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Introduction

Bariatric surgery is an effective tool for achieving durable weight loss and improving weight-related comorbidities with relatively low incidences of report-ed morbidity and mortality.1 Bariatric procedures induce weight loss by imparting restriction, malab-sorption, or a combination of both. However, the caloric restriction and/or malabsorption that accom-panies these weight-loss procedures can put patients at risk for developing significant nutritional deficien-cies that can lead to metabolic bone disease,2-5 neuro-logic abnormalities,6-11 and protein malnutrition.12-16 Some of these deficiencies can develop rapidly after surgery, and most worsen with time as body stores of nutrients and vitamins are depleted within 1 year of surgery. Ironically, given the perception that weight gain is related to overeating, therefore leading the obese individual to get adequate nutrients, it has been reported that preoperative nutrient levels in many of these patients are suboptimal.17-19

As more bariatric operations are performed, the po-tential increases for more patients to present with nutrient abnormalities. Therefore, health care practi-tioners must learn to recognize and treat the nutritional consequences of weight-loss operations as well as know how to screen for and prevent deficiencies.

This review begins with the B vitamins and iron, of which most practitioners are aware for the potential of health concerns. Calcium and vitamin D are addressed next because of their effect on bone health. The other fat soluble vitamins—A, E, and K—are then discussed, followed by the trace minerals that may be of concern postoperatively. Protein malnutrition is reviewed last.

The B Vitamins

The B vitamins are comprised of 8 essential nutrients. Levels have been analyzed in patients before and after weight-loss surgery. Reports show preoperative defi-ciencies of cyanocobalamin (vitamin B12), thiamine (vita-min B1), and pyridoxine (vitamin B6). All of these, along with folate (vitamin B9) and riboflavin (vitamin B2), have been shown to be low postoperatively.

V

ITAMIN

B

12

Vitamin B12 deficiency is among the most common nutritional consequences of weight-loss surgery. Operations that limit stomach capacity significantly impair the body’s ability to absorb vitamin B12. Following bariatric surgery, the remaining smaller gastric pouch secretes less acid, which leads to incomplete release of vitamin B12, a food-bound vitamin. There is also less intrinsic factor—a protein produced by glands in the

lthough bariatric surgery can aid patients in rapidly losing large amounts of

unhealthy excess weight, nutritional complications that range from mild to

severe can follow.

Nutritional Deficiencies

Following Bariatric

Surgery

A

L

IZ

G

OLDENBERG

, MPH, RD, CDN

NewYork-Presbyterian Hospital/ Weill Cornell Medical Center New York City, New York

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Treatments for deficiency can be given in many forms: oral crystalline tablets, sublingual preparations, intramuscular (IM) injections, and nasal sprays.27 One recommendation is 1,000 to 3,000 mcg of vitamin B12 given IM postoperatively and then repeated every 6 to 12 months.28

T

HIAMINE

A variety of food sources contain significant amounts of thiamine (Table 1). Rice-based diets, diets high in other refined starches, or chronic alcohol consumption put people at risk for developing thiamine deficiency, also known as beriberi. Bariatric surgery, malabsorption, and prolonged vomiting can further increase this risk. Low preoperative thiamine levels were found in 15.5% and 29% of patients presenting for obesity surgery at centers in Florida and New York, respectively.19,29 Beriberi may be more common in blacks and Hispanics than in whites.17

Early thiamine deficiency produces fatigue, poor memory, anorexia, and abdominal discomfort. Wernicke-Korsakoff syndrome may present with eye changes, atax-ia, confusion, and encephalopathy, which may lead to coma.28,30 Cardiovascular changes (“wet beriberi”) may be recognized as high cardiac output with vasodilation and warm extremities, which can lead to heart failure.

