Assessing Chronotypes by Ambulatory Circadian Monitoring

Antonio Martinez-Nicolas, Maria Jose Martinez-Madrid, Pedro Francisco Almaida-Pagan, Maria-Angeles Bonmati-Carrion, Juan Antonio Madrid, Maria Angeles Rol, Antonio Martinez-Nicolas, Maria Jose Martinez-Madrid, Pedro Francisco Almaida-Pagan, Maria-Angeles Bonmati-Carrion, Juan Antonio Madrid, Maria Angeles Rol

Abstract

In order to develop objective indexes for chronotype identification by means of direct measurement of circadian rhythms, 159 undergraduate students were recruited as volunteers and instructed to wear ambulatory circadian monitoring (ACM) sensors that continuously gathered information on the individual's environmental light and temperature exposure, wrist temperature, body position, activity, and the integrated TAP (temperature, activity, and position) variable for 7 consecutive days under regular free-living conditions. Among all the proposed indexes, the night phase marker (NPM) of the TAP variable was the best suited to discriminate among chronotypes, due to its relationship with the Munich ChronoType Questionnaire (β = 0.531; p < 0.001). The NPM of TAP allowed subjects to be classified as early- (E-type, 20%), neither- (N-type, 60%), and late-types (L-type, 20%), each of which had its own characteristics. In terms of light exposure, while all subjects had short exposure times to bright light (>100 lux), with a daily average of 93.84 ± 5.72 min, the earlier chronotypes were exposed to brighter days and darker nights compared to the later chronotypes. Furthermore, the earlier chronotypes were associated with higher stability and day-night contrast, along with an earlier phase, which could be the cause or consequence of the light exposure habits. Overall, these data support the use of ACM for chronotype identification and for evaluation under free living conditions, using objective markers.

Keywords: activity; ambulatory circadian monitoring; chronotype; circadian rhythm; distal skin temperature; light exposure.

Copyright © 2019 Martinez-Nicolas, Martinez-Madrid, Almaida-Pagan, Bonmati-Carrion, Madrid and Rol.

Figures

FIGURE 1
FIGURE 1
Mean waveforms and actograms for early (E-types, in yellow; n = 20% of total subjects), neither (N-types, in dotted black; n = 60% of total subjects), and late-types (L-types, in blue; n = 20% of total subjects) for: (A) light exposure (L; total subjects = 137) and (B) environmental temperature (ET; total subjects = 137). Waveform data are expressed as mean ± SEM. Plotted actograms correspond to the first tercile values (values corresponding to the rest phase).
FIGURE 2
FIGURE 2
Mean waveforms and actograms for early (E-types, in yellow; n = 20% of total subjects), neither (N-types, in dotted black; n = 60% of total subjects), and late-types (L-types, in blue; n = 20% of total subjects) for: (A) wrist temperature (WT; total subjects = 159), (B) activity (A; total subjects = 159), and (C) body position (P; total subjects = 159). Waveform data are expressed as mean ± SEM. WT actogram corresponds to the third tercile values, while activity and body position actograms correspond to the first tercile values (values corresponding to the rest phase).
FIGURE 3
FIGURE 3
Mean waveforms and actograms for early (E-types, in yellow; n = 20% of the total subjects), neither (N-types, in dotted black; n = 60% of the total subjects), and late-types (L-types, in blue; n = 20% of the total subjects) for: (A) TAP (total subjects = 159) and (B) sleep (S; total subjects = 148). Waveform data are expressed as mean ± SEM. TAP and sleep actograms correspond to the first and third tercile values, respectively (values corresponding to the rest phase).

