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Clinical Nutrition
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Review
a r t i c l e i n f o s u m m a r y
Article history: Non-Organic Feeding Disorders (NOFEDs) are frequently encountered in children younger than 6 years
Received 12 March 2014 old. NOFED are characterized by feeding aversion, failure to advance to age-appropriate foods, food
Accepted 29 August 2014 selectivity and negative mealtime behaviors. Parents of children with feeding disorders often use
abnormal feeding behaviors, such as intrusive feeding. Persistent inadequate caloric intake leads to non-
Keywords: organic failure to thrive in up to 40e50% of cases. Managing children with NOFED is a challenge for even
Feeding disorders
the most experienced pediatric specialists. Management by a multidisciplinary team, as outpatient or
Failure to thrive
inpatient should address both nutritional support and feeding behavior modification. Even in the
Nutrition care plan
Aversive feeding behaviors
absence of failure to thrive, children with behavioral feeding problems are at risk of negative health,
social and emotional outcomes, including nutrient deficiencies, social and family disruption or conflict.
The aims of the current review are to present an update of the definition, classification, etiology,
epidemiology of NOFED, as well as clinical presentation, evaluation and management of this condition
and non-organic failure to thrive, often associated with NOFED.
© 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
1. Introduction introduced to lumpier textures earlier [4]. In theory, any child has the
potential to develop feeding deviations. In fact, patterns and behaviors
Successful feeding has been acknowledged as a notable develop- around mealtimes and eating have been identified in normally
mental milestone for infants. Variation in bolus type (liquid or solid), developing children. Feeding difficulties, such as selective eating, food
characteristics (hardness, homogeneity, volume, viscosity, texture, refusal, exceedingly slow eating, and tantrums, are common among
moisture content), and other sensory particularities (taste) serve to young children. Some children, however, fail to develop the skills
modulate the timing and pattern of motor components which necessary to manage the new feeding demands. Lengthy mealtimes,
constitute the overall feed sequence [1]. Following breastfeeding (or pocketing food, and tantrums at mealtimes are typical negative be-
formula feeding), complementary/solid food feeding constitutes the haviors of dysfunctional feeding.
next major feeding stage in an infant's life. Developmental readiness The aims of the current review are to present an update of the
for solid foods feeding varies considerably among infants. In most definition, classification, etiology, epidemiology of non-organic
babies, the developmental skills (chewing and swallowing soft, solid feeding disorders (NOFED), as well as clinical presentation, evalu-
foods) needed to begin complementary foods are present between 4 ation and management of this condition and non-organic failure to
and 6 months of age. Oral motor control and reduction in sensitivity to thrive, often associated with NOFED. We carried out a systematic
touch within the mouth and lips are necessary to manage and accept search through MEDLINE via PubMed (http://www.ncbi.nlm.nih.
solid foods [2]. In fact it may be important that an infant is allowed the gov/pubmed/) to identify all the articles published in English up
opportunity to use their oral skills as soon as they develop [3]. Studies to date based on the following keywords “feeding disorders” or “
have demonstrated that infants exposed to textures after nine months failure to thrive”.
of age were more likely to have feeding difficulties and be seen by their
parents as fussy eaters compared with children who had been 2. Non- organic feeding disorders, definition, classification,
epidemiology and risk factors
* Corresponding author. Pediatric Department, University of Messina, Via Con-
solare Valeria, 98125 Messina, Italy. Tel.: þ39 90 2212918; fax: þ39 90 2213788. Non-organic feeding disorders (NOFEDs) is a formal diagnostic
E-mail address: romanoc@unime.it (C. Romano). term used to indicate a condition in children who show deviating
http://dx.doi.org/10.1016/j.clnu.2014.08.013
0261-5614/© 2014 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
196 C. Romano et al. / Clinical Nutrition 34 (2015) 195e200
feeding behaviors as food refusal, aversion to feeding, selective retardation and prematurity occurred more often in children aged
eating and low food intake without organic disease. In 1994, the less than 2 years with feeding disorders [11]. The most serious
American Psychiatric Association (APA) added “Feeding Disorder of complication of NOFED is failure to thrive (FTT). Non-organic failure
Infancy and Early Childhood” to the Diagnostic and Statistical to thrive (NOFTT) describes infants with growth faltering secondary
Manual of Mental Disorders (DSM-IV) [5]. The ICD-10 Classification to poor caloric intake in the absence of organic disease or any
of Behavioral and Mental Disorders also has a broad category called demonstrable abnormalities of swallowing mechanisms [12].
