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Current Medical Research & Opinion Vol. 30, No.

6, 2014, 1065–1069

0300-7995 Article ST-0409.R1/887003


doi:10.1185/03007995.2014.887003 All rights reserved: reproduction in whole or part not permitted

Brief report
Gastrointestinal bleeding in hospitalized children
in the United States
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Chaitanya Pant Abstract


Department of Medicine, Kansas University Medical
Center, Kansas City, KS, USA Objective:
To investigate the epidemiology of GI bleeding in hospitalized children in the United States.
Senthilkumar Sankararaman
Department of Pediatrics, Louisiana State University
Health Sciences Center, Shreveport, LA, USA
Methods:
Data were obtained from the Healthcare Cost and Utilization Project Kids’ Inpatient Database, Agency for
Abhishek Deshpande Healthcare Research and Quality for the year 2009. The data were weighted to generate national-level
Department of Medicine, Medicine Institute, Cleveland estimates.
Clinic, Cleveland, OH, USA
For personal use only.

Mojtaba Olyaee Results:


Department of Medicine, Kansas University Medical There were 23,383 pediatric discharges with a diagnosis of GI bleeding accounting for 0.5% of all
Center, Kansas City, KS, USA discharges. Children with a GI bleed compared to those without were more likely to be male (54.5% vs.
45.8%; P50.001), older (children 11 years; 50.8% vs. 38.7%; P50.001), and admitted to a teaching
Michael P. Anderson hospital (70.5% vs. 56.4%; P50.001). Children 11–15 years of age had the highest incidence of GI
Department of Biostatistics and Epidemiology,
University of Oklahoma Health Sciences Center, bleeding (84.2 per 10,000 discharges) and children less than 1 year of age the lowest (24.4 per 10,000
Oklahoma City, OK, USA discharges). The highest incidence of GI bleeding was attributable to cases coded as blood in stool (17.6 per
10,000 discharges) followed by hematemesis (11.2 per 10,000 discharges). Those with a GI bleed had a
Thomas J. Sferra higher co-morbid burden (12.3% vs. 2.3%; P50.001) and severity of illness (40.1% vs. 14.5%;
Department of Pediatrics, Case Western Reserve P50.001). The highest mortality rates associated with GI bleeding were observed in cases with
University School of Medicine, UH Rainbow Babies &
intestinal perforation (8.7%) and esophageal perforation (8.4%). GI bleeding was independently
Children’s Hospital, Cleveland, OH, USA
associated with a higher risk of mortality (aOR 1.68, CI 1.53–1.84).

Address for correspondence: Conclusions:


Thomas J. Sferra MD, Martin and Betty Rosskamm
Our results describe the epidemiology of GI bleeding in hospitalized children within the United States. We
Chair in Pediatric Gastroenterology, Chief, Pediatric
found a substantial risk of mortality attributable to GI bleeding in this patient population. Our study is limited
Gastroenterology & Nutrition, Rainbow Babies and
Children’s Hospital, 11100 Euclid Avenue, Suite 737, by the exclusion of non-hospitalized children, the reliance on ICD-9-CM codes and the absence of
Cleveland, OH 44106, USA. longitudinal follow up of patients.
Tel: +1 216 844 1765;

thomas.sferra@uhhospitals.org
Background
Keywords: Gastrointestinal (GI) bleeding in a child is a common reason for referral to a
Adolescent – Child – Epidemiology – Gastrointestinal pediatric gastroenterologist1. Despite this, data regarding the epidemiology of GI
bleeding – Incidence – Outcomes – Pediatric bleeding in the pediatric population within North America are limited, consist-
Accepted: 14 January 2014; published online: 4 February 2014 ing of a few single-center studies many of which were published over 20 years
Citation: Curr Med Res Opin 2014; 30:1065–9
ago. Moreover, it is difficult to draw generalizable conclusions from these studies
as they differ in patient care setting, type of GI bleeding investigated, and overall
study objective. In a retrospective cohort study published in 1979 from a pedi-
atric tertiary referral center, hematemesis accounted for 0.2% of 316,020 emer-
gency department visits2. In 1994, Teach and Fleisher reported that of more than
40,000 visits to the Boston Children’s Emergency Department, 0.3% of children
had a presenting complaint of rectal bleeding3. In a 1992 prospective study,

