Roles for estrogen in bone loss and arthralgia during aromatase inhibitor treatment

Current Opinion in Oncology

Volumn 19, Issue SUPPL. 1, 2007, Pages

  Josse, Robert G ^a  

^a ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

Aromatase inhibitors; Arthralgia; Breast cancer; Estrogen

Indexed keywords

AMINOGLUTETHIMIDE; ANASTROZOLE; ESTROGEN; EXEMESTANE; FADROZOLE; FORMESTANE; LETROZOLE; PLACEBO; PYRIDOGLUTETHIMIDE; TAMOXIFEN;

ARTHRALGIA; BONE DENSITY; BONE INJURY; BONE REMODELING; BONE TURNOVER; BREAST CANCER; CLINICAL TRIAL; DISEASE ASSOCIATION; DRUG EFFECT; DRUG SUBSTITUTION; DRUG WITHDRAWAL; ENZYME ACTIVITY; ENZYME INHIBITION; ESTROGEN ACTIVITY; ESTROGEN BLOOD LEVEL; ESTROGEN DEFICIENCY; ESTROGEN SYNTHESIS; GONAD; HUMAN; MENOPAUSE; MONOTHERAPY; NOCICEPTION; OSTEOLYSIS; PAIN THRESHOLD; PATHOGENESIS; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW; SIDE EFFECT; UTERUS CANCER;

EID: 34248194979     PISSN: 10408746     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.cco.0000266465.24079.63     Document Type: Review

References (97)

