Insulin-like growth factors, their binding proteins, and prostate cancer risk

Analysis of individual patient data from 12 prospective studies

Andrew W. Roddam, Naomi E. Allen, Paul Appleby, Timothy J. Key, Luigi Ferrucci, H. Ballentine Carter, E. Metter, Chu Chen, Noel S. Weiss, Annette Fitzpatrick, Ann W. Hsing, James V. Lacey, Kathy Helzlsouer, Sabina Rinaldi, Elio Riboli, Rudolf Kaaks, Joop A.M.J.L. Janssen, Mark F. Wildhagen, Fritz H. Schröder, Elizabeth A. Platz & 19 others Michael Pollak, Edward Giovannucci, Catherine Schaefer, Charles P. Quesenberry, Joseph H. Vogelman, Gianluca Severi, Dallas R. English, Graham G. Giles, Pär Stattin, Göran Hallmans, Mattias Johansson, June M. Chan, Peter Gann, Steven E. Oliver, Jeff M. Holly, Jenny Donovan, François Meyer, Isabelle Bairati, Pilar Galan

Research output: Contribution to journalArticle

219 Citations (Scopus)

Abstract

Background: Some, but not all, published results have shown an association between circulating blood levels of some insulin-like growth factors (IGFs) and their binding proteins (IGFBPs) and the subsequent risk for prostate cancer. Purpose: To assess the association between levels of IGFs and IGFBPs and the subsequent risk for prostate cancer. Data Sources: Studies identified in PubMed, Web of Science, and CancerLit. Study Selection: The principal investigators of all studies that published data on circulating concentrations of sex steroids, IGFs, or IGFBPs and prostate cancer risk using prospectively collected blood samples were invited to collaborate. Data Extraction: Investigators provided individual participant data on circulating concentrations of IGF-I, IGF-II, IGFBP-II, and IGFBP-III and participant characteristics to a central data set in Oxford, United Kingdom. Data Synthesis: The study included data on 3700 men with prostate cancer and 5200 control participants. On average, case patients were 61.5 years of age at blood collection and received a diagnosis of prostate cancer 5 years after blood collection. The greater the serum IGF-I concentration, the greater the subsequent risk for prostate cancer (odds ratio [OR] in the highest vs. lowest quintile, 1.38 [95% CI, 1.19 to 1.60]; P < 0.001 for trend). Neither IGF-II nor IGFBP-II concentrations were associated with prostate cancer risk, but statistical power was limited. Insulin-like growth factor I and IGFBP-III were correlated (r = 0.58), and although IGFBP-III concentration seemed to be associated with prostate cancer risk, this was secondary to its association with IGF-I levels. Insulin-like growth factor I concentrations seemed to be more positively associated with low-grade than high-grade disease; otherwise, the association between IGFs and IGFBPs and prostate cancer risk had no statistically significant heterogeneity related to stage or grade of disease, time between blood collection and diagnosis, age and year of diagnosis, prostate-specific antigen level at recruitment, body mass index, smoking, or alcohol intake. Limitations: Insulin-like growth factor concentrations were measured in only 1 sample for each participant, and the laboratory methods to measure IGFs differed in each study. Not all patients had disease stage or grade information, and the diagnosis of prostate cancer may differ among the studies. Conclusion: High circulating IGF-I concentrations are associated with a moderately increased risk for prostate cancer.

Original languageEnglish (US)
Pages (from-to)461-471
Number of pages11
JournalAnnals of internal medicine
Volume149
Issue number7
DOIs
StatePublished - Oct 7 2008

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Insulin-Like Growth Factor Binding Proteins
Prostatic Neoplasms
Prospective Studies
Insulin-Like Growth Factor I
Somatomedins
Insulin-Like Growth Factor II
Research Personnel
Information Storage and Retrieval
Prostate-Specific Antigen
PubMed
Body Mass Index
Smoking
Odds Ratio
Steroids
Alcohols

