130
Views
0
CrossRef citations to date
0
Altmetric
Review

Pharmacological management of invasive mold infections in solid organ transplant recipients

Pages 239-254 | Received 09 Nov 2023, Accepted 29 Feb 2024, Published online: 11 Mar 2024

References

  • Gavalda J, Len O, San Juan R, et al. Risk factors for invasive aspergillosis in solid-organ transplant recipients: a case-control study. Clin Infect Dis. 2005;41(1):52–59. doi: 10.1086/430602
  • Pappas PG, Alexander BD, Andes DR, et al. Invasive fungal infections among organ transplant recipients: results of the transplant-associated infection surveillance network (TRANSNET). Clin Infect Dis. 2010;50(8):1101–1111. doi: 10.1086/651262
  • Neofytos D, Chatzis O, Nasioudis D, et al. Epidemiology, risk factors and outcomes of invasive aspergillosis in solid organ transplant recipients in the Swiss transplant cohort study. Transpl Infect Dis. 2018;20(4):e12898. doi: 10.1111/tid.12898
  • Gavaldà J, Meije Y, Fortún J, et al. Invasive fungal infections in solid organ transplant recipients. Clin Microbiol Infect. 2014;20(Suppl 7):27–48. doi: 10.1111/1469-0691.12660
  • López-Medrano F, Fernández-Ruiz M, Silva JT, et al. Clinical presentation and determinants of mortality of invasive pulmonary aspergillosis in kidney transplant recipients: a multinational cohort study. Am J Transplant. 2016;16(11):3220–3234. doi: 10.1111/ajt.13837
  • Saliba F, Pascher A, Cointault O, et al. Randomized trial of micafungin for the prevention of invasive fungal infection in high-risk liver transplant recipients. Clin Infect Dis. 2015;60(7):997–1006. doi: 10.1093/cid/ciu1128
  • Fortun J, Martin-Davila P, Montejo M, et al. Prophylaxis with caspofungin for invasive fungal infections in high-risk liver transplant recipients. Transplantation. 2009;87(3):424–435. doi: 10.1097/TP.0b013e3181932e76
  • Fernández-Ruiz M, Cardozo C, Salavert M, et al. Candidemia in solid organ transplant recipients in Spain: epidemiological trends and determinants of outcome. Transpl Infect Dis. 2019;21(6):e13195. doi: 10.1111/tid.13195
  • O’Halloran JA, Powderly WG, Spec A. Cryptococcosis today: it is not all about HIV infection. Curr Clin Microbiol Rep. 2017;4(2):88–95. doi: 10.1007/s40588-017-0064-8
  • Trujillo H, Fernández-Ruiz M, Gutierrez E, et al. Invasive pulmonary aspergillosis associated with COVID-19 in a kidney transplant recipient. Transpl Infect Dis. 2021;23(2):e13501. doi: 10.1111/tid.13501
  • Donnelly JP, De Pauw BE. Voriconazole-a new therapeutic agent with an extended spectrum of antifungal activity. Clin Microbiol Infect. 2004;10(Suppl 1):107–117. doi: 10.1111/j.1470-9465.2004.00838.x
  • Herbrecht R. Voriconazole: therapeutic review of a new azole antifungal. Expert Rev Anti Infect Ther. 2004;2(4):485–497. doi: 10.1586/14787210.2.4.485
  • Herbrecht R, Denning DW, Patterson TF, et al. Voriconazole versus amphotericin B for primary therapy of invasive aspergillosis. N Engl J Med. 2002;347(6):408–415. doi: 10.1056/NEJMoa020191
  • Denning DW, Ribaud P, Milpied N, et al. Efficacy and safety of voriconazole in the treatment of acute invasive aspergillosis. Clin Infect Dis. 2002;34(5):563–571. doi: 10.1086/324620
  • Perfect JR, Marr KA, Walsh TJ, et al. Voriconazole treatment for less-common, emerging, or refractory fungal infections. Clin Infect Dis. 2003;36(9):1122–1131. doi: 10.1086/374557
  • Walsh TJ, Anaissie EJ, Denning DW, et al. Treatment of aspergillosis: clinical practice guidelines of the infectious diseases society of America. Clin Infect Dis. 2008;46(3):327–360. doi: 10.1086/525258
  • Tsiodras S, Zafiropoulou R, Giotakis J, et al. Deep sinus aspergillosis in a liver transplant recipient successfully treated with a combination of caspofungin and voriconazole. Transpl Infect Dis. 2004;6(1):37–40. doi: 10.1111/j.1399-3062.2004.00039.x
  • Levin T, Suh B, Beltramo D, et al. Aspergillus mediastinitis following orthotopic heart transplantation: case report and review of the literature. Transpl Infect Dis. 2004;6(3):129–131. doi: 10.1111/j.1399-3062.2004.00064.x
  • Fortun J, Martin-Davila P, Sanchez MA, et al. Voriconazole in the treatment of invasive mold infections in transplant recipients. Eur J Clin Microbiol Infect Dis. 2003;22(7):408–413. doi: 10.1007/s10096-003-0960-0
  • Baden LR, Katz JT, Fishman JA, et al. Salvage therapy with voriconazole for invasive fungal infections in patients failing or intolerant to standard antifungal therapy. Transplantation. 2003;76(11):1632–1637. doi: 10.1097/01.TP.0000089109.42239.75
  • Wieland T, Liebold A, Jagiello M, et al. Superiority of voriconazole over amphotericin B in the treatment of invasive aspergillosis after heart transplantation. J Heart Lung Transplant. 2005;24(1):102–104. doi: 10.1016/j.healun.2003.10.014
  • Ullmann AJ, Aguado JM, Arikan-Akdagli S, et al. Diagnosis and management of aspergillus diseases: executive summary of the 2017 ESCMID-ECMM-ERS guideline. Clin Microbiol Infect. 2018;24:e1–e38. doi: 10.1016/j.cmi.2018.01.002
  • Husain S, Camargo JF. Invasive aspergillosis in solid-organ transplant recipients: guidelines from the American society of transplantation infectious diseases community of practice. Clin Transplant. 2019;33(9):e13544.