1. Clemons M, Goss P. Estrogen and the risk of breast cancer. N Engl J Med 2001; 344:276-285.
2. Huang HJ, Neven P, Drijkoningen M, et al. Association between tumour characteristics and HER-2/neu by immunohistochemistry in 1362 women with primary operable breast cancer. J Clin Pathol 2005; 58:611-616.
3. Rhodes A, Jasani B, Balaton AJ, et al. Frequency of oestrogen and progesterone receptor positivity by immunohistochemical analysis in 7016 breast carcinomas: correlation with patient age, assay sensitivity, threshold value, and mammographic screening. J Clin Pathol 2000; 53:688-696.
4. Kaaks R, Rinaldi S, Key TJ, et al. Postmenopausal serum androgens, oestrogens and breast cancer risk: the European prospective investigation into cancer and nutrition. Endocr Relat Cancer 2005; 124:1071-1082.
5. Rinaldi S, Key TJ, Peeters PH, et al. Anthropometric measures, endogenous sex steroids and breast cancer risk in postmenopausal women: a study within the EPIC cohort. Int J Cancer 2006; 118:2832-2839.
6. Goss PE, Strasser K. Aromatase inhibitors in the treatment and prevention of breast cancer. J Clin Oncol 2001; 19:881-894.
7. Salhab M, Reed MJ, Al Sarakbi W, et al. The role of aromatase and 17-I(2)-hydroxysteroid dehydrogenase type 1 mRNA expression in predicting the clinical outcome of human breast cancer. Breast Cancer Res Treat 2006; 99:155-162.
8. Yoshimura N, Harada N, Bukholm I, et al. Intratumoural mRNA expression of genes from the oestradiol metabolic pathway and clinical and histopathological parameters of breast cancer. Breast Cancer Res 2004; 6:R46-R55.
9. Catherino WH, Jordan VC. A risk-benefit assessment of tamoxifen therapy. Drug Saf 1993; 8:381-397.
10. Early Breast Cancer Trialists' Collaborative Group (EBCTCG). Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005; 365:1687-1717.
11. Cosman F, Lindsay R. Selective estrogen receptor modulators: clinical spectrum. Endocr Rev 1999; 20:418-434.
12. Barsalou A, Gao W, Anghel SI, et al. Estrogen response elements can mediate agonist activity of anti-estrogens in human endometrial Ishikawa cells. J Biol Chem 1998; 273:17138-17146.
13. Sasaki-Iwaoka H, Maruyama K, Endoh H, et al. A trans-acting enhancer modulates estrogen-mediated transcription of reporter genes in osteoblasts. J Bone Miner Res 1999; 14:248-255.
14. Wijayaratne AL, McDonnell DP. The human estrogen receptor-alpha is a ubiquitinated protein whose stability is affected differentially by agonists, antagonists, and selective estrogen receptor modulators. J Clin Biochem 2001; 276:35684-35692.
15. Horner-Glister E, Maleki-Dizaji M, Guerin CJ, et al. Influence of oestradiol and tamoxifen on oestrogen receptors-alpha and -beta protein degradation and non-genomic signalling pathways in uterine and breast carcinoma cells. J Mol Endocrinol 2005; 35:421-432.
16. Ellis MJ, Rosen E, Dressman H, et al. Neoadjuvant comparisons of aromatase inhibitors and tamoxifen: pretreatment determinants of response and on-treatment effect. Steroid Biochem Mol Biol 2003; 86:301-307.
17. Wilking N, Carlstrom K, Skoldefors H, et al. Effects of tamoxifen on the serum levels of oestrogens and adrenocortical steroids in postmenopausal breast cancer patients. Acta Chir Scand 1982; 148:345-349.
18. Brueggemeier RW, Hackett JC, Diaz-Cruz ES. Aromatase inhibitors in the treatment of breast cancer. Endocr Rev 2005; 26:331-345.
19. Dowsett M, Jones A, Johnston SR, et al. In vivo measurement of aromatase inhibition by letrozole (CGS 20267) in postmenopausal patients with breast cancer. Clin Cancer Res 1995; 1:1511-1515.
20. Geisler J, King N, Anker G, et al. In vivo inhibition of aromatization by exemestane, a novel irreversible aromatase inhibitor, in postmenopausal breast cancer patients. Clin Cancer Res 1998; 4:2089-2093.
21. Geisler J, King N, Dowsett M, et al. Influence of anastrozole (Arimidex), a selective, non-steroidal aromatase inhibitor, on in vivo aromatisation and plasma oestrogen levels in postmenopausal women with breast cancer. Br J Cancer 1996; 74:1286-1291.
22. Paridaens R, Thomas J, Wildiers J, et al. Safety, activity, and estrogen inhibition by exemestane in postmenopausal women with advanced breast cancer: a phase I study. Anticancer Drugs 1998; 9:675-683.
23. Goss PE, Ingle JN, Martino S, et al. Randomized trial of letrozole following tamoxifen as extended adjuvant therapy in receptor-positive breast cancer: updated findings from NCIC CTG MA. J Natl Cancer Inst 2005; 97:1262-1271.
