© 1999 by Oxford University Press
Journal of the National Cancer Institute, Vol. 91, No. 6, 542-547,
March 17, 1999
© 1999 Oxford University Press
REPORTS |
Prospective Study of Adult Onset Diabetes Mellitus (Type 2) and Risk of Colorectal Cancer in Women
Affiliations of authors: F. B. Hu, Department of Nutrition, Harvard School of Public Health, Boston, MA; J. E. Manson, Department of Epidemiology, Harvard School of Public Health, and Channing Laboratory and Division of Preventive Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston; S. Liu, Departments of Nutrition and Epidemiology, Harvard School of Public Health; D. Hunter, G. A. Colditz, K. B. Michels, Department of Epidemiology, Harvard School of Public Health, and Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School; F. E. Speizer, Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School; E. Giovannucci, Department of Nutrition, Harvard School of Public Health, and Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School.
Correspondence to: Frank B. Hu, M.D., Department of Nutrition, Harvard School of Public Health, 665 Huntington Ave., Boston, MA 02115 (e-mail: frank.hu{at}channing.harvard.edu).
 |
ABSTRACT |
|---|
 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
BACKGROUND: The remarkable similarity of lifestyle and environmental risk factors for type 2 (non-insulin-dependent) diabetes mellitus and colon cancer has led to the hypothesis that diabetes may increase the risk of this cancer. We prospectively examined the relationship between diabetes and risk of colorectal cancer in a cohort of 118 403 women aged 30 through 55 years who were without previously diagnosed cancer at baseline in 1976. METHODS: The women, who were enrolled in the Nurses' Health Study, were assessed for history of diabetes at baseline and during follow-up by use of biennial questionnaires. Self-reported diabetes was validated by information obtained from a supplemental questionnaire on symptoms and treatment and was confirmed by medical record review in a sample of the participants. Incident cases of colorectal cancer were ascertained through medical record review. All reported P values are two-sided. RESULTS: During 18 years of follow-up (2 001 061 person-years), we documented 892 new cases of colorectal cancer. After adjustment for age, body mass index (weight in kg/height in m2), physical activity, and other covariates, relative risks (RRs) were 1.43 (95% confidence interval [CI] = 1.10-1.87; P = .009) for colorectal cancer, 1.49 (95% CI = 1.09-2.06; P = .01) for colon cancer, 1.11 (95% CI = 0.56-2.21; P = .76) for rectal cancer, 1.56 (95% CI = 1.07-2.28; P = .02) for advanced colorectal cancer, and 2.39 (95% CI = 1.46-3.92; P = .0005) for fatal colorectal cancer. CONCLUSION: Our data provide support for the hypothesis that diabetes is associated with an increased risk of colorectal cancer in women.
|
INTRODUCTION |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
The remarkable similarity of lifestyle and environmental risk factors for type 2 (non-insulin-dependent) diabetes mellitus and colon cancer, such as high body mass index, increased central obesity, physical inactivity, and higher intake of refined carbohydrates, has led to the hypothesis that type 2 diabetes itself is a risk factor for colon cancer (1). This hypothesis is spawned from a more general hypothesis that hyperinsulinemia (excessively high blood insulin levels) increases the risk of colon cancer by directly promoting colon carcinogenesis and stimulating insulin-like growth factor-I (IGF-I) receptors (1,2). The expected relationship between type 2 diabetes and colon cancer based on the insulin-colon cancer hypothesis, however, is complex because hyperinsulinemia exists at an early stage of insulin resistance but, as glucose intolerance worsens, intensified hyperglycemia and depletion of ß cells may lead to a hypoinsulinemic response. Thus, it is important to consider both the duration and severity of diabetes when examining the relationship of type 2 diabetes with colon cancer.
Epidemiologic data on the association between diabetes and risk of colon cancer are sparse and inconclusive. When compared with the age-standardized cancer rates in the general populations, diabetics appear to have slightly elevated rates of colorectal cancer (3-5). However, these results are difficult to interpret because individuals in the cohorts may differ in many aspects (especially body mass index) from external comparison populations. A positive association between history of diabetes and colorectal cancer has been reported in several case-control studies (6-9), but not in all (10). Also, the positive association tended to be stronger for men than for women (6,7,10). However, the small number of colon cancer cases among diabetics (6-10), potential recall bias (6,7,10), lack of control for important confounders such as obesity and physical activity (7,10), and failure to consider the type or duration of diabetes (6,7,10) have hampered the interpretation of the findings. Recently, a prospective study (11) with 13 years of follow-up found a significant positive association between diabetes and incidence of colorectal cancer in men (relative risk [RR] = 1.30; 95% confidence interval [CI] = 1.03-1.65) and a weaker nonsignificant positive association in women (RR = 1.16; 95% CI = 0.87-1.53). However, diabetes was not associated with an increased risk of fatal colon cancer. This finding raises the question of detection or diagnostic bias because earlier and less aggressive cancers are typically more prone to heightened detection and surveillance that may occur among individuals with diabetes.
The present study, with 18 years of follow-up, examines the relationship of diabetes with the incidence of colorectal cancers among women enrolled in the Nurses' Health Study. We specifically examine this relationship by years since the diagnosis of diabetes because insulin levels may differ depending on earlier or later stage of type 2 diabetes.
|
SUBJECTS AND METHODS |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
Subjects
The Nurses' Health Study cohort was established in 1976 when 121 700 female registered nurses 30-55 years of age completed a mailed questionnaire on their medical histories and lifestyles. Every 2 years, follow-up questionnaires are sent to obtain updated information on risk factors and to identify newly diagnosed diseases. The validity of the biennial questionnaire on medical history and lifestyle factors has been described in detail previously (12). Beginning in 1980, validated food-frequency questionnaires have been used to assess dietary intakes at 2- to 4-year cycles (13). The participants in the present study included women who were free of diagnosed cancer at baseline in 1976 (n = 118 403). This study was approved by the Human Research Committee at the Brigham and Women's Hospital.
