Journal List > Korean J Health Promot > v.18(3) > 1102149

Lee, Lee, Kang, Shim, and Paik: Gender Perspectives on the Relationship between Red and Processed Meat Intake and Colorectal Cancer: A Systematic Review and Meta-Analysis

Abstract

Background

Men and women choose different food items, and consume different amounts of food, due to biological, cultural, and social differences. However, when dietary assessment instruments are developed, gender differences in food selection and/or the portion sizes are often not considered.

Methods

Prospective cohort studies with men and women that examined the association between red or processed meat intake and colorectal cancer and published up to July 2017, were identified using PubMed. Studies were categorized as gender-specific (GS) group if the Food Frequency Questionnaire was developed using gender-specific data, and as not gender-specific (NGS) group if not gender-specific data were used.

Results

For cohort studies that reported combined intake estimates of men and women, a 100 g/day increment in red and processed meat intake was positively associated with a risk of colorectal or colon cancer in GS group (relative risk [RR], 1.23; 95% confidence interval [CI], 1.14–1.32) but not in NGS group (RR, 1.13; 95% CI, 0.90–1.35). For processed meat, the RR for 50 g/day increase was 1.28 (95% CI, 1.15–1.40) in GS group and 1.15 (95% CI, 1.03–1.27) in NGS group.

Conclusions

Gender differences need to be considered during development of dietary assessment tools because this may improve the quality of the findings of nutritional epidemiological studies.

