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Hospital-acquired malnutrition in children with mild clinical conditions
Nutrition 25 (2009) 540 –547 www.nutritionjrnl.com
Applied nutritional investigation
Hospital-acquired malnutrition in children with mild clinical conditions Angelo Campanozzi, M.D.a,*, Massimo Russo, Ph.D.b, Alessandra Catucci, M.D.a, Irene Rutigliano, M.D.a, Gennaro Canestrino, M.D.a, Ida Giardino, M.D.c, Arturo Romondia, M.D.d, and Massimo Pettoello-Mantovani, M.D., Ph.D.a,e a
Department of Medical Sciences, Pediatrics, University of Foggia, Foggia, Italy b Institute of Statistics, University of Foggia, Foggia, Italy c Department of Biomedical Sciences, University of Foggia, Foggia, Italy d Pediatric Unit, Public City Hospital, OORR, Foggia, Italy e World Health Policy Forum (WHPF), Giessen, Germany Manuscript received July 6, 2008; accepted November 19, 2008.
Abstract
Objective: Little is known about the incidence and risk factors of hospital-acquired malnutrition in children with mild illness (grade 1 clinical conditions) and its timing of occurrence. The aim of this study was to recognize any early stage of denutrition and possible risk factors leading to nutritional deterioration in children hospitalized due to mild clinical conditions. Methods: Four hundred ninety-six children (age 1–192 mo) with mild clinical conditions were studied. Weight and height were measured. Weight was assessed daily and body mass index (BMI) Z-score was calculated for all patients. Results: Children with a BMI Z-score ⬍⫺2 SD on admission showed a mean BMI decrease at the end of their hospital stay, which was significantly higher than in children who showed a better nutritional condition at admission. Risk factors for hospital-acquired malnutrition were an age ⬍24 mo, a duration of hospital stay ⬎5 d, fever, and night-time abdominal pain. Conclusion: Hospital stay has an impact on the nutritional status of children affected by mild clinical conditions. Children already malnourished on admission were found to be at risk for further nutritional deterioration during their hospital stay; and in all groups of children identified by their BMI Z-score at admission, nutritional status declined progressively. © 2009 Published by Elsevier Inc.
Keywords:
Children; Hospital malnutrition; Body mass index
Introduction Malnutrition is the cellular imbalance between the supply of nutrients and energy and the body’s demand for these to ensure growth, maintenance, and specific functions [1]. It is observed most frequently in economically challenged countries, where it remains one of the most serious public health problems in hospitalized and non-hospitalized children ⬍5 y old [2]. In Asian, Latin American, Near Eastern, and African countries, hospital-acquired malnutrition continues to be an important comorbidity in children, affecting their clinical outcomes [3]. However, hospital-based malnutrition has been described with increasing frequency in * Corresponding author. Tel./fax: ⫹39-0881-733718. E-mail address: [email protected] (A. Campanozzi). 0899-9007/09/$ – see front matter © 2009 Published by Elsevier Inc. doi:10.1016/j.nut.2008.11.026
hospitalized and chronically ill children in economically advantaged countries such as the United States and Europe [3,4]. For instance, protein– energy malnutrition [5] is the most common form of nutritional deficiency in children who are hospitalized in the United States [6]. Protein– energy malnutrition is a term used to describe a broad array of clinical conditions ranging from mild to serious, in which consumption of protein and energy (measured by calories) is insufficient to satisfy the body’s nutritional needs [5]. As many as half of all patients admitted to the hospital in the United States have malnutrition to some degree [7,8], and in a recent study in a large children’s hospital, the prevalence of acute and chronic protein– energy malnutrition was greater than one half [8]. Furthermore, in a survey focusing on low-income areas of the United States, 22–35% of children 2– 6 y of age were reported to be significantly under-
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
weight; and recent studies in European countries also have suggested that children hospitalized due to clinical mild or moderate stress factors are at risk for fat or protein depletion and development of malnutrition [4,8 –10]. The nutritional status of children often declined after admission to the hospital, resulting in early and serious consequences, such as slowing of growth and increased susceptibility to various infections [4,11,12]. Although hospital-acquired malnutrition is frequently associated with a risk of adverse clinical events and a longer hospital stay leading to higher health care costs [12], it is a problem that remains largely underestimated and often unrecognized by health care workers [4,13]. Malnutrition in adult hospitalized subjects is well documented [14], yet relatively few studies have investigated the nutritional status of children admitted to hospitals. Such studies have shown that malnutrition is also a common finding in pediatric inpatients [15]. However, they have focused particularly on severe and chronically ill children, documenting a significant increased risk for malnutrition in these subjects [4]. The impact of hospitalization on the nutritional status of children with mild illness is still not completely clarified [4,9]. Although no classification system for pathologic condition in children is currently accepted worldwide, the criteria proposed by the American Academy of Pediatrics (AAP) and the American Dietetic Association (ADA) [4,16,17] are generally adopted to assess nutritional risk factors in hospitalized children [4]. According to such classification, patients are ranked in three grades. Grade 1 conditions involve mild stress factors, e.g., admission for diagnostic procedures, minor infection, other episodic illnesses, or minor surgery. Grade 2 conditions involve moderate stress factors, e.g., severe but not life-threatening infection, routine surgery, fracture, chronic illness without acute deterioration, or inflammatory bowel disease. Grade 3 conditions involve severe stress factors, e.g., acquired immunodeficiency syndrome, malignancy, severe sepsis, major surgery, multiple injuries, acute deterioration of chronic disease, or major depression. Few studies are available in the literature and very little is known about the onset of malnutrition in children with grade 1 conditions, its timing of occurrence, and its relation to length of hospital stay or other possible clinical variables. The present study was undertaken to evaluate the incidence of malnutrition in children admitted for grade 1 conditions to a general medical pediatric ward and during their hospital stay. The study aimed at identifying any early stage of undernutrition and possible risk factors leading to nutritional deterioration in children hospitalized for mild stress factors.
