Advertisement

Increased risk of osteoporosis with hysterectomy: A longitudinal follow-up study using a national sample cohort

Published:February 12, 2019DOI:https://doi.org/10.1016/j.ajog.2019.02.018

      Background

      Premenopausal hysterectomy is associated with a decreased ovarian reserve, follicular atresia, and subsequently reduced long-term estrogen secretion. Therefore, women who undergo hysterectomy will experience greater gradual bone mineral loss than women with an intact uterus and have an increased risk of osteoporosis.

      Objective

      This study aimed to evaluate the association between hysterectomy without/with bilateral oophorectomy and the occurrence of osteoporosis using a national sample cohort from South Korea.

      Study Design

      Using the national cohort study from the Korean National Health Insurance Service, we extracted data for patients who had undergone hysterectomy (n=9082) and for a 1:4 matched control group (n=36,328) and then analyzed the occurrence of osteoporosis. The patients were matched according to age, sex, income, region of residence, and medical history. A Cox proportional hazards model was used to analyze the hazard ratios and 95% confidence intervals. Subgroup analyses were performed based on age and bilateral oophorectomy status. The age of the participants was defined as the age at the time of hysterectomy.

      Results

      The adjusted hazard ratio for osteoporosis was 1.45 (95% confidence interval, 1.37–1.53, P<.001) in the hysterectomy group. The adjusted hazard ratios for osteoporosis in the different age subgroups of this group were 1.84 (95% confidence interval, 1.61–2.10) for ages 40–44 years, 1.52 (95% confidence interval, 1.39–1.66) for ages 45–49 years, 1.44 (95% confidence interval, 1.28–1.62) for ages 50–54 years, 1.61 (95% confidence interval, 1.33–1.96, all P<.001) for ages 55–59 years, and 1.08 (95% confidence interval, 0.95–1.23, P=.223) for ages ≥60 years. The adjusted hazard ratios for osteoporosis according to hysterectomy/oophorectomy status were 1.43 (95% confidence interval, 1.34–1.51) in the hysterectomy without bilateral oophorectomy group and 1.57 (95% confidence interval, 1.37–1.79) in the hysterectomy with bilateral oophorectomy group.

      Conclusion

      The occurrence of osteoporosis was increased in patients who had undergone hysterectomy compared with that in matched control subjects regardless of bilateral oophorectomy status.

