ORIGINAL

 

Evolution of nutritional, hematologic and biochemical changes in obese women during 8 weeks after Roux-en-Y gastric bypasss

Evolución de los cambios nutricionales, hematológicos y bioquímicos en mujeres obesas durante 8 semanas después de bypass gástrico en Y de Roux

 

 

V. Custódio Afonso Rocha¹, L. Ramos de Arvelos², G. Pereira Felix¹, D. Nogueira Prado de Souza¹, M. Bernardino Neto², E. Santos Resende¹ and N. Penha-Silva²

¹Faculdade de Medicina. Universidade Federal de Uberlândia. Uberlândia. MG. Brasil
²Instituto de Genética e Bioquímica. Universidade Federal de Uberlândia. MG. Brasil

Correspondence

 

 

---

ABSTRACT

Obesity is a chronic disease of multifactorial origin and currently is a serious public health problem. The treatment of morbid obesity can be effectively done by bariatric surgery. The present study aimed to evaluate the influence of changes in food intake on body composition and some hematologic and biochemical variables in the period of eight weeks after Roux-en-Y gastric bypass (RYGB). The study included 22 women submitted to RYGB. We evaluated anthropometric, nutritional, hematologic and biochemical variables before and 14, 28, 42 and 56 days after surgery. The patients showed a decrease in caloric intake and hence macro- and micronutrients, with significant loss of weight and decrease in body mass index (BMI). Decreases in body weight and BMI were associated with reduced blood levels of total cholesterol, VLDL-C, LDL-C, triglycerides and glucose with time after surgery. The decrease in caloric intake was also associated with decreased intake of protein, iron and calcium, with a decline in hemoglobin, hematocrit and red blood count, and RDW increased after surgery.

Key words: Bariatric surgery. Gastric bypass. Obesity. Weight loss. Nutrition.

---

RESUMEN

La obesidad es una enfermedad crónica de origen multifactorial y actualmente es un problema grave de salud pública. El tratamiento de la obesidad mórbida puede hacerse eficazmente por la cirugía bariátrica. El presente estudio tuvo como objetivo evaluar la influencia de los cambios en la ingesta de alimentos sobre la composición corporal y algunas variables hematológicas y bioquímicas en el plazo de ocho semanas después de bypass gástrico en Y de Roux (BGYR). El estudio incluyó a 22 mujeres sometidas a BGYR. Se evaluaron los parámetros antropométricos, nutricionales, bioquímicos antes de la operación y el 14^o, 28^o, 42^o e 56^o día después de la cirugía. Los pacientes mostraron cambios significativos en la ingesta de alimentos, con una disminución en la ingesta de calorías y por lo tanto, los macro y micronutrientes, con una pérdida significativa de peso y disminución del índice de masa corporal (IMC). La disminución en el peso corporal y el IMC se asoció con niveles reducidos de colesterol total, VLDL-C, LDL-C, triglicéridos y glucosa con el tiempo después de la cirugía. La disminución de la ingesta calórica también se asoció con disminución de la ingesta de proteínas, hierro y calcio, con una disminución en la hemoglobina, el hematocrito y el recuento de glóbulos rojos, y RDW aumentado después de la cirugía.

Palabras clave: Cirugía bariátrica. Bypass gástrico. Obesidad. Pérdida de peso. Nutrición.

---

 

Introduction

Obesity is a chronic, heterogeneous and multifactorial disease, resulting from an imbalance between energy intake and energy consumed. Currently, it is considered a major public health problem in developed countries due to the increase of its prevalence and the fact that it is associated with several diseases such as hypertension (HBP), diabetes mellitus (DM), arthropathies, dyslipidemia, respiratory insufficiencies and coronary heart disease, among others.¹ Obesity is considered by itself a cardiovascular risk factor, besides being the main risk factor for type 2 diabetes.^2,3

