Progress in the study of sleep and circadian rhythm disturbances in Huntington’s disease_West China Medical Journal

Authors：

TIAN Yuan , OU Ruwei ,  SHANG Huifang

Department of Neurology, West China Hospital, Sichuan University, Chengdu, Sichuan 610041, P. R. China;

Corresponding author：

SHANG Huifang, Email: hfshang2002@163.com

Keywords：

Huntington’s disease; Sleep disturbances; Circadian rhythm disturbances; Suprachiasmatic nucleus

DOI：

10.7507/1002-0179.201904199

Video：

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Huntington’s disease (HD) is characterized by chorea, cognitive impairment, and psychiatric symptoms. Sleep and circadian rhythm disturbances are one of the important symptoms of HD that have been gradually recognized in recent years, and have a serious impact on the quality of life of patients and their caregivers. The clinical manifestations of sleep and circadian rhythm disturbances in HD are different from those of other neurodegenerative diseases. The exact pathological mechanisms of these disturbances remain unclear and there is no specific treatment. This article reviews the current progress in the study of sleep and circadian rhythm disturbances in HD, including its pathological mechanisms, clinical manifestations, assessment methods, correlation with cognitive impairment and psychiatric symptoms, treatment and management.

Citation： TIAN Yuan, OU Ruwei, SHANG Huifang. Progress in the study of sleep and circadian rhythm disturbances in Huntington’s disease. West China Medical Journal, 2019, 34(10): 1179-1183. doi: 10.7507/1002-0179.201904199 Copy

