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Microelimination of hepatitis C in patients with chronic hemolytic anemias: a single-center experience

Abstract

Background

Patients with chronic hemolytic anemias (CHA) are at a high risk for transfusion-transmitted infections. Various studies in Egypt have shown a prevalence of hepatitis C virus (HCV) infection in 24–37% of those patients. Elimination of hepatitis C virus (HCV) in patients with CHA would prevent early progression of liver disease. In this study, we aimed to assess the efficacy, safety, and tolerability of sofosbuvir (SOF) and daclatasvir (DAC) in the special population of HCV-infected patients with CHA. In this prospective study, 21 consenting hepatitis C patients were recruited and treated using ribavirin-free SOF/DAC regimen for either 12 or 24 weeks according to categorization of patients into easy or hard-to-treat in accordance with the national protocols. Sustained virological response was assessed by RT-PCR for HCV-RNA at 12 weeks post-treatment (SVR12). Any treatment-related adverse events were noted.

Results

All patients were adherent to treatment with no discontinuation of therapy. SVR12 was achieved in 19 out of 21 patients (90.5%). There was a significant improvement in levels of ALT (p<0.009) after completion of therapy. On the other hand, the hemoglobin, total bilirubin, and ferritin levels showed a non-significant difference (p<0.501, p<0.542, and p<0.339, respectively). Moderate adverse events were observed in 2 out of 21 patients (9.5%), including sickling crisis and hepatic decompensation.

Conclusion

The results of this study substantiate the favorable efficacy, safety, and tolerability of ribavirin-free direct-acting antivirals (DAAs) in the special population of HCV-infected patients with CHA. Micro-elimination of HCV in special patient populations allows for pragmatic delivery of care to patients with co-morbid conditions who are in most need for treatment and allows for achievement of global elimination of HCV worldwide.

Background

CHA is a common blood disorder which occurs either due to hereditary or acquired causes [1]. Survival of most of this group of patients depends mainly upon regular blood transfusion which makes them at risk for iron overload and transfusion-transmitted infections [2].

Hepatitis C is considered to be one of the major transfusion-transmitted infections which represents a serious public health problem worldwide [3]. According to the World Health Organization (WHO), about 71 million people in the world are chronically infected with HCV, with the prevalence of this infection varying throughout the world [4].

Various studies have reported the prevalence of HCV in patients with thalassemia in different countries, e.g., 16.7 % in India, 22.4% in Malaysia, and 63.8% in Iran [5]. In Egypt, studies conducted in different regions showed that the prevalence ranged between 24 and 37% [2].

Pegylated interferon-α (PEG-INF) and ribavirin (RBV) was the only treatment available for HCV infection for several years. It showed a moderate efficacy in patients with chronic hemolytic anemias especially those with thalassemia. Its use was also limited by poor tolerance, and some concerns about RBV-induced hemolysis [6].

The advent of DAAs has brought about a sudden renaissance in the treatment of chronic HCV infection with SVR rates now routinely >90%. The shorter treatment duration and fewer side effects make DAAs the current standard of care for treatment of HCV in adults [7]. According to recent guidelines, patients with chronic hemolytic anemias should be treated with DAAs, preferably by RBV-free regimens [8].

The efficacy of the new DAAs regimens helped WHO to adopt its first Global Health Sector Strategy on Viral Hepatitis in 2016. Its goal was to simply combat hepatitis by calling for the elimination of HCV as a public health threat by 2030. The strategy defined elimination as an 80% reduction in new HCV infections and a 65% reduction in HCV mortality [9].

The most accepted pragmatic approach was to break down the national elimination goals into smaller sub-goals uniquely tailored for individual populations, for which treatment and prevention strategies can be delivered more quickly and efficiently. This concept was known as “micro-elimination”. Among these individual populations are patients with hemolytic anemias [10].