Neurologic effects (“dry beriberi”) include paresthe-sias of the toes, burning in the feet, muscle cramps in the calves, and hyporeflexia. Thaisetthawatkul et al noted that 16% of patients undergoing bariatric surgery had peripheral neuropathy, which was positively corre-lated with the rate and amount of weight loss, reduced serum albumin and transferrin, gastrointestinal compli-cations, and attendance at a nutrition clinic.8It should be noted that many other, more rare nutrient deficien-cies—including vitamin E, vitamin B6, and copper—also cause neuropathies. It is unclear whether thiamine or another nutrient or combination of nutrients is responsi-ble for the neuropathy seen after weight-loss surgery, which was recently termed acute postgastric reduction surgery neuropathy.7,8

Thiamine deficiency has been seen in patients follow-ing both restrictive and malabsorptive operations.7,9,10 Most reports are of young women following a period of prolonged vomiting about 4 to 12 weeks after surgery, possibly because vitamin stores last approximately 3 to 6 weeks.11,20,31

Because postoperative dietary assessments show inadequate thiamine intake, a daily multivitamin con-taining thiamine is recommended.6,32Treatment options include 50 to 100 mg of I.V. or IM thiamine daily for 2 days followed by 20 mg orally for 2 weeks11,20,33 or 100 mg of thiamine, I.V. or IM, for 7 to 14 days followed by 10 mg orally daily.27To treat encephalopathy, 100 mg I.V. every 8 hours has been recommended.28

F

OLATE

Inadequate levels of folate may result from foods having less exposure to gastric acid and to the upper

Table 1.

Food Sources of Vitamins

Nutrient: Vitamin Thiamine (B1) Riboflavin (B2) Vitamin B6 (pyridoxine) Folate* Vitamin B12 (cyanocobalamin) Vitamin A Food Source

Beef, pork, whole grains, dried beans, peas

Enriched grains, liver, milk, wheat germ, yeast

Whole grains, nuts, bananas, meats, beans

Oranges, liver, beans, green leafy vegetables

Beef, poultry, fish, liver, eggs, milk

Butter, margarine, eggs, milk, liver, fish oil, apricots, cantaloupe, carrots, pumpkin, sweet potato (beta-carotene sources) Vitamin D

Vitamin E

Eggs, fish oil, sardines, salmon, liver, milk

Vegetable oils and margarine, green leafy vegetables, nuts, seeds, wheat germ

Vitamin K Green leafy vegetables, green tea, liver, soy beans, soybean oil

stomach lining—available to bind to the vitamin in the duodenum. Intrinsic factor and vitamin B12 form a complex that is later absorbed in the ileum.20,21 Also, many foods that are good sources of vitamin B12may be difficult for the postoperative patient to tolerate, and are thus avoided (Table 1).

In 1 study, 5% of patients were found to be deficient in vitamin B12 preoperatively,22 whereas at least 3 other studies found that levels were adequate.17,23,24 Postoperatively, deficiency is common after vitamin stores are depleted, at approximately the 1-year mark. Symptoms of deficiency include glossitis, weakness, depression, poor appetite, megaloblastic anemia, peripheral neuropathy, and ataxia. The amount of vita-min B12 in standard multivitamins is not adequate to prevent deficiency or elevated homocysteine lev-els.23-25Because early deficiency may not be sympto-matic, patients should undergo regular blood work and be proactively supplemented with 100 to 350 mcg of crystalline B12daily.24,26,27

*Folic acid is the synthetic form of folate.

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section of the small intestine after surgery. Folate is an essential component in metabolic pathways and is nec-essary to form DNA and red blood cells. Many patients undergoing bariatric surgery are women of childbearing age; thus, folate deficiency can be a special concern because of its correlation with neural tube birth defects.34,35Other complications to note are myelopa-thy, peripheral neuropamyelopa-thy, restless leg syndrome, sore red tongue, confusion, and weakness. Low folate levels are not as prevalent as vitamin B12 and iron deficien-cies.20

Multivitamin supplements appear adequate to pre-vent folate deficiencies.24,37 If deficiency is detected, noncompliance with daily multivitamin supplements that contain 400 mcg of folic acid should be suspected. Folate deficiency can be easily treated with resumption of same.37

V

ITAMIN

B

6AND

R

IBOFLAVIN

A few studies have examined the vitamin B6 and riboflavin status of bariatric surgery patients. Nutritionists are aware of health issues associated with deficiencies of these vitamins. Vitamin B6 deficiency may cause anemia, dermatitis, seizures, and neuro-pathies.6Riboflavin deficiency may cause anemia, stom-atitis, rash, and impaired growth.