24. Howell A, Cuzick J, Baum M, et al. Results of the ATAC (Arimidex, tamoxifen, alone or in combination) trial after completion of 5 years' adjuvant treatment for breast cancer. Lancet 2005; 365:60-62.
25. Coombes RC, Hall E, Gibson LJ, et al. A randomized trial of exemestane after two to three years of tamoxifen therapy in postmenopausal women with primary breast cancer. N Engl J Med 2004; 350:1081-1092.
26. Goss PE, Ingle JN, Martino S, et al. A randomized trial of letrozole in postmenopausal women after five years of tamoxifen therapy for early-stage breast cancer. N Engl J Med 2003; 349:1793-1802.
27. Kaufmann M, Jonat W, Hilfrich J, et al. Survival benefit of switching to anastrozole after 2 years' treatment with tamoxifen versus continued tamoxifen therapy. In: The ARNO 95 Study [poster]. American Society of Clinical Oncology, Atlanta, GA, 2-6 June 2006.
28. Coombes RC, Paridaens R, Jassem J, et al., for the Intergroup Exemestane Study (IES). First mature analysis of the Intergroup Exemestane Study [Abstract LBA527]. J Clin Oncol 2006; 24:18S.
29. Winer EP, Hudis C, Burstein HJ, et al. American Society of Clinical Oncology technology assessment on the use of aromatase inhibitors as adjuvant therapy for postmenopausal women with hormone receptor-positive breast cancer: status report 2004. J Clin Oncol 2005; 23:619-629.
30. Almeida M,Han L,O'Brien CA,et al. Classicalgenotropic versus kinase-initiated regulation of gene transcription by the estrogen receptor alpha. Endocrinology 2006; 147:1986-1996.
31. Kennedy AM, Shogren KL, Zhang M, et al. 17Beta-estradiol-dependent activation of signal transducer and activator of transcription-1 in human fetal osteoblasts is dependent on Src kinase activity. Endocrinology 2005; 146:201-207.
32. Kousteni S, Han L, Chen JR, et al. Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest 2003; 111:1651-1664.
33. Manavathi B, Kumar R. Steering estrogen signals from the plasma membrane to the nucleus: two sides of the coin. J Cell Physiol 2006; 207:594-604.
34. Doren M, Nilsson JA, Johnell O. Effects of specific post-menopausal hormone therapies on bone mineral density in post-menopausal women: a meta-analysis. Hum Reprod 2003; 18:1737-1746.
35. Nelson HD, Humphrey LL, Nygren P, et al. Postmenopausal hormone replacement therapy: scientific review. JAMA 2002; 288:872-881.
36. Torgerson DJ, Bell-Syer SE. Hormone replacement therapy and prevention of nonvertebral fractures: a meta-analysis of randomized trials. JAMA 2001; 285:2891-2897.
37. Komm BS, Terpening CM, Benz DJ, et al. Estrogen binding, receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science 1988; 241:81-84.
38. Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000; 21:115-137.
39. Manolagas SC, Kousteni S, Jilka RL. Sex steroids and bone. Recent Prog Horm Res 2002; 57:385-409.
40. Tomkinson A, Reeve J, Shaw RW, Noble BS. The death of osteocytes via apoptosis accompanies estrogen withdrawal in human bone. J Clin Endocrinol Metab 1997; 82:3128-3135.
41. Hughes DE, Dai A, Tiffee JC, et al. Estrogen promotes apoptosis of murine osteoclasts mediated by TGF-beta. Nat Med 1996; 2:1132-1136.
42. Weitzmann MN, Pacifici R. The role of T lymphocytes in bone metabolism. Immunol Rev 2005; 208:154-168.
43. Kousteni S, Bellido T, Plotkin LI, et al. Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 2001; 104:719-730.
44. Jilka RL, Takahashi K, Munshi M, et al. Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 1998; 101:1942-1950.
45. Weitzmann MN, Roggia C, Toraldo G, et al. Increased production of IL-7 uncouples bone formation from bone resorption during estrogen deficiency. J Clin Invest 2002; 110:1643-1650.
46. Gilbert L, He X, Farmer P, et al. Inhibition of osteoblast differentiation by tumor necrosis factor-alpha. Endocrinology 2000; 141:3956-3964.
47. Garcia-Moreno C, Catalan MP, Ortiz A, et al. Modulation of survival in osteoblasts from postmenopausal women. Bone 2004; 35:170-177.
48. Weitzmann MN, Pacifici R. Estrogen deficiency and bone loss: an inflammatory tale. J Clin Invest 2006; 116:1186-1194.
49. Lean JM, Davies JT, Fuller K, et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J Clin Invest 2003; 112:915-923.
50. Lean JM, Jagger CJ, Kirstein B, et al. Hydrogen peroxide is essential for estrogen-deficiency bone loss and osteoclast formation. Endocrinology 2005; 146:728-735.