Assessment of Diabetes Mellitus
On the baseline and subsequent biennial questionnaires, we asked the participants if and when they had ever been diagnosed with diabetes (either insulin-dependent or non-insulin-dependent). At baseline, 2095 women reported a previous diagnosis of diabetes. During follow-up (1976-1992), an additional 5305 women reported a diagnosis. We excluded women who had diabetes before age 30 years because they were most likely to have type 1 diabetes (n = 331).
Self-reported diabetes was validated by a supplementary questionnaire regarding symptoms, diagnostic tests, and treatment of diabetes and confirmed by medical record review in a sample (14). We obtained medical records in a random sample of 84 participants who reported a diagnosis of diabetes. Of the 84 women, 71 provided permission for medical record review; medical records could be obtained for 62. An endocrinologist who was blinded to the information reported on the supplementary questionnaire reviewed the available records using the National Diabetes Data Group Criteria (15). The diagnosis of type 2 diabetes was confirmed by medical record review in 61 (98.4%) of the 62 women (14).
Identification of Cases of Colorectal Cancer
We identified cases of colorectal cancer through biennial questionnaires and medical record review (16). On each follow-up questionnaire, we asked whether cancer of the colon or rectum has been diagnosed during the previous 2 years. In addition to reports from next of kin, we also used the National Death Index and the U.S. Postal Service to identify fatalities; we estimate that more than 98% of deaths were ascertained (17). When a participant (or the next of kin for decedents) reported a diagnosis of cancer of the colon or rectum on our follow-up questionnaire, we asked her (or the next of kin) for permission to obtain hospital records and pathology reports pertaining to this diagnosis. A study physician blinded to the exposure information reviewed the medical records to extract information on the histologic type, the anatomic location, and the stage of the cancer. Proximal colon cancers were defined as those from the cecum to and including the splenic flexure, and distal colon cancers were defined as those in the descending and sigmoid colon. Advanced cancers were defined as those with evidence of metastasis (to regional lymph nodes or to distant organs) at diagnosis. Fatal cancers were defined as those diagnosed since 1976 but fatal by the end of the follow-up (June 1, 1994).
Statistical Analysis
Person-time for each participant was calculated from the date of return of the 1976
questionnaire to the date of colorectal cancer diagnosis, death from any cause, or June 1, 1994,
whichever came first. Diagnosis of diabetes was reported at baseline and updated every 2 years.
For incident diabetic cases (diabetes occurring during follow-up), diabetic person-years were
calculated from the diagnosis of the diabetes. For prevalent diabetic cases (diabetes at baseline),
diabetic person-years were calculated from the beginning of the study (1976). Women who
reported cancer on previous questionnaires were excluded from subsequent analyses. We
calculated incidence rates of colorectal cancer for women diagnosed with diabetes by dividing
the number of incident cases by the number of person-years of follow-up. The RR was computed
as the rate among women with diabetes divided by the rate among nondiabetics, with adjustment
for 5-year age categories. Years since diagnosis of diabetes was determined by questionnaire at
baseline and updated every 2 years. We classified years since diagnosis into four categories based
on the frequency distribution (no diabetes, 
10 years, 11-15 years, and >15 years).
We used pooled logistic regression across the nine 2-year intervals (June 1976-June 1978 and
similar time periods in the following years: 1978-1980, 1980-1982, 1982-1984, 1984-1986,
1986-1988, 1988-1990, 1990-1992, and 1992-1994) (18), which is
asymptotically equivalent to time-varying Cox regression, to adjust simultaneously for potential
confounding variables, including age (age groups: <49, 50-54, 55-59, 60-64, 
65 years
old); body mass index (10 categories); and menopausal status (premenopausal, postmenopausal
without hormone replacement, postmenopausal with past hormone replacement, and
postmenopausal with current hormone replacement). These variables were first assessed in 1976
and updated every 2 years. We also adjusted for multivitamin use (yes or no); alcohol
consumption (0, >0-4, 5-14, or 15 g/day); aspirin use (yes or no); and average hours per
week of moderate or vigorous activity (<1, 1-1.9, 2-3.9, 4-6.9, or 7). These variables
were first assessed in 1980 and updated every 2 to 4 years. We also adjusted for intake of red
meat (including beef as a main dish, beef in a sandwich or mixed dish, hamburger, hot dog,
processed meat, and bacon), which was assessed in 1980, 1984, 1986, and 1990. To best
represent long-term diet and reduce measurement error, we adjusted for cumulative averages of
red meat intake in the pooled logistic model (19). For example, 1980
meat intake was related to incident colorectal cancer from 1980 through 1984 and the average of
1980 and 1984 intakes was related to incident cases from 1984 through 1986. For variables that
were initially assessed in 1980, we replaced missing values in 1976 with the values from 1980. In
addition, we controlled for pack-years of smoking before age 30 because it was more predictive
of colon cancer than was current or lifetime smoking (20). We also
controlled for parental history of colorectal cancer. All reported P values were derived
from the two-sided Wald test.
|
RESULTS |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
During 18 years of follow-up (2 001 061 person-years), we documented 892 new cases of colorectal cancer, including 607 colon cancers and 176 rectal cancers (subsite information was unavailable for 109 cases). Of these cancers, 414 were defined as advanced colorectal cancers (metastasis at diagnosis or fatal by June 1994), and 177 were fatal colorectal cancers by June 1994.
Table 1
shows baseline characteristics for all self-reported diabetics
(n = 7069) and nondiabetics (n = 111,003) up to 1992. Smoking rate, parental
history of colorectal cancer, aspirin use, multivitamin supplement use, and intakes of red meat,
dietary fats, and folate were similar between diabetics and nondiabetics. Diabetic women were
slightly less active and substantially heavier. Utilization of colonoscopy or sigmoidoscopy by
1992 was comparable among diabetic and nondiabetic women.
|
After adjustment for age, history of diabetes was significantly associated with increased risk of colorectal cancer (Table 2).