Materials and methods The Pediatric Unit of the Public City Hospital of Foggia, Italy, was selected for the study. At the time of our survey, it was the only pediatric unit serving the city and surrounding area (approximately 200 000 people). The absence of
541
options in the choice for the hospital by the children’s parents or guardians made this pediatric unit a relatively closed system. It was sufficiently descriptive of the health problems affecting the local pediatric population and useful to study the nutritional status of children hospitalized for grade 1 clinical conditions identified according to AAP and ADA criteria [4]. During a period of 6 mo all children within an age range of 1 mo to 16 y, consecutively admitted to the medical pediatric ward for grade 1 conditions, were enrolled in the study. Grade 1 conditions, characterized by mild stress factors, were those involving admission for diagnostic procedures, minor infections, or other episodic illness as described elsewhere [4]. The research was conducted as follows: 1) classification of patients in homogeneous subgroups in terms of nutritional deterioration after 72 h of hospital stay and on discharge; 2) identification of an early segmentation model by using the entire number of pediatric patients observed as a learning sample. The outcome variable was nutritional status on discharge, and the information collected on admission was assumed as predictive variables. 3) Identification of a further segmentation model that uses the same outcome variable as before and considers those observations collected after the 72-h hospital stay as additional predictive variables. The exclusion criteria were a hospital stay ⬍72 h, an age ⬍1 mo, chronic disease, a need for hydroelectrolytic parenteral support or dehydration identified by a prolonged capillary refill time, skin turgor, and an abnormal respiratory pattern. Weight and height were measured as a part of the routine admission procedure. Standard measurement techniques were applied, such as measuring supine length up to 24 mo of age and standing height from 24 mo onward. Standing height was measured to the nearest 0.5 cm on a standardized wallmounted height board. Weight was measured daily under the same conditions (nude, after voiding, in the morning before breakfast) and was determined to the nearest 0.1 kg by a physician scale; a baby scale was used for infants weighing ⬍15 kg. The weight at admission was considered the reference weight. Body mass index (BMI), based on age and sex, was evaluated for each patient using well-established reference curves by Rolland-Cachera et al. [16]. BMI was calculated from body weight (in kilograms) divided by height (meters) squared. It was registered on admittance, after 72 h, and on discharge. A BMI Z-score system was used according to methods and values previously reported [16] to evaluate the nutritional status of children, because it is widely recognized as being a most reliable system for analysis of anthropometric data [16]. It expresses anthropometric values as several standard deviations (SDs) below or above the reference mean or median value. Because the Z-score scale is linear, summary statistics such as means, SDs, and standard errors can be computed from Z-score values. Furthermore, Z-score summary statistics are helpful for grouping growth data by age and sex and the summary statistics can
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Table 1 Characteristics of 496 children hospitalized for mild clinical conditions at study entry Variable Age (mo) 1–12 13–24 25–36 37–72 ⬎72 Nutritional status on admission BMI Z-score ⬍⫺2 BMI Z-score ⫺2/⫹2 BMI Z-score ⬎⫹2 Diagnosis on admission Respiratory infections Gastrointestinal infections Other minor infections Food intake ⬎50% Food intake ⬍50%
No. of patients (%) 174 (35) 72 (14.5) 48 (9.7) 84 (16.9) 118 (23.8) 51 (10.2) 387 (78.1) 58 (11.7) 187 (37.7) 131 (26.4) 178 (35.9) 246 (49.6) 250 (50.4)
BMI, body mass index
be compared with the reference, which has an expected mean Z-score of 0 and an SD of 1.0 for all normalized growth indices [16]. The 95% distribution of BMI values, from ⫺2 to ⫹2 Z-score (cutoff points), was considered the normal range for nutritional screening of the patients enrolled in the study and a BMI decrease ⱖ0.25 Z-score was arbitrarily taken as the endpoint criterion to reveal evidence of nutritional deterioration during their hospital stay. Parents and, when possible, patients were interviewed by the same pediatric dietitian on admission and after 3 d of hospital stay to evaluate food intake (⬍50% or ⬎50% of the dietary allowance offered by the hospital catering service, in accordance with the recommended dietary allowance), difficulty retaining food (at least three episodes per day of loose stools or at least three episodes per day of vomiting), and pain. Symptoms and clinical signs that interfered with food intake were properly reported, in particular daytime or night-time abdominal pain and fever. Length of hospital stay was registered. The study was performed according to the World Medical Association Declaration of Helsinki for ethical principles in medical research involving human subjects and approved by the internal ethical committee of the Medical School of the University of Foggia for studies performed in subjects of minor age (ⱕ16 y). Written informed consent to the study was obtained by the parents or guardians for the participation of their child in the study. Statistical analysis Classification trees analysis [17] was used to study the relation between malnutrition and a list of predictive variables recorded in the course of hospitalization. Classification tree is a multivariate analysis that classifies different
groups of patients, the most homogeneous possible, with regard to the outcome variable (nutritional deterioration), for estimating the potential risk of malnutrition within each group. The exhaustive chi-square automatic interaction detector method [18,19] was used due to the qualitative nature of the outcome variable (presence or absence of nutritional deterioration), the simultaneous presence of qualitative and quantitative independent variables, and the advantages from non-binary partition. Data elaboration was realized by using SPSS 11.0 (Answer Tree 3.0; SPSS Inc., Chicago, IL, USA). The parameters included in the analysis were age, sex, BMI, type of disease (gastrointestinal, respiratory, others), malnutrition at 72 h (as measured by BMI changes), food intake, vomiting, diarrhea, bloody diarrhea, dysphagia, night-time abdominal pain, daytime abdominal pain, fever, and duration of hospital stay. Student’s t test was used to verify the difference between quantitative parameters of two populations. A Z test was performed to evaluate differences between percentage values. Statistical significance was predetermined as P ⬍ 0.05.
Results A total of 496 children, 276 boys (55.6%) and 220 girls (44.4%), were enrolled in the study. Median age was 25 mo (range 1–192 mo). Children admitted to the study showed the following grade 1 clinical conditions: 26.4% had acute gastrointestinal disorders, 37.7% had upper or lower acute respiratory infections, and 35.9% had other minor infections (urinary infections, arthritis, viral rashes) or were hospitalized because of an elective diagnostic procedure (biopsies, upper or lower gastrointestinal endoscopies, magnetic resonance imaging). Their baseline characteristics are listed in Table 1.
140 120
Number of Patients
542
100 80 60 40 20 0 <-2
- 2/- 1
- 1/ 0
0/+1
+1/+2
>+2
BMI Z-score Fig. 1. Nutritional conditions in 496 children 1–16 y of age hospitalized for mild stress factors (grade 1). Distribution of BMI Z-scores on admission. BMI, body mass index.
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547 Table 3 Mean BMI variation during hospital stay of children hospitalized for mild clinical conditions, according to their BMI Z-score on admission
80 70
Number of Patients
543
60 50 40
BMI Z-score on admission
After 72 h
Discharge
⬍⫺2 ⫺2/0 0/⫹2 ⬎⫹2
⫺0.07 ⫾ 0.8 ⫺0.01 ⫾ 0.4 ⫺0.02 ⫾ 0.23 ⫺0.04 ⫾ 0.17
⫺0.27 ⫾ 2.7 ⫺0.01 ⫾ 0.4* ⫺0.02 ⫾ 0.32† ⫺0.04 ⫾ 0.18‡
BMI, body mass index * P ⬍ 0.05 versus a BMI Z-score ⬍⫺2. † P ⬍ 0.05 versus a BMI Z-score ⬍⫺2. ‡ P ⫽ NS versus a BMI Z-score ⬍⫺2.
30 20 10 0 - 2/- 1
-1/ 0
0/+1
+1/+2
>+2
BMI Z-score Fig. 2. Nutritional conditions in 246 children ⬍2 y of age hospitalized for mild stress factors (grade 1). Distribution of BMI Z-scores on admission. BMI, body mass index.
