Feeding disorders are common in young children (1,2). Of all of the children with congenital malformations, mental retardation, or complex early medical history, between 40% and 70% develop severe feeding problems (1,3). The causes of the feeding problems range from anatomic or functional orofacial and or chronic illness with food requirements exceeding the child's feeding ability, to food refusal due to phobia or aversion. Many of these children are dependent on tube feeding. Although this is an effective means to ensure that the child thrives and grows adequately, it also decreases the child's hunger-driven motivation to eat, reduces positive oral stimulation, and can contribute to oral aversion as a chronic noxious stimulus (4,5). A child who does not accept any foods orally is not able to make the link between eating and satisfying hunger. This interferes with the reintroduction of oral feeding and can result in behavioral problems and finally in pathological food refusal (PFR) (5,6).
Managing these feeding problems and especially weaning the child off tube feeding are major challenges for the parents and for all health workers involved, including dietitians, speech therapists, psychologists, nurses, and pediatricians. Studies aiming at weaning children off tube feeding are scarce; most are based on behavioral approaches, and the results vary (4,6–14). In the Netherlands, a hunger provocation program was developed and used with considerable success (15), but the results were not published in the medical literature.
In this study, we investigated whether children with complex feeding problems and PFR could be weaned off tube feeding with provocation of hunger as the motivation to resume oral feeding (16). The study was performed in the pediatric department of the Vrije Universiteit Medical Centre, a university-based tertiary care hospital. To our knowledge, this is the first time such a program has been described in the literature.
PATIENTS AND METHODS
Children were eligible for the hunger provocation program when they were younger than 2 years of age, had a history of PFR, and had been fully dependent on nasogastric tube feeding for at least 3 months. Exclusion criteria were the presence of anatomic, neurological, or functional conditions that could account for these feeding difficulties; the presence of a medical indication for tube feeding (eg, renal disease requiring adequate supply of fluids and electrolyte solutions); and lack of parental informed consent.
Diagnostic Evaluation Before Admission
Before admission, all of the children underwent evaluation by a multidisciplinary feeding team consisting of a pediatrician, pediatric gastroenterologist, nurse, dietitian, speech-language pathologist, and psychologist, regarding the patient's history, physical examination results, eating behavior, oral aversion, and feeding skills. Weight and height were assessed with a length board and a digital scale. If judged necessary, then blood was taken to exclude infections or other organic illnesses. When a more complex oral motor dysfunction could not be ruled out, a videofluoroscopic swallow study was performed.
During admission and in the follow-up period, the multidisciplinary feeding team was directly involved in all of the steps of the program. In particular, the dietitian estimated and calculated the intake, recommended nutrition, and supported the parents during the clinical and outpatient periods. The child psychologist took care of the psychological support and behavioral counseling of parents and child by psychoeducating parents about feeding problems and behavioral aspects, explaining general and specific behavioral techniques, and preparing the parents for the test day at home and the final discharge. The speech-language pathologist evaluated the oral motor function and oral sensibility before the program was started. Later, she gave advice about feeding techniques, seating posture, and type and textures of food to support oral feeding. The nurses feeding the child were skilled and experienced with this protocol. They used positive reinforcement while feeding the child. The team convened daily to discuss progress and decide on the transition to the next treatment step. The parents were informed about the progress every day.
The patients followed a designated hunger provocation program (Table 1). The basic principle of this program is that prolonged withholding of adequate feeding amounts provokes hunger, which may stimulate the motivation to eat as long as oral feeding is not forced. This is obtained by reducing the amount of feeding given by tube to 50% of the preadmission levels, and decreasing it further to the mere substitution of insensible loss, estimated at 400 mL/m2, with water (Table 1). The children were monitored closely with daily physical examination and weight assessment 3 times per week. In addition, vital signs, food and fluid intake, and urine and stool output were carefully documented to monitor excessive weight loss and signs of dehydration, orthostasis, hypoglycemia, and intercurrent infection. Weight loss up to 15% was accepted. To reduce negative stimuli as much as possible, no laboratory tests were carried out during admission. The protocol was approved by the Ethics Committee of the Vrije Universiteit Medical Centre.