References

    1. Adan A., Archer S. N., Hidalgo M. P., Di Milia L., Natale V., Randler C. (2012). Circadian typology: a comprehensive review. Chronobiol. Int. 29 1153–1175. 10.3109/07420528.2012.719971
    1. Adan A., Lachica J., Caci H., Natale V. (2010a). Circadian typology and temperament and character personality dimensions. Chronobiol. Int. 27 181–193. 10.3109/07420520903398559
    1. Adan A., Natale V., Caci H., Prat G. (2010b). Relationship between circadian typology and functional and dysfunctional impulsivity. Chronobiol. Int. 27 606–619. 10.3109/07420521003663827
    1. Allebrandt K. V., Teder-Laving M., Kantermann T., Peters A., Campbell H., Rudan I., et al. (2014). Chronotype and sleep duration: the influence of season of assessment. Chronobiol. Int. 31 731–740. 10.3109/07420528.2014.901347
    1. Batinga H., Martinez-Nicolas A., Zornoza-Moreno M., Sánchez-Solis M., Larqué E., Mondejar M. T., et al. (2015). Ontogeny and aging of the distal skin temperature rhythm in humans. Age 37:29. 10.1007/s11357-015-9768-y
    1. Bonmati-Carrion M. A., Arguelles-Prieto R., Martinez-Madrid M. J., Reiter R. J., Hardeland R., Rol M. Á, et al. (2014a). Protecting the melatonin rhythm through circadian healthy light exposure. Int. J. Mol. Sci. 15 23448–23500. 10.3390/ijms151223448
    1. Bonmati-Carrion M. A., Middleton B., Revell V., Skene D. J., Rol M. A., Madrid J. A. (2014b). Circadian phase asessment by ambulatory monitoring in humans: correlation with dim light melatonin onset. Chronobiol. Int. 31 37–51. 10.3109/07420528.2013.820740
    1. Cain N., Gradisar M. (2010). Electronic media use and sleep in school-aged children and adolescents: a review. Sleep Med. 11 735–742. 10.1016/j.sleep.2010.02.006
    1. Carissimi A., Martins A. C., Dresch F., da Silva L. C., Zeni C. P., Hidalgo M. P. (2016). School start time influences melatonin and cortisol levels in children and adolescents–a community-based study. Chronobiol. Int. 33 1400–1409. 10.1080/07420528.2016.1222537
    1. Chang A.-M., Aeschbach D., Duffy J. F., Czeisler C. A. (2014). Evening use of light-emitting Ereaders negatively affects sleep, circadian timing, and next-morning alertness. Proc. Natl. Acad. Sci. U.S.A. 112:201418490. 10.1073/pnas.1418490112
    1. Charkoudian N. (2003). Skin blood flow in adult human thermoregulation: how it works, when it does not, and why. Mayo Clin. Proc. 78 603–612. 10.4065/78.5.603
    1. Dewan K., Benloucif S., Reid K., Wolfe L. F., Zee P. C. (2011). Light-induced changes of the circadian clock of humans: increasing duration is more effective than increasing light intensity. Sleep 34 593–599. 10.1016/j.yspm.2011.09.019
    1. Di Milia L., Adan A., Natale V., Randler C. (2013). Reviewing the psychometric properties of contemporary circadian typology measures. Chronobiol. Int. 30 1261–1271. 10.3109/07420528.2013.817415
    1. Ebisawa T., Uchiyama M., Kajimura N., Mishima K., Kamei Y., Katoh M., et al. (2001). Association of structural polymorphisms in the human. Mol. Biol. 2 342–346.
