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Title: Meat consumption and cancer risk: a critical review of

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Author: <ce:author id="aut0005" biographyid="vt0005"

orcid="0000-0001-9523-9054"> Giuseppe Lippi Camilla
Mattiuzzi Gianfranco Cervellin

PII: S1040-8428(15)30078-0
DOI: http://dx.doi.org/doi:10.1016/j.critrevonc.2015.11.008
Reference: ONCH 2080

To appear in: Critical Reviews in Oncology/Hematology

Received date: 5-3-2015

Revised date: 27-10-2015
Accepted date: 12-11-2015

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Meat consumption and cancer risk: a critical review of published
meta-analyses.
Short title: Meat consumption and cancer risk.
Giuseppe Lippi1* giuseppe.lippi@univr,it, [email protected], Camilla Mattiuzzi2, Gianfranco
Cervellin3
1
Section of Clinical Biochemistry, University of Verona, Verona, Italy.
2
Service of Clinical Governance, General Hospital of Trento, Trento, Italy.
3
Emergency Department, Academic Hospital of Parma, Parma, Italy.
*
Corresponding author at: University Hospital of Verona, Piazzale L.A. Scuro 10,
37134 - Verona, Italy. Tel.: 0039-045-8074308.

1
Highlights

 Diet plays a substantial role for increasing or reducing the risk of cancer

 We reviewed 42 meta-analyses assessing the association between meat and cancer

 Increased red and processed meat consumption was associated with cancer risk

 White meat or poultry consumption was negatively associated with some types of

cancer

 Higher beef consumption was associated with some cancers

2
Abstract

Dietary habits play a substantial role for increasing or reducing cancer risk. We

performed a critical review of scientific literature, to describe the findings of meta-

analyses that explored the association between meat consumption and cancer risk.

Overall, 42 eligible meta-analyses were included in this review, in which meat

consumption was assumed from sheer statistics. Convincing association was found

between larger intake of red meat and cancer, especially with colorectal, lung,

esophageal and gastric malignancies. Increased consumption of processed meat was

also found to be associated with colorectal, esophageal, gastric and bladder cancers.

Enhanced intake of white meat or poultry was found to be negatively associated with

some types of cancers. Larger beef consumption was significantly associated with

cancer, whereas the risk was not increased consuming high amounts of pork. Our

analysis suggest increased risk of cancer in subjects consuming large amounts of red

and processed meat, but not in those with high intake of white meat or poultry.

Keywords: Meat; Red meat; Processed meat; Cancer; Neoplasm; Risk.

3
1. Introduction

Cancer is one of the leading causes of morbidity and death around the globe,

averaging approximately 14 million new cases and 8.2 million cancer-related deaths

each year. Even more importantly, the number of new cancer cases is expected to rise

by nearly 70% over the next two decades, up to 22 million new cases per year, which

would probably make it the first cause of mortality worldwide (1). The five most

common types of malignancies are represented by lung, prostate, colorectal, stomach,

and liver cancers in men, whereas breast, colorectal, lung, cervix and stomach cancers

are the five most common types of malignancies in women, respectively (1). Although

cancer pathogenesis is challenging and multifaceted, it is now established that genetic

and environment factors interplay to promote carcinogenesis. In particular, certain

physical (e.g., ultraviolet and ionizing radiation) and biological carcinogens (viral,

bacterial or parasitic infections) interact with behavioural and dietary risk factors such

as obesity, low fruit and vegetable intake, lack of physical activity, tobacco and alcohol,

to favour the transformation of a normal cell into a malignant cell, a phenomenon that

can be particularly magnified in genetically predisposed individuals (2).

Among the various factors, diet habits play a substantial role for increasing or

reducing the risk of various cancers. Although the causal link between diet and cancer is

complex and can be hardly unravelled due to the fact that conventional diets entail many

different foods and nutrients, evidence is being gathered that certain foods may be more

harmful than others (3).

A reasonable amount of meat is part of a balanced humans diet, since it provides

valuable nutrients such as proteins and essential amino acids, vitamins, minerals and

other micronutrients (4). In the traditional culinary terminology, meat is conventionally

classified as “red” when characterized by a typical red hue, whereas “white” usually
4
defines a lighter-coloured subtype. Although a semantic debate is still opened, the

former type defines the meat of most adult mammals (i.e., cow, pork, sheep, horse),

whereas the latter is typically used to identify poultry (i.e., chicken, turkey) and rabbit.

The meat can be marketed fresh, immediately after slaughter, or processed by means of

salting, curing, addiction of spices and non-meat additives, stuffing, fermentation,

drying or smoking (5).

According to the recent statistics of the Food and Agriculture Organization of

the United Nations (FAO), the current worldwide consumption of meat is as high as

311.8 million tonnes/year, and prevalently include pork (115.5 million tonnes),

followed by poultry (108.7 million tonnes), beef (68.0 million tonnes) and ovine (14.0

million tonnes) (6). Importantly, the worldwide meat production is projected to double

by the year 2050, especially in developing countries. Due to the development of

societies, urbanization and growth in disposable income levels, the demand for

processed meat will also consistently increase (6). Therefore, the impact of fresh and

processed meat on human health is expected to grow exponentially in the next decades.

In a recent meta-analysis including 13 cohort studies and 1,674,272 individuals (7),

higher intake of processed meat was found to be a significant risk factor for all-cause

(relative risk [RR], 1.22; 95% CI, 1.16-1.29) and cardiovascular (RR, 1.18; 95% CI,

1.05-1.32) mortality. A higher intake of total red meat was significantly associated with

cardiovascular mortality (RR, 1.16; 95% CI, 1.03-1.32), whereas no significant

association was found between all-cause death and total meat intake (RR, 1.04; 95% CI,

0.84-1.30) or total white meat (RR; 0.90; 95% CI, 0.73-1.11). These results were

substantially confirmed in another meta-analysis including 9 prospective studies and

1,330,352 individuals (8), in which all-cause mortality was significantly associated with

higher intake of total red meat (RR, 1.29; 95% CI, 1.24, 1.35) and processed meat (RR,
5
1.23; 95% CI, 1.17-1.28), but not of unprocessed meat (RR, 1.10; 95% CI, 0.98-1.22).

According to this persuasive epidemiological evidence, the American Institute for

Cancer Research published a public health goal, that population average consumption of

red meat should be less than 300 g (11 oz) a week, very little (if any) to be processed

(2).

Therefore, to establish whether the consumption of total meat and meat subtypes

may be associated with human cancer, we performed a critical review of meta-analyses

that have been published so far on this topic.

2. Search methodology

We performed an electronic search on Medline and Scopus, using the keywords

“meat” AND “cancer” OR “neoplasm” OR “tumor” OR “malignancy” AND “meta-

analysis” OR “critical review” in “Title/Abstract/Keywords”, with no language

restriction. The search was limited to recent meta-analyses, i.e., those published in the

past 10 years (between 2005 and 2015). Clinical studies, letters or commentaries,

review articles with no data on cancer risk; review articles with no data on meat

consumption, and review articles lacking results of meta-analysis were also excluded.

The references of the selected articles were also scrutinized in order to identify other

pertinent items. After elimination of duplicates across the two scientific databases, a

total number of 85 publications could be finally identified. Forty three documents were

excluded (5 clinical studies, 3 letters or commentaries, 9 review articles with no data on

cancer risk; 14 review articles with no data on meat consumption, and 12 review articles

lacking results of meta-analysis). Therefore, 42 eligible meta-analyses were finally

included in this review (12 for colorectal cancer, 6 for esophageal cancer, 4 for gastric

cancer, 3 for breast and kidney cancers, 2 for lung, pancreatic, bladder and ovarian
6
cancers, 1 for non-Hodgkin lymphoma, endometrial, prostate, thyroid and liver cancer).

When available, detailed information on search methodology and the association

between meat intake and cancer risk was reported in the following parts of this article.

2. Results

The main outcome of this systematic literature search about meat intake and

cancer risk is shown in Table 1, 2 and 3.

