Nutritional Status of Children With Autism Spectrum Disorders (Asds) : A Case-Control Study

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 14

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/265393430

Nutritional Status of Children with Autism Spectrum Disorders (ASDs): A


Case–Control Study

Article  in  Journal of Autism and Developmental Disorders · September 2014


DOI: 10.1007/s10803-014-2205-8 · Source: PubMed

CITATIONS READS

39 899

5 authors, including:

Salvador Marí-Bauset Itziar Zazpe


University of Valencia Universidad de Navarra
19 PUBLICATIONS   237 CITATIONS    81 PUBLICATIONS   1,767 CITATIONS   

SEE PROFILE SEE PROFILE

Amelia Mari-Sanchis Maria Morales Suárez-Varela


Complejo Hospitalario de Navarra University of Valencia
20 PUBLICATIONS   298 CITATIONS    307 PUBLICATIONS   3,540 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

FACTORES DE RIESGO PRENATALES, PERINATALES Y NEONATALES EN EL DESARROLLO DEL TRASTORNO DEL ESPECTRO AUTISTA View project

Hazardous waste, nursing, dyalisis, environment View project

All content following this page was uploaded by Salvador Marí-Bauset on 23 May 2016.

The user has requested enhancement of the downloaded file.


636976
research-article2016
AUT0010.1177/1362361316636976AutismMarí-Bauset et al.

Original Article
Autism

Comparison of nutritional status between 1­–13


© The Author(s) 2016
Reprints and permissions:
children with autism spectrum disorder sagepub.co.uk/journalsPermissions.nav
DOI: 10.1177/1362361316636976

and typically developing children in the aut.sagepub.com

Mediterranean Region (Valencia, Spain)

Salvador Marí-Bauset1,2, Agustín Llopis-González1,2,3,


Itziar Zazpe4,5, Amelia Marí-Sanchis6 and
Maria Morales Suárez-Varela1,2,3

Abstract
This case-control study investigated nutrient intake, healthy eating index with 10 items on foods and nutrients, on
3-day food diaries and anthropometric measurements in 105 children with autism spectrum disorder and 495 typically
developing children (6–9 years) in Valencia (Spain). Children with autism spectrum disorder were at a higher risk for
underweight, eating more legumes, vegetables, fiber, and some micronutrients (traditional Mediterranean diet) but fewer
dairy and cereal products, and less iodine, sodium, and calcium than their typically developing peers. Differences existed
in total energy intake but healthy eating index and food variety score differences were not significant. Autism spectrum
disorder group failed to meet dietary recommendations for thiamin, riboflavin, vitamin C, or calcium. Risk of inadequate
intake of fiber, vitamin E, and sodium was lower in children with autism spectrum disorder than typically developing
children. Results suggest that (1) risk of inadequate intake of some micronutrients in children with autism spectrum
disorder and (2) cultural patterns and environment may influence food intake and anthropometric characteristics in
autism spectrum disorder. Primary care should include anthropometric and nutritional surveillance in this population
to identify intervention on a case-by-case basis. Future research should explore dietary patterns and anthropometric
characteristics in different autism spectrum disorder populations in other countries, enhancing our understanding of the
disorder’s impact.

Keywords
autism, autism spectrum disorder, feeding assessment, growth, healthy eating index, nutrition

Introduction
Autism spectrum disorder (ASD) is a neurodevelopmental have been observed in many studies over the years.
condition characterized by poor social-emotional reciproc- However, “food selectivity” is used in the literature to refer
ity, impairments in language, and repetitive, stereotyped to a range of concepts including, for example, food refusal,
behaviors (American Psychiatric Association (APA),
2014). Its prevalence has significantly increased in the last 1University of Valencia, Spain
few decades (Matson and Kozlowski, 2011). In 2010, 2CIBERESP, Institute of Health Carlos III, Spain
3Center for Public Health Research (CSISP-FISABIO), Spain
overall ASD prevalence in the United States was 14.7 per
4University of Navarre, Spain
1000 (one in 68) children aged 8 years, and the male-to- 5CIBERobn, Institute of Health Carlos III, Spain
female ratio was 5:1 (Centers for Disease Control and 6Clinical Nutrition and Dietetics Unit, Spain
Prevention (CDC), 2014).
Eating is among the most essential of human activities, Corresponding author:
Maria Morales Suárez-Varela, Unit of Public Health and Environmental
necessary not only to sustain life but also to ensure proper Care, Department of Preventive Medicine, University of Valencia, Avd.
development. In this context, behavioral problems in chil- Vicente Andres Estellés s/n, Burjassot, 46100 Valencia, Spain.
dren with ASD at meal times, including food selectivity, Email: maria.m.morales@uv.es

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


2 Autism

a limited repertoire of accepted foods, high-frequency sin- with ASD (n = 272) from the population of all primary-age
gle food intake, excessive intake of a few foods (Bandini children with ASD in the metropolitan area of Valencia
et al., 2010; Hubbard et al., 2014), or selective intake of (Spain), attending special schools and primary schools
certain food categories (such as carbohydrates or fats or with inclusion classes for children with this disorder.
proteins (Attlee et al., 2015). The lack of consensus regard- Candidate TD children (n = 1364) were identified from the
ing the definition of selectivity complicates the assessment population of all pupils (n = 15,838) at the inclusive ele-
and comparison of results from different studies. Atypical mentary schools attended by some of the children with
feeding behaviors, adoption of intentional diet restrictions, ASD. After visiting all the schools and identifying the
and the peculiar lifestyle of individuals with ASD (with not number of classrooms per academic year, we constructed a
only different levels of physical activity, but also idiosyn- stratified randomization table and randomly assigned eli-
cratic social skills and poor social interaction) are factors gible participants, balanced by school and classroom.
that imply risks of both excessive and insufficient intakes The Ethics Committee of the Dr Peset University
(Twachtman-Reilly et al., 2008). Notably, negative effects Hospital (Valencia, Spain) approved this study (ref. 46/10).
on anthropometric development, such as unhealthy weight In the first appointment, before we started the research, we
and/or body mass index (BMI), could have adverse conse- explained the study to the parents of all the children
quences due to the incidence of significant comorbid involved, including the tests that would be carried out. We
chronic conditions in the third or fourth decade of life (e.g. also informed them that the data collected would be kept
osteoporosis, hypertension, dyslipidemia, cardiovascular confidential in line with the Spanish data protection law,
disease, diabetes, and high blood pressure), or even earlier and we requested informed consent from both parents or
(sleep apnea, menstrual disorders, or psychosocial disor- whichever parent accompanied the child at the time of the
ders). To date, research on growth in children with ASD has visit. If the parents gave consent and the children met the
been inadequate with inconsistent, or even contradictory, selection criteria, an appointment was arranged for assess-
results as reported in a systematic review by Marí-Bauset ments of the children.
et al. (2015b). ASD diagnoses were based on results of the Autism
Macro- and micronutrient intakes of foods have been Diagnostic Observation Schedule-Generic (ADOS-G) (Le
compared between children with ASD and their typically Couteur et al., 2008; Lord et al., 2000) and the Autism
developing (TD) peers. Nearly three decades ago, a nutri- Diagnostic Interview-Revised (ADI-R) (Lord et al., 1994)
tional assessment of children with ASD found overall intake from the clinical opinion of experienced clinical psychol-
adequacy to be comparable to that in controls (Raiten and ogists. We only considered diagnosis, and not disorder
Massaro, 1986), and similar conclusions have been drawn severity.
more recently by other authors (Schmitt et al., 2008; Staff on the local education board indicated that all the
Zimmer et al., 2012). On the other hand, several authors children (with and without ASD) had similar socio-eco-
(Bandini et al., 2010; Emond et al., 2010; Ho et al., 1997; nomic backgrounds. We cannot rule out the possibility of
Hyman et al., 2012) have reported that intakes of some there being children with high-functioning ASD among
nutrients are insufficient: vitamins A, C, B6, B12, D, E, or K, or the controls, but this risk is very low as clinical psycholo-
folate, phosphorous, fiber, zinc, calcium, or iron). Overall, the gists routinely assess all the pupils at the schools from
data available are currently insufficient and therefore, there is which TD children were recruited. On the other hand, in
no clear consensus on whether nutritional intake is generally schools where children with ASD attend, behavioral inter-
impaired in children with ASD or regarding the potential con- ventions are implemented by psycho-education specialists
sequences of this in terms of their development. trained in specific techniques to address feeding problems
We hypothesized that, in general, children with ASD in children with this disorder.
would (1) have lower anthropometric measurements To be included in the study, both the children with ASD
(height, weight, and calculated BMI); (2) have lower food and the TD children were required to be 6–9 years old (the
intake of macro- and micronutrients; (3) have lower Spanish DRIs, the same in this age group for both gen-
healthy eating index (HEI) scores, overall and for food ders). The exclusion criteria for both groups were as fol-
variety; and (4) meet Spanish Dietary Reference Intakes lows: use of dietary supplements; any medical condition
(DRIs) less often than TD children. To test these hypothe- (endocrine, metabolic diseases, etc.) that could influence
ses, we aimed to characterize the nutritional status of chil- food intake, and/or physical activity habits; use of drugs
dren diagnosed with ASD. (e.g. stimulants, atypical antipsychotics, tricyclic antide-
pressants, steroids, and mood stabilizers) that could affect
food intake; not attending study interview appointments;
Methods and not completing nutritional records properly.
For both groups, we first excluded families who
Participants declined to participate, then applied the selection criteria
This case-control study of children with ASD and their TD set out above, and subsequently excluded those who we
peers was carried out in Valencia (eastern area of Spain) in were unable to contact and/or failed to complete nutri-
the second half of 2014. We identified candidate children tional records (see below). Figure 1 illustrates the flow

