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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.
weight; and recent studies in European countries also have options in the choice for the hospital by the children’s
suggested that children hospitalized due to clinical mild or parents or guardians made this pediatric unit a relatively
moderate stress factors are at risk for fat or protein depletion closed system. It was sufficiently descriptive of the health
and development of malnutrition [4,8 –10]. problems affecting the local pediatric population and useful
The nutritional status of children often declined after to study the nutritional status of children hospitalized for
admission to the hospital, resulting in early and serious grade 1 clinical conditions identified according to AAP and
consequences, such as slowing of growth and increased ADA criteria [4].
susceptibility to various infections [4,11,12]. Although During a period of 6 mo all children within an age range of
hospital-acquired malnutrition is frequently associated 1 mo to 16 y, consecutively admitted to the medical pediatric
with a risk of adverse clinical events and a longer hos- ward for grade 1 conditions, were enrolled in the study. Grade
pital stay leading to higher health care costs [12], it is a 1 conditions, characterized by mild stress factors, were those
problem that remains largely underestimated and often involving admission for diagnostic procedures, minor infec-
unrecognized by health care workers [4,13]. tions, or other episodic illness as described elsewhere [4].
Malnutrition in adult hospitalized subjects is well docu- The research was conducted as follows: 1) classification of
mented [14], yet relatively few studies have investigated the patients in homogeneous subgroups in terms of nutritional
nutritional status of children admitted to hospitals. Such studies deterioration after 72 h of hospital stay and on discharge; 2)
have shown that malnutrition is also a common finding in identification of an early segmentation model by using the
pediatric inpatients [15]. However, they have focused particu- entire number of pediatric patients observed as a learning
larly on severe and chronically ill children, documenting a sample. The outcome variable was nutritional status on dis-
significant increased risk for malnutrition in these subjects [4]. charge, and the information collected on admission was as-
The impact of hospitalization on the nutritional status of chil- sumed as predictive variables. 3) Identification of a further
dren with mild illness is still not completely clarified [4,9]. segmentation model that uses the same outcome variable as
Although no classification system for pathologic condition before and considers those observations collected after the
in children is currently accepted worldwide, the criteria pro- 72-h hospital stay as additional predictive variables.
posed by the American Academy of Pediatrics (AAP) and the The exclusion criteria were a hospital stay ⬍72 h, an age
American Dietetic Association (ADA) [4,16,17] are generally ⬍1 mo, chronic disease, a need for hydroelectrolytic par-
adopted to assess nutritional risk factors in hospitalized chil- enteral support or dehydration identified by a prolonged
dren [4]. According to such classification, patients are ranked capillary refill time, skin turgor, and an abnormal respira-
in three grades. Grade 1 conditions involve mild stress factors, tory pattern.
e.g., admission for diagnostic procedures, minor infection, Weight and height were measured as a part of the routine
other episodic illnesses, or minor surgery. Grade 2 conditions admission procedure. Standard measurement techniques were
involve moderate stress factors, e.g., severe but not life-threat- applied, such as measuring supine length up to 24 mo of age
ening infection, routine surgery, fracture, chronic illness with- and standing height from 24 mo onward. Standing height was
out acute deterioration, or inflammatory bowel disease. Grade measured to the nearest 0.5 cm on a standardized wall-
3 conditions involve severe stress factors, e.g., acquired im- mounted height board. Weight was measured daily under the
munodeficiency syndrome, malignancy, severe sepsis, major same conditions (nude, after voiding, in the morning before
surgery, multiple injuries, acute deterioration of chronic dis- breakfast) and was determined to the nearest 0.1 kg by a
ease, or major depression. physician scale; a baby scale was used for infants weighing
Few studies are available in the literature and very little is ⬍15 kg. The weight at admission was considered the reference
known about the onset of malnutrition in children with grade 1 weight.
conditions, its timing of occurrence, and its relation to length of Body mass index (BMI), based on age and sex, was
hospital stay or other possible clinical variables. The present evaluated for each patient using well-established reference
study was undertaken to evaluate the incidence of malnutrition curves by Rolland-Cachera et al. [16]. BMI was calculated
in children admitted for grade 1 conditions to a general medical from body weight (in kilograms) divided by height (meters)
pediatric ward and during their hospital stay. The study aimed squared. It was registered on admittance, after 72 h, and on
at identifying any early stage of undernutrition and possible discharge. A BMI Z-score system was used according to
risk factors leading to nutritional deterioration in children hos- methods and values previously reported [16] to evaluate the
pitalized for mild stress factors. nutritional status of children, because it is widely recog-
nized as being a most reliable system for analysis of an-
thropometric data [16]. It expresses anthropometric values
Materials and methods as several standard deviations (SDs) below or above the
reference mean or median value. Because the Z-score scale
The Pediatric Unit of the Public City Hospital of Foggia, is linear, summary statistics such as means, SDs, and stan-
Italy, was selected for the study. At the time of our survey, dard errors can be computed from Z-score values. Further-
it was the only pediatric unit serving the city and surround- more, Z-score summary statistics are helpful for grouping
ing area (approximately 200 000 people). The absence of growth data by age and sex and the summary statistics can
542 A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
100
ical Association Declaration of Helsinki for ethical princi-
ples in medical research involving human subjects and ap- 80
proved by the internal ethical committee of the Medical
School of the University of Foggia for studies performed in 60
subjects of minor age (ⱕ16 y). Written informed consent to
40
the study was obtained by the parents or guardians for the
participation of their child in the study. 20
Statistical analysis 0
<-2 - 2/- 1 - 1/ 0 0/+1 +1/+2 >+2
Classification trees analysis [17] was used to study the BMI Z-score
relation between malnutrition and a list of predictive vari- Fig. 1. Nutritional conditions in 496 children 1–16 y of age hospitalized for
ables recorded in the course of hospitalization. Classifica- mild stress factors (grade 1). Distribution of BMI Z-scores on admission.
