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ORIGINAL CONTRIBUTIONS
High Frequency of Serum Chromium Deficiency and Association
of Chromium with Triglyceride and Cholesterol Concentrations
in Patients Awaiting Bariatric Surgery
Karla V. G. Lima &Raquel P. A. Lima &Maria C. R. Gonçalves &
Joel Faintuch &Liana C. S. L. Morais &
Luiza S. R. Asciutti &Maria J. C. Costa
Published online: 20 November 2013
#Springer Science+Business Media New York 2013
Abstract
Background To our knowledge, the frequency of serum chro-
mium deficiency in patients awaiting bariatric surgery has not
been determined. This study was designed to assess chromium
concentration and its association with glycemic levels and
lipid profile in patients prior to bariatric surgery.
Methods This study recruited 73 candidates for bariatric sur-
gery between March and September 2012. Their
sociodemographic, anthropometric, and biochemical data
were collected.
Results Of the 73 patients, 55 (75.3 %) were women
(75.34 %). Mean patient age was 37.20± 9.92 years, and
mean body mass index was 47.48 kg/m
2
(range, 43.59 to
52.50 kg/m
2
). Chromium deficiency was observed in 64
patients (87.7 %). Correlation analysis showed significant
negative relationships between chromium concentration
and BMI and zinc concentration and a significant positive
relationship between chromium and glycated hemoglobin.
Multiple linear regression analysis showed that serum
chromium concentration was significantly associated
with total cholesterol (β=0.171, p=0.048) and triglycer-
ide (β=−0.181, p=0.039) concentrations.
Conclusions Serum chromium deficiency is frequent in can-
didates for bariatric surgery and is associated with total cho-
lesterol and triglyceride concentrations. Early nutritional in-
terventions are needed to reduce nutritional deficiencies and
improve the lipid profile of these patients.
Keywords Chromium .Cholesterol .Triglycerides .Bariatric
surgery .Preoperative
Introduction
Bariatric surgery is currently the most effective treatment
modality and the treatment of choice for patients with morbid
obesity. Its benefits include weight loss and long-term main-
tenance of lower weight, improvement or control of diseases
associated with obesity [1], and improvements in quality of
life [2].
Prior to surgery, many obese patients have micronutrient
deficiencies [3–5], including clinical or sub-clinical deficien-
cies in vitamin B12, vitamin D, iron, and zinc. These findings
indicated that postoperative deficiencies are not due exclu-
sively to reduced ingestion or that absorption of these nutri-
ents in the gastrointestinal tract [6] became questionable since
micronutrient deficiencies can also be found preoperatively.
K. V. G. Lima (*)
Graduate Program in Nutritional Sciences, Health Sciences Center,
NIESN—Interdisciplinary Center for Studies in Health and
Nutrition, Federal University of Paraíba, Castelo Branco,
João Pessoa, PB 58059-900, Brazil
e-mail: karlla_gomes@hotmail.com
R. P. A. Lima :M. C. R. Gonçalves :L. C. S. L. Morais :
M. J. C. Costa
Graduate Program in Nutritional Sciences, Department of Nutrition,
Center for Health Sciences, NIESN—Interdisciplinary Center for
Studies in Health and Nutrition, Federal University of Paraíba,
Castelo Branco, João Pessoa, PB 58059-900, Brazil
L. S. R. Asciutti
Undergraduate Program in Nutrition, Faculty of Medical Sciences,
NIESN—Interdisciplinary Center for Studies in Nutrition and
Health, Federal University of Paraíba, João Pessoa,
PB 58010-740, Brazil
J. Faintuch
Graduate Department of Gastroenterology, Faculty of Medicine,
University of São Paulo, Cerqueira César, São Paulo,
SP 05403-900, Brazil
OBES SURG (2014) 24:771–776
DOI 10.1007/s11695-013-1132-7
It is important to determine the frequency of chromium
deficiency in patients undergoing bariatric surgery since appro-
priate intervention measures are needed during follow-up to
improve their clinical profiles and achieve better perioperative
responses. To our knowledge, however, the frequency of serum
chromium deficiency in patients awaiting bariatric surgery has
not been determined despite chromium being an essential
element necessary for insulin function, glucose availability,
and maintenance of lipid metabolism [7]. Moreover, chromium
concentration may be associated with weight loss in these
patients since chromium activation of insulin-sensitive
glycoreceptors in the brain may suppress appetite and stimulate
thermogenesis [8]. This study was therefore designed to mea-
sure serum chromium concentrations in obese patients selected
for bariatric surgery and to assess the associations between
chromium and glycemic control markers and lipid profiles.