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


Marí-Bauset et al. 3

Figure 1.  Flow diagram of participants through the study (STROBE statement).
Symbol “*” indicates some children met more than one exclusion criterion, and hence the subgroups sum to more than the total.

of children in both groups through the study (in accord- assess the food and drink their child consumed by record-
ance with the Strengthening the Reporting of ing estimated portion sizes (measured or assessed accord-
Observational Studies in Epidemiology (STROBE) state- ing to a visual guide provided to improve accuracy) for
ment; Vandenbroucke et al., 2007). each food item. The same training was given to caregivers
in the school dining halls. Parents were asked to hand in
food labels with ingredients, added ingredients, brands, and
Data collection recipes for homemade dishes, whenever possible. The
Examination protocol and measurements researchers contacted parents by telephone if there were
any incomplete or missing data.
During appointments, the following data were collected by
administering a questionnaire to parents: child’s age, back-
Anthropometric measurements
ground of the child’s birth, and child’s medical history. If
they met the selection criteria, the children were included, During the scheduled appointment, the principal investi-
and we gave their parents a detailed explanation of how to gator himself, a registered dietitian, measured the height

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


4 Autism

(in centimeters) and weight (in kilograms) of the child (EARs), adequate intakes (AIs), tolerable upper intake lev-
using standard anthropometric techniques (World Health els (ULs), and acceptable macronutrient distribution
Organization, 1996) with a Seca 213® stadiometer and ranges (AMDRs). We classified children as being at risk of
Seca 813® scale, respectively. Both measurements were having inadequate intake for specific nutrients depending
taken in duplicate and the mean values were used to calcu- on whether they met DRIs and Spanish nutritional targets
late BMI (kg/m2). BMI (kg/m2) was converted into a or not (Federación Española de Sociedades de Nutrición,
z-score with the WHO Anthro software, v.3.2. (Onis et al., Alimentación y Dietética (FESNAD), 2010). Comparisons
2007). Based on the percentile ranking, BMI status was were made with the DRIs used in the United States (IOM,
categorized, using National Health and Nutrition 2010) to examine any differences. Intake distributions
Examination Survey (NHANES) criteria, into the follow- were adjusted for day-to-day variation using a statistical
ing four categories: underweight (⩽5th percentile); healthy modeling approach (National Research Council (NCR),
(>5th to <85th percentiles); overweight (⩾85th to <95th 1985). We used this approach to ensure that data reflected
percentiles); and obese (⩾95th percentile) (CDC, 2000). usual intake. The probability of adequacy for usual nutri-
ent intake was calculated as z-score = (estimated nutrient
intake − EAR)/SD of EAR (Carriquiry, 1999). Applying
Dietary assessment
these statistical approaches, intake of beneficial nutrients
On a form provided, parents were asked to record all the was considered adequate if covering at least the AMDR for
foods and drinks that their child consumed over a 3-day macronutrients, the EAR (or AI as appropriate) for micro-
period, including one nonworking day (Barrett-Connor, nutrients, and the EER for energy. For nutrients presumed
1991; Institute of Medicine (IOM), 2001). In order to cal- to be detrimental (e.g. total fat, cholesterol, and sodium),
culate intakes of calories, and macro- and micronutrients the opposite interpretation was applied, which means the
of known public health relevance, researchers entered data diet was considered inadequate if the limit was exceeded,
from these food records into an open-source computer pro- and adequate if the intake was below the limit.
gram, DIAL®. This program, developed by the Department
of Nutrition and Dietetics at the Complutense University
Statistical analysis
of Madrid, is widely used in Spain and has previously been
validated to assess diets and manage nutritional data. It For anthropometric measures, we compared the two study
includes a list of fortified/enriched foods commonly avail- groups in the four BMI categories (underweight, healthy,
able in Spain, to which other items can be added. With this overweight, and obese), applying Bonferroni corrections
feature, we included the nutritional composition of pack- to control for multiple comparisons. The probabilistic
aged foods according to the food labels that parents sub- approach and the EAR cut-point method were used to
mitted. The results were compared with Spanish food assess risk of the inadequacy of nutrient intakes. A
composition tables (Moreiras et al., 2013). Student’s t-test was run to compare the nutritional intakes
DIAL also calculates the HEI (Kennedy et al., 1995) in children with ASD versus TD children. With dichoto-
from the data supplied. The HEI consists of 10 items: 1–5 mous categorical variables, we compared the diet of the
concerning the intake of five major food group categories, children with ASD with recommended intakes (recom-
cereals, fruit, vegetables, dairy products, and meat; and mendations met, not at risk vs not met, at risk) using con-
6–10 related to nutritional recommendations, total fats, tingency tables, odds ratios (ORs), and the χ2 test (or
saturated fats, cholesterol, salt, and food variety. We classi- Fisher’s exact test, as required) to assess statistical signifi-
fied individuals into three groups: scores >80 points were cance. The Shapiro–Wilk test was used to confirm assump-
considered to indicate a “healthy” diet; 50–80 points indi- tions of normality, linearity, homoscedasticity, and
cated “needs to improve”; and ⩽50 points corresponded to independence. We fitted four multivariable-adjusted mod-
a “poor” diet (Kennedy et al., 1995). Component 10 of the els for each dietary variable to control the following poten-
HEI assesses variety in diet. Higher scores indicated the tial sources of bias: (1) age (continuous) and gender (two
child ate more different food items contributing at least half categories); (2) the aforementioned variables, plus weight
a serving to any of the food groups: a score of 0 correspond- (continuous) and height (continuous); (3) the aforemen-
ing to ⩽6 foods over the 3 days; and a score of 10 to ⩾16 tioned variables, plus total energy intake (continuous); and
foods (Kennedy et al., 1995). An intake of ⩾11 foods dur- (4) the aforementioned variables and diet type (two cate-
ing this period (score = 5) was considered the cut-off, sug- gories: a gluten-free casein-free diet and a regular diet).
gesting a high likelihood of adequate micronutrient intake. We compared the intakes in the two groups with multi-
ple linear regression by taking nutrients as the dependent
(continuous) variable to generate the corresponding β
Estimating nutrient adequacy/deficiency regression coefficients and 95% confidence intervals
DRIs (IOM, 2001, 2003; Murphy and Barr, 2011) include (CIs), using the TD children as the reference category. We
estimated energy requirements (EERs), recommended die- used logistic regression models to evaluate the inadequacy
tary allowances (RDAs), estimated average requirements of the DRIs or nutritional targets in all the children, again

