bile duct cancer; NOS scale, the Newcastle–Ottawa Scale for assessing the quality of nonrandomized studies in meta-analyses (range, 1–9 stars). a Nested case–control study. 15

16

Table 1B Characteristics of prospective studies included in meta-analysis of associations between BMI and non-cancer biliary tract diseases. BMI category (kg/m2)

Relative risk (95% CI) Men

Women

M W

95/11,188 (M) 201/13,075 (W)

1.00 (reference) 2.31 (1.35–3.97) 2.12 (1.03–4.37) 2.62 (0.60– 11.42)

GBD (cholelithiasis, cholecystitis or chelocystectomy)

W

24,953/ 1,282,547

b25 25–b30 30–b35 ≥35 mean: 27.5 (M) 28 (W) b18.5 18.5–24.9 25.0–29.9 30.0–39.9 ≥40.0

A year for each person (pregnant duration +4–6 weeks postpartum)

GSD (sludge or stones)

W

Case/control 205/443

b25.0 25.0–29.9 ≥30.0 mean: 26.9 (case)

Sweden (Swedish twin study)

c1:1970–2002 c2:1974–2002

GSD (symptomatic)

C

1398/45,648

18.5–24.9 25.0–29.9 ≥30.0

González-Perez and García Rodriguez (2007)a

United Kingdom

1996 mean: 0.9 years

GSD (symptomatic or cholecystectomy)

C

Case/control

b20 1895/7445 20–24 25–29 ≥30

Combined men and women 1.00 (reference) 1.86 (1.52–2.28) 3.38 (2.28–5.02) Combined men and women 0.68 (0.51–0.91) 1.00 (reference) 1.80 (1.58–2.05) 2.52 (2.18–2.91)

Tsai et al. (2004)

United States (HPFS)

1986–1998

GSD (symptomatic or cholecystectomy)

M

1093/29,847

b22.2 22.2–b23.3 23.3–b24.1 24.1–b25.0 25.0–b25.8 25.8–b26.7 26.7–b28.5 ≥28.5

1.00 (reference) 1.24 (0.92–1.67) 1.32 (0.97–1.79) 1.03 (0.75–1.42) 1.21 (0.88–1.67) 1.07 (0.77–1.48) 1.22 (0.88–1.71) 1.29 (0.91–1.85)

Boland et al. (2002)

United States (ARIC)

1987–1996 mean: 8.2 years

GBD (cholelithiasis, cholecystitis, or cholecystectomy)

M W

141/5832 (M) 255/6929 (W)

b25 25–29 30–34 35–39 N40

1.00 (reference) 0.83 (0.50–1.30) 0.64 (0.30–1.20) 1.38 (0.60–3.10) 1.23 (0.30–5.40)

Country (study population)

Follow-up years

End point

Banim et al. (2011)

United Kingdom (EPIC-Norfolk)

1993–2007

GSD (symptomatic or cholecystectomy)

Liu et al. (2008a)

England and Scotland (1.3 million women study)

1996–2005 2005 (Eng.), 2003 (Scot.) mean: 6.1 years

Ko et al. (2008)a

United States (parent cohort study)

Katsika et al. (2007)

Sex

BMI Case ascertainment determination

Adjustment for confounders

NOS scale

1.00 (reference) 1.60 (1.14–2.24) 2.57 (1.73–3.89) 3.60 (2.11–6.14)

Direct measurement

Matching with the Norfolk Health Authority's computer records after 18 months

Age, physical activity, and alcohol intake (hormone replacement therapy and parity for women)

7

076 (0.64–0.91) 1.00 (reference) 1.81 (1.75–1.86) 2.56 (2.48–2.65) 2.58 (2.37–2.81)

Self-report

Linkage to hospital admission records and review

8

1.00 (reference) 1.12 (0.72–1.75) 2.17 (1.29–3.66)

Self-report

Diagnosis by physician (ultrasonography)

Self-report

Linkage to Swedish hospital discharge and causes of death registry

Age at recruitment, socioeconomic status, region of recruitment, smoking, alcohol use, parity, use of hormone replacement therapy and history of medical illness HOMA-IR, Hispanic ethnicity, HDL cholesterol at 27– 29 weeks, waist-hip ratio and 2nd and 3rd trimester physical activity Crude

