OBES SURG DOI 10.1007/s11695-014-1198-x
ORIGINAL CONTRIBUTIONS
Food Quality in the Late Postoperative Period of Bariatric Surgery: An Evaluation Using the Bariatric Food Pyramid Fernando Lucas Soares & Larissa Bissoni de Sousa & Carla Corradi-Perini & Magda Rosa Ramos da Cruz & Mario Gilberto Jesus Nunes & Alcides José Branco-Filho
# Springer Science+Business Media New York 2014
Abstract Bariatric surgery is an effective intervention in the treatment of obesity, but lifestyle and diet should be monitored after this procedure to ensure success. The Bariatric Food Pyramid was created basing on long-term nutritional care that proposes a standard of healthy living and eating habits considering gastric capacity and specific nutritional needs. The purpose of the current study is to evaluate the life habits and diet quality of patients who have undergone bariatric surgery (who have been recovering for at least 6 months) based on the specific food pyramid. Retrospective data analysis was performed using medical records of patients who had been followed for at least 6 months after bariatric surgery. The following data were collected from patient records: age, gender, education level (years), BMI (preoperative and
postoperative), percentage of excess weight loss (EWL) relative to the time of surgery, frequency of physical activity, use of nutritional supplements, usual dietary intake history, and fluid intake. Results were analyzed using descriptive statistics. We evaluated 172 patient records. In this study, there was a low prevalence of physical activity, use of vitamin–mineral supplements, and water intake. There also was low consumption of protein, fruit, vegetables, and vegetable oils. In addition, intake of carbohydrates, sugars, and fats were higher than the recommendations established by the pyramid. The results indicate that patients who have undergone bariatric surgery have an inadequate diet according to food evaluation with the specific pyramid. In the long term, this may lead to weight gain and vitamin and mineral deficiencies.
F. L. Soares : L. Bissoni de Sousa : C. Corradi-Perini (*) : M. R. Ramos da Cruz Nutrition Department, Health and Biosciences School, Pontifical Catholic University of Parana, 1155 Imaculada Conceição Street, Prado Velho, Curitiba, Paraná 80215-901, Brazil e-mail: [email protected]
Keywords Bariatric surgery . Nutrition assessment . Obesity . Food pyramid
F. L. Soares e-mail: [email protected]
In the past decade, the prevalence of obesity has increased at alarming rates worldwide. The causes go beyond the consumption of hypercaloric foods and low physical activity, but can also be genetic [1]. In the last two decades, the rate of morbid obesity, defined as body mass index (BMI) over 40 kg/m2, increased to approximately 15 million people in the USA [2]. When patients do not achieve effective results through nutritional counseling, drug treatment, or exercise, a more satisfactory and long-lasting intervention is necessary. One approach is bariatric surgery. However, after surgery, some nutrient deficiencies may occur because of decreased amount of food consumption, intestinal malabsorption, and presence of food intolerances. Nutritional deficiencies are dependent on the type of surgical technique used [3–6].
L. Bissoni de Sousa e-mail: [email protected] M. R. Ramos da Cruz e-mail: [email protected] M. G. J. Nunes Nursing Department, Health and Biosciences School, Pontifical Catholic University of Parana, 1155 Imaculada Conceição Street, Prado Velho, Curitiba, Paraná 80215-901, Brazil e-mail: [email protected] A. J. Branco-Filho Bariatric Surgery Services, Santa Casa de Misericordia Hospital, 665 República Argentina Avenue, Água Verde, Curitiba, Paraná 80240-210, Brazil e-mail: [email protected]
Introduction/Purpose
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The main affected nutrients after bariatric surgery are vitamin B12, folic acid, iron, vitamin D, and calcium. The nutritional treatment is essential for successful and satisfactory weight loss and to decrease or avoid nutritional deficiencies that in the long run can bring serious consequences [4–8]. The American Society for Metabolic and Bariatric Surgery created dietary recommendations to maintain health, preserve lost weight, and decrease the occurrence of nutritional deficiencies [9]. These recommendations are outlined in a nutritional pyramid created for patients in the late postoperative bariatric surgery [10]. This pyramid is a standard for long-term healthy living and eating habits that considers these patients’ gastric capacity and specific nutritional needs. The bottom of the pyramid includes standards for vitamin–mineral supplements, water, and decaffeinated beverages. The second level up includes four to six servings per day of lean meat, dairy products with little or no fat (e.g., cheese, milk, and yogurt), legumes, and eggs. The third level includes two to three servings per day of vegetables, vegetable oils (preferably olive), and fruit (divided into high- and low-sugar concentrations). The fourth level includes two servings per day of carbohydrates (e.g., cereals, tubers, and legumes). The top of the pyramid includes foods that should be avoided, such as foods containing high amounts of saturated and trans fats, cholesterol, sugar, and alcoholic and carbonated beverages [10]. To our knowledge, no studies have used this pyramid to analyze food quality or lifestyle of patients who have undergone bariatric surgery. For this reason, the aim of this study is to evaluate food quality and lifestyle habits of patients who have had bariatric surgery (and have been recovering for at least 6 months) by comparing their dietary records to the specific food pyramid.
Materials and Methods Records of patients who underwent Roux-en-Y gastric bypass at the Nutrition Clinic of Bariatric Surgery were used in this study. These patients began the process of nutritional education preoperatively. They were instructed to follow a postoperative diet and use nutritional supplements. This nutrition education was performed in periodic and individualized consultations, as established in the service protocol, which is based on the American Society for Metabolic and Bariatric Surgery dietary recommendations. Retrospective data analysis was performed using medical records of patients who had been followed for at least 6 months after bariatric surgery. Of the 172 patient records selected to provide information about the sixth month after bariatric surgery, only 154 were used with 1 year or more because 18 records had incomplete data.
The following data were collected from the patient records: age, gender, education level (years), BMI (preoperative and postoperative), and percentage of excess weight loss (EWL) relative to the time of surgery. We also collected data on physical activity, use of nutritional supplements, usual dietary intake history, and fluid intake. Physical activity was defined as exercise performed at least three times a week for 40 min. Usual dietary intake history is a method that asks the patient to recall a typical daily intake pattern, including amount, frequency, and food preparation method of food consumed. This intake history includes all meals, beverages, and snacks. Advantages of this method are that it evaluates long-term dietary habits and is quick and easy to complete. The main disadvantage is that a limited amount of information on the actual quantities of food and beverages is obtained. In addition, this method works only if a patient can describe a typical daily intake pattern. Another disadvantage is that patients may not report foods they know are unhealthy. Analysis of usual intake history was performed using the number of servings per food group and comparing the value obtained with the optimal value recommended by the specific pyramid. To determine the number of servings from each food group, dietary data from nutritional records were analyzed individually. With the aid of specific tables [11–13], household measures were converted into grams, thereby quantifying the number of portions eaten from each food group present in the pyramid. For this study, we made adjustments and standardizations to better assess the records of the studied population. Because of the high amount of carbohydrates found in legumes, we considered these foods carbohydrates. However, if a patient was vegetarian, we considered these foods as protein. Margarine was included in vegetable oils because it has a small amount of saturated fat and contains no trans fat. Alcohol and carbonated beverages were counted as fats and sugars. The variables were analyzed with descriptive statistics using simple frequency distributions: percentages, frequencies, averages, standard deviations, and minimum and maximum values. The number of servings eaten by each individual was classified as either within or over the recommendation [10].
