Are Oxidative Stress and Inflammation Mediators of Bone Loss Due to Estrogen Deficiency? A Review of Current Evidence

Author(s): Nur-Vaizura Mohamad, Soelaiman Ima-Nirwana, Kok-Yong Chin*

Journal Name: Endocrine, Metabolic & Immune Disorders - Drug Targets
Formerly Current Drug Targets - Immune, Endocrine & Metabolic Disorders

Volume 20 , Issue 9 , 2020


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Graphical Abstract:


Abstract:

Osteoporosis is one of the major health issues associated with menopause-related estrogen deficiency. Various reports suggest that the hormonal changes related to menopausal transition may lead to the derangement of redox homeostasis and ultimately oxidative stress. Estrogen deficiency and oxidative stress may enhance the expression of genes involved in inflammation. All these factors may contribute, in synergy, to the development of postmenopausal osteoporosis. Previous studies suggest that estrogen may act as an antioxidant to protect the bone against oxidative stress, and as an antiinflammatory agent in suppressing pro-inflammatory and pro-osteoclastic cytokines. Thus, the focus of the current review is to examine the relationship between estrogen deficiency, oxidative stress and inflammation, and the impacts of these phenomena on skeletal health in postmenopausal women.

Keywords: Inflammation, menopause, estrogen, osteoporosis, oxidative stress, review.

[1]
Gallagher, J.C.; Goldgar, D.; Moy, A. Total bone calcium in normal women: effect of age and menopause status. J. Bone Miner. Res., 1987, 2(6), 491-496.
[http://dx.doi.org/10.1002/jbmr.5650020605 ] [PMID: 3455633]
[2]
Gauthier, A.; Kanis, J.A.; Jiang, Y.; Martin, M.; Compston, J.E.; Borgström, F.; Cooper, C.; McCloskey, E.V. Epidemiological burden of postmenopausal osteoporosis in the UK from 2010 to 2021: estimations from a disease model. Arch. Osteoporos., 2011, 6(1-2), 179-188.
[http://dx.doi.org/10.1007/s11657-011-0063-y ] [PMID: 22886104]
[3]
Simpson, E.R. Sources of estrogen and their importance. J. Steroid Biochem. Mol. Biol., 2003, 86(3-5), 225-230.
[http://dx.doi.org/10.1016/S0960-0760(03)00360-1 ] [PMID: 14623515]
[4]
Riggs, B.L.; Melton, L.J., III The prevention and treatment of osteoporosis. N. Engl. J. Med., 1992, 327(9), 620-627.
[http://dx.doi.org/10.1056/NEJM199208273270908 ] [PMID: 1640955]
[5]
Vrtačnik, P.; Ostanek, B.; Mencej-Bedrač, S.; Marc, J. The many faces of estrogen signaling. Biochem. Med. (Zagreb), 2014, 24(3), 329-342.
[http://dx.doi.org/10.11613/BM.2014.035 ] [PMID: 25351351]
[6]
Madeddu, C.; Gramignano, G.; Floris, C.; Murenu, G.; Sollai, G.; Macciò, A. Role of inflammation and oxidative stress in post-menopausal oestrogen-dependent breast cancer. J. Cell. Mol. Med., 2014, 18(12), 2519-2529.
[http://dx.doi.org/10.1111/jcmm.12413 ] [PMID: 25338520]
[7]
Signorelli, S.S.; Neri, S.; Sciacchitano, S.; Pino, L.D.; Costa, M.P.; Marchese, G.; Celotta, G.; Cassibba, N.; Pennisi, G.; Caschetto, S. Behaviour of some indicators of oxidative stress in postmenopausal and fertile women. Maturitas, 2006, 53(1), 77-82.
[http://dx.doi.org/10.1016/j.maturitas.2005.03.001 ] [PMID: 16325025]
[8]
McLean, R.R. Proinflammatory cytokines and osteoporosis. Curr. Osteoporos. Rep., 2009, 7(4), 134-139.
[http://dx.doi.org/10.1007/s11914-009-0023-2 ] [PMID: 19968917]
[9]
Cervellati, C.; Bonaccorsi, G.; Cremonini, E.; Bergamini, C.M.; Patella, A.; Castaldini, C.; Ferrazzini, S.; Capatti, A.; Picarelli, V.; Pansini, F.S.; Massari, L. Bone mass density selectively correlates with serum markers of oxidative damage in post-menopausal women. Clin. Chem. Lab. Med., 2013, 51(2), 333-338.
[http://dx.doi.org/10.1515/cclm-2012-0095 ] [PMID: 23089610]
[10]
Simpson, E.R.; Clyne, C.; Rubin, G.; Boon, W.C.; Robertson, K.; Britt, K.; Speed, C.; Jones, M. Aromatase--a brief overview. Annu. Rev. Physiol., 2002, 64(1), 93-127.
[http://dx.doi.org/10.1146/annurev.physiol.64.081601.142703 ] [PMID: 11826265]
[11]
Mauvais-Jarvis, F.; Clegg, D.J.; Hevener, A.L. The role of estrogens in control of energy balance and glucose homeostasis. Endocr. Rev., 2013, 34(3), 309-338.
[http://dx.doi.org/10.1210/er.2012-1055 ] [PMID: 23460719]
[12]
Faulds, M.H.; Zhao, C.; Dahlman-Wright, K.; Gustafsson, J-Å. The diversity of sex steroid action: Regulation of metabolism by estrogen signaling. J. Endocrinol., 2012, 212(1), 3-12.
[http://dx.doi.org/10.1530/JOE-11-0044 ] [PMID: 21511884]
[13]
Green, S.; Kumar, V.; Krust, A.; Walter, P.; Chambon, P. Cold. Spring. Harb. Symp. Quant. Biol; Cold Spring Harbor Laboratory Press, 1986, Vol. 51, pp. 751-758.
[14]
Kuiper, G.G.; Enmark, E.; Pelto-Huikko, M.; Nilsson, S.; Gustafsson, J-A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA, 1996, 93(12), 5925-5930.
[http://dx.doi.org/10.1073/pnas.93.12.5925 ] [PMID: 8650195]
[15]
Stice, J.P.; Knowlton, A.A. Estrogen, NFkappaB, and the heat shock response. Mol. Med., 2008, 14(7-8), 517-527.
