Comparison of different liver fibrosis scores following sleeve gastrectomy

doi:10.21203/rs.3.rs-4866913/v1

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Short Report

Comparison of different liver fibrosis scores following sleeve gastrectomy

https://doi.org/10.21203/rs.3.rs-4866913/v1

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Purpose

The prevalence of obesity, along with that of its associated health conditions, including cardiovascular diseases, diabetes mellitus, and liver diseases, such as non-alcoholic fatty liver disease (NAFLD), is increasing annually. Bariatric surgery is indicated for the treatment of obesity if conservative treatment fails. While various liver fibrosis scores have been proposed for assessing liver function, they are typically used prior to bariatric surgery. This study aimed to determine whether fibrosis scores calculated from non-invasive parameters are effective in monitoring liver function after bariatric surgery.

Methods

This study analyzed data from 151 patients who underwent sleeve gastrectomy (SG) and were followed up at 3, 6, 9, 12, 24, and 36 months postoperatively. From the routinely collected parameters, liver fibrosis scores (APRI, Fib-4, BARD, Forns index [FORNS], Lok score [LOK], and NAFLD scores) were calculated retrospectively and compared to diabetes status % excess weight loss (%EWL) and % total weight loss (%TWL) over a 3-year follow-up period.

Results

After SG, APRI, FORNS, and NAFLD scores showed significant improvements, whereas Fib-4, BARD, and LOK scores did not improve. Similarly, body mass index, %EWL, %TWL, and diabetes status also improved significantly. Throughout the 3-year follow-up period, only the APRI and NAFLD scores showed significant improvement.

Conclusion

Only APRI and NAFLD scores changed significantly after SG. Thus, these two scores may be used to reflect and monitor liver function in patients who have undergone SG.

bariatric surgery

liver fibrosis score

NAFLD

obesity

sleeve gastrectomy

Along with the steadily increasing prevalence of obesity, body mass index (BMI) and the prevalence of other obesity-related comorbidities, such as non-alcoholic fatty liver disease (NAFLD), non-alcoholic steatohepatitis (NASH), liver cirrhosis, and cholelithiasis, have also increased [1, 2]. Currently, the worldwide prevalence of NAFLD is 25% [3]. Metabolic syndrome—a cluster of conditions that include arterial hypertension, dyslipidemia, peripheral insulin resistance, pre-diabetes, type 2 diabetes mellitus, fatty liver disease, and psychological dysfunction—is a comorbidity of obesity [4–7]. For sustained reduction of body mass, bariatric surgery is indicated when conservative treatment of obesity has failed [8]. Of patients undergoing bariatric surgery, 95% have pre-existing NAFLD [9]. In addition to Roux-en-Y gastric bypass (RYGB) surgery, sleeve gastrectomy (SG) is the most frequently performed type of bariatric surgery [10, 11].

In addition to biopsy, noninvasive methods such as serum-based fibrosis scores or FibroScan may be used to monitor liver disease [12]. Thus, this study aimed to investigate whether fibrosis scores could suitably reflect an improved condition of the liver parenchyma following SG.

Study design

This study was based on anonymized data obtained from patients who underwent SG at the University Hospital of Friedrich Schiller University between 2010 and 2022 and who were followed up for 36 months. During follow-up visits, routine laboratory parameters were measured from blood samples at 3, 6, 9, 12, 240, and 36 months postoperatively and were used to calculate the fibrosis scores. Diabetes status was determined on the basis of HbA1c levels.

We compared pre- and post-operative liver fibrosis scores (aspartate aminotransferase-to-platelet ratio [APRI] [13], Fibrosis-4 [Fib-4] [14], BARD [15], Forns index [FORNS] [16], Lok score [LOK] [17], and NAFLD fibrosis score [18] values) to evaluate whether these scores could be used to indicate changes in liver status after SG.

All procedures were performed in accordance with the ethical standards of the local ethics committee that approved this study. The requirement for obtaining patient consent for data use was waived owing to the retrospective nature of the study.

