Proximal Small Intestine Bypass Outperforms Roux-en-Y and Jejunoileal Bypass in Glucose Regulation in Streptozotocin‑Induced Diabetic Rats

doi:10.21203/rs.3.rs-4662428/v1

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Proximal Small Intestine Bypass Outperforms Roux-en-Y and Jejunoileal Bypass in Glucose Regulation in Streptozotocin‑Induced Diabetic Rats

https://doi.org/10.21203/rs.3.rs-4662428/v1

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Background This study aimed to compare the efficacy of modified proximal small intestine bypass (PSIB), Roux-en-Y gastric bypass (RYGB), and conventional jejunoileal bypass (JIB) in weight loss and glucose metabolism in streptozotocin (STZ)-induced diabetic rats.

Methods Rats with STZ-induced diabetes were randomly divided into PSIB, RYGB, JIB, and sham-operated (sham) groups. Body weight, food intake, fasting blood glucose (FBG) level, oral glucose tolerance test (OGTT), insulin tolerance test (ITT), liver function, and blood lipids were measured in rats in each group from 1 to 6 weeks after surgery.

Results No significant difference in the body weight of the rats in the PSIB and RYGB groups was observed postoperatively, whereas the body weight of the rats in the JIB group was significantly lower. The food intake of the rats in all three surgical groups was significantly less than that in the sham group. The PSIB group had a better glucose-lowering effect than the RYGB and JIB groups. Glucose tolerance improved significantly in all three surgical groups at 2 weeks postoperatively; with improved glucose tolerance in the PSIB group than in the RYGB and JIB groups. At postoperative week 2, insulin sensitivity improved only in the PSIB group; however, by postoperative week 6, insulin sensitivity improved significantly in both the PSIB and JIB groups.

Conclusion PSIB demonstrated excellent hypoglycemic effects and OGTT improvements in the early postoperative period, with better efficacy than that of RYGB and JIB. Compared with PSIB and RYGB, conventional JIB was more effective for weight loss.

Proximal small bowel bypass (approximately 60%) induces a better hypoglycemic efficacy than conventional jejunoileal bypass (approximately 85%).
Proximal small intestine bypass induces a better hypoglycemic efficacy than the Roux-en-Y gastric bypass, which is a more difficult operation.
Conventional jejunoileal bypass has a better effect on weight loss

Compared to conservative treatments, such as medications, metabolic surgery (MS) provides better control of blood glucose levels and diabetic complications[1–3]. Given its favorable outcomes in weight loss and hypoglycemic effects, jejunoileal bypass (JIB) was extensively used as a primary treatment for morbidly obese patients in the late 1960s and early 1970s[4]. However, owing to its adverse postoperative complications, JIB was discontinued. Now, Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG) are currently the most commonly employed procedures in MS[5]. However, owing to the complexity and difficulty of the procedure, there is a decreasing trend in the number of RYGB performed in clinical settings. Although there is an increasing trend for SG in clinical practice, its main role is weight loss, and its efficacy in treating diabetes is much lower than that of RYGB[6].

An extremely high percentage of absent intestines (up to 85%) could be attributed to the serious postoperative complications following conventional JIB. A modified approach to small intestinal bypass, which includes removing a smaller percentage of the proximal small intestines (approximately 60%), may contribute to effective glucose reduction and improve glucose tolerance[7]. To our knowledge, systematic comparisons of the weight loss and hypoglycemic effects of proximal small intestine bypass (PSIB), RYGB, and JIB in non-obese diabetic rats are lacking. In this study, PSIB, RYGB, and JIB surgeries were performed in a streptozotocin-induced diabetic (STZ-DM) rat model and compared their efficacies in terms of glucose reduction and weight loss. The primary objective was to investigate whether bypassing a smaller percentage of the small intestine could achieve weight loss and hypoglycemic effect comparable to that of RYGB or conventional JIB.