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


Marí-Bauset et al. 5

Table 1.  Main characteristics of children with autism spectrum disorder (ASD) and typically developing (TD) children.a

Main Children with ASD (n = 105) TD children (n = 495) p value


characteristics
N (%) Boys n (%) Boys Total Girls Boys

Total Mean Total Mean


(SD) (SD)

Girls Girls
105 (100) 12 (11) 93 (89) 495 (100) 229 (46) 266 (54)
Age (months) 93.68 (14.76) 100.58 (17.47) 93.78 (14.24) 95.46 (13.51) 96.34 (13.24) 94.71 (13.72) 0.22 0.29 0.25
Weight (kg) 28.3 (7.64) 29.19 (6.98) 28.19 (7.75) 29.77 (7.04) 29.90 (7.29) 29.65 (6.83) 0.05 0.74 0.08
Height (cm) 126.62 (9.54) 126.92 (9.30) 126.58 (9.62) 129.10 (9.03) 128.66 (8.76) 129.48 (9.25) 0.012 0.54 0.004
BMI (kg/m2) 17.42 (3.06) 17.88 (2.62) 17.36 (3.12) 17.67 (2.65) 17.84 (2.72) 17.52 (2.60) 0.44 0.96 0.67
BMI z-score 0.69 (1.50) 1.02 (1.23) 0.65 (1.53) 0.82 (1.20) 0.89 (1.19) 0.76 (1.20) 0.37 0.71 0.53
kcal/day 1955 (288) 2056 (345) 1942 (279) 1961 (288) 1975 (292) 1948 (283) 0.86 0.62 0.85
HEI 65.32 (10.79) 65.69 (9.95) 65.27 (10.94) 66.17 (10.22) 67.01 (10.04) 65.45 (10.34) 0.43 0.66 0.89
Food variety 3.72 (2.60) 3.50 (2.71) 3.75 (2.61) 3.53 (2.31) 3.44 (2.29) 3.62 (2.31) 0.45 0.93 0.65
score

BMI: body mass index; HEI: healthy eating index; SD: standard deviation.
aStudent’s t-test was used to compare values for children with ASD and TD children (p < 0.05 being considered significant).

taking the TD children as the reference category. We esti- with ASD (2 girls, 17% vs 7 TD girls, 3%; OR: 4.88, 95%
mated the crude and multivariate-adjusted ORs with 95% CI: 0.91–26.33), the sample size was too small to draw
CIs as follows: failing to comply with these recommenda- conclusions. In the other BMI categories, no significant
tions (OR > 1). All the p values were two-tailed. Statistical differences were found between the groups.
significance was set at the conventional cut-off (p < 0.05). The HEI scores were similar in the two groups, all the
Data were entered into an Excel spreadsheet, using children’s diets being classified as “needs to improve.”
double-data entry to minimize the risk of errors. Data were Then, considering individual scores, we found that only
then transferred to IBM SPSS Statistics for Windows, ver- 9% of children with ASD (n = 9) and 6% of TD children
sion 19, for the statistical analysis. (n = 31) consumed poor diets (χ2 = 0.74; p = 0.39). On com-
ponent 10 of the HEI assessing variety in diet, percentages
of children failing to reach the cut-off for adequate food
Results variety were similar in the two groups: 64% of children
with ASD (n = 67) and 65% TD children (n = 323) ate ⩽11
Final samples foods over 3 days (χ2 = 0.08; p = 0.78); and mean food vari-
A final sample of 105 children with ASD, 93 (89%) boys ety scores were also similar with means (standard devia-
and 12 (11%) girls, completed the study. The final sample tion (SD)) of 3.72 (2.60) versus 3.53 (2.31), respectively
size of TD children was 495, 266 (54%) boys and 229 (p = 0.45), both of which can be considered limited.
(46%) girls. This ratio of cases and controls (1:4.71) is in
line with Wacholder et al. (1992).
Analysis of nutrients and food groups
Table 1 compares the crude data on characteristics of
the participants: age, anthropometric parameters, total Children with ASD had much higher intakes of fiber,
energy intake, and the HEI scores (overall and for food folate, vitamins E and K, and iron, and a lower intake of
variety) per group, overall and by gender. Analyzing the calcium than controls. The crude mean nutrient intakes in
anthropometric data, the only statistically significant dif- both groups are reported in detail in Supplementary Online
ferences were in height: children with ASD overall Table 1.
(p = 0.012) and boys (p = 0.004) were shorter than their TD Table 2 summarizes comparisons between the groups
peers. Subsequently, children with ASD were compared to adjusted for age, gender, height, weight, total energy, and
the controls by BMI category, with TD children as the ref- diet type (on gluten-free casein-free diet or not). Children
erence category, and the analysis indicated an underweight with ASD ate considerably fewer cereals and dairy prod-
status in 12 (11%) children with ASD versus 20 (4%) TD ucts, but more legumes and vegetables than TD children.
children (OR: 3.03, 95% CI: 1.42–6.45; p < 0.008) overall After adjustments with linear regression, in addition to
and in 10 (11%) boys with ASD versus 13 (5%) TD boys fiber, folate, vitamins E and K, and iron, their intakes of
(OR: 2.39, 95% CI: 1.01–5.69; p < 0.04). Although there vitamin B6, zinc, magnesium, and potassium were found to
was also a higher risk of being underweight among girls be significantly higher, while intakes of calcium, iodine,

