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OBES SURGDOI 10.1007/s11695-016-2064-9 ORIGINAL CONTRIBUTIONS Nutritional Status Prior to Laparoscopic SleeveGastrectomy Surgery Shiri Sherf Dagan 1,2,3 & Shira Zelber-Sagi3,4 & Muriel Webb3 & Andrei Keidar1,5 &Asnat Raziel2 & Nasser Sakran 2,6 & David Goitein1,2,7 & Oren Shibolet1,3 # Springer Science+Business Media New York 2016 Results One-hundred patients completed the pre-operative Background Two main causes for nutrient deficiencies fol- measurements (60 % female) with a mean age of 41.9 lowing bariatric surgery (BS) are pre-operative deficiencies ± 9.8 years and a mean BMI of 42.3 ± 4.7 kg/m2. Pre-opera- and favoring foods with high-energy density and poor micro- tively, deficiencies for iron, ferritin, folic acid, vitamin B1, nutrient content. The aims of this study were to evaluate nu- vitamin B12, vitamin D, and hemoglobin were 6, 1, 1, 6, 0, tritional status and gender differences and the prevalence of 22, and 6 %, respectively. Pre-surgery, mean energy, protein, nutritional deficiencies among candidates for laparoscopic fat, and carbohydrate intake were 2710.7 ± 1275.7 kcal/day, sleeve gastrectomy (LSG) surgery.
114.2 ± 48.5, 110.6 ± 54.5, and 321.6 ± 176.1 gr/day, respec- Methods A cross-sectional analysis of pre-surgery data col- tively. The intakes for iron, calcium, folic acid, vitamin B12, lected as part of a randomized clinical trial on 100 morbidly and vitamin B1 were below the Dietary Reference Intake obese patients with non-alcoholic fatty liver disease (NAFLD) (DRI) recommendations for 46, 48, 58, 14, and 34 % of the admitted to LSG surgery at Assuta Medical Center between study population, respectively.
February 2014 and January 2015. Anthropometrics, food in- Conclusion We found a low prevalence of nutritional defi- take, and fasting blood tests were evaluated during the base- ciencies pre-operatively except for vitamin D. Most micronu- trient intake did not reach the DRI recommendations, despite Shiri Sherf Daganshirisherf@gmail.com Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel Shira Zelber-Sagi Assuta Medical Center, Tel Aviv, Israel Department Gastroenterology, Tel-Aviv Medical Center, 6 Weizman St., 6423906 Tel-Aviv, Israel School of Public Health, Faculty of Social Welfare and Health Sciences, University of Haifa, Haifa, Israel The Department of Surgery, Rabin Medical Center, Campus Beilinson, Petach Tiqva, Israel Department of Surgery A, Emek Medical Center, Afula, Israel Department of Surgery C, Sheba Medical Center, Tel high-caloric and macronutrient intake indicating a poor die- the Assuta hospitals' bariatric multidisciplinary team to undergo tary quality.
BS (the team includes registered dietitian, social worker/phycol-ogist, internist/ endocrinologist, and surgeon), ultrasound- Keywords Obesity . Bariatric surgery . Micronutrient diagnosed NAFLD, and ability to sign an informed consent.
deficiencies . Dietary supplements . Food intake Major exclusion criteria were fatty liver suspected to be second-ary to hepatotoxic drugs, excessive alcohol consumption ],mental illness or cognitive deterioration, and previous BS. Dia- betic patients who were treated with anti-diabetic medicationsother than treatment with metformin at a stable dose for at least Bariatric surgery (BS) is currently the most effective treatment 6 months exclusively were also excluded.
modality for obesity and its associated metabolic complica- Prior to their meeting with the bariatric multidisciplinary tions []. The main benefits of this intervention include team, all patients must be evaluated and cleared by a registered prolonged weight loss, improvement of associated comorbid- dietitian. The registered dietitian assesses each patient's indi- ities, and quality of life The total number of BS performed vidual nutritional needs and food intake history, reviews prop- worldwide in 2013 were 468,609; 37 % of them were laparo- er nutrition, and discusses protein intake, and vitamin and scopic sleeve gastrectomy (LSG) surgeries In Israel, 11, mineral supplementation needs post-surgery. All patients get 452 people with morbid obesity underwent BS in 2013 and a recommendation by the registered dietitian to use supple- LSG was the leading procedure []. All candidates for BS ments if nutritional deficiencies are detected. In addition, 2– undergo pre-operative nutritional evaluation, including micro- 3 weeks before the surgery, all patients are recommended to nutrient measurements [It was previously shown that if follow a low-carbohydrate diet and during that time, to take a micronutrient deficiencies are not detected and corrected, they daily multivitamin supplement ].
