The Role of Chronic Psychological Stress in the Pathogenesis of Osteoporosis: Associated Mechanisms and Potential Biomarkers

Yıl 2023, Cilt: 6 Sayı: 1, 40 - 51, 30.04.2023

Cihan Akdoğan Funda Bayındır

https://doi.org/10.47141/geriatrik.1147586

Öz

Osteoporosis is an age-related bone disease characterized by reduced bone mass and destruction of bone microarchitecture, leading to fracture risk. Organisms are constantly exposed to various stressful stimuli that affect physiological processes. At the present time, it has been shown that physical stress affects the bone structure by stimulates the bone remodeling. It is reported in the literature that chronic psychological stress as well as physical stress is a risk factor for osteoporosis by various signaling pathways. Both animal and human studies show that chronic psychological stress causes reduction in bone mass and deterioration in bone quality by affecting various pathways, including the hypothalamic-pituitary-adrenocortical (HPA) axis, sympathetic nervous system, and other endocrine factors. This review discusses for psychological stress as risk factor for osteoporosis, associated mechanisms and potential biomarkers.

Anahtar Kelimeler

biomarker, osteoporosis, physiological stress

Kronik Psikolojik Stresin Osteoporoz Patogenezindeki Rolü: İlişkili Mekanizmalar ve Potansiyal Biyobelirteçler

Öz

Osteoporoz, azalmış kemik kütlesi ve kemik mikromimarisinin yıkımı ile karakterize kırık riskine neden olan yaşa bağlı bir kemik hastalığıdır. Organizmalar sürekli olarak fizyolojik süreçleri etkileyen çeşitli stresli uyaranlara maruz kalırlar. Günümüzde, fiziksel stresin kemik remodelingini uyararak kemik yapısını etkilediği gösterilmiştir. Literatürde, fiziksel stresin yanı sıra kronik psikolojik stresin de çeşitli sinyal yollarıyla osteoporoz için bir risk faktörü olduğu bildirilmektedir. Hem hayvan hem de insan çalışmaları, kronik psikolojik stresin hipotalamik-hipofiz-adrenokortikal (HPA) ekseni, sempatik sinir sistemi ve diğer endokrin faktörleri dahil olmak üzere çeşitli yolları etkileyerek kemik kütlesinde azalmaya ve kemik kalitesinde bozulmaya neden olduğunu göstermektedir. Bu derlemede, osteoporoz için risk faktörü olarak kronik psikolojik stres, ilişkili mekanizmalar ve potansiyal biyobelirteçler tartışılmaktadır.

