PRACTICE APPLICATIONS
Topics of Professional Interest
Nutrition Management of Gastrointestinal Symptoms in Children with Autism Spectrum Disorder: Guideline from an Expert Panel
A
UTISM SPECTRUM DISORDER (ASD) is characterized by a core deficit in social communication with concomitant repetitive/perseverative behaviors and restriction in interests,1 and individuals
This article was written by Rashelle C. Berry, MPH, MS, RD, CSP, lead nutritionist, Pediatric Feeding Disorders Program, Marcus Autism Center, Atlanta, GA; Patricia Novak, MPH, RD, EMPOWER project coordinator, Children’s Hospital of Los Angeles, Los Angeles, CA; Nicole Withrow, PhD, RD, assistant professor and dietetic internship coordinator, University of Northern Colorado, Greeley; Brianne Schmidt, RD, clinical nutrition specialist, Division of Neurodevelopmental and Behavioral Pediatrics, Golisano Children’s Hospital at Strong, University of Rochester Medical Center, Rochester, NY; Sheah Rarback, MS, RD, director of nutrition, Mailman Center for Child Development, Miller School of Medicine, University of Miami, Miami, FL; Sharon Feucht, MA, RD, nutritionist, Center on Human Development and Disability, University of Washington, Seattle; Kristen K. Criado, PhD, psychologist, Pediatric Feeding Disorders Program, Marcus Autism Center, Atlanta, GA, and assistant professor, Department of Pediatrics, Emory University School of Medicine, Atlanta, GA; and William G. Sharp, PhD, director, Pediatric Feeding Disorders Program, Marcus Autism Center, Atlanta, GA, and assistant professor, Department of Pediatrics, Emory University School of Medicine, Atlanta, GA. http://dx.doi.org/10.1016/j.jand.2015.05.016 Available online 9 July 2015
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ª 2015 by the Academy of Nutrition and Dietetics.
with ASD experience varying degrees of impairment.2 The estimated prevalence of ASD in pediatric populations has climbed dramatically during the past decade, with approximately 1 in every 68 children currently meeting diagnostic criteria in the United States.3 High prevalence occurs against a backdrop of increased health care costs 4 and social burden. 5 Medical comorbidities are significantly overrepresented compared with other pediatric populations, and children with ASD often present with medical conditions affecting multiple organ systems.6 Dysfunction of the gastrointestinal (GI) tract is among the most frequently cited comorbidities. A recent meta-analysis indicated that children with ASD were four times more likely to experience general GI complaints, are more than three times more prone to experience constipation and diarrhea, and complain twice as frequently about abdominal pain compared with peers.7 Lack of data prevented analysis of other GI symptoms (eg, gastroesophageal reflux, celiac disease, lactose intolerance) typically associated with organic etiologies; however, a 2010 consensus report concluded that, at a minimum, rates of other GI pathophysiology in ASD should be viewed as occurring at similar levels to those observed in the general population.8 This includes consideration of the potential contribution of factors such as GI motility, altered gut microbiome, immune abnormalities, and food allergy when GI symptoms are detected.7 In addition to calling for greater research scrutiny in this area, the expert panel of pediatric gastroenterologists also emphasized the need to develop evidence-based standards for the evaluation and treatment of GI symptoms in ASD. Nutrition management is often critical in the treatment of GI symptoms in other
pediatric populations9,10; however, no guidelines are available for adapting existing practices for use among children with ASD. Current standards of care might be neither practical nor feasible, given the combination of behavioral, developmental, medical, and social deficits associated with the condition. For example, children with ASD often present with limited communication and, as a result, their symptom presentation may be unusual compared with that of their peers.7,8,11,12 In many cases, GI symptoms might only manifest as a change in behavior, such as the emergence or exacerbation of problem behaviors like aggression, self-injury, sleep disturbance, or irritability.7,13 As a result, recognition and treatment of GI disorders in children with ASD remain ill-defined and poorly understood,11 particularly when it comes to the challenge of untangling the relative contribution of diet when underlying GI pathology is suspected. The diagnostic and intervention process is further complicated by the high prevalence of feeding problems in ASD. Evidence suggests children with ASD have a fivefold increase in problematic eating and feeding behaviors compared with typically developing peers.14 Food selectivity, defined as a limited food repertoire (eg, only eating a few foods and/or rejection of one or more food groups) or high intake of a single food,15 is the most frequently documented feeding issue associated with ASD. Dietary intake in ASD often involves strong preferences for highly processed foods, snacks, and sweets,16 and a lower intake of fruits and vegetables.15,17,18 High intake of simple carbohydrates and fat coinciding with low intake of fiber complicates the diagnostic process, making it difficult to determine whether food selectivity directly contributes to the onset of GI symptoms or simply exacerbates a preexisting GI condition.19 For example, a child may be constipated
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PRACTICE APPLICATIONS due to poor motility as the result of impaired gastric emptying and/or low muscle tone, with more severe symptom presentation in cases involving poor dietary diversity. Alternatively, constipation could be the direct result of a diet lacking in fruits, vegetables, and whole grains and, therefore, low in fiber and fluid.7 In both cases, nutrition intervention can improve overall symptom presentation, however, a more detailed medical workup (eg, allergy, GI) would also be necessary if possible organic etiology is suspected. When developing a nutrition intervention, food selectivity may place limits on introducing and/or removing foods from the diet. Specifically, restricted patterns of intake in ASD are often maintained by refusal behaviors (eg, tantrums, aggression) in response to the presentation of nonpreferred foods or novel feeding demands.20 As a result, caregivers may be unable to adhere to clinical recommendations due to the intensity of their child’s behavioral response to the new therapeutic diet. In addition, it may be difficult to anticipate how a child will respond to efforts to
remove and/or replace preferred foods, including the possibility of further selfimposed dietary restriction after intervention beyond targeted foods. With this in mind, the clinician must determine how to best manage the child’s nutrition while considering his or her overall medical status. Nutrition management must also account for the proliferation of caregivermediated dietary restrictions in the ASD community. Children with ASD are significantly more likely to be placed on caregiver-initiated complementary/ alternative diet therapies as compared to peers.21 Common dietary interventions applied in this population are listed in Figure 1. In general, these diets restrict or completely eliminate certain food groups. For example, the glutenfree, casein-free diet, arguably the most well-known type of dietary manipulation in ASD, eliminates gluten (found in wheat, barley, and rye) and casein (found in cow’s milk dairy products).28 Without the guidance of a registered dietitian nutritionist (RDN), this level of restriction may increase risk of macronutrient and micronutrient
Diet
Foods restricted
Elimination diets/elemental diet22,23
Elimination diet (6 foods): milk, egg, wheat, soy, peanuts/tree nuts, fish/shellfish Elemental: all foods except an amino acid based formula
Fermentable oligo-dimonosaccharides and polyols24,25
Foods containing fructose (eg, fruit, highfructose corn syrup), lactose (eg, cow’s milk dairy), fructans (eg, wheat, onion, garlic), galactans (eg, legumes), and polyols (eg, sorbitol, cherries, avocados)
Food coloring/food additives avoidance26,27
Foods that contain food color additives (food dye)
Gluten-free, casein-free28-30
Foods containing gluten (eg, bread, pasta) and casein (eg, cow’s milk, yogurt)
Ketogenic diet or modified Atkins diet31,32
Carbohydrate-rich foods, including sugar
Specific carbohydrate diet29,33,34
Cereal grains (eg, wheat, oats, rice), processed meats (eg, lunch meats, hot dogs), canned vegetables, canned fruits, most fruit juices, soy beans, chick peas, bean sprouts, mung beans, fava beans, yogurt, milk, processed cheese, tubers (eg, potatoes, yams), curry, onion powder, garlic powder
Figure 1. Possible caregiver-initiated restrictions in autism spectrum disorder (in alphabetical order). 1920
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deficiencies in a population already prone for underlying dietary insufficiencies related to food selectivity,14 and the potential for further nutritional deficits and associated health concerns presents unique challenges for designing interventions. When a caregiver-initiated or other restrictive diet is in place, the RDN must work with the family to determine which foods (if any) can be added, removed, and/or reintroduced to alleviate GI concerns, while concurrently attempting to best meet nutrition needs. Many caregivers, however, may be resistant to incorporate recommendations that involve the reintroduction of currently restricted foods. If specific foods previously removed place the child at nutrition risk and cannot be reintroduced, appropriate substitutions need to be identified; although this may be difficult in cases involving extremely limited food repertoires and resistance to the introduction of new foods. The unique dietary, medical, and behavioral challenges observed in children with ASD combined with an overall lack of data on management of GI disorders in this population11 presents a pressing need to develop a guideline for nutrition intervention. Consistent with previous work to develop standards of care in ASD,11 expert opinion was viewed as a critical first step in this process, given the absence of relevant data. Therefore, a committee of RDNs specializing in the nutrition care of children with ASD was formed and a focus group was conducted to develop a clinical practice guideline. This article describes the process of convening the expert committee, outlines considerations for adapting existing nutrition practice, and presents a guideline for the nutrition management of GI symptoms in children with ASD.