1.	The Huntington’s Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell, 1993, 72(6): 971-983.
2.	Bates GP, Dorsey R, Gusella JF, et al. Huntington disease. Nat Rev Dis Primers, 2015, 1: 15005.
3.	Bruzelius E, Scarpa J, Zhao Y, et al. Huntington’s disease in the United States: variation by demographic and socioeconomic factors. Mov Disord, 2019, 34(6): 858-865.
4.	McColgan P, Tabrizi SJ. Huntington’s disease: a clinical review. Eur J Neurol, 2018, 25(1): 24-34.
5.	Lazar AS, Panin F, Goodman AO, et al. Sleep deficits but no metabolic deficits in premanifest Huntington’s disease. Ann Neurol, 2015, 78(4): 630-648.
6.	Goodman AO, Morton AJ, Barker RA. Identifying sleep disturbances in Huntington’s disease using a simple disease-focused questionnaire. PLoS Curr, 2010, 2: RRN1189.
7.	Goodman AO, Rogers L, Pilsworth S, et al. Asymptomatic sleep abnormalities are a common early feature in patients with Huntington’s disease. Curr Neurol Neurosci Rep, 2011, 11(2): 211-217.
8.	Brzezinski A. Melatonin in humans. N Engl J Med, 1997, 336(3): 186-195.
9.	Bragantini D, Sivertsen B, Gehrman P, et al. Variations in circadian genes and individual nocturnal symptoms of insomnia.The HUNT study. Chronobiol Int, 2019, 36(5): 681-688.
10.	Vitaterna MH, Shimomura K, Jiang P. Genetics of Circadian Rhythms. Neurol Clin, 2019, 37(3): 487-504.
11.	Zisapel N. New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation. Br J Pharmacol, 2018, 175(16): 3190-3199.
12.	Kräuchi K, Cajochen C, Werth E, et al. Functional link between distal vasodilation and sleep-onset latency?. Am J Physiol Regul Integr Comp Physiol, 2000, 278(3): R741-R748.
13.	Ciarochi JA, Johnson HJ, Calhoun VD, et al. Concurrent cross-sectional and longitudinal analyses of multivariate white matter profiles and clinical functioning in pre-diagnosis Huntington disease. J Huntingtons Dis, 2019, 8(2): 199-219.
14.	Hansotia P, Wall R, Berendes J. Sleep disturbances and severity of Huntington’s disease. Neurology, 1985, 35(11): 1672-1674.
15.	Soneson C, Fontes M, Zhou Y, et al. Early changes in the hypothalamic region in prodromal Huntington disease revealed by MRI analysis. Neurobiol Dis, 2010, 40(3): 531-543.
16.	Cuturic M, Abramson RK, Vallini D, et al. Sleep patterns in patients with Huntington’s disease and their unaffected first-degree relatives: a brief report. Behav Sleep Med, 2009, 7(4): 245-254.
17.	Mena-Segovia J, Cintra L, Prospéro-García O, et al. Changes in sleep-waking cycle after striatal excitotoxic lesions. Behav Brain Res, 2002, 136(2): 475-481.
18.	Politis M, Pavese N, Tai YF, et al. Hypothalamic involvement in Huntington’s disease: an in vivo PET study. Brain, 2008, 131(Pt 11): 2860-2869.
19.	Roos RA, Aziz NA. Hypocretin-1 and secondary signs in Huntington’s disease. Parkinsonism Relat Disord, 2007, 13(Suppl 3): S387-S390.
20.	Aron AR, Schlaghecken F, Fletcher PC, et al. Inhibition of subliminally primed responses is mediated by the caudate and thalamus: evidence from functional MRI and Huntington’s disease. Brain, 2003, 126(Pt 3): 713-723.
21.	van Wamelen DJ, Shan L, Aziz NA, et al. Functional increase of brain histaminergic signaling in Huntington’s disease. Brain Pathol, 2011, 21(4): 419-427.
22.	Goodman AO, Barker RA. How vital is sleep in Huntington’s disease?. J Neurol, 2010, 257(6): 882-897.
23.	Aziz NA, Pijl H, Frölich M, et al. Delayed onset of the diurnal melatonin rise in patients with Huntington’s disease. J Neurol, 2009, 256(12): 1961-1965.
24.	Kalliolia E, Silajdžić E, Nambron R, et al. Plasma melatonin is reduced in Huntington’s disease. Mov Disord, 2014, 29(12): 1511-1515.
25.	Adamczak-Ratajczak A, Kupsz J, Owecki M, et al. Circadian rhythms of melatonin and cortisol in manifest Huntington’s disease and in acute cortical ischemic stroke. J Physiol Pharmacol, 2017, 68(4): 539-546.
26.	Kurtis MM, Balestrino R, Rodriguez-Blazquez C, et al. A review of scales to evaluate sleep disturbances in movement disorders. Front Neurol, 2018, 9: 369.
27.	Piano C, Della Marca G, Losurdo A, et al. Subjective assessment of sleep in Huntington disease: reliability of sleep questionnaires compared to polysomnography. Neurodegener Dis, 2017, 17(6): 330-337.
28.	Marinus J, Visser M, van Hilten JJ, et al. Assessment of sleep and sleepiness in Parkinson disease. Sleep, 2003, 26(8): 1049-1054.
29.	Orr WC. Utilization of polysomnography in the assessment of sleep disorders. Med Clin North Am, 1985, 69(6): 1153-1167.
30.	Tahmasian M, Khazaie H, Sepehry AA, et al. Ambulatory monitoring of sleep disorders. J Pak Med Assoc, 2010, 60(6): 480-487.
31.	Baillet M, Cosin C, Schweitzer P, et al. Mood influences the concordance of subjective and objective measures of sleep duration in older adults. Front Aging Neurosci, 2016, 8: 181.