! 2014 Informa UK Ltd www.cmrojournal.com GI bleeding in children Pant et al. 1065


Current Medical Research & Opinion Volume 30, Number 6 June 2014

63 (6.4%) upper GI bleeds were detected among 984 chil- states in the KID. We categorized patients into the follow-
dren admitted to a pediatric ICU over a 55 week period4. ing age groups: 51, 1–5, 6–10, 11–15, and 16–20 years of
Higher rates (up to 25%) of upper GI bleeding in children age. Normal, uncomplicated, in-hospital births were
also from the ICU setting have been reported in two smal- excluded from our study. Median household income was
ler prospective studies5,6. classified according to income quartiles (1st–4th) per
Currently, there are no large, multi-center studies that HCUP documentation based on patient residence.
have investigated the epidemiology of GI bleeding in chil- Insurance status was grouped into private, public
dren. Our objective was to define the recent incidence and (Medicaid/Medicare), and none (no pay, self-pay, or
associated mortality of GI bleeding in hospitalized chil- other). Hospital characteristics included teaching status
dren using a United States nationwide administrative (teaching versus non-teaching), location (urban versus
database. rural) and region (Northeast, Midwest, South, or West).
Severity of illness (minor, moderate, major, or extreme)
was categorized per the hospitalization’s All Patient
Materials and methods Refined Diagnosis-Related Group (APR-DRG) code8,9.
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The examined comorbid conditions consisted of the 29


Data source
disease states contained within the Elixhauser comorbidity
We used the 2009 Kids’ Inpatient Database (KID) for the index10. This is a widely used index in which higher scores
year 2009 for this study. The KID is part of the Healthcare indicate a greater comorbid disease burden11,12. We also
Cost and Utilization Project (HCUP) sponsored by the extracted patient information pertaining to in-hospital
United States Agency for Healthcare Research and mortality, hospital charges and hospital length of stay
Quality. Individual hospitalizations in which the patient (each of which is coded within the database). Data were
age is 20 or less at the time of admission are maintained in analyzed and are presented using weights provided in the
the KID as unique entries (the unit of observation is the KID to derive national level estimates.
inpatient stay record; individual patients cannot be
For personal use only.

tracked across multiple hospitalizations). Discharge Statistical methods


weights are provided to calculate national level estimates
for the extracted data. For 2009, the KID contains Statistical analyses were performed using SAS version 9.2
7,370,203 weighted pediatric discharges from 4121 com- (SAS institute, Cary, NC, USA). Categorical data are
munity hospitals (as defined by the American Hospital reported as frequencies and percentages and the chi-
Association; nonfederal, short-term general and specialty square test was used for comparing differences between
hospitals accessible by the general public) from 44 states. these variables. Rates of GI bleeding are reported as per
10,000 hospital discharges. The threshold for significance
for these analyses was P50.05. To assess the independent
Diagnoses and ICD-9-CM effect of GI bleeding on mortality a multiple variable logis-
We used the International Classification of Diseases, tic regression was performed with the presence or absence
Ninth Revision, Clinical Modification (ICD-9-CM) diag- of death as the dichotomous outcome variable. The mul-
nostic codes to identify GI bleeding in the KID. Our use of tiple variable logistic regression model was built by select-
ICD-9-CM codes were identical to, and the classification ing variables that had a logical association with mortality
of GI bleeding is based on, the methods of Zhao and (GI bleeding, demographics [age, sex, hospital region,
Encinosa7 who reported hospitalizations for GI bleeding location and teaching status, median household income,
in adults from the HCUP Nationwide Inpatient Sample and payer type], severity of illness categorized as per the
(NIS); the KID and NIS are from the same family of data- APR-DRG code and the comorbid burden determined by
bases. We categorized GI bleeding into three major classes: the Elixhauser scale). We felt that given the very large
upper GI bleeding, lower GI bleeding, and unspecified GI number of patients to number of variables under study,
bleeding. Unspecified GI bleeding is comprised of two dis- overfitting the model was not a problem. We tested all
tinct ICD-9-CM codes: 578.9 (hemorrhage of the GI tract; between-variable estimated correlation coefficients and
unspecified) and 578.1 (blood in stool). ICD-9-CM 578.1 determined that multicollinearity was not a problem.
can refer to hematochezia (generally lower GI bleeding) or Adjusted odds ratio (aOR) and 95% confidence intervals
melena (generally upper GI bleeding). (CIs) are reported.