NA

Data review of computer profiles

5

Self-report

Self-report of physiciandiagnosis

Direct measurement

Self-report and hospitalization records

Age, sex, heart failure, hyperlipidemia, stroke, hypertension, ischemic heart disease, osteoarthritis, rheumatoid arthritis, diabetes, alcohol, smoking, prior GI disease and health services utilization Age, weight change during the past 2 years, physical activity, dietary fiber intake, regular use of thiazide diuretics or non-steroidal antiinflammatory drugs, pack-years of smoking, caffeine intake, alcohol intake, total energy intake, and heightadjusted waist circumference Age, race, waist-tohip ratio, multiple metabolic syndrome components, ARIC field center, and hormone replacement therapy (for women only)

1.00 (reference) 1.13 (0.80–1.60) 1.29 (0.90–1.90) 1.53 (0.90–2.60) 1.75 (0.90–3.50)

3

5

6

5

M. Park et al. / Preventive Medicine 65 (2014) 13–22

No. of case/ at risk

Author (year)

United States (Nurses' Health Study I 86–96)

1986–1996

GSD

W

5233/72,724

Sahi et al. (1998)

United States (Harvard Alumni)

1962–1977

GBD

M

268/16,414

Acalovschi et al. (1997)

Romania (longitudinal ultrasound follow-up)

2–6 years mean: 3.95 years

GSD (asymptomatic or symptomatic)

W

16/157

Misciagna et al. (1996)

Italy (Castellana population)

1985–1993

GSD or surgery for gallstone

C

104/1962

Grodstein et al. (1994a)

United States (Nurses' Health Study II 89–91)

1989–1991

GSD (symptomatic or cholecystectomy)

W

399/96,185

b21 21–b23 23–b24 24–b25 25–b27 27–b29 29–b31 31–b32 32–b34 34–b36 ≥36

Kato et al. (1992)

United States (Honolulu Heart Program)

1965–1990

GBD (cholelithiasis or cholecystitis)

M

471/7826

Maclure et al. (1989)

United States (Nurses' Health Study I 80–84)

1980–1984

GSD (symptomatic or cholecystectomy)

W

612/88,837

Layde et al. (1982)

United Kingdom (Oxford/Family Planning Association Contraceptive Study)

1968–1981

GBD (cholelithiasis, cholecystitis or cholecystectomy)

W

227/17,032

b21.65 21.65–23.79 23.80–25.80 N25.80 b20.0 20.0–b20.9 21.0–b21.9 22.0–b22.9 23.0–b23.9 24.0–b24.9 25.0–b26.9 27.0–b28.9 29.0–b31.9 ≥32 Categorizationc b20.0 20.0–22.4 22.5–24.9 25.0–27.4 27.5–29.9 ≥30.0

18.5–21.9 22.0–24.9 25.0–29.9 30.0–34.9 ≥35.0 b22.0 22.0–23.9 24.0–26.9 ≥27.0

Quartile median Q1: 28.2 Q2: 30.4 Q3: 32.8 Q4: 34.0 mean: 31.4 b24.1 24.1–26.7 26.8–29.7 N29.7

1.00 (reference) 1.40 (1.30–1.60) 2.30 (2.10–2.50) 3.20 (2.80–3.50) 3.70 (3.30–4.20) 1.00 (reference) 1.54 (0.94–2.51) 1.84 (1.13–2.99) 2.71 (1.57–4.66)

1.00 (reference) 1.83 (0.34–9.77) 1.05 (0.21–5.33) 2.77 (0.54– 14.15)

Combined men and women 1.00 (reference) 1.38 (0.68–2.79) 1.58 (0.81–3.08) 2.80 (1.50–5.24) 1.00 (reference) 1.30 (0.90–1.80) 1.20 (0.70–1.90) 2.00 (1.30–3.20) 2.80 (1.80–4.30) 2.60 (1.60–4.30) 3.40 (2.00–5.70) 7.20 (1.40– 13.00) 6.50 (3.80–11.00) 6.50 (3.60–12.00) 6.10 (3.60–10.00) 1.00 (reference) 1.10 (0.90–1.50) 1.40 (1.10–1.90) 1.80 (1.40–2.30) 1.00 (reference) 0.80 (0.40–1.40) 0.90 (0.50–1.70) 1.20 (0.70–2.20) 1.10 (0.60–2.10) 1.30 (0.70–2.50) 2.20 (1.10–4.10) 2.60 (1.30–5.10) 3.00 (1.50–6.10) 4.80 (2.40–10.00) 1.00 (reference) 1.05 (0.66–1.67) 1.36 (0.86–2.16) 1.74 (1.03–2.95) 3.26 (1.84–5.78) 5.54 (3.12–9.83)

Self-report

Self-report and confirmed by medical report review

Age, smoking status and race

5

Self-report

Self-report of physician-diagnose

6

NA

Diagnosis by physicians (ultrasonography)

