Detection and quantification of bacterial biofilms combining high-frequency acoustic microscopy and targeted lipid microparticles

Journal of Nanobiotechnology

Volumn 12, Issue 1, 2014, Pages

  Anastasiadis, Pavlos ^a,b,c   Mojica, Kristina D A ^d,e   Allen, John S ^c   Matter, Michelle L ^a  

^a UNIVERSITY OF HAWAII CANCER CENTER   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c University of Hawaii at Manoa   (United States)

^d UNIVERSITY OF HAWAII   (United States)

^e ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

Acoustic microscopy; Biofilm matrix; Cancer; Lipid particles; Microbubbles; Molecular imaging; Targeted therapy; Targeted ultrasound contrast agents

Indexed keywords

ACOUSTIC IMPEDANCE; ACOUSTIC MICROSCOPES; ACOUSTIC VARIABLES MEASUREMENT; BACTERIA; CHEMOTHERAPY; DISEASES; ENZYME INHIBITION; IMAGING TECHNIQUES; MOLECULAR IMAGING; TISSUE; ULTRASONIC APPLICATIONS; DIAGNOSIS; HISTOLOGY;

ACOUSTIC MICROSCOPY; BIOFILM MATRIX; CANCER; LIPID PARTICLES; MICROBUBBLES; TARGETED THERAPY; ULTRASOUND CONTRAST AGENT;

BIOFILMS;

ECHO CONTRAST MEDIUM; LIGAND; LIPID; CONTRAST MEDIUM;

ACOUSTIC IMPEDANCE; ACOUSTIC MICROSCOPY; ARTICLE; BACTERIAL CELL; BIOFILM; EPIFLUORESCENCE MICROSCOPY; HUMAN; IMMUNOFLUORESCENCE; IN VITRO STUDY; MOLECULAR IMAGING; NONHUMAN; STAPHYLOCOCCUS AUREUS; BACTERIUM DETECTION; CONTROLLED STUDY; DONKEY; MICROBIAL BIOMASS; MICROSCOPY; CHEMISTRY; DEVICES; FLUORESCENCE MICROSCOPY; ISOLATION AND PURIFICATION; METABOLISM; MICROBUBBLE; PROCEDURES;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

BIOFILMS; CONTRAST MEDIA; LIPIDS; MICROBUBBLES; MICROSCOPY, ACOUSTIC; MICROSCOPY, FLUORESCENCE; MOLECULAR IMAGING; STAPHYLOCOCCUS AUREUS;

EID: 84905560525     PISSN: None     EISSN: 14773155     Source Type: Journal    
DOI: 10.1186/1477-3155-12-24     Document Type: Article

References (77)