Bariatric surgery is considered an effective strategy for weight loss in morbid obesity.⁴ Among the various types of bariatric surgery there is the technique of Roux-en-Y gastric bypass (RYGB), which has been considered the most effective procedure^5,6 and therefore is the most widely used in Brazil. This type of surgery provides a satisfactory loss of weight excess, in addition to the concomitant improvement of comorbidities and quality of life.^7,8,9

RYGB surgery also results in changes in nutritional status of the patient. Limiting the intake of food due to restriction of stomach capacity, along with the direct passage of food to the jejunum, results in decreased intake and absorption of some nutrients. However, there are still few studies that address the changes in food intake of macro-and micronutrients and their relationship to hematologic and biochemical changes to which are subject patients undergoing RYGB, particularly in the short term. Within this context, this study aims to evaluate the influence of these changes at different times after surgery to RYGB.

 

Material and methods

This study followed the ethical standards of the Declaration of Helsinki and was approved by the Ethics Committee in Research of the Federal University of Uberlândia, Brazil. Each participant signed a consent form.

We conducted a prospective observational study with 22 women candidates for bariatric surgery in the Obesity Center of Uberlândia (CENTROBESO), of which 15 had morbid obesity and 7 had class II obesity. All patients underwent RYGB surgery, in line with inclusion and exclusion criteria for surgery as the consensus of surgery for morbid obesity.¹⁰

Anthropometric parameters (weight, BMI), clinical history (comorbidities, medication use), and hematologic and biochemical variables (total cholesterol and fractions, triglycerides and fasting glucose) of the patients were evaluated before and 14, 28, 42 and 56 days after surgery. Blood samples for hematologic and biochemical tests were collected after an overnight fast of 12 hours.

The patients were instructed regarding the changes in eating habits after surgery, especially regarding the quantity and nutritional quality of food eaten. The postoperative diet consisted of four phases according with the nutritional protocol of CENTROBESO: 1) liquid diet (21 days), 2) soft diet (7 days), 3) semi-solid diet (15 days) and 4) solid diet (final). All patients were advised to make use of multivitamin-mineral supplementation and iron (50 mg of elemental iron daily) after 15 days of surgery.

Dietary intake was assessed using three food records made in two midweek days and in one weekend day, at different times (before surgery and in the four phases of the diet after surgery). For the nutritional analysis of food records and macronutrients (carbohydrates, proteins and lipids) and micronutrients (iron and calcium), we used the software Virtual Nutri Plus^a (VirtualNutri +, São Paulo, SP, Brazil). Statistical analysis was performed using the application OriginPro 8.0 (Microcal Inc., Northampton Massachusetts, USA).

The numerical results were evaluated for distribution through the Kolmogorov-Smirnov test. The results were expressed as mean and standard deviation (SD). The correlations between changes in variables were tested using Pearson's correlation, with P < 0.05 indicating statistically significant relationships.

 

Results

The average age of the population was 37.91 ± 9.13 years. The mean body weight of patients before surgery was 115.25 ± 15.59 kg and mean BMI was 44.28 ± 5.45 kg/m². The evolution of body weight, weight loss, excess weight loss (EWL) and BMI of patients undergoing the RYGB at different times is shown in table I.

Of the 22 volunteers, six (27.3%) had impaired fasting glucose (100-125 mg/dL), one (4.5%) was classified as diabetic (≥ 126 mg/dL) and 15 (68.2%) had normal preoperative glucose (70-99 mg/dL).¹¹ After 56 days of surgery, only one patient had impaired fasting glucose (4.5%) and the remaining 21 patients (95.5%) had normal fasting glucose.