Results We retrospectively analyzed the data from the medical records of 172 patients (92.52 % females) who had undergone bariatric surgery (and had been recovering for at least 6 months). The average age of the patients was 42.38±9.00 years, ranging from 22 to 62 years old. The level of education of the majority of the patients (50 %) was basic education (Table 1). We analyzed the post-operatory BMI at 6 and 12 months (Table 2) and observed that the medium EWL was more than 50 % in both periods. We initiated the evaluation of lifestyle
OBES SURG Table 1 Demographic characteristics of the studied population Variable Gender Female Male Length of education Basic (12 years)
n=172
Percentage
159 13
92.44 7.56
86 69 17
50 40.11 9.89
habits and diet quality of patients at the first level of the pyramid, which consists of physical activity, use of vitamin– mineral supplements, and water intake. Of the 172 patients, 63.01 % engaged in physical activity regularly 6 months after surgery, and 60.39 % were physically active 12 months after surgery. Regarding the use of vitamin– mineral supplements, only 38.73 and 25.97 % were taking supplements at 6 and 12 months after surgery, respectively. Next, we analyzed the bottom of the pyramid, which includes liquids without caffeine, sugar, and gas. The average water intake of the patients was 1,056±571.51 mL (n=172) at 6 months and 1,070±568.13 mL (n=154) 1 year after surgery. These averages are lower than the recommended amounts. Five patients within 6 months and one patient within 12 months had consumed liquid other than plain water (i.e., coconut water). Low water intake can impair the patients’ bodily functions, such as bowel function, and cannot replace losses happening through physical activity, presence of diarrhea, or vomiting. The second level of the food group pyramid is presented in terms of the recommended servings of each food. Table 3 presents the averages, standard deviations, and minimum and maximum serving values according to the dietary records of the patients in both study periods. These values are compared with the recommended servings of the pyramid. We observed that the average consumption of protein, vegetables, vegetable oils, and fruits was lower than the recommended amounts at both 6 and 12 months. Groups of grains and cereals were consumed over the recommended servings in both periods. Figure 1 shows the percentages of the patients who had consumed portions of the food groups within or over the recommendations of the pyramid, both in 6 months and 1 year. More than half of the patients had insufficient intake of fruits Table 2 BMI and EWL of the studied population
Data are expressed as average ± SD BMI body mass index, EWL excess weight loss
Table 3 Daily intake of food groups servings by patients after gastric bypass bariatric surgery
BMI (Kg/m2) Minimum to maximum EWL (%) Minimum to maximum
Food groups (recommended servings)
6 months postsurgery (n=172)
≥1 year postsurgery (n=154)
Proteins (4–6) Minimum to maximum Vegetables (2–3) Minimum–maximum Vegetal oil (2–3) Minimum to maximum Fruits (2–3) Minimum to maximum Grains and cereals (2) Minimum to maximum
3.24±1.40 0.00–7.32 1.07±0.81 0.00–4.23 0.69±1.01 0.00–6.76 1.72±1.46 0.00–8.14 3.25±1.67 0.00–9.44
3.19±1.56 0.00–7.60 1.04±0.74 0.00–3.85 0.85±0.86 0.00–4.00 1.87±1.57 0.00–7.71 4.16±2.06 0.55–16.24
Data are expressed as average ± SD
and protein foods at 6 and 12 months. In addition, more than 80 % had insufficient intake of vegetables and vegetable oils. At 6 months, the intake of grains and cereals was over the recommended amount by 70.5 %, and this percentage increased to 87.1 % at 12 months. In this study, alcoholic and carbonated beverages were considered fats and sugars. Three patients at 6 months and nine patients at 1 year reported consuming carbonated beverages. Only one patient reported the intake of alcoholic beverages at 6 months after surgery.
Discussion In this study, the majority of participants were women, which is consistent with other studies [14–18]. This may be because women seek treatment for obesity more often [19]. A higher prevalence of female patients may influence food intake results. Research from clinical practice has shown that women eat less protein and more carbohydrates. Furthermore, these types of foods often cost less, suggesting a relationship with level of education. Most of the patients in this study completed only primary education, and they used the public health system. This suggests that the patients in this study have low
Before surgery (n=172)
6 months postsurgery (n=172)
≥1 year postsurgery (n=154)
46.88±5.97 34.52–74.14 – –
34.48±4.71 23.17–53.25 56.41±15.23 12.47–117.89
31.36±4.58 21.74–45.86 71.81±18.22 28.01–125.86
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Fig. 1 Analysis of consumed food group adequacy using bariatric pyramid recommendations. The patients’ dietary records at 6 months and 1 year after bariatric surgery were analyzed using specific tables to convert household measures into grams, allowing the quantification of the consumed food groups, which are demonstrated as percentages of portions that are below, within, or over the recommendation of the specific pyramid
purchasing power. This may have contributed to the low intake of fruits, vegetables, and protein foods, which cost more in this country. Other studies have demonstrated that low education is one factor related to inadequate weight loss of patients after surgery [20]. Regarding post-operative BMI, we demonstrated that the results up to 6 months and 1 year were similar to those of the studies of Pedrosa et al. [21]. Although we observed that most patients after 12 months of surgery still had grade 1 obesity as measured by BMI, the percentage of EWL was adequate (above 50 %) [22, 23]. The main goal of treatment is not for these patients to reach a normal BMI, but it is to improve comorbidities. One factor that helps maintain weight loss and improve body composition is physical activity [24]. In this study, more than 60 % of patients were physically active. Physical activity was defined as regular exercise for at least three times a week for 40 min. The predominant form of exercise was walking, probably because of the low cost. Another factor that may have been related to cost was the use of vitamin–mineral supplements. Less than 30 % of patients were taking supplements at 12 months after surgery. These results are similar to those found in the research conducted by Lizer et al. [25]. However, in other studies with different populations who underwent bariatric surgery, a higher percentage of patients who used supplements were found [4, 26]. The use of supplements is indicated for the patients because of the high risk of developing nutrient deficiencies, a wellknown complication after bariatric surgery. This is because a regular diet may not meet the recommended daily requirements.