Animal Model

A total of 60 male 7-week-old Sprague-Dawley (SD) rats weighing 278.0 ± 16 g were purchased from Shanghai Slaughter Laboratory Animals Ltd (Shanghai, China). All animals were housed at 18°C-25°C under 12-h light and dark cycles and had ad libitum access to food and water. The rats were acclimatized in a single cage for one week after intraperitoneal injection of 60 mg/kg streptozotocin (STZ, Sigma, St. Louis, MO, USA). Seventy-two hours after the injection of STZ, rats with random blood glucose ≥ 16.7 mmol/L were selected for further study. Animal experiments were conducted in accordance with the standards of the Guidelines for Animal Experiments of Nanchang University and approved by the Animal Ethics Committee of Nanchang University.

PSIB (60% Bypass of the Small Intestine)

The rats were allowed to fast for 14 h before surgery. Following anesthesia (isoflurane, 4% for induction and 2% for maintenance), the abdomen of the rats was carefully shaved, and a 4-cm-long incision was made in the middle of the abdomen.

A side-to-side anastomosis was performed between the proximal jejunum and ileum at a distance of 10 cm distal to the ligament of Treitz and 30 cm proximal to the ileocecal valve as a point of reference (approximately 60% of the proximal small bowel was bypassed) to maintain parasympathetic activity in the small bowel and intestinal continuity (Fig. 1A). A single interrupted suture with a 6 − 0 nylon thread (Hangzhou Huawei Medical Treatment Articles Co., Ltd.) was placed. The length of the anastomosis was approximately 4 mm, and the intestinal collaterals were ligated with a No. 0 silk thread (ETHICON SA84G; Johnson & Johnson) near the small bowel anastomosis in the bypass. Finally, the abdomen was sutured using 3 − 0 silk thread.

JIB (with 85%- Bypassing of the Small Intestine)

For JIB, the jejunum was dissected 10 cm distal to the ligament of Treitz, and the proximal small bowel was anastomosed end-to-side with the ileum. Anastomosis was performed approximately 5 cm from the ileum (bypassing approximately 85% of the small bowel) (Fig. 1B). The blind ends of the jejunum and jejunum-ileum anastomosis were closed with a single interrupted layer of 6 − 0 nylon thread, and the anastomosis was approximately 4 mm long. Finally, the abdomen was sutured using a 3 − 0 silk thread.

RYGB

For RYGB, a gastric pouch of approximately 20% of the gastric volume was first created, and the pouch and distal stomach were closed using a single layer of interrupted 6 − 0 silk sutures. The jejunum was transected 10 cm distal to the ligament of Treitz, and the severed end of the jejunum was closed with a single layer of interrupted 6 − 0 silk suture, with the distal jejunum anastomosed side-to-side with the gastric pouch. At 15 cm from the gastro-jejunal anastomosis, the jejunal stump was anastomosed end-to-side with the distal jejunum (Fig. 1C). All anastomoses, measuring approximately 4 mm long, were closed with a 6 − 0 nylon thread in a single interrupted layer. Finally, the abdomen was sutured with a 3 − 0 silk thread.

Sham Operation

In the sham-operated group, the bowel was exposed, as previously described, without any other manipulation, and the duration of the operation was prolonged to produce an anesthetic stress comparable to that in the other two groups.

Body Weight and Food Intake

Body weight and average food intake were measured preoperatively and at 1, 2, 3, 4, 5, and 6 weeks postoperatively.

Fasting blood glucose (FBG)

Glucose levels in the tail vein blood of conscious rats were measured using an electronic glucometer (Accu-Chek Performa®, Roche Diagnostics, Switzerland). FBG levels were measured at 9 a.m. (after 14 h of fasting) preoperatively and at 1, 2, 3, 4, 5, and 6 weeks postoperatively.

Oral Glucose Tolerance Tests (OGTT) and Insulin Tolerance Tests (ITT)

OGTT and ITT was performed at postoperative weeks 2 and 6, respectively. The rats were fasted overnight, and blood glucose was measured before and 15, 30, 60, 90, 120, and 180 min after gavage of 20% glucose (1 g/kg glucose).

ITT was performed by measuring glucose levels before and 15, 30, 45, and 60 min after intraperitoneal injection of 0.5 IU/kg human insulin (Wanbang Biopharmaceuticals, Jiangsu, China).

