Serum Vitamin and Trace Element Levels of Patients Undergoing Laparoscopic Sleeve Gastrectomy

Abstract

Aim:

The aim of this study was to determine the change in serum vitamin and trace element levels of patients undergoing laparoscopic sleeve gastrectomy (LSG), which is one of the bariatric surgery methods used as a treatment of obesity.

Materials and Methods:

The severely obese patients who planned to undergo LSG surgery were included in the study. The anthropometric measurements and blood samples of patients were taken preoperatively and at the third month of postoperative follow-up. The results obtained from serum samples collected for routine postbariatric surgery biochemical test panel were evaluated by clinical biochemistry specialists based on the reference intervals indicated in the kit insert. The data were analyzed using SPSS 25 Package Program with independent samples t-test.

Results:

Serum Se²⁻, total iron-binding capacity, mean corpuscular hemoglobin, and folate mean values of the patients decreased after surgery. There was no statistically significant difference of serum Mg²⁺, Zn²⁺, Fe²⁺, hemoglobin, red blood cell count, mean corpuscular volume, ferritin, and vitamin B₁₂ mean values at postoperative follow-up at third month.

Conclusion:

This study showed that multidisciplinary evaluation of patients' preoperative nutritional profile with clinical biochemistry specialists, dietitian, and bariatric surgery team is essential for planning of surgery and sufficient postoperative follow-up. To better understand the effects of bariatric surgery on micronutrient status, studies with bigger sample size and longer follow-up are needed.

Introduction

Obesity is a rapidly increasing health problem worldwide. In developed countries, the prevalence of obesity in adults has tripled in the last decade and reached ∼20–35% of the general population. Obesity is considered as one of the most common causes of death in the world leading to chronic diseases, including type 2 diabetes mellitus, ischemic heart disease, hypertension, and various types of cancers.^1,2

It has been proved in both clinical and randomized controlled trials that the most effective way of treatment of severe obesity and obesity related comorbidities is bariatric surgery.^3–9 Roux-en-Y gastric bypass (RYGB) and laparoscopic sleeve gastrectomy (LSG) are the most common bariatric surgery methods. RYGB surgery is a bariatric surgical method that allows the 15–20 mL gastric pouch to be connected to the small intestine by gastrojejunostomy and enables the rapid passage of nutrients into the small intestine. It provides ∼25–30% weight loss after surgery.^10,11 LSG is a type of partial gastrectomy with longitudinal resection of the stomach with a gastric pouch of ∼100 mL. LSG was initially used as a part of the duodenal switch method, but it is now used commonly as a bariatric surgery method because it provided 20–30% weight loss after surgery and has a lower risk of complications compared to other methods.^10,12

Being an effective method for the treatment of obesity and comorbidities, bariatric surgery has some complications such as micronutrient deficiencies after surgery. Various reasons have been proposed in such studies conducted to explain vitamin and mineral deficiencies after bariatric surgery; including that some of the obese patients may have vitamin and mineral deficiencies in the preoperative period, postoperative decrease in absorption in the gastrointestinal tract or deficiency due to inadequate nutritional intake because of change in feeding patterns after surgery. Vitamin B₁₂, folate, and iron deficiency are common in the early period after bariatric surgery and calcium, vitamin D, and trace element deficiencies are also observed.¹³

Trace element deficiencies in the postoperative period after bariatric surgery are not unexpected, especially after RYGB surgery, selenium and zinc absorption in the duodenum is decreased and it can be shown as a major factor of deficiency.¹⁴ However, current data on changes in serum trace element and vitamin levels before and after bariatric surgery are limited. Studies in the literature are generally focused on RYGB surgery. In particular, data on LSG surgery, which is also the surgical method of patients who have been included in our study, are limited.

The aim of our study was to determine the changes in serum vitamin and trace element levels of LSG surgery performed on severely obese patients.

Materials and Methods

A prospective study was conducted, including 58 patients who underwent LSG between December 2018 and April 2019 at Bakirkoy Dr. Sadi Konuk Training & Research Hospital in General Surgery Department, Istanbul, Turkey. Included patients were between ages of 18 and 65 and all the experimental procedures were conducted by following hospital approved guidelines. A signed consent form was collected from all patients. The study has been approved by hospital Ethics Committee (number: 2018-14-07).

Patients diagnosed with severe obesity with a body mass index (BMI) >40 or >35 kg/m² plus obesity related comorbidities were included in the study.