The age-adjusted RR was 1.53
(95% CI = 1.18-1.99; P = .001). After adjustment for body mass
index, smoking, alcohol use, menopause and estrogen use, family history of colorectal cancer,
aspirin use, physical activity, and red meat intake, the RR was 1.43 (95% CI =
1.10-1.87; P = .009). The positive association was stronger for colon cancer (RR
= 1.49; 95% CI = 1.09-2.06; P = .01) than for rectal cancer
(RR = 1.11; 95% CI = 0.56-2.21; P = .76). History of
diabetes was associated with increased risk of both proximal and distal colon cancers. The
multivariate RRs were 1.56 (95% CI = 1.07-2.28; P = .02) for
advanced colorectal cancer and 2.39 (95% CI = 1.46-3.92; P =
.0005) for fatal colorectal cancer. In stratified analyses by menopausal status, regular exercise at
least once per week (no or yes), and body mass index (27 kg/m2 versus >27
kg/m2), we found positive associations across different strata of these variables and
observed no statistically significant interactions between these variables and diabetes.
|
We conducted secondary analyses using diabetes classified by the supplementary questionnaire as the exposure variable (5434 women were classified as type 2 diabetes by the supplementary questionnaire). The age-adjusted RR of colorectal cancer was 1.49 (95% CI = 1.11-1.99), and the multivariate RR was 1.36 (95% CI = 1.01-1.84). The wide CIs were due to smaller number of colorectal cancer case patients (n = 48) in the diabetic group.
The positive associations were strongest among women whose diabetes had been diagnosed
for 11-15 years (Table 3). Compared with nondiabetics, the multivariate
RRs for this group were 2.30 (95% CI = 1.43-3.71; P = .0006) for
colorectal cancer, 2.83 (95% CI = 1.67-4.78; P = .0001) for colon
cancer, 2.25 (95% CI = 1.11-4.58; P = .02) for advanced
colorectal cancer, and 3.96 (95% CI = 1.72-9.12; P = .001) for
fatal colorectal cancer. (We did not analyze rectal cancer because of the small number of cases.)
These RRs diminished among women whose diabetes had been diagnosed for more than 15
years, although positive associations remained.
|
|
DISCUSSION |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
In this large prospective study of women, we observed a significant positive association between history of diabetes and risk of colorectal cancer. After we accounted for age, body mass index, and other potential confounders, diabetic women had a 43% increased risk of colorectal cancer and a 49% increase in colon cancer compared with nondiabetic women.
Physician-diagnosed diabetes was reported by the participants, but with high accuracy according to additional information obtained from supplemental questionnaires asking about symptoms and treatment and a validation study using medical record review (14). Some diabetics may have been undiagnosed, but this percentage would be relatively small compared with that in the general population because of the nurses' relative greater access to medical care. Moreover, misclassification in the diagnosis of diabetes would tend to attenuate any true association between diabetes and colon cancer. In additional analyses, we found a similar positive association when confirmed diabetes (based on women who returned the supplementary questionnaires) was used as an exposure variable.
Detection bias is the most plausible alternative explanation for the observed positive association because, among diabetics, early colorectal cancer may be more likely to be diagnosed as a result of a heightened screening and detection. Several lines of evidence, however, argue against this explanation. First, we found that the positive association was stronger for advanced and fatal colorectal cancers, which would be less prone to detection and diagnostic biases. Second, the increased risk was stronger among women who had diabetes for a considerable amount of time (i.e., 11-15 years). Enhanced surveillance and detection are probably more likely to occur in the first several years following diagnosis. Finally, utilization of colonoscopy or sigmiodoscopy was comparable among diabetic and nondiabetic women (28% and 26%, respectively, by 1992).
Confounding is another concern but was unlikely to explain our findings. As shown in Table
1,
colon cancer risk profiles were generally similar between diabetics and
nondiabetics. Body mass index and lack of physical activity are potentially the most important
known confounders for the positive association between diabetes and colon cancer. However, a
statistically significant association persists even after adjustment for these variables, both of
which were assessed multiple times during follow-up and the repeated assessments were used in
the analyses. Some of the covariates, such as alcohol consumption, red meat intake, and
multivitamin use, were first measured in 1980 rather than in 1976. However, when we controlled
for these variables, the multivariate RRs were similar to the age-adjusted ones; thus, any
uncontrolled confounding due to incomplete data for these variables was unlikely to account for
the observed association between diabetes and colorectal cancer. Also, analyses using 1980 as
baseline yielded similar results.
Previous epidemiologic studies of diabetes and colorectal cancer have suggested a positive association, but the data are not entirely consistent. Two studies of diabetic patients using external population comparisons (3,5) have found a small and nonsignificant excess in rate of colorectal cancer in men but not in women. In a case-control study conducted in Italy, history of diabetes was significantly associated with risk of both colon cancer (odds ratio [OR] = 1.7) and rectal cancer (OR = 1.5) (8). In a subsequent larger case-control study conducted by the same group (9), the OR was 1.2 for colon cancer and 1.5 for rectal cancer. The former study found the strongest association among subjects whose diabetes had been diagnosed for 5-9 years, and the latter found a stronger association among subjects who had diabetes for 10 years or more. Neither study examined the association among women who had diabetes for a longer duration. In our study, we observed a weaker positive association for rectal cancer, but the number of rectal cancer cases among diabetics was small (nine cases). In parallel, associations between obesity and a sedentary lifestyle have usually been observed with colon cancer but not with rectal cancer (1). In addition, we found that the positive association for colorectal cancer was greatest within 11-15 years after diagnosis of diabetes and diminished after 15 years of diagnosis (see the explanations below). In the only previous prospective cohort study (11), the RRs of colorectal cancer were 1.30 for men and 1.16 for women. However, in this study, status of diabetes was not updated during follow-up. The observed weaker associations were probably a result of prolonged follow-up.
