Introduction
Review
Literature search and study identification
Data extraction and statistical analysis
Results
Author, year | Study cohort (Country) | No. of subjects (No. of cases) | Age range (mean) | Year baseline diet assessed | Follow up, years | Meat exposures analyzed | Prostate cancer outcome | Statistical adjustments |
---|---|---|---|---|---|---|---|---|
Agalliu et al, 2011 [13] | Canadian Study of Diet, Lifestyle and Health (Canada) | 1864 (661) | 69.3 (10.5) [mean (SD) controls]; 66.2 (8.4) [mean (SD) cases] | 1995–1998 | 8 | Red meat | All PCa; nonadvanced PCa; advanced PCa | Age at baseline, race, BMI, exercise activity, and education |
Allen et al, 2004 [29] | Life Span Study Cohort (Japan) | 18,119 (196) | 51–89 | 1979–1980 | 16.9 [mean] | Pork | All PCa | Age, calendar period, city of residence, radiation dose and education level |
Allen et al, 2008 [30] | EPIC (Europe) | 142,241 (2727) | 52 [median] | 1989–2004 | 18 | Red meat; processed meat | All PCa | Study center, education, marital status, height, weight, and energy intake |
Cross et al, 2005 [47] | PLCO (US) | 29,361 (1338) | 55–74 | 1993–2001 | 11 | Red meat; processed meat | Total PCa; incident PCa; advanced PCa | Age, race, study center, fam hx, history of diabetes, number of screening exams during follow-up, smoking status, physical activity, aspirin use, BMI, and intake of total energy, supplemental vitamin E, and lycopene |
Gann et al, 1994 [32] | PHS (US) | 240 (120) | 40–84 | 1982 | 6 | Beef, pork, or lamb as a main dish | All PCa | None reported |
Hsing et al, 1990 [33] | LBC (US) | 17,633 (149) | ≥35 | 1966 | 20 | Red meat (processed and unprocessed) | Fatal PCa | Age, tobacco use |
Koutros et al, 2008 [34] | AHS (US) | 23,080 (668) | 48.3 [mean] | 1993–1997 | 10 | Red meat; pork chops/ham steaks; beef steaks; hamburgers; bacon/sausage | Total PCa; incident PCa; advanced PCa | Age, state of residence, race, fam hx, and smoking status |
Le Marchand et al, 1994 [35] | Hawaiian State Department of Health (US) | 8881 (198) | ≥18 | 1975–1980 | 14 | Pork; beef | Total PCa; localized stage PCa; regional and distant stage PCa | Age, ethnicity, and income |
Major et al, 2011 [19] | NIH-AARP (US) | 7949 (1089) (Blacks only) | 50–71 | 1995–1996 | 11 | Red meat; processed meat | Total PCa; Advanced PCa | Age, education, marital status, fam hx, hx of diabetes, smoking, health status, BMI, alcohol, fruit intakes |
Michaud et al, 2001 [36] | HPFS (US) | 47,780 (1987) | 40–75 | 1986 | 10 | Red meat; beef, pork, lamb (main dish); beef, pork, lamb (sandwich or mixed dish); hamburger, processed meat (sausage, salami, bologna); bacon; hot dogs | Total PCa, Advanced PCa | Age, calories, calcium, smoking, tomato use, vigorous exercise, saturated and alpha linolenic fat |
Mills et al, 1989 [37] | Seventh Day Adventists (US) | 14,000 (180) | ≥25 | 1976 | 6 | Beef hamburger; beef steak; other beef and veal; beef index | All PCa | Age |
Neuhouser et al, 2007 [38] | CAROT (US) | 12,000 (890) | 50–69 | 1989 | 11 [mean] | Red meat | Total PCa; aggressive PCa; nonaggressive PCa | Age, energy intake, BMI, smoking, fam hx, and race/ethnicity |
