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Pseudomonas aeruginosa dose response and bathing water infection

  • D. J. ROSER (a1), B. VAN DEN AKKER (a1), S. BOASE (a2), C. N. HAAS (a3), N. J. ASHBOLT (a1) (a4) and S. A. RICE (a5) (a6)...


Pseudomonas aeruginosa is the opportunistic pathogen mostly implicated in folliculitis and acute otitis externa in pools and hot tubs. Nevertheless, infection risks remain poorly quantified. This paper reviews disease aetiologies and bacterial skin colonization science to advance dose-response theory development. Three model forms are identified for predicting disease likelihood from pathogen density. Two are based on Furumoto & Mickey's exponential ‘single-hit’ model and predict infection likelihood and severity (lesions/m2), respectively. ‘Third-generation’, mechanistic, dose-response algorithm development is additionally scoped. The proposed formulation integrates dispersion, epidermal interaction, and follicle invasion. The review also details uncertainties needing consideration which pertain to water quality, outbreaks, exposure time, infection sites, biofilms, cerumen, environmental factors (e.g. skin saturation, hydrodynamics), and whether P. aeruginosa is endogenous or exogenous. The review's findings are used to propose a conceptual infection model and identify research priorities including pool dose-response modelling, epidermis ecology and infection likelihood-based hygiene management.

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Corresponding author

* Author for correspondence: D. J. Roser, UNSW Water Research Centre, School of Civil and Environmental Engineering, University of New South Wales, Sydney, New South Wales, 2052, Australia. (Email:


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1. Mena, KD, Gerba, CP. Risk assessment of Pseudomonas aeruginosa in water. In: Whitacre, DM, ed. Reviews of Environmental Contamination and Toxicology: Springer USA, 2009: 71115.
2. Rice, SA, et al. A risk assessment of Pseudomonas aeruginosa in swimming pools: a review. Journal of Water and Health 2012; 10: 181196.
3. Julien, E, et al. The key events dose-response framework: a cross-disciplinary mode-of-action based approach to examining dose-response and thresholds. Critical Reviews in Food Science and Nutrition 2009; 49: 682689.
4. Jacobson, J. Pool-associated Pseudomonas aeruginosa dermatitis and other bathing-associated infections. Infection Control 1985; 6: 398401.
5. Maniatis, AN, et al. Pseudomonas aeruginosa folliculitis due to Non-O:11 serogroups: acquisition through use of contaminated synthetic sponges. Clinical Infectious Diseases 1995; 21: 437439.
6. Beers, SL, Abramo, TJ. Otitis externa review. Pediatric Emergency Care 2004; 20: 250256.
7. Barna, Z, Kádár, M. The risk of contracting infectious diseases in public swimming pools. A review. Annali dell'Istituto Superiore di Sanità 2012; 48: 374386.
8. Price, D, Ahearn, DG. Incidence and persistence of Pseudomonas aeruginosa in whirlpools. Journal of Clinical Microbiology 1988; 26: 16501654.
9. Magnússon, SH, et al. State of the art in benefit–risk analysis: food microbiology. Food and Chemical Toxicology 2012; 50: 3339.
10. Ratnam, S, et al. Whirlpool-associated folliculitis caused by Pseudomonas aeruginosa: report of an outbreak and review. Journal of Clinical Microbiology 1986; 23: 655659.
11. Schets, FM, Schijven, JF, de Roda Husman, AM. Exposure assessment for swimmers in bathing waters and swimming pools. Water Research 2011; 45: 23922400.
12. Kaper, JB, Nataro, JP, Mobley, HLT. Pathogenic Escherichia coli . Nature Reviews Microbiology 2004; 2: 123140.
13. Sattentau, Q. Avoiding the void: cell-to-cell spread of human viruses. Nature Reviews Microbiology 2008; 6: 815826.
14. Teunis, PFM, Havelaar, AH. The Beta Poisson dose-response model is not a single hit model. Risk Analysis 2000; 20: 513520.
15. Haas, CN, Eisenberg, JNS. Risk assessment. In: Fewtrell, L, Bartram, J, eds. Water Quality Guidelines, Standards and Health: Assessment of Risk and Risk Management for Water-related Infectious Disease. London UK.: IWA Publishing/WHO, 2001, pp. 161183.
16. Teunis, PFM, Ogden, ID, Strachan, NJC. Hierarchical dose response of E. coli O157:H7 from human outbreaks incorporating heterogeneity in exposure. Epidemiology and Infection 2008; 136: 761770.
17. Furumoto, WA, Mickey, R. A mathematical model for the infectivity-dilution curve of tobacco mosaic virus: theoretical considerations. Virology 1967; 32: 216223.
18. Furumoto, WA, Mickey, R. A mathematical model for the infectivity-dilution curve of tobacco mosaic virus: experimental tests. Virology 1967; 32: 224233.
19. Tamrakar, SB, Haas, CN. Dose-response model of rocky mountain spotted fever (RMSF) for humans. Risk Analysis 2011; 31: 16101621.
20. Tamrakar, SB, Dose-response models of rickettsiae and other biological agents of concern (thesis). Philadelphia, PA, USA: Drexel University, 2011, 220 pp.
21. Rose, JB, Haas, CN. A risk assessment framework for the evaluation of skin infections and the potential impact of antibacterial soap washing. American Journal of Infection Control 1999; 27: S26S33.
22. Highsmith, AK, et al. Characteristics of Pseudomonas aeruginosa isolated from whirlpools and bathers. Infection Control 1985; 6: 407412.
23. Hajjartabar, M. Poor-quality water in swimming pools associated with a substantial risk of otitis externa due to Pseudomonas aeruginosa . Water Science and Technology 2004; 50: 6367.
24. Van, Asperen IA, et al. Risk of otitis externa after swimming in recreational fresh water lakes containing Pseudomonas aeruginosa . British Medical Journal 1995; 311: 14071410.
25. Jones, F, et al. Results of the first pilot-scale controlled cohort epidemiological investigation into the possible health effects of bathing in seawater at Langland Bay, Swansea. Water and Environment Journal 1991; 5: 9198.
26. Prieto, MD, et al. Recreation in coastal waters: health risks associated with bathing in sea water. Journal of Epidemiology and Community Health 2001; 55: 442447.
27. Hojyo-Tomoka, MT, Marples, RR, Kligman, AM. Pseudomonas infection in superhydrated skin. Archives of Dermatology 1973; 107: 723.
28. Grice, EA, Segre, JA. The skin microbiome. Nature Reviews Microbiology 2011; 9: 244253.
29. Leyden, JJ, Stewart, R, Kligman, AM. Experimental inoculation of Pseudomonas aeruginosa and Pseudomonas cepaciae on human skin. Journal of the Society of Cosmetic Chemists 1980; 31: 1928.
30. Gustafson, TL, et al. Pseudomonas folliculitis: an outbreak and review. Review of Infectious Diseases 1983; 5: 18.
31. Rice, SA, et al. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. ISME Journal 2008; 3: 271282.
32. Lyczak, JB, Cannon, CL, Pier, GB. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes and Infection 2000; 2: 10511060.
