National Hospitalization Trends for Pediatric Pneumonia and Associated Complications Grace E. Lee, Scott A.

Lorch, Seth Sheffler-Collins, Matthew P. Kronman and Samir S. Shah Pediatrics 2010;126;204-213; originally published online Jul 19, 2010; DOI: 10.1542/peds.2009-3109

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://www.pediatrics.org/cgi/content/full/126/2/204

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2010 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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National Hospitalization Trends for Pediatric Pneumonia and Associated Complications

WHATS KNOWN ON THIS SUBJECT: The incidence of IPD has decreased since widespread use of PCV7. Postlicensure epidemiological studies revealed conicting data about changes in CAP and CAP-associated complications. Previous studies focused on empyema and typically did not include school-aged children or adolescents. WHAT THIS STUDY ADDS: With nationally representative data, we found that rates of CAP discharges remained relatively unchanged overall. Systemic complication rates were greatest for infants. Local complication rates increased in all age groups and were highest among 1- to 5-year-old children.
AUTHORS: Grace E. Lee, MD,a,b,c Scott A. Lorch, MD, MSCE,c,d,e,f Seth Shefer-Collins, MPH,b Matthew P. Kronman, MD,b,f and Samir S. Shah, MD, MSCEa,b,c,e,f
Divisions of aGeneral Pediatrics, bInfectious Diseases, and dNeonataology, Childrens Hospital of Philadelphia, Philadelphia, Pennsylvania; and Departments ofcPediatrics and eBiostatistics and Epidemiology and fCenter for Clinical Epidemiology and Biostatistics, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania KEY WORDS pneumonia, pleural empyema, epidemiology, heptavalent pneumococcal conjugate vaccine ABBREVIATIONS CAP community-acquired pneumonia PCV7 heptavalent pneumococcal conjugate vaccine PPV2323-valent polysaccharide pneumococcal vaccine IPDinvasive pneumococcal disease KIDKids Inpatient Database ICD-9-CMInternational Classication of Diseases, Ninth Revision, Clinical Modication CI condence interval The content of this article is solely the responsibility of the authors and does not necessarily represent the ofcial views of the National Institutes of Health. www.pediatrics.org/cgi/doi/10.1542/peds.2009-3109 doi:10.1542/peds.2009-3109 Accepted for publication May 11, 2010 Address correspondence to Samir S. Shah, MD, MSCE, Childrens Hospital of Philadelphia, Division of Infectious Diseases, Room 1526, North Campus, 34th Street and Civic Center Boulevard, Philadelphia, PA 19104. E-mail: shahs@email.chop.edu PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright 2010 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no nancial relationships relevant to this article to disclose. Funded by the National Institutes of Health (NIH).

abstract
OBJECTIVE: To determine current rates of and trends in hospitalizations for community-acquired pneumonia (CAP) and CAP-associated complications among children. METHODS: We performed a cross-sectional, retrospective, cohort study by using the 1997, 2000, 2003, and 2006 Kids Inpatient Database. National estimates for CAP and CAP-associated local and systemic complication rates were calculated for children 18 years of age. Patients with comorbid conditions or in-hospital birth status were excluded. Percentage changes were calculated by using 1997 (before heptavalent pneumococcal conjugate vaccine [PCV7]) and 2006 (after PCV7) data. RESULTS: There were a total of 619 102 CAP discharges for 1997, 2000, 2003, and 2006, after application of inclusion and exclusion criteria. Overall rates of CAP discharges did not change substantially between 1997 and 2006, but stratication according to age revealed a 22% decrease for children 1 year of age, minimal change for children 1 to 5 years of age, and increases for children 6 to 12 years (22%) and 13 years (41%) of age. Systemic complication rates were highest among children 1 year of age but decreased by 36%. In all other age groups, systemic complication rates remained stable. Local complication rates increased 78% overall. Children 1 to 5 years of age had the highest local complication rates. CONCLUSIONS: After the introduction of PCV7 in 2000, rates of CAPassociated systemic complications decreased only for children 1 year of age. Rates of pediatric CAP-associated local complications are increasing in all age groups. Pediatrics 2010;126:204213