2. 1 Colorectal cancer

Larsson and Wolk investigated the epidemiological evidence linking red or

processed meat intake with the risk of colorectal cancer by searching Medline up to

March 2006 (9). Overall, 15 prospective studies were identified and meta-analyzed. The

comparison of the highest versus the lowest intake categories revealed the existence of a

significant association between colorectal cancer and intake of total red meat (RR, 1.28;

95% CI, 1.15-1.42) or processed meat (RR, 1.20; 95% CI, 1.11-1.31). Increases of 120

g/day of red meat and 30 g/day of processed meat were associated with a 28% (95% CI,

18-39%) and 9% (95% CI, 5-13%) higher risk of colorectal cancer, respectively.

Huxley et al evaluated the strength of association between risk factors for

colorectal cancer by pertinent studies in Medline and Embase up to December 2008

(10). A total number of 26 cohort studies were identified and included in the meta-

analysis. The cumulative risk of colorectal cancer for the highest versus the lowest

consumption level was found to be significant for total red meat (RR, 1.21; 95% CI,

1.13-1.29). The association was similar for both colon cancer (RR, 1.14; 95% CI, 1.02-

1.28) and rectal cancer (RR, 1.28; 95% CI, 1.02-1.60). A significant association was

7
also found between colorectal cancer risk and processed meat intake (RR, 1.19; 95% CI,

1.12-1.27), but not with consumption of poultry (RR, 0.96; 95% CI, 0.86-1.08).

Alexander et al investigated the risk of colorectal cancer associated with meat

consumption in prospective studies by searching Medline until July 2009 (11). Overall,

28 prospective studies could be identified, 20 of which on independent populations. A

high intake of processed meat was found to be significantly associated with colorectal

cancer risk (RR, 1.16; 95% CI, 1.10-1.23). A similar independent association was found

for both colon cancer risk (RR, 1.19; 95% CI, 1.10-1.28) and rectal cancer risk (RR,

1.18; 95% CI, 1.03-1.36).

Smolińska and Paluszkiewicz explored the risk of colorectal cancer in

association with meat intake by searching Medline, Scopus, Embase, CancerLit, Google

Scholar and Cochrane Library up to December 2009 (12). Overall, 22 studies were

included in the meta-analysis. A total red meat intake more frequently than once/day

was found to be significantly associated with both colon cancer risk (RR, 1.37; 95% CI,

1.09-1.7) and rectal cancer risk (RR, 1.43; 95% CI, 1.24-1.64).

In a further meta-analysis, Alexander et al performed a literature search in

Medline until June 2009, to find prospective studies investigating the association

between meat consumption and colorectal cancer (13). Overall, 34 prospective studies

could be identified, 25 of which from independent populations. After estimating the risk

related to high versus low intake, colorectal cancer was found to be significantly

associated with total red meat intake (RR, 1.12; 95% CI, 1.04−1.12). Moreover, each

incremental serving per week of total red meat was associated with a 2% (95% CI, 0-

4%) higher risk of colorectal cancer.

Chan et al identified relevant prospective studies on the association between

colorectal cancer risk and meat intake by searching Medline until March 2011 (14).
8
Overall, 13 prospective studies could be used for a highest versus lowest intake meta-

analyses, which showed that total red and processed meat consumption was

significantly associated with this type of cancer (RR, 1.22; 95% CI, 1.11-1.34). A 100

g/day increased intake of total red and processed meat was also found to be associated

with a 14% (95% CI, 4-24%) increased risk of colorectal cancer. A further analysis of

meat subtypes also revealed that consumption both total red meat (RR; 1.10; 95% CI,

1.00-1.21) and processed meat (RR, 1.17; 95% CI, 1.09-1.25) was significantly

associated with colorectal cancer risk.

Magalhães et al performed a systematic review and meta-analysis of studies

exploring the association between colorectal cancer and dietary patterns available in

Medline, ISI Web of Science and Scopus until August 2010 (15). A final number of 8

cohort and 8 case-control studies were included in the meta-analysis. A Western diet

prevalently based on high consumption of red or processed meat was found to be

significantly associated with colorectal cancer (RR; 1.29; 95% CI, 1.13-1.48).

Hutter et al selected data from 5 nested case-control studies in prospective US

cohorts and 4 case-control studies from the US, Canada and Europe, to characterize

gene-environment interactions for colorectal cancer (16). The study population was

divided according to meat intake (above or below the median consumption), and a

significant association was observed between colorectal cancer risk and higher intake of

total red meat (odds ratio [OR], 1.25; 95% CI, 1.15-1.35) or processed meat (OR, 1.25;

95% CI, 1.16-1.35).

Johnson et al reviewed published evidence about demographic, behavioral, and

environmental factors that may be potentially associated with the risk of colorectal

cancer, by performing a systematic search in Medline between 1966 and 2010 (17). A

total of 5 cohort, 8 case-control and 1 nested case-control studies were identified and
9
meta-analyzed. A significant positive correlation was found between colorectal cancer

and total red meat consumption (5 servings/week versus no intake: RR, 1.13; 95% CI,

1.09-1.16), but not with processed meat intake (5 servings/week versus no intake: RR,

1.09; 95% CI: 0.93-1.25).

Pham et al investigated Medline up to August 2013 for identifying published

studies about meat consumption and colorectal cancer risk in Japanese populations (18).

A total number of 6 cohort and 13 case-control studies were identified and included in

the meta-analysis. A significant association was found with colorectal cancer by

comparing the highest versus the lowest categories of total red meat consumption (RR,

1.16; 95% CI, 1.00-1.34) and processed red meat consumption (RR, 1.17; 95% CI, 1.02-

1.35). Interestingly, a significant and inverse association was instead observed between

colorectal cancer risk and poultry intake (RR, 0.80; 95% CI, 0.67-0.96).

Woo et al performed a literature search in KMBase, KoreaMed and Medline

until June 2014, to identify case-control or cohort studies reporting on cancer risk and

diet in Korean populations (19). Three Korea-based studies were finally included in the

meta-analysis. When the highest category of food intake was compared with the lowest,

a significant association was found between total meat consumption and colorectal

cancer (RR, 1.25; 95% CI, 1.15-1.36).

Carr et al performed a subsequent systematic review and meta-analysis of

prospective studies reporting the association between intake of meat subtypes and

colorectal cancer (20). More specifically, an electronic search was carried out in

Medline and ISI Web of Science until August 2014. Overall, 19 studies were identified,

which analyzed 5 different meat subtypes (beef, pork, lamb, veal, poultry). By

comparison of the highest versus the lowest intake, consumption of beef (RR, 1.1; 95%

CI, 1.07-1.44) and lamb (RR, 1.24; 95% CI, 1.08-1.44) was found to be significantly
10
associated with colorectal cancer risk, whereas no significant association was found

with consumption of pork (RR, 1.07; 95% CI, 0.90-1.27) or poultry (RR, 0.96; 95% CI,

0.88-1.04).

2.2 Breast cancer

Taylor et al performed a literature search in Medline on the association between

breast cancer risk and meat consumption in premenopausal women up to May 2009

(21). A total of 10 studies (6 case-control, one nested case-control and 3 cohort) were

identified and finally included in the meta-analysis. A significant association was found

between breast cancer risk and total red meat intake (RR, 1.24; 95% CI, 1.08-1.42).

Alexander et al carried out a literature search in Medline up to July 2009 to

identify published prospective studies investigating the association between breast

cancer risk and red or processed meat intake (22). A final number of 11 prospective

studies were included in the meta-analysis. The comparison of the highest versus the

lowest category of intake revealed that total red meat was non-significantly associated

with breast cancer risk (RR, 1.07; 95 % CI, 0.98-1.17), whereas a significant association

was found with processed meat (RR, 1.08; 95% CI, 1.01-1.16).

Namiranian et al searched Medline, Scopus, ISI Web of Science up to August

2012 for studies reporting information on breast cancer and meat intake (23). Overall, 3

studies were included in the meta-analysis. Total meat consumption for more than three

times per week was found to be significantly associated with the risk of developing

breast cancer (OR, 1.39; 95% CI, 1.03-1.87).

