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Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115 [E. G., W. C. W., M. J. S., G. A. C., F. E. S., S. E. H.]; Departments of Nutrition [E. G., E. A. P., W. C. W., M. J. S.] and Epidemiology [E. G., E. A. P., W. C. W., M. J. S., G. A. C. S. E. H.], Harvard School of Public Health, Boston, Massachusetts 02115; and Cancer Prevention Research Unit, Departments of Medicine and Oncology, Jewish General Hospital and McGill University, Montreal, Quebec, H3T 1E2 Canada [M. N. P., N. M.]
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Abstract |
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1 cm
or tubulovillous/villous histology), and 107 cases of early-stage
adenoma (<1 cm and tubular histology). After matching controls (2:1
for cancers and 1:1 for adenomas) to cases by age, month of blood draw,
fasting status, and indication for endoscopy (for adenoma controls),
plasma IGF-1 and IGFBP-3 levels were measured. Controlling for IGFBP-3
level, relative to women in the low tertile of IGF-1, those in the high
tertile were at elevated risk of intermediate/late-stage colorectal
neoplasia adenoma [multivariate relative risk (RR), 2.78; 95%
confidence interval (CI), 0.76–9.76] and cancer (RR, 2.18; 95% CI,
0.94–5.08). Controlling for IGF-1 level, relative to women in the low
tertile of IGFBP-3, women in the high tertile of IGFBP-3 were at lower
risk of intermediate/late-stage colorectal adenoma (RR, 0.28; 95% CI,
0.09–0.85) and cancer (RR, 0.28; 95% CI, 0.10–0.83). Neither IGF-1
nor IGFBP-3 had any appreciable relation with early-stage adenoma.
These analyses indicate that high levels of circulating IGF-1 and
particularly low levels of IGFBP-3 are associated independently with an
elevated risk of large or tubulovillous/villous colorectal adenoma and
cancer. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Normal colorectal epithelia and cancer cells express IGF-1 receptors, which stimulate mitogenesis when activated by IGF-1 in vitro (7 , 8) . As mitogens, IGFs may be important in colorectal carcinogenesis, possibly by increasing the risk of cellular transformation by enhancing cell turnover. Moreover, in colon cancer cell lines, IGF-1 increases production of vascular endothelial growth factor, an angiogenic factor that supports cancer growth (9) , and overexpression of IGF-1 receptors is also important for the survival and maintenance of transformed cells (10) . Indeed, acromegaly, characterized by chronically elevated growth hormone levels that cause IGF-1 hypersecretion, is associated with increased epithelial cell proliferation in the sigmoid colon (11) and elevated risk of tubulovillous adenomas and colorectal cancer (12) .
In recent studies, high but normal plasma IGF-1 and low IGFBP-3 levels were independently associated with a greater risk of prostate cancer (13) , premenopausal breast cancer (14) , and lung cancer (15) . A recent analysis in the Physicians’ Health Study found high IGF-1 levels and, in particular, low IGFBP-3 levels, to be related to a high risk of colorectal cancer in men (16) . Here, we examine the relationship between plasma IGF-1 and IGFBP-3 levels and risk of colorectal adenoma and cancer in a case-control study of women nested within the prospective NHS.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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When women reported a diagnosis of colorectal cancer or adenoma on the questionnaires, these were confirmed through histopathological reports reviewed by a study investigator. On the basis of the endoscopy and pathology reports, we recorded adenoma number, site, size, and histology (tubular, tubulovillous, and villous). For cancers, we recorded site and Duke’s stage at diagnosis.
Eligible colorectal cancer cases were women who supplied a blood sample
between 1989 and 1990, were diagnosed with adenocarcinoma of the colon
or rectum between the date of return of the blood sample and June 1,
1994, and had no prior (noncutaneous) cancer diagnosis. Controls were
selected from the 32,826 women who provided a blood sample. Controls
were required to not have had a cancer diagnosis at the time the
matched case was diagnosed. We chose at random two controls matched to
each case on year of birth, fasting status (for 68% of blood samples,
the participant had fasted for 8 h), and month of blood draw. For the
analyses, 79 cases and 158 matched controls were included.
Seventy-eight % of the cases were diagnosed at least 1 year after the
blood sample was provided. Thirty-one of the 158 had had an endoscopy
between 1980 and 1989.
