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Saudi Journal of Kidney Diseases and Transplantation
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Table of Contents   
ORIGINAL ARTICLE  
Year : 2017  |  Volume : 28  |  Issue : 4  |  Page : 764-773
Assessment of hepatic fibrosis by fibroscan in egyptian chronic hemodialysis patients with chronic Hepatitis C (genotype 4): A single-center study


1 Department of Internal Medicine and Nephrology, Faculty of Medicine, Cairo University, Cairo, Egypt
2 Department of Endemic Medicine and Hepatology, Faculty of Medicine, Cairo University, Cairo, Egypt
3 Medical Biochemistry and Molecular Biology, Faculty of Medicine, Cairo University, Cairo, Egypt

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Date of Web Publication21-Jul-2017
 

   Abstract 


Assessing hepatic fibrosis in hemodialysis patients with chronic hepatitis C (CHC) can help to evaluate the long-term prognosis, complications of hepatitis C virus (HCV) as well as eligibility for renal transplantation,. Our aim was to assess liver fibrosis in Egyptian hemodialysis (HD) patients infected with CHC genotype 4 using a fibroscan. This cross-sectional observational study was conducted over two years on a cohort of 134 Egyptian patients on prevalent HD at Kasr Al Ainy Hospital. All patients were subjected to routine laboratory evaluation including, hepatitis B surface antigen, hepatitis B core antibody, hepatitis Be antigen, hepatitis C antibody (HCVAb) and human immunodeficiency virus antibody, quantitative polymerase chain reaction (PCR) for both HCV and hepatitis B virus (HBV), serum hyaluronic acid level, and alpha-fetoprotein (AFP). Fibroscan was performed on all HCV-positive patients. The mean age was 47.43 ± 12.65 years, 50.7% were male, and 49.3% were female. The most common causes of end-stage renal disease were hypertensive nephropathy (32.1%) and diabetic nephropathy (18.7%). HCVAb was positive in 57.5% of the patients and HBV was positive in 3%. Forty HCV-positive patients (57.1%) who underwent fibroscan had mild to significant fibrosis, and thirty patients (42.9%) had advanced fibrosis. There was significant correlation between HCV PCR and duration on HD, number of blood transfusions, and hyaluronic acid (HA) level. In addition, there was a significant correlation between serum HA and HD duration as well as liver fibrosis. No significant correlation was found between duration on HD and fibrosis stage (P = 0.619); also, no significant correlation was noted between the age of the patients and HA level or stage of fibrosis (P = 0.970). Fibro-scan is a simple noninvasive test that can be used to assess liver fibrosis in HD patients with CHC. Most of the study patients had mild to significant fibrosis.

How to cite this article:
Zayed BE, Elsharkawy A, Abdou M, Abd Al Fatah DS, El-Shabony TH. Assessment of hepatic fibrosis by fibroscan in egyptian chronic hemodialysis patients with chronic Hepatitis C (genotype 4): A single-center study. Saudi J Kidney Dis Transpl 2017;28:764-73

How to cite this URL:
Zayed BE, Elsharkawy A, Abdou M, Abd Al Fatah DS, El-Shabony TH. Assessment of hepatic fibrosis by fibroscan in egyptian chronic hemodialysis patients with chronic Hepatitis C (genotype 4): A single-center study. Saudi J Kidney Dis Transpl [serial online] 2017 [cited 2022 Jul 1];28:764-73. Available from: https://www.sjkdt.org/text.asp?2017/28/4/764/211338



   Introduction Top


Hemodialysis (HD) patients with hepatitis C virus (HCV) infection are at increased risk for death whether they remain on HD or undergo kidney transplantation,[1] with prediction of worse outcomes after kidney transplant. Assessing hepatic fibrosis among HD patients with chronic hepatitis C (CHC) can help to evaluate the eligibility for renal transplantation, the necessity for HCV treatment, the long-term prognosis, and complications related to portal hypertension and hepatocellular carcinoma. Few studies have been performed using ultrasound transient elastography (TE, Fibroscan) to predict the severity of hepatic fibrosis in this group of patients.