Hyperinsulinemia has been proposed to be the underlying link between diabetes and colon cancer (1). This insulin-colon cancer hypothesis is based on strong epidemiologic evidence that major environmental risk factors for type 2 diabetes (such as high body mass index, increased central obesity, sedentary lifestyle, and possibly higher intake of refined carbohydrates) are remarkably similar to those for colon cancer. There is strong evidence that these factors are important determinants of insulin resistance and hyperinsulinemia (21,22). Since insulin is an important growth factor for colonic mucosal cells and colonic cancer cells and a mitogen of tumor cell growth in vitro (23,24) and a colon tumor promoter in vivo (25), high plasma insulin levels may mediate the effect of these factors on the risk of colon cancer. Based on the insulin hypothesis, the expected relationship between type 2 diabetes and colon cancer is complex because, at the early stage of type 2 diabetes, hyperinsulinemia exists but, in later stages, pancreatic beta cell malfunction leads to a hypoinsulinemic response. As expected a priori, we found that the increased risk of colorectal cancer diminished among women who had had diabetes for a long duration (i.e., after 15 years from diagnosis). However, the insulin hypothesis cannot be directly confirmed by these data because we did not measure plasma insulin levels and, also, the induction period for an effect of insulin on colon cancer risk is unknown.
Another line of evidence for the proposed insulin-colon cancer relationship is the observation that a high glycemic index diet, which has been associated with risk of type 2 diabetes (26,27) and coronary heart disease (28), is also associated with risk of colon cancer (29). A dietary glycemic index is used to quantify the response of blood glucose and insulin to a diet (30,31). The higher the glycemic index, the greater the glycemic and insulinemic responses. In a case-control study, Slattery et al. (29) found a positive association between dietary glycemic index and colon cancer. Higher intake of refined sugars, which produces a sharp glycemic response due to readily absorbable glucose, has been associated with increased risk of colon cancer in one prospective cohort study (32) and a number of case-control studies (33-37). In addition, higher intake of rapidly digestible starches, such as breads, potatoes, cakes, and dessert, may also increase risk of colon cancer (38). These findings suggest that glycemic and insulinemic responses may contribute to the effect of diet on the risk of colon cancer.
Besides insulin, several other mechanisms for the positive association have been proposed, including elevated levels of fecal bile acid associated with increased blood glucose and triglyceride levels (2) and slower bowel transit (11), which contributes to increased exposure to toxic substances and increased production of carcinogenic bile acids among diabetics.
In conclusion, our data provide support for the hypothesis that type 2 diabetes is associated with increased risk of colon cancer in women. These findings provide further epidemiologic evidence for the hypothesis that hyperinsulinemia, a compensatory response to insulin resistance, may be an underlying pathway for the development of colon cancer.
|
NOTES |
|---|
Supported by Public Health Service (PHS) grant CA40356 (National Cancer Institute) and PHS grants DK46200 and T32DK07703 (National Institute of Diabetes and Digestive and Kidney Diseases), National Institutes of Health, Department of Health and Human Services. F. B. Hu is a recipient of a Charles A. King Trust Research Fellowship from the Medical Foundation, Boston.
We are indebted to the participants in the Nurses' Health Study for their continuing outstanding level of cooperation; to Karen Corsano, Gary Chase, and Barbara Egan for their unfailing help; and to Drs. Walter Willett and Meir Stampfer for helpful comments.
|
REFERENCES |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1 Giovannucci E. Insulin and colon cancer. Cancer Causes Control 1995;6:164-79.[CrossRef][Web of Science][Medline]cancerlit;95267979
2 McKeown-Eyssen G. Epidemiology of colorectal cancer revisited: are serum triglycerides and/or plasma glucose associated with risk? Cancer Epidemiol Biomarkers Prev 1994;3:687-95.[Abstract]cancerlit;95187076
3 Adami HO, McLaughlin J, Ekbom A, Berne C, Silverman D, Hacker D, et al. Cancer risk in patients with diabetes mellitus. Cancer Causes Control 1991;2:307-14.[CrossRef][Web of Science][Medline]cancerlit;92032506
4 Kessler II. Cancer mortality among diabetics. J Natl Cancer Inst 1970;44:673-86.
5 Ragozzino M, Melton LJ 3d, Chu CP, Palumbo PJ. Subsequent cancer risk in the incidence cohort of Rochester, Minnesota, residents with diabetes mellitus. J Chronic Dis 1982;35:13-9.[CrossRef][Web of Science][Medline]cancerlit;82167921
6 Hardell L, Fredrikson M, Axelson O. Casecontrol study on colon cancer regarding previous disease and drug intake. Int J Oncol 1996;8:439-44.[Web of Science]
7 O'Mara BA, Byers T, Schoenfeld E. Diabetes mellitus and cancer risk: a multisite case-control study. J Chronic Dis 1985;38:435-41.[CrossRef][Web of Science][Medline]cancerlit;85208148
8 La Vecchia C, D'Avanzo B, Negri E, Franceschi S. History of selected diseases and the risk of colorectal cancer. Eur J Cancer 1991;27:582-6.cancerlit;91274048
9 La Vecchia C, Negri E, Decarli A, Franceschi S. Diabetes mellitus and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 1997;6:1007-10.[Abstract]cancerlit;98080665
10
Kune GA, Kune S, Watson LF. Colorectal cancer risk, chronic
illnesses, operations, and medications: case control results from the Melbourne Colorectal
Cancer Study. Cancer Res 1988;48:4399-404.
11
Will JC, Galuska DA, Vinicor F, Calle EE. Colorectal cancer:
another complication of diabetes mellitus? Am J Epidemiol 1998;147:816-25.
12
Colditz GA, Martin P, Stampfer MJ, Willett WC, Sampson L,
Rosner B, et al. Validation of questionnaire information on risk factors and disease outcomes in a
prospective cohort study of women. Am J Epidemiol 1986;123:894-900.
13
Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C,
Witschi J, et al. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 1985;122:51-65.
14
Manson JE, Colditz GA, Stampfer MJ, Willett WC, Krolewski
AS, Rosner B, et al. A prospective study of maturity-onset diabetes mellitus and risk of coronary
heart disease and stroke in women. Arch Intern Med 1991;151:1141-7.
