Abstract
BACKGROUND:
American Indian (AI) populations suffer disproportionately from cardiovascular disease and depression as compared to other racial/ethnic groups. Behaviors that contribute to obesity are considered obesogenic and include poor diet, low physical activity, and high screen time. This study examined the relationship between depressive symptoms and obesogenic behaviors on cardiometabolic risk factors in AI youth.
METHODS:
Participants (n=121) were evaluated for depressive symptoms, obesogenic behaviors, weight, blood pressure, lipids, and glucose levels.
RESULTS:
All participants failed to meet guidelines for intake of sugar-sweetened beverages and fruits/vegetables, 74% did not meet physical activity guidelines, and 85% did not meet screen time guidelines. Lower physical activity was associated with higher body fat percentage (β=−4.20 ± 1.82, p=0.022). Elevated depressive symptoms and presence of at-risk cardiometabolic risk factors were found. Higher depressive symptoms were associated with higher blood glucose (random, fasting, and hemoglobin A1c)
CONCLUSIONS:
Low physical activity, high screen time, and the presence of depressive symptomology heighten cardiometabolic risk factors in AI children. Associations between depressive symptoms and blood glucose underscore the impact of emotional health on cardiometabolic disease and emphasize need for proper depression assessment in chronic disease prevention efforts.
DISEASES that are apparently unrelated may share common etiological pathways. For example, depressive symptoms instigate biological responses that lead to cardiometabolic disease.(1) Obesity and cardiometabolic disease can lead to depressive symptoms,(2,3) creating a cyclical metabolic pathology. This constellation of diseases is particularly troubling for children who have a high prevalence of these disorders, such as American Indians (AI).(4) In a recent study, 63% of 7- to 13-year-old AI youth were overweight/obese,(5) compared to 34% in the general population.(6) Furthermore, AI children have the highest prevalence of type 2 diabetes as compared to US Blacks, Hispanics, and Whites.(7) Twelve(8) to 14%(4) of AI children were hypertensive, compared to 2% in the general population of 8- to 12-year-olds.(9)
A review of 21 studies found that depressive symptoms are related to obesogenic behaviors in children and youth.(10) Children who engage in obesogenic behaviors are at higher risk for obesity,(11,12) cardiovascular disease,(13) pediatric metabolic syndrome,(14,15) and depressive symptoms.(16–19) However, no previous studies concomitantly examined the emotional (specifically depression) and cardiometabolic risk factors or specifically included AI children. AI youth participate in more obesogenic behaviors than non-AI peers, which exacerbate the early development of pathological progression.(5) For example, AI youth 7- to 13-years-old had higher daily consumption of sugar-sweetened beverages than the general population (309 vs 178 kcal for 2–111 year olds] and 286 kcal for 12–19 year olds),(5,20) and the percentage of AI children meeting 1 hour of physical activity (PA)/day was lower than the general population (32% vs 70%).(5,21) Understanding the relationship between behavioral risk factors and physical and mental health is important for effective interventions within high-risk populations.(22) Therefore, the purpose of this project was to examine the relationship between depressive symptoms and obesogenic behaviors on cardiometabolic risk factors in 7- to 13-year-old AI youth.
Methods
Study Design
This cross-sectional study included 7-to 13-year-old children (n=121) who attended a wellness summer camp. The wellness summer camp, Native Youth Preventing Diabetes, is a 5-day, 4-night diabetes prevention intervention. The intervention was offered at low or no-cost to participants from eligible coalition partners. Eligibility included freedom from diagnosed metabolic-disease. Self-reported behaviors (diet, physical activity, and screen time), self-reported depressive symptoms, and biological measures were ascertained by trained technicians. Study personnel assisted with reading comprehension as needed. Parents voluntarily consented and children voluntarily assented. University ethics committee and tribal coalition reviewed and approved this study and procedures.
Dietary Intake Behavior
An abbreviated Beverage Questionnaire-15 (Bevq-15)(23) was used to assess sugar-sweetened beverage consumption. Questions included frequency and volume of sweetened juice/beverages, regular soft drinks, diet soft drinks, sweetened teas, fruit juice, and energy/sports drinks. Summing the caloric value of the daily consumption of each beverage estimates the total daily sugar-sweetened beverage consumption in kilocalories.(24) The Bevq-15 is validated in children 9+ years.(23) While this tool has not been validated for younger children, no difference was observed in responses between the 7- and 8-year-olds and the older children.(5) The selected psychometric properties for these questions are r2=0.52–0.95 (p<0.001), indicating a moderate-to-strong test-retest reliability.(23)
Frequency of breakfast, lunch, and dinner consumption was assessed in three questions using the Project Eating Among Teens (EAT)-2010 Survey.(25,26) Median values were used to calculate total daily meal frequency.(27)
Select questions from the Youth Behavior Risk Surveillance Survey (YBRSS) examined fruit and vegetable intake frequency.(28) These questions assessed the weekly frequency of fruit, green salad, potato, carrot, and “other” vegetable consumption. The median value for each answer option range was used to calculate daily fruit and vegetable intake.(29) Psychometric properties for this survey instrument are unavailable.
Physical Activity and Screen Time Behavior
Time spent in physical activity (PA) and screen time (ST) was reported using the Project EAT 2010 Survey.(26) Three questions assessed participation in mild, moderate, and vigorous PA.(30) Eight questions assessed time in hours spent watching TV, using a computer, playing sedentary electronic games, and playing non-sedentary (i.e., exergaming) electronic games for week and weekend days.(31) Median values were used to calculate daily time spent in PA and ST.(27) Daily moderate and vigorous PA were summed to create moderate + vigorous PA (MVPA).(27) Psychometric properties for this tool show a moderate test-retest reliability in 12- to 18-year-old adolescents: mild PA r=0.54, moderate PA r=0.53, and vigorous PA r=0.72, watching TV/DVD; r=0.81 using computer; r=0.84 sedentary video games; and r=0.73 non-sedentary video games.(31) This tool has not been validated in children <12 years; however, no difference in responses between children of younger and older ages were previously observed.(5)
Depressive Symptoms
The 27-item Child Depression Inventory (CDI) was used to evaluate depressive symptoms.(32,33) Each item of the CDI score was assigned a value from 0–2, with final score representing an average of all items. Participants with an average score ≤0.86 were considered to be negative for depressive symptomology, while participants with an average score ≥0.90 were considered to be positive for depressive symptomology. For this study, participants who scored between 0.87–0.89 or who showed an inclination for suicide were individually reassessed by an on-site licensed clinical psychologist for depressive symptomology.(32) The continuous average score ranging from 0 to 2 was an independent variable in this study. It has been validated in children ages 6–17 years (Cronbach’s alpha=0.86).