“feeding disorder of infancy and childhood”, which includes Generally, linear growth and head circumference are either not
rumination. In the last revision of the “Diagnostic Classification of affected, or are affected to a lesser degree than weight. More exact
Mental Health and Developmental Disorders of Infancy and Early definitions, based upon precise weight percentile, rate of weight
Childhood-Revised”, DC:0-3R, Zero-to-Three, a diagnostic system, gain or weight loss, or changes in other parameters exist, but are no
which classifies psychopathological pictures in the first years of life, more useful than the above definition [13]. In routine clinical
has introduced a classification of ‘’Feeding Behavior Disorder’’ practice, FTT is commonly defined as either a weight for age that
which includes three different diagnostic subtypes of FD [6]. Table 1 falls below the 5th percentile on multiple occasions or as weight
presents the classification and subtypes of NOFED. About 20e60% deceleration that crosses two major percentile lines on a growth
of parents report that their children are not eating optimally, that chart [14]. Growth variations in normal infants can confound the
they are picky, have food phobia, eat too little and have inappro- diagnosis of FTT as 25% of children change their weight or height by
priate weight gain [7]. Approximately 25% of normally developing more than 25 percentile points in the first two years of life. Within
children experience feeding problems, with 1e2% suffering from this group lie four main patterns: a) infants who have small parents
severe feeding difficulties [8]. Feeding disorders are in most cases and are growing to their genetic potential, b) infants with consti-
transient, but in 3e10% become persistent and carries the risk of tutional delay in growth, c) infants born prematurely who are
inadequate growth. The prevalence of parent-reported feeding growing below their age matched peers, and c) infants with post-
problems in children with neurological disabilities and chronic natal ‘catch down’ growth. Traditionally, FTT has been dichoto-
medical conditions is estimated at around 40e70% and even higher mized into two mutually exclusive categories based on the
in children with autistic spectrum disorders [9,10]. Other high-risk presumed etiology. Population and hospital based studies found
groups include infants of premature birth, children with craniofa- substantial organic disease in only 5e10% of children with slow
cial anomalies, and those with certain genetic syndromes. Rommel weight gain [15,16]. A number of authors have questioned the
N. et al. showed that lower length of gestation, intrauterine growth utility of a dichotomus classification for FTT. Homer and Ludwig S,
therefore, suggested that FTT is best described using three etiologic
categories: a) organic, b) nonorganic, and c) mixed (i.e., with both
Table 1 physical and psychosocial components) [16]. Such a partition
Classification. adequately accounts for the interactive influences of organic dis-
Classification Category Subtype ease and psychosocial variables on infant weight gain and
acknowledge the continuous, rather than dichotomous, nature of
DSM-IV Feeding disorder of Pica
infancy or early Rumination disorder FTT. In the United States, FTT is seen in 5e10 percent of children in
childhood primary care settings and accounts for 1e5% of pediatric hospital
DC:0-3R Eating behavior Infantile anorexia admission for children younger than 2 years [17]. However, up to
disorder Feeding disorders associated with 15e20% of hospitalized children younger than 2 years from a
insults to the gastrointestinal tract
Sensory food aversion
medically ward population met the criteria of FTT. Regardless of the
Chatoor I Feeding behavior Feeding disorder of state regulation etiology, inadequacy of nutrition and feeding difficulties are at the
disorders Feeding disorder of reciprocity heart of NOFTT [15]. Levy, et all identified five “triggers”, vulnerable
(previously “feeding disorder of conditions or children at risk of NOFTT: 1) infants with low birth
attachment”)
weight (premature, and small for-gestational age) which are often
Infantile anorexia
Sensory food aversions perceived by parents or the medical team to be too small, leading to
Feeding disorder associated with persistent attempts to feed the infant beyond the infant's hunger
concurrent medical condition cues, 2) traumatic events during feeding transition time, 3) organic
Posttraumatic feeding disorder conditions that cause decreased hunger or painful feeding and food
Crist and Complex Picky eaters
Napier-Phillips biobehavioral Toddler refusal e general
refusal, which lead to intrusive or persecutory feeding and subse-
pediatric feeding Toddler refusal e textures quent food refusal, even if the initial disease has been resolved, 4)
disorders Older children refusal e general mechanistic feeding which ignores child's hunger cues, and 5)
Stallers posttraumatic causes [18].
Burklow et al. Behavioral Structural abnormalities
Observational studies have shown that feeding difficulties such
pediatric feeding Neurologic conditions
problems Behavioral and psychosocial as low appetite, weak suck, and weaning difficulties are associated
problems with weight faltering [19e21]. The presence of oral-motor
Cardiorespiratory problems dysfunction (OMD) may prevent some children from achieving a
Metabolic dysfunction satisfactory nutritional intake due to prolonged mealtimes and
Dovey TM etal Food refusal Learning dependent food refusal
behaviors Medical complications related food
inappropriate parental responses [22]. Approximately half of the 4
refusal year olds with chronic growth retardation studied by Heptinstall
Selective food refusal et al. had some disorder of OMD and had begun to fail to thrive in
Fear based food refusal the first year of life [23]. Ramsey et al. evaluated 38 infants with
Appetite awareness and autonomy
NOFTT and 22 with organic FTT. The histories of the children with
based food refusal.
