Meta-Analysis
Copyright ©2014 Baishideng Publishing Group Inc.
World J Gastroenterol. Nov 14, 2014; 20(42): 15879-15898
Published online Nov 14, 2014. doi: 10.3748/wjg.v20.i42.15879
Table 1 Characteristics of published cohort studies on dairy product consumption and gastric cancer risk
Ref.Region and designNo. of cases(outcome)Sample sizeFollow-up(yr)Type of meat andconsumption categoriesAdjusted RR(95%CI)Covariate adjustments
Nomura et al[49], 1990United States; cohort150 (incidence)7990 men19Milk (times/wk) ≤ 1 2-4 ≥ 5 Ice cream (times/wk) ≤ 1 2-4 ≥ 5 Butter, margarine, cheese (times/wk) ≤ 1 2-4 ≥ 51.0 1.5 (0.8-2.5) 1.2 (0.8-1.6) 1.0 0.9 (0.6-1.3) 1.1 (0.7-1.8) 1.0 1.1 (0.5-2.1) 1.4 (0.9-2.2)Age
Kneller et al[50], 1991United States; cohort75 (mortality)17633 men20Dairy Quartiles Milk (glasses/d) < 1 1 2-3 ≥ 4 Used before but not currently1.00 1.2 (0.67-2.26) 1.1 (0.61-2.10) 1.2 (0.61-2.44) 1.00 1.4 (0.76-2.74) 0.9 (0.45-1.70) 2.4 (1.10-5.04) 1.2 (0.50-2.68)Year of birth and current cigarette smoking
Galanis et al[51], 1998United States; cohort108 (44 women, 64 men) (incidence)11907 (6297 women, 5610 men)14.8Milk (cups/d) 0 ≥ 1 Milk (cups/d) 0 ≥ 1 Milk (cups/d) 0 ≥ 1Women 1.0 1.0 (0.5-1.8) Men 1.0 1.0 (0.6-1.7) Total (women and men) 1.0 1.0 (0.7-1.5)Age, years of education, Japanese place of birth, gender. Among man also adjusted for cigarette smoking and alcohol intake status
Ngoan et al[52], 2002Japan; cohort116 (39 women, 77 men) (mortality)13250 (7333 women, 5917 men)10.5Fresh milk ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Fresh milk ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Fresh milk ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Milk products ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Milk products ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Milk products ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Margarine ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/d Margarine ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/dWomen 0.9 (0.3-2.3) 1.3 (0.6-2.6) Men 1.3 (0.7-2.4) 0.9 (0.5-1.6) Total (women and men) 1.5 (0.8-3.0) 0.8 (0.4-1.6) Women 1.2 (0.3-5.6) 3.1 (0.8-11.6) Man 1.7 (0.8-3.6) 1.5 (0.5-4.2) Total (women and men) 1.3 (0.6-2.8) 1.4 (0.5-3.6) Women 0.6 (0.2-1.9) 0.9 (0.3-2.9) Man 1.1 (0.5-2.1) 1.1 (0.5-2.6)Women or men: adjust for age Total: adjust for age, sex, smoking, processed meat, liver, cooking or salad oil, suimono and pickled food
Margarine ≤ 2-4 times/mo 2-4 times/wk ≥ 1 time/dTotal (women and men) 0.8 (0.4-1.8) 0.7 (0.3-1.8)
Khan et al[53], 2004Japan; cohort51 (15 women and 36 men) (mortality)3158 (1634 women, 1524 men )14.8Milk A B Milk A B Butter/margarine A B Butter/margarine A B Cheese A B Cheese A BWomen 1.0 (0.4-3.0) Men 1.1 (0.5-2.2) Women 0.6 (0.2-2.3) Men 1.7 (0.9-3.2) Women 1.2 (0.3-5.4) Men 1.2 (0.5-3.0)Women: adjust for age, health status, health education, health screening and smoking Men: adjust for age, smoking