      Key words

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to American Journal of Obstetrics & Gynecology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Glaser D.L.
        • Kaplan F.S.
        Osteoporosis. Definition and clinical presentation.
        Spine. 1997; 22: 12S-16S
        • Park E.J.
        • Joo I.W.
        • Jang M.J.
        • Kim Y.T.
        • Oh K.
        • Oh H.J.
        Prevalence of osteoporosis in the Korean population based on Korea National Health and Nutrition Examination Survey (KNHANES), 2008-2011.
        Yonsei Med J. 2014; 55: 1049-1057
        • van Geel T.A.
        • Geusens P.P.
        • Winkens B.
        • Sels J.P.
        • Dinant G.J.
        Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study.
        Eur J Endocrinol. 2009; 160: 681-687
        • Cauley J.A.
        • Danielson M.E.
        • Jammy G.R.
        • et al.
        Sex steroid hormones and fracture in a multiethnic cohort of women: the Women's Health Initiative Study (WHI).
        J Clin Endocrinol Metab. 2017; 102: 1538-1547
        • Faubion S.S.
        • Kuhle C.L.
        • Shuster L.T.
        • Rocca W.A.
        Long-term health consequences of premature or early menopause and considerations for management.
        Climacteric. 2015; 18: 483-491
        • Parker W.H.
        • Jacoby V.
        • Shoupe D.
        • Rocca W.
        Effect of bilateral oophorectomy on women's long-term health.
        Womens Health. 2009; 5: 565-576
        • Casiano E.R.
        • Trabuco E.C.
        • Bharucha A.E.
        • et al.
        Risk of oophorectomy after hysterectomy.
        Obstet Gynecol. 2013; 121: 1069-1074
        • Whiteman M.K.
        • Hillis S.D.
        • Jamieson D.J.
        • et al.
        Inpatient hysterectomy surveillance in the United States, 2000-2004.
        Am J Obstet Gynecol. 2008; 198: 34 e1-34 e7
        • Lee E.J.
        • Park H.M.
        Trends in laparoscopic surgery for hysterectomy in Korea between 2007 and 2009.
        J Obstet Gynaecol Res. 2014; 40: 1695-1699
        • Xiangying H.
        • Lili H.
        • Yifu S.
        The effect of hysterectomy on ovarian blood supply and endocrine function.
        Climacteric. 2006; 9: 283-289
        • Trabuco E.C.
        • Moorman P.G.
        • Algeciras-Schimnich A.
        • Weaver A.L.
        • Cliby W.A.
        Association of ovary-sparing hysterectomy with ovarian reserve.
        Obstet Gynecol. 2016; 127: 819-827
        • Abdelazim I.A.
        • Abdelrazak K.M.
        • Elbiaa A.A.
        • Farghali M.M.
        • Essam A.
        • Zhurabekova G.
        Ovarian function and ovarian blood supply following premenopausal abdominal hysterectomy.
        Prz Menopauzalny. 2015; 14: 238-242
        • Duraes Simoes R.
        • Chada Baracat E.
        • Szjenfeld V.L.
        • de Lima G.R.
        • Jose Goncalves W.
        • de Carvalho Ramos Bortoletto C.
        Effects of simple hysterectomy on bone loss.
        Sao Paulo Med J. 1995; 113: 1012-1015
        • Larcos G.
        Hysterectomy with ovarian conservation: effect on bone mineral density.
        Aust N Z J Obstet Gynaecol. 1998; 38: 452-454
        • Melton 3rd, L.J.
        • Achenbach S.J.
        • Gebhart J.B.
        • Babalola E.O.
        • Atkinson E.J.
        • Bharucha A.E.
        Influence of hysterectomy on long-term fracture risk.
        Fertil Steril. 2007; 88: 156-162
        • Lee J.
        • Lee J.S.
        • Park S.H.
        • Shin S.A.
        • Kim K.
        Cohort Profile: the National Health Insurance Service-National Sample Cohort (NHIS-NSC), South Korea.
        Int J Epidemiol. 2017; 46: e15
        • Clarke B.L.
        • Khosla S.
        Androgens and bone.
        Steroids. 2009; 74: 296-305
        • Cauley J.A.
        Estrogen and bone health in men and women.
        Steroids. 2015; 99: 11-15
        • Shoupe D.
        • Parker W.H.
        • Broder M.S.
        • Liu Z.
        • Farquhar C.
        • Berek J.S.
        Elective oophorectomy for benign gynecological disorders.
        Menopause. 2007; 14: 580-585
        • Berek J.S.
        • Chalas E.
        • Edelson M.
        • et al.
        Prophylactic and risk-reducing bilateral salpingo-oophorectomy: recommendations based on risk of ovarian cancer.
        Obstet Gynecol. 2010; 116: 733-743
        • Finch A.P.
        • Lubinski J.
        • Moller P.
        • et al.
        Impact of oophorectomy on cancer incidence and mortality in women with a BRCA1 or BRCA2 mutation.
        J Clin Oncol. 2014; 32: 1547-1553
        • Shuster L.T.
        • Gostout B.S.
        • Grossardt B.R.
        • Rocca W.A.
        Prophylactic oophorectomy in premenopausal women and long-term health.
        Menopause Int. 2008; 14: 111-116
        • Melton 3rd, L.J.
        • Khosla S.
        • Malkasian G.D.
        • Achenbach S.J.
        • Oberg A.L.
        • Riggs B.L.
        Fracture risk after bilateral oophorectomy in elderly women.
        J Bone Miner Res. 2003; 18: 900-905
        • Rodriguez M.
        • Shoupe D.
        Surgical Menopause.
        Endocrinol Metab Clin North Am. 2015; 44: 531-542
        • Ravn P.
        • Lind C.
        • Nilas L.
        Lack of influence of simple premenopausal hysterectomy on bone mass and bone metabolism.
        Am J Obstet Gynecol. 1995; 172: 891-895
        • Moorman P.G.
        • Myers E.R.
        • Schildkraut J.M.
        • Iversen E.S.
        • Wang F.
        • Warren N.
        Effect of hysterectomy with ovarian preservation on ovarian function.
        Obstet Gynecol. 2011; 118: 1271-1279
        • Petri Nahas E.A.
        • Pontes A.
        • Nahas-Neto J.
        • Borges V.T.
        • Dias R.
        • Traiman P.
        Effect of total abdominal hysterectomy on ovarian blood supply in women of reproductive age.
        J Ultrasound Med. 2005; 24: 169-174
        • Derksen J.G.
        • Brolmann H.A.
        • Wiegerinck M.A.
        • Vader H.L.
        • Heintz A.P.
        The effect of hysterectomy and endometrial ablation on follicle stimulating hormone (FSH) levels up to 1 year after surgery.
        Maturitas. 1998; 29: 133-138
        • Chalmers C.
        Does hysterectomy in a premenopausal woman affect ovarian function?.
        Med Hypotheses. 1996; 46: 573-575
        • Cheng S.
        • Sievanen H.
        • Heinonen A.
        • et al.
        Does hysterectomy with ovarian conservation affect bone metabolism and density?.
        J Bone Miner Metab. 2003; 21: 12-16
        • Kirchengast S.
        • Gruber D.
        • Sator M.
        • Huber J.
        Hysterectomy is associated with postmenopausal body composition characteristics.
        J Biosoc Sci. 2000; 32: 37-46
        • Park C.Y.
        • Lim J.Y.
        • Park H.Y.
        Age at natural menopause in Koreans: secular trends and influences thereon.
        Menopause. 2018; 25: 423-429
        • Davey D.A.
        Androgens in women before and after the menopause and post bilateral oophorectomy: clinical effects and indications for testosterone therapy.
        Womens Health. 2012; 8: 437-446
        • Gallagher J.C.
        Effect of early menopause on bone mineral density and fractures.
        Menopause. 2007; 14: 567-571
        • Mucowski S.J.
        • Mack W.J.
        • Shoupe D.
        • Kono N.
        • Paulson R.
        • Hodis H.N.
        Effect of prior oophorectomy on changes in bone mineral density and carotid artery intima-media thickness in postmenopausal women.
        Fertil Steril. 2014; 101: 1117-1122
        • Park M.B.
        • Kim C.B.
        • Nam E.W.
        • Hong K.S.
        Does South Korea have hidden female smokers: discrepancies in smoking rates between self-reports and urinary cotinine level.
        BMC Womens Health. 2014; 14: 156
        • Hong J.W.
        • Noh J.H.
        • Kim D.J.
        The prevalence of and factors associated with high-risk alcohol consumption in Korean adults: The 2009-2011 Korea National Health and Nutrition Examination Survey.
        PLoS One. 2017; 12: e0175299
        • Cho D.K.
        • Park H.M.
        The national use of hormonal therapy in postmenipausal women in 2010.
        J Korean Soc Menopause. 2011; 17: 150-154

