Molecular methods in the diagnosis of Clostridium difficile infections: an update

References

• Jones AM, Kuijper EJ, Wilcox MH. Clostridium difficile: a European perspective. J. Infect. 66(2), 115–128 (2013).
   PubMed Web of Science ®Google Scholar
• 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. 31(5), 431–455 (2010).
   PubMed Web of Science ®Google Scholar
• Wilcox MH, Planche T, Fang FC, Gilligan P. What is the current role of algorithmic approaches for diagnosis of Clostridium difficile infection? J. Clin. Microbiol. 48(12), 4347–4353 (2010).
   PubMed Web of Science ®Google Scholar
• Peterson LR, Mehta MS, Patel PA et al. Laboratory testing for Clostridium difficile infection: light at the end of the tunnel. Am. J. Clin. Pathol. 136(3), 372–380 (2011).
   PubMed Web of Science ®Google Scholar
• Sharp SE, Ruden LO, Pohl JC, Hatcher PA, Jayne LM, Ivie WM. Evaluation of the C.Diff Quik Chek Complete Assay, a new glutamate dehydrogenase and A/B toxin combination lateral flow assay for use in rapid, simple diagnosis of Clostridium difficile disease. J. Clin. Microbiol. 48(6), 2082–2086 (2010).
   PubMed Web of Science ®Google Scholar
• Surawicz CM, Brandt LJ, Binion DG et al. Guidelines for Diagnosis, Treatment, and Prevention of Clostridium difficile Infections. Am. J. Gastroenterol. 108(4), 478–498 (2013).
   PubMed Web of Science ®Google Scholar
• Stamper PD, Alcabasa R, Aird D et al. Comparison of a commercial real-time PCR assay for tcdB detection to a cell culture cytotoxicity assay and toxigenic culture for direct detection of toxin-producing Clostridium difficile in clinical samples. J. Clin. Microbiol. 47(2), 373–378 (2009).
   PubMed Web of Science ®Google Scholar
• Eastwood K, Else P, Charlett A, Wilcox M. Comparison of nine commercially available Clostridium difficile toxin detection assays, a real-time PCR assay for C. difficile tcdB, and a glutamate dehydrogenase detection assay to cytotoxin testing and cytotoxigenic culture methods. J. Clin. Microbiol. 47(10), 3211–3217 (2009).
   PubMed Web of Science ®Google Scholar
• Lalande V, Barrault L, Wadel S, Eckert C, Petit JC, Barbut F. Evaluation of a loop-mediated isothermal amplification assay for diagnosis of Clostridium difficile infections. J. Clin. Microbiol. 49(7), 2714–2716 (2011).
   PubMed Web of Science ®Google Scholar
• Planche T, Wilcox M. Reference assays for Clostridium difficile infection: one or two gold standards? J. Clin. Pathol. 64(1), 1–5 (2011).
   PubMed Web of Science ®Google Scholar
• Finegold SM. Clinical considerations in the diagnosis of antimicrobial agent-associated gastroenteritis. Diagn. Microbiol. Infect. Dis. 4(3 Suppl.), 87S–91S (1986).
   PubMed Web of Science ®Google Scholar
• Johal SS, Hammond J, Solomon K, James PD, Mahida YR. Clostridium difficile associated diarrhoea in hospitalised patients: onset in the community and hospital and role of flexible sigmoidoscopy. Gut 53(5), 673–677 (2004).
   PubMed Web of Science ®Google Scholar
• Dubberke ER, Han Z, Bobo L et al. Impact of clinical symptoms on interpretation of diagnostic assays for Clostridium difficile infections. J. Clin. Microbiol. 49(8), 2887–2893 (2011).
   PubMed Web of Science ®Google Scholar
• Hink T, Burnham CA, Dubberke ER. A systematic evaluation of methods to optimize culture-based recovery of Clostridium difficile from stool specimens. Anaerobe 19, 39–43 (2013).