In relation to blood cholesterol, 22 volunteers from 11 (50%) had elevated cholesterol (≥ 240 mg/dL), 9 (40.9%) had borderline cholesterol (200-239 mg/dL) and 2 (9.1%) had cholesterol levels within desirable levels before surgery (< 200 mg/dL).¹² On 56 day after surgery, only one volunteer (4.5%) had high cholesterol, 3 (13.6%) had borderline cholesterol and 18 (81.8%) had normal cholesterol. The levels of HDL-C were lower than recommended (< 40 mg/dL) before the procedure in 6 (27.3%) and desirable in 16 (72.7%) of the volunteers (≥ 40 mg/dL).¹² After 14 days of surgery, the HDL-C levels were low in 19 (86.4%) and desirable in 3 (13.6%) of the volunteers. But 56 days after surgery the levels of HDL-C remained below the recommended in 9 (40.9%) and within the recommended values in 13 (59.1%) of the volunteers.

Before surgery, triglyceride levels were high (201499 mg/dL) in four (18.2%), borderline (150-200 mg/dL) in 8 patients (36.4%) and optimum (<150 mg/dL) in 10 (45.5%) of the volunteers.¹² At 56 days after surgery, levels of triglycerides were borderline in 5 (22.7%) and optimum in 17 (77.3%) of the volunteers.

The simple correlation analysis between anthropometric, hematologic and biochemical variables with time of surgery were statistically significant, except for HDL-C, MCHC, MCH and MCV, as shown in table II.

After bariatric surgery, patients showed significant changes in food intake, with decreased caloric intake and, therefore, of macronutrients (fig. 1) and micronutrients (fig. 2).

 

Discussion

With the increase in the incidence of obesity and the failure of noninvasive methods for promoting weight loss and its maintenance, bariatric surgery has become an effective strategy for the treatment of morbid obesity, and consequently for the improvement of comorbidities and quality of life of the patient.

The RYGB promotes a reduction in body weight due to decreased energy intake. The weight loss supports the biochemical changes associated with structural and functional homeostasis of the organism, such as the improvement in glycemic control. The reduction in body weight also leads to biochemical and hematologic changes that affect the supply and demand of O₂ in the tissues (fig. 3).

 

In this prospective study conducted with 22 women submitted to RYGB, patients experienced a significant loss of body weight and, therefore, of BMI, during the period evaluated.

The prevalence of type 2 diabetes is attributable to overweight and obesity in more than 95% of cases.¹³ Several studies show that the risk of developing this disease increases with increasing body weight. Indeed, in a population of 46 subjects with morbid obesity, Ocon and colleagues¹⁴ found 67.3% of patients with insulin resistance before RYGB, but no patients with this clinical condition after surgery.

The results of this study showed a prevalence of 27.3% of patients with impaired fasting glucose (100-125 mg/dL) and 4.5% of diabetic patients (≥ 126 mg/dL) in the population studied. It is worth mentioning that the size of this population was lower when compared to other studies in the literature.^15,16,17

The results also showed that half of the patients had higher than desirable cholesterol (≥ 240 mg/dL), 27.3% had HDL-C levels below recommended levels (< 40 mg/dL) and 18.2% had triglycerides above the value of reference (201-499 mg/dL). These values were close to the frequencies of 53 of hypercholesterolemia and 18.6% of hypertriglyceridemia reported by Cercato and colleagues¹⁸ in a population of 412 obese women with 42.9 ± 13.4 years in São Paulo.

In the preoperative period was observed average intakes of 1,845.47 ± 526.33 kcal/day, 231.06 ± 80.01 g/day (50.1%) of carbohydrates, 86.45 ± 24.94 g/day (18.7%) of proteins and 64.15 ± 26.33 g/day (31.3%) of lipids. These data are similar to values of 1,608 ± 752 kcal/day, 219.3 ± 111.6 g/day (54.5%) of carbohydrates, 69.1 ± 27.4 g/day (17.7%) of proteins and 48.8 ± 30.0 g/day (26.8%) of lipids, reported by Carrasco and colegas¹⁹ for a population of 23 women with BMI of 44.5 ± 3.7 prior to the RYGB.

The reduced caloric intake found before surgery can be partly explained by subnotification of food consumption by patients or even because they were following nutritional guidelines they had before the study.

