Research Section
Analysis of 200 food items for benzo[a]pyrene and estimation of its intake in an epidemiologic study

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Abstract

Animal studies have shown that dietary intake of benzo[a]pyrene (BaP), a polycyclic aromatic hydrocarbon (PAH), causes increased levels of tumors at several sites, particularly in the upper gastrointestinal tract. However, the role of dietary intake of BaP and cancer in humans is not clear. We created a BaP database of selected food products that could be linked to Food Frequency Questionnaires (FFQs) to estimate BaP intake. BaP levels were measured for each food line-item (composite samples) which consisted of a variety of foods in a FFQ. Composite sample parts were derived from the Second National Health and Nutrition Examination Survey (NHANES II) which represents the most common food items consumed by the general population. Meat samples were cooked by different techniques in controlled conditions, and by various restaurants and fast-food chains. Non-meat products were purchased from the major national supermarket chains. The quantities of BaP were measured using a thin-layer chromatography (TLC)/spectrofluorometer technique and were highly correlated with both BaP (radius=0.99) and sum of carcinogenic PAH (r=0.98) measured by HPLC technique. We linked our database to the results from a FFQ and estimated the daily BaP intake of various food items in 228 subjects in the Washington, DC metropolitan area. The highest levels of BaP (up to about 4 ng BaP/g of cooked meat) were found in grilled/barbecued very well done steaks and hamburgers and in grilled/barbecued well done chicken with skin. BaP concentrations were lower in meats that were grilled/barbecued to medium done and in all broiled or pan-fried meat samples regardless of doneness level. The BaP levels in non-meat items were generally low. However, certain cereals and greens (e.g. kale, collard greens) had levels up to 0.5 ng/g. In our population, the bread/cereal/grain, and grilled/barbecued meat, respectively, contributed 29 and 21 percent to the mean daily intake of BaP. This database may be helpful in initial attempts to assess dietary BaP exposures in studies of cancer etiology.

Introduction

Benzo[a]pyrene (BaP), a member of the polycyclic aromatic hydrocarbon (PAH) class, is one of the most potent PAH carcinogens in animal experiments (Howard and Fazio, 1980) and is embryotoxic and teratogenic in mice (IARC, 1983). Leukemia, gastric tumor and pulmonary adenoma or tumor developed in the strain of white Swiss mice that were fed BaP (Rigdon and Neal, 1966, Rigdon and Neal, 1969, Neal and Rigdon, 1967, Rigdon, Neal and Mack, 1967). A study by Weyand et al. (1995) showed an association between the ingestion of a diet containing BaP and forestomach tumors in A/J strain of mice. A more recent study by Culp et al. (1998) examined the histopathological sections of other sites such as small intestine, tongue and esophagus in female B6C3F1 mice. This study showed that BaP treatment in a 2-year feeding study resulted in an increased incidence of papillomas and/or carcinoma of forestomach, esophagus and tongue. Although the mechanism of BaP carcinogenicity in humans is not clear, a study by Autrup et al. (1982) investigated the BaP metabolism in cultured normal human bronchus, colon, duodenum and esophagus from the same patient. In that study, the highest total metabolism was found in bronchus and duodenum. The descending order for the ‘BaP mean binding levels’ was observed in bronchus, esophagus, duodenum and transverse colon. Because of species differences in carcinogenesis by BaP with respect to the site and type of tumor formation (Weyand and Bevan, 1987), BaP carcinogenicity in humans remains unclear.

BaP concentration is a good marker of carcinogenic PAH levels in environmental samples (Bjorseth, 1983, Buutler et al., 1993). BaP is the most known and studied member of the PAH because it is one of the most potent PAH animal carcinogens (Howard and Fazio, 1980), and it is relatively easy to separate and analyze by longer wavelength fluorescence. BaP is present in a wide variety of food items (IARC, 1983). The Total Human Exposure to Environmental Substances (THEES) study had shown that people in the general population without substantial exposure to pollution and occupational exposure had a higher exposure to carcinogenic BaP by food ingestion than by inhalation (Butler et al., 1993).

