Published online July 2, 2007
PEDIATRICS
Vol. 120
No. 2
August 2007, pp.
e236-e243
(doi:10.1542/peds.2006-3268)
Trends in Hospitalizations of HIV-Infected Children and Adolescents in the United States: Analysis of Data From the 1994–2003 Nationwide Inpatient Sample
Athena P. Kourtis, MD, PhD, MPHa,b,
Pooja Bansil, MPHc,
Samuel F. Posner, PhDa,
Christopher Johnson, MSa and
Denise J. Jamieson, MD, MPHa
a Division of Reproductive Health, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
b Department of Obstetrics/Gynecology, Eastern Virginia Medical School, Norfolk, Virginia
c Contraceptive Research and Development Program, Arlington, Virginia
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ABSTRACT
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OBJECTIVE. The objective of this study was to describe trends in hospital use by HIV-infected children and adolescents in the United States in the 10 years from 1994 (before highly active antiretroviral therapy) to 2003 (widespread use of highly active antiretroviral therapy).
METHODS. Data from the Nationwide Inpatient Sample database were used. The most frequent diagnoses were evaluated by year, and trends in hospitalizations for selected diagnoses and procedures were examined by multivariate logistic regression.
RESULTS. In 2003, there were an estimated 3419 hospitalizations of HIV-infected children who were 18 years or younger, compared with 11785 such hospitalizations in 1994 (a 71% decrease). This decrease was more marked among infants and children who were younger than 5 years (94% for boys and 92% for girls) than among adolescents (decrease of 47% for boys and increase of 23% for girls 15–18 years of age). The inpatient fatality rate among HIV-infected children decreased from 5.0% in 1994 to 1.8% in 2003. The number of hospitalizations among HIV-infected children in the highly active antiretroviral therapy era decreased significantly compared with before highly active antiretroviral therapy (1994–1996) for Pneumocystis jiroveci, bacterial infection, or sepsis; fungal infection; encephalopathy; failure to thrive; and lymphocytic interstitial pneumonia. No significant change in the number of hospitalizations for Pneumococcus or cytomegalovirus was observed.
CONCLUSIONS. Dramatic decreases in the number of hospitalizations among HIV-infected children occurred since the advent of highly active antiretroviral therapy in the United States. However, this trend is not seen in hospitalizations of adolescents, particularly girls. Hospitalizations for several HIV-related conditions are less frequent in the highly active antiretroviral therapy era, but for certain other conditions, the hospitalization burden remains high.
Key Words: HIV • children • adolescents • hospitalizations • United States • Healthcare Cost and Utilization Project • diagnosis • trends
Abbreviations: HAART—highly active antiretroviral therapy • NIS—Nationwide Inpatient Sample • ICD-9-CM—International Classification of Diseases, Ninth Revision, Clinical Modification • FTT—failure to thrive • PCP—Pneumocystis jiroveci pneumonia
After the introduction of highly active antiretroviral therapy (HAART), the length and quality of life of HIV-infected individuals, including children, improved substantially.1–5 Consistent with these improvements, the number of HIV-related hospitalizations and the average length of hospital stay among HIV-infected patients declined.1–3,6,7 Some studies of adults suggested that hospitalization trends leveled off in recent years.4 Although some data on pediatric trends recently appeared, no national estimates of the effect of HAART on use of inpatient hospital services by US children and adolescents with HIV are published, although such estimates are important in this era of rapidly changing health care practices.
The purpose of this study was to describe trends in use of inpatient hospital services by children and adolescents with HIV infection in the United States during 1994–2003, which includes the year when widespread use of HAART began (1997).8 Specifically, we investigated shifts in the burden of pediatric HIV-related hospitalizations by gender, age group, and other demographic or hospital characteristics. We were particularly interested in trends of hospitalizations for specific HIV/AIDS-related conditions, whose incidence may have changed with the implementation of specific prophylactic regimens but most important with the introduction of HAART. Such trends, although perhaps recognized in clinical practice, are not described on a national scale and are important in determining progress, reassessing health care priorities, and monitoring for emerging problems.
