New opportunities for improved ribotyping of C. difficile clinical isolates by exploring their genomes

Journal of Microbiological Methods

Volumn 93, Issue 3, 2013, Pages 257-272

  Gürtler, Volker ^a   Grando, Danilla ^a  

^a RMIT UNIVERSITY   (Australia)

Author keywords

Clostridium difficile; Indel; ITS; Point of care; Ribotyping

Indexed keywords

INTERNAL TRANSCRIBED SPACER 1; RIBOSOME RNA; RNA 16S; RNA 23S;

BACTERIAL CHROMOSOME; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CLOSTRIDIUM DIFFICILE; COPY NUMBER VARIATION; DNA SEQUENCE; GENE SEQUENCE; GENOME ANALYSIS; HIGH RESOLUTION MELTING ANALYSIS; HUMAN; INTERMETHOD COMPARISON; MOLECULAR CLONING; MOLECULAR TYPING; NONHUMAN; NUCLEIC ACID DATABASE; NUCLEOTIDE SEQUENCE; OPERON; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVIEW; RIBOTYPING; RNA GENE; SEPARATION TECHNIQUE; SEQUENCE ANALYSIS; SOUTHERN BLOTTING;

CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; COMPUTATIONAL BIOLOGY; CROSS INFECTION; DIARRHEA; DNA PRIMERS; DNA, BACTERIAL; DNA, RIBOSOMAL SPACER; GENES, RRNA; GENOME, BACTERIAL; HUMANS; MOLECULAR EPIDEMIOLOGY; RIBOTYPING;

EID: 84877120397     PISSN: 01677012     EISSN: 18728359     Source Type: Journal    
DOI: 10.1016/j.mimet.2013.02.013     Document Type: Review

References (96)

