Abstract
This study aimed to analyze temporal trends by gender and age in Clostridium difficile infection (CDI)-related hospitalization rates in the Autonomous Community of Madrid (Spain) over a 12-year period. A population-based cross-sectional study of all hospital admissions with a CDI diagnosis from 2003 to 2014 was carried out. Annual age-specific hospitalization rates were calculated by gender. All the analyses were performed separately for total hospitalizations and hospitalizations with CDI as the primary diagnosis. Joinpoint regression models were used to analyze time trends. A total of 13,526 hospital discharges were identified (26.8 % with CDI as the primary diagnosis). In both sexes, a gradient in age-specific rates was observed, ranging in 2014 from 5.92 hospitalizations per 100,000 person-years in patients <15 years of age to 378.96 in patients ≥85 years of age. Since 2009, in the age group of 15–44 years, both men and women presented an increasing trend of around 18 %. A significantly increasing trend was detected in women of age 45–84 years, with an estimated annual percentage of change of 7.6 % in the age group of 45–64 years, and rounding with 4.5 % in the age group of 65–84 years. In men of age 45–64 years, the average annual percentage of increase was 4.7 %, and it was 21.1 % between 2010 and 2014 in the age group of 65–74 years. No trends were identified in the 85 years and over age group. Surveillance methods to assess trends by age group should be implemented. Preventive and therapeutic initiatives should remain a priority.
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References
Bujanda L, Cosme A (2009) Clostridium-difficile-associated diarrhea. Gastroenterol Hepatol 32:48–56
Leffler DA, Lamont JT (2015) Clostridium difficile infection. N Engl J Med 372:1539–1548
Leffler DA, Lamont JT (2009) Treatment of Clostridium difficile-associated disease. Gastroenterology 136:1899–1912
Debast SB, Bauer MP, Kuijper EJ; European Society of Clinical Microbiology and Infectious Diseases (2014) European Society of Clinical Microbiology and Infectious Diseases: update of the treatment guidance document for Clostridium difficile infection. Clin Microbiol Infect 20(Suppl 2):1–26
Lo Vecchio A, Zacur GM (2012) Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options. Curr Opin Gastroenterol 28:1–9
Asensio A, Vaque-Rafart J, Calbo-Torrecillas F, Gestal-Otero JJ, López-Fernández F, Trilla-Garcia A et al (2008) Increasing rates in Clostridium difficile infection (CDI) among hospitalised patients, Spain 1999–2007. Euro Surveill 13. pii: 18943
Chitnis AS, Holzbauer SM, Belflower RM, Winston LG, Bamberg WM, Lyons C et al (2013) Epidemiology of community-associated Clostridium difficile infection, 2009 through 2011. JAMA Intern Med 173:1359–1367
Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B et al (2010) The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev 23:529–549
Wilcox MH, Mooney L, Bendall R, Settle CD, Fawley WN (2008) A case–control study of community-associated Clostridium difficile infection. J Antimicrob Chemother 62:388–396
Khanna S, Pardi DS, Aronson SL, Kammer PP, Orenstein R, St Sauver JL et al (2012) The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol 107:89–95
Kuntz JL, Polgreen PM (2015) The importance of considering different healthcare settings when estimating the burden of Clostridium difficile. Clin Infect Dis 60:831–836
Asensio A, Monge D (2012) Epidemiology of Clostridium difficile infection in Spain. Enferm Infecc Microbiol Clin 30:333–337
Soler P, Nogareda F, Cano R (2008) Rates of Clostridium difficile infection in patients discharged from Spanish hospitals, 1997–2005. Infect Control Hosp Epidemiol 29:887–889
Esteban-Vasallo MD, Naval Pellicer S, Domínguez-Berjón F, Cantero Caballero M, Asensio Á, Saravia G et al (2016) Clostridium difficile-related hospitalizations in Madrid (Spain) between 2003 and 2014, a rising trend. J Infect 72:401–403
Alcalá L, Martín A, Marín M, Sánchez-Somolinos M, Catalán P, Peláez T et al (2012) The undiagnosed cases of Clostridium difficile infection in a whole nation: where is the problem? Clin Microbiol Infect 18:E204–E213
Alonso-Fernández P, Wu Lai TI, García-Salmones M, Saavedra-Cervera B, García-Salguero C, Merino P (2015) Clostridium difficile, are all our patients diagnosed? Rev Calid Asist 30:79–85
Burckhardt F, Friedrich A, Beier D, Eckmanns T (2008) Clostridium difficile surveillance trends, Saxony, Germany. Emerg Infect Dis 14:691–692
Di Bella S, Musso M, Cataldo MA, Meledandri M, Bordi E, Capozzi D et al (2013) Clostridium difficile infection in Italian urban hospitals: data from 2006 through 2011. BMC Infect Dis 13:146
Lucado J, Gould C, Elixhauser A (2012) Clostridium Difficile infections (CDI) in hospital stays, 2009: Healthcare Cost and Utilization Project (HCUP). Statistical Brief #124. Agency for Health Care Policy and Research, Rockville, MD
