Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Association of inflammation-related exposures and ovarian cancer survival in a multi-site cohort study of Black women

British Journal of Cancer volume 129, pages 1119–1125 (2023)Cite this article

Subjects

Abstract

Background

An association was observed between an inflammation-related risk score (IRRS) and worse overall survival (OS) among a cohort of mostly White women with invasive epithelial ovarian cancer (EOC). Herein, we evaluated the association between the IRRS and OS among Black women with EOC, a population with higher frequencies of pro-inflammatory exposures and worse survival.

Methods

The analysis included 592 Black women diagnosed with EOC from the African American Cancer Epidemiology Study (AACES). Cox proportional hazards models were used to compute hazard ratios (HRs) and 95% confidence intervals (CIs) for the association of the IRRS and OS, adjusting for relevant covariates. Additional inflammation-related exposures, including the energy-adjusted Dietary Inflammatory Index (E-DIITM), were evaluated.

Results

A dose–response trend was observed showing higher IRRS was associated with worse OS (per quartile HR: 1.11, 95% CI: 1.01–1.22). Adding the E-DII to the model attenuated the association of IRRS with OS, and increasing E-DII, indicating a more pro-inflammatory diet, was associated with shorter OS (per quartile HR: 1.12, 95% CI: 1.02–1.24). Scoring high on both indices was associated with shorter OS (HR: 1.54, 95% CI: 1.16–2.06).

Conclusion

Higher levels of inflammation-related exposures were associated with decreased EOC OS among Black women.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

Data availability

The datasets generated and/or analysed during the current study are available on reasonable request, in accordance with the NIH data sharing policy.

Code availability

All analyses were performed using R (version 4.2.0), and the code is available on reasonable request.

References

  1. Torre LA, Trabert B, DeSantis CE, Miller KD, Samimi G, Runowicz CD, et al. Ovarian cancer statistics, 2018. CA Cancer J Clin. 2018;68:284–96.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Peres LC, Risch H, Terry KL, Webb PM, Goodman MT, Wu AH, et al. Racial/ethnic differences in the epidemiology of ovarian cancer: a pooled analysis of 12 case-control studies. Int J Epidemiol. 2018;47:1011.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA Cancer J Clin. 2022;72:7–33.

    Article  PubMed  Google Scholar 

  4. Terplan M, Smith EJ, Temkin SM. Race in ovarian cancer treatment and survival: a systematic review with meta-analysis. Cancer Causes Control. 2009;20:1139–50.

    Article  PubMed  Google Scholar 

  5. Howell EA, Egorova N, Hayes MP, Wisnivesky J, Franco R, Bickell N. Racial disparities in the treatment of advanced epithelial ovarian cancer. Obstet Gynecol. 2013;122:1025–32.

    Article  PubMed  Google Scholar 

  6. Basch E, Reeve BB, Mitchell SA, Clauser SB, Minasian LM, Dueck AC, et al. Development of the National Cancer Institute’s patient-reported outcomes version of the common terminology criteria for adverse events (PRO-CTCAE). J Natl Cancer Inst. 2014;106:dju244.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Du XL, Sun CC, Milam MR, Bodurka DC, Fang S. Ethnic differences in socioeconomic status, diagnosis, treatment, and survival among older women with epithelial ovarian cancer. Int J Gynecol Cancer. 2008;18:660–9.

    Article  CAS  PubMed  Google Scholar 

  8. Jemal A, Ward EM, Johnson CJ, Cronin KA, Ma J, Ryerson B, et al. Annual report to the nation on the status of cancer, 1975-2014, featuring survival. J Natl Cancer Inst. 2017;109:djx030.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Brenner DR, Scherer D, Muir K, Schildkraut J, Boffetta P, Spitz MR, et al. A review of the application of inflammatory biomarkers in epidemiologic cancer research. Cancer Epidemiol Biomark Prev. 2014;23:1729–51.

    Article  CAS  Google Scholar 

  10. Schildkraut JM. Invited Commentary: Relationship between ovulation and markers of systemic inflammation versus markers of localized inflammation. Am J Epidemiol. 2020;189:671–3.

