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Susceptibility

In Vitro Drug Interaction Modeling of Combinations of Azoles with Terbinafine against Clinical Scedosporium prolificans Isolates

Joseph Meletiadis, Johan W. Mouton, Jacques F. G. M. Meis, Paul E. Verweij
Joseph Meletiadis
1Department of Medical Microbiology, University Medical Center Nijmegen
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Johan W. Mouton
2Department of Medical Microbiology and Infectious Diseases, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands
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Jacques F. G. M. Meis
2Department of Medical Microbiology and Infectious Diseases, Canisius Wilhelmina Hospital, Nijmegen, The Netherlands
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Paul E. Verweij
1Department of Medical Microbiology, University Medical Center Nijmegen
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  • For correspondence: p.verweij@mmb.azn.nl
DOI: 10.1128/AAC.47.1.106-117.2003
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  • FIG. 1.
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    FIG. 1.

    Assessment of the in vitro interaction between voriconazole (VCZ) and terbinafine (TB) against a clinical S. prolificans strain (AZN87898) based on the LA-based models using the SP48 data. (Ai) Checkerboard showing the percentage of growth for each combination, combinations with more than 50% growth (light grey area), the MIC-2 of voriconazole and terbinafine (percentages in boldface type) as well as the iso-effective combinations based on which the ΣFIC-2 indices were calculated (dark grey area), combinations with ΣFIC-2 indices lower than 0.5 (underlined percentages) and the combination with the lowest ΣFIC-2 index (0.20), corresponding to the FICi-2 (percentage shown in black cell). (Aii) Corresponding isobologram with the additivity line (dashed line). (B) The 3-D (i) and contour (ii) plots of the percent synergy calculated with the Greco model with the following fitted parameters (means ± 95% CI): IC50,TB = 5.33 ± 0.57, IC50,VCZ = 2.63 ± 0.31, mTB = − 0.51 ± 0.04, mVCZ = −1.1 ± 0.11, α = 13.9 ± 1.6.

  • FIG. 2.
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    FIG. 2.

    Assessment of the in vitro interaction between voriconazole (VCZ) and terbinafine (TB) against a clinical S. prolificans strain (AZN7898) based on BI-based models using the SP48 data. (A) The 3-D (i) and contour (ii) plots of the percent synergy calculated with the nonparametric approach, which resulted in 700% synergy. (B) The 3-D (i) and contour (ii) plots of the percent synergy calculated with the semiparametric approach, which resulted in 1,118% synergy with the following fitted parameters (means ± 95% CI) of the Emax model: IC50,TB = 19.9 ± 6.7, mTB = −0.76 ± 0.21, IC50,VCZ = 2.8 ± 0.7, mVCZ = −1.3 ± 0.37.

Tables

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  • TABLE 1.

    Susceptibilities of S. prolificans strains against various azoles alone and in combination with terbinafinea

    Combination and strainGM MIC-1 (range)
    Drug aloneDrugs in combination
    AzoleTBAzoleTB
    VCZ and TB
        78989.51 (8-16)>64 (>64)0.71 (0.13-2)9.51 (2-32)
        79016.73 (4-8)>64 (>64)0.25 (0.03-1)6.73 (4-16)
        79026.73 (4-8)>64 (>64)0.5 (0.13-1)8 (8)
        79068 (8)>64 (>64)1 (0.5-2)9.51 (8-16)
        79189.51 (8-16)>64 (>64)1.19 (0.5-2)11.31 (2-32)
    MCZ and TB
        789864 (32->64)>64 (>64)1.19 (0.25-4)2.83 (2-4)
        7901>64 (>64)>64 (>64)2.83 (2-4)2 (1-4)
        790245.25 (8->64)>64 (>64)2 (0.13-8)2 (2)
        7906>64 (>64)>64 (>64)2.83 (2-4)1.41 (1-4)
        791826.91 (8->64)>64 (>64)0.84 (0.13-2)2.38 (2-4)
    ICZ and TB
        7898>32 (>32)>64 (>64)1 (0.5-2)16 (16)
        7901>32 (>32)>64 (64->64)10.01 (4-16)12.7 (8-16)
        7902>32 (>32)>64 (64->64)4 (0.5-16)8 (8)
        7906>32 (>32)>64 (>64)3.17 (1-16)8 (2-16)
        7918>32 (>32)>64 (>64)4 (1-16)10.08 (2-16)
    • ↵ a Based on the MIC-1 and SP72 data. Abbreviations: VCZ, voriconazole; MCZ, miconazole; ICZ, itraconazole; TB, terbinafine.