FOCUS GROUP MEETING AND ALGORITHM DEVELOPMENT The first step toward creating a standard of care for RDNs to use when working with children with GI symptoms and ASD involved identifying experts in the field. Our search process consisted of contacting major autism treatment centers in the United States, listserv solicitation through the Autism Speaks’ Autism Treatment Network, and comprehensive review December 2015 Volume 115 Number 12
December 2015 Volume 115 Number 12
Suspected or confirmed GI problem and nutrition intervention clinically indicated, begin with nutrition assessment 1
Food selectivity a concern? 2
Caregiver initiated diet in place?
No
Gaps in caregiver knowledge?
No 3
No 4
Provider works to identify barriers to diet recs 4a
Yes
Yes
Yes Caregiver willing to adjust diet? 3a
RD identifies barriers to meeting appropriate volume of target foods
Provider works to identify foods within diet restrictions
No
3b
2a Yes Foods within existing repertoire? 2b
Barriers within scope of practice? 4b
Yes No Foods within existing repertoire? 3c
Yes Yes
5
No RD assess possible nutrition concerns (Box 9) and refers to appropriate medical intervention (Box 11) 3d
6
Diet nutritionally adequate?
4c
7
No
Referral to behavioral intervention specialist to address food selectivity/meal structure
RD refers to appropriate behavioral (Box 8) medical intervention (Box 11)
No
Yes
Consider supplementation (e.g., nutritionally complete drink)
8
9
Arrange follow-up to meet treatment goals 10
Adjust nutritional recommendations (if applicable) AND GI consult to identify red flags or medical alternatives
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11
No
Treatment reduces/eliminates symptoms? 10
Yes
Figure 2. Algorithm for nutrition management of gastrointestinal concerns in children with autism spectrum disorder.
Continue Therapy/Arrange long term follow-up 10
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RD counsels family on treatment approach: Readjust diet to involve rec volume of target foods
RD counsels family on treatment approach: Increase or decrease volume of select target foods
No
PRACTICE APPLICATIONS Box
Details
1
Full nutrition assessment after referral to address GI symptoms. In addition to a standard assessment (ie, food intake analysis, anthropometrics, labs), assessment should include detailed discussion and identification of potential foods that may be causing an adverse reaction in the child. This includes assessment of known food allergies, as well as evaluation of risk for additional food allergies, food intolerances (ie, lactose intolerance), and other potential adverse reactions to foods (ie, celiac disease).
2
Food selectivity is present if child has a limited food repertoire, high-frequency consumption of a few foods, and significant problem behaviors, including, but not limited to crying, leaving the meal, gagging, aggressing, and/or vomiting when nonpreferred foods are presented.
2a
Full assessment of dietary repertoire, including detailed examination of foods accepted by major food group (fruits, vegetables, meats/beans, dairy, grains). Include questions to determine the volume and frequency of intake. Assess responses to changes in meal routines, such as environment, temperature, method of presentation, and food type/texture presented.
2b
Current list of accepted foods evaluated to determine if consistent with proposed medical nutrition therapy guidelines.
3
Caregiver-initiated diet includes alternative diet therapies (eg, gluten-free, casein-free) and medically prescribed diets (eg, hypoallergenic).
3a
Discuss with caregiver acceptability and ability to veer from current dietary plan. This precludes medically indicated diets based on underlying organic pathology (eg, celiac disease, food allergy).
3b
Full assessment of acceptable foods within dietary restrictions, including detailed examination of foods accepted by major food group (fruits, vegetables, meats/beans, dairy, grains). Include questions to determine the volume and frequency of intake. Assess behavioral response to changes in meal routines, such environment, temperature, method of presentation, and food presented. Consider how dietary changes will impact development and social inclusion.
3c
Clinician works to find foods that are congruent with dietary repertoire and will meet medical nutrition therapy guidelines for GI symptoms.
3d
If nutrition intervention is not possible based on restrictions, a two-pronged approach is warranted: Assess for any nutritional insufficiencies and whether supplementation is indicated. Determine the most effective method to assure formula acceptance. Refer to medical provider to consider alternative treatment approaches.
4
No level of dietary restriction (food selectivity or caregiver-initiated) identified. Caregiver and child will be able to follow recommendations as outlined by registered dietitian nutritionist.
4a
Typical nutrition assessment of factors influencing nutritional status, such as meal planning, food security, and ability to prepare food. Additional barriers to consider can include the child’s general behavior, sensory processing, cognitive development, communication skills, oral health and motor planning, family socioeconomic circumstances, and community support and resources.
4b
Assess whether barriers fall within the scope of dietetics. Concerns falling outside of scope include need for parent training to address disruptive behavior, motor dysfunction, sensory concerns, and/or possible neglect.
4c
If nutrition intervention is not possible based on restrictions, a two-pronged approach is warranted: Refer to feeding team. Refer to medical provider to consider alternative treatment approaches (including nonoral feeds, if indicated).
5
Treatment approach involves using only preferred foods to create a prescription diet to address GI concerns. Volumes of foods typically presented might be adjusted to meet treatment needs. (continued on next page)
Figure 3. Accompanying text for algorithm for nutrition management of gastrointestinal concerns in children with autism spectrum disorder.
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PRACTICE APPLICATIONS Box
Details
6
Treatment approach involves developing meal plan to address GI concerns in line with medical nutrition therapy guidelines. While consideration should be given to possible behavioral response to changes related to autism spectrum disorders, greater flexibility in treatment planning is possible due to lack of caregiver restriction.
7
Re-evaluation of diet, growth, and weight change occurs after prescription has been provided. This might include dietary analysis using dietary recall or food intake records. Labs can be ordered if there is continued concern of dietary insufficiencies. Goal to assure overall nutrition planning with optimal energy and nutrient intake.
8
Referral to a feeding therapist is indicated if prescribed diet is not able to be followed due to mealtime difficulties with the introduction of nonpreferred foods or if general behavior-management during meals is needed due to changes in meal routines.
9
Nutrition supplementation (vitamins, minerals, and/or nutritionally complete drink) is indicated if current diet does not meet nutrition needs or if the level of dietary restriction needed (ie, allergies, GI concerns) does not allow for optimal intake from foods alone.
10
Follow up includes reassessment of growth, nutrition, and alleviation of GI symptoms
11
Provider works to adjust nutrition recommendations to alleviate GI symptoms. If recommended diet is ineffective, provider should refer back to physician to determine medical alternatives.
Figure 3. (continued) Accompanying text for algorithm for nutrition management of gastrointestinal concerns in children with autism spectrum disorder.
of the literature. The selection criteria required committee members to be certified as an RDN; spend at least 25% of professional time engaged in clinical nutrition activities (assessment and/or treatment) with children with ASD; have practiced in the field of nutrition for at least 3 years; and possess experience (past or current) working in a multidisciplinary environment (eg, medical or research center, feeding clinic). The final six-member committee (authors Berry, Novak, Withrow, Schmidt, Rarback, and Feucht) has a combined 125 years of clinical experience working in the field of nutrition and with children with ASD. Once identified, the expert panel assembled for a focus group in August 2014. A trained facilitator moderated the meeting using a semi-structured interview guide to elicit information about nutrition management of GI symptoms in this population. The committee subsequently used this information to develop clinical practice recommendations for conditions in which nutrition management is clinically indicated based on established models of care.35 Available guidelines and algorithms for constipation management in children11,35 served as templates for an ASD-specific algorithm and accompanying text. The Pediatric Nutrition Care Manual,9 which provides evidence-based practice guidelines for December 2015 Volume 115 Number 12
pediatric RDNs working in a variety of clinical settings, also informed the development process. To ensure relevant evidence was not omitted from the algorithm, comprehensive literature reviews regarding GI concerns,7 prevalence of feeding problems,14 and treatment of feeding disorders36 in ASD were reviewed for additional data.
