© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Pediatric Diabetes 2014: 15: 599–605 doi: 10.1111/pedi.12125 All rights reserved
Pediatric Diabetes
Original Article
Mood and its association with metabolic health in adolescents: a longitudinal study, EarlyBird 65 Jeffery AN, Hyland ME, Hosking J, Wilkin TJ. Mood and its association with metabolic health in adolescents: a longitudinal study, EarlyBird 65. Pediatric Diabetes 2014: 15: 599–605. Background: Mood comprises two main traits – positive and negative affect, both associated with depression and anxiety. Studies in children have linked depression with obesity, but the association with metabolic health is unclear. Objective: To explore the relationship between mood and metabolic health in adolescents. Methods: We studied 208 healthy children (115 boys) enrolled in the longitudinal EarlyBird Diabetes Study, and reviewed at 7 and 16 yr. Participants completed the Positive Affect and Negative Affect Schedule – Child Form (PANAS-C) at 16yr to assess positive and negative affect, together representing mood. Measures at 7 and 16 yr: body mass index (BMI), fat (%; dual energy X-ray absorptiometry), physical activity (accelerometer), metabolic risk z-score comprising homeostasis model assessment-insulin resistance (HOMA-IR), triglycerides, total cholesterol/high density lipoprotein (HDL) ratio and blood pressure. Pubertal development was determined by age at peak height velocity. Results: Positive affect was higher in boys than girls, (50 vs. 46, p = 0.001), negative affect higher in girls than boys (26 vs. 22, p < 0.001). Those with lower mood were fatter (r = −0.24, p < 0.001), had higher HOMA-IR (r = −0.12, p = 0.05), higher cholesterol:HDL ratio (r = −0.14, p = 0.02), were less active (r = 0.20, p = 0.003) and had earlier pubertal development (r = 0.19, p = 0.004). Inverse associations between mood and metabolic risk z-score and change in metabolic risk z-score 7–16yr (β = −0.26, p = 0.006, and −0.40, p = 0.004, respectively) were independent of adiposity, physical activity and puberty and sex. Conclusions: Low mood in healthy children is associated with poorer metabolic health independently of adiposity. These findings may have implications for the physical and mental health of contemporary youngsters, given their increasing obesity and cardiometabolic risk.
Mood or trait affect has been associated with mental health problems such as depression and anxiety in both adults (1) and children (2, 3) and comprises two components, negative affect and positive affect. Negative affect is a broad general factor of emotional distress that includes moods such as fear, sadness and guilt and is present in both anxiety and depression. Positive affect is represented by pleasant feelings (e.g., interested, strong, and active), and low positive affect is specific to depression. Both negative and positive
Alison N. Jefferya , Michael E. Hylandb , Joanne Hoskinga and Terence J. Wilkinc a Institute of Translational and Stratified Medicine, Plymouth University Peninsula Schools of Medicine and Dentistry, Plymouth, UK; b Department of Psychology, Plymouth University, Plymouth, UK; and c Institute of Health and Social Research, University of Exeter Medical School, Exeter, UK
Key words: child – insulin resistance – longitudinal study – mood – weight perception Corresponding author: Dr Alison Jeffery University Medicine, Level 7 Derriford Hospital Plymouth PL6 8DH UK. Tel: 44 1752 792649; fax: 44 1752 792471; e-mail: [email protected] Submitted 27 September 2013. Accepted for publication 8 January 2014
affect are associated with adult health (4, 5) and are relatively stable as people age from childhood into adulthood (6). Mood is associated with diabetes (7, 8), the metabolic syndrome (9), immune function (10), insulin resistance (IR) (11, 12) and cardiovascular disease (13–15). Interestingly, Lawlor et al. reported an inverse association between IR and depression in middle aged women (16), but none in men (17). A meta-analysis showed that the prevalence of depression is doubled in individuals with type 2
599
Jeffery et al. diabetes compared with those without diabetes (18). However, the temporal relationship between depression and type 2 diabetes remains unclear – depression may develop as a result of living with the burden of diabetes (19) through affecting behavioural patterns such as increased energy intake or reduced physical activity. There is also evidence that depression is an independent risk factor for the development of type 2 diabetes (11, 12). In a meta-analysis of longitudinal studies in adults, Knol et al. (20) concluded that elevated depressive symptoms were associated with a 37% increased risk of developing type 2 diabetes in the future, and this effect was not significantly diminished by confounders such as body mass index (BMI). Depressive symptoms may activate underlying physiological stress pathways, including upregulating the hypothalamic–pituitary–adrenal axis, altering insulin signalling in the brain or increasing proinflammatory factors (21). The association between obesity and depression in children is established (22), and depressive symptoms in adolescents have been shown to predict obesity a year later (23). Cross-sectional studies of adolescents have found depressive symptoms to be associated with insulin sensitivity, both dependent (24) and independent of adiposity (25, 26). Louise et al. (25) also reported an inverse relationship between anxious-depressed scores and systolic blood pressure trajectories during childhood. Given the increasing incidence of type 2 diabetes in youth, (27, 28) it is important to consider whether the association between depressive symptoms and increased metabolic risk is evident during childhood. If the association is established, careful monitoring of mental health in youth with type 2 diabetes may be warranted. Two longitudinal studies of mood and metabolic risk factors have involved children. In the first study of mainly obese participants (29), depressive symptoms measured once between 6 and 13 yr were associated with IR 6 yr later, but IR was not associated with later depression. This study was limited by low participant retention (58%) and the findings are not generalizable to normal weight children. The second (30) reported that females born in 1946 who experienced emotional problems as adolescents were more likely to be diagnosed with the metabolic syndrome in middle age. To our knowledge, no other longitudinal studies have examined the association between metabolic health and mood in a contemporary cohort of otherwise healthy children, yet disturbance in the former is an important health risk (27, 28, 31). We hypothesised that: 1 Lower mood and increased metabolic risk would be correlated at 16 yr, and that adiposity would explain some of this association.
