Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Ontogeny and aging of the distal skin temperature rhythm in humans

  • 228 Accesses

  • 12 Citations

Abstract

In circadian terms, human ontogeny is characterized by the emergence of a daily pattern, from a previous ultradian pattern, for most variables during the first 6 months of life. Circadian aging in humans is characterized by a phase advance, accompanied by rhythm fragmentation and flattening. Despite an expanding body of literature focused on distal skin temperature, little information is available about the ontogeny and practically nothing about age-related changes in this rhythm. Thus, the aim was to evaluate the degree of maturation and aging of the circadian pattern of distal skin temperature to identify those parameters that are modified throughout life and could be used to differentiate subjects according to their age. For this, distal skin temperature was measured in 197 volunteers (55 % women), including babies aged 15 days (30 subjects), 1 month (28 subjects), 3 months (31 subjects), and 6 months (10 subjects); young adults aged 19 years (37 subjects); middle-aged persons aged 46 years (27 subjects); older people aged 72 (34 subjects). Circadian system maturation was associated with an increase in amplitude and a reduction in skin temperature during sleep. During adulthood, women showed a more robust pattern (lower fragmentation, and higher night-time temperature, amplitude, circadian function index, and first harmonic relative power); however, these differences were lost with aging, a period of life that was consistently associated with a phase advance of the rhythm. In summary, distal skin temperature pattern can be used as a robust variable to discern between different ages throughout the life.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Adan N, Natale V (2002) Gender differences in morningness-eveningness preference. Chronobiol Int 19:709–720

  2. Azevedo CVM, Sousa I, Paul K, MacLeish MY, Mondéjar MT, Sarabia JA, Rol MA, Madrid JA (2008) Teaching chronobiology and sleep habits in school and university. Mind Brain Educ 2:34–47

  3. Bandín C, Martinez-Nicolas A, Ordovás JM, Ros Lucas JA, Castell P, Silvente T, Madrid JA, Garaulet M (2012) Differences in circadian rhythmicity in CLOCK 3111T/C genetic variants in moderate obese women as assessed by thermometry, actimetry and body position. Int J Obes 37:1044–1050

  4. Blazquez A, Martinez-Nicolas A, Salazar FJ, Rol MA, Madrid JA (2012) Wrist skin temperature, motor activity, and body position as determinants of the circadian pattern of blood pressure. Chronobiol Int 29:747–756

  5. Bonmati-Carrion MA, Middleton B, Revell V, Skene DJ, Rol MA, Madrid JA (2014) Circadian phase assessment by ambulatory monitoring in humans: correlation with dim light melatonin onset. Chronobiol Int 31:37–51

  6. Buijs RM, la Fleur SE, Wortel J, Van Heyningen C, Zuiddam L, Mettenleiter TC, Kalsbeek A, Nagai K, Niijima A (2003) The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J Comp Neurol 464:36–48

  7. Cajochen C, Zeitzer JM, Czeisler CA, Dijk DJ (2000) Dose-response relationship for light intensity and ocular and electroencephalographic correlates of human alertness. Behav Brain Res 115:75–83

  8. 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

  9. Dijk DJ, Duffy JF, Czeisler CA (2000) Contribution of circadian physiology and sleep homeostasis to age-related changes in human sleep. Chronobiol Int 17:285–311

  10. Garaulet M, Ordovás JM, Madrid JA (2010) The chronobiology, etiology and pathophysiology of obesity. Int J Obes 34:1667–1683

  11. Harper DG, Volicer L, Stopa EG, McKee AC, Nitta M, Satlin A (2005) Disturbance of endogenous circadian rhythm in aging and Alzheimer disease. Am J Geriatr Psychiatr 13:359–368

  12. Hofman MA, Swaab DF (2006) Living by the clock: the circadian pacemaker in older people. Ageing Res Rev 5:33–51

  13. Kendall AR, Lewy AJ, Sack RL (2001) Effects of aging on the intrinsic circadian period of totally blind humans. J Biol Rhythm 16:87–95

  14. Kräuchi K (2002) How is the circadian rhythm of core body temperature regulated? Clin Auton Res 12:147–149

  15. 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

  16. Kräuchi K, Cajochen C, Wirz-Justice A (2005) Thermophysiologic aspects of the three-process-model of sleepiness regulation. Clin Sports Med 24:287–300

  17. Kräuchi K, Knoblauch V, Wirz-Justice A, Cajochen C (2006) Challenging the sleep homeostat does not influence the thermoregulatory system in men: evidence from a nap vs. sleep deprivation study. Am J Physiol Regul Integr Comp Physiol 290:R1052–R1061

  18. Martinez-Nicolas A, Ortiz-Tudela E, Rol MA, Madrid JA (2013) Uncovering different masking factors on wrist skin temperature rhythm in free-living subjects. PLoS One 8:e61142

