Nutrient deficiencies secondary to bariatric surgery

Jacqueline I. Alvarez-Leite

Purpose of review Introduction

The number of adolescent and adult patients submitting to Obesity is a multifactorial disease where the excess of
bariatric surgery is increasing rapidly around the world. This body fat is related to genetic predisposition and, mainly,
review describes the literature published in the last few years environmental factors. Patients with severe obesity often
concerning nutritional deficiencies after bariatric surgery as well suffer serious illness as well as physical and psychological
as their etiology, incidence, treatment and prevention. disabilities that markedly increase mortality and morbid-
Recent findings ity. Certainly, the first-choice therapy for severe obesity
Although bariatric surgery was first introduced in the 1950s, is a nonsurgical program that integrates behavior
safe and successful surgical management has progressed over modifications, adequate physical activity and psycho-
the last two decades and longer post-surgical follow-up data logical support. However, in many cases of severe
are now available. Most of the patients undergoing obesity, nonsurgical treatment fails in providing sus-
malabsorptive procedures will develop some nutritional tained weight loss and surgical treatment can be
deficiency, justifying mineral and multivitamin supplementation indicated in some specific cases (body mass index 440
to all postoperatively. Nutrient deficiency is proportional to the or 435 with comorbities).
length of absorptive area and to the percentage of weight loss.
Low levels of iron, vitamin B12, vitamin D and calcium are Although bariatric surgery was first introduced in the
predominant after Roux-en-Y gastric bypass. Protein and fat- 1950s, safe and successful surgical management has
soluble vitamin deficiencies are mainly detected after progressed over the last two decades [1 .]. However, due
biliopancreatic diversion. Thiamine deficiency is common in to undernutrition imposed on the patient and inherent
patients with frequent vomiting. As the incidence of these complications after all bariatric procedures, patients
deficiencies progresses with time, the patients should be should be regularly accompanied, in both the pre and
monitored frequently and regularly to prevent malnutrition. post-operative periods, by a multidisciplinary team with
Summary medical, surgical, psychiatric, and nutritional expertise
Nutritional deficiencies can be prevented if a multidisciplinary [2 .].
team regularly assists the patient. Malnutrition is generally
reverted with nutrient supplementation, once it is promptly There are several recent studies showing fast improve-
diagnosed. Especial attention should be given to adolescents, ment of major obesity complications after bariatric
mainly girls at reproductive age who have a substantial risk of surgery [3 .,4–7]. However, the most important outcomes
developing iron deficiency. Future studies are necessary to of any weight-loss program should also include long-term
detect nutrient abnormalities after new procedures and to data of changes in health-related quality of life [8,9] as
evaluate the safety of bariatric surgery in younger obese well as a close follow up of psychological and nutritional
patients. status. The improvement of health quality in obese
patients after bariatric surgery has been confirmed by
Keywords different studies [10 .–13 .,14,15].
bariatric surgery, nutrient deficiency, obesity
Bariatric surgeries are divided into restrictive, restrictive/
Curr Opin Clin Nutr Metab Care 7:569–575. # 2004 Lippincott Williams & Wilkins. malabsorptive and malabsorptive procedures. Several
recent reviews about open and laparoscopic procedures
Biochemistry and Immunology Department, Institute of Biological Sciences and Alfa
Institute of Gastroenterology, Clinics Hospital, Medical School, Federal University of have been published [5,16 . .,17 .,18 . .,19 .,20 .,21 . .,22 .,
Minas Gerais, Brazil 23–26].
Correspondence to Jacqueline I. Alvarez-Leite, Laboratory of Nutritional Biochem-
istry, Department of Biochemistry and Immunology, ICB/UFMG, Caixa Postal 486 Purely restrictive procedures, including vertical banded
Belo Horizonte 30161-970, MG Brazil gastroplasties and silastic ring vertical gastroplasties, are
Tel: +55 31 34992652; fax: +55 31 34992614; e-mail: alvarez@[Link]
based on the reduction of gastric capacity, reducing food
Current Opinion in Clinical Nutrition and Metabolic Care 2004, 7:569–575 intake. The weight loss in these techniques is modest, in
Abbreviation general less than that established as the criterion of
RYGB Roux-en-Y gastric bypass success (excess-weight loss 450% sustained for at least 5
years after surgery) [18 . .].
# 2004 Lippincott Williams & Wilkins
1363-1950 The classical restrictive/malabsorptive surgery is the
Roux-en-Y gastric bypass (RYGB). In this procedure,
569
570 Nutrition and the gastrointestinal tract