Park et al, 2007 [39] | Multiethnic Cohort (US) | 82,483 (4404) | ≥45 | 1993–1996 | 8 | Red meat; beef; pork; processed meat | Total PCa; non-localized or high grade PCa; | Time on study, ethnicity, family history of prostate cancer, education, BMI, smoking status and energy intake |
Richman et al, 2011 [15] | HPFS (US) | 27,607 (199) | 40–75 | 1986 | 22 | Total red meat (processed and unprocessed); unprocessed red meat; processed red meat | Lethal PCa | Age, energy, BMI, smoking, vigorous activity, and lycopene intake |
Rodriguez et al, 2006 [40] | Cancer Prevention Study II (US) | 65,590 (5113) | 50–74 | 1992 | 9 | Total red meat (processed and unprocessed); unprocessed red meat; | All PCa; metastatic PCa | Age at entry, total calorie intake, BMI, level of education, fam hx, history of PSA testing, and hx of diabetes |
Rohrmann et al, 2007 [41] | CLUE II (US) | 3892 (199) | ≥35 | 1989 | 15 | Red meat (processed and unprocessed); beef; pork; processed meats; sausages; bacon; ham/lunchmeat; hot dogs | Total PCa; low-stage PCa; high-stage PCa | Age, energy intake, consumption of tomato products, BMI at age 21, and intake of saturated fat |
Schuurman et al, 1999 [42] | NLCS (Netherlands) | 2167 (642) | 55–69 | 1986 | 6.3 | Beef; pork; minced meat (beef and pork); boiled ham; bacon | Total PCa; localized tumors; advanced tumors | Age, fam hx, and socioeconomic status |
Severson et al, 1989 [43] | Hawaiian Men of Japanese Ancestry (US) | 7998 (174) | 46–65 | 1965–1968 | 21 | Ham, bacon, sausage | Total PCa | Age |
Sinha et al, 2009 [44] | NIH-AARP (US) | 175,343 (10,313) | 50–71 | 1995–1996 | 8 | Red meat (processed and unprocessed); processed meat | Total PCa; advanced PCa; fatal PCa | Age, total energy intake, race/ethnicity, education, marital status, undergoing prostate-specific antigen testing in the past 3 years, hx of diabetes, BMI, smoking history, frequency of vigorous physical activity, and intakes of alcohol, calcium, tomatoes, alpha-linolenic acid, vitamin E, zinc, and selenium |
Veierod et al, 1997 [45] | Norwegian men 1977–1983 (Norway) | 25,708 (72) | 16–56 | 1977–1983 | 15 | Main meals with hamburgers, meatballs, etc. | Total PCa | Age at inclusion and attained age |
Wright et al, 2012 [14] | ATBC (Finland) | 27,111 (1929) | 50–69 | 1985–1988 | 21 | Red meat; beef; sausages | All PCa; advanced PCa | Age, energy intake, smoking dose and duration, trial intervention assignment, education level, and dietary fat intake |
Wu et al, 2006 [28] | HPFS | 47,725 (3002) | 40–75 | 1986 | 14 | Total red meat, processed meat | Advanced PCa | Age, height, smoking, family history of prostate cancer, race, history of vasectomy, vigorous exercise, body mass index, alcohol intake, and total energy intake |
Model (number of studies a or data points†) | SRRE | 95 % CI |
P-value for Heterogeneity; I2
|
---|---|---|---|
Total red meat | |||
Total red meat and total prostate cancer (n = 10) | 1.02 | 0.92–1.12 | 0.006; 61.0 % |
Per 1 serving/day increase
| 0.96 | 0.91–1.00 | |
Intake of 0–0.50 servings/day (n = 5)
| 1.41 | 1.09–1.81 | 0.189; 34.85 % |
Intake of >0.50–1.0 servings/day (n = 13)
| 1.02 | 0.98–1.05 | 0.735; 0.00 % |
Intake of >1.0–1.5 servings/day (n = 10)
| 1.01 | 0.93–1.10 | 0.077; 42.07 % |
Intake of >1.0 servings/day (n = 7)
| 0.88 | 0.75–1.04 | 0.005; 67.68 % |
