The impact of bariatric surgery on nutritional status of patients

Introduction

According to World Health Organization data from 2012, over half of the European Union population is overweight and 17% is obese [1]. According to the results of WOBASZ, a study conducted in Poland between 2003 and 2005, the percentage of obese men was 21.2% and that of obese women was 22.4%; among them morbid obesity (body mass index (BMI) > 40 kg/m²) was respectively 0.6% and 2.2% [2]. Conservative treatment of patients with morbid obesity is inefficient, which is why surgical treatment is necessary. Surgical treatment is recommended for patients between 18 and 60 years old with BMI ≥ 40 kg/m² or BMI ≥ 35 kg/m² with co-morbidities connected with obesity, in which a surgically induced effect of body mass reduction would lead to their recovery. According to available data from 2011, 340 768 bariatric procedures have been performed worldwide. The most frequently performed procedures were Roux-en-Y gastric bypass (RYGB) (46.6%), sleeve gastrectomy (SG) (27.8%), adjustable gastric banding (AGB) (17.8%) and biliopancreatic diversion/duodenal switch (BPD/DS) (2.2%) [3]. It is estimated that in Poland 1200 bariatric operations are performed per year [3]. Although bariatric treatment is associated with the occurrence of complications resulting from the procedure or from nutritional insufficiencies, it leads to significant body mass reduction and metabolic improvement of obese patients.

Aim

The aim of the study was to evaluate changes in nutritional status and selected biochemical parameters of blood of patients after surgical treatment of obesity in the early postoperative period – the first 6 months after the surgery.

Material and methods

The study included 50 patients – 30 women (average age 38.8 ±8.9) and 20 men (average age 47.6 ±12.1) after surgical treatment of obesity. Sixty-five percent of patients underwent laparoscopic sleeve gastrectomy (LSG) and 35% underwent RYGB.
All bariatric procedures (SG and gastric bypass) were performed laparoscopically by one panel of surgeons including one operator and two assistants. Both operations were performed with the patient in Fowler’s position at approximately 30° by using 5 trocars: 2 × 13 mm, 2 × 10 mm, 1 × 5 mm. 
Laparoscopic sleeve gastrectomy lasted approximately 64 min. This procedure particularly included cutting of the gastrocolic omentum near the wall of the stomach 4–6 cm from the pylorus to the left diaphragmatic branch. The size of the stomach was limited to the tube with diameter of 34–36 Fr and next 4–5 linear staplers of different colors (Echelon, EndoGIA) were applied.
The gastric bypass procedure lasted approximately 78 min and involved creating a 20 ml pouch from the upper part of the stomach using linear staplers. Furthermore, a nutritional loop of approximately 120–150 cm was created and connected with the stomach using a 45 mm linear stapler, and next the enzymatic loop of 60 cm was connected with the nutritional loop using a 45 mm linear stapler.
At the end of both procedures the tightness was checked with the methylene blue test and a drain was placed in the peritoneal cavity.
After surgery (SG and gastric bypass) on the second or third day patients were discharged home and remained under the control of a clinical dietician and out-patient clinic. A low-calorie diet was the main recommendation. However, in the first 2 weeks after the procedure a low-sodium, semi-liquid diet was recommended, followed by a low-fat and low-carbohydrate diet.
The criteria to include patients in the study were: age 18–64 years, BMI ≥ 40 kg/m² or BMI ≥ 35 kg/m² with co-morbidities connected with obesity. The exclusion criteria were: cardio-respiratory failure, gastrointestinal tract neoplasms and pregnancy. During the preliminary visit (1 day before the surgery) and during control visits (1, 3 and 6 months after the surgery) the evaluation of nutritional status (body mass, BMI, waist and hip circumference, body content) and selected biochemical blood parameters was conducted.
Body mass (with an accuracy of 0.1 kg) and body height (with an accuracy of 0.1 cm) were determined using a medical weighing scale with a RADWAG WPT 100/200 OW stadiometer (patients dressed in light outerwear, without shoes). Waist circumference (at the height of the navel) and hip circumference were measured using a tape measure. Using the Lorentz formula, ideal body weight was established for each patient [women’s ideal body weight = height in cm – 100 – (height in cm – 150)/2; men: ideal body weight = height in cm – 100 – (height in cm – 150/4]. Furthermore, the percentage of excess weight loss (%EWL) was determined %EWL = [(preoperative weight – current weight)/(preoperative weight – ideal weight) × 100] in every examined period (1, 3 and 6 months after the surgery) [4].
Assessment of body content was conducted using the method of bioelectrical impedance. The content of fat tissue (kg and % of body mass), fat-free body mass (kg and % of body mass) and water (liters and % of body mass), muscle mass (kg) and value of resting metabolic rate (kcal/day) were estimated using the analyzer of body content BioScan 920, Maltron International Ltd.
Biochemical blood assays, such as complete blood count (erythrocytes, leucocytes, hemoglobin, blood platelets), lipids (total, low-density lipoprotein (LDL) and high-density lipoprotein (HDL) cholesterol, triglycerides), urine acid (uric acid???), fasting glucose, insulin and C-reactive protein (CRP), were conducted in diagnostic laboratories of the University Hospital in Bialystok. As norms, standard ranges of referential values were adopted.
The study obtained the consent of the Bioethical Committee of the Medical University of Bialystok no. R-I-002/525/2010. Each patient signed voluntarily consent to participate in the study.

