Three out of four American households own a barbecue grill, according to the Health, Patio, & Barbecue Association. Yet many consumers are unaware that grilling some popular food items can produce cancer-causing compounds called heterocyclic amines (HCAs). Which foods contain the highest concentrations of HCAs? To answer that question, nutrition professionals with The Cancer Project determined the level of HCAs found in commonly grilled foods.

Background
HCAs, a family of mutagenic and cancer-causing compounds, are produced during the cooking of many animal products, including chicken, beef, pork, and fish. In January of 2005, the federal government officially added HCAs to its list of known carcinogens.1

Findings
Cancer Project nutritionists determined that many commonly grilled foods contain alarmingly high levels of HCAs. This table lists the five foods containing the highest levels.

Top Five Worst Foods to Grill

Food HCAs ng/100g*

1. Chicken breast, well done : 14,300 ng/100g2

2. Steak, grilled, well done : 810 ng/100g3

3. Pork, barbecued : 470 ng/100g4

4. Salmon, grilled with skin : 166 ng/100g5

5. Hamburger, grilled, well done : 130 ng/100g3

Safer Alternatives for Grilling
Other foods produce undetectable levels or negligible concentrations of HCAs when they are grilled. These include soy-based veggie burgers, veggie brochettes, and portabello mushroom “steaks.” These healthy vegetarian alternatives are also low in fat and cholesterol.

Grilled Meat High in HCAs
Grilled meat yields some of the highest concentrations of heterocyclic amines (HCAs).6 These compounds form when a combination of creatine (a specific amino acid found in muscle) and sugars, which are both found naturally in meats, are heated during cooking.7 Grilling is particularly carcinogen-forming because the process involves high heat and long cooking times. Nearly all meats, including chicken and fish, produce significant amounts of HCAs when tossed on the grill.

Meat that is grilled, fried, or oven-broiled often produces large quantities of HCAs.8,9,10 The longer and hotter the meat is cooked, the more these compounds form. The major classes of HCAs include amino-imidazo-quinolines, or amino-imidazo-quinoxalines (collectively called IQ-type compounds), and amino-imidazo-pyridines. Within these families, MeIQx and PhIP are the members most abundantly found in cooked meats.

High meat intake has been correlated with increased risk of cancer, particularly of the breast and colon.11 While the fat in meat is most commonly associated with cancer risk, HCAs also play a role. As known mutagens, HCAs can bind directly to DNA, cause mutation, and promote cancer initiation.12

Because HCA concentration increases with heat and time, it would be expected that well-done meat would increase the risk of cancer. This is exactly what researchers have found. In a recent review of 30 epidemiologic studies investigating the link between well-done meat consumption and cancer at various sites, 80 percent showed a positive correlation.13

Plant-Based Foods Yield Negligible HCAs
Since creatine, one of the ingredients for the formation of HCAs, is mostly found in muscle tissue, it is not surprising that grilled veggie burgers and other vegetarian foods contain either no HCAs or negligible levels.6

Choosing plant-based foods instead of meat also lowers cancer risk in other ways. Not only are vegetables low in fat and high in fiber, they also contain many cancer-fighting substances. Carotenoids, the pigment that gives fruits and vegetables their dark colors, have been shown to help prevent cancer. Beta-carotene, present in dark green and yellow vegetables, helps protect against lung cancer and may help prevent cancers of the bladder, mouth, larynx, esophagus, breast, and other sites. Many studies have found that diets rich in fruits and vegetables and low in animal fat cut cancer risks.

Other Dangers of Grilled Meat
Grilling meat also produces other types of food mutagens. Grilling or broiling meat over a direct flame results in fat dropping on the hot fire and the production of polycyclic aromatic hydrocarbon-containing flames. Polycyclic aromatic hydrocarbons (PAHs) adhere to the surface of food; the more intense the heat, the more PAHs are present.14 They are widely believed to play a significant role in human cancers.15 A fairly consistent association between grilled or broiled, but not fried, meat consumption and stomach cancer implies that dietary exposure to PAHs may play a role in the development of stomach cancer.11

Hotdogs Contain Other Carcinogens
While HCAs do not form in grilled hotdogs, these highly processed meat products contain other carcinogens. Nitrates and N-nitroso compounds, preservatives found in processed foods such as hotdogs and sausages, have long been recognized as potent carcinogens.16 Increased dietary intake of processed meats have been linked to increased cancers at various sites, including the colon,17 the pancreas,18 and the gastrointestinal tract.19

Red Meat Increases Cancer Risk
Red meat increases the risk of cancer. Recent studies show that red meat can increase colon cancer risk as much as 300 percent.20 While dietary factors such as the fat content and the lack of protective fiber in red meat are considered significant contributors, HCAs were specifically found to increase colon cancer risk.21

Chicken and Fish Increase Cancer Risk
Many people switch to chicken and fish, believing these to be healthier alternatives to beef. But that is not the case. On the grill, chicken produced more than 10 times the amount of the carcinogenic heterocyclic amines found in grilled beef. Furthermore, nearly all the HCAs detected were in the form of PhIP, which has specifically been implicated in breast cancer risk.12 This increased PhIP formation is likely due to the fact that chicken contains a large amount of phenylalanine, tyrosine, and isoeucine, amino acids that contribute to HCA formation. Fish also contains significant amounts of creatine, one of the other main ingredients for the formation of the carcinogens; not surprisingly, fish showed significant HCA formation as well.