Micro-elimination strategy was accepted globally, and most high-income countries have already begun its implementation [11]. Other countries including Egypt, Iceland, Portugal, and Spain have also undertaken such strategy as a step to achieve broader elimination goals aimed at the general population [10].

Limited studies addressed the efficacy and safety of the currently available DAAs in this special population. Therefore, this study aimed to assess the efficacy and safety of SOF/DAC regimen in patients with CHA and HCV infection.

Methods

This was a prospective study of patients diagnosed with chronic HCV infection who presented to our institution to receive therapy with DAAs between January 2018 and January 2020. Out of 9500 registered patients, 171 (1.8%) were diagnosed with co-morbid hematological disorders; among those, 21 had chronic hemolytic anemias. Patients with decompensated liver disease, hepatitis B virus (HBV), or human immune-deficiency virus (HIV) co-infection and those with underlying malignancies were excluded. An informed written consent was obtained from all patients before inclusion in this study. The study was approved by the Ethical Review Board of our institution (Reference Number: FMASU M S 67/2019). The study protocol conforms to the ethical guidelines of the 1975 Declaration of Helsinki as reflected in a priori approval by the institution's human research committee.

The demographics of enrolled patients, type of hemolytic anemia, treatment status (naïve or experienced), frequency of blood transfusion, and type of iron chelators before treatment were all recorded both electronically and in a patient report form.

Baseline investigations included complete blood count (CBC), alanine aminotransferase (ALT), aspartate aminotransferase (AST), serum total and indirect bilirubin, serum albumin, international normalization ratio (INR), serum creatinine, alpha-fetoprotein, serum ferritin level, and pelvi-abdominal ultrasound, in addition to non-invasive assessment of liver stiffness by FIB4 and APRI scores. HCV viral load was determined by real-time polymerase chain reaction (RT-PCR) assay.

All patients received SOF 400mg and DAC 60mg daily. None of the patients received RBV in addition to their treatment regimen to avoid the hematological adverse events. The treatment duration ranged between 12 and 24 weeks according to baseline patients’ categorization as either easy or hard to treat in accordance with the national protocols.

Patients were categorized as hard to treat if meeting any of the following criteria: PEG-INF treatment-experienced (TE), total bilirubin ≥1.2 mg/dl, serum albumin ≤3.5 g/dl, INR ≥1.2, or platelet count <15,0000/mm3. The easy to treat group included 8 patients who were treated with SOF/DAC for 12 weeks. The difficult to treat group included 13 patients who were treated with SOF/DAC for 24 weeks.

Patients underwent a 4-weekly follow-up of CBC, serum total and indirect bilirubin, ALT, AST, INR, and serum creatinine. The monthly blood transfusion requirements, as well as any treatment-related adverse events, were recorded every visit. Twelve weeks after the end of SOF/DAC treatment, patients were tested for SVR12 HCV-RNA, serum ferritin level, a pelvi-abdominal ultrasound, and non-invasive assessment of liver fibrosis by FIB-4 and APRI. Change in blood transfusion and iron chelators requirements compared to baseline was also recorded.

The primary aim of our study was to assess the effectiveness of SOF/DAC regimen in this special population of patients by achievement of SVR as defined by undetectable HCV RNA twelve weeks after the end of therapy. The secondary aim was to study the safety and tolerability of DAAs in this special population of patients. All treatment-related adverse events were noted.

All results were collected, tabulated, and statistically analyzed using computer software (IBM SPSS ver. 22). Descriptive statistical tests of frequency, mean, and standard deviation (SD) were used to describe the obtained data. Moreover, different variables were compared before and after treatment using paired T-test (for parametric data) and related-sample Wilcoxon signed-rank test (for non-parametric data).

