LGCmain
Indian Journal of Pathology and Microbiology
Home About us Instructions Submission Subscribe Advertise Contact e-Alerts Ahead Of Print Login 
Users Online: 688
Print this page  Email this page Bookmark this page Small font sizeDefault font sizeIncrease font size


 
  Table of Contents    
ORIGINAL ARTICLE  
Year : 2011  |  Volume : 54  |  Issue : 3  |  Page : 454-459
Steatosis in chronic hepatitis B: Prevalence and correlation with biochemical, histologic, viral, and metabolic parameters


1 Department of Pathology, Institute of Liver and Biliary Sciences, New Delhi, India
2 Department of Pathology, GB Pant Hospital, New Delhi, India
3 Department of Hepatology, Institute of Liver and Biliary Sciences, New Delhi; Special Centre for Molecular Medicine, Jawaharlal Nehru University, New Delhi, India
4 Department of Gastroenterology, GB Pant Hospital, New Delhi, India
5 Department of Hepatology, Institute of Liver and Biliary Sciences, New Delhi; Department of Gastroenterology, GB Pant Hospital, New Delhi; Special Centre for Molecular Medicine, Jawaharlal Nehru University, New Delhi, India

Click here for correspondence address and email

Date of Web Publication20-Sep-2011
 

   Abstract 

Background and Aims: Hepatic steatosis (HS) is highly prevalent in chronic hepatitis C and is an important variable predicting progression of histological injury, insulin resistance, and reduced response to antiviral therapy. There are limited data on HS in patients with chronic hepatitis B (CHB). This is relevant since response to current antiviral therapies for CHB is rather limited. We investigated the spectrum and predictors of HS in CHB patients. Materials and Methods: Liver biopsies of consecutive patients of chronic Hepatitis B Virus (HBV) infection were studied and were categorized as: Group I - hepatosteatosis (>5%) and Group II - no steatosis (£5%). Anthropometric, histological, biochemical, virological, and metabolic determinants were compared. Logistic regression analysis was applied to identify variables that were independently associated with the presence of steatosis. Results: Of the 350 patients, 118 (33.7%) liver biopsies showed steatosis (Group I); 65 (55.1%) had mild (6 to <25%) and 53 (44.9%) had moderate to severe steatosis (325%). Patients in group I, compared with group II, were older (35.5 ± 10.5 vs 27.9 ± 14.0 years, P < 0.01), predominantly male (M: F, 10.8: 1 vs 4.8: 1, P = 0.035), obese (75.0% vs 23.4%, P < 0.01), with higher body mass index (25.2 ± 4.8 vs 20.4 ± 3.5, P < 0.01), with higher triglycerides (138.8 ± 62.1 vs 88.0 ± 27.9, P = 0.02), with higher cholesterol (171.9 ± 43.5 vs 139.3 ± 37.6, P = 0.017), and with higher serum insulin (13.1 ± 9.1 vs 9.1 ± 6.0, P < .027) levels. HBV DNA level was significantly lower in group I than group II; however, HBV genotype did not influence HS. By multivariate regression analysis, only high serum triglyceride level was independent parameter associated with HS. Conclusions: Steatosis is seen in one-third cases with HBV-related chronic liver disease and is associated with host metabolic factors, especially serum triglyceride levels, whereas HBV DNA level negatively correlated with HS.

Keywords: Body mass index, chronic hepatitis B, fibrosis, genotypes, hepatic steatosis, necroinflammatory activity

How to cite this article:
Rastogi A, Sakhuja P, Kumar A, Hissar S, Jain A, Gondal R, Sarin SK. Steatosis in chronic hepatitis B: Prevalence and correlation with biochemical, histologic, viral, and metabolic parameters. Indian J Pathol Microbiol 2011;54:454-9

How to cite this URL:
Rastogi A, Sakhuja P, Kumar A, Hissar S, Jain A, Gondal R, Sarin SK. Steatosis in chronic hepatitis B: Prevalence and correlation with biochemical, histologic, viral, and metabolic parameters. Indian J Pathol Microbiol [serial online] 2011 [cited 2020 Nov 29];54:454-9. Available from: https://www.ijpmonline.org/text.asp?2011/54/3/454/85074



   Introduction Top


Hepatic steatosis (HS) is defined as excessive lipid accumulation within the hepatocyte cytoplasm and has been recognized as a significant cause for cirrhosis. [1] Most investigators define steatosis as triglyceride content exceeding 5% of the liver weight. [2] The prevalence of steatosis ranges from 35 to 81% in chronic hepatitis C (CHC). [3] It has been found to be associated with progression of fibrosis [4],[5] and impaired response to antiviral therapy. [6] Two possible mechanisms for steatosis include risk factors such as obesity, hyperlipidemia, and insulin resistance [7] and the direct cytopathic effect of hepatitis C virus (HCV). [7]

