Advertisement

Breast Cancer Research and Treatment

, Volume 173, Issue 1, pp 217–224 | Cite as

Psychosocial stress is associated with benign breast disease in young Chinese women: results from Project ELEFANT

  • Timothy M. Barrow
  • Cheng Peng
  • Ander Wilson
  • Hao Wang
  • Hongbin Liu
  • Lilin Shen
  • Nai-jun Tang
  • Chanachai Sae-Lee
  • Peng-hui Li
  • Liqiong GuoEmail author
  • Hyang-Min Byun
Epidemiology

Abstract

Purpose

Psychosocial stress, including bereavement and work-related stress, is associated with the risk of breast cancer. However, it is unknown whether it may also be linked with increased risk of benign breast disease (BBD).

Methods

Our study leveraged 61,907 women aged 17–55 years old from the Project ELEFANT study. BBD was diagnosed by clinician. Self-reported data on psychosocial stress over a 10-year period was retrospectively collected from questionnaires and categorised by cause (work, social and economic) and severity (none, low and high). Odd ratios (ORs) for the development of BBD were estimated using logistic regression. The model was adjusted for age, BMI, TSH levels, smoking, alcohol consumption, family history, age of menarche, oral contraceptive usage, education and occupation.

Results

Within our study, 8% (4,914) of participants were diagnosed with BBD. Work-related stress [OR 1.57, 95% confidence interval (CI) 1.46–1.69] and financial stress (OR 1.34, 95% CI 1.24–1.44) were significantly associated with BBD incidence, with a smaller but still significant association with social stress (OR 1.11, 95% CI 1.01–1.21). The associations remained significant after exclusion of participants with first- and second-degree family history of breast disease. The presence of multiple forms of stress did not synergistically increase risk. The neutrophil–lymphocyte ratio (NLR), a marker of systemic inflammation and prognostic marker for breast cancer, was not associated with BBD.

Conclusions

Psychosocial stress, particularly work-related and financial stress, is associated with increased risk of benign breast disease among young Chinese women.

Keywords

Benign breast disease Stress Psychosocial stress Neutrophil–lymphocyte ratio 

Abbreviations

BBD

Benign breast disease

BMI

Body Mass Index

NLR

Neutrophil–lymphocyte ratio

OR

Odds ratio

SD

Standard deviation

Notes

Acknowledgements

We are extremely grateful to the Tianjin Research Institute for Family Planning which provided the data and samples for the study.

Funding

This work was supported by the National Natural Science of China, Foundation of China Youth Science Fund Projects (Grant Numbers: 81602827 for LG and 41601548 for PL), and by the Tianjin Natural Science Foundation (Grant Number: 18JCQNJC11700 for LG).

Compliance with ethical standards

Conflict of interest

All the authors declare that they have no conflicts of interest.

Ethical approval

All procedures and study protocols were approved by the ethical committee of Tianjin Medical University and were in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

All the participants within the study provided written informed consent.

Supplementary material

10549_2018_4979_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 KB)