Exclusion criteria were preoperative use of medication or presence of any diseases that may affect absorption in intestines, current reversible endocrine, or other disorders that can cause obesity, preoperative gut malabsorption syndrome.

The surgical method was LSG, which standardized and remained the same throughout the whole study period. All patients included in our study were recommended to follow the same diet plan suitable for postoperative period at the general surgery department of the hospital. The diet recommendations were planned according to Allied Health Nutritional Guidelines for the Surgical Weight Loss Patient of American Society for Metabolic and Bariatric Surgery (ASMBS) Nutrition Committee. After the operation, no nutritional supplements were prescribed, which may affect the results and none of the patients had used nutritional supplements before and after surgery during the trail.

Anthropometric measurements and blood samples were taken from patients who underwent LSG, before and at the third month follow-up after surgery. Patients' height and body weight were determined and BMI was calculated before and after surgery. The demographic characteristics of the patients were obtained with a questionnaire for our study.

Biochemical assessment

Serum samples collected for routine biochemistry tests were analyzed on Beckman Coulter AU 5800 and Beckman Coulter DXI 800 devices, and whole blood count on Sysmex XN1000 device. Kits supplied by the device manufacturers were used for analyses. For the evaluation of the results, the reference intervals stated in the package insert are used and approved by the biochemists. The method information of the tests studied in the devices are as follows: completed blood count; current meter method, magnesium; by enzymatic (isocitrate dehydrogenase) method, iron; colorimetric method, iron-binding capacity (IBC); colorimetric method, folate; immunoenzymatic method, ferritin; immunoenzymatic method, vitamin B₁₂; immunoenzymatic method, selenium; ICP MS (inductively coupled plasma mass spectrometry) method, zinc; and ICP was measured by MS method.

Statistical analysis

All analyses were processed using the IBM^® Statistical Package for the Social Sciences^® (SPSS^®) version 25. Values are reported as mean ± standard deviation (SD) of the mean unless otherwise specified. To examine micronutrient status of the patients at two different time points, an independent samples t-test was performed. A value of p < 0.05 was considered statistical significance.

Results

Demographic and anthropometric characteristics of the study population are shown at Table 1. A total number of 58 severely obese patients aged between 18 and 65 years were included to study (44 women and 14 men). The mean weight before LSG was 127 ± 17.96 kg (SD), mean BMI 47.6 ± 4.90 kg/m², and mean age 39.4 ± 10.8 years (Table 1). A marked reduction in weight and BMI was observed following LSG. At the third month of follow-up, mean weight was 98 ± 14.98 kg and mean BMI was 37 ± 4.45 kg/m².

Table 1.

Characteristics of Study Population (n = 58)

Gender
Male, n (%)	14 (24.1)
Female, n (%)	44 (75.9)
Age, years	39.4 ± 10.8
Weight (preop), kg	127 ± 17.96
Weight (postop), kg	98 ± 14.98
BMI (preop), kg/m²	47.6 ± 4.90
BMI (postop), kg/m²	37 ± 4.45

Results are expressed as mean ± SD.

BMI, body mass index; SD, standard deviation.

Mean serum Mg²⁺ level of the patients was 2 ± 0.9 mg/dL preoperatively, and the mean serum level was 2.04 ± 0.24 mg/dL at the third month of follow-up (Tables 2–5). We had compared the preoperative mean serum Mg²⁺ levels and postoperative mean serum levels of patients using t-test and no statistically significant difference was found (p = 0.170).

Table 2.

Mean Levels and Standard Deviations of Patients' Serum Trace Elements Levels in Preoperative and Postoperative Periods

Parameters	Preoperative		Postoperative		T	p
Parameters	Mean	SD	Mean	SD	T	p
Mg²⁺(mg/dL)	2	0.19	2.04	0.24	−1.38	0.170
Se²⁻ (μg/L)	74.33	9.55	66.98	8.61	5.98	<0.001^a
Zn²⁺ (μg/L)	0.85	0.08	0.87	0.12	−1.41	0.16

Statistical significance was set at p < 0.05.

Independent samples t-test was applied.

Table 3.