Tokui et al[54], 2005Japan; cohort859 (285 women, 574 men) (mortality)110792 women and men11Milk None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Milk None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Yogurt None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Yogurt None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Cheese None 1-2 times/mo 1-2 times/wk 3-4 times/wk ≥ 1 times/d Cheese None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Butter None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Butter None 1-2/mo 1-2/wk 3-4/wk ≥ 1/dWomen 1.00 (Referent) 0.62 (0.33-1.18) 0.90 (0.58-1.38) 0.78 (0.50-1.21) 0.83 (0.60-1.13) Men 1.00 (Referent) 1.13 (0.79-1.63) 1.17 (0.87-1.58) 1.08 (0.79-1.48) 1.06 (0.84-1.35) Women 1.00 (Referent) 0.95 (0.63-1.43) 1.38 (0.93-2.05) 0.85 (0.44-1.63) 0.88 (0.47-1.64) Men 1.00 (Referent) 0.69 (0.49-0.98) 0.86 (0.58-1.28) 1.22(0.76-1.97) 0.82 (0.50-1.37) Women 1.00 (Referent) 1.31(0.92-1.85) 0.93 (0.57-1.52) 0.60 (0.24-1.46) 1.18 (0.52-2.69) Men 1.00 (Referent) 0.93 (0.72-1.20) 1.08 (0.80-1.48) 1.32 (0.86-2.04) 0.79 (0.39-1.61) Women 1.00 (Referent) 0.76 (0.50-1.17) 1.27 (0.85-1.90) 0.37 (0.14-1.01) 1.22 (0.65-2.26) Men 1.00 (Referent) 0.97 (0.75-1.27) 0.96 (0.70-1.33) 0.92 (0.57-1.47) 0.70 (0.38-1.29)Age
Margarine None 1-2/mo 1-2/wk 3-4/wk ≥ 1/d Margarine None 1-2/mo 1-2/wk 3-4/wk ≥ 1/dWomen 1.00 (Referent) 0.98 (0.64-1.50) 1.09 (0.74-1.59) 0.69 (0.39-1.22) 0.82 (0.50-1.33) Men 1.00 (Referent) 0.83 (0.61-1.12) 1.14 (0.87-1.49) 0.92 (0.62-1.36) 0.72 (0.48-1.10)
Van der Pols et al[55], 2007United Kingdom, Scotland; cohort770 (mortality)4383 children65Total dairy Group 1 (low) Group 2 Group 3 Group 4 (high) Milk (cups/d) < 0.5 0.5-0.8 > 0.8 - < 1.2 ≥ 1.21.00 1.17 (0.39-3.47) 1.46 (0.44-4.89) 0.81 (0.09-7.34) 1.00 1.17 (0.41-3.34) 1.40(0.46-4.26) 0.79 (0.11-5.73)Age, sex, energy, fruit, and calcium intakes
Pham et al[56], 2010Japan; cohort477 (157 women, 320 men) (mortality)63403 (women 37 673, men 25 730)-Dairy products pattern (factor score) Quartiles Dairy products pattern (factor score) QuartilesWomen 1.00 0.96 (0.64-1.45) 0.74 (0.47-1.18) 0.77 (0.48-1.23) Men 1.00 0.82 (0.61-1.10) 0.74 (0.54-1.01) 0.72 (0.52-0.99)Age, tobacco smoking status, history of gastric ulcer, stomach cancer screening, body mass index, educational level, and total energy intake
Buckland et al[57], 2010European countries; cohort449 (190 women, men 259) (incidence)485044 (women 340467, men 144577)8.9Dairy products Tertiles Dairy products Tertiles Dairy products TertilesWomen 1 (reference) 1.22 (0.84-1.77) 0.97 (0.65-1.45) Men 1 (reference) 0.86 (0.63-1.17) 0.98 (0.70-1.37) Total (women and men) 1 (reference) 1.01 (0.80-1.27) 0.97 (0.75-1.25)Sex, body mass index, educational level, smoking status, cigarette smoking intensity, and total energy intake.