11
2.3 Lung cancer

Yang et al performed a systematic search in Medline, Embase and ISI Web of

Science up to November 2011, to investigate the relationship between meat

consumption and lung cancer risk (24). A final number of 23 case-control and 11 cohort

studies were included in the meta-analysis. By comparison of the highest with the

lowest intake categories, a significant association was found between lung cancer and

total meat (RR,1.35; 95% CI, 1.08-1.69), total red meat (RR, 1.34; 95% CI 1.18-1.52),

but not with processed meat (RR, 1.06; 95% CI, 0.90-1.25) or total white meat (RR,

1.06; 95% CI; 0.82-1.37). These associations remained significant in all subgroup

analyses, irrespective of quality and design of the study, smoking status, gender and

histologic subtype. Interestingly, an inverse association was also found between lung

cancer risk and higher intake of poultry (RR, 0.91; 95% CI 0.85-0.97).

Xue et al carried out a literature search in PubMed, Embase, ISI Web of Science,

National Knowledge Infrastructure and Wanfang Database until June 2013 for

identifying published articles about the association between red or processed meat

consumption and lung cancer (25). Six cohort studies and 28 case-control investigations

were included in the meat-analysis. Overall, total red meat consumption was found to be

associated with lung cancer (RR, 1.55; 95% CI, 1.35-1.77). A further analysis according

to red meat subtypes also revealed that consumption of beef (RR, 1.39; 95% CI, 1.14-

1.69) but not pork (RR, 1.10; 95% CI, 0.70-1.73) or lamb (RR, 1.25; 95% CI, 0.97-

1.61) were significantly associated with lung cancer risk. Even more interestingly,

increments of 120 grams red meat per day were found to increase the risk of lung cancer

by 35%.

12
2.4 Esophageal cancer

The risk of esophageal cancer associated with meat consumption was

investigated by Huang et al, who performed a search in Medline and Embase up to May

2012 (26). Overall, 3 cohort and 7 case-control studies were identified and meta-

analyzed. The risk of esophageal adenocarcinoma (highest versus lowest intake

categories) was found to be significant for higher intake of both total red meat (RR,

1.31; 95% CI, 1.05-1.64) and processed meat (RR; 1.41; 95% CI, 1.09-1.83).

Choi et al carried out a search in Medline and Embase until May 2012 (27).

Overall, 4 cohort and 23 case-control studies were meta-analyzed. After comparison of

the highest and the lowest categories of intake, the consumption of total red meat was

found to be significantly associated with both esophageal adenocarcinoma (RR, 1.42;

95% CI, 1.02-1.98) and esophageal squamous cell carcinoma (RR, 1.55; 95% CI, 1.10-

2.17). The consumption of processed meat was also found to be significantly associated

with esophageal adenocarcinoma (RR; 1.38; 95% CI, 1.07-1.78), but not with

esophageal squamous cell carcinoma (RR, 1.08; 95% CI, 0.80-1.44).

In a subsequent article, Jiang et al investigated the association between white

meat and esophageal cancer risk by performing a search in Medline until December

2012 (28). A total of 17 case-control (9 including poultry) and 3 cohort studies (3

including poultry) were meta-analyzed. When low versus high intake was compared,

larger consumption of poultry was not associated with risk of esophageal cancer (RR,

0.83; 95% CI, 0.62-1.12).

Salehi et al also carried out a meta-analysis in Medline, Embase and ISI Web of

Knowledge for identifying studies published between 1990 and 2011 (29). The

electronic search produced 4 cohorts and 31 case-control studies. After comparison of

the highest versus the lowest level of intake, the risk of esophageal cancer was found to
13
be associated with consumption of total red meat (RR, 1.40; 95% CI, 1.09-1.81) and

processed meat (RR; 1.41; 95% CI, 1.13-1.76), but not with higher intake of total meat

(RR, 0.99; 95% CI, 0.85-1.15) and poultry (RR; 0.87; 95% CI, 0.60-1.24).

Qu et al performed a search in Medline and Embase until 31 October 2012 to

identify observational studies linking esophageal cancer and meat intake (30). A total of

19 case-control and 2 cohort studies were included in the meta-analysis. When subjects

reporting higher intake were compared to those reporting lower consumption,

esophageal cancer risk was found to be significantly associated with higher intake of

total red meat (RR, 1.57; 95% CI, 1.26-1.95) and processed meat (RR, 1.55; 95% CI,

1.22-1.97).

More recently, Zhu et al investigated the relationship between meat consumption

and esophageal cancer risk by identifying cohort and case-control studies in Medline,

Embase and Cochrane Library until April 2013 (31). A total number of 7 cohort and 28

case-control studies were meta-analyzed. A significant risk (highest versus the lowest

consumption categories) was found for total red meat (RR, 1.55; 95% CI, 1.22-1.96)

and processed meat (RR, 1.33; 95% CI, 1.04-1.69), but not for total meat (RR, 1.19;

95% CI, 0.98-1.46). Interestingly, an inverse association was observed between

esophageal cancer risk and larger intake of white meat (RR, 0.72; 95% CI, 0.60-0.86) or

poultry (RR, 0.83; 95% CI, 0.72-0.96).

2.5 Gastric cancer

Larsson et al performed a search in Medline up to March 2006 to identify

clinical studies linking processed meat consumption with stomach cancer risk (32). A

total number of 6 prospective cohort and 9 case-control studies were identified and

included in the meta-analysis. When subjects in the highest category of intake were
14
compared to those in the lowest, larger consumption of processed meat was found to be

associated with the risk of colorectal cancer in both prospective cohort (RR, 1.15; 95%

CI, 1.04-1.27) and case-control studies (RR, 1.38; 95% CI, 1.19-1.60). Interestingly,

increased intake of sausages (RR, 1.37; 95% CI, 1.06-1.78) and bacon (RR, 1.49; 95%

CI, 1.09-2.03) was also associated with gastric cancer risk.

Bonequi et al investigated the relationship between gastric cancer and dietary

habits in Latin America, by performing a search in Medline and regional databases for

studies published up to December 2011 (33). A total number of 6 studies were identified

and included in the meta-analysis. After comparison of the highest versus the lowest

intake categories, gastric cancer risk was found to be significantly associated with larger

consumption of total red meat (OR, 1.73; 95% CI, 1.20-2.51), and with higher intake of

processed and salted meat (OR, 1.64; 95% CI, 1.08-2.48).

Zhu et al performed an electronic search in Medline, Embase and Cochrane

Library until April 2013 to identify cohort and case-control studies assessing the

association between gastric cancer risk and red and/or processed meat (34). Overall, 12

cohort and 30 case-control studies were meta-analyzed. The comparison of the highest

versus the lowest category of intake revealed significant associations between gastric

cancer risk and larger consumption of total red meat (RR, 1.45; 95% CI: 1.22-1.73) or

processed meat (RR, 1.45; 95% CI: 1.26-1.65). The analysis of meat subtypes also

revealed significant associations between gastric cancer and higher consumption of beef

(RR, 1.28; 95% CI: 1.04-1.57), bacon (RR, 1.37; 95% CI, 1.17-1.61), sausage (RR,

1.33; 95% CI, 1.16-1.52) and ham (RR, 1.44; 95% CI, 1.00-2.06), but not pork (RR,

1.31; 95% CI, 0.97-1.78).

In a subsequent publication, Song et al searched PubMed and Embase until

December 2013, to identify cohort and case-control studies providing a quantitative

15
assessment of the association between red meat consumption and gastric cancer risk

(35). Overall, 18 studies were included in the meta-analysis. When the highest category

of intake was compared with the lowest, a significant association was found between

gastric cancer and larger consumption of total red meat (RR, 1.37; 95% CI, 1.18-1.59).

Accordingly, a 17% increased risk of gastric cancer was estimated for every 100 g/day

increment of total red meat (RR, 1.17; 95% CI, 1.05-1.32).

2.6 Hepatocellular carcinoma

Luo et al searched Medline, ISI Web of Science and EMBASE up to July 2013,

to identify studies exploring the association between meat consumption and risk of

hepatocellular carcinoma (36). A total number of 7 cohort studies and 10 case-control

studies were included in the meta-analysis. The comparison of the highest and the

lowest category of intake did not reveal any significant association between

hepatocellular carcinoma and larger consumption of total meat (RR, 0.97; 95% CI,

0.85-1.11), total red meat (RR, 1.10; 95% CI, 0.85-1.42) or processed red meat (RR,

1.01; 95% CI, 0.79-1.28).

