Enteral nutrition (EN) is the preferred mode of nutrient intake in critically ill patients with a functional gastrointestinal (GI) system because of its lower complication rate and cost compared with parenteral nutrition (PN) (1). To realize the potential benefits of EN in the pediatric intensive care unit, early initiation and maintenance of EN must be ensured. In adults, successful commencement of EN within 48 hr of mechanical ventilation (MV) is associated with up to 20% decrease in mortality in the intensive care unit (ICU) and a 25% decrease in hospital mortality in artificially ventilated patients (2). Early initiation of EN is particularly important in infants and children because they are at risk of rapid nutritional depletion that can lead to muscle wasting, impairment of vital organ function, compromised wound healing, and decreased immune function (3). Studies undertaken in children with burns and critical illness have shown that early EN is well tolerated without detrimental effects (4, 5).

Unfortunately, the delivery of EN is fraught with practical difficulties. There is often a delay in the initiation of EN or hesitation in increasing enteral caloric intake, even if patients are eligible for tube feeding while waiting for bowel sounds, and the managing physicians often underestimate nutritional needs incritically ill patients or prescribe an inadequate amount of nutrients. In addition, EN is frequently interrupted because of nursing interventions or delayed gastric emptying (6, 7).

We hypothesized that a significant proportion of delayed EN in critically ill children is avoidable. The objective of this study was to evaluate the current nutrition support behavior in the care of critically ill children and to identify avoidable reasons for delayed EN.

A retrospective chart review was conducted on pediatric patients admitted to the ICU at Severance Hospital between January 2008 and December 2011. Children were included in the review if they were younger than 19 yr and had been in the ICU for a minimum of 3 days. Patients who stayed for longer than 30 days or were admitted to the general surgery and trauma services were excluded from the study because decisions regarding nutrition in these patients are made by the surgical, rather than critical care, staff. The following patient characteristics were recorded: sex, age, diagnosis on admission, and severity of illness at admission rated by three scoring systems, pediatric index of mortality 2 (PIM2), pediatric risk of mortality (PRISM), and pediatric logistic organ dysfunction (PELOD). Outcomes such as duration of mechanical ventilation support, length of ICU stay, and time of achieving caloric goal were abstracted retrospectively from patient charts. We compared patients receiving EN (EN group) with those not receiving any EN (non-EN group) during the ICU course.

Medical records were available for 200 children (112 males, 88 females) who met the study criteria. The median age was 37.5 (range 1-216) months and 41.5% of the patients were younger than 2 yr. Respiratory problems were the most common causes of ICU admission, followed by neurologic problems and sepsis/septic shock. The median length of ICU stay was 9 (3-30) days. One hundred and fifteen children required mechanical ventilation and the median duration of mechanical ventilation was 6.5 (0-30) days. During hospitalization in the ICU 30 deaths occurred, corresponding to 15% of the cases (Table 1).

Nutritional therapy in any form was started on the day of admission in 74% of the patients. Seven patients did not receive any nutrients during their ICU stay. PN was used for 88.5% of the children and the median time to initiation was 1 day after admission to the ICU. EN was administered to 115 patients, with a median time to EN initiation of 5 days. Only 17% of the patients received EN within 72 hr of ICU admission. The median duration from EN initiation to achievement of calorie goal via EN was 8.5 days in 22 patients.

Among the patients in this study, EN was often initiated as late as day 5 after admission and only 34 patients received EN within 72 hr of admission despite the fact that early EN is known to improve clinical outcomes, decrease infection rates, decrease length of stay, and be cost-effective (1, 9-11). The current clinical guidelines for nutritional support in critically ill adults recommend early initiation of EN within the first 24-48 hr following admission (12, 13). Because there are currently no clinical guidelines for nutritional support in critically ill children, we defined delayed EN as initiation of EN later than 72 hr after admission to ICU - a looser criterion than for adults. The delivery of EN in the ICU may be delayed for several reasons, including GI dysfunction, elective discontinuation of procedures, and physicians' ignorance of nutritional requirements (7, 14). It is important that physicians understand the importance of feeding for appropriate nutritional support because the physician's order is the first step in nutrition delivery. However, many physicians are reluctant to start EN, especially in critically ill patients, because it is known to be associated with an increased risk of aspiration pneumonia (2). In our study, there was no description of the reasons for withholding EN in the medical records of 27% of the patients who received EN late or never received it.