  • Barchiesi F, Mazzocato S, Mazzanti S, et al. Invasive aspergillosis in liver transplant recipients: epidemiology, clinical characteristics, treatment, and outcomes in 116 cases. Liver Transpl. 2015;21(2):204–212. doi: 10.1002/lt.24032
  • Farges C, Cointault O, Murris M, et al. Outcomes of solid organ transplant recipients with invasive aspergillosis and other mold infections. Transpl Infect Dis. 2020;22(1):e13200. doi: 10.1111/tid.13200
  • Veroux M, Corona D, Gagliano M, et al. Voriconazole in the treatment of invasive aspergillosis in kidney transplant recipients. Transplant Proc. 2007;39(6):1838–1840. doi: 10.1016/j.transproceed.2007.05.012
  • Abe K, Shinoda M, Uno S, et al. Invasive pulmonary aspergillosis after liver transplantation: lessons from successfully treated cases and review of the literature. Surg Today. 2021;51(8):1361–1370. doi: 10.1007/s00595-021-02263-z
  • Neofytos D, Treadway S, Ostrander D, et al. Epidemiology, outcomes, and mortality predictors of invasive mold infections among transplant recipients: a 10-year, single-center experience. Transpl Infect Dis. 2013;15(3):233–242. doi: 10.1111/tid.12060
  • Baddley JW, Andes DR, Marr KA, et al. Antifungal therapy and length of hospitalization in transplant patients with invasive aspergillosis. Med Mycol. 2013;51(2):128–135. doi: 10.3109/13693786.2012.690108
  • Lutsar I, Roffey S, Troke P. Voriconazole concentrations in the cerebrospinal fluid and brain tissue of guinea pigs and immunocompromised patients. Clin Infect Dis. 2003;37(5):728–732. doi: 10.1086/377131
  • Weiler S, Fiegl D, MacFarland R, et al. Human tissue distribution of voriconazole. Antimicrob Agents Chemother. 2011;55(2):925–928. doi: 10.1128/AAC.00949-10
  • Schwartz S, Reisman A, Troke PF. The efficacy of voriconazole in the treatment of 192 fungal central nervous system infections: a retrospective analysis. Infection. 2011;39(3):201–210. doi: 10.1007/s15010-011-0108-6
  • Kramer M, Kramer MR, Blau H, et al. Intravitreal voriconazole for the treatment of endogenous aspergillus endophthalmitis. Ophthalmol. 2006;113(7):1184–1186. doi: 10.1016/j.ophtha.2006.01.059
  • Ferreira TB, Vaz F, Rodrigues A, et al. Intravitreal voriconazole as primary treatment for endogenous Aspergillus endophthalmitis. BMJ Case Rep. 2009;2009(may21 1):bcr1020081110. doi: 10.1136/bcr.10.2008.1110
  • Patterson TF, Thompson GR, Denning DW, et al. Practice guidelines for the diagnosis and management of aspergillosis: 2016 update by the infectious diseases society of America. Clin Infect Dis. 2016;63(4):e1–e60. doi: 10.1093/cid/ciw326
  • Wiederhold NP, Lewis RE. The echinocandin antifungals: an overview of the pharmacology, spectrum and clinical efficacy. Expert Opin Investig Drugs. 2003;12(8):1313–1333. doi: 10.1517/13543784.12.8.1313
  • Raasch RH. Anidulafungin: review of a new echinocandin antifungal agent. Expert Rev Anti Infect Ther. 2004;2(4):499–508. doi: 10.1586/14787210.2.4.499
  • Hiemenz JW, Raad II, Maertens JA, et al. Efficacy of caspofungin as salvage therapy for invasive aspergillosis compared to standard therapy in a historical cohort. Eur J Clin Microbiol Infect Dis. 2010;29(11):1387–1394. doi: 10.1007/s10096-010-1013-0
  • Aguado JM, Varo E, Usetti P, et al. Safety of anidulafungin in solid organ transplant recipients. Liver Transpl. 2012;18(6):680–685. doi: 10.1002/lt.23410
  • Winkler M, Pratschke J, Schulz U, et al. Caspofungin for post solid organ transplant invasive fungal disease: results of a retrospective observational study. Transpl Infect Dis. 2010;12(3):230–237. doi: 10.1111/j.1399-3062.2009.00490.x
  • Petrovic J, Ngai A, Bradshaw S, et al. Efficacy and safety of caspofungin in solid organ transplant recipients. Transplant Proc. 2007;39(10):3117–3120. doi: 10.1016/j.transproceed.2007.10.003
  • Groetzner J, Kaczmarek I, Wittwer T, et al. Caspofungin as first-line therapy for the treatment of invasive aspergillosis after thoracic organ transplantation. J Heart Lung Transplant. 2008;27(1):1–6. doi: 10.1016/j.healun.2007.10.002
  • Keating G, Figgitt D. Caspofungin: a review of its use in oesophageal candidiasis, invasive candidiasis and invasive aspergillosis. Drugs. 2003;63(20):2235–2263. doi: 10.2165/00003495-200363200-00008
  • Pettit NN, Carver PL. Isavuconazole: a new option for the management of invasive fungal infections. Ann Pharmacother. 2015;49(7):825–842. doi: 10.1177/1060028015581679
  • Owusu Obeng A, Egelund EF, Alsultan A, et al. CYP2C19 polymorphisms and therapeutic drug monitoring of voriconazole: are we ready for clinical implementation of pharmacogenomics? Pharmacotherapy. 2014;34(7):703–718. doi: 10.1002/phar.1400
  • Wu X, Clancy CJ, Rivosecchi RM, et al. Pharmacokinetics of intravenous isavuconazole in solid-organ transplant recipients. Antimicrob Agents Chemother. 2018;62(12). doi: 10.1128/AAC.01643-18
  • Kim SH, Kwon JC, Park C, et al. Therapeutic drug monitoring and safety of intravenous voriconazole formulated with sulfobutylether beta-cyclodextrin in haematological patients with renal impairment. Mycoses. 2016;59(10):644–651. doi: 10.1111/myc.12517
