The association between socioeconomic status and tumour stage at diagnosis of ovarian cancer: A pooled analysis of 18 case-control studies

Camilla Præstegaard¹, Susanne K Kjaer², Thor S S Nielsen¹, Signe M Jensen³, Penelope M Webb⁴, Christina M Nagle⁵, Estrid Høgdall⁶, Harvey A Risch⁷, Mary Anne Rossing⁸, Jennifer A Doherty⁹, Kristine G Wicklund¹⁰, Marc T Goodman¹¹, Francesmary Modugno¹², Kirsten Moysich¹³, Roberta B Ness¹⁴, Robert P Edwards¹⁵, Ellen L Goode¹⁶, Stacey J Winham¹⁷, Brooke L Fridley¹⁷, Daniel W Cramer¹⁸, Kathryn L Terry¹⁹, Joellen M Schildkraut²⁰, Andrew Berchuck²¹, Elisa V Bandera²², Lisa Paddock²³, Lambertus A Kiemeney²⁴, Leon F Massuger²⁵, Nicolas Wentzensen²⁶, Paul Pharoah²⁷, Honglin Song²⁸, Alice S Whittemore²⁹, Valerie McGuire²⁹, Weiva Sieh²⁹, Joseph Rothstein²⁹, Hoda Anton-Culver³⁰, Argyrios Ziogas³¹, Usha Menon³², Simon A Gayther³², Susan J Ramus³³, Aleksandra Gentry-Maharaj³², Anna H Wu³³, Celeste L Pearce³⁴, Malcolm C Pike³⁵, Alice W Lee³³, Jenny Chang-Claude³⁶, Allan Jensen³⁷; Ovarian Cancer Association Consortium

Affiliations

¹ Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark.
² Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark; Department of Gynecology, Rigshospitalet, Copenhagen University Hospital, Blegdamsvej 9, DK-2100 Copenhagen, Denmark.
³ Statistics, Bioinformatics and Registry, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark.
⁴ Population Health Department, QIMR Berghofer Medical Research Institute, 300 Herston Rd, Herston, Queensland 4006, Brisbane, Australia; Peter MacCallum Cancer Centre, East Melbourne, Victoria, Australia.
⁵ Population Health Department, QIMR Berghofer Medical Research Institute, 300 Herston Rd, Herston, Queensland 4006, Brisbane, Australia.
⁶ Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark; Molecular Unit, Department of Pathology, Herlev Hospital, Copenhagen University Hospital, Herlev Ringvej 75, DK-2730 Herlev, Denmark.
⁷ Department of Chronic Disease Epidemiology, Yale School of Public Health, LEPH 413, 60 College Street, New Haven, CT 06510, USA.
⁸ Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, PO Box 19024, Seattle, WA 98109-1024, USA; Department of Epidemiology, University of Washington, PO Box 19024, Seattle, WA 98109-1024, USA.
⁹ Department of Community and Family Medicine, Section of Biostatistics & Epidemiology, Geisel School of Medicine, Dartmouth College, 1 Medical Center Drive, 7927 Rubin Building, Room 884, Lebanon, Hanover, NH 03756, USA.
¹⁰ Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, PO Box 19024, Seattle, WA 98109-1024, USA.
¹¹ Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, 8700 Beverly Blvd., Room 1S37, Los Angeles 90048, CA, USA; Community and Population Health Research Institute, Department of Biomedical Sciences, Cedars-Sinai Medical Center, 8700 Beverly Blvd., Room 1S37, Los Angeles 90048, CA, USA.
¹² Department of Obstetrics, Gynecology and Reproductive Sciences, Division of Gynecologic Oncology, University of Pittsburgh School of Medicine, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA; Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA; Womens Cancer Research Program, Magee-Womens Research Institute and University of Pittsburgh Cancer Institute, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA.
¹³ Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263, USA.
¹⁴ The University of Texas, School of Public Health, P.O. Box 20186, Houston, TX 77225, USA.
¹⁵ Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA.
¹⁶ Department of Health Science Research, Division of Epidemiology, Mayo Clinic, 200 First Street SW, Charlton 6, Rochester, MN, USA.
¹⁷ Department of Biostatistics, University of Kansas, 5028B Robinson Building, 3901 Rainbow Blvd, Kansas City, KS 66160, USA.
¹⁸ Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, 221 Longwood Avenue, RFB 368, Boston, MA 02115, USA.
¹⁹ Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, 221 Longwood Avenue, RFB 368, Boston, MA 02115, USA; Department of Epidemiology, Harvard T.H. Chan School of Public Health, 221 Longwood Avenue, RFB 368, Boston, MA 02115, USA.
²⁰ Department of Public Health Sciences, School of Medicine, University of Virginia, Box: 800717, Charlottesville, VA 22908, USA.
²¹ Department of Obstetrics and Gynecology, Duke University Medical Center, 3079, Durham, NC 27710, USA.
²² Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, 195 Little Albany Street, Room 5568, New Brunswick, NJ 08903, USA.
²³ New Jersey State Cancer registry, PO Box 369, Trenton, NJ 08625-0369, USA; Rutgers School of Public Health, Piscataway, NJ, USA.
²⁴ Department for Health Evidence, Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands; Department of Urology, Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands.
²⁵ Department of Obstetrics and Gynaecology, Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands.
²⁶ Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd, Rockville, MD 20852, USA.
²⁷ Department of Oncology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Wortscauseway, Cambridge, CB1 8RN, United Kingdom.
²⁸ Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Wortscauseway, Cambridge, CB1 8RN, United Kingdom.
²⁹ Department of Health Research and Policy-Epidemiology, Stanford University School of Medicine, 259 Campus Drive, Stanford, CA 94305-5405, USA.
³⁰ Department of Epidemiology, University of California Irvine, Center for Cancer Genetics Research & Prevention, School of Medicine, 224 Irvine Hall, Irvine, CA 92697-7550, USA.
³¹ Department of Epidemiology, University of California Irvine, 224 Irvine Hall, Irvine, CA 92697-7550, USA.
³² Women's Cancer, UCL EGA Institute for Women's Health, Maple House 1st Floor, 149 Tottenham Court Road, London W1T 7DN, United Kingdom.
³³ Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Harlyne Norris Research Tower 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA.
³⁴ Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Harlyne Norris Research Tower 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA; Department of Epidemiology, University of Michigan School of Public Health, 1415 Washington Heights, SPH Tower, Office #4642, Ann Arbor, MI 48109-2029, USA.
³⁵ Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Harlyne Norris Research Tower 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA; Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, 307 East 63rd Street, New York, NY 10065, USA.
³⁶ German Cancer Research Center, Division of Cancer Epidemiology, Postfach 101949, 69009 Heidelberg, Germany.
³⁷ Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark. Electronic address: allan@cancer.dk.