  • TABLE 2.

    In vitro interaction between voriconazole and terbinafine against S. prolificans

    Method and strainResult according to theory
    LABIa
    Nonparametric [median (range)]Parametricb (α ± 95% CI)NonparametricSemiparametricc
    FICi-2FICi-1ΣSYN (n)ΣANT (n)ΣSYN (n)ΣANT (n)
    SP48
        78980.13 (0.07-0.19)0.10 (0.06-0.28)13.9 ± 1.6700 (29)0 (0)1,118 (51)0 (0)
        79010.25 (0.08-0.75)0.10 (0.05-0.13)10.8 ± 1.8428 (29)0 (0)742 (48)0 (0)
        79060.26 (0.13-0.38)0.13 (0.06-0.25)16.3 ± 4.5457 (26)0 (0)566 (36)0 (0)
        79180.09 (0.04-0.13)0.09 (0.04-0.09)2,479.8 ± 289.1409 (21)0 (0)702 (39)0 (0)
        79020.14 (0.05-0.27)0.09 (0.06-0.13)42.2 ± 7.3709 (44)0 (0)987 (53)0 (0)
            Median0.140.1016.3045707420
    SP72
        78980.07 (0.05-0.31)0.14 (0.13-0.75)13.0 ± 3.41,582 (49)0 (0)942 (42)0 (0)
        79010.32 (0.04-0.75)0.13 (0.07-0.25)32.4 ± 6.0195 (14)−3 (1)702 (43)0 (0)
        79060.38 (0.13-0.50)0.28 (0.19-0.38)8.4 ± 3.357 (8)0 (0)67 (4)0 (0)
        79180.08 (0.02-0.28)0.27 (0.16-0.50)1,517.5 ± 334.8770 (29)−9 (2)520 (21)−12 (1)
        79020.29 (0.13-0.31)0.19 (0.08-0.25)6.6 ± 2.1185 (15)0 (0)579 (41)−10 (2)
            Median0.290.1914.0419505790
    COL72
        78980.25 (0.02-0.63)0.13 (0.04-0.16)8.9 ± 4.0165 (10)0 (0)442 (20)0 (0)
        79010.75 (0.50-1.00)0.16 (0.13-0.16)29.9 ± 16.80 (0)0 (0)23 (4)0 (0)
        79060.53 (0.07-0.75)0.17 (0.07-0.19)8.0 ± 3.034 (4)0 (0)72 (7)0 (0)
        79180.13 (0.08-0.25)0.20 (0.04-0.31)40.7 ± 16.5254 (8)0 (0)49 (3)0 (0)
        79020.16 (0.08-0.50)0.11 (0.04-0.19)42.0 ± 12.2619 (22)0 (0)903 (32)0 (0)
            Median0.250.1629.901650720
    mCOL48
        78980.25 (0.25-0.26)0.25 (0.25-0.50)1,754.9 ± 947.1299 (15)−4 (1)373 (19)−5 (2)
        79010.25 (0.25)0.25 (0.19-0.25)33.7 ± 11.5413 (25)−5 (2)564 (34)0 (0)
        79060.25 (0.25)0.27 (0.25-0.38)2.7 ± 1.5532 (35)0 (0)753 (40)0 (0)
        79180.25 (0.25-0.26)0.13 (0.13-0.25)9.9 ± 4.1214 (10)0 (0)75 (5)0 (0)
        79020.26 (0.25-0.50)0.27 (0.13-0.38)8.2 ± 2.572 (5)0 (0)236 (11)0 (0)
            Median0.250.259.929903730 (0)
    mCOL72
        78980.13 (0.08-0.13)0.07 (0.06-0.07)10.3 ± 7.6279 (6)0 (0)56 (3)0 (0)
        79010.25 (0.09-0.38)0.13 (0.07-0.13)5.0 ± 2.6795 (16)0 (0)379 (8)0 (0)
        79060.31 (0.13-0.31)0.13 (0.06-0.13)3.9 ± 2.4566 (180)0 (0)1,072 (26)0 (0)
        79180.13 (0.07-0.13)0.14 (0.07-0.14)4.7 ± 2.9579 (11)0 (0)513 (11)0 (0)
        79020.13 (0.07-0.25)0.09 (0.06-0.13)14.8 ± 5.0464 (9)0 (0)468 (10)0 (0)
            Median0.130.135.056604680
    • ↵ a The median absolute coefficient of variation of the differences between observed and predicted percent growth at each drug combination among the replicates of all strains ranged from 41 to 232% (median, 57%) for the SP method, 68 to 166% (median, 123%) for the COL method, and 44 to 83% (median, 53%) for the mCOL method with the semiparametric approach and from 49 to 165% (median, 88%) for the SP method, 86 to 180% (median, 105%) for the COL method, and 45 to 64% (median 51%) for the mCOL method with the nonparametric approach.

