Home Effects of sleeve gastrectomy on liver enzymes, non-alcoholic fatty liver disease-related fibrosis and steatosis scores in morbidly obese patients: first year follow-up
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Effects of sleeve gastrectomy on liver enzymes, non-alcoholic fatty liver disease-related fibrosis and steatosis scores in morbidly obese patients: first year follow-up

  • Evrim Kahramanoğlu Aksoy EMAIL logo , Zeynep Göktaş , Özgür Albuz , Muhammet Yener Akpınar , Doğan Öztürk , Hakan Buluş and Metin Uzman
Published/Copyright: March 6, 2019
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Journal of Laboratory Medicine
From the journal Journal of Laboratory Medicine Volume 43 Issue 2

Abstract

Background

Non-alcoholic fatty liver disease (NAFLD) has a high prevalence among patients undergoing laparoscopic sleeve gastrectomy (LSG). Although liver biopsy is the gold standard for assessing histopathologic changes in the liver, it is an invasive procedure. The objective of this study was to evaluate the effect of sleeve gastrectomy on liver enzymes, fibrosis and steatosis scores; ultrasonographic findings; biochemical parameters; and anthropometric measurements in morbidly obese patients with NAFLD.

Methods

Ninety-seven obese patients who underwent LSG were included in this study. Sex, age, body mass index (BMI), comorbidities, liver enzymes, ultrasonographic findings and laboratory parameters to calculate fibrosis and steatosis scores were collected before surgery and after 1 year of follow-up.

Results

A total of 88.7% of patients had liver steatosis at the pre-surgical ultrasonographic evaluation and this ratio decreased to 46.4% 1 year after surgery. Alanine aminotransferase (ALT), homeostatic model assessment of insulin resistance index (HOMA-IR), aspartate aminotransferase-to-platelet ratio index (APRI) and liver fat score (LFS) were significantly higher in patients with steatosis grade III vs. others. There were improvements in high-density lipoprotein (HDL), triglycerides (TG), glycated hemoglobin (HbA1c), glucose, insulin, BMI, liver enzymes and all NAFLD-related fibrosis and steatosis scores.

Conclusions

HOMA-IR, ALT, LFS and APRI scores can be used for follow-up procedures in morbidly obese patients with NAFLD who underwent LSG.

Keywords: non-alcoholic fatty liver disease; obesity; sleeve gastrectomy

Introduction

Non-alcoholic fatty liver disease (NAFLD) encompasses a wide spectrum of pathologies from simple fat accumulation in the liver to non-alcoholic steatohepatitis (NASH) or even cirrhosis. It is characterized by more than 5% lipid accumulation in the liver [1]. It has been associated with other components of metabolic syndrome such as type 2 diabetes mellitus, obesity, dyslipidemia, hypertension and cardiovascular diseases [2], [3]. NAFLD is expected to be the most common cause of end-stage liver disease and a common cause of liver transplantation. The number of end-stage liver disease and liver transplantation due to hepatitis C decreased due to the success of new antiviral treatments. The number of end-stage liver disease and liver transplantation due to NAFLD increased due to adoption of a sedentary lifestyle [4], [5], [6].

The prevalence of NAFLD has been found to range from 15% to 30% in the general population. It has a high prevalence among obese patients at 75.8%, of which 25% is NASH [7].

NAFLD is usually diagnosed through incidental findings of elevated liver enzymes, or with an imaging method that determines fatty liver. Although liver biopsy is the only effective method for assessing histopathologic changes in the liver, it is not clear as to whether it should be obtained from all patients because it is an invasive procedure and associated with morbidity and mortality [8]. Losing weight is the gold standard treatment option for obesity-related NAFLD. Bariatric surgery is the most effective treatment for those who cannot achieve permanent weight loss with lifestyle changes, exercise and diet programs [9]. Reduction of steatosis and reversal of fibrosis were demonstrated by liver biopsies in patients who underwent bariatric surgery [10].

