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Copyright ©2013 Baishideng Publishing Group Co.
World J Gastroenterol. Feb 21, 2013; 19(7): 1020-1029
Published online Feb 21, 2013. doi: 10.3748/wjg.v19.i7.1020
Table 1 Characteristics of the studies included in the meta analysis
Ref.Study periodSexNo. of casesNo. cohorts or controlsDietary assessmentExposure and comparison levelAdjusted RR (95%CI)Study quality1Adjustment for confounders
Cohort studies
Keszei et al[11]1986-2002MESCC: 107120 852FFQ 150 itemsRed meat9Age, smoking (including years and numbers per day), total energy, BMI, alcohol drinking, vegetable, fruit, education, non-occupational PA
FEAC: 145ESCC
MQ5 vs Q12.66 (0.94-7.48)
FT3 vs T10.87 (0.42-1.79)
EAC
MQ5 vs Q10.57 (0.28-1.19)
FT3 vs T11.09 (0.44-2.75)
Processed meat
ESCC
MQ5 vs Q13.47 (1.21-9.94)
FT3 vs T10.63 (0.28-1.44)
EAC
MQ5 vs Q10.94 (0.46-1.89)
FT3 vs T10.58 (0.22-1.50)
Cross et al[12]1995-2006CESCC: 215494 979FFQ 124 itemsRed meat (Q5 vs Q1)9Age, sex, BMI, education, ethnicity, smoking, alcohol drinking, PA at work, vigorous PA, daily intakes of fruit, vegetable, saturated fat, energy
EAC: 630ESCC1.79 (1.07-3.01)
EAC1.15 (0.84-1.57)
Processed meat (Q5 vs Q1)
ESCC1.32 (0.83-2.10)
EAC1.08 (0.81-1.43)
González et al[13]1992-1998CEAC: 65521 457FFQ 88-266 itemsRed meat (T3 vs T1)1.67 (0.75-3.72)8Sex, height, weight, education, smoking, smoking intensity, work and leisure PA, intakes of alcohol, energy, vegetable, citrus fruit, non-citrus fruit, types of meat intake were mutually adjusted
Processed meat (T3 vs T1)3.54 (1.57-7.99)
Yu et al[14]1974-1989CAll: 116212 693Questionnaire 15 itemsPork (never vs regular/occasional)1.37 (1.11-1.68)7Age, sex
Case-control studies
Ward et al[15]1988-1993CEAC: 124449Questionnaire 100 itemsRed meat (> 157.2 g/d vs ≤ 73.8 g/d)2.85 (1.00-8.16)5Age, sex, race, vital status, year of birth, sex, No. of cigarettes per day, BMI, intakes of retinoic acid, folate, riboflavin, zinc, carbohydrate, protein, total energy.