Cardiometabolic Risk Factors
Height in inches, without shoes, was measured using a portable Seca stadiometer (Seca Corp., Chino, CA). Participants were measured for weight (lbs) and body fat percentage using a Tanita TBF-310 Body Composition Analyzer (Tanita Corporation, Arlington Heights, IL). Participants’ body mass index (BMI) percentiles for age and sex were calculated(34) and classified as under-weight, healthy weight, overweight, or obese (i.e., at-risk ≥85th percentile).(35)
Blood pressure was measured in triplicate using an automatic Omron blood pressure machine (Kyoto, Japan) and averaged. Blood pressure percentile was determined for age and gender.(36) At-risk blood pressure was ≥90th percentile as defined by the National High Blood Pressure Education Program.(37)
Waist circumference was measured at midline using an abdominal circumference tension-tape by a registered nurse or registered dietitian and recorded in centimeters. Participants with a waist circumference measurement ≥90th percentile for age and sex were classified as at-risk.(38) Acanthosis nigricans, a thickening and darkening of skin associated with insulin resistance, was evaluated at the neck, armpit, elbow, and knee joint by a physician or physician assistant.(39) Those participants with acanthosis nigricans were classified as at-risk.
Fasting lipids and glucose, total cholesterol, HDL cholesterol, LDL cholesterol, triglycerides, VLDL cholesterol, and blood sugar were measured by a point-of-care lipid analyzer, the Alere Cholestech Analyzer (Alere Corporation, Waltham, MA), via finger-stick blood test after a controlled 10-hr fast. Participants’ outcomes were reported on a continuous scale and additionally classified as normal or at-risk. At-risk lipids were defined as LDL cholesterol >110 mg/dL, triglycerides ≥100 mg/dL, and HDL cholesterol <50 mg/dL.(40) At-risk fasting glucose was defined as ≥110 mg/dL.(15) With the exception of the LDL cholesterol analysis, which is not utilized in metabolic syndrome classification, the Alere Cholestech Analyzer meets the National Cholesterol Education Program guidelines for acceptable laboratory accuracy.(41)
Hemoglobin A1c (HgbA1c) was measured by a point-of-care HgbA1c analyzer, the Siemens DCA Analyzer (Siemens Corp., Malvern, PA). Participants were assessed after a controlled 10-hr fast via finger-stick blood test. Participants’ outcomes were reported on a continuous scale and classified as normal or at-risk.(42) At-risk HgbA1c values were >5.7%.(43) The Siemens DCA analyzer shows good validity and reliability in a field setting,(44) and additionally, recent research suggests that in obese youth without diabetes, HgbA1c results combined with 2-hr post-meal blood glucose show a high rate of sensitivity to impaired glucose.(45) Participants were measured for post-prandial glucose tolerance via finger-stick blood test using a Freestyle Freedom Lite monitor (Abbott Laboratories, Abbott Park, IL) 2 hrs after a 75-g glucose challenge meal. Participant outcomes were reported on a continuous scale and classified as normal or at-risk.(42,46) At-risk post-prandial glucose values were classified as ≥140 mg/dL.
Individual cardiometabolic outcomes were clustered using two mechanisms: a composite cardiometabolic risk score and presence of metabolic syndrome.(15) The composite cardiometabolic risk score was the sum of presence of at-risk scores for each of the following: waist circumference percentile >75th, blood pressure >90th, LDL cholesterol >110 mg/dL, triglycerides >100 mg/dL, HDL cholesterol <50 mg/dL, fasting glucose >110 mg/dL, and acanthosis nigricans positive. For example, if a participant were at risk for waist circumference, triglycerides, HDL cholesterol, and acanthosis nigricans, their composite cardiometabolic risk score was 4. Metabolic syndrome is determined by the presence or absence of three or more of the following five risk factors: waist circumference percentile (>75th), blood pressure percentile (>90th), HDL cholesterol (<50 mg/dL), triglycerides (>100 mg/dL), and fasting glucose (>110 mg/dL).(15) With the exception of adding LDL cholesterol and acanthosis nigricans to the continuous cardiometabolic risk score, the same constituent risk factors were used for both definitions; the former highlights the risk for chronic disease, the latter highlights presence of disease.
Data Analysis
Descriptive statistics included means ± standard deviation (SD) and frequency. Differences between sexes for obesogenic behaviors, depressive symptoms, and continuous scale cardiometabolic risk factors were analyzed using independent t-test. Differences between sexes for acanthosis nigricans were analyzed with Pearson’s chi-square. Association of obesogenic behaviors and depressive symptomology with individual and clustered cardiometabolic risk factors was assessed with a series of linear regression models. Logistic regression models were used to determine the association between obesogenic behaviors, depressive symptomology, acanthosis nigricans, and metabolic syndrome. Covariates included age and sex. Cohen’s d and r were calculated to determine effect size for independent samples t-tests. Data analyses used SPSS 10® (IBM Corporation, Armonk, NY). p-Values <0.05 were significant.
Results
Obesogenic behaviors, depressive symptoms, and cardiometabolic risk factors for the total sample and by sex are shown in Table 1. The study participants’ mean age was 10.5 ± 1.6 yrs and 60% (n=73) were female. All participants exceeded the federal guidelines of zero sugar-sweetened beverages and consumed insufficient fruit/vegetable servings per day. Additionally, 74% had insufficient PA, while 85% exceeded ≥2 hrs of ST/day. The prevalence of at-risk for variables is as follows: BMI% (64%), waist circumference (60%), HDL (57%), triglycerides (17%), blood pressure (13%), total cholesterol (13%), depressive symptomology (12%), and LDL cholesterol (8%). Females had a significantly lower sugar-sweetened beverage intake, higher body fat percentage, lower HDL cholesterol level, and higher prevalence of acanthosis nigricans.
