SHOULD ROUTINE LIVER BIOPSY BE CONSIDERED IN BARIATRIC SURGICAL PRACTICE? AN ANALYSIS OF THE LIMITATIONS OF NON-INVASIVE NAFLD MARKERS

CONCON, Matheus Mathedi; GESTIC, Martinho Antonio; UTRINI, Murillo Pimentel; CHAIM, Felipe David Mendonça; CHAIM, Elinton Adami; CAZZO, Everton

doi:10.1590/S0004-2803.202200001-19

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ORIGINAL ARTICLE • Arq. Gastroenterol. 59 (01) • Jan-Mar 2022 • https://doi.org/10.1590/S0004-2803.202200001-19 copy

SHOULD ROUTINE LIVER BIOPSY BE CONSIDERED IN BARIATRIC SURGICAL PRACTICE? AN ANALYSIS OF THE LIMITATIONS OF NON-INVASIVE NAFLD MARKERS

A realização sistemática de biópsia hepática deveria ser considerada na prática cirúrgica bariátrica? Uma análise das limitações de marcadores não-invasivos de DHGNA

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Background

Non-invasive markers are useful and practical tools for assessing non-alcoholic fatty liver disease (NAFLD), but liver biopsy remains the gold-standard method. Liver biopsy can be easily obtained on individuals undergoing bariatric surgery, but there is no ultimate evidence on the relationship between costs, risks and benefits of its systematic performance.

Objective

To compare the diagnostic accuracy of non-invasive methods with liver biopsy for detection and staging of NAFLD in obese individuals undergoing bariatric surgery.

Methods

This is a cross-sectional, observational and descriptive study which enrolled individuals who underwent bariatric surgery from 2018 through 2019 at a public tertiary university hospital. Ultrasound scan, hepatic steatosis index, Clinical Non-Alcoholic Steatohepatitis Score (C-NASH), hypertension, alanine aminotransferase (ALT) and insulin resistance (HAIR), aspartate aminotransferase (AST) to Platelet Ratio Index (APRI), NAFLD Fibrosis Score (NFS) and body mass index, AST/ALT ratio, and diabetes (BARD) were the methods compared with the histopathological examination of wedge liver biopsies collected during surgery.

Results

Of 104 individuals analyzed, 91 (87.5%) were female. The mean age was 34.9±9.7 years. There was no biopsy-related morbidity. The respective overall accuracies of each marker analyzed were: ultrasound scan (79.81% for steatosis), hepatic steatosis index (79.81% for steatosis), HAIR (40.23% for steatohepatitis), C-NASH (22.99% for steatohepatitis), APRI (94.23% for advanced fibrosis), NFS (94.23% for advanced fibrosis), and BARD (16.35% for advanced fibrosis).

Discussion

Given the high prevalence of liver disease within this population, even the most accurate markers did not present enough discretionary power to detect and/or rule out the NAFLD aspects they were designed to assess in comparison with liver biopsy, which is safe and easy to obtain in these patients.

Conclusion

Wedge liver biopsy during bariatric surgery helps to diagnose and stage NAFLD, presents low risks and acceptable costs; given the limitations of non-invasive methods, it is justifiable and should be considered in bariatric routine.

Keywords:
Non-alcoholic fatty hepatopathy; fatty liver; obesity; bariatric surgery; liver function tests

Score	Rationale	How to perform or calculate		Cut-off values and interpretation
US	Used to determine the presence of liver steatosis⁵5. National Institutes of Health. Gastrointestinal surgery for severe obesity: National Institutes of Health Consensus Development Conference Statement. Am J Clin Nutr. 1992;55:(Suppl 2);615S-9S. doi: 10.1093/ajcn/55.2.615s. https://doi.org/10.1093/ajcn/55.2.615s... .	Qualitative visualization of hepatic echogenicity, measurement of the difference of the hepatic parenchyma compared to the renal parenchyma, evaluation of the penetration of the deep portion of the liver and through the determination of the hepatic structures, for example.		Subjective: normal, mild, moderate or severe.

HSI	Created to predict the occurrence of steatosis in the general population⁶6. Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:7392-402..	HSI =8 x ALT/AST + BMI (+2 if T2DM, +2 if female)		A score >36 indicates the presence of steatosis, while a score <30 indicates absence of steatosis.

NFS	Designed for prediction of advanced fibrosis in NAFLD patients⁶6. Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:7392-402..	NFS =-1.675 + 0.037 X age (years) + 0.094 X BMI (kg/m²) X IGT/T2D (Yes =1 OR No =0) +0.99 X AST/ALT — 0.013 X Platelet count (X 10⁹/L) — 0.66 X Albumin (g/dL)		A score over 0.676 indicates advanced fibrosis, while a score below -1.455 excludes advanced fibrosis.

APRI	Developed to predict advanced fibrosis and cirrhosis in patients with hepatitis C, it was then validated for detection of advanced fibrosis in NAFLD⁶6. Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:7392-402..	APRI = {[(observed AST/AST (upper limit in iU/L)] / Platelet count (10⁹/L)} x 100		A score 0.98 indicates advanced fibrosis.

