Hospitalization for Community-Acquired Pneumonia in Children: Effect of an Asthma Codiagnosis

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1 RESEARCH ARTICLE Hospitalization for Community-Acquired Pneumonia in Children: Effect of an Asthma Codiagnosis Karen M. Wilson, MD, MPH, a Michelle R. Torok, PhD, b,c Russell Localio, PhD, d Lisa McLeod, MD, MSCE, a Rajendu Srivastava, MD, FRCP(C), MPH, e Xianqun Luan, MS, f Zeinab Mohamad, DrPH, f Samir S. Shah, MD, MSCE, g for the Pediatric Research in Inpatient Settings (PRIS) Network ABSTRACT a Section of Pediatric Hospital Medicine, Children s Hospital Colorado and the University of Colorado School of Medicine, Aurora, Colorado; b Section of Pediatric Hospital Medicine, Children s Hospital Colorado, Aurora, Colorado; c Children s Outcomes Research, University of Colorado School of Medicine, Aurora, Colorado; d Department of Biostatistics and Epidemiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania; e Division of Pediatric Inpatient Medicine, Department of Pediatrics, Primary Children s Hospital and Institute for Healthcare Delivery Research, Intermountain Healthcare, Salt Lake City, Utah; f Healthcare Analytics Unit, PolicyLab, Children s Hospital of Philadelphia, Philadelphia, Pennsylvania; and g Divisions of Hospital Medicine and Infectious Diseases, Cincinnati Children s Hospital Medical Center, Cincinnati, Ohio BACKGROUND AND OBJECTIVE: Community-acquired pneumonia (CAP) is a common and expensive cause of hospitalization among US children, many of whom receive a codiagnosis of acute asthma. The objective of this study was to describe demographic characteristics, cost, length of stay (LOS), and adherence to clinical guidelines among these groups and to compare health care utilization and guideline adherence between them. METHODS: This was a multicenter retrospective cohort study using data from the Pediatric Health Information System. Children aged 2 to 18 who were hospitalized with uncomplicated CAP from July 1, 2007, to June 30, 2012 were included. Demographics, LOS, total standardized cost, and clinical guideline adherence were compared between patients with CAP only and CAP plus acute asthma. RESULTS: Among the admissions, 57% were diagnosed with CAP only; 43% had a codiagnosis of acute asthma. The geometric mean for standardized cost was $4830; for LOS, it was 2.01 days. Eighty-four percent of patients had chest radiographs; CAP1acute asthma patients were less likely to have a blood culture performed (36% vs 62%, respectively) and more likely not to have a complete blood count performed (49% vs 27%, respectively). Greater guideline adherence was associated with higher cost at the patient-level but lower average cost per hospitalization at the hospital level. CAP1acute asthma patients had higher relative costs (11.8%) and LOS (5.6%) within hospitals and had more cost variation across hospitals, compared with patients with CAP only. CONCLUSIONS: A codiagnosis of acute asthma is common for children with CAP. This could be from misdiagnosis or co-occurrence. Diagnostic and/or management variability appears to be greater in patients with CAP1asthma, which may increase resource utilization and LOS for these patients. DOI: /hpeds Copyright 2015 by the American Academy of Pediatrics Address correspondence to Karen M. Wilson, MD, MPH, Section of Pediatric Hospital Medicine, Children s Hospital Colorado, University of Colorado School of Medicine, E. 16th Ave, B302, Aurora, CO Karen.wilson@childrenscolorado.org HOSPITAL PEDIATRICS (ISSN Numbers: Print, ; Online, ). FINANCIAL DISCLOSURE: Drs Wilson, Srivastava, and Shah were supported by the Children s Hospital Association. The other authors have indicated that they have no financial relationships relevant to this article to disclose. FUNDING: A grant from the Children s Hospital Association to the Pediatric Research in Inpatient Settings Network POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose. Dr Wilson conceptualized the design and led the study and drafted the initial manuscript; Dr Torok helped with analytic planning and methods, completed statistical analyses, and helped draft the manuscript; Dr Localio led the analytic plan and advised on statistical procedures and study design, performed statistical analyses, drafted parts of the manuscript, and helped edit the manuscript; Mr Luan and Dr Mohamad completed statistical analyses, assisted with study design, and helped edit the manuscript; Drs McLeod, Srivastava, and Shah participated in the study design, analytic planning, and data quality review and edited the manuscript; and all authors approved the final manuscript as submitted. HOSPITAL PEDIATRICS Volume 5, Issue 8, August