    • ↵ b The R2 from the nonlinear regression analysis for the fully parametric Greco model ranged from 0.83 to 0.96 (median, 0.90). The IC50s ranged from 0.96 to 2342 mg/liter (geometric mean, 5.9 mg/liter) of terbinafine and from 1.2 to 25 mg/liter (geometric mean, 4.2 mg/liter) of voriconazole. The slope (m) ranged from −0.16 to −1.46 (median, −0.61) for terbinafine and from −0.45 to −1.79 (median, −0.94) for voriconazole.

    • ↵ c The R2 from the nonlinear regression analysis for the Emax model of the semiparametric approach ranged from 0.74 to 0.99 (median, 0.90). The IC50s ranged from 1.6 to 67.4 mg/liter (geometric mean, 10.6 mg/liter) of terbinafine and from 0.24 to 16.7 mg/liter (geometric mean, 2.9 mg/liter) of voriconazole. The slopes m ranged from −0.44 to −4.38 (median, −0.92) for terbinafine and from −0.13 to −5.2 (median, −1.2) for voriconazole.

  • TABLE 3.

    In vitro interaction between miconazole and terbinafine against S. prolificans

    Method and strainResult according to theory
    LABIa
    Nonparametric [median (range)]Parametricb (α ± 95% CI)NonparametricSemiparametricc
    FICi-2FICi-1ΣSYN (n)ΣANT (n)ΣSYN (n)ΣANT (n)
    SP48
        78980.13 (0.02-0.28)0.04 (0.01-0.05)302.1 ± 32.6173 (15)0 (0)242 (17)0 (0)
        79010.11 (0.02-0.14)0.05 (0.02-0.06)3,072.0 ± 441.7243 (15)0 (0)396 (22)0 (0)
        79020.17 (0.14-0.28)0.08 (0.01-0.28)111.1 ± 17.5163 (20)0 (0)206 (22)−4 (1)
        79060.17 (0.09-0.28)0.04 (0.01-0.13)565.0 ± 110.7160 (11)0 (0)284 (18)0 (0)
        79180.06 (0.03-0.15)0.03 (0.02-0.08)9,462.1 ± 1,194.5460 (33)0 (0)615 (40)0 (0)
            Median0.130.04565.017802840
    SP72
        78980.06 (0.02-0.09)0.05 (0.03-0.08)552.1 ± 77.657 (5)0 (0)135 (13)0 (0)
        79010.05 (0.02-0.08)0.05 (0.03-0.06)5,516.6 ± 966.9146 (10)0 (0)365 (21)0 (0)
        79020.06 (0.03-0.28)0.06 (0.03-0.14)1,374.9 ± 242.910 (2)0 (0)78 (8)−6 (1)
        79060.09 (0.03-0.13)0.05 (0.02-0.07)434.5 ± 124.967 (4)0 (0)138 (11)0 (0)
        79180.06 (0.03-0.16)0.05 (0.03-0.27)5,464.7 ± 1,082.9392 (27)0 (0)505 (33)0 (0)
            Median0.060.051,374.96701380
    COL72
        78980.06 (0.03-0.09)0.04 (0.02-0.06)817.5 ± 297.57 (1)0 (0)14 (1)0 (0)
        79010.19 (0.06-0.28)0.03 (0.02-0.04)180.1 ± 50.317 (3)0 (0)92 (11)−25 (2)
        79020.05 (0.02-0.08)0.05 (0.02-0.08)128.2 ± 28.48 (1)0 (0)0 (0)0 (0)
        79060.030.05 (0.03-0.16)55.5 ± 23.80 (0)0 (0)0 (0)0 (0)
        79180.08 (0.03-0.19)0.04 (0.02-0.09)633.2 ± 162.257 (3)0 (0)0 (0)0 (0)
            Median0.060.04180.18000
    MCOL48
        78980.27 (0.27-0.28)0.05 (0.04-0.13)9.8 ± 2.2556 (49)0 (0)567 (43)−6 (1)
        79010.16 (0.09-0.31)0.05 (0.04-0.05)44.3 ± 11.4955 (55)0 (0)941 (49)0 (0)
        79020.27 (0.27-0.50)0.04 (0.03-0.05)34.1 ± 8.2354 (41)0 (0)392 (35)0 (0)
        79060.38 (0.31-0.51)0.04 (0.04-0.05)18.5 ± 5.0539 (35)0 (0)526 (37)0 (0)
        79180.27 (0.13-0.28)0.31 (0.05-0.31)3,807.5 ± 1,479.4259 (32)0 (0)372 (33)0 (0)
            Median0.270.0534.153905260
    MCOL72
        78980.03 (0.03-0.04)0.06 (0.06-0.13)9,505.2 ± 2,824.2487 (30)0 (0)518 (28)−9 (1)
        79010.03 (0.02-0.04)0.09 (0.06-0.09)6,768.1 ± 2,078.91,051 (37)0 (0)1,006 (36)0 (1)
        79020.03 (0.02-0.03)0.06 (0.06-0.13)7,740.3 ± 1,887.31,751 (61)0 (0)1,295 (46)0 (0)
        79060.03 (0.02-0.04)0.13 (0.06-0.13)7,872.5 ± 3,421.3606 (39)0 (0)517 (38)0 (0)
        79180.06 (0.03-0.09)0.08 (0.06-0.08)534.6 ± 141.8595 (45)0 (0)538 (34)0 (0)
            Median0.030.087,740.360605380
    • ↵ a The median absolute coefficient of variation of the differences between observed and predicted percent growth at each drug combination among the replicates of all strains ranged from 60 to 124% (median, 95%) for the SP method, 142 to 227% (median, 173%) for the COL method, and 24 to 49% (median, 40%) for the mCOL method with the semiparametric approach and from 69 to 191% (median, 123%) for the SP method, 118 to 343% (median, 236%) for the COL method, and 23 to 56% (median, 36%) for the mCOL method with the nonparametric approach.

