Antiviral Therapy 2016; 21: (doi: /IMP2987)
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1 Antiviral Therapy 2016; 21: (doi: /IMP2987) Case report Virological failure in two patients with HIV-1 RNA viral loads >1,000,000 copies/ml initiated on elvitegravir/cobicistat/emtricitabine/tenofovir disoproxil fumarate Jessica L Adams 1,2,3 *, Dana Byrne 2,3, Rosalie Pepe 2,3, Anastasia Gray 2, John D Baxter 2,3 1 University of the Sciences, Philadelphia College of Pharmacy, Philadelphia, PA, USA 2 Cooper University Hospital, Camden, NJ, USA 3 Cooper Medical School of Rowan University, Camden, NJ, USA *Corresponding author j.adams@usciences.edu Very high baseline HIV-1 RNA viral loads require potent and robust antiretroviral regimens to achieve virological suppression. The coformulated single tablet regimen of elvitegravir/cobicistat/emtricitabine/tenofovir disoproxil fumarate (EVG/COBI/FTC/TDF) is recommended by the US Department of Health and Human Services for the treatment of HIV-1 in treatment-naive adults and adolescents regardless of baseline CD4 + T-cell count and viral load. We report two cases of HIV-infected, treatment-naive patients, with baseline HIV-1 RNA viral loads >1,000,000 copies/ml who were initiated on the single tablet regimen EVG/COBI/FTC/TDF, but failed to attain viral load suppression and developed resistance to the components of EVG/ COBI/FTC/TDF. Introduction Elvitegravir/cobicistat/emtricitabine/tenofovir disoproxil fumarate (EVG/COBI/FTC/TDF) is a recommended first-line antiretroviral (ARV) regimen for the treatment of HIV-1 in treatment-naive patients regardless of baseline CD4 + T-cell count or HIV RNA viral load according to the current US Department of Health and Human Services Guidelines for the Treatment of HIV-1 in Adults and Adolescents [1]. This recommendation is supported by Phase III data showing non-inferiority of EVG/COBI/FTC/TDF to both atazanavir/ritonavir/ftc/ TDF (ATV/r+FTC/TDF) and efavirenz/ftc/tdf (EFV/ FTC/TDF) [2,3]. In these two parallel Phase III studies, patients with baseline HIV-1 RNA viral loads >100,000 copies/ml were found to have a similar virological response to EVG/COBI/FTC/TDF as patients with baseline HIV-1 RNA viral loads 100,000 copies/ml [4]. Additionally, patients with baseline CD4 + T-cell counts <200 copies/mm 3 were found to have similar response rates to EVG/COBI/FTC/TDF as those with baseline CD4 + T-cell counts >200 copies/mm 3 [4]. While this data does support EVG/COBI/FTC/TDF as effective regardless of HIV-1 RNA viral load or CD4 + T-cell count studied, the number of patients with baseline viral loads >1,000,000 copies/ml in Phase III studies has not been reported [4]. We present two cases of treatment-naive patients presenting with baseline HIV viral loads over 1,000,000 copies/ml who were started on EVG/COBI/ FTC/TDF as their initial ARV regimen and were unable to suppress their very high viral load, ultimately failing therapy with drug resistance. Case descriptions Case 1 A 47-year-old female was referred to the HIV clinic after testing positive for HIV. Her HIV-1 RNA viral load was 2,633,760 copies/ml and CD4 + T-cell count was 90 cells/mm 3 at the time of diagnosis. A baseline genotype was performed that showed no reverse transcriptase resistance mutations, although a minor protease mutation, A71V, was detected. The single tablet regimen of EVG/COBI/FTC/TDF daily was chosen as her initial regimen. It was not expected to have significant drug drug interactions with the patient s concomitant medications, including sulfamethoxazole/ trimethoprim, tramadol, dexlansoprazole, montelukast, albuterol inhaler and beclomethasone inhaler. Of note, it was found that this patient was also concomitantly 2016 International Medical Press (print) (online) 175
