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The Journal of Clinical Endocrinology & Metabolism Vol. 82, No. 2 536-540
Copyright © 1997 by The Endocrine Society

Pediatric Endocrinology

Circadian Cortisol Rhythms in Healthy Boys and Girls: Relationship with Age, Growth, Body Composition, and Pubertal Development1

Urban Knutsson, Jovanna Dahlgren, Claude Marcus, Sten Rosberg, Mikael Brönnegård, Pontus Stierna and Kerstin Albertsson-Wikland

Department of Otorhinolaryngology (U.K., P.S.) and the Unit for Endocrinology (C.M., M.B.), Department of Pediatrics, Karolinska Institute, Huddinge University Hospital, Stockholm; and International Pediatric Growth Research Center, Department of Pediatrics (J.D., S.R., K.A.-W.), University of Göteborg, Göteborg, Sweden

Address all correspondence and requests for reprints to: Dr. Kerstin Albertsson-Wikland, University of Goteborg, Department of Pediatrics, International Pediatric Growth Research Center, East Hospital, S-416 85 Goteborg, Sweden. E-mail: Kerstin.Albertsson{at}pediat.gu.se


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
To provide basic information on the normal functioning of the hypothalamus-pituitary-adrenal axis in relation to pubertal development, growth (weight and height), body composition, and gender and to obtain reference data for serum cortisol concentrations in children, we investigated the basal circadian rhythm of serum cortisol in a group of 235 healthy children (162 boys and 73 girls). The age range was between 2.2–18.5 yr. Serum cortisol was analyzed from venous blood samples taken at 1400, 1800, 2200, 0200, 0400, 0600, and 1000 h. No evidence was found for differences in temporal placement or level of the circadian cortisol rhythm in relation to age, growth, or body composition. However, we found a broad range of cortisol levels in a healthy population, with individual mean diurnal levels ranging from 100–510 nmol/L. Regardless of high or low mean diurnal cortisol levels, repeated measurements within and between pubertal stages indicated that an individual remains in his or her cortisol range throughout pubertal development. In conclusion, the present study shows that 1) serum cortisol levels do not correlate with either age or gender; 2) there is a large and significant interindividual variability in endogenous mean diurnal cortisol levels; and 3) despite this variability between individuals, there is no correlation between cortisol levels and either body composition or growth rate. This suggests that the variability in cortisol levels is an expression of normal homeostasis rather than pathology.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
THE HYPOTHALAMUS-pituitary-adrenal (HPA) axis has an important role in maintaining physiological homeostasis under both basal and pathophysiological conditions (1). A basic understanding of the regulation and function of the HPA axis and of its wide basal variability within and between individuals is of vital importance in assessing both pathological changes and the potential adverse effects of glucocorticoid treatment. Although glucocorticoids are commonly used in the treatment of various inflammatory diseases, such as asthma and rhinitis, the functioning of the HPA axis in patients taking glucocorticoids is still not completely understood.

Limited information is available on the role of diurnal variations in serum cortisol levels in healthy children and adolescents in relation to age, gender, growth, and pubertal development. A significant variability in homeostasis of the HPA axis has been observed (2). It is not known, however, whether individual differences in the function of the HPA axis, particularly the circadian rhythm of cortisol secretion, are correlated with age, growth, body composition, gender, or pubertal development.

The purpose of this study was to gain insight into adrenocortical activity throughout childhood and to assess the relationship, if any, between serum cortisol levels and age, sex, weight, height, body composition, and pubertal stage. A further objective was to obtain reference data for serum cortisol levels by studying a large group of healthy boys and girls.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

A total of 235 healthy children (162 boys, 218 cortisol circadian profiles; 73 girls, 120 cortisol circadian profiles) were investigated on 1 or more occasions at the Children’s Hospital (Göteborg, Sweden). Their chronological ages ranged from 2.2–18.5 yr, and their bone ages were within ±2 SD scores for chronological age. All children were healthy and well nourished and had normal thyroid, liver, and kidney functions. Coeliac disease was excluded. No child was receiving any medical treatment.