Chronic hepatitis B (CHB) and hepatitis C (CHC) infections are common globally. CHB is commoner in Asia and nearly 45 million people suffer from this infection [8] HS could be significant in some of these subjects as reported by our group and others. [9],[10] A few studies have even shown that steatosis in CHB appears to be related to metabolic syndrome. [11],[12],[13],[14]

The clinical significance of HS in HBV-infected patients and its contribution to the histopathological injury in CHB has not been looked into in detail. It is not known whether the rate of HBV-related disease progression, fibrosis, and cirrhosis are influenced by the underlying steatosis. [4] The relation of steatosis and HCV genotypes is well established. [15] The significance of steatosis in CHB subjects and its relation to HBV genotypes is not known. We undertook this study to assess the presence, degree, and distribution of HS in patients with CHB and to determine its association with various histological, biochemical, virological, and metabolic parameters.


   Materials and Methods Top


Patients

We retrospectively evaluated liver biopsies of patients with chronic HBV infection that were received in the department of Pathology. The following selection criteria were used:

Inclusion Criteria

Presence of HBV-related chronic liver disease with hepatitis B surface antigen positive for over 6 months and availability of adequate liver biopsy. A liver biopsy was considered adequate if it was 1.5-cm long and/or contained at least 4 to 5 portal tracts. [16]

Exclusion Criteria

Those receiving antiviral treatment before the biopsy, consuming alcohol regularly (more than 30 g/day for males and 20 g/day for females), and diagnosed as having coinfection with other viruses (HCV, HIV). HCV and HIV infections were excluded by serological testing with enzyme-linked immunosorbent assay.

A total of 380 liver biopsies from such patients were retrieved. Three hundred and fifty cases fulfilled the selection criteria as mentioned above.

Methods

The patients were divided into two groups based on the result of liver biopsy: Group I, with HS (>5%) and group II, without HS (≤5%).

The groups were compared in terms of age, gender, liver enzymes, HBeAg status, HBV viral load, HBV genotypes, histological findings of necroinflammatory activity and fibrosis, type and distribution of steatosis, and metabolic determinants.

In a subset of patients, comparison between body mass index (BMI), waist circumference, triglyceride, cholesterol, sugar, insulin, c-peptide, and leptin levels was also done between the two groups. Using the criteria for the Asian population, the patients were categorized into five BMI groups as follows: underweight (<18.5 kg/m 2 ), normal weight (18.5-22.99 kg/m 2 ), mildly obese (23-24.99 kg/m 2 ), moderately obese (25-29.99 kg/m 2 ), and severely obese/manifest obesity (≥30 kg/m 2 ). [17] Fasting sugar >126 mg/dl was considered impaired glucose metabolism. Triglyceride level >150 mg/dl and cholesterol level >200 mg/dl were abnormal.

Insulin resistance was measured by Homeostasis Model of Assessment - Insulin Resistance (HOMA-IR), and was calculated using International Formula (fasting glucose [mmol/l] fasting insulin [mU/l]/22.5).

HBV Genotyping

HBV genotypes were determined by multiplex-polyperase chain reaction (PCR) method. For this, HBV viral DNA isolation was done by Phenol-Chloroform method. Multiplex PCR was performed with the GeneAmp PCR System 2700. [18] After this, PCR samples were run on agarose gel. The samples were randomly selected for direct sequencing for confirming the data.

HBV DNA Quantification

Serum HBV DNA levels were quantified with a hybrid capture assay (Digene Labs, USA) that has a lower limit of detection of 0.017 pg/ml.

Serum Leptin

It was measured by commercially available enzyme-linked immunosorbent kit (Leptin [human] EIA Kit, Assay Designs, Inc, Ann Arbor, Michigan, USA).

Liver Histology

Liver biopsies of 350 patients who fulfilled the criteria were retrospectively reviewed by three experienced histopathologists (A.R., P.S., R.G.) blinded to the clinical data. Serial sections of liver biopsies stained with hematoxylin and eosin, Masson's trichrome, Reticulin silver stain, and Orcein were examined for the presence and degree of steatosis, necroinflammatory activity, and fibrosis. The degree of hepatic inflammation and fibrosis were graded using modified Knodell histological index. [19] The chronic hepatitis grading score (0-18), representing the necroinflammatory activity, was the sum of piecemeal necrosis score (0-10), lobular inflammation score (0-4), and portal inflammation score (0-4). The chronic hepatitis staging score (0-4), also referred to as the fibrosis score, was based on the degree and extent of fibrosis and development of cirrhosis. Necroinflammatory activity ≥6 and fibrosis grade 3 to 4 were considered significant for the present study. HS was assessed by visual method and graded semiquantitatively based on the proportion of hepatocytes with fat. After an initial analysis, steatosis scores were grouped as none (≤5%), mild (6 to <25%), or moderate to severe (≥25%). Distribution pattern and type of steatosis in liver biopsies were also recorded.

