Development of cortisol circadian rhythm in infancy
Abstract
Background and aims Cortisol is the final product of the hypothalamus-pituitary-adrenal (HPA) axis. It is secreted in a pulsatile fashion that displays a circadian rhythm. Infants are born without a circadian rhythm in cortisol and they acquire it during their first year of life. Studies do not agree on the age of appearance of the circadian rhythm (varying between 2 weeks till the age of 9 months) nor on whether it is related to the appearance of the sleep-wake circadian rhythm. The object of the present study was to find evidence of the age of appearance of the diurnal rhythm of cortisol and to compare the results obtained by several different analysis methods on a new data set. Design and measures Cortisol was determined in salival samples of 14 normally developing infants who were followed monthly between the ages of 2 and 5 months. The data were analyzed with several previously published analysis methods as well as with Multilevel Analysis (Hierarchical Linear Modeling). Results The previously published analysis methods each produced different results when applied to the current data set. Moreover, our results indicate striking differences between young infants in both age of appearance and stability of the diurnal cortisol rhythm. Also, a link was found between the appearance of the sleep-wake circadian rhythm and the cortisol circadian rhythm. An important intraindividual variability in cortisol levels was found even after correcting for the different variables that af…
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Prenatal exposure to maternal stress hormones is linked to temperamental reactivity and stress physiology, likely through epigenetic regulation of gene expression.
“prenatal exposure to maternal stress hormones is linked to temperamental reactivity and stress physiology, likely through epigenetic regulation of gene expression”
From The Adaptive Calibration Model of stress responsivity (2011) · cites this paper as de Weerth et al., 2003
Cites
Hierarchical Linear Models: Applications and Data Analysis Methods.
Longford, N. T., Bryk, A. S., & Raudenbush, S. W. (1993) · Contemporary Sociology A Journal of Reviews · doi:10.2307/2075823 · Cited by 18,768 · see citing works
Hierarchical Linear Models: Applications and Data Analysis Methods.
Goldstein, H., Bryk, A. S., & Raudenbush, S. W. (1993) · Journal of the American Statistical Association · doi:10.2307/2290750 · Cited by 3,320 · see citing works
Salivary cortisol in psychoneuroendocrine research: recent developments and applications
Kirschbaum, C., & Hellhammer, D. H. (1994) · Psychoneuroendocrinology · doi:10.1016/0306-4530(94)90013-2 · Cited by 2,107 · see citing works
Salivary Cortisol in Psychobiological Research: An Overview
Kirschbaum, C., & Hellhammer, D. H. (2008) · Neuropsychobiology · doi:10.1159/000118611 · Cited by 1,532 · see citing works
Effects of gender and age on the levels and circadian rhythmicity of plasma cortisol
Van Cauter, E. (1996) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.81.7.2468 · Cited by 951 · see citing works
Genetic factors, perceived chronic stress, and the free cortisol response to awakening
Wüst, S., Federenko, I. S., Hellhammer, D. H., & Kirschbaum, C. (2000) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(00)00021-4 · Cited by 642 · see citing works
Characterization of the normal temporal pattern of plasma corticosteroid levels.
KRIEGER, D. T., ALLEN, W., RIZZO, F., & KRIEGER, H. P. (1971) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-32-2-266 · Cited by 549 · see citing works
Kudielka, B. M., Broderick, J. E., & Kirschbaum, C. (2003) · Psychosomatic Medicine · doi:10.1097/01.psy.0000058374.50240.bf · Cited by 489 · see citing works
Stone, A. A., Schwartz, J. E., Smyth, J. M., Kirschbaum, C., Cohen, S., Hellhammer, D. H., & Grossman, S. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(00)00057-3 · Cited by 347 · see citing works
Kiess, W., Meidert, A. S., Dressendörfer, R. A., Schriever, K., Kessler, U., Köunig, A., Hp, S., & Strasburger, C. J. (1995) · Pediatric Research · doi:10.1203/00006450-199504000-00020 · Cited by 319 · see citing works
Emotion, Development, and Self-Organization
(2000) · Cambridge University Press eBooks · doi:10.1017/cbo9780511527883 · Cited by 314 · see citing works
Adam, E. K. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(00)00045-7 · Cited by 300 · see citing works
Age of appearance of circadian rhythm in salivary cortisol values in infancy.