  • Maertens JA, Raad II, Marr KA, et al. Isavuconazole versus voriconazole for primary treatment of invasive mould disease caused by aspergillus and other filamentous fungi (SECURE): a phase 3, randomised-controlled, non-inferiority trial. Lancet. 2016;387(10020):760–769. doi: 10.1016/S0140-6736(15)01159-9
  • Fernandez-Ruiz M, Bodro M, Gutierrez Martin I, et al. Isavuconazole for the treatment of invasive mold disease in solid organ transplant recipients: a multicenter study on efficacy and safety in real-life clinical practice. Transplantation. 2023;107(3):762–773. doi: 10.1097/TP.0000000000004312
  • Monforte A, Los-Arcos I, Martin-Gomez MT, et al. Safety and effectiveness of isavuconazole treatment for fungal infections in solid organ transplant recipients (ISASOT study). Microbiol Spectr. 2022;10(1):e0178421. doi: 10.1128/spectrum.01784-21
  • Maertens JA, Rahav G, Lee DG, et al. Posaconazole versus voriconazole for primary treatment of invasive aspergillosis: a phase 3, randomised, controlled, non-inferiority trial. Lancet. 2021;397(10273):499–509. doi: 10.1016/S0140-6736(21)00219-1
  • Kersemaekers WM, Dogterom P, Xu J, et al. Effect of a high‐fat meal on the pharmacokinetics of 300‐milligram posaconazole in a solid oral tablet formulation. Antimicrob Agents Chemother. 2015;59(6):3385–3389. doi: 10.1128/AAC.05000-14
  • Krishna G, Moton A, Ma L, et al. Effects of oral posaconazole on the pharmacokinetic properties of oral and intravenous midazolam: a phase I, randomized, open-label, crossover study in healthy volunteers. Clin Ther. 2009;31(2):286–298. doi: 10.1016/j.clinthera.2009.02.022
  • Gu TM, Lewis JS, Le H, et al. Comparative effects of fluconazole, posaconazole, and isavuconazole upon tacrolimus and cyclosporine serum concentrations. J Oncol Pharm Pract. 2022;28(6):1357–1362. doi: 10.1177/10781552211029046
  • Chanoine S, Gautier-Veyret E, Pluchart H, et al. Tablets or oral suspension for posaconazole in lung transplant recipients? Consequences for trough concentrations of tacrolimus and everolimus. Br J Clin Pharmacol. 2021;87(2):427–435. doi: 10.1111/bcp.14398
  • Cornely OA, Alastruey-Izquierdo A, Arenz D, et al. Global guideline for the diagnosis and management of mucormycosis: an initiative of the European confederation of medical mycology in cooperation with the mycoses study group education and research consortium. Lancet Infect Dis. 2019;19(12):e405–e421. doi: 10.1016/S1473-3099(19)30312-3
  • Linden P, Williams P, Chan KM. Efficacy and safety of amphotericin B lipid complex injection (ABLC) in solid-organ transplant recipients with invasive fungal infections. Clin Transplant. 2000;14(4 Pt 1):329–339. doi: 10.1034/j.1399-0012.2000.140409.x
  • Forrest GN, Mankes K. Outcomes of invasive zygomycosis infections in renal transplant recipients. Transpl Infect Dis. 2007;9(2):161–164. doi: 10.1111/j.1399-3062.2006.00197.x
  • Sun HY, Forrest G, Gupta KL, et al. Rhino-orbital-cerebral zygomycosis in solid organ transplant recipients. Transplantation. 2010;90(1):85–92. doi: 10.1097/TP.0b013e3181dde8fc
  • Sun HY, Aguado JM, Bonatti H, et al. Pulmonary zygomycosis in solid organ transplant recipients in the current era. Am J Transplant. 2009;9(9):2166–2171. doi: 10.1111/j.1600-6143.2009.02754.x
  • Husain S, Alexander BD, Munoz P, et al. Opportunistic mycelial fungal infections in organ transplant recipients: emerging importance of non-Aspergillus mycelial fungi. Clin Infect Dis. 2003;37(2):221–229. doi: 10.1086/375822
  • Park BJ, Pappas PG, Wannemuehler KA, et al. Invasive non-aspergillus mold infections in transplant recipients, United States, 2001-2006. Emerg Infect Dis. 2011;17(10):1855–1864. doi: 10.3201/eid1710.110087
  • Song Y, Qiao J, Giovanni G, et al. Mucormycosis in renal transplant recipients: review of 174 reported cases. BMC Infect Dis. 2017;17(1):283. doi: 10.1186/s12879-017-2381-1
  • Coste A, Conrad A, Porcher R, et al. Improving diagnosis of pulmonary mucormycosis: leads from a contemporary national study of 114 cases. Chest. 2023;164(5):S0012–3692(23)00946–7. doi: 10.1016/j.chest.2023.06.039
  • Bansal SB, Rana A, Babras M, et al. Risk factors and outcomes of COVID associated mucormycosis in kidney transplant recipients. Transpl Infect Dis. 2022;24(2):e13777. doi: 10.1111/tid.13777
  • Meshram HS, Kute VB, Chauhan S, et al. Mucormycosis in post-COVID-19 renal transplant patients: a lethal complication in follow-up. Transpl Infect Dis. 2021;23(4):e13663. doi: 10.1111/tid.13663
  • Tobon AM, Arango M, Fernandez D, et al. Mucormycosis (zygomycosis) in a heart-kidney transplant recipient: recovery after posaconazole therapy. Clin Infect Dis. 2003;36(11):1488–1491. doi: 10.1086/375075
  • Deyo JC, Nicolsen N, Lachiewicz A, et al. Salvage treatment of mucormycosis post-liver transplant with posaconazole during sirolimus maintenance immunosuppression. J Pharm Pract. 2017;30(2):261–265. doi: 10.1177/0897190016628702
