Name of journal: World Journal of Gastroenterology esps manuscript no: 12307 Columns: Topic Highlight


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Although some studies have failed to find a negative impact on clinical outcomes after KT[126,127], the majority of studies so far reported indicate that HCV infection is associated with increased liver-related mortality and fibrosis progression among HCV-infected KT patients, with a significant reduction in patient and graft survival, possibly related to accelerated fibrogenesis and increased liver damage induced by the use of immunosuppressive regimens[88,91–93,123,128–133]. Recent evidence also suggests that KT recipients with chronic HCV infection have an increased risk of post-transplant de novo glomerulonephritis[89,90,134], diabetes mellitus[90,135], and azathioprine hepatotoxicity[136].

In contrast to what is observed in CKD patients under dialysis, HCV-positive KT recipients more often present with false-negative anti-HCV results, even with newer immunoassays[63,137]. In a recent study, 19 out of 417 KT recipients were HCV RNA-positive and 3 of those patients (16%) were anti-HCV-negative by using chemiluminescence immunoassays[63]. This inability to mount an antibody response against HCV is probably related to the immunosuppressive therapy. Another consequence of immunosuppression is the significant increase in HCV viral load, with no reports of intermittent viremia so far[9,138]. Interestingly, similarly to hemodialysis subjects, there is a very low prevalence of occult HCV infection in KT recipients[63].

There is still no consensus on the best immunosuppressive strategy in HCV-positive KT recipients. Antiviral activity of cyclosporine A (CsA), probably acting by antagonizing the effect of cyclophilin B on HCV replication[139], has been demonstrated both in vitro and in vivo[139–143], and it is possible that CsA may exert a beneficial effect on necroinflammatory activity in HCV-related liver disease among KT recipients[144–146].

Additional differences from hemodialysis patients are the higher prevalence of advanced liver disease in KT recipients[59,91,92], and the better accuracy of aminotransferases for the prediction of significant histological lesions[147–149]. Although liver biopsy is still recommended to evaluate the severity of hepatic lesions in patients on hemodialysis patients as well as in transplant recipients[150,151], several noninvasive methods for the assessment of liver fibrosis have been studied in HCV-positive KT patients, including simple blood tests[58], Fibrotest[85,152], and liver elastography[152,153], with fair diagnostic performances. In selected cases, these methods can be used as alternatives to liver biopsy. Screening for hepatocellular carcinoma and esophageal varices is indicated for patients with advanced fibrosis or cirrhosis.

As for antiviral therapy, there are several heterogeneous studies including small series of HCV-infected KT patients (ranging from 3 to 32 subjects), treated with standard or pegylated IFN alone or in combination with low dose ribavirin[154–170] (Table 4). Seventeen studies have been compiled in 2 meta-analyses[94,171], and the mean overall estimates for SVR with IFN monotherapy (10 studies), IFN plus ribavirin (4 studies) and PEG-IFN plus ribavirin (3 studies) were 16%, 36% and 43%, respectively.

Despite initial concerns about increased risk of graft dysfunction and loss, ranging from 0% to 40% in early studies[159–162,166], more recent series have shown lower graft rejection rates, between 0 and 5%[167–170]. Advances in immunosuppression therapy and the use of the less immunogenic PEG-IFN are possible explanations for this observation. However, dropout rates remain high (mean incidence of 28%) and do not differ greatly between early and recent studies[154–170], probably due to the worse anemia found in those receiving IFN in combination with ribavirin.

AASLD and KDIGO guidelines recommend against antiviral therapy for HCV-infected KT recipients, with the exceptions of fibrosing cholestatic hepatitis or life-threatening vasculitis[150,172]. Nevertheless, treatment with PEG-IFN and ribavirin should be considered for patients with advanced fibrosis, always taking into account time after transplantation, eGFR and renal function stability.

With the aid of EPO supplementation (doses up to 40000 IU/wk to maintain hemoglobin levels  10 g/dL), an initial ribavirin dose of 200 mg once a day is given, followed by increments of 200 mg every two weeks until the maximum dose tolerated, with target dosage of ribavirin defined according to eGFR (Table 2). After stabilization of ribavirin dosage (usually between 400 to 800 mg/d), interferon is initiated and used for 48 wk, irrespective of HCV genotype. Even in absence of comparative trials, it is suggested to use PEG-IFN (preferably PEG-IFN alfa-2a 135 g) once a week, after dialysis session, in combination with ribavirin (see Figure 3). There are no studies supporting the use of DAAs for the treatment of KT HCV-positive recipients, but it is expected that these patients will benefit from interferon-free regimens.

Treatment with IFN (standard or pegylated) and ribavirin is associated with frequent and sometimes serious side effects[173,174]. Among the latter are autoimmune diseases (worsening or de novo thyroid disorders, diabetes mellitus, psoriasis, etc.), significant hemolytic anemia and severe depression. In a recent meta-analysis of eleven clinical studies published by Fabrizi et al[103], the summary estimate for dropout rate was 0.18 (95%CI: 0.08-0.35), with a large heterogeneity across studies, mainly due to anemia (24%) and infections (13%).