All Science Journal Classification (ASJC) codes

  • Internal Medicine

Cite this

Insulin-like growth factors, their binding proteins, and prostate cancer risk : Analysis of individual patient data from 12 prospective studies. / Roddam, Andrew W.; Allen, Naomi E.; Appleby, Paul; Key, Timothy J.; Ferrucci, Luigi; Carter, H. Ballentine; Metter, E.; Chen, Chu; Weiss, Noel S.; Fitzpatrick, Annette; Hsing, Ann W.; Lacey, James V.; Helzlsouer, Kathy; Rinaldi, Sabina; Riboli, Elio; Kaaks, Rudolf; Janssen, Joop A.M.J.L.; Wildhagen, Mark F.; Schröder, Fritz H.; Platz, Elizabeth A.; Pollak, Michael; Giovannucci, Edward; Schaefer, Catherine; Quesenberry, Charles P.; Vogelman, Joseph H.; Severi, Gianluca; English, Dallas R.; Giles, Graham G.; Stattin, Pär; Hallmans, Göran; Johansson, Mattias; Chan, June M.; Gann, Peter; Oliver, Steven E.; Holly, Jeff M.; Donovan, Jenny; Meyer, François; Bairati, Isabelle; Galan, Pilar.

In: Annals of internal medicine, Vol. 149, No. 7, 07.10.2008, p. 461-471.

Research output: Contribution to journalArticle

Roddam, AW, Allen, NE, Appleby, P, Key, TJ, Ferrucci, L, Carter, HB, Metter, E, Chen, C, Weiss, NS, Fitzpatrick, A, Hsing, AW, Lacey, JV, Helzlsouer, K, Rinaldi, S, Riboli, E, Kaaks, R, Janssen, JAMJL, Wildhagen, MF, Schröder, FH, Platz, EA, Pollak, M, Giovannucci, E, Schaefer, C, Quesenberry, CP, Vogelman, JH, Severi, G, English, DR, Giles, GG, Stattin, P, Hallmans, G, Johansson, M, Chan, JM, Gann, P, Oliver, SE, Holly, JM, Donovan, J, Meyer, F, Bairati, I & Galan, P 2008, 'Insulin-like growth factors, their binding proteins, and prostate cancer risk: Analysis of individual patient data from 12 prospective studies', Annals of internal medicine, vol. 149, no. 7, pp. 461-471. https://doi.org/10.7326/0003-4819-149-7-200810070-00006
Roddam, Andrew W. ; Allen, Naomi E. ; Appleby, Paul ; Key, Timothy J. ; Ferrucci, Luigi ; Carter, H. Ballentine ; Metter, E. ; Chen, Chu ; Weiss, Noel S. ; Fitzpatrick, Annette ; Hsing, Ann W. ; Lacey, James V. ; Helzlsouer, Kathy ; Rinaldi, Sabina ; Riboli, Elio ; Kaaks, Rudolf ; Janssen, Joop A.M.J.L. ; Wildhagen, Mark F. ; Schröder, Fritz H. ; Platz, Elizabeth A. ; Pollak, Michael ; Giovannucci, Edward ; Schaefer, Catherine ; Quesenberry, Charles P. ; Vogelman, Joseph H. ; Severi, Gianluca ; English, Dallas R. ; Giles, Graham G. ; Stattin, Pär ; Hallmans, Göran ; Johansson, Mattias ; Chan, June M. ; Gann, Peter ; Oliver, Steven E. ; Holly, Jeff M. ; Donovan, Jenny ; Meyer, François ; Bairati, Isabelle ; Galan, Pilar. / Insulin-like growth factors, their binding proteins, and prostate cancer risk : Analysis of individual patient data from 12 prospective studies. In: Annals of internal medicine. 2008 ; Vol. 149, No. 7. pp. 461-471.
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title = "Insulin-like growth factors, their binding proteins, and prostate cancer risk: Analysis of individual patient data from 12 prospective studies",
abstract = "Background: Some, but not all, published results have shown an association between circulating blood levels of some insulin-like growth factors (IGFs) and their binding proteins (IGFBPs) and the subsequent risk for prostate cancer. Purpose: To assess the association between levels of IGFs and IGFBPs and the subsequent risk for prostate cancer. Data Sources: Studies identified in PubMed, Web of Science, and CancerLit. Study Selection: The principal investigators of all studies that published data on circulating concentrations of sex steroids, IGFs, or IGFBPs and prostate cancer risk using prospectively collected blood samples were invited to collaborate. Data Extraction: Investigators provided individual participant data on circulating concentrations of IGF-I, IGF-II, IGFBP-II, and IGFBP-III and participant characteristics to a central data set in Oxford, United Kingdom. Data Synthesis: The study included data on 3700 men with prostate cancer and 5200 control participants. On average, case patients were 61.5 years of age at blood collection and received a diagnosis of prostate cancer 5 years after blood collection. The greater the serum IGF-I concentration, the greater the subsequent risk for prostate cancer (odds ratio [OR] in the highest vs. lowest quintile, 1.38 [95{\%} CI, 1.19 to 1.60]; P < 0.001 for trend). Neither IGF-II nor IGFBP-II concentrations were associated with prostate cancer risk, but statistical power was limited. Insulin-like growth factor I and IGFBP-III were correlated (r = 0.58), and although IGFBP-III concentration seemed to be associated with prostate cancer risk, this was secondary to its association with IGF-I levels. Insulin-like growth factor I concentrations seemed to be more positively associated with low-grade than high-grade disease; otherwise, the association between IGFs and IGFBPs and prostate cancer risk had no statistically significant heterogeneity related to stage or grade of disease, time between blood collection and diagnosis, age and year of diagnosis, prostate-specific antigen level at recruitment, body mass index, smoking, or alcohol intake. Limitations: Insulin-like growth factor concentrations were measured in only 1 sample for each participant, and the laboratory methods to measure IGFs differed in each study. Not all patients had disease stage or grade information, and the diagnosis of prostate cancer may differ among the studies. Conclusion: High circulating IGF-I concentrations are associated with a moderately increased risk for prostate cancer.",
author = "Roddam, {Andrew W.} and Allen, {Naomi E.} and Paul Appleby and Key, {Timothy J.} and Luigi Ferrucci and Carter, {H. Ballentine} and E. Metter and Chu Chen and Weiss, {Noel S.} and Annette Fitzpatrick and Hsing, {Ann W.} and Lacey, {James V.} and Kathy Helzlsouer and Sabina Rinaldi and Elio Riboli and Rudolf Kaaks and Janssen, {Joop A.M.J.L.} and Wildhagen, {Mark F.} and Schr{\"o}der, {Fritz H.} and Platz, {Elizabeth A.} and Michael Pollak and Edward Giovannucci and Catherine Schaefer and Quesenberry, {Charles P.} and Vogelman, {Joseph H.} and Gianluca Severi and English, {Dallas R.} and Giles, {Graham G.} and P{\"a}r Stattin and G{\"o}ran Hallmans and Mattias Johansson and Chan, {June M.} and Peter Gann and Oliver, {Steven E.} and Holly, {Jeff M.} and Jenny Donovan and Fran{\cc}ois Meyer and Isabelle Bairati and Pilar Galan",
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TY - JOUR