    Article  PubMed  Google Scholar 

  11. Hathaway CA, Wang T, Townsend MK, Vinci C, Jake-Schoffman DE, Saeed-Vafa D, et al. Lifetime exposure to cigarette smoke and risk of ovarian cancer by T-cell tumor immune infiltration. Cancer Epidemiol Biomark Prev. 2023;32:66–73.

    Article  CAS  Google Scholar 

  12. Ye CJ, Feng T, Kwon HK, Raj T, Wilson M, Asinovski N, et al. Intersection of population variation and autoimmunity genetics in human T cell activation. Science. 2014;345:1254665.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Brieger KK, Peterson S, Lee AW, Mukherjee B, Bakulski KM, Alimujiang A, et al. Menopausal hormone therapy prior to the diagnosis of ovarian cancer is associated with improved survival. Gynecol Oncol. 2020;158:702–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Brieger KK, Phung MT, Mukherjee B, Bakulski KM, Anton-Culver H, Bandera EV, et al. High prediagnosis inflammation-related risk score associated with decreased ovarian cancer survival. Cancer Epidemiol Biomark Prev. 2022;31:443–52.

    Article  CAS  Google Scholar 

  15. Schildkraut JM, Johnson C, Dempsey LF, Qin B, Terry P, Akonde M, et al. Survival of epithelial ovarian cancer in Black women: a society to cell approach in the African American cancer epidemiology study (AACES). Cancer Causes Control. 2022;34:251–65.

  16. Peres LC, Moorman PG, Alberg AJ, Bandera EV, Barnholtz-Sloan J, Bondy M, et al. Lifetime number of ovulatory cycles and epithelial ovarian cancer risk in African American women. Cancer Causes Control. 2017;28:405–14.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Peres LC, Hebert JR, Qin B, Guertin KA, Bandera EV, Shivappa N, et al. Prediagnostic proinflammatory dietary potential is associated with all-cause mortality among African-American women with high-grade serous ovarian carcinoma. J Nutr. 2019;149:1606–16.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Peres LC, Bandera EV, Qin B, Guertin KA, Shivappa N, Hebert JR, et al. Dietary inflammatory index and risk of epithelial ovarian cancer in African American women. Int J Cancer. 2017;140:535–43.

    Article  CAS  PubMed  Google Scholar 

  19. Block G, Woods M, Potosky A, Clifford C. Validation of a self-administered diet history questionnaire using multiple diet records. J Clin Epidemiol. 1990;43:1327–35.

    Article  CAS  PubMed  Google Scholar 

  20. Tucker JM, Welk GJ, Beyler NK. Physical activity in U.S.: adults compliance with the Physical Activity Guidelines for Americans. Am J Prev Med. 2011;40:454–61.

    Article  PubMed  Google Scholar 

  21. Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, et al. A New Dietary Inflammatory Index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr. 2009;139:2365–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17:1689–96.

    Article  PubMed  Google Scholar 

  23. Buuren S, van, Groothuis-Oudshoorn K. mice: Multivariate Imputation by Chained Equations in R. J Stat Softw. 2011;45:1–67.

    Article  Google Scholar 

  24. Li R, Chambless L. Test for additive interaction in proportional hazards models. Ann Epidemiol. 2007;17:227–36.

    Article  PubMed  Google Scholar 

  25. VanderWeele TJ. Causal interactions in the proportional hazards model. Epidemiology. 2011;22:713–7.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the AACES interviewers Brandy Arredondo, Rachel Boehm, Dannelle Charles, Melody Chavez, Lauren Dempsey, Kierstin Faw, Juliana Fucinari, Mary Kan, Mary Beth Kolbicz, Arianna Mason, Juana Paniagua, and Maelia Pendley. We also acknowledge the individuals responsible for facilitating case ascertainment across the sites, including Kevin Ward and Mackenzie Crawford (Georgia); Tingting Li and Lauren Maniscalco (Louisiana); Dhanya Chanumolu and Myneka Macenat (New Jersey); Paul Terry (Tennessee); Ann Hamilton (California), Mary Beth Kolbicz (Michigan); Cynthia Webb, JoElla Marting, and Heather Tipaldos (North Carolina); and Maxwell Akonde, Stephanie Chiodini, and Deb Hurley (South Carolina).