Price, D., Close, G. C., & Fielding, B. (1983) · Archives of Disease in Childhood · doi:10.1136/adc.58.6.454 · Cited by 236 · see citing works
Diurnal and Ultradian Rhythms in Human Endocrine Function: A Minireview
Cauter, E. V. (2008) · Hormone Research · doi:10.1159/000181794 · Cited by 231 · see citing works
GRAY, C. H., & Bacharach, A. L. (1979) · Medical Entomology and Zoology · Cited by 165 · see citing works
Twin study of the 24-h cortisol profile: evidence for genetic control of the human circadian clock
Linkowski, P., Onderbergen, A. V., Kerkhofs, M., Bosson, D., Mendlewicz, J., & Cauter, E. V. (1993) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1993.264.2.e173 · Cited by 163 · see citing works
Developmental Change in Infants' Responses to Stress
Lewis, M., & Ramsay, D. S. (1995) · Child Development · doi:10.1111/j.1467-8624.1995.tb00896.x · Cited by 158 · see citing works
White, B. P., Gunnar, M. R., Larson, M. C., Donzella, B., & Barr, R. G. (2000) · Child Development · doi:10.1111/1467-8624.00196 · Cited by 141 · see citing works
Longitudinal evaluation of the development of salivary cortisol circadian rhythm in infancy
Santiago, L. B., Jorge, S. M., & Moreira, A. C. (1996) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1996.645466.x · Cited by 138 · see citing works
Spangler, G. (1991) · Early Human Development · doi:10.1016/0378-3782(91)90116-k · Cited by 131 · see citing works
Endocrine and other biological rhythms
Cauter, E. V. (2001) · Medical Entomology and Zoology · Cited by 116 · see citing works
Developmental Change in Infants' Responses to Stress
Lewis, M., & Ramsay, D. S. (1995) · Child Development · doi:10.2307/1131941 · Cited by 106 · see citing works
Antonini, S. R. R., Jorge, S. M., & Moreira, A. C. (2000) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2000.tb00561.x · Cited by 98 · see citing works
Larson, M. C., Gunnar, M. R., & Hertsgaard, L. A. (1991) · Child Development · doi:10.1111/j.1467-8624.1991.tb01537.x · Cited by 97 · see citing works
Use of Salivary Cortisol Measurements in Young Infants: A Note of Caution
Magnano, C. L., Diamond, E. J., & Gardner, J. M. (1989) · Child Development · doi:10.1111/j.1467-8624.1989.tb03541.x · Cited by 95 · see citing works
Use of Salivary Cortisol Measurements in Young Infants: A Note of Caution
Magnano, C. L., Diamond, E. J., & Gardner, J. M. (1989) · Child Development · doi:10.2307/1130784 · Cited by 75 · see citing works
Postnatal Development of Circadian Rhythm in Serum Cortisol Levels in Children
Onishi, S., Miyazawa, G., Nishimura, Y., Sugiyama, S., Yamakawa, T., Inagaki, H., Katoh, T., Itoh, S., & lsobe, K. (1983) · PEDIATRICS · doi:10.1542/peds.72.3.399 · Cited by 68 · see citing works
de Weerth, C., & van Geert, P. L. C. (2002) · Infant Behavior and Development · doi:10.1016/s0163-6383(02)00141-8 · Cited by 66 · see citing works
Intraindividual variability in infant behavior.
de Weerth, C., van Geert, P. L. C., & Hoijtink, H. J. A. (1999) · Developmental Psychology · doi:10.1037//0012-1649.35.4.1102 · Cited by 65 · see citing works
Larson, M. C., Gunnar, M. R., & Hertsgaard, L. A. (1991) · Child Development · doi:10.2307/1131009 · Cited by 63 · see citing works
The determination of cortisol in human plasma: Evaluation and comparison of seven assays
Thijssen, J. H. H., van den Berg, J. H. M., Adlercreutz, H., Gijzen, A. H. J., de Jong, F. H., Meijer, J. C., & Moolenaar, A. J. (1980) · Clinica Chimica Acta · doi:10.1016/0009-8981(80)90183-7 · Cited by 61 · see citing works
Diurnal Variation of Plasma Cortisol Levels in Infancy
Mantagos, Moustogiannis, A., & Vagenakis, A. G. (1998) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem.1998.11.4.549 · Cited by 54 · see citing works
Intraindividual variability in infant behavior.
de Weerth, C., van Geert, P. L. C., & Hoijtink, H. (1999) · Developmental Psychology · doi:10.1037/0012-1649.35.4.1102 · Cited by 48 · see citing works
Hertsgaard, L. A., Gunnar, M. R., Larson, M., Brodersen, L., & Lehman, H. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250503 · Cited by 39 · see citing works
Mindell, J. A. A. (1997) · Cited by 20 · see citing works
Neonatal Stimulation and Maturation of the 24-Hour Adrenocortical Rhythm
Ader, R. (1975) · Progress in brain research · doi:10.1016/s0079-6123(08)63690-0 · Cited by 9 · see citing works
Emotion-related behaviors in infants: a longitudinal study of patterns and variability
de Weerth, C. (1998) · Cited by 9 · see citing works
The Dynamics of Emotion-Related Behaviors in Infancy
de Weerth, C., & van Geert, P. L. C. (2000) · Cambridge University Press eBooks · doi:10.1017/cbo9780511527883.014 · Cited by 7 · see citing works
Flagged first, then by citations
2 of the 40 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The Adaptive Calibration Model of stress responsivity
Del Giudice, M., Ellis, B. J., & Shirtcliff, E. A. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.11.007 · Cited by 1,373 · see citing works
“…2005); likewise, prenatal exposure to maternal stress hormones is linked to temperamental reactivity and stress physiology, likely through epigenetic regulation of gene expression (de Weerth et al., 2003; Gutteling et al., 2005; Möhler et al., 2006; O’Connor et al., 2005; Poggi Davis et al., 2010).”
Prenatal depression effects on the fetus and newborn: a review
Field, T., Diego, M., & Hernandez-Reif, M. (2006) · Infant Behavior and Development · doi:10.1016/j.infbeh.2006.03.003 · Cited by 592 · see citing works
Measuring cortisol in serum, urine and saliva—Are our assays good enough?
