| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
Epidemiology and Prevention |
Division of Cancer Epidemiology and Genetics [R. S., W. H. C., M. G-C., R. W., R. N. H., N. R.] and Division of Cancer Prevention [M. K.], National Cancer Institute, NIH, Rockville, Maryland 20892, and National Naval Medical Center, Bethesda, Maryland 20889 [J. D., J. B.]
 |
ABSTRACT |
|---|
 Top ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
|
INTRODUCTION |
|---|
|
TopABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
To investigate the role of meat-cooking practices, we designed a meat cooking module within a FFQ.3 Using this module, we attempted to disentangle the role of cooking methods and doneness levels from red meat consumption in a case-control study of colorectal adenomas. We studied adenomas because the majority of colorectal cancers are thought to arise from these benign precursor lesions (17) , and it allows the evaluation of risk factors early in the colorectal neoplastic process among essentially healthy subjects. Furthermore, because changes in life-style factors after adenoma diagnosis are expected to be minimal, reporting of such information by adenoma patients would be less likely to be subject to recall bias than information from cancer patients.
|
MATERIALS AND METHODS |
|---|
|
TopABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
The study was conducted in two phases: (a) at the hospital clinic; and (b) in the subject’s home. The cases were identified from a colonoscopy clinic register, and informed consent was obtained during a return visit after histological confirmation of the adenomas. Some cases had flexible sigmoidoscopy before colonoscopy, whereas other cases had only a colonoscopy. Twice a week, a study staff member was present at a flexible sigmoidoscopy clinic where the controls were consented. Before the home visit, a self-administered FFQ was delivered to the subject’s home. During the home visit, the FFQ was checked for completeness by a trained interviewer. In addition, an in-person interview was conducted to obtain information on meat-cooking practices, demographic background, medication and medical history, physical activity, sun exposures, tobacco and alcohol consumption, and occupational history. The home phase was identical for both cases and controls. Controls were interviewed at a median time of 90 days (10th percentile, 40 days; 90th percentile, 164 days) after sigmoidioscopy, and the cases were interviewed at a median time of 66 days ( 10th percentile, 29 days; 90th percentile, 121 days) after colonoscopy. In addition, subjects provided a blood sample during the clinic visit as well as multiple urine samples during the home visit.
The participation rates were 84% for the cases (244 of the 289 eligible cases identified) and 74% for the controls (231 of 314 eligible controls). The main reason for nonparticipation was subject refusal (12% of cases and 21% of controls), followed by illness (3% of cases and 4% of controls) and other reasons (1% of cases and 1% of controls). Of the 244 participants, 93 were excluded from the current report because of a history of previous adenomas. Two cases and three controls were excluded because of implausible dietary information, leaving 146 cases and 228 controls.
The validated FFQ, a modified version of the 100-item Health Habits and History Questionnaire (18) , was used to obtain information on usual diet (frequency of consumption and portion size) approximately 1 year before sigmoidoscopy/colonoscopy. In addition, we developed a meat cooking module that included 23 meat items and has been validated using 12-day food diaries and a 24-h recall. 4 For meats prepared with variable cooking techniques, we obtained information on the typical level of doneness and cooking method. The five red meat items with doneness information (hamburger/cheeseburger, beef steak, pork chops/ham steaks, sausage/hot dogs, and bacon) are henceforth referred to as the "five red meats." For hamburger and steak, the doneness was determined as rare, medium-rare, medium, medium-well, well done, or very well done. For pork chops/ham steaks, sausage/hot dogs, and bacon, the doneness was defined as just until done, well done/crisp, and very well done/charred. This information was collected in two ways, verbally and by using photographs (19 , 20) . Those red meat items without doneness information are referred to as "other than five red meats." For the seven red meat items (the five red meats plus beef roast and pork roast) with cooking method information, henceforth referred to as the "seven red meats," the methods of cooking were classified as pan-fried, grilled/barbecued, oven-broiled, baked/roasted, or microwaved. Other red meat items, such as luncheon meats, beef stew, meatloaf, and liverwurst, are typically cooked in a standard way not fitting the above classifications. These are referred to as the "other than seven red meats."