T1 - Insulin-like growth factors, their binding proteins, and prostate cancer risk

T2 - Analysis of individual patient data from 12 prospective studies

AU - Roddam, Andrew W.

AU - Allen, Naomi E.

AU - Appleby, Paul

AU - Key, Timothy J.

AU - Ferrucci, Luigi

AU - Carter, H. Ballentine

AU - Metter, E.

AU - Chen, Chu

AU - Weiss, Noel S.

AU - Fitzpatrick, Annette

AU - Hsing, Ann W.

AU - Lacey, James V.

AU - Helzlsouer, Kathy

AU - Rinaldi, Sabina

AU - Riboli, Elio

AU - Kaaks, Rudolf

AU - Janssen, Joop A.M.J.L.

AU - Wildhagen, Mark F.

AU - Schröder, Fritz H.

AU - Platz, Elizabeth A.

AU - Pollak, Michael

AU - Giovannucci, Edward

AU - Schaefer, Catherine

AU - Quesenberry, Charles P.

AU - Vogelman, Joseph H.

AU - Severi, Gianluca

AU - English, Dallas R.

AU - Giles, Graham G.

AU - Stattin, Pär

AU - Hallmans, Göran

AU - Johansson, Mattias

AU - Chan, June M.

AU - Gann, Peter

AU - Oliver, Steven E.

AU - Holly, Jeff M.