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Streptococcus pneumoniae is the most-commonly identied bacterial cause of community-acquired pneumonia (CAP) in children. A heptavalent pneumococcal conjugate vaccine (PCV7) was licensed in the United States in February 2000 and subsequently was added to the routine childhood vaccination schedule. Since then, overall rates of invasive pneumococcal disease (IPD) (ie, bacteremia and meningitis) have decreased for both children17 and adults,810 largely because of signicant reductions in the burden of disease caused by vaccine serotype isolates. However, reductions in the incidence of pediatric CAP seem to be less dramatic and have been limited to young children. In prelicensure, randomized, controlled trials, the risk of radiographically conrmed pneumonia was 20% lower for PCV7 recipients 2 years of age, compared with nonrecipients.11 Postlicensure epidemiological studies revealed decreases in all-cause pneumonia incidence rates of 39% to 52% among children 2 years of age12,13 but no changes for older children.13,14 The impact of PCV7 vaccination on the severity of pediatric CAP is less clear. Although vaccination with PCV7 has reduced the incidence of IPD in children, several authors reported regional increases in rates of pediatric empyema, a CAP-associated complication, after widespread PCV7 uptake.1517 Studies examining national trends in pneumonia-associated complications also focused solely on empyema18,19 and were limited to infants and preschool-aged children.18 Among adults hospitalized with CAP, previous recipients of a 23-valent polysaccharide pneumococcal vaccine (PPV23) had lower all-cause mortality rates and risks of respiratory failure, sepsis syndrome, and cardiac arrest, compared with vaccine nonrecipients.20 To our knowledge, there have been no
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studies evaluating the impact of PCV7 introduction on the severity of illness in children hospitalized with CAP. We conducted a retrospective crosssectional study by using a national database to determine the rates of hospitalizations with CAP and CAPassociated complications in otherwise healthy children in the United States and to describe changes in rates, if any, after the introduction of PCV7.

talization because of CAP in 1997, 2000, 2003, or 2006. Denition of Pneumonia By using a previously validated algorithm, patients were considered to have CAP if they met 1 of 2 criteria, that is, (1) an International Classication of Diseases, Ninth Revision, Clinical Modication (ICD-9-CM), primary diagnosis code indicating pneumonia (codes 480 483 and 485 486), empyema (code 510), or pleurisy (codes 511.0, 511.1, and 511.9) or (2) a primary diagnosis of a pneumonia-related symptom (eg, cough, fever, or tachypnea) (see Appendix 1 for ICD-9-CM codes) and a secondary diagnosis of pneumonia, empyema, or pleurisy.22 Exclusion Criteria Patients with the following comorbid conditions were excluded, because these comorbidities are characterized by risk factors not reective of the general pediatric population: acquired or congenital immunologic disorders, malignancies, collagen vascular disease, sickle cell disease, cystic brosis, organ transplant, congenital heart defects, and heart failure (Appendix 1). Cases identied as in-hospital births were excluded, to minimize the inclusion of perinatally acquired and neonatal nosocomial infections. Patients with a secondary diagnosis code indicating trauma also were excluded, because a diagnosis of pneumonia in this population likely reects a nosocomial cause (Appendix 1). CAP-associated complications were identied by using ICD-9-CM diagnosis and procedure codes (Appendix 2). Complications were classied as local (empyema, lung abscess, necrotizing pneumonia, or bronchopleural stula), systemic (acute respiratory failure, sepsis, extracorporeal membrane oxygenation, or hemolytic uremic syndrome), or metastatic (meningitis, central nervous system abscess, mastoiditis,
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METHODS
Study Design and Data Source We performed a cross-sectional analysis of pediatric hospitalizations in the United States by using the 1997, 2000, 2003, and 2006 Kids Inpatient Database (KID). The KID is part of the Healthcare Cost and Utilization Project sponsored by the Agency for Healthcare Research and Quality. It is the only data set on hospital use and outcomes that was designed specically to study childrens use of hospital services in the United States The KID samples pediatric discharges from all community nonrehabilitation hospitals (including academic medical centers) in states participating in the Healthcare Cost and Utilization Project, across pediatric discharge type and hospital characteristics, by using a complex stratication system. Discharge-level weights assigned to discharges within the stratum permit calculations of national estimates. Each data set contains 3 million discharges (unweighted), and data sets have been released every 3 years, beginning in 1997. The 2006 KID is the most-recent data set available and contains hospital administrative data from 38 states, representing 88.8% of the estimated US population.21 Study Participants Inclusion Criteria Patients 18 years of age were eligible for inclusion if they required hospi-