El-Farhan, N., Rees, D. A., & Evans, C. (2017) · Annals of Clinical Biochemistry: International Journal of Laboratory Medicine · doi:10.1177/0004563216687335 · Cited by 395 · see citing works
“In contrast, studies in saliva have demonstrated a discernible circadian rhythm in full-term neonates at 1 month of age,(142) albeit with significant intra and interindividual variability in terms of how early the rhythm appears and how persistent it is once it has appeared.(141,142,144) Further study is now needed to…”
ResultShirtcliff, E. A., Allison, A. L., Armstrong, J. M., Slattery, M. J., Kalin, N. H., & Essex, M. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20607 · Cited by 230 · see citing works
Prenatal mood disturbance predicts sleep problems in infancy and toddlerhood
O’Connor, T. G., Caprariello, P. A., Blackmore, E. R., Gregory, A. M., Glover, V. A. S., & Fleming, P. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2006.08.006 · Cited by 219 · see citing works
“First, several studies report a link between the establishment of a diurnal pattern in cortisol and sleeping through the night in infancy(44).”
BackgroundChildren's elevated cortisol levels at daycare: A review and meta-analysis
Vermeer, H. J., & van IJzendoorn, M. H. (2006) · Early Childhood Research Quarterly · doi:10.1016/j.ecresq.2006.07.004 · Cited by 216 · see citing works
“For instance, napping (e.g., Watamura et al., 2004), respiratory illness, and feeding (De Weerth et al., 2003) have been found to influence the HPA axis.”
BackgroundResultNeuroendocrine dysregulation following early social deprivation in children
Fries, A. B. W., Shirtcliff, E. A., & Pollak, S. D. (2008) · Developmental Psychobiology · doi:10.1002/dev.20319 · Cited by 192 · see citing works
Ruttle, P. L., Shirtcliff, E. A., Serbin, L. A., Fisher, D. B., Stack, D. M., & Schwartzman, A. E. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.10.015 · Cited by 188 · see citing works
“Although a normal pattern of diurnal cortisol production is typically established within the first year of life (de Weerth et al., 2003), the HPA axis continues to develop into early childhood and may continue to be sensitive to external influences during the formative early years.”
Bailey, D., Colantonio, D., Kyriakopoulou, L. G., Cohen, A. H., Chan, M. K., Armbruster, D., & Adeli, K. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2013.204222 · Cited by 187 · see citing works
Do bacteria shape our development? Crosstalk between intestinal microbiota and HPA axis
de Weerth, C. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.09.016 · Cited by 181 · see citing works
“Infants are born without a circadian rhythm in cortisol and they normally acquire it within the first six months (de Weerth et al., 2003; Lupien et al., 2009).”
Maternal prenatal stress and cortisol reactivity to stressors in human infants
Tollenaar, M. S., Beijers, R., Jansen, J., Riksen‐Walraven, J. M., & de Weerth, C. (2010) · Stress · doi:10.3109/10253890.2010.499485 · Cited by 171 · see citing works
“The HPA axis starts to develop prenatally and fully matures after birth, including the development of a diurnal cortisol rhythm in the first year of life (De Weerth et al. 2003; Lupien et al. 2009).”
BackgroundGenetic forms of hypopituitarism and their manifestation in the neonatal period
Alatzoglou, K. S., & Dattani, M. (2009) · Early Human Development · doi:10.1016/j.earlhumdev.2009.08.057 · Cited by 145 · see citing works
“During the first six months of life the circadian rhythm of cortisol excretion has not yet been established, baseline morning versus evening samples are not conclusive and treatment with steroids complicates the interpretation of results [93].”
BackgroundEpidemiology of Stress and Asthma: From Constricting Communities and Fragile Families to Epigenetics
Wright, R. J. (2010) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2010.09.011 · Cited by 145 · see citing works
“, diurnal rhythm, coritsol awakening response (CAR)] (95,101).”
BackgroundInfluentialTegethoff, M., Pryce, C. R., & Meinlschmidt, G. (2009) · Endocrine Reviews · doi:10.1210/er.2008-0014 · Cited by 139 · see citing works
“, whether basal hpa function in newborns was assessed under fasting conditions, the stage of perinatal remodeling of the adrenocortex, diurnal variability of hpa activity (203)].”