Funding

The AACES study was funded by the National Cancer Institute (R01CA142081 and R01CA237318). Additional support was provided by Metropolitan Detroit Cancer Surveillance System (MDCSS) with federal funds from the National Cancer Institute, National Institute of Health, Dept. of Health and Human Services, under Contract No. HHSN261201000028C and the Epidemiology Research Core, supported in part by NCI Center Grant (P30CA22453) to the Karmanos Cancer Institute, Wayne State University School of Medicine. This work has been supported in part by the Participant Research, Interventions, and Measurements Core Facility at the H. Lee Moffit Cancer Center & Research Institute, an NCI designated Comprehensive Cancer Center (P30-CA076292). LJC was supported by K99CA277580 from the National Cancer Institute of the National Institutes of Health.

Author information

Authors and Affiliations

  1. Department of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA, USA

    Courtney E. Johnson, Hannah B. Mandle & Joellen M. Schildkraut

  2. Department of Epidemiology and Biostatistics, University of South Carolina Arnold School of Public Health, Columbia, SC, USA

    Anthony J. Alberg, Maxwell Akonde & James R. Hébert

  3. Cancer and Epidemiology and Health Outcomes, Rutgers Cancer Institute of New Jersey, New Brunswick, NJ, USA

    Elisa V. Bandera & Bonnie Qin

  4. Department of Cancer Epidemiology, H. Lee Moffitt Cancer Center and Research Institute, Tampa, FL, USA

    Lauren C. Peres

  5. Department of Population Health Sciences, University of Utah Huntsman Cancer Institute, Salt Lake City, UT, USA

    Lindsay J. Collin

  6. Melvin and Bren Simon Comprehensive Cancer Center, Indiana University, Bloomington, IN, USA

    Michele L. Cote

  7. Department of Oncology, Wayne State University School of Medicine, Detroit, MI, USA

    Theresa A. Hastert

  8. Department of Epidemiology, University of Nebraska Medical Center College of Public Health, Omaha, NE, USA

    Edward S. Peters

  9. Department of Medicine, University of Tennessee Medical Center-Knoxville, Knoxville, TN, USA

    Paul Terry

  10. Department of Oncology, Wayne State University School of Medicine Karmanos Cancer Institute, Detroit, MI, USA

    Ann G. Schwartz

  11. Department of Epidemiology and Population Health, Stanford University School of Medicine, Stanford, CA, USA

    Melissa Bondy

  12. Department of Human Genetics, Emory University School of Medicine, Atlanta, GA, USA

    Michael P. Epstein

  13. Department of Surgery, Duke University School of Medicine, Durham, NC, USA

    Jeffrey R. Marks

  14. Department of Public Health Sciences, Medical University of South Carolina, Charleston, SC, USA

    Andrew B. Lawson

  15. Usher Institute, School of Medicine, University of Edinburgh, Edinburgh, Scotland

    Andrew B. Lawson

Authors
  1. Courtney E. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony J. Alberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elisa V. Bandera
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lauren C. Peres
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maxwell Akonde
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lindsay J. Collin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Michele L. Cote
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Theresa A. Hastert
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. James R. Hébert
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Edward S. Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Bonnie Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Paul Terry
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ann G. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Melissa Bondy
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Michael P. Epstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Hannah B. Mandle
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Jeffrey R. Marks
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Andrew B. Lawson
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Joellen M. Schildkraut
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The following authors were a part of the writing group: CEJ, JMS, AJA, EVB, PT, ESP, BQ, HBM, MLC, MA, TAH, and LJC. The analysis was completed by: CEJ. The following authors provided comments and edits to the manuscript: LVP, AGS, ABL, and JRH. The following authors helped in data collection: JMSchildkraut, AJA, EVB, PT, MA, ESP, MLC, JRM, MB, AGS, and HBM. JRH developed the energy-adjusted dietary inflammatory index.

Corresponding author

Correspondence to Joellen M. Schildkraut.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

This study was approved by the Western Institutional Review Board-Copernicus Group (WCG IRB). The study was performed in accordance with the Declaration of Helsinki. Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Johnson, C.E., Alberg, A.J., Bandera, E.V. et al. Association of inflammation-related exposures and ovarian cancer survival in a multi-site cohort study of Black women. Br J Cancer 129, 1119–1125 (2023). https://doi.org/10.1038/s41416-023-02385-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41416-023-02385-w

Search

Advanced search

Quick links