1. Liu D, Lau YL, Chau YK, Pacepavicius G. Simple technique for estimation of biofilm accumulation. Bull Environ Contam Toxicol 1994, 53(6):913-918.
2. Allison DG, Ruiz B, SanJose C, Jaspe A, Gilbert P. Extracellular products as mediators of the formation and detachment of Pseudomonas fluorescens biofilms. Fems Microbiol Letters 1998, 167(2):179-184.
3. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999, 284(5418):1318-1322.
4. Wingender J, Neu TR, Flemming HC. What are Bacterial Extracellular Substances?. Microbial Extracellular Polymeric Substances: Characterization, Structure and Function 1999, 1-19. Berlin: Springer, Wingender J, Neu TR, Flemming HC, 1.
5. Strathmann M, Wingender J, Flemming HC. Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of pseudomonas aeruginosa. J Microbiol Methods 2002, 50(3):237-248.
6. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004, 2(2):95-108.
7. Davey ME, GA O. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 2000, 64(4):847-867.
8. Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010, 8(9):623-633.
9. Lambe DW, Ferguson KP, Mayberry-Carson KJ, Tober-Meyer B, Costerton JW. Foreign-body-associated experimental osteomyelitis induced with bacteroides fragilis and staphylococcus epidermidis in rabbits. Clin Orthop Relat Res 1991, 266:285-294.
10. Harris LG, Richards RG. Staphylococci and implant surfaces: a review. Injury-Int J Care Injured 2006, 37:3-14.
11. Baldassarri L, Montanaro L, Creti R, Arciola CR. Underestimated collateral effects of antibiotic therapy in prosthesis-associated bacterial infections. Int J Artif Organs 2007, 30:786-791.
12. Kaplan JB. Methods for the treatment and opinion prevention of bacterial biofilms. Expert Opinion Therap Patents 2005, 15(8):955-965.
13. Sullam PM, Drake TA, Sande MA. Pathogenesis of endocarditis. Am J Med 1985, 78(6B):110-115.
14. Caldwell DA, Lovasik D. Endocarditis in the immunocompromised. Am J Nurs 2002, (Suppl):32-36.
15. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002, 15(2):167-193.
16. Petti CA, Fowler VG. Staphylococcus aureus bacteremia and endocarditis. Cardiol Clin 2003, 21(2):219-233. vii.
17. Nickel JC, Wright JB, Ruseska I, Marrie TJ, Whitfield C, Costerton JW. Antibiotic-resistance of pseudomonas-aeruginosa colonizing a urinary catheter invitro. Eur J Clin Microbiol Infect Dis 1985, 4(2):213-218.
18. Allison DG, Gilbert P. Modification by surface association of antimicrobial susceptibility of bacterial-populations. J Ind Microbiol 1995, 15(4):311-317.
19. Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet 2001, 358(9276):135-138.
20. Parsek MR, Singh PK. Bacterial biofilms: an emerging link to disease pathogenesis. Annu Rev Microbiol 2003, 57:677-701.
21. Furuya EY, Lowy FD. Antimicrobial strategies for the prevention and treatment of cardiovascular infections. Curr Opin Pharmacol 2003, 3(5):464-469.
22. Durack DT, Lukes AS, Bright DK, Alberts MJ, Bashore TM, Corey GR, Douglas JM, Gray L, Harrell FE, Harrison JK, Heinle SA, Morris A, Kisslo JA, Nicely LM, Oldham N, Penning LM, Sexton DJ, Towns M, Waugh RA. New criteria for diagnosis of infective endocarditis - utilization of specific echocardiographic findings. Am J Med 1994, 96(3):200-209.
23. Baddour LM, Bettmann MA, Bolger AF, Epstein AE, Ferrieri P, Gerber MA, Gewitz MH, Jacobs AK, Levison ME, Newburger JW, Pallasch TJ, Wilson WR, Baltimore RS, Falace DA, Shulman ST, Tani LY, Taubert KA. Infective endocarditis: diagnosis, antimicrobial therapy, and management of complications. Circulation 2005, 112(15):2373.
24. Shemesh H, Goertz DE, van der Sluis LW, de Jong N, Wu MK, Wesselink PR. High frequency ultrasound imaging of a single-species biofilm. J Dent 2007, 35(8):673-678.
25. Vaidya K, Osgood R, Ren D, Pichichero ME, Helguera M. Ultrasound imaging and characterization of biofilms based on wavelet de-noised radiofrequency data. Ultrasound Med Biol 2014, 40(3):583-595.
26. Good MS, Wend CF, Bond LJ, McLean JS, Panetta PD, Ahmed S, Crawford SL, Daly DS. An estimate of biofilm properties using an acoustic microscope. IEEE Trans Ultrason Ferroelectr Freq Control 2006, 53(9):1637-1646.
27. Holmes AK, Laybourn-Parry J, Parry JD, Unwin ME, Challis RE. Ultrasonic imaging of biofilms utilizing echoes from the biofilm/air interface. IEEE Trans Ultrason Ferroelectr Freq Control 2006, 53(1):185-192.