Variables Results
Patient characteristics included age, gender, income, In 2009, there were 23,383 pediatric hospitalizations with
health insurance coverage, and comorbid conditions. a diagnosis of GI bleeding. Table 1 details the character-
Race was not included since it is not reported by all istics of these hospitalizations in comparison to those

1066 GI bleeding in children Pant et al. www.cmrojournal.com ! 2014 Informa UK Ltd


Current Medical Research & Opinion Volume 30, Number 6 June 2014

Table 1. Characteristics of cases with and without a discharge diagnosis of Table 2. Comorbidity burden, severity of disease, and outcome measures
gastrointestinal bleedinga. of cases with and without a discharge diagnosis of gastrointestinal
bleedinga.
Variableb GIB Without GIB
(n ¼ 23,383) (n ¼ 4,533,603) Variableb GIB Without GIB
(n ¼ 23,383) (n ¼ 4,533,603)
Age (median, IQR, years) 11 (15) 3 (17)
Age group (%) Elixhauser Comorbidity Score 1.1 (1.2) 0.4 (0.8)
51 year 18.9 39.8 (mean  SD)
1–5 years 18.6 14.0 Elixhauser Comorbidity Score
6–10 years 11.7 7.5 (% by score)
11–15 years 15.4 9.4 0 38.6 74.3
16–20 years 35.4 29.3 1 32.7 17.6
Sex (%) 2 16.4 5.9
Female 45.5 54.2 3 12.3 2.3
Male 54.5 45.8 Severity of illness (%)
Hospital setting (%) Minor 26.0 49.1
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Rural 7.1 11.2 Moderate 34.0 36.4


Urban 92.9 88.8 Major 23.5 11.8
Teaching status (%) Extreme 16.6 2.7
Teaching 70.5 56.4 LOS (median, IQR, days) 3 (5) 2 (2)
Non-teaching 29.5 43.6 Charges (median, IQR, $) 18,651 (39,654) 9461 (15,558)
Geographic region (%) Mortality (%) 2.8 0.6
Northeast 15.7 17.1
a
Midwest 23.2 21.5 All data are weighted to produce national estimates.
b
South 37.2 29.3 For each variable there are significant differences (P50.001) between
West 23.9 22.1 patients with and without GIB.
Household income (%) GIB, gastrointestinal bleed; IQR, interquartile range; LOS, length of stay;
1st quartile 29.0 32.7 SD, standard deviation.
2nd 25.6 26.1
3rd 23.9 22.7
For personal use only.