  • Gani I, Doroodchi A, Falkenstrom K, et al. Gastric mucormycosis in a renal transplant patient treated with isavuconazole monotherapy. Case Rep Transplant. 2019;2019:9839780. doi: 10.1155/2019/9839780
  • Hoellinger B, Magnus L, Ruch Y, et al. Case report and literature review of prosthetic cardiovascular mucormycosis. Emerg Infect Dis. 2023;29(11):2388–2390. doi: 10.3201/eid2911.230837
  • Klimova K, Padilla Suarez C, Pelaez T, et al. Cutaneous mucormycosis as a rare complication of a liver transplantation. Enferm Infec Microbiol Clin. 2014;32(8):537–539. in Spanish. doi: 10.1016/j.eimc.2014.05.007
  • Abboud CS, Bergamasco MD, Baia CE, et al. Case report of hepatic mucormycosis after liver transplantation: successful treatment with liposomal amphotericin B followed by posaconazole sequential therapy. Transplant Proc. 2012;44(8):2501–2502. doi: 10.1016/j.transproceed.2012.07.042
  • Martin MS, Smith AA, Lobo M, et al. Successful treatment of recurrent pulmonary mucormycosis in a renal transplant patient: a case report and literature review. Case Rep Transplant. 2017;2017:1925070. doi: 10.1155/2017/1925070
  • Greenberg RN, Mullane K, van Burik JA, et al. Posaconazole as salvage therapy for zygomycosis. Antimicrob Agents Chemother. 2006;50(1):126–133. doi: 10.1128/AAC.50.1.126-133.2006
  • Wand O, Unterman A, Izhakian S, et al. Mucormycosis in lung transplant recipients: a systematic review of the literature and a case series. Clin Transplant. 2020;34(2):e13774. doi: 10.1111/ctr.13774
  • Marty FM, Ostrosky-Zeichner L, Cornely OA, et al. Isavuconazole treatment for mucormycosis: a single-arm open-label trial and case-control analysis. Lancet Infect Dis. 2016;16(7):828–837. doi: 10.1016/S1473-3099(16)00071-2
  • Panackal AA. Combination antifungal therapy for invasive aspergillosis revisited. Med Mycol Open Access. 2016;2(2). doi: 10.21767/2471-8521.100012
  • Marr KA, Schlamm HT, Herbrecht R, et al. Combination antifungal therapy for invasive aspergillosis: a randomized trial. Ann Intern Med. 2015;162(2):81–89. doi: 10.7326/M13-2508
  • Raad II, Zakhem AE, Helou GE, et al. Clinical experience of the use of voriconazole, caspofungin or the combination in primary and salvage therapy of invasive aspergillosis in haematological malignancies. Int J Antimicrob Agents. 2015;45(3):283–288. doi: 10.1016/j.ijantimicag.2014.08.012
  • Wattier RL, Dvorak CC, Hoffman JA, et al. A prospective, international cohort study of invasive mold infections in children. J Pediatric Infect Dis Soc. 2015;4(4):313–322. doi: 10.1093/jpids/piu074
  • Munoz P, Singh N, Bouza E. Treatment of solid organ transplant patients with invasive fungal infections: should a combination of antifungal drugs be used? Curr Opin Infect Dis. 2006;19(4):365–370.
  • Singh N, Limaye AP, Forrest G, et al. Combination of voriconazole and caspofungin as primary therapy for invasive aspergillosis in solid organ transplant recipients: a prospective, multicenter, observational study. Transplantation. 2006;81(3):320–326. doi: 10.1097/01.tp.0000202421.94822.f7
  • Spellberg B, Fu Y, Edwards JE Jr., et al. Combination therapy with amphotericin B lipid complex and caspofungin acetate of disseminated zygomycosis in diabetic ketoacidotic mice. Antimicrob Agents Chemother. 2005;49(2):830–832. doi: 10.1128/AAC.49.2.830-832.2005
  • Ibrahim AS, Gebremariam T, Fu Y, et al. Combination echinocandin-polyene treatment of murine mucormycosis. Antimicrob Agents Chemother. 2008;52(4):1556–1558. doi: 10.1128/AAC.01458-07
  • Reed C, Bryant R, Ibrahim AS, et al. Combination polyene-caspofungin treatment of rhino-orbital-cerebral mucormycosis. Clin Infect Dis. 2008;47(3):364–371. doi: 10.1086/589857
  • Abidi MZ, Sohail MR, Cummins N, et al. Stability in the cumulative incidence, severity and mortality of 101 cases of invasive mucormycosis in high-risk patients from 1995 to 2011: a comparison of eras immediately before and after the availability of voriconazole and echinocandin-amphotericin combination therapies. Mycoses. 2014;57(11):687–698. doi: 10.1111/myc.12222
  • Rodriguez MM, Serena C, Marine M, et al. Posaconazole combined with amphotericin B, an effective therapy for a murine disseminated infection caused by rhizopus oryzae. Antimicrob Agents Chemother. 2008;52(10):3786–3788. doi: 10.1128/AAC.00628-08
  • Gebremariam T, Gu Y, Singh S, et al. Combination treatment of liposomal amphotericin B and isavuconazole is synergistic in treating experimental mucormycosis. J Antimicrob Chemother. 2021;76(10):2636–2639. doi: 10.1093/jac/dkab233
  • Patel A, Agarwal R, Rudramurthy SM, et al. Multicenter epidemiologic study of coronavirus disease-associated mucormycosis, India. Emerg Infect Dis. 2021;27(9):2349–2359. doi: 10.3201/eid2709.210934
  • Groll AH, Townsend R, Desai A, et al. Drug-drug interactions between triazole antifungal agents used to treat invasive aspergillosis and immunosuppressants metabolized by cytochrome P450 3A4. Transpl Infect Dis. 2017;19(5). doi: 10.1111/tid.12751
  • Saeki T, Ueda K, Tanigawara Y, et al. Human P-glycoprotein transports cyclosporin a and FK506. J Biol Chem. 1993;268(9):6077–6080. doi: 10.1016/S0021-9258(18)53221-X