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TABLE 1 Characteristics of Patients With CAP Discharges in 19972006

Year 1997 (N Race White Black Other Missing data Age 1y 15 y 612 y 1318 y Male Died 148 702) 2000 (N n (%) 157 847) 2003 (N 157 743) 2006 (N 156 810)

56 348 (38) 22 864 (15) 22 203 (15) 47 287 (32) 43 851 (29) 75 033 (50) 19 372 (13) 10 446 (7) 83 291 (56) 334 (0.22)

68 643 (44) 22 580 (14) 38 448 (24) 28 175 (18) 44 470 (28) 76 385 (48) 21 403 (14) 15 589 (9) 87 891 (56) 394 (0.25)

54 903 (35) 17 960 (11) 39 138 (25) 45 588 (29) 37 798 (24) 77 530 (49) 23 126 (15) 19 289 (12) 86 034 (55) 270 (0.17)

56 108 (36) 18 800 (12) 40 803 (26) 41 099 (26) 37 705 (24) 79 519 (51) 23 494 (15) 16 092 (10) 85 508 (55) 193 (0.12)

(Stata Corp, College Station, TX). This study was considered exempt from the need for review by the institutional review board of the Childrens Hospital of Philadelphia.

RESULTS
Study Sample The 1997, 2000, 2003, and 2006 KID contained a total of 28 916 332 weighted pediatric discharges. Of those, 619 102 cases (2.1%) remained after inclusion and exclusion criteria for CAP were applied. Subject Characteristics Table 1 presents subject characteristics according to year. Age category proportions remained stable over time, with children 1 to 5 years of age representing the largest age group. There was a slight predominance of male participants in all years. White children composed the largest represented racial group (35% 44%) in all years; race data were missing for 18% to 32% of discharges. Mortality rates were low at 0.25% for all pediatric CAP discharges in each sample year. Rates of CAP Overall The rates of CAP discharges according to year are shown in Table 2. Overall rates of pediatric CAP discharges

pericarditis, endocarditis, osteomyelitis, or septic arthritis). Statistical Analyses Cases were characterized on the basis of age, race, gender, presence and type of complication, and discharge status (in-hospital death). Analyses were subsequently stratied according to age and race. Age groups were dened as 1 year (infant), 1 to 5 years (preschool age), 6 to 12 years (school age), or 13 years (adolescent), to capture differences in CAP and CAP-associated complication rates related to age-inuenced factors such as PCV7 vaccination status, CAP microbiologic cause, and age-based sociological factors. Race was recorded as a single variable (white, black, other, or missing data). Rate estimates for each race category were calculated; cases with missing

race data were included as a separate variable, to preserve the integrity of our estimates. Ratios of CAP discharge and CAP-associated complication rates for black and white study participants were calculated by using sameyear data. Categorical variable results were summarized as frequencies and proportions. Rate calculations were performed by using weighted observations as numerators and annual, age-specic population estimates obtained from the US Census Bureau as denominators.23 Point estimates with 95% condence intervals (CIs) were calculated by using Taylor series estimates. Percentage changes for CAP and CAP-associated complications were calculated by using 1997 (pre-PCV7 period) and 2006 (post-PCV7 period) rates. Calculations were performed by using Stata 10