15 Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance. National Diabetes Data Group. Diabetes 1979;28:1039-57.[Web of Science][Medline]
16
Willett WC, Hunter DJ, Stampfer MJ, Colditz GA, Manson JE,
Spiegelman D, et al. Dietary fat and fiber in relation to risk of breast cancer: an 8-year follow-up.JAMA
1992;268:2037-44.
17
Stampfer MJ, Willett WC, Speizer FE, Dysert DC, Lipnick R,
Rosner B, et al. Test of the National Death Index. Am J Epidemiol 1984;119:837-9.
18 D'Agostino RB, Lee ML, Belanger AJ, Cupples LA, Anderson K, Kannel WB. Relation of pooled logistic regression to time dependent Cox regression analysis: the Framingham Heart Study. Stat Med 1990;9:1501-15.[Web of Science][Medline]
19
Hu FB, Stampfer MJ, Manson JE, Rimm E, Colditz GA, Rosner
BA, et al. Dietary fat intake and risk of coronary heart disease in women. N Engl J Med 1997;337:1491-9.
20
Giovannucci E, Colditz GA, Stampfer MJ, Hunter D, Rosner
BA, Willett WC, et al. A prospective study of cigarette smoking and risk of colorectal adenoma
and colorectal cancer in U.S. women. J Natl Cancer Inst 1994;86:192-9.
21 Bjorntorp P. Metabolic implications of body fat distribution. Diabetes Care 1991;14:1132-43.[Abstract]
22 Koivisto VA, Yki-Jarvinen H, DeFronzo RA. Physical training and insulin sensitivity. Diabetes Metab Rev 1986;1:445-81.[Medline]
23 Koenuma M, Yamori T, Tsuruo T. Insulin and insulin-like growth factor 1 stimulate proliferation of metastatic variants of colon carcinoma 26. Jpn J Cancer Res 1989;80:51-8.[CrossRef][Web of Science][Medline]cancerlit;89213535
24 Watkins LF, Lewis LR, Levine AE. Characterization of the synergistic effect of insulin and transferrin and the regulation of their receptors on a human colon carcinoma cell line. Int J Cancer 1990;45:372-5.[Web of Science][Medline]cancerlit;90152943
25 Tran TT, Medline A, Bruce WR. Insulin promotion of colon tumors in rats. Cancer Epidemiol Biomarkers Prev 1996;5:1013-5.[Abstract]cancerlit;97118483
26
Salmeron J, Manson JE, Stampfer MJ, Colditz GA, Wing AL,
Willett WC. Dietary fiber, glycemic load, and risk of non-insulin-dependent diabetes mellitus in
women. JAMA 1997;277:472-7.
27 Salmeron J, Ascherio A, Rimm EB, Colditz GA, Spiegelman D, Jenkins DJ, et al. Dietary fiber, glycemic load, and risk of NIDDM in men. Diabetes Care 1997;20:545-50.[Abstract]
28 Liu S, Stampfer MJ, Manson JE, Hu FB, Franz M, Hennekens CH, et al. A prospective study of dietary glycemic load and risk of myocardial infarction in women [abstract]. FASEB J 1998;12:A260.
29
Slattery ML, Benson J, Berry TD, Duncan D, Edwards SL,
Cann BJ, et al. Dietary sugar and colon cancer. Cancer Epidemiol Biomarkers Prev1997
;6:677-85.
30
Jenkins DJ, Wolever TM, Taylor RH, Barker H, Fielden H,
Baldwin JM, et al. Glycemic index of foods: a physiological basis for carbohydrate exchange. Am J Clin Nutr 1981;34:362-6.
31
Jenkins DJ, Wolever TM, Buckley G, Lam KY, Giudici S,
Kalmusky J, et al. Low-glycemic-index starchy foods in the diabetic diet. Am J Clin Nutr 1988;48:248-54.
32 Bostick RM, Potter JD, Kushi LH, Sellers TA, Steinmetz KA, McKenzie DR, et al. Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 1994;5:38-52.[CrossRef][Web of Science][Medline]cancerlit;94169287
33 Bristol JB, Emmett PM, Heaton KW, Williamson RC. Sugar, fat, and the risk of colorectal cancer. Br Med J (Clin Res Ed) 1985;291:1467-70.
34 La Vecchia C, Negri E, Decarli A, D'Avanzo B, Gallotti L, Gentile A, et al. A case-control study of diet and colorectal cancer in northern Italy. Int J Cancer 1988;41:492-8.[Web of Science][Medline]cancerlit;88186256
35 Macquart-Moulin G, Riboli E, Cornee J, Charnay B, Berthezene P, Day N. Case-control study on colorectal cancer and diet in Marseilles. Int J Cancer 1986;38: 183-91.[Web of Science][Medline]cancerlit;86277006
36 Manousos O, Day NE, Trichopoulos D, Gerovassilis F, Tzonou A, Polychronopoulou A. Diet and colorectal cancer: a case-control study in Greece. Int J Cancer 1983;32: 1-5.[Web of Science][Medline]cancerlit;83237067
37
Pickle LW, Greene MH, Ziegler RG, Toledo A, Hoover R,
Lynch HT, et al. Colorectal cancer in rural Nebraska. Cancer Res 1984;44:363-9.