Mean Levels and Standard Deviations of Patients' Serum Vitamin and Trace Elements Levels in Preoperative and Postoperative Periods

Parameters	Preoperative		Postoperative		T	p
Parameters	Mean	SD	Mean	SD	T	p
Fe²⁺ (μg/dL)	66.66	34.23	64.34	23.54	0.5	0.619
IBC (μg/dL)	370.91	57.37	331.98	62.58	5	<0.001^a
HGB (g/dL)	13.13	1.62	13.39	1.42	−1.87	0.06
MCH (pg)	27.01	2.11	27.39	1.81	−2.17	<0.001^a
RBC (10⁶/μL)	4.86	0.42	4.88	0.41	−0.57	0.56
MCV (fL)	82.37	4.7	82.46	4.01	−0.21	0.83

Statistical significance was set at p < 0.05.

Independent samples t-test was applied.

IBC, iron-binding capacity; HGB, hemoglobin; MCH, mean corpuscular hemoglobin; MCV, mean corpuscular volume; RBC, red blood cell count.

Table 4.

Mean Levels and Standard Deviations of Patients' Serum Vitamin and Trace Elements Levels in Preoperative and Postoperative Periods

Parameters	Preoperative		Postoperative		T	p
Parameters	Mean	SD	Mean	SD	T	p
Vitamin B₁₂ (pmol/L)	235.46	116.11	265	220.26	−0.96	0.33
Ferritin (mg/L)	59.63	58.69	49.39	47.05	1.96	0.05
Folate (ng/mL)	7.85	3.28	6.51	2.49	4.15	<0.001^a

Statistical significance was set at p < 0.05.

Independent samples t-test was applied.

Table 5.

Mean Levels and Standard Deviations of Patients' Serum Vitamin and Trace Elements Levels in Preoperative and Postoperative Periods

Parameters	Preoperative		Postoperative		T	p
Parameters	Mean	SD	Mean	SD	T	p
Mg²⁺ (mg/dL)	2	0.19	2.04	0.24	−1.38	0.170
Se²⁻ (μg/L)	74.33	9.55	66.98	8.61	5.98	<0.001^a
Zn²⁺ (μg/L)	0.85	0.08	0.87	0.127	−1.41	0.163
Vitamin B₁₂ (pmol/L)	235.46	116.11	265	220.26	−0.96	0.33
Ferritin (mg/L)	59.63	58.69	49.39	47.05	1.96	0.05
Folate (ng/mL)	7.85	3.28	6.51	2.49	4.15	<0.001^a
Fe²⁺ (μg/dL)	66.66	34.23	64.34	23.54	0.5	0.619
IBC (μg/dL)	370.91	57.37	331.98	62.58	5	<0.001^a
HGB (g/dL)	13.13	1.62	13.39	1.42	−1.87	0.06
MCH (pg)	27.01	2.11	27.39	1.81	−2.17	<0.001^a
RBC (10⁶/μL)	4.86	0.42	4.88	0.41	−0.57	0.56
MCV (fL)	82.37	4.7	82.46	4.01	−0.21	0.83

Statistical significance was set at p < 0.05.

Independent samples t-test was applied.

Mean serum Se²⁻ levels statistically decreased after third month of LSG (p < 0.001). Mean Serum Se²⁻ level of the patients was 74.33 ± 9.55 μg/L preoperatively, and the mean serum level was 66.98 ± 8.61 μg/L at the third month of follow-up (Table 2).

The mean serum Fe²⁺, hemoglobin, red blood cell count, and mean corpuscular volume (MCV) levels did not change over time, no statistically significant difference was found between preoperative and postoperative periods (p = 0.619; p = 0.06; p = 0.56; p = 0.83). Mean serum total iron-binding capacity (TIBC) and MCV values were statistically lower compared with values before surgery (p < 0.001) (Tables 3–5).

The mean serum folate level statistically decreased within the first 3 months after intervention (p < 0.01). Mean serum vitamin B₁₂ and ferritin levels remained stable after LSG, no statistically significant change was observed postoperatively (p = 0.33; p = 0.05) (Tables 4–5).

Discussion

Bariatric surgery is the most effective method in the treatment of obesity for both adults and adolescents in the cases when weight loss and treatment of obesity-related diseases cannot be achieved with diet, behavior change, and exercise. The present studies clearly confirm that bariatric surgery also improves quality of life by providing a positive effect on obesity's comorbidities, including hypertension, diabetes, hyperlipidemia, and obstructive sleep apnea.¹³ However, patients undergoing LSG are at severe risk of complications developing after surgery. Macro and micronutrient deficiencies are one of the most common complications.^15–18 These deficiencies are associated with reduced food consumption due to the reduced absorption of foods as a result of the physiological effect of surgery and anatomical changes in the gastro-intestinal tract, as well as the changing postoperative diet habits. Obese patients are also characterized with having vitamin and mineral deficiencies before surgery due to low quality of the foods they consume, even they generally consume high energy foods.¹⁸ Malabsorptive bariatric surgery methods (RYGB, biliopancreatic diversion) have a high risk of nutrient deficiencies in the postoperative period. Vitamins and trace elements act as enzymatic cofactors in various biochemical pathways in the human body, and their deficiencies can cause clinical effects that may include the neurological, cardiovascular, and gastrointestinal systems. Therefore, it is very important to follow the biochemical values after surgery. Data on LSG surgery, where food passes through the upper gastrointestinal tract faster but still contacts the antrum, duodenum, and proximal jejunum, are limited.¹⁹

