Journal of Digestive Disorders And Diagnosis

Journal of Digestive Disorders and Diagnosis

Journal of Digestive Disorders and Diagnosis

Current Issue Volume No: 1 Issue No: 3

Research Article Open Access Available online freely Peer Reviewed Citation

Nutritional Deficiencies in Pregnancy after Surgery for Morbid Obesity

Andreas Alexandrou 1,   George Tzikos 2,   Sofia Chatzi 2,   Areti Augoulea 2,   Anastasios Angelou 1,   Adamantios Michalinos 1,   Irene Lambrinoudaki 2  

1Department of Surgery, National and Kapodestrian University of Athens, Medical School, Laiko General Hospital, 17 Agiou Thoma St, GR-11527 Athens, Greece

2Department of Obstetrics and Gynecology, National and Kapodestrian University of Athens, Medical School,, Aretaieio Hospital, 76 Vas. Sofias Ave, GR-11528, Athens, Greece

Abstract

Objectives:

The rate of morbid obesity among women of reproductive age continues to rise worldwide. Surgical treatment remains the most effective mean to face it. Anatomical, physiological and nutritional modifications lead to several challenges for pregnancy after bariatric procedures. In spite of routine supplementation after bariatric surgery, vitamin and mineral deficiency frequently appear in bariatric pregnancies. The aim of this review is to summarize the existing data on the prevalence and management of nutritional deficiencies in pregnancy after bariatric surgery.

Methodology:

A comprehensive search of Pubmed Database was conducted for English-language studies using a list of key words.

Results:

The most common post-operative deficiencies in pregnancy include iron, vitamin B12, folate, vitamin D and magnesium deficiency. Less common are selenium, vitamin A, vitamin B6 and vitamin C deficiency. Finally, copper, vitamin K, vitamin B1, vitamin E and albumin deficiencies are considered to be relatively rare.

Conclusions:

Pregnancy after bariatric surgery has been proven to be safe for both the mother and the fetus. However, there is still the risk of significant nutritional deficiencies with adverse effects on pregnancy and lactation. As a result, a thorough customized nutritional assessment is mandatory for every woman in reproductive age who has undergone a bariatric operation, with strict regular follow-up during pregnancy and lactation.

Author Contributions
Received 16 Sep 2017; Accepted 24 Sep 2017; Published 26 Sep 2017;

Academic Editor: Rongbiao Tang, Ruijin hospital

Checked for plagiarism: Yes

Review by: Single-blind

Copyright ©  2017 Andreas

License
Creative Commons License     This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Competing interests

The authors have declared that no competing interests exist.

Citation:

Andreas Alexandrou, George Tzikos, Sofia Chatzi, Areti Augoulea, Anastasios Angelou et al. (2017) Nutritional Deficiencies in Pregnancy after Surgery for Morbid Obesity . Journal of Digestive Disorders and Diagnosis - 1(3):17-33. https://doi.org/10.14302/issn.2574-4526.jddd-17-1776

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DOI 10.14302/issn.2574-4526.jddd-17-1776

Introduction

Obesity has taken an epidemic form during the last two decades. The World Health Organization (WHO) assessed than in 2008 there were more than 1.4 billion overweight and more than half a billion obese adults. Excess body weight is the 5th leading risk factor for global deaths. More than 2.8 million adults die each year due to being overweight or obese1. It is estimated that in Greece, the prevalence of obesity in the adult population is approximately 17.3%, 0.8 units over the mean prevalence of Europe2. All age groups face this problem but the incidence is greater for females. About 25% of women meet the obesity criteria, one-third of which are in the reproductive age3.

Maternal obesity has turned out to be one of the most commonly occurring risk factors for pregnancy, delivery and postpartum complications, not to mention the negative effects on fertility as it is characterized by polycystic ovarian syndrome leading to oligo- or amennorhea4.

Maternal risks associated with obesity include increased prevalence of stillbirth and intrauterine fetal death, preterm labor, miscarriage, fetal chromosomal anomalies and macrosomia. Obese women are more likely to suffer from thromboembolism, gestational diabetes and pre-eclampsia. Moreover dysfunctional labour, cesarian section, perioperative complications and postpartum hemorrhage are more common in these women 5, 6.

Therefore, weight loss, ideally before conception, appears imperative. Bariatric surgery (BS) remains the only effective means of treatment for morbid obesity7. It promotes weight loss, ameliorates related comorbidities and improves reproductive function and infertility. Pregnancy outcome following bariatric surgery depends on the procedure type that has been performed.

Two of the most common bariatric procedures are Roux-en -Y gastric bypass (RYGBP) and the vertical sleeve gastrectomy (VSG). During RYGBP, the stomach is divided and a small gastric pouch that can hold approximately 30ml is created, thus inducing a restriction of the amount of food the recipient can ingest. Subsequently, the jejunum is divided 0.6 -1 meter distally to the ligament of Treitz with the distal segment anastomosed to the gastric pouch (gastro-jejunal anastomosis, GJ), thus reducing the absorbing capacity of the alimentary tract. Eventually, the continuity of the alimentary tract is restored with the construction of a jejuno-jejunal anastomosis (JJ) 1-1.5 meters distally to the gastro-jejunal anastomosis. So RYGBP is a combined restrictive and malabsorptive procedure. The VSG on the other hand is a purely restrictive procedure. The greater curvature of the stomach is resected, leaving a narrow vertical tube that can hold a volume of approximately 150 ml 7, 8. This reduction of the gastric capacity along with the loss of appetite, induced by the lower levels of ghreline, an orexigenic peptide normally secreted by the cells of the gastric fundus which is resected, result in considerable excess weight loss with profound effects on the general health status.

Nevertheless, in both techniques the anatomy of the gastrointestinal tract is modified and this leads to micronutrient deficiencies. Risk factors for this include preoperative malnutrition, decreased food intake, food intolerances, excessive vomiting, inadequate nutrient supplementation and nutrient malabsorbtion. All of these problems are amplified for women in pregnancy or lactation since during both of these conditions the demands for micronutrients are increased3, 7. Women of reproductive age are advised to avoid pregnancy for at least one year after surgical treatment of morbid obesity, but since at some point this will definitely occur for an increasing number of women, a review of the existing data concerning the nutritional status and needs after bariatric surgery can be very useful for any clinician dealing with these patients.

Methodology

A comprehensive search of Pubmed Database was conducted between April and May 2014. The review covered a period from 1991 to 2014. The keywords which were used individually or in combination were: bariatric surgery (BS), obstetric outcome, nutritional deficiencies, iron, Vitamin D, B12, B6, B1, C, A, E, K, folate, albumin, zinc, magnesium, calcium, biotin, copper, selenium and supplementation.

Results

Iron:

Many studies have shown that iron deficiency exists already pre-operatively in obese patients and more particularly in female bariatric surgery patients of childbearing age due to heavy menstrual periods. Even more, all patients after bariatric surgery face a decrease in the production of hydrochloric acid, subsequently contributing to a lower iron uptake, since the Fe3+ to Fe2+ conversion is reduced, due to the resection of 75-80% of the stomach and the administration of PPIs (proton pumps inhibitors). Futhermore red meat, which is rich in iron, is less well-tolerated after BS 9, 10, 11. As a result iron deficiency often is seen among bariatric patients who have undergone RYGBP as this procedure leads to iron malabsorbtion and reduced food intake but also after VSG due to lower acid content in the stomach. As a result, iron deficiency is one of the most common nutritional deficiencies after bariatric surgery Table 110, 12, 13, 14, 15. In 2014, Alexandrou et al, in their pilot study have reported that in 40 patients undergoing BS, 30% of them developed iron deficiency and 7% ferritin deficiency after a 4-year follow up 16 . During the same year, Van Rutte et al, found that in 200 patients who underwent VSG, one year post-operatively, 37 of them (18,5%) had iron deficiency and in 16 of them (8%) ferritin levels were below the normal range. Before the operation the prevelance of iron and ferritin deficiency was 38% and 7% respectively17 . In 2012, two studies reported iron deficiency from 0% - 10.5% 1 to 5 years postoperatively 18, 19 .