References

1. Gender, women and Health. [Internet]. Geneva: World Health Organization;2015. [Accessed August 31, 2017] Available from:. https://www.legal-tools.org/doc/a33dc3/pdf/.
2. Schiebinger L, Schraudner M. Interdisciplinary approaches to achieving gendered innovations in science, medicine, and engineering. Interdiscip Sci Rev. 2011; 36(2):154–67.
3. Bates CJ, Prentice A, Finch S. Gender differences in food and nutrient intakes and status indices from the National Diet and Nutrition Survey of people aged 65 years and over. Eur J Clin Nutr. 1999; 53(9):694–9.
4. Wardle J, Haase AM, Steptoe A, Nillapun M, Jonwutiwes K, Bellisle F. Gender differences in food choice: the contribution of health beliefs and dieting. Ann Behav Med. 2004; 27(2):107–16.
crossref
5. Turrell G. Determinants of gender differences in dietary behavior. Nutr Res. 1997; 17(7):1105–20.
crossref
6. Brug J, Tak NI, te Velde SJ, Bere E, de Bourdeaudhuij I. Taste preferences, liking and other factors related to fruit and vegetable intakes among schoolchildren: results from observational studies. Br J Nutr. 2008; 99(Suppl 1):S7–14.
crossref
7. Blaak E. Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care. 2001; 4(6):499–502.
crossref
8. Tarnopolsky MA. Females and males: should nutritional recommendations be gender specific? Schweiz Z Med Traumatol. 2003; 51(1):39–46.
9. Wu BN, O'Sullivan AJ. Sex differences in energy metabolism need to be considered with lifestyle modifications in humans. J Nutr Metab. 2011; 2011:391809.
crossref
10. Lee H, Kang M, Song WO, Shim JE, Paik HY. Gender analysis in the development and validation of FFQ: a systematic review. Br J Nutr. 2016; 115(4):666–71.
crossref
11. Willett W. Nutritional epidemiology. 3rd ed.New York: Oxford University Press;2012. p. 70–141.
12. Bouvard V, Loomis D, Guyton KZ, Grosse Y, Ghissassi FE, Benbrahim-Tallaa L, et al. Carcinogenicity of consumption of red and processed meat. Lancet Oncol. 2015; 16(16):1599–600.
crossref
13. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000; 283(15):2008–12.
14. Sato Y, Nakaya N, Kuriyama S, Nishino Y, Tsubono Y, Tsuji I. Meat consumption and risk of colorectal cancer in Japan: the Miyagi cohort study. Eur J Cancer Prev. 2006; 15(3):211–8.
crossref
15. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7(3):177–88.
crossref
16. Orsini N, Bellocco R, Greenland S. Generalized least squares for trend estimation of summarized doseresponse data. Stata J. 2006; 6(1):40–57.
crossref
17. Chan DS, Lau R, Aune D, Vieira R, Greenwood DC, Kampman E, et al. Red and processed meat and colorectal cancer incidence: metaanalysis of prospective studies. PLoS One. 2011; 6(6):e20456.
crossref
18. Kang M, Park S, Boushey CJ, Wilkens LR, et al. Portion sizes from 24-hour dietary recalls differed by sex among those who selected the same portion size category on a food frequency questionnaire. J Acad of Nutr Diet. 2018; 118(9):1711–8.
crossref
19. Marks GC, Hughes MC, van der Pols JC. The effect of personal characteristics on the validity of nutrient intake estimates using a food-frequency questionnaire. Public Health Nutr. 2006; 9(3):394–402.
crossref
20. Marks GC, Hughes MC, van der Pols JC. Relative validity of food intake estimates using a food frequency questionnaire is associated with sex, age, and other personal characteristics. J Nutr. 2006; 136(2):459–65.
crossref
21. Cade JE, Burley VJ, Warm DL, Thompson RL, Margetts BM. Food-frequency questionnaires: a review of their design, validation and utilisation. Nutr Res Rev. 2004; 17(1):5–22.
crossref
22. Berndt SI, Platz EA, Fallin MD, Thuita LW, Hoffman SC, Helzlsouer KJ. Genetic variation in the nucleotide excision repair pathway and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev. 2006; 15(11):2263–9.
crossref
23. Chao A, Thun MJ, Connell CJ, McCullough ML, Jacobs EJ, Flanders WD, et al. Meat consumption and risk of colorectal cancer. JAMA. 2005; 293(2):172–82.
crossref
24. Takachi R, Tsubono Y, Baba K, Inoue M, Sasazuki S, Iwasaki M, et al. Red meat intake may increase the risk of colon cancer in Japanese, a population with relatively low red meat consumption. Asia Pac J Clin Nutr. 2011; 20(4):603–12.
25. English DR, MacInnis RJ, Hodge AM, Hopper JL, Haydon AM, Giles GG. Red meat, chicken, and fish consumption and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev. 2004; 13(9):1509–14.
26. Cross AJ, Leitzmann MF, Gail MH, Hollenbeck AR, Schatzkin A, Sinha R. A prospective study of red and processed meat intake in relation to cancer risk. PLoS Med. 2007; 4(12):e325.
crossref
27. Singh PN, Fraser GE. Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol. 1998; 148(8):761–74.
crossref
28. Norat T, Bingham S, Ferrari P, Slimani N, Jenab M, Mazuir M, et al. Meat, fish, and colorectal cancer risk: the European prospective investigation into cancer and nutrition. J Natl Cancer Inst. 2005; 97(12):906–16.
29. Järvinen R, Knekt P, Hakulinen T, Rissanen H, Heliövaara M. Dietary fat, cholesterol and colorectal cancer in a prospective study. Br J Cancer. 2001; 85(3):357–61.
crossref
30. Knekt P, Järvinen R, Dich J, Hakulinen T. Risk of colorectal and other gastrointestinal cancers after exposure to nitrate, nitrite and N-nitroso compounds: a follow-up study. Int J Cancer. 1999; 80(6):852–6.
31. Iso H, Kubota Y. Japan Collaborative Cohort Study for Evaluation of Cancer. Nutrition and disease in the Japan collaborative cohort study for evaluation of cancer (JACC). Asian Pac J Cancer Prev. 2007; 8(Suppl):35–80.
32. Ollberding NJ, Wilkens LR, Henderson BE, Kolonel LN, Le Marchand L. Meat consumption, heterocyclic amines and colorectal cancer risk: the Multiethnic Cohort Study. Int J Cancer. 2012; 131(7):E1125–33.
crossref
33. Chen J, Stampfer MJ, Hough HL, Garcia-Closas M, Willett WC, Hennekens CH, et al. A prospective study of N-acetyltransferase genotype, red meat intake, and risk of colorectal cancer. Cancer Res. 1998; 58(15):3307–11.
34. Balder HF, Vogel J, Jansen MC, Weijenberg MP, van den Brandt PA, Westenbrink S, et al. Heme and chlorophyll intake and risk of colorectal cancer in the Netherlands cohort study. Cancer Epidemiol Biomarkers Prev. 2006; 15(4):717–25.
crossref
35. Wada K, Oba S, Tsuji M, Tamura T, Konishi K, Goto Y, et al. Meat consumption and colorectal cancer risk in Japan: the Takayama study. Cancer Sci. 2017; 108(5):1065–70.
crossref