Age, calendar year, BMI, BMI change between college and 1962/1966, smoking habit, and physical activity index Age

6

Direct measurement

Diagnosis by physicians (ultrasonography and cholecystography)

Age, sex

8

Self-report

Self-report of physiciandiagnosis

Age, oral contraceptive use, postmenopausal hormone use, parity, alcohol intake and cigarette smoking

5

Direct measurement

Histologic or radiologic diagnosis by physician

Age

6

Self-report

Self-report of physician-diagnosis

Age, weight change from 1976 to 1980, energy intake, and alcohol intake

4

Self-report

Review hospital admissions by ICD code

Parity, social class, smoking status, age at first term birth, total duration of oral contraceptive use

6

M. Park et al. / Preventive Medicine 65 (2014) 13–22

Field et al. (2001)b

Abbreviations: BMI, body mass index; CI, confidence interval; NA, data not applicable in this manuscript; M, men; W, women; C, combined gender; GSD, gallstone disease; GBD, gallbladder disease; NOS scale, The Newcastle–Ottawa Scale for assessing the quality of nonrandomized studies in meta-analyses (range, 1–9 stars). a Nested case–control study. b We included only Nurses' Health Study in the analysis because the association in the Health Professional Follow-Up Study with a longer follow-up was examined in Tsai et al. (2004). c We converted the unit of quetelet's index from g/cm2 to kg/m2.

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M. Park et al. / Preventive Medicine 65 (2014) 13–22

(Ko et al., 2008) and a study that had few cases in the top category of BMI (Kuriyama et al., 2005). Publication bias was evaluated with Egger's regression asymmetry test (Egger et al., 1997); and P b 0.1 was considered to be statistically significant. All analyses were conducted with STATA statistical software package version 11 (Stata Corp., College Station, TX, USA); except where otherwise specified, P b 0.05 (2-sided) was considered statistically significant. Supplemental analysis To examine the associations for subtypes of cancer including gallbladder cancer, extrahepatic bile duct cancer, and Ampullar of Vater cancer, we performed supplemental analysis. We included nine case–control studies (Ahrens et al., 2007; Alvi et al., 2011; Chow et al., 1994; Grainge et al., 2009; Hsing et al., 2008; Nakadaira et al., 2009; Serra et al., 2002; Strom et al., 1995; Zatonski et al., 1997) (Supplementary Table 1) using the same strategy we used for searching prospective studies of biliary tract cancer. Search terms we used included: (1) For PubMed: “obesity, overweight, body mass index, biliary tract neoplasms, bile duct neoplasms, gallbladder neoplasms, and cholangiocarcinoma” for biliary tract cancer; and (2) For EMBASE: “obesity, body mass, gallbladder tumor, biliary tract tumor, and bile duct tumor” for biliary tract cancer. Also, we searched human studies published as full-text manuscript in Englishlanguage and the bibliographies of retrieved papers. Articles were selected if 1) the main exposure of interest was BMI; 2) the endpoints of interest were biliary tract cancer (cancers of gallbladder, extrahepatic bile duct and Ampullar of Vater); and 3) relative risks (RRs) with 95% confidence intervals (CIs) were reported. We estimated the combined RR comparing top with bottom category and the RR per 5 kg/m2 increase in BMI according to subtypes of biliary tract cancer. When there were multiple publications that covered the same study population, we only included the study with a larger sample size.

relevant studies. The literature search identified 29 articles from two databases after screening the titles, abstracts and methods part. A total of 10 articles were excluded after a review of the full-texts: 9 articles (Ko et al., 2000, 2005; Misciagna et al., 1999, 2000; Oh et al., 2005; Robsahm and Tretli, 1999; Song et al., 2008; Stampfer et al., 1992; Syngal et al., 1999) analyzed data which overlapped with papers included; and 1 article (Williams, 2008) did not report RRs for each BMI category and specific unit of continuous BMI. Three additional studies were identified from the references of the retrieved articles. As a result, 19 cohort studies and 3 nested case–control studies were included. Study characteristics

Results

Tables 1A and 1B present the characteristics of studies included: first author's name, publication year, country, definition of study population, follow-up years, sex, the number of analyzed participants, BMI categories, relative risks for categories of BMI, ascertainment of exposure and outcome, potential confounders controlled in studies, and the Newcastle–Ottawa Scale reflecting study quality. A total of 5733 incident cases of biliary tract cancer and 37,566 incident cases of non-cancer biliary tract disease were included in this meta-analysis. In our metaanalysis, a total of 7 studies for biliary tract cancer (Engeland et al., 2005; Ishiguro et al., 2008; Jee et al., 2008; Kuriyama et al., 2005; Máchová et al., 2007; Samanic et al., 2006; Schlesinger et al., 2013) and 15 studies for non-cancer biliary tract disease (Acalovschi et al., 1997; Banim et al., 2011; Boland et al., 2002; Field et al., 2001; González-Perez and García Rodriguez, 2007; Grodstein et al., 1994a; Kato et al., 1992; Katsika et al., 2007; Ko et al., 2008; Layde et al., 1982; Liu et al., 2008a; Maclure et al., 1989; Misciagna et al., 1996; Sahi et al., 1998; Tsai et al., 2004) were included.