In clinical practice, liver enzymes and laboratory-based formulae are frequently used in the follow-up of patients with NAFLD [7]. The aim of this study was to evaluate the effect of sleeve gastrectomy on liver enzymes, fibrosis and steatosis scores, ultrasonographic findings, biochemical parameters and anthropometric measurements in morbidly obese patients with NAFLD.

Materials and methods

Patients

Ninety-seven obese patients who underwent laparoscopic sleeve gastrectomy (LSG) between January 2015 and January 2017 at Keçiören Training and Research Hospital general surgery service were included in this retrospective study. All patients were aged over 18 years and met the criteria and clinical guidelines for bariatric surgery. Patients with alcoholic, viral and autoimmune liver diseases were excluded. Sex, age, body mass index (BMI), comorbidities, liver enzymes, ultrasonographic findings and laboratory parameters to calculate fibrosis and steatosis scores were collected before surgery and after 1 year of follow-up. This study was approved by the Institutional Local Ethics Committee.

Laboratory parameters, fibrosis and steatosis scores

Non-invasive liver fibrosis and steatosis scores can be used to detect NAFLD to avoid invasive liver biopsies and expensive imaging modalities. These scores are based on standard laboratory parameters and anthropometric measurements.

BMI (kg/m2) was calculated using weight (kg) and height (m) measurements. Serum levels of fasting blood glucose (mg/dL), insulin (μU/mL), alanine aminotransferase (ALT, U/L), aspartate aminotransferase (AST, U/L), alkaline phosphatase (ALP, U/L) and γ-glutamyl transpeptidase (GGT, U/L), total cholesterol (TC, mg/dL), triglycerides (TG, mg/dL), high-density lipoprotein (HDL, mg/dL), low-density lipoprotein (LDL, mg/dL), albumin (g/dL), total bilirubin (ng/dL), C-reactive protein (CRP, mg/L), glycated hemoglobin (HbA1c, %) and platelet counts were recorded.

The hepatic steatosis index (HSI), liver fat score (LFS), AST-to-platelet ratio index (APRI), fibrosis-4 (FIB-4), NAFLD-fibrosis score (NAFLDFS) and homeostatic model assessment of insulin resistance index (HOMA-IR) were calculated according to the following formulae:

(1)HSI=8×ALT/AST+BMI  (+2 if type 2 diabetes, +2 if female) [11]
(2)LFS=−2.89+1.18×metabolic syndrome (yes: 1, no: 0) + 0.45×type 2 diabetes (yes: 2, no: 0)  + 0.15 insulin inμU/L+0.04 × AST in U/L–0.94×AST/ALT [12]
(3)APRI=([AST/ULN ALT]×100)/platelets [109/L]) [13]
(4)FIB-4=(age [years]×AST [U/L])/ (platelets [109​/L]×ALT [U/L]) [14]
(5)NAFLDFS=−1.675+0.037×age (years) + 0.094×BMI (kg/m2)+ 1.13 × IFG/diabetes (yes=1,no=0)+ 0.99 × IAST/ALT ratio–0.013×platelet (×109/L) – 0.66×albumin (g/dL) [15]
(6)HOMA-IR=glucose level (mg/dL)  × insulin concentration (μU/mL)/405 [16]

Ultrasonography

Abdominal ultrasonography was performed in all patients by the same doctor preoperatively and 1 year after surgery on the same day when the blood samples were collected and anthropometric measurements were recorded. Ultrasonographic steatosis severity assessment was as follows: grade I (mild) – increased parenchymal echogenicity with obvious periportal and diaphragmatic echogenicity; grade II (moderate) – increased parenchymal echogenicity with impaired appearance of the echogenic walls of the portal vein branches and grade III (severe) – increased parenchymal echogenicity with indistinguishable periportal echogenicity and impaired appearance of the diaphragmatic outline.