Of the 120 profiles in girls, 48 were taken during prepuberty, 17 during pubertal stage 2, 16 during stage 3, 22 during stage 4, and 17 during stage 5. Of the 218 profiles in boys, 136 were taken during prepuberty, 40 during pubertal stage 2, 18 during stage 3, 10 during stage 4, and 14 during stage 5. Puberty was assessed according to Tanner for pubic hair and breast development (3) and according to Prader for testicular volume (4). When adrenarche and gonadarche differed, the pubertal stage was rated after development of gonadarche, i.e. breast development in girls and testicular volume in boys. Height and weight were converted into SD score using the Swedish Growth Reference Values for healthy children (5). The growth of the children had been followed since birth; height ranged from -4.3 to 5.3 SD score, and weight for height ranged from -2.67 to 3.47 SD score according to the formula of Albertsson-Wikland et al. (6).

Study protocol

Cross-sectional study. The children were accommodated at the hospital for at least a 24-h period with the minimal stress possible, during which time they received a normal diet and were allowed routine activity and sleep. A heparinized needle was inserted into an antecubital vein mainly in the afternoon of the day before the sampling began. Blood sampling was initiated at 1400 h, and further samples were obtained at 1800, 2200, 0200, 0400, 0600, and 1000 h. The serum was separated and kept frozen until assayed for cortisol. The number of measurements and the interval between them were chosen so that the circadian rhythm could be studied with as few measurements as possible, taking account of the times when the most dynamic changes occur.

Longitudinal study. A subgroup of 28 children (18 boys and 10 girls) was followed longitudinally with 2–7 repeated profiles within and/or across pubertal stages, giving a total of 87 profiles. The median time interval between the repeated profiles was 1.05 yr (range, 0.5–8.0 yr).

The study protocol was approved by the ethical committee of the Medical Faculty (Göteborg, Sweden). Informed consent was obtained from the children, if they were old enough, and their parents.

Measurement of cortisol

Serum cortisol was determined with a RIA from Farmos Diagnostica (Åbo, Finland). The analysis was performed at the Department of Clinical Chemistry at Sahlgren’s Hospital (Göteborg, Sweden; accredited laboratory no. 1240 according to European home EN 45001). All points within a profile were measured in the same run. Inter- and intra-assay coefficients of variation were less than 10% over a concentration range between 30–800 nmol/L.

Statistical analysis

The results are expressed as the mean ± SEM unless otherwise indicated. For each profile the area under the curve (AUC) was calculated, and this estimate was used for statistical comparisons. The Mann-Whitney U test was used, and P < 0.05 was considered significant. When multiple comparisons were made, the P value was adjusted, using the Bonferroni method, with the number of comparisons to compensate for a mass-significance effect (7).


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Cross-sectional analysis

A complete data set of 338 24-h cortisol profiles was obtained from the 235 healthy children and adolescents examined. As illustrated in Fig. 1Go, there was no age-related difference in mean cortisol levels over the age range studied (2–18 yr). Furthermore, when analyzing all subjects as a group, no correlation was observed between cortisol levels and weight, height, or body composition, expressed as the weight for height SD score.



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  		Figure 1. Mean serum concentration of cortisol for all children as a function of age. The inset shows the distribution of the serum cortisol values.

 
The prepubertal subjects were divided into boys and girls and further divided into three groups according to height: tall (>2 SD score; 7 boys and 7 girls), normal (>2 SD score <2; 30 boys and 13 girls), and short (<2 SD score; 92 boys and 24 girls) children. The mean values of plasma cortisol from each group were calculated for each sampling time. As illustrated in Fig. 2Go, there was no evidence of any significant differences in the mean cortisol profiles in relation to gender or height.



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  		Figure 2. Serum cortisol profiles for prepubertal boys and girls of short, normal, and tall stature. The values shown are the mean ± SEM. The AUCs were 4298 ± 288 for short girls, 4614 ± 455 for normal girls, 4145 ± 226 for tall girls, 4236 ± 133 for short boys, 4128 ± 262 for normal boys, and 4294 ± 738 for tall boys. There were no significant differences between the groups (by Mann-Whitney U test).