1. Akerlund T., Persson I., Unemo M., Noren T., Svenungsson B., Wullt M., Burman L.G. Increased sporulation rate of epidemic Clostridium difficile type 027/NAP1. J. Clin. Microbiol. 2008, 46:1530-1533.
2. Aronsson B., Mollby R., Nord C.E. Diagnosis and epidemiology of Clostridium difficile enterocolitis in Sweden. J. Antimicrob. Chemother. 1984, 14(Suppl. D):85-95.
3. Arroyo L.G., Kruth S.A., Willey B.M., Staempfli H.R., Low D.E., Weese J.S. PCR ribotyping of Clostridium difficile isolates originating from human and animal sources. J. Med. Microbiol. 2005, 54:163-166.
4. Asai T., Zaporojets D., Squires C., Squires C.L. An Escherichia coli strain with all chromosomal rRNA operons inactivated: complete exchange of rRNA genes between bacteria. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:1971-1976.
5. Barbut F., Mastrantonio P., Delmee M., Brazier J., Kuijper E., Poxton I. Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. Clin. Microbiol. Infect. 2007, 13:1048-1057.
6. Bartlett J.G., Chang T.W., Gurwith M., Gorbach S.L., Onderdonk A.B. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N. Engl. J. Med. 1978, 298:531-534.
7. Baverud V. Clostridium difficile infections in animals with special reference to the horse. A review. Vet. Q. 2002, 24:203-219.
8. Bidet P., Barbut F., Lalande V., Burghoffer B., Petit J.C. Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol. Lett. 1999, 175:261-266.
9. Bidet P., Lalande V., Salauze B., Burghoffer B., Avesani V., Delmee M., Rossier A., Barbut F., Petit J.C. Comparison of PCR-ribotyping, arbitrarily primed PCR, and pulsed-field gel electrophoresis for typing Clostridium difficile. J. Clin. Microbiol. 2000, 38:2484-2487.
10. Bowman R.A., O'Neill G.L., Riley T.V. Non-radioactive restriction fragment length polymorphism (RFLP) typing of Clostridium difficile. FEMS Microbiol. Lett. 1991, 79:269-272.
11. Brazier J.S. Typing of Clostridium difficile. Clin. Microbiol. Infect. 2001, 7:428-431.
12. Brouwer M.S., Warburton P.J., Roberts A.P., Mullany P., Allan E. Genetic organisation, mobility and predicted functions of genes on integrated, mobile genetic elements in sequenced strains of Clostridium difficile. PLoS One 2011, 6:e23014.
13. Brouwer M.S., Allan E., Mullany P., Roberts A.P. Draft genome sequence of the nontoxigenic Clostridium difficile strain CD37. J. Bacteriol. 2012, 194:2125-2126.
14. Cangelosi G.A., Weigel K.M., Lefthand-Begay C., Meschke J.S. Molecular detection of viable bacterial pathogens in water by ratiometric pre-rRNA analysis. Appl. Environ. Microbiol. 2010, 76:960-962.
15. Cartmill T.D., Panigrahi H., Worsley M.A., McCann D.C., Nice C.N., Keith E. Management and control of a large outbreak of diarrhoea due to Clostridium difficile. J. Hosp. Infect. 1994, 27:1-15.
16. Cartwright C.P., Stock F., Beekmann S.E., Williams E.C., Gill V.J. PCR amplification of rRNA intergenic spacer regions as a method for epidemiologic typing of Clostridium difficile. J. Clin. Microbiol. 1995, 33:184-187.
17. Centers for Disease Control, Prevention (CDC) Severe Clostridium difficile-associated disease in populations previously at low risk-four states, 2005. Morbidity and Mortality Weekly Report 2005, 54:1201-1205.
18. Chachaty E., Depitre C., Mario N., Bourneix C., Saulnier P., Corthier G., Andremont A. Presence of Clostridium difficile and antibiotic and beta-lactamase activities in feces of volunteers treated with oral cefixime, oral cefpodoxime proxetil, or placebo. Antimicrob. Agents Chemother. 1992, 36:2009-2013.
19. Cheng V.C., Yam W.C., Lam O.T., Tsang J.L., Tse E.Y., Siu G.K., Chan J.F., Tse H., To K.K., Tai J.W., Ho P.L., Yuen K.Y. Clostridium difficile isolates with increased sporulation: emergence of PCR ribotype 002 in Hong Kong. Eur. J. Clin. Microbiol. Infect. Dis. 2011, 30:1371-1381.
20. Collier M.C., Stock F., DeGirolami P.C., Samore M.H., Cartwright C.P. Comparison of PCR-based approaches to molecular epidemiologic analysis of Clostridium difficile. J. Clin. Microbiol. 1996, 34:1153-1157.
