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

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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 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.

Electronic supplementary material

The online version of this article (doi:10.1007/s10552-017-0883-1) contains supplementary material, which is available to authorized users.

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Most cited references 173

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Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study.

J M Chan, M Stampfer, E Giovannucci … (1998)

Insulin-like growth factor-I (IGF-I) is a mitogen for prostate epithelial cells. To investigate associations between plasma IGF levels and prostate cancer risk, a nested case-control study within the Physicians' Health Study was conducted on prospectively collected plasma from 152 cases and 152 controls. A strong positive association was observed between IGF-I levels and prostate cancer risk. Men in the highest quartile of IGF-I levels had a relative risk of 4.3 (95 percent confidence interval 1.8 to 10.6) compared with men in the lowest quartile. This association was independent of baseline prostate-specific antigen levels. Identification of plasma IGF-I as a predictor of prostate cancer risk may have implications for risk reduction and treatment.

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Methods for summarizing the risk associations of quantitative variables in epidemiologic studies in a consistent form.

S. Thompson, G Chêne (1996)

A major problem in reviewing the published results of different epidemiologic studies of the relation between a quantitative variable and the risk of disease is that the results are presented in many different ways. The purpose of this paper is to exemplify methods by which results expressed either as risks (or rates) according to quantlle groups of the quantitative variable or as results derived from a logistic regression analysis can be reexpressed in a uniform manner, as a mean difference in the quantitative variable between the cases of disease and the other subjects in the study. An important assumption of the methods is that the quantitative variable has an approximately normal distribution, and a way of investigating the appropriateness of this assumption is given. The methods can be applied to both prospective and case-control studies and are exemplified by a number of studies of serum albumin concentrations and mortality. In some applications, these methods can be used as a precursor to formal meta-analysis, for example, when differential control of potential confounding factors is not a problem. At the least, the methods can be useful either in quantitatively reviewing published studies before undertaking new research or in putting the results of a new study into the context of previously published ones.

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Insulin-like growth factors, their binding proteins, and prostate cancer risk: analysis of individual patient data from 12 prospective studies.

Elizabeth A. Platz, W Hsing-Hsien, Naomi Allen … (2008)

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. To assess the association between levels of IGFs and IGFBPs and the subsequent risk for prostate cancer. Studies identified in PubMed, Web of Science, and CancerLit. 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. 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. 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. 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. High circulating IGF-I concentrations are associated with a moderately increased risk for prostate cancer.

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Author and article information

Contributors

Sarah J. Lewis: s.j.lewis@bristol.ac.uk

Journal

Journal ID (nlm-ta): Cancer Causes Control

Journal ID (iso-abbrev): Cancer Causes Control

Title: Cancer Causes & Control

Publisher: Springer International Publishing (Cham )

ISSN (Print): 0957-5243

ISSN (Electronic): 1573-7225

Publication date (Electronic): 30 March 2017

Publication date PMC-release: 30 March 2017

Publication date (Print): 2017

Volume: 28

Issue: 6

Pages: 497-528

Affiliations

[1 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, School of Social and Community Medicine, , University of Bristol, ; Bristol, UK

[2 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, MRC Integrative Epidemiology Unit (IEU), , University of Bristol, ; Bristol, UK

[3 ]ISNI 0000 0004 0417 1173, GRID grid.416201.0, IGFs & Metabolic Endocrinology Group, School of Clinical Sciences at North Bristol, , Southmead Hospital, ; BS10 5NB Bristol, UK

[4 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Nuffield Department of Population Health, , University of Oxford, ; Oxford, UK

[5 ]ISNI 0000 0001 0807 5670, GRID grid.5600.3, , Cardiff University, ; Cardiff, UK

[6 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, CLAHRC West, , University of Bristol, ; Bristol, UK

[7 ]ISNI 0000000405980095, GRID grid.17703.32, , International Agency for Research on Cancer, ; Lyon, France

[8 ]ISNI 0000 0004 1936 7603, GRID grid.5337.2, School of Oral and Dental Sciences,, , University of Bristol, ; Bristol, UK

[9 ]ISNI 0000000121885934, GRID grid.5335.0, Department of Pathology, , University of Cambridge, ; Cambridge, UK

[10 ]ISNI 0000 0004 0380 7336, GRID grid.410421.2, National Institute for Health Research Biomedical Research Unit in Nutrition, Diet and Lifestyle, , University Hospitals Bristol NHS Foundation Trust and the University of Bristol, ; BS2 8AE Bristol, UK

Author information

Sean Harrison http://orcid.org/0000-0002-7966-0700

Article

Publisher ID: 883

DOI: 10.1007/s10552-017-0883-1

PMC ID: 5400803

PubMed ID: 28361446

SO-VID: 6e3eaf86-7915-47ca-aacd-20fdd4e5fb3e

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

History

Date received : 10 May 2016

Date accepted : 10 March 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100000321, World Cancer Research Fund;

Award ID: RFA 2012/620

Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;

Award ID: 102432/Z/13/Z

Award Recipient : Sean Harrison

Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;

Award ID: MC_UU_12013/1

Award ID: MC_UU_12013/2

Funded by: FundRef http://dx.doi.org/10.13039/501100000289, Cancer Research UK;

Award ID: C18281/A19169

Funded by: FundRef http://dx.doi.org/10.13039/501100000272, National Institute for Health Research;

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: prostate cancer,insulin-like growth factors,milk,mechanistic pathway,systematic review,meta-analysis

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ScienceOpen disciplines: Oncology & Radiotherapy

Keywords: prostate cancer, insulin-like growth factors, milk, mechanistic pathway, systematic review, meta-analysis

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

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Karger: Oncology

Most cited references 173

Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study.

Methods for summarizing the risk associations of quantitative variables in epidemiologic studies in a consistent form.

Insulin-like growth factors, their binding proteins, and prostate cancer risk: analysis of individual patient data from 12 prospective studies.

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