On admission, 51 of 496 children (10.2%) were below the normal range distribution of BMI Z-scores (⬍⫺2), 387 (78.1%) were within the normal range (⫺2/⫹2), and 58 (11.7%) were above the upper limit (⬎⫹2; Fig. 1). Similar results were seen if the analysis of data was limited to the group of 246 children (49.5%) 1–24 mo of age (Fig. 2). By applying Waterlow’s criteria [21] to monitor the nutritional status of children during their hospital stay, only a nonsignificant increasing trend of mild acute malnutrition was observed between the first and last days of hospitalization (Table 2). However, children with a BMI Z-score ⬍⫺2 SD on admission showed a mean BMI decrease at the end of their hospital stay that was significantly higher (P ⬍ 0.05) than the children with a better nutritional condition at admission (BMI ⫺2 to ⫹2; Table 3 and Fig. 3). Vomiting was observed in 106 patients (21.3%), but their BMI Z-score decrease was not significantly different from children without vomiting (– 0.09 ⫾ 0.3 and – 0.02 ⫾ 0.3, respectively). Diarrhea was present in 87 children (17.5%) and the BMI Z-score change (⫺0.07 ⫾ 0.32) in these subjects was not significantly different from patients without diarrhea (0.03 ⫾ 0.26). Based on their nutritional conditions at discharge, patients were divided in two groups: children who at discharge reached the endpoint criterion of a BMI decrease ⱖ0.25 SD Table 2 Waterlow’s criteria for categorizing acute malnutrition in 496 children with mild clinical conditions during their hospital stay Type of acute malnutrition
No. of patients at hospital admission (%)
No. of patients at hospital discharge (%)
Mild Moderate Severe Total
73 (14.7) 15 (3.1) 4 (0.8) 92 (18.5%)
80 (16.1) 15 (3.1) 2 (0.4) 97 (19.6)
(group A) and those with a BMI decrease not reaching the endpoint criterion (group B). Group A consisted of 97 children (19.56% of total population) with a BMI decrease ⱖ0.25 SD and group B included 399 children (80.44% of total population) with a BMI decrease not reaching the endpoint criterion (Table 4). Early nutritional deterioration was present after 72 h in 86.3% of patients in group A versus 8.0% of patients in group B (P ⬍ 0.001). In children already malnourished on admission found to be at risk of further nutritional deterioration in the course of their hospital stay and in all groups of children identified by their BMI Z-score at admission, nutritional status declined progressively. Figure 4 shows a significant BMI Z-score decrease (ⱖ0.25 SD) at discharge in patients whose Z-score at admission was ⬍⫺2 to ⫹2. Daily food intake is a variable recognized to affect the nutritional status of hospitalized subjects. A BMI Z-score decrease ⱖ0.25 SD was present in 11.8% (29 of 246) of children usually eating ⱖ50% of their dietary allowance and in 27.2% (68 of 250) of those accepting ⬍50% (P ⬍ 0.001). Based on the chi-square automatic interaction detector tree (Fig. 5), four main risk factors for nutritional deterio-
p <0.05
Mean BMI Z-score loss during Hospital Stay
<-2
p <0.05
-0,3 -0,25 -0,2 After 72 h Discharge
-0,15 -0,1 -0,05 0 <-2
-2/0
0/+2
>+2
BMI Z-score on admission
Fig. 3. Mean of BMI decrease measured after 72 h and at discharge in 496 children hospitalized for mild stress factors (grade 1). Subjects were grouped based on their BMI Z-score on admission: 51 children (10.2%) showed a BMI Z-score ⬍⫺2, 387 (78.1%) were within the normal range (⫺2/⫹2), and 58 (11.7%) had a score ⬎⫹2. BMI, body mass index.
544
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Table 4 Comparison between children hospitalized for mild clinical conditions who at discharge showed a BMI decrease ⱖ0.25 SD (group A) and those with a BMI decrease ⬍0.25 SD (group B) Group
No. of patients (%)
A B
BMI Z-score
97 (19.56) 399 (80.44)
P
At admission
At discharge
Admission versus discharge
⫺0.22 ⫾ 2.12 ⫹0.23 ⫾ 1.93
⫺0.88 ⫾ 2.65 ⫹0.34 ⫾ 1.88
⫺0.49 ⫾ 0.27 ⫹0.08 ⫾ 0.20
⬍0.05 NS
BMI, body mass index
ration were identified in the 496 children enrolled in the study: 1) an age ⬍24 mo, 2) a hospital stay ⬎5 d, 3) fever, and 4) night-time abdominal pain.
hospital stay, in 35 of 119 children (29.4%) hospitalized for 6 – 8 d, and in 20 of 49 children (40.8%) with ⬎8 d of hospitalization (Fig. 7).
Age younger than 24 mo
Fever
A BMI Z-score decrease ⱖ0.25 SD was present in 60 of 246 children (24.4%) 1–24 mo of age and in 37 of 250 children (14.8%) ⬎24 mo (P ⬍ 0.001; Table 5). A mean Z-score variation of – 0.006 ⫾ 0.48 was documented in children ⬍2 y, and a variation of – 0.02 ⫾ 0.38 (P ⫽ NS) was observed in children ⬎2 y.
The nutritional endpoint criterion was reached by 29 of 73 patients with fever (39.7%) and by 68 of 423 children (16.0%) without fever (P ⬍ 0.001; Table 5).
Hospital stay longer than 5 d The mean length of hospitalization was 5.1 ⫾ 2.2 d (range 3–14 d) for the total population; hospital stays were 6.6 ⫾ 3.3 d in children who at discharge reached the established endpoint criterion of a BMI decrease ⱖ0.25 SD (group A) and 5.2 ⫾ 2.3 d in children with a BMI decrease not reaching the endpoint criterion (group B). The difference between groups A and B was significant (P ⬍ 0.05). A significant difference of BMI (P ⬍ 0.001) was also observed between children with ⱕ5 d of hospital stay (Z-score 0.05 ⫾ 0.4) and children with ⬎5 d of hospital stay (Z-score ⫺0.11 ⫾ 0.4; Fig. 6). A BMI Z-score decrease ⱖ0.25 SD was significantly higher in children hospitalized for ⬎5 d (Table 5). In particular, BMI Z-score decreases ⱖ0.25 SD were present in 42 of 328 children (12.8%) with ⱕ5 d of
Percentage of patients
35%
*° * ° p< 0.05
30% 25%
*
20%
°
After 72 h Discharge
15% 10% 5% 0% <-2
-2/0
0/+2
>+2
Z-scores on admission Fig. 4. Percentage of BMI decrease ⱖ0.25 SD during hospitalization in 496 children with mild clinical conditions. Subjects were grouped by their Z-score at admission in the hospital. BMI, body mass index.
Night-time abdominal pain In children with night-time abdominal pain, a BMI Zscore decrease ⱖ0.25 SD was present in 38% (29 of 76) of cases and in 16% (68 of 420) of those without nocturnal abdominal pain (P ⬍ 0.001; Table 5). These results, obtained by multivariate analysis, persisted after excluding the group of children with acute digestive disease.
Discussion Nutritional status in children is an indicator of health and well-being at the individual and population levels [9]. Malnutrition has been associated with an increased prevalence of complications in hospitalized children and several studies have suggested that providing appropriate nutritional support during hospital stay decreases the risk of slowing of growth and an increased susceptibility to various infections [12]. The majority of the available studies have assessed the nutritional status of children hospitalized for a wide range of pathologic conditions after their admission to the hospital, whereas in our study we investigated the impact of hospital stay on the nutritional status of children affected by grade 1 clinical conditions [4] (mild stress factors) from the time of admission to discharge. Our study confirms that malnutrition, either overnutrition or undernutrition, is a frequent finding in children at the time of their hospital admission (Table 1) and it shows that a risk for hospital-acquired nutritional deterioration is present in children with mild illness-related stress factors. In fact, the growth charts of Rolland-Cachera et al. [16], used as references/standards, indicated that 19.56% of children
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
545
Fig. 5. Risk factors for nutritional deterioration identified by multivariate analysis in the 496 children enrolled in the study (chi-square automatic interaction detector tree of decision). abd., abdominal.