may influence post-operative morbidity and even mortality The baseline evaluations were performed on average 24 [According to recently published studies, the pre- ± 12 days pre-surgery. Medical history for comorbidities was operative deficiency prevalence for vitamin B12 is 13–18 %, obtained from the patients' medical records.
for iron is 8–47 %, for folic acid is 0–32 %, for vitamin D is25–99 %, and for vitamin B1 is 0–29 % –].
Causes of nutritional deficiencies in obesity are multifacto- Biochemical Evaluation rial and include high intake of foods with high caloric densityand low nutritional quality, defective storage and bio- Each participant underwent biochemical testing, following a availability of some nutrients (e.g., vitamin D), increased 12 h fast, for lipid panel, glucose, HbA1C, insulin, C-reactive hepcidin synthesis leading to reduce iron absorption due to protein (CRP), vitamin B1, vitamin B12, vitamin D, iron, ferri- chronic inflammation, and small intestinal bacterial over- tin, folic acid, and hemoglobin (Hb). Patients were asked not to growth which may consume vitamin B1 and B12 and fat- take supplements a day before blood was drawn in order not to soluble vitamins leading to their absence cause spuriously elevated levels. Deficiency of a vitamin or a Causes and mechanisms of nutrient deficiencies following mineral was defined as a plasma level below the reference range BS are also multifactorial and are influenced by type of proce- recommended by the kit manufacturer (Fig. ).
dure, pre-operative deficiencies, sustained post-operativevomiting, food intolerance, modified eating behavior, and non-adherence to dietary and supplement recommendations The aims of our study were to evaluate and to compare be- tween genders, dietary intake, and micronutrient deficiencies Weight and height were measured on a digital medical scale, among 100 candidates for LSG surgery with morbid obesity.
and waist circumference (WC) was measured twice at thelevel of the umbilicus by a single surveyor. BMI was calcu-lated using weight (in kilograms) divided by the height Materials and Methods squared (in square meter).
A cross-sectional analysis of pre-surgery data was collected aspart of a randomized clinical trial (RCT) of 6-month treatment Dietary Intake Evaluation with probiotic vs. placebo among 100 non-alcoholic fatty liverdisease (NAFLD) patients who underwent LSG surgery at the Patients filled out a detailed semi-quantitative food frequency Assuta Medical Center from February 2014 to January 2015.
questionnaire (FFQ) reporting their habitual nutritional intake Inclusion criteria were age between 18 and 65 years old, in the past year. The FFQ was assembled by the Food and BMI > 40 or BMI > 35 kg/m2 with comorbidities, approval of Nutrition Administration, Ministry of Health, and was Fig. 1 Prevalence ofmicronutrient deficiencies previously described in detail It was adjusted for the current study needs. Caloric, macronutrient, and micronutrientintake were assessed based on the Israeli nutrient software One-hundred patients completed the pre-operative measure- BZameret, which was developed by the Israeli Ministry of ments (60 % female). Their mean age was 41.9 ± 9.8 years and Health, and compared to recommended values of the Dietary the mean pre-operative BMI was 42.3 ± 4.7 kg/m2; 13 % were Reference Intake (DRI) recommendations [–].
diabetic (eight treated with metformin), 59 % had dyslipidemia,and 21 % had hypertension (Table Fifteen patients (15 %)began a low-carbohydrate diet with the additional multivitaminsupplementation 3–10 days before the baseline measurements.
