A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk

Ruth C. Travis; Paul N. Appleby; Richard M. Martin; Jeffrey M P Holly; Demetrius Albanes; Amanda Black; H. Bas Bueno-De-Mesquita; June M. Chan; Chu Chen; Maria Dolores Chirlaque; Michael B. Cook; Mélanie Deschasaux; Jenny L. Donovan; Luigi Ferrucci; Pilar Galan; Graham G. Giles; Edward L. Giovannucci; Marc J. Gunter; Laurel A. Habel; Freddie C. Hamdy; Kathy J. Helzlsouer; Serge Hercberg; Robert N. Hoover; Joseph A M J L Janssen; Rudolf Kaaks; Tatsuhiko Kubo; Loic Le Marchand; E. Jeffrey Metter; Kazuya Mikami; Joan K. Morris; David E. Neal; Marian L. Neuhouser; Kotaro Ozasa; Domenico Palli; Elizabeth A. Platz; Michael N. Pollak; Alison J. Price; Monique J. Roobol; Catherine Schaefer; Jeannette M. Schenk; Gianluca Severi; Meir J. Stampfer; Pär Stattin; Akiko Tamakoshi; Catherine M. Tangen; Mathilde Touvier; Nicholas J. Wald; Noel S. Weiss; Regina G. Ziegler; Timothy J. Key; Naomi E. Allen

doi:10.1158/0008-5472.CAN-15-1551

A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk

Ruth C. Travis^*, Paul N. Appleby, Richard M. Martin, Jeffrey M P Holly, Demetrius Albanes, Amanda Black, H. Bas Bueno-De-Mesquita, June M. Chan, Chu Chen, Maria Dolores Chirlaque, Michael B. Cook, Mélanie Deschasaux, Jenny L. Donovan, Luigi Ferrucci, Pilar Galan, Graham G. Giles, Edward L. Giovannucci, Marc J. Gunter, Laurel A. Habel, Freddie C. HamdyKathy J. Helzlsouer, Serge Hercberg, Robert N. Hoover, Joseph A M J L Janssen, Rudolf Kaaks, Tatsuhiko Kubo, Loic Le Marchand, E. Jeffrey Metter, Kazuya Mikami, Joan K. Morris, David E. Neal, Marian L. Neuhouser, Kotaro Ozasa, Domenico Palli, Elizabeth A. Platz, Michael N. Pollak, Alison J. Price, Monique J. Roobol, Catherine Schaefer, Jeannette M. Schenk, Gianluca Severi, Meir J. Stampfer, Pär Stattin, Akiko Tamakoshi, Catherine M. Tangen, Mathilde Touvier, Nicholas J. Wald, Noel S. Weiss, Regina G. Ziegler, Timothy J. Key, Naomi E. Allen

^*Corresponding author for this work

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Abstract

The role of insulin-like growth factors (IGF) in prostate cancer development is not fully understood. To investigate the association between circulating concentrations of IGFs (IGF-I, IGF-II, IGFBP-1, IGFBP-2, and IGFBP-3) and prostate cancer risk, we pooled individual participant data from 17 prospective and two cross-sectional studies, including up to 10,554 prostate cancer cases and 13,618 control participants. Conditional logistic regression was used to estimate the ORs for prostate cancer based on the study-specific fifth of each analyte. Overall, IGF-I, IGF-II, IGFBP-2, and IGFBP-3 concentrations were positively associated with prostate cancer risk (P_trend all ≤ 0.005), and IGFBP-1 was inversely associated weakly with risk (P_trend = 0.05). However, heterogeneity between the prospective and cross-sectional studies was evident (P_{heterogeneity} = 0.03), unless the analyses were restricted to prospective studies (with the exception of IGF-II, P_{heterogeneity} = 0.02). For prospective studies, the OR for men in the highest versus the lowest fifth of each analyte was 1.29 (95% confidence interval, 1.16-1.43) for IGF-I, 0.81 (0.68-0.96) for IGFBP-1, and 1.25 (1.12-1.40) for IGFBP-3. These associations did not differ significantly by time-to-diagnosis or tumor stage or grade. Aftermutual adjustment for each of the other analytes, only IGF-I remained associated with risk. Our collaborative study represents the largest pooled analysis of the relationship between prostate cancer risk and circulating concentrations of IGF-I, providing strong evidence that IGF-I is highly likely to be involved in prostate cancer development.