Total red meat and non-advanced prostate cancer (n = 3) | 0.98 | 0.63–1.53 | 0.051; 66.3 % |
Per 1 serving/day increase
| 0.71 | 0.46–1.10 | |
Intake of <1 serving/day (n = 4)
| 1.10 | 0.92–1.31 | 0.619; 0.00 % |
Intake of >1 serving/day (n = 5)
| 0.89 | 0.66–1.19 | 0.060; 55.69 % |
Total red meat and advanced prostate cancer (n = 9) | 1.01 | 0.86–1.17 | 0.177; 30.2 % |
Per 1 serving/day increase
| 0.97 | 0.91–1.04 | |
Intake of 0–0.75 servings/day (n = 9)
| 1.08 | 0.94–1.23 | 0.319; 13.78 % |
Intake of >0.75–1.0 servings/day (n = 4)
| 1.06 | 0.92–1.23 | 0.697; 0.00 % |
Intake of >1.0–1.5 servings/day (n = 8)
| 1.04 | 0.92–1.18 | 0.481; 0.00 % |
Intake of >1.0 servings/day (n = 4)
| 1.14 | 0.95–1.37 | 0.328; 12.95 % |
Total red meat and fatal prostate cancer (n = 3) | 1.06 | 0.82–1.37 | 0.35; 4.80 % |
Per 1 serving/day increase
| 1.05 | 0.73–1.52 | |
Intake of <1 serving/day (n = 5)
| 1.09 | 0.91–1.30 | 0.350; 9.89 % |
Intake of >1 serving/day (n = 5)
| 1.15 | 0.96–1.38 | 0.474; 0.00 % |
Fresh red meat | |||
Fresh red meat and total prostate cancer (n = 9) | 1.06 | 0.97–1.16 | 0.113; 38.3 % |
Per 1 serving/day increase
| 0.91 | 0.81–1.03 | |
Intake of 0- < 0.25 servings/day (n = 9)
| 1.08 | 0.97–1.19 | 0.924; 0.00 % |
Intake of 0.25- < 0.5 servings/day (n = 8)
| 1.07 | 1.02–1.13 | 0.519; 0.00 % |
Intake of 0.5–0.75 servings/day (n = 6)
| 1.04 | 0.97–1.12 | 0.363; 8.28 % |
Intake of >0.75 servings/day (n = 9)
| 1.07 | 0.95–1.19 | 0.171; 30.95 % |
Fresh red meat and advanced prostate cancer (n = 6) | 1.01 | 0.86–1.20 | 0.180; 34.107 % |
Per 1 serving/day increase
| 0.88 | 0.69–1.12 | |
Intake of 0–0.25 servings/day (n = 9)
| 1.14 | 0.97–1.34 | 0.776; 0.00 % |
Intake of >0.25–0.50 servings/day (n = 8)
| 0.99 | 0.89–1.10 | 0.543; 0.00 % |
Intake of >0.50 servings/day (n = 10)
| 0.99 | 0.89–1.11 | 0.398; 4.66 % |
Processed meat | |||
Processed red meat and total prostate cancer (n = 11) | 1.05 | 1.01–1.10 | 0.406; 3.38 % |
Per 1 serving/day increase
| 1.01 | 0.96–1.05 | |
Intake of 0–0.25 servings/day (n = 9)
| 1.05 | 0.99–1.10 | 0.369; 7.93 % |
Intake of >0.25–0.50 servings/day (n = 12)
| 1.05 | 1.00–1.09 | 0.407; 3.91 % |
Intake of >0.50–0.75 servings/day (n = 6)
| 1.02 | 0.97–1.07 | 0.506; 0.00 % |
Intake of >0.75 servings/day (n = 10)
| 1.04 | 0.99–1.10 | 0.176; 29.20 % |
Processed meat and advanced prostate cancer (n = 8) | 1.12 | 0.95–1.33 | 0.040; 52.4 % |
Per 1 serving/day increase
| 1.10 | 0.98–1.24 | |
Intake of 0–0.25 servings/day (n = 12)
| 0.95 | 0.80–1.12 | 0.004; 60.09 % |
Intake of >0.25–0.50 servings/day (n = 9)
| 1.07 | 0.90–1.26 | 0.009; 60.61 % |
Intake of >0.50 servings/day (n = 8)
| 1.13 | 0.99–1.29 | 0.116; 39.42 % |
Processed meat and fatal prostate cancer (n = 2) | 1.09 | 0.63–1.90 | 0.073; 68.9 % |
Per 1 serving/day increase
| 0.84 | 0.44–1.61 | |
Intake of <0.50 servings/day (n = 4)
| 0.93 | 0.75–1.15 | 0.276; 22.49 % |
Intake of >0.50 servings/day (n = 3)
| 0.95 | 0.69–1.30 | 0.112; 54.36 % |
Total red meat
Fresh red meat
Processed meat
Cooking methods and heterocyclic amines
Author, year | Study cohort (Country) | No. of subjects (No. of cases) | Age range (mean) | Year baseline diet assessed | Follow-up, years | Meat cooking methods exposures analyzed | Heterocyclic amine or heme iron exposures analyzed | Prostate cancer outcome |