BARD	Derived to detect advanced fibrosis in a population comprised exclusively of individuals with biopsy-proven NAFLD⁷7. Lee JH, Kim D, Kim HJ, Lee CH, Yang JI, Kim W, et al. Hepatic steatosis index: a simple screening tool reflecting nonalcoholic fatty liver disease. Dig Liver Dis. 2010;42:503-8..	BMI greater than or equal to 28 earns 1 point, AST/ALT ratio greater than or equal to 0.8 earns 2 points and presence of diabetes earns 1 point.		BARD Score	Risk of advanced fibrosis
				0—1	Low
				2—4	High

HAIR	Developed to detect steatohepatitis in bariatric surgery patients⁸8. Dixon JB, Bhathal PS, O’Brien PE. Nonalcoholic fatty liver disease: Predictors of nonalcoholic steatohepatitis and liver fibrosis in the severely obese. Gastroenterology. 2001;121:91-100..	The variables used are the presence of hypertension, ALT greater than 40 and an insulin resistance index greater than 5. Each variable earns 1 point.		A sum of points ≥2 indicates a high probability of NASH.

C-NASH	Designed to predict the occurrence of NASH based in clinical characteristics⁶6. Lee SS, Park SH. Radiologic evaluation of nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:7392-402..	Clinical aspect	Points	A sum of points ≥3 indicates the presence of steatohepatitis.
		BMI (kg/m²)
		40—45	1
		>45	2
		AST >40 iU/L	2
		Triglycerides >140 mg/dL	1

	N (%)
Steatosis	84 (80.8%)
Macrovesicular	83 (79.8%)
Mild	58 (55.8%)
Moderate	21 (20.2%)
Severe	3 (2.9%)
Microvesicular	30 (28.8%)

Fibrosis	86 (82.7%)
0	18 (17.3%)
1a	38 (36.5%)
1b	4 (3.8%)
1c	2 (1.9%)
2	38 (36.5%)
3	4 (3.9%)
4	0 (0%)

Steatohepatitis	85 (81.7%)
Acinar inflammation	80 (76.9%)
Mild	58 (55.8%)
Moderate	19 (18.3%)
Severe	3 (2.9%)
Portal inflammation	84 (80.8%)
Mild	61 (58.7%)
Moderate	22 (21.2%)
Severe	1 (1%)

Fasting glucose (mg/dL)	91.5±27.8
Aspartate aminotransferase (U/L)	22.9±11.1
Alanine aminotransferase (U/L)	28±22.8
Alkaline phosphatase (U/L)	65.2±18.2
Gamma-Glutamyl Transferase (U/L)	23.1±14.7
Platelet count (x10⁹/L)	271.7±81.6
Albumin (g/dL)	4.3±0.3
Insulin (mU/L) (N=87)	15.6±10.7
Triglycerides (mg/dL)	106.9±55.9
High density lipoprotein (mg/dL)	38.2±8.5
Total cholesterol (mg/dL)	166.8±33.5
Homeostasis model assessment — insulin resistance (HOMA-IR) (N=87)	3.5±2.6

	Test/disease	Present	Absent	Total
Ultrasound scan (diagnosis of steatosis)	Present	True positive: 83	False positive: 20	103
	Absent	False negative: 1	True negative: 0	1
	Total	84	20	104
	Sensitivity: 98.81%; specificity: 0; positive predictive value: 80.58%; negative predictive value: 0; positive likelihood ratio: 0.99; negative likelihood ratio: 0; overall accuracy: 79.81%.

HSI (diagnosis of steatosis)	Present	True positive: 83	False positive: 20	103
	Absent	False negative: 1	True negative: 0	1
	Total	84	20	104
	Sensitivity: 98.81%; specificity: 0; positive predictive value: 80.58%; negative predictive value: 0; positive likelihood ratio: 0.99; negative likelihood ratio: 0; overall accuracy: 79.81%.

HAIR (diagnosis of steatohepatitis)	Present	True positive: 26	False positive: 7	33
	Absent	False negative: 45	True negative: 9	54
	Total	71	16	87
	Sensitivity: 36.62%; specificity: 56.25%; positive predictive value: 78.79%; negative predictive value: 16.67%; positive likelihood ratio: 0.84; negative likelihood ratio: 1.13; overall accuracy: 40.23%.

C-NASH (diagnosis of steatohepatitis)	Present	True positive: 4	False positive: 0	4
	Absent	False negative: 67	True negative: 16	83
	Total	71	16	87
	Sensitivity: 5.63%; specificity: 100%; positive predictive value: 100%; negative predictive value: 19.28%; positive likelihood ratio: 0; negative likelihood ratio: 0.94; overall accuracy: 22.99%.

APRI (diagnosis of advanced fibrosis)	Present	True positive: 0	False positive: 2	2
	Absent	False negative: 4	True negative: 98	102
	Total	4	100	104
	Sensitivity: 0; specificity: 98%; positive predictive value: 0; negative predictive value: 96.08%; positive likelihood ratio: 0; negative likelihood ratio: 1.02; overall accuracy: 94.23%.

NFS (diagnosis of advanced fibrosis)	Present	True positive: 0	False positive: 2	2
	Absent	False negative: 4	True negative: 98	102
	Total	4	100	104
	Sensitivity: 0; specificity: 98%; positive predictive value: 0; negative predictive value: 96.08%; positive likelihood ratio: 0; negative likelihood ratio: 1.02; overall accuracy: 94.23%.

BARD (diagnosis of advanced fibrosis)	Present	True positive: 4	False positive: 87	91
	Absent	False negative: 0	True negative: 13	13
	Total	4	100	104
	Sensitivity: 100%; specificity: 13%; positive predictive value: 4.40%; negative predictive value: 100%; positive likelihood ratio: 1.15; negative likelihood ratio: 0; overall accuracy: 16.35%.

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[1] Corresponding author: Everton Cazzo. E-mail: evertoncazzo@yahoo.com.br