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Joint exposure to smoking, excessive weight, and physical inactivity and survival of ovarian cancer patients, evidence from the Ovarian Cancer Association Consortium

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Abstract

Purpose

Previous epidemiologic studies have shown that smoking, obesity, and physical inactivity are associated with poor survival following a diagnosis of ovarian cancer. Yet, the combined relationship of these unfavorable lifestyle factors on ovarian cancer survival has not been sufficiently investigated.

Methods

Using data pooled from 13 studies, we examined the associations between combined exposures to smoking, overweight/obesity weight, and physical inactivity and overall survival (OS) as well as progression-free survival (PFS) among women diagnosed with invasive epithelial ovarian carcinoma (n = 7,022). Using age- and stage-adjusted Cox proportional hazards regression models, we estimated hazard ratios (HRs) and 95% confidence intervals (CIs) associated with joint exposure to these factors.

Results

Combined exposure to current smoking, overweight/obesity, and physical inactivity prior to diagnosis was associated with a significantly increased risk of mortality compared to women who never smoked, had normal body mass index (BMI), and were physically active (HR = 1.37; 95% CI 1.10–1.70). The association for a joint exposure to these factors exceeded that of each exposure individually. In fact, exposure to both current smoking and overweight/obesity, and current smoking and physical inactivity was also associated with increased risk of death (HR = 1.28; 95% CI 1.08–1.52, and HR = 1.26; 95% CI 1.04–1.54, respectively). The associations were of a similar magnitude when former smoking was assessed in combination with the other exposures and when excessive weight was limited to obesity only. No significant associations were observed between joint exposure to any of these factors and PFS.

Conclusions

Joint exposure to smoking, excessive weight, and physical inactivity may negatively impact survival of ovarian cancer patients. These results suggest the importance of examining the combined effect of lifestyle factors on ovarian cancer patients’ survival.

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Acknowledgments

The Australian Ovarian Cancer Study Management Group (D. Bowtell, G. Chenevix-Trench, A. deFazio, D. Gertig, A. Green, P. Webb) and ACS Investigators (A. Green, P. Parsons, N. Hayward, P. Webb, D. Whiteman) thank all the clinical and scientific collaborators (see http://www.aocstudy.org/) and the women for their contribution. The cooperation of the 32 Connecticut hospitals, including Stamford Hospital, in allowing patient access, is gratefully acknowledged (CON). This study was approved by the State of Connecticut Department of Public Health Human Investigation Committee. Certain data used in this study were obtained from the Connecticut Tumor Registry in the Connecticut Department of Public Health. The authors assume full responsibility for analyses and interpretation of these data.

Funding

A.N. Minlikeeva was supported by National Cancer Institute (NCI) NIH/NCI 4R25CA113951 and NIH/NCI P50CA159981; K.B. Moysich was supported by NIH/NCI (2R25CA113951, R01CA095023, R01CA126841, P50CA159981) and the Roswell Park Alliance Foundation; K. Odunsi was supported by the Roswell Park Alliance Foundation and NIH/NCI P50CA159981; J.B. Szender, K. Starbuck, and P.C. Mayor were supported by the NIH T32 training grant T32CA108456; S.J. Jordan was supported by National Health & Medical Research Council of Australia NHMRC APP1061341, C.M. Nagle by NHMRC APP1073898, and PM Webb by NHMRC APP1043134; AUS was supported by U.S. Army Medical Research and Materiel Command (DAMD17-01-1-0729), NHMRC (199600 and 400281), Cancer Councils of New South Wales, Victoria, Queensland, South Australia and Tasmania, and the Cancer Foundation of Western Australia; CON was supported by NIH (R01-CA074850 and R01-CA080742); DOV was supported by NIH (R01-CA112523 and R01-CA87538); HAW was supported by NIH (R01-CA58598, N01-CN-55424 and N01-PC-67001); HOP was supported by Department of Defense (DOD): DAMD17-02-1-0669 and NIH/NCI (K07-CA080668, R01-CA95023, P50-CA159981, and R01-CA126841); JPN was supported by Grant-in-Aid for the Third Term Comprehensive 10-Year Strategy for Cancer Control from the Ministry of Health, Labour and Welfare; MAC and MAY were supported by NIH (R01-CA122443, P30-CA15083, P50-CA136393), Mayo Foundation, Minnesota Ovarian Cancer Alliance, and Fred C. and Katherine B; MAL was supported by NIH/NCI (R01-CA61107), Danish Cancer Society (Research Grant 94 222 52), and the Mermaid I project; NEC was supported by NIH (R01-CA54419 and P50-CA105009) and DOD (W81XWH-10-1-02802); NJO was supported by NIH/NCI (K07 CA095666, K22-CA138563, and P30-CA072720) and the Cancer Institute of New Jersey; OPL was supported by National Health and Medical Research Council (NHMRC) of Australia (APP1025142, APP1120431); USC was supported by P01CA17054, P30CA14089, R01CA61132, N01PC67010, R03CA113148, R03CA115195, N01CN025403, and California Cancer Research Program (00-01389V-20170, 2II0200).

