BRIEF REPORT
Emergency Department Visits Related to Clostridium difficile Infection: Results From the Nationwide Emergency Department Sample, 2006 Through 2010 Chaitanya Pant, MD, Thomas J. Sferra, MD, Mojtaba Olyaee, MD, Richard Gilroy, MD, Michael P. Anderson, PhD, Amit Rastogi, MD, Prashant K. Pandya, DO, and Abhishek Deshpande, MD, PhD
Abstract Objectives: The objective was to estimate emergency department (ED) visits for Clostridium difficile infection in the United States for the years 2006 through 2010. Methods: Estimates of ED visits for C. difficile infection were calculated in patients 18 years and older using the Nationwide Emergency Department Sample. Results: During the calendar years 2006 through 2010, there were an estimated total of 491,406,018 ED visits. Of these, 462,160 ED visits were associated with a primary International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis of C. difficile. The C. difficile infection ED visit rate (visits/ 100,000 census population) increased from 34.1 in 2006 to 42.3 in 2010, an increase of 24% (p < 0.01). There was also a significant overall increased trend in the number of ED visits for C. difficile from 2006 through 2010 (p < 0.01). The highest ED visit rate for C. difficile was observed for patients 65 years and older (163.18 per 100,000), while the lowest visit rate was for patients aged 18 to 24 years (5.10 per 100,000). The greatest increase in C. difficile infection visits occurred in the age group 18 to 24 years. Conclusions: These results indicate an increased trend of ED visits for C. difficile in the period 2006 through 2010 with an overall population-adjusted increase of 24%. This represents important complementary data to previous studies reporting an increase in the rate of C. difficile infections in the U.S. hospitalized population. ACADEMIC EMERGENCY MEDICINE 2015;22:117–119 © 2014 by the Society for Academic Emergency Medicine
C
lostridium difficile is the major cause of nosocomial diarrhea in the United States. In the past several years both hospital- and communityacquired cases have increased significantly, which coincides with the emergence of a hypervirulent strain of the bacterium. Recently, Halabi et al.1 interrogated a nationwide U.S. inpatient hospital database for the
years 2001 through 2010 and reported a 47% increase in the rate of C. difficile infection. However, these data are derived from a hospitalized cohort of patients and do not accurately represent the burden of disease encountered by medical providers in the emergency department (ED). The goal of our study was to determine the burden of C. difficile infection in patients pre-
From the Division of Gastroenterology, Hepatology and Motility, Department of Internal Medicine, University of Kansas Medical Center (CP, MO, RG, AR, PKP), Kansas City, KS; the Division of Pediatric Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Case Western Reserve University School of Medicine, UH Rainbow Babies & Children’s Hospital (TJS), Cleveland, OH; the Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center (MPA), Oklahoma City, OK; and the Medicine Institute Center for Value Based Care Research and Department of Infectious Diseases, Medicine Institute, Cleveland Clinic (AD), Cleveland, OH. Received June 22, 2014; revision received August 12, 2014; accepted August 16, 2014. Presented at the 2014 Combined Annual Meeting of the Central Society for Clinical and Translational Research (CSCTR) and the Midwestern Section of the American Federation for Medical Research (MWAFMR) Annual Meeting, Chicago, IL, April 2014. The authors have no relevant financial information or potential conflicts to disclose. Supervising Editor: Elizabeth Alpern, MD, MSCE. Address for correspondence and reprints: Chaitanya Pant, MD; e-mail: [email protected]
© 2014 by the Society for Academic Emergency Medicine doi: 10.1111/acem.12552
ISSN 1069-6563 PII ISSN 1069-6563583
117 117
118
senting to EDs. We therefore analyzed a national ED database to study exclusively those patients who presented to these facilities with a primary diagnosis of C. difficile infection. METHODS Study Design This was a cohort study using the Healthcare Cost and Utilization Project Nationwide Emergency Department Sample (HCUP-NEDS) years 2006 through 2010. Data Source The NEDS is a component database of the HCUP sponsored by the Agency for Healthcare Research and Quality.2 The NEDS is constructed using a 20% stratified sample of U.S. hospital-based EDs to ensure that it is representative of the entire country. To obtain nationwide estimates, weights were developed using the American Hospital Association universe as the standard.2 The 2010 HCUP-NEDS comprises approximately 28 million ED visits sampled from 961 hospitals in 29 U.S. states representing a 20% stratified sample of U.S. hospital-based EDs. After weighting, national estimates pertain to almost 130 million ED visits in 2010. The NEDS contains event-level records, not patient-level records; individual patients who visit the ED more than once in a year may be recorded in the NEDS multiple times. Each ED visit entry contains one primary discharge diagnosis, one to 14 secondary diagnoses, one to nine procedure codes (based on the International Classification of Diseases, Ninth Revision, Clinical Modification [ICD-9-CM], diagnosis and procedure codes), demographic information, details of disposition from the ED, and details pertaining to hospitalizations that occurred from the ED (mortality, total charges, and length of stay [LOS]). Variable Definition The predictor variable was the presence of a diagnosis of C. difficile infection. Adult patients were identified starting at age 18 years. We extracted all entries with a primary discharge diagnosis of C. difficile infection (ICD-9-CM code 008.45).