32.	Kaplan KA, Talbot LS, Gruber J, et al. Evaluating sleep in bipolar disorder: comparison between actigraphy, polysomnography, and sleep diary. Bipolar Disord, 2012, 14(8): 870-879.
33.	Mundt JM, Crew EC, Krietsch K, et al. Measuring treatment outcomes in comorbid insomnia and fibromyalgia: concordance of subjective and objective assessments. J Clin Sleep Med, 2016, 12(2): 215-223.
34.	Townhill J, Hughes AC, Thomas B, et al. Using actiwatch to monitor circadian rhythm disturbance in Huntington’ disease: a cautionary note. J Neurosci Methods, 2016, 265: 13-18.
35.	Sitek EJ, Thompson JC, Craufurd D, et al. Unawareness of deficits in Huntington’s disease. J Huntingtons Dis, 2014, 3(2): 125-135.
36.	Aziz NA, Anguelova GV, Marinus J, et al. Sleep and circadian rhythm alterations correlate with depression and cognitive impairment in Huntington’s disease. Parkinsonism Relat Disord, 2010, 16(5): 345-350.
37.	Silvestri R, Raffaele M, De Domenico P, et al. Sleep features in Tourette’s syndrome, neuroacanthocytosis and Huntington’s chorea. Neurophysiol Clin, 1995, 25(2): 66-77.
38.	Wiegand, M, Möller A, Lauer, C, et al. Nocturnal sleep in Huntington’s disease. J Neurol, 1991, 238(4): 203-208.
39.	Wiegand M, Möller AA, Schreiber W, et al. Brain morphology and sleep EEG in patients with Huntington’s disease. Eur Arch Psychiatry Clin Neurosci, 1991, 240(3): 148-152.
40.	Videnovic A, Leurgans S, Fan W, et al. Daytime somnolence and nocturnal sleep disturbances in Huntington disease. Parkinsonism Relat Disord, 2009, 15(6): 471-474.
41.	Piano C, Losurdo A, Della Marca G, et al. Polysomnographic findings and clinical correlates in Huntington disease: a cross-sectional cohort study. Sleep, 2015, 38(9): 1489-1495.
42.	Nance MA, Westphal B, Nugent S. Diagnosis of patients presenting to a Huntington disease (HD) clinic without a family history of HD. Neurology, 1996, 47(6): 1578-1580.
43.	Neutel D, Tchikviladzé M, Charles P, et al. Nocturnal agitation in Huntington disease is caused by arousal-related abnormal movements rather than by rapid eye movement sleep behavior disorder. Sleep Med, 2015, 16(6): 754-759.
44.	Arnulf I, Nielsen J, Lohmann E, et al. Rapid eye movement sleep disturbances in Huntington disease. Arch Neurol, 2008, 65(4): 482-488.
45.	André VM, Cepeda C, Levine MS. Dopamine and glutamate in Huntington’s disease: a balancing act. CNS Neurosci Ther, 2010, 16(3): 163-178.
46.	Thu DC, Oorschot DE, Tippett LJ, et al. Cell loss in the motor and cingulate cortex correlates with symptomatology in Huntington’s disease. Brain, 2010, 133(Pt 4): 1094-1110.
47.	Kyriacou CP, Hastings MH. Circadian clocks: genes, sleep, and cognition. Trends Cogn Sci, 2010, 14(6): 259-267.
48.	Peigneux P, Laureys S, Fuchs S, et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron, 2004, 44(3): 535-545.
49.	Ghilardi MF, Silvestri G, Feigin A, et al. Implicit and explicit aspects of sequence learning in pre-symptomatic Huntington’s disease. Parkinsonism Relat Disord, 2008, 14(6): 457-464.
50.	Baker CR, Domínguez D JF, Stout JC, et al. Subjective sleep problems in Huntington’s disease: a pilot investigation of the relationship to brain structure, neurocognitive, and neuropsychiatric function. J Neurol Sci, 2016, 364: 148-153.
51.	Barbanoj MJ, Clos S, Romero S, et al. Sleep laboratory study on single and repeated dose effects of paroxetine, alprazolam and their combination in healthy young volunteers. Neuropsychobiology, 2005, 51(3): 134-147.
52.	Mason SL, Barker RA. Advancing pharmacotherapy for treating Huntington’s disease: a review of the existing literature. Expert Opin Pharmacother, 2016, 17(1): 41-52.
53.	Pallier PN, Maywood ES, Zheng Z, et al. Pharmacological imposition of sleep slows cognitive decline and reverses dysregulation of circadian gene expression in a transgenic mouse model of Huntington’s disease. J Neurosci, 2007, 27(29): 7869-7878.
54.	Schiefer J. Compensation in the course of Huntington’s disease - more than just a hypothesis?. EBioMedicine, 2015, 2(10): 1286-1287.
55.	van Wamelen DJ, Aziz NA, Anink JJ, et al. Suprachiasmatic nucleus neuropeptide expression in patients with Huntington’s disease. Sleep, 2013, 36(1): 117-125.
56.	Hattar S, Lucas RJ, Mrosovsky N, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature, 2003, 424(6944): 76-81.
57.	Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science, 2002, 295(5557): 1070-1073.
58.	Cuesta M, Aungier J, Morton AJ. Behavioral therapy reverses circadian deficits in a transgenic mouse model of Huntington’s disease. Neurobiol Dis, 2014, 63: 85-91.
59.	Whittaker DS, Loh DH, Wang HB, et al. Circadian-based treatment strategy effective in the BACHD mouse model of Huntington’s disease. J Biol Rhythms, 2018, 33(5): 535-554.
60.	Wang HB, Loh DH, Whittaker DS, et al. Time-restricted feeding improves circadian dysfunction as well as motor symptoms in the Q175 mouse model of Huntington’s disease. eNeuro, 2018, 5(1).