These deficiencies are because of gastric capacity restriction, food intolerances, absorptive area reduction, fast weight loss, and preoperative deficiencies [27, 28]. The most common vitamin–mineral deficiencies in patients who have undergone surgery with the Roux-en-Y technique are as follows: vitamin B1, vitamin B12, folic acid, vitamin D, vitamin A, vitamin E, iron, calcium, zinc, magnesium, selenium, and chromium [25, 27, 28]. Most of these nutrients are found in foods with protein, which are included in the second level of the pyramid at four to six servings per day. Therefore, low intake of the protein food group can cause deficiencies in micronutrients [29–31]. In this study, we found that most patients had insufficient intake of protein. These results occurred at both 6 and 12 months post-surgery. Inadequate protein is the most commonly reported deficiency in this population [28]. Low intake may be associated with energy restriction after surgery and intolerance to food sources, such as red meat and milk [22, 30–32]. Low protein intake can increase the loss of lean body mass. Use of protein supplements is a nutritional strategy that can be used to correct this deficiency [31]. Low intake of dairy products is associated with deficiency of calcium and vitamin D in bariatric surgery patients [30]. This deficiency is related to immunologic system dysfunction [32], secondary hyperparathyroidism, and damage to bone metabolism, which may lead to osteoporosis [27, 33]. The third level of the pyramid includes fruits, vegetables, and vegetable oils. Fruits and vegetables are foods that provide a wide range of nutrients. Bariatric surgery patients have a high risk of folic acid deficiency which can be caused by decreased fruit and vegetable intake [28, 31]. Schweiger et al. [32] conducted a study that assessed the food tolerance of patients. He found that patients were tolerant of vegetables and salads not only in the first months after surgery but also through 12 subsequent months. Quadros et al. [34] found a similar result. Vegetable oils, which also are included in the third level of the pyramid, are vehicles of fat-soluble vitamins, sources of essential fatty acids, and have the characteristic of increasing satiety. However, these oils are highly caloric. Because only moderate intake of vegetable oils is recommended, patients after surgery are at risk for developing liposoluble vitamin deficiencies [27, 30, 35]. There was a high percentage of patients with insufficient intake of oils. This may have been because patients did not report consumption because vegetable oils are considered forbidden foods. Another reason is that patients may not consider vegetable oil a food because it is consumed in small quantities. Some studies have found a high prevalence of food intolerance postoperatively from carbohydrates. Rice, noodles, and bread intolerances were reported most often [22, 32, 34, 36, 37]. Faria et al. [38] conducted a study that analyzed food
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intake and monthly weight loss of 89 bariatric surgery patients. They found that daily intake of carbohydrates, as well as the glycemic load of the meal, is negatively associated with monthly weight loss. In fact, this may have influenced weight loss by 63 %. Therefore, it is necessary to verify the consumption of carbohydrates and glycemic load in long-term nutritional monitoring of these patients to prevent weight regain. The top of the pyramid includes foods that must be avoided by patients. These foods are sugars, fats, and carbonated and alcoholic beverages. Foods containing sugar, such as chocolates, candies, ice cream, and cakes, provide extra calories that inhibit weight loss. Moreover, these foods are highly osmotic and can cause dumping syndrome [8, 27, 35]. Cruz and Morimoto [37] observed that the frequency of vomiting among patients in the postoperative period is related to the intake of fatty foods or concentrated sweets. Consumption of carbonated beverages with sugar is associated with high caloric intake, weight gain, and negative interactions with the bioavailability of some micronutrients (e.g., iron and calcium) [39]. Alcohol provides a high dietary intake of calories and avoids fat oxidation. High intake of alcohol diminishes the effectiveness of weight loss, favors the development of vitamin and mineral deficiencies, decreases bone mass, and increases nutritional medical complications. Thus, it is recommended that bariatric surgery patients drink alcohol with caution [27]. One year after surgery, a significant increase in the consumption of carbohydrates, sugars, and fats were found (i.e., patients tended to return to previous habits). Foods high in fat, such as sausages, pates, fried foods, fatty meats, and cheeses, should be avoided because of possible intolerances and the high level of saturated fats. In addition, these foods are highly caloric, which inhibits weight loss and facilitates weight regain [27]. Lima and Sampaio [19] found that severely obese patients who have not undergone bariatric surgery had a high fat intake. These habits can persist and recur after surgery, justifying high fat intake in this population. In this study, the method we used to assess food consumption has some weaknesses. These weaknesses include a limited amount of information collected on the quantities of food and beverages and the possibility that patients may not report foods they know are unhealthy. Nevertheless, our results give valuable information to improve nutritional counseling for this population. After bariatric surgery, patients not only have the benefit of weight loss but also have the opportunity to improve the quality of their food intake [16]. However, for these benefits to occur, it is important for these patients to have long-term periodic nutritional monitoring. According to the literature, there is a possible chance of weight regain in the second year following surgery [36]; thus, at year 2, there should be high attention given to nutritional analysis of food intake. This should be the objective of research studies.
Conclusion In this study, we identified inadequacies in lifestyle and eating habits of the bariatric surgery patients. We found that a low proportion of the population engaged in physical activity, used vitamin–mineral supplements, and consumed adequate amounts of foods from the protein, fruit, vegetable, and vegetable oils food groups. Moreover, we observed a high consumption of carbohydrates, sugars, and fats at both 6 months and 1 year postoperatively. Although the bariatric surgery patients in this study lost an appropriate amount of weight, it is likely that these patients may regain weight due to poor dietary intake and the return to old eating habits. In addition, these patients also may develop severe nutritional deficiencies and have comorbidities that existed preoperatively. Conflict of Interest Fernando Lucas Soares, Larissa Bissoni de Sousa, Carla Corradi Perini, Magda Rosa Ramos da Cruz, Mario Gilberto Jesus Nunes, and Alcides José Branco-Filho report no conflicts of interest and make no disclosures.
