Effect of thermal control of dry fomites on regulating the survival of human pathogenic bacteria responsible for nosocomial infections


Autoři: Tomoko Shimoda aff001;  Torahiko Okubo aff002;  Yoshiki Enoeda aff001;  Rika Yano aff001;  Shinji Nakamura aff003;  Jeewan Thapa aff002;  Hiroyuki Yamaguchi aff002
Působiště autorů: Department of Fundamental Nursing, Faculty of Health Sciences, Hokkaido University, Sapporo, Japan aff001;  Department of Medical Laboratory Science, Faculty of Health Sciences, Hokkaido University, Sapporo, Japan aff002;  Laboratory of Morphology and Image Analysis, Biomedical Research Center, Juntendo University Graduate School of Medicine, Tokyo, Japan aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226952

Souhrn

We monitored the survival of human pathogenic bacteria [Escherichia coli (ATCC), extended-spectrum β-lactamase-producing E. coli (Clinical isolate), New Delhi metallo-β-lactamase-producing E. coli (clinical isolate), Staphylococcus aureus (ATCC)] on dry materials (vinyl chloride, aluminum, plastic, stainless steel) at distinct temperatures (room temperature or 15°C–37°C). These bacteria favored a lower temperature for their prolonged survival on the dry fomites, regardless of the material type. Interestingly, when mixed with S. aureus, E. coli survived for a longer time at a lower temperature. Cardiolipin, which can promote the survival of S. aureus in harsh environments, had no effect on maintaining the survival of E. coli. Although the trends remained unchanged, adjusting the humidity from 40% to 60% affected the survival of bacteria on dry surfaces. Scanning electron microscopic analysis revealed no morphological differences in these bacteria immediately before or after one day of dry conditions. In addition, ATP assessment, a method used to visualize high-touch surfaces in hospitals, was not effective at monitoring bacterial dynamics. A specialized handrail device fitted with a heater, which was maintained at normal human body core temperature, successfully prohibited the prolonged survival of bacteria [Enterococcus faecalis (ATCC), E. coli (ATCC), Pseudomonas aeruginosa (ATCC), S. aureus (ATCC), Acinetobacter baumannii (clinical isolate), and Serratia marcescens (clinical isolate)], with the exception of spore-forming Bacillus subtilis (from our laboratory collection) and the yeast-like fungus Candida albicans (from our laboratory collection)] on dry surfaces. Taken together, we concluded that the tested bacteria favor lower temperatures for their survival in dry environments. Therefore, the thermal control of dry fomites has the potential to control bacterial survival on high-touch surfaces in hospitals.

Klíčová slova:

Bacterial pathogens – Body temperature – Enterococcus faecalis – Humidity – Chlorides – Nosocomial infections – Stainless steel – Staphylococcus aureus


Zdroje

1. Cobrado L, Silva-Dias A, Azevedo MM, Rodrigues AG. (2017) High-touch surfaces: microbial neighbours at hand. Eur J Clin Microbiol Infect Dis 36:2053–2062. doi: 10.1007/s10096-017-3042-4 28647859

2. Han JH, Sullivan N, Leas BF, Pegues DA, Kaczmarek JL, Umscheid CA. (2015) Cleaning Hospital Room Surfaces to Prevent Health Care-Associated Infections: A Technical Brief. Ann Intern Med 163:598–607. doi: 10.7326/M15-1192 26258903

3. Carling PC, Bartley JM. (2010) Evaluating hygienic cleaning in health care settings: what you do not know can harm your patients. Am J Infect Control 38(5 Suppl 1):S41–50. doi: 10.1016/j.ajic.2010.03.004 20569855

4. Rutala WA, Weber DJ. (2016) Monitoring and improving the effectiveness of surface cleaning and disinfection. Am J Infect Control 44(5 Suppl):e69–76. doi: 10.1016/j.ajic.2015.10.039 27131138