Study selection

Meta-analysis

A total of 788 articles were extracted by search through December 31, 2013. We identified 22 articles which met the inclusion criteria after a full-text review. Fig. 1 shows a flow diagram of the selection of

High BMI was significantly associated with higher risk of biliary tract disease (biliary tract cancer and non-cancer biliary tract disease combined); combined RR (95% CI) comparing the top with bottom category

Fig. 1. Flow diagram of publication selection for inclusion in this meta-analysis.

M. Park et al. / Preventive Medicine 65 (2014) 13–22

3.93) for women in non-cancer biliary tract disease (P for difference by sex = 0.04). The associations for biliary tract cancer or non-cancer biliary tract disease did not differ by site of cancer, geographic region, BMI ascertainment method, outcome ascertainment method, follow-up duration, the Newcastle–Ottawa Scale, or adjustment for smoking, alcohol or parity (Table 2). When we examined whether the association varied by top cut-off of the BMI category in non-cancer biliary tract disease, we found that combined RRs were 3.01 (95% CI = 2.23–3.79) for studies with greater than 30 of BMI in the highest category and 2.29 (95% CI = 1.72–2.87) for studies with 30 or less of BMI in the highest category (P for difference = 0.20). In sensitivity analyses where we omitted one study at a time, one study (only women) (Engeland et al., 2005) for biliary tract cancer and two studies for non-cancer biliary tract disease (Field et al., 2001; Liu et al., 2008a) influenced the overall results. When we excluded those studies in the analysis, heterogeneity decreased, but the results were similar to those in the analysis where we included all the studies. When we estimated the combined RR from both case–control and prospective studies for comparing top with bottom category for subtypes of cancer, there were statistically significant associations of BMI

of BMI was 2.08 (1.73–2.43).We found a stronger association for noncancer biliary tract disease than biliary tract cancer (P for difference b 0.001); combined RRs (95% CIs) were 2.75 (2.35–3.15) for noncancer biliary tract disease and 1.40 (1.15–1.65) for biliary tract cancer (Fig. 2). When we analyzed BMI as a continuous variable by including 28 studies subdivided by sex, combined RRs (95% CIs) for a 5 kg/m2 increment of BMI were 1.11 (1.05–1.17) for biliary tract cancer and 1.40 (1.29–1.51) for non-cancer biliary tract disease (P for difference = 0.003). When publication bias was assessed by evaluating the symmetry of the funnel plot, overall studies were symmetric for non-cancer biliary tract disease (P for Egger's test = 0.60). For biliary tract cancer studies, inclusion of one study (Máchová et al., 2007) was generated to some degree asymmetry (P for Egger's test = 0.09). However, when we analyzed publication bias for all biliary tract cancer studies in a dose–response analysis, there was no statistically significant publication bias (P for Egger's test = 0.61). When we examined whether the association differed by sex, the association for BMI was more pronounced among women than men for non-cancer biliary tract disease (Table 2); combined RRs (95% CIs) comparing the top with bottom category of BMI were 1.44 (1.12–1.76) for men and 1.37 (0.83–1.91) for women for biliary tract cancer (P for difference by sex = 0.74); and 2.01 (1.66–2.37) for men and 3.21 (2.48–

Study

Year

Sex

Population

Biliary tract cancer Schlesinger S 2013 C W A Ishiguro S 2008 M A Ishiguro S 2008 W Jee SH 2008 M A A Jee SH 2008 W W Machova 2007 M W Machova 2007 W Samanic C 2006 M W A Kuriyama S 2005 M A Kuriyama S 2005 W W Engeland A 2005 M W Engeland A 2005 W Subtotal (I−squared = 36.7%, p = 0.097) . Non−cancer biliary tract disease W Banim PJ 2011 M W Banim PJ 2011 W W Liu B 2008 W W Ko CW 2008 W W Katsika D 2007 C Gonzalez−perez A 2007 C W W Tsai CJ 2004 M W Boland LL 2002 M W Boland LL 2002 W W Field AE 2001 W Sahi T 1998 M W W Acalovschi MV 1997 W W Misciagna G 1996 C Grodstien F 1994 W W W Kato I 1992 M W Maclure KM 1989 W W Layde PM 1982 W Subtotal (I−squared = 66.5%, p = 0.000) . Overall (I−squared = 82.4%, p = 0.000)