PMID: 26851750
PMCID: PMC4993452
DOI: 10.1016/j.canep.2016.01.012

The association between socioeconomic status and tumour stage at diagnosis of ovarian cancer: A pooled analysis of 18 case-control studies

Camilla Præstegaard et al. Cancer Epidemiol. 2016 Apr.

. 2016 Apr:41:71-9.

doi: 10.1016/j.canep.2016.01.012. Epub 2016 Feb 3.

Authors

Affiliations

¹ Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark.
² Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark; Department of Gynecology, Rigshospitalet, Copenhagen University Hospital, Blegdamsvej 9, DK-2100 Copenhagen, Denmark.
³ Statistics, Bioinformatics and Registry, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark.
⁴ Population Health Department, QIMR Berghofer Medical Research Institute, 300 Herston Rd, Herston, Queensland 4006, Brisbane, Australia; Peter MacCallum Cancer Centre, East Melbourne, Victoria, Australia.
⁵ Population Health Department, QIMR Berghofer Medical Research Institute, 300 Herston Rd, Herston, Queensland 4006, Brisbane, Australia.
⁶ Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark; Molecular Unit, Department of Pathology, Herlev Hospital, Copenhagen University Hospital, Herlev Ringvej 75, DK-2730 Herlev, Denmark.
⁷ Department of Chronic Disease Epidemiology, Yale School of Public Health, LEPH 413, 60 College Street, New Haven, CT 06510, USA.
⁸ Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, PO Box 19024, Seattle, WA 98109-1024, USA; Department of Epidemiology, University of Washington, PO Box 19024, Seattle, WA 98109-1024, USA.
⁹ Department of Community and Family Medicine, Section of Biostatistics & Epidemiology, Geisel School of Medicine, Dartmouth College, 1 Medical Center Drive, 7927 Rubin Building, Room 884, Lebanon, Hanover, NH 03756, USA.
¹⁰ Program in Epidemiology, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, PO Box 19024, Seattle, WA 98109-1024, USA.
¹¹ Cancer Prevention and Control, Samuel Oschin Comprehensive Cancer Institute, Cedars-Sinai Medical Center, 8700 Beverly Blvd., Room 1S37, Los Angeles 90048, CA, USA; Community and Population Health Research Institute, Department of Biomedical Sciences, Cedars-Sinai Medical Center, 8700 Beverly Blvd., Room 1S37, Los Angeles 90048, CA, USA.
¹² Department of Obstetrics, Gynecology and Reproductive Sciences, Division of Gynecologic Oncology, University of Pittsburgh School of Medicine, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA; Department of Epidemiology, University of Pittsburgh Graduate School of Public Health, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA; Womens Cancer Research Program, Magee-Womens Research Institute and University of Pittsburgh Cancer Institute, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA.
¹³ Department of Cancer Prevention and Control, Roswell Park Cancer Institute, Elm and Carlton Streets, Buffalo, NY 14263, USA.
¹⁴ The University of Texas, School of Public Health, P.O. Box 20186, Houston, TX 77225, USA.
¹⁵ Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh School of Medicine, Magee-Womens Hospital, 300 Halket Street (Room #2130), Pittsburgh, PA 15222, USA.
¹⁶ Department of Health Science Research, Division of Epidemiology, Mayo Clinic, 200 First Street SW, Charlton 6, Rochester, MN, USA.
