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; Jeff Holly; Julian P T Higgins; Mike Gardner; Claire Perks; Tom Gaunt; Vanessa Tan; Cath Borwick; Pauline Emmet; Mona Jeffreys; Kate Northstone; Sabina Rinaldi; Stephen Thomas; Suzanne D Turner; Anna Pease; Vicky Vilenchick; Richard M Martin; Sarah J 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, Jeff Holly, Julian P T Higgins, Mike Gardner, Claire Perks, Tom Gaunt, Vanessa Tan, Cath Borwick, Pauline Emmet, Mona Jeffreys, Kate Northstone, Sabina Rinaldi, Stephen Thomas, Suzanne D Turner, Anna Pease, Vicky Vilenchick, Richard M Martin, Sarah J Lewis

Applied Health Research

Research output: Contribution to journal › Review article › peer-review

40 Citations (Scopus)

135 Downloads (Pure)

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 analyzed using meta-analysis where possible, with summary data presented otherwise.

RESULTS: One hundred and seventy-two studies met the 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 standardized 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 tumor size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumor 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 & Control
Volume	28
Issue number	6
DOIs	https://doi.org/10.1007/s10552-017-0883-1
Publication status	Published - 30 Mar 2017

Keywords

Animals
Disease Progression
Humans
Insulin-Like Growth Factor Binding Protein 1/metabolism
Insulin-Like Growth Factor Binding Protein 2/metabolism
Insulin-Like Growth Factor Binding Protein 3/metabolism
Insulin-Like Growth Factor I/metabolism
Insulin-Like Growth Factor II/metabolism
Male
Milk/adverse effects
Prostate/metabolism
Prostatic Neoplasms/metabolism
Risk

UN SDGs

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

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Cite this

Harrison, S., Lennon, R., Holly, J., Higgins, J. P. T., Gardner, M., Perks, C., Gaunt, T., Tan, V., Borwick, C., Emmet, P., Jeffreys, M., Northstone, K., Rinaldi, S., Thomas, S., Turner, S. D., Pease, A., Vilenchick, V., Martin, R. M., & Lewis, S. J. (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 & 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 analyzed using meta-analysis where possible, with summary data presented otherwise.RESULTS: One hundred and seventy-two studies met the 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 standardized 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 tumor size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumor progression.CONCLUSION: IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.",

keywords = "Animals, Disease Progression, Humans, Insulin-Like Growth Factor Binding Protein 1/metabolism, Insulin-Like Growth Factor Binding Protein 2/metabolism, Insulin-Like Growth Factor Binding Protein 3/metabolism, Insulin-Like Growth Factor I/metabolism, Insulin-Like Growth Factor II/metabolism, Male, Milk/adverse effects, Prostate/metabolism, Prostatic Neoplasms/metabolism, Risk",

author = "Sean Harrison and Rosie Lennon and Jeff Holly and Higgins, {Julian P T} and Mike Gardner and Claire Perks and Tom Gaunt and Vanessa Tan and Cath Borwick and Pauline Emmet and Mona Jeffreys and Kate Northstone and Sabina Rinaldi and Stephen Thomas and Turner, {Suzanne D} and Anna Pease and Vicky Vilenchick and Martin, {Richard M} and Lewis, {Sarah J}",

year = "2017",

month = mar,

day = "30",

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

language = "English",

volume = "28",

pages = "497--528",

journal = "Cancer Causes & Control",

issn = "0957-5243",

publisher = "Springer",

number = "6",

}

Harrison, S, Lennon, R, Holly, J, Higgins, JPT, Gardner, M, Perks, C, Gaunt, T, Tan, V, Borwick, C, Emmet, P, Jeffreys, M, Northstone, K, Rinaldi, S, Thomas, S, Turner, SD, Pease, A, Vilenchick, V, Martin, RM & Lewis, SJ 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 & Control, vol. 28, no. 6, pp. 497-528. https://doi.org/10.1007/s10552-017-0883-1

TY - JOUR

T1 - Does milk intake promote prostate cancer initiation or progression via effects on insulin-like growth factors (IGFs)?

T2 - a systematic review and meta-analysis

AU - Harrison, Sean

AU - Lennon, Rosie

AU - Holly, Jeff

AU - Higgins, Julian P T

AU - Gardner, Mike

AU - Perks, Claire

AU - Gaunt, Tom

AU - Tan, Vanessa

AU - Borwick, Cath

AU - Emmet, Pauline

AU - Jeffreys, Mona

AU - Northstone, Kate

AU - Rinaldi, Sabina

AU - Thomas, Stephen

AU - Turner, Suzanne D

AU - Pease, Anna

AU - Vilenchick, Vicky

AU - Martin, Richard M

AU - Lewis, Sarah J

PY - 2017/3/30

Y1 - 2017/3/30

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 analyzed using meta-analysis where possible, with summary data presented otherwise.RESULTS: One hundred and seventy-two studies met the 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 standardized 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 tumor size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumor 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 analyzed using meta-analysis where possible, with summary data presented otherwise.RESULTS: One hundred and seventy-two studies met the 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 standardized 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 tumor size, and contradictory evidence with regards to the effect of IGFBP-3 suppression on tumor progression.CONCLUSION: IGF-I is a potential mechanism underlying the observed associations between milk intake and prostate cancer risk.

KW - Animals

KW - Disease Progression

KW - Humans

KW - Insulin-Like Growth Factor Binding Protein 1/metabolism

KW - Insulin-Like Growth Factor Binding Protein 2/metabolism

KW - Insulin-Like Growth Factor Binding Protein 3/metabolism

KW - Insulin-Like Growth Factor I/metabolism

KW - Insulin-Like Growth Factor II/metabolism

KW - Male

KW - Milk/adverse effects

KW - Prostate/metabolism

KW - Prostatic Neoplasms/metabolism

KW - Risk

U2 - 10.1007/s10552-017-0883-1

DO - 10.1007/s10552-017-0883-1

M3 - Review article

C2 - 28361446

SN - 0957-5243

VL - 28

SP - 497

EP - 528

JO - Cancer Causes & Control

JF - Cancer Causes & Control

IS - 6

ER -