Why might children with pediatric intestinal failure be less interested in eating?

The paper by Pires et al.1 in this issue of Nutrition in Clinical Practice contributes to the limited literature about feeding challenges in pediatric intestinal failure (PIF). It is the first study to compare eating behaviors in those still dependent on parenteral nutrition (PN) with those who achieved enteral autonomy (EA). This study prompts the question: why might children with PIF be less interested in eating? The development of eating behavior is complex, especially for children whose eating progression has been disrupted. Eating behavior represents an interplay of physiologic, psychologic, social, and genetic factors that influence food preferences, as well as the selection, quantity, and timing of food intake.2 Eating-related pleasure has a central role in the development of eating habits in the first 2 years of life,3 and the enjoyment of food is an important psychosocial aspect of quality of life.4 Understanding eating behaviors is important in this population, as children with PIF may be difficult to feed.5 Recent data suggest that feeding difficulties may be prevalent in PIF,6, 7 and that children with PIF may have delays in acquiring feeding skills.6 There is a unique paradigm of risk factors for feeding difficulties in PIF.8 The European Society for Pediatric Gastroenterology, Hepatology, and Nutrition has recently recognized that oral aversion is an important complication of short bowel syndrome that should be prevented.9 Thus, there is value in understanding both disordered eating behaviors and interest in food in this population. The study by Pires et al. was conducted in southern Brazil with a PIF population under the care of a multidisciplinary intestinal rehabilitation team that included support from a speech and language pathologist. Their standard care included an oral feeding training protocol. The researchers compared those receiving PN with those who had achieved EA using two feeding assessment tools: the child eating behavior questionnaire (CEBQ)10 and an oral feeding assessment using the American Speech-Language-Hearing Association National Outcomes Measurement System (ASHA-NOMS).11 Among children receiving PN, approximately half required modified feeding techniques (altered solid food consistency and/or tube feeds) but only 11% received tube feeds alone, 26% received tube feeds and oral feeds, and 63% received oral feeds alone. All those who had achieved EA were fully orally fed and did not need any dietary modifications. The center's practice to promote oral feeds may have contributed to the impressive observation of full oral age-appropriate feeding in all those who had achieved EA. The time interval between achieving EA and being fully orally fed or the time of being autonomous before study participation is not known and would further our understanding of the course to full oral feeds. As the authors note, this is the first PIF study published to use the ASHA-NOMS tool, a systematic classification of feeding stage that emphasizes dysphagia, feeding safety, and the need for modified feeding strategies. In the absence of a neuromotor condition, in PIF, the main driver of feeding progression is enteral tolerance. There are times when feeding or feeding progression is just not possible. The “safety” considerations are usually less about swallowing, and “risk” is more related to worsening enteral tolerance or surgical considerations. This study highlights that there may be benefit to a PIF-specific classification tool in which the oral feeding stage classification goes beyond dysphagia, the need for modified feeding strategies and qualifies if the progression of oral feeds is limited by surgical risk status, enteral tolerance, and/or difficult feeding behaviors. According to the CEBQ tool, those children receiving PN had higher satiety responsiveness (perceived fullness) and lower enjoyment of food and food responsiveness compared with those who had achieved EA. The pattern was more marked in those with a higher degree of PN dependence as measured by the PN dependency index.12 Those with a mild degree of PN dependence had lower food fussiness scores than those with a moderate or severe degree of PN dependence. The authors propose that the PN dependency index may relate to eating behavior in PIF. The reasons for food avoidance and decreased in food interest in PIF merits reflection. Firstly, the disease-related gastrointestinal symptomatology can cause a chronic negative effect on oral sensory experience and contribute to appetite dysregulation, the disruption of feeding and feeding skills development.8 It is noteworthy that the time on PN for the EA group was significantly shorter than that of the group currently receiving PN. It was acknowledged that the eating behavior differences between the groups may reflect a difference in disease severity between the groups. Nutrition support may impact appetite. In clinical practice, it is observed that PN may suppress appetite, although the study of this is limited. Some studies suggest that PN may decrease oral intake,13-15 and other adult studies have found that hunger is not reduced.16 The impact of enteral nutrition on oral feeding is more evident. The use of enteral tube feeds will suppress appetite and may interfere with the child's learning experience about hunger and satiety cues and progression of achieving feeding milestones.17 In this study, there was no difference