Table 1. Prevalence of iron or ferritin deficiency after bariatric surgery.
  Year Author Number of patients Years of follow up Prevalenc of iron deficiency postoperatively (%) Prevalence of ferritin deficiency postoperatively (%)
2014 Van Rutte et al.17 200 1 18.5 8
2013 Alexandoru et al.16 40 4 30 7
2013 Coupaye et al.43 30 1 NR 30
2013 Eltweri et al.22 41 NR NR 8
2012 Saif et al.19 82 1 / 3 / 5 3 / 10.5 / 0 8.6 / 15.8 / 5.6
2012 Damms-Machado et al.18 54 1 4.3 NR
2010 Aarts et al.104 60 1 43 NR
2010 Gehrer et al.27 50 3 18 NR
2009 Hakeam et al.37 61 1 4.9 NR
2009 Toh et al.105 64 1 11 0

• NR: Not Reported

The main cause of anemia in pregnancy is iron deficiency. Pregnancy anemia can be aggravated by various conditions such as uterine or placental bleedings, gastrointestinal bleedings, and peripartum blood loss. In addition to the general consequences of anemia, there are specific risks during pregnancy for the mother and the fetus such as intrauterine growth retardation, prematurity, feto-placental miss ratio, and higher risk for peripartum blood transfusion 3, 7, 20, 21.

Vitamin B12:

Vitamin B12 deficiency is also very common before and after bariatric surgery (Table 2). Its preoperative prevalence ranges between 3-18%22, 23, 24, 25. After bariatric surgery the absorption of the B12 may be impaired at different levels depending on the type of procedure. Absence of acid environment following gastric bypass surgery, inadequate secretion of intrinsic factor and malabsorption result in the decrease of vitamin B12 absorption in the terminal ileum leading to B12 deficiency 3. Two studies have found that cobalamin deficiency after BS was 11,5% and 5%, after a one year and a four year follow-up, respectively 16, 17 . Moreover, there is another study which has reported that in 41 patients having udergone BS, vitamin B12 deficiency was 20% post-operatively 22 . In addition, Pech et al, found that in their two different studies, the need for supplementation after BS procedure in a total of 182 patients was between 42 and 46,3% during the first two postoperative years, and vitamin B12 levels remained clearly within the lower third of the reference ranges during this period, which means that without the supplementation, a vitamin B12 deficiency would likely have occurred 23, 24 . In three more studies, vitamin B12 deficiency fluctuated between 0% and 17,2% one year after BS 18, 25, 26 and Gehrer et al, reported that cobalamin deficiency after a 3-year follow-up in 50 patients was 18% 27 . Apart from the obvious hematologic effects, low concetration of cobalamin may result in elevation of serum homocystein. Hyperhomocysteinemia is known to be directly related to early loss of pregnancy. Moreover, inappropriate levels of B12 during pregnancy due to lower intake can result in neurobehavioral disorders and anemia in the infants 28, 29.

Table 2. Prevalence of vitamin B12 deficiency after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of vitamin B12 deficiency postoperatively (%)
2014 Van Rutte et al.17 200 1 11.5
2013 Alexandrou et al.16 95 4 5
2013 Eltweri et al.22 41 NR 20
2012 Moizẽ et al.44 61 5 12.5
2012 Saif et al.19 82 1 / 3 / 5 2.9 / 0 / 0
2012 Damms-Machado et al.18 54 1 17.2
2010 Aarts et al.104 60 1 9
2010 Gehrer et al.27 50 3 18
2009 Toh et al.105 64 1 0

• NR: Not Reported

Folate(vitamin B9):

Folate absorption occurs along most of the small intestine, mainly in the duodenum and in the jejenum, and depends on pH level, mechanisms of the intestinal wall which have to do with nutrient’s transport, and saturation points 30, 31. After bariatric surgery,follic acid can be absorbed throughout the entire intestinal tract, through mechanisms of adaptation 15. Therefore, folate deficiency after BS ensues primarily due to low intake of folate-rich food, such as legumes, lettuce and green leafy vegetables, and/or due to vitamin B12 malabsorption 32, 33 . If maternal folate stores are insufficient prior to conception, the risk of folic acid deficiency is higher and is associated with fetal neural tubes disorders (NTDs), while also the risk of an adverse pregancy outcome such as a preterm delivery and birth defects in the following pregnancy increases. 20, 42. According to the results of the reviewed studies (Table 3), pre-operative folate deficiency has been estimated to exist in up to 54% of the subjects, whereas recent studies from the USA support that this prevalence is much lower, about 0-6% 34, 35, 36. Five studies found that the prevalence of follic acid deficiency one year after BS ranges between 0% and 15% 17, 19, 25, 26, 37 . Furthermore, Ruiz-Tovar et al. found that in 30 BS patients the prevalence of follic acid deficiency was 0% after a two-year follow-up. On the same wavelength, Toh et al. observed in their study that none of the patients developed folate deficiency one year postoperatively, too26. On the other hand, Gehrer et al, found the highest prevalence of this deficiency in the literature, which was 22% in fifty patients 3 years after the BS 27, 38. Finally, Aarts et al. and Hakeam et al. found in their studies that folate deficiency occurred in 15% and 9,8% of their patients respectively, one year after VSG 25, 37.

Table 3. Prevalence of folate deficiency after bariatric surgery
Year Author Number of patients Years of follow-up Prevalence of folate deficiency postoperatively (%)
2014 Van Rutte et al.17 200 1 12.5
2013 Eltweri et al.22 41 NR 3
2012 Saif et al.19 82 1 / 3 / 5 8.8 / 5.5 / 0
2012 Damms-Machado et al.18 54 1 13.8
2011 Ruiz-Tovar et al.106 30 2 0
2010 Aarts et al.104 60 1 15
2010 Gehrer et al.27 50 3 22
2009 Toh et al.105 64 1 0
2009 Hakeam et al.37 61 1 9.8

• NR: Not Reported

Vitamin D, Calcium, Parathormone (PTH):