Statistical analysis

Statistical analyses were performed using the Statistical Package for the Social Sciences (SPSS) 22.0 software package (IBM, Armonk, NY, USA). The Kolmogorov-Smirnov and Shapiro-Wilk tests of normality were used to test the distribution of variables. The paired-sample t-test and analysis of variance (ANOVA) were used for the comparison of group means. The Wilcoxon signed-rank and Kruskal-Wallis tests were used to analyze nonparametric data. McNemar’s test was used to compare nominal variables between pre- and post-surgery data. Pearson correlation was used to evaluate the linear relationship between the tested biomarkers. Data are presented as means±standard deviation or median (interquartile range) or number and percentage. Differences were considered significant at p<0.05.

Results

A total of 97 patients’ data were evaluated. No complications were observed during follow-up. The demographic characteristics of the patients are shown in Table 1.

Table 1:

Demographic characteristics of the patients.

n=97
Age, years (mean±SD)38.0±11.48
BMI, kg/m2 (mean±SD)44.9±5.15
Sex, % (M/F)75.3/24.7
Hypertension, %[16] 15.7%
Diabetes, %[17] 23.5%
Dyslipidemia[11] 10.8%

  1. BMI, body mass index; SD, standard deviation.

Ultrasonography

Some 88.7% of the patients had liver steatosis at the pre-surgical ultrasonographic evaluation and this ratio decreased to 46.4% 1 year after surgery. Grade III steatosis was present in 22.7% of patients pre-surgically, but there was no grade III steatosis 1 year after surgery (Table 2). More than half (53.6%) of the patients had no steatosis 1 year after surgery.

Table 2:

Ultrasonographic findings of the patients pre-surgery and 12 months post-surgery.

USGPre-surgery (n=97)Post-surgery (12 months) (n=97)p-Valuea
−11 (11.3%)52 (53.6%)<0.001
+30 (30.9%)42 (43.3%)>0.05
++34 (35.1%)3 (3.1%)<0.001
+++22 (22.7%)0 (0.0%)–

  1. aMcNemar’s test was used for analysis. USG, ultrasonographic findings. Bold values indicate significant p-value.

ALT, HOMA-IR, APRI and LFS levels were significantly higher in patients with grade III steatosis compared with others (Figure 1A–D).

Figure 1: HOMA-IR, ALT, APRI and LFS levels in different steatosis grades.(A) HOMA-IR scores were significantly higher in steatosis grade III vs. others. (B) ALT levels were significantly higher in steatosis grade III vs. others. (C) APRI scores were significantly higher in steatosis grade III vs. others. (D) LFS scores were significantly higher in steatosis grade III vs. others.
Figure 1:

HOMA-IR, ALT, APRI and LFS levels in different steatosis grades.

(A) HOMA-IR scores were significantly higher in steatosis grade III vs. others. (B) ALT levels were significantly higher in steatosis grade III vs. others. (C) APRI scores were significantly higher in steatosis grade III vs. others. (D) LFS scores were significantly higher in steatosis grade III vs. others.

Anthropometric and laboratory parameters of patients at the 1-year follow-up

Table 3 shows the differences of anthropometric and laboratory parameters at baseline and at the first year after surgery. The BMI at baseline was 44.9±5.15 kg/m2 and declined to 27.7±3.42 kg/m2 at the first year. There was a significant improvement in glucose (111.5±43.80 mg/dL vs. 85.3±10.86 mg/dL; p<0.001), insulin (15.7±9.18 mg/dL vs. 6.09±2.25 mg/dL; p<0.001) and HbA1c (6.1±1.20% vs. 5.18±0.75%; p<0.001) levels. There was also a significant decrease in TG (152.7±69.21 mg/dL vs. 113.8±63.00 mg/dL; p<0.001) and HOMA-IR (4.37±2.82 vs. 1.29±0.53; p<0.001) and a significant increase in HDL (40.9±7.48 mg/dL vs. 48.9±8.32 mg/dL; p<0.001), albumin (4.02±0.37 g/dL vs. 4.20±0.81 g/dL; p<0.001) and platelet levels (273.1±71.48×103/L vs. 298.6±68.08×103/L; p<0.001).