[http://dx.doi.org/10.2119/2008-00026.Stice ] [PMID: 18431462]
[16]
Kuiper, G.G.; Carlsson, B.; Grandien, K.; Enmark, E.; Häggblad, J.; Nilsson, S.; Gustafsson, J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology, 1997, 138(3), 863-870.
[http://dx.doi.org/10.1210/endo.138.3.4979 ] [PMID: 9048584]
[17]
Björnström, L.; Sjöberg, M. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol., 2005, 19(4), 833-842.
[http://dx.doi.org/10.1210/me.2004-0486 ] [PMID: 15695368]
[18]
Börjesson, A.E.; Lagerquist, M.K.; Windahl, S.H.; Ohlsson, C. The role of estrogen receptor α in the regulation of bone and growth plate cartilage. Cell. Mol. Life Sci., 2013, 70(21), 4023-4037.
[http://dx.doi.org/10.1007/s00018-013-1317-1 ] [PMID: 23516016]
[19]
Bord, S.; Horner, A.; Beavan, S.; Compston, J. Estrogen receptors α and β are differentially expressed in developing human bone. J. Clin. Endocrinol. Metab., 2001, 86(5), 2309-2314.
[http://dx.doi.org/10.1210/jc.86.5.2309 ] [PMID: 11344243]
[20]
Braidman, I.P.; Hainey, L.; Batra, G.; Selby, P.L.; Saunders, P.T.; Hoyland, J.A. Localization of estrogen receptor β protein expression in adult human bone. J. Bone Miner. Res., 2001, 16(2), 214-220.
[http://dx.doi.org/10.1359/jbmr.2001.16.2.214 ] [PMID: 11204421]
[21]
Crusodé de Souza, M.; Sasso-Cerri, E.; Cerri, P.S. Immunohistochemical detection of estrogen receptor beta in alveolar bone cells of estradiol-treated female rats: possible direct action of estrogen on osteoclast life span. J. Anat., 2009, 215(6), 673-681.
[http://dx.doi.org/10.1111/j.1469-7580.2009.01158.x ] [PMID: 19930518]
[22]
Kovats, S. Estrogen receptors regulate innate immune cells and signaling pathways. Cell. Immunol., 2015, 294(2), 63-69.
[http://dx.doi.org/10.1016/j.cellimm.2015.01.018 ] [PMID: 25682174]
[23]
Härkönen, P.L.; Väänänen, H.K. Monocyte-macrophage system as a target for estrogen and selective estrogen receptor modulators. Ann. N. Y. Acad. Sci., 2006, 1089(1), 218-227.
[http://dx.doi.org/10.1196/annals.1386.045 ] [PMID: 17261769]
[24]
Karsenty, G.; Wagner, E.F. Reaching a genetic and molecular understanding of skeletal development. Dev. Cell, 2002, 2(4), 389-406.
[http://dx.doi.org/10.1016/S1534-5807(02)00157-0 ] [PMID: 11970890]
[25]
Hadjidakis, D.J.; Androulakis, I.I. Bone remodeling. Ann. N. Y. Acad. Sci., 2006, 1092, 385-396.
[http://dx.doi.org/10.1196/annals.1365.035 ] [PMID: 17308163]
[26]
Väänänen, H.K.; Härkönen, P.L. Estrogen and bone metabolism. Maturitas, 1996(Suppl. 23), S65-S69.
[http://dx.doi.org/10.1016/0378-5122(96)01015-8 ] [PMID: 8865143]
[27]
Florencio-Silva, R.; Sasso, G.R.S.; Sasso-Cerri, E.; Simões, M.J.; Cerri, P.S. Effects of estrogen status in osteocyte autophagy and its relation to osteocyte viability in alveolar process of ovariectomized rats. Biomed. Pharmacother., 2018, 98, 406-415.
[http://dx.doi.org/10.1016/j.biopha.2017.12.089 ] [PMID: 29276969]
[28]
Garnero, P.; Sornay-Rendu, E.; Chapuy, M.C.; Delmas, P.D. Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. J. Bone Miner. Res., 1996, 11(3), 337-349.
[http://dx.doi.org/10.1002/jbmr.5650110307 ] [PMID: 8852944]
[29]
Manolagas, S.C. Birth and death of bone cells: Basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr. Rev., 2000, 21(2), 115-137.
[PMID: 10782361]
[30]
Kousteni, S.; Chen, J.R.; Bellido, T.; Han, L.; Ali, A.A.; O’Brien, C.A.; Plotkin, L.; Fu, Q.; Mancino, A.T.; Wen, Y.; Vertino, A.M.; Powers, C.C.; Stewart, S.A.; Ebert, R.; Parfitt, A.M.; Weinstein, R.S.; Jilka, R.L.; Manolagas, S.C. Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science, 2002, 298(5594), 843-846.
[http://dx.doi.org/10.1126/science.1074935 ] [PMID: 12399595]
[31]
Khosla, S.; Atkinson, E.J.; Dunstan, C.R.; O’Fallon, W.M. Effect of estrogen versus testosterone on circulating osteoprotegerin and other cytokine levels in normal elderly men. J. Clin. Endocrinol. Metab., 2002, 87(4), 1550-1554.
[http://dx.doi.org/10.1210/jcem.87.4.8397 ] [PMID: 11932280]
[32]
Takahashi, N.; Udagawa, N.; Akatsu, T.; Tanaka, H.; Isogai, Y.; Suda, T. Deficiency of osteoclasts in osteopetrotic mice is due to a defect in the local microenvironment provided by osteoblastic cells. Endocrinology, 1991, 128(4), 1792-1796.
[http://dx.doi.org/10.1210/endo-128-4-1792 ] [PMID: 2004603]
[33]
Boyle, W.J.; Simonet, W.S.; Lacey, D.L. Osteoclast differentiation and activation. Nature, 2003, 423(6937), 337-342.
[http://dx.doi.org/10.1038/nature01658 ] [PMID: 12748652]
[34]
Hofbauer, L.C.; Khosla, S.; Dunstan, C.R.; Lacey, D.L.; Boyle, W.J.; Riggs, B.L. The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J. Bone Miner. Res., 2000, 15(1), 2-12.