Biochemical Test

At 6 weeks postoperatively, the rats were euthanized after a 10-h fast, and portal blood was collected and placed in biochemical test tubes containing coagulants. The blood was centrifuged at 3000 rpm for 15 min at 4°C, then immediately transferred to new tubes and stored at -80°C until further analysis. A fully automated biochemical analyzer was used to determine serum total cholesterol (TC), triglycerides (TG), high-density lipoprotein (HDL), low-density lipoprotein (LDL), alanine aminotransferase (ALT), aspartate aminotransferase (AST), total protein (TP), and albumin (ALB) levels. All the assays and analyses were performed in a biochemical laboratory.

Statistical Analysis

All data are expressed as the mean ± standard error of the mean. All statistical analyses were performed using GraphPad Prism version 9.5.0 (La Jolla, CA, USA), and p < 0.05 indicated statistical significance. The area under the curve (AUC) was calculated using the trapezoidal integration method. Two-way analysis of variance (ANOVA) was used to analyze changes in body weight, food intake, FBG, OGTT, and ITT. One-way ANOVA was used to analyze lipid levels and liver function.

Body Weight

From postoperative weeks 2 to 6, all rats showed a slight increase in body weight; however, the body weights of rats in the JIB group were lower than those in the sham group (P < 0.05), and the weight of the JIB group was lower than that of the RYGB and PSIB groups (Fig. 2A).

Global Food Intake

The global food intake of rats in all the surgical groups was significantly lower than that of rats in the sham group (all Ps < 0.01), and rats in the JIB group had a lower food intake than those in the RYGB group (Fig. 2B).

FBG

No difference in preoperative FBG levels was observed among the rats. However, the FBG levels of rats in the PSIB, RYGB, and JIB groups were significantly lower than those in the sham group (all Ps < 0.01) between weeks 1 and 6 postoperatively. Moreover, among the operated groups, FBG levels in the PSIB group were lower than those in the RYGB and JIB groups (both Ps < 0.01) (Fig. 3A).

OGTT and ITT

Significant improvement in OGTT was observed among the rats in the PSIB, RYGB, and JIB groups at postoperative week 2 (all Ps < 0.01). However, rats in the PSIB group exhibited better glucose tolerance than those in the RYGB and JIB groups (P < 0.05 and P < 0.01, respectively) (Fig. 3B and Fig. 3C). By postoperative week 6, rats in the surgical groups continued to exhibit improvement in OGTT (all Ps < 0.01); however, the difference was not statistically significant (Fig. 3D).

Figure 4 shows the ITT results of the rats in the surgical and sham-operated groups. At postoperative week 2, only rats in the PSIB group exhibited an improvement in insulin sensitivity (P < 0.05), with a statistically significant difference in insulin sensitivity between the PSIB group and the RYGB and JIB groups (both Ps < 0.05). At postoperative week 6, insulin sensitivity improved in both the PSIB and JIB groups (both Ps < 0.05), indicated by a faster rate of glycemic decline at 60 min of ITT.

Biochemical Testing

At 6 weeks postoperatively, only the TP level in the JIB group was lower than that in the sham group (P < 0.01), whereas the TB level in the PSIB group was higher than that in the JIB group (P < 0.01), with no statistically significant difference in the ALB level between the groups (Fig. 5A and Fig. 5B). In addition, only the ALT level in the PSIB group was lower than that in the sham group (P < 0.05), whereas no statistically significant difference in the AST levels was observed between the groups (Fig. 5C and Fig. 5D). In terms of lipid metabolism, the levels of TC, HDL, and HDL in the JIB group were lower than those in the sham group (all Ps < 0.05). Moreover, the levels of TC in the JIB group were lower than those in the PSIB and RYGB groups; and the levels of HDL and LDL in the JIB group were lower than those in the RYGB group (Fig. 6).

This is the first systematic study to compare the efficacy of PSIB with RYGB and JIB for weight loss and glucose reduction using the STZ-induced diabetic rat. Our findings elucidated that: (1) all three surgical groups had reduced blood glucose levels and improved glucose tolerance, and the efficacy of PSIB was better than that of RYGB and JIB; (2) although the rats in all three surgical groups exhibited reduced appetite, only JIB reduced body weight in STZ-DM rats; and (3) within a short span, partial hepatic function was improved by PSIB but impaired by JIB.

