Methods for in vitro evaluating antimicrobial activity: A review

Journal of Pharmaceutical Analysis

Volumn 6, Issue 2, 2016, Pages 71-79

  Balouiri, Mounyr ^a   Sadiki, Moulay ^a   Ibnsouda, Saad Koraichi ^a  

^a SIDI MOHAMED BEN ABDELLAH UNIVERSITY   (Morocco)

Author keywords

Agar diffusion method; Antimicrobial gradient method; Thin layer chromatography (TLC) bioautography; Time kill test

Indexed keywords

ADENOSINE TRIPHOSPHATE; AGAR; AMINOGLYCOSIDE; ANTIBIOTIC AGENT; ANTIFUNGAL AGENT; ANTIINFECTIVE AGENT; ANTIMYCOBACTERIAL AGENT; CEPHALOSPORIN DERIVATIVE; ESSENTIAL OIL; MACROLIDE; PLANT EXTRACT; TETRACYCLINE DERIVATIVE;

AGAR DIFFUSION; AGAR DILUTION; AGAR MEDIUM; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOASSAY; BIOLUMINESCENCE; BROTH DILUTION; CELL DAMAGE; CELL VIABILITY; CULTURE MEDIUM; CYTOFLUOROMETRY; DISK DIFFUSION; DRUG SCREENING; FLOW CYTOMETRY; HUMAN; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PETRI DISH; THIN LAYER CHROMATOGRAPHY;

EID: 84954287070     PISSN: 20951779     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jpha.2015.11.005     Document Type: Review

References (101)

