Allergy
Allergy
Allergy
Review
Mirna Chehade, MD, MPH *; Rosan Meyer, RD, PhD y; Alexia Beauregard, MS, RD z
* Mount Sinai Center for Eosinophilic Disorders, Icahn School of Medicine at Mount Sinai, New York, New York
y
Department of Pediatrics, Imperial College, London, England
z
The Ellyn Satter Institute, Madison, Wisconsin
Key Messages
NoneIgE-mediated food allergic gastrointestinal (GI) disorders can disrupt a child’s feeding skill acquisition, resulting in feeding
difficulties.
Symptoms related to noneIgE-mediated food allergic GI disorders can affect the relationship children have with food.
Overly restricted dietary elimination diets in early childhood can limit exposure and increase feeding difficulties.
Feeding difficulties can result in nutritional deficiencies and faltering growth. Therefore, timely recognition and referral for man-
agement are of paramount importance.
Several management approaches to feeding difficulty exist, dictated by the type of feeding difficulty present.
Successful management of a child with feeding difficulty is best achieved using a multidisciplinary approach, with addressing the
child’s feeding and the caregiver feeding style being equally important.
A R T I C L E I N F O A B S T R A C T
Article history: Objective: To review the signs and symptoms of feeding difficulties in children with noneIgE-mediated food
Received for publication January 8, 2019.
allergic gastrointestinal disorders and provide practical advice, with the goal of guiding the practitioner to timely
Received in revised form March 11, 2019.
Accepted for publication March 15, 2019. referral for further evaluation and therapy. Various management approaches are also discussed.
Data Sources: Articles and chapters related to normal feeding patterns and the diagnosis and management
of feeding difficulties in children were reviewed.
Study Selections: Selections were based on relevance to the topic and inclusion of diagnostic and man-
agement recommendations.
Results: Because most noneIgE-mediated food allergic gastrointestinal disorders occur in early childhood,
feeding skills can be disrupted. Feeding difficulties can result in nutritional deficiencies, faltering growth, and a
significant impact on quality of life. Specific symptoms related to each noneIgE-mediated food allergic
gastrointestinal disorder can lead to distinctive presentations, which should be differentiated from simple picky
eating. Successful management of feeding difficulties requires that the health care team views the problem as a
relational disorder between the child and the caregiver and views its association with the symptoms experi-
enced as a result of the noneIgE-mediated food allergic gastrointestinal disorder. Addressing the child’s
Reprints: Mirna Chehade, MD, MPH, Mount Sinai Center for Eosinophilic Disorders, Icahn School of Medicine at Mount Sinai, One Gustave L. Levy Place, Box 1198, New York,
NY 10029; E-mail: mirna.chehade@mssm.edu.
Disclosures: Dr Chehade received research funding from the National Institutes of Health (U54 AI117804), Patient-Centered Outcomes Research Institute, American Part-
nership for Eosinophilic Disorders (APFED), American Academy of Allergy Asthma and Immunology and Nutricia; clinical trial funding from Regeneron, Shire, and Allakos;
consulting fees from Shire, Allakos, and Adare; and lecture fees from Danone and the Annenberg Center for Health Sciences at Eisenhower and serves (no fees) on the medical
advisory board for APFED, Campaign Urging Research for Eosinophilic Disease, and the International Food ProteineInduced Enterocolitis Syndrome Association. Dr Meyer
received lecture fees from Mead Johnson, Danone and Nestle. Ms Beauregard received consulting fees from Nutricia North America and Nestle Health Sciences and
serves on the medical advisory board for the Food ProteineInduced Enterocolitis Syndrome Foundation.
https://doi.org/10.1016/j.anai.2019.03.020
1081-1206/Ó 2019 American College of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.
604 M. Chehade et al. / Ann Allergy Asthma Immunol 122 (2019) 603e609
concern with eating needs to be done in the context of the family unit, with coaching provided to the caregiver
as necessary while ensuring nutritional adequacy. Treatment approaches, including division of responsibility,
food chaining, and sequential oral sensory, are commonly described in the context of feeding difficulties.
Conclusion: A multidisciplinary approach to management of feeding difficulties in noneIgE-mediated food
allergic gastrointestinal disorders is of paramount importance to ensure success.
Ó 2019 American College of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.
