Chemical and stress resistances of clostridium difficile spores and vegetative cells

Frontiers in Microbiology

Volumn 7, Issue OCT, 2016, Pages

  Edwards, Adrianne N ^a   Karim, Samiha T ^a   Pascual, Ricardo A ^a   Jowhar, Lina M ^a   Anderson, Sarah E ^a   McBride, Shonna M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anaerobe; Clostridium difficile; Clostridium difficile infection (CDI); Germination; Resistance; Spores; Sporulation

Indexed keywords

ALCOHOL; CHLOROFORM; HYDROGEN PEROXIDE;

ARTICLE; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; COLONY FORMING UNIT; CONTROLLED STUDY; HEAT; LIMIT OF DETECTION; NONHUMAN; OPTICAL DENSITY; OXIDATIVE STRESS; PEPTOCLOSTRIDIUM DIFFICILE; PHASE CONTRAST MICROSCOPY; PHYSICAL SENSITIVITY AND TOLERANCE;

EID: 84997545303     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01698     Document Type: Article

References (83)

1. Alfa, M. J., Lo, E., Wald, A., Dueck, C., DeGagne, P., and Harding, G. K. (2010). Improved eradication of Clostridium difficile spores from toilets of hospitalized patients using an accelerated hydrogen peroxide as the cleaning agent. BMC Infect. Dis 10:268. doi: 10.1186/1471-2334-10-268.
2. Ali, S., Moore, G., and Wilson, A. P. (2011). Spread and persistence of Clostridium difficile spores during and after cleaning with sporicidal disinfectants. J. Hosp. Infect. 79, 97-98. doi: 10.1016/j.jhin.2011.06.010.
3. Balassa, G. (1971). The genetic control of spore formation in bacilli. Curr. Top. Microbiol. Immunol 56, 99-192.
4. Baumann, E. R., and Ludwig, D. D. (1962). Free available chlorine residuals for small nonpublic water supplies. J. Am. Water Works Assoc. 54, 1379-1388.
5. Bhattacharjee, D., Francis, M. B., Ding, X., McAllister, K. N., Shrestha, R., and Sorg, J. A. (2016). Reexamining the germination phenotypes of several Clostridium difficile strains suggests another role for the CspC germinant receptor. J. Bacteriol. 198, 777-786. doi: 10.1128/JB.00908-915.
6. Bidet, P., Lalande, V., Salauze, B., Burghoffer, B., Avesani, V., Delmee, M., et al. (2000). Comparison of PCR-ribotyping, arbitrarily primed PCR, and pulsed-field gel electrophoresis for typing Clostridium difficile. J. Clin. Microbiol. 38, 2484-2487.
7. Bouillaut, L., McBride, S. M., and Sorg, J. A. (2011). Genetic manipulation of Clostridium difficile. Curr Protoc Microbiol. Chap. 9, Unit9A.2. doi: 10.1002/9780471729259.mc09a02s20.
8. Burns, D. A., Heap, J. T., and Minton, N. P. (2010). The diverse sporulation characteristics of Clostridium difficile clinical isolates are not associated with type. Anaerobe 16, 618-622. doi: 10.1016/j.anaerobe.2010.10.001.
9. Burns, D. A., Heeg, D., Cartman, S. T., and Minton, N. P. (2011). Reconsidering the sporulation characteristics of hypervirulent Clostridium difficile BI/NAP1/027. PLoS ONE 6:e24894. doi: 10.1371/journal.pone.0024894.
10. Carlson, P. E. Jr., Kaiser, A. M., McColm, S. A., Bauer, J. M., Young, V. B., Aronoff, D. M., et al. (2015). Variation in germination of Clostridium difficile clinical isolates correlates to disease severity. Anaerobe 33, 64-70. doi: 10.1016/j.anaerobe.2015.02.003.
11. CDC (2013). Antibiotic Resistance Threats in the United States, 2013. Available at: http://www.cdc.gov/features/AntibioticResistanceThreats/.
12. Dawson, L. F., Valiente, E., Faulds-Pain, A., Donahue, E. H., and Wren, B. W. (2012). Characterisation of Clostridium difficile biofilm formation, a role for Spo0A. PLoS ONE 7:e50527. doi: 10.1371/journal.pone.0050527.
13. de Hoon, M. J., Eichenberger, P., and Vitkup, D. (2010). Hierarchical evolution of the bacterial sporulation network. Curr. Biol. 20, R735-R745. doi: 10.1016/j.cub.2010.06.031.
