Table 2 Characteristics of case-controls studies of meat consumption and esophageal cancer riska
Author, year, region / Journal / No. of cases / No. and type of control subjects / Type of cancer / Type of meat / Consumption categories / Adjusted OR (95%CI) / Adjusted variables / Quality scoreCook-Mozaffari PJ, 1979,
Iran / Br J Cancer / 344 (217 males and 127 females) (incidence) / 688 population-based
controls / Esophageal cancer / Meat
Poultry
Fish / > once a week/≤ once a week
>once a month/≤ once a month
>once a month/≤ once a month / Men
0.85 (0.59-1.22)
Women
1.12 (0.71-1.79)
Men
0.79 (0.55-1.14)
Women
0.72(0.45-1.14)
Men
0.85 (0.59-1.25)
Women
0.96 (0.59-1.56) / Residence / 6
Notani PN, 1987, India / Nutr Cancer / 236 (incidence) / 177 population-based and 215 hospital-based controls / Esophageal cancer / Meat
Poultry
Fish
Meat
Poultry
Fish / > once a week/≤ once a week
> once a week/≤ once a week / Population controls
1.46(0.9-2.5)
3.50(0.3-48.9)
3.77(2.3-6.3)
Hospital controls
1.00(0.7-1.6)
1.55(0.2-11.7)
2.18(1.4-3.3) / Age and tobacco habits. / 6
Brown LM, 1988, USA / J Natl Cancer Inst / 207 (incidence) / 422 hospital-based controls / Esophageal cancer / Meat and poultry
Tertiles
Fish and shellfish
Tertiles / T1
T2
T3
T1
T2
T3 / 1.0 (Referent)
1.5(0.9-2.7)
1.1(0.6-2.0)
1.0 (Referent)
1.2(0.7-2.2)
1.2(0.6-2.1) / Age, sex, race, smoking, and alcohol use / 5
De Stefani E, 1990, Uruguay / Cancer Res / 261 (incidence) / 522 hospital-based controls / Esophageal squamous cell carcinoma / Fresh meat
Barbecued meat / <once a week
1-3 times/week
>3 times/week
Daily
<once a week
1-3 times/week
>3 times/week
Daily / 1.00 (0.7-1.6)
0.3 (0.1-0.8)
0.38 (0.2-1.0)
0.61 (0.2-1.5)
1.00 (0.7-1.6)
0.86 (0.6-1.2)
1.04 (0.6-1.9)
2.66 (1.3-5.5) / Age, residence, smoking duration, type of tobacco, and alcoholconsumption. / 8
Tavani A, 1994, Italy / Cancer Epidemiol Biomarkers Prev / 46 (incidence) / 230 hospital-based controls / Esophageal cancer / Meat
(portions/week)
Fish
(portions/week) / <5
5-6
>6
No or occasionally
1
>1 / 1.0 (Referent)
1.5 (0.6-3.5)
1.5 (0.7-3.3)
1.0 (Referent)
0.2 (0.1-0.5)
0.5 (0.2-1.2) / Age, sex, education, and total energy intake / 6
Rolón PA, 1995, Paraguay / Cancer Epidemiol Biomarkers Prev / 131 (incidecne) / 381 hospital-based controls / Esophageal cancer / Red meat
Quartile
Fish
Quartile / Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4 / 1.0 (Referent)
3.1 (1.2-7.8)
3.0 (1.2-7.5)
3.8 (1.3-11.0)
1.0 (Referent)
2.0 (0.9-4.4)
2.0 (0.9-4.3)
1.5 (0.6-4.0) / Age, sex, hospital group, alcohol, cigarette smoking, fat, and milk. / 7
Ward MH, 1997, USA / Int J Cancer / 143 (incidence) / 502 population-based controls / Esophageal adenocarcinoma / Total red meat
(times/week)
Processed meat
(times/week) / <8
8-12
13-18
>19
<4
4-5
6-8
>8 / 1.0 (Referent)
1.3 (0.6-2.9)
1.4 (0.7-2.9)
2.0 (1.0-4.0)
1.0 (Referent)
1.3 (0.6-2.6)
1.1 (0.6-2.1)
1.7 (0.9-3.3) / Age, sex / 5
Launoy G, 1998, France / Int J Cancer / 208 (males only) (incidence) / 399 (males only) hospital-based controls / Esophageal squamous cell carcinoma / Meat
