Animal Protein and Cancer Risk

question mark

Do all animal foods increase the risk for cancer?  What factors within animal food are problematic?

Claim: A plant-based diet with minimal to no animal protein is the best diet to lower cancer risk.   

Overview

In this article we will be reviewing various animal proteins and if the consumption of these foods is associated with an increased risk for cancer.  We will also explore the effects of preparation and processing of the animal protein compared to the protein itself.  Our goal is to evaluate and decide whether or not it is safe to eat an omnivorous diet and to discuss specific guidelines as to how much, how often, and with what overall dietary pattern we should be aiming for.

There have been several decades of research on this topic.  We have limited our review to the last 10 years to try and get the most recent data on this subject.  We will spend quite a bit of the discussion looking at the mechanisms as to why some animal proteins may be more problematic than plant sources of protein. 

Below is a list of the animal proteins we will be researching.

Animal Protein

Examples

Red Meat

Beef, veal, lamb, pork

Processed Meat   

Red meat that has been preserved (curing, smoking, salting, drying)

Poultry

Chicken, turkey, duck

Dairy

Milk, yogurt, cheese

Eggs

 

Fish

Fin and shellfish

 

Cooking and Processing Methods

Cooking animal foods at high-heat will create carcinogens. The by-products include Heterocyclic Amines (HCAs) and Polycylic Aromatic Hydrocarbons (PAHs). HCAs are made when creatines and amino acids (both found in meats) react together with heat.  This reaction starts to occur at 212 F (100 C) but happens more rapidly from about 572 F (300 C) and higher. PAHs include over 100 different compounds formed by the incomplete burning of organic matter at temperatures in excess of 392 F (200 C). Essentially the hotter and longer a meat is cooked, the more HCAs and PAHs produced. Direct heat methods like grilling and frying produce more HCA’s and PAH’s than indirect-heat methods like stewing, steaming, or poaching.

Processing meats add chemicals, like nitrites, that generate N-Nitroso Compounds (NOCs); another class of carcinogenic compounds.

Nutrients Within

Does the problem lie with the nutrients within the animal food? Some of the problems that will be discussed further relate to the fat content, specifically cholesterol content of the food. Another concern is heme iron, which is particularly high in red meat, liver, and processed meat. Yet another concern lies with choline content, which is high in eggs, liver, red meat, and milk. The potential concern with choline is that it is eventually converted in the liver to trimethylamine oxide, which increases inflammation in the body. (1)

Industry Practices

Yet another potential problem is how the industrialized husbandry practices affect the quality of the animal food we are eating.  Pesticides used on feed and/or medications or hormones given to the animal can create toxic residues left in the meat that we then consume. In addition to whether pesticides are being used on the feed, what the animal is eating is equally important. As discussed in Important Foods for Cancer Patients, there is concern regarding the inflammation producing properties found in meat from animals fed grain-based diets. According to a Review written in Nutrition Journal in 2010 (2), grass-based diets produce higher contents of omega-3s and CLA in the beef as well as higher levels of antioxidants. We’ve discussed the anti-inflammatory benefits of Omega-3s throughout the website. Conjugated Linoleic Acid (CLA) is a naturally occurring fatty acid made from the omega-6 essential fatty acids found in meat and dairy. The isomers of CLA have been studied for their potential benefit with immune support and in weight loss. Research suggests that pastured cows produce up to 500% more CLA than grain-fed cows (2).

 

What is the Evidence?

Before we get into the details of the research we reviewed we think it’s important to point out some of the limitations of the research in this area. Almost all of the studies we reviewed were pre-clinical animal model studies, which means that those results may or may not translate to human populations. Most of the rest of the studies were epidemiological, which is not possible to be conclusive regarding cause and effect. It’s also important to point out that none of the studies commented on whether the animal protein consumed was organic or grass-fed. Based on what we know about the inflammatory markers alone this is a very important factor when making correlations between exposure and disease risk.

Red Meat:

In the text above we described how cooking methods are one of the factors contributing to the concern with meat and cancer. The by-products of high heat cooking have been shown to be carcinogenic. According to a number of pre-clinical animal studies, HCAs have been shown to increase the occurrence of tumors in multiple sites; mammary, lung, colon, stomach, prostate, pancreas, esophagus (3). It’s important to keep in mind that any animal protein can create HCAs if cooked at a high enough heat.

