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Longitudinal trajectories of lifetime body shape and prostate cancer angiogenesis

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Abstract

Angiogenesis potentially underlies the pathway between excess adiposity and prostate carcinogenesis. This study examined the association between lifetime body shape trajectories and prostate cancer angiogenesis. 521 prostate cancer patients who underwent prostatectomy or transurethral resection between 1986 and 2000 were enrolled from the Health Professionals Follow-up Study. Cancers were immunostained and quantitated for cancer vessel regularity, diameter, area, and density, and composite angiogenesis (factor analysis). To identify distinct groups of body shape change, we conducted group-based trajectory modeling. We used multivariable linear regression to estimate the percentage difference in angiogenesis score and 95% confidence interval (CI) between body shape change trajectories during lifetime (age 5–60 years), early life (age 5–30 years), or later life (age 30–60 years). Compared to men with lifetime lean or medium body shape, higher angiogenesis scores were observed in men with moderate increase [percentage difference of 35% (95% CI 5–64)], marked increase [24% (95% CI − 2 to 51)], and constantly heavy with mild increase body shape [38% (95% CI 8–69)]. However, a lower angiogenesis score was noted in men with early-life marked increase (− 22%, 95% CI − 44 to 0) and stable medium body shape (− 14%, 95% CI − 40 to 12), compared to moderate increase body shape. Increased angiogenesis was also found for absolute weight gain from age 21–60 years. Lifetime body fatness accumulation, especially after age 21, was associated with increased prostate cancer angiogenesis, while weight gain in early-life adulthood was associated with lower cancer angiogenesis.

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Abbreviations

BMI:

Body mass index

OR:

Odds ratio

HPFS:

Health professionals follow-up study

PSA:

Prostate-specific antigen

AHEI:

Alternative healthy eating index dietary score

NSAID:

Non-steroidal anti-inflammatory drug

MET:

Metabolic equivalent task

OCC:

Odds of correct classification

CI:

Confidence interval

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Acknowledgements

We would like to thank the participants and staff of the Health Professionals Follow-Up Study for their valuable contributions as well as the following state cancer registries for their help: Alabama, Arizona, Arkansas, California, Colorado, Connecticut, Delaware, Florida, Georgia, Idaho, Illinois, Indiana, Iowa, Kentucky, Louisiana, Maine, Maryland, Massachusetts, Michigan, Nebraska, New Hampshire, New Jersey, New York, North Carolina, North Dakota, Ohio, Oklahoma, Oregon, Pennsylvania, Rhode Island, South Carolina, Tennessee, Texas, Virginia, Washington and Wyoming. The authors assume full responsibility for the analyses and interpretation of these data.

Funding

This work was supported by the Erik and Edith Fernström Foundation (2019-00424) and Svenska Läkaresällskapet (SLS-869891). The Health Professionals Follow-up Study is supported by U01 167552. This project was a partnership of the Dana-Farber/Harvard Cancer Center (NIH P30 006516) and The Ohio State University Comprehensive Cancer Center: NIH P30 CA016058.

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Authors and Affiliations

  1. Department of Nutrition, Harvard T.H. Chan School of Public Health, Room 371, Bldg. 2, 665 Huntington Avenue, Boston, MA, 02115, USA

    Qiao-Li Wang, Mingyang Song & Edward L. Giovannucci

  2. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Qiao-Li Wang, Mingyang Song, Lorelei A. Mucci & Edward L. Giovannucci

  3. Upper Gastrointestinal Surgery, Department of Molecular Medicine and Surgery, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden

    Qiao-Li Wang & Jesper Lagergren

  4. Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Room 821, Smith Building, 450 Brookline Avenue, Boston, MA, 02215, USA

    Qiao-Li Wang

  5. Clinical and Translational Epidemiology Unit and Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, USA

    Mingyang Song

  6. Division of Medical Oncology, Department of Internal Medicine, and the Comprehensive Cancer Center, The Ohio State University, Columbus, OH, USA

    Steven K. Clinton

  7. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Lorelei A. Mucci & Edward L. Giovannucci

  8. School of Cancer and Pharmaceutical Sciences, King’s College London, London, UK

    Jesper Lagergren

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  1. Qiao-Li Wang
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Contributions

Study concept and design: QLW and ELG; acquisition of data: SKC, LAM and ELG; data analysis: QLW; interpretation of results: all authors; drafting the manuscript: QLW; critical revision of the manuscript for valuable intellectual content: all authors; supervision: JL and ELG. All authors have approved the final version of the manuscript. The corresponding author attests that all listed authors meet authorship criteria and that no others meeting the criteria have been omitted.

Corresponding authors

Correspondence to Qiao-Li Wang or Edward L. Giovannucci.

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The study sponsors had no role in the study design, the data collection, analysis, and interpretation, the writing of the report, or the decision to submit the manuscript for publication. The authors declare that they have no conflict of interest.

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The study protocol was approved by the institutional review boards of the Brigham and Women’s Hospital and Harvard T.H. Chan School of Public Health, and those of participating registries as required.

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Wang, QL., Song, M., Clinton, S.K. et al. Longitudinal trajectories of lifetime body shape and prostate cancer angiogenesis. Eur J Epidemiol 37, 261–270 (2022). https://doi.org/10.1007/s10654-021-00838-1

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