Previous studies have indicated that iron malabsorption in patients with low ferritin or hemoglobin levels after LSG is due to reduced hydrochloric acid secretion after surgery or following the restricted diet at postoperative period and avoiding consuming meat products, which are sources of high bioavailable heme iron.^13,16 In addition, iron absorption and metabolism are associated with serum levels of other nutrients such as zinc, vitamin C, and copper. Dietary intake of large amounts of zinc may compete with iron during absorption and causes reduction of iron absorption. Dietary vitamin C increases the absorption of nonheme iron.²⁰ Copper is essential for ceruloplasmin, which catalyzes the conversion of Fe²⁺ to Fe³⁺ to enter the circulation via transferrin. In iron deficiency diagnosis, TIBC or serum transferrin receptor is shown as a better iron deficiency marker compared to serum iron or ferritin.²¹ We noticed that there was no statistically significant difference between preoperative serum Ferritin and Fe^{2 +} mean values and postoperative mean values (p = 0.055, p = 0.619). According to the guidelines, a comprehensive assessment, including serum levels of folate, copper, selenium, and zinc, as well as serum iron, vitamin B₆ and B₁₂, should be controlled for accurate interpretation of anemia following bariatric surgery.²² We observed a decrease in the TIBC mean values of patients after surgery (p < 0.001). The discrepancies in these data, which decrease in TIBC mean values without same changes in ferritin and serum iron values, may be due to challenges in standardizing the unsaturated iron binding capacity measurement method.

Damms-Machado et al.²³ reported that 1 year after LSG surgery, 11% of patients had serum vitamin B₁₂ values below the reference value. They expressed that LSG surgery had an effect on vitamin and trace element deficiencies during the first year follow-up of operation. Alexandrou et al.²⁴ determined that patients who underwent RYGB had a higher rate of vitamin B₁₂ deficiency compared to LSG (RYGB: 42.1% LSG: 5%, p = 0.003). Consistently with our results, there was no statistically significant difference between the mean values of preoperative serum vitamin B₁₂ and the postoperative mean values (p = 0.333). According to previous studies, main causes of vitamin B₁₂ deficiency after LSG surgery are related to reduce the intrinsic factor secretion due to fundus resection. Reduction in intrinsic factor, which is essential for the absorption of vitamin B₁₂ taken with foods, may lead to vitamin B₁₂ malabsorption.^17,25 Compared to this study, the reason for the absence of a difference in serum vitamin B₁₂ levels in our study can be considered as a short follow-up period.

Recent studies show that mean selenium levels decreased over time, and prevalence of those below the reference ranges increased over time; which is in agreement with our observations.^26,27 The prevalence of low selenium level after LSG was increased from 2% to 11–15%.²⁸ Shankar et al. reported that 14–24% of patients having a low selenium level 5 years after RYGB and LSG surgery.¹⁴ Selenium deficiency is expected as selenium is absorbed in the duodenum and proximal jejunum. However, previous studies have reported that selenium deficiency may vary between 3.2% and 58% in morbidly obese patients who have not undergone bariatric surgery.²⁹ In severe selenium deficiency, symptoms such as loss of skin and hair pigmentation, whitening of the nail structure, and tissue disorder may be seen. It can also cause diseases such as myopathy, cardiomyopathy, arrhythmia, muscle loss, immune disorder, and low thyroid function.³⁰ Accordingly, it is important to monitor serum levels regularly.

In the report of Saif et al.,³¹ no statistically significant change in serum magnesium levels indicated but serum magnesium levels increased significantly from baseline to first year and fifth year in the group receiving nutritional supplements (p = 0.0002, p = 0.0012). Our findings are consistent with this report, and we observed no statistically significant difference between preoperative serum Mg mean values and postoperative mean values (p = 0.170).