Pant et al. • ED VISITS FOR C. DIFFICILE INFECTION
491,406,018 ED visits. There were 462,160 of these visits associated with an ICD-9 primary diagnosis of C. difficile infection. The ED visit rate (visits/100,000 census population) for C. difficile increased from 34.1 (95% confidence interval [CI] = 33.8 to 34.3) in 2006 to 42.3 (95% CI = 42.0 to 42.5) in 2010; this represented an increase of 24% (p < 0.01). We also observed a significant increased trend in the number of ED visits for C. difficile from 2006 through 2010 (p < 0.01). In an analysis of combined data 2006 through 2010, the highest C. difficile ED visit rate was recorded in patients 65 years and older (163.2; 95% CI = 162.6 to 163.7), while the lowest incidence was in patients ages 18 to 24 years (5.1; 95% CI = 5.0 to 5.2). A significant increase in C. difficile infection ED visits was noted in each of the age groups under study (Figure 1). The greatest percentage increase in ED visits for C. difficile occurred in the 18- to 24-year age group. A total of 427,389 (92.5%) C. difficile cases evaluated in the ED resulted in hospital admission; 16,309 (3.8%) of these patients died during their hospitalizations. Inpatient and ED charges increased during the period of the study, from a median of $20,000 (Interquartile range [IQR] = $12,000 to $36,000) in 2006 to $24,000 (IQR = $14,000 to $41,000) in 2010 (p < 0.01). LOS remained constant at a median of 5 days (IQR = 3 to 8 days) for the study period. DISCUSSION The C. difficile infection represents an enormous and increasing health care problem in the United States. Several studies have focused on C. difficile–related hospitalizations using large, national databases such as the Nationwide inpatient sample (NIS).1,3 However, to address the full effect and burden of this disease, C. difficile–related ED visits must be included in the overall analysis. Our results from the NEDS demonstrate an increased trend of ED visits for C. difficile infection for the years 2006 through 2010. The highest incidence rate of ED visits for C. difficile was observed for patients 65 years and older. Advanced age is a well-recognized risk factor for C. difficile infection.4 The greatest increase in C. difficile ED visits occurred in the age group 18 to 24 years. This is
Data Analysis Statistical analyses were performed using SAS (version 9.3). The ED visit rate associated with C. difficile infection was expressed per 100,000 census population, thereby adjusting for the increase in the U.S. population. Data were obtained from the U.S. Census Bureau, Population Division, Annual Estimates of the Population for the United States, Regions, and Divisions and U.S. Census Bureau, Current Population Reports. The chisquare and Kruskal-Wallis tests were used to compare differences between categorical and continuous variables, respectively. For trend analysis, we used the Cochran-Armitage test. The threshold for significance for all analyses was p < 0.01 due to large sample size. RESULTS In the United States during the calendar years 2006 through 2010, there were an estimated total of
Figure 1. Increase in population-based incidence of C. difficile infection (CDI)-related ED visits in the United States from 2006 through 2010. Data from the Healthcare Cost and Utilization Project Nationwide Emergency Department Sample (HCUPNEDS).
