Vol. 70 No. 2 (2024), REVIEWS

Vol. 70 No. 2 (2024)

Inflammatory Rheumatic Disorders as a Complication of Endocrine Therapy for Breast Cancer

REVIEWS

https://doi.org/10.37469/0507-3758-2024-70-2-259-266

Published 06.05.2024

Anastasia D. Koltakova⁺⁻
Alexandr M. Lila⁺⁻

Anastasia D. Koltakova

V.A. Nasonova Research Institute of Rheumatology

https://orcid.org/0000-0003-0576-4870

Alexandr M. Lila

V.A. Nasonova Research Institute of Rheumatology

https://orcid.org/0000-0002-6068-3080

pdf (Русский)

Keywords

arthralgia
aromatase inhibitors
tamoxifen
breast cancer
rheumatic disorders
musculoskeletal disorders
hormone therapy

How to Cite

Koltakova, A. D., & Lila, A. M. (2024). Inflammatory Rheumatic Disorders as a Complication of Endocrine Therapy for Breast Cancer. Voprosy Onkologii, 70(2), 259–266. https://doi.org/10.37469/0507-3758-2024-70-2-259-266

Abstract

Hormone-sensitive breast cancer (HSC) is a common neoplastic disorder. HSC treatment involves endocrine therapy, which is strongly associated with joint pain. The cause of arthralgia in these patients is still unclear, but there are indications that it may be inflammation driven. The article presents the current understanding of this issue and highlights the pathophysiological mechanisms of the autoimmune and autoinflammatory pathology development in BC patients receiving estrogen deprivation therapy.

https://doi.org/10.37469/0507-3758-2024-70-2-259-266

pdf (Русский)

References

Sung H., Ferlay J., Siegel R.L., et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021; 71(3): 209-249.-DOI: https://doi.org/10.3322/caac.21660.

Мерабишвили В.М. Состояние онкологической помощи в России: рак молочной железы среди женского населения. Заболеваемость, смертность, достоверность учета, детальная локализационная и гистологическая структура. (Популяционное исследование на уровне федерального округа). Вопросы онкологии. 2022; 68(3): 286-293.-DOI: https://doi.org/10.37469/0507-3758-2022-68-3-286-293. URL: https://voprosyonkologii.ru/index.php/journal/article/view/1373.

[Merabishvili V.M. The state of cancer care In Russia: breast cancer among the female population. Morbidity, mortality, index of accuracy, detailed localization and histological structure. (Population study at the federal district level). Voprosy Onkologii = Problems in Oncology. 2022; 68(3): 286-293.-DOI: https://doi.org/10.37469/0507-3758-2022-68-3-286-293. URL: https://voprosyonkologii.ru/index.php/journal/article/view/1373. (In Rus)].

Howlader N., Altekruse S.F., Li C.I., et al. US incidence of breast cancer subtypes defined by joint hormone receptor and HER2 status. J Natl Cancer Inst. 2014; 106(5): dju055.-DOI: https://doi.org/10.1093/jnci/dju055.

Cardoso F., Senkus E., Costa A., et al. 4th ESO-ESMO International Consensus Guidelines for Advanced Breast Cancer (ABC 4). Ann Oncol. 2018; 29(8): 1634-57.-DOI: https://doi.org/10.1093/annonc/mdy192.

Кононенко И.Б., Снеговой А.В., Гребенникова О.П., и др. Побочные эффекты адъювантной гормонотерапии. Медицинский совет. 2018; (10): 64-69.-DOI: https://doi.org/10.21518/2079-701X-2018-10-64-69.

[Kononenko I.B., Snegovoi AV, Grebennikova O.P., et al. Adverse effects of adjuvant endocrine therapy. Meditsinskiy sovet = Medical Council. 2018; (10): 64-69.-DOI: https://doi.org/10.21518/2079-701X-2018-10-64-69. (In Rus)].

Beckwée D., Leysen L., Meuwis K., Adriaenssens N. Prevalence of aromatase inhibitor-induced arthralgia in breast cancer: a systematic review and meta-analysis. Support Care Cancer. 2017; 25(5): 1673-86.-DOI: https://doi.org/10.1007/s00520-017-3613-z.

Rangel-Méndez J.A., Rubi-Castellanos R., Sánchez-Cruz J.F., Moo-Puc R.E. Tamoxifen side effects: pharmacogenetic and clinical approach in Mexican mestizos. Transl Cancer Res. 2019; 8(1): 23-34.-DOI: https://doi.org/10.21037/tcr.2018.12.27.

Friedman A.J., Juneau-Norcross M., Rein M.S. Adverse effects of leuprolide acetate depot treatment. Fertil Steril. 1993; 59(2): 448-50.-DOI: https://doi.org/10.1016/s0015-0282(16)55701-x.