2 JL Adams et al. taking ferrous sulfate. Approximately six weeks after starting therapy, her viral load decreased to 398,930 copies/ml but then increased to 797,830 copies/ml by 15 weeks on therapy (Figure 1). A repeat genotype, including an integrase genotype, was performed. The following reverse transcriptase mutations were found: M184V, K65R and A62V, conferring resistance to the nucleoside/nucleotide reverse transcriptase inhibitors (NRTIs) in her regimen, FTC and TDF. The following integrase mutations were also found: E138K, Q148R and S147G conferring resistance to the integrase strand transfer inhibitor (InSTI) in her regimen, EVG [5] (Table 1). The patient denied missing any doses and consistently refilled her prescription on time. She was changed to a salvage regimen of zidovudine, etravirine and darunavir/ritonavir and has had an appropriate viral load decline to 90 copies/ml at last measure. Case 2 A 51-year-old male presented to the HIV clinic following diagnosis by his primary care physician. His HIV-1 RNA viral load was 1,127,897 copies/ml and CD4 + T-cell count was 25 cells/mm 3. A baseline genotype was performed that showed no reverse transcriptase or protease resistance mutations. The single tablet EVG/COBI/ FTC/TDF was chosen as his initial regimen. It was not expected to interact with his medications including atovaquone for pneumocystis pneumonia prophylaxis, and ethambutol and azithromycin for the treatment of mycobacterium avium complex. Three weeks after starting therapy, his viral load decreased to 13,665 copies/ml, but then increased to 232,898 copies/ml by week 11 on therapy and 136,184 copies/ml upon repeat at week 13 (Figure 2). A phenotype test and an integrase genotype were performed. Phenotype testing predicted resistance to FTC and lamivudine. The integrase genotype showed the following resistance mutations: T66I, T97A and G163K conferring resistance to the InSTI in his regimen, EVG [5] (Table 1). He denied missing any doses and refilled his prescription on time each month. This patient has since achieved viral load suppression on a salvage regimen consisting of FTC/TDF, dolutegravir and darunavir/ COBI. Discussion We present two cases of treatment-naive patients with baseline viral loads >1,000,000 copies/ml and CD4 + T-cell counts less than 100 cells/mm 3 who were started on EVG/COBI/FTC/TDF and experienced virological failure with the emergence of resistance. Previous data has supported that very high baseline HIV-1 RNA viral loads are more difficult to suppress. In a meta-analysis of 21 clinical trials, rates of virological suppression by 48 weeks on therapy were significantly lower in Figure 1. HIV-1 RNA viral load trend following initiation of EVG/COBI/FTC/TDF 10,000,000 Case 1 HIV-1 RNA viral load, copies/ml 1,000, ,000 10,000 1, Time on EVG/COBI/FTC/TDF, weeks Weeks after starting therapy HIV-1 RNA viral load, copies/ml 2,633, , ,830 EVG/COBI/FTC/TDF, elvitegravir/cobicistat/emtricitabine/tenofovir disoproxil fumarate International Medical Press
3 Failure of EVG/COBI/FTC/TDF with HIV-1 RNA VLs >1,000,000 copies/ml Table 1. Resistance detected with virological failure on elvitegravir/cobicistat/emtricitabine/tenofovir disoproxil fumarate Case 1 Case 2 Reverse transcriptase mutations M184V, K65R, A62V Phenotypic resistance to emtricitabine and lamivudine Integrase mutations E138K, Q148R, S147G T66I, T97A, G163K Figure 2. HIV-1 RNA viral load trend following initiation of EVG/COBI/FTC/TDF 10,000,000 Case 2 HIV-1 RNA viral load, copies/ml 1,000, ,000 10,000 1, Time on EVG/COBI/FTC/TDF, weeks Weeks after starting therapy HIV-1 RNA viral load, copies/ml 0 1,127, , , ,184 EVG/COBI/FTC/TDF, elvitegravir/cobicistat/emtricitabine/tenofovir disoproxil fumarate. patients with baseline viral loads >100,000 copies/ml compared to those with <100,000 copies/ml across all ARV classes [6]. In one study of 1,430 patients starting their first ARV regimen, 15% of patients had viral loads >500,000 copies/ml [7]. Only 83% of those patients achieved viral load suppression by week 48, compared to >90% of patients with viral loads <500,000 copies/ml (P<0.001). The patients with high viral loads showed decreased virological