Article

Brief Communication

Ann Lab Med 2019; 39(3): 317-321

Published online May 1, 2019 https://doi.org/10.3343/alm.2019.39.3.317

Copyright © Korean Society for Laboratory Medicine.

Laboratory Diagnosis of Clostridium difficile Infection in Korea: The First National Survey

Hae-Sun Chung, M.D., Ph.D.1, Jeong Su Park, M.D., Ph.D.2, and Bo-Moon Shin , M.D., Ph.D.3

1Department of Laboratory Medicine, Ewha Womans University College of Medicine, Seoul, Korea; 2Department of Laboratory Medicine, Seoul National University Bundang Hospital, Seongnam, Korea; 3Department of Laboratory Medicine, Sanggye Paik Hospital, School of Medicine, Inje University, Seoul, Korea

Correspondence to: Bo-Moon Shin, M.D. https://orcid.org/0000-0001-8432-9556
Department of Laboratory Medicine, Sanggye Paik Hospital, School of Medicine, Inje University, 1342 Dongil-ro, Nowon-gu, Seoul 01757, Korea
Tel: +82-2-950-1227
Fax: +82-2-950-1244
E-mail: ortensia5577@gmail.com

Received: August 2, 2018; Revised: October 11, 2018; Accepted: December 11, 2018

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

In May 2015, we conducted a voluntary online survey on laboratory diagnostic assays for Clostridium difficile infection (CDI) across clinical microbiology laboratories in Korea. Responses were obtained from 66 laboratories, including 61 hospitals and five commercial laboratories. Among them, nine laboratories reported having not conducted CDI assays. The toxin AB enzyme immunoassay (toxin AB EIA), nucleic acid amplification test (NAAT), and C. difficile culture, alone or in combination with other assays, were used in 51 (89.5%), 37 (64.9%), and 37 (64.9%) of the remaining 57 laboratories, respectively, and 23 (40.4%) of the laboratories performed all three assays. Only one laboratory used the glutamate dehydrogenase assay. Nine laboratories used the toxin AB EIA as a stand-alone assay. The median (range) of examined specimens in one month for the toxin AB EIA, NAAT, and C. difficile culture was 160 (50–2,060), 70 (7–720), and 130 (9–750), respectively. These findings serve as valuable basic data regarding the current status of laboratory diagnosis of CDI in Korea, offering guidance for improved implementation.

Keywords: Clostridium difficile infection, Laboratory diagnosis, Toxin AB enzyme immunoassay, Nucleic acid amplification test, Culture, Survey, Korea

Clostridium difficile assay methods and the numbers of laboratories that participated in the survey

Assay typeNameManufacturerTargetMethodLaboratories (N)
Toxin AB EIAVIDAS CD ABbioMérieux, Marcy-l'Étoile, FranceToxin A and BAutomated EIA36
RIDASCREEN Clostridium difficile Toxin A/BBioPharm, Darmstadt, GermanyToxin A and BWell-type EIA9
Clostridium difficile Tox A/B IITechLab, Blacksburg, VA, USAToxin A and BWell-type EIA6
Total51
NAATXpert C. difficileCepheid, Sunnyvale, CA, USAtcdB, cdt, tcdCReal-time PCR21
AdvanSure CDLG Life Sciences, Seoul, KoreatcdA, tcdBReal-time PCRTotal11
BD Max CdiffBecton Dickinson, Sparks, MD, USAtcdBReal-time PCR2
Illumigene C. difficileMeridian Bioscience, Cincinnati, OH, USAtcdALAMP1
Seeplex Diarrhea ACE DetectionSeegene, Seoul, KoreatcdBMultiplex PCR1
Home-made2
36*
CultureChromeID C. difficilebioMérieux, Marcy-l'Étoile, FranceC. difficile24
CDSABecton Dickinson, Sparks, MD, USAC. difficile9
Blood agarC. difficile1
Home-madeC. difficile5
Total37
GDHVIDAS GDHbioMérieux, Marcy-l'Étoile, FranceGDHAutomated EIA1
Total1

Combinations of assays types for diagnosis of Clostridium difficile infection according to hospital size

Assay typeHospital beds (N)Total (%)
Toxin AB EIANAATCultureGDH< 300300–500> 500–1,000> 1,000CL*
+++1146223 (40.4)
++1719 (15.8)
++5229 (15.8)
+16119 (15.8)
++1214 (7.0)
++11 (1.8)
+11 (1.8)
+11 (1.8)
Total313711557 (100)

Numbers of specimens examined for CDI diagnosis according to assay types and hospital size per month in 2015

Size of hospital (N of beds)Toxin AB EIANAATCulture
Hospitals (N)Specimens, median (range)Hospitals (N)Specimens, median (range)Hospitals (N)Specimens, median (range)
< 3002140 (80–200)225 (10–40)242 (10–74)
300–500190170
< 500–1,00033155 (50–489)2370 (10–373)22100 (9–200)
> 1,00010200 (80–750)780 (35–300)9300 (80–750)
Subtotal46160 (50–750)3370 (7–370)33120 (9–750)
CL5568 (65–2,060)2365 (10–720)4140 (95–340)
Total51160 (50–2,060)35*70 (7–720)37130 (9–750)