51. Ioannidis JP, Ralston SH, Bennett ST, et al. Differential genetic effects of ESR1 gene polymorphisms on osteoporosis outcomes. JAMA 2004; 292:2105-2114.
52. Albagha OM, Pettersson U, Stewart A, et al. Association of oestrogen receptor alpha gene polymorphisms with postmenopausal bone loss, bone mass, and quantitative ultrasound properties of bone. J Med Genet 2005; 42:240-246.
53. Laflamme N, Giroux S, Loredo-Osti JC, et al. A frequent regulatory variant of the estrogen-related receptor alpha gene associated with BMD in French-Canadian premenopausal women. J Bone Miner Res 2005; 20:938-944.
54. Bulun SE, Simpson ER. Competitive reverse transcription-polymerase chain reaction analysis indicates that levels of aromatase cytochrome P450 transcripts in adipose tissue of buttocks, thighs, and abdomen of women increase with advancing age. J Clin Endocrinol Metab 1994; 78:428-432.
55. Nawata H, Tanaka S, Tanaka S, et al. Aromatase in bone cell: association with osteoporosis in postmenopausal women. J Steroid Biochem Mol Biol 1995; 53:165-174.
56. Burger HG, Dudley EC, Hopper JL, et al. Prospectively measured levels of serum follicle-stimulating hormone, estradiol, and the dimeric inhibins during the menopausal transition in population-based cohort of women. J Clin Endocrinol Metab 1999; 84:4025-4030.
57. Pfeilschifter J, Diel IJ. Osteoporosis due to cancer treatment: pathogenesis and management. J Clin Oncol 2000; 18:1570-1593.
58. Chapurlat RD, Gamero P, Sornay-Rendu E, et al. Longitudinal study of bone loss in pre- and perimenopausal women: evidence for bone loss in perimenopausal women. Osteoporos Int 2000; 11:493-498.
59. Sowers MR, Jannausch M, McConnell D, et al. Hormone predictors of bone mineral density changes during the menopausal transition. J Clin Endocrinol Metab 2006; 91:1261-1267.
60. Perrien DS, Achenbach SJ, Bledsoe SE, et al. Bone turnover across the menopause transition: correlations with inhibins and follicle-stimulating hormone. J Clin Endocrinol Metab 2006; 91:1848-1854.
61. Stepan JJ, Pospichal J, Presl J, et al. Bone loss and biochemical indices of bone remodeling in surgically induced postmenopausal women. Bone 1987; 8:279-284.
62. Khosla S, Atkinson EJ, Melton LJ III, Riggs BL. Effects of age and estrogen status on serum parathyroid hormone levels and biochemical markers of bone turnover in women: a population-based study. J Clin Endocrinol Metab 1997; 82:1522-1527.
63. Khosla S, Melton LJ III, Atkinson EJ, et al. Relationship of serum sex steroid levels and bone turnover markers with bone mineral density in men and women: a key role for bioavailable estrogen. J Clin Endocrinol Metab 1998; 83:2266-2274.
64. Slemenda C, Longcope C, Peacock M, et al. Sex steroids, bone mass, and bone loss. A prospective study of pre-, peri-, and postmenopausal women. J Clin Invest 1996; 97:14-21.
65. Rogers A, Saleh G, Hannon RA, et al. Circulating estradiol and osteoprotegerin as determinants of bone turnover and bone density in postmenopausal women. J Clin Endocrinol Metab 2002; 87:4470-4475.
66. Garnero P, Sornay-Rendu E, Claustrat B, Delmas PD. Biochemical markers of bone turnover, endogenous hormones and the risk of fractures in postmenopausal women: the OFELY study. J Bone Miner Res 2000; 15:1526-1536.
67. Stone K, Bauer DC, Black DM, et al. Hormonal predictors of bone loss in elderly women: a prospective study. J Bone Miner Res 1998; 13:1167-1174.
68. Ettinger B, Pressman A, Sklarin P, et al. Associations between low levels of serum estradiol, bone density, and fractures among elderly women: the study of osteoporotic fractures. J Clin Endocrinol Metab 1998; 83:2239-2243.
69. Cummings SR, Browner WS, Bauer D, et al. Endogenous hormones and the risk of hip and vertebral fractures among older women. N Engl J Med 1998; 339:733-738.
70. Devine A, Dick IM, Dhaliwal SS, et al. Prediction of incident osteoporotic fractures in elderly women using the free estradiol index. Osteoporos Int 2005; 16:216-221.
71. Goss PE, Qi S, Cheung AM, et al. Effects of the steroidal aromatase inhibitor exemestane and the nonsteroidal aromatase inhibitor letrozole on bone and lipid metabolism in ovariectomized rats. Clin Cancer Res 2004; 10:5717-5723.
72. Goss PE, Qi S, Josse RG, et al. The steroidal aromatase inhibitor exemestane prevents bone loss in ovariectomized rats. Bone 2004; 34:384-392.
73. Johannessen DC, Engan T, Di Salle E, et al. Endocrine and clinical effects of exemestane (PNU 155971), a novel steroidal aromatase inhibitor, in postmenopausal breast cancer patients: a phase I study. Clin Cancer Res 1997; 3:1101-1108.