Results

Study population

This study included 21 patients with CHA recruited from our institution. These patients included 11 females (52.4%) and 10 males (47.6%), with age ranging between 18 and 62 years (median 33 years). Most of the patients were diagnosed with β-thalassemia (12 patients with thalassemia major [57.1%] and 6 patients with thalassemia intermedia [28.6%]). All patients were treatment-naïve apart from one patient who had been previously treated with PEG-INF (95.2% vs 4.8%, respectively). All patients were either non-cirrhotic or compensated liver cirrhosis (Child A/B). Decompensated cirrhotic patients were excluded from the study. The rest of patients’ characteristics and baseline laboratory investigations are summarized in Tables 1 and 2.

Table 1 Baseline demographic, clinical, and laboratory data for enrolled patients with CHA and HCV infection (n=21)
Table 2 Comparison between baseline and end-of-treatment laboratory investigations among enrolled patients with CHA and HCV

Patients received iron chelator therapy as follows: desferoxamine was given intravenously at a dose of 40–50 mg/kg/day over 8–12 h for 5–7 days/week. Deferiperone was given orally at an initial dose of 75mg/kg/day, and a maximum dose of 99 mg/kg/day. The total daily dose was divided twice or thrice daily. No dose adjustment was needed for patients with mild or moderate impairment of hepatic function. Deferasirox was given orally at a dose of 10 mg/kg/day with a maximum dose of 20 mg/kg/day. No dose adjustment was required in patients with Child A, while the dose was decreased by 50% in patients with Child B.

Treatment response

Nineteen out of 21 patients (90.5%) achieved SVR 12 weeks after the end of DAA therapy. The only treatment-experienced (TE) patient in the study achieved SVR (100%), while 18 out of 20 treatment-naïve patients (TN) achieved SVR (90%). According to treatment duration, all 8 patients who received treatment for 12 weeks achieved SVR (100%), while 11 out of 13 patients who received treatment for 24 weeks achieved SVR (84.6%). Both non-responders were β-thalassemia major patients with advanced liver disease treated with SOF 400 mg and DAC 60 mg for 24 weeks. They were ineligible to receive RBV to avoid increased frequency of blood transfusion (mean Hb 7.65 g/dl).

The first non-responder was a 33-year-old female patient who presented with baseline HCV-RNA of 1,458,963 copies/ml, elevated transaminases (ALT 61 IU/L, AST 116 IU/L), serum ferritin 577 ng/ml, and advanced liver fibrosis (fibroscan liver stiffness 9.6 kPa, F3). She was kept on Deferasirox for iron chelation. The patient was retreated using ritonavir-boosted paritaprevir/ombitasvir and SOF for 24 weeks due to RBV ineligibility and achieved SVR.

The second non-responder was a 32-year-old male patient who presented with baseline HCV-RNA >4 million copies/ml, elevated transaminases (ALT 66 IU/L, AST 99 IU/L), serum ferritin 1670 ng/ml, and advanced liver fibrosis (fibroscan liver stiffness 34.8 kPa, F4). He was kept on deferiprone for iron chelation. The patient was retreated with SOF, DAC, and simeprevir for 24 weeks, and achieved SVR.

Among the studied group, the hemoglobin and ferritin levels did not change after treatment from baseline levels (p<0.501 and p<0.339, respectively). Similarly, the mean total serum bilirubin did not show a significant difference between baseline and post-treatment levels (2.62±1.11 vs 2.49±1.48 mg/dl, respectively, p<0.542). However, ALT levels dropped significantly at the end of treatment compared to baseline levels (41.41± 24.02 IU/L vs 54.48 ± 22.9, respectively, p<0.009).

The non-invasive assessment of liver fibrosis pre- and post-treatment showed significant improvement in APRI (0.44±0.27 vs 0.32±0.22, p<0.046) but not in FIB-4 scores (0.78±0.7 vs 0.61±0.5, p<0.175) in this population.

The frequency of blood transfusion was assessed by regular monthly follow-up of patient-reported blood transfusion, followed by calculation of mean transfusion amount throughout treatment period and comparing it to baseline mean transfusion requirements. The frequency did not change in the majority of patients. At the end of the DAA treatment period, 12 patients (57.14%) had no change in their blood transfusion requirements and one patient (4.76%) had a decrease in his requirements, while 8 patients (38.1%) had an increase in their requirements, rising from 293.75 ml/month at baseline to 697.89 ml/month at the end of treatment period.