The mechanisms which affect calcium metabolsim afterbariatric procedures are not clearly understood. Lower Vitamin D - mediated absorption of calcium due to Vitamin-D deficiency, changes in HCl (hydrochloric acid) secretion and intolerance of calcium-rich food after bariatric procedures are pathways which can influence calcium nutrient status. Moreover, hypovitaminosis D may occur due to less sun exposure, increased uptake of Vitamin D in adipose tissue and vitamin D malabsorption caused by bypassing segments of the intestine where it is naturally absorbed. Because of the inverse relationship between the levels of serum Vitamin D/serum calcium and the levels of serum PTH, vitamin D deficiency provoking secondary hyperparathyroidism is frequently observed post-operatively. However, serum calcium levels are usually within the normal ranges 11, 39, 40, 41, 42. Four different studies with one year follow up reported that the prevalence of vitamin D deficiency fluctuated between 39 and 70,4 % and true secondary hyperparathyroidism occurred in 18 and 39% of the patients. However, it was found that calcium levels were within the normal ranges for almost all the patients in all these studies 17, 18, 25, 43 In addition, one study with 40 individuals reported that four years after BS, hypovitaminosis D was found in 56,3% of the patients and elevated levels of PTH in 43,3% of them 16. Furthermore, on the same wavelength was also the study of Saif et al., who found that 5 years after, BS vitamin D deficiency and hyperparathyroidism were present in 42% and 58,3% of 82 patients respectively. However, calcium levels were within normal values 19. On the other hand, Moize et al, did not find any vitamin deficiency D, 5 years after BS in 61 patients although, it should be noticed that the prevalence of hypovitaminosis D, 4 years after the procedure, was 44,4% 48. The prevalence of calcium deficiency was 12,5% and hyperparathyroidism was present in 87,5% of them. 44 Furthermore, in another study, the prevalence of Vitamin D deficiency and elevated PTH was only 3,3% for both markers in 30 patients 2 years after BS, whereas, pre-operatively it was 96,7% and 20% respectively38. Finally, Gehrer et al, reported in their study that hypovitaminosis D and elevated levels of PTH was found in 32% and 14% of 50 patients, who underwent BS, after a 3-year follow-up, with calcium levels within normal ranges for all of them 27 . Data regarding the frequency of vitamin D deficiency, calcium deficiency and hyperparathyroidism after bariatric surgery is presented in Table 4.

Table 4. Prevalence of vitamin D as well as calcium deficiency, and rates of secondary hyperparathyroidism after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of Vitamin D deficiency postoperatively (%) Prevalence of calcium deficiency postoperatively (%) Prevalence of hyperparathyroidism (%)
2014 Coupaye et al.43 43 1 70 0 NR
2014 Van Rutte et al.17 200 1 36 2 18
2013 Alexandrou et al.16 40 4 56.3 NR 43.3
2012 Saif et al.19 82 1 / 3 / 5 34.3 / 55.6 / 42 0 / 0 / 0 23.2 / 7.7 / 58.3
2012 Moizẽ et al.44 61 4 / 5 44.4 / 0 4.8 / 12.5 57.1 / 87.5
2012 Damms-Machado etal.18 54 1 70.4 0 NR
2011 Ruiz-Tovar et al.106 30 2 3.3 NR 3.3
2010 Aarts et al.104 60 1 39 0 39
2010 Gehrer et al.27 50 3 32 0 14

• NR: Not Reported

Pregnancy is characterized by many hormonological and metabolic changes 45 and vitamin D deficiency is relatively common, especially in obese women 46, 47 . Bodnar et al. documented a significantly higher percentage of vitamin D deficiency in obese pregnant women. Bariatric surgery also can lead to a postoperative vitamin D deficiency in pregnant women 55. Maternal vitamin D deficiency is associated with a variety of maternal and fetal complications, such as pre-eclampsia, gestational diabetes and a higher risk of asthma and schizophrenia in childhood 48. The exact mechanism by which vitamin D can facilitate the onset of pre-eclampsia is unclear 49, 50.. Another important observation is that maternal vitamin D levels can influence the bone status of the newborn. Viljakainen et al. showed a significant smaller tibia mineral content in the newborns of pregnant women with lower levels of 25(OH)D during pregnancy 50 .

Zinc:

Zinc is a trace element which is only second to iron in concentration in the human body 51. Zinc plays a pivotal role in the cellular metabolism, being essential for more than three hundred enzymatic reactions 52. Prior to bariatric surgery, serum zinc levels in obese women are generally lower than in healthy ones 53. Zinc deficiency after bariatric surgery should always be considered, especially for pregnant women, since many factors could contribute to it. These include bypassing intestinal segments of zinc absobtion duodenum and jejunum), intolerance to zinc-rich sources (red meat, fish), reduced gastric acid production (required for zinc absorbtion and bioavailability) and bacterial overgrowth (due to alterations of the intestinal tract) 54, 55, 56, 57. In addition to these, zinc levels decline by about 30% during pregnancy. Low levels of zinc have been associated with premature deliveries, low birth weight, abnormal fetal development and neurological defects such as spina bifida. Cases of zinc deficiency during lactation are accompanied by skin rashes or dermatitis, often in combination with failure to thrive and irritability 58, 59, 60. Zinc deficiency is not invariably reported after bariatric surgery (Table 5). Reportedly, it was calculated approximately 5%, one year after BS 17 . Hair loss, as a sign of zinc deficiency, was observed in 30% of the 43 individuals who underwent BS, one year postoperatively 43 . Moreover, Moize et al, found that 5 years after BS, zinc deficiency was 12,5% in 61 patients, while 4 years postoperatively, in the same study, zinc deficiency was 47,6% 44 . Furthermore, Gehrer et al, reported that zinc was below the normal ranges in 34% of the fifty patients who underwent BS, after a 3-year follow-up period 27 and Salle et al, found in their study that zinc deficiency was 18,8% one year after BS 61. In addition, one study found that zinc deficiency was 14% two years after BS 23, which was in agreement with another study which reported 14,3% zinc deficiency five years after the operation 19 .

Table 5. Prevalence of zinc deficiency after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of zinc deficiency postoperatively (%)
2014 Van Rutte et al.17 200 1 5
2012 Saif et al.19 82 5 14.3
2012 Moizẽ et al.44 61 4 / 5 47.6 / 12.5
2012 Pech et al.23 100 2 14
2010 Salle et al.107 33 1 18.8
2010 Gehrer et al.27 50 3 34

Magnesium:

Since magnesium is an essential trace element for optimal metabolic function, magnesium deficiency may be a risk factor not only for neurological and cardiovascular complaints but also for metabolic syndrome 62, 63, 64, 65. Futhermore adequate intake of the mineral is needed for normal embrionic and fetal development 66. Magnesium deficiency is not reported as commonly as other nutritional deficiencies and accordingly there are only sparse data about postoperative hypomagnesemia (Table 6). One study, found that magnesium deficiency was present in 3% of 200 subjects having undergone BS (versus 2% preoperatively) one year after the procedure 17 . Furthermore, there are two different studies which agree that magnesium deficiency did not occur after BS 19, 22 , whereas Moize et al, reported that hypomagnesemia was observed in 12,5% of 61 patients, five years after BS 44 . Finally, Coupaye et al, reported that cramps were observed in 3% of 43 individuals who underwent BS43 . Although COPPER: Copper as a nutrient is essential in many enzymatic reactions and is involed in red cell production and function of the nervous system 76, 77. It is absorbed in the stomach and the proximal duodeum 78, 79. Patients undergoing malabsorptive bariatric surgery are at risk of impaired copper status due to hypoacidity in the remnant stomach pouch and bypass of the duodeum80. Deficiecy seems to be rare after BS. The only data we found refers to Amar’s et. al. study in which they found that there was no deficiency in 41 patients after VSG 22. Although it is uncommon, clinicians should be vigilant in its early detection as iron and copper deficiency often coexist, especially in pregnancy. As a result, hypocupremia is often misdiagnosed until serious neurological symptoms, anemia and heart enlargement occurs 81.