Boylan et al found preoperative vitamin B6 deficiency in 46% of patients.24A second study conclud-ed that postoperative vitamin B6levels were insufficient in most patients despite taking a supplement containing 1.6 mg daily, which was the US recommended daily allowance at the time of the study.32 (Note that the 2004 Dietary Reference Intake [DRI], still in use today, is actually lower, at 1.3 mg per day.) Other studies con-clude that in the absence of prolonged vomiting, a sup-plement containing the DRI for vitamin B6 should be adequate for these patients.6,38 High-protein diets increase the need for vitamin B6.39 Also, there is evi-dence that supplementation of vitamin B6 may improve the symptoms of carpal tunnel syndrome.40

The limited data available on riboflavin seem to con-clude that postoperative intakes may be inadequate, but as with vitamin B6 and in the absence of protracted vomiting, supplementing with multivitamins that con-tain riboflavin should prevent tissue depletion.38

Iron

Iron deficiency and anemia are frequent concerns regarding pre- and postoperative bariatric surgery patients. The 3 most common causes for iron deficiency appear to be decreased absorption of iron because of bypass of the duodenum; less gastric acid, so iron is therefore not reduced to its more absorbable ferrous form; and lower iron intake from avoiding certain foods (Table 2). Iron is necessary for numerous oxidation-reduction reactions and as a means of oxygen transport in hemoglobin. Common symptoms of deficiency are fatigue, glossitis, stomatitis, and impaired temperature regulation (complaints of feeling cold). There have been

Table 2.

Food Sources of Minerals

Nutrient: Mineral Calcium Copper Iron Selenium Zinc Food Source

Dairy products, canned fish with bones, almonds, brazil nuts, oysters, tofu

Eggs, fish, kidney, liver, poultry, nuts, legumes, whole grains

Green leafy vegetables, blackstrap molasses, eggs, fish, legumes, liver, beef, poultry, enriched cereals

Brazil nuts, whole grains, beef, seafood

Nuts, meat, liver, eggs, seafood, whole grains

reports of pica—strong cravings for non-nutritive sub-stances such as ice or clay—after gastric bypass, which were treated with iron supplementation.41

There have been reports of preoperative iron defi-ciency ranging from 14% to 44% of patients.17,22Studies show that iron levels continuously decline after surgery. Iron deficiency does not appear to correlate with the amount of weight lost.4Incidence as high as 74% have been reported following distal Roux-en-Ygastric bypass (RYGB).42 The risk is highest for menstruating women, who lose 30 mcg/kg per day of iron during bleeding.43

Supplementation is recommended for all patients undergoing weight-loss operations, although the amount of iron in multivitamins is inadequate to pre-vent deficiency in most.5,42,44Noncompliance with pre-scribed supplements is a concern, and because of gastrointestinal intolerance and constipation,24,44,46 different dosages and forms of iron supplementation have been suggested. One such regimen is 40 to 65 mg of ferrous iron as gluconate, sulfate, or fumarate 3 times per day.27Another suggestion is 320 mg of fer-rous sulfate twice per day.44The addition of vitamin C to iron therapy following gastric bypass may be bene-ficial.5 At least 1 practice has reported it regularly treats deficiency with I.V. iron.47

Calcium and Vitamin D

There are multiple reports of increased bone turnover and reduced bone mineral density following bariatric surgery. Calcium is absorbed in the duodenum and jejunum, whereas vitamin D is absorbed in the jejunum and ileum.48The anatomical changes from surgery along

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Table 4.

