Feb 4, 2018 - Background Boys with autism spectrum disorder (ASD) have lower bone mineral .... offices, the Internet, advertisement within the hospital, and.
RESEARCH
Original Research: Brief
Nutrition and Bone Density in Boys with Autism Spectrum Disorder Ann M. Neumeyer, MD; Natalia Cano Sokoloff, MD; Erin I. McDonnell; Eric A. Macklin, PhD; Christopher J. McDougle, MD; Tara M. Holmes, MS, RD, CSP, LDN, CBDT; Jane L. Hubbard, MS, RD, LDN, CBDT; Madhusmita Misra, MD ARTICLE INFORMATION Article history: Submitted 17 July 2017 Accepted 7 November 2017 Available online 4 February 2018
Keywords: Autism spectrum disorder Nutrient intake Bone mineral density Physical activity 2212-2672/Copyright ª 2018 by the Academy of Nutrition and Dietetics. https://doi.org/10.1016/j.jand.2017.11.006
ABSTRACT Background Boys with autism spectrum disorder (ASD) have lower bone mineral density (BMD) than typically developing controls. Differences in diet and exercise may contribute to low BMD. Objective Our aim was to examine macro- and micronutrient intakes and self-reported physical activity in boys with ASD compared to TDC and the relationship of these variables with BMD. Design/methods We conducted a cross-sectional study of 49 boys (25 ASD, 24 typically developing controls) assessed for 3-day food records and physical activity records, and BMD of the whole body less head, hip, and spine using dual-energy x-ray absorptiometry. Fasting levels of 25(OH) vitamin D and calcium were obtained. Participants Participants were adolescent boys, aged 8 to 17 years, recruited from a clinic population (ASD) or community advertisements (ASD and typically developing controls) matched for age. Results ASD participants were approximately 9 months younger than typically developing control participants on average. Body mass index and serum vitamin D and calcium levels were similar. Boys with ASD consumed 16% fewer calories, with a larger percentage obtained from carbohydrates, and 37% less animal protein and 20% less fat than typically developing controls. A lower proportion of ASD participants were categorized as “very physically active” (27% vs 79%; P0.99
0.06 (1.53 to 1.64)
0.94
>0.99
1.22 (1.21 to 3.65)
0.32
>0.99
Total PUFA, g/kg
0.36 (0.03)
0.37 (0.03)
4.46 (23.90 to 19.96)
0.69
>0.99
11.96 (30.75 to 11.92)
0.30
>0.99
Calories from PUFA, %
7.99 (0.39)
7.22 (0.45)
0.77 (0.39 to 1.93)
0.19
>0.99
0.71 (0.69 to 2.11)
0.32
>0.99
Total dietary fiber, g/kg
0.34 (0.03)
0.39 (0.03)
13.02 (31.17 to 9.91)
0.24
>0.99
24.15 (40.02 to 4.09)
0.021*
0.52
Soluble dietary fiber, g/kg
0.11 (0.01)
0.12 (0.01)
12.94 (31.04 to 9.92)
0.24
>0.99
22.57 (38.51 to 2.50)
0.030*
0.62
Insoluble dietary fiber, g/kg
0.23 (0.02)
0.26 (0.02)
12.74 (32.73 to 13.19)
0.30
24.88 (43.16 to 0.71)
0.044*
0.84