We estimated the amount of meat intake (grams/day) from the frequency of consumption and portion size. For the five red meats, we estimated grams of meat consumed according to doneness level and created three different categories: (a) very well done; (b) well done; and (c) medium/rare. To calculate very well done categories, we added grams of very well done steak and hamburger; charred hot dog or sausage, bacon, and breakfast sausage; and very well done pork chops and ham steaks. To calculate the amount of meat in the well done categories, we added grams of well-done steak and hamburger; well-done/crisp hot dog or sausage, bacon, and breakfast sausage; and well-done pork chops and ham steaks. To calculate the medium/rare variable, we added up grams of meats cooked to the rare and medium level of doneness. A variable was also created for each of the cooking techniques (bake/roast, pan fry, grill/barbecue, microwave, oven broil, and other methods), reflecting the daily gram intake of each based on the seven red meats with such information.
ORs and 95% CIs were based on the same number of individuals and calculated using unconditional logistic regression (21) .We present ORs reflecting the relative risk associated with a 10 g/day increase in reported daily consumption of meat. This provides us with the ability to directly compare ORs for the same amount of meat cooked in different manners. It also makes it easier to compare results between studies with different populations, where the amounts consumed might differ. The ORs for meat consumption were modeled using a linear relationship between the amount of reported meat intake and the log odds of disease. The linear relationship was checked by adding a quadratic term to the regression model, which in no case was statistically significant. Moreover, nonparametric logistic regression models using generalized additive models (22) also indicated that a linear model was appropriate for this data. We also present ORs comparing the risk of disease at the 90th versus 10thpercentiles of meat intake, based on the same logistic regression models with continuous data. Tests for trend were calculated using the continuous data. Furthermore, we analyzed the data categorized in quintiles, according to the meat intake distribution in the control population. If more than 20% had zero consumption, all of these were included in the first quintile, reducing the numbers in the second.
All ORs were adjusted for age, gender, total caloric intake, reason for screening (routine or other), physical activity level, pack-years of cigarette smoking, and use of NSAIDs. Additional adjustment for consumption of total fat, saturated fat, fruits, vegetables, fiber, or alcohol or for education, race, body mass index, bowel frequency, and family history of colorectal cancer did not substantially alter the findings.
To check for potential selection bias, we examined the risks for various subsets of the subjects, excluding cases with adenomas only in the right colon, cases with only rectal adenomas, and subjects who came to the clinic because of positive occult blood or visible blood in the feces.
|
RESULTS |
|---|
|
TopABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
. Some notable case/control differences were a higher smoking history and lower percentage of NSAID use among cases compared with controls. There were no major differences in caloric intake or physical activity. A higher proportion of cases (26%) compared to controls (10%) were referred to the clinic because of gastrointestinal symptoms, such as blood in stool, occult blood, or diarrhea.
|
We found a nonsignificant increased risk of colorectal adenomas of 4% per 10 g/day increase in total meat intake (OR, 1.04; CI, 0.98–1.09), as shown in Fig. 1
. This increased risk of 4% per 10 g/day partitioned into a significant 11% per 10 g/day (OR, 1.11; CI, 1.03–1.19) risk increase for consumption of red meat and a nonsignificant decrease in risk of 5% per 10 g/day (OR, 0.95; CI, 0.87–1.03) for white meat intake. The test for trend for the red meat was significant (P = 0.005). The difference in risk between the red meat and white meat consumption was significant (P = 0.01). Similar results were observed in categorical analyses when we compared the lowest quintile to the 2nd, 3rd, 4th, and 5th quintiles; the ORs for red meat were 0.97 (CI, 0.43–2.20), 1.57 (CI, 0.72–3.41), 1.73 (CI, 0.78–3.82), and 2.28 (CI, 1.01–5.16), respectively.
|
. We further partitioned the five red meats by doneness level and found that the risk increased by 29% per 10 g/day (OR, 1.29; CI, 1.08–1.54) for red meat cooked well done/very well done in contrast to 10% per 10 g/day (OR, 1.10; CI, 0.96–1.26) for red meat cooked rare/medium. The test for trend for well done/very well done was significant (P = 0.005). The difference in risk between the well-done/very well-done red meat and rare/medium red meat was nonsignificant (P = 0.1). Compared with the lowest quintile, the ORs for well-done/very well-done red meat were 0.82 (CI, 0.35–1.94), 1.07 (CI, 0.53–2.16), 1.18 (CI, 0.60–2.34), and 1.67 (CI, 0.85–3.27) for the 2nd, 3rd, 4th, and 5th quintiles, respectively. The results were essentially similar from the analyses when the doneness levels were calculated from the photographs. When we subdivided the well done/very well done category, we observed an increased risk of 111% per 10 g/day (OR, 2.11; CI, 0.90–4.93) for red meat cooked very well done and 21% per 10 g/day (OR, 1.21; CI, 0.99– 1.48) for well-done red meat.