Suggested Laboratory

Analyses Following Weight-Loss

Surgery (3 months, 6 months, 1 year,

annually thereafter)

ALT, albumin, ALP, AST, BUN, calcium, cholesterol, creatinine, glucose, phosphorus, total protein, triglycerides Vitamin A Vitamin B12, folate Magnesium PTH (Intact) Ceruloplasmin (copper) CBC PT/PTT Selenium Vitamin D25total, fractionated D2and D3

Iron, TIBC, ferritin, transferrin

Thiamine (vitamin B1)

Zinc

ALT, alanine aminotransferase; ALP,alkaline phosphatase;

AST, aspartate aminotransferase; BUN,blood urea nitrogen;

CBC, complete blood count; PT/PTT, prothrombin time/partial thromboplastin time; TIBC, total iron-binding capacity

explanation is decreased vitamin D bioavailability due to enhanced uptake and clearance by adipose tissue.50,51 Malabsorption of fat-soluble vitamins caused by the delayed mixing of bile and pancreatic enzymes with fat also contributes to lowering vitamin D levels postopera-tively. Malabsorptive procedures such as biliopancreatic diversion (BPD) and duodenal switch (DS) carry a high-er risk of metabolic bone disease.

It should be noted that vitamin D deficiencies and elevated PTH levels are seen both pre- and postopera-tively. Buffington et al found that 62% preoperative obese subjects were vitamin D deficient,50 and Sanchez-Hernandez et al found that number to be 69%.51 Additionally, there was a negative correlation between vitamin D levels and body mass. Postoperatively, there are reports of hypocalcemia, elevated alkaline phosphatase, PTH, and N-telopeptide levels, as well as decreased bone density at the total hip, trochanter, and total body.2,20,49,52-55 Patients with early bone disease may present with fatigue, hypocalcemic tetany, arthral-gia, and myalgia that can progress to osteomalacia, dif-fuse bone pain from microfractures, and, ultimately, spontaneous fractures.28,34

Although there is universal support for supplement-ing both nutrients, there are mixed results as to whether supplementation leads to improvements in PTH levels or other bone markers. Weight loss independently causes bone loss.56Daily supplementation to a level of 1,200 mg of calcium and 8 mcg of vitamin D (equivalent to 320 IU)49or even 1,200 mg calcium and 800 IU, in addi-tion to dietary sources,2 may not be sufficient protec-tion. Riedt et al supplemented gastric bypass patients with a total intake of 1,800 mg of calcium daily and test-ed their calcium absorption.57 Calcium absorption decreased but remained within a normal range, whereas markers of bone resorption increased significantly after surgery. In the authors’ New York City practice, patients often require daily therapy with 1,600 mg of calcium and 2,400 IU of vitamin D3(or 14,000 IU vitamin D2) to sup-press PTH levels (unpublished data). It is inconclusive as to whether gastric acid affects calcium absorption,58yet most recommendations are for calcium supplements in the citrate form because its absorption is less affected by a low-acid environment.

Other Fat-Soluble Vitamins: A, E, and K

The mechanism whereby inadequate exposure of nutrients to biliopancreatic secretions imparts malab-sorption is mentioned above. Malabmalab-sorption of fat and fat-soluble vitamins has significant nutritional conse-quences. There are at least 4 published accounts of vita-mins A, K, and E deficiencies in the literature. Patients undergoing malabsorptive surgeries clearly raise more serious concerns than those whose operations impart merely restriction.55,59,60 Calculating fecal fat measure-ments in 10 DS and 9 RYGB patients, Gagner et al found that DS patients excreted 81% of the fat they con-sumed—significantly more than the RYGB group.61

Hypovitaminosis A is most commonly linked with eye

Table 3.

Suggested Nutritional

Laboratory Analyses Prior to

Weight Loss Surgery

Albumin

Vitamin B12, folate

Vitamin D25

CBC

Iron, TIBC, ferritin, transferrin

PTH (intact)

Thiamine (vitamin B1)

CBC,complete blood count; PTH, parathyroid hormone; TIBC,

total iron-binding capacity

with limited intake of dairy products because of intoler-ance can decrease both calcium and vitamin D absorp-tion and intake.34 High-protein intakes also tend to increase urinary calcium excretion.48

Vitamin D plays an essential role in calcium absorp-tion. Deficiencies of vitamin D and calcium cause an ele-vation of parathyroid hormone (PTH), which subse-quently increases calcium resorption from bone.49 The exact etiology of deficiency in the obese is still unclear, but it is affected by climate, wearing sunscreen and cov-ering skin, and skin pigmentation, because vitamin D is synthesized in the skin from sun exposure. Another

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Table 5.