Table 6. Prevalence of magnesium deficiency after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of magnesium deficiency postoperatively (%)
2014 Van Rutte et al.17 200 1 3
2013 Eltweri et al.22 41 NR 0
2012 Saif et al.19 82 5 0
2012 Moizẽ et al.44 61 5 12.5

• NR: Not Reported

Chromium and Vanadium:

There are no reports referring to chromium or vanadium deficiency in pregnant women after bariatric surgery.

it is not common, maternal magnesium deficiency has been associated with premature labor, small-for-gestational-age (SGA) neonates, pre-eclamsia and the pathogenesis of the sudden infant death syndrom (SIDS). Tayaka et. al., showed a significant lower level of Mg concentrations in umbilical cord blood in SGA neonates compared to that of control group 66, 67, 68. Nevertheless, further studies should investigate the impact of Mg deficit in fetuses.

Selenium:

Selenium is a trace element with an essential role in human biology 69. It is necessery for normal growth and reproduction. Selenium deficiency is implicated with maternal and fetal adverse outcomes, such as infertility, miscariagges, pre-eclampsia, pre-term labor, small for gestational age newborns, gestational diabetes and nervous damage of the fetus 70, 71. In addition, Skroder et al, found a possible negative impact in psychomotor and language development of children from mothers with reduced levels of selenium during pregnancy 72. Searching in the literature, only few data were found referring to selenium deficiency after bariatric surgery 73, 74, 75. Studies have shown a decrease at the level of selenium after RYGBP. One study also reported that 9 out of 21 patients (43%) suffered from selenium deficiency after VSG 22 . Moreover, Pech et al, found that in 100 individuals who underwent VSG, a significant decrease in serum selenium levels occurred three months after the procedure and 8 out of 82 (9,7%) patients suffered from selenium deficiency and were therefore given supplementation22

Vitamin A:

Vitamin A is included in the fat-solube vitamins and its absorption occurs in the small intestine either as retinol (animal sources) or qas caroten (plants and vegetables). Vitamin A plays an important role in cells’ reproduction, differentiation and proliferation and its’ requirements during pregnancy and lactation are higher by 20% 82. Adequate levels of vitamin A are necessery, especially in the second and third pregnancy trimester, for normal fetal lung development and maturation, vision and immunity 77, 83. Also Vitamin A deficiency has been shown to increase the risk of maternal mortality, premature birth, intra-uterine growth retardation, low birth weight and ante-partum hemorrhage due to abruption placentae 84, 85, 86. Finally vitamin A deficiency may exacerbate iron deficiency, which is relativly common during pregnancy 82.

After a bariatric procedure Vitamin A deficiency can arise due to the bypassing of intestinal segments, reduced dietary intake, oxidative stress, lipid malabsoption and excessive vomiting, which can be even more profound during pregnancy 87. Two different studies reported that Vitamin A deficiency was present in 20% of 43 patients, and in 4% of 60 patients respectively one year after BS 25, 43 . On the other hand, Saif et al. found that hypovitaminosis A did not occur five years after BS . However, there are also three studies which have reported a vitamin A excess with a prevalence between 7,9% and 55,5% . Rates of vitamin A excess and deficiency after surgery for morbid obesity are presented in Table 7.

Table 7. Prevalence of vitamin A deficiency or excess after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of Vitamin A deficiency postoperatively (%) Prevalence of vitamin A excess postoperatively (%)
2014 Coupaye et al.43 43 1 20 NR
2014 Van Rutte et al.17 200 1 NR 55.5
2012 Saif et al.19 82 5 0 NR
2012 Damms-Machado et al.18 54 1 NR 7.9
2010 Aarts et al.104 60 1 4 48

• NR: Not Reported

Vitamin K:

Vitamin K is another fat-solube vitamin which is absorbed primarily in the ileum. It is notable that vitamin K has an already limited placental transfer during pregnancy, but its deficiency is rare. The excessive vomiting or fat malabsorption affecting pregnant women, particularly after bariatric surgery, may lead to a higher risk of vitamin K deficiency and concomitant disorders such as clotting abnormalities and an increased bleeding tendency 88. Eerdekens et. al. have reported on 5 cases with severe neonatal intracranial bleeding, complicating births from women who had undergone BS, all possibly related to Vitamin K deficiency 89.

Vitamin E:

Vitamin E, being also a fat-solube vitamin, is mainly absorbed in the small intestine, especially in the terminal ileum. Since the intestinal segment which is bypassed in malabsoptive procedures such as RYGBP is jejunum and not the distal ileum, vitamin E deficiency seems to be uncommon after bariatric surgery. One study reported that hypovitaminosis E was found in 3% of 43 patients who underwent BS one year after the procedure 43. Furthermore, on the same wavelength, another study reported that there were not any patients who were deficient regarding vitamin E one year after BS 18 . Although uncommon, women in pregnancy should be monitored, because low concentration of Vitamin E has been accosiated with abruptio placentae in normal pregnancies and higher incidence of miscarriages 82.

Vitamin B1 (Thiamine):

Water-soluble vitamin B1 is absorbed in the proximal small intestine (mainly in the ileum) and its deficiency may occur due to persistent vomiting, from which pregnant women commonly suffer, reduced intake and malabsorption. Thiamine deficiency has been associated with encephalopathies, namely Wernicke’s encepalopathy and Korsakoff’s syndrome, dry Beri-Beri, ataxia and mental status changes 90, 91 . Although Vitamin B1 deficiency seems to be relatively rare, it may lead to serious health problems. Rates of vitamin B1 deficiency and excess after surgery for morbid obesity are presented in Table 8. Gehrer et. al. reported in their study that there was no thiamine deficient patient three years after VSG, and Moize et al. concluded the same after a five-year follow-up period 27, 44 . Nevertheless, in a small sample of 13 individuals, vitamin B1 deficiency was about 30,8% five years after VSG and in three other studies the prevalence of this deficiency flunctuated between 9% and 23% one year after the procedure. It should be highlighted that none of these four studies, which reported a higher prevalence of thiamine deficiency, noticed any clinical comorbidities relevant to the reported deficiency 17, 19, 25, 43 . On the other hand, there were two studies which found a thiamine excess after BS. The prevalence of this excess was 4,5% and 31% respectively 17, 25.

Table 8. Prevalence of Vitamin B1 deficiency or excess after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of Vitamin B1 deficiency postoperatively (%) Prevalence of Vitamin B1 excess postoperatively (%)
2014 Coupaye et al.43 43 1 23 NR
2014 Van Rutte et al.17 200 1 9 4.5
2012 Moizẽ et al.44 61 5 0 NR
2012 Saif et al.19 82 5 30.8 NR
2010 Aarts et al.104 60 1 11 31
2010 Gehrer et al.27 50 3 0 NR

• NR: Not Reported

Vitamin B6 (Pyridoxine):

Vitamin B6 concetrations decline during pregnancy as a physiologic adjustment secondary to increased blood volume or as a result of increased requirements for active transport across the placenta 82. Vitamin B6 deficiency is rare but it has been associated with pre-eclampsia, carbohydrate intolerance, hyperemesis gravidarum and neurologic disease of the infants 92. As a water-soluble vitamin, B6 is absorbed primarily in the duodeum after exposure to the gastric acid 11, 30. Pregnant women with a history of bariatric surgery are in danger due to the bypassing of the responsible for the absorption intestinal segments and the reduction of the gastric acidity, conditions that ensue both after RYGBP and VSG. Rates of postoperative vitamin B6 deficiency and excess are presented in Table 9. Three different studies conducted with a one-year follow-up, reported that the prevalence of vitamin B6 deficiency was 4%, 17% and 17,2% respectively after BS, while on the other hand an excess of pyridoxine with a prevalence between 9,2% and 47,5% has also been reported 17, 18, 43. Moreover, Aarts et al. found also that 30% of sixty individuals who underwent BS had a vitamin B6 excess, while none of them was deficient 25. Finally, Moize et al. and Gehrer et al. both reported that the prelalence of vitamin B6 deficiency was 0%,five and 3 years respectively after BS 27, 44.

