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National Trends in the Incidence, Outcomes and Charges of Pediatric Osteoarticular Infections, 1997–2012

Stockmann, Chris MSc*†‡; Ampofo, Krow MD*; Pavia, Andrew T. MD*; Byington, Carrie L. MD*; Blaschke, Anne J. MD, PhD*; Sherwin, Catherine M.T. PhD†‡; Spigarelli, Michael G. MD, PhD†‡; Hersh, Adam L. MD, PhD*

The Pediatric Infectious Disease Journal: June 2015 - Volume 34 - Issue 6 - p 672–674
doi: 10.1097/INF.0000000000000686
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In the United States, the incidence of osteoarticular infections among hospitalized children increased 15% from 2.07 to 2.38 cases per 1000 admissions from 1997 through 2012. The incidence of methicillin-resistant Staphylococcus aureus-coded infections increased from 0.02 to 0.36 cases per 1000 admissions. Methicillin-resistant S. aureus-coded cases had a larger number of therapeutic procedures, longer hospital stays and higher hospital charges.

Supplemental Digital Content is available in the text.

From the *Division of Pediatric Infectious Diseases, Division of Clinical Pharmacology, Department of Pediatrics, and Department of Pharmacology/Toxicology, University of Utah College of Pharmacy, Salt Lake City, UT.

Accepted for publication December 4, 2104.

Funding: C.S. is supported by the American Foundation for Pharmaceutical Education’s Clinical Pharmaceutical Sciences Fellowship.

The authors have no conflicts of interest to disclose.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s website (www.pidj.com).

Address for correspondence: Chris Stockmann, MSc, Division of Pediatric Infectious Diseases, Department of Pediatrics, University of Utah School of Medicine, 295 Chipeta Way, Salt Lake City, UT 84108. E-mail: Chris.Stockmann@hsc.utah.edu

There are few national estimates of the burden of pediatric osteoarticular infections, including pyogenic arthritis and osteomyelitis. Historically, methicillin-susceptible Staphylococcus aureus (MSSA) has been the predominant cause of these infections.1 Within the past 15 years, the epidemiology of pediatric pyogenic arthritis and osteomyelitis has changed following the emergence of community-associated methicillin-resistant S. aureus (MRSA) infections.2 Single center studies and evaluations conducted among freestanding children’s hospitals have reported an increase in the incidence of MRSA-associated osteoarticular infections.2,3 Our objectives were to evaluate the national incidence, outcomes and hospital charges associated with pediatric pyogenic arthritis and osteomyelitis. Additionally, we compared the incidence, outcomes and charges of MRSA-coded osteoarticular infections with those caused by other organisms.

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MATERIALS AND METHODS

Data Source

This was a retrospective cohort study that used data from the United States Agency for Healthcare Research and Quality (AHRQ) Healthcare Cost and Utilization Project (HCUP) Kids’ Inpatient Database (KID). KID is a de-identified administrative data set designed specifically to assess the use of hospital services by children. KID contains inpatient data for children hospitalized at nonfederal, nonrehabilitation, general, specialty and pediatric hospitals. In KID, hospitals are categorized by their geographic location according to US Census Regions (see Table, Supplemental Digital Content 1, http://links.lww.com/INF/C86). At its inception in 1997, 22 states contributed data. By 2012, 44 states contributed data. KID samples 10% of uncomplicated deliveries and 80% of all other admissions for children <21 years of age. We excluded all normal, uncomplicated deliveries and restricted the analysis to children <18 years. Data sets were available for 1997, 2000, 2003, 2006, 2009 and 2012.

Therapeutic and diagnostic procedures were identified using the Procedure Classes software tool, which was developed for use with HCUP databases.4 Magnetic resonance imaging (MRI) scans were identified by the inclusion of “MRI” or “magnetic res image” in the procedure description.

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Identification of Pyogenic Arthritis and Osteomyelitis Hospitalizations

Pyogenic arthritis cases were identified using methods described by Freedman et al5 Briefly, cases were identified using an International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) code of 711.0 (pyogenic arthritis). Osteomyelitis cases were identified using ICD-9-CM codes 730.0× (acute osteomyelitis) and 730.2× (unspecified osteomyelitis) as previously described.6 For both conditions, cases were defined using ICD-9-CM codes in any of the 15 diagnosis fields. MRSA-associated osteoarticular infections were defined by the presence of an ICD-9-CM code for MRSA (V09.0, V12.04, 038.12 or 041.12) in combination with an ICD-9-CM code consistent with pyogenic arthritis or osteomyelitis.7

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Total Hospital Charges

Total hospital charges are reported to AHRQ by each state and undergo review by professional KID database coders. For these analyses, all total hospital charges were inflation-adjusted using the medical care component of the Consumer Price Index to 2013 US dollars ($).8

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Statistical Analyses

We used the HCUP weighting procedure and the survey package in R 3.1.2 (R Foundation for Statistical Computing, Vienna, Austria) to obtain nationally representative estimates for all reported characteristics (see Table, Supplemental Digital Content 2, http://links.lww.com/INF/C87).9 The incidence of hospitalizations for pyogenic arthritis and osteomyelitis is reported as the number of cases per 1000 hospital admissions.