Table 3:

Anthropometric and biochemical characteristics of the patients pre-surgery and 12 months post-surgery.

Pre-surgery (n=97)Post-surgery (12 months) (n=97)Paired differencesp-Valuea
Weight, kg122.9±15.2776.6±9.8146.3±11.01<0.001
BMI, kg/m244.9±5.1527.7±3.4217.3±4.70<0.001
HbA1c, %6.16±1.205.18±0.750.98±0.88<0.001
Glucose, mg/dL111.5±43.8085.3±10.8626.2±39.44<0.001
Insulin, mg/dL15.7±9.186.09±2.259.73±8.33<0.001
HOMA-IR4.37±2.821.29±0.533.08±2.59<0.001
Creatinine, mg/dL0.81±0.880.71±0.110.01±0.11>0.05
Total protein, g/dL6.40±1.717.10±0.420.85±1.21>0.05
Albumin, g/dL4.02±0.374.20±0.81−0.35±0.400.001
Total bilirubin, mg/dL0.73±0.450.84±0.59−0.14±0.46>0.05
Direct bilirubin, mg/dL0.28±0.190.29±0.14−0.03±0.21>0.05
Total cholesterol, mg/dL196.8±38.89202.3±27.3810.1±35.47>0.05
HDL, mg/dL40.9±7.4848.9±8.32−8.18±6.73<0.001
Triglyceride, mg/dL152.7±69.21113.8±63.0074.4±59.11<0.001
WBC (×109/L)9.19±3.317.38±2.381.23±2.150.001
Neutrophils5.69±2.864.32±1.891.07±1.75<0.001
Lymphocytes2.51±0.802.45±0.650.09±0.46>0.05
Monocytes0.57±0.350.41±0.110.16±0.32<0.001
Platelet (×103/L)273.1±71.48298.6±68.08−26.5±59.94<0.001
PDW17.9±1.1617.7±1.120.21±1.02>0.05
MPV, fL8.25±1.588.12±1.650.09±1.30>0.05
Hemoglobin, g/dL13.5±1.9513.0±1.760.21±2.31>0.05
PCT, ng/mL0.21 (0.03)0.22 (0.09)−0.174b>0.05
Ferritin, ng/mL45.7 (67.4)17.1 (26.2)3.458b0.001
CRP, mg/dL1.89±4.480.32±0.601.32±2.87>0.05
B12, pg/mL292.9±16.11285.6±15.3020.4±19.8>0.05
Vitamin D, ng/mL16.7±3.1419.6±4.28−6.31±2.630.009

  1. aPaired t-test and Wilcoxon signed-rank test were used for analysis. bZ-score for Wilcoxon signed-rank test. BMI, body mass index; HbA1c, glycated hemoglobin; HOMA-IR, homeostatic model assessment of insulin resistance index; HDL, high-density lipoprotein; WBC, white blood cells; PDW, platelet distribution width; MPV, mean platelet volume; PCT, procalcitonin; CRP, C-reactive protein. Bold values indicate significant p-value.

Liver enzymes and fibrosis and steatosis scores

Liver enzymes and fibrosis and steatosis scores are shown in Table 4. There was a significant improvement in AST (26.0±14.90 U/L vs. 14.7±5.13 U/L; p<0.001), ALT (30.6±19.03 U/L vs. 15.2±7.70 U/L; p<0.001), GGT (36.1±26.62 U/L vs. 16.7±9.92 U/L; p<0.001) and ALP (74.7±21.28 U/L vs. 65.7±16.52 U/L; p=0.04). APRI (0.21 [0.18] vs. 0.12 [0.07]; p<0.001), FIB-4 (0.64 [0.44] vs. 0.51 [0.35]; p<0.001), NAFLDFS (−0.05±1.20 vs. −2.96±1.19; p<0.001), HSI (53.9±8.35 vs. 38.2±4.84; p<0.001) and LFS (1.00±1.65 vs. −2.41±0.56; p<0.001) improved at the first year after surgery.

