Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis

Sean Harrison; Rosie Lennon; Jeffrey M P Holly; Julian Higgins; Mike P Gardner; Claire Perks; Tom Gaunt; Vanessa Tan; Catherine Borwick; Pauline Emmett; Mona Jeffreys; Kate Northstone; Sabina Rinaldi; Stephen Thomas; Suzanne Turner; Anna Pease; Vicky Vilenchik; Richard Martin; Sarah Lewis

doi:10.1007/s10552-017-0883-1

Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis

Sean Harrison, Rosie Lennon, Jeffrey M P Holly, Julian Higgins, Mike P Gardner, Claire Perks, Tom Gaunt, Vanessa Tan, Catherine Borwick, Pauline Emmett, Mona Jeffreys, Kate Northstone, Sabina Rinaldi, Stephen Thomas, Suzanne Turner, Anna Pease, Vicky Vilenchik, Richard Martin, Sarah Lewis

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

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Abstract

Purpose: To establish whether the association between milk intake and prostate cancer operates via the insulin-like growth factor (IGF) pathway (including IGF-I, IGF-II, IGFBP-1, IGFBP-2 and IGFBP-3).

Methods: Systematic review, collating data from all relevant studies examining associations of milk with IGF, and those examining associations of IGF with prostate cancer risk and progression. Data were extracted from experimental and observational studies conducted in either humans or animals, and analysed using meta-analysis where possible, with summary data presented otherwise.

Results: One hundred and seventy two studies met inclusion criteria: 31 examining the milk-IGF relationship; 132 examining the IGF-prostate cancer relationship in humans; and 10 animal studies examining the IGF-prostate cancer relationship. There was moderate evidence that circulating IGF-I and IGFBP-3 increase with milk (and dairy protein) intake (an estimated standardised effect size of 0.10 SD increase in IGF-I and 0.05 SD in IGFBP-3 per 1 SD increase in milk intake). There was moderate evidence that prostate cancer risk increased with IGF-I (Random effects meta-analysis OR per SD increase in IGF-I: 1.09; 95% CI: 1.03, 1.16; N = 51 studies) and decreased with IGFBP-3 (OR: 0.90; 0.83, 0.98; N = 39 studies), but not with other growth factors. The IGFBP-3 -202A/C single nucleotide polymorphism was positively associated with prostate cancer (pooled OR for A/C vs AA =1.22; 95% CI: 0.84, 1.79; OR for C/C vs AA = 1.51; 1.03, 2.21, N = 8 studies). No strong associations were observed for IGF-II, IGFBP-1 or IGFBP-2 with either milk intake or prostate cancer risk. There was little consistency within the data extracted from the small number of animal studies. There was additional evidence to suggest that the suppression of IGF-II can reduce tumour size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumour progression.

Conclusion: IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.

Original language	English
Pages (from-to)	497–528
Number of pages	32
Journal	Cancer Causes and Control
Volume	28
Issue number	6
Early online date	30 Mar 2017
DOIs	https://doi.org/10.1007/s10552-017-0883-1
Publication status	Published - Jun 2017

Research Groups and Themes

ICEP
Bristol Population Health Science Institute

Keywords

Prostate Cancer
insulin-like growth factors
milk
mechanistic pathway
systematic review
meta-analysis

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1007/s10552-017-0883-1

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NIHR BRC BEI
Sterne, J. A. C. (Principal Investigator)
1/04/17 → 31/03/22
Project: Research, Parent
NIHR BRC Nutrition
Ness, A. R. (Principal Investigator)
1/04/17 → 31/03/22
Project: Research, Parent
MRC UoB UNITE Unit - Programme 1
Davey Smith, G. (Principal Investigator)
1/06/13 → 31/03/18
Project: Research

Professor Sarah J Lewis
- S.J.Lewisbristol.acuk
- Bristol Medical School (PHS) - Professor of Molecular Epidemiology
- Bristol Population Health Science Institute
- MRC Integrative Epidemiology Unit
- Cancer
Person: Academic , Member

Cite this

Harrison, S., Lennon, R., Holly, J. M. P., Higgins, J., Gardner, M. P., Perks, C., Gaunt, T., Tan, V., Borwick, C., Emmett, P., Jeffreys, M., Northstone, K., Rinaldi, S., Thomas, S., Turner, S., Pease, A., Vilenchik, V., Martin, R., & Lewis, S. (2017). Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis. Cancer Causes and Control, 28(6), 497–528. https://doi.org/10.1007/s10552-017-0883-1