Owens C., Andelkovic V., Pathmanathan S., et al. Early discontinuation rates of aromatase inhibitors due to musculoskeletal side effects. Breast Cancer Management. 2016: 5(1);13-20.-DOI: https://doi.org/10.2217/bmt.15.29.

Henry N.L., Azzouz F., Desta Z., et al. Predictors of aromatase inhibitor discontinuation as a result of treatment-emergent symptoms in early-stage breast cancer. J Clin Oncol. 2012; 30: 936-42.-DOI: https://doi.org/10.1200/JCO.2011.38.0261.

Wendling D., Letho-Gyselinck H., Guillot X., et al. Arthralgia and aromatase inhibitors. Joint Bone Spine. 2014; 81(2): 187-8.-DOI: https://doi.org/10.1016/j.jbspin.2013.06.011.

Chim K., Xie S.X., Stricker C.T., et al. Joint pain severity predicts premature discontinuation of aromatase inhibitors in breast cancer survivors. BMC Cancer. 2013; 13: 401.-DOI: https://doi.org/10.1186/1471-2407-13-401.

Hershman D.L., Shao T., Kushi L.H., et al. Early discontinuation and non-adherence to adjuvant hormonal therapy are associated with increased mortality in women with breast cancer. Breast Cancer Res Treat. 2011; 126(2): 529-37.-DOI: https://doi.org/10.1007/s10549-010-1132-4.

Donnellan P.P., Douglas S.L., Cameron D.A., Leonard R.C. Aromatase inhibitors and arthralgia. J Clin Oncol. 2001; 19(10): 2767.

Moxley G. Rheumatic disorders and functional disability with aromatase inhibitor therapy. Clin Breast Cancer. 2010; 10(2): 144-7.-DOI: https://doi.org/10.3816/CBC.2010.n.019.

Henry N.L., Giles J.T., Ang D., et al. Prospective characterization of musculoskeletal symptoms in early stage breast cancer patients treated with aromatase inhibitors. Breast Cancer Res Treat. 2008; 111(2): 365-72.-DOI: https://doi.org/10.1007/s10549-007-9774-6.

Lintermans A., Laenen A., Van Calster B., et al. Prospective study to assess fluid accumulation and tenosynovial changes in the aromatase inhibitor-induced musculoskeletal syndrome: 2-year follow-up data. Ann Oncol. 2013; 24(2): 350-5.-DOI: https://doi.org/10.1093/annonc/mds290.

Shin D.J., Nam K.E., Song D.H., et al. Carpal tunnel syndrome and tenosynovitis in women with breast cancer associated with hormone therapy: A multi-institutional analysis using a clinical data warehouse. Medicine (Baltimore). 2022; 101(5): e28786.-DOI: https://doi.org/10.1097/MD.0000000000028786.

Morales L., Pans S., Paridaens R., et al. Debilitating musculoskeletal pain and stiffness with letrozole and exemestane: associated tenosynovial changes on magnetic resonance imaging. Breast Cancer Res Treat. 2007; 104(1): 87-91.-DOI: https://doi.org/10.1007/s10549-006-9394-6.

Scarpa R., Atteno M., Peluso R., et al. Rheumatic complaints in women taking aromatase inhibitors for treatment of hormone-dependent breast cancer. J Clin Rheumatol. 2011; 17(4): 169-72.-DOI: https://doi.org/10.1097/RHU.0b013e31821bfc48.

Laroche M., Borg S., Lassoued S., et al. Joint pain with aromatase inhibitors: abnormal frequency of Sjögren's syndrome. J Rheumatol. 2007; 34(11): 2259-63.

Laroche M., Seniow M., Roché H., et al. Arthralgia associated with autoimmune abnormalities under aromatase inhibitor therapy: outcome after cessation of treatment. J Rheumatol. 2016; 43(10): 1945-6.-DOI: https://doi.org/10.3899/jrheum.160254.

Chen J.Y., Ballou S.P. The effect of antiestrogen agents on risk of autoimmune disorders in patients with breast cancer. J Rheumatol. 2015; 42(1): 55-9.-DOI: https://doi.org/10.3899/jrheum.140367.

Caprioli M., Carrara G., Sakellariou G., et al. Influence of aromatase inhibitors therapy on the occurrence of rheumatoid arthritis in women with breast cancer: results from a large population-based study of the Italian Society for Rheumatology. RMD Open. 2017; 3(2): e000523.-DOI: https://doi.org/10.1136/rmdopen-2017-000523.

Chien H.C., Kao Yang Y.H., Kwoh C.K., et al. Aromatase Inhibitors and Risk of Arthritis and Carpal Tunnel Syndrome among Taiwanese Women with Breast Cancer: A Nationwide Claims Data Analysis. J Clin Med. 2020; 9(2): 566.-DOI: https://doi.org/10.3390/jcm9020566

Колтакова А.Д., Лила А.М., Алексеева О.Г. Ревматические аспекты артралгий, ассоциированных с терапией ингибиторами ароматазы (анализ серии клинических случаев). Современная ревматология. 2023; 17(1): 51-7.-DOI: https://doi.org/10.14412/1996-7012-2023-1-51-57.