To be eligible for selection as a case or control for the colorectal
adenoma analyses, women must have supplied a blood sample between 1989
and 1990, must have undergone sigmoidoscopy or colonoscopy after the
date of return of the blood sample (1989–1994), and not have had a
cancer or adenoma diagnosis, excluding nonmelanoma skin cancer, prior
to the date of endoscopy. Because the majority of women who underwent
endoscopy had a sigmoidoscopy, we included as cases only women with
adenomas of the distal colorectum. Controls were matched to cases on
year of birth, month of blood draw, fasting status, time period of
endoscopy (within 2 years), and routine screening, gastrointestinal
symptoms, or family history of colorectal cancer as indication(s) for
endoscopy. A total of 207 matched pairs were included in the analysis,
including 90 large (1 cm) or tubulovillous/villous adenomas (69 were
large; 21 were <1 cm and tubulovillous/villous) and 107 small, tubular
adenomas (10 adenomas had missing data on size or histological
subtype). Seventy-six % of the adenoma cases were diagnosed at least 1
year after the blood sample was provided.
Plasma IGF-1 and IGFBP-3 Assays.
Plasma IGF-1 and IGFBP-3 were assayed using ELISAs with reagents
from Diagnostic Systems Laboratory Inc. (Webster, TX). The IGF-1 values
obtained by the ELISA were highly correlated (Pearson r = 0.97) with values obtained by radioimmunoassay after acid
chromatography. All assays were carried out blinded to case-control
status, and quality control samples were included within assay runs.
Matched pairs were analyzed in the same run. The mean intrapair
coefficients of variation were 7.2 and 8.6% for IGF-1 and IGFBP-3,
respectively, for the adenoma analyses, and 2.5 and 3.9% for the
cancer analyses. We have demonstrated previously that our collection
methods did not adversely affect sample integrity (13)
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Assessment of Other Factors.
Mean values for demographic, dietary, and other covariates were
computed from the 1980 through 1990 questionnaires, including BMI
(weight in kg/square of height in m), physical activity
(MET-hours/week), aspirin use (days/month), cigarette pack-years
smoked, alcohol intake (g/day), red meat intake (servings/day), and
dietary intake of vitamin D, calcium, phosphorus, folate, and
methionine (all nutrients were adjusted for total energy intake by
residual analysis; Ref. 18
). We also assessed current (1990) use of
postmenopausal hormones.
Statistical Analysis.
We computed odds ratios to estimate the RR and corresponding 95% CI
using conditional logistic regression (SAS version 6.12; SAS Institute,
Cary, NC). Because IGF-1 and IGFBP-3 levels are positively correlated
but have opposing effects biologically, it was necessary to adjust
simultaneously for these factors to observe their independent effects.
Tests for trend using two-sided Ps were calculated by
entering the tertile-specific median value for IGF-1 and IGFBP-3 as
continuous variables in logistic regression models.
We examined the relation of IGF on three empirical stages of colorectal
carcinogenesis: (a) early-stage small, tubular adenomas that
may represent adenoma formation or "initiation", (b)
intermediate/late-stage adenomas 1 cm in diameter or those that had a
villous component (tubulovillous, villous), representing adenoma
progression (these include in situ cancers); and
(c) adenocarcinomas.
We computed independent effects of IGF-1 and IGFBP-3 in models with each of the following established or potential risk factors averaged from 1980 to 1990 for colorectal cancer (19) : intake of fat, carbohydrate, protein, folate, methionine, red meat, and alcohol, physical activity, BMI, pack-years smoked, aspirin use, and current (1990) postmenopausal hormone use. These covariates were included only if there was indication of confounding, i.e., if the RRs for IGF-1 or IGFBP-3 were appreciably different when these were added to models.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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shows the levels of IGF-1 and IGFBP-3, their interrelationships, and
their correlations with age, among controls, who represent the
underlying population. The higher mean plasma IGF-1 for the adenoma
controls reflects their lower median age compared with the cancer
controls. For the controls for small tubular adenoma cases, the mean
plasma IGF-1 level was 170.6 ng/ml, and the mean plasma IGFBP-3 level
was 3822 ng/ml; for controls for large or villous adenoma cases, these
respective levels were 162.5 and 3755 ng/ml. As expected, IGF-1 and
IGFBP-3 were strongly correlated, and a moderate inverse correlation
existed between age and total IGF-1, and age and IGF-1 adjusted for
IGFBP-3 level (Table 1)
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shows results for total colorectal cancer, intermediate late-stage
adenoma, and early-stage adenoma in relation to IGF-1 and IGFBP-3
levels. The patterns were similar for intermediate/late-stage adenoma
and cancer but different for small, tubular adenomas (Table 2)
. High
levels of IGF-1 were associated with increased risk of both cancer and
intermediate/late stage adenoma, although conventional statistical
significance was not achieved for either. Even stronger (inverse)
associations were observed for these endpoints with IGFBP-3 levels.
