What is the evidence to support or refute an interaction between cyclophosphamide and azole antifungals?

Comment by InpharmD Researcher

Clinical data show notable increases in cyclophosphamide (and metabolite) levels when co-administered with triazole antifungals, primarily via inhibition/competition of CYP2B6, CYP3A4/5, CYP2C9, and/or CYP2A6. Interactions with P-gp and other drug transporters further complicate this interaction. Studies of posaconazole with cyclophosphamide-based therapy can be found in Tables 4-5, suggesting safe use with judicious monitoring.

Background

Cyclophosphamide (CY) is a prodrug metabolized primarily via CYP2B6, CYP3A4/5, CYP2C9, and CYP2A6; it is widely used in chemotherapy regimens, which may necessitate antifungal prophylaxis in immunocompromised patients. Inhibition of CYP3A4 and CYP2C9 by triazoles raises concerns about potential drug-drug interactions (DDIs) that could alter cyclophosphamide metabolism, leading to increased toxicity. Ketoconazole, known for its robust inhibitory effects on CYP3A4 and CYP3A5, notably increases the plasma exposure of cyclophosphamide by dampening its CYP3A-mediated metabolism, more so than itraconazole, which has a milder inhibitory effect on CYP3A4. Fluconazole, a potent competitive inhibitor of CYP2C9 and CYP2C19 but a weak inhibitor of CYP3A4, exhibits limited influence on the pharmacokinetics of cyclophosphamide compared to the other two triazoles. Additionally, cyclophosphamide's altered plasma exposure may be further complicated by its interaction with P-glycoprotein (P-gp), an efflux transporter that affects drug absorption, distribution, metabolism, and excretion, and is implicated in cancer multidrug resistance. Inhibition of P-gp by ketoconazole could contribute to increased cyclophosphamide accumulation. [1], [2], [3]

A 2004 trial (Table 1) randomized patients undergoing allogeneic stem cell transplantation (SCT) to either itraconazole (200 mg IV daily or 2.5 mg/kg PO TID) or fluconazole (400 mg IV or PO daily), starting with conditioning therapy and continuing for at least 120 days post-transplant. After an interim review by a data and safety monitoring board, patients receiving itraconazole demonstrated higher serum bilirubin and creatinine levels, particularly within the first 20 days post-SCT, and most notably in those also receiving CY-based conditioning. Subsequent pharmacokinetic analyses assessed a subset of patients, revealing that itraconazole recipients had increased exposure to the active CY metabolite 4-hydroxycyclophosphamide (HCY) and its downstream products, including keto-cyclophosphamide (ketoCY) and carboxyethylphosphoramide mustard (CEPM). In contrast, fluconazole recipients exhibited increased exposure to CY and deschloroethyl-cyclophosphamide (DCCY), suggesting differential modulation of CY metabolism by these azole antifungals. A concurrent analysis of 149 patients showed patients receiving fluconazole had significantly higher CY (p=0.0065) and DCCY (p=0.007) exposure, whereas those given itraconazole exhibited a 20% increase in CY clearance (p=0.007) and markedly elevated HCY (p<0.001) and ketoCY (p<0.001) exposure. The pattern of metabolite alterations corresponded with early hepatic and renal toxicities primarily observed in itraconazole recipients. These findings indicated that itraconazole, a potent inhibitor of CYP3A4, alters CY metabolism in a manner that increases HCY and its toxic downstream metabolites, potentially exacerbating conditioning-related toxicities. Conversely, fluconazole's inhibition of CYP2C9 may reduce HCY formation, offering a relative protective effect. [1], [2]

Voriconazole, posaconazole, and isavuconazole are important broad antifungal spectrum in hematology/oncology patients, which may present problems when co-administered with antineoplastic agents, primarily due to inhibition of CYP450 enzymes and transport proteins (i.e., P-gp and breast cancer resistance protein). Among the notable interactions, voriconazole and posaconazole were associated with increased plasma concentrations of substrates metabolized by CYP3A4, thereby elevating the risk of toxicity and QT prolongation. In contrast, isavuconazole exhibited a milder inhibitory effect on CYP3A4 and a unique QT-shortening profile, suggesting a potentially safer alternative in patients receiving concomitant cardiotoxic agents. Impaired cylophosphamide metabolism and resultant increased exposure have been noted in patients co-treated with azole antifungals like itraconazole, fluconazole, and ketoconazole, potentially due to CYP2B6 inhibition; however, data on isavuconazole as a CYP2B6 inducer suggest it might reduce cyclophosphamide levels, but is not conclusively confirmed. Treatment with cyclophosphamide has been associated with cardiac arrhythmias such as supraventricular arrhythmias, including atrial fibrillation, and ventricular arrhythmias, including severe QT prolongation. [3], [4]