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


6

Table 2.  Linear multiple regression analysis.a

Crude Multivariable 1 Multivariable 2 Multivariable 3 Multivariable 4

  Coeff. ß 95% CI Coeff. ß 95% CI Coeff. ß 95% CI Coeff. ß 95% CI Coeff. ß 95% CI
Cereals (g) −21.02 −32.57 to −9.48** −22.75 −33.96 to −11.55** −19.43 −30.25 to −8.61** −18.98 −28.65 to −9.31** −20.01 −30.45, −9.58**
Legumes (g) 38.03 23.29–52.77** 39.36 24.02–54.69** 39.34 23.9–54.77** 39.28 23.84–54.72** 21.17 4.98, 37.36*
Vegetables (g) 23.96 7.6–40.33* 28.29 11.61–44.97** 31.42 14.87–47.97** 31.47 14.92–48.02** 22.52 4.77, 40.28*
Dairy products (g) −82.86 −118.61 to −47.12** −95.76 −132.7 to −58.83** −92.92 −129.85 to −55.99** −92.30 −128.66 to −55.95** −40.84 −78.46, −3.22*
Fiber 1.41 0.48–2.35* 1.51 0.59–2.43* 1.80 0.91–2.7** 1.83 0.99–2.67** 1.20 0.3, 2.09*
Vit. B6 (mg) 0.12 −0.02 to 0.26 0.15 0.01–0.29* 0.18 0.03–0.32* 0.18 0.04–0.32* 0.16 0.01, 0.31*
Folate (mcg) 18.49 2.9–34.09* 21.21 5.64–36.79* 25.51 10.2–40.82 25.87 11.06–40.68** 21.63 5.68, 37.59*
Vit. E (mg) 1.08 0.41–1.74* 1.04 0.36–1.72* 1.21 0.54–1.88** 1.23 0.59–1.87** 1.00 0.31, 1.68*
Vit. K (mcg) 23.45 12.66–34.24** 24.49 13.44–35.54** 26.49 15.48–37.49** 26.68 15.87–37.49** 23.48 11.83, 35.13**
Calcium (mg) −88.93 −140.93 to −36.93** −111.12 −163.83 to −58.42** −101.18 −153 to −49.36** −99.65 −148.81 to −50.49** −29.16 −79.97, −21.65*
Iron (mg) 1.33 0.6–2.07** 1.38 0.65–2.1** 1.61 0.9–2.31** 1.63 0.97–2.29** 1.10 0.39, 1.8*
Iodine (mcg) −5.33 −10.41 to 0.25 −6.46 −11.58 to −1.34* −5.09 −10.11 to −0.08* −4.98 −9.82 to −0.13* −3.26 −8.47, −0.19*
Zinc (mg) 0.48 −0.03 to 0.93 0.40 −0.04 to 0.85 0.53 0.1–0.96* 0.55 0.16–0.94* 0.49 0.07, 0.91*
Magnesium (mg) 13.07 −2.14 to 23.99 12.90 2.13–23.66* 16.33 5.98–26.68* 16.73 7.32–26.14* 10.46 0.4, 20.52*
Sodium (mg) −148.75 −275.95 to −21.55* −171.60 −297.47 to −45.73* −129.06 −248.79 to −9.34* −124.04 −230.82 to −17.26* −61.94 −176.38, −52.51*
Potassium (mg) 116.88 −7.68 to 226.08 106.58 3.03–216.18* 143.87 38.93–248.8* 147.42 49.68–245.16* 150.94 45.48, 256.41*

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


ASD: autism spectrum disorder; TD: typically developing; Vit.: vitamin; CIs: confidence intervals.
Beta (β) coefficients and 95% CIs are interpreted as the mean difference in intake between children with ASD and TD children.
Multivariable 1: adjusted for age (continuous) and sex.
Multivariable 2: also adjusted for weight (continuous) and height (continuous).
Multivariable 3: also adjusted for total energy intake (continuous).
Multivariable 4: also adjusted for diet type (gluten-free casein-free vs regular diet).
aIntake of TD children is used as the reference (zero values).

Level of significance *p < 0.05, **p < 0.001.


Autism
Marí-Bauset et al. 7

and sodium were significantly lower than those in TD chil-

1.41–147.43*
1.04–164.13*

1.09–46.26*
1.69–6.31**
dren. Exploring nutritional inadequacy in the two groups

0.09–0.82*

1.12–6.03*
0.25–0.79*

0.27–0.90*
of children compared to DRIs, we found the following: (1)

95% CI
High percentages failing to meet recommendations were

Multivariable 4
common in both groups with low intakes of carbohydrate
(91% in children with ASD vs 87.47% in the controls),

0.28
4.25
13.08
2.60
0.43
3.26
7.09
0.49
vitamin D (82.86% vs 84.24%, respectively), iodine

OR.
(62.86% vs 65.66%, respectively), and excessive fat
intakes (71% vs 69.49%, respectively), and the differences
were not significant. (2) The amount of fluoride consumed

0.84–108.36

3.11–9.99**
0.44–91.72
0.07–0.52*

0.23–0.77*

0.28–0.86*
0.79–4.06

0.44–10.8
was insufficient in all the children (in both groups). (3)

95% CI
The percentage of children consuming less than the recom-

Multivariable 3
mended amount of fiber and vitamin E intake was higher
in TD children than their peers with ASD. And finally, (4)
deficient riboflavin, vitamin A, and calcium intakes were

0.20
6.37
9.52
1.79
0.42
5.57
2.18
0.48
OR.
more common in children with ASD than their TD peers,
while a sodium intake lower than the DRIs was more fre-
quent in the ASD than the TD group. For all the other

0.48–91.31
0.91–84.42
0.09–0.59*

0.24–0.78*

0.33–0.91*
2.95–9.2**
0.78–3.97

0.4–8.48
nutrients, no statistically significant differences were

95% CI
found between the groups when comparing intakes to
DRIs, and the distribution of intakes was similar. The

Multivariable 2
results are listed in detail in Supplementary Online Table
2. When these comparisons were made with the DRIs for
the United States (IOM, 2010), we observed similar inad-

0.23
6.62
8.77
1.76
0.44
5.21
1.84
0.55
OR.
equate intake levels, except for carbohydrates (AMDR in
Spain 50–55 vs 45–65% in United States) and iodine
(EAR: 120 vs 65 mcg, respectively) (data not shown).
1.31–107.63*
0.58–101.84

3–9.25**
Table 3 summarizes the risk of inadequate intakes in
0.11–0.68*

0.29–0.91*

0.30–0.79*
0.89–4.44

0.48–9.73
children with ASD using the logistic regression analysis
95% CI

with TD children taken as the reference category. The ORs

DRIs: dietary reference intakes; TD: typically developing; Vit.: vitamin; CIs: confidence intervals.
in the adjusted model indicate a higher risk of failing to
Multivariable 1

meet recommendations for certain nutrients in children


with ASD: thiamin (4.25-fold), riboflavin (13.08-fold),
vitamin C (2.60-fold), iron (7.09-fold), and calcium (3.26-

Multivariable 4: also adjusted for diet type (gluten-free casein-free vs regular diet).
0.27
7.67
11.86
1.99
0.52
5.27
2.17
0.48
OR.

fold). On the other hand, the risk of inadequate intakes was


Multivariable 2: also adjusted for weight (continuous) and height (continuous).
higher in TD children for fiber, vitamin E, and sodium.
We repeated the main analyses using the EAR cut-point
2.16–176.88*

method and the results were very similar (data not shown).
2.29–6.15**
0.21–26.38
0.13–0.68*

0.31–0.91*

0.34–0.83*

Multivariable 3: also adjusted for total energy intake (continuous).


0.42–5.97
0.72–3.2
95% CI

Risk of failing to meet DRIs or nutritional targets in children.

Discussion
aIntake of TD children is taken as the reference (1 Ref.).
Multivariable 1: adjusted for age (continuous) and sex.