DESCRIPTION OF THE ALGORITHM Evaluation and intervention recommendations were designed to assist clinicians with navigating potential barriers associated with food selectivity, caregiver-initiated complementary/alternative diet therapies, and/or nutritional deficits/excesses often observed in this population.14,37 The committee also emphasized the importance of a multidisciplinary approach during assessment and intervention to elucidate the causal relationship between nutritional intake and possible organic etiology, as well as provide complementary treatment avenues in cases involving severe food selectivity and/or lack of response to dietary intervention. This included coordinating care with input from medicine, behavioral psychology, occupational therapy, and speech-language pathology.38 Finally, the committee highlighted the need to consider a child’s possible behavioral
response (eg, tantrums, aggression) to changes in mealtime routine (eg, introduction of novel or non-preferred feeding demands) when planning an intervention. The derived algorithm describes 11 steps in nutrition evaluation and management of GI concerns in children with ASD to guide development and application of a prescriptive diet (Figure 2). A smooth-edged box represents a starting or ending point, a diamond shape indicates a question or decision, and a sharp-edged box corresponds to specific action or process undertaken by the clinician. Each shape is assigned a number that corresponds to accompanying text providing further detail (Figure 3). The algorithm begins with development of a prescriptive diet to alleviate GI dysfunction, which involves identifying potential barriers (ie, food selectivity, caregiver-initiated restrictions, gaps in knowledge) that would limit possible therapeutic foods. In cases involving dietary restriction (either child- or caregiver-mediated), the RDN must determine whether there is enough flexibility within the diet to develop an intervention. If foods are available, the prescriptive diet involves working within the confines of dietary restriction to increase daily servings of target foods and/or concurrently reduce intake of highly preferred food items (eg, crackers,
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PRACTICE APPLICATIONS chips). In cases involving severe food selectivity (ie, eating fewer than six different food items), nutrition therapy should occur concurrently with feeding therapy. During the assessment process, the RDN can help to identify safe foods as well as determine which foods might be causing the child pain and should therefore be avoided. Feeding therapy focuses on acceptance and increased (or decreased) intake of targeted foods for the dietary intervention.20,39 Greater flexibility with meal planning is possible for cases in which a family is willing to consider modifications to previously recommended and/or implemented diets. In such cases, the RDN has a greater palette of foods available with which to create a prescription diet to address GI symptoms consistent with medical nutrition therapy guidelines.9 With this said, insistence on sameness and behavioral rigidity are core features of ASD1 and the possibility of a reaction to the therapeutic diet should be considered throughout the assessment and treatment process. If a strong reaction is anticipated, caregivers are resistant to or are unwilling to modify or discontinue a current dietary treatment (eg, gluten-free, casein-free), and/or no foods can be identified for intervention, alternative medical strategies should be considered in consultation with a pediatric gastroenterologist. The algorithm also involves determining whether there are remaining gaps in the diet that need to be targeted by feeding intervention and/or the use of nutrition supplementation before arranging follow-up care. Supplementation in the form of vitamins and/or minerals, in cases of micronutrient deficits, or nutritionally complete drinks, in cases of energy deficits and/or macronutrient deficits in addition to micronutrient deficits, may be indicated if the child is not able to consume a nutritionally complete diet using food alone. This may be due to caregiver restriction or medically indicated elimination (ie, allergy/intolerance). Consistent with nutrition therapy in the general population, this should include use of elemental formula when medically suggested for conditions such as eosinophilic esophagitis (EoE), milk-protein intolerance, and multiple food allergies. The use of supplementation should also be considered if the current diet does not 1924
meet nutrition needs due to food selectivity, while concurrently referring to feeding therapy. As noted in the algorithm (Figure 3), the nutrition assessment should include screening for food intolerances, food allergies, and foods causing GI discomfort. Finally, to help practitioners apply this approach in the community setting and support future evaluation of the algorithm, descriptions on the application of the model with constipation and EoE were completed (Figure 4). Constipation was selected because it is one of the most common GI disorders among children with ASD7,11; EoE was chosen as an example due to established evidence regarding dietary intervention as a treatment for this GI disorder.40
IMPLICATIONS FOR CLINICAL PRACTICE Greater risk of general GI symptoms among children with ASD is well documented, yet much remains unknown regarding the recognition and treatment of these concerns due to lack of conclusive research on this topic.7,8 Dietary modification often plays a central role in managing GI symptoms in pediatric populations, as highlighted by a recent guideline for treating constipation in children with ASD.11 Clinical experience and review of the literature, however, suggest that high prevalence of food selectivity combined with frequent use of caregiver-initiated dietary restrictions necessitates modifications to existing practice. By combining data from clinical expertise and the extant literature, an expert committee established an algorithm for applying evidence-based nutrition practice guidelines9 to the evaluation and management of GI symptoms in ASD. In doing so, the project represents a critical first step toward developing standards of care that take into consideration the unique combination of dietary restriction and related medical/nutrition concerns in this population.14 As emphasized by the algorithm, nutrition management in ASD should involve a tiered approach. This involves first identifying and working through barriers that might impede the development of a prescriptive diet (eg, food selectivity) targeting GI concerns, followed by a more general focus on
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assuring that all nutrition-related concerns are evaluated and addressed during the course of intervention. Multidisciplinary collaboration in the evaluation and treatment process is also recommended, including coordinating care with a pediatric gastroenterologist, as well as involvement of feeding therapy in cases where severe food selectivity and/or behavior management during meals falls outside the RDN’s scope of practice. At this time, behavioral intervention is the only treatment for severe food selectivity in ASD with well-established empirical support,36,39 yet treatment must also consider factors influencing eating, such as GI discomfort, food allergies, sensory processing, and oral-motor skills, during assessment and intervention to maximize effectiveness.38 Finally, RDNs should assess a child’s possible behavioral response (eg, tantrums, aggression) to change in the meal, a consideration that should be foremost in the minds of clinicians when planning intervention, given the ubiquity of feeding problems in this population.14 A practice guideline of this nature reflects a more general need to further elucidate the role of nutrition management in ASD. Diet and ASD are frequently linked due to the prevalence of food selectivity, frequent use of diet as a complementary/alternative treatment avenue in this population, and an increased incidence of GI symptoms. In addition, food selectivity increases the risk of nutrition and/or medical concerns in ASD, including significant specific deficits (eg, lower intake of calcium and protein) and a higher number of overall nutritional deficits.14 This risk, however, may go undetected in pediatric settings without a detailed examination of nutrient intake because it does not necessarily translate into compromised growth or decreased energy intake, which typically trigger attention in pediatric settings.7 Evidence indicates that excessive consumption of processed snacks and calorie-dense foods is associated with overweight and obesity, which, in turn, is associated with increased prevalence of diet-related diseases (eg, obesity, cardiovascular disease) in both children and adults. Children with ASD experience obesity at higher rates compared to peers.41,42 A recent large-scale chart review suggests this trend extends into adulthood.43 December 2015 Volume 115 Number 12
PRACTICE APPLICATIONS Condition
Nutrition Treatment
Autism Spectrum DisorderLSpecific Considerations (Algorithm Box)
Constipation
Increase fluid and fiber in the diet (fruit, vegetables, whole grains)
Will the child eat fruits, vegetables, and whole grains (2)? If yes, are there enough accepted foods in the diet to create a nutritionally adequate diet (7)? If no, should the child be referred to feeding therapy (8)? Are some whole-grain products restricted by caregivers (3)? Is the caregiver open to adding whole-grain products to the diet (3a)? Are there other sources of fiber in the child’s diet (3c)? Does the caregiver know to offer fruits, vegetables, and whole grains (4)?
Daily physical activity
Does the child resist activity (4a)? Does the child have motor-planning concerns that require a specialist to determine physical activity options (4b)?
Add a bulk-forming agent/prebiotic/ probiotic to child’s daily regimen
Will the child take the supplement (2)? Does adding the supplement to food or drink increase the risk of refusal (2a)?
Correct nutritional deficiencies
Will the child eat the foods identified to correct nutritional deficiencies (2b)? Is the child only eating pureed foods due to difficulties swallowing? Are these foods commercially prepared infant foods (2)? Is the RDNa able to create a nutritionally complete diet given this selectivity (7)? Will the child eat appropriate volumes of less preferred foods to meet nutrition needs (5)?
Eliminate allergens in the diet
Are there enough foods in the child’s repertoire once allergens have been eliminated (2b)? Is the allergen-free diet in conflict with a caregiver-initiated diet (3)? Does the child need a supplement due to number of allergens (9) and will the child accept the supplement (2)?
Counsel on elimination diet
Are there enough foods in the child’s repertoire once allergens have been eliminated (2b)? Will the child need to participate in feeding therapy to consume enough foods to create a nutritionally complete diet (8)? Should supplementation be considered, given diet inadequacies (9)?
Eosinophilic esophagitis
a
RDN¼registered dietitian nutritionist.
Figure 4. Practical application of nutrition-management algorithm for gastrointestinal symptoms in autism spectrum disorder with constipation and eosinophilic esophagitis.
When compared to typically developing peers, adults with ASD experienced a 69% higher incidence of obesity, 42% greater risk of hypertension, and 50% increase in diabetes. This highlights the need to enhance involvement of RDNs in the broader diagnostic and treatment December 2015 Volume 115 Number 12
process, which would necessitate more definitive guidance regarding the timing and scope of involvement (possibly in a manner similar to the current algorithm) in order to maximize the contribution and subsequent benefit of nutrition management in ASD.