Statistical analysis

Statistical analyses were performed using Microsoft Excel (Microsoft Corp., Redmond, WA, USA) and IBM SPSS v.25 (IBM SPSS Inc., Armonk, NY, USA). P-values for fibrosis scores, % excess weight loss (%EWL), % total weight loss (%TWL), BMI, and diabetes status were calculated using Freidman’s two-way analysis of variance by rank for related samples. Hypotheses resulting in a p-value below 0.05 were considered statistically significant.

Patient characteristics

Of 151 patients included in the study (97 females), 32 had preoperative diabetes mellitus. A total of 142 patients were classified as having grade 3 obesity and 8 as having grade 2 obesity (Table 1).

Table 1

Patient characteristics
Females, N = 151	97 (64.2)
Negative diabetes status, N = 151	32 (21.19)
Obesity Grade, N = 150	Obesity Grade 1	0.00 (0.00)
	Obesity Grade 2	8.00 (5.30)
	Obesity Grade 3	142.00 (94.70)
Age (Years), N = 150	51.00 [42.0; 56.25]
Height (cm), N = 150	169.00 [162.75; 176.50]
Body mass (kg), N = 150	137.55 [123.00; 160.40]
BMI (kg/m²), N = 150	49 [44; 54]
Descriptive data are provided, presented as median [interquartile range] or N (%).
BMI, body mass index

Changes in liver fibrosis scores, BMI, %TWL, and %EWL over the total follow-up period

Changes over the total follow-up period are shown in Table 2. Over 36 months after SG, patients’ BMI, diabetes status, APRI, and NAFLD scores decreased significantly (p < 0.001). The Fib-4 (p = 0.407) and LOK (p = 0.782) scores did not significantly change. With changes in BMI, the %TWL, and %EWL increased significantly (p < 0.001). The BARD score increased significantly (p < 0.001).

Table 2: Changes in scores, BMI, %EWL, %TWL and diabetes status during the course of follow-up

Pre-OP

3 M

6 M

9 M

12 M

24 M

36 M

P-Value

Until 12 M follow-up^a

P-Value

Annual follow-up^b

P-Value

Full follow-up period^c

APRI

0.30

[0.20; 0.40]

0.30

[0.20; 0.40]

0.20

[0.20; 0.30]

0.20

[0.20; 0.30]

0.20

[0.20; 0.30]

0.20

[0.20; 0.30]

0.20

[0.20; 0.30]

<0.001

Fib-4

0.91

[0.65; 1.18]

0.99

[0.72; 1.35]

1.02

[0.72; 1.34]

1.05

[0.78; 1.42]

0.98

[0.73; 1.32]

1.02

[0.77; 1.39]

1.12

[0.75; 1.50]

<0.001

0.129

BARD

2.00

[2.00; 3.00]

4.00

[2.00; 4.00]

4.00

[3.00; 4.00]

4.00

[3.00; 4.00]

4.00

[3.00; 4.00]

3.00

[3.00; 4.00]

3.00

[3.00; 4.00]

<0.001

FORNS

5.82

[4.76; 6.47]

5.33

[4.38; 6.25]

5.27

[4.45; 5.92]

5.49

[4.50; 6.13]

5.31

[4.29; 6.09]

5.50

[4.62; 6.03]

5.21

[4.56; 6.05]

<0.001

0.287

0.407

LOK

-1.61

[-2.14; -1.02]

-0.57

[1.85; 0.49]

-0.55

[-1.25; -0.02]

-0.59

[-0.97; 0.10]

-0.36

[-0.83; 0.31]

-0.69

[-1.28; -0.16]

-0.81

[-1.3; 0.22]

0.592

0.020

0.782

NAFLD

0.63

[-0.24; 1.53]

0.08

[-0.67; 0.97]

-0.05

[-0.95; 0.72]

0.09

[-1.28; 0.72]

-0.19

[-1.33; 0.58]

-0.26

[-1.43; 0.3]

-0.73

[-1.62; 0.57]

<0.001

BMI

49.00

[44.00; 54.00]