Suggested Supplementation

Following Weight-Loss Surgery

Roux-en-Y Gastric Bypass

Calcium citrate 1,200 mg (with vitamin D)

Irona

Multivitaminb

Laparoscopic Adjustable Gastric Band

Calcium citrate 600-1,200 mg (with vitamin D)c

Multivitaminb

Duodenal Switch

Vitamin A 25,000 IU

Calcium citrate 1,200-1,600 mg

Vitamin D31,200 IU daily

or vitamin D250,000 per week

Irona

Multivitaminb

aIron should contain vitamin B12, vitamin C, and folic acid, or should be added separately

bMultivitamin should contain zinc and selenium

cMen: 600 mg, women: 1,200 mg or based on individual intake of dairy

disease. In addition to night blindness, eye-related symptoms of vitamin A deficiency include xeropthalmia, Bitot’s spots, and keratomalacia. Skin signs include xero-sis and petechiae. There are at least 4 accounts of post-bariatric surgery night blindness.62-65Treatments varied between 10,000 IU of oral vitamin A daily; 100,000 IU of IM vitamin A 3 times daily; and 300,000 IU of IM vitamin A twice weekly for 4 weeks along with 100,000 IU of oral vitamin A daily (1 case study did not detail supple-ment dosing). Many multivitamins contain 3,500 to 5,000 IU of vitamin A, but this may be inadequate.42 Marceau et al suggested 25,000 IU daily for patients undergoing BPD and DS.13A review of patients with BPD and DS in New York and Australia found inadequate serum vitamin A levels in 52% (n=46) after 1 year and 69% (n=28) after 4 years.55In patients with distal RYGB, only 10% demonstrated deficiency.42

Less is known about vitamins K and E. Available data on the incidence of vitamin K deficiency show that between 42% and 68% of patients are deficient after malabsorptive surgeries.55 Low levels of this vitamin alter clotting and result in an increased tendency for bleeding, which may present as excessive bruising or bleeding gums. One suggestion is to supplement vita-min K for international normalized ratio greater than 1:4.13

Reports of vitamin E deficiency rarely appear in patients who receive multivitamin supplements contain-ing vitamin E. Low levels of this antioxidant vitamin have been associated with neurologic abnormalities.6Boylan et al found that 23% of patients had marginal tocopherol levels preoperatively, and postoperatively, levels corre-lated with vitamin E supplement intake.24More recently, Slater and Dolan found only 4% and 5% of patients, respectively, to be deficient.14,55 Most programs do not currently measure vitamin E levels.20

Zinc

Low zinc levels may be associated with hair loss, dermatitis, impaired immunity, and delayed wound healing. There is very little research relating zinc defi-ciency with hair changes following bariatric surgery. Situations that likely play a role in deficiency include the primary site of zinc absorption being bypassed in weight-loss operations that alter the gastrointestinal tract, a reduced intake of foods that provide good sources of zinc (Table 2), and increased stool losses via steatorrhea.

Preoperative zinc deficiency was reported in 5.2% to 16.7% of patients;66postoperatively, reports are var-ied. Approximately 10.5% to 50% of malabsorptive surgery patients have been found to have low zinc levels.14,55,66 However, zinc blood levels alone are not considered an accurate measure of zinc status.

A recent study analyzed plasma, erythrocyte, and urinary zinc levels after RYGB and found changes that might lead to long-term deficiency as well as lower zinc intakes.18 The authors concluded that zinc sup-plementation is necessary beginning 2 months

post-operatively in patients who present with normal levels preoperatively. They also recommended that zinc dietary intake, as well as plasma and urinary levels, should be monitored regularly after surgery. Another study correlated cessation of hair loss with supple-mentation of 200 mg zinc sulfate 3 times daily, but blood levels were not checked in this report.67