   PubMed Web of Science ®Google Scholar
• She RC, Durrant RJ, Petti CA. Evaluation of enzyme immunoassays to detect Clostridium difficile toxin from anaerobic stool culture. Am. J. Clin. Pathol. 131(1), 81–84 (2009).
   PubMed Web of Science ®Google Scholar
• Kato N, Ou CY, Kato H et al. Detection of toxigenic Clostridium difficile in stool specimens by the polymerase chain reaction. J. Infect. Dis. 167(2), 455–458 (1993).
   PubMed Web of Science ®Google Scholar
• Boondeekhun HS, Gurtler V, Odd ML, Wilson VA, Mayall BC. Detection of Clostridium difficile enterotoxin gene in clinical specimens by the polymerase chain reaction. J. Med. Microbiol. 38(5), 384–387 (1993).
   PubMed Web of Science ®Google Scholar
• Persson S, De Boer RF, Kooistra-Smid AM, Olsen KE. Five commercial DNA extraction systems tested and compared on a stool sample collection. Diagn. Microbiol. Infect. Dis. 69(3), 240–244 (2011).
   PubMed Web of Science ®Google Scholar
• Lyras D, O'connor JR, Howarth PM et al. Toxin B is essential for virulence of Clostridium difficile. Nature 458(7242), 1176–1179 (2009).
   PubMed Web of Science ®Google Scholar
• Kuehne SA, Cartman ST, Heap JT, Kelly ML, Cockayne A, Minton NP. The role of toxin A and toxin B in Clostridium difficile infection. Nature 467(7316), 711–713 (2010).
   PubMed Web of Science ®Google Scholar
• Bauer MP, Notermans DW, Van Benthem BH et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet 377(9759), 63–73 (2011).
   PubMed Web of Science ®Google Scholar
• Shin BM, Kuak EY, Yoo HM et al. Multicentre study of the prevalence of toxigenic Clostridium difficile in Korea: results of a retrospective study 2000–2005. J. Med. Microbiol. 57( Pt 6), 697–701 (2008).
   PubMed Web of Science ®Google Scholar
• Kozak K, Elagin V, Noren T, Unemo M. Targeting the tcdA gene: is this appropriate for detection of A and/or B Clostridium difficile toxin-producing strains? J. Clin. Microbiol. 49(6), 2383, author reply 2383–2384 (2011).
   Google Scholar
• Squire MM, Carter GP, Mackin KE et al. Novel molecular type of Clostridium difficile in neonatal pigs, Western Australia. Emerg. Infect. Dis. 19(5), 790–792 (2013).
   PubMed Web of Science ®Google Scholar
• Peterson LR, Manson RU, Paule SM et al. Detection of toxigenic Clostridium difficile in stool samples by real-time polymerase chain reaction for the diagnosis of C. difficile-associated diarrhea. Clin. Infect. Dis. 45(9), 1152–1160 (2007).
   PubMed Web of Science ®Google Scholar
• Barbut F, Monot M, Rousseau A et al. Rapid diagnosis of Clostridium difficile infection by multiplex real-time PCR. Eur. J. Clin. Microbiol. Infect. Dis. 30(10), 1279–1285 (2011).
   PubMed Web of Science ®Google Scholar
• Saunders N, Zambon M, Sharp I et al. Guidance on the development and validation of diagnostic tests that depend on nucleic acid amplification and detection. J. Clin. Virol. 56(3), 260–270 (2013).
   PubMed Web of Science ®Google Scholar
• Munson E, Bilbo D, Paul M, Napierala M, Hryciuk JE. Modifications of commercial toxigenic Clostridium difficile PCR resulting in improved economy and workflow efficiency. J. Clin. Microbiol. 49(6), 2279–2282 (2011).