Ko et al[58], 2013South Korea; cohort166 (incidence)9724 women and men8.5Dairy products Almost never 1-4 times/mo 1-4 times/wk ≥ 1 time/d Dairy products Low intake High intake Dairy products Low intake High intakeTotal (women and men) 1.15 (0.78-1.70) 1.25 (0.82-1.92) 1.30 (0.83-2.06) Women 1.10 (0.91-1.33) Men 1.05 (0.92-1.19)Total: adjust for age, sex, cigarette smoking, body mass index, alcohol drinking, and area of residence Women or men: adjust for age, cigarette smoking, body mass index, alcohol drinking, and area of residence
A: Reference group = took never + took several times per year + took several times per month; B: Comparison group = took several times per week + took every day. RR: Relative risk (rate ratio or hazard ratio); CI: Confidence interval.
Table 2 Characteristics of published case-control studies on dairy product consumption and gastric cancer risk
Ref.Region and designCases/controlsType of item and consumption categoriesAdjusted RR (95%CI)Covariate adjustments
Correa et al[59], 1985United States; case control (hospital based)391/391Dairy products Dairy productsWhites 1.06 (0.68-1.63) Blacks 0.85 (0.53-1.34)Age, sex, respondent status, education, income, tobacco, and alcohol use
Wu-Williams et al[60], 1990United States; case control (population based)137/137Milk ≤ 1/wk ≥ 2-4/wk ≥ 5/wk1.0 0.8 (0.4-1.7) 1.0 (0.6-1.7)
Mettlin et al[24], 1990United States; case control (hospital based)115/1300Whole Milk None < Daily Daily 2%Milk None < Daily Daily Skim Milk None < Daily Daily1.0 2.9 (1.7-4.9) 3.9 (2.3-6.6) 1.0 0.5 (0.3-0.9) 0.4 (0.2-0.6) 1.0 1.0 (0.5-2.3) 0.5 (0.2-1.3)Age, sex, smoking history, education, and country of residence
Boeing et al[61], 1991Germany; case control (hospital based)143/579Milk Tertiles Dairy products Tertiles Cheese Tertiles1.0 1.23 (0.77-1.97) 1.31 (0.82-2.10) 1.0 0.71 (0.45-1.12) 0.63 (0.39-1.03) 1.0 1.09 (0.67-1.75) 0.55 (0.30-0.98)Milk and dairy products: adjust for age, sex, hospital Cheese: adjust for age, sex, hospital, raw vegetables, citrus fruit, processed meat, whole-meal bread
Boeing et al[62], 1991Poland; case control (hospital based)741/741Cheese score Low Moderate High1.0 0.92 (0.73-1.17) 0.92 (0.67-1.26)Age, sex, education, occupation, residence
Yu et al[63], 1991China, case control (population based)84/2676Milk Nonusers Users1.0 0.9 (0.5-1.7)Age, sex, family income, family history of stomach cancer, family history of other cancer, history of tuberculosis, blood type, cigarette smoking, alcohol, strong tea, fruit, and milk consumption
Hoshiyama et al[39], 1992Japan; case control population based hospital based294/294 294/202Dairy products ≤ 1/wk 2-4/wk ≥ 5/wk Dairy products ≤ 1/wk 2-4/wk ≥ 5/wk1.0 0.6 (0.4-1.0) 0.8 (0.6-1.2) 1.0 0.9 (0.5-1.6) 1.0 (0.7-1.6)Age, sex, administrative division, and smoking status Age, sex, area, smoking status
Memik et al[64], 1992Turkey; case control (population based)252/609Milk 0-200 mL/wk 200-600 mL/wk 600 mL/wk1.0 0.91 (0.43-1.94) 5.33 (3.09-9.26)
