Differences in executive functions applied to memory processes in people with migraine: a cross-sectional study
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may 18, 2017
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Resumen
The aim of this cross-sectional study was to identify differences in memory processes and the role of executive functions in memory, in people with migraine and in a control group. Neuropsychological evaluation was made in one session on 63 participants distributed into interictal migraine-with-aura (n = 24), interictal migraine-without-aura (n = 16) and control (n = 23) groups. ANOVAs on the individual tasks revealed statistically significant differences between groups on Rey-Osterrieth direct and percentile copy strategy and recall (both p < 0.001). Differences were identified between control and migraine groups in performance on the Rey-Osterrieth Complex Figure, but not on other memory tasks, suggesting the existence of brain dysfunctions in people with migraine affecting organizational and planning abilities that are necessary for visual memory.
Keywords
Aura, funciones ejecutivas, memoria, migrañaAura, executive functions, memory, migraine
References
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Borsook, D., Maleki, N., & Burstein, R. (2015). Migraine. In M. J. Zigmond, J. T. Coyle, & L. Rowland (Eds.), Neurobiology of Brain Disorders (pp. 693-708). San Diego: Academic Press.
Bussone, G. (2004). Pathophysiology of migraine. Neurol Sci, 25 Suppl 3, S239-241. doi:10.1007/s10072-004-0295-3
Calandre, E. P., Bembibre, J., Arnedo, M. L., & Becerra, D. (2002). Cognitive disturbances and regional cerebral blood flow abnormalities in migraine patients: their relationship with the clinical manifestations of the illness. Cephalalgia, 22(4), 291-302.
Camarda, C., Monastero, R., Pipia, C., Recca, D., & Camarda, R. (2007). Interictal executive dysfunction in migraineurs without aura: relationship with duration and intensity of attacks. Cephalalgia, 27(10), 1094-110. doi:10.1111/j.1468-2982.20070.01394.x
Clerici, F., Ghiretti, R., Di Pucchio, A., Pomati, S., Cucumo, V., Marcone, A., Cappa, S. F. (2015). Construct validity of the Free and Cued Selective Reminding Test in older adults with memory complaints. J Neuropsychol. doi:10.1111/jnp.12087
Coppola, G., Di Renzo, A., Tinelli, E., Iacovelli, E., Lepre, C., Di Lorenzo, C., Pierelli, F. (2015). Evidence for brain morphometric changes during the migraine cycle: a magnetic resonance-based morphometry study. Cephalalgia, 35(9), 783-791. doi:10.1177/0333102414559732
Duncan, J., Burgess, P., & Emslie, H. (1995). Fluid intelligence after frontal lobe lesions. Neuropsychologia, 33(3), 261-268.
Faria, V., Erpelding, N., Lebel, A., Johnson, A., Wolff, R., Fair, D., Borsook, D. (2015). The migraine brain in transition: girls vs boys. Pain, 156(11), 2212-2221. doi:10.1097/j.pain0.0000000000000292
Finocchi, C., & Strada, L. (2014). Sex-related differences in migraine. Neurol Sci, 35 Suppl 1, 207-213. doi:10.1007/s10072-014-1772-y
Friedman, N. P., Miyake, A., Corley, R. P., Young, S. E., Defries, J. C., & Hewitt, J. K. (2006). Not all executive functions are related to intelligence. Psychol Sci, 17(2), 172-179. doi:10.1111/j.1467-9280.20060.01681.x
Gaist, D., Pedersen, L., Madsen, C., Tsiropoulos, I., Bak, S., Sindrup, S., Christensen, K. (2005). Long-term effects of migraine on cognitive function: a population-based study of Danish twins. Neurology, 64(4), 600-607. doi:10.1212/01.WNL0.0000151858.15482.66
Garcia-Herranz, S., Diaz-Mardomingo, M. C., & Peraita, H. (2014). Evaluation and follow-up of healthy aging and aging with mild cognitive impairment (MCI) through TAVEC. Anales De Psicologia, 30(1), 373-380. doi:10.6018/analesps.30.1.150711
Gil-Gouveia, R., Oliveira, A. G., & Martins, I. P. (2015a). Assessment of cognitive dysfunction during migraine attacks: a systematic review. J Neurol, 262(3), 654-665. doi:10.1007/s00415-014-7603-5
Gil-Gouveia, R., Oliveira, A. G., & Martins, I. P. (2015b). Sequential brief neuropsychological evaluation of migraineurs is identical to controls. Acta Neurol Scand. doi:10.1111/ane.12530
Harmon, T. P. (2015). Diagnosis and management of migraines and migraine variants. Prim Care, 42(2), 233-241. doi:10.1016/j.pop.20150.010.003
Horn, J. L., & Cattell, R. B. (1966). Refinement and test of the theory of fluid and crystallized general intelligences. J Educ Psychol, 57(5), 253-270.