33. Cogen, AL, Nizet, V, Gallo, RL. Skin microbiota: a source of disease or defence? British Journal of Dermatology 2008; 158: 442455.
34. Schets, F, et al. Cercarial dermatitis in the Netherlands caused by Trichobilharzia spp. Journal of Water and Health 2008; 6: 187195.
35. Hattermann, D, Ries, S. Motility of Pseudomonas syringae pv. glycinea and its role in infection. Phytopathology 1989; 79: 284289.
36. Otberg, N, et al. Variations of hair follicle size and distribution in different body sites. Journal of Investigative Dermatology 2004; 122: 1419.
37. Poet, TS, McDougal, JN. Skin absorption and human risk assessment. Chemico-Biological Interactions 2002; 140: 1934.
38. Spagnuolo, AM, DiRita, V, Kirschner, D. A model for Vibrio cholerae colonization of the human intestine. Journal of Theoretical Biology 2011; 289: 247258.
39. Bartumeus, F, et al. Optimizing the encounter rate in biological interactions: Lévy versus Brownian strategies. Physical Review Letters 2002; 88: 097901.
40. Valentine, RC, Allison, AC. Virus particle adsorption I. Theory of adsorption and experiments on the attachment of particles to non-biological surfaces. Biochimica et Biophysica Acta 1959; 34: 1023.
41. Allison, AC, Valentine, RC. Virus particle adsorption: II. Adsorption of vaccinia and fowl plague viruses to cells in suspension. Biochimica et Biophysica Acta 1960; 40: 393399.
42. Murray, AG, Jackson, GA. Viral dynamics: a model of the effects size, shape, motion and abundance of single-celled planktonic organisms and other particles. Marine Ecology Progress Series 1992; 89: 103116.
43. Mueller, RF. Bacterial transport and colonization in low nutrient environments. Water Research 1996; 30: 26812690.
44. Wei, Y, et al. The population dynamics of bacteria in physically structured habitats and the adaptive virtue of random motility. Proceedings of the National Academy of Sciences USA 2011; 108: 40474052.
45. Kim, Y-C. Diffusivity of bacteria. Korean Journal of Chemical Engineering 1996; 13: 282287.
46. Ping, L. Cell orientation of swimming bacteria: from theoretical simulation to experimental evaluation. Science China Life Sciences 2012; 55: 202209.
47. Panopoulos, N, Schroth, M. Role of flagellar motility in the invasion of bean leaves by Pseudomonas phaseolicola . Phytopathology 1974; 64: 13891397.
48. Liu, J, Ford, RM, Smith, JA. Idling time of motile bacteria contributes to retardation and dispersion in sand porous medium. Environmental Science & Technology 2011; 45: 39453951.
49. Katsikogianni, M, Missirlis, Y. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria–material interactions. European Cells and Materials 2004; 8: 3757.
50. Miller, MB, Bassler, BL. Quorum sensing in bacteria. Annual Reviews in Microbiology 2001; 55: 165199.
51. Wingender, J, Flemming, H-C. Biofilms in drinking water and their role as reservoir for pathogens. International Journal of Hygiene and Environmental Health 2011; 214: 417423.
52. Charlton, TS, et al. A novel and sensitive method for the quantification of N-3-oxoacyl homoserine lactones using gas chromatography–mass spectrometry: application to a model bacterial biofilm. Environmental Microbiology 2000; 2: 530541.
53. Krachler, AM, Ham, H, Orth, K. Turnabout is fair play: use of the bacterial multivalent adhesion molecule 7 as an antimicrobial agent. Virulence 2012; 3: 6871.
54. Jacobs, A, et al. Kinetic adhesion of bacterial cells to sand: cell surface properties and adhesion rate. Colloids and Surfaces. B: Biointerfaces 2007; 59: 3545.
55. Liu, Y, Tay, J-H. The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Research 2002; 36: 16531665.
56. Fletcher, M. The effects of culture concentration and age, time, and temperature on bacterial attachment to polystyrene. Canadian Journal of Microbiology 1977; 23: 16.
57. Mueller, RF, et al. Characterization of initial events in bacterial surface colonization by two Pseudomonas species using image analysis. Biotechnology and Bioengineering 1992; 39: 11611170.
58. Chen, MJ, Zhang, Z, Bott, TR. Effects of operating conditions on the adhesive strength of Pseudomonas fluorescens biofilms in tubes. Colloids and Surfaces. B: Biointerfaces 2005; 43: 6171.
59. Li, G, Tam, L-K, Tang, JX. Amplified effect of Brownian motion in bacterial near-surface swimming. Proceedings of the National Academy of Sciences USA 2008; 105: 1835518359.
60. Conrad, JC, et al. Flagella and pili-mediated near-surface single-sell motility mechanisms in P . aeruginosa. Biophysical Journal 2011; 100: 16081616.
61. Celli, JP, et al. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proceedings of the National Academy of Sciences USA 2009; 106: 1432114326.
62. Xie, L, et al. Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis. Proceedings of the National Academy of Sciences USA 2011; 108: 22462251.
63. Kato, J, et al. Pseudomonas aeruginosa as a model microorganism for investigation of chemotactic behaviors in ecosystem. Journal of Bioscience and Bioengineering 2008; 106: 17.
64. Armitage, JP, Evans, MCW. The motile and tactic behaviour of Pseudomonas aeruginosa in anaerobic environments. FEBS Letters 1983; 156: 113118.
