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4 - Disrupted Circadian Rhythms, Stress, and Allostatic Load

Published online by Cambridge University Press:  07 October 2023

By
Ilia N. Karatsoreos
Edited by
Laura K. Fonken  and
Randy J. Nelson
Laura K. Fonken
Affiliation:
University of Texas, Austin
Randy J. Nelson
Affiliation:
West Virginia University
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Summary

The brain and body work together to ensure survival. Under typical conditions, the endogenous circadian (daily) clock helps predict regularly occurring events, like the day–night cycle, to build a behavioral and physiological framework that optimizes use of resources while taking advantage of environmental opportunities. On the other hand, the stress system responds to emergencies, deploying countermeasures that promote survival in the face of threat. When the stress system is engaged inappropriately or for too long, factors that help promote adaptation (allostatic mediators) can cause damage to the biological systems they are meant to protect. This allostatic load can lead to allostatic overload, where a cascading set of failures in these systems lead to pathology. Here, I discuss the interplay between the stress and circadian systems, how disruption of the circadian clock can contribute to allostatic load and overload, and the negative health consequences that this can cause.

Keywords

metabolismimmuneadaptationsleep
Type
Chapter
Information
Biological Implications of Circadian Disruption
A Modern Health Challenge
 , pp. 84 - 99
Publisher: Cambridge University Press
Print publication year: 2023

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References

Agorastos, A., Nicolaides, N. C., Bozikas, V. P., Chrousos, G. P., & Pervanidou, P. (2020). Multilevel interactions of stress and circadian system: Implications for traumatic stress. Front Psychiatry, 10, 1003.Google Scholar
Albers, H. E., Yogev, L., Todd, R. B., & Goldman, B. D. (1985). Adrenal corticoids in hamsters: Role in circadian timing. Am J Physiol, 248(4 Pt 2), R434–R438.Google Scholar
Amir, S., Lamont, E. W., Robinson, B., & Stewart, J. (2004). A circadian rhythm in the expression of PERIOD2 protein reveals a novel SCN-controlled oscillator in the oval nucleus of the bed nucleus of the stria terminalis. J Neurosci, 24(4), 781–790.Google Scholar
Aronsson, M., Fuxe, K., Dong, Y., Agnati, L. F., Okret, S., & Gustafsson, J. A. (1988). Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. Proc Nat Acad Sci USA, 85(23), 9331–9335.Google Scholar
Balsalobre, A., Brown, S. A., Marcacci, L., Tronche, F., Kellendonk, C., Reichardt, H. M., Schutz, G., & Schibler, U. (2000). Resetting of circadian time in peripheral tissues by glucocorticoid signaling. Science, 289(5488), 2344–2347.Google Scholar
Bedrosian, T. A., Vaughn, C. A., Galan, A., Daye, G., Weil, Z. M., & Nelson, R. J. (2013). Nocturnal light exposure impairs affective responses in a wavelength-dependent manner. J Neurosci, 33(32), 13081–13087.CrossRefGoogle Scholar
Buijs, R. M., Hermes, M. H., & Kalsbeek, A. (1998). The suprachiasmatic nucleus-paraventricular nucleus interactions: A bridge to the neuroendocrine and autonomic nervous system. Prog Brain Res, 119, 365–382.Google Scholar
Buijs, R. M., Wortel, J., Van Heerikhuize, J. J., Feenstra, M. G., Ter Horst, G. J., Romijn, H. J., et al. (1999). Anatomical and functional demonstration of a multisynaptic suprachiasmatic nucleus adrenal (cortex) pathway. Eur J Neurosci, 11(5), 1535–1544.Google Scholar