Statistical analysis

Statistical analysis of data (mean values, standard deviation, minimum and maximum values) was conducted using Statistica 10. Results of examinations performed before the surgery were compared with results obtained 1, 3 and 6 months after the surgery. To compare results in particular periods, Student’s t-test for independent samples was used. Results where p ≤ 0.05 were assumed to be statistically significant.

Results

The study included 50 obese patients – 30 women (average age 38.8 ±8.9 years) and 20 men (average age 47.6 ±12.1 years) treated surgically. Body mass in women before the surgery was between 82 kg and 169.9 kg (average 120.66 ±21.24 kg) and BMI between 36.7 kg/m² and 72.6 kg/m² (average 44.55 ±9.73 kg/m²). In the group of men, body mass before the surgery was between 130 kg and 175 kg (average 142.83 ±28.41 kg) and BMI was 38,3–60,5 kg/m² (average 47.75 ±9.78 kg/m²). Average waist circumference of examined women was 130.96 ±20.48 cm and examined men 146.33 ±17.96 cm. In women, average hip circumference before the surgery was 137.46 ±14.53 cm and in men it was 137.08 ±17.90 cm. Average body mass, average waist and hip circumference and average BMI in women decreased significantly 3 and 6 months after the surgery. Results are presented in Table I. In the case of men, mean values of aforementioned parameters also decreased but differences were statistically insignificant (Table II).
In this study, percentage of excess weight loss (%EWL) in patients 1, 3 and 6 months after the surgery was determined. In women %EWL was 19.74 ±6.98% 1 month after the surgery, 33.97 ±12.47% 3 months after the surgery and 47.43 ±16.67% 6 months after the surgery, and in men it was 22.38 ±6.65% 1 month after the surgery, 34.49 ±10.69% 3 months after the surgery and 45.53 ±16.83% 6 months after the surgery. Analysis of body content of patients before the surgery revealed a high percentage of fat tissue (women average 50.79 ±5.24%, men average 41.28 ±7.93%), which in women was significantly reduced 3 months after the surgery (44.37 ±6.39%), and after 6 months (41.93 ±8.31%). In the case of men the reduction of fat tissue was respectively 36.01 ±7.66% and 35.30 ±11.20%. In both examined groups, the percentage of fat-free body mass increased. In women fat-free body mass before the surgery was 49.20 ±5.24%; 3 months (55.62 ±4.60%) and 6 months (57.51 ±16.55%) after the surgery a statistically significant (p ≤ 0.05) increase of fat-free body mass was observed. In men an increase of fat-free body mass was also observed from 58.72 ±7.93% before the surgery to 66.55 ±9.41% 6 months after the surgery. Despite a beneficial proportion of fat-free mass (FFM) in comparison to fat mass (FM), a statistically significant loss of fat-free mass was observed in women, from 58.44 ±5.73 kg before the surgery to 53.68 ±5.07 kg 6 months after the surgery. An adverse effect was observed in both groups concerning loss of muscle mass. In women muscle mass was reduced 3 months after the surgery (23.54 ±2.36 kg), and after 6 months (22.79 ±2.45 kg). In men average muscle mass before the surgery was 39.20 ±8.00 kg and after 6 months it decreased to 35.69 ± 5.11 kg. What is more, 6 months after the surgery, an increase of total content of water in the body was observed – in women from 40.94 ±3.87% to 45.29 ±4.19% (p ≤ 0.05) and in men from 47.23 ±5.69% to 51.75 ±7.14%. Results are presented in Tables I and II.
In the present study, both groups revealed a significant decrease in average fasting glucose concentration, average fasting insulin concentration 3 and 6 months after the surgery and average triglycerides concentration 6 months after the surgery (Figure 1). Results of remaining biochemical blood parameters (excluding HDL cholesterol), such as LDL cholesterol (Figure 2), concentration of erythrocytes and leukocytes, blood platelets and hemoglobin, also showed decreases during 6 months after the surgery, but the differences were statistically insignificant. Average concentration of total cholesterol in serum periodically fluctuated (Figure 3). In the first month after the surgery, concentration of cholesterol in women decreased from 197.64 ±21.20 mg/dl to 164.69 ±37.01 mg/dl, and in men from 192.67 ±28.63 mg/dl to 169.67 ±31.19 mg/dl, and 3 months after the surgery it reached 184.07 ±28.30 mg/dl in women and 180.67 ±31.38 mg/dl in men. However, average values of evaluated parameters 1, 3, and 6 months after the surgery were within the standard. Evaluation of HDL cholesterol concentration in serum revealed a decrease 1 month after the surgery (women average from 51.14 ±11.01 mg/dl to 42.46 ±11.79 mg/dl; men average from 40.83 ±8.20 mg/dl to 35.33 ±6.68 mg/dl) and then a gradual increase 3 months (women average 47.14 ±8.91 mg/dl, men average 39.83 ±8.06 mg/dl) and 6 months after the surgery (women average 54.07 ±12.42 mg/dl; men average 43.17 ±7.49 mg/dl) (Figure 4). In both groups, an increase of serum uric acid concentration was observed 1 month after the surgery and a decrease 3 and 6 months after the surgery. In the case of CRP, a decrease of its average concentration to normal values was observed 6 months after the surgery (in women average concentration 3.11 ±6.25 mg/l, in men average concentration 3.7 ±3.06 mg/l). Results of laboratory tests are presented in Tables III and IV.