Patients were granted feeding at fixed moments, 4 or 5 times per day depending on the patient's age. Meal characteristics varied from patient to patient, being adapted to their individual preferences as much as possible. The type of food, the seating posture made feeding comfortable, and the type of eating equipment were determined by the multidisciplinary team in consultation with the parents.
The feeding sessions took place in quiet, distraction-free surroundings. Feeding was given by the nurse in the absence of the parents. The nurse was instructed to avoid pressure on the child when he refused to eat and to positively reinforce the child's behavior immediately after he accepted some food. Any negative reinforcement, such as physical pressure or forced feeding, was strictly avoided. The sessions were limited to 15 minutes unless the patient wanted to continue eating, and ended with an activity that the child was known to enjoy.
After discharge, frequent contact between the parents and the multidisciplinary team was provided, according to the individual needs of the child and the parents. The children's conditions were reevaluated 3 and 6 month after discharge. Food intake, feeding changes, and eating behavior were documented and analyzed. The children were physically examined, and weight and height were assessed. Height and weight-for-height were evaluated according to Dutch growth standards (17,18).
During the study period, 10 children (7 girls and 3 boys) with PFR were admitted to the hunger provocation program. The children had a complicated medical history (Table 2) and were fully dependent (∼100% of daily intake) on nasogastric tube feeding for a mean duration of 13.5 months (range 7–19 months). All of the patients had withstood earlier interventions, including speech-language pathology, dietary changes, and behavioral treatment. The children's ages ranged between 9 and 21 months (mean 15.7 months). At the time of admission, the height standard deviation scores (SDS) of the children ranged between −4.5 and 0, with weights ranging between 7.5 and 10.2 kg (mean 9.2 kg), accounting for weight-for-height SDS of between −2.0 and 1.3 (mean −0.93) (Table 2).
All but 1 of the children followed and completed the in-hospital hunger provocation program successfully and without complications. One child (patient 5) developed acute rotavirus gastroenteritis during the program, which necessitated temporary interruption of the program and caused prolongation of the intervention to 33 days. All of the other children remained in stable condition during the intervention and showed no signs of dehydration, infection, or hypoglycemia. One child (patient 9), who initially had followed the program successfully, refused to eat adequately during the test period at home, resulting in more than 15% weight loss and the resumption of tube feeding for 1 month.
All 10 children started to eat within 1 week, and the supply of food or fluids through nasogastric tube was stopped after a mean period of 9.1 days (range 4–24 days). As expected, all of the children went through a catabolic state, as demonstrated by ketonuria, which emerged a few days after the beginning of the program. During the period of catabolism, the children were less energetic and weaker, acted slower, and were irritable. These symptoms disappeared once they started to eat more than the calculated insensible loss. Maximum weight loss ranged between 320 and 1390 g (mean 856 g), which was between 3.7% and 15.6% (mean 9.2%) of the weight before intervention (Table 3). The mean duration of inpatient treatment was 17.3 days (range 9–33 days).
At follow-up after 3 and 6 months, 9 of 10 and 8 of 10 patients, respectively, were eating adequately and gaining weight without tube feeding (Table 3). One child (patient 10), who had Noonan syndrome and immunoglobulin G2 deficiency, experienced multiple respiratory infections during the winter season; this resulted in inadequate food intake. Partial (50%) tube feeding was resumed 1 month after discharge, and because of persistence of the feeding problems the child finally underwent gastrostomy. Another child (patient 5), with a complex surgical history (Table 2) and multiple infections after discharge, finally required resumption of partial (25%) tube feeding 4 months after discharge.
The 8 remaining children were gaining weight at 3 months (body weights 7.34–10.50 kg, mean 9.04 kg), with increases over discharge weights of between 240 (3.0%) and 1730 g (22.9%) (mean 690 g, or 8.3%). At follow-up at 6 months they had body weights of 7.80 to 10.69 kg (mean 9.43 kg), accounting for increases in body weight over discharge weight of 700 to 2110 g, or 9.5% to 28% (mean 1.200 g, or 14.6%) and actual weight-for-height SDS of −2.2 to ±0.1, mean −1.3) (Table 3). Nine patients were followed up for periods between 1 and 4.5 years. At the last known date, all but 1 (patient 6) had height SDS similar to or better than those at inclusion, whereas average weight-for-height SDS was similar to that with tube feeding (range −3.6 to 0, mean −0.9) (Table 3).