IGF-1 and IGFBP-3 were strong negative confounders of each other, and
associations for both were considerably stronger for cancer and
intermediate/late-stage adenoma when IGF-1 and IGFBP-3 were adjusted
for simultaneously.
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60
years of age. BMI and alcohol intake were both risk factors for
colorectal cancers (cases: mean alcohol, 8.1 g; mean BMI, 26.0
kg/m2; controls: mean alcohol, 6.7 g; mean BMI, 24.7
kg/m2). For total adenomas, alcohol intake and BMI were
slightly but nonsignificantly higher in cases, but alcohol was
significantly related to higher risk of large or villous adenomas. The
results were slightly weaker but still statistically significant for
IGFBP-3 when alcohol and BMI were not included. The associations were
similar whether we used average alcohol intake and BMI from 1980 to
1990 or the 1990 status only. Results were not materially altered when
we controlled individually in separate models for intake of fat,
carbohydrate, protein, folate, methionine, and red meat, physical
activity, pack-years smoked, aspirin use, and current postmenopausal
hormone use. The relationships observed in the overall analyses were
broadly similar for results limited to colon cancer
(n = 55) and for metastatic colorectal cancer
(n = 37).
No appreciable relationship was observed for either IGF-1 or IGFBP-3
and the early-stage small, tubular adenomas (Table 2)
. With IGF-1 and
IGFBP-3 modeled simultaneously, the RR for total distal colorectal
adenoma was 1.01 (95% CI, 0.53–1.93; P, trend, 0.96) and
0.87 (95% CI, 0.48–1.60; P, trend, 0.65), respectively,
comparing the high to the low tertiles for each.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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We found in women that a single measure of circulating IGF-1 and IGFBP-3 levels predicted risk of colorectal cancers and adenomas that were large or had a villous component. In contrast, no consistent relation between IGF-1 and IGFBP-3 and small tubular adenomas was observed, indicating that the IGF axis may be more important in late (adenoma growth and transformation) stages, or that only a subset of adenomas are primed to respond to IGF. Large or villous adenomas are clinically relevant, whereas smaller, tubular adenomas are of questionable relevance.
Growth hormone increases production of both IGF-1 and IGFBP-3, accounting in part for the relatively high correlation between plasma IGF-1 and IGFBP-3. Because of this correlation, it is important to control for these simultaneously to observe their independent effects. Our finding that, controlling for level of IGF-1, IGFBP-3 is a strong independent protective factor may reflect binding of IGF-1, making IGF-1 not available, or direct apoptotic effects by IGFBP-3, or both (4) . The 3–4-fold risk differential for colorectal cancer, also observed in men in a recent analysis (16) , suggests a more important role for this binding protein for colorectal cancer than had been indicated for prostate (13) or breast cancer (14) .
We considered the potential impact of chance or methodological biases in our study. Chance alone was unlikely to account for our findings because, individually, for large adenomas, tubulovillous/villous adenomas, and colorectal cancer, positive trends were observed for IGF-1, and highly significant inverse trends with IGFBP-3 were apparent. Although blood specimens were collected prior to the diagnosis, an undiagnosed cancer could theoretically have increased circulating IGF-1 while lowering IGFBP-3. This bias is unlikely because IGF-1 levels were not differentially elevated and IGFBP-3 levels were not depressed for the colorectal cases diagnosed earlier during follow-up rather than later. Moreover, these biases would be very unlikely for the large or tubulovillous/villous adenomas, preinvasive lesions.
Other measures, such as adolescent IGF-1 and IGFBP-3, mean circulating levels assessed over adolescence and adulthood, mean growth hormone level, or direct measures of tissue IGF bioactivity, might better capture the aspects of IGF physiology relevant for colorectal risk. We did not measure growth hormone level because it fluctuates widely over time, and hepatic IGF-1 production and release (and hence circulating IGF-1 level) integrates growth hormone level. To the extent that a single measure of circulating IGF-1 and IGFBP-3 is a proxy for the biologically relevant exposure and that measurement errors are random between cases and controls, our study design would tend to underestimate the magnitude of any true association. Over a short-term basis, the circulating IGF-1 level is quite stable; in one study, r = 0.97 between two measures taken an average of 5.8 days apart in 10 subjects, and r = 0.94 between two measures taken an average 42 days apart in 24 subjects (21) .