Our first hypothesis was that children with ASD would


Crude

have significantly lower anthropometric values, and this is


19.56
0.30
2.37

1.52
0.53
3.75
1.59
0.52
OR.

confirmed by our results (ORs adjusted for the BMI cate-


Table 3.  Logistic regression analysis.a

Level of significance *p < 0.05, **p < 0.001.

gories showed high risks of being underweight in all chil-


dren with ASD and boys with ASD). Furthermore, children
DRIs/targets

with ASD overall and boys (this does not occur with girls)
were shorter than TD children. There is no consensus
⩽2400
6–9 y.

among previous research comparing the anthropometric


800
0.8
1.2
25

55
8

values of children with ASD and TD children (e.g. Attlee


et al., 2015; Bauset et al., 2013; Curtin et al., 2010; Egan
Riboflavin (mg)

et al., 2013; Emond et al., 2010; Evans et al., 2012; Ho et al.,


Calcium (mg)
Thiamin (mg)

Sodium (mg)
Vit. C (mg)

1997; Zimmer et al., 2012). Likewise, Hill et al. (2015)


Vit. E (mg)

Iron (mg)
Fiber (g)

found that prevalence of overweight and obesity was sig-


nificantly higher among young children (2–5 years of age)

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


8 Autism

and adolescents (12–17 years of age) with ASD compared criteria, analysis of single individuals or small or age-
with the matched controls. However, for ages 6–11 years, heterogeneous samples, among others), the nutritional
no prevalence differences were found. In addition, Hyman assessment has indicated limited food variety in the ASD
et al. (2012) reported in their study that children aged population and has not confirmed significant differences
2–5 years with ASD had more overweight and obesity, and on macronutrients; yet it has shown an inadequate intake
children aged 6–11 years had more underweight than the of certain types of micronutrients in children with ASD
NHANES-matched cohort. These results are consistent with respect to DRIs or controls. These findings are con-
with studies previously carried out in Spain (Bauset et al., sistent with those obtained in our study. Indeed, nutritional
2013; Marí-Bauset et al., 2015a), and with our findings in requirements in these children in terms of energy and
the 6–9 years age group in this study. These differences macronutrients seem to be satisfied despite the rates of
observed in terms of the age group studied could be food selectivity and dietary restrictions. However, all the
explained due to the fact that children with ASD and aged previously cited studies, as well as our study, found that a
2–5 years spend more time carrying out therapeutic activi- wide range of nutritional inadequacies—both excessive
ties, where snacks can be used to reinforce participation, and insufficient intake of micronutrients—existed in chil-
which may favor unhealthy weight gain. Also, they may dren with ASD.
have fewer opportunities for or interest in active playing Previous studies assessing nutritional factors among
than their matched TD peers, a circumstance which can children with ASD have reported mixed results regarding
favor unhealthy weight gain. However, the exact reason nutritional deficiencies in this population (e.g. Alpert,
why the weight would be unhealthy among children with 2007; Keen, 2008; Kranz et al., 2006; Schreck et al., 2004).
ASD is not clear. Among schoolchildren of the age studied Notably, a body of previous research conducted among
herein, growth is highly sensitive to the balance between individuals with selective eating patterns like those
energy intake and total energy expenditure (Bölte et al., observed in ASD has shown inadequate intakes of low-
2002; Ho et al., 1997). However, in our sample, the energy energy foods, such as fruit and vegetables (Dovey et al.,
intake estimates in children with ASD and TD children 2008; Dubois et al., 2007; Emond et al., 2010; Evans et al.,
were similar. Apart from physical activity, abnormal 2012; Kranz et al., 2006), high-fiber foods, and lean pro-
behaviors can also result in higher levels of stress. Also, tein-rich foods (Dovey et al., 2008; Dubois et al., 2007;
other mechanisms that can cause development in these Evans et al., 2012), trends which contrast with the charac-
children with ASD to differ from that in TD children teristics of a Mediterranean diet.
include, among others, medical comorbidities (e.g. gastro- On the other hand, studies comparing the nutrient
intestinal diseases), or even neuroendocrine or genetic fac- intake of children with ASD with that of TD children have
tors (Newschaffer et al., 2007). Likewise, ASD and TD often minimized differences in nutrient intake between
groups could present different patterns of growth through- these groups. For instance, Shearer et al. (1982) used
out timelife (Hill et al., 2015). In any case, although BMI 3-day diet record, as we did, and observed lower calcium
is an important indicator for healthy weight, it is not neces- and riboflavin intake in children with ASD than TD con-
sarily a good indicator of nutrient status. trols, yet concluded that overall, the nutrient intake of
Second, we hypothesized that children with ASDs children with ASD was adequate and typical of well-fed
would have lower macro- and micronutrient intakes from American children. A classic study (Raiten and Massaro,
food than TD children, and we found this to be true only 1986) indicated that individuals with ASD presented sig-
for intakes of dairy products, cereals, calcium, iodine, and nificantly higher intakes of total energy, proteins, and car-
sodium. In contrast, the intakes of children with ASD were bohydrates, but not of fat; however, the authors concluded
significantly higher for legumes, vegetables, fiber, folate, that despite food selectivity, the overall adequacy of the
vitamins B6, E, and K, iron, zinc, magnesium, and potas- diets consumed was similar for both groups. Other
sium. These findings are in line with the traditional researchers (Hyman et al., 2012; Shearer et al., 1982)
Mediterranean diet in our geographical region (Valencia, have reported significantly lower total energy intakes.
Spain), and different from the so-called Western diet. The More recent studies (Emond et al., 2010; Johnson et al.,
review of the nutritional results of the cited articles quickly 2008; Lockner et al., 2008) have not observed major dif-
revealed that the existing body of literature is best described ferences in nutritional intake (total energy, fats, carbohy-
as highly limited in terms of research quality. Only three drates, proteins) compared to TD children, although
nutritional studies (Hediger et al., 2008; Herndon et al., children with ASD display more behavioral problems at
2009; Hyman et al., 2012) were of sufficient experimental meal times (Johnson et al., 2008).
rigor, due to the study design and size, so as to be classified Regarding specific micronutrients, children with ASD
as high-quality evidence. According to a recent systematic have been observed to have much higher intakes for niacin,
review (Marí-Bauset et al., 2015b), despite the fact that the thiamin, and riboflavin (Raiten and Massaro, 1986); sev-
studies in this area have suffered from methodological eral studies have reported low vitamin intakes, for vitamin
weaknesses (the lack of control groups, unclear selection A (Hyman et al., 2012; Raiten and Massaro, 1986; Shearer