What Should Go On the Grill?
Consumers who want to reduce their cancer risk need not give up grilling. Reducing exposure to carcinogens is as simple as grilling veggie burgers instead of hamburger, or a thick portabello mushroom instead of a steak. Steering clear of animal products is a key step in avoiding heterocyclic amines, polyaromatic hydrocarbons, nitrosamines, and other cancer-promoting substances. For healthy recipes, go to PCRM's great recipes for the grill and picnic basket.

References:
1. U.S. Department of Health and Human Services, Public Health Service, National Toxicology Program. 2005. 11th Report on Carcinogens. Available at ntp.niehs.nih.gov/ntp/roc/toc11.html.
2. Sinha R, Rothman N, Brown ED, Salmon CP, Knize MG, Swanson CA, Rossi SC, Mark SD, Levander OA, Felton JS. High concentrations of the carcinogen 2-amino-1-methyl-6-phenylimidazo- [4,5-b]pyridine (PhIP) occur in chicken but are dependent on the cooking method. Cancer Res. 1995 Oct 15;55(20):4516-9.
3. Sinha R, Rothman N, Salmon CP, Knize MG, Brown ED, Swanson CA, Rhodes D, Rossi S, Felton JS, Levander OA. Heterocyclic amine content in beef cooked by different methods to varying degrees of doneness and gravy made from meat drippings. Food Chem Toxicol. 1998 Apr;36(4):279-87.
4. Murray S, Lynch AM, Knize MG, Gooderham MJ. Quantification of the carcinogens 2-amino-3,8-dimethyl- and 2-amino-3,4,8-trimethylimidazo[4,5-f]quinoxaline and 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in food using a combined assay based on gas chromatography-negative ion mass spectrometry. J Chromatogr. 1993 Jul 2;616(2):211-9.
5. Kataoka H, Nishioka S, Kobayashi M, Hanaoka T, Tsugane S. Analysis of mutagenic heterocyclic amines in cooked food samples by gas chromatography with nitrogen-phosphorus detector. Bull Environ Contam Toxicol. 2002 Nov;69(5):682-9.
6. Nagao, M and Sugimura, T. Food Borne Carcinogens: Heterocyclic Amines. John Wiley & Sons, Ltd. New York: 2000.
7. Jagerstad M, Skog K, Grivas S, Olsson K. Formation of heterocyclic amines using model systems. Mutat Res. 1991;259:219-33.
8. Skog KI, Johansson MAE, Jagerstad MI. Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence, and intake. Food and Chem Toxicol 1998;36:879-96.
9. Robbana-Barnat S, Rabache M, Rialland E, Fradin J. Heterocyclic amines: occurrence and prevention in cooked food. Environ Health Perspect 1996;104:280-8.
10. Thiebaud HP, Knize MG, Kuzmicky PA, Hsieh DP, Felton JS. Airborne mutagens produced by frying beef, pork, and a soy-based food. Food Chem Toxicol 1995;33:821-8.
11. World Cancer Research Fund. Food, nutrition, and the prevention of cancer: A global perspective. American Institute of Cancer Research. Washington, DC: 1997.
12. Felton JS, Knize MG, Salmon CP, Malfatti MA, Kulp KS. Human Exposure to Heterocyclic Amine Food Mutagens/Carcinogens: Relevance to Breast Cancer. Environmental and Molecular Mutagenesis. 2002: 39;112-118.
13. Knize MG, Felton JS. Formation and Human Risk of Carcinogenic Heterocyclic Amines Formed from Natural Precursors in Meat. Nutr Rev. 2005 May;63(5):158-65.
14. World Cancer Research Fund. Food, nutrition, and the prevention of cancer: A global perspective. American Institute of Cancer Research. Washington, DC: 1997.
15. Norat T, Riboli E. Meat consumption and colorectal cancer: a review of epidemiologic evidence. Nutr Rev. 2001 Feb;59(2):37-47
16. Forman, D. Dietary exposure to N-nitroso compounds and the risk of human cancer. Cancer Surv. 1987;6(4):719-38.
17. Willett WC, Stampfer MJ, Colditz GA, Rosner BA, and Speizer FE. Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N Engl J Med. 1990 Dec 13;323(24):1664-72.
18. Nöthlings U, Wilkens LR, Murphy SP, Henderson BE, Kolonel LN. Meat intake increases the risk for pancreatic cancer: The Multiethnic Cohort. Poster presented at: American Association for Cancer Research; April 20, 2005; Anaheim, CA.
19. De Stefani E, Correa P, Boffetta P, Deneo-Pellegrini H, Ronco AL, Mendilaharsu M. Dietary patterns and risk of gastric cancer: a case-control study in Uruguay. Gastric Cancer. 2004;7(4):211-20.
20. Fraser GE. Associations between diet and cancer, ischemic heart disease, and all-cause mortality in non-Hispanic white California Seventh-day Adventists. Am J Clin Nutr 1999;70(suppl):532S-8S.
21. Butler LM, Sinha R, Millikan RC, Martin CF, Newman B, Gammon MD, Ammerman AS, Sandler RS. Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol. 2003;157:434-45.
The Cancer Project is a collaborative effort of physicians, researchers, and nutritionists who have joined together to educate individuals, families, and the public about the benefits of a healthy diet for cancer prevention and survival. Based in Washington, D.C., The Cancer Project is an affiliate of The Physicians Committee for Responsible Medicine.