    1. Erren T. C., Reiter R. J. (2009). Defining chronodisruption. J. Pineal Res. 46 245–247. 10.1111/j.1600-079X.2009.00665.x
    1. Erren T. C., Reiter R. J. (2013). Revisiting chronodisruption: when the physiological nexus between internal and external times splits in humans. Naturwissenschaften 100 291–298. 10.1007/s00114-013-1026-25
    1. Espiritu R., Kripke D., Ancoli-Israel S., Mowen M., Mason W., Fell R., et al. (1994). Low illumination experienced by san diego adults: association with atypical depressive symptoms. Biol. Psychiatr. 35 403–407. 10.1016/0006-3223(94)90007-8
    1. Fabbian F., Zucchi B., De Giorgi A., Tiseo R., Boari B., Salmi R., et al. (2016). Chronotype, gender and general health. Chronobiol. Int. 33 863–882. 10.1080/07420528.2016.1176927
    1. Gamble K. L., Motsinger-Reif A. A., Hida A., Borsetti H. M., Servick S. V., Ciarleglio C. M., et al. (2011). Shift work in nurses: contribution of phenotypes and genotypes to adaptation. PLoS One 6:e18395. 10.1371/journal.pone.0018395
    1. Giannotti F., Cortesi F., Sebastiani T., Ottaviano S. (2002). Circadian preference, sleep and daytime behaviour in adolescence. J. Sleep Res. 11 191–199. 10.1046/j.1365-2869.2002.00302.x
    1. Gomez-Garcia T., Ruzafa-Martinez M., Fuentelsaz-Gallego C., Madrid J. A., Rol M. A., Martinez-Madrid M. J., et al. (2016). Nurses’ sleep quality, work environment and quality of care in the spanish national health system: observational study among different shifts. BMJ Open 6 1–11. 10.1136/bmjopen-2016-012073
    1. Horne J. A., Ostberg O. (1976). A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int. J. Chronobiol. 4 97–110. 10.1177/0748730405285278
    1. Hubert M., Dumont M., Paquet J. (1998). Seasonal and diurnal patterns of human illumination under natural conditions. Chronobiol. Int. 15 59–70. 10.3109/07420529808998670
    1. Jewett M. E., Forger D. B., Kronauer R. E. (1999). Revised limit cycle oscillator model of human circadian pacemaker. J. Biol. Rhythms 14 493–499. 10.1177/074873099129001064
    1. Juda M., Vetter C., Roenneberg T. (2013). Chronotype modulates sleep duration, sleep quality, and social jet lag in shift-workers. J. Biol. Rhythms 28 141–151. 10.1177/0748730412475042
    1. Kantermann T., Juda M., Merrow M., Roenneberg T. (2007). The human circadian clock’s seasonal adjustment is disrupted by daylight saving time. Curr. Biol. 17 1996–2000. 10.1016/j.cub.2007.10.025
    1. Khalsa S., Jewett M., Cajochen C., Czeisler C. A. (2003). A phase response curve to single bright light pulses in human subjects. J. Physiol. 549 945–952. 10.1113/jphysiol.2003.040477
    1. Kolodyazhniy V., Spati J., Frey S., Gotz T., Wirz-Justice A., Kräuchi K., et al. (2011). Estimation of human circadian phase via a multi-channel ambulatory monitoring system and a multiple regression model. J. Biol. Rhythms 26 55–67. 10.1177/0748730410391619
    1. Kolodyazhniy V., Späti J., Frey S., Götz T., Wirz-Justice A., Kräuchi K., et al. (2012). An improved method for estimating human circadian phase derived from multichannel ambulatory monitoring and artificial neural networks. Chronobiol. Int. 29 1078–1097. 10.3109/07420528.2012.700669
    1. Kräuchi K., Wirz-Justice A. (1994). Circadian rhythm of heat production, heart rate, and skin and core temperature under unmasking conditions in men. Am. J. Physiol. 267 R819–R829.