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METHODS
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Description of the Databases
We obtained hospital discharge data from the Nationwide Inpatient Sample (NIS), part of the Health care Cost and Utilization Project family of research databases and software tools sponsored by the Agency for Healthcare Research and Quality in partnership with state data collection organizations to produce national estimates of inpatient care delivered in the United States.9
The NIS is the largest all-payer inpatient care database in the United States and includes patient demographic data, diagnostic and procedural data, and facility information. The NIS is a sample of 
20% of all US community hospitals as defined by the American Hospital Association. The American Hospital Association defines community hospitals as nonfederal, short-term (average length of stay <30 days) general and specialty hospitals whose facilities are open to the public. Hospitals are selected for the NIS on the basis of 5 characteristics: geographic region, ownership, location (rural or urban), teaching status, and bed size. The sampled hospitals retain all discharge data. The NIS has data on 7 million discharged inpatients from 1000 community hospitals; the data are weighted so that national trends can be estimated.
We analyzed NIS data from 1994 to 2003. Beginning in 1998, the NIS differs from previous years: as more states made their data available to the Healthcare Cost and Utilization Project, the sampling frame increased from 17 states in 1994 to 37 states in 2003. In addition, the NIS sample design changed to reflect better the cross-sectional population of the hospitals represented in the sample by excluding from the frame short-term rehabilitation hospitals, redefining stratification variables, changing the definition of discharges, and no longer giving sampling preference to previous-year NIS hospitals. To account for these changes in our analysis, we used an alternative set of NIS discharge and hospital weights, recalculated on the basis of the 1998 sampling design, for the 1994–1997 NIS data sets.9,10 This research involved already collected and deidentified data and was reviewed and determined exempt.
Study Design and Statistical Analysis
Data from children and adolescents who were 18 years and younger were included in our analysis; neonates who were hospitalized in the first month of life and hospitalizations for conditions related to pregnancy and delivery were excluded. Hospital discharge diagnoses and procedures were coded in accordance with the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) and the Clinical Classifications Software tool, developed by the Agency for Healthcare Research and Quality, for clustering ICD-9-CM patient diagnoses and procedures into a manageable number of clinically meaningful categories.11,12 These codes can be found in the Appendix.
Data on hospitalized patients were examined by sociodemographic and hospital characteristics, including gender, age group (0–4 years, 5–9 years, 10–14 years, and 15–18 years), expected primary payer (public [Medicare/Medicaid] or nonpublic [private, self-pay, other]), location (urban or rural), and hospital region (Northeast, Midwest, South, or West). 
2 tests with a significance level of 0.05 were used to assess differences in the hospitalization characteristics of children and adolescents with and without HIV. The average length of hospital stay, charges associated with the hospitalizations (adjusted for inflation), and the number of diagnoses and procedures per hospitalization were also examined and compared by HIV infection status by using Student's t test in the 2 groups. Multivariate logistic regression was used to estimate odds ratios for hospitalizations of select (most frequent, clinically important, or HIV specific) diagnoses and procedures in the era of widespread HAART (2001–2003), compared with the pre-HAART period (1994–1996), adjusting for gender and age group (0–9 years and 10–18 years). Hospital charges were adjusted to 1994 dollars to account for inflation. All statistical analyses were conducted using SUDAAN software (Research Triangle Institute, Research Triangle Park, NC) by using survey methods that adjusted for sampling weights. Programming and data results were confirmed by 2 independent researchers.
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RESULTS
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General Trends in Hospitalizations of HIV-Infected Children and Adolescents
We estimated that there were 3419 pediatric and adolescent hospital discharges with an HIV diagnosis in the United States in 2003 compared with 11785 in 1994 (a 71% decrease; Table 1). In both 1994 and 2003, HIV-infected children had longer mean hospital stays than those who were not infected with HIV (1994: 10.1 vs 4.8 days [P < .001]; 2003: 8.1 vs 3.7 days [P < .001]), higher mean hospital charges per hospitalization (1994: $21216 vs $8465 [P < .001]; 2003: $32495 vs $14159 [P < .001]), and higher mean number of diagnoses (1994: 5.6 vs 2.9 [P < .001]; 2003: 4.7 vs 3.0 [P < .001]) and procedures (1994: 1.80 vs 0.93 [P = .003]; 2003: 1.18 vs 0.80 [P < .001]) per hospitalization.