2 Community-acquired pneumonia (CAP) ranks among the most common and costly reasons for hospitalization of children. 1 Children hospitalized with CAP often receive a diagnosis of asthma, a condition colloquially referred to as asthmonia. Distinguishing CAP occurring alone from CAP occurring with an asthma exacerbation can be challenging because viral respiratory tract infections predispose to bacterial pneumonia and also trigger asthma exacerbations. In addition, although CAP is typically diagnosed by chest radiograph or focal lung findings, there is evidence that atelectasis can mimic infiltrates, 2 which could lead to misdiagnosis of pneumonia in a patient with asthma. Children with asthma are at increased risk for invasive pneumococcal infections, 3 including pneumonia. An important challenge in the management of CAP occurring with an asthma exacerbation is that national guidelines focus treatment on a single diagnosis (CAP alone or asthma alone), and in some cases, the guidelines conflict on ideal management. 4,5 The guidelines for treatment of uncomplicated CAP include obtaining bacterial cultures, viral testing, inflammatory markers, chest radiography, and the use of an aminopenicillin. Corticosteroids, a mainstay of asthma therapy, have not been proven effective for the treatment of CAP in randomized trials involving adults 6 and are not recommended. There is no role for bronchodilators in the treatment of CAP. In contrast, management of an acute asthma exacerbation includes administration of oral corticosteroids and bronchodilators. Routine chest radiographs and viral testing are not recommended, and in fact, chest radiographs in pediatric asthma were chosen as one of the Choosing Wisely campaign s procedures not to order. 7 Previous studies of hospital-level adherence to CAP guidelines have shown variability; the average percent of patients receiving a chest radiograph for CAP across 29 children s hospitals ranged from 54% to 90%, whereas the average percent of patients with a documented blood culture ranged from 0% to 92%. 8 Conversely, adherence to the asthma care guidelines of using systemic corticosteroids and bronchodilators was high and consistent across hospitals. 9 Although the recommendations for management of uncomplicated pneumonia alone or asthma alone are well defined, they do not provide direction for a common clinical occurrence: treating patients who are diagnosed with both. We hypothesized that this might lead to more diagnostic uncertainty, and therefore decreased adherence to clinical care guidelines, increased health care utilization, and variation in the clinical management and treatment of these patients. Understanding how patients who have pneumonia and asthma codiagnoses influence utilization might help to clarify more appropriate patient selection for guidelines use, and allow systems of care based interventions to more accurately measure patient and cost outcomes. We used data from a national multihospital cohort of children to determine the variation in resource utilization and adherence to the pneumonia guidelines in children with CAP with and without a concomitant diagnosis of asthma. METHODS Data Source and Study Design We conducted a retrospective, multicenter cohort study using data from the Pediatric Health Information System (PHIS), an administrative database that contains inpatient data from.40 pediatric hospitals in the United States. Detailed hospitalization and resource utilization data, such as demographic, diagnostic, procedural, outcome, and charge information, are contained in PHIS. Data are deidentified; however, encrypted medical record numbers permit tracking of patients within hospitals across hospitalizations. The Children s Hospital Association and participating hospitals jointly ensure data quality as previously described. 10 This study, using deidentified data, was considered exempt according to the policies of the Cincinnati Children s Hospital Medical Center Institutional Review Board. Study Cohort We created a cohort of patients with uncomplicated CAP and CAP1asthma for which the pneumonia guidelines would apply. 