Table 1:
Obesogenic Behaviors, CDI score, Cardio-metabolic risk factor, metabolic syndrome for AI children ages 7–13 years by total sample and sex (n=121)
| Total Sample | Females (n=73) | Males (n=48) | |||||
|---|---|---|---|---|---|---|---|
| Mean ± SD | At-Risk % | Mean ± SD | At-risk % | Mean ± SD | At-risk % | p-value | |
| Obesogenic Behaviors (daily) | |||||||
| All Sugar-sweetened beverages (kcal intake) | 381.9 ± 248.1 | 100 | 323.7 ± 207.7 | 100 | 470.7 ± 279.0 | 100 | 0.002 |
| All Fruit and Vegetable intake frequency (servings) | 1.9 ± 0.9 | 100 | 1.9 ± 0.9 | 100 | 2.1 ± 1.0 | 100 | 0.338 |
| All Meal frequency intake | 2.4 ± 0.73 | 2.5 ± 0.7 | 2.3± 0.8 | 0.486 | |||
| Moderate +vigorous physical activity (hours) | 0.7 ± 0.5 | 74.4 | 0.7 ± 05 | 74 | 0.7 ± 0.6 | 75 | 0.503 |
| Total screen time per average weekday (hours) | 7.2 ± 5.7 | 83.5 | 6.5 ± 4.7 | 79.5 | 8.5 ± 6.9 | 89.6 | 0.079 |
| Total screen time per average weekend day (hours) | 7.3 ± 6.1 | 84.3 | 6.8 ± 5.4 | 82.2 | 8.1 ± 7.0 | 87.5 | 0.295 |
| CDI score | 0.4 ± 0.3 | 11.6 | 0.4 ± 0.3 | 11 | 0.4 ± 0.3 | 12.5 | 0.812 |
| Body mass index percentile | 80.7 ± 24.2 | 64 | 80.5 ± 25.7 | 66 | 80.9 ± 22.0 | 60 | 0.929 |
| Waist circumference percentile | 67.5 ± 26.3 | 60 | 66.9 ± 26.9 | 60 | 68.4 ± 25.6 | 60 | 0.744 |
| Body fat percentage | 26.8 ± 10.9 | - | 28.7 ±10.6 | - | 23.9 ± 11.0 | - | 0.019 |
| Blood pressure percentile | 55.6 ± 14.6 | 13 | 54.0 ± 12.5 | 10 | 58.2 ± 17.3 | 19 | 0.156 |
| Total cholesterol (mg/dl) | 144.3 ± 27.9 | 13 | 140.4 ± 25.8 | 8 | 150.2 ± 30.2 | 21 | 0.067 |
| HDL cholesterol (mg/dl) | 48.8 ±14.5 | 57 | 46.3 ± 13.3 | 66 | 52.6 ± 15.4 | 44 | 0.023 |
| LDL cholesterol (mg/dl) | 86.8 ± 27.1 | 8 | 84.5 ± 26.1 | 8 | 93.6 ± 29.8 | 8 | 0.303 |
| Triglycerides(mg/dl) | 88.7 ± 44.5 | 17 | 90.4 ± 47.8 | 23 | 83.4 ± 33.5 | 8 | 0.536 |
| Post-prandial glucose(mg/dl) | 95.3 ± 24.9 | 1 | 94.9 ± 31.3 | 1 | 95.8 ± 9.0 | 0 | 0.806 |
| Fasting blood glucose(mg/dl) | 87.0 ± 15.5 | 7 | 86.3 ± 17.2 | 4 | 88.0± 12.4 | 10 | 0.539 |
| HgbA1c~ (%) | 5.3 ± 0.9 | 5 | 5.4 ± 1.0 | 5 | 5.3 ± 0.7 | 7 | 0.759 |
| Acanthosis nigricans(+ or −) | n/a | 30 | n/a | 37 | n/a | 19 | 0.032 |
| Cardio-metabolic risk factor score (range 0–7)* | 1.3 ± 1.3 (0–5) | n/a | 2.2 ± 1.5 (0–4) | n/a | 2.0 ± 1.8 (0–5) | n/a | 0.229 |
| Metabolic syndrome risk score (range 0–5)** | 1.6 ± 1.1 (0–5) | 21 | 1.6 ± 1.0 | 23 | 1.4 ± 1.2 | 19 | 0.310 |
Does not include incomplete values, to include low or abnormal hemoglobin results (n=112)
Cardio Metabolic Risk is a continuous sum of risk scores for: blood pressure percentile, waist circumference percentile, HDL cholesterol, LDL cholesterol, triglycerides, fasting glucose, acanthosis nigricans
Metabolic syndrome is categorically defined by having at least three at-risk scores from the following: blood pressure percentile, waist circumference percentile, HDL cholesterol, triglycerides, fasting glucose. Pearson’s Chi-square used for categorical analysis such as acanthosis nigricans and metabolic syndrome.
Independent means t-tests used for continuous variables to include: BMI, Waist Circumference, Blood pressure, body fat, lipid and glucose variables.
Body mass index percentile was calculated using height, weight, gender and age in months
Blood pressure percentile was determine via the average of three separate blood pressures and plotted by gender, age and height percentile
Body fat percent was calculated by the Tanita 300 scale
Waist circumference percentile was measured in centimeters at midline and calculated using gender and age
Total cholesterol, HDL cholesterol, LDL cholesterol, triglycerides, fasting glucose, HgbA1c was obtained (via fingerstick) after a fast (>8 hours)
Post-prandial glucose was obtained 2 hours after a high carbohydrate, low fat, low fiber meal
Acanthosis nigricans was assessed by a trained medical professional (physician, nurse practitioner, physician assistant) and recorded as negative or positive
Depressive Symptoms—Child Depression Inventory (CDI) score is an average of a 27-item continuous score
Associations between obesogenic behaviors and depressive symptomology and individual and composite cardiometabolic risk factors are shown in Table 2. In models including both obesogenic behaviors and depressive symptomology, clustered cardiometabolic risk score and metabolic syndrome were not found to be associated; however, several individual scores were (Table 2). Lower MVPA was associated with higher body fat percentage. Higher ST was associated with higher HDL cholesterol, independent of depressive symptoms. Independent of obesogenic behaviors, depressive symptoms were associated with higher post-prandial glucose, fasting glucose, and HgbA1C. For example, for each point increase in CDI score, random glucose was 24.22 percentiles higher in this analysis.