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TABLE 1 Hospitalizations Among US Children and Adolescents With and Without HIV in 1994 and 2003, According to Particular Patient or Hospital Characteristics
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Infants and children who were younger than 5 years accounted for a progressively lower proportion of all hospitalizations of HIV-infected children, from 61% in 1994 to 17% in 2003 (Table 1). In contrast, children and adolescents who were aged 10 to 18 years accounted for a progressively higher proportion of all hospitalizations of the HIV-infected population (from 18% in 1994 to 62% in 2003). Of interest, whereas the number of hospitalizations of HIV-infected children who were younger than 5 years consistently and markedly decreased from 1994 to 2003 (a decrease of 94% for boys and 92% for girls), a differential pattern by gender appears among adolescents: the number of hospitalizations of boys 15 to 18 years of age has decreased by 47% (from 587 in 1994 to 311 in 2003), but the number of hospitalizations of girls 15 to 18 years of age has increased by 23% (from 469 in 1994 to 578 in 2003; Fig 1).
Throughout the 10-year period, most HIV-infected pediatric patients had Medicaid or Medicare as their expected payer and were hospitalized almost exclusively in urban areas (Table 1). The southern United States had the highest burden (approximately half) of all HIV pediatric hospitalizations (Table 1). After adjustment for inflation from 1994 to 2003, the mean hospital charges for both HIV-infected and noninfected children increased to a similar extent (by 27% and 26%, respectively).13 From 1994 to 2003, the mean length of hospitalizations decreased for both HIV-infected and noninfected children (Table 1). Throughout the period, inpatient fatality was higher among children who were hospitalized with HIV than among those without HIV (Table 1). However, from 1994 to 2003, the mean inpatient fatality decreased 62% for HIV-infected children and adolescents and decreased 27% for those who were not infected by HIV; both decreases were statistically significant. The decrease in inpatient deaths of HIV-infected children was more marked for children who were younger than 10 years (95.3% decrease) than it was for adolescents who were 10 to 18 years of age (63.8% decrease).
Most Frequent Diagnoses and Trends in Selected AIDS-Related Conditions
In 1994, the most frequent ICD-9-CM diagnostic codes among hospitalizations of children with an HIV diagnosis code were oral candidiasis, pneumonia, anemia, and failure to thrive (FTT; Table 2). In 2003, the respective codes, in order of frequency, were pneumonia, oral candidiasis, volume depletion, and asthma. These were followed by noncompliance with medical treatment. It is interesting that asthma and volume depletion, 2 diagnostic codes that consistently are seen among the most frequent causes for hospitalization of non–HIV-infected children, also appear in 2003 among the most frequent diagnoses of HIV-infected children, exceeding anemia and FTT. This reflects a trend toward normalization of the hospitalization pattern of HIV-infected children (Table 2). Of interest, depression and adjustment disorders were coded in 9.3% of all HIV-related hospitalizations in 2003, compared with 1.3% in 1994. With regard to procedures, bronchial biopsy, infusion of substances other than antibiotics and chemotherapy, hemodialysis and esophagogastroduodenoscopy were more frequent among hospitalizations of HIV-infected children than among those of non–HIV-infected ones (data not shown).
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TABLE 2 Five Most Common Hospital Discharge Diagnoses Among Children and Adolescents With and Without HIV: United States, 1994 and 2003
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Compared with the pre-HAART era (1994–1996), the era of widespread HAART use (2001–2003) had a significant decrease in hospitalizations of HIV-infected pediatric patients with diagnoses that included Pneumocystis jiroveci pneumonia (PCP), bacterial infections or sepsis, mycoses, encephalopathy, FTT, infections caused by Mycobacterium avium complex, and lymphocytic interstitial pneumonia, after adjustment for gender and age group (Table 3 and Fig 2). The number of hospitalizations of HIV-infected children with a diagnosis of cytomegalovirus or pneumococcal disease did not change significantly over time; indeed, there was a slight upward trend in the diagnosis of pneumococcal disease (Table 3). There was a marked increase in coding for noncompliance with medical care in the era of HAART, compared with pre-HAART, among HIV-infected patients (Table 3), a finding also seen among patients without HIV, although not as pronounced (odds ratio: 2.18; 95% confidence interval: 1.89–2.52). Depression and adjustment disorders were more frequently coded for children both with HIV (Table 3) and without HIV (data not shown). As for procedures, antibiotic injections, diagnostic spinal taps, and transfusions of packed red blood cells were significantly less likely to be administered to HIV-infected patients in the HAART era than in the pre-HAART era (Table 3). Over time, the number of percutaneous gastrostomy procedures increased among HIV-infected children who were hospitalized (Table 3).