gastric capacity is reduced by 90–95%. The biliopan- development, and compliance is essential to avoid
creatic limb includes stomach, duodenum, and part of adverse physical, cognitive, and psychosocial outcomes
jejunum and drains bile, digestive enzymes, and gastric following bariatric surgery.
secretions. The distal end of the jejunum is anastomosed
to the gastric pouch (Roux or alimentary limb) and Predicting and preventing nutritional
carries ingested food. The biliopancreatic limb is deficiencies after bariatric surgery
anastomosed generally 50–100 cm above the ileocecal Many obese subjects already have clinical or subclinical
valve, creating the common limb. As food and enzymes nutritional deficiencies before surgery, such as of vitamin
are only mixed in the small area of the common limb, the D, folate, and vitamin B12. For this reason, nutritional
digestion and absorption of most nutrients are compro- assessment, including serum levels of vitamins and
mised. The mean excess-weight loss (60–75%) depends minerals, should be evaluated before surgery to avoid,
on the length of the common limb [18 . .,23,26]. retard, or minimize the installation of nutritional
complications in the post-surgical period.
The first malabsorptive operation was the jejunoileal
bypass. Due to severe nutritional complications, this Conceptually, specific nutritional deficiencies are less
procedure is now discredited. Biliopancreatic diversion common in restrictive than in malabsorptive procedures
with or without duodenal switch replaced jejunoileal [37 . .,38 .]. However, poor eating behavior, food intoler-
bypass. Biliopancreatic diversion consists of a modest ance, and food restriction are frequently seen in patients
gastric restriction associated with a long biliopancreatic submitted to restrictive surgeries [39,40]. Consequently,
limb with the common limb of 50 cm. In biliopancreatic long-term follow up is also necessary to prevent or detect
diversion with duodenal switch, there is a smaller gastric potential nutritional deficiencies in these patients.
pouch with preservation of the pylorus and a small
portion of duodenum. As a consequence of these Malabsorptive procedures are more related to nutritional
malabsorptive procedures, an excess-weight loss of disorders. Generally, more aggressive procedures lead to
75–80% can be reached [18 . .,27]. a higher incidence of nutritional deficiencies [41,42 .].
Patients submitted to RYGB are at risk from developing
Especial attention should be given to adolescent and iron, vitamin B12, folate, and calcium deficiencies [42 .].
pregnant women submitted to bariatric surgery. Preg- In biliopancreatic diversion with duodenal switch,
nancy in women submitted to bariatric surgery could be protein and fat-soluble vitamin deficiencies are also seen
associated with nutritional deficiencies in both mother [43 . .]. The incidences of abnormal levels of serum
and child, due to the higher nutritional requirements. albumin, hemoglobin, and calcium 3 years after duode-
However, Marceau et al. [28 .] found a reduction of fetal nal switch are about 2, 48, and 29% respectively [44 . .].
macrosomia and normalization of the infant’s birth
weight in pregnant women previously submitted to Although nutritional problems are more prevalent in
biliopancreatic diversion. Despite favorable pregnancy biliopancreatic diversion than in RYGB [41], retro-
outcomes after bariatric surgery, careful studies are spective analysis comparing both procedures showed
required to evaluate nutritional status in both mother no differences in the occurrence of nutritional deficien-
and child after bariatric surgery in mothers. cies, except ferritin [45]. However, there was a high and
progressive incidence of nutritional disorders in both
A significant number of severely obese adolescents procedures when the pre- and post-surgical periods were
have now been submitted to bariatric surgery. In compared. Low levels of hemoglobin, iron, and ferritin
recent years, information about efficiency, risks, and were found in more than 44% of patients and vitamin
follow up of post-surgical adolescents has been B12 deficiency was found in about one-third of patients
published [29 . .,30 .–32 .,33,34 .,35 .,36]. Gastroplasty after 4 years of RYBG or biliopancreatic diversion. It has
used to be the first-choice technique, but it has been been estimated that after 1 year of biliopancreatic
replaced by gastric bypass. Different groups suggested diversion, one-third of the patients develop anemia
that RYGB is safe and effective, reducing complica- and/or fat-soluble vitamin deficiencies and less than 5%
tions and improving quality of life [29 . .,30 .,31 .]. are hospitalized for treatment of protein-calorie malnu-
However, long-term safety should be evaluated care- trition [23].
fully, since nutritional status has not been analyzed
carefully in many of these studies. Type and frequency Specific deficiencies
of nutritional complications are similar to those seen in The main nutrients affected by bariatric surgery are
adults, namely anemia, deficiencies of vitamins D and protein, vitamin B12 and folate, iron and calcium. For this
B, and folate, and protein-calorie malnutrition [36]. reason, a careful and regular check of these nutrients
However, as pointed out by Garcia et al. [32 .], should be also introduced once their deficiencies limit
application of the principles of adolescent growth, quality of life.
 Nutrient deficiencies secondary to bariatric surgery Alvarez-Leite 571

Protein-calorie deficiencies deficiency after vertical banded gastroplasty are about 46