600
2 Increases in metabolic risk and adiposity during childhood would predict lower mood at 16 yr.
Methods EarlyBird is an observational cohort study of 307 children recruited at 5 yr from randomly selected schools, with a wide socio-economic range (32). The majority (98%) were white Caucasian, with a wide socio-economic mix representative of the UK as a whole (mean Index of Multiple Deprivation (IMD): 21.7, range: 6.5–73.0; UK mean: 26.3). Ethical approval was obtained in 1999, with additional approval for the mood study in 2010. Parents gave written consent at baseline and their children gave verbal assent for all tests. Both parent and child gave further informed written consent to complete the mood questionnaire at the 16 yr data collection (2010–2011). The study was conducted in accordance with the Declaration of Helsinki. Measures relevant to this report include exact age, height to the nearest 1 mm (blind duplicates; Leicester Height Measure, Child Growth Foundation, London), weight to the nearest 200 g (blind duplicates; Tanita Solar 1632W electronic scales, Amsterdam, The Netherlands). The children were dressed in shirt and underwear only. BMI was calculated as weight/height2 and standard deviation scores (SDS) derived in relation to the UK 1990 BMI reference curves (33). Body fat was measured annually by dual energy X-ray absorptiometry (DEXA: Lunar Prodigy Advanced fan beam system, Lunar Corporation, Madison, WI, USA) and is presented as percentage of body mass that comprises fat (fat %). Systolic and diastolic blood pressure were measured seated (SBP, DBP; Welch Alleyn automated sphygmomanometer, Aston Abbotts, UK) and the mean of two measures calculated. All blood samples were taken fasting between 9:00 and 9:45, and included serum insulin (DPC Immulite, Los Angeles, USA, cross-reactivity with proinsulin 0.9 (35). A mean metabolic risk z-score was calculated comprising sex and age-specific standardised measures of IR, CHR, triglycerides, SBP, and DBP (36), a higher score representing poorer metabolic health. Pubertal development was assessed by age at peak height velocity (APHV), determined as the tangential velocity at the middle time-point of three consecutive Pediatric Diabetes 2014: 15: 599–605
Mood and metabolic health in adolescents Table 1. Characteristics of cohort at 7 and 16 yr, mean (SD)
n: Boys (girls) Age (yr) Age at peak height velocity (yr) Positive affect Negative affect Mood Physical activity x 1000 (mean counts per day) BMI (SDS) Fat (%) Insulin resistance (HOMA-IR) Triglycerides (mmol/l) Cholesterol:HDL ratio Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Metabolic z-score
7 yr
16 yr
T for difference 7 vs. 16 yr
p for difference 7 vs. 16 yr
115 (93) 6.87 (0.29) 367.46 (75.44) 0.35 (1.20) 15.99 (8.22) 0.36 (0.25) 0.57 (0.28) 2.70 (0.56) 98.08 (5.23) 60.73 (5.22) −0.03 (0.60)
115 (93) 15.82 (0.28) 12.42 (1.32) 48.17 (9.31) 24.95 (8.42) 23.23 (14.78) 348.22 (14.36) 0.56 (1.19) 23.53 (12.20) 0.58 (0.74) 0.71 (0.33) 2.96 (0.72) 111.60 (9.39) 68.72 (6.47) 0.18 (0.66)
56.22 −4.46 13.40 −7.92 −7.45 −6.88 −18.06 −19.09 −3.11
Pediatric Diabetes 2014: 15: 599–605 doi: 10.1111/pedi.12125 All rights reserved
Pediatric Diabetes
Original Article
Mood and its association with metabolic health in adolescents: a longitudinal study, EarlyBird 65 Jeffery AN, Hyland ME, Hosking J, Wilkin TJ. Mood and its association with metabolic health in adolescents: a longitudinal study, EarlyBird 65. Pediatric Diabetes 2014: 15: 599–605. Background: Mood comprises two main traits – positive and negative affect, both associated with depression and anxiety. Studies in children have linked depression with obesity, but the association with metabolic health is unclear. Objective: To explore the relationship between mood and metabolic health in adolescents. Methods: We studied 208 healthy children (115 boys) enrolled in the longitudinal EarlyBird Diabetes Study, and reviewed at 7 and 16 yr. Participants completed the Positive Affect and Negative Affect Schedule – Child Form (PANAS-C) at 16yr to assess positive and negative affect, together representing mood. Measures at 7 and 16 yr: body mass index (BMI), fat (%; dual energy X-ray absorptiometry), physical activity (accelerometer), metabolic risk z-score comprising homeostasis model assessment-insulin resistance (HOMA-IR), triglycerides, total cholesterol/high density lipoprotein (HDL) ratio and blood pressure. Pubertal development was determined by age at peak height velocity. Results: Positive affect was higher in boys than girls, (50 vs. 46, p = 0.001), negative affect higher in girls than boys (26 vs. 22, p < 0.001). Those with lower mood were fatter (r = −0.24, p < 0.001), had higher HOMA-IR (r = −0.12, p = 0.05), higher cholesterol:HDL ratio (r = −0.14, p = 0.02), were less active (r = 0.20, p = 0.003) and had earlier pubertal development (r = 0.19, p = 0.004). Inverse associations between mood and metabolic risk z-score and change in metabolic risk z-score 7–16yr (β = −0.26, p = 0.006, and −0.40, p = 0.004, respectively) were independent of adiposity, physical activity and puberty and sex. Conclusions: Low mood in healthy children is associated with poorer metabolic health independently of adiposity. These findings may have implications for the physical and mental health of contemporary youngsters, given their increasing obesity and cardiometabolic risk.