Childhood and adolescent levels of IGF-1 influence linear growth and correlates with height, and tallness is a risk factor for colorectal cancer (22, 23, 24, 25) . In the current study, height in 1976 was poorly correlated with adult IGF-1 level (r = 0.02 for 367 cancer and adenoma controls combined; P = 0.75), consistent with previous studies indicating that adolescent, but not adult, IGF-1 level correlates with height (26) . Integrated mean growth hormone level would be of interest because growth hormone stimulates local production of IGF-1 in addition to increasing circulating IGF-1 level.
Hyperinsulinemia has been proposed to explain why the Western lifestyle is related to colon cancer risk (27) . Some of the cancer-enhancing effect of insulin may be mediated through the IGF axis. Although supraphysiologic levels of insulin are required to activate the IGF receptor and stimulate cell division, insulin lowers circulating levels of IGFBP-1, a serum protein produced primarily by the liver (28 , 29) . IGFBP-1 binds the IGFs with high affinity and inhibits IGF action in vitro (30, 31, 32) . Conditions associated with decreased insulin levels, including fasting, exercise, and poorly controlled juvenile-onset diabetes mellitus, are associated with elevated IGFBP-1 (33, 34, 35, 36, 37, 38) . Serum IGFBP-1 fluctuates throughout the day, in parallel with insulin levels. Plausibly, IGFBP-1 may be an important mediator of the mitogenic effects of insulin.
If confirmed, our ability to demonstrate an association between IGF parameters with large, villous adenomas and localized colorectal cancers has potential clinical utility, because detecting and removing these lesions is the basis of secondary prevention of colorectal cancer incidence and mortality. However, a considerably larger study would be required to evaluate clinically utility. Of note, the relative risk of colorectal neoplasia related to "high risk" IGF profile is of the range of 2–4-fold. Although this relative risk is considerably weaker than those for hereditary syndromes (e.g., familial adenomatous polyposis, hereditary nonpolyposis colorectal cancer), the "high risk" profile as defined for IGF (e.g., top tertile) is far more common than the hereditary syndromes and thus influences a substantial number of cases.
Our results also suggest that lifestyle or pharmacologic approaches to decrease IGF-1 bioactivity may warrant investigation as risk reduction strategies targeted at individuals with increased IGF-1 levels relative to IGFBP-3. Unfortunately, relatively little is known about determinants of normal variation of IGF-1 and IGFBP-3 levels (39) . In cases of severe energy or protein restriction, IGF-1 levels are lowered (40, 41, 42) , and in various rodent tumors, IGF-1 appears to mediate the benefits of caloric restriction (43 , 44) . However, the influence of feasible reductions in energy or protein intake on IGF-1 is unclear. A recent study reported a moderate correlation between IGF-1 levels and alcohol consumption, but this association was observed only for men, and IGFBPs were not considered (21) . Pharmaceutical suppression of the growth hormone-IGF-1 axis by somatostatin analogues (45) or growth hormone-releasing hormone antagonists (46) may provide a more potent strategy, but issues of cost and side effects become important. Whether anti-IGF therapy has efficacy to treat colorectal cancer is unclear; our results apply directly to the prediagnostic stage. Finally, our results as well as other recent reports (4 , 13 , 15 , 16 , 47) raise concern that the chronic administration of growth hormone or IGF-1 over long periods may increase the risk of epithelial cancers. Such therapy has been proposed to delay some of the effects of aging (48) , but it would be prudent to evaluate any objective benefits of such intervention in the context of the potential risks associated with it.
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Acknowledgments |
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Footnotes |
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1 Supported by Research Grants CA 40356 and CA
49449 from the NIH and a grant from the National Cancer Institute of
Canada (to M. N. P.). 
2 To whom requests for reprints should be
addressed, at Channing Laboratory, 181 Longwood Avenue, Boston, MA
02115. Phone: (617) 432-4648; Fax: (617) 432-2435; E-mail: edward.giovannucci{at}channing.harvard.edu
3 The abbreviations used are: IGF-1, insulin-like
growth factor-1; IGFBP-3, insulin-like growth factor binding protein-3;
RR, relative risk; CI, confidence interval; NHS, Nurses’ Health Study;
BMI, body mass index.
Received 7/12/99; revised 12/31/99; accepted 1/24/00.
