Laparoscopic sleeve gastrectomy and laparoscopic sleeve gastrectomy with jejunojejunal bypass surgery in patients with obesity: a correlation analysis between body weight, inflammation, glucose metabolism, and sex

doi:10.21203/rs.3.rs-4564463/v1

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Research Article

Laparoscopic sleeve gastrectomy and laparoscopic sleeve gastrectomy with jejunojejunal bypass surgery in patients with obesity: a correlation analysis between body weight, inflammation, glucose metabolism, and sex

https://doi.org/10.21203/rs.3.rs-4564463/v1

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Background

Bariatric surgery, which can be performed via laparoscopic sleeve gastrectomy (LSG) or laparoscopic sleeve gastrectomy with jejunojejunal bypass (LSG + JJB), is a promising treatment for patients with obesity. However, the influencing factors in LSG and LSG + JJB surgery remain unclear.

Methods

This study included 60 patients with obesity, divided randomly into LSG group and LSG + JJB group based on the surgical type. The weight loss and diabetes remission were compared at 3 months after surgery. Blood glucose metabolism indices including fasting blood glucose (FBG), homeostatic model assessment of insulin resistance (HOMA-IR), glycated hemoglobin (HbA1c), as well as inflammatory factors were measured.

Results

We found that the hypoglycemic effect in the LSG + JJB group was significantly superior to that in the LSG group. In the LSG + JJB group, weight was associated with inflammatory factors, including IL-8 (r = 0.431, P = 0.017), TNF-α (r = 0.381, P = 0.038), IL-10 (r = 0.410, P = 0.024), and glucose metabolism indicators FBG (r = 0.360, P = 0.050) and HOMA-IR (r = 0.374, P = 0.042). In addition, we observed a correlation between inflammatory factors and glucose metabolism in this group. The operative effect was also found to correlate with sex; males showed a more optimal effect in decreasing glucose metabolism and reducing inflammatory factors than females who underwent LSG + JJB surgery.

Conclusion

LSG + JJB surgery was related to inflammation, glucose metabolism, and sex, providing valuable insights for effective treatment approaches targeting individuals with obesity.

Obesity

Laparoscopic sleeve gastrectomy

Laparoscopic sleeve gastrectomy with jejunojejunal bypass

Inflammatory factors

Glucose metabolism

Sex differences

Obesity is a chronic metabolic disorder characterized by an excessive or abnormal accumulation of body fat; a body mass index (BMI) > 28 kg/m² is considered indicative of obesity. Due to the mounting pressures of modern life and changes in dietary patterns, the prevalence of obesity has steadily increased over the years. In China, 6.8% of preschoolers under 6 years old are classified as overweight, with 3.6% falling into the obese category. Furthermore, approximately 34.3% adults are overweight, with 16.4% classified as obese. Obesity results in disruption of the normal metabolic processes involving sugar, fat, and uric acid within the body, significantly elevating the risk for various diseases such as diabetes, hypertension, coronary heart disease, and stroke(Cleven et al., 2020).Type 2 diabetes poses a grave threat to human health by inducing disturbances in lipid metabolism in addition to impaired sugar tolerance and glucose toxicity(Berberich & Hegele, 2022; Pedro et al., 2020). Compared to conventional treatments, such as lifestyle modifications and medications, bariatric metabolic surgery has emerged as a swifter, more efficacious, and enduring solution for obesity or its related complications. Bariatric metabolic surgery has made rapid advancements in recent years(Affinati et al., 2019; Perdomo et al., 2023). At present, laparoscopic sleeve gastrectomy (LSG) and laparoscopic sleeve gastrectomy with jejunojejunal bypass (LSG + JJB) are widely employed techniques in the field of bariatric surgery.

LSG is primarily utilized in early surgical interventions for severely patients with obesity; it is a relatively simple procedure with few complications. A substantial body of clinical evidence has indicated that LSG yields favorable outcomes in terms of weight loss and metabolic improvement(Balasubaramaniam & Pouwels, 2023; Cosentino et al., 2021; De Luca et al., 2023). On the other hand, LSG + JJB involves preserving the excised portion of the greater curvature while incorporating a 200 cm long jejunum into the procedure based on the principles of LSG. This approach places a particular emphasis on preventing gastrointestinal ulcers during postoperative vagal anastomosis(Alamo et al., 2012). However, it remains unclear whether LSG or LSG + JJB results in superior effects in terms of weight reduction and blood glucose control. Furthermore, our understanding regarding the hypoglycemic effects and influencing factors associated with these two techniques is limited.