Table 9. Prevalence of Vitamin B6 deficiency or excess after bariatric surgery
Year Author Number of patients Years of follow-up Prevalence of Vitamin B6 deficiency postoperatively (%) Prevalence of Vitamin B6 excess postoperatively (%)
2014 Coupaye et al.43 43 1 17 NR
2014 Van Rutte et al.17 200 1 4 47.5
2012 Damms-Machado et al.18 54 1 17.2 9.2
2012 Moizẽ et al.44 61 5 0 NR
2010 Aarts et al.104 60 1 0 30
2010 Gehrer et al.27 50 3 0 NR

• NR: Not Reported

Vitamin B2 (Riboflavin), Vitamin B3 (Niacin), Vitamin B5 (Pantothenic Acid), Vitamin B7 (Biotin):

Riboflavin deficiency during pregnancy can result in pre-eclamsia and birth defects including congenital heart deffect and limb deformities 93. Deficiency of niacin is also a concern during pregnancy but it is relativly common. Finally research data suggest that a substantial number of women develop marginal or subclinicqal biotin deficiecy during normal pregnancy with a potential risk for teratogenesis 94.

For pregnant women who have undergone bariatric surgery the risk of those deficiencies is greater due to malabsorbtion but there are no specific data referring to these water-soluble vitamins either after RYGBP or after VSG.

Vitamin C (Ascorbic Acid):

Vitamin C is an essential water-soluble vitamin, involved in many biological mechanisms. During pregnancy, serum levels of vitamin C progressively decrease almost by 50%, because of the extra uptake by the fetus and the hemodilution. It’s deficiency except from fatigue, bleeding gums, petechia, crockscrew hair, hyperceratosis, myalgias/arthralgias is also associated with pre-eclampsia, poor fetal growth and premature birth 95, 96. This deficiency seems more likely after bariatric surgery, although few data are available in the published literature refering to it. Moreover, during lactation, vitamin C requirements are even higher, and since the maternal vitamin C levels are associated with the levels of vitamin C in the milk, monitoring should be close 82.

Total Protein, Prealbumin, Albumin:

The evaluation of protein status includes the assessment of the following parameters: 1) total protein, 2) prealbumin and 3) albumin. The majority of the proteins are absorbed in the duodeum. Protein deficiency after BS may occur due to the ensuing anorexia, lower protein uptake, reduced protein digestion caused by poor HCl secretion, and malabsorption. It is associated with loss of muscle, oedema and hypoalbuminaemia. Prealbumin is considered to be an indicative parameter of adequacy of protein intake 97 . Several studies have been conducted in order to assess either all of these parameters or only some of them (Table 10). Coupaye et al. found that one year after VSG, albumin and prealbumin deficiency were both rare (3%), in a sample of 43 subjects43 .Moize et al. reported in their study that after a five-year follow-up, no one of the 61 patients who had undergone VSG, was deficient, concerning albumin and prealbumin status 44. On the same wavelength, five more studies, agreed that the prevalence of albumin deficiency after VSG was 0% 18, 22, 26, 38, 98 . Furthermore, Saif et al. found that in 18 patients, who had undergone VSG and were assessed for five years, only one (5,5%) had an albumin deficiency 19, and Gehrer et al. reported that 4% of the fifty individulas were deficient with regards to total protein, three years post-operatively 27. Finally, on the contrary, Aarts et al. reported a prevalence of albumin deficiency of about 15% one year after BS, which was relatively higher, compared to the above mentioned studies 25.

Table 10. Prevalence of albumin, prealbumin or total protein deficiency after bariatric surgery.
Year Author Number of patients Years of follow-up Prevalence of albumin deficiency postoperatively (%) Prevalence of prealbumin deficiency postoperatively (%) Prevalence of total protein deficiency postoperatively (%)
2014 Coupaye et al.43 43 1 3 3 NR
2013 Eltweri et al.22 41 NR 0 NR NR
2012 Saif et al.19 82 1 / 3 / 5 5.5 NR NR
2012 Moizẽ et al.44 61 4 / 5 0 0 NR
2012 Damms-Machado et al.18 54 1 0 NR NR
2011 Ruiz-Tovar et al.106 30 2 0 NR NR
2010 Aarts et al.104 60 1 15 NR NR
2010 Gehrer et al.27 50 3 0 NR 4
2009 Toh et al.105 64 1 0 NR NR
2006 Hamoui et al.108 118 1 0 NR NR

• NR: Not Reported

Post-Operative Management of Nutritional Deficiencies in Pregnancy.

The above mentioned research data have shown that obese women in reproductive age suffer quite often from several nutritional deficiencies, even prior to bariatric surgery, and there is a high risk of aggravation of these defeciencies after either RYGBP or VSG for various reasons. Pregnancy can further amplify some of these nutritional deficiencies either by increasing the demand or by decreasing the intake 99.Therefore, life-long supplementation of vitamins and trace elements is highly recommended after bariatric procedures 10, 100, 101, 102. For pregnant women the importance of routine nutritional screening is heightened. They should be closely monitored and clinicians should be vigilant for the detection of any deficiency that may occur, in order to prevent adverse outcomes, maternal or fetal. Table 11 lists the nutrient supplements which are recommended for patients after BS, for women in normal pregnancies and during pregnancy after BS. These suggested supplementations should be regarded as general recommendations, since individual requirements may vary depending on the results of frequent testing that may detect a state of deficiency or deficiency symptoms.

Table 11. Recommended supplementation for the general bariatric population, for pregnant women and for pregnant women with a history of bariatric surgery
Micronutrient Recommendation for general bariatric population Recommendation for pregnant women Recommendation for pregnant women with a history of bariatric surgery
Iron 65 mg 30 mg 40-65 mg
Vitamin B12 5 mg 3 mg 4-5 mg
Folate   4 mg 4 mg
Calcium 1200-2000mg oral - 2000mg calcium citrate
Vitamin D 800-1000iu - 2000-6000iu
Zinc 8-15mg - 15mg
Magnesium - - 200-1000mg (if states of deficiency or symptoms occur)
Vitamin K 300mg - Close follow up
Copper 2-8mg - 2-8mg
Vitamin A 10.000 iu - 5.000 iu
Vitamin C 500mg - 500-1000mg

Further testing should be conducted for the evaluation of more nutrient markers, namely magnesium, PTH, copper and other water-soluble vitamins 10, 103 . Overall, in the management of obesity, teamwork has proved to be beneficial, and a comprehensive group of well-trained professionals is vital for the efficient and effective nutritional care of the patient.bariatric surgery is associated with several nutritional deficiencies. As a result, it is recommended that a thorough, customized nutrition assessment should be conducted for every woman of reproductive age, potential candidate for bariatric surgery, pre-operatively, in regular post-operative intervals, and even more intensively during pregnancy. The most common deficiencies include iron, folate, vitamin B12, vitamin D and calcium deficiency. Most women should be supplemented even before conception and especially during pregnancy . Furthermore, many other nutrients, including vitamins of the B-complex (thiamine, pyridoxal), other fat-soluble vitamins (A, E, K) and minerals (copper, zinc, selenium), although rarely deficient, should be tested periodically, to ensure their levels remain within normal range.