[http://dx.doi.org/10.1359/jbmr.2000.15.1.2 ] [PMID: 10646108]
[35]
Shevde, N.K.; Bendixen, A.C.; Dienger, K.M.; Pike, J.W. Estrogens suppress RANK ligand-induced osteoclast differentiation via a stromal cell independent mechanism involving c-Jun repression. Proc. Natl. Acad. Sci. USA, 2000, 97(14), 7829-7834.
[http://dx.doi.org/10.1073/pnas.130200197 ] [PMID: 10869427]
[36]
Bord, S.; Ireland, D.C.; Beavan, S.R.; Compston, J.E. The effects of estrogen on osteoprotegerin, RANKL, and estrogen receptor expression in human osteoblasts. Bone, 2003, 32(2), 136-141.
[http://dx.doi.org/10.1016/S8756-3282(02)00953-5 ] [PMID: 12633785]
[37]
Nakamura, T.; Imai, Y.; Matsumoto, T.; Sato, S.; Takeuchi, K.; Igarashi, K.; Harada, Y.; Azuma, Y.; Krust, A.; Yamamoto, Y.; Nishina, H.; Takeda, S.; Takayanagi, H.; Metzger, D.; Kanno, J.; Takaoka, K.; Martin, T.J.; Chambon, P.; Kato, S. Estrogen prevents bone loss via estrogen receptor α and induction of Fas ligand in osteoclasts. Cell, 2007, 130(5), 811-823.
[http://dx.doi.org/10.1016/j.cell.2007.07.025 ] [PMID: 17803905]
[38]
Melville, K.M.; Kelly, N.H.; Khan, S.A.; Schimenti, J.C.; Ross, F.P.; Main, R.P.; van der Meulen, M.C. Female mice lacking estrogen receptor-alpha in osteoblasts have compromised bone mass and strength. J. Bone Miner. Res., 2014, 29(2), 370-379.
[http://dx.doi.org/10.1002/jbmr.2082 ] [PMID: 24038209]
[39]
Hart, N.H.; Nimphius, S.; Rantalainen, T.; Ireland, A.; Siafarikas, A.; Newton, R.U. Mechanical basis of bone strength: Influence of bone material, bone structure and muscle action. J. Musculoskelet. Neuronal Interact., 2017, 17(3), 114-139.
[PMID: 28860414]
[40]
Deng, Y-T.; Kang, W-B.; Zhao, J-N.; Liu, G.; Zhao, M-G. Osteoprotective effect of echinocystic acid, a triterpone component from eclipta prostrata, in ovariectomy-induced osteoporotic rats. PLoS One, 2015, 10(8), e0136572-e0136572.
[http://dx.doi.org/10.1371/journal.pone.0136572 ] [PMID: 26317835]
[41]
Parvaneh, K.; Ebrahimi, M.; Sabran, M.R.; Karimi, G.; Hwei, A.N.; Abdul-Majeed, S.; Ahmad, Z.; Ibrahim, Z.; Jamaluddin, R. Probiotics (Bifidobacterium longum) Increase Bone Mass Density and Upregulate Sparc and Bmp-2 Genes in Rats with Bone Loss Resulting from Ovariectomy. BioMed Res. Int., 2015, 2015 897639
[http://dx.doi.org/10.1155/2015/897639 ] [PMID: 26366421]
[42]
Fernández-Murga, M.L.; Vinué, Á.; Caeiro, J.R.; Guede, D.; Tarín, J.J.; Andrés, V.; Cano, A. Impact of estrogens on atherosclerosis and bone in the apolipoprotein E-deficient mouse model. Menopause, 2015, 22(4), 428-436.
[http://dx.doi.org/10.1097/GME.0000000000000328 ] [PMID: 25203894]
[43]
Du, Z.; Steck, R.; Doan, N.; Woodruff, M.A.; Ivanovski, S.; Xiao, Y. Estrogen Deficiency-Associated Bone Loss in the Maxilla: A methodology to quantify the changes in the maxillary intra-radicular alveolar bone in an ovariectomized rat osteoporosis model. Tissue Eng. Part C Methods, 2015, 21(5), 458-466.
[http://dx.doi.org/10.1089/ten.tec.2014.0268 ] [PMID: 25315176]
[44]
Zaid, S.S.M.; Sulaiman, S.A.; Othman, N.H.; Soelaiman, I-N.; Shuid, A.N.; Mohamad, N.; Muhamad, N. Protective effects of Tualang honey on bone structure in experimental postmenopausal rats. Clinics (São Paulo), 2012, 67(7), 779-784.
[http://dx.doi.org/10.6061/clinics/2012(07)13 ] [PMID: 22892923]
[45]
Fathilah, S.N.; Nazrun Shuid, A.; Mohamed, N.; Muhammad, N.; Nirwana Soelaiman, I. Labisia pumila protects the bone of estrogen-deficient rat model: A histomorphometric study. J. Ethnopharmacol., 2012, 142(1), 294-299.
[http://dx.doi.org/10.1016/j.jep.2012.04.029 ] [PMID: 22542643]
[46]
Mohamed, N.; Gwee Sian Khee, S.; Shuid, A.N.; Muhammad, N.; Suhaimi, F.; Othman, F.; Babji, A.S.; Soelaiman, I.-N. The effects of Cosmos caudatus on structural bone histomorphometry in ovariectomized rats. Evid-Based. Complementary. Altern. Med.,, 2012.
[47]
Liu, Z.; Liu, L.; Kang, C.; Xie, Q.; Zhang, B.; Li, Y. Effects of estrogen deficiency on microstructural changes in rat alveolar bone proper and periodontal ligament. Mol. Med. Rep., 2015, 12(3), 3508-3514.
[http://dx.doi.org/10.3892/mmr.2015.3891 ] [PMID: 26044123]
[48]
Ahmad, N.; Chillara, R.; Kushwaha, P.; Khedgikar, V.; Karvande, A.; Choudhary, D.; Adhikary, S.; Maurya, R.; Trivedi, R. Evaluation of anti-osteoporotic activity of butanolic fraction from Passiflora foetida in ovariectomy-induced bone loss in mice. Biomed. Pharmacother., 2017, 88, 804-813.
