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Published in: Archives of Gynecology and Obstetrics 3/2019

01-03-2019 | Ovarian Cancer | Review

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

Authors: Xiaqin Huo, Liang Yao, Xue Han, Wen Li, Junjuan Liu, Lijun Zhou, Yuanfeng Gou, Kehu Yang, Huiling Liu

Published in: Archives of Gynecology and Obstetrics | Issue 3/2019

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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.
Literature
1.
go back to reference 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):461–470CrossRef 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):461–470CrossRef
2.
go back to reference 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 222:113–118CrossRef 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 222:113–118CrossRef
3.
go back to reference 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):121–129CrossRef 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):121–129CrossRef
4.
go back to reference Neis KJ, Zubke W, Fehr M, Romer T, Tamussino K, Nothacker M (2016) Hysterectomy for benign uterine disease. Dtsch Arztebl Int 113(14):242–249PubMedPubMedCentral Neis KJ, Zubke W, Fehr M, Romer T, Tamussino K, Nothacker M (2016) Hysterectomy for benign uterine disease. Dtsch Arztebl Int 113(14):242–249PubMedPubMedCentral
5.
go back to reference 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) 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)
6.
go back to reference 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–S88CrossRef 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–S88CrossRef
7.
go back to reference 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 220:79–83CrossRef 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 220:79–83CrossRef
8.
go back to reference 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 e193CrossRef 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 e193CrossRef
9.
go back to reference 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):dju410CrossRef 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):dju410CrossRef
10.
go back to reference 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):460–472CrossRef 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):460–472CrossRef
11.
go back to reference 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 205:170–173CrossRef 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 205:170–173CrossRef
12.
go back to reference 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):829–841CrossRef 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):829–841CrossRef
13.
go back to reference Rice MS, Murphy MA, Tworoger SS (2012) Tubal ligation, hysterectomy and ovarian cancer: a meta-analysis. J Ovarian Res 5(1):13CrossRef Rice MS, Murphy MA, Tworoger SS (2012) Tubal ligation, hysterectomy and ovarian cancer: a meta-analysis. J Ovarian Res 5(1):13CrossRef
14.
go back to reference 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):3638–3647CrossRef 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):3638–3647CrossRef
15.
go back to reference 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):1138CrossRef 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):1138CrossRef
16.
go back to reference 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):2108–2120CrossRef 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):2108–2120CrossRef
17.
go back to reference 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):733–743CrossRef 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):733–743CrossRef
18.
go back to reference 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 100:86–91CrossRef 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 100:86–91CrossRef
19.
go back to reference 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 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
20.
go back to reference Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634CrossRef Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634CrossRef
21.
go back to reference 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):14–23CrossRef 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):14–23CrossRef
22.
go back to reference Modugno F, Ness RB, Wheeler JE (2001) Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Ann Epidemiol 11(8):568–574CrossRef Modugno F, Ness RB, Wheeler JE (2001) Reproductive risk factors for epithelial ovarian cancer according to histologic type and invasiveness. Ann Epidemiol 11(8):568–574CrossRef
23.
go back to reference 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):1072–1078CrossRef 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):1072–1078CrossRef
24.
go back to reference 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):215–225CrossRef 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):215–225CrossRef
25.
go back to reference 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):733–740CrossRef 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):733–740CrossRef
26.
go back to reference 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):318–322CrossRef 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):318–322CrossRef
27.
go back to reference 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):598–606CrossRef 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):598–606CrossRef
28.
go back to reference 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):188–196CrossRef 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):188–196CrossRef
29.
go back to reference 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):2197–2206CrossRef 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):2197–2206CrossRef
30.
go back to reference 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):1406–1417CrossRef 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):1406–1417CrossRef
31.
go back to reference 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):89–93CrossRef 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):89–93CrossRef
32.
go back to reference Pasalich M, Su D, Binns CW, Lee AH (2013) Reproductive factors for ovarian cancer in southern Chinese women. J Gynecol Oncol 24(2):135–140CrossRef Pasalich M, Su D, Binns CW, Lee AH (2013) Reproductive factors for ovarian cancer in southern Chinese women. J Gynecol Oncol 24(2):135–140CrossRef
33.
go back to reference 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):2415–2421CrossRef 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):2415–2421CrossRef
34.
go back to reference 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):46–53CrossRef 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):46–53CrossRef
35.
go back to reference 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 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
36.
go back to reference 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):363–373CrossRef 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):363–373CrossRef
37.
go back to reference 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):153–159CrossRef 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):153–159CrossRef
38.
go back to reference 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):2888–2898CrossRef 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):2888–2898CrossRef
39.
go back to reference Kurman RJ, Shih Ie M (2011) Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 42(7):918–931CrossRef Kurman RJ, Shih Ie M (2011) Molecular pathogenesis and extraovarian origin of epithelial ovarian cancer-shifting the paradigm. Hum Pathol 42(7):918–931CrossRef
40.
go back to reference 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):298–304CrossRef 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):298–304CrossRef
42.
go back to reference 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):55–67CrossRef 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):55–67CrossRef
43.
go back to reference 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 85:50–58CrossRef 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 85:50–58CrossRef
44.
go back to reference 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 74:73–79CrossRef 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 74:73–79CrossRef
41.
go back to reference 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):385–394CrossRef 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):385–394CrossRef
Metadata
Title
Hysterectomy and risk of ovarian cancer: a systematic review and meta-analysis
Authors
Xiaqin Huo
Liang Yao
Xue Han
Wen Li
Junjuan Liu
Lijun Zhou
Yuanfeng Gou
Kehu Yang
Huiling Liu
Publication date
01-03-2019
Publisher
Springer Berlin Heidelberg
Published in
Archives of Gynecology and Obstetrics / Issue 3/2019
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-018-5020-1

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