Saudi Journal of Gastroenterology
Home About us Instructions Submission Subscribe Advertise Contact Login    Print this page  Email this page Small font sizeDefault font sizeIncrease font size 
Users Online: 2461 


 
Table of Contents   
ORIGINAL ARTICLE  
Year : 2020  |  Volume : 26  |  Issue : 4  |  Page : 204-209
Prevalence of biopsy-proven nonalcoholic fatty liver among patients with gallstone disease


1 Department of Surgery, College of Medicine, King Saud University, Riyadh, Kingdom of Saudi Arabia
2 Liver Disease Research Center, King Saud University, Riyadh, Kingdom of Saudi Arabia
3 Department of Surgery, King Salman Hospital, Riyadh, Kingdom of Saudi Arabia
4 Department of Pathology, College of Medicine, King Saud University, Riyadh, Kingdom of Saudi Arabia
5 Department of Radiology and Medical Imaging, College of Medicine, King Saud University, Riyadh, Kingdom of Saudi Arabia
6 Department of Medicine, Gastroenterology Unit, King Abdulaziz Medical City, Jeddah, Kingdom of Saudi Arabia
7 Liver Disease Research Center, King Saud University; Department of Liver Transplant, King Faisal Specialist Hospital and Research Center, Riyadh, Kingdom of Saudi Arabia

Click here for correspondence address and email

Date of Submission27-Jan-2020
Date of Acceptance19-Feb-2020
Date of Web Publication14-Apr-2020
 

   Abstract 


Background/Aim: Gallstone disease (GD) and nonalcoholic fatty liver disease (NAFLD) are associated with metabolic syndrome. Despite the benign nature of NAFLD, 10% of patients may develop advanced fibrosis and cirrhosis. We aimed to identify the prevalence and factors associated with NAFLD among GD patients in the Saudi population.
Patients and Methods: This is a single-center, observational cohort study that included patients seen in general surgery clinics at our institution from 2011 to 2017. All liver biopsies were taken at the same time as the cholecystectomy. Demographical and clinical data were prospectively collected from the study population.
Results: Of the 301 GD patients in the study, 15% had a normal body mass index (BMI), 29% were overweight, and 56% were obese. There were 143 (47.8%) patients with NAFLD, of which 125 (41.8%) showed steatosis and 18 (6%) had nonalcoholic steatohepatitis. There was a significant positive correlation between NAFLD and age (r = 0.243; P < 0.0001), and BMI (r = 0.242; P < 0.0001). Obese patients with BMI 30–40 kg/m[2] were 2.403 (P = 0.039) more likely to have NAFLD compared with normal BMI patients, and this value increased to 6.145 (P = 0.002) in patients with BMI >40 kg/m[2]. Additionally, patients with T2DM were 2.839 times (P = 0.015) more likely to have NAFLD compared with those who did not.
Conclusions: The prevalence of NAFLD among GD patients is high. High BMI and diabetes are independent factors associated with NAFLD in GD patients. The results suggest that there may be a need for routine liver biopsy in selected patients during cholecystectomy.

Keywords: Diabetes, gallstone, NAFLD, obese, prevalence

How to cite this article:
Alsaif FA, Alqahtani SH, Alsadoon AM, Alswat KA, Abdo AA, Hassanain MM, Alsharabi AB, Aljuhani GR, Alkhalidi HM, Elsharkawy MS, Alotaibi MA, Sanai FM, Al-hamoudi WK. Prevalence of biopsy-proven nonalcoholic fatty liver among patients with gallstone disease. Saudi J Gastroenterol 2020;26:204-9

How to cite this URL:
Alsaif FA, Alqahtani SH, Alsadoon AM, Alswat KA, Abdo AA, Hassanain MM, Alsharabi AB, Aljuhani GR, Alkhalidi HM, Elsharkawy MS, Alotaibi MA, Sanai FM, Al-hamoudi WK. Prevalence of biopsy-proven nonalcoholic fatty liver among patients with gallstone disease. Saudi J Gastroenterol [serial online] 2020 [cited 2020 Nov 29];26:204-9. Available from: https://www.saudijgastro.com/text.asp?2020/26/4/204/282502





   Introduction Top


Gallstone disease (GD) is one of the most common gastrointestinal disorders. The prevalence of GD is estimated to be around 15% in developed countries. Most patients are asymptomatic and the disease is usually detected when acute pancreatitis, cholecystitis, or biliary pain occurs as part of the complications.[1] Cholecystectomy is the standard treatment for GD.