Methods
This study recruited obese individuals selected for bariatric
surgery according to the criteria established by the
International Federation for Obesity Surgery and the Brazilian
Society for Bariatric Surgery [9] at Santa Isabel Municipal
Hospital in João Pessoa, Paraiba, Brazil, from March to
September 2012. To calculate sample size, the prevalence of
obesity in Brazil (34.3 %) was used as a reference [10], along
with a sampling error of 10 % and a confidence level of 95 %.
We calculated that 66 patients were needed; to allow for a 10 %
dropout rate, 73 participants were recruited. The study protocol
was approved by the Ethics Research Committee, Center of
Health Sciences, Federal University of Paraíba, under protocol
no. 0294/2011, and all participants provided written informed
consent. This observational cross-sectional study included in-
dividuals of both sexes, irrespective of race, age of 18 to
59 years, and a BMI >35 kg/m
2
plus comorbidities (diabetes,
hypertension, sleep apnea, arthropathy, and/or disc herniation)
or ≥40 kg/m
2
without comorbidities. Patients were included if
they were not taking vitamin–mineral supplements containing
chromium, had not previously undergone bariatric or gastroin-
testinal tract surgery, were not pregnant or lactating, and did not
have type 1 diabetes, intestinal disorders, cancer, or organic
disorders of, e.g., the kidneys, liver, and heart, and had been
morbidly obese for more than 3 years.
Participants were interviewed to assess their demograph-
ic characteristics (e.g., age, sex, and level of education),
lifestyle (duration of obesity, use of alcohol, smoking, use
of multivitamins, and physical activity), and medication use
(dose and duration of each agent). The presence of comor-
bidities (hypertension, diabetes, and dyslipidemia) was de-
termined by review of their medical records. Weight and
height were measured in each patient, with BMI subse-
quently calculated.
Preoperative blood samples were collected and analyzed at
the clinical laboratory of the Santa Isabel Municipal Hospital.
Serum concentrations of fasting glucose, glycated hemoglo-
bin, total cholesterol and its fractions (high-density lipoprotein
[HDL] and low-density lipoprotein [LDL]), and triglycerides
were measured, with the limits adopted based on serum con-
centrations in healthy adults [11](Table1).
Chromium concentrations were determined using blood sam-
ples (5 mL) collected after an 8-h fasting period; these samples
were forwarded to the Laboratory of Clinical Pathology and
Hematology, João Pessoa, Paraíba, Brazil, which analyzed nu-
trients according to international standards. Serum concentra-
tions of chromium were measured using an atomic absorption
spectrophotometry method (Zeeman Graphite Furnace), with
reference values ranging from 0.7 to 2.2 mcg/L [12].
Statistical analyses and hypothesis tests were performed
using Sigma Stat 3.5 statistical software. Parametric data
were reported as mean ± standard deviation and non-
parametric data as median with 25th and 75th percentiles.
Hypothesis tests were defined according to normality re-
sults using the Kolmogorov–Smirnov test, followed by
t-tests for parametric and Mann–Whitney U-tests for non-
parametric results. Correlations were assessed using the
Spearman correlation test.
Multiple linear regression analysis was performed to
evaluate the relationships between chromium concentration
(response variable) and demographic, anthropometric, and
biochemical variables (regressive variables). The proposed
model could be expressed as: [chromium=1.073+
(0.0690, sex)−(0.0373, age)+(0.0328, BMI)−(0.0812,
fasting glucose)+(0.171, total cholesterol) −(0.181, tri-
glycerides)−(0.0653, schooling)]. Statistical significance
was defined as a pvalue≤0.05.