14. Deakin, L. J., Clare, S., Fagan, R. P., Dawson, L. F., Pickard, D. J., West, M. R., et al. (2012). The Clostridium difficile spo0A gene is a persistence and transmission factor. Infect. Immun. 80, 2704-2711. doi: 10.1128/IAI.00147-12.
15. Driks, A. (2002). Overview: development in bacteria: spore formation in Bacillus subtilis. Cell. Mol. Life Sci. 59, 389-391. doi: 10.1007/s00018-002-8430-x.
16. Driks, A. (2003). The dynamic spore. Proc. Natl. Acad. Sci. U.S.A. 100, 3007-3009. doi: 10.1073/pnas.0730807100.
17. Dubberke, E. (2012). Strategies for prevention of Clostridium difficile infection. J. Hosp. Med. 7(Suppl. 3), S14-S17. doi: 10.1002/jhm.1908.
18. Dubberke, E. R., and Olsen, M. A. (2012). Burden of Clostridium difficile on the healthcare system. Clin. Infect. Dis. 55(Suppl. 2), S88-S92. doi: 10.1093/cid/cis335.
19. Eckstein, B. C., Adams, D. A., Eckstein, E. C., Rao, A., Sethi, A. K., Yadavalli, G. K., et al. (2007). Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods. BMC Infect. Dis. 7:61. doi: 10.1186/1471-2334-7-61.
20. Edmonds, S. L., Macinga, D. R., Mays-Suko, P., Duley, C., Rutter, J., Jarvis, W. R., et al. (2012). Comparative efficacy of commercially available alcohol-based hand rubs and World Health Organization-recommended hand rubs: formulation matters. Am. J. Infect. Control 40, 521-525. doi: 10.1016/j.ajic.2011.08.016.
21. Edwards, A. N., Nawrocki, K. L., and McBride, S. M. (2014). Conserved oligopeptide permeases modulate sporulation initiation in Clostridium difficile. Infect. Immun. 82, 4276-4291. doi: 10.1128/IAI.02323-14.
22. Edwards, A. N., Suarez, J. M., and McBride, S. M. (2013). Culturing and maintaining Clostridium difficile in an anaerobic environment. J. Vis. Exp. 79, e50787. doi: 10.3791/50787.
23. Edwards, A. N., Tamayo, R., and McBride, S. M. (2016). A novel regulator controls Clostridium difficile sporulation, motility and toxin production. Mol. Microbiol. 100, 954-971. doi: 10.1111/mmi.13361.
24. Ezeji, T., Milne, C., Price, N. D., and Blaschek, H. P. (2010). Achievements and perspectives to overcome the poor solvent resistance in acetone and butanol-producing microorganisms. Appl. Microbiol. Biotechnol. 85, 1697-1712. doi: 10.1007/s00253-009-2390-0.
25. Fawley, W. N., Underwood, S., Freeman, J., Baines, S. D., Saxton, K., Stephenson, K., et al. (2007). Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains. Infect. Control Hosp. Epidemiol. 28, 920-925. doi: 10.1086/519201.
26. Fimlaid, K. A., Bond, J. P., Schutz, K. C., Putnam, E. E., Leung, J. M., Lawley, T. D., et al. (2013). Global analysis of the sporulation pathway of Clostridium difficile. PLoS Genet. 9:e1003660. doi: 10.1371/journal.pgen.1003660.
27. Fimlaid, K. A., Jensen, O., Donnelly, M. L., Francis, M. B., Sorg, J. A., and Shen, A. (2015). Identification of a novel lipoprotein regulator of Clostridium difficile spore germination. PLoS Pathog. 11:e1005239. doi: 10.1371/journal.ppat.1005239.
28. Francis, M. B., Allen, C. A., Shrestha, R., and Sorg, J. A. (2013). Bile acid recognition by the Clostridium difficile germinant receptor, CspC, is important for establishing infection. PLoS Pathog. 9:e1003356. doi: 10.1371/journal.ppat.1003356.
29. Heeg, D., Burns, D. A., Cartman, S. T., and Minton, N. P. (2012). Spores of Clostridium difficile clinical isolates display a diverse germination response to bile salts. PLoS ONE 7:e32381. doi: 10.1371/journal.pone.0032381.
30. Henriques, A. O., and Moran, C. P. Jr. (2007). Structure, assembly, and function of the spore surface layers. Annu. Rev. Microbiol. 61, 555-588. doi: 10.1146/annurev.micro.61.080706.093224.
31. 2-affected gene expression of Clostridium acetobutylicum. J. Bacteriol. 191, 6082-6093. doi: 10.1128/JB.00351-09.