ACADEMIC EMERGENCY MEDICINE • January 2015, Vol. 22, No. 1 • www.aemj.org
consistent with reports that community-acquired C. difficile is increasing in incidence and affects younger adults who lack traditional risk factors for the infection.5 A large proportion (more than 90%) of patients presenting to the ED with C. difficile were admitted to the hospital. In contrast, using the NEDS, Self et al.6 reported that approximately 39% of pneumonia cases diagnosed in the ED were managed on a treat-andrelease outpatient basis. Patients admitted to the hospital with C. difficile use considerable resources in terms of both hospital charges and LOS. While hospital charges increased during the period of study, the LOS remained constant. In interpreting the study data, we examined two important considerations. First, individuals may have been admitted to the hospital with an alternate medical diagnosis and subsequently developed C. difficile as inpatients. However, we included only a primary discharge diagnosis of C. difficile infection in our study, and an HCUP special report concluded that the primary discharge diagnosis accurately represented the “code for the diagnosis, condition, problem or other reason encounter/visit shown in the medical record to be chiefly responsible for the services provided.”7 Second, the high rate of admission for C. difficile cases may have been the result of an information bias. Patients presenting with moderate to severe symptoms of colitis and other exigent circumstances such as advanced age and comorbid conditions likely received strong initial consideration for hospital admission, and C. difficile testing was subsequently completed on an inpatient basis. Conversely, patients in overall better health and with milder symptoms may have been discharged without completing testing for C. difficile. LIMITATIONS The NEDS lacks data detailing laboratory results and therefore we relied exclusively on the use of ICD-9 codes for the identification of cases of C. difficile infection. Although multiple studies have shown good correlation between ICD-9 codes and toxin assay results,8,9 this may have resulted in a falsely elevated estimation of ED visits for C. difficile.10 We excluded patients with secondary diagnoses of C. difficile infection, which may have resulted in an overestimation of the overall admission rate. Conversely, since we also excluded patients with alternate primary diagnoses such as diarrhea, our search methodology may have underestimated the true number of ED visits for C. difficile. There is an absence of individual identifiers in the NEDS, and one patient may potentially account for several ED visits. The widespread use of real-time polymerase chain reaction assays that have enhanced sensitivity for C. difficile detection may partly account for our observation of increased disease-related ED visits. Finally, our results represent a weighted estimate of national data. CONCLUSIONS Our analysis of the Nationwide Emergency Department Sample data indicates an increased trend of ED visits
119
for C. difficile infection in the period 2006 through 2010, with an overall population-adjusted increase of 24.0%. These data represent important complementary information to the study of the overall effect of C. difficile infection in the United States. The authors acknowledge Healthcare Cost and Utilization Project Healthcare Cost and Utilization Project Nationwide Emergency Department Sample (HCUP-NEDS) sponsored by the Agency for Healthcare Research and Quality that contribute to HCUP (http:// www.hcup-us.ahrq.gov/db/hcupdatapartners.jsp)
References 1. Halabi WJ, Nguyen VQ, Carmichael JC, Pigazzi A, Stamos MJ, Mills S. Clostridium difficile colitis in the United States: a decade of trends, outcomes, risk factors for colectomy, and mortality after colectomy. J Am Coll Surg 2013;217:802–12. 2. Agency for Healthcare Research and Quality, Healthcare Cost and Utilization Project. Overview of the Nationwide Emergency Department Sample (NEDS). Available at: www.hcup-us.ahrq.gov/nedsoverview.jsp. Accessed Oct 20, 2014. 3. Lucado J, Gould C, Elixhauser A. Clostridium Difficile Infections (CDI) in Hospital Stays, 2009: Statistical Brief #124. Rockville, MD: Healthcare Cost and Utilization Project, 2006. 4. Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol 2010;31:431–55. 5. Khanna S, Pardi DS, Aronson SL, et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol 2012;107:89–95. 6. Self WH, Grijalva CG, Zhu Y, et al. Rates of emergency department visits due to pneumonia in the United States, July 2006-June 2009. Acad Emerg Med 2013;20:957–60. 7. Senathirajah M OP, Mutter R, Nagamine M. Special Study on the Meaning of the First-Listed Diagnosis on Emergency Department and Ambulatory Surgery Records. HCUP Methods Series Report # 2011-03. Available at: http://www.hcup-us.ahrq.gov/ reports/methods/2011_03.pdf. Accessed Oct 20, 2015. 8. Dubberke ER, Reske KA, McDonald LC, Fraser VJ. ICD-9 codes and surveillance for Clostridium difficile-associated disease. Emerg Infect Dis 2006;12: 1576–9. 9. Scheurer DB, Hicks LS, Cook EF, Schnipper JL. Accuracy of ICD-9 coding for Clostridium difficile infections: a retrospective cohort. Epidemiol Infect 2007;135:1010–3. 10. Dubberke ER, Butler AM, Nyazee HA, et al. The impact of ICD-9-CM code rank order on the estimated prevalence of Clostridium difficile infections. Clin Infec Dis 2011;53:20–5.