(grams/day)
Fresh fish
(grams/day) / 0-80
80-120
120-160
>160
0-10
10-20
20-30
>30 / 1.0 (Referent)
0.66 (0.39-1.13)
0.55 (0.29-1.02)
0.51 (0.26-0.98)
1.0 (Referent)
0.69 (0.40-1.21)
0.45 (0.24-0.83)
0.35 (0.18-0.67) / Age, interviewer, smoking, beer, aniseed aperitifs,hot Calvados, whisky, total alcohol, total energy intake, and othersignificant food groups(for fresh fish only). / 7
De Stefani E, 1999, Uruguay / Int J Cancer / 82 (incidence) / 248 hospital-based controls / Esophageal squamous cell carcinoma / Total meat
Tertiles
Red meat
Tertiles
Processed meat
Tertiles
White meat
Tertiles / T1
T2
T3
T1
T2
T3
T1
T2
T3
T1
T2
T3 / 1.0 (Referent)
0.67 (0.31-1.42)
1.09 (0.49-2.41)
1.0 (Referent)
0.91 (0.45-1.89)
0.97 (0.47-2.04)
1.0 (Referent)
0.90 (0.45-1.79)
0.64 (0.29-1.41)
1.0 (Referent)
0.55 (0.28-1.09)
0.77 (0.36-1.69) / Age, sex, residence, urban/rural status, education,family history of esophageal cancer, BMI, tobaccosmoking, total alcohol intake, mate intake, total food intake andvegetables and fruits. / 9
Fernandez E, 1999, Italy / Am J Clin Nutr / 316 (incidence) / 1990 hospital-based controls / Esophageal cancer / Fish
(servings/week) / <1
1
>2
Per 1 serving/week / 1.0 (Referent)
0.7 (0.5-0.9)
0.6 (0.4-0.9)
0.8 (0.7-0.9) / Age, sex, area of residence, education, smoking, alcohol consumption,and BMI. / 8
Pan G, 1999, China / Am J Ind Med / 125 (males only) (mortality) / 250 (males only) population-based controls / Esophageal cancer / Meat
Fish / History of high consumption / 0.55 (0.36–0.85)
0.56 (0.35–0.88) / Unadjusted / 3
Bosetti C, 2000, Italy / Int J Cancer / 304 (incidence) / 743 hospital-based controls / Esophageal squamous cell carcinoma / Red meat
(servings/week)
Processed meat
(servings/week)
Poultry
(servings/week)
Fish
(servings/week) / <2.9
2.9-3.9
3.9-5.2
5.2-6.7
>6.7
<1.4
1.4-1.9
1.9-2.9
2.9-4.4
>4.4
<0.9
0.9-1.4
1.4-1.9
1.9-2.9
>2.9
<0.9
0.9-1.4
1.4-1.9
1.9-2.9
>2.4 / 1.0 (Referent)
1.98 (1.15-3.41)
1.78 (1.15-3.41)
1.76 (1.00-3.08)
1.93 (1.09-3.41)
1.0 (Referent)
0.92 (0.55-1.56)
0.94 (0.57-1.56)
1.10 (0.68-1.78)
1.39 (0.85-2.26)
1.0 (Referent)
0.95 (0.60-1.51)
0.64 (0.35-1.17)
0.64 (0.39-1.03)
0.44 (0.26-0.76)
1.0 (Referent)
0.59 (0.37-0.95)
0.61 (0.37-1.00)
0.71 (0.42-1.19)
0.57 (0.33-0.97) / Age, sex, area of residence, education, tobacco smoking, alcohol
drinking and non-alcohol energy / 9
Levi F, 2000, Switzerland / Eur J Cancer Prev / 101 (incidence) / 327 hospital-based controls / Esophageal cancer (92 ESCC, 9 EAC) / Red meat
(servings/week)
Pork and processed meat
(servings/week)
Poultry
Fish / <2.83
2.84-4.70
>4.71
Per one serving/day
<3.1
3.2-6.9
>6.9
Per one serving/day
<0.5
0.6-1.0
>1.0
<1.2
1.3-1.7
>1.7 / 1.0 (Referent)
1.8 (0.8-4.4)
3.53 (1.46-8.53)
1.69 (1.3-2.2)
1.0 (Referent)
3.78 (1.5-9.3)
8.02 (3.1-20.5)
1.59 (1.2-2.1)
1.0 (Referent)
0.88 (0.2-5.0)
0.96 (0.2-5.1)
1.0 (Referent)
0.99 (0.4-2.3)
0.90 (0.55-1.8) / Age, sex, education, smoking, alcohol and non-alcohol total energy intake. / 9
