Changes in the rest-activity rhythm in migraine patients are associated with anxiety symptoms

David, Mírian C.M.M.; Mattos, Marina S.B.; Souto, Jandirlly J.S.; Brito, Sarah A.C.F.; Leite, Etcheverry S.; Valença, Eduardo N.; Galdino, Gilma S.; Sampaio, Patrick G.G.; Moura, Daniel M.C.; Miguel, Mário A.L.; Araújo, John F.; Franco, Carlúcia I.F.; Matos, Rhowena J.B.

doi:10.47626/1516-4446-2021-2367

Mírian C.M.M. David

Programa de Pós-Graduação em Neuropsiquiatria e Ciências do Comportamento (Posneuro), Universidade Federal de Pernambuco (UFPE), Recife, PE, Brazil

https://orcid.org/0000-0002-7152-8852

Marina S.B. Mattos

Departamento de Fisioterapia, Universidade Estadual da Paraíba (UEPB), Campina Grande, PB, Brazil

https://orcid.org/0000-0002-4445-0754

Jandirlly J.S. Souto

Programa de Pós-Graduação em Psicologia Social, Universidade Federal da Paraíba (UFPB), João Pessoa, PB, Brazil

https://orcid.org/0000-0003-1746-332X

Sarah A.C.F. Brito

Departamento de Fisioterapia, Universidade Estadual da Paraíba (UEPB), Campina Grande, PB, Brazil

Etcheverry S. Leite

Departamento de Fisioterapia, Universidade Estadual da Paraíba (UEPB), Campina Grande, PB, Brazil

Eduardo N. Valença

Departamento de Educação Física, UEPB, Campina Grande, PB, Brazil

Gilma S. Galdino

Departamento de Fisioterapia, Universidade Estadual da Paraíba (UEPB), Campina Grande, PB, Brazil

https://orcid.org/0000-0001-8644-5251

Patrick G.G. Sampaio

Faculdade de Ciências Médicas de Campina Grande (FCM-CG), Centro Universitário UNIFACISA, Campina Grande, PB, Brazil

https://orcid.org/0000-0003-0952-9798

Daniel M.C. Moura

Faculdade de Ciências Médicas de Campina Grande (FCM-CG), Centro Universitário UNIFACISA, Campina Grande, PB, Brazil

Mário A.L. Miguel

Departamento de Fisiologia, Universidade Federal do Rio Grande do Norte (UFRN), Natal, RN, Brazil

https://orcid.org/0000-0002-7248-3529

John F. Araújo

Departamento de Fisiologia, Universidade Federal do Rio Grande do Norte (UFRN), Natal, RN, Brazil

https://orcid.org/0000-0002-8022-2425

Carlúcia I.F. Franco

Departamento de Fisioterapia, Universidade Estadual da Paraíba (UEPB), Campina Grande, PB, Brazil

https://orcid.org/0000-0001-6653-8864

Rhowena J.B. Matos Correspondence: Rhowena Jane Barbosa de Matos, Centro de Ciências da Saúde, Universidade Federal do Recôncavo da Bahia (UFRB), Av. Carlos Amaral, 1015, Cajueiro, CEP 44574-490, Santo Antônio de Jesus, BA, Brazil. E-mail: rhowena.matos@ufrb.edu.br

Programa de Pós-Graduação em Neuropsiquiatria e Ciências do Comportamento (Posneuro), Universidade Federal de Pernambuco (UFPE), Recife, PE, Brazil

Centro de Ciências da Saúde, Universidade Federal do Recôncavo da Bahia (UFRB), Santo Antônio de Jesus, BA, Brazil

https://orcid.org/0000-0001-5914-7304

Correspondence: Rhowena Jane Barbosa de Matos, Centro de Ciências da Saúde, Universidade Federal do Recôncavo da Bahia (UFRB), Av. Carlos Amaral, 1015, Cajueiro, CEP 44574-490, Santo Antônio de Jesus, BA, Brazil. E-mail: rhowena.matos@ufrb.edu.br

Disclosure The authors report no conflicts of interest.

