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Cancer Causes & Control

, Volume 30, Issue 5, pp 537–547 | Cite as

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

  • Albina N. Minlikeeva
  • Rikki Cannioto
  • Allan Jensen
  • Susanne K. Kjaer
  • Susan J. Jordan
  • Brenda Diergaarde
  • J. Brian Szender
  • Kunle Odunsi
  • Hani Almohanna
  • Paul Mayor
  • Kirsten Starbuck
  • Emese Zsiros
  • Elisa V. Bandera
  • Daniel W. Cramer
  • Jennifer A. Doherty
  • Anna DeFazio
  • the Australian Ovarian Cancer Study Group
  • Robert Edwards
  • Ellen L. Goode
  • Marc T. Goodman
  • Estrid Høgdall
  • Keitary Matsuo
  • Mika Mizuno
  • Christina M. Nagle
  • Roberta B. Ness
  • Lisa E. Paddock
  • Celeste L. Pearce
  • Harvey A. Risch
  • Mary Anne Rossing
  • Kathryn L. Terry
  • Anna H. Wu
  • Francesmary Modugno
  • Penelope M. Webb
  • Kirsten B. MoysichEmail author
  • the Ovarian Cancer Association Consortium
Original Paper
  • 70 Downloads

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.

Keywords

Smoking cigarettes Overweight Obesity Physical inactivity Ovarian cancer survival Prognosis 

Notes

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).

Compliance with ethical standards

Conflict of interest

No potential conflicts of interest were disclosed.

Supplementary material

10552_2019_1157_MOESM1_ESM.docx (35 kb)
Supplementary material 1 (DOCX 34 KB)