References 1. Owens TM. Morbid obesity: the disease and comorbidities. Crit Care Nurse Q. 2003;26(2):162–5. PMID: 12744597. 2. Livhits M, Mercado C, Yermilov I, et al. Is social support associated with greater weight loss after bariatric surgery? A systematic review. Obes Rev. 2010;12:142–8. PMID: 20158617. 3. Xanthakos SA. Nutritional deficiencies in obesity and after bariatric surgery. Pediatr Clin N Am. 2009;56(5):1105–21. PMID: 19931066. 4. Aasheim ET, Björkman S, Søvik TT, et al. Vitamin status after bariatric surgery: a randomized study of gastric bypass and duodenal switch. Am J Clin Nutr. 2009;90(1):15–22. PMID: 19439456. 5. Davies DJ, Baxter JM, Baxter JN. Nutritional deficiencies after bariatric surgery. Obes Surg. 2007;17(9):1150–8. PMID: 18074487. 6. Shankar P, Boylan M, Sriram K. Micronutrient deficiencies after bariatric surgery. Nutrition. 2010;26(11–12):1031–7. PMID: 20363593. 7. Bloomberg RD, Fleishman A, Nalle JE, et al. Nutritional deficiencies following bariatric surgery: what have we learned? Obes Surg. 2005;15:145–54. PMID: 15802055. 8. Fujioka K. Follow-up of nutritional and metabolic problems after bariatric surgery. Diabetes Care. 2005;28:481–4. PMID: 15677821. 9. Committee AHSSAHN. Aills L, Blankenship J, Buffington C, Furtado M, Parrott J. ASMBS allied health nutritional guidelines for the surgical weight loss patient. Surg Obes Relat Dis. 2008;4(5 Suppl):S73–108. 10. Moizé VL, Pi-Sunyer X, Mochari H, et al. Nutritional pyramid for post-gastric bypass patients. Obes Surg. 2010;20(8):1133–41. PMID: 20401543. 11. Pinheiro ABV. Tabela para avaliação de consumo alimentar em medidas caseiras. 5th ed. São Paulo: Atheneu; 2008. 12. Pacheco M. Tabela de equivalentes, medidas caseiras e composição química dos alimentos. Rio de Janeiro: Rubio; 2006. 13. Moreira MA. Medidas caseiras no preparo de alimentos. Goiânia: AB; 2002. 14. Dymek MP, Grange D, Neven K, et al. Quality of life after gastric bypass surgery: a cross-sectional study. Obes Res. 2002;10(11): 1135–42. PMID: 12429877.
OBES SURG 15. Toledo CC, Camilo GB, Guimarães RL, et al. Qualidade de vida no pós-operatório tardio de pacientes submetidos à cirurgia bariátrica. Rev APS. 2010;13(2):202–9. 16. Júnior FCM, Júnior WSS, Filho NS, et al. Efeito da perda ponderal induzida pela cirurgia bariátrica sobre a prevalência de síndrome metabólica. Arq Bras Cardiol. 2009;92(6):452–6. PMID: 19629308. 17. Balduf LM, Kohn GP, Galanko JA, et al. The impact of socioeconomic factors on patient preparation for bariatric surgery. Rev Obes Surg. 2009;19:1089–95. PMID: 19517200. 18. Faria SL, Kelly E, Faria OP. Energy expenditure and weight regain in patients submitted to Roux-en-Y gastric bypass. Rev Obes Surg. 2009;19:856–9. PMID: 19399563. 19. Lima LP, Sampaio HAC. Caracterização socioeconômica, antropométrica e alimentar de obesos graves. Rev Ciênc Saúde Coletiva. 2007;12(4):1011–20. PMID: 17680159. 20. Júnior WS, Amaral JL, Nonino-Borges CB. Factors related to weight loss up to 4 years after bariatric surgery. Rev Obes Surg. 2011;21(11): 1724–30. PMID: 21509481. 21. Pedrosa IV, Burgos MGPA, Souza NC, et al. Aspectos nutricionais em obesos antes e após a cirurgia bariátrica. Rev Col Bras Cir. 2009;36(4):316–22. PMID: 20076921. 22. Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA. 2002;288:2793–6. PMID: 12472304. 23. World Health Organization. Obesity. Preventing and managing the global epidemic. Report of a WHO consultation on obesity. WHO/ NUT/NCD/981. Geneva: WHO; 1998. PMID: 11234459. 24. Jacobi D, Ciangura C, Couet C, et al. Physical activity and weight loss following bariatric surgery. Rev Obes Rev. 2011;12:366–77. PMID: 20331508. 25. Lizer MH, Papageorgeon H, Glembot TM. Nutritional and pharmacologic challenges in the bariatric surgery patient. Rev Obes Surg. 2010;20:1654–9. PMID: 20107919. 26. Wardé-Kamar J, Rogers M, Flancbaum L, et al. Calorie intake and meal patterns up to 4 years after Roux-en-Y gastric bypass surgery. Rev Obes Surg. 2004;14:1070–9. PMID: 15479596. 27. Rubio MA, Moreno C. Implicaciones nutricionales de la cirugía bariátrica sobre el tracto gastrointestinal. Rev Nutr Hosp. 2007;22(2):124–34. PMID: 17679300.
28. Bordalo LA, Salesteixeira TF, Bressan J, et al. Cirurgia bariátrica: como e por que suplementar. Rev Assoc Med Bras. 2011;57(1):113– 20. PMID: 21390468. 29. Sallé A, Demarsy D, Poirier AL, et al. Zinc deficiency: a frequent and underestimated complication after bariatric surgery. Rev Obes Surg. 2010;20:1660–70. PMID: 20706804. 30. Ziegler O, Sirveaux MA, Brunaud L, et al. Medical follow-up after bariatric surgery: nutritional and drug issues. General recommendations for the prevention and treatment of nutritional deficiencies. Diabetes Metab. 2009;35:544–57. PMID: 20152742. 31. Vargas-Ruiz AG, Hernández-Rivera G, Herrera MF. Prevalence of iron, folate, and vitamin B12 deficiency anemia after laparoscopic Roux-en-Y gastric bypass. Rev Obes Surg. 2008;18:288–93. PMID: 18214631. 32. Schweiger C, Weiss R, Keidar A. Effect of different bariatric operations on food tolerance and quality of eating. Rev Obes Surg. 2010;20:1393–9. PMID: 20680506. 33. Viégas M, Vasconcelos RS, Neves AP, et al. Cirurgia bariátrica e metabolismo ósseo: uma revisão sistemática. Arq Bras Endocrinol Metab. 2010;54(2):158–63. PMID: 20485904. 34. Quadros MRR, Savaris AL, Ferreira MV, et al. Intolerância alimentar no pós-operatório de pacientes submetidos à cirurgia bariátrica. Rev Bras Nutr Clin. 2007;22(1):15–9. 35. Parkes E. Nutritional management of patients after bariatric surgery. Am J Med Sci. 2006;331(4):207–13. PMID: 16617236. 36. Hernández MAR, Sancho EM, Fuster MA, et al. Comparación a 5 años de dos técnicas de cirugía bariátrica en pacientes con obesidad mórbida seguidos en consulta enfermera. Rev Nutr Hosp. 2009;24(6):667–75. PMID: 20049369. 37. Cruz MRR, Morimoto IMI. Intervenção nutricional no tratamento cirúrgico da obesidade mórbida: resultados de um protocolo diferenciado. Rev Nutr. 2004;17(2):263–72. 38. Faria SL, Faria OP, Lopes TC, et al. Relation between carbohydrate intake and weight loss after bariatric surgery. Rev Obes Surg. 2009;19:708–16. PMID: 18618210. 39. Vartanian LR, Schwartz MB, Brownell KD. Effects of soft drink consumption on nutrition and health: a systematic review and metaanalysis. Am J Public Health. 2007;97(4):667–75. PMID: 17329656.