Table 2.
Association between depressive symptoms (CDI score) and individual obesogenic behaviors on individual and clustered metabolic risk, adjusted for age and gender in 7 – 13 year old American Indian children without diabetes.
| Child’s Depression Inventory and Obesogenic Behaviors | ||||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| CDI | Daily Sugar Sweet Beverage Intake (kcal) | CDI | Daily Fruit and Vegetable Intake (servings) | CDI | Daily Meal Intake Frequency | CDI | Daily Moderate and Vigorous Physical Activity (time in hours) | CDI | Daily Weekday Screen time (time in hours) | CDI | Daily Weekend Screen time (time in hours) | |
| Outcomes | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE | Beta ± SE |
| Body mass index percentile | 7.13 ± 7.69 | 0.01 ± 0.01 | 6.44 ± 7.79 | −2.98 ± 2.46 | 5.67 ± 8.24 | −13.59 ± 17.32 | 6.26 ± 7.70 | −1.04 ± 0.60 | 5.72 ± 7.92 | 0.53 ± 0.64 | 6.21 ± 8.14 | 0.30 ± 0.45 |
| Waist circ. percentile | 6.07 ± 8.34 | 0.02 ± 0.01 | 6.06 ± 8.50 | −2.24 ± 2.69 | 4.83 ± 8.97 | −14.12 ± 18.87 | 4.89 ± 8.32 | −1.42 ± 0.64 | 4.25 ± 8.60 | 0.70 ± 0.49 | 3.48 ± 8.82 | 0.65 ± 0.49 |
| Body fat percent | 4.37 ± 3.36 | 0.01 ± 0.00 | 4.37 ± 3.41 | −0.64 ± 1.09 | 3.94 ± 3.61 | −4.48 ± 7.61 | 3.84 ± 3.33 | −3.95 ± 1.83 | 4.31 ± 3.41 | 0.09 ± 0.21 | 4.15 ± 3.68 | 0.06 ± 0.20 |
| Blood pressure percentile | −0.26 ± 4.71 | 0.00 ± 0.01 | 0.24 ± 4.77 | 0.42 ± 1.51 | 0.70 ± 5.03 | 43.03 ± 10.58 | −0.21 ± 4.75 | −0.145 ± 0.36 | −0.81 ± 4.84 | 0.20 ± 0.28 | −0.18 ± 4.97 | 0.04 ± 0.28 |
| Total cholesterol (mg/dl) | −8.42 ± 8.68 | 0.00 ± 0.01 | −8.48 ± 8.77 | −0.25 ± 2.80 | −8.16 ± 9.27 | 1.08 ± 19.57 | −8.55 ± 8.71 | −0.13 ± 0.68 | −9.88 ± 8.95 | 0.34 ± 0.53 | −11.06 ± 9.167 | 0.45 ± 0.52 |
| HDL cholesterol (mg/dl) | −6.22 ± 4.55 | −0.00 ± 0.01 | −6.30 ± 4.60 | −0.02 ± 1.47 | −7.27 ± 4.85 | −5.76 ± 10.25 | −6.05 ± 4.57 | 0.16 ± 0.36 | −8.88 ± 4.61 | 0.58 ± 0.27 | −9.83 ± 4.73 | 0.59 ± 0.27 |
| LDL cholesterol (mg/dl) | −11.89 ± 12.918 | −0.00 ± 0.02 | −13.27 ± 13.45 | −1.27 ± 4.20 | −16.15 ± 12.77 | 48.01 ± 29.4 | −10.16 ± 12.45 | 2.13 ± 1.12 | −10.09 ± 13.04 | −0.61 ± 0.85 | −8.08 ± 13.43 | −0.76 ± 0.84 |
| Triglycerides (mg/dl) | −16.86 ± 19.79 | 0.00 ± 0.03 | −23.09 ± 19.79 | −9.06 ± 6.65 | −13.03 ± 20.05 | 34.48 ± 47.89 | −16.33 ± 19.50 | −0.80 ± 1.83 | −20.15 ± 20.32 | 0.83 ± 1.37 | −27.58 ± 21.08 | 1.68 ± 1.32 |
| Post-prandial glucose (mg/dl) | 22.05 ± 7.74 | 0.01 ± 0.01 | 24.22 ± 7.83 | 2.76 ± 2.49 | 22.13 ± 8.31 | −3.87 ± 17.55 | 24.33 ± 7.73 | 1.01 ± 0.61 | 19.70 ± 7.97 | 0.69 ± 0.47 | 16.74 ± 8.08 | 1.01 ± 0.46 |
| Fasting glucose (mg/dl) | 9.81 ± 4.85 | 0.01 ± 0.01 | 10.45 ± 4.92 | 0.59 ± 1.57 | 10.93 ± 5.19 | 4.61 ± 10.96 | 11.19 ± 4.82 | 0.68 ± 0.38 | 7.98 ± 4.97 | 0.49 ± 0.29 | 6.78 ± 5.08 | 0.56 ± 0.29 |
| HgbA1c (%) | 0.73 ± 0.27 | 0.00 ± 0.00 | 0.84 ± 0.27 | .16 ± 0.09 | 0.75 ± 0.29 | −0.09 ± 0.62 | 0.81 ± 0.27 | 0.03 ± 0.02 | 0.70 ± 0.28 | 0.02 ± 0.02 | 0.61 ± 0.29 | 0.03 ± 0.02 |
| Cardio-metabolic Risk* | 0.29 ± 0.43 | 0.00 ± 0.00 | 0.27 ± 0.43 | −0.04 ± 0.14 | 0.33 ± 0.45 | 0.22 ± 0.96 | 0.28 ± 0.43 | −0.07 ± 0.24 | 0.29 ± 0.44 | 0.00 ± 0.03 | 0.34 ± 0.45 | −0.01 ± 0.03 |
| Odds Ratio | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) | (95% CI) |
| Acanthosis nigricans (+ or −) | 1.77 (0.45, 6.92) | 1.00 (1.00, 1.00) | 1.80 (0.45, 7.13) | 1.03 (0.65, 1.63) | 1.73 (0.402, 7.409) | 0.888 (0.04, 21.33) | 1.81 (0.46, 7.10) | 1.16 (0.53, 2.50 | 2.11 (0.51, 8. 8) | 0.96 (0.09, 1.05) | 2.01 (0.46, 8.73) | 0.98 (0.90, 1.07) |
| Metabolic Syndrome** | 3.059 (0.707, 13.231) | 1.001 (0.999, 1.003) | 3.303 (0.759, 14.374) | 1.091 (0.662, 1.797) | 4.241 (0.884, 20.340) | 5.905 (0.153, 228.465) | 3.003 (0.694, 12.986) | 0.734 (0.304, 1.774) | 3.471 (0.750, 16.063) | 0.98 (0.89, 1.08) | 2.72 (0.57, 12.99) | 1.02 (0.94, 1.12) |
Cardio Metabolic Risk is a continuous sum of risk scores for: blood pressure percentile, waist circumference percentile, HDL cholesterol, LDL cholesterol, triglycerides, fasting glucose, acanthosis nigricans
Metabolic syndrome is categorically defined by having at least three at-risk scores from the following: blood pressure percentile, waist circumference percentile, HDL cholesterol, triglycerides, fasting glucose