Discussion

In the literature, there is a constantly increasing amount of data regarding high and long-term efficiency of bariatric surgery in treatment of morbid obesity [5, 6]. Efficiency of surgical treatment of obesity is evaluated mainly by percentage of excess weight loss (%EWL) and changes in BMI. The surgical procedure is considered to be successful when after 5 years the loss of ≥ 50% of excess body mass is obtained [7]. Available publications indicate that weight loss as %EWL during 3–6 years after the surgery is 25–65% after laparoscopic adjustable gastric banding (LAGB) 66–68% after SG and 53–77% after RYGB [5, 6]. In this study, percentage of excess weight loss in the early postoperative period (first 6 months) was determined. In women the average was 47.43 ±16.67% and in men it was 45.53 ±16.83%. As the available data suggest, in patients after SG %EWL was 35–49% 6 months after the surgery [8–12]. Six months after RYGB, %EWL was higher and amounted to 56–64% [13, 14]. Higher %EWL was connected with the fact that RYGB, unlike gastrectomy, is a mixed procedure. It means that despite the considerable limitation of consumed food, it also limits the absorption of nutrients, mainly carbohydrates, which are the main source of energy.
It would be the most beneficial if the loss of excess body weight was caused only by the reduction of fat tissue. According to Christensen, maximum content of fat tissue in the body of healthy women should be 35% of body mass and in the case of men 22% [15]. In the present study, in the group of women statistically significant reduction of fat tissue was observed 3 and 6 months after the surgery. Similar results were obtained by Bavaresco et al., but they examined only patients after RYGB [16]. In our own study, in women average content of fat tissue 6 months after the surgery was 41.93 ±8.31% and in men it was 35.3 ±11.20%. In the study by de Freitas Junior, the percentage of fat tissue in the body was 38.67 ±7.86 [17]. Significant reduction of body mass and fat tissue after bariatric procedures suggests the efficiency of the applied procedure. It should be noted that in the period of intensive body mass loss, also fat-free body mass is reduced, including muscles (approximately 50%), soft tissues, bones and collagen [17]. Fat-free body mass is an important component of lost body mass after a bariatric procedure, especially during the first 6 months after the surgery [18]. In our study, average loss of fat-free body mass in women was 9.42 ±1.48%, and in men it was 11.68 ±10.81%. In the examination conducted among 36 obese patients after open gastric bypass, significant, over 19%, loss of fat-free body mass was observed 6 months after the surgery [17]. As Chaston et al. suggest in their review article, fat-free body mass may be even 31.3% of lost body mass in patients after RYGB [19]. In order to prevent excessive loss of fat-free body mass, optimal supply of protein and regular physical activity should be ensured [20, 21]. According to Heber et al. and Moize et al., protein supply 1.5 g/kg of ideal body weight may help to maintain a positive nitrogen balance and thus prevent loss of fat-free body mass [22, 23].