65. Stoodley, P, et al. Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology. Biotechnology and Bioengineering 1999; 65: 8392.
66. Wosicka, H, Cal, K. Targeting to the hair follicles: current status and potential. Journal of Dermatological Science 2010; 57: 8389.
67. Toll, R, et al. Penetration profile of microspheres in follicular targeting of terminal hair follicles. Journal of Investigative Dermatology 2003; 123: 168176.
68. Fiorillo, L, et al. The Pseudomonas hot-foot syndrome. New England Journal of Medicine 2001; 345: 335338.
69. Maroonroge, S, Emanuel, DC, Letowski, TR. Basic anatomy of the hearing system. In: Rash, CE, et al. , eds. Helmet-Mounted Displays: Sensation, Perception and Cognition Issues. Fort Rucker, Alabama: U.S. Army Aeromedical Research Laboratory, 2000, pp. 279306.
70. Miller, MC, McCave, IN, Komar, PD. Threshold of sediment motion under unidirectional currents. Sedimentology 1977; 24: 507527.
71. McCoy, WF, et al. Observations of fouling biofilm formation. Canadian Journal of Microbiology 1981; 27: 910917.
72. Stanley, PM. Factors affecting the irreversible attachment of Pseudomonas aeruginosa to stainless steel. Canadian Journal of Microbiology 1983; 29: 14931499.
73. Vargiolu, H, Zahouani, R. Skin line morphology: tree and branches. In: Agache, P, et al. , eds. Measuring the Skin. Heidelberg: Springer-Verlag, 2004, pp. 4059.
74. Scheuerman, TR, Camper, AK, Hamilton, MA. Effects of substratum topography on bacterial adhesion. Journal of Colloid and Interface Science 1998; 208: 2333.
75. Frank, JF. Microbial attachment to food and food contact surfaces. Advances in Food and Nutrition Research 2001; 43: 319370.
76. Judd, SJ, Bullock, G. The fate of chlorine and organic materials in swimming pools. Chemosphere 2003; 51: 869879.
77. Goeres, DM, et al. Evaluation of disinfectant efficacy against biofilm and suspended bacteria in a laboratory swimming pool model. Water Research 2004; 38: 31033109.
78. Stover, CK, et al. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 2000; 406: 959964.
79. Ramos, JL, ed. Pseudomonas: Genomics, Life Style and Molecular Architecture: Kluwer, New York, 2004, pp. 835.
80. Huang, Y, Haas, CN. Time-dose-response models for microbial risk assessment. Risk Analysis 2009; 29: 648661.
81. Warner, RR, Stone, KJ, Boissy, YL. Hydration disrupts human stratum corneum ultrastructure. Journal of Investigative Dermatology 2003; 120: 275284.
82. Hudson, PJ, et al. Duration of whirlpool-spa use as a risk factor for Pseudomonas dermatitis. American Journal of Epidemiology 1985; 122: 915917.
83. Richards, AM, et al. Cellular microbiology and molecular ecology of Legionella–amoeba interaction. Virulence 2013; 4: 307314.
84. Frank, DN, et al. Culture-independent molecular analysis of microbial constituents of the healthy human outer ear. Journal of Clinical Microbiology 2003; 41: 295303.
85. Hanger, H, Mulley, G. Cerumen: its fascination and clinical importance: a review. Journal of the Royal Society of Medicine 1992; 85: 346.
86. Campos, A, et al. Influence of human wet cerumen on the growth of common and pathogenic bacteria of the ear. Journal of Laryngology & Otology 2000; 114: 925929.
87. Steuer, MK, et al. Are ABH antigenic determinants on human outer ear canal epithelium responsible for Pseudomonas aeruginosa infections? Journal of Otorhinolaryngology and Related Specialities 1995; 57: 148152.
88. World Health Organization. Guidelines for Safe Recreational Water Environments. Volume 2, Swimming pools and similar environments. World Health Organisation, 2006.
89. Hollyoak, V, Boyd, P, Freeman, R. Whirlpool baths in nursing homes: use maintenance and contamination with Pseudomonas aeruginosa . Communicable Disease Report 1995; 5: R102R104.
90. Hollyoak, V, Allison, D, Summers, J. Pseudomonas aeruginosa wound infection associated with a nursing home's whirlpool bath. Communicable Disease Report 1995; 5: R100R101.
91. Khabbaz, RF, et al. Pseudomonas aeruginosa serotype 0:9 : New cause of whirlpool-associated dermatitis. American Journal of Medicine 1983; 74: 7377.
92. Washburn, J, et al. Pseudomonas aeruginosa rash associated with a whirlpool. Journal of the American Medical Association 1976; 235: 22052207.
93. Hopkins, RS, Abbott, DO, Wallace, LE. Follicular dermatitis outbreak caused by Pseudomonas aeruginosa associated with a motel's indoor swimming pool. Public Health Reports 1981; 96: 246249.
94. Hewitt, JH. Pseudomonas aeruginosa and whirlpools. British Medical Journal 1985; 290: 13531354.
95. Kush, BJ, Hoadley, AW. A preliminary survey of the association of Ps. aeruginosa with commercial whirlpool bath waters. American Journal of Public Health 1980; 70: 279281.
96. Moore, J, et al. Incidence of Pseudomonas aeruginosa in recreational and hydrotherapy pools. Communicable Disease and Public Health 2002; 5: 2326.


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Pseudomonas aeruginosa dose response and bathing water infection

  • D. J. ROSER (a1), B. VAN DEN AKKER (a1), S. BOASE (a2), C. N. HAAS (a3), N. J. ASHBOLT (a1) (a4) and S. A. RICE (a5) (a6)...


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