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


Marí-Bauset et al. 9

et al., 1982), vitamin C (Emond et al., 2010; Hyman et al., lipids (Cornish, 1998; Souza et al., 2012) and proteins
2012; Raiten and Massaro, 1986; Shearer et al., 1982), vita- (Cornish, 1998; Levy et al., 2007; Sadowska and Cierebiej,
min D (Emond et al., 2010), and/or riboflavin (Hyman 2011; Souza et al., 2012) than the recommended. In addi-
et al., 2012; Shearer et al., 1982). Significantly higher tion, some authors found the intakes of calories, carbohy-
intakes for calcium, phosphorus, and iron (Raiten and drates, and fats to be adequate in most children with ASD
Massaro, 1986) have also been indicated. On the other (Levy et al., 2007), whereas others observed intakes of
hand, other research studies (Hyman et al., 2012; Shearer calories and proteins to be adequate in the vast majority of
et al., 1982) found significantly lower intakes of calcium, children with ASD, but fat intake to be lower than DRIs in
zinc, and phosphorus, but concluded that children with these children (Xia et al., 2010). On the other hand, several
ASD eat similar amounts of nutrients to controls. studies (Herndon et al., 2009; Hyman et al., 2012; Kranz
Our third hypothesis was that the overall HEI scores et al., 2006; Sadowska and Cierebiej, 2011) have found
and for food variety for children with ASD would be sig- low intakes of fiber compared to DRIs, consistent with our
nificantly lower than those of TD children. Yet despite results, and many previous studies (Cornish, 1998; Hediger
inadequate intakes of one or more macro- or micronutri- et al., 2008; Herndon et al., 2009; Hyman et al., 2012;
ents, in our sample, differences between groups were not Lindsay et al., 2006; Moore et al., 2004; Neumeyer et al.,
significant for the HEI. The HEI scores classified the diets 2013; Sadowska and Cierebiej, 2011; Zimmer et al., 2012)
of children with ASD and TD children as “needs to be have obtained similar results to ours regarding vitamin D,
improved.” This quantitative result is comparable to previ- intakes being below nutritional recommendations.
ous findings (Hyman et al., 2012; Johnson et al., 2008; Regarding vitamins, we found a smaller proportion of
Lockner et al., 2008; Raiten and Massaro, 1986), although children with ASD than their peers failed to meet vitamin
these earlier studies did not explicitly report HEI values. E intake recommendations. However, other studies
To our knowledge, only two other studies have investi- (Herndon et al., 2009; Suitor and Gleason, 2002) have
gated the HEI in ASD. Graf-Myles et al. (2013) found that reported children with ASD to have lower vitamin E
the children with ASD who did not follow a restricted diet intakes, failing to meet nutritional recommendations. On
obtained significantly lower HEI scores than those on a the other hand, some authors have observed that niacin,
restricted diet and TD children, while Johnson et al. (2014) vitamin B1, and vitamin B2 sufficed for most children with
suggested that as feeding and mealtime behaviors are ASD (Xia et al., 2010), and others that a high proportion of
worse in children with ASD, the quality of their diet would children with ASD presented lower than the recommended
also be worse. intakes of riboflavin (Shearer et al., 1982), niacin (Cornish,
The scores of component 10 of HEI (“variety in diet”) 1998), or pantothenic acid (Lindsay et al., 2006). Low
were not significantly different in the two groups. This intakes of vitamin B12 (Zimmer et al., 2012), vitamin B6
finding may be explained by the fact that parents and car- (Cornish, 1998; Xia et al., 2010), and folate (Cornish,
egivers whose offspring have been diagnosed with ASD 1998) have also been reported. Furthermore, intakes have
pay particular attention to diet and nutrition of their chil- been reported to be lower than DRIs for vitamin A
dren and this may compensate to some degree for difficult (Sadowska and Cierebiej, 2011; Xia et al., 2010), vitamin
eating behaviors. In any case, our data showed limited C (Cornish, 1998; Xia et al., 2010), and vitamin K (Lindsay
food variety in children with ASD. et al., 2006) in some individuals, although growth rates do
Finally, our fourth hypothesis proposed that children not seem to be affected (Xia et al., 2010).
with ASD would meet Spanish daily recommended intakes With regard to minerals, several studies have indicated
less often than TD children. Significant differences were similar results for children with ASD to those reported
only found for certain nutrients: (1) a high percentage of herein, with calcium intakes below DRIs (Bandini et al.,
children in both groups exceeded the DRIs for sodium, but 2010; Cornish, 1998; Hediger et al., 2008; Herndon et al.,
a sodium intake in line with recommendations (i.e. lower 2009; Ho et al., 1997; Johnson et al., 2008; Neumeyer
than the DRIs) was more common in the children with ASD; et al., 2013; Suitor and Gleason, 2002). Numerous studies
and (2) despite intakes being adequate in most children in (Bilgiç et al., 2010; Cornish, 1998; Dosman et al., 2007;
both groups, the percentage of children with ASD who met Herndon et al., 2009; Ho et al., 1997; Johnson et al., 2008;
the guidelines was higher for vitamin E, but lower for biotin, Latif et al., 2002; Reynolds et al., 2012; Sadowska and
riboflavin, vitamin A, and calcium than in TD children. Cierebiej, 2011; Shearer et al., 1982; Xia et al., 2010) have
Furthermore, the majority of children in both groups failed reported that children with ASD do not meet DRIs for iron,
to meet the recommendations for carbohydrates, with lower while other data (Sadowska and Cierebiej, 2011; Shearer
intakes than DRIs, and the same could be said for lipids, et al., 1982; Xia et al., 2010), including those of this study,
with excessive intakes, but differences were not significant. are inconsistent with these earlier findings. Several authors
Some previous research has observed low protein observed mixed results for magnesium: a high intake
intakes (Zimmer et al., 2012), while other studies have (Sadowska and Cierebiej, 2011; Zimmer et al., 2012), AI
reported imbalanced macronutrients with higher intakes of in most children with ASD (Xia et al., 2010), or low daily

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


10 Autism

intake (Levy et al., 2007), while intakes of zinc were lower from the outset and were extensively trained and supported
than DRIs (Xia et al., 2010; Zimmer et al., 2012). Others in the completion of the food records. All this can compen-
(Sadowska and Cierebiej, 2011) have published results sate for the limitations that the selection of the sample may
regarding intakes of sodium and phosphorus, but the val- impose or for external validity generalization. We should
ues did not differ significantly from those of the reference also point out that data for the cases and controls that were
population. compared had been adjusted for age, sex, weight, height,
The general picture remains unclear. Some authors and total energy intake as potential confounders, as well as
have concluded that the mean intakes for macronutrients all children having a similar place of residence and socio-
and micronutrients tend to exceed DRIs (Lindsay et al., economic status, and being followed up over the same
2006) while others have indicated that the majority of chil- time period. We believe that these factors may help to
dren with ASD do not generally meet recommended nutri- compensate for limitations in generalizability and external
ent intakes (Ho et al., 1997). validity associated with participant selection. Furthermore,
It could be argued that DRIs should differ for children our study was also substantially larger than any previous
with ASD. However, despite there being biological differ- research work of this type conducted in Spain. Finally, it
ences between the groups, there is still no basis to date to could be that DRIs should be different for children with
assert that they have different metabolic requirements. ASD, although for the moment, no alternative recommen-
Furthermore, the mixed results available should be inter- dations have been proposed.
preted cautiously. Comparisons can be hindered by the fol-
lowing: a lack of standard criteria for nutritional tables
across countries; variations in age groups for which rec- Conclusion
ommendations are defined; authors using distinct cut-off
Recommendations and implications for practice
values to define “inadequacy”; and recommended levels
not specifying the availability and consumption of forti- Although many children with ASD in our sample did not
fied foods. All these aspects may lead to studies producing eat the recommended intakes of certain nutrients, this is
results that are not directly comparable, and this likely generally the case for the Spanish child population (Varela-
underlies the seemingly inconsistent results. Moreiras et al., 2010). So far, the data available remain
insufficient to reach a clear consensus as to whether nutri-
tional intake is generally impaired in children with ASD
Study limitations and regarding its potential consequences for their develop-
Our results show a probability of inadequacy, but do not ment. However, given some evidence that certain children
determine whether the diet of the ASD group is adequate with ASD do not eat a balanced diet, anthropometric moni-
or not. Real nutritional deficiency should be confirmed by toring is important and it is necessary to investigate the
specific biomarkers of nutrient intake. In our sample of range and severity of risk of deficiencies or excesses with
children with ASD, there were considerably more boys longitudinal studies to better manage their diet in order to
than girls, reflecting the gender imbalance in the preva- minimize the possible risk of them developing comorbid
lence of the disorder. Although this imbalance was not pre- chronic conditions.
sent in the TD sample, the Spanish dietary recommendations More research is needed to corroborate our findings.
for the age group studied (6–9 years) are the same for boys Given stark differences between our findings and reports
and girls, and this homogeneity in the age group, as well as from other parts of the world, future research should con-
multivariable-adjusted models, reduces the impact of this sider the role of environment and cultural dietary patterns
potential source of bias. in food selectivity and food intake in children with ASD
In addition, results obtained using two different meth- and attempt to clarify the relationships between ASD-
ods (the probabilistic approach and the EAR cut-point related symptoms, anthropometric values, eating patterns,
approach) to estimate nutrient intake adequacy were very and health status. Other areas for future work include
similar. The use of the latter approach as a reference for characterizing the various behavioral ASD phenotypes by
estimating nutritional adequacy compared with the DRIs considering more detailed diagnoses and standardizing
value avoids overestimation of the prevalence of dietary protocols to assess nutritional problems. HEI results can
inadequacy. Although the sample sizes were relatively be used to guide clinical and research activities in this
small in comparison with several studies previously car- area although more data are needed to validate food vari-
ried out by researchers in other countries and may not be ety as an indicator of the risk of deficient or excessive
fully representative of the population of the country, we nutrient intakes. Our anthropometric and nutritional
believe that our study offers strong internal validity given results in children with ASD suggest that these variables
the low attrition rate. We are confident about the good may be useful for stratifying this study population for
quality of the self-reported information used for the nutri- clinical and genetic studies, and for developing new ave-
tional assessment. Parents were very interested in the study nues of research in the epigenetics field, particularly in

