Abstract
A 53-year-old woman with a history of acute myeloid leukemia received a
second allogenic hematopoietic stem cell transplant (HSCT) and was
prescribed, among other medications, acyclovir and letermovir (480 mg
daily oral dose) for prophylaxis of respectively herpes simplex and
cytomegalovirus infection. The patient was admitted in the intensive
care unit (ICU) for dyspnea and oliguria. Laboratory investigations
revealed acute kidney injury, but also a severe and progressive lactic
acidosis. Liver function tests were within normal range. The combination
of lactic acidosis, hypoglycaemia and acylcarnitine profile in plasma
suspected a mitochondrial toxicity. Letermovir therapy was interrupted
and determination of plasma letermovir pharmacokinetics revealed a
prolonged terminal half-life (40.7 h) that was not significantly
influenced by continuous venovenous hemofiltration. Exploration for
genetic polymorphisms revealed that the patient was SLCO1B1 *5/*15
(c.521T>C homozygous carrier and c.388A>G
heterozygous carrier) with a predicted non-functional OATP1B1 protein.
The relationship between letermovir accumulation and development of
lactic acidosis requires further observations.
Key words: letermovir – hematopoietic stem cell
transplantation – pharmacokinetics SLCO1B1 gene polymorphism – lactic
acidosis
Introduction
Letermovir is an inhibitor of cytomegalovirus (CMV) viral terminase that
has been approved for prophylaxis of CMV infection and disease in
CMV-seropositive allogeneic hematopoietic stem cell transplant (HSCT)
recipients. Letermovir is well tolerated in populations with mild to
moderate hepatic or renal impairment [1,2]. Letermovir
pharmacokinetics may be affected by variants of the solute carrier
organic anion transporter family member 1B1 (SLCO1B1) gene and also by
some drug-drug interaction, but usually with a limited clinical impact
[3,4].
Case report
A 53-year-old woman was admitted in the Intensive Care Unit (ICU) for
progressive dyspnea and oliguria. She had a medical past history of
acute myeloid leukemia (AML) with inv(16) (CBF-MYH11) and FLT3-ITD
that relapsed after a first allogeneic HSCT. The patient had reveiced a
second allogeneic HSCT 13 days before ICU admission and was treated with
empiric piperacillin/tazobactam plus vancomycin for febrile neutropenia.
Prophylaxis against herpes simplex and cytomegalovirus included
respectively oral acyclovir (400 mg daily, reduced to 200 mg after
progression of renal dysfunction) and oral letermovir (480 mg daily
since HSCT). Other medications are listed in Table I. The respiratory
condition progressively deteriorated on the hematology ward, together
with a decrease in urine output. On physical examination, the patient
was fully conscious with high respiratory rate (45/min), but preserved
blood pressure (143/90 mmHg). Laboratory investigations on admission
revealed: pH 7.25, pCO2 28 mm Hg, bicarbonate 13 mmol/L,
lactic acid 5.5 mmol/L, anion gap 24.5 mmol/L, serum creatinine 3.16
mg/dL (estimated glomerular filtration rate 16 mL/min/1.73m²), glucose
130 mg/dL. Liver function tests were normal. Echocardiography showed a
moderate mitral valve regurgitation with a well preserved left
ventricular function. No hemodynamic support was required. The central
venous oxygen saturation (ScvO2) was 61.8%. The abdomen
computed tomography (CT) excluded intestinal ischemia. The patient
experienced hypoglycemic episodes and dextrose 50% was then
continuously infused. The blood 3-hydroxybutyrate concentration was 448
µmol/L. The acylcarnitine profile in plasma was altered and revealed
increased concentrations of short, medium and long chains as follows:
C4:0 0.53 µmol/L (<0.38), C5:0 0.45 (<0.23), C5DC
0.37 (<0.13) , C6:0 0.57 µmol/L (< 0.13), C8:0 0.58
µmol/L (<0.21), C10:0 1.52 µmol/L (<0.35), C12:0
0.73 µmol/L (<0.15), C14:1 0.72 µmol/L (<0.18),
C16:0 0.82 µmol/L (<0.22) and C18:1 1.24 (<0.41).
In front of an unexplained lactic acidosis and in the absence of
recommendation for letermovir following acute kidney injury, this
medication was interrupted. Blood was sampled for the determination of
plasma letermovir concentration before the start of continuous
venovenous hemofiltration (CVVH), 18 hours after the last oral
administration. Plasma letermovir was measured using a validated high
performance liquid chromatography tandem mass spectrometry method.