Results
Of the 73 patients, 55 (75.3 %) were female and 18 (24.7 %)
were male. Their mean age was 37.20±9.92 years, their mean
BMI was 47.48 kg/m
2
(range 43.59 to 52.50) kg/m
2
, and their
mean duration of obesity was 15.89±7.15 years.
Table 1 Reference values employed in biochemical evaluation
Parameters Methodology Reference
value
Fasting glucose Enzymatic method—hexokinase 70–110 mg/dL
Glycated hemoglobin Chromatography automated <7 %
Total cholesterol Enzymatic colorimetric method <200 mg/dL
HDL-cholesterol ≥60 mg/dL
LDL-cholesterol < 100 mg/dL
Triglycerides < 150 mg/dL
772 OBES SURG (2014) 24:771–776
In assessing lifestyle factors, we found that 56 patients
(76.7 %) were sedentary, 36 (49.3 %) were hypertensive, 22
(30.1 %) were alcoholics, 28 (38.4 %) had hypercholesterol-
emia, and 36 (49.3 %) had hypertriglyceridemia, but only six
(8.2 %) were smokers.
All nine diabetic individuals (12.3 %) were being treated with
oral hypoglycemic agents, and 33 of the 36 (91.7 %) hyperten-
sive patients were being treated with antihypertensive agents. In
contrast, only 3 % of the patients with hypercholesterolemia
and/or hypertriglyceridemia were being treated with lipid-
lowering agents. The median number of drugs taken daily by
these patients was 1 (maximum, 5), with antihypertensive drugs
being the most frequent. The mean medication intake time was
36 months (range 12–72 months), with a maximum of
144 months. Only three patients (4.1 %) were taking vitamin
supplements, including vitamin D alone and multivitamins con-
taining vitamin B12, iron, and folic acid.
When we assessed the serum concentrations of chromium
in these 73 patients, we observed lower than normal concen-
trations in 64 (87.7 %) compared with reference values, al-
though most parameters did not differ significantly in men and
women (Table 2).
Correlation analysis showed that as chromium concentra-
tions increased, zinc concentrations and BMI (R=−0.02) de-
creased and glycated hemoglobin concentrations (R=0.27)
increased (Table 3). In analyzing the influence of one variable
on another by calculating determination coefficients (R
2
), we
found that 4.84 % of the BMI variability and 7.29 % of the
glycated hemoglobin variability could be attributed to chro-
mium concentrations.
Multiple linear regression analysis showed that chromium
concentration was significantly and independently associated
with total cholesterol (β=0.171, p=0.048) and triglyceride
(β=−0.181, p=0.039) concentrations (Table 4).
Discussion
The relative lack of information about the prevalence of
chromium deficiency in the general population [13,14]and
absence of patients in preoperative bariatric surgery and in
patients with morbid obesity (BMI≥40 kg/m
2
) reinforce the
need to evaluate this mineral. The present study found that a
high percentage (87.67 %) of individuals awaiting bariatric
surgery had serum chromium concentrations below reference
values (0.7 to 2.2 mcg/L), with mean of 0.2±0.2 mcg/L in
men and 0.3±0.2 mcg/L in women. Similarly, mean serum
chromium concentrations were shown to be below reference
values in men (0.14± 0.01 mcg/L) and women (0.15±
0.01 mcg/L) with moderate central obesity, but that study
did not report the percentages of individuals with chromium
deficiency [15]. Concentrations of chromium were also found
to be lower than reference values in groups of young diabetic
patients and aged-matched controls, with mean concentrations
lower in the diabetic group and mean concentrations in the
control group similar to those observed in this study [16].
Other studies have also reported differences in serum chromi-
um concentrations between healthy subjects and diabetic pa-
tients [17–19].