Anahtar Kelimeler

biyobelirteç, osteoporoz, psikolojik stres

Kaynakça

• He Y, Wuertz K, Kuehl L, Wippert P-M. Extracellular Vesicles: Potential Mediators of Psychosocial Stress Contribution to Osteoporosis? International Journal of Molecular Sciences. 2021;22:5846.
• Kelly RR, McDonald LT, Jensen NR, Sidles SJ, LaRue AC. Impacts of Psychological Stress on Osteoporosis: Clinical Implications and Treatment Interactions. Frontiers in psychiatry. 2019;10:200.
• Singhal S, Chand P, Singh BP, Singh SV, Rao J, Shankar R, et al. The effect of osteoporosis on residual ridge resorption and masticatory performance in denture wearers. Gerodontology. 2012;29(2):e1059-e66.
• von Wowern N, Kollerup G. Symptomatic osteoporosis: a risk factor for residual ridge reduction of the jaws. The Journal of prosthetic dentistry. 1992;67(5):656-60.
• Berkey DB, Berg RG, Ettinger RL, Mersel A, Mann J. The old-old dental patient: the challenge of clinical decision-making. Journal of the American Dental Association (1939). 1996;127(3):321-32.
• Duymuş ZY, Esra K. Total protez olgularinda si̇stemi̇k hastaliklarin önemi̇. Atatürk Üniversitesi Diş Hekimliği Fakültesi Dergisi.24(Supplement 8):125-30.
• de Medeiros F, Kudo GAH, Leme BG, Saraiva PP, Verri FR, Honório HM, et al. Dental implants in patients with osteoporosis: a systematic review with meta-analysis. Int J Oral Maxillofac Surg. 2018;47(4):480-91.
• Alghamdi HS, Jansen JA. Bone regeneration associated with nontherapeutic and therapeutic surface coatings for dental implants in osteoporosis. Tissue Engineering Part B: Reviews. 2013;19(3):233-53.
• Alghamdi H, Cuijpers V, Wolke J, Van den Beucken J, Jansen J. Calcium-phosphate-coated oral implants promote osseointegration in osteoporosis. Journal of dental research. 2013;92(11):982-8.
• Alsaadi G, Quirynen M, Komárek A, Van Steenberghe D. Impact of local and systemic factors on the incidence of oral implant failures, up to abutment connection. Journal of clinical periodontology. 2007;34(7):610-7.
• Von Wowern N, Gotfredsen K. Implant‐supported overdentures, a prevention of bone loss in edentulous mandibles? A 5‐year follow‐up study. Clinical oral implants research. 2001;12(1):19-25.
• Sözen T, Özışık L, Başaran N. An overview and management of osteoporosis. European journal of rheumatology. 2017;4(1):46-56.
• Osteoporosis prevention, diagnosis, and therapy. Jama. 2001;285(6):785-95.
• Cizza G, Primma S, Csako G. Depression as a risk factor for osteoporosis. Trends in endocrinology and metabolism: TEM. 2009;20(8):367-73.
• Bab I, Yirmiya R. Depression, selective serotonin reuptake inhibitors, and osteoporosis. Current osteoporosis reports. 2010;8(4):185-91.
• Erez HB, Weller A, Vaisman N, Kreitler S. The relationship of depression, anxiety and stress with low bone mineral density in post-menopausal women. Archives of osteoporosis. 2012;7:247-55.
• Chrousos GP. Stress and disorders of the stress system. Nature reviews Endocrinology. 2009;5(7):374-81.
• Nicolaides NC, Kyratzi E, Lamprokostopoulou A, Chrousos GP, Charmandari E. Stress, the stress system and the role of glucocorticoids. Neuroimmunomodulation. 2015;22(1-2):6-19.
• Kvetnansky R, Lu X, Ziegler MG. Stress-triggered changes in peripheral catecholaminergic systems. Advances in pharmacology (San Diego, Calif). 2013;68:359-97.
• Baum A. Stress, intrusive imagery, and chronic distress. Health psychology : official journal of the Division of Health Psychology, American Psychological Association. 1990;9(6):653-75.
• Miller GE, Murphy ML, Cashman R, Ma R, Ma J, Arevalo JM, et al. Greater inflammatory activity and blunted glucocorticoid signaling in monocytes of chronically stressed caregivers. Brain, behavior, and immunity. 2014;41:191-9.