TABLE 2 Rates of CAP and Associated Complications in 19972006

1997 CAP discharges, estimate (95% CI), cases per 100 000 Any complication Rate, estimate (95% CI), cases per 100 000 Proportion of CAP cases, % Local complications Rate, estimate (95% CI), cases per 100 000 Proportion of CAP cases, % Systemic complications Rate, estimate (95% CI), cases per 100 000 Proportion of CAP cases, % 199.1 (198.1200.1) 11.8 (11.612.1) 5.9 5.4 (5.25.6) 2.7 6.8 (6.67.0) 3.4 2000 207.6 (206.6208.6) 14.6 (14.314.8) 7.0 7.4 (7.27.6) 3.6 7.7 (7.57.9) 3.7 2003 204.3 (203.1205.3) 15.8 (15.315.8) 7.7 8.9 (8.69.0) 4.4 7.5 (7.37.7) 3.7 2006 201.2 (200.2202.2) 15.1 (14.815.3) 7.5 9.6 (9.49.9) 4.8 6.2 (6.06.3) 3.1 Change, 1997 vs 2006, % 1.1 28.0

77.8

8.8

Rates are reported as cases per 100 000 age-specic US population.

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TABLE 3 Rates of CAP in 19972006, Stratied According to Age

Age n (%) 1997 Rate, Estimate (95% CI), Cases per 100 000 n (%) 2000 Rate, Estimate (95% CI), Cases per 100 000 n (%) 2003 Rate, Estimate (95% CI), Cases per 100 000 n (%) Change, 1997 vs Rate, Estimate (95% 2006, % CI), Cases per 100 000 21.9 1.9 21.9 40.5 2006

1y 15 y 612 y 1318 y

43 851 (30) 1169.0 (1158.21179.9) 75 033 (50) 383.1 (380.3385.8) 19 372 (13) 69.3 (68.370.2) 10 446 (7) 44.7 (43.845.5)

44 691 (28) 1159.1 (1148.41169.8) 76 775 (48) 397.7 (394.9400.5) 21 531 (14) 74.1 (73.175.1) 15 663 (10) 64.7 (63.665.7)

37 798 (24) 937.6 (928.2947.0) 37 705 (24) 912.9 (903.8922.1) 77 530 (49) 395.6 (392.8398.4) 79 519 (51) 390.4 (387.7393.2) 23 126 (15) 80.9 (79.982.0) 23 494 (15) 84.5 (83.485.6) 19 289 (12) 77.1 (76.178.2) 16 092 (10) 62.8 (61.963.8)

Rates are reported as cases per 100 000 age-specic US population.

peaked in 2000 and then returned to pre-PCV7 levels. According to Age The rates of CAP discharges varied inversely with age, with the highest rates occurring for children 1 year of age. The rates of CAP discharges for children 1 year of age decreased by 21.9% between 1997 and 2006, with 90% of the decrease occurring by 2003. There were minimal interval changes in rates of CAP discharges for children 1 to 5 years of age, whereas rates increased by 21.9% for children 6 to 12 years of age and by 40.5% for children 13 years of age (Table 3).

According to Race Rates of CAP discharges for black children were greater than those for white children in all years studied (Table 4). However, this difference decreased over time, from a rate ratio of 1.98 in 1997 to a rate ratio of 1.59 in 2006. Rates of CAP-Associated Complications Overall Between 1997 and 2006, the rate of discharges with any CAP-associated complication increased by 28% (11.8 and 15.1 cases per 100 000 population, respectively), whereas the rate of local

complications increased by 77.8% (5.4 and 9.6 cases per 100 000 population, respectively). Empyema accounted for 97% of all local complications. The systemic complication rate decreased by 8.8% (6.8 and 6.2 cases per 100 000, respectively) (Table 2). The proportion of discharges with any associated complication increased from 5.9% to 7.5%, whereas the proportion with local complications increased from 2.7% to 4.8%. The proportion with systemic complications remained relatively stable at 3.1% to 3.7%. In 1997, 2000, 2003, and 2006, there were an estimated 75, 100, 72, and 98 discharges, respec-

TABLE 4 Rates and Rate Ratios of CAP and CAP-Associated Complications in 19972006, Stratied According to Race
Year n (%) 1997 Rate, Estimate (95% CI), Cases per 100 000 n (%) 2000 Rate, Estimate (95% CI), Cases per 100 000 n (%) 2003 Rate, Estimate (95% CI), Cases per 100 000 n (%) 2006 Change, 1997 vs Rate, Estimate (95% 2006, % CI), Cases per 100 000 3.4 22.3