41.00

[36.00; 46.00]

36.00

[32.00; 41.00]

34.00

[30.00; 39.50]

33.00

[29.00; 38.00]

32.00

[28.25; 37.75]

33.00

[29.00; 38.00]

<0.001

%EWL

27.3

[19.88; 35.55]

43.30

[32.00; 52.30]

49.70

[39.30; 61.80]

54.80

[43.05; 64.95]

56.20

[44.10; 70.90]

52.20

[43.18; 66.35]

<0.001

0.004

<0.001

%TWL

31,95

[21,75; 39,98]

38,5

[29,60; 46,55]

40,5

[32,90; 48,50]

44,95

[34,80; 50,68]

46,55

[38,05; 51,60]

43,8

[36,45; 50,60]

<0.001

Negative diabetes status

29.00

(19.60)

28.00

(19.30)

30.00

(20.70)

31.00

(21.50)

34.00

(23.80)

36.00

(27.4)

45.00

(49.50)

0.14

<0.001

Descriptive data are presented, presented as median [interquartile range] or N (%). The P-values for the evaluation of APRI, Fib-4, BARD, FORNS, LOK, NAFLD, BMI, %EWL, %TWL and diabetes status were determined using Friedman's related-samples two-way analysis of variance by ranks.

Pre-OP, preoperative; M, month; APRI, AST-to-platelet ratio index; Fib-4, Fibrosis-4; FORNS, Forns index; LOK, Lok score; NAFLD, non-alcoholic liver disease fibrosis score; BMI, body mass index; %EWL, percentage excess weight loss; %TWL, percentage total weight loss

^a P-values for comparison of data over the first year of follow-up (Pre-OP, 3 M, 6 M, 9 M, and 12 M)

^b P-values for comparison of data over the annual follow-up period (Pre-OP, 12 M, 24 M, and 36 M)

^c P-values for comparison of data over the full follow-up period (Pre-OP, 3 M, 6 M, 9 M, 12 M, 24 M, 36 M)

The recorded data were interpreted as follows: APRI scores < 0.5, BARD scores < 2, and a FORNS < 4.21 preclude significant fibrosis [16, 19]. Fib-4 scores ≤ 1.30 (< 2.0 from the age of 65 years) reflect a low risk of advanced liver fibrosis [20]. LOK scores < 0.2 suggest a low likelihood of cirrhosis [18]. NAFLD scores between − 1.455 and 0.676 allow neither exclusion nor diagnosis of fibrosis [21].

Changes in liver fibrosis scores, BMI, %TWL, and %EWL over the first year of follow-up

Changes over the first year of follow-up are shown in Table 2. The BMI, APRI, FORNS, and NAFLD scores decreased significantly (p < 0.001) within the first 12 months after surgery. The Fib-4, BARD score, %TWL, and %EWL were significantly increased (p < 0.001). The %EWL in the first year was 54.80%. The LOK score (p = 0.592) and diabetes status did not change significantly over the first year (p = 0.14).

Scores, BMI, %TWL, and %EWL over the annual follow-up visits

Changes over the annual follow-up visits are shown in Table 2. The BMI, APRI, and NAFLD scores decreased significantly (p < 0.001). The Fib-4 (p < 0.001), BARD (p < 0.001), and LOK scores (p = 0.020) increased, as did the %EWL (p = 0.004), %TWL (p < 0.001), and diabetes status (p < 0.001). The FORNS did not change significantly from year to year (P = 0.287).

In this study, we investigated whether fibrosis scores calculated from non-invasive parameters are effective in monitoring liver function after bariatric surgery. We found that the APRI, FORNS, and NAFLD scores showed significant improvements in the first year, whereas the Fib-4, BARD, and LOK scores did not improve significantly after bariatric surgery. BMI, %TWL, and %EWL, as well as diabetes status also improved significantly. Over the full 3-year follow-up period, only the APRI and NAFLD scores showed significant improvement.