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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]
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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]
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F. Canzian, J. D. McKay, R. J. Cleveland, L. Dossus, C. Biessy, C. Boillot, S. Rinaldi, M. Llewellyn, V. Chajes, F. Clavel-Chapelon, et al. Genetic Variation in the Growth Hormone Synthesis Pathway in Relation to Circulating Insulin-Like Growth Factor-I, Insulin-Like Growth Factor Binding Protein-3, and Breast Cancer Risk: Results from the European Prospective Investigation into Cancer and Nutrition Study Cancer Epidemiol. Biomarkers Prev., October 1, 2005; 14(10): 2316 - 2325. [Abstract] [Full Text] [PDF]
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T. O. Keku, P. K. Lund, J. Galanko, J. G. Simmons, J. T. Woosley, and R. S. Sandler Insulin Resistance, Apoptosis, and Colorectal Adenoma Risk Cancer Epidemiol. Biomarkers Prev., September 1, 2005; 14(9): 2076 - 2081. [Abstract] [Full Text] [PDF]
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S. E Chiuve, E. L Giovannucci, S. E Hankinson, D. J Hunter, M. J Stampfer, W. C Willett, and E. B Rimm Alcohol intake and methylenetetrahydrofolate reductase polymorphism modify the relation of folate intake to plasma homocysteine Am. J. Clinical Nutrition, July 1, 2005; 82(1): 155 - 162. [Abstract] [Full Text] [PDF]
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R. Zhao, M. Berho, J. Nogueras, D. Sands, E. Weiss, S. Wexner, F. M. Giardiello, and M. Cruz-Correa Positive Correlation of Insulin-Like Growth Factor-II with Proliferating Cell Index in Patients with Colorectal Neoplasia Cancer Epidemiol. Biomarkers Prev., July 1, 2005; 14(7): 1819 - 1822. [Abstract] [Full Text] [PDF]
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L. M. Morimoto, P. A. Newcomb, E. White, J. Bigler, and J. D. Potter Variation in Plasma Insulin-Like Growth Factor-1 and Insulin-Like Growth Factor Binding Protein-3: Genetic Factors Cancer Epidemiol. Biomarkers Prev., June 1, 2005; 14(6): 1394 - 1401. [Abstract] [Full Text] [PDF]
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J. A. Meyerhardt, J. A. Sloan, D. J. Sargent, R. M. Goldberg, M. Pollak, R. F. Morton, R. K. Ramanathan, S. K. Williamson, B. P. Findlay, and C. S. Fuchs Associations between Plasma Insulin-Like Growth Factor Proteins and C-Peptide and Quality of Life in Patients with Metastatic Colorectal Cancer Cancer Epidemiol. Biomarkers Prev., June 1, 2005; 14(6): 1402 - 1410. [Abstract] [Full Text] [PDF]
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L. M. Morimoto, P. A. Newcomb, E. White, J. Bigler, and J. D. Potter Insulin-like Growth Factor Polymorphisms and Colorectal Cancer Risk Cancer Epidemiol. Biomarkers Prev., May 1, 2005; 14(5): 1204 - 1211. [Abstract] [Full Text] [PDF]
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L. Le Marchand, L. N. Kolonel, B. E. Henderson, and L. R. Wilkens Association of an Exon 1 Polymorphism in the IGFBP3 Gene with Circulating IGFBP-3 Levels and Colorectal Cancer Risk: The Multiethnic Cohort Study Cancer Epidemiol. Biomarkers Prev., May 1, 2005; 14(5): 1319 - 1321. [Abstract] [Full Text] [PDF]
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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]
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J. A Lavigne, D. J Baer, H. H Wimbrow, P. S Albert, E. D Brown, J. T Judd, W. S Campbell, C. A Giffen, J. F Dorgan, T. J Hartman, et al. Effects of alcohol on insulin-like growth factor I and insulin-like growth factor binding protein 3 in postmenopausal women Am. J. Clinical Nutrition, February 1, 2005; 81(2): 503 - 507. [Abstract] [Full Text] [PDF]
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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]
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H.-L. Wong, K. DeLellis, N. Probst-Hensch, W.-P. Koh, D. Van Den Berg, H.-P. Lee, M. C. Yu, and S. A. Ingles A New Single Nucleotide Polymorphism in the Insulin-Like Growth Factor I Regulatory Region Associates with Colorectal Cancer Risk in Singapore Chinese Cancer Epidemiol. Biomarkers Prev., January 1, 2005; 14(1): 144 - 151. [Abstract] [Full Text] [PDF]