GD is more common in females of childbearing age and is associated with age, smoking, sedentary lifestyle, central obesity, impaired glucose tolerance, diabetes mellitus type 2 (T2DM), hypertriglyceridemia, and cholesterolemia.[2] These risk factors can lead to nonalcoholic fatty liver disease (NAFLD).

NAFLD is one of the most common liver diseases encountered worldwide.[3] It is characterized by abnormal fat accumulation in the liver, leading to histological changes similar to those seen in alcoholic liver disease, but occurring in people who do not drink alcohol excessively.[4] NAFLD exists on a spectrum, starting from simple steatosis, steatohepatitis, cirrhosis, to end-stage liver failure, and hepatocellular carcinoma (HCC). Although it is benign in most patients, 10% may develop advanced fibrosis and cirrhosis. Obesity, especially central adiposity, T2DM, and dyslipidemia, which are collectively defined as the metabolic syndrome, are well-known risk factors of developing NAFLD.[5],[6]

The global prevalence of NAFLD is 25.24%, with the highest prevalence in the Middle East and South America and lowest in Africa. Metabolic comorbidities associated with NAFLD include obesity, T2DM, hyperlipidemia, hypertension, and metabolic syndrome. The high prevalence of DM and obesity serves as major risk factors for nonalcoholic steatohepatitis (NASH) and significantly impact the increasing prevalence of NAFLD.[6],[7] A recent meta-analysis on the prevalence of NAFLD in T2DM revealed that the pooled prevalence of NAFLD in T2DM patients, by a random-effects model, was 59.67%.[8] NAFLD shares many risk factors with GD such as obesity, T2DM, sedentary lifestyle, and hyperlipidemia. Previous studies suggest that insulin resistance and hyperinsulinemia are risk factors for both GD and NAFLD. This indicates a possible link with abdominal adiposity.[9],[10],[11] Furthermore, a recent study by Ali et al. demonstrated that patients who underwent cholecystectomy were more likely to gain weight significantly in a relatively short period of time.[12] These observations imply that the prevalence of NAFLD could be increased in GD patients compared to that in the general population. This was first suggested by a study by Roesch-Dietlen et al. whereby 54.7% of their GD patients had associated NAFLD.[13] Medina et al. demonstrated that 55% of patients who presented with symptoms and had been operated for GD had associated NAFLD.[14]

To date, there are no studies on the association between NAFLD and GD in the Saudi or Middle-eastern populations. Given the high prevalence of obesity and GD, it is logical to assume that NAFLD prevalence in GD patients is high. Thus, we aimed to identify the prevalence and factors associated with NAFLD among GD patients in the Saudi population. This study could be useful in developing a liver biopsy protocol during cholecystectomy in selected patients.


   Study Population and Methods Top


The study population consisted of all gallstone patients seen in general surgery clinics at King Saud University Medical City (KSUM) from 2011 to 2017. There were 301 patients scheduled for cholecystectomy enrolled in the study. Informed consent was obtained from all patients at the point of recruitment for the study while an additional, standard, institutional consent was obtained for the liver biopsy. The study was approved by the institutional review board.

Adult male and female, nonalcohol-consuming patients aged between 18 and 70 years age, having ultrasound evidence of gallstones such as echogenicity, distal shadowing, and movable structures inside the gallbladder were included in the study. Patients were excluded if they fulfilled any of the following criteria: (1) history of alcohol intake; (2) chronic liver disease of any other etiology; (3) presence of secondary causes of NAFLD; (4) history of neoplastic disease of the liver and gallbladder; (5) hemolytic disorders; (6) evidence or history of severe systemic illness; (7) prior liver biopsy confirming the diagnosis of NAFLD.