The change in diet after the surgery leads to a drastic reduction in the ingestion of calories and hence also of macro- and micronutrients. As might be expected due to the surgical procedure, in the present study there was a reduction in caloric intake and thus lower intake of proteins, lipids, carbohydrates and micronutrients. 14 days after surgery, the liquid diet provided to patients an average intake of 375.92 ± 103.03 kcal/day, 56.2 ± 17.52 g/day of carbohydrates, 23.12 ± 7.50 g/day protein and 7.16 ± 3.84 g/day of lipids.

In the present study there was a progressive increase in caloric intake with the time of surgery. About two months after surgery, the patients took an average of 617.82 ± 116.17 kcal/day of energy, 82.21 ± 19.24 g/day of carbohydrates, 36.26 ± 9.30 g/day of proteins and 17.46 ± 5.93 g/day of lipids. Dias and colleagues,²⁰ assessing the food intake of 40 women with three months of surgery, found an average intake of 529.4 ± 47.5 kcal/day of energy.

The results presented in figures 1 and 2 show that the mean energy intake was significantly larger before than at all times after surgery. However, there was a significant increase in the average caloric intake between the 14^th and 56^th days after surgery. Although the average intake of macronutrients (carbohydrates, proteins and lipids) after surgery was significantly lower than in the preoperative period, there was a significant increase in the average intake of proteins in the 56^th postoperative day when compared with the 14^th and 28^th days after surgery. The average intake of iron and calcium decreased significantly postoperatively. However, the average intake of iron showed a significant increase between the 28^th and 56^th days postoperatively.

Several studies show that there is a progressive increase in food intake after surgery.^19,20,21 The diet in the immediate postoperative period has a very low calorie content that increases slowly over the months. But even after a year of surgery, most patients remain with intakes of calories and proteins much smaller than those recommended.

Dietary proteins are important for promoting satiety and maintenance of lean body mass in weight loss,²² although it is questionable the role of protein-rich diet to prevent weight regain in patients undergoing RYGB.²³

The intake of 60-120 g of protein daily is recommended for the maintenance of lean body mass during the loss of weight.²² Protein intakes in the assessed periods were below the recommended levels in the current study, as well as in other published studies,^19,21 which makes necessary the supplementation of this nutrient. The low protein intake, especially in the first month after surgery is due to intolerance for foods, especially meat, and to the small amount of food ingested.^21,24

There was a gradual increase in energy intake with the time of surgery, as well as the intake of lipids, as previously described. After 56 days of surgery, there was an average intake of 17.5 g of lipids, which corresponds to 25.4% of the caloric intake. Brolin and colleagues²⁵ found 31% and 34% of caloric intake in lipids 6 and 12 months after surgery, respectively. The lower intake of lipids found in the present study can be due to the period analyzed, when patients still have a more restrictive diet.

Recent guidelines for nutritional support for patients undergoing bariatric surgery do not recommend a specific ratio of carbohydrates in the diet. Observational studies show an intake of approximately 45% of carbohydrates.^26,27 The higher average consumption of carbohydrates (50,1%) observed in this study can be explained by period of time considered, as in the first months after surgery carbohydrates predominate in the diets.

In this study, we also evaluated the intake of the micronutrients calcium and iron. Calcium intake was far below the recommendation for the age group of volunteers, which is 1 g/day,²⁸ both before (517.4 mg/day) and 56 days after surgery (343.2 mg/day).

A study by Campos²⁹ found an average calcium intake of 525.5 mg/day in a population consisting of 40 women after more than eight years of RYGB. These data show that low calcium intake continues in the long term.

With respect to iron, there was an ingestion of this mineral below the 18 mg/day recommended³⁰ for the age range of the volunteers, especially in the first month after surgery. In this study, all patients were advised to make use of complex of vitamins and minerals, prescribed at hospital discharge.

Regarding hematologic variables considered in this study, there was a decrease in hemoglobin, hematocrit and red blood count, but increase in RDW, with time after surgery.