Table 4:

Liver enzyme levels and NAFLD characteristics of the patients pre-surgery and 12 months post-surgery.

Pre-surgery (n=97)Post-surgery (12 months) (n=97)Paired differencesp-Valuea
ALT, U/L30.6±19.0315.2±7.7015.7±18.77<0.001
AST, U/L26.0±14.9014.7±5.1311.6±14.04<0.001
GGT, U/L36.1±26.6216.7±9.9219.5±21.870.001
ALP, U/L74.7±21.2865.7±16.527.56±18.130.040
APRI0.21 (0.18)0.12 (0.07)−7.493b<0.001
FIB40.64 (0.44)0.51 (0.35)−4.308b<0.001
HSI53.9±8.3538.2±4.8415.7±8.45<0.001
LFS1.00±1.65−2.41±0.563.45±1.60<0.001
NAFLDFS−0.05±1.20−2.96±1.193.05±0.85<0.001

  1. aPaired t-test and Wilcoxon signed-rank test were used for analysis. bZ-score for Wilcoxon signed-rank test. NAFLD, non-alcoholic fatty liver disease; ALT, alanine aminotransferase; AST, aspartate aminotransferase; GGT, γ-glutamyl transpeptidase; ALP, alkaline phosphatase; APRI, AST to platelet ratio index; FIB4, fibrosis-4; HIS, hepatic steatosis index; LFS, liver fat score; NAFLDFS, NAFLD-fibrosis score. Bold values indicate significant p-value.

Correlation between liver enzymes, fibrosis and steatosis scores and anthropometric variables

The correlations between liver enzymes, fibrosis and steatosis scores before and after surgery are shown in Tables 5 and 6, respectively. Before surgery, APRI scores positively correlated with HOMA-IR, ALT, AST, GGT, LFS and NAFLDFS (r=0.215, p=0.034; r=0.552, p<0.001; r=0.694, p<0.001; r=0.399, p<0.001; r=0.353, p=0.001; and r=0.499, p<0.001, respectively), whereas after surgery, APRI scores positively correlated with only ALT, AST and LFS scores (r=0.339, p=0.003; r=0.597, p<0.001; and r=0.245, p=0.044; respectively). FIB-4 showed a strong positive correlation with NAFLDS before and after surgery (r=0.689, p<0.001 and r=0.739, p<0.001, respectively). There were significant positive correlations between HSI and BMI before and after surgery (r=0.466, p<0.001 and r=0.626, p<0.001, respectively). LFS showed positive correlations with HbA1c, HOMA-IR and GGT before and after surgery (pre-surgery: r=0.249, p=0.016; r=0.807, p<0.001; and r=0.280, p=0.005, respectively; post-surgery: r=0.299, p=0.013; r=0.698, p<0.001; and r=0.341, p=0.004, respectively).

Table 5:

Correlations of anthropometric and liver parameters with NAFLD characteristics of the patients pre-surgerya.

APRIFIB4HSILFS
Weight, kgr=0.188r=−0.011r=0.188r=0.251
p>0.05p>0.05p>0.05p=0.015
BMI, kg/m2r=−0.033r=0.0r=0.466r=0.033
p>0.05p>0.05p<0.001p>0.05
HbA1c, %r=0.164r=0.150r=0.033r=0.249
p>0.05p>0.05p>0.05p=0.016
HOMA-IRr=0.215r=0.076r=−0.011r=0.807
p=0.034p>0.05p>0.05p<0.001
ALT, U/Lr=0.552r=0.066r=−0.235r=0.517
p<0.001p>0.05p=0.021p<0.001
AST, U/Lr=0.694r=0.511r=0.013r=0.352
p<0.001p<0.001p>0.05p=0.001
GGT, U/Lr=0.399r=0.146r=−0.106r=0.289
p<0.001p>0.05p>0.05p=0.005
ALP, U/Lr=−0.114r=−0.264r=0.236r=0.086
p>0.05p>0.05p>0.05p>0.05
LFSr=0.353r=0.079r=−0.0651
p=0.001p>0.05p>0.05
NAFLDFSr=0.449r=0.689r=0.105r=−0.056
p<0.001p<0.001p>0.05p>0.05