Hansson et al[65], 1993Sweden; case control (population based)338/669Whole milk (mL/wk) ≤ 199 > 199-2700 > 2700-4100 > 4100-6900 > 6900 Skimmed milk (mL/wk) 0 > 01.19 (0.68-2.05) 1.58 (0.97-2.59) 1.35 (0.83-2.20) 1.73 (1.02-2.94) 0.77 (0.53-1.12)Age, gender, SES
Soured milk (times/mo) ≤ 0.9 > 0.9-70.82 (0.54-1.24)
> 7-11 > 11-19 > 19 Cheese (times/mo) ≤ 7 > 7-29 > 29-59 > 590.84 (0.55-1.26) 0.81 (0.51-1.30) 0.90 (0.58-1.42) 1.03 (0.64-1.65) 0.84 (0.53-1.31) 0.79 (0.48-1.32)
Inoue et al[66], 1994Japan; case control (hospital based)668/668Milk < 3-4 times/wk ≥ 3-4 times/wk1.0 (0.80-1.25)Sex
Falcao et al[67], 1994Portugal; case control (hospital based)74/193Milk ≤ 0.51/d0.33 (0.11-0.99)
Cornée et al[68], 1995France; case control (hospital based)92/128Total dairy products Tertiles Milk (all types) Tertiles Hard cheese Tertiles Soft cheese Tertiles Yoghurt Tertiles Butter and cream Tertiles1.0 1.10 (0.53-2.30) 1.80 (0.89-3.66) 1.0 1.53 (0.73-3.19) 1.57(0.75-3.29) 1.0 1.09 (0.52-2.26) 1.48 (0.74-2.96) 1.0 0.64 (0.31-1.30) 0.92 (0.47-1.80) 1.0 0.86 (0.40-1.88) 0.75 (0.37-1.54) 1.0 1.31 (0.64-2.71) 1.44 (0.71-2.93)Age, sex, occupation and total energy intake
Muñoz et al[4], 1997Italy; case-control (hospital based)88/103Butter (score) Low Intermediate/high Margarine (score) Low Intermediate/high1.0 1.88 (1.03-3.44) 1.0 2.42 (1.06-5.51)Age, sex, area of residence, and education
Watabe et al[69], 1998Japan; case control (population based)242/484Milk Daily Cheese ≥ 3/wk Butter ≥ 3/wk Yogurt Daily0.6 (0.43-0.83) 0.83 (0.51-1.33) 1.57 (0.96-2.53) 0.66 (0.38-1.09)
Ward et al[70], 1999Mexico; case control (population based)220/752Dairy products (times/wk) < 5 5-10 11-16 ≥ 171.0 2.1 (1.2-3.7) 2.3 (1.2-4.2) 2.7 (1.4-5.0)Age, gender, total calories, chili pepper consumption, added salt, history of peptic ulcer, cigarette smoking, SES
Muñoz et al[71], 2001Venezuela, case control (population based)292/485Dairy products Quartiles1.0 1.58 (0.98-2.55) 2.08 (1.30-3.32) 2.43 (1.46-4.04)Age, sex, tobacco, alcohol, total calories and SES
Kim et al[72], 2002Korea; case control (hospital based)136/136Milk and milk products Low Medium High1.00 0.75 (0.42-1.35) 0.68 (0.34-1.36)Age, sex, SES, family history and refrigerator use
Chen et al[73], 2002United States; case control (population based)124/449Dairy products (times/wk) Quartiles0.79 (0.35-1.7) 1.40 (0.68-2.8) 0.76 (0.34-1.7)Age, sex, energy, respondent type, body mass index, alcohol use, tobacco use, education, family history, vitamin supplement
Milk (times/wk) Quartiles0.72 (0.33-1.6) 1.7 (0.85-3.5) 0.86 (0.39-1.9)
Ito et al[74], 2002Japan; case control (hospital based)508/36490Milk Almost never Occasionally 3-4 times/wk Everyday1.0 0.98 (0.75-1.27) 1.09 (0.85-1.39) 0.85 (0.62-1.18)Age, year, season of fist hospital visit, smoking habit, family history of gastric cancer