Finally, recommendations were designed to provide clinicians with a general roadmap for nutrition intervention in ASD vs a model for counseling caregivers on the merits and risks of elimination diets. Clinicians, however, will likely encounter this
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PRACTICE APPLICATIONS topic in practice, particularly when making inquiries about the use of and possible deviation from caregiverinitiated complementary/alternative diet therapies. With this in mind, an overarching consideration for nutrition management in ASD is to assure a healthy and well-balanced diet. In general, complementary/alternative diets target core features of ASD (ie, impairments in social communication, restriction in interests, and repetitive behaviors) as opposed to treating underlying GI concerns.44 Many different dietary treatments have been proposed to treat ASD, yet empirical investigation has not substantiated the use of dietary manipulation as an ASDfocused treatment.28 Without RDN guidance, the associated risks of these diets may outweigh the benefits. For example, provisional evidence suggests that use of a gluten-free, casein-free diet can lead to greater deficits in bone development among children with ASD.45,46 Despite the lack of evidence on the effectiveness of dietary intervention to influence behavioral expression of ASD, Elder and colleagues28 report that parents chose to continue with the diet after study conclusion due to perceived benefit, reinforcing the importance of nutrition management to assure a child’s diet is nutritionally adequate.
similar to that outlined by Furuta and colleagues.11 In addition, the guideline relies exclusively on parent report for assessment and intervention, which is common practice, given that communication barriers are often observed in children with ASD.7,8 When possible, child report of GI symptoms should be included in all aspects of assessment and intervention. These limitations accentuate the need to enhance our knowledge regarding assessment of GI symptoms and disorders in ASD,7 including factors guiding preference and response to novel feeding demands in this population.14 With this in mind, this project represents an important first step toward developing and evaluating nutritionmanagement strategies specifically tailored to the distinct dietary challenges in this population. A detailed algorithm is provided for clinicians in the hope of accelerating adoption of practice recommendations. Moving forward, greater clinical and research scrutiny is needed to increase awareness on this topic and support development of the best standards of care.
1.
FUTURE DIRECTIONS
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Buie T, Campbell DB, Fuchs GJ III, et al. Evaluation, diagnosis, and treatment of gastrointestinal disorders in individuals with ASDs: A consensus report. Pediatrics. 2010;125(suppl 1):S1-S18.
9.
Nutrition Care Manual. Gastrointestinal diseases. http://www.nutritioncaremanual. org/category.cfm?ncm_category_id¼13 &ncm_heading¼Nutrition%20Care. Accessed November 25, 2014.
10.
Mascarenhas MR, Enriquez L. What is pediatric nutrition support?. In: Baker S, ed. Pediatric Nutrition Support. Sudbury, MA: Jones and Bartlett; 2007:123-133.
11.
Furuta GT, Williams K, Kooros K, Kaul A, Panzer R, Coury D, Fuchs D. Management of constipation in children and adolescents with autism spectrum disorders. Pediatrics. 2012;130(suppl 2):S98-S105.
12.
Graf-Myles J, Farmer C, Thrum A. Dietary adequacy of children with autism compared with controls and the impact of the restricted diet. J Dev Behav Pediatr. 2013;34(7):449-459.
13.
Chaidez V, Hanse RL, Herz-Piccioto I. Gastrointestinal problems in children with autism, developmental delays, or typical development. J Autism Dev Disord. 2014;44(5):1117-1127.
14.
Sharp WG, Berry RC, McCracken C, et al. Feeding problems and nutrient intake in children with autism spectrum disorders: A meta-analysis and comprehensive review of the literature. J Autism Dev Disord. 2013;43(9):2159-2173.
15.
Bandini LG, Anderson SE, Curtin C, et al. Food selectivity in children with autism spectrum disorders and typically developing children. J Pediatr. 2010;157(2): 259-264.
16.
Schmitt L, Heiss CJ, Campdell E. A comparison of nutrient intake and eating behaviors of boys with and without autism. Topics in Clin Nutr. 2008;23(1):23-31.
17.
Lukens CT, Linscheid TR. Development and validation of an inventory to assess mealtime behavior problems in children with autism. J Autism Dev Disord. 2008;38(2):342-352.
18.
Martins Y, Young RL, Robson DC. Feeding and eating behaviors in children with autism and typically developing children. J Autism Dev Disord. 2008;38(10):18781887.
19.
Slavin JL. Position of the American Dietetic Association: Health implications of dietary fiber. J Am Diet Assoc. 2008;108(10):1716-1731.
20.
Sharp WG, Jaquess DL, Morton JF, Miles AG. A retrospective chart review of dietary diversity and feeding behavior of children with autism spectrum disorder before and after admission to a day treatment program. Focus Autism Other Dev Disabil. 2011;26(1):37-48.
21.
Kirby M, Danner E. Nutritional deficiencies in children on restricted diets. Pediatr Clin N Am. 2009;56(5):1085-1103.
22.
Jyonouchi H. Food allergy and autism spectrum disorders: Is there a link? Curr Allergy Asthma Rep. 2009;9(3):194-201.
23.
de Theije CG, Bavelaar BM, Lopes da Silva S, et al. Food allergy and foodbased therapies in neurodevelopmental
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The use of the algorithm proposed here provides a structured approach for management of GI symptoms in ASD and is intended to serve as a tool to individualize treatment to address GI symptoms, while lessening the risk of exacerbating potential nutrient deficits due to behavioral feeding concerns and caregiver-initiated restriction. Although there are unique barriers in working with children with ASD, the overarching goals of medical nutrition therapy are the same as they are in the general population: to provide adequate intake of macro- and micronutrients to promote optimal growth and development. Development of recommendations was based on expert opinion and clinical experience due to lack of consensus on nutrition management in ASD. Although constipation and EoE are provided as examples, field testing represents a critical next step to assess and refine the algorithm in a process
8.
3.
4.
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-V. Washington, DC: American Psychiatric Publishing, Inc; 2013. Croen LA, Grether JK, Selvin S, Croen LA, Grether JK, Selvin S. Descriptive epidemiology of autism in a California population: Who is at risk? J Autism Dev Disord. 2002;32(3):217-224. Centers for Disease Control and Prevention. Prevalence of Autism Spectrum Disorder among children aged 8 years—Autism and Developmental Disabilities Monitoring Network, 11 sites, United States, 2010. MMWR Surveill Summ. 2014;63(SS03):1-21. www.cdc.gov/mmwr/preview/mmwrhtml/ ss6302a1.htm?s_cid¼ss6302a1_w. Accessed November 15, 2014. Croen LA, Najjar DV, Ray GT, Lotspeich L, Bernal P. A comparison of health care utilization and costs of children with and without autism spectrum disorders in a large group-model heath plan. Pediatrics. 2006;118(4):e1203-e1211.
5.
Fletcher PC, Markoulakis R, Bryden PJ. The costs of caring for a child with an autism spectrum disorder. Issues Comp Pediatr Nurs. 2012;35(1):45-69.
6.
Kohane IS, McMurry A, Weber G, et al. The co-morbidity burden of children and young adults with autism spectrum disorders. PLoS One. 2012;7(4):e33224.
7.
McElhanon BO, McCracken C, Karpen S, Sharp WG. Gastrointestinal symptoms in autism spectrum disorders: A metaanalysis. Pediatrics. 2014;133(5):872883.
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PRACTICE APPLICATIONS disorders. Pediatr Allergy 2014;25(3):218-226. 24.
Gibson PR, Muir JG. Non-nutritional effects of food: An underutilized and understudied therapeutic tool in chronic gastrointestinal diseases. J Gastroenterol Hepatol. 2013;28(suppl 4):37-44.
25.
Halmos EP, Power VA, Shepherd SJ, Gibson PR, Muir JG. A diet low in FODMAPs reduces symptoms of irritable bowel syndrome. Gastroenterology. 2014;146(1):67-75.e5.
26.
27.
28.
29.
30.
31.
behavior: Pilot study. J Child Neurol. 2003;18:113-118.
Immunol.
Stevens LJ, Kuczek T, Burgess JR, Hurt E, Arnold LE. Dietary sensitivities and ADHD symptoms: 35 years of research. Clin Pediatr. 2011;50(4):279-293.
32.
Napoli E, Dueñas N, Giulivi C. Potential therapeutic use of the ketogenic diet in autism spectrum disorders. Front Pediatr. 2014;2:69.
33.
Kang DW, Park JG, Ilhan ZE, et al. Reduced incidence of Prevotella and other fermenters in intestinal microflora of autistic children. PLoS One. 2013;8(7):e68322.
34.
Louis P. Does the human gut microbiota contribute to the etiology of autism spectrum disorders? Dig Dis Sci. 2012;57(8): 1987-1990.
35.
McCann D, Barrett A, Cooper A, et al. Food additives and hyperactive behaviour in 3-year-old and 8/9-yearold children in the community: A randomised, double-blind, placebocontrolled trial. Lancet. 2007;370(9598): 1560-1567. Elder JH, Shankar M, Shuster J, Theriaque D, Burns S, Sherrill L. The gluten-free, casein-free diet in autism: Results of a preliminary double blind clinical trial. J Autism Dev Disord. 2006;36(3):413-420. Williams BL, Hornig M, Buie T, et al. Impaired carbohydrate digestion and transport and mucosal dysbiosis in the intestines of children with autism and gastrointestinal disturbances. PLoS One. 2011;6(9):e24585. Horvath K, Perman JA. Autism and gastrointestinal symptoms. Curr Gastroenterol Rep. 2002;4(3):251-258. Evangeliou A, Vlachonikolis I, Mihailidou H, et al. Application of a ketogenic diet in children with autistic
36.