Table 1
Common Feeding Difficulties Resulting From Symptoms Caused by Each NoneIgE-Mediated Food Allergic Gastrointestinal Disorder
NoneIgE-mediated food allergic Symptoms associated with the development of feeding Common presenting feeding difficulty
gastrointestinal disorder difficulties
EoE Vomiting, abdominal pain, dysphagia, early satiety, faltering Fear of eating (ie, fear of swallowing or food stuck in the
growth esophagus, possible pain with eating)
Selective eating (ie, selective about textures)
Limited appetite and food refusal (ie, consume small
amounts)
EGIDs besides EoE Vomiting, abdominal pain, diarrhea Fear of eating (ie, fear of abdominal pain and discomfort)
Selective eating (ie, selective about texture)
Limited appetite (ie, attributable to dysmotility that affects
appetite and satiety)
FPIES Acute vomiting, shock Fear of eating (ie, concern of further reactions)
Selective eating (ie, limiting variety of food because of fear
of new reactions)
FPIP Blood in the stool Parental fear of feeding
Food proteineinduced allergic Vomiting, diarrhea, constipation,b faltering growth Fear of feeding
dysmotility disordersa Selective intake
Limited appetite
Abbreviations: EGIDs, eosinophilic gastrointestinal disorders; EoE, eosinophilic esophagitis; FPIES, food proteineinduced enterocolitis syndrome, FPIP, food proteineinduced
proctocolitis.
a
This includes dysmotility conditions that can be food protein induced, including gastroesophageal reflux disease2 and constipation.3,4
b
Should only be considered in food allergy if associated with other atopic symptoms and if standard dietary and medical management is not effective.
M. Chehade et al. / Ann Allergy Asthma Immunol 122 (2019) 603e609 605
mouth for a spoon, use their tongue to move the food bolus to the of this process caused by symptoms related to the noneIgE-medi-
back of their mouth to swallow it, and keep the food in their mouth. ated GI disease, or by the dietary interventions, can create feeding
Oral function progresses to a bite-and-release pattern at 5 to 6 difficulties.25
months of age. By 7 months of age, they can close their lip on the Levy et al26 established common triggers for feeding difficulties
spoon and use their upper lip to clear the spoon, and most can in children, including size (faltering growth), transitioning (puree
remove food from the spoon with their lips by 12 months of age. to lumpier textures), organic disease (including GI disorders),
Sustained biting and the beginning of rotary chewing are typically mechanistic feeding (ignoring absent hunger cues), and post-
seen at 9 to 12 months of age. If all goes well, a child will progress traumatic event (traumatic event around feeding, including
with food textures from purees to ground or mashed and then choking and violent vomiting). In noneIgE-mediated food allergic
chopped table foods. At 7 to 8 months of age, most infants can grasp GI disorders, most of these triggers are present in the well-
food with their hands and begin self-feeding. Although most infants documented symptoms (Table 1). Faltering growth is a common
can hold food in their hand and have begun trying to hold a spoon at presenting symptom, with low weight and in particular low height
8 months of age, most can feed themselves with a spoon without found in approximately 10% of children with this diagnosis.27 Poor
much spilling by 19 to 24 months of age. Between 8 and 12 months, growth often leads to heightened parental anxiety around feeding
children can bite crunchier foods as their teeth erupt, and by 15 as well as a mechanistic feeding pattern, with hunger and satiety
months of age most children have the ability to chew food. As ignored to enable more food intake.28 NoneIgE-mediated allergic
chewing continues to mature, most show interest in a large variety GI symptoms, including gastroesophageal reflux, abdominal pain,
of textures without gagging.17,18 Those offered more solid textures at and constipation, are also associated with feeding difficulties.29,30
6 months of age have better chewing skills by 12 months of age.17 In Of these difficulties, frequent vomiting has been best described as
addition, they are more accepting of, and are able to adequately having a negative impact, in particular on children with EoE.30e32
chew, most table foods by 2 years of age.17 There seems to be a critical Constipation and abdominal pain in noneIgE-mediated GI al-
period when infants are most receptive to different food textures. lergies have also been associated with feeding difficulties.29 It is
Infants who were introduced to lumpy foods after 9 months of age hypothesized that through visceral hypersensitivity that affects
have been observed to demonstrate a highly selective pattern and visceral pain pathways, sensory perception is affected, as was the
exhibited more feeding problems by 7 years of age.19 case in other pediatric chronic diseases that led to feeding diffi-
Not only is the oral-motor system progressive and critical, but culties.33 Chronic pain or discomfort also affects the willingness to
oral sensory development also follows very specific temporal mile- eat and explore new foods, affecting the development of oral-motor
stones. The extent to which food flavors are liked or disliked is skills and sensory perception of food.34 NoneIgE-mediated allergic
determined by innate factors, nutritional interventions, and GI conditions can also affect motility,35 which in turn may alter
learning.20 Infants get exposed to a variety of food flavors that their appetite and satiety, which then feeds into compensatory feeding.