An indisputable advantage of bariatric surgery is the possibility of improvement of metabolic balance in obese patients (improved metabolism of insulin, glucose and lipids). Only 3 months after the surgery, concentration of glucose and triglycerides in serum significantly decreases [24]. In our study, 3 months after the surgery a significant decrease in fasting glucose and insulin concentration was seen in both groups. The level of triglycerides did not decrease substantially until 6 months after the surgery. Similar results were obtained by other authors [16, 25–28]. In a prospective cohort study including 15 patients after RYGB, a significant decrease in serum concentration of insulin and LDL cholesterol 6 months after the surgery was observed [29]. Auguet et al. 6 months after laparoscopic sleeve gastrectomy noted a significant reduction of glucose, insulin, triglycerides and CRP concentration and an increase of serum HDL cholesterol concentration [30]. What is more, they proved that lowering of triglycerides concentration with a simultaneous increase of serum HDL cholesterol raises the risk of cardiovascular diseases. This risk significantly drops 12 months after the surgery [30]. Similar results were obtained by Ruiz-Tovar et al. [24].
A substantial role in arteriosclerosis pathogenesis and ischemic heart disease is also played by the inflammatory state connected with obesity (especially of visceral tissue) [31]. One of the active agents of the inflammatory reaction is CRP [32]. C-reactive protein is synthesized in the liver mainly as a response to interleukin 6 (IL-6) [31]. Based on values of serum CRP, the risk of cardiovascular incidents is estimated. According to the American Heart Association and the Centers for Disease Control and Prevention, low risk occurs when CRP < 1 mg/l, moderate when CRP is 1–3 mg/l and high when CRP > 3 mg/l [33]. One study proved that elevated level of CRP was positively correlated with BMI, concentration of glucose, total cholesterol, triglycerides and uric acid and negatively correlated with concentration of serum HDL cholesterol [34]. In this study, concentration of CRP > 3 mg/l was proved in 77% of patients qualified for surgical treatment. Six months after the surgery this percentage fell to 31.6%. In the study of Hakeam et al., before sleeve gastrectomy, CRP concentration exceeded 3 mg/l in 89.6% of obese patients [35]. Six months after the surgery CRP concentration had normalized in approximately 50% (44% of all examined patients) with high CRP [35].
Bariatric procedures, especially malabsorptive, may lead to insufficiencies in macro- and micronutrients. A deficit of protein, iron, vitamin B12 and folic acid manifests mainly in lowering of the number of erythrocytes and hemoglobin concentration. Furthermore, a deficit in folic acid and vitamin B12 causes disturbances in deoxyribonucleic acid synthesis, amino acids and bone proteins and hence leads to a decrease of the number of leukocytes and blood platelets. In the study of Coupane, average concentration of hemoglobin 6 months after sleeve gastrectomy was 13.5 ±1.3 g/dl and after gastric bypass 13.1 ±1.0 g/dl [25]. Blume et al. observed that 6 months after RYGB average concentration of hemoglobin was 13.0 ±1.1 g/dl [36]. Obtained values are comparable with the results obtained in this study.