  1. aPearson correlation test was used for analysis. NAFLD, non-alcoholic fatty liver disease; BMI, body mass index; HbA1c, glycated hemoglobin; HOMA-IR, homeostatic model assessment of insulin resistance index; ALT, alanine aminotransferase; AST, aspartate aminotransferase; GGT, γ-glutamyl transpeptidase; ALP, alkaline phosphatase; APRI, AST to platelet ratio index; FIB4, fibrosis-4; HIS, hepatic steatosis index; LFS, liver fat score; NAFLDFS, NAFLD-fibrosis score. Bold values indicate significant p-value.

Table 6:

Correlations of anthropometric and liver parameters with NAFLD characteristics of patients 12 months post-surgerya.

APRIFIB4HSILFS
Weight, kgr=0.129r=0.108r=0.329r=0.165
p>0.05p>0.05p=0.001p>0.05
BMI, kg/m2r=−0.084r=0.012r=0.626r=0.088
p>0.05p>0.05p<0.001p>0.05
HbA1c, %r=−0.007r=0.149r=−0.179r=0.299
p>0.05p>0.05p>0.05p=0.013
HOMA-IRr=0.148r=0.128r=0.069r=0.698
p>0.05p>0.05p>0.05p<0.001
ALT, U/Lr=0.339r=0.025r=−0.211r=0.114
p=0.003p>0.05p>0.05p>0.05
AST, U/Lr=0.597r=0.097r=−0.257r=0.139
p<0.001p>0.05p=0.019p>0.05
GGT, U/Lr=0.153r=0.045r=−0.135r=0.341
p>0.05p>0.05p>0.05p=0.004
ALP, U/Lr=0.402r=0.251r=0.140r=0.177
p=0.030p>0.05p>0.05p>0.05
LFSr=0.245r=0.052r=−0.2341
p=0.044p>0.05p>0.05
NAFLDFSr=0.269r=0.739r=0.189r=−0.416
p>0.05p<0.001p>0.05p=0.020

  1. aPearson correlation test was used for analysis. NAFLD, non-alcoholic fatty liver disease; BMI, body mass index; HbA1c, glycated hemoglobin; HOMA-IR, homeostatic model assessment of insulin resistance index; ALT, alanine aminotransferase; AST, aspartate aminotransferase; GGT, γ-glutamyl transpeptidase; ALP, alkaline phosphatase; APRI, AST-to-platelet ratio index; FIB4, fibrosis-4; HIS, hepatic steatosis index; LFS, liver fat score; NAFLDFS, NAFLD-fibrosis score. Bold values indicate significant p-value.

Discussion

Despite widespread use of elevated liver enzymes and imaging techniques, liver biopsy is the gold standard for demonstrating liver injury. Although being an invasive procedure, liver biopsies are performed with no morbidity and mortality in bariatric surgery studies where the liver is evaluated [18]. However, it is an expensive and invasive procedure for post-surgical follow-up. We evaluated pre- and post-surgical laboratory parameters and fibrosis and steatosis scores of patients undergoing LSG who were diagnosed as having NAFLD according to pre-surgical elevated liver enzymes that were unexplained by other reasons or ultrasonographic findings. There were improvements in HDL, TG, HbA1c, glucose, insulin, BMI and liver enzymes and all NAFLD-related fibrosis and steatosis scores.

In this study, we found a significant difference between pre- and post-surgical liver enzymes (ALT, AST, GGT, ALP), similar to previous findings demonstrating positive effects of bariatric surgery on liver enzymes and histologic findings of the liver [10], [19], [20], [21], [22]. Although some studies suggested that ALT alone or both ALT and AST might be used as follow-up markers of NAFLD in patients undergoing bariatric surgery, Dixon et al. indicated that decreases in GGT levels, and less frequently in AST levels, might predict histologic recovery more accurately in these patients [19], [21], [23]. In our study, we did not perform liver biopsy, but we found that ALT levels were significantly higher in patients with grade III steatosis, but this was not reflected in AST or GGT levels.