Statistical Methods Pre-Surgery Nutritional Deficiencies Statistical analyses were performed using SPSS version 22(SPSS Inc., Chicago, IL, USA) software. The Kolmogorov- Pre-operative nutritional deficiencies were found in 6, 1, 0, 37, Smirnov test was used to assess whether the data were nor- 1, and 6 % of the participants for iron, ferritin, and vitamin mally distributed. Results were expressed as mean ± standard B12 for the laboratory cutoff (<175 pg/ml) and vitamin B12, deviation (SD) and/or by percentage. To test differences in folic acid, and vitamin B1 for the cutoff <350 pg/ml, respec- continuous variables between two groups, the independent tively. Vitamin D levels were categorized as deficiency sample t test was performed. Associations between nominal (<20 ng/ml) found in 22 % and insufficiency (<30 ng/ml) variables were performed with the Pearson's chi-squared test.
found in 83 % of the participants (Tables and ). Hemoglo- P < 0.05 was considered statistically significant for all bin was low in 6 % of the patients (Fig. ). No significant differences were found between genders for all micronutrient Table 1 Baseline characteristicsof the study sample 41.9 ± 9.8 (21.0–63.0) 43.5 ± 9.4 (24.0–63.0) 40.7 ± 10.0 (21.0–60.0) 121.2 ± 19.5 (86.0–203.5) 135.2 ± 19.6 (106.8– 111.9 ± 12.8 (86.0–149.6) 1.69 ± 0.09 (1.52–1.93) 1.78 ± 0.06 (1.66–1.93) 1.63 ± 0.05 (1.52–1.74) 42.3 ± 4.7 (34.6–60.0) 42.6 ± 5.1 (34.6–60.0) 42.1 ± 4.4 (34.7–55.0) 124.3 ± 12.3 (101.0– 131.0 ± 11.9 (109.0– 119.9 ± 10.5 (101.0– Type 2 diabetes (%) Thalassemia minor Current smoker (%) BMI body mass index, WC waist circumferencea Values are expressed as the average ± standard deviation (range) Table 2 The prevalence of pre-operative treatment with different All population (%) dietary supplements Other supplements Total vitamins and minerals deficiencies. Only 10 % of women and 18.3 % of men did not ± 1275.7 kcal/day, 114.2 ± 48.5 gr/day (17 % of calories), present any nutritional deficiency pre-surgery.
1.0 ± 0.4 gr/day, 110.7 ± 54.5 gr/day (36 % of calories), and321.6 ± 176.1 gr/day (47 % of calories), respectively, which is Pre-Surgery Nutritional Intake above the DRI recommendations. Mean fiber intake was 28.1± 16.5 gr/day for men, which is below the DRI recommenda- Mean energy, protein, protein intake per kilogram of body tions, and 34.8 ± 24.3 gr/day for women, which is adequate to weight, and fat and carbohydrate intake were 2710.7 the DRI recommendations. Mean sugar-sweetened beverages Table 3 Biochemical parametersand comparison between men and 70–100Insulin (mcu/ml) Diabetes ≥6.5 %Tg (mg/dl) 50–150TC (mg/dl) 150–200HDL (mg/dl) M 35–70; W 39–90LDL (mg/dl) 60–160CRP (mg/l) 0–5Iron (μg/dl) 40–150Ferritin (ng/ml) M 14–163; W 7.1–151Vitamin B12 (pg/ml) 175–961Vitamin B1 (pg/ml) 32–95Folic acid (ng/ml) 2.6–17.1Vitamin D (ng/ml) Insufficiency 20–30Deficiency <20 M 13.2–17; W 11.7–15.5 TC total cholesterol, LDL-C low-density lipoprotein cholesterol, HDL-C high-density lipoprotein cholesterol, Tgtriglycerides, CRP C-reactive protein, HbA1C hemoglobin A1c, Hb hemoglobina Values are expressed as the average ± standard deviation and sweets and desserts were 1.1 ± 2.2 cups/day and 2.7 ± 3.4 except for meat and processed meat intake which were found servings/day, respectively. Mean meat (all kinds) and proc- higher for men than women (Table ).