References

  1. 1.
    Berkey CS, Willett WC, Tamimi RM, Rosner B, Frazier AL, Colditz GA (2013) Vegetable protein and vegetable fat intakes in pre-adolescent and adolescent girls, and risk for benign breast disease in young women. Breast Cancer Res Treat 141(2):299–306PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Brinton LA, Vessey MP, Flavel R, Yeates D (1981) Risk factors for benign breast disease. Am J Epidemiol 113(3):203–214PubMedCrossRefGoogle Scholar
  3. 3.
    Cheng J, Qiu S, Raju U, Wolman SR, Worsham MJ (2008) Benign breast disease heterogeneity: association with histopathology, age, and ethnicity. Breast Cancer Res Treat 111(2):289–296PubMedCrossRefGoogle Scholar
  4. 4.
    Farland LV, Tamimi RM, Eliassen AH, Spiegelman D, Collins LC, Schnitt SJ, Missmer SA (2016) A prospective study of endometriosis and risk of benign breast disease. Breast Cancer Res Treat 159(3):545–552PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Nelson ZC, Ray RM, Wu C, Stalsberg H, Porter P, Lampe JW, Shannon J, Horner N, Li W, Wang W et al (2010) Fruit and vegetable intakes are associated with lower risk of breast fibroadenomas in Chinese women. J Nutr 140(7):1294–1301PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Samoli E, Trichopoulos D, Lagiou A, Zourna P, Georgila C, Minaki P, Barbouni A, Vassilarou D, Tsikkinis A, Sfikas C et al (2013) The hormonal profile of benign breast disease. Br J Cancer 108(1):199–204PubMedCrossRefGoogle Scholar
  7. 7.
    Berkey CS, Willett WC, Frazier AL, Rosner B, Tamimi RM, Rockett HR, Colditz GA (2010) Prospective study of adolescent alcohol consumption and risk of benign breast disease in young women. Pediatrics 125(5):e1081–e1087PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Berkey CS, Tamimi RM, Willett WC, Rosner B, Lindsay Frazier A, Colditz GA (2014) Adolescent physical activity and inactivity: a prospective study of risk of benign breast disease in young women. Breast Cancer Res Treat 146(3):611–618PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Boeke CE, Tamimi RM, Berkey CS, Colditz GA, Eliassen AH, Malspeis S, Willett WC, Frazier AL (2014) Adolescent carotenoid intake and benign breast disease. Pediatrics 133(5):e1292–e1298PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Cohen K, Liu Y, Luo J, Appleton CM, Colditz GA (2017) Plasma carotenoids and the risk of premalignant breast disease in women aged 50 and younger: a nested case-control study. Breast Cancer Res Treat 162(3):571–580PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Jung MM, Colditz GA, Collins LC, Schnitt SJ, Connolly JL, Tamimi RM (2011) Lifetime physical activity and the incidence of proliferative benign breast disease. Cancer Causes Control 22(9):1297–1305PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Cui Y, Page DL, Chlebowski RT, Hsia J, Allan Hubbell F, Johnson KC, Rohan TE (2007) Cigarette smoking and risk of benign proliferative epithelial disorders of the breast in the Women’s Health Initiative. Cancer Causes Control 18(4):431–438PubMedCrossRefGoogle Scholar
  13. 13.
    Parazzini F, Ferraroni M, La Vecchia C, Baron JA, Levi F, Franceschi S, Decarli A (1991) Smoking habits and risk of benign breast disease. Int J Epidemiol 20(2):430–434PubMedCrossRefGoogle Scholar
  14. 14.
    Liu T, Gatsonis CA, Baylin A, Buka SL (2010) Prenatal exposure to cigarette smoke and benign breast disease. Epidemiology 21(5):736–743PubMedCrossRefGoogle Scholar
  15. 15.
    Bertelsen L, Mellemkjaer L, Balslev E, Olsen JH (2008) Benign breast disease among first-degree relatives of young breast cancer patients. Am J Epidemiol 168(3):261–267PubMedCrossRefGoogle Scholar
  16. 16.
    Jorgensen TJ, Helzlsouer KJ, Clipp SC, Bolton JH, Crum RM, Visvanathan K (2009) DNA repair gene variants associated with benign breast disease in high cancer risk women. Cancer Epidemiol Biomarkers Prev 18(1):346–350PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Deschamps M, Hislop TG, Band PR, Coldman AJ (1986) Study of benign breast disease in a population screened for breast cancer. Cancer Detect Prev 9(1–2):151–156PubMedGoogle Scholar
  18. 18.
    Dyrstad SW, Yan Y, Fowler AM, Colditz GA (2015) Breast cancer risk associated with benign breast disease: systematic review and meta-analysis. Breast Cancer Res Treat 149(3):569–575PubMedCrossRefGoogle Scholar