Continuous variables are reported as the median [interquartile range (IQR)] and compared using the nonparametric Wilcoxon–Mann–Whitney rank-sum test. Categorical variables are presented as the n (%) and compared using Fisher’s exact test or the χ2 test, as appropriate. All statistical comparisons are two-sided with an α of 0.05.

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RESULTS

Overall and Age-Stratified Incidence

The overall incidence of hospitalizations for acute osteoarticular infections increased 15% [95% confidence interval (CI): 12–19%] from 2.07 per 1000 admissions in 1997 to 2.38 per 1000 in 2012 (P < 0.001; Table 1). Nationally, the pediatric population grew by nearly 6% over the same period. The increase in osteoarticular infections was driven primarily by an increase in the incidence of osteomyelitis, which increased 28% (95% CI: 22–34%) from 0.97 to 1.24 per 1000 admissions (P < 0.001); however, the incidence of pyogenic arthritis also increased from 1.23 to 1.36 per 1000 admissions (P < 0.001). Changes in the incidence of osteoarticular infections varied by age (see Tables, Supplemental Digital Content 3 and 4, http://links.lww.com/INF/C88 and http://links.lww.com/INF/C89).

TABLE 1

TABLE 1

The incidence of pediatric osteoarticular infections also varied by region. The largest increase was in the Midwest, with a 29% (95% CI: 19–38%) increase from 1.78 to 2.28 per 1000 admissions (P < 0.001). Similar increases were noted in the South (27%; 95% CI: 21–34%) and the Northeast (20%; 95% CI: 11–29%; P < 0.001 for both). Conversely, in the West, the incidence of osteoarticular infections decreased by 12% (95% CI: 6–17%) from 2.65 to 2.34 per 1000 (P < 0.001).

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Clinical Care and Outcomes

There was a 23% increase in therapeutic procedures (P < 0.001) and a 94% increase in MRIs performed (0.06 MRIs/patient in 1997 vs. 0.12 MRIs/patient in 2012; P < 0.001). The median total hospital length of stay increased by 18.0 hours (95% CI: 14.3–21.6; P < 0.001). From 1997 to 2012, the mortality rate for all osteoarticular infections remained stable at 0.3%.

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Total Hospital Charges

For children with osteoarticular infections, the median inflation-adjusted hospital charge increased from $17,677 (IQR: $10,078–31,250) in 1997 to $34,549 (IQR: $20,078–64,386) in 2012 (P < 0.001). The median increase in hospital charges was $643 and $1270 per year for pyogenic arthritis and osteomyelitis, respectively.

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MRSA-Coded Osteoarticular Infections

The incidence of MRSA-coded osteoarticular infections increased from 0.02 per 1000 admissions in 1997 to 0.36 per 1000 in 2012 (P < 0.001). The percentage of MRSA-coded cases among all osteoarticular infections increased from 0.8% to 15.1%. The incidence of MRSA-coded osteoarticular infections varied by region, although all regions experienced an increase over the study period (Table 1). Children with an MRSA code had longer lengths of stay [median 7 (IQR: 4–13) vs. 5 (IQR: 3–8) days; P < 0.001] and higher hospital charges [median $42,982 (IQR: $23,951–85,965) vs. $24,643 (IQR: $13,902–45,618); P < 0.001] when compared with children without an MRSA code. Therapeutic procedures were performed for 86% of children with a code for MRSA, when compared with 78% of children without an MRSA code (P < 0.001).

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DISCUSSION

Using a nationally representative database, we found that the incidence of hospitalizations for pediatric osteoarticular infections increased 15% from 1997 to 2012, which was partially driven by an increase in MRSA-coded cases. We found evidence that MRSA-associated osteoarticular infections may be more complicated, with a longer hospital length of stay, a larger number of therapeutic procedures and higher charges.