[http://dx.doi.org/10.1016/j.biopha.2017.01.100 ] [PMID: 28160755]
[49]
Wen, X.X.; Xu, C.; Wang, F.Q.; Feng, Y.F.; Zhao, X.; Yan, Y.B.; Lei, W. Temporal changes of microarchitectural and mechanical parameters of cancellous bone in the osteoporotic rabbit. BioMed Res. Int., 2015, 2015 263434
[http://dx.doi.org/10.1155/2015/263434 ] [PMID: 25918705]
[50]
Aktifanus, A.T.; Shuid, A.N.; Rashid, N.H.A.; Ling, T.H.; Loong, C.Y.; Saat, N.M.; Muhammad, N.; Mohamed, N.; Soelaiman, I.N. Comparison of the effects of tocotrienol and estrogen on the bone markers and dynamic changes in postmenopausal osteoporosis rat model. Asian J. Anim. Vet. Adv., 2012, 7(3), 225-234.
[http://dx.doi.org/10.3923/ajava.2012.225.234]
[51]
Abdul-Majeed, S.; Mohamed, N.; Soelaiman, I-N. Effects of tocotrienol and lovastatin combination on osteoblast and osteoclast activity in estrogen-deficient osteoporosis. Evid-Based. Complementary. Altern. Med., 2012, 2012 960742
[52]
Isomura, H.; Fujie, K.; Shibata, K.; Inoue, N.; Iizuka, T.; Takebe, G.; Takahashi, K.; Nishihira, J.; Izumi, H.; Sakamoto, W. Bone metabolism and oxidative stress in postmenopausal rats with iron overload. Toxicology, 2004, 197(2), 93-100.
[http://dx.doi.org/10.1016/j.tox.2003.12.006 ] [PMID: 15003320]
[53]
Wheater, G.; Elshahaly, M.; Tuck, S.P.; Datta, H.K.; van Laar, J.M. The clinical utility of bone marker measurements in osteoporosis. J. Transl. Med., 2013, 11, 201-201.
[http://dx.doi.org/10.1186/1479-5876-11-201 ] [PMID: 23984630]
[54]
Liu, H.; Li, W.; Jia, S.; Li, B. Puerarin and zinc additively prevent mandibular bone loss through inhibiting osteoclastogenesis in ovariectomized rats. Histol. Histopathol., 2017, 32(8), 851-860.
[PMID: 27966208]
[55]
Christenson, E.S.; Jiang, X.; Kagan, R.; Schnatz, P. Osteoporosis management in post-menopausal women. Minerva Ginecol., 2012, 64(3), 181-194.
[PMID: 22635014]
[56]
Cadarette, S.M.; McIsaac, W.J.; Hawker, G.A.; Jaakkimainen, L.; Culbert, A.; Zarifa, G.; Ola, E.; Jaglal, S.B. The validity of decision rules for selecting women with primary osteoporosis for bone mineral density testing. Osteoporos. Int., 2004, 15(5), 361-366.
[http://dx.doi.org/10.1007/s00198-003-1552-7 ] [PMID: 14730421]
[57]
Tian, L.; Yang, R.; Wei, L.; Liu, J.; Yang, Y.; Shao, F.; Ma, W.; Li, T.; Wang, Y.; Guo, T. Prevalence of osteoporosis and related lifestyle and metabolic factors of postmenopausal women and elderly men: A cross-sectional study in Gansu province, Northwestern of China. Medicine (Baltimore), 2017, 96(43), e8294-e8294.
[http://dx.doi.org/10.1097/MD.0000000000008294 ] [PMID: 29068999]
[58]
Kazi, M.; Abullah, F.; Abbas, Q.; Bawany, S. Assessment of Osteoporosis and Osteopenia amongst Menopausal Women of North Nazimabad, Karachi, Pakistan. Sindh University Research Journal-SURJ, 2019, 51(01), 147-150.
[http://dx.doi.org/10.26692/sujo/2019.01.26]
[59]
Chan, C.Y.; Subramaniam, S.; Mohamed, N.; Ima-Nirwana, S.; Muhammad, N.; Fairus, A.; Ng, P.Y.; Jamil, N.A.; Abd Aziz, N.; Chin, K-Y. Determinants of Bone Health Status in a Multi-Ethnic Population in Klang Valley, Malaysia. Int. J. Environ. Res. Public Health, 2020, 17(2) E384
[http://dx.doi.org/10.3390/ijerph17020384 ] [PMID: 31936034]
[60]
Subramaniam, S.; Chan, C-Y.; Soelaiman, I-N.; Mohamed, N.; Muhammad, N.; Ahmad, F.; Abd Manaf, M.R.; Ng, P-Y.; Jamil, N.A.; Chin, K-Y. Prevalence and Predictors of Osteoporosis Among the Chinese Population in Klang Valley, Malaysia. Appl. Sci. (Basel), 2019, 9(9), 1820.
[http://dx.doi.org/10.3390/app9091820]
[61]
Mederle, O.A.; Balas, M.; Ioanoviciu, S.D.; Gurban, C-V.; Tudor, A.; Borza, C. Correlations between bone turnover markers, serum magnesium and bone mass density in postmenopausal osteoporosis. Clin. Interv. Aging, 2018, 13, 1383-1389.
[http://dx.doi.org/10.2147/CIA.S170111 ] [PMID: 30122910]
[62]
Khanizadeh, F.; Rahmani, A.; Asadollahi, K.; Ahmadi, M.R.H. Combination therapy of curcumin and alendronate modulates bone turnover markers and enhances bone mineral density in postmenopausal women with osteoporosis. Arch. Endocrinol. Metab., 2018, 62(4), 438-445.
[http://dx.doi.org/10.20945/2359-3997000000060 ] [PMID: 30304108]
[63]
Thompson, D.M.; Lee, H.M.; Stoner, J.A.; Golub, L.M.; Nummikoski, P.V.; Payne, J.B. Loss of alveolar bone density in postmenopausal, osteopenic women is associated with circulating levels of gelatinases. J. Periodontal Res., 2019, 54(5), 525-532.
[http://dx.doi.org/10.1111/jre.12656 ] [PMID: 31032961]
[64]
Gutierrez-Buey, G.; Restituto, P.; Botella, S.; Monreal, I.; Colina, I.; Rodríguez-Fraile, M.; Calleja, A.; Varo, N. Trabecular bone score and bone remodelling markers identify perimenopausal women at high risk of bone loss. Clin. Endocrinol. (Oxf.), 2019, 91(3), 391-399.