BackgroundGrant, K., McMahon, C. A., Austin, M., Reilly, N. M., Leader, L. R., & Ali, S. (2009) · Developmental Psychobiology · doi:10.1002/dev.20397 · Cited by 140 · see citing works
Salivary cortisol and cortisone in the clinical setting
Blair, J., Adaway, J., Keevil, B., & Ross, R. (2017) · Current Opinion in Endocrinology, Diabetes & Obesity · doi:10.1097/med.0000000000000328 · Cited by 138 · see citing works
Luijk, M. P. C. M., Saridjan, N., Tharner, A., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Jaddoe, V. W. V., Hofman, A., Verhulst, F. C., & Tiemeier, H. (2010) · Developmental Psychobiology · doi:10.1002/dev.20446 · Cited by 135 · see citing works
Attachment in Toddlers with Autism and Other Developmental Disorders
Naber, F. B. A., Willemsen‐Swinkels, S. H. N., Buitelaar, J. K., Bakermans‐Kranenburg, M. J., van IJzendoorn, M. H., Dietz, C., van Daalen, E., & van Engeland, H. (2006) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-006-0255-2 · Cited by 134 · see citing works
Self-citationTu, M. T., GRUNAU, R. E., Petrie, J., Haley, D. W., Weinberg, J., & Whitfield, M. F. (2007) · Developmental Psychobiology · doi:10.1002/dev.20204 · Cited by 131 · see citing works
Dobrova‐Krol, N. A., van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Cyr, C. P., & Juffer, F. (2008) · Infant Behavior and Development · doi:10.1016/j.infbeh.2008.04.001 · Cited by 128 · see citing works
The Dynamic Development of Gender Variability
Fausto‐Sterling, A. (2012) · Journal of Homosexuality · doi:10.1080/00918369.2012.653310 · Cited by 124 · see citing works
Egliston, K.-A., McMahon, C. A., & Austin, M. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.10.003 · Cited by 123 · see citing works
Marceau, K., Ruttle, P. L., Shirtcliff, E. A., Essex, M. J., & Susman, E. J. (2014) · Developmental Psychobiology · doi:10.1002/dev.21214 · Cited by 120 · see citing works
“Researchers generally agree that there is significant individual variability in when diurnal patterns emerge and studies vary considerably on when a reliable diurnal rhythm can be detected, generally suggesting between 2 and 9 months of age (de Weerth et al., 2003; Kiess et al., 1995).”
BackgroundCong, X. S., Ludington‐Hoe, S. M., & Walsh, S. J. (2010) · Biological Research For Nursing · doi:10.1177/1099800410385839 · Cited by 118 · see citing works
Sleep quality, cortisol levels, and behavioral regulation in toddlers
Scher, A., Hall, W. A., Zaidman‐Zait, A., & Weinberg, J. (2009) · Developmental Psychobiology · doi:10.1002/dev.20410 · Cited by 115 · see citing works
“Intraindividual variability in cortisol levels was noted by de Weerth, Zijl, and Buitelaar (2003), who studied the early maturation of the cortisol circadian rhythm and highlighted its links with sleep.”
BackgroundDevelopment of the circadian system in early life: maternal and environmental factors
Wong, S. D., Wright, K. P., Spencer, R. L., Vetter, C., Hicks, L. M., Jenni, O. G., & LeBourgeois, M. K. (2022) · Journal of PHYSIOLOGICAL ANTHROPOLOGY · doi:10.1186/s40101-022-00294-0 · Cited by 106 · see citing works
Letourneau, N., Stewart, M., Dennis, C.-L., Hegadoren, K., Duffett-Leger, L., & Watson, B. (2011) · International Journal of Mental Health Nursing · doi:10.1111/j.1447-0349.2010.00736.x · Cited by 97 · see citing works
Development of Salivary Cortisol Circadian Rhythm and Reference Intervals in Full-Term Infants
Ivars, K., Nelson, N., Theodorsson, A., Theodorsson, E., Ström, J. O., & Mörelius, E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129502 · Cited by 87 · see citing works
“Price and coworkers analyzed their data with parametric tests and defined CCR as occurring when the morning cortisol level was 2 nmol/L higher than evening cortisol level [4, 9].”
MethodResultNeu, M., Goldstein, M., Gao, D., & Laudenslager, M. L. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2006.04.003 · Cited by 87 · see citing works
“[21] reported an association between the development of circadian sleep cycle and the development of a stable diurnal circadian cortisol pattern.”
BackgroundResultCortisol in the first year of life: Normative values and intra-individual variability
Tollenaar, M. S., Jansen, J., Beijers, R., Riksen‐Walraven, J. M., & de Weerth, C. (2010) · Early Human Development · doi:10.1016/j.earlhumdev.2009.12.003 · Cited by 87 · see citing works
“While several studies have examined the development of circadian rhythms (see [3]) or reactivity to mild stressors (see [4,5]), a full understanding of the normative development of basal cortisol levels has not yet been achieved.”
BackgroundGranger, D. A., Blair, C., Willoughby, M., Kivlighan, K. T., Hibel, L. C., Fortunato, C. K., & Wiegand, L. E. (2007) · Developmental Psychobiology · doi:10.1002/dev.20247 · Cited by 83 · see citing works
Human milk as “chrononutrition”: implications for child health and development
Hahn‐Holbrook, J., Saxbe, D., Bixby, C., Steele, C., & Glynn, L. M. (2019) · Pediatric Research · doi:10.1038/s41390-019-0368-x · Cited by 84 · see citing works
Primary adrenal insufficiency in children: Diagnosis and management
Kırkgöz, T., & Güran, T. (2018) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2018.05.010 · Cited by 80 · see citing works
Assessing stress reactivity indexed via salivary cortisol in preschool-aged children
Kryski, K. R., Smith, H. J., Sheikh, H. I., Singh, S. M., & Hayden, E. P. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.02.003 · Cited by 77 · see citing works
“Also, cortisol varies throughout the day, with peak levels being reached upon awakening, and lowest levels found after sleep onset (deWeerth et al., 2003; Gunnar and Talge, 2008).”