1. The Huntington’s Disease Collaborative Research Group. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell, 1993, 72(6): 971-983.
2. Bates GP, Dorsey R, Gusella JF, et al. Huntington disease. Nat Rev Dis Primers, 2015, 1: 15005.
3. Bruzelius E, Scarpa J, Zhao Y, et al. Huntington’s disease in the United States: variation by demographic and socioeconomic factors. Mov Disord, 2019, 34(6): 858-865.
4. McColgan P, Tabrizi SJ. Huntington’s disease: a clinical review. Eur J Neurol, 2018, 25(1): 24-34.
5. Lazar AS, Panin F, Goodman AO, et al. Sleep deficits but no metabolic deficits in premanifest Huntington’s disease. Ann Neurol, 2015, 78(4): 630-648.
6. Goodman AO, Morton AJ, Barker RA. Identifying sleep disturbances in Huntington’s disease using a simple disease-focused questionnaire. PLoS Curr, 2010, 2: RRN1189.
7. Goodman AO, Rogers L, Pilsworth S, et al. Asymptomatic sleep abnormalities are a common early feature in patients with Huntington’s disease. Curr Neurol Neurosci Rep, 2011, 11(2): 211-217.
8. Brzezinski A. Melatonin in humans. N Engl J Med, 1997, 336(3): 186-195.
9. Bragantini D, Sivertsen B, Gehrman P, et al. Variations in circadian genes and individual nocturnal symptoms of insomnia.The HUNT study. Chronobiol Int, 2019, 36(5): 681-688.
10. Vitaterna MH, Shimomura K, Jiang P. Genetics of Circadian Rhythms. Neurol Clin, 2019, 37(3): 487-504.
11. Zisapel N. New perspectives on the role of melatonin in human sleep, circadian rhythms and their regulation. Br J Pharmacol, 2018, 175(16): 3190-3199.
12. Kräuchi K, Cajochen C, Werth E, et al. Functional link between distal vasodilation and sleep-onset latency?. Am J Physiol Regul Integr Comp Physiol, 2000, 278(3): R741-R748.
13. Ciarochi JA, Johnson HJ, Calhoun VD, et al. Concurrent cross-sectional and longitudinal analyses of multivariate white matter profiles and clinical functioning in pre-diagnosis Huntington disease. J Huntingtons Dis, 2019, 8(2): 199-219.
14. Hansotia P, Wall R, Berendes J. Sleep disturbances and severity of Huntington’s disease. Neurology, 1985, 35(11): 1672-1674.
15. Soneson C, Fontes M, Zhou Y, et al. Early changes in the hypothalamic region in prodromal Huntington disease revealed by MRI analysis. Neurobiol Dis, 2010, 40(3): 531-543.
16. Cuturic M, Abramson RK, Vallini D, et al. Sleep patterns in patients with Huntington’s disease and their unaffected first-degree relatives: a brief report. Behav Sleep Med, 2009, 7(4): 245-254.
17. Mena-Segovia J, Cintra L, Prospéro-García O, et al. Changes in sleep-waking cycle after striatal excitotoxic lesions. Behav Brain Res, 2002, 136(2): 475-481.
18. Politis M, Pavese N, Tai YF, et al. Hypothalamic involvement in Huntington’s disease: an in vivo PET study. Brain, 2008, 131(Pt 11): 2860-2869.
19. Roos RA, Aziz NA. Hypocretin-1 and secondary signs in Huntington’s disease. Parkinsonism Relat Disord, 2007, 13(Suppl 3): S387-S390.
20. Aron AR, Schlaghecken F, Fletcher PC, et al. Inhibition of subliminally primed responses is mediated by the caudate and thalamus: evidence from functional MRI and Huntington’s disease. Brain, 2003, 126(Pt 3): 713-723.
21. van Wamelen DJ, Shan L, Aziz NA, et al. Functional increase of brain histaminergic signaling in Huntington’s disease. Brain Pathol, 2011, 21(4): 419-427.