21. Dawson L.F., Valiente E., Wren B.W. Clostridium difficile-a continually evolving and problematic pathogen. Infect. Genet. Evol. 2009, 9:1410-1417.
22. Debast S.B., van Leengoed L.A., Goorhuis A., Harmanus C., Kuijper E.J., Bergwerff A.A. Clostridium difficile PCR ribotype 078 toxinotype V found in diarrhoeal pigs identical to isolates from affected humans. Environ. Microbiol. 2009, 11:505-511.
23. Delmee M., Laroche Y., Avesani V., Cornelis G. Comparison of serogrouping and polyacrylamide gel electrophoresis for typing Clostridium difficile. J. Clin. Microbiol. 1986, 24:991-994.
24. Dial S., Delaney J.A., Barkun A.N., Suissa S. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA: J. Am. Med. Assoc. 2005, 294:2989-2995.
25. Dial S., Kezouh A., Dascal A., Barkun A., Suissa S. Patterns of antibiotic use and risk of hospital admission because of Clostridium difficile infection. CMAJ 2008, 179:767-772.
26. Drummond A.J., Ashton B., Buxton S., Cheung M., Cooper A., Duran C., Field M., Heled J., Kearse M., Markowitz S., Moir R., Stones-Havas S., Sturrock S., Thierer T., Wilson A. Geneious v5.0.4 Available from. http://www.geneious.com/%3E.
27. Evguenieva-Hackenberg E. Bacterial ribosomal RNA in pieces. Mol. Microbiol. 2005, 57:318-325.
28. Fawley W.N., Freeman J., Smith C., Harmanus C., Van Den Berg R.J., Kuijper E.J., Wilcox M.H. Use of highly discriminatory fingerprinting to analyze clusters of Clostridium difficile infection cases due to epidemic ribotype 027 strains. J. Clin. Microbiol. 2008, 46:954-960.
29. Forgetta V., Oughton M.T., Marquis P., Brukner I., Blanchette R., Haub K., Magrini V., Mardis E.R., Gerding D.N., Loo V.G., Miller M.A., Mulvey M.R., Rupnik M., Dascal A., Dewar K. Fourteen-genome comparison identifies DNA markers for severe-disease-associated strains of Clostridium difficile. J. Clin. Microbiol. 2011, 49:2230-2238.
30. Freeman J., Bauer M.P., Baines S.D., Corver J., Fawley W.N., Goorhuis B., Kuijper E.J., Wilcox M.H. The changing epidemiology of Clostridium difficile infections. Clin. Microbiol. Rev. 2010, 23:529-549.
31. Golledge C.L., McKenzie T., Riley T.V. Extended spectrum cephalosporins and Clostridium difficile. J. Antimicrob. Chemother. 1989, 23:929-931.
32. Goorhuis A., Bakker D., Corver J., Debast S.B., Harmanus C., Notermans D.W., Bergwerff A.A., Dekker F.W., Kuijper E.J. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin. Infect. Dis. 2008, 47:1162-1170.
33. Gould L.H., Limbago B. Clostridium difficile in food and domestic animals: a new foodborne pathogen?. Clin. Infect. Dis. 2010, 51:577-582.
34. Grando D., Said M.M., Mayall B.C., Gurtler V. High resolution melt analysis to track infections due to ribotype 027 Clostridium difficile. J. Microbiol. Methods 2012, 89:87-94.
35. Gurtler V. Typing of Clostridium difficile strains by PCR-amplification of variable length 16S-23S rDNA spacer regions. J. Gen. Microbiol. 1993, 139:3089-3097.
36. Gurtler, V., 1996. Typing of strains of Clostridium difficile and Staphylococcus aureus by analysis of variable length 16S-23S rDNA spacer regions, Thesis (Ph.D.) submitted to the School of Microbiology, Faculty of Science and Technology La Trobe University, Melbourne, Australia.
37. Gurtler V. The role of recombination and mutation in 16S-23S rDNA spacer rearrangements. Gene 1999, 238:241-252.
38. Gurtler V., Stanisich V.A. New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 1996, 142(Pt 1):3-16.
39. Gurtler V., Wilson V.A., Mayall B.C. Classification of medically important clostridia using restriction endonuclease site differences of PCR-amplified 16S rDNA. J. Gen. Microbiol. 1991, 137:2673-2679.
40. Gurtler V., Grando D., Mayall B.C., Wang J., Ghaly-Derias S. A novel method for simultaneous Enterococcus species identification/typing and van genotyping by high resolution melt analysis. J. Microbiol. Methods 2012, 90:167-181.
41. Gurtler V., Mayall B.C., Wang J. HRM confirmation of Neisseria gonorrhoeae in clinical specimens by G→A (position 857) mutation detection in the 16S rRNA gene before sequencing and after porA confirmation. J. Microbiol. Methods 2012, 89:148-152.
