Abstract
Introduction:
Bariatric surgery is the effective treatment for morbid obesity that has inevitable complications, including postoperative bleeding and staple-line leakage. Erythrocyte sedimentation rate (ESR) can be a clinical indicator for prediction of leakage.
Methods:
This retrospective cohort study was done on 1999 patients who underwent sleeve gastrectomy in Erfan-Niyayesh Hospital, Tehran, Iran. ESR levels of patients were evaluated in cases that had postoperative leak. Statistical analyses were performed using SPSS software.
Results:
Among the 2350, 50 subjects experienced gastric leak (2.12%). ESR mean was 73.1 mm/h for cases, statistically significant in patients with leakage compared with the control group. Also, ESR serum level mean was 31.34 mm/h for control groups. Other variables, including C-reactive protein and platelet count, were not statistically significant.
Conclusion:
Higher ESR serum level can be seen in various conditions, but in obese patients who undergo the bariatric surgery, it can be a reliable predictor for postoperative gastric leak complication.
Introduction
Bariatric surgery has become one of the most effective treatments for morbid obesity, with extremely good long-term results on weight loss, comorbidities, and low mortality as well as postoperative complications rate. 1 Bariatric surgery of morbid obese has been improved in the past 15 years. 2 According to the every published report, bariatric surgery is one of the safest operations with complications of <1%.3,4 However, the knowledge about its anatomic reconstruction, the physiological effects of bariatric surgery, and even the prevention and management of complications after bariatric procedure have not directly incorporated in general procedure preparing programs.5,6 Hence, general surgeons should expand their knowledge in basic anatomic, clinical, and surgical understanding because they might face postoperatively acute or chronic complications for their patients. 6 Bariatric surgery can cause early complications, including primarily staple-line leakage and bleeding in the immediate postoperative days. Late postoperative complications include abscess development or delayed postoperative staple-line leakage with fistula as well as sleeve stenosis. In addition, some patients can develop a rare case of sleeve gastrectomy, which is deep vein thrombosis. 7
As mentioned, gastrointestinal staple-line leakage remains one of the most unavoidable complications after procedure, resulting in increased health care cost and postoperative pain in patients. 8 According to several meta-analyses reports, gastrointestinal leak rate has been estimated ranging from 2.5% to 7% after various types of bariatric surgery.6–9 However, the postoperative gastrointestinal leak has been constantly dropping recently and its occurrence is low 10 ; nonetheless, the leakage is still a principal complication, leading to increased morbidity and mortality rate. Various surgeons have employed different interventions for detecting leaks either intraoperatively or postoperatively such as placement of an orogastric tube with distention of the gastric pouch with air, endoscopy with carbon dioxide insufflations, and methylene blue dye. 6
Researchers have recently found that in patients with low body mass index (BMI), postoperative increased heart rate (tachycardia >120 beats per minute [bpm]), evidence of respiratory distress and decreased hemoglobin were significantly associated with bleeding.11,12 Fazl Alizadeh et al. reported that oxygen dependency, hypoalbuminemia, sleep apnea, hypertension, and diabetes were critical factors related to increased risk of leak. 13 In addition, preoperative platelet count and Preoperative Normalised Ratio and systolic blood pressure were not significantly related to postoperative bleeding. 12 On the other side, the association between preoperative partial thromboplastin time and bleeding was significant. 12 Burgos et al. believed that increased white blood cell (WBC) and C-reactive protein (CRP) levels, abdominal pain, tachycardia, tachypnea, and fever are more common in subjects with gastric leak. 11
From clinical perspective, an erythrocyte sedimentation rate (ESR) is one of the blood tests, is usually ordered by physicians for patients with symptoms such as inflammation in the body, headaches, fever, joint stiffness, neck or shoulder pain, weight loss, loss of appetite, anemia, and fever.14,15
Higher ESR levels may be associated with a medical condition, such as infection or inflammation (especially inflammatory bowel disease), rheumatoid arthritis, cardiovascular or kidney disease, and some types of cancers. Higher ESR levels do not necessarily mean that the patients have a medical condition that requires treatment. 15 For example, certain medications and dietary supplements can also affect ESR results, including oral contraceptives, cortisone, vitamin A, and aspirin. A moderate ESR may indicate pregnancy, menstruation, or anemia, rather than an inflammatory disease. A slow ESR may indicate a blood disorder such as polycythemia, sickle cell anemia, and leukocytosis.14,15
The main purpose of this study was to evaluate correlations of ESR, CRP, and platelet count with incidence of intermediate gastrointestinal leak in obese subjects who underwent sleeve gastrectomy.