Plasma level was 5300 µg/L and the terminal elimination half-life (t½)
calculated on four consecutive data points was 40.7 Additionally, the
blood tacrolimus concentrations rose from 10.5 to 28.8 ng/mL by the same
day. Evolution of lactate concentrations is illustrated in Figure 1 and
letermovir pharmacokinetics in Figure 2. The patient died on ICU day 6
from unrelated neurological complications (refractory status
epilepticus). Genotyping of relevant pharmacogenes revealed that the
patient was CYP3A4*1/*1 (absence of main CYP3A4 variants
including c.522-191C>T defined as CYP3A4*22 ),CYP3A5*3/*3 (CYP3A5 non expresser, c.219-237A>G
homozygous carrier) and SLCO1B1 *5/*15 (c.521T>C
homozygous carrier and c.388A>G heterozygous carrier) with
a predicted non-functional OATP1B1 protein.
Discussion
Among the medications that the patient received at the time of the
development of lactic acidosis, none could be clearly associated with
this type of complication. In particular, lactic acidosis is generally
not a complication of acyclovir therapy, even in the patients who
developed acute kidney injury. Some antiviral drugs can induce lactic
acidosis, but to date, there was no mention of letermovir. The
alterations of the acylcarnitines profile, including the elevation of
several lengths of acylcarnitines, together with lactic acidosis, could
suggest a mitochondrial toxicity. Such acylcarnitines profiles are seen
in mitochondrial disorders such as multiple acyl-CoA dehydrogenase
deficiency.
Letermovir therapy is usually well tolerated, adverse effects include
nausea, vomiting and diarrhea. Letermovir is a substrate of CYP3A4/5 and
UGT1A1/3 in vitro , and an inhibitor of P-gp, OATP1B1 and OATP1B3
[5]. Letermovir is highly protein bound (99%) and no significant
epuration should be expected from renal replacement techniques. Renal
excretion represents less than 2%, while fecal excretion is reaching
93% (unchanged for 70%). No dose adjustments are recommended for
patients with an estimated glomerular filtration rate > 10
mL/min. Due to the lack of data, letermovir is not recommended for
patients with end-stage renal disease with or without dialysis [2].
Previous observations have documented elevated drug exposure in renally
impaired subjects. During normal therapeutic use, the plasma terminal
half-life is 12 hours [5].
There are limited data regarding therapeutic drug monitoring of orally
administered letermovir prophylaxis in allogenic HSCT recipients. In a
population of 40 consecutive patients, letermovir trough concentration
remained stable during the first 70 days post-HSCT at a median of 286
µg/L (interquartile range, 131 to 591 µg/L), with large
inter-patient/intra-patient variability [4]. Patients who received
simultaneously either posaconazole or cyclosporine had higher letermovir
trough concentrations. Patients with letermovir-associated adverse
effects had also higher trough concentrations. These adverse
manifestations mainly involved atrial fibrillation, peripheral oedema,
myalgias, and the causality was never firmly demonstrated. No case of
lactic acidosis was documented. Other studies coming from the organ
transplant literature have shown higher untimed letermovir
concentrations, ranging from not detectable to 24,250 µg/L [6]. In a
series of 74 letermovir trough samples obtained in patients receiving
oral letermovir in real-life conditions, the mean trough concentration
was 3397 ± 2531 µg/L [7]. Two patients on renal replacement therapy
(RRT) received letermovir intravenously at a dosage of 480 mg daily; one
patient had a mean trough level of letermovir 1.7-fold higher than
reported in the previous study and did not experience adverse effects.
There was no influence of RRT on letermovir concentrations [8]. This
apparent discrepancy between the studies in the interpretation of
letermovir pharmacokinetics may be explained not only by the large
inter-individual and intra-individual variability, but also by the lack
of precise timing of blood sampling and differences in testing methods
[4,7].
Regarding drug-drug interactions, concomitant use of letermovir and
tacrolimus or cyclosporine may result in an increase in trough
concentrations of the immunosuppressants by CYP3A inhibition [9].
The pharmacokinetics of fluconazole and letermovir was not significantly
changed following co-administration [10]. This was also the case for
combined therapy with mycophenolate mofetil [9].
Analysis of the patient’s pharmacogenetic profile showed a CYP3Agenotype expected for a Caucasian population, namely normal CYP3A4
activity and the absence of CYP3A5 activity. In contrast, theSLCO1B1 genotype (*5/*15) corresponds to a complete absence of
OATP1B1 activity and is quite rare in the Caucasian population
(c.521T>C, rs4149056, MAF: 0.16; expected frequency of
homozygous carriers 2.6% according ensemble.org). The absence of
OATP1B1 activity in this patient therefore most likely contributed to
the marked increase in letermovir plasma concentrations.
CONCLUSION
In conclusion, our observation suggests that higher letermovir trough
concentrations and prolonged terminal half-life elimination may be
observed in selected HSCT recipients under some conditions of drug-drug
interaction and/or altered metabolism and transport. The relationship
with the development of otherwise unexplained lactic acidosis remains
hypothetical and requires further observations. Therefore, monitoring of
letermovir concentrations could be useful in a high-risk population with
renal or hepatic dysfunction, or co-medications.