5. Donskey CJ. (2013) Does improving surface cleaning and disinfection reduce health care-associated infections? Am J Infect Control 41(5 Suppl):S12–19. doi: 10.1016/j.ajic.2012.12.010 23465603

6. Boyce JM. (2016) Modern technologies for improving cleaning and disinfection of environmental surfaces in hospitals. Antimicrob Resist Infect Control 5:10. doi: 10.1186/s13756-016-0111-x 27069623

7. Dancer SJ, White LF, Lamb J, Girvan EK, Robertson C. (2009) Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med 7:28. doi: 10.1186/1741-7015-7-28 19505316

8. Dancer SJ, White L, Robertson C. (2008) Monitoring environmental cleanliness on two surgical wards. Int J Environ Health Res 18:357–364. doi: 10.1080/09603120802102465 18821374

9. Dancer SJ. (2009) The role of environmental cleaning in the control of hospital-acquired infection. J Hosp Infect 73:378–385. doi: 10.1016/j.jhin.2009.03.030 19726106

10. Carling PC. (2016) Optimizing Health Care Environmental Hygiene. Infect Dis Clin North Am 30:639–660. doi: 10.1016/j.idc.2016.04.010 27515141

11. Anderson RE, Young V, Stewart M, Robertson C, Dancer SJ. (2011) Cleanliness audit of clinical surfaces and equipment: who cleans what? J Hosp Infect 78:178–181. doi: 10.1016/j.jhin.2011.01.030 21497943

12. Carling PC, Bartley JM. (2010) Evaluating hygienic cleaning in health care settings: what you do not know can harm your patients. Am J Infect Control 38(5 Suppl 1):S41–50. doi: 10.1016/j.ajic.2010.03.004 20569855

13. Park JW, Lee KJ, Lee KH, Lee SH, Cho JR, Mo JW, Choi SY, Kwon GY, Shin JY, Hong JY, Kim J, Yeon MY, Oh JS, Nam HS. (2017) Hospital Outbreaks of Middle East Respiratory Syndrome, Daejeon, South Korea, 2015. Emerg Infect Dis 23:898–905. doi: 10.3201/eid2306.160120 28516865

14. Ocampo W, Geransar R, Clayden N, Jones J, de Grood J, Joffe M, Taylor G, Missaghi B, Pearce C, Ghali W, Conly J. (2017) Environmental scan of infection prevention and control practices for containment of hospital-acquired infectious disease outbreaks in acute care hospital settings across Canada. Am J Infect Control 45:1116–1126. doi: 10.1016/j.ajic.2017.05.014 28732739

15. Hurford A, Lin AL, Wu J. (2015) Determinants of the Final Size and Case Rate of Nosocomial Outbreaks. PLoS One 10:e0138216. doi: 10.1371/journal.pone.0138216 26371880

16. Watanabe R, Shimoda T, Yano R, Hayashi Y, Nakamura S, Matsuo J, Yamaguchi H. (2014) Visualization of hospital cleanliness in three Japanese hospitals with a tendency toward long-term care. BMC Res Notes 7:121. doi: 10.1186/1756-0500-7-121 24593868

17. Shimoda T, Yano R, Nakamura S, Yoshida M, Matsuo J, Yoshimura S, Yamaguchi H. (2015) ATP bioluminescence values are significantly different depending upon material surface properties of the sampling location in hospitals. BMC Res Notes 8:807. doi: 10.1186/s13104-015-1757-9 26689425

18. Yano R, Shimoda T, Watanabe R, Kuroki Y, Okubo T, Nakamura S, Matsuo J, Yoshimura S, Yamaguchi H. (2017) Diversity changes of microbial communities into hospital surface environments. J Infect Chemother 23:439–445. doi: 10.1016/j.jiac.2017.03.016 28431935

19. Panagea S, Winstanley C, Walshaw MJ, Ledson MJ, Hart CA. (2005) Environmental contamination with an epidemic strain of Pseudomonas aeruginosa in a Liverpool cystic fibrosis centre, and study of its survival on dry surfaces. J Hosp Infect 59:102–107. doi: 10.1016/j.jhin.2004.09.018 15620443