Kececi, H., & Atakay, S. (2009). Effects of topiramate on neurophysiological and neuropsychological tests in migraine patients. Journal of Clinical Neuroscience, 16(12), 1588-1591.
Koppen, H., Palm-Meinders, I., Kruit, M., Lim, V., Nugroho, A., Westhof, I., Hommel, B. (2011). The impact of a migraine attack and its after-effects on perceptual organization, attention, and working memory. Cephalalgia, 31(14), 1419-1427. doi:10.1177/0333102411417900
Le Pira, F., Reggio, E., Quattrocchi, G., Sanfilippo, C., Maci, T., Cavallaro, T., & Zappia, M. (2014). Executive dysfunctions in migraine with and without aura: what is the role of white matter lesions? Headache, 54(1), 125-130. doi:10.1111/head.12158
Le Pira, F., Zappalà, G., Giuffrida, S., Lo Bartolo, M. L., Reggio, E., Morana, R., & Lanaia, F. (2000). Memory disturbances in migraine with and without aura: a strategy problem? Cephalalgia, 20(5), 475-478.
Lemos, R., Simoes, M. R., Santiago, B., & Santana, I. (2015). The free and cued selective reminding test: Validation for mild cognitive impairment and Alzheimer's disease. Journal of Neuropsychology, 9(2), 242-257. doi:10.1111/jnp.12048
Liu, J., Zhao, L., Lei, F., Zhang, Y., Yuan, K., Gong, Q., Tian, J. (2015). Disrupted resting-state functional connectivity and its changing trend in migraine suffers. Hum Brain Mapp, 36(5), 1892-1907. doi:10.1002/hbm.22744
Maleki, N., Linnman, C., Brawn, J., Burstein, R., Becerra, L., & Borsook, D. (2012). Her versus his migraine: multiple sex differences in brain function and structure. Brain, 135(Pt 8), 2546-2559. doi:10.1093/brain/aws175
Mathur, V. A., Khan, S. A., Keaser, M. L., Hubbard, C. S., Goyal, M., & Seminowicz, D. A. (2015). Altered cognition-related brain activity and interactions with acute pain in migraine. Neuroimage Clin, 7, 347-358. doi:10.1016/j.nicl.20150.010.003
Moutran, A. R., Villa, T. R., Diaz, L. A., Noffs, M. H., Pinto, M. M., Gabbai, A. A., & Carvalho, D. e. S. (2011). Migraine and cognition in children: a controlled study. Arq Neuropsiquiatr, 69(2A), 192-195.
Mulder, E. J., Linssen, W. H., Passchier, J., Orlebeke, J. F., & de Geus, E. J. (1999). Interictal and postictal cognitive changes in migraine. Cephalalgia, 19(6), 557-565; discussion 541.
Nakano, K., Ogino, T., Watanabe, K., Hattori, J., Ito, M., Oka, M., & Ohtsuka, Y. (2006). A developmental study of scores of the Boston Qualitative Scoring System. Brain Dev, 28(10), 641-648. doi:10.1016/j.braindev.20060.040.011
Nieto, A., Hernandez-Rodriguez, E., Hernandez-Torres, A., Velasco Rodriguez-Solis, P., Hess-Medler, S., Machado-Fernandez, A., . . . Barroso, J. (2014). Alternate form of the test de aprendizaje verbal Espana-Complutense (TAVEC). Revista De Neurologia, 58(9), 389-395.
Ogino, T., Watanabe, K., Nakano, K., Kado, Y., Morooka, T., Takeuchi, A., Ohtuska, Y. (2009). Predicting executive function task scores with the Rey-Osterrieth Complex Figure. Brain and Development, 31(1), 52 - 57.