PAH are found in grilled/barbecued meat, vegetables, oils, grains/cereals, fruits, smoked fish and seafood in concentrations as low as 0.001 ng/ per g (200 ppb) (Lijinsky and Ross, 1967, Lo and Sandi, 1978, Lintas et al., 1979, Howard and Fazio, 1980, Santodonato, Howard and Basu, 1981, Dennis et al., 1983, IARC, 1983, Larsson, 1986, Vaessen, Jekel and Wilbers, 1988, de Vos et al., 1990, Greenberg et al., 1990). As there is no comprehensive PAH database, epidemiologic studies have not been able to estimate dietary PAH intake and investigate the risk of cancer associated with it. However, investigators have evaluated the relationship between the intake of several foods that may have high level of PAH (e.g. smoked or grilled/barbecued meats) and risk for cancer at several sites including stomach and esophagus (Soos, 1980, Ward et al., 1997), colorectal (Peters et al., 1989, O'Neill et al., 1990a, O'Neill et al., 1990b, Schiffman and Felton, 1990, Gerhardsson de Verdier et al., 1991, Lang et al., 1994, Muscat and Wynder, 1994, Sinha et al., 1999), pancreatic (Norell et al., 1986) and bladder cancer (Steineck et al., 1990). Because PAH are contained in wide variety of foods, it is necessary to directly estimate the dietary intake of BaP from all dietary sources to evaluate the relationship between dietary intake of BaP and risk of cancer.

Although there are extensive data on PAH in food, the data have not been collected in a way that could be incorporated in dietary questionnaires. Previous studies have looked at cooking methods in measuring BaP content in meats and poultry, but have not provided detailed BaP levels in meat cooked by a number of techniques and varying levels of doneness. In addition, previous studies have not reported BaP and/or total PAH concentrations in food in a way that could be linked to dietary questionnaires used in epidemiologic studies (Dennis et al., 1983, Vaessen, Jekel and Wilbers, 1988, de Vos et al., 1990, Lodovici et al., 1995). The objectives of our study were to: (1) create a database of food items with BaP concentrations that could be linked to FFQs that have been used in epidemiologic studies; and (2) determine BaP intake using a FFQ in a disease-free population.

Section snippets

Selection of food items

The first objective of our study was to create a database of food items with BaP concentrations that could be linked to a FFQ. We used a modified version of the Health Habits and History Questionnaire (HHHQ), a FFQ developed by the National Cancer Institute IMS Inc. and Block Dietary Data Systems (1994) to determine a variety of food items for which we could measure BaP concentrations. Each food line-item of this FFQ was a composite sample, for example, mixed greens: two parts mustard, one part

Results

The BaP concentrations of the various food items are shown in Table 1, Table 2, Table 3, Table 4, Table 5, Table 6, Table 7, Table 8 as ng/g as well as the amount in a “medium” portion size. Items with the highest concentration of BaP were very well done grilled/barbecued steak, well done grilled/barbecued chicken with skin, very well done grilled/barbecued hamburger, collard greens and kale, pumpkin pie, pretzels, bran and granola cereal, cooked cereal, margarine and french fries. The

Discussion

Our data showed that grilled/barbecued steak, well done grilled/barbecued chicken with skin, and very well done grilled/barbecued hamburger had the highest concentrations of BaP, but the BaP content in grilled/barbecued steak samples were much higher than grilled/barbecued hamburger samples. Grilled/barbecued meat contributed 21% to the total mean daily BaP intake in our subjects. Although the bread/cereal/grain food group contributed 29% to the total BaP intake in the subjects, the individual

Acknowledgements

We thank Christine Swanson and Joanne Holden for their help in defining the sampling method and identifying the surveys that were used in this study. We also thank William Blot for helping us to obtain funding for this project. Additionally, we thank Jane Curtin of IMS Inc., Rockville, MD, for her computer support.

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    The opinions or assertions contained herein are the private ones of the author and are not to be construed as official or reflecting the views of the United States Department of Defense or the Uniformed Services University of the Health Sciences.

    1

    Current address: Department of Hospital and Health Care Administration, Chung-Tai Institute of Health Sciences and Technology, 11, Po-tze Lane, Takun, Taichung, 40605, Taiwan, ROC.

    2

    Current address: Department of Chemistry, University of New Hampshire, Durham, NH 03824, USA.

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