essed meat were 1.4 ± 1.1 and 0.4 ± 0.8 servings/day, The intake of iron, calcium, folic acid, vitamin B12, and vitamin B1 were found to be as under the DRI recommenda- No significant differences were found between genders for tions for 46, 48, 58, 14, and 34 % of the study population, all macronutrient, micronutrient, and food group intake, respectively (Fig. Table 4 Nutritional intake andcomparison between men and Energy/day (kcal) 2,710.7 ± 1,275.7 2,615.6 ± 1,215.7 2,774.2 ± 1,320.4 Protein (gr) per weight (kg) Carbohydrates/day (gr) Magnesium/day (mg) Phosphorus/day (mg) Potassium/day (mg) 4,125.0 ± 2,331.2 3,866.4 ± 1,847.7 4,297.4 ± 2,605.2 4,664.8 ± 2,508.9 4,463.4 ± 2,078.7 4,800.0 ± 2,767.7 Vitamin A/day (IU) 10,169.8 ± 9,941.4 8,320.5 ± 6,019.9 11,402.7 ± 11,748.1 Vitamin E/day (mg) Vitamin C/day (mg) Vitamin B1/day (mg) Vitamin B2/day (mg) Vitamin B3/day (mg) Vitamin B6/day (mg) Folic acid/day (μg) Vitamin B12/day (μg) Cholesterol/day (mg) Saturate fat acid/day (gr) Meat (all kinds)/dayb Processed meat/dayb Sweets and desserts/dayb Soft drinks (cups)/day IU international unit, MUFA monounsaturated fatty acid, PUFA polyunsaturated fatty acid, DHAdocosahexaenoic acid, EPA eicosapentaenoic acida Values are expressed as the average ± standard deviationb Serving/day Fig. 2 Prevalence ofmicronutrient intake below theDRI recommendations [, ] Nutritional Deficiencies by Dietary Supplement Intake population consumed more sugar-sweetened beverages andsweets and desserts than the WHO's current recommendation The majority (59 %) of the study population undertook dietary for sugar consumption [], more than double of the WHO's supplementation, with similar distribution across gender ex- current recommendation for sodium consumption ], and cept for lower vitamin D supplementation among men (32.5 more processed meat than the World Cancer Research Fund vs. 58.3 % for men and women, p = 0.011, respectively) public health recommendations which is more reminis- (Table ). Mean vitamin B12 and folic acid levels were sig- cent of a Western diet pattern. This diet may have negative nificantly higher in users of dietary supplementation com- effects on health, specifically on the risk for NAFLD, obesity, pared to non-users (448.8 vs. 376.3 pg/ml, p = 0.021, and 9.9 metabolic syndrome, type 2 diabetes, cardiovascular disease, vs. 8.1 ng/ml, p = 0.031, respectively). No other differences in and cancer [].
nutritional status were noted between supplement users and Overall, we found a low prevalence of pre-operative nutri- tional deficiencies. Our findings are in contrast to other studiesdemonstrating more pronounced vitamin deficiencies amongmorbidly obese patients. However, vitamin D was found with high-deficiency prevalence, similar to previous studies , Two main causes for nutrient deficiencies following BS are Reasons discussed for high prevalence of vitamin D defi- pre-operative deficiencies and inappropriate eating behavior, ciency among morbidly obese patients were inadequate in- favoring foods with high-energy density and poor micronutri- take, reduced sun exposure, and decreased bioavailability of ent content There is limited information available regard- vitamin D due to it being deposited in adipose tissue ing dietary intake by obese patients prior to BS. The current There is no consensus defining optimal 25-hydroxyvitamin study shows that most micronutrient intake did not reach to D concentrations. Growing evidence suggests that the DRI recommendations, despite high-caloric and macronu- levels > 30 ng/ml may be sufficient to maintain health ].
trient intake pre-operatively, which point to a consumption of We examined deficiencies for vitamin B12 with the labo- poor quality diet low in micronutrients. Few previous studies ratory cutoff (<175 pg/ml) and also acut off <350 pg/ml. Lab- reported also on low consumption of micronutrients in the diet oratory cutoff values do not rule out the diagnosis of vitamin B12 deficiency in patients with compatible clinical abnormal- In our study, average energy intake was higher than the ities. However, serum vitamin B12 with the cutoff 350 pg/ml recommended caloric intake by age and gender of the 2010 has sensitivity of 90 % and specificity of 25 % for detecting American dietary guidelines for both genders [], but similar elevated level of methylmalonic acid, which is a more accu- to studies in Chilean women and a Spanish population, seek- rate marker of clinical vitamin B12 deficiency []. Further ing BS and higher in 500 kcal/day than another study studies should test this cutoff for BS patients.
in 355 Spanish patients prior to BS [].