37.
Constipation Guideline Committee of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. Evaluation and treatment of constipation in infants and children: Recommendations of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition. J Pediatr Gastroenterol Nutr. 2006;43(3): e1-e13. Sharp WG, Jaquess DL, Morton JS, Herzinger C. Pediatric feeding disorders: A quantitative synthesis of treatment outcomes. Clin Child Fam Psychol Rev. 2011;13(4):348-365. Hyman SL, Steward PA, Schmidt B, et al. Nutrient intake from food in children with autism. Pediatrics. 2012;130(suppl 2):S145-S153.
38.
Lukens CG, Silverman AH. Systematic review of psychological interventions for pediatric feeding problems. J Pediatr Psychol. 2014;39(8):903-917.
39.
Ledford JR, Gast DL. Feeding problems in children with autism spectrum disorders: A review. Focus Autism Other Dev Disablil. 2006;21(3):153-166.
40.
Arias A, Gonzalez-Cervera J, Tenias J, Lucendo AJ. Efficacy of dietary interventions for inducing histologic remission in patients with eosinophilic esophagitis: A systematic review and meta-analysis. Gastroenterology. 2014;146: 1639-1648.
41.
Curtin C, Anderson SE, Must A, Bandini L. The prevalence of obesity in children with autism: A secondary data analysis using nationally representative data from the National Survey of Children’s Health. BMC Pediatrics. 2010;10:11.
42.
Egan AM, Dreyer ML, Odar CC, Beckwith M, Garrison CB. Obesity in young children with autism spectrum disorders: Prevalence and associated factors. Child Obesity. 2013;9(2):125-131.
43.
Croen LA, Zerbo O, Qian Y, Massolo ML. Psychiatric and Medical Conditions Among Adults with ASD. Paper presented at the 14th Annual Meeting of the International Society for Autism Research (INSAR). Atlanta, GA, May 2014. Abstract available at: https://imfar.confex.com/ imfar/2014/webprogram/start.html. Accessed October 22, 2014.
44.
Geraghty M, Bates-Wall J, RatliffSchaub K, et al. Nutritional interventions and therapies in autism. ICAN. 2010;2(2): 120-133.
45.
Hediger ML, England LJ, Molloy CA, Yu KF, Manning-Courtney P, Mills JL. Reduced bone cortical thickness in boys with autism or autism spectrum disorder. J Autism Dev Disord. 2008;38(5):848-856.
46.
Neumeyer AM, O’Rourke JA, Massa A, et al. Brief report: Bone fractures in children and adults with autism spectrum disorders. J Autism Dev Disord. 2015;45(3):881-887.
DISCLOSURES STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.
FUNDING/SUPPORT This work was supported by a 2014 Education Grant from Nutricia North America.
December 2015 Volume 115 Number 12
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Topics of Professional Interest
Nutrition Management of Gastrointestinal Symptoms in Children with Autism Spectrum Disorder: Guideline from an Expert Panel
A
UTISM SPECTRUM DISORDER (ASD) is characterized by a core deficit in social communication with concomitant repetitive/perseverative behaviors and restriction in interests,1 and individuals
This article was written by Rashelle C. Berry, MPH, MS, RD, CSP, lead nutritionist, Pediatric Feeding Disorders Program, Marcus Autism Center, Atlanta, GA; Patricia Novak, MPH, RD, EMPOWER project coordinator, Children’s Hospital of Los Angeles, Los Angeles, CA; Nicole Withrow, PhD, RD, assistant professor and dietetic internship coordinator, University of Northern Colorado, Greeley; Brianne Schmidt, RD, clinical nutrition specialist, Division of Neurodevelopmental and Behavioral Pediatrics, Golisano Children’s Hospital at Strong, University of Rochester Medical Center, Rochester, NY; Sheah Rarback, MS, RD, director of nutrition, Mailman Center for Child Development, Miller School of Medicine, University of Miami, Miami, FL; Sharon Feucht, MA, RD, nutritionist, Center on Human Development and Disability, University of Washington, Seattle; Kristen K. Criado, PhD, psychologist, Pediatric Feeding Disorders Program, Marcus Autism Center, Atlanta, GA, and assistant professor, Department of Pediatrics, Emory University School of Medicine, Atlanta, GA; and William G. Sharp, PhD, director, Pediatric Feeding Disorders Program, Marcus Autism Center, Atlanta, GA, and assistant professor, Department of Pediatrics, Emory University School of Medicine, Atlanta, GA. http://dx.doi.org/10.1016/j.jand.2015.05.016 Available online 9 July 2015
To take the Continuing Professional Education quiz for this article, log in to www.eatrightPRO. org, go to the My Account section of the My Academy Toolbar, click the “Access Quiz” link, click “Journal Article Quiz” on the next page, and then click the “Additional Journal CPE quizzes” button to view a list of available quizzes.
ª 2015 by the Academy of Nutrition and Dietetics.
with ASD experience varying degrees of impairment.2 The estimated prevalence of ASD in pediatric populations has climbed dramatically during the past decade, with approximately 1 in every 68 children currently meeting diagnostic criteria in the United States.3 High prevalence occurs against a backdrop of increased health care costs 4 and social burden. 5 Medical comorbidities are significantly overrepresented compared with other pediatric populations, and children with ASD often present with medical conditions affecting multiple organ systems.6 Dysfunction of the gastrointestinal (GI) tract is among the most frequently cited comorbidities. A recent meta-analysis indicated that children with ASD were four times more likely to experience general GI complaints, are more than three times more prone to experience constipation and diarrhea, and complain twice as frequently about abdominal pain compared with peers.7 Lack of data prevented analysis of other GI symptoms (eg, gastroesophageal reflux, celiac disease, lactose intolerance) typically associated with organic etiologies; however, a 2010 consensus report concluded that, at a minimum, rates of other GI pathophysiology in ASD should be viewed as occurring at similar levels to those observed in the general population.8 This includes consideration of the potential contribution of factors such as GI motility, altered gut microbiome, immune abnormalities, and food allergy when GI symptoms are detected.7 In addition to calling for greater research scrutiny in this area, the expert panel of pediatric gastroenterologists also emphasized the need to develop evidence-based standards for the evaluation and treatment of GI symptoms in ASD. Nutrition management is often critical in the treatment of GI symptoms in other
pediatric populations9,10; however, no guidelines are available for adapting existing practices for use among children with ASD. Current standards of care might be neither practical nor feasible, given the combination of behavioral, developmental, medical, and social deficits associated with the condition. For example, children with ASD often present with limited communication and, as a result, their symptom presentation may be unusual compared with that of their peers.7,8,11,12 In many cases, GI symptoms might only manifest as a change in behavior, such as the emergence or exacerbation of problem behaviors like aggression, self-injury, sleep disturbance, or irritability.7,13 As a result, recognition and treatment of GI disorders in children with ASD remain ill-defined and poorly understood,11 particularly when it comes to the challenge of untangling the relative contribution of diet when underlying GI pathology is suspected. The diagnostic and intervention process is further complicated by the high prevalence of feeding problems in ASD. Evidence suggests children with ASD have a fivefold increase in problematic eating and feeding behaviors compared with typically developing peers.14 Food selectivity, defined as a limited food repertoire (eg, only eating a few foods and/or rejection of one or more food groups) or high intake of a single food,15 is the most frequently documented feeding issue associated with ASD. Dietary intake in ASD often involves strong preferences for highly processed foods, snacks, and sweets,16 and a lower intake of fruits and vegetables.15,17,18 High intake of simple carbohydrates and fat coinciding with low intake of fiber complicates the diagnostic process, making it difficult to determine whether food selectivity directly contributes to the onset of GI symptoms or simply exacerbates a preexisting GI condition.19 For example, a child may be constipated
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PRACTICE APPLICATIONS due to poor motility as the result of impaired gastric emptying and/or low muscle tone, with more severe symptom presentation in cases involving poor dietary diversity. Alternatively, constipation could be the direct result of a diet lacking in fruits, vegetables, and whole grains and, therefore, low in fiber and fluid.7 In both cases, nutrition intervention can improve overall symptom presentation, however, a more detailed medical workup (eg, allergy, GI) would also be necessary if possible organic etiology is suspected. When developing a nutrition intervention, food selectivity may place limits on introducing and/or removing foods from the diet. Specifically, restricted patterns of intake in ASD are often maintained by refusal behaviors (eg, tantrums, aggression) in response to the presentation of nonpreferred foods or novel feeding demands.20 As a result, caregivers may be unable to adhere to clinical recommendations due to the intensity of their child’s behavioral response to the new therapeutic diet. In addition, it may be difficult to anticipate how a child will respond to efforts to