20. Espinal P, Martí S, Vila J. (2012) Effect of biofilm formation on the survival of Acinetobacter baumannii on dry surfaces. J Hosp Infect 80:56–60. doi: 10.1016/j.jhin.2011.08.013 21975219

21. Warnes SL, Keevil CW. (2011) Mechanism of copper surface toxicity in vancomycin-resistant enterococci following wet or dry surface contact. Appl Environ Microbiol 77:6049–6059. doi: 10.1128/AEM.00597-11 21742916

22. Maudsdotter L, Imai S, Ohniwa RL, Saito S, Morikawa K. (2015) Staphylococcus aureus dry stress survivors have a heritable fitness advantage in subsequent dry exposure. Microbes Infect 17:456–461. doi: 10.1016/j.micinf.2015.02.004 25749710

23. Havill NL, Boyce JM, Otter JA. (2014) Extended survival of carbapenem-resistant Enterobacteriaceae on dry surfaces. Infect Control Hosp Epidemiol 35:445–447. doi: 10.1086/675606 24602956

24. Havill NL, Boyce JM, Otter JA. (2014) Extended survival of carbapenem-resistant Enterobacteriaceae on dry surfaces. Infect Control Hosp Epidemiol 35:445–447. doi: 10.1086/675606 24602956

25. Farhana I, Hossain ZZ, Tulsiani SM, Jensen PK, Begum A. (2016) Survival of Vibrio cholerae O1 on fomites. World J Microbiol Biotechnol 32:146. doi: 10.1007/s11274-016-2100-x 27430513

26. Okubo T, Matushita M, Ohara Y, Matsuo J, Oguri S, Fukumoto T, Hayasaka K, Akizawa K, Shibuya H, Shimizu C, Yamaguchi H. (2017) Ciliates promote the transfer of a plasmid encoding blaNDM-5 from Escherichia coli, isolated from a hospital in Japan, to other human pathogens. Int J Antimicrob Agents 49:387–388. doi: 10.1016/j.ijantimicag.2017.01.003 28167346

27. Okubo T, Matsushita M, Nakamura S, Matsuo J, Nagai H, Yamaguchi H. (2018) Acanthamoeba S13WT relies on its bacterial endosymbiont to backpack human pathogenic bacteria and resist Legionella infection on solid media. Environ Microbiol Rep 10:344–354. doi: 10.1111/1758-2229.12645 29611898

28. Maudsdotter L, Imai S, Ohniwa RL, Saito S, Morikawa K. (2015) Staphylococcus aureus dry stress survivors have a heritable fitness advantage in subsequent dry exposure. Microbes Infect 17:456–461. doi: 10.1016/j.micinf.2015.02.004 25749710

29. Beining PR, Huff E, Prescott B, Theodore TS. (1975) Characterization of the lipids of mesosomal vesicles and plasma membranes from Staphylococcus aureus. J Bacteriol 121:137–143. 1116984

30. Shannon RP. (2011) Eliminating hospital acquired infections: is it possible? Is it sustainable? Is it worth it? Trans Am Clin Climatol Assoc 122:103–114. 21686213

31. Farhangi MB, Safari Sinegani AA, Mosaddeghi MR, Unc A, Khodakaramian G. (2013) Impact of calcium carbonate and temperature on survival of Escherichia coli in soil. J Environ Manage 119:13–19. doi: 10.1016/j.jenvman.2013.01.022 23434791

32. Redfern J, Verran J. (2017) Effect of humidity and temperature on the survival of Listeria monocytogenes on surfaces. Lett Appl Microbiol 64:276–282. doi: 10.1111/lam.12714 28101930

33. Browne C, Loeffler A, Holt HR, Chang YM, Lloyd DH, Nevel A. (2017) Low temperature and dust favour in vitro survival of Mycoplasma hyopneumoniae: time to revisit indirect transmission in pig housing. Lett Appl Microbiol 64:2–7. doi: 10.1111/lam.12689 27759918

34. Esteves DC, Pereira VC, Souza JM, Keller R, Simões RD, Winkelstroter Eller LK, Rodrigues MV. (2016) Influence of biological fluids in bacterial viability on different hospital surfaces and fomites. Am J Infect Control 4:311–314.