Similarly, the requirements for iron chelation therapy after the end of treatment showed no change among 15 patients (71.4%) and 4 patients (19%) had decreased requirements, while 2 patients (9.5%) had increased requirements.

Safety

Apart from minor adverse events, e.g., dizziness and anorexia (Table 3), one patient with β-thalassemia major who received SOF/DAC for 24 weeks experienced a severe adverse event necessitating immediate withholding of therapy. The patient presented with dyspnea and hepatic decompensation at week 16 and Child-Pugh score deteriorated from A5 to B7. Laboratory investigations revealed hypoalbuminemia (1.9 g/dl vs 3.7 g/dl at baseline) and hyperbilirubinemia (2.6 mg/dl vs 1.9 mg/dl at baseline). A computed tomography of the chest revealed bilateral pleural effusion, and a small rim of pericardial effusion. The patient was admitted to the hospital for management and follow-up. All lab parameters improved thereafter, and the patient achieved SVR.

Table 3 Adverse events reported during treatment

Another patient experienced a sickle cell crisis at week 12; vaso-occlusive painful crises with generalized severe bone pains and chest pain which resolved by intravenous fluid replacement therapy and packed RBCs. This patient had another episode of sickle cell crisis 3 month following the completion of DAA treatment, which increases the possibility of a non-treatment-related adverse event.

Discussion

HCV infection represents a major clinical health issue in patients with CHA. About 70–80% of infected patients develop chronic hepatitis and up to 20% progress to cirrhosis [12].

The introduction of DAAs has dramatically changed HCV treatment due to its high efficacy (>90%) and superior safety profile compared to INF-based therapy. Although limited data exist on the use of DAAs in hepatitis C patients with chronic hemolytic anemias, current guidelines recommend using DAAs in this group of patients [8].

The current study showed a high SVR of 90.5%, which agrees with other studies done on this special population of patients by Nagral and Alvi and their colleagues showing SVR of 100% using different DAA regimens including fixed dose combination of Ledipasvir (LED/SOF) with and without RBV, and fixed dose combination of Velpatasvir/SOF, in addition to SOF/DAC [7, 13].

Moreover, a large multi-center phase 3 study done on 156 patients with different inherited blood disorders including β-thalassemia and sickle cell anemia reported SVR of 93.5% using fixed dose combination of elbasvir/grazoprevir for 12 weeks [14]. This variability in the treatment regimens used further proves the efficacy of different DAA regimens in management of HCV in patients with CHA.

In contrast, the high SVR in our study differs from a multi-center study done by Di Marco et al. on 230 patients with thalassemia major, which showed very low SVR ranging from 37 to 62% across different HCV genotypes. The main explanation for this contradiction is due to the fact that this study used Peg-interferon (Peg-INF) and RBV not DAAs [15].

Our study achieved complete cure of a single patient with sickle cell anemia, agreeing with a study done by Moon et al. including 10 patients with SVR achieved in 9 patients and failure of only one patient due to drug non-compliance, although in that study, fixed dose combination of LED/SOF was used [16].

Our results therefore confirm that the advent of DAAs has revolutionized the treatment of CHC in subjects with CHA. Not only the rate of premature withdrawal because of adverse events has been reduced to zero while it was as high as 25% with INF-containing regimens, but also the achievement of SVR has dramatically increased from a range of 28 to 66% in patients under INF monotherapy, and from a range of 31 to 93% in patients treated with PEG-INF and RBV to results close to 100% in patients treated with DAAs [15].

This study showed that there was a statistically significant reduction in ALT at end-of-treatment, agreeing with other different studies on patients with thalassemia major (p<0.009) [8, 14, 17]. The significant drop in ALT paralleled the drop in the levels of HCV RNA. This could be attributed to the reduction in the liver parenchymal inflammation.