During the preoperative visit, patients provided informed consent to participate and study procedures were carried out according to the Declaration of Helsinki. A panel of laboratory tests was requested, which included a complete blood count, serum concentrations of alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP), gamma-glutamyl transferase (GGT), total bilirubin, albumin, fasting glucose levels, hemoglobin A1c (HbA1c), and a lipid profile. Additionally, all participants received a complete assessment of metabolic and autoimmune liver disease. All laboratory tests were performed at the central laboratory of KSUM.

All liver biopsies were taken at the time of the cholecystectomy surgery using a biopsy gun (18 × 20 cm, BARD, Max-Core, Arizona, USA) from the right lobe. Biopsies were placed in 10% formalin, transferred to the histopathology laboratory, and stained using routine hematoxylin and eosin stain. All biopsies were reviewed and interpreted by one experienced hepatopathologist who was blinded to the clinical data. Grading for steatotic hepatocytes was as follows: grade 0: <5%; grade 1: 5–33%; grade 2: >33–66%; and grade 3: >66%. Normal patients were in grade 0 for steatosis and stage 0–1 for fibrosis with no or mild inflammation. Fatty liver was defined as the presence of at least 5% steatotic hepatocytes with or without mild lobular or portal inflammation and stage 0–1 fibrosis. All liver biopsies contained at least 10 portal tracts.

Histological diagnosis of NASH was based on the NAFLD Activity Score (5 or more) which is a combination of steatosis grade, hepatocyte ballooning, and lobular inflammation with or without fibrosis.

Statistical analysis

Frequencies are expressed as absolute (number, n) and relative (percentage, %) values for categorical variables. Central tendency (median) and dispersion ( first, third quartiles) are used to present continuous variables that were not normally distributed. Variables that were normally distributed are presented as mean ± standard deviation. Data between groups were compared by Pearson's Chi-squared test or Fisher's exact test as appropriate. Pearson's correlation coefficient, r, was used to measure the correlation between continuous variables. Binary logistic regression analysis was performed to identify independent factors associated with NAFLD in the entire study population.

A two-tailed P value of <0.05 was used to determine statistical significance. Statistical analysis was performed using Statistical Package for Social Sciences (SPSS) software version 23.0 (SPSS Inc., Chicago, IL, USA).


   Results Top


The mean age of the patients was 41 ± 12 years, and the majority were females (76.1%). Overall, 15% had normal BMI, 29% were overweight, and 56% were obese. When subclassified, there were 32.6% with BMI 30–34.9 kg/m[2], 15% with BMI 35–39.9 kg/m[2], and 8% with BMI more than >40 kg/m[2]. Most (85.2%) were not diabetic and the mean glucose and HbA1c levels were within the normal range, 5.74 ± 2.32 mmol/L and 5.78 ± 1.08%, respectively. In addition, the following parameters fell within their respective normal range: ALT 48.54 ± 65.53 U/L, AST 25.77 ± 59.16 U/L, ALP 110.61 ± 70.63 U/L, GGT 76.18 ± 139.96 U/L, total bilirubin 8.68 ± 11.28 μmol/L, albumin 37.00 ± 4.16 g/L, cholesterol 4.78 ± 1.03 mmol/L, triglycerides 1.35 ± 1.07 mmol/L, hemoglobin 129.00 ± 16.33 g/L, white blood cell count 7.35 ± 2.00 × 10[9]/L, platelet count 273.53 ± 71.20 × 10[9]/L, and international normalized ratio (INR) 1.05 ± 0.39 [Table 1].
Table 1: Sociodemographic and clinical characteristics of gallstone disease patients

Click here to view


There were 51.8% (155) patients with normal liver histology, 41.8% (125) patients with simple steatosis, and 6% (18) with steatohepatitis, of which 1.7% (5) had fibrosis and 0.3% (1) had cirrhosis [Figure 1].
Figure 1: Frequency of nonalcoholic fatty liver disease (NAFLD) among gallstone disease patients

Click here to view


There was a positive correlation between NAFLD and age (r = 0.243; P < 0.0001) and BMI (r = 0.242; P < 0.0001), and a significant weak correlation with glucose level (r = 0.149; P < 0.012).