Serum chromium deficiency may be associated with con-
temporary diets, which are poor in this essential trace element
owing to soil depletion, refined foods, excessive sugar con-
sumption, lack of exercise, and obesity [20]. Chromium defi-
ciencies in diabetic patients may also be related to alterations
Table 2 Body mass and bio-
chemical variables in men and
women prior to bariatric surgery
Data presented as mean ± stan-
dard deviation or median with
25th and 75th percentiles
(in brackets). Non-parametric da-
ta were compared using the
Mann–Whitney U-test (+) and
parametric data using
Student's t-test
BMI body mass index
*p≤0.05
Parameters Men (n=18) Women (n=55) P
Age [years]
+
33.1±9.2 38.5 ±9.8 0.080
34.0 (24.0–40.0) 37.0 (31.2–46.75)
IMC [Kg/m
2
]
+
50.1±9.3 49.95±9.0 0.964
48.5 (42.9–52.2) 47.4 (43.7–53.1)
Fasting glucose [mg/dL]
+
101.1±12.7 102.6±38.5 0.062
100.5 (95.0–110.0) 93.0 (86.0–99.7)
Glycated hemoglobin [%]
+
6.4± 2.5 6.2± 2.7 0.446
5.6 (4.9–6.2) 5.4 (4.6–6.9)
Total cholesterol [mg/L]
+
200.9±40.2 184.6±36.2 0.179
194.0 (172.0–225.0) 176.0 (155.0–214.0)
LDL-cholesterol [mg/L] 124.8±29.2 111.4± 30.3 0.105
128.5 (105.0–150.0) 106.0 (90.7–128.5)
HDL-cholesterol [mg/L] 37.7±11.9 40.5±7.3 0.232
36.0 (30.0–42.0) 40.0 (35.0–45.0)
Triglycerides [mg/L]
+
201.1±9.0 162.6±81.4 0.085
176.5 (128.0–297.0) 137.0 (101.5–206.0)
Chromium [mcg/L]
+
0.2± 0.2 0.3± 0.2 0.779
0.1 (0.1–0.3) 0.2 (0.1–0.3)
OBES SURG (2014) 24:771–776 773
in chromium metabolism, including increased loss and de-
creased absorption [21]. Chromium metabolism is also im-
paired following bariatric surgery since deficiencies in this
element may worsen owing to vomiting, decreased food in-
take, food intolerance, and removal of absorption areas [22].
Chromium is an essential mineral required for glucose
metabolism since it increases the activity of insulin [23]. The
mechanism proposed for chromium action is that the mineral
increases the cell membrane fluidity to facilitate binding of
insulin to its receptor [24]. Chromium has also been charac-
terized as a component that participates in the mechanism that
enhances cell signaling of insulin or a contributing factor in
the increased sensitivity of insulin receptors on the plasma
membrane [25]. Thus, chromium concentrations have been
analyzed in individuals with insulin resistance and/or diabetes.
Chromium supplementation in patients with diabetes has been
found to alter glycemic control (e.g., fasting glucose, insulin,
and glycated hemoglobin concentrations) and lipid profiles
[26–29]. However, individuals with normal chromium con-
centrations do not require supplementation [30], perhaps
explaining the lack of effects of other studies of chromium
supplementation, e.g., in diabetic subjects [31], adults and
elderly with metabolic syndrome [32,33], and adults at high
risk of type 2 diabetes [34].
Similarly to our findings, a previous study observed an
inverse relationship between serum chromium concentration
and BMI in that chromium concentrations were lower in
subjects with moderate central obesity, although that popula-
tion did not meet the criteria for bariatric surgery [15]. Similar
results were observed in a study of chromium status and
glucose intolerance in Saudi men with coronary artery disease,
which found that serum chromium concentrations were higher
in individuals with lower BMI [35].
The inverse relationship between serum chromium levels
and weight suggests that chromium supplementation may
result in weight loss owing to a decrease in insulin resistance.
Chromium may result in greater weight loss when the excess
weight is centrally distributed and therefore more associated
with insulin resistance [33]. Chromium-induced weight loss
may also be due to appetite suppression and stimulation of
thermogenesis [8].
We observed a positive relationship between serum chro-
mium and glycated hemoglobin (HbA1c) concentrations.
Similarly, poorer metabolic control, as measured by increased
HbA1c, was found to result in higher plasma chromium
concentrations [36]. Our finding of a lack of relationship
between serum chromium and fasting glucose concentrations
was also described in a previous meta-analysis [31].
Univariate analyses showed that serum chromium concen-
trations were correlated with BMI, glycated hemoglobin, and
dietary zinc; however, multivariate linear regression analysis
showed that serum chromium levels were positively associat-
ed with total cholesterol and negatively associated with tri-
glyceride concentrations. The relationship between chromium
and triglycerides has been observed previously [15].