success that was independent of age, gender, CD4 + T-cell count, transmitted drug resistance, year and ARV drug administered. Of note, the patients included in this study were on nonnucleoside reverse transcriptase inhibitor (NNRTI) or protease inhibitor (PI)-based ARV regimens, not InSTIs. In studies of the InSTI raltegravir as part of NRTI sparing regimens, virological failure with resistance was more common in those with high HIV RNA viral loads [8,9]. In the ACTG 5262 study, a combination of raltegravir, darunavir and ritonavir was given to treatment-naive patients in a Phase IIb, single-arm, open-label study. Virological failure by 48 weeks was found to be associated with baseline HIV RNA viral load >100,000 copies/ ml. Five subjects were found to have integrase resistance mutations at virological failure, and all five had baseline viral loads >100,000 copies/ml [8]. The NEAT-001 study, compared raltegravir, darunavir, ritonavir to a standard regimen of FTC/TDF, darunavir and ritonavir. Virological failure was seen in 36% of patients on the raltegravir, daruanvir, ritonavir regimen compared to 27% on the FTC/TDF, daruanvir, ritonavir regimen when the baseline viral load was >100,000 copies/ml, and 39% versus 21% when the baseline CD4 + T-cell count was <200 cells/mm 3. Five subjects failing raltegravir, darunavir, ritonavir were found to have integrase resistance mutations, and again, all five had baseline HIV RNA viral loads >100,000 copies/ml, with >500,000 copies/ml at baseline in four of the five [9]. Phase III studies of EVG/COBI/FTC/TDF stratified patients to >100,000 copies/ml and <100,000 copies/ml [2,3]. In Study 102 comparing EVG/COBI/FTC/TDF to Antiviral Therapy
4 JL Adams et al. EFV/FTC/TDF, 118 patients (34%) given EVG/COBI/ FTC/TDF had baseline viral loads >100,000 copies/ml. These patients were shown to have similarly high rates of viral load suppression as those with viral loads <100,000 copies/ml [2]. In Study 103 comparing EVG/ COBI/FTC/TDF to ATV/r+FTC/TDF, 150 patients (42%) given EVG/COBI/FTC/TDF had baseline viral loads >100,000 copies/ml and these patients also had similarly high rates of viral load suppression as those with viral loads <100,000 copies/ml at baseline [3]. Further data was provided on key subgroups who received EVG/COBI/FTC/TDF in a pooled 144 week subgroup analysis of both studies [4]. In this analysis, subjects were stratified to baseline viral loads 100,000 copies/ml, >100,000 to 400,000 copies/ml and >400,000 copies/ml. The efficacy of EVG/COBI/FTC/TDF was similar to both ATV/r+FTC/TDF and EFV/FTC/TDF at all viral loads. A total of 54 subjects with baseline viral loads >400,000 copies/ml received EVG/COBI/FTC/ TDF and of these, 43 (80%) achieved viral load suppression (<50 copies/ml) at 144 weeks. This was compared to 24/29 (83%) who received EFV/FTC/TDF and 21/29 (72%) who received ATV/r+FTC/TDF. The number of patients in this subgroup was small and the viral load range was not reported, therefore, the number of patients successfully treated with EVG/COBI/FTC/TDF with a baseline viral load >1,000,000 copies/ml remains unclear from published data. More concerning than the virological failure experienced by these two patients is the rapid development of drug resistance to the components of EVG/COBI/FTC/ TDF that will limit future ARV options. In Study 102, ten subjects on EVG/COBI/FTC/TDF developed resistance to one or more components of the regimen by week 144 [10]. Eight of the ten had baseline viral loads >100,000 copies/ml and only one subject had a baseline viral load >1,000,000 copies/ml. Eight patients developed resistance on EVG/COBI/FTC/TDF by week 144 in Study 103 [11]. Seven of the eight had baseline viral loads >100,000 copies/ml, two had >500,000 copies/ml, and none had >1,000,000 copies/ml. The resistance patterns that developed in our two patients were consistent with those that developed on therapy with EVG/COBI/ FTC/TDF in studies 102 and 103. Most of the subjects