Original language	English
Pages (from-to)	2288-2300
Number of pages	13
Journal	Cancer Research
Volume	76
Issue number	8
Early online date	26 Feb 2016
DOIs	https://doi.org/10.1158/0008-5472.CAN-15-1551
Publication status	Published - 15 Apr 2016

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Centre for Surgical Research

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10.1158/0008-5472.CAN-15-1551

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Professor Richard M Martin
- Richard.Martin@bristol.ac.uk
- Bristol Population Health Science Institute
- MRC Integrative Epidemiology Unit
- Cancer
- Bristol Medical School (PHS) - Professor of Clinical Epidemiology
Person: Academic , Member

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Travis, R. C., Appleby, P. N., Martin, R. M., Holly, J. M. P., Albanes, D., Black, A., Bueno-De-Mesquita, H. B., Chan, J. M., Chen, C., Chirlaque, M. D., Cook, M. B., Deschasaux, M., Donovan, J. L., Ferrucci, L., Galan, P., Giles, G. G., Giovannucci, E. L., Gunter, M. J., Habel, L. A., ... Allen, N. E. (2016). A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk. Cancer Research, 76(8), 2288-2300. https://doi.org/10.1158/0008-5472.CAN-15-1551

Travis, Ruth C. ; Appleby, Paul N. ; Martin, Richard M. ; Holly, Jeffrey M P ; Albanes, Demetrius ; Black, Amanda ; Bueno-De-Mesquita, H. Bas ; Chan, June M. ; Chen, Chu ; Chirlaque, Maria Dolores ; Cook, Michael B. ; Deschasaux, Mélanie ; Donovan, Jenny L. ; Ferrucci, Luigi ; Galan, Pilar ; Giles, Graham G. ; Giovannucci, Edward L. ; Gunter, Marc J. ; Habel, Laurel A. ; Hamdy, Freddie C. ; Helzlsouer, Kathy J. ; Hercberg, Serge ; Hoover, Robert N. ; Janssen, Joseph A M J L ; Kaaks, Rudolf ; Kubo, Tatsuhiko ; Le Marchand, Loic ; Metter, E. Jeffrey ; Mikami, Kazuya ; Morris, Joan K. ; Neal, David E. ; Neuhouser, Marian L. ; Ozasa, Kotaro ; Palli, Domenico ; Platz, Elizabeth A. ; Pollak, Michael N. ; Price, Alison J. ; Roobol, Monique J. ; Schaefer, Catherine ; Schenk, Jeannette M. ; Severi, Gianluca ; Stampfer, Meir J. ; Stattin, Pär ; Tamakoshi, Akiko ; Tangen, Catherine M. ; Touvier, Mathilde ; Wald, Nicholas J. ; Weiss, Noel S. ; Ziegler, Regina G. ; Key, Timothy J. ; Allen, Naomi E. / A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk. In: Cancer Research. 2016 ; Vol. 76, No. 8. pp. 2288-2300.