[http://dx.doi.org/10.1111/cen.14042 ] [PMID: 31141196]
[65]
Gutteridge, J.M.C.; Halliwell, B. Mini-Review: Oxidative stress, redox stress or redox success? Biochem. Biophys. Res. Commun., 2018, 502(2), 183-186.
[http://dx.doi.org/10.1016/j.bbrc.2018.05.045 ] [PMID: 29752940]
[66]
Son, Y.; Kim, S.; Chung, H-T. Methods. Enzymol; Elsevier, 2013, Vol. 528, pp. 27-48.
[67]
Newsholme, P.; Cruzat, V.F.; Keane, K.N.; Carlessi, R.; de Bittencourt, P.I.H. Jr Molecular mechanisms of ROS production and oxidative stress in diabetes. Biochem. J., 2016, 473(24), 4527-4550.
[http://dx.doi.org/10.1042/BCJ20160503C ] [PMID: 27941030]
[68]
Romagnoli, C.; Marcucci, G.; Favilli, F.; Zonefrati, R.; Mavilia, C.; Galli, G.; Tanini, A.; Iantomasi, T.; Brandi, M.L.; Vincenzini, M.T. Role of GSH/GSSG redox couple in osteogenic activity and osteoclastogenic markers of human osteoblast-like SaOS-2 cells. FEBS J., 2013, 280(3), 867-879.
[PMID: 23176170]
[69]
Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol., 2007, 39(1), 44-84.
[http://dx.doi.org/10.1016/j.biocel.2006.07.001 ] [PMID: 16978905]
[70]
Redza-Dutordoir, M.; Averill-Bates, D.A. Activation of apoptosis signalling pathways by reactive oxygen species. Biochim. Biophys. Acta, 2016, 1863(12), 2977-2992.
[http://dx.doi.org/10.1016/j.bbamcr.2016.09.012 ] [PMID: 27646922]
[71]
Tew, K.D.; Townsend, D.M. Glutathione-s-transferases as determinants of cell survival and death. Antioxid. Redox Signal., 2012, 17(12), 1728-1737.
[http://dx.doi.org/10.1089/ars.2012.4640 ] [PMID: 22540427]
[72]
Laborde, E. Glutathione transferases as mediators of signaling pathways involved in cell proliferation and cell death. Cell Death Differ., 2010, 17(9), 1373-1380.
[http://dx.doi.org/10.1038/cdd.2010.80 ] [PMID: 20596078]
[73]
Baek, K.H.; Oh, K.W.; Lee, W.Y.; Lee, S.S.; Kim, M.K.; Kwon, H.S.; Rhee, E.J.; Han, J.H.; Song, K.H.; Cha, B.Y.; Lee, K.W.; Kang, M.I. Association of oxidative stress with postmenopausal osteoporosis and the effects of hydrogen peroxide on osteoclast formation in human bone marrow cell cultures. Calcif. Tissue Int., 2010, 87(3), 226-235.
[http://dx.doi.org/10.1007/s00223-010-9393-9 ] [PMID: 20614110]
[74]
Lean, J.M.; Jagger, C.J.; Kirstein, B.; Fuller, K.; Chambers, T.J. Hydrogen peroxide is essential for estrogen-deficiency bone loss and osteoclast formation. Endocrinology, 2005, 146(2), 728-735.
[http://dx.doi.org/10.1210/en.2004-1021 ] [PMID: 15528306]
[75]
Domazetovic, V.; Fontani, F.; Marcucci, G.; Iantomasi, T.; Brandi, M.L.; Vincenzini, M.T. Estrogen inhibits starvation-induced apoptosis in osteocytes by a redox-independent process involving association of JNK and glutathione S-transferase P1-1. FEBS Open Bio, 2017, 7(5), 705-718.
[http://dx.doi.org/10.1002/2211-5463.12216 ] [PMID: 28469982]
[76]
El Wakf, A.M.; Hassan, H.A.; Gharib, N.S. Osteoprotective effect of soybean and sesame oils in ovariectomized rats via estrogen-like mechanism. Cytotechnology, 2014, 66(2), 335-343.
[http://dx.doi.org/10.1007/s10616-013-9580-4 ] [PMID: 23748642]
[77]
Effendy, N.M.; Shuid, A.N. Time and dose-dependent effects of Labisia pumila on bone oxidative status of postmenopausal osteoporosis rat model. Nutrients, 2014, 6(8), 3288-3302.
[http://dx.doi.org/10.3390/nu6083288 ] [PMID: 25195641]
[78]
Muthusami, S.; Gopalakrishnan, V.; Stanley, J.A.; Krishnamoorthy, S.; Ilangovan, R.; Gopalakrishnan, V.K.; Srinivasan, N. Cissus quadrangularis prevented the ovariectomy induced oxidative stress in the femur of adult albino rats. Biomed. Pharmacother., 2016, 81, 416-423.
[http://dx.doi.org/10.1016/j.biopha.2016.04.021 ] [PMID: 27261621]
[79]
Kireev, R.A.; Tresguerres, A.C.; Garcia, C.; Borras, C.; Ariznavarreta, C.; Vara, E.; Vina, J.; Tresguerres, J.A. Hormonal regulation of pro-inflammatory and lipid peroxidation processes in liver of old ovariectomized female rats. Biogerontology, 2010, 11(2), 229-243.
[http://dx.doi.org/10.1007/s10522-009-9242-2 ] [PMID: 19633997]
[80]
Oliveira, M.C.; Campos-Shimada, L.B.; Marçal-Natali, M.R.; Ishii-Iwamoto, E.L.; Salgueiro-Pagadigorria, C.L. A Long-term Estrogen Deficiency in Ovariectomized Mice is Associated with Disturbances in Fatty Acid Oxidation and Oxidative Stress. Rev. Bras. Ginecol. Obstet., 2018, 40(5), 251-259.
[http://dx.doi.org/10.1055/s-0038-1666856 ] [PMID: 29913542]
[81]
Sankar, P.; Zachariah, B.; Vickneshwaran, V.; Jacob, S.E.; Sridhar, M.G. Amelioration of oxidative stress and insulin resistance by soy isoflavones (from Glycine max) in ovariectomized Wistar rats fed with high fat diet: The molecular mechanisms. Exp. Gerontol., 2015, 63, 67-75.