tion tree is a multivariate analysis that classifies different BMI, body mass index.
A. Campanozzi et al. / Nutrition 25 (2009) 540 –547 543
Table 3
80 Mean BMI variation during hospital stay of children hospitalized for
mild clinical conditions, according to their BMI Z-score on admission
70
BMI Z-score on admission After 72 h Discharge
Number of Patients
60
⬍⫺2 ⫺0.07 ⫾ 0.8 ⫺0.27 ⫾ 2.7
50 ⫺2/0 ⫺0.01 ⫾ 0.4 ⫺0.01 ⫾ 0.4*
0/⫹2 ⫺0.02 ⫾ 0.23 ⫺0.02 ⫾ 0.32†
40 ⬎⫹2 ⫺0.04 ⫾ 0.17 ⫺0.04 ⫾ 0.18‡
0
<-2 - 2/- 1 -1/ 0 0/+1 +1/+2 >+2
(group A) and those with a BMI decrease not reaching the
BMI Z-score endpoint criterion (group B). Group A consisted of 97
children (19.56% of total population) with a BMI decrease
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. ⱖ0.25 SD and group B included 399 children (80.44% of
BMI, body mass index. 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
On admission, 51 of 496 children (10.2%) were below versus 8.0% of patients in group B (P ⬍ 0.001).
the normal range distribution of BMI Z-scores (⬍⫺2), 387 In children already malnourished on admission found to
(78.1%) were within the normal range (⫺2/⫹2), and 58 be at risk of further nutritional deterioration in the course of
(11.7%) were above the upper limit (⬎⫹2; Fig. 1). Similar their hospital stay and in all groups of children identified by
results were seen if the analysis of data was limited to the their BMI Z-score at admission, nutritional status declined
group of 246 children (49.5%) 1–24 mo of age (Fig. 2). By progressively. Figure 4 shows a significant BMI Z-score
applying Waterlow’s criteria [21] to monitor the nutritional decrease (ⱖ0.25 SD) at discharge in patients whose Z-score
status of children during their hospital stay, only a non- at admission was ⬍⫺2 to ⫹2.
significant increasing trend of mild acute malnutrition was Daily food intake is a variable recognized to affect the
observed between the first and last days of hospitalization nutritional status of hospitalized subjects. A BMI Z-score
(Table 2). However, children with a BMI Z-score ⬍⫺2 SD decrease ⱖ0.25 SD was present in 11.8% (29 of 246) of
on admission showed a mean BMI decrease at the end of children usually eating ⱖ50% of their dietary allowance
their hospital stay that was significantly higher (P ⬍ 0.05) and in 27.2% (68 of 250) of those accepting ⬍50% (P ⬍
than the children with a better nutritional condition at ad- 0.001).
mission (BMI ⫺2 to ⫹2; Table 3 and Fig. 3). Vomiting was Based on the chi-square automatic interaction detector
observed in 106 patients (21.3%), but their BMI Z-score tree (Fig. 5), four main risk factors for nutritional deterio-
decrease was not significantly different from children
without vomiting (– 0.09 ⫾ 0.3 and – 0.02 ⫾ 0.3, respec-
p <0.05
tively). Diarrhea was present in 87 children (17.5%) and
Mean BMI Z-score loss during Hospital Stay
Table 2 -0,05
Waterlow’s criteria for categorizing acute malnutrition in 496 children
with mild clinical conditions during their hospital stay 0
<-2 -2/0 0/+2 >+2
Type of acute No. of patients at No. of patients at BMI Z-score on admission
malnutrition hospital admission (%) hospital discharge (%)
Mild 73 (14.7) 80 (16.1) Fig. 3. Mean of BMI decrease measured after 72 h and at discharge in 496
Moderate 15 (3.1) 15 (3.1) children hospitalized for mild stress factors (grade 1). Subjects were
Severe 4 (0.8) 2 (0.4) grouped based on their BMI Z-score on admission: 51 children (10.2%)
Total 92 (18.5%) 97 (19.6) 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 (%) BMI Z-score P
ration were identified in the 496 children enrolled in the hospital stay, in 35 of 119 children (29.4%) hospitalized for
study: 1) an age ⬍24 mo, 2) a hospital stay ⬎5 d, 3) fever, 6 – 8 d, and in 20 of 49 children (40.8%) with ⬎8 d of
and 4) night-time abdominal pain. hospitalization (Fig. 7).