Carroll, R. G., Timmons, G. A., Cervantes-Silva, M. P., Kennedy, O. D., & Curtis, A. M. (2019). Immunometabolism around the clock. Trends Molec Med, 25(7), 612–625.Google Scholar
Casiraghi, L. P., Alzamendi, A., Giovambattista, A., Chiesa, J. J., & Golombek, D. A. (2016). Effects of chronic forced circadian desynchronization on body weight and metabolism in male mice. Physiol Rep, 4(8), e12743.Google Scholar
Castanon-Cervantes, O., Wu, M., Ehlen, J. C., Paul, K., Gamble, K. L., Johnson, R. L., Besing, R. C., Menaker, M., Gewirtz, A. T., & Davidson, A. J. (2010). Dysregulation of inflammatory responses by chronic circadian disruption. J Immunol, 185(10), 5796–5805.Google Scholar
Cavadini, G., Petrzilka, S., Kohler, P., Jud, C., Tobler, I., Birchler, T., & Fontana, A. (2007). TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc Nat Acad Sci USA, 104(31), 12843–12848.Google Scholar
Chen, S., Fuller, K. K., Dunlap, J. C., & Loros, J. J. (2020). A pro- and anti-inflammatory axis modulates the macrophage circadian clock. Front Immunol, 11, 867.Google Scholar
Chrobok, L., Klich, J. D., Jeczmien-Lazur, J. S., Pradel, K., Palus-Chramiec, K., Sanetra, A. M., Piggins, H. D., & Lewandowski, M. H. (2022). Daily changes in neuronal activities of the dorsal motor nucleus of the vagus under standard and high-fat diet. J Physiol, 600(4), 733–749.CrossRefGoogle ScholarPubMed
Cohen, H., Kozlovsky, N., Savion, N., Matar, M. A., Loewenthal, U., Loewenthal, N., Zohar, J., & Kaplan, Z. (2009). An association between stress-induced disruption of the hypothalamic–pituitary–adrenal axis and disordered glucose metabolism in an animal model of post-traumatic stress disorder. J Neuroendocrinol, 21(11), 898–909.Google Scholar
Curtis, A. M., Bellet, M. M., Sassone-Corsi, P., & O’Neill, L. A. J. (2014). Circadian clock proteins and immunity. Immunity, 40(2), 178–186.Google Scholar
Davidson, A. J., Sellix, M. T., Daniel, J., Yamazaki, S., Menaker, M., & Block, G. D. (2006). Chronic jet-lag increases mortality in aged mice. Curr Biol, 16(21), R914–R916.Google Scholar
Dhabhar, F. S. (2009). Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation, 16(5), 300–317.Google Scholar
Dhabhar, F. S. (2014). Effects of stress on immune function: The good, the bad, and the beautiful. Immunol Res, 58(2–3), 193–210.Google Scholar
Díaz-Morales, J. F., & Escribano, C. (2015). Social jetlag, academic achievement and cognitive performance: Understanding gender/sex differences. Chronobiol Int, 32(6), 822–831.Google Scholar
Fonken, L. K., Weil, Z. M., & Nelson, R. J. (2013). Mice exposed to dim light at night exaggerate inflammatory responses to lipopolysaccharide. Brain Behav Immun, 34, 159–163.Google Scholar
Fonken, L. K., Workman, J. L., Walton, J. C., Weil, Z. M., Morris, J. S., Haim, A., & Nelson, R. J. (2010). Light at night increases body mass by shifting the time of food intake. Proc Natl Acad Sci USA, 107(43), 18664–18669.Google Scholar
Gibson, E. M., Wang, C., Tjho, S., Khattar, N., & Kriegsfeld, L. J. (2010). Experimental “jet lag” inhibits adult neurogenesis and produces long-term cognitive deficits in female hamsters. PLoS One, 5(12), e15267.CrossRefGoogle ScholarPubMed