in these studies who developed primary integrase mutations also developed the M184V mutation [10 11]. In both cases presented here multiple integrase mutations were detected within 4 months of initiating EVG/COBI/ FTC/TDF. Case 1 developed major integrase mutations S147G and Q148R, which are selected by EVG, and E138K, an accessory mutation usually occurring with 148 position mutations. The pattern of mutations detected in Case 1 is associated with broad resistance to InSTIs, including full resistance to raltegravir and EVG, as well as intermediate susceptibility to dolutegravir. Case 2 was found to have the major integrase resistance mutation T66I, selected by EVG, and accessory mutations T97A and G163K. This pattern is associated with resistance to EVG, probable resistance to raltegravir and full susceptibility to dolutegravir [12]. Although the role of ARV adherence must be considered, Cases 1 and 2 were both reliable patients deemed likely to have been adherent by their HIV clinicians. Their pharmacy refill records were consistent each month (without the use of automatic refills), viral loads initially declined 1 2 logs, and they have both responded to salvage regimens. Both patients returned to clinic consistently for follow-up with initial followup labs within 2 8 weeks after starting therapy as recommended by the Department of Health and Human Services treatment guidelines [1]. The second followup labs for Case 1 were 9 weeks after initial follow-up labs, which was a week outside of the recommended 4 8 weeks for patients whose viral load is not yet suppressed [1]. This patient did have a cancelled appointment that was rescheduled in this time frame. The second follow-up labs for Case 2 were 8 weeks after initial follow-up labs, which was just barely within the 4 8 week recommended time frame, but no appointments were missed [1]. Since both patients had drops in HIV RNA viral load on initial follow-up labs, their HIV clinicians were not yet concerned for failure (Figures 1 and 2). Although the InSTIs as a class are potent and typically able to achieve rapid viral load suppression with adequate adherence, the barrier to resistance of raltegravir and EVG is much lower than the PIs and likely even lower than most NRTIs with the exception of FTC and lamivudine [13,14]. It is possible that these patients missed doses early on in their treatment, developing resistance quickly, which led to failure of therapy despite improved adherence thereafter. Additionally for Case 1, the concomitant use of ferrous sulfate with EVG could have resulted in decreased concentrations of EVG contributing to treatment failure. Polyvalent cations including iron are not recommended to be given simultaneously with EVG [15]. This recommendation is based on data from a healthy volunteer study where polyvalent antacids were administered with EVG leading to a decrease in EVG area under the curve, maximum concentration (C max ), and minimum concentration (C min ) by 45%, 47% and 41% [16]. Tolerability, dosing, administration and adherence, in addition to the barrier to adherence, are all important factors in treatment success. Another factor to consider is the potential that these two case patients had transmitted ARV resistance not detected on their baseline genotypes. It is possible that baseline reverse transcriptase mutations were not detected because the viral loads were elevated enough that the mutant variants had become minor species in International Medical Press