remove and/or replace preferred foods, including the possibility of further selfimposed dietary restriction after intervention beyond targeted foods. With this in mind, the clinician must determine how to best manage the child’s nutrition while considering his or her overall medical status. Nutrition management must also account for the proliferation of caregivermediated dietary restrictions in the ASD community. Children with ASD are significantly more likely to be placed on caregiver-initiated complementary/ alternative diet therapies as compared to peers.21 Common dietary interventions applied in this population are listed in Figure 1. In general, these diets restrict or completely eliminate certain food groups. For example, the glutenfree, casein-free diet, arguably the most well-known type of dietary manipulation in ASD, eliminates gluten (found in wheat, barley, and rye) and casein (found in cow’s milk dairy products).28 Without the guidance of a registered dietitian nutritionist (RDN), this level of restriction may increase risk of macronutrient and micronutrient
Diet
Foods restricted
Elimination diets/elemental diet22,23
Elimination diet (6 foods): milk, egg, wheat, soy, peanuts/tree nuts, fish/shellfish Elemental: all foods except an amino acid based formula
Fermentable oligo-dimonosaccharides and polyols24,25
Foods containing fructose (eg, fruit, highfructose corn syrup), lactose (eg, cow’s milk dairy), fructans (eg, wheat, onion, garlic), galactans (eg, legumes), and polyols (eg, sorbitol, cherries, avocados)
Food coloring/food additives avoidance26,27
Foods that contain food color additives (food dye)
Gluten-free, casein-free28-30
Foods containing gluten (eg, bread, pasta) and casein (eg, cow’s milk, yogurt)
Ketogenic diet or modified Atkins diet31,32
Carbohydrate-rich foods, including sugar
Specific carbohydrate diet29,33,34
Cereal grains (eg, wheat, oats, rice), processed meats (eg, lunch meats, hot dogs), canned vegetables, canned fruits, most fruit juices, soy beans, chick peas, bean sprouts, mung beans, fava beans, yogurt, milk, processed cheese, tubers (eg, potatoes, yams), curry, onion powder, garlic powder
Figure 1. Possible caregiver-initiated restrictions in autism spectrum disorder (in alphabetical order). 1920
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deficiencies in a population already prone for underlying dietary insufficiencies related to food selectivity,14 and the potential for further nutritional deficits and associated health concerns presents unique challenges for designing interventions. When a caregiver-initiated or other restrictive diet is in place, the RDN must work with the family to determine which foods (if any) can be added, removed, and/or reintroduced to alleviate GI concerns, while concurrently attempting to best meet nutrition needs. Many caregivers, however, may be resistant to incorporate recommendations that involve the reintroduction of currently restricted foods. If specific foods previously removed place the child at nutrition risk and cannot be reintroduced, appropriate substitutions need to be identified; although this may be difficult in cases involving extremely limited food repertoires and resistance to the introduction of new foods. The unique dietary, medical, and behavioral challenges observed in children with ASD combined with an overall lack of data on management of GI disorders in this population11 presents a pressing need to develop a guideline for nutrition intervention. Consistent with previous work to develop standards of care in ASD,11 expert opinion was viewed as a critical first step in this process, given the absence of relevant data. Therefore, a committee of RDNs specializing in the nutrition care of children with ASD was formed and a focus group was conducted to develop a clinical practice guideline. This article describes the process of convening the expert committee, outlines considerations for adapting existing nutrition practice, and presents a guideline for the nutrition management of GI symptoms in children with ASD.
FOCUS GROUP MEETING AND ALGORITHM DEVELOPMENT The first step toward creating a standard of care for RDNs to use when working with children with GI symptoms and ASD involved identifying experts in the field. Our search process consisted of contacting major autism treatment centers in the United States, listserv solicitation through the Autism Speaks’ Autism Treatment Network, and comprehensive review December 2015 Volume 115 Number 12
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Suspected or confirmed GI problem and nutrition intervention clinically indicated, begin with nutrition assessment 1
Food selectivity a concern? 2
Caregiver initiated diet in place?
No
Gaps in caregiver knowledge?
No 3
No 4
Provider works to identify barriers to diet recs 4a
Yes
Yes
Yes Caregiver willing to adjust diet? 3a
RD identifies barriers to meeting appropriate volume of target foods
Provider works to identify foods within diet restrictions
No
3b
2a Yes Foods within existing repertoire? 2b
Barriers within scope of practice? 4b
Yes No Foods within existing repertoire? 3c
Yes Yes
5
No RD assess possible nutrition concerns (Box 9) and refers to appropriate medical intervention (Box 11) 3d
6
Diet nutritionally adequate?
4c
7
No
Referral to behavioral intervention specialist to address food selectivity/meal structure
RD refers to appropriate behavioral (Box 8) medical intervention (Box 11)
No
Yes
Consider supplementation (e.g., nutritionally complete drink)
8
9
Arrange follow-up to meet treatment goals 10
Adjust nutritional recommendations (if applicable) AND GI consult to identify red flags or medical alternatives
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11
No
Treatment reduces/eliminates symptoms? 10
Yes
Figure 2. Algorithm for nutrition management of gastrointestinal concerns in children with autism spectrum disorder.
Continue Therapy/Arrange long term follow-up 10
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RD counsels family on treatment approach: Readjust diet to involve rec volume of target foods
RD counsels family on treatment approach: Increase or decrease volume of select target foods
No
PRACTICE APPLICATIONS Box
Details
1
Full nutrition assessment after referral to address GI symptoms. In addition to a standard assessment (ie, food intake analysis, anthropometrics, labs), assessment should include detailed discussion and identification of potential foods that may be causing an adverse reaction in the child. This includes assessment of known food allergies, as well as evaluation of risk for additional food allergies, food intolerances (ie, lactose intolerance), and other potential adverse reactions to foods (ie, celiac disease).
2
Food selectivity is present if child has a limited food repertoire, high-frequency consumption of a few foods, and significant problem behaviors, including, but not limited to crying, leaving the meal, gagging, aggressing, and/or vomiting when nonpreferred foods are presented.
2a
Full assessment of dietary repertoire, including detailed examination of foods accepted by major food group (fruits, vegetables, meats/beans, dairy, grains). Include questions to determine the volume and frequency of intake. Assess responses to changes in meal routines, such as environment, temperature, method of presentation, and food type/texture presented.
2b
Current list of accepted foods evaluated to determine if consistent with proposed medical nutrition therapy guidelines.
3
Caregiver-initiated diet includes alternative diet therapies (eg, gluten-free, casein-free) and medically prescribed diets (eg, hypoallergenic).
3a
Discuss with caregiver acceptability and ability to veer from current dietary plan. This precludes medically indicated diets based on underlying organic pathology (eg, celiac disease, food allergy).
3b
Full assessment of acceptable foods within dietary restrictions, including detailed examination of foods accepted by major food group (fruits, vegetables, meats/beans, dairy, grains). Include questions to determine the volume and frequency of intake. Assess behavioral response to changes in meal routines, such environment, temperature, method of presentation, and food presented. Consider how dietary changes will impact development and social inclusion.
3c
Clinician works to find foods that are congruent with dietary repertoire and will meet medical nutrition therapy guidelines for GI symptoms.
3d
If nutrition intervention is not possible based on restrictions, a two-pronged approach is warranted: Assess for any nutritional insufficiencies and whether supplementation is indicated. Determine the most effective method to assure formula acceptance. Refer to medical provider to consider alternative treatment approaches.
4
No level of dietary restriction (food selectivity or caregiver-initiated) identified. Caregiver and child will be able to follow recommendations as outlined by registered dietitian nutritionist.
4a
Typical nutrition assessment of factors influencing nutritional status, such as meal planning, food security, and ability to prepare food. Additional barriers to consider can include the child’s general behavior, sensory processing, cognitive development, communication skills, oral health and motor planning, family socioeconomic circumstances, and community support and resources.
4b
Assess whether barriers fall within the scope of dietetics. Concerns falling outside of scope include need for parent training to address disruptive behavior, motor dysfunction, sensory concerns, and/or possible neglect.
4c
If nutrition intervention is not possible based on restrictions, a two-pronged approach is warranted: Refer to feeding team. Refer to medical provider to consider alternative treatment approaches (including nonoral feeds, if indicated).
5
Treatment approach involves using only preferred foods to create a prescription diet to address GI concerns. Volumes of foods typically presented might be adjusted to meet treatment needs. (continued on next page)
Figure 3. Accompanying text for algorithm for nutrition management of gastrointestinal concerns in children with autism spectrum disorder.
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PRACTICE APPLICATIONS Box
Details
6
Treatment approach involves developing meal plan to address GI concerns in line with medical nutrition therapy guidelines. While consideration should be given to possible behavioral response to changes related to autism spectrum disorders, greater flexibility in treatment planning is possible due to lack of caregiver restriction.