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title = "Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis",

abstract = "Purpose: To establish whether the association between milk intake and prostate cancer operates via the insulin-like growth factor (IGF) pathway (including IGF-I, IGF-II, IGFBP-1, IGFBP-2 and IGFBP-3).Methods: Systematic review, collating data from all relevant studies examining associations of milk with IGF, and those examining associations of IGF with prostate cancer risk and progression. Data were extracted from experimental and observational studies conducted in either humans or animals, and analysed using meta-analysis where possible, with summary data presented otherwise.Results: One hundred and seventy two studies met inclusion criteria: 31 examining the milk-IGF relationship; 132 examining the IGF-prostate cancer relationship in humans; and 10 animal studies examining the IGF-prostate cancer relationship. There was moderate evidence that circulating IGF-I and IGFBP-3 increase with milk (and dairy protein) intake (an estimated standardised effect size of 0.10 SD increase in IGF-I and 0.05 SD in IGFBP-3 per 1 SD increase in milk intake). There was moderate evidence that prostate cancer risk increased with IGF-I (Random effects meta-analysis OR per SD increase in IGF-I: 1.09; 95% CI: 1.03, 1.16; N = 51 studies) and decreased with IGFBP-3 (OR: 0.90; 0.83, 0.98; N = 39 studies), but not with other growth factors. The IGFBP-3 -202A/C single nucleotide polymorphism was positively associated with prostate cancer (pooled OR for A/C vs AA =1.22; 95% CI: 0.84, 1.79; OR for C/C vs AA = 1.51; 1.03, 2.21, N = 8 studies). No strong associations were observed for IGF-II, IGFBP-1 or IGFBP-2 with either milk intake or prostate cancer risk. There was little consistency within the data extracted from the small number of animal studies. There was additional evidence to suggest that the suppression of IGF-II can reduce tumour size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumour progression.Conclusion: IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.",

keywords = "Prostate Cancer, insulin-like growth factors, milk, mechanistic pathway, systematic review, meta-analysis",

author = "Sean Harrison and Rosie Lennon and Holly, {Jeffrey M P} and Julian Higgins and Gardner, {Mike P} and Claire Perks and Tom Gaunt and Vanessa Tan and Catherine Borwick and Pauline Emmett and Mona Jeffreys and Kate Northstone and Sabina Rinaldi and Stephen Thomas and Suzanne Turner and Anna Pease and Vicky Vilenchik and Richard Martin and Sarah Lewis",

year = "2017",

month = jun,

doi = "10.1007/s10552-017-0883-1",

language = "English",

volume = "28",

pages = "497–528",

journal = "Cancer Causes and Control",

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publisher = "Springer International Publishing AG",

number = "6",

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Harrison, S, Lennon, R, Holly, JMP, Higgins, J, Gardner, MP, Perks, C , Gaunt, T , Tan, V, Borwick, C, Emmett, P, Jeffreys, M, Northstone, K, Rinaldi, S, Thomas, S, Turner, S, Pease, A, Vilenchik, V, Martin, R & Lewis, S 2017, 'Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis', Cancer Causes and Control, vol. 28, no. 6, pp. 497–528. https://doi.org/10.1007/s10552-017-0883-1

Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis. / Harrison, Sean; Lennon, Rosie; Holly, Jeffrey M P et al.
In: Cancer Causes and Control, Vol. 28, No. 6, 06.2017, p. 497–528.