[http://dx.doi.org/10.1016/j.exger.2015.02.001 ] [PMID: 25660477]
[82]
Shehata, M.; Kamel, M.A. Protective effect of antioxidant adjuvant treatment with hormone replacement therapy against cardiovascular diseases in ovariectomized rats. Endocr. Regul., 2008, 42(2-3), 69-75.
[PMID: 18624609]
[83]
He, X.F.; Zhang, L.; Zhang, C.H.; Zhao, C.R.; Li, H.; Zhang, L.F.; Tian, G.F.; Guo, M.F.; Dai, Z.; Sui, F.G. Berberine alleviates oxidative stress in rats with osteoporosis through receptor activator of NF-kB/receptor activator of NF-kB ligand/osteoprotegerin (RANK/RANKL/OPG) pathway. Bosn. J. Basic Med. Sci., 2017, 17(4), 295-301.
[PMID: 29055350]
[84]
Zhou, X.J.; Xia, Y.; Zhao, Y.Y.; Gu, W.Q.; Xiao, X.; Bai, X.C.; Liu, J.; Li, M. Estradiol significantly increases the expression of antioxidant enzymes in osteoporotic rats and osteoblasts in vitro. Nan Fang Yi Ke Da Xue Xue Bao, 2018, 38(4), 402-408.
[PMID: 29735439]
[85]
Yang, Y.; Zheng, X.; Li, B.; Jiang, S.; Jiang, L. Increased activity of osteocyte autophagy in ovariectomized rats and its correlation with oxidative stress status and bone loss. Biochem. Biophys. Res. Commun., 2014, 451(1), 86-92.
[http://dx.doi.org/10.1016/j.bbrc.2014.07.069 ] [PMID: 25063028]
[86]
Giorgio, M.; Trinei, M.; Migliaccio, E.; Pelicci, P.G. Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat. Rev. Mol. Cell Biol., 2007, 8(9), 722-728.
[http://dx.doi.org/10.1038/nrm2240 ] [PMID: 17700625]
[87]
Russell, S.J.; Kahn, C.R. Endocrine regulation of ageing. Nat. Rev. Mol. Cell Biol., 2007, 8(9), 681-691.
[http://dx.doi.org/10.1038/nrm2234 ] [PMID: 17684529]
[88]
Abdul-Rasheed, O.F.; Al-Shamma, G.A.; Zillo, B.H. Serum γ-glutamyltransferase as oxidative stress marker in pre-and postmenopausal Iraqi women. Oman Med. J., 2010, 25(4), 286-288.
[http://dx.doi.org/10.5001/omj.2010.83 ] [PMID: 22043359]
[89]
Cervellati, C.; Bonaccorsi, G.; Cremonini, E.; Romani, A.; Fila, E.; Castaldini, M.C.; Ferrazzini, S.; Giganti, M.; Massari, L. Oxidative stress and bone resorption interplay as a possible trigger for postmenopausal osteoporosis. BioMed Res. Int., 2014, 2014 569563
[http://dx.doi.org/10.1155/2014/569563 ] [PMID: 24524081]
[90]
Vural, P.; Akgül, C.; Canbaz, M. Effects of menopause and tibolone on antioxidants in postmenopausal women. Ann. Clin. Biochem., 2005, 42(Pt 3), 220-223.
[http://dx.doi.org/10.1258/0004563053857941 ] [PMID: 15949158]
[91]
Bednarek-Tupikowska, G.; Tworowska, U.; Jedrychowska, I.; Radomska, B.; Tupikowski, K.; Bidzinska-Speichert, B.; Milewicz, A. Effects of oestradiol and oestroprogestin on erythrocyte antioxidative enzyme system activity in postmenopausal women. Clin. Endocrinol. (Oxf.), 2006, 64(4), 463-468.
[http://dx.doi.org/10.1111/j.1365-2265.2006.02494.x ] [PMID: 16584521]
[92]
Medzhitov, R. Inflammation 2010: new adventures of an old flame. Cell, 2010, 140(6), 771-776.
[http://dx.doi.org/10.1016/j.cell.2010.03.006 ] [PMID: 20303867]
[93]
Tanaka, T.; Narazaki, M.; Kishimoto, T. IL-6 in inflammation, immunity, and disease. Cold Spring Harb. Perspect. Biol., 2014, 6(10) a016295
[http://dx.doi.org/10.1101/cshperspect.a016295 ] [PMID: 25190079]
[94]
Parameswaran, N.; Patial, S. Tumor necrosis factor-α signaling in macrophages. Crit. Rev. Eukaryot. Gene Expr., 2010, 20(2), 87-103.
[http://dx.doi.org/10.1615/CritRevEukarGeneExpr.v20.i2.10 ] [PMID: 21133840]
[95]
Schroecksnadel, K.; Frick, B.; Winkler, C.; Fuchs, D. Crucial role of interferon-gamma and stimulated macrophages in cardiovascular disease. Curr. Vasc. Pharmacol., 2006, 4(3), 205-213.
[http://dx.doi.org/10.2174/157016106777698379 ] [PMID: 16842138]
[96]
Ambili, R.; Santhi, W.S.; Janam, P.; Nandakumar, K.; Pillai, M.R. Expression of activated transcription factor nuclear factor-kappaB in periodontally diseased tissues. J. Periodontol., 2005, 76(7), 1148-1153.
[http://dx.doi.org/10.1902/jop.2005.76.7.1148 ] [PMID: 16018758]
[97]
Garcia de Aquino, S.; Manzolli Leite, F.R.; Stach-Machado, D.R.; Francisco da Silva, J.A.; Spolidorio, L.C.; Rossa, C., Jr Signaling pathways associated with the expression of inflammatory mediators activated during the course of two models of experimental periodontitis. Life Sci., 2009, 84(21-22), 745-754.
[http://dx.doi.org/10.1016/j.lfs.2009.03.001 ] [PMID: 19285515]
[98]
Vijayan, V.; Khandelwal, M.; Manglani, K.; Gupta, S.; Surolia, A. Methionine down-regulates TLR4/MyD88/NF-κB signalling in osteoclast precursors to reduce bone loss during osteoporosis. Br. J. Pharmacol., 2014, 171(1), 107-121.
[http://dx.doi.org/10.1111/bph.12434 ] [PMID: 24111943]
[99]
Cenci, S.; Weitzmann, M.N.; Roggia, C.; Namba, N.; Novack, D.; Woodring, J.; Pacifici, R. Estrogen deficiency induces bone loss by enhancing T-cell production of TNF-alpha. J. Clin. Invest., 2000, 106(10), 1229-1237.