42. Gutell R.R., Gray M.W., Schnare M.N. A compilation of large subunit (23S and 23S-like) ribosomal RNA structures: 1993. Nucleic Acids Res. 1993, 21:3055-3074.
43. He M., Sebaihia M., Lawley T.D., Stabler R.A., Dawson L.F., Martin M.J., Holt K.E., Seth-Smith H.M., Quail M.A., Rance R., Brooks K., Churcher C., Harris D., Bentley S.D., Burrows C., Clark L., Corton C., Murray V., Rose G., Thurston S., van Tonder A., Walker D., Wren B.W., Dougan G., Parkhill J. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:7527-7532.
44. Hensgens M.P., Keessen E.C., Squire M.M., Riley T.V., Koene M.G., de Boer E., Lipman L.J., Kuijper E.J. Clostridium difficile infection in the community: a zoonotic disease?. Clin. Microbiol. Infect. 2012, 18:635-645.
45. Hill C.W., Harnish B.W. Inversions between ribosomal RNA genes of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 1981, 78:7069-7072.
46. Hunt D.E., Klepac-Ceraj V., Acinas S.G., Gautier C., Bertilsson S., Polz M.F. Evaluation of 23S rRNA PCR primers for use in phylogenetic studies of bacterial diversity. Appl. Environ. Microbiol. 2006, 72:2221-2225.
47. Indra A., Huhulescu S., Schneeweis M., Hasenberger P., Kembichler S., Fiedler A., Wewalka G., Allerberger F., Kuijper E.J. Characterization of Clostridium difficile isolates using capillary gel electrophoresis-based PCR ribotyping. J. Med. Microbiol. 2008, 57:1377-1382.
48. Indra A., Blaschitz M., Kernbichler S., Reischl U., Wewalka G., Allerberger F. Mechanisms behind variation in the Clostridium difficile 16S-23S rRNA intergenic spacer region. J. Med. Microbiol. 2010, 59:1317-1323.
49. Janezic S., Indra A., Allerberger F., Rupnik M. Use of different molecular typing methods for the study of heterogeneity within Clostridium difficile toxinotypes V and III. J. Med. Microbiol. 2011, 60:1101-1107.
50. Janezic S., Ocepek M., Zidaric V., Rupnik M. Clostridium difficile genotypes other than ribotype 078 that are prevalent among human, animal and environmental isolates. BMC Microbiol. 2012, 12:48.
51. Keel K., Brazier J.S., Post K.W., Weese S., Songer J.G. Prevalence of PCR ribotypes among Clostridium difficile isolates from pigs, calves, and other species. J. Clin. Microbiol. 2007, 45:1963-1964.
52. Khanna S., Pardi D.S., Aronson S.L., Kammer P.P., Orenstein R., St Sauver J.L., Harmsen W.S., Zinsmeister A.R. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am. J. Gastroenterol. 2012, 107:89-95.
53. Killgore G., Thompson A., Johnson S., Brazier J., Kuijper E., Pepin J., Frost E.H., Savelkoul P., Nicholson B., Van Den Berg R.J., Kato H., Sambol S.P., Zukowski W., Woods C., Limbago B., Gerding D.N., McDonald L.C. Comparison of seven techniques for typing international epidemic strains of Clostridium difficile: restriction endonuclease analysis, pulsed-field gel electrophoresis, PCR-ribotyping, multilocus sequence typing, multilocus variable-number tandem-repeat analysis, amplified fragment length polymorphism, and surface layer protein a gene sequence typing. J. Clin. Microbiol. 2008, 46:431-437.
54. Kitahara K., Sato N.S., Namba N., Yokota T., Tsujimura T., Suzuki T. Systematic deletion of rRNAs for investigating ribosome architecture and function. Nucleic Acids Symp. Ser. (Oxf.) 2006, 287-288.
55. Klappenbach J.A., Dunbar J.M., Schmidt T.M. rRNA operon copy number reflects ecological strategies of bacteria. Appl. Environ. Microbiol. 2000, 66:1328-1333.
56. Koene M.G., Mevius D., Wagenaar J.A., Harmanus C., Hensgens M.P., Meetsma A.M., Putirulan F.F., van Bergen M.A., Kuijper E.J. Clostridium difficile in Dutch animals: their presence, characteristics and similarities with human isolates. Clin. Microbiol. Infect. 2012, 18:778-784.
57. Kostman J.R., Edlind T.D., LiPuma J.J., Stull T.L. Molecular epidemiology of Pseudomonas cepacia determined by polymerase chain reaction ribotyping. J. Clin. Microbiol. 1992, 30:2084-2087.