A pharmacokinetic study (Table 1) investigated interactions between cyclophosphamide and three triazole antifungals (fluconazole, itraconazole, and ketoconazole) using physiologically based pharmacokinetic (PBPK) modeling. To assess interactions, simulations were conducted using Simcyp software, evaluating single and multiple-dose regimens of orally administered triazoles with intravenous cyclophosphamide in virtual cancer populations. Model validation was performed by comparing simulated results with existing clinical pharmacokinetic data, ensuring reliability with fold-error values below two for key pharmacokinetic parameters. The 2019 PBPK modeling study demonstrated that all three triazole antifungals increased cyclophosphamide plasma exposure, but with varying extents of interaction. After a single dose, coadministration with fluconazole, itraconazole, or ketoconazole increased the area under the concentration-time curve (AUC) of cyclophosphamide by 10%, 17%, and 76%, respectively. With multiple doses, these increases were more pronounced, reaching 29% for fluconazole, 63% for itraconazole, and 102% for ketoconazole. Ketoconazole exhibited the strongest inhibitory effect due to its potent CYP3A4 inhibition, whereas fluconazole, a weaker inhibitor of CYP3A4, had the least impact. These findings suggest that concurrent use of triazole antifungals, particularly ketoconazole, necessitates close monitoring for potential cyclophosphamide toxicity, reinforcing the need for careful antifungal selection in oncology settings. [1]

A 2021 study investigated the potential drug interaction between cyclophosphamide and voriconazole via CYP2B6 inhibition using a combination of in vitro, in vivo, and database-driven pharmacovigilance approaches. The inhibitory potential of voriconazole on CYP2B6 was assessed through an in vitro cocktail incubation method, demonstrating an IC50 of 0.12 µM, indicating potent inhibition. In mouse liver microsomes, voriconazole suppressed the formation of 4-hydroxycyclophosphamide, the active metabolite of cyclophosphamide, by over 90% at concentrations of 10 µM and above. A pharmacokinetic study in mice co-administered with cyclophosphamide and voriconazole revealed a 2.3-fold increase in cyclophosphamide blood concentrations, confirming the inhibition of its metabolic activation. Additionally, cyclophosphamide-induced toxicities, including alopecia and leukopenia, were significantly attenuated when administered with voriconazole, supporting a clinically relevant interaction. An analysis of adverse event reporting systems, including data from FAERS and JADER, further corroborated this interaction. The proportional reporting ratio for cyclophosphamide-associated neutropenia, hemorrhagic cystitis, and alopecia was significantly reduced when cyclophosphamide was co-prescribed with voriconazole, fluconazole, or itraconazole. Notably, in the FDA Adverse Events Reporting System, the proportional reporting ratio for alopecia with voriconazole was reduced approximately 30-fold, removing the adverse event signal entirely. These findings suggest that the inhibition of CYP2B6-mediated cyclophosphamide activation by voriconazole alters both pharmacokinetics and therapeutic outcomes, highlighting the need for clinical awareness of potential drug interactions that may compromise efficacy in chemotherapy regimens. [5]

References:

[1] Cai T, Liao Y, Chen Z, Zhu Y, Qiu X. The Influence of Different Triazole Antifungal Agents on the Pharmacokinetics of Cyclophosphamide. Ann Pharmacother. 2020;54(7):676-683. doi:10.1177/1060028019896894
[2] Marr KA, Leisenring W, Crippa F, et al. Cyclophosphamide metabolism is affected by azole antifungals. Blood. 2004;103(4):1557-1559. doi:10.1182/blood-2003-07-2512
[3] Azanza JR, Mensa J, Barberán J, et al. Recommendations on the use of azole antifungals in hematology-oncology patients. Rev Esp Quimioter. 2023;36(3):236-258. doi:10.37201/req/013.2023
[4] Brüggemann RJ, Alffenaar JW, Blijlevens NM, et al. Clinical relevance of the pharmacokinetic interactions of azole antifungal drugs with other coadministered agents. Clin Infect Dis. 2009;48(10):1441-1458. doi:10.1086/598327
[5] Shibata Y, Tamemoto Y, Singh SP, et al. Plausible drug interaction between cyclophosphamide and voriconazole via inhibition of CYP2B6. Drug Metab Pharmacokinet. 2021;39:100396. doi:10.1016/j.dmpk.2021.100396

Literature Review

A search of the published medical literature revealed 5 studies investigating the researchable question:

What is the evidence to support or refute an interaction between cyclophosphamide and azole antifungals?

Level of evidence

C - Multiple studies with limitations or conflicting results  Read more→



Please see Tables 1-5 for your response.


 

The Influence of Different Triazole Antifungal Agents on the Pharmacokinetics of Cyclophosphamide
Design

Pharmacokinetic modeling study

Objective

To investigate the effects of different triazole antifungal drugs, including fluconazole, itraconazole, and ketoconazole, on the pharmacokinetics (PK) of cyclophosphamide and to characterize the potential drug-drug interactions (DDIs) between cyclophosphamide and various triazole antifungal drugs

Methods

Physiologically-based pharmacokinetic models were developed and validated using Simcyp software to evaluate potential DDIs between cyclophosphamide and three different triazole antifungal agents: fluconazole, itraconazole, and ketoconazole. Triazole antifungal agents were simulated by oral administration, whereas cyclophosphamide was simulated by intravenous administration. The models were validated using observed plasma concentration-time profiles.

Outcome Measures

Primary: Changes in pharmacokinetic parameters of cyclophosphamide (Cmax, Tmax, AUC) when coadministered with triazole antifungals

Observed and Simulated Pharmacokinetic Parameters  

Cmax (µg/mL)

Tmax (h) AUC (µg h/mL)

Cyclophosphamide 800 mg IV

Observed

Predicted

 

22.40

24.80

 

1.04

0.96

 

173.00

145.00

Fluconazole 100 mg PO

Observed

Predicted

 

1.70

1.60

 

4.29

2.89

 

93.00

80.60

Itraconazole 200 mg PO

Observed

Predicted

 

0.28

0.31

 

4.36

2.41

 

1.97

2.69

Ketoconazole 400 mg PO

Observed

Predicted

 

10.62

6.94

 

1.67

2.08 

 

68.53

55.90

Model-Predicted Pharmacokinetic Parameters of Cyclophosphamide Given with Triazoles Cyclophosphamide DDI with

Cmax (µg/mL)

Tmax (h) AUC (µg h/mL)

Fluconazole

DDI with fluconazole (single dose)

DDI with fluconazole (multiple doses)

 

25.10

28.5

 

0.96

1.32

 

160

246

Itraconazole

DDI with itraconazole (single dose)

DDI with itraconazole (multiple doses)

 

25.90

31.2

 

0.96

1.32

 

169

311

Ketoconazole

DDI with ketoconazole (single dose)

DDI with ketoconazole (multiple doses)

 

26.80

32.7

 

0.96

1.32

 

255

191

Study Author Conclusions

Ketoconazole had the greatest effect on the PK of cyclophosphamide among the 3 triazole antifungals. The toxicity and adverse drug reactions associated with cyclophosphamide should be closely monitored when coadministered with ketoconazole.

Critique

The study effectively uses physiology-based PK modeling to predict DDIs, providing valuable insights into potential interactions between cyclophosphamide and triazole antifungals. However, the study is limited by its reliance on simulations rather than clinical data, which may not fully capture the complexity of in vivo interactions. Further clinical studies are needed to validate these findings in diverse patient populations.

