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Different surgical approaches in laparoscopic sleeve gastrectomy and their influence on metabolic syndrome

Different surgical approaches in laparoscopic sleeve gastrectomy and their influence on metabolic... Obesity is a growing health, social, and economic issue and became an epidemic, according to recent report of World Health Organization. The only method with scientifically proved efficiency of body mass loss is a surgical treatment. Laparoscopic sleeve gastrectomy (LSG) is recently a leading method in metabolic surgery. There are no standards of operative technique for LSG so far. The influence of technique modification on metabolic effect has not been described clearly. The aim of this study was to evaluate metabolic effects in patients with morbid obesity who underwent various surgical approaches of LSG. The study included 120 patients who were randomly divided into 3 groups: Group I, where bougie size was 32French (Fr), Group II —36Fr and Group III—40Fr. Each group was divided into 2 subgroups, based on the distance of resection beginning from the pylorus—2 or 6cm. Statistical analysis of: body mass index (BMI), the Percentage of Excess Weight Loss (%EWL), the Percentage of Excess BMI Loss (%EBMIL), levels of glucose and insulin on an empty stomach, glycated hemoglobin (HbA1c), insulin resistance (Homeostatic Model Assessment of Insulin Resistance Index—HOMA-IR), aspartate transaminase (AST), alanine transaminase (ALT), total cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides (TG), and C-reactive protein (CRP) were under investigation. Statistically significant decrease in body mass, BMI, %EWL, %EBL, glucose, and insulin concentrations has been observed in all studied groups. It was the highest when the smallest calibration tube has been used (32Fr). Similar results were observed in HOMA- IR and HbA1c levels. Statistically significant decrease of total cholesterol, LDL, and TG concentrations have been observed. Significant increase of HDL in every group has been also noted. Postoperative CRP values were the lowest when the smallest bougie was used. LSG is effective method of obesity treatment. Metabolic effects of LSG are the most noticeable when a small bougie size is used. Abbreviations: %EBMIL = the Percentage of Excess BMI Loss, %EWL = the Percentage of Excess Weight Loss, ALT = alanine transaminase, ASMBS = American Society for Metabolic and Bariatric Surgery, AST = aspartate transaminase, BMI = body mass index, CRP = C-reactive protein, Fr = French, GLP-1 = glucagon-like peptide 1, HbA1c = glycated hemoglobin, HDL = high-density lipoprotein, HOMA-IR = Homeostatic Model Assessment of Insulin Resistance Index, LDL = low-density lipoprotein, LSG = laparoscopic sleeve gastrectomy, NAFLD = nonalcoholic fatty liver disease, PYY = peptide YY, RYGB = Roux-Y gastric bypass, TG = triglycerides. Keywords: bariatric surgery, bougie size, laparoscopic sleeve gastrectomy, metabolic syndrome 1. Introduction Editor: Yan Li. Funding: The study was funded by Medical University of Bialystok (grant no. N/ Obesity is a process of excessive fat accumulation in the body ST/ZB/15/002/1140). which results in homeostasis breakdown and causes biochemical The authors have no conflicts of interest to disclose. and physiological dysfunctions of tissues. Obesity also leads to a b the development of comorbidities such as hypertension, diabetes 1st Department of General and Endocrinological Surgery, Department of Endocrinology, Diabetology and Internal Medicine, Department of Emergency mellitus type 2, sclerosis, nonalcoholic fatty liver disease [1–4] Medicine and Disasters, Medical University of Bialystok, Bialystok, Podlaskie, (NAFLD), goat, obstructive sleep apnea, and tumors. Poland. Conservative treatment, which consists of diet, lifestyle Correspondence: Dawid Groth, Medical University of Bialystok, Bialystok, modification, cognitive behavioral therapy, and pharmacothera- Podlaskie, Poland (e-mail: dawidgroth@gmail.com). py, must be systematic and long-term. However, body weight loss Copyright © 2018 the Author(s). Published by Wolters Kluwer Health, Inc. [5] success rate does not exceed 10%. Due to unsatisfactory results This is an open access article distributed under the Creative Commons of aforementioned methods, surgical treatment has become Attribution License 4.0 (CCBY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. increasingly important. Obesity surgery is the most effective way [6] to long-term weight loss. Nowadays, among many surgical Medicine (2018) 97:4(e9699) approaches, laparoscopic sleeve gastrectomy (LSG) gains Received: 25 August 2017 / Received in final form: 13 December 2017 / Accepted: 2 January 2018 popularity, because of satisfactory weight loss and remission of comorbidities. Final effect of the therapy is a result of http://dx.doi.org/10.1097/MD.0000000000009699 1 Hady et al. Medicine (2018) 97:4 Medicine decreased stomach volume and, in consequence, lower food total cholesterol, HDL, LDL, and TG were evaluated in order to intake. Moreover, recent studies suggest that resecting a larger control changes in particular time points after the surgery. Rates part of the stomach (fundus and body), affects gastrointestinal of %EWL, %EBMIL, and HOMA-IR were calculated according tract peristalsis, neurohormonal system, and carbohydrate–fat to the following formulas: [7,8] balance. LSG has no established standards regarding the (1) %EWL=(preoperative weightfollow-up weight)/(preoper- diameter of the stomach left after the surgery. Recommendations ative weightideal weight)100 of surgical associations are a result of clinical reports and For ideal weight calculations, the Lorenz formulas were metaanalyses, however, there is still a lack of final agreement on used: the technique of LSG. The knowledge about the influence of Ideal female weight=(height in cm100)((height in surgical approach on patient metabolic response is still cm150)/2), incomplete. Ideal male weight=(height in cm100)((height cm The aim of this study was to analyze body weight, BMI, the 150)/4). Percentage of Excess Weight Loss (%EWL), the Percentage of (2) %EBMIL=(preoperative BMIfollow-up BMI)/(preopera- Excess BMI Loss (%EBMIL) in patients with morbid obesity who tive BMI25)100 underwent various surgical approaches of LSG: different (3) HOMA-IR=glucose level (mg/dL)insulin concentration diameter of bougie for stomach volume calibration and different (mU/L)/405; quotient >2.6 supported insulin resistance. distance of cut-off line from the pylorus. Levels of glucose and insulin on an empty stomach, glycated hemoglobin (HbA1c), All data were extracted from original sources to fields within an insulin resistance (Homeostatic Model Assessment of Insulin Excel (Microsoft, Redmond, WA) database. Data manipulation Resistance Index—HOMA-IR), aspartate transaminase (AST), and analysis was conducted using SPSS statistical software for alanine transaminase (ALT), total cholesterol, high-density Windows, version 21 (IBM SPSS, Chicago, IL). Selected lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides demographic (age, weight, body mass index [BMI, kg/m ]) and (TG), and C-reactive protein (CRP) were also under investiga- surgical technique (bougie size and distance from pylorus) tion. variables were estimated using mean, SD, range, and the percentage of studies reporting on each variable. Comparison of 3 studied groups was performed using 2. Patients and methods ANOVA with post hoc Tukey test. Pairwise t test was used to The material consists of 120 patients hospitalized in 1st evaluate the statistical significance between the same groups in Department of General and Endocrinological Surgery, Medical the different periods of the follow-up (1, 3, and 6 months after the University of Bialystok, between 2012 and 2014 who underwent surgery). Pearson test was used to determine whether there were LSG in order to treat morbid obesity. Patients were divided into 3 any differences in the distribution of gender by reinforcement groups by the bougie size: Group I, where bougie size was 32 method. French (Fr), Group II—36Fr and Group III—40Fr. The bougie Statistical tests were 2-tailed and values of P<.05 were size was chosen randomly for each patient before the surgery. considered statistically significant. Each group was divided into 2 subgroups, based on the distance Pearson test was used to determine whether there were any of resection beginning from the pylorus—2 or 6cm. correlations between studied groups. Values of P<.05 were Criteria of qualification of patients to the surgery were considered statistically significant. All calculations were per- [9] described previously. All patients had met at least 3 criteria formed by professional statistician. necessary for the diagnosis of metabolic syndrome according to [10] the International Diabetes Federation. Follow-up of the level 3. Results of metabolic syndrome reduction was limited to 1 year. All patients provided written informed consent before the In all studied groups a statistically significant decrease in body study and