CAP White Black Black/white rate ratio Any complication White Black Black/white rate ratio Local complications White Black Black/white rate ratio Systemic complications White Black Black/white rate ratio

56 348 (38) 96.0 (95.296.8) 68 975 (43) 115.5 (114.7116.4) 54 903 (35) 91.3 (90.592.1) 56 108 (36) 92.7 (92.093.5) 22 864 (15) 190.0 (187.5192.5) 22 694 (14) 182.6 (180.3185.0) 17 960 (11) 142.6 (140.6144.7) 18 800 (12) 147.6 (145.5149.8) 1.98 (1.942.01) 1.58 (1.561.60) 1.56 (1.541.59) 1.59 (1.561.62)

3567 (40) 1108 (13)

6.1 (5.96.3) 9.2 (8.79.8) 1.51 (1.421.62)

4757 (43) 8.0 (7.78.2) 1394 (13) 11.2 (10.611.8) 1.40 (1.331.49)

4578 (38) 1207 (10)

7.6 (7.47.8) 9.6 (9.110.1) 1.26 (1.181.34)

4609 (39) 7.6 (7.47.8) 1356 (12) 10.7 (10.111.2) 1.40 (1.311.49)

24.6 16.3

1831 (46) 491 (12)

3.1 (3.03.3) 4.1 (3.74.5) 1.32 (1.181.45)

2771 (49) 719 (13)

4.6 (4.54.8) 5.8 (5.46.2) 1.26 (1.151.35)

2839 (42) 714 (11)

4.7 (4.64.9) 5.7 (5.36.1) 1.21 (1.111.30)

3100 (41) 871 (12)

5.1 (4.95.3) 6.8 (6.47.3) 1.33 (1.241.44)

64.5 65.9

1854 (37) 650 (13)

3.2 (3.03.3) 5.4 (5.05.8) 1.69 (1.561.87)

2175 (37) 730 (12)

3.6 (3.53.8) 5.9 (5.56.3) 1.61 (1.481.75)

1959 (34) 553 (10)

3.3 (3.13.4) 4.4 (4.04.8) 1.35 (1.221.48)

1750 (36) 559 (12)

2.9 (2.83.0) 4.4 (4.04.8) 1.52 (1.381.67)

9.4 18.5

Rates are reported as cases per 100 000 US population

18 years of age.

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tively, with CAP-associated metastatic complications. There were so few metastatic complications as to preclude us from presenting meaningful rates or subset analyses. According to Age Between 1997 and 2006, rates of any CAP-associated complication among children 1 year of age decreased (Fig 1A), whereas rates in all other age groups increased (Fig 1 BD). The rate of any CAP-associated complication was highest at each time point for children 1 year of age; however, this group experienced a 25.5% decrease between 1997 and 2006 (from 54.9 to 40.9 cases per 100 000). Among children 1 to 5 years of age, the rate of any

complication increased 31.5%, from 19.7 to 25.9 cases per 100 000. Among children 6 to 12 years of age, the rate of any complication increased 44.4%, from 5.4 to 7.8 cases per 100 000. Children 13 years of age had the largest percentage rate increase, with a 67.2% increase between 1997 and 2006 (from 6.1 to 10.2 cases per 100 000). Rates of CAP-associated systemic complications were highest among children 1 year of age in all years studied, whereas the lowest rates occurred among children 6 to 12 years of age. Between 1997 and 2006, rates of systemic complications in children 1 year of age decreased from 49.0 to 31.6 cases per 100 000, representing a

35.5% decrease. Rates remained stable among the other age groups. Rates of CAP-associated local complications increased in all age groups. Although rates of local complications were highest among children 1 to 5 years of age for all years studied, children 13 years of age had the largest percentage increase in rates over time. Among children 1 year of age, rates increased 67.2%, from 6.7 to 11.2 cases per 100 000 (Fig 1A). Among children 1 to 5 years of age, rates increased 79.3%, from 9.2 to 16.5 cases per 100 000 (Fig 1B). Among children 6 to 12 years of age, rates increased 71.4%, from 3.5 to 6.0 cases per 100 000 (Fig 1C). Children 13 years of

FIGURE 1
Rates of hospital discharges for CAP-associated complications in 19972006, stratied according to age. A, 1 year; B, 1 to 5 years; C, 6 to 12 years; D, 13 to 18 years. Open circles indicate any complication, black squares indicate systemic complications, and black circles indicate local complications. Vertical lines indicate 95% CIs. Rates are cases per 100 000 age-specic US population.