Bolded values indicate statistical significance (p<0.05)
Predictor variables
Child Depression Inventory (CDI) score is an average of a 27-item continuous score
Total sugar sweetened beverage (SSB) intake is a daily kilocalorie average of all SSB variables
Total fruit and vegetable intake is a daily frequency sum of all fruit and vegetable variables
Total meal frequency is a daily frequency sum of all meal variables
Moderate and vigorous physical activity is a daily time average(hours) of moderate and vigorous physical activity variables
Weekday screen time is a daily time average (hours) of all weekday sedentary screen time variables
Weekend screen time is a daily time average(hours) of all weekend sedentary screen time variables
Outcome variables
Body mass index percentile was calculated using height, weight, gender and age in months
Blood pressure percentile was determine via the average of three separate blood pressures and plotted by gender, age and height percentile
Body fat percent was calculated by the Tanita 300 scale for
Waist circumference percentile was measured in centimeters at midline and calculated using gender and age
Total cholesterol, HDL cholesterol, LDL cholesterol, triglycerides, fasting glucose, HgbA1c was obtained (via fingerstick) after a fast (>8 hours)
Random glucose was obtained 2 hours after a high carbohydrate, low fat, low fiber meal
Acanthosis nigricans was assessed by a trained medical professional (physician, nurse practitioner, physician assistant) and recorded as negative or positive
Discussion
This study contributes to the knowledge gap regarding obesogenic behaviors and cardiometabolic risk and depressive symptoms in AI children. While composite scores that included multiple risk factors were not associated with obesogenic behaviors or depressive symptomology, individual cardiometabolic risk factors were, indicating a link between early behaviors and/or depressive symptomology before cardiometabolic risk is manifest. This study also highlights the prevalence of obesogenic behaviors, depressive symptoms, and cardiometabolic risk factors in AI children, data rarely available.
AI children have higher rates of cardiometabolic risk factors than children in the general population. Sixty-four percent of AI children in our study were overweight/obese. These findings were similar to a 63% overweight/obesity finding in a previous study of AI children(5) and higher than the national prevalence of 34% for overweight/obesity.(6,47) Approximately 13% were considered hypertensive as compared to 2% nationally.(9) Nearly 60% of participants had depressed HDL cholesterol compared to 23% nationally.(9) Prevalence of metabolic syndrome was higher in this population than the general U.S. pediatric population (21% vs 3.5%)(48) and similar to national adult prevalence of metabolic syndrome in the (34%).(49) This finding emphasizes that AI children have a higher prevalence of cardiometabolic disease than the U.S. general pediatric population and forecasts chronic health problems with subsequent need for more advanced health care and higher medical-related expenses.
Approximately 74% of participants did not meet the federal PA guidelines of 60 min/day (compared to 30% nationally)(21) and 85% do not meet ST guidelines of <2 hrs/day (compared to 46% nationally).(21) All study participants failed to meet federal recommendations of zero servings of sugar-sweetened beverages (compared to 20% nationally).(50) The significant difference between sugar-sweetened beverage intakes by sex compounded with a medium-sized effect strengthens the argument that sex influences dietary intake. No study participants met the fruit and vegetable intake recommendation of five servings per day, which is similar to the national intake.(51) With the exception of fruit and vegetable intake where the AI and general population both had a prevalence of near zero, AI children had higher prevalence of obesogenic behaviors. It is evident that nutrition and movement behavior change and improvement are needed within this population.