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D. W. Voskuil, A. Vrieling, L. J. van't Veer, E. Kampman, and M. A. Rookus The Insulin-like Growth Factor System in Cancer Prevention: Potential of Dietary Intervention Strategies Cancer Epidemiol. Biomarkers Prev., January 1, 2005; 14(1): 195 - 203. [Abstract] [Full Text] [PDF]
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 M. Terzolo, G. Reimondo, M. Gasperi, R. Cozzi, R. Pivonello, G. Vitale, A. Scillitani, R. Attanasio, E. Cecconi, F. Daffara, et al. Colonoscopic Screening and Follow-Up in Patients with Acromegaly: A Multicenter Study in Italy J. Clin. Endocrinol. Metab., January 1, 2005; 90(1): 84 - 90. [Abstract] [Full Text] [PDF]
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K. DeLellis, S. Rinaldi, R. J. Kaaks, L. N. Kolonel, B. Henderson, and L. Le Marchand Dietary and Lifestyle Correlates of Plasma Insulin-Like Growth Factor-I (IGF-I) and IGF Binding Protein-3 (IGFBP-3): The Multiethnic Cohort Cancer Epidemiol. Biomarkers Prev., September 1, 2004; 13(9): 1444 - 1451. [Abstract] [Full Text] [PDF]
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C. Hoppe, T. Rovenna Udam, L. Lauritzen, C. Molgaard, A. Juul, and K. Fleischer Michaelsen Animal protein intake, serum insulin-like growth factor I, and growth in healthy 2.5-y-old Danish children Am. J. Clinical Nutrition, August 1, 2004; 80(2): 447 - 452. [Abstract] [Full Text] [PDF]
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X. Wu, H. Zhao, K.-A. Do, M. M. Johnson, Q. Dong, W. K. Hong, and M. R. Spitz Serum Levels of Insulin Growth Factor (IGF-I) and IGF-Binding Protein Predict Risk of Second Primary Tumors in Patients with Head and Neck Cancer Clin. Cancer Res., June 15, 2004; 10(12): 3988 - 3995. [Abstract] [Full Text] [PDF]
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 E. Giovannucci Obesity, insulin, and colon cancer. AACR Meeting Abstracts, March 1, 2004; 2004(1): 1319 - 1320. [Abstract]
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J. A. Meyerhardt, J. E. Tepper, D. Niedzwiecki, D. R. Hollis, A. D. McCollum, D. Brady, M. J. O'Connell, R. J. Mayer, B. Cummings, C. Willett, et al. Impact of Body Mass Index on Outcomes and Treatment-Related Toxicity in Patients With Stage II and III Rectal Cancer: Findings From Intergroup Trial 0114 J. Clin. Oncol., February 15, 2004; 22(4): 648 - 657. [Abstract] [Full Text] [PDF]
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A. Decensi, U. Veronesi, R. Miceli, H. Johansson, L. Mariani, T. Camerini, M. G. Di Mauro, E. Cavadini, G. De Palo, A. Costa, et al. Relationships between Plasma Insulin-like Growth Factor-I and Insulin-like Growth Factor Binding Protein-3 and Second Breast Cancer Risk in a Prevention Trial of Fenretinide Clin. Cancer Res., October 15, 2003; 9(13): 4722 - 4729. [Abstract] [Full Text] [PDF]
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A. M. Y. Nomura, G. N. Stemmermann, J. Lee, and M. N. Pollak Serum Insulin-like Growth Factor I and Subsequent Risk of Colorectal Cancer among Japanese-American Men Am. J. Epidemiol., September 1, 2003; 158(5): 424 - 431. [Abstract] [Full Text] [PDF]
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N. M. Probst-Hensch, H. Wang, V. H. H. Goh, A. Seow, H.-P. Lee, and M. C. Yu Determinants of Circulating Insulin-like Growth Factor I and Insulin-like Growth Factor Binding Protein 3 Concentrations in a Cohort of Singapore Men and Women Cancer Epidemiol. Biomarkers Prev., August 1, 2003; 12(8): 739 - 746. [Abstract] [Full Text] [PDF]
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 E. J. Kim, I.-J. Kang, H. J. Cho, W. K. Kim, Y.-L. Ha, and J. H. Y. Park Conjugated Linoleic Acid Downregulates Insulin-Like Growth Factor-I Receptor Levels in HT-29 Human Colon Cancer Cells J. Nutr., August 1, 2003; 133(8): 2675 - 2681. [Abstract] [Full Text] [PDF]
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 B. S. Kristal and U. Paolucci Caloric Restriction in trans Sci. Aging Knowl. Environ., July 9, 2003; 2003(27): pe19 - 19. [Abstract] [Full Text]