22. Goodman AO, Barker RA. How vital is sleep in Huntington’s disease?. J Neurol, 2010, 257(6): 882-897.
23. Aziz NA, Pijl H, Frölich M, et al. Delayed onset of the diurnal melatonin rise in patients with Huntington’s disease. J Neurol, 2009, 256(12): 1961-1965.
24. Kalliolia E, Silajdžić E, Nambron R, et al. Plasma melatonin is reduced in Huntington’s disease. Mov Disord, 2014, 29(12): 1511-1515.
25. Adamczak-Ratajczak A, Kupsz J, Owecki M, et al. Circadian rhythms of melatonin and cortisol in manifest Huntington’s disease and in acute cortical ischemic stroke. J Physiol Pharmacol, 2017, 68(4): 539-546.
26. Kurtis MM, Balestrino R, Rodriguez-Blazquez C, et al. A review of scales to evaluate sleep disturbances in movement disorders. Front Neurol, 2018, 9: 369.
27. Piano C, Della Marca G, Losurdo A, et al. Subjective assessment of sleep in Huntington disease: reliability of sleep questionnaires compared to polysomnography. Neurodegener Dis, 2017, 17(6): 330-337.
28. Marinus J, Visser M, van Hilten JJ, et al. Assessment of sleep and sleepiness in Parkinson disease. Sleep, 2003, 26(8): 1049-1054.
29. Orr WC. Utilization of polysomnography in the assessment of sleep disorders. Med Clin North Am, 1985, 69(6): 1153-1167.
30. Tahmasian M, Khazaie H, Sepehry AA, et al. Ambulatory monitoring of sleep disorders. J Pak Med Assoc, 2010, 60(6): 480-487.
31. Baillet M, Cosin C, Schweitzer P, et al. Mood influences the concordance of subjective and objective measures of sleep duration in older adults. Front Aging Neurosci, 2016, 8: 181.
32. Kaplan KA, Talbot LS, Gruber J, et al. Evaluating sleep in bipolar disorder: comparison between actigraphy, polysomnography, and sleep diary. Bipolar Disord, 2012, 14(8): 870-879.
33. Mundt JM, Crew EC, Krietsch K, et al. Measuring treatment outcomes in comorbid insomnia and fibromyalgia: concordance of subjective and objective assessments. J Clin Sleep Med, 2016, 12(2): 215-223.
34. Townhill J, Hughes AC, Thomas B, et al. Using actiwatch to monitor circadian rhythm disturbance in Huntington’ disease: a cautionary note. J Neurosci Methods, 2016, 265: 13-18.
35. Sitek EJ, Thompson JC, Craufurd D, et al. Unawareness of deficits in Huntington’s disease. J Huntingtons Dis, 2014, 3(2): 125-135.
36. Aziz NA, Anguelova GV, Marinus J, et al. Sleep and circadian rhythm alterations correlate with depression and cognitive impairment in Huntington’s disease. Parkinsonism Relat Disord, 2010, 16(5): 345-350.
37. Silvestri R, Raffaele M, De Domenico P, et al. Sleep features in Tourette’s syndrome, neuroacanthocytosis and Huntington’s chorea. Neurophysiol Clin, 1995, 25(2): 66-77.
38. Wiegand, M, Möller A, Lauer, C, et al. Nocturnal sleep in Huntington’s disease. J Neurol, 1991, 238(4): 203-208.
39. Wiegand M, Möller AA, Schreiber W, et al. Brain morphology and sleep EEG in patients with Huntington’s disease. Eur Arch Psychiatry Clin Neurosci, 1991, 240(3): 148-152.
40. Videnovic A, Leurgans S, Fan W, et al. Daytime somnolence and nocturnal sleep disturbances in Huntington disease. Parkinsonism Relat Disord, 2009, 15(6): 471-474.
41. Piano C, Losurdo A, Della Marca G, et al. Polysomnographic findings and clinical correlates in Huntington disease: a cross-sectional cohort study. Sleep, 2015, 38(9): 1489-1495.