 
To examine the effects of pubertal status on cortisol levels, all subjects were divided according to pubertal stage, but no significant differences were found in the cortisol rhythm and/or absolute values between pubertal stages. However, when these groups were further divided by gender, there was no difference between boys and girls during pubertal development, except for a minor difference (P < 0.05) at pubertal stage 2 (Fig. 3Go).



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  		Figure 3. Serum cortisol profiles for boys and girls during pubertal development. The values shown are the mean ± SEM. The AUCs for the girls were 4383 ± 199, 4642 ± 393, 3694 ± 234, 3809 ± 274, and 4058 ± 375 at pubertal stages 1–5, respectively; the AUCs for the boys were 4201 ± 110, 3715 ± 123, 3561 ± 219, 3037 ± 219, and 3662 ± 171 at pubertal stages 1–5, respectively. There was a significant difference (P < 0.05) between boys and girls at pubertal stage 2 (by Mann-Whitney U test).

 
Longitudinal analysis

In a longitudinal analysis, no significant differences were observed between repeated cortisol profiles for each individual, whether analyzed within a specific pubertal stage or across several or all five pubertal stages. Figure 4Go (upper panels) illustrates results from selected individuals from each gender, indicating that the pattern of cortisol secretion and circadian rhythmicity remained stable and reproducible within the individual during pubertal development. There were, however, significant interindividual variations in the normal population. Figure 4Go (lower panels) shows serum cortisol values for all five pubertal stages analyzed as the percentage of the individual cortisol profile at pubertal stage 1, further demonstrating the consistent nature of individual cortisol profiles during development. Figure 5Go shows the differences (as a percentage) of the AUC between the first and second 24-h profiles, between the second and third profiles, and between the third and fourth profiles, illustrating the high degree of reproducibility between repeated profiles.



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  		Figure 4. Longitudinal serum cortisol profiles for boys and girls during pubertal development. The upper panels show profiles for a typical boy and girl. The lower panels show the mean ± SEM for the different pubertal stages normalized around pubertal stage 1, the mean of which was set at 100%. There were no significant differences between pubertal stages (by Mann-Whitney U test).

 


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  		Figure 5. Difference (percentage) between the AUCs of successive profiles. All children with more than one profile, regardless of pubertal stage, were included. The square and error bars indicate the mean and 95% confidence limits of the differences. The median time intervals (ranges) between the repeated profiles were 1.3 (0.6–8.0), 1.0 (0.5–4.9), and 1.0 (0.7–1.8) yr for the three groups.

 
Reference values

A wide variability in circadian cortisol levels between individuals was found, with individual mean diurnal values ranging from 100–510 nmol/L. All individual profiles together with percentile ranges are presented in Fig. 6Go (left panel). The right panels of Fig. 6Go show the profiles for 3 subgroups, consisting of 15 subjects each, representing individuals with the highest, median, and lowest mean diurnal level of cortisol. For the group as a whole there was no correlation between the levels of cortisol (AUC) and the peak/nadir quotient. However, the 5 individuals with the highest AUC had a lower peak/nadir value (median, 2.6; range, 1.3–3.4) than the rest of the group (median, 8.2; range, 3.1–15.7; 5–95% percentiles). Despite the relatively small number of measurements, circadian rhythmicity was observed in all children.



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  		Figure 6. All serum cortisol profiles for the boys and girls at all pubertal stages (left panel). Also indicated are the 5th, 25th, 50th, 75th, and the 95th percentiles. The right panels show the 15 lowest, 15 highest, and 15 median profiles.

 

   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
The aim of the present investigation was 2-fold: 1) to determine the effects of age, gender, and pubertal stage on the circadian rhythm of cortisol, and 2) to establish a normative database of cortisol in healthy children and adolescents. Our results clearly indicate that the diurnal rhythm of cortisol is an extremely robust rhythm; is unaffected by age, gender, or pubertal status; and is not correlated with height SD scores.