    • ↵ b The R2 from the nonlinear regression analysis for the fully parametric Greco model ranged from 0.76 to 0.93 (median, 0.88). The IC50s ranged from 0.23 × 103 to −7.2 × 103 mg/liter (geometric mean, 22.1 mg/liter) of terbinafine and from 0.53 to 32.9 mg/liter (geometric mean, 4.2 mg/liter) of miconazole. Relatively high IC50s of terbinafine were obtained after 72 h of incubation. The slope (m) ranged from −0.1 to −0.53 (median, −0.16) for terbinafine and from −0.27 to −4.4 (median, −0.44) for miconazole.

    • ↵ c The R2 from the nonlinear regression analysis for the Emax model of the semiparametric approach ranged from 0.73 to 0.99 (median, 0.88). The IC50s ranged from 0.57 to 1,028 mg/liter (geometric mean, 11.4 mg/liter) of terbinafine and from 0.19 to 43.74 mg/liter (geometric mean, 4.43 mg/liter) of miconazole. The slope (m) ranged from −0.10 to −0.86 (median, −0.35) for terbinafine and from −0.24 to −1.63 (median, −0.45) for miconazole.

  • TABLE 4.

    In vitro interaction between itraconazole and terbinafine against S. prolificans

    Method and strainResult according to theory
    LABIa
    Nonparametric [median (range)]Parametricb (α ± 95% CI)NonparametricSemiparametricc
    FICi-2FICi-1ΣSYN (n)ΣANT (n)ΣSYN (n)ΣANT (n)
    SP48
        78980.13 (0.07-0.16)0.19 (0.13-0.19)4.3 ± 1.319 (2)−20 (1)244 (18)−45 (3)
        79010.52 (0.51-0.52)0.13 (0.13-0.19)9.3 ± 1.836 (3)−25 (2)90 (15)−27 (2)
        79020.07 (0.02-0.56)0.13 (0.13-0.25)203.8 ± 49.149 (4)0 (0)144 (8)0 (0)
        79060.16 (0.04-0.51)0.14 (0.13-0.19)3.3 ± 0.8230 (14)0 (0)291 (16)0 (0)
        79180.51 (0.07-0.51)0.13 (0.09-0.38)25.1 ± 9.652 (5)0 (0)167 (11)0 (0)
            Median0.160.139.34901670
    SP72
        78980.13 (0.07-0.56)0.14 (0.13-0.16)25.9 ± 8.276 (6)−31 (2)202 (16)−178 (11)
        79010.75 (0.52-1.00)0.31 (0.31-0.38)57.2 ± 14.710 (1)−85 (4)7 (1)−98 (4)
        79020.02 (0.02-0.28)0.19 (0.07-0.38)182.9 ± 48.141 (4)0 (0)90 (7)0 (0)
        79060.13 (0.06-0.38)0.16 (0.14-0.27)8.1 ± 2.5536 (26)0 (0)428 (23)0 (0)
