Microbial Sampling from Dry Surfaces: Current Challenges and Solutions

  • Ilya Digel
  • Nuraly Sh. Akimbekov
  • Aida Kistaubayeva
  • Azhar A. Zhubanova
Chapter

Abstract

Sampling of dry surfaces for microorganisms is a main component of microbiological safety and is of critical importance in many fields including epidemiology, astrobiology as well as numerous branches of medical and food manufacturing. Aspects of biofilm formation, analysis and removal in aqueous solutions have been thoroughly discussed in literature. In contrast, microbial communities on air-exposed (dry) surfaces have received significantly less attention. Diverse surface sampling methods have been developed in order to address various surfaces and microbial groups, but they notoriously show poor repeatability, low recovery rates and suffer from lack of mutual consistency. Quantitative sampling for viable microorganisms represents a particular challenge, especially on porous and irregular surfaces. Therefore, it is essential to examine in depth the factors involved in microorganisms’ recovery efficiency and accuracy depending on the sampling technique used. Microbial colonization, retention and community composition on different dry surfaces are very complex and rely on numerous physicochemical and biological factors. This study is devoted to analyze and review the (a) physical phenomena and intermolecular forces relevant for microbiological surface sampling; (b) challenges and problems faced by existing sampling methods for viable microorganisms and (c) current directions of engineering and research aimed at improvement of quality and efficiency of microbiological surface sampling.

Keywords

Sampling methods Surface microorganisms Dry surfaces Microbial adhesion Swabbing Contact plates Sonication 

Notes

Acknowledgements

Our research for this chapter was partially financially supported by the K2-Commission of FH-Aachen University of Applied Sciences. We have also received very helpful input from Peter Kayser, Dariusz Porst, Alexandra Lösch, Konstantin Kotliar, Bernd Dachwald, Stephan Neumann, Gerhard Artmann, Shachriar Dantism. We would like to thank Ms. Danielle Hillebrecht for the valuable comments and help in the manuscript preparation.

References

  1. 1.
    Ismaïl, R., Aviat, F., Michel, V., Le Bayon, I., Gay-Perret, P., Kutnik, M., et al. (2013). Methods for recovering microorganisms from solid surfaces used in the food industry: A review of the literature. International Journal of Environmental Research and Public Health, 10(11), 6169–6183.  https://doi.org/10.3390/ijerph10116169.CrossRefGoogle Scholar
  2. 2.
    Dunne, W. M. (2002). Bacterial adhesion: Seen any good biofilms lately? Clinical Microbiology Reviews, 15(2), 155–166.  https://doi.org/10.1128/cmr.15.2.155-166.2002.CrossRefGoogle Scholar
  3. 3.
    Watnick, P., & Kolter, R. (2000). Biofilm, city of microbes. Journal of Bacteriology, 182(10), 2675–2679.CrossRefGoogle Scholar
  4. 4.
    Parsek, M. R., & Fuqua, C. (2004). Biofilms 2003: Emerging themes and challenges in studies of surface-associated microbial life. Journal of Bacteriology, 186(14), 4427–4440.  https://doi.org/10.1128/jb.186.14.4427-4440.2004.CrossRefGoogle Scholar
  5. 5.
    Schmedes, S. E., Sajantila, A., & Budowle, B. (2016). Expansion of microbial forensics. Journal of Clinical Microbiology, 54(8), 1964–1974.  https://doi.org/10.1128/jcm.00046-16.CrossRefGoogle Scholar
  6. 6.
    Smith, D., Martin, D., & Novossiolova, T. (2017). Microorganisms: Good or evil. MIRRI provides biosecurity awareness. Current Microbiology, 74(3), 299–308.  https://doi.org/10.1007/s00284-016-1181-y.CrossRefGoogle Scholar
  7. 7.
    Hess, B. M., Amidan, B. G., Anderson, K. K., Hutchison, J. R. (2016). Evaluating composite sampling methods of bacillus spores at low concentrations. PLoS One 11(10).  https://doi.org/10.1371/journal.pone.0164582.CrossRefGoogle Scholar
  8. 8.