The restriction of exogenous energy availability is the and 32% respectively [59]. The incidence of iron
goal of bariatric surgery. Energy deficits occur as a deficiency or anemia estimated by the American Society
consequence of low food intake, food intolerance of Bariatric Surgery surgeons is about 14–16% in RYBG
(mainly meat and dairy products), or nutrient malabsorp- and 21–26% after biliopancreatic diversion [41], lower
tion (mainly fat and protein). The ratio of fat-mass to fat- than the levels estimated in the literature. In superobese
free-mass loss is about 4:1 in restrictive techniques patients submitted to RYGB, iron deficiency occurred in
[37 . .,46 .,47 .]. 49–52% and anemia in 35–74% after 3 years, depending
on the Roux limb length [24]. Comparing patients
Protein deficiency is seen after RYGB [48 .] and, mainly, undergoing RYGB or biliopancreatic diversion, in a 5-
after biliopancreatic diversion [24,49]. The latter appears year follow up, incidence of iron deficiency was similar
to cause severe protein-calorie deficiencies in some after both operations [45].
studies [50,51] although low incidences have been
described by others [52,53]. The etiology of iron deficiency is multifactorial. In order
to be absorbed, dietary iron (as ferric ion) must be
Vitamin B12 and folate reduced to the ferrous state by the acid secretion of the
Vitamin B12 deficiency is common after gastric surgery, stomach. Since there is a reduced production of
mainly when restrictive procedures are involved. The hydrochloric acid after restrictive procedures, iron is less
deficiency is due to a failure of separation of vitamin B12 available to be absorbed. Moreover, with the exclusion
from protein foodstuffs and to a failure of absorption of of duodenum and proximal jejunum, the main areas of
crystalline vitamin B12, since intrinsic factor is not its absorption are bypassed.
present. Although the body storage of vitamin B12 is
substantial (about 2000 mg) compared to the small daily Iron deficiency and microcytic anemia are also very
needs (2 mg/day), the deficiency is relatively common in common in adolescents and women with active men-
patients after 1–9 years of gastric bypass. struation [29 . .,36]. Most multivitamin and mineral
supplements contain sufficient amounts of iron to
In patients after RYGB, the prevalence of B12 deficiency prevent deficiency. However, iron deficiency and anemia
is estimated in 12–33% [41]. However, clinical symptoms sometimes persist even in patients taking multivitamins.
are less common [45,54]. Currently the majority of In these cases an additional iron supplementation
patients undergoing RYGB are monitored and treated (300 mg of ferrous sulfate three times a day associated
with B12 once they have demonstrated low blood levels with ascorbic acid) should be prescribed to correct it.
of this vitamin. The use of 350 mg/day generally corrects
a low level of this vitamin [55,56,57 . .]. Only a small Thiamine
percentage of individuals will require parenteral admin- Thiamine is absorbed in the entire duodenum, mainly in
istration of B12 (2000 mg/month) [57 . .]. However, due to the acid milieu of the proximal duodenum. The
the frequent lack of symptoms, the need to follow or deficiency occurs through the combination of a reduction
treat low levels of B12 vitamin and folate (unless the in acid production by the gastric pouch, restriction of
patient has symptoms) has been questioned. This food intake, and frequent episodes of vomiting [60 .–
decision should be carefully analyzed, since there is 62 .,63–67,68 .,69,70]. Cases of clinical deficiency were
the risk of irreversible neurological damage if B12 published in the last decade, the majority associated with
deficiency is maintained for a long period. There is also persistent vomiting or hyperemesis [60 .,61 .,63–
a case reported of an exclusively breastfed infant with 67,68 .,69,71,72]. Due to the participation of thiamine
B12 deficiency, born of an asymptomatic mother that had in carbohydrate metabolism, high dietary intake of
undergone gastric bypass [58]. carbohydrate or administration of glucose could precipi-
tate clinical symptoms in patients with low reserves of
Folate deficiency is less common than B12 deficiency thiamine [61 .,63].
and occurs secondary to decreased dietary intake.
Although folate absorption occurs preferentially in the Chang et al. [73 .] found 40 cases of vitamin B and/or
proximal portion of the intestine, it can take place along thiamine deficiency in a total of 168 010 bariatric cases
the entire small bowel with adaptation after surgery. related by members of the American Society of Bariatric
Folate deficiency is preventable and promptly corrected Surgery. Compliance to multivitamin intake could
with multivitamin supplementation (1 mg/day). prevent thiamine deficiency in most of the cases. In
suspected deficiency, administration of 50–100 mg of
Iron thiamine should correct the deficiency. In patients with
Iron deficiency is one of the most frequent deficiencies hyperemesis, parenteral administration of thiamine 6
after bariatric surgery. The incidences of anemia or iron weeks after surgery should prevent the deficiency.
572 Nutrition and the gastrointestinal tract