        79180.51 (0.06-0.52)0.14 (0.09-0.38)457.6 ± 148.581 (8)0 (0)180 (17)0 (0)
            Median0.130.1657.27601800
    COL72
        78980.07 (0.02-0.26)0.16 (0.09-0.16)202.9 ± 130.70 (0)−46 (40)0 (0)−109 (8)
        79010.13 (0.01-0.16)0.26 (0.25-0.27)5.2 ± 3.37 (1)−83 (8)0 (0)0 (0)
        79020.13 (0.01-1.02)0.19 (0.14-0.25)29.1 ± 20.510 (1)−53 (4)179 (11)−3 (1)
        79060.04 (0.02-0.13)0.13 (0.09-0.25)23.7 ± 13.76 (1)−209 (26)16 (3)−404 (13)
        79180.16 (0.08-0.26)0.16 (0.13-0.16)69.9 ± 59.7380 (12)0 (0)384 (15)−4 (1)
            Median0.130.1629.17−5316−4
    MCOL48
        78980.34 (0.19-0.50)0.27 (0.27-0.28)105.4 ± 39.125 (5)−1 (1)69 (8)0 (0)
        79010.14 (0.13-0.15)0.20 (0.14-0.26)802.1 ± 310.8276 (22)0 (0)417 (20)0 (0)
        79020.27 (0.25-0.28)0.20 (0.16-0.25)23.9 ± 9.4105 (12)0 (0)209 (20)−0 (0)
        79060.20 (0.16-0.25)0.23 (0.19-0.27)81.6 ± 28.031 (4)0 (0)88 (6)0 (0)
        79180.11 (0.06-0.16)0.08 (0.02-0.14)795.3 ± 435.979 (5)0 (0)49 (2)0 (0)
            Median0.200.20105.4790880
    MCOL72
        78980.21 (0.14-0.28)0.18 (0.04-0.31)959.7 ± 542.4146 (5)0 (0)529 (18)0 (0)
        79010.04 (0.02-0.07)0.15 (0.05-0.25)5,091.5 ± 3,287.1942 (31)0 (0)372 (15)0 (0)
        79020.30 (0.28-0.31)0.05 (0.04-0.06)404.7 ± 242.3533 (22)0 (0)616 (23)−5 (10)
        79060.28 (0.25-0.31)0.06 (0.05-0.07)2,351.3 ± 1,445.183 (5)0 (0)300 (19)0 (0)
        79180.04 (0.03-0.05)0.07 (0.05-0.09)7,673.7 ± 389.4263 (10)0 (0)1,354 (44)0 (0)
            Median0.210.07959.72630529−16
    • ↵ a The median absolute coefficient of variation of the differences between observed and predicted percent growth at each drug combination among replicates of all strains ranged from 58 to 157% (median, 106%) for the SP method, 59 to 222% (median, 106%) for the COL method, and 51 to 69% (median, 61%) for mCOL method with the semiparametric approach and from 57 to 287% (median, 154%) for the SP method, 51 to 195% (median, 115%) for the COL method, and 58 to 89% (median, 71%) for the mCOL method with the non-parametric approach.