A prospective Indian study assessing the safety and efficacy of SOF-based DAAs including 29 thalassemic patients showed significant decline in serum ferritin levels after treatment despite an increase in transfusion requirements during treatment [18]. Similar results have been presented by Nagral, Alvi, Ponti, and their colleagues [13, 19, 20]. Similarly, the present study showed that there was a decline in serum ferritin at end-of-treatment although it was not statistically significant (1807.63±1480.36 vs 1762.63±1918.7 ng/ml, p<0.339). This decline could be due to the use of chelation therapy prior to initiation of DAA therapy to prevent iron overload.

The change in Hb levels was not statistically significant when compared pre- and post-treatment as the study conducted by Nagral and his colleagues [20].

The effect of new antivirals on blood consumption in our cohort was negligible, 38.1% of the patients experienced increase in blood requirements while the majority (57.14%) did not experience any change in transfusion requirements.

In the present study, most patients (71.4%) had no change in their iron chelator requirements, 4 patients (19%) had a decrease, while 2 patients (9.5%) had an increase in their requirements. This comes in accordance with other studies in which there was no significant difference in requirements of iron chelators when compared pre- and 3-month post-treatment [17, 20].

Most patients did not experience any side effects during treatment, and the side effects reported were negligible in comparison with those depicted in previous antiviral regimens including INF. The most relevant side effect was hepatic decompensation in one patient which necessitated treatment discontinuation.

Conclusion

RBV-free DAAs are considered safe, tolerable, and effective modalities in treatment of hepatitis C patients with CHA. Microelimination of HCV in special patients’ populations is currently the accepted pragmatic approach to aid in achieving global goals for elimination of HCV worldwide. However, this study was limited by relatively small sample size, and absence of patients with decompensated liver cirrhosis. More studies are needed to address such aspects in the future.

Availability of data and materials

The datasets used and analyzed during the current study are available from corresponding author upon reasonable request.

Abbreviations

ALT:

Alanine aminotransferase

AST:

Aspartate aminotransferase

CBC:

Complete blood count

CHA:

Chronic hemolytic anemia

DAAs:

Direct-acting antivirals

DAC:

Daclatasvir

HBV:

Hepatitis B virus

HCV:

Hepatitis C virus

HIV:

Human immune-deficiency virus

INR:

International normalization ratio

LED:

Ledipasvir

PEG-INF:

Pegylated interferon-α

RBV:

Ribavirin

RT-PCR:

Real-time polymerase chain reaction

SOF:

Sofosbuvir

SVR12:

Sustained virological response at 12 weeks post-treatment

WHO:

World Health Organization

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WH formulated the research idea and shared in the data collection, analysis, and manuscript revision. ME supervised the data analysis and manuscript drafting. OA shared in the manuscript revision. HD, MS, and AS analyzed the collected data and revised the final manuscript. MN shared in the data collection and manuscript drafting. SI shared in the statistical analysis of collected data, together with manuscript revision. AM shared in formulation of research hypothesis, data processing, statistical analysis, and drafting of final manuscript. All authors have read and approved the final manuscript.

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Correspondence to Ahmed Mansour.

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All subjects involved in the study signed an informed written consent to participate. The study was approved by the Ethical Review Board of our institution (Reference Number: FMASU M S 67/2019). The study protocol conforms to the ethical guidelines of the 1975 Declaration of Helsinki as reflected in a priori approval by the institution’s human research committee.

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Hashem, W.M., El-Sayed, M.H., Ahmed, O.A. et al. Microelimination of hepatitis C in patients with chronic hemolytic anemias: a single-center experience. Egypt Liver Journal 11, 48 (2021). https://doi.org/10.1186/s43066-021-00117-4

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Keywords

  • Microelimination
  • Hepatitis C
  • Anemia
  • Hemolytic
  • Thalassemia
  • Antiviral agents
  • Daclatasvir
  • Sofosbuvir