The decrease at the mean serum Folate levels of patients 3 months after LSG in this study is concurrent with the previous studies (p < 0.001). Aarts et al. reported folate deficiency in 15% of patients 1 year after LSG with multivitamin supplements. Gehrer et al. detected the deficiencies in 12% of the patients after RYGB and 14% of the patients after LSG. Previous reports have revealed that main cause of folate deficiency after LSG surgery is not surgical intervention, but the reason is the restrictive diet after surgery. Insufficient folate intake with nutrients due to the changing in diet causes decreases in deposited folate levels rapidly.³²

Deficiencies in serum zinc have been noticed 42.5% of patients at 1-year post-LSG and RYGB in study of Saif et al. However, in preceding articles the deficiencies are more commonly observed after malabsorptive operations and less commonly observed after purely restrictive procedures. Consistently, we observed no difference in mean values of serum zinc levels before and after surgery (p = 0.163). Serum zinc level may also decrease in inflammation due to obesity; therefore, the evaluation of zinc levels via systemic zinc concentrations in bariatric surgery patients can be misleading.³³ In addition, zinc is an element that is abundant in the environment. Samples should be taken carefully in order not to contaminate, and metal-free biochemistry tubes should be used.³⁴

Conclusion

LSG has less severe effects on mineral and vitamin deficiencies in the first 2 years compared to other bariatric surgical procedures. Longer follow-ups are required for more precise results. Multivitamin supplements are insufficient to prevent specific nutritional deficiencies after bariatric surgery, and more aggressive and faster treatments are needed. To better demonstrate the effect of bariatric surgery on vitamins and minerals balance in body, studies with higher number of patients and longer follow-up periods are needed. We concluded that the evaluation of nutritional profile of the patients at the postoperative follow-ups has a crucial role in terms of patients' health and well-being after surgery. Bariatric surgery follow-ups should be done by multidisciplinary team, including clinical biochemistry specialists, dietitians, and surgical team.

Footnotes

Author Disclosure Statement

No competing financial interests exist.

Funding Information

The authors received no financial support for the research, authorship and publication of this article.

References

Rodgers

, Tschop

, Wilding

. Anti-obesity drugs: past, present and future. Dis Model Mech, 2012; 5:621–626.

Haslam

, James

. Obesity. Lancet, 2005; 366:1197–1209.

Sjöström

, Narbro

, Sjöström

, Karason

, Larsson

, Wedel

, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med, 2007; 357:741–752.

Sjöström

, Peltonen

, Jacobson

, Sjöström

, Karason

, Wedel

, et al. Bariatric surgery and long-term cardiovascular events. JAMA, 2012; 307:56–65.

Mingrone

, Peltonen

, Jacobson

, Wolski

, Brethauer

, Navaneethan

, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med, 2012; 366:1577–1585.

Schauer

, Kashyap

, Wolski

, Brethauer

, Kirwan

, Pothier

, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med, 2012; 366:1567–1576.

Dixon

, O'Brien

, Playfair

, Chapman

, Schachter

, Skinner

, et al. Adjustable gastric banding and conventional therapy for type 2 diabetes: a randomized controlled trial. JAMA, 2008; 299:316–323.

Ribaric

, Buchwald

, McGlennon

. Diabetes and weight in comparative studies of bariatric surgery vs conventional medical therapy: a systematic review and meta-analysis. Obes Surg, 2014; 24:437–455.

Schauer

, Bhatt

, Kirwan

, Wolski

, Brethauer

, Navaneethan

, et al. Bariatric surgery versus intensive medical therapy for diabetes—3-year outcomes. N Engl J Med, 2014; 370:2002–2013.

10.

Miras

, Le Roux

. Can medical therapy mimic the clinical efficacy or physiological effects of bariatric surgery?. Int J Obes, 2014; 38:325–333.

11.

Buchwald

, Avidor

, Braunwald

, Jensen

, Pories

, Fahrbach

, et al. Bariatric surgery: a systematic review and meta-analysis. J Am Med Assoc, 2004; 292:1724–1737.

12.

Brethauer

, Hammel

, Schauer

. Systematic review of sleeve gastrectomy as staging and primary bariatric procedure. Surg Obes Relat Dis, 2009; 5:469–475.

13.

Saltzman

, Philip Karl

. Nutrient deficiencies after gastric bypass surgery. Annu Rev Nutr, 2013; 33:183–203.

14.