The findings of this study support the use of a multidisciplinary hunger provocation protocol in children with PFR and tube feeding dependency. All of the patients had a complex medical history that contributed to their feeding problems, and all of them were fully dependent on tube feeding before the intervention. The 2 patients in whom complete weaning from tube feeding failed at follow-up had a complex medical history, which was further complicated by multiple infections after discharge, necessitating the reintroduction of (partial) tube feeding. One of them had Noonan syndrome, which also includes feeding difficulties and failure to thrive in most patients during infancy (19). Therefore, this case is probably not an example of failure of the program but is attributable more to the underlying disease.
The remaining 8 children both resumed eating within 1 week after starting the hunger provocation program and showed weight gain during the 6-month follow-up period. At long-term follow-up (1–4.5 years), most of them were able to keep both height and weight-for-height at the levels they had during full tube feeding at inclusion. Taking into account the complex medical history of most of them, continuation of tube feeding would probably not have led to better growth parameters.
Most studies on weaning off tube feeding are based on a behavioral approach (4,6–14). We are aware of only 2 studies using food intake reduction to stimulate appetite (4,7). Benoit et al (7) reduced tube feeding with 25% in 64 children, 32 of whom also received intensive behavioral therapy. Although 47% of the patients in the combination therapy group could be weaned off tube feeding, none of the children in the feeding reduction–alone group could. Byars et al (4) used a multicomponent behavioral feeding program in 9 children who underwent Nissen fundoplication with gastrostomy tube placement. In addition to behavioral treatment and parent training, these authors restricted energy intake to about 50% to stimulate appetite. After discharge, 4 of 9 children, and after 3 months, 6 of 9 children, were weaned completely off tube feeding. Linscheid (14) recently reviewed the Ohio State program on behavioral interventions for pediatric feeding disorders and reported a success rate of 87.9% by adding elimination of feeding to the behavioral program.
To our knowledge, this is the first study that evaluates the efficacy of short-term hunger provocation as the main intervention strategy to obtain the resumption of full oral feeding in young children with PFR. Hunger results from the complex interaction of a variety of sensory inputs, limbic and cortical modulators, visceral feedback, and hormonal effects. The appetite control center resides in the hypothalamus. Shea et al (20), studying a normal pediatric population, showed that reduction of energy intake stimulates appetite and induces eating within a few hours. Rapid weaning promotes the experience of hunger, which is imperative to overcome learned oral feeding aversion. Creating and stimulating hunger is the drive to start eating. This is not different in PFR children.
The intensive multidisciplinary program with significant energy restriction that we used necessitates careful monitoring and therefore inpatient treatment. Thus, an appropriate and safe learning environment is provided that cannot be reached at home. Hunger provocation in this way induces adequate energy intake within a few weeks in children who would otherwise be condemned to tube feeding for possibly several years. This has an important positive impact on the quality of life for both the child and the parents, improves the relationship between the parents and the child, and—although we did not study this aspect—is obviously cost effective in the long run.
Although we consider the findings in this study remarkable and promising, their generalizability and applicability must be carefully evaluated. We studied only a small series of patients and did not include a control group. Inasmuch as we worked with a dedicated and experienced multidisciplinary team, possible confounding effects such as therapist competence, intensive individual contact, and even therapeutic alliance may have influenced the results. This should be addressed in further studies.
In conclusion, our findings suggest that short-term intensive multidisciplinary treatment with a hunger provocation program is feasible and effective. Further studies should incorporate more patients and use more formal outcome measures. In particular, the hunger provocation program should be compared with intensive outpatient treatment, including support and treatment by the speech-language pathologist, psychologist, dietitian, and pediatric gastroenterologist with a similar intensity as in the program outlined in this study.
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