mothers ingest via amniotic fluid, and if they are breastfed, via breast Finally, events such as violent vomiting in acute FPIES or dysphagia
milk. These exposures influence their flavor preferences shortly after and esophageal food impactions in EoE can be traumatic for parents
birth and at weaning.20 These varied sensory experiences with food as well as the child. Once triggers have been identified, it is useful to
flavors help explain why breastfed infants are more willing to try be able to classify the feeding difficulty according to the universal
new foods.21 In nonbreastfed children with food allergy, hypoaller- classification by Kerzner et al,36 which includes children with
genic formulas are required, and data indicate that infants younger limited appetite, those with selective intake, and children with a
than 2 months have willingness to drink a bitter and sour protein fear of feeding (Table 2).
hydrolysate formula, whereas 7- to 8-month-old infants rejected Not only can symptoms be associated with feeding difficulties,
it.22 The experiences with the formula flavor affected their prefer- but also overly restricted dietary therapies implemented for many
ences for food taste qualities later on during weaning.23 Infants of the noneIgE-mediated diseases during critical phases of feeding
feeding protein hydrolysate formulas, which are typically bitter and developmental progression can lead to a limited range of textures
sour, preferred savory, bitter, and sour cereals much more than those and flavor exposure. This in turn can lead to an arrest in the
fed intact cow’s milkebased formulas.23 These flavor preferences development of proper oral-motor and sensory functions.32
were present even at 11.5 years of age.24 In addition, the behavioral aspects of feeding should be
remembered. Rommel et al30 found that medical and oral-motor
causes are mainly to blame for feeding difficulties at younger
Where and When Feeding and Eating Could Go Wrong
than 2 years, and above that age, feeding behavior is a more com-
Feeding skills, including oral-motor, sensory, behavioral or mon problem. In noneIgE-mediated GI allergies, dietary avoidance
emotional, and communication skills, develop early, and disruption is the mainstay for management, which entails careful product
Table 2
Types of Feeding Difficulty With Suggested Corresponding Therapeutic Strategies
selection and food preparation. Children also learn to eat through may refuse to eat their favorite foods if they are on the same plate as
parental modeling. Therefore, essential allergen-free product se- unfamiliar foods. Some children may begin to gag the moment they
lection and reluctance to introduce new foods because of fear of a see or smell food.15,40 Children become more accepting of new food
reaction can easily be adopted by children who then become very if they are around adults that enjoy eating a wide variety of foods,
selective in their intake.37 Food neophobia (fear of trying a new including unfamiliar foods.
food) is a normal occurrence in early childhood when a child wants Children with noneIgE-mediated food allergic GI disorders are
to be independent, which can have a further negative effect on at particular risk for developing feeding difficulties because of their
feeding.38,39 negative experiences with food. Determining when a practitioner
should refer a family for further assessment of a feeding difficulty
presents a challenge. As described above, feeding a healthy child
Diagnostic Approach for Feeding Difficulties can be a challenge during different developmental stages as chil-
Picky eating should be differentiated from a pathological prob- dren learn how to express their own opinions and set their own
lem. Parents or caregivers often report that their children are boundaries around what foods they put into their mouths. Children
“picky” some or most of the time. Toddlers may eat less than before. often have periods when they would prefer to eat only a limited
They are opinionated, skeptical, and erratic when they eat; they are number of foods, which is sometimes referred to as a food jag.
fickle, cautious, messy, and picky. Some days, they would rather Feeding difficulties may also be transient. Signs and symptoms36
play than eat. Toddlers have a lot to learn about food and how to that may indicate that a child is experiencing something other
eat. Preschoolers are often less skeptical about new food and should than a typical or transient feeding issue include the following:
be more willing to try it. They often wiggle and squirm when they
sit at the table and cannot be fooled by hiding vegetables in foods. Falling off of the growth curve (further evaluation needed to
During the school-age years, children want to practice grown-up ensure that growth was properly assessed)
skills, and they grow more confident in their ability to feed them- List of preferred foods becomes shorter and shorter
selves. They will often use utensils but may still use their fingers Child begins to exhibit fear or anxiety around new foods
from time to time. The list of foods they are willing to eat on a A child who was once well behaved at the table now may cry or
regular basis is getting longer. Adolescents can be described as even refuse to come to the table
toddlers with attitude and can be just as erratic as toddlers with A child becomes very rigid in the way in which food needs to be
their mood. The physical changes that occur in adolescents may prepared or insists on only eating the same brand of food
make them self-conscious, and their appetites can increase notably.