Although the studies we reviewed showed a positive association with high meat intake and the following cancers: esophageal, lung, pancreatic, colorectal, breast, and stomach, there were mixed results seen for a correlation between meat intake and endometrial, bladder, or ovarian cancer. 

Among over 60,000 women in the Swedish Mammography Cohort, a modest elevation in risk for endometrial cancer was shown with those with the highest intake of heme iron, especially from consuming liver (4). There was no statistically significant association observed for intakes of other red or processed meats. The pooled results of 10 cohort studies and 11 case-control studies indicate that overall meat intake was not related to risk of bladder cancer, however, those with the highest intake of red and processed meats were at a 17% or 10% increased risk respectively (5). A dose-response meta-analysis of 8 cohort studies concluded that there was no association seen between the intake of red and processed meats and the risk for ovarian cancer (6).

According to the results of 4 different meta-analysis (7-10), the combined results of 7 cohort and over 30 case control studies, concluded that individuals with the highest intake of red meat, which was measured at 3.5-4.2 ounces of red meat per day, have an increased risk for developing esophageal cancer; ranging from 26-57% higher risk depending on the study. Most concern seems to lie in the high amount of heme iron found in meat as well as the HCAs and PAHs produced from cooking meat at high temperatures. 

A number of studies in the literature have examined the association between red meat intake and colorectal cancer. The potential mechanisms may be due to the production of HCAs secondary to high-heat cooking. According to 1 meta-analysis of 16 case-control and 5 cohort studies, for every 100 gram (3.5 oz) per day increase in red meat intake there is a 36% increased risk of colorectal cancer (11). According to another meta-analysis of 3 case-control and 21 cohort studies, the risk of colorectal cancers significantly increases linearly with increasing intake of red meat up to 140 grams (5 oz) per day, where the curve approaches its plateau (12).

For breast cancer the association between red meat intake and increased risk seems to be due to a combination of factors including heme iron content, by-products of cooking, exogenous hormones used to treat commercially raised cattle, and an animal sugar known as NEUR5gc, which can be absorbed by human tissue and leads to inflammation and tumor formation in prospective studies (13). One prospective study suggested an association between higher red meat intake in early adulthood and increased risk for breast cancer later in life (14). This same study showed that by replacing red meat with a combination of other proteins (legumes, poultry, nuts, fish) one could reduce their risk for breast cancer.

The heme iron content of red meat may also be implicated for an increased risk of stomach cancer as heme iron is a growth factor for H. Pylori (15). The by-products of high-heat cooking have shown an association with an increased risk of pancreatic cancer (16).  Reviewing data from a large prospective cohort study (over 12,000 people) showed that total dietary fat intake, specifically saturated fat from red meat and dairy products, was associated with increased risk for pancreatic cancer (17). Furthermore, a meta-analysis of pancreatic cancer risk factors showed a positive association with red meat consumption, but only in men (18). Consuming meat 3 or more times per week may also increase the risk of lung cancer by as much as 35%, according to evidence from the meta-analysis of 23 case-control and 11 cohort studies (19).

Processed Meat:

The link between cancer risk and consumption of processed meats is well supported in the literature. This association is due not only to the mechanistic concerns with red meat, heme iron content, HCAs and PAHs, but also from the processing methods that add an additional layer of toxic compounds. 

As with red meat, the association with processed meat and esophageal cancer is relatively robust. A 2014 meta-analysis showed high processed meat intake was likely to increase the risk of esophageal cancer (10). Two other meta-analysis showed associations that individuals with the highest consumption of processed meat, measured between 50-100 grams per day (1.75-3.5 oz), were at highest risk for developing esophageal cancer; up to a 40% higher risk (7, 9). In other observational studies, the risk ranged from 41-55% of developing esophageal cancer for those with a high intake of processed meat (8, 20). With many of these studies, the primary concern relates to the heme iron content. Salted meat consumption in particular seems to have a strong association with esophageal cancer, particularly when it’s combined with alcohol and/or smoking (21).

Salted meat also seems to increase the risk of gastric cancer, according to another meta-analysis (22). The high salt intake damages mucosa within the stomach and increases the risk for H. pylori infection; a known risk factor for gastric cancer.