Red meat was also partitioned according to cooking technique. Intake of grilled/barbecued red meat was associated with a significant 26% increase in risk per 10 g/day (OR, 1.26; CI, 1.06–1.50). The test for trend for grilled/barbecued meat was significant (P = 0.008). The difference in risk between grilled/barbecued meat and other methods of cooking meat was suggestive (P = 0.08). Compared with the lowest quintile, the ORs for grilled/barbecued red meat were 0.36 (CI, 0.07–1.83), 0.84 (CI, 0.42–1.66), 1.31 (CI, 0.70–2.48), and 1.87 (CI, 1.01–3.47) for the 2nd, 3rd, 4th, and 5th quintiles, respectively.
The risk was further elevated to 85% per 10 g/day (OR, 1.85; CI, 1.24–2.75) among subjects who ate their grilled meat cooked well done/very well done (Fig. 2)
.
|
When we analyzed subgroups to check for potential bias due to recruitment strategy, the results were essentially unchanged. After excluding cases with only right-sided adenomas, the ORs for total red meat, well-done red meat, and grilled red meat were 1.09 (CI, 1.00–1.22), 1.29 (CI, 1.08–1.55), and 1.24 (CI, 1.03–1.48) respectively. The corresponding ORs after excluding subjects with rectal adenomas were 1.10 (CI, 1.00–1.12), 1.28 (CI, 1.06–1.54), and 1.22 (CI, 1.02–1.47), respectively; and the ORs were 1.11 (CI, 1.00– 1.22), 1.34 (CI, 1.12–1.61), and 1.29 (CI, 1.08–1.54) after excluding subjects with positive occult blood or visible blood in the feces.
To evaluate the risk of colorectal adenomas and the amount of red meat consumed in this population, we also present the ORs based on the 90th versus the 10th percentile consumed among controls. These ORs were 1.69 (CI, 1.17–2.44) for well-done/very well-done red meat and 1.84 (CI, 1.67–2.91) for grilled/barbecued red meat. They are essentially identical to the estimated ORs for the 5th to the 1st quintiles obtained from a categorical model.
|
DISCUSSION |
|---|
|
TopABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
This study has several strengths. In this study, we have collected detailed information on cooking practices and doneness levels for specific types of commonly consumed meats. This is necessary to obtain accurate estimates of total intake by doneness and cooking method. It also allowed us to analyze risk by subtypes of meat cooked to different levels of doneness with various cooking techniques.
Another strength of this study is that cases had adenomas rather than cancer. As a consequence, their current dietary habits were less likely to have changed after diagnosis, and their responses to questions about usual dietary habits were less likely to be influenced by their treatment. In addition, the study had relatively high participation rates for a biologically intensive study with both a clinic and a home phase component. Finally, both cases and controls were recruited from a well-defined base of individuals, who were on active duty, retired from the uniformed services, or military dependents.
This study also has several limitations. We interviewed subjects after their diagnostic and treatment procedures were completed, so there is a potential for recall bias. However, as noted above, this is likely to be less of a problem when studying precancerous adenomas, which are completely removed by treatment, as compared to cancer. In addition, because the well-done meat intake hypothesis was not well established, patients were not advised by health care professionals at any stage of examination and treatment to reduce their intake of red meat or to modify its preparation.
Cases had a full colonoscopy, whereas the controls had only a flexible sigmoidoscopy; thus, some controls might have had undetected adenomas in the right-side colon. If risk factors for right-sided adenomas are similar to risk factors for left-sided adenomas, undetected adenomas among the controls would tend to attenuate our results. However, when the analysis was restricted to cases with left-sided colon adenomas, which are easily detectable by sigmoidoscopy, the results were essentially unchanged.