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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]
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H. G. Skinner, D. S. Michaud, G. A. Colditz, E. L. Giovannucci, M. J. Stampfer, W. C. Willett, and C. S. Fuchs Parity, Reproductive Factors, and the Risk of Pancreatic Cancer in Women Cancer Epidemiol. Biomarkers Prev., May 1, 2003; 12(5): 433 - 438. [Abstract] [Full Text] [PDF]
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 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]
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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]
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 P. Boyle and M. E. Leon Epidemiology of colorectal cancer Br. Med. Bull., December 1, 2002; 64(1): 1 - 25. [Abstract] [Full Text] [PDF]
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S. M. Firth and R. C. Baxter Cellular Actions of the Insulin-Like Growth Factor Binding Proteins Endocr. Rev., December 1, 2002; 23(6): 824 - 854. [Abstract] [Full Text] [PDF]
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K. H. Schmitz, R. L. Ahmed, and D. Yee Effects of a 9-Month Strength Training Intervention on Insulin, Insulin-like Growth Factor (IGF)-I, IGF-binding Protein (IGFBP)-1, and IGFBP-3 in 30-50-Year-Old Women Cancer Epidemiol. Biomarkers Prev., December 1, 2002; 11(12): 1597 - 1604. [Abstract] [Full Text] [PDF]
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T. Standal, M. Borset, S. Lenhoff, F. Wisloff, B. Stordal, A. Sundan, A. Waage, and C. Seidel Serum insulinlike growth factor is not elevated in patients with multiple myeloma but is still a prognostic factor Blood, December 1, 2002; 100(12): 3925 - 3929. [Abstract] [Full Text] [PDF]
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M. R. Spitz, M. J. Barnett, G. E. Goodman, M. D. Thornquist, X. Wu, and M. Pollak Serum Insulin-like Growth Factor (IGF) and IGF-binding Protein Levels and Risk of Lung Cancer: A Case-Control Study Nested in the {beta}-Carotene and Retinol Efficacy Trial Cohort Cancer Epidemiol. Biomarkers Prev., November 1, 2002; 11(11): 1413 - 1418. [Abstract] [Full Text] [PDF]
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E. Giovannucci, C. A. Haiman, E. A. Platz, S. E. Hankinson, M. N. Pollak, and D. J. Hunter Dinucleotide Repeat in the Insulin-like Growth Factor-I Gene Is Not Related to Risk of Colorectal Adenoma Cancer Epidemiol. Biomarkers Prev., November 1, 2002; 11(11): 1509 - 1510. [Full Text] [PDF]
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M. D. Holmes, M. N. Pollak, W. C. Willett, and S. E. Hankinson Dietary Correlates of Plasma Insulin-like Growth Factor I and Insulin-like Growth Factor Binding Protein 3 Concentrations Cancer Epidemiol. Biomarkers Prev., September 1, 2002; 11(9): 852 - 861. [Abstract] [Full Text] [PDF]
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M. D. Holmes, M. N. Pollak, and S. E. Hankinson Lifestyle Correlates of Plasma Insulin-like Growth Factor I and Insulin-like Growth Factor Binding Protein 3 Concentrations Cancer Epidemiol. Biomarkers Prev., September 1, 2002; 11(9): 862 - 867. [Abstract] [Full Text] [PDF]
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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]
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S. Teramukai, T. Rohan, H. Eguchi, T. Oda, K. Shinchi, and S. Kono Anthropometric and Behavioral Correlates of Insulin-like Growth Factor I and Insulin-like Growth Factor Binding Protein 3 in Middle-aged Japanese Men Am. J. Epidemiol., August 15, 2002; 156(4): 344 - 348. [Abstract] [Full Text] [PDF]
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S. Chang, X. Wu, H. Yu, and M. R. Spitz Plasma Concentrations of Insulin-like Growth Factors among Healthy Adult Men and Postmenopausal Women: Associations with Body Composition, Lifestyle, and Reproductive Factors Cancer Epidemiol. Biomarkers Prev., August 1, 2002; 11(8): 758 - 766. [Abstract] [Full Text] [PDF]
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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]