Paemeleire, K. (2009). Brain lesions and cerebral functional impairment in migraine patients. J Neurol Sci, 283(1-2), 134-136. doi:10.1016/j.jns.20090.02.333
Pearson, A. J., Chronicle, E. P., Maylor, E. A., & Bruce, L. A. (2006). Cognitive function is not impaired in people with a long history of migraine: a blinded study. Cephalalgia, 26(1), 74-80. doi:10.1111/j.1468-2982.20050.01001.x
Peña-Casanova, J., Gramunt-Fombuena, N., Quinones-Ubeda, S., Sanchez-Benavides, G., Aguilar, M., Badenes, D., Team, N. S. (2009). Spanish Multicenter Normative Studies (NEURONORMA Project): Norms for the Rey-Osterrieth Complex Figure (Copy and Memory), and Free and Cued Selective Reminding Test. Archives of Clinical Neuropsychology, 24(4), 371-393. doi:10.1093/arclin/acp041
Ravishankar, N., & Demakis, G. J. (2007). The neuropsychology of migraine. Dis Mon, 53(3), 156-161. doi:10.1016/j.disamonth.20070.040.006
Rist, P. M., Kang, J. H., Buring, J. E., Glymour, M. M., Grodstein, F., & Kurth, T. (2012). Migraine and cognitive decline among women: prospective cohort study. BMJ, 345, e5027.
Rist, P. M., & Kurth, T. (2013). Migraine and cognitive decline: a topical review. Headache, 53(4), 589-598. doi:10.1111/head.12046
Santamarta, E., Meilán, A., Saiz, A., Larrosa, D., Cernuda-Morollón, E., Calleja, S., Pascual, J. (2014). Chronic migraine does not increase posterior circulation territory (PCT) infarct-like lesions. J Neurol Sci, 336(1-2), 180-183. doi:10.1016/j.jns.2013.10.035
Sas, K., Párdutz, A., Toldi, J., & Vécsei, L. (2010). Dementia, stroke and migraine--some common pathological mechanisms. J Neurol Sci, 299(1-2), 55-65. doi:10.1016/j.jns.2010.080.001
Schmitz, N., Arkink, E. B., Mulder, M., Rubia, K., Admiraal-Behloul, F., Schoonman, G. G., van Buchem, M. A. (2008). Frontal lobe structure and executive function in migraine patients. Neurosci Lett, 440(2), 92-96. doi:10.1016/j.neulet.20080.050.033
Suhr, J. A., & Seng, E. K. (2012). Neuropsychological functioning in migraine: clinical and research implications. Cephalalgia, 32(1), 39-54. doi:10.1177/0333102411430265
The International classification of Headache disorders. (2013). (3rd edition ed., Vol. 33, pp. 629-808): Cephalalgia.
van Aken, L., Kessels, R. P., Wingbermühle, E., van der Veld, W. M., & Egger, J. I. (2015). Fluid intelligence and executive functioning more alike than different? Acta Neuropsychiatr, 1-7. doi:10.1017/neu.2015.46
Waldie, K. E., Hausmann, M., Milne, B. J., & Poulton, R. (2002). Migraine and cognitive function: a life-course study. Neurology, 59(6), 904-908.
Wang, R., Dong, Z., Chen, X., Zhang, M., Yang, F., Zhang, X., Yu, S. (2014). Gender differences of cognitive function in migraine patients: evidence from event-related potentials using the oddball paradigm. J Headache Pain, 15, 6. doi:10.1186/1129-2377-15-6
Watanabe, K., Ogino, T., Nakano, K., Hattori, J., Kado, Y., Sanada, S., & Ohtsuka, Y. (2005). The Rey–Osterrieth Complex Figure as a measure of executive function in childhood. Brain and Development, 27(8), 564 - 569.