How to cite this article: David MCMM, Mattos MSB, Souto JJS, Brito SACF, Leite ES, Valença EN, et al. Changes in the rest-activity rhythm in migraine patients are associated with anxiety symptoms. Braz J Psychiatry. 2022;00:000-000. http://doi.org/10.47626/1516-4446-2021-2367

Variables	Concept	Interpretation
Cosinor method²⁵25. Nelson W, Tong YL, Lee JK, Halberg F. Methods for cosinor-rhythmometry. Chronobiologia. 1979;6:305-23.
MESOR	Mean estimated statistic over rhythm.	Higher values indicate greater activity.
Amplitude	Difference between the highest value and the MESOR.	Higher values indicate greater activity.
Acrophase	Highest phase point.	The higher the value, the later the individual has his/her peak activity.
Rhythmic percentage (V%)	The degree of fit of the rest-activity rhythm to the cosine curve. In other words, it is the proportion of the overall variance accounted for by the fitted model.	The higher the value, the more rhythmic the individual.
Nonparametric method²⁶26. Gonçalves BSB, Adamowicz T, Louzada FM, Moreno CR, Araujo JF. A fresh look at the use of nonparametric analysis in actimetry. Sleep Med Rev. 2015;20:84-91.
L₅	Average activity of the 5 continuous least active hours.	Higher values indicate agitation during sleep.
M₁₀	Average activity of the 10 continuous most active hours.	The higher the value, the more active the individual during wakefulness.
RA	The difference between M10 and L5, divided by the sum of M10 and L5.	Higher values indicate a greater discrepancy in the intensity of activity between the periods of wakefulness and sleep, representing a more expressive rhythm.
IS	Stability of the rhythm over days.	The higher the values, the more stable the rhythm across the days.
IV	A proxy of fragmentation of the rhythm.	The higher the value, the more fragmented the rhythm.
Other variables²⁷27. Ortiz-Tudela E, Martinez-Nicolas A, Campos M, Rol MA, Madrid JA. A new integrated variable based on thermometry, actimetry and body position (TAP) to evaluate circadian system status in humans. PLoS Comput Biol. 2010;6:e1000996. 28. Phillips AJK, Clerx WM, O’Brien CS, Sano A, Barger LK, Picard RW, et al. Irregular sleep/wake patterns are associated with poorer academic performance and delayed circadian and sleep/wake timing. Sci Rep. 2017;7:3216.-²⁹29. Lim ASP, Yu L, Costa MD, Buchman AS, Bennett DA, Leurgans SE, et al. Quantification of the fragmentation of rest-activity patterns in elderly individuals using a state transition analysis. Sleep. 2011;34:1569-81.
AUC_Activity	Area under the curve of the amount of activity over 24 hours.	Higher values indicate greater activity over 24 hours.
% AUC_4h	Amount of activity 4 hours before sleep onset. This parameter is associated to difficulties in sleep onset (i.e., increased sleep latency).	Higher values indicate greater agitation before sleep, that is, greater difficulty falling asleep.
% AUC_Sleep	The amount of activity between sleep onset and offset, i.e., the amount of activity during sleep.	Higher values indicate agitation during sleep.
CVAON	Variation in time to awakening.	Higher values indicate that individuals wake up at different times throughout the days.
CVAOF	Variation in time to fall asleep.	Higher values indicate that individuals fall asleep at different times throughout the days.
CFI	Overall measure to assess the robustness of the rest-activity rhythm. CFI incorporates three parameters: IV, IS and RA.	Higher values indicate a more robust rhythm, i.e., the higher, the better the rest-activity rhythm.
SRI	Regularity of sleeping and waking times throughout the days.	Higher values indicate that the individual sleeps and wakes up at the same times throughout the days.
fSoD	Fractional volume of epochs identified as sleep over daytime, using Cole-Kripke sleep-wake scoring algorithm.	Higher values indicate greater presence of sleep during the day.
Transition probability to awake once in sustained sleep (k_RA)	Used to quantify the probability to transition from a rest state to an active state. This provides a quantification of the sleep fragmentation.	The higher the value, the greater the possibility of waking up from sleep (i.e., sleep fragmentation).