AU - Donovan, Jenny

AU - Meyer, François

AU - Bairati, Isabelle

AU - Galan, Pilar

PY - 2008/10/7

Y1 - 2008/10/7

N2 - Background: Some, but not all, published results have shown an association between circulating blood levels of some insulin-like growth factors (IGFs) and their binding proteins (IGFBPs) and the subsequent risk for prostate cancer. Purpose: To assess the association between levels of IGFs and IGFBPs and the subsequent risk for prostate cancer. Data Sources: Studies identified in PubMed, Web of Science, and CancerLit. Study Selection: The principal investigators of all studies that published data on circulating concentrations of sex steroids, IGFs, or IGFBPs and prostate cancer risk using prospectively collected blood samples were invited to collaborate. Data Extraction: Investigators provided individual participant data on circulating concentrations of IGF-I, IGF-II, IGFBP-II, and IGFBP-III and participant characteristics to a central data set in Oxford, United Kingdom. Data Synthesis: The study included data on 3700 men with prostate cancer and 5200 control participants. On average, case patients were 61.5 years of age at blood collection and received a diagnosis of prostate cancer 5 years after blood collection. The greater the serum IGF-I concentration, the greater the subsequent risk for prostate cancer (odds ratio [OR] in the highest vs. lowest quintile, 1.38 [95% CI, 1.19 to 1.60]; P < 0.001 for trend). Neither IGF-II nor IGFBP-II concentrations were associated with prostate cancer risk, but statistical power was limited. Insulin-like growth factor I and IGFBP-III were correlated (r = 0.58), and although IGFBP-III concentration seemed to be associated with prostate cancer risk, this was secondary to its association with IGF-I levels. Insulin-like growth factor I concentrations seemed to be more positively associated with low-grade than high-grade disease; otherwise, the association between IGFs and IGFBPs and prostate cancer risk had no statistically significant heterogeneity related to stage or grade of disease, time between blood collection and diagnosis, age and year of diagnosis, prostate-specific antigen level at recruitment, body mass index, smoking, or alcohol intake. Limitations: Insulin-like growth factor concentrations were measured in only 1 sample for each participant, and the laboratory methods to measure IGFs differed in each study. Not all patients had disease stage or grade information, and the diagnosis of prostate cancer may differ among the studies. Conclusion: High circulating IGF-I concentrations are associated with a moderately increased risk for prostate cancer.

AB - Background: Some, but not all, published results have shown an association between circulating blood levels of some insulin-like growth factors (IGFs) and their binding proteins (IGFBPs) and the subsequent risk for prostate cancer. Purpose: To assess the association between levels of IGFs and IGFBPs and the subsequent risk for prostate cancer. Data Sources: Studies identified in PubMed, Web of Science, and CancerLit. Study Selection: The principal investigators of all studies that published data on circulating concentrations of sex steroids, IGFs, or IGFBPs and prostate cancer risk using prospectively collected blood samples were invited to collaborate. Data Extraction: Investigators provided individual participant data on circulating concentrations of IGF-I, IGF-II, IGFBP-II, and IGFBP-III and participant characteristics to a central data set in Oxford, United Kingdom. Data Synthesis: The study included data on 3700 men with prostate cancer and 5200 control participants. On average, case patients were 61.5 years of age at blood collection and received a diagnosis of prostate cancer 5 years after blood collection. The greater the serum IGF-I concentration, the greater the subsequent risk for prostate cancer (odds ratio [OR] in the highest vs. lowest quintile, 1.38 [95% CI, 1.19 to 1.60]; P < 0.001 for trend). Neither IGF-II nor IGFBP-II concentrations were associated with prostate cancer risk, but statistical power was limited. Insulin-like growth factor I and IGFBP-III were correlated (r = 0.58), and although IGFBP-III concentration seemed to be associated with prostate cancer risk, this was secondary to its association with IGF-I levels. Insulin-like growth factor I concentrations seemed to be more positively associated with low-grade than high-grade disease; otherwise, the association between IGFs and IGFBPs and prostate cancer risk had no statistically significant heterogeneity related to stage or grade of disease, time between blood collection and diagnosis, age and year of diagnosis, prostate-specific antigen level at recruitment, body mass index, smoking, or alcohol intake. Limitations: Insulin-like growth factor concentrations were measured in only 1 sample for each participant, and the laboratory methods to measure IGFs differed in each study. Not all patients had disease stage or grade information, and the diagnosis of prostate cancer may differ among the studies. Conclusion: High circulating IGF-I concentrations are associated with a moderately increased risk for prostate cancer.

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