In this study, we observed a reduction in body weight and a decrease in inflammatory factors in both the LSG and LSG + JJB groups, while the hypoglycemic effect in the LSG + JJB group was significantly superior to that in the LSG group. Additionally, a correlation among body weight, inflammatory factors, and glucose metabolism was observed in the LSG + JJB group. Compared with females who underwent LSG + JJB surgery, males showed the most optimal effect in decreasing glucose metabolism and reducing inflammatory factors. Overall, this study found that LSG + JJB surgery resulted in a better hypoglycemic effect, especially in males. These findings provide valuable insights for effective treatment approaches targeting individuals with obesity in clinical practice.

Clinical data

Selection criteria

In total, 30 patients who underwent LSG surgery at our hospital between December 2020 and February 2023 were selected from the Greater China Metabolic and Bariatric Surgery Database (ClinicalTrials.gov Identifier: NCT03800160). Additionally, 30 patients who underwent LSG+JJB surgery during the same period were randomly chosen. Subsequently, a randomized controlled study was conducted to compare the surgical outcomes and postoperative follow-up data between these two groups. All patients met the surgical indications outlined in the "Chinese guidelines for surgical treatment of obesity and type 2 diabetes (2020)".

Exclusion criteria

Patients with a duration of diabetes exceeding 15 years; fasting serum C peptide levels below one-third of the normal value; presence of complicated malignant tumors; individuals diagnosed with insulin autoantibodies-positive diabetes; and patients unable to undergo surgery due to poor cardiac, liver, or kidney function.

Surgical methods

The key procedures involved in the LSG surgery were as follows. In the stomach, the fundus of stomach and greater curvature were completely dissociated. A 36 Fr gastric calibration tube was utilized for intragastric support, and the cutting starting point of the greater curvature located 3–6 cm from the pylorus. The incision extended from the left side to a position where the fundus was 1 cm away from the His angle, ensuring complete resection while preserving both the fundus and greater curvature, in addition to maintaining integrity at the cardia. In cases were a routine intraoperative exploration revealed a hiatal hernia, immediate repair was performed. To reinforce stability, suturing of gastric remnant was performed. The LSG method involved using a 60 mm linear stapler to cut from the gastric sinus to the His angle, with continuous suture reinforcement guided by a supporting gastric tube measuring 36 Fr in diameter.

The key aspects of the LSG+JJB procedure were as follows. JJB was performed after LSG. The jejunum was transected at 30 cm from the Treitz ligament. A 60 mm linear stapler was utilized for jejunojejunostomy, positioned 200 cm below the disconnection site. The common opening was securely closed using the laparoscopic linear stapler, while suturing was used to address any mesenteric perforations.

Clinical indices and follow-up

Follow surgery, patients were routinely administered a variety of vitamin and trace element preparations. The patients were followed up 3 months after surgery to record and compare body weight, blood glucose metabolism, and inflammatory factors between the two groups. Weight-related indices included weight 3 months after surgery, BMI, absolute weight loss, percentage of total weight loss (%TWL, %TWL = [(baseline weight – follow-up weight) / (baseline weight)] × 100). The blood glucose metabolism indices included fasting blood glucose (FBG), insulin resistance index (HOMA-IR, HOMA-IR = [FBG × fasting insulin] / 22.5), and glycated hemoglobin (HbA1c).

Statistical methods

SPSS 26.0 was used for statistical analyses. The measurement data conforming to the normal distribution was expressed as the mean ± standard deviation, which was analyzed by the independent sample t-test. Non-normality distributed data was expressed as quartiles, and was analyzed using the rank sum test. The sample rate of the enumeration data was analyzed by the χ² test. P < 0.05 was considered statistically significant.