Zimmerman, M. E., Katz, M. J., Wang, C., Burns, L. C., Berman, R. M., Derby, C. A., Lipton, R. B. (2015). Comparison of “Word” vs. “Picture” version of the Free and Cued Selective Reminding Test (FCSRT) in older adults. Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring, 1(1), 94-10. doi: http://dx.doi.org/10.1016/j.dadm.2014.110.006
Öze, A., Nagy, A., Benedek, G., Bodosi, B., Kéri, S., Pálinkás, É., . . . Braunitzer, G. (2016). Acquired equivalence and related memory processes in migraine without aura. Cephalalgia. doi:10.1177/0333102416651286
Borsook, D., Maleki, N., & Burstein, R. (2015). Migraine. In M. J. Zigmond, J. T. Coyle, & L. Rowland (Eds.), Neurobiology of Brain Disorders (pp. 693-708). San Diego: Academic Press.
Bussone, G. (2004). Pathophysiology of migraine. Neurol Sci, 25 Suppl 3, S239-241. doi:10.1007/s10072-004-0295-3
Calandre, E. P., Bembibre, J., Arnedo, M. L., & Becerra, D. (2002). Cognitive disturbances and regional cerebral blood flow abnormalities in migraine patients: their relationship with the clinical manifestations of the illness. Cephalalgia, 22(4), 291-302.
Camarda, C., Monastero, R., Pipia, C., Recca, D., & Camarda, R. (2007). Interictal executive dysfunction in migraineurs without aura: relationship with duration and intensity of attacks. Cephalalgia, 27(10), 1094-110. doi:10.1111/j.1468-2982.20070.01394.x
Clerici, F., Ghiretti, R., Di Pucchio, A., Pomati, S., Cucumo, V., Marcone, A., Cappa, S. F. (2015). Construct validity of the Free and Cued Selective Reminding Test in older adults with memory complaints. J Neuropsychol. doi:10.1111/jnp.12087
Coppola, G., Di Renzo, A., Tinelli, E., Iacovelli, E., Lepre, C., Di Lorenzo, C., Pierelli, F. (2015). Evidence for brain morphometric changes during the migraine cycle: a magnetic resonance-based morphometry study. Cephalalgia, 35(9), 783-791. doi:10.1177/0333102414559732
Duncan, J., Burgess, P., & Emslie, H. (1995). Fluid intelligence after frontal lobe lesions. Neuropsychologia, 33(3), 261-268.
Faria, V., Erpelding, N., Lebel, A., Johnson, A., Wolff, R., Fair, D., Borsook, D. (2015). The migraine brain in transition: girls vs boys. Pain, 156(11), 2212-2221. doi:10.1097/j.pain0.0000000000000292
Finocchi, C., & Strada, L. (2014). Sex-related differences in migraine. Neurol Sci, 35 Suppl 1, 207-213. doi:10.1007/s10072-014-1772-y
Friedman, N. P., Miyake, A., Corley, R. P., Young, S. E., Defries, J. C., & Hewitt, J. K. (2006). Not all executive functions are related to intelligence. Psychol Sci, 17(2), 172-179. doi:10.1111/j.1467-9280.20060.01681.x
Gaist, D., Pedersen, L., Madsen, C., Tsiropoulos, I., Bak, S., Sindrup, S., Christensen, K. (2005). Long-term effects of migraine on cognitive function: a population-based study of Danish twins. Neurology, 64(4), 600-607. doi:10.1212/01.WNL0.0000151858.15482.66
Garcia-Herranz, S., Diaz-Mardomingo, M. C., & Peraita, H. (2014). Evaluation and follow-up of healthy aging and aging with mild cognitive impairment (MCI) through TAVEC. Anales De Psicologia, 30(1), 373-380. doi:10.6018/analesps.30.1.150711
Gil-Gouveia, R., Oliveira, A. G., & Martins, I. P. (2015a). Assessment of cognitive dysfunction during migraine attacks: a systematic review. J Neurol, 262(3), 654-665. doi:10.1007/s00415-014-7603-5
Gil-Gouveia, R., Oliveira, A. G., & Martins, I. P. (2015b). Sequential brief neuropsychological evaluation of migraineurs is identical to controls. Acta Neurol Scand. doi:10.1111/ane.12530
Harmon, T. P. (2015). Diagnosis and management of migraines and migraine variants. Prim Care, 42(2), 233-241. doi:10.1016/j.pop.20150.010.003
Horn, J. L., & Cattell, R. B. (1966). Refinement and test of the theory of fluid and crystallized general intelligences. J Educ Psychol, 57(5), 253-270.