• Azuma K, Adachi Y, Hayashi H, Kubo KY. Chronic Psychological Stress as a Risk Factor of Osteoporosis. Journal of UOEH. 2015;37(4):245-53.
• Schulz A, Vögele C. Interoception and Stress. Frontiers in psychology. 2015;6:993.
• Oakley RH, Cidlowski JA. The biology of the glucocorticoid receptor: new signaling mechanisms in health and disease. The Journal of allergy and clinical immunology. 2013;132(5):1033-44.
• Sapolsky RM, Romero LM, Munck AU. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine reviews. 2000;21(1):55-89.
• Cohen S, Janicki-Deverts D, Miller GE. Psychological stress and disease. Jama. 2007;298(14):1685-7.
• Marin MF, Lord C, Andrews J, Juster RP, Sindi S, Arsenault-Lapierre G, et al. Chronic stress, cognitive functioning and mental health. Neurobiology of learning and memory. 2011;96(4):583-95.
• Proietti R, Mapelli D, Volpe B, Bartoletti S, Sagone A, Dal Bianco L, et al. Mental stress and ischemic heart disease: evolving awareness of a complex association. Future cardiology. 2011;7(3):425-37.
• Furuzawa M, Chen H, Fujiwara S, Yamada K, Kubo KY. Chewing ameliorates chronic mild stress-induced bone loss in senescence-accelerated mouse (SAMP8), a murine model of senile osteoporosis. Experimental gerontology. 2014;55:12-8.
• Kurahashi M, Kondo H, Iinuma M, Tamura Y, Chen H, Kubo KY. Tooth loss early in life accelerates agerelated bone deterioration in mice. Tohoku J Exp Med. 2015;235(1):29-37.
• Zigdon-Giladi H, Rudich U, Michaeli Geller G, Evron A. Recent advances in bone regeneration using adult stem cells. World journal of stem cells. 2015;7(3):630-40.
• Bonewald LF. The amazing osteocyte. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 2011;26(2):229-38.
• Yoo S, Blackshaw S. Regulation and function of neurogenesis in the adult mammalian hypothalamus. Progress in neurobiology. 2018;170:53-66.
• Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, et al. Leptin regulates bone formation via the sympathetic nervous system. Cell. 2002;111(3):305-17.
• Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell. 2000;100(2):197-207.
• Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman J. Positional cloning of the mouse obese gene and its human homolog. Nature. 1995;372:425-32.
• Tartaglia LA, Dembski M, Weng X, Deng N, Culpepper J, Devos R, et al. Identification and expression cloning of a leptin receptor, OB-R. Cell. 1995;83(7):1263-71.
• Riggs BL, Melton LJ, 3rd. Involutional osteoporosis. The New England journal of medicine. 1986;314(26):1676-86.
• Ahima RS, Bjorbaek C, Osei S, Flier JS. Regulation of neuronal and glial proteins by leptin: implications for brain development. Endocrinology. 1999;140(6):2755-62.
• Ahima RS. Body fat, leptin, and hypothalamic amenorrhea. The New England journal of medicine. 2004;351(10):959-62.
• Elefteriou F, Campbell P, Ma Y. Control of bone remodeling by the peripheral sympathetic nervous system. Calcified tissue international. 2014;94(1):140-51.
• de Vries F, Pouwels S, Bracke M, Leufkens HG, Cooper C, Lammers JW, et al. Use of beta-2 agonists and risk of hip/femur fracture: a population-based case-control study. Pharmacoepidemiology and drug safety. 2007;16(6):612-9.
• Farr JN, Charkoudian N, Barnes JN, Monroe DG, McCready LK, Atkinson EJ, et al. Relationship of sympathetic activity to bone microstructure, turnover, and plasma osteopontin levels in women. The Journal of clinical endocrinology and metabolism. 2012;97(11):4219-27.
• Seibel MJ, Cooper MS, Zhou H. Glucocorticoidinduced osteoporosis: mechanisms, management, and future perspectives. The lancet Diabetes & endocrinology. 2013;1(1):59-70.
• Franquinho F, Liz MA, Nunes AF, Neto E, Lamghari M, Sousa MM. Neuropeptide Y and osteoblast differentiation--the balance between the neuroosteogenic network and local control. The FEBS journal. 2010;277(18):3664-74.