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P. Lucidi, N. Parlanti, F. Piccioni, F. Santeusanio, and P. de Feo Short-Term Treatment with Low Doses of Recombinant Human GH Stimulates Lipolysis in Visceral Obese Men J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3105 - 3109. [Abstract] [Full Text] [PDF]
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R. E. Schoen, J. Schragin, J. L. Weissfeld, F. L. Thaete, R. W. Evans, C. J. Rosen, and L. H. Kuller Lack of Association between Adipose Tissue Distribution and IGF-1 and IGFBP-3 in Men and Women Cancer Epidemiol. Biomarkers Prev., June 1, 2002; 11(6): 581 - 586. [Abstract] [Full Text] [PDF]
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S. J. London, J.-M. Yuan, G. S. Travlos, Y.-T. Gao, R. E. Wilson, R. K. Ross, and M. C. Yu Insulin-Like Growth Factor I, IGF-Binding Protein 3, and Lung Cancer Risk in a Prospective Study of Men in China J Natl Cancer Inst, May 15, 2002; 94(10): 749 - 754. [Abstract] [Full Text] [PDF]
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R Palmqvist, G Hallmans, S Rinaldi, C Biessy, R Stenling, E Riboli, and R Kaaks Plasma insulin-like growth factor 1, insulin-like growth factor binding protein 3, and risk of colorectal cancer: a prospective study in northern Sweden Gut, May 1, 2002; 50(5): 642 - 646. [Abstract] [Full Text] [PDF]
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 C. S. Carter, M. M. Ramsey, R. L. Ingram, A. B. Cashion, W. T. Cefalu, Z.Q. Wang, and W. E. Sonntag Models of Growth Hormone and IGF-1 Deficiency: Applications to Studies of Aging Processes and Life-Span Determination J. Gerontol. A Biol. Sci. Med. Sci., May 1, 2002; 57(5): B177 - 188. [Abstract] [Full Text]
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L. Le Marchand, T. Donlon, A. Seifried, R. Kaaks, S. Rinaldi, and L. R. Wilkens Association of a Common Polymorphism in the Human GH1 Gene with Colorectal Neoplasia J Natl Cancer Inst, March 20, 2002; 94(6): 454 - 460. [Abstract] [Full Text] [PDF]
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M. J. Borugian, S. B. Sheps, A. S. Whittemore, A. H. Wu, J. D. Potter, and R. P. Gallagher Carbohydrates and Colorectal Cancer Risk among Chinese in North America Cancer Epidemiol. Biomarkers Prev., February 1, 2002; 11(2): 187 - 193. [Abstract] [Full Text] [PDF]
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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]
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A. Decensi, H. Johansson, R. Miceli, L. Mariani, T. Camerini, E. Cavadini, M. G. Di Mauro, A. Barreca, A. G. Gonzaga, S. Diani, et al. Long-Term Effects of Fenretinide, a Retinoic Acid Derivative, on the Insulin-like Growth Factor System in Women with Early Breast Cancer Cancer Epidemiol. Biomarkers Prev., October 1, 2001; 10(10): 1047 - 1053. [Abstract] [Full Text] [PDF]
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J. Ma, E. Giovannucci, M. Pollak, J. M. Chan, J. M. Gaziano, W. Willett, and M. J. Stampfer Milk Intake, Circulating Levels of Insulin-Like Growth Factor-I, and Risk of Colorectal Cancer in Men J Natl Cancer Inst, September 5, 2001; 93(17): 1330 - 1336. [Abstract] [Full Text] [PDF]
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C. Deal, J. Ma, F. Wilkin, J. Paquette, F. Rozen, B. Ge, T. Hudson, M. Stampfer, and M. Pollak Novel Promoter Polymorphism in Insulin-Like Growth Factor-Binding Protein-3: Correlation with Serum Levels and Interaction with Known Regulators J. Clin. Endocrinol. Metab., March 1, 2001; 86(3): 1274 - 1280. [Abstract] [Full Text]
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J. Ma, M. Stampfer, and M. Pollak RESPONSE: More About: Prospective Study of Colorectal Cancer Risk in Men and Plasma Levels of Insulin-Like Growth Factor (IGF)-I and IGF- Binding Protein-3 J Natl Cancer Inst, December 6, 2000; 92(23): 1949 - 1949. [Full Text] [PDF]
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A. G. Renehan, S. T. O'Dwyer, and S. M. Shalet RESPONSE: More About: Prospective Study of Colorectal Cancer Risk in Men and Plasma Levels of Insulin-Like Growth Factor (IGF)-I and IGF-Binding Protein-3 J Natl Cancer Inst, December 6, 2000; 92(23): 1949a - 1949a. [Full Text] [PDF]
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