Pectins, g/kg
0.03 (0.00)
0.04 (0.01)
17.72 (42.82 to 18.39)
0.29
22.09 (48.29 to 17.40)
0.23
g
>.099 >0.99
>0.99
Intake from food and supplements May 2018 Volume 118 Number 5
Energy, kcal
2,050 (95.2) 2,430 (120.3) 15.67 (26.08 to 3.79)
Total carbohydrate, g/kg
5.35 (0.40)
5.88 (0.38)
9.01 (25.33 to 10.87)
0.011* 0.35
0.25
10.59 (22.62 to 3.31)
0.13
>0.99
>0.99
17.60 (32.76 to 0.96)
0.062
>0.99
Total protein, g/kg
1.41 (0.09)
1.95 (0.13)
27.77 (39.43 to 13.87) 0.99
0.089
0.003* >0.99
(continued on next page)
RESEARCH
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Table 2. Daily macronutrient intake in boys with autism spectrum disorder vs typically developing controls
Estimates and P values are reported from generalized estimating equation models that accounted for covariance among siblings and included either age or age and log-transformed Oxford Physical Activity Questionnaire physical activity levels as covariates. b ASD¼autism spectrum disorder. c TDC¼typically developing control. d Both nominal P values and P values corrected for multiple comparisons using a step-down Bonferroni-adjustment are reported. e SFA¼saturated fatty acid. f MUFA¼monounsaturated fatty acid. g PUFA¼polyunsaturated fatty acid. *P0.99 0.30 12.74 (32.73 to 13.19) 0.26 (0.02) 0.23 (0.02) Insoluble dietary fiber, g/kg
a
0.62
0.52
22.57 (38.51 to 2.50) >0.99
0.030*
24.15 (40.02 to 4.09) >0.99
0.36 0.12 (0.01)
10.74 (30.10 to 14.00)
0.39 (0.03)
0.11 (0.01)
May 2018 Volume 118 Number 5
Soluble dietary fiber, g/kg
Total dietary fiber, g/kg
0.35 (0.03)
12.08 (30.59 to 11.37)
0.29
0.021*
>0.99 0.30 11.79 (30.57 to 12.06) >0.99 0.71 0.37 (0.03) PUFA, g/kg
0.36 (0.03)
4.20 (23.65 to 20.21)
Nominal Corrected P valued P valued Nominal Corrected ASD vs TDC, P valued P valued difference (95% CI) ASD vs TDC, difference (95% CI) TDCc ASDb Variable
Results from Models Adjusting for Agea
Table 2. Daily macronutrient intake in boys with autism spectrum disorder vs typically developing controls (continued)
Results from Models Adjusting for Age and Physical Activitya
RESEARCH physical activity in addition to age, neither consumption of carbohydrates nor consumption of total fat differed between study groups. Our findings were similar for macronutrient intake from food and supplements.
Micronutrient Intake. Table 3 compares daily micronutrient intake in ASD vs typically developing control participants, adjusting for age. Evaluating food intake alone, boys with ASD consumed significantly less calcium, iron, phosphorous, selenium, vitamins A, riboflavin, niacin, vitamin B-6, vitamin B-12, and dietary folate equivalents, with deficiencies ranging from 19% to 35%. Marginal deficiencies were also observed in copper, magnesium, thiamin, and vitamin D (P0.99
9.69 (24.79 to 8.45)
0.28
>0.99