Calcium, vitamin D, and bone metabolism Other fat-soluble vitamins and antioxidant status
Patients who have been submitted to restrictive or Fat malabsorption is common following RYGB and,
malabsorptive bariatric surgery are prone to bone mass mainly, biliopancreatic diversion where only about 32%
abnormalities [46 .,74 . .,75 .–77 .,78,79,80 .,81 .]. It is of the dietary fat is absorbed [84]. This occurs due to
caused by restriction of calcium intake associated with short common channels that lead to a delayed mixing of
malabsorption of both calcium and vitamin D. fat with pancreatic enzymes and bile salts. The
Reduced calcium absorption is secondary to the consequence is fat and fat-soluble vitamin malabsorp-
exclusion of duodenum and proximal jejunum, where tion. Moreover, food intolerance may reduce fat con-
calcium is maximally absorbed. Vitamin D is absorbed sumption and aggravate malabsorption.
preferentially in the jejunum and ileum. The defec-
tive absorption of fat and fat-soluble vitamins, Vitamin E deficiency is not common in patients
including vitamin D, aggravates calcium malabsorp- supplemented with multivitamin, although it was already
tion. The relative lack of calcium stimulates the reported after gastroplasty [85] and biliopancreatic
production of parathyroid hormone that, in turn, diversion [86 .]. An increase of serum a-tocopherol
causes increased production of 1,25-dihydroxyvitamin associated to low levels of lipid peroxidation was
D and increased release of calcium from bone. The described after vertical banded gastroplasty, suggesting
result of this process is the long-term risk of an improvement in antioxidant balance [87].
osteoporosis.
Clinical manifestation of vitamin A deficiency (night
Coates et al. [74 . .] studied bone metabolism in blindness) has already been reported [88,89 .,90], includ-
patients after laparoscopic RYGB. Bone-turnover mar- ing a report describing a newborn infant who developed
kers were significantly elevated, despite increased vitamin A deficiency as a result of maternal malabsorp-
dietary calcium and vitamin D intake and unchanged tion after biliopancreatic diversion [91].
levels of serum 25-hydroxyvitamin D and parathyroid
hormone. After 9 months of surgery, patients showed Up to now, clinical manifestations of vitamin K
bone mineral density reduced in the hip, trochanter, deficiency have not been published despite a report of
and total body. Slater et al. [43 . .] studied serum fat- high incidence of hypovitaminemia K after biliopancrea-
soluble vitamin and calcium metabolism in patients tic diversion [43 . .].
supplemented with calcium and vitamin D after
biliopancreatic diversion. They found abnormal levels Slater et al. [43 . .] examined the incidence of fat-soluble
of calcium and vitamin D in 57 and 63% of patients 1 vitamin deficiency following biliopancreatic diversion.
and 4 years after surgery respectively. Hypocalcaemia The incidence of vitamin A deficiency was 69%, vitamin
was also present in 15 and 48% of patients 1 and 4 K deficiency 68%, vitamin D deficiency 63%, and
years after biliopancreatic diversion. Secondary hyper- vitamin E deficiency 4% by the fourth year after surgery.
parathyroidism was present in 69% of patients after 4 Based on these results, it is recommended to check
years. Clinically significant hyperparathyroidism and serum fat-soluble vitamins before and regularly after
raised alkaline phosphatase were seen in 27 and 6% of biliopancreatic diversion.
these cases, respectively.
Zinc
On the other hand, Marceau et al. [82] reported only As a nutrient that depends on fat absorption, low serum
modest changes in bone mass in patients undergoing concentrations were observed in patients after biliopan-
biliopancreatic diversion 4–10 years after surgery. How- creatic diversion or duodenal switch [43 . .]. Low serum
ever, these patients were under close surveillance to levels of zinc were also described after gastroplasty as a
avoid metabolic complications and appropriated vitamin/ consequence of reduced dietary intake [85]. However,
mineral supplementation. clinical manifestations of zinc deficiency are not common
after bariatric surgery. There is one report of resolution
For these reasons calcium, phosphorus, alkaline phos- of alopecia after supplementation of high doses of zinc
phatase, parathyroid hormone, and 25-hydroxyvitamin sulfate in patients submitted to vertical gastroplasty [92].
D should be regularly monitored in patients submitted
to bariatric surgery. Besides high intake of calcium (2 g/ Conclusion
day) and vitamin D (400 i.u./day), calcium supplemen- Most publications about bariatric surgery state that the
tation (1.2–1.5 g/day) is also recommended [53,83]. analysis of excess-weight loss and improvement of
Calcium citrate rather than calcium carbonate is the metabolic complications are the major goals of this type
required form to be supplemented, since calcium from of surgery. However, as pointed out by Oria [93 .], the
carbonate is not bioavailable in the absence of stomach success of surgical treatment of morbid obesity needs to
acid. include not only weight loss and the improvement in
 Nutrient deficiencies secondary to bariatric surgery Alvarez-Leite 573

12 Ballantyne GH. Measuring outcomes following bariatric surgery: weight loss

obesity-related comorbidities, but also changes in quality . parameters, improvement in co-morbid conditions, change in quality of life
of life experienced by the patients after the operation. In and patient satisfaction. Obes Surg 2003; 13:954–964.
Good review of several parameters of success of bariatric surgery, including fat
addition, a careful and regular check of nutrients should mass loss, bariatric analysis reporting outcome system (BAROS) and IWQoL-Lite.
be also introduced once their deficiencies limit quality of
13 Sugerman HJ, Wolfe LG, Sica DA, Clore JN. Diabetes and hypertension in
life. As both success of surgery and incidence of . severe obesity and effects of gastric bypass-induced weight loss. Ann Surg
nutritional deficiencies are related to the magnitude of 2003; 237:751–756.
Good retrospective study analyzing the relationship between obesity, hypertension
weight loss, especial attention should be given to and diabetes and their relationship with gastric bypass-induced weight loss.
patients undergoing more aggressive malabsorptive 14 Wolf AM, Falcone AR, Kortner B, Kuhlmann HW. BAROS: an effective
procedures. Adolescents and women in reproductive system to evaluate the results of patients after bariatric surgery. Obes Surg
2000; 10:445–450.
age are the most vulnerable groups at risk of nutritional
deficiencies. To avoid severe nutritional deficiencies as 15 Victorzon M, Tolonen P. Bariatric Analysis and Reporting Outcome System
(BAROS) following laparoscopic adjustable gastric banding in Finland. Obes
seen in the first years after bariatric surgery it is Surg 2001; 11:740–743.
important to predict, prevent, and promptly treat 16 Steinbrook R. Surgery for severe obesity. N Engl J Med 2004; 350:1075–
..
nutritional abnormalities in vulnerable patients. 1079.
Good and critical review about the surgeons’ perspectives and surgery for obese
patients and the future of bariatric surgery in USA.
17 Podnos YD, Jimenez JC, Wilson SE, et al. Complications after laparoscopic
Acknowledgements . gastric bypass: a review of 3464 cases. Arch Surg 2003; 138:957–961.
The author wishes to acknowledge Dr Enio Cardillo Vieira for his help in An interesting review of studies cited in Medline comparing type and frequency of
the preparation of this review. complications after laparoscopic or open gastric banding.
18 Fobi MA. Surgical treatment of obesity: a review. J Natl Med Assoc 2004;
.. 96:61–75.
Good review about techniques and complications of bariatric surgery, including
References and recommended reading incidence and treatment of nutritional deficiencies.
Papers of particular interest, published within the annual period of review, have
been highlighted as: 19 Herron DM. The surgical management of severe obesity. Mt Sinai J Med
. 2004; 71:63–71.
. of special interest
.. of outstanding interest Review of types of bariatric surgery, early and late complications and
recommended supplementation of nutrients.

