Skip to main content
SpringerLink
Log in

Hysterectomy and risk of ovarian cancer: a systematic review and meta-analysis

  • Review
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

The association between hysterectomy for benign gynecologic disease and ovarian cancer risk was controversial. Thus, we perform a systematic review and meta-analysis to evaluate the effect of hysterectomy and ovarian cancer risk.

Methods

PubMed, Cochrane Library, and Embase were searched from 2000 toJanuary 2018. A random-effect model was used to obtain the summary odds risks (ORs) and 95% confidence intervals (CIs).

Results

A total of 18 case–control studies were included in the meta-analysis. We found that there was no statistical significance for ovarian cancer risk following hysterectomy (OR 0.97, 95% CI 0.83–1.12). And in subgroup analysis, the protective effects were observed for invasive endometrioid/clear cell carcinomas after hysterectomy (OR 0.70, 95% CI 0.51, 0.94; I2 = 0%), and no statistical significance for serous and mucinous.

Conclusions

Hysterectomy showed no relationship with ovarian cancer. But a reduced risk was found for endometrioid-invasive OC. These findings could provide evidence for patients with benign gynecological disease and clinicians to make appropriate decision about whether to conduct hysterectomy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2
Fig 3
Fig 4

Similar content being viewed by others

References

  1. Dessources K, Hou JY, Tergas AI, Burke WM, Ananth CV, Prendergast E et al (2015) Factors associated with 30-day hospital readmission after hysterectomy. Obstet Gynecol 125(2):461–470

    Article  Google Scholar 

  2. Billfeldt NK, Borgfeldt C, Lindkvist H, Stjerndahl JH, Ankardal M (2018) A Swedish population-based evaluation of benign hysterectomy, comparing minimally invasive and abdominal surgery. Eur J Obstet Gynecol Reprod Biol 222:113–118

    Article  Google Scholar 

  3. Louie M, Spencer J, Wheeler S, Ellis V, Toubia T, Schiff LD et al (2017) Comparison of the levonorgestrel-releasing intrauterine system, hysterectomy, and endometrial ablation for heavy menstrual bleeding in a decision analysis model. Int J Gynaecol Obstet 139(2):121–129

    Article  Google Scholar 

  4. Neis KJ, Zubke W, Fehr M, Romer T, Tamussino K, Nothacker M (2016) Hysterectomy for benign uterine disease. Dtsch Arztebl Int 113(14):242–249

    PubMed  PubMed Central  Google Scholar 

  5. de Bruijn AM, Ankum WM, Reekers JA, Birnie E, van der Kooij SM, Volkers NA et al (2016) Uterine artery embolization vs hysterectomy in the treatment of symptomatic uterine fibroids: 10-year outcomes from the randomized emmy trial. Am J Obstet Gynecol 215(6) 745:e741–e745 (e712)

    Google Scholar 

  6. Cayrac M, Warembourg S, Le Normand L, Fatton B (2016) L’hystérectomie modifie-t-elle les résultats anatomiques et fonctionnels de la cure de prolapsus ? Recommandations pour la pratique clinique. Progrès en Urologie 26:S73–S88

    Article  Google Scholar 

  7. van IJsselmuiden MN, Detollenaere RJ, Gerritse MBE, Kluivers KB, Bongers MY, van Eijndhoven HWF, (2018) Dutch women's attitudes towards hysterectomy and uterus preservation in surgical treatment of pelvic organ prolapse. Eur J Obstet Gynecol Reprod Biol 220:79–83

    Article  Google Scholar 

  8. Rice MS, Hankinson SE, Tworoger SS (2014) Tubal ligation, hysterectomy, unilateral oophorectomy, and risk of ovarian cancer in the nurses' health studies. Fertil Steril 102(1):192–198 e193

    Article  Google Scholar 

  9. Falconer H, Yin L, Gronberg H, Altman D (2015) Ovarian cancer risk after salpingectomy: a nationwide population-based study. J Natl Cancer Inst 107(2):dju410

    Article  Google Scholar 

  10. Peres LC, Risch H, Terry KL, Webb PM, Goodman MT, Wu AH et al (2018) Racial/ethnic differences in the epidemiology of ovarian cancer: a pooled analysis of 12 case–control studies. Int J Epidemiol 47(2):460–472

    Article  Google Scholar 

  11. Ruiz MP, Morales-Ramirez PB, Dziadek OL, Algren SD (2016) Epithelial ovarian cancer and type of peritoneal insult: a case–control study. Eur J Obstet Gynecol Reprod Biol 205:170–173

    Article  Google Scholar 

  12. Le ND, Leung A, Brooks-Wilson A, Gallagher RP, Swenerton KD, Demers PA et al (2014) Occupational exposure and ovarian cancer risk. Cancer Causes Control 25(7):829–841