Processed meat (> 52.3 g/d vs ≤ 16.1 g/d)1.40 (0.62-3.15)
De Stefani et al[16]1996-2004CESCC: 2342020FFQ 64 itemsRed meat ( T3 vs T1)4.97 (2.98-8.29)7Age, sex, residence, education, BMI, smoking, drinking, mate temperature, total energy, total intakes of vegetable and fruit, scored pattern
Processed meat (T3 vs T1)0.76 (0.51-1.13)
Gao et al[17]1997-2005CESCC: 6001514Questionnaire 35 itemsRed meat (> weekly vs monthly/seldom/never)1.37 (1.03-1.82)5Age, sex, geographic region
Wu et al[18]2003-2007CAll: 14953819FFQRed meat (Q4 vs Q1)1.13 (0.94-1.36)7Age, sex, education, previous income, BMI, pack-years smoking, weekly ethanol intake, study area
Hajizadeh et al[19]N/ACESCC: 4796FFQ168 itemsRed meat (T3 vs T1)2.47 (0.76-7.96)6Age, sex, education, tobacco smoking, symptomatic gastroesophageal reflux, BMI, total energy
Processed meat (T3 vs T1)1.10 (0.36-2.47)
O'Doherty et al[20]2002-2005CEAC: 221256FFQ101 itemsRed meat (Q4 vs Q1)3.15 (1.38-7.20)7Age, sex, smoking, BMI 5 yr before interview date, education, job type, Intakes of energy, fruit, vegetable, alcohol (g/d), Helicobacter pylori infection, nonsteroidal anti-inflammatory drug use 5 yr before, interview date, gastroesophageal reflux symptoms, location, types of meat intake were mutually adjusted
Processed meat (Q4 vs Q1)1.41 (0.67-2.95)
Sapkota et al[21]1999-2003CESCC: 1871110Questionnaire 23 itemsRed meat (≥ 1/wk vs < 1/mo)0.62 (0.19-2.09)6Age, sex, country, tobacco pack-year, education, BMI, frequency of alcohol consumption, vegetable, fruit consumption
Processed meat (≥ 1 time/wk vs < 1 time/mo)1.12 (0.52-2.41)
Navarro Silvera et al[22]1993-1995CEAC: 282687FFQ104 itemsRed meat (high vs low)3.02 (1.65-5.52)7Age, sex, study site, race, proxy status, income, education, BMI, No. of smoking cigarettes per day, intakes of beer, wine, liquor, and energy
Wang et al[23]2004-2006MESCC: 355408QuestionnairePork (often vs none/seldom)2.06 (1.42-2.99)5Age, sex, marital status, education
F1.91 (1.16-3.16)
Wu et al[24]1992-1997CEAC: 2061308Questionnaire 124 itemsRed meat (Q4 vs Q1)1.29 (0.8-2.2)5Age, sex, race, birthplace, education, smoking, BMI, reflux, use of vitamins, total energy
Processed meat (Q4 vs Q1)1.23 (0.7-2.1)
Chen et al[25]1988-1993CEAC: 124449Questionnaire54 itemsRed meat (Q4 vs Q1)1.4 (0.61-3.2)7Age, sex, energy intake, respondent type, BMI, alcohol drinking, smoking, education, family history, vitamin supplement use, age squared for EAC
Processed meat (Q4 vs Q1)1.7 (0.71-3.9)
Takezaki et al[26]1988-1997MAll: 28411 888QuestionnaireBeef (≥ 3/wk vs ≤ 3/mo)0.9 (0.6-1.5)5Age, year and season of visit, smoking, drinking
Bosetti et al[27]1992-1997CESCC:304743FFQ78 itemsRed meat (Q5 vs Q1)1.93 (1.09-3.41)5Age, sex, area of residence, education, tobacco smoking, alcohol drinking, non-alcohol energy
Rolón et al[28]1988-1991CAll: 131379FFQRed meat (highest vs lowest)3.8 (1.3-11.0)5Age, sex, alcohol, smoking, design variable of the study, hospital group, intakes of red meats, fats, fish, milk