Several hypotheses may explain the eff.ect of chromium on
lipid metabolism [37]; for example, the increase in cholesterol
levels observed in subjects with elevated serum chromium
may be due to increased concentrations of secondary serum
lipids resulting from increased insulin action or the direct
effect of chromium on the expression of the binding protein
to the sterol regulatory element (SERBP-1), which regulates
cholesterol synthesis [38].
Mechanisms related to the negative relationship between
chromium and triglycerides may include the ability of chro-
mium to enhance insulin sensitivity, reducing the hydrolysis
of triglycerides in adipocytes and lowering the levels of non-
Table 3 Correlation between serum chromium concentrations and BMI,
lipid profile and glycemic control indicators in patients awaiting bariatric
surgery
Parameters Chromium
Rp
Schooling −0.15 0.21
BMI (kg/m
2
)−0.22 0.05*
Total cholesterol (mg/L) −0.07 0.58
LDL-cholesterol (mg/L) −0.01 0.93
HDL-cholesterol (mg/L) 0.11 0.37
Triglycerides (mg/L) −0.05 0.63
Fasting glucose (mg/dL) 0.02 0.84
Glycated hemoglobin (%) 0.27 0.02*
Correlation tested based on Spearman test
BMI body mass index
*p≤0.05
Table 4 Multiple linear regression model of serum chromium and de-
mographic, anthropometric, and biochemical variables
Va r i ab l e s C h r om i u m
Regression coefficient P
Sex 0.07 0.462
Age −0.04 0.376
Schooling 0.06 0.223
BMI 0.03 0.706
Fasting glucose −0.08 0.405
Total cholesterol 0.17 0.048*
Triglycerides −0.18 0.039*
R
2
adjusted 0.139
p(model) 0.0458
BMI body mass index
*p≤0.05
774 OBES SURG (2014) 24:771–776
esterified fatty acids in serum. In addition, the decreased flow
of non-esterified fatty acids to the liver limits the production of
triglycerides and very low-density lipoprotein [37,39].
Limitations of this study include sample size and gender
homogeneity, with a much higher percentage of women than
men in the study group. This distribution, however, is typical
of patients seeking bariatric surgery [40,41]. Moreover, we
did not assess chromium intake by this population either using
appropriate software or a table of food composition.
Additional studies are needed, including a control group with
adequate BMI and normal waist circumference, to determine
if chromium deficiency and its associations are restricted to
obese bariatric surgery candidates or are common to the
general population.
Conclusion
Chromium deficiency is common in candidates for bariatric
surgery. Serum chromium concentrations are positively cor-
related with cholesterol and negatively correlated with triglyc-
eride concentrations. Due to the importance of chromium in
various physiological processes, additional studies on chro-
mium deficiency and the relationship between chromium and
cholesterol and triglyceride concentrations in patients
awaiting bariatric surgery are needed to establish safe limits
for dietary chromium intake, both to treat this deficiency and
to balance lipid profiles before surgery.
The importance of the results of this study related to the
high frequency of serum chromium deficiency interfering
with lipid metabolism ensures the recommendation of
assessing the chromium, cholesterol, and triglyceride levels
pre-operatively of patient candidates for bariatric surgery. This
assessment is particularly useful to adjust the low serum
chromium levels, observing whether the triglyceride and cho-
lesterol values also normalize. Further studies should be car-
ried out to find the best way for preventing chromium defi-
ciency from supplements or balanced diet in candidates for
bariatric surgery.
Conflict of Interest The authors have no conflict of interest.
References
1. Khavandi K, Brownirgg J, Hankir M, Sood H, Younis N, Worth J,
Greenstein A, Soran H, Wierzbicki A, Goldsmith DJ. Interrupting the
natural history of diabetes mellitus: lifestyle, pharmacological and
surgical strategies targeting disease progression. Curr Vasc
Pharmacol. 2012.
2. Chopra A, Chao E, Etkin Y, et al. Laparoscopic sleeve gastrectomy
for obesity: can it be considered a definitive procedure? Surg Endosc.
2012;26(3):831–7.