Several studies show a significant improvement in lipid profile after bariatric surgery, including lowering triglycerides and LDL-C and increased HDL-C.¹³ The relations of the biochemical variables with time after surgery showed the occurrence of decline in triglycerides, total cholesterol, VLDL-C and LDL-C and also in the blood levels of glucose.

In the preoperative stage of the study, one patient was classified as diabetic and six patients had impaired fasting glucose, but 56 days after surgery there was significant decline in blood glucose and only one patient, one previously diagnosed as diabetic, had impaired fasting glucose.

Observational studies show an improvement in glycemic control in a few days after surgery.³¹ According to Cummings,³² this acute improvement could not be attributed to weight loss and nor to the improvement in insulin resistance.

A study by Lim and colleagues,³³ in which 11 volunteers with diabetes underwent a severe dietary restriction, reported normalization of fasting glucose and sensitivity to insulin after eight weeks of energy restriction.

The negative energy balance that occurs immediately after surgery may explain the normalization of blood glucose due to the reduction of glucotoxicity on pancreatic cells.³⁴ The glucotoxicity, characterized by chronic effects of hyperglycemia on the pancreatic beta cell function, leads to decreased glucose tolerance due to exhaustion of these cells and reduction of its mass by apoptosis.³⁵

After surgery, patients gradually increase the ingestion of calories. However, concomitant weight loss occurs, which leads to improved glucose tolerance. This improvement is due to increased sensitivity to insulin, with decreasing glucotoxicity, lipotoxicity on pancreatic beta cells.³² The lipotoxicity, resulting from high levels of fatty acids for prolonged periods, results in a reduction of beta cell responsiveness to blood levels of glucose.^35,36

Another mechanism that may act in the reversal of hyperglycemia in association with low energy intake involves a set of changes in the release of gastrointestinal hormones, such as reduced production of ghrelin and elevation of serum GLP1.³⁷

In summary, the remission of hyperglycemia after RYGB surgery should be the result of a combination of factors such as low-calorie diet associated with weight loss, and changes in production and/or sensitivity to the action of gastrointestinal hormones and own insulin.³⁸

 

Conclusions

Data from this study show that patients undergoing RYGB presented declines in body weight and BMI in the study period. These results were associated with a reduction in calorie intake, with decreased blood levels of total cholesterol, VLDL-C, LDL-C, triglycerides and glucose after surgery. Although the decrease in energy intake has meant an improvement in obesity-related comorbidities, it was also associated with decreased intake of proteins and iron, with a reduction in hemoglobin, hematocrit and red blood count, and RDW increased after the RYGB procedure, even with supplementation of vitamins and minerals after 15 days of surgery.

 

References

1. Austin H, Austin JMJr, Partridge EE, Hatch KD, Shingleton HM. Endometrial cancer, obesity and body fat distribution. Cancer Res 1991; 51: 568-72.         [ Links ]

2. Formigueira X, Cantón A. Obesity: epidemiology and clinical aspects. Best Pract Res Clin Gastroenterol 2004; 18: 1125-46.         [ Links ]

3. Buchwald H, Estok R, Fahrbach K, Banel D, Jensen MD, Pories WJ et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med 2009; 122: 248-56.         [ Links ]

4. Shikora AS. Techniques and procedures: surgical treatment for severe obesity: the state-of-the-art for new millenium. Nutr Clin Pract 2000; 15: 13-22.         [ Links ]

5. Rico Hernández M^a A, Martínez Sancho E, Armero Fuster M, Díaz Gómez J, Calvo Viñuela I. Comparación a 5 años de dos técnicas de cirugía bariátrica en pacientes con obesidad mórbida seguidos en consulta enfermera. Nutr Hosp 2009; 24:667-75.         [ Links ]

6. Camberos-Solis R, Jiménez-Cruz A, Bacardí-Gascón M, Culebras JM. Efectividad y seguridad a largo plazo del bypass gástrico en "Y" de Roux y de la banda gástrica: revisión sistemática. Nutr Hosp 2010; 25: 964-70.         [ Links ]

7. Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K et al. Bariatric surgery: a systematic review and meta-analysis. JAMA 2004; 292: 1724-37.         [ Links ]

8. Barreto Villela N, Braghrolli Neto O, Lima Curvello K, Eduarda Paneili B, Seal C, Santos D et al. Quality of life of obese patients submitted to bariatric surgery. Nutr Hosp 2004; 19: 367-71.         [ Links ]

9. Martínez Y, Ruiz-López MD, Giménez R, Pérez de la Cruz AJ, Orduña R. Does bariatric surgery improve the patient's quality of life? Nutr Hosp 2010; 25: 925-30.         [ Links ]

10. National Institutes of Health Consensus Development Conference Panel. Gastrointestinal surgery to severe obesity. Ann Inter Med 1991; 115: 956-61.         [ Links ]

11. The expert Committee on Diagnosis and Classification of Diabetes: follow-up on diagnosis of Diabetes Mellitus. Diabetes Care 2003; 26: 3160-67.         [ Links ]

12. National Institutes of Health, Third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation and treatment of high blood cholesterol in adults (Adult Treatment Panel III); 2002: Publication (NIH 02-5215).         [ Links ]

13. Bouldin MJ, Ross LA, Sumrall CD, Loustalot FV, Low AK, Land KK. The effect of obesity surgery on obesity comorbidity. Am J Med Sci 2006; 331: 183-93.         [ Links ]

14. Ocón J, García B, Benito P, Gimeno S, García R, López P. Efecto del bypass gástrico en el síndrome metabólico y en riesgo cardiovascular. Nutr Hosp 2010; 25: 67-71.         [ Links ]

15. Malerbi DA, Franco LJ. Multicenter study of the prevalence of diabetes mellitus and impaired glucose tolerance in the urban Brazilian population aged 30-69 yr. Diabetes Care 1992; 15:1509: 16.         [ Links ]

16. Porto MCV, Brito IC, Calfa ADF, Amoras M, Villela NB, Araújo LMB. Perfil do obeso classe III do ambulatório de obesidade de um hospital universitário de Salvador, Bahia. Arq Bras Endocrinol Metab 2002; 46: 668-73.         [ Links ]

17. Ruano Gil M, Silvestre Teruel V, Aguirregoicoa García E, Criado Gómez L, Duque López Y, García-Blanch G. Nutrición, síndrome metabólico y obesidad mórbida. Nutr Hosp 2011; 26:759-64.         [ Links ]

18. Cercato C, Silva S, Sato A, Mancini M, Halpern A. Risco cardiovascular em uma população de obesos. Arq Bras Endocrinol Metab 2000; 44: 45-48.         [ Links ]

19. Carrasco F, Rojas P, Ruz M, Rebolledo A, Codoceo J, lnostroza J et al. Gasto energético y composición corporal en mujeres con obesidad severa y mórbida sometidas a bypass gástrico. Rev Méd Chile 2008; 136: 570-77.         [ Links ]

20. Dias MCG, Ribeiro AG, Scabim VM, Faintuch J, Zilberstein B, Gama-Rodrigues JJ. Dietary intake of female bariatric patients after anti-obesity gastroplasty. Clinics 2006; 61: 93-98.         [ Links ]

21. Andreu A, Moizé V, Rodríguez L, Flores L, Vidal J. Protein intake, body composition, and protein status following bariatric surgery. Obes Surg 2010; 20: 1509-15.         [ Links ]

22. Faria SL, Faria OP, Buffington C, de Almeida Cardeal M, Ito MK. Dietary protein intake and bariatric surgery patients: a review. Obes Surg 2011 May 18; Epub ahead of print.         [ Links ]

23. Faria SL, de Oliveira Kelly E, Lins RD, Faria OP. Nutritional management of weight regain after bariatric surgery. Obes Surg 2010; 20: 135-39.         [ Links ]