  19. Martinez-Nicolas A, Madrid JA, Rol MA (2014) Day-night contrast as source of health for the human circadian system. Chronobiol Int 31:382–393

  20. McGraw K, Hoffman R, Harker C, Herman JH (1999) The development of circadian rhythms in a human infant. Sleep 22:303–310

  21. Minors D, Atkinson G, Bent N, Rabbit P, Waterhouse J (1998) The effects of age upon some aspects of lifestyle and implications for studies on circadian rhythmicity. Age Ageing 27:67–72

  22. Ortiz-Tudela E, Martinez-Nicolas A, Campos M, Rol MA, Madrid JA (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. doi:10.1371/journal.pcbi.1000996

  23. Reilly T, Waterhouse J (2009) Circadian aspects of body temperature regulation in exercise. J Therm Biol 34:161–170

  24. Reiter RJ, Tan DX, Korkmaz A, Erren TC, Piekarski C, Tamura H, Manchester LC (2007) Light at night, chronodisruption, melatonin suppression, and cancer risk: a review. Crit Rev Oncog 13:303–328

  25. Rivkees SA (2003) Developing circadian rhythmicity in infants. Pediatrics 112:373–381

  26. Roenneberg T, Kuehnle T, Juda M, Kantermann T, Allebrandt K, Gordijn M, Merrow M (2007) Epidemiology of the human circadian clock. Sleep Med Rev 11:429–438

  27. Romejin N, Someren EJW (2011) Correlated fluctuations of daytime skin temperature and vigilance. J Biol Rhythm 26:68–77

  28. Sarabia JA, Rol MA, Mendiola P, Madrid JA (2008) Circadian rhythm of wrist temperature in normal-living subjects: a candidate of new index the circadian system. Physiol Behav 95:570–580

  29. Sosa M, Mondéjar MT, Martinez-Nicolas A, Ortiz-Tudela E, Sarabia JA, Sosa J, Otalora B, Rol MA, Madrid JA, Campos M, Marín R (2010) Circadianware. Spanish Patent 08/2010/183

  30. Stratmann M, Schibler U (2006) Properties, entrainment, and physiological functions of mammalian peripheral oscillators. J Biol Rhythm 21:494–506

  31. Turek FW, Penev P, Zhang Y, van Reeth O, Zee P (1995) Effects of age on the circadian system. Neurosci Biobehav Rev 19:53–58

  32. Van Someren EJW (2000) More than a marker: interacion between the circadian regulation of temperature and sleep, age-related changes, and treatment possibilities. Chronobiol Int 17:313–354

  33. Van Someren EJW, Swaab DF, Colenda CC, Cohen W, McCall WV, Rosenquist PB (1999) Bright light therapy: improved sensitivity to its effects on rest-activity rhythms in Alzheimer patients by application of nonparametric methods. Chronobiol Int 16:505–518

  34. Wakamura T, Tokura H (2002) Circadian rhythm if rectal temperature in humans under different ambient temperature cycles. J Therm Biol 27:439–447

  35. Waterhouse J, Fukuda Y, Morita T (2012) Daily rhythms of the sleep-wake cycle. J Physiol Anthropol 31:5

  36. Weinert D (2005) Ontogenic development of the mammalian circadian system. Chronobiol Int 22:179–205

  37. Worobey J, Vetrini NR, Rozo EM (2009) Mechanical measurement of infant activity: a cautionary note. Infant Behav Dev 32:167–172

  38. Zornoza-Moreno M, Fuentes-Hernández S, Sánchez-Solis M, Rol MA, Larqué E, Madrid JA (2011) Assessment of circadian rhythms of both skin temperature and motor activity in infants during the first 6 months of life. Chronobiol Int 28:330–337

Download references

Acknowledgments

This work was supported by the Ministry of Economy and Competitiveness and the Instituto de Salud Carlos III—RETICEF (The Aging and Frailty Cooperative Research Network, RD12/0043/0011, RD12/0043/006, and RD12/0043/0020), the Ministry of Education and Science, and the Ministry of Economy and Competitiveness (BFU2010-21945-C02-01 and IPT-2011-0833-900000), including FEDER cofunding provided to J. A. Madrid. We would like to thank Imanol Martínez for his kind revision of the manuscript.

Conflict of interest

The authors have reported no conflicts of interest.

Author information

Correspondence to M. A. Rol.

Additional information

H. Batinga and A. Martinez-Nicolas contributed equally to this work.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Batinga, H., Martinez-Nicolas, A., Zornoza-Moreno, M. et al. Ontogeny and aging of the distal skin temperature rhythm in humans. AGE 37, 29 (2015). https://doi.org/10.1007/s11357-015-9768-y

Download citation

Keywords

  • Distal skin temperature
  • Circadian rhythm
  • Ontogeny
  • Human
  • Newborns
  • Aging