  19. 19.
    Worsham MJ, Abrams J, Raju U, Kapke A, Lu M, Cheng J, Mott D, Wolman SR (2007) Breast cancer incidence in a cohort of women with benign breast disease from a multiethnic, primary health care population. Breast J 13(2):115–121PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Tice JA, O’Meara ES, Weaver DL, Vachon C, Ballard-Barbash R, Kerlikowske K (2013) Benign breast disease, mammographic breast density, and the risk of breast cancer. J Natl Cancer Inst 105(14):1043–1049PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Hartmann LC, Sellers TA, Frost MH, Lingle WL, Degnim AC, Ghosh K, Vierkant RA, Maloney SD, Pankratz VS, Hillman DW et al (2005) Benign breast disease and the risk of breast cancer. N Engl J Med 353(3):229–237PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298(14):1685–1687PubMedCrossRefGoogle Scholar
  23. 23.
    Vanitallie TB (2002) Stress: a risk factor for serious illness. Metabolism 51(6 Suppl 1):40–45PubMedCrossRefGoogle Scholar
  24. 24.
    Cooper CL, Cooper R, Faragher EB (1989) Incidence and perception of psychosocial stress: the relationship with breast cancer. Psychol Med 19(2):415–422PubMedCrossRefGoogle Scholar
  25. 25.
    Duijts SF, Zeegers MP, Borne BV (2003) The association between stressful life events and breast cancer risk: a meta-analysis. Int J Cancer 107(6):1023–1029PubMedCrossRefGoogle Scholar
  26. 26.
    Kocic B, Filipovic S, Vrbic S, Pejcic I, Rancic N, Cvetanovic A, Milenkovic D (2015) Stressful life events and breast cancer risk: a hospital-based case–control study. J BUON 20(2):487–491PubMedGoogle Scholar
  27. 27.
    Lillberg K, Verkasalo PK, Kaprio J, Teppo L, Helenius H, Koskenvuo M (2003) Stressful life events and risk of breast cancer in 10,808 women: a cohort study. Am J Epidemiol 157(5):415–423PubMedCrossRefGoogle Scholar
  28. 28.
    Vin-Raviv N, Dekel R, Barchana M, Linn S, Keinan-Boker L (2014) World War II-related post-traumatic stress disorder and breast cancer risk among Israeli women: a case–control study. Int Psychogeriatr 26(3):499–508PubMedCrossRefGoogle Scholar
  29. 29.
    Eskelinen M, Ollonen P (2010) Life stress due to losses and deficit in childhood and adolescence as breast cancer risk factor: a prospective case–control study in Kuopio, Finland. Anticancer Res 30(10):4303–4308PubMedGoogle Scholar
  30. 30.
    Kuper H, Yang L, Theorell T, Weiderpass E (2007) Job strain and risk of breast cancer. Epidemiology 18(6):764–768PubMedCrossRefGoogle Scholar
  31. 31.
    Eskelinen M, Ollonen P (2010) Life stress and losses and deficit in adulthood as breast cancer risk factor: a prospective case-control study in Kuopio, Finland. In Vivo 24(6):899–904PubMedGoogle Scholar
  32. 32.
    Chen CC, David AS, Nunnerley H, Michell M, Dawson JL, Berry H, Dobbs J, Fahy T (1995) Adverse life events and breast cancer: case–control study. BMJ 311(7019):1527–1530PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Siu O, Donald I, Cooper CL. The use of the occupational stress indicator (OSI) in factory workers in China. Int J Stress Manage 1997; 4171Google Scholar
  34. 34.
    Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24(4):385–396PubMedCrossRefGoogle Scholar
  35. 35.
    Hall LC, Salazar EP, Kane SR, Liu N (2008) Effects of thyroid hormones on human breast cancer cell proliferation. J Steroid Biochem Mol Biol 109(1–2):57–66PubMedCrossRefGoogle Scholar
  36. 36.
    Søgaard M, Farkas DK, Ehrenstein V, Jørgensen JO, Dekkers OM, Sørensen HT (2016) Hypothyroidism and hyperthyroidism and breast cancer risk: a nationwide cohort study. Eur J Endocrinol 174(4):409–414PubMedCrossRefGoogle Scholar
  37. 37.
    Weng CH, Chen YH, Lin CH, Luo X, Lin TH (2018) Thyroid disorders and breast cancer risk in Asian population: a nationwide population-based case-control study in Taiwan. BMJ Open 8(3):e020194PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Ethier JL, Desautels D, Templeton A, Shah PS, Amir E (2017) Prognostic role of neutrophil-to-lymphocyte ratio in breast cancer: a systematic review and meta-analysis. Breast Cancer Res 19(1):2PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Kruk J, Aboul-Enein HY (2004) Psychological stress and the risk of breast cancer: a case-control study. Cancer Detect Prev 28(6):399–408PubMedCrossRefGoogle Scholar