      Linked Article

      • Reply
        American Journal of Obstetrics & GynecologyVol. 222Issue 1
        • Preview
          We thank Dr Morse for his interest and comments on our recent paper regarding hysterectomy and the risk of osteoporosis. Accordingly, we again reviewed our manuscript.
        • Full-Text
        • PDF
      • Hysterectomy and the risk of osteoporosis
        American Journal of Obstetrics & GynecologyVol. 222Issue 1
        • Preview
          I read with interest the study by Choi et al1 regarding the association of subsequent development of osteoporosis with previous hysterectomy. The completeness and universality of South Korea’s National Healthcare database is enviable. However, their singular focus on the possible loss of ovarian reserve as the explanation for this association does seems somewhat narrow. Although this is indeed a possible explanation, one should be somewhat circumspect about a finding of a modest increase in adjusted hazard ratios based on what is essentially an administrative claims database.
        • Full-Text
        • PDF
      • Additional procedures for measuring the effect of hysterectomy on osteoporosis
        American Journal of Obstetrics & GynecologyVol. 221Issue 2
        • Preview
          Choi et al1 analyzed the risk of osteoporosis in women who underwent hysterectomy using Korean insurance cohort data. The authors suggested that hysterectomy increases the risk of osteoporosis.1 The authors performed 1:4 matching according to age, income, and region of residence to reduce the bias in their study. Despite these efforts, however, there are some problems with the study.
        • Full-Text
        • PDF
      • Reply
        American Journal of Obstetrics & GynecologyVol. 221Issue 2
        • Preview
          We thank Dr Kim and his colleagues for their interest and comments on our recent paper regarding an additional procedure for measuring the effect of hysterectomy on osteoporosis. Accordingly, we again reviewed our manuscript. We know that several gynecological cancers can negatively affect bone directly or through cancer treatment, including chemotherapy and sex-hormone deprivation therapy.1
        • Full-Text
        • PDF