3. Schilling PL, Davis MM, Albanese CT, et al. National trends in
adolescent bariatric surgical procedures and implications for surgical
centers of excellence. J Am Coll Surg. 2008;206:1–12.
4. Nicoletti CF, Lima TP, Donadelli SP, Salgado WJR, Marchini JS,
Nonino CB. New look at nutritional care for obese patient candidates
for bariatric surgery. Surg Obes Relat Dis. 2013;9(2):323–7.
5. de Luis DA, Pacheco D, Izaola O, Terroba MC, Cuellar L, Cabezas
G. Micronutrient status in morbidly obese women before bariatric
surgery. Surg Obes Relat Dis. 2013;9(4):520–5.
6. Toh SY, Zarshenas N, JorgensenJ.Prevalenceofnutrient deficiencies
in bariatric patients. Nutrition. 2009;25(11–12):1150–6.
7. Vincent JB. Chromium: celebrating 50 years as an essential element?
Dalton Trans. 2010;39:3787–94.
8. Wang ZQ, Qin J, Martin J, et al. Phenotype of subjects with type 2
diabetes mellitus may determine clinical response to chromium sup-
plementation. Metabolism. 2007;56:1652–5.
9. CFM - Conselho Federal de Medicina. Resolução no. 1.766/05.
Publicada no D.O.U., 11 Jul 2005, Seção I, p.114.
10. Sociedade Brasileira de Cirurgia Bariátrica e Metabólica. Obesidade
sem marcas: cirurgia menos invasiva é um direito (Press Kit). São
Paulo: Sociedade Brasileira de Cirurgia Bariátrica e Metabólica,
2010. Disponível em: <http://www.sbcbm.org.br/imagens/PressKit_
SBCBM.pdf >. Acessado em: 04 out. 2012.
11. Kratz A, Pesce MA, Fink DJ. Appendix: laboratory values of clinical
importance. In: FAUCI AS, BRAUNWALD E, KASPER DL,
HAUSER SL, LONGO DL, JAMESON JL, LOSCALZO J.
Harrison's principles of internal medicine, ed.17, 2008. Disponível
em: http://www.accessmedicine.com/content.aspx?aID=2904600.
Acessado: 15 de dez. 2012.
12. Brune D, Aitio A, Nordberg G, et al. Normal concentrations of
chromium in serum and urine—a TRACY project. Scand J Work
Environ Health. 1993;19 Suppl 1:39–44.
13. Cefalu WT, Hu FB. Role of chromium in human health and in
diabetes. Diabetes Care. 2004;27:2742–51.
14. Kaidar-Person O, Person B, Szomstein S, et al. Nutritional deficien-
cies in morbidly obese patients: a new form of malnutrition? Part B:
minerals. Obes Surg. 2008;18:1028–34.
15. Wysocka E, Cymerys M, Mielcarz G, et al. The way of serum
chromium utilization may contribute to cardiovascular risk factors
in centrally obese persons. Arch Med Sci. 2011;7(2):257–63.
16. Basaki M, Saeb M, Nazifi S, et al. Zinc, copper, iron, and chromium
concentrations in young patients with type 2 diabetes mellitus. Biol
Trace Elem Res. 2012;148:161–4.
17. Kazi TG, Afridi HI, Kazi N, et al. Copper, chromium, manganese,
iron, nickel, and zinc levels in biological samples of diabetes mellitus
patients. Biol Trace Elem Res. 2008;122:1–18.
18. Abou-Seif MA, Youssef A. Evaluation of some biochemical changes
in diabetic patients. Clin Chim Acta. 2004;346:161–70.
19. Ekmekcioglu C, Prohaska C, Pomazal K, et al. Concentrations of
seven trace elements in different hematological matrices in patients
with type 2 diabetes as compared to healthy controls. Biol TraceElem
Res. 2001;79:205–19.
20. Davies S, Mclaren Howard J, Hunnisett A, et al. Age-related decreases
in chromium levels in 51,665 hair, sweat and serum samples from 40,
872 patients—implications for the prevention of cardiovascular disease
and type II diabetes mellitus. Metabolism. 1997;46:469–73.
21. Cunningham JJ. Micronutrients as nutriceutical interventions in dia-
betes mellitus. J Am Coll Nutr. 1998;17:7–10.