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Relative Ratio (95% CI)

Endpoint

BTC BTC BTC GBC GBC GBC GBC GBC GBC GBC GBC GBC

1.26 (0.87, 1.83) 1.62 (0.93, 2.84) 1.19 (0.69, 2.04) 1.65 (1.11, 2.44) 1.44 (0.98, 2.12) 0.76 (0.08, 7.41) 0.73 (0.36, 1.50) 1.40 (0.73, 2.70) 0.46 (0.05, 3.93) 4.45 (1.39, 14.23) 1.38 (1.01, 1.89) 1.88 (1.60, 2.21) 1.40 (1.15, 1.65)

GSD GSD GBD GBD GSD GSD GSD GBD GBD GSD GBD GSD GSD GSD GBD GSD GBD

2.62 (0.60, 11.42) 3.60 (2.11, 6.14) 2.58 (2.37, 2.81) 2.17 (1.29, 3.66) 3.38 (2.28, 5.02) 2.52 (2.18, 2.91) 2.30 (1.76, 3.00) 2.02 (0.50, 8.40) 2.48 (1.40, 4.50) 3.70 (3.30, 4.20) 2.71 (1.57, 4.66) 2.77 (0.54, 14.15) 2.80 (1.50, 5.04) 6.10 (3.60, 10.00) 1.80 (1.40, 2.30) 4.80 (2.10, 10.00) 5.54 (3.12, 9.83) 2.75 (2.35, 3.15) 2.08 (1.73, 2.43)

.05

.5

1

1.5

2

3

4

5

Fig. 2. The combined relative risk (95% CI, 95% confidence intervals) of BMI and biliary tract disease, comparing the top with bottom category. The squares represent the study-specific relative risks; the horizontal lines represent 95% confidence intervals. The area of squares reflects the study-specific weights (inverse of the variance). The dash line indicates the combined RR and the diamonds indicate the 95% confidence intervals for the combined RR. BTC = Biliary tract cancer; GBC = Gallbladder cancer; GSD = Gallstone disease; GBD = Gallbladder disease; M = Men; W = Women; C = Combined gender; W = Western population; A = Asian population. P for difference by biliary tract cancer vs. non-cancer biliary tract disease was b0.001.

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M. Park et al. / Preventive Medicine 65 (2014) 13–22

Table 2 Subgroup meta-analysis of the associations of BMI with biliary tract cancer and non-cancer biliary tract disease. Biliary tract cancer

Non-cancer biliary tract disease

No. of studiesa

RR (95% CI)

I2 (%)

Pdifference

No. of studiesa

RR (95% CI)

I2 (%)

Pdifference

Sex Men Women

61–6 51–3,5,6

1.44 (1.12–1.76) 1.37 (0.83–1.91)

0 72.3

0.74

57–11 97,9,12–18

2.01 (1.66–2.37) 3.21 (2.48–3.93)

0 72.1

0.04

Site of cancer Only gallbladder Gallbladder and other biliary tract

121–6,19 32,19

1.39 (1.12–1.65) 1.29 (0.93–1.65)

39.2 0

0.48

Geographic region of study Western Asian

63,4,6,19 61,2,5

1.36 (0.95–1.76) 1.43 (1.10–1.77)

65.3 0

0.72

177–18,20–22 0

BMI ascertainment Self-report Direct measurement

42,5 81,3,4,6,19

1.29 (0.76–1.82) 1.41 (1.12–1.71)

0 52.2

0.89

98,10,12–14,16–18,20 67,9,11,22

3.03 (2.44–3.63) 1.98 (1.57–2.39)

74.2 0

0.17

Outcome ascertainment Self-report Data review/data linkage/diagnosis

0 121–6,19

78–10,14,16,17 107,11–13,15,18,20–22

3.11 (2.24–3.97) 2.47 (2.12–2.82)

67.0 43.9

0.31

Follow-up duration b10 years ≥10 years

35,19 91–4,6

99,12,13,15–17,21,22 87,8,10,11,14,18,20

2.57 (2.39–2.75) 2.96 (2.12–3.80)

82.7 0

0.92

NOS scale ≤5 scores N5 scores

0 121–6,19

89,13,14,16,17,20,21 97,8,10–12,15,18,22

2.65 (1.96–3.35) 2.73 (2.27–3.19)