Except from hemolytic anemia, side effects are mainly related to IFN. The majority of the patients receiving IFN presents with a flu-like syndrome, characterized by diffuse myalgia, headache, fatigue and fever. Generally, these symptoms are self-limited and managed by common analgesics. Depression can be induced by IFN in 20% to 30% of the cases, usually after three months of treatment[175]. Being mild to moderate in intensity, IFN-induced depression can generally be handled with conservative measures, by non-psychiatrist professionals. However, if severe depression develops, HCV treatment must be stopped and the patient should be immediately referred to a psychiatrist. IFN-induced cytopenias (thrombocytopenia and leucopenia), are relatively common, typically dose-dependent and rarely associated with clinically significant complications, even in CKD patients. IFN dose reductions and the use of growth factors usually allow the continuation of therapy[173,174].

On the other hand, as previously discussed, the ribavirin-induced hemolytic anemia is very common and troublesome in CKD patients, due to its severity and potential noxious consequences in these subjects with high cardiovascular risk. Initial low doses of ribavirin, early dose reductions, and EPO supplementation are the main strategies for the management of anemia in this context. It should be mentioned that ribavirin can carry an increased risk of birth defects, and proper contraception during and up to six months after therapy must be adopted. Minor side effects like cough and skin rash also seem to be mostly associated with ribavirin[173,174].

With the first-generation HCV protease inhibitors (PIs), boceprevir and telaprevir, complex drug-to-drug interactions and tolerability issues remain a concern[176,177]. Boceprevir is associated with an increased incidence of anemia and dysgeusia and telaprevir is associated with an increased incidence of dermatological disorders, anemia, and anorectal symptoms[178-181]. An approximately 15% to 26% increase in anemia incidence in patients under triple therapy with boceprevir or telaprevir has been observed[178-181]. In these patients, anemia is considered the consequence of the combined effects of ribavirin-induced hemolysis and the bone marrow suppression of IFN and PI. In the same manner of dual therapy, ribavirin dose reductions and EPO are used for the management of anemia, although blood transfusions are also frequently required. Dysgeusia and anorectal symptoms are infrequently severe and often improve under conservative measures and dietetic modifications. A wide spectrum of dermatological disorders has been described in approximately 50% of the patients treated with first-generation PIs, particularly with telaprevir, ranging from simple pruritus with or without rash to severe skin reactions like Stevens-Johnson’s syndrome or DRESS syndrome[182]. Emollients/moisturizers and topical corticosteroids are sufficient for most cases (90% to 95%), but dermatological consultations are frequently needed for more severe cases. Treatment discontinuation is required in about 6% of patients[182].

In spite of the increment in SVR rates with the use of the first-generation PIs telaprevir and boceprevir in subjects with preserved renal function, the higher incidence of significant side effects (mainly severe anemia and dermatological reactions) and the frequent drug-drug interactions have hampered their widespread use in difficult-to-treat populations, such as CKD patients. Newer DAAs, like sofosbuvir (a nucleotide NS5B polymerase inhibitor), simeprevir (a second generation PI), and daclatasvir (a NS5A replication complex inhibitor), with or without PEG-IFN and/or ribavirin, or used in different combinations with one another, produces SVR rates superior to 90%)[183-188]. Besides leading to the highest SVR rates ever seen, these emerging DDAs seems to exhibit a reduced potential for drug-drug interactions and a better safety profile, which will probably facilitate their use for the treatment of HCV infection in CKD subjects. However, the appropriate dose of sofosbuvir has not been identified for subjects with severe renal impairment (eGFR < 30 mL/min per 1.73 m2) or hemodialysis patients and dose adjustments might be necessary[189]. Likewise, although simeprevir is primarily metabolized by the liver and its renal elimination is minimal, the safety of the drug has not been evaluated in patients with CKD stages 4 and 5. Conversely, unpublished data suggested that dose reduction would not be needed for the use of daclatasvir in patients with any stage of renal impairment. Finally, a phase 3 study will evaluate the safety and efficacy of the all-oral and IFN-free combination therapy with ombitasvir (a NS5A replication complex inhibitor), paritaprevir (ABT-450, a second-generation PI) and dasabuvir (a non-nucleoside NS5B polymerase inhibitor), with or without ribavirin, for the treatment of genotype 1-infected CKD patients ( identifier NCT02207088)[190].


HCV infection is highly prevalent among CKD subjects and, consequently, in KT recipients, exerting a significant negative impact on clinical outcomes both before and after KT. Although interferon-based antiviral therapy in CKD patients is associated with poor tolerability and suboptimal efficacy, there has been mounting evidence that many patients can benefit from treatment. In those individuals, accurate characterization of liver disease and adequate assessment of comorbidities are mandatory for optimal management and therapeutic decisions.


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