Kececi, H., & Atakay, S. (2009). Effects of topiramate on neurophysiological and neuropsychological tests in migraine patients. Journal of Clinical Neuroscience, 16(12), 1588-1591.
Koppen, H., Palm-Meinders, I., Kruit, M., Lim, V., Nugroho, A., Westhof, I., Hommel, B. (2011). The impact of a migraine attack and its after-effects on perceptual organization, attention, and working memory. Cephalalgia, 31(14), 1419-1427. doi:10.1177/0333102411417900
Le Pira, F., Reggio, E., Quattrocchi, G., Sanfilippo, C., Maci, T., Cavallaro, T., & Zappia, M. (2014). Executive dysfunctions in migraine with and without aura: what is the role of white matter lesions? Headache, 54(1), 125-130. doi:10.1111/head.12158
Le Pira, F., Zappalà, G., Giuffrida, S., Lo Bartolo, M. L., Reggio, E., Morana, R., & Lanaia, F. (2000). Memory disturbances in migraine with and without aura: a strategy problem? Cephalalgia, 20(5), 475-478.
Lemos, R., Simoes, M. R., Santiago, B., & Santana, I. (2015). The free and cued selective reminding test: Validation for mild cognitive impairment and Alzheimer's disease. Journal of Neuropsychology, 9(2), 242-257. doi:10.1111/jnp.12048
Liu, J., Zhao, L., Lei, F., Zhang, Y., Yuan, K., Gong, Q., Tian, J. (2015). Disrupted resting-state functional connectivity and its changing trend in migraine suffers. Hum Brain Mapp, 36(5), 1892-1907. doi:10.1002/hbm.22744
Maleki, N., Linnman, C., Brawn, J., Burstein, R., Becerra, L., & Borsook, D. (2012). Her versus his migraine: multiple sex differences in brain function and structure. Brain, 135(Pt 8), 2546-2559. doi:10.1093/brain/aws175
Mathur, V. A., Khan, S. A., Keaser, M. L., Hubbard, C. S., Goyal, M., & Seminowicz, D. A. (2015). Altered cognition-related brain activity and interactions with acute pain in migraine. Neuroimage Clin, 7, 347-358. doi:10.1016/j.nicl.20150.010.003
Moutran, A. R., Villa, T. R., Diaz, L. A., Noffs, M. H., Pinto, M. M., Gabbai, A. A., & Carvalho, D. e. S. (2011). Migraine and cognition in children: a controlled study. Arq Neuropsiquiatr, 69(2A), 192-195.
Mulder, E. J., Linssen, W. H., Passchier, J., Orlebeke, J. F., & de Geus, E. J. (1999). Interictal and postictal cognitive changes in migraine. Cephalalgia, 19(6), 557-565; discussion 541.
Nakano, K., Ogino, T., Watanabe, K., Hattori, J., Ito, M., Oka, M., & Ohtsuka, Y. (2006). A developmental study of scores of the Boston Qualitative Scoring System. Brain Dev, 28(10), 641-648. doi:10.1016/j.braindev.20060.040.011
Nieto, A., Hernandez-Rodriguez, E., Hernandez-Torres, A., Velasco Rodriguez-Solis, P., Hess-Medler, S., Machado-Fernandez, A., . . . Barroso, J. (2014). Alternate form of the test de aprendizaje verbal Espana-Complutense (TAVEC). Revista De Neurologia, 58(9), 389-395.
Ogino, T., Watanabe, K., Nakano, K., Kado, Y., Morooka, T., Takeuchi, A., Ohtuska, Y. (2009). Predicting executive function task scores with the Rey-Osterrieth Complex Figure. Brain and Development, 31(1), 52 - 57.