Food choices may change based on many factors, including peer Figure 1 outlines these factors and provides a guide for the
pressure or environmental effect.40 practitioner on when to refer for feeding difficulties.
Picky eaters may behave well most of the time during meals and
may eat 1 or 2 foods on their plate and ignore the others. They may
Management of Feeding Difficulties
touch or otherwise play with their food, but in general they are not
afraid of it; they simply may not be prepared to put it in their Feeding difficulties cannot be viewed as just the child’s problem.
mouths. Fussy or problematic eaters may behave poorly at the ta- Successful management requires that the health care team views
ble. They may become very upset at the sight of any new foods on this as a relational disorder between the child and the parent or
their plate. Fussy eaters may cry, throw their plate, or refuse to caregiver.40 Addressing the child’s concerns with food and eating
come to the table if the food reaches the table before they do. They must be done in the context of the family unit and may require the
Red flags
Referral needed
Pediatric Gastroenterologist
Allergist
No referral needed if
Registered dietitian Child follows their growth curve
Speech language pathologist Food repertoire broadens
Occupational therapist No changes in behavior around
Behavioral therapist food
Figure 1. Proposed algorithm to guide practitioners on when to refer for feeding difficulties.
a
Persistent feeding difficulty is defined as a feeding issue in which the child becomes more selective or restricted, growth may become compromised, and there are high levels
of stress around eating in the home.
b
Transient feeding difficulty is defined as a change in the child’s eating pattern that lasts a short period and therefore does not threaten nutritional status and the child is able to
bring himself/herself along to a wider eating pattern with proper support from parents.
M. Chehade et al. / Ann Allergy Asthma Immunol 122 (2019) 603e609 607
parent or caregiver to get significant coaching in how to feed the Division of Responsibility Approach
child.36 The parent or caregiver may also need counseling to help
Satter’s Division of Responsibility (sDOR) is an effective man-
them address any underlying anxiety that may be preventing them
agement strategy that can help address the parent/caregiver
from offering a wider variety of safe foods.
feeding style as well as the child’s eating style.40 sDOR states that
Four different types of caregiver feeding styles have been
the parent/caregiver’s job is to determine when food is served,
described36,40: responsive or authoritative, neglectful, controlling
what food is served, and where it is served. The child’s job is to
or authoritarian, and indulgent or permissive. The responsive or
determine if he/she will eat the food that is being served and how
authoritative feeder follows a division of responsibility in which
much. As long as the parent/caregiver does his/her job with feeding
the feeder decides what, where, and when food is offered and
and allows the child to do his/her job with eating, the child will eat
lets the child determine if and how much they are going to eat.
the amount of food that is right for them.
The neglectful feeder may fail to offer food at regular times and
The parent/caregiver who follows sDOR does not use pressure
to set limits as to what food is offered and when, and may offer
language (offering bribes or threatening punishment) and does not
developmentally inappropriate foods. They may not sit with their
come to the table with an agenda to get the child to eat. The adult
child during meal or snack times and if they do, may not make
offers an organized, pleasant meal or snack time experience with
eye contact or engage in conversation. The controlling or
flavors and textures that are developmentally appropriate for the
authoritarian feeder often decides how much food the child
child he/she is feeding. This parent/caregiver is considerate by of-
should eat, ignores the child’s own hunger and satiety cues, and
fering foods that the child likes but does not cater to the child’s
may use rewards or punishment to get the child to eat. The
every demand for food. These parents/caregivers also understand
indulgent feeder completely caters to the child and may provide
that children may eat quite a lot at one meal and not very much at
very little structure with meal and snack times. They will offer
the next. They are also comfortable knowing that if the child does
whatever food the child demands and may make separate food
not prefer the foods served during the meal, the child will have an
for each child at the table.36,40
opportunity to eat at the next snack time.