    Article  Google Scholar 

  13. Rice MS, Murphy MA, Tworoger SS (2012) Tubal ligation, hysterectomy and ovarian cancer: a meta-analysis. J Ovarian Res 5(1):13

    Article  Google Scholar 

  14. Jordan SJ, Nagle CM, Coory MD, Maresco D, Protani MM, Pandeya NA et al (2013) Has the association between hysterectomy and ovarian cancer changed over time? A systematic review and meta-analysis. Eur J Cancer 49(17):3638–3647

    Article  Google Scholar 

  15. Wang C, Liang Z, Liu X, Zhang Q, Li S (2016) The association between endometriosis, tubal ligation, hysterectomy and epithelial ovarian cancer: meta-analyses. Int J Environ Res Public Health 13(11):1138

    Article  Google Scholar 

  16. Walker JL, Powell CB, Chen LM, Carter J, Bae Jump VL, Parker LP et al (2015) Society of gynecologic oncology recommendations for the prevention of ovarian cancer. Cancer 121(13):2108–2120

    Article  Google Scholar 

  17. Berek JS, Chalas E, Edelson M, Moore DH, Burke WM, Cliby WA et al (2010) Prophylactic and risk-reducing bilateral salpingo-oophorectomy: recommendations based on risk of ovarian cancer. Obstet Gynecol 116(3):733–743

    Article  Google Scholar 

  18. Perez-Lopez FR, Ceausu I, Depypere H, Kehoe S, Lambrinoudaki I, Mueck A et al (2017) Interventions to reduce the risk of ovarian and fallopian tube cancer: a European menopause and andropause society postition statement. Maturitas 100:86–91

    Article  Google Scholar 

  19. Wells GA, Shea BJ, O'Connell D, Peterson J, Welch V, Losos M et al (2014) The newcastle–ottawa scale (nos) for assessing the quality of non-randomized studies in meta-analysis. Appl Eng Agric 18(6):727–734

    Google Scholar 

  20. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  Google Scholar 

  21. Beard CM, Hartmann LC, Atkinson EJ, O'Brien PC, Malkasian GD, Keeney GL et al (2000) The epidemiology of ovarian cancer: a population-based study in olmsted county, minnesota, 1935–1991. Ann Epidemiol 10(1):14–23

    Article  CAS  Google Scholar 

  22. Modugno F, Ness RB, Wheeler JE (2001) Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Ann Epidemiol 11(8):568–574

    Article  CAS  Google Scholar 

  23. Rutter JL, Wacholder S, Chetrit A, Lubin F, Menczer J, Ebbers S et al (2003) Gynecologic surgeries and risk of ovarian cancer in women with brca1 and brca2 ashkenazi founder mutations: an israeli population-based case–control study. JNCI J Natl Cancer Inst 95(14):1072–1078

    Article  Google Scholar 

  24. Mills PK, Riordan DG, Cress RD (2004) Epithelial ovarian cancer risk by invasiveness and cell type in the central valley of california. Gynecol Oncol 95(1):215–225

    Article  Google Scholar 

  25. Modugno F, Ness RB, Allen GO, Schildkraut JM, Davis FG, Goodman MT (2004) Oral contraceptive use, reproductive history, and risk of epithelial ovarian cancer in women with and without endometriosis. Am J Obstet Gynecol 191(3):733–740

    Article  Google Scholar 

  26. Chiaffarino F, Parazzini F, Decarli A, Franceschi S, Talamini R, Montella M et al (2005) Hysterectomy with or without unilateral oophorectomy and risk of ovarian cancer. Gynecol Oncol 97(2):318–322

    Article  Google Scholar 

  27. Moorman PG, Palmieri RT, Akushevich L, Berchuck A, Schildkraut JM (2009) Ovarian cancer risk factors in african-american and white women. Am J Epidemiol 170(5):598–606

    Article  Google Scholar 

  28. Ness RB, Dodge RC, Edwards RP, Baker JA, Moysich KB (2011) Contraception methods, beyond oral contraceptives and tubal ligation, and risk of ovarian cancer. Ann Epidemiol 21(3):188–196

    Article  Google Scholar 

  29. Faber MT, Jensen A, Frederiksen K, Glud E, Hogdall E, Hogdall C et al (2013) Oral contraceptive use and impact of cumulative intake of estrogen and progestin on risk of ovarian cancer. Cancer Causes Control 24(12):2197–2206

    Article  CAS  Google Scholar 

  30. 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(5):1406–1417

    Article  CAS  Google Scholar 

  31. Pajenga E, Rexha T, Çeliku S, Bejtja G, Pisha M (2013) Hormonal risk factors for ovarian cancer in the albanian case–control study. Bos J Basic Med Sci 13(2):89–93

    Article  Google Scholar 

  32. Pasalich M, Su D, Binns CW, Lee AH (2013) Reproductive factors for ovarian cancer in southern Chinese women. J Gynecol Oncol 24(2):135–140