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


Marí-Bauset et al. 11

nutrigenomics and nutrigenetics. Finally, the main impli- Curtin C, Anderson SE, Must A, et al. (2010) The prevalence
cations of this study for practice are that clinical recom- of obesity in children with autism: a secondary data analy-
mendations should be made on a case-by-case basis after sis using nationally representative data from the National
considering together dietary assessment, anthropometric, Survey of Children’s Health. BMC Pediatrics 23(10): 11.
Dosman CF, Brian JA, Drmic IE, et al. (2007) Children with
and laboratory results.
autism: effect of iron supplementation on sleep and ferritin.
Pediatric Neurology 36(3): 152–158.
Acknowledgements Dovey TM, Staples PA, Gibson EL, et al. (2008) Food neophobia
The authors wish to thank the children who participated and their and “picky/fussy” eating in children: a review. Appetite 50:
parents for collaborating with the study. The authors are also 181–193.
grateful for support from colleagues at the Dr Peset University Dubois L, Farmer AP, Girard M, et al. (2007) Preschool chil-
Hospital (Valencia, Spain). No external funding was received for dren’s eating behaviors are related to dietary adequacy and
this study. body weight. European Journal of Clinical Nutrition 61:
846–855.
Declaration of conflicting interests Egan AM, Dreyer ML, Odar CC, et al. (2013) Obesity in young
children with autism spectrum disorders: prevalence and
The author(s) declared no potential conflicts of interest with respect associated factors. Childhood Obesity 9(2): 125–131.
to the research, authorship, and/or publication of this article. Emond A, Emmett P, Steer C, et al. (2010) Feeding symptoms,
dietary patterns, and growth in young children with autism
Funding spectrum disorders. Pediatrics 126(2): 337–342.
The author(s) received no financial support for the research, Evans EW, Must A, Anderson SE, et al. (2012) Dietary pat-
authorship, and/or publication of this article. terns and body mass index in children with autism and
typically developing children. Research in Autism Spectrum
References Disorders 6: 399–405.
Federación Española de Sociedades de Nutrición, Alimentación
Alpert M (2007) The autism diet. Scientific American 296:
y Dietética (FESNAD) (2010) Ingestas Dietéticas de
19–20.
Referencia [Dietary Reference Intakes, DRIs]. Pamplona:
American Psychiatric Association (APA) (2014) Diagnostic and
Ed. Eunsa.
Statistical Manual of Mental Disorders. 5th ed. Washington,
Graf-Myles J, Farmer C, Thurm A, et al. (2013) Dietary ade-
DC: APA.
quacy of children with autism compared with controls and
Attlee A, Kassem H, Hashim M, et al. (2015) Physical status and
the impact of restricted diet. Journal of Developmental and
feeding behavior of children with autism. Indian Journal of
Behavioral Pediatrics 34(7): 49–59.
Pediatrics 82(8): 682–687.
Hediger ML, England LJ, Molloy CA, et al. (2008) Reduced bone
Bandini LG, Anderson SE, Curtin C, et al. (2010) Food selectiv-
cortical thickness in boys with autism or autism spectrum
ity in children with autism spectrum disorders and typically
disorder. Journal of Autism and Developmental Disorders
developing children. Journal of Pediatrics 157(2): 259–264.
38: 848–856.
Barrett-Connor E (1991) Nutrition epidemiology: how do we
Herndon AC, Di Guiseppi C, Johnson SL, et al. (2009) Does nutri-
know what they ate? American Journal of Clinical Nutrition
tional intake differ between children with autism spectrum
54: 182S–187S.
disorders and children with typical development? Journal of
Bauset SM, Zazpe I, Sanchis AM, et al. (2013) Are there anthro-
Autism and Developmental Disorders 39: 212–222.
pometric differences between autistic and healthy children? Hill AP, Zuckerman KE and Fombonne E (2015) Obesity and
Journal of Child Neurology 28(10): 1226–1232. autism. Pediatrics 136(6): 1051–1061.
Bilgiç A, Gürkan K, Türkoğlu S, et al. (2010) Iron deficiency Ho HH, Eaves LC and Peabody D (1997) Nutrient intake and
in preschool children with autistic spectrum disorders. obesity in children with autism. Focus on Autism and Other
Research in Autism Spectrum Disorders 4(4): 639–644. Developmental Disabilities 12: 187–193.
Bölte S, Özkara N and Poutska F (2002) Autism spectrum dis- Hubbard L, Anderson SE, Curtin C, et al. (2014) A comparison
orders and low body weight: is there really a systematic of food refusal related to characteristics of food in children
association? International Journal of Eating Disorders 31: with autism spectrum disorder and typically developing
349–351. children. Journal of the Academy of Nutrition and Dietetics
Carriquiry AL (1999) Assessing the prevalence of nutrient inad- 114(12): 1981–1987.
equacy. Public Health Nutrition 2: 23–33. Hyman SL, Steward PA, Schmidt B, et al. (2012) Nutrient intake
Centers for Disease Control and Prevention (CDC) (2000) from food which autism. Pediatrics 103(Suppl. 2): 145–153.
Defining childhood overweight and obesity. Available at: Institute of Medicine (IOM) (2001) Dietary Reference Intakes:
http://www.cdc.gov/obesity/childhood/defining.html Applications in Dietary Assessment. Washington, DC:
Centers for Disease Control and Prevention (CDC) (2014) National Academy Press.
Prevalence of autism spectrum disorders. Surveillance sum- Institute of Medicine (IOM) (2003) Dietary Reference Intakes:
maries MMWR. Available at: http://www.cdc.gov/media/ Applications in Dietary Planning. Washington, DC:
releases/2012/a0329_autism_disorder.html National Academy Press.
Cornish E (1998) A balanced approach towards healthy eating Institute of Medicine (IOM) (2010) Dietary Reference Intakes
in autism. Journal of Human Nutrition and Dietetics 11: for Calcium and Vitamin D. Washington, DC: National
501–509. Academy Press.