Higher depressive symptoms were associated with higher blood glucose variables (post-prandial glucose, fasting glucose, and HgbA1c), even as obesogenic behaviors that could attenuate the relationship were included. These findings support previous studies and highlight the biologic effects of depressive symptoms on insulin resistance(52) and demonstrate that depressive symptoms have a profound and possibly singular influence on blood glucose, since both hypertension and dyslipidemia are included in the insulin resistance progression(53) and are not associated with depressive symptoms in this population. This emphasizes the underlying biological impact of severe depressive symptoms on insulin resistance(52) and embraces the effect of chronic stress through depression on essential brain functions via the hypothalamic-pituitary-adrenal (HPA) axis and subsequent glucose control.(54) Additionally, in populations with a high prevalence of overweight/obesity, as is observed in AI, the effects of depressive symptomology on metabolic disorder may be more severe.(55)
Contrary to the study hypothesis and other studies,(56–58) dietary behaviors were not associated with cardiometabolic risk factors. This may be a result of the instrument focus on healthy rather than unhealthy food intake. For example, sugar-sweetened beverages and meal skipping are associated with cardiometabolic risk but fruit and vegetable intake was not.(59) In support of previous literature,(48,60–62) higher MVPA was associated with lower body fat percentages. It should be noted that higher ST is associated with higher post-prandial glucose and fasting glucose and that this association is stable when controlling for depressive symptoms, possibly indicating that ST may play a role in this relationship. This is consistent with another study in a similarly-aged population that showed higher ST was found to be associated with a decreased insulin response and resistance.(63)
In contrast to a recent review inversely linking sedentary time with HDL cholesterol,(64) ST was positively associated with HDL cholesterol independent of depressive symptoms. However, the review did not include depressive symptoms,(64) which may explain the difference. Our outcomes do support reports that depressive symptomology is associated with elevated HDL cholesterol.(65,66)
Strengths and Limitations
The investigators included depressive symptoms and cardiometabolic risk factors in AI youth, which should be considered a strength of the current study. Due to the invasive nature of conducting these tests, this type of information has historically been unavailable in controlled study. While this was a field-based study, the equipment used for blood analyses had been shown to remain accurate in previous field-based studies.(41,44)
Study limitations are centered on study type, sample size, and tools used. This study was cross-sectional, and therefore outcomes inference was limited to correlational analysis. Study recruitment was restricted to camp participation, and therefore, sample size and variability were solely controlled by camp participation, and opportunities to increase or change the make-up of the sample did not exist. Camp participation was open to all eligible AI children; however, this did not control for parent perception of camp eligibility and therefore may have been more likely to send children who were at higher risk for diabetes than children who were not. Data collection opportunities were restricted to the duration of the camp week. Although a search for age-appropriate tools was conducted, such tools were scarce and further limited by time availability of participants and the environment in which the study took place. Therefore, some of the study tools utilized had not yet been validated for the younger ages of this sample. The ability to generalize outcomes is limited due to the nature of this project; however, AI children in Oklahoma do stand to benefit from the outcomes. These outcomes may also serve as a comparison group to other minority groups such as children of African-Americans and Hispanic-Americans.
Conclusions
Participants in this study are at higher-risk for obesogenic behaviors, elevated body weight, severe depressive symptomology, hypertension, dyslipidemia, and metabolic syndrome than their non-AI counterparts. The positive association of depressive symptomology and elevated blood sugar variables remained significant when obesogenic behaviors were considered in the analysis model. Depressive symptomology and obesogenic behaviors did not show an increased risk with clustered risk scores such as cardiometabolic risk and metabolic syndrome. As expected, physical activity was associated with weight indicators, and weekday and weekend screen time was associated with blood glucose variables. Unexpectedly, higher weekday and weekend screen times were associated with higher HDL cholesterol when depressive symptomology was also considered.
The effects of both obesogenic behaviors and depressive symptomology on individual cardiometabolic risk factors and the comparatively high prevalence of depressive symptomology in this population are justification for inclusion of mental health intervention in disease prevention models. While interventions highlighting diet, physical activity, and reduced screen time remain necessary, the inclusion of prevention and treatment of depressive symptomology would be beneficial. Future research is called for to include further evaluation of the effect of behavioral health intervention in the chronic disease model and the differences in macronutrient percent intake between males and females and how this may affect chronic disease development.
Footnotes
The authors report no funding or conflicts of interest related to this study.
References
- 1.Martinac M, Pehar D, Karlovic D, et al. Metabolic syndrome, activity of the hypothalamic-pituitary-adrenal axis and inflammatory mediators in depressive disorder. Acta Clin Croat. 2014; 53(1):55–71. [PubMed] [Google Scholar]
- 2.Jackson JS, Knight KM, Rafferty JA. Race and unhealthy behaviors: chronic stress, the HPA axis, and physical and mental health disparities over the life course. Am J Public Health. 2010; 100(5):933–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Zhao G, Ford ES, Li C, Tsai J, et al. Waist circumference, abdominal obesity, and depression among overweight and obese U.S. adults: National Health and Nutrition Examination Survey 2005–2006. BMC Psychiatry. 2011;11:130. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Wheelock KM, Sinha M, Knowler WC, et al. Metabolic risk factors and type 2 diabetes incidence in American Indian children. J Clin Endocrinol Metab. 2016;101(4):1437–44. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Dennison ME, Sisson SB, Lora K, et al. Assessment of body mass index, sugar sweetened beverage intake and time spent in physical activity of American Indian children in Oklahoma. J Community Health. 2015;40(4):808–14. [DOI] [PubMed] [Google Scholar]