A strength of our study is that we used a nationally representative data set of osteoarticular infections involving hospitalized children in a variety of acute care settings. Our findings build on previous studies that reported an increase in the incidence of pediatric pyogenic arthritis and osteomyelitis.2,3 In Tennessee, the incidence of acute osteoarticular infections among hospitalized children more than doubled from 2.6 to 6.0 per 1000 admissions between 2000 and 2004.2 Over the same period, the authors reported a 10-fold increase in the proportion of cases caused by MRSA. Similarly, Gerber et al3 described an increase in the incidence of MRSA-associated osteomyelitis from 0.3 to 1.4 per 1000 admissions from 2002 to 2007 among a network of >40 freestanding children’s hospitals. In our national study that included a broader sample of hospital types, the increase in the incidence of osteoarticular infections was somewhat less dramatic, but nonetheless highlights the large increase attributable to MRSA nationwide. We also identified variations in the incidence of MRSA-associated osteoarticular infections among different geographic regions, which corroborate earlier reports from the US Centers for Disease Control and Prevention’s Active Bacterial Core Surveillance Program.8

The growth in inflation-adjusted hospital charges for pediatric osteoarticular infections averaged 6.4% each year, which was higher than the 3.0% national rate of growth in per capita healthcare expenditures from 1997 to 2012.11 The increase in hospital charges observed in this study may be attributable to the increase in therapeutic procedures and use of MRIs, which temporally coincided with an increase in MRSA-coded infections. Arnold et al2 evaluated the severity of pediatric osteoarticular infections and found that 91% of patients with MRSA required a surgical procedure when compared with 62% of children with MSSA. Additionally, the authors described a median length of stay of 7 days for children with MSSA-associated osteoarticular infections when compared with 10 days for children with MRSA.

Use of the KID database affords the opportunity to examine national-level, inpatient pediatric data; however, the KID database does not include microbiologic data, and we therefore used ICD-9-CM discharge diagnosis codes to identify MRSA-associated osteoarticular infections. Although ICD-9-CM codes are generally specific, they are unlikely to feature ideal sensitivity, and thus, we may have underestimated the actual incidence of MRSA. However, our use of 15 discharge diagnosis fields is similar to previous studies that evaluated the epidemiology of pediatric MRSA infections.3,7 Because of the lack of microbiological data in KID, trends in other etiological agents of osteoarticular infections could not be assessed.

In this study, we showed that the national incidence of hospitalizations for osteoarticular infections among hospitalized children increased 15% from 1997 to 2012. The increased burden of osteoarticular infections in children was explained by rising rates of MRSA infection—and in particular MRSA-associated osteomyelitis. MRSA-associated osteoarticular infections may be more severe than those caused by other organisms. Effective preventative and therapeutic strategies are needed to reduce the clinical and economic burden of pediatric osteoarticular infections.

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REFERENCES

1. Luhmann JD, Luhmann SJ.. Etiology of septic arthritis in children: an update for the 1990s. Pediatr Emerg Care. 1999;15:40–42
2. Arnold SR, Elias D, Buckingham SC, et al. Changing patterns of acute hematogenous osteomyelitis and septic arthritis: emergence of community-associated methicillin-resistant Staphylococcus aureus. J Pediatr Orthop. 2006;26:703–708
3. Gerber JS, Coffin SE, Smathers SA, et al. Trends in the incidence of methicillin-resistant Staphylococcus aureus infection in children’s hospitals in the United States. Clin Infect Dis. 2009;49:65–71
4. HCUP Procedure Classes. Healthcare Cost and Utilization Project (HCUP). March 2014. Rockville, MD: Agency for Healthcare Research and Quality Available at: www.hcup-us.ahrq.gov/toolssoftware/procedure/procedure.jsp. Accessed April 10, 2014.
5. Freedman J, Guller U, Benjamin DK, et al. National trends in health care utilization and racial and socioeconomic disparities in pediatric pyogenic arthritis. J Pediatr Orthop. 2006;26:709–715
6. Zaoutis T, Localio AR, Leckerman K, et al. Prolonged intravenous therapy versus early transition to oral antimicrobial therapy for acute osteomyelitis in children. Pediatrics. 2009;123:636–642
7. Schweizer ML, Eber MR, Laxminarayan R, et al. Validity of ICD-9-CM coding for identifying incident methicillin-resistant Staphylococcus aureus (MRSA) infections: is MRSA infection coded as a chronic disease? Infect Control Hosp Epidemiol. 2011;32:148–154
8. Fridkin SK, Hageman JC, Morrison M, et al.Active Bacterial Core Surveillance Program of the Emerging Infections Program Network. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med. 2005;352:1436–1444
9. Lumley T.. Analysis of complex survey samples. J Stat Soft. 2004;9:1–19
10. Centers for Medicare and Medicaid Services, Office of the Actuary, National Health Statistics Group. U.S. Department of Commerce, Bureau of Economic Analysis. Available at: http://www.cms.gov/Research-Statistics-Data-and-Systems/Statistics-Trends-and-Reports/NationalHealthExpendData/NationalHealthAccountsHistorical.html. Accessed June 2, 2014
    11. Council of Economic Advisers. Trends in health care cost growth and the role of the Affordable Care Act;. November 2013. Available at: http://www.whitehouse.gov/sites/default/files/docs/healthcostreport_final_noembargo_v2.pdf. Accessed November 19, 2014
    Keywords:

    osteoarticular infections; children; infectious diseases; Staphylococcus aureus; MRSA

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