    Priyanka, B., Patil, R. K., & Dwarakanath, S. (2016). A review on detection methods used for foodborne pathogens. Indian Journal of Medical Research, 144(3), 327–338.  https://doi.org/10.4103/0971-5916.198677.CrossRefGoogle Scholar
  9. 9.
    Treaty on Principles Governing the Activities of States in the Exploration and Use of Outer Space, including the Moon and Other Celestial Bodies. http://disarmament.un.org/treaties/t/outer_space/text. Accessed 13 Jun 2017.
  10. 10.
    Pinna, D. (2014). Biofilms and lichens on stone monuments: Do they damage or protect? Frontiers in Microbiology, 5.  https://doi.org/10.3389/fmicb.2014.00133.
  11. 11.
    Tan, M. S. F., Moore, S. C. Tabor, R. F., et al. (2016). Attachment of Salmonella strains to a plant cell wall model is modulated by surface characteristics and not by specific carbohydrate interactions. BMC Microbiology, 16.  https://doi.org/10.1186/s12866-016-0832-2.
  12. 12.
    Brown, G. S., Betty, R. G., Brockmann, J. E., et al. (2007). Evaluation of vacuum filter sock surface sample collection method for Bacillus spores from porous and non-porous surfaces. Journal of Environmental Monitoring, 9(7), 666–671.  https://doi.org/10.1039/b700163k.CrossRefGoogle Scholar
  13. 13.
    Probst, A., Facius, R., Wirth, R., et al. (2010). Validation of a nylon-flocked-swab protocol for efficient recovery of bacterial spores from smooth and rough surfaces. Applied and Environment Microbiology, 76(15), 5148–5158.  https://doi.org/10.1128/aem.00399-10.CrossRefGoogle Scholar
  14. 14.
    Tang, G., Yip, H.-K., Samaranayake, L. P., et al. (2004). Direct detection of cell surface interactive forces of sessile, fimbriated and non-fimbriated Actinomyces spp. using atomic force microscopy. Archives of Oral Biology, 49(9), 727–738.  https://doi.org/10.1016/j.archoralbio.2004.04.003.CrossRefGoogle Scholar
  15. 15.
    Herman, P., El-Kirat-Chatel, S., Beaussart, A., et al. (2014). The binding force of the staphylococcal adhesin SdrG is remarkably strong. Molecular Microbiology, 93(2), 356–368.  https://doi.org/10.1111/mmi.12663.CrossRefGoogle Scholar
  16. 16.
    Dufrêne, Y. F. (2015). Sticky microbes: Forces in microbial cell adhesion. Trends in Microbiology, 23(6), 376–382.  https://doi.org/10.1016/j.tim.2015.01.011.CrossRefGoogle Scholar
  17. 17.
    Marshall, K. C. (1986). Adsorption and adhesion processes in microbial growth at interfaces. Advances in Colloid and Interface Science, 25(1), 59–86.CrossRefGoogle Scholar
  18. 18.
    Vigeant, M. A.-S., Ford, R. M., Wagner, M., et al. (2002). Reversible and irreversible adhesion of motile escherichia coli cells analyzed by total internal reflection aqueous fluorescence microscopy. Applied and Environment Microbiology, 68(6), 2794–2801.  https://doi.org/10.1128/aem.68.6.2794-2801.2002.CrossRefGoogle Scholar
  19. 19.
    Petrova, O. E., & Sauer, K. (2012). Sticky situations: Key components that control bacterial surface attachment. Journal of Bacteriology, 194(10), 2413–2425.  https://doi.org/10.1128/jb.00003-12.CrossRefGoogle Scholar
  20. 20.
    Hoffman, M. D., Zucker, L. I., Brown, P. J. B., et al. (2015). Timescales and frequencies of reversible and irreversible adhesion events of single bacterial cells. Analytical Chemistry, 87(24), 12032–12039.  https://doi.org/10.1021/acs.analchem.5b02087.CrossRefGoogle Scholar
  21. 21.