• Hill EL, Elde R. Distribution of CGRP-, VIP-, D beta H-, SP-, and NPY-immunoreactive nerves in the periosteum of the rat. Cell and tissue research. 1991;264(3):469-80.
• Bjurholm A, Kreicbergs A, Terenius L, Goldstein M, Schultzberg M. Neuropeptide Y-, tyrosine hydroxylase- and vasoactive intestinal polypeptideimmunoreactive nerves in bone and surrounding tissues. Journal of the autonomic nervous system. 1988;25(2-3):119-25.
• Ahmad T, Ugarph-Morawski A, Li J, Bileviciute- Ljungar I, Finn A, Ostenson CG, et al. Bone and joint neuropathy in rats with type-2 diabetes. Regulatory peptides. 2004;119(1-2):61-7.
• Ahmed M, Srinivasan GR, Theodorsson E, Bjurholm A, Kreicbergs A. Extraction and quantitation of neuropeptides in bone by radioimmunoassay. Regulatory peptides. 1994;51(3):179-88.
• Bjurholm A. Neuroendocrine peptides in bone. International orthopaedics. 1991;15(4):325-9.
• Bjurholm A, Kreicbergs A, Schultzberg M, Lerner UH. Neuroendocrine regulation of cyclic AMP formation in osteoblastic cell lines (UMR-106-01, ROS 17/2.8, MC3T3-E1, and Saos-2) and primary bone cells. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 1992;7(9):1011-9.
• Cosman F. Long-term treatment strategies for postmenopausal osteoporosis. Current opinion in rheumatology. 2018;30(4):420-6.
• Kerschan-Schindl K. Prevention and rehabilitation of osteoporosis. Wiener medizinische Wochenschrift (1946). 2016;166(1-2):22-7.
• Baccaro LF, Conde DM, Costa-Paiva L, Pinto- Neto AM. The epidemiology and management of postmenopausal osteoporosis: a viewpoint from Brazil. Clinical interventions in aging. 2015;10:583-91.
• Schweiger U, Deuschle M, Körner A, Lammers CH, Schmider J, Gotthardt U, et al. Low lumbar bone mineral density in patients with major depression. The American journal of psychiatry. 1994;151(11):1691-3.
• Coelho R, Silva C, Maia A, Prata J, Barros H. Bone mineral density and depression: a community study in women. Journal of psychosomatic research. 1999;46(1):29-35.
• Jacka FN, Pasco JA, Henry MJ, Kotowicz MA, Dodd S, Nicholson GC, et al. Depression and bone mineral density in a community sample of perimenopausal women: Geelong Osteoporosis Study. Menopause (New York, NY). 2005;12(1):88-91.
• Wong SY, Lau EM, Lynn H, Leung PC, Woo J, Cummings SR, et al. Depression and bone mineral density: is there a relationship in elderly Asian men? Results from Mr. Os (Hong Kong). Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2005;16(6):610-5.
• Halbreich U, Rojansky N, Palter S, Hreshchyshyn M, Kreeger J, Bakhai Y, et al. Decreased bone mineral density in medicated psychiatric patients. Psychosomatic medicine. 1995;57(5):485-91.
• Cizza G, Primma S, Coyle M, Gourgiotis L, Csako G. Depression and osteoporosis: a research synthesis with meta-analysis. Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme. 2010;42(7):467-82.
• Yirmiya R, Bab I. Major depression is a risk factor for low bone mineral density: a meta-analysis. Biological psychiatry. 2009;66(5):423-32.
• Wu Q, Magnus JH, Liu J, Bencaz AF, Hentz JG. Depression and low bone mineral density: a metaanalysis of epidemiologic studies. Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2009;20(8):1309-20.
• Bottaccioli AG, Bottaccioli F, Minelli A. Stress and the psyche-brain-immune network in psychiatric diseases based on psychoneuroendocrineimmunology: a concise review. Annals of the New York Academy of Sciences. 2019;1437(1):31-42.
• Chrousos GP. Stress, chronic inflammation, and emotional and physical well-being: concurrent effects and chronic sequelae. The Journal of allergy and clinical immunology. 2000;106(5 Suppl):S275-91.