4 We used a previously validated algorithm for identifying hospitalized patients with CAP from PHIS. 11 Patients aged.3 months and,18 years between July 1, 2007, and June 30, 2012, with principal or secondary diagnosis International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis codes of pneumonia were eligible. We excluded patients who were unlikely to have a diagnosis of uncomplicated CAP using the following criteria: (1) receipt of antibiotics not typically used for CAP on day 0, 1, or 2 12 ; (2) no charge for antibiotics on the first hospital day; (3) an International Classification of Diseases code for viral pneumonia; (4) complex chronic condition 13 ; (5) age,2 years (to avoid misclassification with bronchiolitis); (6) a charge for a chest computed tomography, ultrasound, or decubitus films on the first hospital day (to exclude complicated pneumonia on presentation); (7) a charge for hyperalimentation on the first hospital day; or (8) a charge for extracorporeal membrane oxygenation on the first hospital day. Three clinicians reviewed all additional diagnoses and procedures and excluded patients with diagnoses or procedures suggesting a low likelihood of CAP (eg, motor vehicle traffic accident). To better ensure patients with a typical presentation of CAP, we excluded hospitalizations for which total costs were beyond the lowest and highest fifth percentile within each hospital. 1 For patients with multiple admissions meeting the inclusion criteria, we selected the first hospitalization. Exposure Measure The main exposure was meeting inclusion criteria for CAP and a codiagnosis of acute asthma (CAP1asthma). Patients were considered to have CAP1asthma if they had any diagnosis code of asthma and a charge for a short-acting bronchodilator use after hospital day 1. Because 35% of children admitted with a diagnosis of CAP in 1 large cohort had received corticosteroids 14 and this was more common in patients in the ICU, we did not include steroid use as a specific marker for asthma to avoid confounding by severity. Patients in the CAP1asthma exposure group were 416 WILSON et al

3 compared with the clinical group who had CAP without acute asthma. Covariables Categorized age (,5, 5 11, $12 years), gender, race (white, black, Asian, other); insurance (government, nongovernment); geographic region (Midwest, Northeast, South, West), mean number of hospital beds, and ICU stay (yes/no) were included in the analyses. Outcome Measures Measured outcomes were length of stay (LOS), total standardized cost, and guideline adherence. LOS in days was measured as a continuous variable. Total standardized cost in US dollars was calculated using a Cost Master Index (CMI) previously developed for research utilizing data from PHIS hospitals. 1 Briefly, standardized costs for an entire patient hospitalization are calculated by first multiplying the billed units of each item by its standardized per unit cost and then summing these itemized costs, resulting in a total standardized hospital bill. 15 All standardized costs were inflated to 2012 dollars by using the medical care services component of the Consumer Price Index. Of the 42 hospitals contained in the PHIS database, 2 were excluded from cost and LOS analyses due to missing data. Adherence to the Pediatric Infectious Diseases Society and the Infectious Diseases Society of America clinical guidelines for the management of children with pneumonia 3 was the final outcome. The following guidelines were assessed, based on availability in the PHIS dataset: receipt of chest radiograph (recommended), blood culture (recommended), respiratory viral panel testing (recommended), Mycoplasma pneumoniae testing when macrolide was ordered (recommended), complete blood count testing (not recommended), and Chlamydophila pneumoniae testing (not recommended). We considered all available recommendations regardless of strength of evidence. Adherence to guidelines on the individual level was depicted as a rate (number of guidelines followed/total guidelines measured). Adherence to guidelines at the hospital-level was depicted as the mean number of guidelines followed per patient with CAP admitted to that particular hospital. Statistical Analysis We described variation in the total standardized costs within hospital using the geometric mean and range. Bivariable differences between the exposure groups were tested using x 2 and Wilcoxon ranksum tests for individual-level characteristics. We used Cochran-Mantel- Haenszel statistics to test differences in demographic and clinical course characteristics between the 2 clinical groups when stratified by hospital, and logrank tests were used for stratified tests to evaluate differences between clinical groups for continuous but skewed characteristics accounting for hospital. Analysis of variance was used to test bivariable differences for hospital-level variables (region and number of beds). We modeled cost and LOS with a log g model with patient-level factors as covariates and accounting for clustering of patients by hospital. These models decomposed the effects of the covariates into within-hospital and between hospital components to rule out possible confounding by hospital in these associations of interest. 