25.1 81.1

0.22

Adjustment for potential confounders Smoking Yes No Alcohol Yes No Parity (only for women) Yes No

1.23 (0.77–1.70) 1.43 (1.15–1.72)

0 44.9

0.87

101–5,19 26

1.26 (1.02–1.50) 1.66 (1.17–2.14)

0 70.2

0.20

78,10,12,14,16,18,21 107,9,11,13,15,17,20,22

2.92 (2.39–3.44) 2.29 (1.82–2.76)

79.8 8.9

0.36

52,5,19 71,3,4,6

1.27 (0.92–1.63) 1.44 (1.10–1.78)

0 55.6

0.67

77,8,12,16,17,21 109–11,13–15,18,20,22

2.57 (2.29–2.85) 2.82 (2.01–3.62)

22.2 76.9

0.71

47,12,16,18 59,13–15,17

3.88 (2.23–5.53) 3.06 (2.12–3.99)

64.7 47.8

0.43

0 51–3,5,6

Abbreviations: BMI, body mass index; NOS scale, the Newcastle–Ottawa Scale for assessing the quality of nonrandomized studies in meta-analyses. Study included in subgroup analysis: 1, Jee et al. (2008); 2, Ishiguro et al. (2008); 3, Máchová et al. (2007); 4, Samanic et al. (2006); 5, Kuriyama et al. (2005); 6, Engeland et al. (2005); 7, Banim et al. (2011); 8, Tsai et al. (2004); 9, Boland et al. (2002); 10, Sahi et al. (1998); 11, Kato I (1992); 12, Liu et al (2008a); 13, Ko et al. (2008); 14, Field et al. (2001); 15, Acalovschi et al. (1997); 16, Grodstein et al. (1994a); 17, Maclure et al. (1989); 18, Layde et al. (1982); 19, Schlesinger et al. (2013); 20, Katsika et al. (2007); 21, González-Perez and García Rodriguez (2007); 22, Misciagna et al. (1996). a Studies were subdivided by sex.

with gallbladder cancer and extrahepatic bile duct cancer. But the association for Ampullar of Vater cancer was not clear. For a dose–response analysis, the risks of gallbladder cancer and extrahepatic bile duct cancer were elevated with 5 kg/m2 increment in BMI (Supplementary Table 2). Discussion In our meta-analysis of prospective studies that examined the association between BMI and incidence of biliary tract disease, we found that people with high BMI had 1.40 times higher risk of biliary tract cancer and 2.75 times higher risk of non-cancer biliary tract disease compared to those with low BMI. For an increment of 5 kg/m2 of BMI, risk of biliary tract cancer increased by 1.11 and risk of non-cancer biliary tract increased by 1.40. Such risk difference between biliary tract cancer and non-cancer biliary tract disease was statistically significant. The association for non-cancer biliary tract disease was more pronounced for women than men, suggesting the hypothesis that obesity confers greater risk for non-cancer biliary tract diseases such as cholelithiasis and cholecystitis among women than men. We also investigated the association between BMI and subtypes of cancer by including both case–control and prospective studies. Obesity was associated with extrahepatic bile duct cancer and gallbladder cancer, but the association was not clear for Ampullar of Vater. However, inclusion of case–control studies did not rule out the possibility of reverse causation.

A previous meta-analysis of obesity and gallbladder cancer incidence and mortality revealed a RR of 1.66 (95% CI = 1.47–1.88), which is similar to our finding (Larsson and Wolk, 2007). For gallbladder disease, a meta-analysis of 4 prospective studies showed that high BMI was associated with higher risk of gallbladder disease incidence (Guh et al., 2009). We compared the associations between biliary tract cancer and non-cancer biliary tract disease and found that excess body weight was more strongly associated with non-cancer biliary tract disease than biliary tract cancer. Although gallstone disease is a risk factor for gallbladder cancer (Wang et al., 2012), not all gallstones progress to gallbladder cancer and other factors such as viral or bacterial infection, and smoking increase the likelihood of gallbladder cancer development. Therefore, it is of interest whether excess body fat may cause biliary tract cancer through biliary tract system impairments, such as biliary tract inflammation and gallbladder motility decrease or through other mechanisms apart from biliary tract diseases. It warrants further investigation. Although the mechanism through which obesity may increase the risk of biliary tract disease is not well established, there are several possible explanations. Adipose tissues in obese humans secrete macrophages and inflammatory cytokines. Especially, visceral fat increases a secretion of cytokines such as tumor necrosis factor-α (TNF-α), type 1 plasminogen activator inhibitor (PAI-1) and interleukin-6 (IL-6) (Calle and Kaaks, 2004; Jeong and Lee, 2012). Obesity-induced chronic inflammation caused by inflammatory products and oxidative stress may