Castelletto et al[29]1986-1989CESCC: 131261FFQ10 food groupsBeef (≥ daily vs < daily)0.6 (0.3-0.9)6Age, sex, design variable, hospital, education, No. of cigarettes smoking per day, intakes of alcohol, barbecued meat, potatoes, raw vegetables, cooked vegetables
Tavani et al[30]1984-1992CAll: 46230FFQ14 itemsHam (Q3 vs Q1)1.4 (0.6-3.3)5.5Age, sex, education, total alcohol intake
Liver (Q2 vs Q1)1.1 (0.5-2.3)
Rogers et al[31]1983-1987CAll: 127466FFQ125 itemsBeef (≥ 1/wk vs < 1/wk)5Age, sex, pack-years of cigarette, drink-years of alcohol, energy intake, beta-carotene intake, ascorbic acid intake
As a main dish0.8 (0.4-1.4)
As a sandwich1.0 (0.6-1.7)
Pork (≥ 1/wk vs < 1/wk)1.2 (0.8-2.5)
Yu et al[32]1975-1981CBeef: 267Beef: 267Questionnaire10 food groupsBeef (≥ 5/wk vs ≤ 1/wk)1.3 (0.6-2.7)5Age, sex, race
Fried bacon or ham: 265Fried bacon or ham: 265Fried bacon or ham ( ≤ 1/wk vs≥ 5/wk )2.0 (1.1-3.5)
Barbecued or smoked meat: 268Barbecued or smoked meat: 268Barbecued or smoked meat (≥ 2/wk vs ≤ 1/wk)1.7 (0.9-3.0)
Chen et al[33]1996-2005MESCC: 320709Questionnaire6 itemsCured meat (≥ 1/wk vs < 1/wk )0.8 (0.4-1.4)5Age, educational level, ethnicity, source of hospital, smoking, alcohol drinking, areca nut chewing
Yang et al[34]2003-2004CAll: 185185Questionnaire 9 ItemsProcessed meat (> 3 meals/wk vs < 1 meal/wk)0.66 (0.31-1.41)5.5Family history of esophageal cancer, occupation, smoking, drinking, eating hot food, eating speed, intakes of vegetables, fruit, pickled vegetables, fresh meat, egg, tea, water supply
Levi et al[35]1992-2002CAll:138660FFQ79 itemsProcessed meat(> 3.2 freq/wk vs < 0.8 freq/wk)4.48 (2.05-9.79)6Age, sex, education, smoking, intakes of alcohol, energy, fruit and vegetable intake
Li et al[36]1997-2000CAll:12481248Questionnaire 12 itemsSowbelly (daily vs < 1/wk)2.28 (1.6-3.3)5Age, sex, income, residence, occupation, alcohol, tobacco
Takezaki et al[37]1995-2000CAll: 199333Questionnaire19 itemsSalted meat (≥ 1/wk vs < 1/mo)0.93 (0.38-2.29)6Age, sex, smoking, drinking
Table 2 Combined relative risks and 95%CI for esophageal cancer associated with red meat or processed meat by other factors in both cohort and case-control studies
Red meat
Processed meat
FactorsStudies (n)Ref.RR (95%CI)P for heterogeneityStudies (n)Ref.RR (95%CI)P for heterogeneity
Histological subtypes
EAC9[11-13,15,20,22,24,25,32]1.42 (1.02-1.98)0.198[11-13,15,20,24,25,32]1.38 (1.07-1.78)0.3
ESCC9[11,12,16,17,19,21,23,27,29]1.55 (1.10-2.17)7[11,12,16,19,21,27,33]1.08 (0.80-1.44)
Study location
Asia6[14,17,18,19,23,26]1.33 (1.09-1.62)0.675[19,33,34,36,37]1.09 (0.61-1.95)0.65
Europe6[11,13,20,21,27,30]1.33 (0.86-2.07)7[11,13,20,21,27,30,35]1.49 (0.99-2.23)
United States7[12,15,22,24,25,31,32]1.32 (1.03-1.70)5[12,15,21,25,32]1.30 (1.08-1.57)
South America3[16,28,29]2.20 (0.48-10.04)1[16]0.76 (0.51-1.13)
Sex
Male3[11,23,26]1.26 (0.66-2.41)0.882[11,33]1.24 (0.58-2.65)0.14
Female2[11,23]1.31 (0.78-2.21)1[11]0.61 (0.33-1.13)
Both19[12-22,24,25,27-32]1.42 (1.17-1.71)16[12,13,15,16,19-21,24,25,27,30,32,34-37]1.43 (1.15-1.77)
Study quality1
≥ 78[11-14,16,18,20,22]1.60 (1.20-2.13)0.236[11-13,16,20,25]1.20 (0.88-1.62)0.42
< 714[15,17,19,21,23-32]1.25 (1.02-1.54)12[15,19,21,24,27,30,32-37]1.43 (1.11-1.86)