additional written informed consent was obtained mass and BMI was observed. The highest weight loss was before the surgical procedure. This study was approved by the observed in Group I, where the smallest bougie was used (32Fr) Ethics Committee of the Medical University of Bialystok, Poland compared to Group II and Group III (Table 2). (No R-I-002/438/2014) in accordance with the guidelines of the Postoperative dynamics of weight and BMI loss were evaluated Helsinki Declaration. using %EWL and %EBMIL. During 6 months follow-up period, There were 76 female (63.3%) and 44 male (36.7%) patients in the most noticeable decrease of body weight and BMI was examined group. Average age was 43. Groups characteristics are observed in Group I. One month after the surgery, %EWL in shown in Table 1. Group I was 22.26%±8.25%, after 3 months was equal to One team of surgeons (1 operator and 2 assistants) performed 41.23±9.69%, and after 6 months reached 59.61±12.59%; the [9] all surgeries, according to the procedure described before. Cut- decrease was statistically significant (Table 2, Fig. 1). off line of the omentum reached upwards the left diaphragmatic BMI loss measured with %EBMIL was significantly lower in branch and downwards approximately 2 or 6cm from the all studied groups. One month after the surgery in Group I it was pylorus. The stomach was reduced to the bougie size 32, 36, or equal to 27.31±12.22%. In 3 months follow-up, it was 50.55± 40Fr (Group I, Group II, and Group III). Leak test was performed 15.3% and at the end of the observation period reached 72.99± with 5% glucose and air insufflation. Patients were discharged 21.08% (Table 2, Fig. 2). There were no statistically significant home in the second or third day after the surgery and were differences between 2 and 6cm cut-off lines start from the regularly examined by clinical dietician and surgeon during the pylorus. follow-up period. In our research, a glucose level was also measured and All patients were examined 1, 3, and 6 months after the compared with preoperative results. During 6 months follow-up, surgery. Fasting 10 to 12hours blood was taken for a clot tube statistically significant changes in glucose concentration in and then centrifuged until serum was obtained. Insulin, glucose, plasma have been observed in every stage of observation and 2 Hady et al. Medicine (2018) 97:4 www.md-journal.com Table 1 Patients characteristics before surgery (mean and SD). Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) P Age, y 41.25± 11.21 42.82± 8.79 45.38± 11.64 NS ∗∗ NS ∗∗∗ NS Sex, F/M 25/15 28/12 23/17 Body mass, kg 130.6± 25.73 135.96± 30.6 140.93± 25.12 NS ∗∗ NS ∗∗∗ NS BMI, kg/m 44.56± 7.88 47.82± 9.13 50.02± 7.15 NS ∗∗ ∗∗∗ NS Glucose, mg/dL 105.58± 31.11 113.65± 32.77 119.14± 33.15 NS ∗∗ ∗∗∗ NS Insulin, mU/mL 20.93± 13.83 22.48± 11.58 32.11± 24.41 NS ∗∗ ∗∗∗ NS HOMA-IR 5.6± 4.14 6.53± 4.55 9.61± 7.75 NS ∗∗ ∗∗∗ NS HbA1C, % 5.77± 0.69 5.89± 0.83 5.88± 0.47 NS ∗∗ NS ∗∗∗ NS ALT, IU/L 39.88± 42.92 31.63± 22.89 35.78± 18.08 NS ∗∗ NS ∗∗∗ NS AST, IU/L 32.05± 21.56 24.53± 12.53 26.4± 9.01 NS ∗∗ NS ∗∗∗ NS Total cholesterol, mg/dL 203.63± 31.62 208.2± 42.52 201.98± 37.97 NS ∗∗ NS ∗∗∗ NS LDL, mg/dL 143.2± 34.33 138.15± 43.22 134.83± 37 NS ∗∗ NS ∗∗∗ NS HDL, mg/dL 45± 11.62 50.43± 13.28 45.28± 12.74 NS ∗∗ NS ∗∗∗ NS TG, mg/dL 166.65± 86.9 154.95± 62.85 165.95± 72.76 NS ∗∗ NS ∗∗∗ NS CRP, mg/L 7.45± 7.08 9.55± 8.34 9.53± 7.78 NS ∗∗ NS ∗∗∗ NS ALT= alanine transaminase, AST= aspartate transaminase, BMI= body mass index, CRP= C-reactive protein, HDL= high-density lipoprotein, HOMA-IR= Homeostatic Model Assessment of Insulin Resistance Index, LDL= low-density lipoprotein, NS= non-significant, SD= standard deviation, TG= triglycerides. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. in all studied groups (Table 3). The highest decrease was observed Insulin and glucose concentrations allowed us to measure in Group I and II (Table 3). HOMA-IR. Reduction of insulin resistance was discovered in every All measurements of insulin concentration were also statisti- studied group, however in Group I it was the most noticeable (2.31± cally significant with a tendency to decrease in comparison to 1.43; Table 3, Fig. 3).Value of HOMA-IR was statistically significant preoperative values (Table 3). The greatest reduction in in every stage of observation. Moreover, a 2cm cut-off line from the concentration of insulin in serum was observed 1 month after pylorus approach was related to lower HOMA-IR 1 month after the the surgery. Three and 6 months postoperatively, the values also LSG in Group I (1.907 compared with 2.718; P=.007) and 3 months decreased, but less dynamically. However, the results were after the surgery in Group II (1.248 vs 2.109; P=.018). statistically significant in every stage of the study. Resection 2cm Our study revealed statistically significant decrease in HbA1c from the pylorus resulted in more dynamic decrease of insulin in studied Group I and II, 3 months after the surgery (5.32± concentration than 6cm approach—1 month after the surgery in 0.51% and 5.32±0.45%) and 6 months after the surgical Group I (respectively, 8.415 and 11.53mU/mL) and 3 months treatment (5.25±0.34 and 5.19±0.46) (Table 3, Fig. 4). after the treatment in Group II (5.842 and 8.785mU/mL). Additionally, high correlation between weight (R=0.52; 3 Hady et al. Medicine (2018) 97:4 Medicine Table 2 Postoperative changes in body weight, BMI, %EWL and %EBMIL. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P Body weight (kg) after 1 mo 116.29 23.69 121.99 25.31 125.63 23.86 NS ∗∗ ∗∗∗ NS Body weight (kg) after 3 mo 104.05 22.19 108.76 22.59 114.68 22.76 NS ∗∗ ∗∗∗ NS Body weight (kg) after 6 mo 91.96 19.39 96.01 21.64 102.53 22.91 NS ∗∗ ∗∗∗ NS BMI (kg/m ) after 1 mo 39.67 7.36 42.94 7.75 44.58 6.85 .017 ∗∗ ∗∗∗ NS BMI (kg/m ) after 3 mo 35.47 6.78 38.28 6.89 40.72 6.82 .019 ∗∗ <.001 ∗∗∗ NS BMI (kg/m ) after 6 mo 31.34 5.9 33.8 6.72 36.39 6.98 .031 ∗∗ <.001 ∗∗∗ NS %EWL after 1 mo 22.26 8.25 18.92 6.89 20.09 6.21 .036 ∗∗ NS ∗∗∗ NS %EWL after 3 mo 41.23 9.69 36.81 11.71 34.5 8.67 NS ∗∗ ∗∗∗ NS %EWL after 6 mo 59.61 12.59 54.73 14.61 36.39 6.98 NS ∗∗ ∗∗∗ NS %EBMIL after 1 mo 27.31 12.22 22.27 8.76 22.76 7.29 .017 ∗∗ ∗∗∗ NS %EBMIL after 3 mo 50.55 15.3 43.32 14.88 40.72 6.82 .027 ∗∗ <.001 ∗∗∗ NS %EBMIL after 6 mo 72.99 21.08 64.5 19.07 57.25 15.66 NS ∗∗ ∗∗∗ NS BMI= body mass index, %EBMIL= the Percentage of Excess BMI Loss, %EWL= the Percentage of Excess Weight Loss, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. P=.0006) and BMI (R=0.46; P=.0026) before and 6 months Group III the relationship was not calculated. However, in this after the surgery (R=0.42; P=.007 vs R=0.34; P=.034) and study Group, the 2cm starting line from the pylorus resulted in HbA1c was observed. In Group II weight and BMI correlated statistically significant higher HbA1c level compared to the 6cm with HbA1c only before the surgery (R=0.47; P=.002). In approach (3 months after the surgery, 5.69% and 5.2%; Figure 1. Changes of %EWL 1, 3, and 6 months after the surgery. Figure 2. Changes of %EBMIL 1, 3, and 6 months following the LSG. 4 Hady et al. Medicine (2018) 97:4 www.md-journal.com Table 3 Postoperative changes in carbohydrate metabolism. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P Glucose (mg/dL) after 1 mo 91.8 10.37 94.9 16.85 101.5 16.26 NS ∗∗ ∗∗∗ Glucose (mg/dL) after 3 mo 91.15 9.25 90.23 10.42 97.1 9.13 NS ∗∗ ∗∗∗ Glucose (mg/dL) after 6 mo 90.03 6.01 89.38 9.3 94.45 7.74 NS ∗∗ ∗∗∗ Insulin (mU/mL) after 1 mo 9.97 5.64 10.79 5.88 16 9.76 NS ∗∗ ∗∗∗ Insulin (mU/mL) after 3 mo 8.68 5.11 7.31 4.06 11.47 6.6 NS ∗∗ ∗∗∗ Insulin (mU/mL) after 6 mo 6.76 4.56 5.98 3.69 9.22 5.8 NS ∗∗ ∗∗∗ <.001 HOMA-IR after 1 mo 2.31 1.43 2.67 1.89 4.21 3.24 NS ∗∗ ∗∗∗ HOMA-IR after 3 mo 2.01 1.37 1.68 1.12 2.8 1.79 NS ∗∗ ∗∗∗ <.001 HOMA-IR after 6 mo 1.52 1.13 1.36 0.98 2.2 1.55 NS ∗∗ ∗∗∗ <.001 HbA1c (%) after 1 mo 5.63 0.77 5.53 0.65 5.71 0.41 NS ∗∗ NS ∗∗∗ NS HbA1c (%) after 3 mo 5.32 0.51 5.32 0.45 5.57 0.34 NS ∗∗ ∗∗∗ HbA1c (%) after 6 mo 5.25 0.34 5.19 0.46 5.43 0.33 NS ∗∗ ∗∗∗ HbA1c= glycated hemoglobin, HOMA-IR= Homeostatic Model Assessment of Insulin Resistance Index, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. P= .022). In 6 months follow-up, the values were 5.58% (2 cm significantly decreased 6 months after the LSG in all studied from the pylorus) and 5.28% (6 cm); P= .004. groups (Table 4, Fig. 5). Our study did not show any abnormalities in AST and ALT We have also studied the effect of LSG on lipid profile of obese levels in obese patients. We observed that ALT concentration patients. During the follow-up, statistically significant decrease in Figure 3. Changes of HOMA-IR 1, 3, and 6 months after the surgery. Figure 4. Changes of HbA1c 1, 3, and 6 months after the surgery. 5 Hady et al. Medicine (2018) 97:4 Medicine Table 4 Postoperative changes in transaminases. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P ALT (IU/L) after 1 mo 39.95 37.23 32.9 15.71 42.08 28.2 NS ∗∗ NS ∗∗∗ NS ALT (IU/L) after 3 mo 23.2 10.22 21.8 9.33 27.35 13.41 NS ∗∗ NS ∗∗∗ NS ALT (IU/L) after 6 mo 17.83 6.85 14.88 5.64 20.85 9.69 .036 ∗∗ NS ∗∗∗ <.001 AST (IU/L) after 1 mo 35.68 24.37 27.1 10.1 32.9 18.89 NS ∗∗ NS ∗∗∗ NS AST (IU/L) after 3 mo 23 10.22 21.8 9.33 27.35 13.41 NS ∗∗ NS ∗∗∗ NS AST (IU/L) after 6 mo 17.5 5.96 16.25 3.5 17.43 5.66 NS ∗∗ NS ∗∗∗ NS ALT= alanine transaminase, AST= aspartate transaminase, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. total cholesterol level in all studied group was observed, however, We have stated a statistically significant decrease in TG in all the reduction was the most dynamic in Group I (Table 5). studied groups, 3 and 6 months postoperatively (Table 5). Analyzing the differences in surgical approach, patients after 2cm Our study also included an evaluation of CRP concentration in resection from the pylorus reached statistically lower levels of plasma. Average level was between reference ranges in all studied total cholesterol than patients in whom the resection started 6cm groups during the whole follow-up, however, CRP values in from the pylorus (177.7mg/dL vs 192.7mg/dL; P=.028). Group I were statistically lower in comparison to Group III in Only at the beginning of the follow-up period the reduction of every stage of the study (Table 6). LDL was statistically significant in all studied groups (126.1± The complication rate in our study group was 2.5% (n=3). 36.29mg/dL vs 125.5±48.14mg/dL vs 126.03±34.78mg/dL) The complications were: acute pancreatitis (0.83%), bleeding compared to the preoperative values (Table 5). from the first trocar site into the abdominal cavity (0.83%) and Changes in HDL level occurred 3 months after the LSG and it superficial thrombophlebitis of the lower extremity (0.83%). raised in all studied groups (data not statistically significant), however, 6 months after the surgery, HDL values significantly 4. Discussion increased in every group (Table 5). In patients who underwent LSG LSG has many advantages such as simplicity of the technique and with 2cm cut-off line from the pylorus, where the bougie size was short operative time (short anesthesia and less postoperative 40Fr (Group III), a significant increase in HDL, 3 and 6 months complications). LSG approach does not need any bypass after the surgery, was observed in comparison to the patients after anastomosis, so the physiological passage of gastrointestinal 6cm resection (after 3 months—52.7mg/dL vs 44.25mg/dL; tract is not interrupted. P=.015 and 6 months—58.05mg/dL vs 46.9mg/dL; P=.002). Our study reveals that the highest BMI and body weight reduction occurs when the smallest bougie size is used (32Fr vs 36Fr vs 40Fr). The decrease was significantly higher in studied Group I compared with Group III. Six months after the surgery in studied Group I patients lost 59.61% of their preoperative weight and 72.99% of BMI (measured with %EWL and %EBMIL). [8] Langer et al obtained similar results. In their study, %EWL in 6 months follow-up was 61.4%±16.3, although the bougie size [11] was 48Fr. Parikh et al observed that differences in %EWL were around 40% between studied groups (40Fr vs 60Fr), however, the results were not statistically significant. It is worth mentioning, that bougie sizes more than 40Fr are rarely used. [12] Yuval et al compared two LSG approaches with different bougie sizes (<40Fr vs ≥40Fr) and stated no statistically significant differences in %EWL between the groups. Unsatisfactory weight loss forces surgeons to change the [13] surgical technique for more restrictive. There is still lack of Figure 5. Changes of triglycerides 1, 3, and 6 months after the LSG. evidence that smaller bougie size is related to more intensive 6 Hady et al. Medicine (2018) 97:4 www.md-journal.com Table 5 Postoperative changes in lipid profile parameters. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P Total cholesterol (mg/dL) after 1 mo 179.35 26.75 181.53 46.16 184.65 35.61 NS ∗∗ NS ∗∗∗ NS Total cholesterol (mg/dL) after 3 mo 189 30.15 186.53 40.46 184.1 30.28 NS ∗∗ NS ∗∗∗ NS Total cholesterol (mg/dL) after 6 mo 182.3 33.61 194.6 47.1 185.15 27.66 NS ∗∗ NS ∗∗∗ NS LDL (mg/dL) after 1 mo 126.1 35.29 125.5 48.14 126.03 34.78 NS ∗∗ NS ∗∗∗ NS LDL (mg/dL) after 3 mo 137 32.77 127.38 41.56 126.35 31.09 NS ∗∗ NS ∗∗∗ NS LDL (mg/dL) after 6 mo 135.68 34.25 133.1 47.5 127 28.49 NS ∗∗ NS ∗∗∗ NS HDL (mg/dL) after 1 mo 38.7 9.41 42.75 11.16 43.03 11.46 NS ∗∗ NS ∗∗∗ NS HDL (mg/dL) after 3 mo 47.05 12.48 49.25 12.97 48.48 11.01 NS ∗∗ NS ∗∗∗ NS HDL (mg/dL) after 6 mo 54.03 18.96 56.13 14.16 52.48 12.27 NS ∗∗ NS ∗∗∗ NS TG (mg/dL) after 1 mo 148.35 52.79 127.78 39.4 152.13 50.16 NS ∗∗ NS ∗∗∗ TG (mg/dL) after 3 mo 135.55 49.3 121.48 38.59 138.6 36.84 NS ∗∗ NS ∗∗∗ TG (mg/dL) after 6 mo 118.2 37.37 106.55 33.12 127.85 38.32 NS ∗∗ NS ∗∗∗ HDL= high-density lipoprotein, LDL= low density lipoprotein, NS= non-significant, SD= standard deviation, TG= triglycerides. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. Table 6 Postoperative changes in C-reactive protein. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P CRP (mg/L) after 1 mo 8.21 12.57 7.4 6.16 8.43 6.17 NS ∗∗ ∗∗∗ NS CRP (mg/L) after 3 mo 6.11 6.52 8.85 10.33 7.41 5.45 NS ∗∗ ∗∗∗ NS CRP (mg/L) after 6 mo 5.45 6.11 6.39 6.7 6.53 3.84 NS ∗∗ ∗∗∗ NS CRP= C-reactive protein, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. 7 Hady et al. Medicine (2018) 97:4 Medicine [14] weight loss. Mongol et al reach %EWL around 41% with digested food than in resection which started 6cm from the [15] bougie size 32Fr, while Han et al observe 72% of weight loss pylorus. Therefore, an insulin secretion, HOMA-IR and total with bougie size 48Fr. cholesterol level were lower in 2cm approach. Surprisingly, It is a well-known fact that dysfunction of carbohydrates HbA1c level was significantly higher in Group III (40Fr), when system, diabetes mellitus inclusive, is highly related with obesity resection started 2cm from the pylorus. This might be explained [16] and lack of physical activity. Ninety percent of diabetes by resection of the different number of cells which produce [17] mellitus type 2 patients are obese or overweight. We have ghrelin, but also by the negative correlation between BMI and [31] found that LSG improves glycemic profile, insulin concentration, ghrelin level. Group III was the only one, where correlation and HbA1c level, even before significant weight reduction. We between BMI and HbA1c was not observed, moreover BMI in have observed a gradual reduction in glucose concentration in this group was higher than in Group I and II, thus the production each studied group. HbA1c level was also decreased in every of ghrelin and influence on carbohydrates metabolism was lower. group, most noticeably in Group I and II, 3 months after the Different studies show that steatohepatitis accompanies 60% [32,33] surgery. The most significant reduction of insulin was observed 1 of obese adults and 55% of children. Standard abdominal month after the treatment in Group I. In further follow-up a ultrasound is characterized by low sensitivity and specificity in [34–36] statistically significant decrease was discovered, but not as detecting a steatohepatitis. Thus, in our study, we have dynamic as at the beginning. Similar changes in HOMA-IR were observed concentrations of AST and ALT in the blood. In every observed. We stated that the most noticeable reduction of insulin step of the study the liver enzymes were between laboratory resistance was in 1 month after the LSG, and then it normalized. reference range values. We did not find any statistically significant Rizzello et al observed HOMA-IR decrease in third postoperative differences in AST and ALT levels between the studied groups. day. Two weeks after the surgery he found that glucose, insulin, Obesity is connected with defects in metabolism of lipids, and HOMA-IR values were significantly lower than before the which result in higher risk of development of cardiovascular [18] [37] surgery and occurred before the noticeable weight loss. diseases. In our research, LSG improved all studied lipid [19] Similar results published Catoi et al where 7 days after the parameters. Total cholesterol, LDL, and TG values significantly LSG insulin resistance decrease was observed and it reached a decreased in all groups, but LDL values did not reach the statistically significant reduction at 30th day of the follow-up. laboratory reference range at the end of the study. 