Abstract
We aimed to determine the incidence of Clostridium difficile infection (CDI), the molecular epidemiology of circulating C. difficile strains and risk factors for CDI among hospitalised children in the Auckland region. A cross-sectional study was undertaken of hospitalised children <15 years of age in two hospitals investigated for healthcare-associated diarrhoea between November 2011 and June 2012. Stool specimens were analysed for the presence of C. difficile using a two-step testing algorithm including polymerase chain reaction (PCR). C. difficile was cultured and PCR ribotyping performed. Demographic data, illness characteristics and risk factors were compared between children with and without CDI. Non-duplicate stool specimens were collected from 320 children with a median age of 1.2 years (range 3 days to 15 years). Forty-six patients (14 %) tested met the definition for CDI. The overall incidence of CDI was 2.0 per 10,000 bed days. The percentage of positive tests among neonates was only 2.6 %. PCR ribotyping showed a range of strains, with ribotype 014 being the most common. Significant risk factors for CDI were treatment with proton pump inhibitors [risk ratio (RR) 1.74, 95 % confidence interval (CI) 1.09–5.59; p = 0.002], presence of underlying malignancy (RR 2.71, 95 % CI 1.65–4.62; p = 0.001), receiving chemotherapy (RR 2.70, 95 % CI 1.41–4.83; p = 0.003) and exposure to antibiotics (RR 1.17, 95 % CI 0.99–1.17; p = 0.03). C. difficile is an important cause of healthcare-associated diarrhoea in this paediatric population. The notion that neonatal populations will always have high rates of colonisation with C. difficile may not be correct. Several risk factors associated with CDI among adults were also found to be significant.
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References
Wilson KH (1993) The microecology of Clostridium difficile. Clin Infect Dis 16:S214–S218
Kyne L, Warny M, Qamar A, Kelly CP (2000) Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med 342:390–397
Mylonakis E, Ryan ET, Calderwood SB (2001) Clostridium difficile-associated diarrhea: a review. Arch Intern Med 161:525–533
Yassin SF, Young-Fadok TM, Zein NN, Pardi DS (2001) Clostridium difficile-associated diarrhea and colitis. Mayo Clin Proc 76:725–730
Pépin J, Valiquette L, Alary ME et al (2004) Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 171:466–472
McDonald LC, Killgore GE, Thompson A et al (2005) An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 353:2433–2441
Kuijper EJ, Coignard B, Brazier JS et al (2007) Update of Clostridium difficile-associated disease due to PCR ribotype 027 in Europe. Euro Surveill 12:E1–E2
Riley TV, Thean S, Hool G, Golledge CL (2009) First Australian isolation of epidemic Clostridium difficile PCR ribotype 027. Med J Aust 190:706–708
Roberts SA, Heffernan H, Al Anbuky N et al (2011) Epidemic strains of Clostridium difficile are present in Auckland, New Zealand. N Z Med J 124:97–101
Cohen MB (2009) Clostridium difficile infections: emerging epidemiology and new treatments. J Pediatr Gastroenterol Nutr 48:S63–S65
Cerquetti M, Luzzi I, Caprioli A, Sebastianelli A, Mastrantonio P (1995) Role of Clostridium difficile in childhood diarrhea. Pediatr Infect Dis J 14:598–603
Boenning DA, Fleisher GR, Campos JM, Hulkower CW, Quinlan RW (1982) Clostridium difficile in a pediatric outpatient population. Pediatr Infect Dis 1:336–338
Larson HE, Barclay FE, Honour P, Hill ID (1982) Epidemiology of Clostridium difficile in infants. J Infect Dis 146:727–733
Al-Jumaili IJ, Shibley M, Lishman AH, Record CO (1984) Incidence and origin of Clostridium difficile in neonates. J Clin Microbiol 19:77–78
Bolton RP, Tait SK, Dear PRF, Losowsky MS (1984) Asymptomatic neonatal colonisation by Clostridium difficile. Arch Dis Child 59:466–472
Tina LG, Proto N, Sciacca A (1994) Asymptomatic intestinal colonization by Clostridium difficile in preterm neonates. Pediatr Infect Dis J 13:1158–1159
Klein EJ, Boster DR, Stapp JR et al (2006) Diarrhea etiology in a children’s hospital emergency department: a prospective cohort study. Clin Infect Dis 43:807–813
Zilberberg MD, Tillotson GS, McDonald LC (2010) Clostridium difficile infections among hospitalized children, United States, 1997–2006. Emerg Infect Dis 16:604–609
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
Nylund CM, Goudie A, Garza JM, Fairbrother G, Cohen MB (2011) Clostridium difficile infection in hospitalized children in the United States. Arch Pediatr Adolesc Med 165:451–457