BackgroundEpigenetic dynamics in infancy and the impact of maternal engagement
Krol, K. M., Moulder, R. G., Jr., Lillard, T. S., Großmann, T., & Connelly, J. J. (2019) · Science Advances · doi:10.1126/sciadv.aay0680 · Cited by 75 · see citing works
Zietlow, A., Nonnenmacher, N., Reck, C., Ditzen, B., & Müller, M. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.02179 · Cited by 77 · see citing works
“Even though the circadian rhythm of the HPA-axis is not fully developed during the first months postpartum (de Weerth et al., 2003; Bright et al., 2012) salivary cortisol can be seen as a valid marker for infant stress reactivity in early infancy (Jansen et al., 2010).”
BackgroundA preliminary study of gut microbiome variation and HPA axis reactivity in healthy infants
Rosin, S., Xia, K., Azcarate-Peril, M. A., Carlson, A. L., Propper, C. B., Thompson, A. L., Grewen, K., & Knickmeyer, R. C. (2021) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.105046 · Cited by 74 · see citing works
Early-life origin of adult insomnia: does prenatal–early-life stress play a role?
Palagini, L., Drake, C. L., Gehrman, P., Meerlo, P., & Riemann, D. W. (2015) · Sleep Medicine · doi:10.1016/j.sleep.2014.10.013 · Cited by 72 · see citing works
Infant hair cortisol: associations with salivary cortisol and environmental context
Flom, M., John, A. M. S., Meyer, J. S., & Tarullo, A. R. (2016) · Developmental Psychobiology · doi:10.1002/dev.21449 · Cited by 71 · see citing works
Children’s cortisol levels and quality of child care provision
Sims, M., Guilfoyle, A. M., & Parry, T. (2006) · Child Care Health and Development · doi:10.1111/j.1365-2214.2006.00632.x · Cited by 70 · see citing works
Provenzi, L., Giusti, L., & Montirosso, R. (2016) · Developmental Review · doi:10.1016/j.dr.2016.07.001 · Cited by 70 · see citing works
Azar, R., Paquette, D., Zoccolillo, M., Baltzer, F., & Tremblay, R. E. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.11.009 · Cited by 66 · see citing works
A comparison of pain measures in newborn infants after cardiac surgery
Franck, L. S., Ridout, D. A., Howard, R. F., Peters, J., & Honour, J. W. (2011) · Pain · doi:10.1016/j.pain.2011.03.017 · Cited by 67 · see citing works
“The development of rhythmicity in cortisol is highly individual in the young infant [7] and we believe that any emerging cycle would have been extinguished by the effects of illness, surgical stress, and intensive care unit setting.”
BackgroundCoregulation in Salivary Cortisol During Maternal Holding of Premature Infants
Neu, M., Laudenslager, M. L., & Robinson, J. L. (2008) · Biological Research For Nursing · doi:10.1177/1099800408327789 · Cited by 65 · see citing works
Pathways Associating Childhood Trauma to the Neurobiology of Schizophrenia.
Ruby, E., Polito, S., McMahon, K. L., Gorovitz, M., Corcoran, C. M., & Malaspina, D. (2014) · PubMed · Cited by 65 · see citing works
Nonclassic adrenal hyperplasia
Speiser, P. (2008) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-008-9097-x · Cited by 62 · see citing works
“Interestingly, infants do not exhibit diurnal variations in adrenal cortical hormone levels at birth, but develop this pattern within the first year of life [ 11 ].”
BackgroundDevelopment of the cortisol circadian rhythm in the light of stress early in life
Simons, S. S. H., Beijers, R., Cillessen, A. H. N., & de Weerth, C. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.08.024 · Cited by 61 · see citing works
“During the first year of life infants acquire the normative cortisol circadian rhythm (e.g., Spangler, 1991; De Weerth and van Geert, 2002; De Weerth et al., 2003; Custodio et al., 2007).”
BackgroundComparisons between salivary cortisol levels in six-months-olds and their parents
Stenius, F., Theorell, T., Lilja, G., Scheynius, A., Alm, J. S., & Lindblad, F. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.12.001 · Cited by 61 · see citing works
“…phase, when the mothers were The diurnal rhythm of the HPA-axis seems to be established during the first months of life even though a delay of up to nine months of age has been reported and individual differences may be prominent as to time and stability (for a review, see de Weerth et al., 2003).”
Seizure occurrence and the circadian rhythm of cortisol: a systematic review
van Campen, J. S., Valentijn, F. A., Jansen, F. E., Joëls, M., & Braun, K. P. J. (2015) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2015.04.071 · Cited by 57 · see citing works
“The circadian cortisol rhythm in children develops between 1month and 2 years of age [15–26].”
BackgroundA time to be stressed? Time perspectives and cortisol dynamics among healthy adults
Olivera-Figueroa, L. A., Juster, R., Morin-Major, J.-K., Marin, M., & LUPIEN, S. J. (2015) · Biological Psychology · doi:10.1016/j.biopsycho.2015.09.002 · Cited by 56 · see citing works
Shiftwork Duration and the Awakening Cortisol Response Among Police Officers
Wirth, M. D., Burch, J. B., Violanti, J. M., Burchfiel, C. M., Fekedulegn, D. B., Andrew, M. E., Zhang, H., Miller, D. B., Hébert, J. R., & Vena, J. E. (2011) · Chronobiology International · doi:10.3109/07420528.2011.573112 · Cited by 56 · see citing works
“The cortisol awakening response (CAR) is characterized by a 40–75% increase of salivary cortisol levels, with maximum values occurring about 30 min after awakening (de Weerth et al., 2003; Fries et al., 2009; Kudielka et al., 2006).”