2 [38] Sharma et al studied a case of 49 years old male (BMI=59kg/m ) Vix et al present similar results. They obtained a short-term who after a LSG achieves a rapid (14 days) insulin concentration reduction of total cholesterol and LDL after the LSG, however, at decrease, moreover HOMA-IR reaches 4.6 compared with 18.82 the end of their study, the values were even higher than in the [39] preoperatively. preoperative period. Iannelli et al indicate statistically Improvement of carbohydrates system after the LSG is highly insignificant increase of total cholesterol and LDL 6 months [40] related with weight and fat tissue loss. Recent studies show that after the LSG. On the other hand, Zhang et al did not observe changes in metabolism of carbohydrates occur few days after the any changes in concentration of total cholesterol and LDL in [20] LSG. We believe that it is caused by neurohormonal changes patients who underwent LSG. It is hypothesized that normal of digestive tract. Resection of major part of the stomach results concentration of total cholesterol in obese patients might be a in removal of cells which produce ghrelin (mainly in fundus). consequence of changes in expression of the receptors, which are According to different studies, ghrelin level decreases about 40% responsible for lipids absorption. It may be also caused by [20–23] [41,42] to 50% in comparison with preoperative values. Reduction changes in gastrointestinal microbiota or viral infection. of ghrelin concentration decreases appetite, lowers glucose level, Important, but less known, is influence of leptin on increases insulin secretion, and improves insulin resistance. gluconeogenesis and lipolysis in fat tissue. Obesity is a state of Additional mechanism which explains process of better elevated concentration of leptin in the blood, at the same time, it [43] carbohydrates metabolism is regulation of incretin hormones. is related to tissue resistance to leptin. Influence of bariatric procedures on normalization of glucose In our study, HDL concentration significantly increased during level is explained by hindgut hypothesis, which holds that the follow-up, however, results before the third postoperative [40] [44] digestive system contents have faster contact with the distant month were unsatisfactory. Zhang et al and Wong et al intestine and it leads to increased GLP-1 (glucagon-like peptide 1) also indicated elevation of HDL values, however, the relation and PYY (protein YY) secretion. Physiology of this process was between changes of HDL and weight loss were not found. studied in RYGB (Roux-Y gastric bypass), however, in LSG it is Analysis of TG values, allows us to state that LSG decreases TG [8,24,25] still unclear. It is hypothesized that LSG results in faster concentration in the blood. The results were statistically [40] stomach emptying and rapid passage of not fully digested food significant. Zhang et al indicate similar conclusion; they also [26–28] through duodenum and proximal intestine. point out the fact that 22.2% of patients after LSG still need a Moreover, in postoperative period, a lower secretion of pharmacotherapy. hydrochloric acid in stomach is observed, which directly Nowadays, it is considered that fat tissue is responsible for enhances production of PYY and secretion of gastrin and homeostasis and plays an important role in human metabolism. [23] GLP-1. Karamanakos et al prove that after LSG, a PYY level Furthermore, adipose tissue macrophages, which are a source of [29] increases and ghrelin secretion is reduced. Basso et al observed pro- and antiinflammatory cytokines, seem to be relevant in a GLP-1 and PYY increase in early postoperative period which development of insulin resistance. Correlation between CRP and [30] confirms the results of Peterli et al. Rise of GLP-1 and PYY is BMI in obesity is well known. It was proved that weight loss [45,46] responsible for lower appetite, glucose level reduction, insulin results in CRP decrease. In our study, average CRP level resistance restoration, inhibition of glucagon secretion, and in was between the laboratory reference rate in every step of the consequence, inhibition of gluconeogenesis. These findings follow-up. Only in studied Group II and III reduction of CRP, 6 [44] explain different results between patients who underwent a months after the LSG, was statistically significant. Wong et al stomach resection 2 and 6cm from the pylorus. The 2cm starting observed statistically significant reduction of CRP connected with [39] line from the pylorus resulted in faster passage of not fully weight loss after LSG. Iannelli et al stated significant 8 Hady et al. Medicine (2018) 97:4 www.md-journal.com [7] Hady HR, Dadan J, Gołaszewski P, et al. Impact of laparoscopic sleeve correlation between CRP and development of metabolic gastrectomy on body mass index, ghrelin, insulin and lipid levels in 100 syndrome. obese patients. Wideochir Inne Tech maloinwazyjne 2012;7:251–9. The most serious complications of LSG are staple line leaks and [8] Langer FB, Reza Hoda MA, Bohdjalian A, et al. Sleeve gastrectomy and [47–49] bleeding, and occur in 1% to 3% of patients. Other gastric banding: effects on plasma ghrelin levels. Obes Surg 2005; 15:1024–9. complications include biliary complications, for example. acute [9] Hady HR, Dadan J, Luba M. The influence of laparoscopic sleeve pancreatitis which may occur in 9.4%, but also, stenosis, gastrectomy on metabolic syndrome parameters in obese patients in own abdominal abscess, pulmonary embolism, deep venous throm- material. Obes Surg 2012;22:13–22. [47,48,50,51] bosis may appear. However, according to the position [10] Alberti KG, Zimmet P, Shaw J. Metabolic syndrome—a new world-wide statement on sleeve gastrectomy as a bariatric procedure by definition. A Consensus Statement from the International Diabetes Federation. Diabet Med 2006;23:469–80. American Society for Metabolic and Bariatric Surgery (ASMBS), [11] Parikh M, Gagner M, Heacock L, et al. Laparoscopic sleeve gastrectomy: LSG is a preferred method of obesity treatment as a first-step does bougie size affect mean %EWL? Short-term outcomes. Surg Obes [52] management. In our study the complication rate was 2.5% Relat Dis 2008;4:528–33. (n=3). We have observed acute pancreatitis, bleeding from the [12] Yuval JB, Mintz Y, Cohen MJ, et al. The effect of bougie caliber on leaks and excess weight loss following laparoscopic sleeve gastrectomy. Is there first trocar site into the abdominal cavity and superficial an ideal bougie size? Obes Surg 2013;23:1685–91. thrombophlebitis of the lower extremity. All complications [13] Weiner RA, Weiner S, Pomhoff I, et al. Laparoscopic sleeve gastrectomy concerned female, who did not follow tobacco smoking – Influence of sleeve size and resected gastric volume. Obes Surg restrictions in the postoperative period. The acute pancreatitis 2007;17:1297–305. was successfully treated by fluid resuscitation, pain control, and [14] Mongol P, Chosidow D, Marmuse J. Laparoscopic sleeve gastrectomy as an initial bariatric operation for high risk patients: initial results in 10 nutritional support. To control the bleeding, the incision line was patients. Obes Surg 2005;15:1030–3. enlarged, the bleeding vessel was identified and coagulated. A [15] Han S, Kim W, Oh J. Results of laparoscopic sleeve gastrectomy (LSG) at venous inflammation was limited to the one superficial vein and it 1 year In morbidly obese Korean patients. Obes Surg 2005;15:1469–75. was less than 5cm, thus conservative treatment was applied and [16] Dixon JB, Zimmet P, ALberti KG, Rubino F. International Diabetes Federation Taskforce on Epidemiology and Prevention. Bariatric the symptoms disappeared in the next few days. Surgery: an IDF statement for obese type 2 diabetes. Surg Obes relat There were several limitations in the study. First of all, our Dis 2011;7:433–47. study had a 120 patients sample size, which could potentially [17] Mokdad AH, Ford ES, Bowman BA, et al. Prevalence of obesity, diabetes affect the accuracy of the analysis. Secondly, all patients were and obesity-related high risk factors. JAMA 2001;289:76–9. Caucasian and came from the one region of Poland, however the [18] Rizzello M, Abbatini F, Casella G, et al. Early postoperative insulin- resistance changes after sleeve gastrectomy. Obes Surg 2010;20:50–5. results were comparable with the worldwide literature. Finally, [19] Catoi AF, Parvu A, Mironiuc A, et al. Effects of sleeve gastrectomy in due to a very limited group of patients who underwent a follow- insulin resistance. 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[26] Rubino F. Is type 2 diabetes an operable intestinal disease? A provocative yet reasonable hypothesis. Diabetes Care 2008;31(Suppl 2):S290–6. [27] Scott WR, Batterham RL. Roux-en-Y gastric bypass and laparoscopic References sleeve gastrectomy: understanding weight loss and improvements in type [1] Obesity and overweight Fact sheet N°311. WHO. January 2015. 2 diabetes after bariatric surgery. Am J Physiol Regul Integr Comp Retrieved 2 February 2016. Physiol 2011;301:R15–27. [2] Bastard JP, Maachi M, Lagathu C, et al. Recent advances in relationship [28] Vigneshwaran B, Wahal A, Aggarwal S, et al. Impact of sleeve between obesity, inflammation and insulin resistance. Eur Cytokine gastrectomy on type 2 diabetes mellitus, gastric emptying time, Netw 2006;17:4–12. glucagon-like peptide 1 (GLP – 1), ghrelin and leptin in non-morbidly [3] Pucci G, Alcidi R, Tap L, et al. Sex- and gender-related prevalence, obese subjects with BMI 30 – 35kg/m2: a prospective study. 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Different surgical approaches in laparoscopic sleeve gastrectomy and their influence on metabolic syndrome

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Copyright © 2018 the Author(s). Published by Wolters Kluwer Health, Inc.