2.7 Pancreatic cancer

Paluszkiewicz et al carried out a literature search in Medline, Cochrane Library,

Embase, CancerLit, Scopus and Google Scholar until December 2010 to identify

potential associations between pancreatic cancer and diet (37). A meta-analysis of 11

case-control studies (5 including data on red meat) and 13 cohorts studies (6 including

data on red meat) was performed. The analysis of high versus low intake revealed the

existence of a significant association between pancreatic cancer risk and larger

16
consumption of total red meat (RR, 1.27; 95% CI, 1.07-1.5), but not with higher poultry

intake (RR, 0.97; 95% CI, 0.84-1.12).

Larsson and Wolk explored the association between meat consumption and

pancreatic cancer by performing a search in Medline and Embase through November

2011 (38). A total number of 11 prospective studies were identified and meta-analyzed.

No significant association was found between pancreatic cancer risk and 120 g per day

increased consumption of total red meat (RR, 1.13; 95% CI, 0.93-1.39), whereas a

greater intake of 50 g per day of processed meat was found to be significantly

associated with pancreatic cancer risk (RR 1.19; 95% CI, 1.04-1.36).

2.8 Renal cancer

Faramawi et al performed a literature search in Medline and Ovid until

December 2006 for studies exploring the association between renal cancer and meat

intake (39). A total number of 13 case-control studies were identified and meta-

analyzed. The comparison of high versus low intake categories revealed a significant

association between renal cancer risk and total meat intake (OR, 1.27; 95% CI, 1.12-

1.43), total red meat intake (OR, 1.30; 95% CI, 1.03-1.63), processed meat (OR, 1.21;

95%, 1.01-1.48) and poultry (OR, 1.21; 95% CI, 1.01-1.48).

Lee et al examined the relationship between renal cancer and meat intake in 13

cohort studies included in the Pooling Project of Prospective Studies of Diet and Cancer

(40). No association was found between renal cancer risk and increase of 2

servings/week of total red meat (RR, 1.00; 95% CI, 0.95-1.06), processed meat (RR,

1.01; 95% CI, 0.99-1.02) or poultry (RR, 1.01; 95% CI, 0.93-1.10).

Alexander and Cushing performed a literature search in Medline until December

2007, to identify relevant publication about the association between renal cancer risk
17
and meat intake (41). Overall, 12 case-control studies, 3 cohort studies and pooled data

from 13 international cohorts were meta-analyzed. After comparison of high versus low

intake categories, no significant association was found between renal cancer risk and

consumption of either total red meat (RR, 1.12; 95% CI, 0.98-1.29) or processed meat

(RR, 1.07; 95% CI, 0.94-1.2).

2.9 Oral cavity and oropharynx cancer

Xu et al conducted an electronic search in Medline, Embase, and Cochrane

Library Central database up to May 2013 to identify relevant studies linking meat

consumption and oral cavity or oropharynx cancers (42). A final number of 12 case-

control and one cohort studies were included in the meta-analysis. Although no

significant association was found between oral cavity or oropharynx cancerz and higher

consumption of total meat (RR, 1.14; 95% CI, 0.78-1.68), total red meat (RR, 1.05;

95% CI, 0.66-1.66) and white meat (RR, 0.81; 95% CI, 0.54-1.22), a larger intake of

processed red meat was found to be associated with increased risk of these types of

cancer (RR, 1.91; 95% CI, 1.19–3.06).

2.10 Bladder cancer

Wang et al carried out a literature search in Medline until October 2010 (43). A

total number of 10 cohort and 11 case-control studies were included in the meta-

analyses. When the highest category of meat intake was compared with the lowest,

increased total meat consumption was not found to be significantly associated with

bladder cancer risk (RR, 1.04; 95% CI, 0.80-1.27). Nevertheless, a significant

association was found with larger intake of total red meat (RR, 1.17; 95% CI, 1.02-1.34)

and processed meat (RR, 1.10; 95% CI, 1.00-1.21), but not with higher consumption of
18
beef (RR, 1.19; 95% CI 0.92-1.46), pork (RR, 0.82; 95% CI, 0.43-1.20) or poultry (RR,

0.77; 95% CI, 0.48-1.06). The findings did not change throughout different subgroup

analyses.

Li et al searched Medline up to May 2014 to explore the association between

bladder cancer and red or processed meat intake (44). As many as 14 studies on red

meat and 11 studies on processed meat were identified and included in the meta-

analysis. The resulting risk estimates of high versus low intake showed that although

larger total red meat intake was not associated with bladder cancer (RR, 1.15; 95% CI,

0.97-1.36), higher intake of red meat was a significant risk factor for this type of cancer

(RR, 1.22; 95% CI, 1.04-1.43). The significance of this association remained unchanged

in subgroup analyses, (i.e., after adjustment for sex and geographical region).

2.11 Ovarian Cancer

Kolahdooz et al performed a meta-analysis of two independent Australian case-

control studies, which estimated the association between meat intake and ovarian cancer

risk (45). Although larger intake (highest versus lowest level of consumption) of total

meat (OR, 1.06; 95% CI, 0.87-1.30), total red meat (OR, 1.07; 95% CI, 0.80-1.42) or

poultry (RR, 0.83; 95% CI, 0.67-1.03) was not associated with ovarian cancer risk, a

significant association was found between this type of cancer and higher consumption

of processed meat (RR, 1.18; 95% CI, 1.15-1.21).

Wallin et al investigated the association between risk of ovarian cancer and red

or processed meat by performing a literature search in Medline and Embase until

January 2011 (46). Overall, 8 cohort studies were meta-analyzed. No significant

association was found between ovarian cancer and 100 g per week intake increment of

19
either total red meat (RR, 1.02; 95% CI, 0.99-1.04) or processed meat (RR, 1.05; 95%

CI, 0.98-1.14).

2.12 Endometrial cancer

Bandera et al performed a literature search in Medline, ISI Web, Embase, Biosis,

Ingenta, CINAHL, Science Direct, LILACS, Pascal, ExtraMed, and Allied CompMed

until December 2006 to identify pertinent studies linking endometrial cancer risk and

dietary intake of animal products (47). Ten studies (1 cohort and 9 case-control)

reporting data on meat intake were included in the meta-analysis. When the highest

category of intake was compared with the lowest, a significant association was found

between endometrial cancer risk and large consumption of total meat (OR, 1.44; 95%

CI, 1.06-1.97), total red meat (RR, 1.59; 95% CI, 1.24-2.05), but not with higher intake

of poultry (RR, 1.03; 95% CI, 0.66-1.62).

2.13 Prostate cancer

Alexander et al carried out a literature search in Medline until January 2009 to

identify relevant publications about prostate cancer risk and meat (48). Overall, 15

studies of red meat and 11 studies of processed meat were selected for the meta-

analysis. When high versus low intake categories were compared, no significant

association was found between prostate cancer risk and higher consumption of either

total red meat (RR, 1.00; 95% CI, 0.96-1.05) or processed meat (RR, 1.05; 95% CI,

0.99-1.12).

20
2.14 Thyroid Cancer

Liu and Lin carried out a literature search in Medline up to March 2014 for

articles containing information about the relationship between dietary factors and

thyroid cancer (49). A total number of 19 cohort and case-control studies were

identified and included in the meta-analysis. When the highest and lowest levels of total

meat consumption were compared, the authors failed to find a significant association

with thyroid cancer (OR, 0.96; 95% CI, 0.70-1.34).

2.15 Non-Hodgkin lymphoma

Fallahzadeh et al carried out a literature search in Cochrane Library, Medline,

and Science Citation Index Expanded databases up to September 2014 (50). Eleven

studies were identified and meta-analyzed. A significant association was found between

increased total red meat intake and risk of non-hodgkin lymphoma (OR, 1.10; 95% CI,

1.02-1.19). When the analysis was limited to processed red meat, the association with

remained statistically significant (OR, 1.17; 95% CI, 1.06-1.29).

3. Discussion

Accurate information on the potential association between meat consumption

and health risk is essential for driving consumer choices, for establishing and

implementing dietary recommendations, for changing diet and lifestyle behaviors, as

well as for reformulating foods to minimize health hazards. A larger intake of meat, and

particularly of red and processed meat, has been convincingly associated with a variety

of human disorders, including cardiovascular disease (7), diabetes (51), gout (52) and

arthritis (53). Several lines of evidence also support a carcinogenic potential of certain

21
types of meat (54), but no published article has provided a systematical and

comprehensive overview across different types of cancer to the best of our knowledge.