   PubMed Web of Science ®Google Scholar
• Selvaraju SB, Gripka M, Estes K, Nguyen A, Jackson MA, Selvarangan R. Detection of toxigenic Clostridium difficile in pediatric stool samples: an evaluation of Quik Check Complete Antigen assay, BD GeneOhm Cdiff PCR, and ProGastro Cd PCR assays. Diagn. Microbiol. Infect. Dis. 71(3), 224–229 (2011).
   PubMed Web of Science ®Google Scholar
• Viala C, Le Monnier A, Maataoui N, Rousseau C, Collignon A, Poilane I. Comparison of commercial molecular assays for toxigenic Clostridium difficile detection in stools: BD GeneOhm Cdiff, XPert C. difficile and illumigene C. difficile. J. Microbiol. Methods 90(2), 83–85 (2012).
   PubMed Web of Science ®Google Scholar
• Louie L, Wong H, Mubareka S, Simor AE. An Unusual Cause of False Positive Results with the BD GeneOhm Cdiff Assay. J. Clin. Microbiol. 51(4), 1348–1349 (2013).
   PubMed Web of Science ®Google Scholar
• Walkty A, Lagace-Wiens PR, Manickam K et al. Laboratory diagnosis of Clostridium difficile infection - Evaluation of an algorithmic approach in comparison with the illumigene assay. J. Clin. Microbiol. 51(4), 1152–1157 (2013).
   PubMed Web of Science ®Google Scholar
• Bruins MJ, Verbeek E, Wallinga JA, Bruijnesteijn Van Coppenraet LE, Kuijper EJ, Bloembergen P. Evaluation of three enzyme immunoassays and a loop-mediated isothermal amplification test for the laboratory diagnosis of Clostridium difficile infection. Eur. J. Clin. Microbiol. Infect. Dis. 31(11), 3035–3039 (2012).
   PubMed Web of Science ®Google Scholar
• Tenover FC, Novak-Weekley S, Woods CW et al. Impact of strain type on detection of toxigenic Clostridium difficile: comparison of molecular diagnostic and enzyme immunoassay approaches. J. Clin. Microbiol. 48(10), 3719–3724 (2010).
   PubMed Web of Science ®Google Scholar
• Zidaric V, Kevorkijan BK, Oresic N, Janezic S, Rupnik M. Comparison of two commercial molecular tests for the detection of Clostridium difficile in the routine diagnostic laboratory. J. Med. Microbiol. 60( Pt 8), 1131–1136 (2011).
   PubMed Web of Science ®Google Scholar
• Novak-Weekley SM, Marlowe EM, Miller JM et al. Clostridium difficile testing in the clinical laboratory by use of multiple testing algorithms. J. Clin. Microbiol. 48(3), 889–893 (2010).
   PubMed Web of Science ®Google Scholar
• Bacci S, Molbak K, Kjeldsen MK, Olsen KE. Binary toxin and death after Clostridium difficile infection. Emerg. Infect. Dis. 17(6), 976–982 (2011).
   PubMed Web of Science ®Google Scholar
• Kok J, Wang Q, Thomas LC, Gilbert GL. Presumptive identification of Clostridium difficile strain 027/NAP1/BI on Cepheid Xpert: interpret with caution. J. Clin. Microbiol. 49(10), 3719–3721 (2011).
   PubMed Web of Science ®Google Scholar
• Dalpke AH, Hofko M, Zorn M, Zimmermann S. Evaluation of the fully automated BD MAX Cdiff and Xpert C. difficile assays for the direct detection of Clostridium difficile in stool specimens. J. Clin. Microbiol. 51(6), 1906–1908 (2013).
   PubMed Web of Science ®Google Scholar
• Le Guern R, Herwegh S, Grandbastien B, Courcol R, Wallet F. Evaluation of a new molecular test, the BD Max Cdiff, for detection of toxigenic Clostridium difficile in fecal samples. J. Clin. Microbiol. 50(9), 3089–3090 (2012).