16,17 This FIGURE 1 Cohort selection flow diagram. CT, computed tomography; ECMO, extracorporeal membrane oxygenation; HOSPITAL PEDIATRICS Volume 5, Issue 8, August

4 decomposition permits 2 comparisons of interest: (1) the effects of the risk factor on outcome when applied to otherwise similar children within a hospital (eg, do 2 similar patients at the same hospital have different outcomes depending on guideline adherence in their management) and (2) the effects when moving from a hospital with 1 average level of a risk factor to a hospital with a different average level of the same factor (eg, do similar patients admitted to 2 hospitals with varying average guideline adherence across their patient populations have different outcomes). 18 Results from this decomposed model of the within hospital comparison were then confirmed with models in which hospital was a fixed effect. We also evaluated the TABLE 1 Bivariable Comparison of Characteristics Between Clinical Groups Characteristics Overall (n ) Range Among Hospitals (n 5 42) (%) CAP (n ) CAP1acute asthma (n ) Age, y (median, SD) 5.0 (3.6) 4.0 (3.7) 5.0 (3.4),.0001 Age, y,.0001,.001, (49.7) (52.0) 5012 (46.7) (41.7) (38.9) 4897 (45.6) $ (8.6) (9.4) 825 (7.7) Female (48.0) (49.6) 4915 (45.8),.0001,.001 Principal payer, government c (41.9) (39.2) 4875 (45.4),.0001,.001 ICU stay 1936 (7.7) (3.6) 1417 (13.2),.0001,.001 Race (n ),.0001,.001 White (54.5) (62.5) 4530 (43.7) Black 6630 (27.4) (19.5) 3934 (37.9) Asian 718 (3.0) (3.6) 220 (2.1) Other 3683 (15.2) (14.4) 1683 (16.2) Region,.0001 N/A Midwest 7306 (29.1) 4046 (28.1) 3260 (30.4) Northeast 2683 (10.7) 1357 (9.4) 1326 (12.4) South 9620 (38.3) 5882 (40.9) 3738 (34.8) West 5515 (21.9) 3105 (21.6) 2410 (22.5) Number of beds,.0001 N/A #200 beds 3191 (12.7) 1695 (11.9) 1496 (13.9) beds 8220 (32.7) 4730 (32.9) 3490 (32.5) beds 6621 (26.4) 4037 (28.1) 2584 (24.1).400 beds 7092 (28.2) 3928 (27.3) 3164 (29.5) Metrics % with chest radiograph (83.5) (82.7) 9067 (84.5) % with blood culture (51.1) (62.1) 3898 (36.3),.0001,.0001 % without CBC 9170 (36.5) (27.5) 5213 (48.6),.0001,.0001 % with respiratory viral panel testing 7935 (31.6) (31.1) 3458 (32.2) % with macrolide with 1693 (6.7) (6.9) 701 (6.5) mycoplasma testing % without Chlamydophila (99.9) (99.8) (99.9) pneumonia testing LOS, d geometric mean (range), d d ( ) 2.1 ( ),.0001,.0001 ICU LOS, geometric mean (range), d e ( ) 1.6 ( ).28,.0001 Total standardized cost, geometric mean (range), US$ d ( ) ( ),.0001,.0001 CBC, complete blood count. a x 2 and Wilcoxon rank-sum test used to test individual-level variables; analysis of variance used to test hospital-level variables (region and number of beds). b Controlling for hospital: Cochran-Mantel-Haenszel statistics used for categorical variables; log-rank test used for continuous variables. c Defined as Charity, In-State Medicaid (managed care), In-State Medicaid (other), Medicare, Other Government, Out-of-State Medicaid (all), TRICARE. d LOS and total cost data missing for 2 hospitals (n ). e Patients with an ICU stay, n P a P b 418 WILSON et al

5 effect of codiagnosis on cost and LOS within hospitals by hospital, by comparing the likelihood ratios from 2 models. The firstwasthesamemodelasdescribed earlier, with hospital as a fixed effect. The second included an interaction term between hospital and clinical group (CAP or CAP1asthma). A likelihood ratio test was performed to examine cost and LOS by hospital. Data were analyzed using SAS v9.3. Finally, we investigated the relative contribution to interhospital variance in standardized costs attributable to CAP and CAP1asthma using a mixed effects model with separate hospital-level random intercepts for the 2 groups. We compared these 2 variance components with total variance (including the residual, withinhospital component), using Stata version 13. Because log g models for this question would not converge, we opted for identity link models for this estimation. RESULTS Patient and Hospital