Phukan RK, 2001, India / Nutr Cancer / 502 (incidence) / 1004 hospital-based controls / Esophageal cancer / Meat
Fish / Never
Occasionally
1-4 times/week
Daily
Never
Occasionally
1-4 times/week
Daily / 1.0 (Referent)
0.95 (0.04-3.6)
0.83 (0.03-5.1)
0.72 (0.01-4.8)
1.0 (Referent)
1.07 (0.06-4.2)
0.85 (0.04-4.1)
0.82 (0.03-3.9) / Age, sex / 4
Takezaki T, 2001, China / Jpn J Cancer Res / 199 (incidence) / 333 population-based
controls / Esophageal cancer / Meat
Salted meat
Poultry
Fish / <1 time/month
1-3 times/month
1-2 times/week
≥3 times/week
<1 times/month
1-3 times/month
≥1 times/week
<1 time/month
1-3 times/month
1-2 times/week
≥3 times/week
<1 time/month
1-3 times/month
1-2 times/week
≥3 times/week / 1.0 (Referent)
0.78 (0.51-1.20)
1.33 (0.79-2.22)
1.31 (0.60-2.85)
1.0 (Referent)
1.34 (0.72-2.48)
0.93 (0.38-2.29)
1.0 (Referent)
1.24 (0.80-1.94)
2.71 (1.55-4.73)
1.42 (0.62-3.25)
1.0 (Referent)
1.02 (0.66-1.57)
1.49 (0.88-2.53)
1.42 (0.67-3.04) / Age, sex, smoking, and drinking habits / 6
Chen H, 2002, USA / Am J Clin Nutr / 124 (incidence) / 449 population-based
controls / Esophageal adenocarcinoma / Total meat
Quartiles
(times/week)
Red meat
Quartiles
(times/week)
Processed meat
Quartiles
(times/week)
Poultry
Quartiles
(times/week)
Fish
Quartiles
(times/week) / Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4 / 1.0 (Referent)
1.5 (0.66-3.5)
1.9 (0.80-4.3)
1.6 (0.61-4.1)
1.0 (Referent)
0.93 (0.49-2.1)
1.0 (0.46-2.2)
1.4 (0.61-3.2)
1.0 (Referent)
1.2 (0.50-2.7)
0.85 (0.38-1.9)
1.7 (0.71-3.9)
1.0 (Referent)
0.71 (0.38-1.3)
0.53 (0.25-1.1)
0.47 (0.17-1.3)
1.0 (Referent)
0.61 (0.31-1.2)
0.28 (0.14-0.57)
0.14 (0.04-0.48) / Age, sex, energy intake, respondent type, BMI, alcohol use, tobacco use, education, familyhistory, vitamin supplement use, and for age squared for esophageal adenocarcinoma. / 9
Ke L, 2002, China / Int J Cancer / 1248 (incidence) / 1248 population-based
controls / Esophageal squamous cell carcinoma / Fermented fish sauce / ≤once/week
2-3/week
3 times/week
Daily / 1.0 (Referent)
2.09 (1.59-2.75)
14.29 (5.88-35.4)
15.78 (7.04-35.42) / Age,sex, region, occupation, income, alcohol, tobacco, pickled vegetable,sowbelly, fruit and vegetable / 8
Wu M, 2006, China / World J Gastroenterol / 531 (incidecne) / 531 population-based controls / Esophageal cancer / Meat
Quartiles
Fish and seafood products
Quartiles / Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4 / Dafeng Conuty
1.0 (Referent)
0.73 (0.29-1.85)
1.66 (0.68-4.10)
1.93 (0.64-5.77)
Ganyu County
1.0 (Referent)
0.54 (0.12-2.42)
1.17 (0.28-4.92)
0.65 (0.11-3.67)
Dafeng Conuty
1.0 (Referent)
1.14 (0.64-2.03)
2.11 (1.12-3.96)
1.91 (1.00-3.64)
Ganyu County
1.0 (Referent)
0.98 (0.42-2.28)
0.64 (0.28-1.44)
1.04 (0.46-2.33) / Age, sex, education, economic status,smoking, alcohol drinking, BMI group, cancerfamily history, eating speed and foodtemperature / 8
Wu AH, 2007, USA / Cancer Causes Control / 206 (incidence) / 1308 population-based controls / Esophageal adenocarcinoma / Total meat & fish
Quartiles
Red meat
Quartiles
Processed meat