enrolled in our study had a BMI decrease in the course of hospitalization. Such risk was present mostly in children already malnourished at their hospital admission. There is no universally accepted nutritional screening tool for children [9]. However, it is standard practice in pediatrics to use height and weight charts to calculate growth velocity, which is highly sensitive to nutritional status [20]. The anthropometric indicator most often used is weight-for-age, but it is less efficient than weight-for-height and height-for-age, because a low weight-for-age does not distinguish between wasting and stunting [4,22]. BMI-for-age provides more information because it correlates weight-forheight to age and the Z-score is a BMI-for-age SD score [21]. This measurement is recommended by the World Health Organization for studies in large populations and it is more accurate than describing anthropometric status by using the centile scale [22]. Our study showed that children with a BMI Z-score ⬍⫺2 SD on admission had a weight decrease in the course of their hospital stay, which was significantly more important than in normally nourished patients. Furthermore, in most of the children who were malnourished at discharge, a BMI decrease was already detected after 72 h. This finding suggests the possibility of early detection of children who are candidates for hospital-acquired malnutrition and establish an appropriate nutritional management tool to prevent
the development of such adverse conditions during their hospital stay. The risk of nutritional depletion in hospitalized children should be recognized as soon as possible to begin a timely and appropriate nutritional intervention [23], particularly in children with grade 1 clinical conditions, because the risk for malnutrition in these subjects might be underestimated [4]. Our study identified four main risk factors for hospitalacquired malnutrition in children hospitalized for mild stress factors: an age ⬍24 mo, length of hospital stay, fever, and night-time abdominal pain. Infants need a daily caloric intake per kilogram of body weight much higher than children and adolescents, and any mild reduction of food intake may lead to a severe reduction of BMI. In fact, several studies have shown that children ⬍24 mo of age are more at risk of hospital malnutrition [24]. Our results confirm these data, because a significantly larger percentage of patients ⬍2 y old reached the cutoff point of ⫺0.25 BMI Z-score. Length of hospital stay negatively affected the nutritional status of children enrolled in the study (Figs. 6 and 7), inducing a significant reduction of their BMI, which was related to reduced food intake compared to the recommended dietary allowance (Table 5). In particular, the nutritional cutoff point of ⫺0.25 BMI Z-score was reached by 12.8% of children hospitalized for 3–5 d, by 29.4% of those
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Risk factors Age (mo) 1–24 Food intake ⬍50% ⬎24 Food intake ⬍50% Hospital stay (d) ⱕ5 Food intake ⬍50% ⬎5 Food intake ⬍50% Fever Present Food intake ⬍50% Absent Food intake ⬍50% Night-time abdominal pain Present Food intake ⬍50% Absent Food intake ⬍50%
No. of patients (%) 60/246 (24.4)* 38/60 (63.3)† 37/250 (14.8)* 29/37 (75.6)†
0,06
BMI Z-score change
Table 5 Risk factors for hospital-acquired malnutrition in children hospitalized for mild clinical conditions
29/73 (39.7)* 23/29 (79.3)† 68/423 (16.0)* 46/68 (67.6)† 29/76 (38.0)* 22/29 (75.8)† 68/420 (16.0)* 48/68 (70.5)†
BMI, body mass index * P ⬍ 0.001, BMI Z-score decrease ⱖ0.25. † P ⫽ NS.
staying 6 – 8 d, and by 40.8% of children with a hospital stay ⬎8 d. In that regard, studies from the literature have suggested a negative relation between the duration of hospital stay and satisfaction with the food provided, with the patients staying longest being the most dissatisfied with the food [25]. Insufficient energy intake is known to be responsible for energy imbalance and malnutrition, and fever is always linked to increased energy expenditure [26]. Furthermore, in case of fever, anorexia is often the result of general malaise, a sense of abandonment, or an alteration of taste and smell resulting from drug–nutrient interactions [27]. In our study, 79% of malnourished children with fever (BMI decrease ⱖ0.25 Z-score) showed a reduction of food intake. We also found that night-time abdominal pain is a further risk factor for hospital-acquired malnutrition. Thirty-eight percent of patients with night-time abdominal pain reached the nutritional endpoint criterion at the end of their hospital stay versus 16% of children with no night-time abdominal pain. This variable has been distinguished from daytime abdominal pain because it is a painful condition that wakes the patient and it is generally not associated with a functional condition. In conclusion, hospital-acquired malnutrition continues to be a common finding in hospitalized children, as recently emphasized in a study by Pawellek et al. [28] that determined the prevalence of malnutrition in a series of unselected patients consecutively admitted as inpatients to a large tertiary care children’s hospital in Germany. Our study has shown that children hospitalized for grade 1 clinical
0,04
326 pts
0,02 0 -0,02
123 pts
47 pts
-0,04 -0,06 -0,08 -0,1
42/328 (12.8)* 30/42 (71.4)† 55/168 (32.7)* 39/55 (70.9)†
-0,12 3-5
6-8
>8
Days of Hospital stay Fig. 6. BMI decrease was related to length of hospital stay in children as demonstrated by the BMI Z-score change in 496 patients hospitalized for mild clinical conditions. BMI, body mass index; pts, patients.
conditions (mild stress factors) also are at risk for malnutrition. Nutritional problems causing potential clinical deterioration and a risk for increased morbidity should be promptly recognized in hospitalized children [29]. We suggest that screening pediatric patients for nutritional conditions at hospital admission and during the first 72 h should be considered standard practice in pediatric care units. BMI measurement is rapid and cost effective to recognize a nutritional risk in hospitalized children and it should be performed routinely by a nutritional team. There is good evidence to suggest that improvements in catering services and a better organization of the daily schedule in pediatric care units will increase a patient’s nutritional intake and status, with a positive impact on length of stay and morbidity of hospitalized children [9]. For instance, many adolescents enrolled in our study la-
Patients (%) with BMI loss ≥ 0.25 SD
546
45 40 35 30 25 20 15 10 5 0 3-5
6-8
>8
Days of Hospital stay Fig. 7. Number of children (percentage) with a BMI decrease ⱖ0.25 SD was related to length of hospitalization in 496 children with mild clinical conditions. BMI, body mass index.
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
mented the impossibility of receiving solid food from 19:00 to 08:00 h, with only milk being available in the kitchen of the ward. The provision of meals should be flexible and individualized, and all patients should have the possibility of ordering food and extra food at any time [27] and be informed of this possibility. Menus for children should also include foods with a high energy density [30]. Furthermore, overnight fasting and bowel-cleansing protocols with dietary restrictions should not be used routinely, because they are nutritionally dangerous and often without any therapeutic effect [31]. Knowledge of performing an appropriate nutritional assessment and implementing a rational nutritional therapy in children should be part of any hospital plan of care. Familiarity with nutritional assessment scoring systems and nutritional assessment tools should be part of the staff expertise in any pediatric care unit.