35. Galvin S, Dolan A, Cahill O, Daniels S, Humphreys H. (2012) Microbial monitoring of the hospital environment: why and how? J Hosp Infect 82:143–151. doi: 10.1016/j.jhin.2012.06.015 23022372

36. Abreu AC, Tavares RR, Borges A, Mergulhão F, Simões M. (2013) Current and emergent strategies for disinfection of hospital environments. J Antimicrob Chemother 68:2718–2732. doi: 10.1093/jac/dkt281 23869049

37. Bergmann TWM, Kappers AM. (2008) Thermosensory reversal effect quantified. Acta Psychol (Amst) 127:46–50.

38. Moore G, Smyth D, Singleton J, Wilson P. (2010) The use of adenosine triphosphate bioluminescence to assess the efficacy of a modified cleaning program implemented within an intensive care setting. Am J Infect Control 38: 617–622. doi: 10.1016/j.ajic.2010.02.011 20605265

39. Boyce JM, Havill NL, Dumigan DG, Golebiewski M, Balogun O, Rizvani R. (2009) Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay. Infect Control Hosp Epidemiol 30: 678–684. doi: 10.1086/598243 19489715

40. Andersen BM, Rasch M, Kvist J, Tollefsen T, Lukkassen R, Sandvik L, Welo A. (2009) Floor cleaning: effect on bacteria and organic materials in hospital rooms. J Hosp Infect 71: 57–65. doi: 10.1016/j.jhin.2008.09.014 19013671

41. Malik RE, Cooper RA, Griffith CJ. (2003) Use of audit tools to evaluate the efficacy of cleaning systems in hospitals. Am J Infect Control 31: 181–187. doi: 10.1067/mic.2003.34 12734526

42. Griffith CJ, Cooper RA, Gilmore J, Davies C, Lewis M. (2000) An evaluation of hospital cleaning regimes and standards. J Hosp Infect 45: 19–28. doi: 10.1053/jhin.1999.0717 10833340

43. Musatov A, Sedlák E. (2017) Role of cardiolipin in stability of integral membrane proteins. Biochimie 142:102–111. doi: 10.1016/j.biochi.2017.08.013 28842204

44. Maudsdotter L, Imai S, Ohniwa RL, Saito S, Morikawa K. (2015) Staphylococcus aureus dry stress survivors have a heritable fitness advantage in subsequent dry exposure. Microbes Infect 17:456–461. doi: 10.1016/j.micinf.2015.02.004 25749710

45. Xie Y, Yang L. (2016) Calcium and magnesium ions are membrane-active against stationary-phase Staphylococcus aureus with high specificity. Sci Rep 6:20628. doi: 10.1038/srep20628 26865182

46. Nepper JF, Lin YC, Weibel DB. (2019) Rcs Phosphorelay Activation in cardiolipin-deficient Escherichia coli reduces biofilm formation. J Bacteriol 201(9). pii: e00804-18.

47. Lin TY, Santos TM, Kontur WS, Donohue TJ, Weibel DB. (2015) A cardiolipin-deficient mutant of Rhodobacter sphaeroides has an altered cell shape and is impaired in biofilm formation. J Bacteriol 197:3446–3455. doi: 10.1128/JB.00420-15 26283770

48. Russotto V, Cortegiani A, Raineri SM, Giarratano A. (2105) Bacterial contamination of inanimate surfaces and equipment in the intensive care unit. J Intensive Care 3:54.

49. Wolkoff P. (2018) Indoor air humidity, air quality, and health—An overview. Int J Hyg Environ Health 221:376–390. doi: 10.1016/j.ijheh.2018.01.015 29398406


Článek vyšel v časopise

PLOS One


2019 Číslo 12