Shankar

, Boylan

, Sriram

. Micronutrient deficiencies after bariatric surgery. Nutrition, 2010; 26:1031–1037.

15.

Shikora

, Kim

, Tarnoff

. Nutrition and gastrointestinal complications of bariatric surgery. Nutr Clin Pract, 2007; 22:29–40.

16.

Xanthakos

. Nutritional deficiencies in obesity and after bariatric surgery. Pediatr Clin North Am, 2009; 56:1105–1121.

17.

Poitou Bernert

, Ciangura

, Coupaye

, Czernichow

, Bouillot

, Basdevant

. Nutritional deficiency after gastric bypass: diagnosis, prevention and treatment. Diabetes Metab, 2007; 33:13–24.

18.

Roust

, DiBaise

. Nutrient deficiencies prior to bariatric surgery. Curr Opin Clin Nutr Metab Care, 2017; 20:138–144.

19.

Malinowski

. Nutritional and metabolic complications of bariatric surgery. Am J Med Sci, 2006; 331:219–225.

20.

Olivares

, Pizarro

, Ruz

, Romana

. Acute inhibition of iron bioavailability by zinc: studies in humans. Biometals, 2012; 25:657–664.

21.

Zimmermann

, Hurrell

. Nutritional iron deficiency. Lancet, 2007; 370:511–520.

22.

Mechanick

, Youdim

, Jones

, Garvey

, Hurley

, McMahon

, et al. Clinical practice guidelines for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient—2013 update: cosponsored by American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery. Obesity (Silver Spring), 2013; 21 Suppl 1(0 1):S1–S27.

23.

Damms-Machado

, Friedrich

, Kramer

, Stingel

, Meile

, Küper

, et al. Pre- and postoperative nutritional deficiencies in obese patients undergoing laparoscopic sleeve gastrectomy. Obes Surg, 2012; 22:881–889.

24.

Alexandrou

, Armeni

, Kouskouni

, Tsoka

, Diamantis

, Lambrinoudaki

. Cross-sectional long-term micronutrient deficiencies after sleeve gastrectomy versus Roux-en-Y gastric bypass: a pilot study. Surg Obes Relat Dis, 2014; 10:262–268.

25.

Kwon

, Kim

, Menzo

, Park

, Szomstein

, Rosenthal

. Anemia, iron and vitamin B12 deficiencies after sleeve gastrectomy compared to Roux-en-Y gastric bypass: a meta-analysis. Surg Obes Relat Dis, 2014; 10:589–597.

26.

Freeth

, Prajuabpansri

, Victory

, Jenkins

. Assessment of selenium in Roux-en-Y gastric bypass and gastric banding surgery. Obes Surg, 2012; 22:1660–1665.

27.

Lefebvre

, Letois

, Sultan

, Nocca

, Mura

, Galtier

. Nutrient deficiencies in patients with obesity considering bariatric surgery: a cross-sectional study. Surg Obes Relat Dis, 2014; 10:540–546.

28.

Papamargaritis

, Aasheim

, Sampson

, Roux

. Copper, selenium and zinc levels after bariatric surgery in patients recommended to take multivitamin-mineral supplementation. J Trace Elem Med Biol, 2015; 31:167–172.

29.

Kimmons

, Blanck

, Tohill

, Zhang

, Khan

. Associations between body mass index and the prevalence of low micronutrient levels among US adults. MedGenMed, 2006; 8:59.

30.

Gletsu-Miller

, Wright

. Mineral malnutrition following bariatric surgery. Adv Nutr, 2013; 4:506–517.

31.

Saif

, Strain

, Dakin

, Gagner

, Costa

, Pomp

. Evaluation of nutrient status after laparoscopic sleeve gastrectomy 1, 3, and 5 years after surgery. Surg Obes Relat Dis, 2012; 8:542–547.

32.

Komorniak

, Szczuko

, Kowalewski

, Stachowska

. Nutritional deficiencies, bariatric surgery, and serum homocysteine level: review of current literature. Obes Surg, 2019; 29:3735–3742.

33.

Liu

, Bao

, Bolin

, Burris

, Xu

, Sun

, et al. Zinc deficiency augments leptin production and exacerbates macrophage infiltration into adipose tissue in mice fed a high-fat diet. J Nutr, 2013; 143:1036–1045.

34.

Pech

, Meyer

, Lippert

, Manger

, Stroh

. Complications and nutrient deficiencies two years after sleeve gastrectomy. BMC Surg, 2012; 12:13.