1. D.L. Mayers, S.A. Lerner, M. Ouelette, and et al. Antimicrobial Drug Resistance C: Clinical and Epidemiological Aspects vol. 2 2009 Springer Dordrecht Heidelberg London pp. 681-1347
2. A. Guschin, P. Ryzhikh, T. Rumyantseva, and et al. Treatment efficacy, treatment failures and selection of macrolide resistance in patients with high load of Mycoplasma genitalium during treatment of male urethritis with Josamycin BMC Infect. Dis. 15 2015 1 7
3. I. Martin, P. Sawatzky, G. Liu, and et al. Antimicrobial resistance to Neisseria gonorrhoeae in Canada: 2009-2013 Can. Commun. Dis. Rep. 41 2015 40 41
4. J. Berdy Bioactive microbial metabolites J. Antibiot. 58 2005 1 26
5. D.K. Runyoro, M.I. Matee, O.D. Ngassapa, and et al. Screening of Tanzanian medicinal plants for anti-Candida activity BMC Complement. Altern. Med. 6 2006 11
6. U. Mabona, A. Viljoen, E. Shikanga, and et al. Antimicrobial activity of Southern African medicinal plants with dermatological relevance: from an ethnopharmacological screening approach, to combination studies and the isolation of a bioactive compound J. Ethnopharmacol. 148 2013 45 55
7. F. Nazzaro, F. Fratianni, L. De Martino, and et al. Effect of essential oils on pathogenic bacteria Pharmaceuticals 6 2013 1451 1474
8. N.G. Heatley A method for the assay of penicillin Biochem. J. 38 1944 61 65
9. CLSI, Performance Standards for Antimicrobial Disk Susceptibility Tests, Approved Standard, 7th ed., CLSI document M02-A11. Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087, USA, 2012.
10. CLSI, Method for Antifungal Disk Diffusion Susceptibility Testing of Yeasts, Approved Guideline. CLSI document M44-A. CLSI, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898, USA, 2004.
11. J.H. Jorgensen, and M.J. Ferraro Antimicrobial susceptibility testing: a review of general principles and contemporary practices Clin. Infect. Dis. 49 2009 1749 1755
12. F. Caron Antimicrobial susceptibility testing: a four facets tool for the clinician J. Des. Anti-Infect. 14 2012 186-174
13. A. Nijs, R. Cartuyvels, A. Mewis, and et al. Comparison and evaluation of Osiris and Sirscan 2000 antimicrobial susceptibility systems in the clinical microbiology laboratory J. Clin. Microbiol. 41 2003 3627 3630
14. B.E. Kreger, D.E. Craven, and W.R. McCabe Gram-negative bacteremia. IV. Re-evaluation of clinical features and treatment in 612 patients Am. J. Med. 68 1980 344 355
15. E. Lopez-Oviedo, A.I. Aller, C. Martín, and et al. Evaluation of disk diffusion method for determining posaconazole susceptibility of filamentous fungi: comparison with CLSI broth microdilution method Antimicrob. Agents Chemother. 50 2006 1108 1111
16. S. Arikan, P. Yurdakul, and G. Hascelik Comparison of two methods and three end points in determination of in vitro activity of Micafungin against Aspergillus spp Antimicrob. Agents Chemother. 47 2003 2640 2643
17. S. Arikan, V. Paetznick, and J.H. Rex Comparative evaluation of disk diffusion with microdilution assay in susceptibility testing of caspofungin against Aspergillus and Fusarium isolates Antimicrob. Agents Chemother. 46 2002 3084 3087
18. CLSI, Method for Antifungal Disk Diffusion Susceptibility Testing of Nondermatophyte Filamentous Fungi, Approved guideline, CLSI document M51-A. Clincal and Laboratory Standards Institute, 950 West Valley Roead, Suite 2500, Wayne, Pennsylvania 19087, USA, 2010.
19. A. Espinel-Ingroff, E. Canton, A. Fothergill, and et al. Quality control guidelines for amphotericin B, itraconazole, posaconazole, and Voriconazole disk diffusion susceptibility tests with nonsupplemented Mueller-Hinton Agar (CLSI M51-A document) for nondermatophyte Filamentous Fungi J. Clin. Microbiol. 49 2011 2568 2571
20. L. Fourati-Ben Fguira, S. Fotso, R. Ben Ameur-Mehdi, and et al. Purification and structure elucidation of antifungal and antibacterial activities of newly isolated Streptomyces sp. strain US80 Res. Microbiol. 156 2005 341 347