Conclusions

Bariatric procedures support a significant reduction of body mass, BMI, and waist and hip circumference. Body mass loss is caused mainly by the reduction of fat tissue in the body. Due to application of surgical methods in treatment of morbid obesity, improvement of insulin, glucose and lipid metabolism has been achieved, which may influence the possibility of resolution of the symptoms resulting from metabolic disorders or cardiovascular diseases. What is more, in the early postoperative period, anemia, which may be the result of insufficient supply of iron in the diet, was not observed.

Acknowledgments

Grant holder of “Studies, research, commercialization – a support programme of UMB doctoral students” Sub-measure 8.2.1 Human Capital Operational Programme, co-financed from the European Union under the European Social Fund.

References

1. Health at a glance: Europe 2012. Available from: http://ec.europa.eu/health/reports/european/health_glance_2012_en.htm
2. Biela U, Pająk A, Kaczmarczyk-Chałas K, et al. Częstość występowania nadwagi i otyłości u kobiet i mężczyzn w wieku 20–74 lat. Wyniki programu WOBASZ. Kardiol Pol 2005; 63 (Suppl. 4): 632-35.
3. Buchwald H, Oien DM. Metabolic/bariatric surgery worldwide 2011. Obes Surg 2013; 24: 427-36.
4. Deitel M, Gawdat K, Melissa J. Reporting weight loss 2007. Obes Surg 2007; 17: 565-8.
5. Musella M, Milone M, Gaudioso D, et al. A decade of bariatric surgery. What have we learned? Outcome in 520 patients from a single institution. Int J Surg 2014; 12 Suppl. 1: S183-8. 
6. Mechanick JI, Kushner RF, Sugerman HJ, et al. American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery Medical guidelines for clinical practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Endocr Pract 2008; 14 (Suppl. 1): 1-83.
7. Szczęsny W, Gniłka W, Dąbrowiecki S, Reśliński A. Rola chirurgii w leczeniu otyłości patologicznej. Co lekarz rodzinny wiedzieć powinien? Nowa Medycyna 2009; 3: 173-7.
8. Zerrweck C, Sepúlveda EM, Maydón HG, et al. Laparoscopic gastric bypass vs. sleeve gastrectomy in super obese patients: early outcomes of an observational study. Obes Surg 2014; 24: 712-7.
9. Milone L, Strong V, Gagner M. Laparoscopic sleeve gastrectomy is superior to endoscopic intragastric balloon as first stage procedure for super-obese patients (BMI > or + 50). Obes Surg 2005; 15: 612-7.
10. Hady HR, Dadan J, Gołaszewski P, Safiejko K. Impact of laparoscopic sleeve gastrectomy on body mass index, grelin, insulin and lipid levels in 100 obese patients. Videosurgery Miniinv 2012; 7: 251-59.
11. Lehmann A, Bobowicz M, Lech P, et al. Comparison of percentage excess weight loss after laparoscopic sleeve gastrectomy and laparoscopic adjustable gastric banding. Videosurgery Miniinv 2014; 9: 351-6.
12. Bužga M, Holéczy P, Švagera Z, et al. Effects of sleeve gastrectomy on parameters of lipid and glucose metabolism in obese women – 6 months after operation. Videosurgery Miniinv 2013; 8: 22-8.
13. Moize V, Andreu A, Flores L, et al. Long-term dietary intake and nutritional deficiencies following sleeve gastrectomy or Roux-en-Y gastric bypass in a Mediterranean population. J Acad Nutr Diet 2013; 113: 400-10.
14. Soares FL, Bissoni de Sousa L, Corradi-Perini C, et al. Food quality in the late postoperative period of bariatric surgery: an evaluation using the bariatric food pyramid. Obes Surg 2014; 24: 1481-6.
15. Christensen K, Kushner R. Measuring body fat in the clinical setting. Obes Manag 2007; 3: 93-5.
16. Bavaresco M, Paganini S, Lima TP, et al. Nutritional course of patients submitted to bariatric surgery. Obes Surg 2010; 20: 716-21.