58. Kristjansson M., Samore M.H., Gerding D.N., DeGirolami P.C., Bettin K.M., Karchmer A.W., Arbeit R.D. Comparison of restriction endonuclease analysis, ribotyping, and pulsed-field gel electrophoresis for molecular differentiation of Clostridium difficile strains. J. Clin. Microbiol. 1994, 32:1963-1969.
59. Larson H.E., Price A.B., Honour P., Borriello S.P. Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1978, 1:1063-1066.
60. Lessa F.C., Gould C.V., McDonald L.C. Current status of Clostridium difficile infection epidemiology. Clin. Infect. Dis. 2012, 55(Suppl. 2):S65-S70.
61. Loo V.G., Poirier L., Miller M.A., Oughton M., Libman M.D., Michaud S., Bourgault A.M., Nguyen T., Frenette C., Kelly M., Vibien A., Brassard P., Fenn S., Dewar K., Hudson T.J., Horn R., Rene P., Monczak Y., Dascal A. A predominantly clonal multi-institutional outbreak of Clostridium difficile-associated diarrhea with high morbidity and mortality. N. Engl. J. Med. 2005, 353:2442-2449.
62. Martirosian G., Kuipers S., Verbrugh H., van Belkum A., Meisel-Mikolajczyk F. PCR ribotyping and arbitrarily primed PCR for typing strains of Clostridium difficile from a Polish maternity hospital. J. Clin. Microbiol. 1995, 33:2016-2021.
63. McFarland L.V., Mulligan M.E., Kwok R.Y., Stamm W.E. Nosocomial acquisition of Clostridium difficile infection. N. Engl. J. Med. 1989, 320:204-210.
64. Merrigan M., Venugopal A., Mallozzi M., Roxas B., Viswanathan V.K., Johnson S., Gerding D.N., Vedantam G. Human hypervirulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production. J. Bacteriol. 2010, 192:4904-4911.
65. Neefs J.M., Van de Peer Y., Hendriks L., De Wachter R. Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res. 1990, 18:2237-2317. (Suppl.).
66. Ojaimi C., Davidson B.E., Saint Girons I., Old I.G. Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii. Microbiology 1994, 140(Pt 11):2931-2940.
67. Oka K., Osaki T., Hanawa T., Kurata S., Okazaki M., Manzoku T., Takahashi M., Tanaka M., Taguchi H., Watanabe T., Inamatsu T., Kamiya S. Molecular and microbiological characterization of Clostridium difficile isolates from single, relapse, and reinfection cases. J. Clin. Microbiol. 2012, 50:915-921.
68. O'Neill G., Adams J.E., Bowman R.A., Riley T.V. A molecular characterization of Clostridium difficile isolates from humans, animals and their environments. Epidemiol. Infect. 1993, 111:257-264.
69. O'Neill G.L., Ogunsola F.T., Brazier J.S., Duerden B.I. Modification of a PCR ribotyping method for application as a routine typing scheme for Clostridium difficile. Anaerobe 1996, 2:205-209.
70. Pepin J., Valiquette L., Alary M.E., Villemure P., Pelletier A., Forget K., Pepin K., Chouinard D. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 2004, 171:466-472.
71. Prompamorn P., Sithigorngul P., Rukpratanporn S., Longyant S., Sridulyakul P., Chaivisuthangkura P. The development of loop-mediated isothermal amplification combined with lateral flow dipstick for detection of Vibrio parahaemolyticus. Lett. Appl. Microbiol. 2011, 52:344-351.
72. Riley T.V., Golledge C.L. Clindamycin and pseudomembranous colitis. Lancet 1995, 346:639.
73. Rodriguez-Palacios A., Stämpfli H.R., Duffield T., Peregrine A.S., Trotz-Williams L.A., Arroyo L.G., Brazier J.S., Weese J.S. Clostridium difficile PCR ribotypes in calves, Canada. Emerg. Infect. Dis. 2006, 12:1730-1736.
74. Rupnik M. Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease?. Clin. Microbiol. Infect. 2007, 13:457-459.
75. Sadeghifard N., Gurtler V., Beer M., Seviour R.J. The mosaic nature of intergenic 16S-23S rRNA spacer regions suggests rRNA operon copy number variation in Clostridium difficile strains. Appl. Environ. Microbiol. 2006, 72:7311-7323.
76. Scaria J., Ponnala L., Janvilisri T., Yan W., Mueller L.A., Chang Y.F. Analysis of ultra low genome conservation in Clostridium difficile. PLoS One 2010, 5:e15147.
77. Schwartz J.J., Gazumyan A., Schwartz I. rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi. J. Bacteriol. 1992, 174:3757-3765.