Our analysis of published meta-analyses reveals that some relationships

seemingly exist between meat intake and cancer (Table 1). A higher total meat intake

was found to be associated with colorectal cancer risk in approximately half of the

studies in which it was investigated (6/13; 46%), whereas no significant association was

found in the remaining. The association was significant in single meta-analyses on

colorectal, breast, lung, endometrial and thyroid cancers. A more convincing association

was observed between cancer and red or processed meat (Table 2). Specifically, larger

total red meat consumption was found to be significantly associated with cancer risk in

73% (24/32) of the meta-analyses in which it was investigated, and especially with

colorectal (9/9; 100%), lung (2/2; 100%), esophageal (5/5; 100%) and gastric (3/3;

100%) cancers, as well as in single meta-analyses on endometrial cancer and non-

Hodgkin lymphoma. No association was instead found with the risk of hepatocellular

carcinoma, pancreatic, ovarian and prostate cancers. The evidence for processed meat

overlaps with that of total red meat consumption, in that a significant association with

cancer risk could be found in 71% (22/31) of the meta-analyses, and especially with

colorectal (7/8; 88%), esophageal (5/6; 83%), gastric (3/3; 100%) and bladder (2/2;

100%) cancers. No association was instead observed in single meta-analyses evaluating

the risk of lung, pancreatic, liver and prostate cancers. Interestingly, larger consumption

of total white meat and poultry was found to be negatively associated with three types

of cancers (colorectal, lung and esophageal), and non-significantly associated (or not

assessed) in the remaining, with the only exception of one meta-analysis reporting a

significant association between renal cancer and high poultry intake. The analysis of the

more common meat subtypes suggested that higher beef consumption was significantly
22
associated with cancer risk (3/4; 75%), whereas the risk of malignancy was not

significantly increased in subjected consuming larger amounts of pork (4/4; 100%)

(Table 3). No conclusive evidence is available for lamb, since the consumption of this

meat was only assessed in 2 meta-analyses (positively associated with colorectal cancer

but not with lung malignancies). Importantly, and at variance with the widespread

perception that the consumption of fresh red is less harmful than that of processed meat

in terms of cancer risk (55), our data seems to support the notion that the overall risk of

these two types of meat is at least comparable across a large number of malignancies,

whereas the larger consumption of other types of meat (especially white and

unprocessed) appears to be at least not harmful. This hypothesis is strengthened by

recent data on all-cause mortality, which convincingly attests that higher intake of either

red (RR, 1.29; 95% CI, 1.24, 1.35) or processed meat (RR, 1.23; 95% CI, 1.17-1.28)

may be associated with increased risk of death, whereas that of unprocessed meat is not

(RR, 1.10; 95% CI, 0.98-1.22) (8).

Some reliable biological explanations have been provided to support these

findings. Indeed, larger consumption of meat is associated with direct intake or

endogenous generation of a vast array of carcinogens such as heterocyclic amines,

polycyclic aromatic hydrocarbons, N-nitroso compounds, omega-3 polyunsaturated

fatty acids and heme, as well as with effects on local immunity and inflammation (56,

57). Among the different subtypes of meat, red and processed meats contain a larger

amount of heterocyclic amines and their consumption is associated with a greater

generation of N-nitroso compounds from heme than white meat (54). Accordingly, a

number of studies showed that a positive relationship exists between release of N-

nitroso compounds and red meat consumption, whereas no convincing association could

be found with white meat (58,59). Similar evidence has recently been provided for
23
polycyclic aromatic hydrocarbons, wherein the generation of these compounds was

found to be largely increased after consumption of red but not white meat (60). Not

surprisingly, processed meat contains on average 50% more nitrates than unprocessed

meat (61), and this evidence also support findings of increased cancer risk and all-cause

mortality.

Another important aspect that deserves particular attention is the dramatic

heterogeneity of the search methodology, which may at least in part explain the

different outcomes observed across the various meta-analyses. This particularly refers to

the literature search using different scientific databases (i.e., Medline, Scopus or

Embase, ISI Web of Science, Google Scholar and Cochrane Library among others) and to

the assorted number of keywords or Medical Subject Headings (MeSH) used for

identifying meat (Table 4). Conventionally, the term “red meat” is used to design beef,

pork, lamb and goat from domesticated animals, whereas “processed meat” defines

types of meat preserved by smoking, curing or salting, or addition of chemical

preservatives (2). Rather intuitively, these definitions are not inclusive of all dietary

sources of animal meat, nor they have been widely acknowledged across the different

studies. The case of horsemeat is paradigmatic. Although its consumption is virtually

banned in some Countries (e.g., US and UK) (62), this type of meat represents a

significant part of diet of some European, South American and Asian populations, with

a worldwide consumption approximating 0.7 million tonnes/year (6). Although the

discussion on ethical opportunity of eating horses is obviously out of scope, the impact

that horsemeat may have on estimating the risk of cancer is not meaningless. Compared

with other subtypes of meat such as pork, beef or poultry, the horsemeat contains higher

amount of heme and omega-3 polyunsaturated fatty acids (63,64), which may increase

the generation of N-nitroso compounds or fat peroxidation, thus ultimately enhancing

24
cancer risk in populations consuming horsemeat. The inclusion of pork as “red meat” in

some meta-analyses and its exclusion in others is also a matter of debate (Table 4).

Indeed, pork is conventionally considered white meat when the animal is young, but is

then regarded as red meat when the animal grows. This evidence calls for a standardized

categorization of this type of meat to prevent misleading interpretation of data.

Another important aspect is the uncertain definition of “processed meat” across

epidemiological studies. Although this term is conventionally used as a synonymous of

processed red meat, deli meats (which also entail processed poultry) have been included

in processed meat in some studies (65). Therefore, development and application of

universally agreed definitions of meat subtypes and products are unavoidable steps in

future clinical studies aimed to investigate the association between meat consumption

and cancer.

In conclusion, this review of the current literature on the association between

cancer risk and meat intake supports the suggestion that consumption of red or

processed meat should be limited (i.e., <300 g a week) (2). Interestingly, similar

conclusions were recently reached by the International Agency for Research on Cancer

(IARC). Specifically, the IARC Working Group analyzed over 800 different studies on

cancer in humans (66), and concluded that processed meat should be classified as

carcinogenic to humans, especially for the development of colorectal cancer (e.g., every

50 gram portion of processed meat eaten daily increases the risk of colorectal cancer by

approximately 18%). It was also highlighted that limited but convincing evidence does

exist for an association between red meat intake and colorectal cancer (e.g., the risk of

colorectal cancer may increase by 17% for every 100 gram portion of red meat eaten

daily). Therefore, the IARC analysis reinforces the former recommendation from the

25
WHO that people who eat meat should moderate the consumption of meat (especially

processed and red meat) to reduce the risk of cancer.

FUNDING SUPPORT

None

CONFLICT OF INTEREST

None.