As was the case with red meat, the consumption of processed meat poses a significant risk for colorectal cancers. According to meta-analysis, processed meat intake is even more closely linked with colorectal cancers than intake of fresh red meat (23). For every 50 gram (1.75 oz) per day increase in processed meat intake there is a 28% increased risk of colorectal cancer (11). The risk of colorectal cancers significantly increases linearly with every 50 gram per day intake of processed meat up to 140 grams (5 oz) per day, where the curve approaches its plateau (12).

As with that of red meat, the association between processed meat intake and increased risk of breast cancer seems to be due to a combination of factors including heme iron content, the by-products of cooking, exogenous hormones used to treat commercially raised cattle, and an animal sugar known as NEUR5gc, which can be absorbed by human tissue and leads to inflammation and tumor formation (13). Furthermore, smoked meat seems to be a particular problem. In a case-controlled study of 400 women, daily intake of smoked meat significantly increased risk for breast cancer in both pre and post-menopausal women (24).

The by-products of processing have also shown associations with several other cancers. There is an increased risk of oral cancer with increasing processed meat intake (25). N-nitroso compounds (NOCs) also seem to be particularly problematic as they have been shown to reach the pancreas via the blood stream. They are potent carcinogens in pre-clinical animal studies thereby increasing the risk for pancreatic cancer (18). They have also been shown to cross the blood brain barrier, which may increase risk for glioma (26). 

Poultry:

Poultry, on the other hand, may lead to a decreased risk of cancer. A meta-analysis looking at poultry intake and colorectal cancer showed a significant inverse association with at least a 50 gram (1.75 oz) per day poultry intake (27). The incidence of esophageal cancer and lung cancer were also decreased with poultry intake (10, 19). The mechanisms responsible for this inverse association may be explained by an overall healthier lifestyle or because of the lower heme iron content in poultry. There was one study looking at the post-diagnosis diet of over 27,000 men diagnosed with prostate cancer which found an increased risk of cancer from those eating chicken with the skin on (28). This increased risk is likely secondary to the formations of HCAs and PAHs from high-heat cooking.

Dairy:

Dairy is an interesting category of animal food as it seems to show some negative and some positive associations with risk for cancer. Certain components of dairy foods such as probiotic content, calcium, vitamin D, and CLA may all have protective effects.  Where-as other compounds such as IGF-1 and phosphorous may have negative effects.

The research is mixed around gastric cancer. A 2015 meta-analysis of 17 case-control and 6 cohort studies showed protective effects with the highest total dairy intake and hypothesized that it may be due to the anti-cancer properties of vitamin D and calcium or probiotic-rich dairy foods (like yogurt and kefir), which interfere with H. pylori colonization, or even the phospholipid content increasing cellular renewal (29). Another meta-analysis showed that dairy products were unlikely to be strongly protective against gastric cancer but didn’t increase risk (30). And yet another meta-analysis showed a non-significant increased risk of gastric cancer with dairy intake (31). As you can see, the research is somewhat conflicting.

The CLA in dairy may be protective against breast cancer due to its anti-inflammatory properties (32). The authors hypothesize that calcium and vitamin D may also offer anti-carcinogenic benefits on breast cancer cells. A meta-analysis of colorectal cancer showed a statistically significant reduction in risk with high intake of milk (7 oz per day) and total dairy, excluding cheese (14 oz per day) (33).  The authors hypothesize that the protection is likely due to high calcium intake as trials have found reduced risk of colorectal recurrence with calcium supplementation (1200-2000 mg/day).

There was no association between dairy intake and pancreatic cancer risk observed in a pooled analysis of 14 cohort studies (34).  Although as mentioned above under “Red Meats”, the dietary fat content of dairy foods has shown some association of increased risk for pancreatic cancer (17). The results of a meta-analysis showed increased prostate cancer risk with high intake of dairy foods; 14 oz/day total dairy, 7 oz/day milk, 3.5 oz/day yogurt, 1.75 oz cheese. One set of authors hypothesize that this is because of dairy’s IGF-1 content, which promotes proliferation of cancer cells and inhibits apoptosis of prostate cells (35). They also speculate that it could be due to dairy’s high calcium intake interfering with vitamin D levels. However, another set of authors believe that it’s dairy’s high phosphate content, rather than the calcium content, that reduces systemic serum vitamin D levels (36). Results from epidemiological studies examining the association between the use of dairy products and risk for ovarian cancer have been conflicting. According to one study, evaluating data from a large Danish population-based case-control study (with over 2000 women), an association between intake of dairy foods and increased risk of ovarian cancer was noted (37). The association, however, was strongest with milk and lowest for cheese.