0.73
20.91 (37.95 to 0.82)
0.058
>0.99
>0.99
16.07 (29.67 to 0.16)
0.052
>0.99
0.004*
28.63 (41.73 to 12.59) 0.001*
0.048*
Selenium, mg
104.17 (4.82)
132.74 (6.80)
21.53 (31.07 to 10.66) 0.99
Thiamin, mg
1.73 (0.16)
2.11 (0.11)
17.96 (33.21 to 0.78)
0.059
17.13 (33.93 to 3.96)
0.10
>0.99
Riboflavin, mg
1.77 (0.16)
2.60 (0.20)
31.86 (46.03 to 13.98)
0.001*
0.050
29.18 (48.42 to 2.76)
0.033*
>0.99
Niacin (vitamin B-3), mg
22.04 (1.53)
27.84 (1.91)
20.83 (33.74 to 5.41)
0.010*
0.33
23.19 (40.01 to 1.64)
0.037*
>0.99
Vitamin B-6 (pyridoxine, pyridoxyl, and pyridoxamine), mg
1.78 (0.14)
2.29 (0.17)
22.20 (37.25 to 3.54)
0.022*
0.66
29.69 (48.09 to 4.78)
0.023*
0.91
>0.99
Vitamin B-12 (cobalamin), mg
4.37 (0.54)
6.01 (0.59)
27.32 (46.66 to 0.97)
0.043*
Dietary folate equivalent, mg
496.21 (49.81)
697.80 (41.05)
28.89 (43.01 to 11.26)
0.003*
>0.99
0.099
0.67
28.34 (48.88 to 0.45)
0.053
>0.99
26.73 (44.36 to 3.52)
0.027*
>0.99
Vitamin C (ascorbic acid), mg
68.32 (11.03)
76.07 (14.09)
10.19 (43.81 to 43.56)
0.65
>0.99
4.44 (50.42 to 84.16)
0.89
>0.99
Vitamin D (calciferol), mg
4.62 (0.78)
6.35 (0.86)
27.30 (52.24 to 10.67)
0.14
>0.99
24.51 (54.48 to 25.22)
0.28
>0.99
Vitamin E (total a-tocopherol), mg
9.27 (1.04)
8.31 (0.75)
11.49 (16.25 to 48.42)
0.46
>0.99
13.54 (23.60 to 68.73)
0.53
>0.99
Vitamin K, mg
67.61 (9.72)
82.67 (13.19)
18.22 (46.01 to 23.87)
0.34
>0.99
12.77 (52.83 to 61.29)
0.66
>0.99
Phytic acid, mg
622.00 (63.60)
719.96 (54.77)
13.61 (32.56 to 10.68)
0.25
>0.99
18.49 (37.96 to 7.10)
0.14
>0.99
Oxalic acid, mg
139.47 (15.64)
154.88 (16.09)
9.95 (33.28 to 21.54)
0.49
>0.99
0.72
>0.99
7.11 (37.83 to 38.78)
May 2018 Volume 118 Number 5
Daidzein, mg
0.11 (0.05)
0.13 (0.05)
15.94 (71.14 to 144.84)
0.75
>0.99
13.28 (78.15 to 244.22)
0.84
>0.99
Genistein, mg
0.14 (0.06)
0.22 (0.07)
38.35 (77.50 to 68.90)
0.35
>0.99
36.97 (82.74 to 130.21)
0.48
>0.99
rate (95% CI)! f
ORg (95% CI)!
OR (95% CI) !
Meeting EAR for calcium, %
28.0 (12.9 to 50.6) 75.0 (53.5 to 88.)
0.1 (0.0 to 0.5)
0.004*
Meeting EAR for vitamin D, %
12.1 (3.0 to 38.4)
0.2 (0.0 to 1.3)
0.1
36.3 (21.8 to 53.8)
0.13
0.2 (0.0 to 1.1)
0.061
>0.99
>0.99
0.2 (0.0 to 1.6)
0.13
>0.99
(continued on next page)
RESEARCH
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Table 3. Daily micronutrient intake in boys with autism spectrum disorder vs typically developing controls
May 2018 Volume 118 Number 5
Table 3. Daily micronutrient intake in boys with autism spectrum disorder vs typically developing controls (continued) Results from Models Adjusting for Agea Variable Intake from food and supplements
ASDb
TDCc
ASD vs TDC, difference (95% CI)
Adjusted for Age and Physical Activitya Nominal Corrected ASD vs TDC, P valued P valued difference (95% CI)
Nominal Corrected P valued P valued
mean (SE)!