Disclosures

The authors have no interest to disclose.

References

  1. 1.. (GHO) WGHO:
  1. 2. (2012) WHO: Health at a Glace Europe 2012-Overweight and obesity among adults.
  1. 3.Kaska L, Kobiela J, Abacjew-Chmylko A, Chmylko L, Wojanowska-Pindel M et al. (2013) Nutrition and pregnancy after bariatric surgery. ISRN. Obes;2013: 492060.
  1. 4.Dag Z O, Dilbaz B. (2015) Impact of obesity on infertility in women. , J Turk Ger Gynecol Assoc2015; 16, 111-117.
  1. 5.Adams TD1 HA,DavidsonLE3,Laferrère B4,Fraser A5,Stanford JB6,Hashibe M6,Greenwood JL6,Kim J6, Taylor D7,Watson AJ8,Smith KR9,McKinlay R10,Simper SC10,Smith SC10,Hunt SC. Maternal and neonatal outcomes for pregnancies before and after gastric bypass surgery. International journal of obesity2015;. 39, 686-694.
  1. 6.Insummary. (2014) it is obvious that pregnancy after Triunfo S, Lanzone A: Impact of overweight and obesity on obstetric outcomes. , J Endocrinol Invest 37, 323-329.
  1. 7.Gletsu-Miller N, Wright. (2013) BN: Mineral malnutrition following bariatric surgery. Adv Nutr. 4, 506-517.
  1. 8.K M A.Preparing for and managing a pregnancy after bariatric surgery. Seminars in perinatology 2011;35:. 3560361.
  1. 9.SST Malik. (2012) ML.: Defining the role of bariatric surgery in polycystic ovarian sydrome patients. , World journal of diabetes 3.
  1. 10. (2008) Allied Health Sciences Section Ad Hoc Nutrition Cea: ASMBS Allied Health Nutritional Guidelines for the Surgical Weight Loss Patient. Surgery for obesity and related deseases : official journal of the American Society for Baristric Surgery. 4, 73-108.
  1. 11.Malinowski S S. (2006) Nutritional and metabolic complications of bariatric surgery. The American journal of the medical sciences. 331, 219-225.
  1. 12.Kehagias I, Karamanakos S N, Argentou M.Kalfarentzos F: Randomized clinical trial of laparoscopic Roux-en-Y gastric bypass versus laparoscopic sleeve gastrectomy for the management of patients with BMI < 50 kg/m2. Obesity surgery 2011;21:. 1650-1656.
  1. 13.A von Drygalski, Andris D A, Nuttleman P R, Jackson S, Klein J et al. (2011) JR: Anemia after bariatric surgery cannot be explained by iron deficiency alone: results of a large cohort study. Surgery for obesity and related diseases : official journal of the American Society for Bariatric Surgery. 7, 151-156.
  1. 14.DA Von Drygalski AA. (2009) Anemia after bariatric surgery: more than just iron deficiency. Nutrition in clinical practice : official publication of the American Society for Parenteral and Enteral Nutrition. 24, 217-226.
  1. 15.Shankar P, Boylan M. (2010) Sriram K: Micronutrient deficiencies after bariatric surgery. Nutrition. 26, 1031-1037.
  1. 16.Alexandrou A, Armeni E, Kouskouni E, Tsoka E, Diamantis T. (2014) Lambrinoudaki I: Cross-sectional long-term micronutrient deficiencies after sleeve gastrectomy versus Roux-en-Y gastric bypass: a pilot study. Surgery for obesity and related diseases : official journal of the American Society for Bariatric Surgery. 10, 262-268.
  1. 17.van Rutte PW, Aarts E O, Smulders J F, Nienhuijs S W. (2014) . Nutrient Deficiencies Before and After Sleeve Gastrectomy. Obesity surgery2014 .
  1. 18.Damms-Machado A, Friedrich A, Kramer K M, Stingel K, Meile T et al.SC: Pre- and postoperative nutritional deficiencies in obese patients undergoing laparoscopic sleeve gastrectomy. Obesity surgery 2012;22:. 881-889.
  1. 19.Saif T, Strain G W, Dakin G, Gagner M, Costa R. (2012) Pomp A: Evaluation of nutrient status after laparoscopic sleeve gastrectomy 1, 3, and 5 years after surgery. Surgery for obesity and related diseases : official journal of the American Society for Bariatric Surgery. 8, 542-547.
  1. 20.Di Renzo GC, Spano F, Giardina I, Brillo E, Clerici G. (2015) Roura LC: Iron deficiency anemia in pregnancy. Womens Health (Lond Engl). 11, 891-900.
  1. 21.VS.Anemia as the main manifestation of myelodysplastic syndromes. Seminars in hematology 2015;52:. 348-356.
  1. 22.Eltweri A M, Bowrey D J, Sutton C D, Graham L, Williams. (2013) RN: An audit to determine if vitamin b12 supplementation is necessary after sleeve gastrectomy. SpringerPlus. 2-218.
  1. 23.Pech N, Meyer F, Lippert H, Manger T, Stroh C. (2012) Complications and nutrient deficiencies two years after sleeve gastrectomy. BMC surgery. 12-13.
  1. 24.Pech N, Meyer F, Lippert H, Manger T, Stroh C.Complications, reoperations, and nutrient deficiencies two years after sleeve gastrectomy. , Journal of obesity2012; 2012, 828737.
  1. 25.Aarts E O, I M Janssen, F J Berends.The gastric sleeve: losing weight as fast as micronutrients? Obesity surgery 2011;21:. 207-211.
  1. 26.Toh S Y, Zarshenas N, Jorgensen J. (2009) Prevalence of nutrient deficiencies in bariatric patients. Nutrition. 25, 1150-1156.
  1. 27.Gehrer S, Kern B, Peters T, Christoffel-Courtin C, Peterli R.Fewer nutrient deficiencies after laparoscopic sleeve gastrectomy (LSG) than after laparoscopic Roux-Y-gastric bypass (LRYGB)-a prospective study. Obesity surgery 2010;20:. 447-453.
  1. 28.Finkelstein J L, Layden A J, Stover P J. (2015) . Vitamin B-12 and Perinatal Health. Adv Nutr 6, 552-563.
  1. 29.Dror D K, Allen.LH: Interventions with vitamins B6, B12 and C in pregnancy. Paediatr Perinat Epidemiol 2012;26 Suppl 1, 55-74.
  1. 30.Alvarez-Leite J I.Nutrient deficiencies secondary to bariatric surgery. Current opinion in clinical nutrition and metabolic care 2004;7:. 569-575.
  1. 31.Desouza C, Keebler M, McNamara D B, Fonseca V. (2002) Drugs affecting homocysteine metabolism: impact on cardiovascular risk. Drugs. 62, 605-616.
  1. 32.Allen L H.Causes of vitamin B12 and folate deficiency. Food and nutrition bulletin 2008;29:. 20-34.
  1. 33.Decker G A, Swain J M, Crowell M D.Scolapio JS: Gastrointestinal and nutritional complications after bariatric surgery. The American journal of gastroenterology 2007;102: 2571-2580; quiz 2581.
  1. 34.Mallory G N, Macgregor.AM: Folate Status Following Gastric Bypass Surgery (The Great Folate Mystery). Obesity surgery 1991;1:. 69-72.