  1. Burnham CA, Carroll KC. Diagnosis of Clostridium difficile infection: an ongoing conundrum for clinicians and for clinical laboratories. Clin Microbiol Rev 2013;26:604-630.
    Pubmed
  2. Bagdasarian N, Rao K, Malani PN. Diagnosis and treatment of Clostridium difficile in adults: a systematic review. JAMA 2015;313:398-408.
    Pubmed
  3. Leffler DA, Lamont JT. Clostridium difficile infection. N Engl J Med 2015;372:1539-1548.
    Pubmed
  4. Lytvyn L, Mertz D, Sadeghirad B, Alaklobi F, Selva A, Alonso-Coello P, et al. Prevention of Clostridium difficile infection: a systematic survey of clinical practice guidelines. Infect Control Hosp Epidemiol 2016;37:901-908.
    Pubmed
  5. Kim YS, Han DS, Kim YH, Kim WH, Kim JS, Kim HS, et al. Incidence and clinical features of Clostridium difficile infection in Korea: a nationwide study. Epidemiol Infect 2013;141:189-194.
    Pubmed
  6. McDonald LC, Gerding DN, Johnson S, Bakken JS, Carroll KC, Coffin SE, et al. Clinical practice guidelines for Clostridium difficile infection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA). Clin Infect Dis 2018;66:e1-e48.
    Pubmed
  7. Crobach MJ, Planche T, Eckert C, Barbut F, Terveer EM, Dekkers OM, et al. European Society of Clinical Microbiology and Infectious Diseases: update of the diagnostic guidance document for Clostridium difficile infection. Clin Microbiol Infect 2016;22:S63-S81.
    Pubmed
  8. Surawicz CM, Brandt LJ, Binion DG, Ananthakrishnan AN, Curry SR, Gilligan PH, et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 2013;108:478-498.
    Pubmed
  9. van Dorp SM, Notermans DW, Alblas J, Gastmeier P, Mentula S, Nagy E, et al. Survey of diagnostic and typing capacity for Clostridium difficile infection in Europe, 2011 and 2014. Euro Surveill 2016;21.
  10. Wong KK, Choi B, Fraser TG, Donskey CJ, Deshpande A. Diagnostic testing methods for Clostridium difficile infection: a statewide survey of Ohio acute care hospitals. Am J Infect Control 2017;45:306-307.
    Pubmed
  11. Spigaglia P, Barbanti F, Morandi M, Moro ML, Mastrantonio P. Diagnostic testing for Clostridium difficile in Italian microbiological laboratories. Anaerobe 2016;37:29-33.
    Pubmed
  12. Alcalá L, Reigadas E, Marín M, Martín A, Catalán P, Bouza E, et al. Impact of clinical awareness and diagnostic tests on the underdiagnosis of Clostridium difficile infection. Eur J Clin Microbiol Infect Dis 2015;34:1515-1525.
    Pubmed
  13. Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, 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;31:431-455.
    Pubmed
  14. Adler A, Schwartzberg Y, Samra Z, Schwartz O, Carmeli Y, Schwaber MJ, et al. Trends and changes in Clostridium difficile diagnostic policies and their impact on the proportion of positive samples: a national survey. Clin Microbiol Infect 2014;20:O904-O910.
    Pubmed
  15. Shin BM, Lee EJ. Comparison of chromID agar and Clostridium difficile selective agar for effective isolation of C. difficile from stool specimens. Ann Lab Med 2014;34:15-19.
    Pubmed
  16. Yim JS, Hwang SM, Kim M, Lim HJ, Shin S, Chung HS, et al. Evaluation of a chromID C. difficile agar for the isolation of Clostridium difficile. Korean J Clin Microbiol 2012;15:88-91.
  17. Han SB, Chang J, Shin SH, Park KG, Lee GD, Park YG, et al. Performance of chromID Clostridium difficile agar compared with BBL C. difficile selective agar for detection of C. difficile in stool specimens. Ann Lab Med 2014;34:376-379.
    Pubmed
  18. Fitzpatrick F, Oza A, Gilleece A, O’Byrne AM, Drudy D. C. difficile subcommittee of the Health Protection Surveillance Centre. Laboratory diagnosis of Clostridium difficile-associated disease in the Republic of Ireland: a survey of Irish microbiology laboratories. J Hosp Infect 2008;68:315-321.
    Pubmed
  19. Könönen E, Rasinperä M, Virolainen A, Mentula S, Lyytikäinen O. Diagnostic trends in Clostridium difficile detection in Finnish microbiology laboratories. Anaerobe 2009;15:261-265.
    Pubmed
  20. Shin BM, Lee EJ, Moon JW, Lee SY. Evaluation of the VIDAS glutamate dehydrogenase assay for the detection of Clostridium difficile. Anaerobe 2016;40:68-72.
    Pubmed