M. Park et al. / Preventive Medicine 65 (2014) 13–22

contribute to biliary tissue damage and tumor development (van Kruijsdijk et al., 2009). High saturation of bile with cholesterol among obese individuals may lead to cholesterol gallstone formation and subsequently gallbladder cancer development (Everhart, 1993). Obese individuals are likely to have larger gallbladder volume accompanying with slower evacuation of gallbladder (Venneman and van Erpecum, 2010) and mucosal abnormalities (Dittrick et al., 2005; Marzio et al., 1988), both of which are associated with gallstone formation. Because gallbladder and bile duct are necessary for a smooth digest of lipids as repository and pathway of bile acids, a high intake of total calorie (Maclure et al., 1989), carbohydrate (Tsai et al., 2005a,b) and saturated fat (Sichieri et al., 1991) could be related to biliary tract disease. Higher risks of biliary tract diseases with high body fatness among women than men could be partly due to the influence of female hormones and pregnancy on gallbladder. Pregnant women in the late duration were found to have incomplete gallbladder emptying, and thus an increase in residual volume and progression to build up of cholesterol crystals (Braverman et al., 1980). A long duration use of oral contraceptive (Bennion et al., 1976; Grodstein et al., 1994a) and hormone replacement therapy (Grodstein et al., 1994b; Liu et al., 2008b) increased risks of gallstones or cholecystectomy in prospective studies, suggesting a possible interaction of female hormones in relation to biliary tract disease. Study limitations and strengths There are some potential limitations in our meta-analysis. First, noncancer biliary tract disease was ascertained through self-report in six US studies. However, 5 US studies, Nurses' Health Study, Health Professionals Follow-up Study and Harvard Alumni Study showed that selfreported gallbladder disease or cholecystectomy corresponded well with medical records in their validation studies (Field et al., 2001; Grodstein et al., 1994a; Maclure et al., 1989; Sahi et al., 1998; Tsai et al., 2004). Secondly, although 11 studies used self-reported weight and height, six of these studies validated those measures and reported a high correlation of self-reported weight and height with direct measurement (Field et al., 2001; Grodstein et al., 1994a; Ishiguro et al., 2008; Ko et al., 2008; Maclure et al., 1989; Tsai et al., 2004). Thirdly, because prevalent types of gallstones are different between Western population and Asian populations (cholesterol gallstones vs. pigment gallstones, respectively) (Hung et al., 2011; Jeong and Lee, 2012), it is necessary to examine the association separately for Western and Asian population. However, no Asian prospective studies were found for biliary tract disease. Our meta-analysis includes several strengths. We examined both biliary tract cancer and non-cancer biliary tract disease and found that BMI was more strongly associated with non-cancer biliary tract disease than biliary tract cancer. We included only the prospective studies to avoid the reverse causation of weight influencing biliary tract disease. We also conducted subgroup analyses to examine whether the associations varied by disease type, sex, site of cancer, geographical region (only biliary tract cancer), ascertainment of BMI or endpoint, quality of papers and adjustment for risk factors. Conclusions Our meta-analysis findings suggest the evidence that high BMI is a risk factor for both biliary tract cancer and non-cancer biliary tract diseases, and the association was stronger for non-cancer biliary tract disease than biliary tract cancer. The difference in magnitude of the associations may be partly explained by a higher incidence of non-cancer biliary tract disease, with a lower incidence of biliary tract cancer in the Western population compared to Asian countries. Further research is warranted to reveal the attribution of risk factors to biliary tract cancer and non-cancer biliary tract disease and the pathophysiological

21

mechanism through which excess body weight contributes to the development of biliary tract disease. Conflict of interest statement The authors declare no conflict of interest.