   PubMed Web of Science ®Google Scholar
• Hicke B, Pasko C, Groves B et al. Automated detection of toxigenic Clostridium difficile in clinical samples: isothermal tcdB amplification coupled to array-based detection. J. Clin. Microbiol. 50(8), 2681–2687 (2012).
   PubMed Web of Science ®Google Scholar
• Buchan BW, Mackey TL, Daly JA et al. Multicenter clinical evaluation of the Portrait toxigenic C. difficile assay for detection of toxigenic Clostridium difficile strains in clinical stool specimens. J. Clin. Microbiol. 50(12), 3932–3936 (2012).
   PubMed Web of Science ®Google Scholar
• Stamper PD, Babiker W, Alcabasa R et al. Evaluation of a new commercial TaqMan PCR assay for direct detection of the Clostridium difficile toxin B gene in clinical stool specimens. J. Clin. Microbiol. 47(12), 3846–3850 (2009).
   PubMed Web of Science ®Google Scholar
• Chun JY, Kim KJ, Hwang IT et al. Dual priming oligonucleotide system for the multiplex detection of respiratory viruses and SNP genotyping of CYP2C19 gene. Nucleic Acids Res. 35(6), e40 (2007).
   PubMed Web of Science ®Google Scholar
• Shin BM, Mun SJ, Yoo SJ, Kuak EY. Comparison of BD GeneOhm Cdiff and Seegene Seeplex ACE PCR assays using toxigenic Clostridium difficile culture for direct detection of tcdB from stool specimens. J. Clin. Microbiol. 50(11), 3765–3767 (2012).
   PubMed Web of Science ®Google Scholar
• Bauer TM, Lalvani A, Fehrenbach J et al. Derivation and validation of guidelines for stool cultures for enteropathogenic bacteria other than Clostridium difficile in hospitalized adults. JAMA 285(3), 313–319 (2001).
   PubMed Web of Science ®Google Scholar
• Delaloye J, Merlani G, Petignat C et al. Nosocomial nontyphoidal salmonellosis after antineoplastic chemotherapy: reactivation of asymptomatic colonization? Eur. J. Clin. Microbiol. Infect. Dis. 23(10), 751–758 (2004).
   PubMed Web of Science ®Google Scholar
• Gyorke CE, Wang S, Leslie JL, Cohen SH, Solnick JV, Polage CR. Evaluation of Clostridium difficile fecal load and limit of detection during a prospective comparison of two molecular tests, the illumigene C. difficile and Xpert C. difficile/Epi tests. J. Clin. Microbiol. 51(1), 278–280 (2013).
   PubMed Web of Science ®Google Scholar
• Gilligan PH. Is a two-step glutamate dehyrogenase antigen-cytotoxicity neutralization assay algorithm superior to the premier toxin A and B enzyme immunoassay for laboratory detection of Clostridium difficile? J. Clin. Microbiol. 46(4), 1523–1525 (2008).
   PubMed Web of Science ®Google Scholar
• Carman RJ, Wickham KN, Chen L et al. Glutamate dehydrogenase is highly conserved among Clostridium difficile ribotypes. J. Clin. Microbiol. 50(4), 1425–1426 (2012).
   PubMed Web of Science ®Google Scholar
• Swindells J, Brenwald N, Reading N, Oppenheim B. Evaluation of diagnostic tests for Clostridium difficile infection. J. Clin. Microbiol. 48(2), 606–608 (2010).
   PubMed Web of Science ®Google Scholar
• Culbreath K, Ager E, Nemeyer RJ, Kerr A, Gilligan PH. Evolution of Testing Algorithms at a University Hospital for Detection of Clostridium difficile Infections. J. Clin. Microbiol. 50(9), 3073–3076 (2012).
   PubMed Web of Science ®Google Scholar
• Akobeng AK. Understanding diagnostic tests 2: likelihood ratios, pre- and post-test probabilities and their use in clinical practice. Acta Paediatr. 96(4), 487–491 (2007).