Variables	Mean (SD)	Minimum	Median	Maximum
Pain intensity (VAS, cm)	7.1 (12.2)	4.0	7.0	9.0
Pain discomfort (VAS, cm)	7.6 (15.1)	4.0	7.0	9.0
HIT-6	65.1 (4.0)	54.0	65.0	76.0
Headache frequency (days per month)	17.4 (7.8)	8.0	16.0	30.0
Medicine frequency (days per week)	3.2 (2.1)	2.0	4.0	7.0

Variables	NH (n=23) (mean ± SD)	CM (n=23) (mean ± SD)	p-value
Pittsburgh Sleep Quality Index	5.17±2.31	8.74±2.60	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.
Epworth Sleepiness Scale	7.13±5.62	7.30±4.30	0.82
Actigraphic parameters
MESOR^† † The variables represent the values of 34 individuals (n=17 each in the NH and CM groups). Shapiro-Wilk normality test; Student’s t-test was used for the variables CFI, SRI, fSoD, AUCActivity, and CVAON. For all other variables, the Mann-Whitney test was applied;	86.69±9.42	72.11±18.94	0.01^* * p < 0.05, p < 0.01, * p <0.001.
Amplitude^† † The variables represent the values of 34 individuals (n=17 each in the NH and CM groups). Shapiro-Wilk normality test; Student’s t-test was used for the variables CFI, SRI, fSoD, AUCActivity, and CVAON. For all other variables, the Mann-Whitney test was applied;	47.35±9.52	34.40±17.50	0.02^* * p < 0.05, p < 0.01, * p <0.001.
Acrophase (min)	918.76±73.87	967.84±180.86	0.04^* * p < 0.05, p < 0.01, * p <0.001.
%V (%)	50.68±5.56	42.01±11.42	0.01^* * p < 0.05, p < 0.01, * p <0.001.
L5^† † The variables represent the values of 34 individuals (n=17 each in the NH and CM groups). Shapiro-Wilk normality test; Student’s t-test was used for the variables CFI, SRI, fSoD, AUCActivity, and CVAON. For all other variables, the Mann-Whitney test was applied;	23.17±5.28	19.91±5.70	0.03^* * p < 0.05, p < 0.01, * p <0.001.
M10^† † The variables represent the values of 34 individuals (n=17 each in the NH and CM groups). Shapiro-Wilk normality test; Student’s t-test was used for the variables CFI, SRI, fSoD, AUCActivity, and CVAON. For all other variables, the Mann-Whitney test was applied;	124.86±13.47	112.31±17.11	0.05
IS	0.50±0.11	0.38±0.14	< 0.01^** * p < 0.05, p < 0.01, * p <0.001.
IV	0.63±0.08	0.67±0,11	0.63
RA	0.69±0.06	0.70±0.06	0.70
AUC_Activity	133193±21238	119000±28599	0.063
%AUC_Sleep	9.35±2.35	13.29±4.18	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.
CVAON	0.17±0.07	0.28±0.12	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.
CVAOF	0.04±0.02	0.10±0.09	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.
CFI	0.58±0.05	0.51±0.08	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.
SRI	66.41±9.76	43.80±20.78	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.
fSoD	0.13±0.08	0.23±0.10	< 0.001^*** * p < 0.05, p < 0.01, * p <0.001.

	STAI-T (+)				STAI-T (-)				STAI-T (total)
Activity/rest rhythm	EST	SE	R²	p-value	EST	SE	R²	p-value	EST	SE	R²	p-value
RA	-26.57	11.61	0.15	0.02^* Multiple linear regression test, * p < 0.05, ** p < 0.01.	-18.50	23.11	0.03	0.42	-4.07	31.07	0.07	0.15
AUC_Activity	0.00	0.00	0.18	0.02^* Multiple linear regression test, * p < 0.05, ** p < 0.01.	0.00	0.00	0.04	0.74	0.00	0.00	0.08	0.27
%AUC_Sleep	1.27	0.35	0.35	0.001^** Multiple linear regression test, * p < 0.05, ** p < 0.01.	1.48	0.75	0.15	0.05^* Multiple linear regression test, * p < 0.05, ** p < 0.01.	2.75	0.96	0.26	0.007^** Multiple linear regression test, * p < 0.05, ** p < 0.01.
CFI	-41.09	21.13	0.13	0.05^* Multiple linear regression test, * p < 0.05, ** p < 0.01.	-26.47	41.50	0.03	0.53	-67.55	56.04	0.06	0.23

[1] Correspondence: Rhowena Jane Barbosa de Matos, Centro de Ciências da Saúde, Universidade Federal do Recôncavo da Bahia (UFRB), Av. Carlos Amaral, 1015, Cajueiro, CEP 44574-490, Santo Antônio de Jesus, BA, Brazil. E-mail: rhowena.matos@ufrb.edu.br

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Changes in the rest-activity rhythm in migraine patients are associated with anxiety symptoms

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