between those with PIF receiving PN and those with EA in the other avoidant feeding behaviors of slowness in eating, food fussiness, and emotional undereating. However, our group observed that in a Canadian PIF cohort in which tube feeds were routinely used, there were higher scores for the CEBQ avoidant feeding behaviors of satiety responsiveness, food fussiness, slowness in eating, and lower enjoyment of food compared with the scores of healthy children.6 In contrast, in the French cohort reported in the same manuscript for whom oral feeds were promoted, there was no difference in these food avoidance behaviors or in the enjoyment of food. There was less emotional undereating compared with healthy children.6 This suggested that a center's approach to feeding in PIF, including the use of enteral tube feeds, likely impacts food avoidance and interest in food. Finally, the presence of an eating disorder may be the reason for poor interest in food. Features of pediatric eating disorders include avoidant eating behaviors, eating skills delay, and a disruption in relationships or the social context around meals with a resultant impact on nutrition status. There are variety of descriptions that have been used to describe the feeding problems in PIF, each definition having limitations in this unique clinical context. The term “oral aversion” captures the sensory feeding refusal aspects in infants and toddlers; however, psychosocial and feeding skills dysfunction are not considered. The Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition definition for avoidant restrictive food intake disorder (ARFID) requires that the eating disturbance not be attributable to a concurrent medical condition and, if it occurs in the context of another condition, the severity of the eating disturbance exceeds that routinely associated with the condition.18 Mental health illness is often a comorbidity, and ARFID does not include a skills deficit. Furthermore, interpreting the degree of an eating disturbance “routinely” associated with PIF may be difficult to determine in practice. The more inclusive pediatric feeding disorder (PFD) definition includes criteria for medical, skills, and psychosocial dysfunction.19 Of note, the PFD skills dysfunction criteria include the need for modification of food texture, feeding position, and equipment or feeding strategies. In PIF, the need for “equipment” would be an inappropriate criterion, as patients with PIF, by definition, are dependent on PN support. This dependence is driven primarily by the disease. Both ARFID and PFD include criteria for an impact on nutrition status or the dependence on enteral tube feeding or oral nutrition supplements. This makes these definitions difficult to apply in PIF, where dependence on enteral nutrition support may be iatrogenic20 and a reflection of feeding practice rather than a feeding disorder. Furthermore, the use of PN and enteral nutrition support in PIF can compensate for the potential observed impact of disordered eating on nutritional status or nutrient deficiency. In the context of PIF, the nutritional consequence is more related to difficulty in weaning nutrition support. We recently proposed a definition for pediatric intestinal failure-associated eating disorder (IFAED)8 adapted from the relevant features of PFD. This definition allows for and recognizes that the feeding difficulties encountered in PIF may be related to the complex aspects of the disease that impact feeding/eating. The criteria include feeding/eating skills dysfunction, psychosocial dysfunction, or impact on nutrition support. The definition assumes the absence of a cognitive process consistent with a body image distortion eating disorder, poor oral intake caused by food insecurity, a diagnosis beyond PIF that is responsible for the feeding problems, and a surgical procedure or an acute exacerbation of gastrointestinal symptoms challenging feeding tolerance. Table 1 summarizes the differences in the diagnostic criteria for ARFID, PFD, and IFAED. Screening for IFAED would include asking questions such as the following: (1) does the child have age-appropriate feeding/eating (eg, skills, food texture, and variety)? (2) does the parent find the child difficult to feed (eg, food avoidance or conflict around eating/food)? and (3) does the feeding/eating difficulty contribute to the need for enteral or PN support or difficulty in weaning nutrition support? This is the first definition to be proposed for the feeding challenges in PIF, and the further evolution to a consensus definition will be important for improving clinical awareness and screening for disordered eating in PIF. Furthermore, adopting a consensus definition will also allow us to better understand the impact of promoting oral feeds on disordered eating behaviors, quality of life indicators, management, and morbidity outcome measures. Patients with PIF are a unique population. The paper by Pires et al. prompts reflection on children's behaviors toward food. The optimized journey to EA includes developing competent eaters who enjoy food in the face of negative stimuli and learn to regulate their food intake according to symptoms. We need to better understand and respect why a child with PIF may not be interested in eating and how to promote their feeding skills development and enjoyment of food so that we can minimize pediatric IFAED. The author declares no conflict of interest.

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