- 6.Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011–2012. JAMA. 2014;311(8):806–14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Dabelea D, Mayer-Davis EJ, Saydah S, et al. Prevalence of type 1 and type 2 diabetes among children and adolescents from 2001 to 2009. JAMA. 2014;311(17):1778–86. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Foulds HJ, Warburton DE. The blood pressure and hypertension experience among North American indigenous populations. J Hypertens. 2014;32(4):724–34. [DOI] [PubMed] [Google Scholar]
- 9.Kit BK, Kuklina E, Carroll MD, et al. Prevalence of and trends in dyslipidemia and blood pressure among US children and adolescents, 1999–2012. JAMA Pediatr. 2015;169(3):272–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Dennison M, Sisson SB, Morris A. Obesogenic behaviours and depressive symptoms in children: a narrative literature review. Obesity Rev. 2016;17(8):735–57. [DOI] [PubMed] [Google Scholar]
- 11.Bjelland M, Bergh IH, Grydeland M, et al. Changes in adolescents’ intake of sugar-sweetened beverages and sedentary behaviour: results at 8 month mid-way assessment of the HEIA study—a comprehensive, multi-component school-based randomized trial. Int J Behav Nutr Phys Activ. 2011;8:63. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Grossman DC, Bibbins-Domingo K, Curry SJ, et al. Screening for obesity in children and adolescents: US Preventive Services Task Force Recommendation Statement. JAMA. 2017;317(23): 2417–26. [DOI] [PubMed] [Google Scholar]
- 13.Freedman DS, Mei Z, Srinivasan SR, et al. Cardiovascular risk factors and excess adiposity among overweight children and adolescents: the Bogalusa Heart Study. J Pediatr. 2007;150(1):12–7.e2. [DOI] [PubMed] [Google Scholar]
- 14.Ahrens W, Moreno LA, Marild S, et al. Metabolic syndrome in young children: definitions and results of the IDEFICS study. Int J Obesity (2005). 2014;38(suppl 2):S4–14. [DOI] [PubMed] [Google Scholar]
- 15.de Ferranti SD, Gauvreau K, Ludwig DS, et al. Prevalence of the metabolic syndrome in American adolescents: findings from the Third National Health and Nutrition Examination Survey. Circulation. 2004;110(16):2494–7. [DOI] [PubMed] [Google Scholar]
- 16.Cao H, Qian Q, Weng T, et al. Screen time, physical activity and mental health among urban adolescents in China. Prev Med. 2011;53(4–5):316–20. [DOI] [PubMed] [Google Scholar]
- 17.Hoare E, Millar L, Fuller-Tyszkiewicz M, et al. Associations between obesogenic risk and depressive symptomatology in Australian adolescents: a cross-sectional study. J Epidemiol Community Health. 2014;68(8):767–72. [DOI] [PubMed] [Google Scholar]
- 18.Kremer P, Elshaug C, Leslie E, et al. Physical activity, leisure-time screen use and depression among children and young adolescents. J Sci Med Sport Sports Med Aust. 2014;17(2):183–7. [DOI] [PubMed] [Google Scholar]
- 19.Maras D, Flament MF, Murray M, et al. Screen time is associated with depression and anxiety in Canadian youth. Prev Med. 2015. [DOI] [PubMed] [Google Scholar]
- 20.Han E, Powell LM. Consumption patterns of sugar-sweetened beverages in the United States. J Acad Nutr Diet. 2013;113(1):43–53. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Fakhouri TH, Hughes JP, Brody DJ, et al. Physical activity and screen-time viewing among elementary school-aged children in the United States from 2009 to 2010. JAMA Pediatr. 2013; 167(3):223–9. [DOI] [PubMed] [Google Scholar]
- 22.Goldbacher EM, Matthews KA. Are psychological characteristics related to risk of the metabolic syndrome? a review of the literature. Ann Behav Med. 2007;34(3):240–52. [DOI] [PubMed] [Google Scholar]
- 23.Hedrick VE, Savla J, Comber DL, et al. Development of a brief questionnaire to assess habitual beverage intake (BEVQ-15): sugar-sweetened beverages and total beverage energy intake. J Acad Nutr Diet. 2012;112(6):840–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Hedrick VE, Comber DL, Estabrooks PA, et al. The beverage intake questionnaire: determining initial validity and reliability. J Acad Nutr Diet. 2010;110(8):1227–32. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Neumark-Sztainer D, Wall M, Perry C, Story M. Correlates of fruit and vegetable intake among adolescents: findings from Project EAT. Prev Med. 2003;37(3):198–208. [DOI] [PubMed] [Google Scholar]
- 26.DeLong AJ, Larson NI, Story M, et al. Factors associated with overweight among urban American Indian adolescents: findings from Project EAT. Ethnicity Dis. 2008;18(3):317–23. [PubMed] [Google Scholar]
- 27.Project EAT and F-EAT Surveys Psychometrics. Available from: http://sph.umn.edu/pdf/research/epi/eat/EAT2010_FEAT_Psychometrics.pdf.
- 28.Kann L, Kinchen SA, Williams BI, et al. Youth risk behavior surveillance—United States, 1999. MMWR CDC Surveill Summ. 2000;49(5):1–32. [PubMed] [Google Scholar]
- 29.Brener ND, Kann L, Kinchen SA, et al. Methodology of the youth risk behavior surveillance system. MMWR Recommend Rep. 2004;53(Rr-12):1–13. [PubMed] [Google Scholar]
- 30.Nelson MC, Neumark-Stzainer D, Hannan PJ, et al. Longitudinal and secular trends in physical activity and sedentary behavior during adolescence. Pediatrics. 2006;118(6):e1627–34. [DOI] [PubMed] [Google Scholar]
- 31.Larson N, Neumark-Sztainer D, Story M, et al. Identifying correlates of young adults’ weight behavior: survey development. Am J Health Behav. 2011;35(6):712–25. [PMC free article] [PubMed] [Google Scholar]
- 32.Gomez R, Vance A, Gomez A. Children’s Depression Inventory: invariance across children and adolescents with and without depressive disorders. Psychol Assess. 2012;24(1):1–10. [DOI] [PubMed] [Google Scholar]
- 33.Saylor CF, Finch AJ Jr, Spirito A, Bennett B. The Children’s Depression Inventory: a systematic evaluation of psychometric properties. J Consult Clin Psychol. 1984;52(6):955–67. [DOI] [PubMed] [Google Scholar]
- 34.Shape Up America!. Childhood Obesity Assessment Calculator 2013. Available from: www.shapeup.org/oap/entry.php. Accessed 2013.
- 35.US Centers for Disease Control. Body Mass Index: Considerations for practitioners 2013. Available from: http://www.cdc.gov/obesity/downloads/bmiforpactitioners.pdf.