ORIGINAL CONTRIBUTIONS
Food Quality in the Late Postoperative Period of Bariatric Surgery: An Evaluation Using the Bariatric Food Pyramid Fernando Lucas Soares & Larissa Bissoni de Sousa & Carla Corradi-Perini & Magda Rosa Ramos da Cruz & Mario Gilberto Jesus Nunes & Alcides José Branco-Filho
# Springer Science+Business Media New York 2014
Abstract Bariatric surgery is an effective intervention in the treatment of obesity, but lifestyle and diet should be monitored after this procedure to ensure success. The Bariatric Food Pyramid was created basing on long-term nutritional care that proposes a standard of healthy living and eating habits considering gastric capacity and specific nutritional needs. The purpose of the current study is to evaluate the life habits and diet quality of patients who have undergone bariatric surgery (who have been recovering for at least 6 months) based on the specific food pyramid. Retrospective data analysis was performed using medical records of patients who had been followed for at least 6 months after bariatric surgery. The following data were collected from patient records: age, gender, education level (years), BMI (preoperative and
postoperative), percentage of excess weight loss (EWL) relative to the time of surgery, frequency of physical activity, use of nutritional supplements, usual dietary intake history, and fluid intake. Results were analyzed using descriptive statistics. We evaluated 172 patient records. In this study, there was a low prevalence of physical activity, use of vitamin–mineral supplements, and water intake. There also was low consumption of protein, fruit, vegetables, and vegetable oils. In addition, intake of carbohydrates, sugars, and fats were higher than the recommendations established by the pyramid. The results indicate that patients who have undergone bariatric surgery have an inadequate diet according to food evaluation with the specific pyramid. In the long term, this may lead to weight gain and vitamin and mineral deficiencies.
F. L. Soares : L. Bissoni de Sousa : C. Corradi-Perini (*) : M. R. Ramos da Cruz Nutrition Department, Health and Biosciences School, Pontifical Catholic University of Parana, 1155 Imaculada Conceição Street, Prado Velho, Curitiba, Paraná 80215-901, Brazil e-mail: [email protected]
Keywords Bariatric surgery . Nutrition assessment . Obesity . Food pyramid
F. L. Soares e-mail: [email protected]
In the past decade, the prevalence of obesity has increased at alarming rates worldwide. The causes go beyond the consumption of hypercaloric foods and low physical activity, but can also be genetic [1]. In the last two decades, the rate of morbid obesity, defined as body mass index (BMI) over 40 kg/m2, increased to approximately 15 million people in the USA [2]. When patients do not achieve effective results through nutritional counseling, drug treatment, or exercise, a more satisfactory and long-lasting intervention is necessary. One approach is bariatric surgery. However, after surgery, some nutrient deficiencies may occur because of decreased amount of food consumption, intestinal malabsorption, and presence of food intolerances. Nutritional deficiencies are dependent on the type of surgical technique used [3–6].
L. Bissoni de Sousa e-mail: [email protected] M. R. Ramos da Cruz e-mail: [email protected] M. G. J. Nunes Nursing Department, Health and Biosciences School, Pontifical Catholic University of Parana, 1155 Imaculada Conceição Street, Prado Velho, Curitiba, Paraná 80215-901, Brazil e-mail: [email protected] A. J. Branco-Filho Bariatric Surgery Services, Santa Casa de Misericordia Hospital, 665 República Argentina Avenue, Água Verde, Curitiba, Paraná 80240-210, Brazil e-mail: [email protected]
Introduction/Purpose
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The main affected nutrients after bariatric surgery are vitamin B12, folic acid, iron, vitamin D, and calcium. The nutritional treatment is essential for successful and satisfactory weight loss and to decrease or avoid nutritional deficiencies that in the long run can bring serious consequences [4–8]. The American Society for Metabolic and Bariatric Surgery created dietary recommendations to maintain health, preserve lost weight, and decrease the occurrence of nutritional deficiencies [9]. These recommendations are outlined in a nutritional pyramid created for patients in the late postoperative bariatric surgery [10]. This pyramid is a standard for long-term healthy living and eating habits that considers these patients’ gastric capacity and specific nutritional needs. The bottom of the pyramid includes standards for vitamin–mineral supplements, water, and decaffeinated beverages. The second level up includes four to six servings per day of lean meat, dairy products with little or no fat (e.g., cheese, milk, and yogurt), legumes, and eggs. The third level includes two to three servings per day of vegetables, vegetable oils (preferably olive), and fruit (divided into high- and low-sugar concentrations). The fourth level includes two servings per day of carbohydrates (e.g., cereals, tubers, and legumes). The top of the pyramid includes foods that should be avoided, such as foods containing high amounts of saturated and trans fats, cholesterol, sugar, and alcoholic and carbonated beverages [10]. To our knowledge, no studies have used this pyramid to analyze food quality or lifestyle of patients who have undergone bariatric surgery. For this reason, the aim of this study is to evaluate food quality and lifestyle habits of patients who have had bariatric surgery (and have been recovering for at least 6 months) by comparing their dietary records to the specific food pyramid.
Materials and Methods Records of patients who underwent Roux-en-Y gastric bypass at the Nutrition Clinic of Bariatric Surgery were used in this study. These patients began the process of nutritional education preoperatively. They were instructed to follow a postoperative diet and use nutritional supplements. This nutrition education was performed in periodic and individualized consultations, as established in the service protocol, which is based on the American Society for Metabolic and Bariatric Surgery dietary recommendations. Retrospective data analysis was performed using medical records of patients who had been followed for at least 6 months after bariatric surgery. Of the 172 patient records selected to provide information about the sixth month after bariatric surgery, only 154 were used with 1 year or more because 18 records had incomplete data.
The following data were collected from the patient records: age, gender, education level (years), BMI (preoperative and postoperative), and percentage of excess weight loss (EWL) relative to the time of surgery. We also collected data on physical activity, use of nutritional supplements, usual dietary intake history, and fluid intake. Physical activity was defined as exercise performed at least three times a week for 40 min. Usual dietary intake history is a method that asks the patient to recall a typical daily intake pattern, including amount, frequency, and food preparation method of food consumed. This intake history includes all meals, beverages, and snacks. Advantages of this method are that it evaluates long-term dietary habits and is quick and easy to complete. The main disadvantage is that a limited amount of information on the actual quantities of food and beverages is obtained. In addition, this method works only if a patient can describe a typical daily intake pattern. Another disadvantage is that patients may not report foods they know are unhealthy. Analysis of usual intake history was performed using the number of servings per food group and comparing the value obtained with the optimal value recommended by the specific pyramid. To determine the number of servings from each food group, dietary data from nutritional records were analyzed individually. With the aid of specific tables [11–13], household measures were converted into grams, thereby quantifying the number of portions eaten from each food group present in the pyramid. For this study, we made adjustments and standardizations to better assess the records of the studied population. Because of the high amount of carbohydrates found in legumes, we considered these foods carbohydrates. However, if a patient was vegetarian, we considered these foods as protein. Margarine was included in vegetable oils because it has a small amount of saturated fat and contains no trans fat. Alcohol and carbonated beverages were counted as fats and sugars. The variables were analyzed with descriptive statistics using simple frequency distributions: percentages, frequencies, averages, standard deviations, and minimum and maximum values. The number of servings eaten by each individual was classified as either within or over the recommendation [10].