[http://dx.doi.org/10.1172/JCI11066 ] [PMID: 11086024]
[100]
Hughes, D.E.; Dai, A.; Tiffee, J.C.; Li, H.H.; Mundy, G.R.; Boyce, B.F. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat. Med., 1996, 2(10), 1132-1136.
[http://dx.doi.org/10.1038/nm1096-1132 ] [PMID: 8837613]
[101]
Oursler, M.J.; Cortese, C.; Keeting, P.; Anderson, M.A.; Bonde, S.K.; Riggs, B.L.; Spelsberg, T.C. Modulation of transforming growth factor-beta production in normal human osteoblast-like cells by 17 beta-estradiol and parathyroid hormone. Endocrinology, 1991, 129(6), 3313-3320.
[http://dx.doi.org/10.1210/endo-129-6-3313 ] [PMID: 1954907]
[102]
Pfeilschifter, J.; Seyedin, S.M.; Mundy, G.R. Transforming growth factor beta inhibits bone resorption in fetal rat long bone cultures. J. Clin. Invest., 1988, 82(2), 680-685.
[http://dx.doi.org/10.1172/JCI113647 ] [PMID: 3165385]
[103]
Villa, A.; Rizzi, N.; Vegeto, E.; Ciana, P.; Maggi, A. Estrogen accelerates the resolution of inflammation in macrophagic cells. Sci. Rep., 2015, 5, 15224.
[http://dx.doi.org/10.1038/srep15224 ] [PMID: 26477569]
[104]
Albayrak, A.; Uyanik, M.H.; Odabasoglu, F.; Halici, Z.; Uyanik, A.; Bayir, Y.; Albayrak, F.; Albayrak, Y.; Polat, B.; Suleyman, H. The effects of diabetes and/or polymicrobial sepsis on the status of antioxidant enzymes and pro-inflammatory cytokines on heart, liver, and lung of ovariectomized rats. J. Surg. Res., 2011, 169(1), 67-75.
[http://dx.doi.org/10.1016/j.jss.2009.09.055 ] [PMID: 20080253]
[105]
Delgobo, M.; Agnes, J.P.; Gonçalves, R.M.; Dos Santos, V.W.; Parisotto, E.B.; Zamoner, A.; Zanotto-Filho, A. N-acetylcysteine and alpha-lipoic acid improve antioxidant defenses and decrease oxidative stress, inflammation and serum lipid levels in ovariectomized rats via estrogen-independent mechanisms. J. Nutr. Biochem., 2019, 67, 190-200.
[http://dx.doi.org/10.1016/j.jnutbio.2019.02.012 ] [PMID: 30951973]
[106]
Varga, C.; Veszelka, M.; Kupai, K.; Börzsei, D.; Deim, Z.; Szabó, R.; Török, S.; Priksz, D.; Gesztelyi, R.; Juhász, B.; Radák, Z.; Pósa, A. The effects of exercise training and high triglyceride diet in an estrogen depleted rat model: The role of the heme oxygenase system and inflammatory processes in cardiovascular risk. J. Sports Sci. Med., 2018, 17(4), 580-588.
[PMID: 30479526]
[107]
Li, P.; Liu, H.; Sun, P.; Wang, X.; Wang, C.; Wang, L.; Wang, T. Chronic vagus nerve stimulation attenuates vascular endothelial impairments and reduces the inflammatory profile via inhibition of the NF-κB signaling pathway in ovariectomized rats. Exp. Gerontol., 2016, 74, 43-55.
[http://dx.doi.org/10.1016/j.exger.2015.12.005 ] [PMID: 26692419]
[108]
Abu-Taha, M.; Rius, C.; Hermenegildo, C.; Noguera, I.; Cerda-Nicolas, J.M.; Issekutz, A.C.; Jose, P.J.; Cortijo, J.; Morcillo, E.J.; Sanz, M.J. Menopause and ovariectomy cause a low grade of systemic inflammation that may be prevented by chronic treatment with low doses of estrogen or losartan. J. Immunol., 2009, 183(2), 1393-1402.
[http://dx.doi.org/10.4049/jimmunol.0803157 ] [PMID: 19553526]
[109]
Rodrigues, M.F.C.; Ferreira, F.C.; Silva-Magosso, N.S.; Barbosa, M.R.; Souza, M.V.C.; Domingos, M.M.; Canevazzi, G.H.R.; Stotzer, U.S.; Peviani, S.M.; de Lira, F.S.; Selistre de Araújo, H.S.; Perez, S.E.A. Effects of resistance training and estrogen replacement on adipose tissue inflammation in ovariectomized rats. Appl. Physiol. Nutr. Metab., 2017, 42(6), 605-612.
[http://dx.doi.org/10.1139/apnm-2016-0443 ] [PMID: 28177709]
[110]
Xu, Y.; Sheng, H.; Bao, Q.; Wang, Y.; Lu, J.; Ni, X. NLRP3 inflammasome activation mediates estrogen deficiency-induced depression- and anxiety-like behavior and hippocampal inflammation in mice. Brain Behav. Immun., 2016, 56, 175-186.
[http://dx.doi.org/10.1016/j.bbi.2016.02.022 ] [PMID: 26928197]
[111]
Cordeau, P., Jr; Lalancette-Hébert, M.; Weng, Y.C.; Kriz, J. Estrogen receptors alpha mediates postischemic inflammation in chronically estrogen-deprived mice. Neurobiol. Aging, 2016, 40, 50-60.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.01.002 ] [PMID: 26973103]
[112]
Yang, Y.H.; Ngo, D.; Jones, M.; Simpson, E.; Fritzemeier, K.H.; Morand, E.F. Endogenous estrogen regulation of inflammatory arthritis and cytokine expression in male mice, predominantly via estrogen receptor alpha. Arthritis Rheum., 2010, 62(4), 1017-1025.
[http://dx.doi.org/10.1002/art.27330 ] [PMID: 20131258]
[113]
Moon, N.; Effiong, L.; Song, L.; Gardner, T.R.; Soung, D.Y. Tart cherry prevents bone loss through inhibition of RANKL in TNF-overexpressing mice. Nutrients, 2018, 11(1), 63.