Materials and Methods
Data source
We performed a retrospective cohort study using the database of Erfan Niayesh Hospital bariatric procedures performed by Taha Anbara, laparoscopic surgeon and MD.
Surgical procedure
Sleeve gastrectomy was performed for all subjects according to the standard protocol and in a similar method by a specific surgeon with similar tools during the same duration. After prep and draping under general anesthesia, a 10 mm trocar cannula (Covidien, Cincinnati, OH) was inserted above the umbilicus. Then three 5 mm trocar canulas and one 15 mm canula (Covidien) were inserted under direct vision in the proper place. The gastrocolic ligament was divided with LigaSure. Then the sleeve gastrectomy was done with seven 4.5 mm staples (black cartridges). The divided part of the stomach was taken out later and the place of staple line was sutured with 2-0 yarn. Afterward the drain was placed in gastrectomy site. The canulas were taken out later under direct sight and then reliable from homeostasis, abdominal gas was drained and the place of canula 10 was repaired. To determine leakage, we transiently block flow into the duodenum with long intestinal forceps at the pyloric channel. The removed specimen, which is removed easily through the 15 mm port at the right upper abdominal quadrant, is sent for histological analysis. Finally, one Silastic drain is always left at side of the gastric suture line.
Clinical evaluation
Clinical sign and symptoms were repeatedly surveyed for all subjects every 6 h after surgery. Intraoperative gastrointestinal leakage was not observed during procedure in any subjects.
Study design and population
Clinical data on adult 199 obese subjects who underwent sleeve gastrectomy were evaluated according to the Current Procedural Terminology code: LSG (43,775). Approval for the use of the data in this study was obtained from the Efran-Niyayesh Hospital. Subjects were categorized into two groups, those who experienced postoperative gastrointestinal leakage (cases) and those without any type of leakage neither intraoperatively nor after procedure (As a control group). Preoperative comorbidities and characteristics were examined to determine predictive factors of leakage. Oral contrast was given during the study and the contrast was followed when it goes from the mouth to the small intestine. Emergent, revisional, and converted cases were excluded. The time/location of appearance and closure of leakages were diligently recorded in all cases.
Definition of leakage
The UK Surgical Infection Study Group has defined a standard definition of anastomotic leakage: “the leak of luminal contents from a surgical join between two hollow viscera,” it may also demonstrate a gastrointestinal leak in a suture line around the organ. According to the time of leakage appearance, they have been previously classified and published 14 as follows: early (leaks appearing 1–3 days after procedure), intermediate (leaks appearing 4 days to a week after surgery), and late (leaks appearing more than a week after procedure).
Patients
Fifty cases who had postoperative gastrointestinal leakage, considered in the study, and 149 control cases (ratio 3 to 1) randomly selected to increase the reliability of the study, and the information of control cases have been extracted from the medical records of Erfan Hospital. All the cases were undergoing the sleeve gastrectomy during 2017–2019 in Erfan Hospital under the supervision of the same surgeon with the same tools. Variables used in the multivariate analyses included demographic data (BMI, age, and gender), preoperative comorbidities, procedural type, and various intraoperative and postoperative interventions.
Statistical analysis
Adjusted and unadjusted binary logistic regression models were used to evaluate effects of independent variables on leaking outcome (0 = no, 1 = yes). Independent variables include gender, age, and ESR. The significance level defined as 0.05 (a = 0.05). Both adjusted and unadjusted variables with significant levels are included in final models and are reported. Statistical analysis was performed using IBM SPSS Statistics 25 (SPSS, Chicago, IL).
The final predicting model for leaking outcome was designed using the following regression model:
The final adjusted prediction model of log (odds) for leaking outcome has been calculated using the following equation:
Results
We investigated that among the 2350 patients who underwent sleeve gastrectomy from 2016 to 2019, 50 subjects experienced gastric leak (2.12%). The total sample size was 199 patients, including 50 cases experiencing leak and 149 controls (randomized from 2350 patients). 69.8% of the cohort, 70% of cases, and 69.8% of controls were females. Mean age for the cohort was 38.15 (minimum 12 years old and maximum 63 years old). ESR mean was 73.1 mm/h for cases, which is statistically significant in patients with leakage compared with the control group. Also, ESR serum level mean was 31.34 mm/h for control groups. More descriptive results are reported in Table 1.
The Distribution of Study Variables
ESR, erythrocyte sedimentation rate.
Results of adjusted and unadjusted logistic regression are reported in Table 2. Females were taken as reference group due to bigger proportion in the sample. The only independent variable that had significant association with staple-line leakage was ESR (OR = 1.051). This means by every 1 U increase of ESR, the odds for staple-line leakage occurrence increase by 5.1%.