References

  1. 1.
    Jemal A, Ward EM, Johnson CJ, Cronin KA, Ma J, Ryerson B, Mariotto A, Lake AJ, Wilson R, Sherman RL, Anderson RN, Henley SJ, Kohler BA, Penberthy L, Feuer EJ, Weir HK (2017) Annual report to the nation on the status of cancer, 1975–2014, featuring survival. J Natl Cancer Inst 109:djx030CrossRefGoogle Scholar
  2. 2.
    Bookman MA (2012) First-line chemotherapy in epithelial ovarian cancer. Clin Obstet Gynecol 55:96–113CrossRefGoogle Scholar
  3. 3.
    SEER (2017) Cancer stat facts: ovarian cancerGoogle Scholar
  4. 4.
    I.W.G.o.t.E.o.C.R.t. (2012) Humans, personal habits and indoor combustions. Volume 100 E. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 100:1–538Google Scholar
  5. 5.
    World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report (2018) Body fatness and weight gain and the risk of cancerGoogle Scholar
  6. 6.
    Cannioto RA, LaMonte MJ, Kelemen LE, Risch HA, Eng KH, Minlikeeva AN, Hong CC, Szender JB, Sucheston-Campbell L, Joseph JM, Berchuck A, Chang-Claude J, Cramer DW, DeFazio A, Diergaarde B, Dörk T, Doherty JA, Edwards RP, Fridley BL, Friel G, Goode EL, Goodman MT, Hillemanns P, Hogdall E, Hosono S, Kelley JL, Kjaer SK, Klapdor R, Matsuo K, Odunsi K, Nagle CM, Olsen CM, Paddock LE, Pearce CL, Pike MC, Rossing MA, Schmalfeldt B, Segal BH, Szamreta EA, Thompson PJ, Tseng CC, Vierkant R, Schildkraut JM, Wentzensen N, Wicklund KG, Winham SJ, Wu AH, Modugno F, Ness RB, Jensen A, Webb PM, Terry K, Bandera EV, Moysich KB (2016) Recreational physical inactivity and mortality in women with invasive epithelial ovarian cancer: evidence from the Ovarian Cancer Association Consortium. Br J Cancer 115:95CrossRefGoogle Scholar
  7. 7.
    Praestegaard C, Jensen A, Jensen SM, Nielsen TS, Webb PM, Nagle CM, DeFazio A, Høgdall E, Rossing MA, Doherty JA, Wicklund KG, Goodman MT, Modugno F, Moysich K, Ness RB, Edwards R, Matsuo K, Hosono S, Goode EL, Winham SJ, Fridley BL, Cramer DW, Terry KL, Schildkraut JM, Berchuck A, Bandera EV, Paddock LE, Massuger LF, Wentzensen N, Pharoah P, Song H, Whittemore A, McGuire V, Sieh W, Rothstein J, Anton-Culver H, Ziogas A, Menon U, Gayther SA, Ramus SJ, Gentry-Maharaj A, Wu AH, Pearce CL, Pike M, Lee AW, Sutphen R, Chang-Claude J, Risch HA, Kjaer SK, Group AOCS, O.C.A. Consortium (2017) Cigarette smoking is associated with adverse survival among women with ovarian cancer: results from a pooled analysis of 19 studies. Int J Cancer 140:2422–2435CrossRefGoogle Scholar
  8. 8.
    Nagle CM, Dixon SC, Jensen A, Kjaer SK, Modugno F, deFazio A, Fereday S, Hung J, Johnatty SE, Fasching PA, Beckmann MW, Lambrechts D, Vergote I, Van Nieuwenhuysen E, Lambrechts S, Risch HA, Rossing MA, Doherty JA, Wicklund KG, Chang-Claude J, Goodman MT, Ness RB, Moysich K, Heitz F, du Bois A, Harter P, Schwaab I, Matsuo K, Hosono S, Goode EL, Vierkant RA, Larson MC, Fridley BL, Høgdall C, Schildkraut JM, Weber RP, Cramer DW, Terry KL, Bandera EV, Paddock L, Rodriguez-Rodriguez L, Wentzensen N, Yang HP, Brinton LA, Lissowska J, Høgdall E, Lundvall L, Whittemore A, McGuire V, Sieh W, Rothstein J, Sutphen R, Anton-Culver H, Ziogas A, Pearce CL, Wu AH, Webb PM, A.O.C.S. Group, O.C.A. Consortium (2015) Obesity and survival among women with ovarian cancer: results from the Ovarian Cancer Association Consortium. Br J Cancer 113:817–826CrossRefGoogle Scholar
  9. 9.
    Nagle CM, Bain CJ, Webb PM (2006) Cigarette smoking and survival after ovarian cancer diagnosis. Cancer Epidemiol Biomark Prev 15:2557–2560CrossRefGoogle Scholar
  10. 10.
    Protani MM, Nagle CM, Webb PM (2012) Obesity and ovarian cancer survival: a systematic review and meta-analysis. Cancer Prev Res (Phila) 5:901–910CrossRefGoogle Scholar