Characteristics Of the admissions eligible for study inclusion, with CAP remained after applying exclusion criteria (Fig 1); of these, 43% had an additional diagnosis of and treatment of acute asthma. The median age was 5.0 years (Table 1). The distribution of age group, insurance, ICU stay, and race varied widely across hospitals. When comparing the 2 clinical groups, patients hospitalized with CAP1 asthma had a greater median age and were more likely to be male, to be black or other race/ethnicity, and to have government insurance than those with CAP only. Because patient characteristics are known to differ by hospital, we compared demographic and clinical course characteristics between the 2 clinical groups adjusting for hospital. The difference in the number of ICU days by clinical group reached statistical significance when accounting for hospital; other results were similar to the unadjusted results (Table 1). Patients with CAP1asthma were more likely to have received a macrolide antibiotic than those with CAP alone (59% vs 37%; P,.001) and to have received corticosteroids (87% vs 12%; P,.001). Resource Utilization Standardized cost varied between hospitals, from $3292 to $6547, with an overall geometric mean of $4830. Figure 2 displays the cost distribution by hospital and clinical group. Thirty-eight of the 40 hospitals had higher costs for the CAP1asthma patients compared with CAP alone. CAP1asthma patients had higher geometric mean cost compared with CAP alone ($5270 vs $4519) (Table 1). Multivariable analysis of total standardized cost within hospitals indicated that CAP1asthma patients were more costly compared with CAP alone (Table 2). We estimated cost variances not explained by patient-level factors between patients with CAP compared with those with CAP1 asthma, and found that unexplained interhospital variation as a percentage of total variation in costs was 7.6% for CAP and 12.3% for CAP1asthma. The likelihood ratio test for within hospital cost was statistically significant, suggesting that there was some variation in total standardized cost between CAP1asthma and CAP only patients across hospitals. However, the data suggest that for the vast majority of hospitals, cost is higher among CAP1asthma patients. The overall geometric mean for LOS was 2.01, with a range of 1.3 to 2.6 between hospitals. For ICU days, the overall mean was 1.63 with a range between hospitals from 1.0 to 2.3 (Table 1). Figure 3 shows the distribution of LOS by clinical group and hospital. Although 7 of 40 hospitals had longer LOS for CAP alone, the majority had longer LOS for CAP1asthma. Patients with CAP1asthma had longer LOS (2.1 vs 1.9); however, ICU LOS was similar (1.6 vs 1.6, P 5.28). Multivariable analysis indicated that patients with CAP1asthma had a 6% longer LOS compared with CAP patients without acute asthma (Table 2). The likelihood ratio test for within hospital LOS was statistically significant, suggesting that there was some variation in LOS between CAP1asthma and CAP-only patients across hospitals. For the majority of hospitals, LOS was longer for CAP1asthma compared with CAP only patients. FIGURE 2 Distribution of total standardized cost by clinical group and hospital (n 5 40). HOSPITAL PEDIATRICS Volume 5, Issue 8, August

6 TABLE 2 Multivariable Regression Results for Total Standardized Cost and LOS 95% CI P Total Standardized Cost (n ) a Guideline Adherence When comparing the 2 clinical groups at the patient level,.80% of patients in both groups received chest radiographs (Table 1). CAP1asthma patients were less likely to have a blood culture performed (36% vs 62%) and more often did not have a CBC performed (49% vs 27%). Few patients in either group received a macrolide with M pneumoniae testing (close to 7% in each group), and few patients in either group had C pneumoniae Relative Cost per Unit Change in Variable Across hospital contrast of effect of diagnosis on costs per 10% increase in the proportion of CAP1acute asthma patients b The difference between CAP-only vs CAP1acute asthma groups within each hospital c ,.0001 LOS (n ) d Relative LOS per Unit Change in Variable Across-hospital contrast of effect of diagnosis on LOS per 10% increase in proportion of CAP1 acute asthma patients The difference between CAP-only vs CAP1acute asthma groups within each hospital e Total Standardized Costs and Guideline Adherence (n ) f,g Relative Cost per Unit Change in Variable Number of guidelines adhered to 1 2 Reference , ,.0001 Mean no. of guidelines to which