21. K. Konaté, J.F. Mavoungou, A.N. Lepengué, and et al. Antibacterial activity against β-lactamase producing Methicillin and Ampicillin-resistants Staphylococcus aureus: Fractional Inhibitory Concentration Index (FICI) determination Ann. Clin. Microbiol. Antimicrob. 11 2012 18
22. V.G. De Billerbeck Huiles Essentielles et Bactéries Résistantes aux Antibiotiques Phytotherapie 5 2007 249 253
23. K. Das, R.K.S. Tiwari, and D.K. Shrivastava Techniques for evaluation of medicinal plant products as antimicrobial agents: current methods and future trends J. Med. Plants Res. 4 2010 104 111
24. J. Hausdorfer, E. Sompek, F. Allerberger, and et al. E-test for susceptibility testing of Mycobacterium tuberculosis Int. J. Tuberc. Lung Dis. 2 1998 751 755
25. C.N. Baker, S.A. Stocker, D.H. Culver, and et al. Comparison of the E Test to agar dilution, broth microdilution, and agar diffusion susceptibility testing techniques by using a special challenge set of bacteria J. Clin. Microbiol. 29 1991 533 538
26. L.J. Berghaus, S. Giguère, K. Guldbech, and et al. Comparison of Etest, disk diffusion, and broth macrodilution for in vitro susceptibility testing of Rhodococcus equi J. Clin. Microbiol. 53 2015 314 318
27. P. Gupta, V. Khare, D. Kumar, and et al. Comparative evaluation of disc diffusion and E-test with broth micro-dilution in susceptibility testing of amphotericin B, voriconazole and caspofungin against clinical Aspergillus isolates J. Clin. Diagn. Res. 9 2015 2013 2016
28. R.L. White, D.S. Burgess, M. Manduru, and et al. Comparison of three different in vitro methods of detecting synergy: time-kill, checkerboard, and E test Antimicrob. Agents Chemother. 40 1996 1914 1918
29. É. Denes, and N. Hidri Synergie et Antagonisme en Antibiothérapie Antibiotiques 11 2009 106 115
30. D. Gülmez, A. Çakar, B. Şener, and et al. Comparison of different antimicrobial susceptibility testing methods for Stenotrophomonas maltophilia and results of synergy testing J. Infect. Chemother. 16 2010 322 328
31. I.H.N. Bassolé, and H.R. Juliani Essential oils in combination and their antimicrobial properties Molecules 17 2012 3989 4006
32. S. Magaldi, S. Mata-Essayag, C. Hartung de Capriles, and et al. Well diffusion for antifungal susceptibility testing Int. J. Infect. Dis. 8 2004 39 45
33. C. Valgas, S.M. De Souza, E.F.A. Smânia, and et al. Screening methods to determine antibacterial activity of natural products Braz. J. Microbiol. 38 2007 369 380
34. A.E. Jiménez-Esquilín, and T.M. Roane Antifungal activities of actinomycete strains associated with high-altitude Sagebrush Rhizosphere J. Ind. Microbiol. Biotechnol. 32 2005 378 381
35. L. Elleuch, M. Shaaban, S. Smaoui, and et al. Bioactive secondary metabolites from a new terrestrial Streptomyces sp. TN262 Appl. Biochem. Biotechnol. 162 2010 579 593
36. M. Lertcanawanichakul, and S. Sawangnop A comparison of two methods used for measuring the antagonistic activity of Bacillus species Walailak J. Sci. Tech. 5 2008 161 171
37. M.S. Ali-Shtayeh, and S.I. Abu Ghdeib Antifungal activity of plant extracts against Dermatophytes Mycoses 42 1999 665 672
38. P.K. Mukherjee, and K. Raghu Effect of temperature on antagonistic and biocontrol potential of Trichoderma sp. on Sclerotium rolfsii Mycopathologia 139 1997 151 155
39. S.N. Kumar, B. Nambisan, A. Sundaresan, and et al. Isolation and identification of antimicrobial secondary metabolites from Bacillus cereus associated with a Rhabditid Entomopathogenic Nematode Ann. Microbiol. 64 2013 209 218
40. R.R. Goodall, and A.A. Levi A microchromatographic method for the detection and approximate determination of the different penicillins in a mixture Nature 158 1946 675
41. R. Fischer, and H. Lautner On the paper chromatographic detection of penicillin preparations Arch. Pharm. 294 1961 1 7
42. G. Horváth, N. Jámbor, A. Végh, and et al. Antimicrobial activity of essential oils: the possibilities of TLC-bioautography Flavour Fragr. J. 25 2010 178 182