    1. Lévi F., Okyar A. (2011). Circadian clocks and drug delivery systems: impact and opportunities in chronotherapeutics. Expert Opin. Drug Deliv. 8 1535–1541. 10.1517/17425247.2011.618184
    1. Li X., Dunn J., Salins D., Zhou G., Zhou W., Schüssler-Fiorenza Rose S. M., et al. (2017). Digital health: tracking physiomes and activity using wearable biosensors reveals useful health-related information. PLoS Biol. 15:e2001402. 10.1371/journal.pbio.2001402
    1. Madrid-Navarro C. J., Cuesta F. J. P., Escamilla-Sevilla F., Campos M., Abellán F. R., Rol M. A., et al. (2019). Validation of a device for the ambulatory monitoring of sleep patterns: a pilot study on Parkinson’s disease. Front. Neurol. 10:356. 10.3389/fneur.2019.00356
    1. Madrid-Navarro C. J., Escamilla-Sevilla F., Mínguez-Castellanos A., Campos M., Ruiz-Abellán F., Madrid J. A., et al. (2018). Multidimensional circadian monitoring by wearable biosensors in Parkinson’s disease. Front. Neurol. 9:157. 10.3389/fneur.2018.00157
    1. Marken W. D. V., Daanen H. A. M., Wouters L., Fronczek R., Raymann R. J. E. M., Severens N. M. W., et al. (2006). Evaluation of wireless determination of skin temperature using iButtons. Physiol. Behav. 88 489–497. 10.1016/j.physbeh.2006.04.026
    1. Martinez-Nicolas A., Guaita M., Santamaría J., Montserrat J. M., Rol M. Á, Madrid J. A. (2017). Circadian impairment of distal skin temperature rhythm in patients with sleep-disordered breathing: the effect of CPAP. Sleep 40:zsx067. 10.1093/sleep/zsx067
    1. Martinez-Nicolas A., Madrid J. A., García F. J., Campos M., Moreno-Casbas M. T., Almaida-Pagán P. F., et al. (2018). Circadian monitoring as an aging predictor. Sci. Rep. 8:15027. 10.1038/s41598-018-33195-93
    1. Martinez-Nicolas A., Madrid J. A., Rol M. Á. (2014). Day-night contrast as source of health for the human circadian system. Chronobiol. Int. 31 382–393. 10.3109/07420528.2013.861845
    1. Martinez-Nicolas A., Ortiz-Tudela E., Madrid J. A., Rol M. Á. (2011). Crosstalk between environmental light and internal time in humans. Chronobiol. Int. 28 617–629. 10.3109/07420528.2011.593278
    1. Mishima K., Okawa M., Shimizu T., Hishikawa Y. (2001). Diminished melatonin secretion in the elderly caused by insufficient environmental illumination. J. Clin. Endocrinol. Metab. 86 129–134. 10.1210/jc.86.1.129
    1. Mormont M., Waterhouse J., Bleuzen P., Mormont M., Waterhouse J., Bleuzen P., et al. (2000). Marked 24-h rest/activity rhythms are associated with better quality of life, better response, and longer survival in patients with metastatic colorectal cancer and good performance status marked 24-h rest/activity rhythms are associated with better. Clin. Cancer Res. 6 3038–3045.
    1. Mullington J. M., Abbott S. M., Carroll J. E., Davis C. J., Dijk D.-J., Dinges D. F., et al. (2016). Developing biomarker arrays predicting sleep and circadian-coupled risks to health. Sleep 39 727–736. 10.5665/sleep.5616
    1. Muro A., Gomà-I-Freixanet M., Adan A. (2009). Morningness-eveningness, sex, and the alternative five factor model of personality. Chronobiol. Int. 26 1235–1248. 10.1080/07420520903240491
    1. Ortiz-Tudela E., Innominato P. F., Rol M. A., Lévi F., Madrid J. A. (2016). Relevance of internal time and circadian robustness for cancer patients. BMC Cancer 16:285. 10.1186/s12885-016-2319-2319
    1. Ortiz-Tudela E., Martinez-Nicolas A., Albares J., Segarra F., Campos M., Estivill E., et al. (2014a). Ambulatory circadian monitoring (ACM) based on thermometry, motor activity and body position (TAP): a comparison with polysomnography. Physiol. Behav. 126 30–38. 10.1016/j.physbeh.2013.12.009