74. Giudici D, Ornati G, Briatico G, et al. 6-Methylenandrosta-1,4- diene-3, 17-dione (FCE 24304): a new irreversible aromatase inhibitor. J Steroid Biochem 1988; 30:391-394.
75. McCloskey E. Effects of third-generation aromatase inhibitors on bone. Eur J Cancer 2006; 42:1044-1051.
76. McCloskey, Hannon R, Lakner G, et al. The letrozole (L), exemestane (E), and anastrozole (A) pharmacodynamics (LEAP) trial: a direct comparison of bone biochemical measurements between aromatase inhibitors (AIs) in healthy postmenopausal women [Abstract 555]. J Clin Oncol 2006; 24:555.
77. Donnellan PP, Douglas SL, Cameron DA, Leonard RC. Aromatase inhibitors and arthralgia. J Clin Oncol 2001; 19:2767.
78. Brown WJ, Mishra GD, Dobson A. Changes in physical symptoms during the menopause transition. Int J Behav Med 2002; 9:53-67.
79. Ikeda T, Makita K, Ishitani K, et al. Status of climacteric symptoms among middle-aged to elderly Japanese women: comparison of general healthy women with women presenting at a menopausal clinic. J Obstet Gynaecol Res 2005; 31:164-171.
80. Jansson C, Johansson S, Lindh-Astrand L, et al. The prevalence of symptoms possibly related to the climacteric in pre- and postmenopausal women in Linkoping, Sweden. Maturitas 2003; 45:129-135.
81. Dugan SA, Powell LH, Kravitz HM, et al. Musculoskeletal pain and menopausal status. Clin J Pain 2006; 22:325-331.
82. Ho SC, Chan SG, Yip YB, et al. Menopausal symptoms and symptom clustering in Chinese women. Maturitas 1999; 33:219-227.
83. Adera T, Deyo RA, Donatelle RJ. Premature menopause and low back pain. A population-based study. Ann Epidemiol 1994; 4:416-422.
84. Felson DT,Cummings SR. Aromatase inhibitors and the syndromeof arthralgias with estrogen deprivation. Arthritis Rheum 2005; 52:2594-2598.
85. Carbone LD, Nevitt MC, Wildy K, et al. The relationship of antiresorptive drug use to structural findings and symptoms of knee osteoarthritis. Arthritis Rheum 2004; 50:3516-3525.
86. Iwamoto J, Takeda T, Sato Y, Uzawa M. Effects of alendronate on metacarpal and lumbar bone mineral density, bone resorption, and chronic back pain in postmenopausal women with osteoporosis. Clin Rheumatol 2004; 23:383-389.
87. Manicourt DH, Brasseur JP, Boutsen Y, et al. Role of alendronate in therapy for posttraumatic complex regional pain syndrome type I of the lower extremity. Arthritis Rheum 2004; 50:3690-3697.
88. Nishii T, Sugano N, Miki H, et al. Does alendronate prevent collapse in osteonecrosis of the femoral head? Clin Orthop Relat Res 2006; 443:273-279.
89. Cocco R, Tofi C, Fioravanti A, et al. Effects of clodronate on synovial fluid levels of some inflammatory mediators, after intra-articular administration to patients with synovitis secondary to knee osteoarthritis. Boll Soc Ital Biol Sper 1999; 75:71-76.
90. Hillner BE, Ingle JN, Chlebowski RT, et al. American Society of Clinical Oncology 2003 update on the role of bisphosphonates and bone health issues in women with breast cancer. J Clin Oncol 2003; 21:4042-4057.
91. Brufsky AU, Harler W, Beck J, et al. Zoledronic acid (ZA) effectively inhibits cancer treatment-induced bone loss (CTIBL) in postmenopausal women (PMW) with early breast cancer (BCa) receiving adjuvant letrozole (Let): 12 mos BMD results of the Z-FAST trial [Abstract 23]. J Clin Oncol 2005; 23 (Suppl. 16):533.
92. Flake NM, Bonebreak DB, Gold MS. Estrogen and inflammation increase the excitability of rat temporomandibular joint afferent neurons. J Neurophysiol 2005; 93:1585-1597.
93. Schaible HG. Spinal mechanisms contributing to joint pain. Novartis Found Symp 2004; 260:4-22.
94. Multon S, Pardutz A, Mosen J, et al. Lack of estrogen increases pain in the trigeminal formalin model: a behavioural and immunocytochemical study of transgenic ArKO mice. Pain 2005; 114:257-265.
95. Bosse R, DiPaolo T. The modulation of brain dopamine and GABAA receptors by estradiol: a clue for CNS changes occurring at menopause. Cell Mol Neurobiol 1996; 16:199-212.
96. Bosse R, Rivest R, Di Paolo T. Ovariectomy and estradiol treatment affect the dopamine transporter and its gene expression in the rat brain. Brain Res Mol Brain Res 1997; 46:343-346.
97. Smith YR, Stohler CS, Nichols TE, et al. Pronociceptive and antinociceptive effects of estradiol through endogenous opioid neurotransmission in women. J Neurosci 2006; 26:5777-5785.