43. M. Mehrabani, A. Kazemi, S.A. Ayatollahi Mousavi, and et al. Evaluation of antifungal activities of Myrtus communis L. by bioautography method Jundishapur J. Microbiol. 6 2013 1 7
44. A. Marston Thin-layer chromatography with biological detection in phytochemistry J. Chromatogr. A 1218 2011 2676 2683
45. S. Dewanjee, M. Gangopadhyay, N. Bhattabharya, and et al. Bioautography and its scope in the field of natural product chemistry J. Pharm. Anal. 5 2015 75 84
46. I.M. Choma, and E.M. Grzelak Bioautography detection in thin-layer chromatography J. Chromatogr. A 1218 2011 2684 2691
47. E.M. Grzelak, B. Majer-Dziedzic, and I.M. Choma Development of a novel direct bioautography-thin-layer chromatography test: optimization of growth conditions for gram-negative bacteria, Escherichia coli J. AOAC Int. 94 2011 1567 1572
48. A.H. Brantner Influence of various parameters on the evaluation of antibacterial compounds by the bioautographic TLC assay Pharm. Pharmacol. Lett. 7 1997 152 154
49. M.T.G. Silva, S.M. Simas, T.G. Batista, and et al. Studies on antimicrobial activity, in vitro, of Physalis angulata L. (Solanaceae) fraction and Physalin B bringing out the importance of assay determination Mem. Inst. Oswaldo Cruz 100 2005 779 782
50. A.A. Shahat, G. El-Barouty, R.A. Hassan, and et al. Chemical composition and antimicrobial activities of the essential oil from the seeds of Enterolobium contortisiliquum (leguminosae) J. Environ. Sci. Health. B 43 2008 519 525
51. M. Suleiman, L. McGaw, V. Naidoo, and et al. Detection of antimicrobial compounds by bioautography of different extracts of leaves of selected South African tree species Afr. J. Tradit. Complement. Altern. Med. 7 2010 64 78
52. A. Homans, and A. Fuchs Direct bioautography on thin-layer chromatograms as a method for detecting fungitoxic substances J. Chromatogr. A 51 1970 327 329
53. M.O. Hamburger, and G.A. Cordell A direct bioautographic TLC assay for compounds possessing antibacterial activity J. Nat. Prod. 50 1987 19 22
54. M. Balouiri, S. Bouhdid, E. Harki, and et al. Antifungal activity of Bacillus spp. isolated from Calotropis procera AIT. Rhizosphere against Candida albicans Asian J. Pham. Clin. Res. 8 2015 213 217
55. M.A. Pfaller, D.J. Sheehan, and J.H. Rex Determination of fungicidal activities against yeasts and molds: lessons learned from bactericidal testing and the need for standardization Clin. Microbiol. Rev. 17 2004 268 280
56. CLSI, Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically, Approved Standard, 9th ed., CLSI document M07-A9. Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087, USA, 2012
57. A.G. Al-Bakri, and F.U. Afifi Evaluation of antimicrobial activity of selected plant extracts by rapid XTT colorimetry and bacterial enumeration J. Microbiol. Methods 68 2007 19 25
58. H. Liang, Y. Xing, J. Chen, and et al. Antimicrobial activities of endophytic fungi isolated from Ophiopogon japonicus (Liliaceae) BMC Complement. Altern. Med. 12 2012 238
59. M.C. Monteiro, M. de la Cruz, J. Cantizani, and et al. A new approach to drug discovery: high-throughput screening of microbial natural extracts against Aspergillus fumigatus using resazurin J. Biomol. Screen. 17 2012 524 529
60. D.M. Kuhn, M. Balkis, J. Chandra, and et al. Uses and limitations of the XTT assay in studies of Candida growth and metabolism J. Clin. Microbiol. 41 2003 506 508
61. R.S. Reis, I. Neves, S.L.S. Lourenço, and et al. Comparison of flow cytometric and alamar blue tests with the proportional method for testing susceptibility of Mycobacterium tuberculosis to Rifampin and Isoniazid J. Clin. Microbiol. 42 2004 2247 2248
62. W. Ouedrhiri, S. Bouhdid, M. Balouiri, and et al. Chemical composition of Citrus aurantium L. Leaves and zest essential oils, their antioxidant, antibacterial single and combined effects J. Chem. Pharm. Res. 7 2015 78 84
