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Archives of Gynecology and Obstetrics

, Volume 299, Issue 3, pp 599–607 | Cite as

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

  • Xiaqin Huo
  • Liang Yao
  • Xue Han
  • Wen Li
  • Junjuan Liu
  • Lijun Zhou
  • Yuanfeng Gou
  • Kehu YangEmail author
  • Huiling LiuEmail author
Review

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.

Keywords

Hysterectomy Ovarian cancer Risk Meta-analysis 

Notes

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 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.

Compliance with ethical standards

Conflict of interest

No conflict of interest.

References

  1. 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):461–470PubMedPubMedCentralGoogle Scholar
  2. 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 222:113–118PubMedGoogle Scholar
  3. 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):121–129PubMedGoogle Scholar
  4. 4.
    Neis KJ, Zubke W, Fehr M, Romer T, Tamussino K, Nothacker M (2016) Hysterectomy for benign uterine disease. Dtsch Arztebl Int 113(14):242–249PubMedPubMedCentralGoogle Scholar
  5. 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. 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–S88PubMedGoogle Scholar
  7. 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 220:79–83PubMedGoogle Scholar
  8. 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 e193PubMedPubMedCentralGoogle Scholar
  9. 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):dju410PubMedGoogle Scholar
  10. 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):460–472PubMedGoogle Scholar
  11. 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 205:170–173PubMedGoogle Scholar
  12. 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):829–841PubMedGoogle Scholar
  13. 13.
    Rice MS, Murphy MA, Tworoger SS (2012) Tubal ligation, hysterectomy and ovarian cancer: a meta-analysis. J Ovarian Res 5(1):13PubMedPubMedCentralGoogle Scholar
  14. 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):3638–3647PubMedGoogle Scholar
  15. 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):1138PubMedCentralGoogle Scholar
  16. 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):2108–2120PubMedGoogle Scholar
  17. 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):733–743PubMedGoogle Scholar
  18. 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 100:86–91PubMedGoogle Scholar
  19. 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):727–734Google Scholar
  20. 20.
    Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634PubMedPubMedCentralGoogle Scholar
  21. 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):14–23PubMedGoogle Scholar
  22. 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):568–574PubMedGoogle Scholar
  23. 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):1072–1078PubMedGoogle Scholar
  24. 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):215–225PubMedGoogle Scholar
  25. 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):733–740PubMedGoogle Scholar
  26. 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):318–322PubMedGoogle Scholar
  27. 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):598–606PubMedPubMedCentralGoogle Scholar
  28. 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):188–196PubMedGoogle Scholar
  29. 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):2197–2206PubMedGoogle Scholar
  30. 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):1406–1417PubMedPubMedCentralGoogle Scholar
  31. 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):89–93Google Scholar
  32. 32.
    Pasalich M, Su D, Binns CW, Lee AH (2013) Reproductive factors for ovarian cancer in southern Chinese women. J Gynecol Oncol 24(2):135–140PubMedPubMedCentralGoogle Scholar
  33. 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):2415–2421PubMedPubMedCentralGoogle Scholar
  34. 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):46–53PubMedPubMedCentralGoogle Scholar
  35. 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–S69Google Scholar
  36. 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):363–373PubMedGoogle Scholar
  37. 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):153–159PubMedGoogle Scholar
  38. 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):2888–2898PubMedPubMedCentralGoogle Scholar
  39. 39.
    Kurman RJ, Shih Ie M (2011) Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 42(7):918–931PubMedPubMedCentralGoogle Scholar
  40. 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):298–304PubMedGoogle Scholar
  41. 42.
    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):55–67PubMedGoogle Scholar
  42. 43.
    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 85:50–58PubMedGoogle Scholar
  43. 44.
    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 74:73–79PubMedGoogle Scholar
  44. 41.
    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):385–394PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Gynecology and ObstetricsGansu Provincial People’s HospitalLanzhouPeople’s Republic of China
  2. 2.Department of Clinical MedicineGansu University of Traditional Chinese MedicineLanzhouPeople’s Republic of China
  3. 3.Evidence-Based Medicine Center, School of Basic Medical SciencesLanzhou UniversityLanzhouPeople’s Republic of China
  4. 4.Institution of Clinical Research and Evidence Based MedicineGansu Provincial HospitalLanzhouPeople’s Republic of China

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