Backgroundde Weerth, C., Buitelaar, J. K., & Beijers, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.07.014 · Cited by 55 · see citing works
“Cortisol was determined with an in house competitive RIA (see below), which is insensitive to breast milk and formula contamination (de Weerth et al., 2003a).”
Self-citationStress measures in tail biters and bitten pigs in a matched case-control study
Munsterhjelm, C., Brunberg, E., Heinonen, M., Keeling, L. J., & Valros, A. (2013) · Animal Welfare · doi:10.7120/09627286.22.3.331 · Cited by 56 · see citing works
The dawn phenomenon and the Somogyi effect - two phenomena of morning hyperglycaemia.
Rybicka, M., Krysiak, R. G., & Okopień, B. (2011) · PubMed · Cited by 55 · see citing works
Liu, C. H., Snidman, N. C., Leonard, A., Meyer, J. S., & Tronick, E. (2016) · Developmental Psychobiology · doi:10.1002/dev.21394 · Cited by 54 · see citing works
Correlation between maternal and infant cortisol varies by breastfeeding status
Neelon, S. E. B., Stroo, M., Mayhew, M., Maselko, J., & Hoyo, C. (2015) · Infant Behavior and Development · doi:10.1016/j.infbeh.2015.06.005 · Cited by 54 · see citing works
Cortisol circadian rhythms and stress responses in infants at risk of allergic disease
Ball, T. M., Anderson, D., Minto, J., & Halonen, M. J. (2006) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2005.11.009 · Cited by 53 · see citing works
Pearson, J., Tarabulsy, G. M., & Bussières, È.-L. (2015) · Infant Behavior and Development · doi:10.1016/j.infbeh.2015.04.004 · Cited by 51 · see citing works
Is physiological glucocorticoid replacement important in children?
Porter, J., Blair, J., & Ross, R. J. (2017) · Archives of Disease in Childhood · doi:10.1136/archdischild-2015-309538 · Cited by 50 · see citing works
Sheikh, H. I., Joanisse, M. F., Mackrell, S. V. M., Kryski, K. R., Smith, H. J., Singh, S. M., & Hayden, E. P. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.08.013 · Cited by 47 · see citing works
“…for use with older children and was designed to emphasize social evaluation under motivated and uncontrollable circumstances,whichhas been shown to elicit large cortisol responses in both adults (Dickerson and Kemeny, 2004; Magnano et al., 1989) and preschool-aged children (Gunnar et al., 2009).”
BackgroundFrigerio, A., Ceppi, E., Rusconi, M., Giorda, R., Raggi, M. E., & Fearon, P. R. M. (2009) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2009.02126.x · Cited by 49 · see citing works
Blunted Stress Response in Small for Gestational Age Neonates
Schäffer, L., Müller-Vizentini, D., Burkhardt, T., Rauh, M., Ehlert, U., & Beinder, E. (2009) · Pediatric Research · doi:10.1203/pdr.0b013e318191fb44 · Cited by 49 · see citing works
Glover, V. A. S., Miles, R., Matta, S., Modi, N., & Stevenson, J. (2005) · Pediatric Research · doi:10.1203/01.pdr.0000185132.38209.73 · Cited by 48 · see citing works
“Although the blood samples were collected at varying times of day, preterm infants of this postnatal age, unlike adults, do not exhibit diurnal variation in cortisol production (26).”
BackgroundCortisol: Circadian Rhythm and Response to a Stressor
Elverson, C. A., & Wilson, M. E. (2005) · Newborn and Infant Nursing Reviews · doi:10.1053/j.nainr.2005.09.002 · Cited by 47 · see citing works
de Bruijn, A. T. C. E., van Bakel, H. J. A., Wijnen, H. A. A., Pop, V. J. M., & van Baar, A. L. (2009) · Developmental Psychobiology · doi:10.1002/dev.20393 · Cited by 48 · see citing works
Tobias Stalder, A., Bäumler, D., Miller, R. E., Alexander, N., Kliegel, M., & Kirschbaum, C. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.07.015 · Cited by 48 · see citing works
“Here, most evidence suggests that the development of a stable circadian pattern of cortisol secretion tends to fall into the first half year of life (Price et al., 1983; Spangler, 1991; Antonini et al., 2000), even though with considerable individual differences (De Weerth et al., 2003).”
Sheikh, H. I., Kryski, K. R., Smith, H. J., Hayden, E. P., & Singh, S. M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.056 · Cited by 46 · see citing works
“All visits began between 12:00 pm and 3:30 pm to minimize the effects of diurnal variation on cortisol samples (de Weerth et al., 2003; Donzella et al., 2008).”
Iwata, O., Okamura, H., Saitsu, H., Saikusa, M., Kanda, H., Eshima, N., Iwata, S., Maeno, Y. V., & Matsuishi, T. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2750 · Cited by 43 · see citing works
Do infants show a cortisol awakening response?