    • ↵ b The R2 from the nonlinear regression analysis for the fully parametric Greco model ranged from 0.69 to 0.95 (median, 0.88). The IC50s ranged from 0.15 to 93.6 mg/liter (geometric mean, 2.98 mg/liter) of terbinafine and 17.5 × 103 to 7 × 103 mg/liter (geometric mean, 404.4 mg/liter) of itraconazole. The slope (m) ranged from −0.15 to −1.7 (median, −0.68) for terbinafine and −0.16 to −26.7 (median, −0.28) for itraconazole.

    • ↵ c The R2 from the nonlinear regression analysis for the Emax model of the semiparametric approach ranged from 0.77 to 0.99 (median, 0.95). The IC50s ranged from 0.23 to 155 mg/liter of terbinafine (geometric mean, 2.85 mg/liter) and from 5.2 to 5011 mg/liter of itraconazole (geometric mean, 298.64 mg/liter). The slope (m) ranged from −0.11 to −1.22 (median, −0.52) for terbinafine and −0.06 to −0.99 (median, −0.43) for itraconazole.

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In Vitro Drug Interaction Modeling of Combinations of Azoles with Terbinafine against Clinical Scedosporium prolificans Isolates
Joseph Meletiadis, Johan W. Mouton, Jacques F. G. M. Meis, Paul E. Verweij
Antimicrobial Agents and Chemotherapy Jan 2003, 47 (1) 106-117; DOI: 10.1128/AAC.47.1.106-117.2003

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In Vitro Drug Interaction Modeling of Combinations of Azoles with Terbinafine against Clinical Scedosporium prolificans Isolates
Joseph Meletiadis, Johan W. Mouton, Jacques F. G. M. Meis, Paul E. Verweij
Antimicrobial Agents and Chemotherapy Jan 2003, 47 (1) 106-117; DOI: 10.1128/AAC.47.1.106-117.2003
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KEYWORDS

antifungal agents
Naphthalenes
Pyrimidines
Scedosporium
triazoles

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