17. de Freitas Junior WR, Ilias EJ, Kassab P, et al. Assessment of the body composition and the loss of fat-free mass through bioelectric impedance analysis in patients who underwent open gastric bypass. Sci World J 2014; 2014: 843253. doi: 10.1155/2014
/843253
18. Santarpia L, Contaldo F, Pasanisi F. Body composition changes after weight-loss interventions for overweight and obesity. Clin Nutr 2013; 32: 157-61.
19. Chaston TB, Dixon JB, O’Brien PE. Changes in fat-free mass during significant weight loss: a systematic review. Int J Obes 2007; 5: 743-50.
20. de Aquino LA, Pereira SE, de Souza Silva J, et al. Bariatric surgery: impact on body composition after Roux-en-Y gastric bypass. Obes Surg 2012; 22: 195-200.
21. Vatier C, Henegar C, Ciangura C, et al. Dynamic relations between sedentary behavior, physical activity, and body composition after bariatric surgery. Obes Surg 2012; 22: 1251-6.
22. Heber D, Greenway FL, Kaplan LM, et al. Endocrine and nutritional management of the post-bariatric surgery patient: an Endocrine Society Clinical Practice Guideline. J Cin Endocrinol Metab 2010; 11: 4823-43.
23. Moizé V, Geliebter A, Gluck ME, et al. Obese patients have inadequate protein intake related to protein intolerance up to 1 year following Roux-en-Y gastric bypass. Obes Surg 2003; 13: 23-8.
24. Ruiz-Tovar J, Oller I, Galindo I, et al. Change in levels of C-reactive protein (CRP) and serum cortisol in morbidly obese after laparoscopic sleeve gastrectomy. Obes Surg 2013; 23: 764-9.
25. Coupaye M, Riviére P, Breuil MC, et al. Comparison of nutritional status during the first year after sleeve gastrectomy and Roux-en-Y gastric bypass. Obes Surg 2014; 24: 276-83.
26. Pedrosa IV, Burgos MG, Souza NC, Morais CN. Nutrition aspects in obese before and after bariatric surgery. Rev Col Bras Cir 2009; 36: 316-22.
27. Sirbu A, Copăescu C, Martin S, et al. Six months results of laparoscopic sleeve gastrectomy in treatment of obesity and its metabolic complications. Chirurgia (Bucur) 2012; 4: 469-75.
28. Proczko M, Kaska Ł, Kobiela J, et al. Roux-en-Y gastric bypass in dialysed morbidly obese patients as a preparation for a kidney transplantation: case series. Videosurgery Miniinv 2013; 8: 174-7.
29. Brethauer SA, Heneghan HM, Eldar S, et al. Early effects of gastric bypass on endothelial function, inflammation, and cardiovascular risk in obese patients. Surg Endosc 2011; 25: 2650-9.
30. Auguet T, Terra X, Hernández M, et al. Clinical and adipocytokine changes after bariatric surgery in morbidly obese women. Obesity 2014; 22: 188-94.
31. Chen JY, Chou CH, Tsai WC, et al. Effects of increased systemic inflammation and central obesity on arterial stiffness in patients with nonalcoholic fatty liver disease. J Am Soc Hypertens 2012; 6: 253-60.
32. Ridker PM. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 2003; 107: 363-9.
33. Pearson TA, Mensah GA, Alexander RW, et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 2003; 107: 499-511.
34. Fröhlich M, Imhof A, Berg G, et al. Association between C-reactive protein and features of the metabolic syndrome: a population-based study. Diabetes Care 2000; 23: 1835-9.
35. Hakeam HA, O’Regan PJ, Salem AM, et al. Inhibition of C-reactive protein in morbidly obese patients after laparoscopic sleeve gastrectomy. Obes Surg 2009; 19: 456-60.
36. Blume CA, Boni CC, Casagrande DS, et al. Nutritional profile of patients before and after roux-en-Y-gastric bypass: 3-year follow-up. Obes Surg 2012; 22: 1676-85.

Received: 22.09.2014, accepted: 18.11.2014.