A BMI Z-score decrease ⱖ0.25 SD was present in 60 of The nutritional endpoint criterion was reached by 29 of
246 children (24.4%) 1–24 mo of age and in 37 of 250 73 patients with fever (39.7%) and by 68 of 423 children
children (14.8%) ⬎24 mo (P ⬍ 0.001; Table 5). A mean (16.0%) without fever (P ⬍ 0.001; Table 5).
Z-score variation of – 0.006 ⫾ 0.48 was documented in
children ⬍2 y, and a variation of – 0.02 ⫾ 0.38 (P ⫽ NS) Night-time abdominal pain
was observed in children ⬎2 y.
In children with night-time abdominal pain, a BMI Z-
Hospital stay longer than 5 d score decrease ⱖ0.25 SD was present in 38% (29 of 76) of
cases and in 16% (68 of 420) of those without nocturnal
The mean length of hospitalization was 5.1 ⫾ 2.2 d abdominal pain (P ⬍ 0.001; Table 5).
(range 3–14 d) for the total population; hospital stays were These results, obtained by multivariate analysis, per-
6.6 ⫾ 3.3 d in children who at discharge reached the sisted after excluding the group of children with acute
established endpoint criterion of a BMI decrease ⱖ0.25 SD digestive disease.
(group A) and 5.2 ⫾ 2.3 d in children with a BMI decrease
not reaching the endpoint criterion (group B). The differ-
ence between groups A and B was significant (P ⬍ 0.05). A
Discussion
significant difference of BMI (P ⬍ 0.001) was also ob-
served between children with ⱕ5 d of hospital stay (Z-score
Nutritional status in children is an indicator of health and
0.05 ⫾ 0.4) and children with ⬎5 d of hospital stay (Z-score
well-being at the individual and population levels [9]. Mal-
⫺0.11 ⫾ 0.4; Fig. 6). A BMI Z-score decrease ⱖ0.25 SD
nutrition has been associated with an increased prevalence
was significantly higher in children hospitalized for ⬎5 d
of complications in hospitalized children and several studies
(Table 5). In particular, BMI Z-score decreases ⱖ0.25 SD
have suggested that providing appropriate nutritional sup-
were present in 42 of 328 children (12.8%) with ⱕ5 d of
port during hospital stay decreases the risk of slowing of
growth and an increased susceptibility to various infections
35%
[12].
*° The majority of the available studies have assessed the
30% * ° p< 0.05
Percentage of patients
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 the development of such adverse conditions during their
hospitalization. Such risk was present mostly in children hospital stay.
already malnourished at their hospital admission. The risk of nutritional depletion in hospitalized children
There is no universally accepted nutritional screening should be recognized as soon as possible to begin a timely
tool for children [9]. However, it is standard practice in and appropriate nutritional intervention [23], particularly in
pediatrics to use height and weight charts to calculate children with grade 1 clinical conditions, because the risk
growth velocity, which is highly sensitive to nutritional sta- for malnutrition in these subjects might be underestimated
tus [20]. The anthropometric indicator most often used is [4]. Our study identified four main risk factors for hospital-
weight-for-age, but it is less efficient than weight-for-height acquired malnutrition in children hospitalized for mild
and height-for-age, because a low weight-for-age does not stress factors: an age ⬍24 mo, length of hospital stay, fever,
distinguish between wasting and stunting [4,22]. BMI-for-age and night-time abdominal pain.
provides more information because it correlates weight-for- Infants need a daily caloric intake per kilogram of body
height to age and the Z-score is a BMI-for-age SD score [21]. weight much higher than children and adolescents, and any
This measurement is recommended by the World Health Or- mild reduction of food intake may lead to a severe reduction
ganization for studies in large populations and it is more of BMI. In fact, several studies have shown that children
accurate than describing anthropometric status by using the ⬍24 mo of age are more at risk of hospital malnutrition
centile scale [22]. [24]. Our results confirm these data, because a significantly
Our study showed that children with a BMI Z-score larger percentage of patients ⬍2 y old reached the cutoff
⬍⫺2 SD on admission had a weight decrease in the course point of ⫺0.25 BMI Z-score.
of their hospital stay, which was significantly more impor- Length of hospital stay negatively affected the nutritional
tant than in normally nourished patients. Furthermore, in status of children enrolled in the study (Figs. 6 and 7),
most of the children who were malnourished at discharge, a inducing a significant reduction of their BMI, which was
BMI decrease was already detected after 72 h. This finding related to reduced food intake compared to the recom-
suggests the possibility of early detection of children who mended dietary allowance (Table 5). In particular, the nu-
are candidates for hospital-acquired malnutrition and estab- tritional cutoff point of ⫺0.25 BMI Z-score was reached by
lish an appropriate nutritional management tool to prevent 12.8% of children hospitalized for 3–5 d, by 29.4% of those
546 A. Campanozzi et al. / Nutrition 25 (2009) 540 –547
Table 5
0,06
Risk factors for hospital-acquired malnutrition in children hospitalized
for mild clinical conditions 0,04 326 pts
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