32. Hillmann, F., Fischer, R. J., Saint-Prix, F., Girbal, L., and Bahl, H. (2008). PerR acts as a switch for oxygen tolerance in the strict anaerobe Clostridium acetobutylicum. Mol. Microbiol. 68, 848-860. doi: 10.1111/j.1365-2958.2008.06192.x.
33. Ho, T. D., and Ellermeier, C. D. (2011). PrsW is required for colonization, resistance to antimicrobial peptides, and expression of extracytoplasmic function sigma factors in Clostridium difficile. Infect. Immun. 79, 3229-3238. doi: 10.1128/IAI.00019-11.
34. Holy, O., and Chmelar, D. (2012). Oxygen tolerance in anaerobic pathogenic bacteria. Folia Microbiol. (Praha) 57, 443-446. doi: 10.1007/s12223-012-0149-y.
35. Horn, K., and Otter, J. A. (2015). Hydrogen peroxide vapor room disinfection and hand hygiene improvements reduce Clostridium difficile infection, methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, and extended-spectrum beta-lactamase. Am. J. Infect. Control 43, 1354-1356. doi: 10.1016/j.ajic.2015.06.029.
36. Hussain, H. A., Roberts, A. P., and Mullany, P. (2005). Generation of an erythromycin-sensitive derivative of Clostridium difficile strain 630 (630Δerm) and demonstration that the conjugative transposon Tn916ΔE enters the genome of this strain at multiple sites. J. Med. Microbiol. 54, 137-141. doi: 10.1099/jmm.0.45790-0.
37. Janoir, C. (2016). Virulence factors of Clostridium difficile and their role during infection. Anaerobe 37, 13-24. doi: 10.1016/j.anaerobe.2015.10.009.
38. Koenigsknecht, M. J., Theriot, C. M., Bergin, I. L., Schumacher, C. A., Schloss, P. D., and Young, V. B. (2015). Dynamics and establishment of Clostridium difficile infection in the murine gastrointestinal tract. Infect. Immun. 83, 934-941. doi: 10.1128/IAI.02768-14.
39. Kwon, J. H., Olsen, M. A., and Dubberke, E. R. (2015). The morbidity, mortality, and costs associated with Clostridium difficile infection. Infect. Dis. Clin. North Am. 29, 123-134. doi: 10.1016/j.idc.2014.11.003.
40. Larson, H. E., Price, A. B., Honour, P., and Borriello, S. P. (1978). Clostridium difficile and the aetiology of pseudomembranous colitis. Lancet 1, 1063-1066. doi: 10.1016/S0140-6736(78)90912-1.
41. Lawley, T. D., Clare, S., Deakin, L. J., Goulding, D., Yen, J. L., Raisen, C., et al. (2010). Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens. Appl. Environ. Microbiol. 76, 6895-6900. doi: 10.1128/AEM.00718-10.
42. Lawley, T. D., Croucher, N. J., Yu, L., Clare, S., Sebaihia, M., Goulding, D., et al. (2009). Proteomic and genomic characterization of highly infectious Clostridium difficile 630 spores. J. Bacteriol. 191, 5377-5386. doi: 10.1128/JB.00597-09.
43. Leggett, M. J., McDonnell, G., Denyer, S. P., Setlow, P., and Maillard, J. Y. (2012). Bacterial spore structures and their protective role in biocide resistance. J. Appl. Microbiol. 113, 485-498. doi: 10.1111/j.1365-2672.2012.05336.x.
44. Lessa, F. C., Gould, C. V., and McDonald, L. C. (2012). Current status of Clostridium difficile infection epidemiology. Clin. Infect. Dis. 55(Suppl. 2), S65-S70. doi: 10.1093/cid/cis319.
45. Levy, A. R., Szabo, S. M., Lozano-Ortega, G., Lloyd-Smith, E., Leung, V., Lawrence, R., et al. (2015). Incidence and costs of Clostridium difficile infections in Canada. Open Forum Infect. Dis. 2, ofv076. doi: 10.1093/ofid/ofv076.
46. Mackin, K. E., Carter, G. P., Howarth, P., Rood, J. I., and Lyras, D. (2013). Spo0A differentially regulates toxin production in evolutionarily diverse strains of Clostridium difficile. PLoS ONE 8:e79666. doi: 10.1371/journal.pone.0079666.
47. Macleod-Glover, N., and Sadowski, C. (2010). Efficacy of cleaning products for C. difficile: environmental strategies to reduce the spread of Clostridium difficile-associated diarrhea in geriatric rehabilitation. Can. Fam. Physician 56, 417-423.