There was no significant correlation between NAFLD and nationality, hemoglobin, white blood cell count, ALT, AST, GGT, and total bilirubin [Table 2].
Table 2: Correlation of factors associated with nonalcoholic fatty liver disease (NAFLD) in gallstone disease patients

Click here to view


Multivariate results showed that increase in age carries a risk of 1.027 (P = 0.021) times and that patients with BMI 30–40 kg/m[2] were 2.403 (P = 0.039) times more likely to have NAFLD compared with normal BMI patients, and this value increased to 6.145 (P = 0.002) times in patients with BMI >40 kg/m[2]. Although the overweight group (BMI 25–29.9 kg/m[2]) had an OR of 2.030, it was statistically insignificant (P = 0.116). In addition, patients with T2DM were 2.839 times (P = 0.015) more likely to have NAFLD compared with those who did not [Table 3] and [Figure 2]. There was no difference in liver enzyme levels between patients with NAFLD and normal liver histology [Table 4].
Table 3: Predictors of NAFLD in gallstone disease patients

Click here to view
Figure 2: Predictors of NAFLD in gallstone disease patients

Click here to view
Table 4: A comparison of liver enzymes level between NAFLD positive patients and healthy subjects

Click here to view



   Discussion Top


NAFLD is one of the most prevalent liver diseases in many developed countries. To our knowledge, this is the first study in our region that evaluates the association between NAFLD and GD.

In view of the growing evidence indicating that NAFLD and GD share the same risk factors, a meta-analysis to assess the relationship between GD and NAFLD was conducted. The meta-analysis found that the pooled prevalence of GD in cases with NAFLD was 17%. NAFLD was significantly correlated with GD compared with the non-NAFLD group.[15] The prevalence of NAFLD in Asia generally ranges from 20 to 33%. The prevalence in China is estimated to be 11.8–24.4% whereas it is 30% in Japan. Korea and Taiwan have the lowest prevalence in Asia at 16.1% and 11.5%, respectively.[16] The prevalence in the United States is 24%.[17],[18] In Saudi Arabia, earlier studies estimated the prevalence of NAFLD to be between 10 and 16.6% based on radiological studies.[19],[20],[21] Because of the obesity and metabolic syndrome epidemic,[22] models were used to estimate NAFLD and NASH disease progression, primarily based on changes in adult prevalence rates of adult obesity and T2DM. In a recently published study, estimates and expert interviews were used to build and validate a model projection for NAFLD. By 2030, the projected NAFLD prevalence is estimated to be around 25–30% in Saudi Arabia.[23]

In this study, we assessed the prevalence of NAFLD based on histological examination of the liver among GD patients. There were 47.8% with NAFLD, of which 41.8% showed simple steatosis, and 6% had NASH. This is in agreement with previously published studies demonstrating a high prevalence of NAFLD in patients with GD. García-Monzón et al. evaluated the prevalence of biopsy-proven NAFLD and NASH among patients with gallstones. They demonstrated that the prevalence of NASH was 10.2% whereas that of simple steatosis was 41.4%. They also demonstrated that NASH was more frequent in patients with metabolic syndrome.[24] Yener et al. evaluated the histological prevalence of NASH in patients with symptomatic gallstones undergoing cholecystectomy. Similarly, they demonstrated that 55% of patients with gallbladder stones had associated NAFLD.[25] A large cross-sectional study enrolled 7,583 Chinese individuals aimed at determining the association between NAFLD and asymptomatic gallstones. The prevalence of NAFLD was significantly higher in patients with asymptomatic gallstones than in those without gallstones (59.0% vs 46.6%, respectively; P < 0.0001). They concluded that asymptomatic gallstones are strongly associated with NAFLD in the Chinese study population.[26]