7
Re-evaluation of diet, growth, and weight change occurs after prescription has been provided. This might include dietary analysis using dietary recall or food intake records. Labs can be ordered if there is continued concern of dietary insufficiencies. Goal to assure overall nutrition planning with optimal energy and nutrient intake.
8
Referral to a feeding therapist is indicated if prescribed diet is not able to be followed due to mealtime difficulties with the introduction of nonpreferred foods or if general behavior-management during meals is needed due to changes in meal routines.
9
Nutrition supplementation (vitamins, minerals, and/or nutritionally complete drink) is indicated if current diet does not meet nutrition needs or if the level of dietary restriction needed (ie, allergies, GI concerns) does not allow for optimal intake from foods alone.
10
Follow up includes reassessment of growth, nutrition, and alleviation of GI symptoms
11
Provider works to adjust nutrition recommendations to alleviate GI symptoms. If recommended diet is ineffective, provider should refer back to physician to determine medical alternatives.
Figure 3. (continued) Accompanying text for algorithm for nutrition management of gastrointestinal concerns in children with autism spectrum disorder.
of the literature. The selection criteria required committee members to be certified as an RDN; spend at least 25% of professional time engaged in clinical nutrition activities (assessment and/or treatment) with children with ASD; have practiced in the field of nutrition for at least 3 years; and possess experience (past or current) working in a multidisciplinary environment (eg, medical or research center, feeding clinic). The final six-member committee (authors Berry, Novak, Withrow, Schmidt, Rarback, and Feucht) has a combined 125 years of clinical experience working in the field of nutrition and with children with ASD. Once identified, the expert panel assembled for a focus group in August 2014. A trained facilitator moderated the meeting using a semi-structured interview guide to elicit information about nutrition management of GI symptoms in this population. The committee subsequently used this information to develop clinical practice recommendations for conditions in which nutrition management is clinically indicated based on established models of care.35 Available guidelines and algorithms for constipation management in children11,35 served as templates for an ASD-specific algorithm and accompanying text. The Pediatric Nutrition Care Manual,9 which provides evidence-based practice guidelines for December 2015 Volume 115 Number 12
pediatric RDNs working in a variety of clinical settings, also informed the development process. To ensure relevant evidence was not omitted from the algorithm, comprehensive literature reviews regarding GI concerns,7 prevalence of feeding problems,14 and treatment of feeding disorders36 in ASD were reviewed for additional data.
DESCRIPTION OF THE ALGORITHM Evaluation and intervention recommendations were designed to assist clinicians with navigating potential barriers associated with food selectivity, caregiver-initiated complementary/alternative diet therapies, and/or nutritional deficits/excesses often observed in this population.14,37 The committee also emphasized the importance of a multidisciplinary approach during assessment and intervention to elucidate the causal relationship between nutritional intake and possible organic etiology, as well as provide complementary treatment avenues in cases involving severe food selectivity and/or lack of response to dietary intervention. This included coordinating care with input from medicine, behavioral psychology, occupational therapy, and speech-language pathology.38 Finally, the committee highlighted the need to consider a child’s possible behavioral
response (eg, tantrums, aggression) to changes in mealtime routine (eg, introduction of novel or non-preferred feeding demands) when planning an intervention. The derived algorithm describes 11 steps in nutrition evaluation and management of GI concerns in children with ASD to guide development and application of a prescriptive diet (Figure 2). A smooth-edged box represents a starting or ending point, a diamond shape indicates a question or decision, and a sharp-edged box corresponds to specific action or process undertaken by the clinician. Each shape is assigned a number that corresponds to accompanying text providing further detail (Figure 3). The algorithm begins with development of a prescriptive diet to alleviate GI dysfunction, which involves identifying potential barriers (ie, food selectivity, caregiver-initiated restrictions, gaps in knowledge) that would limit possible therapeutic foods. In cases involving dietary restriction (either child- or caregiver-mediated), the RDN must determine whether there is enough flexibility within the diet to develop an intervention. If foods are available, the prescriptive diet involves working within the confines of dietary restriction to increase daily servings of target foods and/or concurrently reduce intake of highly preferred food items (eg, crackers,
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PRACTICE APPLICATIONS chips). In cases involving severe food selectivity (ie, eating fewer than six different food items), nutrition therapy should occur concurrently with feeding therapy. During the assessment process, the RDN can help to identify safe foods as well as determine which foods might be causing the child pain and should therefore be avoided. Feeding therapy focuses on acceptance and increased (or decreased) intake of targeted foods for the dietary intervention.20,39 Greater flexibility with meal planning is possible for cases in which a family is willing to consider modifications to previously recommended and/or implemented diets. In such cases, the RDN has a greater palette of foods available with which to create a prescription diet to address GI symptoms consistent with medical nutrition therapy guidelines.9 With this said, insistence on sameness and behavioral rigidity are core features of ASD1 and the possibility of a reaction to the therapeutic diet should be considered throughout the assessment and treatment process. If a strong reaction is anticipated, caregivers are resistant to or are unwilling to modify or discontinue a current dietary treatment (eg, gluten-free, casein-free), and/or no foods can be identified for intervention, alternative medical strategies should be considered in consultation with a pediatric gastroenterologist. The algorithm also involves determining whether there are remaining gaps in the diet that need to be targeted by feeding intervention and/or the use of nutrition supplementation before arranging follow-up care. Supplementation in the form of vitamins and/or minerals, in cases of micronutrient deficits, or nutritionally complete drinks, in cases of energy deficits and/or macronutrient deficits in addition to micronutrient deficits, may be indicated if the child is not able to consume a nutritionally complete diet using food alone. This may be due to caregiver restriction or medically indicated elimination (ie, allergy/intolerance). Consistent with nutrition therapy in the general population, this should include use of elemental formula when medically suggested for conditions such as eosinophilic esophagitis (EoE), milk-protein intolerance, and multiple food allergies. The use of supplementation should also be considered if the current diet does not 1924
meet nutrition needs due to food selectivity, while concurrently referring to feeding therapy. As noted in the algorithm (Figure 3), the nutrition assessment should include screening for food intolerances, food allergies, and foods causing GI discomfort. Finally, to help practitioners apply this approach in the community setting and support future evaluation of the algorithm, descriptions on the application of the model with constipation and EoE were completed (Figure 4). Constipation was selected because it is one of the most common GI disorders among children with ASD7,11; EoE was chosen as an example due to established evidence regarding dietary intervention as a treatment for this GI disorder.40
IMPLICATIONS FOR CLINICAL PRACTICE Greater risk of general GI symptoms among children with ASD is well documented, yet much remains unknown regarding the recognition and treatment of these concerns due to lack of conclusive research on this topic.7,8 Dietary modification often plays a central role in managing GI symptoms in pediatric populations, as highlighted by a recent guideline for treating constipation in children with ASD.11 Clinical experience and review of the literature, however, suggest that high prevalence of food selectivity combined with frequent use of caregiver-initiated dietary restrictions necessitates modifications to existing practice. By combining data from clinical expertise and the extant literature, an expert committee established an algorithm for applying evidence-based nutrition practice guidelines9 to the evaluation and management of GI symptoms in ASD. In doing so, the project represents a critical first step toward developing standards of care that take into consideration the unique combination of dietary restriction and related medical/nutrition concerns in this population.14 As emphasized by the algorithm, nutrition management in ASD should involve a tiered approach. This involves first identifying and working through barriers that might impede the development of a prescriptive diet (eg, food selectivity) targeting GI concerns, followed by a more general focus on
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assuring that all nutrition-related concerns are evaluated and addressed during the course of intervention. Multidisciplinary collaboration in the evaluation and treatment process is also recommended, including coordinating care with a pediatric gastroenterologist, as well as involvement of feeding therapy in cases where severe food selectivity and/or behavior management during meals falls outside the RDN’s scope of practice. At this time, behavioral intervention is the only treatment for severe food selectivity in ASD with well-established empirical support,36,39 yet treatment must also consider factors influencing eating, such as GI discomfort, food allergies, sensory processing, and oral-motor skills, during assessment and intervention to maximize effectiveness.38 Finally, RDNs should assess a child’s possible behavioral response (eg, tantrums, aggression) to change in the meal, a consideration that should be foremost in the minds of clinicians when planning intervention, given the ubiquity of feeding problems in this population.14 A practice guideline of this nature reflects a more general need to further elucidate the role of nutrition management in ASD. Diet and ASD are frequently linked due to the prevalence of food selectivity, frequent use of diet as a complementary/alternative treatment avenue in this population, and an increased incidence of GI symptoms. In addition, food selectivity increases the risk of nutrition and/or medical concerns in ASD, including significant specific deficits (eg, lower intake of calcium and protein) and a higher number of overall nutritional deficits.14 This risk, however, may go undetected in pediatric settings without a detailed examination of nutrient intake because it does not necessarily translate into compromised growth or decreased energy intake, which typically trigger attention in pediatric settings.7 Evidence indicates that excessive consumption of processed snacks and calorie-dense foods is associated with overweight and obesity, which, in turn, is associated with increased prevalence of diet-related diseases (eg, obesity, cardiovascular disease) in both children and adults. Children with ASD experience obesity at higher rates compared to peers.41,42 A recent large-scale chart review suggests this trend extends into adulthood.43 December 2015 Volume 115 Number 12
PRACTICE APPLICATIONS Condition
Nutrition Treatment
Autism Spectrum DisorderLSpecific Considerations (Algorithm Box)
Constipation
Increase fluid and fiber in the diet (fruit, vegetables, whole grains)
Will the child eat fruits, vegetables, and whole grains (2)? If yes, are there enough accepted foods in the diet to create a nutritionally adequate diet (7)? If no, should the child be referred to feeding therapy (8)? Are some whole-grain products restricted by caregivers (3)? Is the caregiver open to adding whole-grain products to the diet (3a)? Are there other sources of fiber in the child’s diet (3c)? Does the caregiver know to offer fruits, vegetables, and whole grains (4)?