48. McBride, S., and Haldenwang, W. G. (2004). Sporulation phenotype of a Bacillus subtilis mutant expressing an unprocessable but active sigmaE transcription factor. J. Bacteriol. 186, 1999-2005. doi: 10.1128/JB.186.7.1999-2005.2004.
49. McDonald, L. C., Lessa, F., Sievert, D., Wise, M., Herrera, R., Gould, C., et al. (2012). Vital signs: preventing Clostridium difficile infections. Morb. Mortal. Wkly. Rep. 61, 157-162.
50. Milhaud, P., and Balassa, G. (1973). Biochemical genetics of bacterial sporulation. IV. Sequential development of resistances to chemical and physical agents during sporulation of Bacillus subtilis. Mol. Gen. Genet. 125, 241-250. doi: 10.1007/BF00270746.
51. Murrell, W. G., and Scott, W. J. (1966). The heat resistance of bacterial spores at various water activities. J. Gen. Microbiol. 43, 411-425. doi: 10.1099/00221287-43-3-411.
52. Nawrocki, K. L., Edwards, A. N., Daou, N., Bouillaut, L., and McBride, S. M. (2015). CodY-dependent regulation of sporulation in Clostridium difficile. J. Bacteriol. 198, 2113-2130. doi: 10.1128/JB.00220-16.
53. Nerandzic, M. M., Sunkesula, V. C. C. T. S., Setlow, P., and Donskey, C. J. (2015). Unlocking the sporicidal potential of ethanol: induced sporicidal activity of ethanol against Clostridium difficile and Bacillus Spores under altered physical and chemical conditions. PLoS ONE 10:e0132805. doi: 10.1371/journal.pone.0132805.
54. Omidbakhsh, N. (2010). Evaluation of sporicidal activities of selected environmental surface disinfectants: carrier tests with the spores of Clostridium difficile and its surrogates. Am. J. Infect. Control 38, 718-722. doi: 10.1016/j.ajic.2010.02.009.
55. Oughton, M. T., Loo, V. G., Dendukuri, N., Fenn, S., and Libman, M. D. (2009). Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile. Infect. Control Hosp. Epidemiol. 30, 939-944. doi: 10.1086/605322.
56. Paredes, C. J., Alsaker, K. V., and Papoutsakis, E. T. (2005). A comparative genomic view of clostridial sporulation and physiology. Nat. Rev. Microbiol. 3, 969-978. doi: 10.1038/nrmicro1288.
57. Paredes-Sabja, D., and Sarker, M. R. (2011). Germination response of spores of the pathogenic bacterium Clostridium perfringens and Clostridium difficile to cultured human epithelial cells. Anaerobe 17, 78-84. doi: 10.1016/j.anaerobe.2011.02.001.
58. Paredes-Sabja, D., Shen, A., and Sorg, J. A. (2014). Clostridium difficile spore biology: sporulation, germination, and spore structural proteins. Trends Microbiol. 22, 406-416. doi: 10.1016/j.tim.2014.04.003.
59. Perez, J., Springthorpe, V. S., and Sattar, S. A. (2005). Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control. Am. J. Infect. Control 33, 320-325. doi: 10.1016/j.ajic.2005.04.240.
60. Pizarro-Guajardo, M., Calderon-Romero, P., Castro-Cordova, P., Mora-Uribe, P., and Paredes-Sabja, D. (2016a). Ultrastructural variability of the exosporium layer of Clostridium difficile spores. Appl. Environ. Microbiol. 82, 2202-2209. doi: 10.1128/AEM.03410-15.
61. Pizarro-Guajardo, M., Calderon-Romero, P., and Paredes-Sabja, D. (2016b). Revising the ultrastructure variability of the exosporium layer of Clostridium difficile spores from sporulating cultures and biofilms. Appl. Environ. Microbiol. 82, 5892-5898. doi: 10.1128/AEM.01463-16.
62. Pizarro-Guajardo, M., Olguin-Araneda, V., Barra-Carrasco, J., Brito-Silva, C., Sarker, M. R., and Paredes-Sabja, D. (2014). Characterization of the collagen-like exosporium protein, BclA1, of Clostridium difficile spores. Anaerobe 25, 18-30. doi: 10.1016/j.anaerobe.2013.11.003.
63. 2 detoxification in Clostridium acetobutylicum. Microbiology 155(Pt 1), 16-24. doi: 10.1099/mic.0.022756-0.
64. Rodriguez-Palacios, A., and Lejeune, J. T. (2011). Moist-heat resistance, spore aging, and superdormancy in Clostridium difficile. Appl. Environ. Microbiol. 77, 3085-3091. doi: 10.1128/AEM.01589-1510.