1 Jones KBJ. Bariatric surgery – where do we go from here? Int Surg 2004; 20 Mattison R, Jensen MD. Bariatric surgery. For the right patient, procedure
. . can be effective. Postgrad Med 2004; 115:49–50, 53–58.
89:51–57.
Shows a personal experience of RYGB in 2400 patients, including complication An objective discussion of bariatric surgery for those patients who have not
and weight loss. The author believes that open RYGB is the best choice for the responded to medically sound weight-loss programs.
majority of patients.
21 Ukleja A, Stone RL. Medical and gastroenterologic management of the post-
.. bariatric surgery patient. J Clin Gastroenterol 2004; 38:312–321.
2 Marcus JD, Elkins GR. Development of a model for a structured support
. group for patients following bariatric surgery. Obes Surg 2004; 14:103–106. Good overview of indications and complications of bariatric surgery, and, mainly,
Describes a model of structured support group before and after bariatric surgery. of clinical management of major nutritional deficiencies after different techniques of
The model of the group incorporates self-responsibility, and group therapy bariatric surgery.
processes.
22 Woodward BG. Bariatric surgery options. Crit Care Nurs Q 2003; 26:89–
3 Pinkney J, Kerrigan D. Current status of bariatric surgery in the treatment of . 100.
. type 2 diabetes. Obes Rev 2004; 5:69–78. The author discusses the concept of achieving malabsorption through manipula-
This is a good review about the impact of bariatric surgery on diabetes, raising the tion of the gastrointestinal contract and describes the techniques and complica-
question of whether it should be used more widely to treat diabetes in obese tions.
patients.
23 Brolin RE. Bariatric surgery and long-term control of morbid obesity. JAMA
4 Dixon JB, O’Brien PE. Lipid profile in the severely obese: changes with 2002; 288:2793–2796.
weight loss after lap-band surgery. Obes Res 2002; 10:903–910.
24 Brolin RE, LaMarca LB, Kenler HA, Cody RP. Malabsorptive gastric bypass
5 Dixon JB, O’Brien PE. Changes in comorbidities and improvements in quality in patients with superobesity. J Gastrointest Surg 2002; 6:195–203.
of life after LAP-BAND placement. Am J Surg 2002; 184:51S–54S.
25 Buchwald H. Overview of bariatric surgery. J Am Coll Surg 2002; 194:367–
6 Arribas del Amo D, Elia Guedea M, Aguilella Diago V, Martinez Diez M. Effect 375.
of vertical banded gastroplasty on hypertension, diabetes and dyslipidemia.
Obes Surg 2002; 12:319–323. 26 Capella JF, Capella RF. An assessment of vertical banded gastroplasty-
Roux-en-Y gastric bypass for the treatment of morbid obesity. Am J Surg
7 Brolin RE, Bradley LJ, Wilson AC, Cody RP. Lipid risk profile and weight
2002; 183:117–123.
stability after gastric restrictive operations for morbid obesity. J Gastrointest
Surg 2000; 4:464–469. 27 Van Hee R. Biliopancreatic diversion in the surgical treatment of morbid
8 Oria HE, Moorehead MK. Bariatric analysis and reporting outcome system obesity. World J Surg 2004; 28:435–444.
(BAROS). Obes Surg 1998; 8:487–499. 28 Marceau P, Kaufman D, Biron S, et al. Outcome of pregnancies after
. biliopancreatic diversion. Obes Surg 2004; 14:318–324.
9 Dymek MP, Le Grange D, Neven K, Alverdy J. Quality of life after gastric
bypass surgery: a cross-sectional study. Obes Res 2002; 10:1135–1142. A very interesting questionnaire-based study about preoperative and postoperative
pregnancy and neonatal outcomes in women undergoing biliopancreatic diversion.
10 Marinari GM, Murelli F, Camerini G, et al. A 15-year evaluation of The results showed that major weight loss following biliopancreatic diversion
. biliopancreatic diversion according to the bariatric analysis reporting outcome improves the reproductive function of obese women.
system (BAROS). Obes Surg 2004; 14:325–328.
An evaluation of bariatric analysis reporting outcome system (BAROS) score to 29 Inge TH, Garcia V, Daniels S, et al. A multidisciplinary approach to the
.. adolescent bariatric surgical patient. J Pediatr Surg 2004; 39:442–447.
biliopancreatic diversion, obtained by questionnaire sent to 1800 patients. A
BAROS score of very good and excellent was seen in more than 60%. A study of 79 obese adolescents undergoing RYGB, outlining the necessity of
multidisciplinary follow up.
11 Dittmar M, Heintz A, Hardt J, et al. Metabolic and psychosocial effects of
. minimal invasive gastric banding for morbid obesity. Metabolism 2003; 30 Sugerman HJ, Sugerman EL, DeMaria EJ, et al. Bariatric surgery for severely
52:1551–1557. . obese adolescents. J Gastrointest Surg 2003; 7:102–107.
This paper outlines the advantages of gastric banding that induce discrete weight Retrospective analysis of 32 adolescents undergoing bariatric operations. Good
loss, but improved atherogenic risks and quality of life. discussion about indications and results.
574 Nutrition and the gastrointestinal tract