Baseline characteristics of the patients

In total, 60 patients with obesity were included in the analysis, which were divided into two groups according to the type of surgery. The baseline characteristics of the two groups are shown in Table 1. The LSG group (n = 30) consisted of 16 males and 14 females, which was equal to that of the LSG + JJB group. Furthermore, the average age (P = 0.737), weight (P = 0.275), and BMI (P = 0.142) of patients were similar between groups. The type 2 diabetes-related indicators were higher than normal in both groups, with a mean FBG of 10.58 ± 1.35 mmol/L and 10.19 ± 1.21 mmol/L (P = 0.247), the mean HOMA-IR of 5.44 ± 0.26 and 5.42 ± 0.24 (P = 0.837), and the mean HbA1c of 7.42 ± 0.95 and 7.38 ± 0.64 (P = 0.850), respectively. Overall, there was no statistical difference in basic data between the two groups.

Table 1

Baseline characteristics of patients
Variable	LSG group	LSG + JJB group	t/χ²	P value
Sex
Male	16 (53.33%)	16 (53.33%)	0
Female	14 (46.67%)	14 (46.67%)	0
Age(year)	32.1 ± 5.29	32.5 ± 6.23	-0.338	0.737
Weight(kg)	113.31 ± 8.16	115.37 ± 6.23	-1.103	0.275
BMI(kg/m²)	32.88 ± 2.21	33.6 ± 1.44	-0.149	0.142
Abdominal girth (cm)	116.65 ± 8.35	116.55 ± 4.43	0.058	0.954
Fasting blood glucose(mmol/L)	10.58 ± 1.35	10.19 ± 1.21	1.170	0.247
Insulin resistance index (HOMA-IR) Glycosylated hemoglobin	5.44 ± 0.26 7.42 ± 0.95	5.42 ± 0.24 7.38 ± 0.64	0.207 0.191	0.837 0.850

Postoperative body weight and blood glucose measurements

Table 2 shows data on the body weight at 3 months after the two surgical procedures. Both groups showed a significant decrease in body weight. When comparing the two groups, the BMI (P = 0.634) and weight loss percentage (P = 1.000) were similar; however, there were significant differences in body weight (P = 0.006), weight loss (P < 0.001), FBG (P < 0.001), HOMA-IR (P < 0.001), and HbA1c (P < 0.001) between the two groups. In the violin plot, the weight distribution of the LSG + JJB group was more concentrated, the maximum value was significantly lower, and the median was lower than that of LSG group (Figure S1). In summary, the LSG + JJB group showed more beneficial antidiabetic and weight-reducing effects.

Table 2

Postoperative indexes of different surgical procedures
Variable	LSG group	LSG + JJB group	t/χ²	P value
Weight(kg)	87.41 ± 8	83.09 ± 2.35	2.832	0.006
BMI(kg/m²)	30.22 ± 1.40	30.38 ± 1.17	-0.479	0.634
Weight loss(kg)	26.08 ± 5.19	21.88 ± 1.84	4.168	< 0.001
Weight loss percentage(%)	23 ± 4.23	19 ± 1.89	4.726	1.000
Fasting blood glucose(mmol/L)	6.19 ± 0.19	5.03 ± 1.12	5.608	< 0.001
Insulin resistance index (HOMA-IR)	4.23 ± 0.36	3.16 ± 1.11	5.027	< 0.001
Glycosylated hemoglobin	5.78 ± 0.18	4.76 ± 0.68	7.969	< 0.001

Effect of LSG and LSG + JJB on inflammatory factors

To investigate the potential anti-inflammatory effects of weight loss surgery, the inflammatory factors were analyzed. The original inflammatory factors of IL-8, TNF-α, IL-10 and IL-1β were produced abundantly by patients. However, their expression levels were decreased after operation, and there was a significant difference between preoperative and postoperative process in both LSG or LSG + JJB group (Table 3). This implies that the anti-inflammatory effects of LSG and LSG + JJB surgery were quite similar.