    Busscher, H. J., Poortinga, A. T., & Bos, R. (1998). Lateral and perpendicular interaction forces involved in mobile and immobile adhesion of microorganisms on model solid surfaces. Current Microbiology, 37(5), 319–323.CrossRefGoogle Scholar
  22. 22.
    Kennedy, J. F., & Cabral, J. M. S. (1990). Use of titanium species for the immobilization of cells. Transition Metal Chemistry, 15(3), 197–207.  https://doi.org/10.1007/bf01038375.CrossRefGoogle Scholar
  23. 23.
    Bodenmiller, D., Toh, E., & Brun, Y. V. (2004). Development of surface adhesion in Caulobacter crescentus. Journal of Bacteriology, 186(5), 1438–1447.CrossRefGoogle Scholar
  24. 24.
    Gottenbos, B., Busscher, H. J., van der Mei, H. C., et al. (2002). Pathogenesis and prevention of biomaterial centered infections. Journal of Materials Science. Materials in Medicine, 13(8), 717–722.CrossRefGoogle Scholar
  25. 25.
    Donlan, R. M., & Costerton, J. W. (2002). Biofilms: Survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews, 15(2), 167–193.  https://doi.org/10.1128/cmr.15.2.167-193.2002.CrossRefGoogle Scholar
  26. 26.
    Daeschel, M. A., & McGuire, J. (1998). Interrelationships between protein surface adsorption and bacterial adhesion. Biotechnology and Genetic Engineering Reviews, 15(1), 413–438.  https://doi.org/10.1080/02648725.1998.10647964.CrossRefGoogle Scholar
  27. 27.
    Krasowska, A., & Sigler, K. (2014). How microorganisms use hydrophobicity and what does this mean for human needs? Frontiers in Cellular and Infection Microbiology, 4, 112.  https://doi.org/10.3389/fcimb.2014.00112.CrossRefGoogle Scholar
  28. 28.
    Bos, R., van der Mei, H. C., Gold, J., et al. (2000). Retention of bacteria on a substratum surface with micro-patterned hydrophobicity. FEMS Microbiology Letters, 189(2), 311–315.CrossRefGoogle Scholar
  29. 29.
    Ebersbach, G., & Jacobs-Wagner, C. (2007). Exploration into the spatial and temporal mechanisms of bacterial polarity. Trends in Microbiology, 15(3), 101–108.  https://doi.org/10.1016/j.tim.2007.01.004.CrossRefGoogle Scholar
  30. 30.
    Kaiser, D., & Yu, R. (2005). Reversing cell polarity: evidence and hypothesis. Current Opinion in Microbiology, 8(2), 216–221.  https://doi.org/10.1016/j.mib.2005.02.002.CrossRefGoogle Scholar
  31. 31.
    Klemm, P., & Schembri, M. A. (2000). Bacterial adhesins: Function and structure. International Journal of Medical Microbiology, 290(1), 27–35.  https://doi.org/10.1016/s1438-4221(00)80102-2.CrossRefGoogle Scholar
  32. 32.
    Klemm, P., & Schembri, M. A. (2000). Fimbrial surface display systems in bacteria: from vaccines to random libraries. Microbiology, 146(Pt 12), 3025–3032.  https://doi.org/10.1099/00221287-146-12-3025.CrossRefGoogle Scholar
  33. 33.
    Donlan, R. M. (2008). Biofilms on central venous catheters: is eradication possible? Current Topics in Microbiology and Immunology, 322, 133–161.Google Scholar
  34. 34.
    Goller, C. C., & Romeo, T. (2008). Environmental influences on biofilm development. Current Topics in Microbiology and Immunology, 322, 37–66.Google Scholar
  35. 35.
    Davey, M. E., & O’Toole, G. A. (2000). Microbial biofilms: From ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 64(4), 847–867.  https://doi.org/10.1128/mmbr.64.4.847-867.2000.CrossRefGoogle Scholar
  36. 36.