• Cohen S, Janicki-Deverts D, Doyle WJ, Miller GE, Frank E, Rabin BS, et al. Chronic stress, glucocorticoid receptor resistance, inflammation, and disease risk. Proceedings of the National Academy of Sciences of the United States of America. 2012;109(16):5995-9.
• Dhabhar FS. Effects of stress on immune function: the good, the bad, and the beautiful. Immunologic research. 2014;58(2-3):193-210.
• Heidt T, Sager HB, Courties G, Dutta P, Iwamoto Y, Zaltsman A, et al. Chronic variable stress activates hematopoietic stem cells. Nature medicine. 2014;20(7):754-8.
• Eastell R, O’Neill TW, Hofbauer LC, Langdahl B, Reid IR, Gold DT, et al. Postmenopausal osteoporosis. Nature reviews Disease primers. 2016;2:16069.
• Michelson D, Stratakis C, Hill L, Reynolds J, Galliven E, Chrousos G, et al. Bone mineral density in women with depression. The New England journal of medicine. 1996;335(16):1176-81.
• Altindag O, Altindag A, Asoglu M, Gunes M, Soran N, Deveci Z. Relation of cortisol levels and bone mineral density among premenopausal women with major depression. International journal of clinical practice. 2007;61(3):416-20.
• Chotiyarnwong P, McCloskey EV. Pathogenesis of glucocorticoid-induced osteoporosis and options for treatment. Nature reviews Endocrinology. 2020;16(8):437-47.
• Lane NE. Glucocorticoid-Induced Osteoporosis: New Insights into the Pathophysiology and Treatments. Current osteoporosis reports. 2019;17(1):1-7.
• Vega D, Maalouf NM, Sakhaee K. The Role of Receptor Activator of Nuclear Factor-κB (RANK)/RANK Ligand/Osteoprotegerin: Clinical Implications. The Journal of clinical endocrinology and metabolism. 2007;92(12):4514-21.
• Schildkraut JJ. The catecholamine hypothesis of affective disorders: a review of supporting evidence. The American journal of psychiatry. 1965;122(5):509-22.
• Vaessen T, Hernaus D, Myin-Germeys I, van Amelsvoort T. The dopaminergic response to acute stress in health and psychopathology: A systematic review. Neuroscience and biobehavioral reviews. 2015;56:241-51.
• Rodrigues WF, Madeira MF, da Silva TA, Clemente- Napimoga JT, Miguel CB, Dias-da-Silva VJ, et al. Low dose of propranolol down-modulates bone resorption by inhibiting inflammation and osteoclast differentiation. British journal of pharmacology. 2012;165(7):2140-51.
• Kondo H, Togari A. Continuous treatment with a low-dose β-agonist reduces bone mass by increasing bone resorption without suppressing bone formation. Calcified tissue international. 2011;88(1):23-32.
• Kondo H, Takeuchi S, Togari A. β-Adrenergic signaling stimulates osteoclastogenesis via reactive oxygen species. American journal of physiology Endocrinology and metabolism. 2013;304(5):E507-15.
• Dimitri P, Rosen C. The Central Nervous System and Bone Metabolism: An Evolving Story. Calcified tissue international. 2017;100(5):476-85.
• Warden SJ, Bliziotes MM, Wiren KM, Eshleman AJ, Turner CH. Neural regulation of bone and the skeletal effects of serotonin (5-hydroxytryptamine). Molecular and cellular endocrinology. 2005;242(1-2):1-9.
• Bliziotes MM, Eshleman AJ, Zhang XW, Wiren KM. Neurotransmitter action in osteoblasts: expression of a functional system for serotonin receptor activation and reuptake. Bone. 2001;29(5):477-86.
• Westbroek I, van der Plas A, de Rooij KE, Klein-Nulend J, Nijweide PJ. Expression of serotonin receptors in bone. J Biol Chem. 2001;276(31):28961-8.
• Battaglino R, Fu J, Späte U, Ersoy U, Joe M, Sedaghat L, et al. Serotonin regulates osteoclast differentiation through its transporter. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 2004;19(9):1420-31.
• Bliziotes M, Eshleman A, Burt-Pichat B, Zhang XW, Hashimoto J, Wiren K, et al. Serotonin transporter and receptor expression in osteocytic MLO-Y4 cells. Bone. 2006;39(6):1313-21.