Table 3

Changes of inflammatory factors after operation
Treatment	Variable (pg/mL)	Preoperative	Postoperative	t/χ²	P value
LSG group	IL-8	559.50 ± 27.50	140.10 ± 60.95	34.353	< 0.001
	TNF-α	32.04 ± 2.30	15.90 ± 2.56	25.720	< 0.001
	IL-10	24.45 ± 2.60	6.15 ± 0.73	37.075	< 0.001
	IL-1β	30.79 ± 2.24	13.56 ± 2.14	30.446	< 0.001
LSG + JJB group	IL-8	551.54 ± 24.21	98.46 ± 48.95	45.438	< 0.001
	TNF-α	30.64 ± 1.50	8.66 ± 6.38	18.382	< 0.001
	IL-10	21.10 ± 1.67	5.89 ± 2.29	29.422	< 0.001
	IL-1β	29.71 ± 1.37	10.55 ± 6.68	15.385	< 0.001

Correlation between body weight and glucose metabolism index and inflammatory factors

In the LSG and LSG + JJB groups, postoperative inflammatory factors and body weight were both considerably lower postoperatively compared to preoperatively. We assessed the correlation between body weight and inflammatory factors in the two groups (Table S1). As shown in Fig. 1, body weight was positively correlated with the levels of IL-8 (r = 0.431, P = 0.017), TNF-α (r = 0.381, P = 0.038), IL-10 (r = 0.410, P = 0.024), FBG (r = 0.360, P = 0.050), and HOMA-IR (r = 0.374, P = 0.042) in the LSG + JJB group. Furthermore, the LSG + JJB group showed a stronger statistically significant association between postoperative body weight, glucose metabolism indicators, and inflammatory markers compared to the LSG group (Fig. 1).

Correlation between inflammatory factors and glucose metabolism indices

Since the postoperative body weight was found to show a stronger correlation with the blood glucose level and inflammatory factors in the LSG + JJB group, we next aimed to determine whether blood glucose levels and inflammatory factors were related. The level of IL-8 in LSG + JJB group was positively correlated with the FBG, HOMA-IR, and HbA1c (r = 0.855, P < 0.001; r = 0.868, P < 0.001; r = 0.856, P < 0.001). The TNF-α level was positively correlated with FBG, HOMA-IR, and HbA1c levels (r = 0.935, P < 0.001; r = 0.932, P < 0.001; r = 0.922; P < 0.001, respectively). In addition, IL-10 and IL-1β levels were positively correlated with the FBG, HOMA-IR, and HbA1c. The correlation between glucose metabolism indexes and inflammatory factors in the LSG group was poor, and only the correlation between GH and the inflammatory factor IL-1β was significant in the LSG group (r = 0.383, P = 0.037) (Table S2). Figure 2 displayed the correlations and significant differences with a heat map. Overall, the relationship between inflammatory factors and glucose metabolism was statistically significant and stronger in the LSG + JJB group (P < 0.001).

Sex differences in the hypoglycemic and anti-inflammatory effects

We previously observed a correlation between weight, inflammatory factors, and glucose metabolism in the LSG + JJB group. We next assessed whether these effects vary depending on sex. Interestingly, we observed sex-related differences in the postoperative anti-inflammatory effects between the two surgical procedures (Table S3). In males, the LSG + JJB group showed a better anti-inflammatory effect, and the levels of IL-8, TNF-α, IL-10, and IL-β were significantly decreased compared to the LSG group (P < 0.001). In females, the expression level of IL-8 (P = 0.058) and TNF-α (P = 0.106) were similar in the LSG and LSG + JJB group, while IL-10 (7.91 ± 1.68 pg/mL vs 6.10 ± 0.76 pg/mL, P = 0.001) and IL-1β (16.66 ± 3.82 pg/mL vs 13.30 ± 2.27 pg/mL, P = 0.009) showed a notable decline in the LSG group, indicating that LSG had a better effect on the reduction of IL-10 and IL-1β levels.

Figure 3A showed the sex differences in IL-8. Males in the LSG + JJB group had the lowest data dispersion and the most concentrated frequency distribution among the four groups, thus showing the greatest impact on decreasing IL-8, as indicated by the lowest median and smallest quartile range. In Fig. 3B, similarly, males in the LSG + JJB group showed a significant effect in reducing inflammatory factors TNF-α, IL-10, and IL-1β. In summary, we observed sex-related differences in the reduction in inflammatory factors levels between the LSG and LSG + JJB group, with males receiving LSG + JJB surgery showing the best anti-inflammatory effect.