Our findings demonstrated the superior efficacy of PSIB over JIB in improving glucose metabolism. Classical JIB requires transection of the jejunum and end-to-end anastomosis of the jejunum to the distal ileum, which separates the jejunal branch from the autologous pacemaker and disrupts the electrophysiology of the small bowel, producing an ectopic pacemaker[8, 9]. In contrast, PSIB did not transect the jejunum, but only made a simple side-to-side anastomosis of the small bowel, which maintained the normal electrophysiology of the small bowel, enabling a certain amount of paraproperistalsis in the bypassed small bowel segments, with a much smaller amount of food regurgitation than that of the end-to-side anastomosis of JIB. Melissas et al.[10] reported that simple side-to-side jejunoileal anastomosis (SJA) to transfer food and biliopancreatic secretions to the distal small bowel normalized FBG levels and OGTT in Goto Kakizaki rats. Therefore, we hypothesized that one of the reasons for the superior efficacy of PSIB over JIB in lowering blood glucose levels could be attributed to the side-to-side anastomosis, which eliminates the retrograde peristalsis of the bypassed small bowel segment, thereby reducing glucose absorption[11]. Furthermore, the proximal end of the blind collaterals were ligated with silk threads, which prevented chyme ingress into the bypassed small bowel segment and reduced the digestive and absorptive area of the GI tract, and achieving a synergistic effect with the side-to-side anastomosis to ensure paraperistalsis of the small bowel. One of our previous studies showed that ligation has a better glycemic effect than no ligation[12]. However, a small amount of bile and other digestive fluids are still allowed to pass through the intestinal collaterals, resulting in substantial changes in the intestinal flora and bile acid metabolism, thereby improving glucose metabolism[13, 14].

Our results showed that in a STZ-induced diabetic rat, the efficacy of PSIB in improving glucose metabolism was better than that of RYGB, with comparable weight loss. RYGB improves glucose metabolism by regulating gastrointestinal hormones, such as GLP-1 and PYY, β-cell function, and intestinal flora[15]. Similar to RYGB, PSIB improves glucose metabolism by regulating gastric hormones, such as gastric starvation hormone, leptin, and fibroblast growth factor 21, and by altering the intestinal flora[16]. Given the superior efficacy of PSIB in treating diabetes mellitus than that of RYGB, we believe that the specific mechanisms are not identical. A study by Patel et al.[17] revealed that gastric bypass plays a dominant role in regulating body weight, whereas small intestinal bypass affects glucose homeostasis mainly through body weight, insulin, and enteric proinsulin-independent mechanisms. However, it does not explain the similarity in the effect of RYGB and PSIB on weight loss in our model. Moreover, Angelini et al.[18] further revealed that the jejunum plays an important role in controlling insulin sensitivity. These two studies may partially explain the effectiveness of PSIB over RYGB in achieving hypoglycemia.In this study, no difference in weight control was observed between PSIB and RYGB; however, further studies are needed to determine whether RYGB is more effective than PSIB in reducing weight in other models, such as the obese rat model. For non-obese patients with diabetes, RYGB should be considered with caution because it is more commonly associated with adverse events and nutritional deficiencies[19, 20]. This study also provides a theoretical basis for the clinical application of PSIB; however, further clinical studies are required.

The overall incidence of hypoalbuminemia after MS is 3–18%[21]. In the present study, total protein levels were significantly decreased in the JIB group, but not in the PSIB or RYGB groups. This aligns with those of previous findings, which demonstrates that excessive bypassing of the small intestine results in malnutrition and consequent liver impairment. In addition, HDL and LDL levels at 6 weeks were lower in the JIB group. Kral et al.[22] suggested that this may be related to increased efflux and/or increased catabolism, e.g., decreased food intake and protein synthesis. Our results showed that although food intake was reduced in both the PSIB and RYGB groups, there was also a trend towards lower TG and LDL levels, but this was not statistically significant. This may be because, although RYGB reverses the dyslipidemia associated with obesity, TG and HDL levels typically improve after weight loss[23].