Girtman, K. L., Baylin, A., O’Brien, L. M., & Jansen, E. C. (2022). Later sleep timing and social jetlag are related to increased inflammation in a population with a high proportion of OSA: Findings from the Cleveland Family Study. J Clin Sleep Med, 18(9), 2179–2187.Google Scholar
Guo, B., Yang, N., Borysiewicz, E., Dudek, M., Williams, J. L., Li, J., Maywood, E. S., Adamson, A., Hastings, M. H., Bateman, J. F., White, M. R. H., Boot-Handford, R. P., & Meng, Q. J. (2015). Catabolic cytokines disrupt the circadian clock and the expression of clock-controlled genes in cartilage via an NFкB-dependent pathway. Osteoarthritis Cartilage, 23(11), 1981–1988.Google Scholar
Hampp, G., Ripperger, J. A., Houben, T., Schmutz, I., Blex, C., Perreau-Lenz, S., Brunk, I., Spanagel, R., Ahnert-Hilger, G., Meijer, J. H., & Albrecht, U. (2008). Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol, 18(9), 678–683.Google Scholar
Haraszti, R. Á., Ella, K., Gyöngyösi, N., Roenneberg, T., & Káldi, K. (2014). Social jetlag negatively correlates with academic performance in undergraduates. Chronobiol Int, 31(5), 603–612.Google Scholar
Hastings, M. H., Reddy, A. B., & Maywood, E. S. (2003). A clockwork web: Circadian timing in brain and periphery, in health and disease. Nat Rev Neurosci, 4(8), 649–661.Google Scholar
Hay-Schmidt, A., Vrang, N., Larsen, P. J., & Mikkelsen, J. D. (2003). Projections from the raphe nuclei to the suprachiasmatic nucleus of the rat. J Chem Neuroanat, 25(4), 293–310.Google Scholar
Herman, J. P., McKlveen, J. M., Ghosal, S., Kopp, B., Wulsin, A., Makinson, R., Scheimann, J., & Myers, B. (2016). Regulation of the hypothalamic-pituitary-adrenocortical stress response. Compr Physiol, 6(2), 603–621.Google Scholar
Herman, J. P., Nawreen, N., Smail, M. A., & Cotella, E. M. (2020). Brain mechanisms of HPA axis regulation: Neurocircuitry and feedback in context Richard Kvetnansky lecture. Stress, 23(6), 617–632.Google Scholar
Karatsoreos, I. N., Bhagat, S., Bloss, E. B., Morrison, J. H., & McEwen, B. S. (2011). Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc Natl Acad Sci USA, 108(4), 1657–1662.Google Scholar
Karatsoreos, I. N., & McEwen, B. S. (2011). Psychobiological allostasis: Resistance, resilience and vulnerability. Trends Cogn Sci, 15(12), 576–584.CrossRefGoogle ScholarPubMed
Kinlein, S. A., & Karatsoreos, I. N. (2020). The hypothalamic-pituitary-adrenal axis as a substrate for stress resilience: Interactions with the circadian clock. Front Neuroendocrinol, 56, 100819.Google Scholar
Kong, X., Ota, S. M., Suchecki, D., Lan, A., Peereboom, A. I., Hut, R. A., & Meerlo, P. (2022). Chronic social defeat stress shifts peripheral circadian clocks in male mice in a tissue-specific and time-of-day dependent fashion. J Biol Rhythms, 37(2), 164–176.Google Scholar
Koopman, A. D. M., Rauh, S. P., van’t Riet, E., Groeneveld, L., van der Heijden, A. A., Elders, P. J., Dekker, J. M., Nijpels, G., Beulens, J. W., & Rutters, F. (2017). The association between social jetlag, the metabolic syndrome, and type 2 diabetes mellitus in the general population: The new Hoorn study. J Biol Rhythms, 32(4), 359–368.Google Scholar
Koronowski, K. B., Kinouchi, K., Welz, P.-S., Smith, J. G., Zinna, V. M., Shi, J., Samad, M., Chen, S., Magnan, C. N., Kinchen, J. M., Li, W., Baldi, P., Benitah, S. A., & Sassone-Corsi, P. (2019). Defining the independence of the liver circadian clock. Cell, 177(6), 1448–1462.e14.Google Scholar