63. S. Bouhdid, J. Abrini, A. Zhiri, and et al. Investigation of functional and morphological changes in Pseudomonas aeruginosa and Staphylococcus aureus cells induced by Origanum compactum essential oil J. Appl. Microbiol. 106 2009 1558 1568
64. A.L. Castilho, K.R. Caleffi-Ferracioli, P.H. Canezin, and et al. Detection of drug susceptibility in rapidly growing mycobacteria by Resazurin broth microdilution assay J. Microbiol. Methods 111 2015 119 121
65. A. Gehrt, J. Peter, P.A. Pizzo, and et al. Effect of increasing inoculum sizes of pathogenic filamentous fungi on MICs of antifungal agents by Broth microdilution method J. Clin. Microbiol. 33 1995 1302 1307
66. J. Meletiadis, J.F.G.M. Meis, and J.W. Mouton Analysis of growth characteristics of filamentous fungi in different nutrient media J. Clin. Microbiol. 39 2001 478 484
67. A. Gomez-Lopez, A. Aberkane, E. Petrikkou, and et al. Analysis of the influence of tween concentration, inoculum size, assay medium, and reading time on susceptibility testing of Aspergillus spp J. Clin. Microbiol. 43 2005 1251 1255
68. J.L. Rodriguez-Tudela, E. Chryssanthou, E. Petrikkou, and et al. Interlaboratory evaluation of hematocytometer method of inoculum preparation for testing antifungal susceptibilities of filamentous fungi J. Clin. Microbiol. 41 2003 5236 5237
69. CLSI, Reference Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts, Approved Standard, 2nd ed., NCCLS document M27-A2. CLSI, 940 West Valley Road, Suite 1400, Wayne, Pennsylvania 19087-1898, USA, 2002.
70. CLSI, Reference Method for Broth Dilution Antifungal Susceptibility Testing Filamentous Fungi, Approved Standard, 2nd ed., CLSI document M38-A2, 950 West Valley Roadn Suite 2500,Wayne, Pennsylvania 19087, USA, 2008.
71. S. Arikan Current status of antifungal susceptibility testing methods Med. Mycol. 45 2007 569 587
72. C. Lass-Flörl, M. Cuenca-Estrella, D.W. Denning, and et al. Antifungal susceptibility testing in Aspergillus spp. according to EUCAST methodology Med. Mycol. 44 2006 319 325
73. E. Petrikkou, J.L. Rodri, A. Gómez, and et al. Inoculum standardization for antifungal susceptibility testing of filamentous fungi pathogenic for humans J. Clin. Microbiol. 39 2001 1345 1347
74. A. Aberkane, M. Cuenca-Estrella, A. Gomez-Lopez, and et al. Comparative evaluation of two different methods of inoculum preparation for antifungal susceptibility testing of filamentous fungi J. Antimicrob. Chemother. 50 2002 719 722
75. CLSI, Methods for Determining Bactericidal Activity of Antimicrobial Agents. Approved Guideline, CLSI document M26-A. Clinical and Laboratory Standards Institute, 950 West Valley Roadn Suite 2500,Wayne, Pennsylvania 19087, USA, 1998.
76. E. Cantón, J. Pemán, A. Viudes, and et al. Minimum fungicidal concentrations of amphotericin B for bloodstream Candida species Diagn. Microbiol. Infect. Dis. 45 2003 203 206
77. A. Espinel-Ingroff, A. Fothergill, J. Peter, and et al. Testing conditions for determination of minimum fungicidal concentrations of new and established antifungal agents for Aspergillus spp.: NCCLS collaborative study J. Clin. Microbiol. 40 2002 3204 3208
78. A. Espinel-Ingroff, V. Chaturvedi, A. Fothergill, and et al. Optimal testing conditions for determining MICs and minimum fungicidal concentrations of new and established antifungal agents for uncommon molds: NCCLS collaborative study J. Clin. Microbiol. 40 2002 3776 3781
79. CLSI, Methods for Antimicrobial Dilution and Disk Susceptibility of Infrequently Isolated or Fastidious Bacteria, Approved Guideline, 2nd. ed., CLSI document M45-A2. Clinical and Laboratory Standards Institute, 950 West Valley Roadn Suite 2500,Wayne, Pennsylvania 19087, USA, 2010.
80. T. Menon, K. Umamaheswari, N. Kumarasamy, and et al. Efficacy of fluconazole and itraconazole in the treatment of oral candidiasis in HIV patients Acta Trop. 80 2001 151 154