  • Marfo K, Altshuler J, Lu A. Tacrolimus pharmacokinetic and pharmacogenomic differences between adults and pediatric solid organ transplant recipients. Pharmaceutics. 2010;2(3):291–299. doi: 10.3390/pharmaceutics2030291
  • Hesselink DA, Bouamar R, Elens L, et al. The role of pharmacogenetics in the disposition of and response to tacrolimus in solid organ transplantation. Clin Pharmacokinet. 2014;53(2):123–139. doi: 10.1007/s40262-013-0120-3
  • Brunet M, van Gelder T, Asberg A, et al. Therapeutic drug monitoring of tacrolimus-personalized therapy: second consensus report. Ther Drug Monit. 2019;41(3):261–307. doi: 10.1097/FTD.0000000000000640
  • Rivosecchi RM, Samanta P, Demehin M, et al. Pharmacokinetics of azole antifungals in cystic fibrosis. Mycopathologia. 2018;183(1):139–150. doi: 10.1007/s11046-017-0189-6
  • Schulz J, Kluwe F, Mikus G, et al. Novel insights into the complex pharmacokinetics of voriconazole: a review of its metabolism. Drug Metab Rev. 2019;51(3):247–265. doi: 10.1080/03602532.2019.1632888
  • Hohmann N, Kocheise F, Carls A, et al. Dose-dependent bioavailability and CYP3A inhibition contribute to non-linear pharmacokinetics of voriconazole. Clin Pharmacokinet. 2016;55(12):1535–1545. doi: 10.1007/s40262-016-0416-1
  • Jeong S, Nguyen PD, Desta Z. Comprehensive in vitro analysis of voriconazole inhibition of eight cytochrome P450 (CYP) enzymes: major effect on CYPs 2B6, 2C9, 2C19, and 3A. Antimicrob Agents Chemother. 2009;53(2):541–551. doi: 10.1128/AAC.01123-08
  • Saari TI, Laine K, Leino K, et al. Effect of voriconazole on the pharmacokinetics and pharmacodynamics of intravenous and oral midazolam. Clin Pharmacol Ther. 2006;79(4):362–370. doi: 10.1016/j.clpt.2005.12.305
  • Tintillier M, Kirch L, Goffin E, et al. Interaction between voriconazole and tacrolimus in a kidney-transplanted patient. Nephrol Dial Transplant. 2005;20(3):664–665. doi: 10.1093/ndt/gfh593
  • Capone D, Tarantino G, Gentile A, et al. Effects of voriconazole on tacrolimus metabolism in a kidney transplant recipient. J Clin Pharm Ther. 2010;35(1):121–124. doi: 10.1111/j.1365-2710.2009.01070.x
  • Food and Drug Administration (FDA). Pfizer Inc. VFEND® (voriconazole) prescribing information. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2022/208562s006lbl.pdf
  • Mori T, Kato J, Yamane A, et al. Drug interaction between voriconazole and tacrolimus and its association with the bioavailability of oral voriconazole in recipients of allogeneic hematopoietic stem cell transplantation. Int J Hematol. 2012;95(5):564–569. doi: 10.1007/s12185-012-1057-2
  • Vanhove T, Bouwsma H, Hilbrands L, et al. Determinants of the magnitude of interaction between tacrolimus and voriconazole/posaconazole in solid organ recipients. Am J Transplant. 2017;17(9):2372–2380. doi: 10.1111/ajt.14232
  • Outeda Macias M, Salvador Garrido P, Elberdin Pazos L, et al. Management of everolimus and voriconazole interaction in lung transplant patients. Ther Drug Monit. 2016;38(3):305–312. doi: 10.1097/FTD.0000000000000294
  • Mathis AS, Shah NK, Friedman GS. Combined use of sirolimus and voriconazole in renal transplantation: a report of two cases. Transplant Proc. 2004;36(9):2708–2709. doi: 10.1016/j.transproceed.2004.09.043
  • Surowiec D, Depestel DD, Carver PL. Concurrent administration of sirolimus and voriconazole: a pilot study assessing safety and approaches to appropriate management. Pharmacotherapy. 2008;28(6):719–729. doi: 10.1592/phco.28.6.719
  • Townsend R, Dietz A, Hale C, et al. Pharmacokinetic evaluation of CYP3A4-mediated drug-drug interactions of isavuconazole with rifampin, ketoconazole, midazolam, and ethinyl estradiol/norethindrone in healthy adults. Clin Pharmacol Drug Dev. 2017;6(1):44–53. doi: 10.1002/cpdd.285
  • Kieu V, Jhangiani K, Dadwal S, et al. Effect of isavuconazole on tacrolimus and sirolimus serum concentrations in allogeneic hematopoietic stem cell transplant patients: a drug-drug interaction study. Transpl Infect Dis. 2019;21(1):e13007. doi: 10.1111/tid.13007
  • Food and Drug Administration (FDA). Pfizer Inc. CRESEMBA® (isavuconazonium sulfate) prescribing information. Available from: https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/207500orig1s000lbl.pdf
  • Kufel WD, Armistead PM, Daniels LM, et al. Drug-drug interaction between isavuconazole and tacrolimus: is empiric dose adjustment necessary? J Pharm Pract. 2020;33(2):226–230. doi: 10.1177/0897190018790688
  • Mitsani D, Nguyen MH, Shields RK, et al. Prospective, observational study of voriconazole therapeutic drug monitoring among lung transplant recipients receiving prophylaxis: factors impacting levels of and associations between serum troughs, efficacy, and toxicity. Antimicrob Agents Chemother. 2012;56(5):2371–2377. doi: 10.1128/AAC.05219-11
  • Hashemizadeh Z, Badiee P, Malekhoseini SA, et al. Observational study of associations between voriconazole therapeutic drug monitoring, toxicity, and outcome in liver transplant patients. Antimicrob Agents Chemother. 2017;61(12). doi: 10.1128/AAC.01211-17