65. Rupnik, M., Wilcox, M. H., and Gerding, D. N. (2009). Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7, 526-536. doi: 10.1038/nrmicro2164.
66. Russell, A. D. (1990). Bacterial spores and chemical sporicidal agents. Clin. Microbiol. Rev. 3, 99-119. doi: 10.1128/CMR.3.2.99.
67. Schiott, T., and Hederstedt, L. (2000). Efficient spore synthesis in Bacillus subtilis depends on the CcdA protein. J. Bacteriol. 182, 2845-2854. doi: 10.1128/JB.182.10.2845-2854.2000.
68. Setlow, P. (2006). Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101, 514-525. doi: 10.1111/j.1365-2672.2005.02736.x.
69. Setlow, P. (2014). Spore resistance properties. Microbiol. Spectr. 2. doi: 10.1128/microbiolspec. TBS-0003-2012.
70. Shen, A. (2012). Clostridium difficile toxins: mediators of inflammation. J. Innate Immun. 4, 149-158. doi: 10.1159/000332946.
71. Slauch, J. M. (2011). How does the oxidative burst of macrophages kill bacteria? Still an open question. Mol. Microbiol. 80, 580-583. doi: 10.1111/j.1365-2958.2011.07612.x.
72. Smits, W. K., Lyras, D., Lacy, D. B., Wilcox, M. H., and Kuijper, E. J. (2016). Clostridium difficile infection. Nat. Rev. Dis. Primers 2, 16020. doi: 10.1038/nrdp.2016.20.
73. Sorg, J. A., and Sonenshein, A. L. (2008). Bile salts and glycine as cogerminants for Clostridium difficile spores. J. Bacteriol. 190, 2505-2512. doi: 10.1128/JB.01765-07.
74. Stabler, R. A., He, M., Dawson, L., Martin, M., Valiente, E., Corton, C., et al. (2009). Comparative genome and phenotypic analysis of Clostridium difficile 027 strains provides insight into the evolution of a hypervirulent bacterium. Genome Biol. 10, R102. doi: 10.1186/gb-2009-10-9-r102.
75. Steindl, G., Fiedler, A., Huhulescu, S., Wewalka, G., and Allerberger, F. (2015). Effect of airborne hydrogen peroxide on spores of Clostridium difficile. Wien. Klin. Wochenschr. 127, 421-426. doi: 10.1007/s00508-014-0682-6.
76. Theriot, C. M., Bowman, A. A., and Young, V. B. (2016). Antibiotic-induced alterations of the gut microbiota alter secondary bile acid production and allow for Clostridium difficile spore germination and outgrowth in the large intestine. mSphere 1, e45-15. doi: 10.1128/mSphere.00045-15.
77. Theriot, C. M., and Young, V. B. (2015). Interactions between the gastrointestinal microbiome and Clostridium difficile. Annu. Rev. Microbiol. 69, 445-461. doi: 10.1146/annurev-micro-091014-104115.
78. Thomas, C. M., and Smith, C. A. (1987). Incompatibility group P plasmids: genetics, evolution, and use in genetic manipulation. Annu. Rev. Microbiol. 41, 77-101. doi: 10.1146/annurev.mi.41.100187.000453.
79. Tracy, B. P., Jones, S. W., and Papoutsakis, E. T. (2011). Inactivation of sigmaE and sigmaG in Clostridium acetobutylicum illuminates their roles in clostridial-cell-form biogenesis, granulose synthesis, solventogenesis, and spore morphogenesis. J. Bacteriol. 193, 1414-1426. doi: 10.1128/JB.01380-10.
80. Vohra, P., and Poxton, I. R. (2011). Efficacy of decontaminants and disinfectants against Clostridium difficile. J. Med. Microbiol 60(Pt 8), 1218-1224. doi: 10.1099/jmm.0.030288-30280.
81. Voth, D. E., and Ballard, J. D. (2005). Clostridium difficile toxins: mechanism of action and role in disease. Clin. Microbiol. Rev. 18, 247-263. doi: 10.1128/CMR.18.2.247-263.2005.
82. Wilcox, M. H., Fawley, W. N., Wigglesworth, N., Parnell, P., Verity, P., and Freeman, J. (2003). Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection. J. Hosp. Infect. 54, 109-114. doi: 10.1016/S0195-6701(02)00400-0.
83. Wilson, K. H., Kennedy, M. J., and Fekety, F. R. (1982). Use of sodium taurocholate to enhance spore recovery on a medium selective for Clostridium difficile. J. Clin. Microbiol. 15, 443-446.