hospital adhered for CAP1acute asthma patients Mean no. of guidelines to which hospital adhered for CAP-only patients Proportion of patients who have CAP1acute asthma Sample sizes do not add up to due to missing data (see Table 1). Estimates are from a log-g model. a Adjusted for gender, insurance, age group, race, ICU stay, mean number of hospitals beds, and mean LOS. b A relative cost of means that across hospitals, a 10% increase in CAP1acute asthma patients is associated with a 35% relative decrease in total standardized cost when controlling for the other variables in the model. c A relative cost of means that within hospitals there is a 11.8% relative increase in cost among CAP1acute asthma patients compared with CAP-only patients when controlling for the other variables in the model. d Adjusted for gender, insurance, age group, race, proportion of blacks at the hospital, and ICU stay. e There is a 5.6% relative increase in LOS among CAP1acute asthma patients compared with CAP only patients when controlling for the other variables in the model. f Adjusted for gender, insurance, age group, race, ICU stay, and mean number of hospital beds. g Controlling for other factors in the model, when 3 4 vs1 2 guidelines are adhered to, there is a relative increase in total standardized cost of 20%. When 5 guidelines vs 1 2 guidelines are adhered to, there is a 40% relative increase in cost. As the mean number of guidelines adhered to at a hospital increases, the relative cost of CAP1acute asthma patients decreases by 18%; for CAP-only patients, the relative total standardized cost decreases 16%. testing. Approximately 30% in each group received respiratory viral panel testing. Across hospitals, the range of the percent of guideline adherence was wide for all of the guidelines except testing for M pneumoniae and C pneumoniae. At the patient-level, greater guideline adherence was associated with higher cost. However, contrasting adherence across hospitals, greater hospital-level guideline adherence was associated with lower average cost per hospitalization (Table 2). DISCUSSION We found a high percentage of cases of pneumonia that had a codiagnosis of and treatment for asthma exacerbation; although we used an algorithm for identifying CAP that has been validated with chart review and radiology data, the presence of an infiltrate on a chest x-ray may not always represent pneumonia but may in fact be atelectasis in a case of primary asthma. In addition, we may be overidentifying cases of asthma in which albuterol is being used inappropriately. Regardless of whether these cases are misdiagnoses or are truly patients with pneumonia and asthma, this study demonstrated the challenge of measuring guideline adherence in the face of codiagnoses and diagnostic uncertainty, particularly in the management of common, acute pulmonary processes in children. In this cohort of patients admitted to 42 children s hospitals, codiagnosis resulted in broader variation in management and higher cost. These results also highlight the complexity of implementing guidelines where there is true codiagnosis or diagnostic uncertainty in carefully identifying the appropriate target population for guideline development and management so that when comparing outcomes, hospitals are using the clinical groups of patients. Overall, CAP1asthma patients within the same hospital had higher costs and longer LOS than those with CAP alone. There was significant variability in cost and LOS among the hospitals for both CAP and CAP1 asthma. Although having a second diagnosis may inherently increase overall cost, a secondary diagnosis of asthma also increased observed variation in costs across hospitals, suggesting that the addition of the second diagnosis may increase uncertainty. This could be diagnostic uncertainty, management uncertainty, or both. Inappropriate diagnosis with a second disease process could result in overuse or misuse of nonrecommended care, and therefore higher costs. Increasing diagnostic precision and standardizing treatment of codiagnoses such as CAP1asthma may 420 WILSON et al