    Costerton, J. (1999). Introduction to biofilm. International Journal of Antimicrobial Agents, 11(3–4), 217–221.  https://doi.org/10.1016/s0924-8579(99)00018-7.CrossRefGoogle Scholar
  37. 37.
    Korber, D. R., Choi, A., Wolfaardt, G. M., et al. (1997). Substratum topography influences susceptibility of Salmonella enteritidis biofilms to trisodium phosphate. Applied and Environment Microbiology, 63(9), 3352–3358.Google Scholar
  38. 38.
    Rasmussen, T. B., & Givskov, M. (2006). Quorum-sensing inhibitors as anti-pathogenic drugs. International Journal of Medical Microbiology, 296(2–3), 149–161.  https://doi.org/10.1016/j.ijmm.2006.02.005.CrossRefGoogle Scholar
  39. 39.
    An, Y. H., & Friedman, R. J. (2010). Handbook of bacterial adhesion: Principles, methods, and applications. Totowa, NJ: Humana Press.Google Scholar
  40. 40.
    Busscher, H. J., & van der Mei, H. C. (2006). Microbial adhesion in flow displacement systems. Clinical Microbiology Reviews, 19(1), 127–141.  https://doi.org/10.1128/cmr.19.1.127-141.2006.CrossRefGoogle Scholar
  41. 41.
    Limoli, D. H, Jones, C. J., Wozniak, D. J. (2015). Bacterial extracellular polysaccharides in biofilm formation and function. Microbiology Spectrum, 3(3).  https://doi.org/10.1128/microbiolspec.mb-0011-2014.
  42. 42.
    Renner, L. D., & Weibel, D. B. (2011). Physicochemical regulation of biofilm formation. MRS Bulletin, 36(5), 347–355.  https://doi.org/10.1557/mrs.2011.65.CrossRefGoogle Scholar
  43. 43.
    Walden, M., Edwards, J. M., Dziewulska, A. M., et al. (2015). An internal thioester in a pathogen surface protein mediates covalent host binding. Elife, 4.  https://doi.org/10.7554/elife.06638.
  44. 44.
    Flint, S., Palmer, J., Bloemen, K., et al. (2001). The growth of Bacillus stearothermophilus on stainless steel. Journal of Applied Microbiology, 90(2), 151–157.  https://doi.org/10.1046/j.1365-2672.2001.01215.x.CrossRefGoogle Scholar
  45. 45.
    Peng, J.-S., Tsai, W.-C., & Chou, C.-C. (2002). Inactivation and removal of Bacillus cereus by sanitizer and detergent. International Journal of Food Microbiology, 77(1–2), 11–18.CrossRefGoogle Scholar
  46. 46.
    Berne, C., Ducret, A., Hardy, G. G., et al. (2015). Adhesins involved in attachment to abiotic surfaces by gram-negative bacteria. Microbiology Spectrum, 3(4).  https://doi.org/10.1128/microbiolspec.mb-0018-2015.
  47. 47.
    Webster, P., Wu, S., Gomez, G., et al. (2006). Distribution of bacterial proteins in biofilms formed by non-typeable Haemophilus influenzae. Journal of Histochemistry and Cytochemistry, 54(7), 829–842.  https://doi.org/10.1369/jhc.6a6922.2006.CrossRefGoogle Scholar
  48. 48.
    Wagner, C., & Hensel, M. (2011). Adhesive mechanisms of Salmonella enterica. Advances in Experimental Medicine and Biology, 715, 17–34.  https://doi.org/10.1007/978-94-007-0940-9_2.CrossRefGoogle Scholar
  49. 49.
    Giltner, C. L., van Schaik, E. J., Audette, G. F., et al. (2006). The Pseudomonas aeruginosa type IV pilin receptor binding domain functions as an adhesin for both biotic and abiotic surfaces. Molecular Microbiology, 59(4), 1083–1096.  https://doi.org/10.1111/j.1365-2958.2005.05002.x.CrossRefGoogle Scholar
  50. 50.