31 Stanford A, Glascock JM, Eid GM, et al. Laparoscopic Roux-en-Y gastric 50 Sugerman HJ. Bariatric surgery for severe obesity. J Assoc Acad Minor Phys
. bypass in morbidly obese adolescents. J Pediatr Surg 2003; 38:430–433. 2001; 12:129–136.
Report of previous experience in four adolescent patients undergoing laparoscopic
gastric bypass, showing no complications and excellent weight loss. 51 Benedetti G, Mingrone G, Marcoccia S, et al. Body composition and energy
expenditure after weight loss following bariatric surgery. J Am Coll Nutr 2000;
32 Garcia VF, Langford L, Inge TH. Application of laparoscopy for bariatric 19:270–274.
. surgery in adolescents. Curr Opin Pediatr 2003; 15:248–255.
Good review of the indication of bariatric surgery in obese adolescents. Points out 52 Totte E, Hendrickx L, van Hee R. Biliopancreatic diversion for treatment of
the importance of multidisciplinary follow up. morbid obesity: experience in 180 consecutive cases. Obes Surg 1999;
9:161–165.
33 Dolan K, Creighton L, Hopkins G, Fielding G. Laparoscopic gastric banding
in morbidly obese adolescents. Obes Surg 2003; 13:101–104. 53 Scopinaro N, Adami GF, Marinari GM, et al. Biliopancreatic diversion. World
J Surg 1998; 22:936–946.
34 Capella JF, Capella RF. Bariatric surgery in adolescence. Is this the best age
. to operate? Obes Surg 2003; 13:826–832. 54 Sheu WH, Wu HS, Wang CW, et al. Elevated plasma homocysteine
Follow up of 10 years showing beneficial results after RYBG in obese concentrations six months after gastroplasty in morbidly obese subjects.
adolescents. No comments about specific nutritional deficiencies. Intern Med 2001; 40:584–588.
35 Abu-Abeid S, Gavert N, Klausner JM, Szold A. Bariatric surgery in 55 Rhode BM, Tamin H, Gilfix BM, et al. Treatment of vitamin B12 deficiency
. adolescence. J Pediatr Surg 2003; 38:1379–1382. after gastric surgery for severe obesity. Obes Surg 1995; 5:154–158.
A 23-month follow up of 11 adolescents who had undergone laparoscopic 56 Kushner R. Managing the obese patient after bariatric surgery: a case report
adjustable gastric banding, showing good weight loss without complications. of severe malnutrition and review of the literature. JPEN J Parenter Enteral
36 Strauss RS, Bradley LJ, Brolin RE. Gastric bypass surgery in adolescents Nutr 2000; 24:126–132.
with morbid obesity. J Pediatr 2001; 138:499–504.
57 Elliot K. Nutritional considerations after bariatric surgery. Crit Care Nurs Q
37 Giusti V, Suter M, Heraief E, et al. Effects of laparoscopic gastric banding on .. 2003; 26:133–138.
.. body composition, metabolic profile and nutritional status of obese women: An objective review that summarizes nutritional deficiencies after different types of
12-months follow-up. Obes Surg 2004; 14:239–345. surgery, as well as the critical care nutrition following bariatric surgery.
A 12-month follow up of 31 women who had undergone gastric banding. No major
58 Grange DK, Finlay JL. Nutritional vitamin B12 deficiency in a breastfed infant
nutritional deficiencies were found.
following maternal gastric bypass. Pediatr Hematol Oncol 1994; 11:311–
38 Chapman AE, Kiroff G, Game P, et al. Laparoscopic adjustable gastric 318.
. banding in the treatment of obesity: a systematic literature review. Surgery
2004; 135:326–351. 59 Kalfarentzos F, Kechagias I, Soulikia K, et al. Weight loss following vertical
Good review comparing the safety and efficacy of laparoscopic adjustable gastric banded gastroplasty: intermediate results of a prospective study. Obes Surg
banding with vertical banded gastroplasty and RYGB. They conclude that 2001; 11:265–270.
laparoscopic gastric banding is safer than vertical banded gastroplasty and 60 Loh Y, Watson WD, Verma A, et al. Acute Wernicke’s encephalopathy
RYGB. . following bariatric surgery: clinical course and MRI correlation. Obes Surg
39 Shai I, Henkin Y, Weitzman S, Levi I. Long-term dietary changes after vertical 2004; 14:129–132.
banded gastroplasty: is the trade-off favorable? Obes Surg 2002; 12:805– Case report of thiamine deficiency associated with alterations in magnetic
811. resonance imaging that were reversed after thiamine supplementation.