 

References:

Cai T, Liao Y, Chen Z, Zhu Y, Qiu X. The Influence of Different Triazole Antifungal Agents on the Pharmacokinetics of Cyclophosphamide. Ann Pharmacother. 2020;54(7):676-683. doi:10.1177/1060028019896894

 

Cyclophosphamide metabolism is affected by azole antifungals

Design

Randomized, open-label trial

N=209

Objective

To compare the safety and efficacy of itraconazole with fluconazole in preventing fungal infections in patients undergoing allogeneic stem cell transplantation (SCT) and to investigate the impact of these azoles on cyclophosphamide (CY) metabolism and related toxicities

Study Groups

Itraconazole (n=105)

Fluconazole (n=104)

Inclusion Criteria

Patients aged ≥13 years undergoing allogeneic SCT, receiving either fluconazole or itraconazole starting with conditioning chemotherapy

Exclusion Criteria

Not specified

Methods

Patients were randomized to receive fluconazole (400 mg daily) or itraconazole (200 mg daily IV or 2.5 mg/kg oral solution 3 times daily) starting with conditioning therapy. Cylophosphamide metabolism was analyzed in a subset of patients to assess exposure to metabolites. Serum bilirubin and creatinine levels were monitored for toxicities.

Duration

First 20 days after SCT

Outcome Measures

Primary: Serum bilirubin and creatinine levels

Secondary: Exposure to cyclophosphamide metabolites (4-hydroxy-cyclophosphamide [HCY], O-carboxyethylphosphoramide mustard [CEPM], deschloroethyl-cyclophosphamide [DCCY], 4-keto-cyclophosphamide [ketoCY], and hydroxyprophylphosphoramide mustard [HPPM])

Baseline Characteristics  

Itraconazole (n=105)

Fluconazole (n=104)

Median serum bilirubin, mg/dL

1.49

1.32

Creatinine level increase ≥2-fold

36 (34%) 21 (20%)
Results  

Itraconazole (n=9)

Fluconazole (n=140) p-value

CY AUC

5077 ± 991 6198 ± 1229 0.0065

DCCY AUC

371 ± 148 615 ± 267 0.007

HCY AUC

231 ± 46 147 ± 59 <0.001

ketoCY AUC

348 ± 121 227 ± 88 <0.001

CEPM AUC

472 ± 135 412 ± 188 0.016
AUC: area under the curve
Adverse Events

Higher serum bilirubin and creatinine levels in the itraconazole group. Increased exposure to toxic cyclophosphamide metabolites (HCY, ketoCY) in itraconazole recipients.

Study Author Conclusions

Itraconazole and fluconazole alter cyclophosphamide metabolism differently, impacting toxicities early after SCT. Caution is advised when coadministering azole antifungals with cytochrome-metabolized cytotoxic agents.

Critique

The study highlights important drug interactions affecting cyclophosphamide metabolism, but the small sample size for itraconazole limits definitive conclusions. The lack of a true control group without azole antifungals also limits the ability to fully understand the mechanisms of interaction.

 

References:

Marr KA, Leisenring W, Crippa F, et al. Cyclophosphamide metabolism is affected by azole antifungals. Blood. 2004;103(4):1557-1559. doi:10.1182/blood-2003-07-2512

 

Fluconazole Coadministration Concurrent with Cyclophosphamide Conditioning May Reduce Regimen-Related Toxicity Post-myeloablative Hematopoietic Cell Transplantation

Design

Two studies:

A pharmacokinetic cohort study (N=73)

A randomized placebo-controlled trial (N=299)

Objective

To investigate whether fluconazole co-administration with cyclophosphamide (CY) reduces CY-related toxicities by inhibiting cytochrome P450 2C9 metabolism

Study Groups

Fluconazole group (n=56)

Non-fluconazole group (n=17)

Fluconazole (n=152)

Placebo (n=147)

Inclusion Criteria

Allogeneic HCT recipients treated with busulfan-CY conditioning and variable antifungals from 2001 to 2005; Patients from a prior randomized trial receiving fluconazole or placebo concurrent with CY-containing conditioning

Exclusion Criteria

Not specified

Methods

Cyclophosphamide was infused at 60 mg/kg body weight over 1-2 hours, with a second infusion the following day. Fluconazole 400 mg daily was administered concomitant with conditioning. Blood samples were collected for CY and CY-metabolite analysis. In the randomized trial, patients received fluconazole or placebo concurrent with CY-containing conditioning.