@article{68bcb6943a2d41d0866554d1d35c84b0,

title = "A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk",

abstract = "The role of insulin-like growth factors (IGF) in prostate cancer development is not fully understood. To investigate the association between circulating concentrations of IGFs (IGF-I, IGF-II, IGFBP-1, IGFBP-2, and IGFBP-3) and prostate cancer risk, we pooled individual participant data from 17 prospective and two cross-sectional studies, including up to 10,554 prostate cancer cases and 13,618 control participants. Conditional logistic regression was used to estimate the ORs for prostate cancer based on the study-specific fifth of each analyte. Overall, IGF-I, IGF-II, IGFBP-2, and IGFBP-3 concentrations were positively associated with prostate cancer risk (Ptrend all ≤ 0.005), and IGFBP-1 was inversely associated weakly with risk (Ptrend = 0.05). However, heterogeneity between the prospective and cross-sectional studies was evident (Pheterogeneity = 0.03), unless the analyses were restricted to prospective studies (with the exception of IGF-II, Pheterogeneity = 0.02). For prospective studies, the OR for men in the highest versus the lowest fifth of each analyte was 1.29 (95% confidence interval, 1.16-1.43) for IGF-I, 0.81 (0.68-0.96) for IGFBP-1, and 1.25 (1.12-1.40) for IGFBP-3. These associations did not differ significantly by time-to-diagnosis or tumor stage or grade. Aftermutual adjustment for each of the other analytes, only IGF-I remained associated with risk. Our collaborative study represents the largest pooled analysis of the relationship between prostate cancer risk and circulating concentrations of IGF-I, providing strong evidence that IGF-I is highly likely to be involved in prostate cancer development.",

author = "Travis, {Ruth C.} and Appleby, {Paul N.} and Martin, {Richard M.} and Holly, {Jeffrey M P} and Demetrius Albanes and Amanda Black and Bueno-De-Mesquita, {H. Bas} and Chan, {June M.} and Chu Chen and Chirlaque, {Maria Dolores} and Cook, {Michael B.} and M{\'e}lanie Deschasaux and Donovan, {Jenny L.} and Luigi Ferrucci and Pilar Galan and Giles, {Graham G.} and Giovannucci, {Edward L.} and Gunter, {Marc J.} and Habel, {Laurel A.} and Hamdy, {Freddie C.} and Helzlsouer, {Kathy J.} and Serge Hercberg and Hoover, {Robert N.} and Janssen, {Joseph A M J L} and Rudolf Kaaks and Tatsuhiko Kubo and {Le Marchand}, Loic and Metter, {E. Jeffrey} and Kazuya Mikami and Morris, {Joan K.} and Neal, {David E.} and Neuhouser, {Marian L.} and Kotaro Ozasa and Domenico Palli and Platz, {Elizabeth A.} and Pollak, {Michael N.} and Price, {Alison J.} and Roobol, {Monique J.} and Catherine Schaefer and Schenk, {Jeannette M.} and Gianluca Severi and Stampfer, {Meir J.} and P{\"a}r Stattin and Akiko Tamakoshi and Tangen, {Catherine M.} and Mathilde Touvier and Wald, {Nicholas J.} and Weiss, {Noel S.} and Ziegler, {Regina G.} and Key, {Timothy J.} and Allen, {Naomi E.}",

year = "2016",

month = apr,

day = "15",

doi = "10.1158/0008-5472.CAN-15-1551",

language = "English",

volume = "76",

pages = "2288--2300",

journal = "Cancer Research",

issn = "0008-5472",

publisher = "American Association for Cancer Research Inc.",

number = "8",

}

Travis, RC, Appleby, PN, Martin, RM, Holly, JMP, Albanes, D, Black, A, Bueno-De-Mesquita, HB, Chan, JM, Chen, C, Chirlaque, MD, Cook, MB, Deschasaux, M, Donovan, JL, Ferrucci, L, Galan, P, Giles, GG, Giovannucci, EL, Gunter, MJ, Habel, LA, Hamdy, FC, Helzlsouer, KJ, Hercberg, S, Hoover, RN, Janssen, JAMJL, Kaaks, R, Kubo, T, Le Marchand, L, Metter, EJ, Mikami, K, Morris, JK, Neal, DE, Neuhouser, ML, Ozasa, K, Palli, D, Platz, EA, Pollak, MN, Price, AJ, Roobol, MJ, Schaefer, C, Schenk, JM, Severi, G, Stampfer, MJ, Stattin, P, Tamakoshi, A, Tangen, CM, Touvier, M, Wald, NJ, Weiss, NS, Ziegler, RG, Key, TJ & Allen, NE 2016, 'A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk', Cancer Research, vol. 76, no. 8, pp. 2288-2300. https://doi.org/10.1158/0008-5472.CAN-15-1551