Calcium, mg
917.54 (103.86)
1,339.03 (88.97)
0.053
>0.99
Copper, mg
1.13 (0.08)
1.24 (0.06)
31.48 (47.22 to 11.04) 9.26 (23.20 to 7.20)
0.25
>0.99
7.12 (23.54 to 12.82)
0.46
>0.99
Iron, mg
16.61 (1.51)
18.33 (1.00)
9.39 (26.34 to 11.47)
0.35
>0.99
11.95 (31.86 to 13.77)
0.33
>0.99
Magnesium, mg
279.08 (22.97)
314.32 (15.56)
11.21 (25.97 to 6.49)
0.20
>0.99
13.00 (27.84 to 4.89)
0.14
>0.99
Phosphorus, mg
1,158.12 (82.94)
1,623.77 (79.95)
28.68 (39.89 to 15.37) 0.99
0.005*
0.005*
Thiamin, mg
1.86 (0.18)
2.11 (0.11)
11.76 (29.26 to 10.08)
0.27
Riboflavin, mg
1.96 (0.18)
2.60 (0.20)
24.62 (40.69 to 4.19)
0.021
Niacin (vitamin B3), mg
24.28 (1.84)
27.85 (1.91)
12.83 (28.12 to 5.71)
Vitamin B-6 (pyridoxine, pyridoxyl, and pyridoxamine), mg
2.05 (0.19)
2.32 (0.18)
0.16
>0.99
30.02 (51.26 to 0.47)
0.049*
0.33
>0.99
22.32 (43.63 to 7.04)
0.12
>0.99
0.16
>0.99
16.07 (34.61 to 7.73)
0.17
>0.99
11.88 (31.02 to 12.57)
0.31
>0.99
18.40 (41.26 to 13.36)
0.23
>0.99
13.96 (37.93 to 19.27)
0.37
>0.99
10.54 (37.31 to 27.66)
0.54
>0.99
12.27 (33.98 to 90.91)
0.67
>0.99
22.37 (40.23 to 150.57)
0.58
>0.99
1.11 (34.54 to 56.19)
0.96
>0.99
16.10 (28.48 to 88.47)
0.55
>0.99
Vitamin B-12 (cobalamin), mg
5.25 (0.68)
6.10 (0.63)
Vitamin C (ascorbic acid), mg
85.96 (17.59)
76.57 (14.25)
Vitamin D (calciferol), mg
6.94 (1.14)
6.86 (0.99)
Vitamin E (total a-tocopherol), mg
9.27 (1.04)
8.31 (0.75)
11.49 (16.25 to 48.42)
0.46
>0.99
13.54 (23.60 to 68.73)
0.53
>0.99
Vitamin K, mg
68.99 (10.07)
82.66 (13.19)
16.54 (45.07 to 26.80)
0.40
>0.99
11.06 (52.07 to 65.02)
0.71
>0.99
Phytic acid, mg
622.00 (63.60)
719.96 (54.77)
13.61 (32.56 to 10.68)
0.25
>0.99
18.49 (37.96 to 7.10)
0.14
>0.99
Daidzein, mg
0.11 (0.05)
0.13 (0.05)
15.94 (71.14 to 144.84)
0.75
>0.99
13.28 (78.15 to 244.22)
0.84
>0.99
Genistein, mg
0.14 (0.06)
0.22 (0.07)
38.35 (77.50 to 68.90)
0.35
>0.99
36.97 (82.74 to 130.21)
0.48
>0.99
Meeting EAR for calcium, %
32.7 (16.3 to 54.9) 74.6 (54.6 to 87.7)
0.2 (0.0 to 0.6)
0.006*
Meeting EAR for vitamin D, %
36.1 (18.9 to 57.7) 41.6 (26.4 to 58.5)
0.8 (0.3 to 2.4)
0.68
rate (95% CI)!
OR (95% CI) !
OR (95% CI) ! 0.22
0.2 (0.0 to 1.1)
0.061
>0.99
>0.99
0.9 (0.2 to 3.6)
0.88
>0.99
Estimates and P values are reported from generalized estimating equation models that accounted for covariance among siblings and included either age or age and log-transformed Oxford Physical Activity Questionnaire physical activity levels as covariates. b ASD¼autism spectrum disorder. c TDC¼typically developing control. d Both nominal P values and P values corrected for multiple comparisons using a step-down Bonferroni-adjustment are reported. e SE¼standard error. f EAR¼Estimated Average Requirement. g OR¼odds ratio. *P