• Gustafsson BI, Thommesen L, Stunes AK, Tommeras K, Westbroek I, Waldum HL, et al. Serotonin and fluoxetine modulate bone cell function in vitro. Journal of cellular biochemistry. 2006;98(1):139-51.
• Yadav VK, Ryu JH, Suda N, Tanaka KF, Gingrich JA, Schütz G, et al. Lrp5 controls bone formation by inhibiting serotonin synthesis in the duodenum. Cell. 2008;135(5):825-37.,
• Collet C, Schiltz C, Geoffroy V, Maroteaux L, Launay JM, de Vernejoul MC. The serotonin 5-HT2B receptor controls bone mass via osteoblast recruitment and proliferation. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2008;22(2):418-27.
• Murphy DL, Lerner A, Rudnick G, Lesch KP. Serotonin transporter: gene, genetic disorders, and pharmacogenetics. Molecular interventions. 2004;4(2):109-23.
• Wade PR, Chen J, Jaffe B, Kassem IS, Blakely RD, Gershon MD. Localization and function of a 5-HT transporter in crypt epithelia of the gastrointestinal tract. The Journal of neuroscience : the official journal of the Society for Neuroscience. 1996;16(7):2352-64.
• Bliziotes M, Eshleman A, Zhang X, Wiren K, editors. Serotonin potentiates PTH-induced collagenase-3 activity in osteoblasts and stimulates adenylyl cyclase activity in osteocytes. JOURNAL OF BONE AND MINERAL RESEARCH; 2002: AMER SOC BONE & MINERAL RES 2025 M ST, NW, STE 800, WASHINGTON, DC 20036 ….
• Mann JJ. Role of the serotonergic system in the pathogenesis of major depression and suicidal behavior. Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology. 1999;21(2 Suppl):99s-105s.
• Stockmeier CA. Involvement of serotonin in depression: evidence from postmortem and imaging studies of serotonin receptors and the serotonin transporter. Journal of psychiatric research. 2003;37(5):357-73.
• Feuer AJ, Demmer RT, Thai A, Vogiatzi MG. Use of selective serotonin reuptake inhibitors and bone mass in adolescents: An NHANES study. Bone. 2015;78:28-33.
• Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, Reginato AM, et al. LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell. 2001;107(4):513-23.
• Rauma PH, Honkanen RJ, Williams LJ, Tuppurainen MT, Kröger HP, Koivumaa-Honkanen H. Effects of antidepressants on postmenopausal bone loss - A5-year longitudinal study from the OSTPRE cohort. Bone. 2016;89:25-31.
• Sheu YH, Lanteigne A, Stürmer T, Pate V, Azrael D, Miller M. SSRI use and risk of fractures among perimenopausal women without mental disorders. Injury prevention : journal of the International Society for Child and Adolescent Injury Prevention. 2015;21(6):397-403.
• Canalis E. Growth factor control of bone mass. Journal of cellular biochemistry. 2009;108(4):769-77.
• Mochizuki H, Hakeda Y, Wakatsuki N, Usui N, Akashi S, Sato T, et al. Insulin-like growth factor-I supports formation and activation of osteoclasts. Endocrinology. 1992;131(3):1075-80.
• Crane JL, Zhao L, Frye JS, Xian L, Qiu T, Cao X. IGF-1 Signaling is Essential for Differentiation of Mesenchymal Stem Cells for Peak Bone Mass. Bone research. 2013;1(2):186-94.
• Amin S, Riggs BL, Melton LJ, 3rd, Achenbach SJ, Atkinson EJ, Khosla S. High serum IGFBP-2 is predictive of increased bone turnover in aging men and women. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 2007;22(6):799-807.
• Yamaguchi T, Kanatani M, Yamauchi M, Kaji H, Sugishita T, Baylink DJ, et al. Serum levels of insulinlike growth factor (IGF); IGF-binding proteins-3, -4, and -5; and their relationships to bone mineral density and the risk of vertebral fractures in postmenopausal women. Calcified tissue international. 2006;78(1):18-24.
• Johansson AG, Lindh E, Blum WF, Kollerup G, Sørensen OH, Ljunghall S. Effects of growth hormone and insulin-like growth factor I in men with idiopathic osteoporosis. The Journal of clinical endocrinology and metabolism. 1996;81(1):44-8.