Lyytikäinen O, Turunen H, Sund R, Rasinperä M, Könönen E, Ruutu P et al (2009) Hospitalizations and deaths associated with Clostridium difficile infection, Finland, 1996–2004. Emerg Infect Dis 15:761–765
Reveles KR, Lee GC, Boyd NK, Frei CR (2014) The rise in Clostridium difficile infection incidence among hospitalized adults in the United States: 2001–2010. Am J Infect Control 42:1028–1032
Wilcox MH, Shetty N, Fawley WN, Shemko M, Coen P, Birtles A et al (2012) Changing epidemiology of Clostridium difficile infection following the introduction of a national ribotyping-based surveillance scheme in England. Clin Infect Dis 55:1056–1063
Vonberg RP, Schwab F, Gastmeier P (2007) Clostridium difficile in discharged inpatients, Germany. Emerg Infect Dis 13:179–180
McDonald LC, Owings M, Jernigan DB (2006) Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996–2003. Emerg Infect Dis 12:409–415
Zilberberg MD, Shorr AF, Kollef MH (2008) Increase in Clostridium difficile-related hospitalizations among infants in the United States, 2000–2005. Pediatr Infect Dis J 27:1111–1113
Kim J, Smathers SA, Prasad P, Leckerman KH, Coffin S, Zaoutis T (2008) Epidemiological features of Clostridium difficile-associated disease among inpatients at children’s hospitals in the United States, 2001–2006. Pediatrics 122:1266–1270
Rodríguez P, Cofré J (2015) Clostridium difficile associated diarrhea in children. Rev Chilena Infectol 32:550–558
Alcalá L, Reigadas E, Marín M, Martín A, Catalán P, Bouza E; Spanish Clostridium difficile Study Group (2015) Impact of clinical awareness and diagnostic tests on the underdiagnosis of Clostridium difficile infection. Eur J Clin Microbiol Infect Dis 34:1515–1525
Lessa FC, Gould CV, McDonald LC (2012) Current status of Clostridium difficile infection epidemiology. Clin Infect Dis 55(Suppl 2):S65–S70
Depestel DD, Aronoff DM (2013) Epidemiology of Clostridium difficile infection. J Pharm Pract 26:464–475
Monge D, Morosini M, Millán I, Pérez Canosa C, Manso M, Guzman MF et al (2011) Risk factors for Clostridium difficile infections in hospitalized patients. Med Clin (Barc) 137:575–580
EPINE: Evolución 1990–2014, con resumen de 2014. Sociedad Española de Medicina Preventiva SPeH (editor); 2015
Bauer MP, Notermans DW, van Benthem BH, Brazier JS, Wilcox MH, Rupnik M et al (2011) Clostridium difficile infection in Europe: a hospital-based survey. Lancet 377:63–73
Loo VG, Poirier L, Miller MA, Oughton M, Libman MD, Michaud S et al (2005) A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N Engl J Med 353:2442–2449
McDonald LC, Killgore GE, Thompson A, Owens RC Jr, Kazakova SV, Sambol SP et al (2005) An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 353:2433–2441
Marín M, Martín A, Alcolea A, Iglesias C, Alcalá L, Peláez T et al (2014) First case of autochthonous Clostridium difficile PCR ribotype 027 detected in Spain. Enferm Infecc Microbiol Clin 32:355–358
Servicio de Microbiología Clínica y Enfermedades Infecciosas. Situación en España de Ribotipo 027 y propuesta Estudio Nacional IV. Hospital General Universitario Gregorio Marañón (editor); 2015
Asensio A, Di Bella S, Lo Vecchio A, Grau S, Hart WM, Isidoro B et al (2015) The impact of Clostridium difficile infection on resource use and costs in hospitals in Spain and Italy: a matched cohort study. Int J Infect Dis 36:31–38
Wiegand PN, Nathwani D, Wilcox MH, Stephens J, Shelbaya A, Haider S (2012) Clinical and economic burden of Clostridium difficile infection in Europe: a systematic review of healthcare-facility-acquired infection. J Hosp Infect 81:1–14
Abou Chakra CN, Pepin J, Sirard S, Valiquette L (2014) Risk factors for recurrence, complications and mortality in Clostridium difficile infection: a systematic review. PLoS One 9, e98400
Collins CE, Ayturk MD, Anderson FA Jr, Santry HP (2015) Predictors and outcomes of readmission for Clostridium difficile in a national sample of medicare beneficiaries. J Gastrointest Surg 19:88–99
Marra F, Ng K (2015) Controversies around epidemiology, diagnosis and treatment of Clostridium difficile infection. Drugs 75:1095–1118
Dubberke ER, Reske KA, McDonald LC, Fraser VJ (2006) ICD-9 codes and surveillance for Clostridium difficile-associated disease. Emerg Infect Dis 12:1576–1579
European Centre for Disease Prevention and Control. European surveillance of Clostridium difficile infections. Surveillance protocol version 2.1. Stockholm: ECDC; 2015
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Esteban-Vasallo, M.D., Naval Pellicer, S., Domínguez-Berjón, M.F. et al. Age and gender differences in Clostridium difficile-related hospitalization trends in Madrid (Spain) over a 12-year period. Eur J Clin Microbiol Infect Dis 35, 1037–1044 (2016). https://doi.org/10.1007/s10096-016-2635-7
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DOI: https://doi.org/10.1007/s10096-016-2635-7