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Abstract

Obesity is a growing health, social, and economic issue and became an epidemic, according to recent report of World Health Organization. The only method with scientifically proved efficiency of body mass loss is a surgical treatment. Laparoscopic sleeve gastrectomy (LSG) is recently a leading method in metabolic surgery. There are no standards of operative technique for LSG so far. The influence of technique modification on metabolic effect has not been described clearly. The aim of this study was to evaluate metabolic effects in patients with morbid obesity who underwent various surgical approaches of LSG. The study included 120 patients who were randomly divided into 3 groups: Group I, where bougie size was 32French (Fr), Group II —36Fr and Group III—40Fr. Each group was divided into 2 subgroups, based on the distance of resection beginning from the pylorus—2 or 6cm. Statistical analysis of: body mass index (BMI), the Percentage of Excess Weight Loss (%EWL), the Percentage of Excess BMI Loss (%EBMIL), levels of glucose and insulin on an empty stomach, glycated hemoglobin (HbA1c), insulin resistance (Homeostatic Model Assessment of Insulin Resistance Index—HOMA-IR), aspartate transaminase (AST), alanine transaminase (ALT), total cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides (TG), and C-reactive protein (CRP) were under investigation. Statistically significant decrease in body mass, BMI, %EWL, %EBL, glucose, and insulin concentrations has been observed in all studied groups. It was the highest when the smallest calibration tube has been used (32Fr). Similar results were observed in HOMA- IR and HbA1c levels. Statistically significant decrease of total cholesterol, LDL, and TG concentrations have been observed. Significant increase of HDL in every group has been also noted. Postoperative CRP values were the lowest when the smallest bougie was used. LSG is effective method of obesity treatment. Metabolic effects of LSG are the most noticeable when a small bougie size is used. Abbreviations: %EBMIL = the Percentage of Excess BMI Loss, %EWL = the Percentage of Excess Weight Loss, ALT = alanine transaminase, ASMBS = American Society for Metabolic and Bariatric Surgery, AST = aspartate transaminase, BMI = body mass index, CRP = C-reactive protein, Fr = French, GLP-1 = glucagon-like peptide 1, HbA1c = glycated hemoglobin, HDL = high-density lipoprotein, HOMA-IR = Homeostatic Model Assessment of Insulin Resistance Index, LDL = low-density lipoprotein, LSG = laparoscopic sleeve gastrectomy, NAFLD = nonalcoholic fatty liver disease, PYY = peptide YY, RYGB = Roux-Y gastric bypass, TG = triglycerides. Keywords: bariatric surgery, bougie size, laparoscopic sleeve gastrectomy, metabolic syndrome 1. Introduction Editor: Yan Li. Funding: The study was funded by Medical University of Bialystok (grant no. N/ Obesity is a process of excessive fat accumulation in the body ST/ZB/15/002/1140). which results in homeostasis breakdown and causes biochemical The authors have no conflicts of interest to disclose. and physiological dysfunctions of tissues. Obesity also leads to a b the development of comorbidities such as hypertension, diabetes 1st Department of General and Endocrinological Surgery, Department of Endocrinology, Diabetology and Internal Medicine, Department of Emergency mellitus type 2, sclerosis, nonalcoholic fatty liver disease [1–4] Medicine and Disasters, Medical University of Bialystok, Bialystok, Podlaskie, (NAFLD), goat, obstructive sleep apnea, and tumors. Poland. Conservative treatment, which consists of diet, lifestyle Correspondence: Dawid Groth, Medical University of Bialystok, Bialystok, modification, cognitive behavioral therapy, and pharmacothera- Podlaskie, Poland (e-mail: dawidgroth@gmail.com). py, must be systematic and long-term. However, body weight loss Copyright © 2018 the Author(s). Published by Wolters Kluwer Health, Inc. [5] success rate does not exceed 10%. Due to unsatisfactory results This is an open access article distributed under the Creative Commons of aforementioned methods, surgical treatment has become Attribution License 4.0 (CCBY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. increasingly important. Obesity surgery is the most effective way [6] to long-term weight loss. Nowadays, among many surgical Medicine (2018) 97:4(e9699) approaches, laparoscopic sleeve gastrectomy (LSG) gains Received: 25 August 2017 / Received in final form: 13 December 2017 / Accepted: 2 January 2018 popularity, because of satisfactory weight loss and remission of comorbidities. Final effect of the therapy is a result of http://dx.doi.org/10.1097/MD.0000000000009699 1 Hady et al. Medicine (2018) 97:4 Medicine decreased stomach volume and, in consequence, lower food total cholesterol, HDL, LDL, and TG were evaluated in order to intake. Moreover, recent studies suggest that resecting a larger control changes in particular time points after the surgery. Rates part of the stomach (fundus and body), affects gastrointestinal of %EWL, %EBMIL, and HOMA-IR were calculated according tract peristalsis, neurohormonal system, and carbohydrate–fat to the following formulas: [7,8] balance. LSG has no established standards regarding the (1) %EWL=(preoperative weightfollow-up weight)/(preoper- diameter of the stomach left after the surgery. Recommendations ative weightideal weight)100 of surgical associations are a result of clinical reports and For ideal weight calculations, the Lorenz formulas were metaanalyses, however, there is still a lack of final agreement on used: the technique of LSG. The knowledge about the influence of Ideal female weight=(height in cm100)((height in surgical approach on patient metabolic response is still cm150)/2), incomplete. Ideal male weight=(height in cm100)((height cm The aim of this study was to analyze body weight, BMI, the 150)/4). Percentage of Excess Weight Loss (%EWL), the Percentage of (2) %EBMIL=(preoperative BMIfollow-up BMI)/(preopera- Excess BMI Loss (%EBMIL) in patients with morbid obesity who tive BMI25)100 underwent various surgical approaches of LSG: different (3) HOMA-IR=glucose level (mg/dL)insulin concentration diameter of bougie for stomach volume calibration and different (mU/L)/405; quotient >2.6 supported insulin resistance. distance of cut-off line from the pylorus. Levels of glucose and insulin on an empty stomach, glycated hemoglobin (HbA1c), All data were extracted from original sources to fields within an insulin resistance (Homeostatic Model Assessment of Insulin Excel (Microsoft, Redmond, WA) database. Data manipulation Resistance Index—HOMA-IR), aspartate transaminase (AST), and analysis was conducted using SPSS statistical software for alanine transaminase (ALT), total cholesterol, high-density Windows, version 21 (IBM SPSS, Chicago, IL). Selected lipoprotein (HDL), low-density lipoprotein (LDL), triglycerides demographic (age, weight, body mass index [BMI, kg/m ]) and (TG), and C-reactive protein (CRP) were also under investiga- surgical technique (bougie size and distance from pylorus) tion. variables were estimated using mean, SD, range, and the percentage of studies reporting on each variable. Comparison of 3 studied groups was performed using 2. Patients and methods ANOVA with post hoc Tukey test. Pairwise t test was used to The material consists of 120 patients hospitalized in 1st evaluate the statistical significance between the same groups in Department of General and Endocrinological Surgery, Medical the different periods of the follow-up (1, 3, and 6 months after the University of Bialystok, between 2012 and 2014 who underwent surgery). Pearson test was used to determine whether there were LSG in order to treat morbid obesity. Patients were divided into 3 any differences in the distribution of gender by reinforcement groups by the bougie size: Group I, where bougie size was 32 method. French (Fr), Group II—36Fr and Group III—40Fr. The bougie Statistical tests were 2-tailed and values of P<.05 were size was chosen randomly for each patient before the surgery. considered statistically