   PubMed Web of Science ®Google Scholar
• Bouza E, Martin A, Van Den Berg RJ, Kuijper EJ. Laboratory-acquired Clostridium difficile polymerase chain reaction ribotype 027: a new risk for laboratory workers? Clin. Infect. Dis. 47(11), 1493–1494 (2008).
   PubMed Web of Science ®Google Scholar
• Aronsson B, Mollby R, Nord CE. Antimicrobial agents and Clostridium difficile in acute enteric disease: epidemiological data from Sweden, 1980–1982. J. Infect. Dis. 151(3), 476–481 (1985).
   PubMed Web of Science ®Google Scholar
• Riggs MM, Sethi AK, Zabarsky TF, Eckstein EC, Jump RL, Donskey CJ. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin. Infect. Dis. 45(8), 992–998 (2007).
   PubMed Web of Science ®Google Scholar
• Alcala L, Martin A, Marin M et al. The undiagnosed cases of Clostridium difficile infection in a whole nation: where is the problem? Clin. Microbiol. Infect. 18(7), E204–E213 (2012).
   PubMed Web of Science ®Google Scholar
• Carroll KC, Bartlett JG. Biology of Clostridium difficile: implications for epidemiology and diagnosis. Annu. Rev. Microbiol. 65, 501–521 (2011).
   PubMed Web of Science ®Google Scholar
• Freeman J, Bauer MP, Baines SD et al. The changing epidemiology of Clostridium difficile infections. Clin. Microbiol. Rev. 23(3), 529–549 (2010).
   PubMed Web of Science ®Google Scholar
• Khanna S, Pardi DS. “Community-acquired Clostridium difficile infection: an emerging entity”. Clin. Infect. Dis. 55(12), 1741–1742 (2012).
   PubMed Web of Science ®Google Scholar
• Dumyati G, Stevens V, Hannett GE et al. Community-associated Clostridium difficile infections, Monroe County, New York, USA. Emerg. Infect. Dis. 18(3), 392–400 (2012).
   PubMed Web of Science ®Google Scholar
• Leffler DA, Lamont JT. Editorial: not so nosocomial anymore: the growing threat of community-acquired Clostridium difficile. Am. J. Gastroenterol. 107(1), 96–98 (2012).
   PubMed Web of Science ®Google Scholar
• Shin BM, Moon SJ, Kim YS, Shin WC, Yoo HM. Characterization of cases of Clostridium difficile infection (CDI) presenting at an emergency room: molecular and clinical features differentiate community-onset hospital-associated and community-associated CDI in a tertiary care hospital. J. Clin. Microbiol. 49(6), 2161–2165 (2011).
   PubMed Web of Science ®Google Scholar
• Venugopal AA, Gerding DN, Johnson S. Clostridium difficile infection rates and spectrum of disease among peripartum women at one hospital from 2003 to 2007 with molecular typing analysis of recovered Clostridium difficile isolates. Am. J. Infect. Control 39(3), 206–211 (2011).
   PubMed Web of Science ®Google Scholar
• Kuntz JL, Yang M, Cavanaugh J, Saftlas AF, Polgreen PM. Trends in Clostridium difficile infection among peripartum women. Infect. Control Hosp. Epidemiol. 31(5), 532–534 (2010).
   PubMed Web of Science ®Google Scholar
• Barbut F, Mastrantonio P, Delmee M et al. Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. Clin. Microbiol. Infect. 13(11), 1048–1057 (2007).
   PubMed Web of Science ®Google Scholar
• Walker AS, Eyre DW, Wyllie DH et al. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin. Infect. Dis. 56(11), 1589–1600 (2013).
   PubMed Web of Science ®Google Scholar
• Walker AS, Eyre DW, Crook DW, Wilcox MH, Peto TE. Regarding “Clostridium difficile ribotype does not predict severe infection”. Clin. Infect. Dis. 56(12), 1845–6 (2013).