Emergency Department Visits Related to Clostridium difficile Infection: Results From the Nationwide Emergency Department Sample, 2006 Through 2010 Chaitanya Pant, MD, Thomas J. Sferra, MD, Mojtaba Olyaee, MD, Richard Gilroy, MD, Michael P. Anderson, PhD, Amit Rastogi, MD, Prashant K. Pandya, DO, and Abhishek Deshpande, MD, PhD
Abstract Objectives: The objective was to estimate emergency department (ED) visits for Clostridium difficile infection in the United States for the years 2006 through 2010. Methods: Estimates of ED visits for C. difficile infection were calculated in patients 18 years and older using the Nationwide Emergency Department Sample. Results: During the calendar years 2006 through 2010, there were an estimated total of 491,406,018 ED visits. Of these, 462,160 ED visits were associated with a primary International Classification of Diseases, Ninth Revision, Clinical Modification diagnosis of C. difficile. The C. difficile infection ED visit rate (visits/ 100,000 census population) increased from 34.1 in 2006 to 42.3 in 2010, an increase of 24% (p < 0.01). There was also a significant overall increased trend in the number of ED visits for C. difficile from 2006 through 2010 (p < 0.01). The highest ED visit rate for C. difficile was observed for patients 65 years and older (163.18 per 100,000), while the lowest visit rate was for patients aged 18 to 24 years (5.10 per 100,000). The greatest increase in C. difficile infection visits occurred in the age group 18 to 24 years. Conclusions: These results indicate an increased trend of ED visits for C. difficile in the period 2006 through 2010 with an overall population-adjusted increase of 24%. This represents important complementary data to previous studies reporting an increase in the rate of C. difficile infections in the U.S. hospitalized population. ACADEMIC EMERGENCY MEDICINE 2015;22:117–119 © 2014 by the Society for Academic Emergency Medicine
C
lostridium difficile is the major cause of nosocomial diarrhea in the United States. In the past several years both hospital- and communityacquired cases have increased significantly, which coincides with the emergence of a hypervirulent strain of the bacterium. Recently, Halabi et al.1 interrogated a nationwide U.S. inpatient hospital database for the
years 2001 through 2010 and reported a 47% increase in the rate of C. difficile infection. However, these data are derived from a hospitalized cohort of patients and do not accurately represent the burden of disease encountered by medical providers in the emergency department (ED). The goal of our study was to determine the burden of C. difficile infection in patients pre-
From the Division of Gastroenterology, Hepatology and Motility, Department of Internal Medicine, University of Kansas Medical Center (CP, MO, RG, AR, PKP), Kansas City, KS; the Division of Pediatric Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, Case Western Reserve University School of Medicine, UH Rainbow Babies & Children’s Hospital (TJS), Cleveland, OH; the Department of Biostatistics and Epidemiology, University of Oklahoma Health Sciences Center (MPA), Oklahoma City, OK; and the Medicine Institute Center for Value Based Care Research and Department of Infectious Diseases, Medicine Institute, Cleveland Clinic (AD), Cleveland, OH. Received June 22, 2014; revision received August 12, 2014; accepted August 16, 2014. Presented at the 2014 Combined Annual Meeting of the Central Society for Clinical and Translational Research (CSCTR) and the Midwestern Section of the American Federation for Medical Research (MWAFMR) Annual Meeting, Chicago, IL, April 2014. The authors have no relevant financial information or potential conflicts to disclose. Supervising Editor: Elizabeth Alpern, MD, MSCE. Address for correspondence and reprints: Chaitanya Pant, MD; e-mail: [email protected]
© 2014 by the Society for Academic Emergency Medicine doi: 10.1111/acem.12552
ISSN 1069-6563 PII ISSN 1069-6563583
117 117
118
senting to EDs. We therefore analyzed a national ED database to study exclusively those patients who presented to these facilities with a primary diagnosis of C. difficile infection. METHODS Study Design This was a cohort study using the Healthcare Cost and Utilization Project Nationwide Emergency Department Sample (HCUP-NEDS) years 2006 through 2010. Data Source The NEDS is a component database of the HCUP sponsored by the Agency for Healthcare Research and Quality.2 The NEDS is constructed using a 20% stratified sample of U.S. hospital-based EDs to ensure that it is representative of the entire country. To obtain nationwide estimates, weights were developed using the American Hospital Association universe as the standard.2 The 2010 HCUP-NEDS comprises approximately 28 million ED visits sampled from 961 hospitals in 29 U.S. states representing a 20% stratified sample of U.S. hospital-based EDs. After weighting, national estimates pertain to almost 130 million ED visits in 2010. The NEDS contains event-level records, not patient-level records; individual patients who visit the ED more than once in a year may be recorded in the NEDS multiple times. Each ED visit entry contains one primary discharge diagnosis, one to 14 secondary diagnoses, one to nine procedure codes (based on the International Classification of Diseases, Ninth Revision, Clinical Modification [ICD-9-CM], diagnosis and procedure codes), demographic information, details of disposition from the ED, and details pertaining to hospitalizations that occurred from the ED (mortality, total charges, and length of stay [LOS]). Variable Definition The predictor variable was the presence of a diagnosis of C. difficile infection. Adult patients were identified starting at age 18 years. We extracted all entries with a primary discharge diagnosis of C. difficile infection (ICD-9-CM code 008.45).