Quartiles
Poultry
Quartiles
Fish/shellfish
Quartiles / Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4 / 1.0 (Referent)
0.89 (0.5-1.4)
0.95 (0.6-1.6)
1.26 (0.8-2.1)
1.0 (Referent)
1.08 (0.7-1.8)
0.82 (0.5-1.4)
1.29 (0.8-2.2)
1.0 (Referent)
1.25 (0.8-2.0)
1.17 (0.7-1.9)
1.23 (0.7-2.1)
1.0 (Referent)
1.48 (0.96-2.3)
1.19 (0.7-1.9)
0.93 (0.6-1.5)
1.0 (Referent)
1.01 (0.7-1.6)
1.13 (0.7-1.8)
0.85 (0.5-1.4) / Age, sex, race,birthplace, education,smoking, alcohol, BMI, reflux, use of vitaminsand total calories / 10
Lucenteforte E, 2008, Italy / Int J Cancer / 304 (incidence) / 743 hospital-based controls / Esophageal squamous cell carcinoma / Meat diversity
(times/week) / <3
3-<4
4-<5
≥5 / 1.0 (Referent)
0.66 (0.41-1.07)
0.71 (0.42-1.18)
0.72 (0.47-1.12) / Age, sex, residence, education,tobacco smoking, alcohol drinking and non-alcohol energy intake / 8
Sapkota A, 2008, central and eastern Europe / Cancer Causes Control / 187 (incidence) / 1228 hospital-based controls / Esophageal squamous cell carcinoma / All meats
Tertiles
Red meats
Tertiles
Ham, salami, sausages
Poultry
Fish / T1
T2
T3
T1
T2
T3
<1 times/month
<1 times/week
≥1 times/week
<1 times/month
<1 times/week
≥1 times/week
<1 times/month
<1 times/week
≥1 times/week / 1.0 (Referent)
1.14 (0.75-1.72)
0.93 (0.56-1.56)
1.0 (Referent)
1.35 (0.89-2.06)
1.00 (0.65-1.54)
1.0 (Referent)
1.16 (0.46-2.92)
1.12 (0.52-2.41)
1.0 (Referent)
0.43 (0.18-1.03)
0.47 (0.21-1.03)
1.0 (Referent)
0.80 (0.50-1.27)
0.70 (0.42-1.15) / Age, country, sex, tobacco, education, BMI,alcohol consumption, total vegetable andtotal fruit consumption / 7
Ganesh B, 2009, India / Cancer Epidemiol / 442 (incidence) / 1628 hospital-based controls / Esophageal cancer / Meat
Fresh fish / No
Yes
No
Yes / 1.0 (Referent)
0.7 (0.5–1.1)
1.0 (Referent)
0.8 (0.5–0.9) / Age, place of residence, religion andoccupation, smoking, alcohol and diet / 7
Gao Y, 2011, China / Cancer Epidemiol / 600 (incidence) / 1514 hospital-based controls / Esophageal squamous cell carcinoma / Red meat
Chicken
Fish / Monthly/seldom/never
Weekly
>Weekly
Never
Seldom
Monthly
Daily/weekly
Never
Seldom
Monthly
Daily/weekly / 1.0 (Referent)
1.14(0.89-1.46)
1.37(1.03-1.82)
1.0 (Referent)
1.37(1.03-1.82)
1.14(0.89-1.46)
0.96(0.50-1.88)
1.0 (Referent)
0.59(0.39-0.88)
0.51(0.29-0.91)
0.50(0.28-0.88) / Age, gender, geographic region / 5
Hajizadeh B, 2011, Iran / Nutr Cancer / 47 (incidence) / 96 hospital-based controls / Esophageal squamous cell carcinoma / All meats
(times/month)
All red meats
(times/month)
Processed red meats
(times/month)
Poultry
(times/month)
Fish
(times/month) / 4.00-25.75
25.76-42.08
42.09-86.00
0-8.00
8.01-19.00
19.01-77.00
0-1.00
1.01-5.00
5.01-26.00
0-9.00
9.01-13.00
13.01-34.00
0-1.00
1.01-3.00
3.01-17.00 / 1.0 (Referent)
1.55 (0.50-4.76)
2.82 (0.88-9.04)
1.0 (Referent)
1.40 (0.44-4.44)
2.47 (0.76-7.96)
1.0 (Referent)
1.50 (0.33-6.75)
1.10 (0.36-2.47)
1.0 (Referent)
0.79 (0.31-2.02)
0.85 (0.43-2.07)
1.0 (Referent)
0.45 (0.12-1.57)
0.67 (0.25-1.83) / Age, sex, symptomatic gastresophageal reflux, BMI / 6