7 FIGURE 3 Distribution of length of stay by clinical group and hospital (n 5 s40). help to decrease interhospital variability in cost. In particular, adhering to the recommendation not to get a chest radiograph in children admitted with clinical asthma exacerbations might significantly decrease the overall cost and variationincare.themeanlosforcap1 asthma of 2.1 days was longer than that reported in another PHIS study for noncomplex asthma alone (1.8 days), 19 also supporting the idea that the additional diagnosis adds complexity. Future studies examining the impact of a pneumonia diagnosis on variation in care for asthma exacerbations may provide corollary information. Overall, hospitals that had greater adherence to the CAP guidelines across their patient population had lower the overall costs for CAP and CAP1asthma, suggesting that although some guidelines may be applied inappropriately, especially for CAP1asthma, standardization of care has some association with lower costs of care. Because adherence to guidelines for both CAP and asthma are being used as quality metrics in some institutions, it may be helpful to use these as metrics for patients only when a codiagnosis is not present. Studies using administrative data are inherently limited by the quality of the data provided by the hospitals, and there are many potential explanatory variables that are not available to us in PHIS. Although PHIS has excellent quality control standards, its data are not routinely validated with chart review. We used an algorithm for diagnosing CAP that has been validated with chart review, 11 but it is nonetheless possible that there was misclassification for both the CAP and asthma diagnoses. In addition, we used antibiotic choice to select out cases of CAP, which meant that we could not include antibiotic selection in our analysis of guideline adherence. Our definition of acute asthma exacerbation may cause us to underestimate such cases. We did not include corticosteroid administration in our definition because corticosteroids, particularly at some hospitals, may be administered to children with CAP. 14 This approach would bias the results to the null hypothesis. We also had a significant number of exclusions to create our final cohort; some of these may have biased our data. Although the pneumonia guidelines have recommendations related to M pneumoniae and C pneumoniae testing, the lack of timely availability of results for these tests at many institutions is likely to be an important barrier to their use. The data are retrospective, and thus we cannot assume causation. Because we limited our analyses to children.2 years of age, this may have increased the potential for asthma codiagnoses. Finally, our data may not be generalizable outside of freestanding children s hospitals. CONCLUSIONS A codiagnosis of acute asthma is common for children with CAP, adding a layer of treatment complexity that may increase resource utilization and LOS, regardless of whether there is diagnostic misclassification or whether there are truly 2 disease processes. There is still a high degree of uncertainty surrounding the most effective and efficient way to treat CAP1 asthma, and the appropriateness of existing guidelines to address the co-occurrence of these conditions. Clinicians should be clear about which diagnosis they are treating, which guideline should be applied when the clinician is unsure, or whether 2 diagnoses are clearly present. Patients with 2 diagnoses deserve to have both diagnoses treated according to evidence-based protocols. In the interim, hospitals can examine their practice patterns for CAP1 asthma and if they are outliers, work to standardize and streamline care. As we increasingly rely on guidelines for the care of children hospitalized with common diseases, it is important to remember that they often have.1 diagnosis, and these guidelines should incorporate evidence about common co-occurring conditions as well as provide recommendations on their treatment. HOSPITAL PEDIATRICS Volume 5, Issue 8, August

8 REFERENCES 1. Keren R, Luan X, Localio R, et al; Pediatric Research in Inpatient Settings (PRIS) Network. Prioritization of comparative effectiveness research topics in hospital pediatrics. Arch Pediatr Adolesc Med. 2012;166(12): Williams GJ, Macaskill P, Kerr M, et al. Variability and accuracy in interpretation of consolidation on chest radiography for diagnosing pneumonia in children under 5 years of age. Pediatr Pulmonol. 2013;48(12): Talbot TR, Hartert TV, Mitchel E, et al. Asthma as a risk factor for invasive pneumococcal disease. N Engl J Med. 2005;352(20): Bradley JS, Byington CL, Shah SS, et al; Pediatric Infectious Diseases Society and the Infectious Diseases Society of America. The management of community-acquired pneumonia in infants and children older than 3 months of age: clinical practice guidelines by the Pediatric Infectious Diseases Society and the Infectious Diseases Society of America. Clin Infect Dis. 2011;53(7):e25 e76 5. National Asthma Education and Prevention Program. Expert Panel Report 3 (EPR-3): Guidelines for the Diagnosis and Management of Asthma- Summary Report J Allergy Clin Immunol. 