Changes in BMI, %TWL, and %EWL

Previous studies have confirmed a significant reduction in BMI, and accordingly a significant increase in %TWL, and %EWL, as well as rapid weight loss shortly after bariatric surgery and further slower weight loss over time. Rapid weight loss is caused by the stimulation of L-cells, which results in an increase in peptide YY (PYY), glucagon-like peptide 1 (GLP-1), and oxyntomodulin levels, which leads to decreased food intake. The synergistic effect of elevated PYY and GLP-1 may act in combination with a reduction in glucose-dependent insulinotropic peptide and ghrelin, as well as the trophic function of GLP-2, leading to a negative energy balance and subsequent weight loss [22].

Changes in diabetes status

At the beginning of the study, all the patients with diabetes mellitus were effectively managed with medication. After 3 years, 49.50% of the cohort had a negative diabetes status, as compared with only 19.60% preoperatively. Several studies have reported improved blood glucose levels after bariatric surgery [23]. Bariatric surgery results in weight loss, accompanied by improved blood sugar levels, blood pressure, and lipid parameters [23]. However, in 30–50% of cases, type 2 diabetes can develop 3–15 years after surgery despite initial remission [24]. Nevertheless, this was not observed in the present study.

Changes in APRI score

The APRI score decreased between the third and sixth months of follow-up, which correlated with the most significant changes in body weight. A cut-off value of < 0.5 in the APRI score ruled out significant fibrosis over the entire follow-up period. The correlation between AST level, platelet count, and calculated APRI score was only marginally related to a reduction in body weight in the present study. An increase in the APRI score can reflect an increase in platelet count and/or a relative decrease in AST levels. A separate study confirmed a 22% reduction in the platelet count within the first year of follow-up after bariatric surgery, whereas alanine transaminase (ALT) levels decreased by 45% within the same period [25]. Another study reported simultaneous decreases in AST and ALT levels after bariatric surgery [26].

Changes in the Fib-4 score

A statistically significant change in the Fib-4 score (p < 0.001) was observed only during the first year of follow-up (Table 3). The score increased slightly to levels indicating a lower risk of advanced liver fibrosis (≤ 1.30, or < 2.0 from the age of 65 years). These scores increased with age and/or AST and/or decreased platelet count and ALT levels, due to the formula used to calculate this score. Other studies have confirmed a decrease in platelet count during follow-up after bariatric surgery [25]. In the present study, while both AST and ALT levels decreased (by 47.7% and 57.6%, respectively), AST levels decreased less steeply so that AST levels were increased relative to ALT levels after surgery [26]. The relationship between these liver enzymes is used only in the calculation of the Fib-4 score, but not in the calculation of the APRI score.

Changes in the BARD score

The BARD score increased significantly over time, providing evidence of patient liver health by considering the AST/ALT ratio, BMI, and diabetes status. However, in a typical NAFLD cohort, a large proportion of patients has a score of ≥ 2 due to obesity and diabetes, thus limiting the value of this score in clinical practice [21]. As diabetes mellitus and BMI decreased after bariatric surgery, the increase in the score was related to the ratio of AST and ALT liver enzyme levels. An AST/ALT ratio of ≥ 0.8 accounts for 2 points in the BARD score equation. One study found a 32.26% reduction in AST concentration within 6 months and a 48.28% reduction in ALT within the same period after SG [27]. The resulting relative increase in AST concentration explains the increase in BARD scores in our study.

Changes in the FORNS

The FORNS decreased significantly only in the first year. All values were within the cutoff limits, indicating a low risk of fibrosis with an uncertain prognosis. According to the formula for calculating the FORNS, decreasing values can be explained by an increase in platelet count and/or cholesterol levels and/or a significant decrease in age and GGT levels. A previous study showed that platelet count decreased after bariatric surgery. Therefore, the change in the scores in our study must be explained by a decrease in GGT and/or an increase in cholesterol levels. This hypothesis is supported by another study that showed a 55–57% reduction in GGT levels after bariatric surgery [25]. A study that examined cholesterol levels over 5 years after SG found no significant reduction in LDL levels [28].