Mood or trait affect has been associated with mental health problems such as depression and anxiety in both adults (1) and children (2, 3) and comprises two components, negative affect and positive affect. Negative affect is a broad general factor of emotional distress that includes moods such as fear, sadness and guilt and is present in both anxiety and depression. Positive affect is represented by pleasant feelings (e.g., interested, strong, and active), and low positive affect is specific to depression. Both negative and positive
Alison N. Jefferya , Michael E. Hylandb , Joanne Hoskinga and Terence J. Wilkinc a Institute of Translational and Stratified Medicine, Plymouth University Peninsula Schools of Medicine and Dentistry, Plymouth, UK; b Department of Psychology, Plymouth University, Plymouth, UK; and c Institute of Health and Social Research, University of Exeter Medical School, Exeter, UK
Key words: child – insulin resistance – longitudinal study – mood – weight perception Corresponding author: Dr Alison Jeffery University Medicine, Level 7 Derriford Hospital Plymouth PL6 8DH UK. Tel: 44 1752 792649; fax: 44 1752 792471; e-mail: [email protected] Submitted 27 September 2013. Accepted for publication 8 January 2014
affect are associated with adult health (4, 5) and are relatively stable as people age from childhood into adulthood (6). Mood is associated with diabetes (7, 8), the metabolic syndrome (9), immune function (10), insulin resistance (IR) (11, 12) and cardiovascular disease (13–15). Interestingly, Lawlor et al. reported an inverse association between IR and depression in middle aged women (16), but none in men (17). A meta-analysis showed that the prevalence of depression is doubled in individuals with type 2
599
Jeffery et al. diabetes compared with those without diabetes (18). However, the temporal relationship between depression and type 2 diabetes remains unclear – depression may develop as a result of living with the burden of diabetes (19) through affecting behavioural patterns such as increased energy intake or reduced physical activity. There is also evidence that depression is an independent risk factor for the development of type 2 diabetes (11, 12). In a meta-analysis of longitudinal studies in adults, Knol et al. (20) concluded that elevated depressive symptoms were associated with a 37% increased risk of developing type 2 diabetes in the future, and this effect was not significantly diminished by confounders such as body mass index (BMI). Depressive symptoms may activate underlying physiological stress pathways, including upregulating the hypothalamic–pituitary–adrenal axis, altering insulin signalling in the brain or increasing proinflammatory factors (21). The association between obesity and depression in children is established (22), and depressive symptoms in adolescents have been shown to predict obesity a year later (23). Cross-sectional studies of adolescents have found depressive symptoms to be associated with insulin sensitivity, both dependent (24) and independent of adiposity (25, 26). Louise et al. (25) also reported an inverse relationship between anxious-depressed scores and systolic blood pressure trajectories during childhood. Given the increasing incidence of type 2 diabetes in youth, (27, 28) it is important to consider whether the association between depressive symptoms and increased metabolic risk is evident during childhood. If the association is established, careful monitoring of mental health in youth with type 2 diabetes may be warranted. Two longitudinal studies of mood and metabolic risk factors have involved children. In the first study of mainly obese participants (29), depressive symptoms measured once between 6 and 13 yr were associated with IR 6 yr later, but IR was not associated with later depression. This study was limited by low participant retention (58%) and the findings are not generalizable to normal weight children. The second (30) reported that females born in 1946 who experienced emotional problems as adolescents were more likely to be diagnosed with the metabolic syndrome in middle age. To our knowledge, no other longitudinal studies have examined the association between metabolic health and mood in a contemporary cohort of otherwise healthy children, yet disturbance in the former is an important health risk (27, 28, 31). We hypothesised that: 1 Lower mood and increased metabolic risk would be correlated at 16 yr, and that adiposity would explain some of this association.