40 Kriwanek S, Blauensteiner W, Lebisch E, et al. Dietary changes after vertical 61 Sola E, Morillas C, Garzon S, et al. Rapid onset of Wernicke’s
. encephalopathy following gastric restrictive surgery. Obes Surg 2003;
banded gastroplasty. Obes Surg 2000; 10:37–40.
13:661–662.
41 Brolin RE, Leung M. Survey of vitamin and mineral supplementation after Case report of acute thiamine deficiency leading to Wernicke’s encephalopathy.
gastric bypass and biliopancreatic diversion for morbid obesity. Obes Surg
1999; 9:150–154. 62 Coskun H, Bozbora A, Ogunc G, Peker Y. Adjustable gastric banding in a
. multicenter study in Turkey. Obes Surg 2003; 13:294–296.
42 Marcason W. What are the dietary guidelines following bariatric surgery? J Shows Turkish experience with adjustable gastric banding, complications and
. Am Diet Assoc 2004; 104:487–488. safety.
Brief review of types of bariatric surgery and nutritional guidelines after surgery.
63 Chaves LC, Faintuch J, Kahwage S, Alencar Fde A. A cluster of
43 Slater GH, Ren CJ, Siegel N, et al. Serum fat-soluble vitamin deficiency and polyneuropathy and Wernicke-Korsakoff syndrome in a bariatric unit. Obes
.. abnormal calcium metabolism after malabsorptive bariatric surgery. J Surg 2002; 12:328–334.
Gastrointest Surg 2004; 8:48–55.
Good prospective study showing high incidence of deficiency of A, D and K 64 Toth C, Voll C. Wernicke’s encephalopathy following gastroplasty for morbid
vitamins after biliopancreatic diversion with duodenal switch. The authors suggest obesity. Can J Neurol Sci 2001; 28:89–92.
that these vitamins should be monitored regularly after surgery to prevent
65 Cirignotta F, Manconi M, Mondini S, et al. Wernicke-korsakoff encephalo-
complications.
pathy and polyneuropathy after gastroplasty for morbid obesity: report of a
44 Anthone GJ, Lord RV, DeMeester TR, Crookes PF. The duodenal switch case. Arch Neurol 2000; 57:1356–1359.
.. operation for the treatment of morbid obesity. Ann Surg 2003; 238:618–627.
66 Bozbora A, Coskun H, Ozarmagan S, et al. A rare complication of adjustable
Examines 701 cases of duodenal switch, showing it is safe and effective. After 3-
gastric banding: Wernicke’s encephalopathy. Obes Surg 2000; 10:274–275.
year follow up, serum albumin remained at normal levels in 98% of patients,
hemoglobin in 52%, and calcium in 71%. 67 Salas-Salvado J, Garcia-Lorda P, Cuatrecasas G, et al. Wernicke’s
45 Skroubis G, Sakellaropoulos G, Pouggouras K, et al. Comparison of syndrome after bariatric surgery. Clin Nutr 2000; 19:371–373.
nutritional deficiencies after Roux-en-Y gastric bypass and after biliopancrea- 68 Houdent C, Verger N, Courtois H, et al. Wernicke’s encephalopathy after
tic diversion with Roux-en-Y gastric bypass. Obes Surg 2002; 12:551–558. . vertical banded gastroplasty for morbid obesity. Rev Med Interne 2003;
46 Strauss BJ, Marks SJ, Growcott JP, Stroud DB, Lo CS, Dixon JB, et al. Body 24:476–477.
. composition changes following laparoscopic gastric banding for morbid Report of two cases of Wernicke’s encephalopathy after restrictive procedure.
obesity. Acta Diabetol 2003; 40 (Suppl 1):S266–S269. 69 Christodoulakis M, Maris T, Plaitakis A, Melissas J. Wernicke’s encephalo-
Adjustable laparoscopic gastric banding induces fat loss without deleterious pathy after vertical banded gastroplasty for morbid obesity. Eur J Surg 1997;
effects on body composition. 163:473–474.
47 Moize V, Geliebter A, Gluck ME, et al. Obese patients have inadequate 70 Mason EE. Starvation injury after gastric reduction for obesity. World J Surg
. protein intake related to protein intolerance up to 1 year following Roux-en-Y 1998; 22:1002–1007.
gastric bypass. Obes Surg 2003; 13:23–28.
Postoperative patients consume insufficient amounts of protein due to protein 71 Koike H, Misu K, Hattori N, et al. Postgastrectomy polyneuropathy with
intolerance. thiamine deficiency. J Neurol Neurosurg Psychiatry 2001; 71:357–362.
48 Faintuch J, Matsuda M, Cruz ME, et al. Severe protein-calorie malnutrition 72 Seehra H, MacDermott N, Lascelles RG, Taylor TV. Wernicke’s encephalo-
. after bariatric procedures. Obes Surg 2004; 14:175–181. pathy after vertical banded gastroplasty for morbid obesity. BMJ 1996;
The authors describe severe malnutrition in 4.7% of patient submitted to RYGB 312:434.
and discuss the exogenous precipitating factors.
73 Chang CG, Adams-Huet B, Provost DA. Acute post-gastric reduction
49 Sugerman HF, Kellum JF, DeMaria E. Conversion of proximal to distal gastric . surgery (APGARS) neuropathy. Obes Surg 2004; 14:182–189.
bypass for failed gastric bypass for superobesity. J Gastrointest Surg 1997; Questionnaire-based study showing a low incidence of polineuropathy secondary
1:517–525. to thiamine deficiency after bariatric surgery.
 Nutrient deficiencies secondary to bariatric surgery Alvarez-Leite 575