Only 6% of our GD study population had NASH which is lower than the reported numbers in previous GD studies.[24],[25],[26] This can be explained by the lack of alcohol intake in our population and the higher prevalence of diabetes and metabolic syndrome in the previously reported studies. Furthermore, Yalmiz et al. examined whether the presence of GD in patients with biopsy-proven NAFLD is associated with liver fibrosis and histological NASH score. They concluded that the presence of GD is not independently associated with advanced fibrosis and definite NASH in patients with biopsy-proven NAFLD.[27]

The risk factors of developing NAFLD and GD are overlapping; obesity, T2DM, and dyslipidemia are among the most known risk factors for both diseases. In this study, we found that age and NAFLD were positively correlated, in agreement with other reports.[25],[26] The association of gender and NAFLD is controversial as many authors have found that NAFLD is more common among men,[21],[24] while others have reported 3.5 times higher risk in women.[26] In our study, gender did not have a correlation with NAFLD. T2DM in our study was found to be an independent predictor for NAFLD with an OR of 2.839 (P < 0.015).

In the current study, we assessed the correlation between different BMI groups and NAFLD among our GD patients and found significant positive correlations. More than half of our population were obese with the highest risk in the morbidly obese category (BMI >40 kg/m[2]), with 6.145 times (P = 0.002) greater likelihood to develop NAFLD compared with normal BMI patients. Interestingly, 10 patients with normal BMI were positive for NAFLD and seven who were morbidly obese were negative for simple steatosis. This raises the question of whether there are other factors involved that need further investigation.

Abnormal liver enzymes have been reported as a screening tool for NAFLD. In our study, there was no difference in liver enzyme levels between patients with NAFLD and normal liver histology. Other studies demonstrated higher liver enzyme levels in NAFLD patients with GD compared with patients with no GD. Although patients with NAFLD commonly come to medical attention because of elevated liver enzymes, normal liver enzyme level does not exclude NAFLD. Furthermore, elevated liver enzymes do not necessarily correlate with histological liver injury.[28],[29]

One of the limitations of this study is that it is cross-sectional in nature, hence, causality cannot be determined. Nevertheless, the study population is a good representation of the Saudi population with GD and highlights some of the factors that are associated with NAFLD in GD patients.


   Conclusion Top


The prevalence of NAFLD among our GD population was 47.8%, with 41.8% showing steatosis and 6% with proven NASH. Age, high BMI, and diabetes were independent factors associated with NALFD. Given the high prevalence of NAFLD in our GD population, it may be useful to perform a routine liver biopsy during cholecystectomy in selected patients. Transient elastography (FibroScan) with a controlled attenuation parameter has demonstrated good accuracy in quantifying the levels of liver steatosis and fibrosis in patients with NAFLD and could be an alternative assessment tool.[30]

Financial support and sponsorship

This work was funded by the National Plan for Science, Technology, and innovation (MAARIFAH), King Abdulaziz City for Science and Technology, Kingdom of Saudi Arabia, grant number 11-MED-1766-02.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Browning JD, Horton JD. Gallstone disease and its complications. Semin Gastrointest Dis 2003;14:165-77.  Back to cited text no. 1
    
2.
Attili AF, Capocaccia R, Carulli N, Desti D, Roda E, Barbara L, et al. Factors associated with gallstone disease in the MICOL experience. Multicenter Italian Study on Epidemiology of Cholelithiasis. Hepatology 1997;26:809-18.  Back to cited text no. 2
    
3.
Chalasani N, Younossi Z, Lavine JE, Charlton M, Cusi K, Rinella M, et al. The diagnosis and management of nonalcoholic fatty liver disease: Practice guidance from the American Association for the Study of Liver Diseases. Hepatology 2018;67:328-57.  Back to cited text no. 3
    