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age experienced an 88.1% increase in rates between 1997 and 2006 (from 4.2 to 7.9 cases per 100 000) (Fig 1D). According to Race Rates of any, systemic, and local CAPassociated complications were higher for black children than for white children for all years studied (Table 4). Ratios of rates for black and white children for any, systemic, and local complications showed a downward trend between 1997 and 2003, with a slight increase from 2003 to 2006. Between 1997 and 2006, rates of any CAPassociated complication increased 24.6% for white children and 16.3% for black children. Systemic complication rates decreased 18.5% for black children and 9.4% for white children. The groups experienced similar increases in rates of local complications (64.5% and 65.9% for white and black children, respectively).

associated complications than did white children in all years studied. Although CAP-related hospitalization rates for the entire cohort were stable overall, there were differences according to age group. Infants were the only age group to experience a decrease in CAP discharge rates, a nding consistent with other studies that showed post-PCV7 reductions in all-cause pneumonia rates for children 2 years of age.1113,25 Although previous postlicensure studies did not show CAP rate changes for children 2 years of age,13,14 we report that CAP discharge rates increased for children 5 years of age. We might have been able to nd a difference in rates for the older age groups because of the larger size of our cohort, compared with previous studies.13,14 However, the reason for the increase in CAP discharges is unclear. Pneumococcal serotype replacement has been occurring since the introduction of PCV71,57,15 and may contribute to the increase in CAP discharge rates for older children, although data suggest that serotype replacement is more commonly seen among young children and older adults.5,6,15 It also is possible that changes in the epidemiological features of other pathogens, such as methicillin-resistant Staphylococcus aureus26,27 or atypical organisms, rather than changes in rates of IPD, are responsible for this trend. This is the rst national study to examine rates of systemic CAP-associated complications in the pre-PCV7 and post-PCV7 eras. Rates of systemic complications varied inversely with age, with infants having the highest rates and children 6 years of age having the lowest rates. The decrease in systemic complication rates for the entire cohort was largely attributable to the decrease in rates for infants and might be explained in part by the fact that infants have been the primary recipi-

DISCUSSION
We describe national changes in discharge rates for pediatric CAP and CAP-associated complications in the pre-PCV7 and post-PCV7 periods. Since the introduction of PCV7 in 2000, uptake has been rapid, with 68% of 19- to 35-month-old children having received 3 doses in 2003 and 87% in 2006.24 We report that, although overall rates of CAP discharges remained relatively unchanged, rates decreased for children 1 year of age and increased for children 6 years of age. Overall rates of systemic complications were dramatically higher for infants than for any other age group, but infants were the only age group to experience decreases over time in this area. In contrast, local complication rates were found to be increasing in all pediatric age groups and were highest among children 1 to 5 years of age. Race seemed to play a role, because black children had consistently higher discharge rates of CAP and CAPPEDIATRICS Volume 126, Number 2, August 2010