Binary Logistic Regression Models Results (Odds Ratio)
Discussion
Sleeve gastrectomy procedure has been popularly employed for the management of morbid obesity, and this operation has a series of inevitable complications. Staple-line leakage is one of these complications, ranging from 7% to 25% after bariatric surgery. 6 Although researchers mentioned various approaches, surgeons utilize the endoscopic approach such as stent inserting, clips, and biologic glue. 16 This study comprises our experiences with 199 patients, with or without staple-line leakage, after sleeve gastrectomy. The final adjusted prediction model of log (odds) for leaking outcome can be used to predict leaking outcome. Exponential of (y) gives odds of occurrence of leaking for each patient with archived ESR. It should be noted that because of the impact of other factors affecting on staple-line leakage outcome, this model might not be 100% precise.
According to the results, ESR serum level in patients with leak after sleeve gastrectomy was significantly increased in comparison with ESR levels of patients without any complications after the surgery. ESR serum levels mean were 73.1 mm/h for cases and 31.34 mm/h for controls.
As previously mentioned, high ESR serum levels can be seen in various conditions such as cardiovascular and kidney disease and obstructive sleep apnea.14,15 However, after bariatric surgery, patients with obesity start to develop weight loss that may lead to an increase in ESR serum levels, but ESR mean in patients with leak compared with control group was significantly higher, which means, by every 1 unit increase in ESR serum levels, the odds for leakage occurrence increase by 5.1% in patients after bariatric surgery. The normal range of ESR for men is 0–22 mm/h and 0–29 mm/h for women, 15 but in subjects with obesity due to a series of interactions, it can get elevated. This means macrophage and adipose tissue secrete cytokines and interleukins, resulted in stimulation of liver to produce fibrinogen, CRP and haptoglobin, which in turn elevate ESR serum levels during inflammation (Fig. 1). 15 Therefore, with this diagnostic value of ESR, surgeons can employ ESR serum levels immediately after procedure, instead of common interventions that might increase the cost and duration of treatment. 6 In vulnerable patients with abnormal ESR levels, a series of technical recommendations can be done to prevent leakage after operation: use a 40 Fr size or more bougie, initiate the gastric transection 5–6 cm from the pylorus, use proper cartridge colors from antrum to fundus, reinforce the staple line with buttress material, 5 order an appropriate staple line, 6 perform an intraoperative methylene blue test, remove the crotch staples, maintain suitable traction on the stomach before firing as well as avert from the angle of His (at least 1 cm) and check the staple-line bleeding during the procedure.

The impacts of inflammation on serum level of ESR. ESR, erythrocyte sedimentation rate.
Although gastric leakage can be caused by either mechanical or ischemic reasons, ESR serum levels might be a reliable predictor for postoperative leakage. Hence, in patients with higher ESR, more sedulous management (leaving a shorter antrum and using a smaller bougie) can be performed by surgeons and this may open a new chapter in terms of personalized surgery with lesser cases of leak complications among subjects. Previous studies have not paid sufficient attention to the molecular dimension of gastric leak, instead most of the studies focused on mechanical dimension and the management of this complication. Researchers found that the greater bougie was related to a leakage rate of 0.6% in comparison with those who used smaller sizes whose leak rate was 2.8%. 16 However, Keren et al. reported normal ESR levels of patients with gastric leakage, which is in contrast to our findings. 17
Other variables, including gender, age as well as platelet count and CRP serum level, were not significantly different compared with control patients. In line with these results, Keren et al., in 2014, and Surace et al., in 2011, reported that gastric leak after sleeve gastrectomy present no correlation with serum levels of CRP and WBC.17,18 Nevertheless, more studies are warranted to address the question why ESR serum level has been increased without any significant changes in CRP levels.
Conclusion
This study reports the clinical correlation of gastric leakage and platelet count, ESR and CRP serum levels, and gives practical instructions to prevent and manage leaks after sleeve gastrectomy. In short, these recommendations are as follows: (1) use greater size of bougie, (2) begin the gastric transection 5–6 cm from the pylorus, (3) use suitable cartridge colors, (4) reinforce the staple line with buttress material, (5) follow an appropriate staple line, (6) remove the crotch staples, (7) maintain adequate traction on the stomach before firing, (8) keep distance from the angle of His, (9) check the staple-line bleeding, and (10) perform a methylene blue test during the procedure.
Footnotes
Acknowledgments
We thank all those who helped in this study.
Author Disclosure Statement
No competing financial interests exist.
Funding Information
No funding was received for this article.