The associations between colorectal tumors and doneness and cooking methods are not consistent in previous studies (9 , 11 , 12 , 14 , 16 , 23) . One reason for the discrepancy may be that different cooking methods have generally been combined together within a question, leading to a dilution of the effect of specific cooking techniques. For example, pan-frying and deep-fat frying produce very different levels of heat on the surface of meat. Similarly, oven broiling, grilling, and pan frying cook meats differently. In the case of oven broiling, the fat and moisture drip out of the meat; in grilling, it falls onto a heated surface producing flames and higher temperatures; and in pan frying, the meat is cooked in the fat. In this study, we obtained details on both cooking methods and doneness level for each meat item rather than for all red meats lumped together as one item because it is reasonable to assume that people eat meats cooked to different levels and doneness depending on the type of meat. For example, a person may eat hamburger patty pan-fried and well-done, steak grilled/barbecued and medium, and bacon oven-broiled and very well done. Assuming that all red meats are cooked by the same technique to the same level of doneness loses much of the relevant information required to examine the hypothesis.
The two main factors that influence the production of pyrolysis products in cooked meats are time and temperature (24 , 25) . Epidemiologists have tried to identify surrogates for these two factors. Doneness of meat or external browning may be a reasonable surrogate for cooking time and temperature. Well-done meat has been associated with increased risk of colon, breast, lung, and stomach cancers (11, 12, 13 , 15 , 16 , 26) . We are now reporting a possible association between well-done red meat and colorectal adenomas with an increased risk of about 29% per 10 g/day (or 2.5 oz/week) of well-done/very well-done red meat consumed. Using cooking method as a surrogate for temperature, we found an increased risk of colorectal adenomas associated with grilled/barbecued red meat. There was an increased risk of approximately 26% for every 10 g/day increase in consumption of grilled/barbecued red meat.
In conclusion, we found evidence of increased colorectal adenoma risk with consumption of certain but not all red meats. We found that the excess risk was mostly confined to intake of well-done/very well-done red meat and meats cooked at high temperature such as grilled and possibly fried red meat. These results are consistent with cooking practices that produce carcinogens such as heterocyclic amines and polycyclic aromatic hydrocarbons.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
1 The opinions and assertions contained herein are the sole views of the authors and should not be construed as official or affecting the views of the Department of the Navy, Department of Defence, or the U. S. Government. The Chief, Navy Bureau of Medicine and Surgery, Washington, D. C., Clinical Investigations Program sponsored this study (B93-004). 
2 To whom requests for reprints should be addressed, at Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Executive Plaza South, Room 7028, 6120 Executive Boulevard, Rockville, MD 20852.
3 The abbreviations used are: FFQ, food frequency questionnaire; OR, odds ratio; CI, confidence interval; NSAID, nonsteroidal anti-inflammatory drugs.
Received 2/17/99. Accepted 7/ 2/99.
|
REFERENCES |
|---|
|
TopABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
This article has been cited by other articles:
|
|
 |
|