Statistical Analysis

Comparison of demographic, biochemical, virological, and histological parameters between the two groups was done. All results were expressed as mean (±SD), median (range), or number (%). Comparison between the two groups was carried out by Student's t-test for parametric data, Mann-Whitney U-test for nonparametric data, and Fisher's exact test for categorical data. Pearson's Chi square test was done to compare the genotype between the two groups. Multivariate logistic regression analysis was performed for assessing independent effect variables on HS using variables found significant on univariate analysis. A P value of <0.05 was considered as significant. Statistical analyses were performed with the SPSS 15.0 statistical package (SPSS Inc., Chicago).


   Results Top


Baseline Characteristics

The 350 patients of CHB included in the study were subdivided into groups, with and without steatosis, according to the findings of the liver biopsy samples. Two hundred and thirty two patients (66.3%) had no steatosis (≤5%, Group I), while 118 (33.7%) had steatosis (>5%, Group II).

Demographic Characteristics

The mean age of the patients was 30.6 ± 13.4 years with male to female ratio 6 : 1. The mean age of the patients in group I was significantly higher than group II (35.5 ± 10.5 year vs . 27.9 ± 14.0 year, P < 0.01). Both the groups showed male preponderance and this was significantly higher in group I as compared with group II (M : F ratio 10.8 : 1 vs. 4.8 : 1, P = 0.035). The findings are summarized in [Table 1].
Table 1: Comparison of groups according to demographic features (n = 350)

Click here to view


Biochemical Characteristics

The difference in the alanine transaminase (ALT) levels between the two groups was not significant; Group I - median 62 (range, 14 to 990) IU/l vs Group II - median 68 (range, 13 to 1 277) IU/l, P = 0.620 [Table 2].
Table 2: Comparison of groups according to biochemical and viral parameters

Click here to view


HBeAg Status

HBeAg status was available in 334 cases; 57.2% patients in group II were HBeAg positive in comparison with 48.8% in group I [Table 2]. The difference was not significant (P = 0.106).

Virological Characteristics

Viral load

Serum HBV DNA levels were available in 232 patients. HBV DNA levels were higher in group II (median, 7.5 x 105 [range, 2.0 x 103 to 1.7 x 109 ] copies/ml), in comparison with group I (median, 6.9 x 104 [range, 3.5 x 101 to 1.7 x 109 ] copies/ml, P = 0.025) [Table 2].

HBV genotypes

HBV Genotype results were available in 80 patients [Table 2]. Eleven patients were of genotype A, 57 were of genotype D, one each of genotype B and C, and mixed genotypes were found in the rest (A+C, 2; A+D, 7; C+A+D, 1). Both the groups had similar genotype predominance (genotype D: 81.2% in group I vs 64.6% in group II, P0 = 1.000; genotype A: 12.5% in group I vs 14.6% in group II, P = 0.134). Among the cases with genotype D, 45.6% had HS, whereas among the cases with genotype A, 33.3% showed steatosis. These differences were not statistically significant.

Metabolic Characteristics

[Table 3] depicts metabolic characteristics. Mean BMI (25.2 ± 4.8 vs 20.4 ± 3.5 kg/m2 , P < 0.01), triglycerides (138.8 ± 62.1 vs 88.0 ± 27.9 mg/dl, P = 0.002), cholesterol (171.85 ± 43.51 vs 139.3 ± 37.6 mg/dl, P = 0.017), and insulin (13.0 ± 9.1 vs 9.1 ± 6.0 IU/l, P = 0.027) were significantly higher in group I as compared with group II.
Table 3: Comparison of groups according to metabolic parameters

Click here to view
Significantly more number of patients in group I were obese (BMI ≥23) than in group II (75% vs 23.4%, P < 0.01). Of them, more than 60% had moderate to severe obesity in group I, whereas only one-third in group II had moderate to severe obesity.

HOMA-IR values are available in only 51 patients (group I, n = 17 and group II, n = 34). The median HOMA values are significantly different between the two groups.

Waist circumference, sugar and leptin levels did not reveal any statistically significant difference between the two groups [Table 3].

Histological Characteristics

One hundred and eighteen cases (33.7%) showed HS, of them 65 (55.1%) had mild steatosis (5-24%), 53 (44.9%) showed moderate to severe steatosis (≥25%). More than 90% of the cases with HS showed predominantly macrovesicular steatosis with centrilobular distribution in 63% of the patients [Figure 1] and [Figure 2].
Figure 1: Photomicrograph showing steatosis and ground glass hepatocytes in liver biopsy of CHB infected patient (Hematoxylin and eosin, x200)

Click here to view
Figure 2: Photomicrograph showing macrovesicular steatosis in perivenular hepatocytes in CHB (Hematoxylin and eosin, x400)