Figure 1.
Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flowchart. Screening and selection of studies analysing the association between meat (red and processed/red/processed) intake and Colorectal cancer risk.
kjhp-18-127f1.tif
Figure 2.
Dose-response meta-analysis between red and processed meat and colorectal or colon cancer in male and female combined cohort studies (P for difference=0.340).
kjhp-18-127f2.tif
Figure 3.
Highest vs. lowest meta-analysis between red and processed meat and colorectal or colon cancer in male and female combined cohort studies (P for difference=0.022).
kjhp-18-127f3.tif
Table 1.
Characteristics of cohort studies included in the meta-analysis
Study Cohort Ethnicity (% of subjects) Baseline population No. of cases Age at baseline Study period (follow-up years) Meat category (intake in quantiles)
GS Group              
  Berndt et al22) (2006) CLUE II Caucasian (98.3%) Men:932 Women:1,292 CRC:202 >35 (mean 48.5) 1996–2003 (mean 13.5) Red and processed meat (T1:<44.0g, T3:≥86.3g)
  Chao et al 23) (2005) CPS II Caucasian (98.0%) Men:69,644 Women:78,946 CC:1,197 RC:470 50–74 (median 63) 1992–2001 Red and processed meat (median) (men Q1: 14.3g, Q5:142.7 g; women Q1:6.1 g, Q5: 101.7g) processed meat (median) (men Q1:1.4 g, Q5:40.4 g; women Q1:O g, Q5:20.7g)
  Takachi et al 24) (2011) JPHC Asian Men:38,462 Women:42,196 CRC:1,145 CC:788 45–74 (mean 56.6) 1995,1999–2006 Red and processed meat (median) (men Q1: 20g, Q5:117 g; women Q1:18 g, Q5: 107 g) Red meat (median) (men Q1:15 g, Q5:102 g; women Q1:14 g, Q5:93 g) Processed Meat (Median) (Men Q1: 0.2g, Q5: 16 g; women Q1:0.4 g, Q5:15 g)
  English et al 25) (2004) MCCS Caucasian Men:14,643 Women:22,469 CRC:451 CC:283 RC:169 27–75 1990,1994–2006 (average 9) Red meat (Q1: <51.4 g, Q4:≥111.4 g) Processed meat (Q1:10.7 g, Q4: 28.6 g)
  Sato et al 14) (2006) Miyagi cohort Asian Men:20,174 Women:21,661 CRC:474 CC:280 RC:198 40–64 (mean 52) 1990–2001 (11) Processed meat (median) (Q1:0 g, Q4: 15.8 g)
  Cross et al 26) (2007) NIH-AARP Caucasian (92.6%) Men:294,724 Women:199,312 CRC:5,107 50–71 (mean 62) 1996–2003 (mean 6.8) Red and processed meat (median) (Q1:9.8 g/1,000 kcal, Q5: 62.7 g/1000 kcal)
NGS Group              
  Singh and Fraser 27) (1998) AHS Caucasian (100.0%%) Men and Women:32,051 CC:135 RC:22 ≥25 1977–1982 (6) Red meat (T1:0 g, T3: 17.1g)
  Norat et al28) (2005) EPIC Caucasian (>97.0%) Men:141,987 Women:336,052 CRC:1,329 CC:855 RC:474 35–70 (mean 51.2) 1992–1998 (mean 4.8) Red and processed meat (Q1:<10 g, Q5≥160 g) Red meat (Q1:<10 g, Q5≥160 g) Processed meat (Q1:<10 g, Q5:≥80 g)
  Järvinen et al 29) (2001) FMCHES Caucasian (100.0%) Men and Women:9,959 CRC:109 CC:63 RC:46 ≥15 (mean 39.1) 1967–1999 (max 32) Red meat (Men Q1:<94 g, Q4>206 g;women Q1: <61 g, Q4:>134g)
  Knekt et al 30) (1999) FMCHES Caucasian (100.0%) Men:5,274 Women:4,711 CRC:73 ≥15 1967–1990 (max 24) Meat and meat products
  Iso et al 31) (2007) JACC Asian Men:44,647 Women:60,992 CC:354 RC:211 40–79 1988–2003 Processed Meat (men T1:<7.1 g, T3:≥21.4 g)
  Ollberding et al 32) (2012) MEC Mixed Men:76,893 Women:88,824 CRC:3,404 45–75 (mean 59.9) 1993–2007 (median 13.6) Red and processed meat (g/1,000 kcal) (Q1: median 7.4g, Q5: median 48.0 g) Red meat (g/1,000 kcal) (Q1: Median 4.6 g, Q5:median 34.9 g) Processed meat (g/1,000 kcal) (Q1:median 1.7 g, Q5: median 18.0 g)
  Chen et al 33) (1998) SCHS Asian Men and Women:61,321 CRC:961 CC:591 RC:370 45–74 1993–2005 (average 9.8) Red Meat (median intake) (case:24 g, noncase:25 g) Processed meat (median intake) (case:1.2 g, noncase:1.3g)
  Balder et al 34) (2006) NLCS Caucasian Men:58,279 Women:62,573 CRC:1,535 55–69 1986-(9.3) Processed Meat (Q1: 0 g, Q5≥20 g [median 32 g])
  Wada et al 35) (2017) Takayama cohort Asian Men:13,957 Women:16,374 CRC:709 CC:222 RC:236 ≥35 (mean 55.7) 1992–2008 Red Meat (median intake) (men Q1:19 g, Q4:64 g; women Q1: 12g, Q4: 49g) Processed meat (median intake) (men Q1:4 g, Q4:23 g; women Q1: 3 g, Q4: 19 g)