  11. 11.
    Bauer UE, Briss PA, Goodman RA, Bowman BA (2014) Prevention of chronic disease in the 21st century: elimination of the leading preventable causes of premature death and disability in the USA. Lancet 384:45–52CrossRefGoogle Scholar
  12. 12.
    Kjaerbye-Thygesen A, Frederiksen K, Høgdall EV, Glud E, Christensen L, Høgdall CK, Blaakaer J, Kjaer SK (2006) Smoking and overweight: negative prognostic factors in stage III epithelial ovarian cancer. Cancer Epidemiol Biomark Prev 15:798–803CrossRefGoogle Scholar
  13. 13.
    Faber MT, Kjaer SK, Dehlendorff C, Chang-Claude J, Andersen KK, Hogdall E, Webb PM, Jordan SJ, Rossing MA, Doherty JA, Lurie G, Thompson PJ, Carney ME, Goodman MT, Ness RB, Modugno F, Edwards RP, Bunker CH, Goode EL, Fridley BL, Vierkant RA, Larson MC, Schildkraut J, Cramer DW, Terry KL, Vitonis AF, Bandera EV, Olson SH, King M, Chandran U, Kiemeney LA, Massuger LF, van Altena AM, Vermeulen SH, Brinton L, Wentzensen N, Lissowska J, Yang HP, Moysich KB, Odunsi K, Kasza K, Odunsi-Akanji O, Song H, Pharaoh P, Shah M, Whittemore AS, McGuire V, Sieh W, Sutphen R, Menon U, Gayther SA, Ramus SJ, Gentry-Maharaj A, Pearce CL, Wu AH, Pike MC, Risch HA, Jensen A (2013) Cigarette smoking and risk of ovarian cancer: a pooled analysis of 21 case-control studies. Cancer Causes Control 24:989–1004CrossRefGoogle Scholar
  14. 14.
    Physical Status (1995) The use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 854:1–452Google Scholar
  15. 15.
    Cannioto R, LaMonte MJ, Risch HA, Hong CC, Sucheston-Campbell LE, Eng KH, Szender JB, Chang-Claude J, Schmalfeldt B, Klapdor R, Gower E, Minlikeeva AN, Zirpoli GR, Bandera EV, Berchuck A, Cramer D, Doherty JA, Edwards RP, Fridley BL, Goode EL, Goodman MT, Hogdall E, Hosono S, Jensen A, Jordan S, Kjaer SK, Matsuo K, Ness RB, Olsen CM, Olson SH, Pearce CL, Pike MC, Rossing MA, Szamreta EA, Thompson PJ, Tseng CC, Vierkant RA, Webb PM, Wentzensen N, Wicklund KG, Winham SJ, Wu AH, Modugno F, Schildkraut JM, Terry KL, Kelemen LE, Moysich KB, A.O.C.S. Group (2016) Chronic recreational physical inactivity and epithelial ovarian cancer risk: evidence from the Ovarian Cancer Association Consortium. Cancer Epidemiol Biomark Prev 25:1114–1124CrossRefGoogle Scholar
  16. 16.
    Schaal C, Chellappan SP (2014) Nicotine-mediated cell proliferation and tumor progression in smoking-related cancers. Mol Cancer Res 12:14–23CrossRefGoogle Scholar
  17. 17.
    Schuller HM (2012) Regulatory role of the alpha7nAChR in cancer. Curr Drug Targets 13:680–687CrossRefGoogle Scholar
  18. 18.
    Singh S, Pillai S, Chellappan S (2011) Nicotinic acetylcholine receptor signaling in tumor growth and metastasis. J Oncol 2011:456743CrossRefGoogle Scholar
  19. 19.
    Jeon SY, Go RE, Heo JR, Kim CW, Hwang KA, Choi KC (2016) Effects of cigarette smoke extracts on the progression and metastasis of human ovarian cancer cells via regulating epithelial-mesenchymal transition. Reprod Toxicol 65:1–10CrossRefGoogle Scholar
  20. 20.
    Kelemen LE, Warren GW, Koziak JM, Köbel M, Steed H (2016) Smoking may modify the association between neoadjuvant chemotherapy and survival from ovarian cancer. Gynecol Oncol 140:124–130CrossRefGoogle Scholar
  21. 21.
    Kim SJ, Rosen B, Fan I, Ivanova A, McLaughlin JR, Risch H, Narod SA, Kotsopoulos J (2017) Epidemiologic factors that predict long-term survival following a diagnosis of epithelial ovarian cancer. Br J Cancer 116:964–971CrossRefGoogle Scholar
  22. 22.
    Calle EE, Kaaks R (2004) Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer 4:579–591CrossRefGoogle Scholar
  23. 23.