    Pratt, L. A., & Kolter, R. (1998). Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Molecular Microbiology, 30(2), 285–293.CrossRefGoogle Scholar
  51. 51.
    Davey, M. E., Caiazza, N. C., & O’Toole, G. A. (2003). Rhamnolipid surfactant production affects biofilm architecture in Pseudomonas aeruginosa PAO1. Journal of Bacteriology, 185(3), 1027–1036.  https://doi.org/10.1128/jb.185.3.1027-1036.2003.CrossRefGoogle Scholar
  52. 52.
    Kuchma, S. L., & O’Toole, G. A. (2000). Surface-induced and biofilm-induced changes in gene expression. Current Opinion in Biotechnology, 11(5), 429–433.  https://doi.org/10.1016/s0958-1669(00)00123-3.CrossRefGoogle Scholar
  53. 53.
    Isenberg, H. D. (1988). Pathogenicity and virulence: Another view. Clinical Microbiology Reviews, 1(1), 40–53.CrossRefGoogle Scholar
  54. 54.
    Arciola, C. R., Campoccia, D., Ravaioli, S., et al. (2015). Polysaccharide intercellular adhesin in biofilm: Structural and regulatory aspects. Frontiers in Cellular and Infection Microbiology, 5, 7.  https://doi.org/10.3389/fcimb.2015.00007.CrossRefGoogle Scholar
  55. 55.
    Silvestri, E. E., Feldhake, D., Griffin, D., et al. (2016). Optimization of a sample processing protocol for recovery of Bacillus anthracis spores from soil. Journal of Microbiological Methods, 130, 6–13.  https://doi.org/10.1016/j.mimet.2016.08.013.CrossRefGoogle Scholar
  56. 56.
    Silvestri, E. E., Yund, C., Taft, S., et al. (2017). Considerations for estimating microbial environmental data concentrations collected from a field setting. Journal of Exposure Science and Environmental Epidemiology, 27(2), 141–151.  https://doi.org/10.1038/jes.2016.3.CrossRefGoogle Scholar
  57. 57.
    Omidbakhsh, N., Ahmadpour, F., Kenny, N. (2014). How reliable are ATP bioluminescence meters in assessing decontamination of environmental surfaces in healthcare settings? PLoS One, 9(6).  https://doi.org/10.1371/journal.pone.0099951.CrossRefGoogle Scholar
  58. 58.
    ECSS Executive Secretariat ECSS-Q-ST-70-55C.Google Scholar
  59. 59.
    Harry, K., Turner, J., & Madhusudhan, K. (2013). Comparison of physical characteristics and collection and elution performance of clinical swab. African Journal of Microbiology Research, 7(31), 4039–4048.  https://doi.org/10.5897/ajmr.CrossRefGoogle Scholar
  60. 60.
    Dalmaso, G., Bini, M., Paroni, R., et al. (2008). Qualification of high-recovery, flocked swabs as compared to traditional rayon swabs for microbiological environmental monitoring of surfaces. PDA Journal of Pharmaceutical Science and Technology, 62(3), 191–199.Google Scholar
  61. 61.
    Verdon, T. J., Mitchell, R. J., & van Oorschot, R. A. H. (2014). Swabs as DNA collection devices for sampling different biological materials from different substrates. Journal of Forensic Sciences, 59(4), 1080–1089.  https://doi.org/10.1111/1556-4029.12427.CrossRefGoogle Scholar
  62. 62.
    Buttner, M. P., Cruz, P., Stetzenbach, L. D., et al. (2007). Evaluation of two surface sampling methods for detection of Erwinia herbicola on a variety of materials by culture and quantitative PCR. Applied and Environment Microbiology, 73(11), 3505–3510.  https://doi.org/10.1128/aem.01825-06.CrossRefGoogle Scholar
  63. 63.