38 Franceschi S, Favero A, La Vecchia C, Negri E, Conti E, Montella M, et al. Food groups and risk of colorectal cancer in Italy. Int J Cancer 1997;72:56-61.[CrossRef][Web of Science][Medline]cancerlit;97355742
Manuscript received September 17, 1998; revised December 21, 1998; accepted December 31, 1998.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  J.-L. Chiasson Early Insulin Use in Type 2 Diabetes: What are the cons? Diabetes Care, November 1, 2009; 32(suppl_2): S270 - S274. [Full Text] [PDF]
|
|
|
|
 |
|
 S. Rinaldi, S. Rohrmann, M. Jenab, C. Biessy, S. Sieri, D. Palli, R. Tumino, A. Mattiello, P. Vineis, A. Nieters, et al. Glycosylated Hemoglobin and Risk of Colorectal Cancer in Men and Women, the European Prospective Investigation into Cancer and Nutrition Cancer Epidemiol. Biomarkers Prev., November 1, 2008; 17(11): 3108 - 3115. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. R. Folsom, J. S. Pankow, J. M. Peacock, S. J. Bielinski, G. Heiss, and E. Boerwinkle Variation in TCF7L2 and Increased Risk of Colon Cancer: The Atherosclerosis Risk in Communities (ARIC) Study Diabetes Care, May 1, 2008; 31(5): 905 - 909. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. N. Ealey, S. Lu, D. Lau, and M. C. Archer Reduced susceptibility of muscle-specific insulin receptor knockout mice to colon carcinogenesis Am J Physiol Gastrointest Liver Physiol, March 1, 2008; 294(3): G679 - G686. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Giovannucci Metabolic syndrome, hyperinsulinemia, and colon cancer: a review Am. J. Clinical Nutrition, September 1, 2007; 86(3): 836S - 842S. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 N Travier, M Jeffreys, N Brewer, C. Wright, C. Cunningham, J Hornell, and N Pearce Association between glycosylated hemoglobin and cancer risk: a New Zealand linkage study Ann. Onc., August 1, 2007; 18(8): 1414 - 1419. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. L. Sedjo, T. Byers, T. R. Levin, S. M. Haffner, M. F. Saad, J. A. Tooze, and R. B. D'Agostino Jr. Change in Body Size and the Risk of Colorectal Adenomas Cancer Epidemiol. Biomarkers Prev., March 1, 2007; 16(3): 526 - 531. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. L. Campbell and A. McTiernan Exercise and Biomarkers for Cancer Prevention Studies J. Nutr., January 1, 2007; 137(1): 161S - 169S. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Sturmer, J. E. Buring, I-M. Lee, J. M. Gaziano, and R. J. Glynn Metabolic Abnormalities and Risk for Colorectal Cancer in the Physicians' Health Study Cancer Epidemiol. Biomarkers Prev., December 1, 2006; 15(12): 2391 - 2397. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Flood, U. Peters, D. J. Jenkins, N. Chatterjee, A. F Subar, T. R Church, R. Bresalier, J. L Weissfeld, R. B Hayes, A. Schatzkin, et al. Carbohydrate, glycemic index, and glycemic load and colorectal adenomas in the Prostate, Lung, Colorectal, and Ovarian Screening Study. Am. J. Clinical Nutrition, November 1, 2006; 84(5): 1184 - 1192. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. S. Kasper and E. Giovannucci A Meta-analysis of Diabetes Mellitus and the Risk of Prostate Cancer. Cancer Epidemiol. Biomarkers Prev., November 1, 2006; 15(11): 2056 - 2062. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Lin, N. R. Cook, I-M. Lee, J. E. Manson, J. E. Buring, and S. M. Zhang Total magnesium intake and colorectal cancer incidence in women. Cancer Epidemiol. Biomarkers Prev., October 1, 2006; 15(10): 2006 - 2009. [Full Text] [PDF]
|
|
|
|
 |
|
 K. Bowers, D. Albanes, P. Limburg, P. Pietinen, P. R. Taylor, J. Virtamo, and R. Stolzenberg-Solomon A Prospective Study of Anthropometric and Clinical Measurements Associated with Insulin Resistance Syndrome and Colorectal Cancer in Male Smokers Am. J. Epidemiol., October 1, 2006; 164(7): 652 - 664. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. Inoue, M. Iwasaki, T. Otani, S. Sasazuki, M. Noda, S. Tsugane, and for the Japan Public Health Center-Based Prospecti Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan. Arch Intern Med, September 25, 2006; 166(17): 1871 - 1877. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 T. Pischon, P. H. Lahmann, H. Boeing, C. Friedenreich, T. Norat, A. Tjonneland, J. Halkjaer, K. Overvad, F. Clavel-Chapelon, M.-C. Boutron-Ruault, et al. Body Size and Risk of Colon and Rectal Cancer in the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst, July 5, 2006; 98(13): 920 - 931. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Irby, W. F. Anderson, D. E. Henson, and S. S. Devesa Emerging and widening colorectal carcinoma disparities between blacks and whites in the United States (1975-2002). Cancer Epidemiol. Biomarkers Prev., April 1, 2006; 15(4): 792 - 797. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. L. Bowker, S. R. Majumdar, P. Veugelers, and J. A. Johnson Increased Cancer-Related Mortality for Patients With Type 2 Diabetes Who Use Sulfonylureas or Insulin Diabetes Care, February 1, 2006; 29(2): 254 - 258. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Kim and B. M Popkin Commentary: Understanding the epidemiology of overweight and obesity--a real global public health concern Int. J. Epidemiol., February 1, 2006; 35(1): 60 - 67. [Full Text] [PDF]
|
|
|
|
|
|