Simpler and more easily applicable methods are considered for following up patients with NAFLD instead of liver biopsy because of its cost and the risk of morbidity and mortality. APRI, FIB-4 and NAFLDFS, which are combinations of serum-based parameters and clinical variables, are the most commonly used scores to assess fibrosis [24]. Although preoperative values were not high, a significant decrease was observed when compared with postoperative values in our study. Nickel et al. demonstrated a significant improvement at the 1-year follow-up in AST/ALT ratio, APRI, NAFLDFS and BARD score. There was no difference between Roux-en-Y gastric bypass (RYGB) and LSG [19]. Cazzo et al. showed a 55% resolution of fibrosis in NAFLDFS after RYGB [17].

Although screening of asymptomatic individuals at risk for NAFLD is usually performed using imaging modalities such as ultrasonography, computed tomography or magnetic resonance imaging (MRI), these methods are expensive for population screening. Liver ultrasonography is the first-line procedure in the detection of liver steatosis, but it is expensive, operator dependent, not widely available and only detects steatosis if present in more than 20–30% of hepatocytes. Therefore, there is a need to use simple, noninvasive, accurate and cheaper scores to identify patients at high risk for NAFLD [11], [25], [26]. In our study, there were improvements in HSI and LFS indexes after surgery, as shown in patients with NAFLD previously.

Transabdominal ultrasonographic screening for gallstones or potential liver diseases is suggested before bariatric surgery by several centers. In this study, we found that 88.7% of patients had liver steatosis. This result was compatible with the study by Tovar et al. who found that 84% of patients had liver steatosis before surgery [20]. In our study, 11 patients had no liver steatosis before surgery and they continued without it, and 41 patients (47.7%) with steatosis of different grades showed complete resolution after surgery. Almazeedi et al. found that 57.2% of patients had fatty liver before surgery [26]. Alsina et al. demonstrated a reduction in the percentage of lipids in the hepatocytes and liver volume, as determined using MR spectroscopy (MRS) and MRI. They represented disappearance of preoperative steatosis in 54.9% of patients [27]. Our findings were compatible with their results.

Obesity is associated with impaired lipid metabolism, and dyslipidemia is one of the most important risk factor for NAFLD. We found a significant improvement in HDL and TG values after bariatric surgery. These results were compatible with previous studies. Karcz et al. found a significant improvement in HDL and TG levels in morbidly obese patients with NASH [28]. However, Karcz et al. showed an improvement in TG levels only in patients who underwent bariatric surgery with healthy livers. Ooi et al. showed a significant improvement in HDL, LDL, TG and TC levels [29]. In our study, the majority of patients had no recorded LDL values, so we were not able to compare these, and the improvement in TC level was not statistically significant.

The major limitations of our study are its retrospective design and lack of histologic assessment of the liver. Therefore, we were not able to compare pathologic fibrosis and steatosis scores with laboratory parameters and calculated scores. Although we used ultrasonographic findings for steatosis grading, the dependence of ultrasonographic evaluation on the individual is an important limitation. MRI and MRS, which are closer to the histological evaluation of liver fat, are very expensive and not accessible everywhere.

We showed a positive correlation between weight and ALT levels. However, there was no correlation between ALT and BMI levels. There was also a positive correlation between ALT levels, HOMA-IR, LFS and APRI, also between AST levels and APRI, FIB-4 and LFS and between GGT levels and HOMA-IR, APRI and LFS. Furthermore, there was a positive correlation between ALP levels and BMI. ALT, HOMA-IR, APRI and LFS levels were significantly higher in patients with grade III steatosis compared with other patients.