Pant et al. • ED VISITS FOR C. DIFFICILE INFECTION
491,406,018 ED visits. There were 462,160 of these visits associated with an ICD-9 primary diagnosis of C. difficile infection. The ED visit rate (visits/100,000 census population) for C. difficile increased from 34.1 (95% confidence interval [CI] = 33.8 to 34.3) in 2006 to 42.3 (95% CI = 42.0 to 42.5) in 2010; this represented an increase of 24% (p < 0.01). We also observed a significant increased trend in the number of ED visits for C. difficile from 2006 through 2010 (p < 0.01). In an analysis of combined data 2006 through 2010, the highest C. difficile ED visit rate was recorded in patients 65 years and older (163.2; 95% CI = 162.6 to 163.7), while the lowest incidence was in patients ages 18 to 24 years (5.1; 95% CI = 5.0 to 5.2). A significant increase in C. difficile infection ED visits was noted in each of the age groups under study (Figure 1). The greatest percentage increase in ED visits for C. difficile occurred in the 18- to 24-year age group. A total of 427,389 (92.5%) C. difficile cases evaluated in the ED resulted in hospital admission; 16,309 (3.8%) of these patients died during their hospitalizations. Inpatient and ED charges increased during the period of the study, from a median of $20,000 (Interquartile range [IQR] = $12,000 to $36,000) in 2006 to $24,000 (IQR = $14,000 to $41,000) in 2010 (p < 0.01). LOS remained constant at a median of 5 days (IQR = 3 to 8 days) for the study period. DISCUSSION The C. difficile infection represents an enormous and increasing health care problem in the United States. Several studies have focused on C. difficile–related hospitalizations using large, national databases such as the Nationwide inpatient sample (NIS).1,3 However, to address the full effect and burden of this disease, C. difficile–related ED visits must be included in the overall analysis. Our results from the NEDS demonstrate an increased trend of ED visits for C. difficile infection for the years 2006 through 2010. The highest incidence rate of ED visits for C. difficile was observed for patients 65 years and older. Advanced age is a well-recognized risk factor for C. difficile infection.4 The greatest increase in C. difficile ED visits occurred in the age group 18 to 24 years. This is
Data Analysis Statistical analyses were performed using SAS (version 9.3). The ED visit rate associated with C. difficile infection was expressed per 100,000 census population, thereby adjusting for the increase in the U.S. population. Data were obtained from the U.S. Census Bureau, Population Division, Annual Estimates of the Population for the United States, Regions, and Divisions and U.S. Census Bureau, Current Population Reports. The chisquare and Kruskal-Wallis tests were used to compare differences between categorical and continuous variables, respectively. For trend analysis, we used the Cochran-Armitage test. The threshold for significance for all analyses was p < 0.01 due to large sample size. RESULTS In the United States during the calendar years 2006 through 2010, there were an estimated total of
Figure 1. Increase in population-based incidence of C. difficile infection (CDI)-related ED visits in the United States from 2006 through 2010. Data from the Healthcare Cost and Utilization Project Nationwide Emergency Department Sample (HCUPNEDS).