ents of PCV7.28 Adult data suggest that pneumococcal vaccination can modify the severity of illness for patients hospitalized with CAP and may reduce the occurrence of CAP-associated complications.20 A plausible mechanism may be the reduction of concomitant pneumococcal bacteremia among PPV23 recipients.29 Experimental model studies showed that cell wall components of killed pneumococci are capable of triggering an inammatory cascade response in the host, resulting in death.30 The reduction of pneumococcal bacteremia may prevent the initiation of these inammatory processes, reducing the severity of illness among patients requiring hospitalization for CAP. Large decreases in rates of IPD, including bacteremia, occurred among children 2 years of age after PCV7 licensure,6,7,15,3135 which possibly explains why, similar to ndings for adult recipients of PPV23, PCV7 may reduce the frequency of CAPassociated systemic complications. In contrast to trends in CAP-associated systemic complication rates, rates of local complications increased for all age groups, with the highest rates occurring among preschool-aged children. In addition, the presence of any CAP-associated complication among children 1 to 18 years of age was largely attributable to local complications. It is unclear, however, whether this trend can be attributed fully to the changing epidemiological features of IPD after the introduction of PCV7. Two studies reported increasing regional rates of empyema in children before PCV7 licensure,27,36 which raises the possibility that the current increase in local complication rates is a continuation of a previous trend. Rates of local complications also may be inuenced by the increasing prevalence of communityacquired methicillin-resistant S aureus, which has become the pathogen most commonly isolated from empyema in several centers.26,27 The limitations of
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standard microbiologic isolation techniques have made etiologic and incidence studies of empyema problematic. Bacteria are isolated infrequently from blood or pleural uid cultures for children with empyema17,26,27 and, at one center, culture-negative empyema accounted for most of the increase in empyema frequency.17 Small studies using polymerase chain reactionbased assays identied S pneumoniae in 75% to 87.5% of culture-negative empyema cases.3740 Empyema may be an overlooked major category of IPD in the post-PCV7 era. Black race is an independent risk factor for IPD,6,41 and racial disparities among children with IPD are greatest for children 2 years of age.42,43 Discharge rates of CAP and CAPassociated complications were higher for black children than for white children. Our ndings suggest that the difference in rates of CAP discharges and systemic complications between black and white children has decreased over time. Postlicensure data demonstrated a similar reduction in the racial disparity in rates of IPD among children after the rst 2 years of widespread PCV7 vaccination.4244 Rates of CAP discharges and systemic complications among black children have seemed to plateau, with no additional decreases after 2003. The groups experienced similar increases in rates of local complications over time. Additional efforts will be required to ensure that reductions in racial disparity can be maintained as the epidemiological features of IPD change. This study has several limitations. First, the KID is an administrative dataREFERENCES
1. Messina AF, Katz-Gaynor K, Barton T, et al. Impact of the pneumococcal conjugate vaccine on serotype distribution and antimicrobial resistance of invasive Streptococcus pneumoniae isolates in Dallas, TX,

base of discharge-level data, without clinical information beyond that captured in ICD-9-CM codes. The identication of CAP discharges depends on the accuracy of ICD-9-CM coding, and miscoding of cases with CAP and CAPassociated complications is possible. We might have underestimated the rate of complications, because patients with CAP and a CAP-associated metastatic complication such as osteomyelitis might have received a primary discharge diagnosis of osteomyelitis rather than CAP, which would have resulted in the exclusion of such patients from our study. This might explain the extremely low incidence of metastatic complications found in our study. We expect that such misclassication would not occur disproportionately in one year versus the next, and the observed trend in CAP-associated complication rates likely reects a true trend. Second, although ICD-9-CM discharge diagnosis codes identify CAP with high sensitivity, ICD-9-CM codes have poor sensitivity in identifying pneumonia caused by specic pathogens.45 Therefore, we could not identify whether changes in rates of CAP-associated complications were attributable to specic pathogens. Third, patients with hospital-acquired pneumonia might have been included, because there is no specic ICD-9-CM code for CAP. We minimized the likelihood of such misclassication by using a previously validated approach to identifying patients with CAP.22 In this approach, patients with pneumonia listed as a secondary diagnosis rather than a primary diagnosis must have a pneumonia-related symptom (eg, cough or tachypnea) listed as the

primary diagnosis. For example, a patient hospitalized after traumatic injury who develops ventilatorassociated pneumonia is likely to have trauma, rather than pneumonia or a pneumonia-related symptom, listed as the primary diagnosis. Fourth, we were unable to determine the vaccination status of our study population, to assess the efcacy of PCV7 in preventing CAP, and could only infer the impact of PCV7 introduction on the general pediatric population. Last, the inclusion of every third year in the KID might have affected our ability to interpret trends accurately, given year-toyear epidemiological uctuations in incidence caused by factors unrelated to pneumococcal vaccination.

