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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

Original Article

Published online: January 10, 2018

DOI: https://doi.org/10.15384/kjhp.2018.18.3.127

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

Han Na Lee1, Jung Eun Lee2,3, Minji Kang1, Jae Eun Shim4,5, Hee-Young Paik1,2,

1Center for Gendered Innovations in Science and Technology Research (GISTeR), Korea Federation of Women's Science & Technology Associations, Seoul, Korea

2Department of Food and Nutrition, Seoul National University, Seoul, Korea

3Research Institute of Human Ecology, Seoul National University, Seoul, Korea

4Department of Food and Nutrition, Daejeon University, Daejeon, Korea

5Daejeon Dong-gu Center for Children's Food Service Management, Daejeon, Korea

￭ Corresponding author: Hee-Young Paik, ScD Center for Gendered Innovations in Science and Technology Researches (GISTeR), Korea Federation of Women's Science & Technology Associations, 22, Teheran-ro 7-gil, Gangnam-gu, Seoul 06130, Korea
Tel: +82-2-565-3701, Fax: +82-2-3452-2912 E-mail: hypaik@kofwst.org

￭ This research was supported by Support Program for Women in Science, Engineering and Technology through the National Research Foundation of Korea (NRF) funded by the Ministry of Science and ICT (No. 2016H1C3A1903202).

Received July 26, 2018       Accepted September 19, 2018

Copyright © 2018 The Korean Society of Health Promotion and Disease Prevention

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
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.

Key words: Gender; Red meat; Processed meat; Colorectal neoplasms; Surveys and questionnaires

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.

aDose-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.

bList of reference number included in summary of RR.

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

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