4.
Clark JM, Brancati FL, Diehl AM. Nonalcoholic fatty liver disease. Gastroenterology 2002;122:1649-57.  Back to cited text no. 4
    
5.
Marchesini G, Bugianesi E, Forlani G, Cerrelli F, Lenzi M, Manini R, et al. Nonalcoholic fatty liver, steatohepatitis, and the metabolic syndrome. Hepatology 2003;37:917-23.  Back to cited text no. 5
    
6.
Younossi ZM, Koenig AB, Abdelatif D, Fazel Y, Henry L, Wymer M. Global epidemiology of nonalcoholic fatty liver disease-Meta-analytic assessment of prevalence, incidence, and outcomes. Hepatology 2016;64:73-84.  Back to cited text no. 6
    
7.
Al-Hamoudi W, Abaalkhail F, Bendahmash A, Allam N, Hegab B, Elsheikh Y, et al. The impact of metabolic syndrome and prevalent liver disease on living donor liver transplantation: A pressing need to expand the pool. Hepatol Int 2016;10:347-54.  Back to cited text no. 7
    
8.
Dai W, Ye L, Liu A, Wen SW, Deng J, Wu X, et al. Prevalence of nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus: A meta-analysis. Medicine (Baltimore) 2017;96:e8179.  Back to cited text no. 8
    
9.
Ruhl CE, Everhart JE. Association of diabetes, serum insulin, and C-peptide with gallbladder disease. Hepatology 2000;31:299-303.  Back to cited text no. 9
    
10.
Sanyal AJ, Americal Gastroenterological Association. AGA technical review on nonalcoholic fatty liver disease. Gastroenterology 2002;123:1705-25.  Back to cited text no. 10
    
11.
Heaton KW. Review article: Epidemiology of gall-bladder disease-role of intestinal transit. Aliment Pharmacol Ther 2000;14(Suppl 2):9-13.  Back to cited text no. 11
    
12.
Ali RB, Cahill RA, Watson RG. Weight gain after laparoscopic cholecystectomy. Ir J Med Sci 2004;173:9-12.  Back to cited text no. 12
    
13.
Roesch-Dietlen F, Perez-Morales A, Melo-Santisteban G, Diaz-Blanco F, Martinez-Fernandez S, Martinez JA, et al. [Frequency and clinical, biochemical and histological characteristics of nonalcoholic fatty liver disease in patients with gallstone disease]. (Spanish) Cir Cir 2008;76:37-42.  Back to cited text no. 13
    
14.
Ramos-De la Medina A, Remes-Troche JM, Roesch-Dietlen FB, Perez-Morales AG, Martinez S, Cid-Juarez S. Routine liver biopsy to screen for nonalcoholic fatty liver disease (NAFLD) during cholecystectomy for gallstone Disease: Is it justified? J Gastrointest Surg 2008;12:2097-102.  Back to cited text no. 14
    
15.
Shen SS, Gong JJ, Wang XW, Chen L, Qin S, Huang LF, et al. Promotional effect of nonalcoholic fatty liver disease on gallstone disease: A systematic review and meta-analysis. Turk J Gastroenterol 2017;28:31-9.  Back to cited text no. 15
    
16.
Wah-Kheong C, Khean-Lee G. Epidemiology of a fast emerging disease in the Asia-Pacific region: Non-alcoholic fatty liver disease. Hepatol Int 2013;7:65-71.  Back to cited text no. 16
    
17.
Sayiner M, Koenig A, Henry L, Younossi ZM. Epidemiology of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis in the United States and the rest of the world. Clin Liver Dis 2016;20:205-14.  Back to cited text no. 17
    
18.
Pappachan JM, Babu S, Krishnan B, Ravindran NC. Non-alcoholic fatty liver disease: A clinical update. J Clin Transl Hepatol 2017;5:384.  Back to cited text no. 18
    