A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk. / Travis, Ruth C.; Appleby, Paul N.; Martin, Richard M.; Holly, Jeffrey M P; Albanes, Demetrius; Black, Amanda; Bueno-De-Mesquita, H. Bas; Chan, June M.; Chen, Chu; Chirlaque, Maria Dolores; Cook, Michael B.; Deschasaux, Mélanie; Donovan, Jenny L.; Ferrucci, Luigi; Galan, Pilar; Giles, Graham G.; Giovannucci, Edward L.; Gunter, Marc J.; Habel, Laurel A.; Hamdy, Freddie C.; Helzlsouer, Kathy J.; Hercberg, Serge; Hoover, Robert N.; Janssen, Joseph A M J L; Kaaks, Rudolf; Kubo, Tatsuhiko; Le Marchand, Loic; Metter, E. Jeffrey; Mikami, Kazuya; Morris, Joan K.; Neal, David E.; Neuhouser, Marian L.; Ozasa, Kotaro; Palli, Domenico; Platz, Elizabeth A.; Pollak, Michael N.; Price, Alison J.; Roobol, Monique J.; Schaefer, Catherine; Schenk, Jeannette M.; Severi, Gianluca; Stampfer, Meir J.; Stattin, Pär; Tamakoshi, Akiko; Tangen, Catherine M.; Touvier, Mathilde; Wald, Nicholas J.; Weiss, Noel S.; Ziegler, Regina G.; Key, Timothy J.; Allen, Naomi E.

In: Cancer Research, Vol. 76, No. 8, 15.04.2016, p. 2288-2300.

Research output: Contribution to journal › Article (Academic Journal) › peer-review

TY - JOUR

T1 - A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk

AU - Travis, Ruth C.

AU - Appleby, Paul N.

AU - Martin, Richard M.

AU - Holly, Jeffrey M P

AU - Albanes, Demetrius

AU - Black, Amanda

AU - Bueno-De-Mesquita, H. Bas

AU - Chan, June M.

AU - Chen, Chu

AU - Chirlaque, Maria Dolores

AU - Cook, Michael B.

AU - Deschasaux, Mélanie

AU - Donovan, Jenny L.

AU - Ferrucci, Luigi

AU - Galan, Pilar

AU - Giles, Graham G.

AU - Giovannucci, Edward L.

AU - Gunter, Marc J.

AU - Habel, Laurel A.

AU - Hamdy, Freddie C.

AU - Helzlsouer, Kathy J.

AU - Hercberg, Serge

AU - Hoover, Robert N.

AU - Janssen, Joseph A M J L

AU - Kaaks, Rudolf

AU - Kubo, Tatsuhiko

AU - Le Marchand, Loic

AU - Metter, E. Jeffrey

AU - Mikami, Kazuya

AU - Morris, Joan K.

AU - Neal, David E.

AU - Neuhouser, Marian L.

AU - Ozasa, Kotaro

AU - Palli, Domenico

AU - Platz, Elizabeth A.

AU - Pollak, Michael N.

AU - Price, Alison J.

AU - Roobol, Monique J.

AU - Schaefer, Catherine

AU - Schenk, Jeannette M.

AU - Severi, Gianluca

AU - Stampfer, Meir J.

AU - Stattin, Pär

AU - Tamakoshi, Akiko

AU - Tangen, Catherine M.

AU - Touvier, Mathilde

AU - Wald, Nicholas J.

AU - Weiss, Noel S.

AU - Ziegler, Regina G.