---|---|---|---|---|---|---|---|---|
Cross et al, 2005 [47] | PLCO (US) | 29,361 (1338) | 55–74 | 1993–2001 | 11 | Barbequed meat; panfried meat; very well-done meat | DiMeIQx; MeIQx; PhIP; B(a)P; Mutagenic activity | Total PCa; incident PCa; advanced PCa |
Jackszyn 2012 [50] | EPIC (Europe) | 139,005 (4606) | >30 | 1989–2004 | 11 | None | Heme iron | Total PCa, advanced PCa, localized PCa |
Koutros et al, 2008 [34] | AHS (US) | 23,080 (668) | 48.3 [mean] | 1993–1997 | 10 | Grilled meat; pan-fried meat; broiled meat; rare or medium cooked meat; well and very well done cooked meat | DiMeIQx; MeIQx; PhIP; B(a)P; Mutagenic activity | Total PCa; incident PCa; advanced PCa |
Rohrmann et al, 2015 [49] | HPFS (US) | 26,030 (2770) | 40–75 | 1996 | 14 | None | MeIQx; DiMeIQx; PhIP; Meat-Derived Mutagenicity Index | Total PCa, advanced or lethal PCa |
Sander et al, 2011 [16] | EPIC-Heidelberg (Germany) | 9578 (337) | 40–65 | 2002–2004 | 7 | Degree of browning: strong/extreme; light/moderate | DiMeIQx; MeIQx; PhIP | Total PCa; advanced PCa |
Sharma et al, 2010 [18] | Multiethnic Cohort (US) | 4169 (2106) | 45–75 | 1993–1996 | 8 | Meat preference: medium; well done | None | Total PCa |
Sinha et al, 2009 [44] | NIH-AARP (US) | 175,343 (10,313) | 50–71 | 1995–1996 | 8 | Grilled/barbequed meat; pan-fried meat; broiled meat; microwaved meat; rare/medium cooked meat; well = done | DiMeIQx; MeIQx; PhIP; B(a)P; heme iron | Total PCa; advanced PCa; fatal PCa |
Model (number of studies) | SRRE | 95 % CI |
P-value for Heterogeneity; I2
|
---|---|---|---|
Cooking methods | |||
Total Prostate Cancer: | |||
Grilled/Barbequed meats (n = 3) | 1.06 | 0.94–1.20 | 0.171; 45.5 % |
Pan-fried meats (n = 3) | 1.00 | 0.96–1.05 | 0.763; 0.00 % |
Broiled meats (n = 2) | 1.04 | 1.00–1.09 | 0.451; 0.00 % |
Well-done/Very well done meats (n = 5) | 1.09 | 0.95–1.26 | 0.062; 55.4 % |
Rare/Medium meats (n = 4) | 1.01 | 0.91–1.12 | 0.245; 27.9 % |
Advanced Prostate Cancer: | |||
Grilled/Barbequed meats (n = 3) | 1.19 | 0.94–1.51 | 0.181; 41.5 % |
Pan-fried meats (n = 3) | 0.97 | 0.77–1.22 | 0.140; 49.2 % |
Broiled meats (n = 2) | 1.00 | 0.87–1.14 | 0.830; 0.00 % |
Well-done/Very well done meats (n = 4) | 1.24 | 0.90–1.71 | 0.075; 56.5 % |
Rare/Medium meats (n = 3) | 1.09 | 0.88–1.34 | 0.331; 9.57 % |
Heterocyclic amines | |||
Total Prostate Cancer: | |||
DiMeIQx (n = 5) | 1.03 | 0.97–1.09 | 0.530; 0.00 % |
MeIQx (n = 5) | 1.06 | 0.96–1.16 | 0.198; 33.5 % |
PhIP (n = 5) | 1.05 | 0.96–1.14 | 0.211; 31.6 % |
Sensitivity analysis including “PhIP from red meat from Rohrmann 2015” | 1.07 | 0.96–1.20 | 0.073; 53.4 % |
B(a)P (n = 3) | 1.01 | 0.90–1.14 | 0.169; 43.8 % |
Mutagenic activity (n = 3) | 1.09 | 1.00–1.20 | 0.725; 0.00 % |
Advanced Prostate Cancer: | |||
DiMeIQx (n = 5) | 1.10 | 0.94–1.29 | 0.747; 0.00 % |
MeIQx (n = 5) | 0.93 | 0.78–1.11 | 0.931; 0.00 % |
PhIP (n = 5) | 0.97 | 0.83–1.14 | 0.668; 0.00 % |
Sensitivity analysis including “PhIP from red meat from Rohrmann 2015” | 1.05 | 0.86–1.30 | 0.192; 34.3 % |
B(a)P (n = 3) | 1.00 | 0.74–1.36 | 0.074; 61.9 % |
Mutagenic activity (n = 3) | 1.04 | 0.84–1.28 | 0.412; 0.00 % |