Author information

Authors and Affiliations

  1. Department of Cancer Prevention and Control, Roswell Park Comprehensive Cancer Center, A-352 Carlton House, Roswell Park Comprehensive Cancer Center, Elm and Carlton Streets, Buffalo, NY, 14263, USA

    Albina N. Minlikeeva, Rikki Cannioto, Hani Almohanna & Kirsten B. Moysich

  2. Department of Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Copenhagen, Denmark

    Allan Jensen, Susanne K. Kjaer & Estrid Høgdall

  3. Deparment of Gynaecology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark

    Susanne K. Kjaer

  4. Population Health Department, QIMR Berghofer Medical Research Institute, Brisbane, QLD, Australia

    Susan J. Jordan, Christina M. Nagle & Penelope M. Webb

  5. The University of Queensland, School of Public Health, Herston, QLD, Australia

    Susan J. Jordan, Christina M. Nagle & Penelope M. Webb

  6. Department of Human Genetics, University of Pittsburgh Graduate School of Public Health, and UPMC Hillman Cancer Center, Pittsburgh, PA, USA

    Brenda Diergaarde

  7. START Center for Cancer Care, San Antonio, TX, USA

    J. Brian Szender

  8. Department of Surgery, Division of Gynecologic Oncology, Roswell Park Comprehensive Cancer Center, Buffalo, NY, USA

    Kunle Odunsi, Paul Mayor & Kirsten Starbuck

  9. Center of Immunotherapy, Roswell Park Comprehensive Cancer Center, Buffalo, NY, USA

    Kunle Odunsi & Emese Zsiros

  10. Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA

    Elisa V. Bandera

  11. Obstetrics and Gynecology Epidemiology Center, Brigham and Women’s Hospital, Boston, MA, USA

    Daniel W. Cramer & Kathryn L. Terry

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

    Daniel W. Cramer & Kathryn L. Terry

  13. Department of Epidemiology, The Geisel School of Medicine, Dartmouth College, Hanover, NH, USA

    Jennifer A. Doherty

  14. Department of Gynecological Oncology, Westmead Hospital and the Westmead Institute for Medical Research, The University of Sydney, Sydney, NSW, Australia

    Anna DeFazio

  15. Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA

    Robert Edwards & Francesmary Modugno

  16. Ovarian Cancer Center of Excellence, Womens Cancer Research Program, Magee-Womens Research Institute and University of Pittsburgh Cancer Institute, Pittsburgh, PA, USA

    Robert Edwards & Francesmary Modugno

  17. Division of Epidemiology, Department of Health Science Research, Mayo Clinic, Rochester, MN, USA

    Ellen L. Goode

  18. Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA

    Marc T. Goodman

  19. Department of Pathology, Herlev and Gentofte Hospital, University of Copenhagen, Copenhagen, Denmark

    Estrid Høgdall

  20. Division of Molecular Medicine and Clinical Epidemiology, Aichi Cancer Center Research Institute, Nagoya, Japan

    Keitary Matsuo

  21. Department of Epidemiology, Nagoya University Graduate School of Medicine, Nagoya, Japan

    Keitary Matsuo

  22. Department of Gynecological Oncology, Aichi Cancer Center Hospital, Nagoya, Aichi, Japan

    Mika Mizuno

  23. School of Public Health, The University of Texas, Houston, TX, USA

    Roberta B. Ness

  24. New Jersey Department of Health and Senior Services, New Jersey State Cancer Registry, Trenton, NJ, USA

    Lisa E. Paddock

  25. Rutgers Cancer Institute, New Brunswick, NJ, USA

    Lisa E. Paddock

  26. Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, MI, USA

    Celeste L. Pearce

  27. Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Los Angeles, CA, USA

    Celeste L. Pearce & Anna H. Wu

  28. Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT, USA

    Harvey A. Risch

  29. Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Mary Anne Rossing

  30. Department of Epidemiology, University of Pittsburgh, Pittsburgh, PA, USA

    Francesmary Modugno

  31. Department of Immunology, Roswell Park Comprehensive Cancer Center, Buffalo, NY, USA

    Kirsten B. Moysich

Authors
  1. Albina N. Minlikeeva
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  2. Rikki Cannioto
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  3. Allan Jensen
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  4. Susanne K. Kjaer
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  5. Susan J. Jordan
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  6. Brenda Diergaarde
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  7. J. Brian Szender
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  8. Kunle Odunsi
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  9. Hani Almohanna
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  10. Paul Mayor
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  11. Kirsten Starbuck
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  12. Emese Zsiros
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  13. Elisa V. Bandera
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  14. Daniel W. Cramer
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  15. Jennifer A. Doherty
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  16. Anna DeFazio
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  17. Robert Edwards
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  18. Ellen L. Goode
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  19. Marc T. Goodman
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  20. Estrid Høgdall
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  21. Keitary Matsuo
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  22. Mika Mizuno
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  23. Christina M. Nagle
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  24. Roberta B. Ness
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  25. Lisa E. Paddock
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the Australian Ovarian Cancer Study Group

the Ovarian Cancer Association Consortium

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Correspondence to Kirsten B. Moysich.

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Minlikeeva, A.N., Cannioto, R., Jensen, A. et al. Joint exposure to smoking, excessive weight, and physical inactivity and survival of ovarian cancer patients, evidence from the Ovarian Cancer Association Consortium. Cancer Causes Control 30, 537–547 (2019). https://doi.org/10.1007/s10552-019-01157-3

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