  1. 35.de Luis DA, Pacheco D, Izaola O, Terroba M C, Cuellar L et al. (2008) Clinical results and nutritional consequences of biliopancreatic diversion: three years of follow-up. Annals of nutrition & metabolism. 53, 234-239.
  1. 36.Gemmel K, Santry H P, Prachand V N. (2009) Alverdy JC: Vitamin D deficiency in preoperative bariatric surgery patients. Surgery for obesity and related diseases : official journal of the American Society for Bariatric Surgery. 5, 54-59.
  1. 37.Hakeam H A, O'Regan P J, Salem A M, Bamehriz F Y.Eldali AM: Impact of laparoscopic sleeve gastrectomy on iron indices: 1 year follow-up. Obesity surgery 2009;19:. 1491-1496.
  1. 38.Ruiz-Tovar J, Oller I, Tomas A, Llavero C, Arroyo A et al.Calpena R: Mid-term Effects of Sleeve Gastrectomy on Calcium Metabolism Parameters, Vitamin D and Parathormone (PTH) in Morbid Obese Women. Obesity surgery 2012;22:. 797-801.
  1. 39.Dewey M H, R. (2011) Vitamin D and calcium status and appropriate recommendations in bariatric surgery patients. Gastrenterology nursing: the official journal of the Society of Gastrenterology Nurses ans Assiciates. 34, 367-374.
  1. 40.Keller J S, T.The role of the gastrointestinal tract in calcium homeostasis and bone remodelling. Osteoporosis international: a journal established as a result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 2013; 24 :. 2737-2748.
  1. 41.Holick M F.Vitamin D deficiency. The New England journal of medicine 2007;357:. 266-281.
  1. 42.Blum. (2008) Mea: Vitamin D(3) in fat tissue. Endocrine. 33, 90-94.
  1. 43.Coupaye M, Riviere P, Breuil M C, Castel B, Bogard C et al. (2014) Comparison of nutritional status during the first year after sleeve gastrectomy and Roux-en-Y gastric bypass. , Obesity surgery; 24, 276-283.
  1. 44.Moize V, Andreu A, Flores L, Torres F, Ibarzabal A et al. (2013) Long-term dietary intake and nutritional deficiencies following sleeve gastrectomy or Roux-En-Y gastric bypass in a mediterranean population. , Journal of the Academy of Nutrition and Dietetics; 113, 400-410.
  1. 45.Shin J S, Choi M Y, Longtine M S, Nelson D M. (2013) Vitamin D effects on pregnancy and the placenta. , Placenta; 31, 1027-1034.
  1. 46.Viljakainen H T, Saarnio E, Hytinantti T, Miettinen M, Surcel H et al. (2010) Maternal vitamin D status determines bone variables in the newborn. , J Clin Endocrinol Metab2010; 95, 1749-1757.
  1. 47.Marwaha R K, Tandon N, Chopra S, Agarwal N, Garg M K et al. (2011) Vitamin D status in pregnant Indian women across trimesters and different seasons and its correlation with neonatal serum 25-hydroxyvitamin D levels. , Br J Nutr2011; 106, 1383-1389.
  1. 48.Sorensen I M, Joner G, Jenum P A, Eskild A, Torjesen P A et al. (2012) Maternal serum levels of 25-hydroxy-vitamin D during pregnancy and risk of type 1 diabetes in the offspring. , Diabetes2012; 61, 175-178.
  1. 49.Liu N Q, Hewison M. (2012) Vitamin D the placenta and pregnancy. , Arch Biochem Biophys2012; 523, 37-47.
  1. 50.Baker A M, Haeri S, Camargo C A, Espinola J A, Stuebe A M. (2010) A nested case-control study of midgestation vitamin D deficiency and risk of severe preeclampsia. , J Clin Endocrinol Metab2010; 95, 5105-5109.
  1. 51.5Chimienti F, Aouffen M, Favier A.Seve M.(2003) Zinc homeostasis-regulating proteins: new drug targets for triggering cell fate. Current drugs targets2003;. 4, 323-338.
  1. 52.McCall K A, Huang C, C A Fierke. (2000) Function and mechanism of zinc metalloenzymes. The journal of nutrition; 130: 1437S -. 1446.
  1. 53.Di Martino Gea. (1993) Relationship between zinc and obesity. , Journal of medicine; 24, 177-183.
  1. 54.GCea Sturniolo. (1991) Inhibition of gastric acid secretion reduces zinc absorption in man. , Journal of the American College of Nutrition;10: 372-375.
  1. 55.Prasad A S.Effects of zinc deficiency on. Th1 and Th2 cytokine shifts. The Journal of infectious diseases 2000;182 Suppl 1, 62-68.
  1. 56.Bhatnagar S T.S.: Zinc and cognitive development. The British journal of noutrition 2001;85. , Suppl 2, 139-145.
  1. 57.Mea Andriollo-Sanchez.Zinc intake and status in middle-aged and older European subjects: the ZENITH study. European journal of clinical nutrition 2005;59 Suppl 2, 37-41.
  1. 58.Wilson H O. (2014) Datta DB: Complications from micronutrient deficiency following bariatric surgery. Ann Clin Biochem. 51, 705-709.
  1. 59.Wang H, Hu Y F, Hao J H, Chen Y H, Su P Y et al. (2015) Maternal zinc deficiency during pregnancy elevates the risks of fetal growth restriction: a population-based birth cohort study. Sci Rep. 5, 11262.
  1. 60.Tamura T, Goldenberg R L, Johnston K E, DuBard M. (2000) Maternal plasma zinc concentrations and pregnancy outcome. , Am J Clin Nutr 71, 109-113.
  1. 61.Aea Salle.Zinc deficiency: a frequent and underestimated complication after bariatric surgery. Obesity surgery 2010;20:. 1660-1670.
  1. 62.Barbagallo M, L J Dominguez, L M Resnick. (2007) Magnesium metabolism in hypertension and type 2 diabetes mellitus. American journal of therapeutics. 14, 375-385.
  1. 63.Barbagallo M, L J Dominguez, L M Resnick.Magnesium metabolism in type 2 diabetes mellitus, metabolic syndrome and insuline resistance. Archives of biochemistry and biophysics 2007;458:. 40-47.
  1. 64.Young G. (2009) Leg cramps. Clinical evidence.
  1. 65.Guerrera M P, S L Volpe, Moa J J.Therapeutic uses of magnesium. American family physician 2009;80:. 157-162.
  1. 66.Schlegel R N, Cuffe J S, Moritz K M. (2015) Paravicini TM: Maternal hypomagnesemia causes placental abnormalities and fetal and postnatal mortality. Placenta. 36, 750-758.
  1. 67.Arnaud M J. (2008) Update on the assessment of magnesium status. , Br J Nutr;99Suppl3: S24 - 36.
  1. 68.Takaya J, Yamato F, Higashino H, Kobayashi Y. (2004) Relationship of intracellular magnesium of cord blood platelets to birth weight. Metabolism. 53, 1544-1547.
  1. 69.Rayman M P. (2000) The importance of selenium to human health. , Lancet; 356, 233-241.
  1. 70.Pieczynska J, Grajeta H. (2015) The role of selenium in human conception and pregnancy. , J Trace Elem Med Biol; 29, 31-38.
  1. 71.Mistry H D, Broughton Pipkin F, Redman C W, Poston L. (2012) Selenium in reproductive health. , Am J Obstet Gynecol; 206, 21-30.