The parent/caregiver plays a critical role in helping a child
The core of sDOR is trust. Eating and feeding is successful when
overcome feeding difficulties. Determining the parent/caregiver’s
there is mutual trust and respect around the table. The parent/
feeding style will help the health care team in offering the re-
caregiver must trust the child’s instincts on what food is safe and
sources and training needed that will allow the parent/caregiver to
that the child will eat the amount of food that is right for them. The
help the child make progress. The health care team also needs to
child must be able to trust that safe foods are going to be offered on
emphasize to parents/caregivers that eating is a skill that children
a regular basis and that they will be allowed to explore new foods in
learn at their own pace and they must be supported at their pace
a way that makes them feel comfortable and safe.40
and not pressured to eat larger quantities or a greater variety of
flavors or textures. Food Chaining Approach
In addition to the feeding style, parental/caregiver anxiety about
feeding the child should also be assessed. Negative experiences The food chaining method is a systematic approach for the
with food may not only be traumatic for children but also the adults treatment of children with selective food intake. This approach was
who witness the event. Children may be ready to expand their food first described by Fraker and Walbert42 in 2003 and uses an indi-
choices long before the parent feels comfortable doing so. Studies vidualized, nonthreatening, home-based feeding program that al-
report that parents of food allergic children have increased levels of lows for the expansion of foods, using new foods with similar
anxiety and poorer quality of life; therefore, parental anxiety rather sensory characteristics to accepted foods, including texture, color,
than the organic disease present in the child may at times drive the and temperature. An example is provided in Figure 3. This method
feeding difficulty.41 was subsequently studied in a small cohort of 10 children with
extremely limited food intake; all children managed to expand
their diet significantly after 3 months.43
Therapy Strategies and Methods of Managing Children With There is paucity of data using this technique in children with
NoneIgE-Mediated Food Allergic GI Disorders noneIgE-mediated food allergic GI disorders, although it is
Although several methods have been described for managing commonly used in practice. Further studies are needed to establish
feeding difficulties, limited data have been published on strategies its effectiveness.
specifically for children with noneIgE-mediated GI food allergies.
Sequential Oral Sensory Approach
Health care professionals working in this area have, however,
implemented many interventions in their patient cohort, with The sequential oral sensory approach has several overlapping
perceived positive results that should be evaluated in future features with the food chaining approach in addressing sensory
studies. These methods are described in further details below, and feeding problems. However, there are some significant differences.
their uses in specific feeding difficulties are summarized in Table 2. The original program developed by Toomey and Ross44 suggests a
A number of overarching strategies can be used in any child with
noneIgE-mediated GI food allergy (Fig. 2) and can be combined
with any of the methods below. A child that only will eat French fries and potato crisps:
- Sensory characteristic: crispy and beige
Food chaining step 1: Offer chicken nuggets/potato waffle fries (both are crispy and
beige but different shape and different taste)
1. Keep mealtimes ideally below 30 minutes Food chaining step 2 : Keep the potato waffle fries and chicken nuggets but add a
2. Avoid distraction, including electronic tablet, television, video games sauce to dip in – for example, cheese sauce (if cheese is tolerated), hummus, or
3. Keep the mealtime environment as relaxed and neutral as possible mayonnaise – the color remains the same, but the texture changes with the sauce.
4. Serve age appropriate portions
5. Encourage self-feeding Food chaining step 3: Offer slices of white meat from the chicken (no skin) with gravy
6. Encourage mess and food exploration (mixed texture)
7. Repeat foods that have been refused up to 15 times
Figure 3. Example of the food chaining approach in managing a child with feeding
Figure 2. General management strategy for management of feeding difficulties. difficulties.
608 M. Chehade et al. / Ann Allergy Asthma Immunol 122 (2019) 603e609
Table 3
Multidisciplinary Team Members That May Be Involved in the Management of Feeding Difficulties in NoneIgE-Mediated Gastrointestinal Allergies
Specialist Benefit
12-week program that is based on 4 tenets: myths about eating, faltering growth. Given the paucity of data on feeding difficulties
systematic desensitization, normal development of feeding and food in noneIgE-mediated food allergic GI disorders, more research
choices, and how these are linked together. This biopsychosocial studies are needed to help determine the extent to which
therapy method uses a multidisciplinary approach that integrates severity of symptoms, extent of dietary restrictions, and parental
posture (not addressed in food chaining), sensory, motor, behavioral perception of the specific food allergic GI disease contribute to
(not addressed in food chaining), and medical and nutritional factors the development of this condition. Addressing feeding diffi-
in therapy sessions that are not home based (unlike food chaining). culties through a multidisciplinary approach will ensure that we
Limited data exist on its efficacy, which has been its main criticism. create a healthy and thriving pediatric population despite their
However, a small number of studies exist in patients with autism, GI allergies.
neurologic impairment, and cerebral palsy.45,46 These studies have
found that overall the SOS approach had a positive effect on feeding,
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