81. A. Imhof, S.A. Balajee, and K.A. Mar New methods to assess susceptibilities of Aspergillus isolates to caspofungin J. Clin. Microbiol. 41 2003 5683 5688
82. M. Mock, M. Monod, F. Baudraz-Rosselet, and et al. Tinea capitis dermatophytes: susceptibility to antifungal drugs tested in vitro and in vivo Dermatology 197 1998 361 367
83. E. Speeleveld, B. Gordts, H.W. Van Landuyt, and et al. Susceptibility of clinical isolates of Fusarium to antifungal drugs Mycoses 39 1996 37 40
84. C.J. Clancy, H. Huang, S. Cheng, and et al. Characterizing the effects of caspofungin on Candida albicans, Candida parapsilosis, and Candida glabrata isolates by simultaneous time-kill and postantifungal-effect experiments Antimicrob. Agents Chemother. 50 2006 2569 2572
85. M.E. Klepser, E.J. Ernst, R.E. Lewis, and et al. Influence of test conditions on antifungal time-kill curve results: proposal for standardized methods Antimicrob. Agents Chemother. 42 1998 1207 1212
86. S.P. Crouch, R. Kozlowski, K.J. Slater, and et al. The use of ATP Bioluminescence as a measure of cell proliferation and cytotoxicity J. Immunol. Methods 160 1993 81 88
87. A. Bozorg, I.D. Gates, and A. Sen, Using Bacterial bioluminescence to evaluate the impact of biofilm on porous media hydraulic properties J. Microbiol. Methods 109 2015 84 92
88. L. Paloque, N. Vidal, M. Casanova, and et al. A new, rapid and sensitive bioluminescence assay for drug screening on Leishmania J. Microbiol. Methods 95 2013 320 323
89. S. Finger, C. Wiegand, and H.J. Buschmann Antibacterial properties of cyclodextrin-antiseptics-complexes determined by microplate laser nephelometry and ATP bioluminescence assay Int. J. Pharm. 452 2013 188 193
90. N. Andreu, T. Fletcher, N. Krishnan, and et al. Rapid measurement of antituberculosis drug activity in vitro and in macrophages using bioluminescence J. Antimicrob. Chemother. 67 2012 404 414
91. B. Beckers, H.R. Lang, D. Schimke, and et al. Evaluation of a bioluminescence assay for rapid antimicrobial susceptibility testing of mycobacteria Eur. J. Clin. Microbiol. 4 1985 556 561
92. S. Finger, C. Wiegand, H. Buschmann, and et al. Antimicrobial properties of cyclodextrin-antiseptics-complexes determined by microplate laser nephelometry and ATP bioluminescence assay Int. J. Pharm. 436 2012 851 856
93. C. Galiger, M. Brock, G. Jouvion, and et al. Assessment of efficacy of antifungals against Aspergillus fumigatus: value of real-time bioluminescence imaging Antimicrob. Agents Chemother. 57 2013 3046 3059
94. L. Vojtek, P. Dobes, E. Buyukguzel, and et al. Bioluminescent assay for evaluating antimicrobial activity in insect haemolymph Eur. J. Entomol. 111 2014 335 340
95. A. Paparella, L. Taccogna, I. Aguzzi, and et al. Flow cytometric assessment of the antimicrobial activity of essential oils against Listeria monocytogenes Food Control. 19 2008 1174 1182
96. R. Ramani, and V. Chaturvedi Flow cytometry antifungal susceptibility testing of pathogenic yeasts other than Candida albicans and comparison with the NCCLS broth microdilution test Antimicrob. Agents Chemother. 44 2000 2752 2758
97. L.J. Green, P. Marder, L.L. Mann, and et al. LY303366 exhibits rapid and potent fungicidal activity in flow cytometric assays of yeast viability Antimicrob. Agents Chemother. 43 1999 830 835
98. L. Green, B. Petersen, L. Steimel, and et al. Rapid determination of antifungal activity by flow cytometry J. Clin. Microbiol. 32 1994 1088 1091
99. R. Ramani, A. Ramani, and S.J. Wong Rapid flow cytometric susceptibility testing of Candida albicans J. Clin. Microbiol. 35 1997 2320 2324
100. A.E. Yousef, and P.D. Courtney Basics of stress adaptation and implications in new-generation foods A.E. Yousef, V.K. Juneja, Microbial Stress Adaptation and Food Safety 2003 CRC Press Washington DC 2 8
101. Y.W. Tang, and C.W. Stratton Advanced Techniques in Diagnostic Microbiology, 2nd ed. 2013 Springer New York Heidelberg Dordrecht, London pp. 937