28. Kujundzic E, Fonseca AC, Evans EA, Peterson M, Greenberg AR, Hernandez M. Ultrasonic monitoring of early-stage biofilm growth on polymeric surfaces. J Microbiol Methods 2007, 68(3):458-467.
29. Sbeity F, Menigot S, Charara J, Girault JM. Contrast improvement in sub- and ultraharmonic ultrasound contrast imaging by combining several hammerstein models. Int J Biomed Imag 2013, 2013:270523.
30. Anderson CR, Hu X, Zhang H, Tlaxca J, Decleves A-E, Houghtaling R, Sharma K, Lawrence M, Ferrara KW, Rychak JJ. Ultrasound molecular imaging of tumor angiogenesis with an integrin targeted microbubble contrast agent. Investig Radiol 2011, 46(4):215-224.
31. Klibanov AL. Microbubble contrast agents - targeted ultrasound imaging and ultrasound-assisted drug-delivery applications. Investig Radiol 2006, 41(3):354-362.
32. Klibanov AL. Ultrasound molecular imaging with targeted microbubble contrast agents. J Nucl Cardiol 2007, 14(6):876-884.
33. Klibanov AL. Preparation of targeted microbubbles: ultrasound contrast agents for molecular imaging. Med Biol Eng Comput 2009, 47(8):875-882.
34. Klibanov AL, Hughes MS, Villanueva FS, Jankowski RJ, Wagner WR, Wojdyla JK, Wible JH, Brandenburger GH. Targeting and ultrasound imaging of microbubble-based contrast agents. Magnet Reson Mat Biol Physics Med 1999, 8(3):177-184.
35. Unnikrishnan S, Klibanov AL. Microbubbles as ultrasound contrast agents for molecular imaging: preparation and application. Am J Roentgenol 2012, 199(2):292-299.
36. Weiss EC, Anastasiadis P, Pilarczyk G, Lernor RM, Zinin PV. Mechanical properties of single cells by high-frequency time-resolved acoustic microscopy. Ultrason Ferroelectr Frequen Contr IEEE Trans 2007, 54(11):2257-2271.
37. Weiss EC, Lemor RM, Pilarczyk G, Anastasiadis P, Zinin PV. Imaging of focal contacts of chicken heart muscle cells by high-frequency acoustic microscopy. Ultrasound Med Biol 2007, 33(8):1320-1326.
38. Zinin PV, Allen JS. Deformation of biological cells in the acoustic field of an oscillating bubble. Phys Rev E 2009, 79(2 Pt 1):021910.
39. Zinin PV, Allen JS, Levin VM. Mechanical resonances of bacteria cells. Phys Rev E Stat Nonlin Soft Matter Phys 2005, 72(6 Pt 1):061907.
40. Moran CM, Watson RJ, Fox KAA, McDicken WN. In vitro acoustic characterisation of four intravenous ultrasonic contrast agents at 30 MHz. Ultrasound Med Biol 2002, 28(6):785-791.
41. Inglis TJ. Evidence for dynamic phenomena in residual tracheal tube biofilm. Br J Anaesth 1993, 70(1):22-24.
42. Goldstein IJ, Hayes CE. The lectins: carbohydrate-binding proteins of plants and animals. Adv Carbohydr Chem Biochem 1978, 35:127-340.
43. Archibald LK, Gaynes RP. Hospital-acquired infections in the United States. The importance of interhospital comparisons. Infect Dis Clin North Am 1997, 11(2):245-255.
44. Azzopardi EA, Ferguson EL, Thomas DW. The enhanced permeability retention effect: a new paradigm for drug targeting in infection. J Antimicrob Chemother 2013, 68(2):257-274.
45. Inglis TJJ, Titmeng L, Mahlee N, Eekoon T, Kokpheng H. Structural features of tracheal tube biofilm formed during prolonged mechanical ventilation. Chest 1995, 108(4):1049-1052.
46. Al Akhrass F, Al Wohoush I, Chaftari AM, Reitzel R, Jiang Y, Ghannoum M, Tarrand J, Hachem R, Raad I. Rhodococcus bacteremia in cancer patients is mostly catheter related and associated with biofilm formation. Plos ONE 2012, 7(3):e32945.
47. Hejsek L, Pasta J. Ultrasonographic biomicroscopy of the eye. Ultrazvukova? Biomikroskopie oka 2005, 61(4):273-280.
48. Liang HD, Blomley MJK. The role of ultrasound in molecular imaging. Br J Radiol 2003, 76(suppl_2):S140-S150.
49. Silverman RH. High-resolution ultrasound imaging of the eye - a review. Clinical Exper Ophthalmol 2009, 37(1):54-67.
50. Silverman RH, Cannata J, Shung KK, Gal O, Patel M, Lloyd HO, Feleppa EJ, Coleman DJ. 75 MHz ultrasound biomicroscopy of anterior segment of eye. Ultrason Imaging 2006, 28(3):179-188.
51. Snetkova YV, Levin VM, Petriniuk YS, Denisov AF, Bogachenkov AN, Denisova LA, Khramtzova YA. Application of the method of acoustic microscopy for the study of eye tissues. Morfologiya 2005, 127(2):72-75.
52. Goertz DE, Frijlink ME, De Jong N, Steen A. Nonlinear intravascular ultrasound contrast imaging. Ultrasound Med Biol 2006, 32(4):491-502.