Sex differences in glucose metabolism

We next assessed whether sex-related differences occurred in glucose metabolism. As shown in Table S4, males in the LSG + JJB group showed a better effect on reducing blood glucose levels, with a significant difference observed between the LSG and LSG + JJB groups (P < 0.001). Females in the LSG surgery group showed a better effect on reducing the HOMA-IR (4.07 ± 0.34 vs 4.31 ± 0.23, P = 0.038), while the LSG + JJB groups showed a better effect on the reduction of HbA1c (5.46 ± 0.18% vs 5.77 ± 0.19%, P < 0.001). In Fig. 4, males in the LSG + JJB group showed the best effect in regulating glucose metabolism. The frequency distribution of males in the LSG + JJB group was the most concentrated and the median was the lowest among the three glucose metabolism indices (FBG, HOMA-IR, and HbA1c), indicating a tight correlation between sex and the hypoglycemic effect.

With the improvement in living standards, the incidence of diseases has been increasing year by year, including obesity, type 2 diabetes, and cardiovascular disease, which poses a serious threat to human health(Aminian et al., 2018). There is a close relationship between obesity and glucose metabolism(Zeng et al., 2021). When hyperglycemia occurs, the body will compensate by the secretion of more insulin, which can result in insulin resistance and hyperinsulinemia. Bariatric and metabolic surgery is the most effective method for the treatment of obesity. The most common procedures are LSG and LSG + JJB. Although bariatric surgery can be used to treat type 2 diabetes, it is not clear what factors affect the reduction of postoperative glucose metabolism indicators, and what indicators could reflect the severity of type 2 diabetes.

Obesity is closely related to glucose metabolism and diabetes. Bariatric metabolic surgery can reduce blood glucose to treat type 2 diabetes; LSG + JJB surgery has a better hypoglycemic effect than LSG surgery, which can be attributed to the following reasons. Firstly, the K cells in the exclusion zone do not receive food stimulation, and the secretion of inflammatory factors decreased; therefore, glucose metabolism was improved(Lopez-Nava et al., 2022). Secondly, under the stimulation of food, the secretion of endocrine regulatory peptide and GP1 was increased in the distal jejunum and ileum. These cytokines stimulate proliferation and reconstruction of islet function(Cottam et al., 2018). Thirdly, laparoscopic bariatric and metabolic surgery can change the volume and pathway of the digestive tract, altering the food intake and absorption methods of patients to regulate the bile acid cycle and gastrointestinal hormones, thus regulating insulin sensitivity and maintaining a satisfying long-term weight loss effect(Rebibo et al., 2019; Soong et al., 2021).

Adipose tissue can secrete a variety of inflammatory factors, such as IL-8, IL-10, TNF-α, and IL-1β. The inflammatory response can promote the occurrence and development of obesity or diabetes, leading to abnormal glucose or lipid metabolism(Cimini et al., 2017; Peña et al., 2023). Excessive activation of the inflammatory response is an important pathological factor affecting insulin biological signal transduction, ultimately resulting in insulin resistance. IL-8, TNF-α, and IL-1β are pro-inflammatory cytokines, which affect insulin sensitivity through the biological activity of inflammatory mediators and inhibit the biological signal transduction of insulin-mediated biological effects, leading to the occurrence of insulin resistance. IL-10 is the most widely studied anti-inflammatory cytokine, which can inhibit the expression of other cytokines, such as TNF-α, IL-1β, and IL-8. Furthermore, the increased secretion of pro-inflammatory factors leads to the increased secretion of IL-10. Previous studies have confirmed that inflammatory factors are significantly reduced after bariatric and metabolic surgery(Wolf et al., 2019). We found that both LSG and LSG + JJB surgery resulted in favorable anti-inflammatory effects. The level of inflammatory factors was significantly decreased at 3 months after surgery; this was quicker than that observed in previous studies, which reported a significant effect at 6 months or even 1 year after surgery.

Patients with obesity are often accompanied by symptoms such as abnormal inflammatory factors and abnormal glucose metabolism. Therefore, in addition to postoperative body weight, bariatric surgery can also be used to regulate inflammatory factors and glucose metabolism. Our study showed that both surgical options have weight loss, hypoglycemic, and anti-inflammatory effects, which was consistent with most research results. In addition, the correlation analysis showed that the body weight was tightly corelated with inflammatory factors and glucose metabolism in the LSG + JJB group, and there was a positive correlation between inflammatory factors and glucose metabolism. Combined with the better hypoglycemic effect of LSG + JJB surgery, it could be concluded that LSG + JJB surgery has a more favorable anti-inflammatory effect.