[http://dx.doi.org/10.3390/nu11010063 ] [PMID: 30597968]
[114]
Calippe, B.; Douin-Echinard, V.; Laffargue, M.; Laurell, H.; Rana-Poussine, V.; Pipy, B.; Guéry, J.C.; Bayard, F.; Arnal, J.F.; Gourdy, P. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J. Immunol., 2008, 180(12), 7980-7988.
[http://dx.doi.org/10.4049/jimmunol.180.12.7980 ] [PMID: 18523261]
[115]
Huang, W.Y.; Hsin, I.L.; Chen, D.R.; Chang, C.C.; Kor, C.T.; Chen, T.Y.; Wu, H.M. Circulating interleukin-8 and tumor necrosis factor-alpha are associated with hot flashes in healthy postmenopausal women., 2017., 12(8), e0184011..
[116]
Cronin, B.E.; Allsopp, P.J.; Slevin, M.M.; Magee, P.J.; McCaffrey, T.A.; Livingstone, M.B.E.; Strain, J.J.; McSorley, E.M. The effect of weight change over a 2-year period on inflammatory status in postmenopausal women. Eur. J. Clin. Nutr., 2018, 72(3), 388-393.
[http://dx.doi.org/10.1038/s41430-017-0014-9 ] [PMID: 29167576]
[117]
Zhang, J.; Wang, H.; Yang, S.; Wang, X. Comparison of lipid profiles and inflammation in pre- and post-menopausal women with cerebral infarction and the role of atorvastatin in such populations. Lipids Health Dis., 2018, 17(1), 20.
[http://dx.doi.org/10.1186/s12944-018-0669-9 ] [PMID: 29391065]
[118]
Ilesanmi-Oyelere, B.L.; Schollum, L.; Kuhn-Sherlock, B.; McConnell, M.; Mros, S.; Coad, J.; Roy, N.C.; Kruger, M.C. Inflammatory markers and bone health in postmenopausal women: A cross-sectional overview. Immun. Ageing, 2019, 16, 15-15.
[http://dx.doi.org/10.1186/s12979-019-0155-x ] [PMID: 31333751]
[119]
Zha, L.; He, L.; Liang, Y.; Qin, H.; Yu, B.; Chang, L.; Xue, L. TNF-α contributes to postmenopausal osteoporosis by synergistically promoting RANKL-induced osteoclast formation. Biomed. Pharmacother., 2018, 102, 369-374.
[http://dx.doi.org/10.1016/j.biopha.2018.03.080 ] [PMID: 29571022]
[120]
Wells, G.; Tugwell, P.; Shea, B.; Guyatt, G.; Peterson, J.; Zytaruk, N.; Robinson, V.; Henry, D.; O’Connell, D.; Cranney, A. Osteoporosis methodology group and the osteoporosis research advisory group. Meta-analyses of therapies for postmenopausal osteoporosis. V. Meta-analysis of the efficacy of hormone replacement therapy in treating and preventing osteoporosis in postmenopausal women. Endocr. Rev., 2002, 23(4), 529-539.
[http://dx.doi.org/10.1210/er.2001-5002 ] [PMID: 12202468]
[121]
Torgerson, D.J.; Bell-Syer, S.E. Hormone replacement therapy and prevention of nonvertebral fractures: A meta-analysis of randomized trials. JAMA, 2001, 285(22), 2891-2897.
[http://dx.doi.org/10.1001/jama.285.22.2891 ] [PMID: 11401611]
[122]
Cauley, J.A.; Robbins, J.; Chen, Z.; Cummings, S.R.; Jackson, R.D.; LaCroix, A.Z.; LeBoff, M.; Lewis, C.E.; McGowan, J.; Neuner, J.; Pettinger, M.; Stefanick, M.L.; Wactawski-Wende, J.; Watts, N.B. Women’s Health Initiative Investigators. Effects of estrogen plus progestin on risk of fracture and bone mineral density: The Women’s Health Initiative randomized trial. JAMA, 2003, 290(13), 1729-1738.
[http://dx.doi.org/10.1001/jama.290.13.1729 ] [PMID: 14519707]
[123]
Greenspan, S.L.; Beck, T.J.; Resnick, N.M.; Bhattacharya, R.; Parker, R.A. Effect of hormone replacement, alendronate, or combination therapy on hip structural geometry: A 3-year, double-blind, placebo-controlled clinical trial. J. Bone Miner. Res., 2005, 20(9), 1525-1532.
[http://dx.doi.org/10.1359/JBMR.050508 ] [PMID: 16059624]
[124]
Beral, V. Million Women Study Collaborators. Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet, 2003, 362(9382), 419-427.
[http://dx.doi.org/10.1016/S0140-6736(03)14065-2 ] [PMID: 12927427]
[125]
Rossouw, J.E.; Anderson, G.L.; Prentice, R.L.; LaCroix, A.Z.; Kooperberg, C.; Stefanick, M.L.; Jackson, R.D.; Beresford, S.A.; Howard, B.V.; Johnson, K.C.; Kotchen, J.M.; Ockene, J. Writing Group for the Women’s Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women’s health initiative randomized controlled trial. JAMA, 2002, 288(3), 321-333.
[http://dx.doi.org/10.1001/jama.288.3.321 ] [PMID: 12117397]
[126]
de Villiers, T.J.; Pines, A.; Panay, N.; Gambacciani, M.; Archer, D.F.; Baber, R.J.; Davis, S.R.; Gompel, A.A.; Henderson, V.W.; Langer, R.; Lobo, R.A.; Plu-Bureau, G.; Sturdee, D.W. International menopause society. Updated 2013 international menopause society recommendations on menopausal hormone therapy and preventive strategies for midlife health. Climacteric, 2013, 16(3), 316-337.
[http://dx.doi.org/10.3109/13697137.2013.795683 ] [PMID: 23672656]
[127]
de Villiers, T.J.; Gass, M.L.; Haines, C.J.; Hall, J.E.; Lobo, R.A.; Pierroz, D.D.; Rees, M. Global consensus statement on menopausal hormone therapy. Climacteric, 2013, 16(2), 203-204.
[http://dx.doi.org/10.3109/13697137.2013.771520 ] [PMID: 23488524]


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VOLUME: 20
ISSUE: 9
Year: 2020
Published on: 05 November, 2020
Page: [1478 - 1487]
Pages: 10
DOI: 10.2174/1871530320666200604160614

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