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[11] Hendrikse WH, Reilly JJ, Weaver RL. Malnutrition in a children’s hospital. Clin Nutr 1997;16:13– 8. [12] Reilly JJ, Hull SF, Albert N, Waller A, Bringardener S. Economic impact of malnutrition: a model system for hospitalized patients. JPEN 1988;12:372– 6. [13] Coats KG, Morgan SL, Bartolucci AA, Weinsier RL. Hospital associated malnutrition: a reevaluation 12 years later. J Am Diet Assoc 1993;93:19 –31. [14] Naber THJ, Schermer T, deBree A, Nusteling K, Eggink L, Kruimel JW, et al. Prevalence of malnutrition in nonsurgical hospitalized patients and its association with disease complication. Am J Clin Nutr 1997;66:1232–9. [15] Handricks KM, Duggan C, Gallagher L, Carlin AC, Richardson DS, Collier SB, et al. Malnutrition in hospitalized pediatric patients. Current prevalence. Arch Pediatr Adolesc Med 1995;149:1118 –22. [16] Rolland-Cachera MF, Cole TJ, Sempé M, Tichet J, Rossignol C, Charraud A. Body mass index variations: centiles from birth to 87 years. Eur J Clin Nutr 1991;45:13–21. [17] Breiman L, Friedman J, Olshen R, Stone C. Classification and regression tree. Belmont CA, Wadsworth; 1984. [18] Kass G. An exploratory technique for investigating large quantities of categorical data. J Appl Stat 1980;29:119 –27. [19] Biggs D, De Ville B, Suen E. A method of choosing multiway partitions for classification and decision trees. J Appl Stat 1991;18: 49 – 62. [20] Waterlow JC. Classification and definition of protein caloric malnutrition. BMJ 1972;3:566 –9. [21] De Onis M, Blössner M. The World Health Organization global database on child growth and malnutrition: methodology and applications. Int J Epidemiol 2003;32:518 –26. [22] World Health Organization. WHO child growth standards: length/ height-for-age, weight-for-age, weight-for-length, weight-for-height and body mass index-for-age: methods and development. Geneva: World Health Organization; 2006. [23] Kyle U, Genton L, Pichard C. Hospital length of stay and nutritional status. Curr Opin Clin Nutr Metab Care 2005;8:397– 402. [24] O’Flynn J, Peake H, Hickson M, Foster D, Frost G. The prevalence of malnutrition in hospitals can be reduced: results from three consecutive cross-sectional studies. Clin Nutr 2005;24:1078 – 88. [25] Stanga Z, Zurfluh Y, Roselli M, Sterchi AB, Tanner B, Knecht G. Hospital food: a survey of patients’ perceptions. Clin Nutr 2003;23: 241– 6. [26] McMahon K, Decker G, Ottery FD. Integrating proactive nutritional assessment in clinical practices to prevent complications and cost. Semin Oncol 1998;25:20 –7. [27] Holm L, Smidt S, Michaelsen KF. The sociopsychological importance of food in hospital. Evaluation of a new meal system in a children’s cancer ward. Ugeskr Laeger 1998;20:4415– 8. [28] Pawellek I, Dokoupil K, Koletzko B. Prevalence of malnutrition in paediatric hospital patients. Clin Nutr 2008;27:72– 6. [29] Kondrup J, Allison S, Elia M,Vellas B, Plauth M. ESPEN guidelines for nutrition screening 2002. Clin Nutr 2003;22:415–21. [30] Beck AM, Balknas UN, Camilo ME, Furst P, Gentile MG, Hasunen K, et al; Hoc Group on Nutrition Programmes in Hospitals, Council of Europe. Practices in relation to nutritional care and support. Report from the Council of Europe. Clin Nutr 2002;21:51– 4. [31] Sandhu BK, Isolauri E, Walker-Smith JA, Banchini G, Van CaillieBertrand M, Dias JA, et al. A multicentre study on behalf of the ESPGHAN working group on acute diarrhea: early feeding in childhood gastroenteritis. J Pediatr Gastroenterol Nutr 1997;24:522–7.
Applied nutritional investigation
Hospital-acquired malnutrition in children with mild clinical conditions Angelo Campanozzi, M.D.a,*, Massimo Russo, Ph.D.b, Alessandra Catucci, M.D.a, Irene Rutigliano, M.D.a, Gennaro Canestrino, M.D.a, Ida Giardino, M.D.c, Arturo Romondia, M.D.d, and Massimo Pettoello-Mantovani, M.D., Ph.D.a,e a
Department of Medical Sciences, Pediatrics, University of Foggia, Foggia, Italy b Institute of Statistics, University of Foggia, Foggia, Italy c Department of Biomedical Sciences, University of Foggia, Foggia, Italy d Pediatric Unit, Public City Hospital, OORR, Foggia, Italy e World Health Policy Forum (WHPF), Giessen, Germany Manuscript received July 6, 2008; accepted November 19, 2008.
Abstract
Objective: Little is known about the incidence and risk factors of hospital-acquired malnutrition in children with mild illness (grade 1 clinical conditions) and its timing of occurrence. The aim of this study was to recognize any early stage of denutrition and possible risk factors leading to nutritional deterioration in children hospitalized due to mild clinical conditions. Methods: Four hundred ninety-six children (age 1–192 mo) with mild clinical conditions were studied. Weight and height were measured. Weight was assessed daily and body mass index (BMI) Z-score was calculated for all patients. Results: Children with a BMI Z-score ⬍⫺2 SD on admission showed a mean BMI decrease at the end of their hospital stay, which was significantly higher than in children who showed a better nutritional condition at admission. Risk factors for hospital-acquired malnutrition were an age ⬍24 mo, a duration of hospital stay ⬎5 d, fever, and night-time abdominal pain. Conclusion: Hospital stay has an impact on the nutritional status of children affected by mild clinical conditions. Children already malnourished on admission were found to be at risk for further nutritional deterioration during their hospital stay; and in all groups of children identified by their BMI Z-score at admission, nutritional status declined progressively. © 2009 Published by Elsevier Inc.
Keywords:
Children; Hospital malnutrition; Body mass index
Introduction Malnutrition is the cellular imbalance between the supply of nutrients and energy and the body’s demand for these to ensure growth, maintenance, and specific functions [1]. It is observed most frequently in economically challenged countries, where it remains one of the most serious public health problems in hospitalized and non-hospitalized children ⬍5 y old [2]. In Asian, Latin American, Near Eastern, and African countries, hospital-acquired malnutrition continues to be an important comorbidity in children, affecting their clinical outcomes [3]. However, hospital-based malnutrition has been described with increasing frequency in * Corresponding author. Tel./fax: ⫹39-0881-733718. E-mail address: [email protected] (A. Campanozzi). 0899-9007/09/$ – see front matter © 2009 Published by Elsevier Inc. doi:10.1016/j.nut.2008.11.026
hospitalized and chronically ill children in economically advantaged countries such as the United States and Europe [3,4]. For instance, protein– energy malnutrition [5] is the most common form of nutritional deficiency in children who are hospitalized in the United States [6]. Protein– energy malnutrition is a term used to describe a broad array of clinical conditions ranging from mild to serious, in which consumption of protein and energy (measured by calories) is insufficient to satisfy the body’s nutritional needs [5]. As many as half of all patients admitted to the hospital in the United States have malnutrition to some degree [7,8], and in a recent study in a large children’s hospital, the prevalence of acute and chronic protein– energy malnutrition was greater than one half [8]. Furthermore, in a survey focusing on low-income areas of the United States, 22–35% of children 2– 6 y of age were reported to be significantly under-
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
weight; and recent studies in European countries also have suggested that children hospitalized due to clinical mild or moderate stress factors are at risk for fat or protein depletion and development of malnutrition [4,8 –10]. The nutritional status of children often declined after admission to the hospital, resulting in early and serious consequences, such as slowing of growth and increased susceptibility to various infections [4,11,12]. Although hospital-acquired malnutrition is frequently associated with a risk of adverse clinical events and a longer hospital stay leading to higher health care costs [12], it is a problem that remains largely underestimated and often unrecognized by health care workers [4,13]. Malnutrition in adult hospitalized subjects is well documented [14], yet relatively few studies have investigated the nutritional status of children admitted to hospitals. Such studies have shown that malnutrition is also a common finding in pediatric inpatients [15]. However, they have focused particularly on severe and chronically ill children, documenting a significant increased risk for malnutrition in these subjects [4]. The impact of hospitalization on the nutritional status of children with mild illness is still not completely clarified [4,9]. Although no classification system for pathologic condition in children is currently accepted worldwide, the criteria proposed by the American Academy of Pediatrics (AAP) and the American Dietetic Association (ADA) [4,16,17] are generally adopted to assess nutritional risk factors in hospitalized children [4]. According to such classification, patients are ranked in three grades. Grade 1 conditions involve mild stress factors, e.g., admission for diagnostic procedures, minor infection, other episodic illnesses, or minor surgery. Grade 2 conditions involve moderate stress factors, e.g., severe but not life-threatening infection, routine surgery, fracture, chronic illness without acute deterioration, or inflammatory bowel disease. Grade 3 conditions involve severe stress factors, e.g., acquired immunodeficiency syndrome, malignancy, severe sepsis, major surgery, multiple injuries, acute deterioration of chronic disease, or major depression. Few studies are available in the literature and very little is known about the onset of malnutrition in children with grade 1 conditions, its timing of occurrence, and its relation to length of hospital stay or other possible clinical variables. The present study was undertaken to evaluate the incidence of malnutrition in children admitted for grade 1 conditions to a general medical pediatric ward and during their hospital stay. The study aimed at identifying any early stage of undernutrition and possible risk factors leading to nutritional deterioration in children hospitalized for mild stress factors.