Click here to view


Mean histological activity (4.8 ± 2.6 vs 4.5 ± 2.9, P = 0.286) and mean fibrosis scores (1.7 ± 1.1 vs 1.5 ± 1.1, P = 0.179) were comparable in the two groups. Patients with activity score ≥6 (33.9% vs 29.3%, P = 0.393) and fibrosis score 3 to 4 (20.3% vs 18.1%, P = 0.356) were similar in the two groups [Table 4]. Fibrosis progression index was available in 95 cases and it did not reveal any correlation with HS (P = 0.721).
Table 4: Comparison of groups according to histological features (n = 350)

Click here to view


Factors Associated with Hepatic Steatosis

Following parameters were found to be significantly associated with HS on univariate analysis: Age, gender, BMI, triglyceride levels, cholesterol levels, serum insulin, and HBV DNA levels [Table 5]. On multivariate analysis, performed using the variables found significant in the univariate analysis, only serum triglyceride level was found to be independently associated with HS.
Table 5: Parameters found to be associated with steatosis

Click here to view



   Discussion Top


In this study of 350 patients, probably the largest, 33.7% of the CHB patients showed evidence of HS, and in 44.9% of them, the steatosis was moderate to severe. In the group with steatosis, a fair proportion had a metabolic basis of steatosis, with elevated serum triglyceride levels.

HS is characterized by the accumulation of lipids in hepatocytes, and is associated with diverse systemic conditions and various primary liver diseases. In the past, simple steatosis was regarded as benign, but the presence of another liver disease may provide a synergistic combination of steatosis, cellular adaptation, and oxidative damage that aggravates liver injury. [20]

Recent interest has focused on the pathophysiologic mechanisms explaining the genesis of steatosis in the setting of CHC and the data suggest that both viral and host factors are involved in this process. [21] As in CHC, HS is also seen in CHB. Only a few studies have dealt with steatosis in association with CHB infection. [11],[12],[13],[14] The prevalence of steatosis in the 350 patients analyzed in the present study is supported by earlier studies which have reported a prevalence of steatosis ranging from 18 to 76%. However, the number of patients in those studies was much smaller compared with the present study [Table 6].
Table 6: Prevalence of steatosis in CHB in various studies

Click here to view


Czaja and Carpenter [22] compared the histological lesions found in hepatitis B and C and autoimmune hepatitis, and observed steatosis in 27% of patients in patients with hepatitis B. Akyol et al. [23] in their comparative CHC and CHB study found steatosis in 60% of CHB cases. Similarly, Malhotra et al. [9] have reported steatosis in 66.6% of their CHB cases.

We attempted to investigate the factors underlying the occurrence of HS in CHB patients. The age, gender, BMI, serum triglycerides, serum cholesterol, serum insulin, HOMA-IR, and HBV DNA levels were found to be significantly associated with steatosis on univariate analysis. Serum triglyceride level was found on multivariate analysis to be the only parameter to independently influence HS. The blood sugar, serum leptin, c-peptide levels, and the waist circumference did not reveal any statistically significant association.

Patients in the group with steatosis were older in our study. Similar findings have been observed by others. [12],[14] In our study, male preponderance was much higher than that observed by others. [12],[13]

Mean HBV viral load was significantly higher in group II (group without steatosis). Others have not found any correlation between the severity of steatosis and viral load. [12],[14] Similarly, we did not find any correlation between HBeAg status and HS. [12],[13] These findings potentiate the possibility of HS in CHB patients to be related to the host factors and not to the virus. This is contrary to HCV genotype 3-related steatosis, where HCV replication levels have direct role in the pathogenesis of HS. [24] This finding of significantly lower HBV DNA in group I needs to be further explored, especially to look for the role of HS in suppressing viral replication.

In both the groups, genotype D was more common. There was no difference in the prevalence of HS in patients with HBV genotype D or A. Our study reconfirms earlier observations that genotypes A and D are predominant in HBV-related chronic liver disease patients of Indian origin. [25] In our study, the prevalence of HS in patients with genotype D and A did not reveal statistically significant difference. As there was no significant correlation between the genotypes A or D with HS, these genotypes do not seem to be steatogenic per se. There is very scarce data in the literature addressing this question. This is in contrast to CHC, in which genotype 3 directly induces development of steatosis. [3]

Patients with HS had significantly higher mean serum levels of triglyceride, cholesterol, higher body mass index, higher incidence of obesity, and higher serum insulin levels as compared with patients without steatosis. Fasting blood sugar was also higher in patients with steatosis, but the findings were not statistically significant. HOMA-IR, although calculated only in a small subset of patients, showed statistically significant difference between the two groups. Similar findings have been observed by others. [11],[12],[13],[14] These findings indicate that HS in CHB appears to be a result of metabolic factors related to insulin action rather than due to viral factors; however, larger studies are needed for validation.