Copper

Copper is a trace mineral that plays an essential role in the structure and function of the nervous system. Absorption is probably in the stomach and duodenum. Kumar et al reported a case of copper deficiency in a woman who had undergone gastric bypass surgery 12 years earlier. The patient presented with a 9-month history of progressive hand and leg parasthesia and unsteadiness. She had multiple nutrient deficiencies and was taking many supplements, including 150 mg of zinc daily. High-dose zinc supplementation interferes with copper bioavailability by increasing levels of a copper-binding protein that prevents cop-per absorption.34,68

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Selenium

Selenium is an antioxidant mineral that is absorbed in the duodenum and works closely with vitamin E. There are very limited data on the importance of seleni-um after bariatric surgery, although there have been reports of both preoperative and postoperative defi-ciencies. Prior to RYGB and laparoscopic adjustable gastric band (LAGB), 6% and 6.3% of patients, respec-tively, had low selenium levels. One year following sur-gery, 7.7% of RYGB and 40% of LAGB patients were selenium deficient.66 Dolan et al reported selenium deficiency in 14.5% of patients following malabsorp-tive surgery.14

There is a case report of selenium deficiency following biliopancreatic diversion surgery.69 The report, published in 2007, describes a man who pre-sented with life-threatening heart failure after losing 100 kg of body weight over nine months. He showed dramatic improvement after selenium deficiency was corrected.

Protein

Considerable research has been devoted to the inci-dence and implications of protein malnutrition in bariatric surgery patients. Statistics vary widely on the percentage of affected patients. Hypoalbuminemia has been described as ranging from 1.3% to 33% of patients. The variations may reflect largely on the sur-gical program’s degree of preoperative nutrition edu-cation and postoperative follow-up.12,15,16,70,71

Protein malnutrition is commonly precipitated by complications such as stricture, excessive vomiting, or what authors consider noncompliance. There is more frequent and more severe hypoalbuminemia in patients who undergo more malabsorptive procedures such as BPD and DS, but it can present after RYGB. In many cases, conventional treatment with nutritional counsel-ing can be effective in reverscounsel-ing malnutrition. Helpcounsel-ing patients increase their intake of protein via foods and liquid supplements so they are consuming 1.5 g/kg ideal body weight or 105 g of protein daily is often an effec-tive intervention.12,71,72Pancreatic enzymes can be used to counteract the effects of malabsorption. More aggressive treatments, such as I.V. nutrition (total par-enteral nutrition) may be required.12Ultimately, a small number of patients will require partial or total reversal of their surgeries to correct deficiencies.73

Conclusion

Although there are numerous benefits to the weight loss attributed to bariatric surgery, there is growing evidence that nutritional consequences exist. Significant nutritional deficiency may be seen in the obese both before and after their procedures. These nutritional abnormalities may be difficult to detect, with symptoms ranging in severity from mild to life threatening. Caring for patients who undergo weight-loss surgery presents a challenge for health care pro-fessionals. Noncompliance with follow-up care and

supplementation may contribute to the undesirable consequences of surgery. A team of physicians, nutri-tionists, and psychologists who monitor blood values, reinforce the importance of regular supplementation, and address the psychological needs of these patients can help improve and possibly prevent significant side effects from bariatric surgery.46,74

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AUTHOR DISCLOSURE—Ms. Goldenberg is a speaker for BariMD and the American Society for Metabolic and Bariatric Surgery.

DISCLAIMER—This review is designed to be a summary of information, and represents the opinions of the author. Although detailed, the review is not exhaustive. Readers are strongly urged to consult any relevant primary literature, the complete prescribing information available in the package insert of each drug, and the appropriate clinical protocols. No liability will be assumed for the use of this review, and the absence of typographical errors is not guaranteed. Copyright © 2007, McMahon Publishing, 545 West 45th Street, 8th Floor, New York, NY 10036. Printed in the USA. All rights reserved, including right of reproduction, in whole or in part, in any form.

Copyright © 2007 McMahon Publishing Gr

oup unless otherwise noted.

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Figure

Table 1. Food Sources of Vitamins
Table 2. Food Sources of Minerals
Table 4. Suggested Laboratory Analyses Following Weight-Loss Surgery (3 months, 6 months, 1 year, annually thereafter)

References

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