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TABLE 3 Trends in Hospitalizations With Particular Conditions and Procedures and Inpatient Deaths Among HIV-Infected Children and Adolescents in the United States in the HAART (2001–2003) and pre-HAART (1994–1996) Eras
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FIGURE 2 Number of pediatric hospitalizations for selected HIV-related conditions: United States, 1994–2003.
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DISCUSSION
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The Centers for Disease Control and Prevention reported that 5400 US children and adolescents younger than 19 years were living with AIDS in 2000.14 Although the annual number of infants who are infected with HIV perinatally has been decreasing, the annual number of adolescents who are infected with HIV has been increasing.14 This increase in the rate of new HIV infections among adolescents is particularly pronounced among black and Hispanic adolescents and girls of all racial or ethnic groups.14,15 Despite the increase of HIV infections among adolescents, the number of AIDS cases and HIV-related deaths has been declining, largely because of the use of combination antiretroviral drug regimens.1,3,5,14
A recent report from the United Kingdom and Ireland demonstrated that pediatric hospital admissions and mortality among HIV-infected children declined by 80% since the introduction of 3- or 4-drug combination therapy in 1997.16 However, given the increased number of HIV-infected children in follow-up, the absolute number of hospitalizations fell by only 26%. Most reductions occurred in 1997–1999, and rates seemed to stabilize between 2000 and 2002. Similar decreases in hospitalizations after the introduction of HAART were demonstrated in a small pilot study in Italy6 and in a study in Spain7; specific causes for hospitalizations were not reported. Two recent reports from 2 US multicenter cohorts demonstrated substantial downward trends in hospitalizations, multiple hospitalizations, and intensive care admissions and a decrease in opportunistic infections among HIV-infected children since the advent of HAART.17,18 Despite decreases in hospitalizations, lifetime treatment costs for HIV-infected children remain relatively stable, a result of increasing drug costs and greater life expectancy.8 Some researchers suggest that shifts in patterns of hospital admission of HIV-infected adults have emerged.19
Results of a recent study of 129 children who were followed at 3 HIV clinics in California showed that the rate of HIV-related deaths, the hospitalization rate, and the average length of hospital stays among perinatally infected children decreased significantly between 1994 and 2001,20 a period when the use of HAART was increasing. They also showed that pneumonia and sepsis were the main causes of hospitalization among these children from 1994 through 1999 but that the rate of hospitalizations for these conditions decreased in 2000–2001.20 In a study of adult HIV-infected patients, bacterial pneumonia followed by PCP were the leading causes of hospitalization, with decreases over time.21 The problem of psychiatric disease among HIV-infected children was recently highlighted when results from the Pediatric AIDS Collaborative Trials Study cohort of 1808 HIV-infected children who were younger than 15 years and followed for 3 years showed them to have a greater risk for psychiatric hospitalization than noninfected children of the same age.22
Similar to other studies, we found a marked decrease in the number of hospitalizations among HIV-infected children who were younger than 19 years in the United States from 1994 to 2003. This decrease is most profound for infants and young children; the number of hospitalizations for adolescents has not decreased. In particular, the number of hospitalizations among adolescent girls actually increased. These findings might reflect a combination of an alarming increase in the number of newly acquired HIV infections among adolescents and a welcome increase in the survival of perinatally infected children in the United States.23 The number of hospitalizations as a result of bacterial and fungal infections decreased, probably an effect of better immune function as a result of HAART. HIV encephalopathy has also significantly decreased, as has FTT and lymphocytic interstitial pneumonia, among HIV-infected hospitalized children. The number of hospitalizations among children with a diagnosis of PCP significantly decreased in all age groups. However, continued vigilance in HIV testing for all women in pregnancy and labor should continue so that perinatally acquired cases of HIV in children are not missed. The number of hospitalizations among children with a diagnosis of Mycobacterium avium complex decreased, probably because of both decreased immunosuppression as a result of HAART and increased availability of prophylaxis. Of interest also is the downward trend (albeit not statistically significant) in hospitalizations