The standard of care of therapy of HCV with interferon (IFN) and ribavirin is of limited utility in these patients due to lack of tolerability and suboptimal response rates.[3] It is of major concern since HCV infections continue to be transmitted between chronic HD patients within their treatment facilities.[4]

The KDIGO guidelines (2008)[5] weakly recommended monotherapy with pegylated IFN with doses adjusted to the level of kidney function for HCV-infected patients with chronic kidney disease (CKD) stages 3, 4, and 5 not yet on dialysis, and monotherapy with standard IFN for CKD stage 5 on maintenance HD that is dose-adjusted for a glomerular filtration rate <15 mL/min/1.73 m2.

Simeprevir, daclatasvir, and the combination of ritonavir-boosted paritaprevir, ombitasvir and dasabuvir are cleared by hepatic metabolism and can be used in patients with severe renal disease according to the EASL recommendation.[6]

The prevalence of HCV infection among HD patients is significantly higher than in healthy blood donors and in the general population. HD patients are at risk for HCV due to the involvement of multiple routes of infection, low standard of dialysis procedures and the unmet needs to apply infection control practices.[7] Although percutaneous liver biopsy (PLB) is the gold standard for staging hepatic fibrosis in HD patients with CHC before renal transplantation or anti-viral therapy, some concerns exist about serious postbiopsy complications.[8] Many studies have been performed to evaluate the role of the non-invasive measures in the assessment of liver fibrosis, especially fibroscan; they concluded that fibroscan could be used for easy and reliable prediction of liver fibrosis in chronic HCV patients.[9],[10],[11]

This study was based on the results of a previous study by Liu and Kao who concluded that TE is superior to aspartate aminotransaminase (AST) in assessing the severity of hepatic fibrosis in patients with CHC.[12]

The aim of this study is to evaluate the efficacy of TE in the diagnosis and staging of hepatic fibrosis instead of PLB among chronic HCV genotype 4 maintenance HD patients.


   Patients and Methods Top


This is a cross-sectional observational study conducted from July 2012 to March 2014 on a cohort of 134 Egyptian patients on chronic HD at Kasr Al Ainy Hospital aged between 18 and 67 years, on HD for more than one year.

Each participant gave written informed consent before enrollment. Patients with causes of chronic liver diseases other than HCV were excluded from the study.

All patients were subjected to viral markers including hepatitis B surface antigen (HBs Ag), hepatitis B core antibody, hepatitis Be antigen, hepatitis C antibody (HCVAb), and human immunodeficiency virus antibody. Quantitative polymerase chain reaction (PCR) for both HCV and hepatitis B virus (HBV) and serum hyaluronic acid (HA) level, and alpha-fetoprotein (AFP) were also performed. Abdominal ultrasound for HCV-infected patients was performed. Liver fibrosis measurement using TE (fibroscan) was performed for HCV-positive patients at Kasr Al-Ainy viral hepatitis center by an experienced operator and by the same technique previously described by Castéra et al.[13] The results were expressed in kilopascals, and the classification used for fibroscan stiffness was that described by De Lédinghen and Vergniol:[14]

F0: ≤5.4 kpa

5.5-5.9 = F0-F1

6-6.9 = F1

7-8.7 = F1-F2

8.8-9.4 = F2

9.5-12.4 = F3

12.5-14.4 kPa = F3-F4

≥14.5 = F4

The procedure was performed with the patients lying in the supine position with the right arm fully abducted behind the head to facilitate probe access. The tip of the probe was placed on the skin of the right intercostal space at the level of the right hepatic lobe where liver biopsy would be performed.

The results of liver stiffness measurement LSM (EXPAND) were expressed in kPa with a median value of at least 10 valid measurements and a successful rate of more than 60%.

LSM failure was defined as zero valid measurement, and unreliable examinations were defined as less than 10 valid measurements, a successful rate of less than 60%, or the interquartile range more than 30% of the median LSM value.

There were seven cases who were HCV-positive who did not undergo fibroscan; five of these patients died during the time of the study, one had ascites, and one underwent renal transplantation.