Results We retrospectively analyzed the data from the medical records of 172 patients (92.52 % females) who had undergone bariatric surgery (and had been recovering for at least 6 months). The average age of the patients was 42.38±9.00 years, ranging from 22 to 62 years old. The level of education of the majority of the patients (50 %) was basic education (Table 1). We analyzed the post-operatory BMI at 6 and 12 months (Table 2) and observed that the medium EWL was more than 50 % in both periods. We initiated the evaluation of lifestyle
OBES SURG Table 1 Demographic characteristics of the studied population Variable Gender Female Male Length of education Basic (12 years)
n=172
Percentage
159 13
92.44 7.56
86 69 17
50 40.11 9.89
habits and diet quality of patients at the first level of the pyramid, which consists of physical activity, use of vitamin– mineral supplements, and water intake. Of the 172 patients, 63.01 % engaged in physical activity regularly 6 months after surgery, and 60.39 % were physically active 12 months after surgery. Regarding the use of vitamin– mineral supplements, only 38.73 and 25.97 % were taking supplements at 6 and 12 months after surgery, respectively. Next, we analyzed the bottom of the pyramid, which includes liquids without caffeine, sugar, and gas. The average water intake of the patients was 1,056±571.51 mL (n=172) at 6 months and 1,070±568.13 mL (n=154) 1 year after surgery. These averages are lower than the recommended amounts. Five patients within 6 months and one patient within 12 months had consumed liquid other than plain water (i.e., coconut water). Low water intake can impair the patients’ bodily functions, such as bowel function, and cannot replace losses happening through physical activity, presence of diarrhea, or vomiting. The second level of the food group pyramid is presented in terms of the recommended servings of each food. Table 3 presents the averages, standard deviations, and minimum and maximum serving values according to the dietary records of the patients in both study periods. These values are compared with the recommended servings of the pyramid. We observed that the average consumption of protein, vegetables, vegetable oils, and fruits was lower than the recommended amounts at both 6 and 12 months. Groups of grains and cereals were consumed over the recommended servings in both periods. Figure 1 shows the percentages of the patients who had consumed portions of the food groups within or over the recommendations of the pyramid, both in 6 months and 1 year. More than half of the patients had insufficient intake of fruits Table 2 BMI and EWL of the studied population
Data are expressed as average ± SD BMI body mass index, EWL excess weight loss
Table 3 Daily intake of food groups servings by patients after gastric bypass bariatric surgery
BMI (Kg/m2) Minimum to maximum EWL (%) Minimum to maximum
Food groups (recommended servings)
6 months postsurgery (n=172)
≥1 year postsurgery (n=154)
Proteins (4–6) Minimum to maximum Vegetables (2–3) Minimum–maximum Vegetal oil (2–3) Minimum to maximum Fruits (2–3) Minimum to maximum Grains and cereals (2) Minimum to maximum
3.24±1.40 0.00–7.32 1.07±0.81 0.00–4.23 0.69±1.01 0.00–6.76 1.72±1.46 0.00–8.14 3.25±1.67 0.00–9.44
3.19±1.56 0.00–7.60 1.04±0.74 0.00–3.85 0.85±0.86 0.00–4.00 1.87±1.57 0.00–7.71 4.16±2.06 0.55–16.24
Data are expressed as average ± SD
and protein foods at 6 and 12 months. In addition, more than 80 % had insufficient intake of vegetables and vegetable oils. At 6 months, the intake of grains and cereals was over the recommended amount by 70.5 %, and this percentage increased to 87.1 % at 12 months. In this study, alcoholic and carbonated beverages were considered fats and sugars. Three patients at 6 months and nine patients at 1 year reported consuming carbonated beverages. Only one patient reported the intake of alcoholic beverages at 6 months after surgery.
Discussion In this study, the majority of participants were women, which is consistent with other studies [14–18]. This may be because women seek treatment for obesity more often [19]. A higher prevalence of female patients may influence food intake results. Research from clinical practice has shown that women eat less protein and more carbohydrates. Furthermore, these types of foods often cost less, suggesting a relationship with level of education. Most of the patients in this study completed only primary education, and they used the public health system. This suggests that the patients in this study have low
Before surgery (n=172)
6 months postsurgery (n=172)
≥1 year postsurgery (n=154)
46.88±5.97 34.52–74.14 – –
34.48±4.71 23.17–53.25 56.41±15.23 12.47–117.89
31.36±4.58 21.74–45.86 71.81±18.22 28.01–125.86
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Fig. 1 Analysis of consumed food group adequacy using bariatric pyramid recommendations. The patients’ dietary records at 6 months and 1 year after bariatric surgery were analyzed using specific tables to convert household measures into grams, allowing the quantification of the consumed food groups, which are demonstrated as percentages of portions that are below, within, or over the recommendation of the specific pyramid
purchasing power. This may have contributed to the low intake of fruits, vegetables, and protein foods, which cost more in this country. Other studies have demonstrated that low education is one factor related to inadequate weight loss of patients after surgery [20]. Regarding post-operative BMI, we demonstrated that the results up to 6 months and 1 year were similar to those of the studies of Pedrosa et al. [21]. Although we observed that most patients after 12 months of surgery still had grade 1 obesity as measured by BMI, the percentage of EWL was adequate (above 50 %) [22, 23]. The main goal of treatment is not for these patients to reach a normal BMI, but it is to improve comorbidities. One factor that helps maintain weight loss and improve body composition is physical activity [24]. In this study, more than 60 % of patients were physically active. Physical activity was defined as regular exercise for at least three times a week for 40 min. The predominant form of exercise was walking, probably because of the low cost. Another factor that may have been related to cost was the use of vitamin–mineral supplements. Less than 30 % of patients were taking supplements at 12 months after surgery. These results are similar to those found in the research conducted by Lizer et al. [25]. However, in other studies with different populations who underwent bariatric surgery, a higher percentage of patients who used supplements were found [4, 26]. The use of supplements is indicated for the patients because of the high risk of developing nutrient deficiencies, a wellknown complication after bariatric surgery. This is because a regular diet may not meet the recommended daily requirements.