42. Nance MA, Westphal B, Nugent S. Diagnosis of patients presenting to a Huntington disease (HD) clinic without a family history of HD. Neurology, 1996, 47(6): 1578-1580.
43. Neutel D, Tchikviladzé M, Charles P, et al. Nocturnal agitation in Huntington disease is caused by arousal-related abnormal movements rather than by rapid eye movement sleep behavior disorder. Sleep Med, 2015, 16(6): 754-759.
44. Arnulf I, Nielsen J, Lohmann E, et al. Rapid eye movement sleep disturbances in Huntington disease. Arch Neurol, 2008, 65(4): 482-488.
45. André VM, Cepeda C, Levine MS. Dopamine and glutamate in Huntington’s disease: a balancing act. CNS Neurosci Ther, 2010, 16(3): 163-178.
46. Thu DC, Oorschot DE, Tippett LJ, et al. Cell loss in the motor and cingulate cortex correlates with symptomatology in Huntington’s disease. Brain, 2010, 133(Pt 4): 1094-1110.
47. Kyriacou CP, Hastings MH. Circadian clocks: genes, sleep, and cognition. Trends Cogn Sci, 2010, 14(6): 259-267.
48. Peigneux P, Laureys S, Fuchs S, et al. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron, 2004, 44(3): 535-545.
49. Ghilardi MF, Silvestri G, Feigin A, et al. Implicit and explicit aspects of sequence learning in pre-symptomatic Huntington’s disease. Parkinsonism Relat Disord, 2008, 14(6): 457-464.
50. Baker CR, Domínguez D JF, Stout JC, et al. Subjective sleep problems in Huntington’s disease: a pilot investigation of the relationship to brain structure, neurocognitive, and neuropsychiatric function. J Neurol Sci, 2016, 364: 148-153.
51. Barbanoj MJ, Clos S, Romero S, et al. Sleep laboratory study on single and repeated dose effects of paroxetine, alprazolam and their combination in healthy young volunteers. Neuropsychobiology, 2005, 51(3): 134-147.
52. Mason SL, Barker RA. Advancing pharmacotherapy for treating Huntington’s disease: a review of the existing literature. Expert Opin Pharmacother, 2016, 17(1): 41-52.
53. Pallier PN, Maywood ES, Zheng Z, et al. Pharmacological imposition of sleep slows cognitive decline and reverses dysregulation of circadian gene expression in a transgenic mouse model of Huntington’s disease. J Neurosci, 2007, 27(29): 7869-7878.
54. Schiefer J. Compensation in the course of Huntington’s disease - more than just a hypothesis?. EBioMedicine, 2015, 2(10): 1286-1287.
55. van Wamelen DJ, Aziz NA, Anink JJ, et al. Suprachiasmatic nucleus neuropeptide expression in patients with Huntington’s disease. Sleep, 2013, 36(1): 117-125.
56. Hattar S, Lucas RJ, Mrosovsky N, et al. Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice. Nature, 2003, 424(6944): 76-81.
57. Berson DM, Dunn FA, Takao M. Phototransduction by retinal ganglion cells that set the circadian clock. Science, 2002, 295(5557): 1070-1073.
58. Cuesta M, Aungier J, Morton AJ. Behavioral therapy reverses circadian deficits in a transgenic mouse model of Huntington’s disease. Neurobiol Dis, 2014, 63: 85-91.
59. Whittaker DS, Loh DH, Wang HB, et al. Circadian-based treatment strategy effective in the BACHD mouse model of Huntington’s disease. J Biol Rhythms, 2018, 33(5): 535-554.
60. Wang HB, Loh DH, Whittaker DS, et al. Time-restricted feeding improves circadian dysfunction as well as motor symptoms in the Q175 mouse model of Huntington’s disease. eNeuro, 2018, 5(1).

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