22. Bloomberg RD, Fleishman A, Nalle JE, et al. Nutritional deficiencies
following bariatric surgery: what have we learned? Obes Surg.
2005;15:145–54.
23. Campbell AP. Diabetes and dietary supplements. Clin Diabetes.
2010;28:35–9.
24. Evans GW, Bowman TD. Chromium picolinate increases
membrane fluidity and rate of insulin internalization. J Inorg
Biochem. 1992;46:243–50.
OBES SURG (2014) 24:771–776 775
25. Vincent JB. Mechanisms of chromium action: low-molecular-weight
chromium binding substance. J Am Coll Nutr. 1999;18:6–12.
26. Broadhurst CL, Domenico P. Clinical studies on chromium picolinate
supplementation in diabetes mellitus—a review. Diabetes Technol
Ther. 2006;8:677–87.
27. Balk EM, Tatsioni A, Lichtenstein AH, et al. Effect of chro-
mium supplementation on glucose metabolism and lipids: a
systematic review of randomized controlled trials. Diabetes
Care. 2007;30(8):2154–63.
28. Wang ZQ, Cefalu WT. Current concepts about chromium supple-
mentation in type 2 diabetes and insulin resistance. Curr Diab Rep.
2010;10(2):145–51.
29. Sharma S, Agrawal RP, Choudhary M, et al. Beneficial effect of
chromium supplementation on glucose, HbA1C and lipid variables in
individuals with newly onset type-2 diabetes. J Trace Elem Med Biol.
2011;25:149–53.
30. Król E, Krejpcio Z, Byks H, et al. Effects of chromium brewer's yeast
supplementation on body mass, blood carbohydrates, and lipids and
minerals in type 2 diabetic patients. Biol Trace Elem Res.
2011;143(2):726–37.
31. Althuis MD, Jordan NE, Ludington EA, et al. Glucose and insulin
responses to dietary chromium supplements: a meta-analysis. Am J
Clin Nutr. 2002;76:148–55.
32. Iqbal N, Cardillo S, Volger S, et al. Chromium picolinate does not
improve key features of metabolic syndrome in obese nondiabetic
adults. Metab Syndr Relat Disord. 2009;7(2):143–50.
33. Yazaki Y, Faridi Z, Ma Y, et al. A pilot study of chromium picolinate
for weight loss. J Altern Complem Med. 2010;16(3):291–9.
34. Ali A, Ma Y, Reynolds J, et al. Chromium effects on glucose
tolerance and insulin sensitivity in persons at risk for diabetes
mellitus. Endocr Pract. 2011;17(1):16–25.
35. Alissa EM, Bahjri SM, Ahmed WH, et al. Chromium status and
glucose tolerance in Saudi men with and without coronary artery
disease. Biol Trace Elem Res. 2009;131:215–28.
36. Rukgauer M, Zeyfang A. Chromium determinations in blood cells:
clinical relevance demonstrated in patients with diabetes mellitus
type 2. Biol Trace Elem Res. 2002;86(3):193–202.
37. Krzysik M, Grajeta H, Preschaa A, et al. Effect of cellulose, pectin
and chromium (III) on lipid and carbohydrate metabolism in rats. J
Trace Elem Med Biol. 2011;25:97–102.
38. Chen G, Liu P, Pattar GR, et al. Chromium activates glucose trans-
porter 4 trafficking and enhances insulin-stimulated glucose transport
in 3T3-L1 adipocytes via a cholesterol dependent mechanism. Mol
Endocrinol. 2006;20:857–70.
39. Ginsberg HN. Insulin resistance and cardiovascular disease. J Clin
Invest. 2000;106:453–8.
40. Aasheim ET, Bjorkman S, Sovik TT, et al. Vitamin status after
bariatric surgery: a randomized study of gastric bypass and duodenal
switch. Am J Clin Nutr. 2009;90:15–22.
41. Ernst B, Thurnheer M, Schmid SM, et al. Evidence for the necessity
to systematically assess micronutrient status prior to bariatric surgery.
Obes Surg. 2009;19:66–73.
776 OBES SURG (2014) 24:771–776