    Renehan AG, Zwahlen M, Egger M (2015) Adiposity and cancer risk: new mechanistic insights from epidemiology. Nat Rev Cancer 15:484–498CrossRefGoogle Scholar
  24. 24.
    Au-Yeung G, Webb PM, DeFazio A, Fereday S, Bressel M, Mileshkin L (2014) Impact of obesity on chemotherapy dosing for women with advanced stage serous ovarian cancer in the Australian Ovarian Cancer Study (AOCS). Gynecol Oncol 133:16–22CrossRefGoogle Scholar
  25. 25.
    McTiernan A (2008) Mechanisms linking physical activity with cancer. Nat Rev Cancer 8:205–211CrossRefGoogle Scholar
  26. 26.
    Ezzati M, Lopez AD (2004) Regional, disease specific patterns of smoking-attributable mortality in 2000. Tob Control 13:388–395CrossRefGoogle Scholar
  27. 27.
    Petersen KE, Johnsen NF, Olsen A, Albieri V, Olsen LK, Dragsted LO, Overvad K, Tjønneland A, Egeberg R (2015) The combined impact of adherence to five lifestyle factors on all-cause, cancer and cardiovascular mortality: a prospective cohort study among Danish men and women. Br J Nutr 113:849–858CrossRefGoogle Scholar
  28. 28.
    Merritt MA, Green AC, Nagle CM, Webb PM (2008) Talcum powder, chronic pelvic inflammation and NSAIDs in relation to risk of epithelial ovarian cancer. Int J Cancer 122:170–176CrossRefGoogle Scholar
  29. 29.
    Risch HA, Bale AE, Beck PA, Zheng W (2006) PGR + 331 A/G and increased risk of epithelial ovarian cancer. Cancer Epidemiol Biomark Prev 15:1738–1741CrossRefGoogle Scholar
  30. 30.
    Bodelon C, Cushing-Haugen KL, Wicklund KG, Doherty JA, Rossing MA (2012) Sun exposure and risk of epithelial ovarian cancer. Cancer Causes Control 23:1985–1994CrossRefGoogle Scholar
  31. 31.
    Rossing MA, Cushing-Haugen KL, Wicklund KG, Doherty JA, Weiss NS (2007) Menopausal hormone therapy and risk of epithelial ovarian cancer. Cancer Epidemiol Biomark Prev 16:2548–2556CrossRefGoogle Scholar
  32. 32.
    Goodman MT, Lurie G, Thompson PJ, McDuffie KE, Carney ME (2008) Association of two common single-nucleotide polymorphisms in the CYP19A1 locus and ovarian cancer risk. Endocr Relat Cancer 15:1055–1060CrossRefGoogle Scholar
  33. 33.
    Lurie G, Wilkens LR, Thompson PJ, McDuffie KE, Carney ME, Terada KY, Goodman MT (2008) Combined oral contraceptive use and epithelial ovarian cancer risk: time-related effects. Epidemiology 19:237–243CrossRefGoogle Scholar
  34. 34.
    Lo-Ciganic WH, Zgibor JC, Bunker CH, Moysich KB, Edwards RP, Ness RB (2012) Aspirin, nonaspirin nonsteroidal anti-inflammatory drugs, or acetaminophen and risk of ovarian cancer. Epidemiology 23:311–319CrossRefGoogle Scholar
  35. 35.
    Hamajima N, Matsuo K, Saito T, Hirose K, Inoue M, Takezaki T, Kuroishi T, Tajima K (2001) Gene-environment interactions and polymorphism studies of cancer risk in the hospital-based epidemiologic research program at Aichi Cancer Center II (HERPACC-II). Asian Pac J Cancer Prev 2:99–107Google Scholar
  36. 36.
    Goode EL, Chenevix-Trench G, Hartmann LC, Fridley BL, Kalli KR, Vierkant RA, Larson MC, White KL, Keeney GL, Oberg TN, Cunningham JM, Beesley J, Johnatty SE, Chen X, Goodman KE, Armasu SM, Rider DN, Sicotte H, Schmidt MM, Elliott EA, Høgdall E, Kjær SK, Fasching PA, Ekici AB, Lambrechts D, Despierre E, Høgdall C, Lundvall L, Karlan BY, Gross J, Brown R, Chien J, Duggan DJ, Tsai YY, Phelan CM, Kelemen LE, Peethambaram PP, Schildkraut JM, Shridhar V, Sutphen R, Couch FJ, Sellers TA, O.C.A. Consortium (2011) Assessment of hepatocyte growth factor in ovarian cancer mortality, Cancer Epidemiol Biomark Prev 20:1638–1648CrossRefGoogle Scholar
  37. 37.