  M. Ryan-Harshman and W. Aldoori Diet and colorectal cancer: Review of the evidence Can Fam Physician, November 1, 2007; 53(11): 1913 - 1920. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. E. Martinez, E. T. Jacobs, E. L. Ashbeck, R. Sinha, P. Lance, D. S. Alberts, and P. A. Thompson Meat intake, preparation methods, mutagens and colorectal adenoma recurrence Carcinogenesis, September 1, 2007; 28(9): 2019 - 2027. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Gunter, R. L. Divi, M. Kulldorff, R. Vermeulen, K. J. Haverkos, M. M. Kuo, P. Strickland, M. C. Poirier, N. Rothman, and R. Sinha Leukocyte polycyclic aromatic hydrocarbon-DNA adduct formation and colorectal adenoma Carcinogenesis, July 1, 2007; 28(7): 1426 - 1429. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. H. Ward, A. J. Cross, H. Divan, M. Kulldorff, S. Nowell-Kadlubar, F. F. Kadlubar, and R. Sinha Processed meat intake, CYP2A6 activity and risk of colorectal adenoma Carcinogenesis, June 1, 2007; 28(6): 1210 - 1216. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Tang, J. J. Liu, A. Rundle, C. Neslund-Dudas, A. T. Savera, C. H. Bock, N. L. Nock, J. J. Yang, and B. A. Rybicki Grilled Meat Consumption and PhIP-DNA Adducts in Prostate Carcinogenesis Cancer Epidemiol. Biomarkers Prev., April 1, 2007; 16(4): 803 - 808. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. I. Berndt, E. A. Platz, M. D. Fallin, L. W. Thuita, S. C. Hoffman, and K. J. Helzlsouer Genetic Variation in the Nucleotide Excision Repair Pathway and Colorectal Cancer Risk. Cancer Epidemiol. Biomarkers Prev., November 1, 2006; 15(11): 2263 - 2269. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. J. Gunter, F. Canzian, S. Landi, S. J. Chanock, R. Sinha, and N. Rothman Inflammation-related gene polymorphisms and colorectal adenoma. Cancer Epidemiol. Biomarkers Prev., June 1, 2006; 15(6): 1126 - 1131. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Sinha, U. Peters, A. J. Cross, M. Kulldorff, J. L. Weissfeld, P. F. Pinsky, N. Rothman, R. B. Hayes, and Prostate, Lung, Colorectal, and Ovarian Cancer Pro Meat, Meat Cooking Methods and Preservation, and Risk for Colorectal Adenoma Cancer Res., September 1, 2005; 65(17): 8034 - 8041. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Sinha, M. Kulldorff, M. J. Gunter, P. Strickland, and N. Rothman Dietary Benzo[a]Pyrene Intake and Risk of Colorectal Adenoma Cancer Epidemiol. Biomarkers Prev., August 1, 2005; 14(8): 2030 - 2034. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. E. Moore, W.-Y. Huang, N. Chatterjee, M. Gunter, S. Chanock, M. Yeager, B. Welch, P. Pinsky, J. Weissfeld, and R. B. Hayes GSTM1, GSTT1, and GSTP1 Polymorphisms and Risk of Advanced Colorectal Adenoma Cancer Epidemiol. Biomarkers Prev., July 1, 2005; 14(7): 1823 - 1827. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. T. Chan, J. Ma, G. J. Tranah, E. L. Giovannucci, N. Rifai, D. J. Hunter, and C. S. Fuchs Hemochromatosis Gene Mutations, Body Iron Stores, Dietary Iron, and Risk of Colorectal Adenoma in Women J Natl Cancer Inst, June 15, 2005; 97(12): 917 - 926. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Robien, K. Curtin, C. M. Ulrich, J. Bigler, W. Samowitz, B. Caan, J. D. Potter, and M. L. Slattery Microsomal Epoxide Hydrolase Polymorphisms Are Not Associated with Colon Cancer Risk Cancer Epidemiol. Biomarkers Prev., May 1, 2005; 14(5): 1350 - 1352. [Full Text] [PDF]
|
|
|
|
|
|
M. J. Gunter, N. M. Probst-Hensch, V. K. Cortessis, M. Kulldorff, R. W. Haile, and R. Sinha Meat intake, cooking-related mutagens and risk of colorectal adenoma in a sigmoidoscopy-based case-control study Carcinogenesis, March 1, 2005; 26(3): 637 - 642. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Chao, M. J. Thun, C. J. Connell, M. L. McCullough, E. J. Jacobs, W. D. Flanders, C. Rodriguez, R. Sinha, and E. E. Calle Meat Consumption and Risk of Colorectal Cancer JAMA, January 12, 2005; 293(2): 172 - 182. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. W. Stewart and A. S. Coates Cancer Prevention: A Global Perspective J. Clin. Oncol., January 10, 2005; 23(2): 392 - 403. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Lin, S. M. Zhang, N. R. Cook, I-M. Lee, and J. E. Buring Dietary Fat and Fatty Acids and Risk of Colorectal Cancer in Women Am. J. Epidemiol., November 15, 2004; 160(10): 1011 - 1022. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Kikugawa Prevention of mutagen formation in heated meats and model systems Mutagenesis, November 1, 2004; 19(6): 431 - 439. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Cantwell, B. Mittl, J. Curtin, R. Carroll, N. Potischman, N. Caporaso, and R. Sinha Relative Validity of a Food Frequency Questionnaire with a Meat-Cooking and Heterocyclic Amine Module Cancer Epidemiol. Biomarkers Prev., February 1, 2004; 13(2): 293 - 298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Peters, D. M. DeMarini, R. Sinha, L. R. Brooks, S. H. Warren, N. Chatterjee, and N. Rothman Urinary Mutagenicity and Colorectal Adenoma Risk Cancer Epidemiol. Biomarkers Prev., November 1, 2003; 12(11): 1253 - 1256. [Abstract] [Full Text]