• Ohlsson C, Mellström D, Carlzon D, Orwoll E, Ljunggren O, Karlsson MK, et al. Older men with low serum IGF-1 have an increased risk of incident fractures: the MrOS Sweden study. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research. 2011;26(4):865-72.
• Liu JM, Zhao HY, Ning G, Chen Y, Zhang LZ, Sun LH, et al. IGF-1 as an early marker for low bone mass or osteoporosis in premenopausal and postmenopausal women. Journal of bone and mineral metabolism. 2008;26(2):159-64.
• Giustina A, Mazziotti G, Canalis E. Growth hormone, insulin-like growth factors, and the skeleton. Endocrine reviews. 2008;29(5):535-59.
• Agha A, Monson JP. Modulation of glucocorticoid metabolism by the growth hormone - IGF-1 axis. Clinical endocrinology. 2007;66(4):459-65.
• Luo JM, Murphy LJ. Dexamethasone inhibits growth hormone induction of insulin-like growth factor-I (IGF-I) messenger ribonucleic acid (mRNA) in hypophysectomized rats and reduces IGF-I mRNA abundance in the intact rat. Endocrinology. 1989;125(1):165-71.
• Bot M, Milaneschi Y, Penninx BW, Drent ML. Plasma insulin-like growth factor I levels are higher in pressive and anxiety disorders, but lower in antidepressant medication users. Psychoneuroendocrinology. 2016;68:148-55.
• Deuschle M, Blum WF, Strasburger CJ, Schweiger U, Weber B, Körner A, et al. Insulin-like growth factor-I (IGF-I) plasma concentrations are increased in depressed patients. Psychoneuroendocrinology. 1997;22(7):493-503.
• Zhao F, Guo L, Wang X, Zhang Y. Correlation of oxidative stress-related biomarkers with postmenopausal osteoporosis: a systematic review and meta-analysis. Archives of osteoporosis. 2021;16(1):4.
• Bai XC, Lu D, Bai J, Zheng H, Ke ZY, Li XM, et al. Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-kappaB. Biochemical and biophysical research communications. 2004;314(1):197-207.
• Lean JM, Davies JT, Fuller K, Jagger CJ, Kirstein B, Partington GA, et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. The Journal of clinical investigation. 2003;112(6):915-23.
• Lean JM, Jagger CJ, Kirstein B, Fuller K, Chambers TJ. Hydrogen peroxide is essential for estrogendeficiency bone loss and osteoclast formation. Endocrinology. 2005;146(2):728-35.
• Kimball JS, Johnson JP, Carlson DA. Oxidative Stress and Osteoporosis. The Journal of bone and joint surgery American volume. 2021;103(15):1451-61.
• Bhatt S, Nagappa AN, Patil CR. Role of oxidative stress in depression. Drug discovery today. 2020;25(7):1270-6.
• Czarny P, Wigner P, Galecki P, Sliwinski T. The interplay between inflammation, oxidative stress, DNA damage, DNA repair and mitochondrial dysfunction in depression. Progress in neuro-psychopharmacology & biological psychiatry. 2018;80(Pt C):309-21.
• Belleau EL, Treadway MT, Pizzagalli DA. The Impact of Stress and Major Depressive Disorder on Hippocampal and Medial Prefrontal Cortex Morphology. Biological psychiatry. 2019;85(6):443-53.
• Michel TM, Frangou S, Thiemeyer D, Camara S, Jecel J, Nara K, et al. Evidence for oxidative stress in the frontal cortex in patients with recurrent depressive disorder--a postmortem study. Psychiatry research. 2007;151(1-2):145-50.
• Michel TM, Thome J, Martin D, Nara K, Zwerina S, Tatschner T, et al. Cu, Zn- and Mn-superoxide dismutase levels in brains of patients with schizophrenic psychosis. Journal of neural transmission (Vienna, Austria : 1996). 2004;111(9):1191-201.
• Michel TM, Camara S, Tatschner T, Frangou S, Sheldrick AJ, Riederer P, et al. Increased xanthine oxidase in the thalamus and putamen in depression. The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry. 2010;11(2 Pt 2):314-20.