    Glud E, Kjaer SK, Thomsen BL, Høgdall C, Christensen L, Høgdall E, Bock JE, Blaakaer J (2004) Hormone therapy and the impact of estrogen intake on the risk of ovarian cancer. Arch Intern Med 164:2253–2259CrossRefGoogle Scholar
  38. 38.
    Soegaard M, Jensen A, Høgdall E, Christensen L, Høgdall C, Blaakaer J, Kjaer SK (2007) Different risk factor profiles for mucinous and nonmucinous ovarian cancer: results from the Danish MALOVA study. Cancer Epidemiol Biomark Prev 16:1160–1166CrossRefGoogle Scholar
  39. 39.
    Kelemen LE, Sellers TA, Schildkraut JM, Cunningham JM, Vierkant RA, Pankratz VS, Fredericksen ZS, Gadre MK, Rider DN, Liebow M, Goode EL (2008) Genetic variation in the one-carbon transfer pathway and ovarian cancer risk. Cancer Res 68:2498–2506CrossRefGoogle Scholar
  40. 40.
    Goode EL, Maurer MJ, Sellers TA, Phelan CM, Kalli KR, Fridley BL, Vierkant RA, Armasu SM, White KL, Keeney GL, Cliby WA, Rider DN, Kelemen LE, Jones MB, Peethambaram PP, Lancaster JM, Olson JE, Schildkraut JM, Cunningham JM, Hartmann LC (2010) Inherited determinants of ovarian cancer survival. Clin Cancer Res 16:995–1007CrossRefGoogle Scholar
  41. 41.
    Terry KL, De Vivo I, Titus-Ernstoff L, Shih MC, Cramer DW (2005) Androgen receptor cytosine, adenine, guanine repeats, and haplotypes in relation to ovarian cancer risk. Cancer Res 65:5974–5981CrossRefGoogle Scholar
  42. 42.
    Merritt MA, De Pari M, Vitonis AF, Titus LJ, Cramer DW, Terry KL (2013) Reproductive characteristics in relation to ovarian cancer risk by histologic pathways. Hum Reprod 28:1406–1417CrossRefGoogle Scholar
  43. 43.
    Bandera EV, King M, Chandran U, Paddock LE, Rodriguez-Rodriguez L, Olson SH (2011) Phytoestrogen consumption from foods and supplements and epithelial ovarian cancer risk: a population-based case control study. BMC Womens Health 11:40CrossRefGoogle Scholar
  44. 44.
    Chandran U, Bandera EV, Williams-King MG, Paddock LE, Rodriguez-Rodriguez L, Lu SE, Faulkner S, Pulick K, Olson SH (2011) Healthy eating index and ovarian cancer risk. Cancer Causes Control 22:563–571CrossRefGoogle Scholar
  45. 45.
    Gifkins D, Olson SH, Paddock L, King M, Demissie K, Lu SE, Kong AN, Rodriguez-Rodriguez L, Bandera EV (2012) Total and individual antioxidant intake and risk of epithelial ovarian cancer. BMC Cancer 12:211CrossRefGoogle Scholar
  46. 46.
    Pike MC, Pearce CL, Peters R, Cozen W, Wan P, Wu AH (2004) Hormonal factors and the risk of invasive ovarian cancer: a population-based case-control study. Fertil Steril 82:186–195CrossRefGoogle Scholar
  47. 47.
    Ness RB, Cramer DW, Goodman MT, Kjaer SK, Mallin K, Mosgaard BJ, Purdie DM, Risch HA, Vergona R, Wu AH (2002) Infertility, fertility drugs, and ovarian cancer: a pooled analysis of case-control studies. Am J Epidemiol 155:217–224CrossRefGoogle Scholar
  48. 48.
    Wu AH, Pearce CL, Tseng CC, Templeman C, Pike MC (2009) Markers of inflammation and risk of ovarian cancer in Los Angeles County. Int J Cancer 124:1409–1415CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Albina N. Minlikeeva
    • 1
  • Rikki Cannioto
    • 1
  • Allan Jensen
    • 2
  • Susanne K. Kjaer
    • 2
    • 3
  • Susan J. Jordan
    • 4
    • 5
  • Brenda Diergaarde
    • 6
  • J. Brian Szender
    • 7
  • Kunle Odunsi
    • 8
    • 9
  • Hani Almohanna
    • 1
  • Paul Mayor
    • 8
  • Kirsten Starbuck
    • 8
  • Emese Zsiros
    • 9
  • Elisa V. Bandera
    • 10
  • Daniel W. Cramer
    • 11
    • 12
  • Jennifer A. Doherty
    • 13
  • Anna DeFazio
    • 14
  • the Australian Ovarian Cancer Study Group
  • Robert Edwards
    • 15
    • 16
  • Ellen L. Goode
    • 17
  • Marc T. Goodman
    • 18
  • Estrid Høgdall
    • 2
    • 19
  • Keitary Matsuo
    • 20
    • 21
  • Mika Mizuno