|
|
|
|
|
|
A. Flood, E. M. Velie, R. Sinha, N. Chaterjee, J. V. Lacey Jr., C. Schairer, and A. Schatzkin Meat, Fat, and Their Subtypes as Risk Factors for Colorectal Cancer in a Prospective Cohort of Women Am. J. Epidemiol., July 1, 2003; 158(1): 59 - 68. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. C-H. Chiu, B.-T. Ji, Q. Dai, G. Gridley, J. K. McLaughlin, Y.-T. Gao, J. F. Fraumeni Jr., and W.-H. Chow Dietary Factors and Risk of Colon Cancer in Shanghai, China Cancer Epidemiol. Biomarkers Prev., March 1, 2003; 12(3): 201 - 208. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. M. Butler, R. Sinha, R. C. Millikan, C. F. Martin, B. Newman, M. D. Gammon, A. S. Ammerman, and R. S. Sandler Heterocyclic Amines, Meat Intake, and Association with Colon Cancer in a Population-based Study Am. J. Epidemiol., March 1, 2003; 157(5): 434 - 445. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. L. Divi, F. A. Beland, P. P. Fu, L. S. Von Tungeln, B. Schoket, J. E. Camara, M. Ghei, N. Rothman, R. Sinha, and M. C. Poirier Highly sensitive chemiluminescence immunoassay for benzo[a]pyrene-DNA adducts: validation by comparison with other methods, and use in human biomonitoring Carcinogenesis, December 1, 2002; 23(12): 2043 - 2049. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Brennan Gene-environment interaction and aetiology of cancer: what does it mean and how can we measure it? Carcinogenesis, March 1, 2002; 23(3): 381 - 387. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Le Marchand, J. H. Hankin, L. R. Wilkens, L. M. Pierce, A. Franke, L. N. Kolonel, A. Seifried, L. J. Custer, W. Chang, A. Lum-Jones, et al. Combined Effects of Well-done Red Meat, Smoking, and Rapid N-Acetyltransferase 2 and CYP1A2 Phenotypes in Increasing Colorectal Cancer Risk Cancer Epidemiol. Biomarkers Prev., December 1, 2001; 10(12): 1259 - 1266. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
U. Peters, K. A. McGlynn, N. Chatterjee, E. Gunter, M. Garcia-Closas, N. Rothman, and R. Sinha Vitamin D, Calcium, and Vitamin D Receptor Polymorphism in Colorectal Adenomas Cancer Epidemiol. Biomarkers Prev., December 1, 2001; 10(12): 1267 - 1274. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. H. Wu, D. Shibata, M. C. Yu, M.-Y. Lai, and R. K. Ross Dietary heterocyclic amines and microsatellite instability in colon adenocarcinomas Carcinogenesis, October 1, 2001; 22(10): 1681 - 1684. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Ulrich, J. Bigler, J. A. Whitton, R. Bostick, L. Fosdick, and J. D. Potter Epoxide Hydrolase Tyr113His Polymorphism Is Associated with Elevated Risk of Colorectal Polyps in the Presence of Smoking and High Meat Intake Cancer Epidemiol. Biomarkers Prev., August 1, 2001; 10(8): 875 - 882. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Andreassen, R. Vikse, I.-L. Steffensen, J. E. Paulsen, and J. Alexander Intestinal tumours induced by the food carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in multiple intestinal neoplasia mice have truncation mutations as well as loss of the wild-type Apc+ allele Mutagenesis, July 1, 2001; 16(4): 309 - 315. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Sinha, M. Kulldorff, W.-H. Chow, J. Denobile, and N. Rothman Dietary Intake of Heterocyclic Amines, Meat-derived Mutagenic Activity, and Risk of Colorectal Adenomas Cancer Epidemiol. Biomarkers Prev., May 1, 2001; 10(5): 559 - 562. [Abstract] [Full Text]
|
|
|
|
 |
|
 A. J. Fretland, U. S. Devanaboyina, Y. Feng, M. A. Leff, G. H. Xiao, S. J. Webb, and D. W. Hein Oral Administration of 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) Yields PhIP-DNA Adducts but Not Tumors in Male Syrian Hamsters Congenic at the N-acetyltransferase 2 (NAT2) Locus Toxicol. Sci., February 1, 2001; 59(2): 226 - 230. [Abstract] [Full Text] [PDF]
|
|