[Koltakova A.D., Lila A.M., Alekseeva O.G. Rheumatic aspects of arthralgias associated with aromatase inhibitor therapy (analysis of a clinical case series). Sovremennaya Revmatologiya = Modern Rheumatology Journal. 2023; 17(1): 51-57.-DOI: https://doi.org/10.14412/1996-7012-2023-1-51-57. (In Rus)].

Szoeke C.E., Cicuttini F.M., Guthrie J.R., et al. The relationship of reports of aches and joint pains to the menopausal transition: a longitudinal study. Climacteric. 2008; 11(1): 55-62.-DOI: https://doi.org/10.1080/13697130701746006.

Goemaere S., Ackerman C., Goethals K., et al. Onset of symptoms of rheumatoid arthritis in relation to age, sex and menopausal transition. J Rheumatol. 1990; 17(12): 1620-2.

Cecil R.L., Archer B.H. Arthritis of the menopause: a study of fifty cases. J Am Med Assoc. 1925; 84: 75-9.-DOI: https://doi.org/10.1001/jama.1925.02660280001001.

Magliano M. Menopausal arthralgia: Fact or fiction. Maturitas. 2010; 67(1): 29-33.-DOI: https://doi.org/10.1016/j.maturitas.2010.04.009.

Cutolo M., Accardo S., Villaggio B., et al. Presence of estrogen-binding sites on macrophage-like synoviocytes and CD8+, CD29+, CD45RO+ T lymphocytes in normal and rheumatoid synovium. Arthritis Rheum. 1993; 36(8): 1087-97.-DOI: https://doi.org/10.1002/art.1780360809.

Richmond R.S., Carlson C.S., Register T.C., et al. Functional estrogen receptors in adult articular cartilage: estrogen replacement therapy increases chondrocyte synthesis of proteoglycans and insulin-like growth factor binding protein 2. Arthritis Rheum. 2000; 43(9): 2081-90.-DOI: https://doi.org/10.1002/1529-0131(200009)43:9<2081::AID-ANR20>3.0.CO;2-I.

Chen X., Cai C., Liu J., et al. Impact of estrogen-related receptor α on the biological characteristics of rat mandibular condylar chondrocytes. Mol Med Rep. 2014; 10(1): 195-202.-DOI: https://doi.org/10.3892/mmr.2014.2210.

Nalbandian G., Kovats S. Estrogen, immunity & autoimmune disease. Curr Med Chem – Immun, Endoc & Metab Agents. 2005; 5: 85-91.-DOI: https://doi.org/10.2174/1568013053005418.

Straub R.H. The complex role of estrogens in inflammation. Endocr Rev. 2007; 28(5): 521-74.-DOI: https://doi.org/10.1210/er.2007-0001.

Josefsson E., Tarkowski A. Suppression of type II collageninduced arthritis by the endogenous estrogen metabolite 2-methoxyestradiol. Arthritis Rheum. 1997; 40(1): 154-63.-DOI: https://doi.org/10.1002/art.1780400120.

Wang J.X., Zhang Q.Y., Jin S., et al. Genistein modulate immune responses in collagen-induced rheumatoid arthritis model. Maturitas. 2008; 59(4): 405-12.-DOI: https://doi.org/10.1016/j.maturitas.2008.04.003.

Jeong H., Bae E.K., Kim H., et al. Estrogen attenuates the spondyloarthritis manifestations of the SKG arthritis model. Arthritis Res Ther. 2017; 19(1): 198.-DOI: https://doi.org/10.1186/s13075-017-1407-9.

Liu Y.P., Li J., Xin S.B., X J. Study the relevance between inflammatory factors and estradiol and their association with knee osteoarthritis in postmenopausal women. Eur Rev Med Pharmacol Sci. 2018; 22(2): 472-478.-DOI: https://doi.org/10.26355/eurrev_201801_14197.

Vural P., Canbaz M., Akgul C. Effects of menopause and postmenopausal tibolone treatment on plasma TNFalpha, IL-4, IL-10, IL-12 cytokine pattern and some bone turnover markers. Pharmacol Res. 2006; 53(4): 367-71.-DOI: https://doi.org/10.1016/j.phrs.2006.01.005.

Afzal S., Khanam A. Serum estrogen and interleukin-6 levels in postmenopausal female osteoarthritis patients. Pak J Pharm Sci. 2011; 24: 217-9.

Saito S., Aras R.S., Lou H., et al. Effects of estrogen on nitric oxide synthase expression in rat aorta allograft and smooth muscle cells. J Heart Lung Transplant. 1999; 18(10): 937-45.-DOI: https://doi.org/10.1016/s1053-2498(99)00060-1.