¹⁷ Department of Biostatistics, University of Kansas, 5028B Robinson Building, 3901 Rainbow Blvd, Kansas City, KS 66160, USA.
¹⁸ Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, 221 Longwood Avenue, RFB 368, Boston, MA 02115, USA.
¹⁹ Obstetrics and Gynecology Epidemiology Center, Brigham and Women's Hospital, 221 Longwood Avenue, RFB 368, Boston, MA 02115, USA; Department of Epidemiology, Harvard T.H. Chan School of Public Health, 221 Longwood Avenue, RFB 368, Boston, MA 02115, USA.
²⁰ Department of Public Health Sciences, School of Medicine, University of Virginia, Box: 800717, Charlottesville, VA 22908, USA.
²¹ Department of Obstetrics and Gynecology, Duke University Medical Center, 3079, Durham, NC 27710, USA.
²² Cancer Prevention and Control Program, Rutgers Cancer Institute of New Jersey, 195 Little Albany Street, Room 5568, New Brunswick, NJ 08903, USA.
²³ New Jersey State Cancer registry, PO Box 369, Trenton, NJ 08625-0369, USA; Rutgers School of Public Health, Piscataway, NJ, USA.
²⁴ Department for Health Evidence, Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands; Department of Urology, Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands.
²⁵ Department of Obstetrics and Gynaecology, Radboud University Medical Center, PO Box 9101, 6500 HB Nijmegen, The Netherlands.
²⁶ Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd, Rockville, MD 20852, USA.
²⁷ Department of Oncology, Department of Public Health and Primary Care, University of Cambridge, Strangeways Research Laboratory, Wortscauseway, Cambridge, CB1 8RN, United Kingdom.
²⁸ Department of Oncology, University of Cambridge, Strangeways Research Laboratory, Wortscauseway, Cambridge, CB1 8RN, United Kingdom.
²⁹ Department of Health Research and Policy-Epidemiology, Stanford University School of Medicine, 259 Campus Drive, Stanford, CA 94305-5405, USA.
³⁰ Department of Epidemiology, University of California Irvine, Center for Cancer Genetics Research & Prevention, School of Medicine, 224 Irvine Hall, Irvine, CA 92697-7550, USA.
³¹ Department of Epidemiology, University of California Irvine, 224 Irvine Hall, Irvine, CA 92697-7550, USA.
³² Women's Cancer, UCL EGA Institute for Women's Health, Maple House 1st Floor, 149 Tottenham Court Road, London W1T 7DN, United Kingdom.
³³ Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Harlyne Norris Research Tower 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA.
³⁴ Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Harlyne Norris Research Tower 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA; Department of Epidemiology, University of Michigan School of Public Health, 1415 Washington Heights, SPH Tower, Office #4642, Ann Arbor, MI 48109-2029, USA.
³⁵ Department of Preventive Medicine, Keck School of Medicine, University of Southern California Norris Comprehensive Cancer Center, Harlyne Norris Research Tower 1450 Biggy Street, Office 2517G, Los Angeles, CA 90033, USA; Department of Epidemiology and Biostatistics, Memorial Sloan Kettering Cancer Center, 307 East 63rd Street, New York, NY 10065, USA.
³⁶ German Cancer Research Center, Division of Cancer Epidemiology, Postfach 101949, 69009 Heidelberg, Germany.
³⁷ Virus, Lifestyle and Genes, Danish Cancer Society Research Center, Strandboulevarden 49, DK-2100 Copenhagen, Denmark. Electronic address: allan@cancer.dk.