2007;120(5 Suppl):S94 S Snijders D, Daniels JM, de Graaff CS, van der Werf TS, Boersma WG. Efficacy of corticosteroids in community-acquired pneumonia: a randomized double-blinded clinical trial. Am J Respir Crit Care Med. 2010;181(9): Quinonez RA, Garber MD, Schroeder AR, et al. Choosing wisely in pediatric hospital medicine: five opportunities for improved healthcare value. J Hosp Med. 2013;8(9): Brogan TV, Hall M, Williams DJ, et al. Variability in processes of care and outcomes among children hospitalized with community-acquired pneumonia. Pediatr Infect Dis J. 2012;31(10): Morse RB, Hall M, Fieldston ES, et al. Hospital-level compliance with asthma care quality measures at children s hospitals and subsequent asthmarelated outcomes. JAMA. 2011;306(13): Mongelluzzo J, Mohamad Z, Ten Have TR, Shah SS. Impact of bacterial meningitisassociated conditions on pediatric inpatient resource utilization. J Hosp Med. 2010;5(6):E1 E7 11. Williams DJ, Shah SS, Myers A, et al. Identifying pediatric communityacquired pneumonia hospitalizations: Accuracy of administrative billing codes. JAMA Pediatr. 2013;167(9): Ambroggio L, Tabb LP, O Meara T, Sheffler-Collins S, McGowan KL, Shah SS. Influence of antibiotic susceptibility patterns on empiric antibiotic prescribing for children hospitalized with community-acquired pneumonia. Pediatr Infect Dis J. 2012; 31(4): Feudtner C, Hays RM, Haynes G, Geyer JR, Neff JM, Koepsell TD. Deaths attributed to pediatric complex chronic conditions: national trends and implications for supportive care services. Pediatrics. 2001;107(6). Available at: content/full/107/6/e Weiss AK, Hall M, Lee GE, Kronman MP, Sheffler-Collins S, Shah SS. Adjunct corticosteroids in children hospitalized with community-acquired pneumonia. Pediatrics. 2011;127(2):e255 e Drummond MF, Schulpher MJ, Torrance GW, O Brien BJ, Stoddart GL. Methods for the Economic Evaluation of Health Care Programmes. 2nd ed. Oxford, UK: Oxford University Press; Berlin JA, Kimmel SE, Ten Have TR, Sammel MD. An empirical comparison of several clustered data approaches under confounding due to cluster effects in the analysis of complications of coronary angioplasty. Biometrics. 1999; 55(2): Neuhaus JM, Kalbfleisch JD. Betweenand within-cluster covariate effects in the analysis of clustered data. Biometrics. 1998;54(2): Begg MD, Parides MK. Separation of individual-level and cluster-level covariate effects in regression analysis of correlated data. Stat Med. 2003; 22(16): Morse RB, Hall M, Fieldston ES, et al. Children s hospitals with shorter lengths of stay do not have higher readmission rates. J Pediatr. 2013;163(4):1034, e1 422 WILSON et al

9 Hospitalization for Community-Acquired Pneumonia in Children: Effect of an Asthma Codiagnosis Karen M. Wilson, Michelle R. Torok, Russell Localio, Lisa McLeod, Rajendu Srivastava, Xianqun Luan, Zeinab Mohamad, Samir S. Shah and for the Pediatric Research in Inpatient Settings (PRIS) Network Hospital Pediatrics 2015;5;415 DOI: /hpeds Updated Information & Services References Subspecialty Collections Permissions & Licensing Reprints including high resolution figures, can be found at: This article cites 17 articles, 1 of which you can access for free at: This article, along with others on similar topics, appears in the following collection(s): Asthma btopic Hospital Medicine edicine_sub Pulmonology gy_sub Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: Information about ordering reprints can be found online:

10 Hospitalization for Community-Acquired Pneumonia in Children: Effect of an Asthma Codiagnosis Karen M. Wilson, Michelle R. Torok, Russell Localio, Lisa McLeod, Rajendu Srivastava, Xianqun Luan, Zeinab Mohamad, Samir S. Shah and for the Pediatric Research in Inpatient Settings (PRIS) Network Hospital Pediatrics 2015;5;415 DOI: /hpeds The online version of this article, along with updated information and services, is located on the World Wide Web at: Hospital Pediatrics is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since Hospital Pediatrics is owned, published, and trademarked by the American Academy of Pediatrics, 345 Park Avenue, Itasca, Illinois, Copyright 2015 by the American Academy of Pediatrics. All rights reserved. Print ISSN:

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