Kwak, Y., Lundkvist, G. B., Brask, J., Davidson, A., Menaker, M., Kristensson, K., & Block, G. D. (2008). Interferon-gamma alters electrical activity and clock gene expression in suprachiasmatic nucleus neurons. J Biol Rhythms, 23(2), 150–159.Google Scholar
Lamia, K. A., Storch, K. F., & Weitz, C. J. (2008). Physiological significance of a peripheral tissue circadian clock. Proc Natl Acad Sci USA, 105(39), 15172–15177.Google Scholar
Lamont, E. W., Robinson, B., Stewart, J., & Amir, S. (2005). The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc Natl Acad Sci USA, 102(11), 4180–4184.Google Scholar
Lamotte, G., Shouman, K., & Benarroch, E. E. (2021). Stress and central autonomic network. Auton Neurosci, 235, 102870.Google Scholar
Lang, V., Ferencik, S., Ananthasubramaniam, B., Kramer, A., & Maier, B. (2021). Susceptibility rhythm to bacterial endotoxin in myeloid clock-knockout mice. ELife, 10, e62469.Google Scholar
Leach, G., Adidharma, W., & Yan, L. (2013). Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). PLoS One, 8(2), e57115.Google Scholar
Lightman, S. L., Birnie, M. T., & Conway-Campbell, B. L. (2020). Dynamics of ACTH and cortisol secretion and implications for disease. Endocr Rev, 41(3), 470–490.Google Scholar
Lightman, S. L., & Conway-Campbell, B. L. (2010). The crucial role of pulsatile activity of the HPA axis for continuous dynamic equilibration. Nature Rev Neurosci, 11(10), 710–718.Google Scholar
Loh, D. H., Navarro, J., Hagopian, A., Wang, L. M., Deboer, T., & Colwell, C. S. (2010). Rapid changes in the light/dark cycle disrupt memory of conditioned fear in mice. PLoS One, 5(9), e12546.Google Scholar
Marcheva, B., Ramsey, K. M., Buhr, E. D., Kobayashi, Y., Su, H., Ko, C. H., Ivanova, G., Omura, C., Mo, S., Vitaterna, M. H., Lopez, J. P., Philipson, L. H., Bradfield, C. A., Crosby, S. D., JeBailey, L., Wang, X., Takahashi, J. S., & Bass, J. (2010). Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature, 466(7306), 627–631.Google Scholar
McCosh, R. B., Breen, K. M., & Kauffman, A. S. (2019). Neural and endocrine mechanisms underlying stress-induced suppression of pulsatile LH secretion. Mol Cell Endocrinol, 498, 110579.Google Scholar
McEwen, B. S. (1998). Stress, adaptation, and disease. Allostasis and allostatic load. Ann NY Acad Sci, 840, 33–44.Google Scholar
McEwen, B. S. (2017). Neurobiological and systemic effects of chronic stress. Chronic Stress (Thousand Oaks), 1, 2470547017692328.Google Scholar
McEwen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Horm Behav, 43(1), 2–15.Google Scholar
Mereness, A. L., Murphy, Z. C., Forrestel, A. C., Butler, S., Ko, C., Richards, J. S., & Sellix, M. T. (2016). Conditional deletion of Bmal1 in ovarian theca cells disrupts ovulation in female mice. Endocrinology, 157(2), 913–927.Google Scholar
Meyer-Bernstein, E. L., Jetton, A. E., Matsumoto, S. I., Markuns, J. F., Lehman, M. N., & Bittman, E. L. (1999). Effects of suprachiasmatic transplants on circadian rhythms of neuroendocrine function in golden hamsters. Endocrinology, 140(1), 207–218.Google Scholar
Moore, R. Y., & Eichler, V. B. (1972). Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res, 42(1), 201–206.CrossRefGoogle ScholarPubMed
Oster, H. (2020). The interplay between stress, circadian clocks, and energy metabolism. J Endocrinol, 247(1), R13–R25.Google Scholar
Ota, S. M., Hut, R. A., Riede, S. J., Crosby, P., Suchecki, D., & Meerlo, P. (2020). Social stress and glucocorticoids alter PERIOD2 rhythmicity in the liver, but not in the suprachiasmatic nucleus. Horm Behav, 120, 104683.Google Scholar