78. Sebaihia M., Wren B.W., Mullany P., Fairweather N.F., Minton N., Stabler R., Thomson N.R., Roberts A.P., Cerdeno-Tarraga A.M., Wang H., Holden M.T., Wright A., Churcher C., Quail M.A., Baker S., Bason N., Brooks K., Chillingworth T., Cronin A., Davis P., Dowd L., Fraser A., Feltwell T., Hance Z., Holroyd S., Jagels K., Moule S., Mungall K., Price C., Rabbinowitsch E., Sharp S., Simmonds M., Stevens K., Unwin L., Whithead S., Dupuy B., Dougan G., Barrell B., Parkhill J. The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat. Genet. 2006, 38:779-786.
79. Songer J.G., Anderson M.A. Clostridium difficile: an important pathogen of food animals. Anaerobe 2006, 12:1-4.
80. Soto J. Clindamycin and pseudomembranous colitis. Lancet 1995, 346:249.
81. Southern E.M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 1975, 98:503-517.
82. Stabler R.A., He M., Dawson L., Martin M., Valiente E., Corton C., Lawley T.D., Sebaihia M., Quail M.A., Rose G., Gerding D.N., Gibert M., Popoff M.R., Parkhill J., Dougan G., Wren B.W. Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol. 2009, 10:R102.
83. Stubbs S.L., Brazier J.S., O'Neill G.L., Duerden B.I. 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. 1999, 37:461-463.
84. Surasilp T., Longyant S., Rukpratanporn S., Sridulyakul P., Sithigorngul P., Chaivisuthangkura P. Rapid and sensitive detection of Vibrio vulnificus by loop-mediated isothermal amplification combined with lateral flow dipstick targeted to rpoS gene. Mol. Cell. Probes 2011, 25:158-163.
85. Tanner H.E., Hardy K.J., Hawkey P.M. Coexistence of multiple multilocus variable-number tandem-repeat analysis subtypes of Clostridium difficile PCR ribotype 027 strains within fecal specimens. J. Clin. Microbiol. 2010, 48:985-987.
86. Tenover F.C., Akerlund T., Gerding D.N., Goering R.V., Bostrom T., Jonsson A.M., Wong E., Wortman A.T., Persing D.H. Comparison of strain typing results for Clostridium difficile isolates from North America. J. Clin. Microbiol. 2011, 49:1831-1837.
87. Warny M., Pepin J., Fang A., Killgore G., Thompson A., Brazier J., Frost E., McDonald L.C. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 2005, 366:1079-1084.
88. Weese J.S. Clostridium difficile in food-innocent bystander or serious threat?. Clin. Microbiol. Infect. 2010, 16:3-10.
89. Weese J.S., Finley R., Reid-Smith R.R., Janecko N., Rousseau J. Evaluation of Clostridium difficile in dogs and the household environment. Epidemiol. Infect. 2010, 138:1100-1104.
90. Weigel K.M., Jones K.L., Do J.S., Melton Witt J., Chung J.H., Valcke C., Cangelosi G.A. Molecular viability testing of bacterial pathogens from a complex human sample matrix. PLoS One 2013, 8:e54886.
91. Westblade L.F., Chamberland R.R., Maccannell D., Collins R., Dubberke E.R., Dunne W.M., Burnham C.A. Development and evaluation of a novel, semiautomated Clostridium difficile typing platform. J. Clin. Microbiol. 2013, 51:621-624.
92. Wilcox M.H., Mooney L., Bendall R., Settle C.D., Fawley W.N. A case-control study of community-associated Clostridium difficile infection. J. Antimicrob. Chemother. 2008, 62:388-396.
93. Wilcox M.H., Shetty N., Fawley W.N., Shemko M., Coen P., Birtles A., Cairns M., Curran M.D., Dodgson K.J., Green S.M., Hardy K.J., Hawkey P.M., Magee J.G., Sails A.D., Wren M.W. Changing epidemiology of Clostridium difficile infection following the introduction of a national ribotyping-based surveillance scheme in England. Clin. Infect. Dis. 2012, 55:1056-1063.
94. Wilson K.H., Blitchington R., Hindenach B., Greene R.C. Species-specific oligonucleotide probes for rRNA of Clostridium difficile and related species. J. Clin. Microbiol. 1988, 26:2484-2488.
95. Wren B.W., Tabaqchali S. Restriction endonuclease DNA analysis of Clostridium difficile. J. Clin. Microbiol. 1987, 25:2402-2404.
96. Xiao M., Kong F., Jin P., Wang Q., Xiao K., Jeoffreys N., James G., Gilbert G.L. Comparison of two capillary gel electrophoresis systems for Clostridium difficile ribotyping, using a panel of ribotype 027 isolates and whole-genome sequences as a reference standard. J. Clin. Microbiol. 2012, 50:2755-2760.