5 Failure of EVG/COBI/FTC/TDF with HIV-1 RNA VLs >1,000,000 copies/ml the absence of drug pressure. This is more likely to have been the case with the NRTI mutations which have been found to be present in approximately 6% of treatmentnaive patients, but is less likely with the integrase mutations as transmitted integrase resistance is still uncommon and both of these patients had likely been infected for years prior to diagnosis [17]. Although it would have been helpful to rule out transmitted integrase resistance, integrase resistance testing was not performed at baseline in either patient and by the time it was apparent that they were failing therapy, baseline samples were no longer available. When more readily available clinically, deep sequencing of the viral genome at baseline may be appropriate for patients with very high viral loads to look for archived or minor mutant species. A study by Simen et al. [18] found that ultra-deep sequencing was able to detect mutant variants in a significantly larger percentage of a treatment-naive population than standard genotypic sequencing (14 versus 28%; P<0.001). In this study, participants found to have mutations detected by ultra-deep sequencing had higher baseline viral loads with a median (IQR) HIV RNA baseline viral load of 324,000 copies/ml (101, ,000 copies/ml). Study participants found to have baseline mutant variants by ultra-deep sequencing alone, had an increased risk of virological failure after initiating NNRTI-based ARV regimens (HR 2.50, 95% CI 1.17, 5.36) [18]. Since the integrase inhibitors, specifically raltegravir and EVG, have low barriers to resistance similar to NNRTIs, perhaps minor mutant variants would have a similar clinical impact. These two case patients give caution to the use of one of our newer single tablet regimens, EVG/COBI/ FTC/TDF, in patients with high baseline viral loads, but it also must be considered that these two patients presented late in their disease progression with very high viral loads as well as significant immunosuppression. Patients who are late presenters are more likely to have a lower perceived risk of acquiring HIV, a lower socioeconomic status and lower health literacy, all of which can lead to an increased risk of non-adherence [19]. Additionally, late presenting patients are more likely to present with an opportunistic infection requiring treatment and an increased pill burden as we saw with Case 2. Because of these psychosocial factors associated with late presentation, additional clinical support and laboratory monitoring may be warranted in these patients despite an initial viral load response. The most reliable strategy for treating patients with very high baseline viral loads is still to be determined. Markowitz et al. [20] compared the use of a standard three-drug ARV regimen to a five-drug intensified ARV regimen in an open-label study. Newly diagnosed patients were randomized to receive either three-drug PI-based therapy or a PI-based therapy with the addition of raltegravir and maraviroc. At baseline, the mean log HIV-1 RNA values were high in both groups: 6.3 log copies/ml in the three-drug group and 5.6 log copies/ml in the five-drug group. By 16 weeks on therapy, 82% of patients in both groups achieved viral load suppression and the authors concluded that there was no apparent benefit to intensification of a standard three-drug PIbased regimen [20]. In conclusion, in the two cases presented, the single tablet regimen of EVG/COBI/FTC/TDF was an attractive initial HIV treatment option due to its general tolerability and convenience of dosing, but was ultimately not effective in suppressing these patients very high baseline viral loads and resulted in the rapid development of resistance. Further data is needed to inform on the best initial ARV options for patients with very high (>1,000,000 copies/ml) baseline viral loads. Disclosure statement JLA has previously received research support from ViiV Healthcare as a trainee. AG serves as a community speaker for ViiV Healthcare and Bristol Myers Squibb. JDB has served as a consultant for Quest Diagnostics and Siemens Healthcare Diagnostics. DB and RP have no competing interests. References 1. Panel on Antiretroviral Guidelines for Adults and Adolescents. Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. Department of Health and Human Services. (Updated 8 April Accessed 20 June 2015.) Available from gov/contentfiles/lvguidelines/adultandadolescentgl.pdf 2. Sax PE, DeJesus E, Mills A, et al. Co-formulated elvitegravir, cobicistat, emtricitabine, and tenofovir versus co-formulated efavirenz, emtricitabine, and tenofovir for initial treatment of HIV-1 infection: a randomised, double-blind, Phase 3 trial, analysis of results after 48 weeks. Lancet 2012; 379: DeJesus E, Rockstroh JK, Henry K, et al. Co-formulated elvitegravir, cobicistat, emtricitabine, and tenofovir disoproxil fumarate versus ritonavir-boosted atazanavir plus co-formulated emtricitabine and tenofovir disoproxil fumarate for initial treatment of HIV-1 infection: a randomised, double-blind, Phase 3, non-inferiority trial. Lancet 2012; 379: Elion R, Squires K, Bloch M, et al. Subgroup analyses of 144-week efficacy and safety of elvitegravir/cobicistat/ emtricitabine/tenofovir DF (EVG/COBI/FTC/TDF). ICAAC. 5 9 September 2014, Washington, DC, USA. Abstract H Wensing AM, Calvez V, Gunthard HF, et al. Special contribution: 2014 update of the drug resistance mutations in HIV-1. Top Antiv Med 2014; 22: Stephan C, Hill A, Sawyer Y, et al. Impact of baseline HIV-1 RNA levels on highly active antiretroviral therapy outcome: a meta-analysis of 12,370 patients in 21 clinical trials. HIV Med 2013; 14: Santoro MM, Armenia D, Alteri C, et al. Impact of pretherapy viral load on virological response to modern firstline HAART. Antivir Ther 2013; 18: Taiwo B, Zheng L, Gallien S, et al. Efficacy of a nucleosidesparing regimen of darunavir/ritonavir plus raltegravir in treatment-naive HIV-1-infected patients (ACTG A5262). AIDS 2011; 25: Antiviral Therapy
6 JL Adams et al. 9. Raffi F, Babiker AG, Richert L, et al. Ritonavir-boosted darunavir combined with raltegravir or tenofovir-emtricitabine in antiretroviral-naive adults infected with HIV 1: 96 week results from the NEAT001/ANRS143 randomised noninferiority trial. Lancet 2014; 384: White KL, Kulkarni R, McColl DJ, et al. Week 144 resistance analysis of elvitegravir/cobicistat/emtricitabine/tenofovir DF versus efavirenz/emtricitabine/tenofovir DF in antiretroviralnaive patients. Antivir Ther 2015; 20: Kulkarni R, Abram ME, McColl DJ, et al. Week 144 resistance analysis of elvitegravir/cobicistat/emtricitabine/ tenofovir DF versus atazanavir + ritonavir + emtricitabine/ tenofovir DF in antiretroviral-naive patients. HIV Clin Trials 2014; 15: Liu TF, Shafer RW. Web resources for HIV type 1 genotypicresistance test interpretation. Clin Infect Dis 2006; 42: Blanco JL, Varghese V, Rhee SY, et al. HIV-1 integrase inhibitor resistance and its clinical implications. J Infect Dis 2011; 203: Geretti AM, Armenia D, Ceccherini-Silberstein F. Emerging patterns and implications of HIV-1 integrase inhibitor resistance. Curr Opin Infect Dis 2012; 25: Stribild (elvitegravir, cobicistat, emtricitabine, tenofovir disoproxil fumarate). Prescribing information. Gilead Sciences Inc., Foster City, CA, USA. 16. Ramanathan S, Mathias A, Wei X, et al. Pharmacokinetics of once-daily boosted-elvitegravir when administered in combination with acid reducing agents. J Acquir Immune Defic Syndr 2013; 64: Kim D, Ziebell R, Saduvala N, et al. Trend in transmitted HIV-1 ARV drug resistance-associated mutations: 10 HIV surveillance areas, US, th Conference on Retroviruses and Opportunistic Infections. 3 6 March 2013, Atlanta, GA, USA. Abstract Simen BB, Simons JF, Hullsiek KH, et al. Low-abundance drug-resistant viral variants in chronically HIV-infected, antiretroviral treatment-naive patients significantly impact treatment outcomes. J Infect Dis 2009; 199: Waters L, Sabin CA. Late HIV presentation: epidemiology, clinical implications, and management. Expert Rev Anti Infect Ther 2011; 9: Markowitz M, Evering TH, Garmon D, et al. A randomized open-label study of three- versus five-drug combination antiretroviral therapy in newly HIV-1 infected individuals. J Acquir Immune Defic Syndr 2014; 66: Accepted 17 August 2015; published online 26 August International Medical Press
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