26
Biography

Giuseppe Lippi, born in Padova (Italy) on October 4th, 1967, currently serves as Full Professor of
Clinical Biochemistry at the University of Verona and Director of the clinical chemistry and haematology
laboratory of the University Hospital of Verona. He has published more than 1150 articles in peer‐reviewed
journals, his total Impact Factor is 4104 and the Hirsch Index (H‐index) is 60. He has recently been awarded
with the 2014 Management Sciences and Patient Safety Division Award of the American Association for
Clinical Chemistry (AACC) for outstanding contributions in the field of patient safety in the clinical
laboratory/healthcare industry.
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34
Tables
Table 1. Description of meta-analyses investigating the association between meat consumption and cancer risk.
Author Type of cancer Risk estimation Outcome Reference
Larsson et al, Colorectal RR (highest versus lowest intake  Total red meat: 1.28 (95% CI, 1.15-1.42) [9]
2006 categories)  Processed meat: 1.20 (95% CI, 1.11-1.31)
Huxley et al, Colorectal RR (highest versus lowest intake  Total red meat: 1.21 (95% CI, 1.13-1.29) [10]
2009 categories)  Processed meat: 1.19 (95% CI, 1.12-1.27)
 Poultry: 0.96 (95% CI, 0.86-1.08)
Alexander et al, Colorectal RR (high versus low intake)  Processed meat: 1.16 (95% CI, 1.10-1.23) [11]
2010
Smolińska et al, Colorectal RR (intake more frequently than  Total red meat: 1.37 (95% CI, 1.09-1.7) for colon cancer [12]
2010 once per day) and 1.43 (95% CI, 1.24-1.64) for rectal cancer
Alexander et al, Colorectal RR (highest versus lowest intake  Total red meat: 1.12 (95% CI, 1.04-1.12) [13]
2011 categories)
Chan et al, 2012 Colorectal RR (highest versus lowest intake  Total red and processed meat: 1.22 (95% CI, 1.11-1.34) [14]
categories)  Total red meat: 1.10 (95% CI, 1.00-1.21)
 Processed red meat: 1.17 (95% CI, 1.09-1.25)
Magalhães et al, Colorectal RR (high versus low intake)  Red or processed meat: 1.29 (95% CI, 1.13-1.48) [15]
2012
Hutter et al, 2012 Colorectal OR (above median versus below  Total red meat: 1.25 (95% CI, 1.15-1.35) [16]
median intake)  Processed meat: 1.25 (95% CI, 1.16-1.35)
Johnson et al, Colorectal RR (5 servings per week versus  Total red meat: 1.13 (95% CI, 1.09-1.16) [17]
2013 no intake)  Processed meat: 1.09 (95% CI: 0.93-1.25)
Pham et al, 2014 Colorectal RR (highest versus lowest intake  Total red meat: 1.16; 95% CI, 1.00-1.34 [18]
categories)  Processed red meat: 1.17; 95% CI, 1.02-1.35
 Poultry: 0.80; 95% CI, 0.67-0.96
Woo et al, 2014 Colorectal RR (highest versus lowest intake  Total meat: 1.25 (95% CI, 1.15-1.36) [19]
categories)
Carr et al, 2015 Colorectal RR (highest versus lowest intake  Lamb: 1.24 (95% CI, 1.08-1.44) [20]
categories)  Beef: 1.1 (95% CI, 1.07-1.44)
 Pork: 1.07 (95% CI, 0.90-1.27)
 Poultry: 0.96 (95% CI, 0.88-1.04)
Taylor et al, 2009 Breast RR (high versus low intake)  Total red meat: 1.24 (95% CI, 1.08-1.42) [21]

35
Alexander et al, Breast RR (highest versus lowest intake  Total red meat: 1.07 (95 % CI, 0.98-1.17) [22]
2010 categories)  Processed meat: 1.08 (95% CI, 1.01-1.16)
Namiranian et al, Breast OR (consumption for more than  Total meat: 1.39 (95% CI, 1.03-1.87) [23]
2014 three times per week versus no
intake)
Yang et al, 2013 Lung RR (highest versus lowest intake  Total meat: 1.35 (95% CI, 1.08-1.69) [24]
categories)  Total red meat: 1.34 (95% CI 1.18-1.52)
 Processed meat: 1.06 (95% CI, 0.90-1.25)
 Total white meat: 1.06 (95% CI; 0.82-1.37)
 Poultry: 0.91 (95% CI 0.85-0.97)
Xue et al, 2014 Lung RR (highest versus lowest intake  Total red meat: 1.55 (95% CI, 1.35-1.77). [25]
categories)  Beef: 1.39 (95% CI, 1.14-1.69)
 Pork: 1.10 (95% CI, 0.70-1.73)
 Lamb: 1.25 (95% CI, 0.97-1.61)
Huang et al, 2013 Esophageal RR (highest versus lowest intake  Total red meat: 1.31 (95% CI, 1.05-1.64) [26]
categories)  Processed meat: 1.41 (95% CI, 1.09-1.83)
Choi et al, 2013 Esophageal RR (highest versus lowest intake  Total red meat: 1.42 (95% CI, 1.02-1.98) for esophageal [27]
categories) adenocarcinoma and 1.55 (95% CI, 1.10-2.17) for
esophageal squamous cell carcinoma
 Processed meat: 1.38 (95% CI, 1.07-1.78) for esophageal
adenocarcinoma and 1.08 (95% CI, 0.80-1.44) for
esophageal squamous cell carcinoma
Jiang et al, 2013 Esophageal RR (high versus low intake)  Poultry: 0.83 (95% CI, 0.62-1.12) [28]
Salehi et al, 2013 Esophageal RR (highest versus lowest intake  Total meat: 0.99 (95% CI, 0.85-1.15) [29]
categories)  Total red meat: 1.40 (95% CI, 1.09-1.81)
 Processed meat: 1.41 (95% CI, 1.13-1.76)
 Poultry: 0.87 (95% CI, 0.60-1.24)
Qu et al, 2013 Esophageal RR (high versus low intake)  Total red meat: 1.57 (95% CI, 1.26-1.95) [30]
 Processed meat: 1.55 (95% CI, 1.22-1.97)

Zhu et al, 2014 Esophageal RR (highest versus lowest intake  Total meat: 1.19 (95% CI, 0.98-1.46) [31]
categories)  Total red meat: 1.55 (95% CI, 1.22-1.96)
 Processed meat: 1.33 (95% CI, 1.04-1.69)

36
  White meat: 0.72 (95% CI, 0.60-0.86)
 Poultry: 0.83 (95% CI, 0.72-0.96)
Larsson et al, Gastric RR (highest versus lowest intake  Processed meat: 1.38 (95% CI, 1.19-1.60) [32]
2006 categories)
Bonequi et al, Gastric OR (highest versus lowest intake  Total red meat: 1.73 (95% CI, 1.20-2.51) [33]
2013 categories)  Processed or salted meat: 1.64 (95% CI, 1.08-2.48)
Zhu et al, 2013 Gastric RR (highest versus lowest intake  Total red meat: 1.45 (95% CI: 1.22-1.73) [34]
categories)  Processed meat: 1.45 (95% CI: 1.26-1.65)
 Beef: 1.28 (95% CI: 1.04-1.57)
 Bacon: 1.37 (95% CI, 1.17-1.61)
 Sausage: 1.33 (95% CI, 1.16-1.52)
 Ham: 1.44 (95% CI, 1.00-2.06)
 Pork: 1.31 (95% CI, 0.97-1.78).
Song et al, 2014 Gastic RR (highest versus lowest intake  Total red meat: 1.37 (95% CI, 1.18-1.59) [35]
categories)
Luo et al, 2014 Hepatocellular RR (highest versus lowest intake  Total meat: 0.97 (95% CI, 0.85-1.11) [36]
categories)  Total red meat: 1.10 (95% CI, 0.85-1.42)
 Processed red meat: 1.01 (95% CI, 0.79-1.28)
Paluszkiewicz et Pancreatic RR (high versus low intake)  Total red meat: 1.27 (95% CI, 1.07-1.5) [37]
al, 2012  Poultry: 0.97 (95% CI, 0.84-1.12)
Larsson et al, Pancreatic RR (50 to 120 g/day increased  Total red meat: 1.13 (95% CI, 0.93-1.39; 120 g/day) [38]
2012 intake)  Processed meat: 1.19 (95% CI, 1.04-1.36; 50 g/day)
Faramawi et al, Renal OR (highest versus lowest intake  Total meat: 1.27 (95% CI, 1.12-1.43) [39]
2007 categories)  Total red meat: 1.30 (95% CI, 1.03-1.63)
 Processed meat: 1.21 (95%, 1.01-1.48)
 Poultry: 1.21 (95% CI, 1.01-1.48)
Lee et al, 2009 Renal RR (increase of 2 servings/week)  Total red meat: 1.00 (95% CI, 0.95-1.06) [40]
 Processed red meat: 1.01 (95% CI, 0.99-1.02)
 Poultry: 1.01 (95% CI, 0.93-1.10)
Alexander et al, Renal RR (high versus low intake)  Total red meat. 1.12 (95% CI, 0.98-1.29) [41]
2009  Processed meat: 1.07 (95% CI, 0.94-1.2)
Xu et al, 2014 Oral cavity and RR (high versus low intake)  Total meat: 1.14 (95% CI, 0.78-1.68) [42]
oropharynx  Total red meat: 1.05 (95% CI, 0.66-1.66)
37
  Processed red meat: 1.91 (95% CI, 1.19–3.06)
 White meat: 0.81 (95% CI, 0.54-1.22)
Wang et al, 2012 Bladder RR (highest versus lowest intake  Total meat: 1.04 (95% CI, 0.80-1.27) [43]
categories)  Total red meat: 1.17 (95% CI, 1.02-1.34)
 Processed meat: 1.10 (95% CI, 1.00-1.21)
 Beef: 1.19 (95% CI 0.92-1.46)
 Pork: 0.82 (95% CI, 0.43-1.20)
 Poultry: 0.77 (95% CI, 0.48-1.06)
Li et al, 2014 Bladder RR (high versus  Total red meat: 1.15 (95% CI, 0.97-1.36) [44]
low intake)  Processed red meat: 1.22 (95% CI, 1.04-1.43)
Kolahdooz et al, Ovarian OR (highest versus lowest intake  Total meat: 1.06 (95% CI, 0.87-1.30) [45]
2010 categories)  Total red meat: 1.07 (95% CI, 0.80-1.42)
 Processed meat: 1.18; 95% CI, 1.15, 1.21)
 Poultry: 0.83 (95% CI, 0.67-1.03)
Wallin et al, 2011 Ovarian RR (100 g per week intake  Total red meat: 1.02 (95% CI, 0.99-1.04) [46]
increment)  Processed meat: 1.05 (95% CI, 0.98-1.14)
Bandera et al, Endometrial RR (highest versus lowest intake  Total meat intake: 1.44 (95% CI, 1.06-1.97) [47]
2007 categories)  Total red meat: 1.59 (95% CI, 1.24-2.05)
 Poultry: 1.03 (95% CI, 0.66-1.62)
Alexander et al, Prostate RR (high versus  Total red meat: 1.00 (95% CI, 0.96-1.05) [48]
2010 low intake)  Processed meat: 1.05 (95% CI, 0.99-1.12)
Liu et al, 2014 Thyroid RR (highest versus lowest intake  Total meat: 0.96 (95% CI, 0.70-1.34) [49]
categories)
Fallahzadeh et al, Non-Hodgkins OR (intake versus no intake)  Total red meat: 1.10 (95% CI, 1.02-1.19) [50]
2014 lymphoma  Processed red meat: 1.17 (95% CI, 1.06-1.29)