Kezner B Feeding difficulties Limited appetite so-called NOFTT were suggestive of an oral-sensor-motor impair-
Highly selective intake ment reported to be present from birth or early infancy [24]. Using
Crying interfering with feeding an assessment schedule previously shown to be both reliable and
(Colic) valid, Reilly SM et al., showed in a population-based study that a
Fear with feeding
substantial number of children previously described as having
C. Romano et al. / Clinical Nutrition 34 (2015) 195e200 197
NOFTT, in fact, have significant OMD [25]. Abnormal feeding lymphoadenopathy, abnormal genitalia and neurological findings
behavior is sometimes caused or follows conditions that lead to a [42]. Growth history should be reviewed by careful plotting of past
painful or challenging feeding [26] NOFED associated with feeding growth points on specific curves, and interpreted in the context of
disorders usually manifest as refusal to feed or low food intake. the family's growth history and pattern. For premature born infants
Other symptoms such as vomiting, gagging or retching, irritability, adjust for prematurity up to age of 2 years. A detailed medical
or apparent difficulty in swallowing, are sometimes present, thus assessment should include family, social, feeding, past and current
mimicking many of the previously mentioned organic conditions. medical histories and a complete physical examination (Table 2).
Berlin et al. revised the medical records of 286 children (mean age Panetta et al. investigated the predictive value of predefined
35e56 months) seen at an outpatient feeding disorders clinic. The symptoms and signs for the diagnosis of NOFTT in a group of 208
review generated 3 co-morbidity patterns: “Behavioral” (58% of children (6 monthse14 years old) with FTT, defined as wasting
cases), “Developmentally Delayed” (37%), and “Autism Spectrum (ideal weight for height <85%) [43]. Multivariate logistic regression
Disorder” (ASD, 5%). Multiple co-occurring conditions of children showed that among the six variables, linked to the outcome at a
with feeding problems suggests that medical and developmental 95% significance level, vomiting (OR ¼ 0.31; 95% CI ¼ 0.13e0.72)
conditions confer general, rather than specific, risk for feeding and abdominal distension (OR ¼ 0.34; 95% CI ¼ 0.13e0.90) were
problems in children [27]. Large cohort studies found variable as- predictive of OFTT diagnosis, while vivacity (OR ¼ 5.18; 95%
sociations between FTT and maternal depression: either no link or a CI ¼ 1.71e15.70) and food restriction and/or feeding rituals
temporary association that disappeared by 12 months [28e34]. (OR ¼ 2.78; 95% CI ¼ 1.13e6.84) characterize NOFTT. Detection of at
Furthermore, social isolation, beliefs and low self-esteem are least one nonorganic symptom or sign with the exclusion of any
associated with reported FD [35e40]. In recent years studies in organic symptom had 90% positive predictive value in the whole
unselected populations have found little evidence of a link between group and 96% in patients aged less than 36 months for NOFTT.
slow weight gain/FTT and maternal disorder. However, two obser- There is no formal evidence to suggest an ideal routine set of in-
vational caseecontrol studies found associated differences in vestigations, but Table 3 shows a suggested schedule of tests to rule
maternal feeding behavior/responsiveness and poor weight gain out possible occult pathology. An exhaustive number of in-
[28,33]. For example, infants with weight faltering had significantly vestigations are often ordered in children with NOFTT of which only
fewer positive interactions (where parents anticipate and support a a small minority contribute to the diagnosis of an organic cause in
child's needs) during meals than controls. Chatoor and her col- FTT. Sills RH et al. found that, in 185 children less than 3 years old,
leagues proposed that the conflictual interactions between admitted for evaluation of FTT, only 36 out of 2.607 laboratory tests
mothers and children with FD are a result of particular child and performed (1.4%) were helpful in making a diagnosis, and all of
mother characteristics [38]. Specifically, when children refuse to these 36 positive results were suspected on clinical grounds [44].
eat, vulnerable mothers may become anxious and insecure and try Clinical evaluation ought to include observation of the infant and
to forcefully feed their children with the creation of a vicious cycle caretaker while feeding and playing. This provides clues about their
[39]. Thus, the quality of parenteinfant interactions as measured by interactions, the caretaker's feeding technique and response to the
mother and newborn feeding behaviors have been shown to pre- infant's physiologic or social cues. The physician should be able to
dict infant growth velocity during the first month of life [39,40]. identify abnormal parental feeding practice or intrusive feeding
Observations of mother-infant/toddler relationships during meal- (nocturnal feeding, persecutory feeding, forced feeding, conditional
times and non feeding interactions should be an integral compo- distraction, and prolonged meals) and possible triggers [45].
nent of an evaluation of NOFED because they provide valuable Trigger is defined as an identified external event or etiology, leading
information about feeding problems associated with poor weight to food refusal and NOFEDs. On the basis of clinical experience, Levy
gain and offer specific behavioral targets for intervention [41]. et al. [18] have distinguished five categories of triggers for NOFEDs
as e Size, Transitional feeding, Organic cause, Mechanistic feeding,
3. Evaluation of children with NOFED and NOFTT
(29.2%), day treatment programs (16.7%), outpatient clinics (10.4%), more advanced, invasive procedures when a medical condition is
and residential facilities (6.3%). A significant proportion of children suspected. In children with established NOFED, behavior modifi-
with tube (69.7%) and bottle dependence (87%) were treated at cation intervention plan constructed and supervised by the clinical
inpatient or day treatment facilities. In contrast, no significant psychology specialist, remains at the core of management of chil-
difference in treatment setting was detected for children treated for dren with NOFED and is usually accessible only in the outpatient/
food selectivity [52]. inpatient setting.
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