A. Seow, J.-M. Yuan, W.-P. Koh, H.-P. Lee, and M. C. Yu Diabetes Mellitus and Risk of Colorectal Cancer in the Singapore Chinese Health Study J Natl Cancer Inst, January 18, 2006; 98(2): 135 - 138. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Lin, P. M. Ridker, A. Pradhan, I-M. Lee, J. E. Manson, N. R. Cook, J. E. Buring, and S. M. Zhang Hemoglobin A1c Concentrations and Risk of Colorectal Cancer in Women Cancer Epidemiol. Biomarkers Prev., December 1, 2005; 14(12): 3010 - 3012. [Full Text] [PDF]
|
|
|
|
 |
|
 T I L Nilsen, P R Romundstad, R Troisi, N Potischman, and L J Vatten Birth size and colorectal cancer risk: a prospective population based study Gut, December 1, 2005; 54(12): 1728 - 1732. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. C. Larsson, N. Orsini, and A. Wolk Diabetes Mellitus and Risk of Colorectal Cancer: A Meta-Analysis J Natl Cancer Inst, November 16, 2005; 97(22): 1679 - 1687. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. K. Wei, E. Giovannucci, C. S. Fuchs, W. C. Willett, and C. S. Mantzoros Low Plasma Adiponectin Levels and Risk of Colorectal Cancer in Men: A Prospective Study J Natl Cancer Inst, November 16, 2005; 97(22): 1688 - 1694. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. Mascitelli and F. Pezzetta C-Reactive Protein and Risk for Colorectal Cancer Ann Intern Med, October 4, 2005; 143(7): 544 - 544. [Full Text] [PDF]
|
|
|
|
|
|
A. Tavani, F. Bravi, C. Bosetti, S. Franceschi, F. Levi, R. Talamini, and C. La Vecchia Diabetes Mellitus and Subsite-Specific Colorectal Cancer Risks in the Iowa Women's Health Study Cancer Epidemiol. Biomarkers Prev., September 1, 2005; 14(9): 2277 - 2277. [Full Text] [PDF]
|
|
|
|
|
|
S. C. Larsson, E. Giovannucci, and A. Wolk Diabetes and Colorectal Cancer Incidence in the Cohort of Swedish Men Diabetes Care, July 1, 2005; 28(7): 1805 - 1807. [Full Text] [PDF]
|
|
|
|
|
|
E. Lim, I.T. Jones, P. Gibbs, S. McLaughlan, I. Faragher, I. Skinner, M.W. Chao, and J. Johns Subsite-Specific Colorectal Cancer in Diabetic and Nondiabetic Patients Cancer Epidemiol. Biomarkers Prev., June 1, 2005; 14(6): 1579 - 1582. [Full Text] [PDF]
|
|
|
|
|
|
E. K. Wei, J. Ma, M. N. Pollak, N. Rifai, C. S. Fuchs, S. E. Hankinson, and E. Giovannucci A Prospective Study of C-Peptide, Insulin-like Growth Factor-I, Insulin-like Growth Factor Binding Protein-1, and the Risk of Colorectal Cancer in Women Cancer Epidemiol. Biomarkers Prev., April 1, 2005; 14(4): 850 - 855. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Yamagata, Y. Kiyohara, S. Nakamura, M. Kubo, Y. Tanizaki, T. Matsumoto, K. Tanaka, I. Kato, T. Shirota, and M. Iida Impact of Fasting Plasma Glucose Levels on Gastric Cancer Incidence in a General Japanese Population: The Hisayama Study Diabetes Care, April 1, 2005; 28(4): 789 - 794. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. G Renehan and S. M Shalet Diabetes, insulin therapy, and colorectal cancer BMJ, March 12, 2005; 330(7491): 551 - 552. [Full Text] [PDF]
|
|
|
|
|
|
G. C. Hall, C. M. Roberts, M. Boulis, J. Mo, and K. D. MacRae Diabetes and the Risk of Lung Cancer Diabetes Care, March 1, 2005; 28(3): 590 - 594. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. H. Jee, H. Ohrr, J. W. Sull, J. E. Yun, M. Ji, and J. M. Samet Fasting Serum Glucose Level and Cancer Risk in Korean Men and Women JAMA, January 12, 2005; 293(2): 194 - 202. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. J. Limburg, K. E. Anderson, T. W. Johnson, D. R. Jacobs Jr., D. Lazovich, C.-P. Hong, K. K. Nicodemus, and A. R. Folsom Diabetes Mellitus and Subsite-Specific Colorectal Cancer Risks in the Iowa Women's Health Study Cancer Epidemiol. Biomarkers Prev., January 1, 2005; 14(1): 133 - 137. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. S. Michaud, C. S. Fuchs, S. Liu, W. C. Willett, G. A. Colditz, and E. Giovannucci Dietary Glycemic Load, Carbohydrate, Sugar, and Colorectal Cancer Risk in Men and Women Cancer Epidemiol. Biomarkers Prev., January 1, 2005; 14(1): 138 - 147. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K.-T. Khaw, N. Wareham, S. Bingham, R. Luben, A. Welch, and N. Day Preliminary Communication: Glycated Hemoglobin, Diabetes, and Incident Colorectal Cancer in Men and Women: A Prospective Analysis from the European Prospective Investigation into Cancer-Norfolk Study Cancer Epidemiol. Biomarkers Prev., June 1, 2004; 13(6): 915 - 919. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Hirose, K. Hata, T. Kuno, K. Yoshida, K. Sakata, Y. Yamada, T. Tanaka, B. S. Reddy, and H. Mori Enhancement of development of azoxymethane-induced colonic premalignant lesions in C57BL/KsJ-db/db mice Carcinogenesis, May 1, 2004; 25(5): 821 - 825. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Cho, S. A. Smith-Warner, J. Ritz, P. A. van den Brandt, G. A. Colditz, A. R. Folsom, J. L. Freudenheim, E. Giovannucci, R. A. Goldbohm, S. Graham, et al. Alcohol Intake and Colorectal Cancer: A Pooled Analysis of 8 Cohort Studies Ann Intern Med, April 20, 2004; 140(8): 603 - 613. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Ma, E. Giovannucci, M. Pollak, A. Leavitt, Y. Tao, J. M. Gaziano, and M. J. Stampfer A Prospective Study of Plasma C-Peptide and Colorectal Cancer Risk in Men J Natl Cancer Inst, April 7, 2004; 96(7): 546 - 553. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. T. Bloomgarden Definitions of the Insulin Resistance Syndrome: The 1st World Congress on the Insulin Resistance Syndrome Diabetes Care, March 1, 2004; 27(3): 824 - 830. [Full Text] [PDF]
|
|
|
|