Duration

Study 1: 2001 to 2005

Study 2: 1990 to 1992

Outcome Measures

Primary: CY and CY-metabolite exposure, hepatic and renal toxicities, survival

Secondary: Probability of relapse of underlying malignancy

Study 1  

Fluconazole (n=56)

Non-fluconazole (n=17) p-value

Area under the curve (AUC)

Cyclophosphamide

CePM

HCY

 

2628 (1375-8086)

489 (215-1165)

272 (92-744)

 

1465 (933-3431)

500 (271-738)

297 (194-353)

 

<0.0001

0.686

0.4395

Cmax, h

Cyclophosphamide after dose 1

Cyclophosphamide after dose 2

HCY after dose 1

 

305 (92-744)

282 (153-1064)

31 (10-65)

 

223 (145-302)

212 (19-403)

43 (20-60)

 

<0.0001

0.0001

0.0056

No significant difference in maximum creatinine level or number of patients reaching >2x baseline was observed. There were nonsignificant trends to higher maximum and daily total serum bilirubin levels in the fluconazole group.

Study 2  

Fluconazole (n=152)

Placebo (n=147) p-value

Probability of survival

Day 20

Day 75

 

95%

83%

 

89%

74%

 

0.04

0.06

Doubling of baseline creatinine

34%

47% 0.02
Median daily total serum bilirubin level (range) 2.0 (0.4-27.7)

2.5 (0.3-27.8)

0.05
Adverse Events

Fewer fluconazole recipients experienced a doubling of baseline creatinine and had lower median daily total serum bilirubin levels compared to placebo.

Study Author Conclusions

High dose fluconazole may impact CY activation, exerting a protective effect against CY-related toxicities. A randomized trial is needed to confirm these findings.

Critique

The study suggests a potential protective effect of fluconazole against CY-related toxicities, but the retrospective nature and lack of randomization in the pharmacokinetic study limit the ability to draw definitive conclusions. Little data was given on the patients, including no baseline characteristics.

 

References:

Upton A, McCune JS, Kirby KA, et al. Fluconazole coadministration concurrent with cyclophosphamide conditioning may reduce regimen-related toxicity postmyeloablative hematopoietic cell transplantation. Biol Blood Marrow Transplant. 2007;13(7):760-764. doi:10.1016/j.bbmt.2007.03.005

 

Posaconazole prophylaxis during induction therapy of patients with acute lymphoblastic leukaemia

Design

Pilot study

N= 8

Objective

To prove the safety of posaconazole in patients undergoing intensified induction phase treatment for acute lymphoblastic leukaemia (ALL)

Study Groups

All patients (n= 8)

Inclusion Criteria

Patients recently diagnosed with ALL, treated at the Dresden University hospital according to the GMALL study group protocol for patients younger than 60 years

Exclusion Criteria

Not specified

Methods

Posaconazole was administered prophylactically at a dose of 200 mg TID during induction chemotherapy for ALL, starting at a leucocyte count of <1 Gpt/L. Induction included cyclophosphamide 200 mg/m2 on days 3-5; a second induction phase included cyclophosphamide 1000 mg/m2 on days 26 and 46.

Posaconazole was withheld on days with vincristine, anthracycline, or asparaginase treatment and reinstituted 48 hours later. In cases of treatment-resistant neutropenic fever, posaconazole was stopped and alternative antifungal drugs were administered.

Outcome Measures

Primary: Safety and tolerability of posaconazole

Secondary: Incidence of invasive fungal infections (IFI)

Results Patient Days of posaconazole ppx Rason for stopping posaconazole ALT >grade 3 AST >grade 3 Bilirubin >grade 3
29 M 21 Neutropenic fever No No No
19 F 42 Neutropenic fever No No No
36 M 45 Not stopped Yes No Yes
43 M 59 Not stopped Yes Yes Yes
32 M 58 Not stopped Yes No Yes
30 M 6 Neutropenic fever Yes Yes No
22 M 49 Neutropenic fever No No No
41 F 6 Neutropenic fever No No No

All 8 patients had a complete response (CR) after induction phase 2. 

Adverse Events

Hepatic toxicity was common, with ALT, AST, and bilirubin levels >grade 3 in some patients. No renal toxicity was observed. One patient developed possible aspergillosis and recovered after voriconazole.