Change in the LOK

A significant increase in the LOK was evident only during the first year. The LOK scores obtained were associated with a low risk of fibrosis throughout the follow-up period. According to the formula for calculating this score, an increase in score values requires an increase in AST and/or international normalized ratio (INR), and/or a decrease in platelet count and/or ALT levels. As discussed above, the AST/ALT ratio increases and the platelet count decreases after bariatric surgery, given alleviation of the preoperative low-grade inflammation caused by obesity. The low weighting factor (0.0089) for the platelet count in the formula may result in a misrepresentation of the score due to the low impact of the platelet count. In the LOK score calculation, the weight assigned to the INR is sizable (5.27), which would cause a more marked impact on the score; however, the INR changed only marginally during the follow-up period in our study.

Change in the NAFLD score

The NAFLD scores decreased significantly over time in this study. This may be attributable to the patients’ increased age and change in weight, diabetes status, and AST levels. Previous studies have demonstrated an increase in the AST/ALT ratio and a decrease in platelet counts after bariatric surgery, resulting in an increase in the NAFLD fibrosis score. Another study confirmed the assumption that albumin concentration increases postoperatively [29]. The decrease in NAFLD scores in our study was due to a significant increase in diabetes-negative status, %EWL, %TWL, and a decrease in BMI. Another study confirmed that this score is most suitable for ruling out fibrosis postoperatively [30].

Change in other parameters by comparison

Although some of the scores mentioned above increased significantly during the follow-up period, this did not indicate deterioration of the liver condition. However, some of the scores are not suitable for monitoring liver function after bariatric surgery. A study using the LiMAx test to assess the functional capacity of the liver after bariatric surgery showed a significant increase in liver capacity postoperatively [31]. Another study that used percutaneous true-cut biopsies to evaluate the recovery of the steatosis/fibrosis of the liver also showed a significant improvement in the liver parenchyma condition postoperatively [32].

Limitations

This retrospective cohort study has some limitations, including incomplete data sets, which can make the analysis more challenging, and inadequate control of confounding factors. Additionally, selection bias may be present owing to the retrospective nature of the study. Further, although associations could be demonstrated, no clear cause-effect relationships could be established. Finally, owing to the retrospective nature of the study, it would not be ethical to compare the results of this study to the biopsy results of these patients. These factors limit the interpretation and generalizability of the results.

Within 12 months after SG, the Fib-4 and BARD scores deteriorated, the LOK score remained stable, and the FORNS values changed only slightly. Therefore, these scores are not suitable for post-bariatric monitoring of liver function. In addition to a significant reduction in the number of patients with diabetes, significant improvements in the APRI and NAFLD scores were demonstrated, implying that these two scores are suitable for monitoring liver function in patients who have undergone SG.

Conflicts of interest:

The authors declare that they have no conflict of interest.

Ethical approval:

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent:

For this type of study, formal consent is not required.

Funding:

None

Author Contribution

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by H.A., R.F., S.U., D.F., A.D.A., K.H., S.L., B.J., and A.M.. The first draft of the manuscript was written by H.A., and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgements:

None

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No competing interests reported.

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Comparison of different liver fibrosis scores following sleeve gastrectomy

Status:

Version 1

Abstract

Purpose

Methods

Results

Conclusion

Introduction

Material and Methods

Study design

Statistical analysis

Results

Patient characteristics

Changes in liver fibrosis scores, BMI, %TWL, and %EWL over the total follow-up period

Changes in liver fibrosis scores, BMI, %TWL, and %EWL over the first year of follow-up

Scores, BMI, %TWL, and %EWL over the annual follow-up visits

Discussion

Changes in BMI, %TWL, and %EWL

Changes in diabetes status

Changes in APRI score

Changes in the Fib-4 score

Changes in the BARD score

Changes in the FORNS

Change in the LOK

Change in the NAFLD score

Change in other parameters by comparison

Limitations

Conclusion

Declarations

Conflicts of interest:

Funding:

Author Contribution

Acknowledgements:

References

Additional Declarations

Status:

Version 1