53. Goertz DE, Frijlink ME, Tempel D, Bhagwandas V, Gisolf A, Krams R, de Jong N, van der Steen AFW. Subharmonic contrast intravascular ultrasound for vasa vasorum imaging. Ultrasound Med Biol 2007, 33(12):1859-1872.
54. Phillips LC, Klibanov AL, Wamhoff BR, Hossack JA. Intravascular ultrasound detection and delivery of molecularly targeted microbubbles for gene delivery. IEEE Trans Ultrason Ferroelectr Freq Control 2012, 59(7):1596-1601.
55. Witkin AJ, Fischer DH, Shields CL, Reichstein D, Shields JA. Enhanced depth imaging spectral-domain optical coherence tomography of a subtle choroidal metastasis. Eye 2012, 26(12):1598-1599.
56. Knspik DA, Starkoski B, Pavlin CJ, Foster FS. A 100-200 MHz ultrasound biomicroscope. IEEE Trans Ultrason Ferroelectr Freq Control 2000, 47(6):1540-1549.
57. Liu Y, Miyoshi H, Nakamura M. Encapsulated ultrasound microbubbles: therapeutic application in drug/gene delivery. J Control Release 2006, 114(1):89-99.
58. Saijo Y, Sasaki H, Okawai H, Nitta S-I, Tanaka M. Acoustic properties of atherosclerosis of human aorta obtained with high-frequency ultrasound. Ultrasound Med Biol 1998, 24(7):1061-1064.
59. Saijo Y, Jorgensen CS, Falk E. Ultrasonic tissue characterization of collagen in lipid-rich plaques in apoE-deficient mice. Atherosclerosis 2001, 158(2):289-295.
60. Saijo Y, Santos E, Sasaki H, Yambe T, Tanaka M, Hozumi N, Kobayashi K, Okada N. Ultrasonic tissue characterization of atherosclerosis by a speed-of-sound microscanning system. IEEE Trans Ultrason Ferroelectr Frequen Contr 2007, 54(8):1571-1577.
61. Saijo Y, Miyakawa T, Sasaki H, Tanaka M, Nitta SI. Acoustic properties of aortic aneurysm obtained with scanning acoustic microscopy. Ultrasonics 2004, 42(1-9):695-698.
62. Brand S, Solanki B, Foster DB, Czarnota GJ, Kolios MC. Monitoring of cell death in epithelial cells using high frequency ultrasound spectroscopy. Ultrasound Med Biol 2009, 35(3):482-493.
63. Brand S, Weiss EC, Lemor RM, Kolios MC. High frequency ultrasound tissue characterization and acoustic microscopy of intracellular changes. Ultrasound Med Biol 2008, 34(9):1396-1407.
64. Strohm EM, Czarnota GJ, Kolios MC. Quantitative measurements of apoptotic cell properties using acoustic microscopy. IEEE Transactions Ultrason Ferroelectr Frequen Contr 2010, 57(10):2293-2304.
65. Baddour RE, Sherar MD, Hunt JW, Czarnota GJ, Kolios MC. High-frequency ultrasound scattering from microspheres and single cells. J Acoust Soc Am 2005, 117(2):934-943.
66. Saijo Y, Tanaka M, Okawai H, Sasaki H, Nitta SI, Dunn F. Ultrasonic tissue characterization of infarcted myocardium by scanning acoustic microscopy. Ultrasound Med Biol 1997, 23(1):77-85.
67. Baddour LM, Bettmann MA, Bolger AF, Epstein AE, Ferrieri P, Gerber MA, Gewitz MH, Jacobs AK, Levison ME, Newburger JW, Pallasch TJ, Wilson WR, Baltimore RS, Falace DA, Shulman ST, Tani LY, Taubert KA. Nonvalvular cardiovascular device-related infections. Circulation 2003, 108(16):2015-2031.
68. DeDent AC, McAdow M, Schneewind O. Distribution of protein A on the surface of staphylococcus aureus. J Bacteriol 2007, 189(12):4473-4484.
69. Schneewind O, Fowler A, Faull KF. Structure of the cell wall anchor of surface proteins in staphylococcus aureus. Science 1995, 268(5207):103-106.
70. Oelze ML, O'Brien WD. Improved scatterer property estimates from ultrasound backscatter for small gate lengths using a gate-edge correction factor. J Acoust Soc Am 2004, 116(5):3212-3223.
71. Briggs A. Advances in Acoustic Microscopy 1995, New York: Plenum Press.
72. Briggs A, Kolosov O. Acoustic Microscopy 2010, New York: Clarendon.
73. Briggs GAD, Rowe JM, Sinton AM, Spencer DS. Quantitative Methods in Acoustic Microscopy. Ultrasonics Symposium Proceedings: 1988 1988, 743-749. Chicago, IL, USA: Publ by IEEE.
74. Briggs GAD, Wang J, Gundle R. Quantitative acoustic microscopy of individual living human cells. J Microsc 1993, 172(Pt1):3-12.
75. Martin G, Carroll ET. Tables of the speed of sound in water. J Acoustic Soc Am 1959, 31(1):75-76.
76. Greenspan M, Tschiegg CE. Tables of the speed of sound in water. J Acoustic Soc Am 1959, 31(1):75-76.
77. Akashi N, Kushibiki J, Dunn F. Acoustic properties of egg yolk and albumen range 20-400 MHz. J Acoust Soc Am 1997, 102(6):3774-3778.