    1. Ortiz-Tudela E., Martinez-Nicolas A., Díaz-Mardomingo C., García-Herranz S., Pereda-Pérez I., Valencia A., et al. (2014b). The characterization of biological rhythms in mild cognitive impairment. BioMed. Res. Int. 2014:524971. 10.1155/2014/524971
    1. Ortiz-Tudela E., Martinez-Nicolas A., Campos M., Rol M. Á, Madrid J. A. (2010). A new integrated variable based on thermometry, actimetry and body position (TAP) to evaluate circadian system status in humans. PLoS Comput. Biol. 6:e1000996. 10.1371/journal.pcbi.1000996
    1. Paine S.-J., Gander P. H., Travier N. (2006). The epidemiology of morningness/eveningness: influence of age, gender, ethnicity, and socioeconomic factors in adults (30-49 years). J. Biol. Rhythms 21 68–76. 10.1177/0748730405283154
    1. Roenneberg T., Hut R., Daan S., Merrow M. (2010). Entrainment concepts revisited. J. Biol. Rhythms 25 329–339. 10.1177/0748730410379082
    1. Roenneberg T., Kantermann T., Juda M., Vetter C., Allebrandt K. V. (2013). “Light and the human circadian clock,” in Handbook of Experimental Pharmacology, eds Kramer A., Merrow M., (Berlin: Springer; ), 311–331. 10.1007/978-3-642-25950-0_13
    1. Roenneberg T., Kuehnle T., Juda M., Kantermann T., Allebrandt K. V., Gordijn M., et al. (2007). Epidemiology of the human circadian clock. Sleep Med. Rev. 11 429–438. 10.1016/j.smrv.2007.07.005
    1. Roenneberg T., Kuehnle T., Pramstaller P. P., Ricken J., Havel M., Guth A., et al. (2004). A marker for the end of adolescence. Curr. Biol. 14 R1038–R1039. 10.1016/j.cub.2004.11.039
    1. Roenneberg T., Wirz-Justice A., Merrow M. (2003). Life between clocks: daily temporal patterns of human chronotypes. J. Biol. Rhythms 18 80–90. 10.1177/0748730402239679
    1. Rubinstein E. H., Sessler D. I. (1990). Skin-surface temperature gradients correlate with fingertip blood flow in humans. Anesthesiology 73 541–545. 10.1097/00000542-199009000-00027
    1. Santisteban J. A., Brown T. G., Gruber R. (2018). Association between the munich chronotype questionnaire and wrist actigraphy. Sleep Disord. 2018:5646848. 10.1155/2018/5646848
    1. Sarabia J. A., Rol M. Á, Mendiola P., Madrid J. A. (2008). Circadian rhythm of wrist temperature in normal-living subjects. A candidate of new index of the circadian system. Physiol. Behav. 95 570–580. 10.1016/j.physbeh.2008.08.005
    1. Savides T., Messin S., Senger C., Kripke D. (1986). Natural light exposure of young adults. Physiol. Behav. 38 571–574. 10.1016/0031-9384(86)90427-0
    1. Schmidt C., Collette F., Reichert C. F., Maire M., Vandewalle G., Peigneux P., et al. (2015). Pushing the limits: chronotype and time of day modulate working memory-dependent cerebral activity. Front. Neurol. 6:199. 10.3389/fneur.2015.00199
    1. Sharkey K. M., Carskadon M. A., Figueiro M. G., Zhu Y., Rea M. S. (2011). Effects of an advanced sleep schedule and morning short wavelength light exposure on circadian phase in young adults with late sleep schedules. Sleep Med. 12 685–692. 10.1016/j.sleep.2011.01.016
    1. Smith M. T., McCrae C. S., Cheung J., Martin J. L., Harrod C. G., Heald J. L., et al. (2018a). Use of actigraphy for the evaluation of sleep disorders and circadian rhythm sleep-wake disorders: an american academy of sleep medicine clinical practice guideline. J. Clin. Sleep Med. 14 1231–1237. 10.5664/jcsm.7702
    1. Smith M. T., McCrae C. S., Cheung J., Martin J. L., Harrod C. G., Heald J. L., et al. (2018b). Use of actigraphy for the evaluation of sleep disorders and circadian rhythm sleep-wake disorders: an american academy of sleep medicine systematic review, meta-analysis, and grade assessment. J. Clin. Sleep Med. 14 1209–1230. 10.5664/jcsm.7228