NAFLD is commonly seen in morbidly obese patients. It is known that bariatric surgery is effective in reducing weight and accompanying comorbidities in these patients. Postoperative liver biopsy is not routinely performed and is not risk free. This study demonstrated the positive effects of bariatric surgery on biochemical parameters, scoring systems and ultrasonographic findings. Although not the gold standard, HOMA-IR, ALT, LFS and APRI values can be used in the follow-up of morbidly obese patients with NAFLD who underwent LSG.

Correspondence: Evrim Kahramanoğlu Aksoy Aksoy, MD, Department of Gastroenterology, Keçiören Training and Research Hospital, Pınarbaşı Mah., Sanatoryum Caddesi Ardahan Sokak D:25, 06280 Keçiören/Ankara, Turkey, Tel.: 00905332121579

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: None declared.

  3. Employment or leadership: None declared.

  4. Honorarium: None declared.

  5. Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.

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Received: 2018-11-18
Accepted: 2019-01-23
Published Online: 2019-03-06
Published in Print: 2019-04-24

©2019 Walter de Gruyter GmbH, Berlin/Boston

This article is distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Articles in the same Issue

  1. Frontmatter
  2. Infectiology and Microbiology
  3. Seroprevalence and geographical distribution of hepatitis C virus in Iranian patients with thalassemia: a systematic review and meta-analysis
  4. Geriatric Laboratory
  5. White blood cell counts, CRP, GGT and LDH in the elderly German population
  6. Laboratory Management
  7. Pre-analytical quality control in hemostasis laboratories: visual evaluation of hemolysis index alone may cause unnecessary sample rejection
  8. Endocrinology
  9. Direct laboratory evidence that pregnancy-induced hypertension might be associated with increased catecholamines and decreased renalase concentrations in the umbilical cord and mother’s blood
  10. Allergy and Autoimmunity
  11. Investigating the presence of human anti-mouse antibodies (HAMA) in the blood of laboratory animal care workers
  12. Original Articles
  13. Lipid indexes and parameters of lipid peroxidation during physiological pregnancy
  14. Biomarkers of oxidative stress in pregnant women with recurrent miscarriages
  15. Effects of sleeve gastrectomy on liver enzymes, non-alcoholic fatty liver disease-related fibrosis and steatosis scores in morbidly obese patients: first year follow-up
  16. Laboratory Case Report
  17. Neuroendocrine differentiation of prostatic adenocarcinoma – an important cause for castration-resistant disease recurrence
https://doi.org/10.1515/labmed-2018-0181
Keywords for this article
non-alcoholic fatty liver disease; obesity; sleeve gastrectomy
Creative Commons
BY-NC-ND 3.0

Articles in the same Issue

  1. Frontmatter
  2. Infectiology and Microbiology
  3. Seroprevalence and geographical distribution of hepatitis C virus in Iranian patients with thalassemia: a systematic review and meta-analysis
  4. Geriatric Laboratory
  5. White blood cell counts, CRP, GGT and LDH in the elderly German population
  6. Laboratory Management
  7. Pre-analytical quality control in hemostasis laboratories: visual evaluation of hemolysis index alone may cause unnecessary sample rejection
  8. Endocrinology
  9. Direct laboratory evidence that pregnancy-induced hypertension might be associated with increased catecholamines and decreased renalase concentrations in the umbilical cord and mother’s blood
  10. Allergy and Autoimmunity
  11. Investigating the presence of human anti-mouse antibodies (HAMA) in the blood of laboratory animal care workers
  12. Original Articles
  13. Lipid indexes and parameters of lipid peroxidation during physiological pregnancy
  14. Biomarkers of oxidative stress in pregnant women with recurrent miscarriages
  15. Effects of sleeve gastrectomy on liver enzymes, non-alcoholic fatty liver disease-related fibrosis and steatosis scores in morbidly obese patients: first year follow-up
  16. Laboratory Case Report
  17. Neuroendocrine differentiation of prostatic adenocarcinoma – an important cause for castration-resistant disease recurrence
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