Hemoglobin level below normal range was found in just The analysis of macronutrient intake in our population six patients, two of them with the genetic trait of Thalassemia shows that energy obtained from fat intake (36 % of calories) minor known to affect hemoglobin levels [. The main was higher compared to the DRI recommendations (20– causes of anemia are deficiencies in iron, vitamin B12, and 35 %), while energy obtained from carbohydrate intake folate which were found to be with low prevalence in our (47 % of calories) was in the lower limits of the DRI recom- population study. Those results are supported by a few studies mendations (45–60 %) []. This macronutrient distribution is [, ] but in contrast to other studies that show higher more typical to the Mediterranean diet pattern. However, our anemia prevalence , ].
There are several explanations for the lower frequency of All procedures performed in this study were ap- proved by the institutional research committees in both participating hos- micronutrient deficiencies seen in our study as compared to pitals and in accordance with the ethical standards of the 1964 Helsinki previously reported data.
Declaration and its later amendments or comparable ethical standards.
Overall, 59 % of our study population reported taking supple- The study was pre-registered in the NIH registration website (TRIAL ments at the baseline measurements, but unfortunately, we lack no. NCT01922830).
data regarding the exact type and duration of supplement used.
Statement of Informed Consent Informed consent was obtained from There is a lack of data on supplement consumption prior to all individual participants included in the study.
BS, and few studies have shown that only 1–2 % of patientsreceived supplements pre-surgery , Although we did The Research Projects and Fellowships Fund on Food and Nutrition with Implications on Public Health (grant number 3–10470).
not assess adherence to supplementation recommendations,we observed higher levels of folic acid and B12 levels in par-ticipants that reported the use of supplementation. Thus, wesuggest a possible positive effect of pre-operative supplemen-tation on the prevention of nutritional deficiencies. We assume the participants' commensurate high socioeconomic status canbe related to high adherence for supplements prior to the sur- Colquitt JL, Pickett K, Loveman E, Frampton GK. Surgery for gery. Furthermore, this cross-sectional study is part of a RCT.
weight loss in adults. The Cochrane Database of Systematic Those trials are frequently performed in a highly motivated population of patients with high adherence rates to treatment de Lima KV, Costa MJ, Goncalves Mda C, Sousa BS.
]. We suggest that accurate assessment of adherence is cru- Micronutrient deficiencies in the pre-bariatric surgery. Arquivosbrasileiros de cirurgia digestiva : ABCD = Brazilian archives of cial and relevant in understanding the true effectiveness of sup- digestive surgery. 2013;26 Suppl 1:63–6 plements and should be part of future research ].
Angrisani L, Santonicola A, Iovino P, Formisano G, Buchwald H, Our study has several limitations. First, it had a relatively Scopinaro N. Bariatric surgery worldwide 2013. Obesity surgery.
small sample size; however, the numbers are similar to previ- Mechanick JI, Youdim A, Jones DB, Garvey WT, Hurley DL, ously reported studies. Secondly, we did not measure some McMahon MM, et al. Clinical practice guidelines for the perioper- important micronutrients such as zinc, selenium, copper, and ative nutritional, metabolic, and nonsurgical support of the bariatric vitamin C. It is important to note that these micronutrients are surgery patient—2013 update: cosponsored by American hard to measure and expensive, making them unlikely to be- Association of Clinical Endocrinologists, The Obesity Society,and American Society for Metabolic & Bariatric Surgery. Obesity come a routine part of clinical routines. Thirdly, the study may (Silver Spring, Md). 2013;21 Suppl 1:S1–27.
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They were of high socioeconomic status and may have been Isom KA, Andromalos L, Ariagno M, Hartman K, Mogensen KM,Stephanides K, et al. Nutrition and metabolic support recommen- more compliant to supplement treatment. However, to the best dations for the bariatric patient. Nutrition in clinical practice : offi- of our knowledge, they represent similar populations world- cial publication of the American Society for Parenteral and Enteral wide, especially in Western countries.
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