AU - Key, Timothy J.

AU - Allen, Naomi E.

PY - 2016/4/15

Y1 - 2016/4/15

N2 - The role of insulin-like growth factors (IGF) in prostate cancer development is not fully understood. To investigate the association between circulating concentrations of IGFs (IGF-I, IGF-II, IGFBP-1, IGFBP-2, and IGFBP-3) and prostate cancer risk, we pooled individual participant data from 17 prospective and two cross-sectional studies, including up to 10,554 prostate cancer cases and 13,618 control participants. Conditional logistic regression was used to estimate the ORs for prostate cancer based on the study-specific fifth of each analyte. Overall, IGF-I, IGF-II, IGFBP-2, and IGFBP-3 concentrations were positively associated with prostate cancer risk (Ptrend all ≤ 0.005), and IGFBP-1 was inversely associated weakly with risk (Ptrend = 0.05). However, heterogeneity between the prospective and cross-sectional studies was evident (Pheterogeneity = 0.03), unless the analyses were restricted to prospective studies (with the exception of IGF-II, Pheterogeneity = 0.02). For prospective studies, the OR for men in the highest versus the lowest fifth of each analyte was 1.29 (95% confidence interval, 1.16-1.43) for IGF-I, 0.81 (0.68-0.96) for IGFBP-1, and 1.25 (1.12-1.40) for IGFBP-3. These associations did not differ significantly by time-to-diagnosis or tumor stage or grade. Aftermutual adjustment for each of the other analytes, only IGF-I remained associated with risk. Our collaborative study represents the largest pooled analysis of the relationship between prostate cancer risk and circulating concentrations of IGF-I, providing strong evidence that IGF-I is highly likely to be involved in prostate cancer development.

AB - The role of insulin-like growth factors (IGF) in prostate cancer development is not fully understood. To investigate the association between circulating concentrations of IGFs (IGF-I, IGF-II, IGFBP-1, IGFBP-2, and IGFBP-3) and prostate cancer risk, we pooled individual participant data from 17 prospective and two cross-sectional studies, including up to 10,554 prostate cancer cases and 13,618 control participants. Conditional logistic regression was used to estimate the ORs for prostate cancer based on the study-specific fifth of each analyte. Overall, IGF-I, IGF-II, IGFBP-2, and IGFBP-3 concentrations were positively associated with prostate cancer risk (Ptrend all ≤ 0.005), and IGFBP-1 was inversely associated weakly with risk (Ptrend = 0.05). However, heterogeneity between the prospective and cross-sectional studies was evident (Pheterogeneity = 0.03), unless the analyses were restricted to prospective studies (with the exception of IGF-II, Pheterogeneity = 0.02). For prospective studies, the OR for men in the highest versus the lowest fifth of each analyte was 1.29 (95% confidence interval, 1.16-1.43) for IGF-I, 0.81 (0.68-0.96) for IGFBP-1, and 1.25 (1.12-1.40) for IGFBP-3. These associations did not differ significantly by time-to-diagnosis or tumor stage or grade. Aftermutual adjustment for each of the other analytes, only IGF-I remained associated with risk. Our collaborative study represents the largest pooled analysis of the relationship between prostate cancer risk and circulating concentrations of IGF-I, providing strong evidence that IGF-I is highly likely to be involved in prostate cancer development.

UR - http://www.scopus.com/inward/record.url?scp=84969972281&partnerID=8YFLogxK

U2 - 10.1158/0008-5472.CAN-15-1551

DO - 10.1158/0008-5472.CAN-15-1551

M3 - Article (Academic Journal)

C2 - 26921328

AN - SCOPUS:84969972281

VL - 76

SP - 2288

EP - 2300

JO - Cancer Research

JF - Cancer Research

SN - 0008-5472

IS - 8

ER -

A meta-analysis of individual participant data reveals an association between circulating levels of IGF-I and prostate cancer risk

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Professor Richard M Martin

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