74 Coates PS, Fernstrom JD, Fernstrom MH, et al. Gastric bypass surgery for 82 Marceau P, Biron S, Lebel S, et al. Does bone change after biliopancreatic
.. morbid obesity leads to an increase in bone turnover and a decrease in bone diversion? J Gastrointest Surg 2002; 6:690–698.
mass. J Clin Endocrinol Metab 2004; 89:1061–1065.
83 Kellum JM, DeMaria EJ, Sugerman HJ. The surgical treatment of morbid
A comparative and prospective study of post-surgical obese patients, showing an
obesity. Curr Probl Surg 1998; 35:791–858.
increase in bone resorption associated with a decrease in bone mass within 3–9
months after RYGB. 84 Scopinaro N, Marinari GM, Pretolesi F, et al. Energy and nitrogen absorption
after biliopancreatic diversion. Obes Surg 2000; 10:436–441.
75 Bell NH. Bone loss and gastric bypass surgery for morbid obesity. J Clin
. Endocrinol Metab 2004; 89:1059–1060. 85 Trostler N, Mann A, Zilberbush N, et al. Nutrient intake following vertical
Shows reduction of bone mass after gastric bypass. banded gastroplasty or gastric bypass. Obes Surg 1995; 5:403–410.

76 Pugnale N, Giusti V, Suter M, et al. Bone metabolism and risk of secondary 86 Vazquez C, Morejon E, Munoz C, et al. Nutritional effect of bariatric surgery
. . with Scopinaro operation. Analysis of 40 cases. Nutr Hosp 2003; 18:189–
hyperparathyroidism 12 months after gastric banding in obese pre-
menopausal women. Int J Obes Relat Metab Disord 2003; 27:110–116. 193.
Study showing that there is a negative remodeling balance without secondary This review shows an improvement in metabolic parameters after surgery, but with
hyperparathyroidism 1 year after gastric banding. high prevalence of nutrient deficiency.

77 Guney E, Kisakol G, Ozgen G, et al. Effect of weight loss on bone 87 Kisakol G, Guney E, Bayraktar F, et al. Effect of surgical weight loss on free
. metabolism: comparison of vertical banded gastroplasty and medical radical and antioxidant balance: a preliminary report. Obes Surg 2002;
intervention. Obes Surg 2003; 13:383–388. 12:795–801.
This study shows that bone loss was related to weight loss, but independent of the 88 Spits Y, De Laey JJ, Leroy BP. Rapid recovery of night blindness due to
method of weight reduction (clinical or surgical). obesity surgery after vitamin A repletion therapy. Br J Ophthalmol 2004;
88:583–585.
78 Goldner WS, O’Dorisio TM, Dillon JS, Mason EE. Severe metabolic bone
disease as a long-term complication of obesity surgery. Obes Surg 2002; 89 Hatizifotis M, Dolan K, Newbury L, Fielding G. Symptomatic vitamin A
12:685–692. . deficiency following biliopancreatic diversion. Obes Surg 2003; 13:655–657.
Case reporting symptomatic vitamin A deficiency secondary to biliopancreatic
79 Cundy T, Evans MC, Kay RG, et al. Effects of vertical-banded gastroplasty diversion associated with deficiencies of vitamins D, E and K, and zinc and
on bone and mineral metabolism in obese patients. Br J Surg 1996; selenium.
83:1468–1472.
90 Quaranta L, Nascimbeni G, Semeraro F, Quaranta CA. Severe corneocon-
80 Hamoui N, Kim K, Anthone G, Crookes PF. The significance of elevated junctival xerosis after biliopancreatic bypass for obesity (Scopinaro’s
. levels of parathyroid hormone in patients with morbid obesity before and after operation). Am J Ophthalmol 1994; 118:817–818.
bariatric surgery. Arch Surg 2003; 138:891–897.
A retrospective analysis of 165 patients after duodenal switch with different 91 Huerta S, Rogers LM, Li Z, et al. Vitamin A deficiency in a newborn resulting
channel lengths. They concluded that patients with shorter common channels had from maternal hypovitaminosis A after biliopancreatic diversion for the
a higher risk of developing hyperparathyroidism. treatment of morbid obesity. Am J Clin Nutr 2002; 76:426–429.
92 Neve HJ, Bhatti WA, Soulsby C, et al. Reversal of hair loss following vertical
81 Hamoui N, Anthone G, Crookes PF. Calcium metabolism in the morbidly
. gastroplasty when treated with zinc sulphate. Obes Surg 1996; 6:63–65.
obese. Obes Surg 2004; 14:9–12.
This paper studies obese patients before surgery. It shows that parathyroid 93 Oria HE. Outcomes evaluation after bariatric surgery. J Am Coll Surg 2004;
hormone is increased in the morbidly obese and is positively correlated with body . 198:500–501.
mass index. Good comment about bariatric surgery.