HS in the present study was predominantly metabolic; similar difference in intracellular distribution and size of lipid accumulation between CHC genotype 3 compared to CHC with other genotypes and CHB has been mentioned by others as well, [7],[11] reflecting different etiologic role of viral and host factors in HS.

We did not find any correlation between serum leptin and HS in CHB, although it was assessed only in a small number of cases. As leptin has a role in fat accumulation in liver and in the enhancement of liver inflammation and fibrogenesis, [26] future studies on larger number of patients are needed to look for its relation with HS in chronic viral liver diseases like CHB.

Similar to other studies, we did not find any significant association between HS and histological indicators of liver damage. [11],[12],[13] Nonalcoholic steatohepatitis, which is considered hepatic manifestation of insulin resistance and a critical link in the chain of metabolic fatty liver disorders, provides a clue to understanding fibrotic progression of chronic liver diseases as in CHC. [6] Studies in CHC have found correlation between HS and fibrosis progression and with necroinflammatory activity. [4],[6] In the present study, there was no correlation between steatosis and fibrosis progression. This probably is related to the role of host factors in etiology rather than the viral factors, as duration of metabolic determinants and steatosis cannot be determined. As steatosis has been reported as a promoting factor for liver damage in HCV infection, [4] further cross-sectional and longitudinal studies are needed to explore relationship between steatosis and disease activity and degree of fibrosis in CHB. This may have impact on future therapeutic strategies for modulating disease progression in relation to steatosis in chronic viral hepatitis.

Studies published till date are all cross-sectional studies. Correlation with fibrosis is based on single liver biopsy. In the present study, we could assess the effect of steatosis on fibrosis progression in a subset of CHB cases. Studies on large cohort of patients with paired liver biopsies and knowledge of duration of steatosis and fibrosis progression index are required to determine whether HS is associated with worsening hepatic fibrosis. Also, in our study, association of steatosis with genotypes was looked for in a subset of our patients. There is only one more study which has tried to look for such association. It was done in very small number of their cases and did not had role in HS. [14] Future studies on a large group of patients are needed to elucidate the role of viral and insulin resistance parameters in the etiology of steatosis.


   Conclusions Top


HS is seen in one-third cases of HBV-related chronic liver disease. Its more frequent association with metabolic determinants and presence of metabolic pattern of fat distribution in liver is suggestive of the role of metabolic factors in the etiology of steatosis in CHB. There is no positive correlation to viral factors like viral load and HBeAg status, although it needs to be assessed in further larger studies. There is no significant correlation between HS and the histological indicators of liver damage; however, impact of steatosis on fibrosis progression needs to be further studied. Also, there is a need to evaluate the efficacy of combined antiviral and "metabolic" approaches vs standard antiviral regimes in patients with steatosis and CHB infection.


   Acknowledgement Top


This work was supported by CSIR, HRDG, India.

 
   References Top

1.Brunt EM. Nonalcoholic steatohepatitis: Definition and pathology. Semin Liver Dis 2001;21:3-16.  Back to cited text no. 1
[PUBMED]    
2.Hoyumpa AM, Greene HL, Dunn GD, Schenker S. Fatty liver: Biochemical and clinical considerations. Am J Dig Dis 1975;20:1142-70.  Back to cited text no. 2
    
3.Lonardo A, Loria P, Adinolfi LE, Carulli N, Ruggiero G. Hepatitis C and steatosis: A reappraisal. J Viral Hepat 2006;3:73-80.  Back to cited text no. 3
    
4.Adinolfi LE, Gambardella M, Andreana A, Tripodi MF, Utili R, Ruggiero G. Steatosis accelerates the progression of liver damage of chronic hepatitis C patients and correlates with specific HCV genotype and visceral obesity. Hepatology 2001;33:1358-64.  Back to cited text no. 4
[PUBMED]  [FULLTEXT]  
5.Perumalswami P, Kleiner DE, Lutchman G, Heller T, Borg B, Park Y, et al. Steatosis and progression of fibrosis in untreated patients with chronic hepatitis C infection. Hepatology 2006;43:780-7.  Back to cited text no. 5
[PUBMED]  [FULLTEXT]  
6.Castera L. Steatosis, insulin resistance and fibrosis progression in chronic hepatitis. Minerva Gastroenterol Dietol 2006;52:125-34.  Back to cited text no. 6
[PUBMED]    
7.Yoon EJ, Ke-Qin Hu. Hepatitis C virus (HCV) infection and hepatic steatosis. Int J Med Sci 2006;3:53-6.  Back to cited text no. 7
    
8.Thyagrajan SP, Jayaram S, Mohanvalli B. Prevalence of HBV in the general population of India, in hepatitis B in India. In: SK Sarin, AK Singhal, editors. New Delhi, India: CBS Publishers and Distributors; 1996. p. 9.  Back to cited text no. 8
    