Our study had certain limitations. First, this study included a small sample size and was conducted over a short period of time. Second, because non-obese rats were selected, significant differences in the efficacy of weight loss could not be demonstrated. Third, alterations in gastrointestinal hormones, pancreatic islet cells, and intestinal bacteria in the surgical group could not be measured or compared, warranting further investigations.

In conclusion, PSIB reduces blood glucose levels and improves glucose tolerance and insulin sensitivity in the early postoperative period, and its efficacy is superior to that of classical RYGB and conventional JIB. Because the non-obese diabetic rat model used in this study did not exhibit significant weight loss after PSIB, this may be beneficial for non-obese diabetic or mildly obese patients with diabetes to achieve good glycemic control without weight loss. Further clinical studies are required to validate these findings.

Conflict of Interest:

All authors declare that they have no conflict of interest.

Ethical Approval:
All animal studies were approved by the Laboratory Animal Ethics Committee of Nanchang University. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Informed consent:
Informed consent does not apply to the study.

Funding:

This study was funded by National Natural Science Foundation of China, No. 82360168, and No. 81960154; Natural Science Foundation of Jiangxi Province, No. 20212BAB206020, and No. 81960154; and Foundation of Health commission of Jiangxi Province, No. SKJP220225830.

Author Contribution

ChiYing Xu, Xin Luo, Kun Yang, RenRan Wu and JinYuan Duan contributed to the conception of the study;ChiYing Xu, Cai TAn, Xin Luo and Lin Lei performed the experiment; ChiYing Xu, Cai Tan and JinYuan Duan contributed significantly to analysis and manuscript preparation; ChiYing Xu, Luo Xin, Kun Yang, Ren Ran, Lei Lin, GuanLei Liu and JinYuan Duan helped perform the analysis with constructive discussions; ChiYing Xu, Cai Tan and JinYuan Duan performed the data analyses and wrote the manuscript.

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No competing interests reported.

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You are reading this latest preprint version

Proximal Small Intestine Bypass Outperforms Roux-en-Y and Jejunoileal Bypass in Glucose Regulation in Streptozotocin‑Induced Diabetic Rats

Status:

Version 1

Abstract

Figures

Key points

Introduction

Materials and Methods

Animal Model

PSIB (60% Bypass of the Small Intestine)

JIB (with 85%- Bypassing of the Small Intestine)

RYGB

Sham Operation

Body Weight and Food Intake

Fasting blood glucose (FBG)

Oral Glucose Tolerance Tests (OGTT) and Insulin Tolerance Tests (ITT)

Biochemical Test

Statistical Analysis

Results

Body Weight

Global Food Intake

FBG

OGTT and ITT

Biochemical Testing

Discussion

Declarations

Conflict of Interest:

Ethical Approval:
All animal studies were approved by the Laboratory Animal Ethics Committee of Nanchang University. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Informed consent:
Informed consent does not apply to the study.

Funding:

Author Contribution

References

Additional Declarations

Status:

Version 1

Proximal Small Intestine Bypass Outperforms Roux-en-Y and Jejunoileal Bypass in Glucose Regulation in Streptozotocin‑Induced Diabetic Rats

Status:

Version 1

Abstract

Figures

Key points

Introduction

Materials and Methods

Animal Model

PSIB (60% Bypass of the Small Intestine)

JIB (with 85%- Bypassing of the Small Intestine)

RYGB

Sham Operation

Body Weight and Food Intake

Fasting blood glucose (FBG)

Oral Glucose Tolerance Tests (OGTT) and Insulin Tolerance Tests (ITT)

Biochemical Test

Statistical Analysis

Results

Body Weight

Global Food Intake

FBG

OGTT and ITT

Biochemical Testing

Discussion

Declarations

Conflict of Interest:

Ethical Approval: All animal studies were approved by the Laboratory Animal Ethics Committee of Nanchang University. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Informed consent: Informed consent does not apply to the study.

Funding:

Author Contribution

References

Additional Declarations

Status:

Version 1

Ethical Approval:
All animal studies were approved by the Laboratory Animal Ethics Committee of Nanchang University. All applicable institutional and/or national guidelines for the care and use of animals were followed.

Informed consent:
Informed consent does not apply to the study.