Ota, S. M., Kong, X., Hut, R., Suchecki, D., & Meerlo, P. (2021). The impact of stress and stress hormones on endogenous clocks and circadian rhythms. Front Neuroendocrinol, 63, 100931.Google Scholar
Ottenweller, J. E., Tapp, W. N., Pitman, D. L., & Natelson, B. H. (1987). Adrenal, thyroid, and testicular hormone rhythms in male golden hamsters on long and short days. Am J Physiol, 253(2 Pt 2), R321–R328.Google Scholar
Parsons, M. J., Moffitt, T. E., Gregory, A. M., Goldman-Mellor, S., Nolan, P. M., Poulton, R., & Caspi, A. (2015). Social jetlag, obesity and metabolic disorder: Investigation in a cohort study. Int J Obes (Lond), 39(5), 842–848.Google Scholar
Pearson, G. L., Savenkova, M., Barnwell, J. J., & Karatsoreos, I. N. (2020). Circadian desynchronization alters metabolic and immune responses following lipopolysaccharide inoculation in male mice. Brain Behav Immun, 88, 220–229.Google Scholar
Petrzilka, S., Taraborrelli, C., Cavadini, G., Fontana, A., & Birchler, T. (2009). Clock gene modulation by TNF-alpha depends on calcium and p38 MAP kinase signaling. J Biol Rhythms, 24(4), 283–294.Google Scholar
Phillips, D. J., Savenkova, M. I., & Karatsoreos, I. N. (2015). Environmental disruption of the circadian clock leads to altered sleep and immune responses in mouse. Brain Behav Immun, 47, 14–23.Google Scholar
Reddy, T. E., Gertz, J., Crawford, G. E., Garabedian, M. J., & Myers, R. M. (2012). The hypersensitive glucocorticoid response specifically regulates period 1 and expression of circadian genes. Mol Cell Biol, 32(18), 3756–3767.Google Scholar
Roenneberg, T., Allebrandt, K. V., Merrow, M., & Vetter, C. (2012). Social jetlag and obesity. Curr Biol, 22(10), 939–943.Google Scholar
Roenneberg, T., Winnebeck, E. C., & Klerman, E. B. (2019). Daylight saving time and artificial time zones: A battle between biological and social times. Front Physiol, 10, 944.Google Scholar
Russell, G. M., Kalafatakis, K., & Lightman, S. L. (2015). The importance of biological oscillators for hypothalamic-pituitary-adrenal activity and tissue glucocorticoid response: Coordinating stress and neurobehavioural adaptation. J Neuroendocrinol, 27(6), 378–388.Google Scholar
Sanford, L. D., Suchecki, D., & Meerlo, P. (2015). Stress, arousal, and sleep. Curr Topics Behav Neurosci, 25, 379–410.Google Scholar
Schroder, E. A., Harfmann, B. D., Zhang, X., Srikuea, R., England, J. H., Hodge, B. A., Wen, Y., Riley, L. A., Yu, Q., Christie, A., Smith, J. D., Seward, T., Wolf Horrell, E. M., Mula, J., Peterson, C. A., Butterfield, T. A., & Esser, K. A. (2015). Intrinsic muscle clock is necessary for musculoskeletal health. J Physiol, 593(24), 5387–5404.CrossRefGoogle ScholarPubMed
Sinha, R. (2008). Chronic stress, drug use, and vulnerability to addiction. Ann NY Acad Sci, 1141, 105–130.Google Scholar
Skinner, N. J., Rizwan, M. Z., Grattan, D. R., & Tups, A. (2019). Chronic light cycle disruption alters central insulin and leptin signaling as well as metabolic markers in male mice. Endocrinology, 160(10), 2257–2270.Google Scholar
So, A. Y.-L., Bernal, T. U., Pillsbury, M. L., Yamamoto, K. R., & Feldman, B. J. (2009). Glucocorticoid regulation of the circadian clock modulates glucose homeostasis. Proc Natl Acad Sci USA, 106(41), 17582–17587.Google Scholar
Stephan, F. K., & Zucker, I. (1972). Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA, 69(6), 1583–1586.Google Scholar