Huang N., Wang C., Zhang N., et al. Effect of estrogen on prostaglandin synthetase in bovine oviduct smooth muscle. Eur J Pharmacol. 2018; 818: 287-93.-DOI: https://doi.org/10.1016/j.ejphar.2017.10.058.

Jung J.H., Bang C.H., Song G.G., et al. Knee osteoarthritis and menopausal hormone therapy in postmenopausal women: a nationwide cross-sectional study. Menopause. 2018; 26(6): 598-602.-DOI: https://doi.org/10.1097/GME.0000000000001280.

Xiao Y.P., Tian F.M., Dai M.W., et al. Are estrogen-related drugs new alternatives for the management of osteoarthritis? Arthritis Res Ther. 2016; 18: 151.-DOI: https://doi.org/10.1186/s13075-016-1045-7.

Jimenez-Balderas F.J., Tapia-Serrano R., Madero-Cervera J.I., et al. Ovarian function studies in active ankylosing spondylitis in women. Clinical response to estrogen therapy. J Rheumatol. 1990; 17(4): 497-502.

Cortés M., Canellada A., Miranda S., et al. Placental secreted factors: their role in the regulation of anti-CII antibodies and amelioration of collagen induced arthritis in rats. Immunol Lett. 2008; 119(1-2): 42-8.-DOI: https://doi.org/10.1016/j.imlet.2008.04.001.

Jingxuan W., Qingyuan Z., Shi J., et al. Immoderate inhibition of estrogen by anastrozole enhances the severity of experimental polyarthritis. Experimental Gerontology. Exp Gerontol. 2009; 44(6-7): 398-405.-DOI: https://doi.org/10.1016/j.exger.2009.03.003.

Watson W.C., Townes A.S. Genetic susceptibility to murine collagen II autoimmune arthritis. Proposed relationship to the IgG2 autoantibody subclass response, complement C5, major histocompatibility complex (MHC) and nonMHC loci. J Exp Med. 1985; 162(6): 1878-9.-DOI: https://doi.org/10.1084/jem.162.6.1878.

Zhao J., Li R., He J., et al. Mucosal administration of an altered CII263–272 peptide inhibits collagen-induced arthritis by suppression of Th1/Th17 cells and expansion of regulatory T cells. Rheumatol Int. 2008; 29(1): 9-16.-DOI: https://doi.org/10.1007/s00296-008-0634-4.

Young N.A., Hampton J., Sharma J., et al. Aromatase inhibitor induced musculoskeletal inflammation is observed independent of oophorectomy in a novel mouse model. BioRxiv. 2022.-DOI: https://doi.org/10.1101/2022.06.22.497263.

Young N.A., Hampton J., Sharma J., et al. Aromatase-inhibitor-induced musculoskeletal inflammation is observed independent of oophorectomy in a novel mouse model. Pharmaceuticals (Basel). 2022; 15(12): 1578.-DOI: https://doi.org/10.3390/ph15121578.

Shim G.J., Warner M., Kim H.J., et al. Aromatase-deficient mice spontaneously develop a lymphoproliferative autoimmune disease resembling Sjogren's syndrome. Proc Natl Acad Sci USA. 2004: 101(34): 12628-33.-DOI: https://doi.org/10.1073/pnas.0405099101.

Iwasa A., Arakaki R., Honma N., et al. Aromatase controls Sjögren syndrome-like lesions through monocyte chemotactic protein-1 in target organ and adipose tissue-associated macrophages. Am J Pathol. 2015; 185(1): 151-61.-DOI: https://doi.org/10.1016/j.ajpath.2014.09.006.

Fuentes N., Silveyra P. Estrogen receptor signaling mechanisms. Adv Protein Chem Struct Biol. 2019; 116: 135-70.-DOI: https://doi.org/10.1016/bs.apcsb.2019.01.001.

Sthoeger Z.M., Zinger H., Mozes E. Beneficial effects of the anti-oestrogen tamoxifen on systemic lupus erythematosus of (NZBxNZW)F1 female mice are associated with specific reduction of IgG3 autoantibodies. Ann Rheum Dis. 2003; 62(4): 341-6.-DOI: https://doi.org/10.1136/ard.62.4.341.

Sturgess A.D., Evans D.T., Mackay I.R., Riglar A. Effects of the oestrogen antagonist tamoxifen on disease indices in systemic lupus erythematosus. J Clin Lab Immunol. 1984; 13(1): 11-4.

Mohammed E.A., Sharief N., Abukashawa S., et al., Tamoxifen-induced lupus erythematosus. J Drug Metab Toxicol. 2013; 4: 1.-DOI: https://doi.org/10.4172/2157-7609.1000138.

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.