9.Malhotra V, Sakhuja P, Gondal R, Sarin SK, Siddhu M, Dutt N. Histological comparison of chronic hepatitis B and C in an Indian population. Trop Gastroenterol 2000;21:20-1.  Back to cited text no. 9
[PUBMED]    
10.Rozario R, Ramakrishna B. Histopathological study of chronic hepatitis B and C: A comparison of two scoring systems. J Hepatol 2003;38:240-2.  Back to cited text no. 10
    
11.Gordon A, McLean CA, Pedersen JS, Bailey MJ, Roberts SK. Hepatic steatosis in chronic hepatitis B and C: Predictors, distribution and effect on fibrosis. J Hepatol 2005;43:38-44.  Back to cited text no. 11
[PUBMED]  [FULLTEXT]  
12.Altlparmak E, Koklu S, Yalinkilic M. Viral and host causes of fatty liver in chronic hepatitis B. World J Gastroenterol 2005;11:3056-9.  Back to cited text no. 12
    
13.Thomopoulos KC, Arvaniti V, Tsamantas AC, Dimitropoulou D, Gogos CA, Siagris D, et al . Prevalence of liver steatosis in patients with chronic hepatitis B: A study of associated factors and of relationship with fibrosis. Eur J Gastroenterol Hepatol 2006;18:233-7.  Back to cited text no. 13
[PUBMED]  [FULLTEXT]  
14.Bondini S, Kallman J, Wheeler A, Prakash S, Gramlich T, Jondle DM, et al. Impact of non-alcoholic fatty liver disease on chronic hepatitis B. Liver Int 2007;27:607.  Back to cited text no. 14
[PUBMED]  [FULLTEXT]  
15.Hissar SS, Goyal A, Kumar M, Pandey C, Suneetha PV, Sood A, et al. Hepatitis C virus genotype 3 predominates in North and Central India and is associated with significant histopathologic liver disease. J Med Virol 2006;78:452-8.  Back to cited text no. 15
[PUBMED]  [FULLTEXT]  
16.Bravo AA, Sheth SG, Chopra S. Liver biopsy. N Engl J Med 2001;344:495- 500.  Back to cited text no. 16
    
17.International obesity task Force. The Asia Pacific perspective: Redefining obesity and its treatment, Sydney. Health Communications Australia 2000;24:358-62.  Back to cited text no. 17
    
18.Kirschberg O, Schuttler C, Repp R, Schaefer S. A multiplex-PCR to identify hepatitis B virus-genotypes A-F. J Clin Virol 2004;29:39-43.  Back to cited text no. 18
    
19.Desmet VJ, Gerber M, Hoofnagle JH, Manns M, Scheuer PJ. Classification of chronic hepatitis: Diagnosis, grading and staging. Hepatology 1994;19:1513-20.  Back to cited text no. 19
[PUBMED]    
20.Powell EF, Jonsson JR, Clouston AD. Steatosis: Co-factor in other liver diseases. Hepatology 2005;42:5-13.  Back to cited text no. 20
    
21.Harrison SA. Steatosis and chronic hepatitis C infection: Mechanisms and significance. Clin Gastroenterol Hepatol 2005;3: S92-6.  Back to cited text no. 21
[PUBMED]  [FULLTEXT]  
22.Czaja AJ, Carpenter HA. Sensitivity, specificity, and predictability of biopsy interpretations in chronic hepatitis. Gastroenterology 1993;105:1824-32.  Back to cited text no. 22
[PUBMED]    
23.Akyol G, Suer O, Sezer C. Comparative histological analysis of hepatitis C virus with hepatitis B. Turk J Med Sci 2001;31:405-10.  Back to cited text no. 23
    
24.Negro F. Mechanism and significance of liver steatosis in hepatitis C virus infection. World J Gastroenterol 2006;12:6756-65.  Back to cited text no. 24
[PUBMED]  [FULLTEXT]  
25.Thakur V, Guptan RC, Kazim SN, Malhotra V, Sarin SK. Profile, spectrum and significance of HBV genotypes in chronic liver disease patients in the Indian subcontinent. J Gastroenterol Hepatol 2002;17:165-70.  Back to cited text no. 25
[PUBMED]  [FULLTEXT]  
26.Tungtrongchitr R, Treeprasertsuk S, Ei NN, Thepouyporn A, Phonrat B, Huntrup A. Serum leptin concentrations in chronic hepatitis. J Med Assoc Thai 2006;89:490-9.  Back to cited text no. 26
[PUBMED]    

Top
Correspondence Address:
Puja Sakhuja
Room No. 326, Department of Pathology, GB Pant Hospital, Affiliated to University of Delhi, New Delhi - 110 002
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.85074

Rights and Permissions


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]