Bright, M. A., Granger, D. A., & Frick, J. E. (2011) · Developmental Psychobiology · doi:10.1002/dev.20617 · Cited by 40 · see citing works
Custódio, R. J., Martinelli, C. E., Milani, S. S., Simões, A. L., de Castro, M., & Moreira, A. C. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02706.x · Cited by 40 · see citing works
The use of cortisol for the objective assessment of stress in animals: Pros and cons
Hart, K. A. (2012) · The Veterinary Journal · doi:10.1016/j.tvjl.2012.03.016 · Cited by 37 · see citing works
Shared Dysregulation of Homeostatic Brain-Body Pathways in Depression and Type 2 Diabetes
Hoogendoorn, C. J., Delgado, J. F. R., & Gonzalez, J. S. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0923-y · Cited by 38 · see citing works
Moreira, A. C., Antonini, S. R. R., & de Castro, M. (2018) · European Journal of Endocrinology · doi:10.1530/eje-18-0102 · Cited by 37 · see citing works
Approaches to Salivary Cortisol Collection and Analysis in Infants
Tryphonopoulos, P. D., Letourneau, N. L., & Azar, R. (2013) · Biological Research For Nursing · doi:10.1177/1099800413507128 · Cited by 38 · see citing works
“…attributed to a number of factors that have impacted studies on the topic such as differing working definitions of circadian rhythm, inconsistent sampling times, infant exposure to antenatal steroids, and variation in data collection procedures and methods of data analysis (de Weerth et al., 2003).”
BackgroundTollenaar, M. S., Beijers, R., Jansen, J., Riksen‐Walraven, J. M., & de Weerth, C. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.017 · Cited by 36 · see citing works
Maternal depression and infant daytime cortisol
Azak, S., Murison, R. C. C., Wentzel‐Larsen, T., Smith, L., & Gunnar, M. R. (2012) · Developmental Psychobiology · doi:10.1002/dev.21033 · Cited by 34 · see citing works
Influence of acoustic stimulation on the circadian and ultradian rhythm of premature infants
Dorn, F., Wirth, L., Gorbey, S., Wege, M., Zemlin, M., Maier, R. F., & Lemmer, B. (2014) · Chronobiology International · doi:10.3109/07420528.2014.948183 · Cited by 34 · see citing works
“…shown that the wide variance of the age of appearance of the circadian rhythm is due to different analytical working definitions and low sample Chronobiology International frequencies (Antonini et al., 2000; Krieger et al., 1971; Price et al., 1983; Santiago et al., 1996; de Weerth et al., 2003).”
BackgroundIntervention Effects on Morning and Stimulated Cortisol Responses among Toddlers in Foster Care
Nelson, E. M. M., & Spieker, S. J. (2013) · Infant Mental Health Journal · doi:10.1002/imhj.21382 · Cited by 35 · see citing works
Colombo, J. A., Carlson, S. E., Algarín, C. R., Reyes, S., Chichlowski, M., Harris, C. L., Wampler, J. L., Peirano, P. D., & Berseth, C. L. (2020) · Pediatric Research · doi:10.1038/s41390-020-1044-x · Cited by 34 · see citing works
Transforming growth factor beta (TGF-B) stimulation of angiogenesis: an electron microscopic study.
Phillips, G. D., Whitehead, R. A., Stone, A. M., Ruebel, M. W., Goodkin, M. L., & Knighton, D. R. (1993) · PubMed · Cited by 34 · see citing works
Albers, E. M., Beijers, R., Riksen-Walraven, J., Sweep, F. C., & de Weerth, C. (2016) · Stress · doi:10.3109/10253890.2015.1089230 · Cited by 33 · see citing works
“Infants acquire the cortisol circadian rhythm during their first year of life (Custodio et al., 2007; de Weerth & van Geert, 2002; de Weerth et al., 2003).”
BackgroundZhang, B. (2017) · PubMed Central · doi:10.13918/j.issn.2095-8137.2017.002 · Cited by 31 · see citing works
Hibel, L. C., Trumbell, J. M., & Mercado, E. (2013) · Early Human Development · doi:10.1016/j.earlhumdev.2013.11.007 · Cited by 31 · see citing works
“Infants develop a diurnal rhythm that consists of relatively high morning and low evening cortisol levels by three months of age [14,15].”
BackgroundMaternal emotional availability at bedtime and infant cortisol at 1 and 3months
Philbrook, L. E., Hozella, A. C., Kim, B. R., Jian, N., Shimizu, M., & Teti, D. M. (2014) · Early Human Development · doi:10.1016/j.earlhumdev.2014.05.014 · Cited by 31 · see citing works
“Many infants did not yet show a circadian pattern at both ages, however, supporting de Weerth and colleagues’ (8) finding that there is substantial interindividual variability in the emergence of a diurnal rhythm in cortisol.”
BackgroundMethodInfluentialPerinatal Programming of Circadian Clock-Stress Crosstalk
Astiz, M., & Oster, H. (2018) · Neural Plasticity · doi:10.1155/2018/5689165 · Cited by 28 · see citing works
Childbirth complications affect young infants’ behavior
de Weerth, C., & Buitelaar, J. K. (2007) · European Child & Adolescent Psychiatry · doi:10.1007/s00787-007-0610-7 · Cited by 28 · see citing works
“This did not affect cortisol levels, as at this age the circadian rhythm is not present [5].”