Study Author Conclusions

The observations indicate a favorable toxicity profile of posaconazole in ALL therapy. Efficacy of the drug has to be further validated in prospective clinical trials.

Critique

The study was limited by its small sample size and retrospective nature. The lack of a control group and detailed pharmacokinetic studies limits the ability to draw definitive conclusions about the safety and efficacy of posaconazole in this setting.

 

References:

Illmer T, Babatz J, Pursche S, et al. Posaconazole prophylaxis during induction therapy of patients with acute lymphoblastic leukaemia. Mycoses. 2011;54(4):e143-e147. doi:10.1111/j.1439-0507.2010.01860.x

 

Successful Treatment of Paecilomyces variotii Pneumonia and Lupus Nephritis With Posaconazole-Cyclophosphamide Co-administration Without Drug Interaction-Induced Toxicity

Design

Case report

Case presentation

A 43-year-old woman from Brazil with a history of hypothyroidism, untreated latent tuberculosis, and systemic lupus erythematosus (SLE) presented with a 3-month history of cough, dyspnea, myalgias, and fevers. Initially thought to be an SLE flare, her condition persisted despite prednisone treatment. A chest radiograph revealed a left upper lobe infiltrate, leading to a bronchoscopy that identified Paecilomyces variotii in bronchoalveolar lavage fluid.

Initial treatment with itraconazole 200 mg q12h was halted due to suspected itraconazole-induced pseudohyperaldosteronism, leading to hypokalemia and new-onset hypertension. She was switched to posaconazole 300 mg/day and developed novel hypertension and nephrotic-range proteinuria owing to severe lupus nephritis, confirmed via renal biopsy showing diffuse proliferative and membranous patterns.

Treatment included hydroxychloroquine, high-dose corticosteroids, cyclophosphamide, isoniazid for latent TB, and atovaquone for Pneumocystis jirovecii prophylaxis. Posaconazole was temporarily held for three days before and one day after each monthly cyclophosphamide infusion, with micafungin used as a bridging antifungal during these interruptions. The patient received seven planned cycles of cyclophosphamide while maintaining posaconazole therapy without developing nephrotoxicity, hepatotoxicity, or myelotoxicity. Serum creatinine levels peaked at 1.46 mg/dL before improving to 0.76 mg/dL by the final cycle, while lupus nephritis showed significant clinical improvement, as evidenced by a reduction in the urine protein-to-creatinine ratio from 5216 mg/g to 818 mg/g.

This regimen was largely well-tolerated, with no significant cyclophosphamide toxicity. Cytomegalovirus reactivation was successfully treated with valganciclovir. Over seven cyclophosphamide cycles, her lupus nephritis improved, as indicated by normalized complement levels, reduced proteinuria, and resolved hypokalemia and hypertension. Kidney function also stabilized, allowing the cessation of additional medications for pseudohyperaldosteronism. Repeat imaging showed resolution of pulmonary abnormalities.

Study Author Conclusions

This case establishes proof of concept for a structured approach to administering high-dose cyclophosphamide alongside triazole antifungal therapy by incorporating drug-hold strategies and alternative antifungal bridging, demonstrating both clinical efficacy and safety in severe lupus nephritis with concurrent fungal pneumonia.

Drug level monitoring demonstrated that posaconazole concentrations before each cyclophosphamide infusion decreased to a range of 81 to 583 ng/mL, effectively mitigating excessive accumulation of cyclophosphamide metabolites. The approach also successfully controlled Paecilomyces variotii pneumonia, with follow-up imaging after six months of treatment showing resolution of pulmonary lesions. Additionally, itraconazole-related pseudohyperaldosteronism, previously evident through hypokalemia and resistant hypertension, resolved after switching to posaconazole.

 

References:

Pechacek J, Webb T, Ferré EMN, et al. Successful Treatment of Paecilomyces variotii Pneumonia and Lupus Nephritis With Posaconazole-Cyclophosphamide Co-administration Without Drug Interaction-Induced Toxicity. Open Forum Infect Dis. 2023;10(8):ofad410. Published 2023 Aug 2. doi:10.1093/ofid/ofad410