    Article  Google Scholar 

  33. Rice MS, Murphy MA, Vitonis AF, Cramer DW, Titus LJ, Tworoger SS et al (2013) Tubal ligation, hysterectomy and epithelial ovarian cancer in the new England case–control study. Int J Cancer 133(10):2415–2421

    Article  CAS  Google Scholar 

  34. Peres LC, Alberg AJ, Bandera EV, Barnholtz-Sloan J, Bondy M, Cote ML et al (2017) Premenopausal hysterectomy and risk of ovarian cancer in African–American women. Am J Epidemiol 186(1):46–53

    Article  Google Scholar 

  35. Kupelian V, Davis F, Mallin K, Rosenblatt K (2000) Tubal sterilization, hysterectomy and risk of ovarian cancer: a case–control study. Am J Epidemiol 151(11):S69–S69

    Google Scholar 

  36. Riman T, Dickman PW, Nilsson S, Correia N, Nordlinder H, Magnusson CM et al (2002) Risk factors for invasive epithelial ovarian cancer: results from a Swedish case–control study. Am J Epidemiol 156(4):363–373

    Article  Google Scholar 

  37. Chene G, Rahimi K, Mesmasson AM, Provencher D (2013) Surgical implications of the potential new tubal pathway for ovarian carcinogenesis. J Minim Invasive Gynecol 20(2):153–159

    Article  Google Scholar 

  38. Wentzensen N, Poole EM, Trabert B, White E, Arslan AA, Patel AV et al (2016) Ovarian cancer risk factors by histologic subtype: An analysis from the ovarian cancer cohort consortium. J Clin Oncol 34(24):2888–2898

    Article  CAS  Google Scholar 

  39. Kurman RJ, Shih Ie M (2011) Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 42(7):918–931

    Article  CAS  Google Scholar 

  40. Ogawa S, Kaku T, Amada S, Kobayashi H, Hirakawa T, Ariyoshi K et al (2000) Ovarian endometriosis associated with ovarian carcinoma: a clinicopathological and immunohistochemical study. Gynecol Oncol 77(2):298–304

    Article  CAS  Google Scholar 

  41. Cibula D, Widschwendter M, Májek O, Dusek L (2011) Tubal ligation and the risk of ovarian cancer: review and meta-analysis. Hum Reprod Update 17(1):55–67

    Article  CAS  Google Scholar 

  42. Tian J, Zhang J, Ge L, Yang K, Song F (2017) The methodological and reporting quality of systematic reviews from china and the USA are similar. J Clin Epidemiol 85:50–58

    Article  Google Scholar 

  43. Yao L, Sun R, Chen YL, Wang Q, Wei D, Wang X et al (2016) The quality of evidence in chinese meta-analyses needs to be improved. J Clin Epidemiol 74:73–79

    Article  Google Scholar 

  44. Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM et al (2012) Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol 13(4):385–394

    Article  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Natural Science Foundation of China (Project No. 81560426) and the Research Project of Gansu Provincial People’s Hospital in China (No. 16GSSY6-8).

Author information

Author notes

  1. Xiaqin Huo and Liang Yao are co-first authors.

Authors and Affiliations

  1. Department of Gynecology and Obstetrics, Gansu Provincial People’s Hospital, Donggang West Road, Lanzhou, 730000, People’s Republic of China

    Xiaqin Huo, Xue Han, Wen Li, Junjuan Liu, Lijun Zhou, Yuanfeng Gou & Huiling Liu

  2. Department of Clinical Medicine, Gansu University of Traditional Chinese Medicine, Lanzhou, 730000, People’s Republic of China

    Xiaqin Huo, Wen Li, Junjuan Liu, Lijun Zhou, Yuanfeng Gou & Huiling Liu

  3. Evidence-Based Medicine Center, School of Basic Medical Sciences, Lanzhou University, 199 Donggang West Road, Lanzhou, 730000, People’s Republic of China

    Xiaqin Huo, Liang Yao & Kehu Yang

  4. Institution of Clinical Research and Evidence Based Medicine, Gansu Provincial Hospital, Lanzhou, 730000, People’s Republic of China

    Xiaqin Huo, Liang Yao & Kehu Yang

Authors
  1. Xiaqin Huo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liang Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xue Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wen Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Junjuan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lijun Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanfeng Gou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kehu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Huiling Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XH and LY: Project development, data collection, manuscript writing/editing. XH and WL: Project development, data analysis, manuscript editing. JL, LZ and YG: Project development. KY and HL: Project development, manuscript editing.

Corresponding authors

Correspondence to Kehu Yang or Huiling Liu.

Ethics declarations

Conflict of interest

No conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huo, X., Yao, L., Han, X. et al. Hysterectomy and risk of ovarian cancer: a systematic review and meta-analysis. Arch Gynecol Obstet 299, 599–607 (2019). https://doi.org/10.1007/s00404-018-5020-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-018-5020-1

Keywords

Search

Navigation