- 36.US National High Blood Pressure Education Program Working Group on Hypertension Control in Children and Adolescents. Update on the 1987 Task Force Report on High Blood Pressure in Children and Adolescents: a working group report from the National High Blood Pressure Education Program. Pediatrics. 1996;98(4 pt 1):649–58. [PubMed] [Google Scholar]
- 37.US National High Blood Pressure Education Program Working Group on Hypertension Control in Children and Adolescents. The fourth report on the diagnosis, evaluation, and treatment of high blood pressure in children and adolescents. Pediatrics. 2004;114(2 suppl 4th report):555–76. [PubMed] [Google Scholar]
- 38.Bassali R, Waller JL, Gower B, et al. Utility of waist circumference percentile for risk evaluation in obese children. Int J Pediatr Obesity. 2010;5(1):97–101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Higgins SP, Freemark M, Prose NS. Acanthosis nigricans: a practical approach to evaluation and management. Dermatol Online J. 2008;14(9):2. [PubMed] [Google Scholar]
- 40.Daniels SR, Greer FR. Lipid screening and cardiovascular health in childhood. Pediatrics. 2008;122(1):198–208. [DOI] [PubMed] [Google Scholar]
- 41.Shephard MD, Mazzachi BC, Shephard AK. Comparative performance of two point-of-care analysers for lipid testing. Clin Lab. 2007;53(9–12):561–6. [PubMed] [Google Scholar]
- 42.Rodbard HW. Diabetes screening, diagnosis, and therapy in pediatric patients with type 2 diabetes. Medscape J Med. 2008; 10(8):184; quiz [PMC free article] [PubMed] [Google Scholar]
- 43.American Diabetes Association. Standards of Medical Care in Diabetes-2016: Summary of Revisions. Diabetes Care. 2016;39 (suppl 1):S4–5. [DOI] [PubMed] [Google Scholar]
- 44.Carter JS, Houston CA, Gilliland SS, et al. Rapid HbA1c testing in a community setting. Diabetes Care. 1996;19(7):764–7. [DOI] [PubMed] [Google Scholar]
- 45.Chan CL, Pyle L, Newnes L, et al. Continuous glucose monitoring and its relationship to hemoglobin A1c and oral glucose tolerance testing in obese and prediabetic youth. J Clin Endocrinol Metab. 2015;100(3):902–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Brar PC, Mengwall L, Franklin BH, Fierman AH. Screening obese children and adolescents for prediabetes and/or type 2 diabetes in pediatric practices: a validation study. Clin Pediatr. 2014;53(8):771–6. [DOI] [PubMed] [Google Scholar]
- 47.Li C, Ford ES, Mokdad AH, Cook S. Recent trends in waist circumference and waist-height ratio among US children and adolescents. Pediatrics. 2006;118(5):e1390–8. [DOI] [PubMed] [Google Scholar]
- 48.Pan Y, Pratt CA. Metabolic syndrome and its association with diet and physical activity in US adolescents. J Am Diet Assoc. 2008;108(2):276–86. [DOI] [PubMed] [Google Scholar]
- 49.Ford ES, Li C, Zhao G. Prevalence and correlates of metabolic syndrome based on a harmonious definition among adults in the US. J Diabetes. 2010;2(3):180–93. [DOI] [PubMed] [Google Scholar]
- 50.Wang YC, Bleich SN, Gortmaker SL. Increasing caloric contribution from sugar-sweetened beverages and 100% fruit juices among US children and adolescents, 1988–2004. Pediatrics. 2008; 121(6):e1604–14. [DOI] [PubMed] [Google Scholar]
- 51.Banfield EC, Liu Y, Davis JS, et al. Poor adherence to us dietary guidelines for children and adolescents in the National Health and Nutrition Examination Survey Population. J Acad Nutr Diet. 2016;116(1):21–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Shomaker LB, Tanofsky-Kraff M, Stern EA, et al. Longitudinal study of depressive symptoms and progression of insulin resistance in youth at risk for adult obesity. Diabetes Care. 2011; 34(11):2458–63. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Bloomgarden ZT. Definitions of the insulin resistance syndrome: the 1st World Congress on the Insulin Resistance Syndrome. Diabetes Care. 2004;27(3):824–30. [DOI] [PubMed] [Google Scholar]
- 54.Golden SH. A review of the evidence for a neuroendocrine link between stress, depression and diabetes mellitus. Curr Diabetes Rev. 2007;3(4):252–9. [DOI] [PubMed] [Google Scholar]
- 55.Coryell WH, Butcher BD, Burns TL, et al. Fat distribution and major depressive disorder in late adolescence. J Clin Psychiatry. 2016;77(1):84–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 56.Ambrosini GL, Oddy WH, Huang RC, et al. Prospective associations between sugar-sweetened beverage intakes and cardiometabolic risk factors in adolescents. Am J Clin Nutr. 2013; 98(2):327–34. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 57.Deshmukh-Taskar P, Nicklas TA, Radcliffe JD, et al. The relationship of breakfast skipping and type of breakfast consumed with overweight/obesity, abdominal obesity, other cardiometabolic risk factors and the metabolic syndrome in young adults: The National Health and Nutrition Examination Survey (NHANES): 1999–2006. Public Health Nutr. 2012:1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58.Moore LL, Singer MR, Bradlee ML, Daniels SR. Adolescent dietary intakes predict cardiometabolic risk clustering. Eur J Nutr. 2016;55(2):461–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 59.Stroehla BC, Malcoe LH, Velie EM. Dietary sources of nutrients among rural Native American and white children. J Am Diet Assoc. 2005;105(12):1908–16. [DOI] [PubMed] [Google Scholar]
- 60.Downs SM, Marshall D, Ng C, Willows ND. Central adiposity and associated lifestyle factors in Cree children. Appl Physiol Nutr Metab. 2008;33(3):476–82. [DOI] [PubMed] [Google Scholar]
- 61.Adams A, Prince R. Correlates of physical activity in young American Indian children: lessons learned from the Wisconsin Nutrition and Growth Study. J Public Health Manag Pract. 2010; 16(5):394–400. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Eisenmann JC, Arnall DA, Kanuho V, McArel H. Growth status and obesity of Hopi children. Am J Hum Biol. 2003;15(6):741–5. [DOI] [PubMed] [Google Scholar]
- 63.Henderson M, Benedetti A, Barnett TA, et al. Influence of adiposity, physical activity, fitness, and screen time on insulin dynamics over 2 years in children. JAMA Pediatrics. 2016; 170(3):227–35. [DOI] [PubMed] [Google Scholar]
- 64.van Ekris E, Altenburg TM, Singh AS, et al. An evidence-update on the prospective relationship between childhood sedentary behaviour and biomedical health indicators: a systematic review and meta-analysis. Obesity Rev. 2016;17(9):833–49. [DOI] [PubMed] [Google Scholar]
- 65.Peng YF, Xiang Y, Wei YS. The significance of routine biochemical markers in patients with major depressive disorder. Sci Rep. 2016;6:34402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Lieberman HR, Kellogg MD, Kramer FM, et al. Lipid and other plasma markers are associated with anxiety, depression, and fatigue. Health Psychol. 2012;31(2):210–6. [DOI] [PubMed] [Google Scholar]