Daily physical activity
Does the child resist activity (4a)? Does the child have motor-planning concerns that require a specialist to determine physical activity options (4b)?
Add a bulk-forming agent/prebiotic/ probiotic to child’s daily regimen
Will the child take the supplement (2)? Does adding the supplement to food or drink increase the risk of refusal (2a)?
Correct nutritional deficiencies
Will the child eat the foods identified to correct nutritional deficiencies (2b)? Is the child only eating pureed foods due to difficulties swallowing? Are these foods commercially prepared infant foods (2)? Is the RDNa able to create a nutritionally complete diet given this selectivity (7)? Will the child eat appropriate volumes of less preferred foods to meet nutrition needs (5)?
Eliminate allergens in the diet
Are there enough foods in the child’s repertoire once allergens have been eliminated (2b)? Is the allergen-free diet in conflict with a caregiver-initiated diet (3)? Does the child need a supplement due to number of allergens (9) and will the child accept the supplement (2)?
Counsel on elimination diet
Are there enough foods in the child’s repertoire once allergens have been eliminated (2b)? Will the child need to participate in feeding therapy to consume enough foods to create a nutritionally complete diet (8)? Should supplementation be considered, given diet inadequacies (9)?
Eosinophilic esophagitis
a
RDN¼registered dietitian nutritionist.
Figure 4. Practical application of nutrition-management algorithm for gastrointestinal symptoms in autism spectrum disorder with constipation and eosinophilic esophagitis.
When compared to typically developing peers, adults with ASD experienced a 69% higher incidence of obesity, 42% greater risk of hypertension, and 50% increase in diabetes. This highlights the need to enhance involvement of RDNs in the broader diagnostic and treatment December 2015 Volume 115 Number 12
process, which would necessitate more definitive guidance regarding the timing and scope of involvement (possibly in a manner similar to the current algorithm) in order to maximize the contribution and subsequent benefit of nutrition management in ASD.
Finally, recommendations were designed to provide clinicians with a general roadmap for nutrition intervention in ASD vs a model for counseling caregivers on the merits and risks of elimination diets. Clinicians, however, will likely encounter this
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PRACTICE APPLICATIONS topic in practice, particularly when making inquiries about the use of and possible deviation from caregiverinitiated complementary/alternative diet therapies. With this in mind, an overarching consideration for nutrition management in ASD is to assure a healthy and well-balanced diet. In general, complementary/alternative diets target core features of ASD (ie, impairments in social communication, restriction in interests, and repetitive behaviors) as opposed to treating underlying GI concerns.44 Many different dietary treatments have been proposed to treat ASD, yet empirical investigation has not substantiated the use of dietary manipulation as an ASDfocused treatment.28 Without RDN guidance, the associated risks of these diets may outweigh the benefits. For example, provisional evidence suggests that use of a gluten-free, casein-free diet can lead to greater deficits in bone development among children with ASD.45,46 Despite the lack of evidence on the effectiveness of dietary intervention to influence behavioral expression of ASD, Elder and colleagues28 report that parents chose to continue with the diet after study conclusion due to perceived benefit, reinforcing the importance of nutrition management to assure a child’s diet is nutritionally adequate.
similar to that outlined by Furuta and colleagues.11 In addition, the guideline relies exclusively on parent report for assessment and intervention, which is common practice, given that communication barriers are often observed in children with ASD.7,8 When possible, child report of GI symptoms should be included in all aspects of assessment and intervention. These limitations accentuate the need to enhance our knowledge regarding assessment of GI symptoms and disorders in ASD,7 including factors guiding preference and response to novel feeding demands in this population.14 With this in mind, this project represents an important first step toward developing and evaluating nutritionmanagement strategies specifically tailored to the distinct dietary challenges in this population. A detailed algorithm is provided for clinicians in the hope of accelerating adoption of practice recommendations. Moving forward, greater clinical and research scrutiny is needed to increase awareness on this topic and support development of the best standards of care.
1.
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Buie T, Campbell DB, Fuchs GJ III, et al. Evaluation, diagnosis, and treatment of gastrointestinal disorders in individuals with ASDs: A consensus report. Pediatrics. 2010;125(suppl 1):S1-S18.
9.
Nutrition Care Manual. Gastrointestinal diseases. http://www.nutritioncaremanual. org/category.cfm?ncm_category_id¼13 &ncm_heading¼Nutrition%20Care. Accessed November 25, 2014.
10.
Mascarenhas MR, Enriquez L. What is pediatric nutrition support?. In: Baker S, ed. Pediatric Nutrition Support. Sudbury, MA: Jones and Bartlett; 2007:123-133.
11.
Furuta GT, Williams K, Kooros K, Kaul A, Panzer R, Coury D, Fuchs D. Management of constipation in children and adolescents with autism spectrum disorders. Pediatrics. 2012;130(suppl 2):S98-S105.
12.
Graf-Myles J, Farmer C, Thrum A. Dietary adequacy of children with autism compared with controls and the impact of the restricted diet. J Dev Behav Pediatr. 2013;34(7):449-459.
13.
Chaidez V, Hanse RL, Herz-Piccioto I. Gastrointestinal problems in children with autism, developmental delays, or typical development. J Autism Dev Disord. 2014;44(5):1117-1127.
14.
Sharp WG, Berry RC, McCracken C, et al. Feeding problems and nutrient intake in children with autism spectrum disorders: A meta-analysis and comprehensive review of the literature. J Autism Dev Disord. 2013;43(9):2159-2173.
15.
Bandini LG, Anderson SE, Curtin C, et al. Food selectivity in children with autism spectrum disorders and typically developing children. J Pediatr. 2010;157(2): 259-264.
16.
Schmitt L, Heiss CJ, Campdell E. A comparison of nutrient intake and eating behaviors of boys with and without autism. Topics in Clin Nutr. 2008;23(1):23-31.
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Lukens CT, Linscheid TR. Development and validation of an inventory to assess mealtime behavior problems in children with autism. J Autism Dev Disord. 2008;38(2):342-352.
18.
Martins Y, Young RL, Robson DC. Feeding and eating behaviors in children with autism and typically developing children. J Autism Dev Disord. 2008;38(10):18781887.
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Slavin JL. Position of the American Dietetic Association: Health implications of dietary fiber. J Am Diet Assoc. 2008;108(10):1716-1731.
20.
Sharp WG, Jaquess DL, Morton JF, Miles AG. A retrospective chart review of dietary diversity and feeding behavior of children with autism spectrum disorder before and after admission to a day treatment program. Focus Autism Other Dev Disabil. 2011;26(1):37-48.
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Kirby M, Danner E. Nutritional deficiencies in children on restricted diets. Pediatr Clin N Am. 2009;56(5):1085-1103.
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Jyonouchi H. Food allergy and autism spectrum disorders: Is there a link? Curr Allergy Asthma Rep. 2009;9(3):194-201.
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de Theije CG, Bavelaar BM, Lopes da Silva S, et al. Food allergy and foodbased therapies in neurodevelopmental
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The use of the algorithm proposed here provides a structured approach for management of GI symptoms in ASD and is intended to serve as a tool to individualize treatment to address GI symptoms, while lessening the risk of exacerbating potential nutrient deficits due to behavioral feeding concerns and caregiver-initiated restriction. Although there are unique barriers in working with children with ASD, the overarching goals of medical nutrition therapy are the same as they are in the general population: to provide adequate intake of macro- and micronutrients to promote optimal growth and development. Development of recommendations was based on expert opinion and clinical experience due to lack of consensus on nutrition management in ASD. Although constipation and EoE are provided as examples, field testing represents a critical next step to assess and refine the algorithm in a process
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DISCLOSURES STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.
FUNDING/SUPPORT This work was supported by a 2014 Education Grant from Nutricia North America.
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