Abbreviations: GS, gender-specific; CLUE II, ‘give us a clue to cancer’ study; CRC, colorectal cancer; CC, colon cancer; RC, rectal cancer; JPHC, Japan Public Health Center-based Prospective Study; MCCS, Melbourne Collaborative Cohort Study; NIH-AARP, American Association of Retired Persons' Diet and Health Study; NGS, not gender-specific; AHS, Adventist Health Study; EPIC, European Prospective Investigation into Cancer and Nutrition; FMCHES, Finnish Mobile Clinic Health Examination Survey; JACC, Japan Collaborative Cohort Study; MEC, multiethnic cohort study; SCHS, Singapore Chinese Health Study; NLCS, Netherlands Cohort Study.

Table 2.
Summary of the estimated RRs and 95% CIs for colorectal or colon cancer risk
  Dose-responsea Highest vs. lowest
N RR 95% CI P for differences Ref.b N RR 95% CI P for differences Ref. b
Red and processed meat       0.340         0.022  
   GS 4 1.23 1.14, 1.32   22,23,24,26) 4 1.24 1.14, 1.34   22,23,24,26)
   NGS 2 1.13 0.90, 1.35   28,35) 2 1.11 0.82, 1.39   28,35)
   Total 6 1.17 1.06, 1.29     6 1.18 1.05, 1.30    
Red meat     NAc         NAc    
   GS 1       25) 1       25)
   NGS 5       27,28,29,32,35) 5       28,29,32,33,35)
   Total 6         6        
Processed meat       0.168         0.409  
   GS 5 1.28 1.15, 1.40   14,23,24,25,26) 5 1.18 1.07, 1.28   14,23,24,25,26)
   NGS 3 1.16 1.04, 1.28   28,34,35) 7 1.12 1.03, 1.21   28,30,31,32, 33,34,35)
   Total 8 1.21 1.13, 1.30     12 1.15 1.08, 1.21    

Abbreviations: RR, relative risk; CI, confidence intervals; Ref., reference; GS, gender-specific; NGS, not gender-specific; NA, not available.

a Dose-response analysis: RR of 100 g/day increase in red and processed meat or red meat and RR of 50 g/day increase in processed meat.

b List of reference number included in summary of RR.

c Summary estimates were not calculated if number of studies was 1 or less in either GS or NGS group.

TOOLS
Similar articles