600
2 Increases in metabolic risk and adiposity during childhood would predict lower mood at 16 yr.
Methods EarlyBird is an observational cohort study of 307 children recruited at 5 yr from randomly selected schools, with a wide socio-economic range (32). The majority (98%) were white Caucasian, with a wide socio-economic mix representative of the UK as a whole (mean Index of Multiple Deprivation (IMD): 21.7, range: 6.5–73.0; UK mean: 26.3). Ethical approval was obtained in 1999, with additional approval for the mood study in 2010. Parents gave written consent at baseline and their children gave verbal assent for all tests. Both parent and child gave further informed written consent to complete the mood questionnaire at the 16 yr data collection (2010–2011). The study was conducted in accordance with the Declaration of Helsinki. Measures relevant to this report include exact age, height to the nearest 1 mm (blind duplicates; Leicester Height Measure, Child Growth Foundation, London), weight to the nearest 200 g (blind duplicates; Tanita Solar 1632W electronic scales, Amsterdam, The Netherlands). The children were dressed in shirt and underwear only. BMI was calculated as weight/height2 and standard deviation scores (SDS) derived in relation to the UK 1990 BMI reference curves (33). Body fat was measured annually by dual energy X-ray absorptiometry (DEXA: Lunar Prodigy Advanced fan beam system, Lunar Corporation, Madison, WI, USA) and is presented as percentage of body mass that comprises fat (fat %). Systolic and diastolic blood pressure were measured seated (SBP, DBP; Welch Alleyn automated sphygmomanometer, Aston Abbotts, UK) and the mean of two measures calculated. All blood samples were taken fasting between 9:00 and 9:45, and included serum insulin (DPC Immulite, Los Angeles, USA, cross-reactivity with proinsulin 0.9 (35). A mean metabolic risk z-score was calculated comprising sex and age-specific standardised measures of IR, CHR, triglycerides, SBP, and DBP (36), a higher score representing poorer metabolic health. Pubertal development was assessed by age at peak height velocity (APHV), determined as the tangential velocity at the middle time-point of three consecutive Pediatric Diabetes 2014: 15: 599–605
Mood and metabolic health in adolescents Table 1. Characteristics of cohort at 7 and 16 yr, mean (SD)
n: Boys (girls) Age (yr) Age at peak height velocity (yr) Positive affect Negative affect Mood Physical activity x 1000 (mean counts per day) BMI (SDS) Fat (%) Insulin resistance (HOMA-IR) Triglycerides (mmol/l) Cholesterol:HDL ratio Systolic blood pressure (mmHg) Diastolic blood pressure (mmHg) Metabolic z-score
7 yr
16 yr
T for difference 7 vs. 16 yr
p for difference 7 vs. 16 yr
115 (93) 6.87 (0.29) 367.46 (75.44) 0.35 (1.20) 15.99 (8.22) 0.36 (0.25) 0.57 (0.28) 2.70 (0.56) 98.08 (5.23) 60.73 (5.22) −0.03 (0.60)
115 (93) 15.82 (0.28) 12.42 (1.32) 48.17 (9.31) 24.95 (8.42) 23.23 (14.78) 348.22 (14.36) 0.56 (1.19) 23.53 (12.20) 0.58 (0.74) 0.71 (0.33) 2.96 (0.72) 111.60 (9.39) 68.72 (6.47) 0.18 (0.66)
56.22 −4.46 13.40 −7.92 −7.45 −6.88 −18.06 −19.09 −3.11