Materials and methods The Pediatric Unit of the Public City Hospital of Foggia, Italy, was selected for the study. At the time of our survey, it was the only pediatric unit serving the city and surrounding area (approximately 200 000 people). The absence of
541
options in the choice for the hospital by the children’s parents or guardians made this pediatric unit a relatively closed system. It was sufficiently descriptive of the health problems affecting the local pediatric population and useful to study the nutritional status of children hospitalized for grade 1 clinical conditions identified according to AAP and ADA criteria [4]. During a period of 6 mo all children within an age range of 1 mo to 16 y, consecutively admitted to the medical pediatric ward for grade 1 conditions, were enrolled in the study. Grade 1 conditions, characterized by mild stress factors, were those involving admission for diagnostic procedures, minor infections, or other episodic illness as described elsewhere [4]. The research was conducted as follows: 1) classification of patients in homogeneous subgroups in terms of nutritional deterioration after 72 h of hospital stay and on discharge; 2) identification of an early segmentation model by using the entire number of pediatric patients observed as a learning sample. The outcome variable was nutritional status on discharge, and the information collected on admission was assumed as predictive variables. 3) Identification of a further segmentation model that uses the same outcome variable as before and considers those observations collected after the 72-h hospital stay as additional predictive variables. The exclusion criteria were a hospital stay ⬍72 h, an age ⬍1 mo, chronic disease, a need for hydroelectrolytic parenteral support or dehydration identified by a prolonged capillary refill time, skin turgor, and an abnormal respiratory pattern. Weight and height were measured as a part of the routine admission procedure. Standard measurement techniques were applied, such as measuring supine length up to 24 mo of age and standing height from 24 mo onward. Standing height was measured to the nearest 0.5 cm on a standardized wallmounted height board. Weight was measured daily under the same conditions (nude, after voiding, in the morning before breakfast) and was determined to the nearest 0.1 kg by a physician scale; a baby scale was used for infants weighing ⬍15 kg. The weight at admission was considered the reference weight. Body mass index (BMI), based on age and sex, was evaluated for each patient using well-established reference curves by Rolland-Cachera et al. [16]. BMI was calculated from body weight (in kilograms) divided by height (meters) squared. It was registered on admittance, after 72 h, and on discharge. A BMI Z-score system was used according to methods and values previously reported [16] to evaluate the nutritional status of children, because it is widely recognized as being a most reliable system for analysis of anthropometric data [16]. It expresses anthropometric values as several standard deviations (SDs) below or above the reference mean or median value. Because the Z-score scale is linear, summary statistics such as means, SDs, and standard errors can be computed from Z-score values. Furthermore, Z-score summary statistics are helpful for grouping growth data by age and sex and the summary statistics can
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Table 1 Characteristics of 496 children hospitalized for mild clinical conditions at study entry Variable Age (mo) 1–12 13–24 25–36 37–72 ⬎72 Nutritional status on admission BMI Z-score ⬍⫺2 BMI Z-score ⫺2/⫹2 BMI Z-score ⬎⫹2 Diagnosis on admission Respiratory infections Gastrointestinal infections Other minor infections Food intake ⬎50% Food intake ⬍50%
No. of patients (%) 174 (35) 72 (14.5) 48 (9.7) 84 (16.9) 118 (23.8) 51 (10.2) 387 (78.1) 58 (11.7) 187 (37.7) 131 (26.4) 178 (35.9) 246 (49.6) 250 (50.4)
BMI, body mass index
be compared with the reference, which has an expected mean Z-score of 0 and an SD of 1.0 for all normalized growth indices [16]. The 95% distribution of BMI values, from ⫺2 to ⫹2 Z-score (cutoff points), was considered the normal range for nutritional screening of the patients enrolled in the study and a BMI decrease ⱖ0.25 Z-score was arbitrarily taken as the endpoint criterion to reveal evidence of nutritional deterioration during their hospital stay. Parents and, when possible, patients were interviewed by the same pediatric dietitian on admission and after 3 d of hospital stay to evaluate food intake (⬍50% or ⬎50% of the dietary allowance offered by the hospital catering service, in accordance with the recommended dietary allowance), difficulty retaining food (at least three episodes per day of loose stools or at least three episodes per day of vomiting), and pain. Symptoms and clinical signs that interfered with food intake were properly reported, in particular daytime or night-time abdominal pain and fever. Length of hospital stay was registered. The study was performed according to the World Medical Association Declaration of Helsinki for ethical principles in medical research involving human subjects and approved by the internal ethical committee of the Medical School of the University of Foggia for studies performed in subjects of minor age (ⱕ16 y). Written informed consent to the study was obtained by the parents or guardians for the participation of their child in the study. Statistical analysis Classification trees analysis [17] was used to study the relation between malnutrition and a list of predictive variables recorded in the course of hospitalization. Classification tree is a multivariate analysis that classifies different
groups of patients, the most homogeneous possible, with regard to the outcome variable (nutritional deterioration), for estimating the potential risk of malnutrition within each group. The exhaustive chi-square automatic interaction detector method [18,19] was used due to the qualitative nature of the outcome variable (presence or absence of nutritional deterioration), the simultaneous presence of qualitative and quantitative independent variables, and the advantages from non-binary partition. Data elaboration was realized by using SPSS 11.0 (Answer Tree 3.0; SPSS Inc., Chicago, IL, USA). The parameters included in the analysis were age, sex, BMI, type of disease (gastrointestinal, respiratory, others), malnutrition at 72 h (as measured by BMI changes), food intake, vomiting, diarrhea, bloody diarrhea, dysphagia, night-time abdominal pain, daytime abdominal pain, fever, and duration of hospital stay. Student’s t test was used to verify the difference between quantitative parameters of two populations. A Z test was performed to evaluate differences between percentage values. Statistical significance was predetermined as P ⬍ 0.05.
Results A total of 496 children, 276 boys (55.6%) and 220 girls (44.4%), were enrolled in the study. Median age was 25 mo (range 1–192 mo). Children admitted to the study showed the following grade 1 clinical conditions: 26.4% had acute gastrointestinal disorders, 37.7% had upper or lower acute respiratory infections, and 35.9% had other minor infections (urinary infections, arthritis, viral rashes) or were hospitalized because of an elective diagnostic procedure (biopsies, upper or lower gastrointestinal endoscopies, magnetic resonance imaging). Their baseline characteristics are listed in Table 1.
140 120
Number of Patients
542
100 80 60 40 20 0 <-2
- 2/- 1
- 1/ 0
0/+1
+1/+2
>+2
BMI Z-score Fig. 1. Nutritional conditions in 496 children 1–16 y of age hospitalized for mild stress factors (grade 1). Distribution of BMI Z-scores on admission. BMI, body mass index.
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547 Table 3 Mean BMI variation during hospital stay of children hospitalized for mild clinical conditions, according to their BMI Z-score on admission
80 70
Number of Patients
543
60 50 40
BMI Z-score on admission
After 72 h
Discharge
⬍⫺2 ⫺2/0 0/⫹2 ⬎⫹2
⫺0.07 ⫾ 0.8 ⫺0.01 ⫾ 0.4 ⫺0.02 ⫾ 0.23 ⫺0.04 ⫾ 0.17
⫺0.27 ⫾ 2.7 ⫺0.01 ⫾ 0.4* ⫺0.02 ⫾ 0.32† ⫺0.04 ⫾ 0.18‡
BMI, body mass index * P ⬍ 0.05 versus a BMI Z-score ⬍⫺2. † P ⬍ 0.05 versus a BMI Z-score ⬍⫺2. ‡ P ⫽ NS versus a BMI Z-score ⬍⫺2.