CONCLUSIONS
Since the introduction of PCV7 in 2000, rates of CAP hospitalizations have decreased for children 1 year of age but seem to be increasing for children 5 years of age. Rates of systemic complications have decreased for children 1 year of age, but rates of local complications are increasing in all pediatric age groups. Additional studies are needed to determine the underlying epidemiological factors associated with these changes.

ACKNOWLEDGMENTS Drs Lee and Kronman are recipients of a Young Investigator Award from the Academic Pediatric Association. Dr Shah received support from the National Institute of Allergy and Infectious Diseases (grant K01 AI73729) and the Robert Wood Johnson Foundation, through its Physician Faculty Scholar Program.

children from 1999 through 2005. Pediatr Infect Dis J. 2007;26(6):461 467 2. Whitney CG, Farley MM, Hadler J, et al. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide

conjugate vaccine. N Engl J Med. 2003;348(18): 17371746 3. Kaplan SL, Mason EO Jr, Wald ER, et al. Decrease of invasive pneumococcal infections in children among 8 childrens hospitals in

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APPENDIX 1 ICD-9-CM Codes Used to Identify Pneumonia-Related Symptoms, Comorbidities, and

Trauma
Symptom Pneumonia-related symptoms Fever Respiratory abnormality, unspecied Shortness of breath Tachypnea Wheezing Cough Hemoptysis Abnormal sputum Chest pain Precordial pain Painful respiration Abnormal chest sound (rales, friction, or abnormal percussion) Comorbidities HIV Malignancy Cystic brosis Immune mechanism disorder Sickle cell disease Diseases of white blood cells Other lung conditions Congenital heart defects Encounter for radiation, chemotherapy, or transplant Trauma Railway accidents Motor vehicle trafc accidents Motor vehicle nontrafc accidents Other road vehicle accidents Water transport accidents Accidental falls Accidents caused by re or ame Accidents caused by submersion or suffocation Other accidents Suicide, self-inicted injury Homicide/injury inicted purposely Legal intervention Undetermined accident or inicted purposely
x indicates digits 0 to 9, where applicable.

ICD-9-CM Codes 780.6 786.00 786.05 786.06 786.07 786.2 786.3 786.4 786.5 786.51 786.52 786.7

042 140.x208.x 277 279, 334.8 282.6x 288 507, 517 745747 V42, V58.0, V48.1x

E800E807 E810E819 E820E825 E826E829 E830E838 E880E888 E890E899 E910E915 E916E925 E953E959 E960E969 E970E977 E983E989

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APPENDIX 2 ICD-9-CM Codes for Identication of CAP-Associated Complications

Complication Subcategory Local Complication Description Emypema Lung abscess Bronchopleural stula Necrotizing pneumonia Acute respiratory failure SIRS/sepsis ECMO Hemolytic uremic syndrome Meningitis Central nervous system abscess Mastoiditis Pericarditis Endocarditis Osteomyelitis Septic arthritis ICD-9-CM Codes 510.x, 511.0, 511.1, 511.9 513.x 33.42, 510.0 32.xa 518.8x, 799.1 995.9x 39.6x 283.11 320.0, 320.1, 320.2, 320.3, 320.8x 324.x 383.0x 420.x 421.x 730.0x, 730.2x 711.x

Systemic

Metastatic

ECMO indicates extracorporeal membrane oxygenation; SIRS, systemic inammatory response syndrome; x, digits 0 to 9, where applicable. a ICD-9-CM code for lung resection as a proxy indicator.

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National Hospitalization Trends for Pediatric Pneumonia and Associated Complications Grace E. Lee, Scott A. Lorch, Seth Sheffler-Collins, Matthew P. Kronman and Samir S. Shah Pediatrics 2010;126;204-213; originally published online Jul 19, 2010; DOI: 10.1542/peds.2009-3109
Updated Information & Services References including high-resolution figures, can be found at: http://www.pediatrics.org/cgi/content/full/126/2/204 This article cites 42 articles, 19 of which you can access for free at: http://www.pediatrics.org/cgi/content/full/126/2/204#BIBL Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://www.pediatrics.org/misc/Permissions.shtml Information about ordering reprints can be found online: http://www.pediatrics.org/misc/reprints.shtml

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