    Moore, G., & Griffith, C. (2007). Problems associated with traditional hygiene swabbing: the need for in-house standardization. Journal of Applied Microbiology, 103(4), 1090–1103.  https://doi.org/10.1111/j.1365-2672.2007.03330.x.CrossRefGoogle Scholar
  64. 64.
    Rose, L. J., Hodges, L., O’Connell, H., et al. (2011). National validation study of a cellulose sponge wipe-processing method for use after sampling Bacillus anthracis spores from surfaces. Applied and Environment Microbiology, 77(23), 8355–8359.  https://doi.org/10.1128/aem.05377-11.CrossRefGoogle Scholar
  65. 65.
    Sanderson, W. T., Hein, M. J., Taylor, L., et al. (2002). Surface Sampling methods for Bacillus anthracis spore contamination. Emerging Infectious Disease Journal, 8(10), 1145.  https://doi.org/10.3201/eid0810.020382.CrossRefGoogle Scholar
  66. 66.
    Stam, C., Behar, A., Cooper, M. (2016). Sampling of microbiological samples. In: M. Micic(Ed) Sample preparation techniques for soil, plant, and animal samples (1st ed., pp. 25–39). New York, NY: Humana Press.Google Scholar
  67. 67.
    Valentine, N. B., Butcher, M. G., Su, Y.-F., et al. (2008). Evaluation of sampling tools for environmental sampling of bacterial endospores from porous and nonporous surfaces. Journal of Applied Microbiology, 105(4), 1107–1113.  https://doi.org/10.1111/j.1365-2672.2008.03840.x.CrossRefGoogle Scholar
  68. 68.
    Lewandowski, R., Kozlowska, K., Szpakowska, M., et al. (2010). Use of a foam spatula for sampling surfaces after bioaerosol deposition. Applied and Environment Microbiology, 76(3), 688–694.  https://doi.org/10.1128/aem.01849-09.CrossRefGoogle Scholar
  69. 69.
    Probst, A., Facius, R., Wirth, R., et al. (2011). Recovery of bacillus spore contaminants from rough surfaces: A challenge to space mission cleanliness control. Applied and Environment Microbiology, 77(5), 1628–1637.  https://doi.org/10.1128/aem.02037-10.CrossRefGoogle Scholar
  70. 70.
    Rossi, E. M., Scapin, D., & Tondo, E. C. (2013). Survival and transfer of microorganisms from kitchen sponges to surfaces of stainless steel and polyethylene. The Journal of Infection in Developing Countries, 7(3), 229–234.  https://doi.org/10.3855/jidc.2472.CrossRefGoogle Scholar
  71. 71.
    Verdon, T. J., Mitchell, R. J., & van Oorschot, R. A. H. (2014). Evaluation of tapelifting as a collection method for touch DNA. Forensic Science International: Genetics, 8(1), 179–186.  https://doi.org/10.1016/j.fsigen.2013.09.005.CrossRefGoogle Scholar
  72. 72.
    Ibfelt, T., Foged, C., & Andersen, L. P. (2014). Validation of dipslides as a tool for environmental sampling in a real-life hospital setting. European Journal of Clinical Microbiology and Infectious Diseases, 33(5), 809–813.  https://doi.org/10.1007/s10096-013-2018-2.CrossRefGoogle Scholar
  73. 73.
    Obee, P., Griffith, C. J., Cooper, R. A., et al. (2007). An evaluation of different methods for the recovery of meticillin-resistant Staphylococcus aureus from environmental surfaces. Journal of Hospital Infection, 65(1), 35–41.  https://doi.org/10.1016/j.jhin.2006.09.010.CrossRefGoogle Scholar
  74. 74.
    Lutz, J. K., Crawford, J., Hoet, A. E., et al. (2013). Comparative performance of contact plates, electrostatic wipes, swabs and a novel sampling device for the detection of Staphylococcus aureus on environmental surfaces. Journal of Applied Microbiology, 115(1), 171–178.  https://doi.org/10.1111/jam.12230.CrossRefGoogle Scholar
  75. 75.