Navarro Silvera SA, 2011, USA / Ann Epidemiol / 488 (incidence) / 687
population-based controls / Esophageal cancer (206 ESCC, 282 EAC) / Meat/nitrite
Quartile
Fish/vitamin C
Quartile / Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4 / ESCC
1.0 (Referent)
1.28 (0.69-2.38)
2.28 (1.13-4.61)
2.01 (0.82-4.95)
EAC
1.0 (Referent)
1.48 (0.91-2.42)
3.19 (1.82-5.59)
5.61 (2.81-11.20)
ESCC
1.0 (Referent)
1.41 (0.78-2.57)
1.57 (0.87-2.84)
1.83 (0.99-3.37)
EAC
1.0 (Referent)
1.00 (0.64-1.56)
0.72 (0.45-1.15)
0.94 (0.59-1.48) / Age, sex, site, race, income, education, proxy status, energy intake, and mutual adjustment for other principle components / 7
O'Doherty MG, 2011, Ireland / Int J Cancer / 224 (incidence) / 256 population-based
controls / Esophageal adenocarcinoma / Total meat
(grams/day)
(median)
Total red meat
(grams/day)
(median)
Processed meat
(grams/day)
(median)
White meat
(grams/day)
(median)
Total fish
(grams/day)
(median) / 82.6
118.7
145.4
195.3
54.7
87.6
113.4
161.1
11.1
31.3
53.3
96.1
8.6
18.7
54.8
56.5
9.3
21.7
31.2
57.0 / 1.0 (Referent)
1.08 (0.49-2.39)
0.82 (0.37-1.82)
1.32 (0.63-2.78)
1.0 (Referent)
0.41 (0.17-1.00)
1.34 (0.62-2.88)
1.18 (0.55-2.54)
1.0 (Referent)
1.39 (0.64-3.04)
1.07 (0.50-2.27)
1.41 (0.67-2.95)
1.0 (Referent)
0.93 (0.46-1.89)
0.70 (0.34-1.46)
0.51 (0.23-1.13)
1.0 (Referent)
0.95 (0.44-2.08)
1.49 (0.70-3.18)
1.49 (0.72-3.10) / Age, sex, smoking status, BMI, job type, education,energy intake, fruit intake, vegetable intake, alcohol intake, Helicobacter pylori infection, NSAIDs use, gastroesophageal reflux symptoms, and location (Northern Ireland, Republic of Ireland), and other types of meat. / 9
De Stefani E, 2012, Uruguay / Int J Cancer / 234 (incidence) / 2020 hospital-based controls / Esophageal squamous cell carcinoma / Red meat
Tertiles
Processed meat
Tertiles
White meat
Tertiles / T1
T2
T3
T1
T2
T3
T1
T2
T3 / 1.0 (Referent)
3.62 (2.14-6.13)
4.97 (2.98-8.29)
1.0 (Referent)
1.03 (0.71-1.50)
0.76 (0.51-1.13)
1.0 (Referent)
0.67 (0.47-0.94)
0.56 (0.38-0.82) / Age, gender, residence, education, BMI,smoking, drinking, mate temperature, total energy, total vegetable andfruits intake, and all scored patterns / 9
Ibiebele TI, 2012, Australia / Br J Nutr / 1094 (incidence) / 1580 population-based
controls / Esophageal cancer (303 ESCC, 426 EGJAC, 365 EAC) / Meat and fat
Quartiles / Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4
Q1
Q2
Q3
Q4 / ESCC
1.0 (Referent)
1.15 (0.73-1•82)
1.64 (1.03-2•63)
2.84 (1.67-4•83)
EGJAC
1.0 (Referent)
0.94 (0.62-1·42)
1.27 (0.84-1·91)
1.88 (1.21-2·94)
EAC
1.0 (Referent)
1.14 (0.72-1.80)
1.25 (0.79-1•98)
2.12 (1.30-3•46) / Age, sex, education, BMI, frequency of heartburn or acid reflux, smoking, NSAIDs use, and total energy intake. / 10
a RR = relative risk (odds ratio); CI = confidence interval; BMI = body mass index; MSI=microsatellite instability; NSAID, nonsteroidal anti-inflammatory drug; . ESCC= esophageal squamous cell carcinoma; EGJAC=esophagogastric junction adenocarcinoma; EAC= esophageal adenocarcinoma.