In the current study, the most common reason for delayed EN was gastrointestinal bleeding, in most cases caused by gastric drainage of old blood. Specific definition of bleeding is very important in the ICU setting. Clinically important hemorrhage is defined as overt bleeding plus either hemodynamic changes or the need for blood transfusion. Hemodynamic changes mean that the patient is hypotensive, tachycardic, or orthostatic and the need for transfusion is usually defined by a requirement for two units of blood (15). Only 8 of 71 patients with gastrointestinal bleeding sign met these criteria.

Twenty patients received EN between 3 and 19 days following admission because of signs of decreased bowel motility such as abdominal distension, high gastric residual volume, or vomiting. An excess of gastric residues is the most common complication in critically ill patients receiving gastric nutrition. There is no evidence that the volume of gastric residues affects the risk of pulmonary aspiration and recently published clinical guidelines do not recommend withholding EN for gastric residual volumes <500 mL in the absence of other signs of intolerance (12). However, there are no reference values for children, and primary physicians have to decide when to withhold EN. A survey of physicians showed substantial discordance over this issue (16). Although most physicians believed that nutrition is important in the ICU, they did all not feel confident in their knowledge of the role of nutrition support in the critically ill. Several factors may contribute to this lack of confidence, including a general lack of awareness and poor familiarity with current guidelines, and difficulty integrating previous dogma with recent clinical practice guidelines. It has been reported that most cases of withholding EN, including delayed initiation of EN, could be avoided by better education on standardized feeding processes (17, 18).

In our study, EN was withheld for 16 patients because of hemodynamic instability. Clinical guidelines recommend that EN should be withheld in patients requiring significant hemodynamic support including high-dose catecholamine agents because of an increased risk for subclinical ischemia/reperfusion injury involving the intestinal microcirculation (12). However, there is no consensus among clinicians on the definition of hemodynamic instability; and King et al. (19) reported that pediatric patients receiving cardiovascular medications tolerated EN without adverse events. Medications such as opioids and bowel edema resulting from fluid resuscitation in critically ill patients may cause decreased gastrointestinal motility. Implementation of an EN protocol has been demonstrated to increase nutritional delivery and minimize the risks of tube feeding (7, 20, 21). In our study, there was no significant difference in the percentage of the patients who received delayed EN between the survivor and the non-survivor group.

Upon admission to the ICU, 40.5% of patients had preexisting malnutrition defined by z score of W/A <-2, similar to results of a previous study (22). Although the prevalence of malnourishment was not significantly changed at the time of discharge from ICU, the z score of W/A significantly decreased during ICU stay in the non-EN group but not in the EN group. Briassoulis et al. (5) reported that nutritional status and clinical outcomes were improved by providing early enteral nutrition to critically ill children within 8 hr of ICU admission. As this was a retrospective study, we could not obtain data about daily nutrient intake from EN and/or PN. Although the z score significantly decreased and mortality was higher in the non-EN group, we cannot conclude that EN had a direct positive effect on nutritional status or mortality. Moreover, the duration of mechanical ventilation and ICU stay was significantly longer in the EN group than in the non-EN group. It is possible that a longer stay in the ICU increased the likelihood of receiving EN, and under such conditions delayed EN would be predominant. Moreover, the clinical effects of EN might have been biased by the presence of healthier patients in the EN group, although there was no significant difference in severity scores between the two groups.

Although this study had some limitations due to its retrospective nature, our data showed that EN was often initiated as late as day 5 after admission. We also found that a significant proportion of delayed EN might be avoidable, for example in cases with old blood clots and lower gastrointestinal bleeding. Identification of avoidable reasons for delaying EN will allow educational intervention and modification of clinical practice with the aim of decreasing the incidence of delayed EN in critically ill children.

In conclusion, this study revealed that EN was often initiated as late as day 5 after admission and that such delays might be avoidable in a significant proportion of cases. Strategies for reducing avoidable delayed EN are required to improve enteral nutrition delivery and nutritional status in the critically ill children.