38
Table 2. Association between cancer risk and consumption of total, red, white or processed meat.
Type of cancer n. of meta-analyses Total meat Total red meat Total white meat Processed meat
 NS  NA  NS  NA  NS  NA  NS  NA
Colorectal 12 1 11 9 3 12 7 1 4
Breast 3 1 2 1 1 1 3 1 2
Lung 2 1 1 2 1 1 1 1
Esophageal 6 2 4 5 1 1 5 5 1
Gastric 4 4 3 1 4 3 1
Hepatocellular carcinoma 1 1 1 1 1
Pancreatic 2 2 2 2 1 1
Renal 3 1 1 1 1 1 1 3 1 2
Oral cavity and oropharynx 1 1 1 1 1
Bladder 2 1 1 1 1 2 2
Ovarian 2 1 1 2 2 1 1
Endometrial 1 1 1 1 1
Prostate 1 1 1 1 1
Thyroid 1 1 1 1 1
Non-Hodgkin lymphoma 1 1 1 1 1
Total 42 6 7 0 29 24 9 0 9 0 1 2 39 22 9 0 11
, increased risk; NS, non-significant association; , decreased risk; NA, not assessed.

39
Table 3. Association between cancer risk and consumption of beef, pork, lamb or poultry.
Type of cancer n. of meta-analyses Beef Pork Lamb Poultry
 NS  NA  NS  NA  NS  NA  NS  NA
Colorectal 12 1 11 1 11 1 11 2 1 9
Breast 3 3 3 3 3
Lung 2 1 1 1 1 1 1 1 1
Esophageal 6 6 6 6 3 3
Gastric 4 1 3 1 3 4 4
Hepatocellular carcinoma 1 1 1 1 1
Pancreatic 2 2 2 2 1 2
Renal 3 3 3 3 1 1 1
Oral cavity and oropharynx 1 1 1 1 1
Bladder 2 1 1 1 1 2 1 1
Ovarian 2 2 2 2 1 1
Endometrial 1 1 1 1 1
Prostate 1 1 1 1 1
Thyroid 1 1 1 1 1
Non-Hodgkin lymphoma 1 1 1 1 1
Total 42 3 1 0 38 0 4 0 38 1 1 0 40 1 10 2 39
, increased risk; NS, non-significant association; , decreased risk; NA, not assessed.