   PubMed Web of Science ®Google Scholar
• Luo RF, Banaei N. Is repeat PCR needed for diagnosis of Clostridium difficile infection? J. Clin. Microbiol. 48(10), 3738–3741 (2010).
   PubMed Web of Science ®Google Scholar
• Rousseau C, Lemee L, Le Monnier A, Poilane I, Pons JL, Collignon A. Prevalence and diversity of Clostridium difficile strains in infants. J. Med. Microbiol. 60( Pt 8), 1112–1118 (2011).
   PubMed Web of Science ®Google Scholar
• Sammons JS, Toltzis P, Zaoutis TE. Clostridium difficile Infection in Children. JAMA pediatr. 167(6), 567–573 (2013).
   PubMed Web of Science ®Google Scholar
• Schutze GE, Willoughby RE, Committee on Infectious D, American Academy Of P. Clostridium difficile infection in infants and children. Pediatrics 131(1), 196–200 (2013).
   PubMed Web of Science ®Google Scholar
• Clayton EM, Rea MC, Shanahan F et al. The vexed relationship between Clostridium difficile and inflammatory bowel disease: an assessment of carriage in an outpatient setting among patients in remission. Am. J. Gastroenterol. 104(5), 1162–1169 (2009).
   PubMed Web of Science ®Google Scholar
• Ananthakrishnan AN, Mcginley EL, Binion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut 57(2), 205–210 (2008).
   PubMed Web of Science ®Google Scholar
• Humphries RM, Uslan DZ, Rubin Z. Performance of Clostridium difficile Toxin Enzyme Immunoassay and Nucleic Acid Amplification Tests Stratified by Patient Disease Severity. J. Clin. Microbiol. 51(3), 869–873 (2013).
   PubMed Web of Science ®Google Scholar
• Longtin Y, Trottier S, Brochu G et al. Impact of the type of diagnostic assay on Clostridium difficile infection and complication rates in a mandatory reporting program. Clin. Infect. Dis. 56(1), 67–73 (2013).
   PubMed Web of Science ®Google Scholar
• Leslie JL, Cohen SH, Solnick JV, Polage CR. Role of fecal Clostridium difficile load in discrepancies between toxin tests and PCR: is quantitation the next step in C. difficile testing? Eur. J. Clin. Microbiol. Infect. Dis. 31(12), 3295–3299 (2012).
   PubMed Web of Science ®Google Scholar
• Chapin K. Discrepancies in testing recommendations for Clostridium difficile infection: updated review favors amplification test systems. Expert Rev. Mol. Diagn. 12(3), 223–226 (2012).
   PubMed Web of Science ®Google Scholar
• Loman NJ, Constantinidou C, Chan JZ et al. High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nat. Rev. Microbiol. 10(9), 599–606 (2012).
   PubMed Web of Science ®Google Scholar
• Didelot X, Eyre DW, Cule M et al. Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol. 13(12), R118 (2012).
   Web of Science ®Google Scholar
• Ylisiurua P, Koskela M, Vainio O, Tuokko H. Comparison of antigen and two molecular methods for the detection of Clostridium difficile toxins. Scand. J. Infect. Dis. 45(1), 19–25 (2013).
   PubMed Web of Science ®Google Scholar
• Goldenberg SD, Dieringer T, French GL. Detection of toxigenic Clostridium difficile in diarrheal stools by rapid real-time polymerase chain reaction. Diagn. Microbiol. Infect. Dis. 67(3), 304–307 (2010).
   PubMed Web of Science ®Google Scholar
• Shin S, Kim M, Kim M et al. Evaluation of the Xpert Clostridium difficile assay for the diagnosis of Clostridium difficile infection. Ann. Lab. Med. 32(5), 355–358 (2012).
   PubMed Web of Science ®Google Scholar