    1. St Hilaire M. A., Gronfier C., Zeitzer J. M., Klerman E. B. (2007a). A physiologically based mathematical model of melatonin including ocular light suppression and interactions with the circadian pacemaker. J. Pineal Res. 43 294–304. 10.1111/j.1600-079X.2007.00477.x
    1. St Hilaire M. A., Klerman E. B., Khalsa S. B. S., Wright K. P., Czeisler C. A., Kronauer R. E. (2007b). Addition of a non-photic component to a light-based mathematical model of the human circadian pacemaker. J. Theor. Biol. 247 583–599. 10.1016/j.jtbi.2007.04.001
    1. Susman E. J., Dockray S., Schiefelbein V. L., Herwehe S., Heaton J. A., Dorn L. D. (2007). Morningness/eveningness, morning-to-afternoon cortisol ratio, and antisocial behavior problems during puberty. Dev. Psychol. 43 811–822. 10.1037/0012-1649.43.4.811
    1. Toh K. L., Jones C. R., He Y., Eide E. J., Hinz W. A., Virshup D. M., et al. (2001). An hPer2 phosphorylation site mutation in familiar advanced sleep phase syndrome. Science 291 1040–1043. 10.1126/science.1057499
    1. Tonetti L., Fabbri M., Natale V. (2009). Relationship between circadian typology and big five personality domains. Chronobiol. Int. 26 337–347. 10.1080/07420520902750995
    1. Touitou Y., Touitou D., Reinberg A. (2016). Disruption of adolescents’ circadian clock: the vicious circle of media use, exposure to light at night, sleep loss and risk behaviors. J. Physiol. Paris 110 467–479. 10.1016/j.jphysparis.2017.05.001
    1. Turner P. L., Mainster M. (2008). Circadian photoreception: ageing and the eye’s important role in systemic health. Br. J. Ophthalmol. 92 1439–1444. 10.1136/bjo.2008.141747
    1. Van Someren E. J. (2000). More than a marker: interaction between the circadian regulation of temperature and sleep, age-related changes, and treatment possibilities. Chronobiol. Int. 17 313–354. 10.1081/cbi-100101050
    1. Van Someren E. J. W., Swaab D. F., Colenda C. C., Cohen W., Mccall W. V., Rosenquist P. B. (1999). Bright light therapy improved rest-activity rhythms in Alzheimer patients by application of nonparametric methods. Chornobiol. Int. 16 505–518. 10.3109/07420529908998724
    1. Witting W., Kwa I. H., Eikelenboom P., Mirmiran M., Swaab D. F. (1990). Alteration in the circadian rest-activity rhythm in aging and alzheimer’s disease. Biol. Psychiatr. 27 563–572. 10.1016/0006
    1. Wittmann M., Dinich J., Merrow M., Roenneberg T. (2006). Social jetlag: misalignment of biological and social time. Chronobiol. Int. 23 497–509. 10.1080/07420520500545979
    1. Wright K. P., Mchill A. W., Birks B. R., Griffin B. R., Rusterholz T., Chinoy E. D. (2013). Entrainment of the human circadian clock to the natural light-dark cycle. Curr. Biol. 23 1554–1558. 10.1016/j.cub.2013.06.039
    1. Zeitzer J. M., Friedman L., Yesavage J. A. (2011). Effectiveness of evening phototherapy for insomnia is reducedby bright daytime light exposure. Sleep Med. 12 805–807. 10.1016/j.sleep.2011.02.005
    1. Zerbini G., Kantermann T., Merrow M. (2018). Strategies to decrease social jetlag: reducing evening blue light advances sleep and melatonin. Eur. J. Neurosci. 10.1111/ejn.14293 [Epub ahead of print].
    1. Zerbini G., Merrow M. (2017). Time to learn: how chronotype impacts education. Psych. J. 6 263–276. 10.1002/pchj.178
    1. Zuurbier L. A., Luik A. I., Hofman A., Franco O. H., Van Someren E. J., Tiemeier H. (2015). Fragmentation and stability of circadian activity rhythms predict mortality - the rotterdam study. Am. J. Epidemiol. 181 54–63. 10.1093/aje/kwu245

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