Methodology of laboratory tests

Five mL of blood was taken from every participant under complete aseptic conditions and were divided into two portions; 3 mL of whole blood was collected in sterile ethylene diamino tetraacetic acid containing tubes for DNA extraction, and the remaining was left for 30 minutes for spontaneous clotting at room temperature and then centrifuged at 3000 rpm for 10 min. Serum samples were separated into another sets of tubes and kept frozen at −70°C for analysis of laboratory parameters. All patients were subjected to the following tests:

  1. Estimation of serum urea, creatinine, alanine amino transaminase, AST measured using the conventional colorimetric method and α-fetoprotein, which was assessed by ELISA kit according to manufacturer’s instructions
  2. Detection of HBsAg by ELISA kit
  3. Detection and quantification of HBV by Artus HBV kit on applied biosystem realtime PCR instrument. This was performed using real-time PCR device, step one (applied biosystem Foster city, USA) using QIAamp MinElute Virus Spin protocol Calculation of DNA viral load was by following the standard curve [Figure 1].
  4. Determination of HCV RNA level.
  5. Figure 1: Standard curve for calculation of qPCR of hepatitis B virus.

    Click here to view


    Blood samples that were centrifuged for serum collection were stored at −20°C or −80°C until usage. RNA extraction from stored frozen samples was performed using QIAamp viral RNA Mini kit (QIAGEN) according to the manufacturer’s instructions supplied with the kit. Extracted RNA was measured and quantitated with UV spectro-photometer at 260–280 wave length. An RT-PCR assay using TaqMan (fluorescence-based real-time PCR), and probes was designed for the quantitative determination of HCV RNA in the clinical blood samples. Absolute quantitation of the concentration of HCV RNA was based on an external standard curve (HCV Standards IU/mL) in the presence of an internal positive control (IPC). IPC was added to mixture of lysis buffer and sample material during RNA extraction of clinical blood samples.

    Calculation of RNA viral load was made by using the standard curve [Figure 2].
    Figure 2: Standard curve for calculation of qPCR of RNA of hepatitis C virus.

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  6. Serological markers: HBs Ag, HBe Ag, HBc Ab, HCV Ab and Anti-HIV, were tested by commercial enzyme-linked immunoassays ELISA (DiaSorin, Italy).
  7. HA assessment was made using Corgenix, Suite 400, Broomfield, CO USA, ELISA kit. All protocols followed the manufacturers’ instructions. Each ELISA test was run in duplicate, with mean absorbance computed from the average for two wells normalized to a zero calibrator well.



   Statistical Analysis Top


The data were analyzed using Statistical Package of Social Science (SPSS) program version 15.0 (SPSS Inc., Chicago, IL, USA). Data were summarized as mean. We performed t-test for analyzing two quantitative data and nonparametric test (Mann–Whitney U-test) when data were not symmetrically distributed. Pearson’s correlation was considered weak for r <0.25, mild for >0.5, moderate for > r ≥0.5, and strong for r ≥0.75. P ≤0.05 were considered statistically significant.


   Results Top


The demographic features of all studied patients are shown in [Table 1]. HCV infection was higher among patients on dialysis for more than five years (P <0.001), and HA was higher among HCV positive than HCV-negative patients (P <0.001). There was no significant difference in age (P = 0.206) or serum AFP (P-value 0.827) among HCV-positive and negative patients [Table 2].
Table 1: Demographic features of the studied population.

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Table 2: Age, duration of dialysis, and laboratory data among hepatitis C virus polymerase chain reaction Positive and negative patients.

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The percentage of HCV-positive patients below the age of 40 years (61.9%) was higher than those above 40 years (55.4%; P = 0.482). The number of HCV-positive male patients was nearly equal to the number of HCV-positive female patients (P = 0.979). The duration on dialysis was related to HCV infection; the number of HCV-positive patients on HD for more than five years was significantly higher than those on less than or equal to five years on HD (P <0.001).

The frequency of blood transfusion affected the incidence of HCV. Patients who received blood transfusion(s) had significantly higher HCV positivity than those who did not receive blood (P <0.001).

Assessment of LSM using fibroscan was performed on 70 out of 77 HCVAb-positive patients; there was no fibrosis in 16 patients, mild to significant fibrosis in 24 patients, and advanced fibrosis and cirrhosis in 30 patients.

The percentage of patients on HD for less than or equal to five years who are staged <F3 (71.4%) was higher than those on HD for more than five years (57.1%).