  • Luong ML, Hosseini-Moghaddam SM, Singer LG, et al. Risk factors for Voriconazole Hepatotoxicity at 12 weeks in lung transplant recipients. Am J Transplant. 2012;12(7):1929–1935. doi: 10.1111/j.1600-6143.2012.04042.x
  • Butler-Laporte G, Langevin MC, Lemieux C, et al. Voriconazole therapeutic drug monitoring among lung transplant recipients receiving targeted therapy for invasive aspergillosis. Clin Transplant. 2022;36(8):e14709. doi: 10.1111/ctr.14709
  • Crone CG, Wulff SM, Helweg-Larsen J, et al. Adverse events associated with universal versus targeted antifungal prophylaxis among lung transplant recipients—A nationwide cohort study 2010–2019. Microorganisms. 2022;10(12):2478. doi: 10.3390/microorganisms10122478
  • Luong ML, Al-Dabbagh M, Groll AH, et al. Utility of voriconazole therapeutic drug monitoring: a meta-analysis. J Antimicrob Chemother. 2016;71(7):1786–1799. doi: 10.1093/jac/dkw099
  • Zhao YC, Lin XB, Zhang BK, et al. Predictors of adverse events and determinants of the voriconazole trough concentration in kidney transplantation recipients. Clin Transl Sci. 2021;14(2):702–711. doi: 10.1111/cts.12932
  • Ilyas M, Colegio OR, Kaplan B, et al. Cutaneous toxicities from transplantation-related medications. Am J Transplant. 2017;17(11):2782–2789. doi: 10.1111/ajt.14337
  • D’Arcy ME, Pfeiffer RM, Rivera DR, et al. Voriconazole and the risk of keratinocyte carcinomas among lung transplant recipients in the United States. JAMA Dermatol. 2020;156(7):772–779. doi: 10.1001/jamadermatol.2020.1141
  • Hamandi B, Fegbeutel C, Silveira FP, et al. Voriconazole and squamous cell carcinoma after lung transplantation: A multicenter study. Am J Transplant. 2018;18(1):113–124. doi: 10.1111/ajt.14500
  • Kolaitis NA, Duffy E, Zhang A, et al. Voriconazole increases the risk for cutaneous squamous cell carcinoma after lung transplantation. Transplant Int. 2017;30(1):41–48. doi: 10.1111/tri.12865
  • Epaulard O, Villier C, Ravaud P, et al. A multistep voriconazole-related phototoxic pathway may lead to skin carcinoma: results from a French nationwide study. Clin Infect Dis. 2013;57(12):e182–188. doi: 10.1093/cid/cit600
  • Wermers RA, Cooper K, Razonable RR, et al. Fluoride excess and periostitis in transplant patients receiving long-term voriconazole therapy. Clin Infect Dis. 2011;52(5):604–611. doi: 10.1093/cid/ciq188
  • Wang TF, Wang T, Altman R, et al. Periostitis secondary to prolonged voriconazole therapy in lung transplant recipients. Am J Transplant. 2009;9(12):2845–2850. doi: 10.1111/j.1600-6143.2009.02837.x
  • Ayub A, Kenney CV, McKiernan FE. Multifocal nodular periostitis associated with prolonged voriconazole therapy in a lung transplant recipient. J Clin Rheumatol. 2011;17(2):73–75. doi: 10.1097/RHU.0b013e31820aff12
  • Wise SM, Wilson MA. A case of periostitis secondary to voriconazole therapy in a heart transplant recipient. Clin Nucl Med. 2011;36(3):242–244. doi: 10.1097/RLU.0b013e31820902d8
  • Sircar M, Kotton C, Wojciechowski D, et al. Voriconazole-induced periostitis & enthesopathy in solid organ transplant patients: case reports. J Biosci Med (Irvine). 2016;4(11):8–17. doi: 10.4236/jbm.2016.411002
  • Bennett MJ, Balcerek MI, Lewis EA, et al. Voriconazole-Associated Periostitis: new insights into pathophysiology and management. JBMR Plus. 2022;6(2):e10557. doi: 10.1002/jbm4.10557
  • Li H, Zhang M, Jiao X, et al. Using disproportionality analysis to explore the association between periostitis and triazole antifungals in the FDA adverse event reporting system database. Sci Rep. 2023;13(1):4475. doi: 10.1038/s41598-023-27687-0
  • Orssaud C, Guillemain R, Lillo Le Louet A. Toxic optic neuropathy due to voriconazole: possible potentiation by reduction of CYP2C19 activity. Eur Rev Med Pharmacol Sci. 2021;25(24):7823–7828. doi: 10.26355/eurrev_202112_27628
  • Assaf A, Faure E, Sermet K, et al. Successful treatment of Aspergillus fumigatus sternal osteomyelitis with isavuconazole in a heart transplant recipient. Transpl Infect Dis. 2020;22(5):e13313. doi: 10.1111/tid.13313
  • Soliman M, Akanbi O, Harding C, et al. Voriconazole-induced myositis in a double lung transplant recipient. Cureus. 2019;11(2):e3998. doi: 10.7759/cureus.3998
  • Trang TP, Hanretty AM, Langelier C, et al. Use of isavuconazole in a patient with voriconazole-induced QTc prolongation. Transpl Infect Dis. 2017;19(4). doi: 10.1111/tid.12712
  • Batista MV, Ussetti MP, Jiang Y, et al. Comparing the real-world use of isavuconazole to other anti-fungal therapy for invasive fungal infections in patients with and without underlying disparities: a multi-center retrospective study. J Fungi. 2023;9(2):166. doi: 10.3390/jof9020166
  • Ordaya EE, Alangaden GJ. Real-life use of Isavuconazole in patients intolerant to other azoles. Clin Infect Dis. 2016;63(11):1529–1530. doi: 10.1093/cid/ciw585
  • Hassouna H, Athans V, Brizendine KD. Real-world use-Isavuconazole at a large academic medical center. Mycoses. 2019;62(6):534–541. doi: 10.1111/myc.12910