Eggs:

Although eggs are lumped into an overall healthier dietary pattern in some prospective studies (chicken, eggs, legumes, nuts), there are other studies suggesting concern around egg consumption and increased cancer risk. For prostate cancer in particular, there are several studies which found an increased risk. According to a prospective study published in Cancer Prevention Research, healthy men who consumed 2.5 or more eggs per week had an 81% increased risk of lethal prostate cancer compared with men who consumed less than 0.5 eggs per week (28). The authors hypothesized that this was due to a high level of cholesterol and choline in the eggs, which are both highly concentrated in prostate cancer cells. In 2012, the authors looked specifically at choline content and found that men in the highest quintile of choline intake (471 mg/day) had a 70% increased risk of lethal prostate cancer (38). Although choline is found in all animal foods it is more highly concentrated in eggs at 250 mg per egg.

A meta-analysis published in 2015 showed a modestly elevated risk for not only prostate cancer but also breast and ovarian cancers for those with the highest intake of eggs, more than 5 per week, as compared to those with no egg consumption at all (39). These authors also suggest that the choline and cholesterol were causative. Choline may increase the proliferation and progression of prostate cancer (1), while cholesterol serves as a pre-cursor for the biosynthesis of sex hormones and a primary metabolite of cholesterol acts as an estrogen receptor agonist in breast cancer cells (39). Another 2015 meta-analysis showed an association between egg consumption and increased risk for ovarian cancer (40). Cohort studies have also shown an association between egg consumption and increased breast cancer risk; especially for post-menopausal women (41). This seemed to be true for those consuming 2-5 eggs/week.

A 2014 meta-analysis published findings from 37 case-control studies and 7 cohort studies supporting the association between egg consumption and increased risk for GI cancers; with a stronger correlation for colon cancer and in Western populations (42). Another recent case control study showed a connection between dietary cholesterol intake and risk of bladder cancer (43). Cholesterol is converted in the liver to primary bile acids, which are then converted in the gut by bacterial flora into secondary bile acids. The concern is that these bile acids produce reactive oxygen species, NF-kB activation, DNA damage, and increase cellular resistance to apoptosis (44). The overall risk for bladder cancer increased two-fold with an intake of 6 fried eggs per week versus those who ate 0 eggs. No association was found with boiled eggs, begging the question that the culprit may again lie with the by-products of high-heat cooking rather than the eggs themselves (43).

Fish:

Fish on the other hand seems protective against cancer. The only exception might be fried fish. Frying fish decreases the omega-3 content of the fish and generates HCAs, oxidized lipids, and trans-fatty acids, all of which then increase cancer risk. A case control study found that frying fish increased the risk for pancreatic cancer (16).

Higher consumption of fish has been associated with decreased risks for all of the following cancers: esophageal, breast, ovarian, colorectal, and liver. The primary mechanism is thought to be related to omega-3 intake. Omega-3s inhibit eicosanoid release, which reduces inflammation. Omega-3s can also regulate transcription factor activity, regulate gene expression and signal transduction for cell growth, apoptosis, angiogenesis, and metastasis (45). Pre-clinical animal studies have shown that supplemental omega-3 has the ability to slow the growth of various cancers and fish consumption has been advised to reduce cancer occurrence (46).

A meta-analysis showed that a daily increase of 50 grams (1.75 oz) per day of fish lowers the risk of esophageal cancer (9). Another meta-analysis also showed an association between fish intake and lowered risk for esophageal cancer (8).

A meta-analysis of prospective cohort studies supported a higher consumption of fish (dietary marine omega-3) to decrease the risk of breast cancer 45. A 50% decreased risk was observed for every 1 gram per day intake of marine omega-3. However, no significant association was seen with plant based dietary omega-3. The fattier the fish the higher amount of omega-3 it contains. This association was demonstrated in a meta-analysis, which initially found no association between fish intake and risk for ovarian cancer but did find a significant decrease in risk associated with fatty fish intake (47).

Another meta-analysis found an association between fish consumption and prevention of colorectal cancer (48). Another study also showed that eating fish reduced the prevalence of colorectal cancers, which the authors felt was due to the high selenium content found in fish (49).