24. Faria SL, Faria OP, Lopes TC, Galvão MV, de Oliveira Kelly E, Ito MK. Relation between carbohydrate intake and weight loss after bariatric surgery. Obes Surg 2009; 19: 708-16.         [ Links ]

25. Brolin RL, Robertson LB, Kenler HA, Cody RP. Weight loss and dietary intake after vertical banded gastroplasty and Roux-en-Y Gastric Bypass. Ann Surg 1994; 220: 782-90.         [ Links ]

26. Lissner L, Lindroos A K, Sjostrom L. Swedish obese subjects (SOS): an obesity intervention study with a nutritional perspective. Eur J Clin Nutr 1998; 52: 316-22.         [ Links ]

27. Wardé-Kamar J, Rogers M, Flancbaum L, Laferrère B. Calorie intake and meal patterns up to 4 years after Roux-en-Y Gastric Bypass surgery. Obes Surg 2004; 14: 1070-79.         [ Links ]

28. Dietary Reference Intakes for Calcium and Vitamin D. Institute of Medicine of the National Academies, Nov. 2010. Disponível em: http://www.iom.edu/vitamind. Acessado em: 15 abr. 2011.         [ Links ]

29. Campos CD, Dalcanale L, Pajecki D, Garrido A B Jr, Halpern A. Calcium intake and metabolic bone disease after eight years of Roux-en-y gastric bypass. Obes Surg 2008; 18: 386-90.         [ Links ]

30. Food and Nutrition Information Center. Dietary Reference Intakes: Elements. Disponível em: http://www.iom.edu/ObjectFile/Master/7/294/0.pdf. Acessado em 15 abr. 2011.         [ Links ]

31. García Caballero M. Cirugía de la diabetes mellitus tipo 2: el gran descubrimiento de la cirugía bariátrica. Nutr Hosp 2010; 25: 693-94.         [ Links ]

32. Cummings DE, Overduin J, Foster-Schubert KE. Gastric bypass for obesity: mechanisms of weight loss and diabetes resolution. J Clin Endocrinol Metab 2004; 89: 2608-15.         [ Links ]

33. Lim EL, Hollingsworth KG, Aribisala BS, Chen MJ, Mathers JC, Taylor R. Reversal of type 2 diabetes: normalisation of beta cell function in association with decreased pancreas and liver triacylglycerol. Diabetologia 2011; 54: 2506-14.         [ Links ]

34. Carvalho PS, Moreira CLCB, Barelli MC, Oliveira FH, Guzzo MF, Miguel GPS et al. Cirurgia Bariátrica Cura Síndrome Metabólica? Arq Bras End Metab 2007; 51: 79-85.         [ Links ]

35. Chang-Chen KJ, Mullur R, Bernal-Mizrachi E. beta-cell failure as a complication of diabetes. Rev EndocrMetab Disord 2008; 9: 329-43.         [ Links ]

36. Forcina DV, Almeida BO, Ribeiro-Jr MAF. Papel da cirurgia bariátrica no controle do diabete melito tipo II. Arq Bras Cir Dig 2008; 21: 130-32.         [ Links ]

37. Zander M, Madsbad S, Madsen JL, Holst JJ. Effect of 6-week course of glucagon-like peptide 1 on glycaemic control, insulin sensitivity, and beta-cell function in type 2 diabetes: a parallel-group study. Lancet 2002; 359: 824-30.         [ Links ]

38. Teijiran T, Jensen C, Dustson E. Bariatric surgery and type 2 diabetes mellitus: surgically induced remission. J Diabetes Sci Technol 2008; 2: 685-91.         [ Links ]

 

 

Correspondence:
Nilson Penha-Silva
Federal University of Uberlândia
Av. Pará, 1720, Campus Umuarama
CP: 38400-902 Uberlândia, MG. Brazil
E-mail: nspenha@ufu.br

Recibido: 21-II-2012
Aceptado: 2-III-2012