PMID: 26851750
PMCID: PMC4993452
DOI: 10.1016/j.canep.2016.01.012

Abstract

Purpose: Socioeconomic status (SES) is a known predictor of survival for several cancers and it has been suggested that SES differences affecting tumour stage at diagnosis may be the most important explanatory factor for this. However, only a limited number of studies have investigated SES differences in tumour stage at diagnosis of ovarian cancer. In a pooled analysis, we investigated whether SES as represented by level of education is predictive for advanced tumour stage at diagnosis of ovarian cancer, overall and by histotype. The effect of cigarette smoking and body mass index (BMI) on the association was also evaluated.

Methods: From 18 case-control studies, we obtained information on 10,601 women diagnosed with epithelial ovarian cancer. Study specific odds ratios (ORs) with corresponding 95% confidence intervals (CI) were obtained from logistic regression models and combined into a pooled odds ratio (pOR) using a random effects model.

Results: Overall, women who completed ≤high school had an increased risk of advanced tumour stage at diagnosis compared with women who completed >high school (pOR 1.15; 95% CI 1.03-1.28). The risk estimates for the different histotypes of ovarian cancer resembled that observed for ovarian cancers combined but did not reach statistical significance. Our results were unchanged when we included BMI and cigarette smoking.

Conclusion: Lower level of education was associated with an increased risk of advanced tumour stage at diagnosis of ovarian cancer. The observed socioeconomic difference in stage at diagnosis of ovarian cancer calls for further studies on how to reduce this diagnostic delay.

Keywords: Epidemiology; Ovarian cancer; Pooled analysis; Socioeconomic status; Tumour stage.

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Conflict of interest statement

None

Figures

**Fig. 1**
Risk of advanced tumour stage at diagnosis of ovarian cancer associated with level of education by study site and overall. Study-specific odds ratios (ORs) and 95% confidence intervals (CIs) were estimated using logistic regression models adjusted for age and race/ethnicity. The pooled odds ratio (pOR) with corresponding 95% CI was estimated using a random effects model. Level of education was parameterized as women who completed high school or less versus women who completed more than high school

See this image and copyright information in PMC

References

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA: A Cancer Journal for Clinicians. 2015;65:87–108. - PubMed
1. Howlader N, Noone AM, Krapcho M, Garshell J, Miller D, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA, editors. Bethesda, MD: National Cancer Institute; [Accessed on November 22]. SEER Cancer Statistics Review, 1975–2012. http://seer.cancer.gov/csr/1975_2012/, based on November 2014 SEER data submission, posted to the SEER web site, April 2015.
1. Kogevinas M, Porta M. Socioeconomic differences in cancer survival: a review of the evidence. IARC Sci Publ. 1997;138:177–206. - PubMed
1. Woods LM, Rachet B, Coleman MP. Origins of socio-economic inequalities in cancer survival: a review. Ann Oncol. 2006;17:5–19. - PubMed
1. Jensen KE, Hannibal CG, Nielsen A, Jensen A, Nohr B, Munk C, Kjaer SK. Social inequality and incidence of and survival from cancer of the female genital organs in a population-based study in Denmark, 1994–2003. Eur J Cancer. 2008;44:2003–2017. - PubMed

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The association between socioeconomic status and tumour stage at diagnosis of ovarian cancer: A pooled analysis of 18 case-control studies

Affiliations

The association between socioeconomic status and tumour stage at diagnosis of ovarian cancer: A pooled analysis of 18 case-control studies

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical