Skip to main content
SpringerLink
Log in

Impact of clinical awareness and diagnostic tests on the underdiagnosis of Clostridium difficile infection

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

A multicenter study of Clostridium difficile infection (CDI) performed during 2008 in Spain revealed that two of every three episodes went undiagnosed or were misdiagnosed owing to nonsensitive diagnostic tests or lack of clinical suspicion and request. Since then, efforts have been made to improve the diagnostic tests used by laboratories and to increase the awareness of this disease among both clinicians and microbiologists. Our objective was to evaluate the impact of these efforts by assessing the current magnitude of underdiagnosis of CDI in Spain using two point-prevalence studies performed on one day each in January and July of 2013. A total of 111 Spanish laboratories selected all unformed stool specimens received for microbiological diagnosis on these days, and toxigenic culture was performed at a central reference laboratory. Toxigenic isolates were characterized both pheno- and genotypically. The reference laboratory detected 103 episodes of CDI in patients aged 2 years or more. Half (50.5 %) of the episodes were not diagnosed in the participating laboratories, owing to insensitive diagnostic tests (15.5 %) or the lack of clinical suspicion and request (35.0 %). The main ribotypes were 014, 078/126, 001/072, and 106. Ribotype 027 caused 2.9 % of all cases. Despite all the interventions undertaken, CDI remains a highly neglected disease because of the lack of sensitive diagnostic tests in some institutions and, especially, the absence of clinical suspicion, mainly in patients with community-associated CDI. Toxigenic C. difficile should be routinely sought in unformed stools sent for microbiological diagnosis, regardless of their origin.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Riley TV, Cooper M, Bell B, Golledge CL (1995) Community-acquired Clostridium difficile-associated diarrhea. Clin Infect Dis 20(Suppl 2):S263–S265

    Article  PubMed  Google Scholar 

  2. McFarland LV, Mulligan ME, Kwok RY, Stamm WE (1989) Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320(4):204–210. doi:10.1056/NEJM198901263200402

    Article  CAS  PubMed  Google Scholar 

  3. Alcalá L, Sánchez-Cambronero L, Catalán MP, Sánchez-Somolinos M, Peláez MT, Marín M, Bouza E (2008) Comparison of three commercial methods for rapid detection of Clostridium difficile toxins A and B from fecal specimens. J Clin Microbiol 46(11):3833–3835. doi:10.1128/JCM.01060-08

    Article  PubMed Central  PubMed  Google Scholar 

  4. Bauer MP, Notermans DW, van Benthem BH, Brazier JS, Wilcox MH, Rupnik M, Monnet DL, van Dissel JT, Kuijper EJ; ECDIS Study Group (2011) Clostridium difficile infection in Europe: a hospital-based survey. Lancet 377(9759):63–73. doi:10.1016/S0140-6736(10)61266-4

    Article  PubMed  Google Scholar 

  5. Alcalá L, Martín A, Marín M, Sánchez-Somolinos M, Catalán P, Peláez T, Bouza E; Spanish Clostridium difficile Study Group (2012) The undiagnosed cases of Clostridium difficile infection in a whole nation: where is the problem? Clin Microbiol Infect 18(7):E204–E213. doi:10.1111/j.1469-0691.2012.03883.x

    Article  PubMed  Google Scholar 

  6. Alcalá L, Marín M, Madrid M, Domínguez-García E, Catalán P, Peláez MT, Sánchez-Somolinos M, Bouza E (2010) Comparison of ImmunoCard Toxins A&B and the new semiautomated Vidas Clostridium difficile Toxin A&B tests for diagnosis of C. difficile infection. J Clin Microbiol 48(3):1014–1015. doi:10.1128/JCM.01642-09

    Article  PubMed Central  PubMed  Google Scholar 

  7. Bouza E, Marín M, Peláez T, Alcalá L; Group for Clostridium difficile Infection of the Spanish Society for Chemotherapy (2013) The situation and management of Clostridium difficile infection in Spain: an opinion document. Rev Esp Quimioter 26(3):261–286

    PubMed  Google Scholar 

  8. Stubbs SL, Brazier JS, O’Neill GL, Duerden BI (1999) PCR targeted to the 16S-23S rRNA gene intergenic spacer region of Clostridium difficile and construction of a library consisting of 116 different PCR ribotypes. J Clin Microbiol 37(2):461–463

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Spigaglia P, Mastrantonio P (2002) Molecular analysis of the pathogenicity locus and polymorphism in the putative negative regulator of toxin production (TcdC) among Clostridium difficile clinical isolates. J Clin Microbiol 40(9):3470–3475

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  10. Persson S, Torpdahl M, Olsen KE (2008) New multiplex PCR method for the detection of Clostridium difficile toxin A (tcdA) and toxin B (tcdB) and the binary toxin (cdtA/cdtB) genes applied to a Danish strain collection. Clin Microbiol Infect 14(11):1057–1064. doi:10.1111/j.1469-0691.2008.02092.x

    Article  CAS  PubMed  Google Scholar 

  11. The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 4.0, 2014. http://www.eucast.org

  12. Clinical and Laboratory Standards Institute (CLSI) (2007) Methods for antimicrobial susceptibility testing of anaerobic bacteria; Approved standard—Seventh edition. CLSI document M11-A7. CLSI, Wayne, PA

  13. Davies KA, Longshaw CM, Davis GL, Bouza E, Barbut F, Barna Z, Delmée M, Fitzpatrick F, Ivanova K, Kuijper E, Macovei IS, Mentula S, Mastrantonio P, von Müller L, Oleastro M, Petinaki E, Pituch H, Norén T, Nováková E, Nyč O, Rupnik M, Schmid D, Wilcox MH (2014) Underdiagnosis of Clostridium difficile across Europe: the European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea (EUCLID). Lancet Infect Dis 14(12):1208–1219. doi:10.1016/S1473-3099(14)70991-0

    Article  PubMed  Google Scholar 

  14. Gilca R, Fortin E, Frenette C, Longtin Y, Gourdeau M (2012) Seasonal variations in Clostridium difficile infections are associated with influenza and respiratory syncytial virus activity independently of antibiotic prescriptions: a time series analysis in Quebec, Canada. Antimicrob Agents Chemother 56(2):639–646. doi:10.1128/AAC.05411-11

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Brown KA, Daneman N, Arora P, Moineddin R, Fisman DN (2013) The co-seasonality of pneumonia and influenza with Clostridium difficile infection in the United States, 1993–2008. Am J Epidemiol 178(1):118–125. doi:10.1093/aje/kws463

    Article  PubMed  Google Scholar 

  16. Bouza E, Peláez T, Alonso R, Catalán P, Muñoz P, Créixems MR (2001) “Second-look” cytotoxicity: an evaluation of culture plus cytotoxin assay of Clostridium difficile isolates in the laboratory diagnosis of CDAD. J Hosp Infect 48(3):233–237. doi:10.1053/jhin.2001.1000

    Article  CAS  PubMed  Google Scholar 

  17. Tenover FC, Baron EJ, Peterson LR, Persing DH (2011) Laboratory diagnosis of Clostridium difficile infection can molecular amplification methods move us out of uncertainty? J Mol Diagn 13(6):573–582. doi:10.1016/j.jmoldx.2011.06.001

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Vasoo S, Stevens J, Portillo L, Barza R, Schejbal D, Wu MM, Chancey C, Singh K (2014) Cost-effectiveness of a modified two-step algorithm using a combined glutamate dehydrogenase/toxin enzyme immunoassay and real-time PCR for the diagnosis of Clostridium difficile infection. J Microbiol Immunol Infect 47(1):75–78. doi:10.1016/j.jmii.2012.07.008

    Article  CAS  PubMed  Google Scholar 

  19. Wilcox MH, Planche T, Fang FC, Gilligan P (2010) What is the current role of algorithmic approaches for diagnosis of Clostridium difficile infection? J Clin Microbiol 48(12):4347–4353. doi:10.1128/JCM.02028-10

    Article  PubMed Central  PubMed  Google Scholar 

  20. Quinn CD, Sefers SE, Babiker W, He Y, Alcabasa R, Stratton CW, Carroll KC, Tang YW (2010) C. Diff Quik Chek complete enzyme immunoassay provides a reliable first-line method for detection of Clostridium difficile in stool specimens. J Clin Microbiol 48(2):603–605. doi:10.1128/JCM.01614-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Kuijper EJ, Coignard B, Tüll P; ESCMID Study Group for Clostridium difficile; EU Member States; European Centre for Disease Prevention and Control (2006) Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 12(Suppl 6):2–18. doi:10.1111/j.1469-0691.2006.01580.x

    Article  CAS  PubMed  Google Scholar 

  22. Khanna S, Pardi DS, Aronson SL, Kammer PP, Orenstein R, St Sauver JL, Harmsen WS, Zinsmeister AR (2012) The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol 107(1):89–95. doi:10.1038/ajg.2011.398

    Article  PubMed Central  PubMed  Google Scholar 

  23. Dumyati G, Stevens V, Hannett GE, Thompson AD, Long C, Maccannell D, Limbago B (2012) Community-associated Clostridium difficile infections, Monroe County, New York, USA. Emerg Infect Dis 18(3):392–400. doi:10.3201/eid1803.102023

    Article  PubMed Central  PubMed  Google Scholar 

  24. Naggie S, Frederick J, Pien BC, Miller BA, Provenzale DT, Goldberg KC, Woods CW (2010) Community-associated Clostridium difficile infection: experience of a veteran affairs medical center in southeastern USA. Infection 38(4):297–300. doi:10.1007/s15010-010-0025-0

    Article  CAS  PubMed  Google Scholar 

  25. Kuntz JL, Chrischilles EA, Pendergast JF, Herwaldt LA, Polgreen PM (2011) Incidence of and risk factors for community-associated Clostridium difficile infection: a nested case–control study. BMC Infect Dis 11:194. doi:10.1186/1471-2334-11-194

    Article  PubMed Central  PubMed  Google Scholar 

  26. Kutty PK, Woods CW, Sena AC, Benoit SR, Naggie S, Frederick J, Evans S, Engel J, McDonald LC (2010) Risk factors for and estimated incidence of community-associated Clostridium difficile infection, North Carolina, USA. Emerg Infect Dis 16(2):197–204. doi:10.3201/eid1602.090953

    Article  PubMed  Google Scholar 

  27. Karlström O, Fryklund B, Tullus K, Burman LG (1998) A prospective nationwide study of Clostridium difficile-associated diarrhea in Sweden. The Swedish C difficile Study Group. Clin Infect Dis 26(1):141–145

  28. van den Berg RJ, Ameen HA, Furusawa T, Claas EC, van der Vorm ER, Kuijper EJ (2005) Coexistence of multiple PCR-ribotype strains of Clostridium difficile in faecal samples limits epidemiological studies. J Med Microbiol 54(Pt 2):173–179

    Article  PubMed  Google Scholar 

  29. Tanner HE, Hardy KJ, Hawkey PM (2010) Coexistence of multiple multilocus variable-number tandem-repeat analysis subtypes of Clostridium difficile PCR ribotype 027 strains within fecal specimens. J Clin Microbiol 48(3):985–987. doi:10.1128/JCM.02012-09

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Marín M, Martín A, Alcolea A, Iglesias C, Alcalá L, Peláez T, Sánchez-Somolinos M, Bouza E (2014) First case of autochthonous Clostridium difficile PCR ribotype 027 detected in Spain. Enferm Infecc Microbiol Clin 32(6):355–358. doi:10.1016/j.eimc.2013.07.004

    Article  PubMed  Google Scholar 

  31. Bouza E, Martin A, Van den Berg RJ, Kuijper EJ (2008) Laboratory-acquired Clostridium difficile polymerase chain reaction ribotype 027: a new risk for laboratory workers? Clin Infect Dis 47(11):1493–1494. doi:10.1086/593109

    Article  PubMed  Google Scholar 

  32. Barbut F, Decré D, Burghoffer B, Lesage D, Delisle F, Lalande V, Delmée M, Avesani V, Sano N, Coudert C, Petit JC (1999) Antimicrobial susceptibilities and serogroups of clinical strains of Clostridium difficile isolated in France in 1991 and 1997. Antimicrob Agents Chemother 43(11):2607–2611

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Brazier JS, Fawley W, Freeman J, Wilcox MH (2001) Reduced susceptibility of Clostridium difficile to metronidazole. J Antimicrob Chemother 48(5):741–742

    Article  CAS  PubMed  Google Scholar 

  34. Peláez T, Cercenado E, Alcalá L, Marín M, Martín-López A, Martínez-Alarcón J, Catalán P, Sánchez-Somolinos M, Bouza E (2008) Metronidazole resistance in Clostridium difficile is heterogeneous. J Clin Microbiol 46(9):3028–3032. doi:10.1128/JCM.00524-08

    Article  PubMed Central  PubMed  Google Scholar 

  35. Wong SS, Woo PC, Luk WK, Yuen KY (1999) Susceptibility testing of Clostridium difficile against metronidazole and vancomycin by disk diffusion and Etest. Diagn Microbiol Infect Dis 34(1):1–6

    Article  CAS  PubMed  Google Scholar 

  36. Keighley MR, Burdon DW, Arabi Y, Williams JA, Thompson H, Youngs D, Johnson M, Bentley S, George RH, Mogg GA (1978) Randomised controlled trial of vancomycin for pseudomembranous colitis and postoperative diarrhoea. Br Med J 2(6153):1667–1669

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Thomas O’Boyle for his help in the preparation of the manuscript.

The members of the Spanish Clostridium difficile Study Group are as follows: F. E. Calvo Muro and M. J. Lezaun Burgui, Hospital Unificado de Álava-Sede Txagorritxu, Vitoria-Gasteiz, Álava; M. Martínez Serrano and M. D. Crespo Sánchez, Complejo Universitario Hospitalario, Albacete; M. Ruiz García, L. Álvarez Paredes, and G. Royo García, Hospital General Universitario, Elche, Alicante; M. Elía López, E. M. Pastor Boix, and P. Cascales Ramos, Hospital General Universitario, Elda, Alicante; M. Navarro Cots and N. Gonzalo Jiménez, Hospital del Servicio Valenciano de la Vega Baja, Orihuela, Alicante; W. Sánchez-Yebra Romera, M. Morales Torres, and A. Sicilia Enríquez de Salamanca, Complejo Hospitalario Torrecárdenas, Almería; B. Iglesias Rodríguez, G. Sierra, P. de la Iglesia, and H. Villar, Hospital San Agustín, Avilés, Asturias; L. Barreiro Hurlé, Hospital Carmen y Severo Ochoa, Cangas del Narcea, Asturias; M. D. Miguel Martínez and L. Otero Guerra, Hospital de Cabueñes, Gijón, Asturias; P. Suárez Leiva and M. J. Santos Rionda, Hospital Universitario Central de Asturias, Oviedo, Asturias; F. Vázquez Valdés, Hospital Monte Naranco, Oviedo, Asturias; M. I. Blanco Costa, Hospital Comarcal de Jarrio-Coaña, Jarrio, Asturias; R. Sánchez Arroyo and A. Gómez del Campo, Hospital Nuestra Señora de Sonsoles (Complejo Hospitalario), Ávila; M. Fajardo Olivares, Hospital Universitario Infanta Cristina, Badajoz; M. Álvarez and J. Vila Estapé, Hospital Clinic, Barcelona; I. Sanfeliú Sala and D. Fontanals Aymerich, Corporació Sanitària Parc Taulí, Sabadell, Barcelona; G. Trujillo Isern, J. López Madueño, and M. Morta, Fundación Althaia-Hospital San Joan de Deu, Manresa, Barcelona; A. Gené Giralt and C. Latorre Otín, Hospital Sant Joan de Déu, Esplugues de Llobregat, Barcelona; J. Niubó Bosh and M. A. Domínguez Luzón, Ciutat Sanitària I Universitaria de Bellvitge-Hospital Princeps d’Espanya, L’Hospitalet de Llobregat, Barcelona; V. Plasència Miguel, J. Gómez, and M. Salvadó Costa, Laboratorio de Referencia-Hospital del Mar, Prat de Llobregat, Barcelona; M. Micó García and P. Coll Figa, Hospital de la Santa Creu i Sant Pau, Barcelona; C. San José Alemany, Hospital Comarcal de Alt Penedès, Villafranca del Penedès, Barcelona; A. Vilamala Bastarras and J. Prat Quinzaños, Consorci Hospitalari de Vic, Vic, Barcelona; J. Sánchez Lafuente, J. L. Díaz de Tuesta del Arco, and R. Cisterna Cáncer, Hospital de Basurto, Bilbao, Bizkaia; L. Elorduy Otazúa, P. Iraurgui Arcarazo, and I. Marzana Sanz, Hospital San Eloy, Barakaldo, Bizkaia; I. Perales Palacios and M. Sota Busselo, Hospital Universitario de Cruces, Barakaldo, Bizkaia; A. P. Martínez de la Fuente and M. J. López de Goikoetxea, Hospital de Galdakao-Usansolo, Galdakao, Bizkaia; G. Megías Lobón and E. A. Ojeda Fernández, Hospital Universitario, Burgos; C. Gimeno Crespo, Hospital Comarcal Santiago Apostol, Miranda de Ebro, Burgos; M. R. Sánchez Benito, R. Íñiguez Ovando, and P. Teno Sánchez, Complejo Hospitalario de Cáceres-Hospital San Pedro de Alcántara, Cáceres; F. Galán Sánchez and M. A. Rodríguez Iglesias, Hospital Universitario Puerta del Mar, Cádiz; A. Sánchez Porto, Hospital del S.A.S. de La Línea de la Concepción, La Línea de la Concepción, Cádiz; M. D. López Prieto, Hospital del S.A.S. de Jerez de la Frontera, Jerez de la Frontera, Cádiz; M. P. Roiz Mesones and L. Martínez Martínez, Hospital Universitario Marqués de Valdecilla, Santander, Cantabria; S. Sabater Vidal and R. Moreno Muñoz, Hospital General de Castellón, Castellón; J. López Barba, Hospital Universitario, Ceuta; I. Barba Ferreras and M. D. Romero Aguilera, Hospital General Universitario, Ciudad Real; M. A. Asencio Egeda, E. Manrique González, and R. Carranza González, Hospital General La Mancha Centro, Alcázar de San Juan, Ciudad Real; M. Causse del Río and M. Casal Román, Hospital Universitario Reina Sofía, Córdoba; M. J. Rodríguez Escudero and M. C. Martínez Medina, Hospital General Virgen de la Luz, Cuenca; A. Peña Monje and F. García García, Hospital Clínico Universitario San Cecilio, Granada; J. Rodríguez Granger, C. Gómez Camarasa, and J. M. Navarro Mari, Hospital General Universitario Virgen de las Nieves, Granada; M. C. Gimeno Fernández and J. Bisquert Santiago, Hospital General Universitario, Guadalajara; M. Alkorta Gurrutxaga and E. Pérez-Trallero, Hospital Universitario de Donostia, San Sebastián, Gipúzkoa; J. M. Saavedra Martín and M. de la Iglesia Salgado, Hospital General Juan Ramón Jiménez, Huelva; A. Milagro Beamonte and M. Ferrero Cáncer, Hospital General San Jorge, Huesca; A. Mena Ribas and J. L. Pérez Sáenz, Hospital Son Espases, Palma de Mallorca, Islas Baleares; J. Sánchez Gómez and A. Hurtado Fernández, Hospital Can Misses, Ibiza, Islas Baleares; P. Ordóñez Barrosa and J. A. Agulla Budiño, Hospital Arquitecto Marcide-Novoa Santos, El Ferrol, La Coruña; A. Álvarez Alba and P. Castro Romero, Hospital General Juan Cardona, El Ferrol, La Coruña; M. D. Rodríguez Mayo and G. Bou Arévalo, Complejo Hospitalario Universitario A Coruña, La Coruña; L. Delgado Pérez and A. Bordes Benítez, Hospital Universitario de Gran Canaria Doctor Negrín, Las Palmas de Gran Canaria, Las Palmas; M. M. Ojeda Vargas and A. M. Martín Sánchez, Hospital Universitario Insular de Gran Canaria, Las Palmas de Gran Canaria, Las Palmas; R. López Medrano and C. Fuster Foz, Hospital del Bierzo, Ponferrada, León; M. A. Remacha Esteras, T. Marrodán Ciordia, I. Fernández Natal, and F. Cachón García, Hospital de León, León; J. Aramburu Arnuelos and B. Pérez Remón, Hospital Universitari Arnau de Vilanova, Lleida; J. Pita Carretero and M. P. Alonso García, Hospital Universitario Lucus Augusti (HULA), Lugo; C. Herrera Rodrigo, M. V. Portús Marco, J. L. Ruiz-Rivas and R. Cortés Bohórquez, Hospital Central de la Cruz Roja Española San José y Santa Adela, Madrid; A. García Blanco, J. Martiáñez Rodríguez, M. López-Brea, and L. Cardeñoso Domingo, Hospital Universitario de la Princesa, Madrid; L. Alcalá, E. Reigadas, M. Marín, A. Martín, P. Catalán, and E. Bouza, Hospital General Universitario Gregorio Marañón, Madrid; M. A. Orellana Miguel and J. J. Rodríguez Otero, Hospital Universitario 12 de Octubre, Madrid; P. Trevisi Lannoó, M. Baquero Mochales, and A. Enríquez Grego, Hospital Universitario Carlos III, Madrid; J. Romero Vivas and R. Cantón Moreno, Hospital Ramón y Cajal, Madrid; I. Sánchez Romero, R. Martínez Ruiz, and M. F. Portero Azorín, Hospital Puerta de Hierro, Madrid; P. Merino Amador, B. Saavedra, and J. J. Picazo, Hospital Clínico San Carlos-Complejo Hospitalario, Madrid; S. García Bujalance, A. Gutiérrez Altés, and J. García Rodríguez, Hospital de la Paz, Madrid; J. A. Cuadros González and J. Vicente Saz, Hospital Príncipe de Asturias, Alcalá de Henares, Madrid; C. García Esteban, D. Molina Arana, and J. I. Alós, Hospital Universitario de Getafe, Getafe, Madrid; M. C. Gómez Criado and I. Wilhelmi de Cal, Hospital Severo Ochoa, Leganés, Madrid; A. Delgado-Iribarren, Fundación Hospital Alcorcón, Alcorcón, Madrid; M. T. Pérez Pomata and J. L. Gómez Garcés, Hospital General, Móstoles, Madrid; M. J. González Abad and J. Otero de Becerra, Hospital del Niño Jesús, Madrid; M. A. Izquierdo Ruiz de la Peña and J. R. Maestre Vera, Hospital Central de la Defensa Gómez Ulla, Madrid, Madrid; M. C. Mediavilla Gradolph and B. Palop Borrás, Hospital Regional Universitario Carlos Haya, Málaga; G. Sena Corrales and E. Clavijo Frutos, Hospital Clínico Universitario Virgen de la Victoria, Málaga; F. Díaz Monllor, Hospital Comarcal, Melilla; C. Guerrero Gómez and R. Blázquez Garrido, Hospital José María Morales Meseguer, Murcia; A. Aguinaga and A. J. Leiva León, Clínica Universitaria de Navarra, Pamplona, Navarra; X. Beristain Rementería and C. Ezpeleta, Complejo Hospitalario de Navarra, Pamplona, Navarra; M. A. Gómez Rial and G. Estebán Meruéndano, Hospital Santa María Nai-Complejo Hospitalario de Ourense, Ourense; M. García Bravo and M. A. García Castro, Hospital General Río Carrión, Palencia; S. Cortizo Vidal and M. García Campello, Complejo Hospitalario, Pontevedra; L. Martínez Lamas and M. T. González del Blanco, Complejo Hospitalario Xeral-Cies, Vigo, Pontevedra; I. Rodríguez Conde, Policlínico Vigo S. A.-POVISA, Vigo, Pontevedra; M. de Frutos Serna and J. E. García Sánchez, Hospital Universitario de Salamanca-Hospital Clínico y Hospital Virgen de la Vega, Salamanca; A. Madueño Alonso and M. Lecuona, Hospital Universitario de Canarias, La Laguna, Santa Cruz de Tenerife; J. Alcoba Flores, M. R. Sánchez Flores, and E. Viejo Rivero, Hospital Universitario Nuestra Señora de Candelaria, Santa Cruz de Tenerife; S. Hernando Real and S. García Carbajosa, Complejo Hospitalario de Segovia (SACYL), Segovia; M. Delgado Valverde and A. Pascual Hernández, Hospital Universitario Virgen de la Macarena, Sevilla; M. C. Lozano Domínguez and J. Aznar Martín, Hospital Universitario Virgen del Rocío, Sevilla; A. I. Aller García and E. Martín Mazuelos, Hospital Universitario Nuestra Señora de Valme, Dos Hermanas, Sevilla; C. Aldea Masilla, T. Nebreda Mayoral, and A. Campos Bueno, Complejo Hospitalario de Soria (Santa Bárbara-Virgen del Mirón), Soria; J. Tapiol Oliva and A. Vilanova Navarro, Hospital de Tarragona Joan XXIII, Tarragona; M. P. Chocarro Escanero and J. Horno, Hospital General Obispo Polanco, Teruel; J. A. Rodríguez Polo, P. Zamarrón Fuertes, S. Brea Zubigaray, and E. Heredero Gálvez, Hospital Virgen de la Salud, Toledo; J. Colomina Rodríguez, Hospital de la Ribera, Alzira, Valencia; N. Orta Mira and J. Díaz Fernández, Hospital Francesc Borja, Gandía, Valencia; J. M. García Aguayo, Hospital General de Requena, Requena, Valencia; S. Giner Almaraz, Hospital Doctor Moliner, Serra, Valencia; T. García Lozano, J. Maiquez Richart, and E. Aznar Oroval, Fundación Instituto Valenciano de Oncología (IVO), Valencia; A. Valentín Martín and C. Segarra Martínez, Hospital Arnau de Vilanova, Valencia; I. Corrales Vázquez, J. Buesa Gómez, and J. García de Lomas, Hospital Clínico de Valencia, Valencia; A. Molina de Diego and José Luis López Hontangas, Hospital Universitario y Politécnico La Fe, Valencia; D. González Granda, M. Pariente Martín, and E. Ochoa Ávila, Hospital Lluis Alcanyis, Xátiva, Valencia; L. Navarro Pérez, M. Jiménez Mayordomo, A. Broseta Tamariz, and J. L. Barberá Comes, Hospital de Manises, Manises, Valencia; C. Gobernado, E. Álvarez Alonso, and R. Órtiz de Lejarazu, Hospital Clínico Universitario de Valladolid, Valladolid; M. Domínguez-Gil González-Eiros and J. Eiros Bouza, Hospital del Río Hortega, Valladolid; M. I. Antolín Ayala, B. Salinas Sánchez, and M. C. García Loygorri, Hospital de Medina del Campo, Medina del Campo, Valladolid; L. López-Urrutia Lorente, M. Albert Hernández, and M. F. Brezmes Valdivieso, Hospital Virgen de la Concha Área 11, Zamora; C. Miñana Amada, Hospital Real y Provincial Nuestra Señora de Gracia, Zaragoza; C. Seral and M. C. Rubio Calvo, Hospital Clínico Universitario Lozano Blesa, Zaragoza; and C. Marne and M. J. Revillo Pinilla, Hospital Universitario Miguel Servet, Zaragoza.

Conflict of interest

The authors declare no conflicts of interest.

Role of funding source

This study was partially financed by grants from Astellas Pharma Inc. for the “European, multicentre, prospective, biannual, point-prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea” (EUCLID), Red Española de Investigación en Patología Infecciosa C/03/14 (REIPI), and Fondo de Investigaciones Sanitarias (FIS 2013/PI-13/00687). Elena Reigadas holds a grant from the Río Hortega program of the Carlos III Health Institute, Spanish Government.

Author information

Authors and Affiliations

  1. Clinical Microbiology and Infectious Diseases Department, Hospital General Universitario Gregorio Marañón, Calle Dr. Esquerdo 46, 28007, Madrid, Spain

    L. Alcalá, E. Reigadas, M. Marín, A. Martín, P. Catalán & E. Bouza

  2. Medicine Department, School of Medicine, Universidad Complutense de Madrid (UCM), Madrid, Spain

    E. Reigadas, M. Marín & E. Bouza

  3. Instituto de Investigación Sanitaria Gregorio Marañón, Madrid, Spain

    L. Alcalá, E. Reigadas, M. Marín & E. Bouza

  4. CIBER de Enfermedades Respiratorias (CIBERES CB06/06/0058), Madrid, Spain

    L. Alcalá, M. Marín & E. Bouza

Authors
  1. L. Alcalá
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Reigadas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Marín
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Catalán
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. E. Bouza
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

on behalf of the Spanish Clostridium difficile Study Group

Corresponding authors

Correspondence to L. Alcalá or E. Bouza.

Additional information

This study was presented at the 24th European Congress of Clinical Microbiology and Infectious Diseases (ECCMID 2014), Barcelona, Spain, May 10–13, 2014.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alcalá, L., Reigadas, E., Marín, M. et al. Impact of clinical awareness and diagnostic tests on the underdiagnosis of Clostridium difficile infection. Eur J Clin Microbiol Infect Dis 34, 1515–1525 (2015). https://doi.org/10.1007/s10096-015-2380-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-015-2380-3

Keywords

Search

Navigation