    Niemeier, R. T., Sivasubramani, S. K., Reponen, T., et al. (2006). Assessment of fungal contamination in moldy homes: comparison of different methods. Journal of Occupational and Environmental Hygiene, 3(5), 262–273.  https://doi.org/10.1080/15459620600637333.CrossRefGoogle Scholar
  76. 76.
    Dillon, H. K., Miller, J. D., Sorenson, W. G., et al. (1999). Review of methods applicable to the assessment of mold exposure to children. Environmental Health Perspectives, 107(Suppl 3), 473–480.CrossRefGoogle Scholar
  77. 77.
    Tittlemier, S. A., Varga, E., Scott, P. M., et al. (2011). Sampling of cereals and cereal-based foods for the determination of ochratoxin A: An overview. Food Additives and Contaminants: Part A: Chemistry, Analysis, Control, Exposure & Risk Assessment, 28(6), 775–785.  https://doi.org/10.1080/19440049.2011.559278.CrossRefGoogle Scholar
  78. 78.
    Wuest, S. B. (2009). Correction of bulk density and sampling method biases using soil mass per unit area. Soil Science Society of America Journal, 73(1), 312.  https://doi.org/10.2136/sssaj2008.0063.CrossRefGoogle Scholar
  79. 79.
    Pearce, R. A., & Bolton, D. J. (2005). Excision vs sponge swabbing—A comparison of methods for the microbiological sampling of beef, pork and lamb carcasses. Journal of Applied Microbiology, 98(4), 896–900.  https://doi.org/10.1111/j.1365-2672.2004.02525.x.CrossRefGoogle Scholar
  80. 80.
    Lindblad, M. (2007). Microbiological sampling of swine carcasses: a comparison of data obtained by swabbing with medical gauze and data collected routinely by excision at Swedish abattoirs. International Journal of Food Microbiology, 118(2), 180–185.  https://doi.org/10.1016/j.ijfoodmicro.2007.07.009.CrossRefGoogle Scholar
  81. 81.
    Packard, B. H., & Kupferle, M. J. (2010). Evaluation of surface sampling techniques for collection of Bacillus spores on common drinking water pipe materials. Journal of Environmental Monitoring, 12(1), 361–368.  https://doi.org/10.1039/b917570a.CrossRefGoogle Scholar
  82. 82.
    Drago, L., Romanò, C. L., Mattina, R., et al. (2012). Does dithiothreitol improve bacterial detection from infected prostheses? A pilot study. Clinical Orthopaedics and Related Research, 470(10), 2915–2925.  https://doi.org/10.1007/s11999-012-2415-3.CrossRefGoogle Scholar
  83. 83.
    Bjerkan, G., Witsø, E., & Bergh, K. (2009). Sonication is superior to scraping for retrieval of bacteria in biofilm on titanium and steel surfaces in vitro. Acta Orthopaedica, 80(2), 245–250.  https://doi.org/10.3109/17453670902947457.CrossRefGoogle Scholar
  84. 84.
    Whitfield, W. J., Beakley, J. W., Dugan, V. L., et al. (1969). Vacuum probe: New approach to the microbiological sampling of surfaces. Applied Microbiology, 17(1), 164–168.Google Scholar
  85. 85.
    Edmonds, J. M., Sabol, J. P., & Rastogi, V. K. (2014). Decontamination efficacy of three commercial-off-the-shelf (COTS) sporicidal disinfectants on medium-sized panels contaminated with surrogate spores of Bacillus anthracis. PLoS ONE, 9(6), e99827.  https://doi.org/10.1371/journal.pone.0099827.CrossRefGoogle Scholar
  86. 86.
    Calfee, M. W., Rose, L. J., Morse, S., et al. (2013). Comparative evaluation of vacuum-based surface sampling methods for collection of Bacillus spores. Journal of Microbiol Methods, 95(3), 389–396.  https://doi.org/10.1016/j.mimet.2013.10.015.CrossRefGoogle Scholar
  87. 87.