In addition, we observed sex-related differences in the postoperative effects of the two surgical approaches. Among the four groups of male LSG, female LSG, male LSG + JJB, and female LSG + JJB, we found that the male LSG + JJB group had the best hypoglycemic and anti-inflammatory effects, which indicated that males may be more suitable for LSG + JJB bariatric surgery. This phenomenon could be explained as follows. Firstly, sex differences in adipose tissue can result in obese males being more prone to obesity-related complications, such as diabetes, hypertension, and dyslipidemia, which in turn leads to abnormalities in related inflammatory factors and glucose metabolism indicators. In addition, abdominal fat content in female patients was correlated with total cholesterol, triglycerides, high-density lipoprotein cholesterol (HDL), and low-density lipoprotein cholesterol while abdominal fat content in male patients was only correlated with the FBG and HDL In addition, males are more likely to return to normal glucose metabolism after losing the same amount of weight(Bouchi et al., 2017; Romano et al., 2021).

In summary, we found that both the LSG and LSG + JJB groups showed a satisfying effect regarding weight loss. The glucose metabolism level was significantly improved after LSG + JJB surgery, which was non-existent in the LSG group. In addition, there was a positive correlation among body weight, inflammatory factors, and glucose metabolism in the LSG + JJB group. The hypoglycemic and anti-inflammatory effects in males were better than in females receiving LSG + JJB surgery. This study demonstrated the influencing factors and sex-related differences in LSG + JJB surgery, providing valuable theoretical reference for the clinical treatment of obesity.

The effect of LSG + JJB surgery on body weight may be due to the inflammatory factors and glucose metabolism, and males receiving LSG + JJB surgery showed the best hypoglycemic and anti-inflammatory effects.

Ethics statement The studies involving human participants were reviewed and approved by the Ethics Committee of the First Hospital of Hebei Medical University (20220543). The patients/participants provided their written informed consent to participate in this study.

Informed Consent Informed consent was obtained from all individual participants included in the study.

Funding

This work was supported by the Science Research Project of Hebei Education Department [grant number QN2023257]; the Central Government Directs Local Science and Technology Development Fund Projects [grant number 236Z2804G]; the Hebei Normal University Doctoral (post) Research Start-up Fund [grant number L2023B24]; the Hebei Province Agricultural Scientific and Technological Achievements Transformation Fund Project [grant number 2024], and the Shijiazhuang Reward Special Fund [grant number 226790217H].

Author Contribution

Feng Feng and Yuqi Gao wrote the main manuscript text. Jiaqi Zhang and Guiqi Wang prepared figures and tables. Liping Peng and Yunjiang Liu directed the data analysis. All authors reviewed the manuscript.

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No competing interests reported.

Supplementaldata.docx
Figure S1. Changes of body weight in LSG and LSG+JJB surgery patients. means P <0.01，* means P <0.001. Table S1. Correlation between body weight and inflammatory factors and glucose metabolism Table S2. Correlation between inflammatory factors and glucose metabolism indexes Table S3. Comparison of inflammatory factors of the same gender Table S4. Comparison of glucose metabolism indexes of the same gender

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You are reading this latest preprint version

Laparoscopic sleeve gastrectomy and laparoscopic sleeve gastrectomy with jejunojejunal bypass surgery in patients with obesity: a correlation analysis between body weight, inflammation, glucose metabolism, and sex

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Abstract

Background

Methods

Results

Conclusion

Figures

Introduction

Materials and methods

Results

Baseline characteristics of the patients

Postoperative body weight and blood glucose measurements

Effect of LSG and LSG + JJB on inflammatory factors

Correlation between body weight and glucose metabolism index and inflammatory factors

Correlation between inflammatory factors and glucose metabolism indices

Sex differences in the hypoglycemic and anti-inflammatory effects

Sex differences in glucose metabolism

Discussion

Conclusion

Declarations

Author Contribution

References

Additional Declarations

Supplementary Files

Status:

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