4th 21.4 18.5


Insurance status (%) Overall, children with a GI bleed during a hospitaliza-
Private 44.9 43.2 tion were sicker than the general hospitalized pediatric
Public 40.7 46.6
None 14.2 10.0 population (Table 2). Patients with GI bleeding had a
a
greater co-morbid burden (comorbidity score 3; 12.3%
All data are weighted to produce national estimates.
b
For each variable there are significant differences (P50.001) between vs. 2.3%; P50.001) and greater severity of illness as
patients with and without GIB. assessed by APR-DRG codes (major or extreme illness;
GIB, gastrointestinal bleed; IQR, interquartile range. 40.1% vs. 14.5%; P50.001). Children with GI bleeding
also had longer median hospital stays (3 days vs. 2 days;
without GI bleeding. Overall, children with GI bleeding P50.001), greater median hospital charges ($18,651 vs.
differed significantly from those without. Those with a GI $9461; P50.001), and higher overall mortality (2.8% vs.
bleed were older (median age 11 versus 3 years; P50.001), 0.6%; P50.001) compared to children without GI bleed-
more likely to be male (54.5% vs. 45.8%, P50.001), and ing. Using a multiple variable logistic regression model
cared for in a teaching hospital (70.5% vs. 56.4%, that adjusted for demographic and comorbid conditions,
P50.001). The incidence of GI bleeding in hospitalized we determined that GI bleeding was independently
children was 51.3 per 10,000 hospitalizations (0.5% of all associated with a higher risk of mortality (aOR 1.68, CI
hospitalizations). Upper GI bleeding was over three times 1.53–1.84).
more frequent than lower GI bleeding (incidence, 22.2 vs. Table 3 describes the incidence of GI bleeding in chil-
6.8 per 10,000 hospitalizations). However, in the majority dren by anatomical site and the corresponding mortality.
of cases there was not a differentiation between upper The highest incidence of GI bleeding in the HCUP-KID
and lower (designated as unspecified, 24.0 per 100,000 was attributable to cases coded as blood in stool (17.6 per
hospitalizations). Although children 16–20 constituted 10,000 discharges) followed by hematemesis (11.2 per
the greatest overall percentage of GI bleeding (35.4%), 10,000 discharges). The highest mortality associated
children 11–15 years of age had the highest overall inci- with GI bleeding was observed in cases with intestinal
dence of GI bleeding (84.2 per 10,000 discharges) (8.7%) and esophageal perforation (8.4%). Children
while children age less than 1 year of age had the lowest with unspecified GI bleeding accounted for the highest
overall incidence (24.4 per 10,000 discharges). Upper GI overall incidence (24.0 per 10,000 discharges) followed
bleeding was more frequent than lower GI bleeding in all closely by cases of upper GI bleeding (22.2 per 10,000
age groups. This location of bleeding was identified in discharges) while the incidence of lower GI bleeding
31.7% of infants (51 year of age) and over 40% at all in children was substantially lower (6.8 per 10,000 dis-
other ages. charges). The mortality, however, was significantly

! 2014 Informa UK Ltd www.cmrojournal.com GI bleeding in children Pant et al. 1067


Current Medical Research & Opinion Volume 30, Number 6 June 2014

higher in children with lower GI bleeding compared to bleeding (84.2 per 10,000 discharges) while children age
bleeding from other sites (P50.001). less than 1 year had the lowest overall incidence (24.4 per
Table 4 describes the incidence of GI bleeding (upper, 10,000 discharges).
lower, unspecified, and overall) by age. Children aged
11–15 years had the highest overall incidence of GI
Discussion
Table 3. Incidence and associated mortality by type of GI bleeda.
In this study, we evaluated the epidemiology of GI bleed-
Type Total Incidence Mortality ing in hospitalized children in the United States. Our data
(per 10,000 (%) represents national-level estimates and is therefore free
discharges)
from single-center or regional-level biases. Our results
Location indicate that hospitalized children with GI bleeding were
All 23,383 51.3 2.8 more likely to be male, older and admitted to teaching
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Upper 10,107 22.2 2.0 hospitals and have more severe illness and a greater comor-
Lower 3106 6.8 4.0
Unspecified 10,927 24.0 3.4 bid burden compared to children without GI bleeding.
Diagnosis Previous studies have noted the association of upper GI
Blood in stool 8021 17.6 1.7 bleeding in children with male gender and the presence of
Hematemesis 5092 11.2 1.5
Unspecified 2978 6.5 7.8 concurrent of medical disorders2,13. The median length of
Rectal bleeding 1904 4.2 1.3 stay, the hospital costs and the mortality were significantly
Gastritis/duodenitis 1806 4.0 2.4 higher in the GI bleeding group. After performing multiple
Intestinal perforation 1155 2.5 8.7
Mallory–Weiss 1063 2.3 0.1 variable regression analysis, GI bleeding in hospitalized
Gastric ulcer 828 1.8 2.3 children remained an independent risk factor for mortal-
Duodenal ulcer 649 1.4 1.8 ity. The incidence of lower GI bleeding in hospitalized
Esophageal variceal 450 0.99 3.8
children was lower compared to the incidence of upper
For personal use only.