This article has been cited by
1 Liver steatosis is a strong predictor of mortality and cancer in chronic hepatitis B regardless of viral load
Noam Peleg,Assaf Issachar,Orly Sneh Arbib,Michal Cohen-Naftaly,Marius Braun,Moshe Leshno,Alon Barsheshet,Amir Shlomai
JHEP Reports. 2019; 1(1): 9
[Pubmed] | [DOI]
2 Inverse relationship between hepatic steatosis and hepatitis B viremia: Results of a large case-control study
R. W. H. Hui,W.-K. Seto,K.-S. Cheung,L.-Y. Mak,K. S. H. Liu,J. Fung,D. K.-H. Wong,C.-L. Lai,M.-F. Yuen
Journal of Viral Hepatitis. 2018; 25(1): 97
[Pubmed] | [DOI]
3 INASL Position Statements on Prevention, Diagnosis and Management of Hepatitis B Virus Infection in India: The Andaman Statements
Anil Arora,Shivaram P. Singh,Ashish Kumar,Vivek A. Saraswat,Rakesh Aggarwal,Manisha Bangar,Pradip Bhaumik,Harshad Devarbhavi,Radha K. Dhiman,Vinod K. Dixit,Ashish Goel,Bhabadev Goswami,Dharmesh Kapoor,Kaushal Madan,Jimmy Narayan,Sandeep Nijhawan,Gaurav Pandey,Ramesh R. Rai,Manoj K. Sahu,Neeraj Saraf,Neeraj Shalimar,Thrivikrama Shenoy,Varghese Thomas,Manav Wadhawan
Journal of Clinical and Experimental Hepatology. 2018; 8(1): 58
[Pubmed] | [DOI]
4 Fatty liver checkmates hepatitis B virus
Gayatri Ramakrishna,Nirupma Trehanpati
Hepatology International. 2018; 12(5): 387
[Pubmed] | [DOI]
5 Factors Associated With Persistent Increase in Level of Alanine Aminotransferase in Patients With Chronic Hepatitis B Receiving Oral Antiviral Therapy
Ira M. Jacobson,Mary K. Washington,Maria Buti,Alexander Thompson,Nezam Afdhal,Robert Flisiak,Ulus Salih Akarca,Konstantin G. Tchernev,John F. Flaherty,Raul Aguilar Schall,Robert P. Myers,G. Mani Subramanian,John G. McHutchison,Zobair Younossi,Patrick Marcellin,Keyur Patel
Clinical Gastroenterology and Hepatology. 2017; 15(7): 1087
[Pubmed] | [DOI]
6 Impact of Non-alcoholic Fatty Liver Disease on Chronic Hepatitis B Infection
Anthony W.H. Chan,Grace L.H. Wong,Vincent W.S. Wong
Current Hepatology Reports. 2017; 16(2): 97
[Pubmed] | [DOI]
7 New trends on obesity and NAFLD in Asia
Jian-Gao Fan,Seung-Up Kim,Vincent Wai-Sun Wong
Journal of Hepatology. 2017; 67(4): 862
[Pubmed] | [DOI]
8 A “systems medicine” approach to the study of non-alcoholic fatty liver disease
Salvatore Petta,Luca Valenti,Elisabetta Bugianesi,Giovanni Targher,Stefano Bellentani,Ferruccio Bonino,Ele Ferrannini,Carmela Loguercio,Amedeo Lonardo,Fabio Marra,Marcello Mancini,Luca Miele,Valerio Nobili,Gianluca Svegliati Baroni,Federico Alessandro,Stefano Ballestri,Maurizia Rossana Brunetto,Barbara Coco,Antonio Grieco,Silvia Fargion,Loreta Kondili,Fabio Nascimbeni,Anna Prinster,Dante Romagnoli,Stefano Taddei,Ester Vanni,Stefano Vella
Digestive and Liver Disease. 2016; 48(3): 333
[Pubmed] | [DOI]
9 Association between hepatitis B and metabolic syndrome: Current state of the art
Peter Jarcuska
World Journal of Gastroenterology. 2016; 22(1): 155
[Pubmed] | [DOI]
10 Hepatic steatosis in HCV-infected persons in the direct-acting antiviral era
Heather L. Stevenson,Netanya S. Utay
Tropical Diseases, Travel Medicine and Vaccines. 2016; 2(1)
[Pubmed] | [DOI]
11 Saturated Fatty Acid Inhibits Viral Replication in Chronic Hepatitis B Virus Infection With Nonalcoholic Fatty Liver Disease by Toll-Like Receptor 4-Mediated Innate Immune Response
Rui-Nan Zhang,Qin Pan,Zheng Zhang,Hai-Xia Cao,Feng Shen,Jian-Gao Fan
Hepatitis Monthly. 2015; 15(5)
[Pubmed] | [DOI]
12 Interactions of Hepatitis B Virus Infection with Nonalcoholic Fatty Liver Disease: Possible Mechanisms and Clinical Impact
Chu-wen Lin,Xiao-li Huang,Hai-lin Liu,Yan Wang
Digestive Diseases and Sciences. 2015; 60(12): 3513
[Pubmed] | [DOI]