Cohen SH, Gerding DN, Johnson S et al (2010) 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 31:431–455
Schutze GE, Willoughby RE; Committee on Infectious Diseases; American Academy of Pediatrics (2013) Clostridium difficile infection in infants and children. Pediatrics 131:196–200
Neuwelt PM, Simmons G (2006) A public health portrait of severe paediatric gastroenteritis in the Auckland region: report of the Auckland Paediatric Gastroenteritis Investigation. Available online at: http://www.arphs.govt.nz/about/publications-and-reports. Accessed 4 Apr 2012
Indra A, Huhulescu S, Schneeweis M et al (2008) Characterization of Clostridium difficile isolates using capillary gel electrophoresis-based PCR ribotyping. J Med Microbiol 57:1377–1382
Tschudin-Sutter S, Tamma PD, Naegeli AN, Speck KA, Milstone AM, Perl TM (2013) Distinguishing community-associated from hospital-associated Clostridium difficile infections in children: implications for public health surveillance. Clin Infect Dis 57:1665–1672
Sandora TJ, Fung M, Flaherty K, Helsing L et al (2011) Epidemiology and risk factors for Clostridium difficile infection in children. Pediatr Infect Dis J 30:580–584
Mitchell DK, Van R, Mason EH, Norris DM, Pickering LK (1996) Prospective study of toxigenic Clostridium difficile in children given amoxicillin/clavulanate for otitis media. Pediatr Infect Dis J 15:514–519
Benson L, Song X, Campos J, Singh N (2007) Changing epidemiology of Clostridium difficile-associated disease in children. Infect Control Hosp Epidemiol 28:1233–1235
Tleyjeh IM, Bin Abdulhak AA, Riaz M et al (2012) Association between proton pump inhibitor therapy and Clostridium difficile infection: a contemporary systematic review and meta-analysis. PLoS One 7:e50836
Turco R, Martinelli M, Miele E et al (2010) Proton pump inhibitors as a risk factor for paediatric Clostridium difficile infection. Aliment Pharmacol Ther 31:754–759
El-Mahallawy HA, El-Din NH, Salah F, El-Arousy M, El-Naga SA (2004) Epidemiologic profile of symptomatic gastroenteritis in pediatric oncology patients receiving chemotherapy. Pediatr Blood Cancer 42:338–342
Tai E, Richardson LC, Townsend J, Howard E, McDonald LC (2011) Clostridium difficile infection among children with cancer. Pediatr Infect Dis J 30:610–612
Castagnola E, Battaglia T, Bandettini R et al (2009) Clostridium difficile-associated disease in children with solid tumors. Support Care Cancer 17:321–324
Wultańska D, Banaszkiewicz A, Radzikowski A et al (2009) Clostridium difficile infection in polish pediatric outpatients with inflammatory bowel disease. Eur J Clin Microbiol Infect Dis 29:1265–1270
Mezoff E, Mann EA, Hart KW, Lindsell CJ, Cohen MB (2011) Clostridium difficile infection and treatment in the pediatric inflammatory bowel disease population. J Pediatr Gastroenterol Nutr 52:437–441
Roberts SA, Heffernan H, Al Anbuky N et al (2011) Molecular epidemiology and susceptibility profiles of Clostridium difficile in New Zealand, 2009. N Z Med J 124:45–51
Barbut F, Mastrantonio P, Delmée M, Brazier J, Kuijper E, Poxton I (2007) Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. Clin Microbiol Infect 13:1048–1057
Stoesser N, Crook DW, Fung R et al (2011) Molecular epidemiology of Clostridium difficile strains in children compared with that of strains circulating in adults with Clostridium difficile-associated Infection. J Clin Microbiol 49:3994–3996
Planche TD, Davies KA, Coen PG et al (2013) Differences in outcome according to Clostridium difficile testing method: a prospective multicentre diagnostic validation study of C. difficile infection. Lancet Infect Dis 13:936–945
Acknowledgements
The authors would like to acknowledge the assistance of Helen Heffernan (ESR, Wellington) for the PCR ribotyping of isolates, and Dr. Lesley Voss and Dr. Emma Best (Paediatric Infectious Diseases Specialists, SCH) for reviewing the manuscript.
Conflict of interest
All authors have no conflicts of interest to declare. Funding for this project was received from A+ Trust, Auckland District Health Board.
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Sathyendran, V., McAuliffe, G.N., Swager, T. et al. Clostridium difficile as a cause of healthcare-associated diarrhoea among children in Auckland, New Zealand: clinical and molecular epidemiology. Eur J Clin Microbiol Infect Dis 33, 1741–1747 (2014). https://doi.org/10.1007/s10096-014-2139-2
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DOI: https://doi.org/10.1007/s10096-014-2139-2