  40. 40.
    Kruk J (2012) Self-reported psychological stress and the risk of breast cancer: a case–control study. Stress 15(2):162–171PubMedCrossRefGoogle Scholar
  41. 41.
    Yasuda MT, Sakakibara H, Shimoi K. Estrogen- and stress-induced DNA damage in breast cancer and chemoprevention with dietary flavonoid. Genes Environ 2017; 3910Google Scholar
  42. 42.
    Schoemaker MJ, Jones ME, Wright LB, Griffin J, McFadden E, Ashworth A, Swerdlow AJ (2016) Psychological stress, adverse life events and breast cancer incidence: a cohort investigation in 106,000 women in the United Kingdom. Breast Cancer Res 18(1):72PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Heikkilä K, Nyberg ST, Theorell T, Fransson EI, Alfredsson L, Bjorner JB, Bonenfant S, Borritz M, Bouillon K, Burr H et al (2013) Work stress and risk of cancer: meta-analysis of 5700 incident cancer events in 116,000 European men and women. BMJ 346:f165PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Schernhammer ES, Hankinson SE, Rosner B, Kroenke CH, Willett WC, Colditz GA, Kawachi I (2004) Job stress and breast cancer risk: the nurses’ health study. Am J Epidemiol 160(11):1079–1086PubMedCrossRefGoogle Scholar
  45. 45.
    Montgomery M, McCrone SH (2010) Psychological distress associated with the diagnostic phase for suspected breast cancer: systematic review. J Adv Nurs 66(11):2372–2390PubMedCrossRefGoogle Scholar
  46. 46.
    Bozovic D, Racic M, Ivkovic N (2013) Salivary cortisol levels as a biological marker of stress reaction. Med Arch 67(5):374–377PubMedCrossRefGoogle Scholar
  47. 47.
    Antonova L, Aronson K, Mueller CR (2011) Stress and breast cancer: from epidemiology to molecular biology. Breast Cancer Res 13(2):208PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Antonova L, Mueller CR (2008) Hydrocortisone down-regulates the tumor suppressor gene BRCA1 in mammary cells: a possible molecular link between stress and breast cancer. Genes Chromosomes Cancer 47(4):341–352PubMedCrossRefGoogle Scholar
  49. 49.
    Schmidt M, Löffler G (1994) Induction of aromatase in stromal vascular cells from human breast adipose tissue depends on cortisol and growth factors. FEBS Lett 341(2–3):177–181PubMedCrossRefGoogle Scholar
  50. 50.
    Lou Z, Li Y, Yang Y, Wang L, Yang J (2015) Affects of anxiety and depression on health-related quality of life among patients with benign breast lumps diagnosed via ultrasonography in China. Int J Environ Res Public Health 12(9):10587–10601PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Byrne C, Webb PM, Jacobs TW, Peiro G, Schnitt SJ, Connolly JL, Willett WC, Colditz GA (2002) Alcohol consumption and incidence of benign breast disease. Cancer Epidemiol Biomarkers Prev 11:369–374Google Scholar
  52. 52.
    Rohan TE, Negassa A, Chlebowski RT, Lasser NL, McTiernan A, Schenken RS, Ginsberg M, Wassertheil-Smoller S, Page DL (2008) Estrogen plus progestin and risk of benign proliferative breast disease. Cancer Epidemiol Biomarkers Prev 17(9):2337–2343PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Timothy M. Barrow
    • 1
  • Cheng Peng
    • 2
  • Ander Wilson
    • 3
  • Hao Wang
    • 4
  • Hongbin Liu
    • 4
  • Lilin Shen
    • 4
  • Nai-jun Tang
    • 5
  • Chanachai Sae-Lee
    • 6
    • 7
  • Peng-hui Li
    • 8
  • Liqiong Guo
    • 5
    Email author
  • Hyang-Min Byun
    • 6
  1. 1.Faculty of Health Sciences & WellbeingUniversity of SunderlandSunderlandUK
  2. 2.Channing Division of Network Medicine, Brigham and Women’s HospitalHarvard Medical SchoolBostonUSA
  3. 3.Department of StatisticsColorado State UniversityFort CollinsUSA
  4. 4.Tianjin Research Institute for Family PlanningTianjinChina
  5. 5.Department of Occupational & Environmental Health, School of Public HealthTianjin Medical UniversityTianjinChina
  6. 6.Human Nutrition Research Centre, Institute of Cellular MedicineNewcastle UniversityNewcastle Upon TyneUK
  7. 7.Research Division, Faculty of Medicine Siriraj HospitalMahidol UniversityBangkokThailand
  8. 8.School of Environmental Science and Safety EngineeringTianjin University of TechnologyTianjinChina

Personalised recommendations