    Lee, S. D., Calfee, M. W., Mickelsen, L., et al. (2013). Evaluation of surface sampling for Bacillus spores using commercially available cleaning robots. Environmental Science and Technology, 47(6), 2595–2601.  https://doi.org/10.1021/es4000356.CrossRefGoogle Scholar
  88. 88.
    U.S. Food and drug Administration. (1993). Validation of cleaning processes (7/93): Guide to inspections validation of cleaning processes. https://www.fda.gov/iceci/inspections/inspectionguides/ucm074922.htm.
  89. 89.
    Blankenship, L. C., Cox, N. A., Craven, S. E., et al. (1975). Total rinse method for microbiological sampling of the internal cavity of eviscerated broiler carcasses. Applied Microbiology, 30(2), 290–292.Google Scholar
  90. 90.
    Sarlin, L. L., Barnhart, E. T., Caldwell, D. J., et al. (1998). Evaluation of alternative sampling methods for Salmonella critical control point determination at broiler processing. Poultry Science, 77(8), 1253–1257.CrossRefGoogle Scholar
  91. 91.
    Fletcher, D. L., Russell, S. M., Walker, J. M., et al. (1993). An evaluation of a rinse procedure using sodium bicarbonate and hydrogen peroxide on the recovery of bacteria from broiler carcasses. Poultry Science, 72(11), 2152–2156.CrossRefGoogle Scholar
  92. 92.
    Zhang, Q., Qini, U., Ye, K., et al. (2012). Comparison of excision, swabbing and rinsing sampling methods to determine the microbiological quality of broiler carcasses. Journal of Food Safety, 32(1), 134–139.  https://doi.org/10.1111/j.1745-4565.2011.00360.x.CrossRefGoogle Scholar
  93. 93.
    Ashokkumar, M. (2016). Handbook of ultrasonics and sonochemistry. Singapore: Springer Science + Business Media.Google Scholar
  94. 94.
    Sanglay, G. C., Eifert, J. D., & Sumner, S. S. (2004). Recovery of Salmonella spp. from raw produce surfaces using ultrasonication. Foodborne Pathogens Diseases, 1(4), 295–299.  https://doi.org/10.1089/fpd.2004.1.295.CrossRefGoogle Scholar
  95. 95.
    Seymour, I. J., Burfoot, D., Smith, R. L., et al. (2002). Ultrasound decontamination of minimally processed fruits and vegetables. International Journal of Food Science & Technology, 37(5), 547–557.  https://doi.org/10.1046/j.1365-2621.2002.00613.x.CrossRefGoogle Scholar
  96. 96.
    Kang, D., Eifert, J. D., Williams, R. C., et al. (2007). Evaluation of quantitative recovery methods for Listeria monocytogenes applied to stainless steel. Journal of AOAC International, 90(3), 810–816.Google Scholar
  97. 97.
    Oulahal-Lagsir, N., Martial-Gros, A., Boistier, E., et al. (2000). The development of an ultrasonic apparatus for the noninvasive and repeatable removal of fouling in food processing equipment. Letters in Applied Microbiology, 30(1), 47–52.CrossRefGoogle Scholar
  98. 98.
    McDonald, W. S., & Nichter, L. S. (1994). Debridement of bacterial and particulate-contaminated wounds. Annals of Plastic Surgery, 33(2), 142–147.CrossRefGoogle Scholar
  99. 99.
    Nishikawa, T., Yoshida, A., Khanal, A., et al. (2010). A study of the efficacy of ultrasonic waves in removing biofilms. Gerodontology, 27(3), 199–206.  https://doi.org/10.1111/j.1741-2358.2009.00325.x.CrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Ilya Digel
    • 1
  • Nuraly Sh. Akimbekov
    • 2
  • Aida Kistaubayeva
    • 2
  • Azhar A. Zhubanova
    • 2
  1. 1.Institute for BioengineeringUniversity of Applied Sciences AachenCampus JülichGermany
  2. 2.Al-Farabi Kazakh National UniversityAlmatyKazakhstan

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