13 A model with combined viral and metabolic factors effectively predicts HBeAg status under long term entecavir therapy: a prospective cohort study
Fen Liu,Feng Zou,Xiwei Wang,Huaidong Hu,Peng Hu,Hong Ren
Virology Journal. 2015; 12(1)
[Pubmed] | [DOI]
14 Thyroid function is associated with non-alcoholic fatty liver disease in chronic hepatitis B-infected subjects
Wen-Jin Ding,Man-Man Wang,Gong-Sui Wang,Fen Shen,Jian-Jun Qin,Jian-Gao Fan
Journal of Gastroenterology and Hepatology. 2015; 30(12): 1753
[Pubmed] | [DOI]
15 Non-invasive assessment of fatty liver
Anna Egresi,Gabriella Lengyel,Krisztina Hagymási
Orvosi Hetilap. 2015; 156(14): 543
[Pubmed] | [DOI]
16 Hepatitis B virus infection and metabolic syndrome: Fact or fiction?
Chia-Chi Wang,Tai-Chung Tseng,Jia-Horng Kao
Journal of Gastroenterology and Hepatology. 2015; 30(1): 14
[Pubmed] | [DOI]
17 Hepatic Steatosis as a Predictive Factor of Antiviral Effect of Pegylated Interferon Therapy in Patients With Hepatitis B
L. Gong,J. Liu,J. Wang,G.Q. Lou,J.P. Shi
Transplantation Proceedings. 2015; 47(10): 2886
[Pubmed] | [DOI]
18 Cardiovascular risk, lipidemic phenotype and steatosis. A comparative analysis of cirrhotic and non-cirrhotic liver disease due to varying etiology
P. Loria,G. Marchesini,F. Nascimbeni,S. Ballestri,M. Maurantonio,F. Carubbi,V. Ratziu,A. Lonardo
Atherosclerosis. 2014; 232(1): 99
[Pubmed] | [DOI]
19 Hepatic Steatosis Is Highly Prevalent in Hepatitis B Patients and Negatively Associated with Virological Factors
Man-Man Wang,Gong-Sui Wang,Feng Shen,Guang-Yu Chen,Qin Pan,Jian-Gao Fan
Digestive Diseases and Sciences. 2014;
[Pubmed] | [DOI]
20 Insulin resistance and steatosis in HBV-HCV co-infected patients: Role of PNPLA3 polymorphisms and impact on liver fibrosis progression
Rosa Zampino
World Journal of Hepatology. 2014; 6(9): 677
[Pubmed] | [DOI]
21 Clinical and laboratory characteristics associated with dyslipidemia and liver steatosis in chronic HBV carriers
Angélica Luciana Nau,Júlia Cristina Soares,Maria Beatriz Cacese Shiozawa,Esther Buzaglo Dantas-Corrêa,Leonardo de Lucca Schiavon,Janaína Luz Narciso-Schiavon
Revista da Sociedade Brasileira de Medicina Tropical. 2014; 47(2): 158
[Pubmed] | [DOI]
22 Hepatic Steatosis: Prevalence and Host/Viral Risk Factors in Iranian Patients with Chronic Hepatitis B Infection
Vahdat Poortahmasebi,Seyed Moayed Alavian,Hossein Keyvani,Mehdi Norouzi,Mahmood Mahmoodi,Seyed Mohammad Jazayeri
Asian Pacific Journal of Cancer Prevention. 2014; 15(9): 3879
[Pubmed] | [DOI]
23 Controlled attenuation parameter for non-invasive assessment of hepatic steatosis: Does etiology affect performance?
Manoj Kumar,Archana Rastogi,Tarandeep Singh,Chhagan Behari,Ekta Gupta,Hitendra Garg,Ramesh Kumar,Vikram Bhatia,Shiv K Sarin
Journal of Gastroenterology and Hepatology. 2013; 28(7): 1194
[Pubmed] | [DOI]
24 Fatty liver reduces hepatitis B virus replication in a genotype B hepatitis B virus transgenic mice model
Zheng Zhang,Qin Pan,Xiao-Yan Duan,Qiang Liu,Guo-Yu Mo,Gui-Rong Rao,Jian-Gao Fan
Journal of Gastroenterology and Hepatology. 2012; 27(12): 1858
[Pubmed] | [DOI]
25 Nonalcoholic Fatty Liver Disease in Chronic Hepatitis B and C Patients from Western Amazon
A. C. M. Nascimento,D. R. Maia,S. M. Neto,E. M. Lima,M. Twycross,R. F. Baquette,C. M. O. Lobato
International Journal of Hepatology. 2012; 2012: 1
[Pubmed] | [DOI]



 

Top
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  


    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusions
   Acknowledgement
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed6398    
    Printed198    
    Emailed1    
    PDF Downloaded214    
    Comments [Add]    
    Cited by others 25    

Recommend this journal