Esophageal perforation 275 0.60 8.4


Esophageal, other 153 0.34 4.6 and unspecified GI bleeding; however, the mortality was
Peptic ulcer, unspecified 97 0.21 3.1 higher in this group. National estimates suggest that in
Esophageal ulcer 86 0.19 0.0
Gastrojejunal ulcer 65 0.14 1.5 hospitalized adult patients, the incidence of lower GI
Angiodysplasia, intestine 30 0.07 3.3 bleeding is also lower compared to upper and unspecified
Angiodysplasia, stom/duod 25 0.05 0.0 GI bleeding; although the overall incidence of lower GI
Diverticular disease 20 0.04 0.0
bleeding is higher in adults, presumably due to a much
a
All data are weighted to produce national estimates. greater incidence of malignancy and diverticulosis7.

Table 4. Age-associated incidencea, percentage, and mortality by type of GI bleedb.

Age group (years)


All ages 51 1–5 6–10 11–15 16–20

All
Incidence 51.3 24.4 68.1 79.6 84.2 61.8
% across age groups 100 18.6 18.6 11.7 15.4 35.4
% within age group – 100.0 100.0 100.0 100.0 100.0
Mortality (%) 4.2 3.2 2.1 2.7 2.0
Upper
Incidence 22.1 7.7 29.6 34.5 36.4 30.2
% across age groups 100 13.9 18.7 11.8 15.5 40.2
% within age group – 31.7 43.4 43.4 43.2 49.0
Mortality (%) 4.2 2.3 0.9 2.5 1.1
Lower 6.8
Incidence 3.0 5.9 8.8 12.4 10.0
% across age groups 100 17.8 12.0 9.8 17.1 43.3
% within age group – 12.5 8.6 11.1 14.8 16.3
Mortality (%) 10.0 3.8 2.0 3.6 2.4
Unspecified
Incidence 24.0 14.3 35.0 38.7 38.5 23.5
% across age groups 100 23.6 20.4 12.2 15.1 28.8
% within age group – 58.5 51.3 48.6 45.7 38.1
Mortality (%) 3.2 4.0 3.2 2.7 3.4
a
Incidence is calculated as the number of cases per 10,000 discharges for each specified age group. All data are weighted to produce
national estimates.
b
All data are weighted to produce national estimates.

1068 GI bleeding in children Pant et al. www.cmrojournal.com ! 2014 Informa UK Ltd


Current Medical Research & Opinion Volume 30, Number 6 June 2014

When cases of GI bleeding were categorized by anatomical Transparency


site, children with blood in stool represented the highest
incidence followed by hematemesis. The highest mortality Declaration of funding
was observed in cases with gut perforation (intestinal or This study was not funded.
esophageal), which may be secondary to the subsequent
Declaration of financial/other relationships
development of peritonitis or sepsis. Age stratification of
C.P., S.S., A.D., M.O., M.P.A., and T.J.S. have disclosed
cases revealed that the incidence of GI bleeding was lowest that they have no significant relationships with or financial
in infants and highest in the 11–15 year age group, interests in any commercial companies related to this study or
although children in the 16–20 year age group accounted article.
for more than one-third of total GI bleeding cases. CMRO peer reviewers may have received honoraria for
A possible explanation for the age-related increase in GI their review work. The peer reviewers on this manuscript
bleeding is a co-incident increase in comorbid conditions have disclosed that they have no relevant financial relationships.
(e.g. portal hypertension) that directly lead to hemorrhage
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from the GI tract. Acknowledgments


Our study has several limitations. Our results pertain The authors acknowledge all of the HCUP Data Partners
to hospitalized children without accounting for those that contribute to HCUP (http://www.hcup-us.ahrq.gov/db/
who were assessed and discharged from the emergency datapartners.jsp).
department. The use of large data sets might show differ-
ences without clinical significance (e.g. the differences we
observed for geographic region, household income, and References
insurance status). Due to our reliance on ICD-9-CM 1. Wolfram WAL, Arensman RM, Bensard D, et al. Pediatric gastrointestinal
codes for this study, the number of upper and lower GI bleeding. Available at: http://emedicine.medscape.com/article/1955984-
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2. Cox K, Ament ME. Upper gastrointestinal bleeding in children and adoles-
unspecified GI bleed category (including blood in stool
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! 2014 Informa UK Ltd www.cmrojournal.com GI bleeding in children Pant et al. 1069

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