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


12 Autism

Johnson CR, Handen BL, Mayer-Costa M, et al. (2008) Eating Moore C, Murphy MM, Keast DR, et al. (2004) Vitamin D
habits and dietary status in young children with autism. intake in the United States. Journal of the American Dietetic
Journal of Developmental and Physical Disabilities 20: Association 104: 980–983.
437–448. Moreiras O, Carbajal A, Cabrera L, et al. (2013) Tablas de com-
Johnson CR, Turner K, Stewart PA, et al. (2014) Relationships posición de alimentos [Food Composition Tables]. 16th ed.
between feeding problems, behavioral characteristics and Madrid: Ed. Pirámide.
nutritional quality in children with ASD. Journal of Autism Murphy SP and Barr SI (2011) Practice paper of the American
and Developmental Disorders 44(9): 2175–2184. Dietetic Association: using the dietary reference intakes.
Keen DV (2008) Childhood autism, feeding problems and fail- Journal of the American Dietetic Association 111(5):
ure to thrive in early infancy. European Child & Adolescent 762–770.
Psychiatry 17(4): 209–216. National Research Council (NCR) (1985) Nutrient Adequacy:
Kennedy ET, Ohls J, Carlso S, et al. (1995) The Healthy Eating Assessment using Food Consumption Surveys. Washington,
Index: design and applications. Journal of the American DC: Subcommittee on Criteria for Dietary Evaluation.
Dietetic Association 95: 1103–1108. Neumeyer AM, Gates A, Ferrone C, et al. (2013) Bone den-
Kranz S, Smiciklas-Wright H and Francis LA (2006) Diet qual- sity in peripubertal boys with autism spectrum disorders.
ity, added sugar, and dietary fiber intakes in American pre- Journal of Autism and Developmental Disorders 43(7):
schoolers. Pediatric Dentistry 61: 492–497. 1623–1629.
Latif A, Heinz P and Cook R (2002) Iron deficiency in autism Newschaffer CJ, Croen LA, Daniels J, et al. (2007) The epide-
and Asperger syndrome. Autism 6(1): 103–114. miology of autism spectrum disorders. Annual Review of
Le Couteur A, Haden G, Hammal D, et al. (2008) Diagnosing Public Health 28: 235–258.
autism spectrum disorders in pre-school children using two Onis M, Onyango AW, Borghi E, et al. (2007) Development of
standardised assessment instruments: the ADI-R and the a WHO growth reference for school-aged children and ado-
ADOS. Journal of Autism and Developmental Disorders lescents. Bulletin of the World Health Organization 85(9):
38(2): 362–372. 660–667.
Levy SE, Souders MC, Ittenbach RF, et al. (2007) Relationship Raiten DJ and Massaro T (1986) Perspectives on the nutri-
of dietary intake to gastrointestinal symptoms in children tional ecology of autistic children. Journal of Autism and
with autistic spectrum disorders. Biological Psychiatry Developmental Disorders 16: 133–143.
61(4): 492–497. Reynolds A, Krebs NF, Stewart PA, et al. (2012) Iron sta-
Lindsay RL, Eugene Arnold L, Aman MG, et al. (2006) Dietary tus in children with autism spectrum disorder. Pediatrics
status and impact of risperidone on nutritional balance in 130(Suppl. 2): S154–S159.
children with autism: a pilot study. Journal of Intellectual & Sadowska J and Cierebiej M (2011) Evaluation of the nutri-
Developmental Disability 31(4): 204–209. tion manner and nutritional status of children with autism.
Lockner DW, Crowe TK and Skipper BJ (2008) Dietary intake Preliminary investigations. Pediatria Współczesna.
and parents’ perception of mealtime behaviors in preschool- Gastroenterologia, Hepatologia i Żywienie Dziecka 13(3):
age children with autism spectrum disorder and in typi- 155–160.
cally developing children. Journal of the American Dietetic Schmitt L, Heiss CJ and Campbell EE (2008) A comparison of
Association 108(8): 1360–1363. nutrient intake and eating behaviors of boys with and with-
Lord C, Risi S, Lambrecht L, et al. (2000) The autism diagnostic out autism. Topics in Clinical Nutrition 23: 23–31.
observation schedule-generic: a standard measure of social Schreck KA, Williams K and Smith AF (2004) A comparison
and communication deficits associated with the spectrum of eating behaviors between children with and without
of autism. Journal of Autism and Developmental Disorders autism. Journal of Autism and Developmental Disorders
30(3): 205–223. 34: 433–438.
Lord C, Rutter M and Le Couteur A (1994) Autism Diagnostic Shearer TR, Larson K, Neuschwander J, et al. (1982) Minerals in
Interview-Revised: a revised version of a diagnostic inter- the hair and nutrient intake of autistic children. Journal of
view for caregivers of individuals with possible perva- Autism and Developmental Disorders 12: 25–34.
sive developmental disorders. Journal of Autism and Souza NC, Mendonca JN, Portari GV, et al. (2012) Intestinal
Developmental Disorders 24: 659–685. permeability and nutritional status in developmental disor-
Marí-Bauset S, Llopis-González A, Zazpe I, et al. (2015a) ders. Alternative Therapies in Health and Medicine 18(2):
Anthropometric measures of Spanish children with autism 19–24.
spectrum disorder. Research in Autism Spectrum Disorders Suitor CW and Gleason PM (2002) Using dietary reference
9: 26–33. intake based methods to estimate the prevalence of inad-
Marí-Bauset S, Zazpe I, Mari-Sanchis A, et al. (2015b) equate nutrient intake among school-aged children. Journal
Anthropometric measurements and nutritional assessment of the American Dietetic Association 102: 530–536.
in autism spectrum disorders: a systematic review. Research Twachtman-Reilly J, Amaral SC and Zebrowski PP (2008)
in Autism Spectrum Disorders 9: 130–143. Addressing feeding disorders in children on the autism
Matson JL and Kozlowski AM (2011) The increasing prevalence spectrum in school-based settings: physiological and behav-
of autism spectrum disorders. Research in Autism Spectrum ioral issues. Language, Speech, and Hearing Services in
Disorders 5(1): 418–425. Schools 39(2): 261–272.

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016


Marí-Bauset et al. 13

Vandenbroucke JP, Von Elm E, Altman DG, et al. (2007) World Health Organization (1996) Physical status: the use
Strengthening the Reporting of Observational Studies in and interpretation of anthropometry. Report of a WHO
Epidemiology (STROBE): explanation and elaboration. expert committee. American Journal of Human Biology
Annals of Internal Medicine 147: W163–W194. 8: 786–787.
Varela-Moreiras G, Avila J, Cuadrado C, et al. (2010) Evaluation Xia W, Zhou Y, Sun C, et al. (2010) A preliminary study on
of food consumption and dietary patterns in Spain by the nutritional status and intake in Chinese children with autism.
Food Consumption Survey: updated information. European European Journal of Pediatrics 169(10): 1201–1206.
Journal of Clinical Nutrition 64: S37–S43. Zimmer MH, Hart LC, Manning-Courtney P, et al. (2012) Food
Wacholder S, Silverman DT, McLaughlin JK, et al. (1992) Selection variety as a predictor of nutritional status among chil-
of controls in case-control studies. III. Design options. dren with autism. Journal of Autism and Developmental
American Journal of Epidemiology 135(9): 1042–1049. Disorders 42: 549–556.

Downloaded from aut.sagepub.com at Universidad de Valencia on May 2, 2016

View publication stats

You might also like