ACADEMIC EMERGENCY MEDICINE • January 2015, Vol. 22, No. 1 • www.aemj.org
consistent with reports that community-acquired C. difficile is increasing in incidence and affects younger adults who lack traditional risk factors for the infection.5 A large proportion (more than 90%) of patients presenting to the ED with C. difficile were admitted to the hospital. In contrast, using the NEDS, Self et al.6 reported that approximately 39% of pneumonia cases diagnosed in the ED were managed on a treat-andrelease outpatient basis. Patients admitted to the hospital with C. difficile use considerable resources in terms of both hospital charges and LOS. While hospital charges increased during the period of study, the LOS remained constant. In interpreting the study data, we examined two important considerations. First, individuals may have been admitted to the hospital with an alternate medical diagnosis and subsequently developed C. difficile as inpatients. However, we included only a primary discharge diagnosis of C. difficile infection in our study, and an HCUP special report concluded that the primary discharge diagnosis accurately represented the “code for the diagnosis, condition, problem or other reason encounter/visit shown in the medical record to be chiefly responsible for the services provided.”7 Second, the high rate of admission for C. difficile cases may have been the result of an information bias. Patients presenting with moderate to severe symptoms of colitis and other exigent circumstances such as advanced age and comorbid conditions likely received strong initial consideration for hospital admission, and C. difficile testing was subsequently completed on an inpatient basis. Conversely, patients in overall better health and with milder symptoms may have been discharged without completing testing for C. difficile. LIMITATIONS The NEDS lacks data detailing laboratory results and therefore we relied exclusively on the use of ICD-9 codes for the identification of cases of C. difficile infection. Although multiple studies have shown good correlation between ICD-9 codes and toxin assay results,8,9 this may have resulted in a falsely elevated estimation of ED visits for C. difficile.10 We excluded patients with secondary diagnoses of C. difficile infection, which may have resulted in an overestimation of the overall admission rate. Conversely, since we also excluded patients with alternate primary diagnoses such as diarrhea, our search methodology may have underestimated the true number of ED visits for C. difficile. There is an absence of individual identifiers in the NEDS, and one patient may potentially account for several ED visits. The widespread use of real-time polymerase chain reaction assays that have enhanced sensitivity for C. difficile detection may partly account for our observation of increased disease-related ED visits. Finally, our results represent a weighted estimate of national data. CONCLUSIONS Our analysis of the Nationwide Emergency Department Sample data indicates an increased trend of ED visits
119
for C. difficile infection in the period 2006 through 2010, with an overall population-adjusted increase of 24.0%. These data represent important complementary information to the study of the overall effect of C. difficile infection in the United States. The authors acknowledge Healthcare Cost and Utilization Project Healthcare Cost and Utilization Project Nationwide Emergency Department Sample (HCUP-NEDS) sponsored by the Agency for Healthcare Research and Quality that contribute to HCUP (http:// www.hcup-us.ahrq.gov/db/hcupdatapartners.jsp)
References 1. Halabi WJ, Nguyen VQ, Carmichael JC, Pigazzi A, Stamos MJ, Mills S. Clostridium difficile colitis in the United States: a decade of trends, outcomes, risk factors for colectomy, and mortality after colectomy. J Am Coll Surg 2013;217:802–12. 2. Agency for Healthcare Research and Quality, Healthcare Cost and Utilization Project. Overview of the Nationwide Emergency Department Sample (NEDS). Available at: www.hcup-us.ahrq.gov/nedsoverview.jsp. Accessed Oct 20, 2014. 3. Lucado J, Gould C, Elixhauser A. Clostridium Difficile Infections (CDI) in Hospital Stays, 2009: Statistical Brief #124. Rockville, MD: Healthcare Cost and Utilization Project, 2006. 4. Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol 2010;31:431–55. 5. Khanna S, Pardi DS, Aronson SL, et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol 2012;107:89–95. 6. Self WH, Grijalva CG, Zhu Y, et al. Rates of emergency department visits due to pneumonia in the United States, July 2006-June 2009. Acad Emerg Med 2013;20:957–60. 7. Senathirajah M OP, Mutter R, Nagamine M. Special Study on the Meaning of the First-Listed Diagnosis on Emergency Department and Ambulatory Surgery Records. HCUP Methods Series Report # 2011-03. Available at: http://www.hcup-us.ahrq.gov/ reports/methods/2011_03.pdf. Accessed Oct 20, 2015. 8. Dubberke ER, Reske KA, McDonald LC, Fraser VJ. ICD-9 codes and surveillance for Clostridium difficile-associated disease. Emerg Infect Dis 2006;12: 1576–9. 9. Scheurer DB, Hicks LS, Cook EF, Schnipper JL. Accuracy of ICD-9 coding for Clostridium difficile infections: a retrospective cohort. Epidemiol Infect 2007;135:1010–3. 10. Dubberke ER, Butler AM, Nyazee HA, et al. The impact of ICD-9-CM code rank order on the estimated prevalence of Clostridium difficile infections. Clin Infec Dis 2011;53:20–5.