 |
|
 E. Giovannucci Obesity, insulin, and colon cancer. AACR Meeting Abstracts, March 1, 2004; 2004(1): 1319 - 1320. [Abstract]
|
|
|
|
 |
|
 D. B. Boyd Insulin and Cancer Integr Cancer Ther, December 1, 2003; 2(4): 315 - 329. [Abstract] [PDF]
|
|
|
|
|
|
S. H. Saydah, C. M. Loria, M. S. Eberhardt, and F. L. Brancati Abnormal Glucose Tolerance and the Risk of Cancer Death in the United States Am. J. Epidemiol., June 15, 2003; 157(12): 1092 - 1100. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. H. Saydah, E. A. Platz, N. Rifai, M. N. Pollak, F. L. Brancati, and K. J. Helzlsouer Association of Markers of Insulin and Glucose Control with Subsequent Colorectal Cancer Risk Cancer Epidemiol. Biomarkers Prev., May 1, 2003; 12(5): 412 - 418. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Komninou, A. Ayonote, J. P. Richie Jr., and B. Rigas Insulin Resistance and Its Contribution to Colon Carcinogenesis Experimental Biology and Medicine, April 1, 2003; 228(4): 396 - 405. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Verlato, G. Zoppini, E. Bonora, and M. Muggeo Mortality From Site-Specific Malignancies in Type 2 Diabetic Patients From Verona Diabetes Care, April 1, 2003; 26(4): 1047 - 1051. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. A. Meyerhardt, P. J. Catalano, D. G. Haller, R. J. Mayer, J. S. Macdonald, A. B. Benson III, and C. S. Fuchs Impact of Diabetes Mellitus on Outcomes in Patients With Colon Cancer J. Clin. Oncol., February 1, 2003; 21(3): 433 - 440. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. M. Brauer, G. E. McKeown-Eyssen, V. Jazmaji, A. G. Logan, D. F. Andrews, D. Jenkins, N. Marcon, F. Saibil, L. Cohen, H. Stern, et al. Familial Aggregation of Diabetes and Hypertension in a Case-Control Study of Colorectal Neoplasia Am. J. Epidemiol., October 15, 2002; 156(8): 702 - 713. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. D. Girnun, W. M. Smith, S. Drori, P. Sarraf, E. Mueller, C. Eng, P. Nambiar, D. W. Rosenberg, R. T. Bronson, W. Edelmann, et al. APC-dependent suppression of colon carcinogenesis by PPARgamma PNAS, October 15, 2002; 99(21): 13771 - 13776. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. S. Sandhu, R. Luben, N. E. Day, and K.-T. Khaw Self-Reported Birth Weight and Subsequent Risk of Colorectal Cancer Cancer Epidemiol. Biomarkers Prev., September 1, 2002; 11(9): 935 - 938. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 L. O. Dragsted, B. Daneshvar, U. Vogel, H. N. Autrup, H. Wallin, L. Risom, P. Moller, A. M. Molck, M. Hansen, H. E. Poulsen, et al. A Sucrose-rich Diet Induces Mutations in the Rat Colon Cancer Res., August 1, 2002; 62(15): 4339 - 4345. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. S. Sandhu, D. B. Dunger, and E. L. Giovannucci Insulin, Insulin-Like Growth Factor-I (IGF-I), IGF Binding Proteins, Their Biologic Interactions, and Colorectal Cancer J Natl Cancer Inst, July 3, 2002; 94(13): 972 - 980. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. J. Jenkins, C. W. Kendall, L. S. Augustin, S. Franceschi, M. Hamidi, A. Marchie, A. L Jenkins, and M. Axelsen Glycemic index: overview of implications in health and disease Am. J. Clinical Nutrition, July 1, 2002; 76(1): 266S - 273. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Giovannucci Insulin, Insulin-Like Growth Factors and Colon Cancer: A Review of the Evidence J. Nutr., November 1, 2001; 131(11): 3109S - 3120. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
F. Grodstein, J. Chen, R. S. Wilson, and J. E. Manson Type 2 Diabetes and Cognitive Function in Community-Dwelling Elderly Women Diabetes Care, June 1, 2001; 24(6): 1060 - 1065. [Abstract] [Full Text]
|
|
|
|
 |
|
 C. A Sabin and A. N Phillips Cohort studies in sexual health Sex Transm Inf, June 1, 2001; 77(3): 174 - 178. [Full Text] [PDF]
|
|
|
|
|
|
W. R. Bruce, A. Giacca, and A. Medline Possible Mechanisms Relating Diet and Risk of Colon Cancer Cancer Epidemiol. Biomarkers Prev., December 1, 2000; 9(12): 1271 - 1279. [Abstract] [Full Text]
|
|
|
|
|
|
K. B. Michels, Edward Giovannucci, K. J. Joshipura, B. A. Rosner, M. J. Stampfer, C. S. Fuchs, G. A. Colditz, F. E. Speizer, and W. C. Willett Prospective Study of Fruit and Vegetable Consumption and Incidence of Colon and Rectal Cancers J Natl Cancer Inst, November 1, 2000; 92(21): 1740 - 1752. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Kaaks, P. Toniolo, A. Akhmedkhanov, A. Lukanova, C. Biessy, H. Dechaud, S. Rinaldi, A. Zeleniuch-Jacquotte, R. E. Shore, and E. Riboli Serum C-Peptide, Insulin-Like Growth Factor (IGF)-I, IGF-Binding Proteins, and Colorectal Cancer Risk in Women J Natl Cancer Inst, October 4, 2000; 92(19): 1592 - 1600. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. L. Slavin Mechanisms for the Impact of Whole Grain Foods on Cancer Risk J. Am. Coll. Nutr., June 1, 2000; 19(90003): 300S - 307. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. M. Ross Re: Prospective Study of Adult Onset Diabetes Mellitus (Type 2) and Risk of Colorectal Cancer in Women J Natl Cancer Inst, August 4, 1999; 91(15): 1334 - 1334. [Full Text] [PDF]
|
|
|
|
|
|
R. E. Schoen, C. M. Tangen, L. H. Kuller, G. L. Burke, M. Cushman, R. P. Tracy, A. Dobs, and P. J. Savage Increased Blood Glucose and Insulin, Body Size, and Incident Colorectal Cancer J Natl Cancer Inst, July 7, 1999; 91(13): 1147 - 1154. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||