19.
Akbar DH, Kawther AH. Nonalcoholic fatty liver disease in Saudi type 2 diabetic subjects attending a medical outpatient clinic: Prevalence and general characteristics. Diabetes Care 2003;26:3351-2.  Back to cited text no. 19
    
20.
El-Hassan AY, Ibrahim EM, Al-Mulhim FA, Nabhan AA, Chammas MY. Fatty infiltration of the liver: Analysis of prevalence, radiological and clinical features and influence on patient management. Brit J Radiol 1992;65:774-8.  Back to cited text no. 20
    
21.
Al-hamoudi W, El-Sabbah M, Ali S, Altuwaijri M, Bedewi M, Adam M, et al. Epidemiological, clinical, and biochemical characteristics of Saudi patients with nonalcoholic fatty liver disease: A hospital-based study. Ann Saudi Med 2012;32:288-92.  Back to cited text no. 21
    
22.
Al-Hussaini A, Bashir MS, Khormi M, AlTuraiki M, Alkhamis W, Alrajhi M, et al. Overweight and obesity among Saudi children and adolescents: Where do we stand today? Saudi J Gastroenterol 2019;25:229-35.  Back to cited text no. 22
[PUBMED]  [Full text]  
23.
Alswat K, Aljumah AA, Sanai FM, Abaalkhail F, Alghamdi M, Al Hamoudi WK, et al. Nonalcoholic fatty liver disease burden-Saudi Arabia and United Arab Emirates, 2017–2030. Saudi J Gastroenterol 2018;24:211.  Back to cited text no. 23
[PUBMED]  [Full text]  
24.
García-Monzón C, Vargas-Castrillón J, Porrero JL, Alonso MT, Bonachía O, Castillo MJ, et al. Prevalence and risk factors for biopsy-proven non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in a prospective cohort of adult patients with gallstones. Liver Int 2015;35:1983-91.  Back to cited text no. 24
    
25.
Yener O, Aksoy F, Demır M, Özçelık A, Erengül C. Gallstones associated with nonalcoholic steatohepatitis (NASH) and metabolic syndrome. Turk J Gastroenterol 2010;21:411-5.  Back to cited text no. 25
    
26.
Qiao QH, Zhu WH, Yu YX, Huang FF, Chen LY. Nonalcoholic fatty liver was associated with asymptomatic gallstones in a Chinese population. Medicine 2017;96:e7853.  Back to cited text no. 26
    
27.
Yilmaz Y, Ayyildiz T, Akin H, Colak Y, Ozturk O, Senates E, et al. Gallstone disease does not predict liver histology in nonalcoholic fatty liver disease. Gut Liver 2014;8:313-7.  Back to cited text no. 27
    
28.
Spengler EK, Loomba R. Recommendations for diagnosis, referral for liver biopsy, and treatment of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Mayo Clin Proc 2015;90:1233-46.  Back to cited text no. 28
    
29.
Zhou JH, Cai JJ, She ZG, Li HL. Noninvasive evaluation of nonalcoholic fatty liver disease: Current evidence and practice. World J Gastroenterol 2019;25:1307-26.  Back to cited text no. 29
    
30.
Mikolasevic I, Orlic L, Franjic N, Hauser G, Stimac D, Milic S. Transient elastography (FibroScan(®)) with controlled attenuation parameter in the assessment of liver steatosis and fibrosis in patients with nonalcoholic fatty liver disease - Where do we stand?. World J Gastroenterol 2016;22:7236-51.  Back to cited text no. 30
    

Top
Correspondence Address:
Dr. Faisal A Alsaif
Department of Surgery, College of Medicine, King Saud University, PO Box 2925, Riyadh - 11461
Kingdom of Saudi Arabia
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/sjg.SJG_29_20

Rights and Permissions


    Figures

  [Figure 1], [Figure 2]
 
 
    Tables

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



 

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
    Study Population...
   Results
   Discussion
   Conclusion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed1022    
    Printed53    
    Emailed0    
    PDF Downloaded112    
    Comments [Add]    

Recommend this journal