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

TY - JOUR

T1 - Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis

AU - Harrison, Sean

AU - Lennon, Rosie

AU - Holly, Jeffrey M P

AU - Higgins, Julian

AU - Gardner, Mike P

AU - Perks, Claire

AU - Gaunt, Tom

AU - Tan, Vanessa

AU - Borwick, Catherine

AU - Emmett, Pauline

AU - Jeffreys, Mona

AU - Northstone, Kate

AU - Rinaldi, Sabina

AU - Thomas, Stephen

AU - Turner, Suzanne

AU - Pease, Anna

AU - Vilenchik, Vicky

AU - Martin, Richard

AU - Lewis, Sarah

PY - 2017/6

Y1 - 2017/6

N2 - Purpose: To establish whether the association between milk intake and prostate cancer operates via the insulin-like growth factor (IGF) pathway (including IGF-I, IGF-II, IGFBP-1, IGFBP-2 and IGFBP-3).Methods: Systematic review, collating data from all relevant studies examining associations of milk with IGF, and those examining associations of IGF with prostate cancer risk and progression. Data were extracted from experimental and observational studies conducted in either humans or animals, and analysed using meta-analysis where possible, with summary data presented otherwise.Results: One hundred and seventy two studies met inclusion criteria: 31 examining the milk-IGF relationship; 132 examining the IGF-prostate cancer relationship in humans; and 10 animal studies examining the IGF-prostate cancer relationship. There was moderate evidence that circulating IGF-I and IGFBP-3 increase with milk (and dairy protein) intake (an estimated standardised effect size of 0.10 SD increase in IGF-I and 0.05 SD in IGFBP-3 per 1 SD increase in milk intake). There was moderate evidence that prostate cancer risk increased with IGF-I (Random effects meta-analysis OR per SD increase in IGF-I: 1.09; 95% CI: 1.03, 1.16; N = 51 studies) and decreased with IGFBP-3 (OR: 0.90; 0.83, 0.98; N = 39 studies), but not with other growth factors. The IGFBP-3 -202A/C single nucleotide polymorphism was positively associated with prostate cancer (pooled OR for A/C vs AA =1.22; 95% CI: 0.84, 1.79; OR for C/C vs AA = 1.51; 1.03, 2.21, N = 8 studies). No strong associations were observed for IGF-II, IGFBP-1 or IGFBP-2 with either milk intake or prostate cancer risk. There was little consistency within the data extracted from the small number of animal studies. There was additional evidence to suggest that the suppression of IGF-II can reduce tumour size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumour progression.Conclusion: IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.

AB - Purpose: To establish whether the association between milk intake and prostate cancer operates via the insulin-like growth factor (IGF) pathway (including IGF-I, IGF-II, IGFBP-1, IGFBP-2 and IGFBP-3).Methods: Systematic review, collating data from all relevant studies examining associations of milk with IGF, and those examining associations of IGF with prostate cancer risk and progression. Data were extracted from experimental and observational studies conducted in either humans or animals, and analysed using meta-analysis where possible, with summary data presented otherwise.Results: One hundred and seventy two studies met inclusion criteria: 31 examining the milk-IGF relationship; 132 examining the IGF-prostate cancer relationship in humans; and 10 animal studies examining the IGF-prostate cancer relationship. There was moderate evidence that circulating IGF-I and IGFBP-3 increase with milk (and dairy protein) intake (an estimated standardised effect size of 0.10 SD increase in IGF-I and 0.05 SD in IGFBP-3 per 1 SD increase in milk intake). There was moderate evidence that prostate cancer risk increased with IGF-I (Random effects meta-analysis OR per SD increase in IGF-I: 1.09; 95% CI: 1.03, 1.16; N = 51 studies) and decreased with IGFBP-3 (OR: 0.90; 0.83, 0.98; N = 39 studies), but not with other growth factors. The IGFBP-3 -202A/C single nucleotide polymorphism was positively associated with prostate cancer (pooled OR for A/C vs AA =1.22; 95% CI: 0.84, 1.79; OR for C/C vs AA = 1.51; 1.03, 2.21, N = 8 studies). No strong associations were observed for IGF-II, IGFBP-1 or IGFBP-2 with either milk intake or prostate cancer risk. There was little consistency within the data extracted from the small number of animal studies. There was additional evidence to suggest that the suppression of IGF-II can reduce tumour size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumour progression.Conclusion: IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.

KW - Prostate Cancer

KW - insulin-like growth factors

KW - milk

KW - mechanistic pathway

KW - systematic review

KW - meta-analysis

U2 - 10.1007/s10552-017-0883-1

DO - 10.1007/s10552-017-0883-1

M3 - Article (Academic Journal)

C2 - 28361446

SN - 0957-5243

VL - 28

SP - 497

EP - 528

JO - Cancer Causes and Control

JF - Cancer Causes and Control

IS - 6

ER -

Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)? A systematic review and meta-analysis

Abstract

Research Groups and Themes

Keywords

UN SDGs

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Projects

NIHR BRC BEI

NIHR BRC Nutrition

MRC UoB UNITE Unit - Programme 1

Profiles

Professor Sarah J Lewis

Cite this