Lissowska et al[75], 2004Poland; case control (population based)274/463Diary product (times/wk) < 18.9 18.9-25.8 25.9-32.9 > 32.91.0 0.96 (0.63-1.46) 0.87 (0.54-1.40) 0.94 (0.57-1.54)Age, sex, education, smoking, and calories from food
De Stefani et al[76], 2004Uruguay; case control (hospital based)240/960Dairy foods Tertiles Dairy foods Highest tertile vs Lowest tertile Dairy foods Highest tertile vs Lowest tertileTotal (women and men) 1.0 1.24 (0.85-1.80) 0.89 (0.59-1.33) Women 1.45 (0.64-3.29) Men 0.75 (0.46-1.20)Total: adjust for age, sex, residence, urban/rural status, education, body mass index, and total energy intake Women or men: adjust for age, residence, urban/rural status, education, body mass index, tobacco smoking, alcohol drinking, and total energy intake
Huang et al[77], 2004Japan; case control (hospital based)GCFH(+) 464/6 310 GCFH(-) 1524/44 396Milk < 1/d ≥ 1/d Milk < 1/d ≥ 1/d0.86 (0.70-1.05) 0.98 (0.88-1.09)Age, sex
Fei et al[78], 2006China; case control (hospital based)189/567Milk products High vs low0.690 (0.524-0.907)
Lucenteforte et al[79], 2008Italy; case control (hospital based)230/547Milk and yogurt (servings/wk) ≤ 0.5 > 0.5-4.5 > 4.5-7 > 7-9 > 9-24 Cheese (servings/wk) ≤ 1.8 > 1.8-3.0 > 3.0-3.8 > 3.8-5.1 > 5.1-10.71.0 0.77 (0.45-1.33) 0.81 (0.50-1.30) 0.88 (0.50-1.54) 1.06 (0.64-1.78) 1.0 1.38 (0.79-2.41) 1.43 (0.82-2.49) 1.22 (0.70-2.15) 1.63 (0.92-2.90)Age, sex, education, year of interview, body mass index, tobacco smoking, family history of stomach cancer, and total energy intake
Chen et al[80], 2009China; case control (hospital based)41/205Dairy products (times/wk) < 3 ≥ 3 Milk (/d) No Yes1.00 0.72 (0.13-4.15) 1.00 1.02 (0.16-7.08)Age and years of schooling
Pourfarzi et al[81], 2009Iran; case control (population based)217/394Dairy products ≤ 2 times/wk 3-4/wk > 1/d Cheese ≤ 2 times/wk 3-4/wk > 1/d1.00 3.77 (1.92-7.42) 2.28 (1.23-4.22) 1.00 1.00 (0.39-2.56) 1.16 (0.54-2.51)Age, sex, education, family history of gastric cancer, citrus fruits, garlic, onion, red meat, fish, dairy products, strength and warmth of tea, preference for salt intake and H. pylori
Lazarevic et al[82], 2010Serbia; case control (hospital based)102/204Milk Tertiles Dairy Tertiles1.00 2.60 (0.86-7.87) 5.08 (1.59-10.16) 1.00 0.42 (0.20-1.23) 0.63 (0.33-1.72)Age, sex, residence, education, meals regularity, tobacco smoking, and history of cancer in the first degree relatives
Icli et al[83], 2011Turkey; case control (hospital based)253/253Milk Low Moderate High1.0 1.4 (0.7-2.6)
Yogurt Low Moderate High1.0 0.8 (0.4-1.5) 1.0 (0.2-4.9)
Pakseresht et al[84], 2011Iran; case control (population based)286/304Dairy Per 100 g1.01 (0.90-1.13)Age, sex, education, living area, smoking, gastric symptoms, income, owning refrigerator, duration of using refrigerator, seeds preparing method, frying H. pylori infection.
RR: Relative risk (rate ratio or hazard ratio); CI: Confidence interval; SES: Socio-economic status; PCC: Population-based case-control; HCC: Hospital-based case-control; H. pylori: Helicobacter pylori.