Acknowledgment This study was supported by the Sookmyung Women's University Research Grant (2014). Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.ypmed.2014.03.027. References Acalovschi, M.V., Blendea, D., Pascu, M., Georoceanu, A., Badea, R.I., Prelipceanu, M., 1997. Risk of asymptomatic and symptomatic gallstones in moderately obese women: a longitudinal follow-up study. Am. J. Gastroenterol. 92 (1), 127–131. Ahrens, W., Timmer, A., Vyberg, M., et al., 2007. Risk factors for extrahepatic biliary tract carcinoma in men: medical conditions and lifestyle: results from a European multicentre case–control study. Eur. J. Gastroenterol. Hepatol. 19 (8), 623–630. Alvi, A.R., Siddiqui, N.A., Zafar, H., 2011. Risk factors of gallbladder cancer in Karachi—a case–control study. World J. Surg. Oncol. 9, 164. Banim, P.J., Luben, R.N., Bulluck, H., et al., 2011. The aetiology of symptomatic gallstones quantification of the effects of obesity, alcohol and serum lipids on risk. Epidemiological and biomarker data from a UK prospective cohort study (EPIC-Norfolk). Eur. J. Gastroenterol. Hepatol. 23 (8), 733–740. Bennion, L.J., Ginsberg, R.L., Gernick, M.B., Bennett, P.H., 1976. Effects of oral contraceptives on the gallbladder bile of normal women. N. Engl. J. Med. 294 (4), 189–192. Bergstrom, A., Pisani, P., Tenet, V., Wolk, A., Adami, H.O., 2001. Overweight as an avoidable cause of cancer in Europe. Int. J. Cancer 91 (3), 421–430. Boland, L.L., Folsom, A.R., Rosamond, W.D., Atherosclerosis Risk in Communities Study (ARIC) Investigators, 2002. Hyperinsulinemia, dyslipidemia, and obesity as risk factors for hospitalized gallbladder disease. A prospective study. Ann. Epidemiol. 12 (2), 131–140. Braverman, D.Z., Johnson, M.L., Kern Jr., F., 1980. Effects of pregnancy and contraceptive steroids on gallbladder function. N. Engl. J. Med. 302 (7), 362–364. Calle, E.E., Kaaks, R., 2004. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4 (8), 579–591. Calle, E.E., Rodriguez, C., Walker-Thurmond, K., Thun, M.J., 2003. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348 (17), 1625–1638. Carriaga, M.T., Henson, D.E., 1995. Liver, gallbladder, extrahepatic bile ducts, and pancreas. Cancer 75 (1 Suppl.), 171–190. Chan, J.M., Rimm, E.B., Colditz, G.A., Stampfer, M.J., Willett, W.C., 1994. Obesity, fat distribution, and weight gain as risk factors for clinical diabetes in men. Diabetes Care 17 (9), 961–969. Chow, W.H., McLaughlin, J.K., Menck, H.R., Mack, T.M., 1994. Risk factors for extrahepatic bile duct cancers: Los Angeles County, California (USA). Cancer Causes Control 5 (3), 267–272. DerSimonian, R., Laird, N., 1986. Meta-analysis in clinical trials. Control. Clin. Trials 7 (3), 177–188. Dittrick, G.W., Thompson, J.S., Campos, D., Bremers, D., Sudan, D., 2005. Gallbladder pathology in morbid obesity. Obes. Surg. 15 (2), 238–242. Egger, M., Davey Smith, G., Schneider, M., Minder, C., 1997. Bias in meta-analysis detected by a simple, graphical test. BMJ 315 (7109), 629–634. Engeland, A., Tretli, S., Austad, G., Bjorge, T., 2005. Height and body mass index in relation to colorectal and gallbladder cancer in two million Norwegian men and women. Cancer Causes Control 16 (8), 987–996. Everhart, J.E., 1993. Contributions of obesity and weight loss to gallstone disease. Ann. Intern. Med. 119 (10), 1029–1035. Everhart, J.E., Ruhl, C.E., 2009. Burden of digestive diseases in the United States part III: liver, biliary tract, and pancreas. Gastroenterology 136 (4), 1134–1144. Field, A.E., Coakley, E.H., Must, A., et al., 2001. Impact of overweight on the risk of developing common chronic diseases during a 10-year period. Arch. Intern. Med. 161 (13), 1581–1586. Gatta, G., van der Zwan, J.M., Casali, P.G., et al., 2011. Rare cancers are not so rare: the rare cancer burden in Europe. Eur. J. Cancer 47 (17), 2493–2511. González-Pérez, A., García Rodríguez, L.A., 2007. Gallbladder disease in the general population: association with cardiovascular morbidity and therapy. Pharmacoepidemiol. Drug Saf. 16 (5), 524–531. Grainge, M.J., West, J., Solaymani-Dodaran, M., Aithal, G.P., Card, T.R., 2009. The antecedents of biliary cancer: a primary care case–control study in the United Kingdom. Br. J. Cancer 100 (1), 178–180. Greenland, S., Longnecker, M.P., 1992. Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am. J. Epidemiol. 135 (11), 1301–1309.

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Body mass index and biliary tract disease: a systematic review and meta-analysis of prospective studies.

To evaluate the association between body mass index (BMI, kg/m(2)) and incidence of biliary tract disease...
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