  1. 72.Skröder HM1 HJ.Tofail F2, Persson LÅ3, Vahter ME4, Kippler MJ: Selenium status in pregnancy influences children's cognitive function at 1.5 years of age. Clinical nutrition 2015;34:. 923-930.
  1. 73.Boldery R, Fielding G, Rafter T, A L Pascoe, G M Scalia.Nutritional deficiency of selenium secondary to weight loss ( bariatric) surgery associated with life-threatening cardiomyopathy. Heart, lung and circulation 2007;16:. 123-126.
  1. 74.K R. (2007) Managing micronutrient deficiency in bariatric surgical patients: treatment of obesity patient. 379-394.
  1. 75.Alasfar F, Ben-Nakhi M, Khoursheed M, E O Kehinde, Alsaleh M.Selenium is significantly depleted among morbidly obese femele patients seeking bariatric surgery. Obesity surgery 2011;21:. 1710-1713.
  1. 76.CIea Prodan.Copper deficiency after gastric surgery: a reason for caution. The American journal of the medical sciences 2009;337:. 256-258.
  1. 77.Juhasz-Pocsine K, S A Rudinicki, R L Archer, S I Harik. (2007) Neurologic complications of gastric bypass surgery for morbid obesity. Neurology. 68, 1843-1850.
  1. 78.Wapnir R A.Copper absorption and bioavailability. The American journal of clinical nutrition 1998;67:. 1054-1060.
  1. 79.Danks D M.Copper deficiency in humans. Annual review of nutrition 1988;8:. 235-257.
  1. 80.Saltzman E, Karl J P.Nutrient deficiencies after gastric bypass surgery. , Annu Rev Nutr 2013, 183-203.
  1. 81.Sengupta S, Bhaskar M V, Haq I. (2010) A study of micronutrient status in pregnancy. , J Indian Med Assoc; 108, 817-822.
  1. 82.Ladipo O A. (2000) Nutrition in pregnancy: mineral and vitamin supplements. The American journal of clinical nutrition;72:. 280-290.
  1. 83.Koffman B M, L J Greenfield, Ali, N A Pirzada.Neurologic complications after surgery for obesity. Muscle and nerve 2006;33:. 166-176.
  1. 84.Tea Grune.Beta-caritene is an important vitamin A source for humans. The journal of nutrition 2010;140:. 2268-2285.
  1. 85.Genaro Pde SM, A L.Vitamin A supplementation and risk of skeletal fracture. Nutrition reviews 2004;62:. 667.
  1. 86.Crandall C. (2004) Vitamin A intake and osteoporosis: a clinical review. , Journal of women’s health; 13, 939-953.
  1. 87.Chaves G V, S E Pereira, C J Saboya, Ramalho.A.: Nutritional status of vitamin A in morbid obesity before and after Roux-en-Y gastic bypass. Obesity surgery2007;17:. 970-976.
  1. 88.Rea Clements.Incidence of vitamin deficiency after laparoscopic Roux-en-Y gastric bypass in a university hospital setting. discussion 1202-1194.The American surgeon 2006;72:. 1196-1202.
  1. 89.Eerdekens A, Debeer A, G Van Hoey, C De Borger, Sachar V et al. (2010) Maternal bariatric surgery: adverse outcomes in neonates. , Eur J Pediatr;169: 191-196.
  1. 90.PMV Dreyfus, M.Effects of thiamine deficiency on the central nervous system. The American journal of clinical nutrition 1961;9:. 414-425.
  1. 91.Berger J R.The neurological complications of bariatric surgery. , Archives of neurology 2004, 1185-1189.
  1. 92.Hovdenak N.Haram K.(2012) Influence of mineral and vitamin supplements on pregnancy outcome. , Eur J Obstet Gynecol Reprod Biol;164: 127-132.
  1. 93.Robitaille J, Carmichael S L, Shaw G M. (2009) Olney RS.(1997-2003) National Birth Defects Prevention S: Maternal nutrient intake and risks for transverse and longitudinal limb deficiencies: data from the National Birth Defects Prevention Study, Birth Defects Res A Clin Mol Teratol. 85, 773-779.
  1. 94.Mock D M.Marginal Biotin Deficiency is Common in Normal Human Pregnancy and Is Highly Teratogenic in Mice. The journal of nutrition 2009;139:. 154-157.
  1. 95.Sharma R, Mehta S. (2014) Ascorbic Acid concentration and preterm premature rupture of membranes. , J Obstet Gynaecol India; 64, 417-420.
  1. 96.Jendryczko A, Tomala J. (1995) The total free radical trapping ability of blood plasma in eclampsia. Zentralbl Gynakol;117: 126-129.
  1. 97.Moize V, Deulofue R, Torres F, Osaba J M de, Vidal J.Nutritional intake and prevalence of nutritional deficiencies prior to surgery in a Spanish morbidly obese population. Obesity surgery 2011;21:. 1382-1388.
  1. 98.Hamoui N, G J Anthone, H S Kaufmann, P F Crookes.Sleeve gastrectomy in the high-risk patient. Obesity surgery 2006;16:. 1445-1449.
  1. 99.Virji A M, M.Caring for patients after bariatric surgery. American family physician 2006;73:. 1403-1408.
  1. 100.Snyder-Marlow G, Taylor D, Lenhard M. (2010) Nutrition care for patients undergoing laparoscopic sleeve gastrectomy for weight loss. , Journal of the American Dietetic Association;110: 600-607.
  1. 101.Je Gille. (2007) [A sizeable chance--surgical managment of profound obesity concurrent with post -traumatic osteoarthrosis]. Der Unfallchirung;110:. 450-455.
  1. 102.JIea Mechanick. (2008) American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery Medical guidelines for clinical practice for the perioperative nutritional, metabolic and nonsurgical support of the bariatric surgery patient Endocrine practice: official journal of the American College of Endocrinology and the American Association of Clinical Endocrinologists;14Suppl1:. 1-83.
  1. 103.JIea Mechanick. (2013) Clinical practise guidelines for the perioperaive 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);21Suppl1:. 1-27.
  1. 104.Aarts E O, Janssen I M, Berends.FJ: The gastric sleeve: losing weight as fast as micronutrients? Obesity surgery 2011;21:. 207-211.
  1. 105.Toh S Y, Zarshenas N, Jorgensen J.Prevalence of nutrient deficiencies in bariatric patients. , Nutrition 2009, 1150-1156.
  1. 106.Ruiz-Tovar J, Oller I, Tomas A, Llavero C, Arroyo A et al.Calpena R: Mid-term effects of sleeve gastrectomy on calcium metabolism parameters, vitamin D and parathormone (PTH) in morbid obese women. Obesity surgery 2012;22:. 797-801.
  1. 107.Salle A, Demarsy D, Poirier A L, Lelievre B, Topart P et al.Rohmer V: Zinc deficiency: a frequent and underestimated complication after bariatric surgery. Obesity surgery 2010;20:. 1660-1670.
  1. 108.Hamoui N, Anthone G J, Kaufman H S, Crookes P F. (2006) Sleeve gastrectomy in the high-risk patient. Obesity surgery;16:. 1445-1449.