30 20 10 0 - 2/- 1
-1/ 0
0/+1
+1/+2
>+2
BMI Z-score Fig. 2. Nutritional conditions in 246 children ⬍2 y of age hospitalized for mild stress factors (grade 1). Distribution of BMI Z-scores on admission. BMI, body mass index.
On admission, 51 of 496 children (10.2%) were below the normal range distribution of BMI Z-scores (⬍⫺2), 387 (78.1%) were within the normal range (⫺2/⫹2), and 58 (11.7%) were above the upper limit (⬎⫹2; Fig. 1). Similar results were seen if the analysis of data was limited to the group of 246 children (49.5%) 1–24 mo of age (Fig. 2). By applying Waterlow’s criteria [21] to monitor the nutritional status of children during their hospital stay, only a nonsignificant increasing trend of mild acute malnutrition was observed between the first and last days of hospitalization (Table 2). However, children with a BMI Z-score ⬍⫺2 SD on admission showed a mean BMI decrease at the end of their hospital stay that was significantly higher (P ⬍ 0.05) than the children with a better nutritional condition at admission (BMI ⫺2 to ⫹2; Table 3 and Fig. 3). Vomiting was observed in 106 patients (21.3%), but their BMI Z-score decrease was not significantly different from children without vomiting (– 0.09 ⫾ 0.3 and – 0.02 ⫾ 0.3, respectively). Diarrhea was present in 87 children (17.5%) and the BMI Z-score change (⫺0.07 ⫾ 0.32) in these subjects was not significantly different from patients without diarrhea (0.03 ⫾ 0.26). Based on their nutritional conditions at discharge, patients were divided in two groups: children who at discharge reached the endpoint criterion of a BMI decrease ⱖ0.25 SD Table 2 Waterlow’s criteria for categorizing acute malnutrition in 496 children with mild clinical conditions during their hospital stay Type of acute malnutrition
No. of patients at hospital admission (%)
No. of patients at hospital discharge (%)
Mild Moderate Severe Total
73 (14.7) 15 (3.1) 4 (0.8) 92 (18.5%)
80 (16.1) 15 (3.1) 2 (0.4) 97 (19.6)
(group A) and those with a BMI decrease not reaching the endpoint criterion (group B). Group A consisted of 97 children (19.56% of total population) with a BMI decrease ⱖ0.25 SD and group B included 399 children (80.44% of total population) with a BMI decrease not reaching the endpoint criterion (Table 4). Early nutritional deterioration was present after 72 h in 86.3% of patients in group A versus 8.0% of patients in group B (P ⬍ 0.001). In children already malnourished on admission found to be at risk of further nutritional deterioration in the course of their hospital stay and in all groups of children identified by their BMI Z-score at admission, nutritional status declined progressively. Figure 4 shows a significant BMI Z-score decrease (ⱖ0.25 SD) at discharge in patients whose Z-score at admission was ⬍⫺2 to ⫹2. Daily food intake is a variable recognized to affect the nutritional status of hospitalized subjects. A BMI Z-score decrease ⱖ0.25 SD was present in 11.8% (29 of 246) of children usually eating ⱖ50% of their dietary allowance and in 27.2% (68 of 250) of those accepting ⬍50% (P ⬍ 0.001). Based on the chi-square automatic interaction detector tree (Fig. 5), four main risk factors for nutritional deterio-
p <0.05
Mean BMI Z-score loss during Hospital Stay
<-2
p <0.05
-0,3 -0,25 -0,2 After 72 h Discharge
-0,15 -0,1 -0,05 0 <-2
-2/0
0/+2
>+2
BMI Z-score on admission
Fig. 3. Mean of BMI decrease measured after 72 h and at discharge in 496 children hospitalized for mild stress factors (grade 1). Subjects were grouped based on their BMI Z-score on admission: 51 children (10.2%) showed a BMI Z-score ⬍⫺2, 387 (78.1%) were within the normal range (⫺2/⫹2), and 58 (11.7%) had a score ⬎⫹2. BMI, body mass index.
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A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Table 4 Comparison between children hospitalized for mild clinical conditions who at discharge showed a BMI decrease ⱖ0.25 SD (group A) and those with a BMI decrease ⬍0.25 SD (group B) Group
No. of patients (%)
A B
BMI Z-score
97 (19.56) 399 (80.44)
P
At admission
At discharge
Admission versus discharge
⫺0.22 ⫾ 2.12 ⫹0.23 ⫾ 1.93
⫺0.88 ⫾ 2.65 ⫹0.34 ⫾ 1.88
⫺0.49 ⫾ 0.27 ⫹0.08 ⫾ 0.20
⬍0.05 NS
BMI, body mass index
ration were identified in the 496 children enrolled in the study: 1) an age ⬍24 mo, 2) a hospital stay ⬎5 d, 3) fever, and 4) night-time abdominal pain.
hospital stay, in 35 of 119 children (29.4%) hospitalized for 6 – 8 d, and in 20 of 49 children (40.8%) with ⬎8 d of hospitalization (Fig. 7).
Age younger than 24 mo
Fever
A BMI Z-score decrease ⱖ0.25 SD was present in 60 of 246 children (24.4%) 1–24 mo of age and in 37 of 250 children (14.8%) ⬎24 mo (P ⬍ 0.001; Table 5). A mean Z-score variation of – 0.006 ⫾ 0.48 was documented in children ⬍2 y, and a variation of – 0.02 ⫾ 0.38 (P ⫽ NS) was observed in children ⬎2 y.
The nutritional endpoint criterion was reached by 29 of 73 patients with fever (39.7%) and by 68 of 423 children (16.0%) without fever (P ⬍ 0.001; Table 5).
Hospital stay longer than 5 d The mean length of hospitalization was 5.1 ⫾ 2.2 d (range 3–14 d) for the total population; hospital stays were 6.6 ⫾ 3.3 d in children who at discharge reached the established endpoint criterion of a BMI decrease ⱖ0.25 SD (group A) and 5.2 ⫾ 2.3 d in children with a BMI decrease not reaching the endpoint criterion (group B). The difference between groups A and B was significant (P ⬍ 0.05). A significant difference of BMI (P ⬍ 0.001) was also observed between children with ⱕ5 d of hospital stay (Z-score 0.05 ⫾ 0.4) and children with ⬎5 d of hospital stay (Z-score ⫺0.11 ⫾ 0.4; Fig. 6). A BMI Z-score decrease ⱖ0.25 SD was significantly higher in children hospitalized for ⬎5 d (Table 5). In particular, BMI Z-score decreases ⱖ0.25 SD were present in 42 of 328 children (12.8%) with ⱕ5 d of
Percentage of patients
35%
*° * ° p< 0.05
30% 25%
*
20%
°
After 72 h Discharge
15% 10% 5% 0% <-2
-2/0
0/+2
>+2
Z-scores on admission Fig. 4. Percentage of BMI decrease ⱖ0.25 SD during hospitalization in 496 children with mild clinical conditions. Subjects were grouped by their Z-score at admission in the hospital. BMI, body mass index.
Night-time abdominal pain In children with night-time abdominal pain, a BMI Zscore decrease ⱖ0.25 SD was present in 38% (29 of 76) of cases and in 16% (68 of 420) of those without nocturnal abdominal pain (P ⬍ 0.001; Table 5). These results, obtained by multivariate analysis, persisted after excluding the group of children with acute digestive disease.