    • 22
  • Christina M. Nagle
    • 4
    • 5
  • Roberta B. Ness
    • 23
  • Lisa E. Paddock
    • 24
    • 25
  • Celeste L. Pearce
    • 26
    • 27
  • Harvey A. Risch
    • 28
  • Mary Anne Rossing
    • 29
  • Kathryn L. Terry
    • 11
    • 12
  • Anna H. Wu
    • 27
  • Francesmary Modugno
    • 15
    • 16
    • 30
  • Penelope M. Webb
    • 4
    • 5
  • Kirsten B. Moysich
    • 1
    • 31
    Email author
  • the Ovarian Cancer Association Consortium
  1. 1.Department of Cancer Prevention and ControlRoswell Park Comprehensive Cancer CenterBuffaloUSA
  2. 2.Department of Virus, Lifestyle and GenesDanish Cancer Society Research CenterCopenhagenDenmark
  3. 3.Deparment of Gynaecology, RigshospitaletUniversity of CopenhagenCopenhagenDenmark
  4. 4.Population Health DepartmentQIMR Berghofer Medical Research InstituteBrisbaneAustralia
  5. 5.The University of Queensland, School of Public HealthHerstonAustralia
  6. 6.Department of Human GeneticsUniversity of Pittsburgh Graduate School of Public Health, and UPMC Hillman Cancer CenterPittsburghUSA
  7. 7.START Center for Cancer CareSan AntonioUSA
  8. 8.Department of Surgery, Division of Gynecologic OncologyRoswell Park Comprehensive Cancer CenterBuffaloUSA
  9. 9.Center of ImmunotherapyRoswell Park Comprehensive Cancer CenterBuffaloUSA
  10. 10.Cancer Prevention and Control ProgramRutgers Cancer Institute of New JerseyNew BrunswickUSA
  11. 11.Obstetrics and Gynecology Epidemiology CenterBrigham and Women’s HospitalBostonUSA
  12. 12.Department of EpidemiologyHarvard T. H. Chan School of Public HealthBostonUSA
  13. 13.Department of Epidemiology, The Geisel School of MedicineDartmouth CollegeHanoverUSA
  14. 14.Department of Gynecological Oncology, Westmead Hospital and the Westmead Institute for Medical ResearchThe University of SydneySydneyAustralia
  15. 15.Division of Gynecologic Oncology, Department of Obstetrics, Gynecology and Reproductive SciencesUniversity of Pittsburgh School of MedicinePittsburghUSA
  16. 16.Ovarian Cancer Center of Excellence, Womens Cancer Research ProgramMagee-Womens Research Institute and University of Pittsburgh Cancer InstitutePittsburghUSA
  17. 17.Division of Epidemiology, Department of Health Science ResearchMayo ClinicRochesterUSA
  18. 18.Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer InstituteCedars-Sinai Medical CenterLos AngelesUSA
  19. 19.Department of Pathology, Herlev and Gentofte HospitalUniversity of CopenhagenCopenhagenDenmark
  20. 20.Division of Molecular Medicine and Clinical EpidemiologyAichi Cancer Center Research InstituteNagoyaJapan
  21. 21.Department of EpidemiologyNagoya University Graduate School of MedicineNagoyaJapan
  22. 22.Department of Gynecological OncologyAichi Cancer Center HospitalNagoyaJapan
  23. 23.School of Public HealthThe University of TexasHoustonUSA
  24. 24.New Jersey Department of Health and Senior ServicesNew Jersey State Cancer RegistryTrentonUSA
  25. 25.Rutgers Cancer InstituteNew BrunswickUSA
  26. 26.Department of EpidemiologyUniversity of Michigan School of Public HealthAnn ArborUSA
  27. 27.Department of Preventive Medicine, Keck School of MedicineUniversity of Southern California Norris Comprehensive Cancer CenterLos AngelesUSA
  28. 28.Department of Chronic Disease EpidemiologyYale School of Public HealthNew HavenUSA
  29. 29.Program in Epidemiology, Division of Public Health SciencesFred Hutchinson Cancer Research CenterSeattleUSA
  30. 30.Department of EpidemiologyUniversity of PittsburghPittsburghUSA
  31. 31.Department of ImmunologyRoswell Park Comprehensive Cancer CenterBuffaloUSA

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