BackgroundResultSelf-citationHalal, C. S. E., Bassani, D. G., Santos, I. S., Tovo‐Rodrigues, L., Del‐Ponte, B., da Silveira, M. F., Bertoldi, A. D., Barros, F. C., & Nunes, M. L. (2020) · Journal of Sleep Research · doi:10.1111/jsr.13047 · Cited by 27 · see citing works
Circle(s) of Life: The Circadian Clock from Birth to Death
Olejniczak, I., Pilorz, V., & Oster, H. (2023) · Biology · doi:10.3390/biology12030383 · Cited by 27 · see citing works
Isaksson, J., Lindblad, F., Valladares, E., & Högberg, U. (2015) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2015.09.016 · Cited by 27 · see citing works
Neonatal Hypopituitarism: Approaches to Diagnosis and Treatment
Kurtoğlu, S., Özdemi̇r, A., & Hatipoğlu, N. (2019) · Journal of Clinical Research in Pediatric Endocrinology · doi:10.4274/jcrpe.galenos.2018.2018.0036 · Cited by 26 · see citing works
“Thus, cortisol should be measured every hour of the day instead of only in the morning (34).”
BackgroundAssociations between bedtime and nighttime parenting and infant cortisol in the first year
Philbrook, L. E., & Teti, D. M. (2016) · Developmental Psychobiology · doi:10.1002/dev.21442 · Cited by 26 · see citing works
Gao, J., Xiao, H., Li, J., Guo, X., Cai, W., & Li, D. (2019) · Nutrients · doi:10.3390/nu11071699 · Cited by 26 · see citing works
“Cortisolcan affect insulin production and glucose metabolism and it can cause insulin resistance [45,46].”
BackgroundGlucocorticoid treatment and adrenal suppression in children: current view and open issues
Improda, N., Chioma, L., Capalbo, D., Bizzarri, C., & Salerno, M. (2024) · Journal of Endocrinological Investigation · doi:10.1007/s40618-024-02461-9 · Cited by 27 · see citing works
Tamayo‐Ortiz, M., Téllez‐Rojo, M. M., Wright, R. J., Coull, B. A., & Wright, R. O. (2016) · Environmental Health · doi:10.1186/s12940-016-0124-1 · Cited by 25 · see citing works
Neuroendocrine and immune pathways from pre- and perinatal stress to substance abuse
Horn, S. R. G.-V., Roos, L. E., Berkman, E. T., & Fisher, P. A. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.09.004 · Cited by 24 · see citing works
Shiftwork and Diurnal Salivary Cortisol Patterns Among Police Officers
Charles, L. E., Fekedulegn, D. B., Burchfiel, C. M., Hartley, T. A., Andrew, M. E., Violanti, J. M., & Miller, D. B. (2016) · Journal of Occupational and Environmental Medicine · doi:10.1097/jom.0000000000000729 · Cited by 23 · see citing works
Effects of Fatigue and Sleep Deprivation on Microvascular Anastomoses
Başaran, K., Mercan, E. S., & Aygıt, A. (2015) · The Journal of craniofacial surgery (Print) · doi:10.1097/scs.0000000000001719 · Cited by 23 · see citing works
“it is responsible for activating the metabolism and inducing glucose and protein release.(23) The maximum sympathomimetic effect of cortisol during the morning surgery (group III, 09.”
BackgroundMehler, K., Ulbrich, L., Börner, S., Joachim, A., Becker, I., Roth, B., & Hünseler, C. (2015) · Early Human Development · doi:10.1016/j.earlhumdev.2015.01.011 · Cited by 22 · see citing works
“infants admitted into the hospital [33], immunizations of late preterm infants and control infants were scheduled at parents' discretion and performed between 8:00 a.”
Thomas, K. A., Burr, R. L., & Spieker, S. J. (2016) · Sleep and Biological Rhythms · doi:10.1007/s41105-015-0046-2 · Cited by 22 · see citing works
Holochwost, S. J., Winebrake, D., Brown, E. D., Happaney, K. R., Wagner, N. J., & Mills-Koonce, R. (2022) · Journal of Cognition and Development · doi:10.1080/15248372.2022.2160721 · Cited by 22 · see citing works
- Authors
- de Weerth, C., Zijl, R. H., & Buitelaar, J. K.
- Affiliations
- University Medical Center Utrecht (NL)
- Radboud University Nijmegen (NL)
- ORCID
- Buitelaar, Jan K
- Venue
- Early Human Development
- Publisher
- Elsevier BV
- Published
- 2003-08
- Volume
- 73
- Issue
- 1-2
- Pages
- 39-52
- ISSN
- 0378-3782 (ISSN-L)
- OpenAlex
- W2112583133
- Cited by
- 248
- References
- 40
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 12 · 2023: 13 · 2022: 12 · 2021: 9 · 2020: 15 · 2019: 12 · 2018: 8 · 2017: 15 · 2016: 18 · 2015: 22 · 2014: 17 · 2013: 14 · 2012: 10
- FWCI
- 1.76
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Early Human Development (publishedVersion)
- PubMed (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- cortisol, circadian rhythm, diurnal cycle, infancy, hypothalamic-pituitary-adrenal axis, salivary cortisol, sleep-wake cycle, age of onset, within-person variability, multilevel analysis
- MeSH terms
- Adult, Biological Clocks, Circadian Rhythm, Female, Humans, Hydrocortisone, Infant, Male, Pregnancy, Saliva, Sleep, Models, Statistical
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review