significant. Each group was divided into 2 subgroups, based on the distance Pearson test was used to determine whether there were any of resection beginning from the pylorus—2 or 6cm. correlations between studied groups. Values of P<.05 were Criteria of qualification of patients to the surgery were considered statistically significant. All calculations were per- [9] described previously. All patients had met at least 3 criteria formed by professional statistician. necessary for the diagnosis of metabolic syndrome according to [10] the International Diabetes Federation. Follow-up of the level 3. Results of metabolic syndrome reduction was limited to 1 year. All patients provided written informed consent before the In all studied groups a statistically significant decrease in body study and additional written informed consent was obtained mass and BMI was observed. The highest weight loss was before the surgical procedure. This study was approved by the observed in Group I, where the smallest bougie was used (32Fr) Ethics Committee of the Medical University of Bialystok, Poland compared to Group II and Group III (Table 2). (No R-I-002/438/2014) in accordance with the guidelines of the Postoperative dynamics of weight and BMI loss were evaluated Helsinki Declaration. using %EWL and %EBMIL. During 6 months follow-up period, There were 76 female (63.3%) and 44 male (36.7%) patients in the most noticeable decrease of body weight and BMI was examined group. Average age was 43. Groups characteristics are observed in Group I. One month after the surgery, %EWL in shown in Table 1. Group I was 22.26%±8.25%, after 3 months was equal to One team of surgeons (1 operator and 2 assistants) performed 41.23±9.69%, and after 6 months reached 59.61±12.59%; the [9] all surgeries, according to the procedure described before. Cut- decrease was statistically significant (Table 2, Fig. 1). off line of the omentum reached upwards the left diaphragmatic BMI loss measured with %EBMIL was significantly lower in branch and downwards approximately 2 or 6cm from the all studied groups. One month after the surgery in Group I it was pylorus. The stomach was reduced to the bougie size 32, 36, or equal to 27.31±12.22%. In 3 months follow-up, it was 50.55± 40Fr (Group I, Group II, and Group III). Leak test was performed 15.3% and at the end of the observation period reached 72.99± with 5% glucose and air insufflation. Patients were discharged 21.08% (Table 2, Fig. 2). There were no statistically significant home in the second or third day after the surgery and were differences between 2 and 6cm cut-off lines start from the regularly examined by clinical dietician and surgeon during the pylorus. follow-up period. In our research, a glucose level was also measured and All patients were examined 1, 3, and 6 months after the compared with preoperative results. During 6 months follow-up, surgery. Fasting 10 to 12hours blood was taken for a clot tube statistically significant changes in glucose concentration in and then centrifuged until serum was obtained. Insulin, glucose, plasma have been observed in every stage of observation and 2 Hady et al. Medicine (2018) 97:4 www.md-journal.com Table 1 Patients characteristics before surgery (mean and SD). Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) P Age, y 41.25± 11.21 42.82± 8.79 45.38± 11.64 NS ∗∗ NS ∗∗∗ NS Sex, F/M 25/15 28/12 23/17 Body mass, kg 130.6± 25.73 135.96± 30.6 140.93± 25.12 NS ∗∗ NS ∗∗∗ NS BMI, kg/m 44.56± 7.88 47.82± 9.13 50.02± 7.15 NS ∗∗ ∗∗∗ NS Glucose, mg/dL 105.58± 31.11 113.65± 32.77 119.14± 33.15 NS ∗∗ ∗∗∗ NS Insulin, mU/mL 20.93± 13.83 22.48± 11.58 32.11± 24.41 NS ∗∗ ∗∗∗ NS HOMA-IR 5.6± 4.14 6.53± 4.55 9.61± 7.75 NS ∗∗ ∗∗∗ NS HbA1C, % 5.77± 0.69 5.89± 0.83 5.88± 0.47 NS ∗∗ NS ∗∗∗ NS ALT, IU/L 39.88± 42.92 31.63± 22.89 35.78± 18.08 NS ∗∗ NS ∗∗∗ NS AST, IU/L 32.05± 21.56 24.53± 12.53 26.4± 9.01 NS ∗∗ NS ∗∗∗ NS Total cholesterol, mg/dL 203.63± 31.62 208.2± 42.52 201.98± 37.97 NS ∗∗ NS ∗∗∗ NS LDL, mg/dL 143.2± 34.33 138.15± 43.22 134.83± 37 NS ∗∗ NS ∗∗∗ NS HDL, mg/dL 45± 11.62 50.43± 13.28 45.28± 12.74 NS ∗∗ NS ∗∗∗ NS TG, mg/dL 166.65± 86.9 154.95± 62.85 165.95± 72.76 NS ∗∗ NS ∗∗∗ NS CRP, mg/L 7.45± 7.08 9.55± 8.34 9.53± 7.78 NS ∗∗ NS ∗∗∗ NS ALT= alanine transaminase, AST= aspartate transaminase, BMI= body mass index, CRP= C-reactive protein, HDL= high-density lipoprotein, HOMA-IR= Homeostatic Model Assessment of Insulin Resistance Index, LDL= low-density lipoprotein, NS= non-significant, SD= standard deviation, TG= triglycerides. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. in all studied groups (Table 3). The highest decrease was observed Insulin and glucose concentrations allowed us to measure in Group I and II (Table 3). HOMA-IR. Reduction of insulin resistance was discovered in every All measurements of insulin concentration were also statisti- studied group, however in Group I it was the most noticeable (2.31± cally significant with a tendency to decrease in comparison to 1.43; Table 3, Fig. 3).Value of HOMA-IR was statistically significant preoperative values (Table 3). The greatest reduction in in every stage of observation. Moreover, a 2cm cut-off line from the concentration of insulin in serum was observed 1 month after pylorus approach was related to lower HOMA-IR 1 month after the the surgery. Three and 6 months postoperatively, the values also LSG in Group I (1.907 compared with 2.718; P=.007) and 3 months decreased, but less dynamically. However, the results were after the surgery in Group II (1.248 vs 2.109; P=.018). statistically significant in every stage of the study. Resection 2cm Our study revealed statistically significant decrease in HbA1c from the pylorus resulted in more dynamic decrease of insulin in studied Group I and II, 3 months after the surgery (5.32± concentration than 6cm approach—1 month after the surgery in 0.51% and 5.32±0.45%) and 6 months after the surgical Group I (respectively, 8.415 and 11.53mU/mL) and 3 months treatment (5.25±0.34 and 5.19±0.46) (Table 3, Fig. 4). after the treatment in Group II (5.842 and 8.785mU/mL). Additionally, high correlation between weight (R=0.52; 3 Hady et al. Medicine (2018) 97:4 Medicine Table 2 Postoperative changes in body weight, BMI, %EWL and %EBMIL. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P Body weight (kg) after 1 mo 116.29 23.69 121.99 25.31 125.63 23.86 NS ∗∗ ∗∗∗ NS Body weight (kg) after 3 mo 104.05 22.19 108.76 22.59 114.68 22.76 NS ∗∗ ∗∗∗ NS Body weight (kg) after 6 mo 91.96 19.39 96.01 21.64 102.53 22.91 NS ∗∗ ∗∗∗ NS BMI (kg/m ) after 1 mo 39.67 7.36 42.94 7.75 44.58 6.85 .017 ∗∗ ∗∗∗ NS BMI (kg/m ) after 3 mo 35.47 6.78 38.28 6.89 40.72 6.82 .019 ∗∗ <.001 ∗∗∗ NS BMI (kg/m ) after 6 mo 31.34 5.9 33.8 6.72 36.39 6.98 .031 ∗∗ <.001 ∗∗∗ NS %EWL after 1 mo 22.26 8.25 18.92 6.89 20.09 6.21 .036 ∗∗ NS ∗∗∗ NS %EWL after 3 mo 41.23 9.69 36.81 11.71 34.5 8.67 NS ∗∗ ∗∗∗ NS %EWL after 6 mo 59.61 12.59 54.73 14.61 36.39 6.98 NS ∗∗ ∗∗∗ NS %EBMIL after 1 mo 27.31 12.22 22.27 8.76 22.76 7.29 .017 ∗∗ ∗∗∗ NS %EBMIL after 3 mo 50.55 15.3 43.32 14.88 40.72 6.82 .027 ∗∗ <.001 ∗∗∗ NS %EBMIL after 6 mo 72.99 21.08 64.5 19.07 57.25 15.66 NS ∗∗ ∗∗∗ NS BMI= body mass index, %EBMIL= the Percentage of Excess BMI Loss, %EWL= the Percentage of Excess Weight Loss, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. P=.0006) and BMI (R=0.46; P=.0026) before and 6 months Group III the relationship was not calculated. However, in this after the surgery (R=0.42; P=.007 vs R=0.34; P=.034) and study Group, the 2cm starting line from the pylorus resulted in HbA1c was observed. In Group II weight and BMI correlated statistically significant higher HbA1c level compared to the 6cm with HbA1c only before the surgery (R=0.47; P=.002). In approach (3 months after the surgery, 5.69% and 5.2%; Figure 1. Changes of %EWL 1, 3, and 6 months after the surgery. Figure 2. Changes of %EBMIL 1, 3, and 6 months following the LSG. 4 Hady et al. Medicine (2018) 97:4 www.md-journal.com Table 3 Postoperative changes in carbohydrate metabolism. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P Glucose (mg/dL) after 1 mo 91.8 10.37 94.9 16.85 101.5 16.26 NS ∗∗ ∗∗∗ Glucose (mg/dL) after 3 mo 91.15 9.25 90.23 10.42 97.1 9.13 NS ∗∗ ∗∗∗ Glucose (mg/dL) after 6 mo 90.03 6.01 89.38 9.3 94.45 7.74 NS ∗∗ ∗∗∗ Insulin (mU/mL) after 1 mo 9.97 5.64 10.79 5.88 16 9.76 NS ∗∗ ∗∗∗ Insulin (mU/mL) after 3 mo 8.68 5.11 7.31 4.06 11.47 6.6 NS ∗∗ ∗∗∗ Insulin (mU/mL) after 6 mo 6.76 4.56 5.98 3.69 9.22 5.8 NS ∗∗ ∗∗∗ <.001 HOMA-IR after 1 mo 2.31 1.43 2.67 1.89 4.21 3.24 NS ∗∗ ∗∗∗ HOMA-IR after 3 mo 2.01 1.37 1.68 1.12 2.8 1.79 NS ∗∗ ∗∗∗ <.001 HOMA-IR after 6 mo 1.52 1.13 1.36 0.98 2.2 1.55 NS ∗∗ ∗∗∗ <.001 HbA1c (%) after 1 mo 5.63 0.77 5.53 0.65 5.71 0.41 NS ∗∗ NS ∗∗∗ NS HbA1c (%) after 3 mo 5.32 0.51 5.32 0.45 5.57 0.34 NS ∗∗ ∗∗∗ HbA1c (%) after 6 mo 5.25 0.34 5.19 0.46 5.43 0.33 NS ∗∗ ∗∗∗ HbA1c= glycated hemoglobin, HOMA-IR= Homeostatic Model Assessment of Insulin Resistance Index, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. P= .022). In 6 months follow-up, the values were 5.58% (2 cm significantly decreased 6 months after the LSG in all studied from the pylorus) and 5.28% (6 cm); P= .004. groups (Table 4, Fig. 5). Our study did not show any abnormalities in AST and ALT We have also studied the effect of LSG on lipid profile of obese levels in obese patients. We observed that ALT concentration patients. During the follow-up, statistically significant decrease in Figure 3. Changes of HOMA-IR 1, 3, and 6 months after the surgery. Figure 4. Changes of HbA1c 1, 3, and 6 months after the surgery. 5 Hady et al. Medicine (2018) 97:4 Medicine Table 4 Postoperative changes in transaminases. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P ALT (IU/L) after 1 mo 39.95 37.23 32.9 15.71 42.08 28.2 NS ∗∗ NS ∗∗∗ NS ALT (IU/L) after 3 mo 23.2 10.22 21.8 9.33 27.35 13.41 NS ∗∗ NS ∗∗∗ NS ALT (IU/L) after 6 mo 17.83 6.85 14.88 5.64 20.85 9.69 .036 ∗∗ NS ∗∗∗ <.001 AST (IU/L) after 1 mo 35.68 24.37 27.1 10.1 32.9 18.89 NS ∗∗ NS ∗∗∗ NS AST (IU/L) after 3 mo 23 10.22 21.8 9.33 27.35 13.41 NS ∗∗ NS ∗∗∗ NS AST (IU/L) after 6 mo 17.5 5.96 16.25 3.5 17.43 5.66 NS ∗∗ NS ∗∗∗ NS ALT= alanine transaminase, AST= aspartate transaminase, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. total cholesterol level in all studied group was observed, however, We have stated a statistically significant decrease in TG in all the reduction was the most dynamic in Group I (Table 5). studied groups, 3 and 6 months postoperatively (Table 5). Analyzing the differences in surgical approach, patients after 2cm Our study also included an evaluation of CRP concentration in resection from the pylorus reached statistically lower levels of plasma. Average level was between reference ranges in all studied total cholesterol than patients in whom the resection started 6cm groups during the whole follow-up, however, CRP values in from the pylorus (177.7mg/dL vs 192.7mg/dL; P=.028). Group I were statistically lower in comparison to Group III in Only at the beginning of the follow-up period the reduction of every stage of the study (Table 6). LDL was statistically significant in all studied groups (126.1± The complication rate in our study group was 2.5% (n=3). 36.29mg/dL vs 125.5±48.14mg/dL vs 126.03±34.78mg/dL) The complications were: acute pancreatitis (0.83%), bleeding compared to the preoperative values (Table 5). from the first trocar site into the abdominal cavity (0.83%) and Changes in HDL level occurred 3 months after the LSG and it superficial thrombophlebitis of the lower extremity (0.83%). raised in all studied groups (data not statistically significant), however, 6 months after the surgery, HDL values significantly 4. Discussion increased in every group (Table 5). In patients who underwent LSG LSG has many advantages such as simplicity of the technique and with 2cm cut-off line from the pylorus, where the bougie size was short operative time (short anesthesia and less postoperative 40Fr (Group III), a significant increase in HDL, 3 and 6 months complications). LSG approach does not need any bypass after the surgery, was observed in comparison to the patients after anastomosis, so the physiological passage of gastrointestinal 6cm resection (after 3 months—52.7mg/dL vs 44.25mg/dL; tract is not interrupted. P=.015 and 6 months—58.05mg/dL vs 46.9mg/dL; P=.002). Our study reveals that the highest BMI and body weight reduction occurs when the smallest bougie size is used (32Fr vs 36Fr vs 40Fr). The decrease was significantly higher in studied Group I compared with Group III. Six months after the surgery in studied Group I patients lost 59.61% of their preoperative weight and 72.99% of BMI (measured with %EWL and %EBMIL). [8] Langer et al obtained similar results. In their study, %EWL in 6 months follow-up was 61.4%±16.3, although the bougie size [11] was 48Fr. Parikh et al observed that differences in %EWL were around 40% between studied groups (40Fr vs 60Fr), however, the results were not statistically significant. It is worth mentioning, that bougie sizes more than 40Fr are rarely used. [12] Yuval et al compared two LSG approaches with different bougie sizes (<40Fr vs ≥40Fr) and stated no statistically significant differences in %EWL between the groups. Unsatisfactory weight loss forces surgeons to change the [13] surgical technique for more restrictive. There is still lack of Figure 5. Changes of triglycerides 1, 3, and 6 months after the LSG. evidence that smaller bougie size is related to more intensive 6 Hady et al. Medicine (2018) 97:4 www.md-journal.com Table 5 Postoperative changes in lipid profile parameters. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P Total cholesterol (mg/dL) after 1 mo 179.35 26.75 181.53 46.16 184.65 35.61 NS ∗∗ NS ∗∗∗ NS Total cholesterol (mg/dL) after 3 mo 189 30.15 186.53 40.46 184.1 30.28 NS ∗∗ NS ∗∗∗ NS Total cholesterol (mg/dL) after 6 mo 182.3 33.61 194.6 47.1 185.15 27.66 NS ∗∗ NS ∗∗∗ NS LDL (mg/dL) after 1 mo 126.1 35.29 125.5 48.14 126.03 34.78 NS ∗∗ NS ∗∗∗ NS LDL (mg/dL) after 3 mo 137 32.77 127.38 41.56 126.35 31.09 NS ∗∗ NS ∗∗∗ NS LDL (mg/dL) after 6 mo 135.68 34.25 133.1 47.5 127 28.49 NS ∗∗ NS ∗∗∗ NS HDL (mg/dL) after 1 mo 38.7 9.41 42.75 11.16 43.03 11.46 NS ∗∗ NS ∗∗∗ NS HDL (mg/dL) after 3 mo 47.05 12.48 49.25 12.97 48.48 11.01 NS ∗∗ NS ∗∗∗ NS HDL (mg/dL) after 6 mo 54.03 18.96 56.13 14.16 52.48 12.27 NS ∗∗ NS ∗∗∗ NS TG (mg/dL) after 1 mo 148.35 52.79 127.78 39.4 152.13 50.16 NS ∗∗ NS ∗∗∗ TG (mg/dL) after 3 mo 135.55 49.3 121.48 38.59 138.6 36.84 NS ∗∗ NS ∗∗∗ TG (mg/dL) after 6 mo 118.2 37.37 106.55 33.12 127.85 38.32 NS ∗∗ NS ∗∗∗ HDL= high-density lipoprotein, LDL= low density lipoprotein, NS= non-significant, SD= standard deviation, TG= triglycerides. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. Table 6 Postoperative changes in C-reactive protein. Group I (32 Fr) Group II (36 Fr) Group III (40 Fr) Mean SD Mean SD Mean SD P CRP (mg/L) after 1 mo 8.21 12.57 7.4 6.16 8.43 6.17 NS ∗∗ ∗∗∗ NS CRP (mg/L) after 3 mo 6.11 6.52 8.85 10.33 7.41 5.45 NS ∗∗ ∗∗∗ NS CRP (mg/L) after 6 mo 5.45 6.11 6.39 6.7 6.53 3.84 NS ∗∗ ∗∗∗ NS CRP= C-reactive protein, NS= non-significant, SD= standard deviation. Statistically significant differences between studied Group I and II. ∗∗ Statistically significant differences between studied Group I and III. ∗∗∗ Statistically significant differences between studied Group II and III. 7 Hady et al. Medicine (2018) 97:4 Medicine [14] weight loss. Mongol et al reach %EWL around 41% with digested food than in resection which started 6cm from the [15] bougie size 32Fr, while Han et al observe 72% of weight loss pylorus. Therefore, an insulin secretion, HOMA-IR and total with bougie size 48Fr. cholesterol level were lower in 2cm approach. Surprisingly, It is a well-known fact that dysfunction of carbohydrates HbA1c level was significantly higher in Group III (40Fr), when system, diabetes mellitus inclusive, is highly related with obesity resection started 2cm from the pylorus. This might be explained [16] and lack of physical activity. Ninety percent of diabetes by resection of the different number of cells which produce [17] mellitus type 2 patients are obese or overweight. We have ghrelin, but also by the negative