The anti-inflammatory properties of omega-3s were also found to be beneficial in reducing the risk of liver cancer (50). Liver cancer risk was reduced by 6-18% with a 1-2 servings per week intake of fish respectively (51).

 

What Is Our Recommendation?

The over-arching claim to avoid all meat and animal products is not warranted. You do not need to be vegan to lower your risk for cancer but you do need to consume a lot of plant foods. After reviewing recent research the risk versus benefit of animal foods varies quite a bit depending on the type of animal protein and the way it is prepared. Overall the cooking method (e.g., high temperature cooking) and processing of meat (e.g., smoking and curing) provide the strongest concern for cancer risk whereas certain animal proteins, especially fish, may actually be protective.

Here are our guidelines:

  • First and foremost include a large variety of colorful fruits and vegetables in your diet.
  • Next, vary your protein sources, including plant based sources of protein (beans, lentils, nuts, seeds) on a regular basis.
    • Aim to have fish 2 or more times per week; the fattier the better.
    • Poultry, without the skin, would be your next best option.
    • Limit eggs to 1 or 2 times per week; soft and hard boiled will be a better option than scrambled or fried.  Consider avoiding eggs completely if you have had a reproductive cancer or are at high-risk for breast, ovarian, and prostate cancer.
    • Limit red meat to once a week or less and avoid cooking at high temperatures.
  • Buy the best quality animal protein that you can to decrease your exposure to environmental carcinogens, antibiotics, and hormones as well as to improve the fat profile; 100% grass-fed or pasture raised is best.
    • Grass fed and pasture raised animals produce meat, dairy, and eggs that are naturally lower in cholesterol and higher in omega-3s, thus reducing the inflammatory potential of the food. In the research we reviewed, there have been no studies comparing the cancer causing risk of grass-fed versus conventionally fed meats.
  • Avoid cooking your animal proteins at high temperature.
    • Keep the heat below 400 degrees Fahrenheit (200 degrees Centigrade).
    • HCA formation can also be substantially decreased by increasing the frequency of flipping during cooking; limit the amount of time you leave the meat on the heat surface (16).
    • Choose cooking methods that avoid direct heat: steaming, poaching, stewing
  • Add marinades and other sources of antioxidants.
    • Formation of HCA during cooking of beef, fish, or chicken can be decreased by marinating or brief microwave cooking before frying, broiling, or grilling (16).
    • Combining colorful vegetables with your meats provides good sources of calcium, chlorophyll, vitamin C, and polyphenols, all of which may reduce the negative effects of heme iron found in the meat (23).
  • Avoid the following:
    • Charred, fried, and processed meats.
    • Gravy made from meat drippings

 

References:

1.           Awwad HM, Geisel J, Obeid R. The role of choline in prostate cancer. Clinical biochemistry 2012;45:1548-53.

2.           Daley CA, Abbott A, Doyle PS, Nader GA, Larson S. A review of fatty acid profiles and antioxidant content in grass-fed and grain-fed beef. Nutrition journal 2010;9:10.

3.           Zheng W, Lee SA. Well-done meat intake, heterocyclic amine exposure, and cancer risk. Nutrition and cancer 2009;61:437-46.

4.           Genkinger JM, Friberg E, Goldbohm RA, Wolk A. Long-term dietary heme iron and red meat intake in relation to endometrial cancer risk. Am J Clin Nutr 2012;96:848-54.

5.           Wang C, Jiang H. Meat intake and risk of bladder cancer: a meta-analysis. Medical oncology (Northwood, London, England) 2012;29:848-55.

6.           Wallin A, Orsini N, Wolk A. Red and processed meat consumption and risk of ovarian cancer: a dose-response meta-analysis of prospective studies. British journal of cancer 2011;104:1196-201.

7.           Choi Y, Song S, Song Y, Lee JE. Consumption of red and processed meat and esophageal cancer risk: meta-analysis. World journal of gastroenterology 2013;19:1020-9.

8.           Huang W, Han Y, Xu J, Zhu W, Li Z. Red and processed meat intake and risk of esophageal adenocarcinoma: a meta-analysis of observational studies. Cancer causes & control : CCC 2013;24:193-201.

9.           Salehi M, Moradi-Lakeh M, Salehi MH, Nojomi M, Kolahdooz F. Meat, fish, and esophageal cancer risk: a systematic review and dose-response meta-analysis. Nutrition reviews 2013;71:257-67.