These deficiencies are because of gastric capacity restriction, food intolerances, absorptive area reduction, fast weight loss, and preoperative deficiencies [27, 28]. The most common vitamin–mineral deficiencies in patients who have undergone surgery with the Roux-en-Y technique are as follows: vitamin B1, vitamin B12, folic acid, vitamin D, vitamin A, vitamin E, iron, calcium, zinc, magnesium, selenium, and chromium [25, 27, 28]. Most of these nutrients are found in foods with protein, which are included in the second level of the pyramid at four to six servings per day. Therefore, low intake of the protein food group can cause deficiencies in micronutrients [29–31]. In this study, we found that most patients had insufficient intake of protein. These results occurred at both 6 and 12 months post-surgery. Inadequate protein is the most commonly reported deficiency in this population [28]. Low intake may be associated with energy restriction after surgery and intolerance to food sources, such as red meat and milk [22, 30–32]. Low protein intake can increase the loss of lean body mass. Use of protein supplements is a nutritional strategy that can be used to correct this deficiency [31]. Low intake of dairy products is associated with deficiency of calcium and vitamin D in bariatric surgery patients [30]. This deficiency is related to immunologic system dysfunction [32], secondary hyperparathyroidism, and damage to bone metabolism, which may lead to osteoporosis [27, 33]. The third level of the pyramid includes fruits, vegetables, and vegetable oils. Fruits and vegetables are foods that provide a wide range of nutrients. Bariatric surgery patients have a high risk of folic acid deficiency which can be caused by decreased fruit and vegetable intake [28, 31]. Schweiger et al. [32] conducted a study that assessed the food tolerance of patients. He found that patients were tolerant of vegetables and salads not only in the first months after surgery but also through 12 subsequent months. Quadros et al. [34] found a similar result. Vegetable oils, which also are included in the third level of the pyramid, are vehicles of fat-soluble vitamins, sources of essential fatty acids, and have the characteristic of increasing satiety. However, these oils are highly caloric. Because only moderate intake of vegetable oils is recommended, patients after surgery are at risk for developing liposoluble vitamin deficiencies [27, 30, 35]. There was a high percentage of patients with insufficient intake of oils. This may have been because patients did not report consumption because vegetable oils are considered forbidden foods. Another reason is that patients may not consider vegetable oil a food because it is consumed in small quantities. Some studies have found a high prevalence of food intolerance postoperatively from carbohydrates. Rice, noodles, and bread intolerances were reported most often [22, 32, 34, 36, 37]. Faria et al. [38] conducted a study that analyzed food
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intake and monthly weight loss of 89 bariatric surgery patients. They found that daily intake of carbohydrates, as well as the glycemic load of the meal, is negatively associated with monthly weight loss. In fact, this may have influenced weight loss by 63 %. Therefore, it is necessary to verify the consumption of carbohydrates and glycemic load in long-term nutritional monitoring of these patients to prevent weight regain. The top of the pyramid includes foods that must be avoided by patients. These foods are sugars, fats, and carbonated and alcoholic beverages. Foods containing sugar, such as chocolates, candies, ice cream, and cakes, provide extra calories that inhibit weight loss. Moreover, these foods are highly osmotic and can cause dumping syndrome [8, 27, 35]. Cruz and Morimoto [37] observed that the frequency of vomiting among patients in the postoperative period is related to the intake of fatty foods or concentrated sweets. Consumption of carbonated beverages with sugar is associated with high caloric intake, weight gain, and negative interactions with the bioavailability of some micronutrients (e.g., iron and calcium) [39]. Alcohol provides a high dietary intake of calories and avoids fat oxidation. High intake of alcohol diminishes the effectiveness of weight loss, favors the development of vitamin and mineral deficiencies, decreases bone mass, and increases nutritional medical complications. Thus, it is recommended that bariatric surgery patients drink alcohol with caution [27]. One year after surgery, a significant increase in the consumption of carbohydrates, sugars, and fats were found (i.e., patients tended to return to previous habits). Foods high in fat, such as sausages, pates, fried foods, fatty meats, and cheeses, should be avoided because of possible intolerances and the high level of saturated fats. In addition, these foods are highly caloric, which inhibits weight loss and facilitates weight regain [27]. Lima and Sampaio [19] found that severely obese patients who have not undergone bariatric surgery had a high fat intake. These habits can persist and recur after surgery, justifying high fat intake in this population. In this study, the method we used to assess food consumption has some weaknesses. These weaknesses include a limited amount of information collected on the quantities of food and beverages and the possibility that patients may not report foods they know are unhealthy. Nevertheless, our results give valuable information to improve nutritional counseling for this population. After bariatric surgery, patients not only have the benefit of weight loss but also have the opportunity to improve the quality of their food intake [16]. However, for these benefits to occur, it is important for these patients to have long-term periodic nutritional monitoring. According to the literature, there is a possible chance of weight regain in the second year following surgery [36]; thus, at year 2, there should be high attention given to nutritional analysis of food intake. This should be the objective of research studies.
Conclusion In this study, we identified inadequacies in lifestyle and eating habits of the bariatric surgery patients. We found that a low proportion of the population engaged in physical activity, used vitamin–mineral supplements, and consumed adequate amounts of foods from the protein, fruit, vegetable, and vegetable oils food groups. Moreover, we observed a high consumption of carbohydrates, sugars, and fats at both 6 months and 1 year postoperatively. Although the bariatric surgery patients in this study lost an appropriate amount of weight, it is likely that these patients may regain weight due to poor dietary intake and the return to old eating habits. In addition, these patients also may develop severe nutritional deficiencies and have comorbidities that existed preoperatively. Conflict of Interest Fernando Lucas Soares, Larissa Bissoni de Sousa, Carla Corradi Perini, Magda Rosa Ramos da Cruz, Mario Gilberto Jesus Nunes, and Alcides José Branco-Filho report no conflicts of interest and make no disclosures.