among children with varicella zoster infection after the introduction of the varicella vaccine in 1995 (this vaccine is indicated for all but the most severely immunocompromised HIV-infected children).24 The decrease in hospitalizations for these conditions among children with HIV was not as pronounced as it was for children without HIV (data not shown), no doubt reflecting the persistent burden of varicella zoster infections among the most severely immunocompromised HIV-infected patients. In contrast, hospitalizations for pneumococcal disease among HIV-infected children actually show an upward trend, underlining a persistent problem in the health care of these children. It will be interesting to follow this trend in time to evaluate what effect the conjugate pneumococcal vaccine, licensed in 2000, will have on invasive pneumococcal disease of HIV-infected children. Similarly, hospitalizations of children with a diagnosis of cytomegalovirus have not changed over time, perhaps reflecting the plateau in the number of hospitalizations of HIV-infected adolescents, in whom cytomegalovirus is more frequent. Noncompliance with medical care among HIV-infected children is coded much more frequently in the HAART era than in the pre-HAART era. Depression and adjustment disorders are also coded much more frequently in the HAART era among HIV-infected children and adolescents, but a similar increase is observed among children without HIV.
To our knowledge, our study is the first to produce national estimates of trends in hospital use by US children and adolescents with HIV and the first to describe trends in specific diseases and opportunistic infections among pediatric HIV patients through the introduction of HAART.
Our study has some limitations, mainly because of its reliance on hospital discharge data for which accuracy depends on the quality and consistency of coding by participating hospitals. We were unable to analyze hospitalization data by principal discharge diagnosis, which would more accurately reflect the main reason for the hospitalization, because HIV infection itself was the primary diagnosis in approximately third of the hospitalizations that involved HIV-infected children,25 probably reflecting nonuniform coding practices. Instead, we analyzed data by all discharge diagnoses, which reflect coexisting conditions that may not always have led to the hospitalization but nevertheless show the complex morbidities that afflict children with HIV infection. Another limitation of this study is that because the data that we used were for discharges rather than for individual patients, data on some children were represented more than once for any given year. Furthermore, given that HIV testing is not universal, some HIV-infected children might have been missed if they were hospitalized for an unrelated cause. Underreporting of procedures, particularly nonoperative ones, such as administration of antibiotics, probably occurs. Because of incomplete data on race in NIS, we were unable to evaluate the effect of race. Other changes in health care and in coding practices during the 10-year study period (eg, increased availability and use of outpatient services for selected conditions and procedures and better recognition of certain conditions) might have influenced our findings to some extent. These limitations notwithstanding, this nationwide look at trends in hospital use and in specific AIDS-related conditions among HIV-infected children and adolescents in the United States after widespread use of HAART provides data that can be used to (1) examine our progress, (2) assess the health care needs of specific groups (eg, adolescents) and for specific conditions (eg, pneumococcus or cytomegalovirus, where progress has not been as fast, and psychiatric diagnoses, which seem to be rising), and (3) define future policies in an era of competing health care priorities.
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APPENDIX Appropriate Diagnoses and Procedure Codes for Hospitalizations Among Children and Adolescents with HIV Infection in the United States
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ACKNOWLEDGMENTS
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We thank Dr Marc Bulterys for reading the manuscript and providing helpful comments.
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FOOTNOTES
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Accepted Jan 26, 2007.
Address correspondence to Athena Kourtis, MD, PHD, MPH, CDC-DRH/NCCDPHP, K34, Koger Center, Columbia Building 2900, Woodcock Blvd, Atlanta, GA 30341. E-mail: apk3{at}cdc.gov
The authors have indicated they have no financial relationships relevant to this article to disclose.
The views expressed in this article are those of the authors and do not necessarily reflect those of the Centers for Disease Control and Prevention.
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PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics
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ABSTRACT
METHODS