The degree of fibrosis was not related to the etiology of renal disease. Among patients who were within F1–F2 stage, 33.3% had diabetic nephropathy, 33.3% of patients had chronic glomerulonephritis, and among F4, 50% of patients had hypertensive nephropathy (P= 0.216).

[Table 4] shows that there was a significant difference between the serum HA level among different stages of fibrosis (P = 0.005); this relation was not found with HCV PCR or serum AFP; P = 0.198; and P = 0.153, respectively.

We observed a strong correlation between duration on HD, HCV PCR, and stage of fibrosis and serum HA levels (P = 0.003, r = 0.252; P = 0.029, r = 0. 249; P = <0.001, r = 0.758, respectively. There was no correlation between duration on HD and stage of fibrosis (P = 0.228), age of the patients, and HA or stage of fibrosis (P = 0.619; and P = 0.970), respectively [Table 3].
Table 3: Fibrosis stages and hemodialysis duration.

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No significant correlation was found between fibrosis and both age and gender of the patients [Table 4] and [Table 5].
Table 4: Hepatitis C virus polymerase chain reaction, Alpha-fetoprotein, and hyaluronic acid among patients with different fibrosis stages.

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Table 5: Correlation between hyaluronic acid and fibrosis stages with different parameters.

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We observed a strong correlation between level of serum HA and stage of fibrosis; P = 0.002) [Table 6]. The receiver operating characteristic curve was used to test the validity of HA in discriminating those with advanced fibrosis ≥F3 from those ≤F3. The area under the curve was found to be 0.967 with P ≤0.001. The HA level was ≥54.00 ng/mL showing a sensitivity and specificity of 70% while the level ≥1.50 ng/mL showed sensitivity of 88.9% and specificity of 100% [Figure 3].
Table 6: Relation between fibrosis stage and age groups.

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Figure 3: Receiver operating characteristic curve to test the validity of hyaluronic acid in discriminating those with F3 stage and higher from those staged less than F3.

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   Discussion Top


Egypt has the highest prevalence of hepatitis C in the world (17%–26%)[15] and the prevalence of HCV antibodies in HD patients ranged from 52.3% to 82.3%.[16] Liu and Kao,[12] reported that TE is useful in assessing the severity of hepatic fibrosis and can substantially decrease the need of staging PLB in HD patients with CHC. Thus, in our study, we did not perform liver biopsy as reference standard based on the previous studies for fear of bleeding which may be fatal in some cases[Table 7] and [Table 8].
Table 7: Relation between fibrosis stage and gender.

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Table 8: Correlation between hyaluronic acid and fibrosis in patients less than and more than 5 years of hemodialysis.

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The percent of HCV-positivity in patients below 40 years was high, and this high prevalence of HCV among young generations in Egypt may be due to high prevalence of HCV infection in our country in the last decades. The HCV prevalence was equal between male and female patients in our study, as in the study of Anwar et al.[17] The percentage of patients on HD for ≤5 years was 61.9% while those on HD for more than five years were 38.1%, with mean duration of 5.96 ± 4.12 years. This may be attributed to the increase in the mortality rate which occurs with increasing duration of HD possibly due to cardiovascular complications, bleeding, sepsis, or vascular access complications. In an earlier study performed by Zahran in 2011,[18] the mean duration on dialysis was found to be 3.4 ± 3.13 years.

We observed a significant difference between the mean duration on HD among HCV positive and negative patients, as was observed by Salama et al.[19] In addition, greater dialytic age might increase cumulative HCV infection risk from exposure in the HD unit, as well as other non-HD health-care exposures. A number of studies have suggested that environmental transmission within dialysis units is a major risk factor for HCV transmission in HD[20],[21],[22] patients. Chronic HCV infection was more prevalent among cases with chronic glomerulonephritis (79.2%), diabetes (52.0%), and obstructive uropathy (55.0%), which could be explained by the observation that CHC can induce GN many years after initial infection with HCV.[23] Cirrhosis and hepatocellular carcinoma (HCC), have been implicated as causes of increased mortality in HD patients with HCV infection.[24],[25] On ultrasound examination of the HCV-positive cases, we did not report any cases of HCC or cirrhosis. Cirrhosis in HCV infection is an immune-mediated reaction, which is impaired in HD patients, and HCC is also a consequence of cirrhosis. Several studies have stated that HCV disease activity in HD patients is mild, and is not progressive, perhaps due to immunological abnormalities in these patients.[26]

A single-center study that evaluated histologic severity of liver disease among patients who had hepatitis C and were awaiting kidney transplantation found that up to 22% of CHC have advanced hepatic fibrosis.[27]

Most of the studied cases had mild-to-significant fibrosis, reflecting the slow process of fibrosis, which may depend on the adaptive immunity of the host in localizing the virus.

