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

Han Na Lee; Jung Eun Lee; Minji Kang; Jae Eun Shim; Hee-Young Paik

doi:10.15384/kjhp.2018.18.3.127

Korean J Health Promot > Volume 18(3); 2018 > Article

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

Korean Journal of Health Promotion 2018;18(3):127-137.

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 Lee^2,³, Minji Kang¹, Jae Eun Shim^4,⁵, Hee-Young Paik^1,^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

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.

Keywords: 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.

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).

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).

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-response^a					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			NA^c					NA^c
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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