10.        Zhu HC, Yang X, Xu LP, et al. Meat consumption is associated with esophageal cancer risk in a meat- and cancer-histological-type dependent manner. Digestive diseases and sciences 2014;59:664-73.

11.        Xu X, Yu E, Gao X, et al. Red and processed meat intake and risk of colorectal adenomas: a meta-analysis of observational studies. Int J Cancer 2013;132:437-48.

12.        Chan DS, Lau R, Aune D, et al. Red and processed meat and colorectal cancer incidence: meta-analysis of prospective studies. PloS one 2011;6:e20456.

13.        Guo J, Wei W, Zhan L. Red and processed meat intake and risk of breast cancer: a meta-analysis of prospective studies. Breast cancer research and treatment 2015;151:191-8.

14.        Farvid MS, Cho E, Chen WY, Eliassen AH, Willett WC. Dietary protein sources in early adulthood and breast cancer incidence: prospective cohort study. BMJ (Clinical research ed) 2014;348:g3437.

15.        Song P, Lu M, Yin Q, et al. Red meat consumption and stomach cancer risk: a meta-analysis. Journal of cancer research and clinical oncology 2014;140:979-92.

16.        Yu XF, Zou J, Dong J. Fish consumption and risk of gastrointestinal cancers: a meta-analysis of cohort studies. World journal of gastroenterology 2014;20:15398-412.

17.        Thiebaut AC, Jiao L, Silverman DT, et al. Dietary fatty acids and pancreatic cancer in the NIH-AARP diet and health study. J Natl Cancer Inst 2009;101:1001-11.

18.        Larsson SC, Wolk A. Red and processed meat consumption and risk of pancreatic cancer: meta-analysis of prospective studies. British journal of cancer 2012;106:603-7.

19.        Yang WS, Wong MY, Vogtmann E, et al. Meat consumption and risk of lung cancer: evidence from observational studies. Annals of oncology : official journal of the European Society for Medical Oncology 2012;23:3163-70.

20.        Qu X, Ben Q, Jiang Y. Consumption of red and processed meat and risk for esophageal squamous cell carcinoma based on a meta-analysis. Annals of epidemiology 2013;23:762-70 e1.

21.        Lin S, Wang X, Huang C, et al. Consumption of salted meat and its interactions with alcohol drinking and tobacco smoking on esophageal squamous-cell carcinoma. Int J Cancer 2015;137:582-9.

22.        Zhu H, Yang X, Zhang C, et al. Red and processed meat intake is associated with higher gastric cancer risk: a meta-analysis of epidemiological observational studies. PloS one 2013;8:e70955.

23.        Bastide NM, Pierre FH, Corpet DE. Heme iron from meat and risk of colorectal cancer: a meta-analysis and a review of the mechanisms involved. Cancer prevention research (Philadelphia, Pa) 2011;4:177-84.

24.        Lee H, Wang Q, Yang F, et al. SULT1A1 Arg213His polymorphism, smoked meat, and breast cancer risk: a case-control study and meta-analysis. DNA and cell biology 2012;31:688-99.

25.        Xu J, Yang XX, Wu YG, Li XY, Bai B. Meat consumption and risk of oral cavity and oropharynx cancer: a meta-analysis of observational studies. PLoS One 2014;9:e95048.

26.        Wei Y, Zou D, Cao D, Xie P. Association between processed meat and red meat consumption and risk for glioma: a meta-analysis from 14 articles. Nutrition (Burbank, Los Angeles County, Calif) 2015;31:45-50.

27.        Shi Y, Yu PW, Zeng DZ. Dose-response meta-analysis of poultry intake and colorectal cancer incidence and mortality. European journal of nutrition 2015;54:243-50.

28.        Richman EL, Kenfield SA, Stampfer MJ, Giovannucci EL, Chan JM. Egg, red meat, and poultry intake and risk of lethal prostate cancer in the prostate-specific antigen-era: incidence and survival. Cancer prevention research (Philadelphia, Pa) 2011;4:2110-21.

29.        Guo Y, Shan Z, Ren H, Chen W. Dairy consumption and gastric cancer risk: a meta-analysis of epidemiological studies. Nutrition and cancer 2015;67:555-68.

30.        Tian SB, Yu JC, Kang WM, Ma ZQ, Ye X, Cao ZJ. Association between dairy intake and gastric cancer: a meta-analysis of observational studies. PloS one 2014;9:e101728.