correlation between BMI and [31] found that LSG improves glycemic profile, insulin concentration, ghrelin level. Group III was the only one, where correlation and HbA1c level, even before significant weight reduction. We between BMI and HbA1c was not observed, moreover BMI in have observed a gradual reduction in glucose concentration in this group was higher than in Group I and II, thus the production each studied group. HbA1c level was also decreased in every of ghrelin and influence on carbohydrates metabolism was lower. group, most noticeably in Group I and II, 3 months after the Different studies show that steatohepatitis accompanies 60% [32,33] surgery. The most significant reduction of insulin was observed 1 of obese adults and 55% of children. Standard abdominal month after the treatment in Group I. In further follow-up a ultrasound is characterized by low sensitivity and specificity in [34–36] statistically significant decrease was discovered, but not as detecting a steatohepatitis. Thus, in our study, we have dynamic as at the beginning. Similar changes in HOMA-IR were observed concentrations of AST and ALT in the blood. In every observed. We stated that the most noticeable reduction of insulin step of the study the liver enzymes were between laboratory resistance was in 1 month after the LSG, and then it normalized. reference range values. We did not find any statistically significant Rizzello et al observed HOMA-IR decrease in third postoperative differences in AST and ALT levels between the studied groups. day. Two weeks after the surgery he found that glucose, insulin, Obesity is connected with defects in metabolism of lipids, and HOMA-IR values were significantly lower than before the which result in higher risk of development of cardiovascular [18] [37] surgery and occurred before the noticeable weight loss. diseases. In our research, LSG improved all studied lipid [19] Similar results published Catoi et al where 7 days after the parameters. Total cholesterol, LDL, and TG values significantly LSG insulin resistance decrease was observed and it reached a decreased in all groups, but LDL values did not reach the statistically significant reduction at 30th day of the follow-up. laboratory reference range at the end of the study. 2 [38] Sharma et al studied a case of 49 years old male (BMI=59kg/m ) Vix et al present similar results. They obtained a short-term who after a LSG achieves a rapid (14 days) insulin concentration reduction of total cholesterol and LDL after the LSG, however, at decrease, moreover HOMA-IR reaches 4.6 compared with 18.82 the end of their study, the values were even higher than in the [39] preoperatively. preoperative period. Iannelli et al indicate statistically Improvement of carbohydrates system after the LSG is highly insignificant increase of total cholesterol and LDL 6 months [40] related with weight and fat tissue loss. Recent studies show that after the LSG. On the other hand, Zhang et al did not observe changes in metabolism of carbohydrates occur few days after the any changes in concentration of total cholesterol and LDL in [20] LSG. We believe that it is caused by neurohormonal changes patients who underwent LSG. It is hypothesized that normal of digestive tract. Resection of major part of the stomach results concentration of total cholesterol in obese patients might be a in removal of cells which produce ghrelin (mainly in fundus). consequence of changes in expression of the receptors, which are According to different studies, ghrelin level decreases about 40% responsible for lipids absorption. It may be also caused by [20–23] [41,42] to 50% in comparison with preoperative values. Reduction changes in gastrointestinal microbiota or viral infection. of ghrelin concentration decreases appetite, lowers glucose level, Important, but less known, is influence of leptin on increases insulin secretion, and improves insulin resistance. gluconeogenesis and lipolysis in fat tissue. Obesity is a state of Additional mechanism which explains process of better elevated concentration of leptin in the blood, at the same time, it [43] carbohydrates metabolism is regulation of incretin hormones. is related to tissue resistance to leptin. Influence of bariatric procedures on normalization of glucose In our study, HDL concentration significantly increased during level is explained by hindgut hypothesis, which holds that the follow-up, however, results before the third postoperative [40] [44] digestive system contents have faster contact with the distant month were unsatisfactory. Zhang et al and Wong et al intestine and it leads to increased GLP-1 (glucagon-like peptide 1) also indicated elevation of HDL values, however, the relation and PYY (protein YY) secretion. Physiology of this process was between changes of HDL and weight loss were not found. studied in RYGB (Roux-Y gastric bypass), however, in LSG it is Analysis of TG values, allows us to state that LSG decreases TG [8,24,25] still unclear. It is hypothesized that LSG results in faster concentration in the blood. The results were statistically [40] stomach emptying and rapid passage of not fully digested food significant. Zhang et al indicate similar conclusion; they also [26–28] through duodenum and proximal intestine. point out the fact that 22.2% of patients after LSG still need a Moreover, in postoperative period, a lower secretion of pharmacotherapy. hydrochloric acid in stomach is observed, which directly Nowadays, it is considered that fat tissue is responsible for enhances production of PYY and secretion of gastrin and homeostasis and plays an important role in human metabolism. [23] GLP-1. Karamanakos et al prove that after LSG, a PYY level Furthermore, adipose tissue macrophages, which are a source of [29] increases and ghrelin secretion is reduced. Basso et al observed pro- and antiinflammatory cytokines, seem to be relevant in a GLP-1 and PYY increase in early postoperative period which development of insulin resistance. Correlation between CRP and [30] confirms the results of Peterli et al. Rise of GLP-1 and PYY is BMI in obesity is well known. It was proved that weight loss [45,46] responsible for lower appetite, glucose level reduction, insulin results in CRP decrease. In our study, average CRP level resistance restoration, inhibition of glucagon secretion, and in was between the laboratory reference rate in every step of the consequence, inhibition of gluconeogenesis. These findings follow-up. Only in studied Group II and III reduction of CRP, 6 [44] explain different results between patients who underwent a months after the LSG, was statistically significant. Wong et al stomach resection 2 and 6cm from the pylorus. The 2cm starting observed statistically significant reduction of CRP connected with [39] line from the pylorus resulted in faster passage of not fully weight loss after LSG. Iannelli et al stated significant 8 Hady et al. Medicine (2018) 97:4 www.md-journal.com [7] Hady HR, Dadan J, Gołaszewski P, et al. Impact of laparoscopic sleeve correlation between CRP and development of metabolic gastrectomy on body mass index, ghrelin, insulin and lipid levels in 100 syndrome. obese patients. Wideochir Inne Tech maloinwazyjne 2012;7:251–9. The most serious complications of LSG are staple line leaks and [8] Langer FB, Reza Hoda MA, Bohdjalian A, et al. Sleeve gastrectomy and [47–49] bleeding, and occur in 1% to 3% of patients. Other gastric banding: effects on plasma ghrelin levels. Obes Surg 2005; 15:1024–9. complications include biliary complications, for example. acute [9] Hady HR, Dadan J, Luba M. The influence of laparoscopic sleeve pancreatitis which may occur in 9.4%, but also, stenosis, gastrectomy on metabolic syndrome parameters in obese patients in own abdominal abscess, pulmonary embolism, deep venous throm- material. Obes Surg 2012;22:13–22. [47,48,50,51] bosis may appear. However, according to the position [10] Alberti KG, Zimmet P, Shaw J. 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Medicine – Wolters Kluwer Health

Published: Jan 1, 2018

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