Table 3 Methodological quality of cohort studies included in this meta-analysis
Ref.Representativeness of the exposed cohortSelection of the non exposed cohortAscertainment of exposureOutcome of interest not present at start of studyControl for important factors1Assessment of outcomeFollow-up long enough for outcomes to occur2Adequacy of follow-up of cohorts3Total quality scores
Nomura et al[49], 1990********8
Kneller et al[50], 1991********8
Galanis et al[51], 1998*********9
Ngoan et al[52], 2002*********9
Khan et al[53], 2004*********9
Tokui et al[54], 2005********8
Van der Pols et al[55], 2007**-*****7
Pham et al[56], 2010*******-*8
Buckland et al[57], 2010********8
Ko et al[58], 2013*********9
1A maximum of two stars could be awarded for this item. Studies that controlled for age received one start, whereas studies that controlled for smoking or drinking received an additional start;
2A cohort study with a follow-up time > 8 years was awarded one start;
3A cohort study with a follow-up rate > 70% was awarded one start.
Table 4 Methodological quality of case-control studies included in this meta-analysis
Ref.Adequate definition of casesRepresentativeness of casesSelectionof controlDefinition of controlControl for important factor or additional factor1Exposure assessmentSame method of ascertainment for cases and cohortsNonresponse rate2Total quality scores
Correa et al[59], 1985**-*****-7
Wu-Williams et al[60], 1990***--**-5
Mettlin et al[24], 1990-*-*****-6
Boeing et al[61], 1991**-****-6
Boeing et al[62], 1991**-****-6
Yu et al[63], 1991********-8
Hoshiyama et al[39], 1992***-****-7
Memik et al[64], 1992****--*-5
Hansson et al[65], 1993***-***-6
Inoue et al[66], 1994**-*-***6
Falcao et al[67], 1994**-*-**-5
Cornée et al[68], 1995**-****-6
Muñoz et al[4], 1997**-****-6
Watabe et al[69], 1998***--**-5
Ward et al[70], 1999********-8
Muñoz et al[71], 2001***-****-7
Kim et al[72], 2002**-****-6
Chen et al[73], 2002***-****-7
Ito et al[74], 2002**-*****-7
Lissowska et al[75], 200***-****-7
De Stefani et al[76], 2004**-*****-7
Huang et al[77], 2004-*-****-5
Fei et al[78], 2006**-*-**-5
Lucenteforte et al[79], 2008**-*****-7
Chen et al[80], 2009**-****-6
Pourfarzi et al[81], 2009*******-7
Lazarevic et al[82], 2010**-*****-7
Icli et al[83], 2011**-*-**-5
Pakseresht et al[84], 2011********-8
1A maximum of two stars could be awarded for this item. Studies that controlled for age received one start, whereas studies that controlled for smoking or drinking received an additional start;
2One star was assigned if there was no significant difference in the response rate between case and control subjects by using the χ2 test (P = NS). NS: Not significant.
Table 5 Subgroup analysis of relative risks for the association between dairy product consumption and gastric cancer risk
No. of studiesRR (95%CI)Q-valuepHI2
Study design
All studies381.06 (0.95-1.18)112.610.00067.1%
Cohort studies101.00 (0.89-1.14)12.900.16730.2%
HCC studies170.94 (0.83-1.08)30.500.01647.5%
PCC studies111.36 (0.94-1.96)59.140.00083.1%
Sex
Women81.00 (0.88-1.13)6.700.4600.0%
Men80.98 (0.90-1.07)9.420.22425.7%
Region
Asia150.92 (0.83-1.02)23.080.05939.3%
Europe131.15 (0.86-1.55)55.500.00078.4%
America101.20 (0.95-1.50)20.180.01755.4%
Adjustments
Smoking No smoking17211.06 (0.90-1.25)1.06 (0.91-1.23)35.00 77.310.0040.00054.3%74.1%
DrinkingNo drinking5331.19 (0.81-1.74)1.04 (0.93-1.17)11.47 98.410.0220.00065.1%67.5%
RR: Relative risk (rate ratio or hazard ratio); CI: Confidence interval.