The variability of serum cortisol is known to be the result of many influences, including feedback between the pituitary secretion of ACTH and adrenal secretion of cortisol, circadian rhythm, episodic secretion, transcortin levels (8, 9), wake-sleep patterns, and stress factors (1, 10, 11, 12). This circadian pattern is absent in the newborn, but is well established by 2 yr of age (13). A certain amount of cortisol is essential for normal, nonstressed activity. The episodic secretion of endogenous cortisol in normal subjects has been well established and is characterized by a constant and reproducible pattern after a daily circadian rhythm under stable physiological conditions (14, 15, 16). This rhythmicity is not easily perturbed, although endogenous hormonal oscillations can be phase delayed (1).

The influence of the circadian rhythm of cortisol secretion on growth and physical development has been investigated in only a small number of studies. Significant age and gender differences in cortisol secretion have been reported (13, 17, 18), as has a relationship between cortisol levels, weight, and pubertal stage (19). The majority of studies, however, have not been able to confirm these results and have indicated that there are no significant effects of age, gender, or sexual maturation on the activity of the HPA axis after the neonatal period (20, 21, 22, 23). Conflicting results have also been obtained in cortisol responses to various physical stress factors (24, 25). These contradictory results probably reflect differences in experimental design and/or methodology. The present results generally agree with those from the majority of previous studies, i.e. age, gender, and puberty do not seem to be important factors for the diurnal cortisol levels.

Our study confirms the marked interindividual variability in the circadian profile of cortisol in a healthy population. However, for each individual, the profiles were very stable and reproducible and were not correlated to age, height, weight, body composition, pubertal development, or gender. In fact, the difference in AUC estimates between repeated profiles was in the same range or lower than the assay imprecision, further strengthening the concept of individually maintained levels of cortisol. In humans, several studies have indicated that genetic factors are involved in the expression of circadian rhythmicity (24, 26, 27). It has also been suggested that the development of the HPA response to stress is determined by events occurring early in life (28).

Induced small variations in plasma cortisol are known to affect lipolysis and glucose homeostasis (29). Despite the significant variability in adrenocortical activity both within and between individuals, the system appears to be well regulated within different tissues and at different cellular levels, as indicated by the childrens’ normal healthy physical development and the absence of any correlation between cortisol levels and body composition, height, and weight. This suggests that differences in cortisol levels reflect normal homeostatic versatility rather than pathology, with variations in cortisol levels perhaps balanced by a corresponding variation in glucocorticoid sensitivity in target cells. Thus, there appears to be an elegantly balanced homeostatic system that encompasses large interindividual differences in cortisol levels under basal conditions without any major disturbances in peripheral tissues.

In summary, our results demonstrating wide interindividual variability in the circadian profile of cortisol in a population of healthy young children are of clinical importance when determining hypo- or hypercortisolism as well as when assessing the effects on the HPA axis of glucocorticoid medication. Moreover, individual differences in cortisol profiles may assume significance in patients requiring high doses of glucocorticoids for long periods of time or in patients predisposed to a disease such as diabetes or osteoporosis. The implications of the findings of our study with regard to symptoms and pathological changes in various diseases as well as sensitivity to glucocorticoid need to be further explored, as clinical observations indicate that some patients receiving traditional glucocorticoid replacement doses became Cushingoid (30), whereas others fail to respond. Normal glucocorticoid replacement doses may, therefore, be either too high or too low for certain individuals. Variations in the range of cortisol secretion should, therefore, be considered when evaluating the effects of glucocorticoid administration.


   Acknowledgments
 
The authors are grateful to the staff of ward 34T at the Children’s Hospital (Goteborg, Sweden) for taking care of the children.


   Footnotes
 
1 This work was supported by grants from the Swedish Medical Research Council (no. 7509, 9522, and 9945), the Lundgren Foundation, the Free Mason Foundation, Pharmacia-Upjohn, the Lundbergs Foundation, the Swedish Asthma and Allergy Association, and the Swedish Heart and Lung Foundation. Back

Received June 13, 1996.

Revised October 22, 1996.

Accepted October 24, 1996.


   References
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 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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