40
Table 4. Description of the search methodology used in the different meta-analyses.
Author Type of cancer Databases Keywords Period Reference
Larsson et al, Colorectal Medline “meat”, “foods”, “diet”, “colorectal”, “colon”, “rectal”, Up to march [9]
2006 “cancer”, “neoplasm”, “prospective” and “cohort” 2006
Huxley et al, Colorectal Medline and Embase “colorectal cancer”, “colorectal neoplasm”, “colon Up to [10]
2009 cancer”, “colon neoplasm”, “rectal cancer”, “rectal December
neoplasm”, “cohort”, “red meat”, “processed meat”, 2008
“fish”, “poultry”, “diet” and “lifestyle”
Alexander et Colorectal Medline “colon cancer”, “rectal cancer”, “colorectal”, “meat”, Up to July [11]
al, 2010 “processed meat”, “preserved meat”, “cured meat”, 2009
“ham” and “sausage”
Smolińska et Colorectal Medline, Scopus, “red meat” or “minced meat” or “ham” or “bacon” or Up to [12]
al, 2010 Embase, CancerLit, “sausages” or “lifestyle” or “diet” and “colorectal December
Google Scholar and cancer” or “colon cancer” or “rectal cancer” or 2009
Cochrane Library “colorectal neoplasm” or “colon neoplasm” or “rectal
neoplasm”
Alexander et Colorectal Medline Unavailable Up to June [13]
al, 2011 2009
Chan et al, Colorectal Medline Unavailable Up to March [14]
2012 2011
Magalhães et Colorectal Medline, ISI Web of “colon” or “rectum” or “colorectal” or “rectal” or Up to [15]
al, 2012 Science and Scopus “colonic” and “cancer” or “colorectal cancer” or “colon August 2012
cancer” or “rectum cancer” or “rectal cancer” and
“dietary pattern(s)” or “eating pattern(s)” or “food
pattern(s)”
Hutter et al, Colorectal Arbitrarily selected Unavailable Unavailable [16]
2012
Johnson et al, Colorectal Medline “colon” “colonic and colorectal neoplasms”, “colorectal 1966-2010 [17]
2013 risk factors” and “colorectal cancer prevention”
Pham et al, Colorectal Medline “meat” or “red meat” or “processed meat” or “poultry” August 2013 [18]
2014 and “colorectal cancer” or “colon cancer” or “rectal
cancer” or “case-control studies” or “cohort studies”
and “Japan” or “Japanese”
Woo et al, Colorectal KMBase, KoreaMed and keywords “Korean” or “Korea” and “food” or “diet” or 20 June 2014 [19]
2014 Medline “intake” or “nutrition” and “cancer risk”
41
Carr et al, Colorectal Medline and ISI Web of “colon” or “rectum” or “rectal” and “cancer” or Up to 1 [20]
2015 Science “neoplasm” or “carcinoma” or “adenoma” and “meat” August 2014
or “red meat” or “beef” or “pork” or “lamb” or “veal” or
“poultry” or “chicken” or “turkey” or “processed meat"
and “cohort” or “case control” or “follow up” or
“prospective” “cross sectional” or “randomized” and
“relative risk” or “rate” or “ratio” or “incidence”
Taylor et al, Breast Medline “breast cancer”, “diet”, “red meat” Up to May [21]
2009 2009
Alexander et Breast Medline “breast cancer(s)” or “breast neoplasm(s)” and “diet” or Up to July [22]
al, 2010 “nutrition” or “food” or “meat” or “beef” or “pork” or 2009
“lamb”
Namiranian et Breast Medline, Scopus, ISI Unavailable Up to 24 [23]
al, 2014 Web of Science August 2012
Yang et al, Lung Medline, Embase and ISI “pulmonary neoplasm” or “lung cancer” and “meat” or Up to [24]
2013 Web of Science “red meat” or “processed meat” or “white meat” or November
“beef” or “pork” or “lamb” or “goat” or “poultry” or 2011
“fish” and “case-control study” or “cohort study” or
“follow-up” or “prospective study” or “longitudinal
study”
Xue et al, 2014 Lung PubMed, Embase, ISI “lung cancer” or “lung tumor” or “lung neoplasm” or Up to 31 [25]
Web of Science, “lung carcinoma” and “dietary” or “food” or “red meat” June 2013
National Knowledge or “beef” or “pork” or “lamb” or “”processed meat” or
Infrastructure and “preserved meat” or “bacon” or “sausage” or “salted
Wanfang meat”
Huang et al, Esophageal Medline and Embase “esophag” and “adenocarcinoma” or “carcinoma” or Up to 31 [26]
2013 “cancer” and ‘‘red meat” or “processed meat” or May 2012
“preserved meat” or “beef” or “pork” or “veal” or
“mutton” or “lamb” or “ham” or “sausage” or “bacon”
or “salted meat”
Choi et al, Esophageal Medline and Embase “oesophageal” or “esophageal” or “esophagus” or Up to May [27]
2013 “oesophagus” and “cancer” or “neoplasm” or 2012
“carcinoma” and “cohort” or “prospective” or “case-
control” and “food” or “diet” or “meat”
Jiang et al, Esophageal Medline “(o)esophagi” and “cancer” or “carcinoma” or Up to [28]
42
2013 “neoplasia” or “adenocarcinoma” and “white meat” or December
“poultry” or “chicken” or “duck” or “fish” or “shellfish” 2012
or “seafood”
Salehi et al, Esophageal Medline, Embase and “meat” or “foods” or “diet” and “esophageal cancer,” 1990-2011 [29]
2013 ISI Web of Knowledge “esophageal neoplasm” “esophagus cancer” or
“esophagus neoplasm”
Qu et al, 2013 Esophageal Medline and Embase “(o)esophageal” or “(o)esophagus” and “cancer” or Up to 31 [30]
“carcinoma” or “neoplasia” and “red meat” or October
“processed meat” or “preserved meat” or “beef” or 2012
“pork” or “veal” or “mutton” or “lamb” or “ham” or
“sausage” or “bacon” or “salted meat”
Zhu et al, 2014 Esophageal Medline, Embase and “esophageal cancer” or “oesophageal cancer” or Up to April [31]
Cochrane Library “esophageal neoplasms” or “esophageal squamous cell 2013
carcinoma” or “esophageal adenocarcinoma” and
“meat” or “red meat” or “processed meat” or “white
meat” or “poultry” or “fish” or “beef” or “pork” or
“lamb” or “goat”
Larsson et al, Gastric Medline “meat” or “foods” and “stomach cancer” or “stomach Up to March [32]
2006 neoplasm” or “gastric cancer” or “gastric neoplasm” 2006
Bonequi et al, Gastric Medline and Latin “gastric cancer” or “stomach cancer” and “risk” or “risk Up to [33]
2013 American databases factors” or “risk assessment” or “epidemiologic factors” December
or “diet” or “food habits” or “meat” or “chili pepper” 2011
and “cohort studies” or “cohort” or “case-control”
Zhu et al, 2013 Gastric Medline, Embase and the “gastric cancer”, “gastric neoplasm”, “stomach cancer”, Up to April [34]
Cochrane Library “stomach neoplasm” in combination with “meat”, “red 2013
meat”, “processed meat”, “preserved meat”, “beef”,
“veal”, “pork”, “lamb”, “ham”, “sausage”, “bacon” “hot
dogs” and “salami”
Song et al, Gastic PubMed and Embase “meat” and “gastric cancer” or “stomach cancer” Up to [35]
2014 December
2013
Luo et al, 2014 Hepatocellular Medline, ISI Web of “hepatocellular carcinoma” or “hepatoma” or “liver Up to July [36]
Science and Embase cancer” or “liver tumor” and “meat” or “red meat” or 2013
“processed meat” or “white meat” or “poultry” or “fish”
or “diet” or “foods” or “beef” or “pork” or “lamb” or
43
 “goat”
Paluszkiewicz Pancreatic Medline, Cochrane “red meat” “minced meat”, “ham”, “bacon”, “sausages”, Up to [37]
et al, 2012 Library, Embase, “white meat”, “poultry”, “vegetables”, “fish”, “eggs”, December
CancerLit, Scopus and “fruits”, “lifestyle”, “diet”, “pancreatic cancer” and 2010
Google Scholar “pancreatic neoplasm”
Larsson et al, Pancreatic Medline and Embase “meat” or “foods” and “pancreatic cancer” or Up to [38]
2012 “pancreatic neoplasm” and “cohort” or “prospective” or November
“nested case-control” 2011
Faramawi et al, Renal Medline and Ovid “meat”, “red meat”, “lamb”, “beef”, “pork”, “bacon”, Up to [39]
2007 “meat products”, “poultry”, “chicken”, “renal December
neoplasm”, “kidney malignancy”, “renal cell 2006
carcinoma” and “renal cancer”
Lee et al, 2009 Renal Pooling Project of Unavailable Unavailable [40]
Prospective Studies of
Diet and Cancer
Alexander et Renal Medline “kidney neoplasm”, “renal cell carcinoma”, “renal Up to [41]
al, 2009 cancer”, “red meat”, “processed meat”, “preserved December
meat”, “beef”, “pork”, “lamb”, “ham”, “sausage” and 2007
“bacon”
Xu et al, 2014 Oral cavity and Medline, Embase, and “meat” or “lamb” or “beef” or “pork” or “bacon” or Up to May [42]
oropharynx Cochrane Library “poultry” or “chicken” and ‘‘cancer(s)’’ or 2013
Central ‘‘neoplasm(s)’’ or ‘‘malignancy(ies)’’ and “oral” or
“mouth” or “pharynx” or “pharyngeal” or
“oropharyngeal”
Wang et al, Bladder Medline “meat”, “bladder cancer”, “urothelial” and “urinary tract Up to [43]
2012 cancer” October
2010
Li et al, 2014 Bladder Medline “bladder” and “carcinoma” or “cancer” or “tumor” or Up to May [44]
“neoplasms” and “meat” or “beef” or “pork” or “lamb” 2014
Kolahdooz et Ovarian Arbitrarily selected Unavailable Unavailable [45]
al, 2010
Wallin et al, Ovarian Medline and Embase “ovarian cancer” or “ovary cancer” and “meat” or “red Up to [46]
2011 meat” or “processed meat” or “pork” or “beef” or January 2011
“foods”
Bandera et al, Endometrial Medline, ISI Web, “diet(s)” or “dietetic” or “dietary” or “eating” or Up to [47]
44
2007 Embase, Biosis, Ingenta, “intake” or “nutrient(s)” or “nutrition” or December
CINAHL, Science “vegetarian(s)” or “vegan(s)” or “seventh day adventist” 2006
Direct, LILACS, Pascal, or “macrobiotic” or “food” and “meat” or “beef” or
ExtraMed, and Allied “pork” or “lamb” or “poultry” or “chicken” or “turkey”
CompMed or “duck” or “fish” or “egg” or “eggs” or “shellfish” or
“seafood” or “dairy” or “milk”
Alexander et Prostate Medline “prostate cancer” and “meat” or “beef” or “pork” or Up to [48]
al, 2010 “lamb” January 2009
Liu et al, 2014 Thyroid Medline Unavailable Up to March [49]
2014
Fallahzadeh et Non-Hodgkins Cochrane Library, “non-Hodgkins lymphoma”, “NHL”, “processed meat”, Up to 5 [50]
al, 2014 lymphoma Medline, and Science “follicular lymphoma”, “FL”, “diffuse large Bcell”, September
Citation Index ”DLBCL”, “chronic lymphocytic leukemia” and 2014
“CLL/SL”

45