This has been explained by Bahadi et al that HCV disease activity in HD patients is mild and is not progressive, perhaps due to immunological abnormalities in these patients.[26]

A study was performed by Fouad et al[28] to assess the costimulatory and coinhibitory markers of dendritic cells in chronic HCV-infected subjects, in chronic HD patients and control group. There was a significant elevation of interleukin (IL-10) and HA levels in chronic HCV patients; IL-10 was higher, and HA was lower in HCV uremic subjects undergoing HD.

HA level can be a good non-invasive marker of significant fibrosis in patients with hepatitis C in end-stage renal disease instead of liver biopsy to avoid severity of complications of liver biopsy in patients with renal failure.[29]

There is a strong correlation between duration on HD and serum HA; longer the patient stays on HD, stronger is the inflammatory process associated with chronic HD and higher level of HA.

It has been previously reported that the time span on HD and certain markers of chronic inflammation, such as dialysis-related amyloid, correlate with serum HA levels, and cytokine production that may be stimulated by contact of the blood with bioincompatible dialysis membranes, and cytokines have been shown to stimulate the synthesis of HA.[30]

However, a study by Avila et al[31] in Brazil found that the length of time on HD did not correlate with HA levels and the reasons for that were uncertain. However, two factors in this study should be considered: (a) most of the patients on HD were women and estrogen decreases serum HA levels; and (b) the mean duration on HD in the study was 9.7 years and a significant difference in HA levels can take more than 10 years to be detected.

There is a correlation between the duration on HD and the stage of fibrosis as confirmed by fibroscan. Advanced fibrosis was more among patients who were on HD for more than five years duration. This confirms the observation that prolonged exposure and the long duration of the disease increases the incidence of progression of fibrosis.

Statistically significant correlation was found between HA and stage of fibrosis by fibroscan, being higher among those with advanced stage of fibrosis; this was in agreement with Esmat et al, who stated that HA was associated with fibrosis and that low levels of HA carry a very low risk of fibrosis. According to many other studies, fibroscan was validated as an accurate representative method of fibrosis in chronic HCV patients.[8],[9],[10]


   Limitations of the study Top


Our study had some limitations; we could not perform fibroscan examination for HCV negative patients on regular HD, and we did not perform liver biopsy because of its life-threatening complications.

In conclusion, fibroscan is a safe and easy method for assessment of hepatic stiffness and fibrosis in HD patients with CHC which can help to assess the liver condition before IFN therapy, before transplantation and in assessing the long-term prognosis in those patients.


   Acknowledgment Top


The authors wish to thank all the patients who participated in the study.

Conflict of interest: None declared.



 
   References Top

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Pawlotsky JM, Aghemo A, Back D, Dusheiko G, Forns X, Puoti M, Sarrazin C. EASL Recommendations on Treatment of Hepatitis C 2015. European Association for Study of Liver. J Hepatol 2015;63(1):199-236.  Back to cited text no. 6
    
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Khodir SA, Alghateb M, Okasha KM, Shalaby Sel-S. Prevalence of HCV infections among hemodialysis patients in Al Gharbiyah Governorate, Egypt. Arab J Nephrol Transplant 2012; 5:145-7.  Back to cited text no. 7
    
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Kaw D, Malhotra D. Platelet dysfunction and end-stage renal disease. Semin Dial 2006;19: 317-22.  Back to cited text no. 8
    
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Vignier N, Esmat G, Elsharkawy A, et al. Reproducibility of liver stiffness measurements in hepatitis C virus (HCV)-infected patients in Egypt. J Viral Hepat 2011;18:e358- 65.  Back to cited text no. 9
    