Paemeleire, K. (2009). Brain lesions and cerebral functional impairment in migraine patients. J Neurol Sci, 283(1-2), 134-136. doi:10.1016/j.jns.20090.02.333
Pearson, A. J., Chronicle, E. P., Maylor, E. A., & Bruce, L. A. (2006). Cognitive function is not impaired in people with a long history of migraine: a blinded study. Cephalalgia, 26(1), 74-80. doi:10.1111/j.1468-2982.20050.01001.x
Peña-Casanova, J., Gramunt-Fombuena, N., Quinones-Ubeda, S., Sanchez-Benavides, G., Aguilar, M., Badenes, D., Team, N. S. (2009). Spanish Multicenter Normative Studies (NEURONORMA Project): Norms for the Rey-Osterrieth Complex Figure (Copy and Memory), and Free and Cued Selective Reminding Test. Archives of Clinical Neuropsychology, 24(4), 371-393. doi:10.1093/arclin/acp041
Ravishankar, N., & Demakis, G. J. (2007). The neuropsychology of migraine. Dis Mon, 53(3), 156-161. doi:10.1016/j.disamonth.20070.040.006
Rist, P. M., Kang, J. H., Buring, J. E., Glymour, M. M., Grodstein, F., & Kurth, T. (2012). Migraine and cognitive decline among women: prospective cohort study. BMJ, 345, e5027.
Rist, P. M., & Kurth, T. (2013). Migraine and cognitive decline: a topical review. Headache, 53(4), 589-598. doi:10.1111/head.12046
Santamarta, E., Meilán, A., Saiz, A., Larrosa, D., Cernuda-Morollón, E., Calleja, S., Pascual, J. (2014). Chronic migraine does not increase posterior circulation territory (PCT) infarct-like lesions. J Neurol Sci, 336(1-2), 180-183. doi:10.1016/j.jns.2013.10.035
Sas, K., Párdutz, A., Toldi, J., & Vécsei, L. (2010). Dementia, stroke and migraine--some common pathological mechanisms. J Neurol Sci, 299(1-2), 55-65. doi:10.1016/j.jns.2010.080.001
Schmitz, N., Arkink, E. B., Mulder, M., Rubia, K., Admiraal-Behloul, F., Schoonman, G. G., van Buchem, M. A. (2008). Frontal lobe structure and executive function in migraine patients. Neurosci Lett, 440(2), 92-96. doi:10.1016/j.neulet.20080.050.033
Suhr, J. A., & Seng, E. K. (2012). Neuropsychological functioning in migraine: clinical and research implications. Cephalalgia, 32(1), 39-54. doi:10.1177/0333102411430265
The International classification of Headache disorders. (2013). (3rd edition ed., Vol. 33, pp. 629-808): Cephalalgia.
van Aken, L., Kessels, R. P., Wingbermühle, E., van der Veld, W. M., & Egger, J. I. (2015). Fluid intelligence and executive functioning more alike than different? Acta Neuropsychiatr, 1-7. doi:10.1017/neu.2015.46
Waldie, K. E., Hausmann, M., Milne, B. J., & Poulton, R. (2002). Migraine and cognitive function: a life-course study. Neurology, 59(6), 904-908.
Wang, R., Dong, Z., Chen, X., Zhang, M., Yang, F., Zhang, X., Yu, S. (2014). Gender differences of cognitive function in migraine patients: evidence from event-related potentials using the oddball paradigm. J Headache Pain, 15, 6. doi:10.1186/1129-2377-15-6
Watanabe, K., Ogino, T., Nakano, K., Hattori, J., Kado, Y., Sanada, S., & Ohtsuka, Y. (2005). The Rey–Osterrieth Complex Figure as a measure of executive function in childhood. Brain and Development, 27(8), 564 - 569.
Zimmerman, M. E., Katz, M. J., Wang, C., Burns, L. C., Berman, R. M., Derby, C. A., Lipton, R. B. (2015). Comparison of “Word” vs. “Picture” version of the Free and Cued Selective Reminding Test (FCSRT) in older adults. Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring, 1(1), 94-10. doi: http://dx.doi.org/10.1016/j.dadm.2014.110.006
Öze, A., Nagy, A., Benedek, G., Bodosi, B., Kéri, S., Pálinkás, É., . . . Braunitzer, G. (2016). Acquired equivalence and related memory processes in migraine without aura. Cephalalgia. doi:10.1177/0333102416651286
Cómo citar
Quiroz Padilla, M. F., Pitta, P., Lombana-Angel, L., Ingram, G., Gómez, C., & Restrepo, J. A. (2017). Differences in executive functions applied to memory processes in people with migraine: a cross-sectional study. Universitas Psychologica, 15(5). https://doi.org/10.11144/Javeriana.upsy15-5.defa
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