  • Kato H, Hagihara M, Asai N, et al. A systematic review and meta-analysis of efficacy and safety of isavuconazole for the treatment and prophylaxis of invasive fungal infections. Mycoses. 2023;66(9):815–824. doi: 10.1111/myc.13622
  • DiPippo AJ, Kontoyiannis DP. Lack of toxicity with Long-term isavuconazole use in patients with hematologic malignancy. Clin Infect Dis. 2019;69(9):1624–1627. doi: 10.1093/cid/ciz159
  • Lauruschkat CD, Einsele H, Loeffler J. Immunomodulation as a therapy for aspergillus infection: current status and future perspectives. J Fungi. 2018;4(4):137. doi: 10.3390/jof4040137
  • German CA, Liao JK. Understanding the molecular mechanisms of statin pleiotropic effects. Arch Toxicol. 2023;97(6):1529–1545. doi: 10.1007/s00204-023-03492-6
  • Tavakkoli A, Johnston TP, Sahebkar A. Antifungal effects of statins. Pharmacol Ther. 2020;208:107483. doi: 10.1016/j.pharmthera.2020.107483
  • Villalobos AP, Foroutan F, Davoudi S, et al. Statin use may be associated with a lower risk of invasive aspergillosis in lung transplant recipients. Clin Infect Dis. 2023;76(3):e1379–e1384. doi: 10.1093/cid/ciac551
  • Majima H, Arai T, Kamei K, et al. In vivo efficacy of pitavastatin combined with itraconazole against Aspergillus fumigatus in silkworm models. Microbiol Spectr. 2023;11(5):e0266623. doi: 10.1128/spectrum.02666-23
  • Lauruschkat C, Einsele H, Loeffler J. Immunomodulation as a therapy for Aspergillus infection: Current status and future perspectives. J Fungi. 2018;4(4):137. doi: 10.3390/jof4040137
  • Armstrong-James D, Teo IA, Shrivastava S, et al. Exogenous interferon-gamma immunotherapy for invasive fungal infections in kidney transplant patients. Am J Transplant. 2010;10(8):1796–1803. doi: 10.1111/j.1600-6143.2010.03094.x
  • Estrada C, Desai AG, Chirch LM, et al. Invasive aspergillosis in a renal transplant recipient successfully treated with interferon-gamma. Case Rep Transplant. 2012;2012:493758. doi: 10.1155/2012/493758
  • Summers SA, Dorling A, Boyle JJ, et al. Cure of disseminated cryptococcal infection in a renal allograft recipient after addition of gamma-interferon to anti-fungal therapy. Am J Transplant. 2005;5(8):2067–2069. doi: 10.1111/j.1600-6143.2005.00947.x
  • Thomson AW, Bonham CA, Zeevi A. Mode of action of tacrolimus (FK506): molecular and cellular mechanisms. Ther Drug Monit. 1995;17(6):584–591. doi: 10.1097/00007691-199512000-00007
  • Steinbach WJ, Singh N, Miller JL, et al. In vitro interactions between antifungals and immunosuppressants against Aspergillus fumigatus Isolates from transplant and nontransplant patients. Antimicrob Agents Chemother. 2004;48(12):4922–4925. doi: 10.1128/AAC.48.12.4922-4925.2004
  • Juvvadi PR, Lee SC, Heitman J, et al. Calcineurin in fungal virulence and drug resistance: Prospects for harnessing targeted inhibition of calcineurin for an antifungal therapeutic approach. Virulence. 2017;8(2):186–197. doi: 10.1080/21505594.2016.1201250
  • Gao L, Sun Y. In vitro interactions of antifungal agents and tacrolimus against Aspergillus biofilms. Antimicrob Agents Chemother. 2015;59(11):7097–7099. doi: 10.1128/AAC.01510-15
  • Schwarz P, Dannaoui E. In vitro interaction between Isavuconazole and tacrolimus, cyclosporin a, or sirolimus against aspergillus species. J Fungi. 2020;6(3):103. doi: 10.3390/jof6030103
  • Sun S, Li Y, Guo Q, et al. In vitro interactions between tacrolimus and azoles against Candida albicans determined by different methods. Antimicrob Agents Chemother. 2008;52(2):409–417. doi: 10.1128/AAC.01070-07
  • Rossato L, Venturini TP, de Azevedo MI, et al. In vitro activity of immunosuppressive agents against Cryptococcus neoformans. Enferm Infecc Microbiol Clin (Engl Ed). 2022;40(2):86–88. doi: 10.1016/j.eimc.2020.09.014
  • Steinbach WJ, Schell WA, Blankenship JR, et al. In vitro interactions between antifungals and immunosuppressants against aspergillus fumigatus. Antimicrob Agents Chemother. 2004;48(5):1664–1669. doi: 10.1128/AAC.48.5.1664-1669.2004
  • Singh N, Avery RK, Munoz P, et al. Trends in risk profiles for and mortality associated with invasive aspergillosis among liver transplant recipients. Clin Infect Dis. 2003;36(1):46–52. doi: 10.1086/345441
  • Terrec F, Jouve T, Malvezzi P, et al. Belatacept use after kidney transplantation and its effects on risk of infection and COVID-19 vaccine response. J Clin Med. 2021;10(21):5159. doi: 10.3390/jcm10215159
  • McGaha T, Murphy JW, Mansfield JM. CTLA-4 down-regulates the protective anticryptococcal cell-mediated immune response. Infect Immun. 2000;68(8):4624–4630. doi: 10.1128/IAI.68.8.4624-4630.2000
  • Roussey JA, Viglianti SP, Teitz-Tennenbaum S, et al. Anti-PD-1 antibody treatment promotes clearance of persistent cryptococcal lung infection in mice. J Immunol. 2017;199(10):3535–3546. doi: 10.4049/jimmunol.1700840
  • Wurster S, Watowich SS, Kontoyiannis DP. Checkpoint inhibitors as immunotherapy for fungal infections: promises, challenges, and unanswered questions. Front Immunol. 2022;13:1018202.