31.        Sun Y, Lin LJ, Sang LX, Dai C, Jiang M, Zheng CQ. Dairy product consumption and gastric cancer risk: a meta-analysis. World journal of gastroenterology 2014;20:15879-98.

32.        Dong JY, Zhang L, He K, Qin LQ. Dairy consumption and risk of breast cancer: a meta-analysis of prospective cohort studies. Breast cancer research and treatment 2011;127:23-31.

33.        Aune D, Lau R, Chan DS, et al. Dairy products and colorectal cancer risk: a systematic review and meta-analysis of cohort studies. Annals of oncology : official journal of the European Society for Medical Oncology 2012;23:37-45.

34.        Genkinger JM, Wang M, Li R, et al. Dairy products and pancreatic cancer risk: a pooled analysis of 14 cohort studies. Annals of oncology : official journal of the European Society for Medical Oncology 2014;25:1106-15.

35.        Aune D, Navarro Rosenblatt DA, Chan DS, et al. Dairy products, calcium, and prostate cancer risk: a systematic review and meta-analysis of cohort studies. Am J Clin Nutr 2015;101:87-117.

36.        Newmark HL, Heaney RP. Dairy products and prostate cancer risk. Nutrition and cancer 2010;62:297-9.

37.        Faber MT, Jensen A, Sogaard M, et al. Use of dairy products, lactose, and calcium and risk of ovarian cancer - results from a Danish case-control study. Acta Oncol 2012;51:454-64.

38.        Richman EL, Kenfield SA, Stampfer MJ, et al. Choline intake and risk of lethal prostate cancer: incidence and survival. Am J Clin Nutr 2012;96:855-63.

39.        Keum N, Lee DH, Marchand N, et al. Egg intake and cancers of the breast, ovary and prostate: a dose-response meta-analysis of prospective observational studies. The British journal of nutrition 2015;114:1099-107.

40.        Zeng ST, Guo L, Liu SK, et al. Egg consumption is associated with increased risk of ovarian cancer: Evidence from a meta-analysis of observational studies. Clinical nutrition (Edinburgh, Scotland) 2015;34:635-41.

41.        Si R, Qu K, Jiang Z, Yang X, Gao P. Egg consumption and breast cancer risk: a meta-analysis. Breast cancer (Tokyo, Japan) 2014;21:251-61.

42.        Tse G, Eslick GD. Egg consumption and risk of GI neoplasms: dose-response meta-analysis and systematic review. European journal of nutrition 2014;53:1581-90.

43.        Li F, Zhou Y, Hu RT, et al. Egg consumption and risk of bladder cancer: a meta-analysis. Nutrition and cancer 2013;65:538-46.

44.        Ajouz H, Mukherji D, Shamseddine A. Secondary bile acids: an underrecognized cause of colon cancer. World journal of surgical oncology 2014;12:164.

45.        Zheng JS, Hu XJ, Zhao YM, Yang J, Li D. Intake of fish and marine n-3 polyunsaturated fatty acids and risk of breast cancer: meta-analysis of data from 21 independent prospective cohort studies. BMJ (Clinical research ed) 2013;346:f3706.

46.        Song J, Su H, Wang BL, Zhou YY, Guo LL. Fish consumption and lung cancer risk: systematic review and meta-analysis. Nutrition and cancer 2014;66:539-49.

47.        Jiang PY, Jiang ZB, Shen KX, Yue Y. Fish intake and ovarian cancer risk: a meta-analysis of 15 case-control and cohort studies. PLoS One 2014;9:e94601.

48.        Wu S, Feng B, Li K, et al. Fish consumption and colorectal cancer risk in humans: a systematic review and meta-analysis. The American journal of medicine 2012;125:551-9 e5.

49.        Pham NM, Mizoue T, Tanaka K, et al. Fish consumption and colorectal cancer risk: an evaluation based on a systematic review of epidemiologic evidence among the Japanese population. Japanese journal of clinical oncology 2013;43:935-41.

50.        Luo J, Yang Y, Liu J, et al. Systematic review with meta-analysis: meat consumption and the risk of hepatocellular carcinoma. Alimentary pharmacology & therapeutics 2014;39:913-22.

51.        Huang RX, Duan YY, Hu JA. Fish intake and risk of liver cancer: a meta-analysis. PLoS One 2015;10:e0096102.

Back to top