Sutton, C. E., Finlay, C. M., Raverdeau, M., Early, J. O., DeCourcey, J., Zaslona, Z., O’Neill, L. A. J., Mills, K. H. G., & Curtis, A. M. (2017). Loss of the molecular clock in myeloid cells exacerbates T cell-mediated CNS autoimmune disease. Nature Commun, 8(1), 1923.Google Scholar
Tahara, Y., Shiraishi, T., Kikuchi, Y., Haraguchi, A., Kuriki, D., Sasaki, H., Motohashi, H., Sakai, T., & Shibata, S. (2015). Entrainment of the mouse circadian clock by sub-acute physical and psychological stress. Sci Rep, 5, 11417.Google Scholar
Torra, I. P., Tsibulsky, V., Delaunay, F., Saladin, R., Laudet, V., Fruchart, J.-C., Kosykh, V., & Staels, B. (2000). Circadian and glucocorticoid regulation of Rev-erbα expression in liver. Endocrinology, 141(10), 3799–3806.Google Scholar
Toufexis, D., Rivarola, M. A., Lara, H., & Viau, V. (2014). Stress and the reproductive axis. J Neuroendocrinol, 26(9), 573–586.Google Scholar
Tsai, L. L., Tsai, Y. C., Hwang, K., Huang, Y. W., & Tzeng, J. E. (2005). Repeated light–dark shifts speed up body weight gain in male F344 rats. Am J Physiol Endocrinol Metab, 289(2), E212–E217.Google Scholar
Turek, F. W., Joshu, C., Kohsaka, A., Lin, E., Ivanova, G., McDearmon, E., Laposky, A., Losee-Olson, S., Easton, A., Jensen, D. R., Eckel, R. H., Takahashi, J. S., & Bass, J. (2005). Obesity and metabolic syndrome in circadian clock mutant mice. Science, 308(5724), 1043–1045.Google Scholar
Vieira, E., Mirizio, G. G., & Barin, G. R. (2020). Clock genes, inflammation and the immune system: Implications for diabetes, obesity and neurodegenerative diseases. Int J Mol Sci, 21(24), 9743.Google Scholar
Vrang, N., Larsen, P. J., & Mikkelsen, J. D. (1995a). Direct projection from the suprachiasmatic nucleus to hypophysiotrophic corticotropin-releasing factor immunoreactive cells in the paraventricular nucleus of the hypothalamus demonstrated by means of Phaseolus vulgaris-leucoagglutinin tract tracing. Brain Res, 684(1), 61–69.Google Scholar
Vrang, N., Larsen, P. J., Moller, M., & Mikkelsen, J. D. (1995b). Topographical organization of the rat suprachiasmatic-paraventricular projection. J Comp Neurol, 353(4), 585–603.Google Scholar
Weil, Z. M., Fonken, L. K., Walker, W. H., Bumgarner, J. R., Liu, J. A., Melendez-Fernandez, O. H., Zhang, N., DeVries, A. C., & Nelson, R. J. (2020). Dim light at night exacerbates stroke outcome. Eur J Neurosci, 52(9), 4139–4146.Google Scholar
Wittmann, M., Dinich, J., Merrow, M., & Roenneberg, T. (2006). Social jetlag: Misalignment of biological and social time. Chronobiol Int, 23(1–2), 497–509.Google Scholar
Wong, C. C., Dohler, K. D., Geerlings, H., & von zur Muhlen, A. (1983). Influence of age, strain and season on circadian periodicity of pituitary, gonadal and adrenal hormones in the serum of male laboratory rats. Horm Res, 17(4), 202–215.Google Scholar
Woodruff, E. R., Chun, L. E., Hinds, L. R., Varra, N. M., Tirado, D., Morton, S. J., McClung, C. A., & Spencer, R. L. (2018). Coordination between prefrontal cortex clock gene expression and corticosterone contributes to enhanced conditioned fear extinction recall. ENeuro, 5(6), e0455-18.2018 1-13.Google Scholar
Zerbini, G., van der Vinne, V., Otto, L. K. M., Kantermann, T., Krijnen, W. P., Roenneberg, T., & Merrow, M. (2017). Lower school performance in late chronotypes: Underlying factors and mechanisms. Sci Rep, 7(1), 4385.Google Scholar

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