References 1. Owens TM. Morbid obesity: the disease and comorbidities. Crit Care Nurse Q. 2003;26(2):162–5. PMID: 12744597. 2. Livhits M, Mercado C, Yermilov I, et al. Is social support associated with greater weight loss after bariatric surgery? A systematic review. Obes Rev. 2010;12:142–8. PMID: 20158617. 3. Xanthakos SA. Nutritional deficiencies in obesity and after bariatric surgery. Pediatr Clin N Am. 2009;56(5):1105–21. PMID: 19931066. 4. Aasheim ET, Björkman S, Søvik TT, et al. Vitamin status after bariatric surgery: a randomized study of gastric bypass and duodenal switch. Am J Clin Nutr. 2009;90(1):15–22. PMID: 19439456. 5. Davies DJ, Baxter JM, Baxter JN. Nutritional deficiencies after bariatric surgery. Obes Surg. 2007;17(9):1150–8. PMID: 18074487. 6. Shankar P, Boylan M, Sriram K. Micronutrient deficiencies after bariatric surgery. Nutrition. 2010;26(11–12):1031–7. PMID: 20363593. 7. Bloomberg RD, Fleishman A, Nalle JE, et al. Nutritional deficiencies following bariatric surgery: what have we learned? Obes Surg. 2005;15:145–54. PMID: 15802055. 8. Fujioka K. Follow-up of nutritional and metabolic problems after bariatric surgery. Diabetes Care. 2005;28:481–4. PMID: 15677821. 9. Committee AHSSAHN. Aills L, Blankenship J, Buffington C, Furtado M, Parrott J. ASMBS allied health nutritional guidelines for the surgical weight loss patient. Surg Obes Relat Dis. 2008;4(5 Suppl):S73–108. 10. Moizé VL, Pi-Sunyer X, Mochari H, et al. Nutritional pyramid for post-gastric bypass patients. Obes Surg. 2010;20(8):1133–41. PMID: 20401543. 11. Pinheiro ABV. Tabela para avaliação de consumo alimentar em medidas caseiras. 5th ed. São Paulo: Atheneu; 2008. 12. Pacheco M. Tabela de equivalentes, medidas caseiras e composição química dos alimentos. Rio de Janeiro: Rubio; 2006. 13. Moreira MA. Medidas caseiras no preparo de alimentos. Goiânia: AB; 2002. 14. Dymek MP, Grange D, Neven K, et al. Quality of life after gastric bypass surgery: a cross-sectional study. Obes Res. 2002;10(11): 1135–42. PMID: 12429877.
OBES SURG 15. Toledo CC, Camilo GB, Guimarães RL, et al. Qualidade de vida no pós-operatório tardio de pacientes submetidos à cirurgia bariátrica. Rev APS. 2010;13(2):202–9. 16. Júnior FCM, Júnior WSS, Filho NS, et al. Efeito da perda ponderal induzida pela cirurgia bariátrica sobre a prevalência de síndrome metabólica. Arq Bras Cardiol. 2009;92(6):452–6. PMID: 19629308. 17. Balduf LM, Kohn GP, Galanko JA, et al. The impact of socioeconomic factors on patient preparation for bariatric surgery. Rev Obes Surg. 2009;19:1089–95. PMID: 19517200. 18. Faria SL, Kelly E, Faria OP. Energy expenditure and weight regain in patients submitted to Roux-en-Y gastric bypass. Rev Obes Surg. 2009;19:856–9. PMID: 19399563. 19. Lima LP, Sampaio HAC. Caracterização socioeconômica, antropométrica e alimentar de obesos graves. Rev Ciênc Saúde Coletiva. 2007;12(4):1011–20. PMID: 17680159. 20. Júnior WS, Amaral JL, Nonino-Borges CB. Factors related to weight loss up to 4 years after bariatric surgery. Rev Obes Surg. 2011;21(11): 1724–30. PMID: 21509481. 21. Pedrosa IV, Burgos MGPA, Souza NC, et al. Aspectos nutricionais em obesos antes e após a cirurgia bariátrica. Rev Col Bras Cir. 2009;36(4):316–22. PMID: 20076921. 22. Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA. 2002;288:2793–6. PMID: 12472304. 23. World Health Organization. Obesity. Preventing and managing the global epidemic. Report of a WHO consultation on obesity. WHO/ NUT/NCD/981. Geneva: WHO; 1998. PMID: 11234459. 24. Jacobi D, Ciangura C, Couet C, et al. Physical activity and weight loss following bariatric surgery. Rev Obes Rev. 2011;12:366–77. PMID: 20331508. 25. Lizer MH, Papageorgeon H, Glembot TM. Nutritional and pharmacologic challenges in the bariatric surgery patient. Rev Obes Surg. 2010;20:1654–9. PMID: 20107919. 26. Wardé-Kamar J, Rogers M, Flancbaum L, et al. Calorie intake and meal patterns up to 4 years after Roux-en-Y gastric bypass surgery. Rev Obes Surg. 2004;14:1070–9. PMID: 15479596. 27. Rubio MA, Moreno C. Implicaciones nutricionales de la cirugía bariátrica sobre el tracto gastrointestinal. Rev Nutr Hosp. 2007;22(2):124–34. PMID: 17679300.
28. Bordalo LA, Salesteixeira TF, Bressan J, et al. Cirurgia bariátrica: como e por que suplementar. Rev Assoc Med Bras. 2011;57(1):113– 20. PMID: 21390468. 29. Sallé A, Demarsy D, Poirier AL, et al. Zinc deficiency: a frequent and underestimated complication after bariatric surgery. Rev Obes Surg. 2010;20:1660–70. PMID: 20706804. 30. Ziegler O, Sirveaux MA, Brunaud L, et al. Medical follow-up after bariatric surgery: nutritional and drug issues. General recommendations for the prevention and treatment of nutritional deficiencies. Diabetes Metab. 2009;35:544–57. PMID: 20152742. 31. Vargas-Ruiz AG, Hernández-Rivera G, Herrera MF. Prevalence of iron, folate, and vitamin B12 deficiency anemia after laparoscopic Roux-en-Y gastric bypass. Rev Obes Surg. 2008;18:288–93. PMID: 18214631. 32. Schweiger C, Weiss R, Keidar A. Effect of different bariatric operations on food tolerance and quality of eating. Rev Obes Surg. 2010;20:1393–9. PMID: 20680506. 33. Viégas M, Vasconcelos RS, Neves AP, et al. Cirurgia bariátrica e metabolismo ósseo: uma revisão sistemática. Arq Bras Endocrinol Metab. 2010;54(2):158–63. PMID: 20485904. 34. Quadros MRR, Savaris AL, Ferreira MV, et al. Intolerância alimentar no pós-operatório de pacientes submetidos à cirurgia bariátrica. Rev Bras Nutr Clin. 2007;22(1):15–9. 35. Parkes E. Nutritional management of patients after bariatric surgery. Am J Med Sci. 2006;331(4):207–13. PMID: 16617236. 36. Hernández MAR, Sancho EM, Fuster MA, et al. Comparación a 5 años de dos técnicas de cirugía bariátrica en pacientes con obesidad mórbida seguidos en consulta enfermera. Rev Nutr Hosp. 2009;24(6):667–75. PMID: 20049369. 37. Cruz MRR, Morimoto IMI. Intervenção nutricional no tratamento cirúrgico da obesidade mórbida: resultados de um protocolo diferenciado. Rev Nutr. 2004;17(2):263–72. 38. Faria SL, Faria OP, Lopes TC, et al. Relation between carbohydrate intake and weight loss after bariatric surgery. Rev Obes Surg. 2009;19:708–16. PMID: 18618210. 39. Vartanian LR, Schwartz MB, Brownell KD. Effects of soft drink consumption on nutrition and health: a systematic review and metaanalysis. Am J Public Health. 2007;97(4):667–75. PMID: 17329656.