  • Vu CTB, Thammahong A, Yagita H, et al. Blockade of PD-1 attenuated postsepsis aspergillosis via the activation of IFN-gamma and the dampening of IL-10. Shock. 2020;53(4):514–524. doi: 10.1097/SHK.0000000000001392
  • Wurster S, Robinson P, Albert ND, et al. Protective activity of programmed cell death protein 1 blockade and synergy with caspofungin in a murine invasive pulmonary aspergillosis model. J Infect Dis. 2020;222(6):989–994. doi: 10.1093/infdis/jiaa264
  • Wurster S, Albert ND, Bharadwaj U, et al. Blockade of the PD-1/PD-L1 immune checkpoint pathway improves infection outcomes and enhances fungicidal host defense in a murine model of invasive pulmonary mucormycosis. Front Immunol. 2022;13:838344. doi: 10.3389/fimmu.2022.838344
  • Grimaldi D, Pradier O, Hotchkiss RS, et al. Nivolumab plus interferon-gamma in the treatment of intractable mucormycosis. Lancet Infect Dis. 2017;17(1):18. doi: 10.1016/S1473-3099(16)30541-2
  • Banck JC, Mueller N, Mellinghoff SC, et al. Immune checkpoint blockade for aspergillosis and Mucormycosis Coinfection. Hemasphere. 2021;5(3):e530. doi: 10.1097/HS9.0000000000000530
  • Khatamzas E, Mellinghoff SC, Thelen M, et al. Nivolumab induces long-term remission in a patient with fusariosis. Eur J Cancer. 2022;173:91–94. doi: 10.1016/j.ejca.2022.06.035
  • Serris A, Ouedrani A, Uhel F, et al. Case report: immune checkpoint blockade plus interferon-gamma add-on antifungal therapy in the treatment of refractory Covid-associated pulmonary aspergillosis and cerebral mucormycosis. Front Immunol. 2022;13:900522. doi: 10.3389/fimmu.2022.900522
  • Lukaszewicz AC, Venet F, Boibieux A, et al. Nivolumab and interferon-gamma rescue therapy to control mixed mould and bacterial superinfection after necrotizing fasciitis and septic shock. Med Mycol Case Rep. 2022;37:19–22. doi: 10.1016/j.mmcr.2022.06.003
  • Zhang P, Zhu G, Li L, et al. Immune checkpoint inhibitor therapy for malignant tumors in liver transplantation recipients: a systematic review of the literature. Transplant Rev (Orlando). 2022;36(4):100712. doi: 10.1016/j.trre.2022.100712
  • Tio M, Rai R, Ezeoke OM, et al. Anti-PD-1/PD-L1 immunotherapy in patients with solid organ transplant, HIV or hepatitis B/C infection. Eur J Cancer. 2018;104:137–144. doi: 10.1016/j.ejca.2018.09.017
  • Abdel-Wahab N, Safa H, Abudayyeh A, et al. Checkpoint inhibitor therapy for cancer in solid organ transplantation recipients: an institutional experience and a systematic review of the literature. J Immunother Cancer. 2019;7(1):106. doi: 10.1186/s40425-019-0585-1
  • Benedict K, Gold JAW, Toda M, et al. Low rates of antifungal therapeutic drug monitoring among inpatients who received itraconazole, posaconazole, or voriconazole, United States, 2019-2021. Open Forum Infect Dis. 2023;10(8):ofad389. doi: 10.1093/ofid/ofad389
  • Höhl R, Bertram R, Kinzig M, et al. Isavuconazole therapeutic drug monitoring in critically ill ICU patients: a monocentric retrospective analysis. Mycoses. 2022;65(7):747–752. doi: 10.1111/myc.13469
  • De Francesco MA. Drug-resistant aspergillus spp: a literature review of its resistance mechanisms and its prevalence in Europe. Pathogens. 2023;12(11):1305. doi: 10.3390/pathogens12111305
  • Pfaller MA, Carvalhaes CG, Rhomberg PR, et al. Trends in the activity of mold-active azole agents against aspergillus fumigatus clinical isolates with and without cyp51 alterations from Europe and North America (2017–2021). J Clin Microbiol. 2024 Jan;9(2):e0114123. epub ahead of print. doi: 10.1128/jcm.01141-23
  • Gioia F, Filigheddu E, Corbella L, et al. Invasive aspergillosis in solid organ transplantation: diagnostic challenges and differences in outcome in a Spanish national cohort (diaspersot study). Mycoses. 2021;64(11):1334–1345. doi: 10.1111/myc.13298
  • Redondo N, Navarro D, Aguado JM, et al. Viruses, friends, and foes: the case of torque teno virus and the net state of immunosuppression. Transpl Infect Dis. 2022;24(2):e13778. doi: 10.1111/tid.13778
  • Lamoth F, Lewis RE, Kontoyiannis DP. Investigational antifungal agents for invasive mycoses: a clinical perspective. Clin Infect Dis. 2022;75(3):534–544. doi: 10.1093/cid/ciab1070
  • Gintjee TJ, Donnelley MA, Thompson GR. 3rd. Aspiring antifungals: review of current antifungal pipeline developments. J Fungi. 2020;6(1):28. doi: 10.3390/jof6010028
  • Faure E, Brugiere O, de Verdiere SC, et al. Refractory microascus bronchopulmonary infection treated with olorofim, France. Emerg Infect Dis. 2023;29(11):2401–2403. doi: 10.3201/eid2911.230984

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.