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Esmat G, Elsharkawy A, El Akel W, et al. Fibroscan of chronic HCV patients coinfected with schistosomiasis. Arab J Gastroenterol 2013;14:109-12.  Back to cited text no. 10
    
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Bonnard P, Elsharkawy A, Zalata K, et al. Comparison of liver biopsy and noninvasive techniques for liver fibrosis assessment in patients infected with HCV-genotype 4 in Egypt. J Viral Hepat 2015;22:245-53.  Back to cited text no. 11
    
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Castéra L, Vergniol J, Foucher J, et al. Prospective comparison of transient elastography, Fibrotest, APRI, and liver biopsy for the assessment of fibrosis in chronic hepatitis C. Gastroenterology 2005;128:343-50.  Back to cited text no. 13
    
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de Lédinghen V, Vergniol J. Transient elastography (FibroScan). Gastroenterol Clin Biol 2008;32 6 Suppl 1:58-67.  Back to cited text no. 14
    
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Lavanchy D. Evolving epidemiology of hepatitis C virus. Clin Microbiol Infect 2011; 17:107-15.  Back to cited text no. 15
    
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Afifi A. Annual Reports of the Egyptian Renal Registry; 1996-2008. Available from: http:// www.esnonline.net. Last accessed 12/10/2012.  Back to cited text no. 16
    
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Anwar MI, Rahman M, Hassan MU, Iqbal M. Prevalence of active hepatitis C virus infections among general public of Lahore, Pakistan. Virol J 2013;10:351.  Back to cited text no. 17
    
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Zahran A. Epidemiology of hemodialysis patients in Menofia governorate, delta region, Egypt. Menoufia Med J 2011;24:59-70.  Back to cited text no. 18
    
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Salama G, Rostaing L, Sandres K, Izopet J. Hepatitis C virus infection in French hemo- dialysis units: A multicenter study. J Med Virol 2000;61:44-51.  Back to cited text no. 19
    
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Fabrizi F, Martin P. Health care-associated transmission of hepatitis B and C viruses in hemodialysis units. Clin Liver Dis 2010;14:49- 60; viii.  Back to cited text no. 20
    
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Sulowicz W, Radziszewski A, Chowaniec E. Hepatitis C virus infection in dialysis patients. Hemodial Int 2007;11:286-95.  Back to cited text no. 21
    
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Meyers CM, Seeff LB, Stehman-Breen CO, Hoofnagle JH. Hepatitis C and renal disease: An update. Am J Kidney Dis 2003;42:631-57.  Back to cited text no. 23
    
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Dattolo P, Lombardi M, Ferro G, Michelassi S, Cerrai T, Pizzarelli F. Natural history of HCV infection and risk of death in a cohort of patients on long-term hemodialysis. G Ital Nefrol 2006;23:585-90.  Back to cited text no. 24
    
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Martin P, Carter D, Fabrizi F, et al. Histopathological features of hepatitis C in renal transplant candidates. Transplantation 2000; 69:1479-84.  Back to cited text no. 27
    
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Fouad H, Raziky MS, Aziz RA, et al. Dendritic cell co-stimulatory and co-inhibitory markers in chronic HCV: An Egyptian study. World J Gastroenterol 2013;19:7711-8.  Back to cited text no. 28
    
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de Paula Farah K, Carmo RA, de Figueiredo Antunes CM, et al. Hepatitis C, HCV genotypes and hepatic siderosis in patients with chronic renal failure on haemodialysis in Brazil. Nephrol Dial Transplant 2007;22:2027- 31.  Back to cited text no. 29
    
30.
Plevris JN, Haydon GH, Simpson KJ, et al. Serum hyaluronan – A non-invasive test for diagnosing liver cirrhosis. Eur J Gastroenterol Hepatol 2000;12:1121-7.  Back to cited text no. 30
    
31.
Avila RE, Carmo RA, Farah Kde P, et al. Hyaluronic acid in the evaluation of liver fibrosis in patients with hepatitis C on haemodialysis. Braz J Infect Dis 2010;14:335-41.  Back to cited text no. 31
    

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Correspondence Address:
Bahaa El-Din Moustafa Zayed
Department of Internal Medicine and Nephrology, Faculty of Medicine, Cairo University, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


PMID: 28748878

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