Discussion Nutritional status in children is an indicator of health and well-being at the individual and population levels [9]. Malnutrition has been associated with an increased prevalence of complications in hospitalized children and several studies have suggested that providing appropriate nutritional support during hospital stay decreases the risk of slowing of growth and an increased susceptibility to various infections [12]. The majority of the available studies have assessed the nutritional status of children hospitalized for a wide range of pathologic conditions after their admission to the hospital, whereas in our study we investigated the impact of hospital stay on the nutritional status of children affected by grade 1 clinical conditions [4] (mild stress factors) from the time of admission to discharge. Our study confirms that malnutrition, either overnutrition or undernutrition, is a frequent finding in children at the time of their hospital admission (Table 1) and it shows that a risk for hospital-acquired nutritional deterioration is present in children with mild illness-related stress factors. In fact, the growth charts of Rolland-Cachera et al. [16], used as references/standards, indicated that 19.56% of children
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
545
Fig. 5. Risk factors for nutritional deterioration identified by multivariate analysis in the 496 children enrolled in the study (chi-square automatic interaction detector tree of decision). abd., abdominal.
enrolled in our study had a BMI decrease in the course of hospitalization. Such risk was present mostly in children already malnourished at their hospital admission. There is no universally accepted nutritional screening tool for children [9]. However, it is standard practice in pediatrics to use height and weight charts to calculate growth velocity, which is highly sensitive to nutritional status [20]. The anthropometric indicator most often used is weight-for-age, but it is less efficient than weight-for-height and height-for-age, because a low weight-for-age does not distinguish between wasting and stunting [4,22]. BMI-for-age provides more information because it correlates weight-forheight to age and the Z-score is a BMI-for-age SD score [21]. This measurement is recommended by the World Health Organization for studies in large populations and it is more accurate than describing anthropometric status by using the centile scale [22]. Our study showed that children with a BMI Z-score ⬍⫺2 SD on admission had a weight decrease in the course of their hospital stay, which was significantly more important than in normally nourished patients. Furthermore, in most of the children who were malnourished at discharge, a BMI decrease was already detected after 72 h. This finding suggests the possibility of early detection of children who are candidates for hospital-acquired malnutrition and establish an appropriate nutritional management tool to prevent
the development of such adverse conditions during their hospital stay. The risk of nutritional depletion in hospitalized children should be recognized as soon as possible to begin a timely and appropriate nutritional intervention [23], particularly in children with grade 1 clinical conditions, because the risk for malnutrition in these subjects might be underestimated [4]. Our study identified four main risk factors for hospitalacquired malnutrition in children hospitalized for mild stress factors: an age ⬍24 mo, length of hospital stay, fever, and night-time abdominal pain. Infants need a daily caloric intake per kilogram of body weight much higher than children and adolescents, and any mild reduction of food intake may lead to a severe reduction of BMI. In fact, several studies have shown that children ⬍24 mo of age are more at risk of hospital malnutrition [24]. Our results confirm these data, because a significantly larger percentage of patients ⬍2 y old reached the cutoff point of ⫺0.25 BMI Z-score. Length of hospital stay negatively affected the nutritional status of children enrolled in the study (Figs. 6 and 7), inducing a significant reduction of their BMI, which was related to reduced food intake compared to the recommended dietary allowance (Table 5). In particular, the nutritional cutoff point of ⫺0.25 BMI Z-score was reached by 12.8% of children hospitalized for 3–5 d, by 29.4% of those
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Risk factors Age (mo) 1–24 Food intake ⬍50% ⬎24 Food intake ⬍50% Hospital stay (d) ⱕ5 Food intake ⬍50% ⬎5 Food intake ⬍50% Fever Present Food intake ⬍50% Absent Food intake ⬍50% Night-time abdominal pain Present Food intake ⬍50% Absent Food intake ⬍50%
No. of patients (%) 60/246 (24.4)* 38/60 (63.3)† 37/250 (14.8)* 29/37 (75.6)†
0,06
BMI Z-score change
Table 5 Risk factors for hospital-acquired malnutrition in children hospitalized for mild clinical conditions
29/73 (39.7)* 23/29 (79.3)† 68/423 (16.0)* 46/68 (67.6)† 29/76 (38.0)* 22/29 (75.8)† 68/420 (16.0)* 48/68 (70.5)†
BMI, body mass index * P ⬍ 0.001, BMI Z-score decrease ⱖ0.25. † P ⫽ NS.
staying 6 – 8 d, and by 40.8% of children with a hospital stay ⬎8 d. In that regard, studies from the literature have suggested a negative relation between the duration of hospital stay and satisfaction with the food provided, with the patients staying longest being the most dissatisfied with the food [25]. Insufficient energy intake is known to be responsible for energy imbalance and malnutrition, and fever is always linked to increased energy expenditure [26]. Furthermore, in case of fever, anorexia is often the result of general malaise, a sense of abandonment, or an alteration of taste and smell resulting from drug–nutrient interactions [27]. In our study, 79% of malnourished children with fever (BMI decrease ⱖ0.25 Z-score) showed a reduction of food intake. We also found that night-time abdominal pain is a further risk factor for hospital-acquired malnutrition. Thirty-eight percent of patients with night-time abdominal pain reached the nutritional endpoint criterion at the end of their hospital stay versus 16% of children with no night-time abdominal pain. This variable has been distinguished from daytime abdominal pain because it is a painful condition that wakes the patient and it is generally not associated with a functional condition. In conclusion, hospital-acquired malnutrition continues to be a common finding in hospitalized children, as recently emphasized in a study by Pawellek et al. [28] that determined the prevalence of malnutrition in a series of unselected patients consecutively admitted as inpatients to a large tertiary care children’s hospital in Germany. Our study has shown that children hospitalized for grade 1 clinical
0,04
326 pts
0,02 0 -0,02
123 pts
47 pts
-0,04 -0,06 -0,08 -0,1
42/328 (12.8)* 30/42 (71.4)† 55/168 (32.7)* 39/55 (70.9)†
-0,12 3-5
6-8
>8
Days of Hospital stay Fig. 6. BMI decrease was related to length of hospital stay in children as demonstrated by the BMI Z-score change in 496 patients hospitalized for mild clinical conditions. BMI, body mass index; pts, patients.
conditions (mild stress factors) also are at risk for malnutrition. Nutritional problems causing potential clinical deterioration and a risk for increased morbidity should be promptly recognized in hospitalized children [29]. We suggest that screening pediatric patients for nutritional conditions at hospital admission and during the first 72 h should be considered standard practice in pediatric care units. BMI measurement is rapid and cost effective to recognize a nutritional risk in hospitalized children and it should be performed routinely by a nutritional team. There is good evidence to suggest that improvements in catering services and a better organization of the daily schedule in pediatric care units will increase a patient’s nutritional intake and status, with a positive impact on length of stay and morbidity of hospitalized children [9]. For instance, many adolescents enrolled in our study la-
Patients (%) with BMI loss ≥ 0.25 SD
546
45 40 35 30 25 20 15 10 5 0 3-5
6-8
>8
Days of Hospital stay Fig. 7. Number of children (percentage) with a BMI decrease ⱖ0.25 SD was related to length of hospitalization in 496 children with mild clinical conditions. BMI, body mass index.
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
mented the impossibility of receiving solid food from 19:00 to 08:00 h, with only milk being available in the kitchen of the ward. The provision of meals should be flexible and individualized, and all patients should have the possibility of ordering food and extra food at any time [27] and be informed of this possibility. Menus for children should also include foods with a high energy density [30]. Furthermore, overnight fasting and bowel-cleansing protocols with dietary restrictions should not be used routinely, because they are nutritionally dangerous and often without any therapeutic effect [31]. Knowledge of performing an appropriate nutritional assessment and implementing a rational nutritional therapy in children should be part of any hospital plan of care. Familiarity with nutritional assessment scoring systems and nutritional assessment tools should be part of the staff expertise in any pediatric care unit.
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